Ilustración de portada Esther Charles Jordán (mira al pajariko®) Diseño de portada Sofía Vázquez Benítez
UNIVERSIDAD AUTÓNOMA DE MADRID FACULTAD DE CIENCIAS
Departamento de Ecología
HABITAT INFLUENCE ON LIFE HISTORY AND BEHAVIOURAL TRAITS OF CAVITY NESTING BIRDS
Memoria presentada por la Licenciada Eva Serrano Davies para optar al grado de Doctora en Ecología con Mención Internacional por la Universidad Autónoma de Madrid, dirigida por el Dr. Juan José Sanz Cid del Museo Nacional de Ciencias Naturales -̶ CSIC.
Madrid, 2016
La doctoranda Vº Bº del Director
Eva Serrano Davies Juan José Sanz Cid
UNIVERSIDAD AUTÓNOMA DE MADRID FACULTAD DE CIENCIAS
Departamento de Ecología
HABITAT INFLUENCE ON LIFE HISTORY AND BEHAVIOURAL TRAITS OF CAVITY NESTING BIRDS
EVA SERRANO DAVIES
Memoria presentada para optar al grado de Doctora en Ecología con Mención Internacional por la Universidad Autónoma de Madrid.
Dirigida por el Dr. Juan José Sanz Investigador Científico
Museo Nacional de Ciencias Naturales-CSIC TESIS DOCTORAL
Madrid, octubre de 2016
THESIS STRUCTURE
This thesis is structured in eight main sections. First section constitutes a general INTRODUCTION, where the conceptual framework, aims and objectives of this work are established. The second details the general METHODS that have been used during the research which includes study species, study sites and general fieldwork procedures. The methodology is supplemented by the specific procedures used to develop each objective and has been included in its relevant section. The following four sections include chapters in standard scientific article format. Last sections include GENERAL DISCUSSION and CONCLUSIONS which complete the present PhD thesis.
FINANCIAL SUPPORT
This thesis has been supported by a Predoctoral Scholarship from Ministerio de Ciencia e Innovación (BES–2011–047046). The studies presented here have been funded by the project CGL2010–21933–C02–01 to Juan José Sanz and the mobility grants EEBB–I–
14–08566 and EEBB–I–15–10364 to Eva Serrano Davies from Ministerio de Ciencia e Innovación.
INDEX
Acknowledgements 3
Abstract 9
Resumen 13
Introduction 17
Aims and objectives 25
Methods 37
Study species 39
Study areas 40
General fieldwork procedures 44
Chapter I. The role of nestbox density and placement on occupation rates and breeding performance: a case study with Eurasian Blue tit
49
Chapter II. Habitat variations modulate nestling diet composition and fitness of Blue tits Cyanistes caeruleus in the Mediterranean region
75
Chapter III. Habitat-specific differences in selection on personality in Mediterranean Blue tits
103
Chapter IV. Foraging strategies, innovativeness and personality variation among wild birds temporarily taken into captivity
131
General discussion 163
Conclusions 175
Conclusiones 177
Acknowledgements
3
ACKNOWLEDGEMENTS
Resulta casi imposible mencionar en unas cuantas líneas a todas aquellas personas que han estado implicadas en la realización de esta tesis doctoral y en mi formación como científica y persona. Aun así quiero empezar dando las GRACIAS a todos los que con vuestro trabajo, vuestros consejos o vuestro apoyo habéis contribuido a que esta tesis saliera adelante.
Gracias a mi director, Juanjo Sanz, por concederme la beca y darme un lugar en tu grupo, permitiéndome así trabajar en lo que más me gusta. Gracias por aceptar cualquier idea nueva con interés y entusiasmo y por contestar siempre a mis múltiples preguntas.
Quiero dar las gracias a Jesús Herranz, que ha sido mi tutor académico durante estos años y que siempre me ha ayudado y estado disponible cuando le he necesitado.
Además tuvo la culpa de mi primer trabajo como bióloga, censando aves a lo largo de la línea de AVE Madrid-Valencia. Gracias también por confiar en mí porque no sabes lo que aprendí de aves aquel verano (también a conducir de noche y no perderme en los caminos).
El primer año de tesis lo pasé trabajando en la Fábrica de Armas, el precioso campus de la UCLM en Toledo. Cuando llegué a la que sería mi oficina en el ICAM me sentaron enfrente de Rafa Barrientos…aquel con el que compartiría despacho hasta casi el final de esta tesis. Gracias Rafa por contestar a los miles de preguntas que te habré hecho durante estos años, por venir a Quintos a ayudarme (y también a comer paella), por corregir mis manuscritos; y también por las risas, las cañas, las confidencias y un largo etc…Has sido un pilar fundamental para que hoy haya llegado hasta aquí. Allí también conocí a Sara Varela quien además de introducirme vilmente al mundo de R, solucionaba mis dudas existenciales acerca de la investigación, la tesis y la vida. Gracias por ser tan maja, tan risueña, tan buena persona y por el tiempo que compartimos en Toledo. A Marta Rodríguez, gracias por esas conversaciones infinitas con un café de la máquina, por animarme y tenerme siempre en cuenta, ¡si hasta viniste a vernos a Quintos con una bandeja de tigres! Sin duda los días en la UCLM fueron infinitamente mejores gracias a ti. No me olvido de los demás integrantes del
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grupo, Javi, Espe y Vicente, quien además ha aportado numerosos datos de campo incluidos en esta tesis.
