Behavioural flexibility predicts invasion success in birds introduced to New Zealand

A fundamental question in ecology is whether there are evolutionary characteristics of species that make some better than others at invading new communities. In birds, nesting habits, sexually selected traits, migration, clutch size and body mass have been suggested as important variables, but behavioural flexibility is another obvious trait that has received little attention. Behavioural flexibility allows animals to respond more rapidly to environmental changes and can therefore be advantageous when invading novel habitats. Behavioural flexibility is linked to relative brain size and, for foraging, has been operationalised as the number of innovations per taxon reported in the short note sections of ornithology journals. Here, we use data on avian species introduced to New Zealand and test the link between forebrain size, feeding innovation frequency and invasion success. Relative brain size was, as expected, a significant predictor of introduction success, after removing the effect of introduction effort. Species with relatively larger brains tended to be better invaders than species with smaller ones. Introduction effort, migratory strategy and mode of juvenile development were also significant in the models. Pair-wise comparisons of closely related species indicate that successful invaders also showed a higher frequency of foraging innovations in their region of origin. This study provides the first evidence in vertebrates of a general set of traits, behavioural flexibility, that can potentially favour invasion success.     

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).     

Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds

The evolution of migration in birds remains an outstanding, unresolved question in evolutionary ecology. A particularly intriguing question is why individuals in some species have been selected to migrate, whereas in other species they have been selected to be sedentary. In this paper, we suggest that this diverging selection might partially result from differences among species in the behavioural flexibility of their responses to seasonal changes in the environment. This hypothesis is supported in a comparative analysis of Palaearctic passerines. First, resident species tend to rely more on innovative feeding behaviours in winter, when food is harder to find, than in other seasons. Second, species with larger brains, relative to their body size, and a higher propensity for innovative behaviours tend to be resident, while less flexible species tend to be migratory. Residence also appears to be less likely in species that occur in more northerly regions, exploit temporally available food sources, inhabit non-buffered habitats and have smaller bodies. Yet, the role of behavioural flexibility as a response to seasonal environments is largely independent of these other factors. Therefore, species with greater foraging flexibility seem to be able to cope with seasonal environments better, while less flexible species are forced to become migratory.     

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.     

Light enough to travel: migratory bats have smaller brains,but not larger hippocampi,than sedentary species

Migratory bird species have smaller brains than non-migratory species. The behavioural flexibility/migratory precursor hypothesis suggests that sedentary birds have larger brains to allow the behavioural flexibility required in a seasonally variable habitat. The energy trade-off hypothesis proposes that brains are heavy, energetically expensive and therefore, incompatible with migration. Here, we compared relative brain, neocortex and hippocampus volume between migratory and sedentary bats at the species-level and using phylogenetically independent contrasts. We found that migratory bats had relatively smaller brains and neocortices than sedentary species. Our results support the energy trade-off hypothesis because bats do not exhibit the same degree of flexibility in diet selection as sedentary birds. Our results also suggest that bat brain size differences are subtler than those found in birds, perhaps owing to bats'' shorter migration distances. Conversely, we found no difference in relative hippocampus volume between migratory and sedentary species, underscoring our limited understanding of the role of the hippocampus in bats.     

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.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.     

