FACTORES QUE AFECTAN A LA

COMPETENCIA ENTRE EL GALÁPAGO

L E P R O S O ( M a u r e m y s l e p r o s a )

Y E L I N T R O D U C I D O G A L Á P A G O

DE FLORIDA (Trachemys scripta )

N u r i a P o l o C a v i a

T E S I S D O C T O R A L

 

FACTORES QUE AFECTAN A LA

COMPETENCIA ENTRE EL GALÁPAGO

LEPROSO (Mauremys leprosa)

Y EL INTRODUCIDO GALÁPAGO

DE FLORIDA (Trachemys scripta)

Nuria Polo Cavia

TESIS DOCTORAL

Madrid 2009

La presente tesis ha sido realizada en el Departamento de Ecología Evolutiva del Museo Nacional de Ciencias Naturales (Consejo Superior de Investigaciones Científicas), Madrid, España. Diversos proyectos financiados por el antiguo Ministerio de Educación y Ciencia y por el actual Ministerio de Ciencia e Innovación, así como una beca predoctoral para la Estación Biológica de El Ventorrillo (CSIC) y una beca de posgrado para la Formación del Profesorado Universitario (MEC) han permitido el desarrollo de las investigaciones. Todos los experimentos cumplieron con las leyes estatales y de las Comunidades Autónomas donde fueron llevados a cabo.

Ilustraciones: Nuria Polo Cavia

Foto de portada: Mauremys leprosa. Nuria Polo Cavia

 

UNIVERSIDAD AUTÓNOMA DE MADRID

FACULTAD DE CIENCIAS

Departamento de Biología

FACTORES QUE AFECTAN A LA COMPETENCIA ENTRE EL GALÁPAGO LEPROSO (Mauremys leprosa)

Y EL INTRODUCIDO GALÁPAGO DE FLORIDA (Trachemys scripta)

Memoria presentada por Nuria Polo Cavia para optar al Grado

de Doctor por la Universidad Autónoma de Madrid,

bajo la dirección del Dr. José Martín Rueda y de la Dra. Pilar López Martínez, y la tutela académica del Dr. Francisco Javier de Miguel Águeda

Madrid, octubre de 2009

Nuria Polo Cavia

Vº Bº José Martín Rueda

Vº Bº Pilar López Martínez

Vº Bº Fº Javier de Miguel Águeda

Nuria Polo Cavia

Departamento de Biología Facultad de Ciencias Universidad Autónoma de Madrid Ciudad Universitaria de Cantoblanco 28049 Madrid, Spain nuria.polo@uam.es

José Martín Rueda

Departamento de Ecología Evolutiva Museo Nacional de ciencias Naturales, CSIC José Gutiérrez Abascal, 2 28006 Madrid, Spain jose.martin@mncn.csic.es

Pilar López Martínez

Departamento de Ecología Evolutiva Museo Nacional de ciencias Naturales, CSIC José Gutiérrez Abascal, 2 28006 Madrid, Spain pilar.lopez@mncn.csic.es

Fº Javier de Miguel Águeda

Departamento de Biología Facultad de Ciencias Universidad Autónoma de Madrid Ciudad Universitaria de Cantoblanco 28049 Madrid, Spain javier.demiguel@uam.es

A mis padres

Página siguiente

Un galápago de Florida se aproxima con determinación al tronco sobre el que descansan tres galápagos leprosos

 

♥♥ ♦♦ ♣♣ ♠♠

The true mystery of the world is the visible, not the invisible.

—OSCAR WILDE, 1890

 

CONTENIDOS Agradecimientos….………………………………………………………...

Introducción general………………………………………………..….…..

Las invasiones biológicas……………………………………..……

El galápago leproso…………………………………..…………….

El galápago de Florida………………………………………...........

Interacciones competitivas entre galápagos nativos e invasores....

Justificación y objetivos.……………………….…………………..

Procedimiento…………..………………………………..………...

Capítulos 1. Diferencias interespecíficas en las respuestas quimiosensoriales

de galápagos: consecuencias en la competencia entre especies nativas e invasoras…………………………….…………………...

Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species……………………….……...……...…

2. Interacciones agresivas durante la alimentación entre especies nativas e invasoras de galápagos…………………….……………..

Aggressive interactions during feeding between native and invasive freshwater turtles………………………………………...

3. Interacciones competitivas durante la actividad de asoleamiento entre especies nativas e invasoras de galápagos……………..….....

Competitive interactions during basking between native and invasive freshwater turtle species…………………………………

4. Las diferencias interespecíficas en las tasas de intercambio de calor pueden afectar a la competencia entre galápagos introducidos y nativos……………………………………………..

Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles……………………………………………………………….

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5. Relación entre el estado nutricional y los requerimientos de asoleamiento de galápagos nativos e invasores……..……………..

Feeding status and basking requirements of freshwater turtles in an invasion context………………………………………….……..

6. Efectos de la temperatura corporal en la respuesta de ‘giro’ de galápagos nativos e invasores: consecuencias en la competencia………………………………………..……………....

Effects of body temperature on righting performance of native and invasive freshwater turtles: consequences for competition…….…………….……………………….……………

7. Las diferencias interespecíficas en las respuestas al riesgo de depredación pueden conferir ventajas competitivas a las especies invasoras de galápagos……………………………….…………….

Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species………………………………………………………………

8. La incapacidad de los renacuajos para reconocer depredadores introducidos puede conferir ventajas competitivas a los galápagos invasores…….………….……………………………….

Failed predator-recognition by tadpole prey may confer competitive advantages to invasive turtle predators…………………………………………….……………...

Síntesis de resultados y discusión………………………….….……………

Conclusiones………………………………………………………………..

Referencias………………………………………………………………….

Anexo…………………………………………………………………..……

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Agradecimientos

Recuerdo con claridad el día en que llegué al Museo para comenzar mi tesis doctoral. Acababan de concederme una beca predoctoral, y este acontecimiento marcaría el inicio de una nueva etapa en mi vida. Sin embargo, todo había empezado mucho antes, cuando ajena por completo al mundo de la ciencia, comenzó a despertarse en mí el interés por la biología evolutiva. Las preguntas más profundas sobre la vida, los organismos y sus comportamientos tenían por fin una respuesta coherente con aquello que observaba. Durante los últimos años de licenciatura, y más tarde, a lo largo del doctorado, empecé a comprender los mecanismos que explican el devenir de la historia natural, y a llamar a los procesos por su nombre. Desde entonces, son muchas las personas que he encontrado en el camino con las que he podido compartir mi pasión por comprender el verdadero misterio de la vida. A ellas les debo en parte lo que soy, y desde luego, la consecución de esta tesis.

En primer lugar, quiero expresar mi agradecimiento a mis directores, José Martín y Pilar López, dos personas fundamentales que me han apoyado desde el principio, guiando cada uno de mis pasos. A ellos les debo su confianza, su paciencia conmigo, y el perdonármelo todo. Su continua orientación y dedicación han hecho posible la realización de esta tesis.

Javier de Miguel ha sido un amigo incondicional durante todos estos años. Desde que firmó mi tutela académica no he parado de importunarle (ya en aquella ocasión le interrumpí en mitad de una reunión de departamento). Sin embargo, aceptó con resignación mi marcha al Museo, recibiéndome pacientemente cada vez que necesitaba resolver algún trámite universitario y participando en cada uno de mis logros. De vuelta en la Autónoma, tengo

Ilustración | Galápagos exóticos se asolean sobre un tronco flotante

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que agradecerle el compartir su despacho y sus jornadas conmigo, su meticulosa revisión de erratas, y el aguantarme sin volverse loco durante la edición y el maquetado de esta tesis.

A José Luis Rubio le debo muchos de mis conocimientos evolutivos y el haberme descubierto el camino de la ciencia en el momento más oportuno, lo bueno y lo malo de este mundo, las puertas a las que llamar y aquéllas de las que huir. A Vicente Polo, el resolver mis problemas matemáticos al aplicar la física a la biología, y a Santiago Merino, el ayudarme a discriminar los diferentes tipos de leucocitos en los frotis sanguíneos (aunque ese trabajo no aparezca reflejado en estas páginas). Alfonso Marzal me permitió trabajar con total libertad en sus dehesas de Olivenza. Su generosidad y la de los suyos facilitaron enormemente el trabajo de campo de esta tesis. En California, el Dr. Tag Engstrom me abrió las puertas de su laboratorio, dándome la oportunidad de ampliar mis perspectivas investigadoras. Les estaré por siempre agradecida, a él y a todas las personas que hicieron de aquélla una experiencia realmente fascinante. Gracias también a Luisma Carrascal, por atender alguna que otra duda estadística, y a Luis Miguel Bautista y a Antonio García-Valdecasas, por animarme con mi futuro posdoctoral.

A mis compañeros y amigos del Museo, Carlos, Adega y Marianne, les estoy especialmente agradecida por todos los buenos momentos que hemos compartido. Con vosotros me he reído tanto que habéis convertido el trabajo de cada día en un verdadero placer. Gracias por apuntarme datos en El Ventorrillo (a veces dos manos no son suficientes) y por cuidar de mis galápagos en los momentos de ausencia. A Carlos le debo el actualizarme de continuo “los últimos hallazgos científicos”, las conversaciones –largas y acaloradas- sobre ciencia en las sobremesas de El Ventorrillo, el hacerme reír con cualquier cosa y el aguantar mi mala costumbre de cuestionarlo todo (a veces con razón, ¿eh?). A Adega, su extraordinaria colaboración en el campo (¿recuerdas cuando cogimos el primer Mauremys en Colmenar?), el preocuparse siempre por mí (sobre todo en Badajoz), las confidencias y esa extraña confianza que existe entre las dos (sabes que puedes contar conmigo, nena). A Marianne, el soportar mis “gloriosas” frases en francés y el sorprenderme con su divertida forma de ver la vida. Gracias también a mis compañeros de la “11 11” (y alrededores) y al resto de personal del Museo, que hicieron más entretenidas las jornadas de trabajo y facilitaron los trámites, las gestiones y el papeleo.

A todas las personas con las que coincidí en El Ventorrillo (becarios, voluntarios e investigadores), gracias por todos los ratos estupendos que hemos echado en la pradera y en los bares de Cercedilla y Navacerrada. Gracias, en especial, a Nino, una persona encantadora, voluntariosa y diligente, siempre presto a ayudarnos a todos. Sin él, El Ventorrillo no sería el mismo lugar.

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Quiero agradecer también a mis compañeros de la Unidad de Zoología de la Universidad Autónoma de Madrid el darme la oportunidad de trabajar con ellos, de disfrutar de la docencia, y por qué no, de terminar esta tesis con un poco más de tiempo y tranquilidad. Isabel, Raquel y Lucía son, además de Javier, las personas con las que he compartido más tiempo, excursiones y buenas conversaciones durante las comidas y los cafés, estrechando nuestra amistad en el día a día.

A los organismos GREFA y EXOTARIUM, que cedieron voluntariamente ejemplares de galápago para los experimentos de esta tesis, y al MNCN y a la Estación Biológica de El Ventorrillo, que pusieron a mi disposición los medios necesarios para que fuera posible llevar a cabo este proyecto.

Por último, mi más sincero agradecimiento a mi familia y amigos, por animarme siempre y por comprender mis “perdonadme, estoy muy liada…”, y muy en particular a mis padres, Arturo y Esperanza, quienes han sido un verdadero estímulo para mi trabajo, demostrándome siempre su apoyo incondicional y su confianza férrea.

Nuria Polo Cavia

Madrid, octubre de 2009

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— INTRODUCCIÓN GENERAL —

Las invasiones biológicas

a introducción de seres vivos fuera de su área de distribución natural representa, tras la pérdida del hábitat, la segunda causa de amenaza a la biodiversidad global (Wilcove et al. 1998; Gurevitch y Padilla 2004). Hoy

en día, gran cantidad de especies son transportadas diariamente por el ser humano, de forma accidental o intencionada, estableciéndose en zonas geográficas que no forman parte de sus rangos históricos, alterando la estructura y el funcionamiento de los ecosistemas y desplazando especies nativas de sus nichos ecológicos (Herbold y Moyle 1986; Williamson 1996). Este proceso es conocido en biología de la conservación como invasión biológica. En el último siglo, los fenómenos de invasión se han multiplicado sobremanera debido al mayor desarrollo y a la creciente intervención humana en el ecosistema. Así, una especie que por medios naturales necesitase del orden de miles de años para alcanzar una nueva región biogeográfica, hoy podría lograrlo en tan sólo un día. BARRERAS GEOGRÁFICAS E INTRODUCCIONES HISTÓRICAS El aislamiento geográfico constituye una de las principales vías de especiación natural (i.e., especiación vicariante, Mayr 1963). Barreras físicas tales como océanos, valles, cadenas montañosas o placas de hielo representan límites que impiden el desplazamiento de los individuos entre poblaciones de una misma especie. Con el tiempo, las poblaciones que se mantienen separadas tienden a divergir entre sí empujadas por las fuerzas de la deriva génica y la selección natural, dando lugar a especies únicas bien diferenciadas. En una etapa posterior, las barreras geográficas que motivaron la especiación pueden ser eliminadas de forma natural por eventos climatológicos o alteraciones geológicas, permitiendo la dispersión de estas nuevas especies y la expansión de sus rangos. Por ejemplo, durante el Mioceno, cuando el istmo de Panamá irrumpió la vía acuática de los trópicos americanos conectando Norte y Sur América, los mamíferos norteamericanos migraron hacia el sur, mientras que las aves y las plantas de los bosques lluviosos suramericanos expandieron sus rangos de distribución hacia el norte (Marshall et al. 1982). Estas expansiones naturales,

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inusualmente rápidas, han sido estudiadas por ecólogos y paleontólogos, considerándose parte de la historia biológica de La Tierra.

Sin embargo, desde que el hombre ha tenido capacidad de dispersión entre los continentes, las migraciones humanas han abierto brechas en las barreras geográficas, interrumpiendo el aislamiento natural y permitiendo el flujo de especies entre ámbitos muy alejados espacialmente. Muchos archipiélagos del Mediterráneo y la Polinesia fueron poblados en tiempos prehistóricos antes del Neolítico –en algunos casos incluso durante el Paleolítico-, manteniéndose la comunicación entre las islas (Schüle 2000; Matisoo-Smith 2002; Hurles et al. 2003; Matisoo-Smith y Robins 2004). En la Antigüedad y la Edad Media, la expansión de la agricultura y la navegación favorecieron el transporte de materiales y la colonización, estableciéndose un flujo principal de Oriente hacia Occidente. Pero fue tras las primeras expediciones transoceánicas del siglo XV, y en especial tras el descubrimiento de América, cuando se abrieron las grandes rutas comerciales marítimas que propiciaron la conexión intercontinental a gran escala y la aceleración en la transferencia de organismos. Desde entonces, millares de especies han sido regularmente transportadas junto con las personas, los animales domésticos y las importaciones (Crosby 1986). Al igual que los grupos de mamíferos, aves y plantas que expandieron sus rangos geográficos durante el gran intercambio biótico americano (Marshall et al. 1982), algunas de estas especies se establecieron en territorios que previamente se encontraban fuera de su alcance, colonizando con éxito los nuevos ambientes. Pero esta vez, en cambio, los colonizadores extendieron su distribución con la ayuda del hombre. INTRODUCCIONES MODERNAS El protagonismo que el descubrimiento y la colonización del Nuevo Mundo tuvieron en la introducción de nuevas especies en el viejo continente es extremo, hasta el punto de que, en Europa, las especies introducidas se clasifican en arqueófitos (introducidas antes de 1500) y neófitos (introducidas después de 1500). A raíz de la conquista de América, las potencias europeas impulsaron enormemente sus viajes de exploración, a la par que la aclimatación de especies exóticas se convirtió en una línea prioritaria tanto para naturalistas e investigadores como para los propios colonos y las soberanías, que introducían cultivos y otras especies de utilidad en el Nuevo y en el Viejo Mundo. Así, además de los trasvases accidentales, empezaron a producirse intercambios masivos intencionados por conveniencia del ser humano. A mediados del siglo XIX, en el máximo apogeo de la revolución industrial y del colonialismo moderno, proliferaron los jardines botánicos y las sociedades de aclimatación en toda Europa y en las colonias, cuya misión última era la introducción y

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aclimatación de animales y plantas para el abastecimiento humano y el mayor bienestar económico (Lever 1992; Dunlap 1997). Ya en el último siglo, el desarrollo económico, el progreso tecnológico y el avance de las comunicaciones han disparado el impacto del hombre sobre el medio natural, incrementando el número de vectores de introducción, y facilitando así la transferencia –intencional o involuntaria- de una mayor cantidad de especies y su posterior supervivencia en los nuevos territorios. VÍAS DE ENTRADA Al igual que la extinción de especies, las invasiones biológicas son un fenómeno natural. Numerosas especies son capaces de atravesar grandes distancias aprovechando los vientos favorables o las corrientes oceánicas (Bush 1991; Mack y Lonsdale 2001; Mack 2004). En algunas ocasiones, incluso, las expansiones históricas han ocurrido en periodos de tiempo relativamente cortos (Vermeij 2005). No obstante, los ecólogos diferencian entre expansiones naturales y expansiones mediadas por el ser humano, al igual que distinguen las extinciones naturales de aquellas otras en las que existe algún tipo de intervención antrópica.

La principal diferencia entre los procesos de colonización naturales y las introducciones mediadas por el hombre radica en la magnitud de la velocidad y la escala geográfica a la que se producen ambos sucesos. Las tasas de invasión históricas han sido calculadas en islas oceánicas como Hawai o la isla de Gough, al sur del Atlántico. Al comparar estas tasas con los ritmos de introducción actuales, se encontró una aceleración asombrosa en el número de especies nuevas por unidad de tiempo que han alcanzado estos remotos lugares en el curso de la historia. La razón de tal incremento en las tasas de invasión es sin duda el profundo cambio que el hombre ha inducido en los vectores de transporte y en las vías de entrada de las especies exóticas, ampliándolas y diversificándolas con respecto a las disponibles en los procesos de colonización natural (ver Tabla 1, con diversos ejemplos de especies introducidas y sus respectivas vías de entrada).  

Las especies exóticas pueden constituir una fuente de recursos (alimenticios, medicinales, cinegéticos, silvícolas o experimentales), o ser de interés ornamental (jardinería, mascotas, etc.). En estos casos, su transporte se realiza deliberadamente, de forma legal o clandestina, con fines determinados. Estas introducciones se consideran por tanto intencionadas. Por otra parte, en las últimas décadas, la intensificación de los movimientos humanos, el comercio y las alteraciones topográficas del paisaje han contribuido a acrecentar el trasvase involuntario de numerosas especies. Este tipo de introducciones no intencionadas se produce de forma accidental, pero siempre a través de agentes antropogénicos. Así, por ejemplo, los vehículos, las embarcaciones y las aguas de

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Tabla 1 Diversos ejemplos de introducciones y vías de entrada de especies exóticas

Tipo Vía-Propósito Especie Fuente

Achillea millefolium, Rumex acetosella Mack 2003

Opuntia ficus-indica Capdevila-Argüelles y Zilletti 2006

Lates niloticus Goldschmidt et al. 1993; Ogutu-Ohwayo 1993

Capra hircus Genovesi 2005

Ovis aries Genovesi et al. 2009

Sus scrofa Vigne et al. 2003

Producción de alimento

Oryctolagus cuniculus Flux y Fullagar 1992

Fines medicinales

Hypericum perforatum Mack 2003

Pinus halepensis Lavi et al. 2005 Producción de madera Acacia spp., Robinia

pseudoacacia Capdevila-Argüelles y Zilletti 2006

Procesos industriales

Artemia franciscana Sorgeloos et al. 1986; Amat et al. 2005

Anas platyrhynchos Long 1981

Phasianidae Lockwood 1999

Ovis orientalis Pascal et al. 2003; Santiago-Moreno et al. 2004

Ammotragus lervia Casinello 2000; Serrano et al. 2002

Cervidae Lever 1985

Micropterus spp., Ictalurus spp.

Moyle 2002

Salvelinus fontinalis Elvira y Almodóvar 2001; Moyle 2002

Oncorhynchus mykiss Lever 1996; Elvira y Almodóvar 2001

Caza y pesca recreativa

Esox lucius, Micropterus salmoides, Perca fluviatilis, Silurus glanis, Stizostedion lucioperca

Elvira y Almodóvar 2001

Artemia franciscana Sorgeloos et al. 1986

Intencionadas

Alimentación de animales en producción Pueraria montana Miller y Edwards 1983

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Tabla 1 - Continuación 

Caulerpa taxifolia, Sargassum muticum Siguan 2004

Acacia spp., Eichhornia crassipes, Robinia pseudoacacia,

Capdevila-Argüelles y Zilletti 2006

Cyprinus carpio, Carassius auratus Elvira y Almodóvar 2001

Sturnus vulgaris Dunlap 1997

Ornamentación y paisajismo

Oxyura jamaicensis Capdevila-Argüelles y Zilletti 2006

Acacia spp. Gardner 2001; Ferrari y Wall 2004 Mejora del

suelo Casuarina spp., Leucaena leucocephala

Ferrari y Wall 2004

Freno de erosión

Acacia dealbata, Chloris gayana Sanz-Elorza et al. 2004

Estabilización dunar

Acacia melanoxylon, Carpobrotus edulis Sanz-Elorza et al. 2004

Euglandina rosea Cowie 1998, 2001

Triops newberry Su y Mulla 2002

Gambusia affinis Lever 1996

Gambusia holbrooki Elvira y Almodóvar 2001

Control de plagas

Herpestes javanicus Simberloff et al. 2000

Procambarus clarkii Gutiérrez-Yurrita et al. 1999

Declive y sustitución de especies nativas

Rutilus rutilus, Scardinius erythrophthalmus, Ameiurus melas, Lepomis gibbosus

Elvira y Almodóvar 2001

Tipo Vía Especie Fuente

Fungi Palm y Rossman 2004

Polychaeta Hendrix y Bohlen 2002 Asociación a sustrato

Rhynchophorus ferrugineus

Capdevila-Argüelles y Zilletti 2006

Ascidiella aspersa Carlton 1996

Hydroides spp. Galil 2001

Womersleyella setacea Boudouresque 2005

No intencionadas

Embarcaciones

Dreissena polymorpha Capdevila-Argüelles y Zilletti 2006

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Tabla 1 - Continuación 

Dreissena polymorpha Capdevila-Argüelles y Zilletti 2006

Rapana venosa Zenetos et al. 2003 Aguas de lastre

Callinectes sapidus Galil et al. 2002

Dreissena polymorpha Jiménez Mur 2001 Eliminación de barreras geográficas Migraciones lessepsianas Por 1978

Plasmodium relictum Warner 1968; Van Riper et al. 1986

Bothriocephalus acheilognathi

Salgado-Maldonado y Pineda-López 2003

Otros organismos como vectores

Miconia calvescens Medeiros et al. 1997

Aedes albopictus Eritja et al. 2005

Transporte de mercancías Linepithema humile Gómez y Espadaler 2004

Tipo Vía Especie Fuente

Caulerpa taxifolia Meinesz 1999

Cerion spp. Cowie y Robinson 2004

Cyprinodon diabolis Sigler y Sigler 1987

Acipenser baerii, Gobio gobio, Oncorhynchus kisutch, Ictalurus punctatus

Elvira y Almodóvar 2001

Mustela vison Bravo y Bueno 1999

Escapes de granjas, zoológicos, jardines botánicos o centros de investigación

Myocastor coipus Capdevila-Argüelles y Zilletti 2006

Caulerpa taxifolia Jousson et al. 2000 Desechos de jardinería Opuntia tunicata Escudero 2003

Trachemys scripta Pleguezuelos 2002

Liberación de mascotas

Myiopsitta monachus, Psittacula kramerii, Estrilda astrild, Amandava amandava

Martí y Del Moral 2003

Rana catesbeiana Pleguezuelos 2002

Procyon lotor Kahuala 1996 Abandono de explotaciones

Myocastor coipus Capdevila-Argüelles y Zilletti 2006

Negligencias

Liberaciones animalistas

Mustela vison Bravo y Bueno 1999; Hammershøj 2004

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lastre, o las propias personas, son susceptibles de transportar propágulos y semillas, larvas, parásitos u otros organismos. De forma similar, la apertura de canales ha permitido la entrada masiva de especies marinas originarias de unos mares a otros (como fue el caso del canal de Suez o del canal de Panamá). A estas dos formas principales de entrada hay que añadir las negligencias (escapes de granjas, desechos de jardinería, liberación de mascotas, etc.), que sin ser introducciones intencionadas (pues no se persigue el establecimiento de una población silvestre), suceden con conocimiento de causa por falta de concienciación o medidas de precaución. EL PROCESO DE INVASIÓN Toda invasión comienza con la recolección de un grupo de individuos (a veces incluso de un solo individuo), que es extraído de su rango original, transportado a un nuevo territorio y liberado en el medio natural. Estos individuos deben entonces ser capaces de establecerse como una población autónoma en su nuevo hábitat, produciéndose la extinción en otro caso. Tras el establecimiento, la población no nativa puede incrementar el número de individuos que la sustentan y expandir su rango geográfico, o bien, mantener sus efectivos y su distribución dentro de un margen restringido (Cuadro 1). En general, sólo cuando una población no nativa ha conseguido expandirse y aumentar su tamaño es capaz de ocasionar algún tipo de daño ecológico o económico, y por tanto, puede ser considerada “invasora” (ver Cuadro 2 para más información sobre la terminología utilizada en el contexto de las invasiones biológicas).

Aun cuando en la realidad estas etapas pueden confundirse, sobrepasar cada una de ellas requiere la superación de ciertas barreras ecológicas que pueden llegar a identificarse. Williamson (1996) fue uno de los primeros ecólogos en representar el fenómeno de invasión como la progresión de una especie nueva en un ecosistema a través de una serie de barreras. Uno de los puntos clave de este modelo es la comprobación de que la mayoría de las especies no logran transitar de una fase a otra del proceso de invasión. De acuerdo con las investigaciones de Williamson (1996), sólo entre el 5 y el 20 % de las especies no nativas consiguen alcanzar la siguiente fase, siendo el promedio del 10 % (patrón que Williamson denominó “regla de los 10”). Si bien se ha demostrado recientemente que este patrón no siempre se cumple (la identidad de la especie invasora, las características del ecosistema receptor y la frecuencia de las introducciones juegan un papel determinante), la aproximación de Williamson sugiere dos importantes presunciones. En primer lugar, la estructura anidada de las invasiones biológicas asegura que tan sólo una pequeña fracción del total de especies que son introducidas fuera de sus rangos naturales causará un impacto ecológico o económico. En segundo lugar, las barreras entre las fases de invasión

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Cualquier especie no nativa debe superar una serie de fases antes de ocasionar un impacto en el ecosistema (e.g., Kolar y Lodge 2001; Fig. 1). El conjunto de estas fases es lo que se ha dado en denominar proceso de invasión. Diversos filtros actúan en las diferentes etapas del proceso, evitando que las especies trasvasadas acaben invariablemente por convertirse en especies invasoras ■

 

Figura 1 Fases discretas del proceso de invasión y alternativas para cada fase. Fuente: modificado de Lockwood 2007

Cuadro 1 Modelo de Kolar y Lodge (2001), esquematizando las fases del proceso de invasión son extraordinarias. Surge entonces una pregunta: ¿por qué unas especies son capaces de rebasar exitosamente estas barreras mientras que otras no logran culminar el proceso de invasión? DE LA INTRODUCCIÓN A LA INVASIÓN: DETERMINANTES DEL ÉXITO Como se ha visto, las invasiones biológicas constituyen sólo uno de los posibles resultados de un proceso de fases anidadas que comienza cuando los organismos son transportados desde sus hábitats originales a nuevas áreas locales. Así, las consecuencias últimas de una introducción dependen tanto de la capacidad de la especie introducida para adaptarse a un hábitat extraño como de la capacidad de las especies nativas para acomodarse o resistir la presencia del invasor (Lockwood 2007). En otras palabras, son tanto las características del invasor como las propiedades de la comunidad que lo acoge las que determinan el éxito o el fracaso de la invasión. Diversos experimentos en laboratorio han demostrado que el orden de introducción de las especies en un ecosistema

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La terminología utilizada en el marco de las invasiones biológicas puede variar ligeramente de unos autores a otros (Tablas 2 y 3). Esta variabilidad en el criterio de los autores, unida a la existencia de términos sinónimos, ha generado cierta confusión semántica.

En general, los términos “introducida”, “exótica”, “alóctona”, “foránea” o “no nativa” (“alien” en inglés) hacen referencia a una especie originaria de otra región y pueden considerarse sinónimos (Vilà et al. 2008). En función de la fase que alcanzan en el proceso de invasión, las especies trasvasadas pueden calificarse como “transitorias” o “casuales”, si no han sido liberadas en el medio; “adventicias”, si se ha producido su liberación (o escape), pero no llegan a establecer poblaciones autosustentables en sus nuevos territorios, sino que su persistencia depende de la proximidad a zonas antropizadas y/o de la entrada continuada de nuevos individuos; “naturalizadas” o “establecidas”, si son capaces de mantener sus poblaciones de forma totalmente autónoma; o “invasoras”, en el caso de que se expandan a gran velocidad lejos del foco de introducción. Cuando las especies invasoras

Tabla 2 Términos más comunes relacionados con las especies invasoras. Fuente: modificado de Vilà et al. 2008

Especies que ocupan su área de distribución original Nativas Autóctonas Indígenas

Especies que se encuentran fuera de su área de distribución natural

Introducidas Exóticas Foráneas Alóctonas No nativas Importadas

Especies introducidas que se extienden de forma autónoma, pero dependientes de sistemas humanizados, o sin capacidad para perdurar en los territorios ocupados

Adventicias Subespontáneas Casuales

Especies introducidas que se extienden a ecosistemas naturales, donde tienen capacidad de mantener poblaciones de forma autónoma

Naturalizadas Establecidas

Especies naturalizadas con gran capacidad de propagación, en número de individuos y/o en distancia

Invasoras

Especies naturalizadas con gran capacidad de propagación, capaces de alterar sustancialmente los ecosistemas nativos y/o ocasionar impactos económicos

Transformadoras Pestes Plagas

Cuadro 2 Terminología de las invasiones biológicas

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generan un impacto ambiental o socioeconómico, se utilizan términos tales como especies “transformadoras”, “pestes” o “plagas”, en función de la magnitud del daño, rigiéndose por un criterio antropocéntrico. Otros autores prefieren considerar como invasoras solamente a aquellas especies que han alterado el medio natural, desplazando especies nativas, provocando cambios en los ciclos de nutrientes, daños en las infraestructuras, etc. Sin embargo, el impacto real de una especie introducida es en muchas ocasiones desconocido, por lo que se recomienda utilizar conjuntamente el criterio de expansión (en abundancia o distribución) de sus poblaciones (Richardson et al. 2000; Colautti y MacIsaac 2004). En otros casos, se ha dado en llamar invasoras a determinadas especies nativas que han expandido sobremanera sus rangos tras beneficiarse de una variación en el ambiente, en lugar de hablar de especies “colonizadoras” u “oportunistas” ■

Tabla 3 Listado de términos recopilados por Lockwood et al. (2007) a partir de varios autores, utilizados para designar a las especies no nativas en relación a las fases del proceso de invasión (transporte, establecimiento, expansión e impacto). Es interesante observar que algunos de estos términos han sido aplicados también a las especies nativas. Fuente: modificado de Lockwood et al. 2007 (basado en Colautti y MacIsaac 2004)

FASE DE INVASIÓN

NATIVAS NO NATIVAS Transp. Establ. Expans. Impacto Adventicias Alien Casuales Colonizadoras Criptogénicas Escapadas Establecidas Exóticas Foráneas Importadas Invasoras Naturalizadas No indígenas Nocivas Perturbadoras Peste Transformadoras Transitorias Translocadas Transportadas Trasplantadas

Cuadro 2 - Continuación

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determina las relaciones entre especies y la estructura final de la comunidad (Drake 1991; Price y Morin 2004). En este sentido, las especies nativas, así como las no nativas previamente establecidas, pueden facilitar u obstaculizar el establecimiento de nuevas especies exóticas, a través de interacciones bióticas tales como la competencia, la depredación o el mutualismo, dando lugar a asociaciones tanto positivas como negativas entre las especies recién introducidas y las residentes. Así, por ejemplo, una especie exótica podría recalar en un hábitat con bajos niveles de competencia y/o carente de depredadores (o que albergue a un depredador de sus depredadores habituales), o establecer una relación simbionte con una o más especies nativas que favorezca su rápida proliferación (Hoopes 1999; Simberloff y Von Holle 1999; Richardson et al. 2000; Facelly y Temby 2002; Kimball y Schiffman 2003; Adam et al 2003). Por el contrario, esta nueva especie podría enfrentarse con eficaces competidores y/o depredadores, o con la ausencia de un mutualista obligado, lo que contendría su expansión en el nuevo hábitat (Nadel et al. 1992; Simberloff et al 2002; Hunt y Behrens Yamada 2003; Green et al. 2004).

En general, las especies introducidas que acaban por convertirse en invasoras suelen presentar una amplia valencia ecológica (capacidad de adaptación a diversos hábitats), basan su ecología reproductiva en la estrategia de la r (amplia procreación con escasa dedicación a las crías), tienden a asociarse con hábitats antrópicos o situaciones de comensalismo con el hombre, y es común que su origen se encuentre en continentes con faunas diversas y saturadas (Sax y Brown 2000; Kolar y Lodge 2001). Por otro lado, un alto grado modificaciones de origen antrópico en el medio, y la ausencia de enemigos de las especies introducidas entre la fauna nativa, son características propias de las regiones que padecen invasiones (Fox y Fox 1986; Smallwood 1994; Ewell 1999; Sax y Brown 2000).

Charles Elton (Cuadro 3) propuso en 1958 que las áreas con mayor diversidad de especies indígenas presentan una mayor resistencia a las invasiones biológicas que aquellas que albergan un menor número de especies nativas (Elton 1958, The ecology of invasions by animals and plants). Esta hipótesis se halla en consonancia con los modelos clásicos de competencia, que sugieren que un gran número de competidores genera un intenso uso del espacio y los recursos, dejando pocos nichos vacíos que puedan ser aprovechados por nuevas especies. Desde un punto de vista ecológico, es también razonable contemplar los puntos calientes de biodiversidad como espacios menos proclives a sufrir invasiones (Kennedy et al. 2002). Sin embargo, la presunción de Elton encierra una importante paradoja: los factores ecológicos que promueven una mayor riqueza de especies nativas deberían favorecer también la diversidad de especies no nativas. La solución a este dilema no es sencilla. Varios experimentos a escala local (Tilman 1999; Kennedy et al. 2002) y algunos modelos matemáticos (e.g., Case 1990) apoyan la hipótesis de Elton, mientras

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Cuadro 3 que un gran número de estudios observacionales a gran escala y la mayoría de los modelos matemáticos sostienen la relación contraria (Lonsdale 1999; Stohlgren et al. 1999, 2003). Por ejemplo, comparando el número de especies no nativas establecidas en un amplio grupo de regiones, Lonsdale (1999) encontró tasas de establecimiento de especies exóticas mayores en las islas que en las regiones continentales, y mayores en el Nuevo Mundo comparadas con las del viejo continente. Lonsdale atribuyó estos resultados a la existencia de un patrón geográfico subyacente. Pero su modelo sugería, además, que la riqueza de especies nativas se halla positivamente correlacionada con la riqueza de especies no nativas, con independencia de la ubicación o grado de protección del área considerada. La razón de esta aparente contradicción entre los patrones obtenidos a gran escala y los resultados de los experimentos a pequeña escala descansa probablemente en la importancia relativa de las relaciones interespecíficas a las diferentes escalas espaciales (Huston 1999; Davies et al. 2005; Lockwood 2007). Mientras que a escala local el establecimiento de nuevas especies en la comunidad se encuentra principalmente limitado por factores intrínsecos como la competencia, a gran escala las interacciones bióticas pierden importancia, en contraposición a las fuerzas extrínsecas que determinan la diversidad de especies en la comunidad, tales como la producción primaria o la heterogeneidad de los recursos. IMPACTO ECOLÓGICO La introducción de especies exóticas constituye, tras la pérdida del hábitat, la segunda causa de amenaza a la biodiversidad global (Wilcove et al. 1998; Gurevitch y Padilla 2004). En numerosas ocasiones, las especies invasoras han alterado comunidades terrestres y acuáticas, desviando flujos de energía y desplazando especies nativas de sus nichos ecológicos (Herbold y Moyle 1986;

Charles Sutherland Elton (1900-1991) —Biólogo y naturalista inglés nacido en Manchester, se graduó en zoología por la Universidad de Oxford en 1922. Fue uno de los primeros científicos en estudiar los animales en su medio natural, desarrollando los conceptos de cadena alimentaria y nicho ecológico, y estableciendo así los principios de la ecología moderna. Su obra, The ecology of invasions by animals and plants, escrita en 1958, pocos años antes de retirarse de su cargo en la Universidad de Oxford, significó la consolidación de la ecología de las invasiones como una disciplina nueva y diferenciada ■

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Williamson 1996). Los efectos de estas introducciones son generalmente impredecibles (a no ser que la demografía, el uso de los recursos y las relaciones bióticas de las especies hayan sido cuidadosamente investigados), pero procesos tales como la contaminación genética, la depredación, la transmisión de patógenos y/o la competencia entre especies nativas e invasoras aparecen con frecuencia a consecuencia de este tipo de alteraciones (Dodd y Seigel 1991; Shigesada y Kawasaki 1997; Butterfield et al. 1997; Manchester y Bullock 2000; Mack et al. 2000; Lockwood et al. 2007).

A nivel genético, las especies exóticas pueden afectar a la integridad genética de las especies indígenas, vía hibridación o introgresión (Krueger y May 1991). Los cruzamientos entre especies nativas e invasoras pueden generar descendencia estéril, lo que supone una reducción en la reproducción de los individuos nativos debido al desperdicio de gametos (Rhymer y Simberloff 1996), o fértil, en cuyo caso los híbridos pueden constituir un nuevo genotipo invasor (Anttila et al. 1998; Ayres et al. 2004). Además, la descendencia fértil puede hibridar con las especies parentales, dando lugar a la introgresión y al flujo génico entre especies, pudiendo conducir incluso a la extinción del genotipo nativo (Dowling y Childs 1992; Rhymer et al. 1994).

Los impactos a nivel individual comprometen la supervivencia y el éxito reproductor de los individuos. Producto de estos impactos son los cambios en la morfología, los patrones de comportamiento y/o la demografía de las poblaciones nativas a consecuencia de la introducción de depredadores, competidores o transmisores de enfermedades (Parker et al. 1999; Mattila y Otis 2003; Orrock y Danielson 2004; Marra et al 2004). Así, los impactos ocasionados sobre los individuos acaban por afectar a la estructura y distribución de las poblaciones, cuyas densidades pueden verse fuertemente reducidas (Cree et al. 1995; Lesica y Shelly 1996; Pell y Tiedemann 1997). En casos de especies raras o vulnerables, la especie nativa puede ser empujada a la extinción si los efectos negativos se producen sobre su rango completo de distribución, o si persisten durante el tiempo suficiente. No obstante, la extinción es la forma más extrema de impacto a nivel poblacional.

Los impactos poblacionales generalizados sobre varias especies nativas pueden traducirse en cambios sustanciales a nivel de la comunidad. Los mamíferos herbívoros domésticos (i.e., Capra hircus, Ovis aries, Equus caballus, Sus domestica, Oryctolagus cuniculus, entre otros) se encuentran entre las especies causantes de las mayores transformaciones acaecidas en las comunidades nativas, especialmente en ecosistemas insulares (Courchamp et al. 2003). El impacto de estos herbívoros introducidos se concentra en la base de la cadena trófica, afectando en consecuencia a una gran cantidad de especies. La presencia de invasores conduce por lo general a una “cascada” de alteraciones en la estructura y composición de la comunidad (Porter y Savignano 1990; Allen et

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al. 2001; Morrison 2002; Ness y Bronstein 2004; Orrock y Danielson 2004; Smith et al. 2004; Lockwood et al. 2007 realiza una completa revisión de los efectos derivados de la introducción de la hormiga Solenopsis invicta en el sureste de los Estados Unidos). En algunos casos, las especies invasoras han ocasionado impactos de tal magnitud que han llegado a provocar la extinción en masa de un sinfín de especies nativas (la introducción de la perca del Nilo, Lates niloticus, en el Lago Victoria a mediados del siglo XX constituye uno de los ejemplos clásicos de extinción en masa a consecuencia de las invasiones biológicas. La entrada de este depredador en la comunidad supuso la desaparición de aproximadamente 200 especies de peces nativos; Witte et al. 2000). Estas extinciones han ocurrido con mayor frecuencia en ecosistemas evolutivamente aislados, en los que la radiación adaptativa se ha producido en ausencia de grandes depredadores o herbívoros.

Los cambios en el comportamiento de los individuos, la dinámica poblacional y la estructura de las comunidades pueden finalmente generar impactos a nivel de ecosistemas, transformando el medio físico o creando nuevos regímenes de perturbación. Así por ejemplo, las especies invasoras son capaces de alterar la salinidad de los hábitats riparios (Di Tomaso 1998), los ciclos de nutrientes (Ehrenfeld 2003) y la disponibilidad de los recursos (Vitousek 1990; Gardner 1995; Simon y Townsend 2003). Un caso particular es el del mejillón cebra, Dreissena polymorpha, capaz de modificar los niveles de nitrógeno, fósforo y carbono disponibles en el medio. Mediante el filtrado de cantidades ingentes de agua a través de su tracto digestivo, este invasor genera un incremento en la disponibilidad de nitrógeno y fósforo en la columna de agua, a la vez que el carbono es desplazado hacia el fondo (Gardner 1995). De forma similar, las plantas fijadoras de nitrógeno establecidas fuera de sus rangos pueden alterar la disponibilidad de los recursos, mediando en la competencia entre la flora nativa y la invasora, afectando a los procesos de sucesión y transformando los ecosistemas (Vitousek 1990).

Aun cuando la mayor parte de las invasiones biológicas va ligada a la pérdida de biodiversidad, numerosas áreas locales han experimentado un incremento en la riqueza de especies tras la introducción de especies exóticas (Sax et al. 2002; Sax y Gaines 2003). Sin embargo, el incremento y la reducción de la diversidad no se producen de manera uniforme en los distintos grupos taxonómicos. Las especies asociadas con los sistemas antrópicos son transportadas con mayor probabilidad fuera de sus hábitats originales, y sus posibilidades de supervivencia en los nuevos territorios son también mayores. En el otro extremo, las especies endémicas que han evolucionado en ausencia de competidores, depredadores o patógenos, o en ambientes ajenos a las perturbaciones humanas, son proclives a sufrir recesiones. Esta pérdida de especies endémicas y el aumento de las especies invasoras comporta un patrón bipolar emergente a gran

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escala: un gran grupo de especies que desaparecen frente a un grupo reducido de especies que prosperan a nivel global, haciéndose más y más numerosas (McKinney y Lockwood 1999). En consecuencia, unas pocas especies comienzan a estar presentes en casi todas las regiones del mundo, al tiempo que la fauna y la flora de los ecosistemas que han sido invadidos se vuelven cada vez más parecidas, especialmente entre aquellas regiones que comparten características climáticas. Este proceso, conocido como homogeneización biótica (McKinney y Lockwood 1999), avanza con sutileza, lo que dificulta en gran medida su detección.

SITUACIÓN ACTUAL DE LAS ESPECIES EXÓTICAS INVASORAS La preocupación por los problemas causados por las especies exóticas invasoras es bastante reciente, en comparación con otras amenazas ambientales como la contaminación, la erosión o la deforestación. En muchos países, la Administración y la opinión pública son aún indiferentes a la necesidad de prevención de las introducciones biológicas (De Klemm 1996). No obstante, el interés de las autoridades e instituciones hacia la naturaleza y los problemas ambientales se ha acrecentado en las últimas décadas. Este hecho, unido al incremento en la concienciación social, ha favorecido un cambio en el panorama de las invasiones biológicas, tanto a nivel de legislación, como en el número de estudios científicos y artículos de divulgación que se han publicado en los últimos años (Pleguezuelos 2002).

