Explanations for variation in cognitive ability : behavioural ecology meets comparative cognition

Sara Shettleworth has played a defining role in the development of animal cognition and its integration into other parts of biology, especially behavioural ecology. Here we chart some of that progress in understanding the causes and importance of variation in cognitive ability and highlight how Tinbergen's levels of explanation provide a useful framework for this field. We also review how experimental design is crucial in investigating cognition and stress the need for naturalistic experiments and field studies. We focus particularly on the example of the relationship among food hoarding, spatial cognition and hippocampal structure, and review the conflicting evidence for sex differences in spatial cognition. We finish with speculation that a combination of Tinbergen and Shettleworth-style approaches would be the way to grapple with the as-yet unanswered questions of why birds mimic heterospecifics.

The personality behind cheating: behavioural types and the feeding ecology of cleaner fish

The complex mutualistic relationship between the cleaner fish (Labroides dimidiatus) and their 'clients' in many reef systems throughout the world has been the subject of debate and research interest for decades. Game-theory models have long struggled with explaining how the mixed strategies of cheating and honesty might have evolved in such a system and while significant efforts have been made theoretically, demonstrating the nature of this relationship empirically remains an important research challenge. Using the experimental framework of behavioural syndromes, we sought to quantitatively assess the relationship between personality and the feeding ecology of cleaner fish to provide novel insights into the underlying mechanistic basis of cheating in cleaner-client interactions. First, we observed and filmed cleaner fish interactions with heterospecifics, movement patterns and general feeding ecology in the wild. We then captured and measured all focal individuals and tested them for individual consistency in measures of activity, exploration and risk taking (boldness) in the laboratory. Our results suggest a syndrome incorporating aspects of personality and foraging effort are central components of the behavioural ecology of L. dimidiatus on the Great Barrier Reef. We found that individuals that exhibited greater feeding effort tended to cheat proportionately less and move over smaller distances relative to bolder more active, exploratory individuals. Our study demonstrates for the first time that individual differences in personality might be mechanistically involved in explaining how the mixed strategies of cheating and honesty persist in cleaner fish mutualisms.

Multiple mating and a low incidence of cuckoldry for nest-holding males in the two-spotted goby, Gobiusculus flavescens

Background: A major question in behavioural ecology concerns the relationship between genetic mating systems and the strength of sexual selection. In this study, we investigated the genetic mating system of the two-spotted goby (Gobiusculus flavescens), a useful fish model for the study of sexual selection whose genetic mating system remains uncharacterized. We developed four polymorphic microsatellite markers and used them to conduct parentage analyses on 21 nests collected during the breeding season to examine the rates of multiple mating by males and to test for evidence of alternative mating strategies.

Results: Results of this study indicate that male G. flavescens mate with multiple females and enjoy confidence of paternity. We detected only one instance of sneaking, so cuckoldry contributed a very small percentage (~0.1%) of the total fertilizations in this population. Nests were nearly full and males that maintain larger nests have higher mating and reproductive success, irrespective of body size.

Conclusion: Overall, our investigation shows that G. flavescens is similar to other, related gobies in that the nests of care-giving males often contain eggs from multiple females. However, G. flavescens differs from other gobies in displaying an extremely low rate of cuckoldry. The study of ecological factors responsible for this important

Building genetic networks using relatedness information : a novel approach for the estimation of dispersal and characterization of group structure in social animals

Natal dispersal is an important life history trait driving variation in individual fitness, and therefore, a proper understanding of the factors underlying dispersal behaviour is critical to many fields including population dynamics, behavioural ecology and conservation biology. However, individual dispersal patterns remain difficult to quantify despite many years of research using direct and indirect methods. Here, we quantify dispersal in a single intensively studied population of the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps) using genetic networks created from the combination of pairwise relatedness data and social networking methods and compare this to dispersal estimates from re-sighting data. This novel approach not only identifies movements between social groups within our study sites but also provides an estimation of immigration rates of individuals originating outside the study site. Both genetic and re-sighting data indicated that dispersal was strongly female biased, but the magnitude of dispersal estimates was much greater using genetic data. This suggests that many previous studies relying on mark–recapture data may have significantly underestimated dispersal. An analysis of spatial genetic structure within the sampled population also supports the idea that females are more dispersive, with females having no structure beyond the bounds of their own social group, while male genetic structure expands for 750 m from their social group. Although the genetic network approach we have used is an excellent tool for visualizing the social and genetic microstructure of social animals and identifying dispersers, our results also indicate the importance of applying them in parallel with behavioural and life history data.

