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Effects of Different Pastures Management on Dung Beetle Communities in a Sub-Mountainous Landscape of Central Italy: a Multicomponent

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Effects of Different Pastures Management on Dung Beetle Communities in a Sub-Mountainous Landscape of Central Italy: a Multicomponent EFFECTS OF DIFFERENT PASTURES MANAGEMENT ON DUNG BEETLE COMMUNITIES IN A SUB-MOUNTAINOUS LANDSCAPE OF CENTRAL ITALY: A MULTICOMPONENT BIODIVERSITY AND ECOLOGICAL PROCESS ANALYSIS Mattia Tonelli Universitat d’Alacant Universidad de Alicante EFFECTS OF DIFFERENT PASTURES MANAGEMENT ON DUNG BEETLE COMMUNITIES IN A SUB-MOUNTAINOUS LANDSCAPE OF CENTRAL ITALY: A MULTICOMPONENT BIODIVERSITY AND ECOLOGICAL PROCESS ANALYSIS Mattia Tonelli Tesis doctoral Alicante, febrero 2017 Instituto de Investigación CIBIO (Centro Iberoamericano de la Biodiversidad) Y Dipartimento di Scienze Pure e Applicate Tesis en cotutela: Università degli Studi di Urbino “Carlo Bo” y “Universidad de Alicante” Effects of different pastures management on dung beetle communities in a sub-mountainous landscape of central Italy: a multicomponent biodiversity and ecological process analysis Mattia Tonelli Tesis presentada para aspirar al grado de DOCTOR POR LA UNIVERSIDAD DE ALICANTE BIODIVERSIDAD: CONSERVACIÓN Y GESTIÓN DE LAS ESPECIES Y SUS HÁBITAT Dirigida por: Prof. José Ramón Verdú Faraco Prof. Mario Zunino Centro Iberoamericano de la Dipartimento di Scienze Pure e Biodiversidad Applicate CIBIO (Universidad de Alicante) Università degli Studi di Urbino “Carlo Bo” Alicante, febrero 2017 A te vengo, balena che tutto distruggi ma non vinci: fino all’ultimo lotto con te; dal cuore dell’inferno ti trafiggo; in nome dell’odio, vomito a te l’ultimo mio respiro (Herman Melville) …nulla si può tentare se non stabilire l’inizio e la direzione di una strada infinitamente lunga. La pretesa di qualsiasi completezza sistematica e definitiva sarebbe, se non altro, un’illusione. Qui il singolo ricercatore può ottenere la perfezione solo nel senso soggettivo che egli comunichi tutto ciò che è riuscito a vedere. (Georg Simmel) Al coraggio di un pettirosso da combattimento INDEX Resumen…………………………………………………………………………………....1 Chapter 1: General introduction and objectives……………………………………...........7 Chapter 2: Effects of grazing intensity and the use of veterinary medical products on dung beetle biodiversity in the sub-mountainous landscape of Central Italy………….....……..27 Chapter 3: Effects of progressive grazing abandonment on dung beetle biodiversity in a central Italian province: nesting behavior and body size matters………………………....69 Chapter 4: The effects of grazing intensity and historical veterinary medical products use on dung beetle functional diversity and ecological process………………………...........113 Chapter 5: The effects of progressive grazing abandonment on dung beetle functional diversity and ecological process………………………………………………………….145 Chapter 6: General discussion and conclusions…………………………………………177 Annex 1: Catalog, biology and phenology of the species………………………………..193 Annex 2: Selected and measured functional traits……………………………………….317 Acknowledgments……………………………………………………………………….343 RESUMEN RESUMEN Los escarabajos coprófagos (Coleoptera: Scarabaeoidea) son un grupo de insectos muy importante en términos de diversidad y biomasa en los pastos de la cuenca del Mediterráneo. A través del uso de estiércol como recurso trófico y para nidificar, estos organismos están involucrados en numerosos procesos ecológicos relacionados con la degradación del estiércol, tales como en el ciclo de nutrientes, en la dispersión secundaria de semillas, contribuyen mejorando la estructura del suelo, en la reducción de emisión de gases de efecto invernadero, así como en el control de endo-ecto parásitos del ganado. A pesar de su importancia ecológica, los escarabajos coprófagos están amenazados por varios factores, entre los cuales se destacan los cambios en el manejo de la ganadería tradicional. En las últimas décadas, la ganadería tradicional ha sufrido cambios radicales debidos principalmente a dos procesos: el abandono progresivo de la ganadería y su intensificación. Por un lado, el abandono progresivo de la ganadería tradicional es un factor clave en la conservación de los escarabajos coprófagos. Debido a la dependencia que este grupo de insectos tiene con el estiércol, este factor llevaría a una disminución del recurso trófico con repercusiones negativas para la comunidad coprófaga. Por millones de años los escarabajos coprófagos han dependido del uso de los excrementos de la megafauna salvaje, y desde su disminución, el estiércol de la ganadería doméstica ha sido su principal recurso trófico. A pesar de lo anterior, en los últimos 50 años, la ganadería tradicional ha comenzado un proceso de abandono progresivo, sobre todo en las áreas marginales como las de montaña. Por otra parte, el uso/abuso de productos médico veterinarios