Defining the Low End of Primate Social Complexity: The Social Organization of the Nocturnal White-Footed Sportive Lemur (Lepilemur leucopus)

Whereas other species of sportive lemurs (genus Lepilemur) have been described as living in dispersed pairs, which are characterized by spatial overlap but a lack of affinity or affiliation between one adult male and female, existing reports on the social organization of the white-footed sportive lemur (Lepilemur leucopus) are conflicting, describing them as either living in dispersed one-male multifemale systems or pairs. We conducted this study in the spiny forest of Berenty Reserve, southern Madagascar, to clarify the social organization and to characterize the level of social complexity of this species. We combined 1530 h of radio-telemetry and behavioral observations over a period of 1 yr to describe the spatiotemporal stability, size, and interindividual overlap of individual home ranges as well as interindividual cohesiveness. Results revealed low intra- and high intersexual home range overlap. Although most of the social units identified consisted of dispersed pairs (N = 5), males were associated with two adult females in two cases. Furthermore, members of a social unit were never observed to groom each other or to share a daytime sleeping site, and Hutchinson’s and Doncaster’s dynamic interaction tests indicated active avoidance between pair partners. Low cohesiveness together with extremely low rates of social interactions therefore arguably places Lepilemur leucopus at the low end of primate social complexity.     

Determinants of Pair‐Living in Red‐Tailed Sportive Lemurs (Lepilemur ruficaudatus)

Pair‐living and a monogamous mating strategy are rare and theoretically unexpected among mammals. Nevertheless, about 10% of primate species exhibit such a social system, which is difficult to explain in the absence of paternal care. In this study, we investigated the two major hypotheses proposed to explain the evolution of monogamy in mammals, the female defence hypothesis (FDH) and the resource defence hypothesis (RDH), in red‐tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal primate from Madagascar. We analysed behavioural data from eight male–female pairs collected during a 24‐mo field study to illuminate the determinants of pair‐living in this species. Male and female L. ruficaudatus were found to live in dispersed pairs, which are characterised by low cohesion and low encounter rates within a common home range. Social interactions between pair partners were mainly agonistic and characterised by a complete absence of affiliative interactions – body contact was only observed during mating. During the short annual mating season, males exhibited elevated levels of aggression towards mates, as well as extensive mate guarding and increased locomotor activity. In addition, males were exclusively responsible for the maintenance of proximity between pair partners during this period, and they defended their territories against neighbouring males but not against females. Together, these results point towards the importance of female defence in explaining pair‐living in L. ruficaudatus. We discuss the spatial and temporal distribution of receptive females in relation to the female defence strategies of males and suggest possible costs that prevent male red‐tailed sportive lemurs from defending more than one female.     

Evolution of Pair-Living in <Emphasis Type="Italic">Phaner furcifer</Emphasis>

Pair-living evolved several times independently in the primate lineage and most likely for more than one reason. Currently, there are 7 hypotheses regarding the evolution of pair-living in primates. They may explain several but not all cases. I investigated the applicability of the explanations to fork-marked lemurs Phaner furcifer. I used information from a long-term study on 8 fork-marked lemur families in Kirindy Forest to evaluate the hypotheses. Fork-marked lemurs live in uniform dispersed pairs, which share and defend a territory but spend three-quarters of their activity time apart from each other. Unconditional female dominance and lack of permanent close association between pair-partners disqualify most hypotheses. Lack of male parental care and long travel distances in small home ranges disqualify other explanations. I conclude that there is no support a priori for any current pair-living hypothesis and that the newly formulated intersexual-feeding-competition hypothesis best explains the evolution of pair-living in fork-marked lemurs. Accordingly, female range exclusivity evolved first as a consequence of intense feeding competition. Subsequently, indirect feeding competition drove females to accept a single male to share their territory as a defense against feeding competition from males whose ranges unsystematically overlap those of several females. This situation led to pair-living because formation of dispersed one-male-multifemale-units was too costly for males in terms of reduced foraging efficiency.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards' sportive lemur (Lepilemur edwardsi)

