Martina Nagy | Friedrich-Alexander-Universität Erlangen-Nürnberg (original) (raw)

Papers by Martina Nagy

1. To make adaptive behavioural decisions, animals must acquire and process information from thei... more 1. To make adaptive behavioural decisions, animals must acquire and process information from their natural and social environment. Reducing uncertainty regarding the actions and goals of conspecifics is especially important for group-living animals. 2. Bats are often highly gregarious and use versatile social vocalizations to mediate social interactions. These social vocalizations encode a substantial amount of ecologically relevant information, such as individual identity, sex and kin. Decoding this information enables receivers to make informed decisions on resource allocation , mate choice, territorial defence and cooperation. Erroneous decisions on such crucial aspects of bats' social behaviour can be costly due to reduced reproductive success or survival. 3. Increasingly complex social interactions require social vocalizations encoding more information which, in turn, could facilitate the evolution of even more complex social interactions. Evidence for the positive correlation of social and vocal complexity is available for several taxa but is currently very limited for bats. 4. We conducted a phylogenetic comparative analysis to link the information content encoded in bats' social vocalizations to the complexity of their social lives, that is the level of uncertainty associated with assessing individual identity. We focused on three different vocalization types encoding individual signatures (pup isolation calls, adult contact calls and male-specific vocalizations). Information content in bit (i.e. the number of binary decisions necessary to discriminate among

Scientific Reports, 2017

Male song in birds and mammals is important for repelling rivals, stimulating mates or attracting... more Male song in birds and mammals is important for repelling rivals, stimulating mates or attracting them to a specific location. Nevertheless, direct experimental evidence for the mate attraction function of male song is limited to a few studies. Here, we provide strong experimental evidence that male songs attract wild female bats (Saccopteryx bilineata). Playbacks of territorial songs reliably elicited phonotaxis in females but not males. Most females captured during playbacks were subadults searching for new colonies to settle in. In S. bilineata, multiple males sing simultaneously at dawn and dusk, thereby creating a conspicuous chorus which encodes information on colony identity and size. Since territorial songs have a large signalling range, male songs constitute acoustic beacons which enable females to localize new colonies. In our playbacks, females strongly preferred local territorial songs over foreign territorial songs from two different locations, indicating that song familiarity influences phonotaxis. Our study provides the first clear experimental evidence that male song elicits female phonotaxis in a non-human mammal. Bats are an especially promising taxon for studying mammalian song since male song has been described in different species with diverse social organisations and natural histories, thus providing exciting opportunities for phylogenetically controlled comparative studies.

With their extraordinary species richness and diversity in ecological traits and social systems, ... more With their extraordinary species richness and diversity in ecological traits and social systems, bats are a promising taxon for testing socio-ecological hypotheses in order to get new insights into the evolution of animal social systems. Regarding its roosting habits, proboscis bats form an extreme by occupying sites which are usually completely exposed to daylight (e.g. tree trunks, vines or rocks). This is accompanied by morphological and behavioural adaptations to remain cryptic in exposed day roosts. With long-term behavioural observations and genetic parentage analyses of individually marked proboscis bats, we assessed its social dispersion and male mating strategy during day and night. Our results reveal nocturnal male territoriality—a strategy which most closely resembles a resource-defence polygyny that is frequent also in other tropical bats. Its contrasting clumped social dispersion during the day is likely to be the result of strong selection for crypsis in exposed roosts and is accompanied by direct female defence in addition to male territoriality. To the best of our knowledge, such contrasting male mating strategies within a single day–night cycle have not been described in a vertebrate species so far and illustrate a possible evolutionary trajectory from resource-defence to female-defence strategy by small ecologically driven evolutionary steps.

Molecular Ecology, 2013

The ultimate causes for predominant male-biased dispersal (MBD) in mammals and female-biased disp... more The ultimate causes for predominant male-biased dispersal (MBD) in mammals and female-biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long-term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father-daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource-defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex-biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.

