Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Seed dispersal by Neotropical bats in human-disturbed landscapes

André Luis Regolin https://orcid.org/0000-0003-1820-8400 A B F , Renata L. Muylaert https://orcid.org/0000-0002-6466-6210 A E , Ana Cristina Crestani https://orcid.org/0000-0002-7707-6199 C , Wesley Dáttilo https://orcid.org/0000-0002-4758-4379 D and Milton Cezar Ribeiro https://orcid.org/0000-0002-4312-202X A
+ Author Affiliations
- Author Affiliations

A Institute of Biosciences, São Paulo State University – UNESP, Campus Rio Claro, Department of Biodiversity, Spatial Ecology and Conservation Lab (LEEC), Avenida 24 A, 1515, Jardim Bela Vista, Rio Claro, São Paulo, CEP 13506900, Brazil.

B Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Wagar Building, CSU Main Campus, Fort Collins, CO 80523, USA.

C Institute of Biosciences, São Paulo State University – UNESP, Campus Rio Claro, Department of Biodiversity, Birds Ecology Lab (LECAVE), Avenida 24 A, 1515, Jardim Bela Vista, Rio Claro, São Paulo, CEP 13506900, Brazil.

D Red de Ecoetología, Instituto de Ecología AC, A Coatepec 351, El Haya, Xalapa-Enríquez, CP 91070, Veracruz, Mexico.

E Present address: Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand.

F Corresponding author. Email: andreregolin@gmail.com

Wildlife Research - https://doi.org/10.1071/WR19138
Submitted: 13 August 2019  Accepted: 7 May 2020   Published online: 5 August 2020

Abstract

In human-modified landscapes, where large bird and mammal species are often functionally extinct, bats are the main seed dispersers. However, the role of seed dispersal by bats for the maintenance of habitat dynamics in fragmented landscapes is still not understood, with information lacking on landscape-level effects of plant–bat interactions. We present some key topics related to spatial ecology of bats and discuss the potential influence of habitat fragmentation on several aspects of seed dispersal by Neotropical bats. We suggest that future studies need to evaluate bat–plant networks along habitat-loss and fragmentation gradients at the landscape level, including changes in land-cover types and habitat structural complexity, going beyond patch-based analysis. By advancing on the comprehension of ecosystem functioning in fragmented landscapes, we will better understand the bat-modulated seed-dispersal process, supporting regeneration and restoration programs that benefit from bat-based functions.

Additional keywords: Chiroptera, ecological networks, ecosystem services, gradients, habitat loss, restoration, tropical ecology.


References

Andrade, T. Y., Thies, W., Rogeri, P., Kalko, E. V., and Mello, M. A. R. (2013). Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera, Phyllostomidae). Journal of Mammalogy 94, 1094–1101.
Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera, Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |

Arroyo-Rodríguez, V., and Fahrig, L. (2014). Why is a landscape perspective important in studies of primates? American Journal of Primatology 76, 901–909.
Why is a landscape perspective important in studies of primates?Crossref | GoogleScholarGoogle Scholar | 24715680PubMed |

Arteaga, L. L., Aguirre, L. F., and Moya, M. I. (2006). Seed rain produced by bats and birds in forest islands in a Neotropical savanna. Biotropica 38, 718–724.
Seed rain produced by bats and birds in forest islands in a Neotropical savanna.Crossref | GoogleScholarGoogle Scholar |

Barros, F. M., Peres, C. A., Pizo, M. A., and Ribeiro, M. C. (2019). Divergent flows of avian-mediated ecosystem services across forest–matrix interfaces in human-modified landscapes. Landscape Ecology 34, 879–894.
Divergent flows of avian-mediated ecosystem services across forest–matrix interfaces in human-modified landscapes.Crossref | GoogleScholarGoogle Scholar |

Bascompte, J. (2010). Structure and dynamics of ecological networks. Science 329, 765–766.
Structure and dynamics of ecological networks.Crossref | GoogleScholarGoogle Scholar | 20705836PubMed |

