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

Complementing functions; Congo Basin; defaunation; Moran's eigenvector maps (MEM); regeneration; seed dispersal; spatial autocorrelation; tropical forest; variation partitioning

Abstract :

[en] 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 (R 2 = 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 (R 2 = 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. © Cambridge University Press 2019.

Disciplines :

Environmental sciences & ecology

Author, co-author :

Trolliet, Franck ; Unité de Biologie du Comportement, UR SPHERES, Université de Liège, Quai van Beneden 22, Liège, 4020, Belgium

Bauman, D.; Laboratoire d'Ecologie Végétale et Biogéochimie, Université Libre de Bruxelles, 50 av. F. D. Roosevelt, CP 244, Brussels, 1050, Belgium

Forget, P.-M.; UMR 7179 MECADEV CNRS-MNHN, Muséum National d'Histoire Naturelle, Département Adaptations du Vivant, Brunoy, France

Doucet, Jean-Louis ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales

Gillet, J.-F.; Nature Forest Environment (Freelance in Tropical Forestry), Belgium

Hambuckers, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale

Language :

English

Title :

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

Publication date :

2019

Journal title :

Journal of Tropical Ecology

Volume :

in press

Peer reviewed :

Peer reviewed

Additional URL :

https://www.scopus.com/inward/record.uri?eid=2-s2.0-85068847396&doi=10.1017%2fS026646741900018X&partnerID=40&md5=6da8c1eb44547a5e2df502e3716e7cd0

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture

Available on ORBi :

since 26 August 2019

Statistics

Number of views

84 (7 by ULiège)

Number of downloads

4 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

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.
Alcomb SORB (2003) Bridging the gap: Influence of seed deposition on seedling recruitment in a primate-tree interaction. Ecological Monographs 73, 625-642.
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.
Arroyo-Rodríguez V, Rös M, Escobar F, Melo FPL, Santos BA, Tabarelli M and Chazdon R (2013) Plant -diversity in fragmented rain forests: Testing floristic homogenization and differentiation hypotheses. Journal of Ecology 101, 1449-1458.
Bauman D, Drouet T, Dray S and Vleminckx J (2018a) Disentangling good from bad practices in the selection of spatial or phylogenetic eigenvectors. Ecography 41, 1638-1649.
Bauman D, Drouet T, Fortin M-J and Dray S (2018b) Optimizing the choice of a spatial weighting matrix in eigenvector-based methods. Ecology 99, 2159-2166.
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.
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.
Bell G, Lechowicz MJ and Waterway MJ (2006) The comparative evidence relating to functional and neutral interpretations of biological communities. Ecology 87, 1378-1386.
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.
Blake S, Deem SL, Mossimbo E, Maisels F and Walsh P (2009) Forest elephants: Tree planters of the Congo. Biotropica 41, 459-468.
Blanchet FG, Legendre P and Borcard D (2008) Forward selection of explanatory variables. Ecology 89, 2623-2632.
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.
Campos-Arceiz A and Blake S (2011) Megagardeners of the forest-the role of elephants in seed dispersal. Acta Oecologica 37, 542-553.
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.
Chaves OM, Arroyo-Rodríguez V, Martínez-Ramos Mand Stoner KE (2015) Primate extirpation from rainforest fragments does not appear to influence seedling recruitment. American Journal of Primatology 77, 468-478.
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.
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.
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.
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.
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.
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitaõ 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.
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.
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.
Effiom EO, Nunez-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.
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.
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.
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.
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.
Fortin M-J and Dale MRT (2014) Spatial Analysis: A Guide for Ecologists. Cambridge: Cambridge University Press.
Foster SA (1986) On the adaptive value of large seeds for tropical moist forest trees: A review and synthesis. Botanical Review 52, 260-299.
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.
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.
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.
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.
Hubbell SP (2001) A Unified Theory of Biodiversity and Biogeography. Princeton, NJ: Princeton University Press.
Hubbell SP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87, 1387-1398.
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.
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.
Legendre P and Legendre L (2012) Numerical Ecology, Third edition. Amsterdam: Elsevier.
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.
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.
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.
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.
McConkey KR and Brockelman W (2016) Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology 92, 1492-1502.
McConkey KR and O'Farrill G (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation 201, 38-49.
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.
McIntire EJB and Fajardo A (2009) Beyond description: The active and effective way to infer processes from spatial patterns. Ecology 90, 46-56.
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.
Nicotra AB, Chazdon RL and Iriarte SVB (1999) Spatial heterogeneity of light andwoodly seedling regeneration in tropicalwet forests. Ecology 80, 1908-1926.
Nunez-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.
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.
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.
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.
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.
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.
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.
Poulsen JR, Rosin C, Meier A, Mills E, Nunez 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.
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.
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.
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.
Sekar N, Chia-Lo L and Sukumar R (2017) Functional nonredundancy of elephants in a disturbed tropical forest. Conservation Biology 31, 1152-1162.
Slocum MG(2012) How tree species differ as recruitment foci in a tropical pasture. Ecology 82, 2547-2559.
Terborgh JW (2013) Using Janzen-Connell to predict the consequences of defaunation and other disturbances of tropical forests. Biological Conservation 163, 7-12.
Terborgh JW, Nunez-Iturri G and Pitman N (2008) Tree recruitment in an empty forest. Ecology 89, 1757-1768.
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.
Trail PW (2007) African hornbills: Keystone species threatened by habitat loss, hunting and international trade. Ostrich-Journal of African Ornithology 78, 609-613.
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.
Trolliet F, Forget P-M, Huynen M-C and Hambuckers A (2017) Forest cover, hunting pressure, and fruit availability influence seed dispersal in a forestsavanna mosaic of the Congo Basin. Biotropica 49, 337-345.
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.
Vleminckx J, Doucet J-L, Morin-Rivat J, Biwolé AB, Bauman D, Hardy OJ, Fayolle A, Gillet J-F, Daïnou K, Gorel Aand 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.
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.
Walsh PD and White LJT (1999) What it will take to monitor forest elephant populations. Conservation Biology 13, 1194-1202.
Wang BC and Smith TB (2002) Closing the seed dispersal loop. Trends in Ecology and Evolution 17, 379-385.
Whytock R, Buij R, Virani Mand 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.
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.