The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Behavioural phenotypes over the lifetime of a holometabolous insect

Introduction: Behavioural traits can differ considerably between individuals, and such differences were found to be consistent over the lifetime of an organism in several species. Whether behavioural traits of holometabolous insects, which undergo a metamorphosis, are consistent across ontogeny is virtually unexplored. We investigated several behavioural parameters at five different time points in the lifetime of the holometabolous mustard leaf beetle Phaedon cochleariae (Coleoptera: Chrysomelidae), two times in the larval (second and third larval stage) and three times in the adult stage. We investigated 1) the stability of the behavioural phenotype (population level), 2) whether individuals rank consistently across behavioural traits and over their lifetime (individual level), and 3) in how far behavioural traits are correlated with the developmental time of the individuals.Results: We identified two behavioural dimensions in every life stage of P. cochleariae, activity and boldness (population level). Larvae and young adults ranked consistently across the investigated behavioural traits, whereas consistency over time was only found in adults but not between larvae and adults (individual level). Compared to adult beetles, larvae were less active. Moreover, younger larvae were bolder than all subsequent life stages. Over the adult lifetime of the beetles, males were less active than females. Furthermore, the activity of second instar larvae was significantly negatively correlated with the development time.Conclusions: Our study highlights that, although there is no individual consistency over the larval and the adult life stage, the behavioural clustering shows similar patterns at all tested life stages of a holometabolous insect. Nevertheless, age- and sex-specific differences in behavioural traits occur which may be explained by different challenges an individual faces at each life stage. These differences are presumably related to the tremendous changes in life-history traits from larvae to adults and/or to a niche shift after metamorphosis as well as to different needs of both sexes, respectively. A faster development of more active compared to less active second instar larvae is in line with the pace-of-life syndrome. Overall, this study demonstrates a pronounced individuality in behavioural phenotypes and presumably adaptive changes related to life stage and sex.     

Turning Shy on a Winter's Day: Effects of Season on Personality and Stress Response in Microtus arvalis

Animal personalities are by definition stable over time, but to what extent they may change during development and in adulthood to adjust to environmental change is unclear. Animals of temperate environments have evolved physiological and behavioural adaptations to cope with the cyclic seasonal changes. This may also result in changes in personality: suites of behavioural and physiological traits that vary consistently among individuals. Winter, typically the adverse season challenging survival, may require individuals to have shy/cautious personality, whereas during summer, energetically favourable to reproduction, individuals may benefit from a bold/risk‐taking personality. To test the effects of seasonal changes in early life and in adulthood on behaviours (activity, exploration and anxiety), body mass and stress response, we manipulated the photoperiod and quality of food in two experiments to simulate the conditions of winter and summer. We used the common voles (Microtus arvalis) as they have been shown to display personality based on behavioural consistency over time and contexts. Summer‐born voles allocated to winter conditions at weaning had lower body mass, a higher corticosterone increase after stress and a less active, more cautious behavioural phenotype in adulthood compared to voles born in and allocated to summer conditions. In contrast, adult females only showed plasticity in stress‐induced corticosterone levels, which were higher in the animals that were transferred to the winter conditions than to those staying in summer conditions. These results suggest a sensitive period for season‐related behavioural plasticity in which juveniles shift over the bold–shy axis.     

Behavioural phenotype affects social interactions in an animal network

Animal social networks can be extremely complex and are characterized by highly non-random interactions between group members. However, very little is known about the underlying factors affecting interaction preferences, and hence network structure. One possibility is that behavioural differences between individuals, such as how bold or shy they are, can affect the frequency and distribution of their interactions within a network. We tested this using individually marked three-spined sticklebacks (Gasterosteus aculeatus), and found that bold individuals had fewer overall interactions than shy fish, but tended to distribute their interactions more evenly across all group members. Shy fish, on the other hand, tended to associate preferentially with a small number of other group members, leading to a highly skewed distribution of interactions. This was mediated by the reduced tendency of shy fish to move to a new location within the tank when they were interacting with another individual; bold fish showed no such tendency and were equally likely to move irrespective of whether they were interacting or not. The results show that animal social network structure can be affected by the behavioural composition of group members and have important implications for understanding the spread of information and disease in social groups.     