Así, las especies exóticas invasoras son actualmente una de las mayores preocupaciones ecológicas a nivel internacional, objeto de esfuerzos de numerosas instituciones protectoras de la biodiversidad. El papel de la Unión Internacional para la Conservación de la Naturaleza (UICN) es clave en la preservación de la fauna y de la flora nativas, evitando que se produzcan mayores daños en los ecosistemas. Recientemente, un proyecto de investigación en el que han participado más de 100 científicos europeos ha visto la luz en el marco de la Unión Europea. Más de 11.000 especies exóticas, sus impactos y consecuencias sobre el ambiente y la sociedad, han sido catalogados por DAISIE (Delivering Alien Invasive Species Inventory for Europe)1. Hasta el momento se conoce el impacto ecológico de 1.094 de estas especies (el 10 % del total), y 1.347 (aproximadamente el 13 % de las registradas) generan daños económicos (DAISIE Handbook of alien species in Europe 2009; Cuadro 4).

Es probable que muchas de las especies potencialmente invasoras, introducidas en el momento actual, no se hayan detectado o reconocido todavía, por lo que se prevé que en un futuro próximo la tasa de invasiones se incremente,

1En el Anexo se incluye un listado con las 100 especies invasoras más dañinas de Europa

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Cuadro 4 Datos revelados por el primer registro de especies invasoras de Europa, elaborado dentro del proyecto europeo DAISIE (Delivering Alien Invasive Species Inventories for Europe).

Fuente: DAISIE-project, disponible on-line en: www.europe-aliens.org afectando a nuevos ecosistemas y regiones geográficas. Por otra parte, la creciente movilidad de las personas y mercancías, y el fenómeno de la globalización, en pleno desarrollo, favorecerán la transferencia a escala global de un gran número de especies en las próximas décadas (Mack 1991; Jenkins 1996; Ruiz et al. 2000). La prevención, evitando la introducción de nuevas especies y actuando antes de que se produzca la colonización de nuevas áreas, es la forma más eficiente y económica de enfrentarse a las invasiones biológicas venideras. En los casos en los que ya se ha producido la introducción, una detección temprana y una respuesta rápida en las primeras fases de la colonización pueden impedir el establecimiento de la especie invasora y lograr su erradicación (Genovesi y Shine 2004).

El galápago leproso

erteneciente a la familia de los batagúridos, el galápago leproso (Mauremys leprosa, Schweiger 1812) es una especie de carácter termófilo, distribuida por el suroeste de Europa y el noroeste de África

(Da Silva 2002). En la Península Ibérica es mucho más común en la mitad sur, escaseando en la meseta septentrional y siendo muy rara su presencia en el norte, encontrándose poblaciones aisladas en puntos dispersos, quizá debidas a

P

Las cifras En Europa habitan 11.000 especies invasoras

Más del 10 % de estas especies son dañinas para los ecosistemas y/o la economía del continente europeo

El Mediterráneo es el área marina más perjudicada, con una superficie afectada de 2.500.000 Km2 y 1.313 de las especies registradas

Las plantas y los invertebrados terrestres son los taxones con mayor número de especies invasoras (6.630 y 2.535 respectivamente) que causan impactos en los ecosistemas

España cuenta con 1.467 especies foráneas

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escapes y/o introducciones (Bea 1998; Gosá y Bergerandi 1994; Galán 1999) (Fig. 2). Habita preferentemente charcas y arroyos de torrentera con vegetación de rivera, siendo menos común en grandes ríos y embalses. Tolera muy bien las aguas salobres, y en cierta medida la contaminación, pero tiende a desaparecer cuando ésta es excesiva (Andreu y López-Jurado 1998; Da Silva 2002). El caparazón, que puede alcanzar los 21 cm, es pardo oliváceo, y el plastrón, amarillo o crema con manchas oscuras. Los jóvenes presentan rayas anaranjadas muy patentes en la cabeza, cuello y patas, que tienden a disolverse con la edad. Las hembras alcanzan tamaños mayores que los machos, y carecen de la patente concavidad que éstos presentan en el plastrón. La porción anterior de la cola, desde la base a la cloaca, es mayor en los machos (Andreu y López-Jurado 1998). Los machos adquieren la madurez sexual en torno a los siete años (cuando alcanzan tamaños de entre 135 y 140 mm), mientras que las hembras la adquieren a edades próximas a los 10 años (con longitudes entre los 140 y los 160 mm) (Pérez et al. 1979). La puesta, de entre 1 y 13 huevos, tiene lugar en primavera, durante los meses de mayo y junio. Las crías miden unos 20 mm al nacer, entre 4 y 16 semanas después de la puesta (Andreu y

Figura 2 Distribución del galápago leproso, M. leprosa, en la P. Ibérica. Basado en Andreu y López-Jurado 1998

Ilustración | Mauremys leprosa

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López-Jurado 1998; Arnold y Ovenden 2002). La alimentación de esta especie, muy variada, se compone de insectos, pequeños moluscos y crustáceos, anfibios, peces, plantas, carroña e incluso excrementos (Salvador 1985; Oliveira y Crespo 1989). Los ejemplares pueden vivir hasta 20 años en cautividad.

La especie se encuentra actualmente catalogada como Vulnerable según los criterios de UICN (Da Silva 2002), al estar desapareciendo en determinadas áreas de su distribución. Su regresión se debe fundamentalmente a la intensa transformación del hábitat y a la excesiva contaminación de las zonas agrícolas e industriales (Da Silva 2002). A estos factores se suma la introducción en las últimas décadas de especies exóticas de galápagos competidores, principalmente el galápago de Florida.

El galápago de Florida

ambién conocido como galápago americano o tortuga de orejas rojas, el galápago de Florida (Trachemys scripta elegans, Wied 1839) es un quelonio perteneciente a la familia de los emídidos. Originario del

sureste de los EEUU y noreste de Méjico, posee un rango geográfico muy amplio, extendiéndose por la cuenca del Mississippi, desde Illinois hasta el Golfode Méjico (Fig. 3). Se trata de una especie semiacuática, generalista y ubiquista, que habita lagunas, canales, áreas pantanosas, arroyos intermitentes y otras zonas húmedas con abundante vegetación (Carr 1952; Gibbons 1990). Se caracteriza por poseer una intensa mancha roja postorbital (de ahí el sobrenombre de “orejas rojas”), estrechas bandas gulares y una banda amarilla transversal en cada escudo pleural (Ernst y Barbour 1989). Su dimorfismo sexual es observable en las uñas de las extremidades anteriores y en la longitud de la

cola (en ambos casos más largas en los machos), así como en el pequeño tamaño de los machos en comparación con las hembras (Gibbons 1990). Los individuos pueden sobrepasar los 30 cm de longitud (N. Polo-Cavia, pers. obs.), y vivir hasta 40 años en condiciones de cautividad (Capdevila-Argüelles y Zilletti 2006). En los machos, la madurez sexual se adquiere al alcanzar un tamaño determinado (80-130 mm en la longitud del plastrón), mientras que en las hembras, la madurez parece estar más

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Figura 3 Área de distribución original del galápago de Florida, T. scripta. Basado en Gibbons 1990

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relacionada con la edad (las primeras puestas suelen producirse entre los 5 y los 7 años) (Gibbons y Greene 1990). La reproducción tiene lugar en primavera, con puestas de 2 a 18 huevos que las hembras entierran en el suelo (Gibbons y Greene 1990). Los huevos eclosionan al cabo de unos tres meses, pero los recién nacidos permanecen en el nido por lo general hasta pasado el invierno (Gibbons y Nelson 1978). Aproximadamente un año después de la puesta, las crías se desplazan hasta el agua y comienzan a alimentarse (Clark y Gibbons 1969). Los juveniles son preferentemente carnívoros, al igual que los adultos cuando existe disponibilidad proteica en el medio (Parmenter 1980).

Durante las últimas décadas, un gran número de juveniles de T. scripta han sido importados en masa por diferentes países, como parte del comercio de mascotas, lo que ha dado lugar a frecuentes introducciones. La especie se encuentra actualmente establecida en diversas regiones de África, Asia y Europa (Tiedemann 1990; Chen y Lue 1998), especialmente en países mediterráneos (Luiselli et al. 1997; Chen y Lue 1998; Pleguezuelos 2002), donde coloniza todo tipo de masas de agua, incluso algunas muy contaminadas, gracias a su gran capacidad de adaptación (Gibbons 1990). Su reproducción en el medio natural ha sido constatada en varias de estas áreas (Luiselli et al. 1997; Martinez-Silvestre et al. 1997; Cadi et al.

Figura 4 Presencia del galápago de Florida, T. scripta, en la P. Ibérica. Basado en Pleguezuelos 2002; Loureiro et al. 2008

Ilustración | Trachemys scripta elegans

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2004). En la Península Ibérica se ha producido una gran expansión de la especie, existiendo poblaciones autónomas de mayor o menor densidad en diversas marismas y humedales de la franja litoral, así como en puntos dispersos del interior (Pleguezuelos 2002; Fig. 4). Estas poblaciones son susceptibles de causar importantes impactos sobre los ecosistemas, pudiendo interferir con las poblaciones de galápagos nativos.

Interacciones competitivas entre galápagos nativos e invasores

lgunas observaciones indican que el galápago de Florida es una especieque compite con los galápagos autóctonos ibéricos (el europeo, Emys orbicularis y el leproso, Mauremys leprosa). Sin embargo, la forma en

que se puedan estar produciendo las interacciones entre especies no está clara. Tanto los galápagos nativos como el americano ingieren materia animal de manera constante –todos depredan sobre anfibios ibéricos-, dedican gran parte del tiempo a asolearse y coinciden en las épocas de reproducción (Gibbons 1990; Andreu y López-Jurado 1998; Pleguezuelos 2002), por lo que es probable que exista competencia por los recursos tróficos, los lugares de asoleamiento o los de nidificación (Crucitti et al. 1990; Cadi y Joly 2003, 2004). La introducción de patógenos por parte de los galápagos exóticos que ataquen a los nativos es otra de las interacciones posibles (Hidalgo Vila et al. 2009). Entre las ventajas potenciales de T. scripta sobre las especies nativas se han citado una mayor tolerancia a la contaminación y a la presencia humana, lo que podría permitirle una distribución más amplia (Pleguezuelos 2002). Además, el galápago de Florida se muestra activo a temperaturas inferiores del agua, por lo que puede comenzar antes su actividad anual, alcanza tallas superiores a las de los galápagos autóctonos, produce una mayor descendencia, tiene una madurez sexual más temprana y una dieta más variada (Gibbons 1990; Pleguezuelos 2002).

En diversas áreas de la Península Ibérica se han encontrado ejemplares de galápago de Florida conviviendo en sintopía con galápagos leprosos, incluso compartiendo los mismos lugares de asoleamiento (Aceituno 2001; Ayres 2001; Balset 2001; Martínez-Silvestre et al. 2001; Díaz-Paniagua et al. 2002). Tanto M. leprosa como T. scripta son especies principalmente acuáticas, pero abandonan el agua para asolearse. Durante estos momentos, los galápagos son presas potenciales de diversos depredadores, como algunas aves o mamíferos terrestres (Greene 1988; Martín y López 1990), por lo que se muestran muy cautelosos, especialmente los leprosos, estando expectantes y en constante alerta, y sumergiéndose en el agua ante la menor señal de peligro (López et al. 2005). Por

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esta razón, los lugares preferidos para el asoleamiento son piedras y troncos emergidos en las áreas centrales de las charcas o arroyos, rodeados de agua profunda (Cadi y Joly 2003). El desplazamiento de E. orbicularis de estos lugares por parte del introducido T. scripta ha sido comprobado experimentalmente (Cadi y Joly 2003), y las observaciones de campo sugieren que es muy posible que la competencia durante el asoleamiento se produzca también entre M. leprosa y T. scripta, puesto que los recursos son limitados y las dos especies se ven obligadas a compartirlos (Díaz-Paniagua et al. 2002; Pleguezuelos 2002; Cadi y Joly 2003). Así, el galápago de Florida podría monopolizar los lugares más aptos para el asoleamiento, impidiendo la adecuada termorregulación de los galápagos nativos, lo que podría afectar gravemente a la eficiencia de sus funciones fisiológicas, especialmente la de aquellas relacionadas con la digestión (Parmenter 1981; Meek y Avery 1988; Avery et al. 1993; Koper y Brooks 2000). Tales efectos negativos, derivados de una actividad de asoleamiento deficiente, podrían afectar últimamente al crecimiento y a la reproducción de los galápagos autóctonos (Obbard y Brooks 1979; Avery et al. 1993). En este sentido, Cadi y Joly (2004) encontraron una significativa pérdida de peso y una elevada mortalidad en el galápago europeo tras someterlo experimentalmente a un largo periodo de competencia con el galápago de Florida.

El desplazamiento de M. leprosa debido a la introducción de T. scripta ha sido observado en algunos enclaves ibéricos. Por ejemplo, en la Laguna del Acebuche (Parque Nacional de Doñana), al extraer galápagos americanos de las zonas más profundas, con menor riesgo de depredación, éstas fueron re-ocupadas por el galápago leproso, lo que indica que la presencia del invasor está afectando al uso del espacio y a la selección de hábitat de los galápagos nativos, llegando incluso a excluirlos de los espacios más favorables (Díaz-Paniagua et al. 2002). Si la competencia con el galápago de Florida supone desventajas para los galápagos autóctonos, es muy posible que M. leprosa evite el contacto directo con T. scripta, utilizando en consecuencia recursos subóptimos y favoreciendo así la expansión de la especie exótica.

Dado que las características específicas de M. leprosa y T. scripta han evolucionado en sus respectivos hábitats naturales, las adaptaciones originales de cada especie podrían conferir ventajas o desventajas a los galápagos en una nueva situación ecológica en la que la especie introducida ocupa un hábitat desconocido y la nativa se enfrenta a la competencia con el invasor. En este sentido, el origen de T. scripta en un medio especialmente competitivo (i.e., la coexistencia de numerosas especies competidoras de galápagos en sintopía es habitual en muchos ecosistemas de Norteamérica; Gibbons 1990) podría dotarle de ciertas habilidades competitivas de las que podrían carecer los galápagos autóctonos, adaptados a ambientes de escasa o nula competencia (tan sólo dos especies de galápagos nativos, op.cit., habitan en la Península Ibérica). En

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consecuencia, una mayor voracidad, agresividad y/o dominancia del galápago de Florida podrían ser la causa principal del desplazamiento que sufre la especie nativa. No obstante, otras diferencias interespecíficas en la morfología, fisiología y comportamiento de los galápagos –hasta ahora inexploradas-, podrían afectar también al resultado de la competencia entre la especie nativa y la invasora. Así, por ejemplo, el galápago de Florida podría beneficiarse de determinadas ventajas termorreguladoras, menores requerimientos energéticos o estrategias depredatorias y/o antidepredatorias de mayor eficacia, producto de la adaptación a sus hábitats naturales, que le permitieran competir ventajosamente con los galápagos nativos en los nuevos territorios en los que ha sido introducido.

Justificación y objetivos

as características morfológicas, ecológicas y el comportamiento de los organismos han sido modelados por la selección natural a lo largo de la historia evolutiva de cada especie, permitiendo una mayor adaptación de

los individuos al conjunto de condiciones bióticas y abióticas de su entorno. Sin embargo, en ambientes que han sufrido una rápida alteración, estas características, anteriormente asociadas con el éxito reproductor y la supervivencia de los organismos (Williams y Nichols 1984), pueden perder repentinamente su valor adaptativo (Schlaepfer et al. 2005). En este sentido, las

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Ilustración | Galápagos exóticos se asolean sobre la vegetación palustre

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especies invasoras constituyen una seria amenaza para los ecosistemas, en tanto que generan nuevos contextos ecológicos en los que las respuestas de los organismos nativos, otrora adaptativas, pueden carecer de funcionalidad (Callaway y Aschehoug 2000; Shea y Chesson 2002). Como consecuencia de este desajuste, las especies nativas son susceptibles de sufrir un detrimento en sus tasas de supervivencia y/o reproducción (Schlaepfer et al. 2002).

Sin embargo, bajo circunstancias favorables, los organismos nativos pueden adquirir mecanismos (por evolución o aprendizaje), que les permitan hacer frente a las invasiones y mantener sus poblaciones (Ancel Meyers y Bull 2002). Así, las especies nativas pueden alterar su comportamiento y/o morfología, como resultado de las interacciones con las especies introducidas (Reznick y Endler 1982; Singer et al. 1993; Singer y Thomas 1996; Carroll et al. 1997, 1998; Magurran 1999). A pesar de ello, el comportamiento y los procesos evolutivos rara vez son integrados explícitamente en los planes y en las estrategias de conservación (e.g., Watters et al. 2003), tal vez debido a la presunción generalizada de que tales procesos operan a escalas espaciales y temporales que escapan a las posibilidades de actuación humana (Ashley et al. 2003). No obstante, existen numerosos ejemplos de rápida adquisición de comportamientos en respuesta a las modificaciones del ambiente (e.g., Griffin 2004), y algunos casos documentados de evolución en tiempo real (i.e., en el orden de años y décadas) inducidos por la actividad antrópica (Ashley et al. 2003; Rice y Emery 2003; Stockwell et al. 2003). Estos ejemplos ofrecen una nueva visión de las invasiones biológicas, así como la posibilidad de gestionar estas alteraciones en base a los regímenes de selección, al comportamiento y a la plasticidad de las especies nativas, con el fin de asegurar su persistencia a largo plazo (lo que se ha denominado en inglés evolutionarily enlightened management; Ashley et al. 2003). Integrar este tipo de gestión en los planes de intervención actuales es esencial para preservar la riqueza de especies nativas, especialmente en los casos en los que la erradicación de la fauna o la flora exótica es económica o biológicamente imposible. Un plan de actuación eventual, que garantice la permanencia de las especies nativas mientras se produce el tránsito a sus nuevos regímenes selectivos será, probablemente, menos costoso y más efectivo a largo plazo que los indefinidos intentos de erradicación de las especies invasoras.

La presente tesis pretende servir a este propósito, abordando en un contexto evolutivo diversos aspectos de la biología, ecología y comportamiento del galápago ibérico Mauremys leprosa, y comparándolos con los del galápago de Florida, Trachemys scripta, con el objetivo de contribuir a esclarecer la naturaleza de las interacciones competitivas que se puedan estar produciendo entre la especie nativa y la invasora. A lo largo de sus ocho capítulos, se han explorado diversos factores que pueden afectar al resultado de la competencia entre estas dos especies, analizando los potenciales efectos adversos que el

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galápago introducido pudiera generar en las poblaciones nativas de galápago leproso2.

Los tres primeros capítulos se han dedicado a examinar algunas de las posibles formas de interferencia directa por parte del galápago de Florida en tres aspectos clave de la ecología y el comportamiento del galápago leproso: uso del espacio, eficiencia de la alimentación y eficiencia termorreguladora. En los siguientes cuatro capítulos se analizan diferentes factores relacionados con el potencial y la habilidad competitiva específicos de cada especie, que podrían afectar indirectamente al resultado de la competencia (i.e., ventajas termorreguladoras, fisiológicas y comportamentales). Finalmente, en el último capítulo se analizan las potenciales ventajas que una trampa evolutiva (i.e., la incapacidad de los renacuajos presa para reconocer depredadores introducidos) podría conferir a los galápagos invasores.

Se han planteado los siguientes OBJETIVOS

Capítulo 1: En muchas especies de galápagos, las sustancias químicas secretadas por diferentes glándulas facilitan el reconocimiento específico y sexual, pudiendo afectar al uso del espacio y a la selección de hábitat de los individuos. El objetivo de este capítulo es analizar la capacidad de M. leprosa y T. scripta para reconocer secreciones químicas de machos y hembras coespecíficos y heteroespecíficos disueltas en el agua, y determinar si la detección de señales químicas de especies competidoras afecta al uso del espacio por parte de los galápagos nativos.

Capítulo 2: El galápago de Florida es una especie agresiva que podría desplazar a los galápagos nativos durante el desarrollo de actividades competitivas tales como la alimentación. Los objetivos de este capítulo son: comparar las tasas de ingestión de M. leprosa y T. scripta en situaciones de competencia intra e interespecífica, analizar el nivel de agresividad y la dominancia establecidos durante la alimentación entre individuos coespecíficos y heteroespecíficos, y determinar si existe relación entre el comportamiento agonístico de T. scripta y el posible desplazamiento de M. leprosa.

2Los capítulos reproducen el texto íntegro de manuscritos que han sido publicados en revistas científicas internacionales, o que se hallan en fase de revisión en el momento presente. Por esta razón se presentan en inglés, idioma original en el que fueron redactados. No obstante, en cada uno ellos se ha incluido un resumen en castellano.

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Capítulo 3: La eficiencia termorreguladora de los galápagos nativos podría verse comprometida en una situación de competencia con el galápago de Florida. El objetivo de este capítulo es determinar si la competencia por los recursos de asoleamiento entre las dos especies, ocasional o a largo plazo, supone una alteración en el tiempo disponible que los galápagos nativos pueden dedicar a asolearse, y si T. scripta desplaza a M. leprosa en la competencia por estos recursos.

Capítulo 4: Las diferencias morfológicas interespecíficas podrían influir significativamente en las tasas de calentamiento y enfriamiento de los galápagos, pudiendo derivarse ventajas termorreguladoras para el galápago de Florida. El objetivo de este capítulo es comparar la relación superficie-volumen de M. leprosa y T. scripta a partir de medidas biométricas y analizar los efectos de su morfología específica en las tasas de intercambio de calor.

Capítulo 5: Un comportamiento de asoleamiento deficiente a consecuencia de la competencia con el galápago de Florida podría ocasionar diversas alteraciones en el metabolismo de M. leprosa. Los objetivos de este capítulo son: comparar los requerimientos de asoleamiento de M. leprosa y T. scripta en condiciones de alimentación ad líbitum vs. ayuno prolongado, determinar el efecto de la privación de alimento en la temperatura preferida de asoleamiento de cada especie, y analizar la relación entre la morfología de los galápagos y esta temperatura.

Capítulo 6: La habilidad de los galápagos para recuperar su posición natural cuando son volteados accidentalmente es crítica para su supervivencia. En consecuencia, las posibles diferencias interespecíficas en el comportamiento de ‘giro’ de M. leprosa y T. scripta podrían contribuir a explicar la mayor capacidad competitiva del galápago introducido. El objetivo de este capítulo es comparar la respuesta de ‘giro’ (en su fase comportamental y mecánica) de ambas especies de galápagos y analizar los efectos de la temperatura corporal y la morfología en la respuesta de ‘giro’ de cada especie.

Capítulo 7: En ambientes alterados antrópicamente, potenciales diferencias en la percepción del riesgo de depredación entre M. leprosa y T. scripta podrían beneficiar a la especie invasora. El objetivo de este capítulo es analizar si existen diferencias interespecíficas en su comportamiento antidepredatorio comparando el tiempo que ambas especies pasan refugiadas en el caparazón tras la amenaza de un depredador en respuesta a diversos factores de riesgo.

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Capítulo 8: Tanto los galápagos nativos como los invasores depredan habitualmente sobre renacuajos de diversas especies de anuros. Estos renacuajos son capaces de reconocer y responder de forma innata a las señales químicas de los depredadores locales, pero su incapacidad para detectar nuevos depredadores podría conferir ventajas competitivas a los galápagos introducidos. El objetivo de este capítulo es analizar la capacidad de cuatro especies de renacuajos de anuros ibéricos para reconocer y responder a estímulos químicos de varias especies de galápagos nativos e invasores presentes en la Península.

Procedimiento

urante las primaveras de 2005 a 2008 se capturaron ejemplares de galápago leproso en diversas localidades de las Comunidades de Madrid y Extremadura. Así mismo, se obtuvieron galápagos de Florida

procedentes de varios centros de recuperación de fauna, donde eran mantenidos en condiciones de semilibertad. Estos galápagos habían sido extraídos de poblaciones introducidas en el medio natural, con el fin de evitar efectos adversos sobre las poblaciones nativas de galápagos. Los sujetos experimentales fueron trasladados a la Estación Biológica de El Ventorrillo (CSIC), próxima a Navacerrada (Madrid), donde se realizaron los experimentos. Los galápagos fueron alojados individualmente en acuarios (60 x 40 x 30 cm) situados al aire libre, que contenían agua y piedras que les permitían asolearse. El fotoperiodo y la temperatura fueron los mismos que los de las zonas de alrededor. Durante el tiempo que permanecieron en cautividad, los galápagos fueron alimentados tres veces por semana con carne picada, lombrices y babosas. Los animales se encontraban en buen estado de salud durante los experimentos, tras los cuales fueron devueltos a sus lugares exactos de captura (galápagos leprosos) o a los centros de recuperación de los que procedían (galápagos exóticos). Los experimentos cumplieron todas las leyes actuales de España y de los Organismos Medioambientales de la Comunidad de Madrid y de la Junta de Extremadura donde fueron llevados a cabo.

Capítulo 1: La capacidad de M. leprosa y T. scripta para reconocer secreciones químicas de individuos coespecíficos y heteroespecíficos disueltas en el agua se analizó comparando el tiempo que los galápagos permanecían en acuarios con agua limpia vs. el tiempo que permanecían en acuarios con los diferentes estímulos químicos. Dos acuarios experimentales (70 x 60 x 15 cm) fueron unidos por rampas que permitían a los galápagos desplazarse fácilmente de uno a

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otro acuario. En las pruebas, uno de los acuarios contenía siempre agua limpia mientras que en el otro se alternaron los tratamientos con los diferentes olores. A cada individuo se le aplicaron todos los tratamientos experimentales en orden aleatorio. Las posiciones de los acuarios fueron también aleatorizadas a lo largo de los experimentos, y se controló que la temperatura, la iluminación y la profundidad del agua fueran similares en todas las pruebas (De Rosa y Taylor 1980). Capítulo 2: Las tasas de ingestión de M. leprosa y T. scripta, así como la frecuencia de las interacciones agresivas entre los galápagos durante la alimentación, fueron comparadas en situaciones de competencia intra e interespecífica en acuarios (60 x 40 x 30 cm) situados al aire libre. Cada galápago competía en cada prueba con un individuo coespecífico o heteroespecífico de tamaño similar por 6 bolas de pienso compuesto, similares en apariencia y dinámica de flotación a determinados componentes de la dieta de los galápagos (i.e., trozos de algas, pequeños moluscos, etc.). Las pruebas se replicaron 5 veces en orden aleatorio en diferentes días, de forma que cada galápago compitió por 30 bolas de pienso en cada tratamiento experimental (i.e., competencia intraespecífica vs. competencia interespecífica). Al final de cada prueba los galápagos eran alimentados ad líbitum, y una vez saciados, mantenidos en ayuno en acuarios individuales hasta la siguiente prueba. Capítulo 3: Para analizar experimentalmente la actividad de asoleamiento de M. leprosa y T. scripta en situaciones de competencia intra e interespecífica por los lugares de asoleamiento se utilizaron acuarios (60 x 40 x 30 cm) provistos de una única plataforma (24 x 11,5 x 7 cm) para el asoleamiento. Los acuarios fueron colocados al aire libre y en cada uno de ellos se introdujo una pareja de individuos coespecíficos o heteroespecíficos de tamaño similar. Los patrones de asoleamiento de ambas especies fueron comparados entre tratamientos (i.e., competencia intraespecífica vs. competencia interespecífica), así como el tiempo que los galápagos se asolearon en solitario con el tiempo que compartieron las plataformas, asoleándose uno sobre otro. Los galápagos eran alimentados ad líbitum al final de cada prueba, pero no se les alimentó durante las observaciones, con el fin de evitar los efectos del estado nutricional en el comportamiento de asoleamiento (Hammond et al. 1988, Dubois et al. 2008). Los tratamientos fueron aleatorizados y se controló que la temperatura, la iluminación y la profundidad del agua fueran similares en todas las pruebas. Capítulo 4: La relación superficie-volumen de los galápagos fue calculada a partir de medidas biométricas, aproximando la forma de su caparazón a la de un semielipsoide de revolución. La superficie y el volumen de los galápagos se estimaron a partir de ecuaciones que fueron validadas cubriendo el caparazón de

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los galápagos con rectángulos de papel y calculando la suma total de sus áreas, y calculando el volumen de agua desplazada por los galápagos al sumergirlos en un recipiente. Para estimar las tasas de enfriamiento en aire de M. leprosa y T. scripta se utilizó una cámara de frío a 15 °C. Para las tasas de calentamiento y de enfriamiento en agua se utilizaron acuarios (60 x 40 x 30 cm) con agua a 15 °C, provistos de una plataforma emergente (24 x 11,5 x 7 cm) sobre la que pendía una lámpara de infrarrojos (250 W, 250 V). Los galápagos eran fijados a la plataforma hasta que su temperatura se estabilizaba en torno a los 30 °C y después liberados en el agua. La temperatura cloacal de los galápagos fue controlada continuamente durante las pruebas por medio de registradores conectados a una sonda (Mrosovsky 1980). Las tasas de intercambio de calor se calcularon a partir de los incrementos de temperatura registrados, ajustando ecuaciones de Bertalanffy (Von Bertalanffy 1960; Kaufman 1981).

Capítulo 5: Los requerimientos térmicos de ambas especies de galápagos se analizaron comparando las temperaturas preferidas de asoleamiento (i.e., la temperatura corporal a la cual cesa esta actividad) de M. leprosa y T. scripta en condiciones de alimentación vs. ayuno. Dependiendo del tratamiento, los galápagos fueron alimentados ad líbitum con pienso compuesto una vez al día durante los 7 días previos a las pruebas, o bien mantenidos en ayuno durante estos 7 días (Bennet y Dawson 1976; Gatten 1974). A cada individuo se le aplicaron ambos tratamientos en orden aleatorio. Durante las pruebas, se permitió a los galápagos asolearse libremente en acuarios (60 x 40 x 30 cm) con agua a temperatura ambiente, provistos de una plataforma emergente (24 x 11,5 x 7 cm) y una lámpara de infrarrojos (250 W, 250 V). Las temperaturas corporales de los galápagos fueron medidas continuamente durante 1 h por medio de registradores conectados a sondas cloacales. Las temperaturas preferidas de asoleamiento quedaban registradas en el momento en el que los galápagos se sumergían en el agua.

Capítulo 6: Para determinar la influencia de la temperatura en la respuesta de ‘giro’ de M. leprosa y T. scripta se midió el tiempo que los galápagos tardaban en darse la vuelta tras ser depositados con el plastrón hacia arriba sobre un sustrato de hierba uniforme, a tres temperaturas experimentales: 15 y 20 °C, y la temperatura preferida de asoleamiento respectiva de cada especie (esta temperatura se determinó siguiendo el mismo procedimiento que en el capítulo 5). Cada individuo fue observado a las tres temperaturas experimentales en orden aleatorio. Antes de cada prueba, los galápagos eran introducidos en una cámara termostática hasta que su temperatura corporal se estabilizaba a la temperatura correspondiente. Acto seguido, los galápagos eran depositados sobre el sustrato. Desde este momento se medía 1) el tiempo de latencia: tiempo

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que los galápagos permanecían inmóviles, y 2) la respuesta mecánica: el tiempo transcurrido desde el primer movimiento hasta que los galápagos completaban el giro. Capítulo 7: Las respuestas antidepredatorias de M. leprosa y T. scripta a los diferentes factores de riesgo se analizaron simulando ataques de diferente intensidad, manipulando a los galápagos durante 2 ó 25 s (‘riesgo bajo’ vs. ‘riesgo alto’) y depositándolos después en contenedores (70 x 60 x 15 cm) provistos de un sustrato de hierba, o bien conteniendo 4 cm de agua limpia (‘tierra’ vs. ‘agua’). Tras liberar a los galápagos, el experimentador se mantenía cerca (1 m), simulando la persistencia en el ataque, o se retiraba a una posición alejada (8 m), simulando el abandono de la presa (‘cerca’ vs. ‘lejos’). A partir de este momento se medía 1) el tiempo de aparición: tiempo desde que los galápagos eran liberados hasta que la cabeza y los ojos emergían del caparazón, y 2) el tiempo de espera: desde que los ojos eran visibles hasta que los galápagos iniciaban la huida. Capítulo 8: La capacidad de los renacuajos para reconocer y responder a estímulos químicos de galápagos nativos e invasores se analizó comparando sus niveles de actividad basal en canaletas (101 x 11,4 x 6,4 cm) con agua limpia vs. agua con los diferentes estímulos químicos de galápagos depredadores (nativos y exóticos) y vs. agua con los estímulos de un pez exótico no depredador. A cada renacuajo se le aplicaron los distintos tratamientos en orden aleatorio. La duración de las pruebas fue de 30 min y se permitió a los renacuajos descansar durante 24 h entre prueba y prueba. En las canaletas se trazaron líneas que permitían registrar la posición de los renacuajos cada minuto. Los niveles de actividad fueron estimados en cada tratamiento a partir del número de líneas cruzadas por los renacuajos durante el tiempo total de las pruebas (Rohr y Madison 2001; Gonzalo et al. 2007).

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Capítulos

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Capítulo 1

 

 

 

  

Diferencias interespecíficas en las respuestas quimiosensoriales de galápagos: consecuencias en la competencia entre 

especies nativas e invasoras 

Nuria Polo Cavia, Pilar López y José Martín

Biological Invasions 11 (2009) 431-440

 

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RESUMEN

El galápago de Florida (Trachemys scripta elegans) es una especie invasora, actualmente introducida en diversos países mediterráneos, donde está desplazando poblaciones nativas de galápago leproso (Mauremys leprosa). Sin embargo, la forma en la que se producen las interacciones competitivas entre estas dos especies permanece relativamente inexplorada. En muchas especies de galápagos, las sustancias secretadas por diferentes glándulas facilitan el reconocimiento específico y sexual. De este modo, es posible que la detección química de especies competidoras afecte al uso del espacio y a la selección de hábitat de los galápagos nativos. En este trabajo se analizó la capacidad de T. scripta y M. leprosa para reconocer señales químicas disueltas en agua, secretadas por machos y hembras coespecíficos y heteroespecíficos. Se comparó el tiempo que los galápagos permanecían en acuarios con agua limpia vs. el tiempo que permanecían en acuarios que contenían diferentes estímulos químicos. T. scripta no prefirió ni evitó los acuarios con estímulos químicos secretados por M. leprosa, lo que podría favorecer la expansión de la especie invasora. En contraste, M. leprosa prefirió agua con estímulos químicos de coespecíficos y evitó el agua con estímulos secretados por T. scripta, lo que sugiere que las señales químicas podrían ser usadas por los galápagos nativos para evitar áreas ocupadas por los galápagos exóticos. Sugerimos que este comportamiento de la especie nativa, M. leprosa, puede ser una de las causas que contribuya al desplazamiento observado de sus poblaciones por la especie invasora, T. scripta ■

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INTERSPECIFIC DIFFERENCES IN CHEMOSENSORY RESPONSES OF

FRESHWATER TURTLES: CONSEQUENCES FOR COMPETITION

BETWEEN NATIVE AND INVASIVE SPECIES

Abstract The red-eared slider (Trachemys scripta elegans) is an introduced invasive species in many Mediterranean countries that is displacing the populations of native endangered Spanish terrapins (Mauremys leprosa). However, it is relatively unknown how potential competitive interactions could be taking place. In many freshwater turtles, semiochemicals from different glands might facilitate species and sex recognition. We hypothesized that chemosensory detection of competitor species might affect space use and habitat selection by freshwater turtles. We analyzed whether T. scripta and M. leprosa turtles recognized chemical cues from male and female conspecifics and heterospecifics in water. We compared time spent by turtles in clean water pools vs. water pools containing the different chemical stimuli. Introduced T. scripta did not avoid nor prefer water pools with chemical stimuli of native M. leprosa terrapins, which might favor the expansion of the invasive species. In contrast, M. leprosa preferred water with chemical stimuli of conspecifics and avoided water with chemical cues of T. scripta, which suggests that chemical cues could be used by native M. leprosa to avoid water pools occupied by introduced T. scripta. We suggest that this avoidance behavior of native M. leprosa may be one of the causes that contribute to the observed displacement of their populations by invasive T. scripta. Keywords Chemoreception • Freshwater turtles • Invasive species • Mauremys leprosa • Trachemys scripta • Use of space

he introduction of species outside their natural ranges represents the second greatest threat to biodiversity after habitat destruction (Wilcove et al. 1998). Alien species may displace native species through

predation, hybridization, introduction of pathogens, or competition for resources (Williamson 1996; Shigesada and Kawasaki 1997). For example, the American red-eared slider (Trachemys scripta elegans) is currently introduced as a breeding species in many countries of Africa, Asia and Europe, especially in the Mediterranean area, where sliders have been uncontrollably released in diverse aquatic habitats after having been imported and sold as pets (Luiselli et al. 1997; Pleguezuelos 2002). Many observations indicate that introduced sliders are competing with native European species of freshwater turtles, such as the European pond terrapin (Emys orbicularis) and the Spanish terrapin (Mauremys leprosa) (Pleguezuelos 2002; Cadi and Joly 2003, 2004). In the Iberian Peninsula, the populations of native Spanish terrapins, M. leprosa, have considerably declined and this terrapin is now considered as an endangered species in some areas (Pleguezuelos et al. 2002). Although habitat destruction and human pressure are major causes for this decline, competition with introduced species, mainly T. scripta, might be worsening the conservation state of native Iberian turtles (Da Silva and Blasco 1995; Pleguezuelos et al. 2002).

T

 

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However, it is not clear how these interactions between native and introduced terrapins are taking place. It is possible that direct competition for food, refuge or basking places occurs (Cadi and Joly 2003, 2004). Also, the advantages of sliders over native freshwater turtles might be larger adult body size, more diverse diet, higher fecundity, and a greater tolerance to pollution and human presence (Pleguezuelos 2002; Polo-Cavia et al. 2008). Field observations showed that introduced T. scripta displaced native M. leprosa in some places, and that after removing T. scripta, these same places were re-occupied by M. leprosa, which indicates exclusion of the native species by the introduced one (Díaz-Paniagua et al. 2002). We hypothesized that, if direct competitive interactions are disadvantageous for native terrapins, they would likely avoid water pools in which they detected the presence of T. scripta, thus favoring the expansion of the invasive species. Freshwater turtles often inhabit quiet and stagnant waters, where dense vegetation and turbidity can make visual cues unreliable, and this would favor chemical detection of conspecifics or competitor species when visual cues are limited (Mason 1992; Muñoz 2004). If scents of T. scripta were aversive for M. leprosa, dispersal would be a logical result in a natural environment. Similarly, in the desert tortoise (Gopherus agassizi), the presence of urine from conspecifics at their sleeping areas do not significantly affect their aggregation behavior, but spreading urine of males of the related Texas tortoise (G. berlandieri) over the sleeping site cause G. agassizi to leave the site and sleep open (Patterson 1971).

However, although chemical communication is widespread among aquatic vertebrates (Müller-Schwarze 2006), very little is known of the chemical communication of freshwater turtles (see Mason 1992). Nevertheless, comparative neurology asserts that many turtles are well equipped anatomically for chemosensory detection (i.e., well developed olfactory and vomeronasal systems; Halpern 1992; Hatanaka and Matsuzaki 1993), and many turtle behaviors seem to be mediated by chemical signals (e.g., Graham et al. 1996; Quinn and Graves 1998; Poschadel et al. 2006; Müller-Schwarze 2006; see reviews in Mason 1992). Many turtles have several specialized glands that secrete potential semiochemicals (Ehrenfeld and Ehrenfeld 1973; Winokur and Legler 1975; Solomon 1984; Legler 1993). These glands are quiescent in juveniles, sexually dimorphic (larger in males), and active during the breeding season only (Rose et al. 1969). Cloacal secretions and faeces are also considered as possible sources of semiochemicals (Mason 1992). Some turtles use chemicals from these glands in foraging, homing behavior, aggregation, aggressive interactions between males, and mating behavior (reviewed in Mason 1992; Müller-Schwarze 2006). Chemical stimuli may also play a major role in sex and species identification (Harless 1979).

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The olfactory anatomy and some behavioral observations suggest that freshwater turtles can detect chemicals in water. Spanish terrapins (M. leprosa) have mental and inguinal Rathke’s glands, clearly visible in males, show frequent and conspicuous sniffing behavior similar to that of related species (Ernst 1971; Seigel 1980; Kramer and Fritz 1989; Kaufmann 1992), and can discriminate between water with chemical cues of male or female conspecifics (Muñoz 2004). Also, male European pond turtles (E. orbicularis) prefer water with the odor of a female over clean water, and can assess female body size based on chemical cues (Poschadel et al. 2006). Sliders (T. scripta elegans) seem to be also able of detecting odors underwater (Cagle 1950; Boycott and Guillery 1962; Parmenter 1980). Early experiments showed that sliders can be trained to make discriminations based on chemical cues (Boycott and Guillery 1962). However, sliders lack inguinal and mental glands, and preliminary comparative tests suggested that they may be less responsive to chemical cues than other freshwater turtles (Cagle 1950).

In this paper, we aimed to explore whether attraction or repulsion for water with conspecific or heterospecific chemical cues might affect space use by freshwater turtles, which might have consequences for the outcome of competition between native and invasive species. We specifically analyzed whether M. leprosa and T. scripta were able to recognize chemical cues from conspecifics and heterospecifics in water. We firstly analyzed in the laboratory the use by T. scripta of pools with clean water compared with pools with water with their own chemical stimuli, or with chemical stimuli from male or female conspecifics. Similar data for M. leprosa are already available (Muñoz 2004). Then, we compared time spent by male and female M. leprosa and T. scripta in pools with clean water vs. time spent in pools with water containing chemical cues from conspecific or heterospecific males or females.

METHODS

Study animals

We obtained red-eared sliders (T. scripta) (carapace length: mean ± SE = 15 ± 1 cm, n = 38), from a large outdoor pond located in Madrid Province (central Spain), where they had been maintained under seminatural conditions by the conservationist private organization ‘‘Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat’’ (GREFA). These sliders had been recently extracted from introduced populations in central Spain to avoid aversive effects on populations of native terrapins. We captured with funnel traps Spanish terrapins (M. leprosa) (carapace length: mean ± SE = 16 ± 2 cm, n = 15) in

 

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several ponds and creeks of the Manzanares river (Madrid Province, Spain), where introduced sliders can be also found.

All turtles were individually housed at ‘‘El Ventorrillo’’ Field Station (Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) filled with water and containing stones that allowed turtles to bask. Temperature and photoperiod were those of the surroundings. Turtles were fed mince meat, worms and slugs three times a week. Turtles were held in their home-aquaria for at least two weeks before testing, so that they became familiarized with captivity conditions. At the end of experiments, all turtles had maintained or increased their body mass, and were returned to the GREFA’s pond (sliders) or to their exact field capture sites (Spanish terrapins).

