Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain''s sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.     

Different strokes: Can managing behavioral types increase post-release success?

Re-introduction programs for endangered animals operate under the hope that protected habitats can sustain viable populations that rely little on humans. The goal of these programs is to supply animals with the resources and skills they need to succeed in the modern wild. However, predicting the set of skills necessary to respond to unpredictable selection events is difficult and efforts sometimes fail as animals respond inappropriately to environmental variation because they lack behavioral flexibility. Population resilience to environmental change may be enhanced if all members of a population do not exhibit the same response when selection pressures change. In many species individual animals express behavioral types that exhibit alternative responses to the same stimuli. Yet when animals are prepared for release to the wild, there is rarely consideration of consistent behavioral variation between individuals. Since experience influences both behavioral and physiological responses to varied stimuli and can shape the future behavioral type of captive animals, pre-release environmental enrichment may be successful in facilitating the expression of varied behavioral types in populations slated for release. This approach to environmental enrichment requires a departure from a ‘one size fits all’ strategy and may also involve exposure to increased challenge and competition. In addition, there is a need for empirical evidence to better understand the role of environmental enrichment and behavioral types on post-release success. The zoo environment provides an excellent arena for examining the development and expression of behavioral types and for taking a novel functional approach to environmental enrichment research that may prove to be very important to re-introduction efforts.     

Less is more: density influences the development of behavioural life skills in trout

Theory suggests that habitat structure and population density profoundly influence the phenotypic development of animals. Here, we predicted that reduced rearing density and increased structural complexity promote food search ability, anti-predator response and the ability to forage on novel prey, all behavioural skills important for surviving in the wild. Brown trout were reared at three densities (conventional hatchery density, a fourth of conventional hatchery density and natural density) in tanks with or without structure. Treatment effects on behaviour were studied on trout fry and parr, whereupon 20 trout from each of the six treatment groups were released in an enclosed natural stream and recaptured after 36 days. Fry reared at natural density were faster to find prey in a maze. Moreover, parr reared at natural density were faster to eat novel prey, and showed more efficient anti-predator behaviour than fish reared at higher densities. Furthermore, parr reared at reduced densities were twice as likely to survive in the stream as trout reared at high density. In contrast, we found no clear treatment effects of structure. These novel results suggest that reduced rearing densities can facilitate the development of behavioural life skills in captive animals, thereby increasing their contribution to natural production.     

Light,heat, action: neural control of fruit fly behaviour

The fruit fly Drosophila melanogaster has emerged as a popular model to investigate fundamental principles of neural circuit operation. The sophisticated genetics and small brain permit a cellular resolution understanding of innate and learned behavioural processes. Relatively recent genetic and technical advances provide the means to specifically and reproducibly manipulate the function of many fly neurons with temporal resolution. The same cellular precision can also be exploited to express genetically encoded reporters of neural activity and cell-signalling pathways. Combining these approaches in living behaving animals has great potential to generate a holistic view of behavioural control that transcends the usual molecular, cellular and systems boundaries. In this review, we discuss these approaches with particular emphasis on the pioneering studies and those involving learning and memory.     

Plasticity and evolution in correlated suites of traits

When organisms are faced with new or changing environments, a central challenge is the coordination of adaptive shifts in many different phenotypic traits. Relationships among traits may facilitate or constrain evolutionary responses to selection, depending on whether the direction of selection is aligned or opposed to the pattern of trait correlations. Attempts to predict evolutionary potential in correlated traits generally assume that correlations are stable across time and space; however, increasing evidence suggests that this may not be the case, and flexibility in trait correlations could bias evolutionary trajectories. We examined genetic and environmental influences on variation and covariation in a suite of behavioural traits to understand if and how flexibility in trait correlations influences adaptation to novel environments. We tested the role of genetic and environmental influences on behavioural trait correlations by comparing Trinidadian guppies (Poecilia reticulata) historically adapted to high‐ and low‐predation environments that were reared under native and non‐native environmental conditions. Both high‐ and low‐predation fish exhibited increased behavioural variance when reared under non‐native vs. native environmental conditions, and rearing in the non‐native environment shifted the major axis of variation among behaviours. Our findings emphasize that trait correlations observed in one population or environment may not predict correlations in another and that environmentally induced plasticity in correlations may bias evolutionary divergence in novel environments.     

