Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.
Citation: Carter G, Leffer L (2015) Social Grooming in Bats: Are Vampire Bats Exceptional? PLoS ONE 10(10): e0138430. doi:10.1371/journal.pone.0138430
Editor: Danilo Russo, Università degli Studi di Napoli Federico II, ITALY
Received: June 26, 2015; Accepted: August 30, 2015; Published: October 7, 2015
Copyright: © 2015 Carter, Leffer. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Data Availability: Data are available from Figshare: (http://figshare.com/s/b8a717681c3611e587c106ec4bbcf141).
Funding: This research was supported in part by a grant to the University of Maryland from the Howard Hughes Medical Institute through the Science Education Program.
Competing interests: The authors have declared that no competing interests exist.
Long-term cooperative relationships are most evident in primates [1–6], but evidence for similar social relationships has been accumulating for several other social vertebrate groups [3, 7, 8], including cetaceans [9, 10], bats , elephants , hyenas [13–15] and ravens [16–20]. The functional importance of these complex social relationships across different species may have led to similar cognitive or behavioral mechanisms for manipulating social bonds [19–24]. A prime example of such a mechanism is social grooming—the cleaning of the body by a partner. Experimental and observational studies show that primate social grooming can be ‘exchanged’ for multiple social benefits, including reciprocal grooming, social tolerance, access to food, and agonistic support [1, 25–37]. Individuals can spend up to 20% of their time grooming others , and the behavior provides proximate physiological rewards for both givers and receiver [39–41]. Although most of what is known about social grooming comes from studies of primates, evidence for a role of social grooming in maintaining social ties is emerging from several other mammals (marsupials , deer , cows , horses , voles , mice , meerkats [48, 49], coati [50, 51], lions ) and group-living birds [53, 54].
In bats, adult social grooming is female-biased in species with female philopatry [55–58], and has been most studied in the common vampire bat (Desmodus rotundus) [55, 59–60]. Kerth et al.  compared social grooming rates of vampire bats with the temperate and insectivorous Bechstein’s bat (Myotis bechsteinii). These two species both have long lifespans and demonstrate fission-fusion social dynamics, where individuals maintain long-term social associations while moving between several roost trees [61–63]. In both species, social grooming rates among individuals were not predicted by self-grooming or numbers of parasites [55, 57]. Bechstein’s bats spent more time grooming themselves (38% of their time in roosts) compared with vampires (23% of their roosting time), but wild vampire bats spent about 5% of their roosting time grooming others, which is 2–4 times higher than Bechstein’s bats [57, 64].
Patterns of social grooming among categories of individuals also differed between the two species. In the Bechstein’s bat, adult female social grooming was not detectably symmetrical, and was predicted by kinship, occurring mostly between adult mothers and daughters, sometimes between sisters, and only rarely between non-kin . In vampires, female social grooming was highly symmetrical and relatively common among non-kin, where it correlated with co-roosting association and food sharing [55, 60].
It is not entirely clear if vampire bat social grooming is typical or exceptional when compared to other bats or non-primate mammals. One hypothesis is that social grooming in vampire bats is exceptional in quantity and quality, because it is related to their uniquely cooperative food sharing behavior . Like many primates, reciprocal patterns of vampire bat food sharing and social grooming extend beyond mother-offspring bonds, suggesting they may provide both direct and indirect fitness benefits [11, 60, 65]. Among bats, the common vampire has an extraordinarily large brain and neocortex for its body size [66, 67]. In primates, increased neocortex size has been linked to higher metrics of social complexity, such as social grooming network size  and strategic deception .
Alternatively, the apparent distinctiveness of vampire bat social grooming might stem from purely ecological factors. Social grooming may be more obvious in vampire bats due to higher levels of ectoparasite infestation. Bat fly density has been linked to species-level grooming rates  and the two vampire species that were observed ranked 5th and 6th place out of 53 neotropical bats for average number of parasitic streblid flies per bat . A sampling bias could also over-emphasize social grooming in vampire bats, because there is much effort focused on studying vampire bat social behavior  and a lack of data on social grooming in other bats.
