Intersexual conflict influences female reproductive success in a female-dispersing primate Abstract In group-living mammals, individual efforts to maximize reproductive success result in conflicts and compromises between the sexes. Females utilize counterstrategies to minimize the costs of sexual coercion by males, but few studies have examined the effect of such behaviors on female reproductive success. Secondary dispersal by females is rare among group-living mammals, but in western gorillas, it is believed to be a mate choice strategy to minimize infanticide risk and infant mortality. Previous research suggested that females choose males that are good protectors. However, how much female reproductive success varies depending on male competitive ability and whether female secondary dispersal leads to reproductive costs or benefits has not been examined. We used data on 100 females and 229 infants in 36 breeding groups from a 20-year long-term study of wild western lowland gorillas to investigate whether male tenure duration and female transfer rate had an effect on interbirth interval, female birth rates, and offspring mortality. We found that offspring mortality was higher near the end of males’ tenures, even after excluding potential infanticide when those males died, suggesting that females suffer a reproductive cost by being with males nearing the end of their tenures. Females experience a delay in breeding when they dispersed, having a notable effect on birth rates of surviving offspring per female if females transfer multiple times in their lives. This study exemplifies that female counterstrategies to mitigate the effects of male-male competition and sexual coercion may not be sufficient to overcome the negative consequences of male behavior. Significance Individual reproductive success is maximized through conflicts and compromises between the sexes in social mammals. In species with high dimorphism, females can experience sexual coercion by males and develop counterstrategies to reduce these costs. We studied this link in western lowland gorillas, which exhibit female secondary dispersal, a strategy that is believed to reflect female choice for the protective abilities of males. We found that females are faced with the dilemma of staying with a silverback at the end of his tenure and risk higher infant mortality versus dispersing and suffering reproductive delays and lower birth rates. This study shows that female reproductive strategies, namely dispersal, used to counter the effects of sexual coercion by males are not sufficient to overcome the negative consequences of male behavior.

Overmarking behaviour of zebra males: no scent masking, but a group cohesion function across three species Abstract Among many hypotheses in the literature that explain overmarking in mammals, most studies favour a sexual selection hypothesis. However, results in the literature are conflicting. In this study, we tested two hypotheses that could explain overmarking by males: (i) as a part of sexual selection, more specifically to mask scent of receptive females and (ii) as a form of communication serving to aid group cohesion. We observed each of the three zebra species in eight different herds at four zoos. In total, we recorded 1395 eliminations (760 defecations, 635 urinations) performed by 78 individuals including 8 stallions. Stallions investigated 248 eliminations and overmarked 124. The rate of overmarking by stallions was higher than those of all other sex and age categories. Stallions of all species overmarked all age and sex categories, except Grévy’s zebra stallions did not overmark foal eliminations. In contrast to our first hypothesis, when attracted to the elimination, stallions overmarked non-oestrus females more often than oestrus ones. Thus, our results did not support the hypothesis that overmarking by males has a sexual selection function, but it could be explained by the group cohesion hypothesis. Based on our results, it seems that overmarking by equid males plays a greater role in intra-specific communication than in intra-sexual competition. In addition, this behaviour might play different roles in different species based on their social organisation. Significance statement Overmarking is ubiquitous among terrestrial mammals; however, the function of this behaviour has not been fully explained. In addition, previous studies came to differing conclusions. In this study, we tested two hypotheses possibly explaining overmarking by adult males in three equid species. We found that adult males overmarked at a much higher rate than individuals of all other sex and age categories. In contrast to many other studies, our results did not support the hypothesis that overmarking by males has a sexual selection function, but it could be explained by a group cohesion hypothesis.

