emoria presentada por pelayo acevedo...
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ECOGEOGRAFÍA DE LA CABRA MONTÉS (CAPRA PYRENAICA): RELACIÓN CON OTROS UNGULADOS EN SIMPATRÍA EN EL
CENTRO-SUR DE LA PENÍNSULA IBÉRICA
MEMORIA PRESENTADA POR
Pelayo Acevedo Lavandera PARA OPTAR AL GRADO DE DOCTOR
VºBº LOS DIRECTORES
DR. CHRISTIAN GORTÁZAR DR. JORGE CASSINELLO DR. JOAQUÍN VICENTE
UNIVERSIDAD DE CASTILLA-LA MANCHA
INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS
(CSIC – UCLM – JCCM)
DEPARTAMENTO DE CIENCIA Y TECNOLOGÍA AGROFORESTAL
Para la realización de este trabajo se ha contado con la financiación de los
proyectos “Bases para la elaboración de un plan de gestión de la cabra
montés” y “Herramientas para la estimación objetiva de situaciones de
sobreabundancia de ciervo y jabalí en Castilla-La Mancha” (Dirección General
de Medio Natural, Junta de Comunidades de Castilla-La Mancha), y de los
convenios entre el Principado de Asturias y el CSIC.
A mis padres José Manuel y Elena y a mis hermanos Adrián y Cristina
Cómo no, a mis primos y tíos, y a mi ahijado Alberto
A Mónica por su cariño, alegría, colaboración y comprensión
A Christian Gortázar, Jorge Cassinello y Joaquín Vicente
AGRADECIMIENTOS
Muchas veces me he planteado la opción de comenzar y acabar esta
sección con la palabra GRACIAS... y nada más. Sencillamente por evitar el
resumir en una página la mención de tantas personas a las que debo mucho.
Primero quiero agradecer a Christian Gortázar la confianza puesta en mí
durante estos cuatro años de trabajo, muchas veces duro aunque siempre
gratificante. Junto a Christian, Jorge Cassinello y Joaquín Vicente me han
“guiado” en esta etapa, gracias por vuestro apoyo y consejos.
Ahora me vienen a la cabeza amigos de la Facultad, Kike, Jacobo,
Pablo, Isaac, Nino..., con vosotros han sido muy placenteros los años vividos
en Oviedo. Y como no, a los amiguetes de la Villa, Gale y Paula, Pedro e Isa,
Dani y les cullebres, Buta y Elena, El Conde, Velín, Fito, Sami y Sandra, Xitin y
Marga, Carlinos y Amparo, Chucho y Ana, Chendo. A los amigos de Ciudad
Real, Elena y Nacho, Raquel y Chesco, Alfredo y Marta, gracias por acogerme
entre vosotros y ser tan buena gente.
Mi vida en el IREC comenzó al poco tiempo de acabar en la Facultad,
fueron Emilio Álvarez y Pilar Collada quienes me hablaron del centro y me
presentaron a toda la gente en Ciudad Real, muchas gracias, os estoy muy
agradecido. Siguiendo con los asturianos me acuerdo y tengo que agradecer la
hospitalidad de la gente del SERIDA, Miguel, Alberto, Ana, Rosa, Isabel y
Paloma. De la Consejería de Medio Ambiente del Principado de Asturias tengo
que agradecer el apoyo de todos los Agentes Medioambientales, y de manera
especial a Jaime, Ángel y Francisco.
A Aurelio Malo y a Joaquín Hortal, gracias por acceder a evaluar la tesis,
y por los buenos consejos. Además a Joaquín debo agradecerle el tiempo que
me ha dedicado, siempre ha estado dispuesto a escuchar mis dudas y
orientarme, muchas gracias por todo.
A la gente de EBRONATURA, Marcu, J. Marco, Javier, José Luis,
gracias por compartir con nosotros toda la información y ser tan pacientes
conmigo. Ha sido muy agradable colaborar con vosotros y espero continuar
haciéndolo por muchos años.
A Carlos Cano, Andrés Alguacil y todos los Guardas Rurales de
Albacete, gracias por el tiempo que me habéis dedicado y por compartir
conmigo todo vuestro conocimiento sobre cabras.
Ya en Ciudad Real, a toda la gente del IREC, empezando por “servicios
generales”, los de arriba del IREC, gracias Andrés, Arturo, Lucía, y a los de
abajo, Jorge, Vicente, Terri, Javi, Mari y Angelines, por vuestra eficacia. A “los
de ecología” y a “los de Albacete” becarios, contratados, “practicantes”,
también a los jefes, recuerdo los buenos momentos vividos con vosotros,
gracias Killo, Jota, Paquillo, Dávila, Viñu, Rafa, Julián, Tomás, Andrés, Gustau,
Loren, Fabi, Luisen, Paqui, Peibol, Inés, Ester, Pablo, Pedro, Joaquín, Esther,
Rouconen, Michi, Jorge, Marisa, María y Nacho. Espero no haber olvidado a
nadie...
Qué decir de los amigos y compañeros de sanidad animal, hemos sido
una piña y espero que siga así por mucho tiempo. Christian y María, Joaquín y
Elo, Vidal, Millaguer, José Manuel, Piratúa y Esther, Chute y Cristina, La Tita,
Francis y Dieguín, Peich, Gildo y lo que venga, Josplis, Juanma y Adrián, la Fli
también jo..., Raquel, Elisa y Loren, Victoria, Pepe, Mario y Bianki, Oscarín,
Álvaro, Gamarra, Rafita, Felisuco, Encarni, Manolo, Paqui y Pablo, Iris, Mónica,
Rafa y Dolo. Sabéis que cada uno de vosotros tiene mis agradecimientos y
siempre estaré dispuesto a echaros una mano. Os deseo lo mejor a todos.
Tesis Doctoral
___________________________________________________________________ I
ÍNDICE
INTRODUCCIÓN……………………………………………………........................... 1
Modelos predictivos: distribución y nicho ecológico de las especies.……………………………..........................................................
3
Modelos predictivos para el estudio de la distribución...................... 5
La distribución de las especies: el nicho ecológico........................... 12
Relaciones interespecíficas y modelos predictivos........................... 15
Bibliografía......................................................................................... 17
Conocimiento actual y líneas futuras de investigación con cabra montés (Capra pyrenaica).........................…...………………….............
25
Resumen........................................................................................… 27
Abstract............................................................................................. 27
Short Foreword.................................................................................. 28
Systematics and taxonomy of the Iberian ibex..……………………… 30
Distribution.........................................…............................................ 31
Population abundance....................................................................... 33
Morphology........................................................................................ 34
Feeding habits………………………………………………………….... 36
Behavioural ecology…………………………………………………….. 37
Epidemiology and health status......................................................... 39
Conservation……………………………………………………………... 42
Future directions of Capra pyrenaica research................................ 43
Acknowledgements……………………………………………………… 45
References........................................................................................ 45
Índice
___________________________________________________________________ II
Objetivos y organización de la Tesis.................………..….................. 53
Objetivos…………………………………………………………………. 55
Organización de la Tesis……………………………………………...... 58
Capítulo 1. DISTRIBUCIÓN Y ESTATUS DE LAS POBLACIONES DE CABRA MONTÉS (Capra pyrenaica hispanica) EN CASTILLA-LA MANCHA………………………………………………………………………………...
61
1.1. El proceso de expansión de la cabra montés en Castilla-La Mancha, y su desplazamiento hacia hábitats subóptimos por la presencia de ganado caprino………………………………………….....
63
Resumen………………………………………………………………..... 65
Abstract………………………………………………………………….... 65
Introduction……………………………………………………………..... 66
Material and Methods………………………………………………….... 68
Results…………………………………………………………………..... 75
Discussion.....................……………………………………………….... 79
Acknowledgements…………………………………………………….... 81
References........................................................................................ 82
1.2. Relaciones entre la excreción de nematodos broncopulmonares y la abundancia relativa de cabra montés (Capra pyrenaica hispanica) en Castilla-La Mancha…………...........
89
Resumen………………………………………………………………..... 91
Abstract………………………………………………………………….... 91
Introduction……………………………………………………………..... 92
Material and Methods………………………………………………….... 93
Results…………………………………………………………………..... 96
Tesis Doctoral
___________________________________________________________________ III
Discussion.....................……………………………………………….... 99
Acknowledgements…………………………………………………….... 101
References......................................................................................... 101
Capítulo 2. LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR EL HOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO DE ESPECIES TAXONÓMICAMENTE DISTANTES: EL CIERVO IBÉRICO Y LA CABRA MONTÉS …………………………………………………….........................
105
Resumen………………………………………………………………..... 107
Abstract………………………………………………………………….... 107
Introduction……………………………………………………………..... 108
Material and Methods………………………………………………….... 112
Results…………………………………………………………………..... 117
Discussion.....................……………………………………….………... 121
Acknowledgements………………………………………………..…….. 125
References......................................................................................... 126
Capítulo 3. LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR EL HOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO: EL CASO DE UNA ESPECIE EXÓTICA, EL ARRUI, Y LA CABRA MONTÉS....................
133
31. Perspectivas de la expansión poblacional del arrui (Ammotragus lervia, Bovidae) en la Península Ibérica: uso de modelos de adecuación de hábitat …………………………….............
135
Resumen………………………………………………………………..... 137
Abstract………………………………………………………………….... 137
Introduction……………………………………………………………..... 138
Material and Methods…………………………………………............... 141
Índice
___________________________________________________________________ IV
Results…………………………………………………………………..... 149
Discussion.....................……………………………………………….... 154
Acknowledgements……………………………………………..……….. 157
References......................................................................................... 157
3.2. Es el arrui (Ammotragus lervia) una amenaza para la cabra montés (Capra pyrenaica)? Una aproximación basada en modelos de adecuación de hábitat……………....................................
165
Resumen………………………………………………………………..... 167
Abstract………………………………………………………………….... 167
Introduction……………………………………………………………..... 168
Material and Methods………………………………………………….... 171
Results…………………………………………………………………..... 175
Discussion.....................………………………….……………………... 179
Acknowledgements……………………………………………………… 184
References......................................................................................... 185
Capítulo 4. SÍNTESIS Y CONCLUSIONES.......................................................... 191
4.1. Síntesis…....................................…………................................... 193
Capítulo 1…....................................................................................... 195
Capítulo 2……………………………………………………………….... 198
Capítulo 3……………..………………………………………………….. 200
4.2. Conclusiones……........................………..................................... 207
MODELOS PREDICTIVOS: DISTRIBUCIÓN Y NICHO ECOLÓGICO DE LAS ESPECIES CONOCIMIENTO ACTUAL Y LÍNEAS FUTURAS DE INVESTIGACIÓN CON CABRA MONTÉS (CAPRA PYRENAICA) OBJETIVOS Y ORGANIZACIÓN DE LA TESIS
INTRODUCCIÓN
MODELOS PREDICTIVOS: DISTRIBUCIÓN Y NICHO ECOLÓGICO DE
LAS ESPECIES
Tesis Doctoral
________________________________________________________________ 5
MODELOS PREDICTIVOS PARA EL ESTUDIO DE LA DISTRIBUCIÓN
El estudio de las relaciones hábitat-especie ha sido uno de los pilares de
desarrollo de la ecología. Dichas relaciones se han enfocado desde muy
diversos niveles, que van desde la distribución geográfica de las especies
hasta el uso que éstas hacen de los recursos en un marco local, por ejemplo su
área de campeo (p.e., MacArthur 1972; Johnson 1980). Como es habitual en el
mundo natural, todos los niveles están organizados (Bissonette 1997) e
interconectados, por lo que los avances que se logren en la comprensión del
funcionamiento de cada uno de ellos pueden ayudar a explicar parte de los
otros. En la presente Tesis Doctoral se han estudiado estas relaciones a nivel
de distribución geográfica basándose para ello en la expresión del nicho
ecológico de las especies.
Los primeros estudios que versan sobre las relaciones hábitat-especie
se remontan a 1800, y en ellos ya se destaca la importancia que tienen los
factores climáticos en los patrones de distribución de los seres vivos (Humboldt
y Bonpland 1807; de Candolle 1855; Salisbury 1926). Otros factores
ambientales han sido incorporados en los estudios con el fin de profundizar en
el conocimiento de los condicionantes de la distribución geográfica de las
especies (p.e., Good 1953; MacArthur 1972; Stott 1981). A partir del
conocimiento de estas relaciones, se construye una disciplina alrededor del
estudio de los patrones espaciales, y que tiene una de sus bases en la
modelización de la distribución de las especies en función de sus
requerimientos ambientales. Además de su relevancia inicial, los modelos de
distribución han ganando una enorme importancia en los últimos años debido a
su utilidad como herramientas para el estudio del impacto de los cambios
ambientales (cambios en el uso del suelo, cambio climático, etc.) sobre la
distribución de los organismos (p.e., Araújo y cols. 2005a; del Barrio y cols.
2006; Rounsevell y cols. 2006; Thuiller y cols. 2006), y de las hipótesis
biogeográficas (p.e., Anderson y Wait 2001; Barret y cols. 2003; Triantis y cols.
2006), así como para el desarrollo y perfeccionamiento de los atlas de
distribución de especies (p.e., Hausser 1995; Araújo y cols. 2005b), o para
Introducción
________________________________________________________________ 6
establecer prioridades en diversos campos de la conservación (p.e., Margules y
Austin 1994; Engler y cols. 2004; Guisan y cols. 2006; Quevedo y cols. 2006).
En las siguientes secciones de este apartado se ha pretendido realizar
una introducción a los modelos predictivos, tanto en sus aspectos
conceptuales, como a las aproximaciones estadísticas en las que se sustentan.
Aspectos conceptuales
Un modelo es una simplificación de la realidad, por lo tanto toda la
complejidad y heterogeneidad de la naturaleza no puede ser predicha con
elevada precisión con un simple modelo. Levins (1966) formula el principio de
que sólo dos de las tres propiedades deseables de un modelo (generalidad,
realidad y precisión) pueden ser potenciadas simultáneamente mientras que la
tercera ha de ser sacrificada. Este balance (del inglés trade-off) permite
distinguir tres grupos de modelos (Sharpe 1990; Prentice y Helmisaari 1991;
Korzukhin y cols. 1996; ver Figura 1).
Figura 1.- Clasificación de los modelos según sus propiedades intrínsecas (Levins 1966). Figura adaptada de Guisan y Zimmermann (2000).
Tesis Doctoral
________________________________________________________________ 7
En el primer grupo están aquellos en los que se potencia la generalidad
y la precisión por lo que los modelos son llamados analíticos (Pickett y cols.
1994), y son designados para predecir correctamente dentro de una realidad
limitada o simplificada, sin saber si el modelo es real o sólo es debido a
correlaciones espúreas. Un segundo grupo de modelos es elegido para ser real
y general, son los llamados mecanísticos (p.e., Prentice 1986), y basan sus
predicciones sobre relaciones causa efecto reales, aunque sus predicciones
son poco precisas. Por último, el tercer grupo sacrifica generalidad por
precisión y realidad, son los llamados modelos empíricos (p.e., Korzukhin y
cols. 1996), cuya formulación matemática tiene como principal propósito
resumir los hallazgos experimentales (p.e., Wissel 1992), aunque sus
resultados puedan no ser generales.
Esta clasificación es ampliamente usada aunque existe cierta
controversia y algunos autores la han criticado (p.e., Prentice y cols. 1992;
Korzukhin y cols. 1996) basándose en que no siempre se sacrifica una de las
propiedades ya que, en ocasiones, se pueden potenciar las tres al mismo
tiempo. Sin embargo otros autores aceptan la clasificación de Levins (1966)
considerando, sobre todo, que es muy aplicable en contextos conceptuales
(Guisan y Zimmermarnn 2000).
Desde la década de los noventa el desarrollo de nuevas teorías
ecológicas y biogeográficas ha ido aumentando, y éstas han podido ser
tratadas desde un enfoque novedoso gracias al perfeccionamiento de
programas informáticos diseñados para el manejo y análisis de la información
espacial, son los Sistemas de Información Geográfica, más conocidos por su
acrónimo SIG. En el entorno de los SIG, están progresando nuevas
metodologías de análisis para el estudio de los patrones espaciales de los
seres vivos, pudiendo englobarse todos estos estudios dentro de la rama
denominada Biogeografía de la Conservación (del inglés Biogeography
Conservation). Este término ha sido recien acuñado por Lomolino (2004), y
posteriormente Whittaker y cols. (2005) han definido sus bases. Estos últimos
autores definen la Biogeografía de la Conservación como la aplicación de los
principios, teorías y análisis biogeográficos (dinámicas de distribución de
taxones tanto individual como colectivamente) a problemas relacionados con la
Introducción
________________________________________________________________ 8
conservación de la biodiversidad. La mayoría de estas metodologías están
basadas en el modelizado de las respuestas de las especies a las condiciones
ambientales. De acuerdo con Austin y cols. (1990), las relaciones entre los
gradientes ambientales (temperatura, precipitación, humedad, etc.) y la
adecuación del medio para la supervivencia de población siguen una curva
normal (es decir, mayor adecuación en el centro del gradiente, y una progresiva
disminución hacia los dos extremos). Analizando estas relaciones con los
gradientes ambientales mediante el empleo de herramientas estadísticas (p.e.,
regresión múltiple), se obtiene un modelo de la respuesta potencial de la
especie a cada uno de los gradientes.
Básicamente, se puede decir que la correcta construcción de un modelo
predictivo comprende cinco pasos fundamentales (Figura 2), que son: i)
concepto sobre el que se desarrolla el modelo, ii) formulación matemática del
mismo, iii) calibración o puesta a punto, iv) obtención de predicciones, y v)
evaluación de su capacidad predictiva.
Figura 2.- Visión general de los sucesivos pasos (de 1 a 5) necesarios para construir un modelo cuando están disponibles dos bases de datos: una para fijar el modelo y otra para evaluarlo. La validación se puede abordar de dos maneras diferentes: usando los mismos datos con los que se ha construido el modelo mediante procedimientos como bootstrap, validación cruzada (del inglés cross-validation) o Jackknife, o usando datos independientes y comparando los valores predichos por el modelo con ellos usando medidas independientes del umbral como la aproximación ROC (del inglés receiver operating characteristic). Figura adaptada de Guisan y Zimmermann (2000).
Tesis Doctoral
________________________________________________________________ 9
Cada uno de estos pasos ha sido recientemente evaluado en numerosas
publicaciones, por ejemplo, en cuanto a la formulación matemática se han
desarrollado trabajos que valoran la capacidad de distintos algoritmos para
predecir correctamente la distribución de las especies (p.e., Guisan y cols.
2002; Elith y cols. 2006), y la capacidad predictiva de los modelos ha sido
estimada siguiendo distintas metodologías y paralelamente han sido
desarrollados estudios comparativos para evaluar la potencia de cada una de
ellas (p.e., Pearce y Ferrier 2000; Segurado y Araújo 2004).
Por tanto, cada uno de los cinco procesos es clave para el correcto
desarrollo del modelo y, en la actualidad, numerosos esfuerzos y proyectos de
investigación están siendo desarrollados para perfeccionar la metodología
participando en ello, y de manera activa, varios equipos españoles (p.e.,
Brotons y cols. 2004; Chefaoui y cols. 2005; Hortal y Lobo 2005; Jiménez-
Valverde y Lobo 2005; Hortal y cols. 2006; Jiménez-Valverde y cols. 2006;
Lobo y cols. 2006).
Aproximaciones estadísticas a los modelos
Para la formulación estadística, llamada verificación por algunos autores
(p.e., Rykiel 1996), se debe seleccionar un algoritmo apropiado con el fin de
predecir un tipo de variable dependiente y estimar los coeficientes del modelo,
así como una aproximación estadística óptima considerando el contexto del
modelo (Guisan y Zimmermann 2000). La mayoría de los modelos son
específicos para un tipo particular de variable dependiente y su distribución
teórica, pudiendo considerarse éste el primer condicionante a la hora de
seleccionar el método de modelización a usar.
A continuación, se muestran y explican brevemente las principales
aproximaciones estadísticas usadas para modelizar, y para ello se agrupan en
siete categorías (Guisan y Zimmermann 2000): regresiones múltiples y sus
formas generalizadas, técnicas de clasificación, envueltas ambientales,
técnicas de ordenación, aproximaciones Bayesianas, redes neuronales y
aproximaciones mixtas.
Introducción
________________________________________________________________ 10
Regresiones generalizadas y técnicas relacionadas: Las regresiones
relacionan una variable dependiente a una (regresión simple) o varias
(regresión múltiple) variables ambientales independientes, también llamados
predictores ambientales. Los Modelos Lineales Generalizados (GLM)
constituyen la familia más flexible de modelos en cuanto a las distribuciones
que puede presentar la variable dependiente (normal, Poisson, binomial o
gamma; McCullagh y Nelder 1989). Otras técnicas de regresión alternativas
están basadas en funciones no paramétricas, son los Modelos Generalizados
Aditivos (GAM). Las regresiones son comúnmente usadas para modelizar la
distribución de las especies (p.e., Bio y cols. 1998; Lehmann 1998; Brotons y
cols. 2004; Engler y cols. 2004; Lobo y cols. 2006; Quevedo y cols. 2006).
Técnicas de clasificación: Dentro de este grupo se incluyen los árboles
de clasificación (p.e., Franklin y cols. 2000), clasificación basada en reglas
(p.e., Lenihan y Neilson 1993) y clasificación por máxima probabilidad (p.e.,
Franklin y Wilson 1991). Algunos SIG implementan las técnicas de máxima
probabilidad bajo los nombres de clasificación supervisada y sin supervisar, en
función de la presencia de datos para la calibración del modelo. Estos métodos
realmente son poco usados en estudios de distribución (p.e., Franklin 1998).
Envueltas ambientales (del inglés Environmental envelopes): Estas
técnicas se han empleado para modelizar la distribución de las especies a
escalas espaciales muy amplias (p.e., Busby 1991; Shao y Halpin 1995).
Dentro de éstas se encuentran modelos como el BIOCLIM (Busby 1986, 1991),
el HABITAT (Cocks y Baird 1991) y el DOMAIN (Carpenter y cols. 1993). En
líneas generales, estos modelos calculan con diversos algoritmos el rango de
condiciones de una serie de variables en las que está presente la especie. En
la actualidad éstas son técnicas en las que se está trabajando con el fin de
potenciar su robustez (p.e., Marra y cols. 2004; Elith y cols. 2006).
Técnicas de ordenación: La mayoría de los modelos que usan técnicas
de ordenación están basados en los análisis canónicos de correspondencia
(ver p.e., Hill 1991; Ohmann y Spiess 1998; Guisan y cols. 1999). En ellos, el
eje de ordenación principal (gradiente directo) es necesariamente una
combinación de los predictores ambientales (ter Braak 1988), y se asume que
las especies aparecen a lo largo del gradiente siguiendo una distribución
Tesis Doctoral
________________________________________________________________ 11
normal. Estos métodos resultan muy apropiados para estudios de especies
raras (p.e., ter Braak 1985; Ohmann y Spiess 1998; Guisan y cols. 1999), esto
es, especies que aparecen con una frecuencia muy baja.
Aproximaciones Bayesianas: Los modelos basados en estadísticos
Bayesianos combinan probabilidades de detección de una especie establecidas
a priori (desde estudios previos) para un lugar concreto (p.e., Skidmore 1989;
Aspinall y Veitch 1993), con las probabilidades de aparición en ese sitio, pero
en este caso, condicionadas al valor de cada predictor ambiental. Son poco
usados en estudios de distribución (Fischer 1990; Brzeziecki y cols. 1993)
debido a sus limitaciones metodológicas.
Redes neuronales: Se ha recurrido a las redes neuronales para estudiar
la distribución de las especies mediante modelos predictivos de hábitat en el
marco de la teledetección (Fitzgerald y Lees 1992). Usando esta metodología,
estos autores han obtenido resultados más robustos que aplicando regresiones
múltiples, sobre todo cuando las relaciones no son lineales. Como este método
aún no ha sido muy usado para modelizar la distribución, no se entrará en
detalle (para una detallada discusión sobre el método, ver Hepner y cols. 1990;
Benediktsson y cols. 1991).
Otras aproximaciones: Entre éstas se encuentran los modelos simples
que pueden ser desarrollados directamente dentro del SIG mediante relaciones
algebraicas con los predictores (Martinez-Taberner y cols. 1992). Otros son los
modelos discriminantes (p.e., Corsi y cols. 1999), que tienen un formulado
similar al de los GLM de distribución binomial. El Análisis Factorial de Nicho
Ecológico (ENFA; Hirzel y cols. 2002) es similar a los basados en envueltas
ambientales pero requiere sólo datos de presencia para computar el modelo de
distribución. Otras metodologías han sido descritas (p.e., GARP, Stockwell y
Peters 1999) y otras nuevas se implementarán para desarrollar modelos
robustos y con elevada capacidad predictiva.
Introducción
________________________________________________________________ 12
LA DISTRIBUCIÓN DE LAS ESPECIES: EL NICHO ECOLÓGICO
El área de distribución de una especie es una compleja expresión de su
ecología e historia evolutiva (Brown 1995), estando determinada por diversos
factores que operan con diferente intensidad y a distintas escalas (Gaston
2003; Pearson y Dawson 2003). Estos factores se pueden clasificar en cuatro
grupos (Soberón y Peterson 2005):
1. Abióticos; que incluyen aspectos del clima, del suelo, etc., y que
imponen los límites fisiológicos sobre la capacidad de una especie para
persistir en un área determinada.
2. Bióticos; considerando las interacciones con otras especies que
modifican la capacidad de permanencia de las poblaciones. Estas
interacciones pueden ser positivas (p.e., mutualismo) o negativas (p.e.,
competición, depredación, parasitismo). Debido a la limitación que
suponen los factores bióticos en los procesos poblacionales, estos
obviamente pueden afectar a sus distribuciones.
3. Potencial dispersivo; son las regiones que tienen potencial como para
que una especie se pueda dispersar desde alguna población que actúa
como núcleo de origen. Este factor es muy usado para distinguir entre la
distribución actual y potencial de una especie, basándose en la
configuración del paisaje y en la capacidad de dispersión de las
especies.
4. Evolutivos; capacidad evolutiva de las poblaciones para adaptarse a
nuevas condiciones. Este factor, en ocasiones considerado
insignificante, es sin embargo de gran importancia para resumir las
posibilidades distributivas de las especies.
Los factores interaccionan dinámicamente para producir la compleja
entidad llamada distribución geográfica de las especies. Se asume que una
especie estará presente en un punto geográfico donde los tres grupos de
factores sean favorables (en este caso no se consideran los evolutivos), esto
es, donde las condiciones abióticas sean adecuadas (región A), donde un
grupo adecuado de especies constituyan el ecosistema (región B), y
Tesis Doctoral
________________________________________________________________ 13
finalmente, donde pueda llegar desde los núcleos poblacionales establecidos
(región M). Esto se representa en el siguiente esquema (Figura 3).
La región A representa la expresión geográfica del Nicho Fundamental
(del inglés Fundamental Niche) de la especie (Hutchinson 1957). La región B
es aquella en las que las relaciones interespecíficas necesarias para que la
especie cohabite quedan satisfechas, tanto las negativas (p.e., competición),
como las positivas (p.e., mutualismo).
Figura 3.- a) El círculo A representa la región geográfica en la que los factores abióticos son adecuados para la especie (nicho fundamental). El círculo B es la región donde se encuentra una combinación de especies tal que permite el asentamiento de la especie considerada. A ∩ B (área sombreada en azul más la región P) es la expresión de su nicho realizado. El círculo M es la parte del mundo en términos ecológicos accesible para la especie, esto es, sin barreras dispersivas. Finalmente A ∩ B ∩ M = P es la región que contiene las peculiaridades tanto abióticas como bióticas y que es accesible para la especie (distribución de la especie). El resto de figuras representan casos extremos en el solapamiento entre las zonas A, B y M (se explican en el texto). Caso I) A = B = M. Caso II) A = M ≠ B. Caso III) A = B ≠ M. Figuras adaptadas de Soberón y Peterson (2005).
Introducción
________________________________________________________________ 14
Por ello, la intersección entre la región A y la B es la parte del mundo
que cumple los requerimientos, abióticos y bióticos, necesarios que permiten el
asentamiento estable de una especie, esto es, su Nicho Realizado (del inglés
Realized Niche; Hutchinson 1957). Finalmente, la región M representa el área
accesible para la especie desde sus núcleos poblaciones de origen, esto es,
considerando la potencialidad del medio para la expansión de la especie. Aquí,
se deben considerar las expansiones no naturales en las que ha intervenido el
hombre por medio de introducciones de especies en lugares lejanos. Desde
una perspectiva heurística, una población estable de una especie sólo puede
encontrarse en el área donde las tres regiones (A, B y M) interseccionan (área
P) y que representa la distribución de la especie (Soberón y Peterson 2005).
Dentro de este contexto, antes de aplicar un modelo matemático sobre los
datos de distribución de una especie es necesario conocer la parte del nicho de
la especie que se está modelizando, esto es, ¿se modeliza su nicho
fundamental?, ¿su nicho realizado?, o incluso ¿su distribución real?
Nunca se debe perder de vista que los datos de distribución de una
especie usados para estos propósitos son datos del área P, que a su vez
pertenece a la regiones A, B y M. En la Figura 3 se representan tres casos
extremos de solapamiento entre estas regiones. Así, el Caso I es el más simple
y optimista de todos. En él las tres regiones están solapadas por lo que el nicho
fundamental y el realizado son similares, y son también similares a la
distribución de la especie. Por lo tanto, modelizaciones de la especie podrían
ser igualmente interpretadas tanto en cuanto a nicho fundamental, como a
nicho realizado o distribución actual. El Caso II representa la situación donde M
se solapa con A, esta situación se puede dar como consecuencia del uso de
escalas espaciales de estudio pequeñas o porque las peculiaridades
dispersivas de la especie y la composición del paisaje hagan que no existan
barreras siendo la mayor parte del nicho fundamental accesible para ella. Aquí,
la región B solapa sólo con una pequeña proporción de las otras dos regiones
debido a fuertes relaciones interespecíficas (positivas y negativas), por lo que
el nicho fundamental de la especie es mucho más amplio que su área de
distribución. En esta situación las interpretaciones de la modelización deben
ser cautelosas ya que se tiende a sobreestimar el nicho fundamental. Por
Tesis Doctoral
________________________________________________________________ 15
último, en el Caso III el nicho fundamental solapa con la región en la que las
interacciones son adecuadas (permiten el asentamiento de la especie), pero sin
embargo, la complejidad geográfica genera barreras que potencian la creación
de núcleos poblacionales aislados. Nuevamente en esta situación el nicho
fundamental es más amplio que el área de distribución de la especie y las
interpretaciones de los modelos han de hacerse con cierta cautela.
RELACIONES INTERESPECÍFICAS Y MODELOS PREDICTIVOS
Como anteriormente se ha descrito, el nicho fundamental de una especie
está modulado, entre otros, por factores biológicos (Soberón y Peterson 2005)
entre los que se encuentran las relaciones interespecíficas, es decir, el rango
geográfico de una especie puede verse restringido por la presencia de
competidores, depredadores, o parásitos, que reducen su nicho fundamental a
una fracción que puede ser explotada de manera estable por la especie. Ésta
es la expresión de su nicho realizado (Hutchinson 1957). Los requerimientos
ecológicos de especies emparentadas son similares y pueden impedir su
coexistencia en un ambiente limitante (p.e., MacArthur 1972), por lo que el
nicho ecológico de una especie puede quedar restringido por la presencia de
otra especie en simpatría. Por ejemplo, especies de mamíferos emparentadas,
cuando aparecen en simpatría, muestran segregación a nivel de micro y de
macrohábitat (p.e., Wilson 1968; Stoecker 1972; Emmons 1980). En algunos
casos han sido documentados comportamientos agresivos como mecanismo
para las relaciones de competencia deducidas desde patrones geográficos
(Brown 1971; Heller 1971; Murie 1971; Sheppard 1971; Stoecker 1972;
Alberico y González-M 1993). Finalmente, experimentos sobre exclusión
competitiva han confirmado la habilidad que presentan algunas especies de
mamíferos para excluir a sus congéneres donde sus rangos geográficos entran
en contacto (Koplin y Hoffmann 1968; Stoecker 1972; Chappell 1978; Schoener
1983).
Sin embargo, diferenciar los determinantes ecológicos e históricos de la
distribución de las especies en un contexto geográfico es una cuestión
Introducción
________________________________________________________________ 16
metodológicamente difícil (Endler 1982). En la mayoría de los casos, la
interpretación de estas relaciones se ha visto entorpecida por una falta de
objetividad a la hora de cuantificar la adecuación de hábitat para las especies
(p.e., MacArthur 1972; Terborgh y Weske 1975; Bergstrom y Hoffmann 1991;
Remsen y Graves 1995).
Los recientes avances en los SIG permiten ahora realizar robustos
análisis del nicho ecológico de las especies (p.e., Chefaoui y cols. 2005;
Acevedo et al. 2006 [Capítulo 1.1]; [Capítulos 2 y 3]), pudiendo ser testadas
hipótesis biogeográficas que anteriormente no podían serlo debido a
limitaciones metodológicas. En este momento, surgen estudios comparativos
entre los nichos de especies relacionadas (p.e., Anderson y cols. 2002;
Chefaoui y cols. 2005; Hortal y cols. 2005; Acevedo y cols. 2006 [Capítulo 1.1]; Lobo y cols. 2006 [Capítulos 2 y 3.2]; Figura 4).
Figura 4.- Ejemplo de estudio de relaciones de nicho entre especies. La figura muestra la variación de la adecuación de hábitat a lo largo del gradiente ambiental de la zona de estudio (factor de marginalidad) para dos especies de escarabajos (Copris hispanus es representada por la línea continua, y C. lunaris por la línea discontinua). Figura tomada de Chefaoui y cols. (2005).
Tesis Doctoral
________________________________________________________________ 17
En un contexto más ecológico y menos geográfico, numerosos trabajos
han manifestado la elevada potencialidad de los ungulados para que se
establezcan relaciones de competencia entre especies que viven en simpatría
(p.e., Putman 1996 y las referencias que cita). Sin embargo, son escasos los
trabajos que evidencien variaciones en parámetros poblacionales debidas
puramente a competencia interespecífica. Respecto a esto, Putman (1996)
concluye que incluso en un ambiente limitante, a pesar de que a priori eran
esperables las relaciones de competencia entre especies simpátricas, y aunque
se detectaron cambios en sus tamaños poblacionales a lo largo del tiempo, no
se pudo concluir la existencia de un claro efecto negativo de una especie sobre
la otra, en este caso del gamo (Dama dama) sobre el corzo (Capreolus
capreolus). Otros autores han demostrado que el rango de separación en las
distribuciones del ciervo de cola blanca (Odocoileus virginianus) y el ciervo
bura (Odocoileus hemionus crooki) ha sido causado por relaciones
competitivas (Anthony y Smith 1977), y recientemente se ha visto que el corzo
ha sido desplazado por el gamo en Italia (Focardi y cols. 2006).