Gracias a Carlos Rodríguez-Vigal y Ángel Moreno, directores de Los Quintos de Mora durante los años de trabajo allí, por darnos todas las facilidades además de un alojamiento en pleno paraíso manchego. También al personal y la guardería, Jose, Justi y Eduardo especialmente, por pararos siempre a preguntar “Niña, ¿cómo vas?”. La belleza y majestuosidad de esta reserva quedará siempre en mi memoria.
Fundamental para el desarrollo de esta tesis ha sido “El Charrancito” mi pequeño Citroën C2 negro que me ha acompañado y aguantado el campo durante 3 duras temporadas como si de un 4x4 se tratase, ha ido a Toledo infinitas veces cuando tocaba despacho, y que sigue dando guerra allí dónde le pido que me lleve.
Tras el primer año vino el traslado al Museo, y con ello pasé formar parte de una enorme familia. Va a ser casi imposible que os mencione a todos pero gracias a Jose, Carol, Diego, Ramón, Raúl, Geizi, Nath, Rodrigo y Laura por todos esos menús diarios de Jaquete con risas incorporadas. Gracias a Isaac por ayudarme con los mapitas de GIS. Gracias en especial a Jaime, Chio, Ester, Vir, Sergio, Chechu, Martí y Jimena con los que he compartido miles de días, de cariño y de conversaciones. Y a “las nuevas”, Irene y Mireia. Entre toda la gente maravillosa que he conocido estos años de trabajo quiero agradecer especialmente a Alex por todo su apoyo. No se puede ser tan pequeño y tan grande a la vez...eres ese hermano mayor que te pregunta 200 veces al día cómo estas, que tarda dos micro-segundos en venir al despacho cuando necesitas algo, que se va de vacaciones y sigue estando pendiente de cómo va el desarrollo de tu tesis, y que te “obliga” a salir a tomar café o subir al gimnasio así sea el fin del mundo.
Y a Elisa, mi Twin Tower, la que ha hecho que mis días sean más divertidos, la que ha escuchado todas mis preocupaciones y alegrías, con la que he bailado, llorado, y reído hasta la saciedad, y de la que no me he separado desde hace ya cuatro años. Mil gracias por ser como eres, porque me siento muy afortunada de que la vida nos haya cruzado.
I am very grateful to Niels Dingemanse, to his family and to the entire
“Evolutionary Ecology of Variation” research group from the Max Plank Institute for Ornithology. Many thanks to welcome me as member of your group and to give me
Acknowledgements
5 the opportunity to carry out part of this thesis on it. Those two months in Seewiesen reminded me that research is amazing! Thanks Marion for helping me when I contacted you initially and doing the external assesment. Gracias a Yimen por hacer posible el tercer capítulo de esta tesis y soportarme ese tiempo en la “Spanish room”,
¡pura vida! Y a Alfredo y Leti, los andaluces más majos y salaos que ha visto Bavaria, por hacer mi estancia en Starnberg más divertida y llevadera.
I also would like to thank John Quinn to host me during my University College Cork stay. Thanks a lot for allowing me to perform the experiments in the aviary and for your support with the fourth chapter of this thesis. Thanks a lot to Will, with whom I worked hand in hand during that 2015 winter in Ireland. You are the next one!!! Y gracias y más gracias a Gema, por acogerme en tu casa, por enseñarme lugares maravillosos de Irlanda y por hacerme la vida mucho más fácil durante mi estancia en Cork.
No dejo de acordarme de aquellos con los he pasado unas cuantas jornadas de anillamiento y que me enseñaron (y seguirán haciéndolo) tanto y tan bien de nuestros queridos emplumados. Gracias Juancho por llevarme aquella primera vez a Las Minas, a Canencia, al Cadí…y por el montón de veces que me has escuchado y animado a seguir adelante a pesar de las dificultades. A Carlos Ponce con el que he censado, anillado y comido galletas Príncipe además de enseñarme a hacer fichas de muda;
gracias por ser tan exigente y tan buen colega y profesional.
Gracias también a mis biólogos los de la UAM: Titu, Irene, Bea, Alfredo, Javi, Raúl y Miguel, porque compartimos el inicio de todo esto, por esas salidas de campo que nunca olvidaré y porque, a pesar de vernos poco, siempre he sentido vuestro cariño. En especial, a Andrea, que siempre me ha dado calma y confianza. Y a Mar (alias Pistacho) porque desde que la conocí el primer día de clase no nos hemos separado, aunque se empeñe en irse cada vez más lejos.
Si a alguien le debo haber llegado hasta aquí, ese sin duda es Cristian. Me resulta imposible seleccionar las razones por las que darte las gracias. Desde aquellos exámenes improvisados de nombres científicos de aves hasta las decenas de cóndores andinos, pasando por los censos de Ricotí o los miles de paseos “a ver qué vemos”; en gran parte si hoy me considero ornitóloga es gracias a tí. Gracias por creer que podría
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con ello, que sería capaz, por animarme siempre cuando los miedos me paralizan. Por compartir conmigo y enseñarme tanto de las aves, de la vida. Gracias porque has corregido casi cada texto de esta tesis, me has acompañado al campo, y gracias por todos los consejos y los ánimos.
