Abstract
Pollen dispersal in tropical seed plants is established mainly by biotic vectors, both in intact and fragmented environments. In urban landscapes, the segregation of natural remnants by an artificial matrix can reduce pollinator foraging efficiency. It is unknown how nectarivorous bats, regarded as long-distance pollen dispersers, respond to such habitat structure combined with city-related factors. Here, we investigated the pollen dispersal pattern between spatially segregated individuals of the bat-pollinated Bignoniaceae Crescentia cujete within an urban environment. From 2015 to 2017, we assessed their spatiotemporal structure, breeding system and annual fruit set in order to relate these factors to the bat activity in the region. We employed fluorescent dyes as pollen analogues to infer the role of bats in pollen flow. Adding to the low density of individuals, we found a low daily flower emission and low flowering synchrony (S = 0,092), all of which are traits that favor outcrossing. Individuals were distributed in two distant groups (>600 m), with no occurrence of dye flow between them. In contrast, flow within the same individual was intense, which points toward bats’ territorial behavior. C. cujete is self-compatible, but not autogamous; therefore, despite few outcross events, bats could be ensuring the plant’s year-round fruit production mainly through self-pollination. Our findings show restricted bat foraging extent, which affects overall pollen dispersal distance and population connectivity. These results can be extrapolated to natural metapopulations inserted in an urban matrix and serve as a groundwork for studying directly the effect of city-related factors on pollinator behavior.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler LS, Irwin RE (2005) Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann Bot 97(1):141–150. https://doi.org/10.1093/aob/mcj012
Armbruster WS, Muchhala N (2009) Associations between floral specialization and species diversity: cause, effect, or correlation? Evol Ecol 23(1):159–179. https://doi.org/10.1007/s10682-008-9259-z
Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15(4):257–267. https://doi.org/10.2307/2387650
Avila-Flores R, Fenton MB (2005) Use of spatial features by foraging insectivorous bats in a large urban landscape. J Mammal 86(6):1193–1204. https://doi.org/10.1644/04-MAMM-A-085R1.1
Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21(1):399–422. https://doi.org/10.1146/annurev.es.21.110190.002151
Benedict MA, McMahon ET (2002) Green infrastructure: smart conservation for the 21st century. Renew Resour J 20(3):12–17
Berthinussen A, Altringham J (2012) The effect of a major road on bat activity and diversity. J Appl Ecol 49(1):82–89. https://doi.org/10.1111/j.1365-2664.2011.02068.x
Browne L, Ottewell K, Sork VL, Karubian J (2018) The relative contributions of seed and pollen dispersal to gene flow and genetic diversity in seedlings of a tropical palm. Mol Ecol 27(15):3159–3173. https://doi.org/10.1111/mec.14768
Bunkley JP, McClure CJ, Kleist NJ, Francis CD, Barber JR (2015) Anthropogenic noise alters bat activity levels and echolocation calls. Glob Ecol Conserv 3:62–71. https://doi.org/10.1016/j.gecco.2014.11.002
Campbell DR (1991) Comparing pollen dispersal and gene flow in a natural population. Evol 45(8):1965–1968. https://doi.org/10.1111/j.1558-5646.1991.tb02702.x
Campbell DR, Waser NM (1989) Variation in pollen flow within and among populations of Ipomopsis aggregata. Evol 43(7):1444–1455. https://doi.org/10.1111/j.15585646.1989.tb02595.x
Chase MR, Moller C, Kesseli R, Bawa KS (1996) Distant gene flow in tropical trees. Nature 383(6599):399–399. https://doi.org/10.1038/383398a0
