Skip to main content
Log in

Kinship, association, and social complexity in bats

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Among mammals, bats exhibit extreme variation in sociality, with some species living largely solitary lives while others form colonies of more than a million individuals. Some tropical species form groups during the day that persist throughout the year while many temperate species only gather into groups during hibernation or parturition. How groups form and then persist has now been described for a number of species, but the degree to which kinship explains patterns of association has never been quantified across species. Here, we use social network analysis and genetic data to determine the extent to which relatedness contributes to associations among individuals estimated from free-ranging animals across nine species from four families of bats. Network analysis reveals that all species show evidence of emergent social structure. Variation in the strength of the relationship between genetic relatedness and social association appears to be related to the degree of roost switching, i.e., species in which individuals change roosts frequently tend to exhibit higher levels of association among relatives. Sex-biased dispersal determines whether associations were between male or female relatives. The strength of associations among kin does not predict known occurrence of complex behaviors, such as dominance or various types of cooperation, indicating that kinship is not a prerequisite for social complexity in bats.

Significance statement

The number of differentiated relationships has been proposed as a way to measure social complexity. Among primates, relationships can be differentiated on the basis of rank, age, kinship, or association. Application of this approach to other groups of mammals that vary in sociality could help reveal ecological, behavioral, or cognitive similarities and differences between species. As a first step toward this approach, we used social network analysis on long-term individual records and estimated relatedness using genetic markers for nine species of bats. We confirmed nonrandom emergent social structure in all species. Kinship was predictive of social association among individuals of the same sex in a few species, but largely independent of the occurrence of complex behaviors, such as dominance among males or cooperation among females. Complex social behavior in bats appears to require frequent interactions among a small number of individuals that roost together for multiple years.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aplin LM, Farine DR, Morand-Ferron J, Sheldon BC (2012) Social networks predict patch discovery in a wild population of songbirds. Proc R Soc Lond B 279:4199–4205

    CAS  Google Scholar 

  • Archie EA, Moss CJ, Alberts SC (2006) The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc Lond B 273:513–522

    CAS  Google Scholar 

  • Arnold BD (2011) Social vocalizations and their implications for group dynamics of pallid bats (Antrozous pallidus). Doctoral dissertation, University of Maryland

  • Arnold BD, Wilkinson GS (2011) Individual specific contact calls of pallid bats (Antrozous pallidus) attract conspecifics at roosting sites. Behav Ecol Sociobiol 65:1581–1593

    Google Scholar 

  • Arnold BD, Wilkinson GS (2015) Female natal philopatry and gene flow between divergent clades of pallid bats (Antrozous pallidus). J Mammal 96:531–540

    Google Scholar 

  • August TA, Nunn MA, Fensome AG, Linton DM, Mathews F (2014) Sympatric woodland Myotis bats form tight-knit social groups with exclusive roost home ranges. PLoS One 9:e112225

    PubMed  PubMed Central  Google Scholar 

  • Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654

    Google Scholar 

  • Avilés L, Harwood G (2012) A quantitative index of sociality and its application to group living spiders and other social organisms. Ethology 118:1219–1229

    PubMed  PubMed Central  Google Scholar 

  • Bell MBV, Nichols HJ, Gilchrist JS, Cant MA, Hodge SJ (2012) The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses. Proc R Soc Lond B 279:619–624

    CAS  Google Scholar 

  • Bell MBV, Cant MA, Borgeaud C, Thavarajah N, Samson J, Clutton-Brock TH (2014) Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats. Nat Commun 5:4499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett NC, Faulkes CG, Molteno AJ (1996) Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc R Soc Lond B 263:1599–1603

    CAS  Google Scholar 

  • Bergman TJ, Beehner JC (2015) Measuring social complexity. Anim Behav 103:203–209

    Google Scholar 

  • Blackwood JC, Streicker DG, Altizer S, Rohani P (2013) Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proc Natl Acad Sci U S A 110:20837–20842

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bohn KM, Moss CF, Wilkinson GS (2009) Pup guarding by greater spear-nosed bats. Behav Ecol Sociobiol 63:1693–1703

    Google Scholar 

  • Bouchard S (2001) Sex discrimination and roostmate recognition by olfactory cues in the African bats, Mops condylurus and Chaerephon pumilus (Chiroptera: Molossidae). J Zool 254:109–117

