Behavioural flexibility and invasion success in birds

Behavioural flexibility has long been thought to provide advantages for animals when they invade novel environments. This hypothesis has recently received empirical support in a study of avian species introduced to New Zealand, but it remains to be determined whether behavioural flexibility is a general mechanism influencing invasion success. In this study, we examined introduction success of 69 bird species in different regions of the world as a function of their degree of behavioural flexibility. Specifically, we predicted that species with relatively large brains and a high frequency of foraging innovations in their area of origin should show a higher probability of establishing themselves where they were introduced than species with small brains and low innovation frequencies. An analysis with general linear modelling (GLM) supported the prediction for relative brain size, even when controlling for phylogenetic biases and potential confounding variables. The only covariates that remained with relative brain size were plumage dimorphism, human commensalism and nest site. A pairwise comparison of closely related species also revealed that successful invaders showed a higher frequency of foraging innovations in their region of origin. This result held even when differences in research effort between species were considered. Overall, the results confirm and generalize the hypothesis that behavioural flexibility is a major determinant of invasion success in birds.     

Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles

Brain size relative to body size varies considerably among animals, but the ecological consequences of that variation remain poorly understood. Plausibly, larger brains confer increased behavioural flexibility, and an ability to respond to novel challenges. In keeping with that hypothesis, successful invasive species of birds and mammals that flourish after translocation to a new area tend to have larger brains than do unsuccessful invaders. We found the same pattern in ectothermic terrestrial vertebrates. Brain size relative to body size was larger in species of amphibians and reptiles reported to be successful invaders, compared to species that failed to thrive after translocation to new sites. This pattern was found in six of seven global biogeographic realms; the exception (where relatively larger brains did not facilitate invasion success) was Australasia. Establishment success was also higher in amphibian and reptile families with larger relative brain sizes. Future work could usefully explore whether invasion success is differentially associated with enlargement of specific parts of the brain (as predicted by the functional role of the forebrain in promoting behavioural flexibility), or with a general size increase (suggesting that invasion success is facilitated by enhanced perceptual and motor skills, as well as cognitive ability).     

Implications of flexible foraging for interspecific interactions: lessons from simple models

1.  Some types of flexible foraging behaviours were incorporated into ecological thought in the 1960s, but the population dynamical consequences of such behaviours are still poorly understood.
2.  Flexible foraging-related traits can be classified as shifts in general and specific foraging effort, and shifts in general and specific defense.
3.  Many flexible foraging behaviours suggested by theory have received very little empirical attention, and empirical techniques used to compare the magnitudes of behavioural and non-behavioural responses to predation are likely to have overestimated the behavioural components.
4.  Adaptively flexible foraging in theory causes significant changes in the forms of consumer functional responses and generates a variety of indirect interactions. These can alter fundamental ecological processes, such as co-existence of competitors, and top-down or bottom-up effects in food webs.
5.  Many aspects of flexible foraging are still largely unknown, including the issues of how to represent the dynamics of such phenotypically plastic traits, how flexible traits in multiple species interact, what types of adaptive movements occur in metacommunities, and how adaptive behaviours influence evolutionary change.
6.  Population dynamics in large food webs may be less dependent on behavioural flexibility than in small webs because species replacement may preempt some potential types of behavioural change within species.     

Coevolving avian eye size and brain size in relation to prey capture and nocturnality

Behavioural adaptation to ecological conditions can lead to brain size evolution. Structures involved in behavioural visual information processing are expected to coevolve with enlargement of the brain. Because birds are mainly vision-oriented animals, we tested the predictions that adaptation to different foraging constraints can result in eye size evolution, and that species with large eyes have evolved large brains to cope with the increased amount of visual input. Using a comparative approach, we investigated the relationship between eye size and brain size, and the effect of prey capture technique and nocturnality on these traits. After controlling for allometric effects, there was a significant, positive correlation between relative brain size and relative eye size. Variation in relative eye and brain size were significantly and positively related to prey capture technique and nocturnality when a potentially confounding variable, aquatic feeding, was controlled statistically in multiple regression of independent linear contrasts. Applying a less robust, brunching approach, these patterns also emerged, with the exception that relative brain size did not vary with prey capture technique. Our findings suggest that relative eye size and brain size have coevolved in birds in response to nocturnal activity and, at least partly, to capture of mobile prey.     

