Oceanic Island Bats as Flower visitors and pollinators
DOI:
https://doi.org/10.26786/1920-7603(2023)764Keywords:
Canary Islands, Chiroptera, diet, nectar, Phyllostomidae, PteropodidaeAbstract
Oceanic islands are relatively poor in insects compared to mainland areas. Therefore, insect-eating island birds and lizards may include other food sources into their diet, e.g. nectar and pollen. Here, we explore if insect-eating island bats face a similar problem and accordingly join the birds and lizards and incorporate plant resources into their diet. Thus, a priory, we assume flower visitation by bats to be more common on oceanic islands than elsewhere. To test this, we reviewed the literature to obtain information on the geographic distribution and diet of all 1,399 species of bats in the world and found that 49%, 21%, and 31% of species have a mainland, mixed mainland-island, and island distribution, respectively. Diets are known for only 65% (905 species) of the bats in the world, and 70%, 22%, and 8% of these, respectively, rely on insects, fruit, and floral resources as their major diet component. Twenty-seven species are even obligate flower visitors. This study confirms that flower-visiting bats, especially Pteropodidae, are significantly more frequent on oceanic islands, while insect eaters are more frequent on mainland and continental islands. Consequently, we argue that flower visitation and pollination by insect-eating island bats require more attention in future island ecology studies. For a start, we list known examples in the literature and report a case study from the Canary Islands. In the latter, we examined the foreheads of 34 museum specimens of the seven Canarian bat species. Half of them carried pollen from ≥ 9 taxa, but only three bat species had larger amounts. Pollen was not identified, but many Canarian and exotic plant species are candidates. Thus, flower visitation by bats may be an oceanic island phenomenon, but requires more focused research, especially night-time flower observations and examination of bats for pollen.
References
Abrahamczyk S (2019) Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide. Biological Reviews, 94: 1658–1671. https://doi.org/10.1111/brv.12520 DOI: https://doi.org/10.1111/brv.12520
Abrahamczyk S, Souto-Vilarós D, Renner SS (2014) Escape from extreme specialization: Passionflowers, bats and the sword-billed hummingbird. Proceedings of the Royal Society B. Biological Sciences 281: 20140888. https://doi.org/10.1098/rspb.2014.0888 DOI: https://doi.org/10.1098/rspb.2014.0888
Allan JD, Barnthouse LW, Prestbye RA, Strong DR (1973) On foliage arthropod communities of Puerto Rican second growth vegetation. Ecology 54: 628–632. https://doi.org/10.2307/1935350 DOI: https://doi.org/10.2307/1935350
Amorim FW, Ballarin CS, Spicacci G, Bergamasco G, Carvalho L, Uieda W, Moraes AP (2023) Opossums and birds facilitate the unexpected bat visitation to the ground-flowering Scybalium fungiforme. Ecology 104: ecy.3935. DOI: https://doi.org/10.1002/ecy.3935
https://doi.org/10.1002/ecy.3935 DOI: https://doi.org/10.1002/ecy.3935
Arkins AM, Winnington AP, Anderson SA, Clout MN (1999) Diet and nectarivorous foraging behaviour of the short-tailed bat (Mystacina tuberculata). Journal of Zoology 247: 183–187. https://doi.org unknown. DOI: https://doi.org/10.1111/j.1469-7998.1999.tb00982.x
Blanco G, Laiolo P, Fargallo JA (2013) Linking environmental stress, feeding-shifts and the "island syndrome": A nutritional challenge hypothesis. Population Ecology 56: 203–216. https://doi.org/10.1007/s10144-013-0404-3 DOI: https://doi.org/10.1007/s10144-013-0404-3
Cordero-Schmidt E, Maruyama PK, Vargas-Mena JC, Oliveira PP, Santos FdAR, Medellín RA, Rodriguez-Herrera B, Venticinque EM (2021) Bat-flower interaction networks in Caatinga reveal generalized associations and temporal stability. Biotropica 53: 1546–1557. https://doi.org/10.1111/btp.13007 DOI: https://doi.org/10.1111/btp.13007
Correcher EJ, Hervías-Parejo S, Carnero RdY, Sauroy-Toucouère S, Traveset A (2023) Environmental and morphological drivers of mutualistic plant-lizard interactions: A global review. Ecography 2023: e06425. https://doi.org/10.1111/ecog.0642 DOI: https://doi.org/10.1111/ecog.06425
Cox PA, Ricklefs RE (1977) Species diversity and ecological release in Caribbean land bird faunas. Oikos 28: 113–122. https://doi.org/10.2307/3543330 DOI: https://doi.org/10.2307/3543330
Datzmann T, Helversen Ov, Mayer F (2010) Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Ecology and Evolution 10: 165. https://doi.org/10.1186/1471-2148-10-165 DOI: https://doi.org/10.1186/1471-2148-10-165
Diniz UM, Aguiar LMdS (2023) The interplay between spatiotemporal overlap and morphology as determinants of microstructure suggests no ‘perfect fit’ in a bat-flower network. Scientific Reports 13: 2737. https://doi.org/10.1038/s41598-023-29965-3 DOI: https://doi.org/10.1038/s41598-023-29965-3
Domingos-Melo A, Milet-Pinheiro P, Navarro DMdAF, Lopes AV, Machado IC (2019) It’s raining fragrant nectar in the Caatinga: Evidence of nectar olfactory signaling in bat-pollinated flowers. Bulletin of the Ecological Society of America 1010: e01640. https://doi.org/10.1002/ecy.2914 DOI: https://doi.org/10.1002/ecy.2914
Fægri K, Pijl Lvd (1971) The principles of pollination ecology. 2nd ed. Pergamon press, Oxford.