    Google Scholar 

  • Boughman JW (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70

    Google Scholar 

  • Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732

    CAS  PubMed  Google Scholar 

  • Bradbury JW (1977) Social organization and communication. In: Wimsatt WA (ed) The biology of bats. Academic Press, New York, pp 1–72

    Google Scholar 

  • Bradbury JW, Vehrencamp SL (1976) Social organization and foraging in emballonurid bats. I. Field studies. Behav Ecol Sociobiol 1:337–381

    Google Scholar 

  • Brent LJ, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr Biol 25:746–750

    CAS  PubMed  Google Scholar 

  • Brooke AP, Decker DM (1996) Lipid compounds in secretions of fishing bat, Noctilio leporinus (Chiroptera: Noctilionidae). J Chem Ecol 22:1411–1428

    CAS  PubMed  Google Scholar 

  • Buchalski MR, Chaverri G, Vonhof MJ (2014) When genes move farther than offspring: gene flow by male gamete dispersal in the highly philopatric bat species Thyroptera tricolor. Mol Ecol 23:464–480

    CAS  PubMed  Google Scholar 

  • Carter G, Leffer L (2015) Social grooming in bats: are vampire bats exceptional? PLoS One 10:e0138430

    PubMed  PubMed Central  Google Scholar 

  • Carter GG, Wilkinson GS (2013a) Cooperation and conflict in the social lives of bats. In: Adams RA, Pedersen SC (eds) Bat evolution, ecology, and conservation. Springer Science Press, New York, pp 225–242

    Google Scholar 

  • Carter GG, Wilkinson GS (2013b) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc Lond B 280:20122573

    Google Scholar 

  • Carter GG, Wilkinson GS (2016) Common vampire bat contact calls attract past food-sharing partners. Anim Behav 116:45–51

    Google Scholar 

  • Carter GG, Logsdon R, Arnold BD, Menchaca A, Medellin RA (2012) Adult vampire bats produce contact calls when isolated: acoustic variation by species, population, colony, and individual. PLoS One 7:e38791

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carter KD, Brand R, Carter JK, Shorrocks B, Goldizen AW (2013) Social networks, long-term associations and age-related sociability of wild giraffes. Anim Behav 86:901–910

    Google Scholar 

  • Castella V, Ruedi M, Excoffier L (2001) Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. J Evol Biol 14:708–720

    Google Scholar 

  • Chapais B (1995) Alliances as a means of competition in primates: evolutionary, developmental, and cognitive aspects. Yearb Phys Anthropol 38:115–136

    Google Scholar 

  • Chaverri G (2010) Comparative social network analysis in a leaf-roosting bat. Behav Ecol Sociobiol 64:1619–1630

    Google Scholar 

  • Chaverri G, Gillam EH (2015) Repeatability in the contact calling system of Spix’s disc-winged bat (Thyroptera tricolor). R Soc Open Sci 2:140197

    PubMed  PubMed Central  Google Scholar 

  • Chaverri G, Kunz TH (2011) All-offspring natal philopatry in a neotropical bat. Anim Behav 82:1127–1133

    Google Scholar 

  • Chaverri G, Gillam EH, Vonhof MJ (2010) Social calls used by a leaf-roosting bat to signal location. Biol Lett 6:441–444

    PubMed  PubMed Central  Google Scholar 

  • Chaverri G, Gillam EH, Kunz TH (2013) A call-and-response system facilitates group cohesion among disc-winged bats. Behav Ecol 24:481–487

    Google Scholar 

  • Chen S-F, Jones G, Rossiter SJ (2008) Sex-biased gene flow and colonization in the Formosan lesser horseshoe bat: inference from nuclear and mitochondrial markers. J Zool 274:207–215

    Google Scholar 

  • Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492

    CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449

    CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Hodge SJ, Flower TP, Spong GF, Young AJ (2010) Adaptive suppression of subordinate reproduction in cooperative mammals. Am Nat 176:664–673

    PubMed  Google Scholar 

  • Connor RC, Smolker RA, Richards AF (1992) Two levels of alliance formation among male bottle-nosed dolphins (Tursiops sp.). Proc Natl Acad Sci U S A 89:987–990

    CAS  PubMed  PubMed Central  Google Scholar 

  • Connor RC, Mann J, Tyack PL, Whitehead H (1998) Social evolution in toothed whales. Trends Ecol Evol 13:228–232

    CAS  PubMed  Google Scholar 

  • Craft ME (2015) Infectious disease transmission and contact networks in wildlife and livestock. Phil Trans R Soc B 370:20140107

