Inon Scharf

Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences

Same-sex sexual (SSS) behavior represents an evolutionary puzzle: whilst associated costs seem obvious, positive contributions to fitness remain unclear. Various adaptive explanations have been proposed and thorough reviews exist for vertebrates, but a thorough synthesis of causes for SSS behavior in invertebrates is lacking. Here we provide evidence for such behavior in ~110 species of insects and arachnids. Males are more frequently involved in SSS behavior in the laboratory than in the field, and isolation, high density, and exposure to female pheromones increase its prevalence. SSS behavior is often shorter than the equivalent heterosexual behavior. Most cases can be explained via mistaken identification by the active (courting/mounting) male. Adaptive explanations, such as sperm transfer of the mounting male via the mounted one or gaining experience by young males, are of limited general significance. The passive (being courted/mounted) male is sometimes responsible for this “mistake” by releasing sex pheromones or carrying female pheromones that were attached to his cuticle during prior mating activity. Passive males often resist courting/mating attempts. SSS behavior in arthropods is predominantly based on mistaken identification and is probably maintained because the cost of rejecting a valid opportunity to mate with a female is greater than that of mistakenly mating with a male. Many species exhibiting SSS behavior also mate with related species, another case of mistaken identification. Future research should focus on uncovering the situations/contexts in which mistaken identification is more or less costly for males.

Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging

Behavioral repeatability is an important trait relevant to personality research and to behavioral ecology in general. We examined here the behavioral repeatability of two activity-related traits: movement and edge preference (proportion of time spent next to the test arena edge). We used the red flour beetle as our test species in order to determine whether repeatability changes throughout metamorphosis and aging and whether there are inter-sexual differences. Young adults moved more than larvae, but movement activity generally declined with age. Behavioral repeatability was high between two successive measurements for larvae and young adults, but did not persist through metamorphosis. These findings support most of the previous studies on insects and probably reflect the occurrence of phenotypic reorganization during metamorphosis. Neither of our predictions of an increase in behavioral repeatability throughout aging and of a higher repeatability of young adults than larvae held true, as repeatability levels estimates remained similar across ontogeny and aging. Similar to other studies on repeatability, estimates declined with the time interval between two pairs of measurements, suggesting an episodic physiological basis for the documented behaviors. Finally, we detected several inter-sexual differences. Females were more active than males and expressed a shallower decline in movement with aging. Female movement activity was also more repeatable, but female edge preference was less repeatable than that of males. We reason that such differences in repeatability may be driven by sex-specific selection pressures on behavioral tendencies.Significance statementWe investigate several questions regarding behavioral repeatability in insects. The two main questions asked are (1) whether inter-individual behavioral differences remain consistent across larvae and adult stage, and (2) how repeatability changes throughout aging. The first question has been only rarely tested in insects that undergo a full metamorphosis. It has been recognized as a timely question and as an opportunity for researchers studying animal personality. Previous results regarding amphibians and insects that undergo partial metamorphosis were inconclusive. The second question is important, because studies rarely follow individuals throughout their lives. This is essential to understand the consequences of aging. We also report on differences between males and females, probably indicating on differences in motivation for activity and in patterns of aging. Finally, the question, how behavior changes with ontogeny, has been already recognized by Tinbergen as a basic one in animal behavior.

