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EL HORNERORevista de Ornitología Neotropical

Volumen 21 Número 2 - Diciembre 2006

Hornero 21 (2) : 61-117, 2006

www.digital.bl.fcen.uba.arPuesto en linea por la Biblioteca Digital de la Facultad de Ciencias Exactas y Naturales

Universidad de Buenos Aires

Número especial

Nuevas miradas sobre las aves migratoriasamericanas: técnicas, patrones,

procesos y mecanismos

Editores

VÍCTOR R. CUETO

JAVIER LOPEZ DE CASENAVE

NUEVAS MIRADAS SOBRE LAS AVES MIGRATORIAS AMERICANAS:TÉCNICAS, PATRONES, PROCESOS Y MECANISMOS

VÍCTOR R. CUETO 1,2 Y JAVIER LOPEZ DE CASENAVE 1

1 Grupo de Investigación en Ecología de Comunidades de Desierto (ECODES), Depto. Ecología, Genética yEvolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Piso 4, Pab. 2, Ciudad

Universitaria, C1428EHA Buenos Aires, Argentina.2 [email protected]

Hornero 21(2):61–63, 2006

Editorial

La migración es generalmente consideradacomo un mecanismo que permite explotarincrementos estacionales en la abundancia delos recursos y evadir los momentos del añocuando éstos escasean. Entre las aves la migra-ción está muy extendida, siendo quizá elgrupo de vertebrados en el cual se producenlos mayores desplazamientos de especies eindividuos (por ejemplo, se estima que aproxi-madamente 50000 millones de aves realizanmovimientos migratorios en algún momentodel ciclo anual 1). En América, las aves migra-torias de los dos hemisferios comparten unorigen evolutivo común, la avifauna Neotropi-cal, y muestran un número similar de espe-cies 2. Sin embargo, nuestro conocimientosobre ambos sistemas migratorios difiere nota-blemente. A pesar de que ya a principios delsiglo XIX Azara 3 había descripto los patronesmigratorios de varias especies rioplatenses,muy poco se adelantó en la comprensión dela biología de las aves migratorias en Américadel Sur comparado con América del Norte 4–6.

La migración en las aves es un proceso com-plejo que requiere la adecuación de un con-junto de factores biológicos para que el viajesea exitoso. Estos factores incluyen instruccio-nes genéticas sobre el calendario y la dura-ción de los desplazamientos migratorios,cambios fisiológicos para el almacenamientode nutrientes (lípidos y proteínas) que utili-zan como combustible durante el vuelo y

adaptaciones del comportamiento para la na-vegación y orientación 1. Además, la supervi-vencia de las poblaciones de las especiesmigratorias depende de las condiciones queenfrentan en sus áreas de reproducción, enlas de reposo y en las que utilizan durante elviaje entre ambas zonas. Esta característica delciclo de vida de las aves migratorias les con-fiere un grado importante de vulnerabilidada las variaciones ambientales y a los cambiosproducidos por las actividades del hombre.Por ejemplo, en varias especies de pase-riformes migratorias que se reproducen enEuropa e invernan en África, y en otras quese reproducen en América del Norte y pasanel invierno en América Central y América delSur, se han registrado importantes declinacio-nes poblacionales en los últimos 30–40 años 7.Sin embargo, las causas de estas declinacio-nes no fueron similares. En el Viejo Mundolos motivos parecen estar relacionados con losefectos de las sequías y con el incremento dela desertificación en África (i.e., en el área noreproductiva). En cambio, en el Nuevo Mundolas causas serían principalmente los cambiosprovocados por el hombre en amplias zonasde América del Norte (i.e., en el área dereproducción), en especial la fragmentaciónde los bosques, con el consecuente incrementode predadores de nidadas y del parasitismopor Molothrus ater 7. En el caso de las aves quemigran en América del Sur no hay actual-

62 NÚMERO ESPECIAL – AVES MIGRATORIAS Hornero 21(2)

mente posibilidad de evaluar el estado de suspoblaciones y, menos aún, especular sobre sustendencias poblacionales. Sin embargo, con-siderando las profundas alteraciones dehábitat que el hombre ha producido, es deesperar que las especies migratorias esténenfrentando un escenario complejo para suconservación. Por ejemplo, registros históricosindican que las poblaciones de Alectrurus risorallegaban hasta Buenos Aires durante la épocareproductiva y se desplazaban hasta Paraguayy Brasil durante la época de reposo reproduc-tivo 8, pero actualmente estas poblaciones es-tán restringidas al noreste de Argentina y sonconsideradas residentes 9.

Conocer los aspectos biológicos básicos quecaracterizan a las aves migratorias tiene unvalor fundamental para mejorar nuestras po-sibilidades de organizar planes que ayuden aconservar a este grupo de aves. Pero, además,ese conocimiento puede jugar un papel im-portante frente a problemas epidemiológicos.En sus desplazamientos, las aves pueden ac-tuar como transporte de virus y bacterias per-judiciales para la salud y la economía delhombre 1. En estos últimos tiempos se han re-gistrado dos situaciones de expansión de en-fermedades en las que han participado avesmigratorias y que tuvieron gran repercusióninternacional: el virus del Oeste del Nilo 10 yel virus de la influenza aviar 11. Por lo tanto,conocer los patrones migratorios y las causasque los determinan puede ser de gran ayudapara planificar escenarios epidemiológicos.

Buscando desafiar la escasez de conocimien-tos sobre las aves migratorias en América delSur, se desarrolló el simposio “Aves migratoriasamericanas: algunos apuntes para conocerlas”durante la XI Reunión Argentina de Ornito-logía, llevada a cabo en Buenos Aires enseptiembre de 2005. Los objetivos del simpo-sio eran aportar información sobre diversosaspectos de la migración en el continente ame-ricano y presentar nuevas técnicas para suestudio. Como las migraciones están presentesen casi todos los órdenes taxonómicos de lasaves, el simposio se caracterizó por el aportede trabajos sobre grupos muy diferentes, in-cluyendo Falconiformes, Charadriiformes yPasseriformes. Un conjunto de investigadoresde Argentina y EEUU que trabajan principal-mente en América del Sur fueron invitados aparticipar, y cinco de los expositores que for-

maron parte del simposio aceptaron volcar enel papel sus presentaciones. El resultado eseste número especial de El Hornero sobre avesmigratorias americanas titulado “Nuevas mi-radas sobre las aves migratorias americanas:técnicas, patrones, procesos y mecanismos”.

En el primero de los artículos presentados,Bechard y colaboradores (pp. 65–72) exami-nan, utilizando telemetría satelital, las carac-terísticas del patrón migratorio de Buteoswainsoni entre América del Norte y Américadel Sur, analizando la velocidad y la duraciónde la migración y los cambios en la masa cor-poral de machos, hembras y juveniles en dife-rentes momentos del ciclo migratorio. Susresultados refutan la hipótesis del ayunodurante la migración y sugieren, en cambio,que las aves utilizan las áreas de parada pararecuperar reservas antes de continuar sus des-plazamientos migratorios. Considerando queButeo swainsoni ha sufrido importantes even-tos de mortalidad debido al uso de insecticidas(particularmente en su área no reproductivaen Argentina), este descubrimiento es de sumaimportancia para los planes de conservación,ya que plantea la necesidad de considerar nosolo las áreas de reproducción y reposo, sinotambién las zonas de parada para un efectivomanejo de las poblaciones de esta rapaz.

Torres Dowdall y colaboradores (pp. 73–84)describen una nueva técnica para determinarla conectividad de las poblaciones de especiesmigratorias que utiliza la composición deisótopos estables de los tejidos de las aves(principalmente en las plumas remeras), uncampo de intensa investigación en los últimosaños 12. Si bien la técnica ha sido aplicadaexitosamente en varias especies de aves, losautores precisan sus alcances y limitaciones,y proveen recomendaciones para mejorar losdiseños de los estudios de manera de mini-mizar la variabilidad de las mediciones e incre-mentar la determinación del origen geográficode los individuos.

La biología de las golondrinas durante lamigración y en las áreas de reposo reproduc-tivo ha recibido muy poca atención en com-paración con los estudios en las áreas de cría.En el tercer trabajo de este número especial,Winkler (pp. 85–97) ofrece una revisión de estatemática. Su análisis remarca la importanciade los sitios con dormideros en el patrón dedesplazamientos de estas aves, lo que las hace

2006 NÚMERO ESPECIAL – AVES MIGRATORIAS 63

extremadamente flexibles con respecto a otraspaseriformes. Además, destaca la utilidad delincremento en la disponibilidad de radaresclimáticos en EEUU como herramienta paramejorar el estudio de los patrones de distri-bución de Tachycineta bicolor y Progne subisdurante la época de reposo reproductivo.

Por su parte, Jahn y colaboradores (pp. 99–108)examinan la importancia de estudiar los me-canismos involucrados en los patronesmigratorios de las aves en América del Sur, yparticularmente el patrón de superposiciónentre áreas de reproducción y de reposo quemuestran muchas especies migratorias. Comoel desarrollo teórico y empírico de lo que sesabe actualmente sobre el fenómeno de lamigración en aves se ha generado principal-mente en sistemas migratorios del Hemisfe-rio Norte, la dilucidación de las causas de lospatrones migratorios en América del Sur per-mitirá poner a prueba las hipótesis derivadasde los otros sistemas, mejorando nuestro co-nocimiento general del fenómeno de la mi-gración e incrementando las bases científicaspara la conservación de las aves migratorias.

En el último de los artículos de este número,González y colaboradores (pp. 109–117) enfo-can sobre un problema poco representado enla literatura sobre aves migratorias: la ecologíade los sitios de parada. En particular, anali-zan el papel de las escalas migratorias en ladinámica poblacional de Calidris canutus rufa,un chorlo que sufrió una drástica declinaciónpoblacional debido a la disminución de suprincipal alimento por sobrepesca en suúltima escala en la migración hacia las áreasde reproducción en el Ártico. Los autoresencontraron un efecto dominó sobre la super-vivencia y reproducción de esta ave, debido aque el efecto de la disminución de alimentoen su última parada antes de arribar a las áreasde reproducción se amplifica en los individuosque tardan más en abandonar los sitios deparada australes.

En conjunto, estos aportes brindan nuevosenfoques, información novedosa y explicacio-

nes alternativas para aumentar nuestro enten-dimiento de la biología de las aves migratoriasamericanas. Esperamos que esta diversidad detemas y puntos de vista sirva para estimularel estudio de este fascinante grupo de aves,especialmente en América del Sur.

1 BERTHOLD P (2001) Bird migration: a general survey.Oxford University Press, Oxford

2 RAPPOLE JH (1995) The ecology of migrant birds: a Neo-tropical perspective. Smithsonian Institution Press,Washington DC

3 AZARA F DE (1802–1805) Apuntamientos para la histo-ria natural de los páxaros del Paraguay y Río de la Plata.Imprenta de la Viuda de Ibarra, Madrid

4 KEAST A Y MORTON ES (1980) Migrant birds in theNeotropics: ecology, behaviour, distribution, and conserva-tion. Smithsonian Institution Press, Washington DC

5 HAGAN JM Y JOHNSTON DW (1992) Ecology and con-servation of Neotropical migrant landbirds. SmithsonianInstitution Press, Washington DC

6 GREENBERG R Y MARRA PP (2005) Birds of two worlds.The ecology and evolution of migration. SmithsonianInstitution y The Johns Hopkins University Press,Washington DC

7 NEWTON I (2004) Population limitation in migrants.Ibis 146:197–226

8 DI GIACOMO AS Y DI GIACOMO AG (2004) Extinción,historia natural y conservación de las poblacionesdel Yetapá de Collar (Alectrurus risora) en la Argen-tina. Ornitología Neotropical 15(Supl.):145–157

9 DI GIACOMO AG (2005) Aves de la Reserva El Bagual.Pp. 201–465 en: DI GIACOMO AG Y KRAPOVICKAS SF(eds) Historia natural y paisaje de la Reserva El Bagual,Provincia de Formosa, Argentina. Inventario de la faunade vertebrados y de la flora vascular de un área protegidadel Chaco Húmedo. Aves Argentinas/AsociaciónOrnitológica del Plata, Buenos Aires

10 MCLEAN RG (2006) West Nile virus in North Ameri-can birds. Ornithological Monographs 60:44–64

11 CLARK L Y HALL J (2006) Avian influenza in wildbirds: status as reservoirs, and risks to humans andagriculture. Ornithological Monographs 60:3–29

12 BOULET M Y NORRIS DR (2006) Patterns of migra-tory connectivity in two Neartic-Neotropical song-birds: new insights from intrinsic markers. Ornitho-logical Monographs 61:1–88

2006 DO SWAINSON'S HAWKS FAST ON MIGRATION? 65

A RE-EVALUATION OF EVIDENCE RAISES QUESTIONSABOUT THE FASTING MIGRATION HYPOTHESIS FOR

SWAINSON’S HAWK (BUTEO SWAINSONI)

MARC J. BECHARD 1,2, JOSE H. SARASOLA 2 AND BRIAN WOODBRIDGE 3

1 Raptor Research Center, Department of Biology, Boise State University. Boise, ID 83725, USA. [email protected] Centro para el Estudio y Conservación de las Aves Rapaces en Argentina (CECARA), Facultad de Ciencias Exactas

y Naturales, Universidad Nacional de La Pampa. Avda. Uruguay 151, 6300 Santa Rosa, La Pampa, Argentina.3 U. S. Fish and Wildlife Service. PO Box 1006, Yreka, CA 96097, USA.

ABSTRACT.— We examined the fasting migration hypothesis for Swainson’s Hawks (Buteoswainsoni) by estimating the length, duration, and speed of the migration between North andSouth America and measuring changes in their body masses at various times throughout theyear. We instrumented 34 adult Swainson’s Hawks with satellite radios on their breeding groundsin western North America to determine the duration, length, and speed of the migration. Mi-grating south at 188 km/day, it took Swainson’s Hawks 51 days to complete their 13504 km mi-gration to their austral summer grounds. Averaging only 150 km/day on their return migration, ittook them 60 days to complete the shorter 11952 km migration back to North America. Adultmale and female Swainson’s Hawks had average body masses of 872 g and 1131 g, respectively,when they departed from North America in September and their body masses upon arrival inArgentina averaged 759 g for adult males and 933 g for adult females, indicating they lost only anaverage of 18% of their body masses during migration. Adult male and female Swainson’s Hawkshad body masses of 792 g and 1013 g, respectively, in February prior to their departure fromArgentina and they returned to the breeding grounds in North America weighing 802 g and1087 g in April. Our results indicate that the fasting migration model does not predict the actualbody masses of Swainson’s Hawks during the migration season and it should be modified toaccount for either lower energy expenditures during migration or the possibility that the birdsuse a stopover strategy during migration, feeding and regaining, or maintaining, fat stores alongthe migration route.KEY WORDS: body mass, Buteo swainsoni, fasting, migration, Swainson’s Hawk.

RESUMEN. NUEVAS EVIDENCIAS CUESTIONAN LA HIPÓTESIS DEL AYUNO DURANTE LA MIGRACIÓN PARA EL

AGUILUCHO LANGOSTERO (BUTEO SWAINSONI).— Se examinó la hipótesis del ayuno durante la mi-gración para el Aguilucho Langostero (Buteo swainsoni) mediante la estimación de la longitud, laduración y la velocidad de migración entre América del Norte y del Sur, y la medición de loscambios en el peso corporal en varios momentos a lo largo del año. Se colocaron transmisoressatelitales a 34 aguiluchos adultos en sus áreas de cría en el oeste de América del Norte para deter-minar la duración, la longitud y la velocidad de la migración. En su migración al sur, a 188 km/día,el Aguilucho Langostero tarda 51 días para completar los 13504 km hasta las áreas donde perma-nece durante el verano austral. A un promedio de solo 150 km/día en su migración de retorno, letoma 60 días completar los 11952 km de regreso a América del Norte. Los machos y hembrasadultos de Aguilucho Langostero tuvieron un peso corporal promedio de 872 g y 1131 g, respec-tivamente, cuando partían de América del Norte en septiembre, y su peso corporal al arribar aArgentina promedió 759 g en los machos adultos y 933 g en las hembras adultas, indicando quepierden, en promedio, solo el 18% de su peso corporal durante la migración. En febrero, antes desu partida de Argentina, los machos y hembras adultos de Aguilucho Langostero tuvieron unpeso corporal de 792 g y 1013 g, respectivamente, y llegaron a sus áreas de cría en América delNorte pesando 802 g y 1087 g, en abril. Los resultados indican que el modelo de ayuno durante lamigración no predice los pesos corporales reales del Aguilucho Langostero durante la estaciónmigratoria y que debería ser modificado para dar cuenta de menores gastos energéticos durantela migración o la posibilidad de que las aves usen una estrategia de paradas durante la migración,alimentándose e incorporando (o manteniendo) grasa a lo largo de la ruta migratoria.PALABRAS CLAVE: Aguilucho Langostero, ayuno, Buteo swainsoni, migración, peso corporal.

Received 2 January 2006, accepted 1 December 2006

Hornero 21(2):65–72, 2006

66 BECHARD ET AL. Hornero 21(2)

Migration poses numerous behavioural andphysiological challenges for birds. For mostspecies, fat is the fuel used on migration. Priorto and during migration, birds deposit fat andthen use it to meet their energy demands(Weis-Fogh 1952, Blem 1980, Ramenofsky1990, McWilliams et al. 2004). Most warblersand shorebirds undergo rapid premigratoryfattening depositing more than 50% of theirbody weight in fat to make long, non-stopflights over oceans, deserts, or other inhospi-table areas where refuelling is difficult if notimpossible (Blem 1980, Moore and Kerlinger1987, Ramenofsky 1990, Jenni and Jenni-Eiermann 1998). However, for most speciesincluding raptors, migration is a slower, moreextended process, involving a “stop and go”migration pattern with birds typically feed-ing en route as they encounter opportunitiesto eat. Using this strategy, migrants may main-tain somewhat elevated levels of stored bodyfat, perhaps using this depot to carry themthrough periods of food scarcity. Neverthe-less, they do not store enough premigratoryfat to fuel their entire migration. This necessi-tates a refuelling strategy which spares theirreserve energy supply and may augment theirfat stores when food supplies are plentifulalong the migration route (Berthold 1975).

There is very little quantitative informationon how birds use stored fat during migration.Most studies that have dealt with this issuehave focused on birds that use powered (flap-ping) flight during migration (Berger and Hart1974, Blem 1980, Ramenofsky 1990). There islittle information about fat deposition and useby falconiforms either before or during mi-gration. However, several authors have main-tained that migrating raptors take on fatdeposits during migration. For example,American Kestrels (Falco sparverius) deposit2–4% body fat during early autumn(Gessaman 1979) and it is well-known thatAmur Falcons (F. amurensis) are extremely fatprior to their long migration over the IndianOcean from India to East Africa (Ali and Ripley1978). Western Honey-buzzards (Pernisapivoris) also undergo large variations inweight that are attributed to massive fat depo-sition prior to migration (Glutz von Blotzheimet al. 1971). Despite this, there is little infor-mation on the energy expenditure involvedwhen birds use soaring flight in long-distancemigrations.

The Swainson’s Hawk (Buteo swainsoni) isone such long-distance, “stop and go” soar-ing migrant. Each year, it migrates back andforth between the plains, shrublands, steppes,and pampas of North and South America.Prior to its southward migration, it changesfrom a carnivore to an insectivore diet andhawks are frequently observed in flocks ofhundreds of birds gorging themselves on in-sects such as grasshoppers (Johnson et al.1987). As they migrate through the Meso-american land corridor at about 30°N latitudethese small flocks coalesce into fewer, verylarge flocks consisting of tens of thousands ofindividuals. As they continue to migratesouthward, the hawks are funnelled into ex-tremely dense concentrations with an esti-mated 800000 hawks passing over the Isthmusof Panama during a nine-day period in lateOctober (Bildstein, unpublished data). Someindividuals drop out of the migration in Cen-tral America (Smith et al. 1986). Nevertheless,most continue their southward migrationwith some settling in Brazil, Uruguay, andBolivia, but most not stopping until they reachtheir austral grounds in the pampas region ofArgentina (England et al. 1997).

Based on the assertion that Swainson’sHawks observed roosting overnight inPanama seemed not to have cast pellets or de-fecated in roost trees (on the basis of a lack of“whitewash” on the forest floor below roosts),and because the species migrates in such largenumbers over most of its migratory route, ithas been suggested that Swainson’s Hawksmay complete most or all of their migrationwithout feeding by fasting and metabolizingfat stores laid down before they depart onmigration (Brown and Amadon 1968, Smithet al. 1986). Smith et al. (1986) presented amodel based on estimates of the energetic costand duration of this migration. Their modelpredicted that hawks would need to accumu-late body fat deposits equalling about 55% oftheir lean body mass before migration to suc-cessfully complete the journey in either direc-tion. Using the model’s assumptions, a maleSwainson’s Hawk with a lean body mass of600 g would have to store 330 g of body fatprior to migration. This model has receivedcriticism (Kirkley 1991) and it is plagued withweaknesses because there have never beenany records of premigratory weights for theSwainson’s Hawk.


Due to the lack of information on migrantSwainson’s Hawks, we undertook a study todocument the timing and geographic lengthof the Swainson’s Hawk migration and thechanges in its body mass prior to its depar-ture on migration and after its arrival on theirbreeding and austral summer grounds. Weused these body mass estimates to test the fast-ing migration model proposed by Smith et al.(1986) in an effort to determine if Swainson’sHawks store sufficient amounts of fat to fueltheir migration without stopping to eat alongthe way.

METHODS

We carried out our main sampling work intwo study areas. One was in the Snake RiverPlain of southern Idaho in North America andthe other was located in the pampas regionof South America in Buenos Aires Provinceand La Pampa Province, central Argentina.Both study areas have undergone extensiveagricultural alteration and currently most ofthe landscape is dominated by croplandsplanted in row crops and plantations of exotictree species including black locust (Robiniapseudoacacia) trees in Idaho and eucalyptus(Eucalyptus spp.) trees in Argentina.

To track the migration of hawks between thetwo study areas, we captured breeding femaleSwainson’s Hawks at their nest sites through-out their North American breeding groundsand instrumented them with Microwave Elec-tronics, Inc. satellite transmitters (PTTs).Details on trapping methods, attachmenttechniques, and duty cycles of PTTs can befound in Fuller et al. (1998). We used the loca-tions obtained from PTTs to determine thelength of the migration route, the duration of

migration period, and the speed of migrationbetween North and South America.

To estimate fat stores before and after migra-tion, we captured and weighed male andfemale Swainson’s Hawks between 1998–2001to obtain body mass estimates for Swainson’sHawks throughout the time they were ontheir breeding grounds in North America andon their austral summer grounds in Argen-tina. We captured hawks using either bal-chatri traps with mouse lures or dho-gaza netswith Great Horned Owl (Bubo virginianus)lures. Captured hawks were weighed using1000 and 2000 g Pesola scales. We also tookmeasurements of wing chord, tail length, cul-men length, tarsus length and width, andhallux length using steel rulers or calipers.Breeding adults were sexed on the basis oftheir behaviour at their nest sites. Juvenilesand adults captured on their austral summergrounds were sexed using blood samples andPCR amplification of chromohelicase-DNAgenes located on the two sex chromosomes(Griffiths et al. 1998). Blood samples were ob-tained from the brachial vein of captured birdsusing 1 ml syringes, and blood was stored ineither EDTA buffer solution or 80% alcohol(Burgoyne et al. 1994).

RESULTS

We captured and attached satellite radios to34 breeding Swainson’s Hawks throughoutthe species’ North American breeding rangein nine states and provinces. From theseinstrumented hawks, we obtained 27 com-plete southward and 19 complete northwardmigration tracks (Table 1). All of the tracksextended between western North Americaand central Argentina and both the southward

Table 1. Southward and northward migration tracks of satellite-tagged Swainson’s Hawks.

