A refined magnetic pulse treatment method for magnetic navigation experiments with adequate sham control: a case study on free-flying songbirds.

Migratory songbirds may navigate by extracting positional information from the geomagnetic field, potentially with a magnetic-particle-based receptor. Previous studies assessed this hypothesis experimentally by exposing birds to a strong but brief magnetic pulse aimed at remagnetizing the particles and evoking an altered behaviour. Critically, such studies were not ideally designed because they lacked an adequate sham treatment controlling for the induced electric field that is fundamentally associated with a magnetic pulse. Consequently, we designed a sham-controlled magnetic-pulse experiment, with sham and treatment pulse producing a similar induced electric field, while limiting the sham magnetic field to a value that is deemed insufficient to remagnetize particles. We tested this novel approach by pulsing more than 250 wild, migrating European robins (Erithacus rubecula) during two autumn seasons. After pulsing them, five traits of free-flight migratory behaviour were observed, but no effect of the pulse could be found. Notably, one of the traits, the migratory motivation of adults, was significantly affected in only one of the two study years. Considering the problem of reproducing experiments with wild animals, we recommend a multi-year approach encompassing large sample size, blinded design and built-in sham control to obtain future insights into the role of magnetic-particle-based magnetoreception in bird navigation.

The urge to breed early: Similar responses to environmental conditions in short- and long-distance migrants during spring migration.

Birds migrating different distances experience different temporal, energetic, physiological, and physical constraints throughout migration, which is reflected in their migration strategy. Consequently, we predict different behavioral decisions to similar environmental cues between short- and long-distance migrants, which has been documented for autumn migration. Here, we focus on the question whether trade-off decisions regarding departure, routing, and landing when alternating between migratory endurance flights and stopovers also differ during spring migration. As early arrivals at the breeding grounds should be ultimately favored regardless of migration distance, selection may favor more similar behavioral decisions in spring than in autumn. We radio-tagged short- and long-distance migratory songbirds at stopover sites along the German North Sea coast during spring and automatically tracked their migratory behavior using a large-scale network of receiver stations. Once departed, birds could either cross the sea or detour along the coast. We corrected for spatially biased detection data, using a hierarchical multistate model to assess how birds respond to variation in environmental conditions in their day-to-day departure decisions and route selection. The day-to-day departure probability was higher in long-distance migrants independently of the routing decision. Irrespective of migration distance, all species more likely departed under light winds and rainless conditions, while the influence of air pressure change and relative humidity was species-specific. By accounting for detection probabilities, we estimated that about half of all individuals of each species crossed the sea but did not find differences between short- and long-distance migrants. Offshore flights were more likely when winds blew offshore and began earlier within the night compared with onshore flights. Our results suggest that selection more similarly affects birds of different migration distances in spring than in autumn. These findings put the focus toward how ultimate mechanisms may shape departure and routing decisions differently between migration seasons.

The oxidative balance and stopover departure decisions in a medium- and a long-distance migrant.

BACKGROUND: Birds have extremely elevated metabolic rates during migratory endurance flight and consequently can become physiologically exhausted. One feature of exhaustion is oxidative damage, which occurs when the antioxidant defense system is overwhelmed by the production of damaging reactive oxygen species (ROS). Migrating birds have been shown to decrease the amount of oxidative lipid damage during stopovers, relatively stationary periods in between migratory flights. It has therefore been argued that, in addition to accumulating fuel, one of the functions of stopover is to restore the oxidative balance. If this is so, we would expect that migrating birds are unlikely to resume migration from stopover when they still have high amounts of lipid damage. METHODS: To test this hypothesis, we measured parameters of the oxidative balance and related these to stopover departure decisions of song thrushes (Turdus philomelos) and northern wheatears (Oenanthe oenanthe), a medium- and long-distance songbird migrant, respectively. We measured malondialdehyde (MDA) concentration, a biomarker for oxidative lipid damage, and total non-enzymatic antioxidant capacity (AOX), an overall biomarker of protection against ROS. Stopover departure decisions were determined using a fully automated telemetry system set-up on our small island study site. RESULTS: The decision to resume migration was not related with MDA concentration in either study species, also not when this was corrected for circulating fatty acid concentrations. Similarly, AOX did not affect this decision, also not when corrected for uric-acid concentration. The time within the night when birds departed also was not affected by MDA concentration or AOX. However, confirming earlier observations, we found that in both species, fat individuals were more likely to depart than lean individuals, and fat northern wheatears departed earlier within the night than lean conspecifics. Northern wheatears additionally departed earlier in spring with more southerly winds. CONCLUSIONS: We found no support for the idea that stopovers departure decisions are influenced by parameters of the oxidative balance. We discuss possible reasons for this unexpected finding.

