Nicholas DiRienzo

Individual- and condition-dependent effects on habitat choice and choosiness

Research on consistent individual differences in behavior, or “behavioral syndromes”, continues to grow rapidly, and yet, the aspects of behavior under consideration have remained remarkably limited. Here, we consider individual variation in consistency of choice (termed here “choosiness”), as expressed during habitat choice. We repeatedly tested the responses of female Western Black Widows, Latrodectus hesperus, to two cues of habitat quality: prey chemical cues and variation in web site illuminance. We estimated females’ response by the distance they positioned themselves from (1) the source of prey chemical cues and (2) the darkest edge of our test arena. Individuals with low variance in their responses are deemed more “choosy”, whereas individuals with high variance are deemed less “choosy”. Generally, most females initiated web construction near the source of the prey chemical cues and tended to place themselves in low-light conditions. However, we detected strong, repeatable differences in females’ intensity of response, and within-individual variance of response (i.e., choosiness) was correlated across situations: females with highly consistent responses towards cricket chemical cues also exhibited highly consistent responses towards variation in light conditions. When deprived of food for extended periods, females were indistinguishable in their responses towards prey chemical cues, but tended to initiate web construction in brighter lighting conditions. Food-deprived females universally exhibited higher variance and diminished consistency in their responses (i.e., they were less choosy). Additionally, higher choosiness was associated with greater mass loss during choice trials, suggesting choosiness is energetically costly. Our results demonstrate that consistency of response to environmental cues is yet another element of behavior that varies among individuals and variation in choosiness could beget speed/quality trade-offs during animal decision making.

Juvenile pathogen exposure affects the presence of personality in adult field crickets

Despite the ever increasing interest in animal personalities, i.e. among-individual variation in behavior, there are still several gaps in our understanding of how experiences during ontogeny influence the expression of behavior in adulthood. Immune challenges during ontogeny have been proposed to drive feedback loops between investment in immune function and personality type. In this study we investigate the effects of an early immune challenge, in the form of an introduced bacterial pathogen, on the development of personality in field crickets. Our results indicate that early pathogen exposure does not influence life history characteristics, immune response, or mean level of boldness behavior. Instead, early immune challenge affects the presence of personality later in the adult stage. Specifically, immune challenged individuals lack repeatability in some aspects of boldness behavior, indicating that among-individual variation is not present, while non-immune challenged individuals remain repeatable in their boldness behavior. This study joins a slowly growing body of literature indicating that experiences during ontogeny can have large influences on the among-individual differences in behaviors, thus affecting the presence of personality as adults.

The contribution of developmental experience vs. condition to life history, trait variation and individual differences.

1. Developmental experience, for example food abundance during juvenile stages, is known to affect life history and behaviour. However, the life history and behavioural consequences of developmental experience have rarely been studied in concert. As a result, it is still unclear whether developmental experience affects behaviour through changes in life history, or independently of it. 2. The effect of developmental experience on life history and behaviour may also be masked or affected by individual condition during adulthood. Thus, it is critical to tease apart the effects of developmental experience and current individual condition on life history and behaviour. 3. In this study, we manipulated food abundance during development in the western black widow spider, Latrodectus hesperus, by rearing spiders on either a restricted or ad lib diet. We separated developmental from condition-dependent effects by assaying adult foraging behaviour (tendency to attack prey and to stay on out of the refuge following an attack) and web structure multiple times under different levels of satiation following different developmental treatments. 4. Spiders reared under food restriction matured slower and at a smaller size than spiders reared in ad lib conditions. Spiders reared on a restricted diet were more aggressive towards prey and built webs structured for prey capture, while spiders reared on an ad lib diet were less aggressive and built safer webs. Developmental treatment affected which traits were plastic as adults: restricted spiders built safer webs when their adult condition increased, while ad lib spiders reduced their aggression when their adult condition increased. The amount of individual variation in behaviour and web structure varied with developmental treatment. Spiders reared on a restricted diet exhibited consistent variation in all aspects of foraging behaviour and web structure, while spiders reared on an ad lib diet exhibited consistent individual variation in aggression and web weight only. 5. Developmental experience affected the average life history, behaviour and web structure of spiders, but also shaped the amount of phenotypic variation observed among individuals. Surprisingly, developmental experience also determined the particular way in which individuals plastically adjusted their behaviour and web structure to changes in adult condition.

Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders

Variation in state, which is any factor that alters the value of decision options, is likely one of the most common drivers of personality differences. However, the general relationship between individuals’ body state and various personality metrics/average behavioral type, repeatability of behavior, and behavioral syndrome structure is still poorly resolved. Here, we manipulate body condition in three spider species (Agelenopsis aperta, Latrodectus hesperus, and Anelosimus studiosus) using contrasting feeding schedules. We then assessed the effects of historic feeding regime on individuals’ body condition, boldness, and foraging aggressiveness. We further assessed the effects of feeding regimes on the repeatability of boldness and aggressiveness and the presence/absence of correlations between these two traits. We found that feeding treatment impacted individuals’ average boldness and aggressiveness in two species (A. aperta and A. studiosus). We also noted that among-individual variance in both boldness and aggressiveness was severely reduced when A. aperta and A. studiosus were subjected to prolonged food restriction, steeply reducing repeatability in these traits. Finally, we noted that correlations between boldness and foraging aggressiveness were detectable only in one case, revealing no compelling relationship between food restriction and the presence/absence of behavioral correlations. Taken together, our results suggest that food restriction has only weak, circumstantial effects on individuals’ average personality type and the correlations between behavioral traits. However, there appears to be a robust positive relationship between food availability and the signature of consistent individual differences in behavior.Significance statementUnder laboratory conditions, we found that lower feeding rates sharply decreased the repeatability of aggressiveness and boldness in two spider species. In doing so, we provide the second body of evidence suggesting that a highly prevalent and ecologically relevant state variable, higher body condition, can increase the repeatability of foraging-related behavioral traits. Additionally, under some feeding regimes, we found that hunger levels could alter the average individual aggressiveness and boldness but not correlations between these traits. This work highlights the importance of state variables such as hunger in eroding behavioral repeatability, the defining trait of personality.

Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets

Among-individual differences in behavior are now a widely studied research focus within the field of behavioral ecology. Furthermore, elements of an animal’s internal state, such as energy or fat reserves, and infection status can have large impacts on behaviors. Despite this, we still know little regarding how state may affect the expression of behavioral variation. Recent exposure to pathogens may have a particularly large impact on behavioral expression given that it likely activates costly immune pathways, potentially forcing organisms to make behavioral tradeoffs. In this study, we investigate how recent exposure to a common bacterial pathogen, Serratia marcescens, affects both the mean behavioral expression and the among-individual differences (i.e., variation) in boldness behavior in the field cricket, Gryllus integer. We find that recent pathogen exposure does not affect mean behavioral expression of the treatment groups, but instead affects behavioral variation and repeatability. Specifically, bacterial exposure drove large among-individual variation, resulting in high levels of repeatability in some aspects of boldness (willingness to emerge into a novel environment), but not others (latency to become active in novel environment), compared to non-infected crickets. Interestingly, sham injection resulted in a universal lack of among-individual differences. Our results highlight the sensitivity of among-individual variance and repeatability estimates to ecological and environmental factors that individuals face throughout their lives.Significance statementAnimals are known to express consistent among-individual differences in behavior, also known as animal personalities, such that some individuals are always more bold, aggressive, or active relative to others. Yet it is relatively unknown how factors such as energy reserves and exposure to pathogens impact these differences in behavior. Here we investigated how exposure to a pathogenic bacteria as adults affects both the mean behavioral expression and the among-individual differences. Our results show that pathogen exposure results in large levels of among-individual differences in some aspects of boldness behavior (willingness to expose oneself to risk), but not others (latency to become active in a novel environment). These results highlight the sensitivity of behavioral differences to elements of state, such as infection status.

Noncompetitive Gametic Isolation between Sibling Species of Cricket: A Hypothesized Link between Within-Population Incompatibility and Reproductive Isolation between Species.

Postmating, prezygotic phenotypes are a common mechanism of reproductive isolation. Here, we describe the dynamics of a noncompetitive gametic isolation phenotype (namely, the ability of a male to induce a female to lay eggs) in a group of recently diverged crickets that are primarily isolated from each other by this phenotype. We not only show that heterospecific males are less able to induce females to lay eggs but that there are male by female incompatibilities in this phenotype that occur within populations. We also identify a protein in the female reproductive tract that correlates with the number of eggs that she was induced to lay. Functional genetic tests using RNAi confirm that the function of this protein is linked to egg-laying induction. Moreover, the dysfunction of this protein appears to underlie both within-population incompatibilities and between-species divergence—thus suggesting a common genetic pathway underlies both. However, this is only correlative evidence and further research is needed to assess whether or not the same mutations in the same genes underlie variation at both levels.

Behavioural hypervolumes of spider communities predict community performance and disbandment

Trait-based ecology argues that an understanding of the traits of interactors can enhance the predictability of ecological outcomes. We examine here whether the multidimensional behavioural-trait diversity of communities influences community performance and stability in situ. We created experimental communities of web-building spiders, each with an identical species composition. Communities contained one individual of each of five different species. Prior to establishing these communities in the field, we examined three behavioural traits for each individual spider. These behavioural measures allowed us to estimate community-wide behavioural diversity, as inferred by the multidimensional behavioural volume occupied by the entire community. Communities that occupied a larger region of behavioural-trait space (i.e. where spiders differed more from each other behaviourally) gained more mass and were less likely to disband. Thus, there is a community-wide benefit to multidimensional behavioural diversity in this system that might translate to other multispecies assemblages.