Southward Northward

Number of individuals tracked 27 19 Departure dates 28 Sep–10 Oct 25 Feb–12 Mar Arrival dates 15 Nov–30 Nov 13 Apr–10 May Mean total migration distance (km) 13503.70 11951.63 Mean rate of migration (km/day) 188.00 149.59 Mean duration of migration (days) 51 60 Range in duration of migration (days) 46–58 43–75


and northward tracks followed a similar route,almost entirely inland except through south-ern Mexico and Central America where someof the segments of the tracks were along thecoast. There were no crossings of large bodiesof water. Departure dates on the southwardmigration varied between late September andearly October, and on the northward migra-tion departure dates varied between lateFebruary and mid-March. The mean total dis-tance hawks migrated southward was slightlyover 13500 km, compared to a mean of slightlyless than 12000 km on the northward migra-tion. Hawks migrating southward migratedat an average rate of 188 km/day, and thosemigrating northward averaged 150 km/day.The duration of the southward and north-ward migrations averaged 51 and 60 days,respectively. Arrival dates in Argentina variedbetween mid- to late November. Arrival dateson the North American breeding groundsvaried between mid-April and early May.

We captured and obtained body mass mea-surements for a total of 41 adult males and 25adult females on their North American breed-ing grounds in 1998 between the time of theirarrival in April and May until their departureon migration in September and October(Table 2). Of these 66 individuals captured intheir breeding area, 21 adults were capturedshortly after their arrival at nesting areas inApril and May. An additional 18 breedingadults were captured in July prior to the fledg-ing of their young. In September, 27 adultswere captured in the vicinity of their nestingareas prior to their departure on migration.In Argentina, we captured a total of 74 adultmales and 37 adult females and 75 juvenilemales and 39 juvenile females between the

time of their arrival on and departure fromtheir austral summer grounds. Of these 225captured hawks in Argentina, a total of 59adults and 39 juveniles were captured in De-cember, whereas 52 adults and 75 juvenileswere captured in January and February priorto their departure on the northward migra-tion (Table 2). From the literature, we also ob-tained estimates of the body mass data for 9adult male and 12 adult female Swainson’sHawks and 14 juvenile male and 6 juvenilefemale Swainson’s Hawks that were capturedin October from 1972–1983 in Panama, ap-proximately midway through their southwardmigration (Smith et al. 1986).

Adult male and female Swainson’s Hawksarrived on their breeding grounds in April andMay averaging (± SD) 802 ± 54 g and1087 ± 87 g, respectively (Fig. 1). During thebreeding season, adults lost body mass andaveraged only 707 ± 29 g for males and

Table 2. Numbers of adult and juvenile Swainson’s Hawks captured in southern Idaho and Argentina.

Figure 1. Annual variations in the body masses (ing) of adult (open circles) and juvenile (filled circles)female and adult (open squares) and juvenile(filled squares) male Swainson’s Hawks in North,Central, and South America.

North America Argentina Adult

Male Adult

Female Adult Male

Juvenile Male

Adult Female

Juvenile Female

April-May 16 5 July 10 8 September 15 12 December 40 29 19 10 January-February 34 46 18 29


1013 ± 38 g for females in July. By September,they had regained body masses averaging872 ± 61 g for males and 1131 ± 72 g for fe-males. Body mass measurements reported forSwainson’s Hawks in Panama (Smith et al.1986), approximately midway through theirsouthward migration, showed that adult maleand female Swainson’s Hawks had lowerbody masses and averaged only 730 ± 42 g,and 980 ± 134 g, respectively. Likewise, juve-nile male and female Swainson’s Hawks inPanama had body masses of only 715 ± 38 gand 941 ± 51 g, respectively (Smith et al. 1986).Adult hawks arriving in Argentina hadslightly higher body masses for adult maleswhich averaged 759 ± 86 g, but about 47 glower for adult females which averaged933 ± 61 g. Juvenile hawks arrived in Argen-tina with lower body masses averaging678 ± 29 g for juvenile males and 802 ± 68 gfor juvenile females. After they settled ontotheir austral summer grounds in Argentinaboth sexes gained body mass. By January andFebruary, adult males averaged 792 ± 50 g,adult females averaged 1013 ± 70 g, juvenilemales averaged 714 ± 54 g, and juvenile fe-males averaged 932 ± 99 g (Fig. 1).

DISCUSSION

The fasting model proposed by Smith et al.(1986) is based on an assumption of a fat-freebody mass of 600 g for a male Swainson’sHawk, and it assumes that males must gain330 g of fat to fuel their 9000 km southwardmigration. Then, they must regain that same

amount of body fat before their northwardmigration in March (Fig. 2). This model doesnot address females; therefore, we assumed alean body mass of 800 g for a female Swainson’sHawk and assumed that they also would needto deposit at least 330 g of body fat prior totheir southward and northward migrations(Fig. 3). Comparison of our body massmeasurements with those of the modelshowed that, while both sexes and age classesunderwent large losses of body mass duringtheir migration, they did not fluctuate as muchas the fasting model predicted. Both adultmale and female Swainson’s Hawks arrivedon their breeding grounds with massesgreater than those predicted. Nevertheless,prior to their departure on their southwardmigration, their body masses were nearlyidentical to those predicted by the model.Body mass measurements for adult and juve-nile hawks of both sexes were also similar tothose predicted by the model when the hawkswere midway through their southward mi-gration in Panama. Our measurements foradult and juvenile male Swainson’s Hawksshowed opposite trends for the remainder ofthe migration. Juvenile males lost a smallamount of body mass (average of 37 g),whereas adult males gained body mass (aver-age of 29 g) between Panama and Argentina.Both adult and juvenile females continued tolose body mass between Panama and Argen-tina. Nevertheless, upon their arrival in Ar-gentina, both sexes and age classes had bodymasses in excess of those predicted by themodel.

Figure 2. Comparison of annual variations in thebody masses (in g) of adult (open squares) and ju-venile (filled squares) male Swainson’s Hawks tothose predicted by the fasting migration hypoth-esis model (filled triangles, broken line).

Figure 3. Comparison of annual variations in thebody masses (in g) of adult (open circles) and ju-venile (filled circles) female Swainson’s Hawks tothose predicted by the fasting migration hypoth-esis model (open triangles, broken line).


Our satellite telemetry data showed thatSwainson’s Hawks undergo a migration pat-tern that Berthold (1993) has described as aconcentration migration. It begins on a broadfront at its onset in North America and thenfunnels down to a narrow flight path as thesouthward migration moves through Mexicoto the southern Gulf of Mexico. The flight pathremains narrow throughout Central andSouth America. All of the hawks we trackedspent the austral summer in central Argen-tina and none went to Florida or central Cali-fornia where small numbers of winteringSwainson’s Hawks are regularly reported. Thenorthward migration again fans out with birdsbecoming more widely dispersed as theytraverse Mexico and enter the southernUnited States. Hawks making the southwardmigration departed from their North Ameri-can breeding grounds by early October andcompleted their 13500 km journey in 51 days.For the migration north, hawks departed fromtheir austral grounds by mid-March, migratingmore slowly and completing their 11950 kmmigration in 60 days. The northward migra-tion is shorter because, unlike southward mi-grants which cross to the Pacific Ocean sideof Central America following the coastline,northward migrants remain on the Caribbeanside of Central America shortening their mi-gration. Nevertheless, the hawks took longerto complete the migration primarily due totheir slower rate of travel. In their model forfasting migration, Smith et al. (1986) assumedthat between Las Cruces (New Mexico) andArgentina the length of the migration routewas 9000 km and the migration took 37.5 daysfor completion. Because we tracked migrantsthe entire length of the migration route frombreeding areas to austral grounds in Argen-tina, our estimated length for the total migra-tion route was over 4500 km longer than thelength used by Smith et al. (1986) in theirmodel. Consequently, our estimated time forthe duration of the migration was 13 dayslonger in autumn and 22 days longer inspring, or 35 and 59% longer, respectively,than assumed in the model.

Our body mass measurements showed that,like other migrants, Swainson’s Hawks un-dergo large-scale annual changes in their bodymasses. While little is known about the sizeof fat deposits of diurnal raptors, it is gener-ally assumed that sizeable changes in body

masses at different times of the year representchanges mainly in the amount of stored fat(Gessaman 1979, Newton 1979, Blem 1980).Our results showed that adult male and fe-male Swainson’s Hawks gained in excess of150 g of fat following the breeding season inpreparation for their southward migration.Males departed weighing an average of 872 gand females departed weighing an average of1131 g. Upon their arrival in Argentina in lateNovember and early December, both sexeshad lost nearly all of this fat reserve losing anaverage of 127 and 143 g, respectively. Adultsgained body mass on the austral groundsgaining an average of only approximately 50 gof fat by January and February. Goldstein etal. (1999) found that body masses of Swainson’sHawks increased from approximately 800 g to900 g over this same time period. Surprisingly,male and female Swainson’s Hawks arrivedon their breeding grounds in North Americaweighing 802 and 1087 g, or more than they didwhen they were in Argentina. Fat levels shownby juveniles of both sexes were consistentlylower than those we recorded in adults. Juve-niles of both sexes had sustained greater lossesin body mass than adults when they arrivedin Argentina. Juveniles also departed fromArgentina with less body fat than adults had.

Our test of the fasting migration model in-dicated that the body mass fluctuations thatSwainson’s Hawks experienced prior to andafter migration were not great enough forthem to have made their migration using onlystored fat. Neither adult nor juvenile maleSwainson’s Hawks had body masses as lowas the lean body mass of 600 g that the modelis based upon. Similarly, neither adult nor ju-venile females had body masses as low as the800 g lean body mass that we used as an esti-mate in our comparison. Both sexes arrivedin North America and South America weighingmore that they should have, if they conformedto the fasting model, and they all departedfrom Argentina weighing far less than theyshould have to successfully complete thenorthward migration using only stored fat.Clearly, the fasting model does not predict theactual body masses of this species throughoutthe year. The hawks do not arrive lean enoughnor do they depart fat enough to accomplishtheir migration solely using pre-departure fatstores of sufficient magnitude as predicted bythe fasting migration hypothesis.


There are several possible explanations forthe failure of the fasting model to account forour body mass data. It is possible that themodel is based on incorrect assumptions. Theassumption that lean male Swainson’s Hawksweigh 600 g seems to be too low. The leanestmales we measured were captured in July inthe middle of the breeding season when en-ergy demands would have been extremelyhigh for males. None of the males we capturedhad a body mass of 600 g and only one male,the lightest, weighed 655 g. Most males hadbody masses greater than 700 g, indicatingthat the estimated lean body mass of maleSwainson’s Hawks should be increased toabout 700 g. A second questionable assump-tion of the fasting model is the metabolic costof migration. The model assumes that the costof soaring flight is twice that of basal meta-bolic rate (BMR). Smith et al. (1986) suggestthat the value for the costs of migratory flightused in their model may vary between 1–3times BMR. In order for the model to fit thebody mass fluctuations we observed, a flightmetabolism rate of 1 BMR would need to beassumed as the estimated cost of soaringflight. When we did so, the model conformedto our body mass data much more closely. Thisimplies that migrating Swainson’s Hawkswould need to use far less energy for flightduring their migration than has been previ-ously considered. There are few estimates ofthe cost of soaring flight in large migratoryraptors. The question our data raises is whetherit is possible for soaring raptors to expend nomore energy than they do at rest. Preliminarydata on the heart rates of migrating TurkeyVultures (Cathartes aura) indicate that the heartrate of vultures actually falls below their rest-ing rate (Mandel and Bildstein, unpublisheddata). Like Turkey Vultures, Swainson’sHawks may also experience very little addedenergy costs while soaring. A confoundingissue is that there are no data available con-cerning the amount of time that Swainson’sHawks spend using flapping flight duringmigration. Swainson’s Hawks have been ob-served in Chiapas (Mexico) using flappingflight in the early morning and near roosts inthe evening, and during windy days, particu-larly when there is a head wind (Kirkley, un-published data). While there are no goodestimates of the metabolic costs of flappingflight, if it is used to any extent during the

migration period, this would increase themetabolic costs of migration necessitating anadjustment in the model’s estimated cost ofmigration. Clearly, the fasting model needs tobe revised extensively in order for it to accu-rately reflect the trends in body mass we ob-served.

One puzzling aspect of our findings for theannual body mass fluctuations of Swainson’sHawks is the fact that these hawks departfrom the austral summer grounds with far lessfat than they should have stored and they ar-rive on their breeding grounds with far morefat than they should have left. One obviouspossibility is that Swainson’s Hawks feed dur-ing their migratory journeys. Our satellite dataindicate that Swainson’s Hawks remain inspecific locations along the migration route foras long as one week (unpublished data). Forexample, some hawks remain in Texas for10 days and some linger in Colombia fornearly one week. Flocks of Swainson’s Hawkshave been observed feeding on crickets andgrasshoppers in Texas (Littlefield 1973) andCosta Rica (Slud 1964). Our telemetry datasuggest that, during migration, flocks ofhawks may settle into strategic stopoverplaces along the route where they feed andregain fat stores. Their stopover in Texasappears to be important because it allowsthem to gain fat fuel to power their migrationthrough the Mesoamerican land corridor. Itmay be speculated that they settle again inCentral America or northern South Americawhere they regain fat stores to fuel theremainder of the migration to Argentina. Or,perhaps, they simply feed continually whileon migration. Swainson’s Hawks become in-sectivorous during the migration season. Theycan potentially feed in flight on airborne in-sects such as dragonflies, grasshoppers, andcrickets that collect in columns of rising aircalled thermals. We have observed flyingSwainson’s Hawks catching and eating whatappear to be insects while migrating throughColombia (unpublished data). The implicationis that Swainson’s Hawks feed while soaringby eating insects that are in the same thermalsthey use while migrating.

While our findings argue convincingly thatthe fasting migration hypothesis for Swain-son’s Hawks is not correct, there is a need formore data to fully explain how this speciessuccessfully completes its long-distance mi-


gration each year between North and SouthAmerica. Further studies are needed whichdocument the body masses of migratingSwainson’s Hawks midway through theirmigration. Capture of migrants in Costa Rica,Panama, and Colombia would better docu-ment our estimates of the body masses andfat stores of these birds when they are half-way through their migration. Observations offlocks at roost sites in Central America are alsoneeded. Further documentation of opportu-nistic feeding and the occurrence of pelletsand faeces at roost sites will enable us toascertain if these birds do, in fact, utilize astopover strategy to feed and maintain fatstores along the migratory route.

ACKNOWLEDGEMENTS

Major financial support and other assistance hasbeen provided by the US Department of Interior,Department of Defense, Department of Agriculture,Boise State University, the University of Minnesota,the Canadian Wildlife Service, the ArgentineInstituto Nacional de Tecnología Agropecuaria(INTA), and the states of Oregon, Arizona, andIdaho. The American Bird Conservancy, NationalFish and Wildlife Foundation, and Novartis, Inchave also provided support. Swainson’s Hawkswere captured by J. McKinley, M. Martel, G.Holroyd, U. Banasch, D. Matiatos, and others.

LITERATURE CITED

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BERGER M AND HART JS (1974) Physiology and ener-getics of flight. Pp. 416–477 in: FARNER DS, KING JRAND PARKES KC (eds) Avian biology. Volume 4. Aca-demic Press, New York

BERTHOLD P (1975) Migration: control and metabolicphysiology. Pp. 77–128 in: FARNER DS AND KING JR(eds) Avian biology. Volume 5. Academic Press, New York

BERTHOLD P (1993) Bird migration: a general survey.Oxford University Press, Oxford

BLEM C (1980) The energetics of migration. Pp.175–224 in: GAUTHREAUX SA (ed) Animal migration,orientation, and navigation. Academic Press, New York

BROWN LH AND AMADON D (1968) Eagles, hawks, andfalcons of the world. McGraw-Hill, New York

BURGOYNE L, KIJAS J, HALLSWORTH P AND TURNER J(1994) Safe collection, storage, and analysis of DNAfrom blood. Pp. 36–54 in: Proceedings of the Fifth In-ternational Symposium on Human Identification.Promega Corporation, Scottsdale

ENGLAND AS, BECHARD MJ AND HOUSTON CS (1997)Swainson’s Hawk (Buteo swainsoni). Pp. 1–28 in:POOLE A AND GILL F (eds) The birds of North America.Academy of Natural Sciences and American Orni-thologists’ Union, Philadelphia and Washington DC

FULLER MR, SEEGAR WS AND SCHUECK LS (1998) Routesand travel rates of migrating Peregrine Falcons Falcoperegrinus and Swainson’s Hawks Buteo swainsoniin the western hemisphere. Journal of Avian Biology29:433–440

GESSAMAN JA (1979) Premigratory fat in the Ameri-can Kestrel. Wilson Bulletin 91:625–626

GLUTZ VON BLOTZHEIM UN, BAUER KM AND BEZZEL E(1971) Handbuch der vögelmitteleuropas. Volume 4.Falconiformes. Akademische Verlagsgesellschaft,Frankfurt

GOLDSTEIN MJ, BLOOM PH, SARASOLA JH AND LACHER

TE (1999) Post-migration weight gain of Swainson’sHawks in Argentina. Wilson Bulletin 111:428–432

GRIFFITHS R, DOUBLE MC, ORR K AND DAWSON RJG(1998) A DNA test to sex most birds. Molecular Ecol-ogy 7:1071–1075

JENNI L AND JENNI-EIERMANN S (1998) Fuel supply andmetabolic constraints in migrating birds. Journal ofAvian Biology 29:521–528

JOHNSON CG, NICKERSON LA AND BECHARD MJ (1987)Grasshopper consumption and summer flocks ofnon-breeding Swainson’s Hawks. Condor89:676–678

KIRKLEY JS (1991) Do migrant Swainson’s Hawks fasten route to Argentina? Journal of Raptor Research25:82–86

LITTLEFIELD CD (1973) Swainson’s Hawks preying onfall army worms. Southwestern Naturalist 17:433

MCWILLIAMS SR, GUGLIELMO C, PIERCE B AND KLAASSEN

M (2004) Flying, fasting, and feeding in birds duringmigration: a nutritional and physiological ecologyperspective. Journal of Avian Biology 35:377–393

MOORE FR AND KERLINGER P (1987) Stopover and fatdeposition by North American Wood Warblers(Parulinae) following spring over the Gulf of Mexico.Oecologia 74:47–54

NEWTON I (1979) Population ecology of raptors. ButeoBooks, Vermillion

RAMENOFSKY M (1990) Fat storage and fat metabolismin relation to migration. Pp. 215–231 in: GWINNER E(ed) Bird migration. Springer-Verlag, Berlin

SLUD P (1964) The birds of Costa Rica. Bulletin of theAmerican Museum of Natural History 128:1–430

SMITH NG, GOLDSTEIN DL AND BARTHOLOMEW GA(1986) Is long-distance migration possible for soaringhawks using only stored fat? Auk 103:607–611

WEIS-FOGH T (1952) Fat combustion and metabolicrate of flying locusts (Schistocerca gregaria Forshal).Philosophical Transactions of the Royal Society of London,B 237:1–36

2006 USO DE ISÓTOPOS ESTABLES EN ESTUDIOS DE AVES MIGRATORIAS 73

USO DE ISÓTOPOS ESTABLES PARA DETERMINARCONECTIVIDAD MIGRATORIA EN AVES:

ALCANCES Y LIMITACIONES

JULIÁN TORRES DOWDALL 1, ADRIAN FARMER 2 Y ENRIQUE H. BUCHER 3

1 Programa de Maestría en Manejo de Vida Silvestre, Universidad Nacional de Córdoba. CC 122, 5000 Córdoba,Córdoba, Argentina. Dirección actual: Department of Biology, Colorado State University. Fort Collins, EEUU.

[email protected] US Geological Survey, Fort Collins Science Center. 2150 Centre Avenue, Building C, Fort Collins, CO 80526-8118, EEUU.

3 Centro de Zoología Aplicada, Universidad de Córdoba. CC 122, 5000 Córdoba, Córdoba, Argentina.

RESUMEN.— La necesidad de determinar la conectividad migratoria en diversas especies de avesha generado el surgimiento de numerosas técnicas de marcado para determinar el origen geo-gráfico de individuos. El uso de la composición de isótopos estables en tejidos animales es una delas técnicas que más se desarrollaron en los últimos tiempos. Su uso se basa, primero, en que losvalores isotópicos de diferentes elementos químicos varían espacialmente debido a procesos na-turales y de origen humano. Segundo, en que un individuo, al alimentarse, asimila y eventual-mente refleja en sus tejidos la composición isotópica del sitio donde se está alimentando. El tejidomás utilizado en este tipo de análisis es el de las plumas remeras, ya que, al crecer, asimilan lacomposición isotópica del alimento, y luego permanecen metabolicamente inactivas hasta el próxi-mo evento de muda. Aunque esta técnica ha sido exitosamente aplicada en distintas especies deaves, la variabilidad observada entre individuos limita de cierta forma su precisión. Esta variabi-lidad puede ser producto de diferentes procesos que afectan el cambio isotópico entre la dieta ylos tejidos de la especie de interés, de desplazamientos durante el periodo de muda o de varia-ciones en la línea de base isotópica (cambios en los valores isotópicos de hidrógeno en las precipi-taciones). Conocer y entender las fuentes de error puede ayudar a diseñar mejores estudios queminimicen la variabilidad y a desarrollar mejores modelos predictivos para determinar el origengeográfico de un individuo.PALABRAS CLAVE: aves migratorias, deuterio, marcadores naturales, variabilidad isotópica.

ABSTRACT. USING STABLE ISOTOPES TO DETERMINE MIGRATORY CONNECTIVITY IN BIRDS: EXTENT AND LIMI-TATIONS.— The need to unravel migratory connectivity in different bird species has generatedthe development of several techniques to determine the geographical origin of individuals. Usingthe stable isotopes composition of animal tissues is one of the emerging techniques that had thegreatest development. The principles of the technique are, first, that there is a geographical pat-tern in stable isotopes values, as a result of natural and anthropogenic processes, and, second,that stable isotopes are assimilated when an organism eats, and eventually they become fixed inanimal tissues, in proportions related to the natural abundance in the environment. The mostcommonly used tissue is from flight feathers, since they incorporate the stable isotope composi-tion of the food and, once moult is finished, they stay metabolically inactive until they are replaced.Although this technique has been applied with success in several species, variability found withinbirds from the same origin limits its potential accuracy. This variability could be the result ofdifferent processes affecting the isotopic change between food and tissues of the target species,winter movements, or baseline changes through time (temporal changes in the hydrogen isoto-pic values in precipitation). A better understanding of the sources of error would help to designbetter studies in order to minimize variability and to develop better models to determine thegeographic origin of individual birds.KEY WORDS: deuterium, isotopic variability, migratory birds, natural markers.

Recibido 10 marzo 2006, aceptado 2 diciembre 2006

Hornero 21(2):73–84, 2006

La complejidad del ciclo de vida de las avesmigratorias hace evidente la necesidad de de-terminar la conectividad migratoria de estas

especies (Webster et al. 2001). Los parámetrospoblacionales de distintas especies migratoriasestán relacionados con la conexión entre los

74 TORRES DOWDALL ET AL. Hornero 21(2)

sitios reproductivos y no reproductivos(Myers et al. 1987, Marra et al. 1998, Sillett etal. 2000, Webster et al. 2001, Webster y Marra2005). Sin embargo, determinar esta conexiónno ha resultado fácil y la principal causa esnuestra limitada habilidad para seguir a losindividuos a través de su ciclo migratorioanual (Webster y Marra 2005). Gran parte dela información obtenida hasta el momento sedebe al uso de marcadores externos, comoanillos numerados o de colores (Webster et al.2001). Estos, en general, han sido exitosos parael estudio de especies cuyos individuos sonfáciles de volver a observar o capturar (e.g.,especies de interés cinegético, especies de dis-tribución limitada). Sin embargo, no resultanútiles cuando la observación de individuosanillados es característicamente baja, aúncuando se realice un gran esfuerzo de marca-do (Bairlein 2001, Webster et al. 2001). Esteproblema se observa comúnmente en espe-cies de tamaño corporal pequeño o mediano,con distribución amplia o comportamiento es-quivo, por lo que volver a observarlas es difí-cil. El uso de isótopos estables surge como unatécnica alternativa para el estudio de la conec-tividad migratoria en aves (Hobson 1999,2005a, Webster et al. 2001), intentando salvarel problema de recapturar o volver a observarindividuos. Esta técnica utiliza la informaciónquímica de los tejidos de individuos captura-dos para determinar su origen geográfico. Latécnica presenta un gran potencial ya que norequiere el marcado de individuos, sino ladeterminación de parámetros poblacionales(e.g., los valores isotópicos promedio de lapoblación), permitiendo pasar del uso demarcadores artificiales (i.e., anillos) al de mar-cadores naturales (i.e., isótopos estables).