Editorial : Q & A John A. Endler

John A. Endler is a Professor of Sensory Ecology and Evolution at Deakin University and an Adjunct professor of Zoology at James Cook University, both in Australia. He regards himself as a 19th century natural historian who uses 21st century techniques to answer questions generated originally from field observations. His research is in the area of overlap among Evolutionary Biology, Sensory Ecology, Behavioural Ecology, Animal Behaviour, Neuroethology and Biophysics. He enjoys combining field work, field experiments, lab work, and theoretical methods as well as constructing electromechanical-optical equipment and software for himself and students.

Characterization of nine polymorphic microsatellite loci in the dyeing poison frog Dendrobates tinctorius (Dendrobatidae), and their cross-species utility in two other dendrobatoid species

While field and laboratory based studies have provided significant insights into the parental care and courtship behaviour of dendrobatoid frogs, a comprehensive assessment of their genetic mating systems and population genetic parameters has been precluded because ofthe lack of highly variable DNA markers. Here we document the development of nine novel polymorphic microsatellite markers for the dyeing poison frog Dendrobates tinct or ius (Dendrobatidae ). We found between three and 16 alleles per locus in 60 individuals (30 males, 30 females) from the field site Saut Parare, French Guiana, with an average observed heterozygosity of 0. 75. None of the loci deviated significantly from Hardy-Weinberg equilibrium or showed linkage disequilibrium. We also report successful cross-species amplification of the nine markers in two other dendrobatoid species (Allobates femora/is and Oophaga pumilio). These markers have the potential to aid in determining the genetic structure of local populations, identifying small-scale phylogenies such as parent-offspring relationships and will allow for cross-species comparisons within dendrobatoid species. Therefore, these markers can be applied to a wide range of scientific fields, such as conservation, behavioural ecology and evolutionary biology.

Charismatic marine mega-fauna: some recent discoveries and future challenges

 The last 20 years have been exciting times for scientists working with charismatic marine mega-fauna. Here recent advances are reviewed. There have been advances in both data gathering and data-analysis techniques that have allowed new insights into the physiological and behavioural ecology of free-ranging mega-faunal species; some marine mega-faunal species have now become model organisms for cutting edge approaches to identify the underlying mathematical properties of animal search patterns and hence the underlying behavioural processes (e.g. Levy flight versus Brownian motion); the implications of climate change have started to become more apparent with extended time-series of animal movements, abundance and performance; conservation issues have become integrated into marine planning and have resulted in the advent of extended networks of marine protected areas (MPAs) as well as large MPAs that span many 100,000 km2; and collaborative crossdisciplinary teams have started to reveal the importance of ocean currents in animal dispersal, the ontogeny of migration and population genetic structure. Looking to the future, increased data availability (e.g. through data sharing) will likely allow more holistic across-taxa analyses to become routine.
© 2013 Elsevier B.V. All rights reserved.

Towards powerful experimental and statistical approaches to study intraindividual variability in labile traits

There is a long-standing interest in behavioural ecology, exploring the causes and correlates of consistent individual differences in mean behavioural traits ('personality') and the response to the environment ('plasticity'). Recently, it has been observed that individuals also consistently differ in their residual intraindividual variability (rIIV). This variation will probably have broad biological and methodological implications to the study of trait variation in labile traits, such as behaviour and physiology, though we currently need studies to quantify variation in rIIV, using more standardized and powerful methodology. Focusing on activity rates in guppies (Poecilia reticulata), we provide a model example, from sampling design to data analysis, in how to quantify rIIV in labile traits. Building on the doubly hierarchical generalized linear model recently used to quantify individual differences in rIIV, we extend the model to evaluate the covariance between individual mean values and their rIIV. After accounting for time-related change in behaviour, our guppies substantially differed in rIIV, and it was the active individuals that tended to be more consistent (lower rIIV). We provide annotated data analysis code to implement these complex models, and discuss how to further generalize the model to evaluate covariances with other aspects of phenotypic variation.