Galápagos lava lizards ( Microlophus bivittatus ) respond dynamically to displays from interactive conspecific robots Abstract In many species, outcomes of male duels determine access to females and, ultimately, male reproductive success. Ritualization of behavior in male contests can reduce the probability of injury, which benefits both contestants. Components of ritualized combat often include postures and displays that showcase a male’s quality in a sequential assessment of fighting ability. Among the most common contest acts in iguanine lizards are bobbing displays. Investigations of bobbing display dynamics often include experimental “playbacks,” in which video or robotic representations of conspecifics are presented to subjects. In most “playback” research, pre-programmed stimuli exhibit behavior that is independent of subjects’ responses, despite the fact that actual animal contests are highly interactive. In the present study, we utilized a robotic Galápagos lava lizard (Microlophus bivittatus) to investigate the importance of interaction in simulated contests under field conditions. Using a matched pairs design where each subject experienced two behavioral variants of the robotic stimulus, we tested the effect of a robot that displayed immediately following a subject’s display versus when the same robot display was postponed 30 s. Results showed that immediate response from the robot stimulated subjects to display significantly more often than when the stimulus was delayed. We speculate that subjects perceived a rapid response from their robotic contestant as being more aggressive than a delayed response. We discuss our results in light of relevant previous work, and we suggest possibilities for future research using interactive lizard robots. Significance statement Some of the most impressive examples of ritualized animal behavior can be observed in male contests for access to reproductive females. The use of stereotyped displays in such duels allows males to assess one another’s quality while avoiding dangerous fighting that can lead to injury. For example, males in many lizard species perform bobbing displays where contestants respond to each other in reciprocal fashion. In this study, we used a realistic lizard robot as a stand-in for a contestant in simulated contests. We found that an immediate display response by the robot to a subject’s bobbing display stimulated subjects to display significantly more often than when the robot’s response was delayed by 30 s. To our knowledge, this is the first interactive robot “playback” experiment with lizards. Future research will further explore the “rules” underlying display behavior in lizard contests.

Multi-scale predictors of parasite risk in wild male savanna baboons ( Papio cynocephalus ) Abstract Several factors are thought to shape male parasite risk in polygynous and polygynandrous mammals, including male-male competition, investment in potentially immunosuppressive hormones, and dispersal. Parasitism is also driven by processes occurring at larger scales, including host social groups and populations. To date, studies that test parasite-related costs of male behavior at all three scales—individual hosts, social groups, and the host population—remain rare. To fill this gap, we investigated multi-scale predictors of helminth parasitism in 97 male savanna baboons (Papio cynocephalus) living in the Amboseli ecosystem in Kenya over a 5-year span. Controlling for multi-scale processes, we found that many of the classic indicators of male mating effort—high dominance rank, testosterone, and glucocorticoids—did not predict helminth infection risk. However, we identified two parasite-related costs associated with male behavior: (i) socially connected males exhibited higher Trichuris trichiura egg counts and greater parasite species richness than socially isolated males and (ii) males with stable group residency exhibited higher parasite species richness than males who frequently dispersed to new social groups. At the population level, males harbored more parasites following periods of drought than rainfall. Lastly, parasites exhibited positive covariance suggesting that infection risk increases if a host already harbors one or more parasite taxa. These results indicate that multi-scale processes are important in driving male parasite risk and that some aspects of male behavior are costly. Together, our results provide an unusually holistic perspective on the drivers of parasite risk in the context of male behaviors and life histories. Significance statement Infection by gastrointestinal helminths can have major consequences for host fitness, especially in the context of male mating effort. Multi-scale processes—from the host to its social group and population—are important for understanding key drivers of parasitism. We leveraged long-term data from one of the longest running behavioral ecology studies of a wild primate population in the world, the well-studied Amboseli baboon population in Kenya. We found that traditional indicators of male mating effort (attaining high dominance rank, high testosterone and glucocorticoids) did not predict parasitism. However, male social connectedness to females, competitive group demography, and harsh weather were all associated with higher parasitism. Because socially connected males faced the highest parasite risk, males may face a tradeoff between male-female relationships and parasitism. Our results show how processes at multiple scales contribute to variation in male parasite risk.