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CONOCIMIENTO ACTUAL Y LÍNEAS FUTURAS DE INVESTIGACIÓN CON
CABRA MONTÉS (CAPRA PYRENAICA) Acevedo, P., Cassinello, J. A REVIEW OF CAPRA PYRENAICA KNOWLEDGE:
TAXONOMY, DISTRIBUTION, ECOLOGY, CONSERVATION AND PROPOSAL FOR FUTURE
RESEARCH LINES. Mammal Review, en evaluación (enviado a 3/08/2006).
Tesis Doctoral
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RESUMEN
1. Se ha realizado una revisión de los conocimientos existentes sobre la cabra
montés, Capra pyrenaica. La mayoría de las publicaciones han sido obtenidas de
revistas locales y libros nacionales, así como de informes inéditos, siendo muy poca la
información disponible en revistas internacionales de fácil acceso para la comunidad
científica. Para solventar el problema de la reducida accesibilidad de buena parte de la
información, se ofrece esta revisión como un resumen y actualización de toda la
información disponible sobre la especie.
2. Análisis genéticos recientes han arrojado algunas dudas sobre la taxonomía
más aceptada de la especie, caracterizada ésta por la presencia de 4 subespecies de
las que sólo persisten dos, C. p. victoriae y C. p. hispanica.
3. Además de las introducciones que se vienen realizando tradicionalmente,
actualmente está teniendo lugar una expansión natural de las poblaciones de
monteses. En esta revisión, se actualiza su estatus poblacional, distribución y
abundancia.
4. Han sido realizados estudios descriptivos sobre la morfología, hábitos
alimenticios, ecología del comportamiento, epidemiología y estado sanitario de la
cabra montés. Sin embargo, estudios que integren todos estos aspectos aún no han
sido realizados.
5. Las extinciones previas deberían hacer que seamos cautelosos en la
preservación de la especie, ya que, aunque actualmente sus poblaciones están en
general expandiéndose, se han identificado una serie de amenazas potenciales para
esta especie entre las que se encuentran la sobreabundancia, las enfermedades, y la
competición tanto con ganado doméstico como con especies invasoras.
6. Finalmente se enumeran líneas de investigación que, a nuestra opinión,
deben ser priorizadas para la conservación de la cabra montés, por ejemplo, la
ecología aplicada dirigida hacia una correcta gestión de las poblaciones, así como
estudios experimentales encaminados a la identificación de posibles amenazas que
pueden acechar sobre esta especie.
ABSTRACT
1. A revision of current knowledge of the Iberian ibex, Capra pyrenaica, is
provided. Most of the published material can be obtained from local journals and
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books, as well as unpublished reports. Very little is to be found on international, easy to
access, sources. In order to solve this lack of information, the present review offers a
compilation and up-to-date revision of the species.
2. Recent genetic analyses have cast some doubts on the generally accepted
taxonomy of the species, conformed by four subspecies, from which only two persist
nowadays, C. p. victoriae and C. p. hispanica.
3. Apart from traditional translocations of ibex populations carried out by man, a
natural expansion of the species is currently taking place. Here, updated information of
its status, distribution and abundance is provided.
4. A series of descriptive studies have been carried out dealing with aspects
such as morphology, feeding habits, behavioural ecology, epidemiology and health
status; but no integrative, evolutionary or ecologically relevant work on these issues
have yet been carried out in this species.
5. Previous extinction events should make us is cautious on the preservation of
the species, since, although its current populations are in general under an expansion
trend, we have identified a series of threats, such as population overabundance,
diseases prevalence and competition against domestic livestock and invasive ungulate
species.
6. We finally enumerate a series of research topics which, to our view, should
be a priority in dealing with this species. Namely, applied ecological issues focused on
a proper management of the populations, as well as an identification of current
ecological threats based on empirical data obtained from populations under different
ecological conditions and regions.
SHORT FOREWORD
The Iberian ibex (Capra pyrenaica) is an endemic caprid of the Iberian
Peninsula, formerly widely distributed in all its mountainous regions, from the
southern coast (Sierra Nevada mountain range) to the Pyrenees. Their
populations started to suffer a steady decrease in numbers during the last
centuries due to great hunting pressure, together with agricultural development
and habitat deterioration, eventually originating the extinction of two of the four
recognized subspecies (e.g., Shackleton 1997; Pérez et al. 2002). When
attaining a scientific literature search of available works devoted to the species,
we rapidly noticed the scarcity of studies published on international, easily
Tesis Doctoral
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accessible, journals, while a number of local works, of a regional nature, were
also compiled.
The present review intends to fill this gap, offering a compilation and up-
to-date revision of the current knowledge of the species. It is noticeable that
prior to 1985 there was practically no mention of the species in the international
literature, afterwards there was an increase of articles, but after 90's decade a
new decline is seen (see Figure 1). We believe that this tendency basically
depends on a few numbers of researchers devoted to the study of this species.
0
5
10
15
20
25
30
35
40
45
before 1985 1985-1990 1991-1995 1996-2000 2001-2005
Years
Num
ber o
f pub
licat
ions
NationalInternationalOverall
Figure 1. The number of publications on the Iberian ibex are depicted according to the data sources: national journals and books (Spain), and international and SCI journals and books.
If we compare the number of research papers on the Iberian ibex and
other Iberian ungulate, the red deer (Cervus elaphus hispanicus), since 1990, a
ratio 34/94 is obtained (ISI Web of Knowledge database) with a clear
predomination of articles on the red deer, despite this being a subspecies of a
very well known species.
Although the term 'Spanish' ibex is commonly used in the literature, we
have gone for 'Iberian' ibex in this review because the species is currently not
only present in Spain but also in Portugal (Pérez et al. 2002). Actually, the
species is an Iberian endemism, as it originally occupied the whole Iberian
Peninsula.
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SYSTEMATICS AND TAXONOMY OF THE IBERIAN IBEX
At least a small numbers of ibexes were present in many Upper
Paleolithic and Azilian archaeological deposits in the Iberian Peninsula and
southern France (Straus 1987; Cardoso 1996). The genus Capra includes
several forms of wild goats that are present in mountain habitats from northern
Mongolia and Russia to Western Europe and Ethiopia (e.g. Manceau et al.
1999a). In Western Europe, wild goats are found in the Alps and in the Spanish
mountains.
According to paleontological studies of Crégut-Bonnoure (1992a, b), two
independent migration waves of wild goats took place in Europe. The first one
occurred some 300,000 years ago, and originated the Alpine ibex (C. ibex ibex);
the second immigration took place from Caucasus around 80,000 years ago,
origin of the Iberian ibex (C. pyrenaica). Under this scenario, no close
relationships would be expected between these European species. However,
allozyme data indicated a much lower genetic distance between the two
European species than between the other existing Capra species (Manceau et
al. 1999a). Thus, Maceau et al. (1999a) proposed another scenario, where only
one wave of immigration of Capra came into Europe, followed by a speciation
process that originated the current two European species. A paleontological
description of a Capra sp. specimen, dated around 120,000 years ago in
Germany (Toepfer 1934), combined the characters of the two European taxa;
this is in accordance with the one-wave hypothesis.
Several authors (e.g. Schaller 1977; Nowak 1991) recognize two different
subspecies for the Iberian ibex according to morphological criteria. However,
the IUCN (Shackleton 1997) recognizes four subspecies: C. pyrenaica
lusitanica, now extinct and formerly located in northern Portugal and southern
Galicia (Alados 1985a); C. p. pyrenaica, in the Pyrenees, recently extinct (Pérez
et al. 2002); C. p. hispanica, in the south and east of the Iberian Peninsula; C.
p. victoriae, mainly in central areas of Spain, such as Gredos mountain range.
However, this taxonomy is questionable because it is only based on two
morphological features: coat colour and horn morphology (Cabrera 1911),
characters that show a high inter-population variability (Couturier 1962; Clouet
1979). Manceau et al. (1999b) tested the morphologically recognized taxonomy
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of C. pyrenaica with mitochondrial DNA sequence polymorphism. Their study
does not support the recognition of the subspecies C. p. victoriae and C. p.
hispanica but it is congruent with the distinction between the Pyrenean
population and the other Iberian ones (ibid.). Although this study may not be
absolutely conclusive, it casts some doubts on the currently accepted taxonomy
for the species (Shackleton 1997):
Class: Mammalia Order: Artiodactyla Suborder: Ruminantia Infraorder: Pecora Family: Bovidae Subfamily: Caprinae Tribe: Caprinii Genus: Capra Linnaeus, 1758 Species : Capra pyrenaica, Schinz (1838) Subespecies: C. p. hispanica, Schimper (1848) C. p. pyrenaica, Schinz (1838) C. p. lusitanica, Schlegel (1872) C. p. victoriae, Cabrera (1911)
DISTRIBUTION
The status and distribution of the Iberian ibex have been studied and
revised by several authors, either in the whole peninsula (e.g. Alados 1997;
Granados et al. 2002; Pérez et al. 2002) or in some particular geographical
areas (e.g. Palomares and Ruiz-Martínez 1993; Pérez et al. 1994; Gortázar et
al. 2000; Sánchez-Hernández 2002; Acevedo et al. 2006 [Capítulo 1.1]).
Current distribution of the species is a consequence of both natural and
unnatural expansion processes. Most of translocations were carried out
posterior to 1970, except in the Maestrazgo area (in 1966), particularly during
1980s and 1990s (Pérez et al. 2002; see Figure 2). Moreover, currently a
natural expansion of the populations has been reported both for C. p. victoriae
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and for C. p. hispanica subspecies (Pérez et al. 2002; Acevedo et al. 2006
[Capítulo 1.1]).
The first distribution study dates back to 1911 (Cabrera 1911), followed
several decades later by a few articles and local reports (e.g. de la Peña 1978;
Alados 1985a, 1997). Recently, a thoroughly and long-expected revision of
current status of the Iberian populations was published (Pérez et al. 2002).
These authors established the distribution and population trends of the species,
concluding that its distribution is fragmented in 51 stable population nuclei and a
more extensive distribution area in comparison to previous studies (e.g. Alados
1997).
Mapping species distribution is a key issue in ecology and conservation
since statement of hypotheses often relies on an accurate knowledge of where
species occur. To map species distributions at large spatial scales, different
approaches have been adopted, the most common of which being the general
atlas-distribution framework (e.g. Underhill and Gibbons 2002). In this sense,
the Sociedad Española para la Conservación y Estudio de Mamíferos promoted
the creation of a distribution atlas of Iberian terrestrial mammals including the
Iberian ibex (Granados et al. 2002).
The ibex distribution in Castile–La Mancha (central Spain) has been very
recently updated (Acevedo et al. 2006 [Capítulo 1.1]). It has been noted a
wider presence of the species in this region in comparison with previous
surveys (Alados 1997; Granados et al. 2002; Pérez et al. 2002). The reported
expansion process of the species in Castile-La Mancha is to be attributed to the
natural increment of the population due to habitat changes and game
management translocations (Gortázar et al. 2000) and probably to a decrease
of its hunting pressure in this area (Garrido 2004).
In Figure 2 current distribution of the Iberian ibex is updated (from
Granados et al. 2002; Pérez et al. 2002; Acevedo et al. 2006 [Capítulo 1.1], unpublished data; C. Gortázar, J. Ferreres and M.A. Escudero personal
communications).
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POPULATION ABUNDANCE
More than 50,000 Iberian ibexes have been estimated to inhabit the
Iberian Peninsula (Pérez et al. 2002). The population status varies among the
different nuclei. The average ibex population’s density is 2.7 ind/km2, ranging
from 0.4 to more than 15.0 ind/km2, and a predomination of densities around
1.2 to 4.4 ind/km2 (Pérez et al. 2002; Sánchez-Hernández 2002; Acevedo et al.
2005a [Capítulo 1.2]).
Figure 2. Current distribution of the Iberian ibex, Capra pyrenaica (Granados et al. 2002; Pérez et al. 2002; Acevedo et al. 2006 [Capítulo 1.1]; C. Gortázar, J. Ferreres and M.A. Escudero personal communication). Dotted lines delimit boundaries of the provinces and the continuous line indicates individual translocations (Pérez et al. 2002). The predictable distribution limit of both subspecies is represented (double line), C. p. victoriae in the north-west, and C. p. hispanica in the south-east. The presence data are referred to UTM grid cells of 10 x 10 km2.
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Populations present in Sierra Nevada Natural Park, Cazorla, Segura y
Las Villas Natural Park and Gredos Regional Park represent more than 45% of
the Iberian ibexes (Pérez et al. 2002), i.e., almost half of the ibex individuals are
concentrated in three population nuclei. This may originate serious risks for the
species, due to the onset of infectious diseases under overabundance
conditions (Gortázar et al. 2006), or the appearance of stochastic negative
events which might cause populations decline. As for the two existing
subspecies, C. p. hispanica is more abundant (more than 80% of the Iberian
population) than C. p. victoriae (see Pérez et al. 2002).
There are different census methods to estimate relative abundance in
Iberian ungulate species (e.g. Alados and Escós 1996), from which indirect
methods based on traits search (e.g. Acevedo et al. 2005a [Capítulo 1.2]) are
particularly interesting, as they are cheap, effective and non-invasive (e.g.
Acevedo et al. 2005a [Capítulo 1.2], b, in press). We encourage carrying out a
proper monitoring through adequate and standardized census methods of the
ibex populations at a large spatial scale (Alados 1997).
MORPHOLOGY
Data on European ibexes morphology are derived principally from
Couturier (1962), Corbet (1966), Hainard (1949), Henrich (1961), Nievergelt
(1966), Van den Brink (1968) and Walker (1968). They are truly mountainous
animals, with large and elastic hooves and short legs, which facilitate them
running and leaping on bare rocky, rough and steep slopes (Straus 1987).
Biometrical data of the Iberian ibex are scarce and partial (Cabrera 1914;
Rodríguez de la Zubia 1969; Cabrera 1985; Escós 1988; Granados et al. 1997,
2001a). Granados et al. (1997, 2001a) studied the basic biometrical parameters
of ibexes from Sierra Nevada and reviewed the biometric data from different
ibex populations (see Table 1). Generally, body size is larger and weight higher
in C. p. victoriae than C. p. hispanica (e.g., Gonçales 1982; Granados et al.
1997; Table 1).
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The Iberian ibex has a remarkable sexual dimorphism, males being
higher in size and weight, and presenting larger horns than females (Fandos
1991; Granados et al. 1997; Table 1). Gállego and Serrano (1998) described
the postcranial skeleton of the species and they showed sex differences in
relation to biometry and bones ossification process. The maximum level of
sexual dimorphism is observed at horn length and basal horn perimeter
(Fandos and Vigal 1993; Granados et al. 2001a). The Iberian ibex horns are
unique among wild caprids, curving out and up and then back, inward, and,
depending of the subspecies, either up again or down (C. p. victoriae and C. p.
hispanica, respectively; see Schaller 1977). Horn shape and fight techniques
were studied by Alvarez (1990). Annual horn growth is influenced by the
previous year horn growth, environmental factors and, principally, by age
(Fandos 1995).
Table 1. Biometric data reported from different ibex populations (updated from Granados et al. 1997). The length measures are in centimetres and the weight is in kilograms (male – female values), “?” symbol show the absence of data.
Body weight
Cross height Body length Horn
length Basal horn perimeter
Albacete Present study 58.4-35.0 ?-? ?-? 55.8-? 23.2-?
Sierra Nevada (Granados et al. 1997) 50.4-31.3 79.3-69.0 108.6-96.9 47.5-13.9 20.7-9.7
(Cabrera 1914) ?-? 65.5-? 121.0-? ?-? ?-? (Cabrera 1985) ?-? 84.1-? 144.0-? ?-? ?-?
(Escos 1988) 65.0-? 65.0-? 132.0-116.0 63.8-19.2 22.7-? Cazorla
(Escos 1988) ?-? 67.2-66.2 128.1-118.2 48.8-13.5 20.1-8.6 (Fandos 1991) 54.9-31.5 81.1-69.7 132.1-112.8 76.0-17.1 ?-?
Gredos (Cabrera 1914) ?-? 70.0-? 135.5-? 73.2-16.5 24.4-10.0
(Gonçales 1982) 90.0-40.0 75.0-65.0 155.0-115.0 ?-? ?-? (Fandos and Vigal 1988) 61.9-36.8 ?-? ?-? 83.7-28.7 ?-?
Las Batuecas (Losa 1993) 78.0-41.0 89.0-76.0 146.0-130.0 74.0-17.0 26.0-11.5
Sierra Morena (Cabrera 1914) ?-? ?-? ?-? 85.0-? ?-?
Pirineos Aragón (Cabrera 1914) ?-? 75.0-? 148.0-? 91.0-26.8 23.0-14.0
C. p. lusitanica (Cabrera 1914) ?-? 74.5-? 142.0-? 42.0-18.0 20.0-? (França 1917) ?-? 69.5-? 140.0-? ?-? ?-?
Pirineos-Gredos (Couturier 1962) 75.0-37.5 ?-? ?-? ?-? ?-?
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Granados et al. (2001a) also studied growth parameters of the Iberian
ibex population of Sierra Nevada. These authors registered a faster female
growth rate, although slower than the ones obtained in other ibex populations
(Fandos et al. 1989; Fandos 1991). This is in agreement with Serrano et al.
(2004) findings, who showed that female ibexes have a faster ossification
process than males, finishing their bone development two years before males
(Serrano et al. 2006).
FEEDING HABITS
The feeding ecology of the Iberian ibex has been studied in several
locations, Sierra Nevada Natural Park (e.g. Martínez 1988a); Cazorla, Segura y
Las Villas Natural Park (e.g. Garcia-Gonzalez and Cuartas 1992; Alados and
Escós 1996); Gredos Regional Park (e.g. Martínez and Martínez 1987); Sierra
de Tejeda-Almijara (Martínez 1988b); Tortosa y Beceite National Game
Reserve (Martínez 1994); and Sierra de Montenegro (Palacios et al. 1978).
The Iberian ibex is a mixed feeder (browser and grazer) varying
seasonally (Garcia-Gonzalez and Cuartas 1992) and geographically (Granados
et al. 2001b) the percentage of each type of resource consumed. Feeding
studies have shown that, when resources are scarce, there is a selection of
certain species (Cuartas and Garcia-Gonzalez 1992; Garcia-Gonzalez and
Cuartas 1992). On the other hand, feeding strategies seasonality was reported
as highly influenced by population density (Garcia-Gonzalez and Cuartas 1992).
The ibex population of Tortosa y Beceite National Game Reserve is
characterized by a remarkable altitudinal gradient in the feeding strategy,
predominating a browsing behaviour at low-middle altitudes and grazing in high
altitude lands (Martínez 1994).
Grazing and browsing behaviours also differ between locations. Thus,
grazing predominates in Gredos Regional Park ibex population (Martínez 2001),
whereas browsing does in Cazorla, Segura y Las Villas Natural Park population,
except in spring time (Martínez et al. 1985). Finally, grazing behaviour has been
registered in Sierra Nevada Natural Park during summer (Martínez 1990).
Tesis Doctoral
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Unfortunately, none of these works have taken into account resources
availability.
Also, the Iberian ibex has been included in a few comparative studies on
wild and domestic ungulates diet (e.g. Garcia-Gonzalez and Cuartas 1989).
Autumn diet comparisons of Iberian ibex, domestic goat (Capra hircus), mouflon
and domestic sheep (Ovis aries) showed than sheep are mainly grazers and
goats browsers (ibid.).
In sum, the Iberian ibex seems to have a high feeding plasticity,
depending on many ecological circumstances; but there is a need for integrating
these results in more ecologically-designed studies, as no hypotheses
explaining such plasticity have yet put forward, such as ibex nutritional
requirements and differences according to sex and age.
BEHAVIOURAL ECOLOGY
Behaviour of the animals can be integrated into the ecological context it
occurs. Among the diverse of topics studied by behavioural ecologists, sexual
segregation is a puzzling one which has stimulated many studies and
hypotheses. In many social ungulates sexes live separately most of the year,
differing in habitat use, particularly those species showing an elevated sexual
size dimorphism. Such segregation has been reported in the Iberian ibex
(Alados 1985b). There are three main hypotheses trying to explain sexual
segregation in ungulates: the predation-risk, forage-selection, and activity
budget hypotheses. They, respectively, relate sexual segregation either to
lactating females' selection of safer habitats; to a differing forage digestion
efficiency made by males and females according to their body size, so that
males may cope better with nutritionally poor habitats; or, finally, to a differing
activity budget between males and females also related to their body size
dimorphism (see Ruckstuhl and Neuhaus 2002). These hypotheses are not
mutually exclusive, and are still under a serious debate.
Although no study testing such hypotheses has been carried out on the
Iberian ibex, a close relative, Alpine ibex (Capra ibex) shows sexual segregation
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according to the three hypotheses. Thus, males are preferentially found in
riskier (Villaret et al. 1997) and poorer habitats than females and both sexes
show a differing percentage of time spent grazing (73%; Ruckstuhl and
Neuhaus 2002).
However, it seems that local conditions play an important role that has
not yet been incorporated into the formulation of sexual segregation
hypotheses. According to the studies carried out on the Iberian ibex, during
most of the year sexes are segregated, there being only-male groups, and
female and offspring-subadults groups, whereas during the rutting season adult
males and females come together (Granados et al. 2001b). However, this
pattern may vary. Thus, in locations such as Cazorla, Segura y Las Villas
Natural Park, Sierra Nevada Natural Park, and Gredos Regional Park, ibexes
are in mixed groups all annual cycle, except in August (Gonçales 1982; Alados
and Escós 1985, 1996). A better knowledge of factors determining sexual
segregation is needed to disentangle this behaviour, which seems not to be so
uncommon in other ungulate species (K. Ruckstuhl, E. Cameron pers. comm.).
One hypothesis raised is the relationship between the optimal group size
attained and males and females densities in a given population (K. Ruckstuhl
pers. comm.). Iberian ibex group size, on the other hand, seems to be
determined by factors such as population density and type of habitat (Granados
et al. 2001b).
Regarding social and individual behaviour in the Iberian ibex, vigilance
behaviour has been studied by Alados (1985c). It was determined that lookout
individuals are adults placed in the periphery of the herds. Ibexes use alarm
calls to alert from potential danger, i.e., the presence of a potential predator.
Escape movements are made in an ordered and coordinated manner, mediated
by the markedly social hierarchies that characterize all the relations and
interactions between herd mates (Alados 1986).
Seasonal partial-migrations are frequent in species inhabiting regions
with pronounced seasonal landscape variability, as it is the case of the Iberian
ibex (Fandos and Martínez 1988). Ibex altitudinal dispersion occurs according
to resources availability, e.g., heading to rich, high altitude areas in summer,
Tesis Doctoral
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which are usually covered by snow in winter (e.g., Gonçales 1982; Escós 1988;
Travesí 1990).
The Iberian ibex dispersive range has been described for Andalusian
populations suggesting 1.8 km per year in Cazorla population (Escós 1988) and
0.7 km per year in Sierra Nevada population (Alados and Escós 1996). The ibex
dispersive capacity is affected by an increase of densities, lost of traditional
agriculture, and habitat improvement (Ibid.).
As for other behavioural studies, the Iberian ibex activity budget has also
been studied by several authors. Thus, higher activity rates were detected at
first and last day hours in Cazorla (Alados and Escós 1988), although this
pattern may vary according to temperature variations (e.g. Fandos 1988). It has
also been reported a seasonal variation of home ranges in this species (Escós
and Alados 1992). Home ranges are smaller during the rutting period than in
spring, depending on resources quality and availability, and ibex population
density (Escós and Alados 1992; Alados and Escós 1996).
EPIDEMIOLOGY AND HEALTH STATUS
The role of diseases on the Iberian ibex population dynamics has been
scarcely studied. The sarcoptic mange produced by Sarcoptes scabiei is the
disease more widely studied in this species (Pérez et al. 1997; León-Vizcaino et
al. 1999). Also, trematode, esporozoe, cestode, nematode and arthropod
parasites, in addition to Sarcoptes, have been studied in Iberian ibex
populations. Good reviews on this subject in Andalusian ibex populations are
Universidad de Jaén (1999), and Granados et al. (2001b) (see Table 2).
More ibex health studies were reported in parasite and eco-pathology
symposiums, such as Groupe d’Etudes sur l’Ecopathologie de la Faune
Sauvage de Montagne, Euro-American Mammal Congress, Congreso Ibérico
de Parasitología, Simposium sobre Gestión de Cabra Montés, including reports
on bacterial and viral diseases. Due to the scarce information available in
symposium abstracts and considering that most of them reported preliminary
results, we have not included them in this review.
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Table 2. Parasites of the Iberian ibex populations from Andalusia. Group (in blood) and species name and prevalence (%) is shown. The capital letters indicate the location of the parasites in the animal, being A: abomasums; I: intestine; BD: bile duct; R: rumen; L: lung; Es: erythrocytes; Ls: leucocytes; D: diaphragm; B: brain, H: head, S: skin (adapted from Universidad de Jaén 1999; Granados et al. 2001b).
Rikettsiae M. occidentalis (7.6), I Anaplasma ovis (4.5), Es Teladorsagia circumcincta (47), I
Ehrlichia phagocytophila (0.9), Ls T. trifurcata (9.1), I Eperytrozoon ovis (1.8), Es T. davtiani (0.3), A
Esporozoe Nematodivirus davtiani alpinus (57.6), I Eimeria arlongi (74.0), I N. oiratianus (56.1), I
E. ninakohlykimovae (6.0), I N. abnormalis (54.5), I E. caprina (5.0), I N. spathiger (3.0), I
E. capraovina (5.0), I N. filicollis (1.5), I E. aspheronica (0.5), I Ostertagia ostertagi (4.5), I E. christenseni (10), I Trichostrongylus vitrinus (4.5), I
E. hirci (1.0), I T. axei (0.5), A E. folchijevi (3.0), I T. capricola (3.0), I Eimeria sp. (0.5), I Trichuris sp. (2.4), I
Sarcocystis sp. (27.4), D Dictyocaulus filarial (1.2), L Babesia ovis (59.8), Es Neostrongylus sp. (31.4), L Theilleria ovis (1.8), Es Muellerius capillaris (74.3), L
Trematode Cystocaulus ocreatus (32.1), L Fasciola hepatica (1.7), BD Protostrongylus sp. (35.2), L
Dicrocoelium dendriticum (0.5), BD Arthropod Parramphistomum sp. (0.5), R Psoroptes sp. (0.6), S
Cestode Trombicula sp. (0.4), S Taenia multiceps (0.3), B Dermacentor marginatus (2.0), S
T. hydatigena (27.1), A D. reticulatus (0.6), S Echinococcus granulosus (0.2), L Haemaphysalis sulcata (32.3), S
Moniezia expansa (8.0), I Ixodes ricinus (4.2), S M. benedeni (7.8), I Rhipicephalus bursa (42.8), S
Avitellina centripunctata (0.2), I Bovicola crassipes (20.2), S Nematode Linognthus stenopsis (1.1), S
Marshallagia marshalli (21.2), I Oestrus caucasicus (62.2), H
The account of scabies epidemiology is characterized by periodic
fluctuations (outbreaks) with cycles ranging from 10 to 30 years, influenced by a
variety of hosts, parasites and external factors (e.g., Pérez et al. 1997; Rossi et
al. in press). During the last few decades, several sarcoptic mange epizootics
have affected ibex populations from, e.g., Cazorla, Segura y Las Villas Natural
Park (Fandos 1991; León-Vizcaino et al. 1999); Sierra Nevada Natural Park
(Pérez et al. 1997); Sierra Magina Range Mountains (Palomares and Ruiz-
Martínez 1993). Recently, another population affected by mange has been
reported, the northern ibex population of Albacete (P. Acevedo and C. Gortázar
unpublished data).
Tesis Doctoral
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When high host densities coincide with limited food availability, high
parasite prevalences can be expected due to a loss of fitness and an increase
of aggregation at the population level (Acevedo et al. 2005a [Capítulo 1.2]; Gortázar et al. 2006). This was apparently the case of the ibex sarcoptic mange
outbreaks in Cazorla, Segura y Las Villas Natural Park (León-Vizcaino et al.
1999) which produced a mortality of over 95% of the population. Nevertheless,
the hypothesis of the transmission of scabies from domestic sheep and goats to
Iberian ibex population has been suggested in the Sierra Nevada population
(Pérez et al. 1997), although no evidence exists. The negative effects of
population overabundance (Caughley 1981; see review in Gortázar et al. 2006)
can be increased by the introductions of exotic and native species, including
domestic species (Richardson and Demarais 1992). These introduced species
may originate two main effects, an increase of diseases abundance and their
transmission rate, and the appearance of new diseases (Hofle et al. 2004; J.
Ortiz pers. comm.). It has been reported a sarcoptic mange episode in free-
ranging exotic aoudads (Ammotragus lervia) in Spain (González-Candela et al.
2004). This exotic species is currently expanding from south eastern Iberian
Peninsula (Cassinello et al. 2004), so that there is a potential risk for it to spread
new diseases that could reach the Iberian ibex populations due to niche overlap
between both species (P. Acevedo, J. Cassinello, J. Hortal and C. Gortázar
unpublished data [Capítulo 3.2]).
Gastrointestinal and bronchopulmonary nematodes have also been
studied in the Iberian ibex populations (e.g., Pérez et al. 2003a; Acevedo et al.
2005a [Capítulo 1.2]). Pérez et al. (2003a) analyzed the content of the
abomasums and small intestine of the population from Sierra Nevada Natural
Park, and identified 15 species of trichostrongylid nematodes, 4 of which found
for the first time in this host. As for bronchopulmonary nematodes, they were
recently surveyed in the ibex population of Castile-La Mancha (Acevedo et al.
2005a [Capítulo 1.2]). The infective larval stages in faeces were analysed, a
non-invasive alternative technique to study host-parasite relationships in wild
ungulate populations (Festa-Bianchet 1991). Acevedo et al. (2005a [Capítulo 1.2]) identified 5 genera of bronchopulmonary nematodes and supported that
Introducción
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density-dependent processes operate in the transmission of these nematodes
in the Iberian ibex.
More sanitary studies should be implemented to unravel the health status
of the Iberian ibex populations, especially in regard to viral and bacterial
diseases, in order to carry out a proper population management. Currently, a
few regional governments are promoting projects on this issue, so that in the
next years ibex epidemiology advances are expected.
Finally, haematology parameters were recently studied and its references
values reported for the Iberian ibex (Pérez et al. 2003b). The variation in these
parameters were studied under diverse stress situations: influence of capture
methods and captivity (Peinado et al. 1993, 1995), acute haemonchosis (Lavín
et al. 1997), infection by Sarcoptes scabiei (Pérez et al. 1999) and hunting
practises (Pérez et al. 2006). In addition, values from blood parameters can
provide useful information about the health and nutritional status of animals,
being also a complementary source of information for monitoring the
physiological status of ibex populations (Pérez et al. 2006).
CONSERVATION
Most Caprinae populations are particularly vulnerable to extinction
because of three main factors: genetic isolation, specialised habitat
requirements, and a low reproductive rate (Shackleton 1997). However, there
are additional factors which interact with these to further complicate
conservation aims.
Shackleton (1997) stated that 71% of the species included in the
subfamily Caprinae are suffering some type of threat, from which 8% are in a
critical situation; 23% threatened; 40% vulnerable; and 28% under a threaten
risk; whereas 1% of the species are insufficiently known.
In Spain, Caprinae conservation programs began in 1905 to preserve the
last remaining population of C. p. victoriae, through the establishment of the
National Refuge of Sierra de Gredos as well as a few more other reserves
Tesis Doctoral
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created to protect caprids (Alados 1997). Alados (1997) considered that the
future of the Iberian ibex depends on developing effective conservation
programs and consolidating the existing protected areas. Two main threats to
ibexes are considered (Alados 1985a, 1997): (1) the increasing presence of
domestic livestock, which might transmit diseases to wild ungulates (see
examples in Gortázar et al. 2006) and compete for resources (Acevedo et al.
2006 [Capítulo 1.1]); and (2) pressure from tourism, an issue currently under
study in Sierra Nevada population (R. Soriguer, personal communication).
These threats can be overcome by establishing management measures to (1)
control the number and health status of livestock, (2) restrict or control tourists'
presence in areas inhabited by ibexes, (3) protect large areas from hunting
when the population size do not permit a sustainable exploitation, and (4)
establish a proper monitoring of ibex populations.
Last report of the World Conservation Union (IUCN 2004) considers C.
pyrenaica as at Low Risk, but near threatened (LR/nt), whereas the existing
subspecies hold different qualifications. C. p. victoriae is Vulnerable (VU D2),
due to the few and small areas it inhabits (see Pérez et al. 2002); C. p.
hispanica is at Low Risk (LC/cd), but its viability depends on current
conservation programmes. Two other subspecies were also distinguished (see
above), but they are extinct nowadays, C. p. pyrenaica and C. p. lusitanica
(ibid).
FUTURE DIRECTIONS OF CAPRA PYRENAICA RESEARCH
The present review has shown that the Iberian ibex current knowledge is
basically focused on some aspects of its behavioural ecology, feeding habits
and diseases. Although descriptive and poorly integrated studies predominate.
We firstly appreciate that most studies and empirical information on the
Iberian ibex is currently produced by regional institutions that carry out
periodical surveys on the species status, mainly in protected areas. It would be
desirable that this kind of valuable information is not retained in poorly
accessible files and local reports, so that promoting contacts between
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managers, forest rangers and environmental agencies and research institutes
should be pursued. This would allow researchers to centralize all the available
diverse information and design adequate research projects.
Concerning new lines of research for the Iberian ibex, it would be
important to identify which aspects on its biology and conservation is a priority,
given current status of the species. We believe that applied ecological studies
should not be overlooked, given that the species, although under an expansion
process, may suffer from competition with other ungulate species (e.g., red
deer, fallow deer, aoudad and livestock; see references above) and has a
markedly hunting interest. Its former sarcoptic mange episodes should also
make to be cautious on overabundance instances in some particular areas.
