Greater Sac-winged Bat Research Articles

Evidence of female preference for odor of distant over local males in a bat with female dispersal

AbstractGeographic variation of sexually selected male traits is common in animals. Female choice also varies geographically and several studies found female preference for local males, which is assumed to lead to local adaptation and, therefore, increases fitness. As females are the nondispersing sex in most mammalian taxa, this preference for local males might be explained by the learning of male characteristics. Studies on the preference of females in female-dispersing species are lacking so far. To find out whether such females would also show preferences for local males, we conducted a study on greater sac-winged bats (Saccopteryx bilineata), a species where females disperse and males stay in their natal colony. Male greater sac-winged bats possess a wing pouch that is filled with odoriferous secretion and fanned toward females during courtship display. In a combination of chemical analysis and behavioral preference tests, we analyzed whether the composition of wing sac secretion varies between two geographically distinct populations (300 km), and whether females show a preference for local or distant male scent. Using gas chromatography, we found significant differences in the composition of the wing sac odors between the two geographically distinct populations. In addition, the behavioral preference experiments revealed that females of both populations preferred the scent of geographically distant males over local males. The wing sac odor might thus be used to guarantee optimal outbreeding when dispersing to a new colony. This is—to our knowledge—the first study on odor preference of females of a species with female-biased dispersal.

Pup Directed Vocalizations of Adult Females and Males in a Vocal Learning Bat

Social feedback plays an important role in human language development and in the vocal ontogeny of non-human animals. A special form of vocal feedback in humans, infant-directed speech – or motherese –facilitates language learning and is socially beneficial by increasing attention and arousal in the child. It is characterized by high pitch, expanded intonation contours and slower speech tempo. Furthermore, the vocal timbre (i.e. ’color’ of voice) of motherese differs from the timbre of adult-directed speech. In animals, pup-directed vocalizations are very common, especially in females. But so far there is hardly any research on whether there is a similar phenomenon as motherese in animal vocalizations. The greater sac-winged bat, Saccopteryx bilineata, is a vocal production learner with a large vocal repertoire that is acquired during ontogeny. We compared acoustic features between female pup-directed and adult-directed vocalizations and demonstrated that they differed in timbre and peak frequency. Furthermore, we described pup-directed vocalizations of adult males. During the ontogenetic period when pups’ isolation calls (used to solicit maternal care) are converging towards each other to form a group signature, adult males also produce isolation calls. Pups’ isolation calls are acoustically more similar to those of males from the same social group than to other males. In conclusion, our novel findings indicate that parent-offspring communication in bats is more complex and multifaceted than previously thought, with female pup-directed vocalizations reminiscent of human motherese and male pup-directed vocalizations that may facilitate the transmission of a vocal signature across generations.

MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal.

Major histocompatibility complex (MHC) genes play a pivotal role in vertebrate self/nonself recognition, parasite resistance and life history decisions. In evolutionary terms, the MHC’s exceptional diversity is likely maintained by sexual and pathogen-driven selection. Even though MHC-dependent mating preferences have been confirmed for many species, the sensory and genetic mechanisms underlying mate recognition remain cryptic. Since olfaction is crucial for social communication in vertebrates, variation in chemosensory receptor genes could explain MHC-dependent mating patterns. Here, we investigated whether female mate choice is based on MHC alleles and linked to variation in chemosensory trace amine-associated receptors (TAARs) in the greater sac-winged bat (Saccopteryx bilineata). We sequenced several MHC and TAAR genes and related their variation to mating and paternity data. We found strong evidence for MHC class I-dependent female choice for genetically diverse and dissimilar males. We also detected a significant interaction between mate choice and the female TAAR3 genotype, with TAAR3-heterozygous females being more likely to choose MHC-diverse males. These results suggest that TAARs and olfactory cues may be key mediators in mammalian MHC-dependent mate choice. Our study may help identify the ligands involved in the chemical communication between potential mates.