Comparing social grooming data across studies can be difficult due to study differences in ectoparasite density, temperature, sampling method, visibility, and level of human disturbance. In this study, we took advantage of an opportunity to compare captive vampire bats with four other captive group-living bat species housed at the same facility under the same light/dark schedule, temperature, humidity, and levels of human disturbance. We compared adult-to-adult social grooming in vampire bats Desmodus rotundus, two frugivorous bats Carollia perspicallata and Artibeus jamaicensis (Family: Phyllostomidae) and two Paleotropical fruit bats, Rousettus aegyptiacus and Eidolon helvum (Family: Pteropodidae). Importantly, the adult bats we compared have fixed levels of social association (stable group composition) and no insect ectoparasites.
All bats were cared for by the Organization for Bat Conservation (at the Cranbrook Institute of Science, Bloomfield Hills, Michigan; under permits: USDA 34-C-0117; US Fish and Wildlife Service MB003342-0), and housed at 25–28 degrees Celsius with >33% humidity on a half-reversed 12 h light/dim light cycle in flight cages that allowed free association among cagemates. Male Artibeus, Carollia, Eidolon, and Rousettus were housed together (4.5 x 3 x 2 m), while females and a few castrated males (see below) of these species were housed together in a different cage (same dimensions). All Desmodus were housed together (3 x 1.5 x 2 m), but sex could still be assigned with certainty because sexes tended to segregate (into female groups with a dominant male and satellite male groups) and bats were individually marked. In all cages, bats were free to hang at any place in the cage. In all species, we only observed interactions between adult bats, and only one dependent offspring was present (in Desmodus). Work was approved by the University of Maryland Institutional Animal Care and Use Committee (Protocol R-13-30).
To compare social grooming and other behaviors across species, we conducted focal sampling. We took instantaneous (“on the beep”) focal samples of a randomly chosen bat. For Artibeus, Desmodus, and Carollia, we obtained 13 samples from both males and females (see Table 1 for numbers of bats in each cage). For Eidolon and Rousettus, we took 13 samples from males. There was a chance (Eidolon = 1/3, Rousettus = 2/9) that attempts to sample a female bat actually sampled a castrated male, because 6 female Eidolon and 9 female Rousettus were housed with two castrated male Eidolon and two castrated male Rousettus. In Table 1, we therefore refer to this category (female and castrated male) as the “no testes” sample. Observers chose a focal bat randomly by counting bats left to right until a specific random number was reached. If a focal bat was asleep or became lost from view, the observer immediately began focal sampling the next closest bat in the same species and sex category.
During each of 26 focal sampling sessions, observers took one observation every 10 s for 10 min (1,560 observations per species). During each observation, observers reported the presence or absence of social grooming (chewing or licking another bat’s body), self-grooming (scratching or licking its own body), feeding, and aggression. We measured self-grooming to see if social grooming differed merely due to differences in grooming, we measured feeding because feeding rates could limit and hence explain social grooming rates, and we measured aggression to see if this behavior was positively or negatively linked to social grooming. Focal sampling sessions occurred at haphazard times when bats were active. However, using logistic fit in JMP 12 we detected no effect of sample time on presence of social grooming either overall or within each species. Because observers also switched to a different species and sex after each observation, there was no reason to expect biased sampling of sexes or species.
To calculate percent time spent social grooming, self grooming, fighting, or feeding, we divided the number of observations of these behaviors by 60 (the number of samples per session). We compared social grooming rates across both species and sexes. To test if vampire bats performed social grooming more than other species, we conducted nonparametric comparisons using the Dunn Method for joint ranking in JMP 12 with Desmodus as the control species. This method computes ranks on all observations then compares Desmodus to all other species in a pairwise manner, and provides p-values with a Bonferroni adjustment. We repeated this analysis for self-grooming. To test for an effect of sex on social grooming rates, we compared social grooming in males and ‘no testes’ bats across all species using a Wilcoxon test. To compute means and 95% confidence intervals of social grooming rates, we used bootstrapping with 1000 permutations in R .
To check for potential inter-observer bias, we ran a permuted linear model in R (lmPerm package) testing for effects of both ‘species’ and ‘observer’ on social grooming rates. We also repeated this procedure with ‘feeding rates’ and ‘aggression’ instead of ‘observer’ to see if observed differences in these factors could help explain social grooming rates after accounting for species differences.
