1

INDICE I. AGRADECIMIENTOS…………………………..………………. 3 II. ESTRUCTURA DE LA TESIS…………………………………. 5 III. INTRODUCCIÓN GENERAL………………..……………….. 6

III.1. Descripción y distribución de la especie…………………………… 6

III.2. Importancia ecológica…..……………………………………........... 8

III.3. Tendencia de sus poblaciones……………………………………… 8

III.4. Factores implicados en la disminución de las poblaciones………10

III.5. El papel de las enfermedades………………..………………………13

III.6. Las repoblaciones como herramienta de gestión……………….... 15

III.7. Bibliografía……………..……………………………………………... 18

IV. OBJETIVOS……………………………………………………………… 26

V. CAPITULO 1…………………………………………………………….. 29 Las repoblaciones con aves de granja como focos de introducción de nuevos parásitos en las poblaciones silvestres de perdiz roja.

Effect of red-legged partridge management in parasite comunities.

European Journal of Wildlife Research. Villanúa, D., Pérez-Rodríguez,

L., Casas, F., Alzaga, V., Acevedo, P. and Gortázar, C. En evaluación.

VI. CAPITULO 2…………………………………………………………… 45 Variaciones en el resultado de los análisis coprológicos preventivos actuales en función del tipo de heces analizadas y de la hora de recogida de las mismas.

2

Avoiding bias in parasite excretion estimates: the effect of sampling time

and type of faeces. Villanúa, D., Pérez-Rodríguez, L, Gortázar, C., Höfle,

U. & Viñuela, J. (2006). Parasitology,133: 251-259.

VII. CAPITULO 3………………………………………………………….. 65 Efectividad de los tratamientos antiparasitarios como método para prevenir la introducción de nematodos en el campo.

How effective is pre-release nematode control in farm reared red-legged

partridges (Alectoris rufa)?. Villanúa, D., Pérez-Rodríguez, L, Rodríguez,

O., Viñuela, J. & Gortázar C (2006). Journal of Helmithology, 81(1): 101-

103.

VIII. CAPITULO 4……………………………………………...………….. 73 Posible transmisión de nematodos propios perdices de granja a especies amenazadas.

First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. A

negative effect of red-legged partridge Alectoris rufa releases on steppe

bird conservation?. Villanúa, D., Casas, F., Viñuela, J., Gortázar, C.,

García de la Morena, E.L. & Morales, M.B. (2007). Ibis (in press) doi:

10.1111/j.1474-919x.2006.00620.x

IX. CAPITULO 5……………………………………………………………. 77 Factores limitantes de la abundancia estival de perdiz roja en Aragón. Posibles alternativas a las repoblaciones con aves de granja.

Factors affecting summer densities of the red-legged partridge in Spain.

Ibis. Villanúa, D., Acevedo, P., Escudero, M.A., Marco, J. and Gortázar,

C. (En evaluación).

X. SÍNTESIS…...……………………………………………………….....… 100

XI. CONCLUSIONES, PERSPECTIVAS Y REFLEXIONES..… 107

3

I. AGRADECIMIENTOS

II. ESTRUCTURA DE LA TESIS

La presente Tesis Doctoral está dividida en Introducción, Objetivos, una

serie de capítulos (1-5), una Síntesis general y una Conclusiones finales,

Perspectivas y Reflexiones. En la introducción, en castellano, se revisan los

antecedentes y el contexto teórico del tema. A continuación se exponen los

objetivos de la Tesis, a desarrollar en los siguientes capítulos. Cada uno de

estos capítulos reproduce el texto íntegro, en inglés, de manuscritos enviados

para su publicación en revistas científicas internacionales (indicándose si es un

manuscrito enviado, aceptado o ya publicado y su referencia). Previamente a

dicho texto en inglés, en cada capítulo se presenta un resumen en castellano.

Finalmente, en la Síntesis General, también en castellano, se discuten los

resultados más relevantes de cada capítulo y se enuncian las principales

Conclusiones, Perspectivas de trabajo y Reflexiones que se extraen de la

presente tesis.

4

III. INTRODUCCIÓN GENERAL

III.1. Descripción y distribución de la especie

La perdiz roja (Alectoris rufa) es una galliforme de entre 300 y 500 gramos,

de aspecto compacto y hábitos gregarios fuera de la temporada de

reproducción. Su coloración se compone de tonos castaños en el dorso,

obispillo y pecho gris azulado, vientre canela y plumas costales con un

característico diseño formado por una banda blanca, una negra y una marrón.

La cara es de un color blanco y está enmarcada por un collar negro que se

inicia en el pico, atraviesa el ojo y se prolonga hasta la garganta formando un

babero. La parte inferior de este collar se prolonga por el lateral del cuello y

parte del pecho en forma de pequeñas listas negras no presentes en el resto

de especies del género alectoris. Tanto el pico como la carúncula ocular y las

patas son de un rojo vivo, que da nombre a la especie.

La gran plasticidad ecológica que presenta la perdiz roja le ha permitido

ocupar multitud de hábitats diferentes, desde el nivel del mar hasta los prados

alpinos por encima de los 2.000 metros (Mullarney et al. 2001). No obstante, el

hábitat ideal para la especie lo constituyen las llanuras cerealistas con

alternancia de otros cultivos, como viñas u olivares, y campos en barbecho y en

la que se haya mantenido la distribución en parcelas de pequeño tamaño que

posibilite la conservación de márgenes de vegetación natural (Cheylan 1976,

Garcia et al. 1983, Lartiges & Mallet 1983, Berger 1984, 1987, Gaudin & Ricci

1987, Lucio & Purroy 1987, Birkan, 1990, Lucio 1991, Reudet 1992, Blanco-

Aguiar et al. 2003). Estas peculiaridades se cumplen en la zona centro-sur de

la Península Ibérica, donde se alcanzan las mayores densidades para la

especie (Blanco Aguiar et al. 2003).

Dentro del género Alectoris se incluyen otras 6 especies más (A.magna, A.

melanocephala, A.philbyi, A. graeca, A. chukar, y A. barbara) distribuidas a lo

largo del paleártico occidental (Cramp & Simmons 1980)(Figura 1). La

distribución natural de la perdiz roja abarca ocupa la mayor parte de la

península Ibérica, sur de Francia y una pequeña franja del noroeste de Italia

(Mullarney et al. 2001). A esta distribución natural hay que añadir la población

5

del este de Inglaterra, originada a partir de unas primeras sueltas de perdices

francesas en 1.770 (Tapper 1992) y mantenida, probablemente, gracias al

continuo aporte de aves de granja (Tapper 1999).

Tradicionalmente se han diferenciado tres subespecies de perdiz roja: A.

rufa rufa, A. r. hispanica y A. r. intercedens. La primera de ellas distribuida por

el sur de Francia y norte de Italia, así como en las poblaciones introducidas del

Reino Unido; la segunda, ocuparía la franja noroeste de la Península Ibérica,

constituida por Cataluña, Aragón, Navarra, País Vasco, Cantabria, Asturias,

Galicia, Castilla León y el norte de Extremadura; y la tercera y última

subespecie, sería la presente en el resto del área de distribución (McGowan

1994, Díaz et al. 1996).

Figura 1. Distribución de las distintas especies del género Alectoris tomado de

Cramp & Simmons (1980).

6

III.2. Importancia ecológica y socioeconómica. El mediano tamaño y la abundancia de esta especie, hacen que alrededor

de 40 especies de predadores la incluyan en su dieta (Yanes et al. 1998),

constituyendo, junto con el conejo de monte, la dieta de especies tan

amenazadas como el lince ibérico (Lynx pardina) o el águila imperial (Aquila

adalberti) (Delibes & Hiraldo 1981, Calderón, 1983). A este papel como presa

de especies amenazadas hay que añadir el papel que desempeña la perdiz

como “especie paraguas” para los ecosistemas agrícolas tradicionales, unos de

los más amenazados en la actualidad (De la Concha et al, 2006), ya que

algunas de las mejoras del hábitat realizadas por el colectivo de cazadores

para la perdiz tiene un efecto muy positivo sobre otras especies vinculadas a

este tipo hábitat tales como el sisón (Tetrax tetrax) o las poblaciones de

alaudidios (De la Concha et al, 2006). Por último hay que considerar también

gran importancia que tiene por sí misma la conservación de la perdiz roja al

tratarse de una de las especies más típicas y emblemáticas de los ambientes

mediterráneos de la Península Ibérica, punto de origen de la especie y casi

reducto exclusivo de sus poblaciones naturales (Cramp and Simmons, 1980).

A este indudable valor ecológico y conservacionista hay que añadir la gran

importancia económica y social que la caza de esta especie tiene en la

península Ibérica. Esta práctica constituye una de las actividades económicas

más importantes en multitud de áreas rurales de nuestro país (APROCA 1998;

Lucio 1998; Bernabeu 2000) y tiene un arraigo cultural y social único (Delibes

1963, 1988). A modo de ejemplo cabe señalar que en la provincia de Ciudad

Real, se ha estimado que la caza de esta especie genera más de 200 millones

de euros anuales (Otero, 1995).

III.3. Tendencia de sus poblaciones.

Las poblaciones de perdiz roja parecen estar sufriendo una marcada

regresión en las últimas décadas (Cramp and Simmons, 1980). Este descenso

ha sido registrado tanto en su área de distribución natural en Francia (ONC

1986), Italia (Baratti et al 2005) y península Ibérica (Rueda et al 1992, Borralho

et al. 1998, Lucio 1998, Blanco Aguiar et al 2003), como en la población

introducida en el Reino Unido (Aebischer and Potts 1994). Esta marcada

7

tendencia, unida a su limitado área de distribución, ha hecho que la perdiz roja

esté considerada actualmente como especie de estatus “Vulnerable” a nivel

mundial (Aebischer and Potts 1994) y haya sido declarada SPEC 2 por Bird Life

International (Tucker and Heath, 1994).

Centrándonos en los trabajos acerca de la evolución de sus poblaciones

en la Península Ibérica, hay que hacer referencia al fuerte descenso registrado

por Antonio Lucio para el caso de Castilla y León (Lucio, 1998). Este autor

encuentra, para un periodo de menos de 20 años, una disminución superior al

70 % en las tablas de caza, pasando de una media de 12 perdices capturadas

por kilómetro cuadrado a finales de los 70 a tan solo 2 en los 90 (Lucio 1998).

En el mismo sentido van los datos demográficos más recientes, obtenidos

mediante el censo por parte de voluntarios de SEO/Birdlife en el programa

SACRE, que sugieren una reducción demográfica del 20 % entre 1996 y 2001

(Blanco Aguiar et al. 2003; Figura 2). Paradójicamente, las estadísticas oficiales

de caza sugieren una notable recuperación en las capturas a partir de

mediados de los 90, que parecen tender a estabilizarse en torno a los 3.5

millones anuales (Baragaño & Otero 2001; Figura 2). No obstante, hay que

tener en cuenta que anualmente se liberan al campo más de 3 millones de

perdices criadas en granja (Millán et al. 2003), de manera que esta aparente

recuperación en las tablas de caza podría ser tan sólo el reflejo de tales

sueltas.

Figura 2. Tendencias recientes en el número de perdices cazadas anualmente (Anuarios

Nacionales les de Estadística Agraria) y de la abundancia de perdiz en los mismos años

(resultados programa SACRE, Sociedad Española de Ornitología)

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8

III.4. Factores implicados en la caída de las poblaciones.

En una población natural, en la que no se llevasen a cabo sueltas de aves

de granja, la abundancia de una población de perdices estaría condicionada

por el aporte anual de nuevos individuos con la reproducción y la extracción de

ejemplares con la depredación, las enfermedades o la actividad cinegética. Así

pues, la disminución de las poblaciones de perdiz durante los últimos años

debería estar motivada por la alteración de alguno de estos parámetros.

III.4.1. Descenso de los parámetros reproductivos

De lo descrito en el punto II se deduce que el papel que la perdiz roja

desempeña en el ecosistema es el de presa, lo que implica que, de manera

natural, va a estar sujeta a numerosas pérdidas de efectivos. Este hecho hace

que el éxito reproductivo sea especialmente importante en esta especie, ya que

con él debe compensar las numerosas bajas naturales (Lebreton, 1982). Así

pues, cualquier causa que pueda limitar la capacidad reproductora de una

población de perdices puede desequilibrar de manera decisiva el sensible

cociente producción / extracción.

Una de las causas de fallo reproductivo más frecuente en galliformes es la

depredación tanto de huevos y pollos, como de adultos incubando (Rands

1988, Yanes et al. 1998). La perdiz roja no es una excepción, tal y como

confirman los trabajos de radio-seguimiento realizados en Francia por Ricci et

al. (1990) y Leonanrd y Reitz (1998). En estos estudios se confirma un alto

porcentaje de pérdida de nidadas (de un 61% y 59% respectivamente), debidas

principalmente a la depredación (>90%). Esta alta tasa de depredación tiene

mucho que ver con las preferencias de la especie a la hora de ubicar el nido.

Así pues, la perdiz roja selecciona para nidificar linderos, setos o bordes de

cultivo (Rands, 1986 a, Ricci et al 1990) en lugar de las manchas más espesas

de matorral, donde su éxito podría ser mayor (Carvalho y Borralho, 1998).

Estas estructuras son peores a la hora de asegurar el éxito reproductivo por

varios motivos; por una parte, se trata de estructuras lineales donde la tasa

natural de depredación es mayor (Angelstam, 1986) y por otra son formaciones

susceptibles de ser modificadas a lo largo del año por las prácticas agrícolas

(Duarte y Vargas, 2002).

9

Esta estrecha relación existente entre productividad de la perdiz y

agricultura es considerado por multitud de autores como uno de los puntos

clave del descenso de las poblaciones (Potts 1980; Lartiges y Mallet, 1983;

Rands, 1987; Pepin y Blayac, 1990; Nadal et al., 1996; Crick et al., 1994;

Aebischer y Kavanagh, 1997; Lucio, 1998, Borralho et al., 2000; Gortázar et al,

2002a) ya que, durante los últimos años, se ha llevado a cabo una

transformación radical de las prácticas agrícolas, coincidente en el tiempo con

la caída de las poblaciones de perdiz. Las concentraciones parcelarias

efectuadas en gran parte del territorio han simplificado enormemente el hábitat

agrícola, implantando el monocultivo y reduciendo a la mínima expresión los

márgenes necesarios para la ubicación de los nidos y para la protección

necesaria frente a depredadores. Además, los recientes avances tecnológicos

han permitido reducir el tiempo requerido para realizar las distintas labores, a la

vez que se han desarrollado variedades de cultivo de ciclo más corto. Con

estas modificaciones, el impacto sobre las especies ligadas al medio agrícola

es mucho mayor, sobre todo durante la cosecha, ya que, en el momento en

que ésta se lleva a cabo, muchas puestas están todavía sin eclosionar, lo que

origina su pérdida por la acción directa de las labores agrícolas (Crick et al.

1994, Green 1995).

III.4.2. Incremento de la pérdida directa de ejemplares

Dentro de este apartado podemos distinguir tres causas diferentes por las

cuales una población de perdices puede “peder ejemplares”, y estas son la

depredación, la caza y las enfermedades. Dentro de la primera podemos

nuevamente hacer una separación entre la depredación sobre adultos y sobre

pollos, que no se hace semejante hasta los 2-3 meses de edad (Hudson and

Rands, 1988).

Pues bien, en lo concerniente a factores que puedan afectar a la

depredación sobre pollos nos encontramos, además de con los descritos

anteriormente para a pérdida de nidos, con el papel que juega la disponibilidad

de insectos, base de la dieta de los pollos de perdiz en los primeros días de

vida (Rueda et al., 1993). Teniendo esto en cuenta, es lógico pensar que

cuanto menos disponibilidad de insectos haya en esos primeros días de vida, el

esfuerzo de búsqueda deberá ser mayor, lo que implica más desplazamientos y

10

por lo tanto más probabilidades de ser detectado por los depredadores. Esta

hipótesis es la barajada por diversos autores que encuentran una relación

significativa del descenso del éxito reproductivo de la aves ligadas al medio

agrícola con el uso de insecticidas (Rands 1986 b, Potts 1986, Campbell et al.

1997, Brickle et al. 2000) o con aquellas variaciones climáticas capaces

también de disminuir la disponibilidad puntual de insectos (Lucio, 1990).

Transcurrida esta primera etapa, las distintas polladas de perdiz se

agrupan formando bandos de mayor tamaño, que ofrecen una mayor

probabilidad de supervivencia ante el frío y la lluvia, y aumenta la capacidad de

vigilancia frente a depredadores (Putaala et al., 1995). A partir de este

momento la depredación pierde protagonismo como causa de muerte de la

perdiz, lugar que pasa a ocupar la caza (Duarte y Vargas, 2002).

La caza, entendida como la extracción racional de los excedentes de unos

recursos renovables que serían las poblaciones de fauna silvestre no tendría

por qué suponer un riesgo para la conservación de dichas especies, ya que,

como se dice en su propia definición, sólo se extraerían los excedentes (Ley

4/1989, de 27 de marzo, de la Conservación de los Espacios Naturales y de la

Flora y Fauna Silvestres). Sin embargo de todos es conocido el caso de la

paloma migratoria (Ectoistes migratorius), la cual, a pesar de ser considerada

como el ave más abundante del mundo llegó a extinguirse por su caza

indiscriminada (Dorst, 1971). Así pues, parece evidente que la actividad

cinegética puede ser capaz de mermar las poblaciones de las especies

cinegéticas si no se gestiona correctamente.

En el caso de la perdiz roja, numerosos autores han considerado la

sobreexplotación cinegética de la especie como uno de los principales

responsables del descenso de las poblaciones (Potts, 1986; Pepin y Blavac,

1990; Lucio y Purroy, 1992; Borralho et al 1997). Un ejemplo cercano es el de

Portugal, donde, a raíz de la Revolución de los Claveles, la gran mayoría de la

superficie del país se convirtió en terreno libre de caza. Esta situación produjo

una clara sobrecaza de las poblaciones de esta especie, que la llevó a una

situación crítica (Borralho et al. 1997). Desde 1988 una nueva ley promovió el

establecimiento de cotos sociales o privados, así como incentivos para la

gestión y mantenimiento de caza sostenible en estos acotados. Desde dicha

fecha, se fueron estableciendo progresivamente los acotados, y en 1996

11

alrededor del 30 % de la superficie del país se encontraba ya dentro de esa

figura (Borralho et al. 1997). Esta nueva situación legal probablemente ha

permitido una recuperación parcial de las poblaciones portuguesas de perdiz

en los últimos años (Borrahlo et al. 1997, 2000).