Experimental procedure

In a first experiment, we analyzed the use by T. scripta of pools with water with chemical stimuli from conspecific males or females, or with their own chemical stimuli. We carried out the experiments outdoor using two artificial pools (i.e., two plastic containers of 70 x 60 x 15 cm each) that were joined by stone ramps, which allowed turtles to move easily from one pool to the other. One pool was always filled with clean water, and the other was filled with water with one of the different chemical stimuli taken from either the home-aquaria of individual donor turtles of the same or the opposite sex of the subject turtle, or from the own home-aquaria of the subject turtle. We tested each subject turtle in three treatments (‘clean vs. same sex stimulus’, ‘clean vs. opposite sex stimulus’, ‘clean vs. own stimulus’) in a random sequence. Clean water was obtained from a nearby mountain stream that does not contain turtles. Home-aquaria of donor turtles had been filled with 15 cm deep clean water, and the donor turtle had been maintained there for 3 days without being fed. Thus, original clean water was pervaded with the donor turtle’s scents alone. The position of the pools with clean and stimulus water was randomized. We also monitored at the beginning of the tests water and air temperatures (with digital thermometers; precision ± 0.1 °C), the extent of illumination by sunlight, and water depth to ensure that they were similar in both pools during all the tests and did not affect the turtle responses (De Rosa and Taylor 1980). To avoid odor contamination, after each trial, we cleaned the pools and the ramps with clean water, and let them dried outdoor for 12 h. Trials were spaced in time for at least 2 days so that possible stress resulting from one test did not affect subsequent tests. The experiment was repeated with different responding individuals during the mating (April) and non-mating (July) seasons (Gibbons and Greene 1990).

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Before the trials, turtles were allowed to bask for at least 2 h in their home-aquaria, so turtles could attain an optimal body temperature. At the beginning of the trials, each turtle was placed over the ramps, in the middle of the experimental pools, so it was given the choice between the two water pools. Turtles usually explored the two pools, changing from one to the other, very often at the beginning of the trial and less frequently as the experiment progressed. We used the instantaneous scan sampling method to monitor each turtle during 3 h, scanning from a hidden position, and recording every 15 min the location of the turtle (12 scans per turtle in total). In each scan, if the turtle was situated in one of the two pools (clean or with chemical stimulus), we assumed that it had chosen that pool, whereas if it was located in a non-specific position (e.g., on the ramps), we assumed that it had made no choice. We assessed the ‘preferences’ of each turtle for each chemical cue from the percentage of time (excluding time spent in the non-choice area) that the turtle spent in each water pool (clean vs. stimulus). Then, we compared the percentage of time that turtles spent in water with different chemical cues to estimate differences in ‘preferences’ between treatments. Preliminary trials showed that there were no significant differences in percentage of use between two clean-water pools.

In a second experiment, we compared the use by M. leprosa and T. scripta of water with conspecific or heterospecific chemical cues. We followed the same procedures as in the first experiment, but the stimulus pool was filled with water from the home-aquaria of individual donor turtles that were either (1) a conspecific of the same sex, (2) a conspecific of the opposite sex, (3) a heterospecific of its same sex, or (4) a heterospecific of the opposite sex. Thus, we tested each subject turtle in four experimental treatments in a random order (‘clean vs. same sex conspecific stimulus’, ‘clean vs. opposite sex conspecific stimulus’, ‘clean vs. same sex heterospecific stimulus’ and ‘clean vs. opposite sex heterospecific stimulus’).

Statistical analyses We used repeated measures analyses of variance (ANOVAs) to analyze the differences in use of water pools with different chemical cues across treatments by the same individual subject turtle. Data from the first experiment were analyzed with a three-way repeated measures ANOVA with the experimental treatment (‘same sex stimulus’ vs. ‘opposite sex stimulus’ vs. ‘own stimulus’) as a within subject factor, and the sex of the subject turtle and the season as two between-subjects factors. In the second experiment, we used a four-way repeated measures ANOVA with the chemical cues treatments, species (‘conspecific stimulus’ vs. ‘heterospecific stimulus’) and sex (‘same sex stimulus’

 

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vs. ‘opposite sex stimulus’), as two within-subjects factors. The sex and the species of the subject turtle were included as between-subjects factors.

Data normality was verified by Shapiro-Wilk’s test and tests of homogeneity of variances (Levene’s test) showed that variances were not significantly heterogeneous. Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995).

RESULTS

Responses of T. scripta to conspecific and own scents There were significant differences between seasons in the overall time that T. scripta spent in pools with water with chemical cues from conspecifics or water from their home-aquaria (three-way repeated measures ANOVA, season: F = 7.33, df = 1,31, P = 0.01) (Fig. 1.1). Thus, sliders spent less time in water with conspecific or own chemical stimuli during the mating season (38 ± 3 %) than during the non-mating season (49 ± 3 %). Sliders tended to prefer water with their own odor in both seasons, but differences between treatments did not reach statistical significance (treatment: F = 2.69, df = 2,62, P = 0.08). The interaction between treatment and season was non-significant (F = 2.05, df = 2,62, P = 0.14). Sex of the subject turtle did not influence the use of water pools (sex: F = 0.11, df = 1,31, P = 0.75). The rest of the interactions were all non-significant (P > 0.40 in all cases). Between-species comparison Overall percent time spent by turtles in pools with different types of water did not differ significantly depending on the species or sex of the subject turtle, and the interaction between these two factors was non-significant (Table 1.1). However, the significant differences between conspecific and heterospecific stimulus and a significant interaction term (species stimulus x species subject) indicated that T. scripta did not show significant differences in the use of pools with water with conspecific or heterospecific chemical cues (Tukey’s test, P = 0.98), but M. leprosa had significantly greater preferences for water with conspecific chemicals than for water with chemicals of T. scripta (P = 0.0003). Time spent in pools with conspecific chemical cues was significantly higher in M. leprosa than in T. scripta (P = 0.0006), while time spent in pools with heterospecific chemical cues was significantly lower in M. leprosa than in T. scripta (P = 0.03) (Fig. 1.2; Table 1.1).

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Figure 1.1 Percent time (mean ± SE) spent by T. scripta in pools with water with chemical cues stimuli from conspecific donor turtles of the same or opposite sex, or with their own chemicals, during (a) mating and (b) non-mating seasons

Figure 1.2 Percent time (mean ± SE) spent by T. scripta and M. leprosa in pools with water with chemical cues stimuli from conspecific or heterospecific donor turtles

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Table 1.1 Results from a four-way repeated measures ANOVA examining the effects of the sex and species of the responding subject turtle, and sex and species of the donor turtle that provided the chemical cues stimulus, on the levels of preference of water with chemical stimuli by subject turtles (df = 1,31 in all cases)

There were no significant overall differences between preferences for

chemicals of the same or the opposite sex, and neither the interactions between species of the subject turtle, or sex of the subject turtle, and preferences for sex stimulus were significant. All of the three factors interactions were non-significant (Table 1.1).  

In addition, there was a significant four way interaction between species and sex of the donor turtle and species and sex of the subject turtle (Fig. 1.3; Table 1.1). Thus, preferences of both male and female T. scripta were not significantly different for any stimuli (Tukey’s tests, P > 0.97 in all cases). However, male M. leprosa had significantly greater preferences for conspecific female chemical cues than for heterospecific female (P = 0.0002) and heterospecific male chemical cues (P = 0.002), and significantly greater preferences for conspecific male chemical cues than for heterospecific male (P = 0.03) and female chemical cues (P = 0.003). In contrast, female M. leprosa had significantly greater preferences for conspecific female chemical cues than for heterospecific female (P = 0.0004) and heterospecific male cues (P = 0.003), but preferences for conspecific and heterospecific male chemical cues were not significantly different (P = 0.40).

Effect F P

Species subject 3.48 0.07 Sex subject 0.83 0.37 Species stimulus 32.98 < 0.0001 Sex stimulus 1.40 0.25 Species subject x sex subject 0.86 0.36 Species stimulus x species subject 25.10 < 0.0001 Species stimulus x sex subject 0.27 0.61 Sex stimulus x species subject 0.06 0.80 Sex stimulus x sex subject 1.60 0.22 Species stimulus x sex stimulus 2.63 0.11 Species stimulus x species subject x sex subject 0.19 0.67 Sex stimulus x species subject x sex subject 0.01 0.99 Species stimulus x sex stimulus x species subject 0.04 0.84 Species stimulus x sex stimulus x sex subject 2.25 0.14 Species stimulus x sex stimulus x species subject x sex subject 6.63 0.02

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Figure 1.3 Percent time (mean ± SE) spent by males and females (a) T. scripta and (b) M. leprosa in pools with water with chemical cues stimuli from conspecific or heterospecific donor turtles of the same or opposite sex

DISCUSSION

Our results first suggest that red-eared sliders, T. scripta, are able to detect chemical cues from conspecifics in water and to vary seasonally their responses, such that sliders spent more time in clean water without conspecific chemical stimuli during the mating season. During breeding, sliders may exhibit aggressive behavior towards each other, with males fighting each other or harassing females (Evans 1952). Thus, sliders may avoid water with conspecific chemical cues during the mating season to avoid potential aggressive encounters with conspecifics. However, sliders did not show a clear significant

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discrimination of the different conspecific chemical stimuli, nor of their own scents, which suggests that these different chemical stimuli were not discriminated, or that the discrimination did not affect their space use. In contrast, a similar experiment showed that Spanish terrapins, M. leprosa, clearly discriminate between male and female conspecific chemical stimuli, especially during the mating season (Muñoz 2004). Therefore, when deciding space use, sliders seem to be less chemosensory dependent than Spanish terrapins, whose reproductive behavior seems based greatly on chemical signals. For example, male head bobbing, which may help to spread scent from mental glands to females (Auffenberg 1966) is a normal behavior of M. leprosa during courtship (N. Polo-Cavia, unpubl. data). Also, throat pumping behavior, a mechanism for moving water across chemoreceptors in the mouth or nasal cavities for chemical sampling (Walker 1959), has been observed in M. leprosa (N. Polo-Cavia, unpubl. data), which suggests a greater use of olfactory senses in this turtle species. In contrast, T. scripta lacks mental glands, and courtship involves a visual dance where the male vibrates his claws on the female’s head (Jackson and Davis 1972). However, olfaction seems to be also used by T. scripta, as one third of the telencephalon is occupied by the olfactory bulbs (Scott 1979), sex recognition seems to depend on chemical cues (Cagle 1950) and sniffing has been observed during courtship (Jackson and Davis 1972). Olfaction also may play a role in prey detection; Parmenter (1980) showed that T. scripta responds to odors from fish-meat baits placed in perforated containers, indicating that location of carrion can be facilitated by olfactory cues.

Our results further indicate that M. leprosa was able to identify scents of conspecifics and heterospecific T. scripta in water, and that M. leprosa avoided water with these heterospecific chemical stimuli. In contrast, T. scripta did not avoid, but neither prefer, water with scent from M. leprosa. The absence of response in T. scripta may be due to inability to detect heterospecific chemical cues, or simply to that, although detected, these cues are not avoided because M. leprosa does not represent a threat for the invasive T. scripta. Preliminary comparative tests suggested that sliders may be less responsive to olfactory cues than other freshwater turtle species (Cagle 1950). However, the ability of sliders to discriminate different olfactory stimulus was established by Boycott and Guillery (1962), who successfully trained sliders to discriminate an olfactory stimulus (i.e., amylacetate, vanillin, or eucalyptus oil) that was presented in water containing also food. It is likely that T. scripta might be able to discriminate scents of M. leprosa too, and that the absence of responses in the use of water pools in our experiment could be due to the absence of negative stimuli associated to the chemical cues of M. leprosa.

On the other hand, the preferences of M. leprosa for water with conspecific chemical stimuli and the avoidance of water with scent of T. scripta suggest that

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M. leprosa may use chemoreception to avoid water pools occupied by T. scripta. This behavior may be applicable to natural habitats because concentrations of the chemical stimuli used in our laboratory experiment may resemble the effect that a new population of introduced sliders, spreading continuously their chemical cues, may cause in a natural body of relatively quiet water. Thus, it is likely that M. leprosa may also identify the presence of chemical cues of T. scripta in natural ponds, and use this information to avoid these areas.

The ability to recognize conspecific scents has been reported in many animal species, and may contribute to decrease the costs of aggressive interactions, or facilitate reproductive interactions (Mason 1992; Müller-Schwarze 2006). However, recognition of heterospecific chemical cues in water may help to assess risk posed by predators or aversive competitor species in many aquatic animals (for reviews see Dodson et al. 1994; Kats and Dill 1998). Prey species often respond to predator or aversive stimuli by reducing activity or seeking refuge, but, in many different animal species, a simpler avoidance response of areas with aversive chemicals is the primary response after chemosensory detection (Kats and Dill 1998). The effects of predator and aversive chemical cues on avoidance behavior have been examined in many terrestrial reptiles (e.g., Downes 2002; Amo et al. 2004), but rarely on aquatic ones. In turtles, Jackson (1990) found that two species of musk turtles (Sternotherus spp.) avoid odors of their predator, the alligator snapping turtle (Macrochelys temminckii). Speed of movement, the frequency of gular pumping behavior, and percentage of time spent by musk turtles in water with chemicals of alligator snapping turtles were lower than those in water with odor of a non-predator turtle species (Pseudemys sp.). This suggests that musk turtles may detect and avoid proximity with water used by the predator turtle species.

In many cases, animals can acquire recognition of an odor as dangerous when they simultaneously detect this odor and known indicators of risk such as the antipredator behavior, or injury-released chemicals, of conspecifics (e.g., Magurran 1989; Mathis et al. 1996; Chivers and Smith 1998). In this context, there are only a few documented cases of native prey able to learn the ability to avoid invasive species. For example, predator-avoidance behavior can propagate through a naïve population of fish in less than two weeks after the introduction of a novel predator (Chivers and Smith 1995). Also, juvenile Pacific treefrogs (Hyla regilla) from a population that co-occurred with introduced bullfrogs (Rana catesbeiana) showed a strong avoidance of chemical cues of bullfrogs (Chivers et al. 2001). It is likely that the presence of an introduced aversive competitor species might have an effect similar to a novel predator. Native species might learn to avoid odors from invasive species if these odors were previously associated with an overt behavioral aggressive response, or

 

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unsuccessful use of resources. For example, two mice species show avoidance response to heterospecific odors in spring, but not in autumn, probably to avoid interspecific aggressive encounters due to competition for habitat resources during the breeding season (Simeonovska-Nikolova 2007). Since T. scripta seems more aggressive than native European turtles in heterospecific encounters competing for food or basking places (Cadi and Joly 2003; Polo-Cavia et al. in press; chapter 2), the avoidance response of native M. leprosa to heterospecific odors of T. scripta might serve as a spacing mechanism to avoid aggressive encounters with the alien species in a situation of competitive disadvantage. Native M. leprosa might acquire information from chemicals in water, and use this information to distinguish between conspecifics and heterospecifics, thereby avoiding to spent time and energy in unfavorable competitive interactions with invasive American turtles. By keeping away from water pools with odors of T. scripta, M. leprosa might evade costly aggressive encounters with this invasive species under severe interspecific competition for limited resources. However, this chemically-mediated avoidance behavior could result in the displacement and progressive replacement of M. leprosa populations by the alien T. scripta, which expansion might be further favored by their lack of chemosensory responses towards native turtle species. Acknowledgements We thank an anonymous reviewer for helpful comments, the ‘‘Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat’’ (GREFA) for providing sliders, and ‘‘El Ventorrillo’’ MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS, and by an ‘‘El Ventorrillo’’ CSIC grant and a MEC-FPU grant to N. P.-C. The experiments enforced all the present Spanish laws and of the Environmental Organisms of Madrid Communities where they were carried out. REFERENCES Amo L, López P, Martín J (2004) Wall lizards combine chemical and visual cues of ambush snake

predators to avoid overestimating risk inside refuges. Anim Behav 67: 647-653 Auffenberg W (1966) On the courtship of Gopherus polyphemus. Herpetologica 22: 113-117 Boycott BB, Guillery RW (1962) Olfactory and visual learning in the red-eared terrapin,

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turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Can J Zool 81: 1392-1398

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PL (eds) Fauna of Australia, Vol 2A. Amphibia and Reptilia. Australian Government Publishing Service, Canberra, pp 108-119

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Pleguezuelos JM, Márquez R, Lizana M (2002) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Asociación Herpetológica Española-Ministerio de Medio Ambiente, Madrid

Polo-Cavia N, López P, Martín J (2008) Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114: 115-123

Polo-Cavia N, López P, Martín J (in press) Competitive interactions during basking between native and invasive freshwater turtle species. Biol Invas

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Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, Oxford

Simeonovska-Nikolova DM (2007) Interspecific social interactions and behavioral responses of Apodemus agrarius and Apodemus flavicollis to conspecific and heterospecific odors. J Ethol 25: 41-48

Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, New York Solomon SE (1984) The characterisation and distribution of cells lining the axilary gland of the

adult green turtle (Chelonia mydas L). J Anat 138: 267-279 Walker WF (1959) Closure of the nostrils in the Atlantic loggerhead and other sea turtles. Copeia

1959: 257-259 Wilcove DS, Rothstein D, Dubow D, Phillips A, Losos E (1998) Quantifying threats to imperiled

species in the United States. Bioscience 48: 607-615 Williamson M (1996) Biological invasions. Chapman and Hall, London Winokur RM, Legler JM (1975) Chelonian mental glands. J Morphol 147: 275-292

Capítulo 2

 

 

 

  

Interacciones agresivas durante la alimentación entre especies nativas e 

invasoras de galápagos 

Nuria Polo Cavia, Pilar López y José Martín

 

En revisión

 

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RESUMEN

El galápago de Florida (Trachemys scripta elegans) es una especie altamente invasiva a nivel mundial, actualmente introducida en la gran mayoría de los humedales debido al comercio masivo de mascotas. En la Península Ibérica, esta especie compite y desplaza al galápago leproso (Mauremys leprosa), especie autóctona protegida. El galápago de Florida está considerado como una especie ecológicamente agresiva, capaz de amenazar o morder a otros individuos mientras realiza actividades competitivas tales como la alimentación. Este comportamiento agonístico de los galápagos introducidos dirigido hacia los galápagos nativos podría afectar negativamente a la eficiencia nutricional de la especie indígena M. leprosa. En este trabajo, se compararon las tasas de ingestión de los galápagos nativos e invasores, y las interacciones agresivas ocurridas durante la alimentación, en situaciones de competencia intra e interespecífica. La cantidad de alimento ingerida por M. leprosa y T. scripta fue similar cuando compitieron con individuos conespecíficos. Sin embargo, en condiciones de competencia interespecífica, la especie invasora ingirió una mayor proporción del alimento suministrado. Además, los galápagos introducidos cometieron la mayor parte de las agresiones observadas durante la actividad de la alimentación, y las agresiones fueron dirigidas con mayor frecuencia hacia individuos heteroespecíficos. Nuestros resultados sugieren una mayor agresividad y un comportamiento más competitivo del introducido galápago de Florida en la pugna por los recursos alimenticios, lo que podría contribuir a explicar el desplazamiento de las poblaciones nativas de M. leprosa ■

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AGGRESSIVE INTERACTIONS DURING FEEDING BETWEEN NATIVE

AND INVASIVE FRESHWATER TURTLES

Abstract The red-eared slider (Trachemys scripta elegans) is a worldwide highly invasive species, currently introduced in most freshwater habitats as a consequence of massive pet trade. In the Iberian Peninsula, this species is competing and displacing the endangered native Spanish terrapin (Mauremys leprosa). Sliders are considered environmentally-aggressive turtles, capable of threatening or biting other individuals during competitive activities such as feeding. We hypothesized that agonistic behavior of introduced sliders against native terrapins might negatively affect the feeding efficiency of M. leprosa. We compared food ingestion of turtles and aggressive interactions during feeding, under situations of conspecific and heterospecific competition. The amount of food ingested by native and introduced turtles was similar under conspecific competition, but T. scripta ingested a greater percentage of food supplied under heterospecific competition. Also, introduced sliders initiated most of the aggressions observed during feeding activity, and aggressions were more frequently directed to heterospecifics. Our results suggest a more aggressive and competitive behavior of introduced T. scripta in vying for food resources, which might contribute to explain the observed displacement of native populations of M. leprosa. Keywords Aggressiveness • Freshwater turtles • Invasive species • Mauremys leprosa • Feeding competition • Trachemys scripta

pecies are being increasingly introduced by humans outside their natural ranges, competing and displacing native organisms from their ecological niches (Herbold and Moyle 1986; Williamson 1996; Mooney and Hobbs

2000; Lockwood et al. 2007). These introductions have altered terrestrial and aquatic communities worldwide, constituting the second greatest threat to biodiversity after habitat destruction (Wilcove et al. 1998; Gurevitch and Padilla 2004). Alien species may displace native species through predation, hybridization, pathogens transmission, or competition for resources (Dodd and Seigel 1991; Shigesada and Kawasaki 1997; Butterfield et al. 1997; Manchester and Bullock 2000).

An example of biological invasion is the red-eared slider (Trachemys scripta elegans), which has been commonly exported from the USA as part of the pet trade, being introduced in many countries of Africa, Asia and Europe, especially in Mediterranean habitats (Luiselli et al. 1997; Chen and Lue 1998; Pleguezuelos 2002). In the Iberian Peninsula, T. scripta has been released in diverse aquatic ecosystems, where it is displacing the native Spanish terrapin (Mauremys leprosa) (Da Silva and Blasco 1995; Pleguezuelos 2002; Vilà et al. 2008). This native species has suffered a considerable recession during the last decades, being currently considered as endangered species (Pleguezuelos et al. 2002). Recent studies have pointed out to diverse competitive advantages of sliders over Spanish terrapins, such as a more accurate assessment of predatory risk in

S

 

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altered habitats, displacement of native turtles mediated by chemical cues avoidance, or a greater thermal inertia that favors heat retention (Polo-Cavia et al. 2008, 2009a,b). Also, turtles may compete for food, nesting sites or basking places (Cadi and Joly 2003, 2004; N. Polo-Cavia, unpubl. data). Sliders are aggressive omnivores with high preferences for a carnivorous diet (growth rates significantly decline when individuals subsist on a vegetative diet, Parmenter 1980; Gibbons 1990), and might likely be involved in interference competition for food with Spanish terrapins, since M. leprosa consumes mainly animal matter and the two turtle species overlap in diet and feeding areas (Keller and Busack 2001; Pleguezuelos 2002).

The ideal free distribution model (IFD, Fretwell and Lucas 1970) predicts that foragers will distribute themselves among resource patches in relation to the quantity of food available in such patches. However, systematic deviations from IFD are expected when competitive asymmetries exist between foragers, and so, the access to resource patches is constrained by dominant individuals (Holmgren 1995; Moody and Houston 1995; Spencer et al. 1995). For example, in habitats with low food availability and difficulties for spatial segregation, patterns of habitat use by tits (Parus spp.) have been shown to be affected by intra and interspecific dominance (Alatalo et al. 1986; Alatalo and Moreno 1987). Similarly, experimental studies on the social rank of the juvenile Atlantic salmon (Salmo salar) showed that dominant fishes occupy the high quality patches, while subordinates are forced out (Huntingford et al. 1993; Huntingford and García de Leániz 1997). Furthermore, under interspecific competition, salmonid fish species with greater innate competitive ability occupy the more suitable habitats while subordinate species are displaced, which cause dominant species to gain higher growth rates than subordinates (Fausch 1984; Nakano 1995).

Several studies addressing overlap food preferences between sympatric species of turtles suggest that food niche separation is common among turtle species with overlapping diets (Moll 1976a; Vogt and Guzman 1988). Williams and Christiansen (1981) found that two species of turtles of the genus Trionyx with high degree of food overlap partitioned the habitat by one being a bottom forager and the other feeding in the water column. However, differences in growth rates and reproductive patterns between populations of the same species are often correlated with different levels of interspecific competition and displacement in the feeding niche (Moll 1976b; Bury 1979; Gibbons et al 1979; Vogt and Guzman 1988), what suggest that interspecific dominance relationships may lead to the lower survival of turtle species enduring high competitive pressures.

Displacement between competitors is mainly expected to occur through aggressive interactions, although subordinates have been observed to

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voluntarily displace themselves when dominant individuals approach (Huntingford and Turner 1987; Lindeman 1999; Polo-Cavia et al. 2009a). Aggressive behaviors such as open-mouth gestures, biting and pushing have been reported in a variety of turtle species, including T. scripta, when resources are limiting (Boice 1970, Lovich 1988; Kaufmann 1992, Lindeman1999). Introduced sliders are considered especially competitive turtles, capable of threatening or biting conspecific and heterospecific individuals during competitive activities (Arvy and Servan 1998, Lindeman 1999). In consequence, T. scripta turtles might impede M. leprosa terrapins to adequately forage, or exclude them from areas with more profitable feeding resources through aggressive interactions. We hypothesized that the higher aggressiveness of introduced sliders might negatively affect the feeding efficiency of native Spanish terrapins. We compared experimentally the food ingestion of both M. leprosa and T. scripta under situations of conspecific and heterospecific competition, analyzing aggressive interactions between turtles during feeding activity. The purpose of this paper was to determine 1) the feeding efficiency of M. leprosa when competition for food resources occurs between conspecific individuals, as opposed to a situation of interspecific competition with introduced sliders, 2) the level of aggressiveness and dominance among conspecific vs. heterospecific turtles during feeding competition, and 3) the relationship between the agonistic behavior of introduced T. scripta and the possible displacement from food resources of native M. leprosa.

METHODS

Study animals

During May 2006, we captured 16 Spanish terrapins (M. leprosa) (carapace length: mean ± SE = 14.2 ± 1.9 cm, range = 10.0-16.6 cm) in several ponds and creeks of the Manzanares River (Madrid Province, Spain), using funnel traps baited with fresh pet food and raw fish. We also obtained 16 red-eared sliders (T. scripta) (carapace length: mean ± SE = 14.5 ± 2.2 cm, range = 10.9-17.4) from a large outdoor pond (Madrid Province, central Spain), where they had been maintained under seminatural conditions by the conservationist organization “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These turtles had been recently extracted from introduced populations in Central Spain to avoid aversive effects on the original ecosystem balance. Sliders were selected basing on their body sizes, which were similar to those of native Spanish terrapins captured in the field. Both samples of M. leprosa and T. scripta were sex-balanced.

 

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All turtles were individually housed at “El Ventorrillo” Field Station (Navacerrada, Madrid Province), in outdoor home aquaria (60 x 40 x 30 cm), filled with water and containing stones that allowed turtles to bask. The temperature and photoperiod were those of the natural surroundings. Turtles were held in captivity for at least two weeks before experiments, to allow them to familiarize with captivity conditions. During this time, turtles were fed ad libitum small pieces of commercial compound feed (dehydrated meat) three times a week, so that they became habituated to the food supplied in the experiments. All turtles were healthy during the trials and all maintained their body mass. At the end of experiments, turtles were returned to the GREFA’s ponds (sliders) or to their exact field capture sites (Spanish terrapins).

Experimental procedure

We compared food ingestion of M. leprosa and T. scripta and frequencies of aggressive interactions between turtles during feeding activity, under situations of conspecific and heterospecific competition, and with competitors of the same and the opposite sex. We performed experiments outdoor, in aquaria exact to home aquaria, but that had not housed any turtle before the trials. For the experiments, each turtle was paired, according with its body size, with (1) a conspecific of the same sex, (2) a conspecific of the opposite sex, (3) a heterospecific of its same sex, and (4) a heterospecific of the opposite sex. Thus, we tested each subject turtle in four experimental treatments in a random order. Both members of the pairs were introduced together in the experimental aquaria right before the trial took place. During trials, we supplied 6 pieces of commercial compound feed to each pair of turtles (the amount of food provided was restricted to elicit competition within pairs). Turtles were used to experimental conditions and experimental food and they were hungry during the trials, so they fought for the pellets and always ate them all in few minutes). We considered that competition for compound feed pellets in captivity properly reflected competition for food in the wild, since these food pellets are similar in appearance, smell and floating dynamic to several food items commonly consumed by M. leprosa and T. scripta turtles, such as shards of algae, pieces of carrion, or slow-moving prey such as snails and other small mollusks (Newbery 1984; Parmenter and Avery 1990; Arnold and Ovenden 2002). From a hidden position, an experimenter recorded the number of food pellets that each turtle ingested, and the number of aggressive interactions (i.e., bites specifically directed to the competitor) that took place between the two members of the pair until all the food was consumed. Then, paired turtles were separated again and returned to their individual home aquaria, where they were fed ad libitum and ate their fill. Trials were replicated 5 times in different days, so that each

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turtle competed for 30 pieces of food within each experimental treatment throughout the whole experiment. Tests were spaced in time for two days so that possible stress resulting from one partner did not affect subsequent behavior with other partners. We did not fed turtles during these two days to encourage them to compete for food in the following trial.

Data analyses

To compare number food pellets ingested by each individual subject turtle across treatments, we used a three-way repeated measures analysis of variance (ANOVA), with the experimental treatments, competitor species (‘conspecific competitor’ vs. ‘heterospecific competitor’) and competitor sex (‘same sex competitor’ vs. ‘opposite sex competitor’), as two within-subjects factors. The species of the subject turtle was included as a between-subjects factor. Previous analyses showed that size differences between turtles were non-significant, as we intended in the selection of the experimental turtles based on similar body sizes. Therefore, size was not included in further analyses. Also, the sex of the subject turtle did not influence the food ingested by turtles, and thus, sex was not considered in final analysis. We verified data normality using Shapiro-Wilk’s test and tested for homogeneity of variances (Levene’s test). Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995).

To analyze agonistic behavior between turtles during feeding activity, we used log-linear models to compare the frequency of aggressive interactions across treatments (Sokal and Rohlf 1981). A four-way contingency table was generated by the factors species of the aggressor, sex of the aggressor, species of the subordinate (‘conspecific subordinate’ vs. ‘heterospecific subordinate’) and sex of the subordinate (‘same sex subordinate’ vs. ‘opposite sex subordinate’). Dominance between the two members of the pairs was established following the criterion of aggressions inflicted less aggressions suffered for each turtle of each pair, computing the 5 replicas of each trial, and defining the turtle with the highest positive sum as the dominant individual (Martín and Salvador 1993). Then, we used chi-square and binomial tests to compare dominance of turtles under intra vs. interspecific competition.

We used Spearman’s rank-order correlations to analyze the relationship between total amount of food ingested and aggressions inflicted and suffered by M. leprosa and T. scripta turtles, under both situations of intra and interspecific competition.

 

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RESULTS

We found significant differences between M. leprosa and T. scripta in total amount of food ingested (three-way repeated measures ANOVA, F = 14.43, df = 1,30, P < 0.001), with a greater overall percentage of food ingested by introduced sliders (55 ± 2 %) than by native terrapins (45 ± 2 %). There were no significant differences in food ingested by turtles under conspecific and heterospecific competition (F = 0.01, df = 1,30, P = 0.99), and the effect of the sex of the competitor was not significant (F = 0.01, df = 1,30, P = 0.99). However, the interaction between species of the subject turtle and species of the competitor was significant (F = 26.15, df = 1,30, P < 0.0001). Thus, food ingestion was similar between M. leprosa and T. scripta turtles under conspecific competition (Tukey’s test, P = 0.99), but under heterospecific competition, sliders ingested a greater percentage of food than Spanish terrapins (P = 0.004) (Fig. 2.1). Also, under heterospecific competition, M. leprosa turtles tended to reduce the amount of food ingested while T. scripta tended to increase it (P = 0.07 in both cases) (Fig. 2.1). The rest of the interactions were non-significant (F ≤ 0.013, df = 1,30, P ≥ 0.91).

Figure 2.1 Percentage of food (mean ± SE) ingested by introduced T. scripta and native M. leprosa under situations of conspecific (open rectangle) and heterospecific (dotted rectangle) feeding competition.

We observed 27 aggressive interactions in total during feeding competition. Aggressions were more frequently inflicted by introduced T. scripta than by native M. leprosa, and occurred more frequently between heterospecific individuals (Table 2.1). These differences were statistically significant, as shown by the fit of log-linear models to the four-way contingency table crossing the effects of the species of the aggressor, the sex of the aggressor, the species of the

T. scripta M. leprosa0

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subordinate and the sex of the subordinate. The sex of the aggressor did not significantly influence aggressiveness of turtles during feeding activity, but there was a tendency of male and female turtles close to signification to attack competitors of the opposite sex more often than competitors of the same sex. The rest of the interactions were non-significant (Table 2.2).

Overall dominance of turtles varied depending on the experimental treatment (intraspecific vs. interspecific competition); under intraspecific competition, dominance was established in 5/32 monospecific pairs of turtles (dominance was observed in 2/16 M. leprosa pairs and in 3/16 T. scripta pairs), while under interspecific competition, we observed dominance in 11/32 mixed

Table 2.1 Frequency of aggressions (bites within experimental pairs) observed during feeding competition between M. leprosa and T. scripta turtles, directed to conspecific and heterospecific individuals of the same and the opposite sex.

M. leprosa T. scripta

Subordinate Male Female Male Female

Conspecific Same sex 1 0 0 0 Opposite sex 1 0 3 0

Heterospecific Same sex 0 1 2 4 Opposite sex 2 0 6 7

Table 2.2 Results of the fit of log-linear models for the four-way contingency table generated by the factors species of the aggressor, sex of the aggressor, species of the subordinate and sex of the subordinate (df = 1 in all cases). Raw data are shown in Table 2.1.

Effect G 2 P

Species of the aggressor 8.62 0.003

Sex of the aggressor 0.26 0.61 Species of the subordinate 8.62 0.003 Sex of the subordinate 3.52 0.06 Species of the aggressor x sex of the aggressor 0.44 0.51 Species of the aggressor x species of the subordinate 1.50 0.22 Species of the aggressor x sex of the subordinate 0.80 0.37 Sex of the aggressor x species of the subordinate 2.25 0.13 Sex of the aggressor x sex of the subordinate 1.42 0.23 Species of the subordinate x sex of the subordinate 0.002 0.97 Species of the aggressor x sex of the aggressor x species of the subordinate 0.12 0.73 Species of the aggressor x sex of the aggressor x sex of the subordinate 0.27 0.60 Species of the aggressor x species of the subordinate x sex of the subordinate 0.37 0.54 Sex of the aggressor x species of the subordinate x sex of the subordinate 0.014 0.91

 

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pairs of M. leprosa and T. scripta (Pearson’s chi-square test, χ2 = 8.53, P = 0.004). Under interspecific competition, dominance of M. leprosa was observed in a lower number of pairs than under intraspecific competition (1/11 vs. 2/5), and dominance of T. scripta was observed in a higher number of pairs than under intraspecific competition (10/11 vs. 3/5) (χ2 = 4.38, P = 0.04). Within heterospecific pairs in which dominance could be established, T. scripta was clearly dominant over M. leprosa (10/11; two-tailed binomial test, P = 0.012).

Total amount of food ingested by M. leprosa under interspecific competition correlated positively with level of aggressiveness suffered by native terrapins (Spearman’s rank-order correlations, rs = 0.53, n = 16, P = 0.04). The rest of the correlations analyzing the relationship between food ingestion and suffered or inflicted aggressiveness were non-significant (M. leprosa: -0.41 ≤rs ≤ 0.25, n = 16, P ≥ 0.11 in all cases; T. scripta: -0.36 ≤ rs ≤ 0.19, n = 16, P ≥ 0.16 in all cases).

DISCUSSION In contrast with the ideal free distribution (IFD) model assumption that all foragers are equal in competitive skills, differing competitive abilities among individual foragers is widespread in nature (Holmgren 1995; Moody and Houston 1995; Spencer et al. 1995). In consequence, some competitors are able to exclude others through aggressive interactions (Schoener 1983). The results of this study show that feeding competition between native Spanish terrapins and introduced red-eared sliders follows this asymmetrical pattern. M. leprosa and T. scripta did not differ in total amount of food ingested under intraspecific competition but, when the two turtle species were forced to forage together, the access of M. leprosa to feeding resources was significantly restricted by T. scripta, which ingested a higher percentage of the food supplied. This suggests a greater competitive ability of introduced sliders in vying for feeding resources.

Our results further indicate that introduced T. scripta is a more aggressive species than native M. leprosa. Observed aggressions during feeding were mainly committed by sliders (more than 81 %), and aggressive interactions were much scarcer under intraspecific competition: less than 14 % of the aggressions committed by T. scripta were directed to conspecific competitors, while the rest of its agonistic behavior was directed to M. leprosa, which attacked sliders only in 3 occasions. Although escalated aggressive behavior was minority across the whole experiment, such a high percentage of aggressions directed by sliders to Spanish terrapins suggests that T. scripta is highly dominant over M. leprosa. Indeed, dominance by means of aggressiveness was significantly greater within pairs subjected to interspecific competition, in which T. scripta widely overcame M. leprosa. Moreover, heterospecific aggressions were consistently initiated by sliders and were never responded by native terrapins. In contrast, in

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the 3 exceptional cases in which M. leprosa attacked T. scripta, sliders immediately after established their superiority by displaying aggressive behavior (e.g., in one instance, a Spanish terrapin targeted the red spot behind the ear of its slider competitor, most probably confounding this characteristic spot with a food pellet. Immediately afterward, the slider responded biting the native terrapin).

The sex of the competitors had no significant effect either in the amount of food ingested, or in their aggressive behavior. However, turtles tended to attack more frequently competitors of the opposite sex, regardless their species identity. Males of both turtle species show lower volumes and weights than females for same body sizes (Polo-Cavia et al. 2009b). Because turtles were paired minimizing differences in body size, females might perceive other females as heavier and more dangerous competitors than males, thus avoiding intrasex confrontations. On the other hand, males might likely evade fighting with other males that might represent a double threat, since competition among males entails not only food resources but also females. Nevertheless, the last would imply sex recognition of heterospecific individuals, which has been poorly supported (Jackson and Davis 1972, Gibbons 1990).

Agonistic behavior during trials was possibly triggered by experimental conditions, since turtles were confined in experimental aquaria and food resources were highly limited in order to force competition. However, in sympatric populations in nature, dominance of introduced sliders over native terrapins might result in displacement of M. leprosa from preferred feeding areas by means of avoidance behavior. Avoidance is known to be used by inferior competitors to reduce interference from more competitive species (Menge and Menge 1974; Sloan 1984; Gaymer et al. 2002). This prediction is consistent with our previous observations that native M. leprosa avoids water pools with chemical stimuli of introduced T. scripta (Polo-Cavia et al. 2009a), presumably as a mechanism to evade aggressive encounters with sliders. By shifting to less profitable habitats, or by directly abandoning food resources, Spanish terrapins might evade costs of hostile interactions with aggressive sliders. Interestingly, percentage of food ingested by M. leprosa under interspecific competition correlated positively with level of aggressiveness suffered by native terrapins. We observed that daring M. leprosa which incurred in active competition for food pellets were harshly punished by aggressive sliders, while shier individuals that displayed a subordinate role were less attacked. This suggests the existence of a trade-off between feeding efficiency and costs of aggressive competition with sliders, which might lead M. leprosa to avoid feeding areas in where T. scripta forages and move away to look for alternative food sources, thus transferring the benefit of exploiting preferred areas to the introduced competitor.

 

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Many authors have suggested that resources partitioning and microhabitat use reduce interspecific competition for food among sympatric turtles (Moll 1976a; Vogt 1981; Williams and Christiansen 1981; Vogt and Guzman 1988). However, switching of inferior competitors to alternative less profitable diets and habitats widely occurs in nature as consequence of asymmetrical interaction between species (Abramsky et al. 1990; Nakano 1995; Gaymer 2001; Ovadia and zu Dohna 2003), and sometimes is hard to elucidate what is partition and what displacement (Kronfeld-Schor and Dayan 1999). For example, consume of animal prey by the omnivorous generalist musk turtle Kinosternon leucostomum has been observed to considerably decrease in localities in which this species coexists with a more specialized competitor (Staurotypus triporcatus), with negative consequences in growth and reproductive output (Vogt and Guzman 1988). Temporal partitioning (usually asymmetrical) is another viable mechanism for coexistence between competitive species (Kronfeld-Schor and Dayan 1999, 2003; Weinstein 2003). For example, interspecific displacement from preferred activity time for foraging has been observed among co-occurring gerbil species (Ziv et al. 1993). However, evolutionary constraints may limit the use of this diel niche axis. When partition occurs, the subordinate species normally experiences a cost in its efficiency of resource exploitation. Thus, interference and niche displacement is underlying the coexistence of many competitive species.

We consider that competition between native and introduced turtles observed in our experiment may be representative of interspecific competitive interactions occurring in the wild, for two main reasons. First, we used small pieces of commercial compound feed that may resemble food items that are part of the natural diet of M. leprosa and T. scripta turtles. Second, direct competition for food between M. leprosa and T. scripta is likely to occur in nature, since both turtle species are opportunistic omnivores, mainly predatory. Although more phytophagous than native terrapins, sliders are preferential carnivores when a high-protein diet is available (Gibbons 1990; Díaz-Paniagua et al. 2002; Pleguezuelos 2002). The two turtle species hunt in the same areas –shallow waters with abundant vegetation-, although M. leprosa may also forage in more open waters (Arnold and Ovenden 2002; Hart 1983). Also, the preferred activity time for feeding seems to overlap between native and introduced turtles. T. scripta eats at any time of the day, but usually in early morning and late afternoon (Cagle 1950; Newbery 1984), very likely interfering on feeding habits of M. leprosa (J.L. Rubio, unpubl. data). In addition, diurnal trapping produced few Spanish terrapins, while tending traps in early evening and prolonging trapping until next morning increased trapping success, probably indicating a more crepuscular or morning feeding activity of M. leprosa.

