Behavioral Ecology and Sociobiology最新文献

Reciprocity allows animals to balance the costs and benefits of cooperative interactions by switching roles over time. Reciprocity can be based on two different processes: a within-dyad process based on temporal relations between cooperative events (partner control) and an across-dyad process based on preferences for the most cooperative partners (partner choice). The relative roles of the two processes remain debated. The aim of our study was to assess how the opportunity of interaction modulates grooming reciprocity in wild Geoffroy’s spider monkeys (Ateles geoffroyi), a species with low grooming rates and variable opportunities for group members to interact due to a high degree of fission-fusion dynamics. We investigated the roles of the aforementioned processes in grooming reciprocity, and the factors affecting them. Receiving grooming increased the probability of immediately returning grooming to the same partner (within-dyad temporal relations between cooperative events). In contrast, we found no evidence that spider monkeys directed most of their grooming to those individuals from which they received most grooming during the entire study period (across-dyad preferences for the most cooperative partners). The probability of returning grooming to the same partner was higher for dyads that spent less time together in the same subgroup, but was unaffected by maternal kinship. Our results suggest the opportunity to interact is a potent modulator of reciprocity. In species characterized by a high degree of fission-fusion dynamics and low grooming rates, short-term reciprocation based on partner control can be favored at the expense of a longer-term process based on partner choice.

Abstract

The parasite-mediated sexual selection hypothesis predicts that color expression in color patches of animals can honestly reflect male quality in terms of resistance to parasites. Sceloporine lizards have structural-based blue color patches that can act as intraspecific signals and may thus reflect immunocompetence. However, both color patch expression and intensity of parasitic infections in lizards can vary across seasons. In consequence, we might expect that coloration would honestly reflect immunocompetence to resist parasites only during the mating season. We sampled males of Sceloporus torquatus in central Mexico in spring, summer, and autumn and quantified the reflectance of two structural-based color patches (throat and venter), abundance of two categories of parasites (mites and hemoparasites), and lizards’ local inflammatory response to a mitogen (IRM) as a measure of immunocompetence. We examined whether (i) the coloration of lizards changed across seasons in the population, (ii) there is a relationship between coloration and parasite load and/or IRM, and (iii) the latter relationships remained consistent across seasons. Our study shows that color expression seasonally varied; the structural-based coloration of the two patches was significantly more intense in summer, before the mating season. Furthermore, the throat color was more intense in those males with lower parasite load and higher IRM. However, season had no effect on these relationships, suggesting that color expression in the males of S. torquatus can consistently reflect some components of their immunocompetence throughout the year, supporting the honesty of the structural-based coloration in this species.

Significance statement

In this study, we aimed to investigate the seasonal variation in structural coloration of a lizard species and its potential relationship with male quality in Torquate lizards (Sceloporus torquatus). Our results revealed distinct seasonal differences in color expression, and furthermore, we found that males displaying more intense blue coloration exhibited lower parasite loads and stronger immune responses. These findings contribute to our understanding of two key aspects: (i) the potential role of structural coloration as an honest signal in organisms of this nature, and (ii) the significance of considering sampling times in organisms with structural coloration, as it can vary throughout the year.

Abstract

Darwin’s finch species in the Galápagos Islands are famously distinguished by their morphology but less attention has been given to behavioral differences between species. In this study, we compared behavior between four Darwin’s finch species on Floreana Island: small ground finch (Geospiza fuliginosa), medium ground finch (G. fortis), small tree finch (Camarhynchus parvulus), and medium tree finch (C. pauper). After capturing birds using mist-nets, we measured three behavioral traits: (1) boldness during human handling, (2) exploration in a novel environment, and (3) aggressiveness towards their mirror image. First, we found that ground finches were bolder and more exploratory than tree finches, consistent with their distinct ecological niches on Floreana Island and with the theoretical prediction that diet generalists should be less wary of novelty. Second, we tested the ecological validity of these behavioral variables at the individual level by relating them to territory defense behavior and breeding success. We found that males that were more exploratory in the novel environment also reacted more aggressively to a simulated territory intruder and showed lower offspring hatching success during the breeding season. Hence, our findings support previous work showing behavioral differences between Darwin’s finch species and also suggest pathways by which behavioral differences among individuals might influence fitness.

