animal extirpation; tropical forest; satiation; forest health indicator
Abstract :
[en] Seed removal is a key component of seed dispersal and may be influenced by both landscape-scale and local attributes, and it has been used as an indicator of the intensity of interactions between ecosystem components. We examined how the seed removal rates, which integrate the activity of seed dispersers and seed predators, vary with landscape-scale forest cover. We collected data under 34 trees belonging to two zoochoric species (Helicostylis tomentosa (Poepp. and Endl.) J. F. Macbr. and Inga vera Willd.) in 17 remnants in the Brazilian Atlantic forest, with different percentages of forest cover. The seed removal rate was estimated using a fast method based on the abundance of intact fruits and fruit scraps on the ground. The amount of forest cover affected the rate of seed removal in a humpbacked shape, with a maximum seed removal rate at intermediate forest cover. Seed removal rates must be related to the amount of food resources offered and diversity of dispersers and predators in the region. In landscapes with intermediate forest amount, there is a better balance between supply and demand for fruits, leading to a higher seed removal rate than more deforested or forested landscape. Our results also show that local factors, such as crop size and canopy surface, together with forest cover amount, are also important to the removal rate, depending on the species. In addition, our results showed that plant–animal interactions are occurring in all fragments, but the health status of these forests is similar to disturbed forests, even in sites immersed in forested landscapes.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Hambuckers, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Trolliet, Franck ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement
Simon, Astrid
Cazetta, E.
Rocha-Santos, L.
Language :
English
Title :
Seed Removal Rates in Forest Remnants Respond to Forest Loss at the Landscape Scale. Forests 2020, 11, 1144.
Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 2003, 34, 487–515. [CrossRef]
Betts, M.G.; Wolf, C.; Ripple, W.J.; Phalan, B.; Millers, K.A.; Duarte, A.; Butchart, S.H.M.; Levi, T. Global forest loss disproportionately erodes biodiversity in intact landscapes. Nature 2017, 547, 441–444. [CrossRef] [PubMed]
Boissier, O.; Bouiges, A.; Mendoza, I.; Feer, F.; Forget, P.-M. Rapid assessment of seed removal and frugivore activity as a tool for monitoring the health status of tropical forests. Biotropica 2014, 46, 633–641. [CrossRef]
Lawton, J.H.; Naeem, S.; Thompson, L.J.; Hector, A.; Crawley, M.J.; Thompson, K.; Hodgson, J.G. Biodiversity and ecosystem function: Getting the Ecotron experiment in its correct context. Funct. Ecol. 1998, 12, 848–853.
Bibby, C.J.; Burgess, N.D.; Hill, D.A.; Mustoe, S. Bird Census Techniques, 2nd ed.; Academic Press: Amsterdam, The Netherlands, 2000.
Gardner, T.A.; Barlow, J.; Araujo, I.S.; Ávila-Pires, T.C.; Bonaldo, A.B.; Costa, J.E.; Esposito, M.C.; Ferreira, L.V.; Hawes, J.; Hernandez, M.I.M.; et al. The cost-effectiveness of biodiversity surveys in tropical forests. Ecol. Lett. 2008, 11, 139–150. [CrossRef] [PubMed]
Abate, T. Environmental rapid-assessment programs have appeal and critics. Are they the domain of the conservation elite? BioScience 1992, 42, 486–489. [CrossRef]
Parker, T.A., III. On the use of tape recorders in avifaunal surveys. Auk 1991, 108, 443–444.
