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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO EN CIENCIAS BIOLÓGICAS INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS Y SUSTENTABILIDAD ECOLOGÍA INTERACCIONES ENTRE VERTEBRADOS Y ENCINOS BAJO DIFERENTES NIVELES DE PERTURBACIÓN HUMANA TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTORA EN CIENCIAS PRESENTA: ELISA MAYA ELIZARRARÁS TUTOR PRINCIPAL DE TESIS: DR. JORGE ERNESTO SCHÖNDUBE FRIEDEWOLD INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS, UNAM COMITÉ TUTOR: DR. ALBERTO KEN OYAMA NAKAGAWA ESCUELA NACIONAL DE ESTUDIOS SUPERIORES, UNAM DR. DAVID VALENZUELA GALVÁN CENTRO DE INVESTIGACIÓN EN BIODIVERSIDAD Y CONSERVACIÓN, UAEM Morelia, Michoacán. Mayo, 2017 UNAM – Dirección General de Bibliotecas Tesis Digitales Restricciones de uso DERECHOS RESERVADOS © PROHIBIDA SU REPRODUCCIÓN TOTAL O PARCIAL Todo el material contenido en esta tesis esta protegido por la Ley Federal del Derecho de Autor (LFDA) de los Estados Unidos Mexicanos (México). El uso de imágenes, fragmentos de videos, y demás material que sea objeto de protección de los derechos de autor, será exclusivamente para fines educativos e informativos y deberá citar la fuente donde la obtuvo mencionando el autor o autores. Cualquier uso distinto como el lucro, reproducción, edición o modificación, será perseguido y sancionado por el respectivo titular de los Derechos de Autor. ~ ii ~ ~ iii ~ UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO EN CIENCIAS BIOLÓGICAS INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS Y SUSTENTABILIDAD ECOLOGÍA INTERACCIONES ENTRE VERTEBRADOS Y ENCINOS BAJO DIFERENTES NIVELES DE PERTURBACIÓN HUMANA TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTORA EN CIENCIAS PRESENTA: ELISA MAYA ELIZARRARÁS TUTOR PRINCIPAL DE TESIS: DR. JORGE ERNESTO SCHÖNDUBE FRIEDEWOLD INSTITUTO DE INVESTIGACIONES EN ECOSISTEMAS, UNAM COMITÉ TUTOR: DR. ALBERTO KEN OYAMA NAKAGAWA ESCUELA NACIONAL DE ESTUDIOS SUPERIORES, UNAM DR. DAVID VALENZUELA GALVÁN CENTRO DE INVESTIGACIÓN EN BIODIVERSIDAD Y CONSERVACIÓN, UAEM Morelia, Michoacán. Mayo, 2017 ~ iv ~ UNAM POSGR DO Ciencias ~iológicas Lic. Ivonne Ramírez Wence Di rectora General de Administración Escolar, UNAM Pr ese nte COORDINACIÓN Por medio de la presente me permito informar a usted. que el Subcomité de Biologia Experimental y Biomedicina del Posgrado en Ciencias Biológicas, en su sesión ordinaria del dia 13 de febrero de 2017, aprobó el jurado para la presentación del examen para obtener el grado de DOCTORA EN CIENCIAS a la alumna MAYA ELlZARRARÁS ELlSA, con número de cuenta 508019517, con la tesis titulada. "Interacciones entre vertebrados y encinos bajo diferentes niveles de perturbación humana", bajo la dirección del Dr. Jorge Ernesto Schondube Friedewold, Tutor principal. Presidente: Dr. Roberto Antonio Lindig Cisneros Dra. Ellen Andresen Vocal: Secretario: Dr. David Valenzuela Galván Dra. Julieta Benitez Malvido Dra. Katherine Rentan Suplente: Suplente: Sin otro particular, quedo de usted. Atentamente "POR MI RAZA HABLARÁ EL EspíRITU" Cd. Universitaria. Cd. Mex., a 03 de mayo de 2017 Dra. María del Coro Arízmendí Arriaga Coordinadora del Programa COOROINACION Unidad de Posgrado' Coordinación del Posgrado en Ciencias Biológicas Edificio D, ler. Piso, Circuito de Posgrados Cd. Universitaria Delegación Coyoacán C.P. 04510 México, n.F. Tel. 5623 7002 http://pcbiol.posgrado.unam.mx ~ v ~ AGRADECIMIENTOS INSTITUCIONALES Al Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México Al Instituto de Investigaciones en Ecosistemas y Sustentabilidad Al Consejo Nacional de Ciencia y Tecnología por el apoyo otorgado a través de una beca de posgrado (CVU: 250180). A mi tutor Dr. Jorge Ernesto Schondube Friedewold A mi comité tutoral, Dr. David Valenzuela Galván y Dr. Alberto Ken Oyama Nakagawa ~ vi ~ AGRADECIMIENTOS A TÍTULO PERSONAL Agradezco a mis papás, Verónica y Baldemar, por darme en todo momento su apoyo incondicional, por sus experimentados consejos, por su amor prodigado a lo largo de toda mi vida, por ser mis primeros maestros, de vida, pero también académicamente. Espero que este producto y lo que de ello derive, reditúe de algún modo todo lo que me han dado a manos abiertas. Los cimientos de mi proceso académico se los debo a ustedes. Gracias. A mis hermanos Luis y Balde por sus enseñanzas de vida, por su camaradería, por estar conmigo en las buenas y en las malas, por acompañarme en mi trabajo de campo, por aguantarme en mis momentos de insoportable, sensible y exigente, por su apoyo incondicional a distancia. A Karen, mi cuñada, por los buenos momentos compartidos. A mis grandes familias Maya y Elizarrarás, abuelos (as), tíos (as), primos (as) y sobrinos (as), porque su palabra amiga y su apoyo incondicional me brindan bienestar. A mis compañeros del laboratorio de ecología funcional. Gracias por su valiosa amistad. 10 años, entre maestría y doctorado, que resumen tantas bienvenidas y despedidas, cumpleaños, convivencias, proyectos en común, viajes, acuerdos y desacuerdos, enseñanzas mutuas, esperanzas y desesperanzas, ilusiones y desilusiones, trabajo y puntos de vista a veces muy diversos. Ojalá colaboremos en futuros proyectos y que nuestros re-encuentros sean siempre agradables. Si he olvidado algún nombre, con antelación ofrezco una disculpa: Caheri López, Carlitos Chávez, Claudia Tapia, Conchita Pérez, Héctor Perdomo, Ian MacGregor, Javi Quesada, Jorgito Ayala, Lety Mirón, Lore Morales, Luz López, Mariano Mejía, Memo Domínguez, Moni Orduña, Nelly Peña, Nicoletta Righini, Nubia Medina, Omar Maya, Pau Cerna, Rafa Bribiesca, Rodrigo Pacheco, Romeo Saldaña y Stephi Ortega. En especial a los biólogos Luz Elena López y Raúl Valdés por darme la oportunidad de dirigir sus tesis de licenciatura. Experiencia inigualable de aprendizaje mutuo y que gracias a la convivencia pudimos cultivar una amistad. Gracias Jorge Chon, aceptarme en tu laboratorio hizo que conociera a estas extraordinarias personas. A Jorge Schondube por su amistad y por tantos momentos compartidos. Gracias por permitirme poner a prueba mi determinación en el seguimiento de mis objetivos. Porque a través de tu ejemplo me quedó claro que debo hacer aquello que me apasione, con organización y disciplina, así como cumplir a cabalidad los compromisos que adquiera. De otro modo defraudo a los que de mi dependen y a mi misma. ~ vii ~ A mi jurado de examen de candidatura, Dr. Antonio González Rodríguez, Dr. Carlos Alberto Lara Rodríguez, Dr. Jorge Humberto Vega Rivera, Dr. Efraín Tovar Sánchez y Dr. David Valenzuela Galván. Su retroalimentación en este proceso académico me impulsó a seguir adelante con mayor determinación. A mi jurado de examen de grado, Dr. Roberto Antonio Lindig Cisneros, Dra. Katherine Renton, Dra. Julieta Benítez Malvido, Dra. Ellen Andresen y Dr. David Valenzuela Galván, porque sus comentarios y sugerencias ayudaron a lograr una mejor versión de este trabajo. A la Dra. Nicoletta Righini por su invaluable y desinteresada ayuda para mejorar esta tesis. A Leonarda Terán Cárdenas por su buena atención siempre y por su ayuda en este proceso de titulación. A mis amigos Aleyda Barraza, Clau Molina, Diego Rocha, Edgar Godínez, Javier Cedeño, Lety Mirón, Lilia Ábrego, Lore Morales, Luz Hinojosa, Manuel Anguiano, Mauricio Chávez, Miguel Montes, Ramiro Cortés y Yuri González. Porque poder haber compartido con ustedes aspectos de vida tan diferentes y experiencias tandiversas, fueron causa de des-estrés, alegría y diversión. A la tropa scout Adzumayama-Makalú (2010-2015), gracias por hacerme sonreír y empujarme siempre a superarme y ver el lado amable de la vida. Aunque fue difícil dedicar el tiempo necesario a cada planeación, actividad, excursión, campamento y evaluación, valió la pena. Agradezco la enorme oportunidad que me dieron para compartir un trecho del camino. Un trecho de su travesía scout. Así como a Karen, Scooby y Tere, miembros del clan rover Carapan (2017), porque me hicieron recordar que el ejemplo es la mejor forma de guiar, y de este modo fueron mi aliciente a cada momento, recordándome que no debo dejar desfallecer mis proyectos por falta de constancia o disciplina. “Són molts els qui no troben el seu cor fins a després d'haver perdut el cap.” Nietzsche ~ viii ~ DEDICATORIA A mis cuatro abuelos, cuyo ejemplo me inspira y cuya fortaleza me enorgullece Concepción Alvarado Elisa Flores David J. Elizarrarás † Eliseo Maya “Hegoak ebaki banizkio, Nerea izango zen, Ez zuen aldegingo. Bainan honela, Ez zen gehiago txoria izango. Eta nik… txoria nuen maite.” Mikel Laboa ~ ix ~ ÍNDICE Resumen x Abstract xi Introducción 1 Alteración del hábitat por extracción de carbón vegetal 3 Cambio de uso de suelo por actividades pecuarias 6 Presentación de la tesis 7 Capítulo I Vertebrates in conserved and managed oak forests:A review 9 Introduction 11 Methods 12 Vertebrates in conserved oak forests 13 Vertebrates in managed oak forests 16 Conclusions 27 References 30 Capítulo II Birds, charcoal and cattle: bird community responses to human activities in an oak forest landscape shaped by charcoal extraction 41 Introduction 43 Methods 44 Results 47 Discussion 53 References 59 Appendix A 64 Capítulo III Changes in bird community behavior in response to oak-forest anthropogenic habitat modification: Drawing a bridge between community ecology, behavior and forest management 67 Introduction 69 Methods 71 Results 76 Discussion 85 References 94 Appendix A 102 Conclusiones 107 Vertebrados en encinares alrededor del mundo 107 Aves, carbón vegetal y ganado 108 Comportamiento de las comunidades de aves 110 Referencias exclusivamente citadas en la introducción 