[en] Animal-mediated seed dispersal is recognized to influence the spatial organization of plant communities but little is known about how frugivores cause such patterns. Here, we explored the role of hornbills and primates in generating recruitment foci under two zoochoric trees, namely Staudtia kamerunensis (Myristicaceae) and Dialium spp. (Fabaceae - Caesalpiniodea) in a forest-savanna mosaic landscape in D.R. Congo. We also examined the influence of the availability of fruits in the neighborhood and the amount of forest cover in the landscape on such clumping patterns. The density and species richness of hornbill-dispersed and the density of primate-dispersed seedlings were significantly higher under Staudtia kamerunensis trees than at control locations. However, we did not find such patterns under Dialium spp. trees compared to control locations except for the density of hornbill-dispersed seedlings which was lower at control locations. Also, we found that an increasing amount of forest cover in the landscape was associated with an increase in the density of hornbill-dispersed seedlings, although the tendency was weak (R2 = 0.065). We concluded that S. kamerunensis acts as a recruitment foci and plays a structuring role in Afrotropical forests. Hornbills were probably the main frugivore taxon responsible for the clumping under that tree and appear as a key ecological component in fragmented and disturbed landscapes where the diversity of large frugivores such as primates is reduced. Our findings improve our understanding of the causal mechanisms responsible for the spatial organization of tropical forests.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Trolliet, Franck ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Modélisation du climat et des cycles biogéochimiques
Forget, Pierre-Michel
Doucet, Jean-Louis ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales
Gillet, Jean-François
Hambuckers, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Language :
English
Title :
Frugivorous birds influence the spatial organization of tropical forests through the generation of seedling recruitment foci under zoochoric trees
Ahumada, J.A., Silva, C.E.F., Gajapersad, K., Hallam, C., Hurtado, J., Martin, E., Mcwilliam, A., Mugerwa, B., Brien, T.O., Rovero, F., Sheil, D., Spironello, W.R., Winarni, N., Andelman, S.J., Community structure and diversity of tropical forest mammals: data from a global camera trap network. Philos. Trans. R. Soc. Biol. Sci. 366 (2011), 2703–2711, 10.1098/rstb.2011.0115.
Albrecht, J., Neuschulz, E.L., Farwig, N., Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation. Basic Appl. Ecol. 13 (2012), 347–354, 10.1016/j.baae.2012.06.005.
Alcomb, S.O.R.B., Bridging the gap: influence of seed deposition on seedling recruitment in a primate – tree interaction. Ecol. Monogr. 73 (2003), 625–642.
Arruda, M.S.P., De Araújo, M.Q., Lôbo, L.T., De Souza Filho, A.P., Alves, S.M., Santos, L.D.S., Müller, A.H., Arruda, A.C., Guilhon, G.M.S.P., Potential allelochemicals isolated from Pueraria phaseoloides. Allelopath. J. 15 (2005), 211–220.
Atuo, F.A., Connell, T.J.O., Abanyam, P.U., An assessment of socio-economic drivers of avian body parts trade in West African rainforests. Biol. Conserv. 191 (2015), 614–622, 10.1016/j.biocon.2015.08.013.
Bastin, J.-F., Barbier, N., Réjou-Méchain, M., Fayolle, A., Gourlet-Fleury, S., Maniatis, D., de Haulleville, T., Baya, F., Beeckman, H., Beina, D., Couteron, P., Chuyong, G., Dauby, G., Doucet, J.-L., Droissart, V., Dufrêne, M., Ewango, C., Gillet, J.-F., Gonmadje, C.H., Hart, T., Kavali, T., Kenfack, D., Libalah, M., Malhi, Y., Makana, J.-R., Pélissier, R., Ploton, P., Serckx, A., Sonké B., Stevart, T., Thomas, D.W., De Cannière, C., Bogaert, J., Seeing Central African forests through their largest trees. Sci. Rep. 5 (2015), 1–8, 10.1038/srep13156.