Departure, routing and landing decisions of long-distance migratory songbirds in relation to weather.

Migrating birds flexibly adjust their individual migratory decisions, i.e. departing, routing and landing, based on intrinsic (e.g. energy stores) and extrinsic (e.g. landscape features and weather) factors modulating the endogenous stimuli. So far, these decisions have mostly been studied separately. Notably, we lack information on which factors landing decisions during active flight are based on. Therefore, we simultaneously recorded all three decisions in free-flying long-distance migratory songbirds in a coastal stopover area via regional-scale radio-telemetry and related them to the prevailing weather. Birds departed under favourable weather conditions resulting in specific nights with increased departure probability. Once departed, birds could either fly offshore or take a route along the coast, which was predicted by wind support. Radio-tracking revealed that departed individuals more likely interrupted their migratory endurance flight under overcast or headwind conditions. Studying departure, routing and landing decisions in concert, we highlight the importance of weather as a common driver across all migratory decisions. By radio-tracking individuals between stopovers, we provide evidence that avoidance of adverse weather conditions is an important function of stopover. Understanding how birds adjust migratory decisions and how they affect the timing of migration and survival is key to link migration performance to individual fitness.

A magnetic pulse does not affect free-flight navigation behaviour of a medium-distance songbird migrant in spring.

Current evidence suggests that migratory animals extract map information from the geomagnetic field for true navigation. The sensory basis underlying this feat is elusive, but presumably involves magnetic particles. A common experimental manipulation procedure consists of pre-treating animals with a magnetic pulse, with the aim of re-magnetising particles to alter the internal representation of the external field prior to a navigation task. Although pulsing provoked deflected bearings in caged songbirds, analogous studies with free-flying songbirds yielded inconsistent results. Here, we pulsed European robins (Erithacus rubecula) at an offshore stopover site during spring migration and monitored their free-flight behaviour with a regional-scale network of radio-receiving stations. We found no pulse effect on departure probability, nocturnal departure timing departure direction or consistency of flight direction. This suggests either no use of the geomagnetic map by our birds, or that magnetic pulses do not affect the sensory system underlying geomagnetic map detection.

No apparent effect of a magnetic pulse on free-flight behaviour in northern wheatears (Oenanthe oenanthe) at a stopover site.

Naïve migrants reach their wintering grounds following a clock-and-compass strategy. During these inaugural migrations, birds internalise, among others, cues from the Earth's magnetic field to create a geomagnetic map, with which they navigate to destinations familiar to them on subsequent migrations. Geomagnetic map cues are thought to be sensed by a magnetic-particle-based receptor, which can be specifically affected by a magnetic pulse. Indeed, the orientation of experienced but not naïve birds was compromised after magnetic pulsing, indicating geomagnetic map use. Little is known about the importance of this putative magnetoreceptor for navigation and decision-making in free-flying migrants. Therefore, we studied in unprecedented detail how a magnetic pulse would affect departure probability, nocturnal departure timing, departure direction and consistency in flight direction over 50-100 km in experienced and naïve long-distant migrant songbirds using a large-scale radio-tracking system. Contrary to our expectations and despite a high sample size (ntotal = 137) for a free-flight study, we found no significant after-effect of the magnetic pulse on the migratory traits, suggesting the geomagnetic map is not essential for the intermediate autumn migration phase. These findings warrant re-thinking about perception and use of geomagnetic maps for migratory decisions within a sensory and ecological context.

