Mating system of a Neotropical roost-making bat: the white-throated, round-eared bat, Lophostoma silvicolum (Chiroptera: Phyllostomidae)

The vast majority of bats strongly depend on, but do not make, shelters or roosts. We investigated Lophostoma silvicolum, which roosts in active termite nests excavated by the bats themselves, to study the relationship between roost choice and mating systems. Due to the hardness of the termite nests, roost-making is probably costly in terms of time and energy for these bats. Video-observations and capture data showed that single males excavate nests. Only males in good physical condition attracted females to the resulting roosts. Almost all groups captured from excavated nests were single male-multifemale associations, suggesting a harem structure. Paternity assignments based on ten polymorphic microsatellites, revealed a high reproductive success of 46% by nest-holding males. We suggest that the mating system of L. silvicolum is based on a resource-defense polygyny. The temperatures in the excavated nests are warm and stable, and might provide a suitable shelter for reproductive females. Reproductive success achieved by harem males appears to justify the time and effort required to excavate the nests. Reproductive success may thus have selected on an external male phenotype, the excavated nests, and have contributed to the evolution of an otherwise rare behavior in bats.Communicated by G. Wilkinson     

Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae)

Males of the sac-winged bat, Saccopteryx bilineata, actively fill their propatagial sacs with secretions from the genital region, the gular gland, urine and saliva. From our observations and those of Starck we deduce that propatagial sacs in S. bilineata do not have a glandular function, but are instead organs for the storage and display of odours. In addition to the already known “salting” and hovering behaviour of male S. bilineata, we describe in detail how odour is fanned to roosting individuals during the complex, stereotypic hovering displays. S. bilineata males also coat the fur of their backs with saliva using the wing tip and might scent-mark territory boundaries. “Yawning” may represent a visual as well as an olfactory cue. Odour seems to play an important role in the social communication of S. bilineata and in other emballonurids, as revealed by the broad distribution of wing sacs in this family. S. bilineata males display odour during energetically costly hovering flights in front of females. We demonstrate that the number of hovering displays increases with harem size. The mating effort of S. bilineata males comprises a multimodal signalling behaviour. Although males defend harem territories in which females gather, females seem to be able to choose the father of their progeny freely among the males of a colony. This may have led to the evolution of the complex mating displays by male S. bilineata. Received: 9 December 1998 / Received in revised form: 6 May 1999 / Accepted: 13 June 1999     

Contrasting home-range size and spatial partitioning in cryptic and sympatric pipistrelle bats

The extent of spatial partitioning in insectivorous bats, whose prey is patchily distributed and transient in nature, remains a contentious issue. The recent separation of a common Palaearctic bat, the pipistrelle, into Pipistrellus pipistrellus and Pipistrellus pygmaeus, which are morphologically similar and sympatric, provides an opportunity to examine this question. The present study used radio telemetry to address the spatial distribution and foraging characteristics of P. pipistrellus and P. pygmaeus in northeast Scotland, to test the hypothesis that coexistence between these species is facilitated through spatial segregation. We reveal large and significant differences in the spatial distribution and foraging characteristics of these two cryptic species. Individual P. pipistrellus home ranges were on average three times as large as that of P. pygmaeus, and they foraged for approximately an hour longer each night. Inter-specific spatial overlap was minimal (<5%) and core foraging areas of either species were essentially mutually exclusive despite the proximity of the two roosts. Inter-specific differences in range size were associated with the spatial dispersion of productive foraging sites within individual foraging ranges. P. pipistrellus foraging sites were highly dispersed, necessitating larger ranges. It is predicted that the spatial segregation revealed by the present study is a result of selection favouring the avoidance of competition in these species through differential habitat use.     