Journal of General Virology, 2013

Bats host a broad diversity of coronaviruses (CoVs), including close relatives of human pathogens... more Bats host a broad diversity of coronaviruses (CoVs), including close relatives of human pathogens. There is only limited data on neotropical bat CoVs. We analysed faecal, blood and intestine specimens from 1562 bats sampled in Costa Rica, Panama, Ecuador and Brazil for CoVs by broad-range PCR. CoV RNA was detected in 50 bats representing nine different species, both frugivorous and insectivorous. These bat CoVs were unrelated to known human or animal pathogens, indicating an absence of recent zoonotic spill-over events. Based on RNAdependent RNA polymerase (RdRp)-based grouping units (RGUs) as a surrogate for CoV species identification, the 50 viruses represented five different alphacoronavirus RGUs and two betacoronavirus RGUs. Closely related alphacoronaviruses were detected in Carollia perspicillata and C. brevicauda across a geographical distance exceeding 5600 km. Our study expands the knowledge on CoV diversity in neotropical bats and emphasizes the association of distinct CoVs and bat host genera.

Ethology, 2014

Bats live substantially longer than any other similar-sized mammal despite high metabolic rates d... more Bats live substantially longer than any other similar-sized mammal despite high metabolic rates during flight. The underlying causes for the longevity of bats and the question whether bats exhibit signs of senescencea progressive deterioration in performanceare still unclear.

Erlangen, Germany: University of Erlangen- …, 2010

... Also inter-colony genetic heterogeneity was higher among males than among females in Trinidad... more ... Also inter-colony genetic heterogeneity was higher among males than among females in Trinidad populations, indicating that males of a colony are more related to each other than are females (McCracken 1984). The ultimate causes (ie avoidance of inbreeding ...

Biology Letters, 2010

Vocal imitation-the ability to learn a previously unknown acoustic signal from a tutor-is conside... more Vocal imitation-the ability to learn a previously unknown acoustic signal from a tutor-is considered to be a key innovation in the evolution of speech. This faculty is very rare and patchily distributed within the animal kingdom, suggesting multiple instances of convergent evolution. It has long been predicted that bats should be capable of vocal imitation and our results provide evidence for this phenomenon. We report that pups of the bat Saccopteryx bilineata learn a complex vocalization through vocal imitation. During ontogeny, pups of both sexes imitate territorial song from adult males, starting with simple precursor songs that develop into genuine renditions. The resemblance of pup renditions to their acoustic model is not caused by physical maturation effects, is independent of pups' gender and relatedness towards adult males and becomes more pronounced during ontogeny, showing that auditory experience is essential for vocal development. Our findings indicate that the faculty of vocal imitation is more widespread than previously thought and emphasize the importance of research on audiovocal communication in bats for a better understanding of the evolutionary origin of vocal imitation.

Behavioral Ecology and Sociobiology, 2014

Recent evidence suggests that tropical bats may frequently depart from the predominant mammalian ... more Recent evidence suggests that tropical bats may frequently depart from the predominant mammalian malebiased 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.

Behavioral Ecology, 2012

Social groups that are characterized by the presence of male kin are rare in mammals. Theory pred... more Social groups that are characterized by the presence of male kin are rare in mammals. Theory predicts that males reproducing in such groups need to overcome the costs of local mate competition, which are supposedly severe in polygynous or promiscuous mating systems. Here, we studied in a polygynous mammal with male philopatry whether male group size renders direct fitness benefits for males that could outweigh the costs of competing with related males for access to territories and mates. We used long-term behavioral observations and genetic data of the greater sac-winged bat to investigate the factors affecting lifetime breeding success (LBS) of harem males living in colonies that contain varying numbers of male residents. We show that tenure of harem males increased with the number of male coresidents and that harem male tenure explained a large proportion of variation in their LBS. Thus, our results provide evidence that males gain direct fitness benefits from a social organization in colonies that include additional harem territories and nonharem males. Immigration of males into colonies was significantly lower when nonharem males (young males that are often related to harem males) were permanently present in colonies, suggesting that larger male groups may be better able to maintain a patriline in a colony and thus also ensure future indirect fitness benefits.

