Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T06:37:03.193Z Has data issue: false hasContentIssue false
  • English
  • Français

The latrine effect: impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil

Published online by Cambridge University Press:  01 May 2009

Sandrine Pouvelle ,
Sylvie Jouard ,
François Feer ,
Thomas Tully  and
Jean-François Ponge
Sandrine Pouvelle
Affiliation:
Muséum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 91800 Brunoy, France
Sylvie Jouard
Affiliation:
Muséum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 91800 Brunoy, France
François Feer
Affiliation:
Muséum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 91800 Brunoy, France
Thomas Tully
Affiliation:
Muséum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 91800 Brunoy, France
Jean-François Ponge*
Affiliation:
Muséum National d'Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 91800 Brunoy, France
*
*Corresponding author. Email: ponge@mnhn.fr
Get access Rights & Permissions [Opens in a new window]

Abstract:

We studied the impact of dung deposition by the red howler monkey (Alouatta seniculus), and subsequent burial by dung beetles and other biotic and abiotic processes, on the distribution of small seeds in the soil seed bank (Nouragues Reserve, French Guiana). Seeds were collected from 54 soil samples taken under three sleeping sites and adjoining control sites, at three positions according to a fixed grid and at three different depths (0–2, 2–4 and 4–6 cm). Despite large differences between the three sites, defecation areas (latrines) were found to contain more seeds and higher seed diversity than control areas. Seed density decreased with depth in the top 6 cm in two sites but not in the third. Shannon diversity decreased with depth in both defecation and control areas. Differences in the distribution of seeds of different species were found according to size and growth habits (pioneer vs non-pioneer species). The viability of seeds, ascertained from toughness and integrity of the seed coat, varied according to depth, site and defecation. Seed viability was on average higher in defecation areas compared with control areas.

Keywords

Alouatta seniculusforest regenerationFrench Guianarain forestseed dispersalsoil seed bank
Type
Research Article
Information
Journal of Tropical Ecology , Volume 25 , Issue 3 , May 2009 , pp. 239 - 248
Copyright
Copyright © Cambridge University Press 2009