Similar is not the same: Social calls of conspecifics are more effective in attracting wild bats to day roosts than those of other bat species

Many bat species regularly need to find new day roosts as they require numerous shelters each breeding season. It has been shown that bats exchange information about roosts among colony members, and use echolocation and social calls of conspecifics in order to find roosts. However, it is unclear if wild bats discriminate between social calls of conspecifics and other bat species while searching for roosts. Furthermore, the extent that bats are attracted to potential roosts by each of these two call types is unknown. We present a field experiment showing that social calls of conspecifics and other bat species both attract bats to roosts. During two summers, we played back social calls of Bechstein’s bats (Myotis bechsteinii) and Natterer’s bats (Myotis nattereri) from different bat boxes that can serve as roosts for these species. All experimental bat boxes were monitored with infrared video to identify the approaching bat species. Three species (M. bechsteinii, M. nattereri, and Plecotus auritus) approached the boxes significantly more often during nights when bat calls were played compared to nights without playbacks. Bechstein’s bats and Natterer’s bats were both more attracted to social calls of conspecifics than of the other species, whereas P. auritus did not discriminate between calls of either Myotis species. Only Bechstein’s bats entered experimental boxes and only at times when calls from conspecifics were played. Our findings show that wild bats discriminate between social calls of conspecifics and other bat species although they respond to both call types when searching for new roosts.     

The economics of harem maintenance in the sac-winged bat, Saccopteryx bilineata (Emballonuridae)

Saccopteryx bilineata has a polygynous mating system in which males defend females in a harem territory. Harem defense and courtship include energetically costly flight maneuvers and hovering displays. We tested if (1) harem males have a greater field metabolic rate than non-harem males or females and if (2) the field metabolic rate of harem males is correlated with the number of females in a harem territory. We measured the energy budget in 32 S. bilineata with the doubly labeled water method and compared these estimates with behavioral observations in the daytime roost. Among adult bats, field metabolic rate varied with body mass by an exponent of approximately two. We found no significant difference in field metabolic rate or mass-specific field metabolic rate between harem and non-harem males. The mass-specific field metabolic rate of harem-males increased with harem size. The latter finding supports the hypothesis that the energy costs of courtship display and territorial defense influence the energy budget of harem males. Overall, field metabolic rates of S. bilineata were lower than those of similarly sized bats of the temperate zone and only 2.3 times above the basal metabolic rate recorded for this species. We suggest that male S. bilineata did not take advantage of their metabolic capacity because a prudent allocation of energy to activities of harem maintenance is an adaptive strategy for males in this mating system.     

Resource quality or harem size: what influences male tenure at refuge sites in tree weta (Orthoptera: Anostostomatidae)?

Rather than seeking females directly, males in many animal species locate and defend sites that contain spatially limited resources essential for female survival and reproduction. In these cases, resident males successfully repelling conspecific rivals will mate with sexually receptive females that seek to use the resident’s resources. Theory predicts that if resources are limiting in nature, are costly to procure, and if residency at the resource site increases male reproductive success, each site should be monopolised by a single adult male. Moreover, if females aggregate at these sites, males should be sedentary and monopolise harems. This predicts that males should reside at resource sites longer than females and male tenure should be positively correlated with harem size. I address these hypotheses using a wild population of the Wellington tree weta, Hemideina crassidens, a sexually dimorphic insect in which males use mandibular weapons in fights to control resource sites (galleries in trees) required by females for diurnal refuge. In a longitudinal study using artificial galleries, I show that male tenure in a gallery is positively related to harem size and, contrary to prediction, not gallery size per se. Moreover, contrary to prediction, females are more sedentary than males: males appear to move frequently between galleries to search for novel mates. I show experimentally that galleries represent mating sites to males: males prefer galleries housing adult females whereas females prefer unoccupied galleries. Females likely avoid male-occupied galleries because they incur injuries when interacting with males.     