para el control de los endo- ecto parásitos del ganado es otro factor importante en tema de conservación de la fauna coprófaga y está relacionado con la intensificación de la ganadería. Estos compuestos médico veterinario, entre los cuales destaca por importancia la ivermectina, son eliminados progresivamente en las heces de los organismos. Estudios recientes han demostrado que los 1 residuos de algunos de estos compuestos tienen efectos sub-letales y letales sobre la fauna coprófaga y sobre todo en los escarabajos. A pesar de la importancia que estos dos factores pueden tener para la conservación de los escarabajos coprófagos, pocos estudios comparativos han investigado el impacto sobre las comunidades de este grupo y como consecuencia sobre el papel ecológico en los cuales están involucrados. Debido a este vacío de conocimiento, el objetivo general de esta tesis fue evaluar los efectos del abandono de la ganadería, su extensificación y uso histórico de productos médico veterinarios sobre las comunidades de escarabajos coprófagos usando medidas de biodiversidad y cuantificando la capacidad de remoción de estiércol en un paisaje sub-montano de la provincia de Pesaro-Urbino (Italia). Después de una introducción general (Capítulo 1) en los capítulos 2 y 3 de esta tesis se abordan los efectos de los diferentes métodos de manejo de la ganadería y se analiza el impacto de estos factores sobre la diversidad alfa y beta, abundancia y biomasa, especies indicadoras, grupos funcionales y clases de tallas de las especies. En los capítulos 4 y 5 se evalúan los efectos de estos factores desde una perspectiva funcional, analizando la diversidad funcional de las comunidades y el desempeño que cada comunidad tiene en la remoción del estiércol. Así mismo, se analizaron las relaciones entre varias medidas de diversidad funcional y de diversidad clásicas (número de especies y diversidad de Shannon) y la relación entre la diversidad funcional y el proceso ecológico. En este trabajo se colectaron un total de 156 936 individuos, pertenecientes a 58 especies de escarabajos coprófagos (3 Geotrupinae; 16 Scarabaeinae; 39 Aphodiinae) y por primera vez se cita Calamosternus mayeri (Pilleri, 1953) en la región Marche. Los resultados de este trabajo sugieren que el uso histórico de productos médico veterinarios tiene un impacto negativo y ubiquitario sobre todas las especies de la comunidad de estudio, llevando a un empobrecimiento de los ensambles y a una pérdida de abundancia y biomasa. No 2 obstante se ha registrado el mantenimiento de la estructura de la comunidad. Estos resultados son corroborados igualmente cuando nos enfocamos en la diversidad funcional. En efecto, el uso histórico de productos médico veterinarios lleva a una pérdida en el número de roles funcionales dentro de la comunidad, sin embargo las abundancias se encuentran repartidas equitativamente dentro de cada nicho funcional. Todos estos efectos sobre la comunidad de escarabajos coprófagos debido al uso de productos médico veterinarios, al final quedan reflejados en una pérdida del 70% en la capacidad de remoción de estiércol, comparados con áreas donde estos productos no son aplicados. La extensificación de la ganadería está representada por áreas que tienen una intensidad de pastoreo muy baja, las cuales pueden ser consideradas como la primera etapa hacia el abandono completo. En este sentido, los resultados de este trabajo demuestran como una simple reducción de la carga ganadera lleva a efectos negativos sobre las comunidades de escarabajos coprófagos, registrando una disminución en la diversidad alpha y en el número de especies indicadoras. Esta disminución en la cantidad de recurso trófico tiene implicaciones sobre la composición de la comunidad, favoreciendo especies oportunistas cuya biología le permite evitar la competencia, como por ejemplo; especies cleptoparásitas o especies cuyas larvas tienen un comportamiento saprófago. Este “efecto filtro” (filter effect) debido a la disminución de la cantidad trófica, está confirmado por los resultados de diversidad funcional, en los cuales se registró una disminución en el número de nichos funcionales y una fuerte redundancia por la presencia de nichos funcionales muy similares entre ellos. Los efectos sobre la comunidad de escarabajos coprófagos en los sitios con baja carga ganadera reflejan finalmente una pérdida en la capacidad de enterramiento del estiércol del 30-40% respecto a las comunidades en áreas con una mayor carga ganadera. Los resultados de este trabajo muestran que en las áreas con abandono total de la ganadería se observó una disminución en el número de especies, en la abundancia y biomasa total, en el número de especies indicadoras, en la abundancia de las especies de gran tamaño 3 y en las especies que no tienen un comportamiento de nidificación durante el periodo reproductivo. Sin embargo, el mantenimiento de una comunidad bien estructurada, subraya la
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