Multidimensionality of Chemical Information in Male Greater Sac-Winged Bats (Saccopteryx bilineata)

The complexity of social signals is thought to depend on the complexity of social systems, but evidence from wild animals is scarce. Here, we investigated the chemical information provided by individual male greater sac-winged bats (Saccopteryx bilineata), a small, long-lived neotropical bat species with a harem-polygynous mating system. We analysed the chemical fingerprints of wing-sac liquids that are displayed by males in front of females. Specifically, we tested if fingerprints of 45 males included information about age (adult, juvenile), year of sampling, and distance between colonies. We confirmed age-specific differences in male-specific substances, but show furthermore that chemical fingerprints correlate with year of collection and distance between colonies. Thus, the wing-sac chemistry of male S. bilineata conveys a multitude of information, which can potentially be used by conspecifics, especially by females to assess the status of potential mates. Our study provides evidence for a multidimensionality of chemical information in a free-ranging mammal with high social complexity.

Responsiveness to conspecific distress calls is influenced by day-roost proximity in bats (Saccopteryx bilineata).

Distress calls signal extreme physical distress, e.g. being caught by a predator. In many bat species, distress calls attract conspecifics. Because bats often occupy perennial day-roosts, they might adapt their responsiveness according to the social relevance in which distress calls are broadcast. Specifically, we hypothesized that conspecific distress calls broadcast within or in proximity to the day-roost would elicit a stronger responsiveness than distress calls broadcast at a foraging site. We analysed the distress calls and conducted playback experiments with the greater sac-winged bat, Saccopteryx bilineata, which occupies perennial day-roosts with a stable social group composition. S. bilineata reacted significantly differently depending on the playback's location. Bats were attracted to distress call playbacks within the day-roost and in proximity to it, but showed no obvious response to distress call playbacks at a foraging site. Hence, the bats adapted their responsiveness towards distress calls depending on the social relevance in which distress calls were broadcast. Distress calls within or in proximity to the day-roost are probably perceived as a greater threat and thus have a higher behavioural relevance than distress calls at foraging sites, either because bats want to assess the predation risk or because they engage in mobbing behaviour.

Learned vocal group signatures in the polygynous bat Saccopteryx bilineata

Vocal group signatures facilitate group cohesion or the exclusion of nongroup members and thus greatly affect the social system of any given species. This is especially significant for highly mobile animals such as bats. The greater sac-winged bat, Saccopteryx bilineata, lives in a harem-based resource defence polygyny with patrilineal kin groups and female-biased natal dispersal. Pups of both sexes produce isolation calls to elicit maternal care. We analysed isolation calls from 25 pups born in seven different social groups in search of vocal signatures. In addition to a constant individual signature, isolation calls exhibited a group signature that became more prominent during ontogeny. Call convergence of fellow pups was independent of relatedness among pups and not driven by maturation effects, showing that the group signature was acquired through social modification, a form of vocal production learning. Behavioural observations of free-living bats indicated that isolation calls were used by adult males to appease more dominant males and to court unfamiliar females. The learned group signature in isolation calls may function as a ‘password’ that reliably associates individuals with their natal colony. This, in turn, could facilitate male harem acquisition and female inbreeding avoidance in the polygynous S. bilineata. The flexibility inherent in the vocal-learning process guarantees that crucial information can be promoted even under shifting social circumstances.

Differences in plasma testosterone levels related to social status are more pronounced during mating than nonmating season in the tropical bat Saccopteryx bilineata (greater sac-winged bat)

Testosterone (T) concentrations often covary strongly with mating activities in temperate-zone vertebrates. Recent studies suggest that males of tropical species experience lower and year-round constant T levels. Here we studied plasma T concentrations in a tropical mammal with a seasonally invariant social system, the greater sac-winged bat ( Saccopteryx bilineata (Temminck, 1838)). Colony composition remains almost stable throughout the year, although mating is restricted to only a few weeks each year. Males follow one of two mating strategies: they either defend a territory with a female group (harem) or live peripheral without females. First, we compared T within the same individuals between seasons, asking whether T levels are higher during mating season. Second, we tested whether T levels are related to social status, and third, whether T correlates with parasite infection because of an immunosuppressive effect. We found high individual T variations. Testosterone was elevated during the mating season only in harem males and was, on average, higher than in peripheral males. We found no correlation between T and parasite infestation. Although reproduction is seasonal in S. bilineata, T concentrations showed no pronounced seasonal pattern, probably because colony members form long-term relationships and live in a year-round stable social system.