Collevatti RG, Estolano R, Garcia SF, Hay JD (2010) Short-distance pollen dispersal and high self-pollination in a bat-pollinated neotropical tree. Tree Genet Genomes 6(4):555–564. https://doi.org/10.1007/s11295-010-0271-4
Dearborn DC, Kark S (2010) Motivations for conserving urban biodiversity. Conserv Biol 24(2):432–440. https://doi.org/10.1111/j.1523-1739.2009.01328.x
Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12(3):753–764. https://doi.org/10.1046/j.1365-294X.2003.01760.x
Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rainforest trees. Trop Plant Biol 1(1):20–33. https://doi.org/10.1007/s12042-0079006-6
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosystems 9(1):5–12. https://doi.org/10.1007/s11252-006-3262-3
Dobat K, Peikert-Holle T (1985) Blüten und Fledermäuse. Bestäubung durch Fledermäuse und Flughunde (Chiropterophilie). Waldemar Kramer, Frankfurt am Main
Erickson JL, West SD (2002) The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropterologica 4(1):17–24. https://doi.org/10.3161/001.004.0103
Faegri KL, Pijl L Van Der (1979) The principles of pollination ecology. Pergamon Press, Oxford
Fenster CB, Dudash MR, Hassler CL (1996) Fluorescent dye particles are good pollen analogs for hummingbird-pollinated Silene virginica (Caryophyllaceae). Can J Bot 74(2):189–193. https://doi.org/10.1139/b96-023
Fenton MB (1970) A technique for monitoring bat activity with results obtained from different environments in southern Ontario. Can J Zool 48(4):847–851. https://doi.org/10.1139/z70-148
Ferreira BHS, Gomes AC, Souza CS, Fabri JS, Sigrist MR (2017) Pollination and reproductive system of synchronopatric species of Cactaceae (Cactoideae) subject to interspecific flow of pollen: an example of ecological adaptation in the Brazilian Chaco. Plant Biol 20(1):101–112. https://doi.org/10.1111/plb.12641
Fleming TH, Geiselman C, Kress WJ (2009) The evolution of bat pollination: a phylogenetic perspective. Ann Bot 104(6):1017–1043. https://doi.org/10.1093/aob/mcp197
Fournier LA (1974) Un método cuantitativo para la medición de características fenológicas enárboles. Turrialba 24:422–423
Freitas L, Bolmgren K (2008) Synchrony is more than overlap: measuring phenological synchronization considering time length and intensity. Braz J Bot 31(4):721–724. https://doi.org/10.1590/S0100-84042008000400017
Fuchs EJ, Lobo JA, Quesada M (2003) Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata. Conserv Biol 17(1):149–157. https://doi.org/10.1646/Q1571
Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25(2):90–98. https://doi.org/10.1016/j.tree.2009.07.016
Gómez-Baggethun E, Gren Å, Barton DN, Langemeyer J, McPhearson T, O’Farrell P, Andersson E, Hamstead Z and Kremer P (2013) Urban ecosystem services. In: Elmqvist et al. (eds) Urbanization, biodiversity and ecosystem services: Challenges and opportunities (pp.). Springer, Dordrecht, p. 175–251
Gonzalez-Terrazas TP, Martel C, Milet-Pinheiro P, Ayasse M, Kalko EK, Tschapka M (2016) Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar. R Soc Open Sci 3(8):160199. https://doi.org/10.1098/rsos.160199
Gribel R, Lemes MR (1997) Mating system and pollen flow of Ceiba pentandra (Bombacaceae) in Central Amazon. Assessment of levels and dynamics of intra-specific genetic diversity of tropical trees. Second Annual Report to the European Commission
Hagen M et al. (2012) Biodiversity, Species Interactions and Ecological Networks in a Fragmented World. Advances in Ecological Research 46: 89–210. https://doi.org/10.1016/B978-0-12-396992-7.00002-2
Harrison T, Winfree R (2015) Urban drivers of plant-pollinator interactions. Funct Ecol 29:879–888. https://doi.org/10.1111/1365-2435.12486