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

The boldness of individual Brachyrhaphis episcopi , collected from regions of high and low predation, was investigated using two independent assays: (1) the time to emerge from cover and (2) the propensity to leave shoal mates and investigate a novel object. A strong correlation between the two assays was revealed such that fish that emerged from shelter sooner were also more likely to approach a novel object. This is indicative of a boldness personality axis acting across both behavioural contexts. Fish from high-predation areas were bolder than those from low-predation areas and males were bolder than females. A significant correlation between body mass, standard length ( L _S) and boldness score was also found. In general, bold fish had a greater body mass at a given L _S than shy fish. These results suggest that personality traits are strongly influenced by population-specific ecological variables and may have fitness consequences in wild populations.     

Plasticity of boldness in rainbow trout,Oncorhynchus mykiss: do hunger and predation influence risk-taking behaviour?

Boldness, a measure of an individual's propensity for taking risks, is an important determinant of fitness but is not necessarily a fixed trait. Dependent upon an individual's state, and given certain contexts or challenges, individuals may be able to alter their inclination to be bold or shy in response. Furthermore, the degree to which individuals can modulate their behaviour has been linked with physiological responses to stress. Here we attempted to determine whether bold and shy rainbow trout, Oncorhynchus mykiss, can exhibit behavioural plasticity in response to changes in state (nutritional availability) and context (predation threat). Individual trout were initially assessed for boldness using a standard novel object paradigm; subsequently, each day for one week fish experienced either predictable, unpredictable, or no simulated predator threat in combination with a high (2% body weight) or low (0.15%) food ration, before being reassessed for boldness. Bold trout were generally more plastic, altering levels of neophobia and activity relevant to the challenge, whereas shy trout were more fixed and remained shy. Increased predation risk generally resulted in an increase in the expression of three candidate genes linked to boldness, appetite regulation and physiological stress responses - ependymin, corticotrophin releasing factor and GABA(A) - but did not produce a significant increase in plasma cortisol. The results suggest a divergence in the ability of bold and shy trout to alter their behavioural profiles in response to internal and exogenous factors, and have important implications for our understanding of the maintenance of different behavioural phenotypes in natural populations.     

Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure

The aim of this study was to identify periods in zebrafish (Danio rerio) development when estrogen exposure has long-term consequences on reproductive capabilities at the adult stage. To this end, zebrafish were exposed to 10 ng/L ethynylestradiol (EE(2)) during three stages of gonadal differentiation: (i) the juvenile hermaphroditic stage when gonads display the morphology of an immature ovary (in our zebrafish colony this lasted from 15 to 42 days post-fertilization [dpf]), (ii) the gonad transition stage when the hermaphroditic gonad differentiates into either testes or ovary (from 43 to day 71 dpf), and (iii) the premature stage of testicular and ovarian development (from 72 to 99 dpf). The consequences of stage-specific exposure to EE(2) were assessed by determining time to first spawning, fecundity (number of eggs per female per day), fertilization success (percentage of fertilized eggs) and sex ratio of the adults. Exposure during the gonad transition period induced a delay in the onset of spawning and a significant reduction of fecundity and fertilization success, whereas exposure during the hermaphroditic stage or during the premature stage had no significant impact on the reproductive parameters of adult fish. The results from this experiment pointed to the gonad transition stage as being most susceptible to persistent effects of developmental estrogen exposure. In a second experiment, the concentration dependency of the EE(2)effects was evaluated by exposing zebrafish during the gonad transition stage (43-71 dpf) to 1.67, 3 or 10 ng EE(2)/L. Significant effects of EE(2) on adult reproduction were found with 3 and 10 ng EE(2)/L, but not with 1.67 ng/L. Histological examination of the gonads revealed that at termination of EE(2) exposure (71 dpf), all individuals in the 3 and 10 ng EE(2)/L treatment possessed ovaries. However, this feminising effect appeared to be reversible since at the adult stage (190 dpf), both fish with ovaries and with testes were found. Thus, EE(2) exposure during the gonad transition stage seems to have no persistent effect on gonad histology but on reproductive capabilities.     

