Hostname: page-component-77f85d65b8-grvzd Total loading time: 0 Render date: 2026-04-18T17:28:30.445Z Has data issue: false hasContentIssue false
  • English
  • Français

Body mass determines the role of mammal species in a frugivore-large fruit interaction network in a Neotropical savanna

Published online by Cambridge University Press:  16 January 2023

Larissa Gabriela Araujo Goebel Open the ORCID record for Larissa Gabriela Araujo Goebel [Opens in a new window] ,
Breno Dias Vitorino Open the ORCID record for Breno Dias Vitorino [Opens in a new window] ,
Angélica Vilas Boas Frota Open the ORCID record for Angélica Vilas Boas Frota [Opens in a new window]  and
Manoel dos Santos-Filho Open the ORCID record for Manoel dos Santos-Filho [Opens in a new window]
Larissa Gabriela Araujo Goebel*
Affiliation:
Programa de Pós-graduação stricto sensu em Ciências Ambientais, Centro de Pesquisa em Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso, Cáceres, Mato Grosso, Brazil Laboratório de Mastozoologia, Cáceres, Mato Grosso, Brazil
Breno Dias Vitorino
Affiliation:
Programa de Pós-graduação stricto sensu em Ciências Ambientais, Centro de Pesquisa em Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso, Cáceres, Mato Grosso, Brazil
Angélica Vilas Boas Frota
Affiliation:
Programa de Pós-graduação stricto sensu em Ciências Ambientais, Centro de Pesquisa em Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso, Cáceres, Mato Grosso, Brazil
Manoel dos Santos-Filho
Affiliation:
Programa de Pós-graduação stricto sensu em Ciências Ambientais, Centro de Pesquisa em Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso, Cáceres, Mato Grosso, Brazil Laboratório de Mastozoologia, Cáceres, Mato Grosso, Brazil
*
Author for correspondence: Larissa Gabriela Araujo Goebel, Email larissagabriela_goebel@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Frugivorous mammals play an important role in maintaining biodiversity and are considered one of the main dispersers of large seeds. In this study, we describe the structure of the interaction network between non-flying mammals and seven plant species with large fruits in a megadiverse savanna-forest mosaic in the Brazilian Cerrado. We also evaluated the individual contribution of each species to the organization of the interaction network and tested whether body mass determined the mammals’ role in the network. To record frugivory events of mammals with arboreal and terrestrial habits, camera traps were installed at ground and canopy levels. We identified 18 mammal species interacting with seven plant species in 515 frugivory events. Our observations highlight an interaction network with a modular and non-nested topology and the important role of large mammals in the network structure, which reflects the importance of the group in potential seed dispersal. The extinction of large frugivorous mammals can cause several damages to ecosystem services in the Brazilian Cerrado through changes in network structure, especially threatening the survival of plant species with large fruits.

