The role of olfaction in the relationship between birds and their environment

Resumen

An increasing number of studies have shown that birds can detect odours in several ecological contexts. The ability to use the sense of smell to detect and respond to chemical cues of prey and predators is essential for the survival of birds, because foraging and predator avoidance are essential requirements with important consequences for the fitness of birds. This thesis considers birds both as predators and prey, providing valuable information about the chemical ecology of birds. Birds have developed different methods for prey location in order to maximize their foraging effort and increase their fitness. Previous evidence shows that birds are able to perceive odours in the process of foraging. This thesis studies the chemical ecology of birds to understand the role of chemical cues in multi-trophic interactions involving trees, insects and insectivorous birds, and whether birds are also able to detect the chemical cues emitted by the prey itself to locate them and maximise their foraging effort. Plants emit herbivore-induced plant volatiles (HIPVs) when they are attacked by herbivorous arthropods to attract natural enemies of herbivores, and previous studies have suggested that insectivorous birds can detect the HIPVs and use them for prey location in order to optimize their foraging effort in different plant-herbivory-predator systems. However, our results showed that neither insectivorous adult birds nor inexperienced nestlings were attracted to trees treated with methyl jasmonate (MeJa), a phytohormone involved in the development of the defence response of plants and in the release of HIPVs (Chapter 1). Further studies are needed to disentangle whether the potential differences in the emission of volatiles between herbivore-infested plants and plants treated with MeJa can explain the lack of attraction of bird predators to MeJa-treated Pyrenean oak trees. In addition to use indirect cues to find their prey, we show that insectivorous birds are able to detect the pheromones emitted by winter moth (Operophtera brumata) females to attract males, exploiting the prey pheromones as a method of prey location (Chapter 2). Therefore, the attraction of birds to the pheromones of female moths adds birds to the list of predators that are able to eavesdrop the chemical cues emitted by their prey for mate attraction. In addition to study the use of chemical cues by birds to locate prey and maximize their foraging effort, we have explored in depth the ability of birds to detect the chemical cues of predators to accurately assess the risk of predation and adjust their antipredatory behaviour accordingly. Birds have developed different strategies to reduce the risk of predation, because the ability to distinguish between threatening cues and non-threatening cues is essential to avoid predation and increase the reproductive success. This thesis explores whether birds are able to ascertain predator presence and respond with different adaptive behavioural strategies when they detected predator chemical cues inside the nest (Chapter 3-5) or when they found predator cues in the surroundings of their nests (Chapter 6). Many bird species can detect predator chemical cues and use them to assess the level of predation risk in different contexts. For example, previous evidence suggests that birds in captivity are able to detect predator scents and avoid roosting in nest boxes containing such cues. We tested whether birds also show this avoidance response under natural conditions, and we found no differences in the use of nest boxes for roosting in relation to the predation risk perceived (Chapter 3). This result suggests that chemical cues indicating the potential presence of a predator are not enough for birds to avoid roosting in nest boxes under natural conditions during the winter. In natural conditions, territory maintenance or thermoregulatory benefits of roosting in nest boxes may overcome the perceived risk of predation when only predator chemical cues are present. Further research is needed to assess whether this lack of avoidance of roosting in predator scented nest boxes is maintained when thermoregulatory costs of sleeping outside nest boxes are lower. Predation can also determine the survival and the reproductive success of birds during the breeding period. Therefore, birds have also developed different behavioural strategies to reduce the risk of predation during the reproduction. For example, bird species that nest in open areas often cover their eggs to decrease the risk of predators detecting the clutches. We simulated the visit of a predator to the nest by introducing chemical cues of a predator inside the nest box during the laying period, and we found that birds exposed to an increase in the risk of predation covered their eggs more frequently than birds exposed to an odorous control (Chapter 4). Therefore, our results suggest that egg covering behaviour may have evolved an antipredator strategy to reduce the risk of egg predation and increase the reproductive success in cavity nester birds. This thesis also shows that birds modified their parental behaviour when they detected predator chemical cues inside the nest, exhibiting behavioural differences between females and males in the risk afforced when taking care of nestlings. When parents were exposed to predator chemical cues, females assumed greater risk than males. Differential investment in the reproduction may explain this sexual differences in risk taking behaviour, as females invest more time and energy than males in nest-building, laying and incubation. Therefore, the value of nestlings may be higher for the females than for the males and females assume greater risks to ensure nestling growth. The results also showed that nestlings detected the chemical cues. Specifically, nestlings respond by decreasing their begging behaviour when they were exposed to the chemical cues of a heterospecific animal, probably to minimize detectability by predators (Chapter 5). Further research in other species with different sexual investment during the reproduction are needed to explore how females and males respond to percived predation risk in relation to the reproductive value of the offspring for each parent sex. In addition to use predator chemical cues, according to the threat sensitive hypothesis, birds may use more than one predator cue in order to accurately assess the level of predation risk. This may be especially important to minimize the risk of predation during the breeding period. In this assessment, the behaviour of predators can provide important information to evaluate the motivation of the predator to launch an attack. However, there were no previous studies that have examined the importance of behavioural, visual and chemical cues of predators on the antipredatory behaviour of birds. Our results show that birds were able to detect the behavioural cues of predators and exhibited greater antipredatory behaviours when exposed to a live predator than to a stuffed model with chemical cues (Chapter 6). This result suggests that birds are able to use the behavioural, visual and chemical cues of predators to assess the level of predation risk and adjust their antipredatory behaviour accordingly. Our results are in accordance with the threat sensitive hypothesis that suggests that natural selection may have favoured the assessment of predation risk by integrating all information available from all predator cues presented to adjust the degree of antipredatory behaviour of animals. Overall, this thesis provides new evidence about the use of olfaction by birds in multiple ecological contexts, and it shows how birds have developed different strategies to solve two of their main needs: foraging and predator avoidance.