The impact of red howler monkey latrines on the distribution of main nutrients and on topsoil profiles in a tropical rain forest

Austral Ecology

Volumn 35, Issue 5, 2010, Pages 549-559

  Dos Santos Neves, Nadia ^a   Feer, François ^a   Salmon, Sandrine ^a   CHateil, Carole ^a   Ponge, Jean François ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Earthworm; Faeces; Latrine; Nutrient; Red howler monkey; Root; Tropical rain forest

Indexed keywords

BEETLE; BIOACTIVITY; EARTHWORM; FECES; GROWTH RATE; HERBIVORE; MICROSTRUCTURE; NUTRIENT AVAILABILITY; NUTRIENT CYCLING; PH; PRIMATE; RAINFOREST; REGENERATION; ROOT SYSTEM; SOIL FAUNA; SOIL FERTILITY; SOIL NUTRIENT; SOIL ORGANIC MATTER; SOIL RESPIRATION; TOPSOIL; VERTICAL DISTRIBUTION;

AMAZON BASIN; FRENCH GUIANA;

ALOUATTA; ALOUATTA SENICULUS; COLEOPTERA; PRIMATES; VERTEBRATA;

EID: 77954842856     PISSN: 14429985     EISSN: 14429993     Source Type: Journal    
DOI: 10.1111/j.1442-9993.2009.02066.x     Document Type: Article

References (63)

