Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus

Many studies assume that selection molds social traits and have investigated the manner in which this occurs, yet very few studies have measured the strength of selection on social traits in natural populations. In this paper, I report results of phenotypic selection analyses on two social traits – the size of social groups and the frequency of group foraging – in Phyllostomus hastatus, the greater spear-nosed bat. I found significant positive directional selection on individual group foraging frequency, but no directional selection on individuals in different-sized social groups. These results have implications for the structure of social groups, cooperative behavior among group mates, and maternal investment strategies. I argue that combining studies of natural selection on wild populations with experiments to identify the agents and mechanisms of selection can do much to increase our understanding of social evolution.     

Greater spear-nosed bats give group-distinctive calls

Individually distinctive vocalizations are ubiquitous; however, group distinctive calls have rarely been demonstrated. Under some conditions, selection should favor calls indicating social group membership in animals that forage in groups. Greater spear-nosed bats (Phyllostomus hastatus) give calls that appear to facilitate recognition of social group mates who are unrelated. Females give loud broadband (4–18 kHz) vocalizations termed screech calls when departing on foraging trips and at foraging sites. Screech calls help to establish foraging groups among social group members, and to maintain contact over the long distances they travel while foraging. I test two hypotheses about how screech calls may be structured to convey caller identity. Individual calls may be distinct and group members may learn to recognize each individual's calls and to associate the individual with the social group. Alternatively, groups may give distinct calls and individuals within groups may share call characteristics. To test these hypotheses I conducted multivariate acoustic analysis of multiple calls from 28 bats from three social groups. Although the ubiquity of individually distinctive calls in other taxa makes this result more likely, the results reveal that group calls are highly distinctive. Individual bats within groups are statistically indistinguishable. Calls appear to decrease slightly in frequency as bats age. Call convergence among unrelated group mates implies vocal learning in this species. Received: 28 March 1996 / Accepted after revision: 6 October 1996     

Social influences on territorial signaling in male greater sac-winged bats

Acoustic territorial displays are common among birds but comparatively rare among mammals. An exceptionally vocal mammal well-known for its elaborate territorial displays is the polygynous greater sac-winged bat, Saccopteryx bilineata. Male S. bilineata are often philopatric and establish small territories in their birth colony in which females can roost during the day. During territorial defense, males produce complex territorial songs that are learned through vocal imitation. Territorial songs are mainly produced at dawn and dusk. We studied social influences on male vocal activity and the occurrence of vocal signatures in territorial songs of 27 male S. bilineata from 12 different-sized colonies in Panama. Males produced significantly more territorial songs when they had more territorial neighbors or when they had females roosting in their territories, indicating that male vocal activity rises with increasing male–male competition. Territorial songs are multisyllabic vocalizations with low-frequency buzz syllables being most prominent. We found statistical evidence for a pronounced individual signature encoded in the buzz syllables of territorial songs that could facilitate individual recognition among rival neighbors. Additionally, we found a vocal group signature in territorial songs, suggesting that young males may learn territorial songs from more than one tutor male. Resident male S. bilineata appear to cooperatively defend their colony against male intruders, making a group signature in territorial songs potentially advantageous.     

Postcopulatory mate guarding by vocalization in the Formosan squirrel

The Formosan squirrel, Callosciurus erythraeus thaiwanensis, emitted different vocalizations in response to terrestrial and aerial predators and snakes. Each vocalization caused nearby individuals to adopt a different type of anti-predator behaviour. In mating bouts, males produced two types of loud calls: precopulatory calls, emitted before copulations, and postcopulatory calls, emitted after copulations. The latter continued for 17 min on average. The estrous female and other males attending the mating bouts stopped moving during the postcopulatory call, so that the calling male was able to tend the female without interruption. The sound characteristics of anti-terrestrial-predator and postcopulatory calls recorded in the captivity were compared, and none of the ten characters of duration and frequency measured differed between the two calls. Playback experiments also showed that responses to the sounds in two different contexts, escape behaviour and defensive immobility, did not differ. The similarity between anti-predator and postcopulatory calls is discussed with reference to the possibility of manipulation and other explanatory hypotheses.     