Time spent social grooming varied by species and sex (Table 1). Social grooming rates for Desmodus were higher than for the other species: Artibeus (z = 2.53, n = 26, p = 0.045), Carollia (z = 3.66, n = 26, p = 0.001), Eidolon (z = 3.28, n = 26, p = 0.004), and Rousettus (z = 3.35, n = 26, p = 0.003; Fig 1). In contrast, self-grooming rates in Desmodus were not significantly different than those for Artibeus (z = 0.02, p = 1), Carollia (z = 1.69, p = 0.36), Eidolon (z = 1.31, p = 0.77), and Rousettus (z = 2.09, p = 0.15; Fig 2). After controlling for the effect of species on social grooming rates, we detected no effect of observer (F(6, 119) = 0.19, p~1), feeding rates (F(1,124) = 0.07, p~1), or aggression (F(1,124) = 0.02, p = 0.3).
Social grooming rates are shown for male (red), female (blue), and non-testes bats (green, see methods). Light blue shading shows probability density functions. Phylogenetic relationships between species are shown on right.
Under similar conditions of captivity and in the absence of external parasites, social grooming in vampire bats (Desmodus rotundus) is elevated beyond the rates found in four other group-living bat species (Fig 1). Vampire bats spent about 1.5–6.3% of their time social grooming, whereas time spent social grooming in the other species reached only 0.5% (Table 1). Vampires spent on average 14 times longer social grooming than the non-vampires. This difference between vampires and the other bats does not extend to self-grooming (Fig 2), and is unlikely to be explained by variation in feeding rates.
Are social grooming differences explained by general differences in social structure? The bat species in this study are all group-living in the wild, but vary in their social structures and degree of sociality. Desmodus rotundus forms stable female social groups of 8–12 adults with offspring, living in a roost site that is defended by a single dominant male against invasions by other males, i.e. resource defense polygyny [62, 64]. Individual recognition is evident from patterns of social behavior [64, 65], and may occur at a distance through individually variable contact calls , which allow vocal discrimination in another vampire bat species [74–75]. Carollia perspicillata female groups vary in size from 2–18 bats, and are based around resource defense polygyny with males performing courtship displays and defending territories [76, 77]. Vocal discrimination is evident between males  and between mothers and pups . In contrast with vampire bats, group membership appears to be less stable . Artibeus jamaicensis also demonstrates resource defense polygyny, and both males and females appear to form cooperative relationships in the wild [58, 80–82]. Dominant males are able to defend larger groups of females by tolerating the presence of subordinate males that are often kin and that help ward off foreign males . These male alliances for cooperative defense of female groups can last more than 2 years . Female groupmates engage in social grooming, and females that are closer to the group’s center are groomed more often . Unlike vampire bats, juveniles do not appear to perform allogrooming . Relatively little is known about the social behavior in Rousettus aegyptiacus and Eidolon helvum in the wild, but both species form aggregations of hundreds to thousands of both male and female individuals . These aggregations likely mask the presence of smaller social networks. Rousettus pups converge on adult repertoire of calls through vocal learning . Both species are highly vocal and frequently squabble among each other. In summary, the differences in social grooming rates we observed cannot easily be explained by straightforward differences in basic social structure.
Vampire bats are the only bats that perform regurgitated food sharing , and the necessity to maintain food-sharing relationships might be important to the evolution of their elevated social grooming rates. Foraging vampire bats are likely to either receive a large meal of blood or none at all, meaning that the costs of sharing are low and benefits of receiving are great . Obtaining regurgitated food donations from social partners appears to be a crucial component to the inclusive fitness of vampire bats, because nearly 1/5 of bats fail to feed on a given night and individuals can starve in under 72 hours . Correlational evidence suggests that vampire bats may use social grooming to maintain social bonds that are crucial for reciprocal food sharing [55,60]. Social grooming requires a relatively small investment of energy compared to regurgitated food sharing, and therefore may be used as way to build such cooperative relationships gradually with increasing investments. This ‘raising-the-stakes’ hypothesis  is consistent with the observation that previously unfamiliar vampire bats placed together in captivity developed social grooming but not food sharing over several weeks .
Wilkinson  suggested that social grooming might help hungry begging bats detect the ability of partners to share food, and other observations show that donors often initiate food sharing by ‘greeting’ and grooming recipients . Social grooming could therefore function as a tactile signal of desire to receive food or an intention to share it. Further comparative studies on social grooming in bats and other mammals will provide insight into whether frequent social grooming may have originated from selective pressures that are similar to those having shaped social grooming in primates. Based on what is known from six bat species from three families (Table 1), the high levels of social grooming observed in vampire bats seem unlikely to reflect a general trait conserved across bats. Rather, elevated social grooming in vampire bats appears to be an adaptive specialization to a cooperative social life.