Bello, C., Galetti, M., Montan, D., Pizo, M. A., Mariguela, T. C., Culot, L., Bufalo, F., Labecca, F., Pedrosa, F., Constantini, R., Emer, C., Silva, W. R., da Silva, F. R., Ovaskainen, O., and Jordano, P. (2017). Atlantic–frugivory: a plant–frugivore interaction dataset for the Atlantic Forest. Ecology 98, 1729.
Atlantic–frugivory: a plant–frugivore interaction dataset for the Atlantic Forest.Crossref | GoogleScholarGoogle Scholar | 28317110PubMed |

Boscolo, D., Tokumoto, P. M., Ferreira, P. A., Ribeiro, J. W., and Santos, J. S. (2017). Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspectives in Ecology and Conservation 15, 18–24.
Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels.Crossref | GoogleScholarGoogle Scholar |

Brady, M. J., McAlpine, C. A., Possingham, H. P., Miller, C. J., and Baxter, G. S. (2011). Matrix is important for mammals in landscapes with small amounts of native forest habitat. Landscape Ecology 26, 617–628.
Matrix is important for mammals in landscapes with small amounts of native forest habitat.Crossref | GoogleScholarGoogle Scholar |

Bueno, R. S., Guevara, R., Ribeiro, M. C., Culot, L., Bufalo, F. S., and Galetti, M. (2013). Functional redundancy and complementarities of seed dispersal by the last Neotropical megafrugivores. PLoS One 8, e56252.
Functional redundancy and complementarities of seed dispersal by the last Neotropical megafrugivores.Crossref | GoogleScholarGoogle Scholar | 23409161PubMed |

Castaño, J. H., Carranza, J. A., and Pérez-Torres, J. (2018). Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats. Acta Oecologica 91, 81–90.
Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats.Crossref | GoogleScholarGoogle Scholar |

Cazetta, E., Galetti, M., Rezende, E. L., and Schaefer, H. M. (2012). On the reliability of visual communication in vertebrate-dispersed fruits. Journal of Ecology 100, 277–286.
On the reliability of visual communication in vertebrate-dispersed fruits.Crossref | GoogleScholarGoogle Scholar |

Chazdon, R. L., and Guariguata, M. R. (2016). Natural regeneration as a tool for large-scale forest restoration in the tropics: prospects and challenges. Biotropica 48, 716–730.
Natural regeneration as a tool for large-scale forest restoration in the tropics: prospects and challenges.Crossref | GoogleScholarGoogle Scholar |

Corro, E. J., Ahuatzin, D. A., Aguirre, A., Favila, M. E., Ribeiro, M. C., Acosta, J. C. L., and Dáttilo, W. (2019). Forest cover and landscape heterogeneity shape ant-plant co-occurrence networks in human-dominated tropical rainforests. Landscape Ecology 34, 93–104.
Forest cover and landscape heterogeneity shape ant-plant co-occurrence networks in human-dominated tropical rainforests.Crossref | GoogleScholarGoogle Scholar |

da Silva, A. G., Gaona, O., and Medellín, R. A. (2008). Diet and trophic structure in a community of fruit-eating bats in Lacandon Forest, México. Journal of Mammalogy 89, 43–49.
Diet and trophic structure in a community of fruit-eating bats in Lacandon Forest, México.Crossref | GoogleScholarGoogle Scholar |

Dáttilo, W., and Rico-Gray, V. (2018). ‘Ecological Networks in the Tropics: an Integrative Overview of Species Interactions from Some of the Most Species-rich Habitats on Earth.’ (Springer: Basel.)

Dirzo, R., Young, H. S., Galetti, M., Ceballos, G., Isaac, N. J. B., and Collen, B. (2014). Defaunation in the Anthropocene. Science 345, 401–406.
Defaunation in the Anthropocene.Crossref | GoogleScholarGoogle Scholar | 25061202PubMed |

Driscoll, D. A., Banks, S. C., Barton, P. S., Lindenmayer, D. B., and Smith, A. L. (2013). Conceptual domain of the matrix in fragmented landscapes. Trends in Ecology and Evolution 28, 605–613.
Conceptual domain of the matrix in fragmented landscapes.Crossref | GoogleScholarGoogle Scholar | 23883740PubMed |

