Oecologia

, Volume 135, Issue 3, pp 400–406 | Cite as

Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora

  • Mauricio Quesada
  • Kathryn E. Stoner
  • Víctor Rosas-Guerrero
  • Carolina Palacios-Guevara
  • Jorge A. Lobo
Plant Animal Interactions

Abstract

In the tropical dry forest of the central Pacific coast of Mexico the pollination and reproductive success of the bombacaceous tree Ceiba grandiflora was negatively affected by habitat disruption. Two of the three bat species that function as effective pollinators for this species (Glossophaga soricina and Musonycteris harrisoni) visited flowers found in trees in disturbed habitats significantly less than trees found in undisturbed habitats. A similar pattern was observed for the effective bat pollinator, Leptonycteris curasoae; however the difference was not significant. The three nectarivorous bats that functioned as effective pollinators of C. grandiflora also visited flowers to exclusively feed on pollen by biting or pulling off an anther (see Fig. S1 of Electronic Supplementary Material). The number of pollen grains deposited on stigmas from flowers in undisturbed areas was significantly greater than from flowers in disturbed habitats. The greater visitation rate and the greater number of pollen grains deposited on flowers from trees in undisturbed forest resulted in a significantly greater fruit set for trees in these areas. Our study demonstrates the negative effect that habitat disruption has on bat pollinators in tropical dry forest ecosystems and documents the negative consequences for the plants they pollinate.

Keywords

Habitat fragmentation Pollination decline Phyllostomid bats Plant reproductive success Plant–animal interactions 