Brains, tools, innovation and biogeography in crows and ravens

ABSTRACT: BACKGROUND: Crows and ravens (Passeriformes: Corvus) are large-brained birds with enhanced cognitive abilities relative to other birds. They are among the few non-hominid organisms on Earth to be considered intelligent and well-known examples exist of several crow species having evolved innovative strategies and even use of tools in their search for food. The 40 Corvus species have also been successful dispersers and are distributed on most continents and in remote archipelagos. RESULTS: This study presents the first molecular phylogeny including all species and a number of subspecies within the genus Corvus. We date the phylogeny and determine ancestral areas to investigate historical biogeographical patterns of the crows. Additionally, we use data on brain size and a large database on innovative behaviour and tool use to test whether brain size (i) explains innovative behaviour and success in applying tools when foraging and (ii) has some correlative role in the success of colonization of islands. Our results demonstrate that crows originated in the Palaearctic in the Miocene from where they dispersed to North America and the Caribbean, Africa and Australasia. We find that relative brain size alone does not explain tool use, innovative feeding strategies and dispersal success within crows. CONCLUSIONS: Our study supports monophyly of the genus Corvus and further demonstrates the direction and timing of colonization from the area of origin in the Palaearctic to other continents and archipelagos. The Caribbean was probably colonized from North America, although some North American ancestor may have gone extinct, and the Pacific was colonized multiple times from Asia and Australia. We did not find a correlation between relative brain size, tool use, innovative feeding strategies and dispersal success. Hence, we propose that all crows and ravens have relatively large brains compared to other birds and thus the potential to be innovative if conditions and circumstances are right.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Tracking Changing Environments: Innovators Are Fast,but Not Flexible Learners

Behavioural innovations are increasingly thought to provide a rich source of phenotypic plasticity and evolutionary change. Innovation propensity shows substantial variation across avian taxa and provides an adaptive mechanism by which behaviour is flexibly adjusted to changing environmental conditions. Here, we tested for the first time the prediction that inter-individual variation in innovation propensity is equally a measure of behavioural flexibility. We used Indian mynas, Sturnus tristis, a highly successful worldwide invader. Results revealed that mynas that solved an extractive foraging task more quickly learnt to discriminate between a cue that predicted food, and one that did not more quickly. However, fast innovators were slower to change their behaviour when the significance of the food cues changed. This unexpected finding appears at odds with the well-established view that avian taxa with larger brains relative to their body size, and therefore greater neural processing power, are both faster, and more flexible learners. We speculate that the existence of this relationship across taxa can be reconciled with its absence within species by assuming that fast, innovative learners and non innovative, slow, flexible learners constitute two separate individual strategies, which are both underpinned by enhanced neural processing power. This idea is consistent with the recent proposal that individuals may differ consistently in ‘cognitive style’, differentially trading off speed against accuracy in cognitive tasks.     

Do smart birds stress less? An interspecific relationship between brain size and corticosterone levels

Vertebrates respond to unpredictable noxious environmental stimuli by increasing secretion of glucocorticoids (CORT). Although this hormonal stress response is adaptive, high levels of CORT may induce significant costs if stressful situations are frequent. Thus, alternative coping mechanisms that help buffer individuals against environmental stressors may be selected for when the costs of CORT levels are elevated. By allowing individuals to identify, anticipate and cope with the stressful circumstances, cognition may enable stress-specific behavioural coping. Although there is evidence that behavioural responses allow animals to cope with stressful situations, it is unclear whether or not cognition reduces investment in the neuroendocrine stress response. Here, we report that in birds, species with larger brains relative to their body size show lower baseline and peak CORT levels than species with smaller brains. This relationship is consistent across life-history stages, and cannot be accounted for by differences in life history and geographical latitude. Because a large brain is a major feature of birds that base their lifetime in learning new things, our results support the hypothesis that enhanced cognition represents a general alternative to the neuroendocrine stress response.     

Big-brained birds survive better in nature

Big brains are hypothesized to enhance survival of animals by facilitating flexible cognitive responses that buffer individuals against environmental stresses. Although this theory receives partial support from the finding that brain size limits the capacity of animals to behaviourally respond to environmental challenges, the hypothesis that large brains are associated with reduced mortality has never been empirically tested. Using extensive information on avian adult mortality from natural populations, we show here that species with larger brains, relative to their body size, experience lower mortality than species with smaller brains, supporting the general importance of the cognitive buffer hypothesis in the evolution of large brains.     