A mis amigas, las de toda la vida. A Eva, Ana y Lau por preguntarme siempre
“¿cuándo acabas?” y escuchar mis historias de pájaros con respeto y cariño. A Sofi, por acompañarme al campo aquel día, por tu apoyo en esta última etapa y la ayuda con el diseño de la portada, al fin las dos…¡hemos acabado! Y a Lu, mi hermana, esa que lleva veintiocho años compartiendo la vida conmigo. Por tu apoyo incondicional, por no dudar ni un momento en que podría con ello, por estar a mi lado ya esté en Madrid o en Honolulú, ¡muchas gracias!
También quiero dar las gracias a Roger. Por confiar en mí mucho más que yo misma, por animarme cuando creo que ya no puedo más. Por acompañarme hasta aquí sin parar de decirme: “Tranquila, que esto lo sacamos adelante”. Gracias por tu paciencia infinita, por saberte de memoria cada uno de mis artículos, por venir a verme vaya donde vaya y por seguirme cuando quiero ir “a ver pájaros”. Por cada uno de tus abrazos de apoyo y por darme tranquilidad cuando pierdo la perspectiva.
Muchas gracias por las flores, los croissanitos y los bailes, que me han ayudado a coger aliento. Sin todo ello no hubiera podido completar esta etapa.
Y también gracias a toda mi familia, que siempre me ha apoyado y ha seguido el desarrollo de este trabajo. En especial, dedico esta tesis a mis abuelos. A Goriche, que le encantaban los pájaros y estaba tan contento de que una de sus “petardas” fuera a ser doctora, aunque no fuera de las que curan enfermos. A mi abuela Luisita, que me enseñó que la bondad humana no tiene límites, que no hay nada mejor que tomar el fresco en las noches de verano o reír a carcajadas, y que fue todo un ejemplo de mujer fuerte y adelantada a su tiempo. A mi abuela Lina, que a través de la música me enseñó lo que es el esfuerzo y la dedicación, y que me inculcó los valores del sacrificio y el tesón. Y a mi abuelo Eduardo, que siempre me exigía ser la mejor y que celebraba con un “¡fenómeno!” todos y cada uno de mis logros, porque sé que hoy estaría muy orgulloso.
Acknowledgements
7 Por último, esta tesis no hubiera sido posible sin ellos, mis padres Lina y Marcos. Gracias papá porque esta tesis es también tuya, por aquella que tú no pudiste terminar. Nunca te agradeceré suficiente la confianza, el apoyo, los tapers de tortilla o filetes empanados que me transportaban a casa cuando la intensidad y soledad del trabajo de campo me abrumaba. Gracias mamá por enseñarme a ser fuerte y luchadora, porque estoy muy orgullosa de esa mala leche que nos ayuda a enfrentar juntas todo tipo de retos en la vida. Gracias por estar siempre pendiente de mi bienestar y mi felicidad. Muchas gracias a los dos por venir a visitarme a Quintos, a Alemania, a Irlanda. Y sobretodo, por confiar en “vuestra niña” y por hacerme la persona que soy hoy.
Abstract
9
ABSTRACT
Identifying general patterns of habitat selection, behavioural adaptations and life- history traits are central issues in evolutionary ecology. Many organisms have been studied to address these issues, but one of the groups with greater influence on current perspectives is birds. This thesis overall aim is to increase knowledge from an evolutionary perspective of the differences associated to habitat characteristics of life- history strategies and behavioural syndromes in cavity-nesting birds such as the Blue tit (Cyanistes caeruleus) and the Great tit (Parus major). By means of descriptive studies and field and captivity experiments this PhD thesis aim to explain the mechanisms underlying nest-site selection, diet composition, personality types and individual foraging strategies in contrasting habitat types.
The use of nestboxes to study bird breeding biology, as well their use as a management tool, is widespread. Different nestbox placements could be differentially chosen by birds; however the influence of determinant factors (e.g. nestbox density) in occupation rates or breeding parameters has not been sufficiently covered. We used the Blue tit as a model species to investigate the influence of nestbox position and breeding pair density on occupation rate and breeding success, controlling for habitat structure. Blue tits preferentially selected nestboxes located high on the tree and with fewest neighbours. Laying date was earlier in higher nestboxes and in those with fewer neighbours and at a greater distance from the nearest neighbour. Also, fledgling number was positively related to shrub cover and medium tree height, fledging mass was higher when distance to the nearest neighbor was greater and fledging tarsus was positively related to oak-species abundance. Our results suggest that disentangling the important factors for nestbox placement and distribution is important to adapt to species-specific requirements in each given habitat.
Nestlings diet composition and feeding rates seem to depend on parental effort, habitat type and their interactions. We compare the nestling diet of Blue tits in two Mediterranean forests (pinewood and oakwood) and its implications in breeding success through recordings within nestboxes when chicks were 11-days-old. We found
Abstract
10
that although caterpillars (Order Lepidoptera) constituted the largest proportion of nestling diet in both habitats, chicks in pinewood were fed more noctuid and tortricid larvae, showing a more homogeneous diet composition than those in oakwood. In contrast, spiders were more frequently fed to oakwood chicks. We demonstrated that these diet differences affect the number of chicks fledged and their body condition.