Farnsworth A (2020) Green-throated Carib (Eulampis holosericeus), v. 1.0. In: Schulenberg TS (ed.) Birds of the World. Cornell Laboratory of Ornithology, Ithaca, NY. DOI: https://doi.org/10.2173/bow.grtcar1.01
Fleming TH, Dávalos LM, Mello MAR (2020) Phyllostomid bats. A unique Mammalian radiation. University of Chicago Press, Chicago. DOI: https://doi.org/10.7208/chicago/9780226696263.001.0001
Fleming TH, Geiselman C, Kress WJ (2009) The evolution of bat pollination: A phylogenetic perspective. Annals of Botany 104: 1017–1043. https://doi.org/10.1093/aob/mcp197 DOI: https://doi.org/10.1093/aob/mcp197
Fleming TH, Kress WJ (2013) The ornaments of life. Coevolution and conservation in the tropics. University of Chicago Press, Chicago. DOI: https://doi.org/10.7208/chicago/9780226023328.001.0001
Frick WF, Heady PA, Hayes JP (2009) Facultative nectar-feeding behavior in a gleaning insectivorous bat (Antrozous pallidus). Journal of Mammalogy 90: 1157–1164. https://doi.org/10.1644/09-MAMM-A-001.1 DOI: https://doi.org/10.1644/09-MAMM-A-001.1
Fuster F, Kaiser-Bunbury C, Olesen JM, Traveset A (2019) Global patterns of the double mutualism phenomenon. Ecography 42: 826–835. https://doi.org/10.1111/ecog.04008 DOI: https://doi.org/10.1111/ecog.04008
González-Gutiérrez K, Castaño JH, Pérez-Torres J, Mosquera-Mosquera HR (2022) Structure and roles in pollination networks between phyllostomid bats and flowers: A systematic review for the Americas. Mammalian Biology 102: 21–49. https://doi.org/10.1007/s42991-021-00202-6 DOI: https://doi.org/10.1007/s42991-021-00202-6
Gribel R, Gibbs PE (2002) High outbreeding as a consequence of selfed ovule mortality and single vector bat pollination in the Amazonian tree Pseudobombax munguba (Bombacaceae). International Journal of Plant Sciences 163: 1035–1043. https://doi.org/10.1086/342518 DOI: https://doi.org/10.1086/342518
Griffin MJ, Trewick SA, Wehi PM, Morgan-Richards M (2011) Exploring the concept of niche convergence in a land without rodents: The case of weta as small mammals. New Zealand Journal of Ecology 35: 302–307. https://doi.org unknown.
Janzen DH (1973) Sweep samples of tropical foliage insects: Effect of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54: 687–708. https://doi.org/10.2307/1935359 DOI: https://doi.org/10.2307/1935359
Kahnt B, Theodorou P, Grimm-Seyfarth A, Onstein RE (2023) When lizards shift to a more plant-based lifestyle: The macroevolution of mutualistic lizard-plant interactions (Squamata: Sauria/Lacertilia). Molecular Phylogenetics and Evolution 186: 107839. https://doi.org/10.1016/j.ympev.2023.107839 DOI: https://doi.org/10.1016/j.ympev.2023.107839
Lopes LE, Fernandes AM, Medeiros MCI, Marini MA (2016) A classification scheme for avian diet types. Journal of Field Ornithology 87: 309–322. https://doi.org/ 10.1111/jofo.12158 DOI: https://doi.org/10.1111/jofo.12158
McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds.) Coevolution of animals and plants. Symposium V, First International Congress of Systematic and Evolutionary Biology, Boulder, Colorado. University of Texas Press, Austin, Texas, pp. 159–191. DOI: https://doi.org/10.7560/710313-009
Meiri S (2018) Traits of lizards of the world: Variation around a successful evolutionary design. Global Ecology and Biogeography 27: 1168–1172. DOI: https://doi.org/10.1111/geb.12773
https://doi.org/10.1111/geb.12773 DOI: https://doi.org/10.1111/geb.12773
Monteiro LR, Nogueira MR (2011) Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Ecology and Evolution 11: 137. https://doi.org/10.1186/1471-2148-11-137 DOI: https://doi.org/10.1186/1471-2148-11-137
Morse DH (1971) The insectivorous bird as an adaptive strategy. Annual Review of Ecology and Systematics 2: 177–200. https://doi.org/10.1146/ANNUREV.ES.02.110171.001141 DOI: https://doi.org/10.1146/annurev.es.02.110171.001141
Nyffeler M, Şekercioğlu CH, Whelan CJ (2018) Insectivorous birds consume an estimated 400-500 million tons of prey annually. Science of Nature 105: 47. https://doi.org/ 10.1007/s00114-018-1571-z DOI: https://doi.org/10.1007/s00114-018-1571-z
Olesen JM (2022) Ego network analysis of the trophic structure of an island land bird through 300 years of climate change and invaders. Ecology and Evolution 12: e8916. https://doi.org/10.1002/ece3.8916 DOI: https://doi.org/10.1002/ece3.8916
Olesen JM, Carstensen DW, Dupont YL (2010) Island pollination: Ways to solve the species poverty problem. In: Pérez–Mellado V, Ramon MaM (eds.) Islands and evolution. Institut Menorquí d’Estudis. Recerca 19, pp. 147–169.