We thank the Organization for Bat Conservation for their unwavering support and for permission to use photos for Fig 1. Jerry Wilkinson and two reviewers provided suggestions that improved the manuscript. Amanda Felk, Erica Antishin, Danielle Dekoski, Jerry Mitchell, and Nadia Siekert helped with data collection. This research was supported in part by a grant to the University of Maryland from the Howard Hughes Medical Institute through the Science Education Program.
Conceived and designed the experiments: GC. Performed the experiments: GC LL. Analyzed the data: GC. Contributed reagents/materials/analysis tools: GC. Wrote the paper: GC LL.
- 1. Seyfarth RM. A model of social grooming among adult female monkeys. J Theor Biol. 1977;65(4):671–98. pmid:406485
- 2. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, et al. The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc B. 2009;276(1670):3099–104. doi: 10.1098/rspb.2009.0681. pmid:19515668
- 3. Seyfarth RM, Cheney DL. The evolutionary origins of friendship. Annu Rev Psychol. 2012;63:153–77. Available: doi: 10.1146/annurev-psych-120710-100337. pmid:21740224
- 4. Seyfarth RM, Cheney DL. Affiliation, empathy, and the origins of theory of mind. Proc Natl Acad Sci USA. 2013;110:10349–56. doi: 10.1073/pnas.1301223110. pmid:23754420
- 5. Seyfarth RM, Silk JB, Cheney DL. Social bonds in female baboons: the interaction between personality, kinship and rank. Anim Behav. 2014;87:23–9.
- 6. Seyfarth RM, Cheney DL. Social cognition. Anim Behav. 2015;103:191–202. doi: 10.1016/j.anbehav.2015.01.030.
- 7. Brent LJ, Chang SW, Gariépy JF, Platt ML. The neuroethology of friendship. Ann NY Acad Sci. 2014;1316(1):1–17.
- 8. Brent LJ. Friends of friends: are indirect connections in social networks important to animal behaviour? Anim Behav. 2015;103:211–22. pmid:25937639
- 9. Gero S, Gordon J, Whitehead H. Individualized social preferences and long-term social fidelity between social units of sperm whales. Anim Behav. 2015;102:15–23.
- 10. Connor RC, Krützen M. Male dolphin alliances in Shark Bay: changing perspectives in a 30-year study. Anim Behav. 2015;103(0):223–35. doi: 10.1016/j.anbehav.2015.02.019.
- 11. Carter GG, Wilkinson GS. Cooperation and conflict in the social lives of bats. In: Adams R, Pedersen S, editors. Bat Evolution, Ecology, and Conservation. New York: Springer Science Press; 2013. p. 225–42.
- 12. Archie EA, Moss CJ, Alberts SC. The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc B. 2006;273(1586):513–22. Available: doi: 10.1098/rspb.2005.3361. pmid:16537121
- 13. Smith JE, Powning KS, Dawes SE, Estrada JR, Hopper AL, Piotrowski SL, et al. Greetings promote cooperation and reinforce social bonds among spotted hyaenas. Anim Behav. 2011;81(2):401–15. Available: doi: 10.1016/j.anbehav.2010.11.007.
- 14. Gersick AS, Cheney DL, Schneider JM, Seyfarth RM, Holekamp KE. Long-distance communication facilitates cooperation among wild spotted hyaenas, Crocuta crocuta. Anim Behav. 2015;103:107–16. Available: doi: 10.1016/j.anbehav.2015.02.003. pmid:25908882
- 15. Holekamp KE, Dantzer B, Stricker G, Shaw Yoshida KC, Benson-Amram S. Brains, brawn and sociality: a hyaena's tale. Anim Behav. 2015;103(0):237–48. Available: doi: 10.1016/j.anbehav.2015.01.023.
- 16. Fraser ON, Bugnyar T. The quality of social relationships in ravens. Anim Behav. 2010;79(4):927–33. Available: doi: 10.1016/j.anbehav.2010.01.008. pmid:25821236
- 17. Boeckle M, Bugnyar T. Long-Term Memory for Affiliates in Ravens. Curr Biol. 2012:1–6. Available: doi: 10.1016/j.cub.2012.03.023.