Non-mimetic shiny cowbird nestlings escape discrimination by baywings in absence of host nest mates Abstract Nestlings of obligate brood parasites must obtain resources from heterospecific hosts that are attuned to the solicitation behaviours of their own progeny. Failing to match the appropriate stimuli may result in suboptimal provisioning or even the starvation of parasite young. Parasitic nestlings could overcome it by sharing the nest with host young, as long as they are able to compete efficiently for parental feedings. Here, we examined if non-mimetic shiny cowbird (Molothrus bonariensis) nestlings reared alone fail to elicit sufficient parental care from the grayish baywing (Agelaioides badius), a host that discriminates between their own and parasitic nestlings based on species-specific begging cues. We manipulated baywing broods to assess the ability of shiny cowbird nestlings to elicit parental provisioning and survive without host nest mates. Host provisioning rates and survival did not differ between shiny cowbirds reared alone and host nestlings in singleton broods. Also, growth patterns of experimental nestlings reared alone were similar to those reported for shiny cowbirds reared alongside baywing young. Hence, we did not find support for the hypothesis that non-mimetic nestlings require the assistance of host nest mates to elicit sufficient parental care from its baywing host. Furthermore, we found that shiny cowbirds that were reared alone continued receiving care from baywings after fledging, unlike shiny cowbirds from mixed broods. Our results add evidence to the idea of opposing selective pressures on the evolution of nest mate acceptance in cowbirds and suggest context-dependent host’s discrimination abilities that deserve further investigation. Significance statement The evolution of nest mate killing versus tolerance strategies is a long-standing question in the study of brood parasitism. Parasitic nestlings may benefit from sharing the nest with host young if they collectively induce more parental provisioning and the parasite can benefit from it. Host nest mates could also confer protection against discrimination when hosts respond preferentially to stimuli of their own kind. We examined this idea in a generalist brood parasite, the shiny cowbird (Molothrus bonariensis), and a host able to discriminate species-specific begging cues. The results showed that shiny cowbirds reared alone performed well and circumvent host discrimination also after leaving the nest. Our study supports the existence of trade-offs on the evolution of nest mate killing behaviours and adds evidence that context-dependent host’s discrimination abilities similar to those observed towards parasitic eggs can be at play towards parasitic fledglings.

Listening in: the importance of vibratory courtship signals for male eavesdropping in the wolf spider, Schizocosa ocreata Abstract Multimodal courtship signals may compensate for environmental interference or loss of signals in some sensory modes but may also increase detection by eavesdroppers. Studies on the wolf spider Schizocosa ocreata (Hentz) have demonstrated that males eavesdrop on visual courtship cues of other males and subsequently initiate courtship. Since S. ocreata males use multimodal courtship signals, we examined responses of males to playback of signals in different sensory modes (visual, vibration, multimodal) to test their relative importance for eavesdropping on courting male rivals. We used a recently developed technique to present male wolf spiders with video and/or vibratory stimuli: (1) a multimodal courting male stimulus, with synchronous visual and vibratory cues; (2) a visual-only courting male stimulus (minus the vibratory cues); (3) vibratory cues only (minus the visual cues); and (4) a control (visual background, no courtship). In single-presentation (no-choice) tests, males displayed more courtship bouts and longer durations of courtship bouts to the vibratory stimulus compared with either the visual or multimodal stimuli. However, in two-choice tests where isolated vibratory cues were paired against visual or multimodal stimuli, test males responded with more courtship bouts and longer durations of courtship bouts to the multimodal and visual stimuli. Results of these experiments suggest that male wolf spiders may vary eavesdropping courtship behaviors to compensate for missing sensory information concerning the location and other distinguishing characteristics of the rival male and the whereabouts of the female. Significance statement Social eavesdropping is used to exploit information in signals of conspecifics, e.g., as a means of mate competition. Studies on Schizocosa ocreata wolf spiders have shown that males eavesdrop on visual courtship displays of other males and subsequently initiate multimodal courtship. We used video/vibration playback to examine responses of males to signals in different sensory modes (visual, vibration, both) and determine their relative importance for eavesdropping on courting male rivals. Results suggest that depending on sensory modes of their rivals’ signals, males may vary their own courtship displays to compensate for missing information. For example, when signals are presented individually, eavesdropping male response patterns are distinctly different from when presented a choice between modes. Males show more displays with isolated vibratory signals, but given a choice, males more often increase their tapping when multimodal cues were present. Ultimately, eavesdroppers that adjust behaviors in response to available sensory cues would be able to “level the playing field” with rivals and potentially increase the probability of gaining attention of females.