    PubMed  Google Scholar 

  • Creel SR, Creel NM (1991) Energetics, reproductive suppression and obligate communal breeding in carnivores. Behav Ecol Sociobiol 28:263–270

    Google Scholar 

  • Creel S, Creel NM, Mills MGL, Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav Ecol 8:298–306

    Google Scholar 

  • Dechmann DKN, Kalko EKV, Kerth G (2007) All-offspring dispersal in a tropical mammal with resource defense polygyny. Behav Ecol Sociobiol 61:1219–1228

    Google Scholar 

  • Defanis E, Jones G (1995) The role of odor in the discrimination of conspecifics by pipistrelle bats. Anim Behav 49:835–839

    Google Scholar 

  • Dunbar RIM (1983) Structure of gelada baboon reproductive units. 2. Social relationships between reproductive females. Anim Behav 31:556–564

    Google Scholar 

  • Englert AC, Greene MJ (2009) Chemically-mediated roostmate recognition and roost selection by Brazilian free-tailed bats (Tadarida brasiliensis). PLoS One 4:e7781

    PubMed  PubMed Central  Google Scholar 

  • Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol Evol 4:1187–1194

    Google Scholar 

  • Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320

    PubMed  PubMed Central  Google Scholar 

  • Farine DR, Sheldon BC (2016) Social ecology of a woodland songbird community: from individual movements to the emergence of population social structure. bioRxiv. https://doi.org/10.1101/085944

  • Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163

    PubMed  PubMed Central  Google Scholar 

  • Fortuna MA, Popa-Lisseanu AG, Ibáñez C, Bascompte J (2009) The roosting spatial network of a bird-predator bat. Ecology 90:934–944

    PubMed  Google Scholar 

  • Freeberg TM, Dunbar RI, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc B 367:1785–1801

    Google Scholar 

  • Gager Y, Gimenez O, O'Mara MT, Dechmann DKN (2016) Group size, survival and surprisingly short lifespan in socially foraging bats. BMC Ecol 16:2

    PubMed  PubMed Central  Google Scholar 

  • Garg KM, Chattopadhyay B, Ramakrishnan U (2018) Social structure in the harem-forming promiscuous fruit bat, Cynopterus sphinx, is the harem truly important? R Soc Open Sci 5:172024

    PubMed  PubMed Central  Google Scholar 

  • Gillam EH, Chaverri G (2012) Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Anim Behav 83:269–276

    Google Scholar 

  • Gillam EH, Chaverri G, Montero K, Sagot M (2013) Social calls produced within and near the roost in two species of tent-making bats, Dermanura watsoni and Ectophylla alba. PLoS One 8:e61731

    CAS  PubMed  PubMed Central  Google Scholar 

  • Girvan M, Newman MEJ (2002) Community structure in social and biological networks. Proc Natl Acad Sci U S A 99:7821–7826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Godinho LN, Lumsden LF, Coulson G, Griffiths SR (2015) Network analysis reveals cryptic seasonal patterns of association in Gould’s wattled bats (Chalinolobus gouldii) roosting in bat-boxes. Behaviour 152:1079–2105

    Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Google Scholar 

  • Günther L, Lopez MD, Knörnschild M, Reid K, Nagy M, Mayer F (2016) From resource to female defence: the impact of roosting ecology on a bat’s mating strategy. R Soc Open Sci 3:160503

    PubMed  PubMed Central  Google Scholar 

  • He P, Maldonado-Chaparro A, Farine DR (2019) The role of habitat configuration in shaping social structure: a gap in studies of animal social complexity. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-018-2602-7

  • Heckel G, von Helversen O (2002) Male tactics and reproductive success in the harem polygynous bat Saccopteryx bilineata. Behav Ecol 13:750–756

    Google Scholar 

  • Hoppitt W, Farine DR (2018) Association indices for quantifying social relationships: how to deal with missing observations of individuals or groups. Anim Behav 136:227–238

    Google Scholar 

  • Jarvis JUM (1981) Eusociality in a mammal—cooperative breeding in naked mole-rat colonies. Science 212:571–573

    CAS  PubMed  Google Scholar 

  • Johnson N, Arechiga-Ceballos N, Aguilar-Setien A (2014) Vampire bat rabies: ecology, epidemiology and control. Viruses 6:1911–1928

    PubMed  PubMed Central  Google Scholar 

  • Kappeler PM (2019) A framework for studying social complexity. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-018-2601-8

  • Kerth G (2008) Causes and consequences of sociality in bats. Bioscience 58:737–746

