Foraging behavior of the lesser kestrel under the movement ecology paradigm revealed using biologgers

Resumen

The recent revolution of biologging technology has provided novel insights into free-ranging animal ecology with an unprecedented spatiotemporal resolution. As a consequence, literature on animal movement has vastly increased. This is the breeding ground over which Movement Ecology has arisen as a new discipline to unify all movement research under a common framework. Accordingly, Movement Ecology states that individual movement results from the interaction between four elements: individual state or motivation (why to move), motion abilities (how to move), navigation capacities (when and where to move), and external factors (both biotic and abiotic). This paradigm stresses the necessity to evaluate these elements in order to get a comprehensive understanding of the movement path. Thus, the Movement Ecology aims to answer old ecological questions and also to generate new ones thanks to the application of the latest technological advances to research on movement. The lesser kestrel (Falco naumanni) is a small insectivorous falcon that breeds in colonies across the Palearctic and winters in Africa. This species suffered a severe world population decline during the second half of the 20th century because of the agricultural intensification. The lesser kestrel has been well-studied during the breeding period, especially in its foraging ecology and mainly focusing on habitat selection and diet. In this PhD thesis, we investigated the foraging ecology of the lesser kestrel from the perspective of Movement Ecology by deploying high-frequency GPS and tri-axial accelerometers dataloggers on 35 individual lesser kestrels at two breeding colonies during four consecutive breeding seasons in southern Spain. Among external factors influencing movement, wind has been reported as one of the most important for flying animals. For this reason, we evaluated the influence of both wind speed and direction on lesser kestrel decisions about which direction to head when leaving the breeding colony to forage throughout the breeding season (Chapter One). We did not find any strong effect of wind conditions on lesser kestrel flights probably due to the prevailing winds registered in the study area that were weak and constant in direction. However, we found that kestrels show a uniform distribution of foraging trip departure directions when foraging early in the breeding season, which seems to be related to more exploratory flights when prey abundance is low and individuals have little knowledge about prey spatial distribution. Meanwhile, at the end of the breeding season kestrels concentrate their departure directions towards high-quality foraging areas when preferred prey abundance, individual experience, and energy demand derived from rearing the offspring are higher. Therefore, individual internal factors (mostly navigation capacities) appear to guide kestrel decision about departure directions of foraging trips, with little effect of external factors like wind. In some species with biparental care each member of the breeding pair cooperates by assisting its partner in every reproductive task, whereas in others each parent specializes in different tasks. The latter case is known as reproductive role specialization. In role-specialized species, such as the lesser kestrel, it is expected that sex will be an important motivational element that influence movement behavior in order to satisfy the temporally dynamic requirements during reproduction. We analyzed the effect of role specialization of the lesser kestrel on its foraging movement patterns throughout the breeding season (Chapter Two). Overall, we found differences in foraging movements between sexes in accordance with the general trend of raptor role specialization. Males fly larger daily distances and perform higher number of shorter foraging trips per day than females being the main responsible for provisioning tasks. Meanwhile, lesser kestrel females tend to stay longer than males at the colony through the day, which agrees with being the main responsible for nest protection, egg incubation and chick brooding. Furthermore, the lesser kestrel shows a sexual spatial segregation, with females constantly flying towards foraging areas located farther from the colony than males. This might be the result from an adaptive foraging strategy based on role specialization in order to avoid prey depletion in the surroundings of the colony and reduce intersexual competition between members of the breeding pair to be successful in reproduction. Most avian species move by flying and they can do it either through flapping, which requires muscles to convert chemical energy into work, or through soaring-gliding, which harvests kinetic energy from moving air masses to replace muscle work. We studied the flight strategy of the lesser kestrel during foraging trips and the effect of solar radiation (as a proxy for thermal updrafts) on several foraging trip parameters during the breeding season (Chapter Three). Surprisingly, we found that the lesser kestrel, which has been traditionally considered as a flapping raptor, relies heavily on thermal soaring during foraging trips, especially at higher values of solar radiation. Individuals fly at slower speeds at higher altitudes and reach farther distances from the colony during foraging trips with thermal soaring events in comparison to those without them. This guides to a circadian pattern of lesser kestrel foraging behavior: individuals fly by flapping their wings towards foraging areas located closer to the colony when thermals are weak or absent, whereas they fly towards foraging areas farther away by soaring on thermals as soon as they are formed. Theoretical flight models indicate that, given the lesser kestrel preference for feeding on large grasshoppers and considering the average distance traveled along the trips, foraging by flapping their wings would result in a negative energy balance for the family group. Apart from tracking devices, a series of animal-borne biological sensors has been developed to help fully understand individual movement, perhaps being accelerometers the most widely used devices nowadays. Tri-axial accelerometers measure body acceleration across three spatial axes at high temporal resolutions (typically 10 Hz or more). On the one hand, tri-axial accelerometry helps inferring animal behavior with no need of direct observation and, on the other hand, it has been also proved to be an effective methodology to measure animal energy expenditure. In Chapter Four, we built a behavioral classification model based on tri-axial accelerometer and GPS data for the lesser kestrel. Then, we investigated the effect of internal (breeding phenology, role specialization) and external factors (prey availability, weather conditions) on the behavioral time and energy budget of the lesser kestrel during the day in general and when foraging in particular. Our behavioral classification model performs well when classifying free-ranging lesser kestrel behaviors. Flapping and hovering flights require more energy than soaring-gliding flights, and these flight behaviors consume more energy than stationary (incubating/brooding and perching) behaviors. The daily time and energy budget of the lesser kestrel is mostly determined by behavior-specific costs and the role specialization between sexes. Lesser kestrels gradually replace flapping with soaring-gliding during commuting flights as solar radiation increases, that is, as thermal updraft gets stronger. Lesser kestrels also progressively substitute perching (i.e., sit-and-wait hunting strategy) with hovering flights (i.e., active hunting strategy) at the foraging patch as wind speed increases, that is, as they experience stronger lifts to be aloft. However, kestrels seem to decide which hunt strategy to use regarding the activity level of the preferred prey, which is influenced by air temperature. Thus, individuals increase the use of hovering flights as air temperature, and prey activity level, also increase. Overall, our results support predictions derived from the optimal foraging theory and suggest that the lesser kestrel prioritizes saving energy than time when foraging throughout the breeding season. This PhD thesis fills a gap of knowledge about the foraging behavior of the lesser kestrel through using the newest biologging technology, and so it has helped to understand better the lesser kestrel ecology during the breeding period.