112 ~ x ~ RESUMEN Los bosques de encino presentan una gran diversidad florística, fisonómica y ecológica, y la importancia que muchas especies de encino tienen para la vida silvestre las ha posicionado como especies clave en sus hábitats naturales. Este tipo de vegetación es uno de los cinco hábitats con mayor riqueza aviafunística en todo el Neotrópico y el que presenta mayor riqueza de endemismos para México. No obstante, alrededor del mundo, importantes agentes relacionados con el cambio global han contribuido a la destrucción de estos bosques y su biodiversidad. En esta tesis doctoral se aborda uno de los principales procesos de cambio global, el cambio de uso de suelo, expresado a través de dos escenarios: a) la alteración y cambio del bosque de encino, a partir de procesos de extracción de leña para la producción de carbón vegetal, y b) la modificación del bosque para la creación y mantenimiento de potreros. Se encontró que las actividades antropogénicas desarrolladas en los encinares, afectaron las comunidades de aves que habitan estos bosques, disminuyendo la riqueza de especies, alterando la estructura de sus comunidades y su diversidad funcional. Adicionalmente, de forma novedosa, se comparó el comportamiento de la avifauna a nivel de comunidad, utilizándolo como un indicador de la respuesta de las aves a perturbaciones antropogénicas de sus hábitats. Los resultados sugieren cambios de comportamiento en las comunidades de aves asociados a las actividades de producción de carbón y pastoreo. De continuar llevándose a cabo, estas actividades podrían disminuir la complejidad de las comunidades de aves de estos hábitats, donde el forrajeo y la anidación de las especies ya ha sido afectado por cambios en la estructura del bosque. Nuestras sugerencias se centran en: 1) mantener parches de bosque maduro donde se excluyan las actividades productivas, 2) mantener encinos grandes (> 40cm DAP) dispersos en todos los hábitats bajo manejo, 3) permitir el desarrollo de arbustos en todos los hábitats, fomentando la riqueza y cobertura de este estrato vegetal, y 4) limitar el pastoreo en las áreas con arbustos, permitiendo así que los hábitats provean de recursos para forrajeo y anidación a las especies de aves que ahí habitan. Esto permitiría mantener comunidades de aves más complejas y diversas en el paisaje. ~ xi ~ ABSTRACT Oak forests present a great floristic, physiognomic and ecological diversity, and the importance that many species of oak trees have for different wildlife species, make these trees key species in several natural habitats. Oak forest is the fifth habitat in relation to bird species richness in the Neotropics, and the habitat with the highest number of endemic bird species for Mexico. However, all around the world, major agents of global change have been important factors in the destruction of oak forests and the biodiversity associated to them. This doctoral thesis addresses one of the main processes related to global change, land-use change, expressed through two scenarios: a) the alteration and change of oak forest caused by the extraction of wood to produce charcoal, and b) the modification of oak forest for the creation, and maintenance, of cattle-grazing areas. We found that these two anthropogenic activities had effects on the bird communities that inhabit these forests, decreasing species richness, altering the structure of their communities and their functional diversity. Additionally, we applied a novel approach, the use of bird community behavior as an indicator of the level of habit alteration by anthropogenic activities, to measure bird responses, and generate management actions for bird conservation. Our results indicate intense behavioral changes in bird communities associated to charcoal production and cattle-grazing activities. If these human activities continue, they could reduce the complexity of the bird communities present in these habitats, where bird foraging and nesting activities have been affected by a reduction in forest structural complexity. We propose the need to: 1) maintain patches of mature forest where human activities are excluded, 2) maintain large oak trees (> 40 cm DBH) in all habitats, 3) allow the growth of different shrub species in all habitats, promoting an increase in shrub cover and species richness, and 4) limiting cattle-grazing on areas with shrubs, allowing the existence of key resources needed for foraging and nesting by the bird species. These actions could generate more diverse and complex bird communities in the landscape. ~ 1 ~ INTRODUCCIÓN Los bosques de encino son comunidades vegetales características de las zonas montañosas de México, y cubren cerca del 5.5% del territorio nacional (sensu Flores et al. 1971 en Rzedowski 2006, Rzedowski 1978, Valencia 2004, Sánchez et al. 2009). Se encuentran encinares en casi todas las zonas de bosques templados del hemisferio norte, así como en regiones tropicales y subtropicales del planeta (Valencia 2004). Estos bosques de encino presentan una gran diversidad florística, fisonómica y ecológica, representando uno de los tipos de vegetación con más alta diversidad β del país (Flores and Gerez 1994, Valencia 2004, Arriaga et al. 2009). En el caso de México esto es muy relevante dada la gran riqueza de especies de encinos que presenta nuestro país, más de 160 especies, constituyéndose como uno de los centros más importantes de diversificaciónpara el género Quercus (Valencia 2004). La importancia que muchas especies de encino tienen para la vida silvestre las ha posicionado como especies clave en sus hábitats naturales. Alrededor del mundo se han desarrollado múltiples trabajos de inventarios sobre comunidades de vertebrados e invertebrados asociados a encinares bajo diferentes escenarios de conservación (Block and Morrison 1987, Tietje and Vreeland 1997, García et al. 1998, Tovar-Sánchez et al. 2003, Zack et al. 2005, Tempel et al. 2006, Johnson et al. 2008, Urbina-Cardona and Flores-Villela 2010). Algunos de estos trabajos incluso documentan cómo inciden los diferentes tipos de manejo del bosque de encino sobre la composición y estructura de las comunidades de fauna que en él habitan (Sánchez and Tellería 1988, Vreeland and Tietje 2002, McShea et al. 2007). Sin embargo, la forma en que los animales utilizan estos bosques es básicamente desconocida en el continente Americano. De este modo, el conocimiento que tenemos sobre el papel que los encinares tienen para mantener la diversidad de fauna al funcionar como sitios de anidación (Ramos-Lara and Cervantes 2007, Hocking et al. 2008, Purcell and Verner 2008), sitios de refugio o descanso, sitios de forrajeo, o bien en relación a la producción de bellotas que funcionan como una importante fuente de alimentación para un gran número de especies, es limitado en su área de mayor diversidad (Santos and Tellería 1997, Schmidt and Timm 1991, Longcore and Rich 2003, Haas and Heske 2005, López- Barrera and Manson 2006, Caprio et al. 2009). ~ 2 ~ Este tipo de vegetación guarda una alta relevancia para la avifauna, siendo uno de los cinco hábitats con mayor riqueza aviafunística en todo el Neotrópico y el que presenta mayor riqueza de endemismos para México (Flores and Gerez 1994, Stotz et al. 1996). Sin embargo, estos bosques cubren menos del 10% del total de la superficie de las áreas naturales protegidas de la República Mexicana (Arriaga et al. 2009). Las comunidades avifaunísticas desarrollan importantes funciones ecológicas en los ecosistemas al actuar como dispersoras de semillas, polinizadoras, controladoras de plagas y fuente de alimento para una gran variedad de animales carnívoros. Además, debido a que las aves pueden desplazarse grandes distancias y tienden a responder rápidamente a cambios en su ambiente, pueden ser utilizadas como un taxón indicador del grado de conservación de un ambiente (Temple and Wiens 1989). No obstante, aunque la biología de diversas especies de aves es conocida (Skutch 1969, Howell and Webb 1995, Hilty and Wolf 2005), su interacción directa y el modo en que interaccionan con especies vegetales bajo diferentes condiciones de perturbación no ha sido ampliamente explorada en el país. Durante el siglo XX, y lo que va del XXI, la tala, los incendios forestales, la ganadería y la urbanización, han sido factores importantes en la destrucción de los bosques y su biodiversidad (Challenger 1998). Los bosques de encino no están a salvo de estos factores de disturbio pese a su antigüedad y a su amplia distribución alrededor del mundo (Shrestha and Paudel 1996, Abrams 2003, Valencia 2004). De hecho, los bosques de encino son uno de los tipos de vegetación más afectados por actividades agropecuarias y por la extracción de madera, lo que hace crucial estudiarlos a fondo (Sánchez et al. 2009). En los bosques de encino de nuestro país, el aprovechamiento forestal se ha dado principalmente a través de la explotación local para la elaboración de artesanías, duelas, horcones, cabos de herramientas, cercas, ejes de carreta o insumo para obtención de celulosa (Espejel-Rodríguez et al. 1999, Arizaga et al. 2009). Sin embargo, de manera generalizada y común en el país, se ha utilizando de manera prioritaria a los encinos como combustible, de manera directa por medio de la extracción de leña, o transformando su madera en carbón (Rzedowski 1978). La producción de carbón es una de las causas principales de la deforestación de grandes extensiones de encinares en las últimas décadas en México (Rzedowski 1978, Works and Hadley 2004, Challenger et al. 2009). ~ 3 ~ Los ecosistemas del mundo han sido transformados de manera dramática desde hace cientos de años. Esta transformación ha estado caracterizada por un intenso uso de la tierra, y cambios drásticos en la vegetación, registrando en las últimas décadas un impacto global dramático donde más del 80% de la superficie terrestre se ha transformado, con un notable decremento de la biodiversidad (Sanderson et al. 2002, Foley et al. 2005, Challenger et al. 2009). Actualmente, diversas actividades humanas, tales como el cambio de uso del suelo, el cambio climático, la sobre-explotación de recursos, la invasión de especies exóticas y los agentes de polución, contribuyen a la destrucción de los hábitats naturales, incrementando la amenaza sobre la biodiversidad (Sala et al. 2000, Millenium Assessment 2005, Challenger 1998). Para efectos de esta tesis, se abordó el efecto que el cambio de uso de suelo y la sobre-explotación de recursos tiene sobre las comunidades de aves que habitan en bosques de encino a través de estudiar dos escenarios relevantes: a) la alteración y cambio del bosque de encino, a partir de procesos de extracción de leña para transformarla en carbón vegetal, y b) el cambio de uso de suelo del bosque para la creación y mantenimiento de potreros. 