    Google Scholar 

  • Kerth G, König B (1999) Fission, fusion and nonrandom associations in female Bechstein’s bats (Myotis bechsteinii). Behaviour 136:1187–1202

    Google Scholar 

  • Kerth G, Morf L (2004) Behavioural and genetic data suggest that Bechstein’s bats predominantly mate outside the breeding habitat. Ethology 110:987–999

    Google Scholar 

  • Kerth G, Reckardt K (2003) Information transfer about roosts in female Bechstein’s bats: an experimental field study. Proc R Soc Lond B 270:511–515

    Google Scholar 

  • Kerth G, Safi K, König B (2002) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein’s bat (Myotis bechsteinii). Behav Ecol Sociobiol 52:203–210

    Google Scholar 

  • Kerth G, Perony N, Schweitzer F (2011) Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proc R Soc Lond B 278:2761–2767

    Google Scholar 

  • Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O (2012) Learned vocal group signatures in the polygynous bat Saccopteryx bilineata. Anim Behav 84:761–769

    Google Scholar 

  • Kudo H, Dunbar RIM (2001) Neocortex size and social network size in primates. Anim Behav 62:711–722

    Google Scholar 

  • Lee PC (1987) Allomothering among African elephants. Anim Behav 35:278–291

    Google Scholar 

  • Lewis SE (1995) Roost fidelity of bats: a review. J Mamm 76:481–496

    Google Scholar 

  • Lewis SE (1996) Low roost-site fidelity in pallid bats: associated factors and effect on group stability. Behav Ecol Sociobiol 39:335–344

    Google Scholar 

  • Lukas D, Clutton-Brock T (2012) Life histories and the evolution of cooperative breeding in mammals. Proc R Soc Lond B 279:4065–4070

    Google Scholar 

  • MacKinnon KC, Fuentes A (2011) Primates, niche construction, and social complexity: the roles of social cooperation and altruism. In: Sussman RW, Cloninger CR (eds) Origins of altruism and cooperation. Springer, New York, pp 121–143

    Google Scholar 

  • MacLeod KJ, Lukas D (2014) Revisiting non-offspring nursing: allonursing evolves when the costs are low. Biol Lett 10:20140378

    PubMed Central  Google Scholar 

  • McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494

    CAS  PubMed  Google Scholar 

  • McCracken GF (1987) Genetic structure of bat social groups. In: Racey PA, Fenton MB, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 281–298

    Google Scholar 

  • McCracken GF, Bradbury JW (1981) Social organization and kinship in the polygynous bat Phyllostomus hastatus. Behav Ecol Sociobiol 8:11–34

    Google Scholar 

  • McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Krutszch PH, Crichton EG (eds) Reproductive biology of bats. Academic Press, New York, pp 321–362

    Google Scholar 

  • Metheny JD, Kalcounis-Rueppell MC, Willis CKR, Kolar KA, Brigham RM (2007) Genetic relationships between roost-mates in a fission–fusion society of tree-roosting big brown bats (Eptesicus fuscus). Behav Ecol Sociobiol 62:1043–1051

    Google Scholar 

  • Moehlman PD, Hofer H (1997) Cooperative breeding, reproductive suppression, and body mass in canids. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, New York, pp 76–128

    Google Scholar 

  • Moller LM, Beheregaray LB, Harcourt RG, Krutzen M (2001) Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proc R Soc Lond B 268:1941–1947

    CAS  Google Scholar 

  • Morrison DW (1979) Apparent male defense of tree hollows in the bat, Artibeus jamaicensis. J Mammal 60:11–15

    Google Scholar 

  • Moussy C, Hosken DJ, Mathews F, Smith GC, Aegerter JN, Bearhop S (2013) Migration and dispersal patterns of bats and their influence on genetic structure. Mamm Rev 43:183–195

    Google Scholar 

  • Nagy M, Knörnschild M, Voigt CC, Mayer F (2012) Male greater sac-winged bats gain direct fitness benefits when roosting in multimale colonies. Behav Ecol 23:597–606

    Google Scholar 

  • Nagy M, Günther L, Knörnschild M, Mayer F (2013) Female-biased dispersal in a bat with a female-defence mating strategy. Mol Ecol 22:1733–1745

    PubMed  Google Scholar 

  • Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131

    CAS  Google Scholar 

  • Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577–8582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Omer DB, Maimon SR, Las L, Ulanovsky N (2018) Social place-cells in the bat hippocampus. Science 359:218–224