III.5.El papel de las enfermedades.

A pesar de que hasta hace relativamente pocos años no se había prestado

demasiada atención al papel de las enfermedades en las especies silvestres,

estas pueden suponer un importante problema para la conservación y gestión

de la fauna. Basta con recordar el efecto que dos enfermedades víricas, la

mixomatosis y la enfermedad vírica hemorrágica, han tenido sobre las

poblaciones de conejo de la península (Muñoz-Goyanes, 1960; Villafuerte et al

1994); e, indirectamente, sobre las de sus depredadores (Moreno y Villafuerte,

1995; Villafuerte et al 1998), para comprender como una enfermedad puede

llevar a una especie al borde de la extinción.

En lo concerniente al papel de las enfermedades com limitantes de las

poblaciones de aves, destacan los trabajos realizados con el nematodo

Trichostrongylus tenuis y el Lagópodo escocés (Lagopus lagopus scoticus). Ya

en 1963, Jenkins et al. encontraban que los lagópodos con mayor intensidad de

infección por este parásito mostraban un menor éxito reproductivo, aunque no

llegaban a aclarar si el parásito era la causa de esta menor tasa reproductiva o

si, por el contrario, el aumento de la intensidad de parasitación era tan sólo una

consecuencia más de otro factor desconocido. Posteriormente, Potts et al.

(1984), profundizaron un poco más en el conocimiento de la relación existente

entre T. tenuis y el Lagópodo escocés, llegando a la conclusión de que dicho

nematodo estaba íntimamente relacionado con los ciclos de abundancia que

mostraba esta tetraónida, aunque nuevamente, no concluyen si el parásito es

la causa, y hacen hincapié en la necesidad de llevar a cabo trabajos de

desparasitación experimental que permitan confirmar si T. tenuis es realmente

el causante. Esta línea de trabajo fue la seguida por Hudson et al., los cuales

consiguieron demostrar mediante desparasitaciones experimentales en el

campo que las aves desparasitadas mostraban, por una parte, un mayor

tamaño de puesta y un mayor número de pollos que alcanzaban la edad de 6

12

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semanas (Hudson, 1986) y por otra, una menor detectabilidad por los

depredadores terrestres (Hudson et al.,1992), lo cual permitía confirmar la

influencia de este parásito en los ciclos de abundancia del lagópodo (Hudson et

al., 1998)(Ver figura 3).

Figura 3. Ciclos de abundancia del Lagópodo escocés (Lagopus lagopus escoticus) causados

por el nematodo Trichostrongylus tenuis. Modificado de Hudson et al., 1998.

Estos trabajos ponen de manifiesto la capacidad de un patógeno para

mermar una población de aves mediante la reducción de su capacidad

reproductiva y un aumento de la depredación de aves adultas, pero existen

también casos en los que la propia enfermedad es capaz de causar un número

alto de bajas y suponer un factor limitante para la población. A modo de

ejemplo cabe citar varios casos recientes y ocurridos en la península Ibérica; el

brote de Tricomoniasis (Trichomonas gallinae) descrito en paloma torcaz

(Columba palumbus) en el sur de la península, en el cual se produjo la muerte

de más de 2.000 aves (un 15% del total de la población) un apenas unos días

(Höfle et al 2004) o el de viruela aviar (Avipoxvirus) en una población de perdiz

roja del sur de la península ibérica, donde encontraban más de un 40% de aves

afectadas (Gortázar et al.,2002b).

13

Queda patente pues el hecho de que las enfermedades son uno de los

factores a tener en cuenta a la hora de analizar las causas de regresión de una

especie.

III.6.Las repoblaciones como herramienta de gestión.

A pesar de la caída de las poblaciones de perdiz roja, la presión que se

ejerce sobre esta especie no ha descendido, sino que ha aumentado

espectacularmente durante los años 60 y 70 y de manera más suave pero

continua durante las últimas décadas (Vargas y Duarte, 2002). Para satisfacer

esta creciente demanda, que supera con mucho la capacidad de producción de

las mermadas poblaciones naturales, muchos gestores o propietarios de

terrenos cinegéticos han optado por la suelta de aves criadas de granja.

Este tipo de actuación se ha generalizado de tal manera que, a día de hoy,

se estima que son más de 3 millones las perdices de granja liberadas

anualmente en nuestro país (Tejedor et al. 1999, Gortázar et al. 2000,

Baragaño y Otero 2001, Millán et al 2003). Si tenemos en cuenta los datos de

las estadísticas oficiales de caza que, como se comentó anteriormente, cifran

en torno a los 3.5 millones las perdices capturadas anualmente (Baragaño &

Otero 2001), podemos darnos cuenta de la importancia alcanzada por las

sueltas de aves de granja en la actualidad.

III.6.1. Viabilidad de las repoblaciones

La viabilidad de las repoblaciones con aves de granja con fines cinegéticos

es en general muy baja e incapaz de recuperar las poblaciones silvestres

(Hessler et al.,1970; Birkan, 1971; Leránoz y Castien, 1989; Dowell, 1992;

Robertson, 1988; Brittas et al., 1992; Sodeikat et al., 1995; Capelo y Pereira,

1996; Gortázar et al., 2000; Millán et al., 2002; Pérez et al., 2004; Alonso et al.,

2005).

En la mayoría de los trabajos científicos en los que se ha evaluado la

supervivencia y las causas de muerte de las aves liberadas se ha llegado a la

conclusión de que el zorro es el principal responsable del fracaso de las

mismas (Papeschi et al., 1993; Gortázar et al., 2000; Millán et al. 2003).

Múltiples factores tales como la falta de comportamiento antipredatorio debido

14

al crecimiento en cautividad (Csermely et al.,1983) o el efecto de los parásitos

(Millán et al. 2002) favorecen el alto grado de predación por parte de este

carnívoro. Por otra parte, una repoblación supone la presencia una alto número

de presas débiles en un área relativamente pequeña, condiciones óptimas para

que se dé el fenómeno conocido como “predación múltiple” ó “síndrome del

gallinero” (Short et al. 2002). Este fenómeno se define como la muerte de

presas a un ritmo mucho mayor de lo que un carnívoro puede consumir en

determinado momento (Kruuk, 1972), y es frecuente en carnívoros oportunistas

como el zorro (Dowell, 1992).

Además del efecto de los depredadores, las perdices criadas en granja

presentan un menor desarrollo de su trato digestivo y corazón (Millán et al.,

2001), lo cual condicionaría notablemente tanto su capacidad para asimilar los

recursos alimentarios presentes en el campo como su capacidad de vuelo y por

lo tanto de huída.

Por último hay que tener en cuenta que las perdices en granja están

expuestas a una serie de parásitos que, como se ha demostrado en trabajos

previos, son diferentes a los presentes en las poblaciones naturales (Millán et

al., 2003, 2004). Pues bien, la liberación al campo de estas aves supone; por

una parte el cese de los tratamientos sanitarios que controlaban a los

patógenos propios de la granja, y por otra, la exposición a nuevos patógenos

para los que no habrían tenido contacto previo. Si a esto añadimos la

inmunodepresión causada por el estrés de la suelta, parece lógico pensar que

la capacidad de respuesta de las aves de granja frente a las enfermedades va

a ser muy baja, y que este va a ser un factor muy importante a la hora de

mermar la supervivencia de las aves liberadas (Villanúa et al., 2006).

III.6.2. Riesgos asociados. Si, como se comentaba en el punto anterior, las diferencias existentes entre

los parásitos propios de granja y los del campo pueden suponer un riesgo para

la viabilidad de las repoblaciones, lo mismo podemos pensar a la inversa, de

manera que la liberación de aves parasitadas al campo podría suponer un

grave riesgo para las poblaciones silvestres. De hecho, la posible transmisión

de enfermedades de los animales liberados a las poblaciones silvestres es uno

de los puntos más importantes a la hora de valorar la idoneidad de un

15

programa de repoblación (Viggers et al., 1993). Trabajos previos llevados a

cabo por Millán et al. (2003, 2004) mostraron como la parasitofauna de las

perdices de granja era totalmente diferente de la que aparecía en las

poblaciones silvestres. Así, las aves de granja aparecían parasitadas por

especies monoxenas, es decir, de ciclo directo; mientras que en las silvestres

se identificaban parásitos heteroxenos, esto es, de ciclo indirecto. Estas

diferencias se explicarían por el hecho de que, en las condiciones de granja,

las perdices no van a tener acceso a los invertebrados necesarios para cerrar

los ciclos de las especies de parásito heteroxenas y viceversa, la menor

agregación existente en el campo, va a dificultar la transmisión de las especies

monoxenas. Teniendo en cuenta estas diferencias, Millán et al., (2003, 2004)

sugerían el grave riesgo que la liberación de aves parasitadas al campo podría

tener para las poblaciones silvestres, ya que estarían introduciendo unos

nuevos patógenos con los que no habrían tenido contacto previo y para los

cuales es de esperar que tuviesen una mayor susceptibilidad.

Un ejemplo lo tenemos en el caso de las sueltas de faisán (Phasianus

colchicus) y el descenso de las poblaciones naturales de perdiz pardilla (Perdix

perdix) en el Reino Unido. Los estudios llevados a cabo por Tompkins et al

(1999, 2000, 2001) demostraban cómo el nematodo intestinal Heterakis

gallinarum tenían un efecto muy negativo sobre la condición física de la perdiz

pardilla, mientras que resultaba prácticamente apatógeno para el faisán. Con

estos resultados planteaban la posible competencia entre el faisán y la perdiz

pardilla aparentemente mediada por este parásito y probablemente

responsable, al menos en parte, del importante descenso sufrido por las

poblaciones de perdiz del Reino Unido durante las últimas décadas (Tompkins

et al., 1999, 2000, 2001). Así pues, si trasladamos estas hipótesis a nuestro

caso, la liberación masiva de perdices de granja podría, lejos de solucionar la

caída de las poblaciones naturales de la especie, estar añadiendo un nuevo

problema a su conservación.

A este problema sanitario hay que añadir otro no menos importante, como

es el de la contaminación genética. A pesar de estar terminantemente prohibido

por la ley, se han venido empleando para repoblar híbridos entre perdiz roja y

perdiz chukar (Alectoris chukar), debido a su elevada productividad en

cautividad (Padrós, 1991), y a que en su segunda generación son

16

prácticamente indistinguibles por rasgos externos de la auténtica perdiz roja

(Negro et al., 2001; Millán et al. 2001). Esta práctica se ha generalizado de tal

manera que a día de hoy resulta difícil encontrar poblaciones silvestres puras y

mucho menos granjas sin contaminación genética (Dávila, 2005). Así pues nos

encontramos con que, por una parte, la mayoría de las granjas de perdiz están

contaminadas genéticamente, y por otra, apenas tenemos poblaciones

naturales puras de las que pudiesen nutrirse las granjas para poder conseguir

ejemplares puros que utilizar en las repoblaciones.

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24

IV. OBJETIVOS La presente Tesis Doctoral ha sido concebida bajo un enfoque

eminentemente práctico, tratando de responder a las dudas de carácter

sanitario que se le plantearían a cualquier persona interesada en la

conservación de la perdiz roja y que barajase la posibilidad de recurrir a

las sueltas de aves de granja como herramienta para recuperar las

poblaciones naturales.

La primera pregunta sería probablemente la siguiente: ¿Qué

riesgos sanitarios podría tener la liberación de las perdices criadas en

cautividad? Mediante el estudio parasitológico de las perdices cazadas

en varias fincas con distintos modelos de gestión, se trata de constatar o

desmentir la introducción de nuevos parásitos en el medio mediante la

repoblación con perdiz roja con fines cinegéticos. Este objetivo se

desarrolla en el capitulo 1.

En caso de demostrase que realmente las aves liberadas pueden

introducir nuevos parásitos en el campo, una de las posibles soluciones

sería la de la de liberar aves que no estuviesen infectadas. Para ello

deberíamos contar con un método seguro que nos permitiese identificar

a las aves parasitadas, lo cual nos plantearía la siguiente pregunta:

¿Son los controles llevados acabo actualmente en las granjas de perdiz

roja suficientemente eficaces como para evitar esta introducción de

parásitos? Para responder a esta pregunta se ha realizado una

experiencia controlada donde se comparan los resultados de los análisis

coprológicos realizados a las mismas aves a distintas horas del día y con

distintos tipos de heces, con el fin de detectar los posibles fallos del

método de control seguido en la actualidad para descartar la presencia

de parásitos en las explotaciones de perdiz. Este objetivo se desarrolla

en el capitulo 2.

Si los controles actuales fuesen insuficientes para garantizar que

las aves liberadas no son portadoras de parásitos, el siguiente paso

sería el de plantear el tratamiento de todas las aves antes de la suelta

para así asegurarnos de que llegasen al campo desparasitadas. Esta

actuación nos plantearía la siguiente pregunta: ¿Son los tratamientos

25

antiparasitarios actuales suficientemente eficaces en la perdiz roja como

para evitar la introducción de parásitos en el campo? Nuevamente se ha

diseñado un experimento controlado con el que poder evaluar la

efectividad del Albendazol, uno de los antihelmínticos más frecuentes en

las granjas de perdiz, como tratamiento frente a Aonchoteca caudinflata

y Heterakis gallinarum, dos de los nematodos más frecuentes en las

perdices de granja pero ausentes en las poblaciones silvestres. Este

objetivo se desarrolla en el capitulo 3.

En caso de demostrar que los tratamientos actuales no son

suficientemente eficaces, cabría la posibilidad de que se planteasen las

sueltas de estas aves en fincas donde no quedasen poblaciones viables

de perdiz natural, donde no existiría por tanto el riesgo de contagio de

estas con sus congéneres de granja. En este caso, la pregunta que se

nos plantearía sería la siguiente: ¿Podrían las sueltas de perdices tener

consecuencias negativas sobre el estado sanitario de otras especies

silvestres? Mediante el caso práctico de un sisón (Tetrax tetrax)

capturado en una zona donde anualmente se liberan miles de perdices

de granja, se trata de demostrar el riesgo que estas repoblaciones

podrían tener para otras especies. Este objetivo se desarrolla en el

capitulo 4.

Por último, y tras haber obtenido unos resultados que

desaconsejasen la repoblación con perdiz de granja, se nos plantearía la

gran duda; si las repoblaciones no son adecuadas ¿Existe alguna salida

para recuperar la perdiz roja? Para responder a esta cuestión se

analizan los datos obtenido en un seguimiento a largo plazo de las

abundancias de perdiz en Aragón, tratando de identificar los factores que

podrían estar causando el descenso de las poblaciones, con el fin de

poder atajar el problema desde su inicio, sin tener que recurrir a la

liberación de aves criadas en granja. Este objetivo se desarrolla en el

capitulo 5.

Así pues, los objetivos de la presente tesis se podrían resumir en

las siguientes preguntas:

26

IV.1. ¿Son realmente las repoblaciones con aves de granja un foco de introducción de nuevos parásitos en las poblaciones silvestres de perdiz roja?

IV.2. ¿Son los controles llevados acabo actualmente en las granjas de perdiz roja suficientemente eficaces como para evitar esta introducción de parásitos?

IV.3. ¿Son los tratamientos antiparasitarios actuales suficientemente eficaces en la perdiz roja como para evitar la introducción de parásitos en el campo?

IV.4. ¿Podrían las sueltas de perdices tener consecuencias negativas sobre el estado sanitario de las especies protegidas?

IV.5. ¿Existen otras salidas para recuperar la perdiz roja?

27

V. CAPITULO 1

Las repoblaciones con aves de granja como focos de introducción de nuevos parásitos en las poblaciones silvestres de perdiz roja.

Effect of red-legged partridge management in parasite comunities.

European Journal of Wildlife Research. Villanúa, D., Pérez-Rodríguez,

L., Casas, F., Alzaga, V., Acevedo, P. and Gortázar, C. En evaluación.

RESUMEN

Se ha estudiado la parasitofauna y la condición física de 99 perdices roja

(Alectoris rufa) cazadas en Ciudad Real (zona centro de España). Cuarenta y

seis de ellas procedían de dos fincas de caza donde anualmente se lleva a

cabo la suelta de un importante número de perdices de granja. Las cincuenta y

tres restantes fueron muestreadas en fincas naturales en las que no se realizan

repoblaciones con aves de granja y de localización próxima a las fincas con

suelta.

En total se identificaron cuatro especies de nemátodos (Heterakis

gallinarum, Aonchoteca caudinflata, Eucoleus contortus and Cheilospirura

gruveli) y dos de cestodos (Raillietina (R.) tetragona and Skryabinia bolivari).

Las fincas con suelta presentaron una mayor diversidad de especies de

parásitos, con mayores prevalencias e intensidades de parasitación para todos

los helmintos encontrados.

Tres de estas especies son típicas de aves criadas en granja y dos de

ellas, A. caundinflata y S. bolivari, fueron encontradas parasitando aves

adultas, lo cual pone de manifiesto la introducción de estos helmintos en la

población natural reproductora.

Las aves muestreadas en las fincas naturals mostraron una condición

física major que la de las de la zona con sueltas, pero esta relación no está

relacionada con la infección con parásitos.

Los resultados obtenidos sugieren que la suelta de aves de granja,

práctica cada vez más común en los cotos de caza españoles, puede suponer

28

un riesgo para la conservación de la poblaciones naturales, ya que se estarían

introduciendo nuevos patógenos al medio. Sin embargo, los resultados

sugieren también que, a día de hoy, el simple cese de las sueltas podría tal vez

suficiente para evitar la incorporación de dichos patógenos al medio.

ABSTRACT We studied the helminth community and body condition of 99 hunter

harvested red-legged partridges (Alectoris rufa) from Ciudad Real (Central

Spain). Forty six were sampled in two game estates where an important number

of farm-reared red-legged partridges are released yearly. The remaining 53

were obtained from natural wild populations adjacent to one of the estates with

releases. Four nematode species (Heterakis gallinarum, Aonchoteca

caudinflata, Eucoleus contortus and Cheilospirura gruveli) and two cestode

species (Raillietina (R.) tetragona and Skryabinia bolivari) were identified. The

managed areas showed higher parasite diversity, with higher prevalences and

intensities for all helminths found. Three of these species were typical of farm-

bred partridges and two of these, A. caundinflata and S. bolivari, were found

parasitizing adult partridges. This suggests introduction of these helminths into

the breeding population of managed states. The birds sampled in the non-

managed estates showed a better body condition, but no relation with parasite

infection was found. Our results suggest that the release of farm reared red-

legged partridges, a strategy that is becoming a common practice in Spanish

hunting areas, poses risk to wild populations because of introducing parasites.