Long life evolves in large-brained bird lineages*

The brain is an energetically costly organ that consumes a disproportionate amount of resources. Species with larger brains relative to their body size have slower life histories, with reduced output per reproductive event and delayed development times that can be offset by increasing behavioral flexibility. The “cognitive buffer” hypothesis maintains that large brain size decreases extrinsic mortality due to greater behavioral flexibility, leading to a longer lifespan. Alternatively, slow life histories, and long lifespan can be a pre-adaptation for the evolution of larger brains. Here, we use phylogenetic path analysis to contrast different evolutionary scenarios and disentangle direct and indirect relationships between brain size, body size, life history, and longevity across 339 altricial and precocial bird species. Our results support both a direct causal link between brain size and lifespan, and an indirect effect via other life history traits. These results indicate that large brain size engenders longer life, as proposed by the “cognitive buffer” hypothesis.     

Differences in behavioural traits among native and introduced colonies of an invasive ant

Identifying the factors that promote the success of biological invasions is a key pursuit in ecology. To date, the link between animal personality and invasiveness has rarely been studied. Here, we examined in the laboratory how Argentine ant populations from the species’ native and introduced ranges differed in a suite of behaviours related to species interactions and the use of space. We found correlations among specific behavioural traits that defined an explorative-aggressive syndrome. The Main “European” supercolony (introduced range) more readily explored novel environments, displayed more aggression, detected food resources more quickly, and occupied more space than the Catalonian supercolony (introduced range) and two other Argentine supercolonies (native range). The two native supercolonies also differed in their personalities; one harbouring the less invasive personality, while the other is intermediate between the two introduced supercolonies. Therefore, instead of a binary pattern, Argentine ant supercolonies display a behavioural continuum that is independent on their geographic origin (native/introduced ranges). Our results also suggest that variability in personality traits is correlated to differences in the ecological success of Argentine ant colonies. Differences in group personalities may facilitate the persistence and invasion of animals under novel selective pressures by promoting adaptive behaviours. We stress that the concept of animal personality should be taken into account when elucidating the mechanisms of invasiveness.     

Gregariousness increases brain size in ungulates

The brain’s main function is to organise the physiological and behavioural responses to environmental and social challenges in order to keep the organism alive. Here, we studied the effects that gregariousness (as a measurement of sociality), dietary habits, gestation length and sex have on brain size of extant ungulates. The analysis controlled for the effects of phylogeny and for random variability implicit in the data set. We tested the following groups of hypotheses: (1) Social brain hypothesis—gregarious species are more likely to have larger brains than non-gregarious species because the former are subjected to demanding and complex social interactions; (2) Ecological hypothesis—dietary habits impose challenging cognitive tasks associated with finding and manipulating food (foraging strategy); (3) Developmental hypotheses (a) energy strategy: selection for larger brains operates, primarily, on maternal metabolic turnover (i.e. gestation length) in relation to food quality because the majority of the brain’s growth takes place in utero, and finally (b) sex hypothesis: females are expected to have larger brains than males, relative to body size, because of the differential growth rates of the soma and brain between the sexes. We found that, after adjusting for body mass, gregariousness and gestation length explained most of the variation in brain mass across the ungulate species studied. Larger species had larger brains; gregarious species and those with longer gestation lengths, relative to body mass, had larger brains than non-gregarious species and those with shorter gestation lengths. The effect of diet was negligible and subrogated by gestation length, and sex had no significant effect on brain size. The ultimate cause that could have triggered the co-evolution between gestation length and brain size remains unclear.     

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.     

Effects of seasonality on brain size evolution: evidence from strepsirrhine primates

Seasonal changes in energy supply impose energetic constraints that affect many physiological and behavioral characteristics of organisms. As brains are costly, we predict brain size to be relatively small in species that experience a higher degree of seasonality (expensive brain framework). Alternatively, it has been argued that larger brains give animals the behavioral flexibility to buffer the effects of habitat seasonality (cognitive buffer hypothesis). Here, we test these two hypotheses in a comparative study on strepsirrhine primates (African lorises and Malagasy lemurs) that experience widely varying degrees of seasonality. We found that experienced seasonality is negatively correlated with relative brain size in both groups, controlling for the effect of phylogenetic relationships and possible confounding variables such as the extent of folivory. However, relatively larger-brained lemur species tend to experience less variation in their dietary intake than indicated by the seasonality of their habitat. In conclusion, we found clear support for the hypothesis that seasonality restricts brain size in strepsirrhines as predicted by the expensive brain framework and weak support for the cognitive buffer hypothesis in lemurs.     

Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds

Brain size relative to body size is smaller in migratory than in nonmigratory birds. Two mutually nonexclusive hypotheses had been proposed to explain this association. On the one hand, the “energetic trade‐off hypothesis” claims that migratory species were selected to have smaller brains because of the interplay between neural tissue volume and migratory flight. On the other hand, the “behavioral flexibility hypothesis” argues that resident species are selected to have higher cognitive capacities, and therefore larger brains, to enable survival in harsh winters, or to deal with environmental seasonality. Here, I test the validity and setting of these two hypotheses using 1466 globally distributed bird species. First, I show that the negative association between migration distance and relative brain size is very robust across species and phylogeny. Second, I provide strong support for the energetic trade‐off hypothesis, by showing the validity of the trade‐off among long‐distance migratory species alone. Third, using resident and short‐distance migratory species, I demonstrate that environmental harshness is associated with enlarged relative brain size, therefore arguably better cognition. My study provides the strongest comparative support to date for both the energetic trade‐off and the behavioral flexibility hypotheses, and highlights that both mechanisms contribute to brain size evolution, but on different ends of the migratory spectrum.     

The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern?

The peak echolocation frequency of insectivorous bats generally declines as body size increases. However, there are notable exceptions to this rule, with some species, such as Rhinolophus clivosus, having a higher than expected peak frequency for their body size. Such deviations from allometry may be associated with partitioning of foraging habitat (the foraging habitat hypothesis) or insect prey (the prey detection hypothesis). Alternatively, the deviations may be associated with the partitioning of sonar frequency bands to allow effective communication in a social context (the acoustic communication hypothesis). We tested the predictions of these hypotheses through comparisons at the family, clade and species level, using species of rhinolophids in general and R. clivosus, a species with a wide distribution, as a specific test case. We compared the wing parameters, echolocation frequency and ecology of R. clivosus to those of the sympatric R. capensis. Rhinolophus clivosus has a much higher echolocation frequency than predicted from its wing loading or body mass. Furthermore, contrary to the predictions of the foraging habitat hypothesis, we found no difference in foraging habitat between R. clivosus and R. capensis. The size range of insect prey taken by the two species also overlapped almost completely, contrary to the prey detection hypothesis. On the other hand, the variation of echolocation frequencies around the allometric relationship for rhinolophids was smaller than that for Myotis spp., supporting the prediction of the acoustic communication hypothesis. We thus propose that the relatively high peak frequency of R. clivosus is the result of partitioning of sonar frequency bands to minimize the ambiguity of echolocation calls during social interactions.     

Large‐brained mammals live longer

Many mammals have brains substantially larger than expected for their body size, but the reasons for this remain ambiguous. Enlarged brains are metabolically expensive and require elongated developmental periods, and so natural selection should have favoured their evolution only if they provide counterbalancing advantages. One possible advantage is facilitating the construction of behavioural responses to unusual, novel or complex socio‐ecological challenges. This buffer effect should increase survival rates and favour a longer reproductive life, thereby compensating for the costs of delayed reproduction. Here, using a global database of 493 species, we provide evidence showing that mammals with enlarged brains (relative to their body size) live longer and have a longer reproductive lifespan. Our analysis supports and extends previous findings, accounting for the possible confounding effects of other life history traits, ecological and dietary factors, and phylogenetic autocorrelation. Thus, these findings provide support for the hypothesis that mammals counterbalance the costs of affording large brains with a longer reproductive life.