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In such ecological context, coexistence between the two turtle species likely implies a transaction between the greater competitiveness of T. scripta vs. the feeding efficiency of M. leprosa. Displacement in the feeding niche between competitive turtle species might lead to negative effects on growth rates and reproductive success of the subordinate species (Moll 1976b; Bury 1979; Gibbons et al 1979; Vogt and Guzman 1988). As a general pattern, an ever slight advantage of one competitor species leads to extinction of the other or to an evolutionary or behavioral shift of the inferior competitor towards a different ecological niche (Gause 1934; Hardin 1960). Among turtle species overlapping considerably in food and feeding areas, populations of the same species at different localities have been described to present or lack specific adaptive morphologies (e.g., wide jaws for crushing mollusks), depending on presence or absence of heterospecific competitors (Webb 1962; Berry 1975; Vogt 1981). Thus, loss of specialized-eating habits or adaptations that drop functionality in sympatry with a more specialized competitor –or a more competitive one-, and development of new strategies allowing exploitation of alternative ecological niches, might explain coexistence between “partial” competitors in sympatry. However, alien species can suddenly alter environments in such a way that indigenous organisms have no sufficient time to assimilate the new ecological contexts and respond to changes in their selective regime via evolution or learning (Schlaepfer et al. 2005). Consequently, native species may become trapped by morphological or behavioral traits that are no longer adaptive, experiencing reduced survival or reproduction. Within this frame, the feeding efficiency of native M. leprosa might result seriously compromised by interference competition with invasive sliders. Thus, the greater aggressiveness and competitive ability of introduced T. scripta in vying for food resources may be one of the causes that contribute to explain the current displacement of native populations of Spanish terrapins in the Iberian Peninsula. Acknowledgements We thank the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and the MCI project CGL2008-02119/BOS, and by a MEC-FPU grant to N. P.-C. The experiments comply with all the present Spanish laws of the Environmental Organisms of the “Comunidad de Madrid” where they were performed. REFERENCES Abramsky Z, Rosenzweig ML, Pinshow B, Brown JS, Kotler BP, Mitchell WA (1990) Habitat

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Interacciones competitivas durante la actividad de asoleamiento entre especies 

nativas e invasoras de galápagos 

Nuria Polo Cavia, Pilar López y José Martín

 

Biological Invasions (2009) In press

 

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RESUMEN

El galápago de Florida (Trachemys scripta elegans) se encuentra actualmente introducido en diversos países mediterráneos, donde se comporta como especie invasora, compitiendo y desplazando poblaciones nativas del protegido galápago leproso (Mauremys leprosa). Sin embargo, la forma en la que se producen las interacciones competitivas entre las dos especies es relativamente desconocida. Factores tales como un mayor tamaño corporal o adaptaciones pre-existentes, originadas en hábitats con alto grado de competencia interespecífica, podrían conferir ventajas competitivas al introducido T. scripta durante la actividad de asoleamiento. Así pues, la eficiencia termorreguladora de los galápagos nativos podría verse comprometida en una situación de competencia por los recursos de asoleamiento con el introducido galápago americano. En este trabajo, se analizó experimentalmente la actividad de asoleamiento de T. scripta y M. leprosa en situaciones de competencia intra e interespecífica por lugares de asoleamiento, ocasional y a largo plazo. Los galápagos nativos sometidos a competencia interespecífica redujeron su actividad de asoleamiento, se asolearon por periodos más cortos que los galápagos exóticos y evitaron compartir los lugares de asoleamiento con la especie introducida. Nuestros resultados sugieren el desplazamiento del galápago leproso durante el asoleamiento por parte del introducido galápago de Florida. Este detrimento en el comportamiento termorregulador de los galápagos nativos cuando se produce competencia directa por los recursos de asoleamiento con los galápagos exóticos podría conducir a una pérdida de eficiencia en las funciones fisiológicas de M. leprosa ligadas a la termorregulación, tales como la digestión o la respuesta locomotora, favoreciéndose así la expansión de la especie invasora ■

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COMPETITIVE INTERACTIONS DURING BASKING BETWEEN NATIVE

AND INVASIVE FRESHWATER TURTLE SPECIES

Abstract The red-eared slider (Trachemys scripta elegans) is currently introduced in many Mediterranean countries, where it behaves as an invasive species that competes and displaces native populations of the endangered Spanish terrapin (Mauremys leprosa). However, the nature of competitive interactions is relatively unknown. During basking activity, factors like greater body size or pre-existing behavioral adaptations to an original habitat with higher levels of interspecific competition might confer competitive advantages to introduced T. scripta with respect to native terrapins. We hypothesized that competition for basking places with the introduced T. scripta might negatively affect the efficiency of basking and thermoregulation of the native Spanish terrapin. We experimentally analyzed the basking activity of T. scripta and M. leprosa under occasional and long-term situations of intra and interspecific competition. Native M. leprosa subjected to interspecific competition reduced their basking activity, basked for shorter periods than T. scripta, and avoided basking stacked with the exotic turtles. These results suggested the displacement from the basking sites of the native terrapin by the introduced T. scripta. The decreased basking activity of native M. leprosa when competing directly for basking places with introduced sliders may lead native terrapins to a loss in the efficiency of physiological functions related to ineffective thermoregulation, such as digestion or locomotor performance, thus favoring the expansion of the invasive species. Keywords Basking • Freshwater turtles • Invasive species • Mauremys leprosa • Thermoregulation • Trachemys scripta

reshwater turtles spend much of their diel activity cycle basking on logs and stones that emerge from the water (Boyer 1965). As in most ectotherms, basking atmospherically serves as the main mechanism to

achieve thermoregulation in aquatic turtles (Boyer 1965; Crawford et al. 1983; Schwarzkopf and Brooks 1985; Meek and Avery 1988). Physiological processes occur optimally at the mean selected temperature of a species, and basking allows turtles to attain and maintain body temperatures close to this optimal temperature (Dawson 1975; Avery 1982; Huey 1982; Edwards and Blouin-Demers 2007). Turtles that bask benefit from a raised metabolic rate (Jackson 1971; Kepenis and McManus 1974; Dubois et al. 2008) that facilitates and increases the efficiency of their physiological processes (Crawford et al. 1983; Hammond et al. 1988; Ben-Ezra et al. 2008). Basking is especially important to maximize digestive processes (Moll and Legler 1971; Parmenter 1981; Gianopulos and Rowe 1999). Dermal synthesis of vitamin D (Pritchard and Greenhood 1968; Avery 1982) and secondary functions have also been attributed to aerial basking behavior, such as conditioning of the skin and shell by drying and ectoparasite removal (Cagle 1950; Neill and Allen 1954; Boyer 1965).

F

 

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The Spanish terrapin (Mauremys leprosa) is a semiaquatic medium-sized turtle that actively bask outside of water to achieve and maintain body temperatures within the intervals necessary for its daily activities (Meek 1983). M. leprosa is widespread in the southern and central Iberian Peninsula and northwestern Africa (Keller and Busack 2001), but its populations have considerably declined during recent decades, and it is currently considered an endangered species (Da Silva 2002). Habitat destruction and human pressure are the major factors responsible for this decline, but competition with exotic introduced turtles, mainly the American red-eared slider (Trachemys scripta elegans), might be worsening the state of the remaining populations (Da Silva and Blasco 1995; Pleguezuelos 2002). Although the nature of the interaction between sliders and Spanish terrapins is not clear, it is possible that direct competition for food, refuges or basking places is present (Crucitti et al. 1990). Recent studies indicated that sliders have diverse advantages over Spanish terrapins (Polo-Cavia et al. 2008, 2009a,b). Competition for basking sites has been described between sliders and the European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and field observations suggest that competition is very likely to occur also between sliders and the Spanish terrapin, as both turtle species are commonly forced to share basking sites (Díaz-Paniagua et al. 2002; Pleguezuelos 2002), such as emergent rocks or logs, which may be a restricted resource in the wild (Cadi and Joly 2003).

Competition for space may occur among conspecific or heterospecific turtles if basking substrates are limiting (Bury and Wolfheim 1973; Auth 1975; Bury et al. 1979; Pluto and Bellis 1986; Lovich 1988; Lindeman 1999). In such situations, body size may play an important role in determining the outcome of the competitive interaction (Bury and Wolfheim 1973; Auth 1975; Lindeman 1999). Consequently, differences in body size between sliders and native turtles might possibly favor invasive species during basking interactions, since T. scripta reaches larger adult body size on average than native freshwater turtles (Da Silva and Blasco 1995; Arvy and Servan 1998). If direct competitive interactions are disadvantageous for native terrapins, they would likely avoid basking places occupied by T. scripta, thus favoring the invasive species. Also, in the original habitats of T. scripta, the species richness of most chelonian assemblages is dramatically higher compared with that of the Iberian assemblages (only two turtle species: M. leprosa and E. orbicularis), which may confer competitive advantages to invasive sliders over native Iberian terrapins. Adapted to environments with greater levels of interspecific competition and aggressiveness, sliders can easily monopolize the most suitable basking sites in their new habitats, where they have been introduced, impeding basking by native turtles (Cadi and Joly 2003), probably contributing to the loss of weight and decreased survival of native terrapins after long-term competition with

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sliders (Cadi and Joly 2004). Since basking is a vital activity in regions where mean temperatures fall below minimum thermal requirements (Hutchison and Maness 1979; Crawford et al. 1983), interference in basking behavior of Spanish terrapins caused by sliders might severely affect the efficiency of thermoregulation and physiological functions of the native species. A decrease in thermoregulatory behavior of native M. leprosa might be one of the causes that contribute to the observed displacement of their populations.

In this study, we experimentally tested the hypothesis that competitive interactions occur between the introduced red-eared slider (T. scripta) and the Spanish terrapin (M. leprosa) during basking activity when basking resources were limited. Our objectives were to determine 1) whether alteration in time spent basking by native Spanish terrapins occurred under occasional and/or long-term interspecific competition with sliders, in comparison with situations of intraspecific competition, and 2) whether invasive sliders had a consistent advantage over Spanish terrapins in competition for basking space.

METHODS

Study animals

During spring, as a part of a long-term study, we captured Spanish terrapins (M. leprosa) with baited funnel traps in several ponds and tributary streams of the Manzanares River (Madrid Province, Spain). We also obtained red-eared sliders (T. scripta) from a large seminatural outdoor pond (Madrid Province, Spain), where they had been maintained by the conservationist organization “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These turtles originated from introduced populations in central Spain.

All turtles were housed in outdoor aquaria at “El Ventorrillo” Field Station (Navacerrada, Madrid Province), about 20-30 km from the capture sites. The temperature and photoperiod were the same as the natural surroundings. Turtles were fed mince meat, earthworms and slugs three times a week. Turtles were held in captivity for at least two weeks before experiments to allow them to habituate to captivity conditions. At the end of experiments, all turtles had maintained their body mass and were returned to the GREFA ponds (sliders) or to their exact field capture sites (Spanish terrapins). The experiments enforced all the present Spanish laws of the Environmental Organisms of Madrid and Community where they were carried out.

Occasional competition

In a first experiment, we compared the use of basking sites by M. leprosa in situations of both intra and interspecific competition and with competitors of

 

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the same and the opposite sex. Spanish terrapins (straight-line carapace length: mean ± SE = 15.2 ± 0.4 cm, range = 10.0-20.4 cm, n = 27) were individually housed in home aquaria (60 x 40 x 30 cm) that were filled with water and contained a single brick (24 x 11.5 x 7 cm) emerging 1 cm above water surface. Turtles were completely free to bask on the brick before and after the experiments.

Trials took place outdoors, in aquaria like the home aquaria, but that had not housed any experimental turtle before the trials. For the trials, each Spanish terrapin was paired, according with its body size, with (1) a conspecific of the same sex, (2) a conspecific of the opposite sex, (3) a heterospecific (T. scripta) of the same sex, and (4) a heterospecific of the opposite sex. Each M. leprosa subject was tested once in each of the four experimental treatments in a random order. Both members of the pairs were introduced together in the experimental aquaria. During the trials, turtles were able to bask on the brick, one at a time, or stacked one on top of the other, given the small surface area available for basking. After each trial, paired turtles were separated again and returned to their individual home aquaria. Tests were spaced in time for at least two days so that possible stress resulting from one partner did not affect subsequent behavior in further tests. Turtles were not fed the day that they were tested. An instantaneous scan sampling method was used and each pair of turtles was monitored during 3 h, recording every 5 min the location of each M. leprosa subject (36 scans per turtle per day in total). We checked that water and air temperatures, illumination, and water depth were similar among tests.

Long-term competition

In a second experiment, the basking patterns of M. leprosa and T. scripta were analyzed, in long-term situations of intra and interspecific competition, when they shared their home aquaria with a conspecific or a heterospecific partner respectively. We used 13 M. leprosa (straight-line carapace: mean ± SE = 14.6 ± 0.4 cm, range = 12.3-16.6 cm) and 11 T. scripta (straight-line carapace: mean ± SE = 13.7 ± 0.6 cm, range = 10.9-16.4 cm) to compose experimental and control pairs of turtles. Each pair was placed into one home aquarium (60 x 40 x 30 cm). Experimental pairs consisted of one Spanish terrapin and one slider of the same sex and similar size, whereas the control pairs were made up of two individuals of the same species and sex, and similar size. A single brick (24 x 11.5 x 7 cm) in each home aquarium forced turtles to compete for basking, as in the first experiment. All turtles were simultaneously introduced into the aquaria, which they occupied during the whole experiment. Turtles remained untested for two weeks prior to observations to allow them to accustom to the competition situation. All turtles had been fed ad libitum the day before the trials and every

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day after finishing the observations, but turtles were not fed during the observations to standardize hunger levels and avoid effects of feeding status on basking activity (Hammond et al. 1988, Dubois et al. 2008).

We used the instantaneous scan sampling method to monitor each pair of turtles from 11:00 to 13:30 h, scanning continuously from a hidden position, and recording every 10 min the location of the turtles (16 scans per pair per day in total). Water and air temperatures were also recorded with digital thermometers (precision ± 0.1 °C). We replicated observations of basking behavior of each pair of control or experimental turtles for 10 non-consecutive days. From the scans, we calculated the percentage of basking activity at each time of day and the average and maximum length of basking events for each turtle, halfway through the 10 days. Length of basking bouts was ensured by confirming visually the persistence of each turtle’s location during the inter-scan intervals. The dates for observation were selected depending on the meteorological conditions (i.e., sunny weather). The interval between tests was of at least 24 h. We controlled the extent of illumination by sunlight and water depth to ensure that they were similar in all home aquaria during the tests and did not affect the turtle responses (De Rosa and Taylor 1980). Terraria with the different treatments were placed randomly, and turtles in all the treatments were tested in parallel in each day.

Data analyses In the first experiment, we used a three-way repeated measures analysis of variance (ANOVA) to analyze the differences in number of observations in which basking was occurring (‘basking activity’) across treatments by the same individual subject M. leprosa. The experimental treatments, competitor species (‘conspecific competitor’ vs. ‘heterospecific competitor’) and competitor sex (‘same sex competitor’ vs. ‘opposite sex competitor’), were included as two within-subjects factors. The sex of the subject turtle was included as a between-subjects factor.

In the second experiment, we used a three-way repeated measures ANOVA to test for differences in basking patterns of M. leprosa and T. scripta under control and experimental treatments (‘intraspecific competition’ vs. ‘interspecific competition’) in each instantaneous scan. Percent time of basking activity was calculated for each turtle in each time of day as the proportion of days that turtles were observed basking in each one of the respective scans. Time of day was included as a within-subjects factor. The species of the subject turtle and the treatment were included as two between-subjects factors. To analyze differences in continuity of basking activity between the two turtle species (measured as the average length of basking events and maximum length

 

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of basking events halfway through the 10 days), we used two-ways repeated measures ANOVAs with the species of the subject turtle and the treatment (‘intraspecific competition’ vs. ‘interspecific competition’) as two between-subjects factors.

To test for differences between basking activity of M. leprosa in both ‘alone’ and ‘stacked’ situations, we analyzed data from the first experiment with a four-way repeated measures ANOVA with the sex of the subject turtle and the sex and species of the competitor as described above, but we also included the basking situation (‘alone’ vs. ‘stacked’) as an additional within-subjects factor.

In all cases, data normality was verified by Shapiro-Wilk’s test and tests of homogeneity of variances (Levene’s test) showed that variances were not significantly heterogeneous. Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995). RESULTS

Basking activity of M. leprosa in situations of occasional competition The species of the competitor significantly influenced the percent time that individual M. leprosa spent basking in transitory situations of competition (three-way repeated measures ANOVA, competitor species: F = 8.21, df = 1,25, P = 0.008). Individual M. leprosa clearly reduced their basking activity when the competitor was a T. scripta (average basking activity with conspecific competitors: mean ± SE = 66 ± 8 %; with heterospecific competitors: 55 ± 8 %) (Fig. 3.1a). No significant differences between male and female M. leprosa were observed in overall percent time that turtles spent basking (subject sex: F = 0.34, df = 1,25, P = 0.57), and the sex of the competitor did not significantly influence basking activity of individual M. leprosa (competitor sex: F = 0.55, df = 1,25, P = 0.47). Male M. leprosa showed a tendency to reduce their basking activity when the competitor was a female, while female M. leprosa tended to increase the time spent basking when the competitor was a male, but differences did not reach statistical significance (subject sex x competitor sex: F = 3.08, df = 1,25, P = 0.09) (Fig. 3.2). All other interactions were non-significant (subject sex x competitor species: F = 0.60, df = 1,25, P = 0.45; competitor sex x competitor species: F = 0.22, df = 1,25, P = 0.64; subject sex x competitor sex x competitor species: F = 0.21, df = 1,25, P = 0.65). Thus, basking activities of male and female M. leprosa were similarly restricted under occasional competition by heterospecific T. scripta competitors independently of the sex of the competitor (Fig. 3.2).

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Figure 3.1 Percent time (mean ± SE) spent basking by (a) M. leprosa in occasional situations of intra (open rectangle) and interspecific (dotted rectangle) competition, and (b) T. scripta and M. leprosa under long-term competition situations, when they shared the home aquaria and the basking site with a conspecific (open rectangle) and a heterospecific (dotted rectangle) competitor

 

                   

Basking patterns of T. scripta and M. leprosa under long-term competition Significant differences were observed in overall percent time spent in basking activity by T. scripta and M. leprosa under prolonged situations of competition (three-way repeated measures ANOVA, species: F = 5.64, df = 1,20, P = 0.028). Thus, sliders spent more time basking (mean ± SE = 69 ± 7 %) than Spanish terrapins (46 ± 7 %) during the whole experiment. The effect of the treatment was non-significant (treatment: F = 0.65, df = 1,20, P = 0.43), but the interaction between species and treatment was significant (F = 4.65, df = 1,20, P = 0.043) (Fig. 3.1b). T. scripta spent more time basking than M. leprosa under interspecific competition (Tukey’s test, P = 0.031), but there were no significant differences

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Figure 3.2 Percent time (mean ± SE) spent basking by male and female M. leprosa when they shared the basking site with a conspecific (open rectangle) or a heterospecific (dotted rectangle) of the same and the opposite sex

between the two species under intraspecific competition (P = 0.99). Differences in basking activity between treatments were non-significant for T. scripta (P = 0.23) and neither were significant for M. leprosa (P = 0.74).

Significant differences were observed in overall basking activity of turtles through the day (time of day: F = 10.47, df = 15,300, P < 0.001), which is explained by the increased basking activity as a result of a lower water temperature than air temperature (Spearman’s rank-order correlation between basking activity and time of day; rs = 0.90, n = 8, P = 0.0024). Basking activity decreased when water temperature became greater than air temperature (rs = -0.95, n = 8, P = 0.0003) (Fig. 3.3). All the interactions between time of day and species or treatments were no significant (time of day x species: F = 0.60, df = 15,300, P = 0.87, time of day x treatment: F = 0.42, df = 15,300, P = 0.97; time of day x species x treatment: F = 1.04, df = 15,300, P = 0.42) (Fig. 3.4).

There were significant differences in the average length of basking events between species (two-way repeated measures ANOVA, species: F = 6.55, df = 1,20, P = 0.019), with sliders basking for longer periods on average (mean ± SE = 98 ± 12 min) than Spanish terrapins (58 ± 11 min). Differences between treatments were non-significant (treatment: F = 0.42, df = 1,20, P = 0.52), but the interaction between species and treatment was significant (F = 5.02, df = 1,20, P = 0.037). Under interspecific competition, average basking events of T.

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scripta (121 ± 19 min) were significantly longer than those of M. leprosa (45 ± 14 min) (Tukey’s test, P = 0.021), but average duration of basking events did not significantly differ between species under intraspecific competition (T. scripta: 76 ± 14 min; M. leprosa: 71 ± 15 min) (P = 0.99). There were no significant differences between intraspecific and interspecific competition in average length of basking periods in either species (T. scripta: P = 0.25; M. leprosa: P = 0.63).

Figure 3.3 (a) Daily temporal variation (mean ± SE) of air and water temperatures during the trials, and (b) associated variation in overall basking activity of turtles. Linear fit breaks at the point in which air and water temperatures coincide

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Figure 3.4 Daily basking patterns of T. scripta and M. leprosa (mean ± SE of percent time spent basking for each time of day), under long-term situations of intra and interspecific competition

Differences in overall longest basking event between species were significant (two-way repeated measures ANOVA, species: F = 6.50, df = 1,20, P = 0.019). Maximum length of T. scripta basking events (mean ± SE = 104 ± 12 min) was greater than maximum length of M. leprosa basking events (64 ± 10 min). The effect of the treatment was non-significant (treatment: F = 0.62, df = 1,20, P = 0.44), but the interaction between species and treatment was significant (F = 5.27, df = 1,20, P = 0.033). Significant differences between maximum length of T. scripta and M. leprosa basking events under interspecific competition was observed (129 ± 19 min vs. 53 ± 14 min respectively, Tukey’s test, P = 0.02), but not under intraspecific competition (80 ± 14 min vs. 76 ± 15 min, P = 0.99). Differences between intraspecific and interspecific competition were not significant for either species (P ≥ 0.20 in both cases).

Alone and stacked basking activity of M. leprosa

Overall percent time that M. leprosa spent basking alone (mean ± SE = 18 ± 4 %) was significantly lower than overall percent time that it spent basking stacked (41 ± 8 %) (four-way repeated measures ANOVA, basking situation: F = 27.70, df = 1,25, P < 0.001). The sex of the subject turtle did not influence the basking situation (basking situation x subject sex: F = 0.28, df = 1,25, P = 0.60), and neither did the sex of the competitor (basking situation x competitor sex: F =

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0.11, df = 1,25, P = 0.75), but the species of the competitor had a significant effect on basking situation (basking situation x competitor species: F = 5.81, df = 1,25, P = 0.024) (Fig. 3.5). When the competitor was a conspecific, percent time spent by individuals M. leprosa basking alone was significantly lower than percent time spent basking stacked (Tukey’s test, P = 0.004), but there were no significant differences in basking activity between alone and stacked situations when the competitor was a heterospecific (P = 0.50). Differences in alone or stacked basking activity between basking with conspecific and heterospecific competitors were non-significant (basking alone: P = 0.92; basking stacked: P = 0.31). The interaction between sex of the subject turtle, sex of the competitor and basking situation was non-significant (F = 3.35, df = 1,25, P = 0.08), but males showed a tendency to spend more time basking alone with a competitor of the same sex while females tended to spend more time basking alone with a competitor of the opposite sex. The rest of the interactions were non-significant (F ≤ 1.72, df = 1,25, P ≥ 0.20 in all cases).

Figure 3.5 Percent time (mean ± SE) spent basking alone and stacked by M. leprosa when they competed for the basking site with a conspecific (open rectangle) or a heterospecific (dotted rectangle)

DISCUSSION The results of our experiments suggest that the presence of invasive sliders alters the basking behavior of native Spanish terrapins. Basking activity of native terrapins subjected to occasional competition situations was significantly lower when the competitor was a slider than when it was a conspecific (first experiment; see Fig. 3.1). Results from the second experiment showed that

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basking activity of M. leprosa was similar to basking activity of T. scripta when turtles shared their home aquaria with conspecific competitors, but when turtles underwent a situation of long term interspecific competition, significant differences in continuity and total time devoted to basking appeared between the two species. In such situation, average and maximum length of the basking events and percent time spent basking by T. scripta were greater than those of M. leprosa. Although differences in continuity and total activity of basking between intra and interspecific competition did not reach statistical significance for either species, T. scripta showed a more efficient occupation of basking resources than M. leprosa under inter but not under intraspecific competition, suggesting the dominance of the introduced species over the native one. Similarly, Cadi and Joly (2003) found that T. scripta outcompeted the European pond turtle, Emys orbicularis, for preferred basking places of experimental ponds (i.e., floating platforms in middle position, surrounded by deep water) in mixed-species groups.

Differences in the magnitude of the effects between the two experiments might be due to the different kinds of competition turtles encountered. While in the second experiment turtles were subjected to prolonged maintained conditions of intra and interspecific competition, in the first experiment, the effect of competition for basking places with a more competitive species might be amplified by the transitory and the new nature of the competition. We hypothesize that M. leprosa had less incentive to compete with sliders for basking sites in the first experiment, given that their basking requirements were regularly satisfied before the trials (because they were housed individually). On the other hand, in the second experiment, M. leprosa suffering from the cumulative effects of deficient basking during several consecutive days might be able to assess the costs of a long-lasting competition with sliders and consequently increase their investment in basking competitive interactions, thus reducing the differences in basking behavior between situations of intra and interspecific competition. Further experiments addressing this hypothesis would be interesting. Nevertheless, negative effects of long-term competition with exotic turtles are expected to persist in the wild, since basking sites are limited, and optimal time for basking is restricted on an annual basis, especially in Mediterranean countries. Thus, native M. leprosa could hardly optimize basking by intercalating their basking bouts within the activity of a more competitive species.

Although time devoted to basking activity of native turtles was similarly restricted by invasive competitors through the whole time of the trials, interferences in temporal patterns of basking of the two species did not occur. Thus, patterns of basking throughout the day performed by invasive and native turtles under interspecific competition were similar to those performed by each

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species under intraspecific competition; both sliders and Spanish terrapins regularly basked atmospherically while air temperature was higher than water temperature and both species reduced their basking activity and spent more time immersed in the water once water temperature became greater than air temperature. This fact supports the hypothesis that thermoregulation is the primary function of basking behavior in freshwater turtles (Boyer 1965; Moll and Legler 1971; Standora 1982; Crawford et al. 1983; Meek and Avery 1988). Therefore, competition for basking sites and decreased basking periods of native terrapins may have important consequences for thermoregulation, with subsequent physiological costs (e.g., Huey 1982; Hammond et al. 1988; Ben-Ezra et al. 2008).

Sex did not appear to affect basking activity of native turtles. Male and female M. leprosa clearly reduced their efficiency in occupying basking sites when competing with sliders, independently of the sex of the competitor, thus indicating that male and female exotic turtles may pose similar dominance over native terrapins. However, male and female M. leprosa tended to spend less time basking when the competitor (conspecific or heterospecific) was a female, likely due to the minimum differences remaining in body size between competitors. Females, which are usually larger than males, might be more successful when competing for basking sites. Higher basking requirements of females related to egg production might be an alternative explanation for this tendency (Lefevre and Brooks 1995; Krawchuk and Brooks 1998; Carrière et al. 2008).

Regarding alone and stacked basking, male and female M. leprosa contrarily tended to spend more time basking stacked with a female competitor (conspecific or heterospecific), which suggests avoidance of physical contact with males by females and between males during basking events. However, there was no statistical significance. Also, native turtles spent more time basking stacked with conspecific competitors than basking alone, but percent times that native turtles spent basking alone and stacked with heterospecific competitors were similar. Considering that the availability of empty basking sites was half the availability of shared ones, M. leprosa terrapins seemed reluctant to share basking sites with heterospecifics, while they did not avoid sharing them with conspecifics. In this regard, Cady and Joly (2003) reported that E. orbicularis shied away from climbing onto a basking site that was already occupied by a T. scripta. They suggested remote identification and active avoidance of interactions with heterospecific competitors by the native species. Also, avoidance by M. leprosa of water with chemical cues of T. scripta has been experimentally demonstrated (Polo-Cavia 2009a), which suggests that Spanish terrapins actively avoid areas occupied by introduced sliders.

 

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If direct competitive interactions with a more aggressive competitor are disadvantageous for native terrapins, they would likely avoid basking sites occupied by sliders, thus reducing considerably the availability of basking resources for the native species and favoring the exploitation of basking sites by the invasive one. A restricted occupation of basking sites might lead to a detriment in efficiency of thermoregulatory behavior of M. leprosa. Deficiencies in thermoregulation negatively affect physiological functions such as food ingestion and digestion (Parmenter 1981; Zimmerman and Tracy 1989; Gianopulos and Rowe 1999), dermal synthesis of vitamin D (Pritchard and Greenhood 1968; Avery 1982), conditioning of the skin and the shell (Cagle 1950; Boyer 1965; Vogt 1979), and may also retard maturation of ova (Ganzhorn and Licht 1983; Mendonca 1987; Sarkar et al. 1996; Rollinson and Brooks 2007). Similarly, such negative consequences of inefficient basking may explain the lower survival rates of E. orbicularis when competing with sliders (Cadi and Joly 2004). In our experiment, native terrapins subjected to interspecific competition ultimately spent insufficient time basking and they basked for shorter periods than T. scripta, which suggests not only avoidance behavior by M. leprosa but also superimposition and active displacement by sliders. However, it is probable that wild Spanish terrapins simply avoid disturbance by shifting their basking activity to less preferred basking sites (Cady and Joly 2003) or to the shores of the ponds, in contrast to the safer basking places emerging in open deep water in the center of the ponds, thus incurring additional costs such as higher predation risk (López et al. 2005; Polo-Cavia et al. 2008). This avoidance behavior and consequent detriment in basking activity of M. leprosa might play an important role in explaining the observed displacement of their populations by the invasive T. scripta.

Our study further clarifies the nature of the basking interactions between the introduced sliders and the Iberian turtle species. The results of our experiments coincide and reinforce those recorded by Cadi and Joly (2003), who observed that native E. orbicularis sharing experimental ponds with sliders occupied basking places of lower quality, while sliders monopolized the preferred basking sites, in absence of agonistic behavior. Factors like differences in body size or a higher aggressiveness, probably due to a “more competitive” original habitat, might explain why T. scripta appear more competitive than the two Iberian turtle species during basking activity. Body size has been shown to play a role in determining the outcome of competitive interactions (Bury and Wolfheim 1973; Auth 1975; Lindeman 1999). Although wild red-eared sliders reach larger body sizes in adulthood than Iberian freshwater turtles (Da Silva and Blasco 1995; Arvy and Servan 1998), turtles from our experiments were paired basing on body size criteria, thus minimizing these differences between the two members of the pair. Consequently, we suggest that other factors such

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as the complexity of interactions among species in the original habitats of the introduced T. scripta would also have a significant implication in explaining the competitive advantages of the exotic species. For example, whereas most Iberian wetlands are occupied by only one or two turtle species (M. leprosa and E. orbicularis), in some assemblages of south Alabama and Mississippi, T. scripta may share their original habitats with many other turtle species, such as Pseudemys floridana, Deirochelys reticularia, Sternotherus odoratus, Kinosternon subrubrum, or Chelydra serpentina (Gibbons 1990). As a result of adaptation to highly competitive environments, sliders are likely endowed with greater competitive abilities than Iberian terrapins. Nevertheless, differences in body size between invasive and native turtles living in the field may favor the introduced competitors, resulting in a more severe displacement of Iberian turtles.

The results of this study may have implications for conservation of wild populations of Spanish terrapins that are suffering competition with introduced sliders. Very often, appropriate basking sites such as emerging logs or rocks are limited and sliders can monopolize progressively these few sites displacing native terrapins (Díaz-Paniagua et al. 2002; see also Cadi and Joly 2003). Although capture and extraction of introduced sliders may be the more effective method, a temporal measurement to help native terrapins could be to provide additional artificial basking platforms (e.g., floating wooden platforms). These new solaria are readily used by turtles (Cadi and Joly 2003, 2004) and might decrease direct competition for basking sites. Therefore, our study stressed the importance of further studies analyzing in detail how competitive interactions between native and introduced species occur in order to design adequate management measurements.

Acknowledgements We thank two anonymous reviewers for helpful comments, the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and the MCI project MCI-CGL2008-02119/BOS, and by an “El Ventorrillo” CSIC grant and a MEC-FPU grant to N. P.-C.

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Avery RA (1982) Field studies of body temperatures and thermoregulation. In: Gans C, Pough FH (eds) Biology of the Reptilia, Vol 12. Academic Press, New York, pp 93-166

Ben-Ezra E, Bulté G, Blouin-Demes G (2008) Are locomotor performances coadapted to preferred basking temperature in the Northern Map Turtle (Graptemys geographica)? J Herpetol 42: 322-331

 

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Jackson DC (1971) The effect of temperature on ventilation in the turtle, Pseudemys scripta elegans. Respir Physiol 12: 131-140

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Keller C, Busack SD (2001) Mauremys leprosa (Schweigger, 1812)-Maurische Bachschildkröte. In: Fritz U (ed) Handbuch der Reptilien und Amphibien Europas, Vol 3/IIIA, Schildkröten (Testudines) I. Aula-Verlag, Wiesbaden, pp 57-88

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Meek R (1983) Body temperatures of a desert population of the stripe-necked terrapin, Mauremys caspica. Brit J Herpetol 6: 335-337

Meek R, Avery RA (1988) Thermoregulation in chelonians. Herpetol J 1: 253-259 Mendonca MT (1987) Photothermal effects on the ovarian cycle of the Musk Turtle, Sternotherus

odoratus. Herpetologica 43: 82-90 Moll EO, Legler JM (1971) The life history of a neotropical slider turtle, Pseudemys scripta

(Schoepff) in Panama. Sci Bull Nat Hist Mus Los Angeles Co 11: 1-102 Neill WT, Allen ER (1954) Algae on turtles: some additional considerations. Ecology 35: 581-584 Parmenter RR (1981) Digestive turnover rates in freshwater turtles: the influence of temperature

and body size. Comp Biochem Physiol A 70: 235-238 Pleguezuelos JM (2002) Las especies introducidas de Anfibios y Reptiles. In: Pleguezuelos JM,

Márquez R, Lizana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Asociación Herpetológica Española-Ministerio de Medio Ambiente, Madrid, pp 501-532

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Polo-Cavia N, López P, Martín J (2009a) Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biol Invas 11: 431-440

Polo-Cavia N, López P, Martín J (2009b) Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biol Invas 11: 1755-1765

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population of Painted Turtles (Chrysemys picta): an empirical test of the bet-hedging paradigm. Can J Zool 85: 177-184

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free-ranging yellow-bellied turtles, Pseudemys scripta. PhD Dissertation, University of Georgia

 

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Vogt RC (1979) Cleaning/feeding symbiosis between grackles (Quiscalus: Icteridae) and map turtles (Graptemys: Emydidae). The Auk 96: 608-609

Zimmerman LC, Tracy CR (1989) Interactions between the environment and ectothermy and herbivory in reptiles. Physiol Zool 62: 374-409

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Las diferencias interespecíficas  en las tasas de intercambio de calor pueden afectar a la competencia entre galápagos 

introducidos y nativos 

Nuria Polo Cavia, Pilar López y José Martín

Biological Invasions 11 (2009) 1755–1765

 

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RESUMEN

En la Península Ibérica, el galápago de Florida (Trachemys scripta elegans) es una especie introducida que se comporta como invasora, desplazando a las poblaciones nativas de galápago leproso (Mauremys leprosa), una especie protegida. Sin embargo, la naturaleza de las interacciones competitivas entre las dos especies no se conoce con seguridad. En zonas templadas, los mecanismos que maximicen la retención de calor corporal podrían resultar selectivamente ventajosos para las especies de galápagos, puesto que los individuos tienden a perder rápidamente el calor adquirido mediante asoleamiento al entrar en el agua. Así, es posible que ciertas diferencias en la morfología, y por tanto en las tasas de calentamiento y enfriamiento, puedan conferir ventajas competitivas al introducido T. scripta. En este trabajo, comparamos la relación superficie-volumen de ambas especies de galápagos a partir de medidas biométricas, y sus efectos en las tasas de intercambio de calor. T. scripta presenta una forma más redondeada, una menor relación superficie-volumen y una mayor inercia térmica, lo que facilita la retención de calor y favorece el desarrollo de actividades y funciones fisiológicas tales como la búsqueda de alimento o la digestión. Estas características del galápago invasor podrían permitirle competir ventajosamente con los galápagos nativos en los hábitats mediterráneos ■

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INTERSPECIFIC DIFFERENCES IN HEAT EXCHANGE RATES MAY AFFECT COMPETITION BETWEEN INTRODUCED AND NATIVE

FRESHWATER TURTLES

Abstract In the Iberian Peninsula, the red-eared slider (Trachemys scripta elegans) is an introduced invasive species that is displacing the endangered native Spanish terrapin (Mauremys leprosa). However, the nature of competitive interactions is relatively unclear. In temperate zones, mechanisms for maximizing heat retention could be selectively advantageous for aquatic turtle species, since individuals usually lose the heat gained from basking very rapidly when entering the water. We hypothesized that interspecific differences in morphology, and thus, in heating and cooling rates, might confer competitive advantages to introduced T. scripta. We compared the surface-to-volume ratios of both, introduced and native turtles, basing on biometric measures, and their effects on thermal exchange rates. T. scripta showed a more rounded shape, a lower surface-to-volume ratio and a greater thermal inertia, what facilitates body heat retention and favors the performance of activities and physiological functions such as foraging or digestion, thus aggravating the competition process with native turtles in Mediterranean habitats. Keywords Freshwater turtles • Heat exchange rates • Invasive species • Mauremys leprosa • Thermoregulation • Trachemys scripta

hermoregulation in aquatic turtles, as in most ectotherms, is primarily achieved through behavioral changes (Hutchison and Maness 1979; Sturbaum 1982; Meek and Avery 1988). Freshwater turtles simply

achieve preferred body temperatures switching between basking outside of water and water immersion, avoiding extreme thermal environments. Although basking behavior of aquatic turtles has long been known, there has been considerable speculation around this behavior, and their specific functions remain unclear. The consensus is that the primary function of basking is thermoregulatory (Boyer 1965; Moll and Legler 1971; Standora 1982; Crawford et al. 1983; Meek and Avery 1988) though more recent studies have pointed out contradictory results (Manning and Grigg 1997). Increased body temperature speeds digestion (Parmenter 1981; Gianopulos and Rowe 1999), and may also speed maturation of ova (Obbard and Brooks 1979; Whittow and Balazs 1982). Cagle (1950) suggested that basking serves a variety of needs in turtles apart from thermoregulation, as conditioning of the skin and shell, avoiding infections by drying and the antibiotic effects of the ultraviolet component of sunlight. Basking also contributes to dermal synthesis of vitamin D (Pritchard and Greenhood 1968; Avery 1982). An interesting point is that freshwater turtles usually lose the heat gained from basking very rapidly when they re-entry to water (Avery 1982; Bartholomew 1982). Turtles that have achieved high body temperatures basking in air may be exposed abruptly to chilling conditions when they dip into water, particularly during spring and fall in

T

 

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middle latitudes. Consequently, mechanism for maximizing heat retention, or even heat production could be selectively advantageous for aquatic species.

Basically, turtles’ abilities to retain and produce heat rest on morphological and physiological specific determining factors (Ernst 1972; Hutchison 1979). The hemispherical shape of turtles gives them relatively small surface-to-volume ratios when compared with other reptiles of the same size, thus minimizing their rates of heat exchange with the environment, and increasing the inertial homeothermy as bigger they are (Bartholomew 1982). Boyer (1965) demonstrated the influence of shell shape on heating rates of freshwater turtles belonging to different genera. Body size and surface-to-volume ratio are clearly correlated with thermal rates in aquatic turtles (Spray and May 1972; Gronke et al. 2006). Also, the presence of a bony shell may influence thermal gradients following insolation. On the other hand, when behavioral strategies are not sufficient to maintain optimal body temperatures within required limits, some turtles can use physiological mechanisms of control of body temperatures for short periods of time. For example, physiological thermoregulatory systems could be based on heat transference mediated by thermal conductivity (Weathers 1970; Weathers and White 1971; Cloudsley-Thompson 1974), respiratory responses to hyperthermia (Sturbaum 1982) or vasomotor responses with adjustments of blood flow within the body (Bartholomew 1982; Turner 1982). Although small differences in morphology and physiological control of rate of change in body temperature are almost trivial when compared with the control by postural adjustments and choice of microhabitat, we should not discard their implications in thermoregulatory behavior of freshwater turtles.

The Spanish terrapin (Mauremys leprosa) is a semiaquatic medium-sized turtle widespread in the South and Central Iberian Peninsula and northwestern Africa (Keller and Busack 2001). These turtles are predominantly aquatic, but they need to come to land for basking to achieve and maintain body temperature within the intervals necessary for their daily activities (Meek 1983). This is an endangered species which populations have considerably declined during the last decades (Pleguezuelos et al. 2002). Habitat destruction and human pressure are the major responsible for this decline, but competition with exotic introduced turtles, mainly the American red-eared slider (Trachemys scripta elegans), might be worsening the state of the remainder populations (Da Silva and Blasco 1995; Pleguezuelos 2002). However, it is not clear how interspecific competitive interactions with sliders are taking place. It is possible that direct competition for food, refuges or basking places is present (Crucitti et al. 1990). Competition for basking places has been described between sliders and the European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and it also occurs between sliders and the Spanish terrapin (Polo-Cavia et al. in press). Sliders can monopolize the most suitable basking places, impeding

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native turtles to adequately bask (Cadi and Joly 2003). However, the effects of morphological and physiological differences, per se, between species on thermoregulatory abilities of native and invasive species of aquatic turtles have never been analyzed. This can be, however, important for the outcome of competitive interactions between freshwater turtles. While each turtle species has probably evolved to optimize their thermal exchange rates in their natural habitat and original conditions, the new situation caused by man (i.e., the introduced species occupies new environmental conditions and the native species faces competition with it) might result in that the original thermoregulatory adaptations conferred advantages or disadvantages to each species in the new ecological situation. Thus, we hypothesized that interspecific intrinsic differences in thermal exchange rates may affect the efficiency of thermoregulation in the new situation, which might finally affect to the result of indirect competitive interactions between the introduced and the native freshwater turtles.

In this study, we compared in the laboratory the rates of heat exchange (heating and cooling rates) of the American red-eared slider (T. scripta) and the Spanish terrapin (M. leprosa), following exposure of turtles to step changes of ambient temperature in air and water. The step changes simulated thermal alterations that turtles experience under natural conditions during basking outside of water and when turtles posteriorly entered into water for foraging or other activities. Morphological differences in body and carapace size and shape between these two species of turtles might result in differences in heat exchange rates. Thus, we also compared the surface-to-volume ratios of the two species, basing on biometric measures, and their effects on thermal exchange rates.

METHODS

Study animals

During spring 2007, we captured with funnel traps Spanish terrapins (M. leprosa) in several ponds and tributary streams of the Guadiana river, located inside dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza (Badajoz Province, southwestern Spain). We selected 5 females of similar body size for carrying out experiments (carapace straight length: mean ± SD = 15.9 ± 0.4 cm, range = 15.2-16.2 cm). We also obtained 5 female red-eared sliders (T. scripta) of equivalent body size (carapace straight length: mean ± SD = 15.8 ± 0.2 cm, range = 15.6-16.1 cm) from a large seminatural outdoor pond located in Madrid Province (Central Spain) where they had been maintained by the conservationist organization ‘‘Grupo de Rehabilitación de la Fauna Autóctona y

 

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su Hábitat’’ (GREFA). These turtles had been extracted from introduced populations in Spain, with the purpose of preserving the original ecosystem balance.

The turtles were transported to ‘‘El Ventorrillo’’ Field Station (Navacerrada, Madrid Province), and individually housed in outdoor aquaria (60 x 40 x 30 cm) with water and stones that allowed them to bask. The temperature and day-length cycle of light were the same as the natural surroundings. Turtles were fed mince beef, earthworms and slugs three times a week. Turtles were habituated to captivity conditions at least two weeks before experiments took place. At the end of the tests, all turtles had maintained their body mass, and were returned to the GREFA ponds (sliders) or to their exact field capture sites (Spanish terrapins). Surface-to-volume ratio To estimate the surface-to-volume ratio of both species of turtles, we used biometric measures of a large set of individuals from the same areas (carapace straight length, M. leprosa: mean ± SE = 14.9 ± 0.2 cm, n = 60; T. scripta: mean ± SE = 15.0 ± 0.3 cm, n = 46). We considered that the hemispherical shape of the carapace of these freshwater turtles resembles a scalene semiellipsoid of revolution where the three semiaxes (a, b, c) are distinct. We approached the shape of turtles to a semiellipsoid whose axes 2a, 2b, 2c were given by CL (carapace straight length), CW (carapace straight width, measured at the 6-7 marginal scutes joint) and 2CH (maximum carapace height), respectively.

Unlike the area of a sphere, the surface area of a general ellipsoid cannot be expressed exactly by an elementary function. The surface area of a scalene ellipsoid is given by:

( ) ( )⎭⎬⎫

⎩⎨⎧

−+−+= mF

cabcmEcabcSA ,,2

22

2222 εοεοπ

where

( )ca /arccos=εο ; ( )22

22

sin εοbcbm −

=; 0>>> cba

m is the modular angle, or angular eccentricity and ( )mE ,εο , ( )mF ,εο are the Legendre elliptic integrals of the first and second kind (Legendre 1811).

An expression that approximates the true surface area of an arbitrary ellipsoid is given by Klamkin (1971):

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( ){ } 2/1222222 3/4 cbcabaSA ++≈ π

To asses the surface area of turtles, we adapted Klamkin’s equation for a semiellipsoid:

( ){ } bacbcabaSA ππ +++≈ 2/1222222 3/2

We validated this adapted equation, both in M. leprosa and T. scripta, by

covering turtle carapaces with rectangles (1 cm width) and computing their summatory area (observed vs. predicted R 2 = 0.946).