Animal Behaviour, 2012

Vocal group signatures facilitate group cohesion or the exclusion of nongroup members and thus gr... more 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.

Journal of Mammalogy, 2008

Like many other mammals, Saccopteryx bilineata exhibits a polygynous mating system, in which each... more Like many other mammals, Saccopteryx bilineata exhibits a polygynous mating system, in which each male defends a group of females called a harem. Colonies consist of several harems, and nonharem males roost adjacent to harems. Unlike most other mammals, females disperse from their natal colony and most juvenile males remain in it. Thus, colonies consist of patrilines, which promotes intense local mate competition. Females are in estrus during a few weeks at the end of the rainy season. Mating is most likely initiated by females and preceded by intense courtship displays of males. Forty percent of colony males do not sire any offspring during their tenure in the colony, whereas a few males can sire up to 6 offspring in a single year. Males use olfactory, visual, and acoustic signals for courtship, and they demonstrate territory ownership by scent marks, lowfrequency calls, and visual displays. Harem males sire on average more offspring than do nonharem males but produce only 30% of the offspring within their own harem territory, with 70% being sired by other harem males or nonharem males. Reproductive success of males increases with decreasing size, fluctuating asymmetry, and fundamental frequency of territorial calls. In addition, females that are closely related to the harem holder are more likely to mate with other males than with the harem holder. Sexual selection in S. bilineata is most likely influenced by intense local mate competition caused by scarce roosts and the patrilineal organization of colonies.

Proceedings of The Royal Society B: Biological Sciences, 2007

In most mammals, dispersal rates are higher in males than in females. Using behavioural and genet... more 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.

Conservation Genetics Resources, 2010

Neotropical emballonurid bats are known to exhibit an exceptional diversity in social systems and... more Neotropical emballonurid bats are known to exhibit an exceptional diversity in social systems and dispersal strategies. Here we report the isolation of eight new microsatellite markers which will be employed to investigate ultimate causes and consequences of sex-biased dispersal by use of paternity, relatedness and population structure analyses. Novel microsatellite markers developed for the species Rhynchonycteris naso turned out to be highly polymorphic. Number of alleles ranged from seven to 31 alleles per locus and expected heterozygosities ranged from 0.74 to 0.95. Seven loci were autosomal and one locus appeared to be situated on the X-Chromosome. Cross-species amplification in four species was more successful in more closely related than in more distantly related genera of neotropical emballonurids. Together with other eleven microsatellites initially isolated for Saccopteryx bilineata, we now posses powerful tools for studying species of the two bat genera, Saccopteryx and Rhynchonycteris.

Behavioral Ecology, 2006

Defense of territories in many animal species involves the advertisement of territory holder qual... more Defense of territories in many animal species involves the advertisement of territory holder quality by acoustic signaling. In the sac-winged bat Saccopteryx bilineata, males engage in territorial countersinging when reoccupying their day-roost territories in the morning and in the evening before abandoning the roost for the night. Females roost mainly in male territories, and territory holders are reproductively more successful than nonterritorial males. In territorial songs of male S. bilineata, we distinguished 6 syllable types and parameterized their acoustic properties. The analysis of 11 microsatellite loci allowed assignments of juveniles to their parents. Males had a higher reproductive success both when they uttered more territorial songs per day and when their long buzz syllables had a lower end frequency of the fundamental harmonic. Long buzzes had a harsh quality due to a pulsation of the fundamental frequency at the syllable onset and also had the highest sound pressure level of all syllable types in most territorial songs. Territorial songs and especially long buzz syllables are thus likely to advertise territory holder quality and competitive ability. http://beheco.oxfordjournals.org/ Downloaded from Behr et al. • Territorial songs indicate male quality in the sac-winged bat 811 by guest on October 27, 2014 http://beheco.oxfordjournals.org/ Downloaded from Behr et al. • Territorial songs indicate male quality in the sac-winged bat 817 by guest on October 27, 2014 http://beheco.oxfordjournals.org/ Downloaded from