Lifetime Observation of Cognition and Physiological Parameters in Male Mice.

Laboratory mice are predominantly used for one experiment only, i.e., new mice are ordered or bred for every new experiment. Moreover, most experiments use relatively young mice in the range of late adolescence to early adulthood. As a consequence, little is known about the day-to-day life of adult and aged laboratory mice. Here we present a long-term data set with three consecutive phases conducted with the same male mice over their lifetime in order to shed light on possible long-term effects of repeated cognitive stimulation. One third of the animals was trained by a variety of learning tasks conducted up to an age of 606 days. The mice were housed in four cages with 12 animals per cage; only four mice per cage had to repeatedly solve cognitive tasks for getting access to water using the IntelliCage system. In addition, these learner mice were tested in standard cognitive tests outside their home-cage. The other eight mice served as two control groups living in the same environment but without having to solve tasks for getting access to water. One control group was additionally placed on the test set-ups without having to learn the tasks. Next to the cognitive tasks, we took physiological measures (body mass, resting metabolic rate) and tested for dominance behavior, and attractivity in a female choice experiment. Overall, the mice were under surveillance until they died a natural death, providing a unique data set over the course of virtually their entire lives. Our data showed treatment differences during the first phase of our lifetime data set. Young learner mice showed a higher activity, less growth and resting metabolic rate, and were less attractive for female mice. These effects, however, were not preserved over the long-term. We also did not find differences in dominance or effects on longevity. However, we generated a unique and valuable set of long-term behavioral and physiological data from a single group of male mice and note that our long-term data contribute to a better understanding of the behavioral and physiological processes in male C57Bl/6J mice.

Are movements of daytime and nighttime passerine migrants as different as day and night?

Even after decades of research, the migration of songbirds still holds numerous secrets. Distinct stopover and routing behavior of diurnally and nocturnally migrating songbirds has been stated in the 1960s, but empirical confirmation is yet lacking widely. We studied the behavior of individual diurnally migrating dunnocks and nocturnally migrating blackcaps by means of large-scale automated radio-telemetry. Birds were radio-tagged during their stopover at the German North Sea coast. Our data indicate longer initial stopover duration in the diurnally migrating dunnocks, opposing the hypothesis of nocturnal migrants needing more time to recover due to their longer migratory flights. Nonetheless, dunnocks stopped over more often along their tracks as when compared to the nocturnally migrating blackcaps. Behavior en route did not differ as clearly between species challenging the general view of contrasting routings of diurnal and nocturnal migrants with regard to landscape and open water. Our results imply additional factors of relevance other than differences in species or daily migration timing per se. We discuss and highlight the need of detailed and individual based data to better understand stopover and routing behavior of songbirds in the environmental context.

To cross or not to cross - thrushes at the German North Sea coast adapt flight and routing to wind conditions in autumn.

BACKGROUND: Although many aspects of passerine migration are genetically determined, routing appears to be flexibly adjusted to the conditions experienced on each individual journey. This holds especially true for routing decisions taken when confronted with large bodies of water. Once taken, these decisions can be hardly altered or revised. In this paper, we analysed stopover and routing decisions taken by three species of thrushes, blackbirds, redwings and song thrushes, at the German North Sea coast. METHODS: Birds were equipped with radio-telemetry tags at stopover sites along the coast during autumn migration and subsequently tracked by an automated receiver network covering the coastline and islands of the German Bight. RESULTS: The thrushes resumed migration in nights with a favourable northward wind component and clear skies. About 40% of the tagged individuals have taken an offshore instead of an alongshore oriented flight route. Routing decisions were influenced by the strength of the eastward wind component with offshore oriented flights taking place primarily under weak winds or winds blowing towards the west. Thrushes that took an offshore oriented route stopped over at the coast longer than those flying alongshore. Interestingly, offshore as well as alongshore oriented flights co-occurred within single nights and under comparable weather conditions. CONCLUSIONS: Migratory flight and routing decisions of thrushes at the German North Sea coast are highly dependent on weather, in particular wind. Still, we found evidence that weather may not be the sole reason for individual routes taken. Physical condition, morphology or animal personality lend themselves as possible additional factors of influence. Enabling a more detailed understanding of thrush migration over and along the German North Sea, our data help to better judge risks that migratory birds are facing when en route conditions are altered, for example by artificial obstacles such as offshore wind turbines.