One size fits all? Relationships among group size, health, and ecology indicate a lack of an optimal group size in a wild lemur population Abstract Group size is a key component of sociality and can affect individual health and fitness. However, proximate links explaining this relationship remain poorly understood, partly because previous studies neglected potential confounding effects of ecological factors. Here, we correlated group size with various measures of health while controlling for measures of seasonality and habitat quality, to explore trade-offs related to group living in a mainly folivorous primate—Verreaux’s sifakas (Propithecus verreauxi). Over a course of 2 years, we studied 42 individuals of 7 differently sized groups (range 2–10) and combined measures of faecal glucocorticoid metabolites (n > 2300 samples), parasitism (n > 500 samples), ranging and activity patterns, together with estimates of habitat quality (measures of ~ 7000 feeding trees). None of our measures was correlated with group size, while seasonality, but not habitat quality, impacted almost all examined variables. We conclude that group size alone might be insufficient to explain patterns in the sociality-health nexus or that the small range of group sizes in this species does not induce effects suggested for species living in larger groups. An optimal group size balancing the advantages and disadvantages of living in differently sized groups may not exist for Verreaux’s sifakas. Our results do not support predictions of the ecological constraints hypothesis or the optimal group size hypothesis as they may only account for species limited in group size by ecological factors—a condition that may not apply to the majority of folivorous mammals, which seem to be limited by social factors. Significance statement Group size is a key component of group living and can crucially impact individual health. Ecological variables may modulate this relationship, but they were often neglected in previous studies. To better understand the links between sociality and health, we, for the first time in a mammal, simultaneously examined variation in ranging patterns, daily activities, glucocorticoid concentrations, and parasitism as a function of group size and under consideration of measures of seasonality and habitat quality in wild Verreaux’s sifakas (Propithecus verreauxi). Group size had no impact on individual health indicators, while seasonal variation in food availability and temperature differences, but not habitat quality, affected the majority of variables. We demonstrate strong impacts of environmental factors on socio-ecological traits and conclude that group size on its own might be insufficient to explain patterns in the sociality-health nexus.

Evidence of phenotypic correlation between exploration activity and resting metabolic rate among populations across an elevation gradient in a small rodent species Abstract Behavior and metabolism are frontline reactions to environmental challenges that can covary in their response through at least two mechanisms. First, natural selection can generate correlation in phenotype among distinct populations if they are exposed to a common selective force. Thus, metabolism and behavior can exhibit phenotypic correlation among populations when responding (independently from each other) to co-varying selective forces. Second, because behavioral responses are energy-demanding, variation in energy acquisition or allocation among individuals of the same population can also generate, respectively, a positive or negative correlation within populations. To address this issue, we investigated among- and within-population (co)variations in exploration activity (EA) and resting metabolic rate (RMR) of adult common voles (Microtus arvalis) issued from four high-elevation populations (> 1400 m a.s.l.) and five low-elevation populations (< 520 m a.s.l.). Individuals were acclimatized for at least 1 month to the same laboratory conditions before being tested for EA and RMR. Voles from high-elevation populations were more explorative and they had higher RMR than their counterparts from low-elevation populations. The similar effects of elevation on EA and RMR accounted for a correlation of 0.28 (0.064; 0.658) between EA and RMR across low- and high-elevation populations. We found no evidence of a within-population correlation between EA and RMR. More work relying, for instance, on repeated sampling or experimental selection is nonetheless needed to confirm a lack of integration between metabolism and behavior at the individual level. Our results highlight the importance of co-varying selective forces in generating among-population phenotypic correlation between EA and RMR in this small rodent species. Significance statement There is increasing interest at deciphering the sources of covariation between metabolism and behavioral traits. Phenotypic covariation can be observed among populations if metabolism and behavior are responding independently from each other to co-varying selective forces. Because behavioral responses are energy-demanding, variation in energy acquisition or allocation between individuals of the same population can also lead to, respectively, a positive or negative phenotypic correlation. In this study, we highlight the importance of co-varying selective forces in generating phenotypic correlation between metabolism and behavior across low- and high-elevation populations of a small rodent species. We found no evidence of a correlation within populations. More work relying, for instance, on repeated sampling or experimental selection is now needed to confirm a lack of integration between metabolism and behavior at the individual level.