1. Andresen E. Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 2002a, 34:261-72.
2. Andresen E. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol. Entomol. 2002b, 27:257-70.
3. Andresen E, Feer F. The role of dung beetles as secondary seed dispersers and their effects on plant regeneration in tropical rainforests. Seed Fate: Predation, Dispersal and Seedling Establishment 2005, 331-49. Forget P M, Lambert J EHulme P EVander Wall S B. eds, CAB International, Wallingford
4. Andresen E, Levey D L. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 2004, 139:45-54.
5. Bal L. Zoological Ripening of Soils 1982, Pudoc, Wageningen
6. Bernier N, Ponge J F. Humus form dynamics during the sylvogenetic cycle in a mountain spruce forest. Soil Biol. Biochem. 1994, 26:183-220.
7. Brown G G, Barois I, Lavelle P. Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur. J. Soil Biol. 2000, 36:177-98.
8. Bruun H H, Lundgren R, Philipp M. Enhancement of local species richness in tundra by seed dispersal through guts of muskox and barnacle goose. Oecologia 2008, 155:101-10.
9. Canellas L P, Olivares F L, Okorokova-Façanha A L, Façanha A R. Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol. 2002, 130:1951-57.
10. Charles-Dominique P. The field station. Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest 2001, 1-7. Bongers FCharles-Dominique PForget P MThéry M. eds, Kluwer, Dordrecht
11. Clayton D. Generalized linear mixed models. Markov Chain Monte Carlo Methods in Practice 1996, 275-303. Gilks W RRichardson SSpiegelhalter D J. eds, Chapman and Hall, New York
12. Dai X. Impact of cattle dung deposition on the distribution pattern of plant species in an alvar limestone grassland. J. Veg. Sci. 2000, 11:715-24.
13. Dalling J W, Muller-Landau H C, Wright S J, Hubbell S P. Role of dispersal in the recruitment limitation of neotropical pioneer species. J. Ecol. 2002, 90:714-27.
14. Decaëns T, Mariani L, Betancourt N, Jiménez J J. Seed dispersion by surface casting activities of earthworms in Colombian grasslands. Acta Oecol. 2003, 24:175-85.
15. Duxbury J M, Scott Smith M, Doran J W. Soil organic matter as a source and a sink of plant nutrients. Dynamics of Soil Organic Matter in Tropical Ecosystems 1989, 33-67. Coleman D C, Oades J M, Uehara G. eds, University of Hawaii Press, Honolulu
16. Estrada A, Anzures D A, Coates-Estrada R. Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am. J. Primatol. 1999, 48:253-62.
17. World Reference Base for Soil Resources 2006, FAO, Food and Agriculture Organization of the United Nations, Rome
18. Feeley K. The role of clumped defecation in the spatial distribution of soil nutrients and the availability of nutrients for plant uptake. J. Trop. Ecol. 2005, 21:99-102.
19. Feer F. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. J. Trop. Ecol. 1999, 15:129-42.
20. Feer F, Pincebourde S. Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. J. Trop. Ecol. 2005, 21:21-30.
21. Fonty E, Sarthou C, Larpin D, Ponge J F. A 10-year decrease in plant species richness on a neotropical inselberg: detrimental effects of global warming? Glob. Change Biol. 2009, 15:2360-74.
22. Gilbert K A. Red howling monkey use of specific defecation sites as a parasite avoidance strategy. Anim. Behav. 1997, 54:451-55.
23. Grimaldi M, Riéra B. Geography and climate. Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest 2001, 9-18. Bongers F, Charles-Dominique PForget P MThéry M. eds, Kluwer, Dordrecht
24. Härdtle W, von Oheimb G, Friedel A, Meyer H, Westphal C. Relationship between pH-values and nutrient availability in forest soils: the consequences for the use of ecograms in forest ecology. Flora 2004, 199:134-42.
25. Heard S B. Pitcher-plant midges and mosquitoes: a processing chain commensalism. Ecology 1994, 75:1647-60.
26. Hope G, Pask J. Tropical vegetational change in the late Pleistocene of New Caledonia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 1998, 142:1-21.
27. James S W. Localized dynamics of earthworm populations in relation to bison dung on North American tallgrass prairie. Soil Biol. Biochem. 1992, 24:1471-76.
28. Jewell P L, Käuferle D, Güsewell S, Berry N R, Kreuzer M, Edwards P J. Redistribution of phosphorus by cattle on a traditional mountain pasture in the Alps. Agr. Ecosyst. Environ. 2007, 122:377-86.
29. Julliot C. Frugivory and seed dispersal by red howler monkeys: evolutionary aspect. Rev. Ecol. 1994, 49:331-41.
30. Julliot C. Seed dispersal by red howler monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. Int. J. Primatol. 1996a, 17:239-57.
31. Julliot C. Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am. J. Primatol. 1996b, 40:261-82.
32. Julliot C. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. J. Ecol. 1997, 85:431-40.
33. Julliot C, Sabatier D. Diet of the red howler monkey (Alouatta seniculus) in French Guiana. Int. J. Primatol. 1993, 14:527-50.