Stability of the guinea pigs personality - cognition - linkage over time.

In human psychological research, personality traits as well as cognitive traits are usually validated for both, their stability over time and contexts. While stability over time gives an estimate on how genetically fixated a trait can be, correlations across traits have the power to reveal linkages or trade - offs. In animals, these validations have widely been done for personality but not for cognitive traits. We tested guinea pigs in four consecutive discrimination tasks using four unique pairs of objects with two objects of the same form but different size in each pair. The same animals were tested twice each for three personality traits, i.e. boldness, aggression and sociopositive behaviour. The animals did not learn to "always choose the larger item" in the cognitive task but learned to discriminate the two objects of each stimulus pair anew, so that we did test for learning speed in four slightly different task setups. Performance over the four tasks was significantly repeatable as well as all tested personality traits. A stable linkage over time was found between sociopositive behaviour and learning performance, probably indicating an ecological relevance for a correlation between these two traits. Still, not all traits seem to be connected amongst each other, as in our case boldness and aggression are both not linked to individual learning performance. Future studies will hopefully further investigate the repeatability of various cognitive traits in several species and thus lead to a better understanding of the interdependence of personality and cognition. This will help to unravel which suites of traits facilitate individual life histories and hence improve our understanding of the emergence and maintenance of individual differences.

Determinants of between-year burrow re-occupation in a colony of the European bee-eater Merops apiaster.

Re-occupation of existing nesting burrows in the European bee-eater Merops apiaster has only rarely - and if so mostly anecdotically - been documented in the literature record, although such behavior would substantially save time and energy. In this study, we quantify burrow re-occupation in a German colony over a period of eleven years and identify ecological variables determining reuse probability. Of 179 recorded broods, 54% took place in a reused burrow and the overall probability that one of 75 individually recognized burrows would be reused in a given subsequent year was estimated as 26.4%. This indicates that between-year burrow reuse is a common behavior in the study colony which contrasts with findings from studies in other colonies. Furthermore, burrow re-occupation probability declined highly significantly with increasing age of the breeding wall. Statistical separation of within- and between-burrow effects of the age of the breeding wall revealed that a decline in re-occupation probability with individual burrow age was responsible for this and not a selective disappearance of burrows with high re-occupation probability over time. Limited duty cycles of individual burrows may be caused by accumulating detritus or decreasing stability with increasing burrow age. Alternatively, burrow fidelity may presuppose pair fidelity which may also explain the observed restricted burrow reuse duty cycles. A consequent next step would be to extend our within-colony approach to other colonies and compare the ecological circumstances under which bee-eaters reuse breeding burrows.

Lifetime development of behavioural phenotype in the house mouse (Mus musculus).

With each trajectory taken during the ontogeny of an individual, the number of optional behavioural phenotypes that can be expressed across its life span is reduced. The initial range of phenotypic plasticity is largely determined by the genetic material/composition of the gametes whereas interacting with the given environment shapes individuals to adapt to/cope with specific demands. In mammalian species, the phenotype is shaped as the foetus grows, depending on the environment in the uterus, which in turn depends on the outer environment the mother experiences during pregnancy. After birth, a complex interaction between innate constitution and environmental conditions shapes individual lifetime trajectories, bringing about a wide range of diversity among individual subjects. In laboratory mice inbreeding has been systematically induced in order to reduce the genetic variability between experimental subjects. In addition, within most laboratories conducting behavioural phenotyping with mice, breeding and housing conditions are highly standardised. Despite such standardisation efforts a considerable amount of variability persists in the behaviour of mice. There is good evidence that phenotypic variation is not merely random but might involve individual specific behavioural patterns consistent over time. In order to understand the mechanisms and the possible adaptive value of the maintenance of individuality we review the emergence of behavioural phenotypes over the course of the life of (laboratory) mice. We present a literature review summarizing developmental stages of behavioural development of mice along with three illustrative case studies. We conclude that the accumulation of environmental differences and experiences lead to a "mouse individuality" that becomes increasingly stable over the lifetime.