Positive association between social and extra-pair mating in a polygynous songbird, the dickcissel (Spiza americana)

In polygynous species, males appear to gain additional offspring by pairing with multiple females simultaneously. However, this may not be true if some females copulate outside of the social pair bond. Polygynous males could experience lower paternity because of trade-offs among gaining multiple social mates, guarding fertility with these mates, and pursuing extra-pair matings. Alternatively, polygynous males could simultaneously gain extra social mates and have high paternity, either because of female preferences or because of male competitive attributes. We tested four predictions stemming from these hypotheses in a facultatively polygynous songbird, the dickcissel (Spiza americana). Unlike most previous studies, we found that males with higher social mating success (harem size) also tended to have higher within-pair paternity and that the number of extra-pair young a male sired increased significantly with his social mating success. Females that paired with mated males were not more likely to produce extra-pair young. In contrast, extra-pair paternity was significantly lower in the nests of females whose nesting activity overlapped that of another female on the same territory. This pattern of mating was robust to differences in breeding density. Indeed, breeding density had no effect on either extra-pair mating or on the association between polygyny and paternity. Finally, nest survival increased with harem size. This result, combined with the positive association between polygyny and paternity, contributed to significantly higher realized reproductive success by polygynous male dickcissels.     

The social organization of the common vampire bat

Summary At a site in Costa Rica, three groups of 8–12 adult female vampire bats, Desmodus rotundus, utilize group-specific sets of hollow trees as day roosts. Long-term nonrandom associations between pairs of females, as measured by the proportion of time one bat spends roosting in the same tree with another bat over a 3 year period, occur even when preferences for particular trees are removed. Significant associations exist between both related and unrelated adult females. Adult male bats, however, show few associations with females or other males. By observing bats within trees and while foraging, and by monitoring feeding flights with radiotelemetry, the following potential benefits of association could be tested. Females roost together to (1) share a suitable microclimate, (2) avoid predators, (3) avoid ectoparasite infestations, (4) minimize travel to mobile prey animals, (5) respond to coercive males, (6) feed simultaneously from a bite, (7) remove ectoparasites by allogrooming, and (8) share food by regurgitating blood to other bats within roosts. The data do not indicate that any of the first five hypotheses provide significant benefits for long-term associations although predators and ectoparasite levels may cause occasional changes in roost sites. Simultaneous feeding was uncommon and apparently confined to females and their recent offspring. Allogrooming, although common, occurred independently of the presence of ectoparasites. Food sharing, however, occurred between both related and unrelated adult females with high levels of association and provides at least one selective advantage for maintaining cohesive female groups.     

Large males dominate: ecology,social organization,and mating system of wild cavies,the ancestors of the guinea pig

Ecological factors differently affect male and female animals and thereby importantly influence their life history and reproductive strategies. Caviomorph rodents are found in a wide range of habitats in South America and different social and mating systems have evolved in closely related species. This permits to study the impact of ecological factors on social evolution. In this study, we investigated the social organization and the mating system of the wild cavy (Cavia aperea), the ancestor of the domestic guinea pig, in its natural habitat in Uruguay. Based on our laboratory investigations, we expected a polygynous system with large males controlling access to females. Results from radiotelemetry and direct observations showed that females occupied small stable home ranges which were largely overlapped by that of one large male, resulting in a social organization of small harems. In some cases, small satellite males were associated with harems and intermediate-sized roaming males were occasionally observed on the study site. However, microsatellite analyses revealed that offspring were exclusively sired by large males of the same or neighboring harems, with a moderate degree of multiple paternity (13–27%). Thus, the mating system of C. aperea can be described as polygynous and contrasts with the promiscuous organization described for other species of cavies (Cavia magna, Galea musteloides and Microcavia australis) living under different ecological conditions. Our findings stress the strong impact of environmental factors on social evolution in Caviomorphs as resource distribution determines female space use and, thereby, the ability of males to monopolize females. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Dispersal and social organization in the Neotropical Grey sac-winged bat Balantiopteryx plicata

