Short-distance pollen dispersal by bats in an urban setting: monitoring the movement of a vertebrate pollinator through fluorescent dyes

  • Ugo M. Diniz
  • Sinzinando A. Lima
  • Isabel C. S. Machado


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.


Breeding system Flowering synchrony Fluorescent dye Fragmentation Metapopulation connectivity Northeastern Brazil 



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.


  1. 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. CrossRefPubMedGoogle Scholar
  2. Armbruster WS, Muchhala N (2009) Associations between floral specialization and species diversity: cause, effect, or correlation? Evol Ecol 23(1):159–179. CrossRefGoogle Scholar
  3. Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15(4):257–267. CrossRefGoogle Scholar
  4. 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. CrossRefGoogle Scholar
  5. Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21(1):399–422. CrossRefGoogle Scholar
  6. Benedict MA, McMahon ET (2002) Green infrastructure: smart conservation for the 21st century. Renew Resour J 20(3):12–17Google Scholar
  7. Berthinussen A, Altringham J (2012) The effect of a major road on bat activity and diversity. J Appl Ecol 49(1):82–89. CrossRefGoogle Scholar
  8. 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. CrossRefPubMedGoogle Scholar
  9. 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. CrossRefGoogle Scholar
  10. Campbell DR (1991) Comparing pollen dispersal and gene flow in a natural population. Evol 45(8):1965–1968. CrossRefGoogle Scholar
  11. Campbell DR, Waser NM (1989) Variation in pollen flow within and among populations of Ipomopsis aggregata. Evol 43(7):1444–1455. CrossRefGoogle Scholar
  12. Chase MR, Moller C, Kesseli R, Bawa KS (1996) Distant gene flow in tropical trees. Nature 383(6599):399–399. CrossRefGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. Dearborn DC, Kark S (2010) Motivations for conserving urban biodiversity. Conserv Biol 24(2):432–440. CrossRefPubMedGoogle Scholar
  15. 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. CrossRefPubMedGoogle Scholar
  16. 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. CrossRefGoogle Scholar
  17. Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosystems 9(1):5–12. CrossRefGoogle Scholar
  18. Dobat K, Peikert-Holle T (1985) Blüten und Fledermäuse. Bestäubung durch Fledermäuse und Flughunde (Chiropterophilie). Waldemar Kramer, Frankfurt am MainGoogle Scholar
  19. 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. CrossRefGoogle Scholar
  20. Faegri KL, Pijl L Van Der (1979) The principles of pollination ecology. Pergamon Press, OxfordGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. 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. CrossRefPubMedGoogle Scholar
  24. Fleming TH, Geiselman C, Kress WJ (2009) The evolution of bat pollination: a phylogenetic perspective. Ann Bot 104(6):1017–1043. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fournier LA (1974) Un método cuantitativo para la medición de características fenológicas enárboles. Turrialba 24:422–423Google Scholar
  26. 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. CrossRefGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25(2):90–98. CrossRefPubMedGoogle Scholar
  29. 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. 175–251Google Scholar
  30. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 CommissionGoogle Scholar
  32. Hagen M et al. (2012) Biodiversity, Species Interactions and Ecological Networks in a Fragmented World. Advances in Ecological Research 46: 89–210.
  33. Harrison T, Winfree R (2015) Urban drivers of plant-pollinator interactions. Funct Ecol 29:879–888. CrossRefGoogle Scholar
  34. 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. CrossRefGoogle Scholar
  35. 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. 41–59Google Scholar
  36. Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosystems 15(1):149–166. CrossRefGoogle Scholar
  37. 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. CrossRefPubMedGoogle Scholar
  38. 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. CrossRefPubMedGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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. CrossRefGoogle Scholar
  42. 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. CrossRefGoogle Scholar
  43. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Law BS, Lean M (1999) Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biol Conserv 91(2):201–212. CrossRefGoogle Scholar
  45. Lemke TO (1985) Pollen carrying by the nectar-feeding bat Glossophaga soricina in a suburban environment. Biotropica 17:107–111. CrossRefGoogle Scholar
  46. Lloyd DG, Schoen DJ (1992) Self-and cross-fertilization in plants. I Functional dimensions Int J Plant Sci 153.3(1):358–369CrossRefGoogle Scholar
  47. Lorenzi H, Souza HM, Torres MAV, Bacher LB (2003) Árvores Exóticas no Brasil. Madeireiras, ornamentais e aromáticas. Instituto Plantarum de Estudos da Flora, Nova OdessaGoogle Scholar
  48. Madhukar VK, Srivastava SK, Dubey NK (2013) Revision of genus Crescentia L. (Bignoniaceae) in India. Am J Plant Sci 4(6):1164–1168. CrossRefGoogle Scholar
  49. Mckinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosystems 11(2):161–176CrossRefGoogle Scholar
  50. Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparo VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823CrossRefGoogle Scholar
  51. 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. CrossRefPubMedGoogle Scholar
  52. Murawski DA, Gilbert LE (1986) Pollen flow in Psiguria warscewiczii: a comparison of Heliconius butterflies and hummingbirds. Oecologia 68(2):161–167. CrossRefPubMedGoogle Scholar
  53. Nor ANM, Corstanje R, Harris JA, Grafius DR, Siriwardena GM (2017) Ecological connectivity networks in rapidly expanding cities. Heliyon 3(6):e00325. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ohashi K, Thomson JD (2009) Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants. Ann Bot 103(9):1365–1378. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120(3):321–326. CrossRefGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. Pernambuco (2017) APAC - Agência Pernambucana de Águas e Clima. Governo do Estado de Pernambuco. Accessed 17 October 2017
  58. Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862CrossRefGoogle Scholar
  59. 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. CrossRefGoogle Scholar
  60. 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. CrossRefGoogle Scholar
  61. Rademaker MCJ, De Jong TJ, Klinkhamer PGL (1997) Pollen dynamics of bumble-bee visitation on Echium vulgare. Funct Ecol 11(5):554–563. CrossRefGoogle Scholar
  62. 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.Google Scholar
  63. Rech AR, Agostini K, Oliveira PEGM, Machado ICS (2014) Biologia da Polinização. Editora Projeto Cultural, Rio de JaneiroGoogle Scholar
  64. 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. CrossRefGoogle Scholar
  65. Schaub A, Ostwald J, Siemers BM (2008) Foraging bats avoid noise. J Exp Biol 211(19):3174–3180. CrossRefPubMedGoogle Scholar
  66. 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):1646–1652CrossRefGoogle Scholar
  67. 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. CrossRefGoogle Scholar
  68. Stone EL, Jones G, Harris S (2009) Street lighting disturbs commuting bats. Curr Biol 19(13):1123–1127. CrossRefPubMedGoogle Scholar
  69. 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. CrossRefGoogle Scholar
  70. 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. mCrossRefPubMedGoogle Scholar
  71. 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. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ugo M. Diniz
    • 1
  • Sinzinando A. Lima
    • 1
  • Isabel C. S. Machado
    • 1
  1. 1.Laboratory of Floral and Reproductive Biology, Botany Department, Center of BiosciencesFederal University of PernambucoRecifeBrazil

Personalised recommendations