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

ANDRESEN, E. 2002a. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27:257–270.Google Scholar
ANDRESEN, E. 2002b. Primary seed dispersal by red howler monkey and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34:262–272.CrossRefGoogle Scholar
ANDRESEN, E. & FEER, F. 2005. The role of dung beetles as secondary seed dispersers and their effects on plant regeneration in tropical rainforests. Pp. 331–349 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.Google Scholar
ANDRESEN, E. & LEVEY, D. J. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45–54.CrossRefGoogle ScholarPubMed
BLOUIN, M., ZUILY-FODIL, Y., PHAM-THI, A. T., LAFFRAY, D., REVERSAT, G., PANDO, A., TONDOH, J. & LAVELLE, P. 2005. Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites. Ecology Letters 8:202–208.CrossRefGoogle Scholar
BORZA, J. K., WESTERMAN, P. R. & LIEBMAN, M. 2007. Comparing estimates of seed viability in three foxtail (Setaria) species using the imbibed seed crush test with and without additional tetrazolium testing. Weed Technology 21:518–522.CrossRefGoogle Scholar
CHARLES-DOMINIQUE, P. 2001. The field station. Pp. 1–7 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.Google Scholar
CHARLES-DOMINIQUE, P. & COCKLE, A. 2001. Frugivory and seed dispersal by bats. Pp. 207–215 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.CrossRefGoogle Scholar
COLWELL, R. K. & CODDINGTON, J. A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 345:101–118.Google ScholarPubMed
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine and in rain forest trees. Pp. 298–312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. PUDOC, Wageningen.Google Scholar
DALLING, J. W., SWAINE, M. D. & GARWOOD, N. C. 1998. Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564–578.CrossRefGoogle Scholar
DALLING, J. W., MULLER-LANDAU, H. C., WRIGHT, S. J. & HUBBELL, S. P. 2002. Role of dispersal in the recruitment limitation of neotropical pioneer species. Journal of Ecology 90:714–727.Google Scholar
DECAËNS, T., MARIANI, L., BETANCOURT, N. & JIMENEZ, J. J. 2003. Seed dispersion by surface casting activities of earthworms in Colombian grasslands. Acta Oecologica 24: 175–185.CrossRefGoogle Scholar
DÍAZ, S., TILMAN, D. & FARGIONE, J. 2005. Biodiversity regulation of ecosystem services. Pp. 297–329 in Hassan, R. M., Scholes, R. & Ash, N. (eds.). Ecosystems and human well-being: current state and trends. Island Press, Washington.Google Scholar
ENGEL, T. 2000. Seed dispersal and forest regeneration in a tropical lowland biocoenosis (Shimba Hills, Kenya). Logos, Berlin. 354 pp.Google Scholar
FAO 2006. World reference base for soil resources. Food and Agriculture Organization of the United Nations, Rome. 142 pp.Google Scholar
FAVRICHON, V. 1994. Classification des espèces arborées en groupes fonctionnels en vue de la réalisation d'un modèle de dynamique des peuplements en forêt guyanaise. Revue d'Écologie (La Terre et la Vie) 49:379–403.CrossRefGoogle Scholar
FEELEY, K. 2005. The role of clumped defecation in the spatial distribution of soil nutrients and the availability of nutrients for plant uptake. Journal of Tropical Ecology 21:99–102.Google Scholar
FEER, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. Journal of Tropical Ecology 15:129–142.CrossRefGoogle Scholar
FEER, F. & HINGRAT, Y. 2005. Effects of forest fragmentation on a dung beetle community in French Guiana. Conservation Biology 19:1103–1112.CrossRefGoogle Scholar
FEER, F. & PINCEBOURDE, S. 2005. Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. Journal of Tropical Ecology 21:21–30.Google Scholar
FORGET, P. M. 1996. Removal of seeds of Carapa procera (Meliaceae) by rodents and their fate in rainforest in French Guiana. Journal of Tropical Ecology 12:751–761.CrossRefGoogle Scholar
FORGET, P. M. 1997. Effect of microhabitat on seed fate and seedling performance in two rodent-dispersed tree species in rain forest in French Guiana. Journal of Ecology 85:693–703.Google Scholar
FORGET, P. M. & JANSEN, P. A. 2007. Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product. Conservation Biology 21:106–113.CrossRefGoogle ScholarPubMed
GRIMALDI, M. & RIÉRA, B. 2001. Geography and climate. Pp. 9–18 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.CrossRefGoogle Scholar
HENRY, M. & JOUARD, S. 2007. Effect of bat exclusion on patterns of seed rain in tropical rain forest in French Guiana. Biotropica 39:510–518.Google Scholar
IHAKA, R. & GENTLEMAN, R. 1996. R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5:299–314.Google Scholar