Beaune, D., Bretagnolle, F., Bollache, L., Hohmann, G., Surbeck, M., Bourson, C., Fruth, B., The Bonobo–Dialium positive interactions: seed dispersal mutualism. Am. J. Primatol. 10 (2013), 1–10, 10.1002/ajp.22121.
Berens, D.G., Farwig, N., Schaab, G., Böhning-Gaese, K., Exotic guavas are foci of forest regeneration in Kenyan farmland. Biotropica 40 (2008), 104–112, 10.1111/j.1744-7429.2007.00338.x.
Blendinger, P., Villegas, M., Crop size is more important than neighborhood fruit availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers. Plant Ecol. 212 (2011), 889–899.
Carlo, T.A., Morales, J.M., Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. J. Ecol. 96 (2008), 609–618, 10.1111/j.1365-2745.2007.0.
Carrière, S.M., Andre, M., Letourmy, P., Olivier, I., McKey, D.B., Seed rain beneath remnant trees in a slash-and-burn agricultural system in southern Cameroon. J. Trop. Ecol. 18 (2002), 353–374, 10.1017/s0266467402002250.
Carrière, S.M., Letourmy, P., McKey, D.B., Effects of remnant trees in fallows on diversity and structure of forest regrowth in a slash-and-burn agricultural system in southern Cameroon. J. Trop. Ecol. 18 (2002), 375–396, 10.1017/S0266467402002262.
Chapman, C.A., Chapman, L.J., Wrangham, R.W., Hunt, K., Gebo, D., Gardner, L., Estimators of fruit abundance of tropical trees. Biotropica 24 (1992), 527–531.
Chasar, A., Harrigan, R.J., Holbrook, K.M., Dietsch, T.V., Fuller, T.L., Wikelski, M., Spatial and temporal patterns of frugivorous hornbill movements in Central Africa and their implications for rain forest conservation. Biotropica 46 (2014), 763–770, 10.1111/btp.12160.
Clark, C.J., Poulsen, J.R., Parker, V.T., The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest. Biotropica 33 (2001), 606–620, 10.1111/j.1744-7429.2001.tb00219.x.
Clark, C.J., Poulsen, J.R., Connor, E.F., Parker, V.T., Fruiting trees as dispersal foci in a semi-deciduous tropical forest. Oecologia 139 (2004), 66–75, 10.1007/s00442-003-1483-1.
Clark, C.J., Poulsen, J.R., Levey, D.J., Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 93 (2012), 554–564.
Côrtes, M.C., Uriarte, M., Integrating frugivory and animal movement: a review of the evidence and implications for scaling seed dispersal. Biol. Rev. 88 (2012), 255–272, 10.1111/j.1469-185X.2012.00250.x.
Cottee-Jones, H.E.W., Bajpai, O., Chaudhary, L.B., Whittaker, R.J., The importance of Ficus (Moraceae) trees for tropical forest restoration. Biotropica 48 (2016), 413–419.
de Wasseige, C., Marcken, D.P., Bayol, N., Hiol-Hio, F., Mayaux, P., Desclee, B., Nasi, R., Billand, A., Defourny, P., Eba'a Atyi, R., The Forests of the Congo Basin: state of the Forest 2010. 2012 doi:10.2788/47210.
Dormann, F.C., McPherson, M.J., Araújo, B.M., Bivand, R., Bolliger, J., Carl, G., Davies, G.R., Hirzel, A., Jetz, W., Daniel Kissling, W., Kühn, I., Ohlemüller, R., Peres-Neto, P.R., Reineking, B., Schröder, B., Schurr, M.F., Wilson, R., Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30 (2007), 609–628, 10.1111/j.2007.0906-7590.05171.x.
Forget, P.-M., Milleron, T., Evidence for secondary seed dispersal by rodents in Panama. J. Trop. Ecol. 87 (1991), 596–599.