Se pueden señalar tres motivos por los cualeslos isótopos estables son buenos para deter-minar conectividad migratoria. En primerlugar, se encuentran naturalmente en el am-biente y su abundancia varía geográficamentedebido a distintos procesos, tanto naturalescomo de origen humano (Rubenstein yHobson 2004). El segundo motivo es quecuando un animal consume alimentos o aguaasimila isótopos estables en las proporcionesen las que estos están presentes en el ambien-te, y esto se refleja en los tejidos (Fig. 1). Deesta forma, todos los individuos de una espe-cie que comparten un ambiente con caracte-rísticas isotópicas comunes presentarán en sus

tejidos una composición isotópica similar, lla-mada “firma isotópica del ambiente”. En ter-cer lugar, debido a que todas las aves de unsitio comparten la misma firma isotópica, noes necesario recapturar al mismo individuopara poder inferir sobre su lugar de origen,sino que todos los individuos están natural-mente marcados. Es necesario aclarar que, enciertos casos específicos, la firma isotópicapuede variar entre individuos de una mismaespecie que utilizan un área común, depen-diendo de la edad o el sexo (Lott et al. 2003).

Esta técnica, sin embargo, presenta algunosproblemas y limitaciones. Para usar isótoposestables se debe conocer la firma isotópica delos distintos sitios de origen de la especie enestudio. Existe información a partir de la cualinferir el patrón de variación espacial para al-gunos isótopos a escala mundial (IAEA 2001,Bowen y Wilkinson 2002, Still et al. 2003), yestos datos son relativamente precisos enAmérica del Norte (Hobson y Wassenaar 1997)y Europa (Hobson 2002). Pero esta informa-ción es limitada para América del Sur (Bowenet al. 2005). Además, algunos autores han en-contrado una gran variabilidad en la compo-sición isotópica de los tejidos de individuosdel mismo origen (Farmer et al. 2004, Wunderet al. 2005). Estos factores, y en particular elúltimo, reducen la posibilidad de aplicar conéxito esta técnica o la precisión al asignarmuestras a los sitios de origen, dependiendode la pregunta y la especie de interés. Por lotanto, afirmar que esta técnica sirve o no esincorrecto (Hobson 2005a).

En este trabajo intentamos introducir al lec-tor en el uso de isótopos estables, sus benefi-cios y complicaciones. Dado que este campode la biología crece diariamente y constante-mente se presentan revisiones de la técnica ynuevos trabajos, no pretendemos realizar unanueva revisión detallada, sino más bien unaintroducción a la técnica. Este trabajo estáorganizado en seis secciones. En primer lugar,presentamos las notaciones y terminologíasusadas en estudios de isótopos estables. Luegoresumimos brevemente el uso de isótoposestables en estudios ecológicos y, principal-mente, en estudios de conectividad migrato-ria. A continuación resumimos los principalespatrones de variación espacial de isótoposestables. En cuarto lugar presentamos infor-mación sobre las tasas de recambio de isótoposestables en distintos tejidos y las consecuen-


cias de la elección de un tejido en particular.En la siguiente sección discutimos los supues-tos del uso de isótopos estables y, finalmente,el problema de la variación en la composiciónisotópica entre individuos de un mismo origen.

ISÓTOPOS ESTABLES: NOTACIÓN YFRACCIONAMIENTO

Los isótopos estables son medidos en unarelación entre la abundancia del isótopo esta-ble raro, más pesado, y la del isótopo establecomún, más liviano. Los isótopos estables quegeneralmente se utilizan en estudios deconectividad migratoria y otros estudios eco-lógicos son los de hidrógeno o deuterio (2H/1Ho D/1H), carbono (13C/12C), nitrógeno (15N/13N),oxígeno (18O/16O) y azufre (34S/32S). Estoscocientes son a su vez comparados con la re-lación de estos isótopos en un estándar inter-nacional, presentándose finalmente un valoren notación delta (δ),

δX = [(Rmuestra

/ Restandar

) - 1] * 1000,

donde X es el isótopo de interés y R es la pro-porción de átomos del isótopo pesado en rela-ción al isótopo liviano. De esta forma, valoresde δX positivos implican que la muestra estáenriquecida en el isótopo más pesado en rela-ción con el estándar y valores negativos im-plican que está empobrecida. Esta notación

permite comparar resultados de análisis reali-zados en distintos momentos y laboratorios.No obstante, esto no es posible para el deute-rio, ya que los tejidos presentan un porcenta-je de hidrogeno que puede ser intercambiadocon la humedad ambiental (Wassenaar yHobson 2003). Variaciones en la humedadambiental entre estaciones del año y entre dis-tintos laboratorios impiden realizar compara-ciones (Hobson 2005a).

Cuando un organismo consume recursos delambiente, los isótopos estables son asimiladosen sus tejidos de acuerdo a la proporción enque se hallan en estos recursos, aunque concierta diferencia debida a distintos procesosmetabólicos. Esta diferencia se conoce comofraccionamiento isotópico y se expresa en lasiguiente ecuación:

δXt= δX

d+ δ∆

dt,

donde t es el tejido de interés, d la dieta y ∆dt

el fraccionamiento entre la dieta y el tejido(Hobson 2005a). Este valor de fraccionamien-to puede variar entre especies, tejidos (Hobsony Clark 1992) y en distintas condiciones am-bientales (Hobson et al. 1993). Sin embargo,debido a que el valor final de un isótopo esta-ble es la suma de numerosos eventos de con-sumo de alimento (Hobson 1999), puededeterminarse un valor promedio de fracciona-miento. Por ejemplo, hay un patrón constante

įD

įDplumas = 0.9 * įDprecipitación - 31

įD

¿?

Figura 1. Esquema del camino de los isótopos estables desde procesos productores de variación espacialhasta las plumas de las aves, ejemplificado con el deuterio. En especies terrestres la cadena más simpleincluye cuatro eslabones (A), mientras que para especies acuáticas comprende cinco eslabones (B). Cadauno de los pasos produce un fraccionamiento entre el valor inicial y el valor final (flechas sólidas). En lafigura se utiliza como ejemplo del valor del fraccionamiento entre precipitaciones y plumas (flechasvacías) a la función para passeriformes de América del Norte (Hobson y Wassenaar 1997, Wassenaar yHobson 2000). No es claro si puede desarrollarse una función para las aves acuáticas.

A B


entre el valor de deuterio en las precipitacio-nes de una determinada localidad y el exis-tente en las plumas de pájaros capturados enesa localidad (Hobson y Wassenaar 1997); paraAmérica del Norte este valor promedio ha sidoestimado entre -5‰ y -25‰ (Wassenaar yHobson 2000, Lott y Smith 2006). Igualmente,se ha determinado que el valor de fracciona-miento de δ15N es de aproximadamente 2‰,lo que resulta de gran utilidad en estudios dedieta y de cadenas tróficas (DeNiro y Epstein1981, Hobson 1999).

PATRONES NATURALES DE VARIACIÓN

ESPACIAL

Los isótopos estables son buenos marcadoresnaturales ya que presentan patrones natura-les de variación espacial (Webster et al. 2001,Rubenstein y Hobson 2004). Debido a estavariación podemos distinguir entre muestrasde diferentes orígenes geográficos. Por ejem-plo, Farmer et al. (2004) encontraron quechorlos provenientes de localidades relativa-mente cercanas, como Río Grande en Tierradel Fuego, Laguna Nimez en Santa Cruz yBahía Lomas en Chile, presentan en sus plu-mas valores isotópicos de C, N y S claramentediferentes. Basados en estas diferencias,Atkinson et al. (2005) calcularon que de losindividuos de Playero Rojizo (Calidris canutus)que paran en la Bahía Delaware en su migra-ción a los sitios reproductivos, el 58% presentavalores isotópicos similares a los de BahíaLomas, mientras que solo el 6% presenta va-lores isotópicos similares a los de Río Grande.

El deuterio y el oxígeno presentan el patrónde variación que ha resultado más útil paraestudios de conectividad migratoria (Hobson2005b). Este patrón fue determinado a partirde los valores isotópicos en las precipitaciones,basándose en información de la AsociaciónInternacional de Energía Atómica, de suprograma Cadena Global de Isótopos en Preci-pitación (IAEA 2001). Existe un claro empobre-cimiento en deuterio y 18O desde los trópicosa los polos y con la altitud (Daansgard 1964,Poage y Chamberlain 2001, Bowen y Wilkin-son 2002). Mapas de la variación espacial delos valores de δD y δ18O en las precipitacioneshan sido desarrollados para prácticamentetodos los continentes, incluyendo América delSur (Bowen et al. 2005). Meehan et al. (2004)han desarrollado un mapa alternativo para los

valores de δD en las precipitaciones conside-rando los efectos de la altitud. Estos mapasson de clara utilidad para el estudio de migra-ción, principalmente en América del Norte yEuropa donde se ha demostrado que los valo-res de δD en las precipitaciones y en las plu-mas están relacionados (Hobson y Wassenaar1997, Meehan et al. 2004, Hobson 2005b).

El carbono muestra diferencias geográficasimportantes a escala mundial producto de ladistribución de plantas C3 y C4. De acuerdo asu proceso fotosintético, las plantas fijan dis-tintas cantidades de 13C, produciendo valoresfácilmente distinguibles: las plantas C3 pro-ducen tejidos empobrecidos en 13C con rela-ción a plantas C4 o CAM (Guy et al. 1993,Lajtha y Marshall 1994). Adicionalmente, exis-ten variaciones en los valores de 13C debido acaracterísticas ambientales asociadas a la can-tidad de agua disponible (Lajtha y Marshall1994). Así, en ambientes más secos las plantasproducen tejidos enriquecidos en 13C compa-rado con los valores isotópicos en ambientesmás húmedos (Rubenstein y Hobson 2004).Por ahora no existen mapas de variación espa-cial de los valores de δ13C; sin embargo, haymapas disponibles que presentan las propor-ciones entre plantas C3 y C4 (Still et al. 2003),permitiendo determinar regiones potencial-mente diferentes con relación a los valores deδ13C (Hobson 2005a). Estos patrones geográ-ficos presentan relativamente poca estabilidaddebido a la producción agrícola, que reem-plaza la vegetación natural (Wassenaar yHobson 2000).

El 15N presenta un patrón de variación menosclaro, determinado principalmente por lahumedad de los ambientes. Los ambientesmás secos presentan valores más altos de δ15Nque los más húmedos (Handly et al. 1999,Rubenstein y Hobson 2004). Los valores deδ15N en el ambiente están notablemente modi-ficados por el uso de fertilizantes nitrogenadosen la agricultura y por su transporte en loscursos de agua. Por ejemplo, patos residentesen humedales afectados por procesos agríco-las presentan valores de δ15N en sus plumasmás altos que los patos de ambientes natura-les (Hebert y Wassenaar 2001).

Los valores de δ34S presentan principalmentediferencias entre ambientes marinos y terres-tres (Rubenstein y Hobson 2004). En general,los ambientes terrestres con influencia marinaestán enriquecidos en 34S comparado a los


ambientes sin influencia marina. Lott et al.(2003), analizando plumas, utilizaron las dife-rencias en los valores de δ34S entre ambientesmarinos y terrestres para diferenciar rapacesque se alimentan sobre la base de una cadenatrófica con origen marino, de aquellos que sealimentan principalmente de una cadenatrófica terrestre.

Otro elemento cuyos isótopos estables pue-den ser de utilidad para estudios de conec-tividad migratoria es el estroncio. Este varíaespacialmente correlacionado con caracterís-ticas geológicas. Suelos más nuevos estánempobrecidos en 87Sr comparados con suelosviejos (Rubenstein y Hobson 2004). El 87Sr esusado comúnmente en estudios de migraciónen peces (Thorrold et al. 2001, Elsdon yGillanders 2003).

TEJIDOS Y TASAS METABÓLICAS

Uno de los factores más importantes para eléxito de un estudio de conectividad migratoriaen el que se usan isótopos estables es la elec-ción del tejido a utilizar. Distintos tejidos pre-sentan diferentes tasas metabólicas, por lo quereflejan los valores isotópicos del alimentoingerido en distintos lapsos temporales(Hobson 2005a). El hígado y el plasma san-guíneo tienen una tasa de recambio muy alta,reflejando la composición isotópica del ali-mento ingerido en los últimos días, mientrasque las células sanguíneas o los músculos pre-sentan una tasa de recambio más lenta yreflejan los valores isotópicos de los alimen-tos ingeridos en los últimos meses.

El tejido más usado para determinar laconectividad migratoria en aves son las plu-mas. La ventaja de éstas es que son metabóli-camente inactivas una vez que terminó sucrecimiento, conservando la firma isotópicade la localidad donde crecieron hasta elsiguiente evento de muda. Esto supone quelas aves no utilizan reservas endógenas parala formación de las plumas (Murphy 1996), locual está respaldado por estudios de labora-torio en los que se observó que cambios en ladieta producen cambios consecuentes en losvalores isotópicos de las plumas (Bearhop etal. 2002). Una desventaja es el desconoci-miento de los ciclos de muda de muchas espe-cies migratorias (Hobson 2005a). Conocer elárea donde la especie en estudio muda es fun-damental, ya que áreas distantes como Amé-

rica del Sur y del Norte presentan valores si-milares en algunos isótopos. Sin embargo, eluso de plumas presenta la ventaja de ser unmétodo no destructivo de muestreo y, alpermanecer metabólicamente inactivo, permi-tiría usar ejemplares de museo para determi-nar valores isotópicos en distintas localidades(Lott et al. 2003).

Otro tejido comúnmente utilizado paradeterminar movimientos migratorios es elsanguíneo. Los tejidos metabólicamente acti-vos brindan información sobre un periodo detiempo anterior al evento de muestreo quedepende de la tasa de recambio isotópico deltejido. La tasa de recambio de la sangre ha sidodeterminada para distintas especies en condi-ciones de laboratorio (Hobson y Clark 1992,Bearhop et al. 2002, Hobson y Bairlein 2003,Evans-Oegen et al. 2004). Pero las condicio-nes de laboratorio raramente simulan las queenfrentan los individuos durante las migra-ciones (Bearhop et al. 2002, Hobson 2005b).No obstante, ciertos estudios de laboratoriosugieren que la tasa de recambio isotópico dela sangre podría no estar afectada por la acti-vidad física (Hobson 2005a). Individuos deGorrión (Passer domesticus) mantenidos a 5 °Cpresentan diferencias en la tasa metabólica conaquellos mantenidos a 22 °C, pero esto no serefleja en la tasa de recambio isotópico de 13Cy 15N (Carleton y Martinez del Rio 2005). Estosugiere que los estudios de laboratorio quedeterminaron la tasa de recambio isotópico ensangre podrían ser utilizados para animalessilvestres.

EL USO DE ISÓTOPOS ESTABLES EN

ECOLOGÍA Y CONECTIVIDAD MIGRATORIA

Los isótopos estables han sido usadosampliamente como marcadores naturales endiversos estudios ecológicos y su uso seincrementó a partir de la década de 1970. Suutilidad radica en que el agua o los nutrientesde distintos orígenes presentan diferentesvalores isotópicos y, al ser asimilados por plan-tas o animales, mantienen estas diferencias.Por ejemplo, el agua subterránea y la de lasprecipitaciones en general difieren en los valo-res de deuterio, por lo que es posible deter-minar, analizando la composición isotópica dela savia de una planta, si está consumiendoagua de lluvia o subterránea (White 1989). Así,es potencialmente posible analizar los isótopos


estables en los tejidos de un individuo y ras-trear su origen a través de la cadena trófica.El lector interesado en otras aplicaciones deisótopos estables en estudios ecológicos pue-de consultar los trabajos de Rundel et al. (1989)y Lajtha y Michener (1994).

La utilización de los isótopos en estudios demigración tiene su origen en los trabajos deHobson y Wassenaar (1997), Marra et al. (1998)y Chamberlain et al. (1997), a fines de la déca-da de 1990, y recientemente el número depublicaciones sobre el tema se ha incremen-tado exponencialmente (Hobson 2005a). Sinembargo, la idea de utilizar marcadores quími-cos para el estudio de movimientos estacio-nales en aves se remonta a los trabajos deKelsall, quien utilizó la composición químicade las plumas como marcadores (Kelsall 1970,Kelsall y Calapric 1972, Kelsall y Burton 1977).

El principio del uso de isótopos estables paradeterminar conectividad migratoria es simple.Al ingerir alimentos, un individuo está asi-milando las características isotópicas del am-biente donde se está alimentando, las cualesse verán reflejada en sus tejidos. Como la com-posición isotópica del ambiente varía espacial-mente, cuando un individuo se desplaza deuna localidad A a una nueva localidad B, lacual difiere isotópicamente de la primera, sustejidos reflejarán la composición isotópica deA (i.e., su localidad de origen) por un periodode tiempo que depende de la tasa metabólicadel tejido analizado. Así, al capturar a esteindividuo en B podemos inferir si es residenteen B o proviene de otra localidad, en este casoA, en base a los valores isotópicos en sustejidos.

Numerosos trabajos han tenido éxito al rela-cionar hábitats o localidades reproductivas yde invernada en distintas especies. Por ejem-plo, Marra et al. (1998), analizando los valo-res isotópicos del carbono en sangre ymúsculo pectoral, relacionaron la fecha dearribo a los sitios reproductivos con la calidaddel hábitat de los sitios invernales de Setophagaruticilla. Los primeros individuos en arribarpresentaron valores isotópicos de carbonorelacionados a bosques húmedos, considera-dos de mejor calidad para la especie, mien-tras que los últimos en arribar mostraronvalores asociados a arbustales secundarios,que representan un hábitat pobre. Rubensteinet al. (2002) determinaron la conectividad

migratoria de Dendroica caerulescens, la cual sereproduce en el este de América del Norte ymigra en invierno a las islas del Caribe. Utili-zando isótopos de hidrógeno y carbono enplumas, estos autores demostraron que laspoblaciones que nidifican en el norte de suárea de distribución pasan el invierno en lasislas del oeste, mientras las que se reproducenen el sur migran a las islas del este del Caribe.

SUPUESTOS EN EL USO DE ISÓTOPOS

ESTABLES PARA DETERMINAR

CONECTIVIDAD MIGRATORIA

La técnica requiere primero determinar lafirma isotópica de las localidades donde eltejido de interés permanece metabólicamenteactivo (i.e., crece y asimila isótopos estables),para luego poder relacionar con esta locali-dad a un individuo capturado en otra sobrela base de su composición isotópica. Existendos aproximaciones a este problema. Una esdeterminando la firma isotópica de la locali-dad de interés de forma directa, midiendo encada sitio los valores isotópicos en plumas dela especie de interés. La segunda, propuestapor Hobson y Wassenaar (1997), es inferir lafirma isotópica a partir de mapas de variaciónespacial de los isótopos estables, como porejemplo los mapas de variación del deuterioy 18O en las precipitaciones (Bowen et al. 2005).Ambos métodos presentan problemas y ven-tajas en su aplicación, y la elección de uno uotro depende de la especie en estudio y de suárea de distribución.

Indudablemente, medir la firma isotópica enplumas en los sitios donde el tejido estámetabólicamente activo es el método más pre-ciso para determinar el origen de especiesmigratorias. Sin embargo, como raramente esposible hacer un muestreo de toda el área dedistribución de una especie, se infieren porintrapolación los valores isotópicos esperadosen los sitios no muestreados usando una re-gresión inversa (Kelly et al. 2002, Rubensteinet al. 2002, Torres Dowdall 2005, Wunder etal. 2005). En general, este método ha produci-do resultados poco precisos (Wunder et al.2005). Por eso, hasta el momento, considerarel espacio como discreto parece ser la mejoraproximación a la técnica (Royle y Rubenstein2004). Mas aún, Royle y Rubestein (2004) yWunder et al. (2005) mostraron que el uso demétodos estadísticos bayesianos y de proba-


bilidades condicionadas, basados en informa-ción previa de las abundancias relativas de losindividuos en cada sitio y el conocimiento delos valores isotópicos esperados, mejora lacalidad predictiva de la técnica.

La segunda posibilidad consiste en inferir losvalores isotópicos de los sitios de interés apartir del uso de mapas de variabilidadisotópicas (ver Patrones naturales de variaciónespacial). Esta aproximación es propuesta porHobson y Wassenaar (1997) a partir de la de-terminación de una relación constante entrelos valores de δD en las precipitaciones y enlas plumas de distintas especies de paseri-formes (Hobson y Wassenaar 1997, Wassenaary Hobson 2000). Básicamente, consiste en de-terminar el valor de δD en las plumas de unindividuo de origen no conocido, utilizar unafunción para relacionar el valor de deuterioen las plumas con el valor en las precipitacio-nes (e.g., δDplumas = 0.9 * δDprecipitaciones - 31;Hobson y Wassenaar 1997) y asignar al indi-viduo muestreado a la región donde la espe-cie muda que presente este valor de δD en lasprecipitaciones. Esto podría describirse comoel uso de un “atajo”, ya que no se conocen losvalores de deuterio en las plumas en los sitiosde muda, sino que se los infiere a partir de losvalores promedios de deuterio en las precipi-taciones (Fig. 1).

Para el deuterio, la relación entre los valoresde δDprecipitaciones y δDplumas fue demostrada enalgunas especies de paseriformes en Américadel Norte (Hobson y Wassenaar 1997,Wassenaar y Hobson 2000) y Europa (Hobsonet al. 2004b, Bowen et al. 2005), y en aves ra-paces (Lott y Smith 2006). Sin embargo, estees un valor promedio; por lo tanto, el fraccio-namiento en individuos puede alejarse más omenos de lo esperado. Además, las diferen-cias en las funciones entre los paseriformesen América del Norte y en Europa (Bowen etal. 2005) y entre éstas y la función para rapaces(Lott y Smith 2006) sugieren que quizás no searecomendable aplicarlas a otros grupos deaves o en otros continentes. Sin embargo,hasta desarrollar funciones que relacionen losvalores de deuterio en plumas y precipi-taciones, las funciones ya desarrolladas pue-den ser usadas si se consideran ciertaslimitaciones. Por ejemplo, este valor no esconstante para rapaces en distintas localida-des de América del Norte (Lott y Smith 2006).Además, es posible que este valor no sea apli-

cable a especies cuya dieta tiene una base deorganismos acuáticos (Hobson 2005a), ya queel deuterio sigue un camino diferente depen-diendo si la especie de interés es terrestre oacuática (Fig. 1). En aves acuáticas, el caminodel deuterio hasta el individuo es más largo,ya que cuenta con la acumulación de agua enlos humedales. Esta es una diferencia impor-tante, ya que la entrada (e.g., precipitaciones,aportes fluviales) y salida (e.g., evaporación)van a regular el valor isotópico del humedal(Fig. 1b). A pesar de que se ha encontradocierta relación entre los valores isotópicos enprecipitaciones y en humedales, en general noexiste tal relación para grandes sistemashídricos (Kendall y Coplen 2001). En concor-dancia con esto, análisis de deuterio en plu-mas de chorlos no mostraron relación algunani con el valor de deuterio en las precipitacio-nes ni con el valor en los cuerpos de agua(Torres Dowdall 2005). Mapas de variación delos valores de deuterio en plumas de chorlosen Argentina muestran un patrón diferenteal esperado a partir de mapas de precipita-ciones, con un enriquecimiento en deuterioen el centro del país y valores más bajos alnorte y al sur (datos no publicados).

