Behavioral Ecology and Sociobiology

, Volume 61, Issue 8, pp 1219–1228 | Cite as

All-offspring dispersal in a tropical mammal with resource defense polygyny

  • Dina K. N. Dechmann
  • Elisabeth K. V. Kalko
  • Gerald Kerth
Original Paper


In polygynous mammals, males are usually responsible for gene flow while females are predominantly philopatric. However, there is evidence that in a few mammalian species female offspring may disperse to avoid breeding with their father when male tenure exceeds female age at maturity. We investigated offspring dispersal and local population structure in the Neotropical bat Lophostoma silvicolum. The mating system of this species is resource defense polygyny, with the resource being active termite nests, excavated by single males, which are then joined by females. We combined field observations of 14 harems during 3 years and data about the genetic structure within and between these groups, calculated with one mitochondrial locus and nine nuclear microsatellite loci. The results show that both male and female offspring disperse before maturity. In addition, we estimated life span of excavated termite nests and the duration they were occupied by the same male. Our findings suggest that long male tenure of up to 30 months is indeed a likely cause for the observed dispersal by female offspring that can reach maturity at a low age of 6 months. We suggest that dispersal by offspring of both sexes may occur quite frequently in polygynous tropical bats and thus generally may be more common in mammals than previously assumed.


Male tenure Roost making Population structure Lophostoma silvicolum Mating system 



The Roche Research Foundation and the ZUNIV-Fonds zur Förderung des Akademischen Nachwuchses (FAN) financed Dina Dechmann during this study. The Julius–Klaus–Stiftung (Zürich) and the Brachet Foundation (Belgium) financed the genetic analyses, which were carried out with much help from J. Garbely. We want to thank the Smithsonian Tropical Research Institute (STRI) and the National Authority for the Environment (ANAM) for research permits and the staff of Barro Colorado Island, especially the game wardens for logistical support. The following people helped with fieldwork, development of equipment and/or with data analysis: A. Beck, M. Demir, S. Heucke, M. Kalka, R. Kays, J. Mandel, F. Neuhäuser-Wespy, K. Safi-Widmer, A. Schulz, M. Weinbeer, S. Wetterich, and especially K. Safi, A. Lang, S. Spehn, and C. Weise. We also thank M. Brigham, F. Mayer, A. McElligott, E. Petit, K. Safi, S. Spehn, and C. Voigt for valuable comments about the manuscript and B. König for her continuous support.