Forget, P.-M., Sabatier, D., Dynamics of the seedling shadow of a frugivore-dispersed tree species in French Guiana. J. Trop. Ecol. 13 (1997), 767–773.
García, D., Martínez, I., Obeso, J.R., Seed transfer among bird-dispersed trees and its consequences for post-dispersal seed fate. Basic Appl. Ecol. 8 (2007), 533–543, 10.1016/j.baae.2006.11.002.
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., Thiollay, J.-M., Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65 (1985), 324–337.
González-Zamora, A., Arroyo-Rodríguez, V., Escobar, F., Rös, M., Oyama, K., Ibarra-Manríquez, G., Stoner, K.E., Chapman, C.A., Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS One, 9, 2014, e89346, 10.1371/journal.pone.0089346.
Guevara, S., Meave, J., Moreno-Casasola, P., Laborde, J., Floristic composition and structure of vegetation under isolated trees in neotropical pastures. J. Veg. Sci. 3 (1992), 655–664.
Haurez, B., Brostaux, Y., Petre, C., Doucet, J., Is the western lowland gorilla a good gardener? Evidence for directed dispersal in Southeast Gabon. Bois Forêt Des. Trop. 324 (2015), 39–50.
Head, J.S., Boesch, C., Makaga, L., Robbins, M.M., Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Int. J. Primatol. 32 (2011), 755–775, 10.1007/s10764-011-9499-6.
Herrera, J.M., García, D., The role of remnant trees in seed dispersal through the matrix: being alone is not always so sad. Biol. Conserv. 142 (2009), 149–158, 10.1016/j.biocon.2008.10.008.
Herrera, C.M., Jordano, P., Lopez-Soria, L., Amat, A.J., Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecol. Monogr. 64 (1994), 315–344.
Hilhorst, H.W.M., Karssen, C.M., Effect of chemical environment on seed germination. Seeds: the Ecology of Regeneration in Plant Communities, 2000, CAB International, Wallingford, 293–309.
Hooper, J., Bullington, R., Invasion of woody plants in abandoned soil bank area of Pine Rock Preserve in Ogle County. Transations Ill. State Acad. Sci. 65 (1973), 58–67.
Hubbell, S.P., A Unified Theory of Biodiversity and Biogeography. 2001, Princeton University Press, Princeton, New Jersey, USA.
Hubbell, S.P., Series, N., Mar, N., Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203 (2007), 1299–1309.
Idani, G., Seed dispersal by pygmy chimpanzees (Pan paniscus): a preliminary report. Primates 27 (1986), 441–447.
Idani, G., Kuroda, S., Kano, T., Asato, R., Flora and vegetation of wamba forest, central zaire, with reference to bonobo (Pan paniscus) foods. TROPICS 3 (1994), 309–332.
Jesus, F.M., Pivello, V.R., Meirelles, S.T., Franco, G.A.D.C., Metzger, J.P., The importance of landscape structure for seed dispersal in rain forest fragments. J. Veg. Sci. 23 (2012), 1126–1136, 10.1111/j.1654-1103.2012.01418.x.
Joshi, S., Biological control of parthenium hysterophorus L. (Asteraceae) by Cassia uniflora mill (Leguminosae), in Bangalore, India. Trop. Pest Manag. 37 (1991), 182–184.
Julliot, C., Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understory of tropical rain forest. J. Ecol. 85 (1997), 431–440.
Kato-Noguchi, H., Isolation and identification of an allelopathic substance in Pisum sativum. Phytochemistry 62 (2003), 1141–1144.
Kunz, B.K., Linsenmair, K., The role of the olive baboon (Papio anubis, Cercopithecidae) as seed disperser in a savanna-forest mosaic of West Africa. J. Trop. Ecol. 24 (2008), 235–246.
Kwit, C., Levey, D.J., Greenberg, C.H., Contagious seed dispersal beneath heterospecific fruiting trees and its consequences. Oikos 107 (2004), 303–308, 10.1111/j.0030-1299.2004.13388.x.
