Animal learning as a source of developmental bias

Research supported in part by a grant from the John Templeton Foundation to K. N. L. (“Putting the extended evolutionary synthesis to the test”, ref 60501), by Japan Society for the Promotion of Science KAKENHI to W. T. (ref 17J01559), and a grant from the Netherlands Organization for Scientific Research to T. O. (ref 019.172EN.011).As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.PostprintPeer reviewe

Young birds switch but old birds lead : how barnacle geese adjust migratory habits to environmental change

This research was funded by a grant from the Netherlands Organization for Scientific Research awarded to TO (ref 019.172EN.011).Long-distance migratory animals must contend with global climate change, but they differ greatly in whether and how they adjust. Species that socially learn their migration routes may have an advantage in this process compared to other species, as learned changes that are passed on to the next generation can speed up adjustment. However, evidence from the wild that social learning helps migrants adjust to environmental change is absent. Here, we study the behavioral processes by which barnacle geese (Branta leucopsis) adjust spring-staging site choice along the Norwegian coast, which appears to be a response to climate change and population growth. We compared individual-based models to an empirical description of geese colonizing a new staging site in the 1990s. The data included 43 years of estimated annual food conditions and goose numbers at both staging sites (1975–2017), as well as annual age-dependent switching events between the two staging sites from one year to the next (2000–2017). Using Approximate Bayesian Computation, we assessed the relative likelihood of models with different “decision rules”, which define how individuals choose a staging site. In the best performing model, individuals traveled in groups and staging site choice was made by the oldest group member. Groups normally returned to the same staging site each year, but exhibited a higher probability of switching staging site in years with larger numbers of geese at the staging site. The decision did not depend on food availability in the current year. Switching rates between staging sites decreased with age, which was best explained by a higher probability of switching between groups by younger geese, and not by young geese being more responsive to current conditions. We found no evidence that the experienced foraging conditions in previous years affected staging site choice. Our findings demonstrate that copying behavior and density-dependent group decisions explain how geese adjust their migratory habits rapidly in response to changes in food availability and competition. We conclude that considering social processes can be essential to understand how migratory animals respond to changing environments.Publisher PDFPeer reviewe

The waterbirds of Parc National du Banc d’Arguin:Evaluation of all complete winter counts, workshop proceedings, and a future perspective

This is the report of an initiative to evaluate the results and methodology of all shorebird counts of the Banc d’Arguin in Mauritania. This was done by means of a workshop with all participants of the 2017 count expedition and a selection of researchers in the area, and an analysis of the 2017 census in the perspective of previous censuses. The goals of this initiative were (a) to gain more knowledge on the (causes of) temporal dynamics in the shorebird numbers at Banc d’Arguin, (b) to discuss the optimal design for future shorebird monitoring of the Banc d’Arguin, and (c) to improve the collaboration between all involved parties.Total bird numbers have been declining since the first complete census in 1980 (2,384,000 birds) with 1,725,000 birds counted in the 2017 census, a slightly higher total estimate than the previous census in 2014 (1,459,000 birds). All seven total censuses combined showed a significant temporal linear trend for six species (all negative, expect for one). For all other species, the data proved insufficient to determine temporal trends on the species level. An ordination analysis of all species per section suggests that species dependent on the intertidal mudflats decline more than species depending on the sublitoral and outer sea. Trends in population growth rates confirm this pattern.Discussions during and after the workshop led to a list of recommendations for future monitoring. To determine population trends, a complete count should be undertaken more frequently, by a trained Mauritanian team. Besides more data, this will lead to more experience and a better census. This is a preferred scenario, but it will take considerable investments, particularly in the installation of a permanent, skilled and motivated team of observers. Senior bird counters, trend analysis professionals, and a local guide should be involved to train this team. A course in count data analysis should be organised the Netherlands, and frequent training sessions should be organized in Mauritania, independent of the actual counts

Patterns of predation of Pink-footed Goose nests by polar bear

This study explored patterns of predation by polar bear Ursus maritimus on the nests of Pink-footed Geese Anser brachyrhynchus on the coastal tundra stretch Nordenskiöldkysten, west coast of Spitsbergen, Svalbard. Goose nests occurred in densities of up to 126 nests/km2 (mean=6.4), at an average distance of 1.5 km from the seashore, and were mainly associated with greenstone outcrops. Open, flat areas were avoided for nesting. Goose pairs nested in colonies of up to 23 nests, with 50% of the pairs nesting in colonies larger than 5. In 2011 and 2012, polar bears invaded the Pink-footed Goose nesting area to consume goose eggs, a behaviour that they had not exhibited in previous years. Polar bears selectively visited the taller outcrops and locations with the larger number of goose nests. Moreover there was a steep gradient in predation from the seashore towards the inland, with no predation at distances greater than 1.8 km from the coastline. We expect that the predation pressure by polar bears will aggravate in the coming years when more bears learn to exploit the inland goose colonies.This study explored patterns of predation by polar bear Ursus maritimus on the nests of Pink-footed Geese Anser brachyrhynchus on the coastal tundra stretch Nordenskiöldkysten, west coast of Spitsbergen, Svalbard. Goose nests occurred in densities of up to 126 nests/km2 (mean=6.4), at an average distance of 1.5 km from the seashore, and were mainly associated with greenstone outcrops. Open, flat areas were avoided for nesting. Goose pairs nested in colonies of up to 23 nests, with 50% of the pairs nesting in colonies larger than 5. In 2011 and 2012, polar bears invaded the Pink-footed Goose nesting area to consume goose eggs, a behaviour that they had not exhibited in previous years. Polar bears selectively visited the taller outcrops and locations with the larger number of goose nests. Moreover there was a steep gradient in predation from the seashore towards the inland, with no predation at distances greater than 1.8 km from the coastline. We expect that the predation pressure by polar bears will aggravate in the coming years when more bears learn to exploit the inland goose colonies