Keywords

Cerradoecological networksfrugivoryseed dispersalTapirus terrestris

Information

Type
Research Article
Information
Journal of Tropical Ecology , Volume 39 , 2023 , e12
Check for updates
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abreu-Jr, EF, Casali, DM, Garbino, GST, Loretto, D, Loss, AC, Marmontel, M, Nascimento, MC, Oliveira, ML, Pavan, SE and Tirelli, FP (2020) Lista de Mamíferos do Brasil 2020. Comitê de Taxonomia da Sociedade Brasileira de Mastozoologia (CT-SBMz). Available at: <https://wwwsbmzorg/mamiferos-do-brasil>. Access on 29 September 2020..+Access+on+29+September+2020.>Google Scholar
Almeida-Neto, M, Guimaraes, P, Guimaraes, PR Jr, Loyola, RD and Ulrich, W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.CrossRefGoogle Scholar
Almeida-Neto, M and Ulrich, W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling & Software 26, 173–178.CrossRefGoogle Scholar
Alvares, CA, Stape, JL, Sentelhas, PC, Moraes Gonçalves, JL and Sparovek, G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.CrossRefGoogle Scholar
Bascompte, J and Jordano, P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review Ecology Evolution and Syst ematics 38, 567–593.CrossRefGoogle Scholar
Bello, C, Galetti, M, Pizo, MA, Magnago, LFS, Rocha, MF, Lima, RAF, Peres, CA, Ovaskainen, O and Jordano, P (2015) Defaunation affects carbon storage in tropical forests. Science Advances 1, 1–11.Google ScholarPubMed
Bogoni, JA, Graipel, ME and Peroni, N (2018) The ecological footprint of Acca sellowiana domestication maintains the residual vertebrate diversity in threatened highlands of Atlantic Forest. PLoS One 13, 1–24.CrossRefGoogle ScholarPubMed
Brasil (2016) Plano de Manejo Estação Ecológica da Serra das Araras. Ministério do Meio Ambiente. Brasília, 252 pp. Available from: <https://www.icmbio.gov.br/portal/images/stories/plano-de-manejo/dcom_plano_de_manejo_Esec_Serra_das_Araras.pdf> Access on 15 de September 2020.+Access+on+15+de+September+2020.>Google Scholar
Brazil Flora (2020) Brazilian Flora 2020 project - Projeto Flora do Brasil 2020. v393.261. Instituto de Pesquisas Jardim Botanico do Rio de Janeiro. Dataset/Checklist. Available at: <https://floradobrasil.jbrj.gov.br/>. Access on 05 January 2020..+Access+on+05+January+2020.>Google Scholar
Cagua, EF, Wootton, KL and Stouffer, DB (2019) Keystoneness, centrality, and the structural controllability of ecological networks. Journal of Ecology 107, 1779–1790.CrossRefGoogle Scholar
Carreira, DC, Dáttilo, W, Bruno, DL, Percequillo, AR, Ferraz, KMPMB and Galetti, M (2020) Small vertebrates are key elements in the frugivory networks of a hyperdiverse tropical forest. Scientific Reports 10, 1–11.CrossRefGoogle ScholarPubMed
Chao, A (1984) Nonparametric estimation of the number of classes in a population. Scandinavian Journal of statistics 11, 265–270.Google Scholar
Chiarello, AG (2000) Density and population size of mammals in remnants of Brazilian Atlantic Forest. Conservation Biology 14, 1649–1657.CrossRefGoogle ScholarPubMed
Crestani, AC, Mello, MAR and Cazetta, E (2019) Interindividual variations in plant and fruit traits affect the structure of a planta-frugivore network. Acta Oecologica 95, 120–127.CrossRefGoogle Scholar
Delmas, E, Besson, M, Brice, MH, Burkle, LA, Dalla Riva, GV, Fortin, MJ, Gravel, D, Guimarães, PR Jr, Hembry, DH, Newman, EA, Olesen, JM, Pires, MM, Yeakel, JD and Poisot, T (2019). Analysing ecological networks of species interactions. Biological Reviews 94, 16–36.CrossRefGoogle ScholarPubMed
Dirzo, R, Young, HS, Galetti, M, Ceballos, G, Isaac, NJ and Collen, B (2014) Defaunation in the Anthropocene. Science 345, 401–406.CrossRefGoogle ScholarPubMed