However, these results also suggest that simply stopping releases may be a

good way to remove locally those parasites from populations.

KEYWORDS: Alectoris rufa, condition, helminths, restocking, Spain

INTRODUCTION

The red-legged partridge (Alectoris rufa) is the most abundant game bird

in the Iberian Peninsula, and its hunting is one of the most important

economical and social activities in central Spain (Bernabeu 2000). During the

last decades, natural populations of this game bird have declined in most of its

distribution range (Aebischer and Potts 1994). In Spain, only declines have

29

been documented (Gortázar et al. 2002, and references therein). The strategy

of many hunting estate managers to overcome this decline has been releasing

farm reared birds.

Previous studies evidenced differences between the parasites found in

farmed and those found in wild red-legged partridges (e.g. Millán et al. 2004a).

Regarding helminths, monoxenous species were more abundant in farms and

heteroxenous parasites in natural populations (Millán et al. 2004b, 2004c).

These differences can negatively affect autochthonous populations in the

managed areas, due to the probably limited previous contact with these

pathogens. In fact, potential disease transmission from released animals to wild

populations is one of the most important points to be considered in restocking

programs (Viggers et al. 1993). As an example, the annual release of farmed

ring necked pheasants (Phasianus colchicus) in the United Kingdom is believed

to maintain or even increase Heterakis gallinarum burdens in the wild pheasant

population (Draycott et al. 2000), which in turn could be one of the factors

involved in the grey partridge Perdix perdix decline (Tompkins et al. 2001).

However, the survival of released red-legged partridges is low (see Birkan

1977; Capelo and Pereira 1996; Gortázar et al. 2000; Duarte and Vargas 2004),

and this could be limiting pathogen transmission between farmed and wild birds.

Thus, the aim of the present study was to confirm if parasites could be

effectively introduced into the field by farm reared red-legged partridge

releases.

MATERIAL AND METHODS Study area

The study was performed in four game estates, ranging from 1009 Ha. to

3145 Ha., located in Ciudad Real (Central Spain, 30T, X419903/Y 4313925).

Habitat is characterized by undulated farmland of wheat and barley crops with

olive trees and vineyard patches. Most cereals are cultured by a traditional two-

year rotation system.

The red-legged partridge is the most important game species in these

hunting areas, although other game species like the Iberian hare (Lepus

granatensis) or the feral pigeon (Columba livia) are present. The red fox (Vulpes

vulpes) is the most abundant predator, but feral cats (Felis catus) and dogs

30

(Canis familiaris), montagu´s harrier (Circus pygargus), marsh harrier (Circus

aeruginosus), buzzards (Buteo buteo) and golden eagle (Aquila chrysaetos) can

prey on red-legged partridges. Moreover, the study area holds important

populations of several species of steppe birds, such as great bustard (Otis

tarda), little bustard (Tetrax tetrax), pin-tailed sandgrouse (Pterocles orientalis),

or stone curlew (Burhinus oedicnemus).

Two of the sampled game estates followed an intensive management

model with more than 2,000 farm reared partridges released yearly. The other

two consisted of wild populations where no restocking with captive-bred game-

birds was performed in the last ten years, and that were adjacent to one of the

managed states.

Study animals

A total of 99 hunter-harvested red-legged partridges were sampled, 46

from the managed areas and 53 from the wild populations. All birds were

weighed using a 1000 g Pesola® precision balance (±5 grams) and left tarsus

length was measured using a caliper (±0.01 mm). All measures were taken by

the same person (LPR). Sex and age were determined in the field according to

the morphological description of Sáenz de Buruaga et al. (2001), but were

confirmed by examination of the gonads and the bursa of Fabricius. We tried to

obtain a sex- and age-ratio next to 50% in our sample.

Partridge body condition was estimated using two different

measurements: the pectoral muscle thickness (PMT), measured using a

portable ultrasonic meter (Krautkramer USM 22 device) (Pérez-Rodríguez et al.

2006) and the residuals of the regression of the body mass on the cube of

tarsus length (RBMTL)(Andersson 1992).

Laboratory methods

The digestive tract was opened longitudinally, and the content was

collected for parasite isolation. The digestive tract was soaked overnight in

water to allow the liberation of any parasite that could be attached to the

mucosa. The liver was cut into 3 mm slices and put into water to allow the visual

inspection for trematodes. The samples obtained were examined by means of a

stereomicroscope and the detected worms were counted and stored in 70 %

31

ethanol before identification. The identification of the parasites was done

according to López-Neyra (1947), Skryabin (1991) and Melhorn et al. (1992).

Statistical analysis

We used Mann-Whitney’s U test to evaluate the influence of

management (natural versus restocking), sex and age on parasite diversity,

parasite burdens, and body condition; and Chi2 tests to evaluate the influence of

these factors on parasite prevalence. The possible relationship between the

parasite burdens and body condition was tested with Spearman’s correlation

test.

RESULTS Four nematode species (Heterakis gallinarum, Aonchoteca caudinflata,

Eucoleus contortus and Cheilospirura gruveli) and two cestode species

(Raillietina (R.) tetragona and Skryabinia bolivari) were identified. No

trematodes were detected.

Heterakis gallinarum, Cheilospirura gruveli and Raillietina (R.) tetragona

were found in both different management strategies. Aonchoteca caudinflata

Eucoleus contortus and Skryabinia bolivari were only found in the managed

areas. Helminth diversity was significantly higher in the managed areas

(0.38±0.58 species per host) than in the natural ones (0.06±0.23)(Z=-3.53;

p<0.001).

In the case of parasites found in both management models, their

prevalence was higher in the managed areas, but these differences reached the

significance level only in the case of H. gallinarum (Table 1). The intensities of

these parasites followed the same trend (Figure 1), but in this case the

significance level was reached by H. gallinarum and Ch. gruveli (Table 2).

No relationships were found between parasite burdens and the two body

condition indexes pectoral muscle thickness, PMT, and regression residuals of

the body mass on the cube of tarsus length, RBMTL (Spearman correlation

tests, rs-0.31 - 0.28, p>0.05). PMT was higher in the wild populations (26.5±2.4

mm) than in the managed areas (24.3±3.1 mm)(Figure 2), but this difference

was only significant in the case of juvenile males (Table 3). No differences were

found in the RBMTL.

32

DISCUSSION

All parasite species found in our study have been previously described

parasitizing the red-legged partridge (López-Neyra 1947; Carvalho-Varela and

Ferradeira 1997; Cordero del Campillo and Rojo 1999; Calvete et al. 2003;

Millán et al. 2004a, 2004b).

The species richness detected in this study (6 species in the managed

area and only 3 in the natural one) is lower than those reported in two previous

large- scale studies (13 different species by Calvete et al. 2003; or 14 different

species by Millán et al. 2004a), but similar to the richness reported by Millán et

al. (2004c) in a small study area in southern Spain (4 species). However,

prevalences and abundances are markedly lower than those reported in these

studies.

Millán et al. (2004a, 2004b) found that the parasite community in wild

populations of red-legged partridges was different from that of farm-bred birds.

They suggested that new parasites could be introduced into the field with the

release of farm-reared birds. Three species identified in our study, Heterakis

gallinarum, Cheilospirura gruveli and Raillietina (R.) tetragona, are usually

found in natural populations (López-Neyra 1947; Tarazona et al. 1979; Millán et

al. 2004b, 2004c). However, the other three ones (Eucoleus contortus,

Aonchoteca caundinflata and Skryabinia bolivari), are more usually found in

farm-reared birds (see Millán et al. 2004a). These were found in our study

parasitizing birds sampled in the managed areas only.

Furthermore, two of these species were found in adult birds in our study.

Partridges released for hunting are usually juveniles. Thus, the presence of

these parasites in adult birds suggests: a) that there had been a transmission

from farmed to wild birds; b) that we found birds released in the previous year

that had kept the infection for a whole year; or c) that some adult birds were

released. Releasing of farm-bred birds had occurred two months before the

samples for this study were taken. This implies that the partridges parasitized

by these helminths must be birds that survived in the field for two months, or

even wild birds. Any of these hypotheses are consistent with the introduction of

these parasites into the field through releases of their farm-bred hosts.

33

The transmission of parasites from released partridges to wild birds could

be facilitated by an increased parasite excretion after releasing, as

experimentally shown in the case of the pheasant (Villanúa et al. 2006a). This in

turn could be due to the absence of antiparasite treatment and the stress

immunodepression that follows releasing into an unknown habitat.

The introduction of new pathogens into a wild population can be an

important conservation problem because natural populations could have lower

resistance to a pathogen to which they have had no previous contact (Newton

1998). In our study area, some endangered steppe birds share habitat with the

red-legged partridge. So, the introduction of new non-specific parasites

supposes an additional problem for their conservation (Villanúa et al. 2007a).

The detection of higher parasite burdens in the managed areas in this

study could be an indicator of the low effectiveness of the preventive measures

to reduce parasites in the released animals. Current preventive measures

applied prior to the release of farm-reared game birds (if they exist) are based

on: i) a coprological analysis performed in faeces collected in the aviary soil,

and ii) antiparasite treatment following the same protocol that is used in the

case of poultry (Villanúa et al. 2007b). The first point of this protocol has the

problem that there are a lot of factors such as host reproductive status (Ruíz de

Ybañez et al. 2004), weather (Vicente et al. 2005), season (Kumba et al. 2003),

random day-to-day variations (Giver et al. 2000), phase of the parasitic infection

(Giver et al. 2000), or hour of sampling (Villanúa et al. 2006b), that can modify

propagule excretion, and are not always considered. In addition, the

effectiveness of antiparasite protocols in game species is insufficient to prevent

introducing parasites into the field as recently shown in the case of Albendazole

treatment against Aonchoteca caudinflata and H. gallinarum in red-legged

partridges (Villanúa et al. 2007b).

If the preventive protocols are not enough to eliminate the parasites from

the released birds, the other option taken is antiparasite treatments

administered in the field. Previous studies evaluated the effect of administering

anthelminthic drugs in the field together with the supplementary food

(Woodburn et al. 2002; Draycott and Sage 2005). These authors found that the

birds given anthelmintic treatment and supplementary food had significantly

lower worm burdens and increased their productivity. Nevertheless, some

34

authors think that treatment of free-living birds is not practical (Cole 1999) and

the pros and cons of the administration of drugs to wild birds have to be

considered carefully, taking ethical and public health concerns into account

(Höfle et al. 2004).

On the other hand, we must remark that the two sampled game states

with wild partridges were adjacent to one of the managed states. Thus, our

results indicate that wild partridge populations have lower parasite diversity,

prevalence and burdens that adjacent populations where thousands of farm-

bred partridges are released yearly, that is, that the transmission of parasites

form farmed birds to wild birds is relatively limited to the hunting lands were

releases are performed, but may not affect so much neighbour populations.

This may be due to natural factors (poor dispersal ability of partridges in

general, or of farmed birds in particular) or to management actions

(maintenance of released partridges within the boundaries of game states by

pursuing them, or intense hunting removing most released partridges before

they may disperse). In any case, this result suggests that when releases are

interrupted in a given hunting land, the problem of parasite transmission may be

largely avoided. In fact, this may be the main reason explaining why when

sampling wild and released populations in Spain we still find differences in

parasite communities, albeit millions of partridges have been released during

last decades all over Spain.

As we have shown, lower body condition found in juvenile partridges

from the managed areas was not apparently related with parasites. It can be

explained by two different causes: a) a deficient muscle development caused by

the farm-rearing (in case a significant part of the juvenile birds sampled in these

areas were farm-reared partridges); or b) the effect of other pathogens such as

bacteria or viruses, that may equally be introduced along with released birds.

However, more specific studies are needed to test this hypothesis.

In conclusion, the present study supports the initial hypothesis that

hunting estates with partridge releases are introducing helminth parasites into

the ecosystem. Thus, improved controls are necessary to prevent associated

risks for sustainable game management and conservation.

ACKNOWLEDGEMENTS

35

The authors thank S. J. Luna, E. Biescas, M.P. Martín and E. Chico for their

assistance in the field, and P. Talavera for help in the lab. This is a contribution

to the joint project CSIC/Principado de Asturias, and to CYCIT projects MCYT-

REN200307851/GLO and CGL2004-02568/BOS. Lorenzo Pérez-Rodríguez

had a FPU grant from the Spanish Ministerio de Educación y Ciencia and

Fabián Casas from Junta de Comunidades de Castilla-La Mancha.

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36. Woodburn, M., Sage, R.B. & Carroll, J.P. (2002) The efficacy of a

technique to control parasitic worm burden in pheasants (Phaisanus

colchicus) in the wild. Zeitschrift für Jagdwissenschaft, 48: 364-372

39

Table 1. Helminth prevalences found in red-legged partridges from two different

management models and significance level of the differences (Chi2 test).

Wild (n=53) Managed (n=45) Mean p

Heterakis gallinarum 3.77 % 17.39 % 5.01 <0.05

Aonchoteca caudinflata 0 % 6.52 % 3.56 ns

Eucoleus contortus 0 % 2.17 % 1.16 ns

Cheilospirura gruveli 1.89 % 10.87 % 3.49 ns

Raillietina tetragona 3.77 % 6.66 % 0.42 ns

Skryabinia bolivari 0 % 4.44 % 2.4 ns

Table 2. Helminth burdens found in red-legged partridges from the two different

management models and significance level of their differences by the Mann-

Whiney U test.

Wild (n=53) Managed (n=45)

Mean min-max SD Mean min-max SD F p

Heterakis gallinarum 0.04 0-1 0,19 0.36 0-5 0.93 -1,22 <0.05

Aonchoteca caudinflata 0.00 0 0,00 0.18 0-3 0.68 -1,89 ns

Eucoleus contortus 0.00 0 0,00 0.04 0-2 0.30 -1,08 ns

Cheilospirura gruveli 0.13 0-7 0,96 1.89 0-30 6.82 -2,17 <0.05

Raillietina tetragona 0.13 0-4 0,68 0.40 0-8 1.61 -0,67 ns

Skryabinia bolivari 0.00 0 0,00 0.91 0-30 4.72 -1,54 ns

40

Table 3. Mann-Whiney U test results for the body condition indexes (pectoral

muscle thickness, PMT, and regression residuals of the body mass on the cube

of tarsus length, RBMTL) found in the different age and sex groups in two

different management models.

RBMTL PMT Males Females Males Females

z p z p z p z p

Adult -0.71 ns -1.84 ns 1.60 ns 0.52 ns

Juvenile 0.10 ns 2.01 ns 2.40 < 0.05 1.65 < 0,1

41

Figure 1. Parasite burdens of the species present in the two different

management models (Cheilospirura gruveli, Heterakis gallinarum and Raillietina

tetragona).

-6

-4

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ruve

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42

Figure 2. Body condition in the two different management models measured

with the regression residuals of the body mass on the cube of tarsus length

(RBMTL) and the pectoral muscle thickness (PMT).

-30

-20

-10

0

10

20

30

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MTL

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43

VI. CAPITULO 2

Variaciones en el resultado de los análisis coprológicos preventivos actuales en función del tipo de heces analizadas y la hora de recogida de las mismas.

Avoiding bias in parasite excretion estimates: the effect of sampling time

and type of faeces. Villanúa, D., Pérez-Rodríguez, L, Gortázar, C., Höfle,

U. & Viñuela, J. (2006). Parasitology,133: 251-259

RESUMEN 1- El creciente interés de los ecólogos en las relaciones parásito-

hospedador hace que hayan proliferado los estudios en los que se recurre a

diferentes métodos con los que estimar el grado de parasitación. En el caso de

los parásitos intestinales, el método más utilizado es la cuantificación de

propágulos parasitarios en heces mediante técnicas coprológicas. Sin

embargo, la excreción parasitaria puede verse influenciada por numeros

factores tanto endógenos como exógenos. La identificación de estos factores

es imprescindible para obtener resultados correctos.

2- En el presente estudio, se analiza el efecto de la hora de recogida de

las heces en el resultado del análisis coprológico cuantitativo para dos

parásitos intestinales, Aonchoteca caudinflata y Eimeria sp., presentes en la

perdiz roja (Alectoris rufa). Además, se evalúan también las posibles

diferencias existentes en el conteo de parásitos en heces corrientes y en heces

procedentes de los ciegos.

3- En Octubre de 2004, ocho perdices rojas fueron separadas durante un

brote de capilariasis en una población de granja. Tras confirmar la infección por

capilarias en todas las aves y por coccidios en seis de ellas, se inició un

protocolo de recogida de heces de manera individual en cuatro momentos del

día y durante un periodo de tiempo de varios días.

4-Se pudo detectar una importante variación en los valores del análisis

coprológico de ambos parásitos en función de la hora de recogida, con un claro

y constante incremento de la excreción conforme avanzaba el día. El día de

recogida influyó de manera significativa en los dos casos, así como su

44

interacción con el individuo en el caso de la excreción de capilaria. Además, los

propágulos de capilaria fueron más abundantes en las heces de intestino,

mientras que en el caso de los coccidios el patrón fue el opuesto, con mayor

recuento de ooquistes en las heces de ciego.

5-Nuestros resultados muestran que la hora del día en que se recoge la

muestra de heces afecta drásticamente al resultado. De ahí que sea necesario

estandarizar la hora de recogida de la muestra para evitar errores. De manera

similar, en el caso de especies con ciegos muy desarrollados, se debe tener en

cuenta el tipo de heces recogidas (a poder ser del tramo donde el parásito sea

más abundante), con el fin de obtener los resultados correctos.

6-Por último, en este trabajo se pone de manifiesto la necesidad de

profundizar en el conocimiento acerca del sistema parástio-hospedador, con el

objetivo de desarrollar un protocolo de muestras adecuado que permita obtener

datos más fiables.

ABSTRACT

1-The interest of ecologists on host-parasite relationships has lead to an

increasing number of studies involving indirect methods of parasite burden

estimation. With regards to intestinal parasites, the most widely employed

method is the quantification of parasite propagules in faeces. However, parasite

excretion in faeces may be subjected to a certain degree of variation due to

endogenous or exogenous factors. The identification of those influencing factors

is required to obtain reliable results.