1. Alteración del hábitat por extracción de carbón vegetal En países en desarrollo como México, cerca del 80% de la madera extraída de los bosques de encino es utilizada para la obtención de leña y carbón vegetal, siendo esta última, una de las principales actividades económicas relacionadas al uso de la madera de encino en México (Aguilar et al. 2012). Puntualmente, en las zonas templadas del estado de Michoacán, hasta 89% de las comunidades humanas prefieren utilizar como combustible a los encinos sobre otras especies vegetales (Masera et al. 1997, Espejel- Rodríguez et al. 1999, García 2007). Quercus castanea es una de las especies preferidas para obtención de combustible en varias localidades, dado que es considerada como una especie que presenta una mayor duración de combustión, que arde con mayor intensidad y que suele ofrecer más calor (García 2007). En relación a la obtención de carbón vegetal, Aus der Beek et al. (2006), mencionan que las especies maderables de hoja ancha, como los encinos parecen ser las mejores y más utilizadas para la producción de carbón vegetal debido a la alta densidad de su madera y su alto contenido de lignina. Adicionalmente, esta preferencia de uso puede deberse a que la madera de encino suele tener buenas características de ~ 4 ~ combustión y a una capacidad de rebrote de los árboles podados, lo que permite ciclos relativamente cortos de cosecha (Aguilar et al. 2012). Sin embargo, existen muchos factores que influyen sobre la exitosa regeneración de los bosques de encino después de la poda o tala, como son la especie de encino, la edad del individuo, la extensión del sistema radicular que permanece después de la poda, el número de ciclos de poda, el desarrollo de los meristemos, la incidencia de incendios y plagas, el sobrepastoreo y las condiciones abióticas del sitio (lluvia, temperatura, radiación solar y fertilidad del suelo; Aguilar et al. 2012). Así mismo, los ciclos de disturbios y los ciclos de rotación de poda son factores que influyen sobre la capacidad de rebrote de los individuos y de las poblaciones de encinos (Kubo et al. 2005). Los ciclos de rotación de poda por lo general tienen una duración de entre 8 y 30 años (García 2007), tiempo que permite un desarrollo suficiente del diámetro a la altura del pecho (DAP) de los encinos para que el carbón sea producido (Aguilar et al. 2012). El método más conocidoy utilizado, y probablemente el más antiguo para obtención de carbón en el mundo (FAO 1985 en Aus Der Beek et al. 2006), es el tradicional horno construido como un hoyo en la tierra. Sin embargo, esta técnica involucra dos principales impactos ecológicos, a) el uso intensivo de los encinos en regeneración, y b) el efecto negativo sobre la regeneración natural de los alrededores. Esto merma la capacidad misma de rebrote en las poblaciones y afecta la vegetación de alrededor de un horno, la cual es cortada para cubrir la madera que será carbonizada (García 2007). Así, la rotación de ciclos y la tala alrededor de los sitios de construcción de hornos moldea los paisajes carboneros, conformados por una colección de fragmentos de bosques secundarios de varios tamaños y formas, y con diferentes historias de uso, pudiendo llegar a constituir cronosecuencias sucesionales (Fig. 1). La sucesión ecológica se define como el cambio que sufre una comunidad biológica después de una perturbación. A lo largo de la sucesión, van cambiando la composición específica de la comunidad y la abundancia relativa de las especies (Horn 1974, Huston and Smith 1987, Villard et al. 1999). Los cambios en la vegetación generados por procesos de sucesión ecológica producen diferentes condiciones de hábitat que inducen respuestas notables en las especies de fauna que los habitan (Landres and MacMahon 1980, Rodewald and Brittingham 2004). Entre los trabajos que estudian comunidades de fauna en cronosecuencias sucesionales de encinares, está ~ 5 ~ el trabajo de Van Der Bergh and Kappelle (2006) llevado a cabo en un bosque de montaña en Costa Rica. Estos autores compararon los ensambles de pequeños roedores terrestres en cinco condiciones de hábitat, incluyendo áreas de pastoreo, encontrando que sólo una especie prefirió bosques maduros y que la heterogeneidad micro-ambiental de los hábitats fue relevante para la comunidad de roedores. Sin embargo, en México son pocos los trabajos que han evaluado el efecto que tiene la sucesión ecológica sobre las comunidades de fauna, particularmente en el caso de comunidades de aves de bosques templados. Asociado a este tema, se ha encontrado que existe un incremento de la diversidad y de la supervivencia de aves cuando incrementa la edad sucesional (Schweiger et al. 2000, Smith et al. 2001). Por el contrario, las abundancias de aves tienden a ser mayores en los sitios de sucesión temprana (Winker et al. 1990, Dunn 2004). Esto genera una dinámica de variación de riqueza y abundancia de aves a lo largo de gradientes sucesionales, que obedece a cambios en la estructura de la vegetación y a los movimientos temporales de las aves en el espacio (Smith et al. 2001, Bojorges and López-Mata 2005). Por otra parte, en respuesta al cambio de la estructura del hábitat y a la heterogeneidad ambiental creada por la perturbación, los recursos alimentarios disponibles cambian, y esto se ve reflejado en la proporción de especies de los diferentes gremios tróficos presentes en una comunidad de aves (Petit et al. 1999, Bojorges and López-Mata 2005, Arriaga-Weiss et al. 2008). En este sentido, existe un incremento de la diversidad de los gremios tróficos cuando se incrementa la complejidad estructural del hábitat, pues las etapas sucesionales más “complejas/viejas” ofrecen una mayor diversidad y abundancia de recursos alimenticios, en particular insectos y frutos (Petit et al. 1999, Smith et al. 2001). ~ 6 ~ 2. Cambio de uso de suelo por actividades pecuarias La transformación del hábitat y la deforestación debida al pastoreo por ganado, que a su vez cambian las asociaciones vegetales naturales, es una de las principales causas de pérdida de biodiversidad alrededor del mundo (Shrestha and Paudel 1996, Dunn 2004, David et al. 2007, García et al. 2008). La conversión a gran escala de vegetación natural a potreros altera la cantidad y calidad de hábitat disponible para aves, afectando negativamente las comunidades de aves reproductivas (Saab and Petit 1992). No obstante, los efectos del pastoreo sobre las comunidades de aves deben ser evaluados específicamente tanto para diferentes tipos de vegetación, como para las distintas especies, pues históricamente diversos ecosistemas han estado sujetos a presiones de pastoreo natural, por lo que la introducción de ganado doméstico puede ser tolerada en muchos casos (Saab et al. 1995). En el caso de los encinares mexicanos se ha reportado una declinación importante de poblaciones de encinos a causa de varios agentes bióticos y abióticos, entre los que destaca el sobrepastoreo (Alvarado-Rosales et al. 2007). En general los potreros representan un hábitat severamente degradado, donde si bien, las aves generalmente no responden a la presencia del ganado en sí mismo, el impacto del ganado sobre la estructura y composición de la vegetación, subsecuentemente afectan la diversidad de la avifauna local (Saab and Petit 1992, Martin and Possingham 2005, Saab et al. 1995). Los impactos que la transformación de hábitats naturales a potreros tiene sobre las comunidades de aves, dependen en gran medida de la identidad de las especies, pues mientras algunas especies son afectadas y tienden a desaparecer, otras no parecen ser sustancialmente afectadas por la ganadería (Saab and Petit 1992). Sin embargo, esto depende de la intensidad e historia de uso de cada potrero. Una alta presión de uso afecta a la mayoría de las especies de aves, disminuyendo la riqueza de especies (Martin and Possingham 2005). Esta pérdida de especies parece ser resultado de una depauperada estructura fisonómica y taxonómica de la vegetación, una diversidad limitada de recursos alimenticios, condiciones climáticas extremas y una gran exposición de las aves a los depredadores (Estrada et al. 1997). ~ 7 ~ Presentación de la tesis El primer capítulo de esta tesis comprende una revisión sobre los trabajos de investigación en los que se mencionan algunos de los efectos que el manejo antropocéntrico de los encinares tiene sobre las comunidades de vertebrados que los habitan en diferentes partes del mundo. La pregunta planteada en este capítulo es ¿Cómo afecta