- 18. Fraser ON, Bugnyar T. Reciprocity of agonistic support in ravens. Anim Behav. 2012;83(1):171–7. Available: doi: 10.1016/j.anbehav.2011.10.023. pmid:22298910
- 19. Massen JJ, Szipl G, Spreafico M, Bugnyar T. Ravens intervene in others’ bonding attempts. Curr Biol. 2014;24(22):2733–6. doi: 10.1016/j.cub.2014.09.073. pmid:25455033
- 20. Massen JJ, Pašukonis A, Schmidt J, Bugnyar T. Ravens notice dominance reversals among conspecifics within and outside their social group. Nature Comm. 2014;5.
- 21. Miklósi Á, Kubinyi E, Topál J, Gácsi M, Virányi Z, Csányi V. A simple reason for a big difference: wolves do not look back at humans, but dogs do. Curr Biol. 2003;13(9):763–6. pmid:12725735
- 22. Hare B, Tomasello M. Human-like social skills in dogs? Trends Cogn Sci. 2005;9(9):439–44. pmid:16061417
- 23. Emery NJ, Clayton NS. The mentality of crows: convergent evolution of intelligence in corvids and apes. Science. 2004;306(5703):1903–7. pmid:15591194
- 24. Emery NJ, Seed AM, von Bayern AMP, Clayton NS. Cognitive adaptations of social bonding in birds. Phil Trans R Soc B. 2007;362(1480):489–505. Available: doi: 10.1098/rstb.2006.1991. pmid:17255008
- 25. Seyfarth RM, Cheney DL. Grooming, alliances and reciprocal altruism in vervet monkeys. Nature. 1984;308(5959):541–3. pmid:6709060
- 26. Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA. Market forces predict grooming reciprocity in female baboons. Proc R Soc B. 1999;266(1420):665–70.
- 27. Hemelrijk CK, Ek A. Reciprocity and interchange of grooming and support in captive chimpanzees. Anim Behav. 1991;41:923–35.
- 28. Muroyama Y. Exchange of grooming for allomothering in female patas monkeys. Behav. 1994;128:103–19.
- 29. Watts DP. Reciprocity and interchange in the social relationships of wild male chimpanzees. Behav. 2002;139:343–370.
- 30. Gomes CM, Mundry R, Boesch C. Long-term reciprocation of grooming in wild West African chimpanzees. Proc R Soc B. 2009;276:699–706. Available: doi: 10.1098/rspb.2008.1324. pmid:18957365
- 31. Schino G, Aureli F. Grooming reciprocation among female primates: a meta-analysis. Biol Lett. 2008;4(1):9–11. pmid:17999942
- 32. Fruteau C, Lemoine S, Hellard E, van Damme E, Noë R. When females trade grooming for grooming: Testing partner control and partner choice models of cooperation in two species of primates. Anim Behav. 2011;81:1223–30.
- 33. Tiddi B, Aureli F, di Sorrentino EP, Janson CH, Schino G. Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin monkeys. Behav Ecol. 2011;22(3):663–9.
- 34. Jaeggi AV, De Groot E, Stevens JM, Van Schaik CP. Mechanisms of reciprocity in primates: testing for short-term contingency of grooming and food sharing in bonobos and chimpanzees. Evol Hum Behav. 2013;34(2):69–77.
- 35. de Waal FB. Food transfers through mesh in brown capuchins. J Comp Psychol. 1997;111(4):370–8. pmid:9419882
- 36. de Waal FBM. The chimpanzee's service economy: Food for grooming. Evol Hum Behav. 1997;18(6):375–86.
- 37. Fruteau C, Voelkl B, van Damme E, Noë R. Supply and demand determine the market value of food providers in wild vervet monkeys. Proc Natl Acad Sci USA. 2009;106:12007–12. doi: 10.1073/pnas.0812280106. pmid:19581578
- 38. Dunbar R. Functional significance of social grooming in primates. Folia Primatol. 1991;57:121–31.