Significance statement

Closely-related species that overlap in their geographical range may differ in their morphology and/or behavior, allowing them to occupy different ecological niches. In this study, we explored behavioral differences between four Darwin’s finch species on Floreana Island in the Galápagos Archipelago. We found clear interspecies differences in behavior, with the ground finches struggling more often during handling (boldness) and visiting more sectors in a novel environment (exploration) compared to the tree finches. After birds were released, we continued to observe a subset of male finches in the wild. An individual’s exploration behavior significantly predicted both its aggressive response to a territory intruder (simulated using song playback) and offspring hatching success during the breeding season. This suggests that individual differences in exploration behavior can potentially be used as a proxy for territorial behavior in the wild and may also predict fitness outcomes.

Abstract

Bees of Ptiloglossa and Xylocopa explore the chiropterophilous flowers of Pseudobombax longiflorum at twilight, but how the bees find the flowers in low light is unclear. In field experiments, we investigated if visual and olfactory floral cues are used by these bees to find P. longiflorum flowers, and which behaviors are triggered by these cues. While the crepuscular Ptiloglossa bees were more attracted to flowers with a combination of visual and olfactory cues than to isolated cues, the diurnal Xylocopa bees were equally attracted to the combination of visual and olfactory cues and to flowers with visual cues alone. Ptiloglossa bees visit the flowers under lower light intensity than Xylocopa bees. This indicates that the synergy between visual-olfactory cues facilitates flower detection in crepuscular bees. However, in higher light intensities, the large size of flowers with their broad spectrum reflectance may be enough to produce a reliable visual signal for the Xylocopa bees. Olfactory stimuli alone trigger only floral approaches in bees, while visual ones frequently trigger approaches followed by landings on flowers. This suggests that olfactory cues guide the bees to the flowers in twilight, but the presence of a visual cue is necessary to trigger landings and collection of floral resources.

Significance statement

Crepuscular and some large diurnal bees fly in the twilight and collect pollen and nectar from flowers with nocturnal anthesis. However, finding food in a dimly lit environment is not an easy task! In this study, we used a combination of visual and chemical approaches to describe, for the first time, how bees do it. We showed that although bees use olfactory and visual floral stimuli as cues, they have different strategies for finding flowers. Furthermore, olfactory and visual cues play different roles during bee foraging. Floral odors are responsible for guiding bees toward flowers in the dark, and the visual cues are responsible not only for guiding bees but also for triggering landings and floral resource collection.

Abstract

Female mate choice is usually based on traits that signal male quality as a sexual partner. According to the “good parent” hypothesis, female mate choice may also consider male quality as a caregiver in species with male-only care. Because parental activities may be costly, males in good condition should be more attractive to females than those in poor condition. We experimentally manipulated the body condition of non-parental and parental males of the egg-tending harvestman Iporangaia pustulosa and then evaluated how it affected their mating success and ability to protect eggs under field conditions. For non-parental males, individuals in good condition had twice the probability of mating than those in poor condition. For parental males, individuals in good condition had two times more chances of mating and acquired five times more eggs than those in poor condition. Surprisingly, males’ body condition had no effect on the efficiency of egg protection. Although our results indicate that the male condition is a sexually selected trait, we found no support for the “good parent hypothesis” given that an increase in body condition does not improve the survival of the offspring under male care. Instead, these findings are congruent with predictions of the “essential male care” model, which suggests that, when the costs of parental care are low (as is the case of egg attendance), most males can provide the minimum necessary care for offspring survival. However, only males in good condition can allocate surplus energy to advertise their overall quality and attract more mates.

Significance statement

Studies examining female mate choice based on condition-dependent traits that serve as reliable indicators of male caregiving quality are mostly limited to vertebrates. We present one of the first empirical examples demonstrating that male body condition influences male attractiveness in an arthropod species exhibiting male-only care. Our field-based results show that females prefer males, whether non-parental or parental, in good body condition over those in poor condition. However, we found no evidence that an increase in body condition improves the survival of the offspring under male care. We propose that males in good body condition are more attractive because the relatively low costs of egg attendance allow them to allocate their surplus energy into advertising their overall quality. Our findings are congruent with predictions of the “essential male care” model, which explores resource allocation between paternal care and sexual advertising.