Un problema importante es que el uso demapas de deuterio en las precipitacionesignora la varianza temporal y espacial en elfraccionamiento del deuterio desde las preci-pitaciones hasta el individuo (Wunder et al.2005). Aunque existen diferencias en el cami-no del deuterio desde las precipitaciones hastalas plumas entre aves acuáticas y terrestres(Fig. 1), en esta discusión se va a considerar lacadena terrestre, ya que es más simple. En unacadena terrestre sencilla, con tres eslabones(i.e., productor, herbívoro, carnívoro; Fig. 1a),se observa que hay cuatro pasos que puedenafectar el valor final de deuterio en las plumasde un individuo. Por lo tanto, el uso de un“atajo” desde el valor de deuterio en las pre-cipitaciones y el valor de deuterio en las plu-mas presenta, al menos, los siguientessupuestos implícitos: (1) no hay variación tem-poral de los valores de δD en las precipitacio-nes, (2) los productores primarios asimilanexclusivamente agua de lluvia, (3) tanto losconsumidores primarios como los secundariospresentan una dieta estable, y (4) no existenfactores que afecten los valores de fracciona-miento isotópico ni en los consumidores pri-marios ni en los secundarios.


Los mapas de variación isotópica presentanun valor promedio de δD en las precipitacio-nes para una determinada región en la épocade crecimiento (i.e., primavera-verano)(Hobson 2005a). Sin embargo, el valor dedeuterio en las precipitaciones puede ser alta-mente variable entre años (Farmer et al. 2003),afectando la precisión en las predicciones dellugar de origen de un individuo. Por ejemplo,en Buenos Aires, los valores de δD en las pre-cipitaciones puede variar notablemente entreaños, abarcando gran parte del rango de varia-ción de deuterio en Argentina (Farmer et al.2003). Hobson (2005a) aclara al respecto queno podemos esperar que los valores dedeuterio en plumas en una localidad dadasean iguales a los valores inferidos a partir deldeuterio en las precipitaciones, ya que los va-lores en los mapas isotópicos de deuterio sonun promedio obtenido a partir de cuarentaaños de registro de la Asociación Internacio-nal de Energía Atómica (IAEA 2001). Por lotanto, es probable que, en un año particular,los valores de δD se alejen más o menos deeste promedio. Por esto, debe considerarseeste valor como una guía, pero de ser posiblees recomendable calibrar los datos con plu-mas colectadas en los sitios de interés.

La técnica también supone que los produc-tores primarios asimilan principalmente aguade lluvia. No obstante, el grado con que lasplantas asimilan agua de lluvia depende delgrado en que el agua es disponible de otrasfuentes (White 1989). En sitios áridos, dondeel agua es limitante, el agua asimilada por lasplantas proviene en general de las precipita-ciones, y esto es reflejado en los valoresisotópicos en la savia de las plantas (White1989). A medida que otras fuentes de aguaestán disponibles, los valores de δD en plantasse relacionan pobremente con los valores enlas precipitaciones (White 1989). Esto puedeafectar notablemente el patrón de variaciónespacial del deuterio en plantas, produciendovalores diferentes a aquellos inferidos a partirde las precipitaciones.

Otro supuesto clave es que los herbívorospresentan un valor característico del sitio. Estoes, que se alientan en proporciones que refle-jan la proporción de plantas C3 y C4 en elambiente. Esto es importante, ya que los valo-res de los isótopos estables en plantas, princi-palmente los valores de δD y δ13C, dependendel proceso fotosintético (Ehleringer y Rundel

1989, Ziegel 1989). De esta forma, el valor finalde la proporción en los tejidos de un orga-nismo de interés depende de la proporciónde plantas C3 y C4 de las que se alimenta(Gannes et al. 1997). Esto es igualmente válidopara carnívoros, ya que las especies especia-listas reflejarán el valor isotópico de suspresas, pero las generalistas mostrarán valo-res promedio y una gran variabilidad entreindividuos (Bearhop et al. 2004, Matthews yMazumder 2004). Hobson (2005a) señala quela cantidad de deuterio en un determinadotejido representa numerosos eventos de ali-mentación; por esto, a pesar de la variaciónespacial o temporal, el valor isotópico finalrepresenta un valor promedio.

Al usar un “atajo” entre las precipitaciones ylas plumas para determinar el origen geográ-fico de un individuo usando isótopos estables,el supuesto de que no hay factores que afectenel fraccionamiento (ver más arriba) entre elalimento y los tejidos de un organismo dadoes el más débil. Numerosos trabajos realiza-dos en laboratorio con diferentes especies su-gieren que hay diversos factores que afectanel valor isotópico final en tejidos animales.Experimentos en cuervos demostraron queuna especie puede presentar valores de frac-cionamiento diferentes dependiendo del tipode alimento (Hobson y Clark 1992). Trabajosen perdices sugieren que el fraccionamientotambién es afectado por la cantidad de alimen-to. Individuos con acceso limitado al alimentopresentan valores más altos de δ15N que aque-llos con acceso ilimitado al alimento (Hobsonet al. 1993). Resultados similares se encontra-ron en peces, donde la calidad y la cantidadde alimento suministrado afectaron los valo-res de δ13C y δ15N (Gaye-Siessegger et al. 2003).Por el contrario, la temperatura ambiental noafectó los valores de δ13C y δ15N en un estudiorealizado en gorriones (Passer domesticus)(Carleton y Martinez del Rio 2005).

VARIABILIDAD ISOTÓPICA

Al ser violados los supuestos discutidos enla sección anterior disminuye la precisión conla cual es posible determinar el origen geo-gráfico de una muestra usando isótopos esta-bles, ya que se incrementa la variabilidad dela firma isotópica en los sitios de origen. Estavariabilidad se ve reflejada en distintos traba-jos en diferentes especies. Sin embargo, este


tema ha sido explícitamente tratado en pocostrabajos, principalmente en aves playeras(Farmer et al. 2004, Wunder et al. 2005) y ra-paces (Lott et al. 2003). Sin embargo, la varia-bilidad máxima encontrada en estos trabajosno es mayor a la encontrada en otros trabajosque no consideran el problema explícitamente(Farmer et al. 2003, 2004, Torres Dowdall 2005).Bowen et al. (2005) tratan explícitamente elproblema de la variabilidad incorporando enlos intervalos de confianza de las prediccio-nes de origen distintos factores productoresde variabilidad. Como resultado, la precisiónde la determinación del origen de paseri-formes, tanto en América del Norte comoEuropa, es limitada (e.g., Fig. 9 en Bowen etal. 2005).

Comparando los valores isotópicos de H, C,N, O y S en plumas de chorlos en tres sitiosen el noroeste argentino, Torres Dowdall(2005) encontró diferencias significativas entredos años consecutivos en al menos un isótopoestable en los tres sitios. Wunder et al. (2005),analizando isótopos de H, C y N en plumasde Charadrius montanus encontró gran variabi-lidad entre individuos en un mismo sitio, afec-tando significativamente la calidad predictivade los modelos que desarrollaron. Los valoresde deuterio en plumas de individuos adultosde Catharus bicknelli en un sitio del este deCanadá presentaban un rango de -114.8‰ a-51.6‰ (Hobson et al. 2004a), mientras que elrango esperado de δD en precipitación paraeste sitio en particular es mucho menor (-79‰a -60‰; Meehan et al. 2004). Estos ejemplossugieren que la variabilidad, a pesar de queno sea considerada explícitamente en muchosestudios, es un factor determinante en el usode isótopos estables para determinar conecti-vidad migratoria. Por esto el estudio de lascausas de la variabilidad y el análisis de lossupuestos de la técnica requieren mayoratención.

En primer lugar, es necesario determinar sihay especies que presentan naturalmentemayor variabilidad que otras. Es esperable queespecies con dietas especializadas presentenmenor variabilidad en la firma isotópica queaquellas oportunistas o generalistas. Esto queparece obvio es, sin embargo, de relevanciaen la aplicación de la técnica. Si existen espe-cies naturalmente más variables que otras, estosignifica que el uso de isótopos estables serámás útil en algunas especies que en otras. Por

lo tanto, no se puede afirmar que la técnicasirve o no sirve para estudiar migraciones,sino más bien que la técnica es útil o no parauna especie determinada (Hobson 2005a). Eneste sentido, también es necesario entenderla historia natural de la especie de interés yresulta imprescindible conocer los ciclos demuda. Muchas especies mudan las plumas devuelo en los sitios reproductivos antes de mi-grar, otras lo hacen una vez que han llegado alos sitios de invernada, mientras que otraspresentan patrones intermedios con mudassuspendidas o mudas en sitios de parada du-rante las migraciones. De esta forma, la infor-mación isotópica en las plumas refleja sitiosdiferentes de acuerdo al patrón de muda.

En segundo lugar, un punto importante enespecies que mudan en sitios no reproducti-vos es determinar si realizan movimientosinvernales, es decir, si permanecen toda latemporada no reproductiva en un sitio espe-cifico o realizan desplazamientos entre dife-rentes sitios (Farmer et al. 2004, TorresDowdall 2005). Si un individuo permanece enun mismo sitio toda la temporada se esperaque todas sus plumas de vuelo presenten va-lores isotópicos similares (i.e., baja variabili-dad entre plumas) y que estos valores reflejenla firma isotópica del sitio de muda. Por el con-trario, si un individuo se desplaza durante elperiodo de muda, la variabilidad entre plu-mas será alta y cada pluma reflejará la firmaisotópica de distintos lugares. Entonces noexiste un único sino múltiples sitios de origen,y la determinación dependerá de la pluma quese analice. Análisis de alas completas dechorlos neárticos sugieren que al menos al-gunos individuos se desplazan durante elperiodo de muda (Farmer et al. 2003). Estavariabilidad dificulta la caracterización desitios no reproductivos basada en la firmaisotópica y, por los tanto, reduce la precisiónde la técnica, aunque brinda informaciónsobre los posibles desplazamientos invernales.

Es necesario continuar los experimentos delaboratorio para poner a prueba los supues-tos de la técnica (Gannes et al. 1997). Este esun campo de investigación que está creciendorápidamente y las publicaciones sobre expe-rimentos con isótopos estables son frecuen-tes. Por esto, es de esperar que nuevosestudios ayuden a entender la variabilidad ob-servada en algunas especies (Farmer et al.2004, Torres Dowdall 2005, Wunder et al. 2005).


Entender cuáles factores afectan la firmaisotópica de cada especie, produciendo varia-bilidad entre individuos en un mismo sitio,ayudará a mejorar los modelos predictivos.

CONCLUSIONES

El uso de isótopos estables presenta un granpotencial para responder preguntas deconectividad migratoria que no eran aborda-bles usando técnicas más tradicionales. Indu-dablemente, su aplicación en el estudio deespecies migratorias aportará valiosa informa-ción para mejorar los criterios de conservacióny manejo, y mejorará nuestro conocimientosobre la biología y ecología de estas especies.Sin embargo, el uso de isótopos estables es unatécnica relativamente nueva y, a medida quese realicen nuevos estudios, se podrá deter-minar más claramente sus límites y alcances.Por esto, se presentaron aquí algunos de losproblemas con el uso de isótopos estables paradeterminar conectividad migratoria, en lacreencia que entender los límites y problemasde una técnica ayuda a diseñar mejores estu-dios y a interpretar mejor los datos. Al mismotiempo, conocer previamente estas limitacio-nes puede ayudar a predecir en qué especieso ecosistemas el uso de isótopos estable puedeser más útil y en cuáles puede ser más limita-do. Las especies especialistas presentan máspotencial que las generalistas para el uso deisótopos estables. Igualmente, especies queutilizan diferentes ambientes van a presentarmayor diferenciación en los valores isotópicosy por ende mayor posibilidad de éxito en elestudio de migraciones. Finalmente, la elec-ción del tejido a ser analizado va a dependerprincipalmente de la pregunta del investiga-dor. Para estudiar conectividad migratoria enaves, las plumas parecen ser la mejor aproxi-mación. Para desplazamientos de corta distan-cia, la sangre puede ser más conveniente.

AGRADECIMIENTOS

Queremos agradecer a Víctor Cueto por la invi-tación a participar en el Simposio de Aves Migrato-rias en la Reunión Argentina de Ornitología 2005.Agradecemos especialmente a Maria Ruiz Garcíapor la ilustración para la figura 1. A Gisela Bazzanoy dos revisores anónimos por los comentarios sobreel manuscrito que ayudaron a mejorarlo. J. TorresDowdall agradece al programa de Maestría enManejo de Vida Silvestre.

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2006 ROOSTS AND MIGRATIONS OF SWALLOWS 85

ROOSTS AND MIGRATIONS OF SWALLOWS

DAVID W. WINKLER

Cornell University Museum of Vertebrates, Department of Ecology and Evolutionary Biology,Cornell University. Ithaca, NY 14853, USA. [email protected]

ABSTRACT.— Swallows of the north temperate zone display a wide variety of territorial behaviourduring the breeding season, but as soon as breeding is over, they all appear to adopt a pattern ofindependent diurnal foraging interleaved with aggregation every night in dense roosts. Swallowsgenerally migrate during the day, feeding on the wing. On many stretches of their annual jour-neys, their migrations can thus be seen as the simple spatial translation of nocturnal roost siteswith foraging routes straightening out to connect them. However, swallows that must make longjourneys over ecological barriers clearly fly at night as well as in the day, and many suggestionsindicate that there is considerable complexity in the altitude and bearing of flights even duringthe day. There are especially intriguing indications that much swallow migration may take placehigh out of sight of ground observers with movements near the ground often associated withforaging in passage. Provided that roost sites can be reliably found, swallow migration can beextremely flexible, and there are interesting contrasts in the biogeography and phenologicalflexibility of swallows compared to other passerine birds. Even within the swallows, there isconsiderable interspecific and intraspecifc variability in the distances of their annual migrations,and we are only just beginning to understand the biological causes and consequences of thisvariation. The profusion of Doppler weather radar stations in the eastern United States has allowedthe characterization in considerable detail of the North American distributions of Tree Swallows(Tachycineta bicolor) and Purple Martins (Progne subis) throughout the non-breeding season.Evaluating the relative roles of movements and mortality in creating these patterns remains animportant challenge for further research.KEY WORDS: diurnal, Hirundinidae, martins, migration, nocturnal, roost, swallows.

RESUMEN. DORMIDEROS Y MIGRACIONES DE GOLONDRINAS.— Las golondrinas de la zona templada deAmérica del Norte poseen una amplia variedad de comportamientos territoriales durante laestación de cría, pero ni bien culmina la reproducción todas parecen adoptar un patrón común,alternando la alimentación diurna independiente con el agrupamiento en populosos dormiderosdurante la noche. Las golondrinas generalmente migran durante el día, alimentándose en vuelo;sus migraciones, entonces, pueden ser vistas como si fuesen un simple traslado entre distintossitios que poseen dormideros nocturnos, con las rutas de alimentación conectándolos directa-mente. Sin embargo, las golondrinas que deben realizar largos viajes cruzando barreras ecológicasvuelan tanto de noche como de día, y hay evidencias que indican que hay una considerablecomplejidad en la altitud y en las características de los vuelos aún durante el día. Hay evidenciasespecialmente interesantes de que la mayor parte de la migración de las golondrinas puede tenerlugar a una altura tal que no es advertida por los observadores en tierra, pero con movimientoscercanos al suelo a menudo asociados con la alimentación. Si los sitios con dormideros puedenser encontrados con certeza, la migración de las golondrinas sería extremadamente flexible, yexisten interesantes contrastes en la biogeografía y la flexibilidad de la fenología de las golondri-nas en comparación con otros paseriformes. Entre las golondrinas mismas hay una considerablevariabilidad inter e intraespecífica en la distancia de migración anual, y estamos aún empezandoa entender las causas y las consecuencias biológicas de esta variación. La creciente disponibilidadde estaciones con radares climatológicos Doppler en el este de Estados Unidos ha permitido lacaracterización, con un considerable detalle, de las distribuciones norteamericanas de la Golon-drina Bicolor (Tachycineta bicolor) y la Golondrina Purpúrea (Progne subis) durante la estación noreproductiva. La evaluación del papel relativo que juegan los movimientos y la mortalidad en laconformación de esos patrones es un importante desafío para futuras investigaciones.PALABRAS CLAVE: diurno, dormidero, golondrinas, Hirundinidae, migración, nocturno.

Received 13 March 2006, accepted 26 December 2006

Hornero 21(2):85–97, 2006

86 WINKLER Hornero 21(2)

The spatial biology of swallows and martins(Hirundinidae) in the breeding season isextremely diverse, ranging from dense andlarge colonial aggregations to dispersed terri-torial breeding (Turner and Rose 1989). Mostspecies are central-place foragers spendingmost of their foraging time well away fromthe immediate vicinity of the nest (Bryant andTurner 1982, Turner 1982, McCarty andWinkler 1999). The diversity of summer soci-ality has engendered a rich literature in thecomparative behavioural ecology of breedingsocial systems (e.g., Hoogland and Sherman1976, Møller 1987, Brown and Brown 1996,Safran 2004). The plethora of data on breed-ing biology and ecology (e.g., Winkler andAllen 1996, Burness et al. 2001, Hasselquist etal. 2001, Ardia et al. 2003, Czarnowski et al.2004, Lombardo et al. 2004, Safran andMcGraw 2004, Safran et al. 2005) contrastssharply with the relatively few studies thathave been published about the biology ofswallows during migration and in the non-breeding season (e.g., Lyuleeva 1973, Meadand Harrison 1979, Szep 1995). My goal hereis to review what we know about swallowmigration and wintering biology and presenthypotheses to explain some of the patternsthat are beginning to appear. I must empha-size that we know far too little, and this reviewis thus intended to serve as an invitation tofurther research rather than a compendiumof established facts.

SWALLOWS AS NOCTURNAL ROOSTERS

At least in the Northern Hemisphere,hirundinids outside the breeding season tendto spend every evening in large dense roosts.These roosts can sometimes be very large (wellin excess of a million birds; van den Brink etal. 2000, Burney 2002, Bijlsma and van denBrink 2005), and there are interesting differ-ences in roosting behaviour among species.Barn Swallows (Hirundo rustica) and TreeSwallows (Tachycineta bicolor) prefer to roostin reed or cane beds usually over water (vanden Brink et al. 2000, Burney 2002), occasion-ally using trees or wires (e.g., Moreau 1972).In contrast, the larger martins in the genusProgne prefer to roost in shrubbery or trees oron ledges under bridges and in large indus-trial buildings (Oren 1980, Russell andGauthreaux 1999, Purple Martin Conservation

Association 2005). All species appear to preferto roost over water, although all will roost intheir favoured substrate over dry land onoccasion (e.g., Skutch 1960). Species in thegenus Progne are variable in their approachto roosts, in some locations flying into theroost in small parties as sunset approaches(Russell and Gauthreaux 1999) and, in others,funnelling-in in one huge concentration (Oren1980). By contrast, Barn, Tree and rough-winged swallows of the genus Stelgidopteryxgenerally enter their roosts in very large, tightand short-duration streams.

One factor determining why Progne speciesprefer to roost in woody vegetation and onfirm structures may be that their larger massserves as a deterrent to perching in the tips ofherbaceous marsh vegetation. This mayexplain why Progne species are less tied toroosting over water than are the smaller spe-cies. The fact that these species enter the roostin a less organized fashion than do the smallerswallow species may also indicate that thesmaller species may have had their roostinghabits most strongly molded by the threat ofpredation. The smaller swallow species tendto come to roost some time in the hour aftersundown. Our observations of Tree Swallowroosts (Burney 2002, pers. obs.) appear to befairly typical of these smaller species (seeSkutch 1960 on Stelgidopteryx species): theswallows display their normal reluctance tosettle into vegetation, and the birds congre-gate a few hundred meters above the roostsite, milling around the site in an increasinglylarge and dense cloud of birds. Finally, as thelast daylight fades, a few courageous birdsmake the plunge downward into the reeds ofthe roost site, followed immediately by a swirl-ing stream of birds pouring into the vegeta-tion, with hundreds of thousands of birdssettling in only a few minutes’ time. Few whohave witnessed these spectacles can avoiddescribing the descending cloud as a tornado.Both the late hour of gathering and whatseems to be the birds’ extreme reluctance toventure solo into the vegetation suggest thatthe principal selective force molding thisbehaviour has been the risk of predation.Observations on Barn Swallows being preyedupon by aerial raptors as they come to roostin Africa (Bijlsma and van den Brink 2005)support this interpretation. This concernabout predation may also explain why the


birds appear to gather higher over the rooston clearer evenings (Skutch 1960).

The truly large roosts of hirundinids occurin migratory species, with the largest roostsgenerally being reported in wintering areasthat support birds that bred over much largerareas in the north. It remains to be seen towhat extent the non-migratory or short-dis-tance species visit roosts in the non-breedingseason. Resident Southern Rough-wingedSwallows (Stelgidopteryx ruficollis) appeared tojoin roosts of migrant Northern Rough-winged Swallows (Stelgidopteryx serripennis)in cane when they were in the vicinity, butthey also roosted in smaller aggregations inthe same site when the migrants were gone(Skutch 1960). Skutch (1960) also describes asmall group of seven Black-capped Swallows(Notiochelidon pileata) roosting together everynight after the breeding season in cold cloudforest habitat, in a burrow that was not usedfor nesting. He also reports that the Blue-and-white Swallow (Notiochelidon cyanoleuca) canroost year-round in and near its nest; thus,these species apparently do not join largepost-breeding roosts. I have seen a White-winged Swallow (Tachycineta albiventer) pair

settle down for the night with a fully volantjuvenile on small branches over a runningstream near Eldorado, Misiones Province,Argentina, on a date (9 March 2001) thatappeared to be outside the local breeding sea-son (Belton 1985). Roosts of 2000–10000 swal-lows (mostly the migrants Hirundo rustica andRiparia riparia in southern summer andTachycineta leucorrhoa and Tachycineta meyeni insouthern winter) occur regularly in the stateof Rio Grande do Sul in Brazil (R Dias and CFontana, pers. com.). And all the South Ameri-can Progne species appear to occur in largeroosts at some time in their annual cycles(Oren 1980, Hill 1995). Further reports on thesizes and locations of the roosts of tropicalswallows and data on whether they live theirmore sedentary lives without visiting largenocturnal roosts, would be very interesting.Such data would help us understand to whatextent nocturnal roosting aggregations aretied with migratory behaviour.

ROOSTS AND RADAR

Roosts generally empty out a few minutesbefore sunrise the next morning, and the birdstend to leave the roost once again en masse,retracing their flight upward to even higheraltitudes before flaring out on foraging flightsin all directions (Skutch 1960). This upwardflight, followed by the near-symmetric exodusof foraging birds in all direction, makes theselarge roosts of swallows apparent in the Dop-pler weather radar now deployed through-out the United States (Russell and Gauthreaux1999, Burney 2002; Fig. 1). The resulting roost“ring-echoes” provide the prospect of a syn-thetic view of the size and seasonal distribu-tion of swallow roosts throughout NorthAmerica (Russell and Gauthreaux 1998,Russell et al. 1998, Burney 2002). These remotemethods are being supplemented by orga-nized citizen science projects in both NorthAmerica (Purple Martin Conservation Asso-ciation 2005) and the United Kingdom (BritishTrust for Ornithology 2006) from which a greatdeal is being learned about comparative roost-ing biology.

One of the interesting aspects of roostingbiology is that roost sites vary considerablyin how consistently they are used from yearto year. For instance, only a few coastal sites,such as the one at Icklesham, Sussex, are reli-

Figure 1. How a flock of swallows emerging in earlymorning from their roost (R) climbs into the alti-tudes being scanned by weather radar (above),and spreading out from there in foraging flights(below) leaves a distinctive ring echo in the radarimage before it spreads out enough that the den-sity of flying swallows becomes so low as to beundetectable by the radar.


able Barn Swallow migratory stopover sitesfrom year to year in the United Kingdom,while all others being monitored so far in thiscountry seem to move around from year toyear (Griffin et al. 2005). Similarly, a largeswallow roost seems to occur every fall in themarshes of Montezuma National WildlifeRefuge near Ithaca, New York, but its preciselocation can vary by 5 km or so from year toyear (Burney 2002, Winkler and Haber,unpublished data). As we learn more abouthirundinid roosting biology, it will be interest-ing and of considerable conservation impor-tance to try to understand just what makes asite attractive from year to year: it may actuallybe the case that unpredictability per se is anadvantage in reducing the familiarity of roostsites to local predators.

