Respuestas comportamentales y fisiológicas frente al parasitismo de cría y a la depredación de nidos en dos especies de paseriformes

Resumen

Brood parasitism and nest predation are two of the most important selective pressures in birds, particularly in altricial species, which are the species whose nestlings, being born unfeathered, blind and helpless, must be cared by parents. Avian brood parasitism in one of the best examples of a coevolutionary process, where hosts evolve a series of adaptations to counteract and limit the fitness costs imposed by brood parasites. Among these defensive adaptations, the recognition and rejection of the parasitic egg are decisive. Nest predation, on the other hand, is a classic example of agonistic interaction, being the most important force shaping nestlings’ life-history traits since it represents the first cause of mortality for avian offspring. The main aim of this thesis is to expand our knowledge on how these two extremely important selective pressures shape some behavioural and physiological responses in birds. In the first part of the thesis we provide new information on the breeding biology of a poorly known bird species, the Western Bonelli’s warbler Phylloscopus bonelli, which is also a potential host for the common cuckoo Cuculus canorus in Southern Europe (Chapter 1). This novel and detailed information is essential not only for expanding our understanding of this species but also to draw attention to the potential risks that it might face in the near future, considering the reduction that this species has suffered in the study area during recent years. The second part of the thesis focuses on brood parasitism. Using the Bonelli’s warbler, we first investigated a methodological question (Chapter 2), whether different characteristics of the parasitic egg (size and material) used in egg-rejection experiments could affect the egg-rejection behaviour of the host. This kind of methodological studies, even though seldomly done, are of key importance in order to determine the validity of experiments in the field. We found that plasticine may misrepresent the responses to experimental parasitism, at least in small host species, because this material facilitates egg ejection, provoking a decrease in nest desertion rate. We also found that small parasitic eggs could be ejected by this nest-abandon species and that warbler nests parasitized with large eggs were more often deserted, thus indicating that nest desertion occurs because of the constrains imposed by the size of parasitic eggs. Within the framework of this second part, and linking with the next one, we also studied the interaction between these two important selective pressures: brood parasitism and nest predation (Chapter 3). In this case we used another (presumably) former host species of cuckoos, the common blackbird (Turdus merula) which suffers high nest predation levels. Several studies on parasite-host systems have investigated adaptations and counter-adaptations associated to this biological interaction, but only recently researchers have understood that the recognition and rejection of parasitic eggs are part of a complex process, in which the decision of rejecting mainly depends on the costs associated to that action, the external stimuli perceived by the host or its internal status of motivation. Therefore, phenotypic plasticity of egg-rejection behaviour might play an important function in the promotion of evolutionary changes. Predation could be one of the environmental pressures that may affect the egg-rejection process, particularly affecting the cost-benefit trade-off. Nevertheless, studies that explore the interaction between predation and brood parasitism are limited. We found that blackbirds exposed to risk of an adult predator showed a partial increase in egg recognition and a significant lower ejection rate, whereas the risk of an offspring (egg) predator did not modify their anti-parasitic behaviours. Interestingly, this effect increased towards the end of the breeding season. This findings open a new research line in the study of brood parasitism and provide new knowledge in our understanding of the regulation of the egg-rejection process. The third part of this thesis focus on nest predation. Studies on the topic have explored the adaptations of prey to predator pressure (i.e. anti-predator strategies), focusing principally on morphological and behavioural defences, while, only recently, researchers have realized that also physiology has a critical role in anti-predator strategies. Predation, and in particular the risk associated to predation, is known to modify some physiological functions of preys like their hormonal responses. However, very little is still known about its effect in other critical physiological systems. The immune system is definitely an important physiological component, which promotes the survival of an organism by defending it from external pathogens, diseases and infection. Despite recent evidence showing that predation risk can alter the immune response of prey, this link has been greatly overlooked. In the first chapter of this part we explored whether a short-term nest predation risk, typical of a predator encounter, can provoke changes in the immune system of nestlings (Chapter 4). Using blackbirds again, we experimentally tested several levels of nest predation risk and measured a complete set of immunological variables in order to capture the most detailed picture of this potential relationship. We found that nest predation risk induced an increase in ovotransferrin, immunoglobulin levels and the number of lymphocytes and eosinophils, suggesting a general activation of the immune response which will prepare nestlings to cope with the possible inflammation or infection provoked by a predator attack. Interestingly, only high and extreme levels of risk caused the immunological changes, indicating that nestlings would be able to modulate their immune responses according to the perceived level of threat. Finally, we tested whether a long-term increase in nest predation risk, more typical of the ecology of fear concept, could also entail immunological changes in nestlings (Chapter 5). Changes in the immune system can impose important costs in organisms, thus, it is possible that the responses to short- or long-term predation risk are different. In addition, the nestling period is particularly critical for birds as, during this phase, they invest most of their resources in the development and this could interfere with the immunological response to predation risk. This is actually what we found. Our manipulation of predation risk during the whole nestling period induced a reduction of immunoglobulins but an increase in lymphocytes, suggesting different effects depending on the duration of the threat and the costs associated with the immunological changes. Interestingly, in the last two studies (Chapters 4 and 5), we found that the condition of the organism (i.e. health status or body condition) affected the immunological responses to nest predation. For instance, only those nestlings without endoparasites or in good body condition were able to increase their immune response for the short-term manipulation, while body condition and growth rate mediated the immunological responses for the long-term manipulation. This thesis confirms that both brood parasitism and nest predation, through the behavioural and physiological mechanisms that induce, are two decisive selective pressures that strongly shape the evolution of the adaptations in altricial birds. Predation risk is able to trigger an immune response in the organism and this might have important consequences in developing organisms, such as nestlings, as it can alter the normal trade-offs between immunity and the physiological processes of the development. Further we demonstrated the interplay between predation and brood parasitism, offering a new perspective of the forces that may shape the evolution of the anti-parasite defences in host.