MAGI-1 Modulates AMPA Receptor Synaptic Localization and Behavioral Plasticity in Response to Prior Experience

It is well established that the efficacy of synaptic connections can be rapidly modified by neural activity, yet how the environment and prior experience modulate such synaptic and behavioral plasticity is only beginning to be understood. Here we show in C. elegans that the broadly conserved scaffolding molecule MAGI-1 is required for the plasticity observed in a glutamatergic circuit. This mechanosensory circuit mediates reversals in locomotion in response to touch stimulation, and the AMPA-type receptor (AMPAR) subunits GLR-1 and GLR-2, which are required for reversal behavior, are localized to ventral cord synapses in this circuit. We find that animals modulate GLR-1 and GLR-2 localization in response to prior mechanosensory stimulation; a specific isoform of MAGI-1 (MAGI-1L) is critical for this modulation. We show that MAGI-1L interacts with AMPARs through the intracellular domain of the GLR-2 subunit, which is required for the modulation of AMPAR synaptic localization by mechanical stimulation. In addition, mutations that prevent the ubiquitination of GLR-1 prevent the decrease in AMPAR localization observed in previously stimulated magi-1 mutants. Finally, we find that previously-stimulated animals later habituate to subsequent mechanostimulation more rapidly compared to animals initially reared without mechanical stimulation; MAGI-1L, GLR-1, and GLR-2 are required for this change in habituation kinetics. Our findings demonstrate that prior experience can cause long-term alterations in both behavioral plasticity and AMPAR localization at synapses in an intact animal, and indicate a new, direct role for MAGI/S-SCAM proteins in modulating AMPAR localization and function in the wake of variable sensory experience.     

Discrimination reversal learning reveals greater female behavioural flexibility in guppies

Behavioural flexibility allows an animal to adapt its behaviour in response to changes in the environment. Research conducted in primates, rodents and domestic fowl suggests greater behavioural persistence and reduced behavioural flexibility in males. We investigated sex differences in behavioural flexibility in fish by comparing male and female guppies (Poecilia reticulata) in a reversal learning task. Fish were first trained on a colour discrimination, which was learned equally rapidly by males and females. However, once the reward contingency was reversed, females were better at inhibiting the previous response and reached criterion twice as fast as males. When reward reversing was repeated, males gradually reduced the number of errors, and the two sexes had a comparable performance after four reversals. We suggest that sex differences in behavioural flexibility in guppies can be explained in terms of the different roles that males and females play in reproduction.     

Ocean acidification impairs crab foraging behaviour

Anthropogenic elevation of atmospheric CO₂ is driving global-scale ocean acidification, which consequently influences calcification rates of many marine invertebrates and potentially alters their susceptibility to predation. Ocean acidification may also impair an organism''s ability to process environmental and biological cues. These counteracting impacts make it challenging to predict how acidification will alter species interactions and community structure. To examine effects of acidification on consumptive and behavioural interactions between mud crabs (Panopeus herbstii) and oysters (Crassostrea virginica), oysters were reared with and without caged crabs for 71 days at three pCO₂ levels. During subsequent predation trials, acidification reduced prey consumption, handling time and duration of unsuccessful predation attempt. These negative effects of ocean acidification on crab foraging behaviour more than offset any benefit to crabs resulting from a reduction in the net rate of oyster calcification. These findings reveal that efforts to evaluate how acidification will alter marine food webs should include quantifying impacts on both calcification rates and animal behaviour.     

Early experience affects learning performance and neophobia in a cooperatively breeding cichlid

The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non‐social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full‐factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents.     

The aggressive behavior of Nile tilapia introduced into novel environments with variation in enrichment

Many studies show environmental enrichment is correlated with benefits to captive animals; however, one should not always assume this positive relationship given that enrichment increases the amount of resources that a territorial animal must defend and possibly affects its aggressive dynamics. In this study, we tested if environmental enrichment affects aggressive interactions in the aggressive fish Nile tilapia (Oreochromis niloticus). We compared fights staged between pairs of male tilapia of similar size (= matched in resource holding potential) in a novel arena that was either barren or enriched, to examine whether enrichment enhances territory value in line with theoretical predictions, with the potential for compromised welfare. We evaluated time elapsed until the first attack (latency), frequency of aggressive interactions and fight duration. We detected fight dynamic differences at the pair level. Higher resource value generated increased aggression but had no effect on fight duration or latency. This conclusion is in line with game theory predictions concerning resource value and contradicts the theory that enrichment of the environment will serve welfare purposes.     