Frequency alternation and an offbeat rhythm indicate foraging behavior in the echolocating bat, Saccopteryx bilineata

The greater sac-winged bat, Saccopteryx bilineata (Emballonuridae), uses two distinct echolocation call sequences: a 'monotonous' sequence, where bats emit ~48 kHz calls at a relatively stable rate, and a frequency-alternating sequence, where bats emit calls at ~45 kHz (low-note call) and ~48 kHz (high-note call). The frequencies of these low-high-note pairs remain stable within sequences. In Panama, we recorded echolocation calls from S. bilineata with a multi-microphone array at two sites: one a known roosting site, the other a known foraging site. Our results indicate that this species (1) only produces monotonous sequences in non-foraging contexts and, at times, directly after emitting a feeding buzz and (2) produces frequency-alternating sequences when actively foraging. These latter sequences are also characterized by an unusual, offbeat emission rhythm. We found significant positive relationships between (1) call intensity and call duration and (2) call intensity and distance from clutter. However, these relationships were weaker than those reported for bats from other families. We speculate on how call frequency alternation and an offbeat emission rhythm might reflect a novel strategy for prey detection at the edge of complex habitat in this ancient family of bats.

The ontogeny of courtship behaviours in bat pups (Saccopteryx bilineata)

Summary In mammals, adult behaviour patterns are often expressed by juveniles throughout ontogeny. In bats, many social behaviours develop before pups are weaned, but the ontogeny of social behaviours in juvenile bats is largely unexplored. We studied bat pups’ social behaviour, specifically the solicitations for maternal care in the greater sac-winged bat, Saccopteryx bilineata. Solicitation periods were prolonged (up to 25 min) and consisted of conspicuous behavioural interactions between pups and their mothers. Since solicitation periods could be initiated by pups or mothers, their duration is probably not caused by a conflict over nursing alone. Solicitation periods were the second most prevalent use of activity time in pups. Some pup behaviours resembled the courtship behaviours of adult males and these incipient courtship behaviours occurred most often within solicitation periods. Both length and complexity of solicitation periods increased significantly during ontogeny but there was no significant difference between male and female pups. Also, the activity outside of solicitation periods was not significantly different between pups of both sexes, even though their activity differs remarkably as adults. Prolonged solicitation periods of S. bilineata pups might be comparable to mammalian play and potentially function as practice for adult courtship behaviours.

Temporal and Spatial Distribution of Male Scent Marks in the Polygynous Greater Sac-Winged Bat

Scent marks are relatively long-lived signals that can be perceived by conspecifics when the producer is absent. Therefore, it is often not obvious to whom the signal is directed. In daytime roosts of the polygynous greater sac-winged bat, males scent mark territories with facial gland secretions. Territories are a valuable resource for males, as they offer exclusive courtship opportunities, which results in increased male reproductive success and, consequently, increased male-male competition over territories. The information encoded in male scent marks could, therefore, be either directed at females as part of an olfactory courtship display or at male competitors as part of territorial behaviour. We expected territorial males to scent mark in the morning, shortly before females return to the territory and close to female roosting sites, if scent marks are directed at females as part of the courtship display. And we expected harem males to scent mark at the territory boundaries, where male-male encounters are most likely to occur, if scent marks are directed at male competitors. We found that males marked more frequently in the afternoon, at a time when all females have already left the territory, and harem males marked at the territory boundaries and not inside their territory in the area where females roost. At boundaries males fan volatiles from specialised wing sacs towards competitors outside the territory. Scent marking of male Saccopteryx bilineata might therefore be congruent with the assessment-hypothesis, which states that scent marks offer intruders the possibility to make an olfactory assessment of the territory owner without direct physical interaction. Thus, scent marks of male S. bilineata are most likely influenced by male-male competition and not by female choice.