Donatti, CI, Guimarães, PR, Galetti, M, Pizo, MA, Marquitti, FMD and Dirzo, R (2011) Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecology Letters 14, 773–781.CrossRefGoogle ScholarPubMed
Dormann, CF, Fruend, J and Gruber, B (2020) Visualising bipartite networks and calculating some (ecological) indices. R package version 2.15.Google Scholar
Dormann, CF and Strauss, R (2014) A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5, 90–98.CrossRefGoogle Scholar
Dugger, PJ, Blendinger, PG, Böhning-Gaese, K, Chama, L, Correia, M, Dehling, DM, Emer, C, Farwig, N, Fricke, EC, Galetti, M, García, D, Grass, I, Heleno, R, Jacomassa, FAF, Moraes, S, Moran, C, Muñoz, MC, Neuschulz, EL, Nowak, L, Piratelli, A, Pizo, MA, Quitián, M, Rogers, HS, Ruggera, RA, Saavedra, F, Sánchez, MS, Sánchez, R, Santillán, V, Schabo, DG, Silva, FR, Timóteo, S, Traveset, A, Vollstädt, MGR and Schleuning, M (2019) Seed-dispersal networks are more specialized in the Neotropics than in the Afrotropics. Global Ecology and Biogeography 28, 248–261.CrossRefGoogle Scholar
Emmons, L and Feer, F (1997) Neotropical rainforest mammals: a field guide. Chicago: The University of Chicago Press, 392 p.Google Scholar
Encinas-Viso, F, Revilla, TA and Etienne, RS (2012) Phenology drives the structure and diversity of the mutualistic network. Ecology Letters 15, 198–208.CrossRefGoogle ScholarPubMed
Ferreira, GB, Collen, B, Newbold, T, Oliveira, MJR, Pinheiro, MS, Pinho, FF, Rowcliffe, M and Carbone, C (2020) Strict protected areas are essential for the conservation of larger and threatened mammals in a priority region of the Brazilian Cerrado. Biological Conservation 251, 108762.CrossRefGoogle Scholar
Fuzessy, LF, Janson, C and Silveira, FAO (2018) Effects of seed size and frugivory degree on dispersal by Neotropical frugivores. Acta Oecologica 93, 41–47.CrossRefGoogle Scholar
Galetti, M, Bovendorp, RS and Guevara, R (2015) Defaunation of large mammals leads to an increase in seed predation in the Atlantic forests. Global Ecology and Conservation 3, 824–830.CrossRefGoogle Scholar
Galetti, M and Dirzo, R (2013) Ecological and evolutionary consequences of living in a defaunated world. Biological Conservation 163, 1–6.CrossRefGoogle Scholar
Galetti, M, Guevara, R, Cortes, MC, Fadini, R, Von Matter, S, Leite, AB, Labecca, F, Ribeiro, T, Carvalho, C S, Collevatti, RG, Pires, MM, Guimaraes, PR, Brancalion, PH, Ribeiro, MC and Jordano, P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090.CrossRefGoogle ScholarPubMed
Godínez-Alvarez, H, Ríos-Casanova, L and Peco, B (2020) Are large frugivorous birds better seed dispersers than medium-and small-sized ones? Effect of body mass on seed dispersal effectiveness. Ecology and Evolution 10, 6136–6143.CrossRefGoogle ScholarPubMed
Golin, V, Santos-Filho, M and Pereira, MJB (2011) Dispersal and predation of araticum seeds in the Cerrado of Mato Grosso, Brazil. Ciência Rural 41, 101–107.CrossRefGoogle Scholar
Harvey, E, Gounand, I, Ward, CL and Altermatt, F (2017) Bridging ecology and conservation: from ecological networks to ecosystem function. Journal of Applied Ecology 54, 371–379.CrossRefGoogle Scholar
Hsieh, TC, Ma, KH and Chao, A (2020) iNEXT: Interpolation and Extrapolation for Species Diversity. R package version 2.0.20. Available at: <http://chao.stat.nthu.edu.tw/wordpress/software_download>. Access on 30 January 2021..+Access+on+30+January+2021.>Google Scholar
IUCN (2022) The IUCN Red List of Threatened Species. Version 2021-3. Available at: <https://www.iucnredlist.org/>. Access on 14 de February 2022..+Access+on+14+de+February+2022.>Google Scholar