High altitude echolocation of insects by bats

Summary The orientation sounds of many bats, almost certainly belonging to the genus Tadarida, were recorded at altitudes of 100 to 300 m above the ground by means of an ultrasonic radio microphone. Both in North Queensland, Australia, and in southern Utah and Nevada, USA, bats were often more numerous at 200 to 300 m than near the ground. Rapid increases in pulse repetition rate often indicated that these bats were actively hunting flying insects. The absence of clutter at high altitudes may significantly facilitate the detection and capture of insect prey.     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Mate guarding and gallivanting by male hoary marmots (Marmota caligata)

Summary Seven years data on the vernal behavior of hoarty marmots, Marmota caligata, suggest that males engage in a two-part reproductive strategy, which consists of guarding their mates against possible copulation with additional males, and also gallivanting — wandering about in search of additional reproductive opportunities for themselves. Data are presented which support seven predictions derived from the assumption that mate guarding and gallivanting are parts of a reproductive strategy by male marmots.     

Interindividual use of echolocation calls: Eavesdropping by bats

Summary The use of other individual's echolocation calls by little brown bats, Myotis lucifugus, was tested by observing the response of free-flying bats to presentations of recorded echolocation calls and artificial sounds. Bats responded by approaching conspecific calls while searching for food, night roosts, nursery colonies and mating/hibernation sites. Response was low or non-existant to other sounds. While searching for prey, M. lucifugus also responded to the echolocation calls of Eptesicus fuscus, a sympatric species with overlapping diet but distinctly different echolocation calls. Subadults were especially responsive to conspecific calls.All four situations in which the bats responded involve patchily distributed resources at which bats accumulate. Concentrations of echolocation calls thus likely serve as cues regarding the location of resources. Individuals approaching feeding groups, for example, could increase prey detection range by up to 50 times over individuals relying solely on their own echolocation.Although the costs associated with eavesdropping may be negligible for M. lucifugus, for other species, particularly territorial ones, being conspicuous may be a disadvantage and the possibility of being over-heard by other bats may have been one factor involved in the evolution of echolocation call design.     

Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda

Cooperative mate guarding by males is unusual in mammals and birds, largely because fertilizations are non-shareable. Chimpanzees live in fission-fusion communities that have cores of philopatric males who cooperate in inter-group aggression and in defending access to the females in their community. Male contest mating competition is restrained within communities, but single high-ranking males sometimes try to mate guard estrous females. Data from an unusually large chimpanzee commmunity at Ngogo, Kibale National Park, Uganda, that contains more males than any previously studied community show new variation in chimpanzee mate-guarding behavior. Contrary to expectation given the large number of males, mate guarding was as common as, or more common than, at other sites, and males other than the alpha male guarded more often. More strikingly, pairs or trios of top-ranking males sometimes engaged in cooperative aggression to prevent estrous females from mating with other males, but tolerated each other's mating activities. Both single males and coalitions mostly guarded periovulatory females. Mate-guarding coalitions were previously unknown in chimpanzees. Coalitions occurred in large mating parties, seemingly because these often contained too many males for single males to maintain exclusive access to estrous females. Coalition members gained higher shares of copulations than they could have expected from solo mate guarding, and suffered lower per capita costs of guarding (as inferred from aggression rates). Two males who most often participated in coalitions formed two-male coalitions at about the point where the number of males present made it unlikely that either could get 50% or more of total copulations on his own, and formed trios when this value dropped below 33%. Kin selection could be a factor in cooperation among male chimpanzees, but coalition members were not necessarily close relatives and the apparent structure of payoffs fit that of mutualism. Furthermore, reliance of male chimpanzees on support from allies to maintain high rank could have led to trading of mating exclusivity for support against mating competitors. Received: 28 May 1997 / Accepted after revision: 16 May 1998     

Oviposition site guarding by male walnut flies and its possible consequences for mating success