Maternal body condition influences magnitude of anti-predator response in offspring

Organisms exhibit plasticity in response to their environment, but there is large variation even within populations in the expression and magnitude of response. Maternal influence alters offspring survival through size advantages in growth and development. However, the relationship between maternal influence and variation in plasticity in response to predation risk is unknown. We hypothesized that variation in the magnitude of plastic responses between families is at least partly due to maternal provisioning and examined the relationship between maternal condition, egg provisioning and magnitude of plastic response to perceived predation risk (by dragonfly larvae: Aeshna spp.) in northern leopard frogs (Lithobates pipiens). Females in better body condition tended to lay more (clutch size) larger (egg diameter) eggs. Tadpoles responded to predation risk by increasing relative tail depth (morphology) and decreasing activity (behaviour). We found a positive relationship between morphological effect size and maternal condition, but no relationship between behavioural effect size and maternal condition. These novel findings suggest that limitations imposed by maternal condition can constrain phenotypic variation, ultimately influencing the capacity of populations to respond to environmental change.     

Age and social experience induced plasticity across brain regions of the paper wasp Polistes fuscatus

Developmental studies of brain volumes can reveal which portions of neural circuits are sensitive to environmental inputs. In social insects, differences in relative investment across brain regions emerge as behavioural repertoires change during ontogeny or as a result of experience. Here, we test the effects of maturation and social experience on morphological brain development in Polistes fuscatus paper wasps, focusing on brain regions involved in visual and olfactory processing. We find that mature wasps regardless of social experience have relatively larger brains than newly emerged wasps and this difference is driven by changes to mushroom body calyx and visual regions but not olfactory processing neuropils. Notably, social wasps invest more in the anterior optic tubercle (AOT), a visual glomerulus involved in colour and object processing in other taxa, relative to other visual integration centres the mushroom body calyces compared with aged socially naive wasps. Differences in developmental plasticity between visual and olfactory neuropil volumes are discussed in light of behavioural maturation in paper wasps, especially as it relates to social recognition. Previous research has shown that P. fuscatus need social experience to develop specialized visual processing of faces, which is used to individually recognize conspecifics. The present study suggests that the AOT is a candidate brain region that could mediate facial processing in this species.     

Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.     

Environmental effects on fish neural plasticity and cognition

Most fishes experiencing challenging environments are able to adjust and adapt their physiology and behaviour to help them cope more effectively. Much of this flexibility is supported and influenced by cognition and neural plasticity. The understanding of fish cognition and the role played by different regions of the brain has improved significantly in recent years. Techniques such as lesioning, tract tracing and quantifying changes in gene expression help in mapping specialized brain areas. It is now recognized that the fish brain remains plastic throughout a fish's life and that it continues to be sensitive to environmental challenges. The early development of fish brains is shaped by experiences with the environment and this can promote positive and negative effects on both neural plasticity and cognitive ability. This review focuses on what is known about the interactions between the environment, the telencephalon and cognition. Examples are used from a diverse array of fish species, but there could be a lot to be gained by focusing research on neural plasticity and cognition in fishes for which there is already a wealth of knowledge relating to their physiology, behaviour and natural history, e.g. the Salmonidae.     

The police are not the army: context-dependent aggressiveness in a clonal ant

Animals often exhibit particular ‘personalities’, i.e. their behaviour is correlated across different situations. Recent studies suggest that this limitation of behavioural plasticity may be adaptive, since continuous adjustment of one''s behaviour may be time-consuming and costly. In social insects, particularly aggressive workers might efficiently take over fighting in the contexts of both nest defence and ‘policing’, i.e. the regulation of kin conflict in the society. Here, we examine whether workers who engage in aggressive policing in the ant Platythyrea punctata play a prominent role also in nest defence against intruders. The participation of individuals in policing and nest defence was highly skewed and a minority of workers exhibited most of the aggression. Workers who attacked reproductives after experimental colony fusion were less active during nest defence and vice versa. This suggests that workers show situation-dependent behavioural plasticity rather than consistently aggressive personalities.     