- 39. Aureli F, Preston SD, de Waal F. Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. J Comp Psychol. 1999;113(1):59. pmid:10098269
- 40. Shutt K, Maclarnon A, Heistermann M, Semple S. Grooming in Barbary macaques: better to give than to receive? Biol Lett. 2007;3(3):231–3. Available: doi: 10.1098/rsbl.2007.0052. pmid:17327200
- 41. Boccia ML, Reite M, Laudenslager M. On the physiology of grooming in a pigtail macaque. Physiol Behav. 1989;45(3):667–70. pmid:2756061
- 42. Russell EM. Social behaviour and social organization of marsupials. Mamm Rev. 1984;14(3):101–54.
- 43. Forand KJ, Marchinton RL. Patterns of social grooming in adult white-tailed deer. Amer Mid Nat. 1989:357–64.
- 44. Wood MT. Social grooming patterns in two herds of monozygotic twin dairy cows. Anim Behav. 1977;25:635–42.
- 45. Kimura R. Mutual grooming and preferred associate relationships in a band of free-ranging horses. Appl Anim Behav Sci. 1998;59(4):265–76.
- 46. Ophir AG, Crino OL, Wilkerson QC, Wolff JO, Phelps SM. Female-directed aggression predicts paternal behavior, but female prairie voles prefer affiliative males to paternal males. Brain Behav Evol. 2008;71(1):32. pmid:17878716
- 47. Stopka P, Graciasová R. Conditional allogrooming in the herb-field mouse. Behav Ecol. 2001;12(5):584–9.
- 48. Kutsukake N, Clutton-Brock T. Social functions of allogrooming in cooperatively breeding meerkats. Anim Behav. 2006;72(5):1059–68.
- 49. Kutsukake N, Clutton-Brock TH. Grooming and the value of social relationships in cooperatively breeding meerkats. Anim Behav. 2010;79(2):271–9.
- 50. Russell JK. Altruism in coati bands: nepotism or reciprocity. In: Wasser SK, editor. Social Behavior of Female Vertebrates. New York: Academic Press; 1983:263–90.
- 51. Hirsch BT, Stanton MA, Maldonado JE. Kinship shapes affiliative social networks but not aggression in ring-tailed coatis. PLOS One. 2012;7(5): e37301. Available: doi: 10.1371/journal.pone.0037301. pmid:22624010
- 52. Matoba T, Kutsukake N, Hasegawa T. Head rubbing and licking reinforce social bonds in a group of captive African lions, Panthera leo. PLOS One. 2013;8(9):e73044. doi: 10.1371/journal.pone.0073044. pmid:24023806
- 53. Gill SA. Strategic use of allopreening in family-living wrens. Behav Ecol Sociobiol. 2012;66(5):757–63.
- 54. Radford AN. Post-allogrooming reductions in self-directed behaviour are affected by role and status in the green woodhoopoe. Biol Lett. 2012;8(1):24–7. doi: 10.1098/rsbl.2011.0559. pmid:21795264
- 55. Wilkinson GS. Social grooming in the common vampire bat, Desmodus rotundus. Anim Behav. 1986;34:1880–9.
- 56. Ancillotto L, Serangeli MT, Russo D. Spatial proximity between newborns influences the development of social relationships in bats. Ethol. 2012;118(4):331–40.
- 57. Kerth G, Almasi B, Ribi N, Thiel D, Lüpold S. Social interactions among wild female Bechstein's bats (Myotis bechsteinii) living in a maternity colony. Acta Ethol. 2003;5(2):107–14.
- 58. Ortega J, Maldonado JE. Female interactions in harem groups of the Jamaican fruit-eating bat, Artibeus jamaicensis (Chiroptera: Phyllostomidae). Acta Chiropterol. 2006;8(2):485–95.
- 59. Arnold BD, Wilkinson GS. Individual specific contact calls of pallid bats (Antrozous pallidus) attract conspecifics at roosting sites. Behav Ecol Sociobiol. 2011;65(8):1581–93.
- 60. Carter GG, Wilkinson GS. Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc B. 2013;280:20122573. Available: doi: 10.1098/rspb.2012.2573. pmid:23282995
- 61. Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, et al. Fission‐fusion dynamics. Curr Anthro. 2008; 49: 627–654.
- 62. Wilkinson GS. The social organization of the common vampire bat: I. Pattern and cause of association. Behav Ecol Sociobiol. 1985;17:111–121.