To assess volume of the turtles’ body, we first calculated values of volume displacement by submerging turtles in water. Then we used these values to obtain an interpolated equation which approaches the volume of the turtles from their shell dimensions (CL, CW, and CH) (non-linear estimation, observed vs. predicted R 2 = 0.999; coefficient values: i = 0.381299, j = 53.3286, k = -2.360010, l = -0.169371):

( )( )( )lCHkCWjCLiV +++≈ 2/2/2/π

We also estimated sphericity and flatness indexes for both species of turtles, using Krumbein’s Sphericity Index (SI) (Krumbein 1941) and Cailleux’s Flatness Index (FI) (Cailleux 1947):

31

2 ⎟⎟⎠

⎞⎜⎜⎝

⎛=

pqrSI

rqpFI

2+

=

where p, q and r were given by CL, CW and CH respectively. Higher values of sphericity index and lower values of flatness index mean a lower surface-to-volume ratio. Higher values of sphericity index and lower values of flatness index mean a lower surface-to-volume ratio. Heating and cooling rates Experiments took place under indoor laboratory conditions. Ambient air temperature in the room was kept at 20 ± 1 °C. To monitor the body temperature (Tb) of turtles during the whole tests, we used HOBO U-12 data loggers with HOBOware Pro Software for Windows (Onset Computer Corporation). A cloacal probe (38 ga copper-constantan thermocouple; temperature range: -200 to 100 °C; precision: ± 1.5 °C; resolution: 0.1 °C) was

 

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inserted into each turtle’s cloaca to approximately a third of the total length of the plastron (Mrosovsky 1980). To prepare the thermally sensitive probe, we entwined the leads at one end of the thermocouple, fused the entwined leads together at the tips, and encapsulated the end in epoxy resin. We used duct tape to secure the exiting thermocouple wire to the turtle’s carapace (Do Amaral et al. 2002). Previous studies have shown that cloacal temperatures of turtles were highly correlated with air and water temperatures immediately surrounding turtles (Obbard and Brooks 1981; Ernst 1982; Wilson 1994). Therefore, we assumed that cloacal temperature was a reasonably accurate estimate of turtles Tb.

To achieve initial body temperatures of turtles, we used a thermostatic chamber that was maintained at 15 ± 1 °C. For the heating experiments, each turtle was initially cooled to a Tb of 15 °C inside the cooling chamber, and then rapidly placed in an aquarium equal to the ones used to house them. The aquarium was filled with 10 L water at 15 °C, and a brick (24 x 11.5 x 7 cm) was placed in the center, emerging 3 cm above the water surface. The turtle was fixed lying on the plastron over the brick’s surface using duct tape. An infrared heat reflector (250 W, 250 V) was situated hanging 52 cm over the brick in the center of the aquarium. In this way, we simulated a basking place located in a body of water reflecting natural temperature conditions. We kept the turtle in this heating experiment until its Tb stabilized. For cooling experiments in air, we quickly removed the turtle from the aquarium and place it into the cooling chamber until its Tb decreased at 15 °C again. For cooling experiments in water, we followed the same procedure for heating until the turtle Tb stabilized, but then we removed the brick and placed the turtle inside the water of the aquarium (15 ± 1 °C) and monitored Tb until it stabilized at water temperature. Analytical model of thermal exchange rates When an ectotherms animal basks, its Tb gradually increases, as time spent basking increases. Therefore, to fit the increment in Tb described by turtles during the heating experiments (i.e., heating rates), we used a Bertalanffy equation (Von Bertalanffy 1960; Kaufman 1981):

⎥⎦

⎤⎢⎣

⎡−+=

)cosh(1 1 b st

vuT

where u was the initial Tb (°C) and v the total increment over the initial Tb at the equilibrium time (°C). s is the slope of the function, defined as the heating rate, and t is the time (min).

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For the cooling experiments, we used a similar Bertalanffy equation describing gradually decreasing Tb:

⎥⎦

⎤⎢⎣

⎡−=

)cosh(1 b st

vwT

where w and v were respectively the Tb at the equilibrium time and the total negative increment over the initial Tb (°C). s is the cooling rate and t is the time (min). Statistical analyses To analyze differences in morphological parameters between both species of turtles, we used general lineal models (GLM) with surface-to-volume ratio, or sphericity or flatness index as dependent variable, species and sex as categorical predictors and body size as continuous predictor. For turtles tested in the thermal exchange experiment, we used Mann-Whitney’s U-tests to analyze differences between species in body size, weight, surface-to-volume ratio, sphericity and flatness indexes, and heating and cooling rates (Sokal and Rohlf 1995). Pairwise comparisons were made using Tukey’s honestly significant difference tests. RESULTS

Surface-to-volume ratio Surface-to-volume ratio was significantly and negatively correlated with body size of turtles (r = -0.67, F = 152.36, df = 1,101, P < 0.001). We found significant differences between the two species of turtles in surface-to-volume ratio after controlling by body size differences (GLM, F = 99.10, df = 1,101, P  <  0.001), with higher values of surface-to-volume ratio for M. leprosa than for T. scripta. Males of both species of turtles showed significantly higher values of surface-to-volume ratio than females (F = 13.81, df = 1,101, P < 0.001), and this difference was greater for M. leprosa than for T. scripta (interaction: F = 4.87, df = 1,101, P = 0.03).

There were no significant correlations between body size and sphericity index (r = -0.14, F = 2.05, df = 1,104, P = 0.16) or flatness index (r = -0.05, F = 0.26, df = 1,104, P = 0.61), so we did not include body size in further analyses. The two turtle species differed significantly in both sphericity (GLM, F = 9.89, df = 1,102, P < 0.001) and flatness indexes (F = 9.84, df = 1,102, P = 0.002) with

 

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higher values of flatness and lower values of sphericity for M. leprosa than for T. scripta. Males showed also higher flatness and lower sphericity indexes than females (F = 14.02, df = 1,102, P < 0.001 and F = 20.08, df = 1,102, P < 0.001, respectively). The interaction between sex and species was non-significant for flatness index (F = 0.43, df = 1,102, P = 0.52) but it was significant for sphericity index (F = 8.80, df = 1,102, P = 0.004). Thus, there were significant differences in sphericity between male and female M. leprosa (higher values for females, Tukey’s test, P < 0.001), but not between male and female T. scripta (P = 0.72).

Heating and cooling rates Mann-Whitney’s U-tests analyzing turtles tested in the thermal exchange experiment showed significant differences between species in body weight, surface-to-volume ratio, and sphericity and flatness indexes, being T. scripta heavier and more spherical and with lower values of surface-to-volume ratio and flatness than M. leprosa (Table 4.1). Size differences were non-significant, as we intended in the selection of the experimental individual turtles based on similar body sizes. Also, there were significant differences between M. leprosa and T. scripta in heating and cooling rates (Table 4.1; Fig. 4.1). T. scripta showed a lower heating rate and also lower cooling rates, both in air and water, than M. leprosa. Values of heating and cooling rates for each individual turtle are provided in Table 4.2. All thermal exchange rates were positively correlated with the surface-to-volume ratio (Spearman’s rank-order correlations, heating rate: rs = 0.79, n = 10, P = 0.006; cooling rate in air: rs = 0.82, n = 10, P = 0.004; cooling rate in water: rs = 0.66, n = 10, P = 0.038). DISCUSSION Our results revealed differences between native M. leprosa and introduced T. scripta turtles in heating and cooling rates. T. scripta showed lower heating rates but also lower cooling rates, both in air and water, thus taking more time than M. leprosa in heating and cooling processes. Although we cannot discard that unknown physiological mechanisms are also playing a role in interspecific differences in thermal exchange rates, our results show that these differences are closely related to differences between turtle species in characteristic shape and morphology. Shape has been established as a critical factor in the ability of organisms to thermoregulate (Bogert 1949; Gould 1966). We found that M. leprosa turtles were flatter than T. scripta, which showed a more spherical shell shape. Thus, M. leprosa have smaller body sizes and higher surface-to-volume ratios for the same body lengths than T. scripta. Since rates of thermal exchange depend upon absolute body size (Grigg et al. 1979; Seebacher et al. 1999), and

b)

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15

20

25

30

0 60 120 180 240Time (min)

Tem

p (ºC

)

M. leprosaT. scripta

Water

0 15 30 45 60Time (min)

M. leprosa T. scripta

Air

15

20

25

30

0 60 120 180 240Time (min)

Tem

p (º

C)

Table 4.1 Results from Mann-Whitney U test examining the effect of the turtle specie on size, weight, surface-to-volume ratio, sphericity and flatness indexes, and heating and cooling rates in tested turtles (mean ± SD; n1= n2 = 5 in all cases)

M. leprosa T. scripta Z P

Size (cm) 15.9 ± 0.4 15.8 ± 0.2 0.94 0.35 Weight (g) 527.49 ± 46.47 685.59 ± 30.11 -2.61 0.009 Surface-to-volume ratio (cm-1) 0.6 ± 0.04 0.52 ± 0.03 2.61 0.009 Sphericity Index 0.64 ± 0.02 0.69 ± 0.02 -2.61 0.009 Flatness Index 2.35 ± 0.1 2.2 ± 0.1 2.19 0.028 Heating rate (°C/min) 0.039 ± 0.003 0.029 ± 0.002 2.61 0.009 Cooling rate (Air) (°C/min) 0.058 ± 0.014 0.031 ± 0.005 2.61 0.009 Cooling rate (Water) (°C/min) 0.194 ± 0.032 0.143 ± 0.019 2.40 0.016

Figure 4.1 Body temperature responses of M. leprosa (——) and T. scripta (-----) to a step change in ambient temperature during (a) heating and (b) cooling experiments

a)

b)

 

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Table 4.2 Morphological measures: size, weight, surface-to-volume ratio (SA/V), sphericity index (SI) and flatness index (FI) for tested turtles, with thermal exchange rates (s) and corresponding R2 values for the three different treatments

thus the surface-to-volume ratio is determinant for bodies of similar length, differences in shell morphology between the two species of turtles may entail a faster thermal exchange with air and water in M. leprosa than in T. scripta. In this regard, shell shape and surface-to-volume ratio have been demonstrated to similarly influence heating and cooling rates among freshwater turtles (Boyer 1965; Spray and May 1972; Gronke et al. 2006). We also found that males of both species had flatter shells and higher values of surface-to-volume ratio, likely as a result of the concavity of the male plastron (which reduces shell height and volume). These differences between males and females were greater

Species Turtle Size (cm)

Weight (g)

SA/V (cm-1)

SI FI Treatment s (min-1)

R 2

M. leprosa 1 1 1

16.1 552.20 0.580 0.65 2.33 Heating Cooling (Air) Cooling (Water)

0.03940.04510.1876

0.965 0.986 0.961

2 2 2

16.1 586.29 0.545 0.67 2.25 Heating Cooling (Air) Cooling (Water)

0.03520.04510.1472

0.943 0.986 0.956

3 3 3

15.2 505.13 0.598 0.66 2.25 Heating Cooling (Air) Cooling (Water)

0.03930.05450.2138

0.974 0.989 0.967

4 4 4

15.9 530.08 0.623 0.63 2.44 Heating Cooling (Air) Cooling (Water)

0.03620.06550.2311

0.971 0.990 0.942

5 5 5

16.2 463.76 0.634 0.62 2.48 Heating Cooling (Air) Cooling (Water)

0.04300.07710.1899

0.977 0.984 0.971

T. scripta 1 1 1

15.7 709.79 0.518 0.69 2.19 Heating Cooling (Air) Cooling (Water)

0.02760.03000.1445

0.986 0.991 0.968

2 2 2

15.8 682.94 0.539 0.68 2.13 Heating Cooling (Air) Cooling (Water)

0.02740.03630.1349

0.978 0.992 0.977

3 3 3

16.0 680.29 0.528 0.68 2.24 Heating Cooling (Air) Cooling (Water)

0.02870.02720.1359

0.981 0.989 0.953

4 4 4

15.6 715.38 0.466 0.72 2.08 Heating Cooling (Air) Cooling (Water)

0.03280.03560.1749

0.976 0.993 0.970

5 5 5

16.1 639.56 0.540 0.67 2.33 Heating Cooling (Air) Cooling (Water)

0.03020.02570.1241

0.982 0.991 0.984

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in M. leprosa than in T. scripta, in agreement with the deeper plastral concavity found in M. leprosa (N. Polo-Cavia, pers. obs.). Although sexual dimorphism has been observed to influence rates of thermal exchange in reptiles (Pearson et al. 2003) and it may likely have influence on thermal behavior of both species of turtles, our results cannot yield the effect of sex on their heating and cooling rates, nor predict its magnitude, as we used only female individuals in our experiment. As expected, body size was negatively correlated with surface-to-volume ratio, but no correlation was found between size and sphericity or flatness indexes. Therefore, when turtles reach greater sizes, their volume increases more than their surface area, while no significant variation in shape occurs.

Both cladogenesis and environment may be considered as significant sources of shape variation in turtles (Claude et al. 2003). While clades mostly differ in shell contour (emydids being posteriorly wider), and in more localized differences (as in the relative extension of scutes or bones), environment acts mostly on shell height and on the architecture of costal plates; aquatic species having a more flattened shell, terrestrial ones a more rounded shape. The flat aquatic shell has been thought to enhance hydrodynamics. For example, an explanation for the flattened shell shape of M. leprosa, compared to the European pond terrapin, Emys orbicularis, might be the hydrodynamic morphofunction it could confer in more open waters (Arnold and Ovenden 2002). However, a flattened shell may also entail disadvantages for turtles. An example is that flat shell turtles are easily caught by avian predators (Janzen et al. 2000). Nevertheless, M. leprosa may compensate the cost of a flattened shell by fleeing quickly to safe water when facing a terrestrial predator (Polo-Cavia et al. 2008). In contrast, a more rounded shell might favor T. scripta in an original habitat where greatest danger comes from aquatic predators (i.e., caimans and crocodiles, Greene 1988) and they are pressured to remain for longer in land, withdrawn inside the shell, exposed to avian and other terrestrial predators (Polo-Cavia et al. 2008). On the other hand, submerged and floating vegetation is usually heavy in T. scripta original habitat (Morreale and Gibbons 1986; Gibbons 1990). Thus, a specific hydrodynamic functional shell should be less expected in this species.

Even if the further evolutionary causes determining species-specific shell shape are unknown, and although we do not know whether other factors such as thickness of carapace bone or differences in color pattern between the two species might also influence heating and cooling rates, it is clear from our results that interspecific differences in shape per se influences surface-to-volume ratio, and thus, rates of thermal exchange with the environment. These interspecific differences may have consequences for the outcome of competition processes between turtle species in a scenario where T. scripta has been

 

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introduced in the original habitat of native M. leprosa. The trade-off fitted between thermal exchange rates of M. leprosa and other ecological requirements such as shape functionality or antipredatory strategies might be threatened when a new competitor interferes in their thermoregulatory behavior, taking advantage of its original adaptations. The rounded shape of T. scripta confers them a low surface-to-volume ratio and a greater thermal inertia, compared with M. leprosa, what might result advantageous in the Mediterranean habitats into which T. scripta is introduced.

The advantages of a high thermal inertia appear intuitively reasonable in larger reptiles (Spotila et al. 1973; Slip and Shine 1988; Spotila et al. 1991). For example, leatherbacks turtles (Dermochelys coriacea) are able to maintain elevated body temperatures in cold water and avoid overheating in the tropics (Paladino et al. 1990), which probably allowed them to exploit an ecological niche unavailable to other marine turtle species (Wallace et al. 2005). On a different scale, but in a similar way, slight differences in thermal inertia between species of small ectotherms might favor introduced species in their new habitats. In the Iberian Peninsula, sliders have been observed to be active at lower water temperatures, and therefore, to start earlier than native turtles their annual cycle (Aceituno 2001). Such adaptation is consistent with the higher thermal inertia of T. scripta observed in our study. In temperate zones, mechanisms for conserving body heat could have selective advantages in aquatic turtles, since individuals that have been basking on land and have achieved high body temperatures may suddenly be exposed to very cool conditions when entering the water (Bartholomew 1982). However, a greater thermal inertia helps to stabilize body temperature, so that rapid changes of temperature in the environment are slowly reflected in changes in body temperature. In this way, the lower cooling rates of introduced T. scripta facilitate body heat retention, thus developing a better performance of activities such as aquatic foraging (Huey and Slatkin 1976; Dunham et al. 1989), and favoring competition with native turtles. Also, the risk of overheating while T. scripta remain withdrawn into the shell for a long period of time, trying to deter a predator (Polo-Cavia et al. 2008), decreases when surface-to-volume ratio is greater and thus, the thermal buffering is more effective.

Although a greater thermal inertia also entails an increment in time necessary to attain optimal temperature, T. scripta may compensate for this cost by being more competitive for basking resources (Cadi and Joly 2003), or by increasing the duration of initial basking before locomotor activity in Mediterranean latitudes (see Spotila et al. 1984, showing that the timing of basking changes with latitude in T. scripta). Also, observations of basking turtles in field and captivity show that introduced turtles commonly bask with all limbs outstretched (contrarily to Spanish terrapins, whose limbs are relaxed in

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the basking position, N. Polo-Cavia, per. obs.), thus considerably increasing their surface-to-volume ratio and optimizing basking (Crawford et al. 1983). Similar behavioral control over the rate of heat transfer by means of changing postures has been observed in large snakes (Ayers and Shine 1997; Rice et al. 2006) and lizards (Martín et al. 1995).

A greater thermal inertia might allow T. scripta to maintain relatively high and constant body temperatures after basking in air, mostly through behavioral thermoregulation in water (aquatic basking and selection of heated areas of water have been demonstrated in T. scripta, Spotila et al. 1984), while native M. leprosa turtles would require a more intermittent basking activity due to their higher rate of thermal exchange with environment. Also, M. leprosa interruptions of basking may result in a more efficient occupation of basking sites by T. scripta. Cadi and Joly (2003) suggested that introduced T. scripta seemed more competitive for the most suitable basking places than native European pond turtles E. orbicularis, which avoided to climb onto a solarium that was already occupied by a slider. Similar competition for basking places between T. scripta and M. leprosa has been confirmed experimentally (Polo-Cavia et al. in press).

With the introduction of a new competitor species interfering in the efficiency of performance of basking, the lower thermal buffering of native M. leprosa turtles may entail a difficulty for heat retention and result in the achievement of suboptimal body temperatures, which may lead to a detriment in the efficiency of their physiological functions. Low body temperatures negatively affect food ingestion and digestion (Gianopulos and Rowe 1999), which ultimately affects growth rates (Congdon 1989; Avery et al. 1993). The rate and efficiency of digestion are enhanced at elevated body temperatures (Parmenter 1981; Zimmerman and Tracy 1989), being food energy incorporated more rapidly and efficiently. This has especial importance to individuals inhabiting Mediterranean regions, in which high temperatures are limited year around (Lysenko and Gillis 1980). A deficiency in basking activity has also consequences in dermal synthesis of vitamin D (Pritchard and Greenhood 1968; Avery 1982), avoidance of fungal infections and riddance of parasites of shell and skin (Cagle 1950; Boyer 1965; Vogt 1979), and may also retard maturation of ova (Obbard and Brooks 1979; Whittow and Balazs 1982).

In conclusion, the more rounded shell of introduced T. scripta endows them with a greater surface-to-volume ratio, compared with native M. leprosa. The Spanish turtle present a more flattened shape; likely due to the hydrodynamic morphofunction it might confer in the more open waters where this species occurs (Arnold and Ovenden 2002). These differences in shape morphology between species are related with differences in thermal exchange rates. Since mechanism for maximizing body heat retention could confer selective

 

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advantages to aquatic turtles, which are exposed to chilling conditions when entering water (Bartholomew 1982), the greater thermal inertia of T. scripta might result in a competitive advantage for this introduced species in Mediterranean habitats. Interactions between T. scripta and native M. leprosa during basking activity could lead to a detriment in the efficiency of basking and thermoregulation of native turtles, with lower capabilities of heat retention. It might finally affect digestion rates and other physiological functions, thus aggravating the outcomes of competition with introduced sliders. Acknowledgements We thank A. Marzal for allowing us to work in his dehesa state (‘‘La Asesera’’), the ‘‘Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat’’ (GREFA) for providing exotic turtles, and ‘‘El Ventorrillo’’ MNCN Field Station for use of their facilities. Helpful suggestions for the analytical model of thermal exchange rates were provided by V. Polo. Financial support was provided by the MEC project CGL2005-00391/BOS and by a MEC-FPU grant to N.P.-C. The experiments comply with the current laws of Spain and the Environmental Agencies of the ‘‘Junta de Extremadura’’ and ‘‘Comunidad de Madrid’’ where they were performed. REFERENCES Aceituno J (2001) La población del galápago de Florida (Trachemys scripta elegans) en la

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Capítulo 5

 

 

 

  

Relación entre el estado nutricional y los requerimientos de asoleamiento de 

galápagos nativos e invasores 

Nuria Polo Cavia, Pilar López y José Martín

 

En revisión

 

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RESUMEN

El comportamiento termorregulador de los ectotermos se encuentra fuertemente ligado a su estado nutricional. Recientemente, se ha sugerido que la existencia de un compromiso entre el mantenimiento del balance energético y la eficiencia de la digestión podría afectar al comportamiento de termorregulación en estos animales. Por otra parte, se ha confirmado la competencia por lugares de asoleamiento entre las especies nativas de galápagos y el introducido galápago de Florida (Trachemys scripta elegans). T. scripta interfiere negativamente en la actividad de asoleamiento de los galápagos nativos y posee, además, una mayor capacidad para retener el calor corporal, lo que en conjunto podría conferir ventajas termorreguladoras a la especie invasora. En consecuencia, a partir de un comportamiento de asoleamiento deficiente podrían derivarse efectos complejos y diversas alteraciones en las tasas metabólicas de los galápagos nativos. En este trabajo, comparamos los requerimientos de asoleamiento de una especie autóctona de la Península Ibérica protegida, el galápago leproso (Mauremys leprosa), con los del introducido galápago de Florida, en condiciones de alimentación ad libitum vs. ayuno. Para ello, se analizó el límite superior del rango de temperaturas seleccionado por cada especie (LSR) (definido como la temperatura corporal a la cual cesa la actividad de asoleamiento). La especie nativa mostró valores más altos de LSR, y ambas especies redujeron esta temperatura en respuesta a la privación de alimento. Esta plasticidad del comportamiento termorregulador de los galápagos en relación a su estado nutricional sugiere la existencia de un mecanismo adaptativo en ectotermos que favorece la depresión metabólica y la conservación de la energía durante periodos de ayuno. Sin embargo, una reducción en las tasas metabólicas de M. leprosa inducida por la competencia con una especie invasora podría derivar en una prolongada deficiencia de las funciones fisiológicas de los individuos, incurriendo por tanto en elevados riesgos de salud y depredación, lo cual podría finalmente favorecer la recesión de la especie nativa en ambientes mediterráneos ■

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FEEDING STATUS AND BASKING REQUIREMENTS OF FRESHWATER

TURTLES IN AN INVASION CONTEXT

Abstract Thermoregulatory behavior and feeding status are strongly related in ectotherms. A trade-off between maintenance of energy balance and digestion efficiency has been recently proposed to affect thermoregulation in these animals. On the other hand, competition for basking sites has been described between Iberian turtles and the introduced red-eared slider (Trachemys scripta elegans). T. scripta negatively interferes on basking behavior of native turtles and benefits from a greater capacity to retain body heat, which may likely result in thermoregulatory advantages for the introduced sliders. Consequently, complex effects and alterations in metabolic rates of native turtles might derive from a deficient basking behavior. We compared the basking requirements of the endangered native Spanish terrapin (Mauremys leprosa) and those of the introduced red-eared slider, analyzing the upper set point temperature (USP) (defined as the body temperature at which basking ceases) of both native and introduced turtles, under feeding and fasting conditions. We found higher values of USP in the native species, and a reduction of this temperature associated with food deprivation in the two turtle species. This adjustment of thermoregulatory behavior to the nutritional status found in freshwater turtles suggests that ectotherms benefit from metabolic depression as an adaptive mechanism to preserve energy during periods of fasting. However, a reduction in metabolic rates induced by competition with sliders might lead M. leprosa to a prolonged deficiency of their physiological functions, thus incurring increased predation risk and health costs, and ultimately favoring the recession of this native species in Mediterranean habitats. Keywords Feeding status • Freshwater turtles • Invasive species • Mauremys leprosa • Thermoregulation • Trachemys scripta

ike in most ecthotherms, thermoregulation is especially important in aquatic turtles, since it affects many of their physiological functions (Huey 1982). Mainly through aerial basking, aquatic turtles can attain

and maintain fairly precise and constant body temperatures (Tb) that allow them to optimize the efficiency of their physiological processes (Boyer 1965; Crawford et al. 1983; Scharzkoplf and Brooks 1985; Meek and Avery 1988). In particular, Tb plays a major role in maximizing digestive processes in reptiles (Harlow et al. 1976; Troyer 1987). By attaining optimal Tb, turtles that adequately bask benefit from a corresponding increase in their metabolic rate (Jackson 1971; Kepenis and McManus 1974; Dubois et al. 2008), digestion speed and digestion efficiency (Kepenis and McManus 1974; Parmenter 1981; Avery et al. 1993; Koper and Brooks 2000; Angilletta 2001; Zhang and Ji 2004).

Many ectotherms change their temperature preferences after feeding. A thermophilic response resulting in increased Tb has been observed in a wide range of reptiles, including crocodilians (Lang 1979), snakes (Lysenko and Gillis 1980; Dorcas et al. 1997; Blouin-Demers and Weatherhead 2001a), lizards (Sievert 1989; Tosini et al. 1994; Brown and Griffin 2005; Brown and Roberts 2008), and turtles (Moll and Legler 1971; Gatten 1974; Hammond et al. 1988;

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Dubois et al. 2008). Most of these experimental studies have analyzed the thermoregulatory behavior of ectotherms after a food ingestion event, while less emphasis has been placed on their feeding status. Diet composition has been reported to influence Tb selected by some reptiles (Geiser et al. 1992; Geiser and Learmonth 1994, Simandle et al. 2001) but little evidence exists to support similar effects induced by prolonged fasting conditions. Recently, Brown and Griffin (2005) described a reduction in the selected Tb of the lizard Anolis carolinensis after food deprivation, suggesting an energy conservation strategy during periods of low food availability. A similar effect is found in some terrapin species (Gatten 1974; Dubois et al. 2008), which suggests that turtles are able to accurately adjust their metabolic rates according to the food intake opportunities, and also that their basking requirements increase in order to attain optimal Tb that allow them to maintain a more active metabolism and an optimal performance of their digestive functions. Many ectothermic vertebrates exhibit a physiological flexibility that allows them to adjust their energy expenditure processes during periods of nutritional bottlenecks (Anderson 1993; Naya and Bozinovic 2006; Naya et al. 2008). Thus, metabolic rates of turtles have been found to decrease as fasting conditions prolong (Belkin 1965; Sievert et al. 1988). Sievert et al. (1988) report drops of 1/3 in oxygen consumption of juvenile turtles Chrysemys picta after only 19 days of fasting. The reduction in metabolic rates of reptiles has been claimed to act to conserve energy resources (Bennett and Dawson 1976).

In the Iberian Peninsula, the red-eared slider (Trachemys scripta) is an introduced exotic turtle (Vilà et al. 2008) that is competing and displacing the native Spanish terrapin (Mauremys leprosa), whose populations have considerably declined during the last decades, being currently considered as an endangered species (Da Silva 2002). The nature of the interspecific interactions between sliders and Spanish terrapins remains unclear, but it is possible that direct competition for food, refuges or basking places occurs (Crucitti et al. 1990). Competition for basking sites has been described between sliders and the European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and recent studies suggest that competition is very likely to occur also between sliders and the Spanish terrapins (Polo-Cavia et al. 2008, 2009a,b). Also, native M. leprosa forced to share basking resources with sliders have been found to reduce their basking activity and to avoid basking stacked with the exotic turtles (Polo-Cavia et al. in press). Sliders can then monopolize the most suitable basking places, impeding native turtles to adequately bask, which might severely affect the efficiency of physiological, especially digestive, functions of the native species. Such negative effects of inefficient basking may explain the loss of weight and decreased survival rates found in native terrapins after long term competition with sliders (Cadi and Joly 2004). However, anatomical and physiological

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differences between native and invasive turtle species might confer them dissimilar thermal requirements in relation with digestive processes. Interspecific differences in thermal exchange rates related to morphological differences in carapace size and shape have been found between these two turtle species (i.e., M. leprosa shows a lower thermal inertia associated with a greater surface-to-volume ratio compared with those of T. scripta, Polo-Cavia et al. 2009b). Different body surface-to-volume ratios entail different heat exchange rates, which might further induce different basking requirements. This might also imply that the feeding status of the turtles may affect differently to the thermoregulatory behavior of sliders and native terrapins. Moreover, an individual that is able to maintain its selected Tb for a longer time period should assimilate more metabolic energy during digestion (Angilletta et al. 2001). Thus, due to their higher thermal inertia, sliders would take more time to attain an optimal Tb but they could maintain body heat for longer when entering the water, favoring the maintenance of elevated metabolic rates and the proper performance of digestive processes. On the other hand, Spanish terrapins would attain faster an optimal Tb during basking, but because of their greater tendency to loss heat when entering water, they might require more frequent basking episodes in order to increase Tb during feeding periods. Then, in a new competitive situation in which introduced sliders actively displace native terrapins from the basking places and impede them to adequately bask, Spanish turtles might not be able to maintain optimal Tb for appropriate food assimilation. This could lead to a reduction of their metabolic activity, and thus to a detriment in the efficiency of food ingestion and digestion, which might finally affect negatively the outcome of competition between introduced and native freshwater turtles.

The purpose of this study was to compare the thermal requirements during basking of native Spanish terrapins M. leprosa and introduced sliders T. scripta, analyzing the effects of prolonged feeding and fasting conditions on preferred basking temperatures. We considered the upper set point temperature (USP), measured as the Tb at which turtles ceased basking and entered into the water, as a good indicator of thermal requirements related with feeding in aquatic turtles (Dubois et al. 2008; see methods). Thus, our objectives were to determine 1) whether differences in USP occurred between native and invasive turtle species, and 2) the effect of food deprivation on the USP of the two turtle species. Finally, since turtles’ morphology might indirectly affect the thermophilic response through its influence on thermal exchange rates, we also analyzed 3) the relation between surface-to-volume ratio and USP of turtles.

 

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METHODS

Study animals

We captured with baited funnel traps 18 individuals of native Spanish terrapins (M. leprosa) (carapace length: mean ± SE = 14.7 ± 0.3 cm, range = 11.5-16.3 cm) in several ponds and tributary streams of the Guadiana River, located inside dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza (Badajoz Province, southwestern Spain). We also obtained 16 red-eared sliders (T. scripta) (carapace length: mean ± SE = 14.8 ± 0.6 cm, range = 11.3-17.9 cm), from a large pond located in Madrid Province (central Spain), where they had been maintained under seminatural conditions by the conservationist private organization “EXOTARIUM” (Exotic Animal Rescue Center). These sliders had been recently extracted from introduced populations in central Spain to avoid aversive effects on the original ecosystem balance.

All turtles were housed individually at “El Ventorrillo” Field Station (Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) filled with water and containing stones that allowed them to bask. The temperature and photoperiod were those of the natural surroundings. Turtles were held in their home-aquaria for at least two weeks before testing, so that they became familiarized with captivity conditions. To avoid potential confounding effects of the diet on the results, turtles were fed ad libitum small pieces of commercial compound feed. All turtles were healthy during the trials and all maintained or increased their body mass. At the end of experiments, turtles were returned to the EXOTARIUM’s pond (sliders) or to their exact field capture sites (Spanish terrapins).

Surface-to-volume ratio

We estimated the surface-to-volume ratio of turtles, basing on biometric measures. We approached the hemispherical shape of the turtles carapace to a scalene semiellipsoid of revolution whose axes 2a, 2b, 2c were given by CL (carapace straight length), CW (carapace straight width, measured at the 6-7 marginal scutes joint) and 2CH (maximum carapace height) respectively.

To assess the surface area of turtles, we adapted Klamkin’s equation (this expression approximates the true surface area of an arbitrary ellipsoid, Klamkin 1971), for a semiellipsoid:

( ){ } bacbcabaSA ππ +++≈ 2/1222222 3/2

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To asses volume of the turtles body, we used an interpolated equation which approaches the volume of the turtles from their shell dimensions (CL, CW and CH) (coefficient values: i = 0.381299, j = 53.3286, k = -2.360010, l = -0.169371):

( )( )( )lCHkCWjCLiV +++≈ 2/2/2/π

This method has been validated and used before in assessing the surface-to-

volume ratio of both M. leprosa and T. scripta species (see Polo-Cavia et al. 2009b for a detailed description).

Set point temperatures

According to the thermal coadaptation hypothesis, since performance is enhanced when Tb approaches a species and specific-process optimal temperature (To), the preferred –or set point- body temperature (Tset) of a species should match this thermal optimum for performance (Huey and Bennett 1987; Angilletta et al. 2006). Consequently, Tset is commonly used to estimate the Tb that maximizes locomotion or physiological performance (Dawson 1975; Stevenson et al. 1985; Hertz et al. 1993; Brown and Weatherhead 2000; Blouin-Demers and Weatherhead 2001b). In estimations of Tb that maximizes digestive functions, in which energy gain typically increases continuously to To and then sharply decreases (Lillywhite et al. 1973; Stevenson et al. 1985; Niu et al. 1999), Tset is more properly defined as the upper set point temperature (USP) selected by an animal in a thermal gradient (Dubois et al. 2008), rather than as the mean (Pough and Gans 1982) or a central quartile range (Hertz et al. 1993). Upper and lower bounds of Tset have to be defined arbitrarily in thermal gradients, but they can be directly determined as the Tb at which an individual shows heat avoidance behavior and shifts to cooling and viceversa (Kingsbury 1993, 1999; Tosini and Avery 1994; Ben-Ezra et al. 2008). Thus, Tb at which aerial basking ceases can be considered an appropriate measure of USP associated with maximizing digestive processes in aquatic turtles.

Experimental procedure

We compared USP of native M. leprosa and introduced T. scripta under feeding and fasting conditions. Each subject turtle was tested in two experimental treatments (‘feeding vs. fasting’), with the order of application differing between individuals (random assignment). For the ‘feeding’ treatment, turtles were fed ad libitum commercial compound feed once a day during seven

 

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consecutive days before testing. All turtles readily ate this type of food, and we considered that turtles were able to eat enough food until satiation. For the ‘fasting’ treatment, turtles were deprived of food for seven consecutive days prior to testing. After this time, turtles were considered to be postabsorptive (i.e., to have digested and absorbed all food in their digestive tract) (Bennet and Dawson 1976; Gatten 1974). Water was continuously available during the period of fasting. At the end of trials, animals were fed ad libitum and recovered their normal nutritional state seven days after trials had finished.

We carried out experiments indoor to maintain experimental conditions stable (ambient air temperature in the laboratory was kept at 20 ± 1 °C). We used an aquarium equal to the ones used to house the turtles. The aquarium was filled with 10 L water at ambient temperature, and a brick (24 x 11.5 x 7 cm) was placed in the center, emerging 3 cm above the water surface. An infrared heat reflector (250 W, 250 V) was situated hanging 30 cm over the brick in the center of the aquarium. In this way, we simulated a basking place located in a body of water reflecting natural temperature conditions. A similar experimental device that allowed turtles to shuttle between aerial basking and cold water has been used before to measure set point temperatures of aquatic turtles (Ben-Ezra et al. 2008). Each turtle was initially cooled inside a thermostatic chamber that was maintained at 15 ± 1 °C until Tb stabilized at 15 °C, and then carefully placed on the plastron over the brick’s surface and left undisturbed for one hour. From that moment, the turtle was free to dip into the water, although the lower Tb encouraged the turtle to bask. Turtles were used to handling and they normally bask as they did in their home aquaria.

We monitored Tb of turtles during the whole tests, using HOBO U-12 data loggers with HOBOware Pro Software for Windows (Onset Computer Corporation). A cloacal probe (38 ga copper-constantan thermocouple; temperature range: -200 to 100 °C; precision: ±1.5 °C; resolution: 0.1 °C) was inserted into each turtle’s cloaca to approximately a third of the total length of the plastron (Mrosovsky 1980). Gauge thermocouples into the anal opening of reptiles are generally well tolerated and spare from disturbing the subject and/or the experiment. Therefore, it is considered an appropriate method for measuring Tb in these animals (Kingsbury 1999). To prepare the thermally sensitive probe, we entwined the leads at one end of the thermocouple, fused the entwined leads together at the tips, and encapsulated the end in epoxy resin. We used duct tape to secure the exiting thermocouple wire to the turtle’s carapace (Do Amaral et al. 2002). Previous studies have shown that cloacal temperatures of turtles were highly correlated with air and water temperatures immediately surrounding turtles (Obbard and Brooks 1981; Ernst 1982; Wilson 1994) and with internal Tb (Edwards and Blouin-Demers 2007; Ben-Ezra et al. 2008; Dubois et al. 2008). Therefore, we assumed that cloacal temperature was a

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reasonably accurate estimate of turtles Tb. Data loggers recorded the changes in the Tb of each turtle during basking, and its USP right before the turtle dived into the water, and consequently, the Tb started to decrease to water temperature (20 °C).

Statistical analyses

We used a two-way repeated measures analyses of variance (ANOVA) to analyze the differences between M. leprosa and T. scripta in USP across treatments by the same individual subject turtle. The experimental treatment (‘feeding’ vs. ‘fasting’) was included as a within subject factor, and the species of the subject turtle as a between-subjects factor. We used simple linear regression to analyze the effect of surface-to-volume ratio on the USP of turtles, under feeding and fasting conditions. Data normality was verified by Shapiro-Wilk’s test and tests of homogeneity of variances (Levene’s test) showed that variances were not significantly heterogeneous.

RESULTS

We found significant differences in overall USP between M. leprosa and T. scripta (two-way repeated measures ANOVA, species: F = 33.05, df = 1,32, P < 0.0001). Native Spanish terrapins showed higher values of USP than invasive sliders (M. leprosa: mean ± SE = 31.9 ± 0.6 °C; T. scripta: mean ± SE = 26.7 ± 0.7 °C). We also found significant differences between treatments (F = 28.16, df = 1,32, P < 0.0001), with greater values of USP when the turtles had been fed than in the fasting treatment (Fig. 5.1). The interaction between species and treatment was non-significant (F = 0.003, df = 1,32, P = 0.95) (Fig. 5.1).

 Figure 5.1 Set point body temperatures (USPs) (mean ± SE) at which basking ceased of introduced T. scripta and native M. leprosa, under feeding and fasting treatments

 

Feeding Fasting22

24

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28

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32

34

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USP

(ºC

)

T. scripta M. leprosa

 

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USP of turtles were positively correlated with their surface-to-volume ratio under feeding and fasting treatments (Pearson’s correlations, feeding: r = 0.69, F = 28.53, df = 1,32, P < 0.0001; fasting: r = 0.60, F = 17.93, df = 1,32, P < 0.0002). Thus, turtles with lower surface-to-volume ratio showed lower USP (Fig. 5.2).

Figure 5.2 Pearson’s correlations between USP and surface-to-volume ratio of turtles, when they were under feeding (solid line) and fasting (dotted line) conditions

DISCUSSION

Our results firstly reveal clear interspecific differences in the Tb at which basking ceased (i.e., USP) between introduced T.scripta and native M. leprosa freshwater turtles, with overall USP being on average 5.2 °C higher in M. leprosa. This result clearly suggests different thermal requirements of sliders and Spanish terrapins. Behavioral thermoregulation through aerial basking allows ectotherms to maximize physiological performance by regulating Tb to approach a species and specific-process optimal temperature (Huey and Slatkin 1976; Huey and Bennett 1987; Angilletta et al. 2002, 2006). Thus, differences in thermal optima for performance between the two species might likely explain their differences in USP.

On the other hand, the correlation found between set point temperatures of turtles and their surface-to-volume ratio points out to a close relation between interspecific differences in basking requirements and interspecific differences in

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carapace morphology. Interspecific differences in thermal exchange rates with the environment related to different surface-to-volume ratios have been reported for M. leprosa and T. scripta (Polo-Cavia et al. 2009b). The more rounded shape of T. scripta confers them a low surface-to-volume ratio and a greater thermal inertia, compared with M. leprosa, which facilitates body heat retention. Since freshwater turtles usually lose the heat gained from basking very rapidly when they re-entry to water (Avery 1982; Bartholomew 1982), strategies that contribute to maximize heat retention could be selectively advantageous for aquatic species, especially in Mediterranean habitats in which high temperatures are limited year around (Lysenko and Gillis 1980). We suggest that Spanish terrapins, more flattened and with higher surface-to-volume ratios, might compensate their greater heat loss by increasing the USP. In this way, Spanish terrapins could benefit from a better performance when entering into water for foraging or other activities. At this regard, a positive effect of increased Tb on aquatic and terrestrial locomotor performance of juvenile western painted turtles (Chrysemys picta bellii) has been reported recently (Elnitsky and Claussen 2006). Also, Ben-Ezra et al. (2008) found that the optimal temperature for swimming and righting of the northern map turtle (Graptemys geographica) fell within Tset, very close to the upper bound. However, because of the wide range of Tset that turtles exhibited, these authors suggested that coadaptation may not reflect selective pressures for the convergence of preferred basking temperature and locomotor performance in this species. Moreover, Ben-Ezra et al. (2008) argued that, in turtles with pronounced aerial basking behavior, the locomotory potential of elevated Tb achieved by basking would rapidly be lost in aquatic environments because of the high thermal conductivity of water. Nevertheless, turtles might be able to maintain relatively high and constant Tb after basking in air by later selecting heated areas of water (aquatic thermoregulatory behavior has been demonstrated in T. scripta, Spotila et al. 1984). Thus, behavioral thermoregulation may be also linked with locomotory performance in aquatic turtles, as it is in other reptiles (Bauwens et al. 1995; Angilletta et al. 2002; Blouin-Demers et al. 2003). Although, behavioral regulation of Tb is considered to primarily serve to maximize energy gain, rather than locomotory performance, and it seems to be of particular importance for turtles inhabiting environments where high temperatures are limited (Dubois et al. 2008).

Since heat transference from air occurs faster in M. leprosa than in T. scripta (Polo-Cavia et al. 2009b), a higher USP would not imply that Spanish terrapins need to have longer basking periods than sliders. Thus, the higher USP of M. leprosa would not necessarily entail a disadvantage in terms of time budget by itself. However, negative effects may arise from basking interactions with the introduced competitor, if native turtles find difficulties to compensate

 

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their faster body heat loss in water with more frequent episodes of aerial basking to regain temperature (see Cady and Joly 2003; Polo-Cavia et al. in press, describing negative impact of sliders introduction on basking behavior of native turtles).

The results of our experiments also reveal a clear variation in USP of turtles associated with feeding status. Both M. leprosa and T. scripta showed USP 2.4 °C higher on average when they had been fed than under fasting conditions. Previous studies on turtles have reported similar effects on thermoregulatory behavior related to feeding (Moll and Legler 1971; Hammond et al. 1988; Dubois et al. 2008), with selected Tb even 4.5 °C higher in recently fed T. scripta (Gatten 1974). Snakes (Lysenko and Gillis 1980; Blouin-Demers and Weatherhead 2001a), crocodilians (Lang 1979), and lizards (Sievert 1989; Tosini et al. 1994; Brown and Griffin 2005; Brown and Roberts 2008) also establish higher Tb after feeding, and a big snake, Boa constrictor, places the portion of its body containing a bolus of food directly below the heat source (Regal 1966). Such thermoregulatory behavior of reptiles in response to feeding conditions is assumed as an adaptive adjustment to the optimal temperatures for some components of the digestive process (Dorcas et al. 1997), which may require different thermal optima from those selected for other behaviors and functions (Huey 1982; Stevenson et al. 1985; Van Damme et al. 1991; Du et al. 2000). The thermophilic response of freshwater turtles found in our experiments is consistent with previous results for correlations between basking and feeding in red-eared sliders (Gatten 1974), and suggests that both M. leprosa and T. scripta require from an extra body heat contribution to successfully complete digestive processes. Thermophilic response elicited by feeding varies widely among reptile species (Sievert 1989), and variability has also found between freshwater and terrestrial turtles (Gatten 1974). Thus, differences in extra heat contribution required by introduced and native turtles could be expected in our experiment. However, the magnitude of the effect of feeding status on the USP of turtles was similar for introduced and native terrapins, indicating that basking requirements of both M. leprosa and T. scripta similarly increment with increased food intake. Since aquatic turtles experiment very contrasting temperatures when they shift between aerial basking and water immersion to maintain Tset, thermoregulation seems to be much more challenging for freshwater turtles than for terrestrial ones (Ben-Ezra et al. 2008). Then, similar basking habits of M. leprosa and T. scripta, and their association with freshwater aquatic habitats, in comparison with terrestrial turtles, may explain the similarities in precision of thermoregulation between the two species.