2-In this paper we analyse the effect of the hour of the day at which

samples are collected in propagule counts of two intestinal parasites infecting

the red-legged partridge: the capillarid nematode Aonchoteca caudinflata and

coccidia of the genus Eimeria. Also, we tests whether there are differences in

propagule counts between caecal and intestinal faeces.

3-In October 2004, eight red-legged partridges were isolated during an

outbreak of capillariasis in a captive population. After confirming the capillarid

infection in these eigth individuals and coccidian infection in six out of them,

individual faecal samples were daily collected at four different hours during

several days.

45

4-Hour of the day exerted a very strong effect in propagule counts,

excretion of both types of parasites showing a clear and constant increase from

dawn to dusk. Day of sampling affected significantly in both cases and

interacted significantly with the individual in the case of capillarid eggs. Also,

capillarid eggs were more abundant in intestinal than in caecal faeces, whereas

the inverse pattern was found for coccidian oocysts.

5-Our results show that hour of the day at which samples are collected

can drastically affect parasite excretion estimates. Standardization of the hour

of sample collection or statistical control of this variable is therefore

recommendable to prevent this bias. Similarly, in the case of bird species with

long caeca, consistent collection of one type of faeces (ideally that one where

propagules are most abundant) may avoid important errors in parasite burden

estimates.

6-Finally, this study stresses the importance of gathering more

information about the studied host-parasite system in order to develop adequate

sampling methods leading to obtain more reliable data.

KEYWORDS: Alectoris rufa, Aonchoteca caudinflata, Eimeria, nematoda,

coccidia

INTRODUCTION

In the last two decades the interest of behavioral ecologists in the effect

of parasites on host fitness has increased. Parasites may affect host body

condition (Hall 1985; Gulland 1995; Delahay et al 1995), survival probabilities

(Vorísek et al. 1998; Murray et al. 1997), some reproductive parameters (Newey

&Thirgood 2004; Albon et al. 2002) or population dynamics (Holmes 1982;

Hudson et al. 1998; Tompkins et al. 2001). Therefore, parasites seem to be an

important factor in host life-history and may exert a strong selective force on

host evolution (Clayton & Moore 1997).

This relatively recent focus on host-parasite interaction has lead to an

increasing number of ecological empirical studies in which parasite load is

related to different measures of host fitness. It uses to be relatively easy to

determine the prevalence and intensity of ectoparasite infection as they can be

46

directly counted or estimated by exploring the skin, hair or feathers of the

individual. In contrast, determining the level of infection by endoparasites is

more difficult, especially when the study requires the individual to remain in

perfect conditions after sampling. Regarding intestinal endoparasites, the most

common approach to solve this problem is to estimate prevalence and intensity

of the infection by the analysis of faecal samples and the quantification of

parasite propagules, typically eggs or larvae (Gordon & Whitlock 1939; Shaw &

Moss 1989; Guyatt & Bundy 1993). However, propagule counts in faeces may

be subjected to a great within-individual variation due to factors like host

reproductive status (Ruiz de Ybañez et al. 2004), weather (Rickard &

Zimmerman 1992; Vicente et al. 2005), season of the year (Shaw & Moss 1989;

Theodoropoulos et al. 1998; Kumba et al. 2003), random day-to-day variations

(Yu et al. 1998; Giver et al, 2000; Utzinger et al. 2001), phase of the parasitic

infection (Giver et al. 2000; Cordero del Campillo et al. 1999) or hour of the day

(Boughton 1933; Brawner & Hill 1999). For example, Brawner & Hill (1999)

showed that a single factor such as hour of the day at which samples are

collected can drastically alter the results of assessment of coccidian prevalence

and individual parasite burden in the house finch (Carpodacus mexicanus).

Therefore, accurate determination of the effect of these variables on

propagule excretion is essential for a correct assessment of parasitic infection

and for a successful testing of the hypothesis studied. Unfortunately, despite the

remarked relevance of knowing the effects of these factors, no accurate

information is available for host-parasite systems with little medical or veterinary

importance, that are precisely the more studied by behavioural and evolutionary

biologists.

In this paper we analyse the day-to-day and daily variation in the

excretion of parasite propagules in red-legged partridges (Alectoris rufa L.)

naturally infected with two different intestinal parasites: coccidia of the genus

Eimeria and the capillarid nematode Aonchoteca caudinflata. Eimeria coccidia

exhibit both sexual and asexual phases in their life cycle. The asexual phase

may occur in the intestinal epithelium or as a diffuse infection in several other

organs. The sexual phase takes place only in the epithelium of the intestine or

intestinal caeca (depending of the species) and results in the production of

oocysts that are elimininated in the faeces of the host (Cordero del Campillo et

47

al. 1999). A. caundinflata is an heteroxenous parasite of the small intestine of

gallinaceus and anatid birds (Anderson 2000). Female worms lay eggs that

mature after ingestion by earthworms (Allobophora caliginosa, Eisenia foetida),

the necessary intermediate hosts.

In many avian taxa, like Galliforms and Anseriforms, intestinal caeca are

specially elongated. In these species, caecal faeces represent a significant

proportion of the total amount of faeces produced and can be easily

distinguished from intestinal faeces by their appearance. In this paper we also

analyse the differences in propagule content of both kinds of faeces in the red-

legged partridge. We finally discuss the implications of our results in the design

of and data analysis of empirical studies involving parasite estimation from

faecal counts.

MATERIAL AND METHODS Data collection took place during October 2004 in the experimental red-

legged partridge farm of the IREC in Ciudad Real (Spain). During late summer-

autumn of that year there was an outbreak of capillariasis in one of the outdoor

aviaries of the farm. As soon as the parasite was identified and before starting

any medication, a sample of 15 birds of the affected aviary was isolated in

individual outdoor elevated cages and individual samples of feces were

collected. The coprological analysis showed that eight of the birds (six females

and two males) were infected by capillarids and these were subsequently

employed for the experiment. Also, six of them were infected by coccidia,

allowing the combined analysis of the daily variation of excretion of both

parasites in the same sample of birds.

During the days 5th, 6th, 12th, 13th, 14th, 15th and 16th of October individual

faecal samples were collected from all birds (except from one of them the day

14th due to an error of sampling) at 08:00, 12:00, 16:00 and 19: 30 hours.

Faecal samples were obtained by placing a large piece of fresh paper on the

ground just below each one of the cages slightly before the designated times

The first droppings produced by each bird during the following 30 minutes were

collected and stored in Eppendorf tubes. Most of the faeces obtained were

intestinal faeces, which is the most common type of faeces produced by

Galliforms. However, when caecal faeces where also found at sampling times,

48

they were collected separately allowing a posterior comparison. Caecal faeces

can be easily and unambiguously distinguished from intestinal faeces by their

colour (dark brown in the former, green-pale brown in the later), texture (soft

and homogeneous in the former, granular in the later) and by the much more

intense odour of caecal faeces.

Quantitative analysis of the parasite propagules (oocysts in the case of

coccidia, eggs in the case of capillarids) present in each faecal sample were

carried out by flotation in a known volume of saturated SO4Zn solution and

counting in MacMaster chambers (Melhorn et al. 1992). The concentration of

oocysts and capillarid eggs was finally referred to the weight of the faecal

sample analysed, obtaining the number of propagules per gram of faeces.

It should be noted that no any capillarid nematode can be identified up to

the species level just by observing its eggs. Therefore, at the end of the

experiment birds were sacrificed as a part of another experiment and adult

worms were identified according to Skryabin (1991), confirming the presence of

Aonchoteca caudinflata.

Statistical analysis

We employed General Linear Mixed Models (GLMMs) for the analysis of

the effect of sampling time on oocyst and capillarid egg counts. As parasite

propagule counts were normally distributed after log10+1 transformation, we

used normal distribution of errors and an identity link function (GLMMs macro of

SAS, Littell et al. 1996). Capillarid eggs or coccidian oocysts (after the cited

transformation) were introduced as dependent variables in the models. Day and

hour of the day (nested in day) were introduced as categorical factors and the

individual was considered in the model as a random variable. As day-to-day

variations in propagule excretion may be caused by endogenous factors, the

effect of this variable could differ for each bird. Therefore, the interaction

between day and individual was also entered in the model as a fixed factor.

Propagule excretion may vary in the time due to changes in the degree of

infection of the individual. Therefore, to minimize the effect of this on our

analysis of day-to-day variation we restricted our analysis to data from the five

consecutive days (12 th to 16 th).

49

However, as the analysis revealed an effect of the day in the models for

capillarids and coccidia (see results) two further GLMMs were performed in

order to assess whether there was a common tendency during the five

consecutive days previously analysed. In both models the number of

propagules (either capillarid eggs or coccidian oocysts) per gram of faeces

(after log10+1 transformation) excreted at 19: 30 hours of each day was entered

as dependent variable whereas day -as a continuous variable- and the

interaction between day and individual were entered as fixed factors. The

individual was again entered as a random factor.

To test for differences between caecal and intestinal faeces, propagule

content of caecal and intestinal faecal samples collected at the same hour of

the same day from each bird were compared by means of Wilcoxon Matched

Pairs Tests (raw data were employed in this analysis because the larger

number of zero values in this data set made impossible data normalization).

RESULTS Effect of the time of the day and day-to-day variation on propagule excretion

GLIMMs results for capillarid eggs and coccidian oocysts are shown in

Table 1. In the case of capillarid egg excretion the hour of the day at which

samples where collected was the most important factor, explaining the 42.17 %

of the deviance of the model.

Capillarid egg shedding followed the same temporal pattern in all birds,

showing a clear and constant increase from dawn to dusk that was repeated

during all the days of sampling (Fig. 1). In fact, the amount of capillarid eggs in

faeces was on average 27.4±14.2 times higher in samples collected at 19: 30

than in those samples collected at 8:00 from the same birds.

Day of sampling also exerted a significant effect (explaining a 7.6% of the

deviance). As can be observed in Fig. 1, in some individuals (e.g. bird 54, bird

59) the line signalling the daily pattern for some days was almost five times

higher than for other days, showing a strong day-to-day variation. In contrast,

such day-to-day variation was minimal in other individuals (e.g. bird 61, bird 72).

Consequently, the deviance explained in the final model was greater for the

interaction between day and individual (27.5%) than for day as a single factor,

suggesting that day-to day-variation in capillarid egg excretion followed a

50

particular pattern for each bird. To assess whether such effect of the day of

sampling indicated a common tendency during the five consecutive days of

study we analysed the amount of propagules shed only at the hour of maximal

excretion (19: 30) entering day as a continuous variable (see Methods for

details about the model). We found a common trend to increase during the five

consecutive days of study (GLMM, parameter estimate=0.21, F1,33=30.1,

p<0.001), although the interaction between day and individual was significant

(GLMM, F1,33=29.3, p<0.001), indicating that not all individuals showed such

trend.

Regarding coccidian oocysts, the results were quite similar to those

reported for capillarids (Table 1). Hour of the day was again the most important

factor, explaining the 41.6% of variance of the final model, and showing the

same pattern of increase described for capillarid eggs (Fig. 2). Day of sampling

affected significantly, although in this case the interaction with the individual

was not significant (Table 1). A further analysis revealed that coccidian oocysts

shedding tended to increase across the five consecutive days entered in the

analysis (GLMM, parameter estimate=0.22, F1,24=12.3, p<0.01). Interaction

between day and individual was not significant (F1,24=0.00, p=0.99), indicating

that this pattern was common for all individuals infected with coccidia.

Effect of type of feces on propagule counts

Capillarid eggs were much more abundant in intestinal faeces compared

to caecal faeces shed by the same individual at the same hour and day

(Wilcoxon matched pairs test: Z=4.8, N=34, P<0.001, Fig. 3). In contrast, the

pattern observed was totally opposed when the abundance of coccidian

ococysts was analysed (Z=3.5, N=33, P<0.001, Fig. 3), the oocysts being more

abundant in caecal than in intestinal faeces (matching by bird, hour and day in

the analysis).

Propagule counts of both types of faeces were not correlated in the case

of capillarids (rS= 0.15 , N= 34, P=0.37), but this relationship was significant for

coccidian oocysts (rS= 0.44 , N= 33, P<0.05).

DISCUSION Our results indicate that the hour of the day may exert a very strong

effect on parasite propagule excretion. This point was confirmed in two different

51

parasite species coming from two extremely different taxa (Nematoda and

Protozoa) infecting the same bird host species (the red legged partridge). In

both cases propagule shedding increased as the day progressed, reaching

maximal values in the late afternoon. Scarce attention has been paid in the

literature to the existence of this kind of consistent daily trends in parasite

propagule excretion, especially for birds or host-parasite systems with little or

no relevance in human health or economy. For example, Giver et. al. (2000)

found no consistent pattern across individuals when comparing morning and

afternoon egg counts in faeces of domestic pigs artificially infected with the

trematode Schistosoma japonicum. In contrast, Boughton (1933) and Brawner

& Hill (1999) described a diurnal periodicity in the eliminiation of oocysts of the

genus Isospora in two avian passerine species (house sparrows and house

finches, respectively) consistent with the pattern found in this study. However,

the diurnal trend found for coccidia in our case does not seem to be as

pronounced as that found by Brawner & Hill (1999). This may be due to intrinsic

differences between host-parasite systems, or to the fact that the intensity of

coccidian infection in our experimental birds was not as high as those studied

by Brawner & Hill (1999). However, to the authors´ knowledge, this is the first

report of the existence of a consistent within-day pattern of excretion in a

nematode parasite of a bird species.

Although the hour was by far the most influencing factor in both

parasites, we also found an effect of the day of sampling. In particular, we found

a tendency to increase parasite propagule excretion during the course of the

study which was stronger for coccidian oocysts than for capillarid eggs. In our

study, samples were collected during five consecutive days just to exclude the

effect of any seasonal variation in propagule excretion as described in other

studies (e.g.: Shaw & Moss 1998; Theodoropoulos et al. 1998; Vicente et al.

2005). It is widely known that propagule excretion varies throughout the course

of a parasitic infection (Cordero del Campillo et al. 1999). Birds employed in this

study were naturally infected during an outbreak of capillariasis that affected our

captive population. As a result, birds may have been in different phases of the

parasitic infection when sampled, explaining why some birds showed a

tendency to increase the amount of capillarid eggs excreted whereas others did

not show this pattern. Unlike capillarids, infection by coccidia seemed to be

52

more benign, as revealed by low number of oocysts counted and the absence

of individuals showing clinical signs compatible with coccidiosis in the preceding

and following months. Probably this difference in the type and degree of

infection may explain the absence of interaction between day and individual in

the case of coccidia, although it may not be coherent with the fact that an

increasing between-day pattern was found in both parasites. One further

possible explanation is that repeated sample collection (that required the

investigator to go under the cages four times each day) may have stressed the

individuals during the five days of study. It is known that physiological stress

may lead to immunosuppression (Sapolsky 1992; Besedowsky & del Rey

1996), leading parasites to take advantage to the host and increase their

reproductive rate and propagule production. This stress-induced effect on

parasite propagule production may be relatively quick, even less than a week

both for nematodes and coccidia, as reflected by a recent study in ring-necked

pheasants (Phasianus colchicus)(Villanúa et al. 2006).

Apart from the effect of time of sampling, we found important differences

in propagule counts between types of faeces. In particular, capillarid eggs were

much more abundant in intestinal faeces than in caecal faeces, whereas the

pattern was the opposite for coccidian oocysts. This tendency was expected

attending to the part of the intestinal tract where the adult reproductive forms of

each parasite live. Adults of the capillarid Aonchoteca caudinflata live in the

intestine and therefore females release the eggs in the intestinal content. In

contrast, the oocysts found in our captive red-legged population belong to two

different species, Eimeria tenella and Eimeria colchici, both with sexual phases

that replicate in the epithelium of the caeca or in the caeca and final portion of

the intestine (the latter)(Cordero del Campillo & Rojo 1999). As a result, the

total number of oocysts counted (oocysts of both species are indistinguishable

unless they are sporulated, which was not the case in our samples) was higher

in caecal than in intestinal faeces.

In the last years the interest of behavioural and evolutionary ecologists

on parasites has increased due to their possible effects on host fitness and

evolution (Clayton & Moore 1997). Apart from ectoparasites, intestinal parasites

are the most commonly studied ones as possible factors affecting several

components of host fitness. Interestingly, both coccidia (Hillgarth 1990;

53

Buchholz 1995; Vorísek et al. 1998) and nematodes (Hudson et al. 1998;

Murray 2002; Newey & Thirgood 2004) are the most commonly endoparasite

taxa employed in such ecological studies, and most of those surveys that do not

involve culling the animal require indirect parasite load estimates based on

counts of the number of propagules in faeces. In parasites from these two taxa

we have found a marked diurnal periodicity in propagule excretion. However,

despite that the hour of the day at which samples are collected may be of vital

relevance, this variable is never controlled for in any study.

The great magnitude of within individual variation in propagule excretion

during the day may covey serious errors in non-invasive parasite load

estimates. Experiments in captivity may easily control for this effect by sampling

all the birds approximately at the same hour, preferentially in the late afternoon,

when propagule shedding is maximal and therefore differences between

individuals are maximised. However, such kind of data standardization is

difficult in the wild. Moreover, most of wild birds are trapped in the morning

hours, when propagule shedding is minimal, thus diminishing the power to

detect differences in intensities of parasite excretion between individuals. As

parasite estimates from birds sampled at morning and late afternoon hours may

not be comparable, the best way to solve this problem in studies in wild is to

control statistically for the hour of sampling in all the analysis by including it as a

covariable. Either the methodological standardization or the statistical control of

the effect of this variable may prevent from fatal errors and will lead to sounder

results. Similarly, studies where faecal samples are collected from the

environment instead of directly from the animal should take into account this

source of variability. Collection of fresh drops exclusively and during the same

hour of the day may be a good option, although the effect of weather in faecal

drying time should be considered. Alternatively, sample collection from places

where individuals are only during a determinate and known period of the day

(roosts, for example) may allow to increase the reliability of the results obtained.

With regards to the differences in parasite counts between types of faeces, the

main implication of our findings is that researchers should pay attention to the

life cycle of the parasite to develop the most appropriate protocol for sample

collection in species with long caeca like Galliforms or Anseriforms. In our

particular case, we have shown that parasite counts coming from intestine or

54

caeca are not comparable for this two parasite species. The ideal procedure

should be to count each parasite only in that type of faeces where it is more

abundant. However, caecal faeces are only a minor proportion of the total

amount of faeces produced by the bird. Therefore, it is very difficult to have the

opportunity to choose what type to collect, especially in the wild, and the

researcher will have to be satisfied with the type of sample excreted by the bird

when trapped (usually a intestinal drop). In our case, consistent collection of

intestinal faeces is suitable for capillarids, but seems to be acceptable for

coccidia too, as caecal and intestinal counts were correlated in the latter.

