Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-18T22:24:40.416Z Has data issue: false hasContentIssue false
  • English
  • Français

How complementary are large frugivores for tree seedling recruitment? A case study in the Congo Basin

Published online by Cambridge University Press:  10 July 2019

Franck Trolliet Open the ORCID record for Franck Trolliet [Opens in a new window] ,
David Bauman Open the ORCID record for David Bauman [Opens in a new window] ,
Pierre-Michel Forget ,
Jean-Louis Doucet ,
Jean-François Gillet  and
Alain Hambuckers
Franck Trolliet*
Affiliation:
Unité de Biologie du Comportement, UR SPHERES, Université de Liège, Quai van Beneden 22, 4020, Liège, Belgium
David Bauman
Affiliation:
Laboratoire d’Ecologie Végétale et Biogéochimie, Université Libre de Bruxelles, 50 av. F. D. Roosevelt, CP 244, 1050 Brussels, Belgium Environmental Change Institute, School of Geography and the Environment, University of Oxford, Oxford OX1 3QY, UK
Pierre-Michel Forget
Affiliation:
UMR 7179 MECADEV CNRS-MNHN, Muséum National d’Histoire Naturelle, Département Adaptations du vivant, Brunoy, France
Jean-Louis Doucet
Affiliation:
TERRA Research Center, Central African Forests, Gembloux Agro-Bio Tech, Université de Liège, Belgium
Jean-François Gillet
Affiliation:
TERRA Research Center, Central African Forests, Gembloux Agro-Bio Tech, Université de Liège, Belgium Nature Forest Environment [freelance in tropical forestry], Belgium
Alain Hambuckers
Affiliation:
Unité de Biologie du Comportement, UR SPHERES, Université de Liège, Quai van Beneden 22, 4020, Liège, Belgium
*
*Author for correspondence: Franck Trolliet, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Large frugivores provide critical seed dispersal services for many plant species and their extirpation from forested ecosystems can cause compositional shifts in regenerating plant cohorts. Yet, we still poorly understand whether large seed-dispersers have complementary or redundant roles for forest regeneration. Here, to assess the functional complementarity of large-bodied frugivores in forest regeneration, we quantified the effects of varying abundance of hornbills, primates and the forest elephant on the density, species richness and the mean weighted seed length of animal-dispersed tree species among seedlings in five sites in a forest–savanna mosaic in D. R. Congo, while accounting for percentage forest cover and the local presence of fruiting trees. We found that the abundance of primates was positively associated with species richness of seedlings, while percentage forest cover was negatively associated (R2 = 0.19). The abundance of hornbills, the presence of elephants and percentage forest cover were positively associated with mean seed length of the regenerating cohort (R2 = 0.13). Spatially explicit analysis indicated that some additional processes have an important influence on these response indices. Primates would seem to have a preponderant role for maintaining relatively high species richness, while hornbills and elephant would seem to be predominantly responsible for the recruitment of large-seeded trees. Our results could indicate that these taxa of frugivores play complementary functional roles for forest regeneration. This suggests that the extirpation of one or more of these dispersers would likely not be functionally compensated for by the remaining taxa, hence possibly cascading into compositional shifts.

Keywords

Complementing functionsCongo BasindefaunationMoran’s eigenvector maps (MEM)regenerationseed dispersalspatial autocorrelationtropical forestvariation partitioning
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 5 , September 2019 , pp. 223 - 236
Copyright
© Cambridge University Press 2019 

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.)