Increased metabolisable energy intakes could be one of the advantages of higher Tb selected by ectotherms during digestion (Angilletta 2001), but energy expenditure increases at elevated Tb, what suggests a trade-off between

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maintenance of energy balance and digestive efficiency. Consequently, a reduction of the Tb could help to improve energy balance during periods of low food availability by means of energy conservation (Lillywhite et al. 1973; Brown and Griffin 2005). Similarly, many ectotherms maintain lower Tb during inactivity (e.g., Hutchison and Spriesterbach 1986; Sievert and Hutchison 1988, 1989; Angilletta and Werner 1998), possibly as an energy saving mechanism (Huey 1982; Hutchison and Spriesterbach 1986). Therefore, the shift in the USP of fasted vs. fed turtles that we found might be due to an adaptive mechanism to moderate the impact of low levels of energy intake during periods of fasting on other parameters of the energy budget. Under prolonged fasting conditions, turtles might save energy reducing activity and metabolic rates (Belkin 1965; Sievert et al. 1988), which would involve accurately adjustment of their thermoregulatory behavior to their feeding status, by reducing basking and selecting lower Tb. Even if there is no supporting evidence that energy saving by decreased Tb could have a substantial impact in wild ectotherms, the shift in the set point temperatures of freshwater turtles observed here contributes to support the generality of the finding of decreased selected Tb associated with periods of food deprivation in ectotherms (Brown and Griffin 2005). Our results further suggest that ectotherms benefit from adjusting their Tb and metabolic rates according to the food intake opportunities.

Thus, feeding status and selected Tb of ectotherms seem to influence each other in a complex bidirectional way. Increased consumption related to increased Tb has been reported for many reptile species (e.g., Dutton et al. 1975; Waldschmidt et al. 1986; Van Damme et al. 1991; Angilletta 2001). Constraints on locomotion and increased gut passage time seem to be responsible for limited consumption at low temperatures (Angilletta 2001). Even if turtles do not use rapid locomotion to capture food (Harding and Bloomer 1979; Ernst 2001), consumption might be constrained by food processing rate, especially at northern latitudes, where temperature may be more limiting than food availability (Congdon 1989; Grant and Porter 1992; Koper and Brooks 2000). Also, many of the processes determining food intake (i.e., prey detection and capture, handling time, ingestion) are sensitive to Tb (Greenwald 1974; Van Damme et al. 1991; Ayers and Shine 1997). Since Tb clearly influences the performance of activities associated with feeding (Bennett 1990), it is very likely that turtles with low basking opportunities show also a less active foraging, besides a reduced metabolism, decreased digestion rates, and a general depression of their physiological functions (Parmenter 1981; Sievert et al. 1988; Zimmerman and Tracy 1989; Gianopulos and Rowe 1999). With the introduction of a new competitor species interfering in their basking behavior, native Spanish terrapins likely find difficulties to properly bask, thus being unable to reach and maintain optimal Tb, with might negatively affect their

 

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food ingestion. Turtles might then experiment a reduction in their selected Tb in order to compensate their energy balance, which might finally induce a feedback effect between basking requirements and feeding performance, thus resulting in a more and more depressed metabolism. Negative effects derived from a dropped metabolism might be poor food energy incorporation (Parmenter 1981; Zimmerman and Tracy 1989), lowered blood circulation and suppressed immune defenses (Cooper et al. 1985), retarded growth rates (Congdon 1989; Avery et al. 1993) or maturation arrest of ova (Obbard and Brooks 1979; Whittow and Balazs 1982). In such lethargic conditions, native turtles might easily incur increased predation risk and health costs, thus aggravating the competition process with introduced turtles and favoring the recession of native Spanish terrapins.

In short, our experiments revealed differences in USP of M. leprosa and T. scripta, which might have different specific thermal optima for performance. However, differences in morphology and associated thermal exchange rates may be also responsible for the different basking requirements of M. leprosa and T. scripta. A similar thermophilic response was elicited by feeding in both turtles species, which showed higher USP during basking. The reduced basking requirements related to fasting conditions that we found in freshwater turtles confirm that ectotherms might benefit from metabolic depression as an adaptive mechanism to preserve energy during periods of low food intake. Nevertheless, a reduction in the metabolic rates of native turtles induced by competition with a new introduced species interfering in their thermoregulatory behavior might lead to serious consequences for Spanish terrapins. Acknowledgements We thank A. Marzal for allowing us to do field work in his dehesa state (“La Asesera”), the Exotic Animal Rescue Center “EXOTARIUM” for providing sliders, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and the MCI project CGL2008-02119/BOS, and by an ‘‘El Ventorrillo’’ CSIC grant and a MEC-FPU grant to N. P.-C. REFERENCES Anderson JF (1993) Respiratory energetics of two Florida harvestmen. Comp Biochem Physiol A

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Efectos de la temperatura corporal en la respuesta de ‘giro’ de galápagos nativos e invasores: consecuencias 

en la competencia  

Nuria Polo Cavia, Pilar López y José Martín

En revisión

 

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RESUMEN

La coadaptación entre la temperatura preferida de asoleamiento y la respuesta locomotora de los galápagos es una cuestión arduamente controvertida, argumentándose que las temperaturas alcanzadas durante el asoleamiento aéreo difícilmente podrían favorecer la locomoción de los galápagos en el agua. Sin embargo, el comportamiento de ‘giro’ de estos animales podría estar sujeto a presiones de coadaptación, puesto que tiene lugar fundamentalmente en tierra y puede determinar críticamente su supervivencia. En este estudio se analizó el efecto de la temperatura corporal (Tb) en la respuesta de ‘giro’ de dos especies de galápagos, el autóctono galápago leproso (Mauremys leprosa) y el introducido galápago de Florida (Trachemys scripta elegans), una especie invasora que está desplazando a las poblaciones nativas en la Península Ibérica. Es posible que la respuesta de ‘giro’ de estas dos especies pudiera verse afectada diferencialmente por la Tb. Así mismo, las diferencias interespecíficas potenciales en el comportamiento de ‘giro’ de los galápagos podrían contribuir a explicar la mayor capacidad competitiva de T. scripta. Los resultados mostraron un claro efecto de la Tb en la repuesta de ‘giro’ tanto de M. leprosa como de T. scripta, la cual fue favorecida a las temperaturas preferidas de asoleamiento respectivas de cada especie, sugiriendo la existencia de coadaptación entre esta temperatura y la respuesta de ‘giro’ de los galápagos. Por otra parte, M. leprosa requirió tiempos medios más largos que T. scripta para volver a la posición prono, lo que indica una mayor eficiencia de la especie invasora en la respuesta de ‘giro’. Esta ventaja competitiva podría favorecer la expansión de los galápagos exóticos en los nuevos ambientes en los que han sido introducidos, en detrimento de las poblaciones nativas de galápago leproso ■

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EFFECTS OF BODY TEMPERATURE ON RIGHTING PERFORMANCE OF NATIVE AND INVASIVE FRESHWATER TURTLES:

CONSEQUENCES FOR COMPETITION

Abstract Coadaptation between preferred basking temperature and locomotion of aquatic turtles remains controversial because aerial basking could hardly improve locomotor performances in water. However, righting behavior might be subject to coadaptation pressures, given that it is mainly performed on land and may critically determine survival of turtles. We analyzed the effect of body temperature (Tb) on righting performance of two species of freshwater turtles, the endangered native Spanish terrapin (Mauremys leprosa), and the red-eared slider (Trachemys scripta elegans), an introduced invasive species that is displacing native turtles in the Iberian Peninsula. We hypothesized that Tb might differently affect righting response of these two turtle species, and that interspecific behavioral asymmetries in righting performance might contribute to explain the greater competitive ability of introduced T. scripta. We found a clear effect of Tb on righting response of both M. leprosa and T. scripta, being the performance enhanced at the preferred basking temperature of each turtle species. These results suggest that righting might be coadapted to preferred basking temperature in freshwater turtles. Also, M. leprosa required longer times to right on average than T. scripta, what denotes a higher efficiency of introduced T. scripta at righting performance. This might favor the expansion of exotic sliders in the new environments in which they are introduced, in detriment of native Spanish terrapins. Keywords Freshwater turtles • Invasive species • Mauremys leprosa • Preferred basking temperature • Righting performance • Trachemys scripta

ccording to the thermal coadaptation hypothesis, the preferred temperature (Tset) of a species should match the thermal optimum (To) of thermally sensitive processes that influence fitness (Huey and

Bennett 1987; Angilletta et al. 2006). In ectotherms such as reptiles, temperature is the major limiting factor affecting locomotor performances, which are determining in critical activities such as foraging, mating, or predator avoidance (Huey 1982; Irschick and Garland 2001). Thus, coadaptation between Tset and To for locomotion is present in many reptile species, including lizards (Bauwens et al. 1995; Angilletta et al. 2002) and snakes (Stevenson et al. 1985; Blouin-Demers et al. 2003). However, it has been claimed recently that Tset and To might not be coadapted for locomotor performances in turtles with pronounced aerial basking behavior, since individuals usually lose the heat gained from basking very rapidly when entering the water (Ben-Ezra et al. 2008).

A locomotor activity of special interest in turtles is the ability of righting. Turtles may result overturned in natural environments while climbing or competing for solaria, during male fights, or as consequence of predatory attacks (Corti and Zuffi 2003; Stancher et al. 2006). In these cases, the capacity of turtles to right is critical to survival, as turtles in an upside-down position are

A

 

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particularly exposed to predators, changes in body temperature (Tb) and dehydration, and may experience difficulties to breathe (Burger 1976; Finkler 1999; Steyermark and Spotila 2001; Martín et al. 2005). Righting performance has been shown to be uncorrelated with swimming and other locomotor performances in turtles (Elnitsky and Claussen 2006), what suggests that righting might be subject to different coadaptation pressures. Because most critical righting behavior occurs mainly on land, where turtles can maintain substantially higher Tbs, it might be possible that selective pressures favor the convergence between preferred basking temperature and To for righting performance in aquatic turtles. By regulating Tb to approach To, turtles may benefit from a positive effect on their lifetime fitness. Thus, a strong thermal dependence of righting has been observed in a variety of turtle species (Steyermark and Spotila 2001; Freedberg et al. 2004; Elnitsky and Claussen 2006). More recently, Ben-Ezra et al. (2008) found that Tset encompasses To for righting in the northern map turtle (Graptemys geographica), an active aerial basker. However, enough evidence for coadaptation between Tset and To for righting in aquatic turtles is not yet provided, and the relationship between behavioral thermoregulation and locomotor performances in turtles with striking aerial basking remains unclear.

In this study, we analyzed the effect of body temperature on righting behavior of two species of freshwater turtles which actively bask on air: the Spanish terrapin (Mauremys leprosa) and the red-eared slider (Trachemys scripta elegans). The Spanish terrapin is widespread in the south and central Iberian Peninsula and northwestern Africa (Keller and Busack 2001). However, this species has suffered a considerable recession during the last decades, being currently considered as an endangered species (Pleguezuelos et al. 2002). Besides habitat destruction and human pressure, the remainder populations endure competition with exotic introduced turtles, mainly American sliders (Da Silva and Blasco 1995; Pleguezuelos 2002; Vilà et al. 2008). Although the nature of the interspecific interactions between native and introduced turtles is not completely clear, recent studies have pointed out to diverse competitive advantages of sliders over Spanish terrapins, such as a more accurate assessment of predatory risk in altered habitats, displacement of native turtles mediated by chemical cues avoidance, or a greater thermal inertia that favors heat retention (Polo-Cavia et al. 2008, 2009a,b). Both M. leprosa and T. scripta turtles are predominantly aquatic, but they actively bask on land to attain and maintain Tb within the intervals necessary for their daily activities (Meek 1983; Gibbons 1990). During basking bouts, turtles are extremely alert and vigilant, as they are potential prey of birds and mammals (Martín and López 1990; López et al. 2005). In such vulnerable situations, overturning accidentally may have serious or even lethal consequences for turtles, if they are not efficient at self-righting.

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Righting response of turtles consists of two different stages, the lag time (time elapsed to response) and the mechanical righting time. The first time represents the behavioral decision of turtles of when to right, while the second one depends mainly on physical traits and physiological state of turtles (Steyermark and Spotila 2001; Elnitsky and Claussen 2006). During the lag phase, turtles must accurately assess the costs of remaining overturned vs. those of returning to prone position, and properly determine the optimal time to initiate righting, basing on this trade-off. Similarly, turtles adjust the time spent inside refuges or withdrawn within the shell so that the optimal time to emerge is the time when the costs of staying equal the costs of leaving (Sih 1992, 1997; Martín et al. 2005; Cooper and Frederick 2007; Polo-Cavia et al. 2008). Specifically, overturned turtles may suffer increased predation exposure, overheating or difficulties to breath, but righting response requires from a particular energy effort related with variables such as health and nutritional state or temperature, which may also vary over time. In this way, the decision of when to start righting (i.e., the duration of the lag phase) may be determined by expectancy of turtles on righting success, which depends on individual intrinsic variables and external factors that affect their physiological response, On the other hand, once a turtle decide to right, the righting response basically relies on its temperature-dependent locomotor performance and physical traits. Morphological comparisons indicate that factors such as neck-length to carapace-height ratio, tail length or shell height and width influence the tactic and efficiency of turtles at mechanical righting (Rivera et al. 2004; Domokos and Várkonyi 2008). Thus, righting performance should be determined by accuracy of turtles during the lag time in assessing risk and own capabilities to return to prone position, and by their specific morphology and physical skills during the mechanical phase. However, righting might be also influenced by environmental factors affecting physiological performance, especially temperature.

Interspecific differences in behavioral responses to predation risk have been found between Spanish terrapins and introduced sliders (Polo-Cavia et al. 2008), as well as anatomical differences in carapace size and shape, what suggests that these two turtle species might also differ in efficiency of righting response. Also, preferred basking temperature and optimal righting performance might be differently related in Spanish terrapins and sliders. We hypothesized that righting responses of M. leprosa and T. scripta might be determined by species specific risk-sensitive decisions and/or morphological traits. But also, we hypothesized that there might be interspecific differences in the effects of Tb of turtles on righting performance, which might differentially affect mechanical aptitudes of turtles to perform righting, and thus, risk assessment during the lag phase. We compared behavioral and mechanical

 

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aspects of righting response of native M. leprosa and introduced T. scripta turtles, examining their relation with Tb of turtles. Our objectives were to determine 1) whether interspecific differences in righting response exist, 2) whether Tb affects differentially the righting performance of native and invasive turtles, and 3) whether possible behavioral asymmetries in righting response between the two turtle species might contribute to the greater competitive ability of introduced T. scripta. Finally, 4) to explain whether possible differences between M. leprosa and T. scripta were due to dissimilarities in morphology that might affect mechanical righting, we compared their carapace height-to-width ratios, sphericity and flatness indexes, and tail-length-to-size ratios, and analyzed within species the effects of sphericity and flatness indexes and tail-length-to-size ratio on mechanical righting times of turtles.

METHODS

Study animals

During May 2007, we captured with baited funnel traps 14 individuals of native Spanish terrapins (M. leprosa) (carapace length: mean ± SE = 14.9 ± 0.3 cm, range = 12.5-16.3 cm) in several ponds and creeks of the Guadiana River at Olivenza (Badajoz Province, southwestern Spain). These freshwater habitats, located inside dehesa woodlands with scattered holm oak (Quercus ilex) held an important population of Spanish turtles. We also obtained 13 introduced red-eared sliders (T. scripta) (carapace length: mean ± SE = 14.3 ± 0.6 cm, range = 11.3-17.4 cm), from a large pond located in Madrid Province (central Spain), where they had been maintained under seminatural conditions by the conservationist private organization “EXOTARIUM” (Exotic Animal Rescue Center). These sliders had been recently extracted from introduced populations in central Spain to preserve the original ecosystem balance. None of the turtles presented shell imperfections that might hinder righting success.

Turtles were individually housed at “El Ventorrillo” Field Station (Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) that were filled with water and provided with stones that allowed turtles to bask. Turtles were maintained under natural temperatures and photoperiods and fed small pieces of commercial compound feed three times per week. We held turtles in their home-aquaria for at least two weeks before testing, so that they became familiarized with captivity conditions. During this time, we minimized contact with animals to avoid habituation to the experimenter that could affect risk assessment during trials. At the end of experiments, all turtles had maintained or increased their body mass, and were returned to the EXOTARIUM’s pond (sliders) or to their exact field capture sites (Spanish terrapins).

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Morphological traits

We compared morphological traits of M. leprosa and T. scripta basing on biometric measures of turtles. Four parameters: CL (carapace straight length), CW (carapace straight width at the 6-7 marginal scutes joint), CH (maximum carapace height), and TL (tail length) were measured with a digital caliper (Mitutoyo) to the nearest mm. Thus, we estimated carapace height-to-width ratio as CH / CW and tail-length-to-size ratio as TL / CL. Carapace height-to-width ratio approximates shell geometry and has been used to classify turtle species into equilibrium classes determining the strategy and efficiency of righting (Domokos and Várkonyi 2008). On the other hand, higher values of tail-length-to-size ratio might favor mechanical righting (Rivera et al. 2004).

We also estimated sphericity and flatness indexes of both species of turtles, using Krumbein’s Sphericity Index (SI) (Krumbein 1941) and Cailleux’s Flatness Index (FI) (Cailleux 1947):

31

2 ⎟⎟⎠

⎞⎜⎜⎝

⎛=

pqrSI

rqpFI

2+

=

where p, q and r were given by CL, CW and CH, respectively (see Polo-Cavia et al. 2009b). Higher values of sphericity index and lower values of flatness index mean a more rounded shell, which entails lower energy barriers between stable and unstable equilibria (Domokos and Várkonyi 2008).

Experimental procedure

We carried out experiments in outdoor enclosures with a substrate of uniform low grass. Trials were performed on sunny days, at an ambient temperature of approximately 25 °C. We tested each subject turtle at three different temperatures (15 °C, 20 °C and its species-specific Tset). Tsets were estimated as the upper set point temperature (USP) selected by turtles in a basking device (see below). The Tb at which turtles cease basking and shift to water represents properly the upper bound of Tset and can be precisely determined. For this reason, it can be considered an appropriate measure of Tset associated with maximizing processes in which performance increases continuously to To and then sharply decreases (Kingsbury 1993, 1999; Tosini and Avery 1994; Ben-Ezra et al. 2008; Dubois et al. 2008). Thus, we considered USP of basking as an appropriate measure of Tset that should maximize righting performance in turtles under the coadaptation hypothesis.

 

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We determined the USPs of M. leprosa and T. scripta as the average USPs of all experimental individuals of each respective species. To allow turtles to bask until they attained USP, we used an infrared heat reflector (250 W, 250 V). An aquarium equal to the ones used to house the turtles was placed indoor (ambient air temperature in the laboratory was kept at 20 ± 1 °C) and filled with 10 L water at ambient temperature. A brick (24 x 11.5 x 7 cm) was placed in the center of the aquarium, emerging 3 cm above the water surface and the heat reflector was situated hanging 30 cm over the brick. In this way, we simulated a basking place located in a body of water reflecting average temperature conditions in the natural environment of turtles. Turtles were initially cooled inside a thermostatic chamber, in order to encourage them to bask. We monitored Tb of each turtle inside the chamber and during the whole time of basking using HOBO U-12 data loggers with HOBOware Pro Software for Windows (Onset Computer Corporation). A cloacal probe (38 ga copper-constantan thermocouple; temperature range: -200 to 100 °C; precision: ± 1.5 °C; resolution: 0.1 °C) was inserted into each turtle’s cloaca (see Polo-Cavia et al. 2009b for a detailed description). Previous studies have shown that cloacal temperatures of turtles were highly correlated with air and water temperatures immediately surrounding turtles (Obbard and Brooks 1981; Ernst 1982; Wilson 1994), and with internal Tb (Edwards and Blouin-Demers 2007; Ben-Ezra et al. 2008; Dubois et al. 2008). Therefore, we assumed that cloacal temperature was a reasonably accurate estimate of turtles Tb. When Tb stabilized at 15 °C, we took the turtle out of the chamber and carefully placed it on the plastron over the brick’s surface. Thereafter, we left the turtle undisturbed for one hour in the aquarium. Turtles were used to handling and they normally basked as they did in their home aquaria. USP values were recorded by data loggers right before the turtles dipped into the water, and consequently, the Tb started to decrease to water temperature (20 °C). Results showed that M. leprosa selected significantly higher average USP values (mean ± SE = 30.6 ± 1.0 °C) than T. scripta (27.5 ± 0.7 °C) after removing the effect of size (General Linear Model, F = 9.36, df = 1,24, P = 0.005).

For righting trials, we carried M. leprosa and T. scripta turtles to three different testing temperatures, placing each turtle inside the thermostatic chamber, until Tb stabilized at 15 °C, 20 °C, or its species-specific USP. Then, we took the turtle out of the chamber, rapidly removed the cloacal probe and placed the turtle upside down in the outdoor enclosure with short grass substrate to start the test. From the moment that turtles were released upside down on the grass, they typically spent some time entirely withdrawn in the shell, after which they put the head partially out and scanned the surroundings. Then, turtles put the head, neck and legs entirely out from the shell, and started to right. From a hidden position, we used a stopwatch to record, to the nearest

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second: (1) the time at the first contact of the head or a limb with the substrate since the turtle was turned over on its back on the grass (‘latency time’), and (2) the time for a turtle to right itself since it initiates righting (‘time to right’). These two different measures have been used before to analyze the two different components of the righting response of turtles (Steyermark and Spotila 2001; Elnitsky and Claussen 2006; Delmas et al. 2007). While the first time represents the lag time, the second time informs about mechanical skills and physiological state of turtles to right. Turtles were given 900 s to start righting and 900 s in addition to return to prone position.

Tests with different temperatures were performed in a random order and each turtle participated in only one trial per day to minimize the influence of stress resulting from one test on the results of subsequent tests. To avoid confounding effects that may affect risk assessment, all turtles were handled by the same person, who performed all the experiments in a standardized way. Times of turtles inside the thermostatic chamber were similar between individuals and species, so we discarded possible effects of different stress levels induced by handling on response times of turtles.

Statistical analyses

We used two-way repeated measures analyses of variance (ANOVAs) to test for differences in latency time and time to right of the same individual turtle at the three different testing temperatures. Temperature was included as a within-subject factor and the turtle species as a between-subject factor. We also included the interaction in the models to analyze whether the effects of temperature changed between species. Previous analyses showed that sex did not influence latency time or time to right and, thus, sex was excluded in final analyses. Righting response times were not normally distributed, so we transformed all data using Box-Cox transformation (Sokal and Rohlf 1995). We verified normality by Shapiro-Wilk’s test and tested for homogeneity of variances (Levene’s test). Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995).

We compared carapace height-to-width ratio, sphericity and flatness indexes, and tail-to-length ratio of M. leprosa and T. scripta turtles using one-way ANOVAs. To analyze the effects of sphericity and flatness indexes and tail-to-length ratio on time to right of the two turtle species, we used simple linear regressions.

 

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RESULTS Latency time There were no significant differences between M. leprosa and T. scripta in overall latency time that they remained waiting before the initiation of righting (two way-repeated measures ANOVA, species: F = 0.66, df = 1,25, P = 0.42). However, we found a significant effect of Tb on latency time of turtles (F = 18.73, df = 2,50, P < 0.0001), and the interaction between species and turtles’ Tb was significant (F = 7.70, df = 2,50, P = 0.001). Thus, while latency times were independent of Tb in T. scripta (Tukey’s tests, P ≥ 0.68 in all cases), in M. leprosa latency times were significantly greater at 15 °C than at 20 °C (P = 0.0002), and than at USP of turtles (P = 0.0001) (Fig. 6.1a). However, differences between latency time of M. leprosa at 20 °C and at USP of turtles were non-significant (P = 0.89). The two turtle species did not significantly differ in latency time at any of the testing temperatures (P ≥ 0.63 in all cases). Time to right We found significant differences between the two species of turtles in overall time required to return to prone position since they started to right (two way-repeated measures ANOVA, species: F = 11.60, df = 1,25, P = 0.002), with lower time to right in T. scripta (mean ± SE = 78 ± 34 s) than in M. leprosa (151 ± 33 s). Time to right was significantly influenced by Tb of turtles (F = 23.64, df = 2,50, P < 0.0001). Thus, time to right was greater at 15 °C than at 20 °C (Tukey’s test, P = 0.001) or at USP of turtles (P = 0.0001), and greater at 20 °C than at USP (P = 0.007) (Fig. 6.1b). The interaction between species and Tb of turtles was non-significant (F = 0.67, df = 2,50, P = 0.52). Therefore, Tb similarly affected the time to right of both M. leprosa and T. scripta. Effects of morphological traits There were no significant differences between M. leprosa and T. scripta in carapace height-to-width ratio (one-way ANOVA, F = 0.05, df = 1,25, P = 0.82) (M. leprosa: mean ± SE = 0.51 ± 0.01; T. scripta: 0.51 ± 0.01). Differences between the two turtle species in sphericity and flatness indexes were significant (one-way ANOVAs, F = 87.63, df = 1,25, P < 0.0001 and F = 11.85, df = 1,25, P = 0.002 respectively), being M. leprosa more flattened (sphericity index: mean ± SE = 0.64 ± 0.004; flatness index: 2.37 ± 0.04) and T. scripta more rounded (sphericity index: 0.70 ± 0.01; flatness index: 2.19 ± 0.04). However, interindividual variation in time to right within each species were not

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a) Figure 6.1 Mean (± SE) of (a) latency time and (b) time to right of T. scripta and M. leprosa, representing behavioral and mechanical components of the righting response at three different body temperatures: 15 °C, 20 °C, and the species-specific preferred basking temperature (USP) of turtles

significantly correlated with any of the two indexes (Pearson’s correlations, sphericity index, M. leprosa: r ≤ -0.40, F ≤ 2.24, df = 1,12, P ≥ 0.16 in all cases, T. scripta: r ≤ -0.40, F ≤ 2.08, df = 1,11, P ≥ 0.18 in all cases; flatness index, M. leprosa: r ≤ 0.38, F ≤ 2.06, df = 1,12, P ≥ 0.18 in all cases, T. scripta: r ≤ 0.42, F ≤ 2.41, df = 1,11, P ≥ 0.15 in all cases).

We also found significant differences between species in tail-length-to-size ratio (one-way ANOVA, F = 10.46, df = 1,24, P = 0.004), with greater values for M. leprosa (mean ± SE = 0.46 ± 0.02) than for T. scripta (0.35 ± 0.02). However, the effect of tail-to-length ratio on times to right of M. leprosa and T. scripta within each species was not significant at any of the testing temperatures (Pearson’s correlations, M. leprosa: r ≤ 0.28, F ≤ 0.92, df = 1,12, P ≥ 0.36 in all cases; T. scripta: r ≤ 0.17, F ≤ 0.34, df = 1,11, P ≥ 0.57 in all cases).

b)

 

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DISCUSSION Our results revealed clear differences between M. leprosa and T. scripta in behavioral and mechanical components of the righting response. Although lengths of latency time that native and introduced turtles remained waiting before the initiation of righting did not significantly differ, the lag phase was independent of Tb in T. scripta, but not in M. leprosa, suggesting that risk assessment during overturning is more influenced by Tb in M. leprosa than in T. scripta. Also, although mechanical phase of the two turtle species similarly speeded up with increasing temperatures, M. leprosa required longer times on average to right than T. scripta, regardless of temperature, which suggests a higher efficiency of mechanical righting in introduced sliders.

Righting performance entails important costs for turtles, such as revealing the own presence to possible predators, and in particular, the great energy expenditure to overcome gravity. However, overturned turtles are especially exposed to suffer increased predation risk, overheating or rather serious difficulties at breathing that may lead turtles to critical conditions (Rivera et al. 2004; Stancher et al. 2006). Because both righting performance and overturning entail costs, turtles must accurately decide when to right, in order to maximize righting response. Thus, turtles should optimize the decision of when to initiate righting, by balancing righting energy inputs with costs of remaining overturned, in a similar way that prey respond to predators by accurately assessing risk level to decide when to change between alternative antipredatory tactics that entail different costs (Lima and Dill 1990; Sih 1997). Supporting this, Martín et al. (2005) observed experimentally that, after a simulated predatory attack, overturned M. leprosa adjusted their righting decisions basing on persistence of predators and proximity to water. In consequence, lag phase of righting is determined by environmental factors such as level of predatory threat, overheating and/or dehydration risks. But also, latency time is influenced by expectancy of turtles on their own mechanical righting response, which depends on intrinsic variables (i.e., morphology and physical skills), and physiological performance of turtles that may vary over time with health and nutritional state, or more unpredictably, with Tb of turtles.

Overall latency times of M. leprosa and T. scripta were similar, what might initially suggest that confidence of native and introduced turtles in their own capacities to perform righting was similar (as environmental variables affecting risk assessment were constant in our experiment). However, times to right of M. leprosa were almost two times longer on average than those of T. scripta, what indicates that sliders are more efficient at mechanical righting than Spanish terrapins. Therefore, one would expect that T. scripta turtles showed lower latency times in comparison with those of M. leprosa terrapins, according

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with an accurate perception of turtles of their own capabilities to perform righting. Similarities in lengths of lag phase between the two turtle species might then be explained by asymmetries in risk assessment between Spanish terrapins and sliders that might compensate the higher confidence in righting success of introduced T. scripta. For example, predation threat while overturning might differ between M. leprosa and T. scripta, which have evolved within dissimilar predatory-systems in their original assemblages (i.e., predation threat is mainly posed by terrestrial mammals and birds in the Iberian Peninsula, while a great variety of aquatic predators are present in the original habitats of sliders). In agreement with the hypothesis of divergences in risk assessment between the two turtle species, we observed in a previous study that, after a simulated predatory attack on land, T. scripta exceeded M. leprosa in length of time that turtles spent withdrawn into the shell before emerging and escaping, likely waiting for the predator to abandon the surroundings and thus, avoiding potential encounters with more dangerous aquatic predators (Polo-Cavia et al. 2008). On the other hand, overheating risk perceived while overturned by sliders might be lower than that perceived by native terrapins, as introduced T. scripta presents greater thermal inertia, and therefore, heat gain is slowed down in this species (Polo-Cavia et al. 2009b). This might also explain that sliders waited for longer than we expected before starting to right. Finally, we cannot discard that other interspecific differences, such as a more protecting shell of T. scripta, or a more constrained physiology of M. leprosa in an upside-down position, might also explain the lack of significant differences in latency times of native and invasive turtles, even when they greatly differed in efficiency of mechanical righting.

Testing temperature did not significantly affect latency times of T. scripta, what suggests that risk assessment during overturning in T. scripta is less dependent on turtles’ Tb. In contrast, lag phase of M. leprosa was greater at 15 °C than at 20 °C or at preferred basking temperature of the species, but lag time was not significantly greater at 20 °C than at the preferred basking temperature. It might be possible that extremely low Tbs discourage M. leprosa from turning right-side up, since in such motionless conditions, the highly increased costs of performing righting might induce turtles to remain for longer onto their carapaces. However, the elevated costs of remaining overturned, and consequently, the strong selective pressure for turtles to right might minimize differences between motivation of turtles to perform righting at 20 °C and at preferred basking temperature, despite the fact that a non-optimal Tb could lead turtles to wait for a longer time in an upside-down position before starting to right. Therefore, only when M. leprosa turtles are extremely cold, the costs of righting seem to incline turtles to remain for longer onto their carapaces. Likewise, the absence of relation between latency times and Tb of turtles in T.

 

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scripta might rely on the short times that they employed to perform righting, compared with those of M. leprosa. A high efficiency of mechanical righting might likely reduce the effect of temperature on risk assessment, explaining that none of the testing temperatures was low enough to incline sliders to assume overturning costs for longer times. Although, it is also possible that the lower preferred basking temperature of T. scripta, which implied less variability between the three testing temperatures, contributes to explain the absence of differences between latency times found in this species.

Interspecific differences in mechanical righting times between the two turtle species must rely on dissimilar specific morphologies and mechanical skills. Recently, Domokos and Várkonyi (2008) established equilibrium classes of turtles and their relation to righting behavior, basing on geometric measures of the shell. They concluded that righting strategy of turtles was basically determined by carapace height-to-width ratio, since this parameter was enough to approximate shell geometry. According with Domokos and Várkonyi’s (2008) models, both M. leprosa and T. scripta turtles from our experiment fell within ‘flat turtles’ class, which present two stable equilibria (one on the plastron and one opposite, on the carapace), and a high energy barrier between stable and unstable equilibria. Since flat turtles with high energy barriers use primarily their necks for righting (Rivera et al. 2004; Domokos and Várkonyi 2008), neck length should be considered the main factor of available biomechanical energy to right in both M. leprosa and T. scripta. However, our geometric models of turtles, based on sphericity and flatness indexes of the shell, have yielded morphological shape differences between M. leprosa and T. scripta (i.e., Spanish turtles being more flattened, sliders more rounded, Polo-Cavia et al. 2009b; this study), which might also play a role in determining the physical skills of the two turtle species to right, jointly with interspecific asymmetries in neck length. Thus, although both M. leprosa and T. scripta turtles from our experiment were considered ‘flat turtles’, Spanish terrapins are more flattened than sliders, which show a more rounded shell that likely endows them with a lower energy barrier between stable and unstable equilibria, thus requiring less time to right. However, mechanical righting times of M. leprosa and T. scripta were not significantly correlated within each species with sphericity or flatness indexes of turtles at any of the testing temperatures, likely due to the effect of individual differences in more determining variables such as neck length. Tail length has also been claimed to influence mechanical phase of righting (Rivera et al. 2004). However, although M. leprosa showed clearly greater tail-length-to-size ratios than T. scripta, M. leprosa took more time to right than T. scripta. Also, tail-length-to-size ratio was not correlated within each species with times to right of turtles. This suggests, in agreement with previous studies, that tail length is not a primary factor determining righting in flat turtles.

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Mechanical righting performance of both M. leprosa and T. scripta were similarly affected by Tb. Turtles took less time to return to prone position as Tb approached their species-specific preferred basking temperature. Because physiological performances in ectotherms typically increase with Tb up to a species and process specific To, after which it steeply decreases (Huey 1982), reptiles are expected to select Tbs that maximize locomotion. However, aquatic turtles with pronounced aerial basking have been claimed to be an exception, since the elevated Tb achieved on land could hardly improve locomotor performances during the vital activities that they normally develop in water (e.g., foraging or mating) (Ben-Ezra et al. 2008). Nevertheless, several studies have reported a sharp thermal dependence of righting, among other locomotor performances, in aquatic turtles (Steyermark and Spotila 2001; Freedberg et al. 2004; Elnitsky and Claussen 2006). In agreement with them, our results indicate that righting behavior of M. leprosa and T. scripta is enhanced at their specific preferred basking temperatures, further suggesting that selected Tbs might be related to locomotion, or at least, to righting performance, in freshwater turtles. Recently, Elnitsky and Claussen (2006) showed that righting response of juvenile western painted turtles (Chrysemys picta bellii) was uncorrelated with other terrestrial and aquatic locomotor performances. This suggests that righting might represent a different locomotor trait following different adaptive forces. Righting constitutes a risky manoeuvre in which a great effort is required to overcome the energy barrier of the unstable equilibrium at the turtle’s side. However, there is a strong selective pressure for turtles to right, as while overturned, they are specially exposed and vulnerable. For these two reasons, maximizing righting performance by regulating Tb seems to be an ability of considerable adaptive value, even for aquatic turtles.

In addition, righting performance is considered an indicator of fitness in freshwater turtles (Delmas et al. 2007). Since efficiency of righting varies significantly with Tb in M. leprosa and T. scripta turtles, individuals that attain and maintain Tbs that approach To will benefit from a positive increment in fitness. Thus, considering that righting performance of the two turtle species is speeded up at their respective species-specific preferred basking temperatures, the higher thermal inertia of exotic T. scripta turtles might confer them a competitive advantage over Spanish terrapins (Polo-Cavia et al. 2009b). Due to their greater capacity to retain heat, sliders might maintain preferred temperatures after basking for longer times than native turtles, whose higher tendency to loss body heat would make them more dependent on basking to maintain selected Tbs (Polo-Cavia et al. 2009b). Then, in a competitive situation in which introduced turtles actively displace native terrapins from the basking places and impede them to adequately bask (Polo-Cavia et al. in press), Spanish turtles might not be able to maintain the elevated Tbs that optimize righting.

 

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Also, T. scripta requires shorter times to turn right-side up than M. leprosa, likely due to their more rounded shell and specific anatomy of its neck, which might facilitate mechanical righting. In this way, introduced sliders could avoid the long exposure to potential predators and overheating risk while overturning that Spanish terrapins might have to endure. In addition, M. leprosa turtles are more prone to suffer a successful predatory attack during the time that they remain overturned, as more flattened turtles are more easily caught by snapping jaws or avian predators (Pritchard 1979; Janzen et al. 2000). Also, more rounded shells confer higher thermal inertias that protect turtles from desiccation and improve thermoregulation (Carr 1952; Wyneken et al. 2008; Polo-Cavia et al. 2009b). Thus, the lower thermal inertia of native turtles, compared with that of exotic ones, entails an increased risk of overheating if turtles become exposed to intense sun rays before they can return to their normal position and shift to a sheltered place. On the other hand, under extremely low temperatures, M. leprosa experiences a considerable increment in lengths of lag phase and mechanical stage of righting performance, which might exceedingly prolong the time overturned, thus compromising the survival of turtles. In contrast, T. scripta might minimize the risks of overturning by means of a more rounded shape that deters predators and facilitates righting, and a greater thermal inertia that protects turtles from overheating and favors the maintenance of selected Tbs that allow a highly efficient righting performance. Hence we can conclude that behavioral asymmetries in righting response between native and invasive turtle species might contribute to the greater competitive ability of T. scripta, thus favoring the expansion of sliders and aggravating the conservation state of populations of Spanish terrapins in environments in which exotic turtles are introduced.

Acknowledgements We thank A. Marzal for allowing field work in his dehesa state (“La Asesera”), the Exotic Animal Rescue Center “EXOTARIUM” for providing red-eared sliders, and “El Ventorrillo” MNCN Field Station for use of facilities. V. Polo helped with useful comments on data transformations. Financial support was provided by a MCI project CGL2008-02119/421 BOS, and by a MEC-FPU grant to N. P.-C. The experiments enforced all current laws of Spain and of the Environmental Organisms of the “Junta de Extremadura” and “Comunidad de Madrid” where they were performed.

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Morphol 260: 322 Sih A (1992) Prey uncertainty and the balancing of antipredator and feeding needs. Am Nat 139:

1052-1069 Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. Trends Ecol Evol

12: 375-376 Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, New York Stevenson RD, Peterson CR, Tsuji JS (1985) The thermal dependence of locomotion, tongue-

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Steyermark AC, Spotila JR (2001). Maternal identity and egg incubation temperature effects on snapping turtle (Chelydra serpentina) righting response. Copeia 2001: 1050-1057

Tosini G, Avery RA (1994) Diel variation in thermoregulatory set points of the lizard Podarcis muralis. Amph Rept 15: 93-96

Vilà M, Valladares F, Traveset A, Santamaría L, Castro P (2008) Invasiones biológicas. Consejo Superior de Investigaciones Científicas, Madrid

Wilson TP (1994) Ecology of the spotted turtles, Clemmys guttata, at the western range limit. PhD Dissertation, Eastern Illionois University

Wyneken J, Godfrey MH, Bels V (2008) Biology of Turtles. CRC Press, Taylor and Francis Group, Boca Raton

Capítulo 7

 

 

 

  

Las diferencias interespecíficas en las respuestas al riesgo de depredación  

pueden conferir ventajas competitivas a las especies invasoras de galápagos  

Nuria Polo Cavia, Pilar López y José Martín

Ethology 114 (2008) 115-123

 

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RESUMEN

La naturaleza de las interacciones competitivas entre especies nativas e introducidas no está clara. En la Península Ibérica, el galápago de Florida (Trachemys scripta elegans) se encuentra introducido como especie invasora, compitiendo y desplazando al galápago leproso (Mauremys leprosa). Es posible que diferencias potenciales en el comportamiento antidepredatorio de las dos especies puedan conferir ventajas competitivas al introducido T. scripta. En este estudio, examinamos si las diferencias interespecíficas en las respuestas al riesgo de depredación afectan al tiempo que los galápagos permanecen refugiados en el interior del caparazón antes de escapar activamente hacia el agua. Ambas especies de galápagos ajustaron el tiempo que pasaron escondidos en el caparazón en función del nivel de amenaza depredatoria, el microhábitat y los costes de mantenerse escondidos. Sin embargo, los introducidos T. scripta pasaron escondidos más tiempo que los nativos M. leprosa, los cuales, en contraste, escaparon rápidamente hacia aguas más profundas. Estas diferencias interespecíficas podrían deberse a los distintos tipos de depredadores (terrestres vs. acuáticos) que amenazan a los galápagos nativos e introducidos en sus respectivos hábitats originales. Sin embargo, en hábitats alterados antropogénicamente donde la presencia de depredadores se ha reducido considerablemente, T. scripta podría evitar los costes potenciales de repetidas e innecesarias huidas hacia el agua (e.g., la interrupción de actividades como el asoleamiento). Estas asimetrías en el comportamiento antidepredatorio entre las dos especies de galápagos podrían en parte explicar la mayor capacidad competitiva del introducido T. scripta en ambientes con modificaciones antropogénicas ■

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INTERSPECIFIC DIFFERENCES IN RESPONSES TO PREDATION RISK

MAY CONFER COMPETITIVE ADVANTAGES TO INVASIVE

FRESHWATER TURTLE SPECIES

Abstract The nature of competitive interactions between native and introduced invasive species is unclear. In the Iberian Peninsula, the introduced red-eared slider (Trachemys scripta elegans) is an invasive species that is competing and displacing the endangered native Spanish terrapin (Mauremys leprosa). We hypothesized that interspecific differences in antipredatory behavior might confer competitive advantages to introduced T. scripta. We examined whether interspecific differences in responses to predation risk affect the time that turtles remained hidden in the shell before using an active escape to water. Both turtle species adjusted hiding times by balancing predation threat, microhabitat conditions and the costs of remaining hidden. However, introduced T. scripta showed longer hiding times before escaping than native M. leprosa, which, in contrast, switched from waiting hidden in the shell to escape to deep water as soon as possible. These interspecific differences might result from the risk of facing different types of predators in different microhabitats (land vs. water) in their original habitats. However, in anthropogenically altered habitats where predators have been greatly reduced, T. scripta may avoid potential costs of unnecessary repeated escape responses to water (e.g., interruption of basking). These behavioral asymmetries could contribute to the greater competitive ability of introduced T. scripta within anthropogenically disturbed environments Keywords Freshwater turtles • Invasive species • Mauremys leprosa • Microhabitat • Predatory threat • Trachemys scripta

he introduction of alien species outside their natural geographic range area represents the second greatest threat to biodiversity after habitat destruction (Devine 1998; IUCN 2000; Mack et al. 2000). Alien species

may displace native species from their ecological niches by means or processes such as predation, hybridization, introduction of pathogens, or competition for resources (Dodd and Seigel 1991; Williamson 1996; Butterfield et al. 1997; Manchester and Bullock 2000). The outcome of competition processes depends on the ability of alien species to adapt to strange habitats, as well as on the ability of native species to resist invasion (Williamson 1996; Joly 2000). Alien invasive species are often those with wide ecological valence, high reproductive output, or that tolerate or benefit from human presence (Sax and Brown 2000; Kolar and Lodge 2001). Invasive species often come from areas with a high diversity of predators, which may favor these species that are better suited for evading predators than native species. Even if a species is introduced in a new habitat with fewer predators, a species subjected to past selection for antipredatory behavior will retain this behavior (i.e., ‘ghost of predators past’ hypothesis; Peckarsky and Penton 1988; Blumstein 2006). On the other hand, native species that occupy geographically isolated habitats, which have been anthropogenically modified and lack predators of alien species, are more prone to suffer invasions (Fox and Fox 1986; Ewell 1999; Sax and Brown 2000).

