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Oecologia

, Volume 173, Issue 1, pp 191–202 | Cite as

Supply determines demand: influence of partner quality and quantity on the interactions between bats and pitcher plants

  • Caroline R. SchönerEmail author
  • Michael G. Schöner
  • Gerald Kerth
  • T. Ulmar Grafe
Plant-animal interactions - Original research

Abstract

Interspecific relationships such as mutualism and parasitism are major drivers of biodiversity. Because such interactions often comprise more than two species, ecological studies increasingly focus on complex multispecies systems. However, the spatial heterogeneity of multi-species interactions is often poorly understood. Here, we investigate the unusual interaction of a bat (Kerivoula hardwickii hardwickii) and two pitcher plant species (Nepenthes hemsleyana and N. bicalcarata) whose pitchers serve as roost for bats. Nepenthes hemsleyana offers roosts of higher quality, indicated by a more stable microclimate compared to N. bicalcarata but occurs at lower abundance and is less common than the latter. Whereas N. hemsleyana benefits from the roosting bats by gaining nitrogen from their feces, the bats’ interaction with N. bicalcarata seems to be commensal or even parasitic. Bats stayed longer in roosts of higher quality provided by N. hemsleyana and preferred them to pitchers of N. bicalcarata in a disturbance experiment. Moreover, bats roosting only in pitchers of N. hemsleyana had a higher body condition and were less infested with parasites compared to bats roosting in pitchers of N. bicalcarata. Our study shows how the local supply of roosts with different qualities affects the behavior and status of their inhabitants and—as a consequence—how the demand of the inhabitants can influence evolutionary adaptations of the roost providing species.

Keywords

Kerivoula hardwickii Nepenthes Mutualism Roost selection Roost quality 

Notes

Acknowledgments

We thank Liaw Lin Ji for assistance in the field and K. Fischer for helpful statistical advice. D. Dekeukeleire, J. Lambert, R. Simon and two anonymous referees kindly reviewed the manuscript. The German Academic Exchange Service (DAAD), the German Research Foundation (DFG: KE 746/5-1) and the University of Brunei Darussalam [RG/1(105) & RG/1(193)] funded this project. The Forestry Department of Brunei Darussalam granted permits to work in the field. This was an observational study of free-ranging animals. The experimental protocols adhered to the Animal Behaviour Society guidelines for the use of animals in research and were approved by the University Brunei Darussalam Research Committee (UBD/PNC2/2/RG 105 &193).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2013_2615_MOESM1_ESM.pdf (129 kb)
Supplementary material 1 (PDF 128 kb)
442_2013_2615_MOESM2_ESM.pdf (122 kb)
Supplementary material 2 (PDF 122 kb)
442_2013_2615_MOESM3_ESM.pdf (146 kb)
Supplementary material 3 (PDF 146 kb)