el manejo de los encinares a los vertebrados que habitan en ellos? En el segundo capítulo, exploramos cómo las comunidades de aves responden a la vegetación presente en una cronosecuencia sucesional de encinares, derivada de la extracción de madera para la obtención de carbón vegetal, y de las actividades agropecuarias. Las preguntas planteadas en este capítulo son: 1) ¿Cómo cambian la riqueza de especies, densidad de individuos, y estructura y composición de las comunidades de aves a causa de la extracción de carbón vegetal y el pastoreo por ganado en los encinares?, 2) ¿En qué medida son similares, taxonómica y funcionalmente, las comunidades de aves que habitan estos encinares perturbados? y 3) ¿Responden los diferentes componentes de la avifauna (aves residentes, migratorias Neotropicales y migratorias intratropicales) de forma similar o diferente a las perturbaciones de los encinares? Finalmente, el tercer capítulo, presenta una aproximación novedosa de observaciones conductuales de toda la comunidad de aves, como un indicador de la respuesta de la avifauna a la producción de carbón y el pastoreo de ganado (Fig. 2). Las preguntas planteadas en este último capítulo son: 1) ¿Cómo cambia el comportamiento de las comunidades de aves con diferentes niveles de disturbio humano?, 2) ¿Podemos identificar especies de aves que dirigen los cambios de comportamiento a nivel de las comunidades? Y finalmente, 3) ¿Qué conductas de las comunidades de aves son afectadas de manera prioritaria por la estructura del hábitat? Para responder estas preguntas, nuestro objetivo central fue analizar los efectos de dos promotores del cambiode uso del suelo (extracción de leña para carbón y uso de encinares como potreros) sobre las siguientes variables de respuesta de las comunidades de aves: a) la riqueza, densidad de individuos, dominancia y diversidad funcional de las comunidades de aves, así como b) las conductas asociadas a actividades de territorialidad, forrajeo y reproducción, analizados todos a nivel de comunidad. Los objetivos particulares, hipótesis y predicciones se mencionan a detalle en cada uno de los capítulos. ~ 8 ~ Figura 2. Contexto y ubicación del proyecto de investigación en el marco del conocimiento de los efectos de dos principales generadores antropogénicos del cambio global. Mediante una serie de mecanismos y procesos, como la alteración del hábitat a través de diferentes agentes de cambio de uso de suelo, se modifica la estructura del hábitat incidiendo sobre los individuos que afectan a su vez poblaciones, comunidades y en conjunto a toda la biodiversidad. Los recuadros sombreados representan tópicos que se abordaron en esta tesis. Las líneas punteadas representan los temas abordados en cada capítulo, numerados (en círculos) por orden de presentación en el documento e indicando los tópicos considerados en cada capítulo (resaltados en negritas). ~ 9 ~ Capítulo I Vertebrates in conserved and managed oak forests: A review Elisa Maya-Elizarrarás1,2, and Jorge E. Schondube2 1Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Universidad 3000, Coyoacán, Ciudad de México, 04510, México. 2Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua carretera a Pátzcuaro 8701, Ex Hacienda de San José de la Huerta, Morelia, Michoacán, 58190, México. Corresponding address: elimaya@cieco.unam.mx ~ 10 ~ ABSTRACT This review explores the diversity of vertebrates that use oak forests as their main habitat. We compiled worldwide information on oak forests, and determined how vertebrates living in this important vegetation type respond to different types of human activities. To conduct this review, we searched for studies using the keywords “fauna”, “vertebrates”, “oak forest”, “Quercus” and “management”, and different combinations of them, in several internet data sets (ISI Web of Science, SCOPUS, Science Direct, and Google Scholar). We classified the studies we found by vertebrate taxonomic group, managed or natural condition, and management type. Management types were grouped into six categories: 1) urbanization, 2) agricultural activities (crops and cattle pastures), 3) dehesas (Mediterranean scrub and forests with low livestock densities), 4) forest fires (both prescribed and not prescribed), 5) wood harvest, logging, and clear-cut practices, and 6) agroforestry and reforestation efforts. The most frequent management activities in oak forests reported in the literature were: wood harvest, logging and clear-cut practices, and agroforestry and reforestation efforts. Wildlife responses to management differed according to their taxonomic identity and the type of management. Usually, oak forests under management showed lower species richness and abundances, inherently reducing the functional diversity and complexity of animal communities present in this vegetation type. Nevertheless, some management practices like prescribed fires, or reforestation efforts improved habitat conditions for wildlife. This review indicates that more sustainable forest management activities should be encouraged to generate better habitat conditions for wildlife in oak forests. More comprehensive management practices, that consider wildlife requirements, could improve wildlife conservation in this important vegetation type around the world. Keywords: clear-cut, forest fire, livestock, logging, reforestation, urbanization, wildlife ~ 11 ~ INTRODUCTION Ecosystems around the world have been used by humankind for thousands of years. This management has generated drastic changes in native vegetation structure, that in the last century have notably impacted biodiversity (Foley et al. 2005, Challenger et al. 2009). Diverse human activities, including the overexploitation of natural resources, the introduction of exotic-invasive species, and pollution, have contributed to habitat destruction and threatened the biodiversity of our planet (Challenger et al. 2009). In the case of forest ecosystems, human activities cause deforestation, with the subsequent use of the deforested land for other activities, like agriculture (Challenger 1998, García et al. 1998, Chakravarty et al. 2012). Other important factors affecting forest ecosystems include fires, and the opening of woodland for pastures (Masera et al. 1995 in Challenger et al. 2009). In oak forests, timber harvesting without immediate deforestation also occurs widely in our planet. This activity is mainly conducted to obtain building materials and fuel for cooking at local scales (Rzedowski 1978). However, on the long term, it has global effects, being one of the processes responsible for the deforestation of large tracts of woodlands in recent decades (Rzedowski 1978, Works and Hadley 2004, Challenger et al. 2009). This is exacerbated by the fact that when wood is used to produce charcoal, oak trees are preferred over other temperate tree species (Aguilar et al. 2012). As a result of these disturbance factors, and their global distribution, oak forests are one of the temperate vegetation types that are more affected by human activities since ancient times (Fig. 1; Shrestha and Paudel 1996, Abrams 2003, Valencia 2004). The main objective of this review is to describe the effects that human activities within managed oak forests have on vertebrate communities around the world. To evaluate the effect of human activities we compared vertebrate species richness, abundances, and functional diversity between conserved and disturbed oak forests. ~ 12 ~ Fig. 1. Worldwide distribution of the member of the Fagaceae family (black). This family include the genera Quercus, Lithocarpus, Castanea and Castanopsis. Image modified from Stevens (2012). METHODS In order to obtain a comprehensive dataset for this review, we conducted a search in the internet using different databases (ISI Web of Science, SCOPUS, Science Direct, and Google Scholar). We included in our search all paper published until May 2011. The key-words we used for our search were “fauna”, “vertebrates”, “oak forests”, “Quercus” and “management”. These keywords were used in different combinations. All the publications obtained in our search were classified according to vertebrate taxonomic groups (birds, mammals, reptiles and amphibians), by habitat conservation status (conserved vs. modified by human activities), and by management type. Management types were grouped in six categories: a) urbanization, considering oak patches modified by urbanization and forest remnants used as parks inside cities; b) agricultural activities, oak forests where agriculture is practiced, including growing crops and cattle-grazing; c) dehesas (Mediterranean scrub and forests with low livestock densities); d) forest fires, including prescribed fires as a management tool, and accidental fires; e) wood harvesting, logging, and clear-cuts; and finally f) agroforestry and restoration efforts. Even though these last two activities have different goals, we considered them as one ~ 13 ~ category because they improve vegetation structure in comparison to non-managed degraded forests, making the habitat structurally more complex. Our search yielded 80 studies. From these, 50% presented data on the response of vertebrates to human activities in oak forests. The more common management activity in our databasewas forest clear-cut, followed by agroforestry and reforestation efforts. Only eight papers included a comparison between conserved and managed oak forests. Most of the publications focused on bird communities, being amphibians the animal group least studied for this vegetation type. The research papers contained data sets mainly from the USA (50%), Spain (25%), and Mexico (10%), and in smaller