O’Farrell, M.J.; Gannon, W.L. A comparison of acoustic versus capture techniques for the inventory of bats. J. Mamm. 1999, 80, 24–30. [CrossRef]
Majumder, A.; Qureshi, Q.; Sankar, K.; Kumar, A. Long-term monitoring of a Bengal tiger (Panthera tigris tigris) population in a human-dominated landscape of Central India. Eur. J. Wildl. Res. 2017, 63, 17. [CrossRef]
Messinger, M.; Asner, G.P.; Silman, M. Rapid assessments of amazon forest structure and biomass using small unmanned aerial systems. Remote Sens. 2016, 8, 615. [CrossRef]
Kellner, J.R.; Armston, J.; Birrer, M.; Cushman, K.C.; Duncanson, L.; Eck, C.; Falleger, C.; Imbach, B.; Král, K.; Krůček, M.; et al. New opportunities for forest remote sensing through ultra-high-density drone lidar. Surv. Geophys. 2019, 40, 959–977. [CrossRef]
Valiente-Banuet, A.; Aizen, M.A.; Alcántara, J.M.; Arroyo, J.; Cocucci, A.; Galetti, M.; García, M.B.; García, D.; Gómez, J.M.; Jordano, P.; et al. Beyond species loss: The extinction of ecological interactions in a changing world. Funct. Ecol. 2015, 29, 299–307. [CrossRef]
Lermyte, C.; Forget, P.-M. Rapid assessment of dispersal failure and seedling recruitment of large-seeded non-timber forest products trees in a tropical rainforest. Trop. Conserv. Sci. 2009, 2, 404–424. [CrossRef]
Hambuckers, J.; Dauvrin, A.; Trolliet, F.; Evrard, Q.; Forget, P.M.; Hambuckers, A. How can seed removal rates of zoochoric tree species be assessed quickly and accurately? For. Ecol. Manag. 2017, 403, 152–160. [CrossRef]
Boissier, O.; Feer, F.; Henry, P.-Y.; Forget, P.-M. Modifications of the rainforest frugivore community are associated with reduced seed removal at the community level. Ecol. Appl. 2020, 30, e02086. [CrossRef] [PubMed]
Albert, A.; Huynen, M.-C.; Savini, T.; Hambuckers, A. Influence of food resources on the ranging pattern of Northern pigtailed macaques (Macaca leonina). Int. J. Primatol. 2013, 34, 693–713. [CrossRef]
José-Domínguez, J.M.; Huynen, M.C.; García, C.J.; Albert-Daviaud, A.; Savini, T.; Asensio, N. Non-territorial Macaques Can Range Like Territorial Gibbons When Partially Provisioned With Food. Biotropica 2015, 47, 733–744. [CrossRef]
Gazagne, E.; José-Domínguez, J.M.; Huynen, M.C.; Hambuckers, A.; Poncin, P.; Savini, T.; Brotcorne, F. Northern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment. Am. J. Primatol. 2020, 82, e23117. [CrossRef]
Patil, G.P.; Brooks, R.P.; Myers, W.L.; Rapport, D.J.; Taillie, C. Ecosystem health and its measurement at landscape scale: Toward the next generation of quantitative assessments. Ecosyst. Health 2001, 7, 307–316. [CrossRef]
Culot, L.; Lazo, F.J.J.M.; Huynen, M.C.; Poncin, P.; Heymann, E.W. Seasonal variation in seed dispersal by tamarins alters seed rain in a secondary rain forest. Int. J. Primatol. 2010, 31, 553–569. [CrossRef]
Lengyel, S.; Gove, A.D.; Latimer, A.M.; Majer, J.D.; Dunn, R.R. Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: A global survey. Perspect. Plant Ecol. Evol. Syst. 2010, 12, 43–55. [CrossRef]
Aliyu, B.; Adamu, H.; Moltchanova, E.; Forget, P.-M.; Chapman, H. The interplay of habitat and seed type on scatterhoarding behavior in a fragmented afromontane forest landscape. Biotropica 2014, 46, 264–267. [CrossRef]
Keuroghlian, A.; Eaton, D.P. Removal of palm fruits and ecosystem engineering in palm stands by white-lipped peccaries (Tayassu pecari) and other frugivores in an isolated Atlantic Forest fragment. Biodivers. Conserv. 2009, 18, 1733–1750. [CrossRef]
Markl, J.S.; Schleuning, M.; Forget, P.M.; Jordano, P.; Lambert, J.E.; Traveset, A.; Wright, S.J.; Böhning-Gaese, K. Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conserv. Biol. 2012, 26, 1072–1081. [CrossRef]
Chen, Q.; Tomlinson, K.W.; Cao, L.; Wang, B. Effects of fragmentation on the seed predation and dispersal by rodents differ among species with different seed size. Integr. Zool. 2017, 12, 468–476. [CrossRef]
Wright, S.J.; Duber, H.C. Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm Attalea butyraceae, with implications for tropical tree diversity. Biotropica 2001, 33, 583–595. [CrossRef]
Herrerías-Diego, Y.; Quesada, M.; Stoner, K.E.; Lobo, J.A.; Hernández-Flores, Y.; Sanchez Montoya, G. Effect of forest fragmentation on fruit and seed predation of the tropical dry forest tree Ceiba aesculifolia. Biol. Conserv. 2008, 141, 241–248. [CrossRef]
Pessoa, M.; Hambuckers, A.; Benchimol, M.; Rocha-Santos, L.; Bomfim, J.A.; Faria, D.; Cazetta, E. Deforestation drives functional diversity and fruit quality changes in a tropical tree assemblage. Perspect. Plant Ecol. Evol. Syst. 2017, 28, 78–86. [CrossRef]
Prado, P.I.; Pinto, L.P.; Moura, R.T.; Carvalho, A.M.; Thomas, W.W.; Amorin, A.M.; Aguiar, C. Caracterizção dos registros de ocorrência de espécies de plantas e mamíferos no sul da Bahia, Brasil. In Corredor de biodiversidade da Mata Atlântica do sul da Bahia; Instituto de Estudos Sócio-Ambientais do Sul da Bahia e Conservation International do Brasil: Ilhéus, Bahia, Brazil, 2003; pp. 1–16.