Foraging behaviour of a neglected pit-building predator: the wormlion

Wormlion larvae (Diptera: Vermileonidae) construct conical pits in fine loose soils and ambush arthropod prey. Their hunting strategy resembles that of pit-building antlions (Neuroptera: Myrmeleontidae), offering a classical example of convergent evolution, as they belong to different orders of insects. However, compared with other trap-building predators, spiders and antlions, the foraging behaviour of wormlions is almost unknown. In this study we used a combination of field observations and laboratory experiments to close this gap and investigate how hunger and ecological factors such as density and spatial pattern affect pit size, that is, how they shape investment in foraging and indicate competition between neighbouring larvae. We found slight, mainly decreasing, changes in pit size with hunger, with no change in response to prey. Surprisingly, body mass and length were not tightly correlated with pit size, unlike in antlions and spiders. Other factors, in addition to body mass and size, affect pit size, as the correlation between pits constructed in the field and in the laboratory was strong. The evidence for competition was mixed. On the one hand, we detected, in the laboratory, a change towards a regular spatial pattern with increasing pit densities, as expected, suggesting interference competition. On the other hand, we detected, in the field, a positive correlation between the sizes of neighbouring pits, and a negative correlation in the laboratory between pit size and distance to the nearest neighbour, both indicating clustering in favourable microhabitats, and not supporting strong competition. We discuss our findings in comparison with other trap-building predators and locate them within the general framework of foraging theory.

Disentangling the Consequences of Growth Temperature and Adult Acclimation Temperature on Starvation and Thermal Tolerance in the Red Flour Beetle

Temperature affects most aspects of animal life, and impacts particularly strongly on ectotherms. We studied the combined effects of growth temperature and adult acclimation temperature on starvation tolerance, cold tolerance, and heat tolerance in the red flour beetle. A lower adult acclimation temperature enhanced starvation tolerance and cold tolerance and impaired heat tolerance. This is an expected outcome of short-term plasticity and of the beneficial acclimation hypothesis. The higher growth temperature led to improved performance of all three measured traits: beetles raised under higher temperature tolerated starvation longer and showed better cold and heat tolerance. While this result fits well the rule “hotter is better”, it is nonetheless surprising that the same temperature had opposite effects when experienced by juveniles and adults (i.e., the effect of the warm temperature on cold tolerance). We emphasize the importance of separating between the juvenile growth temperature (developmental plasticity) and adult temperature (acclimation), as they can have opposite effects on adult performance.

The role of per-capita productivity in the evolution of small colony sizes in ants

The evolution of colony size in social insects is influenced by both extrinsic and colony-intrinsic factors. An important intrinsic trait, per-capita productivity, often declines in larger colonies. This pattern, known as Michener’s paradox, can limit the growth of insect societies. In this study, we first describe this problem, survey its occurrence across different ant species, and present a case study of eight cavity-dwelling ants with very small colony sizes. In these species, colonies might never reach sizes at which per-capita productivity decreases. However, in six out of the eight focal species, per-capita productivity did decline with increasing size, in accordance with other studies on per-capita productivity in ants. Several mechanisms, such as resource availability or nest-site limitation, may explain the decrease in per-capita productivity with increases in colony size in our focal species. In these central-place foragers, the individual foraging mode is expected to lead to an increase in travel time as colonies grow. We suggest that polydomy, the concomitant occupation of several nest sites, could serve as a potential strategy to overcome this limitation. Indeed, for one species, we show that polydomy can help to circumvent the reduction in productivity with increasing colony size, suggesting that limited resource availability causes the observed decrease in per-capita productivity. Finally, we discuss the influence of other factors, such as the nesting ecology and colony homeostasis, on the evolution of colony size in these cavity-dwelling ants.

Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae

Social interactions in animal groups can buffer environmental stress and may enhance survival under unfavourable conditions. In the present study, the impact on starvation endurance of social group, access to larvae and cold shock is studied in the ant Temnothorax nylanderi Förster. Resource sharing is expected to lead to grouped workers surviving longer than isolated ones. Access to larvae may increase longevity if larvae serve as food, or may interfere with survival if they induce caring behaviour in workers. Cold shock serves as a stress factor and a negative influence on survival is expected. The results show that isolated workers have a shorter lifespan than grouped workers, which in turn live for a shorter period than grouped workers with larvae. Beneficial ‘group effects’ contribute to group survival and the presence of larvae increases worker survival because the workers presumably feed on the larvae. Thus, improved starvation endurance may reflect an additional benefit of a social lifestyle. Moreover, variance in survival is lower for grouped workers than for isolated workers: group members not only demonstrate improved survival, but also smaller within‐group differences. Although a negative influence on survival is the expected outcome, this type of thermal stress is found to have no direct impact on starvation endurance other than moderating the differences between isolated and grouped workers.