Jordano, P, Bascompte, J and Olesen, JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6, 69–81.CrossRefGoogle Scholar
Jordano, P, Forget, PM, Lambert, JE, Böhning-Gaese, K, Traveset, A and Wright, SJ (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7, 321–323.CrossRefGoogle ScholarPubMed
Jordano, P, Garcia, C, Godoy, JA and García-Castaño, JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proceedings of the National Academy of Sciences 104, 3278–3282.CrossRefGoogle ScholarPubMed
Kuhlmann, M (2018) Frutos e Sementes do Cerrado: Espécies Atrativas Para A Fauna. Brasília, Brazil: Ipsis Gráfica e Editora, pp. 1–464.Google Scholar
Lacher, TE, Davidson, AD, Fleming, TH, Gómez-Ruiz, EP, McCracken, GF, Owen-Smith, N, Peres, CA and Vander Wall, SB (2019) The functional roles of mammals in ecosystems. Journal of Mammalogy 100, 942–964.CrossRefGoogle Scholar
Lim, JY, Svenning, JC, Göldel, B, Faurby, S and Kissling, WD (2020) Frugivore-fruit size relationships between palms and mammals reveal past and future defaunation impacts. Nature Communications 11, 1–13.CrossRefGoogle ScholarPubMed
Machado-de-Souza, T, Campos, RP, Devoto, M and Varassin, IG (2019) Local drivers of the structure of a tropical bird-seed dispersal network. Oecologia 189, 421–433.CrossRefGoogle ScholarPubMed
Magioli, M, Barros, KMPM, Chiarello, AG, Galetti, M, Setz, EZF, Paglia, AP, Abregoi, O, Ribeiro, MC and Ovaskainen, O (2021a) Land-use changes lead to functional loss of terrestrial mammals in a Neotropical rainforest. Perspectives in Ecology and Conservation 19, 161–170.CrossRefGoogle Scholar
Magioli, M, Rios, E, Benchimol, M, Casanova, DC, Ferreira, AS, Rocha, J, Melo, FR, Dias, MP, Narezi, G, Crepaldi, MO, Mendes, LAM, Nobre, RA, Chiarello, AG, García-Olaechea, A, Nobre, AB, Devids, CC, Cassano, CR, Koike, CDV, Bernardo, CSS, Homem, DH, Ferraz, DS, Abreu, DG, Cazetta, E, Lima, EF, Bonfim, FCG, Lima, F, Prado, HA, Santos, HG, Nodari, JZ, Giovanelli, JGR, Nery, MS, Faria, MB, Ferreira, PCR, Gomes, PS, Rodarte, R, Borges, R, Zuccolotto, TFS, Sarcinelli, TS, Endo, W, Matsuda, Y, Camargos, VL, Morato, RG (2021b) The role of protected and unprotected forest remnants for mammal conservation in a megadiverse Neotropical hotspot. Biological Conservation 259, 109173.CrossRefGoogle Scholar
Martín González, AM, Dalsgaard, B and Olesen, JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity 7, 36–43.CrossRefGoogle Scholar
Moore, JF, Soanes, K, Balbuena, D, Beirne, C, Bowler, M, Carrasco-Rueda, F, Cheyne, SM, Coutant, O, Pierre-Michel, F, Haysom, JK, Houlihan, PR, Olson, ER, Lindshield, S, Martin, J, Tobler, M, Whitworth, A and Gregory, T (2021) The potential and practice of arboreal camera trapping. Methods in Ecology and Evolution 2021, 1–12.Google Scholar
Naniwadekar, R, Chaplod, S, Datta, A, Rathore, A and Sridhar, H (2019) Large frugivores matter: insights from network and seed dispersal effectiveness approaches. Journal of Animal Ecology 88,1–13.CrossRefGoogle ScholarPubMed
O’Farrill, G, Galetti, M and Campos-Arceiz, A (2013) Frugivory and seed dispersal by tapirs: an insight on their ecological role. Integrative Zoology 8, 4–17.CrossRefGoogle ScholarPubMed
Olesen, JM, Bascompte, J, Dupont, YL and Jordano, P (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences 104, 19891–19896.CrossRefGoogle ScholarPubMed
Palacio, RD, Valderrama-Ardila, C and Kattan, GH (2016) Generalist species have a central role in a highly diverse plant-frugivore network. Biotropica 48, 349–355.CrossRefGoogle Scholar
Queiroz, JA, Diniz, UM, Vázquez, DP, Quirino, ZM, Santos, FA, Mello, MA and Machado, IC (2021) Bats and hawkmoths form mixed modules with flowering plants in a nocturnal interaction network. Biotropica 53, 596–607.CrossRefGoogle Scholar