Field studies showed that male Rhagoletis juglandis and R. boycei flies guard egg-laying punctures (and the eggs within) on host walnut (Juglans major) fruit and defend those sites from conspecific and heterospecific males. In field experiments with artificially punctured fruit,as well as field observations on unmanipulated fruit, males were consistently more likely to be sighted and stayed longer on damaged fruit than on undamaged fruit. On artificially punctured fruit, they consistently spent more time in the vicinity of a puncture than expected by chance alone. Males together on damaged fruit were more likely to engage in contests over those fruit than males together on undamaged fruit. Copulations were consistently more frequent for either species on damaged than undamaged fruit, both in observations of unmanipulated fruit and in artificial puncture experiments. Analyses which controlled for the longer male residence time on damaged fruit suggested strongly that copulations were consistently achieved at higher per capita rates on damaged than on undamaged fruit, indicating that puncture-guarding functions to increase access to females. An exception to the pattern in male mating success was noted at a site where both species used host fruit on the same trees. In this case, R. juglandis males were only slightly more common on punctured fruit than on control fruit and male success in copulation did not differ significantly between the two types of fruit. This anomalous result was apparently due to an almost absolute advantage enjoyed by R. boycei males in on-fruit contests with R. juglandis males. A likely basis for improvements in mating success associated with puncture guarding was a propensity for females to deposit eggs into existing punctures. Both in observations of unmanipulated fruit and in artificial puncture experiments, females consistently attempted oviposition more often in damaged than undamaged fruit. In artificial puncture experiments, both species at both sites deposited most clutches in damaged fruit. Mating generally took place as females initiated oviposition. The possible functions of puncture use by females as well as alternative functions of puncture guarding by males are discussed.     

Chemosensory mate recognition may facilitate prolonged mate guarding by male snow skinks, Niveoscincus microlepidotus

We provide evidence that male lizards can use chemosensory cues to identify individual females and probably therefore maintain long-term associations with these females in the wild. In the laboratory, males preferentially followed the scent trail of their vitellogenic female “partner” rather than that of another vitellogenic female. Our 5-year field study of the small viviparous scincid lizard (Niveoscincus microlepidotus) in alpine Tasmania showed that sexually mature males and females commonly formed “pairs” for long periods (on average 29 days). These pairs occurred primarily during the mating season, always involved one adult male and one adult female, and usually involved vitellogenic rather than gravid females. Our laboratory experiments suggest that a significant factor in maintaining those prolonged partnerships is male scent trailing of partners. Received: 28 October 1997 / Accepted after revision: 28 May 1998     

Non-aggressive mate guarding by the blue-footed booby: a balance of female and male control

Thirteen pairs of blue-footed boobies (Sula nebouxii) were observed on their colony. Pairs courted frequently and, on average, copulated 24 times during the 30 days before laying, with 38% of those copulations occurring in the last 5 days (presumed fertile period). Males and females increased attendance at the nest site as laying approached. Seven females performed an average seven extra-pair copulations, with 1–2 paired male neighbors, but these were less concentrated in the presumed fertile period than within-pair copulations, and the last two copulations of all 7 females were with their social mates. Rates of female extra-pair copulations were six times lower when their social mate was present, and during the presumed fertile period, no female performed an extra-pair copulation in the presence of her mate. Males did not respond to infidelity of social mates with aggression, prompt copulation, retaliatory copulation, or increase in copulation. Seven of 13 males performed an average of five extra-pair copulations, with 1–3 paired female neighbors, before their own mates began egg-laying. The males' extra-pair copulations represented only 4% of their total copulations during their own mates' presumed fertile periods. Females, the larger sex, apparently control sexual access and copulate with extra males to achieve extra-pair fertilization. Males pursue a mixed strategy: they copulate with extra females, mostly outside their own mate's presumed fertile period, and they copulate increasingly with their social mate as laying approaches, probably assuring some paternity by mate guarding, involving attendance and courtship. Behavior of males and females is also consistent with other hypotheses for extensive joint nest site attendance: pairbonding, copulation access, and territory acquisition. Received: 14 November 1997 / Accepted after revision: 16 May 1998     

Male copulatory guarding enhances female foraging in a water strider

Summary In the laboratory, females of Gerris remigis foraging singly after being separated from a copulating male averaged 16 times longer to repel male copulatory attempts compared to repelling time when copulating (60 trials). In<10 min after separation, all females either became immobile at the edge (in 34% of all trials), or recopulated and either continued to forage (61%) or swam to the edge and became immobile (5%). Copulating females captured 85% of imitation prey, but single females, harassed by males, captured only 32% of prey.During a census of 2 small streams, in the pools with swimming single males, >99% of all swimming females were copulating, <1% being single. Ninety seven percent of all single females were immobile at the edge, whereas only 11% of all pairs were at the edge. In pools without swimming single males, 32% of all single females were swimming, compared to <1% in pools with swimming males. Introductions of a male into 4 pools with a female swimming singly in each resulted in the females either becoming immobile at the edge or copulating. The 2 streams had a : sex ratio of 1.6:1, and 79% of all females were copulating during the census. Foraging, copulation and copulatory attempts continued at a reduced level during the night.Thus in streams where male G. remigis are attempting to copulate, females can forage effectively only by carrying a copulating male who apparently repels copulatory attempts by other males.     