Recent evidence suggests that tropical bats may frequently depart from the predominant mammalian male-biased dispersal pattern. So far, two emballonurid bat species that are closely related to our study species (Grey sac-winged bat, Balantiopteryx plicata) have been found to exhibit exceptional female-biased dispersal that is in accordance with father–daughter inbreeding avoidance. In contrast, using a combination of long-term behavioral observations of banded bats and DNA sequencing of the mitochondrial d-loop, our results suggest that B. plicata is the first Neotropical emballonurid with female philopatry and frequent male dispersal. However, just like in the other emballonurids, the age of females at first conception fell below the tenure of males. Thus, philopatric B. plicata females might face a father–daughter inbreeding risk if mating with males from their roosts. Such risk could be circumvented if mating occurs outside the nursing roost, e.g., in male mating aggregations. In contrast to other Neotropical emballonurid bats, the Grey sac-winged bat forms colonies with a greatly male-biased sex ratio (only 5 and 21 % females). Males of such colonies showed high roost fidelity and the sex ratio did not change throughout the year and for up to many years, suggesting an important role in mating. We conclude that studying the diverse mating and dispersal patterns of Neotropical emballonurids shows great potential to enlarge our understanding on how the proposed ultimate causes (i.e., avoidance of inbreeding and local competition between kin) affect the evolution of sex-biased dispersal.     

Female aggression and male peace-keeping in a cichlid fish harem: conflict between and within the sexes in Lamprologus ocellatus

Summary Conflicts of interest within and between the sexes are important processes leading to variability in mating systems. The behavioral interactions mediating conflict are little documented. We studied pairs and harems of the snail-shell inhabiting cichlid fish Lamprologus ocellatus in the laboratory. Due to their larger size, males controlled the resource that limited breeding: snail shells. Males were able to choose among females ready to spawn. Females were only accepted if they produced a clutch within a few days of settling. When several females attempted to settle simultaneously the larger female settled first. Females were least aggressive when guarding eggs. Secondary females were more likely to settle when the primary female was guarding eggs. In established harems females continued to be aggressive against each other. The male intervened in about 80% of female aggressive interactions. Male intervention activity correlated with the frequency of aggression among the females in his harem. The male usually attacked the aggressor and chased her back to her own snail shell. When a male was removed from his harem, aggression between females increased immediately and usually the secondary female was expelled by the primary female within a few days. Time to harem break-up was shorter the more mobile the primary females' young were and did not correlate with the size difference between harem females. Male L. ocellatus interfere actively in female conflict and keep the harem together against female interests. Female conflict presumably relates to the cost of sharing male parental investment and to the potential of predation by another female's large juveniles on a female's own small juveniles.Correspondence to: F. Trillmich     

Behavioural determinants of gene flow in the bat Miniopterus schreibersii

Dispersal and migratory behaviours are often important determinants of gene flow in wild species, and we have studied their role using ringing-recapture data in the Portuguese population of Miniopterus schreibersii, a cave-dwelling bat that forms large maternity colonies. Juvenile dispersal, usually a major agent of gene flow, appears to be negligible, as young females never settled to give birth in foreign colonies. Likewise, there was virtually no dispersal of adult females to foreign maternity colonies. This strong philopatry virtually eliminated female-mediated gene flow, but we found a great potential for male-mediated gene flow among colonies, as regional migrations temporarily joined both sexes from different colonies in the same roosts, during the mating season. In fact, females from some colonies were more likely to mate with males from foreign colonies than from their own, thus potentially bringing home genes of foreign males. In spite of this abundant gene flow, we found a pattern of isolation by distance and even strong barriers to gene flow, which is explained by the fact that migrations were usually too short to allow direct flow among distant colonies. We concluded that potential gene flow is influenced by the distance between colonies and the availability of mating roosts between them. In addition, we found this flow to be asymmetrical, with a dominant direction from the largest to the smallest colonies. Our ringing-recapture estimates of potential gene flow based on dispersal and migratory behaviour are compatible with the genetic structure of the population for both nuclear and mitochondrial DNA. Our conclusions have implications for the conservation of bats with a spatial behaviour similar to that of M. schreibersii. Colonies should be managed individually because strict female philopatry not only promotes their isolation but also minimises the contribution of immigration in rescuing declining colonies. Furthermore, the results underline the importance of preserving mating roosts to maintain gene flow among colonies.     