Raíces, DSL, Ferreira, PM, Mello, JHF and Bergallo, HG (2017) Smile, you are on camera or in a live trap! the role of mammals in dispersion of jackfruit and native seeds in Ilha Grande state park, Brazil. Nature Conservation Research 2, 78–89.CrossRefGoogle Scholar
Raimundo, RLG, Guimarães, PR and Evans, DM (2018) Adaptive networks for restoration ecology. Trends in Ecology & Evolution 33, 664–675.CrossRefGoogle ScholarPubMed
Ramos-Robles, M, Andresen, E and Díaz-Castelazo, C (2018) Modularity and robustness of a plant-frugivore interaction network in a disturbed tropical forest. Ecoscience 25, 209–222.CrossRefGoogle Scholar
R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available at <https://www.r-project.org/>. Access on 10 December 2020..+Access+on+10+December+2020.>Google Scholar
Ripple, WJ, Newsome, TM, Wolf, C, Dirzo, R, Everatt, KT, Galetti, M, Hayward, MW, Kerley, GIH, Levi, T, Lindsey, PA, Macdonald, DW, Malhi, Y, Painter, LE, Sandom, CJ, Terborgh, J and Valkenburgh, BV (2015) Collapse of the world’s largest herbivores. Science Advances 1, 1e1400103.CrossRefGoogle ScholarPubMed
Santos-Filho, M, Frieiro-Costa, F, Ignácio, ÁRA and Silva, MF (2012) Use of habitats by non-volant small mammals in Cerrado in Central Brazil. Brazilian Journal of Biology 72, 893–902.CrossRefGoogle ScholarPubMed
Santos-Filho, M and Silva, MNF (2002) Uso de habitats por mamíferos em área de Cerrado do Brasil Central: um estudo com armadilhas fotográficas. Revista Brasileira de Zoociências 4, 57–73.Google Scholar
Sukma, HT, Di Stefano, J, Swan, M and Sitters, H (2019) Mammal functional diversity increases with vegetation structural complexity in two forest types. Forest Ecology and Management 433, 85–92.CrossRefGoogle Scholar
Vázquez, DP, Melián, CJ, Williams, NM, Blüthgen, N, Krasnov, BR and Poulin, R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116, 1120–1127.CrossRefGoogle Scholar
Vidal, MM, Pires, MM and Guimarães, PR (2013) Large vertebrates as the missing components of seed-dispersal networks. Biological Conservation 163, 42–48.CrossRefGoogle Scholar
Villar, N, Paz, C, Zipparro, V, Nazareth, S, Bulascoschi, L, Bakker, ES and Galetti, M (2020) Frugivory underpins the nitrogen cycle. Functional Ecology 35, 357–368 . CrossRefGoogle Scholar
Vitorino, BD, da Frota, AVB, Castrillon, SKI and Nunes, JRS (2018) Birds of Estação Ecológica da Serra das Araras, state of Mato Grosso, Brazil: additions and review. Check List 14, 893–922.CrossRefGoogle Scholar
Wilman, H, Belmaker, J, Simpson, J, de la Rosa, C, Rivadeneira, MM and Jetz, W (2014) EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027–2027.CrossRefGoogle Scholar
Wintle, BA, Kujala, H, Whitehead, A, Cameron, A, Veloz, S, Kukkala, A, Moilanen, A, Gordon, A, Lentini, PE, Cadenhead, NCR and Bekessy, SA (2019) Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proceedings of the National Academy of Sciences 116, 909–914.CrossRefGoogle ScholarPubMed
Young, HS, McCauley, DJ, Galetti, M and Dirzo, R (2016) Patterns, causes, and consequences of anthropocene defaunation. Annual Review of Ecology, Evolution, and Systematics 47, 333–358.CrossRefGoogle Scholar
Zhu, C, Li, W, Gregory, T, Wang, D, Ren, P, Zeng, D, Kang, Y, Ding, P and Si, X (2021) Arboreal camera trapping: a reliable tool to monitor plant-frugivore interactions in the trees on large scales. Remote Sensing in Ecology and Conservation 8, 92–104.CrossRefGoogle Scholar
Supplementary material: File

Goebel et al. supplementary material

Goebel et al. supplementary material

Download Goebel et al. supplementary material(File)
File 516.6 KB