Martini, A.M.Z.; Fiaschi, P.; Amorim, A.M.; Paixão, J.L.D. A hot-point within a hot-spot: A high diversity site in Brazil’s Atlantic Forest. Biodivers. Conserv. 2007, 16, 3111–3128. [CrossRef]
Canale, G.R.; Peres, C.A.; Guidorizzi, C.E.; Gatto, C.A.F.; Kierulff, M.C.M. Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLoS ONE 2012, 7, e41671. [CrossRef]
Cassano, C.R.; Barlow, J.; Pardini, R. Large mammals in an agroforestry mosaic in the Brazilian Atlantic Forest. Biotropica 2012, 44, 818–825. [CrossRef]
Flesher, K.M.; Laufer, J. Protecting wildlife in a heavily hunted biodiversity hotspot: A case study from the Atlantic Forest of Bahia, Brazil. Trop. Conserv. Sci. 2013, 6, 181–200. [CrossRef]
Beca, G.; Vancine, M.H.; Carvalho, C.S.; Pedrosa, F.; Alves, R.S.C.; Buscariol, D.; Peres, C.A.; Ribeiro, M.C.; Galetti, M. High mammal species turnover in forest patches immersed in biofuel plantations. Biol. Conserv. 2017, 210, 352–359. [CrossRef]
Rocha-Santos, L.; Benchimol, M.; Mayfield, M.M.; Faria, D.; Pessoa, M.S.; Talora, D.C.; Mariano-Neto, E.; Cazetta, E. Functional decay in tree community within tropical fragmented landscapes: Effects of landscape-scale forest cover. PLoS ONE 2017, 12, e0175545. [CrossRef]
Decaëns, T.; Martins, M.B.; Feijoo, A.; Oszwald, J.; Dolédec, S.; Mathieu, J.; Arnaud de Sartre, X.; Bonilla, D.; Brown, G.G.; Cuellar Criollo, Y.A.; et al. Biodiversity loss along a gradient of deforestation in Amazonian agricultural landscapes. Conserv. Biol. 2018, 32, 1380–1391. [CrossRef] [PubMed]
Macedo-Reis, L.E.; Quesada, M.; de Siqueira Neves, F. Forest cover drives insect guild diversity at different landscape scales in tropical dry forests. For. Ecol. Manag. 2019, 443, 36–42. [CrossRef]
McGarigal, K.; Cushman, S.A. Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecol. Appl. 2002, 12, 335–345. [CrossRef]
Rocha-Santos, L.; Pessoa, M.S.; Cassano, C.R.; Talora, D.C.; Orihuela, R.L.L.; Mariano-Neto, E.; Morante-Filho, J.C.; Faria, D.; Cazetta, E. The shrinkage of a forest: Landscape-scale deforestation leading to overall changes in local forest structure. Biol. Conserv. 2016, 196, 1–9. [CrossRef]
Pessoa, M.; Rocca, L.; Talora, D.; Faria, D.; Mariano-Neto, E.; Hambuckers, A.; Cazetta, E. Fruit biomass availability along a forest cover gradiant. Biotropica 2016, 49, 45–55. [CrossRef]
Rocha-Santos, L.; Talora, D.C. Recovery of atlantic rainforest areas altered by distinct land-use histories in northeastern Brazil. Trop. Conserv. Sci. 2012, 5, 475–494. [CrossRef]
Arruda, Y.M.B.C.; Ferraz, I.D.K. Inharé-da-folha-peluda Helicostylis tomenosa (Poep. & Endl.) Rusby. In Informativo Técnico. Rede de Sementes da @mazônia; Ferraz, I.D.K., Sidney, A.N., Ferreira, S.A.N., Camargo, J.L.C., Eds.; INPA: Manaus, Brazil, 2008; pp. 1–2.
de Souza Pessoa, M.; de Vleeschouwer, K.; Amorim, A.M.; Custódio Talora, D. Calendário Fenológico. Uma Ferramenta Para Auxiliar No Cultivo de Espécies Arbóreas Nativitas da Floresta Atläntica no Sul da Bahia; Edus-Editoria da UESC: Ilheus, Brazil, 2011.