Emer, C., Galetti, M., Pizo, M. A., Guimarães, P. R., Moraes, S., Piratelli, A., and Jordano, P. (2018). Seed-dispersal interactions in fragmented landscapes: a metanetwork approach. Ecology Letters 21, 484–493.
Seed-dispersal interactions in fragmented landscapes: a metanetwork approach.Crossref | GoogleScholarGoogle Scholar | 29368364PubMed |

Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics 34, 487–515.
Effects of habitat fragmentation on biodiversity.Crossref | GoogleScholarGoogle Scholar |

Fahrig, L. (2013). Rethinking patch size and isolation effects. The habitat amount hypothesis. Journal of Biogeography 40, 1649–1663.
Rethinking patch size and isolation effects. The habitat amount hypothesis.Crossref | GoogleScholarGoogle Scholar |

Farneda, F. Z., Rocha, R., López-Baucells, A., Groenenberg, M., Silva, I., Palmeirim, J. M., Bobrowiec, P. E. D., and Meyer, C. F. J. (2015). Trait-related responses to habitat fragmentation in Amazonian bats. Journal of Applied Ecology 52, 1381–1391.
Trait-related responses to habitat fragmentation in Amazonian bats.Crossref | GoogleScholarGoogle Scholar |

Fenton, M. B., and Simmons, N. (2014). ‘Bats: a World of Science and Mystery.’ (The University of Chicago Press: Chicago, IL, USA.)

Galetti, M., Guevara, R., Cortes, M., Fadini, R., Von Matter, S., Leite, A. B., Labecca, F., Ribeiro, T., Carvalho, C., Collevatti, R., Pires, M., Guimaraes, P. R., Brancalion, P. H., Ribeiro, M. C., and Jordano, P. (2013). Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090.
Functional extinction of birds drives rapid evolutionary changes in seed size.Crossref | GoogleScholarGoogle Scholar | 23723235PubMed |

Galindo-González, J., Guevara, S., and Sosa, V. J. (2000). Bat- and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conservation Biology 14, 1693–1703.

García-García, J. L., Santos-Moreno, A., and Kraker-Castañeda, C. (2014). Ecological traits of phyllostomid bats associated with sensitivity to tropical forest fragmentation in Los Chimalapas, Mexico. Tropical Conservation Science 7, 457–474.
Ecological traits of phyllostomid bats associated with sensitivity to tropical forest fragmentation in Los Chimalapas, Mexico.Crossref | GoogleScholarGoogle Scholar |

Geiselman, C. K., Defex, T., Brown, T., and Younger, S. (2015). Database Bat Eco-interactions [WWW document]. Available at http://www.batplant.org/search [verified 1 January 2019].

Gorresen, P. M., and Willig, M. R. (2004). Landscape responses of bats to habitat fragmentation in Atlantic Forest of Paraguay. Journal of Mammalogy 85, 688–697.
Landscape responses of bats to habitat fragmentation in Atlantic Forest of Paraguay.Crossref | GoogleScholarGoogle Scholar |

Gregorin, R., Bernard, B., Lobão, K. W., Oliveira, L. F., Machado, F. S., Gil, B. B., and Tavares, V. C. (2017). Vertical stratification in bat assemblages of the Atlantic Forest of south-eastern Brazil. Journal of Tropical Ecology 33, 299–308.
Vertical stratification in bat assemblages of the Atlantic Forest of south-eastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Hernández-Montero, J. R., Saldaña-Vázquez, R. A., Galindo-González, J., and Sosa, V. J. (2015). Bat–fruit interactions are more specialized in shaded-coffee plantations than in tropical mountain cloud forest fragments. PLoS One 10, e0126084.
Bat–fruit interactions are more specialized in shaded-coffee plantations than in tropical mountain cloud forest fragments.Crossref | GoogleScholarGoogle Scholar | 25992550PubMed |

Howe, H. F. (2016). Making dispersal syndromes and networks useful in tropical conservation and restoration. Global Ecology and Conservation 6, 152–178.
Making dispersal syndromes and networks useful in tropical conservation and restoration.Crossref | GoogleScholarGoogle Scholar |

Jackson, H. B., and Fahrig, L. (2015). Are ecologists conducting research at the optimal scale? Global Ecology and Biogeography 24, 52–63.
Are ecologists conducting research at the optimal scale?Crossref | GoogleScholarGoogle Scholar |

Kerches-Rogeri, P., Niebuhr, B. B., Muylaert, R. L., and Mello, M. A. R. (2020). Individual specialization in the space use of frugivorous bats. Journal of Animal Ecology.