References

Literature cited

Abernethy, KA, Coad, L, Taylor, G, Lee, ME and Maisels, F (2013) Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century. Philosophical Transactions of the Royal Society of Biological Sciences 368, 20120303.CrossRefGoogle ScholarPubMed
Alcomb, SORB (2003) Bridging the gap: influence of seed deposition on seedling recruitment in a primate– tree interaction. Ecological Monographs 73, 625–642.CrossRefGoogle Scholar
Anderson, MJ and Legendre, P (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. Journal of Statistical Computation and Simulation 62, 271–303.CrossRefGoogle Scholar
Arroyo-Rodríguez, V, Rös, M, Escobar, F, Melo, FPL, Santos, BA, Tabarelli, M and Chazdon, R (2013) Plant β-diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses. Journal of Ecology 101, 1449–1458.CrossRefGoogle Scholar
Bauman, D, Drouet, T, Dray, S and Vleminckx, J (2018 a) Disentangling good from bad practices in the selection of spatial or phylogenetic eigenvectors. Ecography 41, 1638–1649.CrossRefGoogle Scholar
Bauman, D, Drouet, T, Fortin, M-J and Dray, S (2018 b) Optimizing the choice of a spatial weighting matrix in eigenvector-based methods. Ecology 99, 2159–2166.CrossRefGoogle ScholarPubMed
Bauman, D, Vleminckx, J, Hardy, OJ and Drouet, T (2019) Testing and interpreting the shared space-environment fraction in variation partitioning analyses of ecological data. Oikos 128, 274–285.CrossRefGoogle Scholar
Beaune, D, Fruth, B and Bollache, L (2013) Doom of the elephant-dependent trees in a Congo tropical forest. Forest Ecology and Management 295, 109–117.CrossRefGoogle Scholar
Bell, G, Lechowicz, MJ and Waterway, MJ (2006) The comparative evidence relating to functional and neutral interpretations of biological communities. Ecology 87, 1378–1386.CrossRefGoogle ScholarPubMed
Bennett, EL, Blencowe, E, Brandon, K, Brown, D, Burn, RW, Cowlishaw, G, Davies, G, Dublin, H, Fa, JE, Milner-Gulland, EJ, Robinson, JG, Rowcliffe, JM, Underwood, FM and Wilkie, DS (2007) Hunting for consensus: reconciling bushmeat harvest, conservation, and development policy in west and central Africa. Conservation Biology 21, 884–887.CrossRefGoogle ScholarPubMed
Blake, S, Deem, SL, Mossimbo, E, Maisels, F and Walsh, P (2009) Forest elephants: tree planters of the Congo. Biotropica 41, 459–468.CrossRefGoogle Scholar
Blanchet, FG, Legendre, P and Borcard, D (2008) Forward selection of explanatory variables. Ecology 89, 2623–2632.CrossRefGoogle ScholarPubMed
Borcard, D and Legendre, P (1994) Environmental control and spatial structure in ecological communities: an example using oribatid mites (Acari, Oribatei). Environmental and Ecological Statistics 1, 37–61.CrossRefGoogle Scholar
Campos-Arceiz, A and Blake, S (2011) Megagardeners of the forest – the role of elephants in seed dispersal. Acta Oecologica 37, 542–553.CrossRefGoogle Scholar
Carrière, SM, Letourmy, P and McKey, DB (2002) Effects of remnant trees in fallows on diversity and structure of forest regrowth in a slash-and-burn agricultural system in southern Cameroon. Journal of Tropical Ecology 18, 375–396.CrossRefGoogle Scholar
Chaves, OM, Arroyo-Rodríguez, V, Martínez-Ramos, M and Stoner, KE (2015) Primate extirpation from rainforest fragments does not appear to influence seedling recruitment. American Journal of Primatology 77, 468–478.CrossRefGoogle Scholar
Clark, CJ, Poulsen, JR and Parker, VT (2001) The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest. Biotropica 33, 606–620.CrossRefGoogle Scholar
Clark, CJ, Poulsen, JR, Connor, EF and Parker, VT (2004) Fruiting trees as dispersal foci in a semi-deciduous tropical forest. Oecologia 139, 66–75.CrossRefGoogle Scholar
Clark, CJ, Poulsen, JR and Levey, DJ (2012) Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 93, 554–564.CrossRefGoogle ScholarPubMed