Social bonds in birds are associated with brain size and contingent on the correlated evolution of life‐history and increased parental investment

In birds, large brains are associated with a series of population‐level phenomena, including invasion success, species richness, and resilience to population decline. Thus, they appear to open up adaptive opportunities through flexibility in foraging and anti‐predator behaviour. The evolutionary pathway leading to large brain size has received less attention than behavioural and ecological correlates. Using a comparative approach, we show that, independent of previously recognized associations with developmental constraints, relative brain size in birds is strongly related to biparental care, pair‐bonding, and stable social relationships. We also demonstrate correlated evolution between large relative brain size and altricial development, and that the evolution of both traits is contingent on biparental care. Thus, biparental care facilitates altricial development, which permits the evolution of large relative brain size. Finally, we show that large relative brain size is associated with pair‐bond strength, itself a likely consequence of cooperation and negotiation between partners under high levels of parental investment. These analyses provide an evolutionary model for the evolution of and prevalence of biparental care, altricial development, and pair‐bonding in birds. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 111–123.     

Infectious disease,behavioural flexibility and the evolution of culture in primates

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.     

Living in the city: can anyone become an ‘urban exploiter'?

Aim As urban landscapes expand, shifts in biodiversity are occurring. This is leading biogeographers and ecologists to consider human‐dominated landscapes in their current work. One question that arises is: what characterizes those species that are widespread in the most highly urban environments compared with those restricted to less urbanized areas in the city? Here, we aim to identify the traits that enable species to become urban exploiters, i.e. to dominate highly urbanized surroundings. Identifying these traits may help us better predict and possibly mitigate the biotic homogenization occurring in these areas. Location Israel in general, with special focus on the city of Jerusalem. Methods Combining literature and field‐based data for birds in Israel we compared phenotypic, behavioural and life‐history traits between urban exploiters and urban adapters. The latter occur in urban landscapes, but are characteristic of the less urbanized parts of the city. We then examined the trends along a finer field‐sampled gradient of increasing urbanization from sub‐natural to downtown areas within the city of Jerusalem. Results Urban exploiters and adapters differed primarily in social structure and migratory status: exploiters were significantly more social and sedentary than urban adapters. Clear trends were also seen for dietary preferences along a gradient of increasing urbanization in Jerusalem, such that, with increasing urbanization, the proportion of granivorous species increased whereas the proportion of species feeding on invertebrates declined. In contrast, neither relative brain size nor behavioural flexibility, as measured by feeding innovations, differed significantly among urban exploiters and adapters in Israel or along the urbanization gradient in Jerusalem specifically. Main conclusions The results of our study suggest that being successful in more vs. less urbanized environments in the city is not necessarily a factor of brain size nor of how flexible and behaviourally innovative the species is; rather, it depends on a combination of traits, including diet, degree of sociality, sedentariness and preferred nesting sites.     

The role of competition and introduction effort in the success of passeriform birds introduced to New Zealand

Abstract The finding that passeriform birds introduced to the islands of Hawaii and Saint Helena were more likely to successfully invade when fewer other introduced species were present has been interpreted as strong support for the hypothesis that interspecific competition influences invasion success. I tested whether invasions were more likely to succeed when fewer species were present using the records of passeriform birds introduced to four acclimatization districts in New Zealand. I also tested whether introduction effort, measured as the number of introductions and the total number of birds released, could predict invasion outcomes, a result previously established for all birds introduced to New Zealand. I found patterns consistent with both competition and introduction effort as explanations for invasion success. However, data supporting the two explanations were confounded such that the greater success of invaders arriving when fewer other species were present could have been due to a causal relationship between invasion success and introduction effort. Hence, without data on introduction effort, previous studies may have overestimated the degree to which the number of potential competitors could independently explain invasion outcomes and may therefore have overstated the importance of competition in structuring introduced avian assemblages. Furthermore, I suggest that a second pattern in avian invasion success previously attributed to competition, the morphological overdispersion of successful invaders, could also arise as an artifact of variation in introduction effort.     

Feeding innovations and parasitism in birds

The rate of behavioural innovation, such as opportunistic feeding innovation, may facilitate adaptation to novel environments. Because parasites may affect how their hosts adopt novel means of resource acquisition, or because opportunistic behaviours may involve the risk of being exposed to a large parasite fauna, we hypothesize an evolutionary link between the rate of feeding innovations and parasitism. We investigated the phylogenetic relationship between relative frequency of feeding innovations (adjusted for research effort and population size) and relative size of immune defense organs (as a relative measure of parasite-mediated selection) and the prevalence of blood parasites in birds. Using generalized least squares models, we found that species with relatively large bursa of Fabricius, thymus, and spleen had higher rates of feeding innovations than species with small immune defense organs. Similarly, there was a positive interspecific association between feeding innovation and haematozoa prevalence. These relationships were not confounded by migration, relative brain size, geographical distribution, and male plumage brightness. Analyses of causality relying on evolutionary modelling of discrete variables and path analysis suggest that increasing rate of feeding innovation may place species under intense selection due to parasitism. Therefore, behavioural adaptation by feeding innovation seems to have consequences for the coevolutionary arm race between parasites and hosts.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 441–455.     