Temnothorax rugatulus ant colonies consistently vary in nest structure across time and context

A host of animals build architectural constructions. Such constructions frequently vary with environmental and individual/colony conditions, and their architecture directly influences behavior and fitness. The nests of ant colonies drive and enable many of their collective behaviors, and as such are part of their ‘extended phenotype’. Since ant colonies have been recently shown to differ in behavior and life history strategy, we ask whether colonies differ in another trait: the architecture of the constructions they create. We allowed Temnothorax rugatulus rock ants, who create nests by building walls within narrow rock gaps, to repeatedly build nest walls in a fixed crevice but under two environmental conditions. We find that colonies consistently differ in their architecture across environments and over nest building events. Colony identity explained 12–40% of the variation in nest architecture, while colony properties and environmental conditions explained 5–20%, as indicated by the condition and marginal R2 values. When their nest boxes were covered, which produced higher humidity and lower airflow, colonies built thicker, longer, and heavier walls. Colonies also built more robust walls when they had more brood, suggesting a protective function of wall thickness. This is, to our knowledge, the first study to explicitly investigate the repeatability of nestbuilding behavior in a controlled environment. Our results suggest that colonies may face tradeoffs, perhaps between factors such as active vs. passive nest defense, and that selection may act on individual construction rules as a mechanisms to mediate colony-level behavior.

Plasticity in extended phenotype increases offspring defence despite individual variation in web structure and behaviour

Many animals actively defend their offspring using a range of behaviours from calling and mobbing in birds, to physical grappling in crustaceans, and the expression of these behaviours positively scale with offspring value. While this role of behaviour in defence is well studied, very little is known about how other traits, specifically the structure of architectural constructions such as webs and nests, contribute to offspring defence. Additionally, although some tax a show consistent individual differences in offspring defence behaviour, it is completely unknown whether individuals also differ in defensive structures. We addressed these questions in the redback spider, Latrodectus hasselti, by measuring how a female laying an eggcase influences female behaviour and web structure, and whether those traits scale with relative reproductive investment. Our results show that females modified web structure in response to an eggcase, but only the protective elements of web structure positively scaled with the relative value of that eggcase. Finally, despite the significant correlations, fixed effects (e.g. eggcase possession/value) in the models explained only 5–23% of the variation in behaviour and web structure, while the random effect of individual identity explained 46–65% of the variation. This variation drove moderate to high repeatability estimates across all traits, suggesting that some individuals consistently invest relatively more in defence, while some invest less. These results highlight that extended phenotypic traits may be a critical component of offspring defence in some taxa. Furthermore, individual variation in these traits suggest that different reproductive strategies may exist, whereby some individuals invest more in reproduction at a cost to safety/foraging and vice versa.

Individual differences are consistent across changes in mating status and mediated by biogenic amines

Although aspects of an individual’s state are well-known to influence the expression of behavior, it is still unclear how elements of state affect consistent among-individual differences in behavior. With binary, irreversible elements of state, such as mating status, there may be optimal behavioral phenotypes before and after mating, with individuals often prioritizing mate acquisition before and resource acquisition after. Yet, limited plasticity may prevent optimal behavior in both contexts. Additionally, it remains largely unknown if some consistencies in neural or physiological traits may limit the ability of the organism to respond to state changes. In this study, we investigated how changes in a binary state variable, mating status, affected both the mean expression and among-individual variation in behavior and web structure of the redback spider, Latrodectus hasselti. Furthermore, we explored the role of biogenic amines in potentially mediating individual differences in behavior and web structure. We found that mated females were overall more aggressive than virgin females and also built webs structured primarily for capturing prey rather than safety. We also found that individual differences in behavior and web structure were maintained across mating statuses, which indicates the stability of these traits and may drive personality-specific state-dependent fitness trade-offs. Finally, we found that aggressive spiders had higher central nervous system dopamine levels. Interestingly, web structure was often correlated with a catabolite of tyramine (N-acetyltyramine), suggesting that variation in amine catabolism, and not the concentrations of the amines themselves, may drive individual differences in some traits.Significance statementOur results demonstrate that although individuals show plasticity in response to changes in state, specifically mating status, individuals also maintain among-individual differences across this state change. Thus, aggressive individuals before mating will tend to be aggressive after. This maintenance of individual differences across state may drive differential fitness benefits before and after mating for different behavioral phenotypes. Furthermore, we show that biogenic amines and their catabolites are related to individual differences, thus identifying a potential mechanism underlying consistent variation.