Extra-pair paternity in the facultatively polygynous spotless starling,<Emphasis Type="Italic"> Sturnus unicolor</Emphasis>

A potential cost of polygyny that may have restrained its evolution in some avian species is the presence of extra-pair offspring in the nests of males mated with several females. However, this relationship is not frequently found and an experimental approach investigating the association between extra-pair offspring and polygyny, while controlling for male traits related to polygyny, has not been undertaken. In this study, we manipulated the testosterone levels of facultatively polygynous spotless starlings, Sturnus unicolor, to establish experimentally different groups of polygyny and analyse its influence on levels of extra-pair offspring in males for which other traits were randomised. During two consecutive breeding seasons, we examined the effects of harem size on the ability of males to assure genetic paternity, assessed by DNA fingerprinting, and on reproductive success in their own nests. The frequency of extra-pair fertilisations varied between 10% (14/140) in 1996 and 20% (39/194) in 1997. Year-to-year analyses of extra-pair paternity variables with treatment as factor and harem size (number of simultaneous mated females) as covariate, were significant only in relation to harem size. Males with few simultaneously mated females were less cuckolded than more polygynous males in 1997 but not in 1996, indicating that mating costs of polygyny occurred, at least in the year with the higher rate of extra-pair paternity. Because polygynous males have more social mates, they may accrue higher reproductive success irrespective of their risk of being cuckolded. However, our results suggest that to be polygynous is costly in terms of paternity loss when we experimentally induce mating status controlling for individual male traits. However, the low values of our power tests for the statistically non-significant results of hormone on cuckoldry do not allow us to discard this hormone effect altogether.     

Why insects swarm: testing the models for lek mating systems on swarming Empis borealis females

Summary Female dance-flies, Empis borealis L., gather to swarm, and males carrying nuptial gifts visit swarms for mating. Field observations and experiments were performed on this behaviorally sex-role reversed species to test models of lekking behavior. The key predictions were: (1) female preference model: male visiting rate and mating rate should increase with the number of females in swarm (swarm size), (2) hotspot model: male visiting rate should be independent of swarm size, and (3) hotshot model: swarm size should be positively correlated with the body size of the largest female in swarm. We found that male visiting rate and mating rate increased with swarm size, and that mating rate per female increased with swarm size. Males also mated more often in larger swarms than in smaller ones. Both males and females visited swarm sites even in the absence of other individuals. When females were successively removed from swarm sites more males than females on average arrived at these sites: 2.25 males per female. When no individuals were present at the swarm site, arriving males moved on to another site, whereas arriving females generally stayed. Larger experimental swarm-markers attracted both more males and more females and even more males when swarming females were present. There was no correlation between mean or median female size in swarms and the number of females in swarms. Thus, the female preference model and the hotspot model were corroborated, while other models were judged unlikely to explain swarming behavior in E. borealis. Correspondence to: B.G. Svensson     

Vocalizations by Alaskan moose: female incitation of male aggression

Evidence of female fomentation of male–male aggression as a mechanism of mate choice is rare, especially in mammals. Female choice of mates in polygynous species may be masked by intense male competition or by males attempting to restrict female choice. We studied protest moans of female Alaskan moose Alces alces gigas in interior Alaska, USA, from 1987 to 1990, to determine if moans incited male–male aggression. Alaskan moose exhibit a mating system in which one dominant male (the harem master) herds, defends, courts, and attempts to mate with females in his harem. Protest moans were given by females only in response to courtship. We hypothesized that if protest moans were related to females reducing harassment and exercising mate choice, females should give protest moans more frequently when courted by small males and less often when courted by large males, and that rates of male–male aggression would be elevated following protest moans. Harems were composed of one large male, with a mean of 4.4 females (median = 3 females); 10% of 132 harems included ≥10 females. The temporal pattern of protest moans from late August through November was associated with, but tended to lag behind, mating behavior. The rate of protest moans given by females decreased with increasing size of males courting them. Male–male aggression was significantly less during periods without protest moans than during periods in which protest moans occurred. These results indicate that female moose gave protest moans to reduce harassment by smaller males, and assure a mating opportunity with the most dominant male. Such a subtle mechanism of indirect mate choice by females may occur in other vertebrates in which choice is limited by a mating system in which male–male combat and male dominance over females reduces opportunities for female choice. The importance of female choice may be undervalued in studies of sexual selection in mammals.     