If waterbirds are nocturnal are we conserving the right habitats?

Waterbirds are key indicators of wetland health and recent declines in their abundance have renewed focus on conservation of their habitats in Australia. Yet conservation efforts have mostly ignored the identification of habitats used at night. In this study we assessed three common species, Grey Teal (Anas gracilis), Chestnut Teal (Anas castanea) and Australian Wood Duck (Chenonetta chubata), during day and night. Thermal imaging technologies were utilised to identify individuals to species, count abundances and observe habitat requirements. We found major differences in abundance between night and day of all three species at our study sites. Further, habitat use of teals differed between nocturnal and diurnal hours, with birds aggregating on the bank during daylight hours and moving onto the water during the night. Our findings suggest that nocturnal waterbird surveys can assist conservation efforts. By monitoring bird numbers by night, the significance of a habitat for feeding and shelter purposes can be determined. Additionally, by studying nocturnal behaviour and habitat use, identification and conservation of important wetlands will be increased.

Flowering ecology of a Box-Ironbark Eucalyptus community

Box-Ironbark forests occur on the inland hills of the Great Dividing Range in Australia, from western Victoria to southern Queensland. These dry, open forests are characteristically dominated by Eucalyptus species such as Red Ironbark E. tricarpa, Mugga Ironbark E. sideroxylon and Grey Box E. microcarpa. Within these forests, several Eucalyptus species are a major source of nectar for the blossom-feeding birds and marsupials that form a distinctive component of the fauna. In Victoria, approximately 83% of the original pre - European forests of the Box-Ironbark region have been cleared, and the remaining fragmented forests have been heavily exploited for gold and timber. This exploitation has lead to a change in the structure of these forests, from one dominated by large 80-100 cm diameter, widely -spaced trees to mostly small (≥40 cm DBH), more densely - spaced trees. This thesis examines the flowering ecology of seven Eucalyptus species within a Box-Ironbark community. These species are characteristic of Victorian Box-Ironbark forests; River Red Gum E. camaldulensis, Yellow Gum E. leucoxylon, Red Stringybark E. macrorhyncha, Yellow Box E. melliodora, Grey Box E. microcarpa, Red Box E. polyanthemos and Red Ironbark E. tricarpa. Specifically, the topics examined in this thesis are: (1) the floral character traits of species, and the extent to which these traits can be associated with syndromes of bird or insect pollination; (2) the timing, frequency, duration, intensity, and synchrony of flowering of populations and individual trees; (3) the factors that may explain variation in flowering patterns of individual trees through examination of the relationships between flowering and tree-specific factors of individually marked trees; (4) the influence of tree size on the flowering patterns of individually marked trees, and (5) the spatial and temporal distribution of the floral resources of a dominant species, E. tricarpa. The results are discussed in relation to the evolutionary processes that may have lead to the flowering patterns, and the likely effects of these flowering patterns on blossom-feeding fauna of the Box-Ironbark region. Flowering observations were made for approximately 100 individually marked trees for each species (a total of 754 trees). The flower cover of each tree was assessed at a mean interval of 22 (+ 0.6) days for three years; 1997, 1998 and 1999. The seven species of eucalypt each had characteristic flowering seasons, the timing of which was similar each year. In particular, the timing of peak flowering intensity was consistent between years. Other spatial and temporal aspects of flowering patterns for each species, including the percentage of trees that flowered, frequency of flowering, intensity of flowering and duration of flowering, displayed significant variation between years, between forest stands (sites) and between individual trees within sites. All seven species displayed similar trends in flowering phenology over the study, such that 1997 was a relatively 'poor' flowering year, 1998 a 'good' year and 1999 an 'average' year in this study area. The floral character traits and flowering seasons of the seven Eucalyptus species suggest that each species has traits that can be broadly associated with particular pollinator types. Differences between species in floral traits were most apparent between 'summer' and 'winter' flowering species. Winter - flowering species displayed pollination syndromes associated with bird pollination and summer -flowering species displayed syndromes more associated with insect pollination. Winter - flowering E. tricarpa