Cold resistance depends on acclimation and behavioral caste in a temperate ant

Adjusting to low temperatures is important for animals living in cold environments. We studied the chill–coma recovery time in temperate ant workers (Temnothorax nylanderi) from colonies collected in autumn and spring in Germany. We experimentally acclimated these ant colonies to cold temperatures followed by warm temperatures. As expected, cold-acclimated workers recovered faster from freezing temperatures, but subsequent heat acclimation did not change the short recovery times observed after cold acclimation. Hence, either heat acclimation improves cold tolerance, possibly as a general response to stress, or at least it does not negate enhanced cold tolerance following cold acclimation. Colonies collected in spring showed similar cold tolerance levels to cold-acclimated colonies in the laboratory. Next, we compared the chill–coma recovery time of different worker castes and found that exterior workers recovered faster than interior workers. This difference may be related to their more frequent exposure to cold, higher activity level, or distinct physiology. Interior workers were also heavier and showed a higher gaster-to-head ratio and thorax ratio compared to exterior workers. An obvious difference between exterior and interior workers is activity level, but we found no link between activity and cold tolerance. This suggests that physiology rather than behavioral differences could cause the increased cold tolerance of exterior workers. Our study reveals the importance of acclimation for cold tolerance under natural and standardized conditions and demonstrates differences in cold tolerance and body dimensions in monomorphic behavioral castes of an ant.

The Effects of Temperature and Diet during Development, Adulthood, and Mating on Reproduction in the Red Flour Beetle

The effects of different temperatures and diets experienced during distinct life stages are not necessarily similar. The silver-spoon hypothesis predicts that developing under favorable conditions will always lead to better performing adults under all adult conditions. The environment-matching hypothesis suggests that a match between developmental and adult conditions will lead to the best performing adults. Similar to the latter hypothesis, the beneficial-acclimation hypothesis suggests that either developing or acclimating as adults to the test temperature will improve later performance under such temperature. We disentangled here between the effect of growth, adult, and mating conditions (temperature and diet) on reproduction in the red flour beetle (Tribolium castaneum), in reference to the reproduction success rate, the number of viable offspring produced, and the mean offspring mass 13 days after mating. The most influential stage affecting reproduction differed between the diet and temperature experiments: adult temperature vs. parental growth diet. Generally, a yeast-rich diet or warmer temperature improved reproduction, supporting the silver-spoon hypothesis. However, interactions between life stages made the results more complex, also fitting the environment-matching hypothesis. Warm growth temperature positively affected reproduction success, but only when adults were kept under the same warm temperature. When the parental growth and adult diets matched, the mean offspring mass was greater than in a mismatch between the two. Additionally, a match between warm adult temperature and warm offspring growth temperature led to the largest offspring mass. These findings support the environment-matching hypothesis. Our results provide evidence for all these hypotheses and demonstrate that parental effects and plasticity may be induced by temperature and diet.

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.

Consequences of the instar stage for behavior in a pit-building antlion

Pit-building antlion larvae are opportunistic predators that dig conical pits in loose soils, and prey on small arthropods that fall into their traps. We investigated different behavioral traits of second and third instar larvae selected for similar body masses, while also exploring the behavioral consistency and personalities of the third instar stage. Second instar larvae constructed smaller pits than third instar larvae. The former also responded more slowly to prey and exploited prey less efficiently. Notably, all these instar-based differences disappeared after molting into the third instar stage. In addition, third instar larvae exhibited consistent behavior in their pit size, response times to prey and to less extent in relocation distances. We detected two axes of behavior. The first axis included a correlation between pit size, response time and prey exploitation efficiency, thus reflecting investment in foraging activity. The second axis seemed to represent a trade-off between response time and relocation distance, implying that individuals that responded more slowly to prey, relocated over larger distances. These results point to coordinated behavior reflecting different levels of investment in foraging, while also emphasizing the importance of instar stage, in addition to body mass, when studying the behavior of such organisms characterized by a complex life cycle.