References

  1. Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine "chaco serrano". Ecol Appl 4:378–392Google Scholar
  2. Aldrich PR, Hamrick JL (1998) Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281:103–105CrossRefPubMedGoogle Scholar
  3. Ayensu ES (1974) Plant and bat interactions in West Africa. Ann Mo Bot Gard 61:702–727Google Scholar
  4. Baker H G (1983) Ceiba pentandra. In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, pp 212–215Google Scholar
  5. Baker HG, Cruden RW, Baker I (1971) Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata. Bioscience 21:1127–1129Google Scholar
  6. Bawa KS (1990) Plant-pollinator interactions in tropical rainforests. Annu Rev Ecol Syst 21:399–342CrossRefGoogle Scholar
  7. Brosset A, Charles-Dominique P, Cockle A, Cosson JF, Masson D (1996) Bat communities and deforestation in French Guiana. Can J Zool 74:1974–1982Google Scholar
  8. Bullock SH (1995) Plant reproduction in neotropical dry forests. In: Bullock SH, Mooney HA, Medina E (eds) Seasonally dry tropical forest. Cambridge University Press, Cambridge, pp 277–303Google Scholar
  9. Casas A, Valiente-Banuet A, Rojas-Martínez A, Dávila P (1999) Reproductive biology and the process of domestication of the columnar cactus Stenocereus stellatus in Central Mexico. Am J Bot 86:534–542PubMedGoogle Scholar
  10. Cascante A, Quesada M, Lobo JA, Fuchs EJ (2002) Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Conserv Biol 16:137–147Google Scholar
  11. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  12. Cockrum EL (1991) Seasonal distribution of northwestern populations of the long-nosed bats Leptonycteris sanborni Phyllostomidae. Ana Inst Biol Univ Nac Auton Mex Ser Zool 62:181–202Google Scholar
  13. Cosson JF, Pons JM, Masson D (1999) Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. J Trop Ecol 15:515–534CrossRefGoogle Scholar
  14. Cunningham SA (2000a) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond Ser B 267:1149–1152CrossRefGoogle Scholar
  15. Cunningham S A (2000b) Effects of habitat fragmentation on the reproductive ecology of four plant species in mallee woodland. Conserv Biol 14:758–768CrossRefGoogle Scholar
  16. Dayanandan S, Dole J, Bawa K, Kesseli R (1999) Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae). Mol Ecol 8:1585–1592CrossRefPubMedGoogle Scholar
  17. Dick C W (2001) Genetic rescue of remnant tropical trees by an alien pollinator. Proc R Soc London Ser B 268:2391–2396CrossRefGoogle Scholar
  18. Donaldson J. Nänni I, Zachariades C, Kemper J (2002) Effects of habitat fragmentation on pollinator diversity and plant reproductive success in renosterved shrublands of South Africa. Conserv Biol 16:1267–1276Google Scholar
  19. Ellstrand NC (1992) Gene flow of pollen: implications for plant conservation genetics. Oikos 63:77–86Google Scholar
  20. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  21. Estrada A, Coates-Estrada R (2002) Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, México. Biol Conserv 103:237–245.CrossRefGoogle Scholar
  22. Feinsinger P (1987) Approaches to nectarivore-plant interactions in the New World. Rev Chil Hist Nat 60:285–319Google Scholar
  23. Fenton MB, Kunz TH (1977) Movements and behavior. In: Baker RJ, Jones JK Jr, Carter DC (eds) Biology of bats of the New World family Phyllostomatidae, part 2. Texas Tech University Press, Lubbock, Tex., pp 351–364Google Scholar
  24. Fenton MB, Acharya L, Audet D, Hickey MBC, Merriman C, Obrist MK, Syme DM (1992) Phyllostomid bats (Chiroptera: Phyllostomatidae) as indicators of habitat disruption in the Neotropics. Biotropica 24:440–446Google Scholar
  25. Fleming TH, Sosa VJ (1994) Effects of nectarivorous and frugivorous mammals on reproductive success of plants. J Mammal 75:845–851Google Scholar
  26. Fleming TH, Nuñez RA, Sternberg LS (1993) Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:72–75Google Scholar
  27. Fuchs EJ, Lobo JA, Quesada M (2003) Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns on the tropical dry forest tree, Pachira quinata (Bombacaceae). Conserv Biol 17:149–157Google Scholar
  28. Ghazoul J, McLeish M (2001) Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica. Plant Ecol 153: 335–345CrossRefGoogle Scholar
  29. Ghazoul J, Liston KA, Boyle TJB (1998) Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. J Ecol 86:462–473CrossRefGoogle Scholar
  30. Gribel R, Gibbs EP, Queiroz AL (1999) Flowering phenology and pollination biology of Ceiba pentandra (Bombacaceae) in central Amazonia. J Trop Ecol 15:247–263CrossRefGoogle Scholar
  31. Heithaus ER, Fleming TH, Opler PA (1975) Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56:841–854Google Scholar
  32. Herrera GL, C Maríntez del Río (1998) Pollen digestion by New World bats: effects of processing time and feeding habits. Ecology 79:2828–2838Google Scholar
  33. Horner MA, Fleming TH Sahley CT (1998) Foraging behaviour and energetics of a nectar-feeding bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J Zool (Lond) 244:575–586Google Scholar
  34. Howell, DJ (1974) Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp Biochem Physiol 48A:263–276CrossRefGoogle Scholar
  35. Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366Google Scholar
  36. Law BS (1992) The maintenance nitrogen requirements of the Queensland blossom bat (Syconycteris australis) on a sugar pollen diet—is nitrogen a limiting resource? Physiol Zool 65:634–648Google Scholar