Brain size predicts the success of mammal species introduced into novel environments

Large brains, relative to body size, can confer advantages to individuals in the form of behavioral flexibility. Such enhanced behavioral flexibility is predicted to carry fitness benefits to individuals facing novel or altered environmental conditions, a theory known as the brain size-environmental change hypothesis. Here, we provide the first empirical link between brain size and survival in novel environments in mammals, the largest-brained animals on Earth. Using a global database documenting the outcome of more than 400 introduction events, we show that mammal species with larger brains, relative to their body mass, tend to be more successful than species with smaller brains at establishing themselves when introduced to novel environments, when both taxonomic and regional autocorrelations are accounted for. This finding is robust to the effect of other factors known to influence establishment success, including introduction effort and habitat generalism. Our results replicate similar findings in birds, increasing the generality of evidence for the idea that enlarged brains can provide a survival advantage in novel environments.     

Determinants of the geographical extent of invasive plants in China: effects of biogeographical origin,life cycle and time since introduction

Plant invasions cause serious impacts to environment and human economy, and lots of researches have been paid to examine factors that determine the geographical extent of plant invaders. Many intrinsic species attributes, external environmental factors, and time since introduction have all been proposed to explain invasive success. Data on invasive plants distribution in province regions in China were collected, and species attributes and historical factors such as biogeographical origin, life cycle, and time since introduction were determined. While some annuals may eventually occupy the whole country area, perennials are unlikely to do so, particularly those from Central and South America. Time since introduction is significantly related to the number of provinces occupied by an invader; nevertheless after control of certain residence time, annuals are not likely to more provinces than the perennial herbs. High-impact invaders tend to spread faster than other invaders, but only when their life cycle is taken into account. This suggests that other plant traits, instead of life cycle, along with extrinsic factors, greatly contribute to invasive success and distribution area. Invasive plants in China are mainly distributed in human-made habitats, and their long-distance dispersal is primarily associated with human activities. Future studies need to consider interactions between species traits, environmental conditions, and human activities for further insights in researches alike.     

Carbohydrate scarcity increases foraging activities and aggressiveness in the ant Prolasius advenus (Hymenoptera: Formicidae)

1. Behavioural responses to varying macronutrient availability are increasingly studied in highly invasive ant species to better understand their ecological success. However, such work is lacking in relation to native ant species confronted with biological invaders. 2. Here the link between diet and behaviour was examined in Prolasius advenus, a native ant from New Zealand facing intense competition for food with invasive insects, including social wasps. A long‐term laboratory experiment was conducted to assess the impact of protein and carbohydrate restriction on several behavioural parameters. 3. Ants shifted their food‐collecting activity towards the least available macronutrient in both protein‐limited and carbohydrate‐limited colonies. But when lacking carbohydrate, they also strongly increased their efforts to discover resources. After 10 weeks, the proportion of the colony patrolling outside of the nest was eight times higher than at the initiation of the experiment. This high patrolling activity was then maintained for several weeks and resulted in a higher efficiency to explore a novel territory. Moreover, ants fed a carbohydrate‐limited diet engaged in longer aggressive acts towards conspecifics. 4. These behavioural responses to carbohydrate scarcity may, in part, enhance the ability of P. advenus to resist a competing invader under natural conditions. While much of the previous research has linked diet and behavioural dominance in invasive ants, the present study shows that conducting similar investigations in the native species to which they are confronted may shed light on the mechanisms behind biotic resistance and the ability of some native species to coexist with highly abundant invaders.     