- 63. Kerth G, Perony N, Schweitzer F. Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proc R Soc B. 2011;278(1719):2761–7. Available: doi: 10.1098/rspb.2010.2718. pmid:21307051
- 64. Wilkinson GS. Reciprocal food sharing in the vampire bat. Nature. 1984;308:181–4.
- 65. Carter G, Wilkinson G. Does food sharing in vampire bats demonstrate reciprocity? Comm Integr Biol. 2013;6(6):e25783. doi: 10.4161/cib.25783.
- 66. Baron G, Stephan H, Frahm HD. Comparative Neurobiology in Chiroptera. Basel: Birkhäuser Verlag; 1996. 1596 p.
- 67. Bhatnagar K. The brain of the common vampire bat, Desmodus rotundus murinus (Wagner, 1840): a cytoarchitectural atlas. Braz J Biol. 2008; 68:583–599. pmid:18833481
- 68. Kudo H, Dunbar RIM. Neocortex size and social network size in primates. Anim Behav. 2001; 62(4), 711–722.
- 69. Byrne RW, Corp N. Neocortex size predicts deception rate in primates. Proc R Soc B. 2004; 271(1549), 1693–1699. pmid:15306289
- 70. ter Hofstede HM, Fenton MB. Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J Zool. 2005;266(04):333–40.
- 71. Patterson BD, Dick CW, Dittmar K. Parasitism by bat flies (Diptera: Streblidae) on neotropical bats: effects of host body size, distribution, and abundance. Parasitol Res. 2008;103(5):1091–100. doi: 10.1007/s00436-008-1097-y. pmid:18633645
- 72. Canty A, Ripley B. boot: Bootstrap R (S-Plus) Functions. R package version 1.5. 2015.
- 73. Carter GG, Logsdon R, Arnold B, Menchaca A, Medellin RA. Adult vampire bats produce contact calls when isolated: acoustic variation between species, colonies, and individuals. PLOS One. 2012;7(6):e38791. Available: doi: 10.1371/journal.pone.0038791. pmid:22719947
- 74. Carter GG, Skowronski M, Faure P, Fenton MB. Antiphonal calling allows individual discrimination in white-winged vampire bats. Anim Behav. 2008;76:1343–55.
- 75. Carter GG, Fenton MB, Faure P. White-winged vampire bats (Diaemus youngi) exchange contact calls. Can J Zool. 2009;87:604–8.
- 76. Williams CF. Social organization of the bat Carollia perspicillata (Chiroptera: Phyllostomidae). Ethol. 1986;71:265–82.
- 77. Knörnschild M, Feifel M, Kalko EK. Male courtship displays and vocal communication in the polygynous bat Carollia perspicillata. Behav. 2014;151(6):781–98.
- 78. Fernandez AA, Fasel N, Knörnschild M, Richner H. When bats are boxing: aggressive behaviour and communication in male Seba's short-tailed fruit bat. Anim Behav. 2014;98:149–56.
- 79. Knörnschild M, Feifel M, Kalko EK. Mother–offspring recognition in the bat Carollia perspicillata. Anim Behav. 2013;86(5):941–8.
- 80. August PV (1979) Distress calls in Artibeus jamaicensis: ecology and evolutionary implications. In: Eisenberg JF, editor. Vertebrate ecology in the northern Neotropics. Washington DC: Smithsonian Institution Press; 1979. pp. 151–159.
- 81. Ortega J, Maldonado JE, Wilkinson GS, Arita HT, Fleischer RC. Male dominance, paternity, and relatedness in the Jamaican fruit‐eating bat (Artibeus jamaicensis). Mol Ecol. 2003;12(9):2409–15. pmid:12919478
- 82. Ortega J, Guerrero JA, Maldonado JE. Aggression and tolerance by dominant males of Artibeus jamaicensis: strategies to maximize fitness in harem groups. J Mammal. 2008;89(6):1372–8.
- 83. Kwiecinski GG, Griffiths TA. Rousettus egyptiacus. Mamm. Species. 1999:1–9.
- 84. Prat Y, Taub M, Yovel Y. Vocal learning in a social mammal: Demonstrated by isolation and playback experiments in bats. Sci Adv. 2015; 1(2), e1500019.
- 85. Roberts G, Thomas NS. Development of cooperative relationships through increasing investment. Nature. 1998; 394(6689),175–179. pmid:9671299