Although in the two parasites studied here the hour of the day and the

type of faeces were by far the most important factors affecting individual

variation in propagule counts, other possible factors may also affect. As said

above, we found an effect of the day of sampling that varied between

individuals in the case of capillarids. Other authors have found a day-to-day

variation in propagule counts that seems to be due to variations in propagule

production by the parasite or to aggregation of the propagules in the feces,

leading to sampling errors (e.g. Yu et al. 1998; Giver et al. 2000; Utzinger et al.

2001). Also, great differences in propagule excretion may occur along the

course of infection (Giver et al. 2000; Cordero del Campillo et al. 1999).

Moreover, in some parasite species, fecal propagule counts may not

necessarily reflect the number of adult parasites present in the body of the

individual (Welch et al. 1991). Density-dependent constraints may also alter the

relationship between parasite burden and faecal counts (Anderson & Shad

1985; Tompkins & Hudson 1999). Hence, the use of propagule counts to

indirectly estimate parasite burden should ideally be addressed in any host-

parasite system before being employed.

It is remarkable that we found identical diurnal trends in two extremely

different taxa of parasites. Although previous studies in other coccidian species

showed the same pattern (Boughton 1933; Brawner & Hill 1999), more research

involving different parasite and host taxa is required to confirm whether such

kind of diurnal variation is common across host-parasite systems. This study

remarks the point made by other authors (McLennan & Brooks 1991; Zuk 1992;

Brawner & Hill 1999) about the necessity of gathering more information about

the studied host-parasite system studied. A survey to identify the best method

55

for assessing parasite prevalence and burdens is recommended as a previous

step for any host-parasite study (e.g.: Seivwright et al. 2004; Brawner & Hill

1999). A better understanding of the dynamics of infection as regards for

example fluctuations in propagule number within and between days or between

types of feces may lead to obtain more reliable data and give the opportunity of

a more throughout understanding.

ACKNOWLEDGEMENTS

We thank Elisa Pérez, Salvador Jesús Luna and Paqui Talavera for

assistance during sample collection and analysis and Jesús Martínez-Padilla for

statistical advice. Financial support was provided by the Research Project PAI-

02-006 of the Junta de Comunidades de Castilla-La Mancha and by the

agreement between CSIC and Principado de Asturias. Lorenzo Pérez-

Rodríguez was supported by a FPU grant from the Ministerio de Educación y

Ciencia.

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15. Hall, A. (1985) Nutritional aspects of parasitic infection. Progress in food

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16. Hillgarth, N. (1990) Parasites and female choice in the ring-necked

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27. Ruiz de Ybáñez, M.R., Goyena, M., Abrigar, T., Garito, M.M., Martínez-Carrasco, C., Espeso, G., Cano, M. & Ortiz, J.M. (2004) Periparturient

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29. Seivwright, L. J., Redpath, S. M., Mougeot, F., Watt, L., & Hudson, P. J. (2004) Faecal egg counts provide reliable measure of Trichostrongylus

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30. Shaw, J. L. & Moss, R. (1989) The role of parasite fecundity and longevity

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31. Skryabin, K. I. (1991) Key to Parasitic Nematodes. E. J. Brill Publishing

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32. Theodoropoulos, G., Koutsotolis, K., Nikolaou, E., Kalogiannis, D. & Petrakos, G. (1998) Seasonal variations of gastrointestinal nematodes of

sheep in the region of Joannina, Greece. International Journal for

Parasitology, 28: 1287-1292.

33. Tompkins, D.M., Dobson, A.P., Arneberg, P., Begon, M.E., Cattadori, I.M., Greenman, J.V., Heesterbeek, H., Hudson, P.J., Newborn, B., Pugliese, A., Rizzoli, A.P., Rosa, R., Rosso, F. & Wilson, K. (2001). Parasites and host population dynamics. Oxford University Press, Oxford.

34. Tompkins, D.M. & Hudson, P.J. (1999) Regulation of nematode fecundity

in the ring-necked pheasant (Phasianus colchicus): not just density

dependence. Parasitology, 118: 417-423.

35. Vicente, J., Fierro, Y. & Gortázar, C. (2005) Seasonal dynamics of the

fecal excretion of Elaphostrongylus cervi (Nematoda, Metastrongyloidea)

first-stage larvae in Iberian red deer (Cervus elaphus hispanicus) from

southern Spain. Parasitology Researchearch, 95(1): 60-4.

36. Villanúa, D., Acevedo, P., Höfle, U., Rodríguez, O. & Gortázar, C. (2006). Changes in transmission stage excretion after pheasant release. Journal of

Helminthology, 80: 1-7.

37. Vorísek, P., Votýpka, J., Zvára, K. & Svobodova, M. (1998). Heteroxenous coccidia increase the predation risk of parasited rodents.

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38. Welch, D.A., Pybus, M.J., Samuel, W.M. & Wilke, C.J., (1991) Reliability

of fecal examination for detecting infections of meningeal worm in elk.

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39. Yu, J.M., de Vlas, S.J., Yuan, H.C. & Gryseels, B. (1998) Variations in

fecal Schistosoma japonicum eggs counts. The American journal of tropical

medicine and hygiene, 59(3): 370-375.

40. Zuk, M. (1992) The role of parasites in sexual selection: current evidence

and future directions. Advances In Study Behaviour., 21: 39-68.

59

Table 1. GLIMMs with normal error and identity link function for capillarid egg

and coccidian oocysts excretion. Hour of the day (nested in day), day and

individual*day interaction were included as categorical fixed factors. The model

for capillarid eggs explained a 59.6 % of the original deviance, whereas the

model for coccidia oocysts explained a 41.6%, without considering the deviance

explained by the individual which was included as random term in both models

(Z=6.96, p<0.001, and Z=0.38, p=0.35, respectively). Statistics for non

significant variables correspond to the step at which they were rejected from the

model.

Dependent Variable Fixed Factors F d.f. P % Deviance Explained Capillarid eggs Hour 4.50 15,97 <0.001 42.17 Day 5.00 4,97 <0.001 7.65 Individual*Day 1.89 34,97 <0.01 27.5 Coccidian oocysts Hour 3.20 15,85 <0.001 41.6 Day 3.13 4,86 <0.05 8.35 Individual*Day 1.25 25,66 0.230

60

Figure 1 Number of capillarid eggs per gram of faeces from eight red legged

partridges collected at four different hours of the day and during five

consecutive days. Dashed lines show daily patterns whereas solid lines indicate

mean values. Error bars have been eliminated for clarity.

Bird 72

0

900

1800

2700

8:00 12:00 16:00 19:30

Bird 71

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 69

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 59

0

9000

18000

27000

8:00 12:00 16:00 19:30

Bird 57

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 62

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 61

0

3000

6000

9000

8:00 12:00 16:00 19:30

Hour of sampling

Cap

illar

ideg

gspe

rgr

amof

faec

es

Bird 72

0

900

1800

2700

8:00 12:00 16:00 19:30

Bird 71

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 69

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 59

0

9000

18000

27000

8:00 12:00 16:00 19:30

Bird 57

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 62

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 61

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 72

0

900

1800

2700

8:00 12:00 16:00 19:30

Bird 71

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 69

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 59

0

9000

18000

27000

8:00 12:00 16:00 19:30

Bird 57

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 62

0

3000

6000

9000

8:00 12:00 16:00 19:30

Bird 61

0

3000

6000

9000

8:00 12:00 16:00 19:30

Hour of sampling

Cap

illar

ideg

gspe

rgr

amof

faec

es

61

Figure 2 Number of coccidian oocysts per gram of faeces from six red legged

partridges collected at four different hours of the day and during five

consecutive days. Dashed lines show daily patterns whereas solid lines indicate

mean values. Error bars have been eliminated for clarity.

Bird 71

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 57

0

7000

14000

21000

8:00 12:00 16:00 19:30

Bird 59

0

4000

8000

12000

8:00 12:00 16:00 19:30

Bird 62

0

10000

20000

30000

8:00 12:00 16:00 19:30

Bird 61

0

2500

5000

7500

8:00 12:00 16:00 19:30

Num

ber

ofoo

cyst

sper

gram

offa

eces

Hour of sampling

Bird 71

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 57

0

7000

14000

21000

8:00 12:00 16:00 19:30

Bird 59

0

4000

8000

12000

8:00 12:00 16:00 19:30

Bird 62

0

10000

20000

30000

8:00 12:00 16:00 19:30

Bird 61

0

2500

5000

7500

8:00 12:00 16:00 19:30

Bird 71

0

5000

10000

15000

8:00 12:00 16:00 19:30

Bird 54

0

2000

4000

6000

8:00 12:00 16:00 19:30

Bird 57

0

7000

14000

21000

8:00 12:00 16:00 19:30

Bird 59

0

4000

8000

12000

8:00 12:00 16:00 19:30

Bird 62

0

10000

20000

30000

8:00 12:00 16:00 19:30

Bird 61

0

2500

5000

7500

8:00 12:00 16:00 19:30

Num

ber

ofoo

cyst

sper

gram

offa

eces

Hour of sampling

62

Figure 3. Mean number of oocysts and capillarid eggs in caecal (solid columns)

and intestinal faeces (open columns). Bars indicate standard errors.

0

1000

2000

3000

4000

5000

6000

capillarid eggs coccidian oocysts

Prop

agul

es p

er g

ram

of f

aece

s

63

VII. CAPITULO 3 Efectividad de los tratamientos antiparasitarios actuales como método para prevenir la introducción de nematodos en el campo.

How effective is pre-release nematode control in farm reared red-legged

partridges (Alectoris rufa)?. Villanúa, D., Pérez-Rodríguez, L, Rodríguez,

O., Viñuela, J. & Gortázar C (2006). Journal of Helmithology (in press).

RESUMEN La cría de la perdiz roja en granja lleva asociado a un alto grado de

parasitación capaz de disminuir la productividad de la propia granja y la

supervivencia de las aves una vez liberadas, además de suponer un riesgo

para las poblaciones naturales. En el presente trabajo se ha evaluado la

efectividad de albendazol (V.O. 20 mg/kg) en perdices de granja infectadas de

manera natural con Aonchoteca caudinflata y Heterakis gallinarum. Las aves

tratadas mostraron una clara mejora de su condición física y se redujo la

excreción de propágulos parasitarios y el porcentaje de hembras grávidas de A.

caudinflat, pero no se consiguieron eliminar los parásitos adultos. La efectividad

encontrada fue de un 36,8 % en A. caudinflata y de un 17,1 en H. gallinarum.

Estos resultados indican que el tratamiento antihelmíntico usado

habitualmente en las granjas de perdiz de nuestro país no es lo suficientemente

efectivo como para evitar la introducción de nuevos parásitos en el campo

mediante las repoblaciones con perdiz roja.

ABSTRACT Game bird farming is associated with higher parasitation levels that

diminish farm productivity, reduce survival after releasing, and may pose a

health risk for natural populations. We evaluated the efficacy of albendazole

(orally, 20 mg/kg) in farmed red-legged partridges naturally infected with

Aonchoteca caudinflata and Heterakis gallinarum. Treated birds improved their

body condition, reduced nematode-egg deposition and the proportion of gravid

64

A. caudinflata females, but not the worm burden. We found a 36.8% and a

17.1% of effectiveness on A. caudinflata and H. gallinarum, respectively.

These results indicate that the anthelmintic treatment used normally in

Spanish partridge farms is not effective enough to avoid the introduction of

parasites into the field after release.

KEYWORDS: Albenzadole, Game birds, Helminths, Treatment.

INTRODUCTION The red-legged partridge Alectoris rufa is one of the most important

game birds in Spain with more than 5 million individuals hunted yearly (Millán et

al., 2004). Natural populations have declined considerably during the past

decade, leading to an important increase in partridge releases to supplement

stocks for shooting (Millán et al., 2003).

The release of farmed animals can involve a risk for wild populations due

to the possible introduction of new parasites into the field (Tompkins et al. 2002;

Millán et al., 2004).

This study evaluates the efficacy of albendazole, one of the most widely

used anthelmintics in Spanish partridge farms (APROCA, 2004), to prevent the

introduction into the field of two nematodes, Aonchoteca caudinflata (Holger-

Madsen, 1954) and Heterakis gallinarum (Scrank, 1788), parasites that are

exclusively found in farm-reared partridges, but not in wild ones (Millán et al.,

2004).

MATERIAL AND METHODS The study was carried out on 16 month old red-legged partridges during

a natural capillarid outbreak in a partridge farm in Ciudad Real, central Spain. In

September 2004, eight randomly selected birds coming from the infected

outdoor pen were isolated in individual elevated wire-cages.

Faecal samples were obtained on day 0 at dusk (time of the day of

maximal nematode egg excretion, Villanúa et al. in press) for a quantitative

coprological analysis in MacMaster chambers as described by Melhorn et al.

(1992), which confirmed the infection of all birds with capillarid nematodes (later

identified as Aonchoteca caudinflata).

65

Five randomly selected individuals were treated orally with 20 mg/kg of

albendazole (Albendavet®, Divasa Farmavic, S.A.) on day 1 and day 15,

according to the manufacturer´s instructions. The same volume of water was

given as a control to the other three infected birds. Fifteen days after the second

administration all birds were humanely sacrified and necropsied.

The necropsy included a second coprological analysis and the

examination of the digestive tract searching for parasites using a

stereomicroscope.

The efficacy (E) of albendazole treatment on worm burden was

calculated as follows after Reina et al.(2000):

Geometric mean of control animals-Geometric mean of treated animalsE= x 100Geometric mean of control animals

The nematode sex-ratio (SR) and fertility (F) were calculated as follows

after Kassai (1998):

Nº female nematodesSR=Nº total nematodes

Nº gravid females F=Nº total females

Body condition of partridges was estimated using three different

methods: an arbitrary score of the degree of fat deposition (1 to 5), the pectoral

angle as a measure of the width of pectoral muscles after Millán et al. (2003),

and the residuals of the regression of body weight on tarsus length after

Andersson (1992).

The effect of Albendazole treatment on propagule excretion, number of

adult worms and partridge body condition was analysed by means of non-

parametric statistics (Wilcoxon matched pairs tests and Mann-Whitney U tests),

as recommended by Kassai (1998) for studies with natural infections.

Differences in nematode sex ratio and fertility were analysed using Chi2 tests. RESULTS

All birds deposited eggs of capillarid nematodes immediately prior to the

experiment. This deposition decreased significantly (-90.75%) after treatment in

the medicated group (Wilcoxon test; Z=2.02; p<0.05) but not in control birds,

where deposition was even higher (+ 80.67%) in the second analysis (Wilcoxon

test; Z=1.6; p>0.05) (Figure 1).

66

After treatment, dosed birds showed higher values for fat index, pectoral

angle and residual body weights than control birds (Figure 2). However, only the

increase in relative body weight of the dosed group was significant when

comparing pre and post treatment values (Wilcoxon test; Z=2.02; p<0.05). Albendazole was shown to have a limited effect against adult

Aonchoteca caudinflata with an effectiveness of 36.8%. Neither the reduction in

the number of worms, nor the change in worm sex-ratios reached a 95%

significancy level. However, the fertility of female A. caudinflata from treated

partridges was significantly lower (51.0%) than in controls (67.7%) (Table 1).

Heterakis gallinarum, not detected by coprological analysis, was found in

the intestinal tract of all birds. No significant difference in worm burden was

found between treated and control birds (Table 1) and no females were gravid.

The effectiveness of the albendazole dose on Heterakis gallinarum was only

17.14%.

DISCUSSION

Despite a small sample size, the results show a limited effect of

albendazole treatment on Aonchoteca caudinflata and Heterakis gallinarum

infection, with an efficacy that is lower than that described for other

benzimidazole anthelmintics in different galliforms. Fenbendazole for example,

was 99.2% effective against Capillaria species when administered to chickens

for 6 days in feed (Taylor et al., 1993). Kirsch (1983) reported that

administration of 100 ppm of fenbendazole in feed to ring-necked pheasants

Phasianus colchicus and grey partridges Perdix perdix, for four consecutive

days, reduced the deposition of Heterakis gallinarum and Capillaria obstignata

eggs and the number of adult worms by more than 90%.

In the present study, a similar reduction in Capillaria egg counts was

obtained, but not in worm burden.This suggests that albendazole has some

limitant effect on the reproduction of nematodes, but it does not eliminate the

infection. This may be due to an insuffcient dosage. In the present study the

dose administred was that recommended for chickens by the manufacturer, so

future studies should confirm whether a dose increase would improve the

efficacy of the treatment.

67

In conclusion, the study shows that the treatment currently used by game

bird farmers in Spain may help to improve body condition of farm-reared

partridges, but is not enough to avoid the introduction of parasites into the field

after release. Alternative drugs, higher doses, or other administration methods

must be evaluated.

This study also highlights that coprological analyses alone are not

enough to ensure the absence of a given nematode species in farm-reared

birds.

Sanitary screenings of farm-reared birds should preferably include some

complete necropsies, for example of casualties, rather than rely exclusively on

non-invasive sampling.

ACKNOWLEDGEMENTS

This contributes to the agreement IREC - Principado de Asturias. We

acknowledge Galiana facilities (FGUCLM) and thank E. Pérez and F. Talavera

for their help. L. Pérez-Rodríguez has a FPU grant and O. Rodríguez a Torres

Quevedo contract partly supported by MEC. Two referees improved the ms.

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Wildlife Management ,68(3): 701-707.

8. Reina, D., Anderson, L., Habela, M., Weatherley, A. J., Navarrete, I. (2000) Efficacy of doramectin against naturally acquired nematode

infection in Iberian swine. Veterinary Parasitology, 89: 139-147.

9. Taylor, S.M., Kenny, J., Houston, A. & Hewitt, S.A. (1993) Efficacy,

pharmacokinetics and effects on eggs-laying and hatchability of two dose

rates of in-feed febendazole for the treatment of Capillaria species

infection in chickens. The Veterinary Record, 20: 519-521.

10. Tompkins, D.M., Parish, D.M.B., and Hudson, P.J. (2002) Parasite-

mediated competition among red-legged partridges and other lowland

gamebirds. Journal of Wildlife Management, 66: 445-450.