  37. Lemke TO (1984) Foraging ecology of the long-nosed bat, Glossophaga soricina, with respect to resource availability. Ecology 65:356–363Google Scholar
  38. Lobo JA, Quesada M, Stoner, KE, Fuchs EJ, Herrerías-Diego Y, Rojas-Sandoval J, Saborío-Rodríguez G (2003) Phenological patterns of bombacaceous species in seasonal forests in Costa Rica and Mexico. Am J Bot (in press)Google Scholar
  39. Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128Google Scholar
  40. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, LondonGoogle Scholar
  41. Medellín RA, Equihua M, Amin MA (2000) Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conserv Biol 14:1666–1675CrossRefGoogle Scholar
  42. Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. J Ecol 90:100–107CrossRefGoogle Scholar
  43. Nason JD, Aldrich PR, Hamrick JL (1997) Dispersal and the dynamics of genetic structure in fragmented tropical tree populations. In: Laurance WF, Bierregaard, RU Jr (eds) Tropical forest remnants: ecology, management, and conservation of fragmented communities. University of Chicago Press, Chicago, pp 30–320Google Scholar
  44. Nobel PS, Quero E (1986) Environmental productivity and indices for a Chihuahuan desert plant Agave lechuguilla. Ecology 67:1–11Google Scholar
  45. Nowak RM (1994) Walker's bats of the world. The Johns Hopkins University Press, Baltimore, MarylandGoogle Scholar
  46. Palacios-Guevarra C (2002) Polinización natural, sistema de apareamiento y éxito reproductivo de Ceiba grandiflora en un bosque tropical caducifolio de México. Undergraduate thesis, Universidad Nacional Autónoma de México, Facultad de estudios superiores Iztacala. Distrito Federal, MexicoGoogle Scholar
  47. Powell HA, G Powell (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19:176–179Google Scholar
  48. Quesada M, Fuchs EJ, Lobo JA (2001) Pollen load size, reproductive success, and progeny kinship of naturally pollinated flowers of the tropical dry forest tree Pachira quinata (Bombacaeae). Am J Bot 88:2113–2118Google Scholar
  49. Rose JN (1895) Report on a collection of plants made in the states of Sonora and Colima, Mexico, by Dr. Edward Palmer, in the years 1890 and 1891. Contrib US Natl Herb 1:293–392Google Scholar
  50. Roulston TH, JH Cane, SL Buchmann (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol Monogr 70:617–643Google Scholar
  51. SAS (2001) SASuser's guide: statistics. Release 8.2. SAS Institute, Cary, N.C., USAGoogle Scholar
  52. Schulke, B, NM Waser (2001) Long-distance pollinator flights and pollen dispersal between populations of Delphinium muttallianum. Oecologia 127:239–245CrossRefGoogle Scholar
  53. Schulze MD, Seavy NE, Whitacre DF (2000) A comparison of the phyllostomid bat assemblages in undisturbed neotropical forest and in forest fragments of a slash-and-burn warming mosaic in Petén, Guatemala. Biotropica 32:174–184Google Scholar
  54. Sih A, Baltus M (1987) Patch size, pollinator behaviour, and pollinator limitation in catnip. Ecology 68:1679–1690Google Scholar
  55. Somanathan H, Borges RM (2000) Influence of exploitation on population structure, spatial distribution and reproductive success of dioecious species in a fragmented cloud forest in India. Biol Conserv 94:234–256Google Scholar
  56. Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224PubMedGoogle Scholar
  57. Spears EE (1987) Island and mainland pollination ecology of Centrosoma virginianum and Opuntia stricta. J Ecol 75:351–362Google Scholar
  58. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440CrossRefGoogle Scholar
  59. Steffan-Dewenter I, Münzenberg U, Tscharntke T (2001) Pollination, seed set and seed predation on a landscape scale. Proc R Soc Lond Ser B 268:1685–1690CrossRefGoogle Scholar
  60. Stephenson, A. G. (1992) The regulation of maternal investment in plants. In: Marshall C (ed) Environmental physiology and ecology of fruits and seeds. Cambridge University Press, Cambridge, pp 151–171Google Scholar
  61. Stephenson AG, Quesada M, Schlichting CD, Winsor JA (1995) Consequences in variation in pollen load size. In: Hosch C, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis, Mo., pp 233–244Google Scholar
  62. Stoner KE, Quesada M, Rosas-Guerrero V, Lobo JA (2002) Effects of forest fragmentation on Colima long-nosed bat (Musonycteris harrisoni) foraging in tropical dry forest in Jalisco, Mexico. Biotropica 34:462–467Google Scholar
  63. Stoner KE, O.-Salazar KA, R.-Fernández RC, Quesada M (2003) Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodivers Conserv 12:357–373CrossRefGoogle Scholar
  64. Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS, Cary, N.C.Google Scholar
  65. Sutherland S, Delph LF (1984) On the importance of male fitness in plants: patterns of fruit set. Ecology 65:1093–1104Google Scholar
  66. Toledo V. M. (1977) Pollination of some rain forest plants by non-hovering birds in Veracruz México. Biotropica 9:262–267Google Scholar
  67. White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Acad Nat Sci USA 99:2038–2042CrossRefGoogle Scholar
  68. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Mauricio Quesada
    • 1
  • Kathryn E. Stoner
    • 1
  • Víctor Rosas-Guerrero
    • 1
  • Carolina Palacios-Guevara
    • 1
  • Jorge A. Lobo
    • 2
  1. 1.Centro de Investigaciones en EcosistemasUniversidad Nacional Autónoma de MéxicoMoreliaMexico
  2. 2.Escuela de BiologíaUniversidad de Costa RicaSan PedroCosta Rica

Personalised recommendations