ROOSTS AND MIGRATION

Over much of their migratory and winter-ing ranges, hirundinid roost sites appear tohave fairly consistent roost spacing. Roost sitesin North America tend to be about 100 to150 km apart, though there are certainly con-secutive roost sites in prospective northboundor southbound directions that are farther apart(Fig. 2). Spacing at distances approximating100 km is very similar to the scale of move-ments reported for roosts of migrant speciesof the genus Hirundo in South Africa (Oatley2000). By contrast, roost sites in Britain are

often much closer together, averaging as littleas 25–30 km apart (Ormerod 1991), and thewave of Barn Swallows returning to Britainmoves about 50 km/day (Huin and Sparks1998). This suggests that migrating hirundi-nids in Britain may actually have the luxuryof hopping over some roost sites in their jour-neys. However, even in North America, thedistances between many of the roost sites arewell within the range of a day’s fairly leisurelyflight. Flight speeds of migrating hirundinidsare in the range of 40–80 km/h (Lyuleeva1973), and even if the speeds of leisurelyforaging birds are half those, most roostspacings would appear to accommodate anunhurried itinerary from site to site.

These observations suggest an interestingmodel for swallow migration, with birdsmigrating through the day linking every nightto the next site in their successive chain ofnocturnal roost sites. Wintering swallows arereasonably seen as classical central place for-agers, with birds radiating out from the roostsite in early morning and most often return-ing to the same roost the following evening.Thus, migration for swallows may often be asimple extension of the loops of daily centralplace foraging into line segments of approxi-mately the same length linking up to the nextroost site (Fig. 3). It would be interesting toexplore how these connections to the nextroosts are made. Individual birds may set outfrom a roost in the morning with a memory

Figure 2. A compilation of weather radar datathroughout the southeastern United States for anearly morning in late summer. The image showsthe clear signatures of roost “ring-echoes” spacedfairly regularly at about 100 km throughout theregion.

Figure 3. A simple graphical interpretation of howmovements by foraging swallows between roostsites may involve very little if any increase in thedistance flown per day (right) relative to birds re-turning to the same roost site in succeeding nights(left).


of the next site on their migratory chain, orthey may simply forage more in the preferredmigratory direction and then be recruited tothe next roost site by aggregating near the endof the day with birds that used the next sitefor their own roost the night before. Thesebehavioural mechanisms of roost joiningwould also presumably illuminate the mys-tery of which sites are used from year to yearand serve as a clue to the causes of the inter-annual ebb and flow of roost size.

HIRUNDINIDAE MIGRATORY BEHAVIOUR

This view of swallow migrations as journeysstitched together by roost sites suggests thatthe exertion of migration on many parts oftheir journeys may not differ substantiallyfrom that expended during the daily and rou-tine foraging movements out from and backto a nocturnal central place. Thus, most move-ments of swallows appear to take place duringthe day with these fairly routine movementsfrom one roost site to the next. Yet, no matterwhat the details of how roosts and migrationare integrated, it is clear that not all parts ofall hirundinid migrations are a simple redi-rection of routine foraging patterns. There arerecords of marked Barn Swallows covering12000 km in 34 days (320 km/day) and 3028 kmin 7 days (433 km/day; Turner 2004). Theserates of movement are much greater thanthose likely to be achieved by birds makingmore leisurely movements from roost to roost.In addition, many of the longest and fastestpassages made by swallows are those madeby the three long-distance European swallowmigrants as they cross the Mediterranean andSahara. Like most passerines that make thistrip twice annually, or die trying, it seemslikely that the vast majority head south fromstaging areas in Spain or Italy (Rubolini et al.2002b), then cross directly to Africa, someprobably stopping to “coast” along theSaharan verge of the sea and others probablycontinuing directly to areas south of theSahara (reviewed by Moreau 1961). Hirundorustica is the most commonly seen bird cross-ing the Sahara, and, especially in spring, it isoften seen flying against, and not uncom-monly succumbing to, the northerly windsthat prevail at that season (Moreau 1961). Aselsewhere in their annual cycle, Hirundo spe-cies tend to fly lower than other hirundinids,

probably making them more visible thanDelichon and Riparia species during passage(Lyuleeva 1973). Moreau (1961) estimated thatall the passerines making the non-stop trans-Saharan trip in spring must fly 50–60 h non-stop against head-winds. Recent radarevidence (Schmaljohann et al. 2007) suggests,however, that the 2100–2400 km trip betweenEurope and tropical Africa is not made non-stop by most European passerines that crossthe Sahara and Mediterranean. Much moredetail is needed on the biology of these mi-grants. Nevertheless, the sudden and sporadicappearance of large numbers of all threeEuropean swallow genera at low elevationsduring migration, together with correlationsbetween the intensity of observed migrationsand local weather, suggest the hypothesis thathirundinids under very favourable winds flyout of sight high above the ground and thatthey fly nearer the ground when they arefaced with head winds or the need to refuelon insects en route. Flying insects are gener-ally more abundant near the ground (e.g.,Glick 1939, Taylor 1974), and it appears likelythat, when insects are relatively abundantover the terrain being over-flown, hirundinidsdescend to lower levels (i.e., nearer theground) to refuel, returning, once fed, tohigher elevations to cover much larger dis-tances when and where the winds arefavourable. This possible alternation betweenhigher altitude cruising and lower altitudeforaging flight could also explain: (1) whymigrating swallows often do not appear atmigration observation stations until hoursafter sunrise (Lyuleeva 1973) when they pre-sumably leave the roosts many hours earlier,and (2) why adults and juveniles appear tofly for different amounts of the day (e.g.,Gatter and Behrndt 1985). Nearly exclusivehigh altitude foraging may also explain theextreme sparseness of observations of somecommon species (e.g., Delichon urbicum;Moreau 1972) on the wintering grounds.

J. Cobb (in Griffin et al. 2005) reported thatHirundo species lured down to nets near aroost site in the United Kingdom by playbackof swallow song in the afternoon, well beforeswallows would be coming to roost, werenever captured in the roost later in the dayand averaged about 2 g heavier than thosecaptured later in the evening at the same site.This seemed to happen after warm days, sug-


gesting interesting environmental effects onthis behaviour; however, it also suggests notonly that high-flying birds may have greaterenergy stores but also that, even in the UnitedKingdom, there may be a diversity of migra-tory strategies in the Hirundo population andthat some birds might even be migrating atnight and making much more direct over-landprogress over the United Kingdom as a result.The generality and interpretation of this resultwould be strengthened enormously by play-back experiments well in advance of the roost-ing hour near hirundinid roost sites in otherplaces.

Any journey of two days or more requiresboth nocturnal and diurnal migrants to aban-don their preferred hours of flight, and it isclear that hirundinids fly both day and nightduring these long migratory passages (re-viewed in Moreau 1961). It remains an openquestion whether and how much hirundinidsfly at night outside the most extreme legs oftheir journeys, but it seems safe to continueto designate them as diurnal migrants.

In the Western Hemisphere, observations ofenormous numbers of migrant swallows pass-ing through Central America (Table 1; Brownand Brown 1999, Ruelas Inzunza et al. 2005),suggest that the bulk of North Americanswallows access wintering ranges south of theGulf of Mexico by an overland route; but thepresence of some individuals from all NorthAmerican species in Caribbean islands andmigrating over water in the Gulf confirm thatat least some individuals attempt the over-water route to the Southern Hemisphere

(Hailman 1962, Yunick 1977, Russell 2005).Given what closely related birds are able todo in the Eastern Hemisphere, it would beinteresting and important to try to determinethe actual proportions of birds using the over-land vs. direct aquatic route over the Gulf ofMexico, especially given that north-boundbirds appear to take more varied routes overland during spring migration than fall (RuelasInzunza et al. 2005, E Ruelas Inzunza, pers.com.).

BIOLOGY OF THE MIGRANTS

Southbound Hirundo species in Europe canaccumulate up to about 40% of their mass asfat (Rubolini et al. 2002a) preparing for theMediterranean–Saharan journey, and theyhave different fat dynamics if heading overGibraltar vs. Italy (Rubolini et al. 2002b). Bycontrast, Hirundo species in fall appear to gainonly 1–2 g (<25% of body mass) on averagein the United Kingdom before heading southto mainland Europe. Other hirundinids inEurope also appear to store less fat than doesHirundo rustica before heading to Africa(Cramp 1988). The dynamics of fat stores indifferent age and geographic classes ofHirundo rustica appears to make sense relativeto the ecologies of those groups (Pilastro andMagnani 1997). However, given the potenti-ally biased qualities of birds caught during mi-grations (see Hirundinidae migratory behaviourabove), interpretation of the masses reportedmust be made cautiously. If indeed themigratory behaviours of hirundinids are

Species Total Day of “peak” flight

Barn Swallow (Hirundo rustica) 2819674 11–16 September Sand Martin (Riparia riparia) 1785996 5–16 September Cliff Swallow (Petrochelidon pyrrhonota) 1301181 12–13 September Northern Rough-winged Swallow (Stelgidopteryx serripennis) 1121414 8–30 October Purple Martin (Progne subis) and Grey-breasted Martin (Progne chalybea) 179466 27 August–5 September All swallows combined 7077906 11–16 September

Table 1. Counts of migratory swallows made on the coastal plain of the Gulf of Mexico at La Mancha(19°36'N, 96°22'W), Veracruz, Mexico, in the autumn of 1999 by Robert Straub, assisted by Tom Valegaand Leticia Cruz. Counts were conducted approximately every other day from 24 August to 30 Novem-ber, 1999. The count was made from sunrise to sunset whenever possible; however, efforts tended to beconcentrated on the higher activity of the morning and afternoon flights. Data compiled by, and cour-tesy of, Ernesto Ruelas Inzunza of the Centro de Investigaciones Costeras de La Mancha (CICOLMA).


actually quite heterogeneous, a careful studyof how changes in body mass and individualbody components relate to the migratorybehaviour of individual birds could be bothextremely difficult and enlightening.

The biology of moult and how it relates tohirundinid breeding and migration appearsto be equally diverse. Among species, there isa gradient from species (such as Tachycinetabicolor; Stutchbury and Rohwer 1990) thatcomplete a full moult of body feathers, rec-trices and remiges before and during migra-tion; through populations that moult bodyfeathers as they initiate migration, stoppingto complete moult of rectrices and remigesbefore making a long-distance migration (e.g.,eastern Stelgidopteryx serripennis; Yuri andRohwer 1997); through species moulting bodyfeathers before and during migration and notinitiating or interrupting early flight feathermoult until reaching the wintering ground

(apparently all trans-Saharan species: Ripariaand Delichon species, Cramp 1988; Hirundorustica, Cramp 1988, van den Brink et al. 2000,Rubolini et al. 2002b, Griffin et al. 2005). Onceagain, there is ample evidence of flexibility inmoult schedules within species, with WesternStelgidopteryx serripennis adopting a strategymore like Tachycineta bicolor, moulting while itmigrates without interruption, in contrast tothe “moult migration” of the Eastern popula-tion (Yuri and Rohwer 1997).

WHY DO SOME MIGRATE SO MUCH

FARTHER THAN OTHERS?

Winkler (2000) suggested that there weremultiple selective reasons that have madechanges in swallow nest-type less evolution-arily flexible than other aspects of the life-his-tory, and much of the spring life history ofthese birds can be seen as adjustments to the

Figure 4. The breeding (right diagonal hatching) and wintering (left diagonal hatching) ranges of six east-ern North American swallow species relative to the type of nest they build at their northern nesting sites.


mode of nesting. The swallow fauna of easternNorth America is distinctive in the presenceof six obligate migrant species with diversenesting mode among them (Fig. 4). Of these,three are cavity adopters, reliant on other spe-cies or processes to create a nest-cavity inwhich they build a grass-nest cup. It seemsmore than coincidence that these three cavity-adopting species migrate the shortest dis-tances of the lot, a feature that likely allowsthem to return to the breeding grounds ear-lier in spring to compete for and secure a nest-cavity, which, unlike the burrowing andmud-nesting species, they cannot make forthemselves (see also Rubolini et al. 2005).

HOW PHYLOGENETICALLY FLEXIBLE IS

MOVEMENT IN SWALLOWS?

An alternative hypothesis to explain themore northerly wintering of the cavity-adopters is that patterns of movement maybe nearly as difficult to evolve as are patternsof nest construction, and that all the longest-distance migrants in the New World hirun-dinid fauna (Riparia riparia, Hirundo rustica andPetrochelidon pyrrhonota; Fig. 4) are derivedfrom Old World forms (Sheldon et al. 2005)that presumably colonized the Western Hemi-sphere relatively recently. However, availableevidence in support of this phylogeneticinertia hypothesis is less than compelling.First, there are two tropical species in the NewWorld fauna, Petrochelidon fulva and Petro-chelidon rufocollaris, that appear to havederived from Petrochelidon pyrrhonota in theNew World, and both are short-distance- ornon-migrants. Second, Riparia riparia, togetherwith its short-distance congener Ripariapaludicola from the Old World, appears to besister group to the genus Tachycineta and muchmore closely related to the endemic NewWorld swallows than they are to other OldWorld forms. Thus, the short-distance or non-migratory habits of Tachycineta species andRiparia paludicola appear not to have beenconstrained by the habits of their long-dis-tance close relative Riparia riparia. Finally,Hirundo rustica has begun breeding in SouthAmerica, on what were solely its winteringgrounds, within the past 30 years (Martínez1983). Though the movement patterns of thissmall breeding population are not known, itappears extremely unlikely that these birds

have retained the long-distance migratoryhabit of their immediate ancestors and per-form a long migration all the way to NorthAmerica in the austral winter (GH Huber, pers.com.). Hirundo rustica is known for the com-plexity of movement patterns within its largepopulations in both the Eastern and Westernhemispheres (Moreau 1972, Phillips 1986,Cramp 1988), with some resident forms inter-acting during parts of the year with both long-and short-distance forms passing through.Furthermore, Hirundo rustica is closely relatedto a large number of other species of the genusHirundo in sub-Saharan Africa, many of whichare residents or short-distance migrants (forall phylogenetic statements in this paragraphsee Sheldon et al. 2005). Finally, patterns ofmovement within the New World endemichirundinids are very flexible. Though thereare no long-distance migrants that go as faras Petrochelidon, Hirundo or Riparia species doin the New World, there is a great deal ofdiversity in distances travelled in the generaTachycineta, Progne and Stelgidopteryx. In short,the distance of movement seems to be quiteflexible in swallows (see also Turner and Rose1989), and the patterns observed above for thesummer and winter ranges of North Americanbreeding species seem more readily explainedby nest-site competition on the breedinggrounds than by phylogenetic conservatismof the traits.

FLEXIBILITY WITHIN SPECIES IN

WHETHER TO MIGRATE

There are at least two observations that sug-gest considerable flexibility in migratoryscheduling within populations of hirundinids.First, many first-year male Progne subis returnto the breeding grounds even though they donot generally breed their first year. Thissuggests that the observation of first-yearmales in the wintering grounds during thenorthern breeding season (Hill 1995) may ac-tually be the result of a strategy by theseyounger birds to forego the return to breed-ing areas until their chances of breeding arehigher (see also comment by Oren 1980). Itwould be interesting to investigate the prop-erties of those birds that stay in the south theirfirst year and compare them to those that com-plete the annual migratory circuit without at-tempting breeding on the northern end.


The other exceptional indicator of flexibilityin breeding and migration is provided bythose northern migrants that have begunbreeding in the southern wintering grounds.Delichon urbicum has bred and produced fledg-lings intermittently in South Africa, withindividual colonies sometimes lasting “forsome years”, but no sustained population hasbeen established (McLachlan and Liversidge1957, Maclean 1988:465). By contrast, and asmentioned above, a breeding population ofHirundo rustica in Buenos Aires Province,Argentina, colonized in the early 1980’s(Martínez 1983) and is still slowly growing (PPetracci and GH Huber, pers. com.). It is notyet clear whether this population is being sus-tained by local production of offspring or con-tinued recruitment from the migrant pool. Inany event, these cases of re-distribution ofmajor life events in the annual cycle suggesta flexibility in swallows that is equalled onlyby nomadic passerines of boreal forest ortropical deserts, and swallows appear to bethe only long-distance migrant passerineswith such flexibility. Just how, physiologically,this readjustment of the life history is per-formed is a fascinating area for on-goingresearch.

IMPLICATIONS OF DIURNAL MIGRATION

Unlike the bulk of other migrant bird spe-cies, the Hirundinidae are cosmopolitan. Fewother bird groups have achieved this breadthof distribution, and the migrations of swal-lows seem analogous with other broadlydistributed migrants, such as Apodidae,Accipitridae and Anatidae, with thrivingNorthern Hemisphere populations linked bymigration to habitats further south in thenorthern winter. All of these groups also sharethe property of being diurnal migrants, andother aerial insectivore long-distance migrants(e.g., Tyrannidae in the Western Hemisphereand Muscicapidae in the East) are nocturnaland are limited to one hemisphere or the otherin their distributions. Of course, there arenumerous insectivorous diurnal migrants thatmigrate smaller distances and do not currentlyoccur in both hemispheres (e.g., Meropidae,Artamidae). To test the possibility thatdiurnality of migration per se is associatedwith the broad-scale distributions of birds atthe family level, I categorized each avian

family into residents and migrants. I furtherdivided the migrants into diurnal, nocturnal,or both, and recorded whether these types aredistributed solely in the Eastern or WesternHemispheres or both (a much more detailedspecies-level treatment of migration modesworld-wide is forthcoming; Farnsworth et al.,unpublished data). In characterizing distribu-tions, I ignored single species in one hemi-sphere that otherwise were endemic to theother in four families (Alaudidae, Troglodyt-idae, Timaliidae and Sylviidae). The resultinganalysis (Table 2) shows, not surprisingly, thatresidents are much more likely to be endemicto one hemisphere or the other (i.e., there arefar fewer distributed in both than expectedby chance). By contrast, diurnal migrants aresignificantly more likely to occur in both hemi-spheres. Exactly how this pattern arises isunclear, but the broad array of visual cuesavailable to diurnal migrants may lend themincreased flexibility and the ability to exploreroutes for migratory possibilities that changewith changing Earth climate and that may notbe available to a more pre-programmed navi-gation–orientation system in nocturnal mi-grants. Hirundinids are clearly one of the mostflexible groups both in their migratory biol-ogy and breeding schedules, and it is perhapsa bit surprising that there are so many tropi-cal forms in this group with such limited dis-tributions (e.g., Hirundo megaensis, Tachycinetastolzmanni, Tachycineta cyaneoviridis, Tachycinetaeuchrysea, Notiochelidon pileata).

THE WAY FORWARD:MIGRATION AND MORTALITY

The exceptional flexibility of hirundinid life-cycles raises many interesting possibilities forresearch, many of which will become avail-able as soon as digital telemetry tags and data-loggers become small enough to deploy onswallows. These technological developmentsraise the prospect of following individualsthrough their annual cycles and relating theirpersonal histories and physiological states tothe movements that they undergo. Such tagsmay also eventually lead to a refinement ofour estimates of where in the life cycle mostswallows die and why.

Improved information on mortality coulddramatically increase our understanding ofthe lives of these resourceful birds and give


us powerful new knowledge to help sustaintheir populations on Earth. It appears thatmost adults die in non-breeding quarters andjuvenile survival is most affected by condi-tions on or near the breeding grounds (Szep1995, Stokke et al. 2005). The huge prepon-derance of juveniles in roosts in northern lati-tudes (Griffin et al. 2005), their variableproportions in African roosts from year to year(van den Brink et al. 2000), and the frequentobservation of dead and dying Hirundo rusticaduring trans-Saharan migration (Moreau1961, 1972) all indicate that mortality can beswift and severe at times.

Understanding the causes of mortality inthese long-distance migrants is a fascinatingand important challenge, but it may also beextremely interesting to apply this increasedknowledge to interpretation of patterns ofseasonal movement. If gathering the traces ofroost ring-echoes from weather radar fromacross North America can be automated, thereis the prospect of understanding the changingdistributions of a very large fraction of theworld’s population of at least Tachycinetabicolor through the annual cycle. When view-ing the changing distributions and sizes ofthese roosts, it is tempting to interpret the

Table 2. Summary of the distributions of families of birds of the world as they relate to the migratorymodes of their members. For each cell, the number of families is followed (in parentheses) by the devia-tion of the observed cell frequency from that expected from the marginal totals. Global analysis:χ2

6 = 66.091, P < 0.001. The two cells that contribute the most to the observed χ2 are indicated by anasterisk. Four families with unknown major migratory mode (Acanthizidae, Eopsaltridae/Petroicidae,Chionididae and Thinocoridae) were left out of this analysis.

Hemisphere of distribution

Migratory mode Eastern Both Western Total

Diurnal 8 (-2.175) a 28 (4.099 *) e 3 (-1.978) i 39 Nocturnal 11(-1.268) b 17 (1.284) f 9 (0.191) j 37 Both 4 (-1.247) c 11 (2.203) g 2 (-0.955) k 17 Resident 57 (2.772) d 6 (-4.454 *) h 28 (1.586) l 91 Total 80 62 42 184 a Alaudidae (one species Holarctic), Anseranatidae, Artamidae, Coliidae, Meliphagidae, Meropidae, Ploceidae, Sturnidae. b Campephagidae, Cisticolidae, Monarchidae, Muscicapidae, Oriolidae, Pittidae, Prunellidae, Pycnonotidae, Remizidae,

Sylviidae, Upupidae. c Coraciidae, Dicruridae, Glareolidae, Zosteropidae. d Acanthisittidae, Aegithinidae, Apterygidae, Atrichornithidae, Balaenicipitidae, Batrachostomidae, Brachypteraciidae,

Bucerotidae, Callaeatidae, Casuariidae, Cinclosomatidae, Climacteridae, Corcoracidae, Cracticidae, Drepanididae, Dromadidae, Estrildidae, Eurylaimidae, Grallinidae, Hemiprocnidae, Hypocoliidae, Ibidorhynchidae, Indicatoridae, Irenidae, Leptosomatidae, Lybiidae, Maluridae, Megalaimidae, Megapodiidae, Melanocharitidae, Menuridae, Mesoenatidae, Musophagidae, Nectariniidae , Numididae, Orthonychidae, Otididae, Pachycephalidae, Paradisaeidae, Paramythiidae, Pardalotidae, Passeridae, Pedionomidae, Philepittidae, Phoeniculidae, Picathartidae, Podargidae, Pomatostomidae, Pteroclididae, Ptilonorhynchidae, Rhynochetidae, Sagittariidae, Scopidae, Struthionidae, Timaliidae, Turnicidae, Vangidae.

e Accipitridae, Alcidae, Anhingidae, Apodidae, Bombycillidae, Ciconiidae, Corvidae, Dendrocygnidae, Diomedeidae, Falconidae, Fringillidae, Gaviidae, Hirundinidae, Hydrobatidae, Laridae, Motacillidae, Pandionidae, Pelecanidae, Pelecanoididae, Phaethontidae, Phalacrocoracidae, Phoenicopteridae, Procellariidae, Psittacidae, Spheniscidae, Stercorariidae, Sternidae, Sulidae.

f Burhinidae, Caprimulgidae, Certhiidae, Charadriidae, Cinclidae, Cuculidae, Haematopodidae, Jacanidae, Picidae, Podicipedidae, Rallidae, Recurvirostridae, Regulidae, Rostratulidae, Sittidae, Strigidae, Tytonidae.

g Alcedinidae, Anatidae, Ardeidae, Columbidae, Emberizidae, Gruidae, Laniidae, Paridae, Scolopacidae, Threskiornithidae, Turdidae.

h Aegithalidae, Aegothelidae, Fregatidae, Heliornithidae, Phasianidae, Trogonidae. i Cathartidae, Cotingidae, Trochilidae. j Cardinalidae, Mimidae, Parulidae, Pluvianellidae, Polioptilidae, Thraupidae, Troglodytidae, Tyrannidae, Vireonidae. k Icteridae, Rynchopidae. l Anhimidae, Aramidae, Bucconidae, Capitonidae, Cariamidae, Conopophagidae, Cracidae, Dendrocolaptidae, Dulidae,

Eurypygidae, Formicariidae, Furnariidae, Galbulidae, Momotidae, Nyctibiidae, Odontophoridae, Opisthocomidae, Oxyruncidae, Phytotomidae, Pipridae, Psophiidae, Ramphastidae, Rheidae, Rhinocryptidae, Steatornithidae, Thamnophilidae, Tinamidae, Todidae.


changes in distributions as representing themovements of birds up and down the northAtlantic coast. But the survival rates ofTachycineta bicolor at our Ithaca study site are,if anything, lower than those of Hirundo rustica(unpublished data). Thus, if we attribute shiftsin distribution to movement, we may forgetthat a large number of the birds detected inthe radars will not be returning to the breed-ing grounds. Just as dispersal from the natalgrounds confounds estimates of survival,movement and mortality may well be con-founded in the non-breeding season as well.When large roosts on the north Atlantic coastdisappear from the radar in autumn, some ofthe animals have no doubt migrated to thesouth, but a large proportion of them mayhave died instead. Short-distance facultativemigrants retain the possibility of getting backto the breeding grounds earlier, but the mor-tality cost of doing so may be larger than theextreme costs incurred by their cousinsmigrating longer distances.