    CAS  PubMed  Google Scholar 

  • Ortega J, Arita HT (2000) Defence of females by dominant males of Artibeus jamaicensis (Chiroptera: Phyllostomidae). Ethology 106:395–407

    Google Scholar 

  • Ortega J, Maldonado JE, Wilkinson GS, Arita HT, Fleischer RC (2003) Male dominance, paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis). Mol Ecol 12:2409–2415

    PubMed  Google Scholar 

  • Packer C, Lewis S, Pusey A (1992) A comparative analysis of nonoffspring nursing. Anim Behav 43:265–281

    Google Scholar 

  • Park SR (1991) Development of social structure in a captive colony of the common vampire bat, Desmodus rotundus. Ethology 89:335–341

    Google Scholar 

  • Parsons KM, Durban JW, Claridge DE, Balcomb KC, Noble LR, Thompson PM (2003) Kinship as a basis for alliance formation between male bottlenose dolphins, Tursiops truncatus, in the Bahamas. Anim Behav 66:185–194

    Google Scholar 

  • Parsons KM, Balcomb KC, Ford JKB, Durban JW (2009) The social dynamics of southern resident killer whales and conservation implications for this endangered population. Anim Behav 77:963–971

    Google Scholar 

  • Parsons JG, SKA R, Shilton LA (2011) Roost fidelity in spectacled flying-foxes Pteropus conspicillatus: implications for conservation and management. In: Law B, Eby P, Lunney D, Lumsden L (eds) The biology and conservation of Australasian bats. Royal Zoological Society of NSW, Mosman, pp 66–71

    Google Scholar 

  • Pasquaretta C, Leve M, Claidiere N et al (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patriquin KJ, Leonard ML, Broders HG, Garroway CJ (2010) Do social networks of female northern long-eared bats vary with reproductive period and age? Behav Ecol Sociobiol 64:899–913

    Google Scholar 

  • Patriquin KJ, Palstra F, Leonard ML, Broders HG (2013) Female northern myotis (Myotis septentrionalis) that roost together are related. Behav Ecol 24:949–954

    Google Scholar 

  • Payne K (2003) Sources of social complexity in the three elephant species. In: de Waal FBM, Tyack PL (eds) Animal social complexity. Harvard University Press, Cambridge, pp 57–85

    Google Scholar 

  • Podgorski T, Lusseau D, Scandura M, Sonnichsen L, Jedrzejewska B (2014) Long-lasting, kin-directed female interactions in a spatially structured wild boar social network. PLoS One 9:e99875

    PubMed  PubMed Central  Google Scholar 

  • Pretzlaff I, Kerth G, Dausmann KH (2010) Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure. Naturwissenschaften 97:353–363

    CAS  PubMed  PubMed Central  Google Scholar 

  • Racey PA, Entwhistle AC (2000) Life history and reproductive strategies of bats. In: Krutzsch PH, Crichton EG (eds) Reproductive biology of bats. Academic Press, New York, pp 363–414

    Google Scholar 

  • Roberts BJ, Catterall CP, Eby P, Kanowski J (2012) Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS One 7:e42532

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barratt EM (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum). Behav Ecol Sociobiol 51:510–518

    Google Scholar 

  • Roulin A (2002) Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Anim Behav 63:201–208

    Google Scholar 

  • Safi K, Kerth G (2003) Secretions of the interaural gland contain information about individuality and colony membership in the Bechstein’s bat. Anim Behav 65:363–369

    Google Scholar 

  • Sah P, Leu ST, Cross PC, Hudson PJ, Bansal S (2017) Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proc Natl Acad Sci U S A 114:4165–4170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schino G, Aureli F (2010) The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett 13:45–50

    PubMed  Google Scholar 

  • Schöner CR, Schöner MG, Kerth G (2010) Similar is not the same: social calls of conspecifics are more effective in attracting wild bats to day roosts than those of other bat species. Behav Ecol Sociobiol 64:2053–2063

    Google Scholar 

  • Seyfarth RM, Cheney DL (1984) Grooming, alliances and reciprocal altruism in vervet monkeys. Nature 308:541–543

    CAS  PubMed  Google Scholar 

  • Shizuka D, Farine DR (2016) Measuring the robustness of network community structure using assortativity. Anim Behav 112:237–246

    PubMed  PubMed Central  Google Scholar 

  • Silk JB (2007) Social components of fitness in primate groups. Science 317:1347–1351

