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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.
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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
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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.
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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
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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).
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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
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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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2,5
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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).
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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
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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
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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
0
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1987 1988 1989 1990 1991 1992 1993 1994 1995 1996
Lagó
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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).
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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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Alectoris rufa releases on steppe bird conservation?. Ibis (in press) doi:
10.1111/j.1474-919x.2006.00620.x
35. Villanúa, D., Pérez-Rodríguez, L., Rodríguez, O., Viñuela, J. & Gortazar, C. (2007b) How effective is pre-release nematode control in
farm reared red-legged partridges (Alectoris rufa)?. Journal of
Helminthology, 81(1): 101-3
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
-2
0
2
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6
8
10
C. g
ruve
li
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±SE
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etra
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Wild
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Managed-1,5
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ruve
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Mean
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Managed-1,5
-1,0
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0,0
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2,0
R. t
etra
gona
Wild
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
40
50
RB
MTL
Managed
21
22
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Wild
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±SE
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Mean
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±SD
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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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.
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36. Villanúa, D., Acevedo, P., Höfle, U., Rodríguez, O. & Gortázar, C. (2006). Changes in transmission stage excretion after pheasant release. Journal of
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37. Vorísek, P., Votýpka, J., Zvára, K. & Svobodova, M. (1998). Heteroxenous coccidia increase the predation risk of parasited rodents.
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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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survival of farm-reared red-legged partridges (Alectoris rufa). Journal of
Comparative Biochemistry and Physiology, 134: 85-91.
68
7. 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.
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).