and E. leucoxylon flowers, for example, were significantly larger, and contained significantly greater volumes of nectar, than those of the summer flowering species, such as E. camaldulensis and E. melliodom. An examination of environmental and tree-specific factors was undertaken to investigate relationships between flowering patterns of individually marked trees of E. microcarpa and E. tricarpa and a range of measures that may influence the observed patterns. A positive association with tree-size was the most consistent explanatory variable for variation between trees in the frequency and intensity of flowering. Competition from near-neighbours, tree health and the number of shrubs within the canopy area were also explanatory variables. The relationship between tree size and flowering phenology was further examined by using the marked trees of all seven species, selected to represent five size-classes. Larger trees (≥40 cm DBH) flowered more frequently, more intensely, and for a greater duration than smaller trees. Larger trees provide more abundant floral resources than smaller trees because they have more flowers per unit area of canopy, they have larger canopies in which more flowers can be supported, and they provide a greater abundance of floral resources over the duration of the flowering season. Heterogeneity in the distribution of floral resources was further highlighted by the study of flowering patterns of E. tricarpa at several spatial and temporal scales. A total of approximately 5,500 trees of different size classes were sampled for flower cover along transects in major forest blocks at each of five sample dates. The abundance of flowers varied between forest blocks, between transects and among tree size - classes. Nectar volumes in flowers of E. tricarpa were sampled. The volume of nectar varied significantly among flowers, between trees, and between forest stands. Mean nectar volume per flower was similar on each sample date. The study of large numbers of individual trees for each of seven species was useful in obtaining quantitative data on flowering patterns of species' populations and individual trees. The timing of flowering for a species is likely to be a result of evolutionary selective forces tempered by environmental conditions. The seven species' populations showed a similar pattern in the frequency and intensity of flowering between years (e.g. 1998 was a 'good' year for most species) suggesting that there is some underlying environmental influence acting on these aspects of flowering. For individual trees, the timing of flowering may be influenced by tree-specific factors that affect the ability of each tree to access soil moisture and nutrients. In turn, local weather patterns, edaphic and biotic associations are likely to influence the available soil moisture. The relationships between the timing of flowering and environmental conditions are likely to be complex. There was no evidence that competition for pollinators has a strong selective influence on the timing of flowering. However, as there is year-round flowering in this community, particular types of pollinators may be differentiated along a temporal gradient (e.g. insects in summer, birds in winter). This type of differentiation may have resulted in the co-evolution of floral traits and pollinator types, with flowers displaying adaptations that match the morphologies and energy requirements of the most abundant pollinators in any particular season. Spatial variation in flowering patterns was evident at several levels. This is likely to occur because of variation in climate, weather patterns, soil types, degrees of disturbance and biotic associations, which vary across the Box-Ironbark region. There was no consistency among sites between years in flowering patterns suggesting that factors affecting flowering at this level are complex. Blossom-feeding animals are confronted with a highly spatially and temporally patchy resource. This patchiness has been increased with human exploitation of these forests leading to a much greater abundance of small trees and fewer large trees. Blossom-feeding birds are likely to respond to this variation in different ways, depending upon diet-breadth, mobility and morphological and behavioural characteristics. Future conservation of the blossom-feeding fauna of Box-Ironbark forests would benefit from the retention of a greater number of large trees, the protection and enhancement of existing remnants, and revegetation with key species, such as E. leucoxylon, E. microcarpa and E. tricarpa. The selective clearing of summer flowering species, which occur on the more fertile areas, may have negatively affected the year-round abundance and distribution of floral resources. The unpredictability of the spatial distribution of flowering patches within the region means that all remnants are likely to be important foraging areas in some years.