Izawa, K. Foods and feeding behavior of wild black-capped capuchin (Cebus apella). Primates 1979, 20, 57–76. [CrossRef]
Catenacci, L.S.; De Vleeschouwer, K.M.; Nogueira-Filho, S.L.G. Seed dispersal by Golden-headed Lion Tamarins Leontopithecus chrysomelas in southern Bahian Atlantic Forest, Brazil. Biotropica 2009, 41, 744–750. [CrossRef]
Stevenson, P.R.; Link, A.; González-Caro, S.; Torres-Jiménez, M.F. Frugivory in canopy plants in a western Amazonian forest: Dispersal systems, phylogenetic ensembles and keystone plants. PLoS ONE 2015, 10, e0140751. [CrossRef]
Bello, C.; Galetti, M.; Montan, D.; Pizo, M.A.; Mariguela, T.C.; Culot, L.; Bufalo, F.; Labecca, F.; Pedrosa, F.; Constantini, R.; et al. Atlantic frugivory: A plant–frugivore interaction data set for the Atlantic Forest. Ecology 2017, 98, 1729. [CrossRef]
Jerozolimski, A.; Ribeiro, M.B.N.; Martins, M. Are tortoises important seed dispersers in Amazonian forests? Oecologia 2009, 161, 517–528. [CrossRef]
Salas, L.A.; Fuller, T.K. Diet of the lowland tapir (Tapirus terrestris L.) in the Tabaro River valley, southern Venezuela. Can. J. Zool. 1996, 74, 1444–1451. [CrossRef]
Prado, H.M. Feeding ecology of five Neotropical ungulates: A critical review. Oecologia Aust. 2013, 17, 459–473. [CrossRef]
Gayot, M.; Henry, O.; Dubost, G.; Sabatier, D. Comparative diet of the two forest cervids of the genus Mazama in French Guiana. J. Trop. Ecol. 2004, 20, 31–43. [CrossRef]
Wiesbauer, M.B.; Giehl, E.L.H.; Jarenkow, J.A. Padrões morfológicos de diásporos de árvores e arvoretas zoocóricas no Parque Estadual de Itapuã, RS, Brasil. Acta Bot. Brasilica 2008, 22, 425–435. [CrossRef]
Orwa, C.; Mutua, A.; Kindt, R.; Jamnadass, R.; Simons, A. Agroforestree Database: A Tree Reference and Selection Guide Version 4.0; World Agroforestry Centre: Nairobi, Kenya, 2009.
Colmanetti, M.A.A.; Barbosa, L.M.; Shirasuna, R.T.; Couto, H.T.Z.D. Phytosociology and structural characterization of woody regeneration from a reforestation with native species of Southeastern Brazil. Rev. Árvore 2016, 40, 209–218. [CrossRef]
Ragusa-Netto, J.; Fecchio, A. Plant food resources and the diet of a parrot community in a gallery forest of the Southern Pantanal (Brazil). Braz. J. Biol. 2006, 66, 1021–1032. [CrossRef] [PubMed]
Carlo, T.A.; Collazo, J.A.; Groom, M.J. Influences of fruit diversity and abundance on bird use of two shaded coffee plantations. Biotropica 2004, 36, 602–614. [CrossRef]
Bevilacqua Marcuzzo, S.; Viera, M. Ecological restoration in Conservation units. In Biodiversity in Ecosystems-Linking Structure and Function; Lo, Y.-H., Blanco, J.A., Roy, S., Eds.; IntechOpen Limited: London, UK, 2015; pp. 493–509.
Galetti, M.; Keuroghlian, A.; Hanada, L.; Morato, M.I. Frugivory and seed dispersal by the lowland tapir (Tapirus terrestris) in Southeast Brazil. Biotropica 2001, 33, 723–726. [CrossRef]
Beck, H. Seed predation and dispersal by peccaries throughout the Neotropics and its consequences: A review and synthesis. In Seed Fate: Predation, Dispersal and Seedling Establishment; Forget, P.M., Hulme, P., Lambert, J.E., Vander Wall, S.B., Eds.; CABI Publishing: Wallinford, UK, 2004; pp. 77–115.
