[en] The quantification of seed dispersal and predation processes has been gaining increased importance in the assessment of forest responses to anthropogenic disturbance, but also in developing an understanding of forest dynamics facing particular reproductive strategies. Seed removal rate is a reliable estimator of animal activities relating to these processes and can be quickly and easily estimated using a rapid assessment method (RAM) described by Lermyte & Forget (2009) and Boissier et al. (2014). This method consists in selecting trees reaching a given fruit crop in plots of interest and estimating, under each tree, the proportion of removed seeds in a single quadrat among the places having the highest crops; the proportion of removed seeds is obtained by enumeration of fruit scraps and intact fruits and estimation of their seed contents. The objective of this work is to evaluate the reliability of this method and to propose alternative estimation protocols (APs) in order to obtain an index of animal interaction with seeds.
To do so, we estimated produced and removed seed numbers in up to 30 random 1 sq.m. quadrats under a total of 19 trees of Afzelia bipindensis, Dialium pachyphyllum/zenkeri and Xylopia staudtii. Secondly, we investigated the influence of tree size and fruit production on seed removal rate using a generalized linear mixed model. Thirdly, we used a generalized linear mixed model and a bootstrap procedure to test if RAM and APs are biased. Then, we compared their accuracy throughout their mean squared error, also obtained with a bootstrap approach.
Despite its interesting accuracy, we showed that the RAM is positively biased. Removal rate was obviously influenced by canopy size and fruit production whereas the quadrats with higher fruit production have higher seed removal rates. Thus, trees with representative sizes and crops of the studied plots have to be sampled. Secondly, as an AP, random selection of several quadrats was found to be the best method. Based on these results, we recommend using the mean of three random quadrats per tree to estimate seed removal rate. It is an unbiased estimator, more accurate and more time efficient than the RAM. However, attention should be paid to select a proper quadrat size, in line with seed and fruit numbers, since the accuracy of the methods depends on these quantities. Such a choice could be made using a mean squared error criterion obtained from a preliminary intensive sampling of some specimens of the focal species.
Disciplines :
Sciences de l’environnement & écologie
Auteur, co-auteur :
Hambuckers, julien ; Université de Liège > HEC Liège : UER > Statistique appliquée à la gestion et à l'économie
Dauvrin, Alice
Trolliet, Franck ; Université de Liège > Département d'astrophys., géophysique et océanographie (AGO) > Modélisation du climat et des cycles biogéochimiques
Evrard, Quentin ; Université de Liège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales
Forget, Pierre-Michel
Hambuckers, Alain ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Langue du document :
Anglais
Titre :
How can seed removal rates of zoochoric tree species be assessed quickly and accurately?
Date de publication/diffusion :
2017
Titre du périodique :
Forest Ecology and Management
ISSN :
0378-1127
eISSN :
1872-7042
Maison d'édition :
Elsevier
Volume/Tome :
403
Pagination :
152-160
Peer reviewed :
Peer reviewed vérifié par ORBi
Organisme subsidiant :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE] ARES - Académie de Recherche et d'Enseignement Supérieur [BE] DFG - German Research Foundation [DE]
Subventionnement (détails) :
F. T. was supported by the FRIA and the FNRS foundations and A. D.
by the ARES. We are grateful to WWF in Congo DR and the Precious
Wood Gabon Society - Compagnie Equatoriale des Bois in Gabon, which
welcomed the field teams. J.H acknowledges the support of the
Research Training Group 1644 “Scaling problems in statistics”, funded
by the German Fund for Scientific Research (DFG).
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 46 (2014), 264–267.
Barnett, A.A., Boyle, S.A., Pinto, L.P., Lourenc, W.C., Almeida, T., Silva, W.S., Ronchi-Teles, B., Bezerra, B.M., Ross, C., MacLarnon, A., Spironello, W.R., Primary seed dispersal by three Neotropical seed-predating primates (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). J. Trop. Ecol. 28 (2012), 543–555.
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. 75 (2013), 394–403.
Beckman, N.G., Muller-Landau, H.C., Differential effects of hunting on pre-dispersal seed predation and primary and secondary seed removal of two neotropical tree species. Biotropica 39 (2007), 328–339.
Blendinger, P.G., Díaz-Vélez, M.C., Experimental field test of spatial variation in rodent predation of nuts relative to distance and seed density. Oecologia 163 (2010), 415–423.
Boissier, O., Impact des pressions anthropiques sur les communautés de frugivores et la dispersion des graines en forêt guyanaise (Thèse de doctorat). 2012, Museum National d'Histoire Naturelle, Paris.