Regional differences in foraging behaviour of invasive green crab (<Emphasis Type="Italic">Carcinus maenas</Emphasis>) populations in Atlantic Canada

Invasive green crab populations initially established in Canada within the Bay of Fundy, New Brunswick in the 1950s and were present in all five Atlantic provinces by 2007. Genetic evidence suggests that the Atlantic Canadian populations originated from two separate introductions with differences in time of establishment among regions and possible population-level behavioural differences. In this study, we examine intraspecific foraging behaviour among crabs from different populations, and interspecific foraging behaviour between genetically similar crabs and juvenile lobsters. Both sets of foraging experiments involved competition for a limited food source over a 1-h period. In intraspecific match-ups, recent invaders from Newfoundland (NL) were significantly superior foragers than long-established invaders from Nova Scotia (NS) and New Brunswick (NB) populations; however, we found no differences between NL and Prince Edward Island (PE) invaders. Crabs from PE were better competitors than those from NS and NB, but these differences were not significant. Interspecific competition experiments indicated that the feeding behaviour of recent invaders (NL) and genetically similar, but long-established invaders (NS), differed in the presence of juvenile lobsters. Our study documents striking behavioural differences among populations of green crab from a small geographic region, which may reflect a combination of both genetic differences and time since establishment. These differences may result in varying impacts on newly invaded habitats.     

Propagule size and the relative success of exotic ungulate and bird introductions to New Zealand

We investigated factors affecting the success of 14 species of ungulates introduced to New Zealand around 1851-1926. The 11 successful species had a shorter maximum life span and were introduced in greater numbers than the three unsuccessful species. Because introduction effort was confounded with other life-history traits, we examined whether independent introductions of the same species were more likely to succeed when a greater number of individuals were introduced. For the six species with introductions that both succeeded and failed, successful introductions always involved an equal or greater number of individuals than unsuccessful introductions of the same species. For all independent introductions, there was a highly significant relationship between the number of individuals introduced and introduction success. When data for ungulate and bird introductions to New Zealand were combined, a variable categorizing species as ungulate or bird was a highly significant predictor of introduction success, after variation in introduction effort was controlled. For a given number of individuals introduced, ungulates were much more likely to succeed than birds.     

Brain size and resource specialization predict long-term population trends in British birds

Large-scale population declines have been documented across many faunal assemblages. However, there is much variation in population trends for individual species, and few indications of which specific ecological and behavioural characteristics are associated with such trends. We used the British Common Birds Census (1968-1995) to identify specific traits associated with long-term abundance trends in UK farmland birds. Two factors, resource specialization and relative brain size, were significantly associated with population trend, such that species using atypical resources and with relatively small brains were most likely to have experienced overall declines. Further analyses of specific brain components indicated that the relative size of the telencephalon, the part of the brain associated with problem solving and complex behaviours, and the brain stem might be better predictors of population trend than overall brain size. These results suggest that flexibility in resource use and behaviour are the most important characteristics for determining a species' ability to cope with large-scale habitat changes.     

Clever birds are lousy: co-variation between avian innovation and the taxonomic richness of their amblyceran lice

Lice (Insecta: Phthiraptera) are ectoparasites that reduce host life expectancy and sexual attractiveness. Their taxonomic richness varies considerably among their hosts. Previous studies have already explored some important factors shaping louse diversity. An unexplored potential correlate of louse taxonomic richness is host behavioural flexibility. In this comparative study, we examine the relationship between louse generic richness, innovative capabilities (as a proxy for behavioural flexibility), and brain size while controlling for host species diversity, phylogeny, body size and research effort. Using data for 108 avian families, we found a highly significant positive relationship between host innovative capabilities and the taxonomic richness of amblyceran lice, but a lack of a similar relationship in ischnoceran lice. Host brain size had only a marginal impact on amblyceran diversity and no correlation with ischnoceran diversity. This suggests that the effect in Amblycera is not mediated by metabolic limitations due to the energetic costs of brain size and maintenance, rather directly caused by the ecological differences between hosts with differing cognitive capabilities. We propose four alternative and mutually non-exclusive hypotheses that may explain this phenomenon.     

Behavioural plasticity in a native species may be related to foraging resilience in the presence of an aggressive invader

Competition between invasive and native species can result in the exploitation of resources by the invader, reducing foraging rates of natives. However, it is increasingly recognized that multiple factors can enhance the resilience of native species competing for limiting resources with invaders. Although extensively studied in terrestrial species, little research has focused on behavioural plasticity in aquatic ecosystems and how this influences native species resilience. Here, we examined the role of behavioural plasticity in interactions between a native Australian fish, Pseudomugil signifer, and a widespread invasive fish, Gambusia holbrooki. To determine whether P. signifer displays behavioural plasticity that may mitigate competition with G. holbrooki, we first quantified social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups. Second, we compared the feeding rates of both species in these groups to ascertain if any modulation of social behaviours and cohesion related to foraging success. We found that aggressive and submissive behaviours of G. holbrooki and P. signifer showed plasticity in the presence of heterospecifics, but social affiliation, shoaling and, most importantly, foraging, remained inflexible. This variation in the degree of plasticity highlights the complexity of the behavioural response of a native species and suggests that both behavioural modulation and consistency may be related to sustaining foraging efficiency in the presence of an invader.     