Moreover, in areas recently colonized by the species, its effects on endemic
flora should also be analysed. Finally, verifying genetic differences between the
assumed subspecies will help in attaining proper conservation and
management steps to preserve their whole genetic pool, as some valuable
populations may be under threat (e.g., C. p. victoriae).
Population management from conservation and game interests should
also be pursued. Currently Iberian ibex trophies may represent an important
economic revenue, and biological features, such as factors affecting horns
growth (e.g., body condition, immune system, age), and the determination of the
genetic breeding value of large-sized horned males, will help in attaining a
sustainable wildlife management, adjusting hunting quotas in such a way that
removing 'valuable' males is prevented.
Finally, less applied but equally valuable studies devoted to natural
history issues should also be implemented in the light of current knowledge. In
sum, the available information on the species should be centralised and its
progress monitored from scientific criteria. It would be useful to carry out a
meeting of specialists to share their views and establish the necessity of a
scientific approach in conservation and management practises.
To our view, the following research topics should be implemented in the
near future to widen our knowledge of the Iberian ibex: applied ecological
studies, identify proper management strategies to preserve ibex populations
Tesis Doctoral
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(evaluation of census methods of mountainous caprids to improve their
efficiency and accuracy, and monitor health status of the populations to identify
disease risks), and other conservation studies (interspecific relationships with
exotic, other autochthonous, and domestic ungulates, and genetic studies to
clarify the still controversial taxonomy of the species).
ACKNOWLEDGEMENTS
We are deeply indebted to all Rural Agents of the Environment Agency of
Castilla-La Mancha. C. Cano and A. Alguacil provided us data on Albacete
population, and J.E. Granados and R. Soriguer provided us of uneasy available
bibliography. JC is currently enjoying a Ramón y Cajal research contract at the
CSIC awarded by the Ministerio de Educación y Ciencia (MEC); he is also
supported by the project PBI-05-010 granted by Junta de Comunidades de
Castilla-La Mancha. PA is enjoying a grant from the Universidad de Castilla-La
Mancha.
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Introducción
________________________________________________________________ 52
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OBJETIVOS Y ORGANIZACIÓN DE LA TESIS
Tesis Doctoral
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OBJETIVOS
En esta Tesis Doctoral se ha pretendido profundizar en el conocimiento
de la cabra montés, especialmente sobre su distribución, y las relaciones entre
ésta y la de otros ungulados con los que cohabita. Es por tanto una
investigación aplicada que pretende mostrar la utilidad de nuevas herramientas
de análisis espacial para la gestión de las poblaciones de ungulados. Con las
herramientas empleadas para el desarrollo de la presente Tesis, se pueden
responder preguntas relevantes para el manejo de las poblaciones de
ungulados en libertad: ¿Cuál es el potencial ambiental que presenta un
territorio para una especie? ¿Se puede acelerar el proceso expansivo de una
especie mediante reintroducciones? ¿Son similares los requerimientos
ecológicos de dos o más especies?
Por otro lado, este trabajo tiene una clara vertiente conservacionista que
va de la mano con la anterior. Una de las necesidades de la conservación es
preservar los ecosistemas singulares o característicos de una determinada
área biogeográfica. Estos ambientes poseen un gran valor ya que han co-
evolucionado con las especies que los habitan y sin ellos, o sin su correcta
gestión, las especies pueden ver limitadas sus posibilidades para el
mantenimiento de poblaciones estables. En este contexto, se han caracterizado
los requerimientos ambientales de ungulados endémicos de la península
Ibérica, como son la cabra montés y el ciervo ibérico, con el fin de conocer su
nicho ecológico y poder conservarlo. Por otro lado, se ha estudiado la
potencialidad ambiental que presenta la zona de estudio para un ungulado
exótico, el arrui, lo que permitirá poseer información sobre las zonas en las que
es esperable que esta especie, que se puede considerar invasora, llegue a
colonizar. Con todo ello, se pretenden conocer las relaciones espaciales que
existen, o se pueden llegar a establecer, entre especies tanto nativas como
introducidas, y la cabra montés, considerando a ésta última como una especie
endémica con gran valor conservacionista y económico en el centro-sur de la
Península Ibérica.
Hasta este trabajo, sólo había sido realizado un análisis sobre la
distribución potencial de la cabra montés. El vacío existente en esta línea de
investigación, no sólo en la cabra montés sino en los ungulados ibéricos en
Introducción
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general, y la necesidad de este tipo de estudios para la correcta gestión y
conservación de las poblaciones, han sido los factores que han impulsado a la
realización de esta Tesis Doctoral. El objetivo general de esta Tesis es, pues,
identificar y caracterizar el nicho ecológico de la cabra montés, así como
las relaciones de nicho existentes entre las monteses y los ungulados
presentes en su área de distribución con los que puede competir. Para
abordar esto, se han planeado las siguientes etapas.
Inicialmente se ha diseñado un muestreo con el fin de actualizar la
distribución y conocer el estatus de las poblaciones de cabra montés de
Castilla-La Mancha, ya que aunque poblaciones de cabra como las de
Andalucía y, en menor medida, Gredos han sido muy estudiadas, las
poblaciones de otras áreas, como Castilla-La Mancha, han estado menos
seguidas. En este análisis también han sido considerados aspectos sanitarios
de la cabra enmarcados en la evaluación del estatus poblacional.
Una vez actualizada la distribución y estatus en esta región, se ha
pretendido estudiar el efecto que otras especies, tanto exóticas como
introducidas, tienen o pueden tener sobre el nicho ecológico de la cabra
montés. Para ello se ha considerando al ganado caprino -como ejemplo de
especies cuya ocupación del medio suele ser temporal-, al ciervo –como
modelo de especies que han sido introducidas en numerosas localidades-, y al
arrui -debido a su carácter exótico e inminentemente invasor-.
Debido a que el hábitat donde pastorean al ganado caprino y el de las
cabras monteses coincide en numerosas ocasiones, se ha pretendido evaluar
el efecto que las especies domésticas pueden tener sobre el uso que las
silvestres hacen del hábitat. Este objetivo se ha llevado a cabo considerando
sólo las poblaciones de Castilla-La Mancha debido a que sólo de ellas se
poseía toda la información necesaria para realizar este análisis.
Siguiendo con el planteamiento anteriormente expuesto, se ha
pretendido evaluar el efecto que tienen las introducciones de animales en la
expresión de su nicho ecológico, esto es, ¿mantiene la especie en el área
donde es introducida el mismo nicho ecológico que expresa en las áreas donde
es autóctona?, y de no ser así, ¿las modificaciones en el nicho pueden
Tesis Doctoral
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ocasionar que se produzca un solapamiento con el de otra especie autóctona?
El tema de las introducciones y reintroducciones de ungulados es de gran
importancia, tanto para la gestión del medio como de las especies autóctonas,
ya que éstas son prácticas habituales en la mayor parte de la Península Ibérica.
Numerosas especies han visto modificado su área de distribución con estas
acciones, y sin embargo, sus implicaciones ecológicas apenas han sido
consideradas.
Ya por último, y en esta misma dirección, se ha pretendido evaluar el
efecto que los ungulados exóticos pueden tener sobre la distribución de una
especie nativa, considerando para ello al arrui, ya que es una especie que ha
sido introducida en la península hace más de 30 años. Además, y de manera
preliminar al objetivo anterior, se ha pretendido evaluar el potencial ambiental
del área de estudio para una especie que proviene de ambientes radicalmente
distintos, como son los macizos del norte de África. El arrui continúa en
expansión desde su introducción en Sierra Espuña, y ha empezado a cohabitar
con la cabra montés hace ya unos años.
Para abordar los tres últimos objetivos expuestos, el área de estudio
seleccionada ha sido el sureste de la Península Ibérica, un territorio en el que
quedan englobados núcleos de cabra montés de gran importancia (Sierra
Nevada y Cazorla, Segura y Las Villas, entre otros), núcleos donde el ciervo es
autóctono (Sierra Morena oriental), donde es introducido (por ejemplo Cazorla y
núcleos aislados de la provincia de Albacete), y la mayor parte del área de
distribución del arrui.
A modo de resumen, se enumeran a continuación los objetivos
planteados en la presente Tesis:
1. Actualizar la distribución y conocer el estatus de las poblaciones de
cabra montés de Castilla-La Mancha.
2. Evaluar el efecto que las especies domésticas pueden tener sobre el
uso que las especies silvestres hacen del hábitat.
3. Evaluar el efecto de las introducciones de ungulados en la expresión
del nicho ecológico de la especie introducida, así como las
implicaciones de las introducciones sobre otras especies.
Introducción
________________________________________________________________ 58
4. Evaluar la potencialidad ambiental del área de estudio para una
especie que proviene de ambientes radicalmente distintos.
5. Evaluar el efecto que los ungulados exóticos pueden tener sobre la
distribución de una especie nativa.
Estos objetivos quedan abordados en los próximos capítulos según se
detalla a continuación.
ORGANIZACIÓN DE LA TESIS
En el Capítulo 1 se ha pretendido actualizar la distribución de cabra
montés en Castilla-La Mancha, así como conocer el estatus de sus poblaciones
y la relación entre la presencia de ganado caprino y el uso que las cabras
monteses hacen del medio. Para ello, se ha realizado un muestreo que
comienza con el diseño de una encuesta sobre distribución de ungulados en
Castilla-La Mancha y que ha sido dirigida a los Agentes Medioambientales de
la Junta de Comunidades de Castilla-La Mancha. Buena parte de los datos de
distribución obtenidos han sido confirmados con visitas al campo en las que se
ha aprovechado para estimar la abundancia relativa de las poblaciones
mediante indicios de presencia, así como para obtener muestras de
excrementos con el fin de poder obtener un aproximación al estado sanitario de
las mismas. Con toda esta información se han planteado dos publicaciones con
las que los objetivos 1 y 2 han quedado cubiertos.
El siguiente capítulo está dedicado al estudio de la influencia de las
introducciones de ungulados sobre la expresión del nicho ecológico de las
especies. En este caso se ha usado como modelo el ciervo ibérico (Capítulo 2).
Para ello, se han considerado dos poblaciones de ciervo en relación con su
origen, una población autóctona, la de Sierra Morena, y una población fruto de
reintroducciones que está más ampliamente distribuida por el área de estudio.
Esta clasificación de las poblaciones se ha realizado basándose en un trabajo
publicado a finales de los 80, en el que queda manifestado esta diferencia de
Tesis Doctoral
________________________________________________________________ 59
origen, así como en muestreos de campo y en las encuestas de distribución
descritas en el Capítulo 1. Paralelamente se ha pretendido analizar si el
solapamiento de las áreas de distribución de ciervo y cabra montés, observado
actualmente en algunas áreas, se hubiera producido sin las reintroducciones, o
si estos altos solapamientos son fruto exclusivo de estas acciones mediadas
por el hombre. Este estudio forma parte de un artículo enviado a publicar con el
que el objetivo 3 queda resuelto.
Por último, en el Capítulo 3 se pretenden abarcar los objetivos 4 y 5.
Para ello se ha evaluado el potencial ambiental del área de estudio para una
especie exótica, el arrui, considerando el efecto que supone la transformación
humana del medio para la distribución potencial de esta especie. En este caso
los datos de distribución del arrui provienen de un artículo publicado en 2004
en el que aparecen citas sobre la presencia de la especie obtenidas mediante
muestreos de campo y entrevistas personales. Con ellas, se pretende
modelizar por un lado el nicho ambiental de la especie, considerando
únicamente variables ambientales, y por otro el nicho observado para el que se
han considerado tanto variables ambientales como antrópicas. Ambos nichos
han sido comparados y se ha podido evaluar el efecto que las alteraciones
humanas pueden tener sobre la distribución potencial de este ungulado exótico.
Por otro lado, y debido a lo proximidad taxonómica, era esperable que el arrui y
la cabra montés pudieran ocupar nichos ecológicos similares dentro del área de
estudio. Por ello, se han descrito los nichos de ambas especies y se han
comparado ambos con el fin de detectar las diferencias y similitudes que
pudieran existir. Además de éstos, se han obtenido las áreas de potencial
coexistencia de ambas especies y éstas también han sido caracterizadas
ambientalmente y comparadas sus peculiaridades ambientales por un lado con
las del nicho del arrui, y por otro el de la cabra.
Estos capítulos tienen formato estándar de artículo científico, están en
inglés, e incluyen un resumen en castellano al principio de cada uno. La Tesis
se cierra con un capítulo en castellano de síntesis y conclusiones (Capítulo 4),
en el que se resumen los resultados más significativos.
A continuación se enumeran los artículos científicos que componen la
presente Tesis Doctoral:
Introducción
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1. Acevedo, P., Cassinello, J. A review of Capra pyrenaica knowledge:
taxonomy, distribution, ecology, conservation and proposal for future
research lines. Mammal Review, en evaluación (enviado a 3/08/2006).
[Introducción].
2. Acevedo, P., Cassinello, J., Gortázar, C. (2006) The Iberian ibex is under
an expansion trend but displaced to suboptimal habitats by the presence
of extensive goat livestock in central Spain. Biodiversity and
Conservation. DOI 10.1007/s10531-006-9032-y [Capítulo 1.1].
3. Acevedo, P., Vicente, J., Alzaga, V., Gortázar, C. (2005) Relationship
between bronchopulmonary nematode larvae and relative abundances of
Spanish ibex (Capra pyrenaica hispanica) from Castilla-La Mancha.
Journal of Helminthology 79, 113-118 [Capítulo 1.2].
4. Acevedo, P., Cassinello, J. Human-induced expansion of wild ungulates
may facilitate niche overlap of taxonomically distant species. Journal of
Biogeography, en evaluación (enviado a 29/09/2006) [Capítulo 2].
5. Cassinello, J., Acevedo, P., Hortal, J. (2006) Prospects for population
expansion of the exotic aoudad (Ammotragus lervia; Bovidae) in the
Iberian Peninsula: clues from habitat suitability modelling. Diversity and
Distributions 12, 666-678 [Capítulo 3.1].
6. Acevedo, P., Cassinello, J., Hortal, J., Gortázar, C. Is introduced exotic
aoudad (Ammotragus lervia) a threat to native Iberian ibex (Capra
pyrenaica)? A habitat suitability model approach. Diversity and
Distributions (enviado a 24/10/2006) [Capítulo 3.2].
CAPÍTULO 1
1.1.- EL PROCESO DE EXPANSIÓN DE LA CABRA MONTÉS EN CASTILLA-LA MANCHA, Y SU DESPLAZAMIENTO HACIA HÁBITATS SUBÓPTIMOS POR LA PRESENCIA DE GANADO CAPRINO 1.2.- RELACIONES ENTRE LA EXCRECIÓN DE NEMATODOS BRONCOPULMONARES Y LA ABUNDANCIA RELATIVA DE CABRA MONTÉS (CAPRA PYRENAICA HISPANICA) EN CASTILLA-LA MANCHA
DISTRIBUCIÓN Y ESTATUS DE LAS POBLACIONES DE CABRA MONTÉS (CAPRA PYRENAICA HISPANICA) EN CASTILLA-LA MANCHA
1.1.- EL PROCESO DE EXPANSIÓN DE LA CABRA MONTÉS EN
CASTILLA-LA MANCHA, Y SU DESPLAZAMIENTO HACIA HÁBITATS
SUBÓPTIMOS POR LA PRESENCIA DE GANADO CAPRINO
Acevedo, P., Cassinello, J., Gortázar, C. (2006) THE IBERIAN IBEX IS UNDER AN
EXPANSION TREND BUT DISPLACED TO SUBOPTIMAL HABITATS BY THE PRESENCE OF
EXTENSIVE GOAT LIVESTOCK IN CENTRAL SPAIN. Biodiversity and Conservation. DOI
10.1007/s10531-006-9032-y.
Tesis Doctoral
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RESUMEN
En el presente trabajo se ha actualizado el área de distribución de la cabra
montés (Capra pyrenaica, Schinz 1838) en Castilla–La Mancha, España central. La
especie está presente en el 19% de la región, y se ha detectado en áreas donde no
había sido citada anteriormente. Paralelamente, se ha realizado un análisis de
adecuación de hábitat aplicando una nueva metodología, el Análisis Factorial de Nicho
Ecológico, que precisa tan solo de datos de presencia para calcular la adecuación del
hábitat para una especie dada. Debido a que la ganadería es una actividad importante
en la región, la presencia de ganado caprino (Capra hircus) ha sido incluida en los
análisis, ya que potencialmente puede competir con las monteses. Los factores que
afectan a la abundancia relativa de cabra montés han sido determinados mediante una
regresión múltiple anidada, utilizando como factor anidado la presencia/ausencia de
ganado caprino. La presencia de cabras domésticas tuvo un efecto negativo sobre la
abundancia relativa de las monteses, causando que las últimas seleccionaran áreas
con menos matorral y más zonas cultivadas y bosques, mientras que en ausencia de
caprino, las cabras monteses estaban presentes principalmente en zonas de pastos y
matorral, con ausencia de cultivos. Finalmente se discuten las implicaciones de estos
resultados para la conservación en el contexto de una región mediterránea en la que
abundan los sistemas de ganadería extensiva.
ABSTRACT
In this paper an updated distribution of the Iberian ibex (Capra pyrenaica,
Schinz 1838) in the central Spanish region of Castile–La Mancha is shown. The
species is present in 19% of the study region, and in areas not cited so far in the
literature. A detailed analysis of habitat suitability was also carried out, applying a new
methodology, Ecological-Niche Factor Analysis, which uses presence data to build a
habitat suitability map of a given species. As livestock activity is quite intense in the
region, the presence of a potential competitor, the domestic goat (Capra hircus), was
included in the analyses. Factors affecting ibex relative abundance were determined by
means of a nested stepwise multiple regression, where livestock presence/absence
was the nested factor. The presence of livestock has a negative effect on ibex relative
abundance, causing the ibex to select areas of poor, sparse vegetation, cultivated
lands and forests, whereas in the absence of livestock, the ibex is mainly present in
Capítulo 1
________________________________________________________________ 66
pasture–scrub lands and non-cultivated lands. Conservation implications of these
results are discussed in the context of a Mediterranean region where extensive
livestock grazing systems abound.
INTRODUCTION
To conservation biologists it is of particular interest to determine the
effects of invasive species on the natural history of autochthonous ones (see
Lodge 1993). A particular example is that of exotic ungulates introduced in
areas where they can potentially compete with native ones (see, e.g.,
Cassinello et al. 2004). Among the former, livestock represent a particular
instance (Voeten and Prins 1999), usually underestimated by conservation
biologists (Fleischner 1994). Although livestock graze more than one-third of the
world’s land area, and in many instances share resources with native ungulates
(see de Haan et al. 1997), evidences of a negative impact on the latter are not
conclusive and highly debated (e.g., Saberwal 1996; Mishra and Rawat 1998;
Madhusudan 2004; Young et al. 2005).
The development of large, relatively permanent, agriculture-based
societies was the primary event initiating livestock domestication about 10,000
years ago (Price 2002). With a few exceptions, ungulate domestication (e.g.
cattle, sheep and goats) mainly began in the Near East (Troy et al. 2001). The
presence of livestock in Europe goes back to Neolithic times, domestic sheep
and goats showing up particularly in Mediterranean countries (see, e.g., Martín
Bellido et al. 2001).
The status and distribution of the Iberian ibex have been studied by
several authors, either in the whole peninsula (e.g. Granados et al. 2002; Pérez
et al. 2002) or in some particular areas (e.g. Palomares and Ruiz-Martínez
1993; Lasso de La Vega 1994; Pérez et al. 1994; Granados et al. 1998;
Gortázar et al. 2000). Concerning Castile-La Mancha region, in central Spain,
Granados et al. (2002) indicate that the ibex is distributed exclusively in 11% of
the region, whereas Pérez et al. (2002) distinguish 51 ibex population nuclei in
Spain, out of which only 4 were located in Castile-La Mancha: Serranía de
Cuenca, Cabañeros National Park, Sierra de Alcaraz (connected to the well
Tesis Doctoral
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established ibex population of Sierra de Cazorla, Segura y Las Villas Natural
Park, it is supposedly in expansion), and Sierra Madrona (a series of
fragmented nuclei connected to other ones in Sierra Morena, Jaén province).
Here, we analyse the current distribution and habitat use of the Iberian
ibex (Capra pyrenaica Schinz 1838) in Castile-La Mancha. We have considered
it appropriate to use a political division to define our study area because in
Spain conservation field is partly ruled by regional governments. This region is
characterized by an intense livestock breeding activity, namely extensive sheep
and goat grazing systems (see Martin Bellido et al. 2001). We have, thus,
included in our analyses the presence of the domestic goat (Capra hircus), a
close relative of the Iberian ibex and, therefore, expected to share feeding
habits and ecological requirements with it; to our knowledge, no comparative
studies of diet and/or spatial niche use have been made so far. Sheep, on the
contrary, show a differing feeding behaviour (Martínez 2002) and probably their
potential as competitor of the Iberian ibex is less pronounced.
The spatial prediction of species distribution is an important tool for
conservation biology and management planning (e.g., Hortal et al. 2005;
Whittaker et al. 2005). Developments of ecological and biogeographic theories
have been translated into different methodologies, which are able to predict the
distribution ranges and habitat suitability of species (see Guisan and
Zimmermann 2000; Ferrier et al. 2002; Scott et al. 2002), using a wide variety of
statistical approaches and Geographical Information Systems tools (GIS) (e.g.,
Austin 2002; Rushton et al. 2004). The use of a Digital Elevation Model (DEM)
constitutes a basis for generating maps of environmental variables (see Guisan
and Zimmermann 2000), as it has basic outcomes, such as altitude, slope or
aspect, which influence the distribution of the organisms. Furthermore, the use
of digitalised land information database, allows a more detailed analysis of
factors determining species distribution.
Predictive models can easily be made from data of the presence and
absence of a given species (e.g., Osborne and Tigar 1992; Brito et al. 1999).
Nevertheless, it is necessary to distinguish true absences from a mere lack of
information (Thuiller et al. 2004; Araújo et al. 2005). The determination of true
absences of a given species in a given area is the main problem of many
Capítulo 1
________________________________________________________________ 68
animal presence/absence data sets (Hirzel et al. 2002; Zaniewski et al. 2002).
Thus, some techniques incorporate presence-only data (Hortal et al. 2005),
such as the relatively novel Ecological Niche Factor Analysis (ENFA) (Hirzel et
al. 2002). ENFA is used to determine habitat suitability starting from the location
of presence-only data. These maps are the result of the location of a given
species within the multidimensional environmental area that is defined by
considering all mapping units within the study area (Guisan and Zimmermann
2000). These habitat suitability maps indirectly reveal the species potential
distribution (Hirzel et al. 2002). This approach is recommended when absence
data are not available (most data banks), unreliable (most cryptic or rare
species) or meaningless (invaders) (Hirzel et al. 2001), the subsequent results
are to be handled with caution (e.g., Brotons et al. 2004; Engler et al. 2004).
Using these data, this method characterizes the realized niche of the species
from a set of environmental predictors. Thus, an application of the method could
be interesting in many domains: landscape management for endangered
species, better knowledge of unknown or inaccessible areas, or also better
knowledge of ‘new species’ ecology and/or distribution (e.g. Reutter et al. 2003;
Gallego et al. 2004; Chefaoui et al. 2005). This method was originally assessed
in the Alpine ibex (Capra ibex) (Hirzel et al. 2002), but is currently widely used
(see a list of publications at http://www2.unil.ch/biomapper/bibliography.html).
Apart from an updated distribution of the Iberian ibex in Castile-La
Mancha, our aim in this study is to carry out a detailed analysis of habitat
suitability of the species and determine which factors affect its abundance
taking into account the influence of livestock presence/absence.
MATERIALS AND METHODS
The study area
Located in central Spain, it corresponds with Castile-La Mancha political
division (U.T.M. 30S 294,348-681,063 4,208,706-4,575,340), which is placed at
the southern plateau of the Iberian Peninsula. Politically, the region is
conformed of five provinces (see Figure 1), where the study species is
Tesis Doctoral
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distributed unevenly. Castile-La Mancha is the Iberian region where game
activity is more intense. It has a surface area of 79,226 Km2, which represents
15.7% of the whole Spanish territory. The area devoted to game activity in this
region is 70,000 Km2 (88% of its territory), big game estates occupying 19,000
Km2 (Junta de Comunidades de Castilla–La Mancha,
http://www.jccm.es/medioambiente/mednat/cazapesca.htm).
The study region shows a typical Mediterranean continental climate, with
dry periods both in summer and winter, rains concentrated in autumn and
spring, and extreme temperatures during the hottest (summer) and coldest
(winter) seasons. Mediterranean woodland vegetation is present and it is
formed of oak trees (Quercus ilex) along with shrubs of different species (e.g.,
Q. coccifera, Pistacia lentiscus, Cistus spp., Rosmarinus officinalis, etc.). Open
lands with scattered trees (evergreen oak savannah like habitats), the so-called
“dehesas”, are also common. In addition, pine woodlands (Pinus spp.) can also
be found in some elevated areas.
Figure 1. Situation of the study area (Castile-La Mancha region in central Spain), the administrative provinces concerned, and its division in 10x10 grids, showing the presence/absence of the Iberian ibex.
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Apart from the Iberian ibex, other ungulate species that can be found
free-ranging in the study area are wild boar (Sus scrofa) and red deer (Cervus
elaphus), and to a lesser extent fallow deer (Dama dama), and roe deer
(Capreolus capreolus) (see, respectively, Rosell and Herrero 2002; Carranza
2002; Braza 2002; San José 2002).
The study species
The Iberian ibex is a wild goat endemic to the Iberian Peninsula. The
IUCN (2004) considered it as at Low Risk, but near threatened (LR/nt), whereas
the existing subspecies hold different qualifications. C. p. victoriae Cabrera,
1911 is Vulnerable (VU D2), due to the few and small areas it inhabits (see
Pérez et al. 2002). C. p. hispanica Shimper, 1848 is at Low Risk (LC/cd), but its
viability depends on current conservation programmes. This latter subspecies is
widely distributed compared to the former one (ibid). Two other subspecies
were also distinguished, but they are extinct nowadays: C. p. pyrenaica Schinz,
1838 and C. p. lusitanica Schlegel, 1872 (ibid). However, the distinction of these
subspecies has been questioned by Manceau et al. (1999), who found no
genetic differences between the two existing subspecies.
The sampling method
Presence of ibexes in the study area was assessed by means of direct
field observations and by carrying out surveys (n=149) addressed to forest
rangers and staff from environmental agencies of the government of Castile-La
Mancha region. Information obtained by other naturalists was verified by visiting
areas where ibexes were reported. The sampling units were 10x10 km UTM
grid cells (n=905).
Survey addressees were asked to draw in a map their work area and the
range occupied by the Iberian ibex, red deer, wild boar and livestock. A
questionnaire was given to them, where they indicated the status of the
populations present, such as the largest group size registered, a straightforward
variable, easy to account for by field watchers.
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In order to assess ibex abundance, we firstly relied on forest rangers and
environmental managers’ indication of the largest group size registered. The
Iberian ibex is characterized by sexual segregation through most of the year,
but the largest group sizes are attained during the mating season (November-
December) according to Granados (2001), when ibexes are also more
conspicuous. We have confirmed that group sizes given in the questionnaire
refer to mixed groups observed during the mating season, when they may
reflect population abundance in species showing sexual segregation (see Toigo
et al. 1996). In addition, we validated these data by carrying out our own field
surveys.
During September 2003, we performed 17 field surveys consisting of line
transects (e.g., Burnham et al. 1980), a methodology widely used to estimate
relative abundance of wild goats (e.g., Pérez et al. 1994; Alados and Escós
1996). Average length of line transects was 3 km., and they were carried out in
the main areas where the Iberian ibex is present in Castile-La Mancha, and
during hours of maximum activity, i.e. at dawn and at dusk (e.g., Alados 1986).
We only registered female groups, and used these data to test whether the
largest group size obtained in the questionnaire was a good estimate of ibex
abundance (see Results).
Habitat suitability
The ENFA computes a habitat suitability model by comparing the
ecogeographical variables (EGVs) which characterize the locations where the
species is detected with those present in the whole study area (Hirzel et al.
2002).
Habitat suitability for the Iberian ibex was assessed in the area where the
species was more abundant according to the surveys, using 1x1 km UTM grid
cells. Twenty-seven EGVs were defined, including topographical features (e.g.
altitude, slope), land cover, and livestock presence (see Table 1), and
normalized by a Box-Cox transformation (Sokal and Rohlf 1981). We did not
considered climatic variables because of the relative homogeneity of the study
area on this matter, where only slight differences can be registered, mainly due
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to topographic variations. Average distances to each land cover classes were
calculated for each sample unit by means of “Distance Operator” tool (Idrisi32
v.32.21) (see Hirzel et al. 2002). The topographic data from a digital elevation
model (DEM) carried out by the Shuttle Radar Topography Mission (European
Environment Agency 2000), with a spatial resolution of 90 m., was extracted by
overlaying the DEM with the cells of 1x1 km. in a geographic information system
(Idrisi32 v32.21) (see Hortal et al. 2001).
Firstly, the ENFA was run, by means of BioMapper software (Hirzel et al.
2001, 2004; see http://www.unil.ch/biomapper/). It computes a global
marginality coefficient, expressing how, on all the EGVs, the species average
differs from the global average, and a global specialization coefficient,
expressing the ratio of global variance to species variance.
Formally, marginality is defined as the absolute difference between the
global mean and the species mean, divided by the standard deviations of the
global distribution multiplied by a constant (see Hirzel 2001 for details). A value
close to one means that the species lives in a very particular habitat relative to
the reference set. Similarly, specialization is defined as the ratio of the standard
deviation of the global distribution to that of the study species (Hirzel 2001). A
randomly-chosen set of cells is expected to have a specialization of one, while
any value exceeding that score indicates some form of specialization.
The factor coefficients for the marginality factor account for the
marginality of a given species in each EGV considered. It is measured as units
of standards deviations of the global distribution. The higher the absolute value
of a coefficient, the further the species departs from the average value of a
given EGV. There are other factors which express a degree of specialization,
where the higher the value, the more restricted is the range of the study species
on the corresponding variable (Hirzel 2001).
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Table 1. Ecogeographical variables (EGVs) used in the ENFA. Average values in the study region are shown (global mean), together with the standardized ones, as provided by ENFA, in areas where the Iberian ibex is present (species mean). All values are in metres, except for orientation, which is in degrees.
Codes Meaning Global mean
Species mean
TOPOGRAFIC altitud_max Maximum altitude 507.24 0.95
aspect Average orientation 98.49 0.87 slope Average slope 2.82 1.44
CULTURES dist_agriculture Average distance to cultivated lands 2260.56 0.82 dist_agroforest Average distance to agroforest lands 11990.41 1.22
dist_annual_crops Average distance to annual crops 19572.28 0.63 dist_complex_cult Average distance to complex cultures 1933.19 0.64 dist_perm_irrigate Average distance to irrigated cultures 1368.97 0.42
FRUIT TREE dist_fruit_tree Average distance to fruit tree cultures 4249.16 0.15
dist_olives Average distance to olive tree cultures 5388.66 0.04 dist_vineyards Average distance to vineyards 4714.15 1.25
WOODLAND dist_broad_leav Average distance to broad leaves forests 4828.36 1.05
dist_mixed_forest Average distance to mixed forests 6194.78 0.72 dist_connifeous Average distance to conniferous forests 3021.63 -0.34
dist_wood_scrub Average distance to wood-scrub ecotones 1509.38 0.81 dist_sclerophyllous Average distance to sclerophyllous areas 1421.79 0.34
SCRUBLAND dist_moors_heath Average distance to moors and heaths areas 29133.07 0.56
GRASSLAND dist_natu_grass Average distance to natural grass lands 2706.51 0.39
SPARSE VEG. dist_sparse_veg Average distance to sparse vegetation 12196.57 -0.32 dist_bare_rocks Average distance to bare rocks areas 24583.19 -0.05
INFRASTRUCTURE dist_village Average distance to villages 3217.65 0.84 dist_industr Average distance to industrial areas 11612.99 1.07
dist_road_rail Average distance to roads and rails 27601.89 0.74 WATER
dist_river Average distance to rivers 10852.34 -0.09 dist_inland_marshes Average distance to inland marshes 20417.79 1.38
dist_water_bodies Average distance to water bodies 14409.52 0.09 LIVESTOCK
dist_goat_livestock Average distance to goat livestock 2515.05 0.07
Habitat use
Information obtained from the surveys was registered in 10x10 km. UTM
grid squares (n=905) by means of Idrisi32 v32.21 software (Clark Labs, Clark
University). For each UTM square the frequency of occurrence of 11
ecogeographical variables (EGVs) were identified (see Table 2). These
variables were obtained from CORINE Land Use/Land Cover database, spatial
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resolution (pixel width) of 250 m (European Environment Agency 1996). From
this information we carried out both the habitat use analysis and the study of the
influence of goat livestock.
The analysis of the variables which determine habitat use (Table 2) by
the Iberian ibex was assessed by a nested stepwise multiple regression
analysis, using domestic goats presence/absence as the nested factor (e.g.
Quinn and Keough 2002). The Iberian ibex abundance was the response
variable. We designed a three step procedure to clarify the significance of the
variables and their interaction with goat livestock on the Iberian ibex habitat use.
In total, 11 habitat factors were considered: 1) We discarded a number of
variables with no statistical significance and avoided multicollinearity by using
the Spearman Rank Correlation coefficients. 2) Each of the independent
variables obtained from step 1 were then related to the dependent variable, ibex
relative abundance. Stepwise multiple regression analysis was used (Quinn and
Keough 2002). 3) Variables that yielded p<0.05 in step 2 were integrated into a
final model which also included the nested factor of livestock presence. Table 2. EGVs used in habitat use analysis for the Iberian ibex relative abundance dependent variable. The significance level of step 2 is provided (** p < 0.01, * p < 0.05, n.s. = non-significant). See text and Table 1 for more details.
Variables Meaning Significance
Goat livestock Presence/Absence of goat livestock ** Highest altitude Maximum altitude (m) n.s. Average altitude Average altitude (m) n.s. Slope Average slope index n.s. Cultures Frequency of cultures per pixel * Woodland Frequency of woodlands per pixel ** Scrubland Frequency of scrublands per pixel ** Grassland Frequency of grasslands per pixel n.s. Sparse vegetation Frequency of sparse vegetations per pixel ** Infrastructures Frequency of human infrastructures per pixel n.s. Water reservoir Frequency of rivers per pixel *
We carried out a nested regression analysis and obtained a final model
through a backward stepwise procedure. The level of significance for step 3
was set at 5%. The statistics package used was SPSS 10.06.