Dispersed pair-living primates provide a unique model for illuminating the evolution of mechanisms regulating spacing and cohesiveness in permanently cohesive groups. We present for the first time data on the spatiotemporal distribution and loud-calling behavior of the Milne Edwards' sportive lemur, known to forage solitarily during the night, but to form stable male-female sleeping groups during the day. Data include radio-tracking observations of sleeping associations, and focal follows of pair partners during dispersal in the evenings and reunions in the mornings. Male-female pairs forming stable sleeping associations during the day were pair-bonded. They used sleeping sites and home ranges exclusively, and exchanged loud calls at potentially restricted resources during dispersal in the evenings and during reunion in the mornings. Direct agonistic conflicts between pairs and others were rare. The acoustic analysis of loud calls revealed nine major call types. They carry signatures for sex and pair identity, and provide the substrate for signaling and the potential for recognizing pair ownership. Thus, pairs use loud call exchanges as a vocal display for signaling territory ownership, thus limiting direct aggressive encounters between neighbors and strangers. Altogether, our findings provide the first empirical evidence for the hypothesis that loud calling has evolved as a key mechanism for regulating space use and cohesiveness in dispersed pair-living primates.     

Spatiotemporal distribution of individuals as an indicator for the social system of Lepilemur sahamalaza

Primate social systems are highly diverse, complicating the classification of particularly elusive species that are difficult to observe. The spatial distribution of individuals over time is a critica lindicator for the social organization and long‐term studies are important to establish patterns of social interactions. In recent years, species of the cryptic, nocturnal sportive lemurs of the genus Lepilemur were found to live in pairs in which a single male and a single female share and defend a mutual home range. The present study aimed to forward research into this underrepresented genus by determining the social organization and structure of the Sahamalaza sportive lemur, L. sahamalaza. We collected 773.15 hr of behavioral and GPS data during a period of 10 months (between 2015 and 2016) on 14 individuals: eight females and six males. There was no evidence of pair‐specific home range use as intra‐ and intersexual home range overlap was high. No pattern of social interactions between focal individuals could be distinguished despite high range overlap. Individuals met and interacted infrequently, resulting in an interaction rate of 0.32 interactions/hr. Sleeping associations between adult individuals were never observed. While both sexes had access to multiple potential mating partners, range sizes or ranging distances did not increase in mating periods. Overall, the social system of Sahamalaza sportive lemurs exhibits aspects of a solitary social organization and structure with potential for the polygamous mating system. These findings underline the importance of detailed social ecology studies that can provide the basis for understanding potential environmental influences on social system variability of closely related species.     

Intertemporal choice in lemurs

Different species vary in their ability to wait for delayed rewards in intertemporal choice tasks. Models of rate maximization account for part of this variation, but other factors such as social structure and feeding ecology seem to underly some species differences. Though studies have evaluated intertemporal choice in several primate species, including Old World monkeys, New World monkeys, and apes, prosimians have not been tested. This study investigated intertemporal choices in three species of lemur (black-and-white ruffed lemurs, Varecia variegata, red ruffed lemurs, Varecia rubra, and black lemurs, Eulemur macaco) to assess how they compare to other primate species and whether their choices are consistent with rate maximization. We offered lemurs a choice between two food items available immediately and six food items available after a delay. We found that by adjusting the delay to the larger reward, the lemurs were indifferent between the two options at a mean delay of 17 s, ranging from 9 to 25 s. These data are comparable to data collected from common marmosets (Callithrix jacchus). The lemur data were not consistent with models of rate maximization. The addition of lemurs to the list of species tested in these tasks will help uncover the role of life history and socio-ecological factors influencing intertemporal choices.     

Duetting—A mechanism to strengthen pair bonds in a dispersed pair‐living primate (Lepilemur edwardsi)?

Duetting is defined as an interactively organized pair display in which one pair partner coordinates its vocalizations in time with those of the other. It is widespread among tropical birds and cohesive pair‐living primates, in which it is suggested to strengthen pair bonds. We know very little about the presence and function of duetting in dispersed pair‐living mammals. We studied duetting behavior in a solitary foraging, but pair‐sleeping, primate, the Milne Edwards' sportive lemur, in a dry deciduous forest of north‐western Madagascar. We radio‐tracked six pairs throughout 1 year and recorded their sleeping sites and associations, home‐range use, and vocal and behavioral interactions. Three different periods were covered (mating, pregnancy, and offspring care). Sleeping partners form long‐term pair bonds, indicated by an almost exclusive pair‐specific usage of sleeping sites and home‐ranges across periods. We explored three functional hypothesis of duetting: mate reunion, pair reunion, and joint‐territorial defense. Pairs regularly engaged in duet calling. Duetting increased significantly during the offspring care period. Duetting occurred significantly more often at feeding sites than at sleeping sites. Pair partners synchronized behavioral activities after duetting. The activity most often synchronized was locomotion. Pair partners played an equal role in duetting with no difference between sexes in starting or terminating duetting. Altogether, our results provide support for the hypothesis that in dispersed pair‐living primates, duetting evolved as a mechanism to coordinate activities between pair partners dispersed in space, to strengthen pair bonds, and, perhaps, to limit infanticide and nutritional stress in lactating females. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