34. Julliot C, Simmen B, Zhang S. Frugivory and seed dispersal by three neotropical primates: impact on plant regeneration. Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest 2001, 197-205. Bongers F, Charles-Dominique P, Forget P MThéry M. eds, Kluwer, Dordrecht
35. Lavelle P, Blanchart E, Martin A. A hierarchical model for decomposition in terrestrial ecosystems: application to soils of the humid tropics. Biotropica 1993, 25:130-50.
36. Lee K E, Foster R C. Soil fauna and soil structure. Aust. J. Soil Res. 1991, 29:745-75.
37. Lussenhop J, Kumar R, Wicklow D T, Lloyd J E. Insect effects on bacteria and fungi in cattle dung. Oikos 1980, 34:54-8.
38. Martens R. Estimation of microbial biomass in soil by the respiration method: importance of soil pH and flushing methods for the measurement of respired CO2. Soil Biol. Biochem. 1987, 19:77-81.
39. Martius C, Höfer H, Garcia M V B, Römbke J, Hanagarth W. Litter fall, litter stocks and decomposition rates in rainforest and agroforestry sites in central Amazonia. Nutr. Cycl. Agroecosyst. 2004, 68:137-54.
40. Nichols E, Larsen T, Spector S. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol. Conserv. 2007, 137:1-19.
41. Pakeman R J, Digneffe G, Small J L. Ecological correlates of endozoochory by herbivores. Funct. Ecol. 2002, 16:296-304.
42. Parry L, Barlow J, Peres C A. Large-vertebrate assemblages of primary and secondary forests in the Brazilian Amazon. J. Trop. Ecol. 2007, 23:653-62.
43. Pearson T R H, Burslem D F R P, Mullins C E, Dalling J W. Functional significance of photoblastic germination in neotropical pioneer trees: a seed's eye view. Funct. Ecol. 2003, 17:394-402.
44. Petersen H, Luxton M. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 1982, 39:287-388.
45. Poncy O, Sabatier D, Prévost M F, Hardy I. The lowland high rainforest: structure and tree sepcies diversity. Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest 2001, 31-46. Bongers F, Charles-Dominique P, Forget P M, Théry M. eds, Kluwer, Dordrecht
46. Ponge J F. Food resources and diets of soil animals in a small area of Scots pine litter. Geoderma 1991, 49:33-62.
47. Ponge J F, André J, Zackrisson O, Bernier N, Nilsson M C, Gallet C. The forest regeneration puzzle: biological mechanisms in humus layer and forest regeneration dynamics. BioScience 1998, 48:523-30.
48. Pouvelle S, Feer F, Ponge J F. Topsoil as affected by dung deposition under resting places of red howler monkey (Alouatta seniculus). Pedosphere 2008, 18:691-98.
49. Pouvelle S, Jouard S, Feer F, Tully T, Ponge J F. The latrine effect: impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil. J. Trop. Ecol. 2009, 25:239-48.
50. Sadaka N, Ponge J F. Climatic effects on soil trophic networks and the resulting humus profiles in holm oak (Quercus rotundifolia) forests in the High Atlas of Morocco as revealed by correspondence analysis. Eur. J. Soil Sci. 2003, 54:767-77.
51. Scown J, Baker G. The influence of livestock dung on the abundance of exotic and native earthworms in a grassland in south-eastern Australia. Eur. J. Soil Biol. 2006, 42:S310-S315.
52. Shapiro S S, Wilk M B. An analysis of variance test for normality (complete samples). Biometrika 1965, 52:591-611.
53. St John T V, Coleman D C, Reid C P P. Growth and spatial distribution of nutrient-absorbing organs: selective exploitation of soil heterogeneity. Plant Soil 1983, 71:487-93.
54. Svendsen T S, Grønvold J, Holter P, Sommer C. Field effects of ivermectin and fenbendazole on earthworm populations and the disappearance of dung pats from bolus-treated cattle. Appl. Soil Ecol. 2003, 24:207-18.
55. Théry M, Larpin D. Seed dispersal and vegetation dynamics at a cock-of-the-rock's lek in the tropical forest of French Guiana. J. Trop. Ecol. 1993, 9:109-16.
56. Tiessen H, Cuevas E, Chacon P. The role of soil organic matter in sustaining soil fertility. Nature 1994, 371:783-85.
57. Tiunov A V, Scheu S. Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 2004, 138:83-90.
58. Topoliantz S, Ponge J F, Viaux P. Earthworm and enchytraeid activity under different arable farming systems, as exemplified by biogenic structures. Plant Soil 2000, 225:39-51.
59. Van den Wollenberg A L. Redundancy Analysis: an alternative for Canonical Correlation Analysis. Psychometrika 1977, 42:207-19.
60. Vieira S, Trumbore S, Camargo P B. Slow growth rates of Amazonian trees: consequences for carbon cycling. Proc. Natl Acad. Sci. USA 2005, 102:18502-7.
61. Vitousek P M. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 1984, 65:285-98.
62. Vulinec K. Dung beetles (Coleoptera: Scarabaeidae), monkeys, and conservation in Amazonia. Fla. Entomol. 2000, 83:229-41.
63. Wardle D A, Bardgett R D, Klironomos J N, Setälä H, Van der Putten W H, Wall D H. Ecological linkages between aboveground and belowground biota. Science 2004, 304:1629-33.