In this Issue

Aim: Molluscivorous shorebirds supposedly developed their present wintering distribution after the last ice age. Currently, molluscivorous shorebirds are abundant on almost all shores of the world, except for those in the Indo-West Pacific (IWP). Long before shorebirds arrived on the scene, molluscan prey in the IWP evolved strong anti-predation traits in a prolonged evolutionary arms race with durophagous predators including brachyuran crabs. Here, we investigate whether the absence of molluscivorous shorebirds from a site in Oman can be explained by the molluscan community being too well-defended. Location: The intertidal mudflats of Barr Al Hikman, Oman. Methods: Based on samples from 282 locations across the intertidal area the standing stock of the macrozoobenthic community was investigated. By measuring anti-predation traits (burrowing depth, size and strength of armour), the fraction of molluscs available to molluscivorous shorebirds was calculated. Results: Molluscs dominated the macrozoobenthic community at Barr Al Hikman. However, less than 17% of the total molluscan biomass was available to shorebirds. Most molluscs were unavailable either because of their hard-to-crush shells, or because they lived too deeply in the sediment. Repair scars and direct observations confirmed crab predation on molluscs. Although standing stock densities of the Barr Al Hikman molluscs were of the same order of magnitude as at intertidal mudflat areas where molluscivorous shorebirds are abundant, the molluscan biomass available to shorebirds was distinctly lower at Barr Al Hikman. Main conclusions: The established strong molluscan anti-predation traits against crabs precludes molluscan exploitation by shorebirds at Barr Al Hikman. This study exemplifies that dispersal of "novel" predators is hampered in areas where native predators and prey exhibit strongly developed attack and defence mechanisms, and highlights that evolutionary arms races can have consequences for the global distribution of species

Changes in the waterbird community of the Parc National du Banc d'Arguin, Mauritania, 1980-2017

The Parc National du Banc d’Arguin in Mauritania hosts the largest concentrations of coastal waterbirds along the East Atlantic Flyway. In spite of this importance, a review of the changes in the numbers of waterbirds in the area is lacking since the first complete count in 1980. Here we analysed the seven complete waterbird counts made since then, and the additional yearly counts made in one subunit (Iwik region) since 2003.We present evidence for changes in the community composition of waterbirds over the past four decades. Total waterbird numbers showed a decrease between 1980 and 2017, with only Great White Pelican Pelecanus onocrotalus showing a significantincrease in numbers. Five species showed significant declines: Long-tailed Cormorant Phalacrocorax africanus, Red Knot Calidris canutus, Bar-tailed Godwit Limosa lapponica, Eurasian Curlew Numenius arquata, and Western Marsh Harrier Circus aeruginosus. In the remaining species, the variation in numbers between counts was too large, and the number of complete counts too small, for trends to be detected. The yearly counts at Iwik region also showed sharp decreases in the numbers of Red Knot, Bar-tailed Godwit, and Marsh Harrier, but not of Long-tailed Cormorant and Eurasian Curlew. A multivariate analysis revealed a significant effect of year on species composition, which was caused mainly by changes in the species depending on the intertidal mudflats for feeding (generally in decline) vs. the species depending on fish and crustaceans in the sublittoral and offshore zones (often showing increases)

Digestive capacity and toxicity cause mixed diets in red knots that maximize energy intake rate

Among energy-maximizing animals, preferences for different prey can be explained by ranking the prey according to their energetic content. However, diet choice also depends on characteristics of the predator, such as the need to ingest necessary nutrients and the constraints imposed by digestion and toxins in food. In combination, these factors can lead to mixed diets in which the energetically most profitable food is not eaten exclusively even when it is abundant. We studied diet choice in red knots (Calidris canutus canutus) feeding on mollusks at a West African wintering site. At this site, the birds fed primarily on two species of bivalves, a thick-shelled one (Dosinia isocardia) that imposed a digestive constraint and a thin-shelled one (Loripes lucinalis) that imposed a toxin constraint. The latter species is toxic due to its symbiotic association with sulfide-oxidizing bacteria. We estimated experimentally the parameters of a linear programming model that includes both digestive and toxin constraints, leading to the prediction that red knots should eat a mixture of both mollusk species to maximize energy intake. The model correctly predicted the preferences of the captive birds, which depended on the digestive quality and toxicity of their previous diet. At our study site, energy-maximizing red knots appear to select a mixed diet as a result of the simultaneous effects of digestive and toxin constraints