Habitat-specific selection pressures have been widely recognized but whether selection favours different personality types in different habitats has rarely been evaluated. We aimed to test whether personality-related differences in annual reproductive success differed between two populations of Blue tits occupying different Mediterranean habitats (oakwood and pinewood). We measured exploration and parental provisioning behaviours, and used a path analytical approach to ask how the interplay between these two behavioural traits affected reproductive success in each of these two habitats. We found that blue tits breeding in the pinewood were slow- exploring compared to blue tits breeding in the oakwood, suggesting the occurrence of personality-related differences in settlement, or phenotypic plasticity in response to habitat differences. Faster explorers were favoured in the pinewood, while there was no selection acting on exploration behaviour in the oak habitat. Our findings emphasize the importance of integrating habitat selection, plasticity, and personality in the study of behavioural evolution.
The tendency to innovate and the reactive-proactive personality axis have been linked to foraging behaviour but their role in driving intake rate and food selectivity remains unclear. We conducted standardized assays on wild-captured Great tits from different habitats to characterize individual variation in exploratory and innovative problem-solving performance, both of which are repeatable and have been linked to foraging behaviour. During trials, birds of known exploration behaviour were provided with three different types of food (sunflower seeds, peanuts and mealworms) in order to detect any diet preference, and daily energy intake was measured. There was no link between exploration behaviour and the amount of calories ingested;
however, bolder great tits consumed a higher proportion of sunflower seeds, while slower individuals preferred peanuts. Problem solving performance showed a significant positive correlation with energy intake for those birds that solve twice.
Abstract
11 Related to habitat type, birds from the coniferous patches ate more peanuts thought mealworms eaten were marginally higher in those from the deciduous plots. Our results evidence the relationship between exploration behaviour and foraging performance in captivity and contribute to the idea that birds may follow alternative foraging strategies, but obtaining the same energy intake.
Resumen
13
RESUMEN
Identificar patrones generales de selección de hábitat, adaptaciones comportamentales y rasgos de estrategias vitales son temas centrales de la ecología evolutiva. Muchos organismos han sido estudiados para tratar estos temas, pero uno de los grupos de mayor interés en las perspectivas actuales son las aves. El objetivo principal de esta tesis es aumentar el conocimiento, desde una perspectiva evolutiva, de las diferencias asociadas a las características del hábitat de las estrategias vitales y el comportamiento de aves que anidan en cavidades, como el herrerillo común (Cyanistes caeruleus) o el carbonero común (Parus major). Mediante estudios descriptivos y experimentos de campo y en cautividad, esta tesis doctoral pretende explicar los mecanismos subyacentes en la selección de lugar de nidificación, composición de la dieta, tipos de personalidad y estrategias de forrajeo individuales en diferentes tipos de hábitat.
El uso de cajas nido para el estudio de la biología de la reproducción en aves, así como su uso como herramienta de gestión, es generalizado. La colocación de las cajas nido en distintas ubicaciones puede generar que sean seleccionadas diferencialmente por las aves; sin embargo, la influencia determinados factores (p. ej., densidad de cajas nido) en las tasas de ocupación o los parámetros de cría no ha sido suficientemente estudiada. Se utilizó el herrerillo común como especie modelo para investigar la influencia de la posición de la caja nido y la densidad de parejas en su tasa de ocupación y éxito de cría, controlando por la estructura del hábitat. Los herrerillos seleccionaron preferentemente cajas nido ubicadas a mayor altitud en el árbol y con menor número de vecinos. La fecha de puesta fue más temprana en las cajas altas, con menos vecinos y situadas a una distancia mayor de la pareja vecina más cercana.
También, el número de volantones, su peso y su tarso estuvieron relacionados con la cobertura arbustiva y la altura de los árboles, la distancia al vecino más cercano y la abundancia de robles respectivamente. Estos resultados sugieren que investigar los factores influyentes en la colocación cajas nido y su distribución es importante para adaptarse a los requerimientos específicos en cada hábitat.
Resumen
14
La composición de la dieta de los polluelos y sus tasas de alimentación parecen depender del esfuerzo parental, el tipo de hábitat y de sus interacciones. Comparamos la dieta de volantones de herrerillo común en dos bosques mediterráneos (pinar y robledal) y sus implicaciones en el éxito reproductor a través de grabaciones dentro de cajas nido cuando los polluelos tenían 11 días de edad. Se encontró que aunque las orugas (orden Lepidoptera) constituyeron la mayor proporción de la dieta de los polluelos en ambos hábitats, aquellos pertenecientes al pinar fueron alimentados con más larvas de noctuido y tortrícido, mostrando una composición de la dieta más homogénea que los del robledal. Por el contrario, los polluelos del robledal fueron alimentados con arañas con mayor frecuencia. Además se mostró que las diferencias en la dieta afectan al número de polluelos volantones y su condición corporal.