Ecology and conservation of insectivorous bats in rural landscapes

Throughout the world, the increasing use of land for agriculture has been associated with extensive loss and fragmentation of natural habitats and, frequently, the degradation of remaining habitats. The effects of such habitat changes have been well studied for some faunal groups, but little is known of their consequences for bats. The aim of this study was to investigate the ecology and conservation of an assemblage of insectivorous bats in a rural landscape, with particular focus on their foraging and roosting requirements. This increased knowledge will, hopefully, assist the formulation of policy and management decisions to ensure the long-term survival of bats in these altered environments. The distribution and abundance of insectivorous bats in the Northern Plains of Victoria was investigated to determine the impacts of land-use change and to identify factors influencing the distribution of bats in rural landscapes. Thirteen species of insectivorous bats were recorded across the region by sampling at 184 sites. Two species were rare, but the remaining 11 species were widespread and occurred in all types of remnant wooded vegetation, ranging from large blocks (≥200 ha) to small isolated remnants (≤5 ha) and scattered trees in cleared farm paddocks. There was no significant difference between remnant types in the relative abundance of bat species, in species richness, or in the composition of bat assemblages at study sites. In a subsequent study, no difference in the activity levels of bats was found between remnants with different tree densities, ranging from densely-vegetated blocks to single paddock trees. However, sites in open paddocks devoid of trees differed significantly from all types of wooded remnants and had significantly lower levels of bat activity and a different species composition. In highly cleared and modified landscapes, all native vegetation has value to bats, even the smallest remnant, roadside and single paddock tree. Roost sites are a key habitat requirement for bats and may be a limiting resource in highly modified environments. Two species, the lesser long-eared bat Nyctophilus geoffroyi and Gould's wattled bat Chalinolobus gouldii, were investigated as a basis for understanding the capacity of bats to survive in agricultural landscapes. These species have different wing morphologies, which may be influential in how they use the landscape, and anecdotal evidence suggested differences in their roosting ecology. Roosting ecology was examined using radio-tracking to locate 376 roosts in two study areas with contrasting tree cover in northern Victoria. Both species were highly selective in the location of their roosts in the landscape, in roost-site selection and in roosting behaviour, and responded differently to differing levels of availability of roosts. The Barmah-Picola study area incorporated remnant vegetation in farmland and an adjacent extensive floodplain forest (Barmah forest). Male N. geojfroyi roosted predominantly within 3 km of their foraging areas in remnants in farmland. However, most female N. geoffroyi, and both sexes of C. gouldii, roosted in Barmah forest up to 12 km from their foraging areas in farmland remnants. These distances were greater than previously recorded for these species and further than predicted by wing morphology. In contrast, in the second study area (Naring) where only small remnants of wooded vegetation remain in farmland, individuals of both species moved significantly shorter distances between roost sites and foraging areas. There were marked inter- and intra-specific differences in the roosts selected. C. gouldii used similar types of roosts in both areas - predominantly dead spouts in large, live trees. N. geoffroyi used a broader range of roost types, especially in the farmland environment. Roosts were typically under bark and in fissures, with males in particular also using anthropogenic structures. A strong preference was shown by both sexes for roosts in dead trees, and entrance dimensions of roosts were consistently narrow (2.5 cm). In Barmah forest, maternity roosts used by N. geoffroyi were predominantly in narrow fissures in large-diameter, dead trees, while at Naring maternity roosts were also found under bark, in buildings, and in small-diameter, live and dead trees. The number of roost trees that are required for an individual or colony is influenced by the frequency with which bats move between roosts, the proportion of roosts that are re-used, the distance between consecutive roosts, and the size of roosting colonies. Both species roosted in small colonies and regularly shifted roost sites within a discrete roost area. These behavioural traits suggest that a high density of roost sites is required. There were marked differences in these aspects of behaviour between individuals roosting in Barmah forest and in the fragmented rural landscape. At Naring, N. geqffroyi remained in roosts for longer periods and moved greater distances between consecutive roosts than in Barmah forest. In contrast, C. gouldii used a smaller pool of roosts in the farmland environment by re-using roosts more frequently. Within Barmah forest, there is an extensive area of forest but the density of hollow-bearing trees is reduced due to timber harvesting and silvicultural practices. Individuals were selective in the location of their roosting areas, with both species selecting parts of the forest that contained higher densities of their preferred roost trees than was generally available in the forest. In contrast, in farmland at Naring, where there were small pockets of remnant vegetation with high densities of potential roost sites surrounded by cleared paddocks with few roosting opportunities, little selection was shown. This suggests that in Barmah forest the density of trees with potential roosts is lower than optimal, while in farmland roosting resources may be adequate in woodland remnants, but limiting at the landscape scale since more than 95% of the landscape now provides no roosting opportunities. Insectivorous bats appear to be less severely affected than some other faunal groups by habitat fragmentation and land-use change. A highly developed capacity for flight, the spatial scale at which they move and their ability to cross open areas means that they can regularly move among multiple landscape elements, rather than depend on single remnants for all their resources. In addition, bats forage and roost mainly at elevated levels in trees and so are less sensitive to degradation of wooded habitats at ground level. Although seemingly resilient to habitat fragmentation, insectivorous bats are fundamentally dependent on trees for roosting and foraging, and so are vulnerable to habitat loss and ongoing rural tree decline. Protection of the remaining large old trees and measures to ensure regeneration to provide ongoing replacement of hollow-bearing trees through time are critical to ensure the long-term conservation of bats in rural landscapes.