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RESULTS
Species distribution according to the surveys
Information covering 97.68% of the whole Castile-La Mancha region has
been obtained from 149 surveys correctly filled in. Results showed that the
Iberian ibex is present in 19% of the study area (175 out of 905 sampling units).
Five population nuclei have been identified: Montes de Toledo mountain range,
Sierra Madrona – Sierra Morena, Alto Tajo – Serranía de Cuenca, Casas
Ibáñez, and south of Albacete (see Figure 1). The species is more widely
distributed in Albacete province (it is present in 47% of the territory), followed by
Guadalajara (21%), Cuenca (15%), Ciudad Real (12%) and Toledo province
(3%).
Habitat suitability An habitat suitability map for the study species was carried out for the
province of Albacete, where the species was more abundant (see above). This
meant a total number of 15,384 1x1 km UTM grid cells.
Table 3. Correlation between ENFA factors and the environmental descriptors (EGVs). Percentages indicate the amount of specialization accounted for by each factor. Factor 1 is Marginality factor.
Variable Factor 1
(87.6%) Factor 2
(55.4%) Factor 3
(19.2%)
altitud_max 0.24 0.01 0.10 aspect 0.22 0.04 0.00 dist_agriculture 0.21 0.08 -0.02 dist_agro_forest 0.31 -0.09 0.32 dist_annual_crops 0.16 -0.26 0.16 dist_broad_leav 0.26 -0.02 0.00 dist_goat_livestock 0.02 -0.06 0.20 dist_coniferous -0.09 0.51 0.61 dist_industr 0.27 0.09 0.23 dist_inland_marshes 0.35 -0.02 -0.37 dist_road_rail 0.19 0.42 0.11 dist_sparse_veg -0.08 0.62 -0.27 dist_villages 0.21 -0.09 0.04 dist_vineyards 0.31 0.12 -0.14 dist_water_bodies 0.02 0.03 -0.34 dist_wood_scrub 0.20 -0.01 -0.01 slope 0.36 0.04 0.01
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Table 1 shows average values for the EGVs that define the habitat, both
in the whole study area (global mean) and in the area where ibexes were found
(species mean, with standardized values). For the ENFA analysis, the variable
“average distance to non-irrigated lands” was discarded due to its discontinuity.
The three significant factors selected (out of 27) explained 87.6% global
marginality and 75.2% global specialization. Coefficients of relationship
between variables and each one of the three factors are shown in Table 3.
Global marginality was 2.03, and global tolerance was 0.49. The habitat
suitability map can be seen in Figure 2. The first factor obtained, marginality
factor, was essentially associated to both high altitudes and slopes, and areas
distant to agro-forest lands, broadleaf woodlands, industrial areas, marshes and
vineyards (see coefficients in Table 3).
Figure 2. Habitat suitability map for the Iberian ibex in Albacete province. Observed ibex distribution is outlined. The arrow indicates a potentially suitable area not occupied by the ibex, and where livestock is present.
Ibexes are extremely sensitive to shifts from their optimal conditions on
this axis. Next factors show a certain degree of specialization, being associated
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to areas distant to coniferous forests, sparse vegetation and human
constructions, such as roads and railways, but also close to annual crops lands.
Factor 3 accounts for 19.2% of specialization, so that information provided is
much less accurate than that of the other two factors (see Table 3).
Habitat use
Relative ibex abundance was assessed by the largest size group
registered in each UTM grid cell considered in the study area, and obtained
from the questionnaire. Previously, we determined the validity of this measure
by relating it to our own average group size (see above). In our field surveys,
we detected 36 ibex groups (167 animals were counted) from the 17 transects
carried out in September 2003. The average group size was 4.76 ± 0.65, and it
correlated with the largest group size obtained in the questionnaire (Spearman
Rank Correlation: n=9, rho=0.80, p=0.01), so that the latter can be considered
as an estimate of ibex abundance. Table 4. Final model obtained for the habitat use analysis for the Iberian ibex relative abundance dependent variable (nested stepwise regression output). GL column refers to goat livestock absence (A) and presence (P). T.E. refers to the typical error.
Parameter GL Estimate T.E . t Probability
Intercept 3.07 0.86 3.58 <0.01
(A) 0.88 0.31 2.88 <0.01 Scrub land (P) -0.94 0.30 -3.13 <0.01
(A) -0.53 0.27 -2.47 0.01 Cultures (P) 0.89 0.19 4.67 <0.01
(A) -0.04 0.22 -0.20 0.84 Wood land (P) 0.81 0.22 3.65 <0.01
(A) -0.27 3.10 -0.09 0.93 Sparse vegetation (P) 1.45 0.45 3.19 <0.01
(A) 5.62 4.02 1.40 0.16 Water (P) 12.55 6.14 2.04 0.04
(A) -4.54 1.23 -3.69 <0.01 Goat livestock (P) 0 0.00 . .
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Figure 3. Relationships between Iberian ibex relative abundance and two EGVs which show opposite directions depending on the presence/absence of goat livestock, i.e. scrub land and cultures (see Table 4).
Nested stepwise multiple regression analysis showed that livestock
influences habitat use of the Iberian ibex, relegating it to suboptimal vegetation
areas (see Table 4). In those grid cells where domestic goat livestock ranges in
sympatry with the ibex, the latter occupies preferentially cultivated lands, sparse
vegetation areas and forests; whereas in absence of livestock the ibex is mainly
found in pasture-scrub areas and non-cultivated lands. The marginal effect
caused by distance to goat livestock herds (see Factor 3 in Table 3), is
exemplified in Figure 2.
In Figure 3 the relationship between those variables which showed
opposite directions, depending on the presence/absence of goat livestock, i.e.
scrub land and cultures, is shown.
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DISCUSSION
Here we have updated the Iberian ibex distribution in the region of
Castile-La Mancha (central Spain). A habitat suitability model has also been
accomplished by using the ENFA technique, particularly suitable for presence-
only data of a given species. Our results indicate that the Iberian ibex is not
occupying its optimal habitat in those areas where it shares its range with
domestic goat herds.
On ibex distribution in the study region, it is noteworthy to point out a
wider presence in comparison with previous surveys (Alados 1997; Pérez et al.
2002). A plausible explanation is the expected increase of the species area of
distribution which is taking place nowadays, in part due to a natural increment of
population numbers due to habitat changes, game management translocations
(Gortázar et al. 2000) or its recovery from past sarcoptic mange epizootics
(Pérez et al. 1997), and a probable decrease of its hunting pressure caused
precisely by the incidence of this disease (see Garrido 2004).
Concerning risks associated to parasite infections of the ibex, the main
agents are host-inspecific, e.g. sarcoptic mange (Pérez et al. 1997), so that they
can infect any ungulate species, among other mammals. Therefore, at high host
densities, as it is the case in areas with high livestock densities, the availability
of habitat for these parasites increases, as does the risk of epizootics (see
Acevedo et al. 2005 [Capítulo 1.2]).
Specific values for marginality and tolerance indexes are bound to
depend on the global set chosen as reference, so that a species might appear
extremely marginal or specialised on the scale of a whole country, but much
less so a subset of it (Hirzel et al. 2002). According to habitat suitability analysis
carried out the Iberian ibex is highly marginal in the studied area, and presents
a medium tolerance, evidencing that, although it is placed in marginal areas in
Castile-La Mancha, it seems to tolerate habitat changes, therefore
compensating its marginality with the expansion to areas of relatively
suboptimal habitat.
In our study, livestock seem to compete and displace the Iberian ibex
from its optimal habitat, i.e. pasture-scrublands (e.g., Chirosa et al. 2002), in
Capítulo 1
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those grid cells where livestock is present (see Figure 2). We have no data on
social avoidance between both species, so that future research should be
focused on confirming this apparent ecological displacement. Similar
conclusions were obtained from a study carried out in the Great Basin, where
pronghorn (Antilocapra americana) avoided areas grazed by sheep during
winter until spring-regrowth occurred, and favoured areas temporarily rested
from sheep use (Clary and Holmgren 1982; Clary and Beale 1983).
This apparent displacement of the Iberian ibex to suboptimal habitats by
livestock presence is confirmed in our nested factor analysis of habitat use. The
results obtained indicate that the ibex occupies different habitats depending on
the presence of domestic goats. When they are present, as seen in the previous
analysis of habitat suitability, the ibex is preferentially found in suboptimal
habitats, according to its resource requirements (see, e.g., Chirosa et al. 2002),
i.e. sparse vegetation, cultures and woodlands; whereas when livestock is
absent, the ibex mainly uses scrub lands and non-cultivated areas, where food
availability according to its diet is higher (e.g., Martínez and Martínez 1987;
Martínez 2000).
The question is whether both species, the ibex and the domestic goat,
actually compete for resources. Resource partitioning is defined as the
differential use by organisms of resources such as food and space (Schoener
1974; Begon et al. 1996), and may explain how species coexist despite
extensive overlap in ecological requirements (Hutchinson 1959; MacArthur and
Wilson 1967; MacArthur 1972; May 1973). On the contrary, competition is
considered to be the major selective force causing this differential use of
resources (Schoener 1974, 1986).
As livestock range and distribution exceed any natural expansion
process, they can be considered as introduced exotic species (see, e.g., Voeten
and Prins 1999), and resource partitioning with native ungulates would not be
expected but, rather, a certain overlap in resource selection (see Fleischner
1994; Edwards et al. 1996; Aagesen 2000; Prins 2000). This is the case in
North American steppes, where livestock replaced the bison (Bison bison) and
pronghorn (Schwartz and Ellis 1981; Hartnett et al. 1997). Thus, dietary niche
divergence in sympatric species can occur even at a very subtle scale (Hartnett
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et al. 1997). Campos-Arceiz et al. (2004) found that food overlap between
Mongolian gazelles (Procapra gutturosa) and livestock occurred not only at the
main forage categories but also at the selection of plant parts for foraging.
Interpretation of measures of niche overlap in terms of the implications
for competitive interactions is problematic (Putman 1996). High observed
overlap can imply competition, but only if resources are limited. In fact,
observations of high overlap might equally well be indicative of a lack of
competition (see Schoener 1983; de Boer and Prins 1990; Putman 1996).
The implications these results may have on the Iberian ibex viability and
expansion can be evaluated from different views. Ibex populations in the study
region seem to be in expansion, particularly in the provinces of Albacete,
Cuenca and Guadalajara, if we compare current abundance of the species
(Figure 1) and that of former studies (e.g. Pérez et al. 2002). Therefore,
currently isolated populations might enter into contact. This may imply new
viability risks associated to the increase of certain diseases, such as sarcoptic
mange. This disease has already been detected sporadically in Albacete
province (C. Gortázar, unpublished data), so that a consequent generalization
of its prevalence might occur in the near future. Finally, hunting pressure on the
Iberian ibex is negligible in Castile-La Mancha: a 0.0004% (63 individuals) of
total big game hunted in 1999-2003 period (Garrido 2004). Therefore, we
believe that game activity is not currently disturbing the Iberian ibex expansion
movements in the region.
As a conclusion, we encourage comparative studies of habitat use with
other ungulate species in sympatry (including exotics), as well as a monitoring
of disease prevalence and colonization process in order to assure the
establishment of the species in central Spain.
ACKNOWLEDGEMENTS
We are grateful to Leticia Díaz for her useful comments on a previous
version of the manuscript as well as her advise on the statistical analyses. We
are also indebted to M. Martínez, V. Alzaga, J. Millán, A. Pérez and J. Vicente
Capítulo 1
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for assistance in the field. This research was supported by a JCCM-CAMA
agreement, and P de Asturias and CSIC. J.C. is currently supported by the
Ministerio de Educación y Ciencia through a Ramón y Cajal contract.
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1.2.- RELACIONES ENTRE LA EXCRECIÓN DE NEMATODOS
BRONCOPULMONARES Y LA ABUNDANCIA RELATIVA DE CABRA
MONTÉS (CAPRA PYRENAICA HISPANICA) EN CASTILLA-LA MANCHA
Acevedo, P., Vicente, J., Alzaga, V., Gortázar, C. (2005) RELATIONSHIP BETWEEN
BRONCHOPULMONARY NEMATODE LARVAE AND RELATIVE ABUNDANCES OF SPANISH
IBEX (CAPRA PYRENAICA HISPANICA) FROM CASTILLA-LA MANCHA. Journal of
Helminthology 79, 113-118.
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RESUMEN
Se ha evaluado la excreción de nematodos broncopulmonares en 160
muestras de heces de cabra montés (Capra pyrenaica hispanica Shimper 1848)
recogidas en 13 poblaciones de Castilla–La Mancha en septiembre de 2003. Se
compararon las intensidades de parasitación y prevalencias, junto con otros factores,
tales como la disponibilidad de pastos y la abundancia de otros ungulados, tanto
domésticos como silvestres. Ello se hizo a dos niveles de estudio, poblacional y grupo
fecal, mediante un procedimiento en dos pasos. Las larvas de Protostrongílidos
mostraron valores (intensidad media: 1.56 ± 0.12, n= 94; prevalencia media: 25.62 ±
6.86 %, n= 160) similares a Dictyocaulus spp. (intensidad media: 1.03 ± 0.11, n= 48;
prevalencia media: 30.00 ± 7.11 %, n= 160). A nivel poblacional, se han encontrado
correlaciones positivas entre las prevalencias de ambos grupos de broncopulmonares.
La prevalencia en ambos, pero no la intensidad de parasitación, también se
correlaciona positivamente con los índices de abundancia de las poblaciones de cabra
montés. Ello ocurre tanto a nivel poblacional como a nivel de los grupos fecales
individuales. Estas relaciones sugieren que: (i) la propagación de estos parásitos en
las poblaciones de cabra montés de Castilla–La Mancha podría responder a procesos
denso-dependientes, y (ii) las poblaciones estudiadas pueden tener una exposición y
susceptibilidad similar a ambos grupos de parásitos broncopulmonares, presentando
patrones parásito-hospedador similares a pesar de sus diferentes ciclos vitales. Los
parásitos broncopulmonares de las poblaciones de cabra montés de Castilla–La
Mancha no parecen representar un riesgo sanitario para este ungulado, pero pueden
ser usados en una red de vigilancia sanitaria para monitorizar de manera no invasiva
estas poblaciones, que actualmente están en expansión.
ABSTRACT
The excretion of bronchopulmonary nematode infective larvae was evaluated in
160 faecal samples of Spanish ibex (Capra pyrenaica hispanica Shimper 1848)
collected from 13 metapopulations in Castilla–La Mancha, south-central Spain in
September 2003. Intensities and prevalences were compared with pasture availability,
abundances of wild and domestic ungulates at both levels, i.e. for populations and for
faeces in a two-step procedure. Protostrongylid larvae showed similar infection rates
(mean intensity: 1.56 ± 0.12, n= 94; mean prevalence: 25.62 ± 6.86 %, n= 160) to
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Dictyocaulus spp. (mean intensity: 1.03 ± 0.11, n= 48; mean prevalence: 30.00 ± 7.11
%, n= 160). At the population level, positive correlation were found between the
prevalences of both bronchopulmonary taxa. The prevalence in both groups, but not
intensity, also correlated positively with Spanish ibex abundance indexes both for the
populations and individual faeces. These findings suggest that: (i) parasite spreading
across Spanish ibex populations in Castilla–La Mancha could respond to host density-
dependent processes, and (ii) these populations may have similar exposition and/or
susceptibility to both bronchopulmonary taxa resulting in similar host-parasite patterns,
despite their different life cycles. Brochopulmonary outputs in the Spanish ibex from
Castilla–La Mancha seems not to represent a health risk for this endemic wild ungulate
but may be useful in any health surveillance scheme for the increasing populations of
Spanish ibex.
INTRODUCTION
Bronchopulmonary nematode parasites are frequently found parasitizing
wild ungulates. These include several homoxenous species belonging to the
Family Dictyocaulidae (Dictyocaulus spp.), and heteroxenous parasites of the
Family Protostrongylidae (Cistocaulus spp., Neostrongylus spp., Muellerius
spp., Protostrongylus spp.), which parasitize terrestrial gasteropods as
secondary hosts (Anderson 2000). Infections are commonly asymptomatic, but
they may occasionally cause severe verminous bronchopulmonary pneumonia
and nodular lesions in the lungs (Boch and Schneidawind 1988). Usually, fatal
cases are associated to concomitant bacterial infection, and predisposing
factors, such as increased exposition to infective larvae in captivity, are involved
(Charleston 1980). Infections by lungworms in wild ungulates warrant the
attention of researchers and wildlife managers (e.g., Festa-Bianchet 1989;
Forrester and Lankester 1997; Enk et al. 2001; Vicente and Gortázar 2001).
The study of infective larval stages in faeces has been employed as a
non-invasive alternative technique to study host-parasite relationships in wild
ungulate populations (e.g., Festa-Bianchet 1991). Both population and
individual factors affecting bronchopulmonary adult infection or larvae outputs
have been evaluated in wild ungulates (e.g., Hugonnet and Cabaret 1987;
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Arnett et al. 1993), but there is little published on mountain ungulates (Manfredi
et al. 1996).
The Spanish ibex (Capra pyrenaica hispanica) is a medium-size
mountain ungulate endemic to the Iberian Peninsula. It is mainly distributed
through most of the Mediterranean range mountains and, to a lesser extent, in
central and northern Spain (Pérez et al. 2002). Currently, the populations at
Castilla-La Mancha are increasing both in distribution area and densities
(Acevedo et al. 2003). Thus, health parameters of this species need to be
monitored in addition to ecological and demographic studies of the Spanish
ibex, other sympatric wildlife, and domestic livestock.
In this context, our objective was to assess at population level the
relationships of Dictyocaulidae and Protostrongylidae bronchopulmonary faecal
larvae with the abundance indexes of the Spanish ibex and sympatric wild and
domestic ungulates in 13 populations from Castilla–La Mancha.
MATERIALS AND METHODS
Fresh faecal samples (n= 160) were collected in conjunction to an
ecological programme on Spanish ibex relative abundances in 13 areas (Figure
1) throughout the current distribution of the species in Castilla–La Mancha
(UTM coordinates: 30S 294,348-681,063 4,208,706-4,575,340; minimum
altitude= 244 m, maximum altitude= 2,274 m) during September 2003. Since
ungulate droppings tend to be aggregated, we developed a simple method
using dropping frequency (instead of their number) to estimate the relative
abundance of wild ungulates including Spanish ibex and red deer (Cervus
elaphus) (Vicente et al. 2004). Briefly, each count consisted of n= 30 transects
of 100 m, divided into ten sectors of 10 m in length. The dropping frequency
was defined as the average of the number of 10 m sectors with Spanish ibex or
red deer droppings in each transect of 100 m. (DF=ΣDi/n; where “D” is the
number of dropping-positive sectors and ranges from 0 to 10, and “n” is the
number of 100 m transects, usually 30). Habitat and management variables
considered in the study were chosen on the basis of their epidemiological
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significance to survival and transmission of infective stages, and the
characteristics of local big game and livestock. Environmental conditions for the
13 study areas were recorded every 200 m in 30 buffer areas of 25 m radio
across the lineal transects (n=15 points per area) to finally obtain mean values
of habitat land uses and habitat structure of each estate.
Figure 1. The location of sampling areas where faeces of Spanish ibex were collected within Castilla–La Mancha, during September 2003.
Thus, we considered schrub / forest / grass / soil covers (%) and habitat
availability (Mediterranean schrublands, Dehesa (Mediterranean savannah-like
habitat), Mediterranean hardwood forest, (Quercus spp.), pine plantations,
pastures, riparian habitat, agricultural areas). Data from private and government
gamekeepers regarding the number of livestock in each study area were obtain
through personal interwiews.
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Bronchopulmonary larvae were extracted from 5 g of faeces using the
beaker larval migration technique as described by Forrester and Lankester
(1997). Larvae were quantified in a Favatti counting chamber and identified to
the genus level according to their morphology and linear lengths using a
calibrated eyepiece micrometer (Melhorn et al. 1992; Cordero del Campillo and
Rojo 1999; Anderson 2000).
The terms relating to prevalence and intensity are considered as
describes Margolis et al. (1982). Standard errors for prevalences were
estimated with the expression S.E. (p) =p(1-p)/n1/2 (Martin et al. 1987).
Analyses of factors affecting the prevalence and intensity of bronchopulmonary
larvae were performed at two levels. First, the bivariable association of mean
excretion rates (prevalences and intensities) at population level for overall
broncopulmonary parasites, Dictyocaulidae, overall Protostrongylidae larvae
and the different genera were compared with habitat variability (pasture
covering) and other ungulate (cattle, sheep/goat or deer) abundance indexes
using nonparametric Spearman rank correlation coefficients (rs, n = 13). Mann-
Whitney and Chi2 non-parametric test were employed to compare the intensities
and prevalences of different protostrongylid genera.
To clarify the initial findings at the population level to elucidate the
relative importance of explanatory variables (avoiding the multiple test problem),
the outcome variables from the previous analysis were evaluated by means of
multivariable analysis for overall bronchopulmonary, Dictyocaulidae and overall
Protostongylidae throughout the faeces (n = 160). Generalized linear models
(GLM) were conducted with overall bronchopulmonary, Dictyocaulidae and
overall Protostongylidae larvae as response variables, respectively (considered
as binomial: presence,1; or absence, 0). To ensure that relationships were not
driven by a few points of small sample size, the sample size at the population
level was controlled by including this in the model as a explanatory variable.
Habitat (pasture availability) was also included as an explanatory variable.
Finally, in the case of the Dictyocaulidae and Protostrongylidae models, both
response and explanatory variables concerning larvae presence (binomial
variables: presence,1; or absence, 0) respectively were interchanged to identify
any significant relationships between these taxa for faeces. A negative binomial
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error distribution and a logistic link function (Crawley 1993) were considered.
The resulting models were reduced to their simplest form by eliminating, in a
backward stepwise manner, any explanatory variables that failed to explain
significant variation in the response. The level of significance was established at
the 5 % level. All P-values refer to two tailed tests, using SPSS 10.0.6 program
(SPSS Inc. 1999) and Statistica (Statsoft Inc. 1999) software packages.
RESULTS
Infection rates of bronchopulmonary larvae in Spanish ibex faeces from
Castilla–La Mancha are shown in Table 1 at the population level. Both overall
Protostrongylidae (mean intensity= 1.56 ± 0.12, n= 94; mean prevalence: 25.62
± 5.88 %, n= 160) and Dictyocaulus spp. (mean intensity= 1.03 ± 0.11, n= 48;
mean prevalence= 30.00 ± 43.14 %, n= 160) larvae in faeces showed similar
rates. Prevalences of Protostrongylidae and Dictyocaulus spp. correlated
positively and significantly at population level (P < 0.05, Figure 2). Table 1. Mean prevalence ± S.E.95% I.C. and mean intensity of infection of the Spanish ibex with Protostrongylidae and Dictyocaulus spp. larvae.
Protostrongylidae Dictyocaulus spp.
Sampling area Mean intensity ±
S.E.95% I.C. (n) Mean prevalence
± S.E.95% I.C Mean intensity ± S.E.95% I.C. (n)
Mean prevalence ± S.E.95% I.C
Madrona (30) 1.64 ± 0.35 (14) 46.67 ± 18.15 1.52 ± 0.48 (5) 16.67 ± 13.57 Viso Marqués (5) 1.75 ± 0.00 (1) 20.00 ± 39.20 0 0.00 ± 0.00 Garganta (10) 1.20 ± 0.21 (8) 80.00 ± 26.13 0.91 ± 0.22 (5) 50.00 ± 32.67 Becerras (10) 1.62 ± 0.43 (7) 70.00 ± 29.95 1.32 ± 0.37 (3) 30.00 ± 29.95 Fuertescusa (10) 1.68 ± 0.38 (5) 50.00 ± 32.68 0.85 ± 0.00 (1) 10.00 ± 19.60 S. Cuenca (13) 1.47 ± 0.62 (5) 45.50 ± 30.89 1.36 ± 0.20 (4) 30.80 ± 26.07 Cabriel (10) 1.45 ± 0.46 (5) 50.00 ± 32.67 0 0.00 ± 0.00 Liétor (10) 1.29 ± 0.39 (8) 80.00 ± 26.13 0.79 ± 0.32 (4) 40.00 ± 32.01 Riopar (12) 0.93 ± 0.38 (5) 41.67 ± 29.13 0.66 ± 0.099 (4) 33.33 ± 27.85 Salobre (10) 2.17 ± 0.17 (6) 60.00 ± 32.01 1.16 ± 0.35 (5) 50.00 ± 32.67 Bogarra (21) 1.17 ± 0.19 (17) 80.95 ± 17.21 0.89 ± 0.20 (12) 57.14 ± 21.70 Casas Lázaro (8) 2.18 ± 0.36 (3) 37.50 ± 35.87 1.08 ± 0.00 (1) 12.50 ± 24.50 Yeste (11) 2.40 ± 0.18 (10) 90.91 ±17.82 0.91 ± 0.18 (4) 36.36 ± 29.81 Overall 1.56 ± 0.12 (94) 25.62 ±5.88 1.03 ± 0.11 (48) 30.00 ± 43.14
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The prevalences of overall Protostongylidae and Dictyocaulus spp.
correlated positively with the Spanish ibex relative abundance (Figure 3).
Regarding the effects of habitat on parasites, pasture availability correlated
positively with the mean prevalence of Protostrongylus spp. (P < 0.05).
From the analysis of individual faeces, the presence of overall
bronchopulmonary, Protostrongylidae and Dictyocaulus spp. larvae in faeces
showed an association with higher Spanish ibex abundance indexes (P < 0.001,
P < 0.01 and P < 0.01 for overall bronchopulmonary, Protostrongylidae and
Dictyocaulus spp. larvae models, respectively). In both the Protostrongylidae
and Dictyocaulus spp. models there was no evidence to link faeces infected
with Dictyocaulus spp. with protostrongylid infections and vice versa.
rs= 0.68, P < 0.05, n=13
0
20
40
60
80
100
0 10 20 30 40 50 60
Protostrongylidae (%)
Dic
tyoc
aulu
s sp
p. (
%)
Figure 2. The relationship between the prevalences (%) of Protostrongylidae and Dictyocaulus spp. larvae in the Spanish ibex from 13 sampling sites in Castilla-La Mancha.
Four different genera of Protostrongylidae were identified: Cistocaulus
spp. (mean intensity= 1.51 ± 0.22, n= 13; mean prevalence= 8.12 ± 4.25, n=
160); Neostrongylus spp. (mean intensity= 1.62 ± 0.21, n= 32; mean
prevalence= 20.00 ± 6.22, n= 160), Muellerius spp. (mean intensity= 1.74 ±
1.17, n= 38; mean prevalence= 23.75 ± 6.61, n= 160) and Protostrongylus spp.
(mean intensity= 1.17 ± 0.15, n= 19; mean prevalence= 11.87 ± 6.05, n= 160).
Thus, all showed similar intensity rates (P > 0.05 referred to all comparison
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pairs), but Muellerius spp. and Neostrongylus spp. showed higher prevalence
values than Cystocaulus spp. and Protostrongylus spp. (P < 0.05 referred to
comparisons of pairs). When considering the different genera of
Protostrongylidae at the population level, Cistocaulus spp. correlated positively
with abundance index of small domestic ruminants (including sheep and goats)
(P < 0.01) and with the density of small ruminants (estimated as heads per km2)
according to keeper interviews (P < 0.05).
Figure 3. Relationships between both Protostrongylidae and Dictyocaulus spp. larvae prevalences (%) with the Spanish ibex relative abundance indexes throughout the study metapopulations.
rs= 0.66, P < 0.05, n=13
0
20
40
60
80
100
0,0 0,5 1,0 1,5 2,0 2,5 3,0Spanish Ibex relative abundance indexes
Dic
tyoc
aulu
s s
pp. (
%)
rs= 0.75, P < 0.01, n=13
0
20
40
60
80
100
Prot
ostr
ongy
lidae
(%)
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DISCUSSION
All taxa of bronchopulmonary parasites found in the present study had
previously been reported in the Spanish ibex. The little available literature
comes from Andalusia (Southern Spain), and includes either necropsies
(Montero et al. 1999, in Sierra Nevada), or both necropsies and coprological
examinations (Universidad de Jaén 1999, in several mountainous areas from
Andalusia). This lack of information limits the comparisons between our
infection rates and previous data.
As in the present study, Muellerius spp. (mean prevalence: 25.77%) was
also the most common protostrongylid species in the previous literature, with a
prevalence of 74.30%, always in concomitant infections with other
bronchopulmonary parasites (Universidad de Jaén 1999). To date, the only
species of the genus Muellerius spp. described in the Spanish ibex is Muellerius
capillaris (Montero et al. 1999; Universidad de Jaén 1999). Our overall
prevalences, not only for Muellerius spp., but also for the remainder of
protostrongylids, are lower than those previously described in coprosurveys.
Regarding Dictyocaulus spp., the overall prevalence data (26.35%) shows a
higher prevalence than previously reported in coprological analyses of 1.20%
(Universidad de Jaén 1999) but lower than that reported at necropsy by
Montero et al. (1999) (37.5%). In addition to the scarcity of data, the present
data refer to late summer, and consequently are not directly comparable to
those previously reported, as lower values in prevalence have been found in the
summer and autumn as compared to winter and spring in Spanish ibex
(Universidad de Jaén 1999) and Alpine ibex (Capra ibex ibex, Manfredi et al.
1996). Despite this, Dictyocaulus spp. presents a higher prevalence when
compared with the majority of the Andalusian populations (Universidad de Jaén
1999). Apart from differences in seasonal sampling, a beaker extraction method
as described by Forrester and Lankester (1997) was used in the present study,
which is an improvement on the classical Baerman funnel method, but makes
comparisons between past and present data difficult.
Factors such as exposure and / or differences in susceptibility to
parasites could be operating at the population level, and hence differences
between host and parasite populations could occur (Wilson et al. 2001). In
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particular, there was a correlation between the prevalences of both groups of
bronchopulmonary parasites (Protostrongylidae and Dictyocaulus spp.) and
host abundances. However, with field collected faeces, host sample size is
unknown but in the present study a positive association between the prevalence
of parasite taxa (overall bronchopulmonary, Dictyocaulus spp. and
protostrongylids) and host abundance supports the idea of density-dependent
processes operating in the transmission of brochopulmonary nematodes in the
Spanish ibex. This is consistent with epidemiological models which predict a
positive relationship between host population density and abundance of
macroparasites since the transmission rate generally is a positive function of
host population density (Arneberg et al. 1998; Arneberg 2001). This relationship
was noted for both indirectly (protostrongylids) and directly transmitted
(Dictyocaulus spp.) nematodes. However, the limited sample sizes of this
scarce wild ungulate in Castilla–La Mancha, which constitutes populations at
their distribution limit coming from other regions, must be taken into account
before precise conclusion can be drawn. More research is needed to elucidate
this aspect.
The Spanish ibex presents a wide range of densities in Castilla–La
Mancha (Figure 3), ranging from 0.2 to 5.8 animals per km2, which may be due
to the current spatial expansion of this species in Castilla–La Mancha, offering
different epidemiological scenarios to parasite transmission. The parasite-host
density relationships are mainly related to parasite dissemination across the
different host populations, but not to intensities. The effects of parasites on host
are expected to be parasite load dependent (e.g., Albon et al. 2002), and
suggest that current bronchopulmonary infection loads are not causing any
detrimental effects on the studied populations, since larval counts were not high
enough to produce clinical infections (Cordero del Campillo and Rojo 1999).
With reference to the relationship between habitat and parasites, a
correlation between pasture availability and the prevalence of Protostrongylus
spp. prevalence was demonstrated. Since pastures are a limited resource in
Mediterranean habitat, this finding could be related to transmission rates of the
parasite depending on the pasture microhabitat availability for infective larvae
and intermediate hosts (gastropods), and on host aggregation in these areas.
Tesis Doctoral
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An additional explanation may be related to pastures shared between
Spanish ibex and domestic livestock. Only the prevalence of Cystocaulus spp.
was correlated with livestock abundance, supporting the idea that wild and
domestic ruminants share at least some parasite genera, which eventually
could be transmitted at the interface.
The present study has therefore indicated a relationship between the
abundance of a wild ungulate, the Spanish ibex, and the prevalence of
bronchopulmonary parasites, suggesting density-dependent transmission rates
of these parasites. Therefore, monitoring herd levels for evidence of
bronchopulmonary parasite infections could prove to be a valuable tool for
wildlife health managers in the surveillance of populations of the endemic
Spanish ibex.
ACKNOWLEDGEMENTS
We are very grateful to public managers and gamekeepers for their help
in the fieldwork. This is a contribution to Junta de Comunidades de Castilla-La
Mancha (Convenio CAMA). Joaquín Vicente was supported by a predoctoral
grant from the Junta de Comunidades de Castilla-La Mancha and Vanesa
Alzaga had a partial grant from Universidad de Castilla-La Mancha.
REFERENCES
Acevedo, P., Alzaga, V., Martínez, M., Pérez, A., Talavera, F., Montarroso, L., Gortázar, C. (2003) Aportaciones al estudio de la distribución, dinámica poblacional y estado sanitario de la cabra montés en Castilla-La Mancha. Proceedings of the Congress VI SECEM, Ciudad Real, Spain.
Albon, S.D., Stien, A., Irving, R.J., Langvatn, R., Ropstad, E., Halvorsen, O. (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London series B-Biological Sciences 269, 1625-1632.
Capítulo 1
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Anderson, R.C. (2000) Nematode parasites of Vertebrates. Their development and transmission. CABI Publishing, New York.
Arneberg, P. (2001) An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite communities. Ecography 24, 352-358.
Arneberg, P., Skorping, A., Grenfell, B., Read, A.F. (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B 265, 1283-1289.
Arnett, E.B., Irby, L.R., Cook, J.G. (1993) Sex and age specific lungworm infection in Rocky Mountain bighorn sheep during winter. Journal of Wildlife Diseases 29, 90-93.
Boch, J., Schneidawind, H. (1988) Krankheiten des jagdbaren Wildes. Verlag Paul Parey, Berlin
Charleston, W.A.G. (1980) Lungworm and lice of the red deer (Cervus elaphus) and the fallow deer (Dama dama), a review. New Zealand Veterinary Journal 28, 150–152.
Cordero del Campillo, M., Rojo, F.A. (1999) Parasitología Veterinaria. McGraw Hill. Interamericana.
Crawley, M.J. (1993) GLIM for ecologists. Blackwell, London.