ACKNOWLEDGEMENTS

Many thanks to Ernesto Ruelas Inzunza, CurtBurney, Eduardo Iñigo-Elias, Rafael Dias and CarlaFontana for sharing unpublished data with me andaiding their interpretation; to Andrew Farnsworthfor sharing his widespread knowledge of themigratory habits of the world’s birds; to AndrewFarnsworth, Jamie Mandel, Gernot Huber, andDave Cerasale for providing me with lots ofinsights and perspectives on bird migration; toTheunis Piersma and Andrew Farnsworth forvaluable comments on the manuscript; and toBenjamin Shattuck and Noah Hamm for help withthe figures. This material is based upon work sup-ported by the National Science Foundation undergrants No. IBN-013437 and 9207231, and a Coop-erative Agreement with the National Center forEnvironmental Assessment, EPA (CR 829374010).

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2006 MECHANISTIC INTERPRETATION OF BIRD MIGRATION 99

TOWARDS A MECHANISTIC INTERPRETATION OFBIRD MIGRATION IN SOUTH AMERICA

ALEX E. JAHN 1,4, DOUGLAS J. LEVEY 1, JENNIFER E. JOHNSON 2,ANA MARIA MAMANI 3 AND SUSAN E. DAVIS 3

1 Department of Zoology, University of Florida. 223 Bartram Hall, Gainesville, FL 32611, USA.2 Department of Biology, Swarthmore College. 500 College Ave., Swarthmore, PA 19081, USA.

3 Museo de Historia Natural Noel Kempff Mercado. Calle Irala N° 565, Santa Cruz, Bolivia.4 [email protected]

ABSTRACT.— Research to date has demonstrated that bird migration is comprised of highly diverseand plastic behavioural patterns. Our objective is to highlight the importance of studying mecha-nisms underlying these patterns in austral migrants. We focus on the high incidence of overlap inbreeding and non-breeding ranges as a particularly thought-provoking pattern. We then explorethe opportunities afforded by partial migration theory to elucidate the mechanisms underlyingseasonal range overlap. We propose that a mechanistic understanding of migration in SouthAmerica will both provide a deeper appreciation of the ecology, physiology and evolution ofmigratory species in the New World, and improve the scientific foundation for their conservation.KEY WORDS: mechanism, partial migration, population, range overlap, Tyrannus.

RESUMEN. HACIA UNA INTERPRETACIÓN MECANÍSTICA DE LA MIGRACIÓN DE AVES EN AMÉRICA DEL SUR.—La investigación reciente sobre aves migratorias ha demostrado que constituyen un grupo quepresenta comportamientos altamente diversos, plásticos y complejos. Nuestro objetivo generales resaltar la importancia de estudiar los mecanismos que generan los patrones que caracterizanla migración de aves en América del Sur. Para ello nos enfocamos en un patrón interesante (la altaincidencia de superposición en la distribución reproductiva y de invernada), analizando las opor-tunidades ofrecidas por la teoría de migración parcial para dilucidar los mecanismos que produ-cen tal superposición. Proponemos que una comprensión mecanística de la migración de aves enAmérica del Sur no solo proveería una apreciación más profunda sobre la ecología, la fisiología yla evolución de las especies migratorias del Nuevo Mundo, sino que también mejoraría los fun-damentos científicos para su conservación.PALABRAS CLAVE: mecanismos, migración parcial, población, superposición de distribuciones, Tyrannus.


Hornero 21(2):99–108, 2006

Research on various aspects of bird migra-tion — from biogeography to ecology andphysiology — has demonstrated that migra-tory behaviour is an extraordinarily diverseand complex phenomenon. For example, itcan evolve relatively rapidly (Able and Belthoff1998, Berthold 1999, Piersma et al. 2005), isphylogenetically flexible (Böhning-Gaese andOberrath 1999), and can appear and disappearthrough time within a lineage (Zink 2002, Jo-seph et al. 2003, Outlaw et al. 2003) or evenwithin an individual’s lifetime (e.g., Schwabland Silverin 1990). In the New World, a con-tinuum of migratory strategies exists, fromlong-distance migrations undertaken by allpopulations of a species to short-distance

migrations undertaken by only some popula-tions (Levey and Stiles 1992) or individuals(e.g., Ketterson and Nolan 1976). Migrationcan even play a central role in speciation(Winker 2000, Winker and Pruett 2006).

To solve persistent riddles about the evolu-tion and regulation of migration requiresteasing apart factors confounded in space andtime. This is difficult to accomplish without abroad geographic scope. In the New World,almost all work on migration has been restric-ted to the north-temperate latitudes (Levey1994, Jahn et al. 2004), with relatively littleattention paid to migration within SouthAmerica (austral migration, sensu Chesser1994). Some species of Neotropical austral

100 JAHN ET AL. Hornero 21(2)

migrants move annually between the tem-perate zone and tropical latitudes and somespecies migrate within either tropical or tem-perate latitudes of the continent (Joseph 1997).There are more than 220 species of Neotropi-cal austral migrants, comprising the largestmigratory system in the Southern Hemi-sphere (Chesser 1994). Recent literature onmigration in South America principally ex-plores biogeographic patterns (e.g., Chesser1994, da Silva 1999, Capllonch and Lobo 2005),evolution (Joseph et al. 2003), habitat associa-tions (e.g., Chesser 1995, Stotz et al. 1996, Jahnet al. 2002) and the timing of migratory move-ments (e.g., Hayes et al. 1994).

The geographical patterns of migration inthe Neotropics are complex (Morton 1977,Winker et al. 1997, Bildstein 2004). In somespecies all populations migrate, but in othersdifferent populations migrate in the same orin different directions. Furthermore, all ofthese strategies can occur within one genus(e.g., genus Tyrannus, Fig. 1; Ridgely and Tu-dor 1994, Chesser 1995). This stands in sharpcontrast to the situation in North America,where all the populations of migratory spe-cies generally move in the same directionduring each season.

Given the diversity of migration strategiesevident within South America, it is clear thatthe phrase “bird migration in South America”encompasses a multitude of inter- and intra-specific patterns at smaller scales than theoverall pattern at the continental level wouldsuggest. Thus, to better understand how mi-gratory birds respond to competing ecologi-cal and physiological demands, it will beessential to form links between patterns ob-served at different spatial and temporal scalesand among taxonomic (e.g., families and spe-cies) and biological levels of organization (e.g.,genotypes, individuals, ecosystems) (Levin1992).

Our objective is to demonstrate that researchon the mechanisms generating specific pat-terns of bird migration in South America is aprerequisite to gaining a better theoreticalfoothold, as well as for the ability to formu-late sound, proactive conservation and man-agement strategies. We use as an example thehigh incidence of seasonal range overlap inthe distributions of South American migratorybird populations to highlight the power ofexisting theory on intrapopulation variationin migratory behaviour to explain such pat-terns.

Figure 1. Generalized seasonal distributions of Tyrannus savana savana (a), Tyrannus albogularis (b), andTyrannus melancholicus melancholicus (c) in South America. Black polygons represent seasonal non-breedingranges, white polygons represent seasonal breeding ranges and the gray polygon represents area ofoverlap in which permanent residents as well as non-breeding (i.e., overwintering) migratory individu-als from the south occur together. Adapted from Chesser (1995).


A FOCUS ON MECHANISMS

Studying mechanisms — the proximate re-lationships between what an individual ex-periences and how it responds — is the keyto being able to explain the causes for ob-served patterns, advancing both basic science(i.e., explanations, predictions, the formula-tion of original questions) as well as practicalapplications (i.e., conservation and environ-mental planning and management). Such re-wards will only result from studies that arefocused on specific questions and employ test-able hypotheses (Vuilleumier 2004).

Tests of mechanistic hypotheses (i.e., howcomponent parts of the phenomenon inter-relate) — rather than phenomenological ex-planations (i.e., models that extrapolate futuretrends based on past trends) — are useful forinterpreting the reasons for changes observedin a pattern (e.g., migratory timing or direc-tion) (Koehl 1989), especially in light of themagnitude and speed of contemporaryanthropogenic changes in global biogeo-chemical cycles (Lubchenco 1998). From anapplied perspective, knowing where speciesare located during the entire annual cycle isnecessary to formulate a basic conservationplan. However, an understanding of the fac-tors influencing survival and reproduction atsmaller spatial scales enables a more effectiveconservation strategy. For example, Marra etal. (1998) demonstrated that the quality ofhabitats occupied by Setophaga ruticilla indi-viduals during the non-breeding season canaffect their physical condition and thus theirarrival date on North American breedingranges, which has consequences for theirreproductive success. In this case, knowledgeof the life-history consequences of habitat useopens the door to the formulation of moredetailed conservation priorities.

Studying the mechanisms that regulate thecomponents of a system also allows patternsto be placed within an evolutionary context.As pointed out by Moore and Aborn (2000),research about habitat selection during migra-tion has historically focused on describinghabitat use rather than examining the mecha-nisms through which selection acts. Thus, toelucidate the processes responsible forobserved patterns, it is important to considerthe evolutionary history of a species as wellas contemporary constraints. Taking just such

an approach, Böhning-Gaese and Oberrath(2003) concluded that contemporary habitatpreferences of migrants have been stronglyinfluenced by the historical occupation of rela-tively open habitats in Africa (by ancestors ofHolarctic migrants) and of Neotropical forests(by ancestors of Nearctic migrants), as well asby contemporary processes.

Nevertheless, an ability to understand thecauses of patterns evident at the populationlevel demands research on processes occur-ring at the individual level (Koehl 1989). Thisis because the evolutionary mechanisms thatgenerate population-level migratory patternsoriginate from variation among individuals.Thus, a focus on the individual is essential forformulating and testing hypotheses about theevolution of migration (Bell 2000). Researchfocused at the level of the individual requiresconsideration of the ecological constraintsencountered by individuals on different scalesthroughout their annual cycle. For example,a bird that forages on a scale of hundreds ofmeters may migrate hundreds of kilometersto search for similar resources at another site.Thus, migratory species are affected byprocesses occurring on vastly different tem-poral and spatial scales (e.g., Alerstam andÅkesson 2003). Forming links between thesedisparate scales is one of the central challengesnot only of migrant bird ecology, but of sciencein general (Levin 1992).

Finally, since migratory behaviour is anattribute regulated by a suite of characters(e.g., physiological, social; Piersma et al. 2005),it is important to formulate hypotheses aboutthese characters within an explicitly phyloge-netic context (Zink 2002). In South America,the diversity of movement patterns, evenwithin a single species (e.g ., Myiarchusswainsoni; Joseph et al. 2003), may be a com-plex and long-term response to changingenvironmental conditions on the continent.However, diverse migratory behaviours canalso appear on much shorter time scales. Onenotable example is the appearance of popula-tions of Hirundo rustica that are beginning toreproduce within their historical non-breedingrange, particularly in the coastal zone of theprovince of Buenos Aires, Argentina (Martínez1983).

We now have the opportunity to designstudies within South America to test theoriesformulated in other migration systems. With


such an approach, we can both enrich ourunderstanding of migration within SouthAmerica and test the explanatory power ofextant theories across migratory systems. Wecan begin to answer such questions as: dosimilar ecological, physiological, and geneticmechanisms underlie all migratory systems?;does migration within South America operateunder different “rules” than in other systems?For example, the capacity for nocturnal com-pass orientation is highly conserved phylo-genetically in migratory birds around theworld (Piersma et al. 2005). In mid- and high-latitudes, migratory birds can use a magneticinclination compass for orientation, but thissystem cannot function at equatorial latitudes(Wiltschko and Wiltschko 1995). Thus, whatalternative cues can migrants use to orient andnavigate in equatorial South America? Clearly,research in this area will allow us to test extantmechanistic theories as well as formulate newhypotheses about the migrations of birds.

In the next section, we use the seasonal over-lap of ranges to launch a discussion of how todistinguish between populations of migratoryspecies, as well as how to study the mecha-nisms operating within these populations.

RANGE OVERLAP

What patterns characterize bird migrationwithin South America? Stotz et al. (1996) andChesser (1994) identified several key features:(1) taxonomic composition (in South America,the family Tyrannidae makes up nearly a thirdof all migratory species on the continent);(2) distance of migration (within SouthAmerica, most migrants move over shorterdistances than do Nearctic-Neotropicalmigrants); (3) proportion of migratory speciesalong a latitudinal gradient (in South America,the gradient of increasing number of migra-tory species with latitude is less dramatic thanin North-temperate latitudes); and (4) rangeoverlap (approximately two-thirds of Neotro-pical austral migrants — 159 species — exhibitoverlap in population ranges across seasons;i.e., migrants of one population migrate toareas already occupied by conspecifics that donot migrate). Although these four patterns arecoarse-grained and described at a continentalscale, they offer a point of departure fromwhich to look for more specific patterns (Stotzet al. 1996). We focus on the pattern of range

overlap among populations as an interestingpattern to explore the mechanisms that mayunderlie it.

Several biogeographical explanations havebeen offered to explain the causes of rangeoverlap. Chesser (1994) offered two hypo-theses. First, given that the South Americancontinent is wider towards the equator, birdsmoving northwards towards the equator afterthe breeding season could experience a reduc-tion in interspecific competition as a conse-quence of lower population densities due tothe increasing land area, reducing their needto continue migrating northward. Second,there are no evident geophysical barriers tothe east of the Andean Cordillera to segregatebreeding and non-breeding ranges. In a simi-lar vein, Hayes et al. (1994) proposed that thediminished land area at high latitudes corres-ponded to a reduced capacity to sustain breed-ing populations of migratory species, thusproducing relatively short migrations be-tween tropical and temperate latitudes.

To test mechanistic hypotheses on the pat-tern of range overlap, however, we mustknow something about the variation inmigratory distance among individuals, sincedifferent strategies among individuals may bepresent across the species’ range. In essence,seasonally overlapping ranges obscure anypattern of exactly where migratory indivi-duals pass the non-breeding season (Stotz etal. 1996). Some populations may even bemigrating within the area of overlappingranges. For example, within any one species,there may be populations that are completelyresident, as well as some that are partiallymigratory (ie., some individuals of a popula-tion migrate; Fig. 2). Thus, the area of overlapmay “mask” substantial variation in migratorymovements among populations. Further-more, migrant and resident individuals maybe partitioning the area of overlap in differentways. For example, Tellería and Pérez-Tris(2004) studied habitat associations in Erithacusrubecula, a European migrant species com-prised of migratory populations whose non-breeding distribution overlaps with thedistribution of resident populations in thesouth of the continent. They found that resi-dents and migrants were physiologicallydifferent and occupied distinct habitats duringthe period of overlap. Consequently, in orderto study the mechanisms underlying range


overlap, it will be important to differentiatebetween populations and to define their“connectivity”: the origin and destination ofmigratory populations (for a review, seeWebster et al. 2002). Once the migratory pat-terns of populations have been characterizedas migratory, resident, or partially migratory,research can turn to the question of whichprocesses underlie their migratory pattern.

Information on connectivity of populationsand, at a local scale, on habitat use by differentindividuals (i.e., migrants vs. residents) hasobvious relevance for conservation policy. Forexample, if one population is in decline in thebreeding area, knowledge of where it spendsthe non-breeding season within the area ofoverlap can greatly help to pinpoint the partof the life cycle in which the greatest threatsto the survival of that population occur.

We now focus on some ideas about how tostudy mechanisms that operate on an intra-population level and produce population-level patterns. We use partial migration as anexample (Fig. 2). For a recent review of otherpopulation-level migration patterns, seeBoulet and Norris (2006).

PARTIAL MIGRATION

Partial migration is perhaps the most com-mon type of bird migration in the world(Berthold 2001). From an evolutionary stand-point, partial migration is thought to be anintermediate step in the evolution of completemigratory behaviour in birds (Berthold 1999).Consequently, studying the processes thatproduce partial migration could be a key tounderstanding more about the proximate andultimate processes that govern migratorymovements in species with overlappingranges.

Before discussing the processes producingpartial migration, it is important to distinguishbetween population-level partial migrationand intra-population partial migration. Inpopulation-level partial migration, somepopulations of a species migrate and otherpopulations do not. For example, in Tyrannussavana, the nominate subspecies is a Neo-tropical austral migrant, while another sub-species (Tyrannus savana sanctaemartae) remainsas permanent resident in the northern part ofthe continent (Chesser 1995, Stiles 2004). Thispopulation-level variation in migration

Figure 2. Two hypothetical patterns of population-level migration of Tyrannus melancholicus melancholicus:(a) migration exclusively of populations between a seasonal breeding area and an area of range overlap,and (b) migration of populations between a seasonal breeding area and an area of overlap, as well aspartial migration of some populations within the area of overlap. Gray areas: populations of permanentresidents, hatched areas: partially migratory populations, white areas: completely migratory popula-tions, dashed arrows: partial migration, closed arrows: complete migration.


characterizes at least 70% of the migratoryspecies in South America (Parker et al. 1996).In the case of intra-population partial migra-tion, some individuals of the same populationmigrate after the breeding season and othersdo not (sensu Lack 1943; for a review, seeBerthold 2001, Jahn et al. 2004). Differencesin migratory behaviour between individualsin the same population have been widelydocumented in other migratory systems buthave not yet been documented in SouthAmerica. Hereafter, when we refer to “partialmigration”, we consider specifically intra-population partial migration.

The first studies on partial migration tendedto be descriptive or to focus on evolutionary,population-level processes (e.g., Lack 1943,1954, Kalela 1954, Cohen 1967, von Haartman1968, Biebach 1983). More recently, emphasishas moved towards identifying and weigh-ing the differences between individuals.Within this context, “migrant” and “resident”are considered to be alternative strategies withdifferent benefits for different individuals ina population (e.g., Swingland 1983). Indi-vidual asymmetries (e.g., age, size) are postu-lated to determine migratory status becauseof differences in competitive advantagebetween individuals. Lundberg (1987) contrib-uted to this framework by adding the para-meter of frequency-dependent choice, inwhich individuals of different social rank (e.g.,juveniles low in the social hierarchy) decidewhether to migrate, depending upon the rela-tive frequencies of the dominant and sub-dominant individuals in the population withwhich they have to compete. Indeed, factorssuch as age, sex and social status in a popula-tion have been shown to determine migratorybehaviour (e.g., Gauthreaux 1982, Schwabl1983, Adriaensen and Dhondt 1990). Forexample, Able and Beltoff (1998) demons-trated that among Carpodacus mexicanusmigrating within North America, youngerindividuals were characterized by a highertendency to migrate. These demographic andsocial conditions are often tightly linked tosuch parameters as competitive ability,physiological tolerance and habitat associa-tions, which in turn are postulated to affectmigratory status (Ketterson and Nolan 1983,Cristol et al. 1999, Tellería and Pérez-Tris 2004).Thus, a test of the relationship between theseparameters (e.g., physiological tolerance,

social dominance) and migratory strategy(e.g., migratory timing, migratory distance)produces mechanistic models on the causesof such patterns as range overlap. It followsthat identifying demographic (e.g., age, sex),social (e.g., dominance), and morphological(e.g., body size) differences between indi-viduals is a prerequisite to studying theprocesses responsible for variation in themigratory behaviour among individuals of apartially migratory population (i.e., whetheror not an individual migrates).

What, then, are some specific, testablemechanistic hypotheses that can begin to teaseapart potential causes for range overlap?Partial migration is one class of the broadercategory of differential migration, in which in-dividuals within a population undertakemigrations of varying distances (e.g., Ketter-son and Nolan 1976). In partial migrants, thedistance travelled by some members of thepopulation falls at an extreme of a gradient:zero migration (i.e., residence). Thus, sincepartial migration is a class of differential mi-gration (Alerstam and Hedenström 1998),much of the theory about differential migra-tion is applicable to partial migration and viceversa. A great variety of theories attempt toexplain partial and differential migration, butthe majority are variations on three generalhypotheses (Bell 2005). The first one is theDominance Hypothesis. Subdominants arepoor competitors for available food; whenthere are not sufficient resources for all theindividuals in a population, subdominants aretherefore more likely to migrate in order toavoid competition with dominant individu-als. Supporting data are principally indirect,based upon the observation that in differentspecies younger individuals or females aresubdominant and migrate longer distances(e.g., Junco hyemalis; Ketterson and Nolan1976). The second hypothesis is the ArrivalTime Hypothesis. Individuals that establishterritories at the beginning of the breedingseason are less likely to migrate as far becausea short migration distance ensures a rapidreturn to the breeding range and access to thebest territories. For example, in a study ofAnser caerulescens, Bêty et al. (2004) found asignificant relationship between the arrivaldate on the breeding grounds and the prob-ability of reproducing (although excessivelyearly arrivals suffered from negative climatic


effects). Finally, the third hypothesis is theBody Size Hypothesis. In accordance with therelationship between body surface area andvolume, larger individuals can better with-stand lower temperatures and endure foodlimitations, giving them a lower probabilityof migrating away for the winter. For example,in Carpodacus mexicanus, females are sociallydominant, but also smaller in size and tend tomigrate further than males (Belthoff andGauthreaux 1991). Studies evaluating thesehypotheses have generally failed to producedata that predict migratory distance (e.g.,Junco hyemalis; Ketterson and Nolan 1985).Future research in South America could testthe explanatory power of these hypotheses ina context independent of the North-temperatesystem within which the hypotheses wereoriginally formulated.

FUTURE DIRECTIONS

Given the challenge of understanding themechanisms underlying such a complexsystem, it is timely to note several themes thatmay put this type of research in perspective.

Comparisons among common taxa in the New World

Current theory postulates a Neotropicalorigin for migratory species in the New World,both Nearctic-Neotropical and Neotropicalaustral migrants (Levey and Stiles 1992,Rappole 1995, Joseph 1997, Chesser and Levey1998, Joseph et al. 1999, Böhning-Gaese andOberrath 2003). A review of the data fromParker et al. (1996) reveals that at least 34 fami-lies, 56 genera and 23 species have popula-tions of both Nearctic-Neotropical andNeotropical austral migrants. For example,Pyrocephalus rubinus have populations that areNearctic-Neotropical migrants and otherpopulations that are Neotropical australmigrants (Parker et al. 1996). Intraspecific com-parisons of populations employing differentstrategies (Neotropical austral vs. Nearctic-Neotropical migration) are therefore possibleand have the advantage of avoiding the con-founding effects of phylogeny that commonlyhaunt interspecific comparative studies.Specifically, intraspecific research amongpopulations of one species rather than com-parisons between species decreases the effectsof a shared phylogenetic history, which isproblematic because it leads to a lack of inde-

pendence in the parameters being compared(e.g., Gittleman and Luh 1992, Garland andAdolph 1994).