Kunz, T. H., Torrez, E. B., Bauer, D., Lobova, T., and Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223, 1–38.
Ecosystem services provided by bats.Crossref | GoogleScholarGoogle Scholar | 21449963PubMed |

Laurindo, R. S., Novaes, R. L. M., Vizentin-Bugoni, J., and Gregorin, R. (2019). The effects of habitat loss on bat–fruit networks. Biodiversity and Conservation 28, 589–601.
The effects of habitat loss on bat–fruit networks.Crossref | GoogleScholarGoogle Scholar |

Lobova, T. A., Geiselman, C. K., and Mori, S. A. (2009). ‘Seed Dispersal by Bats in the Neotropics.’ (The New York Botanical Garden Press: New York, NY, USA.)

McConkey, K. R., and O’Farrill, G. (2012). Seed dispersal in changing landscapes. Biological Conservation 146, 1–13.
Seed dispersal in changing landscapes.Crossref | GoogleScholarGoogle Scholar |

Medeiros, H. R., Hoshino, A. D., Ribeiro, M. C., and Junior, A. O. M. (2016). Landscape complexity affects cover and species richness of weeds in Brazilian agricultural environments. Basic and Applied Ecology 17, 731–740.
Landscape complexity affects cover and species richness of weeds in Brazilian agricultural environments.Crossref | GoogleScholarGoogle Scholar |

Medellín, R. A., and Gaona, O. (1999). Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, México. Biotropica 31, 478–485.
Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, México.Crossref | GoogleScholarGoogle Scholar |

Mello, M. A. R., Leiner, N. O., Guimarães-Jr, P. R., and Jordano, P. (2005). Size-based fruit selection of Calophyllum brasiliense (Clusiaceae) by bats of the genus Artibeus (Phyllostomidae) in a Restinga area, southeastern Brazil. Acta Chiropterologica 7, 179–182.
Size-based fruit selection of Calophyllum brasiliense (Clusiaceae) by bats of the genus Artibeus (Phyllostomidae) in a Restinga area, southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Mello, M. A. R., Marquitti, F. M. D., Guimarães-Jr, P. R., Kalko, E. K. V., Jordano, P., and Aguiar, M. A. M. (2011). The missing part of seed dispersal networks, structure and robustness of bat-fruit interactions. PLoS One 6, e17395.
The missing part of seed dispersal networks, structure and robustness of bat-fruit interactions.Crossref | GoogleScholarGoogle Scholar |

Mello, M. A. R., Rodrigues, F. A., Costa, L. F., Kissling, W. D., Şekercioğlu, C. H., Marquitti, F. M. D., and Kalko, E. K. V. (2015). Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124, 1031–1039.
Keystone species in seed dispersal networks are mainly determined by dietary specialization.Crossref | GoogleScholarGoogle Scholar |

Mello, M. A. R., Felix, G. M., Pinheiro, R. B., Muylaert, R. L., Geiselman, C., Santana, S. E., Tschapka, M., Lofti, N., Rodrigues, F. A., and Stevens, R. D. (2019). Insights into the assembly rules of a continent-wide multilayer network. Nature Ecology & Evolution 3, 1525–1532.
Insights into the assembly rules of a continent-wide multilayer network.Crossref | GoogleScholarGoogle Scholar |

Melo, F. P. L., Rodriguez-Herrera, B., Chazdon, R. L., Medellin, R. A., and Ceballos, G. G. (2009). Small tent-roosting bats promote dispersal of large-seeded plants in a Neotropical forest. Biotropica 41, 737–743.
Small tent-roosting bats promote dispersal of large-seeded plants in a Neotropical forest.Crossref | GoogleScholarGoogle Scholar |

Muscarella, R., and Fleming, T. H. (2007). The role of frugivorous bats in tropical forest succession. Biological Reviews of the Cambridge Philosophical Society 82, 573–590.
The role of frugivorous bats in tropical forest succession.Crossref | GoogleScholarGoogle Scholar | 17944618PubMed |

Muylaert, R. L. (2014). Influência multi-escala da paisagem e limiar da fragmentação em morcegos no cerrado. Masters Dissertation, Universidade Estadual Paulista ‘Júlio de Mesquita’, Brazil.