Abstract

Mutualistic relationships confer selective advantages to interacting species through enhanced ecological benefits but may be functionally limited to certain life history stages. However, it is not yet known whether one party can indirectly benefit from risky cues released when the other party is threatened. Larval glochidia of the Chinese pond mussel (Anodonta woodiana) attach to fishes including the rosy bitterling (Rhodeus ocellatus) for dispersal, while reproductive-phase bitterling use the gills of adult mussels as spawning substrate, and their larvae remain inside the host mussel shells until they are capable of swimming. Here, we examined heterospecific responses to risky chemical cues by rosy bitterling as an indirect indicator of species affinity consistent with mutualism at different life history stages, to test for age-dependent response patterns indicating temporal patterning of shared predation risk. Bitterling demonstrated equivocal but similar responses to water controls and mussel odor and significant antipredator responses to bitterling chemical alarm cues (CAC) independent of life stage, while only reproductive adult bitterling demonstrated significant antipredator responses to mussel CAC. These findings suggest that the mutualistic affinity to mussels present in reproductive-phase adult rosy bitterling may result in shared predation risk and therefore provide them with additional indirect antipredator benefits. Our results revealed a life history stage-dependent mutualism in this bitterling-mussel system and describe a novel application of predation risk assays for studying temporal patterning in mutualistic relationships.

Significance statement

Interspecific interactions, including mutualisms, are a central component of community composition. Some freshwater fishes, including the rosy bitterling, and mussels share an interesting mutualism where each species provides early life habitat to the other. However, does mutualism provide additional indirect benefits? Here, we used responses to conspecific and Chinese pond mussel chemical cues in different life stages of bitterling to identify the occurrence of mutualistic behaviors. We demonstrated that the putative occurrence of mutualistic behaviors in rosy bitterling is not consistent over time and instead varies predictably with reproductive status of different life history stages. This study provides a novel perspective for a deeper understanding of labile interspecific relationships and provides a theoretical basis for indirectly examining mutualisms through chemical communication-based behavioral assays.

Abstract

Conspicuous coloration is often seen as the evolutionary consequence of either sexual selection or warning predators visually about prey defences, although not all conspicuous species fit this paradigm. Exceptions include several species of colobus monkeys whose black-and-white coloration, characteristic of larger colobines, has never been explained. Here, using photographs of black-and-white colobus (Colobus vellerosus) taken in the wild, quantitative image analysis, and vision modelling (acuity-corrected feline, chimpanzee, and raptor vision), we provide evidence that their coloration provides distance-dependent camouflage in natural forest environments. At all viewing distances, black-and-white colobus monkeys blend into their environment because of their high chromatic overlap with the background when viewed by ecologically relevant predator vision models which have low visual acuities. Additionally, for chimpanzee and felid vision, there was evidence of edge disruption at longer viewing distances. Our comparative analyses of different species of colobines do not support an association between black-and-white coloration and larger body mass or group size, but this may simply be due to the limited number of species within the family. We reason that black-and-white colobines gain visually protective coloration through background matching against felids, and also benefit through disruptive coloration against felids and chimpanzees but rely on these protective coloration mechanisms less against raptors.

Significance statement

Conspicuous black-and-white coloration in colobus monkeys has long eluded an evolutionary explanation. Our research, employing photographs of colobus monkeys, image analysis, and vision modelling, unveils a novel approach to this coloration. We show that in their natural forest habitats, black-and-white colobus monkeys employ distance-dependent camouflage against ecologically relevant predators with low visual acuity, blending in with the background at increasing viewing distances. In summary, the evolution of black-and-white colobus coloration appears to be related to background matching against felids, with added benefits of disruptive camouflage against felids and chimpanzees, less so to raptors, offering fresh insights into the complex interplay of coloration and survival strategies in mammals.

Abstract

Insurance-based mechanisms, where surviving group-members can complete parental care after the death of a nestmate, are key to the origin of cooperative group formation in insects. Selection for group living via these models is proposed to be dependent on the life expectancy of adult carers relative to the duration of offspring dependency on parental care. Progressive provisioning, where adults feed offspring gradually as they grow, is thought to extend this period of dependency and is therefore suggested to be an important factor promoting the evolution of sociality. In contrast, mass-provisioning species provide offspring with all the food they need to reach maturity at the beginning of their development. Since offspring are then nutritionally independent, the applicability of insurance models is less clear. In this paper we experimentally demonstrate that adult presence on the nest, even after the end of provisioning, is critical for brood survival in the mass provisioning silk wasp Microstigmus rosae. After 10 days, experimentally orphaned nests contained 65% fewer healthy offspring than controls. Adult females were also recorded performing post-provisioning parental care behaviours including nest maintenance and repair, putative hygienic brood care and aggressive nest defence against both ants and parasitoid wasps. By demonstrating the potential applicability of insurance advantages our results highlight how, even in mass provisioners, insurance-based mechanisms may be part of what favours group living.