Boissier, O., Bouiges, A., Mendoza, I., Feer, F., Forget, P.-M., Rapid assessment of seed semoval and frugivore activity as a aool for monitoring the health status of tropical forests. Biotropica 46 (2014), 633–641.
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H., White, J.-S.S., Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24 (2008), 127–135.
Brewer, S.W., Rejmánek, M., Small rodents as significant dispersers of tree seeds in a Neotropical forest. J. Veg. Sci. 10 (1999), 165–174.
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. 31 (2007), 8–12.
Calvino-Cancela, M., Rubido-Bará, M., Effects of seed passage through slugs on germination. Plant Ecol. 213 (2012), 663–673.
Chapman, C.A., Chapman, L.J., Wangham, R., Hunt, K., Gebo, D., Gardner, L., Estimators of fruit abundance of tropical trees. Biotropica 24 (1992), 527–531.
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.
Culot, L., Mann, D.J., Muñoz Lazo, F.J.J., Huynen, M., Heymann, E.W., Tamarins and dung deetles: an efficient diplochorous dispersal system in the Peruvian Amazonia. Biotropica 43 (2011), 84–92.
Duncan, R.S., Chapman, C.A., Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecol. Appl. 9 (1999), 998–1008.
Efron, B., Bootstrap methods: another look at the Jackknife. Ann. Stat. 7 (1979), 1–26.
Efron, B., Tibshirani, J.T., An Introduction to the Bootstrap. 1993, Chapman & Hall CRC, Boca Raton.
Flohic, G.L., Motsch, P., DeNys, H., Childs, S., Courage, A., King, T., Behavioural ecology and group cohesion of juvenile western lowland gorillas (Gorilla g. gorilla) during rehabilitation in the Batéké Plateaux National Park, Gabon. PLoS ONE, 10, 2015, e0119609.
Flörchinger, M., Braun, J., Böhning-Gaese, K., Schaefer, H.M., Fruit size, crop mass, and plant height explain differential fruit choice of primates and birds. Oecologia 164 (2010), 151–161.
Forget, P.M., Jansen, P.A., Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product. Conserv. Biol. 21 (2007), 106–113.
Forget, P.-M., Wenny, D., How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal. Forget, P.-.M., Lambert, J.E., Hulme, P.E., Vander Wall, S.B., (eds.) Seed Fate: Predation, Dispersal, and Seedling Establishment, 2005, CABI, Wallingford, 379–394.
Foster, M.S., Factors influencing bird foraging preferences among conspecific fruit trees. Condor 92 (1990), 844–854.
Gartlan, J.S., Struhsaker, T., Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Afr. J. Zool. 168 (1972), 221–266.
Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, 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.
Guitián, J., Munilla, I., Responses of mammal dispersers to fruit availability: Rowan (Sorbus aucuparia) and carnivores in mountain habitats of northern Spain. Acta Oecol. 36 (2010), 242–247.
Hernández, Á., Cherry removal by seed-dispersing mammals: Mutualism through commensal association with frugivorous birds. Pol. J. Ecol. 56 (2008), 127–138.
Hulme, P.E., Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111 (1997), 91–98.
Izhaki, I., Emodin - a secondary metabolite with multiple ecological functions in higher plants. New Phytol. 155 (2002), 205–217.
Janmaat, K.R.L., Ban, S.D., Boesch, C., Chimpanzees use long-term spatial memory to monitor large fruit trees and remember feeding experiences across seasons. Anim. Behav. 86 (2013), 1183–1205.
Jones, F.A., Comita, L.S., Density-dependent pre-dispersal seed predation and fruit set in a tropical tree. Oikos 119 (2010), 1841–1847.
Jordano, P., Fruits and frugivory. Fenner, M., (eds.) Seeds: the Ecology of Plant Regeneration in Plant Communities, 2000, CABI, Wallingford, 125–166.
Krief, S., Jamart, A., Hladik, C.M., On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45 (2004), 141–145.
Leighton, M., Leighton, D.R., The relationship of size of feeding aggregate to size of food patch: howler monkeys (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica 14 (1982), 81–96.
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. 12 (2010), 43–55.
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. 2 (2009), 404–424.
Lottf, Y.V.D., Thatcher, R.L., Rossomv, L., Reimiardt, C.F., The influence of baboon predation and time in water on germination and early establishment of Opuntia stricta (Australian pest pear) in the Kruger National Park. Koedoe 42 (1999), 43–50.