Histological examinations of facial glands in Saccopteryx bilineata (Chiroptera, Emballonuridae), and their potential use in territorial marking

Scent marking is widespread among individuals of Mammalia species, especially in resource defence social systems. Apart from urine and faeces that are used for claiming resource ownership, specialised scent glands are the main source of secretions in scent marking individuals. Most previous studies have described secretory epithelia macroscopically, since many glands are conspicuous. But macroscopically inconspicuous scent glands or morphological structures might then be overlooked. In Saccopteryx bilineata (greater sac-winged bat), behavioural observations suggest that both sexes have, apart from the conspicuous gular glands of males, specialised facial glands to display territorial marking. We investigated the facial glands of two males and one female S. bilineata histologically and found, first, that both sexes possess a bilateral symmetrically intermandibular gland, which is composed of a bed of modified apocrine sudoriferous cells. Second, we found lip glands consisting of modified apocrine sudoriferous cell units with pigmented ducts around the upper and the lower lip. Both gland types are probably involved during territorial marking.

Nonmutual vocal mother–pup recognition in the greater sac-winged bat

We investigated the acoustical component of the recognition process leading to successful mother–pup reunions in the greater sac-winged bat, Saccopteryx bilineata, using both a statistical approach and playback experiments. Statistical evidence for individual distinctiveness was found in the isolation calls uttered by pups and, to a weaker degree, in the echolocation pulse trains emitted by mothers. In contrast to other bat species, isolation calls of S. bilineata pups were complex and multisyllabic, with most of the vocal signature information encoded in the composite syllables at the end of calls. Playback experiments with free-living bats revealed that mothers were able to discriminate between their own pup and an alien young on the basis of isolation calls alone, which confirms the results of the acoustical analysis on vocal signatures in isolation calls. Pups, on the other hand, indiscriminately vocalized in response to echolocation pulse trains from their own and alien mothers, rendering the mother–pup recognition process unidirectional. The one-sidedness of the vocal recognition process in S. bilineata as well as in other bat species might be explained by a lack of selection pressures that shape mutual vocal parent–offspring recognition in other species of mammals and birds. To our knowledge, this study is the first in which playbacks were used to elicit antiphonal calling behaviour between bat mothers and pups experimentally. We argue that vocal responses to playback stimuli are a more feasible and reliable response measure for conducting mother–pup recognition playbacks in bats than the phonotaxis behaviour used in the past.

Assessment of fecal testosterone metabolite analysis in free-ranging Saccopteryx bilineata (Chiroptera: Emballonuridae)

ABSTRACT Acquiring hormonal data from small, free-ranging mammals can be challenging when conventional techniques pose too much stress on animals, e.g., by trapping, handling, and bleeding. We assessed the feasibility of measuring plasma testosterone levels indirectly via fecal testosterone metabolites (Tmet) in a small, tropical mammal, the greater sac-winged bat. Saccopteryx bilineata forms stable, harem-polygynous societies, in which males defend female groups throughout the whole year. Firstly, we validated fecal Tmet measurements by performing a challenge experiment using gonadotropin releasing hormone (GnRH). Secondly, we compared Tmet concentrations of harem males and subordinate males in fecal samples collected during the mating season, expecting that fecal Tmet concentrations should be higher in harem than in subordinate males. Thirdly, we monitored fecal Tmet concentrations, courtship intensity and territoriality of harem males during and after the mating season, expecting that fecal Tmet values...

Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny.

In most mammals, dispersal rates are higher in males than in females. Using behavioural and genetic data of individually marked bats, we show that this general pattern is reversed in the greater sac-winged bat (Saccopteryx bilineata). Dispersal is significantly female biased and male philopatry in combination with rare male immigration causes a patrilineal colony structure. Female dispersal helps avoid father-daughter inbreeding, as male tenure exceeds female age at first breeding in this bat species. Furthermore, our data suggest that females may engage in extra-harem copulations to mate with genetically dissimilar males, and thus avoid their male descendants as mating partners. Acquaintance with the natal colony might facilitate territory takeover since male sac-winged bats queue for harem access. Given the virtual absence of male immigration and the possible lower reproductive success of dispersing males, we argue that enhancing the likelihood of settlement of male descendants could be adaptive despite local mate competition. We conclude that resource defence by males is important in promoting male philopatry, and argue that the potential overlap of male tenure and female first conception is the driving force for females to disperse.