Enk, T.A., Picton, H.D., Williams, J.S. (2001) Factors limiting a bighorn sheep population in Motana following a dieoff. Northwest Science 75, 280-291.
Festa-Bianchet, M. (1989) Individual-differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). Journal of Animal Ecology 58, 785-795.
Festa-Bianchet, M. (1991) Numbers of lungworms larvae in faeces of bighorn sheep: yearly changes, influence of host sex, and effects on host survival. Canadian Journal of Zoology 69, 547-554.
Forrester, S.G., Lankester, M.W. (1997) Extracting Protostrongylid nematode larvae from ungulate feces. Journal of Wildlife Diseases 33, 511-516.
Hugonnet, L., Cabaret, J. (1987) Infection of roe-deer in France by lung nematode, Dictyocaulus eckerti Skrjabin, 1931 (Trichostrongyloidea): Influence of environmental factors and host density. Journal of Wildlife Diseases 23, 109-112.
Manfredi, M.T., Zaffaroni, E., Fraquelli, C., Bonicalzi, A., Lanfranchi, P. (1996) Diffusione del parassitismo broncopulmonare nello Stambecco (Capra i. ibex) del Piz Albris. Supplemento alle Ricerche di Biologia della Selvaggina XXIV, 97-104.
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Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M., Schad, G.A. (1982) The use of ecological terms in parasitology (report of an Ad Hoc Committee of the American Society of Parasitologists). Journal of Parasitology 68, 131-133.
Martin, S.W., Meek, A.H., Willeberg, P. (1987) Veterinary Epidemiology. Iowa State University Press, Ames.
Melhorn, H., Düwel, D., Raether, W. (1992) Atlas de Parasitologia Veterinaria. Grass, Barcelona.
Montero, E., Montero, F.J., Espinosa, O., Cano, J. (1998) Capra pyrenaica var. hispanica wild population of the Sierra Nevada (Spain): bronchopneumonic pathology. In: Proccedings of Congress Euro-American Mammal, Santiago de Compostela.
Pérez, J.M., Granados, J.E., Soriguer, R.C., Fandos, P., Marquez, F.J., Crampe, J.P. (2002) Distribution, status and conservation problems of the Spanish ibex, Capra pyrenaica (Mammalia : Artiodactyla). Mammal Review 32, 26-39.
Universidad de Jaén (1999) Seguimiento y control de la Sarna Sarcóptica que afecta a las poblaciones de cabra montés (Capra pyrenaica hispanica) existentes en Andalucía. Junta de Andalucía.
Vicente, J., Gortázar, C. (2001) High prevalence of large spiny-tailed protostrongylid larvae in Iberian red deer. Veterinary Parasitology 96, 165-170.
Vicente, J., Segalés, J., Höfle, U, Balasch, M., Plana-Durán, J, Domingo, M., Gortázar, C. (2004) Epidemiological study on porcine circovirus type 2 (PCV2) infection in the European wild boar (Sus scrofa). Veterinary Research 35, 243-253.
Wilson, K., Bjornstad, O.N., Dobson, A.P., Merler, S., Poglayen, G., Randolph, S.E., Read, A.F., Skorping, A. (2001) Heterogeneities in macroparasite infections: patterns and processes. In: The Ecology of Wildlife Diseases. P.J. Hudson, A. Rizzoli, B.T. Grenfell, H. Heesterbeek, A.P. Dobson (eds.). Oxford University Press, Oxford.
CAPÍTULO 2
Acevedo, P., Cassinello, J. HUMAN-INDUCED EXPANSION OF WILD UNGULATES MAY
FACILITATE NICHE OVERLAP OF TAXONOMICALLY DISTANT SPECIES. Journal of
Biogeography, en evaluación (enviado a 29/09/2006).
LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR ELHOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO DE ESPECIESTAXONÓMICAMENTE DISTANTES: EL CIERVO IBÉRICO Y LA CABRAMONTÉS
Tesis Doctoral
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RESUMEN
1. La explotación de las especies cinegéticas normalmente determina un incremento
de su área de distribución más allá de su propio potencial dispersivo. Sin embargo, los
efectos ecológicos que pueden originar las expansiones mediadas por el hombre han sido
poco estudiados. Dichas expansiones pueden producir un aumento de la presión de
herbivoría y de las relaciones de competencia por los recursos con otros herbívoros.
2. El empleo de nuevas metodologías basadas en los SIG puede ser útil para
abordar este tema. El nicho realizado del ciervo en el sureste de España se ha analizado
mediante modelos de adecuación de hábitat. Para ello se han diferenciado dos poblaciones
de ciervo en función de su origen: una población autóctona y otra introducida, originada tras
numerosas introducciones realizadas con fines cinegéticos.
3. Ambas poblaciones están bien establecidas y aparentemente se reproducen con
éxito. Sin embargo, su nicho realizado difiere sustancialmente. Esto muestra que el ciervo
presenta una elevada plasticidad ecológica, siendo capaz de adaptarse a condiciones
ecológicas subóptimas en donde ha sido introducido.
4. Las áreas de interés cinegético incluidas en este estudio, donde el ciervo ha sido
ampliamente introducido, son zonas nativas de la cabra montés. Un análisis comparativo de
la distribución potencial de ambas especies, ciervo y cabra, muestra un elevado
solapamiento de sus nichos ecológicos.
Síntesis y aplicaciones. Se muestra la presencia de diferentes nichos realizados para
poblaciones de una misma especie que únicamente difieren en su origen: poblaciones nativa
e introducida de ciervo ibérico, siendo las últimas potenciadas por intereses cinegéticos. Las
poblaciones introducidas de ciervo muestran un elevado solapamiento de nicho con la cabra
montés, pudiendo suponer una amenaza para ésta debido a la competencia por los recursos
y a la posible transmisión de enfermedades, todo ello agravado en situaciones de
sobreabundancia. Estos resultados se discuten en el contexto de las invasiones biológicas, y
se sugiere que las especies que han ampliado su distribución más allá de su potencial
dispersivo, gracias a la acción humana, deberían ser consideradas como un caso especial
de especies invasoras.
ABSTRACT
1. Game species exploitation usually determines an increase of their distribution,
further from their own dispersal potential, but we know too little on the ecological effects
these human-induced expansions may originate, particularly as an increase of herbivory
pressure and competition for resources with other herbivore species.
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2. The use of new GIS-based methodologies may help in addressing this issue. Red
deer realized niche in the south east of Spain has been analyzed by means of habitat
suitability modelling. Two populations have been distinguished, according to their origin: an
autochthonous one, inhabiting an area where the presence of the species is known since
prehistoric times, and an introduced population, originated by several introductions carried
out by human hunting interests.
3. Both populations are well-established and apparently successfully breeding.
However, the realized niche differs substantially between them. Thus, the red deer is
expressing a high ecological plasticity, adapting to suboptimal ecological conditions in areas
where it is introduced.
4. The areas of hunting interest included in our study, where the red deer has been
widely introduced, are the native land of the Iberian ibex. A comparative analysis of potential
distributions of both species showed a strong niche overlap.
Synthesis and applications. We provide evidence of differing realized niche for
populations of different origin of the same species: native and introduced populations of
Iberian red deer, the latter promoted by sport game interests. The introduced deer population
shows a strong niche overlap with native Iberian ibex, which might be under threat due to
resource competition and/or disease transmission produced by overabundance of ungulates.
We discuss these results in the light of biological invasions, and proclaim that human-
induced expansion of native species, out of their own dispersal potential, should be regarded
as a particular case of invasive species.
INTRODUCTION
According to niche theory, a given species is optimally present in any habitat
offering the fundamental requirements for it to survive, grow and reproduce, i.e., the
fundamental niche (Hutchinson 1958). However, in the light of competition between
species, the niche used is usually smaller, the so-called realized niche (ibid.). On the
other hand, the concept of native species is not actually based on ecological
assumptions, but rather on whether its presence in a given area is natural and not
caused by human intervention; whereas a non-native species is the one occupying
an area outside its natural past or present range and dispersal potential (Falk-
Petersen et al. 2006). Being native or non-native to an area does not imply
necessarily getting or not getting one's niche requirements.
Tesis Doctoral
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A non-native species may successfully inhabit an area provided its realized
niche is accomplished. If this establishment comes along with an expansion of its
range then it is regarded as an invasive species (ibid.). The degree of alteration
caused by invasive species on the host ecosystem depends on their capacity to
establish, reproduce and spread (Bright and Smithson 2001), i.e., on becoming
"naturalized" (Falk-Petersen et al. 2006), which is affected by the presence of
predators, competitors, parasites or diseases (Hengeveld 1989).
The unnatural, human-induced expansion of native large herbivores in Europe,
due to hunting interests, is well documented (e.g., Braza et al. 1989; Gortázar et al.
2000; Pérez et al. 2002; Mátrai et al. 2004), an expansion that might be regarded as
a particular case of invasive species. Currently, there is evidence of wild ungulates
increasing in numbers and expanding in some European countries (e.g., Cargnelutti
et al. 2002; Acevedo et al. 2005, 2006a [Capítulo 1.1]). This generalized expansion
may be facilitated by recent increasing control of exploitation and poaching and land
use changes, such as agricultural abandonment (see Acevedo et al. 2005), creation
of protected areas and conservation reserves (e.g., Alados 1997); but also facilitated
by translocations and introductions (see Falk-Petersen et al. 2006) carried out by
hunting interests (Gortázar et al. 2000; Whittaker et al. 2001; Pérez et al. 2002). But
we do not know which effects these ungulates expansions may have on the host
ecosystems and viability of ungulate populations themselves.
Spatially explicit models are increasingly applied to predict species potential
distribution and habitat suitability maps (e.g., Guisan and Zimmermann 2000;
Soberón and Peterson 2005). Most models are empirically deduced, relating
observed patterns of occupancy to environmental parameters (Corsi et al. 2000).
Despite their wide application, such models also have a series of draw-backs (Wiens
2002). One rarely considered point is that spatial models may fail to depict the native
area of occupancy, not only due to changes in habitat availability, but also because
past anthropogenic disturbance may have confounded the underlying patterns of
habitat use (Baumann et al. 2005). Hence, given an interest in the native status,
extant patterns of habitat use and distribution should be viewed in the light of
historical determinism (Patterson 1999), landscape change (Knick and Rotenberry
2000), and anthropogenic changes of faunal community structures (Berger et al.
2001).
Capítulo 2
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The fitness of ungulates is known to vary with individual access to preferred
habitat (Nielsen et al. 2004). Changes in spatial patterns of habitat conditions such
as forage availability (lason et al. 1986; Acevedo et al. 2006b), predation risk
(Skogland 1991), or vegetation cover (Mysterud and Østbye 1999; Acevedo et al.
2006b), may therefore be followed by changes in population density and distribution,
as well as alterations in habitat use or landscape colonization (Pettorelli et al. 2001;
Acevedo et al. 2005). Effects of this kind may themselves become conservation
problems (Mack et al. 2000), as ungulate species can affect their habitat negatively
by selective feeding and overgrazing of the vegetation (Soriguer et al. 2001) and for
potential competition with other native species (P. Acevedo unpublished data).
The Iberian red deer (Cervus elaphus hispanicus Hilzheimer 1909) is one of
the 12 red deer subspecies currently recognized, which were originally distributed
throughout Eurasia and the Maghreb (Geist 1998; see also Carranza 2004, and
references therein). During the last glacial period (the Würm glaciation), which ended
10,000 ybp, Eurasian large herbivores were relegated to southern and more
temperate areas; but deer were of great interest to humans as game species, and
were later reintroduced in the whole continent, including the Iberian Peninsula (e.g.,
Braza et al. 1989; Soriguer et al. 1994). Currently, the red deer is widely distributed in
the Iberian Peninsula, except for the northwestern corner and the east cost
(Carranza 2002; Figure 1). The red deer is present in practically all Iberian habitats,
provided pastures and woody plants (bushlands) are present (e.g., San José et al.
1997; Bugalho et al. 2001). It tends to occupy ecotones between forest and
shrubland-pastures, specially in Mediterranean habitats (Braza et al. 1984; Escós
and Alados 1992; Lazo et al. 1994; San José et al. 1997). The extraordinary ubiquity
of the Iberian red deer has been facilitated by human actions, direct or indirectly.
Thus, game stock introductions throughout the Iberian Peninsula started to take
place during 1950's, mainly from two mountainous regions, Sierra Morena and
Montes de Toledo (Braza et al. 1989; Gortázar et al. 2000; see Figure 1). Soriguer et
al. (1994) reported that the Servicio Nacional de Caza y Pesca introduced more than
1500 red deer individuals between 1950 and 1964 in more than 17 Spanish
provinces. This impressive human-induced expansion has originated its presence in
areas traditionally under the natural range distribution of other large herbivores, such
Tesis Doctoral
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as the Iberian ibex, Capra pyrenaica, a typical mountainous ungulate (Escós and
Alados 1992).
In this paper we analyse potential red deer distribution in southeastern Iberian
Peninsula, defining and comparing niches of autochthonous areas (obtained from
historical data) and areas where the species has been introduced in recent times,
away from its natural range (Braza et al. 1989). It is noteworthy the abundance of the
Iberian ibex in the study region (Pérez et al. 2002), so that a comparison with its
environmental niche will also be conducted.
Figure 1. Indication of some localities in the Iberian Peninsula where the red deer was introduced from autochthonous populations of Montes de Toledo (arrows, Centro Quintos de Mora, 1970-1990, unpub. report). In grey, current red deer distribution (adapted from Carranza 2002).
Capítulo 2
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To our knowledge, this is the first attempt to characterize the niche utilized by
the same species under its natural range distribution and the one promoted by
relatively recent human introductions.
MATERIALS AND METHODS
The study area
To properly define the realized niche (Hutchinson 1958; but see Soberón and
Peterson 2005) of a species within a given region, the area used to investigate the
species' relationship with environmental variables should encompass extreme
conditions present in the region (e.g., Austin 2002). In this sense, to carry out our
analyses, we chose a study area that contains:
- A remarkable environmental gradient.
- Population nuclei of autochthonous and introduced Iberian red deer,
and native Iberian ibex.
The study area is located in the SE of the Iberian Peninsula. It is 340 km wide
and 270 km long, and 61961 km2 corresponded to dry land (UTM 29N geographic
reference system; NW corner: 450,000, 4,330,000; SE corner: 790,000; 4,060,000;
Figure 2), including the Sierra Nevada mountain range in the SW (rising over 3400
m.a.s.l.), Segura coastal basin in the east (with mean altitudes below 20 m.a.s.l.), as
well as several other mountain ranges and high-altitude plains. Mediterranean
bushlands, oak trees (Quercus spp.) and reforestations with Pinus halepensis and P.
pinaster abound in the study area (see details in Cassinello et al. 2004).
Study ungulates distribution data
Red deer distribution data comes from literature sources and field works
(Braza et al. 1989; Carranza 2002; P. Acevedo and C. Gortázar, unpublished data;
Figure 2). We transformed the available data on deer presence from diverse scales
to 1x1 km UTM grid cells, which is sensible to available local cartography and
climatic information (see Chefaoui et al. 2005; Acevedo et al. 2006a [Capítulo 1.1]).
Tesis Doctoral
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Since the red deer in the study area have two independent population nuclei
regarding their historical origin, we built two different models: one for the
autochthonous population of Sierra Morena (258 grid cells of presence, Braza et al.
1989), and other one for several introduced population nuclei (253 grid cells of
presence, Braza et al. 1989; Carranza 2002; P. Acevedo and C. Gortázar,
unpublished data).
Figure 2. Distribution of ungulate populations in the study area: (a) autochthonous and introduced red deer presences (Braza et al. 1989); (b) Iberian ibex presences (Pérez et al. 2002; Acevedo et al. 2006a [Capítulo 1.1]).
Capítulo 2
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Iberian ibex distribution data were obtained from Pérez et al. (2002) and
Acevedo et al. (2006a [Capítulo 1.1]) and it was transformed to the same scale used
for red deer presences. We considered 199 grid cells of ibex presence for the
analyses (Figure 2).
Environmental data
Many factors have been described to affect the population abundance and
distribution of ungulate species in the Iberian Peninsula (e.g., Acevedo et al. 2005,
2006b). We selected 17 variables that could act as constraints of red deer and
Iberian ibex distributions in SE Iberian Peninsula (Table 1), these variables cover the
range of climatic and ecological traits present in the study region. Environmental
predictors can exert direct or indirect effects on species, arranged along a gradient
from proximal to distal predictors (Austin 2002), and are optimally chosen to reflect
the three main types of influences on the species: regulators, disturbances and
resources (sensu Guisan and Thuiller 2005).
Table 1. Variables used in the analyses (including abbreviations). See text for details and data sources.
Variables (unit) Codes
CLIMATE Winter rainfall (mm) PW
Summer rainfall (mm) PSm Mean summer temperature (ºC) TSm
Annual range of temperatures (ºC) TRn GEOMORPHOLOGY
Maximum altitude (m) AltMx Altitude range (m) AltRn
Mean slope (degrees) Slp Maximum slope (degrees) SlpMx
HABITAT STRUCTURE Forest area (%) HFr
Distance to coniferous forest area (m) DCFr Distance to broadleaved forest area (m) DBFr
Bushland area (%) HBsh Xeric-leave bush area (%) HXBsh
Distance to humid-leave bush area (m) DHBsh HUMAN PRESSURE
Distance to urban areas (m) DUr Distance to the nearest road (m) DRd
Wild Ungulates Landscape Avoidance Index WULAI
Tesis Doctoral
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All climate variables are courtesy of the Spanish Instituto Nacional de
Meteorología (http://www.inm.es/). Geomorphology variables were obtained from an
Iberian Digital Elevation Model of 100 m pixel width. Habitat structure variables were
obtained from the 250 m pixel width land use information of the CORINE NATLAN
European project (EEA 2000). Finally, three variables accounting for human activity
in the study area were obtained. Firstly, distance to urban areas (i.e. to the urban and
industrial categories following CORINE land use map), and distance to the nearest
road (including motorways and national and local roads, extracted from the Spanish
National Digital Atlas, courtesy of the Instituto Geográfico Nacional;
http://www.ign.es/) .
In addition, we used a Wild Ungulates Land Avoidance Index (WULAI), an
index based in the degree of alteration of landscapes by human activity and its
resultant potential avoidance by wild ungulates (Cassinello et al. 2006, [Capítulo 3.1]). Land use variables received a score according to the degree of alterations
caused by human activity, i.e., the further to the natural habitat the higher the score
(up to 100). Thus, in the original CORINE NATLAN map we assigned 100 to urban
and other constructed areas; 50 to irrigated croplands; 30 to fruit orchards and
patchy crops; 20 to vineyards; 10 to dry crops, olive groves, managed grasslands
and mosaic of crops and natural vegetation; and finally 0 landscape avoidance to
forest, bare rock, bushlands and natural grasslands. Then, mean score per 1 km2
pixel was calculated to obtain WULAI scores, ranging from 0 (minimum avoidance,
maximum preference) to 100 (maximum avoidance, minimum preference).
All variables were handled and processed in Idrisi 32 software (Clark Labs
2004). All predictors were standardized to 0 mean and 1 standard deviation to
eliminate the effect of measurement-scale differences.
Statistical methods
A variety of methods are currently available to model species distributions
(Guisan and Zimmerman 2000; Scott et al. 2002). These techniques either consider
only presence data (enveloping models) or both presence and absence data (group
discrimination techniques). The latter work more accurately when reliable absence
data of species are available (Hirzel et al. 2001; Segurado and Araújo 2004). When a
Capítulo 2
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given species is not detected in areas with theoretically suitable environmental
conditions, pseudoabsences can be obtained from available presence records
(Schadt et al. 2002; Zaniewski et al. 2002), or by distinguishing the most probable
absence localities through niche-based modelling of presence alone (Engler et al.
2004).
The two statistical methods used to model the study populations were: i)
Ecological Niche Factor Analyses (ENFA), and ii) Generalized Linear Models (GLM).
Here, ENFA was only used to obtain pseudoabsences from which the distribution
models were built through GLMs (Engler et al. 2004).
i) ENFA (Hirzel et al. 2002) is a method based on a comparison between the
environmental niche of the species and the environmental characteristics of the
entire study area (stored as GIS layers). Hence, ENFA only needs a set of presence
data and a set of background GIS predictors (Hirzel et al. 2001). Because most of the
information is usually contained in a few first factors (see ibid.), only these are kept to
compute the final Habitat Suitability map (HS map). All cells in the map obtain a HS
value that is proportional to the distance between their position and the position of
the species optimum in the new factorial space.
The generation of pseudoabsences was done by ENFA predictions, i.e. by the
HS map. The absences were chosen at random, but only in areas where predictions
by the ENFA were lower than 0.1 (see Engler et al. 2004). To avoid bias due to
inclusion of a comparatively higher number of absences (Kink and Zeng 2001), a
number of absences 10 times higher than the number of presences were selected
(see Lobo et al. 2006). All ENFA analyses were performed within the Biomapper
software (Hirzel et al. 2004).
ii) GLM (McCullagh and Nelder 1989; for habitat suitability studies application
of GLM see Guisan et al. 2002) are an extension of the classical multiple regression,
allowing non-normal response variables to be modelled. GLM (binomial with
logarithmic link function) were used here to model presence – pseudoabsence of the
study species. To select the most parsimonious model, we used a forward stepwise
model-selection procedure (see Engler et al. 2004). The statistic used to select the
final model was the Akaike Information Criteria (AIC; Chambers and Hastie 1997). All
calculations were made using STATISTICA software (StatSoft 2001).
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The Receiver Operating Characteristic (ROC, Zweig and Campbell 1993),
from a plot of sensitivity (ratio of correctly predicted positives to the total number of
positives cases) and specificity (ratio of correctly predicted negative cases to the total
number of negative cases), was used to measure of performance of models (e.g.,
Lobo et al. 2006). To compare observed and predicted maps, the continuous
probability variable generated by logistic regression should be converted to a binary
one (presence – absence), selecting a threshold cut-off point which minimizes the
difference between sensitivity and specificity (Liu et al. 2005). The area under the
ROC function (AUC), independent of the presence – pseudoabsence threshold
(Fielding 2002), is the best measure of model prediction accuracy.
We have evaluated by means of one way ANOVA if red deer introductions
were carried out on suitable areas according to the autochthonous population
realized niche. To evaluate the relationship between the HS maps obtained in the
three models, they were reclassified to obtain highly suitable areas for each model,
and then their overlap was analysed.
RESULTS
Attaining the habitat suitability models
Firstly, we carried out the ENFA models, which happened to be quite robust,
as the explained information was higher than 78% in all of them. Based on random
habitat units with a suitability <0.10 according to the ENFA analysis, a series of
random pseudoabsences were selected (2580 for the autochthonous red deer model,
2530 for the introduced one, and 1990 for the Iberian ibex model).
The results obtained in univariate logistic regressions for the three models are
shown in Table 2. The step-up model selection procedure based on the AIC, the
resulting final models and the explained deviance for each one are shown in Table 3.
Table 4 shows the coefficients and significance values of the predictors retained in
the final models. The parameters of the predictive power of the models are
summarized in Table 5 being all models classified as outstanding (sensu Hosmer
and Lemeshow 2000). The habitat suitability values assigned by GLM to the habitat
units are shown in Figure 3.
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One to one comparison between autochthonous and introduced red deer models and Iberian ibex model
The highly suitable areas (HS>0.50) for the autochthonous red deer population
covered 4.34% of the study area, of which 6.70% was highly suitable for the
introduced red deer and 13.47% for the Iberian ibex. On the other hand, the highly
suitable areas for the introduced red deer covered 7.61% of the study area, of which
3.82% was highly suitable for the autochthonous red deer and 81.58% for the Iberian
ibex. Finally, the highly suitable areas for the Iberian ibex covered 13.19% of the
study area, of which 4.43% was highly suitable for the autochthonous red deer and
47.03% for the introduced one (see Figure 3). In addition, we obtained that the red
deer introductions were carried out in areas with lower suitability scores for the
autochthonous red deer population (F1, 509=91.63 , p<0.001).
Table 2. Summary of the results of each univariate model (GLM binomial with logarithmic link function). The Wald statistics and p-values are shown, ns = non-significant. Variable codes as in Table 1.
Autochthonous red deer
Introduced red deer Iberian ibex Variable
codes Wald p Wald p Wald p
AltMx 3.09 ns 368.34 <0.001 245.84 <0.001 AltRn 14.99 <0.001 281.70 <0.001 238.87 <0.001
HFr 2.52 ns 421.83 <0.001 279.40 <0.001 DRd 152.21 <0.001 106.08 <0.001 163.83 <0.001
DCFr 22.16 <0.001 131.03 <0.001 109.64 <0.001 DBFr 3.34 ns 12.54 <0.001 55.982 <0.001
DHBsh 18.49 <0.001 67.99 <0.001 12.12 <0.001 LAI 82.80 <0.001 155.30 <0.001 114.26 <0.001
HBsh 56.66 <0.001 9.10 <0.001 1.94 ns HXBsh 3.56 ns 31.96 <0.001 11.10 <0.001 SlpMx 3.13 ns 287.89 <0.001 223.60 <0.001
Slp 9.02 <0.001 303.27 <0.001 256.21 <0.001 PW 76.88 <0.001 401.88 <0.001 265.91 <0.001
PSm 0.11 ns 314.94 <0.001 170.81 <0.001 TSm 127.06 <0.001 367.13 <0.001 256.73 <0.001 TRn 163.23 <0.001 92.83 <0.001 16.69 <0.001 DUr 127.22 <0.001 191.12 <0.001 187.84 <0.001
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Table 3. Summary of the step-up model selection procedure based on Akaike Information Criterion (AIC). D2 = percentage of the explained deviance. Variable codes as in Table 1.
D2 AIC Autochthonous red deer TRn 66.83 383.24 TRn + DHBsh 79.63 358.19 TRn + DHBsh + DUr 82.34 313.37 TRn + DHBsh + DUr + WULAI 82.89 305.85 TRn + DHBsh + DUr + WULAI + PW 83.38 299.39 TRn + DHBsh + DUr + WULAI + PW + AltMx 84.13 288.41 Introduced red deer PW 47.04 671.57 PW + PSm 60.75 629.49 PW + PSm + AltMx 68.71 604.83 PW + PSm + AltMx + HFr 70.95 551.51 PW + PSm + AltMx + HFr + DUr 71.69 528.61 PW + PSm + AltMx + HFr + DUr + DCFr 72.62 510.69 Iberian ibex AltMx 60.01 533.24 AltMx + DCFr 60.62 525.21 AltMx + DCFr + TRn 68.18 424.44 AltMx + DCFr + TRn + HXBsh 69.67 404.49 AltMx + DCFr + TRn + HXBsh + DHBsh 75.16 331.25 AltMx + DCFr + TRn + HXBsh + DHBsh + DUr 77.00 306.78 AltMx + DCFr + TRn + HXBsh + DHBsh + DUr + SlpMx 78.61 285.26
Table 4. Coefficients and significance values of the exploratory variables entered in the final models (p-values are shown ** = p<0.01) for the three study ungulate populations. Variable codes as in Table 1.
Autochthonous red deer Introduced red deer Iberian ibex Variable
codes Estimate Wald Estimate Wald Estimate Wald
(Intercept) -15.30 81.01** -4.69 339.69** -7.64 132.58** WULAI -1.08 10.35** - - - -
DUr 0.63 13.06** 0.86 49.35** 0.96 35.56** AltMx 1.95 13.27** - - 2.24 105.53** PW -2.28 18.04** 0.72 56.58** - -
DHBsh -3.44 60.27** - - 1.40 37.30** TRn 11.34 102.68** 0.86 17.61** 2.35 45.51** PSm - - 1.61 81.26** - - HFr - - 0.58 27.01** - -
DCFr - - -1.19 19.80** -7.27 44.18** HXBsh - - - - -1.10 21.67** SlpMx - - - - 1.03 19.92**
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Table 5. Summary of the statistical values of the habitat suitability models
Models AUC values
Cut-off values
Sensitivity (%)
Specificity (%)
Autochthonous red deer 0.97 0.24 98.45 98.18 Introduced red deer 0.96 0.37 91.70 91.15 Iberian ibex 0.97 0.26 95.98 96.03
Figure 3. Habitat suitability maps for the Iberian red deer and ibex in the south east of Spain: (a) autochthonous red deer population, (b) introduced red deer population, (c) Iberian ibex population.
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DISCUSSION
In this study, we provide evidence of differing realized niche for Iberian red
deer populations of different origin in the SE of the Iberian Peninsula: a native
population, with its own dispersal tendencies, and an introduced one, expanded by
human game interests. Our goal was also to test whether introduced populations
may become a threat to other sympatric autochthonous ungulates, by niche
overlapping. This seems to be the case of the Iberian ibex.
Environmental niches of autochthonous and introduced red deer populations
The potential distribution of the native red deer population is very restricted in
the study area, practically circumscribed to Sierra Morena mountain range. On the
contrary, the distribution obtained for the introduced red deer populations in the same
area is completely different, scarcely overlapping with the suitable areas of the
autochthonous deer, and showing a wide area of potential distribution. Our analyses
showed that the red deer was introduced in places with poorly environmental
characteristics according to the realized niche of the native populations.
One of the first interpretations of our results would be that the red deer
expresses a high ecological plasticity (e.g., Hofmann 1985; Gebert and Verheyden-
Tixier 2001); adapting to suboptimal ecological conditions in areas where it is
introduced (Mátrai et al. 2004). The successful establishment of these populations, in
habitats outside their ecological range and dispersal potential, identifies them to non-
native invasive species (see Falk-Petersen et al. 2006), which may originate severe
ecological disturbances in the host environment, so that, if not extirpated, at least
they should be carefully monitored (e.g., Moriarty 2004). Such disturbances can
affect the natural vegetation, other native animal species, and the own introduced
population.
Concerning mountainous habitats, in the study region there are several
Natural Parks where endemic plant species abound (Gómez-Mercado 1989), so that
they may be under threat due to the presence of introduced large herbivores. Given
that local plant and animal species may have evolved without such herbivore
pressure, these invasive species can substantially influence the composition and
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structure of plant and animal communities (Mack et al. 2000; Holmgren 2002;
González-Megías et al. 2004).
Under invasive species presence, the conservation of native animal species is
facing a series of risks, such as hybridization (e.g., Goodman et al. 1999; Carranza et
al. 2003), and competition (e.g., Forsyth and Duncan 2001). Also, the introduction of
uncontrolled individuals may originate the prevalence of new diseases (Hofle et al.
2004).
Finally, if invasive populations of red deer succeed and find no ecological
constraints they may reach high densities, there being a chance for overabundance-
driven consequences to arise, such as a decrease of fitness and a higher prevalence
of parasite and infectious diseases (Gortázar et al. 2006).
Which environmental traits explain better the autochthonous and introduced red deer distributions?
According to the GLM carried out to obtain the realized niche of the study
species, the native population is distributed in areas characterized by a high
temperature range, nearest to humid-leave bush areas, with a low winter rainfall
regime, high altitudes, far from human population nuclei, and where human
perturbations on landscape are low (WULAI low values) (Table 4).
These results are generally in agreement with the expected red deer habitat
requirements in the Iberian Peninsula (Carranza et al. 1991; Soriguer et al. 1994;
San José et al. 1997; Bugalho and Milne 2003), and in other European countries
(Morellet et al. 1996; Latham and Staines 1997; Debeljak et al. 2001). The red deer
live under Mediterranean climatic conditions and their presence in the Iberian
Peninsula has traditionally been associated with a well-developed Mediterranean-
type bush lands with small areas of pastures scattered among densely wooded areas
(Caballero 1985).
Our results suggest that the native red deer population stands for relatively
high seasonal bioclimatic variations, as it is positively related to the annual range of
temperatures (see Latham and Staines 1997; San José et al. 1997). Under this
scenario, summer is the critical period when high temperatures provoke food
shortage, as herbaceous vegetation becomes senescent (Álvarez and Ramos 1991),
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a situation resembling that described for the red deer in Scotland in winter (Clutton-
Brock and Albon 1989). Small size ungulates, such as the Iberian ibex or roe deer,
need higher quality resources than larger ones, such as the red deer, that take more
advantage from low nutritional quality plants (Gordon 1989). This may partly explain
why the red deer shows well-established populations in its native area of distribution
(Figure 2; Vicente et al. 2006), in comparison with other native ungulate species
(Pérez et al. 2002). The red deer is a mixed feeder (Hofmann 1989), being capable
of ingesting high proportions of browse during the summer (Zamora et al. 2001).
Feeding studies showed that the humid-leave bushes contributed a 30% in the red
deer diet in Mediterranean mountain ranges (Soriguer et al. 1994). This habitat also
provides suitable micro-climatic conditions, i.e. refuge (see Soriguer et al. 1994),
mainly during the critical annual periods (Lazo et al. 1994).
A highly significant relationship between habitat suitability and the intensity of
human disturbance has been appreciated in the autochthonous red deer model (see
Table 4). Humanized landscapes with moderate-to-high avoidance index scores
appear not to be suitable for the species. The effect of human population nuclei on
red deer distribution has already been reported by other authors (Debeljak et al.
2001). The red deer seems to be positively associated to the least human-induced
landscapes, similarly to other deer species (Morellet et al. 1996; Hewison et al. 2001;
but see Acevedo et al. 2005).
On the other hand, the introduced red deer populations are distributed in areas
characterized by high summer and winter rainfall regimes, far from human population
nuclei, high percentage of woodlands, close to coniferous forest, and high
temperature range (Table 4). These results are in agreement with red deer habitat
requirements in areas where the species has been introduced in the Iberian
Peninsula, e.g., Cazorla Natural Park (Soriguer et al. 1994).
Two preferred forest types emerged from the model, proximity to coniferous
forests and the proportion of woody plants (Table 5). The genus Pinus spp. is an
important food source in poor areas and during shortage periods for deer species
(Matrai and Kabay 1989; Debeljak et al. 2001), as well as for other Iberian ungulates
(Martínez 1994). In winter time, coniferous forests has more suitable micro-climatic
conditions due to its dense canopy layer (Telfer 1988), which offers shelter and safer
refuges against predators (carnivores and humans), contrary to broadleaf stands
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(Nyberg 1990). It is remarkable that habitat requirements and potential distribution of
the introduced red deer populations are close to the Iberian ibex ones (Figure 3;
Acevedo et al. 2006a [Capítulo 1.1]), whereas the native red deer does not follow
this pattern (see below).