  1. Banks SC, Skerratt LF, Taylor AC (2002) Female dispersal and relatedness structure in common wombats (Vombatus ursinus). J Zool 256:389–399CrossRefGoogle Scholar
  2. Barclay RMR, Ulmer J, MacKenzee CJA, Thompson MS, Olson L, McCool J, Cropey EE, Poll G (2004) Variation in the reproductive rate of bats. Can J Zool 82:688–693CrossRefGoogle Scholar
  3. Belwood JJ (1988) The influence of bat predation on calling behaviour in Neotropical forest katydids (Insecta: Orthoptera: Tettigoniidae). University of Florida, GainesvilleGoogle Scholar
  4. Bockholdt C (1998) Hangplatzwahl, Aktivitätsrhythmik und Aktionsraum der neotropischen Fledermaus Tonatia silvicola (D’Orbigny, 1836). Fakultät für Biologie. Universität Freiburg, Freiburg, pp 94Google Scholar
  5. Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L (2004) Dispersed male networks in western gorillas. Curr Biol 14:510–513PubMedCrossRefGoogle Scholar
  6. Brooke AP (1997) Social organization and foraging behaviour of the fishing bat, Noctilio leporinus (Chiroptera:Noctilionidae). Ethology 103:421–436CrossRefGoogle Scholar
  7. Burland TM, Worthington-Wilmer JW (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409PubMedCrossRefGoogle Scholar
  8. Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc R Soc Lond B 266:975–980CrossRefGoogle Scholar
  9. Burland TM, Barratt EM, Nichols RA, Racey PA (2001) Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus. Mol Ecol 10:1309–1321PubMedCrossRefGoogle Scholar
  10. 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 14:708–720CrossRefGoogle Scholar
  11. Clarke AL, Saether B-E, Roskraft E (1997) Sex biases in avain dispersal: a reappraisal. Oikos 79:429–438CrossRefGoogle Scholar
  12. Clifford SL, Anthony NM, Bawe-Johnson M, Abernethy KA, Tutin CEG, White LJT, Bermejo M, Goldsmith ML, McFarland K, Jeffery KJ, Bruford MW, Wickings EJ (2004) Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla). Mol Ecol 13:1551–1565PubMedCrossRefGoogle Scholar
  13. Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford, UKGoogle Scholar
  14. Clutton-Brock TH (1989a) Female transfer and inbreeding avoidance in social mammals. Nature 337:70–72PubMedCrossRefGoogle Scholar
  15. Clutton-Brock TH (1989b) Mammalian mating systems. Proc R Soc Lond B 236:339–372PubMedCrossRefGoogle Scholar
  16. Dechmann DKN, Garbely E, Kerth G, Garner TWJ (2002) Highly polymorphic microsatellites for the study of the round-eared bat, Tonatia silvicola (d’Orbigny). Conservation Genetics 3:455–458CrossRefGoogle Scholar
  17. Dechmann DKN, Kalko EKV, Kerth G (2004) Ecology of an exceptional roost: energetic benefits could explain why the bat Lophostoma silvicolum roosts in active termite nests. Evol Ecol Res 6:1037–1050Google Scholar
  18. Dechmann DKN, Kalko EKV, König B, Kerth G (2005) Mating system of a Neotropical roost making bat: the white-throated, round-eared bat, Lophostoma silvicolum (Chiroptera: Phyllostomidae). Behav Ecol Sociobiol 58:316–325CrossRefGoogle Scholar
  19. Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30:1183–1192CrossRefGoogle Scholar
  20. Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: Evidence from field data and microsatellite patterns. Proc R Soc Lond B Biol Sci 264:127–132CrossRefGoogle Scholar
  21. Goudet J, Raymond M, de Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  22. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  23. Hammond RL, Lawson Handley LJ, Wineey BJ, Bruford MW, Perrin N (2006) Genetic evidence for female-biased dispersal and gene flow in a polygynous primate. Proc R Soc B 273:479–484PubMedCrossRefGoogle Scholar
  24. Heckel G, Von Helversen O (2003) Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata. Mol Ecol 12:219–227PubMedCrossRefGoogle Scholar
  25. Heckel G, Voigt CC, Mayer F, Von Helversen O (1999) Extra-harem paternity in the white-lined bat Saccopteryx bilineata (Emballonuridae). Behaviour 136:1173–1185CrossRefGoogle Scholar
  26. Kalko EKV, Handley CO, Handley D (1996) Organization, diversity, and long-term dynamics of a Neotropical bat community. In: Cody ML, Smallwood JA (eds) Long-term studies of vertebrate communities. Academic Press, San Diego, pp 503–553Google Scholar
  27. Kalko EKV, Friemel D, Handley CO, Schnitzler HU (1999) Roosting and foraging behavior of two Neotropical gleaning bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica 31:344–353CrossRefGoogle Scholar
  28. Kalko EKV, Ueberschaer K, Dechmann DKN (2006) Roost structure, modification, and availability in the white-throated, round-eared bat, Lophostoma silvicolum (Phyllostomidae) living in active termite nests. Biotropica 38:1–7CrossRefGoogle Scholar
  29. Kerth G, König B (1996) Transponder and an infrared-videocamera as methods used in a field study on the social behaviour of Bechstein’s Bat (Myotis bechsteinii). Myotis 34:27–34Google Scholar
  30. Kerth G, König B (1999) Fission, fusion and nonrandom associations in female Bechstein’s bats (Myotis bechsteinii). Behaviour 136:1187–1202CrossRefGoogle Scholar
  31. Kerth G, Morf L (2004) Behavioural and genetic data suggest that Bechstein’s bats predominantly mate outside the breeding habitat. Ethology 110:987–999CrossRefGoogle Scholar
  32. Kerth G, Mayer F, König B (2000) Mitochondrial DNA (mtDNA) reveals that female Bechstein’s bats live in closed societies. Mol Ecol 9:793–800PubMedCrossRefGoogle Scholar
  33. Kerth G, Mayer F, Petit E (2002a) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein’s bat (Myotis bechsteinii). Mol Ecol 11:1491–1498PubMedCrossRefGoogle Scholar