Las presiones selectivas específicas de cada hábitat han sido ampliamente estudiadas, pero raramente se ha evaluado si la selección favorece determinados tipos de personalidad en diferentes hábitats. El objetivo fue comprobar si las diferencias en éxito reproductivo anual relacionadas con la personalidad difirieron entre dos poblaciones de herrerillo común en dos hábitats mediterráneos (pinar y robledal). Se midieron los comportamientos de exploración y de aprovisionamiento parental, y se utilizó el análisis de pautas (path analysis) para explorar cómo la interacción entre estos dos rasgos de comportamiento afecta al éxito reproductivo en cada uno de los dos hábitats. Se encontró que los herrerillos que crían en el pinar son exploradores más lentos comparados con los herrerillos del robledal, sugiriendo la aparición de diferencias de personalidad en función del lugar de cría, o plasticidad fenotípica en respuesta a las diferencias de hábitat. Los exploradores más rápidos se vieron favorecidos en el pinar, mientras que no hubo ninguna fuerza de selección actuando sobre el comportamiento de exploración en el robledal. Estos resultados acentúan la importancia de integrar la selección de hábitat, la plasticidad y la personalidad en el estudio de la evolución comportamental.
El comportamiento de innovación y la personalidad han sido relacionados con el comportamiento de forrajeo, pero su papel en la tasa de consumo y la selección de dieta aún no se ha determinado. Se caracterizó la variación individual en el comportamiento exploratorio y de resolución de problemas en carboneros comunes
Resumen
15 en cautividad procedentes de diferentes hábitats. Se les proporcionó tres tipos de alimento (semillas de girasol, cacahuetes y gusanos de la harina) con el fin de detectar preferencias en la dieta y se midió su ingesta de energía diaria. Los carboneros más exploradores consumieron una mayor proporción de semillas de girasol, mientras que los menos exploradores prefirieron los cacahuetes. El comportamiento de resolución de problemas estuvo correlacionado con un mayor consumo de energía. Los carboneros procedentes de parches de coníferas consumieron más cacahuetes, mientras que los procedentes de parches caducifolios consumieron cantidades de gusanos de la harina ligeramente mayores. Estos resultados evidencian la relación entre el comportamiento de exploración y de forrajeo en cautividad, y contribuyen a la idea de que las aves pueden seguir estrategias alternativas de forrajeo obteniendo el mismo aporte calórico.
INTRODUCTION
Cover picture Introduction. Pyrenean oak (Quercus pyrenaica) forest in Quintos de Mora (Author: Juan José Sanz).
Introduction
19 A major challenge in evolutionary ecology is to understand why and how populations respond to environmental heterogeneity (Blondel 2007). This is a prerequisite for explaining adaptation and predicting the evolutionary responses of organisms to several components of global change. Most populations exhibit some kind of phenotypic variation as a response to habitat heterogeneity which is universal whatever the spatial scale and the parameters considered (Bell et al. 1993). Traditional sources of environmental variation relate to factors associated with habitat quality and are formed from interactions between the availability of food and the distribution of parasites or competitors, while other sources of variation relate to the optimum conditions required by the focal species and its food supply, and include factors such as temperature and exposure (Wilkin et al. 2007).
Forest habitat quality is influenced by a combination of vegetation structure and floristic composition, micro-climatic conditions, plot area, and the nature of the surrounding landscape (Santos & Tellería 1995; Bellamy et al. 2003). European forests are a good example of mosaic landscapes, characterised by a large variety of habitats due to small-scale heterogeneity in such factors as altitude, geological substrate, isolation, and especially variation in dominant tree species (deciduous broad-leaved, evergreen broad-leaved, coniferous; see Blondel et al. 1993). In addition, due to intensive forestry management, the cover of mature deciduous forest has been greatly reduced both in temperate and boreal Europe (Riddington & Gosler 1995; Esseen et al.
1997). This habitat loss has become a major threat for many species in the last few decades (Owens & Bennett 2000; Sih et al. 2000; Heinrichs et al. 2016; Torres et al.
2016), and is also forcing animal populations to occupy alternative habitats instead of traditional ones (e.g. Newton 1998; Dias et al. 2014; Gossner et al. 2014; Harrison et al.
2016 for bird populations). The cost of settling in suboptimal habitats is dependent on an organism’s ontogenetic plasticity and evolutionary capacity to cope with rapidly changing environments (Lambrechts et al. 2004).
Fitness is strongly affected by local habitat quality through environmental characteristics (Cody 1981; Martin 1993), which thus generate strong selective pressures for optimal breeding habitat selection strategies (Martin 1993; Doligez et al.
2003). Therefore, individuals may need to gather information on potential breeding
Introduction
20
patches by assessing environmental quality in order to select a breeding habitat (Badyaev et al. 1996). Life history theory is based on the idea that reproductive costs generate trade-offs and that organisms take breeding decisions that maximize their fitness (Lessells 1991; Roff 1992). Plasticity in life history traits is ubiquitous in animal populations. It is usually measured using a “reaction norm” approach that describes patterns of phenotypic expression of genotypes across a range of environments, i.e.
how individuals respond to varying environments (Nussey et al. 2007).
