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Ecosphere Volume 10 ,Issue 3 ,2019-03-18
Birds of a feather flock together: Functionally similar vertebrates positively co‐occur in Guianan forests
Thomas Denis 1 , 2 Cécile Richard‐Hansen 1 Olivier Brunaux 3 Stéphane Guitet 3 , 4 Bruno Hérault 5 , 6
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Received 2018-09-11, accepted for publication 2018-10-19, Published 2018-10-19

Abstract Medium‐ and large‐sized vertebrates play a key role in shaping overall forest functioning. Despite this, vertebrate interactions, from competition to mutualism, remain poorly studied, even though these interactions should be taken into account in our conservation and management strategies. Thus, we tackled the question of vertebrate co‐occurrence in tropical rainforests: Are (negative or positive) co‐occurrences dependent on forest structure and composition? and Are these co‐occurrences linked to functional species similarity? We recorded the occurrence of 21 medium‐ and large‐sized vertebrates in 19 French Guianan locations in which a large set of forest structure and composition descriptors were collected. We used a probabilistic model to look for co‐occurrences at different spatial scales, and species pairwise co‐occurrences were then compared to those generated solely on the basis of forest structure and composition. We then quantified the co‐occurrence strength between pairwise species dyads and determined whether they relied on species functional similarity, controlling for the environmental effects. We found that positive co‐occurrences vastly outnumbered negative co‐occurrences, were only partly shaped by the local environment, and were closely linked to species functional similarity. Thus, groups of species sharing similar functional traits are more prone to co‐occur, highlighting the key role of functional redundancy in structuring species assemblages. We discuss how positive interactions could generate the predominance of positive co‐occurrences in oligotrophic terra firme (unflooded) forests when resources are scarce and dispersed in dry season. Finally, we identified functional groups based on co‐occurrence strength and suggested that frugivory/granivory and body size are of primary importance in species interactions in Neotropical vertebrate communities.


terra firme;mutualism;mixed‐species associations;mammals;information exchange;Guiana Shield;birds;activity matching


© 2019 The Ecological Society of America


Study area in French Guiana, northern South America, including 19 survey sites. The left part of the figure illustrates the sampling design: Four line transects were used to sample the diurnal medium‐ and large‐sized vertebrates (100‐m transect unit) and environmental conditions (i.e., forest structure and forest composition measured in each plot of 100 m × 20 m). Data were aggregated to calculate species occurrence and environmental conditions for different spatial scales from 200 to 3000 m.

Comparison of the percentage of significant positive (red) and negative (blue) co‐occurrence types between pairwise species for different spatial scales. Dashed line is the percentage of significant pairwise species co‐occurrences at P = 0.05 (significant level). Lower and upper borders of envelopes are the 0.01 and 0.10 significant levels, respectively.

Comparison of the observed number of negative (A) and positive (B) co‐occurrences between pairwise species and the expected number (5th–95th quantile) under environmentally constrained models from forest structure (solid envelopes) or forest composition (dashed envelopes) environmental covariates.

Influence of species functional dissimilarity on the co‐occurrence strength of unconstrained models and environmentally constrained models generated by forest structure. The weighted Spearman's r of each observed co‐occurrence type is compared with those of the 5th–95th quantile ranges of distributions of the environmentally constrained models generated by forest structure (central panel). See similar results for forest composition (Appendix S1: Fig. S3). Top (negative co‐occurrence) and bottom (positive co‐occurrence) panels illustrate the observed relationship, from which the Spearman's r was calculated between the species dissimilarity and the co‐occurrence strength for the 200‐, 400‐, 900‐, and 3000‐m plots. The co‐occurrence strength was calculated as the difference between the observed and expected number of plots that the two species i and j co‐occur (Jijobs‐Jijexp; Veech 2014).

Significance of univariate relationships between positive species co‐occurrence strength and trait similarity. Levels of significance are shown for the environmentally constrained model at different spatial scales and are given for the forest structure and forest composition. Circle color corresponds to the component of the environmental conditions (forest structure and composition), and the circle size to the significance level of the relationship.