Conducting comparative studies amongmigratory systems offers the additional ben-efit of avoiding the circular logic of attempt-ing to test a hypothesis explaining the causesof a pattern in the same system within whichthe hypothesis was originally developed. Forexample, within South America, at least twodistinct migratory sub-systems have evolved(Joseph 1997). Extant hypotheses can beevaluated in each sub-system independently.

Available techniques and technologies

The complexity of migration within SouthAmerica demands an interdisciplinary re-search approach, incorporating a variety oftechniques and technologies (Alerstam andÅkesson 2003, Barlein 2003). What tools canbe applied to migration research in SouthAmerica? New technologies exist that can sup-ply data on diverse temporal scales (betweenyears, months, or days), spatial scales (metersor kilometers), and between levels of biologi-cal organization (cellular, organismal, popu-lation-level). One particularly exciting newtool is stable isotope analysis, which can beused to determine the origins of migratory in-dividuals (see Hobson 2005 for a review, andTorres Dowdall et al. 2006, in this volume).Base isotope maps do not currently exist formost isotopes throughout the whole of SouthAmerica, but may be available in the nearfuture.

International collaboration

Because migratory species confront varyingconstraints throughout the annual cycle(Sillett and Holmes 2002), and since events inone season can exert substantial influenceover processes in subsequent seasons (e.g.,Marra et al. 1998, Norris et al. 2004), researchshould be conducted throughout all phasesof the annual cycle. This may most easily beaccomplished by establishing collaborativeinternational networks of researchers andconservation practitioners (e.g., Barlein 2003).Such associations could standardize methodsand share data about the same species andpopulations. These activities will be essentialfor advancing the study of patterns andmechanisms (see Stiles 2004 for suggestions


and interesting questions), as well as advancingthe conservation of populations of migratoryspecies that cross political boundaries.

Research at the individual level

We emphasize the value of collecting indi-vidual-specific data (e.g., through colour-banding and genetics). Mechanisms apparentat the population level originate at the indi-vidual level; therefore, descriptive studiesconducted at the individual level, such asMcNeil’s (1982) work documenting winter sitefidelity in Elaenia parvirostris, are particularlyuseful to guide the development and testingof mechanistic hypotheses.

CONCLUSION

Numerous questions are wide-open lines ofresearch — both descriptive and hypothesis-based — in South America. Much progresshas been made on other continents aboutproblems that remain unsolved in SouthAmerica, such that existing bodies of theory,technologies and methods could be readilyapplied to research on South American mi-gration. Interesting questions concerning theevolution of migration for which we knowlittle in South America include: (1) biogeo-graphy (what is the relationship between spe-ciation rates and migratory behaviour acrossclades?, how does this relationship comparein South America to other migratory sys-tems?); (2) ecology (what is the winter ecol-ogy of Neotropical austral migrants?, what isthe relationship between migratory timingand biotic vs. abiotic factors?); (3) physiology(do Neotropical austral migrants employ asimilar navigation system as migrants in othersystems?, what are the energetic constraintsto migration in South America relative to othersystems?); (4) life-history (which part of thelife cycle is most limiting in terms of repro-ductive success and survival?, are there carry-over effects for reproductive success betweenseasons?). The answers to such questions willprovide a basis upon which to ask more ques-tions and further develop more detailed,mechanistic hypotheses. Given the complex-ity that characterizes austral migration, ourunderstanding of New World bird migrationwill be greatly enriched when we undertakea multidisciplinary approach that incorporatesboth descriptive and theoretical research to

elucidate the origins and maintenance ofmigratory patterns in South America.

ACKNOWLEDGEMENTS

We thank Víctor Cueto for his invitation toparticipate in the symposium “Aves migratoriasamericanas: algunos apuntes para conocerlas” andthe organizers of the XI Reunión Argentina deOrnitología for their support. Comments from twoanonymous reviewers served to greatly improvethe quality of this paper. These ideas are based ingreat part on the present research of the authorswhich is financed in part by the National ScienceFoundation (OISE-0313429, 0612025), AmericanOrnithologists’ Union, Wilson OrnithologicalSociety, Western Bird Banding Association, Schoolof Natural Resources and Environment-Universityof Florida, and Estancia Caparú (Bolivia).

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2006 DOMINO EFFECTS AT STOPOVER SITES IN RED KNOTS 109

ANNUAL SURVIVAL OF RED KNOTS (CALIDRIS CANUTUS RUFA)USING THE SAN ANTONIO OESTE STOPOVER SITE

IS REDUCED BY DOMINO EFFECTS INVOLVINGLATE ARRIVAL AND FOOD DEPLETION IN DELAWARE BAY

PATRICIA M. GONZÁLEZ 1,4, ALLAN J. BAKER 2,3 AND MARÍA EUGENIA ECHAVE 1

1 Fundación Inalafquen. Roca 135, 8520 San Antonio Oeste, Río Negro, Argentina.2 Royal Ontario Museum. 100 Queen’s Park, Toronto, ON M5S 2C6, Canada.

3 Department of Zoology, University of Toronto. Toronto, Canada.4 [email protected]

ABSTRACT.— Ecological conditions in breeding and non-breeding areas of migrant birds havebeen linked to their annual survival and production of young, but the role of stopover sites isunder-appreciated. Through banding studies and censuses along the flyway from Tierra del Fuegoto the Canadian Arctic, the drastic decline in 2000–2001 of Red Knots (Calidris canutus rufa) popu-lation summering in southern South America in the northern winter was shown to be related tothe overharvesting of horseshoe crabs (Limulus polyphemus) in Delaware Bay, USA, their last stop-over site before reaching their breeding grounds, and to the late arrival of the birds at this site. InSan Antonio Oeste, Argentina, where 25–50% of the Tierra del Fuego Red Knots population con-gregates every northward migration season, annual survival of the cohort of experienced birdsbanded in March 1998 was impacted a year later than the general decline. Knots marked at SanAntonio Oeste earlier in March arrived in Delaware Bay on average before those marked 15 dayslater. Additionally, early migrating knots with active body moult in San Antonio Oeste exhibiteda higher return rate in the following years than late and non-moulting birds. Since the decline,birds arriving late in Delaware Bay have been at increased risk of not being able to refuel properlyor on time because food is no longer superabundant at that stopover site. These domino effectsindicate that there are fitness consequences to individual migration strategies adopted by birdsat austral summering and stopover sites, which can be amplified by compressed timing inDelaware Bay when food is depleted at this final stopover site.KEY WORDS: Calidris canutus, domino effects, migration, population decline, Red Knot, stopover ecology.

RESUMEN. REDUCCIÓN DE LA SUPERVIVENCIA ANUAL DEL PLAYERO ROJIZO (CALIDRIS CANUTUS RUFA) ENSU ESCALA MIGRATORIA DE SAN ANTONIO OESTE, ARGENTINA, POR EFECTOS DOMINÓ DE LLEGADA TARDÍA YDEPRESIÓN DEL RECURSO TRÓFICO EN BAHÍA DELAWARE.— Si bien se ha relacionado la condición delas áreas de estadía no reproductiva y reproductiva de las aves migratorias con su supervivenciay producción de crías, el papel de los sitios de escala como limitante del tamaño poblacional esescasamente conocido. Mediante estudios de anillado y censos a lo largo de la ruta de vuelodesde Tierra del Fuego hasta el Ártico de Canadá, hemos relacionado la drástica declinación de lapoblación de Playero Rojizo (Calidris canutus rufa) ocurrida durante 2000–2001 con la sobrepescadel cangrejo herradura (Limulus polyphemus) en su última escala en la migración hacia el norte(Bahía Delaware, EEUU) y la llegada tardía de las aves. En San Antonio Oeste, Argentina, dondese congrega el 25–50% de la población de Tierra del Fuego durante la migración al norte, el segui-miento de aves experimentadas de la cohorte anillada en marzo de 1998 permitió estimar que susupervivencia fue afectada un año más tarde que la declinación general. Las aves marcadas mástemprano en marzo llegaron antes a Bahía Delaware, en promedio, que las marcadas 15 díasdespués. Además, las aves tempranas con presencia de muda activa de plumaje corporal mostraronuna tasa de retorno significativamente mayor en años posteriores que las aves sin muda activa.Desde la declinación, las aves tardías incrementaron el riesgo de no acumular reservas apropiada-mente o a tiempo, debido a que el recurso trófico dejó de ser superabundante en Bahía Delaware.Estos efectos dominó indican que las estrategias de migración individuales originadas en las áreasde estadía austral y en los sitios de escala migratoria tienen consecuencias sobre la adecuaciónbiológica y que éstas pueden ser amplificadas por la reducción en el tiempo de estadía en BahíaDelaware cuando el recurso trófico es escaso en este sitio.PALABRAS CLAVE: Calidris canutus, declinación poblacional, ecología de escala migratoria, efecto dominó,migración, Playero Rojizo.


Hornero 21(2):109–117, 2006

110 GONZÁLEZ ET AL. Hornero 21(2)

The role of the condition of birds in non-breeding staging areas, breeding sites, or bothin limiting long-term or year-to-year popula-tion sizes in migrants has been the subject ofmany studies in different bird taxa, especiallyin shorebirds (e.g., Evans and Pienkowski1984, Evans et al. 1984, Pienkowski and Evans1985, Newton 2004). In some species, habitatsoccupied in wintering areas (also known as“austral summering areas” in the SouthernHemisphere) and migration flyways, and theirassociated food supplies, can influence thebody condition, migration dates and subse-quent breeding success of migrants (Marra etal. 1998, Drent et al. 2003). Similarly, the num-bers of young produced in one region could,through density-dependent processes, affectsubsequent overall mortality in another region(e.g., Goss-Custard et al. 1995). Thus, eventsin breeding, migration and “wintering areas”are interdependent in their effects on birdnumbers (reviewed in Newton 2004). Althoughless is known about long distance migrants,we hypothesize that population size might belimited by intra- or interspecific competitionat key stopover sites if they face low foodavailability, higher predation risk, and in-creased disturbance or poor quality roostingplaces.

One of the best known shorebird species isthe Red Knot Calidris canutus (Scolopacidae)which has a circumpolar breeding distributionin the Northern Hemisphere comprised of sixdiscrete populations that are recognized assubspecies on the basis of differences inmorphometrics and plumage (Piersma et al.2005). Of these subspecies, Calidris canutus rufatravels the longest migration of about 16000 kmtwice a year between their breeding groundsin the Arctic and their summering (= north-ern wintering areas) sites in Tierra del Fuegoand Patagonian Argentina (Morrison andHarrington 1992, Piersma and Davidson 1992,Harrington 2001, Tomkovich 2001). Duringtheir journeys, they congregate at the scarcewetlands extensive enough to support largeflocks of birds. Such wetlands occur thou-sands of kilometres apart in the Atlanticflyway, like San Antonio Oeste at Río NegroProvince in Argentina, Rio Grande do Sul andMaranhão in Brazil, and Delaware Bay in USA(Fig. 1).

The majority of adults in the Tierra del Fuegopopulation make a stopover in Delaware Bayevery May, and mix with separate populationsthat spend the non-breeding season inMaranhão in northern Brazil and Florida,respectively (Atkinson et al. 2005, Baker et al.2005). Until 2000 Red Knots and other migrantshorebirds fed almost exclusively on a super-abundant supply of eggs of spawning horse-shoe crabs (Limulus polyphemus) (Castro andMyers 1993, Tsipoura and Burger 1999),enabling them to store nutrients quickly andalmost double their body mass for the finalleg of migration to the Arctic breeding grounds.Extra stores are carried not only so that thebirds can survive poor weather or lack of foodafter arrival, which can cause high levels ofmortality (Morrison 1975, 2006, Boyd 1992),but also to enable the birds to undergo a seriesof physiological transformations from a statesuitable for migration to one for breeding(Morrison et al. 2005). Beginning in 1990 andpeaking in 1995-1996, there was a dramaticincrease in commercial fishing to provide baitfor eel and conch fisheries (Walls et al. 2002),which resulted in a six-fold decline in thenumbers of horseshoe crabs caught in surveytrawls in Delaware Bay (S. Michels, unpub-lished data; cited in Andres 2003). Since 2000,crab eggs are no longer superabundant inDelaware Bay.

Figure 1. Red Knot flyway depicted on the basis ofresightings of individuals colour-banded in Argen-tina from 1995 onwards. Black dots indicateresighting places during southern migration andwhite dots during northward migration. Key stop-over study sites are indicated (González et al., un-published data).


Several lines of evidence suggest linkagesbetween events at stopover sites in San Anto-nio Oeste and Delaware Bay and the breedinggrounds. First, studies that captured andcolour-banded northbound Red Knots (9851individuals) in Delaware Bay during each Mayfrom 1997 to 2002 showed that fewer RedKnots reached threshold departure masses of180–200 g (Baker et al. 2004). As the abundanceof crab eggs declined from 1997-1998 to 2001-2002, the predicted proportion of well-condi-tioned knots (200 g or greater) in DelawareBay near departure time on 28 May decreasedsignificantly by 70% (Baker et al. 2004). In the2–3 days before the peak departure for theArctic, mean body masses declined signifi-cantly from 183 g in 1997 to 162 g in 2002.Return rates of northbound adults caught inDelaware Bay also showed that Red Knotsknown to survive to a later year by beingrecaptured or resighted throughout the fly-way were significantly heavier at initial cap-ture than birds never seen again (Baker et al.2004). Second, emerging evidence suggeststhat northbound birds from Tierra del Fuegomay be arriving in Delaware Bay later in thespring than in earlier years, and that late birdsare increasingly delaying departure for thebreeding grounds (Baker et al. 2004). Latearrival on the breeding grounds often confersa strong reproductive disadvantage; latearrivals are predicted to have a lower prob-ability of surviving and producing offspringif they attempt to breed. Resights of colour-banded birds showed that arrival time of theTierra del Fuego birds in Delaware Bay rela-tive to the more northerly summering birdsin Florida and Maranhão have differed overtime, although in most years the former onaverage arrive later in Delaware Bay thanbirds from northern Brazil or Florida. In 2000and 2001 the highest proportion of Tierra delFuego birds occurred at or after the peak aerialcount, meaning that Florida and Maranhãobirds may have departed earlier, or there weremore late arrivals from Tierra del Fuego, orboth (Baker et al. 2004).

Fitness consequences of reduced adult sur-vival and recruitment are consistent with thealarming decline in population size of RedKnots in Tierra del Fuego from 51000 to 27000in 2000–2002 (González et al. 2004, Morrisonet al. 2004); such a rapid decline may seriouslythreaten the viability of this subspecies.

Annual survival of adult birds at DelawareBay arriving from Tierra del Fuego and north-ern South America decreased by 37% betweenMay 2000 and May 2001. In addition, annualsurvival estimated from captured and markedbirds (3644 individuals) from 1995 to 2003 inSan Antonio Oeste and in Tierra del Fuegodeclined significantly from an average of 85%in the three migration years from 1994-1995to 1997-1998 to 56% in the ensuing three-yearperiod to 2000-2001. Recruitment, as mea-sured by the proportion of second-year birds,comprised 19% of annual catches of 500–600Knots in Tierra del Fuego in 1995, 16% in 2000and 10% in 2001 (Baker et al. 2004).

In this paper we examine the role of two keystopover sites in the flyway of Calidris canutusrufa and assess the possible flow-on or dominoeffects (Piersma 1987) that can accrue after thebirds leave the austral summering sites inTierra del Fuego and migrate northwards enroute to the breeding grounds. These sites are(1) San Antonio Oeste in Argentina, the mainstopover site on the coast of Patagonia for RedKnots, where most adults undergo bodymoult into breeding plumage before under-taking long flights northwards, and (2) Dela-ware Bay in USA, the critical final springrefuelling site where they must accumulatelarge stores of nutrients before departing forthe breeding grounds in the Arctic. San Anto-nio Oeste is located at 40°45'S, 64°55'W in RíoNegro Province of Argentina, and hosts25–50% of the total population from Tierra delFuego during northward migration from lateJanuary to April (González et al. 2004). Herethe primary food for Red Knots during theday (Sitters et al. 2001) is the musselBrachidontes rodriguezi that they find on a rockyintertidal habitat locally known as “restinga”(González et al. 1996). Specifically, our objec-tives were to investigate whether habitatconditions and the timing of migration at astopover site in the southern end of the flywaymight be exacerbated by the declining foodsupplies in Delaware Bay, and the flow-onfitness consequences of decreased refuellingrates on late arriving Red Knots at thispenultimate staging site.

METHODS

We analyzed arrival time of Red Knots inDelaware Bay in relation to their banding time


in San Antonio Oeste. As part of an interna-tional research project on Red Knot popula-tions throughout the flyway, a bandingexpedition to San Antonio Oeste was orga-nized in 1998 (Baker et al. 1999, 2001, Piersmaet al. 2005), during which knots were caughtwith cannon nets in five catches on 5, 13, 16,20 and 28 March during the peak of migra-tion (n = 1000, Table 1). Age class (juvenile oradult), body mass, body moult activity on thebreast, and percentage of breeding plumagewere recorded on captured birds. In additionto a metal numbered band most knots(n = 780) were banded with standard combi-nations of two colour bands and a colouredflag to identify “time cohorts” (distinctivecombinations for 5 and 13 March, 16 and 20March, and 28 March), while 126 birds weremarked with individual schemes of orangeflag and four colour bands.

In May 1998 we compared the return ratesin Delaware Bay of birds previously colour-banded at San Antonio Oeste during the firsthalf (“early cohort”: knots colour-bandedduring 5 and 13 March) and the second half(“late cohort”: knots colour-banded during 16and 20 March) of March 1998. To keepresighting probabilities approximately equalfor the two time cohorts the sample from 28March was not included in the analysis. Threeobservers regularly carried out scans of theflocks of Red Knots at different sites on theshores of Delaware Bay in New Jersey andDelaware and recorded the numbers ofbanded individuals relative to the numbersof unbanded birds. To avoid any biases intro-duced by the visual attraction of colour-

banded birds, we made sure that all observedbirds received scores as we examined as manydifferent parts of feeding flocks as possible.We analyzed the data for each time cohortusing Binary Logistic Regression with depen-dent variable (1: banded; 0: non-banded) onindependent categorical variables (shore,observer) and day as a continuous variable.

In subsequent years from 1999 to 2003,resighting efforts of individually colour-banded adults at San Antonio Oeste wereused to estimate annual apparent survival ofthe “1998 year cohort”. The data conformedto Cormack-Jolly-Seber assumptions accord-ing to Choquet et al. (2001). Survival analyseswere run in Mark 3.2 (White and Burnham1999) using Cormack-Jolly-Seber models bycohort. Model selection was based on theAkaike Information Criterion. Binary Logis-tic Regression with logit link and sigma-restricted parameterization was used toanalyze the return rate in the six followingyears (1: seen again, 0: not seen again) fromrecapture and resighting of banded birds(n = 228) related to the presence of activebody moult, percentage of breeding plumage(categorical independent variables), bodymass and day of initial capture (continuousindependent variables).

RESULTS

Arrival times in Delaware Bay

Return rates in Delaware Bay estimated fromresightings or recaptures of both early and latecohorts of Red Knots banded in San AntonioOeste in 1998 (n = 19884) increased through

Date Juveniles Retraps With standard combination

With individual combination

Total colour marked Total catch

5 March 5 12 270 33 303 321 13 March 6 5 79 39 118 124 16 March 5 24 241 7 248 280 20 March 5 23 137 17 154 178 28 March 7 10 53 30 83 97 Total 28 74 780 126 906 1000

Table 1. Details of Red Knots catches (number of individuals) made at San Antonio Oeste, Río Negro,Argentina, in March, 1998. Retraps indicates knots banded previously in this or other expeditions. Analy-ses were based only on the 906 colour-banded birds.


the season (Day b = 0.064, SE = 0.02, P < 0.001;Fig. 2), either because birds from the un-banded Maranhão or Florida summeringpopulations were leaving or more bandedknots from San Antonio Oeste were presentat the end of the season, or both. Despite thesimilar numbers of birds banded at San Anto-nio Oeste in both time cohorts, the late cohorthad a lower return rate than the earlierbanded cohort (Fig. 2), indicating that the latecohort was on average arriving later in Dela-ware Bay, that at least some birds had notreached the bay by the end of May, or that ahigher proportion of the late cohort used sitesother than Delaware Bay, or a combination ofthese factors. Red Knots from San AntonioOeste were more represented on the shoresof Delaware than New Jersey (Shore b = 0.36,SE = 0.10, P < 0.0001), but the same trend intrue detection rates was apparent in bothstates.

Apparent survival

Because we have shown previously (Bakeret al. 2004) that a two time period model(1998-1999 to 2000-2001) was the best-fittingmodel for the Tierra del Fuego population, wecompared this model for the 1998 San AntonioOeste cohort with another that allowed a one

year lag in survival effects between theperiods 1998-2001 and 2001-2002. We also com-puted standard time dependent and constantsurvival and resighting probability models tocheck for goodness of fit. The model with theone year lag in the decline of annual survivaland with a constant resighting probability wasthe best model (Table 2A). Annual survival ofthe San Antonio Oeste 1998 cohort was esti-mated to drop from 80.3% between 1998 and2001 to 65.9% between 2001 and 2002, one yearafter the general population passing throughDelaware Bay had suffered a similar drop inannual survival (Table 2B). Although the 95%confidence intervals of the estimates of annualsurvival in the San Antonio Oeste 1998 cohortmodel before and after 2001 partly overlapbecause of the relatively small size of thecolour-banded 1998 cohort (n = 126), there isno indication of a decline in annual survivalbefore 2001.

Variables explaining return rates

The best logistic regression model for returnrates of San Antonio Oeste 1998 knots accord-ing to the Akaike Information Criterionincluded the effect of both day of initial cap-ture and presence of body moult they wereundergoing (P < 0.0001). The probability fora 1998 cohort bird to be seen in the followingyears was negatively correlated (b = -0.090,SE = 0.025) with day of initial capture(P < 0.0001), indicating that birds capturedlate in March were less likely to be seen againthan those captured in the early half of themonth. Red Knots in body moult had a higherprobability of being seen in future years thanbirds that were not moulting (b = 4.43,SE = 0.277, P < 0.0001), thereby relating thecondition of the bird to an indirect measureof survival. Although percentage of breedingplumage and body mass are indices of bodycondition and thus we would expect thatredder-plumaged and heavier birds exhibit ahigher probability of survival, these variablesare collinear (positively correlated) with dayof initial capture through the season. Thus, amodel with percentage of breeding plumageand presence of body moult showed thatredder knots had a lower likelihood of beingseen in following years (b = -0.412, SE = 0.16,P < 0.01; number of birds seen again = 57,number of birds not seen again = 171). Amodel including only body mass and presence

Figure 2. Return rates in Delaware Bay of “early”(filled circles) and “late” (open circles) cohorts ofRed Knots banded at San Antonio Oeste, RíoNegro, Argentina. The time dependent model ofthe return rate of colour-banded knots during thefirst half of March 1998 (early cohort, solid line;n = 421, b = 0.049, SE = 0.024, P < 0.043) iscompared with the model for those banded in thesecond half of March 1998 (late cohort, dashed line;n = 402, b = 0.092, SE = 0.034, P < 0.007). Numberof checked birds was 19884.


of body moult as independent variables wasnot significant for body mass because latecohort knots were heavier than early cohortbirds (128.0 ± 0.9 g, n = 122, and 123.7 ± 1.0 g,n = 106, respectively, mean ± SE; ANOVA:F1, 226 = 13.66, P < 0.0003). However, moultingbirds were heavier on average than non-moulting birds (127.2 ± 0.8 g, n = 191, and122.5 ± 1.7 g, n = 37, respectively; ANOVA:F1, 226 = 6.26, P < 0.0130). These results suggestthat later captured Red Knots stayed later atthe San Antonio Oeste stopover site to gainmass and complete the acquisition of redderbreeding plumage than did earlier capturedRed Knots.