Domestication effects on behavioural traits and learning performance: comparing wild cavies to guinea pigs.

The domestication process leads to a change in behavioural traits, usually towards individuals that are less attentive to changes in their environment and less aggressive. Empirical evidence for a difference in cognitive performance, however, is scarce. Recently, a functional linkage between an individual's behaviour and cognitive performance has been proposed in the framework of animal personalities via a shared risk-reward trade-off. Following this assumption, bolder and more aggressive animals (usually the wild form) should learn faster. Differences in behaviour may arise during ontogeny due to individual experiences or represent adaptations that occurred over the course of evolution. Both might singly or taken together account for differences in cognitive performance between wild and domestic lineages. To test for such possible linkages, we compared wild cavies and domestic guinea pigs, both kept in a university stock for more than 30 years under highly comparable conditions. Animals were tested in three behavioural tests as well as for initial and reversal learning performance. Guinea pigs were less bold and aggressive than their wild congeners, but learnt an association faster. Additionally, the personality structure was altered during the domestication process. The most likely explanation for these findings is that a shift in behavioural traits and their connectivity led to an altered cognitive performance. A functional linkage between behavioural and cognitive traits seems to exist in the proposed way only under natural selection, but not in animals that have been selected artificially over centuries.

Lifelong consequences of early nutritional conditions on learning performance in zebra finches (Taeniopygia guttata).

Long-term effects of early developmental conditions on physiological and behavioural traits are common in animals. Yet, such lifelong effects of early life conditions on learning skills received relatively less attention, even though they are expected to have strong fitness effects. To test the lifelong impact of the early environment on associative and reversal learning performance, we tested zebra finches (Taeniopygia guttata) in a reversal learning task about five years after they were raised either under low or high quality food treatments in their first month of life. The early nutritional treatment and its respective growth patterns significantly influenced learning performance: Zebra finches who received a high-quality nutrition early in life gained more weight during the treatment period but needed more trials to associate a cue with a reward. The early growth rate during the treatment phase was linked to how fast the birds detected the food at the onset of training in our learning task as well as to their associative learning performance. However, in the reversal learning step of the task testing for behavioural flexibility, no differences with respect to early nutritional treatments or related growth rates were apparent. We show that early life conditions directly affect the approach to our task and learning abilities over an entire lifetime, emphasizing how crucial the early environment is for understanding adult behaviour throughout life.

Learning and personality types are related in cavies (Cavia aperea).

The evolution and maintenance of consistent individual differences, so called animal personalities, have attracted much research interest over the past decades. Variation along common personality traits, such as boldness or exploration, is often associated with risk-reward trade-offs. Individuals that are bolder and hence take more risks may be more successful in acquiring resources over the short term. Cautious individuals taking fewer risks may, on the other hand, live longer, but may also gather fewer resources over the short term. According to recent theory, individual differences in personality may be functionally related to individual differences in cognitive performance (i.e., the way in which individuals acquire or use information). Individual differences in the acquisition speed of cognitively challenging tasks are often associated with a speed-accuracy trade-off. Accuracy can be improved by investing more time in the decision-making process or, conversely, decisions can be made more quickly at the cost of making more mistakes. Hence, the speed-accuracy trade-off often involves a risk-reward trade-off. We tested whether 3 personality traits, boldness, activity, and aggressiveness, are correlated with individual learning, associative learning speed, and behavioral flexibility as assessed by reversal learning in wild cavies (Cavia aperea). We found strong positive relationships between all personality traits and learning speed, whereas flexibility was negatively associated with aggressiveness. Our results support the hypothesis that performance reflects individual differences in personality in a predictable way.