11. Villanúa, D., Pérez-Rodríguez, L., Gortázar, C., Höfle, U. & Viñuela, J. (2006). Avoiding bias in parasite excretion estimates: the effect of

sampling time and type of faeces. Parasitology, 133: 251-259

69

0

1000

2000

3000

4000

5000

6000

7000

8000

9000

Control Treatment

Prop

agul

e / g

Table 1. Efficacy of albendazole treatment on establishment of Heterakis gallinarum,

worm numbers of Aonchoteca caudinflata, and on sex ratio and fertility of Aonchoteca

caudinflata in red-legged partridges.

Treated birds Control birds Nematode Species

Mean SD Mean SD Statistical analysis Efficacy

Heterakis gallinarum 5,8 6,6 7 7,8 Z=0.74; p>0.05 17,14%

Aonchoteca caudinflata 20.2 21,2 32 20.4 Z=0.75; p>0.05 36,87%

A. caudinflata sex ratio 0.42 0.20 0.43 0.01 X2=1,03; df=1; p >0.05

A. caudinflata fertility 0.51 0.30 0.68 0.19 X2=5,43; df=1; p<0.05

Figure 1. Deposition of Aonchoteca caudinflata eggs per gram of faeces before ( )

and after ( ) treatment with albendazole (Mean + SE).

70

Figure 2. Body condition of control and albrendazole treated red-legged partridges as

reflected by three different methods: fat deposition index (in an arbitrary scale from 1 to

5), residuals of the regression of weight over tarsus length, and pectoral angle

(expressed in degrees).

Control Treated

Fat d

epos

ition

inde

xPe

ctor

al a

ngle

(º)

Res

idua

l wei

ght

Mean ±SE ±95%C.I.

5

4

3

-30

0

30

60

13

14

15

16

17

71

VIII. CAPITULO 4

Posible transmisión de nematodos propios perdices de granja a especies amenazadas.

First occurence of Eucoleus contortus in a little bustard Tetrax tetrax. A

negative effect of red-legged partridge Alectoris rufa releases on steppe

bird conservation?. Villanúa, D., Casas, F., Viñuela, J., Gortázar, C.,

García de la Morena, E.L. & Morales, M.B. (2007). Ibis (in press).

RESUMEN Cinco adultos de Eucoleus contortus fueron encontrados en el buche de

un macho de sisón, Tetrax tetrax, procedente de Ciudad Real (España, UTM

0421739 4311458).

En la zona en la que se recogió el animal se llevan a cabo munerosas

sueltas cinegéticas de perdiz roja (Alectoris rufa) criadas en granja.

El nematodo Eucoleus contortus nunca había sido descrito en sisones ni

avutardas (Otididae), pero es un parásito común en perdices de granja. Por

ello, este hallazgo pone de manifiesto la importancia de realizar estudios

parasicológicos comparativos en aquellas zonas sometidas a repoblaciones

para la caza.

ABSTRACT Five adult forms of Eucoleus contortus were found in the crop of a male

little bustard, Tetrax tetrax, from Ciudad Real (Spain, UTM 0421739 4311458).

This area is subject of many releases of farm bred red-legged partridges

(Alectoris rufa) for hunting.

Eucoleus contortus had never been reported in bustards (Otididae), but

is a common parasite of farmed gamebirds. Hence, this finding highlights the

interest of compared parasitological studies in areas managed for hunting.

KEYWORDS: Eucoleus contortus; Game management; Tetrax tetrax; Partridge

releases; Bird conservation

72

Little bustard (Tetrax tetrax), populations are rapidly declining in most

European countries (BirdLife International 2004). The cereal steppes of central

Spain are the most important wintering quarters for the little bustard, with more

than 90% of the west European population (De Juana and Martínez 2001,

García de la Morena et al. 2004). These steppe habitats are also important

partridge hunting areas in Spain.

During the last decades, natural populations of the red-legged partridge

(Alectoris rufa), have declined considerably in their historical range and more

than 4 million farm-reared partridges are released yearly in autumn to

compensate this decline. This has already raisen concerns regarding the

possible introduction of new parasites into natural populations (Millán et al.

2004a, 2004b).

In winter 2005, 14 little bustards (5 males and 9 females) were captured

with cannon nets in Miguelturra (Ciudad Real, Central Spain, UTM 0421739

4311458) for radio-tagging. The capture area was close (less than 5 km) to an

important hunting estate where partridge releases are common (about 3000

partridges released yearly).

One adult male died due to traumatism during the capture and was

necropsied. In the parasitological examination, adult forms of a capillarid

nematode were found in the crop. After further examination under a

stereomicroscope, these were found to represent adults of Eucoleus contortus

Creplin, 1839 (3 males, 2 gravid females) according to Anderson (2000).

The body condition of the necropsied bird, estimated as the ratio of body

weight on cube tarsus length (0,0018g/mm3), was lower than the ones found in

other 15 adult males captured the same season (0,0025 ± 0,0004; mean ±

standard desviation ).

No E. contortus have been found in any of 4 little bustards, nor in any of

17 great bustards (Otis tarda), both species sampled in central Spain and

necropsied in our laboratory.

In contrast, E. contortus is present in 7.7% of the red-legged partridges

from a neighboring hunting estate where releases of farm-bred gamebirds take

place (the authors, in prep.).

73

Like other monoxenous nematodes, Eucoleus contortus is almost

exclusively found in farmed gamebirds (Millán et al. 2004b) and had, to the best

of our knowledge, never been found in members of the Otididae family (Cordero

del Campillo et al. 1994).

E. contortus can affect the host´s body condition (Bosch et al. 2000), and

make their hosts more vulnerable to predation (Millán et al. 2002).

Our results suggest that the release of farm reared gamebirds can

eventually introduce new pathogens to wild populations of different species,

many of which are of conservation concern, as it is the case in the little bustard .

As hypothesized by Tompkins et al., (2001), if these parasites are able to find a

new host, they can become an additional problem for its conservation.

ACKNOWLEDGEMENTS This is a contribution to the agreement between IREC and Principado de

Asturias and to the CICYT Project CGL2004-06147-C02/BOS. We wish to thank

I. Hervás, R. Agudo, R. Mateo, M. Martínez and S. Luna for their assistance in

the field. F. Casas has a JCCM grant and E. L. García de la Morena was

funded by the Ministry of Education’s FPU Program. This experiment was made

following European, National and University of Castilla – La Mancha Ethics

Committee regulations.

REFERENCES

1. Anderson, R.C. (2000) Nematode parasites of vertebrales: their

development and transmission. CABI Publishing, Wallingford.

2. Birdlife International (2004) Birds in Europe II: Population

Estimates, Trends and Conservation Status. BirdLife International,

Cambridge.

3. Bosch, M., Torres, J. & Figuerola, J. (2000) A helminth community

in breeding Yellow-legged Gulls (Larus cachinnans): pattern of

association and its effect on host fitness. Canadian Journal of

Zoology , 78: 777-786.

4. Cordero del Campillo, M., Castañón, L. & Reguera, A. (1994) Índice-catálogo de zooparásitos ibéricos. Universidad de León, León.

74

5. De Juana, E. & Martínez, C. (2001). European Union Species Action

Plan For Little Bustard (Tetrax tetrax). In Schäffer, N & Gallo-Orsi, U.

(eds.), European Union Action Plans for eight priority birds species.

Office for Official Publications of the European Communities,

Luxembourg (pp. 1-17).

6. García de la Morena, E.L., De Juana, E., Martínez, C., Morales, M.B. & Suárez, F. (2004) Sisón Común, Tetrax tetrax. In Madroño, A,

González, C. & Atienza, J.C. (eds.), Libro Rojo de las Aves de

España. Dirección General para la Biodiversidad-SEO/Birdlife.

Madrid (pp. 202-207).

7. Millán, J., Gortázar, C., Tizzani, P. & Buenestado, F.J. (2002) Do

helmints increase the vulnerability of released pheasants to fox

predation?. Journal of Helminthology, 76: 225-229.

8. Millán, J., Gortázar, C., Martín-Mateo, M.P. & Villafuerte, R. (2004a) Comparative survey of the ectoparasite fauna of wild and

farm-reared red-legged partridges (Alectoris rufa), with an ecological

study in wild populations. Parasitology Research , 93(1): 605-611.

9. Millán, J., Gortázar, C. & Villafuerte, R. (2004b). A comparison of

the helminth faunas of wild and farm-reared red-legged partridges.

Journal of Wildlife Management 68(3): 701-707.

10. Tompkins, D.M., Greenman, J.V., Hudson, P.J. (2001) Differential

impact of shared nematode parasite on two gamebird hosts:

implications for apparent competition. Parasitology, 122: 187-193.

75

IX. CAPITULO 5 Factores limitantes de la abundancia estival de perdiz roja en Aragón. Posibles alternativas a las repoblaciones con aves de granja.

Factors affecting summer densities of the red-legged partridge (Alectoris

rufa). Ibis. Villanúa, D., Acevedo, P., Escudero, M.A., Marco, J. and

Gortázar, C. (En evaluación).

RESUMEN

La perdiz roja (Alectoris rufa) es el ave de caza más importante en la

península Ibérica. A lo largo de los últimos años, el colectivo de cazadores ha

percibido un descenso de sus poblaciones en la práctica totalidad de su área

de distribución. Diversos factores, tales como la depredación, la presión

cinegética, la meteorología o la alteración del hábitat han sido considerados

abitualemento como las posibles causas de este descenso.

En el presente trabajo se ha estimado la densidad de perdices tras la

reproducción (siguiendo el método de Kelker) en 36 acotados (con una media

de 5 transectos por acotado repetidos anualmente) desde 1998 hasta 2004. Se

ha testado el efecto de factores meteorológicos, de hábitat, de depredación

(abundancia de carnívoros) y presión cinegética sobre las variaciones en la

abundancia de perdiz roja.

Los resultados obtenidos muestran que los factores meteorológicos son

los más limitantes para esta especie. La temperatura máxima y el número de

días de lluvia en concreto fueron los parámetros más significativamente

relacionados con la abundancia de perdices. Además de estos dos factores,

varias características del hábitat mostraron una influencia significativa sobre las

abundancias de perdiz. Así pues, las mayores abundancias se encontraron en

los acotados con un alto grado de mosaico de cultivos, en parcelas irregulares

y con alta cantidad de linderos. No se detectó relación entre la presión

cinegética o la depredación y la abundancia de perdices en esa época del año.

ABSTRACT

76

The red-legged partridge (Alectoris rufa) is the most important game bird

in the Iberian peninsula. During the last years, hunters perceive the decline of

partridge populations in practically all its distribution area. Factors such as

predation, hunting pressure, meteorology, and habitat structure are known to

affect game bird populations.

We estimated postreproductive partridge densities (following Kelker’s

method) in 36 hunting estates (an average of 5 transects per hunting estate).

Transects were carried out yearly from 1998 to 2004, and the influence of

different meteorological factors, habitat characteristics, predation (carnivore

abundance) and hunting pressure was analysed.

Our results suggest that the meteorological conditions were the most

important factor limiting partridge abundance, but also in determining inter-

annual variations. Partridge densities were significantly limited by the maximum

temperature and by the number of days of hail. Some habitat characteristics do

benefit the partridge densities. The highest ones were found in areas with high

patch density of irregular mosaic cultures. No effect was found between the

hunting pressure and predation on the partridge’s abundance.

KEY WORDS: Agricultural landscape, Density, Game birds, Fox predation,

Hunting, Meteorology.

INTRODUCTION Red-legged partridge (Alectoris rufa) hunting is one of the more important

economical and social activities in the rural areas of the Iberian peninsula

(Delibes 1988, Lucio 1998, Bernabeu 2000). In addition, this species is, along

with the wild rabbit (Oryctolagus cuniculus), one of the most important preys for

endangered Mediterranean predators such as the Iberian imperial eagle (Aquila

adalberti) (Delibes & Hiraldo 1981, Calderón 1983).

During the last years, populations of this game bird have declined

seriously in almost all its distribution area (Cramp & Simons 1980, Potts 1980,

Aebischer & Potts 1994, Baratti et al 2005), including the Iberian peninsula

(Rueda et al 1992, Nadal et al. 1996, Borralho et al. 1998, Lucio 1998, Carvalho

et al. 1998, Duarte 1998, Blanco Aguiar et al 2003, SEO/BirdLife 2004). The

causes of this decline are not clear, but agriculture intensification (Potts 1980;

77

Lartiges y Mallet, 1983; Rands, 1987; Pepin y Blayac, 1990; Crick et al. 1994,

Green 1995, Nadal et al., 1996; Aebischer y Kavanagh, 1997; Lucio, 1998,

Borralho et al., 2000; Gortázar et al, 2002), hunting pressure (Potts, 1986;

Pepin y Blavac, 1990; Lucio y Purroy, 1992; Borralho et al 1997), predation

(Ricci et al. 1990, Rands 1988, Yanes et al. 1998, Leonanrd y Reitz 1998) or

meteorological factors (Lucio 1990) are ones of the most important causes

implicated in this decrease.

There are many papers on the influence of habitat, climate, and

predation pressure factors on partridge densities in the Iberian peninsula,

however, some of these are limited to a few years of data (Lucio 1990, Nadal et

al. 1996, Borralho et al. 1998, Fortuna 2002), and others focused on small study

areas or on specific habitats (Lucio 1990; Nadal et al. 1996, Borralho et al.

1998, Fortuna 2002). Gortázar et al. (2002) gave the first large-scale data on

summer red-legged partridge abundance, based on the data of the first year

(1998) of regular partridge census in Aragón, north-eastern Spain. These

authors suggested that the lower partridge densities found in Aragón, relatively

to those in Central and Southern Spain, can be explained by climatic and

habitat-related factors, but also by management differences.

The aim of our present study is to evaluate how habitat, hunting

pressure, fox predation and meteorology affect summer red-legged partridge

densities during a 7-years series (from 1998 to 2004) in a wide range of habitats

in north-eastern Spain.

MATERIAL AND METHODS

Study area The study area (40º01'13''N to 42º23'27''N in latitude and from

03º53'22''W to 06º13'14''W in longitude) is located in the region of Aragón, north

east of the Iberian peninsula (Figure 1). Aragón is an autonomous region of

47,669 km2. It includes the central part of the Spanish Pyrenean mountains

(more than 3000 m a.s.l.), the southeastern part of the Iberian mountain chain

and the Central Ebro Valley (less than 300 m a.s.l.). This gradient explains the

presence of both big game species (includes Rupicapra pyrenaica, Capra

pyrenaica, Sus scrofa, Cervus elaphus and Capreolus capreolus), and small

78

game species (including Alectoris rufa, Lepus europaeus, L. granatensis and

Oryctolagus cuniculus).

Aragón has a diverse raptor and carnivore community, but the red fox is

clearly the most important predator for small game species (e.g. Villafuerte et al.

1996, Gotázar 1997, Gortázar et al. 2000).

The climate is Mediterranean, more continental as it gets away from the

sea, with an Atlantic influence in the western Pyrenees. Wood and scrublands

cover 13,518 km2. Fifty percent of the 1.2 million inhabitants concentrate in the

largest city, Zaragoza. Rural abandonment has been especially severe during

the industrial development of the sixties, allowing the natural vegetation to

recover (Bielza de Ory 1993).

Within this area, 5 biogeographical areas can be distinguished (Gortázar

et al. 2002), see Figure 1: (1) the Pyrenees (yearly mean temperature (T) lower

than 12ºC, annual rainfall (R) 800-1700 mm), (2) the Pyrenean foothills (T: 12-

14 ºC, R: 500-800 mm), (3) the Ebro depression (T: 13-15 ºC, R: 250-500 mm),

(4) the northern Iberian mountains (T: 10-14 ºC, R: 400-700 mm) and (5) the

southern Iberian mountains (T: 8-11 ºC, R: 400-800 mm). The last 4 areas are

occupied by the red-legged partridge and were included in our research.

The hunting in Aragón have not the commercial character typical from

the south of Spain, and the main part of the 2,091 hunting estates present in the

region are managed directly by the local associations. This social character

cause that game bird releases will be very rare. For this reason, all hunting

estates included in our research have only natural populations of red-legged

partridges where no restocking with captive-bred game-birds was performed in

the last ten years.

Partridge densities

The partridge densities (individuals/100 ha) was estimated in 36 different

hunting estates throughout the study area (Figure 1) using the censuses

included in the hunting species abundance monitoring plan, promoted by the

Aragon’s Govern. These censuses were made in August and September

because the aim of this monitoring plan is to know the hunting species

abundance just before the hunting season, in October. In each hunting estate, 5

fixed transects were placed selecting open areas of high visibility. The transects

79

were georeferenced (by mean of GPS, Garmin eTrex Vista™) on the Forest

Map of Aragón (vector map produced by Aragón Government, scaled 1:

50,000). The censuses were repeated during 7 consecutive years (from 1998 to

2004) for a total of 1,112 transects (552 km/year). As described Gortázar et al.

(2002), each fixed transect was 3,000 m long and 100 m wide (30 ha), and was

censused by 3 observers, thus the transect width for each observer was 34 m.

The short distance between observers, and the selection of rather open

habitats, should reduce the bias due to visibility (see Bibby et al. 1992), and

made us confident of having little underestimation. We assumed that all birds

within the transect width were detected. Censuses began shortly after dawn

until 3 to 5 hours later and were done by foot. In order to reduce variability, only

days without wind, rain or other unfavourable meteorological circumstances

were selected.

Partridge density for each transect was estimated with Kelker´s method

(see Burnham et al. 1980), using the formula:

6· ·10nD

L W −=

where D is the partridge density per 100 ha, n is the number of partridges seen

inside the 100 m counting strip, and 6· ·10L W − is the surface of the counting strip in

100 ha units (i.e. 3000·100·10-6= 0.3). Annual partridge density for each hunting

estate was calculated as the average of partridge densities obtained in the fixed

transects (generally, 5 transects per hunting estate).

Weather conditions Meteorological data were taken from 24 official meteorological stations of

the National Institute of Meteorology located across the study area from 1998 to

2002. To select the most representative parameters, a previous correlation

analysis was made with the different meteorological data. After this first

selection, we used the following indicators:

• Rainfall: winter rainfall accumulation, number of days of hail and number of

days of storm from April to September, number of days with precipitation

higher than 300 mm in the same period.

• Temperature: average of the maximum temperatures per month, average of

the minimum temperatures per month, number of days with maximum

80

temperature higher than 25 ºC and number of days with minimum

temperature lower than –5 ºC.