Heithaus ER, Fleming TH, Opler PA (1975) Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecol 56(4):841–854. https://doi.org/10.2307/1936295
Helversen O Von (1993) Adaptations of flowers to pollination by glossophagine bats. In: Barthlott W (ed) Animal-plant interactions in tropical environments. Museum Koenig, Bonn, p. 41–59
Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosystems 15(1):149–166. https://doi.org/10.1007/s11252-011-0202-7
Herrera CM (1989) Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system. Oecologia 80(2):241–248. https://doi.org/10.1007/BF00380158
Hobbhahn M, Steenhuisen S, Olsen T, Midgley JJ, Johnson SD (2017) Pollination and breeding system of the enigmatic south African parasitic plant Mystropetalon thomii (Mystropetalaceae): rodents welcome, but not needed. Plant Biol 19(5):775–786. https://doi.org/10.1111/plb.12580
Horner MA, Fleming TH, Sahey CT (1998) Foraging behaviour and energetics of a nectar-feeding bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J Zool 244(4):575–586. https://doi.org/10.1111/j.1469-7998.1998.tb00062.x
Kameyama Y, Kudo G (2009) Flowering phenology influences seed production and outcrossing rate in populations of an alpine snowbed shrub, Phyllodoce aleutica: effects of pollinators and self-incompatibility. Ann Bot 103(9):1385–1394. https://doi.org/10.1093/aob/mcp037
Kormann U, Scherber C, Tscharntke T, Klein N, Larbig M, Valente JJ, Hadley AS, Betts MG (2018) Corridors restore animal-mediated pollination in fragmented tropical forest landscapes. Proc R Soc B 283:20152347. https://doi.org/10.1098/rspb.2015.2347
Lacerda EAB, Kanashiro M, Sebbenn AM (2008) Long-pollen movement and deviation of random mating in a low-density continuous population of a tropical tree Hymenaea courbaril in the Brazilian Amazon. Biotropica 40(4):462–470. https://doi.org/10.1111/j.1744-7429.2008.00402.x
Lacoeuilhe A, Machon N, Julien JF, Le Bocq A, Kerbiriou C (2014) The influence of low intensities of light pollution on bat communities in a semi-natural context. PLoS One 9(10):e103042. https://doi.org/10.1371/journal.pone.0103042
Law BS, Lean M (1999) Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biol Conserv 91(2):201–212. https://doi.org/10.1016/S0006-3207(99)00078-6
Lemke TO (1985) Pollen carrying by the nectar-feeding bat Glossophaga soricina in a suburban environment. Biotropica 17:107–111. https://doi.org/10.2307/2388502
Lloyd DG, Schoen DJ (1992) Self-and cross-fertilization in plants. I Functional dimensions Int J Plant Sci 153.3(1):358–369
Lorenzi H, Souza HM, Torres MAV, Bacher LB (2003) Árvores Exóticas no Brasil. Madeireiras, ornamentais e aromáticas. Instituto Plantarum de Estudos da Flora, Nova Odessa
Madhukar VK, Srivastava SK, Dubey NK (2013) Revision of genus Crescentia L. (Bignoniaceae) in India. Am J Plant Sci 4(6):1164–1168. https://doi.org/10.4236/ajps.2013.46143
Mckinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosystems 11(2):161–176
Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparo VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823
Muchhala N, Thomson JD (2010) Fur versus feathers: pollen delivery by bats and hummingbirds and consequences for pollen production. The Am Nat 175:717–726. https://doi.org/10.1086/652473
Murawski DA, Gilbert LE (1986) Pollen flow in Psiguria warscewiczii: a comparison of Heliconius butterflies and hummingbirds. Oecologia 68(2):161–167. https://doi.org/10.1007/BF00384782
Nor ANM, Corstanje R, Harris JA, Grafius DR, Siriwardena GM (2017) Ecological connectivity networks in rapidly expanding cities. Heliyon 3(6):e00325. https://doi.org/10.1016/j.heliyon.2017.e00325
Ohashi K, Thomson JD (2009) Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants. Ann Bot 103(9):1365–1378. https://doi.org/10.1093/aob/mcp088