Furthermore, WULAI was not retained in the introduced red deer model; a
plausible explanation might be that introductions were carried out in relatively high
human-transformed landscapes, where red deer would have adapted to (e.g.,
Morellet et al. 1996). It has already been reported that deer spatial use may differ
depending on local conditions (Beier and McCullough 1990). Also, Lazo et al. (1994)
showed that deer density is the most influential factor on habitat and space use,
mainly in males.
Niche comparison between red deer study populations and Iberian ibex
Red deer introductions in the Iberian Peninsula, basically due to game
interests (Braza et al. 1989; Gortázar et al. 2000), have been carried out without any
previous ecological study. This might explain the differences found between the
realized niches occupied by the same species in our study. Areas where the red deer
has been introduced, suitable for sport hunting, are typically of low productivity,
rugged high altitude areas, and in many instances home of the native Iberian ibex.
Furthermore, our results suggest that the introduced red deer have similar habitat
requirements and potential distribution than the native Iberian ibex, since their
suitability maps extraordinarily resemble to each other (Figure 3), and a 81.58% of
the highly suitable areas are overlapped. The autochthonous red deer, however,
presents a different potential distribution in the study area (see Figure 3), there being
a scarce overlap with the Iberian ibex one.
The introduction of red deer in habitats typically occupied by the Iberian ibex
might represent a threat for the latter. High diet overlap between both species has
been reported (Martínez et al. 1992), so that interspecific competition might occur,
particularly when resources are limited. Also, higher body size may represent an
advantage for the red deer when competing for resources (e.g., Gordon 1989).
Competition occurring, there is a risk of displacement of Iberian ibex population to
suboptimal habitats (see Acevedo et al. 2006a [Capítulo 1.1]).
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When high population densities are reached along with limited food
availability, high parasite abundances can be expected due to a loss of fitness and
increased aggregations (Gortázar et al. 2006). This could be another effect of wildlife
introductions as was apparently the case of the sarcoptic mange (Sarcoptes scabiei)
outbreaks in the Iberian ibex populations of Cazorla (León-Vizcaíno et al. 1999).
Since these human-induced introductions have originated the presence of the
red deer in new habitats, where the species has successfully established, we might
be before a particular case of biological invasion. This involves two essential stages:
transport of an organism to a new location (Mack et al. 2000), and establishment and
population increase in the invaded locality (Veltman et al. 1996). A third stage,
applicable to most of the invasions, is regional spread from initial successful
populations (Shigesada and Kawasaki 1997). The effects of environmental
constraints, if any, on introduced red deer populations in SE Spain may have been
mitigated by game management strategies, such as the use of fenced, protected
against predators estates, extra feeding and watering (see Vicente et al. 2006). On
the other hand, an invader will be at an advantage if its maintenance requirements
are lower than those of a resident even under environmental harshness, or if it has a
stronger response to increased resources than the resident (Shea and Chesson
2002).
ACKNOWLEDGEMENTS
We are indebted to A. Jiménez-Valverde for his help on the statistical
procedures, J. Hortal for his comments on a previous version of the manuscript, and
J. Lobo, A. Jiménez-Valverde, R. Chefaoui and J. Hortal for providing GIS
information. JC is currently enjoying a Ramón y Cajal research contract at the CSIC
awarded by the Ministerio de Educación y Ciencia (MEC); he is also supported by
the project PBI-05-010 granted by Junta de Comunidades de Castilla-La Mancha.
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CAPÍTULO 3
3.1.- PERSPECTIVAS DE LA EXPANSIÓN POBLACIONAL DEL ARRUI (AMMOTRAGUS LERVIA, BOVIDAE) EN LA PENÍNSULA IBÉRICA: USO DE MODELOS DE ADECUACIÓN DE HÁBITAT 3.2.- ES EL ARRUI (AMMOTRAGUS LERVIA) UNA AMENAZA PARA LA CABRA MONTÉS (CAPRA PYRENAICA)? UNA APROXIMACIÓN BASADA EN MODELOS DE ADECUACIÓN DE HÁBITAT
LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR EL HOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO: EL CASO DE UNA ESPECIE EXÓTICA, EL ARRUI, Y LA CABRA MONTÉS
3.1.- PERSPECTIVAS DE LA EXPANSIÓN POBLACIONAL DEL ARRUI
(AMMOTRAGUS LERVIA, BOVIDAE) EN LA PENÍNSULA IBÉRICA: USO
DE MODELOS DE ADECUACIÓN DE HÁBITAT
Cassinello, J., Acevedo, P., Hortal, J. (2006) PROSPECTS FOR POPULATION
EXPANSION OF THE EXOTIC AOUDAD (AMMOTRAGUS LERVIA; BOVIDAE) IN THE IBERIAN
PENINSULA: CLUES FROM HABITAT SUITABILITY MODELLING. Diversity and
Distributions 12, 666-678.
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RESUMEN
Se ha estudiado la distribución geográfica y la adecuación de hábitat del arrui
(Ammotragus lervia), ungulado introducido y actualmente en expansión en el sureste de la
Península Ibérica. Se ha evaluado el nicho de la especie usando el Análisis Factorial de
Nicho Ecológico (ENFA) sobre i) variables medioambientales (clima y tipo de hábitat), y ii)
índice de evitación del paisaje del arrui y otras variables relacionadas con alteraciones en el
medio producidas por el hombre. Ambas descripciones del nicho han sido comparadas para
estudiar el impacto de las interferencias humanas sobre la selección de nicho de la especie.
Los modelos ENFA se han calibrado usando datos de la población original de arrui en la
Península Ibérica, Sierra Espuña, y se han validado usando datos de otra población libre,
originada de forma independiente, en la provincia de Alicante. El modelo de adecuación de
hábitat para el nicho puramente ambiental predice una distribución potencial para el arrui a
lo largo de un eje suroeste-noreste, siguiendo la Cordillera Subbética, y está limitado por
una baja precipitación en invierno, altas altitudes, fuertes pendientes y por la presencia de
bosques. Además de estos condicionantes ecológicos, las carreteras y el uso humano del
medio restringen la potencialidad ambiental para el arrui. Teniendo en cuenta que,
potencialmente, el arrui es un competidor de los ungulados nativos y una amenaza para la
flora endémica, el estudio de sus tendencias expansivas puede ser de gran valor para la
conservación.
ABSTRACT
We studied the geographic distribution and habitat suitability of an introduced
ungulate, the aoudad (Ammotragus lervia), that is currently expanding its range in
southeastern Iberian Peninsula. We assessed the niche of the species using Ecological
Niche Factor Analysis (ENFA) on i) environmental variables (climate and habitat type), and ii)
potential aoudad landscape avoidance and human disturbance variables. We compared both
niche descriptions to study the impact of human interference on niche selection of the
species. ENFA models were calibrated using data on the population growth from the original
release location, in Sierra Espuña mountains, and validated using data from another free-
ranging population, originated independently in the Alicante province. The habitat suitability
model for the purely environmental niche predicts a potential distribution along a SW-NE axis
in the study area, following the Cordillera Sub-Bética mountain range, being constrained by
low winter precipitation, high altitude, high terrain slope and the presence of forest. In
addition to these ecological traits, roads and landscape use restricted the environmental
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range potentially available for the species. Since the aoudad is a potential competitor of
native ungulates and a threat to endemic flora, prospects for its potential dispersion might be
of great conservation value.
INTRODUCTION
Both passive and active human actions have facilitated the transportation of
species outside their original distribution range and habitats. Introduction of exotic
species has become a serious issue in conservation ecology, resulting in the birth of
a new discipline, the study of biological invasions (e.g. Hengeveld 1989; Lodge 1993;
Ruesink et al. 1995; Mooney and Hobbs 2000; Sax et al. 2005). It has been generally
assumed that invasive alien species pose one of the greatest threats to biodiversity
(Diamond 1989; Wilcove et al. 1998; but see also Sax and Brown 2000; Brown and
Sax 2004; Gurevitch and Padilla 2004; Didham et al. 2005; Borges et al. 2006). In
this context, the interest in game species has played a major role in spreading many
exotic mammals (e.g., Crosby 1986; Macdonald et al. 1988; Jaksic et al. 2002;
Richardson et al. 2003). These introductions were often carried out without regard for
their effects on the environment, e.g. threats to native species and endemic flora
(e.g., Mack and D'Antonio 1998).
The aoudad, Ammotragus lervia Pallas 1777, is a North African caprid
successfully introduced as a game species in mountainous desert regions of Texas,
New Mexico and California in USA (Ogren 1965), and southern Spain (Cassinello
2000). The aoudad has shown a formidable capacity to establish, spread and extend
its distribution (Gray 1985; Cassinello et al. 2004), the characteristics typical of
biological invasions (Williamson 1996). During the phase of establishment of an
invasive species a series of factors that determine success operate in a stochastic
manner primarily on mortality and sex ratios. Spread occurs when an established
population grows in size and increases in distribution, thereby escaping stochastic
extinction effects (Soulé 1987).
Very few individuals are required for introduced ungulate populations to
become established (Forsyth and Duncan 2001). The aoudad, which is native to the
Saharan Desert mountains where resources are scarce and sparsely distributed,
encountered richer habitats where it was introduced in USA and Spain. Increased
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food availability, along with a scarcity of competitors and predators, allowed high birth
rates, and a swift spread of the population (see Wolf et al. 1996). Following Colautti
and MacIsaac’s (2004) terminology, in this region the aoudad is in the process of
changing from Stage III (localized and not dominant) to Stage IVa (widespread but
not dominant). Here we analyse several environmental and anthropogenic factors
(both humanized landscape configuration and human degree or disturbance) that
might be influencing the spread of the introduced aoudad population in southeastern
Spain. This knowledge may help to establish management procedures to prevent
further range expansion, and reduce the potential negative effects of the aoudad on
native fauna and flora.
The relationship between environmental variation (temperature, precipitation,
humidity) and the survival of a species can be used to model its potential response to
environmental gradients (Austin et al. 1990). These descriptions can be used to
produce predictive maps of species distribution (see reviews at Guisan and
Zimmermann 2000; Ferrier et al. 2002; Scott et al. 2002; Guisan and Thuiller 2005),
as well as to describe the characteristics of the niche of the species (see, e.g.,
Peterson et al. 1999; Robertson et al. 2001; Soberón and Peterson 2005; Araújo and
Guisan 2006). In conjunction with the use of modern statistics, predictive models
have become powerful tools to address relationships between species and their
environment, being increasingly common in ecological literature. They gained
importance as a research tool on conservation issues (see Araújo and Guisan 2006;
Guisan et al. 2006), especially to assess the effect of climatic change on the
distribution of organisms (e.g., Thuiller et al. 2006), to study species niche (Guisan
and Zimmermann 2000) and the spatial patterns of biodiversity (e.g., Hortal et al.
2004). A variety of methods have been used to analyse the ecological niche of the
species from data on their presence (see Guisan and Zimmermann 2000; Soberon
and Peterson 2005). Among others, there are methods based on presence-only data,
such as BIOCLIM (Hortal et al. 2005); methods that can handle with presence-only
data, among others, such as ENFA, GARP (e.g., Anderson 2002) or MAXENT (see,
e.g., Guisan et al. 2006); methods based on both presence and absence (or
pseudoabsence) data, such as GLM (Lobo et al. 2006) (see a review of the
performance of a number of methods at Elith et al. 2006). In addition to these
methods, others try to develop resource selection methods from data on the
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abundance of the species (e.g., Olivier and Wotherpoon 2005; Boyce 2006; Meyer
and Thuiller 2006).
The adaptation of niche theory to species distribution modelling is currently
under debate (Soberón and Peterson 2005; Araújo and Guisan 2006). Since, current
terminology is rather ambiguous, and therefore could be misleading for the
development of a general framework (Araújo and Guisan 2006), a clear definition of
the niche concepts used is needed when studying the geographic response of a
species. To clarify the two different expressions of the geographic response of the
aoudad, we use two different definitions of aoudad’s geographic response based on
Soberón and Peterson's (2005) and Araújo and Guisan's (2006) recent works:
Environmental Niche (similar to Soberón and Peterson’s Fundamental Niche), which
is merely the response of the species to abiotic factors, and Observed Niche
(following Araújo and Guisan 2006), which includes its interactions with the biotic part
of the studied systems, in our case landscape configuration and human disturbance.
In fact, following Araújo and Guisan (2006), the Environmental Niche could be better
described as the Observed Environmental Niche, but we have preferred the term
Environmental Niche throughout the text for the sake of clarity.
Ecological Niche Factor Analysis (ENFA; Hirzel 2001; Hirzel et al. 2001, 2002)
provides a good tool to describe the geographic expression of the niche of a species.
This ordination technique identifies the main gradients that a species responds to in
an area. ENFA uses presence-only, presence/absence or abundance data to
compute a number of orthogonal factors from several predictors. Since these factors
are built to maximize the discrimination between the areas where the species is
present, compared to the rest of the region, they might be seen as the most
important gradients the species is responding to in the study area (Hirzel et al. 2002;
see also Chefaoui et al. 2005). It is then assumed that the response of a species
along the principal axes constitutes a description of its observed niche (i.e. the spatial
expression of its niche with regard to habitat conditions included within the
predictors). ENFA methodology has been successfully used to model the
environmental response of other caprids in their native range (Capra ibex, Hirzel
2001; Capra pyrenaica, Acevedo et al. 2006 [Capítulo 1.1]) as well as of
reintroduced populations (e.g., Gypaetus barbatus in Switzerland, Hirzel et al.
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2004a). Note that several other approaches are available to build spatial predictions
from presence only data (Hortal et al. 2005; see a comparison in Elith et al. 2006).
We used ENFA, as well as the derived niche description method proposed by
Chefaoui et al. (2005; see also Hortal et al. 2005), to: a) model the potential
distribution of the introduced aoudad in the southeastern Iberian Peninsula; b) study
the environmental determinants underlying the aoudad's spatial response (i.e. its
environmental niche); and c) evaluate the effect of landscape structure and human
disturbance on such response (i.e. its observed niche).
MATERIALS AND METHODS
The study area
To properly define the geographic niche of a species within a given region, the
area used to investigate the species' relationship with environmental variables should
encompass extreme conditions present in the region. Thus, to carry out ENFA
analyses, we chose a study area that contains both the aoudad population nuclei,
and the coastal and mountain environments present in SE Iberian Peninsula. The
study area was 340 km wide and 270 km long, and 61961 km2 corresponded to dry
land (UTM 29N geographic reference system; NW corner: 450,000, 4,330,000; SE
corner: 790,000; 4,060,000; Figure 1), including the Sierra Nevada mountain range in
the SW (rising over 3400 m.a.s.l.), Segura coastal basin in the east (with mean
altitudes below 20 m.a.s.l.), as well as several other mountain ranges and high-
altitude plains. The study area comprised a number of sub-areas defined by the
vegetation succession series present, which identify plant communities and soil
composition (Rivas Martínez 1987). Mediterranean bushlands, oak trees (Quercus
spp.) and reforestations with Pinus halepensis and P. pinaster abound in the study
area (see details in Cassinello et al. 2004).
The study species
The aoudad, a North African caprid (subfamily Caprinae), is now a common
inhabitant of southeastern Spain having been introduced as a small population (16
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males and 20 females) in Sierra Espuña Natural Park in 1970 (see details in
Cassinello 2000; Cassinello et al. 2004). Since then the population has increased
rapidly and by 1990 around 2,000 individuals were estimated to inhabit the Sierra
Espuña and surroundings mountains (ARMAN 1991).
Figure 1.- Location of the study area in southeastern Spain. Province boundaries are shown. The records of the aoudad presence are depicted. The southernmost group (circles) corresponds to the dispersion of the Sierra Espuña nucleus, whereas the eastern ones (squares) are the nuclei in the Alicante province. The geographic coordinate system shown is the UTM.
A sarcoptic mange episode affected the aoudad population in 1991, during
which time the numbers of aoudad decreased by over 90% (González-Candela and
León-Vizcaíno 1999). However, the aoudad population recovered very quickly in the
area, and is currently estimated to be over 1,000 individuals (González-Candela et al.
2004). Apart from the population that originated in the Sierra Espuña, since 1990
another free-ranging population of aoudads has established in the Alicante province,
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originating from escapes from two game estates in the area (Serrano et al. 2002;
Cassinello et al. 2004).
Data origin
Distributional data
The aoudad presence data come from Cassinello et al. (2004), and were
obtained by surveys conducted intermittently during 3 years (from 1999 to 2001),
mainly during August, September and October, the beginning of the mating season,
when animal visibility is enhanced (Solbert 1980; Gray and Simpson 1982, 1983; J.
Cassinello, pers. obs.).
In geographically explicit analyses, the spatial resolution (grid cell size)
constitutes a key decision for the accuracy and reliability of the results (see Chefaoui
et al. 2005). In this study, we transformed the available data on aoudad presence
(Cassinello et al. 2004) from 100 x 100 m UTM grid cells to a 1 x 1 km UTM grid
cells. This could create error and scale problems, but previous studies have shown a
degree of correlation in species' distribution patterns across narrow ranges of scales
(Hartley et al. 2004).
Since free-ranging aoudads in the study area have two independent
population nuclei, we used one population to calibrate ENFA models (Sierra Espuña
population nucleus, n=60 records), and the other, as an independent set, for the
empirical evaluation of the predictive maps (Alicante population nuclei, n=22
records).
Environmental data
Data from an Iberian GIS database compiled and managed by J. M. Lobo, A.
Jiménez-Valverde, R. M. Chefaoui and J. Hortal (for details contact JH, or see
http://www.biogeografia.com/ for additional information) was imported and processed
into the raster-based Idrisi GIS System (Clark Labs 2001, 2004). A set of GIS maps
for the study area was produced, including a number of continuous variables that
were thought to determine the aoudad distribution (see below). All of the variables
were extracted at a 1-km2 resolution, corresponding to the chosen resolution of
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aoudad presence data. This grain size chosen for the analyses is a consensus
between the spatial accuracy of biological data, the mobility of the aoudad, and the
large spatial extent used (see another example at Chefaoui et al. 2005).
Many climatic and ecological factors have been used to explain the variations
in population abundance and distribution of ungulate species in the Iberian Peninsula
(e.g., Acevedo et al. 2005, 2006 [Capítulo 1.1]). Here, we selected 42 variables that
could act as determinants of current aoudad distribution in SE Iberian Peninsula; 38
accounting for environmental variation (climate, habitat structure, vegetation
characteristics and geomorphology), one index of the adequacy of landscape to
aoudads, and four for direct human disturbance (Table 1):
i) Seventeen climate variables were obtained from the monthly values of the
digital version of the Spanish National Climate Atlas (provided by the Instituto
Nacional de Meteorología; freely available at http://www.inm.es/); four accounting for
seasonal precipitations (mm), twelve accounting for the mean, maximum and
minimum temperature at each season (ºC), and one accounting for the annual range
of temperatures (ºC).
ii) Nine geomorphology variables were extracted for each 1 km2 pixel from an
Iberian Digital Elevation Model of 100 m pixel width extracted from a global DEM
(Clark Labs 2000): mean, maximum and minimum altitude (m.a.s.l.), altitude range
(meters), mean, maximum and minimum slope (degrees), percentage of area with
slopes greater than 30º, and mean aspect diversity, using a 7x7 pixel kernel on a 9-
categories reclassified aspect map (see Clark Labs 2001, 2004 for the method; and
Chefaoui et al. 2005 for an example of the use of this variable).
iii) Habitat structure variables were obtained from the 250 m pixel width land
use information of the CORINE NATLAN European project (EEA 2000); six variables
accounting for land cover (Table 1) were extracted as percentages of each land
category per 1 km2 pixel, whereas mean land use diversity was obtained with the
same technique as aspect diversity.
iv) Five variables account for the type of vegetation available, according to its
nutritional value; the information on vegetation composition coming from the digital
version of the Spanish National Forest Map (Ruiz de la Torre 2002) was rasterized to
a 100 m pixel width resolution, and reclassified to obtain the surface of each 1 km2
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pixel occupied by pine trees (Pinus sp.), xeric-leaved trees (e.g., Quercus ilex,
Juniperus sp.), humid-leaved trees (e.g., Quercus pyrenaica, Fraxinus sp.), xeric-
leaved bushes (e.g., Cistus sp.), and humid-leaved bushes (e.g., Pistacia sp.).
v) A landscape avoidance index was created by combining available land use
map and the degree of alteration made by human activity in comparison to natural
habitats. This index was based on potential land avoidance by the aoudad rather
than landscape preference or use, and could be applicable to most Mediterranean
wild ungulates. We have denominated it Wild Ungulates Land Avoidance Index
(WULAI). Land use variables receive a score proportional to the rareness of
encountering aoudads in these landscapes, i.e., the further to the original habitat the
higher the score (up to 100). Thus, in the original CORINE NATLAN map (100 x 100
m pixel resolution; EEA 2000) we assigned 100 to urban and other constructed
areas; 50 to irrigated croplands; 30 to fruit orchards and patchy crops; 20 to
vineyards; 10 to dry crops, olive groves, managed grasslands and mosaic of crops
and natural vegetation; and finally 0 landscape avoidance to forest, bare rock,
bushlands and natural grasslands. WULAI scores were averaged across each
square kilometre, ranging from 0 (minimum avoidance, maximum use) to 100
(maximum avoidance, minimum use).
vi) Finally, four distance variables account for potential human disturbance
(see, e.g., Osborne et al. 2001; Schadt et al. 2002): the distance to urban areas,
roads, and first order roads (highways and national level roads), calculated with the
Distance Operator tool of Idrisi 32 software. In addition, the distance to the Sierra
Espuña population nucleus (DSE), i.e. the original release location (Cassinello 2000),
was used in several analyses, to account for the recent dispersion of the species
(see Acevedo et al. 2005).
All variables were Box-Cox normalized prior to their use in the ENFA analyses.
Statistical Analyses
Niche modelling
ENFA analyses were conducted using BioMapper (Hirzel et al. 2004b; freely
available at http://www.unil.ch/biomapper/). This software uses the ENFA
methodology to produce predictive maps of habitat suitability (i.e., potential
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distribution) from GIS information (see applications at Hirzel 2001; Hirzel et al. 2001,
2002; Hirzel and Arlettaz 2003; Gallego et al. 2004; Hirzel et al. 2004a; Chefaoui et
al. 2005; Hortal et al. 2005; Acevedo et al. 2006 [Capítulo 1.1]). We developed two
different ENFA analyses, one to describe the Environmental Niche (herein,
environmental niche model) using the variables in the first four of the above-
mentioned groups and using all variables present in the six groups above to describe
the likely Observed Niche. Table 1.- Variables used in the analyses (including abbreviations). See text for details and data sources. Climate Geomorphology PW Precipitation in winter (mm) Alt Mean altitude (m) PF Precipitation in autumn (mm) AltMx Maximum altitude (m) PSp Precipitation in spring (mm) AltMn Minimum altitude (m) PSm Precipitation in summer (mm) AltRn Altitude range (m) TW Mean temperature in winter (ºC) Slp Mean slope (º) TF Mean temperature in autumn (ºC) SlpMx Maximum slope (º) TSp Mean temperature in spring (ºC) SlpMn Minimum slope (º) TSm Mean temperature in summer (ºC) Slp30 Area with slope > than 30º (%) TMxW Maximum temperature in winter (ºC) AspDv Aspect diversity (H’ index) TMxF Maximum temperature in autumn (ºC) TMxSp Maximum temperature in spring (ºC) Habitat structure TMxSm Maximum temperature in summer (ºC) HFr Forest area (%) TMnW Minimum temperature in winter (ºC) HCFr Coniferous forest area (%) TMnF Minimum temperature in autumn (ºC) HBFr Broadleaved forest area (%) TMnSp Minimum temperature in spring (ºC) HBsh Bushland area (%) TMnSm Minimum temperature in summer (ºC) HGrs Grassland area (%) TRn Annual range of temperatures (ºC) HDC Dryland crops (%) LUDv Land use diversity (H’ index) Vegetation VHTr Humid-leave tree area (%) Landscape use VXTr Xeric-leave tree area (%) WULAI Landscape Avoidance Index VHBsh Humid-leave bush area (%) VXBsh Xeric-leave bush area (%) Human disturbance VPTr Pine tree area (%) DUr Distance to urban areas (km) DRd Distance to the nearest road (km) DHw Distance to the nearest highway (km) DSE Distance to Sierra Espuña nucleus (km)
These analyses, and the resulting habitat suitability maps, are produced in two
steps:
1. ENFA was used to characterize the response of the aoudad to the main
variations of the used predictors in the study area. ENFA analysis identifies two key
components of species environmental niches: marginality and tolerance, that is, how
rare are the conditions selected by the species within the context of the studied
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region, and how tolerant is the species to modifications of these conditions produced
by secondary gradients (see Hirzel 2001 and Hirzel et al. 2002). Computationally,
marginality is a measure of the distance between the central trend of the species
environmental selection and the mean environmental conditions of the region in the
most important environmental gradient (i.e. the higher the marginality, the more
extreme the conditions with regard to the area studied), and tolerance measures the
range width with regard to all gradients present in the study area (see below), that is,
how the species tolerates environmental variations (varying from 0 to 1; i.e. the
closer to 0, the more specialist the species). In this context, the specialisation of a
species is defined as the inverse of its tolerance. In our study, aoudad presence data
was used to identify a number of orthogonal factors in the predictors, accounting for
the maximum differentiation between mean conditions for the study area, and mean
conditions where the aoudad was found. The first factor (Marginality Factor) accounts
for the marginality of the species, whereas the other factors (Specialization Factors)
account for the species' response to other secondary environmental gradients.
2. Once ENFA factors are computed, habitat suitability scores for each pixel
are calculated and mapped in accordance to the responses of the species to each
factor. Partial suitability scores are computed for each factor as the percent distance
to the median scores of observed presences, and Habitat Suitability is obtained as a
weighted average of these partial suitabilities, according to the variability explained
by each factor. These scores are then mapped using the ENFA factor maps (Hirzel et
al. 2002).
Model validation and accuracy
Two measures of how the resulting suitability model explains the observed
data were used: Explained Information, which accounts for the total variability of the
species distribution explained by the model, and Explained Specialisation, which
accounts for additional variability in the Marginality and Specialisation Factors that is
not included in the Explained Information measure (Hirzel et al. 2004b).
Since both Explained Information and Explained Specialisation measures are
derived from the observed data, no assessment of how the model can be
extrapolated to the rest of the region is made. However, before using the ENFA
results or habitat suitability maps (HSMs), we needed to evaluate their accuracy in
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describing the actual spatial response of the aoudad. A good way to assess the real
accuracy of any spatial prediction is to use independent data to determine how model
predictions perform outside the boundaries of the data used in developing the ENFA.
We used two different validation strategies based in such assumption to determine a)
the predictive power of the ENFA model within the range of the population used to
calibrate it (within-data validation; i.e. the accuracy to describe the distribution of the
Sierra Espuña population), and b) its ability to predict the geographic responses of
other aoudad populations (external validation; i.e., placed outside of the bounds of
the range used to develop the model). While the former measures how the model fit
into the data, the latter gives a measure of the generality of the niche description of
the species.
Within-data validation was made through the Jackknife cross validation
procedure implemented in Biomapper 3.0 software (Hirzel et al. 2001; Boyce et al.
2002). Briefly, the data originally used for the ENFA analysis is partitioned in several
spatially-aggregated groups; each group is extracted once from the original dataset,
the models is recalibrated according to the new dataset, and the prediction results
are compared to the group of data plots extracted; this procedure is repeated as
much times as groups defined (see Boyce et al. 2002 for details). Model accuracy is
measured as the agreement between independent and calibration data, using
Spearman correlations. For the external validation, we used the presence data from
Alicante population nuclei; the predictions of the Sierra Espuña model are compared
with the presences in Alicante, and the degree of agreement between predictions
and independent data is measured using Spearman correlations. This way, a truly
empirical evaluation of the generality of the ENFA model in describing aoudad
distribution is performed using an independent population.
Niche analysis
Following Chefaoui et al. (2005), we assume that the variation of habitat
suitability scores across environmental gradients provides a description of the shape
of the species' response to such gradients. To obtain a graphic representation of this
response, we divided the Marginality Factor scores in 20 homogeneous intervals,
and the average habitat suitability scores at each interval were represented for each
habitat model (see Chefaoui et al. 2005; Hortal et al. 2005).
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To evaluate the relationship between the habitat suitability maps obtained in
the two models, they were reclassified to obtain suitable areas (HS scores between
50-75) and highly suitable areas (HS scores >75) for each model, and then, we
analysed the surface occupied by them.
RESULTS
Description of the Environmental Niche
Thirty-one environmental variables were used for the ENFA analysis, being
reduced to four factors that explained 77.5% of the variance (Table 2).
Table 2. Coefficients of the variables used in the environmental niche ENFA. Variable codes as in Table 1.
Variable Marginality Factor 2 Factor 3 Factor 4
1 HFr 0.324 0.000 0.000 0.000 2 HBsh 0.023 0.000 0.000 0.000 3 VXBsh 0.131 0.000 0.000 0.000 4 VPTr 0.205 0.000 0.000 0.000 5 HDc -0.125 0.000 0.000 0.000 6 AltMx 0.231 0.702 0.707 0.731 7 AltMn 0.017 -0.636 -0.64 -0.662 8 AspDv 0.077 0.000 0.000 0.000 9 LUDv -0.023 0.000 0.000 0.000 10 Alt 0.184 0.000 0.000 0.000 11 SlpMx 0.438 0.000 0.000 0.000 12 Slp 0.386 0.000 0.000 0.000 13 SlpMn 0.155 0.000 0.000 0.000 14 PW -0.142 0.000 0.000 0.000 15 PF -0.012 0.000 0.000 0.000 16 PSp -0.086 0.000 0.000 0.000 17 PSm -0.034 0.000 0.000 0.000 18 AltRn 0.361 -0.149 -0.15 -0.155 19 TRn -0.052 0.128 0.116 0.025 20 TMxW -0.016 0.000 0.000 0.000 21 TMxF -0.083 0.000 0.000 0.000 22 TMxSp -0.043 0.000 0.000 0.000 23 TMxSm -0.101 0.000 0.000 0.000 24 TW -0.122 0.206 0.187 0.04 25 TF -0.171 0.000 0.000 0.000 26 TSp -0.144 0.000 0.000 0.000 27 TSm -0.213 -0.15 -0.136 -0.029 28 TMnW -0.081 0.000 0.000 0.000 29 TMnF -0.095 0.000 0.000 0.000 30 TMnSp -0.095 0.000 0.000 0.000 31 TMnSm -0.124 0.000 0.000 0.000
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The marginality factor (first axis) explained a lowest percentage (0.73%) than
specialization. The specialization factors (2, 3 and 4) explained 38.35%, 26.61%, and
11.81%, respectively. The maximum and mean slopes and altitude range were, in
that order, the variables with the highest marginality coefficients, i.e., the scores of
these variables in the presence cells differed from their mean values in the study
area (Table 2).
Figure 2a.- Habitat Suitability Maps for the environmental niche model. The scale on the right shows habitat suitability values (0 = low suitability; 100 = high suitability). The geographic coordinate system shown is the UTM.
Prospects on the observed niche
Thirty-seven environmental, landscape and human disturbance variables were
included in the ENFA to develop the observed niche model (see Table 3). These
variables were reduced to four factors explaining 75.6 % of the variance (Table 3).
Such reduction in explained variability from the environmental niche model
comes from the higher complexity in the description of the region, provided by the
new variables, which might be uncorrelated with the environmental ones used in the
other model.
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Table 3. Coefficients of the variables used in the observed niche. Variable codes as in Table 1. DSE refers to the distance to the original release location in Sierra Espuña.
Variable Marginality Factor 2 Factor 3 Factor 4
1 HFr 0.270 0.000 0.000 0.000 2 HBsh 0.019 0.000 0.000 0.000 3 VXBsh 0.109 0.000 0.000 0.000 4 VPTr 0.171 0.000 0.000 0.000 5 HDc -0.104 0.000 0.000 0.000 6 AltMx 0.192 0.668 0.625 -0.694 7 AltMn 0.142 -0.605 -0.566 0.628 8 AspDv 0.064 0.000 0.000 0.000 9 LUDv -0.019 0.000 0.000 0.000 10 Alt 0.153 0.000 0.000 0.000 11 SlpMx 0.364 0.000 0.000 0.000 12 Slp 0.321 0.000 0.000 0.000 13 SlpMn 0.129 0.000 0.000 0.000 14 PW -0.118 0.000 0.000 0.000 15 PF -0.010 0.000 0.000 0.000 16 PSp -0.072 0.000 0.000 0.000 17 PSm -0.029 0.000 0.000 0.000 18 AltRn 0.300 -0.141 -0.132 0.147 19 TRn -0.043 0.184 -0.234 -0.144 20 TMxW -0.013 0.000 0.000 0.000 21 TMxF -0.069 0.000 0.000 0.000 22 TMxSp -0.036 0.000 0.000 0.000 23 TMxSm -0.084 0.000 0.000 0.000 24 TW -0.101 0.296 -0.377 -0.232 25 TF -0.143 0.000 0.000 0.000 26 TSp -0.120 0.000 0.000 0.000 27 TSm -0.177 -0.214 0.273 0.168 28 TMnW -0.067 0.000 0.000 0.000 29 TMnF -0.079 0.000 0.000 0.000 30 TMnSp -0.079 0.000 0.000 0.000 31 TMnSm -0.103 0.000 0.000 0.000 32 DSE -0.473 0.000 0.000 0.000 33 DHw 0.107 0.000 0.000 0.000 34 DRd 0.184 0.000 0.000 0.000 35 DUr 0.188 0.000 0.000 0.000 36 WULAI -0.058 0.000 0.000 0.000
Since ENFA is an ordination technique, based in the differences between the
central trends of species and the whole region in the hyperspace formed by the
descriptor variables used, the higher the number of uncorrelated variables, the more
complex the description of variability, and thus the smaller the variability explained
when these variables are incorporated to the analysis.
The marginality factor explained the lowest percentage (0.17%) of
specialization in this model. The specialization factors (2, 3 and 4) explained 34.39%,
22.60%, and 18.43%, respectively. The proximity to the original release location,
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followed by the maximum and mean slopes, and the altitude range were the
variables with higher marginality coefficients, i.e., the scores of these variables in the
presence cells differed from their mean values in the study area (Table 3). As in the
environmental niche model, this result indicates that aoudads show a preference for
using rough and craggy areas. Similarly, maximum and minimum altitude had the
highest coefficients amongst the specialization factors. The marginality coefficient
obtained was 1.55, demonstrating an even higher separation of the species from the
central part of the environmental gradient.