The genetic covariance between life cycle stages separated by metamorphosis

Metamorphosis is common in animals, yet the genetic associations between life cycle stages are poorly understood. Given the radical changes that occur at metamorphosis, selection may differ before and after metamorphosis, and the extent that genetic associations between pre- and post-metamorphic traits constrain evolutionary change is a subject of considerable interest. In some instances, metamorphosis may allow the genetic decoupling of life cycle stages, whereas in others, metamorphosis could allow complementary responses to selection across the life cycle. Using a diallel breeding design, we measured viability at four ontogenetic stages (embryo, larval, juvenile and adult viability), in the ascidian Ciona intestinalis and examined the orientation of additive genetic variation with respect to the metamorphic boundary. We found support for one eigenvector of G (g_obsmax), which contrasted larval viability against embryo viability and juvenile viability. Target matrix rotation confirmed that while g_obsmax shows genetic associations can extend beyond metamorphosis, there is still considerable scope for decoupled phenotypic evolution. Therefore, although genetic associations across metamorphosis could limit that range of phenotypes that are attainable, traits on either side of the metamorphic boundary are capable of some independent evolutionary change in response to the divergent conditions encountered during each life cycle stage.     

Can We Predict Personality in Fish? Searching for Consistency over Time and across Contexts

The interest in animal personality, broadly defined as consistency of individual behavioural traits over time and across contexts, has increased dramatically over the last years. Individual differences in behaviour are no longer recognised as noise around a mean but rather as adaptive variation and thus, essentially, raw material for evolution. Animal personality has been considered evolutionary conserved and has been shown to be present in all vertebrates including fish. Despite the importance of evolutionary and comparative aspects in this field, few studies have actually documented consistency across situations in fish. In addition, most studies are done with individually housed fish which may pose additional challenges when interpreting data from social species. Here, we investigate, for the first time in fish, whether individual differences in behavioural responses to a variety of challenges are consistent over time and across contexts using both individual and grouped-based tests. Twenty-four juveniles of Gilthead seabream Sparus aurata were subjected to three individual-based tests: feed intake recovery in a novel environment, novel object and restraining and to two group-based tests: risk-taking and hypoxia. Each test was repeated twice to assess consistency of behavioural responses over time. Risk taking and escape behaviours during restraining were shown to be significantly consistent over time. In addition, consistency across contexts was also observed: individuals that took longer to recover feed intake after transfer into a novel environment exhibited higher escape attempts during a restraining test and escaped faster from hypoxia conditions. These results highlight the possibility to predict behaviour in groups from individual personality traits.     

Express yourself: bold individuals induce enhanced morphological defences

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey''s lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences.     

Shoal composition determines foraging success in the guppy

The composition of an animal group can impact greatly on thesurvival and success of its individual members. Much recentwork has concentrated on behavioral variation within animalpopulations along the bold/shy continuum. Here, we screenedindividual guppies, Poecilia reticulata, for boldness usingan overhead fright stimulus. We created groups consisting of4 bold individuals (bold shoals), 4 shy individuals (shy shoals),or 2 bold and 2 shy individuals (mixed shoals). The performanceof these different shoal types was then tested in a novel foragingscenario. We found that both bold and mixed shoals approacheda novel feeder in less time than shy shoals. Interestingly,we found that more fish from mixed shoals fed than in eitherbold or shy shoals. We suggest that this can be explained bythe fact that nearly all the cases where one fish was followedinto the feeder by another occurred within mixed shoals andthat it was almost always a shy fish following a bold one. Theseresults suggest clear foraging benefits to shy individuals throughassociating with bold ones. Surprisingly, our results also suggestpotential foraging benefits to bold individuals through associatingwith shy individuals. This study highlights a possible mechanismby which interindividual variation in behavioral types is maintainedin a population.     

Risk‐taking behaviour variation over time in sea bass Dicentrarchus labrax: effects of day–night alternation,fish phenotypic characteristics and selection for growth

Differences in bold and shy personality on sea bass Dicentrarchus labrax were investigated between a population (wild) produced from wild‐brood fish and a population (selected) produced from selected‐brood fish. During the experiment (112 days), fish were reared under self‐feeding condition to characterize the feeding behaviour of each individual fish. Three risk‐taking tests (T1, T2 and T3 of 24 h with day–night alternation) were carried out at > 1 month intervals on 180 fish of each strain in order to monitor D. labrax behaviour over time and in relation to the light:dark period. A risk‐taking score was evaluated via a preference choice between a safe zone (without food) and a risky zone (potentially with food) by recording the number and the duration of individual passages through an opening in an opaque divider. Results showed that fish performed passages preferentially during the night period and that wild fish were generally bolder than selected fish during T1 and T2 but showed a decrease in risk taking during T3, contrary to selected fish which showed a constant increase in their risk‐taking behaviour. The phenotypic characteristics of the bold fish were different in the two strains: wild bold fish were the smallest within the wild strain and selected bold fish presented the higher growth rate within the selected strain. For both strains, these bold fish were also generally characterized by a high feed‐demand activity. Fish hunger state thus seemed to be the highest motivation for risk‐taking behaviour under the present conditions. Furthermore, behavioural variations over tests such as higher risk taking (number of passages) and faster exploratory responses (higher score emergence) could be interpreted as relevant indicators of the learning process and habituation. According to the results, however, no real difference in coping strategy between strains could be observed at this first stage of domestication and selection.     