Traditional behavioural ecological theory assumes that individuals are highly plastic and an individuals' behaviour should match the requirements of its environment and be reversible (Sih et al. 2004). The behavioural adaptive response of organisms to spatial heterogeneity may be either ontogenetic phenotypic plasticity, the potential for a given genotype to be expressed differently in different environments (Pigliucci 2001), or local adaptation, the evolution of traits in a local population that provide an advantage under its local environmental conditions (Kawecki & Ebert 2004). Several factors, including the scale, amplitude and variation of environmental heterogeneity, determine which of these two mechanisms is selected for (Blondel 2007). Therefore, identifying general patterns of habitat selection, behavioural adaptations and life-history traits are central issues in evolutionary ecology. Many organisms have been studied to address these issues, but one of the groups with greater influence on current perspectives is birds.
HABITAT INFLUENCE IN BREEDING PERFORMANCE Nest-site selection
Most bird species have specific habitat requirements for breeding (Cody 1981), but they are also able to use a wide range of habitats within a heterogeneous landscape (e.g. Jones 2001; Mörtberg 2001). Reproductive success depends on many interacting factors and consequently most nest-building birds are thought to expend time and energy choosing their nest site (Goodenough et al. 2009) by following possible cues such as their own current success, the presence of parasites or predators, or vegetation type (see Doligez et al. 2003 and references therein).
Introduction
21 Several studies have already reported differences among habitat types in cavity-nesting species, such as the Pied flycatcher (Ficedula hypoleuca; Siikamäki 1995), the Great tit (Parus major; Sanz 1998; Sanz et al. 2010), or the Blue tit (Cyanistes caeruleus; Blondel 2007; Arriero et al. 2010), due to habitat traits around the nesting sites can be responsible for local variation in breeding parameters. Thereby, for example laying date, clutch size or incubation effort, have been shown to be correlated with variation in temperature (e.g. Perrins 1965; Balen 1973; Dhondt et al. 1984;
Cresswell et al. 2004; Ardia et al. 2009), to topographical variation and woodland edge proximity (Wilkin et al. 2007), or to the succession stage of the vegetation (Arriero et al. 2010).
In addition, many non-habitat related phenomena influence nest-site selection.
Usually birds select sites with reduced predation risk (Nilsson 1984; Parejo & Avilés 2011) and competition (Newton 1994; Sorace & Carere 1996; Robles & Martin 2013), which allows for high levels of brood survival (Wesolowski 2002; Lõhmus & Remm 2005). It has been shown that breeding parameters, such as clutch size (Kluijver 1951;
Lack 1958; Perrins 1965), fledgling mass (Both 1998; Garant et al. 2004) and offspring recruitment (Both & Visser 2001) are negatively affected by population density in many cavity-nesting birds. Also, perceived predation risk has a strong influence on the ecology and behaviour of prey species, which are therefore likely to show adaptive strategies such as appropriate habitat choice (Orians & Wittenberger 1991), and it may affect its fitness by reducing clutch size (Perrins 1977; Slagsvold 1984; Lundberg 1985) or the nest attendance required (Slagsvold 1984). There needs to be explicit recognition of how habitat-related and non-habitat related parameters affect both the choices made by individuals and the fitness consequences of those choices (Jones 2001).
Nestling diet and parental provisioning effort
Habitat type and nest-site characteristics determine also food resources available for breeding birds (Blondel et al. 1991; Mägi 2007). Food availability in right time to feed nestlings is considered as a major factor influencing the evolution of life-history in birds (e.g. Lack 1950; Perrins 1991). The seasonality of different habitat types
Introduction
22
determines the peak availability of certain food types and potentially affects breeding performance (Burger et al. 2012). Because many bird species raise offspring during a very short period of the year (Dias & Blondel 1996; Lambrechts et al. 1997; Blondel et al. 1999), there is selective pressure to synchronize breeding with preferred food peaks (i.e. at maximal availability). For example, previous studies have demonstrated that several tit species (Parus spp.) use a series of environmental cues before or around the egg laying stage to anticipate a period of maximum caterpillar availability (Lambrechts
& Perret 2000; Cole et al. 2015; Hinks et al. 2015), as this food type is only available during a brief period. Thus, caterpillar phenology seems to determine the optimal time window for Tits reproduction, and the extent of synchrony with their main prey is crucial, as nestling development outside this period has severe fitness consequences (Noordwijk et al. 1995; Samplonius et al. 2016). Therefore, it is important to determine how bird species adapted to a specific habitat cope with available food resources (e.g.
Barba et al. 2004), such that preferred food types and food abundance is determined by floristic composition (Blondel et al. 1991; Lundberg & Alatalo 1992).
BEHAVIOURAL SYNDROMES AND HABITAT-RELATED DECISIONS Habitat-specific differences in selection on personality
Behavioural differences between individuals that are consistent over time and across situations are commonly referred to as animal personality (Gosling 2001; Sih et al.
2004; Réale et al. 2007). Personality was firstly studied in considerable detail in a few primates, domesticated animals and laboratory rodents (Sih et al. 2004); however, much research has been done in a broad range of ‘non-model organisms’ (Gosling 2001). One of the most intensively studied species for animal personality research is the Great tit. Theory in this area predicts that different personality types may be favoured under different environmental conditions or contexts (Dall et al. 2004; Sih et al. 2004; Réale et al. 2010; Wolf & Weissing 2010). Personality differences are also thought to mediate trade-offs between life-history traits (Wolf et al. 2007; Réale et al.