Figure 2b.- Habitat Suitability Maps for the observed niche model. The scale on the right shows habitat suitability values (0 = low suitability; 100 = high suitability). The geographic coordinate system shown is the UTM.
The global tolerance value was 0.27, which suggests that the aoudad is
relatively specialized in this region of Southern Spain. The HSM (Figure 2b) showed
a high probability of appearance of the aoudad in the centre of the study area
following a southwest – northeast axis, but this distribution was more patchily than in
the environmental niche model. Again, Jackknife validation indicates that the
predictive map of aoudad’s observed niche is reliable (within-data validation; mean
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Spearman R = 0.92), also showing a high predictive capacity when is validated with
the Alicante population (external validation; mean Spearman R = 0.61).
Changes in Habitat Suitability
The variation of mean habitat suitability scores of both environmental and
observed niche models along the gradient identified by the marginality factors can be
seen in Figure 3. Both models showed similar environmental adaptations; however,
the observed niche model was more restricted and had lower habitat suitability
values than the environmental niche model.
Figure 3.- Variation of the mean habitat suitability scores along the gradient defined by the marginality factor. As the marginality factors for both models were highly correlated, we plotted them against the one from the environmental niche model. The marginality factor was divided into 20 intervals, and mean values per interval are shown.
The suitable areas (HS>50) in the environmental model covered 7.78% of the
study area (4823 km2) 34.77% of this area was suitable, and 12.32% was highly
suitable (HS>75) in the observed niche model (1677 and 594 km2, respectively). On
the other hand, the highly suitable areas in the introduced model covered 1.39% of
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the study area (861 km2), being 76.07% suitable and 36.01% highly suitable in the
observed niche model (655 and 310 km2, respectively).
DISCUSSION
We performed an analysis of the factors determining habitat suitability (both in
the environmental and observed niches) in the introduced aoudad population in
southeastern Spain. The species currently occupies several mountainous areas of
the Cordillera Sub-Bética mountain range. Two main zones can be distinguished
from the presence data, the one originating from the first release in Sierra Espuña
Natural Park in 1970, which comprises a wide-ranging population; and a second one,
further north, originating from escapes from a couple of hunting estates in Alicante
(see Cassinello et al. 2004). Since data on habitat suitability in its native range in
North Africa is not available, we have used nuclei from one of these zones (Alicante)
as an independent test to determine the reliability of the geographic expression of
both niche descriptions calculated from the other (Sierra Espuña nucleus).
Habitat suitability of the aoudad in Spain
According to our characterization of its environmental niche (see Figure 2a),
the aoudad selected areas characterized by a low winter precipitation regime, high
altitudes and terrain slopes as well as with the presence of forest lands. These
results agree with the habitat selection expected for a mountain ungulate such as the
aoudad, where rocky and precipitous areas abound, from the sea level up to the
extent of snow-free altitudes (see Shackleton 1997). This niche characterization for
the aoudad is highly reliable, as our maps showed a high predictive power when
validated using the second population in Alicante. Therefore, we suggest a high
potentiality for this exotic ungulate to conquer new areas around its current
distribution range in southern Spain.
The description of aoudad’s current habitat suitability varies when landscape
avoidance and anthropogenic variables are included in the analysis to develop the
observed niche model. When landscape avoidance and human disturbance effects
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are included in the ENFA model, it appeared that the aoudad was associated with
less mountainous areas, with higher temperatures, forest and dryland crop areas
(see Table 3). Human land use data will also be more patchily distributed than
environmental parameters, therefore contributing to a more patchy distribution. This
resulted in a narrower, more patchy suitability map (Figure 2b), due to the landscape
and human disturbance constraints added to ENFA calculations. The high
coefficients obtained for the distance to the original release locality indicate that
current aoudad distribution is clearly shaped by the location of the initial release. In
addition, the observed niche was narrower than the environmental niche, and was
also placed nearer to one of the extremes of the marginality factor axis (see Figure
3).
There was an important relationship between habitat suitability for the aoudad
and the intensity of human disturbance; humanized landscapes with moderate-to-
high WULAI scores appear not to be suitable for the species. If WULAI scores are
plotted against HSM scores, there is a progressive diminution of the maximum
habitat suitability for the aoudad as its landscape avoidance increases, reaching 0
above intermediate levels of disturbance (Figure 4).
Figure 4.- Relationship between the habitat suitability for the aoudad, and the Wild Ungulates Land Avoidance Index (WULAI) from the observed niche analysis (see Figure 2b).
However, the current analysis does not allow us to separate the effects of
different types of land use on the aoudad range expansion. These single effects
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could be even stronger than that measured by our landscape use index, so the exact
effects of landscape modification by humans on aoudad dispersion remain untested.
As an example, distance to roads presents more explanatory power than WULAI
(see Table 3), an effect of using a complex mixture of land use categories (EEA
2000) within a single index (see Methods). Thus, further analyses are needed to
unravel the individual effects of these human impacts on aoudad habitat selection.
Conservation concerns
Most ungulate species in Spain are currently expanding in range (e.g., the
Iberian ibex; Pérez et al. 2002; Acevedo et al. 2006 [Capítulo 1.1]). Some species
are occupying new habitats that may have not supported large herbivores for a long
time; consequently, local plant species may have evolved without recovering high
grazing pressure, so that they may not be tolerant to a more intensive herbivore
presence. Furthermore, the increasing presence of allochthonous ungulates, such as
the European mouflon (Ovis aries musimon) and the aoudad, make things worse as
they may particularly threaten local plant species (Rodríguez-Piñero and Rodríguez-
Luengo 1992). It has been seen that exotic species can substantially influence the
composition and structure of plant and animal communities, alter nutrient and water
cycles, and change disturbance regimes (e.g. Parker et al. 1999; Mack et al. 2000;
Holmgren 2002).
This work shows that the potentially high expansion capacity of the exotic
aoudad in the south of Spain is resulting from the similarity of the host habitat to that
of the region of origin, North Africa. In Spain, the aoudad has not yet reached
suitable areas located at much higher altitudes (i.e., Sierra Nevada mountain range),
which is the native land of the Iberian ibex. We hypothesize that if the aoudad
reaches these areas, potential competition may arise with the ibex, given the
biological similarities of these caprid species. In addition, the Sierra Nevada (a
Spanish National Park) is known to be an important hotspot for Iberian plants, both in
terms of richness and endemism (see Castro Parga et al. 1996; Lobo et al. 2001).
Therefore, if the aoudad reached the region, many endangered endemic plants could
be at a higher risk. Given this potential threat, it is important to develop strategies to
prevent the aoudad dispersing through the suitable areas located in the western
limits of its current distribution (see Figure 2). Our analysis has identified several
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constraints to the dispersal of the aoudad associated with the intensity of human
disturbance and land use. This suggests that further investigations on the individual
effects (e.g., management of cultivated landscapes, grazing intensities and
competition with livestock) could help to design land use strategies that are able to
create a landscape matrix which offers a high frictional effect on aoudad dispersal.
ACKNOWLEDGEMENTS
We are indebted to Falk Huettmann and two anonymous referees for their help
in revising a previous version of the manuscript. We also wish to thank Jorge M.
Lobo, Alberto Jiménez-Valverde and Rosa M. Chefaoui for their work on and
maintenance of the GIS database, and to them and David Nogués-Bravo and Miguel
B. Araújo for some discussions on the geographic expression of the niche of the
species. This work has also benefited from the critical comments of Burt P. Kotler as
well as from some discussion with Miguel B. Araújo and David Nogués-Bravo. JC is
currently enjoying a Ramón y Cajal research contract at the CSIC awarded by the
Ministerio de Educación y Ciencia (MEC); he is also supported by the project PBI-05-
010 granted by Junta de Comunidades de Castilla-La Mancha. PA is enjoying a grant
from Principado de Asturias and CSIC. JH is supported by a Portuguese FCT
(Fundação para a Ciência e Tecnologia) grant (BPD/20809/2004), and also by the
Fundación BBVA project “Yámana - Diseño de una red de reservas para la
protección de la biodiversidad en América del Sur Austral utilizando modelos
predictivos de distribución con taxones hiperdiversos”, as well as the Spanish MEC
project CGL2004-0439/BOS.
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3.2.- ES EL ARRUI (AMMOTRAGUS LERVIA) UNA AMENAZA PARA LA
CABRA MONTÉS (CAPRA PYRENAICA)? UNA APROXIMACIÓN BASADA EN
MODELOS DE ADECUACIÓN DE HÁBITAT
Acevedo, P., Cassinello, J., Hortal, J., Gortázar, C. IS INTRODUCED EXOTIC AOUDAD
(AMMOTRAGUS LERVIA) A THREAT TO NATIVE IBERIAN IBEX (CAPRA PYRENAICA)? A HABITAT
SUITABILITY MODEL APPROACH. Diversity and Distributions, en evaluación (enviado a
24/10/2006).
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RESUMEN
La llegada de especies invasoras es una de las principales amenazas para la
conservación de la biodiversidad. Un caso particular es el de los ungulados silvestres que
están en aumento en regiones fuera de su rango natural de expansión debido a intereses
cinegéticos. Desafortunadamente se conoce poco sobre los efectos que estos herbívoros
pueden ocasionar en el ecosistema hospedador. El presente estudio es el primer análisis
comparativo de los requerimientos de hábitat de dos especies de ungulados que pueden
estar compitiendo por los recursos en el sur de Europa: la endémica cabra montés (Capra
pyrenaica) y el exótico arrui (Ammotragus lervia). El arrui es un caprino norteafricano
introducido en 1970 como especie de caza en el sureste de España, en donde se ha
adaptado formidablemente, estando sus poblaciones en expansión. El Análisis Factorial de
Nicho Ecológico es usado para describir el nicho realizado de ambas especies en donde sus
rangos de distribución se fusionan. Las especies estudiadas ocupan áreas marginales de
relieve accidentado en la región. La marginalidad es mayor para la cabra montés y su
distribución parece estar más en equilibrio con las condiciones regionales que en el caso del
arrui, el cual es menos tolerante a gradientes ambientales secundarios. Las áreas con
elevada adecuación para cada especie son secundariamente adecuadas para la otra. La
reclasificación de los mapas de adecuación muestra las áreas de potencial coexistencia
espacial, así como los rasgos ecológicos que las diferencian. Los resultados obtenidos no
permiten inferir competición por los recursos entre estas especies. Sin embargo, la
expansión actual del arrui podría ocasionar la invasión de los hábitats favoritos de la cabra
montés. La inadecuada política cinegética y la semejanza climática de la región de estudio
con las áreas nativas del arrui, debido a un fuerte proceso de desertificación, están
facilitando una alta tasa de expansión de esta especie. Se recomienda monitorizar las
poblaciones de esta especie exótica, así como promover prácticas de conservación activas
con el fin de preservar los recursos naturales de esta región europea.
ABSTRACT
The arrival of alien species is one of the main threats to the conservation of
biodiversity. One particular case is that of wild ungulates, which are increasingly present in
regions further to their natural expansion range due to human hunting interest. Unfortunately,
we know little on the effects these large herbivores may have on the host ecosystems. This
study deals with a first comparative analysis of habitat requirements of two ungulate species
that may be facing competition for resources in the south of Europe: the native Iberian ibex
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(Capra pyrenaica) and the exotic aoudad (Ammotragus lervia). The aoudad is a North
African caprid introduced in 1970 as a game species in southeastern Spain. It formidably
adapted and populations are freely expanding since then on. Ecological Niche Factor
Analysis is used to describe the realized niche of both species where their distribution ranges
merge. Both species occupy marginal areas of rugged terrain in the region. Marginality is
higher for the Iberian ibex, whose distribution appears to be more in equilibrium with regional
conditions than that of the aoudad, which is less tolerant to secondary environmental
gradients. Highly suitable areas for each species are secondarily-suitable for the other.
Reclassified and cross-tabulated habitat suitability maps showing the areas of potential
spatial coexistence and differences in ecological traits between both species are provided.
The results obtained do not allow inferring resource competition between these species.
However, current aoudad expansion could lead it to invade ibex favourite habitats.
Inadequate hunting policy and monitoring, and increasing climatic resemblance of the study
region with the native aoudad areas, due to a strong desertification process, are facilitating a
high rate of expansion. We strongly recommend monitoring these exotic populations, and
promote active conservation practices, if we want to preserve the unique natural resources
present in this European region.
INTRODUCTION
One of the main threats to biodiversity is the arrival of alien species in regions
further to their natural expansion range, reaching new ecosystems which may be
altered by their presence, thus affecting the viability of autochthonous fauna and flora
(e.g., Diamond 1989; Wilcove et al. 1998; Gurevitch and Padilla 2004; Didham et al.
2005). Sport hunting activity is becoming the main driving force of the unnatural
expansion of some species of ungulates all over the world (e.g., Crosby 1986;
Macdonald et al. 1988; Gortázar et al. 2000; Jaksic et al. 2002).
Uncontrolled exploitation and poaching used to be the main threat to
European autochthonous ungulate populations, although current hunting regulations
are causing their recovery and even expansion in some countries (e.g., Cargnelutti et
al. 1992; Sidorovich et al. 2003; Geisser and Reyer 2004; Acevedo et al. 2006a
[Capítulo 1.1]). Such expansion is noteworthy in areas where game activity is not
allowed, i.e., protected lands and those close to urban zones (e.g. Whittaker et al.
2001; Cahill et al. 2003). In the Iberian Peninsula, the expansion of the wild boar, Sus
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scrofa, has been registered since several decades ago (Sáez-Royuela and Tellería
1986; Gortázar et al. 2000; Acevedo et al. 2006b). Other recent examples are roe
deer, Capreolus capreolus (Acevedo et al. 2005) and Iberian ibex, Capra pyrenaica
(Pérez et al. 2002; Acevedo et al. 2006a [Capítulo 1.1]). The expansion of the latter
may rely on recent habitat changes, i.e. agricultural lands abandonment, game
management translocations (Gortázar et al. 2000), its recovery from past sarcoptic
mange epizootics (Pérez et al. 1997), and a decrease of its hunting pressure
probably caused by the incidence of this disease (see Garrido 2004).
These rapid increases in the populations of large herbivores are provoking
their local overabundance (Gortázar et al. 2006). These high densities are resulting
in a serious threat for plant communities due to overgrazing pressures, which are
also rising due to the increasing presence of allochthonous ungulates, such as the
European mouflon (Ovis aries musimon) and the aoudad (Ammotragus lervia).
Of special concern is the aoudad, an African generalist ungulate, which has
been successfully introduced outside its African range as a game species in USA
and Spain. There, it has adapted formidably to Mediterranean-like regions, where
food resources are abundant, in contrast with the desert lands occupied in its native
African range. In these areas, the abundance of resources, along with the scarcity of
competitors and predators, results in high birth rates and a quick spread of the
population (see Wolf et al. 1996). Due to this, the aoudad has rapidly adapted to
southern Iberian habitats, presenting elevated population growth rates (Cassinello
2000; Cassinello et al. 2004). The effects that this alien species may cause on native
flora and fauna are yet uncertain, although its potential as a competitor of native
ungulates has already been postulated, mainly based on diet overlap between the
aoudad and desert bighorn, Ovis canadensis nelsoni (Simpson et al. 1978) and mule
deer, Odocoileus hemionus (Bird and Upham 1980; Krysl et al. 1980).
The relationships between environmental gradients and the adequacy for the
survival of the populations of a species can be used to model the potential response
of the species to these gradients (Austin et al. 1990). Such description can be used
to produce predictive maps of species distribution (Guisan and Zimmermann 2000;
Araújo and Guisan 2006), and to describe the characteristics of the niche of the
species (e.g., Peterson et al. 1999; Robertson et al. 2001; Chefaoui et al. 2005;
Soberón and Peterson 2005; Araújo and Guisan 2006). Two kinds of predictive maps
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can be obtained for a species, describing i) current distribution or ii) habitat suitability
(i.e., potential distribution). The latter could serve as a tool for the study and threat
assessment of biological invasions, as habitat suitability can be used as an indicator
of the risk for a particular territory to be invaded by the alien species (e.g., Peterson
and Vieglais 2001; Peterson 2003).
The Ecological Niche Factor Analysis (ENFA, Hirzel et al. 2002) models
habitat suitability by comparing the environmental response of the species to the
environmental characteristics of the entire study area. This methodology can be used
to develop habitat suitability maps from raw presence data. Therefore, ENFA is
recommended when absence data are not available (most data banks), unreliable
(most cryptic and rare species) or meaningless (invaders) (Hirzel et al. 2001).
Recently, Chefaoui et al. (2005) proposed to describe the realized niche of a species
using ENFA results. Given that the factors identified by ENFA represent the main
environmental gradients that are shaping the spatial response of the species in the
study region, it can be assumed that the response of a species to these gradients
constitutes its realized niche. Therefore, the distribution of habitat suitability scores
through these factors could be used to describe and study the characteristics of the
realized niche of species, as well as niche differentiation among several related
species (Chefaoui et al. 2005; Hortal et al. 2005). Here, the realized niche is intended
as the portion of the fundamental niche where the species is currently present, rather
than where is competitively dominant (the original definition of Hutchinson 1958, see
discussion in Soberón and Peterson 2005; Araújo and Guisan 2006).
We compare habitat requirements and habitat suitability for autochthonous
Iberian ibex and exotic aoudad inhabiting the southeastern Iberian Peninsula,
according to their current distribution (Pérez et al. 2002; Cassinello et al. 2004;
Acevedo et al. 2006a [Capítulo 1.1]). Our goal is to compare the environmental
requirements of both species to identify differences and similarities, and advance
whether competition for resources and threats to the Iberian ibex are expected. To do
this, we use ENFA and the niche description proposed by Chefaoui et al. (2005) to
characterize the response of both ungulate species to the main environmental
variations in the study area, as well as to predict their potential distribution. This is
the first attempt to compare ecological traits between aoudads and Iberian ibexes, as
to date no field study whatsoever has been carried out in the regions where both
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species coexist. The results are used to assess the potential impacts of current
aoudad expansion in the conservation of ibex populations.
MATERIAL AND METHODS
Study region
We have chosen a geographic extent that hosts the environmental extremes
present in SE Iberian Peninsula (i.e., coastal and mountain), the current area of
expansion of the aoudad (Cassinello et al. 2004).
Figure 1. Presence data of the Iberian ibex (black dots) and the aoudad (grey dots), and location of the study area. Provinces borders are shown along with the main mountain ranges where the species can be found.
Such window encompasses 340 km width and 270 km height (61,961 km2 of
land area; UTM 29N geographic reference system; NW corner: 450,000-4,330,000;
SE corner: 790,000-4,060,000; Figure 1), including Sierra Nevada mountain range in
the SW (rising over 3,400 m.a.s.l.), Segura coastal basin in the east (with mean
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altitudes below 20 m.a.s.l.), as well as several other mountain ranges and high-
altitude plains, such as Sierra Espuña (origin of the aoudad introduced population),
Sierra María, Sierra de Los Filabres, and Cazorla, Segura y Las Villas Natural Park.
Aoudad and Iberian ibex distribution data
Aoudad distribution data (Cassinello et al. 2004, Figure 1) comes from direct
field observations and interviews to local shepherds, hunters, and biologists and park
managers from regional environmental agencies, and verified with visits to the areas
where aoudads were reported. Iberian ibex distribution data were obtained by means
of direct field observations and interviews addressed to forest rangers and staff from
environmental agencies (Pérez et al. 2002; Acevedo et al. 2006a [Capítulo 1.1]).
Environmental data
Many climatic and ecological factors have been described to affect the
population abundance and distribution of ungulate species in the Iberian Peninsula
(e.g., Virgós 2002; Acevedo et al. 2005, 2006b). We selected 12 variables that could
act as determinants of current aoudad and Iberian ibex distribution in SE Iberian
Peninsula, also encompassing the range of climatic and ecological traits present in
the study region (Table 1). Ten of these variables account for environmental
variations (climate, habitat structure, vegetation characteristics and geomorphology),
and the other two do for human impact.
Data comes from an Iberian GIS database compiled and managed by J. M.
Lobo, A. Jiménez-Valverde, R. M. Chefaoui and J. Hortal. Climate variables were
obtained from the monthly values of the digital version of the Spanish National
Climate Atlas (provided by the Instituto Nacional de Meteorología; available at
http://www.inm.es/). Geomorphology variables were calculated from an Iberian Digital
Elevation Model of 100 m pixel width. Habitat structure variables were obtained from
the 250 m pixel width land use information of the CORINE NATLAN European project
(EEA 2000). Finally, two variables accounting for human pressure on aoudad and
ibex populations were obtained: distance to urban areas (i.e. to the urban and
industrial categories following CORINE land use map), and distance to the nearest
road (including motorways and national and local roads, extracted from the Spanish
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National Digital Atlas, courtesy of the Instituto Geográfico Nacional;
http://www.ign.es/). All variables were handled and processed in a GIS environment
(Clark Labs 2004). Information was extracted at 1 km2 grain (1 x 1 km pixels), to fit
with the spatial resolution of biological data (see another examples at Chefaoui et al.
2005; Acevedo et al. 2006a [Capítulo 1.1]). In addition, these variables were Box-
Cox normalized prior to their use in the ENFA analyses.
Table 1. Variables used in the analyses (and their measurement units). Average values are shown for the whole study region (global), and for the areas where the aoudad and the Iberian ibex are present.
Means VARIABLES (UNIT)
Global Aoudad Iberian ibex
CLIMATE Winter rainfall (mm) 132.92 108.65 209.14
Summer rainfall (mm) 46.29 40.73 61.69 Mean summer temperature (ºC) 22.95 21.9 19.28
Annual range of temperatures (ºC) 15.33 15.21 15.58
GEOMORPHOLOGY Maximum altitude (m) 806.46 1066.77 1670.46
Altitude range (m) 101.14 187.37 204.59 Mean slope (degrees) 5.56 10.40 11.21
Maximum slope (degrees) 12.23 23.01 22.24
HABITAT STRUCTURE Forest area (%) 11.86 33.17 39.80
Shrubland area (%) 27.72 33.88 17.08
HUMAN PRESSURE Distance to urban areas (m) 3974.88 5714.69 7335.62
Distance to the nearest road (m) 2050.21 2915.65 3431.15
Statistical analyses
Niche modelling
BioMapper 3.0 (Hirzel et al. 2004a; http://www.unil.ch/biomapper) was used to
model the niche of the study species. This software uses ENFA to produce predictive
maps of habitat suitability (i.e., potential distribution) from GIS variables (see
applications at Hirzel 2001; Hirzel et al. 2001, 2002; Hirzel and Arlettaz 2003;
Gallego et al. 2004; Hirzel et al. 2004b; Chefaoui et al. 2005; Hortal et al. 2005;
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Acevedo et al. 2006a [Capítulo 1.1]; Cassinello et al. 2006 [Capítulo 3.1]). These
maps are produced in two steps.
In a first step, a description of the realized niche of the species is build. The
response of the species to the main environmental variations in the study area is
characterized from presence data using ENFA. Briefly, the predictors are reduced to
a number of orthogonal factors, accounting for the maximum differentiation between
the average conditions at the whole study territory, and at the sites where the species
is present (Hirzel 2001). The factor scores of the first axis (marginality factor) express
the Marginality of the focal species on each predictor variable. A Marginality
coefficient is also computed taking into account all predictor variables, so that the
marginalities of different species within a given area can be directly compared (Hirzel
et al. 2002). The factor scores of the subsequent factors, specialisation factors,
receive a different interpretation: the higher (absolute values) scores, the more
restricted is the range of the focal species on the corresponding variable. A
Tolerance coefficient is also computed (ibid.). ENFA is similar to the Principal
Component Analysis, but looks for factors of biological significance (Hirzel et al.
2001). The marginality factor reflects the direction on which the species niche mostly
differs from the available conditions in the global area. Subsequent factors represent
the specialisation, and are extracted successively by computing the direction that
maximises the ratio of the species distribution (Hirzel 2001). The higher absolute
value of the factor scores of a variable, the further the species departs from the mean
available habitat regarding the corresponding variable (scores<0 indicate that
species prefers values that are lower than average with respect to the study area,
while scores>0 indicate preference for higher than average values).
Secondly, predictive maps of habitat suitability are produced. Once ENFA
factors are computed, a habitat suitability map (HSM) is calculated and mapped from
the responses of the species to each factor. Briefly, partial suitability scores are
computed for each factor as the average distance to the median scores of observed
presences, and HSM is obtained as a weighted average of these partial suitabilities
(Hirzel et al. 2002).
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Model validation and accuracy
Explained Information (ExI) and Explained Specialisation (ExS) are used to
measure how the resulting suitability model explains the observed data. The former
accounts for the total variability of the species distribution explained by the model,
whereas the latter does for additional variability on the marginality and specialisation
factors not included in the Explained Information measure (Hirzel et al. 2004a). In
addition, the robustness and predictive power of the HSMs were assessed by means
of the spatially explicit Jackknife cross-validation procedure implemented in
Biomapper software (Boyce et al. 2002; Hirzel et al. 2002).
Niche description
ENFA analysis identifies two descriptors of species environmental niches:
marginality and tolerance coefficients (see above). We also described the shape of
the environmental niche of the species as the variation in the habitat suitability scores
throughout the environmental gradient defined by the Marginality Factor (see
Chefaoui et al. 2005; Hortal et al. 2005). To do this, Marginality Factor scores were
divided in a number of homogeneous intervals, and mean habitat suitability scores at
each interval were represented for each species. In addition, the HSM map obtained
for each species was reclassified (see Chefaoui et al. 2005) in three categories
according to HSM scores: low habitat suitability (0-33); medium habitat suitability (34-
66) and high habitat suitability (66-100). These new maps were cross-tabulated in the
GIS environment to pinpoint zones suitable for the two study species (high habitat
suitability for the Iberian ibex and high habitat suitability for the aoudad), where
coexistence and competition could occur. The environmental variables that
characterize each zone were examined using Bonferroni corrected ANOVA analyses
(Perneger 1998).
RESULTS
The 12 environmental variables considered were reduced to three factors in
both ENFA analyses (see Table 2), explaining 82.34% and 83.20% of the variance in
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the aoudad and Iberian ibex distributions, respectively. The first axes explained very
low percentages of the specialization for both species (<4%).
Maximum and mean slopes, altitude range and presence of forests were the
variables with higher scores in the marginality factor for the aoudad model, while low
summer temperatures, maximum altitude, mean slope and winter rainfall were so in
the ibex model. Temperature range and winter rainfall presented the higher
coefficients at the specialization factors for the two species, which thus show similar
secondary restrictions (Table 2).
Table 2. Coefficients of the variables used in ENFA, and percentages explained by marginality (MF) and specialization factors (SF).
Aoudad model Iberian ibex model Variables
MF SF 1 (43.49%)
SF 2 (17.53%) MF SF 1
(48.01%) SF 2
(14.54%)
Forest area 0.362 0.000 0.006 0.264 0.075 -0.140 Shrubland area 0.026 0.146 0.029 0.025 0.115 -0.275 Maximum altitude 0.258 -0.281 0.257 0.475 -0.099 -0.366 Distance to the nearest road 0.248 0.069 0.018 0.219 0.015 -0.085 Distance to urban areas 0.253 0.093 -0.103 0.271 0.04 -0.154 Maximum slope 0.490 0.111 -0.151 0.252 0.205 -0.044 Mean slope 0.432 -0.074 -0.365 0.279 -0.094 -0.055 Winter rainfall -0.159 0.583 -0.330 0.277 0.298 -0.403 Summer rainfall -0.038 -0.507 0.410 0.212 0.088 0.404 Altitude range 0.404 -0.029 0.228 0.269 -0.013 0.135 Annual range of temperatures -0.058 -0.444 -0.657 0.040 -0.893 -0.154 Mean summer temperature -0.238 -0.272 -0.071 -0.495 0.155 -0.606
Both ungulate species occupy marginal areas in the study region (aoudad
marginality coefficient=1.15; ibex marginality coefficient=2.08, see Figure 2).
However, although the Iberian ibex is more marginal than the aoudad in its
environmental selection according to the main environmental gradient in the region,
this species is quite tolerant to the secondary environmental gradients (tolerance
coefficient=0.84). Therefore, ibex distribution appears to be more in equilibrium with
regional conditions than aoudad distribution, which is less tolerant to secondary
gradients (tolerance coefficient=0.68). Moreover, highly suitable areas for each
species were secondarily-suitable for the other one (Figure 2).
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0
10
20
30
40
50
60
70
-4,05
-2,56
-1,80
-1,21
-0,70
-0,20 0,4
21,3
42,8
65,3
8
Ibex Marginality Factor
Hab
itat S
uita
bilit
y
AoudadIberian Ibex
Figure 2. Variation of mean habitat suitability scores along the marginality factor. The factor was divided into 20 intervals, and mean HSM values are shown. As marginality factors for both models were highly correlated, only one was used for plot the figure, the ibex model.
Figure 3a. Habitat suitability maps for the study species: a) the aoudad. Habitat suitability
scores have been reclassified in three categories (0-33 = low suitability, 34-66 = medium suitability, and 67-100 = high suitability).
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Figure 3b. Habitat suitability maps for the study species: b) the Iberian ibex. Habitat suitability scores have been reclassified in three categories (0-33 = low suitability, 34-66 = medium suitability, and 67-100 = high suitability).
The so-obtained HSMs are highly reliable, since our model validation
produced the following outcome: ExI=66%, ExS=83%, and average Spearman
coefficient at Jackknife validations of 0.97 for the ibex, and ExI=65%, ExS=82%, and
Spearman coefficient = 0.95 for the aoudad.
Figure 4. Map showing the highly suitable areas (habitat suitability > 66) for each one of the study species, as well as the areas of potential coexistence.
Tesis Doctoral
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Reclassified HSMs for both species are shown in Figure 3, where areas of
low, medium and high habitat suitability are depicted. Cross-tabulated HSMs show
the areas of spatial coexistence between both species (i.e., highly suitable for both
species) as well as those ones highly suitable for one of them exclusively (Figure 4).
High suitability areas were significantly different in ecological traits for the two
species (Table 3, Figure 5), and were also different to the sites highly suitable for
both species.
DISCUSSION
One of the possible adverse consequences of the presence of the exotic
aoudad in the south of Europe is its incidence on other taxonomically close
autochthonous ungulates, or on ecologically convergent species. Here we present
the first study on habitat similarities between aoudad and Iberian ibex, according to
data on the distribution of both species in the south east of the Iberian Peninsula.
Table 3. Environmental differentiation between the areas of potential coexistence of the aoudad and the Iberian ibex, and the areas suitable to each one of these species (HS > 66 in both models). Results of the analyses of variance are shown; ANOVA test coefficient (F), Bonferroni-corrected p-value (ns=no significant, ***p≤0.0001); the areas with significantly higher values for a given dependent variable in each comparison are indicated (A=aoudad, C=potential coexistence, and I=Iberian ibex).
Aoudad vs. potential
coexistence
Aoudad vs. Iberian ibex
Iberian ibex vs. potential
coexistence
Variables
F p-value
area with a higher mean value
F p-value
area with a higher mean value
F p-value
area with a higher mean value
Forest area 56.52*** C 72.13*** I 8.34ns - Shrubland area 19.28*** A 0.82ns - 14.75*** I Maximum altitude 612.68*** C 3212.16*** I 27.82*** I Distance to the nearest road 48.89*** A 43.11*** I 95.35*** I Distance to urban areas 30.23*** C 94.01*** I 0.12ns - Maximum slope 0.30ns - 70.04*** I 13.84*** I Mean slope 0.52ns - 225.10*** I 57.60*** I Winter rainfall 814.17*** C 1046.59*** I 65.42*** C Summer rainfall 1168.11*** C 941.18*** I 84.14*** C Altitude range 2.89ns - 209.29*** I 64.14*** I Annual range of temperatures 193.29*** C 150.00*** I 96.73*** C Mean summer temperature 498.62*** A 2222.7*** A 15.61*** C
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On the methodological approach
The ENFA-based methodological approach used here (based on Chefaoui et
al. 2005) could be of great utility for the study of the realized niches of most species,
as well as for monitoring the potential spread of invasive species. Since the seminal
works of Austin, Nicholls and Margules (Margules et al. 1987; Nicholls 1989; Austin
et al. 1990), Generalized Linear and Generalized Additive Models (GLM and GAM,
respectively), linked to GIS applications, have become very popular in species
distribution predictions (e.g., Guisan et al. 2002; Dennis and Shreeve 2003; Nogués-
Bravo and Martínez-Rica 2004; Quevedo et al. 2006). When absence or pseudo-
absence data are available, more robust habitat models can be built from these
techniques (e.g., Engler et al. 2004; Lobo et al. 2006; but see Hirzel et al. 2001).
However, in the specific case of invading species, some times these species are not
yet occupying all their potential habitats in the landscape, and ENFA could produce
better results to GLM as 'absence data' of this species would not be reliable (Hirzel et
al. 2001).
Figure 5. Plots showing mean (±SE95%C.I.) values of some ecological variables present in highly suitable areas for the aoudad, aoudad and Iberian ibex (potential coexistence areas) and Iberian ibex. Statistically significant differences are indicated in Table 3. (a) Percentage of forest and shrubland areas; (b) maximum altitude and slope; (c) winter rainfall and mean summer temperature; (d) distances to urban areas and roads.
Tesis Doctoral
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Given that both the Iberian ibex and the aoudad are under remarkable
expansion processes in the study region (Cassinello 2000; Pérez et al. 2002;
Cassinello et al. 2004; Acevedo et al. 2006a [Capítulo 1.1]; Cassinello et al. 2006
[Capítulo 3.1]), we used ENFA analyses to implement maps of the potential
distribution of both species. In addition, ENFA could also be more useful than GLM
when ecological interpretation is the aim of the study, even in situations where GLM
provides higher correlations to the observed data (Hirzel et al. 2001). The niche-
description methodology derived by Chefaoui et al. (2005), based in such premises,
is used here to describe the realized niches of both caprids in southeastern Iberian
Peninsula. However, ENFA results usually overestimate habitat suitability (Zaniewski
et al. 2002; Engler et al. 2004); therefore, such limitation should be considered when
interpreting our results.
Niche description for the study species
The Iberian ibex and the aoudad occupy restricted habitats in the study area,
but ibex distribution appeared to be more in equilibrium with regional conditions than
that of aoudad, which is less tolerant to secondary environmental gradients. It then
emerges that the aoudad in Spain has not reached all its potentially suitable areas
yet, some of them located at higher altitudes. According to the known biology and
ecology of the aoudad (e.g., Ogren 1965; Shackleton 1997; Cassinello 1998), as well
as to our results (see Figure 1), the species show a strong potential to reach and
settle in other mountainous regions, native to the Iberian ibex, such as Sierra Nevada
mountain range (part of the Spanish National Parks network since 1999).