DISCUSSION

Domino effects at stopover sites

Baker et al. (2004) argued that food suppliesat Delaware Bay, the last stopover site beforethe flight to the High Arctic breeding grounds,limited the Patagonian wintering populationof Red Knots. The new analyses presentedhere further suggest that different segmentsof the population may be differently affectedby staging site problems; in particular, the latemigration strategy adopted by some indivi-duals is now associated with greater risks of

mortality than in the past. Long-distancemigrants from the Red Knot population insouthern South America are more restrictedin their timing of migration into Delaware Baythan are northern populations. On averagethey arrive later in Delaware Bay than donortherly wintering knots as shown here forthe migration season of 1998, when conditionsin Delaware Bay were good (see also Baker etal. 2004). In the years of severe food limita-tion that occurred in Delaware Bay after 2000,we predicted that Red Knots would sufferpotentially drastic consequences on survivaland recruitment. Prior to 2000, knots refuel-ling in Delaware Bay departed en masse forthe Arctic in the period May 28–30, but as thesupply of horseshoe crab eggs was depletedin subsequent years more birds have beendelaying their departure by 7–14 days (Bakeret al. 2004, pers. obs.). A domino effectbetween the two stopover sites in San AntonioOeste and Delaware Bay has thus appearedand been exacerbated mainly by poor refuel-ling conditions in the final stopover site. Drentet al. (2003:274) emphasized the “critical roleof the final take-off site” of Pink-footed Geese(Anser brachyrhynchus) as suggested by a posi-tive relationship between en route bodycondition and subsequent breeding success.

Table 2. Apparent survival of the San Antonio Oeste 1998 cohort from Cormack-Jolly-Seber capture-recapture analysis: (A) model selection, (B) real function parameters of the best-fitting model for indi-vidually colour-banded Red Knots. AIC: Akaike Information Criterion, ϕ: apparent survival, p: probabilityof recapture or resighting, (.): constant model, (t): time dependent model, t

1: 1998–2001, t

2: 2001-2002, t

3:

1998–2000, t4: 2000–2002. Model selection based on correction for over-dispersion with c-hat = 1.509.

(A)

Model AIC c δ AIC c AIC c weights Model likelihood Number of parameters Deviance

ϕ (t1, t2) p (.) 442.3 0 0.2943 1 3 24.14 ϕ (t3, t4) p (.) 443.4 1.04 0.1747 0.59 3 25.18 ϕ (.) p (t) 443.6 1.30 0.1535 0.52 6 19.21 ϕ (.) p (.) 444.4 2.06 0.1049 0.36 2 28.25 ϕ (t) p (.) 444.4 2.11 0.1026 0.35 5 22.18 ϕ (t1, t2) p (t) 444.6 2.28 0.0943 0.32 7 18.08 ϕ (t3, t4) p (t) 445.4 3.09 0.0629 0.21 7 18.89 ϕ (t) p (t) 448.6 6.27 0.0128 0.04 9 17.81 (B)

Model Parameter Period Estimate SE 95% confidence interval

ϕ (t1, t2) p (.) ϕ 1 1998–2001 0.803 0.037 0.721–0.866 ϕ 2 2001-2002 0.659 0.112 0.420–0.838 p 1998–2002 0.508 0.045 0.421–0.595


Fitness consequences ofindividual migration strategies

The migration schedules of the australsummering population in Tierra del Fuegopotentially could have fitness consequences,as northbound knots arriving later at their firstsouthern stopover site in San Antonio Oesteon average also arrive later in Delaware Bayand thus have compressed refuelling time andlater departure for the breeding grounds.However, arrival timing in San Antonio Oestecould be related to habitat condition in Tierradel Fuego or differences in individual strate-gies of Red Knots or both, rather than to a limi-tation from poor quality stopover. This isbecause day of initial capture at San AntonioOeste does not necessarily reflect departuredate, as some earlier arrivals left in a few dayswhile others remained until the end of theseason in April, and thus late arrivals mightdepart together with some early birds (Gon-zález et al., unpublished data). The rate ofstorage of nutrients at the San Antonio Oestestopover site is around 0.5 g/day (Piersma etal. 2005), which is very low compared withthe average 4.6 g/day that knots achieve atDelaware Bay, the highest recorded amongthe world’s subspecies and staging sites(Piersma et al. 2005). Thus, birds departingfrom San Antonio Oeste in early March arelikely to have lower body mass than those thatremain until the middle of April. Birds thatare minimizing the cost of energy transportare expected to stop at all useful sites alongthe route to carry the smallest possible fuelloads (Gudmundsson et al. 1991, Alerstam andHedenström 1998); while our results suggestthat early cohort knots in San Antonio Oesteare following this general strategy, late cohortknots in contrast seems to adjust to time-selected migration, where birds should accruesubstantial fuel loads to minimize migrationtime to Delaware Bay.

These differences in individual migratorystrategies indicate why body mass could notexplain the likelihood of return rates at SanAntonio Oeste, whereas at Delaware Bay it isa significant explanatory variable. While RedKnots at Delaware Bay appear more synchro-nized in migration timing for refuelling anddepartures because the Arctic breedinggrounds are only available during a shortperiod in the year, at San Antonio Oeste Red

Knots have a broader window of time whereindividual strategies can be employed.

Apparent survival estimates for the San An-tonio Oeste 1998 cohort indicate that birds inthis cohort did not suffer the decline that theaverage adult passage population in DelawareBay did between 2000-2001, but instead had alag until one year later when they had asignificant drop in survival. We interpret thisto mean that early migrating and experiencedbirds in the San Antonio Oeste 1998 cohort(whose survivors would have been older thanthe general population in 2000-2001) were ableto avoid mortality better than the generalpopulation in Tierra del Fuego which includesyounger adult birds, and only were affectedlate in the population decline.

Role of stopover sites in population limitation

The importance of the last stopover as arefuelling site before departing for the breed-ing grounds and of late arrival has beenshown to have fitness consequences in birds(Alerstam and Hedenström 1998, Madsen2001, Drent et al. 2003, Morrison 2006).Morrison (2006) found that Calidris canutusislandica departing from their last stopover sitein Iceland in better than average conditionhad a higher probability of being seen againfollowing a series of years with difficultweather conditions in the Arctic. This showsthat being in superior condition was linkedwith higher survival; in this case conditionswere normal at the final stopover area but thebirds encountered unusually difficult condi-tions on the breeding grounds. The situationin Delaware Bay again demonstrates the linkbetween condition and survival; birds wereunable to reach suitable departure conditionbecause of a reduction in the available foodsupplies resulting in reduced survival. In theWadden Sea, reduction in food stocks forshorebirds due to overharvesting in the cocklefishery has resulted in a concomitant reduc-tion in bird numbers, providing anotherexample of how human activities can severelyimpact population sizes in migratory shore-birds (Stroud et al. 2006). Under conditions offood depletion in Delaware Bay there can bea domino effect from the timing of refuellingin southern stopover sites in South Americalike San Antonio Oeste, as birds arriving latein the USA will then be delayed further in


their departure or be underfuelled, resultingin overall lower breeding success and in-creased mortality in the population. Thisemphasizes the migratory connectivity ofpopulations of knots at these and other sitesas well as the role of individual migrationstrategies. An integrated flyway-wide approachto management and recovery is required foreffective conservation of this rapidly declin-ing population. In the absence of effectivemanagement at sites throughout the flywaywe can expect the worldwide decline in shore-bird numbers to continue, and face the grimprospect of extinction of populations orspecies at an accelerating rate.

ACKNOWLEDGEMENTS

We acknowledge financial support from theRoyal Ontario Museum Foundation and theNatural Sciences and Engineering ResearchCouncil of Canada, NOAA, US Fish and WildlifeService and the Canadian Wildlife Service. Wethank N. Garfield and B. Archer for supporting ourwork in South America, and Birders Exchange ofAmerican Birding Association for donating bi-noculars and telescopes. We thank CODEMA inRío Negro, Prefectura Naval Argentina, and theBaraschi and Echave families for providinglogistical support in San Antonio Oeste, andDNREC and NJFWS in Delaware Bay. We thankTheunis Piersma and Guy Morrison for manyhelpful suggestions which improved the manu-script, and two anonymous referees for theirconstructive comments. The authors owe a debtof gratitude to numerous researchers, volunteers,teachers and students, especially to T. Piersma, P.de Goeij, D. Price, P. Ireland, H. Sitters, M. Carbajal,G. Escudero, G. Murga, R. I. G. Morrison, R. Pissaco,L. Benegas and G. Guerrero who made it possibleto catch, process and resight knots in Argentina.

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2006 ÍNDICES 119

Índices

Volumen 21

2006

El HorneroRevista de Ornitología Neotropical

120 ÍNDICES Hornero 21

2006 ÍNDICES 121

Contenidos

Volumen 21 Número 1, Agosto 2006

Punto de vistaEscalas en ecología: su importancia para el estudio de la selección de hábitat en avesScale in ecology: its importance for the study of avian habitat selection

VÍCTOR R. CUETO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1–13

ArtículosReconstrucción de las características de historia de vida en los ancestros de los tordos: un

análisis de las adaptaciones al parasitismo de críaReconstruction of ancestral states of life-history traits in cowbirds: an analysis of adaptations to brood parasitism

E. MANUELA PUJOL Y MYRIAM E. MERMOZ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15–23Ensambles de aves en calles arboladas de tres ciudades costeras del sudeste de la provincia

de Buenos Aires, ArgentinaBird assemblages in wooded streets along three coastal cities in Southeastern Buenos Aires Province, Argentina

CARLOS M. LEVEAU Y LUCAS M. LEVEAU . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25–30Dieta del Águila Mora (Geranoaetus melanoleucus) en una transecta oeste–este en el ecotono

norpatagónicoDiet of Black-chested Buzzard-Eagle (Geranoaetus melanoleucus) in a west–east transect in the ecotone of

northern Patagonia

ANA TREJO, MARCELO KUN Y SUSANA SEIJAS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31–36El Maracaná Lomo Rojo (Primolius maracana) en Argentina: ¿de plaga a la extinción en 50 años?The Blue-winged Macaw (Primolius maracana) in Argentina: from pest to extinction in 50 years?

ALEJANDRO BODRATI, KRISTINA COCKLE, JUAN IGNACIO ARETA, GABRIEL CAPUZZI Y RODRIGO

FARIÑA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37–43

ComunicacionesReview of records and notes on King Penguin (Aptenodytes patagonicus) and Rockhopper

Penguin (Eudyptes chrysocome) in BrazilRevisión de registros y notas de Pingüino Rey (Aptenodytes patagonicus) y Pingüino Penacho Amarillo

(Eudyptes chrysocome) en Brasil

VIVIANE BARQUETE, LEANDRO BUGONI, RODOLFO P. SILVA-FILHO AND ANDRÉA C. ADORNES 45–48Confirmación de la presencia del Picaflor Tijereta (Eupetomena macroura) en ArgentinaConfirmation of the presence of the Swallow-tailed Hummingbird (Eupetomena macroura) in Argentina

JUAN CARLOS CHEBEZ, RODRIGO CASTILLO, ROBERTO GÜLLER Y CARLOS FERRARI . . . . . . . . . 49–51

LibrosUn pequeño en peligro: ecología y distribución de la Mosqueta de los Sauces (SOGGE ET AL.:

Ecology and conservation of the Willow Flycatcher)RAMÓN ALBERTO SOSA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53–56Una nueva lista de aves para Chile (MARIN: Lista comentada de las aves de Chile / Annotated

checklist of the birds of Chile)JAIME R. RAU . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56–57

Volumen 21 Número 2, Diciembre 2006

Número especial: Nuevas miradas sobre las aves migratorias americanas: técnicas, patrones,procesos y mecanismosSpecial issue: New perspectives on American migratory birds: techniques, patterns, processes andmechanisms


EditorialNuevas miradas sobre las aves migratorias americanas: técnicas, patrones, procesos

y mecanismosNew perspectives on American migratory birds: techniques, patterns, processes and mechanisms

VÍCTOR R. CUETO Y JAVIER LOPEZ DE CASENAVE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61–63

ArtículosA re-evaluation of evidence raises questions about the fasting migration hypothesis for

Swainson’s Hawk (Buteo swainsoni)Nuevas evidencias cuestionan la hipótesis del ayuno durante la migración para el Aguilucho Langostero

(Buteo swainsoni)MARC J. BECHARD, JOSE H. SARASOLA AND BRIAN WOODBRIDGE . . . . . . . . . . . . . . . . . . . . . . . 65–72Uso de isótopos estables para determinar conectividad migratoria en aves: alcances y

limitacionesUsing stable isotopes to determine migratory connectivity in birds: extent and limitations

JULIÁN TORRES DOWDALL, ADRIAN FARMER Y ENRIQUE H. BUCHER . . . . . . . . . . . . . . . . . . . . . 73–84Roosts and migrations of swallowsDormideros y migraciones de golondrinas

DAVID W. WINKLER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85–97Towards a mechanistic interpretation of bird migration in South AmericaHacia una interpretación mecanística de la migración de aves en América del Sur

ALEX E. JAHN, DOUGLAS J. LEVEY, JENNIFER E. JOHNSON, ANA MARIA MAMANI AND

SUSAN E. DAVIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99–108Annual survival of Red Knots (Calidris canutus rufa) using the San Antonio Oeste stopover

site is reduced by domino effects involving late arrival and food depletion in Delaware BayReducción de la supervivencia anual del Playero Rojizo (Calidris canutus rufa) en su escala migratoria de San

Antonio Oeste, Argentina, por efectos dominó de llegada tardía y depresión del recurso trófico en Bahía Delaware

PATRICIA M. GONZÁLEZ, ALLAN J. BAKER AND MARÍA EUGENIA ECHAVE . . . . . . . . . . . . . . . 109–117

Índices del volumen .................................................................................................................. 119–127

2006 ÍNDICES 123

Índice de organismos

Abrocoma bennetti 34Abrothryx longipilis 35Abrothryx olivaceus 35Acanthiza lineata 4Acanthizidae 94Accipitridae 93Agelaioides badius 16,18,28Agelaius cyanopus 16,18Agelaius humeralis 16,18Agelaius icterocephalus 16,18Agelaius phoeniceus 16,18Agelaius ruficapillus 16,18Agelaius thilius 16,18Agelaius tricolor 16,18Agelaius xanthomus 16,18Agelaius xanthophthalmus 16Águila Mora (véase Geranoaetus melanoleucus)Aguilucho Langostero (véase Buteo swainsoni)Alaudidae 93Alectrurus risora 62Amazona vinacea 40Amblyramphus holosericeus 16,18American Kestrel (véase Falco sparverius)Amur Falcon (véase Falco amurensis)Anatidae 15,35,93Anser brachyrhynchus 114Anser caerulescens 104Apodidae 93Aptenodytes patagonicus 45–48Apterocaulus 35Aratinga leucophthalmus 39,42Artamidae 93Aulacopalpus 35

Barn Swallow (véase Hirundo rustica)Barypus 35Black-browed Albatross (véase Diomedea melanophris)Black-capped Swallow (véase Notiochelidon pileata)Black-chested Buzzard-Eagle (véase Geranoaetus

melanoleucus)Blue-and-white Swallow (véase Notiochelidon

cyanoleuca)Blue-winged Macaw (véase Propyrrhura maracana)Bolborhinum 35Brachidontes rodriguezi 111Brachysternus 35Bubo magellanicus 36Bubo virginianus 67Buteo swainsoni 62,65–72

Calancate Ala Roja (véase Aratinga leucophthalmus)Calidris canutus 63,76,109–117Callipepla californica 35Campylopterus macrourus 49–51

Cardenal Amarillo (véase Gubernatrix cristata)Carduelis chloris 28Carpodacus mexicanus 104,105Cathartes aura 71Catharus bicknelli 81Charadrius montanus 81Chelemys macronyx 35Chionididae 94Cliff Swallow (véase Petrochelidon pyrrhonota)Cnemalobus 35Colaptes pitius 35Columba livia 27,28,30Columba picazuro 28Crypturellus tataupa 4Ctenomys haigi 35Cuculinae 15,16,22Curaeus curaeus 16,18Cylydrorhinus 35

Delichon 91Delichon urbicum 89,93Dendroica caerulescens 2,78Diomedea chlororhynchos 47Diomedea melanophris 47Dives dives 16,18

Elaenia parvirostris 9–11,106Eligmodontia morgani 35Emmalodera 35Empidonax alnorum 56Empidonax difficilis 54Empidonax minimus 2Empidonax traillii 53-56Eopsaltridae 94Epipedonota 35Erithacus rubecula 102Eudyptes chrysocome 45–48Eudyptes chrysolophus 47Euneomys 35Eupetomena macroura (= Campylopterus macrourus)Euphagus carolinus 16,18Euphagus cyanocephalus 16,18

Falco amurensis 66Falco sparverius 66Furnarius rufus 28,29

Geranoaetus melanoleucus 7,31–36Gnorimopsar chopi 16,18Gorrión (véase Passer domesticus)Great Horned Owl (véase Bubo virginianus)Grey-breasted Martin (véase Progne chalybea)Gubernatrix cristata 56Gymnomystax mexicanus 16,18,20


Hirundinidae 85–97Hirundo megaensis 93Hirundo rustica 86–95,101Hypopyrrhus pyrohypogaster 20

Icteridae 15–17Indicatoridae 15,16,22

Junco hyemalis 104,105

King Penguin (véase Aptenodytes patagonicus)

Lampropsar tanagrinus 16,20Lepus europaeus 33Limulus polyphemus 110,111Loro Maitaca (véase Pionus maximiliani)Loro Vinoso (véase Amazona vinacea)Loxodontomys micropus 35Lyncodon patagonicus 33,35

Macaroni Penguin (véase Eudyptes chrysolophus)Macroagelaius imthurni 16Macronectes giganteus 47Magellanic Penguin (véase Spheniscus magellanicus)Maracaná Lomo Rojo (véase Propyrrhura maracana)Meropidae 93Microcavia australis 35Milvago chimango 26Mimus saturninus 28,29Molothrus aeneus 16,18Molothrus ater 16,18,21,55,61Molothrus badius (= Agelaioides badius)Molothrus bonariensis 16,18,21,28Molothrus oryzivorus 16,18Molothrus rufoaxillaris 16,18,21Mosqueta Boreal (véase Empidonax alnorum)Mosqueta de los Sauces (véase Empidonax traillii)Muscicapidae 93Myiarchus swainsoni 101

Neomorphinae 15,16,22Nesopsar nigerrimus 16Northern Rough-winged Swallow (véase Stelgidopteryx

serripennis)Notiochelidon cyanoleuca 87Notiochelidon pileata 87,93Nyctelia rotundipennis 35Nyctopetus 35

Octodon degu 34Oligoryzomys longicaudatus 35Oreopsar bolivianus 16Oryctolagus cuniculus 33Ovis aries 33,35

Pappipapus 35Parula pitiayumi 7,9–11Passer domesticus 27–30,77,80Patagona gigas 49Pernis apivoris 66Petrochelidon fulva 92Petrochelidon pyrrhonota 90–92Petrochelidon rufocollaris 92Petroicidae 94

Phrygilus 35Phyllotis xanthopygus 35Picaflor Cometa (véase Sappho sparganura)Picaflor Corona Violácea (véase Thalurania glaucopis)Picaflor Gigante (véase Patagona gigas)Picaflor Tijereta (véase Campylopterus macrourus)Pingüino Penacho Amarillo (véase Eudyptes chrysocome)Pingüino Rey (véase Aptenodytes patagonicus)Pionus maximiliani 42Pitangus sulphuratus 28Plathestes 35Playero Rojizo (véase Calidris canutus)Ploceidae 15,16Podicipedidae 35Polioptila dumicola 9–11Primolius maracana (= Propyrrhura maracana)Progne 86,87Progne chalybea 28,90Progne subis 63,90–92Propyrrhura maracana 37–43Pseudoleistes guirahuro 16,18Pseudoleistes virescens 16,18Psittacidae 35Pteroptochos tarnii 35Purple Martin (véase Progne subis)Pyrocephalus rubinus 105

Quiscalus 16–22Quiscalus lugubris 16,18Quiscalus major 16,18Quiscalus mexicanus 16,18Quiscalus niger 16,18Quiscalus quiscula 16,18

Red Knot (véase Calidris canutus)Reithrodon auritus 35Riparia 89Riparia paludicola 92Riparia riparia 87,90–92Rockhopper Penguin (véase Eudyptes chrysocome)Ryephenes 35

Sand Martin (véase Riparia riparia)Sappho sparganura 49Scaphidura oryzivora (= Molothrus oryzivorus)Sericoides 35Serpophaga subcristata 9–11,28Setophaga ruticilla 2,78,101Southern Giant-Petrel (= Common Giant-Petrel;

véase Macronectes giganteus)Southern Rough-winged Swallow (véase Stelgidopteryx

ruficollis)Spheniscus magellanicus 47Stelgidopteryx 86,92Stelgidopteryx ruficollis 87Stelgidopteryx serripennis 87,90,91Sturnella loyca 35Swainson’s Hawks (véase Buteo swainsoni)Swallow-tailed Hummingbird (véase Campylopterus

macrourus)Sylviidae 93

2006 ÍNDICES 125

Tachycineta 92Tachycineta albiventer 87Tachycineta bicolor 63,86,91,94,95Tachycineta cyaneoviridis 93Tachycineta euchrysea 93Tachycineta leucorrhoa 28,87Tachycineta meyeni 87Tachycineta stolzmanni 93Thalurania glaucopis 49Thinocoridae 94Thylamys 35Timaliidae 93Tree Swallow (véase Tachycineta bicolor)Troglodytes musculus 28Troglodytidae 93Tucúquere (véase Bubo magellanicus)Turdus rufiventris 28

Turkey Vulture (véase Cathartes aura)Tyrannidae 35,93Tyrannus 99–108Tyrannus albogularis 100Tyrannus melancholicus 28,100,103Tyrannus savana 100,103

Vanellus chilensis 35Vidua 16,22

Western Honey-buzzard (véase Pernis apivoris)White-winged Swallow (véase Tachycineta albiventer)

Xanthopsar flavus 16,18

Yellow-nosed Albatross (véase Diomedea chlororhynchos)

Zaedyus pichiy 35Zenaida auriculata 27–30,35Zonotrichia capensis 28


Índice de Autores

Adornes AC 45–48Areta JI 37–43Baker AJ 109–117Barquete V 45–48Bechard MJ 65–72Bodrati A 37–43Bucher EH 73–84Bugoni L 45–48Capuzzi G 37–43Castillo R 49–51Chebez JC 49–51Cockle K 37–43Cueto VR 1–13,61–63Davis SE 99–108Echave ME 109–117Fariña R 37–43Farmer A 73–84Ferrari C 49–51González PM 109–117Güller R 49–51

Jahn AE 99–108Johnson JE 99–108Kun M 31–36Leveau CM 25–30Leveau LM 25–30Levey DJ 99–108Lopez de Casenave J 61–63Mamani AM 99–108Mermoz ME 15–23Pujol EM 15–23Rau JR 56–57Sarasola JH 65–72Seijas S 31–36Silva-Filho RP 45–48Sosa RA 53–56Torres Dowdall J 73–84Trejo A 31–36Winkler DW 85–97Woodbridge B 65–72

2006 ÍNDICES 127

Revisores

El equipo editorial de El Hornero agradece a los colegas que han evaluado los manuscritos enviados a larevista. Su labor desinteresada permite mantener el rigor y la relevancia en los artículos publicados.Abajo está la lista completa de los revisores que actuaron en este volumen.

Sara BertelliKeith L. BildsteinPedro BlendingerMaría Susana BóEnrique BucherElizabeth Chang ReissigJuan Carlos ChebezLuis ChiappeCharles DeemingMario DíazAlejandro G. Di GiacomoRussell GreenbergCristián HernándezSantiago ImbertiJuan Pablo IsacchJaime E. JiménezJennifer JohnsonLeo JosephJack Kirkley

Bettina MahlerMónica MartellaViviana MassoniR. I. Guy MorrisonJorge NoriegaFábio OlmosJuan Francisco OrnelasUlyses PardiñasMark PearmanGuillermo E. PérezRicardo Rodríguez EstrellaKevin R. RussellAdrián SchiaviniSusan K. SkagenRoberto J. StraneckJuan Carlos Torres-MuraAlejandro TravainiMaría Elena ZaccagniniSergio M. Zalba

el hornero - biblioteca digital exactas · 2018-01-08 · el hornero revista de ornitología...

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