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120(3):321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Parsons KN, Jones G, Greenaway F (2003) Swarming activity of temperate zone microchiropteran bats: effects of season, time of night and weather conditions. J Zool 261(3):257–264. https://doi.org/10.1017/S0952836903004199
Pernambuco (2017) APAC - Agência Pernambucana de Águas e Clima. Governo do Estado de Pernambuco. http://www.apac.pe.gov.br/. Accessed 17 October 2017
Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862
Queiroz JA, Quirino ZGM, Lopes AV, Machado IC (2016) Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ 125:21–30. https://doi.org/10.1016/j.jaridenv.2015.09.015
Quesada M, Stoner KE, Lobo JA, Herrerías-Diego Y, Palacios-Guevara C, Munguía-Rosas MA, Salazar KAO, Rosas-Guerrero V (2004) Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated bombacaceous trees. Biotropica 36(2):131–138. https://doi.org/10.1646/Q1571
Rademaker MCJ, De Jong TJ, Klinkhamer PGL (1997) Pollen dynamics of bumble-bee visitation on Echium vulgare. Funct Ecol 11(5):554–563. https://doi.org/10.1046/j.1365-2435.1997.00124.x
Ramalho MMM, Locatelli E (2011) Interações ecológicas em Crescentia cujete L. (Bignoniaceae): uma espécie quiropterófila. In: Resumos X Congresso de Ecologia do Brasil. São Lourenço. 3 pp.
Rech AR, Agostini K, Oliveira PEGM, Machado ICS (2014) Biologia da Polinização. Editora Projeto Cultural, Rio de Janeiro
Scanlon AT, Petit S (2009) Effects of site, time, weather and light on urban bat activity and richness: considerations for survey effort. Wildl Res 35(8):821–834. https://doi.org/10.1071/WR08035
Schaub A, Ostwald J, Siemers BM (2008) Foraging bats avoid noise. J Exp Biol 211(19):3174–3180. https://doi.org/10.1242/jeb.037283
Siemers BM, Schaub A (2011) Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators. Proceedings of the Royal Society of London B: Biol Sci 278(1712):1646–1652
Stacy EA, Hamrick JL, Nason JD, Hubbell SP, Foster RB, Condit R (1996) Pollen dispersal in low-density populations of three neotropical tree species. The Am Nat 148(2):275–298. https://doi.org/10.1086/285925
Stone EL, Jones G, Harris S (2009) Street lighting disturbs commuting bats. Curr Biol 19(13):1123–1127. https://doi.org/10.1016/j.cub.2009.05.058
Thiele J, Winter Y (2005) Hierarchical strategy for relocating food targets in flower bats: spatial memory versus cue-directed search. Anim Behav 69(2):315–327. https://doi.org/10.1016/j.anbehav.2004.05.012
Thomson JD, Price MV, Waser NM, Stratton DA (1986) Comparative studies of pollen and fluorescent dye transport by bumblebees visiting Erythronium grandiflorum. Oecologia 69:561–566. https://doi.org/10.1007/BF00410363 m
Winter Y, Stich KP (2005) Foraging in a complex naturalistic environment: capacity of spatial working memory in flower bats. J Exp Biol 208(3):539–548. https://doi.org/10.1242/jeb.01416
Acknowledgments
To National Council of Scientific and Technological Development (CNPq) for the concession of research scholarships to UMD and SAL during 2016 and 2017 (Proc.n. 138381/2016; 106160/2017-6), a research grant to ICM (Proc.n. 311021/2014-0), and also for partial financial support (Proc.n. 459485/2014-8). To R.C.G Oliveira for the support in the field and A.D. Melo for suggestions on data analysis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Diniz, U.M., Lima, S.A. & Machado, I.C.S. Short-distance pollen dispersal by bats in an urban setting: monitoring the movement of a vertebrate pollinator through fluorescent dyes. Urban Ecosyst 22, 281–291 (2019). https://doi.org/10.1007/s11252-019-0825-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-019-0825-7