Olesen JM, Damgaard CF, Fuster F, Heleno RH, Nogales M, Rumeu B, Trøjelsgaard K, Vargas P, Traveset A (2018) The disclosure of the double role of birds in the Galápagos. Scientific Reports 8: 57. https://doi.org/10.1093/aobpla/plz001 DOI: https://doi.org/10.1038/s41598-017-17592-8
Olesen JM, Valido A (2003a) Lizards as pollinators and seed dispersers: An island phenomenon. Trends in Ecology and Evolution 18: 177–181. https://doi.org/ 10.1016/S0169-5347(03)00004-1 DOI: https://doi.org/10.1016/S0169-5347(03)00004-1
Olesen JM, Valido A (2003b) Bird pollination in Madeira Island. Ardeola 50: 65–67. https://www.jstor.org/stable/3554673
Percival MS (1965) Floral biology. Pergamon Press, Oxford.
Rojas D, Vale Á, Ferrero V, Navarro L (2011) When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Molecular Ecology 20: 2217–2228. https://doi.org/ 10.1111/j.1365-294X.2011.05082.x DOI: https://doi.org/10.1111/j.1365-294X.2011.05082.x
Spears EE (1987) Island and mainland pollination ecology of Centrosema virginianum and Opuntia stricta. Journal of Ecology 75: 351–362. https://doi.org/10.2307/2260423 DOI: https://doi.org/10.2307/2260423
Traveset A, Olesen JM, Nogales M, Vargas P, Jaramillo P, Antolín E, Trigo MM, Heleno R (2015) Bird-flower visitation networks in the Galápagos unveil a widespread interaction release. Nature Communications 6: 6376. https://doi.org/10.1038/ncomms7376 DOI: https://doi.org/10.1038/ncomms7376
Tripp EA, Manos PS (2008) Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution 62: 1712–1737. https://doi.org/10.1111/j.1558-5646.2008.00398.x DOI: https://doi.org/10.1111/j.1558-5646.2008.00398.x
Trujillo D (1991) Murciélagos de las Islas Canarias. Icona, Ministerio de Agricultra, Pesca y Alimentación, Madrid.
Uetz P, Freed P, Aguilar R, Hošek J (eds.) (2022) The Reptile Database. http://www.reptile-database.org
Valido A, Dupont YL, Olesen JM (2004) Bird-flower interactions in the Macaronesian Islands. Journal of Biogeography 31: 1945–1953. DOI: https://doi.org/10.1111/j.1365-2699.2004.01116.x
https://doi.org/10.1111/j.1365-2699.2004.01116.x DOI: https://doi.org/10.1111/j.1365-2699.2004.01116.x
Valido A, Olesen JM (2010) Pollination on islands: Examples from the Macaronesian archipelagos. In: Serrano ARM, Borges PAV, Boieiro M, Oromí P (eds.) Terrestrial Arthropods of Macaronesia – Biodiversity, Ecology and Evolution. Fundação para a Ciência e a Tecnologia, Portugal, pp. 249–283.
Valido A, Olesen JM (2019) Frugivory and seed dispersal by lizards: A global review. Frontiers in Ecology and Evolution 7: 49. https://doi.org/10.3389/fevo.2019.00049 DOI: https://doi.org/10.3389/fevo.2019.00049
Wilman H, Belmaker J, Simpson J, de La Rosa C, Rivadeneira MM, Jetz W (2014) Elton Traits 1.0: Species-level foraging attributes of the world’s birds and mammals. Ecology 95: 2014–2027. https://doi.org/ 10.1890/13-1917.1 DOI: https://doi.org/10.1890/13-1917.1
Wilson DE, Lacher Jr TE, Mittermeier RA (eds.) (2016) Lagomorphs and Rodents I. Handbook of the mammals of the world. Vol. 6. Lynx Edicions, Barcelona.
Wilson DE, Lacher Jr TE, Mittermeier RA (eds.) (2016) Rodents II. Handbook of the mammals of the world. Vol. 7. Lynx Edicions, Barcelona.
Wilson DE, Mittermeier RA (eds.) (2019) Bats. Handbook of the mammals of the world. Vol. 9. Lynx Edicions, Barcelona.
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