The biology and ecology of the ocean sunfish Mola mola : a review of current knowledge and future research perspectives

Relatively little is known about the biology and ecology of the world’s largest (heaviest) bony fish, the ocean sunfish Mola mola, despite its worldwide occurrence in temperate and tropical seas. Studies are now emerging that require many common perceptions about sunfish behaviour and ecology to be re-examined. Indeed, the long-held view that ocean sunfish are an inactive, passively drifting species seems to be entirely misplaced. Technological advances in marine telemetry are revealing distinct behavioural patterns and protracted seasonal movements. Extensive forays by ocean sunfish into the deep ocean have been documented and broad-scale surveys, together with molecular and laboratory based techniques, are addressing the connectivity and trophic role of these animals. These emerging molecular and movement studies suggest that local distinct populations may be prone to depletion through bycatch in commercial fisheries. Rising interest in ocean sunfish, highlighted by the increase in recent publications, warrants a thorough review of the biology and ecology of this species. Here we review the taxonomy, morphology, geography, diet, locomotion, vision, movements, foraging ecology, reproduction and species interactions of M. mola. We present a summary of current conservation issues and suggest methods for addressing fundamental gaps in our knowledge.

Movement ecology of nomadic arid zone waterfowl

This thesis provides insights into the spatial and temporal patterns of movement in nomadic waterfowl, the response of birds to rapid environmental change, behavioural flexibility of avian movements and the ability of birds to locate seemingly unpredictable water bodies in vast arid landscapes.

Does angling technique selectively target fishes based on their behavioural type?

Recently, there has been growing recognition that fish harvesting practices can have important impacts on the phenotypic distributions and diversity of natural populations through a phenomenon known as fisheries-induced evolution. Here we experimentally show that two common recreational angling techniques (active crank baits versus passive soft plastics) differentially target wild largemouth bass (Micropterus salmoides) and rock bass (Ambloplites rupestris) based on variation in their behavioural tendencies. Fish were first angled in the wild using both techniques and then brought back to the laboratory and tested for individual-level differences in common estimates of personality (refuge emergence, flight-initiation-distance, latency-to-recapture and with a net, and general activity) in an in-lake experimental arena. We found that different angling techniques appear to selectively target these species based on their boldness (as characterized by refuge emergence, a standard measure of boldness in fishes) but not other assays of personality. We also observed that body size was independently a significant predictor of personality in both species, though this varied between traits and species. Our results suggest a context-dependency for vulnerability to capture relative to behaviour in these fish species. Ascertaining the selective pressures angling practices exert on natural populations is an important area of fisheries research with significant implications for ecology, evolution, and resource management.