numbers from Japan, Italy, Portugal, and Morocco, among 5 other countries. VERTEBRATES IN CONSERVED OAK FORESTS The relationship between oak forests and wildlife has been described in several research-papers from around the world (see Block and Morrison 1987, Tietje and Vreeland 1997, Zack et al. 2005, Tempel et al. 2006, and Johnson et al. 2008 among others). Usually, these studies only present species lists, diversity indices, and/or species abundances. Generally, the animal groups better represented are birds and mammals, followed by reptiles, and finally amphibians (Taper and Case 1987, García et al. 1998, Vreeland and Tietje 2002, Jentsch et al. 2008, Urbina-Cardona and Flores-Villela 2010). Oaks are considered a keystone resource in undisturbed temperate ecosystems (Longcore and Rich 2003, Terborgh 1983 in Watson and Herring 2012), and keystone habitat elements in habitats modified by human activities (DeMars et al. 2010). They enable the survival and permanence of many wildlife species by providing crucial food resources. Animals obtain food from them by directly feeding on oak leaves and acorns, or indirectly by feeding on insects on the oak leaves, branches and trunks (Kikuzawa 1988, McShea 2000, Pereira et al. 2014). Additionally, due to their complex branch configuration, oak trees offer important shelter and nesting sites for wildlife (Schmidt and Timm, 1991, Longcore and Rich 2003, Caprio et al. 2009). A recurring theme in most studies that explore the relationships between vertebrates and oaks was the use of acorns as a food resource for wildlife (Santos and Tellería 1997, Koenig and Haydock 1999, Bonal and Muñoz 2007, Pastor and Bonet 2007). Some of the studies conducted in the Mediterranean region have identified a significant diversity of animals that feed on acorns. These include wild pigs (Sus ~ 14 ~ scrofa), wood mice (Apodemus sylvaticus), and different bird species like tits, chaffinches, wood pigeons, robins, nuthatches, and jays (Santos and Tellería 1997). For North America, approximately 96 vertebrate species include acorns in their diets (Haas and Heske 2005) with 30 bird species using acorns as food only in California (Schmidt and Timm 1991). Similarly, Ramírez-Bastida et al. (2015) listed 42 bird species that ingested acorns in Mexican oak forests. While the diversity of vertebrate species feeding on acorns is large, the main consumers of this resource worldwide include: white-tailed deer (Odocoileus virginianus), black and brown bears (Ursus americanus, Ursus arctos), peccaries (Tayassuidae), mice (Peromyscus spp.), wood rats and squirrels (Rodentia), raccoons (Procyon lotor), acorn woodpeckers (Melanerpes formicivorus), jays and magpies (Corvidae), tits (Paridae), quails (Odontophoridae), and wild turkeys (Meleagris gallopavo; McShea 2000, Haas and Heske 2005, Zack et al. 2005, Dickinson 2006, López-Barrera and Manson 2006). Additionally, in some areas of North America, introduced wild pigs (Sus scrofa) have displaced native species as the main acorn consumer (Elston and Hewitt 2010). Oak-dominated forests have inter-annual events of extremely high acorn production known as mast events. Mast events act as critical episodes for wildlife, were food is not limited, and the populations of different species with fast life-cycles that can use this food resource can grow exponentially (Jones et al. 1998, Clotfelter et al. 2007). Mast events can control periodic wildlife population fluctuations, the social structure of populations, and even affect disease prevalence in animal communities (Dickinson 2006, Clotfelter et al. 2007). During a mast event, large mammals like white tail-deer tend to increase substantially their fat reserves, with acorns becoming the main element of their diet (McShea and Schwede 1993). Additionally, a mast event can cause large carnivores, like black bears, to change their spring feeding habits. The ingestion of large amounts of acorns allows them to increase milk fat percentage, increasing cub survivorship (McDonald and Fuller 2005). These massive events of acorn production and their effects on vertebrate communities show the importance of oaks in shaping wildlife communities in temperate areas (Ostfeld and Keesing 2000, Clotfelter et al. 2007, McShea et al. 2007). However, the role that mast events have on vertebrate communities in subtropical, and tropical areas have not been evaluated. Acorn production, predation, and dispersal have important effects on forest regeneration and dynamics (Schmidt and Timm 1991, Haas and Heske 2005, López- Barrera and Manson 2006, Lundberg et al. 2008, Perea et al. 2011). López-Barrera and ~ 15 ~ Manson (2006) found that acorn consumers like field mice (Peromyscus spp.) and squirrels (Sciurus spp.) store significant amounts of acorns for later use during periods of food shortage. Acorns in these caches, while mostly consumed by the animals, are sometimes not eaten, thus allowing seed germination or multiple events of secondary dispersal (Vander Wall 1990, Moore et al. 2007). Nevertheless, seed dispersal by rodents comes at a very high cost for oaks, because a large proportion of acorns are consumed, with these animals acting only as moderately effective disperser (Gómez et al. 2008). This makes acorn dispersal an asymmetric interaction (Vander Wall and Beck 2012). Other animals like jays and acorn woodpeckers, also transport and store acorns allowing for medium- to large-distance dispersal events. These birds can transport and store up to 1 billion seeds per year in oak forests in California (MacRoberts 1970, Schmidt and Timm 1991). So, while oaks are important food resources for vertebrate species, animals that feed on them can play an important role dispersing them, influencing genetic diversity, and tree species composition at different spatial scales in several temperate forest ecosystems that include oak trees (Miyaki and Kikuzawa 1988, Pons and Pausas 2008, Pausas et al. 2009, Scofield et al. 2010). Oaks also provide other important resources for wildlife, such as nesting sites for several mammal and bird species. This topic has been less explored in the literature, and there is limited information on the number of species that use oaks as sites to nest (but see Brito-Aguilar 2005, Winslow and Tietje 2007, Robles et al. 2011). Some woodpeckers can make their nests in oak trees by digging cavities, which, when abandoned, may be secondarily occupied by other species that cannot pierce the wood by themselves (Martin and Eadie 1999, Martin et al. 2004). In relation to secondary cavity nesters, Purcell and Verner (2008) found that several species of passerines birds (i.e. Thryomanes bewickii, Sturnus vulgaris, Sialia mexicana, Tachycineta bicolor, Sitta carolinensis, Myiarchus cinerascens, Troglodytes aedon, and Baeolophus inornatus) coexist in oak forests while using abandoned cavities as nesting sites. But not only birds use abandoned cavities in hardwoods. Mammals (like Glaucomys sabrinus, Pteromys volans, or Martes pennanti) and reptiles, also use them as shelter or nesting sites (Kotaka and Matsuoka 2002, Martin et al. 2004, Smith 2006, Robles et al. 2011, Bunell 2013). While oak trunk cavities are important for a large number of animals for building nests, a much larger diversity of animals have been recorded nesting on the surface of oak branches and twigs (Brito-Aguilar 2005, Zack et al. 2005). For example,~ 16 ~ a diverse array of bird species like gnatcatchers, hawks, jays, magpies, pigeons, sparrows, tanagers, thrashers, towhees, vireos, and warblers use oak trees as platforms to build their nest (Zack et al. 2005, Artman et al. 2008). Furthermore, tree squirrels (Sciurus spp.), and field mice (Apodemus spp.) also build nests on oak branches (Lee and Tietje 2005, Ramos-Lara and Cervantes 2007). Other wildlife associated to, and living in oaks, and/or relying on elements of the oak forest include salamanders, frogs and toads, and a diverse arrange of lizards and snakes. These animals not only use abandoned and natural cavities in the oaks, but also depend on other habitat traits like leaf-litter depth, and woody debris produced by the oaks (Block and Morrison 1998). VERTEBRATES IN MANAGED OAK FORESTS Since ancient times oak forests have been an important resource for people (Shrestha and Paudel 1996, McShea et al. 2000, Asbjornsen et al. 2004). However, even before the 20th century their decline has been evident due to multiple human disturbances and exploitative management practices that have caused oak-forest fragmentation and alteration of their natural regeneration (Shrestha and Paudel 1996, McShea et al. 2000, Asbjornsen et al. 2004, Álvarez-Zúñiga et al. 2010). The main disturbance forces acting on oak forests are urbanization, agricultural practices, grazing, logging or harvesting (including wood extraction for fuel), cork or litter collection, and fires (Shrestha and Paudel 1996, McShea et al. 2000, Asbjornsen et al. 2004, Chace and Walsh 2006, Dickinson 2006, Álvarez-Zúñiga et al. 2010, Leal et al. 2011). The reduction in the extension, and the degree of human disturbance of oak forests have profound effects on the wildlife communities associated to this vegetation type (Shrestha and Paudel 1996, McShea et al. 2007). Urbanization In the last decade, studies that describe animal responses to urbanization have become more frequent in the literature (see Chace and Walsh 2006, Soulsbury and White 2015). The fast and uncontrolled growth of cities tends to devour and embed the natural ecosystems surrounding them, altering the composition and structure of plant communities, as well as the animal communities that inhabit