  34. Kerth G, Safi K, Konig B (2002b) 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 52:203–210CrossRefGoogle Scholar
  35. Kerth G, Kiefer A, Trappmann C, Weishaar M (2003) High gene diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein’s bat. Conservation Genetics 4:491–499CrossRefGoogle Scholar
  36. Koenig WD, Van Vuren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11:514–517CrossRefGoogle Scholar
  37. Lang AB, Kalko EKV, Römer H, Bockholdt C, Dechmann DKN (2006) Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146:659–666PubMedCrossRefGoogle Scholar
  38. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  39. McCracken GF, Bradbury JW (1981) Social organization and kinship in the polygynous bat Phyllostomus hastatus. Behav Ecol Sociobiol 8:11–34CrossRefGoogle Scholar
  40. McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic Press, London, pp 321–357Google Scholar
  41. Moore J, Ali R (1984) Are dispersal and inbreeding avoidance related. Anim Behav 32:94–112CrossRefGoogle Scholar
  42. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  43. Müllenbach R, Lagoda PJL, Welter C (1989) An efficient salt chloroform extraction method of DNA from blood and tissues. Trends Genet 5:391PubMedGoogle Scholar
  44. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  45. Ortega J, Maldonado JE, Arita HT, Wilkinson GS, Fleischer RC (2002) Characterization of microsatellite loci in the Jamaican fruit-eating bat Artibeus jamaicensis and cross-species amplification. Mol Ecol Notes 2:462–464CrossRefGoogle Scholar
  46. 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 12:2409–2415PubMedCrossRefGoogle Scholar
  47. Perrin N, Mazalov V (1999) Dispersal and inbreeding avoidance. Am Nat 154:282–292PubMedCrossRefGoogle Scholar
  48. Petit E, Balloux F, Goudet J (2001) Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55:635–640PubMedCrossRefGoogle Scholar
  49. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43:258–275CrossRefGoogle Scholar
  50. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  51. Reid FA (1997) A field guide to the mammals of Central America and Southeast Mexico. Oxford University Press, New York, OxfordGoogle Scholar
  52. Rossiter SJ, Jones G, Ransome RD, Barratt EM (2000a) Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum. Mol Ecol 9:1131–1135PubMedCrossRefGoogle Scholar
  53. Rossiter SJ, Jones G, Ransome RD, Barratt EM (2000b) Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc R Soc Lond, B Biol Sci 267:545–551CrossRefGoogle Scholar
  54. 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 51:510–518CrossRefGoogle Scholar
  55. Rossiter SJ, Ransome RD, Faulkes CG, Le Comber SC, Jones G (2005) Mate fidelity and intra-lineage polygyny in greater horseshoe bats. Nature 437:408–411PubMedCrossRefGoogle Scholar
  56. Ruckstuhl KE, Neuhaus P (2000) Sexual segregation in ungulates: a new approach. Behaviour 137:361–377CrossRefGoogle Scholar
  57. Schneider S, Roessli D, Escoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  58. Sedgeley JA, O’Donnell CFJ (1999) Roost selection by the long-tailed bat, Chalinolobus tuberculatus, in temperate New Zealand rainforest and its implications for the conservation of bats in managed forests. Biol Conserv 88:261–276CrossRefGoogle Scholar
  59. Seielstad MT, Minch E, Cavalli-Sforza LL (1998) Genetic evidence for a higher female migration rate in humans. Nat Genet 20:278–280PubMedCrossRefGoogle Scholar
  60. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton Press, PrincetonGoogle Scholar
  61. Storz JF, Bhat HR, Kunz TH (2000) Social structure of a polygynous tent-making bat, Cynopterus sphinx (Megachiroptera). J Zool 251:151–165CrossRefGoogle Scholar
  62. Storz JF, Bhat HR, Kunz TH (2001) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. I. Inbreeding, outbreeding, and population subdivision. Evolution 55:1215–1223PubMedCrossRefGoogle Scholar
  63. Vonhof MJ, Whitehead H, Fenton MB (2004) Analysis of Spix’s disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats. Anim Behav 68:507–521CrossRefGoogle Scholar
  64. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  65. Wilkinson GS (1985) The social-organization of the common vampire bat 2. Mating system, genetic-structure, and relatedness. Behav Ecol Sociobiol 17:123–134Google Scholar
  66. Wilkinson GS, Chapman AM (1991) Length and sequence variation in evening bat D-Loop MtDNA. Genetics 128:607–617PubMedGoogle Scholar
  67. Wilkinson GS, Mayer F, Kerth G, Petri B (1997) Evolution of repeated sequence arrays in the D.loop region of bat mitochondrial DNA. Genetics 146:1035–1048PubMedGoogle Scholar
  68. Williams DA, Rabenold KN (2005) Male-biased dispersal, female philopatry, and routes to fitness in a social corvid. J Anim Ecol 74:150–159CrossRefGoogle Scholar
  69. Worthington-Wilmer J, Hall L, Barratt E, Moritz C (1999) Genetic structure and male-mediated gene flow in the ghost bat (Macroderma gigas). Evolution 53:1582–1591CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Dina K. N. Dechmann
    • 1
    • 2
    • 5
  • Elisabeth K. V. Kalko
    • 2
    • 3
  • Gerald Kerth
    • 1
    • 4
  1. 1.Zoologisches InstitutUniversität ZürichZürichSwitzerland
  2. 2.Experimental EcologyUniversity of UlmUlmGermany
  3. 3.Smithsonian Tropical Research InstituteBalboaPanama
  4. 4.Department of Ecology and EvolutionUniversity of Lausanne, BiophoreLausanneSwitzerland
  5. 5.Institute of Anatomy - Division of NeuroanatomyUniversity Zürich-IrchelZürichSwitzerland

Personalised recommendations