Muylaert, R. L., Matos, D. M. D. S., and Mello, M. A. R. (2014). Interindividual variations in fruit preferences of the yellow-shouldered bat Sturnira lilium (Chiroptera, Phyllostomidae) in a cafeteria experiment. Mammalia 78, 93–101.
Interindividual variations in fruit preferences of the yellow-shouldered bat Sturnira lilium (Chiroptera, Phyllostomidae) in a cafeteria experiment.Crossref | GoogleScholarGoogle Scholar |

Muylaert, R. L., Steves, R. D., and Ribeiro, M. C. (2016). Threshold effect of habitat loss on bat richness in cerrado–forest landscapes. Ecological Applications 26, 1854–1867.
Threshold effect of habitat loss on bat richness in cerrado–forest landscapes.Crossref | GoogleScholarGoogle Scholar | 27755693PubMed |

Niebuhr, B. B. S., Wosniack, M. E., Santos, M. C., Raposo, E. P., Viswanathan, G. M., Luz, M. G. E., and Pie, M. R. (2015). Survival in patchy landscapes, the interplay between dispersal, habitat loss and fragmentation. Scientific Reports 5, 11898.
Survival in patchy landscapes, the interplay between dispersal, habitat loss and fragmentation.Crossref | GoogleScholarGoogle Scholar |

Oliveira, M. A., Grillo, A. S., and Tabarello, M. (2004). Forest edge in the Brazilian Atlantic forest, drastic changes in tree species assemblages. Oryx 38, 389–394.
Forest edge in the Brazilian Atlantic forest, drastic changes in tree species assemblages.Crossref | GoogleScholarGoogle Scholar |

Oliveira, H. F. M., Camargo, N. F., Gager, Y., Muylaert, R. L., Ramon, E., and Martins, R. C. C. (2019). Protecting the cerrado: where should we direct efforts for the conservation of bat–plant interactions? Biodiversity and Conservation , .
Protecting the cerrado: where should we direct efforts for the conservation of bat–plant interactions?Crossref | GoogleScholarGoogle Scholar |

Peña-Domene, M., Martínez-Garza, C., Palmas-Pérez, S., Rivas-Alonso, E., and Howe, H. F. (2014). Roles of birds and bats in early tropical-forest restoration. PLoS One 9, 1–6.

Ribeiro, M. C. (2010). Simulation models applied to the conservation of fragmented landscapes in the Brazilian Atlantic Forest. Ph.D. Dissertation, Universidade de São Paulo, São Paulo, SP, Brazil.

Sarmento, R., Alves-Costa, C. P., Ayub, A., and Mello, M. A. R. (2014). Partitioning of seed dispersal services between birds and bats in a fragment of the Brazilian Atlantic Forest. Zoologia 31, 245–255.
Partitioning of seed dispersal services between birds and bats in a fragment of the Brazilian Atlantic Forest.Crossref | GoogleScholarGoogle Scholar |

Simmons, N.B. and A.L. Cirranello. (2019). ‘Bat Species of the World: a Taxonomic and Geographic Database.’ Available at https://www.batworlds.com/bat-species/ [verified 12 October 2019].

Voigt, C. C., Frick, W. F., Holderied, M. W., Holland, R., Kerth, G., Mello, M. A. R., Plowright, R. K., Swartz, S., and Yovel, Y. (2017). Principles and patterns of bat movements, from aerodynamics to ecology. The Quarterly Review of Biology 92, 267–287.
Principles and patterns of bat movements, from aerodynamics to ecology.Crossref | GoogleScholarGoogle Scholar | 29861509PubMed |