Variable parental responses to changes in offspring demand have implications for life history theory Abstract Parental care, a component of reproductive effort, should evolve in response to its impact on both offspring and parent fitness. If so, manipulations in brood value should shift levels of care in predictable ways, provided that appropriate cues about the change in offspring value are altered. Prior brood size manipulations in birds have produced considerable variation in responses that have not been fully investigated. We conducted paired, short-term (2 h) reductions and enlargements in brood size (± 2 nestlings) of house sparrows in each of 4 years. Parents at reduced broods shifted parental care downward in all four seasons. Parents experiencing increased broods responded significantly variably across years; in some, they increased care, but in others, they decreased care compared with control periods. Nestlings in both treatments gained less mass than during control sessions, with year producing variable effects. We found evidence that parents experiencing reduced broods behave as if recurring predation is a risk, but we found no evidence that parents with enlarged broods were responding to inappropriate cues. Instead, parent sparrows may be behaving prudently and avoid costs of reproduction when faced with either broods that are too small or too large. We modified a published model of optimal care, mimicked our empirical manipulation, and found that the model replicated our results provided cost and benefit curves were of a particular shape. Variation in ecology among years might affect the exact nature of the relationship between care and either current or residual reproductive value. Other data from the study population support this conclusion. Significance statement Parent animals often adjust their levels of care in response to manipulations of offspring value, but considerable variation in these responses exists. This suggests either a mismatch between manipulation and natural cues or undetected subtleties in the fitness consequences of care. Over 4 years, we conducted manipulations of offspring number in the biparental house sparrow (Passer domesticus). We found little evidence that parents misinterpreted cues regarding the change in number, but they behaved differently depending on the year of the manipulation. A model recovered the observed patterns if a parameter influencing the curve relating offspring fitness to levels of care was altered. This parameter should vary with food supply, and our data suggested that this varied in the years of our study. Our results emphasize that predictions about patterns of parental care are risky without attending to the shapes of fitness curves and that some organisms may be particularly sensitive to food supply.

Social preferences and network structure in a population of reef manta rays Abstract Understanding how individual behavior shapes the structure and ecology of populations is key to species conservation and management. Like many elasmobranchs, manta rays are highly mobile and wide-ranging species threatened by anthropogenic impacts. In shallow water environments, these pelagic rays often form groups and perform several apparently socially mediated behaviors. Group structures may result from active choices of individual rays to interact or passive processes. Social behavior is known to affect spatial ecology in other elasmobranchs, but this is the first study providing quantitative evidence for structured social relationships in manta rays. To construct social networks, we collected data from more than 500 groups of reef manta rays (Mobula alfredi) over 5 years in the Raja Ampat Regency of West Papua. We used generalized affiliation indices to isolate social preferences from non-social associations, the first study on elasmobranchs to use this method. Longer lasting social preferences were detected mostly between female rays. We detected assortment of social relations by phenotype and variation in social strategies, with the overall social network divided into two main communities. Overall network structure was characteristic of a dynamic fission-fusion society, with differentiated relationships linked to strong fidelity to cleaning station sites. Our results suggest that fine-scale conservation measures will be useful in protecting social groups of M. alfredi in their natural habitats and that a more complete understanding of the social nature of manta rays will help predict population responses to anthropogenic pressures, such as increasing disturbance from dive tourism. Significance statement In social animals, relationships between individuals have important implications for species conservation. Like many other sharks and rays, manta rays are threatened species, and little is known about their natural behavior or how their populations are structured. This study provides evidence of social structure in a wild, free-ranging population of reef manta rays. We show for the first time that individual manta rays have preferred relationships with others that are maintained over time, and structured societies. This study extends our knowledge of elasmobranch ecology and population structuring. Results suggest that understanding social relationships in manta rays will be important in protecting populations from human impacts and developing sustainable, localized conservation and management initiatives.