2010; Nicolaus et al. 2016), and affect overall fitness (Sih et al. 2004; Sih & Bell 2008).
The reactive-proactive personality axis is common in many vertebrate groups and has been linked to life-history trade-offs because, at one end of the continuum,
Introduction
23 reactive or responsive individuals tend to be slow but thorough-exploring, cautious and shy, compared with those at the other end of the continuum, where proactive routine-forming individuals tend to be fast but superficial-exploring, bold and predation-risk prone (Wolf et al. 2007). The pace-of-life syndrome (POLS) hypothesis for animal personality proposes that variation among individuals in life-history strategies is associated with long term maintenance of consistent differences in behaviour, implying that bold individuals have a greater annual reproductive success but shorter life span compared to shy individuals but may overall have a similar fitness (Réale et al. 2010). Furthermore, the ability to acquire high-quality territories has also been associated with exploration behaviour (Dingemanse & Goede 2004; Both et al.
2005), and females in such territories typically lay earlier in the season, and produce larger clutches compared to those breeding on low-quality territories (Lambrechts et al. 2004). Differential settlement may therefore constitute a mechanism by which differences in pace-of-life are mediated, which implies that individuals might settle in habitats that best match their phenotype (habitat matching hypothesis; Edelaar et al.
2008).
Behavioural patterns of food intake
Finding food and ingesting nutrients are the most fundamental activities in the natural world, and thus natural selection favours individual organisms that do so optimally (Pyke 1984; Stephens & Krebs 1986). Nevertheless individuals vary in how they acquire nutrients, potentially leading to effects on foraging efficiency and fitness (Partridge 1976; Burskirk et al. 1989; Bolnick et al. 2003). Thus, the reactive-proactive personality axis has also been linked to foraging. Individual differences in foraging may arise because of correlations with other personality traits, that constrain foraging plasticity and can lead to alternative strategies (DeWitt et al. 1998; Gosling 2001; Bolnick et al.
2003; Dall et al. 2004; Sih et al. 2004). In this context, local adaptation may give birds preferences for handling food of different kinds depending on what they primarily feed on in their habitat (e.g. Balen 1973). Also, there is wide evidence that the proactive- reactive axis is associated with metabolic rate (Careau et al. 2008; Bouwhuis et al.
Introduction
24
2014) and energy intake rate (Davies 1977; Wansink & Tinbergen 1994; Wilson et al.
2015), which are closely related to foraging behaviour performance.
In parallel to research on personality, the implications of individual cognitive variation for adaptive behaviour is also attracting increasing attention (see Morand- Ferron et al. 2016 and references therein). For example innovativeness - where individuals feed on novel food types or adopt new foraging techniques - is considered to be an important component of animal cognition (Roth & Dicke 2005; Lefebvre 2011;
Reader et al. 2011;) but is also influenced by personality (Morand-Ferron et al. 2011).
Innovative problem-solving performance influences foraging (Oers et al. 2004; Quinn et al. 2009, 2016; Cole & Quinn 2012), and it is not only thought to allow individuals increase their food intake or enhance their feeding efficiency (Reader & Laland 2003;
Morand-Ferron & Quinn 2011); it has been viewed as an alternative foraging strategy that helps some individuals avoid costs associated with intense competition (Bolnick et al. 2003). Nevertheless, little is known about the influence of personality on foraging strategies related to food intake and diet choice, and the extent to which innovativeness may improve foraging success or whether it simply represents an alternative strategy.
Introduction
25
AIMS AND OBJECTIVES
This thesis overall aim is to increase knowledge from an evolutionary perspective of the differences associated to habitat characteristics of life-history strategies and behavioural syndromes in cavity-nesting birds such as the Blue tit and the Great tit.
This PhD thesis involves descriptive studies and field and captivity experiments which aim to explain the mechanisms underlying nest-site selection, diet composition, personality types and individual foraging strategies in contrasting habitat types.
The specific objectives of the present thesis are listed below:
Objective I. Identify the most determinant factors in nest-site selection and analyse their influence on the breeding performance of a Blue tit population settled in a sub- optimal habitat.
Objective II. Determine how habitat type leads to differences in Blue tit nestling diet composition, differential parental effort and its influence in fitness.
Objective III. Investigate Blue tit personality performance in two different habitats, as this would help to explain the maintenance of individual variation in behaviour.
Objective IV. Test whether variation among individuals foraging behaviour is associated to consistent differences in behavioural syndromes, i.e. personality and problem solving performance, and also in what manner habitat type determines foraging strategies in Great tits.
These objectives have been addressed through four chapters. First, (chapter I) we have evaluated the influence of breeding site selection on breeding success in a Blue tit population in a Mediterranean pine plantation. We have settled nestboxes in different locations and quantified the surrounding habitat parameters and population density to identify the most influencing factors for nest-site selection and breeding success; also we have reported the main characteristics that are needed to take into account when providing nestboxes to wild bird populations. In the next chapter
Introduction
26
(chapter 2), we have described Blue tit nestlings diet composition and its variation between two Mediterranean forests, a native oak forest and a pine plantation. By means of video recordings we aim to determine the effects of parental feeding behaviour and diet selection on the breeding performance in a “preferred” (oakwood) versus “alternative” (pinewood) breeding site. In the third chapter (chapter 3) we have measured two key behavioural traits, parental provisioning and exploratory behaviour, and have investigated how those traits mediated short-term fitness (annual reproductive success) in the same breeding Blue tit populations than in chapter 2.