Coping styles and behavioural flexibility: towards underlying mechanisms

A coping style (also termed behavioural syndrome or personality) is defined as a correlated set of individual behavioural and physiological characteristics that is consistent over time and across situations. This relatively stable trait is a fundamental and adaptively significant phenomenon in the biology of a broad range of species, i.e. it confers differential fitness consequences under divergent environmental conditions. Behavioural flexibility appears to be an important underlying attribute or feature of the coping style that might explain consistency across situations. Proactive coping is characterized by low flexibility expressed as rather rigid, routine-like behavioural tendencies and reduced impulse control (behavioural inhibition) in operant conditioning paradigms. This article summarizes some of the evidence that individual differentiation in behavioural flexibility emerges as a function of underlying variability in the activation of a brain circuitry that includes the prefrontal cortex and its key neurochemical signalling pathways (e.g. dopaminergic and serotonergic input). We argue that the multidimensional nature of animal personality and the terminology used for the various dimensions should reflect the differential pattern of activation of the underlying neuronal network and the behavioural control function of its components. Accordingly, unravelling the molecular mechanisms that give rise to individual differences in the coping style will be an important topic in biobehavioural neurosciences, ecology and evolutionary biology.     

Relationship between spatial working memory performance and diet specialization in two sympatric nectar bats

Behavioural ecologists increasingly recognise spatial memory as one the most influential cognitive traits involved in evolutionary processes. In particular, spatial working memory (SWM), i.e. the ability of animals to store temporarily useful information for current foraging tasks, determines the foraging efficiency of individuals. As a consequence, SWM also has the potential to influence competitive abilities and to affect patterns of sympatric occurrence among closely related species. The present study aims at comparing the efficiency of SWM between generalist (Glossophaga soricina) and specialist (Leptonycteris yerbabuenae) nectarivorous bats at flowering patches. The two species differ in diet--the generalist diet including seasonally fruits and insects with nectar and pollen while the specialist diet is dominated by nectar and pollen yearlong--and in some morphological traits--the specialist being heavier and with proportionally longer rostrum than the generalist. These bats are found sympatrically within part of their range in the Neotropics. We habituated captive individuals to feed on artificial flower patches and we used infrared video recordings to monitor their ability to remember and avoid the spatial location of flowers they emptied in previous visits in the course of 15-min foraging sequences. Experiments revealed that both species rely on SWM as their foraging success attained significantly greater values than random expectations. However, the nectar specialist L. yerbabuenae was significantly more efficient at extracting nectar (+28% in foraging success), and sustained longer foraging bouts (+27% in length of efficient foraging sequences) than the generalist G. soricina. These contrasting SWM performances are discussed in relation to diet specialization and other life history traits.     

Inter-individual variability in fear of humans and relative brain size of the species are related to contemporary urban invasion in birds

Background

Urbanization is the most prevailing cause of habitat transformation worldwide, differing from others by its intense levels of human activity. Despite its obvious impact on wildlife, it is still unclear why and how some species are able to adapt to urban settings. One possibility is that fear of humans and vehicles could preclude most species from invading cities. Species entering urban environments might be those that are more tolerant of human disturbance (i.e., tame species). Alternatively or in addition, urban invaders could be a fraction of variable species, with “tame” individuals invading urban habitats and other individuals remaining in rural areas.

Methodology

Using the contemporary urban invasion by birds in a recently established South American city, we tested both hypotheses by relating interspecific differences in invasiveness to their flight initiation distances (i.e., the distances at which birds flee from approaching cars, FID), as well as to their relative brain size (RBS), a correlate of measures of behavioral flexibility.

Principal Findings

Urban invasiveness was not significantly related to species'' average rural FIDs but positively related to their RBS and inter-individual variability in FID. Moreover, FIDs were consistently lower in urban than in rural conspecifics, and the FIDs of urban individuals were within the lower-range distribution of their rural conspecifics. RBS indirectly influenced urban invasion through its positive effect on inter-individual variability in FID.

Conclusions/Significance

Urban invaders do not appear to be individuals from apparently tame species, but rather tame individuals from species with a variable response regarding fear of people. Given the positive relationship between RBS and inter-individual variability in FID, our results suggest that behavioural flexibility should be regarded as a specific trait encompassing variability among individuals. Further research is needed to ascertain the neurophysiological mechanisms underlying the relationship between brain size and inter-individual variability in behavioural traits.