Rondeux, J. La Mesure des Arbres et des Peuplements Forestiers; Presses Agronomiques de Gembloux: Gembloux, Belgium, 1993.
Kalogirou, S. Package ‘lctools’. Local Correlation, Spatial Inequalities and Other Tools. Available online: https://CRAN.R-project.org/package=lctools (accessed on 15 September 2020).
Bivand, R.; Altman, M.; Anselin, L.; Assunção, R.; Berke, O.; Bernat, A.; Blanchet, G. Package ‘spdep’. Available online: https://github.com/r-spatial/spdep/(accessed on 15 September 2020).
Dormann, C.F.; McPherson, J.M.; Araújo, M.B.; Bivand, R.; Bolliger, J.; Carl, G.; Davies, R.G.; Hirzel, A.; Jetz, W.; Kissling, W.D.; et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: A review. Ecography 2007, 30, 609–628. [CrossRef]
McLeod, A.I.; Xu, C. Best subset GLM and regression utilities. Available online: https://CRAN.R-project.org/package=bestglm (accessed on 16 June 2020).
Zhang, D. R-squared and related measures. Available online: https://CRAN.R-project.org/package=rsq (accessed on 19 October 2020).
Boyle, S.A.; Smith, A.T. Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biol. Conserv. 2010, 143, 1134–1143. [CrossRef]
Raboy, B.E.; Christman, M.C.; Dietz, J.M. The use of degraded and shade cocoa forests by Endangered golden-headed lion tamarins Leontopithecus chrysomelas. Oryx 2004, 38, 75–83. [CrossRef]
Tisovec, K.C.; Cassano, C.R.; Boubli, J.P.; Pardini, R. Mixed-species groups of marmosets and tamarins across a gradient of agroforestry intensification. Biotropica 2014, 46, 248–255. [CrossRef]
De Vleeschouwer, K.M.; Oliveira, L.C. Report on the presence of a group of golden-headed lion tamarins (Leontopithecus chrysomelas), an endangered primate species in a rubber plantation in southern Bahia, Brazil. Primate Biol. 2017, 4, 61–67. [CrossRef]
Galetti, M.; Donatti, C.I.; Pires, A.S.; Guimarães Jr, P.R.; Jordano, P. Seed survival and dispersal of an endemic Atlantic forest palm: The combined effects of defaunation and forest fragmentation. Bot. J. Linn. Soc. 2006, 151, 141–149. [CrossRef]
Soares, L.A.S.S.; Faria, D.; Vélez-Garcia, F.; Vieira, E.M.; Talora, D.C.; Cazetta, E. Implications of habitat loss on seed predation and early recruitment of a keystone palm in anthropogenic landscapes in the Brazilian Atlantic rainforest. PLoS ONE 2015, 10, e0133540. [CrossRef]
Pérez-Méndez, N.; Jordano, P.; García, C.; Valido, A. The signatures of Anthropocene defaunation: Cascading effects of the seed dispersal collapse. Sci. Rep. 2016, 6, 24820. [CrossRef] [PubMed]
Barcellos de Souza, J.B.; Nóbrega Alves, R.R. Hunting and wildlife use in an Atlantic Forest remnant of northeastern Brazil. Trop. Conserv. Sci. 2014, 7, 145–160. [CrossRef]
Ordano, M.; Blendinger, P.G.; Lomáscolo, S.B.; Chacoff, N.P.; Sánchez, M.S.; Núñez Montellano, M.G.; Jiménez, J.; Ruggera, R.A.; Valoy, M. The role of trait combination in the conspicuousness of fruit display among bird-dispersed plants. Funct. Ecol. 2017, 31, 1718–1727. [CrossRef]
Palacio, F.X.; Ordano, M. The strength and drivers of bird-mediated selection on fruit crop size: A meta-analysis. Front. Ecol. Evol. 2018, 6, 18. [CrossRef]
Briani, D.C.; Guimarães, P.R., Jr. Seed predation and fruit damage of Solanum lycocarpum (Solanaceae) by rodents in the cerrado of central Brazil. Acta. Oecol. 2007, 31, 8–12. [CrossRef]
Trolliet, F.; Forget, P.-M.; Huynen, M.-C.; Hambuckers, A. Forest cover, hunting pressure, and fruit availability influence seed dispersal in a forest-savanna mosaic in the Congo Basin. Biotropica 2017, 49, 337–345. [CrossRef]