The lack of female dominance in golden‐brown mouse lemurs suggests alternative routes in lemur social evolution

Female dominance is a well‐known trait of lemurs, although it has not been reported from all species and is still often unexplored, especially in the nocturnal species. We examined the intersexual dominance relationships in Microcebus ravelobensis, a congener of M. murinus who is well known for its female dominance. Given the many similarities in biology, it was predicted that M. ravelobensis should also possess female dominance. Seventeen unfamiliar male–female pairs were formed with animals captured in northwestern Madagascar and kept in a two‐cage setting (one cage for each animal) for up to 1 week. Four encounter experiments were conducted with each pair. In contrast to the expectations, females were not consistently dominant over their male partners. Only 3 of 17 dyads developed a clear agonistic asymmetry, among which were two cases of male dominance and only one case of female dominance. Because body mass differences did not explain the findings, various other possible explanations are discussed. It is suggested that food may not be the driving factor of female dominance in mouse lemurs. Instead, it is hypothesized that species‐specific differences in the quality of sleeping sites (i.e., tree holes) and in social grouping patterns may better explain why some mouse lemur species have female dominance, whereas others like the golden‐brown mouse lemur do not. It is concluded thatthese arguments and hypotheses may even hold true for other solitary foragers and may thereby lead to a better understanding of the variable social evolution in lemurs and primates in general. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.     

Effects of territorial intrusions, courtship feedings and mate fidelity on the copulation behaviour of the osprey

We studied copulation behaviour of the osprey, Pandion haliaetus, a semicolonial, fish-eating raptor, in Corsica (Mediterranean). Pairs copulated over a long period (45 days) and at a high rate, with, on average, 288 within-pair copulations (WPCs) for a clutch. Pairs breeding at higher density faced more frequent territorial intrusions than others and were potentially at an increased cuckoldry risk. However, and contrary to predictions of the ‘paternity assurance’ hypothesis for frequent copulations, we found that WPC rate decreased with increasing frequency of territorial intrusions. Male territory attendance increased with territorial intrusion frequency, to the detriment of the food provisioning of the female. Both attempted and successful WPC rates were positively related to the amount of food delivered by the male. Thus, the more frequent the territorial intrusions, the more time the male spent within his territory, the less he courtship fed and the smaller the fish he delivered, and the less the pair copulated successfully. WPC rate was also higher in newly formed pairs than in established pairs, and decreased with increasing pair bond length. The results suggest that males rely on mate guarding rather than frequent copulations to ensure paternity, and do not support the idea that sperm competition is the main cause of frequent WPCs. Nonfertilization functions of frequent copulations, such as pair bonding, mate assessment and mate retention, were likely early in the prelaying period. The findings that WPC rate decreased with mate fidelity and that females traded copulations for food suggest that mate retention was a possible function of frequent copulations in this species. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Evidence for social enhancement of reproduction in two Eulemur species

Across the past 20 years, captive reproduction has declined steeply in mongoose lemurs (Eulemur mongoz) and has been only moderately successful in black lemurs (E. macaco). At the same time, reproduction has been so successful in brown lemurs (E. fulvus) that contraception has been used since 1987 to limit captive numbers. No obvious cause for the differential reproductive success has been identified. Our experience with a pair of unrelated mongoose lemurs at the Philadelphia Zoological Garden suggested that they reproduced in only those years when they were caged in close proximity to another nonreproductive, full-sibling pair of mongoose lemurs. Examination of the worldwide pattern of captive reproduction by Eulemur species during the past two decades revealed that female black and mongoose lemurs housed in institutions with either additional conspecific males or additional conspecific pairs had a higher rate of reproduction than those maintained as an isolated pair. Black lemurs also had higher rates of reproduction when additional conspecific females were present. No similar pattern was found for brown lemurs or for two comparable mammals, the pudu (Pudu pudu) and the okapi (Okapia johnstoni). The evidence presented for the black and mongoose lemurs supports the existence of the Allee effect in these two species, namely, that reproduction is enhanced by the presence of conspecifics. © 1996 Wiley-Liss, Inc.     

Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations

Background

A central question in evolutionary biology is how cryptic species maintain species cohesiveness in an area of sympatry. The coexistence of sympatrically living cryptic species requires the evolution of species-specific signalling and recognition systems. In nocturnal, dispersed living species, specific vocalisations have been suggested to act as an ideal premating isolation mechanism. We studied the structure and perception of male advertisement calls of three nocturnal, dispersed living mouse lemur species, the grey mouse lemur (Microcebus murinus), the golden brown mouse lemur (M. ravelobensis) and the Goodman's mouse lemur (M. lehilahytsara). The first two species occur sympatrically, the latter lives allopatrically to them.

Results

A multi-parameter sound analysis revealed prominent differences in the frequency contour and in the duration of advertisement calls. To test whether mouse lemurs respond specifically to calls of the different species, we conducted a playback experiment with M. murinus from the field using advertisement calls and alarm whistle calls of all three species. Individuals responded significantly stronger to conspecific than to heterospecific advertisement calls but there were no differences in response behaviour towards statistically similar whistle calls of the three species. Furthermore, sympatric calls evoked weaker interest than allopatric advertisement calls.

Conclusion

Our results provide the first evidence for a specific relevance of social calls for speciation in cryptic primates. They furthermore support that specific differences in signalling and recognition systems represent an efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species.     

Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?

In group-living Malagasy primates (Lemuriformes), certain demographic and morphological traits deviate both from theoretical expectations derived from sexual selection theory and from patterns in better-known anthropoid primates. Lemurs lack sexual dimorphism in body and canine size and live in relatively small multimale-multifemale groups with, on average, even adult sex ratios, despite a polygynous mating system. In addition, the majority of gregarious lemurs are cathemeral, that is, they are regularly active both day and night. The social system of cathemeral lemurs has been considered an adaptation to their activity pattern. If so, groups should consist of multiple pairs that aggregate during diurnal activity and range separately at night in response to predation and infanticide risk, respectively. Moreover, mating privileges should exist between pair partners. We tested this hypothesis with data collected on two groups of wild redfronted lemurs in western Madagascar during 1023 focal animal hours spanning 4 months including the mating season. In addition, data on spatial relations were collected on 12 nights. We found no differences in group cohesion between day and night and no behavioural evidence for multiple male-female pairs. Instead, one male in each group monopolized social interactions with all females. However, females copulated with all resident males, although most often with the central male. Thus, basic predictions of the cathemerality hypothesis are unsupported. Multiple matings and indications of oestrous synchrony can be viewed as female counterstrategies against infanticide, whereas reproductive strategies of redfronted lemur males remain obscure. Copyright 1999 The Association for the Study of Animal Behaviour.     

Out of Sight but Not Out of Mind? Behavioral Coordination in Red-Tailed Sportive Lemurs (<Emphasis Type="Italic">Lepilemur ruficaudatus</Emphasis>)

Many animals are organized into social groups and have to synchronize their activities to maintain group cohesion. Although activity budgets, habitat constraints, and group properties may impact on behavioural synchrony, little is known regarding how members of a group reach a consensus on the timing of activities such as foraging bouts. Game theory predicts that pair partners should synchronize their activities when there is an advantage of foraging together. As a result of this synchronization, differences in the energetic reserves of the two players develop spontaneously and the individual with lower reserves emerges as a pacemaker of the synchrony. Here, we studied the behavioral synchrony of pair-living, nocturnal, red-tailed sportive lemurs (Lepilemur ruficaudatus). We observed 8 pairs continuously for ≥1 annual reproductive cycle in Kirindy Forest, Western Madagascar. During focal observations, one observer followed the female of a pair and, simultaneously, another observer followed the male. We recorded the location and behavioral state of the focal individual every 5 min via instantaneous sampling. Although behavioral synchrony of pair partners appeared to be due mainly to endogenous activity patterns, they actively synchronized when they were in visual contact (<10 m). Nevertheless, red-tailed sportive lemurs benefit from synchronizing their activity only for 15% of the time, when they are close together. The lack of an early warning system for predators and weak support for benefits via social information transfer in combination with energetic constraints may explain why red-tailed sportive lemurs do not spend more time together and thus reap the benefits of behavioral synchrony.     

Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history

The ring-tailed lemurs at Beza Mahafaly Special Reserve, Madagascar, exhibit a high frequency of severe wear and antemortem tooth loss. As part of a long-term study, we collected dental data on 83 living adult ring-tailed lemurs during 2003 and 2004. Among these individuals, 192 teeth were scored as absent. The most frequently missing tooth position is M1 (24%). As M1 is the first tooth to erupt, its high frequency of absence (primarily a result of wear) is not remarkable. However, the remaining pattern of tooth loss does not correlate with the sequence of eruption. We suggest that this pattern is a function of 1) feeding ecology, as hard, tough tamarind fruit is a key fallback food of ring-tailed lemurs living in gallery forests; 2) food processing, as tamarind fruit is primarily processed in the P3-M1 region of the mouth; and 3) tooth structure, as ring-tailed lemurs possess thin dental enamel. The incongruity between thin enamel and use of a hard, tough fallback food suggests that ring-tailed lemurs living in riverine gallery forests may rely on resources not used in the past. When comparing dental health in the same individuals (n=50) between 2003 and 2004, we found that individual tooth loss can show a rapid increase over the span of one year, increasing by as much as 20%. Despite this rapid loss, individuals are able to survive, sometimes benefiting from unintentional assistance from conspecifics, from which partially processed tamarind fruit is obtained. Although less frequent in this population, these longitudinal data also illustrate that ring-tailed lemurs lose teeth due to damage and disease, similar to other nonhuman primates. The relationship between tooth loss, feeding ecology, dental structure, and individual life history in this population has implications for interpreting behavior based on tooth loss in the hominid fossil record.     

Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator

Interactions between intraguild species that act as both competitors and predator–prey can be especially complex. We studied patterns of space use by the black-footed ferret (Mustela nigripes), a prairie dog (Cynomys spp.) specialist, and the American badger (Taxidea taxus), a larger generalist carnivore that competes for prairie dogs and is known to kill ferrets. We expected that ferrets would spatially avoid badgers because of the risk of predation, that these patterns of avoidance might differ between sexes and age classes, and that the availability of food and space might influence these relationships. We used location data from 60 ferrets and 15 badgers to model the influence of extrinsic factors (prairie dog density and colony size) and intrinsic factors (sex, age) on patterns of space use by ferrets in relation to space use by different sex and age categories of badgers. We documented asymmetric patterns of avoidance of badgers by ferrets based on the sex of both species. Female ferrets avoided adult female badgers, but not male badgers, and male ferrets exhibited less avoidance than female ferrets. Additionally, avoidance decreased with increasing densities of prairie dogs. We suggest that intersexual differences in space use by badgers create varying distributions of predation risk that are perceived by the smaller carnivore (ferrets) and that females respond more sensitively than males to that risk. This work advances understanding about how competing species coexist and suggests that including information on both intrinsic and extrinsic factors might improve our understanding of behavioral interactions between sympatric species.     

The inbreeding strategy of a solitary primate,Microcebus murinus

Inbreeding depression may be common in nature, reflecting either the failure of inbreeding avoidance strategies or inbreeding tolerance when avoidance is costly. The combined assessment of inbreeding risk, avoidance and depression is therefore fundamental to evaluate the inbreeding strategy of a population, that is how individuals respond to the risk of inbreeding. Here, we use the demographic and genetic monitoring of 10 generations of wild grey mouse lemurs (Microcebus murinus), small primates from Madagascar with overlapping generations, to examine their inbreeding strategy. Grey mouse lemurs have retained ancestral mammalian traits, including solitary lifestyle, polygynandry and male‐biased dispersal, and may therefore offer a representative example of the inbreeding strategy of solitary mammals. The occurrence of close kin among candidate mates was frequent in young females (~37%, most often the father) and uncommon in young males (~6%) due to male‐biased dispersal. However, close kin consistently represented a tiny fraction of candidate mates (< 1%) across age and sex categories. Mating biases favouring partners with intermediate relatedness were detectable in yearling females and adult males, possibly partly caused by avoidance of daughter–father matings. Finally, inbreeding depression, assessed as the effect of heterozygosity on survival, was undetectable using a capture–mark–recapture study. Overall, these results indicate that sex‐biased dispersal is a primary inbreeding avoidance mechanism at the population level, and mating biases represent an additional strategy that may mitigate residual inbreeding costs at the individual level. Combined, these mechanisms explain the rarity of inbreeding and the lack of detectable inbreeding depression in this large, genetically diverse population.