Discovery of postcopulatory mate guarding in Copepoda Harpacticoida (Crustacea)

Mating behaviour of four species of Tisbe (Tisbidae) and of Paramphiascella fulvofasciata (Diosaccidae) was filmed with a videocamera during 1992 and 1993 at the University of Oldenburg. This behaviour is complex and can be divided into different phases: grasping of the female; courtship; copula and postcopulatory mate guarding. During courtship both partners lie parallel in opposite directions with their ventral sides facing each other. The male strokes the abdomen of the female with his second to fourth peracopods. As a result the female becomes motionless. The copula is a quick process of only a few seconds during which spermatophore transfer takes place. When this has happened, males do not leave the females but become inactive and are carried around by them for varying lengths of time. This pattern and the fact that only adult partners are involved in these associations prove that this behaviour is very different from the precopulatory mate guarding presumed to be ubiquitous among Harpacticoida. Cases of postcopulatory mate guarding have never been explicitly demonstrated for Harpacticoida. The minimum duration of guarding was found to match the time necessary for spermatophore discharge. Guarding is, therefore, interpreted as a strategy to secure paternity. New definitions are given for courtship, copula and postcopulatory mate guarding in Harpacticoida to help avoiding misinterpretations of associations between adult partners. Such misinterpretations abound in the literature.     

Behaviour of bats during a lunar eclipse

Summary The hunting activity of tropical bats was observed during a lunar eclipse at night. During the eclipse, the activity was significantly higher than before and after when the bright full moon was visible. The decrease of hunting activity in bright light is interpreted as a direct adaptation to the light conditions, whereas endogenous factors seem not to be involved. The possible role of predators feeding on bats is discussed.     

Brood guarding and the evolution of male parental care in burying beetles

Summary Parental behavior that has an impact on the increased survival of offspring, an important factor in the evolution of parental care, can include both guarding and provisioning. The effects of these two components of parental care can be separated and quantified in the burying beetle Nicrophorus orbicollis in which both male and female cooperate to rear young. Although in the absence of competition, reproductive success is reduced by the presence of the second parent in the brood chamber, two parents dramatically reduce the probability that conspecifics will usurp the resource, replace either the male or female, kill the newly hatched brood, and produce a replacement clutch. After the establishment of the burial chamber (but not before) beetles appear to assist their mates in driving off intrasexual competitors. Male assistance in burial does not account for very much of the variance in the speed in which the carcass can be concealed nor are two parents essential to guard against insect predators. There were no significant differences in the duration of parental care by males paired with virgin and non-virgin females suggesting that paternity of the brood for which the male provides care is not a factor determining the length of care. Since male and female reproductive success is limited in Nicrophorus by access to suitable carcasses, many of the typical asymmetries in the costs and benefits of parental care are lacking. However since sperm displacement is not complete, paternity of the replacement clutch, for which the male does not provide care, may be a factor encouraging male desertion before female desertion. Other factors important in the evolution of paternal care, especially the probability of additional reproductive opportunities, are discussed.     

Trade-off between mate guarding and mate attraction in the polygynous great reed warbler

Summary In a Swedish population of the polygynous great reed warbler Acrocephalus arundinaceus, about 40% of the males formed pairs with more than one female. Males sang two completely separated types of song: (1) long song when they tried to attract mates and (2) short shong when they guarded a fertile female. As soon as a male had attracted a female he immediately switched from long to short song and apparently guarded her for at least 3 days. Most males left their female and started singing long several days before her fertile period ended. This behavior probably increased the risk of cuckoldry. By assuming that males of polygynous species maximize their fitness over the whole breeding season (i.e., maximize fitness rate), we predicted longer mate guarding periods when the probability of attracting a second female was low and the risk of cuckoldry was high. These predictions were supported by observations. The probability of attracting a second female decreased during the breeding season and, in accordance, the number of days that males sang long song during the primary female's fertile period was negatively correlated with the time of the season. This trend held also for individual males when comparing mating periods of their primary and secondary female. The increasing rate of male intrusions with season may also have contributed to the increasing mate guarding periods. Offprint requests to: D. Hasselquist