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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

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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.

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References

  • Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine "chaco serrano". Ecol Appl 4:378–392

    Google Scholar 

  • Aldrich PR, Hamrick JL (1998) Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281:103–105

    Article  CAS  PubMed  Google Scholar 

  • Ayensu ES (1974) Plant and bat interactions in West Africa. Ann Mo Bot Gard 61:702–727

    Google Scholar 

  • Baker H G (1983) Ceiba pentandra. In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, pp 212–215

  • Baker HG, Cruden RW, Baker I (1971) Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata. Bioscience 21:1127–1129

    Google Scholar 

  • Bawa KS (1990) Plant-pollinator interactions in tropical rainforests. Annu Rev Ecol Syst 21:399–342

    Article  Google Scholar 

  • Brosset A, Charles-Dominique P, Cockle A, Cosson JF, Masson D (1996) Bat communities and deforestation in French Guiana. Can J Zool 74:1974–1982

    Google Scholar 

  • 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 277–303

  • 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 86:534–542

    PubMed  Google Scholar 

  • 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 16:137–147

    Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • 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 62:181–202

    Google Scholar 

  • Cosson JF, Pons JM, Masson D (1999) Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. J Trop Ecol 15:515–534

    Article  Google Scholar 

  • Cunningham SA (2000a) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond Ser B 267:1149–1152

    Article  CAS  Google Scholar 

  • Cunningham S A (2000b) Effects of habitat fragmentation on the reproductive ecology of four plant species in mallee woodland. Conserv Biol 14:758–768

    Article  Google Scholar 

  • 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 8:1585–1592

    Article  PubMed  Google Scholar 

  • Dick C W (2001) Genetic rescue of remnant tropical trees by an alien pollinator. Proc R Soc London Ser B 268:2391–2396

    Article  CAS  Google Scholar 

  • 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 16:1267–1276

    Google Scholar 

  • Ellstrand NC (1992) Gene flow of pollen: implications for plant conservation genetics. Oikos 63:77–86

    Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Feinsinger P (1987) Approaches to nectarivore-plant interactions in the New World. Rev Chil Hist Nat 60:285–319

    Google Scholar 

  • 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 351–364

  • 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 24:440–446

    Google Scholar 

  • Fleming TH, Sosa VJ (1994) Effects of nectarivorous and frugivorous mammals on reproductive success of plants. J Mammal 75:845–851

    Google Scholar 

  • 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 94:72–75

    Google Scholar 

  • 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 17:149–157

    Google Scholar 

  • Ghazoul J, McLeish M (2001) Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica. Plant Ecol 153: 335–345

    Article  Google Scholar 

  • Ghazoul J, Liston KA, Boyle TJB (1998) Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. J Ecol 86:462–473

    Article  Google Scholar 

  • Gribel R, Gibbs EP, Queiroz AL (1999) Flowering phenology and pollination biology of Ceiba pentandra (Bombacaceae) in central Amazonia. J Trop Ecol 15:247–263

    Article  Google Scholar 

  • Heithaus ER, Fleming TH, Opler PA (1975) Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56:841–854

    Google Scholar 

  • Herrera GL, C Maríntez del Río (1998) Pollen digestion by New World bats: effects of processing time and feeding habits. Ecology 79:2828–2838

    Google Scholar 

  • Horner MA, Fleming TH Sahley CT (1998) Foraging behaviour and energetics of a nectar-feeding bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J Zool (Lond) 244:575–586

    Google Scholar 

  • Howell, DJ (1974) Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp Biochem Physiol 48A:263–276

    Article  Google Scholar 

  • Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366

    Google Scholar 

  • 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 65:634–648

    CAS  Google Scholar 

  • Lemke TO (1984) Foraging ecology of the long-nosed bat, Glossophaga soricina, with respect to resource availability. Ecology 65:356–363

    Google Scholar 

  • 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)

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128

    CAS  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, London

  • Medellín RA, Equihua M, Amin MA (2000) Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conserv Biol 14:1666–1675

    Article  Google Scholar 

  • Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. J Ecol 90:100–107

    Article  Google Scholar 

  • 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 30–320

    Google Scholar 

  • Nobel PS, Quero E (1986) Environmental productivity and indices for a Chihuahuan desert plant Agave lechuguilla. Ecology 67:1–11