References

  1. Anonymous (2008) Government of Brunei Darussalam. Heart of Borneo Project Implementation Framework, Negara Brunei DarussalamGoogle Scholar
  2. Arthur L, Lemaire M (2009) Les chauves-souris de France, Belgique. Luxembourg et Suisse. Biotope. Museum national d’HistoireNaturelle, MèzeGoogle Scholar
  3. Ashton PS, Kamariah AS, Said IM (2003) A field guide to the forest trees of Brunei Darussalam. Universiti Brunei Darussalam, Brunei DarussalamGoogle Scholar
  4. Baudunette RV, Wells RT, Sanderson KJ, Clark B (1994) Microclimatic conditions in maternity caves of the bent-wing bat, Miniopterus schreibersii: an attempted restoration of a former maternity site. Wildl Res 21:607. doi: 10.1071/WR9940607 CrossRefGoogle Scholar
  5. Bauer U, Grafe TU, Federle W (2011) Evidence for alternative trapping strategies in two forms of the pitcher plant, Nepenthes rafflesiana. J Exp Bot 62:3683–3692. doi: 10.1093/jxb/err082 PubMedCrossRefGoogle Scholar
  6. Bauer U, Clemente CJ, Renner T, Federle W (2012) Form follows function: morphological diversification and alternative trapping strategies in carnivorous Nepenthes pitcher plants. J Evol Biol 25:90–102PubMedCrossRefGoogle Scholar
  7. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  8. Bohn HF (2004) Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proc Natl Acad Sci USA 101:14138–14143. doi: 10.1073/pnas.0405885101 PubMedCrossRefGoogle Scholar
  9. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347CrossRefGoogle Scholar
  10. Brigham RM, Brigham AC (1989) Evidence for association between a mother bat and its young during and after foraging. Am Midl Nat 121:205–207CrossRefGoogle Scholar
  11. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51CrossRefGoogle Scholar
  12. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287. doi: 10.1046/j.1461-0248.2001.00218.x CrossRefGoogle Scholar
  13. Brown CR, Brown MB (1986) Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67:1206–1218CrossRefGoogle Scholar
  14. Carpenter RE, Graham JB (1967) Physiological responses to temperature in the long-nosed bat, Leptonycteris sanborni. Comp Biochem Physiol 22:709–722PubMedCrossRefGoogle Scholar
  15. Chin L, Moran JA, Clarke CM (2010) Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytol 186:461–470. doi: 10.1111/j.1469-8137.2009.03166.x PubMedCrossRefGoogle Scholar
  16. Chruszcz BJ, Barclay RM (2002) Thermoregulatory ecology of a solitary bat, Myotis evotis, roosting in rock crevices. Funct Ecol 16:18–26. doi: 10.1046/j.0269-8463.2001.00602.x CrossRefGoogle Scholar
  17. Clarke C (2006) Nepenthes of Borneo. Natural History Publications in association with Science and Technology Unit, Kota KinabaluGoogle Scholar
  18. Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA (2009) Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biol Lett 5:632–635. doi: 10.1098/rsbl.2009.0311 PubMedCrossRefGoogle Scholar
  19. Clarke CM, Moran JA, Lee CC (2011) Nepenthes baramensis (Nepenthaceae) - a new species from north-western Borneo. Blumea 56:229–233. doi: 10.3767/000651911X607121 CrossRefGoogle Scholar
  20. Davis JM (2008) Patterns of variation in the influence of natal experience on habitat choice. Q Rev Biol 83:363–380. doi: 10.1086/592851 PubMedCrossRefGoogle Scholar
  21. Davis SJ, Becker P (1996) Floristic composition and stand structure of mixed dipterocarp and heath forests in Brunei Darussalam. J Trop For Sci 8:542–569Google Scholar
  22. de Mazancourt C, Loreau M, Dieckmann UL (2005) Understanding mutualism when there is adaptation to the partner. J Ecol 93:305–314. doi: 10.1111/j.0022-0477.2004.00952.x CrossRefGoogle Scholar
  23. Dechmann DK, Kalko EK, 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
  24. Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B (1997) Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112:217–224. doi: 10.1007/s004420050303 CrossRefGoogle Scholar
  25. Fiala B, Grunsky H, Maschwitz U, Linsenmair KE (1994) Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97:186–192. doi: 10.1007/BF00323148 CrossRefGoogle Scholar
  26. Franks NR, Dornhaus A, Fitzsimmons JP, Stevens M (2003) Speed versus accuracy in collective decision making. Proc R Soc Lond B 270:2457–2463. doi: 10.1098/rspb.2003.2527 CrossRefGoogle Scholar
  27. Fraser AM, Axén AH, Pierce NE (2001) Assessing the quality of different ant species as partners of a myrmecophilous butterfly. Oecologia 129:452–460Google Scholar
  28. Frederickson ME (2005) Ant species confer different partner benefits on two neotropical myrmecophytes. Oecologia 143:387–395. doi: 10.1007/s00442-004-1817-7 PubMedCrossRefGoogle Scholar
  29. Gaume L, Di Giusto B (2009) Adaptive significance and ontogenetic variability of the waxy zone in Nepenthes rafflesiana. Ann Bot 104:1281–1291. doi: 10.1093/aob/mcp238 PubMedCrossRefGoogle Scholar