Lenz, J., Fiedler, W., Caprano, T., Friedrichs, W., Gaese, B., Wikelski, M., Böhning-Gaese, K., Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. Proc. R. Soc. Biol. Sci. 278 (2011), 2257–2264.
Levine, J., Murrell, D., The community-level consequences of seed dispersal patterns. Annu. Rev. Ecol. Evol. Syst. 34 (2003), 549–574, 10.1146/132400.
Lundberg, J., Moberg, F., Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6 (2003), 87–98.
Manasse, R., Howe, H., Competition for dispersal agents among tropical trees: influences of neighbors. Oecologia, 1983, 185–190.
McConkey, K.R., Primary seed shadow generated by gibbons in the rain forests of Barito Ulu, central Borneo. Am. J. Primatol. 52 (2000), 13–29 doi:10.1002/1098-2345(200009)52:1<13::AID-AJP2>3.0.CO;2-Y.
McDonnell, M.J., Stiles, E.W., The structural complexity of old field vegetation and the recruitment of bird-dispersed plant species. Oecologia 56 (1983), 109–116, 10.1007/BF00378225.
Moran, C., Catterall, C.P., Responses of seed-dispersing birds to amount of rainforest in the landscape around fragments. Conserv. Biol. 28 (2014), 551–560, 10.1111/cobi.12236.
Naniwadekar, R., Shukla, U., Isvaran, K., Datta, A., Reduced hornbill abundance associated with low seed arrival and altered recruitment in a hunted and logged tropical forest. PLoS One, 10, 2015, e0120062, 10.1371/journal.pone.0120062.
Nathan, R., Muller-Landau, H.C., Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15 (2000), 278–285.
Nicotra, A.B., Chazdon, R.L., Iriarte, S.V.B., Spatial heterogeneity of light and woodly seedling regeneration in tropical wet forests. Ecology 80 (1999), 1908–1926, 10.1890/0012-9658(1999)080[1908:SHOLAW]2.0.CO;2.
Nuñez-Iturri, G., Howe, H., Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in Western Amazonia. Biotropica 39 (2007), 348–354.
Petre, C.-A., Tagg, N., Beudels-Jamar, R.C., Haurez, B., Salah, M., Spetschinsky, V., Willie, J., Doucet, J.-L., Quantity and spatial distribution of seeds dispersed by a western lowland gorilla population in south-east Cameroon. J. Trop. Ecol., 2015, 1–12, 10.1017/S0266467415000073.
Pinheiro, J., Bates, D., Debroy, S., Sarkar, D., Linear and nonlinear mixed effects models. R. Core Team, 2012.
Pizo, M.A., Almeida-Neto, M., Determinants of fruit removal in Geonoma pauciflora, an understory palm of neotropical forests. Ecol. Res. 24 (2009), 1179–1186.
Poulsen, J.R., Clark, C.J., Smith, T.B., Seed dispersal by a diurnal primate community in the Dja Reserve. Cameroon. J. Trop. Ecol. 17 (2001), 787–808.
Poulsen, J.R., Clark, C.J., Bolker, B.M., Experimental manipulation of seed shadows of an Afrotropical tree determines drivers of recruitment. Ecology 93 (2012), 500–510.
Razafindratsima, O.H., Dunham, A.E., Assessing the impacts of non random seed dispersal by multiple frugivores partners on plant recruitment. Ecology 96 (2015), 24–30.
Russo, S.E., Augspurger, C.K., Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol. Lett. 7 (2004), 1058–1067.
Saracco, J.F., JA, C., Groom, M., Carlo, T.A., Crop size and fruit neighborhood effects on bird visitation to fruiting hefflera morototoni trees in Puerto Rico. Biotropica 37 (2005), 81–87.