These factors characterized meteorologically each hunting estate.

Vegetation and orography characteristics

To characterize the vegetation and orography of each hunting estate

(sampling area) we used Geographic Information Systems.

We defined 10 different classes of vegetation (patch types) using the

Forest Map of Aragón (scaled 1: 50,000): oak and pine woodlands, oak

savannah habitats (“dehesas”), short scrub, tall scrub, cultures mosaic, sparse

pines, cereal cultures, woody cultures, pastures, and others (vegetation classes

that rarely occurred in the study area).

We used the following indices:

• Patch Density (PD): the total number of patches per unit area (number of

patches/m2). We considered the number of patches of each vegetation class

(vegetation-class level) and/or the total number of patches per sampling unit

(landscape level) to calculate the PD index.

• Average Size of Patches (ASP) of each vegetation class (m2).

• Average Edge length of Patches (AEP) of each vegetation class (m).

• Average Edge length per unit Area (AEA) of each vegetation class (m-1).

The orography characteristics were obtained from a digital elevation model,

spatial resolution (pixel width) of 100 m (SRTM, European Environment Agency

2000). The average altitude and slope of each sampling unit were considered to

evaluate the influence of the orography on red-legged partridge abundance.

Fox population trends

The red fox (Vulpes vulpes) is considered one of the most important

partridge predator (e.g. Tapper et al. 1982, Calderón 1983), hence his

population trend for each estate was included in the analysis. Red fox

abundance was estimated using the censuses included in the hunting species

abundance monitoring plan, promoted by the Aragón’s Govern. The abundance

estimates were carried out on fixed routes that cross open habitats far from

forests or human-inhabited places. The same two rangers carried out all

81

surveys of a given locality (n=24) using a 4-wheel drive vehicle with a handheld

100-watt spotlight, which light was swept round in a semi-circle (Barnes &

Tapper 1984).

Annually, from1998 to 2004, each transect was censused an average of

4 times. Every fixed route was about 30 km long, and the average speed was

20 km/h. Data were converted into abundance per 100 km (100*KA) to get a

relative abundance index. These values were also used to calculate a fox trend

index (percentage of a common base value). This base value was the average

of the different yearly abundances (see Crawford 1991 for a discussion on the

calculation of indexes in monitoring schemes). Thus, the population trend

indexes do reflect the % abundance in relation to the average for the whole 7-

year period, and are independent from the detectability.

Only nights close to the new moon and without rain or strong winds are

used. This distance, speed, and period has been recommend by other authors

for nightspotting surveys of medium-sized mammals (Stahl 1990, Weber et al.

1991). The total sampling effort was 552 counts with 16,560 km.

Hunting pressure

The low inhabitant’s density typical from the rural areas in Aragón and

the social characteristic of hunting in this region, originates a lower hunting

pressure to those in other areas from Spain (Gortázar et al. 2002). In the

present study, we use the number of hunters per ha like estimator of the hunting

pressure in each hunting state.

Statistical analysis

Linear regression analyses were used to calculate partridge population

trends. Moreover, we designed a 2 step procedure to assess the effect of the

environmental variables on red-legged partridge density.

First, the bivariate association between the hypothesized factors and

partridge summer abundances were analysed by means of Spearman’s

correlations. The variables which captured the effect of any set of highly

correlated variables on the outcome were selected for inclusion in the models

(to avoid multicollinearity). For categorical variables, Kruskall-Wallis analysis

was used for simple assessment of associations.

82

As second step, we conducted a generalized linear mixed model

(GLIMMIX) and used partridge densities per 100 hectare as response variable

(n=213). We considered a Poisson error distribution and a logarithmic link

function (Wilson & Grenfell 1997). The models were reduced to their simplest

form by eliminating in a backward stepwise procedure any explanatory variables

that failed to explain significant variation in the response (Crawley 1993). We

controlled for the hunting estate as random factor.

RESULTS Descriptive: partridges and foxes

The red-legged partridge average densities expressed in number of

partridges per 100 ha were the following (mean ± SE, n, minimum - maximum):

22.91 ± 3.24, n= 20, (12.13 – 74.49) in the Pyrenean foothills, 21.64 ± 2.02,

n=37, (0.00 –49.29) in the Ebro depression, 16.75 ± 1.56, n=77, (0.00 – 58.75)

in the northern Iberian chains, and 18.56 ± 1.78, n=79, (0.00 – 67.78) in the

southern Iberian chains. No clear population trends have been observed for the

study period at a regional scale (beta = -0.18, p>0.05). Among the

biogeographical areas, partridge densities varied between years, as is shown in

Figure 2, but it can be observed that only the Pyrenean foothills area show a

significant decrease trend.

The red fox average trend expressed in percentage of a common base

value (above 100 the population increases, and below 100 the population

decreases) were the following (mean ± SE, n, minimum - maximum): 100.44 ±

5.65, n= 16, (56.47 – 135.83) in the Pyrenean foothills, 101.72 ± 10.02, n=20,

(21.13 –196.18) in the Ebro depression, 95.99 ± 2.40, n=47, (56.67 – 143.45) in

the northern Iberian chains, and 92.82 ± 3.44, n=52, (38.99 – 148.69) in the

southern Iberian chains.

Multivariate analysis

Twelve factors were selected after step 1. The selected factors were:

year, number of days of hail –from April to September-, maximum temperatures

per month, number of days with temperature higher than 25 ºC, number of

83

days with temperature lower than –5 ºC, tall scrub PD, mosaic cultures PD,

pastures PD, cereal cultures ASP, woody cultures ASP, short scrub AEA, and

fox population trend. The final model evidenced that red legged partridge

summer density was positively associated with the patch density of cultures. It

was negatively associated with the number of days of hail (from April to

September), and with the average of maximum temperatures per month (see

Table 1). It is remarkable that fox population trend was retained in the final

model although no significant effect was shown.

DISCUSSION This paper presents an analysis of red-legged partridge population

densities over seven years in many localities in north-eastern Spain, combined

with a look at important factors that may affect these densities. Truly the only

conclusive statement this study makes is that in the whole region of Aragón,

partridge population densities are not decreasing significantly, which is a very

considerable finding in itself.

Partridge densities

A wide range of red-legged partridge density values is described in the

literature. The highest densities, over 400 partridges per 100 ha, were found in

intensively managed hunting areas from central Spain (Nadal 1998). However,

in some natural populations without this kind of management, partridge

densities were around 50 to 100 partridges per 100 ha (e.g. in French

scrublands, Pepin & Blayac 1990; and in Spanish olive groves, Duarte 1998).

Our results showed much lower partridge densities, only similar to those

obtained in released populations (Carvalho et al. 1998, Mereggi & Mazzoni

della Stella 2004), and in areas with low partridge densities (e.g. in Portuguese

agricultural lands, Borralho et al. 1996). The lower densities found in Aragón as

compared to other areas were documented previously by Gortázar et al. (2002).

We used the same fixed transects than the previous study. They attributed the

low densities obtained to two possibilities, the use by different authors of a wide

number of field methods to estimate partridge densities, and a true effect of

environmental constraints.

84

No clear population trends were observed for the study period at a

regional scale. This is in contrast with the hunters’ perceptions and with

previous authors (e.g. Carvalho et al. 1998). Among the biogeographical areas,

partridge densities varied between years but clear population trends were not

observed, and even a slight increase occurred in the southern Iberian chains.

The lowest partridge densities were obtained in the Iberian chains, which

showed the most stable population trends during the study period (see Figure

2). In the northern Iberian chains some areas have a well-preserved habitat and

a favourable climate. In contrast, some of the higher zones in the south Iberian

chains have a lack of cereal crops due to rural abandonment and most areas

are above 1,000 m a.s.l., with frequent frost that may limit the reproductive

success of the partridges (Slagsvold & Grasaas 1979). The highest densities

were obtained in the Pyrenean foothills and Ebro depression populations, the

trend being slightly decreasing in the 7 studied years. These differences could

be do to the intensification of agricultural practices in some areas of the

depression (mainly in the 1980’s), while traditional agriculture still dominates in

the mountain areas (Gortázar et al. 2002).

Influence of meteorological factors

Our results suggest that meteorological conditions are the main factors

affecting the summer abundance of red-legged partridges, even over the habitat

quality or predation. Most authors think that climatic conditions are key factors

limiting the galliform densities (Slagsvold & Grasaas 1979, Hermes et al. 1983,

Green 1984, Lucio 1990, Panek 1992, 2005), the weather conditions causing

only annual fluctuations (Panek 2005). The latter author suggested that the

weather conditions were an additional reason for the inter-annual density

changes, and consequently partridge populations oscillated around their

equilibrium level due to density-dependent parameters. We found that extreme

temperatures and hail were negatively related with partridge densities. This can

be explained in different ways:

i) Decreasing the chick survival: chick survival is a fundamental factor in

galliform population dynamics (Potts 1986), and the differences in this

parameter may produce the year-to-year changes in population densities (Blank

85

et al. 1967). Weather characteristics can influence the partridge chick, affecting

the quality and availability of food to both chicks and adults. Some studies have

shown that changes in temperature limit the number of chicks per pair in natural

populations of grey partridge, Perdix perdix, (Panek 1992) and red-legged

partridge (Lucio 1990). The influence of temperature on the number of chicks

per pair was demonstrated experimentally (Hermes et al. 1983). These authors

found two explanations for this influence. First, excessively low temperatures in

winter may motivate a decrease in insect abundance (Panek 1992) that is

positively correlated with chick survival rates (Green 1984, Lucio 1991, Panek

1992). Second, the relationship found between maximum temperature and

partridge densities can be related with chick death-rate during the harvest

period. High spring temperatures can bring forward the development of

vegetation (Lucio 1990), but this is associated with bringing forward the harvest

period. Hence, it can increase the chick death-rate by agricultural machinery

(Ricci 1985, Lucio 1990, Nadal et al. 1996, Meriggi & Mazzoni della Stella

2004).

Additionally, extremely high summer temperatures may increase the

death of partridges due to miopathy-like syndromes, that are reported in other

lowland partridge habitats in Spain (Höfle et al. 2004).

ii) Decreasing the productivity: it is well known that the climate influences

a bird’s fertility and productivity. Slagsvold & Grasaas (1979) working with

capercaille (Tetrao urogallus) found a positive relationship between the early

defrosting and autumnal densities. The food critical period can influence the

nest size (Lack 1968). The percentage of successfully hatched eggs may also

depend on factors such as temperature, storms, hail and rainfall (Green 1984).

iii) Increasing the predation of adults: the activity of partridges decreases

with low temperature and wet weather (Green 1984). This can make the birds

more vulnerable to predators, and can cause a loss of condition, again

increasing the vulnerability.

Normally, these demographic parameters do control the partridge

population dynamics. This is well known in grey partridge decrease populations.

86

The grey partridge decrease in Great Britain between the 1960s and the 1990s

was a result of a decrease of both brood-production rate and chick survival rate

(Potts 1986, Potts & Aebischer 1994). Nevertheless, the grey partridge

decrease in France in 1990s was mainly an outcome of a decline in the survival

rate of adults birds (Bro et al. 2000, Reitz 2000). The population decrease of

grey partridges in Poland showed that it was connected with the drop of

reproductive success, including both the brood-production rate and the chick-

survival rate, as well as with the decline of annual survival rate of adult birds

(Panek 2005).

Habitat structure

Our results showed that cultures in mosaic were the habitat type with

most influence on red-legged partridge densities. This type of habitat is

associated to traditional agriculture schemes. These traditional schemes were

based on the distribution of cultures in small patches where the hedges were a

key landscape structure feature.

The development of agriculture was characterized by the increase of plot

dimension, hedge destruction, monocultures and development of harvesting

mechanization (Myers et al. 2000). Intensified agricultural practises and habitat

changes are believed to be key factors in explaining the decline of many

agricultural bird species (Chamberlain et al. 2000, Siriwardena et al. 2000).

Fuller et al. (1995) argued that the decrease in area of semi-natural grasslands

has reduced their capacity for farmland birds. Pärt & Söderström (1999) argued

that the combined effects of good foraging habitat close to safe nesting sites are

critical factors for breeding farmland birds. The negative effect of modern

agriculture on partridge populations was suggested before by several authors

(Ricci 1985, Lucio1991, Nadal et al. 1996, Fortuna 2002, Meriggi & Mazzoni

della Stella 2004). The grouping of agricultural plots that has taken place during

the last decades, has already been indicated as a constraint for red-legged

partridge density in the north-west of Spain (Lucio 1991). Hedge reduction also

has a negative effect on partridge density in Spain (Fortuna 2002). Hedges are

areas with high availability of food, nesting-sites, shade and cover. The last two

characteristics can also be supplied by other types of vegetation, such as

vineyards or olive trees (Borralho et al. 1998). In our study, vineyards and olive

87

trees (noted woody cultures) were not related with the highest partridge

densities. These habitat types give shade and protective cover and are rich in

hedge-like microhabitats, but are intensively managed with agrochemicals and

machinery.

Fox predation The red fox is the most abundant wild rabbit predator in Aragón (Gortázar

1997), and rabbit populations were decreasing in practically all its distribution

area due to the additive effect of myxomatosis and RHD (e.g. Villafuerte et al.

1995, Gortázar 1997). Thus, one cause of the decline in the red legged

partridge populations could have been the switch of rabbit hunters and

predators towards alternative prey species following the decline in rabbit

populations (Gortázar et al. 2002). A few studies have shown the red fox or

generalist carnivores and raptors to be a significant cause of mortality in

partridge populations (e.g. Tapper et al. 1996, Bro et al. 2001, Panek 2005).

Through a predator control experiment, Tapper et al. (1996) showed that grey

partridge population densities were reduced by the combined effects of

predation by several farmland bird predators, including red fox. Panek (2005)

suggested that to improve the situation of grey partridges, efforts should be

focused on the reduction of predators, mainly red fox populations. Moreover,

the environmental changes may have increased predator impact (Reynolds &

Tapper 1996).

Much to our surprise, fox predation effects were not clearly evidenced in

our study. The first explanation for this apparent lack of relationship is that foxes

were counted in transects that were close to, but not exactly at the partridge

census transects. Moreover, no fox data were available for 12 of 36 sites. But it

may also be explained by the low fox abundances according to our surveys and

to similar data already reported from the region (Gortázar et al. 2000, 2002).

From a regional perspective, our results did not show any correlation

between partridge population densities and red fox population trends. While

trends do not directly measure predation pressure, as was done in other

studies, it would be expected that if fox predation was a main cause of partridge

death for a majority of the localities in our study then there would be a negative

correlation between the two species’ population parameters.

88

Conclusions

We found that the meteorological circumstances were the most important

factors that limited partridge densities. Hence, the climatic characteristics of a

territory are, in our opinion, the main factor that determines their environmental

potentiality as far as the red-legged partridge summer abundance is concerned.

Within a given bioclimatic area, some habitat characteristics such as

small plot size and high boundary proportion do also benefit the partridge

densities. One of the main conservation challenges in Mediterranean areas is

the loss of this habitat type caused by the intensification of agricultural

practices.

According to the premise that red-legged partridge exploitation should be

sustainable, populations with low densities generate questions regarding the

management of the hedges in the landscape, regeneration of agricultural

mosaics and predator control to improve partridge densities.

ACKNOWLEDGEMENTS Partridge censusing is part of the game management actions of Asesoría

de Caza y Pesca, Dirección General de Medio Natural, Gobierno de Aragón.

Special thanks to Emilio Escudero, Adela García and Gaspar León who

coordinate the scheme. This work would never have been done without the

enthusiastic collaborations of Aragón`s Game Rangers. Joaquín Vicente helped

us with the statistical analysis. D Villanúa and P Acevedo were supported by the

joint project CSIC/Principado de Asturias.

89

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95

63. Table 1. Generalized linear models for red-legged partridge densities.

The distribution error is the Poisson with a logarithmic link function. The

model explained 60.18 % of the original deviance. The effects not

included in the models with the lower AIC value are highlighted in bold.

VARIABLES d.f. F p-value Estimat

e

Number of days with hail (from April to

September) 97.5 2.54 0.048 -0.0666

Maximum temperatures per month 84 7.21 0.008 -0.0168

Cultures mosaic PD 17.8 5.20 0.035 530.210

0

Fox trend 111 0.42 0.216 -0.0011

96

Figure 1. Aragón region boundaries and hunting estates boundaries are shown

in black. The white circles show the locations of the transects (N=184). Relief of

Aragón region and biogeographical areas are displayed (darkest greys showing

higher altitudes).

97

Figure 2. Annual variation (1=1998, 2=1999, 3=2000, 4=2001, 5=2002, 6=2003,

and 7=2004, in horizontal axis) in red-legged partridge summer densities for

each biogeographical area. The B coefficients show the population trends for

each area (+=p<0.05, and n.s.=p>0.05).

0

10

20

30

40

50

60

70

1 2 3 4 5 6 7 1 2 3 4 5 6 7 1 2 3 4 5 6 7 1 2 3 4 5 6 7

Part

ridg

es d

ensi

ty p

er 1

00 h

a

Pyrenean foothills B=-0.77 +

Ebro depression B=-0.01 n.s.

N. Iberian chains B=-0.29 n.s.

S. Iberian chains B=0.34 n.s.

98

X. SÍNTESIS GENERAL

Este apartado pretende ser, como su propio nombre indica, una síntesis

de los resultados más relevantes obtenidos durante la realización de la

presente Tesis Doctoral, discutiendo especialmente sus posibles implicaciones

en la conservación y gestión de la perdiz roja.

La introducción de patógenos. (Capítulos 1 y 4)

Uno de los resultados más relevantes de la presente tesis es sin duda el

hallazgo en las fincas con suelta de tres especies de parásitos (Eucoleus

contortus, Skyabinia bolivari y Aonchoteca caundinflata), típicas de aves de

granja y no descritas anteriormente en perdices silvestres (Millán et al., 2004).

La presencia de estos parásitos en aves cazadas podría deberse en

principio a dos situaciones; o bien que estuviesen parasitando aves de granja

que portasen los parásitos antes de la suelta o que se tratase de aves

silvestres que se hubiesen infectado con los parásitos traídos por las perdices

liberadas.

La distinción entre aves de granja y silvestres puede resultar, a pesar de

las diferencias esplagnométricas existentes entre unas y otras (Millán et al

2001), sumamente difícil si las aves liberadas no van convenientemente

anilladas. Por este motivo se nos hace necesario analizar las consecuencias

que podrían tener una y otra posibilidad.