Small within-day increases in temperature affects boldness and alters personality in coral reef fish

Consistent individual differences in behaviour, termed personality, are common in animal populations and can constrain their responses to ecological and environmental variation, such as temperature. Here, we show for the first time that normal within-daytime fluctuations in temperature of less than 3°C have large effects on personality for two species of juvenile coral reef fish in both observational and manipulative experiments. On average, individual scores on three personality traits (PTs), activity, boldness and aggressiveness, increased from 2.5- to sixfold as a function of temperature. However, whereas most individuals became more active, aggressive and bold across temperature contexts (were plastic), others did not; this changed the individual rank order across temperatures and thus altered personality. In addition, correlations between PTs were consistent across temperature contexts, e.g. fish that were active at a given temperature also tended to be both bold and aggressive. These results (i) highlight the importance of very carefully controlling for temperature when studying behavioural variation among and within individuals and (ii) suggest that individual differences in energy metabolism may contribute to animal personality, given that temperature has large direct effects on metabolic rates in ectotherms.     

Larval development of the oriental lancelet, Branchiostoma belcheri, in laboratory mass culture

We are successfully maintaining a laboratory colony of the lancelet Branchiostoma belcheri bred in the laboratory. Based on living individuals in this mass culture, morphological characteristics from the seven-day larval to benthic juvenile stages have been studied. Most striking was that later larval development of B. belcheri showed great individual variation even in a rather stable culture environment. Metamorphosis first occurred on 60 days post fertilization (dpf) and was continuously observed throughout the present study up to 100 dpf. Morphological traits such as the number of primary gill slits and body size at the start of metamorphosis are apparently affected by culture condition. Body size measured in the largest individuals showed nearly linear growth at 0.087 mm/day. The variability found in larval development calls for caution when developmental stages and chronological ages are compared between populations. However, the developmental flexibility of this animal also raises the possibility that growth and sexual maturation could be controlled artificially in captivity.     

Linking larval history to juvenile demography in the bicolor damselfish Stegastes partitus (Perciformes: Pomacentridae)

Otolith-based reconstructions of daily larval growth increments were used to examine the effect of variation in larval growth on size and age at settlement and post-settlement growth, survival and habitat preferences of juvenile bicolor damselfish (Stegastes partitus Poey). During August 1992 and 1994, newly settled S. partitus were collected from Montastraea coral heads and Porites rubble piles in Tague Bay, St. Croix, U.S. Virgin Islands (17 degrees 45'N, 64 degres 42' W). Daily lapillar otolith increments from each fish were counted and measured with Optimas image analysis software. S. partitus pelagic larval duration was 23.7 d in 1992 (n = 70) and 24.6 d in 1994 (n = 38) and larval age at settlement averaged 13.0 mm total length both years. Analysis of daily otolith increments demonstrated that variation in larval growth rates and size and age at settlement had no detectable effect on post-settlement survivorship but that larger larvae showed a preference for Montastraea coral at settlement. Late larval and early juvenile growth rates showed a significant positive relationship indicating that growth patterns established during the planktonic stage can span metamorphosis and continue into the benthic juvenile phase. Larval growth rates during the first two weeks post-hatching also had a strong effect on age to developmental competence (ability to undergo metamorphosis) in both 1992 and 1994 with the fastest growing larvae being 8 d younger and 0.8 mm smaller at settlement than the slowest growing larvae. These differential growth rates in early stage larvae established trajectories toward larval developmental competence and may prove important in biogeographical studies of larval dispersal.     

Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis

The ecological role of parasites in the early life-history stages of coral reef fish is far from clear. Parasitism in larval, recently settled and juvenile stages of a coral reef fish damselfish (Pomacentridae) was therefore investigated by quantifying the ontogenetic change in parasite load and comparing the growth rates of parasitized juvenile fish to those of unparasitized ones. Parasite prevalence in two lunar pulses of Pomacentrus moluccensis was 4 and 0% for larval stage fish, 34 and 56% for recently settled fish and 42 and 49% for juveniles. A significant increase in parasite prevalence with age group was found; the most marked increase occurred immediately after larval fish had settled. Standard length did not model prevalence well; as length is a proxy for age, this indicates that the higher prevalence in recently settled and juvenile fish compared with larvae was not a simple result of parasites accumulating with age. In one of three cohorts, there was some evidence that parasitism affected the growth rate of juveniles, as measured by otolith width. The study suggests that settling on the reef exposes young fish to potentially harmful parasites. This supports the idea that the pelagic phase may have the effect of reducing the exposure of young fish to the debilitating effects of parasites.     

Onset and time course of apoptosis in the developing zebrafish retina

In mammalian development, apoptosis spreads over the retina in consecutive waves and induces a remarkable amount of cell loss. No evidence for such consecutive waves has been revealed in the fish retina so far. As the zebrafish is of growing importance as a model for retinal development and for degenerative retinal diseases, we examined the onset and time course of apoptosis in the developing zebrafish retina and in adult fish. We found that apoptosis peaked in the ganglion cell layer (GCL) and inner nuclear layer (INL) in early developmental stages (3-4 days post-fertilization; dpf) followed by a second, but clearly smaller wave at 6-7dpf. Apoptosis in the outer nuclear layer (ONL) started at 5dpf and peaked at 7dpf. This late-onset high peak of apoptosis of photoreceptors is different from that of all other species examined to date. With 1.09% of cells in the GCL and 1.10% in the ONL being apoptotic, the rate of apoptosis in the developing zebrafish retina was conspicuously lower than that observed in other vertebrates (up to 50% in GCL). During development (2-21dpf), apoptotic waves were most obvious in the central retina, whereas in the periphery near the marginal zone (MZ), apoptosis was much lower; in adult animals, practically no apoptosis was present in the central retina but it still occurred near the MZ. Our data show that the onset and time course of apoptosis in the GCL and INL of the zebrafish is comparable with other vertebrates; however, the amount of apoptosis is clearly reduced. Thus, apoptosis in the zebrafish retina may serve more as a mechanism for the fine tuning of the retinal neuronal network after mitotic waves during development or in remaining mitotic areas than as a mechanism for eliminating large numbers of excess cells.     

Consistency in Context-specific Measures of Shyness and Boldness in Rainbow Trout, Oncorhynchus mykiss

Shyness and boldness has been considered a fundamental axis of human behavioural variation. At the extreme ends of this behavioural continuum subjects vary from being bold and assertive to shy and timid. Analogous patterns of individual variation have been noted in a number of species including fish. There has been debate on the nature of this continuum as to whether it depends on context. That is, whether it is domain‐general (as in humans), or context‐specific. The purpose of our study was to test if shyness and boldness depends on context in rainbow trout, Oncorhynchus mykiss and to this end we estimated boldness in five different situations. Our data provide evidence of a shy–bold behavioural syndrome in rainbow trout. Bold trout tended to be bold in four situations when the context was similar (when the context concerned foraging). However, in a different context, exploring a swim flume, the ranking was entirely different. We suggest that shyness and boldness depends on context in rainbow trout.     

Zebrafish monosex population reveals female dominance in sex determination and earliest events of gonad differentiation

The zebrafish is a popular model for genetic analysis and its sex differentiation has been the focus of attention for breeding purposes. Despite numerous efforts, very little is known about the mechanism of zebrafish sex determination. The lack of discernible sex chromosomes and the difficulty of distinguishing the sex of juvenile fish are two major obstacles that hamper the progress in such studies. To alleviate these problems, we have developed a scheme involving methyltestosterone treatment followed by natural mating to generate fish with predictable sex trait. Female F1 fish that gave rise to all-female offspring were generated. This predictable sex trait enables characterization of gonadal development in juvenile fish by histological examination and gene expression analysis. We found the first sign of zebrafish sex differentiation to be ovarian gonocyte proliferation and differentiation at 10 to 12 days post-fertilization (dpf). Somatic genes were expressed indifferently at 10 to 17 dpf, and then became sexually dimorphic at three weeks. This result indicates clear distinction of male and female gonads derived independently from primordial gonads. We classified the earliest stages of zebrafish sex determination into the initial preparation followed by female germ cell growth, oocyte differentiation, and somatic differentiation. Our genetic selection scheme matches the prediction that female-dominant genetic factors are required to determine zebrafish sex.