Schupp, E.W., Milleron, T., Russo, S.E., Dissemination limitation and the origin and maintenance of species-rich tropical forests. Levey, D.J., Silva, W.R., Galetti, M., (eds.) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, 2002, CAB International, São Pedro, São Paulo, Brazil, 19–33.
Serckx, A., Huynen, M.-C., Bastin, J.-F., Hambuckers, A., Beudels-Jamar, R.C., Vimond, M., Raynaud, E., Kühl, H.S., Nest grouping patterns of bonobos (Pan paniscus) in relation to fruit availability in a forest-savannah mosaic. PLoS One, 9, 2014, e93742, 10.1371/journal.pone.0093742.
Serckx, A., Huynen, M.-C., Beudels-Jamar, R.C., Vimond, M., Bogaert, J., Kühl, H.S., Bonobo nest site selection and the importance of predictor scales in primate ecology. Am. J. Primatol. 78 (2016), 1326–1343, 10.1002/ajp.22585.
Slocum, M.G., How tree species differ as recruitment foci in a tropical pasture. Ecology 82 (2012), 2547–2559, 10.1890/0012-9658(2001) 082[2547:HTSDAR]2.0.CO;2.
Slocum, M.G., Horvitz, C.C., Seed arrival under different genera of trees in a neotropical pasture. Plant Ecol. 149 (2000), 51–62, 10.1023/A:1009892821864.
Souza Filho, A.P.S., Gurgel, E.S.C., Queiroz, M.S.M., Santos, J.U.M., Allelophatic activity of crude extracts from three species of Copaifera (Leguminosae-Caesalpinioidedae). Planta Daninha 28 (2010), 743–751.
Seltzer Carrie, E., Ndangalasi Henry, J., Cordeiro Norbert, J., Seed dispersal in the dark: shedding light on the role of fruit bats in Africa. Biotropica 45 (2013), 450–456.
Team, R.D.C., R: a Language and Environment for Statistical Computing. 2015, R Foundation for Statistical Computing, Vienna, Austria.
Terborgh, J.W., Nuñez-Iturri, G., Disperser-free tropical forests await an unhappy fate. Emerging Threats to Tropical Forests, 2006, University of Chicago Press 520 pp.
Trolliet, F., Serckx, A., Forget, P.-M., Beudels-Jamar, R.C., Huynen, M.-C., Hambuckers, A., Ecosystem services provided by a large endangered primate in a forest-savanna mosaic landscape. Biol. Conserv. 203 (2016), 55–66.
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 of the Congo Basin. Biotropica 49 (2017), 337–345, 10.1111/btp.12417.
Tsuji, Y., Yangozene, K., Sakamaki, T., Estimation of seed dispersal distance by the bonobo, Pan paniscus, in a tropical forest in Democratic Republic of Congo. J. Trop. Ecol. 26 (2010), 115–118.
Urquiza-Haas, T., Peres, C.A., Dolman, P.M., Regional scale effects of human density and forest disturbance on large-bodied vertebrates throughout the Yucatán Peninsula, Mexico. Biol. Conserv. 142 (2009), 134–148, 10.1016/j.biocon.2008.10.007.
Vanthomme, H., Bellé B., Forget, P.-M., Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42 (2010), 672–679.
Wang, B.C., Sork, V., Leong, M., Smith, T.B., Hunting of mammals reduces seed removal and dispersal of the afrotropical tree Antrocaryon klaineanum (Anacardiaceae). Biotropica 39 (2007), 340–347.
Wenny, D.G., Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol. Ecol. Res. 3 (2001), 51–74.
Whytock, R., Buij, R., Virani, M., Morgan, B., Do large birds experience previously undetected levels of hunting pressure in the forests of Central and West Africa?. Oryx 50 (2016), 76–83, 10.1017/S0030605314000064.
Wiegand, T., Martínez, I., Huth, A., Wiegand, T., Martı I., Huth, A., Recruitment in tropical tree species: revealing complex spatial patterns. Am. Nat. 174 (2016), 106–140, 10.1086/605368.