Dominance and competition in an herbivorous lizard

Summary A study of social organization in an herbivorous lizard Ctenosaura hemilopha investigated the role of dominance in group member behavior. Attention focused on a very populous (16 ind.) colony to examine causes and effects of crowding with respect to competitive factors. Lizards were colonial, with a top-rank male, one or more adult females, and various subadults and juveniles. Top-rank males defended harems, with colonies female-biased (1:4 in focal colony). Dominance hierarchy was observed, with females more aggressive than males, except for the top-rank male. Group awareness facilitated adaptive responses to threatening dominants and predators. Strong correlations existed among individual size, rank, and aggression. Top-rank male aggressiveness was partly explained by harem defense. Food resource competition, which causes aggression in female insectivorous lizards, did not explain female C. hemilopha behavior. Response to predators, predator fecal pellet analysis, and tail break frequencies implicate crevice escape sites for predator avoidance as a prime controller of social and population structure in these lizards.     

Histology of the gonads and observations on the social behavior of the Caribbean angelfish Holacanthus tricolor

Male and female specimens of Holacanthus tricolor were collected in May 1981 and September 1982 off the Island of St. Croix. U.S. Virgin Islands, and their gonads were examined histologically. All testes examined showed vasa deferentia which were characteristic of secondary males, suggesting protogynous sex change. A transitional individual supported this interpretation. Ovarian histology and size-specific egg counts revealed seasonal differences in spawning frequency and clutch size. Females appeared to spawn every day in May. The timing of final maturation and hydration of the oocytes indicated that spawning occurred in the late afternoon or early evening. Not all females spawned every day in September, and clutch sizes were smaller than those of May. Behavioral observations of H. tricolor in the field revealed that males defended harems of two to four smaller females. Within each harem, females of different sizes had overlapping home ranges, while the home ranges of females of similar size did not overlap. Besides size dimorphism between the sexes, H. tricolor exhibited a previously unreported sexual dichromatism.     

Sexual selection favours small and symmetric males in the polygynous greater sac-winged bat Saccopteryx bilineata (Emballonuridae, Chiroptera)

We investigated how morphological traits of territorial males in the polygynous bat Saccopteryx bilineata were related to their reproductive success. Because of the frequency of aerial courtship displays and defence manoeuvres, and the high energetic costs of flight, we expected small and symmetric males to be better able to court females on the wing and to monopolize copulations with females in their harems. We predicted that small and symmetric males would sire more offspring within the colony and a larger portion of the young born within their harem than large or asymmetric males. We measured size and fluctuating asymmetry of 21 territorial males and analysed their reproductive success in 6 offspring cohorts (n=209 juveniles) using 11 microsatellite loci. As predicted, small and symmetric males had, on average, a higher reproductive success in the colony than large and asymmetric males. The percentage of young sired by males within their harem increased as males decreased in size, but was not influenced by fluctuating asymmetry. As fluctuating asymmetry of males correlated with their reproductive success within the colony but not within their harems, we infer that fluctuating asymmetry is probably related to female choice, whereas male size is probably important for harem defence on the wing.Communicated by G. Wilkinson     

Social organization and space-use in Gunnison's prairie dog

Summary Social organization of the Gunnison's prairie dog, Cynomys gunnisoni, was studied in two populations in south-central Colorado. Gunnison's prairie dogs live in complex, interactive societies fitting current definitions of highly social ground squirrels. Members of harems (coteries) cooperatively use and defend a common territory. Spatial overlap is extensive between the adult male(s) and adult females, and among adult females within the harem through the active season. Amicable behavioral interactions are frequent within the harem, whereas interactions between members of different harems are primarily agonistic and spatial overlap is minimal. Although their behavioral repertoire is more limited, social organization of the Gunnison's prairie dog most closely resembles that of the black-tailed prairie dog, C. ludovicianus. Although body size, age of first reproduction, and age of emigration differed between the two study populations (Rayor 1985a), a comparison of social traits did not reveal substantial differences.