En caso de tratarse de aves de granja, estas llevarían en el campo más

de dos meses en el momento de la toma de muestras, tiempo más que

suficiente para transmitir los nuevos parásitos a sus congéneres silvestres.

Esta transmisión se vería además favorecida por el incremento de la excreción

de propágulos parasitarios que sigue a la suelta, motivado por el estrés que

supone para las aves la liberación a un medio desconocido y al cese de los

tratamientos (Villanúa et al 2006).

La otra posibilidad sería, como decíamos, que se tratase de aves

silvestres que se hubiesen infectado tras la llegada de los nuevos parásitos con

la suelta de aves de granja. A favor de esta hipótesis estaría el hecho de que

menos de un 20 % de las perdices de granja liberadas sobreviven dos meses

99

en el campo (Birkan, 1971; Capelo y Pereira, 1996; Gortázar et al., 2000), que

la supervivencia se supone todavía menor en aves parasitadas por el

nematodo Eucoleus contortus, ya que este hace a las galliformes más

detectables por el zorro (Millán et al 2002) y que dos de estos parásitos fueron

encontrados en aves adultas, cuando las sueltas se llevan a cabo con

individuos juveniles.

Parece pues más probable que las aves infectadas por estos parásitos

propios de granja fuesen aves silvestres a las que les hubiesen transmitido los

patógenos las aves liberadas con fines cinegéticos.

Otra posible prueba de la introducción de parásitos sería el hallazgo del

nematodo Eucoleus contortus parasitando un macho de sisón (Tetrax tetrax),

procedente de una finca en la que se realizan sueltas de perdices con fines

cinegéticos. Nunca antes se había detectado este parásito en esta especie ni a

ninguna otra propia de los ambientes esteparios, mientras que resulta muy

frecuente en perdices en cautividad y se ha encontrado en ejemplares de

granja cazados en esta misma finca.

Para comprender la magnitud del problema que podría suponer la

introducción de nuevos patógenos en el campo se puede recurrir a los trabajos

de Tompkins et al (1999, 2000, 2001) ya comentados en la introducción. Estos

autores demuestran, basándose en estudios experimentales (Tompkins et al

1999 y 2001) y en modelos matemáticos (Tompkins et al 2000), que la

introducción del nematodo Heterakis gallinarum con las sueltas de faisán vulgar

con fines cinegéticos podría ser uno de los principales factores causantes del

descenso sufrido por la perdiz pardilla en Inglaterra. El efecto negativo se

debería a que, al no haber tenido contacto previo con este parásito, la

patogenicidad del mismo sobre la perdiz pardilla es muy importante,

produciéndole una grave pérdida de condición corporal que limitaría tanto su

supervivencia y su éxito reproductivo (Tompkins et al 1999).

Así pues, si trasladamos este ejemplo a nuestro caso, la suelta de

perdices de granja, con la consiguiente exposición de las poblaciones naturales

de perdiz u otras aves como el sisón a los nuevos parásitos introducidos,

podría tener graves consecuencias desde e punto de vista de conservación de

las mismas, ya que la patogenicidad de los mismos sobre estos nuevos

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hospedadores sería a todas luces muy elevada, pudiendo condicionar su

supervivencia en el medio.

Como nota de esperanza cabe señalar el hecho de que, el hallazgo de

estos parásitos propios de granja se ha limitado a aquellas zonas en las que se

realizan repoblaciones, no habiéndose encontrado nunca en fincas de perdiz

salvaje limítrofes a dichas fincas con suelta. Parece pues que la capacidad de

dispersión de estos patógenos en el campo está limitada a una superficie

pequeña, lo que permitiría a cada gestor controlar la introducción de estos

patógenos a sus poblaciones independientemente de lo que se haga en las

fincas vecinas.

La insuficiente profilaxis actual. (Capítulos 2 y 3) La cría de perdices en cautividad se inició en nuestro país hace apenas

30 años (Millán et al., 2004) y su relevancia dentro del mundo veterinario-

ganadero es todavía poco importante, motivos por los cuales la investigación

de las industrias farmacológicas en este campo ha sido muy escasa. Fuera de

nuestras fronteras existe algún trabajo acerca de la efectividad de tratamientos

antiparasitarios en aves cinegéticas de granja (Kirsch, 1983), pero se trata de

experiencias con otras especies (faisán y perdiz pardilla) y son relativamente

antiguas (casi 25 años). Este vacío de conocimientos científicos acerca de los

tratamientos en perdiz roja ha forzado a los propietarios y veterinarios de las

granjas de esta especie a copiar los protocolos de tratamiento de la industria

avícola que, como se ha puesto de manifiesto en el capitulo 3 de la presente

tesis, no tienen porque ser los adecuados.

Así pues hemos podido comprobar como el tratamiento con Albendazol

que habitualmente se usa para tratar las infecciones por nemátodos en las

granjas de perdiz puede disminuir la excreción de propágulos parasitarios, pero

no es capaz de acabar con la infección. Desde un punto de vista de producción

en granja tal vez pudiese ser suficiente, ya que sin duda este tratamiento

disminuirá los síntomas e incluso acabe con las bajas, pero desde luego no

basta cuando lo que se busca es conseguir aves para liberar al campo.

La misma situación de falta de conocimientos específicos que hemos

comentado para el caso de los tratamientos es la que nos encontramos al

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revisar los protocolos diagnósticos utilizados. Los resultados expuestos en el

capítulo 2 ponen de manifiesto como, factores tan simples como la hora de

recogida de las muestras o el tipo de heces analizadas, son capaces de

hacernos considerar sana a una perdiz gravemente parasitada.

Mediante un experimento controlado, se pudo detectar un aumento muy

significativo en la excreción de E. contortus y Eimeria sp. a lo largo del día,

hasta el punto de que en las heces de aves que a las 8:00 de la mañana

estaban libres de excreción, doce horas más tarde se cuantificaban más de

15.000 propágulos por gramo para el caso de Eucoleus contortus o 30.000

ooquistes por gramo para el caso de Eimeria sp. Una situación semejante

sucedía al comparar los resultados de los análisis coprológicos realizados

sobre heces corrientes o sobre heces de ciegos, con una ausencia casi total de

propágulos de Eucoleus contortus en las de ciego y una presencia mucho

menor de ooquistes de Eimeria sp. en las heces corrientes. Estos errores

serán probablemente poco importantes en los sistemas de producción avícola

industrial, donde las aves reproductoras están permanentemente alojadas en

jaulas elevadas que cortan los ciclos parasitarios y los pollos van a matadero

con apenas 2 meses de vida, pero en el caso de las perdices criadas en granja

para su liberación en el campo el problema es muy grave, y debe ser por tanto

enfocado desde un punto de vista totalmente diferente.

En definitiva que, teniendo en cuenta la insuficiente efectividad de los

tratamientos actuales y la baja fiabilidad en la detección de las aves

parasitadas, a día de hoy parece totalmente contraproducente realizar

repoblaciones con perdices de granja, al menos si lo que se busca es mejorar

el estado de las poblaciones naturales.

Otro mundo mejor es posible. (Capitulo 5)

El análisis de los datos de abundancia obtenidos dentro del plan de

monitorización de las especies en Aragón ha puesto de manifiesto que las

poblaciones de perdiz de esta comunidad autónoma no están sufriendo el

detrimento registrado en las zonas del centro y sur de la península Ibérica. Así

pues, parece lógico pensar que, para conservar la perdiz roja en el centro y sur,

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se debería tal vez adoptar el modelo de gestión de Aragón, donde la suelta de

perdices es algo muy poco frecuente.

En este mismo estudio se ha podido comprobar que, si bien los factores

climáticos son el principal factor limitante de las abundancias de perdiz, existen

una serie de elementos del hábitat que son de vital importancia para el

mantenimiento de las poblaciones de perdiz roja y que son susceptibles de ser

fomentados. El más significativo resultó ser el parámetro que cuantificaba el

mosaico de cultivos, de manera que las mayores abundancias de perdiz se

encontraban en aquellas zonas en las que no se había perdido todavía la

agricultura tradicional, con alternancia de cereales con otros cultivos como el

olivo, la viña o los espárragos. A lo largo de los últimos años, este tipo de

paisaje ha sido sustituído en gran parte de la península Ibérica por los

monicultivos de cereal derivados de concentraciones parcelarias y un mal

enfoque de la Política Agraria Comunitaria (PAC)(Díaz et al. 2006). Parece

lógico asumir pues que esta importante pérdida de calidad del hábitat sea una

de las causas del declive de la perdiz roja, pero no lo es menos pensar que, si

se consiguiese restaurar este paisaje, las poblaciones de perdiz podrían

también recuperarse. A día de hoy nos encontramos en plena renovación de

los Programas de Desarrollo Rural (PDR) debido a la aplicación del

Reglamento (CE) nº 1698/2005 para el periodo 2007-2013, motivo por el cual

es el momento idóneo para, a traves de subvenciones, tratar de recuperar este

mosaico de cultivos y con el las aves ligadas este medio, entre las que se

encontraría la perdiz roja (De la Concha et al, 2006).

Bibliografía

1. Birkan, M. (1990). La perdrix rouge. Brochures techniques O.N.C.,

Paris. 36 pp.

2. Capelo, M. y Castro Pereira, D. (1996). Sobrevivência e dispersão de

perdizes (Alectoris rufa L.) largadas em duas operações de

repovoamento cinegético. Revista Forestal, 9: 245- 253.

3. De la Concha, I., Hernández, C y Pinilla, J. (2006). Medidas

beneficiosas para las aves financiables a traves del nuevo reglamento

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de desarrollo rural. Sugerencias para su diseño y aplicación en NATURA

2000. SEO/Birdlife. Madrid. España.196 pp.

4. Díaz, M., Baquero, R.A., Carricondo, A., Fernández, F., García, J. y

Yela, J.L. (2006). Bases ecológicas para la definición de las prácticas

agrarias compatibles con las Directivas de Aves y de Hábitats. Convenio

Ministerio MEdio Ambiente-Universidad de Castilla la Mancha. Informe

Inédito.

5. Gortázar, C., Villafuerte, R., y Martín, M. (2000) Success of traditional

restocking of red-legged partridge for hunting purposes in areas of low

density of northeast Spain Aragón. Zeitschrift für Jagdwissenschaft, 46:

23-30.

6. Kirsch, R. (1983) Treatment of Nematodiasis in Poultry and Game birds

with Febendazole. Avian Diseases, 28(2): 311-318.

7. Millán, J., Gortazar, C., and Villafuerte, R. (2001) Marked differences

in the splanchnometry of farm-bred and wild red-legged partridges

(Alectoris rufa L.). Poultry Science, 80: 972-976.

8. Millán, J., Gortázar, C., Tizzani, P. and Buenestado F.J. (2002) Do

helmints increase the vulnerability of released pheasants to fox

predation?. Journal of Helmintology, 76: 225-229.

9. Millán, J., Gortázar, C. & Villafuerte, R. (2004) A comparison of the

helminth faunas of wild and farm-reared red-legged partridges. Journal of

Wildlife Management, 68(3): 701-707

10. Tompkins, D.M., Dickson, G. y Hudson, P.J. (1999). Parasite-

mediated competition between pheasant and grey partridge: a

preliminary investigation. Oecologia, 119: 378-382

11. Tompkins, D.M., Greenman, J.V., Robertson, P.A. y Hudson, P.J. (2000). The role of shared parasites in the exclusion of wildlife host:

Heterakis gallinarum in the ring-necked pheasant and the grey partridge.

Journal of Animal Ecology, 69: 829-840.

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12. Tompkins, D.M., Greenman, J.V. y Hudson P.J. (2001). Differential

impact of shared nematode parasite on two gamebird host: implications

for apparent competition. Parasitology, 122: 187-193.

13. Villanúa, D., Acevedo, P., Höfle, U., Rodríguez, O. & Gortázar, C. (2006). Changes in transmission stage excretion after pheasant release.

Journal of Helminthology, 80: 1-7.

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XI. CONCLUSIONES, PERSPECTIVAS Y RELFLEXIONES

Conclusiones

1. La liberación con fines cinegéticos de perdices criadas en granja supone

un grave riesgo sanitario para las poblaciones silvestres tanto de perdiz

roja como de otras especies de aves que compartan con esta un mismo

hábitat, ya que llevan asociada la introducción de nuevos patógenos en

el medio.

2. La capacidad de diseminación de estos patógenos parece sin embargo

limitada, hasta el punto de que la política de gestión en un coto no tiene

porque tener efectos, desde punto de vista sanitario, en los cotos

colindantes.

3. Los protocolos actuales de detección de aves parasitadas, basados en

exámenes coprológicos de heces recogidas directamente del suelo, no

ofrecen suficientes garantías, ya que la excreción de propágulos

parasitarios varía a lo largo del día y con el tipo de heces, hasta el punto

de que aves altamente parasitadas pueden pasar por sanas.

4. El tratamiento con Albendazol, habitualmente utilizado contra las

infecciones por nemátodos en las granjas de perdiz roja reduce la

excreción de parásitos pero no consigue eliminar a los adultos, de

manera que no es capaz de evitar la introducción de estos parásitos en

el medio.

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5. Las poblaciones de perdiz roja de la comunidad autónoma de Aragón,

donde las sueltas son una práctica muy poco frecuente, no parecen

estar sufriendo el acusado descenso detectado para la zona centro y sur

de la península Ibérica.

6. En la comunidad autónoma de Aragón, la abundancia de perdiz en el

mes de agosto está más condicionada por la temperatura máxima

mensual, el número de días de lluvia entre abril y septiembre y la

abundancia de cultivos en mosaico, que por la abundancia de

depredadores o la presión cinegética del año anterior.

Perspectivas y reflexiones

A lo largo del desarrollo de la presente tesis han ido surgiendo dudas y se

han puesto de manifiesto vacíos de conocimiento que sería interesante abarcar

en futuros trabajos. Como asumimos que el hecho de que es un poco culpa de

todos que no se hayan realizado hasta ahora, creemos acertado poner la

coletilla de “reflexiones”.

• Mejora de los tratamientos profilácticos.

A lo largo del desarrollo de la presente tesis se ha podido comprobar

como existen numerosos trabajos científicos en los que se recurre a las

desparasitaciones como parte del estudio, tratando de evaluar el efecto que la

eliminación de los parásitos tendría sobre el éxito reproductor, la condición

física o cualquier otro parámetro. Por contra, apenas hay unos pocos estudios

en los que se evalúe la eficacia del fármaco utilizado o las posibles limitaciones

de los métodos diagnósticos utilizados. Como ya hemos mencionado

anteriormente, este vacío hace que los protocolos profilácticos utilizados en

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fauna silvestre sean inadecuados. Así pues, nos parece muy importante que

una parte del esfuerzo investigador en fauna silvestre se centre en tratar de

encontrar protocolos de tratamiento mejores a los actuales puesto que es poco

probable que la industria farmacológica lo haga, y la falta de estos protocolos

puede suponer un grave problema de conservación.

• Evaluación del papel de las repoblaciones como focos de introducción

de otros patógenos, tales como bacterias o virus.

Por motivos económicos y de tiempo, esta tesis tuvo que centrarse en el

estudio de los parásitos, pero parece lógico pensar que otros agentes

patógenos, como bacterias o virus, puedan estar siendo también introducidos

en el campo con la suelta de aves de granja. Teniendo en cuenta que dentro de

los agentes infecciosos que afectan a las perdices en granja se encuentran

varias enfermedades de declaración obligatoria (Bronquitis infecciosa aviar,

enfermedad de Gumboro, clamidiosis aviar, enfermedad de Marek, enfermedad

de Newcastle, influenza aviar, laringotraqueítis infecciosa, micoplasmosis aviar,

tifosis aviar…) para las cuales existe además plan de erradicación en España,

parece lógico pensar que la importancia que tendría la introducción de estas en

el campo sería grandísima.

• Divulgación de los trabajos científicos en los colectivos implicados.

En muchos casos, cuando un gestor de caza se plantea soltar perdices de

granja en la finca o coto que gestiona lo hace porque piensa que es una buena

actuación y que con esa suelta está colaborando a la conservación de la

especie. Esa idea está, por desgracia, muy generalizada en el colectivo de

gestores y cazadores, y no hay otra causa que la amplia divulgación que se le

da dentro de la prensa del sector. Basta con ojear cualquier revista relacionada

con la caza para comprobar cuan numerosos son los artículos en los que se

alaban las extraordinarias tasas de supervivencia y capacidad de vuelo de las

perdices de tal o cual criador. Sin embargo, apenas aparecen unos pocos

artículos en los que se cuestione la idoneidad de estas actuaciones o en los

que se analice científicamente la viabilidad de las sueltas. Por el contrario,

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cuando revisamos la bibliografía científica acerca del tema ocurre lo contrario;

encontramos numerosos trabajos en los que se demuestra la escasa

supervivencia de las aves criadas en granja y los graves riesgos que estas

actuaciones pueden suponer para las poblaciones naturales pero no

encontramos ni un solo trabajo en el que se demuestre lo contrario. Así pues,

una de las primeras actuaciones que el colectivo científico debería llevar a cabo

para conservar la perdiz roja sería divulgar sus trabajos en medios accesibles

al colectivo de cazadores, que es al final quien decide si suelta o no aves de

granja en su acotado.

• Evaluación de medidas de gestión alternativas a las sueltas.

Se ha puesto de manifiesto el papel clave del modelo de agricultura

tradicional con alternancia de cultivos sobre la abundancia de perdiz roja, pero

todavía no existen trabajos en los que se actúe experimentalmente sobre los

hábitats tratando de mejorar su potencialidad para la perdiz roja y otras

especies ligadas a los medios agrarios. Resulta triste que, debido a este vacio

de conocimiento científico, la administración apenas sepa qué medidas exigir

para el cumplimiento de la “Directiva Aves” (79/409/CEE del Consejo, de 2 de

abril de 1979) y a la “Directiva Hábitats” (92/43/CEE del Consejo, de 21 de

mayo de 1992) requisito necesario para el cobro de las ayudas europeas. Así

pues, sería muy necesario analizar científicamente la idoneidad de distintas

actuaciones, tales como el mantenimiento de bandas sin cultivar, el uso de

cultivos alternativos o la modificación de alguna práctica agrícola, de cara a

tratar de incluirlas, bien dentro de las medidas obligatorias de “condicionalidad

de la PAC” o bien dentro de las medidas opcionales y subvencionadas por el

plan de desarrollo rural (PDR).