Finally, in the last chapter (chapter 4) we have performed exploration behaviour and problem-solving tests to wild-caught Great tits from two different habitat types (deciduous and coniferous) in southern Ireland to test their association with foraging performance and to disentangle whether local adaptation influences behavioural syndromes on individual’s food selection.
Introduction
27
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METHODS
Cover picture Methods. Tarsus length measurement with a digital calliper (Author: Roger Colominas).
Methods
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STUDY SPECIES
Blue tit
The Eurasian Blue tit (Linneo 1758) is a small (7–11 g) non-migratory insectivorous passerine, from the family Paridae, common throughout the western Palearctic. It usually prefers deciduous forests, but can also be found in evergreen and mixed forest habitats (Cramp & Perrins 1993). During the breeding season, pairs of Blue tits defend territories and breed in small natural cavities (e.g. in trees), but also accepts nestboxes to build the nest, which consist of a basic moss layer lined with feathers and plant material (aromatic plants, moss and grass). Laying date of the first egg typically is around the second half of April, and the clutch size range from 4 to 14 eggs (Gibb 1950; Nur 1984). Females incubate the eggs around 13 days, and both parents take care of the nestlings. Blue tit nestlings are mostly fed caterpillars found on young oak tree leaves (Quercus spp., Bańbura et al. 1994, 1999), and they leave the nest 17–20 days elapsed after the date of hatching. During the winter months, Blue tits join mixed foraging flocks near to their original breeding or natal territory.
Mediterranean populations of Blue tit are at the southern end of the distribution range of the species (Cramp & Perrins 1993). In this region, its optimal habitat, the deciduous forests, are highly fragmented due to natural and anthropic factors and appear relegated to small patches located in shady spots or elevated areas.
Great tit
The Great tit (Linneo 1758), is also an insectivorous songbird from the family Paridae, but bigger than the Blue tit (body mass 18–20 g). It occurs in forest areas in much of Eurasia, and occupies a wide range of habitats, from open deciduous woodlands, mixed forests, forest edges and man-made habitats.
Similarly to the Blue tit, breeds in secondary nest holes and readily accepts artificial nest holes (i.e. nextboxes) for breeding (Kluijver 1950; Perrins 1965; Drent 1983).
During the breeding season Great tits are territorial, whilst form inter-specific flocks during winter. Usually this species lay between 5–12 eggs which are incubated by the female for 13–14 days. Nestlings are fed by both parents until they are independent at 2–4 weeks (Perrins 1965; Harrison & Castell 1998). It is well known that caterpillars are
Methods
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the preferred food for many woodland passerines including Great tits, which feed off- spring a diet consisting of up to 95% caterpillars (Gosler 1993). Great tits are usually resident and non-migratory.
STUDY AREAS
Mediterranean: Quintos de Mora
Quintos de Mora, central Spain (39° 25’ N, 4° 04’ W, Los Yébenes, Toledo), is a national game reserve (6,864 ha) managed by the Organismo Autónomo Parques Nacionales (OAPN). This area exhibits considerable habitat heterogeneity and is partitioned into two main landscape units including a huge flood-plain (”raña”) with scattered trees and 750 m above sea level, and two surrounding mountain ranges (“El Pocito”
mountain chain to the south and “Las Guadalerzas” mountain chain to the north) with a maximum elevation of 1,240 m a.s.l. In the mountain areas, Pyrenean oak (Quercus pyrenaica), Zeen oak (Quercus faginea), Strawberry tree (Arbutus unedo) and Mediterranean shrubs such as Heath (Erica spp.), Common hawthorn (Crataegus monogyna), Blackberry (Rubus sp.) or Rockrose (Cistus ladanifer) dominate, but in humid environments Ash maple (Acer monspessulanum) is also common. The plain is covered by scattered Holm (Quercus rotundifolia) and Zeen oaks with understory pasture, and some Maritime pine (Pinus pinaster) and Stone pine (Pinus pinea) plantations from the 1940s are distributed at the foothills. These pine patches penetrate the areas of the mountain range where they are mixed with the original vegetation forming a habitat mosaic. The area is located at the Mesomediterranean bioclimatic zone, with a continental Mediterranean climate and presents irregular temperature and rainfall regimes (584 mm mean annual rainfall). This reserve has a high density of big-game hunting species such as wild boar (Sus scrofa) and Red deer (Cervus elaphus). For more details about this natural reserve see Tornero 2003 and San Miguel et al. 2011.
Three of the studies presented in this thesis were conducted in this reserve during the springs of 2012, 2013 and 2014. The study sites were Pyrenean oak (Quercus pyrenaica) dominated forests and a hillside dominated by Maritime pine (Pinus pinaster; Table 1, Figure 1), where 260 nestboxes were erected mounted on tree