    CAS  PubMed  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2004) Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim Behav 67:573–582

    Google Scholar 

  • Storz JF (2000) Social structure of a polygynous tent-making bat, Cynopterus sphinx (Megachiroptera). J Zool 251:151–165

    Google Scholar 

  • Storz JF, Bhat HR, Kunz TH (2001a) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. I. Inbreeding, outbreeding, and population subdivision. Evolution 55:1215–1223

    CAS  PubMed  Google Scholar 

  • Storz JF, Bhat HR, Kunz TH (2001b) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. II. Variance in male mating success and effective population size. Evolution 55:1224–1232

    CAS  PubMed  Google Scholar 

  • Trune DR, Slobodchikoff CN (1976) Social effects of roosting on the metabolism of the pallid bat (Antrozous pallidus). J Mammal 57:656–663

    CAS  PubMed  Google Scholar 

  • Tuttle MD, Stevenson D (1982) Growth and survival of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 105–150

    Google Scholar 

  • Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145

    PubMed  Google Scholar 

  • Wang J (2017) Estimating pairwise relatedness in a small sample of individuals. Heredity 119:302–313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208

    Google Scholar 

  • Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. Chicago University Press, Chicago

    Google Scholar 

  • Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778

    Google Scholar 

  • Wilkinson GS (1984) Reciprocal food sharing in vampire bats. Nature 309:181–184

    Google Scholar 

  • Wilkinson GS (1985a) The social organization of the common vampire bat. I. Pattern and cause of association. Behav Ecol Sociobiol 17:111–121

    Google Scholar 

  • Wilkinson GS (1985b) The social organization of the common vampire bat. II. Mating system, genetic structure, and relatedness. Behav Ecol Sociobiol 17:123–134

    Google Scholar 

  • Wilkinson GS (1986) Social grooming in the common vampire bat, Desmodus rotundus. Anim Behav 34:1880–1889

    Google Scholar 

  • Wilkinson GS (1987) Altruism and cooperation in bats. In: Racey PA, Fenton MB, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 299–323

    Google Scholar 

  • Wilkinson GS (1992a) Communal nursing in evening bats. Behav Ecol Sociobiol 31:225–235

    Google Scholar 

  • Wilkinson GS (1992b) Information transfer at evening bat colonies. Anim Behav 44:501–518

    Google Scholar 

  • Wilkinson GS, Boughman JW (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350

    CAS  PubMed  Google Scholar 

  • Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131

    CAS  PubMed  Google Scholar 

  • Wilkinson GS, Carter GG, Bohn KM, Adams DM (2016) Non-kin cooperation in bats. Philos Trans R Soc B 371:20150095

    Google Scholar 

  • Wiszniewski J, Brown C, Moller LM (2012) Complex patterns of male alliance formation in a dolphin social network. J Mammal 93:239–250

    Google Scholar 

  • Wittemyer G, Okello JB, Rasmussen HB, Arctander P, Nyakaana S, Douglas-Hamilton I, Siegismund HR (2009) Where sociality and relatedness diverge: the genetic basis for hierarchical social organization in African elephants. Proc R Soc Lond B 276:3513–3521

    Google Scholar 

  • Worthington-Wilmer J, Barratt EM (1996) A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res News 37:1–3

    Google Scholar 

  • Zeus VM, Reusch C, Kerth G (2018) Long-term roosting data reveal a unimodular social network in large fission-fusion society of the colony-living Natterer’s bat (Myotis nattereri). Behav Ecol Sociobiol 72:99–112

    Google Scholar 

Download references

Acknowledgments

We thank B. Negash for assistance in preparing data and H. Whitehead, D. Lukas, P. Kappeler, and two anonymous reviewers, as well as several other participants of the Göttinger Freilandtage, for useful suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerald S. Wilkinson.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by T. Clutton-Brock

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is a contribution to the Topical Collection Social complexity: patterns, processes, and evolution - Guest Editors: Peter Kappeler, Susanne Shultz, Tim Clutton-Brock, and Dieter Lukas

Electronic supplementary material

ESM 1

(PDF 129 kb)

ESM 2

(PDF 2575 kb)

ESM 3

(TXT 285 kb)

ESM 4

(TXT 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wilkinson, G.S., Carter, G., Bohn, K.M. et al. Kinship, association, and social complexity in bats. Behav Ecol Sociobiol 73, 7 (2019). https://doi.org/10.1007/s00265-018-2608-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2608-1

Keywords

Navigation