How to solve novel problems: the role of associative learning in problem-solving performance in wild great tits Parus major.

Although problem-solving tasks are frequently used to assess innovative ability, the extent to which problem-solving performance reflects variation in cognitive skills has been rarely formally investigated. Using wild breeding great tits facing a new non-food motivated problem-solving task, we investigated the role of associative learning in finding the solution, compared to multiple other non-cognitive factors. We first examined the role of accuracy (the proportion of contacts made with the opening part of a string-pulling task), neophobia, exploration, activity, age, sex, body condition and participation time on the ability to solve the task. To highlight the effect of associative learning, we then compared accuracy between solvers and non-solvers, before and after the first cue to the solution (i.e., the first time they pulled the string opening the door). We finally compared accuracy over consecutive entrances for solvers. Using 884 observations from 788 great tits tested from 2010 to 2015, we showed that, prior to initial successful entrance, solvers were more accurate and more explorative than non-solvers, and that females were more likely to solve the task than males. The accuracy of solvers, but not of non-solvers, increased significantly after they had the opportunity to associate string pulling with the movement of the door, giving them a first cue to the task solution. The accuracy of solvers also increased over successive entrances. Our results demonstrate that variations in problem-solving performance primarily reflect inherent individual differences in associative learning, and are also to a lesser extent shaped by sex and exploratory behaviour.

Host dispersal shapes the population structure of a tick-borne bacterial pathogen.

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick-borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies "Candidatus Borrelia aligera" was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick-borne pathogens are shaped by their host associations and the movement patterns of these hosts.

Divergence in problem-solving skills is associated with differential expression of glutamate receptors in wild finches.

Problem solving and innovation are key components of intelligence. We compare wild-caught individuals from two species that are close relatives of Darwin's finches, the innovative Loxigilla barbadensis, and its most closely related species in Barbados, the conservative Tiaris bicolor. We found an all-or-none difference in the problem-solving capacity of the two species. Brain RNA sequencing analyses revealed interspecific differences in genes related to neuronal and synaptic plasticity in the intrapallial neural populations (mesopallium and nidopallium), especially in the nidopallium caudolaterale, a structure functionally analogous to the mammalian prefrontal cortex. At a finer scale, we discovered robust differences in glutamate receptor expression between the species. In particular, the GRIN2B/GRIN2A ratio, known to correlate with synaptic plasticity, was higher in the innovative L. barbadensis. These findings suggest that divergence in avian intelligence is associated with similar neuronal mechanisms to that of mammals, including humans.

Effect of an anti-malaria drug on behavioural performance on a problem-solving task: an experiment in wild great tits.

Malaria parasites have been shown to decrease host fitness in several species in the wild and their detrimental effects on host cognitive ability are well established in humans. However, experimental demonstrations of detrimental effects on non-human host behaviour are currently limited. In this study, we experimentally tested whether injections of an anti-malaria drug affected short-term behavioural responses to a problem-solving task during breeding in a wild population of great tits (Parus major) naturally infected with malaria. Adult females treated against malaria were more active than control females, even though they were not more likely to solve the task or learn how to do so, suggesting that energetic constraints could shape differences in some behaviours while changes in cognitive performances might require more time for the neural system to recover or may depend mainly on infection at the developmental stage. Alternatively, parasite load might be a consequence, rather than a cause, of inter-individual variation in cognitive performance. These results also suggest that inter-individual as well as inter-population differences in some behavioural traits may be linked to blood parasite load.

Selective disappearance of individuals with high levels of glycated haemoglobin in a free-living bird.

Although disruption of glucose homeostasis is a hallmark of ageing in humans and laboratory model organisms, we have little information on the importance of this process in free-living animals. Poor control of blood glucose levels leads to irreversible protein glycation. Hence, levels of protein glycation are hypothesized to increase with age and to be associated with a decline in survival. We tested these predictions by measuring blood glycated haemoglobin in 274 adult collared flycatchers of known age and estimating individual probability of recapture in the following 2 years. Results show a strong decrease in glycated haemoglobin from age 1 to 5 years and an increase thereafter. Individuals with high levels of glycated haemoglobin had a lower probability of recapture, even after controlling for effects of age and dispersal. Altogether, our findings suggest that poor control of glucose homoeostasis is associated with lower survival in this free-living bird population, and that the selective disappearance of individuals with the highest glycation levels could account for the counterintuitive age-related decline in glycated haemoglobin in the early age categories.

Innovative foraging behaviour in birds: what characterizes an innovator?

Innovative foraging behaviour has been observed in many species, but little is known about how novel behaviour emerges or why individuals differ in their propensity to innovate. Here, we investigate these questions by presenting 36 wild-caught adult male Carib grackles (Quiscalus lugubris) with a novel problem-solving task. Twenty birds solved the task ("innovators") while 16 did not ("non-innovators"). We compared innovators to non-innovators and explored variation in latency to innovate to determine the characteristics of an innovative bird. Innovativeness was not predicted by any morphological trait, but innovators had higher exploration scores and lower object neophobia scores than non-innovators. Within the innovators, latency to innovate was positively correlated with learning speed. Video analysis also revealed a marked difference in the way individuals interacted with the novel apparatus: when innovators contacted the correct part of the apparatus, they continued to do so until they solved the problem. Non-innovators often contacted the correct part of the apparatus, but did not persist in doing so. The importance of obstacle movement cues was confirmed by an experiment where they were manipulated.