(A) Cluster dendrogram of overall vertebrate assemblage based on Jaccard distance of species presence/absence. (B) Schematic illustration of presumed interspecific interactions (commensalism and mutualism). Positive co‐occurrences between species pairwise are represented by red lines. We support that terrestrial species benefit by commensalism from feeding, foraging, and other behaviors of arboreal species. Solid and dashed lines represent positive co‐occurrences within species groups and between species groups, respectively. Find after full common names sorted by initial letters and corresponding scientific names: Amazonian brown brocket deer, Mazama nemorivaga (F. Cuvier, 1817); Black curassow, Crax alector (Linnaeus, 1766); Black spider monkey, Ateles paniscus (Linnaeus, 1758); Collared peccary, Pecari tajacu (Linnaeus, 1758); Common squirrel monkey, Saimiri sciureus (Linnaeus, 1758); Guianan brown capuchin, Sapajus [Cebus] apella (Linnaeus, 1758); Golden‐handed tamarin, Saguinus midas (Linnaeus, 1758); Great Tinamou, Tinamus major (Gmelin, 1789); Guianan weeper capuchin, Cebus olivaceus (Schomburgk, 1848); Grey‐winged trumpeter, Psophia crepitans (Linnaeus, 1758); Lowland tapir, Tapirus terrestris (Linnaeus, 1758); Little tinamous, Crypturellus spp.; Marail guan, Penelope marail (Müller, 1776); Marbled wood‐quail, Odontophorus gujanensis (Gmelin, 1789); Red acouchi, Myoprocta acouchy (Erxleben, 1777); Red brocket, Mazama americana (Erxleben, 1777); Red howler monkey, Alouatta macconnelli (Linnaeus, 1766); Red‐rumped agouti, Dasyprocta leporina (Linnaeus, 1758); Tayra, Eira barbara (Linnaeus, 1758); White‐faced saki, Pithecia pithecia (Linnaeus, 1766); Yellow‐footed tortoise, Geochelone denticulata (Linnaeus, 1766).

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Thomas Denis.Office National de la Chasse et de la Faune Sauvage, UMR EcoFoG (AgroParisTech, Cirad, CNRS, INRA, Université des Antilles, Université de Guyane), 97310, Kourou, French Guiana, France;Université de Guyane, UMR EcoFoG, 97310, Kourou, French Guiana, France.thomas.denis@ecofog.gf


Thomas Denis,Cécile Richard‐Hansen,Olivier Brunaux,Stéphane Guitet,Bruno Hérault. Birds of a feather flock together: Functionally similar vertebrates positively co‐occur in Guianan forests. Ecosphere ,Vol.10, Issue 3(2019)