Cottee-Jones, HEW, Bajpai, O, Chaudhary, LB and Whittaker, RJ (2016) The importance of Ficus (Moraceae) trees for tropical forest restoration. Biotropica 48, 413–419.CrossRefGoogle Scholar
Diniz-Filho, JAF and Bini, LM (2005) Modelling geographical patterns in species richness using eigenvector-based spatial filters. Global Ecology and Biogeography 14, 177–185.CrossRefGoogle Scholar
Dormann, CF, Elith, J, Bacher, S, Buchmann, C, Carl, G, Carré, G, Marquéz, JRG, Gruber, B, Lafourcade, B, Leitão, PJ, Münkemüller, T, McClean, C, Osborne, PE, Reineking, B, Schröder, B, Skidmore, AK, Zurell, D and Lautenbach, S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46.CrossRefGoogle Scholar
Dray, S, Legendre, P and Peres-Neto, PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling 196, 483–493.CrossRefGoogle Scholar
Dray, S, Pélissier, R, Couteron, P, Fortin, M-J, Legendre, P, Peres-Neto, PR, Bellier, E, Bivand, R, Blanchet, FG, De Cáceres, M, Dufour, AB, Heegaard, E, Jombart, T, Munoz, F, Oksanen, J, Thioulouse, J and Wagner, HH (2012) Community ecology in the age of multivariate multiscale spatial analysis. Ecological Monographs 82, 257–275.CrossRefGoogle Scholar
Effiom, EO, Nuñez-Iturri, G, Smith, HG, Ottosson, U and Olsson, O (2013) Bushmeat hunting changes regeneration of African rainforests. Proceedings of the Royal Society of Biological Sciences 280, 20130246.CrossRefGoogle ScholarPubMed
Effiom, EO, Birkhofer, K, Smith, HG and Olsson, O (2014) Changes of community composition at multiple trophic levels due to hunting in Nigerian tropical forests. Ecography 37, 367–377.CrossRefGoogle Scholar
Fa, JE, Ryan, S and Bell, D (2005) Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in afrotropical forests. Biological Conservation 121, 167–176.CrossRefGoogle Scholar
Fleury, M, Silla, F, Rodrigues, RR, Hilton, TZ and Galetti, M (2014) Seedling fate across different habitats: the effects of herbivory and soil fertility. Basic and Applied Ecology 16, 141–151.CrossRefGoogle Scholar
Forget, P-M, Dennis, A, Mazer, S, Jansen, PA, Kitamura, S, Lambert, JE and Westcott, DA (2007) Seed allometry and disperser assemblages in tropical rain forests: a comparison of four floras on different continents. In Dennis, AJ, Schupp, EW, Green, RA and Westcott, DA (eds), Seed Dispersal: Theory and its Application in a Changing World . Wallingford: CAB International, pp. 5–36.CrossRefGoogle Scholar
Fortin, M-J and Dale, MRT (2014) Spatial Analysis: A Guide for Ecologists . Cambridge: Cambridge University Press.Google Scholar
Foster, SA (1986) On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis. Botanical Review 52, 260–299.CrossRefGoogle Scholar
Gautier-Hion, A, Duplantier, J, Quris, R, Feer, F, Sourd, C, Decoux, J-P, Dubost, G, Emmons, L, Erard, C, Heckestweiler, P, Moungazi, A, Roussilhon, C and Thiollay, J-M (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65, 324–337.CrossRefGoogle Scholar
Hall, JS, White, LJT, Inogwabini, BI, Omari, I, Morland, HS, Williamson, EA, Saltonstall, K, Walsh, P, Sikubwabo, C, Bonny, D, Kiswele, KP, Vedder, A and Freeman, K (1998) Survey of Grauer’s gorillas (Gorilla gorilla graueri) and eastern chimpanzees (Pan troglodytes schweinfurthi) in the Kahuzi-Biega National Park lowland sector and adjacent forest in eastern Democratic Republic of Congo. International Journal of Primatology 19, 207–235.CrossRefGoogle Scholar
Harrison, R, Tan, S, Plotkin, J, Slik, JWF, Detto, M, Brenes, T, Itoh, A and Davies, S (2013) Consequences of defaunation for a tropical tree community. Ecology Letters 16, 687–694.CrossRefGoogle ScholarPubMed
Herrera, CM, Jordano, P, Lopez-Soria, L and Amat, AJ (1994) Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecological Monographs 64, 315–344.CrossRefGoogle Scholar