them (Blair 1996). Additionally, an increase in low-income human population in urban areas is associated with an increase in the demand for wood to be used as fuel for cooking, modifying dramatically oak forests associated to urban sites (Aus Der Beek et al. 2006, Masera et ~ 17 ~ al. 2010). There are several examples of how urbanization has affected oak forests in different parts of the world, threatening wildlife communities, and even some endemic species such as Xantusia lizard populations in the State of Jalisco, Mexico (Cruz-Sáenz and Lazcano 2012). The effects of urbanization on oak forests are not different to those that occur in other natural vegetation types. Sánchez and Tellería (1988) found significant differences between oak woodlands in urbanized areas versus rural oak woodlands. These include important differences in soil characteristics, herbaceous, shrub and tree cover, shrub and trees species richness, and tree trunk diameter and height. Associated to these changes in vegetation structure and diversity, a significant loss of avian species can occur since the start of the urbanization process (Chace and Walsh 2006). Sánchez and Tellería (1988) found a significant decrease in the species richness of avian communities of oak woodlands affected by urbanization. Oaks tend to play an important role in urban landscapes that occupy areas formerly dominated by oak forests. These trees provide shade, food, and cover for wildlife in urban environments (Kotaka and Matsuoka 2002, Longcore and Rich 2003, Lundberg et al. 2008, Costello et al. 2011). Additionally, they offer several ecosystem services inside cities like acting as wind barriers, visual buffer zones, and esthetically pleasing landscape components in parks, along streets, in yards, and in other urban public areas (Dickinson 2006). The importance of oaks for vertebrates in urbanized landscapes had been poorly explored (Smith 2006). However, Blair (1996) reported that oak forest remnants in an urban gradient presented higher avian species richness and abundances than other habitats, acting as areas of intermediate or low disturbance in urban ecosystems. While studies on the responses of oak forest wildlife to urbanization are relevant to generate urban wildlife management plans, the knowledge of the use of oaks by many animal groups in urban systems is still very limited. Crop and cattle-grazing activities Important changes in land use have occurred in recent decades, causing a high loss of biodiversity worldwide (Sanderson et al. 2002, Millennium Ecosystem Assessment 2005). Most of these land use changes are related to the transformation of forest habitats to agricultural plots, and the intensification of agricultural activities. As a result of this, crop growing and cattle-grazing activities occupy around 40% of the world’s land surface (Wallis de Vries et al. 2007, Child et al. 2009). Agriculture modifies natural ~ 18 ~ systems and processes by altering habitat structure and biogeochemical cycles (Vitousek et al. 1997, Sanderson et al. 2002, Harvey et al. 2008, Child et al. 2009). Furthermore, this activity involves the use of pesticides, inorganic fertilizers and other agriculture concomitants (Pretty 1995, Vitousek et al. 1997). The transformation of oak forests to agricultural plots involves a large number of important changes in habitat characteristics, which vary depending on the production system (crops vs. pastures; Martin and Possingham 2005, Tárrega et al. 2006, Wallis de Vries et al. 2007). From the vegetation perspective, land use change from oak forest to agricultural plots alters the population structure of the oak stands. This is caused by the removal of trees and the livestock ingesting both acorns and seedlings (Schmidt and Timm 1991). Additionally, in the case of pastures there is a substitution of native grasses with exotic species, which in turn alter fire regimes and compete with oak saplings for resources (Block and Morrison 1987). On top of that, agricultural activities generate soil compaction, which reduces the capacity of the seedling roots to penetrate the ground, reducing dramatically oak forest regeneration (Schmidt and Timm 1991, Saab et al. 1995). Although several vertebrate species can respond positively to these habitat changes (like some granivorous bird and mammal species), most of them are negatively affected (Saab et al. 1995, Ficetola et al. 2007, Harvey et al. 2008, Child et al. 2009). The response of wildlife to the conversion of oak forests to agricultural plots varies depending on the habitat requirements, and the life history of the different animal species. Regarding the effects on birds, insectivores, nectarivores, carnivores and scavengers are particularly sensitive to agricultural transformation were native vegetation is removed (Child et al. 2009). Agricultural activities negatively affect those species dependent on dense ground cover for nesting and/or foraging, modifying bird species richness, abundances, functional diversity, and even changing the behavior of the bird communities (Saab et al. 1995, Maya-Elizarrarás and Schondube unpublished data - see Chapter 3 in this thesis). Agricultural activities also increased the vulnerability of bird nests to cowbird parasitism due to the reduction habitat structural complexity (Saab et al. 1995). However, these new habitat conditions generated by agricultural activities seem to be preferred by some bird species, such as several Neotropical migrants (Lynch 1989, Saab and Petit 1992, Hutto et al. 1986, Smithet al. 2001), and some bird species that evolved with large herbivores in the prairies of North America, like Mountain Plovers (Charadrius montanus) and Baird’s Sparrows ~ 19 ~ (Ammodramus bairdii), increase their population sizes when cattle-grazing activities are present (Saab et al. 1995, Fuhlendorf and Engle 2001). Changes in oak forest species richness and structure by agricultural activities are related to the loss of avian functional richness in the landscape. However, when using functional richness as an indicator of resilience, or the delivery of ecosystem services, it is important to notice that complex agricultural landscapes that include patches of original oak forests can support an important functional diversity at a regional scale (Child et al. 2009). As a result of this, and in order to improve species richness in agricultural landscapes, management practices like the use of hedgerows, fencerows, shelter-belts and other strip-cover habitats have been proposed (DeMars et al. 2010). An important element of these management practices in agricultural landscapes consists in retaining isolated trees, also called scattered trees. These trees have positive effects on the vertebrate fauna under different environmental contexts (Manning et al. 2006). DeMars et al. (2010) found that the architecture, size, and tree cover of isolated trees in areas of the landscape surrounding transformed oak forests, were the vegetation traits that best predicted bird diversity and habitat use by these animals. Additionally, the presence of isolated trees and remnants of original forests, provide crucial resources for wildlife like food (fruits and foliage), shelter and nesting sites in these human modified landscapes (Manning et al. 2006). And scattered large trees within early successional stages of oak forests improve bird species richness and offer more resources for avian communities in human modified landscapes that are dominated by this vegetation type (Maya-Elizarrarás and Schondube 2015). Dehesas as an important agricultural activity in oak forests The use of oak forest areas for cattle-grazing activities is an ancient management tradition in the Old World (Díaz et al. 1996, López-Sáez et al. 2007). In the Mediterranean region, oak forests have been transformed and used for cattle-grazing activities since the IV millennia BC (López-Sáez et al. 2007). One of the most important silvopastoral systems in Europe associated to oak forests is the dehesa. This system is similar to a savanna ecosystem, constituted by large grass prairies that include scattered oak trees (Penco 1992, López-Sáez et al. 2007). The dehesa includes only grasses and oak trees of the genus Quercus, and has been molded by grazing activities that take advantage of the oaks to offer shade, protection from bad weather, and additional food for cattle in the form of oak seedlings, saplings, leaves, and acorns ~ 20 ~ (Penco 1992, Díaz et al. 1996, Shrestha and Paudel 1996). Additionally, people use oak wood and bark from this system (Shrestha and Paudel 1996, López-Sáez et al. 2007). Similar silvopastoral systems exist in the New World, with large areas of California being covered with cattle ranches that include oak trees in their grazing prairies (Block and Morrison 1987, Schmidt and Timm 1991), and subtropical temperate rural landscapes of Mexico that present combinations of agricultural activities and scattered oak trees (López-Barrera and Manson 2006, Maya-Elizarrarás and Schondube 2015). The effect of these agro-silvopastoral systems for vertebrate wildlife has been described for dehesas with different structural characteristics (Díaz et al. 1997, Tellería 2001, Martín and López 2002). Compared to other human-productive systems in the Mediterranean region, dehesas increase wildlife species richness, maintaining more diverse wildlife communities than treeless pastures, and croplands (Díaz et al. 1997, Tellería 2001, Martín and López 2002). Additionally, dehesas are relevant for wildlife conservation, even maintaining populations of endangered species such as Lynx pardina, Aquila adalberti, and