McClearn, D., Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. J. Mammal. 73 (1992), 245–261.
Meunier, Q., Moumbogou, C., Doucet, J.L., Les arbres utiles du Gabon. 2015, Les Presses Agronomiques de Gembloux, Gembloux.
Mood, A.M., Graybill, F.A., Boes, D.C., Introduction to the Theory of Statistics. 1974, McGraw-Hill, New-York.
Moreira, J.I., Riba-Hernández, P., Lobo, J.A., Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large-seeded tree (Virola surinamensis) in a human-modified landscape. Biotropica 49:4 (2017), 502–510.
Naito, Y., Kanzaki, M., Numata, S., Obayashi, K., Konuma, A., Nishimura, S., Ohta, S., Tsumura, Y., Okuda, T., Lee, S.L., Muhammad, N., Size-related flowering and fecundity in the tropical canopy tree species, Shorea acuminata (Dipterocarpaceae) during two consecutive general flowerings. J. Plant Res. 121 (2008), 33–42.
Niederhauser, E.C., Matlack, G.R., All frugivores are not equal exploitation competition determines seed survival and germination in a fleshy-fruited forest herb. Plant Ecol. 216 (2015), 1203–1211.
Norden, N., Chave, J., Belbenoit, P., Caubère, A., Châtelet, P., Forget, P.-M., Thébaud, C., Mast fruiting is a frequent strategy in woody species of Eastern South America. Plos One, 2, 2007, e1079.
Ortiz-Pulido, R., Rico-Gray, V., The effect of spatio-temporal variation in understanding the fruit crop size hypothesis. Oikos 91 (2000), 523–527.
Poulsen, J.R., Clark, C.J., Connor, E.F., Smith, T.B., Differential resource use by primates and hornbills Implications for seed dispersal. Ecology 83 (2002), 228–240.
Rosenberger, A.L., Evolution of feeding niches in New World monkeys. Am. J. Phys. Anthropol. 88 (1992), 525–562.
Rosin, C., Poulsen, J.R., Telemetric tracking of scatterhoarding and seed fate in a Central African forest. Biotropica 49 (2016), 170–176.
Schaefer, H.M., Schmidt, V., Winkler, H., Testing the defence trade-off hypothesis How contents of nutrients and secondary compounds affect fruit removal. Oikos 102 (2003), 318–328.
Steele, M.A., Bugdal, M., Yuan, A., Bartlow, A., Buzalewski, J., Lichti, N., Swihart, R., Cache placement, pilfering, and a recovery advantage in a seed-dispersing rodent could predation of scatter hoarders contribute to seedling establishment?. Acta Oecol. 37 (2011), 554–560.
Stevenson, P.R., Link, A., Ramírez, B.H., Frugivory and seed fate in Bursera inversa (Burseraceae) at Tinigua Park, Colombia Implications for primate conservation. Biotropica 37 (2005), 431–438.
Suarez, S.A., Ecological factors predictive of wild spider monkey (Ateles belzebuth) foraging decisions in Yasuní. Ecuador. Am. J. Primatol. 76 (2014), 1185–1195.
Toh, I., Gillespie, M., Lamb, D., The role of isolated trees in facilitating tree seedling recruitment at a degraded sub-tropical rainforest site. Restor. Ecol. 7 (1999), 288–297.
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 49 (2017), 337–345.
Trolliet, F., Serckx, A., Forget, P.M., Beudels-Jamar, R., 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., Vermeulen, C., Huynen, M.-C., Hambuckers, A., Use of camera traps for wildlife studies a review. BASE 18 (2014), 446–454.
Türke, M., Andreas, K., Gossner, M.M., Kowalski, E., Lange, M., Boch, S., Socher, S.A., Müller, J., Prati, D., Fischer, M., Meyhöfer, R., Weisser, W.W., Are gastropods, rather than ants, important dispersers of seeds of myrmecochorous forest herbs?. Am. Nat. 179 (2012), 124–131.
Venables, W.N., Ripley, B.D., Modern Applied Statistics with S. 2002, Springer Science + Bussiness Media, New York.
Wang, B.C., Sork, V.L., Leong, M.T., 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., Seed dispersal, seed predation, and seedling recruitment of a Neotropical montane tree. Ecol. Monogr. 70 (2000), 331–351.
Wilks, C., Issembé, Y., Les arbres de la Guinée Equatoriale Région continentale. 2000, CUREF, Bâta (Guinée Equatoriale).
Willson, M.F., Irvine, A.K., Walsh, N.G., Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21 (1989), 133–147.