  30. Gaume L, Forterre Y, Lynn D (2007) A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS ONE 2:e1185. doi: 10.1371/journal.pone.0001185 PubMedCrossRefGoogle Scholar
  31. Geiser F, Stawski C (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr Comp Biol 51:337–348. doi: 10.1093/icb/icr042 PubMedCrossRefGoogle Scholar
  32. Genoud M, Bonaccorso FJ, Anends A (1990) Rate of metabolism and temperature regulation in two small tropical insectivorous bats (Peropteryx macrotis and Natalus tumidirostris). Comp Biochem Physiol 97:229–234CrossRefGoogle Scholar
  33. Giardina C, Sanford R, Døckersmith I (2000) Changes in soil phosphorus and nitrogen during slash-and-burn clearing of a dry tropical forest. Soil Sci Soc Am J 64:399. doi: 10.2136/sssaj2000.641399x CrossRefGoogle Scholar
  34. Gomulkiewicz R, Nuismer SL, Thompson JN (2003) Coevolution in variable mutualisms. Am Nat 162:S80–S92. doi: 10.1086/378705 PubMedCrossRefGoogle Scholar
  35. Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG (2011) A novel resource-service mutualism between bats and pitcher plants. Biol Lett 7:436–439. doi: 10.1098/rsbl.2010.1141 PubMedCrossRefGoogle Scholar
  36. Heil M, Gonzalez-Teuber M, Clement LW, Kautz S, Verhaagh M, Bueno JC (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096. doi: 10.1073/pnas.0904304106 PubMedCrossRefGoogle Scholar
  37. Herreid CF, Schmidt-Nielson K (1966) Oxygen consumption, temperature, and water loss in bats from different environments. Am J Physiol 211:1108–1112PubMedGoogle Scholar
  38. Howe HF (1984) Constraints on the evolution of mutualisms. Am Nat 123:764–777CrossRefGoogle Scholar
  39. Janzen DH (1974) Epiphytic myrmecophytes in Sarawak: mutualism through the feeding of plants by ants. Biotropica 6:237–259CrossRefGoogle Scholar
  40. Jenkins EV, Laine T, Morgan SE, Cole KR, Speakman JR (1998) Roost selection in the pipistrelle bat, Pipistrellus pipistrellus (Chiroptera: Vespertilionidae), in northeast Scotland. Anim Behav 56:909–917PubMedCrossRefGoogle Scholar
  41. Kerth G, Weissmann K, König B (2001) Day roost selection in female Bechstein’s bats (Myotis bechsteinii): a field experiment to determine the influence of roost temperature. Oecologia 126:1–9CrossRefGoogle Scholar
  42. Kerth G, Ebert C, Schmidtke C (2006) Group decision-making in fission-fusion societies: evidence from two field experiments in Bechstein’s bats. Proc R Soc Lond B 273:2785–2790CrossRefGoogle Scholar
  43. Klopfer P (1963) Behavioral aspects of habitat selection: the role of early experience. Wilson Bull 75:15–22Google Scholar
  44. Kunz TH, MacCracken GF (1996) Tents and harems: apparent defence of foliage roosts by tent-making bats. J Trop Ecol 12:121–137CrossRefGoogle Scholar
  45. Lausen CL, Barclay RM (2003) Thermoregulation and roost selection by reproductive female big brown bats (Eptesicus fuscus) roosting in rock crevices. J Zool 260:235–244CrossRefGoogle Scholar
  46. Lewis SE (1996) Low roost-site fidelity in pallid bats: associated factors and effect on group stability. Behav Ecol Sociobiol 39:335–344. doi: 10.1007/s002650050298 CrossRefGoogle Scholar
  47. Lourenço SI, Palmeirim JM (2007) Can mite parasitism affect the condition of bat hosts? Implications for the social structure of colonial bats. J Zool 273:161–168. doi: 10.1111/j.1469-7998.2007.00322.x CrossRefGoogle Scholar
  48. Macfarlane JM (1908) Nepenthaceae. In: Engler A (ed) Sarraceniales. Das Pflanzenreich, vol 111. von Wilhelm Engelmann, Leipzig, pp 1–92Google Scholar
  49. Manser MB, Bell MB (2004) Spatial representation of shelter locations in meerkats, Suricata suricatta. Anim Behav 68:151–157CrossRefGoogle Scholar
  50. Merbach MA, Merbach DJ, Maschwitz U, Booth WE, Fiala B, Zizka G (2002) Mass march of termites into the deadly trap. Nature 415:36–37. doi: 10.1038/415036a PubMedCrossRefGoogle Scholar
  51. Miller TE (2007) Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116:500–512. doi: 10.1111/j.2007.0030-1299.15317.x CrossRefGoogle Scholar
  52. Moeller DA (2005) Pollinator community structure and sources of spatial variation in plant-pollinator interactions in Clarkia xantiana ssp. xantiana. Oecologia 142:28–37. doi: 10.1007/s00442-004-1693-1 PubMedCrossRefGoogle Scholar
  53. Moran JA (1996) Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. J Ecol 84:515–525CrossRefGoogle Scholar
  54. Moran JA, Booth WE, Charles JK (1999) Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture. Ann Bot 83:521–528. doi: 10.1006/anbo.1999.0857 CrossRefGoogle Scholar
  55. Moran JA, Clarke CM, Hawkins BJ (2003) From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. Int J Plant Sci 164:635–639CrossRefGoogle Scholar
  56. Noë R, Hammerstein P (1994) Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol 35:1–11. doi: 10.1007/BF00167053 CrossRefGoogle Scholar