    Google Scholar 

  • Nowak RM (1994) Walker's bats of the world. The Johns Hopkins University Press, Baltimore, Maryland

  • 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, Mexico

  • Powell HA, G Powell (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19:176–179

    Google Scholar 

  • 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 88:2113–2118

    Google Scholar 

  • 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 1:293–392

    Google Scholar 

  • Roulston TH, JH Cane, SL Buchmann (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol Monogr 70:617–643

    Google Scholar 

  • SAS (2001) SASuser's guide: statistics. Release 8.2. SAS Institute, Cary, N.C., USA

  • Schulke, B, NM Waser (2001) Long-distance pollinator flights and pollen dispersal between populations of Delphinium muttallianum. Oecologia 127:239–245

    Article  Google Scholar 

  • 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 32:174–184

    Google Scholar 

  • Sih A, Baltus M (1987) Patch size, pollinator behaviour, and pollinator limitation in catnip. Ecology 68:1679–1690

    Google Scholar 

  • 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 94:234–256

    Google Scholar 

  • Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224

    PubMed  Google Scholar 

  • Spears EE (1987) Island and mainland pollination ecology of Centrosoma virginianum and Opuntia stricta. J Ecol 75:351–362

    Google Scholar 

  • Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440

    Article  Google Scholar 

  • Steffan-Dewenter I, Münzenberg U, Tscharntke T (2001) Pollination, seed set and seed predation on a landscape scale. Proc R Soc Lond Ser B 268:1685–1690

    Article  CAS  Google Scholar 

  • 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 151–171

  • 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 233–244

  • 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 34:462–467

    Google Scholar 

  • 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 12:357–373

    Article  Google Scholar 

  • Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS, Cary, N.C.

  • Sutherland S, Delph LF (1984) On the importance of male fitness in plants: patterns of fruit set. Ecology 65:1093–1104

    Google Scholar 

  • Toledo V. M. (1977) Pollination of some rain forest plants by non-hovering birds in Veracruz México. Biotropica 9:262–267

    Google Scholar 

  • 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 99:2038–2042

    Article  CAS  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  Google Scholar 

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Acknowledgements

We are grateful for support provided by grants from the Consejo Nacional de Ciencia y Tecnología, México, to M.Q., K.E.S. and J.A.L. (31826-N), the Dirección General de Asuntos del Personal Académico at the Universidad Nacional Autónoma de México to M.Q., K.E.S. and J.A.L. (IN213999), the Programa de Cooperación para el Desarrollo México-Costa Rica to M.Q., K.E.S., and J.A.L. (302CR075), the Vicerrectoria de Investigación at the Universidad de Costa Rica to J.A.L. (III-99-319), and the International Foundation for Science to M.Q. (D/2617–3). V.R.-G. received a scholarship from the Consejo Nacional de Ciencia y Tecnología y DGEP de UNAM and C.P.-G. received a scholarship from the Programa de Becas para tesis de licenciatura, UNAM. This study was performed in partial fulfillment of the requirements of the M.S. degree of V.R.-G. at the Universidad Nacional Autónoma de México. We thank A. Miranda and M. Valtierra from the Fundación Cuíxmala A.C. for logistical support and Y. Herrerías, L. Alemán-Figueroa, K.A.O. Salazar, and M.A. Munguía-Rosas for valuable assistance in the field. This manuscript was improved by the helpful comments of two anonymous reviewers.

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  1. Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27–3 (Xangari), 58089 , Morelia, Michoacán, Mexico

    Mauricio Quesada, Kathryn E. Stoner, Víctor Rosas-Guerrero & Carolina Palacios-Guevara

  2. Escuela de Biología, Universidad de Costa Rica, San Pedro, Costa Rica

    Jorge A. Lobo

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  1. Mauricio Quesada
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  2. Kathryn E. Stoner
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Correspondence to Mauricio Quesada.

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Quesada, M., Stoner, K.E., Rosas-Guerrero, V. et al. 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 . Oecologia 135, 400–406 (2003). https://doi.org/10.1007/s00442-003-1234-3

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