Significance statement

Extended parental care is an important precursor to the evolution of eusociality. In this context, group living can serve as a form of “life insurance”, ensuring that dependent offspring receive the care they need to reach maturity should the mother die. Such mechanisms are especially important to our understanding of social evolution as they are able to account for the origins of cooperative group formation, not just its maintenance. However, for mass-provisioning species, where all food items are provided upfront, the significance of insurance advantages remains unclear. In this study, we experimentally demonstrate that adult attendance is critical for brood survival in the mass provisioning wasp, Microstigmus rosae. Our results reveal the applicability of insurance advantages to M. rosae with important implications for our understanding of the potential adaptive value of group living in mass provisioning species.

Abstract

The estimation of heritability is a common practice in the field of ecology and evolution. Heritability of the traits is often estimated using one single measurement per individual, although many traits (especially behavioural and physiological traits) are characterized by large within-individual variance, and ideally a large number of within individual measurements can be obtained. Importantly, the effect of the within-individual variance and the rate at which this variance is sampled on the estimation of heritability has not been thoroughly tested. We fill this gap of knowledge with a simulation study, and assess the effect of within- and between-individual sample size, and the true value of the variance components on the estimation of heritability. In line with previous studies we found that the accuracy and precision of heritability estimation increased with sample size and accuracy with higher values of additive genetic variance. When the sample size was above 500 accuracy and power of heritability estimates increased in the models including repeated measurements, especially when within-individual variance was high. We thus suggest to use a sample of more than 100 individuals and to include more than two repeated measurements per individual in the models to improve estimation when investigating heritability of labile traits.

Significance statement

Heritability reflects the part of the trait’s phenotypic variation underlined by genetic variation. Despite the difficulties of heritability calculation (high number of individuals is needed with known relatedness), it is a widely used measure in evolutionary studies. However, not every factor potentially affecting the quality of heritability estimation is well understood. We thus investigated with a comprehensive simulation study how the number of repeated measurements per individuals and the amount of within-individual variation influence the goodness of heritability estimation. We found that although the previously described effect of the number of studied individuals was the most important, including repeated measurements also improved the reliability of the heritability estimates, especially when within-individual variation was high. Our results thus highlight the importance of including repeated measurements when investigating the heritability of highly plastic traits, such as behavioural or physiological traits.

Abstract

While there are many studies documenting female mating preferences across taxa, male mate choice remains relatively understudied. Male mate choice often develops when there is variation in female quality and thus the fitness benefits of mating with particular females. Specifically, males tend to prefer females with traits that confer direct fitness benefits such as large body size, which may be linked with high fecundity. Prior work has shown that females of the strawberry poison frog, Oophaga pumilio, prefer males bearing certain coloration (most often the female’s own color), and that this preference can be learned through maternal imprinting. Females have been shown to prefer larger males as well. Here we test whether similar mate preferences for color and size exist in males of this species using two-way choice tests on captive bred male O. pumilio. In each test focal males were placed in an arena with two stimulus females: either both of the same size but differing in color, or both of the same color but differing in size. We found only weak evidence for behavioral biases toward particular colors and no evidence for biases toward larger females, suggesting that males of O. pumilio do not predictably choose mates based on these female traits. Despite several aspects of their natural history that suggest males have reasons to be choosy, our findings suggest that the cost of mate rejection may outweigh any fitness benefits derived from being selective of mates. Studies of additional populations, ideally conducted on wild individuals, are needed to better understand the range of conditions under which males may exhibit mate choice and the types of traits on which they base these choices.

Significance statement

To fully understand the fitness landscapes and evolutionary trajectories that result from sexual selection, we need to understand when and how the mate preferences of the two sexes act and interact. While female mate choice has been widely studied, male mate choice remains poorly understood. To help bridge this gap, we studied male mate preferences in the strawberry poison frog Oophaga pumilio, a small brightly colored frog for which female preferences for male color and size have been well-documented. We found no evidence that male O. pumilio exhibit mate preferences based on female size and little evidence for male mate preferences based on female color. This is surprising given that larger females are often more fecund, male O. pumilio are known to exhibit color-based behavioral biases in the context of male-male competition, and both sexes provide parental care.