According to our analyses, the aoudad selects areas characterized by high
slopes and altitude ranges, and an important presence of forests. Such requirements
agree with the habitat selection made by the aoudad both in its native North African
range (Shackleton 1997) and in the regions where it has been introduced (Johnston
1980; Cassinello 2000). On the contrary, although the Iberian ibex also selects
mountainous areas, they are more marginal than the used by the aoudad, pictured by
low summer temperatures and high altitudes, and, to a lower extent, by high slopes
(see also Acevedo et al. 2006a [Capítulo 1.1]) and high winter rainfall. In these
areas, food availability according to its diet is expected to be higher (Martínez and
Martínez 1987; Martínez 2000).
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The results of this study defined a series of ecological traits that can be easily
related to the mountain ranges where the two study species are predominantly found
in the south east of Spain (see Figure 1). Thus, the aoudad ranges a wide variety of
mountainous regions of very different altitudes and scattered throughout the study
area (see Figure 3a), whereas the ibex is found in spatially restricted areas, in the
mountain ranges with higher elevations in the study area (Figure 3b).
Cross-tabulated HSMs allowed the comparison between areas highly suitable
for one of the study species (but not for the other) and areas highly suitable for both
species (the areas of potential coexistence). Differences found between the
ecological variables included in the analyses can be explained by the characteristics
of the mountain ranges concerned. Basically, we appreciate higher marginality
values and lower plasticity in the Iberian ibex than in the aoudad, which
comparatively tends to act as a generalist in terms of habitat preference (e.g., Gray
and Simpson 1980; Escós and Alados 1992). Also, areas of coexistence are more
similar in terms of climate to highly suitable areas exclusively of the ibex, so that
before a hypothetical competitive situation, the autochthonous caprid may be at an
advantage. It is noticeable that the aoudad significantly selects areas with lower
winter rainfall and higher mean summer temperatures, thus resembling its North
African origin (Shackleton 1997). Finally, the areas highly suitable for the aoudad are
closer to urban areas and roads than the Iberian ibex ones, probably because of the
higher niche plasticity of aoudads and the location of their release site, Sierra Espuña
and surrounding mountains (see Cassinello 2000).
Implications for conservation
A competition conflict could arise in areas of potential coexistence between
the Iberian ibex and the aoudad, due to the a priori biological similarities of both
caprids (Schaller 1977). Current distribution of the study species already overlaps
(Figure 1), and our HSMs indicate that this overlap might increase in time. If the
aoudad reaches core native areas of the Iberian ibex (e.g., Sierra Nevada, Sierra de
Cazorla), there might be a conservation problem for the latter. But, would the aoudad
actually be a threat to the Iberian ibex?
Tesis Doctoral
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Given our results, the aoudad might not be such a serious threat for the
Iberian ibex at southeastern Spain, since areas of coexistence are potentially scarce
(merely 14.8% of the whole highly suitable areas for the ibex) and they tend to be
closer to optimal conditions for the ibex, despite the fact that the aoudad has not
probably found its optimum. However, as Putman (1996) highlights, it is problematic
to extract the implications for competitive interactions from measures of niche
overlap. High overlaps can imply competition, but only if resources are limited. In fact,
observations of high overlap might equally well be indicative of a lack of competition
(de Boer and Prins 1990; Putman, 1996). On the other hand, species segregation
can also be a result of competition. However, the aoudad has reached the Iberian
ibex' domains only recently. Therefore, we would not expect that competition leading
to segregation has already happened between both species. As far as we know, it
would be then premature to indicate whether the aoudad will or will not be a threat to
the autochthonous ibex and to which degree.
Despite this reasoning, recent evidence showed the displacement of the
Iberian ibex to suboptimal habitats by extensive goat livestock presence in central
Spain (Acevedo et al. 2006a [Capítulo 1.1]). This should alert us on possible similar
effects in southeastern Spain caused by the aoudad, a species strongly gregarious
(Gray and Simpson 1982; J. Cassinello, pers. obs.).
There is also another threat to be considered. Both study species are
colonizing new habitats in the south of Spain and their expansive movements are
noticeable (Pérez et al. 2002; Cassinello et al. 2004; Acevedo et al. 2006a [Capítulo 1.1]), although both have experienced similar population decreases due to sarcoptic
mange episodes few years ago (Pérez et al. 1997; González-Candela and León-
Vizcaíno 1999). Concerning to future sarcoptic episodes, as the current ibex
distribution in the study region is characterized by isolated nuclei (see Figure 1;
Pérez et al. 2002), contacts between them would be less probable than contacts with
hypothetically infected aoudad populations, which may occupy larger extensions in
the study area. Thus, if the aoudad acts as a vector of this disease, it would then
represent a risk for the ibex.
The increasing presence of allochthonous ungulates in Spain, due to sport
hunting introductions (i.e. the European mouflon and the aoudad), may particularly
threaten local plant species (Rodríguez-Piñero and Rodríguez-Luengo 1992; Zamora
Capítulo 3
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et al. 2001). In the case of the aoudad, its expansion might put in serious risk the yet
threatened, highly endemic flora of Sierra Nevada. The key importance of such
mountain range for the conservation of Iberian plant biodiversity (see, e.g., Castro
Parga et al. 1996; Blanca et al. 1998; García et al. 1999; Lobo et al. 2001)
recommends monitoring the aoudad grazing habits (either intensity and grazed
species) in their expansion.
Finally, there are a series of aspects that may determine the degree of Iberian
ibex and aoudad current expansion and effects caused by the latter on
autochthonous fauna and flora. Recent climatic changes and the strong
desertification which are taking place in the south east of Spain (e.g., Puigdefábregas
and Mendizábal 2004), originating lower rainfall regimes and higher mean annual
temperatures, may cause significant habitat changes which will favour the expansion
of a desert caprid, such as the aoudad. On the other hand, the strong game interest
showed on the aoudad by private game estates in the south of Spain, and the
subsequent risk of animals escaping from badly protected fences (Serrano et al.
2002; Cassinello et al. 2004; P. Acevedo, direct observations), may speed up its
colonizing process and therefore their effects on the host ecosystem.
ACKNOWLEDGEMENTS
We thank J.M. Lobo, A. Jiménez-Valverde, D. Nogués-Bravo and M.B. Araújo
for the output of hours of conceptual and practical discussion on niche modelling. We
are also indebted to J.M. Lobo, A. Jiménez-Valverde and R.M. Chefaoui and for their
work on the original GIS database. The Spanish Instituto Nacional de Meteorología
kindly provided climate data for such database. PA is enjoying a grant from
University of Castilla-La Mancha. JC is currently enjoying a Ramón y Cajal research
contract at the CSIC awarded by the Ministerio de Educación y Ciencia (MEC); he is
also supported by the project PBI-05-010 granted by Junta de Comunidades de
Castilla-La Mancha. JH is supported by a Portuguese FCT (Fundação para a Ciência
e Tecnologia) grant (BPD/20809/2004), and also by the Spanish MEC project
CGL2004-0439/BOS.
Tesis Doctoral
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CAPÍTULO 4
4.1.- SÍNTESIS 4.2.- CONCLUSIONES
SÍNTESIS Y CONCLUSIONES
4.1.- SÍNTESIS
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En este apartado se pretenden destacar los resultados más relevantes de
cada uno de los capítulos presentados. Por lo tanto, éste se plantea como un
apartado resumen de los resultados más destacables, y no se entrará en
demasiados aspectos relativos a la discusión de los mismos, ya que esa tarea ya ha
sido realizada de manera independiente en cada uno de los capítulos.
Capítulo 1- DISTRIBUCIÓN Y ESTATUS DE LAS POBLACIONES DE CABRA MONTÉS (Capra pyrenaica hispanica) EN CASTILLA-LA MANCHA
Resulta destacable el aumento que se ha detectado en la distribución de
cabra montés en Castilla-La Mancha. Han sido descritos dos nuevos núcleos
poblacionales, el de la zona de Casas Ibáñez (noreste de Albacete) y el de los
términos municipales próximos a Los Navalucillos (en los Montes de Toledo). El
primero de ellos parece tener como origen la expansión de las poblaciones de la
Muela de Cortes (suroeste de Valencia) y de las Hoces del Cabriel (sureste de
Cuenca). El núcleo de los Montes de Toledo es posible que se estableciera a partir
de cabras que se han escapado de fincas privadas, valladas perimetralmente, y en
la actualidad han formado una población en terrenos abiertos que presenta, por el
momento, un reducido número de efectivos. Por lo tanto esta especie se ha
mostrado en proceso de expansión también en Castilla-La Mancha, siendo éste
particularmente acentuado en alguno de sus núcleos poblaciones, entre los que se
pueden citar el del sur de Albacete (principalmente las poblaciones de las cuencas
del Río Mundo y Río Segura), y el de la Serranía de Cuenca y Alto Tajo (norte de
Cuenca y este de Guadalajara).
Se puede decir que el incremento de las poblaciones de ungulados silvestres
en la Península Ibérica es debido, en gran medida, a tres causas comunes: cambios
en los usos del suelo que están originando una re-naturalización del medio, ausencia
de depredadores y manejo cinegético al que están sujetas las poblaciones. Como
factor limitante del crecimiento de las poblaciones, habría que añadir la sarna
sarcóptica, que ha provocado grandes fluctuaciones poblacionales. Dependiendo de
la especie objeto de estudio, cada una de estas causas tendrá un peso relativo
distinto. Así, se ha visto que los cambios de uso del suelo han tenido gran influencia
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en la expansión, tanto numérica como del área de distribución, del jabalí en la
Península; sin embargo la actividad cinegética parece ser la principal responsable de
la expansión del ciervo.
En este sentido, la cabra montés muestra una situación intermedia entre los
dos ejemplos anteriormente citados. Se consideran como determinantes de su
expansión la presión cinegética, que es reducida en muchos de sus núcleos
poblacionales, la ausencia de depredadores y la modulación poblacional mediada
por relaciones interespecíficas. Esta última causa no se ha citado anteriormente
como general ya que apenas tiene efecto sobre especies como el ciervo y el jabalí,
aunque en otras, como el corzo y la cabra montés, parece ejercer una elevada
influencia.
Con los datos actualizados de la distribución de la cabra montés, y mediante
el Análisis Factorial de Nicho Ecológico (ENFA, su acrónimo en inglés), se ha podido
caracterizar medioambientalmente el nicho que la cabra montés ocupa en la
provincia de Albacete. Se ha visto que la cabra ocupa zonas marginales dentro del
área de estudio, en pocas palabras, se distribuye por zonas que presentan unas
características ambientales diferentes a las del conjunto de la provincia.
Medioambientalmente, las zonas ocupadas por la cabra presentan elevadas
pendientes y, en menor medida, elevadas altitudes, y están lejos de zonas alteradas
por el hombre, como pueden ser cultivos (viñedos en este caso) y zonas industriales.
Esta descripción de nicho es característica de un ungulado de montaña que ocupa
un medio adecuado para la especie aunque completamente rodeado de zonas
humanizadas, o al menos transformadas por el hombre.
Por otro lado, en este apartado ha quedado manifiesto un desplazamiento de
la cabra montés debido a la presencia de rebaños de ganado caprino. Ambas
especies cohabitan en Castilla-La Mancha siendo habitual que las zonas donde las
domésticas son pastoreadas sean las más adecuadas para las monteses. En este
trabajo se ha podido observar como en las zonas donde hay rebaños de domésticas,
la mayor abundancia de monteses aparece en ambientes a priori sub-óptimos para
ellas, esto es, zonas con mayor proporción de cultivos y menor proporción de
matorrales. Estos resultados pueden ser reflejo de una exclusión competitiva, ya que
en ausencia de ganado caprino se observa la situación inversa, es decir, hay mayor
abundancia de monteses en los medios con reducida proporción de cultivos y
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elevada de matorrales. La relación entre ambas especies, por lo tanto, puede verse
marcada por el establecimiento de una competición por los recursos o bien, aunque
no es excluyente, las monteses pueden estar indirectamente evitando algún parásito
de las domésticas, que llega al medio mediante los excrementos y otros exudados.
Enlazando con esto, se ha realizado un estudio parasitológico, más
concretamente de los nematodos broncopulmonares, en los principales núcleos
poblacionales de cabra montés en Castilla-La Mancha teniendo en cuenta la
presencia de ganado doméstico. Para ello se ha usado una técnica no invasiva
como son los análisis coprológicos. Esta metodología permite la obtención de
prevalencias e intensidades medias de excreción larvaria a nivel de género.
Se han identificado 5 géneros de la familia Protostongylidae y uno de la
familia Dictyocaulidae, y los resultados aquí obtenidos concuerdan con los de otros
estudios sobre la especie en cuanto a los géneros que han sido identificados y a la
frecuencia de aparición de cada uno de ellos. Las prevalencias e intensidades de
excreción larvaria han sido relacionadas con factores ambientales y con la
abundancia de ungulados (cabra montés y ganado caprino) a nivel poblacional. Se
ha obtenido que ambas familias parecen presentar patrones de trasmisión
dependientes de la densidad de cabra montés, ya que sus prevalencias, aunque no
sus intensidades de parasitación, se relacionan positivamente con la abundancia de
cabra montés. Este resultado es interesante puesto que aún siendo dos familias de
parásitos que presentan ciclos de vida muy diferentes, Protostongylidae necesita de
un hospedador intermediario mientras que Dictyocaulus spp. presenta un ciclo
directo, parecen mostrar el mismo patrón de transmisión. Del mismo modo, se ha
obtenido una relación positiva entre la abundancia de ganado caprino y la
prevalencia de Cystocaulus spp., y otra relación, y en el mismo sentido, entre
Protostongylus spp. y la proporción de pastizales. Esto pone de manifiesto que
domésticos y silvestres pueden estar compartiendo parásitos. Además de la relación
directa observada con Cystocaulus spp., la relación entre la prevalencia de
Protostongylus spp. y los pastizales indica la posibilidad de interacción entre ambas
especies, ya que es en los pastizales donde puede ocurrir la exposición común a las
formas infestantes de los citados parásitos en el pasto durante las horas de
alimentación. Estos resultados van en la línea de la relación descrita anteriormente
entre las cabras domésticas y silvestres bajo un planteamiento basado en el uso que
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los animales hacen del medio. La competición interespecífica mediada por parásitos
ha sido descrita como una interacción capaz de desplazar unas especies frente a
otras. Sin embargo, serían necesarios estudios experimentales y comparativos de la
parasitofauna de ambas especies para poder corroborar esta hipótesis. En un
sentido más amplio, estos resultados también evidencian el riesgo de transmisión de
otros agentes infecto-contagiosos derivado del uso común del hábitat, como la sarna
sarcóptica, especialmente cuando el ganado caprino que ocupa zonas marginales
suele presentar las peores condiciones sanitarias dentro de la cabaña ganadera.
Capítulo 2- LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR EL HOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO DE ESPECIES TAXONÓMICAMENTE DISTANTES: EL CIERVO IBÉRICO Y LA CABRA MONTÉS
Las introducciones de ciervos en la Península Ibérica han modificado
notoriamente el área de distribución de la especie. Estas acciones han sido y
continúan siendo habituales dentro de las estrategias de manejo de las poblaciones
de ungulados cinegéticos. En este contexto, se ha recopilado, a modo de ejemplo,
buena parte de la información existente sobre las introducciones de ciervo que se
han realizado con ejemplares provenientes de una sola finca de los Montes de
Toledo, Los Quintos de Mora. Es destacable que desde esta población se
repartieran, entre 1970 y 1990, más de 3500 ciervos que han llegado a un gran
número de regiones para ser introducidos tanto en fincas privadas como en montes
públicos.
En este capítulo se ha usado al ciervo como modelo de especie ampliamente
introducida para estudiar el efecto que estas introducciones pueden tener sobre: i) la
expresión del nicho ecológico de la propia especie introducida, ii) sobre otras
especies autóctonas que comparten el medio. Para abordar el primer punto se han
considerado dos poblaciones de ciervos en función de su origen poblacional, una
población autóctona (distribuida por Sierra Morena), y una población introducida
(considerada así la población de Cazorla, Segura y Las Villas, y otros núcleos
aislados), para modelizar el nicho ocupado por ambas. Los datos de distribución y
origen de estas poblaciones han sido obtenidos de fuentes bibliográficas y de
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muestreos de campo, y se han considerado factores climáticos, geomorfológicos, de
estructura y composición del hábitat, y antrópicos como predictores para construir los
modelos. La modelización se ha realizado siguiendo metodologías descritas y
evaluadas recientemente que se basan en la generación de pseudo-ausencias para,
con ellas, implementar el modelo predictivo mediante Modelos Lineales
Generalizados.
Como primer resultado se ha obtenido que ambas poblaciones ocupan nichos
ecológicos diferentes aún siendo poblaciones de la misma especie. Brevemente, el
nicho ecológico de la población autóctona está condicionado positivamente por el
rango de temperaturas, la disponibilidad de matorral y la altitud máxima, y
negativamente por el índice de evitación del paisaje, la proximidad a las zonas
urbanas y la cantidad de precipitación en invierno. Similarmente, el modelo realizado
para las poblaciones de ciervo introducido ha permitido caracterizar su nicho
ecológico en el área de estudio. La adecuación del hábitat para esta población, esto
es, su nicho realizado, está relacionada positivamente con la cantidad de
precipitación, tanto en invierno como en verano, con el rango de temperaturas, con
el porcentaje de bosques y con la proximidad a los bosques de coníferas, y
negativamente con la proximidad a los núcleos urbanos.
Como puede deducirse desde estas breves descripciones de los nichos de
ambas poblaciones, los condicionantes ambientales que modulan ambos son
claramente distintos. Esto resulta más visible aún observando la representación
espacial de ambos modelos, en la que se puede observar que la distribución
potencial predicha para ambas poblaciones apenas se solapa. Llegados a este
punto se puede afirmar que, según los modelos realizados, el ciervo ha sido
introducido en áreas fuera de su potencial expansivo, esto es, áreas que no
hubiesen alcanzado las poblaciones nativas de manera natural. El establecimiento
de estas poblaciones introducidas puede haber originado perturbaciones en los
ambientes hospedadores. Cuando se menciona el término perturbación se pretende
hacer referencia al impacto que estas poblaciones pueden causar sobre la
vegetación natural, sobre la fauna nativa y sobre la propia especie introducida. Se
considera que, al menos, estas poblaciones introducidas deben ser monitorizadas y
eficientemente manejadas para que sus efectos sobre el ecosistema hospedador no
lleguen a ser críticos y mucho menos irreversibles.
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Por otro lado, y con el fin de abordar el segundo punto expuesto al principio
de este apartado, se ha visto que la distribución potencial predicha para la cabra
montés está ampliamente solapada con la de las poblaciones introducidas de ciervo,
no siendo así con la de las poblaciones de ciervo autóctonas. Este resultado pone
de manifiesto que las introducciones de ciervo han facilitado el solapamiento del
nicho ecológico con la cabra montés. A grandes rasgos, Sierra Morena sería la única
zona del área de estudio donde la población de ciervo autóctono y la cabra montés
cohabitarían. Sin embargo, el solapamiento entre las poblaciones de ciervo
introducidas y las de cabra montés es mucho más amplio, pudiendo llegar a
establecerse en un porcentaje muy alto de las zonas ecológicamente adecuadas
para la cabra montés. Este resultado pone de manifiesto nuevamente que las
introducciones de animales realizadas sin ninguna base científico-técnica pueden
acarrear efectos negativos en el ecosistema. En este caso, el solapamiento de los
nichos de ambas especies podría originar el establecimiento de relaciones de
competencia por los recursos, sobre todo cuando éstos son limitantes, ya que ha
sido descrito que ambas especies, ciervo y cabra montés, presentan un elevado
solapamiento en su dieta. Estas relaciones de competencia podrían acarrear el
desplazamiento de una especie, en este caso la cabra al ser a priori
competitivamente inferior que el ciervo, fuera de su nicho ecológico óptimo de
manera similar a la relación anteriormente descrita entre las cabras domésticas y las
silvestres.
Capítulo 3- LA EXPANSIÓN DE UNGULADOS SILVESTRES MEDIADA POR EL HOMBRE PUEDE FACILITAR EL SOLAPAMIENTO DE NICHO: EL CASO DE UNA ESPECIE EXÓTICA, EL ARRUI, Y LA CABRA MONTÉS
Además de las introducciones realizadas con especies nativas, como el caso
descrito y estudiado en el apartado anterior, son también frecuentes las
introducciones de ungulados exóticos enmarcadas, nuevamente, dentro de la
gestión cinegética. En la Península Ibérica los ungulados exóticos más ampliamente
introducidos son el arrui y el muflón, no descartando con ello que otros ungulados
exóticos, africanos o asiáticos, puedan encontrarse actualmente en suelo peninsular.
Un caso distinto es el del gamo, especie que también ha sido repartida por nuestra
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geografía. Actualmente existe cierta controversia sobre si los gamos deben ser
considerados o no como ungulados exóticos en la península. Parece que, a día de
hoy, destacan los defensores de su condición autóctona que, entre otras cuestiones,
argumentan la posibilidad de que los antecesores del gamo nunca llegaran a
desaparecer tras la última glaciación, por lo que la especie sería propia de la
península; del mismo modo destaca la existencia de citas muy antiguas sobre la
presencia de gamos en la península, entre las que se encuentra una sobre la
existencia de pastores de gamos en la zona del Parque Nacional de Doñana ya en
1580. No se pretende aquí formar parte de este debate, por lo que para estudiar el
efecto de las especies exóticas se ha empleado como modelo al arrui, ya que nadie
tiene dudas sobre su carácter exótico.
Primeramente se ha evaluado el potencial ambiental del área de estudio para
el arrui. Para ello se han implementado dos modelos de adecuación de hábitat
basados en el ENFA, considerando en uno de ellos únicamente variables
ambientales, y en el otro tanto variables ambientales como antrópicas. Comparando
los resultados obtenidos en ambos modelos se puede estudiar el efecto que las
alteraciones que el hombre introduce en el medio producen sobre la selección del
nicho de la especie.
La distribución actual del arrui en el área de estudio se encuentra
fragmentada en dos núcleos poblacionales entre los que todavía parece que no
existe flujo de individuos. El origen de cada uno de ellos es diferente, así el más
ampliamente distribuido, el núcleo de Sierra Espuña, es el resultado de la
introducción de unos pocos animales en 1970, y sin embargo, el núcleo de Alicante
se ha establecido desde unos ejemplares que se escaparon de acotados cinegéticos
privados en 1990. Se ha partido de datos de observaciones de individuos de ambas
poblaciones para construir los modelos predictivos aquí presentados. Al contar con
datos de dos poblaciones independientes, el poder predictivo de los modelos
realizados puede ser evaluado de una manera robusta, es decir, con los datos de
una población, en este caso la de Sierra Espuña, se construyen los modelos y se
evalúa la capacidad predictiva de los mismos con los datos de la otra población, la
de Alicante.
Los resultados de los análisis que se han realizado indican que el nicho
ambiental que está ocupando el arrui en la península es próximo al que ocupa en
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África. Esta afirmación puede resultar un tanto arriesgada, aunque si se enmarca en
el contexto de que el nicho ambiental del arrui se ha caracterizado por reducidas
precipitaciones, altas altitudes y pendientes, y presencia de cobertura forestal, nadie
dudaría que se pudieran estar describiendo condiciones similares a las del macizo
del Atlas, una de las zonas de donde es nativo. Resulta destacable el elevado
potencial ambiental del área de estudio para esta especie, por lo que sería esperable
que el arrui, con elevada capacidad de adaptación al medio, aumentase su actual
área de distribución en años venideros.
Cuando las variables antrópicas (variables relacionadas con las alteraciones
del medio debidas a acciones humanas) se incluyen en los modelos, la adecuación
del territorio varía respecto a la obtenida en el modelo puramente ambiental. El nicho
observado, en este caso, presenta una distribución fragmentada debido a que,
generalmente, los usos del suelo alterados por el hombre se disponen en el espacio
de manera más parcheada que otros usos del suelo que pueden considerarse
naturales. Además de la fragmentación, el nicho observado de la especie, en el que
se incluyen los condicionantes antrópicos, presenta menor amplitud que el basado
únicamente en factores ambientales. Este resultado podría estar indicando que el
arrui se podría haber expandido por el área de estudio a una mayor velocidad, y
podría estar más ampliamente distribuido de lo que está en la actualidad si el medio
hubiera estado poco humanizado. Debe también apuntarse, a la vista de los
resultados, la posibilidad de que podría producirse un aumento de la capacidad
expansiva de esta especie como consecuencia del abandono del medio rural en las
zonas de sierra del área de estudio.
Otra cuestión destacable está relacionada con el índice de la evitación del
paisaje por los ungulados (WULAI, su acrónimo en inglés) y los modelos de
adecuación obtenidos. El cálculo de este índice está basado en el conocimiento
previo que existe sobre la ecología de ungulados, así como en el grado de alteración
humana que presenta cada uno de los usos del suelo. Se ha visto que existe una
relación entre el WULAI y la adecuación del hábitat para el arrui, poniendo esto de
manifiesto que el índice tiene la capacidad de estimar la potencialidad ambiental del
territorio para, al menos, el arrui. Sin embargo, los análisis realizados no permiten
separar de manera independiente los efectos de los diferentes usos del suelo sobre
el rango de expansión de la especie. Serían necesarios más estudios para evaluar el
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efecto individual de los diferentes usos del suelo sobre la distribución de los
ungulados.
Las especies exóticas, como el arrui, pueden ocasionar efectos negativos
sobre la fauna y flora del ecosistema que actúa como hospedador. En el caso de la
fauna, estos efectos serán más acentuados sobre especies taxonómicamente
cercanas, o bien sobre especies ecológicamente convergentes. Desde este punto de
vista, se hipotetiza la posibilidad de que el arrui alcance nichos ecológicos propios
de otras especies nativas, como la cabra montés debido a la potencialidad ambiental
del territorio para esta especie exótica, y el marcado proceso de expansión en el que
están inmersas sus poblaciones. Si esta hipótesis se cumpliera, se podrían
establecer relaciones interespecíficas entre las especies nativas y exóticas a gran
escala, y todo ello podría desembocar en un importante problema de conservación.
Enlazando con esto se han evaluado los nichos ambientales de la cabra
montés y del arrui con el fin de identificar diferencias y similitudes que pudieran
existir entre ellos. Los resultados obtenidos muestran que ambas especies ocupan
hábitats marginales dentro del área de estudio, estando la distribución de la cabra
montés en una situación de mayor equilibrio con las condiciones ambientales que la
del arrui. Este resultado es lógico teniendo en cuenta que la cabra montés es una
especie autóctona que lleva evolucionando con el medio desde tiempos del
Paleolítico. Sin embargo el arrui, aunque ya lleva más de 30 años en la península,
todavía no ha alcanzado su óptimo ambiental. Esta especie se ha mostrado menos
tolerante a los gradientes ambientales secundarios que la cabra, siendo este
resultado un indicio más de que el arrui todavía no ha alcanzado todas las zonas
ambientalmente adecuadas del área de estudio, aunque estos y otros estudios dejan
entrever que el que esta especie alcance su nicho óptimo en la Península Ibérica es
cuestión de tiempo.
La descripción del nicho de la cabra montés obtenida aquí es similar a la
obtenida en los análisis realizados en el Capítulo 1. Las diferencias que se pueden
encontrar entre ambas descripciones son debidas a que los modelos predictivos son
contexto-dependientes, esto es, dependen de la extensión y de los gradientes
ambientales existentes en el área de estudio. En este análisis, el nicho ambiental de
la cabra montés se caracteriza por presentar bajas temperaturas en verano,
elevadas altitudes y pendientes, y altas precipitaciones en invierno. El nicho del arrui
Capítulo 4
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se caracteriza por elevadas pendientes y amplios rangos de altitud, y con elevada
presencia de bosques. Estos análisis muestran que los nichos de ambas especies
presentan unos rasgos ecológicos que pueden ser fácilmente relacionados con
ambientes agrestes. De este modo, se puede decir que el arrui ocupa una amplia
variedad de sistemas montañosos de diferente altitud que se encuentran dispersos
por el área de estudio, mientras que la cabra montés se distribuye por áreas muy
restringidas en el contexto del presente estudio, que son los sistemas montañosos
con mayores altitudes.
Se ha realizado una comparación entre las áreas que presentan alta
adecuación de hábitat para las especies estudiadas, considerando para ello tres
escenarios: i) zonas de elevada adecuación para la cabra montés pero no para el
arrui, por lo tanto “exclusivas” de cabra, ii) zonas de elevada adecuación para el arrui
pero no para la cabra, “exclusivas” de arrui y iii) zonas de elevada adecuación para
ambas especies, que se han denominado zonas de potencial coexistencia. Existen
sutiles diferencias ambientales que definen cada uno de los escenarios
considerados. Estas diferencias ponen de manifiesto que la cabra montés presenta
menor plasticidad ecológica que el arrui, esto es, las monteses sólo habitan en
medios donde sus requerimientos ambientales queden cubiertos, mientras que el
arrui tiene una elevada capacidad para adaptarse a medios distintos lo que hace que
actúe como una especie generalista en lo que a preferencia de hábitat se refiere.
Climatológicamente hablando, las áreas de coexistencia parecen ser más similares a
las “exclusivas” de la cabra montés que a las “exclusivas” de arrui. Esto puede
indicar que, ante una hipotética relación competitiva entre ambas especies, la cabra
montés estaría en situación ventajosa respecto al exótico. Esta afirmación debe ser
considerada en el contexto de que actualmente el arrui puede no haber alcanzado
su nicho óptimo, por lo que su proceso expansivo y adaptativo podría hacer que esta
situación se viese alterada en un futuro. Por otro lado, la escasa plasticidad
ecológica que ha mostrado la cabra montés en este estudio, podría estar indicando
que ante una situación de competencia con una especie que alcance y colonice su
nicho ecológico, se producirían efectos negativos sobre las poblaciones de
monteses ya que si éstas son desplazadas de sus ambientes óptimos,
previsiblemente, y debido a su reducida capacidad de adaptación, el estatus de sus
poblaciones podría verse mermado.
Tesis Doctoral
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Además de la competición por los recursos, la expansión del arrui por los
ambientes donde se asientan poblaciones de cabra montés puede ser una amenaza
para las nativas debido a que ambas especies comparten enfermedades, como por
ejemplo la sarna sarcóptica. Por ello, otro de los posibles efectos negativos que los
arruis pueden ejercer sobre la cabra montés radica en que los exóticos podrían
llegar a actuar como vehículos de enfermedades facilitando su transmisión entre
poblaciones.
4.2.- CONCLUSIONES
Tesis Doctoral
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Las conclusiones que se han podido extraer desde los estudios realizados en
esta Tesis Doctoral son:
1- La cabra montés está en marcado proceso expansivo en Castilla-La Mancha
destacando los núcleos de la Serranía de Cuenca-Alto Tajo y el del sur de
Albacete. Han sido descritos dos nuevos núcleos poblacionales, el de Casas
Ibáñez, y el de Los Navalucillos. En la provincia de Albacete, las principales
zonas adecuadas para las cabras se caracterizan por: i) estar muy ligadas a las
cuencas del Río Mundo y del Río Segura, ii) presentar orografía complicada, y iii)
presentar una reducida proporción de usos del suelo transformados por el
hombre.
2- La presencia de ganado caprino y su interacción con variables ambientales ha
permitido detectar una relación interespecífica entre domésticas y silvestres. El
ganado caprino desplaza a las cabras monteses hacia hábitats, a priori, menos
adecuados para ellas, como son los medios con elevada proporción de cultivos y
reducida proporción de matorrales.
3- Los nematodos broncopulmonares, ampliamente distribuidos por la poblaciones
de cabra montés de Castilla-La Mancha, presentan patrones de excreción de
larvas compatibles con fenómenos de transmisión dependientes de la densidad de
hospedadores. Por vez primera se han encontrado evidencias de que cabra
montés y ganado doméstico podrían compartir la epidemiología de algunos
géneros de nematodos broncopulmonares. Estos parásitos podrían ser de
utilidad como indicadores en una red de vigilancia sanitaria de las poblaciones de
cabra montés de Castilla–La Mancha.
4- Las introducciones de ciervo se han realizado en áreas no adecuadas para la
especie según los requerimientos ambientales que han mostrado las poblaciones
autóctonas. Introducir ciervos más allá de su potencial dispersivo hace que la
expresión del nicho ecológico de la especie se vea modificada. La introducción
de ciervos con fines cinegéticos ha facilitado el solapamiento de su “nuevo” nicho
ecológico con el de la cabra. Estrategias de gestión, como las introducciones
para la generación de nuevas poblaciones, deben tener en cuenta los
requerimientos ambientales de la especie en sus núcleos originales con el fin de
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no perturbar ni el comportamiento de la propia especie, ni el ecosistema
hospedador.
5- Los resultados de los análisis que se han realizado indican que el nicho
ambiental que está ocupando el arrui en la península es próximo al que ocupa en
África. Éste se caracteriza por reducidas precipitaciones, altas altitudes y
pendientes, y presencia de cobertura forestal.
6- Las variables relacionadas con las alteraciones del medio debidas a acciones
humanas fragmentan el nicho observado y restringen levemente la distribución
potencial del arrui. Estos resultados sugieren que el arrui se hubiera expandido
por el área de estudio a una mayor velocidad, y estaría más ampliamente
distribuido de lo que está en la actualidad, si el medio hubiera estado menos
humanizado.
7- Existen similitudes en las características ambientales que definen los nichos del
arrui y de la cabra montés. Sin embargo, pequeñas diferencias ambientales
definen los nichos exclusivos de ambas especies como las áreas donde,
potencialmente, pueden cohabitar. Estas últimas presentan características
ambientales más próximas al nicho de la cabra que al del arrui. Por ello se
concluye que: i) la cabra montés presenta menor plasticidad ecológica que el
arrui, ii) ante una hipotética relación competitiva entre ambas especies, la cabra
montés estaría en situación ventajosa respecto al arrui debido a que esta relación
se establecería en un medio con características ambientales más adecuadas
para la cabra. Esta afirmación debe ser considerada en el contexto de que
actualmente el arrui no ha alcanzado su nicho óptimo, por lo que su proceso
expansivo y adaptativo podría hacer que esta situación se viese alterada en unos
pocos años.