The challenge of managing Spix Macaws (Cyanopsitta spixii) at Qatar - an eleven-year retrospection

This article summarizes the experience of 11 years Spix's Macaw captive management in Al Wabra Wildlife Preservation (AWWP)/Qatar. Details on AWWP's acquisition of Spix's Macaws, research, breeding management, demographics, diet, housing, veterinary work, behavioural enrichment and problems are described and explained. At the end we discuss the future prospects and plans related to this species in AWWP. To our knowledge, at the time of writing, 87 Spix's macaws are existing in captivity, 75 of them participate in the international breeding program, initiated and managed by the “Institute Chico Mendes of Biodiversity Conservation (ICMBio)”, the Brazilian environmental agency. In 2011, 55 of these breeding program birds live at AWWP in Qatar.     

Field crickets change mating preferences using remembered social information

Plasticity in female mate choice can fundamentally alter selection on male ornaments, but surprisingly few studies have examined the role of social learning in shaping female mating decisions in invertebrates. We used the field cricket Teleogryllus oceanicus to show that females retain information about the attractiveness of available males based on previous social experience, compare that information with incoming signals and then dramatically reverse their preferences to produce final, predictable, mating decisions. Male ornament evolution in the wild may depend much more on the social environment and behavioural flexibility through learning than was previously thought for non-social invertebrates. The predictive power of these results points to a pressing need for theoretical models of sexual selection that incorporate effects of social experience.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Chemosensory basis of behavioural plasticity in response to deterrent plant chemicals in the larva of the Small Cabbage White butterfly Pieris rapae

Behavioural and electrophysiological responsiveness to three chemically different secondary plant substances was studied in larvae of Pieris rapae L. (Lepidoptera: Pieridae). Three groups of caterpillars were studied that during their larval development were exposed to different rearing diets: an artificial diet or one of two host-plants, cabbage, Brassica oleracea, or nasturtium, Tropaeolum majus. In dual-choice leaf disc assays, caterpillars reared on cabbage were strongly deterred by the phenolic chlorogenic acid, the flavonol glycoside naringin and the alkaloid strychnine. However, behavioural plasticity was found in caterpillars reared on nasturtium or artificial diet in that these did not discriminate against chlorogenic acid. Caterpillars reared on the artificial diet were also significantly less sensitive to naringin and strychnine in the behavioural assay. Electrophysiological studies of the maxillary sensilla styloconica revealed that the deterrent neuron in the medial sensillum, but not in the lateral sensillum, of cabbage-reared caterpillars was more sensitive than the same neuron type of caterpillars reared on nasturtium or artificial diet. We conclude that (1) the diet-induced behavioural habituation to deterrents can at least partly be explained by chemosensory desensitisation of a generalist type of maxillary deterrent neuron; (2) behavioural cross-habituation to the three structurally diverse deterrent compounds can be traced back to cross-sensitivity for these compounds in the same gustatory neuron.     

Predators modify the evolutionary response of prey to temperature change

As climate regimes shift in many ecosystems worldwide, evolution may be a critical process allowing persistence in rapidly changing environments. Organisms regularly interact with other species, yet whether climate-mediated evolution can occur in the context of species interactions is not well understood. We tested whether a species interaction could modify evolutionary responses to temperature. We demonstrate that predation pressure by Dipteran larvae (Chaoborus americanus) modified the evolutionary response of a freshwater crustacean (Daphnia pulex) to its thermal environment over approximately seven generations in laboratory conditions. Daphnia kept at 21°C evolved higher population growth rates than those kept at 18°C, but only in those populations that were also reared with predators. Furthermore, predator-mediated selection resulted in the evolution of elevated Daphnia thermal plasticity. This laboratory natural selection experiment demonstrates that biotic interactions can modify evolutionary adaptation to temperature. Understanding the interplay between multiple selective forces can improve predictions of ecological and evolutionary responses of organisms to rapid environmental change.