  57. Osunkoya OO, Daud SD, Wimmer FL (2008) Longevity, lignin content and construction cost of the assimilatory organs of Nepenthes species. Ann Bot 102:845–852. doi: 10.1093/aob/mcn162 PubMedCrossRefGoogle Scholar
  58. Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci USA 107:17234–17239. doi: 10.1073/pnas.1006872107 PubMedCrossRefGoogle Scholar
  59. Payne J, Francis CM, Phillipps K (1985) A field guide to the mammals of Borneo. Sabah Society, World Wildlife Fund Malaysia, Kota KinabaluGoogle Scholar
  60. Perkins JM (1996) Does competition for roosts influence bat distribution in a managed forest? In: Barclay RMR, Brigham RM (eds) Bats and Forests Symposium, October 19-21, 1995. Victoria, British Columbia, Canada. Research Branch, BC Ministry of Forests, Victoria, pp 164–172Google Scholar
  61. Radovsky FJ (1967) The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic on bats. Univ Calif Publ Entomol 46:1–288Google Scholar
  62. Reckardt K, Kerth G (2007) Roost selection and roost switching of female Bechstein’s bats (Myotis bechsteinii) as a strategy of parasite avoidance. Oecologia 154:581–588. doi: 10.1007/s00442-007-0843-7 PubMedCrossRefGoogle Scholar
  63. Reckardt K, Kerth G (2009) Does the mode of transmission between hosts affect the host choice strategies of parasites? Implications from a field study on bat fly and wing mite infestation of Bechstein’s bats. Oikos 118:183–190. doi: 10.1111/j.1600-0706.2008.16950.x CrossRefGoogle Scholar
  64. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716. doi: 10.1046/j.0028-646x.2001.00210.x CrossRefGoogle Scholar
  65. Riedel M, Eichner A, Jetter R (2003) Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers. Planta 218:87–97. doi: 10.1007/s00425-003-1075-7 PubMedCrossRefGoogle Scholar
  66. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592PubMedCrossRefGoogle Scholar
  67. Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225:519–521. doi: 10.1126/science.225.4661.519 PubMedCrossRefGoogle Scholar
  68. 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. doi: 10.1007/s00265-010-1019-8 CrossRefGoogle Scholar
  69. Schulz M (2000) Roosts used by the golden-tipped bat Kerivoula papuensis (Chiroptera: Vespertilionidae). J Zool 250:467–478. doi: 10.1111/j.1469-7998.2000.tb00790.x CrossRefGoogle Scholar
  70. Schulze W, Frommer WB, Ward JM (1999) Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. Plant J 17:637–646. doi: 10.1046/j.1365-313X.1999.00414.x PubMedCrossRefGoogle Scholar
  71. Schwarzkopf L, Alford RA (1996) Desiccation and shelter-site use in a tropical amphibian: comparing toads with physical models. Funct Ecol 10:193–200CrossRefGoogle Scholar
  72. Sedgeley JA (2001) Quality of cavity microclimate as a factor influencing selection of maternity roosts by a tree-dwelling bat, Chalinolobus tuberculatus, in New Zealand. J Appl Ecol 38:425–438. doi: 10.1046/j.1365-2664.2001.00607.x CrossRefGoogle Scholar
  73. Sedgeley JA, O’Donnell CF (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
  74. Stachowicz JJ, Hay ME (1996) Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105:377–387. doi: 10.1007/BF00328741 CrossRefGoogle Scholar
  75. Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23. doi: 10.1086/378646 PubMedCrossRefGoogle Scholar
  76. Struebig MJ, Bozek M, Hildebrand J, Rossiter SJ, Lane DJW (2012) Bat diversity in the lowland of the Heart of Borneo. Biodivers Conserv. doi: 10.1007/s10531-012-0393-0 Google Scholar
  77. Studier EH (1970) Evaporative water loss in bats. Comp Biochem Physiol 35:935–943CrossRefGoogle Scholar
  78. Thornham DG, Smith JM, Grafe TU, Federle W (2012) Setting the trap: cleaning behaviour of Camponotus schmitzi increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata. Funct Ecol 26:11–19CrossRefGoogle Scholar
  79. Vonhof MJ, Barclay RM (1997) Use of tree stumps as roosts by the western long-eared bat. J Wildl Manag 61:674–684CrossRefGoogle Scholar
  80. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060CrossRefGoogle Scholar
  81. Whitaker JO Jr, Ritzi CM, Dick CW (2009) Collecting and preserving bat ectoparasites for ecological study. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. Johns Hopkins University Press, Baltimore, pp 806–827Google Scholar
  82. Zahn A, Rupp D (1999) Ectoparasite load in European vespertilionid bats. J Zool 262:383–391. doi: 10.1017/S0952836903004722 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Caroline R. Schöner
    • 1
    Email author
  • Michael G. Schöner
    • 1
  • Gerald Kerth
    • 1
  • T. Ulmar Grafe
    • 2
  1. 1.Zoological Institute and MuseumGreifswald UniversityGreifswaldGermany
  2. 2.Department of BiologyUniversity Brunei DarussalamGadongBorneo

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