T

 

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The American red-eared slider (Trachemys scripta elegans) is currently introduced as a breeding species in many countries of Africa, Asia and Europe, especially in Mediterranean countries (Luiselli et al. 1997; Chen and Lue 1998; Pleguezuelos 2002). In the Iberian Peninsula, T. scripta have been released in diverse aquatic habitats after having been imported and sold as pets (Pleguezuelos 2002). Many observations indicate that introduced T. scripta are competing with the two native Iberian freshwater turtle species; the European pond terrapin (Emys orbicularis) and the Spanish terrapin (Mauremys leprosa). These native terrapins are considered as endangered species because their populations have considerably declined (Pleguezuelos 2002). However, the nature of the interspecific competitive interactions is unclear. Competition for food, refuges or basking places are likely to occur (Crucitti et al. 1990; Cadi and Joly 2003). The advantages of T. scripta as an invasive species over native freshwater turtles might be larger adult body size, more diverse diet, higher fecundity, earlier sexual maturity, adaptation to lower water temperatures, and a greater tolerance to pollution and human presence (Gibbons 1990; Pleguezuelos 2002). Also, the absence of Spanish terrapins in areas with high predation risk occupied by T. scripta (Pleguezuelos 2002) suggests that the native species is more sensitive to predation pressure. Although these freshwater turtles are predominately aquatic, they have to come to land for basking, where they are potential prey of birds and mammals (Greene 1988; Martín and López 1990). For this reason, they are very cautious, being extremely alert and vigilant, and diving quickly when disturbed. However, this seems to be especially true for native terrapins in Iberian habitats (López et al. 2005; N. Polo-Cavia, unpubl. data).

Turtles usually escape to a safe refuge such as water or thick vegetation when they detect danger. However, if a predator approaches close enough, turtles will withdraw and hide the legs, tail and head inside the shell, trying to deter the attack (Greene 1988; Hugie 2003). Most predators would leave turtles alone if they do not come out of the shell. However, some predators are able to break the shell or to access the soft parts of the turtle’s body (Greene 1988; Martín and López 1990; see also Mima et al. 2003 for a similar situation in hermit crabs). Turtles must choose between two alternative antipredatory tactics (passive hiding or active escape), but both may imply costs. Escaping to water may be safer in some habitats, but, apart from the energy lost in the escape sequence (Martín and López 1999a), it supposes an interruption of basking with a subsequent decrease in the efficiency of digestion under the low temperatures of water (Parmenter 1981; Huey 1982). Also, in some habitats entering the water soon after predator detection may expose turtles to aquatic predators. On the other hand, hiding in the shell allows turtles to continue basking, but it may decrease time available for mating or foraging (Sih et al. 1990; Koivula et al. 1995; Dill and Fraser 1997; Martín et al. 2003a,b), and this

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strategy may greatly increase the risk of being damaged at land (Mima et al. 2003).

Prey should adjust time spent inside refuges so that the optimal time to emerge is the time when the costs of staying exceed the costs of leaving (Sih 1992, 1997; Dill and Fraser 1997; Martín and López 1999b). Also, when using non-secure refuges, animals should estimate predation threat to decide whether and when to employ alternative defensive tactics if a predator persists in the attack (Martín and López 2003). Similarly, in turtles, the decision of when to emerge from their shells should be a trade-off between the perceived predation threat and the probability of reaching safe habitat and encountering a novel predator vs. the costs of remaining within the shell (Sih et al. 1998; Martín et al. 2005). This would require turtles to accurately assess predation threat and flexibly employ different antipredatory tactics as risk level changes. In the Iberian Peninsula, we have observed that a simulated terrestrial predator may approach closer to introduced T. scripta than to native M. leprosa while they are basking before they plunge in the water (N. Polo-Cavia, unpubl. data). This suggests that risk perception while basking might be different in native or invasive turtles, which might be due to the different types of predators in their original habitats. In this paper, we analyzed whether there were interspecific differences in responses to predation threat between introduced T. scripta and native M. leprosa in Iberian habitats. We specifically asked whether differences in risk assessment may affect the decision of using diverse antipredatory tactics that have different potential costs. We simulated attacks of different characteristics (different combinations of several factors of risk posed by the predator) and under different conditions of proximity to water refuges, which would contribute to the total estimation of risk. Particularly, we examined how perceived predation threat affected the time that turtles remained hidden in the shell before using an active escape strategy. We hypothesized that T. scripta will remain withdrawn into the shell for longer, trying to deter the predator, before incurring costs of an active escape. In contrast, M. leprosa will initiate, as soon as possible, an active flee to deep water. Thus, in habitats where current human pressure had greatly reduced the numbers of predators, the costs derived from interruption of basking and repeated unnecessary flees to water (Dill and Fraser 1997; Sih 1997; Martín and López 1999a) might suppose a disadvantage for native turtles when competing with introduced ones.

METHODS

Study Animals

During May 2005, we captured 20 adult T. scripta (9 males and 11 females; carapace straight length: mean ± SE = 15.1 ± 1.5 cm, range = 12.7-17.7 cm) from

 

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a large seminatural outdoor pond where they had been maintained by the conservationist organization “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These turtles had been extracted from introduced populations in central Spain to avoid their negative effects on populations of native terrapins. We also captured, during May, with funnel traps 16 adult M. leprosa (9 females and 7 males; carapace straight length: mean ± SE = 15.2 ± 0.5 cm, range = 14.6-19.3 cm) in several ponds and tributary streams of the Guadiana river, located inside dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza and Alconchel (Badajoz Province, southwestern Spain). In this area, we verified the presence of many known potential predators of this turtle, including birds such as white storks (Ciconia ciconia), grey herons (Ardea cinerea), Egyptian vultures (Neophron percnopterus) and black kites (Milvus migrans), and mammals, such as wild boars (Sus scrofa), and foxes (Vulpes vulpes) (Martín and López 1990; Andreu and López-Jurado 1998). All turtles were individually housed at “El Ventorrillo” Field Station (Navacerrada, Madrid Province), in outdoor aquaria (60 x 40 x 30 cm) with water and stones that allowed them to bask. The temperature and photoperiod were the same as the natural surroundings. Turtles were fed mince beef, earthworms and slugs three times a week. Turtles were held in captivity for at least two weeks before experiments, to allow turtles to habituate to captivity conditions. At the end of experiments, all turtles had maintained their body mass, and were returned to the GREFA ponds (T. scripta) or to their exact field capture sites (M. leprosa).

Experimental Procedure

We simulated predatory attacks toward individual turtles in an outdoor transparent plastic container (70 x 60 x 15 cm) with either a substrate of low grass (‘land’ treatment) or filled with 4 cm deep clean water (‘water’ treatment). This container was used as a mean to keep water or grass within a controlled standardized area, but turtles could see all the surroundings and easily go out from the container, so that their behavior was not restricted by the container walls. Thus, we simulated two different microhabitat conditions: the turtle was attacked on land, away from a water pool, or in a shallow water area similar to river banks, presumably close to deeper water areas (Martín et al. 2005). To simulate different levels of predation threat, we took one turtle from its aquarium and after handling it gently for 2 s, we released it in the middle of the experimental container (‘low predation threat’ treatment). Alternatively, we handled the turtle for 5 s, left it in the experimental container, and we continued simulating the attack by handling and tapping the shell with the hand during 20 s before definitively releasing it (‘high predation threat’

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treatment). Thereafter, and without further handling, the experimenter simulated either a persistent waiting predator by remaining immobile at a point close to the container (<1 m; ‘close’ treatment), or a predator that left the area to a hidden position at a distance of 8 m (‘far’ treatment). To avoid confusing effects that may affect risk perception, all experiments were performed by the same person, in a similar way and wearing the same clothes (Burger and Gochfeld 1993).

We tested each individual turtle under all the eight possible combinations of treatments, and order of presentation of treatments was randomized. Each turtle participated in only one trial per day to minimize the influence of stress resulting from one test on the results of subsequent tests. Before the trials, turtles were allowed to bask for at least 2 h in their home aquaria, so that they could attain optimal body temperatures (Andreu and López-Jurado 1998). We ensured that ambient temperature was similar during all tests.

After the attacks, and as a result of handling, turtles usually remained withdrawn into the shell (head, legs and tail were not visible from above the carapace). After some time spent entirely withdrawn in the shell, turtles typically put the head partially out from the shell until the eyes could be used to scan the surroundings. Then, turtles waited for a while, and finally put the head, neck and legs entirely out from the shell, and started to walk. We used a stopwatch to record, to the nearest second, the time that turtles spent withdrawn inside their shell after release into the container until the head emerged and the eyes were out of the carapace (appearance time). We then measured the time from appearance until the head and legs emerged completely and the turtle started walking (waiting time). These two hiding times were considered because turtles entirely withdrawn into the shell had no visual information of the predator or the surroundings until the ‘appearance time’. Thus, ‘waiting time’ represented the time during which the turtle could visually scan the environment, and decide whether and when to switch to active escape toward safer refuges (Martín and López 1999b; Martín et al. 2005).

Data Analyses

We used repeated measures analyses of variance (ANOVAs) to test for differences in appearance and waiting times of the same individual turtle in each condition of microhabitat (land vs. water), perceived predation threat (low vs. high) and predator persistence (close vs. far), all of them within factors. The turtle species was included as a between-subjects factor. Data were log-transformed to ensure normality (verified by Shapiro-Wilk’s test) and we tested for homogeneity of variances (Levene’s test). Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995).

 

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RESULTS

Appearance Time

The two turtle species differed significantly in the length of time they remained entirely hidden inside their shells after a staged predatory encounter (repeated measures ANOVA, F = 7.92, df = 1,32, P = 0.008), with T. scripta having longer overall appearance times (mean ± SE = 19 ± 5 s) than M. leprosa (5 ± 6 s). There were no significant differences between sexes in appearance time for either turtle species (sex: F = 0.01, df = 1,32, P = 0.96; sex x species: F = 0.02, df = 1,32, P = 0.88). Thus, sex was not considered in further analyses.

Despite the magnitude of differences in appearance times between species, the effects of microhabitat and perceived predation threat were similar for both turtle species (i.e., no interaction with species). Appearance times were significantly longer on land than in water, and significantly longer when perceived predation threat was high than when it was low (Fig. 7.1; Table 7.1). However, there was a significant interaction between microhabitat and perceived predation threat. Both turtle species appeared from their shells more quickly following a low predation threat attack than a high predation threat attack when they were on land (Tukey’s test, P = 0.0002), but there was no significant difference in their response to low vs. high predation threat in water (P = 0.97).

The effect of predator persistence differed significantly between the two turtle species (interaction: persistence x species; Table 7.1). However, post hoc Tukey’s tests did not provide any significant result for these differences (P > 0.46 in all cases). The rest of effects and interactions were non-significant (Table 7.1). Waiting Time

The two turtle species differed significantly in the length of time they remained waiting with their heads partially out of the shell until they started walking (repeated measures ANOVA, F = 34.98, df = 1,32, P < 0.001), with overall waiting times of T. scripta (174 ± 27 s) being significantly longer than those of M. leprosa (93 ± 30 s). Waiting time did not significantly differ between sexes in any turtle species (sex: F = 0.69, df = 1,32, P = 0.41; sex x species: F = 0.10, df = 1,32, P = 0.75). Thus, sex was not considered in further analyses.

Microhabitat and predator persistence affected waiting times of both turtle species. Thus, overall waiting times were significantly longer on land than in water, and significantly longer when the predator remained close to the turtle

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Figure 7.1 Mean (± SE) appearance times from their shells of (a) introduced T. scripta and (b) native M. leprosa after an attack. Six conditions of attacks were simulated: two different perceived predation threat levels (‘low’ vs. ‘high’), two different microhabitats (‘land’ vs. ‘water’) and the experimenter either remained close to the turtle (‘close’) or retreated to a distant hidden position (‘far’)

Table 7.1 Results from three-way repeated measures ANOVAs examining the effects of turtle species, microhabitat, perceived predation threat and predator persistence on appearance and waiting times of turtles (df = 1,34 in all cases)

Appearance time Waiting time

Effect F P F P

Species 8.53 0.006 35.58 < 0.0001 Microhabitat 23.16 < 0.0001 38.16 < 0.0001 Microhabitat x species 0.07 0.80 2.93 0.10 Predation threat 11.69 0.0016 1.11 0.30 Predation threat x species 0.35 0.56 0.25 0.62 Persistence 0.25 0.62 38.71 < 0.0001 Persistence x species 6.95 0.012 2.04 0.16 Microhabitat x predation threat 20.29 < 0.0001 17.30 0.0002 Microhabitat x predation threat x species 1.76 0.19 7.52 < 0.01 Microhabitat x persistence 2.11 0.16 15.58 0.0004 Microhabitat x persistence x species 1.43 0.24 27.41 < 0.0001 Predation threat x persistence 0.34 0.56 2.65 0.11 Predation threat x persistence x species 1.87 0.18 0.54 0.47

 

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Figure 7.2 Mean (± SE) waiting times of (a) introduced T. scripta and (b) native M. leprosa after an attack. Six conditions of attacks were simulated: two different perceived predation threat levels (‘low’ vs. ‘high’), two different microhabitats (‘land’ vs. ‘water’) and the experimenter either remained close to the turtle (close) or retreated to a distant hidden position (far)

after the attack. However, the effects of predation threat level and predator persistence depended of microhabitat and differed between turtle species (Fig. 7.2; Table 7.1). Thus, with respect to the interaction ‘microhabitat x predation threat x species’, predation threat level did not significantly influence waiting times of T. scripta in either microhabitat (Tukey’s test, P = 0.99 in both cases), whereas waiting times of M. leprosa were not affected by predation threat level on land (P = 0.64) but were significantly shorter under high predation threat in water (P = 0.0007). With respect to the interaction ‘microhabitat x persistence x species’, waiting times of T. scripta were not affected by predator persistence in any microhabitat (Tukey’s tests, water: P = 0.14; land: P = 0.64), whereas in M. leprosa predator persistence was not important in water (P = 0.99), but on land waiting times were significantly longer when the predator remained close (P = 0.0001). The rest of interactions were non-significant (Table 7.1).

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DISCUSSION

Our results revealed that T. scripta and M. leprosa differed in the magnitude of their hiding responses after a predatory attack. The invasive T. scripta spent longer times withdrawn into the shell before emerging and switching to an active escape response. However, despite the magnitude of differences in hiding times, both turtle species also adjusted the time spent withdrawn into their own shell by assessing predation threat, and microhabitat conditions.

In response to predators, basking turtles may choose between withdrawing into their shells and actively escaping to a water source (Martín et al. 2005). Predators typically would abandon immobile hidden prey (Martín and López 1999a,b; Hugie 2003). However, time spent within the shell implies costs such as the risk of overheating on land, or the loss of time available for foraging or mate searching (Martín et al. 2003a,b). But initiating active escape entails other more important costs for turtles, such as alerting the predator in case it has not noticed the prey, the energy spending in the dash for flee, and especially the interruption of basking. Basking is a crucial activity for turtles and other ectotherms (Huey 1982; Crawford et al. 1983) because increasing body temperature activates metabolism and digestive turnover rates (Kepenis and McManus 1974; Parmenter 1981). Therefore, to decide when to change between these two antipredatory tactics (i.e., duration of hiding times), turtles must be able to balance all the costs associated to both tactics, the risk of emerging from the shell before the predator has left (Sih 1992; Hugie 2003), the possibility of reaching a safer refuge in different microhabitats (Martín et al. 2005), and also the potential risk of predation in water by other types of predators (Sih et al. 1998). Similar modification of hiding times occurs in sessile animals hidden inside their defensive structures (Dill and Gillett 1991; Johansson and Englund 1995; Dill and Fraser 1997), and in mobile animals hidden in external refuges (Cooper 1998; Martín and López 1999a,b).

Interestingly, our results indicate that the combined effects of these factors also differed between turtle species. Thus, on land both turtle species appeared sooner if the risk was low than if it was high, but, in the water, they appeared quickly from the shell under both predation threat levels as the possibility of escaping successfully toward safer deep waters is greater than the one of dissuading the terrestrial predator by remaining hidden. However, T. scripta did not alter waiting time in response to predation threat, but had shorter waiting times in the water than on land, whereas M. leprosa did alter their waiting times in response to predation threat and microhabitat, having shorter waiting times under high threat compared with low threat in the water, but not on land.

 

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Predator persistence did not affect appearance from shell in any species, suggesting that when the turtles are withdrawn inside the shell, they could not visually determine whether a predator was still present (Martín et al. 2005). Only when turtles had their eyes outside the shell, they can acquire more visual information on the predator. However, waiting times were not affected by predator persistence in T. scripta, whereas in M. leprosa, predator persistence influenced waiting times only when turtles were on land and there were no other alternative refuges, but not when they could escape toward a safer refuge in water even if the predator was close.

These interspecific differences in responses to predation risk might be explained because predators of adult M. leprosa are terrestrial mammals and birds (Martín and López 1990), and, thus, this turtle species is safer in deep water, where no predators occur. In contrast, T. scripta elegans comes from an original habitat with terrestrial predators that prey mainly on young and eggs (e.g., raccoons, skunks, foxes, raptors and storks), but where the greatest danger comes from aquatic predators (i.e., caimans and crocodiles), which also attack adults (Greene 1988). Prey exposed to multiple types of predators can experience two conflicts; if enhanced survival to one predator simultaneously increases vulnerability to another predator, or if prey have limitations to produce only one type of defensive response at a time (Sih et al. 1998; DeWitt et al. 2000). If prey have a conflict with specific defensive tactics to multiple predators, and one predator type is more dangerous than the other, then prey should tend to ignore the less dangerous predator (Lima 1992; McIntosh and Peckarsky 1999; Bouwma and Hazlett 2001). Thus, in their original habitat, basking T. scripta should remain hidden inside the shell for longer before initiating active escape toward the water, since entering quickly in water can face sliders with other more dangerous aquatic predators. In contrast, basking M. leprosa should favor the strategy of escaping toward the safety of deep water whenever possible and immediately after any smallest alarm signal on land (López et al. 2005). This latter species would use the shell as a refuge only when it was on land far from water and predator’s harassment was extreme. In agreement with this prediction, preliminary field observations in Iberian habitats suggested that a terrestrial predator might approach closer to basking T. scripta than to basking M. leprosa before they dived in water (N. Polo-Cavia unpubl. data).

In their original habitat, T. scripta would be able to face potential attacks by little dangerous terrestrial predators, by just remaining immobile on basking places, while avoiding exposure to more dangerous, aquatic predators. Also, the antipredatory behavior of native M. leprosa could decrease predation by their main terrestrial predators in their natural habitats. However, in circumstances in which human pressure on the ecosystems increases and terrestrial predators

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are reduced, interspecific differences in responses to predation risk may confer a greater competitive ability to introduced T. scripta. This is especially true when human disturbance, which carries little risk of actual predation, leads to unnecessary escapes by native species. In these altered habitats, where T. scripta is mainly introduced, T. scripta could avoid unnecessary fled tactics and perform basking with fewer interruptions than M. leprosa. Actually, introduced T. scripta seemed more competitive for the most suitable basking places than native European pond turtles E. orbicularis, resulting in a more efficient occupation of basking sites by American turtles (Cadi and Joly 2003). A similar competition for basking places between T. scripta and M. leprosa has been confirmed experimentally (Polo-Cavia et al. in press).

In conclusion, antipredatory decisions of turtles were influenced by predation threat and by the costs of using refuges, but also by characteristic responses to risk by each species in the different microhabitats. However, these antipredatory strategies may not be entirely optimal for both turtles species in anthropogenically altered habitats into which T. scripta are introduced. These results provide an interesting opportunity for further field studies that investigate the impact of habitat conservation on the success of invaders. Nevertheless, these interspecific differences are probably not sufficient to explain the displacement of native M. leprosa by introduced T. scripta. Therefore, other factors such as differences in feeding, thermal requirements, growth, and reproductive efficiency, must be considered as jointly responsible for the recession that native European freshwater turtles suffer at this moment. Acknowledgements We thank two anonymous reviewers for helpful comments, the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders, A. Marzal, D. Martín, and A. Pintado for allowing field work in their dehesa states, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the project MEC-CGL2005-00391 ⁄ BOS, and by an “El Ventorrillo” CSIC grant and a MEC-FPU grant to N. P.-C. The experiments enforced all the present Spanish laws and of the Environmental Organisms of the Extremadura and Madrid Communities where they were carried out. REFERENCES Andreu AC, López-Jurado LF (1998) Mauremys leprosa (Schweigger, 1812). In: Ramos MA (ed)

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Capítulo 8

 

 

 

  

La incapacidad de los renacuajos  para reconocer depredadores introducidos puede conferir ventajas competitivas 

 a los galápagos invasores 

Nuria Polo Cavia, Adega Gonzalo, Pilar López y José Martín

En revisión

 

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RESUMEN

El impacto que los depredadores exóticos ejercen sobre las poblaciones de presas nativas es de sobra conocido en biología de la conservación. Sin embargo, se ha prestado escasa atención a los efectos negativos que la introducción de depredadores exóticos puede ocasionar sobre los depredadores nativos a través de la competencia por los recursos tróficos. En la Península Ibérica, el galápago de Florida (Trachemys scripta elegans) se encuentra introducido junto con otras especies exóticas de galápagos. Estos galápagos se comportan como especies invasoras, compitiendo y desplazando a los galápagos nativos (el galápago europeo, Emys orbicularis, y el galápago leproso, Mauremys leprosa). Aunque no está claro cómo se producen las interacciones competitivas, es posible que exista competencia directa por la alimentación. Tanto los galápagos nativos como los exóticos depredan habitualmente sobre renacuajos de anfibios. Los renacuajos son capaces de reconocer y responder de forma innata a las señales químicas de los depredadores locales, pero a menudo se muestran incapaces de reconocer especies nuevas de depredadores potenciales con los que no han compartido una larga historia evolutiva. Examinamos la capacidad de cuatro especies de renacuajos de anuros ibéricos para reconocer y responder a estímulos químicos de galápagos nativos y exóticos invasores. Tres de las cuatro especies de renacuajos redujeron su actividad natatoria frente a estímulos químicos de galápagos nativos presentes en el agua, pero ninguna de ellas modificó su nivel de actividad frente a estímulos químicos de galápagos exóticos. Sugerimos que esta incapacidad de las presas para discriminar y responder de forma innata a las sustancias químicas de depredadores introducidos podría conferir ventajas competitivas a las especies invasoras. Esta podría ser una de las causas que expliquen el desplazamiento de las poblaciones nativas de galápagos ibéricos por los galápagos exóticos invasores, y podría también contribuir a clarificar la paradoja de por qué los depredadores exóticos a menudo prosperan mejor en sus nuevos hábitats que los depredadores nativos localmente adaptados ■

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FAILED PREDATOR-RECOGNITION BY TADPOLE PREY MAY CONFER

COMPETITIVE ADVANTAGES TO INVASIVE TURTLE PREDATORS

Abstract The impact of alien predators on prey populations is well known by conservation biologists, but little attention has been paid to the negative effects that the introduction of exotic predators may have over native predators through competition for food. In the Iberian Peninsula, the red-eared slider (Trachemys scripta elegans) and other exotic freshwater turtles have been introduced. These exotic turtles behave as invasive species that compete and displace the populations of native endangered terrapins (the European pond turtle, Emys orbicularis, and the Spanish terrapin, Mauremys leprosa). Although the nature of competitive interactions is not clear, direct competition for food is likely to occur. Both native and invasive freshwater turtles are common predators of amphibian tadpoles. Naïve amphibian tadpoles may be able to recognize and respond to local predators with no prior experience, but tadpoles might not recognize new potential predatory species, since they have not shared a long evolutionary history with them. We examined the ability of four species of Iberian anuran tadpoles to recognize and respond to chemical cues from invasive and native freshwater predatory turtles. Three of the four tadpole species tested reduced their swimming activity when chemical cues from native turtles were present in water, but activity levels remained invariable when cues belonged to exotic turtles. We suggest that this inability of tadpole prey to innately discriminate and respond to chemicals from introduced predatory turtles might confer a competitive advantage to invasive turtles over native terrapins. This may be one of the causes that explains the displacement of native populations of Iberian terrapins by invasive exotic turtles, and may contribute to clarify the paradox of why alien predators sometimes prosper better in new habitats than locally adapted predators. Keywords Alien predators • Amphibian tadpoles • Chemoreception • Freshwater turtles • Invasions • Predation risk

he introduction of alien predators outside their natural geographic range area can create novel ecological contexts in which the adaptive antipredatory responses of native prey may not be successful (Callaway

and Aschehoug 2000; Shea and Chesson 2002). Decision making rules or ‘Darwinian algorithms’ (Cosmides and Tooby 1987) are expected to be adaptive in the environment in which species evolved, because they rely on cues that, over evolutionary time, promote survival and reproductive success in such environments (Williams and Nichols 1984). Thus, adaptive evolutionary responses of prey to predation risk adequately work in their specific habitats, but organisms may not be innately equipped to cope with suddenly introduced new predators (Schlaepfer et al. 2002). Prey are often naïve to the hunting tactics of novel introduced species or unable to detect these alien predators, which result more harmful to prey populations than native predators (Salo et al. 2007). In this context, alien predators are considered to be one of the most important causes of decline and extinction of prey species (Vitousek et al. 1997).

Impact of alien predators on prey populations is well documented (Dickman 1996; Kinnear et al. 2002), but less attention has been paid to the competitive

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advantages of alien predatory species over endangered native ones. When invasive predators alter environments in such a way that normal antipredatory strategies of native prey are no longer adaptive, they may benefit from evolutionary releases (Schlaepfer et al. 2005). The advantage of an evolutionary release may explain the paradox of why invasive species sometimes enjoy a competitive advantage over locally adapted species (Blossey and Notzold 1995; Shea and Chesson 2002; Allendorf and Lundquist 2003). For example, several studies have demonstrated that larval amphibians from populations that have co-occurred during long time with predatory fish or bullfrogs are able to recognize and respond to these predators without any prior experience (Kats et al. 1988; Sih and Kats 1994; Kiesecker and Blaustein 1997). In contrast, naïve larval amphibian often cannot recognize introduced species such as bullfrogs (Kiesecker and Blaustein 1997) or crawfish (Marquis et al. 2004) as potential predators, since these prey have not shared a long evolutionary history with these novel predators. As a result, alien predators are released from some of the difficulties of finding larval amphibian prey, which keep working for native predators (Lawler et al. 1999; Kiesecker et al. 2001; Baber and Babbitt 2003). Nevertheless, there are a few documented cases of native prey able to learn or evolve the ability to avoid invasive species (Chivers and Smith 1995; Kiesecker and Blaustein 1997; Chivers et al. 2001).

In the Iberian Peninsula, the two native freshwater turtles, Emys orbicularis and Mauremys leprosa, are common predators of amphibian tadpoles (Arnold and Ovenden 2002; Gomez-Mestre and Keller 2003). Both turtle species are similar in body size and may be locally abundant in permanent and temporary ponds, posing a threat to tadpole populations, especially in spring, when peak densities of many tadpole species coincide with the main activity season of turtles (Díaz-Paniagua 1988; Keller 1997). Both turtle species consume mainly animal matter, although M. leprosa also feeds on plants, whereas E. orbicularis is an almost strict carnivore and insectivore (Keller and Busack 2001). Both terrapins are considered as endangered species due to the considerable decline of their populations since the last decades (Pleguezuelos et al. 2002). Although habitat destruction and human pressure are major causes for this recession, competition with introduced exotic turtle species might be worsening the conservation state of native Iberian turtles (Da Silva and Blasco 1995; Pleguezuelos et al. 2002). Red-eared sliders (Trachemys scripta elegans) and other exotic freshwater turtle species are nowadays introduced as breeding species in diverse aquatic habitats of many Mediterranean countries (Luiselli et al. 1997; Pleguezuelos 2002). The introduction of these turtles was due to uncontrolled releases after having been imported into Europe and sold as pet animals. Many observations indicate that introduced turtles are competing with the native Iberian turtle species. However, how the interactions are taking

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place is not clear. Competition has been described between sliders and the European pond turtle (Emys orbicularis) (Cadi and Joly 2003), and recent studies suggest that competition is very likely to occur also between sliders and the Spanish terrapins (Polo-Cavia et al. 2008, 2009a,b). A greater tolerance to pollution and human presence (Pleguezuelos 2002), combined with larger adult body sizes and higher fecundity (Gibbons 1990), seem to be the main advantages of introduced turtles in the Iberian habitats. Although sliders are more phytophagous than the two native terrapins (Díaz-Paniagua et al. 2002), direct competition for food is very likely to occur in wild, because invasive freshwater turtles also feed on animal matter (frequently native amphibians), as native turtles do (Pleguezuelos 2002). Feeding competition between sliders and native terrapins has been confirmed in laboratory, as well as predatory events over amphibian tadpoles by both native and invasive turtles (N. Polo-Cavia, unpubl. data). In this context, we hypothesized that the ability of larval amphibian prey to innately detect predation risk posed by native turtle predators, but not risk posed by invasive ones, might confer an initial competitive advantage to alien freshwater turtle species over native ones (at least until learned predator-avoidance behavior propagates through a naïve tadpole population), thus favoring the expansion of invasive turtle species.

It has been widely tested that tadpoles (among other aquatic prey) strongly respond to the presence of chemical cues from potential predators by reducing their activity levels as an antipredatory strategy (e.g., Stauffer and Semlitsch 1993; Wilson and Lefcort 1993; Holomutzki 1995; Kiesecker et al. 1996; see Kats and Dill 1998 for a review). In this study, we experimentally tested the ability of different species of native anuran larvae to recognize in water chemical cues from native and exotic freshwater turtle species, and consequently to display antipredatory responses. We used naïve tadpoles that had no previous contact with invasive turtles to avoid conditioning the response by learned recognition of the introduced predators. METHODS Study animals During May 2007, we collected by netting larval tadpoles of four anuran species. We collected tadpoles of common tree frogs (Hyla arborea) in several ponds located inside dehesa woodlands with scattered holm oak (Quercus ilex) at Olivenza (Badajoz Province, southwestern Spain) where native turtles were common but exotic ones did not occur. Tadpoles of Iberian green frogs (Pelophylax perezi), natterjack toads (Bufo calamita) and western spadefoot (Pelobates cultripes) were collected in several temporary small ponds in Collado

 

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Mediano (Madrid, central Spain), where native and exotic turtles were absent. Tadpoles were transported to “El Ventorrillo” Field Station (Navacerrada, Madrid Province) and housed individually in plastic inner aquaria (18 x 25 x 10 cm) with water at ambient temperature and under a natural photoperiod. They were fed every two days with commercial fish flakes. No contact with the scent and visual stimuli of turtles was allowed before tadpoles were tested.

We also captured with baited funnel traps some individuals of native and invasive freshwater turtle species that are common potential predators of tadpoles to be used as predator scent donors. Native Spanish terrapins (M. leprosa) and European pond terrapins (E. orbicularis) were collected in ponds and tributary streams of the Guadiana River at Olivenza (Badajoz Province, southwestern Spain). Introduced red-eared sliders (T. scripta) and false map turtles (Graptemys pseudogeografica) were obtained from a large seminatural outdoor pond where they had been maintained by the conservationist organization “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA). These turtles had been extracted from introduced populations in central Spain, with the purpose of preserving the original ecosystem balance. Turtles were housed individually at “El Ventorrillo” Field Station in outdoor aquaria (60 x 40 x 30 cm) with water and stones that allowed them to bask. The temperature and day-length cycle of light were the same as the natural surroundings. To avoid potential confounding effects of the diet on the results, all turtles were fed small pieces of commercial compound feed, which did not contain tadpoles, during two weeks before collecting their chemical stimuli.

We obtained from a commercial dealer non-predatory zebra danio fish (Brachyodanio rerio) to be used as source of neutral scent. Before and after the experiment finished, fishes were maintained in a large filtered aquarium and regularly fed with commercial fish flakes.

All the animals were healthy during the trials, all maintained or increased their original body mass, and all tadpoles metamorphosed into subadult anurans. At the end of the tests, all these frogs and toads and the turtles were returned to their exact field capture sites or to the GREFA ponds.

Chemical stimuli

Each turtle aquaria was filled with 5 L of clean water and left overnight to prepare the turtle scents. Then, we extracted and mixed the water of two conspecific turtles, and froze it in 10 mL portions until use. Clean water was collected from a nearby high mountain spring that did not house frogs nor fishes nor turtles.

The neutral stimulus was prepared by placing zebra danio fishes in groups of three into a 3 L aquarium with clean water for three days. These aquaria

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were aerated but not filtered. Fishes were not fed during this short period to avoid contaminating water with food odor. Thereafter, water was drawn from the aquaria and frozen in 10 mL portions until its use in experiments. Fishes were returned and fed in their home large aquaria. We prepared control water in an identical manner but without placing fishes or turtles in the aquaria (Woody and Mathis 1998; Gonzalo et al. 2007).

Experimental procedure

To determine whether larval anuran tadpoles assess predation risk of native and exotic turtles differently, we designed an experiment to analyze the levels of basal activity of tadpoles in pools filled with water with chemical stimuli from different species of turtles. We tested separately 15 individual tadpoles of each anuran species in six different treatments (‘clean water’ vs. ‘E. orbicularis scent’ vs. ‘M. leprosa scent’ vs. ‘T. scripta scent’ vs. ‘G. pseudogeographica scent’ vs. ‘non-predatory fish scent’) in a random sequence. We allowed tadpoles to rest for one day between trials to avoid stress. ‘Clean water’ treatment was included to determine the basal activity level of tadpoles in a predator-free environment, and to use it as a control for the effect of the different turtle predators and the fish. The ‘non-predatory fish scent’ treatment was used to test for a possible alteration of activity levels due to any strange odor present in the water. The six treatments were carried out in parallel, and observations were carried out blind.

Tadpoles were tested individually in grey, U-shaped, gutters (101 x 11.4 x 6.4 cm) sealed at both ends with plastic caps. We marked the internal part of the gutters with four crossing lines that created five subdivisions of equal surface. We filled each gutter with 3 L of clean water from a mountain spring at 20 °C and 20 mL test solutions (two ice aliquots) of clean water or turtle or fish scent. We assigned test solutions to one end of each trough (right or left) by stratified randomization (see Rohr and Madison 2001; Gonzalo et al. 2007).

We placed a single tadpole covered with a release cage (made of clear plastic; 21 x 7.6 x 6.4 cm) in the middle of the central subdivisions of each gutter, and waited 5 min for acclimation. Then we deposited the test solution ice aliquots and we began trials by slowly lifting the cages above each tadpole 5 min after we deposited the test solution ices aliquots (i.e., after the ices aliquots had entirely thawed). We used the instantaneous scan sampling method to monitor each tadpole during 30 min, scanning as motionless as possible from a hidden position and recording at 1 min intervals the quadrant that each tadpole occupied (30 scans per tadpole in total). We calculated levels of activity from the number of lines crossed by each tadpole during the observation period (Rohr and Madison 2001; Gonzalo et al. 2007). Diffusion of chemicals in still water may be a slow process. However, all individual tadpoles used in the

 

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experiment were observed at least once in all of the subdivisions of the gutter, so we were confident that all tadpoles were really exposed to the chemical stimuli. Moreover, tadpoles often showed episodes of fast swimming which should contribute to diffuse chemicals in water.

Statistical analyses

We used separate one-way repeated measures analyses of variance (ANOVAs) for each tadpole species to analyze the differences in basal activity levels of the same individual tadpole across the six treatments with water containing different chemical cues (within subject factor; ‘clean water’ vs. ‘non-predatory fish’ vs. ‘E. orbicularis’ vs. ‘M. leprosa’ vs. ‘T. scripta’ vs. ‘G. pseudogeographica’). Levels of activity (number of lines crossed by tadpoles) were log-transformed to ensure normality (verified by Shapiro-Wilk’s test) and tests of homogeneity of variances (Levene’s test) showed that variances were not significantly heterogeneous. Pairwise comparisons were made using Tukey’s honestly significant difference tests (Sokal and Rohlf 1995). RESULTS

We found significant differences between predator cue treatments in overall activity levels of three of the four species of anuran tadpoles that we tested (Fig. 8.1). Tadpoles of H. arborea, P. perezi and P. cultripes showed significantly different levels of activity between treatments (one-way repeated measures ANOVAs, H. arborea: F = 6.97, df = 5,70, P < 0.0001; P. perezi: F = 15.02, df = 5,70, P < 0.0001; P. cultripes: F = 7.20, df = 5,70, P < 0.0001). However, there were no significant differences in overall activity levels of B. calamita tadpoles between treatments (F = 0.26, df = 5,70, P = 0.93).

Baseline activity levels of H. arborea tadpoles in clean water were not significantly different of those in the non-predatory fish treatment (Tukey’s tests, P > 0.99) and in both exotic turtle treatments (T. scripta: P = 0.94; G. pseudogeographica: P = 0.58). However, H. arborea tadpoles significantly responded to chemical cues from native turtle species by reducing their activity levels with respect to their baseline activity in clean water (E. orbicularis: P = 0.002; M. leprosa: P = 0.0008). Activity levels of H. arborea tadpoles in water with non-predatory fish stimulus did not significantly differ from those in water with both T. scripta and G. pseudogeographica cues (P > 0.80 in both cases), but activity levels were significantly lower in water with chemical cues from both native turtles than in water with non-predatory fish stimulus (E. orbicularis: P = 0.007; M. leprosa: P = 0.003). Responses to both E. orbicularis and M. leprosa stimuli significantly differed from responses to T. scripta

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Figure 8.1 Activity levels (mean ± SE number of lines crossed during 30 min) of four species of anuran tadpoles: (a) H. arborea, (b) P. perezi, (c) P. cultripes and (d) B. calamita, in trials with clean water, water with chemical cues from a non-predatory fish and water with chemical cues from two native predatory turtle species (Emys orbicularis and Mauremys leprosa), and two exotic predatory turtle species (Trachemys scripta and Graptemys pseudogeographica) 

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stimulus (P = 0.03 and P = 0.01 respectively), but they did not differ significantly from responses to G. pseudogeographica stimulus (P = 0.17 and P = 0.09 respectively). Responses to chemical cues from the two native turtles were not significantly different (P > 0.99), and neither were responses to chemical cues from the two exotic turtles (P = 0.98).

Tadpoles of P. perezi showed no significant differences between activity levels in clean water and those in water with chemical cues from the non-predatory fish, or from both exotic predatory turtles (Tukey’s tests, P > 0.99 in all cases). However, P. perezi tadpoles reduced their activity in water with chemical cues from both native predatory turtles (E. orbicularis: P = 0.0001; M. leprosa: P = 0.002). Responses to the non-predatory fish stimulus did not significantly differ from responses to both exotic turtle stimuli (P > 0.99 in both cases), but responses to fish were significantly different from responses to both native turtle stimuli (E. orbicularis: P = 0.0001; M. leprosa: P = 0.005). Responses to both exotic turtles differed significantly from responses to both native turtles (P < 0.003 in all cases). There were no significant differences between responses to E. orbicularis and M. leprosa stimuli (P = 0.17) and neither there were between responses to T. scripta and G. pseudogeographica (P > 0.99).

Tadpoles of P. cultripes significantly reduced their activity levels in water with chemical cues from the native turtle E. orbicularis in comparison with their basal activity in clean water (P = 0.004), but there were non-significant differences in activity between clean water and the rest of experimental treatments (non-predatory fish: P = 0.80; M. leprosa: P = 0.12; both exotic turtles: P > 0.99). Differences between responses to non-predatory fish stimulus and both exotic turtles stimuli were non-significant (P > 0.60 in both cases), but differences between responses to non-predatory fish stimulus and both native turtles stimuli were significant (E. orbicularis: P = 0.0002; M. leprosa: P = 0.004). Activity levels of P. cultripes tadpoles in water with chemical cues from native E. orbicularis were significantly different from those in water with chemical cues from both exotic turtles (T. scripta: P = 0.004; G. pseudogeographica: P = 0.01), but they did not differ from those in water with chemical cues from native M. leprosa (P = 0.80). However, activity levels in water with M. leprosa cues were not significantly different from those in water with chemical cues from exotic turtles (T. scripta: P = 0.14; G. pseudogeographica: P = 0.24). There were no significant differences between responses to the two exotic turtles’ stimuli (P > 0.99).

DISCUSSION

Our results confirm that antipredatory responses in amphibian larvae are mediated by water-borne chemical cues, and particularly show that different

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species of native Iberian anuran tadpoles can use chemoreception to assess predation risk. We observed substantial variation in the activity levels of H. arborea, P. perezi and P. cultripes tadpoles when they perceived dissimilar degrees of predatory threat through chemical cues present in water, thus indicating that these tadpole species are able to discriminate predator-specific scents and consequently respond to the predation risk assessed.

In contrast, B. calamita tadpoles seemed unable to discriminate chemical cues released by predators in water, or, at least, the presence of such cues did not affect their predation risk assessment, as tadpoles did not show any significant variation in their swimming activity between treatments. However, several studies have shown that Bufo species reduce activity when they are exposed to predators that were fed with conspecifics (Skelly and Werner 1990; Semlitsch and Gavasso1992; Anholt et al. 1996; Kiesecker et al. 1996; Summey and Mathis 1998). It is possible that the simple presence of predator scents may have a less important role in the chemical detection of predators by bufonid tadpoles compared with the presence of additional cues provided by predators that have eaten conspecifics tadpoles. In this regard, Marquis et al. (2004) found a slight but non-significant reduction in swimming behavior of the common toad (Bufo bufo) in presence of chemical cues from starved sympatric predators, while swimming activity of these tadpoles significantly decreased in response to chemical cues released by crushed conspecifics. Thus, the absence of responses that we found in B. calamita might be due to that none of the experimental subjects we used to provide chemical stimuli (neither the turtles nor the non-predatory fishes) were fed with anuran tadpoles.

On the other hand, several studies have reported unpalatability of Bufo embryos and tadpoles to vertebrate predators (Heyer et al. 1975; Denton and Beebee 1991; Azevedo-Ramos and Magnusson 1999). It might be also possible that antipredatory strategies of B. calamita tadpoles mainly rely on the defensive value of producing substances aimed at distastefulness. Also, Gomez-Mestre and Keller (2003) suggested that Iberian turtles are generally keener on large tadpoles (as for example P. cultripes), which are easier to see when they move, and represent a higher energy reward per unit of effort. In this way, small B. calamita tadpoles might have experienced a slighter selective pressure in the development of mechanisms to detect specific turtle cues, what might also contribute to explain the absence of specific antipredatory responses found in our experiment.