JANKOWSKA-BŁASCZUK, M. & GRUBB, P. J. 2006. Changing perspectives on the role of the soil seed bank in northern temperate deciduous forests and in tropical lowland rain forests: parallels and contrasts. Perspectives in Plant Ecology, Evolution and Systematics 8:3–21.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104:501–528.CrossRefGoogle Scholar
JULLIOT, C. 1992. Utilisation des ressources alimentaires par le singe hurleur roux, Alouatta seniculus (Atelidae, Primates), en Guyane: impact de la dissémination des graines sur la régénération forestière. D.Sc. Thesis, University of Tours, France.Google Scholar
JULLIOT, C. 1994. Frugivory and seed dispersal by red howler monkeys: evolutionary aspect. Revue d'Écologie (La Terre et la Vie) 49:331–341.CrossRefGoogle Scholar
JULLIOT, C. 1996a. Seed dispersal by red howler monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology 17:239–258.Google Scholar
JULLIOT, C. 1996b. Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. American Journal of Primatology 40:261–282.Google Scholar
JULLIOT, C. 1997. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. Journal of Ecology 85:431–440.CrossRefGoogle Scholar
JULLIOT, C. & SABATIER, D. 1993. Diet of the howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology 14:527–550.Google Scholar
JULLIOT, C., SIMMEN, B. & ZHANG, S. 2001. Frugivory and seed dispersal by three neotropical primates: impact on plant regeneration. Pp. 197–205 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.CrossRefGoogle Scholar
LAMBERT, J. E. & CHAPMAN, C. A. 2005. The fate of primate-dispersed seeds: deposition pattern, dispersal distance and implications for conservation. Pp. 137–150 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.Google Scholar
LEVEY, D. J. & BYRNE, M. M. 1993. Complex ant–plant interactions: rain forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74:1802–1812.Google Scholar
MARTHEWS, T. R., MULLINS, C. E., DALLING, J. W. & BURSLEM, D. F. R. P. 2008. Burial and secondary dispersal of small seeds in a tropical forest. Journal of Tropical Ecology 24:595–605.CrossRefGoogle Scholar
PEARSON, T. R. H., BURSLEM, D. F. R. P., MULLINS, C. E. & DALLING, J. W. 2003. Functional significance of photoblastic germination in neotropical pioneer trees: a seed's eye view. Functional Ecology 17:394–402.CrossRefGoogle Scholar
PINHEIRO, J. C. & BATES, D. M. 2000. Mixed-effects models in S and S-Plus. Springer, New York. 528 pp.CrossRefGoogle Scholar
PIZO, M. A., PASSOS, L. & OLIVEIRA, P. S. 2005. Ants as seed dispersers of fleshy diaspores in Brazilian Atlantic forests. Pp. 315–329 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.Google Scholar
PONCE-SANTIZO, G., ANDRESEN, E., CANO, E. & CUARÓN, A. D. 2006. Dispersión primaria de semillas por Primates y dispersión secundaria por escarabajos coprófagos en Tikal, Guatemala. Biotropica 38:390–397.CrossRefGoogle Scholar
PONCY, O., SABATIER, D., PRÉVOST, M. F. & HARDY, I. 2001. The lowland high rainforest: structure and tree species diversity. Pp. 31–46 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.CrossRefGoogle Scholar
POUVELLE, S., FEER, F. & PONGE, J. F. 2008. Topsoil effects of dung deposition under red howler monkey (Alouatta seniculus) resting places. Pedosphere 18:691–698.Google Scholar
SAULEY, S. M. & SWAINE, M. D. 1988. Rain forest seed dynamics during succession at Gogol, Papua New Guinea. Journal of Ecology 76:1133–1152.CrossRefGoogle Scholar
SHEIL, D. & BURSLEM, D. F. R. P. 2003. Disturbing hypotheses in tropical forests. Trends in Ecology and Evolution 18:18–26.CrossRefGoogle Scholar
SIMMEN, B., JULLIOT, C., BAYART, F. & PAGÈS-FEUILLADE, E. 2001. Diet and population densities of the primate community in relation to fruit supplies. Pp. 89–101 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Théry, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.CrossRefGoogle Scholar
THÉRY, M. & LARPIN, D. 1993. Seed dispersal and vegetation dynamics at a cock-of-the-rock's lek in the tropical forest of French Guiana. Journal of Tropical Ecology 9:109–116.CrossRefGoogle Scholar
VANDER WALL, S. B. & LONGLAND, W. 2004. Diplochory: are two dispersers better than one? Trends in Ecology and Evolution 19:155–161.Google Scholar
VITOUSEK, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298.CrossRefGoogle Scholar
VULINEC, K., LAMBERT, J. E. & MELLOW, D. J. 2006. Primate and dung beetle communities in secondary growth rain forests: implications for conservation of seed dispersal systems. International Journal of Primatology 27:855–879.Google Scholar