Ciconia nigra, among many others (Díaz et al. 1997, Tellería 2001). Changes in land-use in these agro-silvopastoral systems affect wildlife due to the reduction of acorn availability, the modification of shrub/grassland vegetation that occurs when livestock activities are increased, and the reduction of oak tree density and regeneration (Díaz et al. 1997). For example, in the Mediterranean region, Díaz et al. (1996) found that the Common Crane (Grus grus) was more negatively affected by croplands than by grazed prairies or shrubby dehesas, due to the presence of acorns in the latter. These authors conclude that in order to increase acorn availability that could be used as a food resource by wildlife, it is necessary to maintain sites without the presence of livestock. Effect of forest fires Many oak forests around the world, like California’s oak woodlands, have been exposed to fire during at least one million years, and are thus fire-adapted ecosystems (Vreelan and Tietje 2002). In fact, there is evidence that suggests that most oak species benefit by relatively frequent low intensity fires that tend to increase oak forest regeneration (Lanham et al. 2006, Patterson 2006). As a result of the importance of fire in the ecology of several oak forest ecosystems worldwide, prescribed fires can be a key tool for the correct management of oak woodlands (Vreelan and Tietje 2002, Patterson ~ 21 ~ 2006). These fires help managers to reduce fuel loads and/or restore these fire adapted ecosystems (Vreeland and Tietje 2002, McCaffrey 2006). The impacts of prescribed fires on plant and animal communities associated to oak forests have received little attention in the literature (Blake 2005). However, the recognition of prescribed fires as a forest management tool with important effects on wildlife communities has increased in the last decade (see Dickinson 2006). For example, Vreeland and Tietje (2002) surveyed vertebrate communities (amphibians, reptiles, breeding birds, and small mammals) in two sites with prescribed fires that had different burning intensities, and compared them with an unburned site. They did not find differences in vertebrate relative abundances among sites. However they recognized the need to evaluate the effects that different experimental fire intensities can have on wildlife. Amphibians and reptiles have received less attention than other groups of vertebrates in relation to their responses to oak forest fires. However, a review for the eastern United States indicates that fire causes little direct mortality on amphibians and reptiles, and that the abundance, diversity and richness for both groups was not different between burned versus unburned sites (Renken 2006), suggesting than prescribed fires may not be detrimental to herpetofaunal communities (Keyser et al. 2004). However, other observations indicate a decrease in salamander-, and increases in lizard- abundances and species richness in burned sites (Renken 2006). These contrasting results show the need of more research on the effects of fire on the amphibians and reptiles present in this vegetation type. Artman et al. (2008) evaluated the effect that repeated burning and recovery of mixed-oak forest had on breeding bird communities in southern Ohio, USA. They found only a minimal difference in species composition among sites with different fire regimens. Additionally, there was an adverse effect of prescribed fires on ground and low-shrub nesting species (i.e. Empidonax virescens, Hylocichla mustelina, Helmitheros vermivorum, Seiurus aurocapilla; Blake 2005). Nevertheless, some shrub-nesting species like the Wood Thrush (Hylocichla mustelina), showed a highadaptability to prescribed fires, placing their nests higher from the ground in response to fires, and being able to maintain a high reproductive success in both burned and unburned areas (Artman and Downhower 2003). Another aspect that has been evaluated is the interaction between prescribed fires and the harvest of dead wood that provides shelters for wildlife. Lanham et al. ~ 22 ~ (2006) defined this as a technique for managing oak-dominated stands, reducing ground-level shade and disturbing the soil, in order to allow oak seedling establishment. These authors compared the presence of birds among sites with different combinations of prescribed fires and harvest regimes. Their results suggest that properly implemented prescribed fires provide habitat diversity that promotes healthful populations of game and non-game birds. In the case of large mammals, the effects of prescribed fires have not been properly evaluated. However, the existing data suggests that fire can have a beneficial impact on habitat quality for an important number of species (Keyser and Ford 2006). The effects of oak forest fires on mammals have mostly been studied for small species (mainly rodents), with almost no studies for medium-sized or large mammals (Vreeland and Tietje 2002, Keyser and Ford 2006). Most studies report a lack of changes in the relative abundance of small mammals in response to prescribed fires. This is explained by the fire-avoidance strategies of small mammals, like hiding in deep borrows or holes in the trees, which allow them to escape from fire (Vreeland and Tietje 2002). Keyser and Ford (2006) found that although prescribed fires changed habitat conditions, creating open gaps, there were mammal species that preferred open canopies and/or the increase of herbaceous understory cover and diversity that occurs in response to low canopy cover. These mammal species could benefit and prosper in the presence of fire. This is the case for some mammal species of high conservation concern, such as the Indiana Bat (Myotis sodalis) or the Fox Squirrel (Sciurus niger). Wood harvesting, logging, and clear-cut activities Oaks are an important source of wood for human populations all over the world. We, as a species, use oak trees for timber or charcoal production, as building materials in rural areas, or as fuel (Shrestha and Paudel 1996, Dickinson 2006). The extraction of wood from oak forests implies a significant reduction in the abundance of oaks, and/or a change in oak architecture, sometimes accompanied by the cleaning of the forest understory (Shrestha and Paudel 1996, Tárrega et al. 2006). All these management actions have profound effects on the wildlife communities that live in oak forests, and could represent a strong impact on local biodiversity (Camprodon and Brotons 2006, McShea et al. 2007). Among these management activities, clear-cutting is a popular technique in many regions because it is a cheap technique that permits to obtain large volumes of timber, and allows the use of multiple methods of forest regeneration, both ~ 23 ~ natural and artificial (Rosenvald and Lohmus 2008). Other forms of logging, like small scale logging and other techniques of wood harvesting, while maintaining part of the forest, can also produce a dramatic structural impact on the forest habitat, and thus on wildlife (Morrison 1992, Meijaard et al. 2005). Both, clear-cut and small-scale logging practices generate early successional habitats, with dramatic effects on vertebrate communities (Keller et al. 2003). Sometimes clear-cutting is recommended as a strategy to increase habitat diversity in the landscape, allowing some species, such as white-tailed deer to increase their numbers (Thompson and Fritzell 1990). However the forest edges created by this practice may negatively affect some forest wildlife species dwelling in mature stands adjacent to the clear-cuts (Thompson and Fritzell 1990). Small scale logging and other timber extraction techniques have varying effects on different animal species, with insectivore and frugivore species being particularly sensitive to wood harvesting, while herbivores and omnivores tend to be more tolerant, or even can benefit from logging activities (Meijaard et al. 2005). Most of the research that explores the effects of clear-cutting and other logging activities on oak forests has focused on avian communities (Keller et al. 2003) because forest birds are good bio-indicators of changes in habitat structure (Skórka and Wójcik 2003). These studies have reported lower total species richness and a smaller number of territorial/breeding species in clear-cuts and/or logged areas, than in conserved forests (Thompson and Fritzell 1990, Thompson et al. 1992, Skórka and Wójcik 2003). Additionally, clear-cuts and logging activities reduced the species richness and abundances of birds that depend on mature forest, and generated an increase in the number of species and individuals of species that use extensively the early and mid- successional forest-stands that form after clear-cuts (Thompson et al. 1992, Brito- Aguilar 2005). Another effect that logging practices have on oak forests is the presence of even- aged and uneven-aged forest stands in the landscape. Morrison (1992) compared bird communities in even-aged versus uneven-aged oak forests stands, finding that the latter had a slight increase in bird species richness. He also found that maintaining high tree diversity in both types of stands contributes to an increase in bird species richness, and allows forest stands with uneven- and even-age to have similar bird communities. Additionally, the large majority of studies that are related to successional habitats in even-aged management stands have found that bird species richness vary according to ~ 24 ~ the different species affinities to mature forests stands or early-successional stands (Yahner 1987, Baker and Lacki 1997, Brito-Aguilar 2005). Bird densities are usually high in young stands