Our results further suggest that native Iberian anuran tadpoles of H. arborea, P. perezi and P. cultripes are capable to discriminate semiochemicals released in water by native predatory turtles, but they are not able to detect chemical cues released by exotic turtle predators when no previous contact has taken place. Tadpoles of these three species significantly reduced their

 

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swimming activity when chemical stimuli from native turtles were present in water. In contrast, their activity levels remained invariable when chemical cues belonged to exotic turtles, suggesting that these tadpole species are capable of facing potential predatory events posed by native predatory turtles, by responding with accurate antipredatory tactics, but they are not able to appropriately respond to introduced turtle predators. Moreover, the presence of a neutral chemical cue (from the non-predatory fish) neither elicited an antipredatory response in any of the tadpole species, thus indicating that reduction of activity only occurred when tadpoles perceived a predatory threat. Such situation was solely induced by the native turtle scents. As a consequence, the failed ability of naïve tadpoles to discriminate chemical cues from unknown turtle predators might represent a competitive advantage for introduced turtles over native ones in the Iberian Peninsula. Once released from being chemosensory detected by prey anuran tadpoles, alien turtles may easily capture and incorporate tadpoles to their diet, in detriment of native turtles, which must still face an effortful hunting. Thus, the interaction between native prey anuran tadpoles and introduced predatory turtles, which do not share an evolutionary history, could result in a positive outcome for the alien predators. A few studies report similar results for interactions between native amphibian prey and introduced predators that benefit from evolutionary releases. For example, naïve red-legged frog, Rana aurora, tadpoles cannot recognize introduced American bullfrog, Rana catesbeiana, as a potential predator, which benefits from prey innocence (Kiesecker and Blaustein 1997). Also, chemical cues from starved crawfish Astacus leptodactylus, a recently introduced predator, produce no change at all in behavior of B. bufo tadpoles (Marquis et al. 2004).

However, the initial competitive advantage that naïve native tadpoles may confer to introduced predatory turtles might vanish if native tadpole species, given enough time, learn or evolve mechanisms to cope with their introduced predators. There are some documented cases on this subject. Chivers and Smith (1995) describe how predator-avoidance behavior propagated through a naïve population of fish in less than two weeks after the introduction of a novel predator. In amphibians, Kiesecker and Blaustein (1997) state that R. aurora individuals are able to acquire the ability to recognize chemical cues of their new predator R. catesbeiana and exhibit predator avoidance behavior. Also, juvenile Pacific treefrogs (Hyla regilla) from a syntopic population with introduced R. catesbeiana showed a strong avoidance of chemical cues from this novel predator (Chivers et al. 2001). Recently, Bosch et al. (2006) found that Rana iberica tadpoles reacted to chemical cues from both native and exotic trout species by decreasing their activity, although the response toward native predators was stronger than the response toward exotic trout. Learned predator

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recognition can also occur in P. perezi tadpoles, when naïve tadpole individuals are exposed to chemical cues from exotic turtle predators jointly with alarm cues released by injured conspecifics tadpoles (A. Gonzalo, unpubl. data).

Some authors have suggested that prey might innately respond to chemical cues released by novel predators that remind them to those released by native ones (Ferrari et al. 2007). Although this strategy may work in other species, the results of our study suggest that Iberian anuran tadpoles are incapable of relating scents from native turtle predators with those from introduced ones, and thus, innately respond to the latter. Nevertheless, H. arborea tadpoles showed a minor tendency to reduce their swimming activity when chemical cues from the exotic turtle G. pseudogeographica were present in water. This behavior might be due to a vague resemblance between exotic and native predators’ cues. However, most of the studies aimed to test generalization of predator recognition in aquatic vertebrates have obtained unsuccessful results (Chivers and Smith 1994; Darwish et al. 2005), and it points out that generalization behavior broadly fails with distantly related predators. Although the native E. orbicularis and the two introduced turtles, T. scripta and G. pseudogeographica, all belong to the family Emydidae, it might seem a too long genetic distance to allow effective chemical generalization of predator recognition by Iberian tadpoles.

Additionally, the results of our study indicate that P. perezi and P. cultripes tadpoles innately respond to the scent of the two native predatory turtle species E. orbicularis and M. leprosa, as no previous contact occurred between prey tadpoles and predators’ cues before the experiment. In contrast, our study can not clarify whether H. arborea responses to chemical cues from native turtles come from innate or learned predator recognition, as H. arborea tadpoles came from a syntopic population with the two native turtle predators. On the other hand, although there were no significant differences in swimming behavior of H. arborea, P. perezi and P. cultripes tadpoles when the scents present in water belonged to E. orbicularis or M. leprosa, we observed a slight tendency of P. perezi and P. cultripes tadpoles to reduce more their activity in presence of chemical cues from E. orbicularis than from M. leprosa. This tendency was more striking for P. cultripes tadpoles, which did not show a significant response to M. leprosa cues. It might be possible that, for native Iberian tadpoles, assessment of predation risk posed by the predatory turtle E. orbicularis was greater than the one posed by M. leprosa, as tadpole consumption rates are significantly higher for the mainly carnivorous E. orbicularis than for M. leprosa (Gomez-Mestre and Keller 2003).

In conclusion, the evolved or learned chemical recognition of native predatory turtles that native anuran tadpoles of H. arborea, P. perezi and P. cultripes species show, and their failure in innate discrimination of chemicals

 

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from introduced turtle predators, may represent a competitive advantage for invasive turtles over native ones in the Iberian Peninsula. However, the magnitude of the negative outcome that this interaction between naïve prey and novel competitive predators may have on native populations of Iberian turtles, E. orbicularis and M. leprosa, remains uncertain, as abilities of amphibian prey to develop learned recognition of novel predators are widely known. Nevertheless, invasive predatory turtle species will still benefiting from inaccurate antipredatory behavior of naïve tadpoles prey, in detriment of native turtles. Thus, the advantage of competitive alien predators may explain why invasive species sometimes prosper in their new habitats better than native adapted species. Our study yield interesting data and points out new perspectives for conservation research in the framework of biological invasions. Future investigations on competitive predation may reveal why certain species are more likely to successfully invade than others. Acknowledgements We thank A. Marzal for allowing us to work in his dehesa state (“La Asesera”), the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing exotic turtles, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and by MEC-FPU grants to N.P.-C. and A.G. The experiments comply with the current laws of Spain and the Environmental Agencies of the “Junta de Extremadura” and “Comunidad de Madrid” where they were performed. REFERENCES Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of

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Capítulo 1 RECONOCIMIENTO QUÍMICO

e encontraron diferencias significativas entre los periodos reproductivo y no reproductivo en el porcentaje de tiempo que Trachemys scripta ocupó acuarios con estímulos químicos propios y de coespecíficos vs. acuarios

con agua limpia (Fig. 1.1)1. Durante el periodo reproductivo, T. scripta permaneció durante un porcentaje de tiempo menor en acuarios que contenían estímulos químicos (media ± EE = 38 ± 3 %) que durante el periodo no reproductivo (49 ± 3 %), lo que sugiere que esta especie es capaz de reconocer sustancias químicas de coespecíficos disueltas en el agua. Los galápagos americanos podrían evitar así potenciales encuentros agresivos con otros individuos de su especie durante la época reproductiva. Sin embargo, al contrario que los galápagos leprosos (Muñoz 2004), los galápagos de Florida no discriminaron claramente entre sus propias secreciones y las pertenecientes a machos y hembras coespecíficos (Fig. 1.1), lo que parece indicar que los galápagos exóticos son menos dependientes de la comunicación química que los galápagos nativos. Así mismo, T. scripta no prefirió ni evitó los acuarios con estímulos químicos secretados por Mauremys leprosa (Fig. 1.2; Tabla 1.1). Esta ausencia de respuesta podría deberse a la incapacidad para detectar sustancias químicas de individuos heteroespecíficos, o simplemente a que estas sustancias, aunque puedan ser reconocidas, no suponen una amenaza para la especie invasora. En contraste, M. leprosa prefirió agua con secreciones de coespecíficos y evitó los acuarios con estímulos secretados por T. scripta (Fig. 1.2), lo que sugiere que estas señales químicas podrían ser usadas por los galápagos nativos para evitar áreas ocupadas por los galápagos exóticos.

En muchas especies de animales, la habilidad para reconocer olores de individuos heteroespecíficos contribuye a evitar depredadores o a reducir los costes de las interacciones agresivas con especies competidoras (Dodson et al. 1994; Kats y Dill 1998). Por otra parte, numerosas especies son capaces de aprender a reconocer olores nuevos como peligrosos cuando éstos son

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1Las tablas y figuras se muestran en el apartado de resultados en cada uno de los capítulos

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detectados simultáneamente con indicadores de riesgo conocidos, como por ejemplo el comportamiento antidepredatorio, o la presencia en el medio de sustancias químicas de alarma, de coespecíficos (e.g., Magurran 1989; Mathis et al. 1996; Chivers y Smith 1998). De forma similar, las especies nativas podrían aprender a evitar olores de especies invasoras que hayan sido previamente asociados con un comportamiento agonístico o con un aprovechamiento ineficiente de los recursos. Así, en una situación de desventaja competitiva por los lugares de asoleamiento o el alimento (Cadi y Joly 2003; Polo-Cavia et al. en prensa; capítulo 2), la aversión de M. leprosa por los estímulos químicos secretados por T. scripta podría constituir un mecanismo para evitar encuentros agresivos con la especie introducida, lo que favorecería la expansión del galápago de Florida.

Capítulo 2 INTERACCIONES AGRESIVAS DURANTE LA ALIMENTACIÓN

os resultados de este trabajo muestran diferencias significativas entre el galápago de Florida y el galápago leproso en la ingesta de alimento en condiciones de competencia intra e interespecífica. La cantidad de

alimento ingerida por M. leprosa y T. scripta fue similar cuando compitieron con coespecíficos, pero cuando estas dos especies compitieron entre sí, el acceso de M. leprosa al alimento fue restringido por T. scripta, que ingirió un porcentaje significativamente mayor de la comida suministrada (Fig. 2.1). Estos resultados indican que la competencia por el alimento entre estas dos especies de galápagos es asimétrica.

Las habilidades competitivas difieren habitualmente entre individuos en la naturaleza (Holmgren 1995; Moody y Houston 1995; Spencer et al. 1995). En consecuencia, algunos individuos son capaces de excluir a otros menos competitivos utilizando la agresividad (Schoener 1983). De las 27 agresiones observadas durante la competencia por el acceso a la comida, tan sólo 5 fueron cometidas por M. leprosa, 2 de ellas sobre individuos coespecíficos y 3 sobre galápagos americanos. T. scripta, en cambio, agredió en 5 ocasiones a individuos coespecíficos y 19 veces a galápagos leprosos. Estos resultados indican que T. scripta es una especie más agresiva que M. leprosa y que las interacciones agresivas se producen con mayor frecuencia entre individuos heteroespecíficos (Tabla 2.2). Además, se observó una correlación positiva entre el porcentaje de alimento ingerido por los galápagos nativos en condiciones de competencia interespecífica y el nivel de agresividad recibido, lo que sugiere la existencia de una relación de compromiso entre la eficiencia alimenticia de M. leprosa y

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los costes de la competencia agresiva con los galápagos exóticos. En las poblaciones simpátridas naturales, la mayor agresividad y dominancia de T. scripta podrían traducirse en el desplazamiento de M. leprosa hacia áreas subóptimas de alimentación. Esta exclusión de los galápagos leprosos de los recursos tróficos preferidos podría finalmente afectar negativamente a sus tasas de crecimiento y reproducción (Moll 1976; Bury 1979; Gibbons et al 1979; Vogt y Guzman 1988), contribuyendo a la recesión actual que sufre la especie.

Capítulo 3 COMPETENCIA DURANTE EL ASOLEAMIENTO

n condiciones de competencia ocasional, el porcentaje de tiempo que los galápagos leprosos dedicaron a asolearse fue significativamente menor cuando el competidor fue un galápago de Florida que cuando fue un

coespecífico (Fig. 3.1a). Cuando la competencia fue a largo plazo, se encontraron diferencias significativas entre la especie nativa y la invasora, dependiendo del tipo de competencia (i.e., intra vs. interespecífica), en el tiempo total de asoleamiento y en la duración media de los periodos dedicados a esta actividad. El tiempo total de asoleamiento fue similar entre las dos especies en condiciones de competencia intraespecífica (Fig. 3.1b), y también la duración media de los periodos de asoleamiento (M. leprosa: 71 ± 15 min; T. scripta: media ± EE = 76 ± 14 min), pero en condiciones de competencia interespecífica, tanto el tiempo total de asoleamiento (Fig. 3.1b) como la duración media de los periodos dedicados a esta actividad (M. leprosa: 45 ± 14 min; T. scripta: 121 ± 19 min) fueron significativamente mayores en el caso de la especie invasora. Los resultados anteriores indican que, cuando las dos especies compiten entre sí por los lugares de asoleamiento, el galápago de Florida es más eficiente en la ocupación de los recursos que el galápago leproso, lo que sugiere la dominancia de la especie invasora sobre la nativa. Factores tales como un mayor tamaño corporal o un hábitat original con niveles elevados de competencia (i.e., T. scripta coexiste con un gran número de especies competidoras de galápagos en su hábitat natural, en comparación con M. leprosa) podrían favorecer la mayor habilidad competitiva del galápago de Florida.

Por otra parte, los galápagos leprosos evitaron compartir los recursos de asoleamiento con galápagos americanos, pero no con individuos coespecíficos (Fig. 3.5). Este comportamiento de M. leprosa coincide con el descrito para el galápago europeo (Emys orbicularis). En sus experimentos, Cadi y Joly (2003) observaron que E. orbicularis evitaba los solarios ocupados por el introducido T.

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scripta, siendo desplazado hacia lugares subóptimos para el asoleamiento (i.e., orillas y aguas someras con mayor riesgo de depredación, López et al. 2005; Polo-Cavia et al. 2008). De forma similar, es posible que los galápagos leprosos en libertad se desplacen hacia las áreas menos preferidas para evitar ser extorsionados durante el asoleamiento por los galápagos exóticos. Esta ocupación deficiente de los recursos de asoleamiento por parte de M. leprosa podría suponer una pérdida de eficiencia en su comportamiento termorregulador, y el subsiguiente detrimento de las funciones fisiológicas dependientes de la termorregulación (Cagle 1950; Vogt 1979; Parmenter 1981; Avery 1982; Gianopulos y Rowe 1999; Rollinson y Brooks 2007).

Capítulo 4 DIFERENCIAS EN LAS TASAS DE INTERCAMBIO DE CALOR

l análisis de las medidas biométricas de M. leprosa y T. scripta mostró, tras corregir por las diferencias entre especies en el tamaño corporal, que la relación superficie-volumen del galápago leproso es

significativamente mayor que la del galápago de Florida. Ambas especies de galápagos difieren también en los índices de esfericidad y de aplanamiento, siendo la forma de los galápagos nativos más aplanada y la de los galápagos exóticos más esférica. Un análisis posterior no paramétrico mostró además diferencias significativas entre especies en las tasas de calentamiento y de enfriamiento (Tablas 4.1 y 4.2; Fig. 4.1), siendo la inercia térmica del galápago de Florida mayor que la del leproso, tanto en el agua como en el aire. Todas las tasas de intercambio de calor de los galápagos correlacionaron positiva y significativamente con su relación superficie-volumen.

La forma del caparazón y la relación superficie-volumen han sido previamente consideradas como factores influyentes en las tasas de calentamiento y de enfriamiento de varias especies de galápagos (Boyer 1965; Spray y May 1972; Gronke et al. 2006). Si bien no es posible descartar que determinados mecanismos fisiológicos puedan estar relacionados con las diferencias observadas en las tasas de intercambio de calor de M. leprosa y T. scripta, los resultados de este trabajo indican que las diferencias morfológicas observadas entre estas dos especies, producto de la adaptación a distintos ambientes, determinan también la existencia de diferencias interespecíficas en sus tasas de intercambio de calor. En un escenario en el que el galápago de Florida ha sido introducido en el hábitat original del galápago leproso, estas diferencias podrían influir en el resultado de la competencia entre ambas

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especies de galápagos. La mayor inercia térmica de T. scripta podría conferir ventajas competitivas a los galápagos introducidos en las regiones templadas, al facilitar la retención de calor corporal y permitir un mejor desarrollo de sus actividades (Huey y Slatkin 1976; Dunham et al. 1989).

Capítulo 5 ESTADO NUTRICIONAL Y REQUERIMIENTOS DE ASOLEAMIENTO

os resultados de este experimento indican que M. leprosa y T. scripta difieren en sus requerimientos térmicos. La temperatura preferida de asoleamiento fue significativamente mayor en la especie nativa que en la

invasora (M. leprosa: media ± EE = 31,9 ± 0,6 °C; T. scripta: 26,7 ± 0,7 °C). Esta temperatura fue mayor en ambas especies en condiciones de alimentación ad líbitum que en condiciones de ayuno prolongado (Fig. 5.1), y correlacionó positivamente con la relación superficie-volumen de los galápagos en ambos estados nutricionales. Así, los individuos con valores de relación superficie-volumen más altos mostraron también temperaturas preferidas de asoleamiento más elevadas (Fig. 5.2).

El comportamiento termorregulador permite a los ectotermos maximizar sus funciones fisiológicas, al aproximar su temperatura corporal a un óptimo térmico específico de cada especie y proceso (Huey y Slatkin 1976; Huey y Bennett 1987; Angilletta et al. 2002, 2006). Así, las diferencias potenciales en los óptimos térmicos de M. leprosa y T. scripta podrían explicar las diferencias interespecíficas observadas en las temperaturas de asoleamiento seleccionadas. Por otra parte, la correlación observada entre las temperaturas preferidas de asoleamiento de los galápagos y su relación superficie-volumen sugiere la existencia de una correspondencia entre los requerimientos térmicos de cada especie y su morfología específica. La forma esférica de T. scripta, en comparación con el perfil más aplanado de M. leprosa, confiere a la especie introducida una menor relación superficie-volumen y una mayor inercia térmica (Polo-Cavia et al. 2009), facilitando la conservación del calor corporal y el desarrollo de actividades tales como la búsqueda de alimento o la digestión. Es posible que los galápagos leprosos, con una mayor relación superficie-volumen, compensen su mayor tendencia a perder calor seleccionando temperaturas de asoleamiento superiores a las de los galápagos exóticos. Sin embargo, a consecuencia de la competencia por los recursos de asoleamiento con el galápago de Florida, los galápagos nativos pueden encontrar dificultades para asolearse (Polo-Cavia et al. en prensa), lo que podría dar lugar a efectos negativos en las tasas de ingestión y en las funciones digestivas de M. leprosa.

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Los resultados de este trabajo revelan también un claro efecto del estado nutricional en el comportamiento termorregulador de los galápagos. Ambas especies respondieron a la privación de alimento seleccionando temperaturas de asoleamiento inferiores, lo que sugiere la existencia de un mecanismo adaptativo que permita el ajuste de la temperatura corporal y del metabolismo en función de la disponibilidad de alimento (Lillywhite et al. 1973; Brown y Griffin 2005). Sin embargo, la introducción de un nuevo competidor interfiriendo en el comportamiento termorregulador de M. leprosa podría empujar a los galápagos nativos hacia una creciente depresión metabólica impulsada por los efectos retroalimentados de una actividad de asoleamiento reducida y un estado nutricional deficiente, favoreciendo así la recesión de la especie nativa.

Capítulo 6 TEMPERATURA CORPORAL Y RESPUESTA DE ‘GIRO’

os resultados de este estudio revelaron claras diferencias entre M. leprosa y T. scripta en los componentes comportamental y mecánico de la respuesta de ‘giro’. A pesar de que la duración media de la fase de

latencia (medida desde el momento en que los galápagos son depositados en el suelo con el plastrón hacia arriba hasta que inician el movimiento de ‘giro’) no difirió significativamente entre galápagos leprosos y americanos, esta fase fue independiente de la temperatura corporal en el caso de T. scripta, pero no en el caso de M. leprosa (Fig. 6.1a). Así, los galápagos leprosos experimentaron un considerable incremento en la duración de sus fases de latencia a 15 °C con respecto a 20 °C y a la temperatura preferida de asoleamiento de la especie, lo que sugiere que la percepción del riesgo durante el tiempo en que los galápagos se encuentran tendidos boca arriba se encuentra más influida por la temperatura corporal en la especie nativa que en la invasora. La duración de la fase mecánica (desde el momento en que los galápagos inician el movimiento de ‘giro’ hasta que recuperan su posición natural) se redujo de forma similar en las dos especies al incrementar la temperatura corporal de los galápagos (Fig. 6.1b), siendo significativamente menor a las temperaturas preferidas de asoleamiento respectivas de cada especie que a 15 y a 20 °C. Esto sugiere la existencia de coadaptación entre esta temperatura y la respuesta de ‘giro’ de los galápagos. Por otra parte, M. leprosa necesitó tiempos más largos que T. scripta para volver a su posición natural con independencia de la temperatura (media ± EE = 151 ± 33 s vs. 78 ± 34 s) (Fig. 6.1b), lo que indica una mayor eficiencia de los galápagos exóticos en la fase mecánica de la respuesta de ‘giro’. La forma más esférica que

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presenta T. scripta en comparación con M. leprosa (Polo-Cavia et al. 2009) podría facilitar la respuesta de ‘giro’ de los galápagos exóticos. Sin embargo, la duración de las fases mecánicas de M. leprosa y T. scripta no correlacionó significativamente con los índices de esfericidad o aplanamiento de cada una de las especies a ninguna de las temperaturas experimentales, probablemente debido al efecto de las diferencias individuales en variables que podrían ser más influyentes en la respuesta de ‘giro’ de estas dos especies de galápagos, como por ejemplo la longitud del cuello (Rivera et al. 2004; Domokos y Várkonyi 2008).

La capacidad de los galápagos para recuperar su posición natural tras resultar volteados accidentalmente, o al ser atacados por un depredador, puede determinar críticamente su supervivencia (Burger 1976; Finkler 1999; Steyermark y Spotila 2001; Martín et al. 2005). En consecuencia, el incremento de tiempo que M. leprosa experimenta a bajas temperaturas en la duración de las fases de latencia y mecánica de su respuesta de ‘giro’ podría comprometer la supervivencia de los galápagos nativos. En contraste, T. scripta posee una respuesta mecánica más eficiente, a la vez que su mayor competitividad por los recursos de asoleamiento (Polo-Cavia et al. en prensa) y su mayor inercia térmica (Polo-Cavia et al. 2009) facilitan el mantenimiento de temperaturas corporales favorables a la respuesta de ‘giro’, lo que en suma podría contribuir a la expansión de los galápagos exóticos.

Capítulo 7 COMPORTAMIENTO ANTIDEPREDATORIO

os resultados de este experimento indican que ambas especies de galápagos son capaces de ajustar el tiempo que permanecen refugiadas en el caparazón tras el ataque de un depredador, decidiendo el momento

más oportuno para escapar activamente en función de la intensidad del ataque, la persistencia del depredador, el microhábitat y los costes de mantenerse escondidos en el interior del caparazón. Sin embargo, los galápagos nativos y los exóticos respondieron de forma diferente al efecto combinado de estos factores de riesgo. El tiempo medio de aparición (medido desde que los galápagos son depositados en el suelo tras la simulación del ataque hasta que la cabeza y los ojos emergen del caparazón) y de espera (desde que los galápagos emergen del caparazón hasta que inician el movimiento y el escape activo) fueron más largos en el caso de T. scripta (tiempo de aparición: media ± EE = 19 ± 5 s; tiempo de espera: 174 ± 27 s) que en el caso de M. leprosa (tiempo de aparición: 5 ± 6 s;

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tiempo de espera: 93 ± 30 s). Cuando se encontraban en tierra, ambas especies de galápagos emergieron antes del caparazón cuando el ataque del depredador fue de menor intensidad, y por tanto, menor el nivel de riesgo percibido por los galápagos, pero en el agua, tanto M. leprosa como T. scripta emergieron rápidamente con independencia del nivel de riesgo (Fig. 7.1; Tabla 7.1). Es posible que los galápagos decidan escapar hacia aguas más profundas y seguras cuando son atacados en aguas someras, en lugar de tratar de disuadir al depredador permaneciendo más tiempo escondidos en el interior del caparazón. Los tiempos de espera de T. scripta no se vieron afectados por el nivel de riesgo percibido, pero sí por el microhábitat, siendo más largos en tierra que en agua (Fig. 7.2; Tabla 7.1). En contraste, la duración de los tiempos de espera de M. leprosa fue independiente del nivel de riesgo percibido en tierra, pero en el agua los galápagos nativos iniciaron antes la huida cuando la intensidad del ataque fue mayor. La persistencia del depredador no afectó significativamente a los tiempos de aparición de ninguna de las dos especies (Fig. 7.1; Tabla 7.1), lo que sugiere que los galápagos no tienen información de la posición del depredador mientras se encuentran escondidos en el interior del caparazón (Martín et al. 2005). La persistencia tampoco influyó en los tiempos de espera de los galápagos introducidos, con independencia del microhábitat. Sin embargo, los tiempos de espera de M. leprosa en tierra fueron significativamente más largos cuando el “depredador” permaneció junto a los galápagos, pero el efecto de este factor no fue significativo en el agua, cuando los galápagos podían escapar hacia un refugio seguro.

Estas diferencias interespecíficas podrían deberse a los distintos tipos de depredadores (terrestres vs. acuáticos) que M. leprosa y T. scripta enfrentan en sus hábitats originales. Mientras que los galápagos leprosos tenderían a escapar rápidamente hacia el agua ante la amenaza de un depredador (López et al. 2005), un galápago de Florida que se estuviera asoleando en tierra en su hábitat original permanecería refugiado en el interior de su caparazón por más tiempo antes de iniciar la huida hacia el agua, donde podría encontrarse con depredadores más peligrosos, como caimanes o cocodrilos (Lima 1992; McIntosh y Peckarsky 1999; Bouwma y Hazlett 2001). Sin embargo, la funcionalidad de las estrategias antidepredatorias de M. leprosa y T. scripta, adaptadas a sus respectivos hábitats naturales, podría verse alterada en hábitats modificados antropogénicamente, donde la presencia de depredadores es reducida. En estos ambientes, T. scripta podría evitar los costes potenciales de repetidas e innecesarias huidas hacia el agua (e.g., la interrupción de actividades como el asoleamiento) provocados por la presencia humana (la cual representa un riesgo bajo de depredación), lo que podría conferir una ventaja competitiva a los galápagos exóticos sobre los nativos. Así pues, las diferencias interespecíficas en el comportamiento antidepredatorio de M. leprosa y T. scripta podrían en parte explicar la mayor

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habilidad competitiva del galápago de Florida en hábitats con alteraciones antrópicas. Estos resultados proporcionan un interesante marco para próximos estudios que investiguen el impacto de la conservación de los ecosistemas en el éxito de las invasiones.

Capítulo 8 RECONOCIMIENTO DE GALÁPAGOS INTRODUCIDOS POR RENACUAJOS PRESA

res de las cuatro especies de larvas de anuros estudiadas (Hyla arborea, Pelophylax perezi y Pelobates cultripes) respondieron a los estímulos químicos de galápagos depredadores disueltos en el agua modificando

sus niveles de actividad natatoria (Fig. 8.1a, b y c). Los niveles de actividad de los renacuajos de Bufo calamita, en cambio, permanecieron invariables entre tratamientos con agua limpia y con los diferentes estímulos químicos (Fig. 8.1d), lo que sugiere que esta especie es incapaz de discriminar las sustancias químicas de potenciales depredadores, o al menos, que la presencia de estas sustancias en el agua no influye en la percepción de riesgo de los renacuajos de esta especie. Estudios previos han demostrado que diversas especies de Bufo requieren de la presencia en el agua de sustancias de alarma de coespecíficos, o de estímulos químicos pertenecientes a depredadores previamente alimentados con individuos coespecíficos, para desencadenar una respuesta antidepredatoria (Semlitsch y Gavasso1992; Summey y Mathis 1998; Marquis et al. 2004).

Los renacuajos de H. arborea, P. perezi y P. cultripes redujeron su actividad, con respecto a la que mostraron en agua limpia, en agua con secreciones de galápagos nativos, pero no en agua con secreciones de galápagos exóticos (Fig. 8.1a, b y c). La presencia de un estímulo químico neutro (perteneciente a un pez exótico no depredador) tampoco desencadenó una respuesta antidepredatoria en ninguna de estas tres especies de anuros, confirmando que la reducción observada experimentalmente en la actividad natatoria de los renacuajos responde a la percepción de una amenaza depredatoria. Estos resultados indican que los renacuajos de estas tres especies de anfibios ibéricos son capaces de responder a los estímulos químicos de galápagos depredadores nativos empleando estrategias antidepredatorias adecuadas, pero que no son capaces de reconocer olores de galápagos depredadores introducidos con los que no comparten una historia evolutiva ni han tenido un contacto previo. En consecuencia, los galápagos exóticos podrían capturar más fácilmente renacuajos nativos e incluirlos en su dieta, en detrimento de los galápagos ibéricos. Esta trampa evolutiva (Schlaepfer et al. 2005) podría contribuir al desplazamiento de las poblaciones de galápagos nativos por los galápagos exóticos invasores. No

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obstante, los renacuajos ibéricos podrían adquirir mecanismos, por evolución o aprendizaje, que les permitieran reconocer a los nuevos depredadores (Chivers y Smith 1995; Kiesecker y Blaustein 1997; Bosch et al. 2006), reduciendo así el impacto de la interacción entre las presas nativas y los galápagos depredadores introducidos sobre las especies nativas de galápagos.

* * * Los resultados de los experimentos planteados en esta tesis sugieren la

mayor habilidad competitiva del introducido galápago de Florida, Trachemys scripta, en la competencia por los recursos con el galápago leproso, Mauremys leprosa. Los galápagos nativos utilizan presumiblemente las señales químicas disueltas en el agua para discriminar entre individuos coespecíficos y heteroespecíficos y evitar así los costes de las interacciones con los galápagos exóticos, abandonando recursos o desplazándose hacia áreas alternativas menos favorables. La expansión del galápago de Florida podría además verse favorecida por la ausencia de respuestas quimiosensoriales hacia los galápagos nativos. Esta alteración en el uso del espacio por M. leprosa en presencia de T. scripta parece responder al efecto negativo de la competencia directa con la especie invasora por el aprovechamiento de recursos fundamentales como el alimento o los lugares de asoleamiento. Los resultados sugieren que la mayor agresividad de los galápagos exóticos y su dominancia sobre los nativos suponen el desplazamiento de M. leprosa hacia recursos subóptimos, y por consiguiente, un detrimento en el estado nutricional y en el comportamiento termorregulador de los galápagos autóctonos.

Además, las características propias de cada especie, resultantes de la adaptación a diferentes ambientes, podrían conferir ventajas competitivas a los galápagos exóticos en los nuevos hábitats en los que han sido introducidos, favoreciendo a la especie invasora en el proceso de competencia con los galápagos nativos. Así, por ejemplo, la forma más esférica de T. scripta le confiere una menor relación superficie-volumen y una mayor inercia térmica que facilita la retención de calor corporal y favorece el desarrollo de actividades y funciones fisiológicas tales como la búsqueda de alimento o la digestión. En contraste, la mayor tendencia a perder calor de M. leprosa, sumada a la introducción de un competidor que interfiere en su comportamiento de termorregulación, podría ocasionar una reducción en la actividad locomotora, en las tasas de ingestión y/o en la eficacia de la digestión de los galápagos nativos. Puesto que un estado nutricional deficiente conlleva temperaturas

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preferidas de asoleamiento más bajas en ambas especies de galápagos, las interferencias de T. scripta en la alimentación y en el comportamiento de asoleamiento de M. leprosa podrían dar lugar a complicados feed-backs y alteraciones negativas en el metabolismo de los galápagos nativos. Por otra parte, la eficiencia en el comportamiento de ‘giro’ de ambas especies de galápagos se encuentra también fuertemente influida por la temperatura. Este comportamiento puede ser crítico para la supervivencia de los galápagos, ya que cuando éstos se encuentran tendidos con el plastrón hacia arriba pueden experimentar diferentes tipos de riesgo (i.e., deshidratación, depredación, dificultades respiratorias, etc.). En consecuencia, aquellos individuos que sean capaces de alcanzar y mantener temperaturas corporales óptimas incrementarán sus posibilidades de supervivencia. De este modo, la mayor inercia térmica de T. scripta y su mayor competitividad por los lugares de asoleamiento podrían también favorecer su supervivencia, en tanto que facilitan su respuesta de ‘giro’, ya de por sí más eficiente que la de los galápagos nativos. La mayor inercia térmica del galápago de Florida reduce además el riesgo de sobrecalentamiento en condiciones en las que los galápagos no pueden controlar su temperatura por medio de la termorregulación (por ejemplo, si son atacados por un depredador).

Tanto el galápago leproso como el de Florida tienden a refugiarse en el interior del caparazón tras el ataque de un depredador, ajustando el tiempo que pasan escondidos en función de factores de riesgo tales como el grado de amenaza, la persistencia del depredador, las posibilidades de escape hacia un refugio más seguro y los costes de mantenerse escondidos en el interior del caparazón (e.g., riesgo de deshidratación, interrupción de actividades como el asoleamiento, la búsqueda de alimento o potenciales parejas, etc.). En estos casos, la forma más esférica de T. scripta reduce el riesgo de depredación, pues dificulta la captura de los galápagos por mamíferos o aves. Por otra parte, los galápagos introducidos tienden a esperar escondidos más tiempo dentro el caparazón mientras que los leprosos intentan escapar rápidamente hacia el agua (probablemente debido a las distintas presiones depredatorias que soportan M. leprosa y T. scripta en sus hábitats originales). Estas diferencias interespecíficas en el comportamiento antidepredatorio de los galápagos podrían conferir ventajas competitivas a la especie introducida en ambientes con modificaciones antrópicas donde el riesgo de depredación es escaso, y los galápagos nativos podrían sufrir los costes de repetidas e innecesarias huidas provocadas por la presencia humana. La alteración del hábitat puede ocasionar desajustes en las estrategias antidepredatorias de los galápagos, pero puede también afectar a la propia depredación de los galápagos nativos, al introducir una especie competidora que constituya una trampa evolutiva para sus presas. Éste es el caso de varias especies de renacuajos de anuros ibéricos, incapaces de reconocer de forma innata a los depredadores introducidos con los que no han coexistido en

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el pasado. En consecuencia, las especies exóticas de galápagos poseen una ventaja sobre las nativas, en tanto que pueden capturar renacuajos ibéricos con mayor facilidad.

En síntesis, las diferencias interespecíficas observadas en los distintos aspectos estudiados de la morfología, ecología y comportamiento del galápago leproso y del galápago de Florida, apoyan la existencia de una mayor habilidad competitiva por parte de la especie introducida. Esta asimetría, producto de la adaptación de M. leprosa y T. scripta a sus respectivos hábitats naturales, parece conferir ventajas a los galápagos exóticos en la competencia por los recursos con los galápagos nativos, favoreciendo el desplazamiento de M. leprosa hacia áreas subóptimas y facilitando así la expansión del galápago de Florida en los nuevos ambientes en los que ha sido introducido, en detrimento de las poblaciones nativas de galápago leproso.

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Ilustración | Dos galápagos leprosos aprovechan las primeras horas de luz sobre unas rocas

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— CONCLUSIONES —

1. El galápago leproso podría utilizar las señales químicas del galápago de Florida para evitar los costes de las interacciones agresivas durante la competencia por los recursos con esta especie introducida, lo que conduciría al progresivo desplazamiento de los galápagos nativos hacia áreas subóptimas ■

2. La mayor agresividad del galápago de Florida y su dominancia sobre el

galápago leproso durante la competencia por los recursos tróficos podrían dar lugar a la exclusión competitiva de los galápagos autóctonos y al consiguiente detrimento en su estado nutricional ■

3. La pérdida de eficiencia observada en la actividad de asoleamiento del

galápago leproso en condiciones de competencia con el galápago de Florida sugiere la existencia de superimposición y desplazamiento de los galápagos nativos de los lugares óptimos para el asoleamiento en presencia de los galápagos exóticos ■

4. La forma más esférica que presenta el galápago de Florida en comparación con el galápago leproso, su menor relación superficie-volumen y su mayor inercia térmica, facilitan la retención de calor corporal, pudiendo conferir ventajas competitivas a la especie introducida en los ecosistemas templados ■

5. Las interferencias del galápago de Florida en la actividad de asoleamiento de

los galápagos leprosos y su mayor capacidad para retener el calor corporal podrían en conjunto conferir ventajas termorreguladoras a la especie invasora ■

6. La relación entre el comportamiento termorregulador de los galápagos y su

estado nutricional podría ser la base de complejos efectos negativos inducidos en el metabolismo de los galápagos leprosos a consecuencia de la competencia con el galápago de Florida por el alimento y los recursos de asoleamiento ■

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7. La mayor capacidad de los galápagos exóticos para recuperar su posición natural tras resultar volteados minimiza el tiempo que permanecen expuestos a diversos peligros (e.g., deshidratación o depredación), favoreciendo su supervivencia. Además, la mayor inercia térmica del galápago de Florida y su mayor competitividad por los lugares de asoleamiento incrementan la eficiencia de la respuesta de ‘giro’ de los galápagos introducidos ■

8. Tanto los galápagos nativos como los exóticos ajustan el tiempo que

permanecen escondidos en el interior del caparazón tras el ataque de un depredador, en función de factores de riesgo tales como la intensidad del ataque, la persistencia del depredador, las posibilidades de escape hacia un refugio más seguro y los costes de mantenerse escondidos en el caparazón ■

9. En ambientes con modificaciones antrópicas en los que la presencia de

depredadores es escasa, la estrategia antidepredatoria del galápago leproso de escapar rápidamente hacia el agua ante la menor señal de peligro podría dar lugar a la interrupción de actividades como el asoleamiento o la búsqueda del alimento, facilitando al galápago de Florida la monopolización de los recursos ■

10. La incapacidad de algunas especies de renacuajos de anuros ibéricos para

detectar y responder de forma innata a los estímulos químicos de los galápagos depredadores introducidos confiere ventajas depredatorias a estas especies invasoras de galápagos, al menos hasta que los renacuajos adquieren mecanismos, por evolución o aprendizaje, que les permiten reconocer a los nuevos depredadores ■

11. Las asimetrías observadas en la morfología, ecología y comportamiento de

los galápagos nativos y exóticos, consecuencia de la adaptación a sus diferentes hábitats naturales, parecen favorecer la expansión del galápago de Florida en los nuevos ambientes en los que ha sido introducido, contribuyendo a la recesión del galápago leproso ■

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— REFERENCIAS —

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— ANEXO —

LISTADO DE LAS 100 ESPECIES INVASORAS MÁS DAÑINAS DE EUROPA Fuente: DAISIE-project, disponible online en: www.europe-aliens.org/speciesTheWorst.do

MARINAS Alexandrium catenella Dinophyta

Balanus improvisus Crustacea

Bonnemaisonia hamifera Rhodophyta

Brachidontes pharaonis Mollusca

Caulerpa racemosa Chlorophyta

Caulerpa taxifolia Chlorophyta

Chattonella cf. Other algae

Codium fragile Chlorophyta

Coscinodiscus wailesii Other algae

Crassostrea gigas Mollusca

Crepidula fornicata Mollusca

Ensis americanus Mollusca

Ficopomatus enigmaticus Annelida

Fistularia commersonii Osteichthyes

Halophila stipulacea Magnoliophyta

Marenzelleria neglecta Annelida

Marsupenaeus japonicus Crustacea

Musculista senhousia Mollusca

Odontella sinensis Other algae

Paralithodes camtschaticus Crustacea

Percnon gibbesi Crustacea

Pinctada radiata Mollusca

Portunus pelagicus Crustacea

Rapana venosa Mollusca

Rhopilema nomadica Cnidaria

 

200

Saurida undosquamis Osteichthyes

Siganus rivulatus Osteichthyes

Spartina anglica Magnoliophyta

Styela clava Tunicata

Teredo navalis Mollusca

Tricellaria inopinata Ectoprocta

Undaria pinnatifida Chromista

DULCEACUÍCOLAS

Anguillicola crassus Nematoda

Aphanomyces astaci Chromista

Cercopagis pengoi Crustacea

Corbicula fluminea Mollusca

Cordylophora caspia Cnidaria

Crassula helmsii Magnoliophyta

Dikerogammarus villosus Crustacea

Dreissena polymorpha Mollusca

Elodea canadensis Magnoliophyta

Eriocheir sinensis Crustacea

Gyrodactylus salaris Platyhelminthes

Mnemiopsis leidyi Ectoprocta

Neogobius melanostomus Osteichthyes

Procambarus clarkii Crustacea

Pseudorasbora parva Osteichthyes

Salvelinus fontinalis Osteichthyes

HONGOS TERRESTRES

Ophiostoma novo-ulmi Fungi

Phytophthora cinnamomi Chromista

Seiridium cardinale Fungi

INVERTEBRADOS TERRESTRES

Aedes albopictus Insecta

Anoplophora chinensis Insecta

Anoplophora glabripennis Insecta

Aphis gossypii Insecta

Arion vulgaris Mollusca

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Bemisia tabaci Insecta

Bursaphelenchus xylophilus Nematoda

Cameraria ohridella Insecta

Ceratitis capitata Insecta

Diabrotica virgifera Insecta

Frankliniella occidentalis Insecta

Harmonia axyridis Insecta

Leptinotarsa decemlineata Insecta

Linepithema humile Insecta

Liriomyza huidobrensis Insecta

Spodoptera littoralis Insecta PLANTAS TERRESTRES Acacia dealbata Magnoliophyta

Ailanthus altissima Magnoliophyta

Ambrosia artemisiifolia Magnoliophyta

Campylopus introflexus Bryophyta

Carpobrotus edulis Magnoliophyta

Cortaderia selloana Magnoliophyta

Echinocystis lobata Magnoliophyta

Fallopia japonica Magnoliophyta

Hedychium gardnerianum Magnoliophyta

Heracleum mantegazzianum Magnoliophyta

Impatiens glandulifera Magnoliophyta

Opuntia ficus-indica Magnoliophyta

Oxalis pes-caprae Magnoliophyta

Paspalum paspaloides Magnoliophyta

Prunus serotina Magnoliophyta

Rhododendron ponticum Magnoliophyta

Robinia pseudoacacia Magnoliophyta

Rosa rugosa Magnoliophyta VERTEBRADOS TERRESTRES Branta canadensis Aves

Cervus nippon Mammalia

Lithobates catesbeianus Amphibia

 

202

Mustela vison Mammalia

Myocastor coypus Mammalia

Nyctereutes procyonoides Mammalia

Ondatra zibethicus Mammalia

Oxyura jamaicensis Aves

Procyon lotor Mammalia

Psittacula krameri Aves

Rattus norvegicus Mammalia

Sciurus carolinensis Mammalia

Tamias sibiricus Mammalia

Threskiornis aethiopicus Aves

Trachemys scripta Reptilia

 

 

a i n t r o d u c c i ó n d e s e r e s v i v o s f u e r a d e s u á r e a d e d i s t r i b u c i ó n n a t u r a l s e p r o d u c e c a d a v e z c o n m a y o r i n t e n s i d a d , d a n d o l u g a r a f e n ó m e n o s d e

i n v a s i ó n , c o m p e t e n c i a y d e s p l a z a m i e n t o d e l o s o r g a n i s m o s n a t i v o s d e s u s n i c h o s e c o l ó g i c o s . E n l a p r e s e n t e t e s i s s e a b o r d a n d i v e r s o s a s p e c t o s d e l a b i o l o g í a , e c o l o g í a y c o m p o r t a m i e n t o d e l g a l á p a g o i b é r i c o M a u r e m y s l e p r o s a , y d e l i n t r o d u c i d o g a l á p a g o d e F l o r i d a , T r a c h e m y s s c r i p t a , q u e p u e d a n a p o r t a r i n f o r m a c i ó n a c e r c a d e c ó m o s e e s t á n p r o d u c i e n d o l a s i n t e r a c c i o n e s c o m p e t i t i v a s e n t r e l a e s p e c i e n a t i v a y l a i n v a s o r a .

L

Departamento de Ecología Evolutiva Museo Nacional de Ciencias Naturales

Consejo Superior de Investigaciones Científicas

Departamento de Biología Facultad de Ciencias

Universidad Autónoma de Madrid