Hubbell, SP (2001) A Unified Theory of Biodiversity and Biogeography . Princeton, NJ: Princeton University Press.Google Scholar
Hubbell, SP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87, 1387–1398.CrossRefGoogle ScholarPubMed
Inogwabini, B, Matungila, B, Mbende, L, Abokome, M and Wa Tshimanga, T (2007) Great apes in the Lake Tumba landscape, Democratic Republic of Congo: newly described populations. Oryx 41, 1–7.CrossRefGoogle Scholar
Inogwabini, B, Mbende, L and Mbenzo, A (2011) The relic population of forest elephants near Lake Tumba, Democratic Republic of Congo: abundance, dung lifespan, food items and movements. Pachyderm 49, 40–47.Google Scholar
Legendre, P and Legendre, L (2012) Numerical Ecology , Third edition. Amsterdam: Elsevier.Google Scholar
Lugon, AP, Boutefeu, M, Bovy, E, Vaz-De-Mello, FZ, Huynen, M-C, Galetti, M and Culot, L (2017) Persistence of the effect of frugivore identity on post-dispersal seed fate: consequences for the assessment of functional redundancy. Biotropica 49, 293–302.CrossRefGoogle Scholar
Mangan, SA, Schnitzer, SA, Herre, EA, Mack, KML, Valencia, MC, Sanchez, EI and Bever, JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755.CrossRefGoogle Scholar
Markl, J, Schleuning, M, Forget, P-M, Jordano, P, Lambert, JE, Traveset, A, Wright, SJ and Böhning-Gaese, K (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conservation Biology 26, 1072–1081.CrossRefGoogle ScholarPubMed
Mathot, L and Doucet, J-L (2006) Méthode d’inventaire faunique pour le zonage des concessions en forêt tropicale. Bois et Forêt des Tropiques 287, 50–70.Google Scholar
McConkey, KR and Brockelman, W (2016) Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology 92, 1492–1502.CrossRefGoogle Scholar
McConkey, KR and O’Farrill, G (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation 201, 38–49.CrossRefGoogle Scholar
McConkey, KR, Brockelman, W, Saralamba, C and Nathalang, A (2015) Effectiveness of primate seed dispersers for an “oversized” fruit, Garcinia benthamii . Ecology 96, 2737–2747.CrossRefGoogle ScholarPubMed
McIntire, EJB and Fajardo, A (2009) Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90, 46–56.CrossRefGoogle ScholarPubMed
Muledi, JI, Bauman, D, Drouet, T, Vleminckx, J, Jacobs, A, Lejoly, J, Meerts, P and Shutcha, MN (2016) Fine-scale habitats influence tree species assemblage in a miombo forest. Journal of Plant Ecology 10, 958–969.Google Scholar
Nicotra, AB, Chazdon, RL and Iriarte, SVB (1999) Spatial heterogeneity of light and woodly seedling regeneration in tropical wet forests. Ecology 80, 1908–1926.CrossRefGoogle Scholar
Nuñez-Iturri, G and Howe, H (2007) Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in Western Amazonia. Biotropica 39, 348–354.CrossRefGoogle Scholar
Peres, CA and Palacios, E (2007) Basin wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal mediated seed dispersal. Biotropica 39, 304–315.CrossRefGoogle Scholar
Peres-Neto, PR and Legendre, P (2010) Estimating and controlling for spatial structure in the study of ecological communities. Global Ecology and Biogeography 19, 174–184.CrossRefGoogle Scholar
Peres-Neto, PR, Legendre, P, Dray, S and Borcard, D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 2614–2625.CrossRefGoogle ScholarPubMed
Poulsen, JR, Clark, CJ and Smith, TB (2001) Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology 17, 787–808.CrossRefGoogle Scholar
Poulsen, JR, Clark, CJ, Connor, EF and Smith, TB (2002) Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83, 228–240.CrossRefGoogle Scholar
Poulsen, JR, Koerner, SE, Moore, S, Medjibe, VP, Blake, S, Clark, CJ, Akou, ME, Fay, M, Meier, A, Okouyi, J, Rosin, C and White, LJT (2017) Poaching empties critical Central African wilderness of forest elephants. Current Biology 27, R134–R135.CrossRefGoogle ScholarPubMed