and older stands that present a higher number of vegetation layers (Dickson et al. 1993), while bird species turnover rates are higher in young even-aged habitats in comparison to mature forests (Yahner 1987). Finally, McDermott and Wood (2009) found that even-aged sites that were harvested more than 20 years ago had lower bird species richness and abundances than sites that were recently harvested. While silvicultural management has negative effects on several species, it also can be used to maintain successional habitats that improve conditions for some vertebrates (McDermott and Wood 2009). While the conservation of forest specialist species requires dense oak trees patches and shrubs, a vegetation mosaic that includes clearings is also necessary for other species (Hardy et al. 2013). There are several ways in which logging activities can increase habitat diversity in oak forests. For example, by maintaining even-aged and uneven-aged forest plots (Morrison 1992), or by creating early successional stands after a clear-cut (McDermott and Wood 2009). The effects of these management practices on wildlife communities varies in relation to geographic area, weather conditions, and the scale, intensity, and frequency of the human activities (Morrison 1992, Keller et al. 2003, Brito-Aguilar 2005, Rosenvald and Lohmus 2008, McDermott and Wood 2009). As a result of this, more work is needed to gain a better understanding about which specific conditions created by logging activities are negative for wildlife. Beside the effects that cutting trees and/or branches have on wildlife, some authors have explored how the cutting of the understory, or the canopy, affect bird diversity in oaks forests. Camprodon and Brotons (2006) found that the removal of the understory in Helm Oak forests (Quercusilex), by simplifying the vertical structure of the forest, reduced foraging and breeding sites for birds. Newell and Rodewald (2012) compared habitat preferences, settlement patterns, age distribution, site fidelity, and nesting success of songbirds between sites that were recently harvested (a partial harvest with open forest canopy) versus closed-canopy mature oak forests. They found that the abundance of nesting bird species differed between these two conditions, negatively affecting ground and shrub nesting birds in harvested sites, although nest survival was similar among treatments. Bird settlement and site fidelity did not differ between harvested and closed-canopy mature forest, but the authors reported an increase in young males in harvested sites, and they argued that this was a result of a colonizing ~ 25 ~ process of the new habitat by individuals from the mature forest stands, creating a metapopulation dynamic. Finally, they pointed out that removal of all the canopy layer would result in the loss of nesting substrates and breeding habitat for canopy songbirds (Newell and Rodewald 2012). Other harvesting activities in oak forests include debarking of cork oaks, and charcoal production. These topics have been poorly explored in relation to their effects on wildlife. This is surprising, considering that in Europe, since ancient times, oak forests were used for the production of charcoal (Amo et al. 2007). Charcoal production generates a heterogeneous landscape by reducing forest cover, and creating mosaics of oak forest habitats with different structure and tree sizes, that directly affects wildlife communities (Díaz et al. 1997, García 2007, Ramírez-Bastida et al. 2015, Maya- Elizarrarás and Schondube 2015). For bird communities, Maya-Elizarrarás and Schondube (2015) found that habitats where wood was extracted for charcoal production had low bird species richness, at least during the summer season. Although resident bird species and Neotropical migrants used all the different habitats created by charcoal production and mature forests in a similar fashion, summer migrants preferred habitats that had tall trees and high values of tree and shrub richness. These habitat variables were negatively affected by wood harvesting for charcoal production, limiting the presence and the species richness of summer migrants in the landscape. In relation to cork extraction, Leal et al. (2011) compared bird communities in stands where cork was recently extracted and sites with older extractions. They found that densities of bark gleaners and bark-foliage gleaners diminished in response to the removal of the cork and the associated decrease in the availability of bark arthropods. However, total species richness and bird densities were unaffected. Interestingly at the landscape level, even bark gleaner species had stable population sizes, suggesting metapopulation dynamics in this system. Agroforestry and reforestation efforts In many countries, agricultural policies have led to the reforestation of natural habitats with native and exotic tree species like pines, spruces or eucalyptus. These tree species have been used mainly as a source of timber, representing an economic resource for local communities (Amo et al. 2007, Barrientos 2010, Proença et al. 2010). In the eastern United States, managers of many National Forests have employed silvicultural practices to regenerate damaged forests (Baker and Lacki 1997). However, plantations ~ 26 ~ sometimes were made hundreds of years ago to replace original vegetation (Amo et al. 2007) and have had effects on wildlife communities. A first approach to understanding the effects that tree plantations have on animal communities is to study vertebrates in both native forests and plantations. Proença et al. (2010) studied forest bird species richness and forest plant species richness in a natural oak forest, a pine plantation (native species), and an eucalyptus plantation (exotic species). They found that bird and plant species richness were higher in both the native oak forest and the pine plantation, than in the eucalyptus plantation. Santos et al. (2006) compared bird communities in oak forest remnants and pine plantations in the Mediterranean region. They found that bird species richness were similar in the two habitats, but species-area relationships differed, with small oak forest fragments holding more species than those of pines, probably due to differences in vegetation structure like understory shrub cover and tree height and cover. Amo et al. (2007) compared the composition of lizard communities and their patterns of microhabitat selection between ancient pine plantations (since Roman period) and original deciduous oak forest sites. They found that lizard species composition was different between oak forest and pine plantations, due to a habitat selection process, based on structural elements such as rocky outcrops, low tree cover, and short distance to the nearest refuge. Based on their results they conclude that pine plantations do not contribute importantly to the diversity of lizard species and suggest several ideas for pine reforestation management including: 1) the recolonization of the habitat by oaks planted in the understory, 2) leaving open areas in the center of the plantations, 3) allowing/promoting the development of a dense shrub cover, and 4) leaving rocks inside reforestation areas. Pine plantations that are planted in areas originally covered by oak forests do not contribute to increase or maintain biodiversity when compared with natural oak habitats that still exist in the same regions (García et al. 1998, Santos et al. 2006, Amo et al. 2007, Proença et al. 2010). This occurs even when the pine species used in the reforestation are native. In the case of birds, this seems to be the result of bird species being closely linked to the original floristic composition, and the habitat heterogeneity provided by primary oak forests (Wiens et al. 1989, García et al. 1998). Pine plantations generate a loss of structural heterogeneity and plant diversity, something commonly found in monocultures, reducing bird species richness (Haskell et al. 2006, Santos et al. 2006). However, early stages of pine plantation can provide habitat for some early- successional specialist birds such as the Prairie Warbler (Setophaga discolor), and the ~ 27 ~ Yellow-breasted Chat (Icteria virens; Haskell et al. 2006). Pine monocultures also affect habitat selection of generalist bird species, like the Great Spotted Woodpecker (Dendrocopos major), which prefers forested patches with high levels of tree diversity and native species as nest-trees (Barrientos 2010). Also it has been recorded that plantations could support fewer specialist bird species, and cavity-nesting species, in relation to native oak forest (Haskell et al. 2006, García et al. 1998). CONCLUSIONS A high number of disturbance factors threaten oak forests and the wildlife associated with them worldwide. There is a large amount of information on modern management activities in oak forests from the USA, however information on old management activities associated to the modification of oak forests by humans comes for Europe. Although many animal species seem resilient to management activities, especially to those that emulate natural conditions such as tree plantations, it is important to notice that species richness is generally lower in these systems in relation to the original natural oak forests (García et al. 1998, Haskell et al. 2006; see Table 1). Several authors have reported behavioral plasticity in many animal species, a trait that allows them to live and survive in new habitat conditions (Artman and Downhower 2003, Sih 2013, Sol et al. 2013). Nevertheless, plasticity is not a common trait
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