Poulsen, JR, Rosin, C, Meier, A, Mills, E, Nuñez, CL, Koerner, SE, Blanchard, E, Callejas, J, Moore, S and Sowers, M (2018) Ecological consequences of forest elephant declines for Afrotropical forests. Conservation Biology 32, 559–567.CrossRefGoogle ScholarPubMed
Ripple, WJ, Abernethy, KA, Betts, MG, Chapron, G, Dirzo, R, Galetti, M, Levi, T, Lindsey, PA, Macdonald, DW, Machovina, B, Newsome, TM, Peres, CA, Wallach, AD, Wolf, C and Young, H (2016) Bushmeat hunting and extinction risk to the world’s mammals. Royal Society Open Science 3, 160498.CrossRefGoogle ScholarPubMed
Rother, DC, Pizo, MA and Jordano, P (2016) Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos 125, 336–342.CrossRefGoogle Scholar
Schleuning, M, Fru, J, Klein, A, Abrahamczyk, S, Albrecht, M, Andersson, GKS, Bazarian, S, Bo, K, Dalsgaard, B, Dehling, DM and Gotlieb, A (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology 22, 1925–1931.CrossRefGoogle ScholarPubMed
Sekar, N, Chia-Lo, L and Sukumar, R (2017) Functional nonredundancy of elephants in a disturbed tropical forest. Conservation Biology 31, 1152–1162.CrossRefGoogle Scholar
Slocum, MG (2012) How tree species differ as recruitment foci in a tropical pasture. Ecology 82, 2547–2559.CrossRefGoogle Scholar
Terborgh, JW (2013) Using Janzen–Connell to predict the consequences of defaunation and other disturbances of tropical forests. Biological Conservation 163, 7–12.CrossRefGoogle Scholar
Terborgh, JW, Nuñez-Iturri, G and Pitman, N (2008) Tree recruitment in an empty forest. Ecology 89, 1757–1768.CrossRefGoogle Scholar
The Angiosperm Phylogeny Group (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APGIII. Botanical Journal of the Linnean Society 161, 105–121.CrossRefGoogle Scholar
Trail, PW (2007) African hornbills: keystone species threatened by habitat loss, hunting and international trade. Ostrich – Journal of African Ornithology 78, 609–613.CrossRefGoogle Scholar
Trolliet, F, Serckx, A, Forget, P-M, Beudels-Jamar, RC, Huynen, M-C and Hambuckers, A (2016) Ecosystem services provided by a large endangered primate in a forest-savanna mosaic landscape. Biological Conservation 203, 55–66.CrossRefGoogle Scholar
Trolliet, F, Forget, P-M, Huynen, M-C and Hambuckers, A (2017) Forest cover, hunting pressure, and fruit availability influence seed dispersal in a forest-savanna mosaic of the Congo Basin. Biotropica 49, 337–345.CrossRefGoogle Scholar
Vanthomme, H, Bellé, B and Forget, P-M (2010) Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42, 672–679.CrossRefGoogle Scholar
Vleminckx, J, Doucet, J-L, Morin-Rivat, J, Biwolé, AB, Bauman, D, Hardy, OJ, Fayolle, A, Gillet, J-F, Daïnou, K, Gorel, A and Drouet, T (2016) The influence of spatially structured soil properties on tree community assemblages at a landscape scale in the tropical forests of southern Cameroon. Journal of Ecology 105, 354–366.CrossRefGoogle Scholar
Wagner, HH and Dray, S (2015) Generating spatially constrained null models for irregularly spaced data using Moran spectral randomization methods. Methods in Ecology and Evolution 6, 1169–1178.CrossRefGoogle Scholar
Walsh, PD and White, LJT (1999) What it will take to monitor forest elephant populations. Conservation Biology 13, 1194–1202.CrossRefGoogle Scholar
Wang, BC andSmith, TB (2002) Closing the seed dispersal loop. Trends in Ecology and Evolution 17, 379–385.CrossRefGoogle Scholar
Whytock, R, Buij, R, Virani, M and Morgan, B (2016) Do large birds experience previously undetected levels of hunting pressure in the forests of Central and West Africa? Oryx 50, 76–83.CrossRefGoogle Scholar
Wright, SJ, Hernandéz, A and Condit, RR (2007) The bushmeat harvest alters seedling banks by favoring lianas, large seeds, and seeds dispersed by bats, birds, and wind. Biotropica 39, 363–371.CrossRefGoogle Scholar