[1] Erard, C., M. Théry, and D. Sabatier. 2007. Fruit characters in the diet of syntopic large frugivorous forest bird species in French Guiana. La Terre et la Vie: Revue d'Ecologie Appliquée 62:323–350.
[2] King, D. I., and J. H. Rappole. 2001. Mixed‐species bird flocks in dipterocarp forest of north‐central Burma (Myanmar). Ibis 143:380–390.
[3] Beaudrot, L., M. J. Struebig, E. Meijaard, S. van Balen, S. Husson, and A. J. Marshall. 2013. Co‐occurrence patterns of Bornean vertebrates suggest competitive exclusion is strongest among distantly related species. Oecologia 173:1053–1062.
[4] Reider, K. E., W. P. Carson, and M. A. Donnelly. 2013. Effects of collared peccary (Pecari tajacu) exclusion on leaf litter amphibians and reptiles in a Neotropical wet forest, Costa Rica. Biological Conservation 163:90–98.
[5] Wagner, F., B. Hérault, C. Stahl, D. Bonal, and V. Rossi. 2011. Modeling water availability for trees in tropical forests. Agricultural and Forest Meteorology 151:1202–1213.
[6] Ferry, B., and F. Morneau. 2010. Higher treefall rates on slopes and waterlogged soils result in lower stand biomass and productivity in a tropical rain forest. Journal of Ecology 98:106–116.
[7] Richard‐Hansen, C., G. Jaouen, T. Denis, O. Brunaux, E. Marcon, and S. Guitet. 2015. Landscape patterns influence communities of medium‐ to large‐bodied vertebrates in undisturbed terra firme forests of French Guiana. Journal of Tropical Ecology 31:423–436.
[8] Ringler, M., W. Hödl, and E. Ringler. 2015. Populations, pools, and peccaries: simulating the impact of ecosystem engineers on rainforest frogs. Behavioral Ecology 26:340–349.
[9] Forget, P.‐M., T. Milleron, F. Feer, O. Henry, and G. Dubost. 2000. Effects of dispersal pattern and mammalian herbivores on seedling recruitment for Virola michelii (Myristicaceae) in French Guiana. Biotropica 32:452–462.
[10] Ter Steege, H., D. Sabatier, H. Castellanos, T. Van Andel, J. Duivenvoorden, A. Adalardo de Oliveira, R. Ek, R. Lilwah, P. Maas, and S. Mori. 2000. An analysis of the floristic composition and diversity of Amazonian forests including those of the Guiana Shield. Journal of Tropical Ecology 16:801–828.
[11] Royan, A., S. J. Reynolds, D. M. Hannah, C. Prudhomme, D. G. Noble, and J. P. Sadler. 2016. Shared environmental responses drive co‐occurrence patterns in river bird communities. Ecography 39:733–742.
[12] Arsenault, R., and N. Owen‐Smith. 2002. Facilitation versus competition in grazing herbivore assemblages. Oikos 97:313–318.
[13] Voss, R. S., and L. H. Emmons. 1996. Mammalian diversity in Neotropical lowland rainforests: a preliminary assessment. Bulletin of the American Museum of Natural History 230:1–115.
[14] Arteaga, M. C., and E. M. Vintincinque. 2008. Influence of topography on the location and density of armadillo burrows (Dasypodidae: Xenarthra) in the Central Amazon, Brazil. Mammalian Biology 73:262–266.
[15] Terborgh, J. 1990. Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. American Journal of Primatology 21:87–100.
[16] Kraft, N. J. B., P. B. Adler, O. Godoy, E. James, S. Fuller, and J. M. Levine. 2015. Community assembly, coexistence, and the environmental filtering metaphor. Functional Ecology 29:592–599.
[17] Tabarelli, M., and C. A. Peres. 2002. Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: implications for forest regeneration. Biological Conservation 106:165–176.
[18] Luna‐Maira, L., G. Alarcon‐Nieto, T. Haugaasen, and D. M. Brooks. 2013. Habitat use and ecology of Wattled Curassows on islands in the lower Caquetá River, Colombia. Journal of Field Ornithology 84:23–31.
[19] Newton, P. N. 1989. Associations between Langur monkeys (Presbytis entellus) and Chital deer (Axis axis): Chance encounters or a mutualism? Ethology 83:89–120.
[20] Maestre, F. T., R. M. Callaway, F. Valladares, and C. J. Lortie. 2009. Refining the stress‐gradient hypothesis for competition and facilitation in plant communities. Journal of Ecology 97:199–205.
[21] Arita, H. T. 2016. Species co‐occurrence analysis: pairwise versus matrix‐level approaches. Global Ecology & Biogeography 25:1397–1400.
[22] Denis, T., C. Richard‐hansen, O. Brunaux, S. Guitet, and B. Hérault. 2017. Biological traits rather than environmental conditions shape detection probability curves of medium‐ and large‐sized vertebrates in Neotropical rainforests. Ecological Applications 27:1564–1577.
[23] Santamaria, M., and A. M. Franco. 2000. Frugivory of Salvin's curassow in a rainforest of the Columbian Amazon. Wilson Bulletin 112:473–481.
[24] Dickman, C. R. 1992. Commensal and mutualistic interaction among terrestrial vertebrates. Trends in Ecology and Evolution 7:194–197.
[25] Varzinczak, L. H., I. P. Bernardi, and F. C. Passos. 2016. Null model analysis on bat species co‐occurrence and nestedness patterns in a region of the Atlantic rainforest, Brazil. Mammalia 80:171–179.
[26] Veech, J. A. 2014. The pairwise approach to analysing species co‐occurrence. Journal of Biogeography 41:1029–1035.
[27] Veech, J. A. 2013. A probabilistic model for analysing species co‐occurrence. Global Ecology and Biogeography 22:252–260.
[28] Seppänen, J.‐T., J. T. Forsman, M. Mönkkönen, and R. L. Thomson. 2007. Social information use is a process across time, space, and ecology, reaching heterospecifics. Ecology 88:1622–1633.
[29] du Toit, J. T. 2003. Large herbivores and savanna heterogeneity. Pages 292–309 in , Kevin H. Rogers, and Harry C. Biggs, editors. The Kruger experience: ecology and management of Savanna heterogeneity. Island Press, Washington, D.C., USA.
[30] Sfenthourakis, S., E. Tzanatos, and S. Giokas. 2006. Species co‐occurrence: the case of congeneric species and a causal approach to patterns of species association. Global Ecology and Biogeography 15:39–49.
[31] van Roosmalen, M. G. M. 1985b. Habitat preferences, diet, feeding strategy and social organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Surinam. Acta Amazônica 15:7–238.
[32] Norconk, M. A. 1990. Introductory remarks: ecological and behavioral correlates of polyspecific primate troops. American Journal of Primatology 21:81–85.
[33] Odadi, W. O., M. K. Karachi, S. A. Abdulrazak, and T. P. Young. 2011. African wild ungulates compete with or facilitate cattle depending on season. Science 333:1753–1755.
[34] Haugaasen, T., and C. A. Peres. 2005. Tree phenology in adjacent Amazonian flooded and unflooded forests. Biotropica 37:620–630.
[35] Ollivier, M., C. Baraloto, and E. Marcon. 2007. A trait database for Guianan rainforest trees permits intra‐ and inter‐specific contrasts. Annals of Forest Science 64:781–786.
[36] Hutto, R. L. 1988. Foraging behavior patterns suggest a possible cost associated with participation in mixed‐species bird flocks. Oikos 51:79–83.
[37] Jaccard, P. 1901. Etude comparative de la distribution florale dans une portion des Alpes et des Jura. Bulletin de Société Vaudoise des Sciences Naturelles 37:547–579.
[38] van Roosmalen, M. G. M. 1985a. Fruits of Guianan flora. Institute of Systematic Botany, University of Utrecht, and Silvicultural Department of Wageningen Agricultural University, Utrecht, The Netherlands.
[39] Sridhar, H., et al. 2012. Positive relationships between association strength and phenotypic similarity characterize the assembly of mixed‐species bird flocks worldwide. American Naturalist 180:777–790.
[40] Torres, C. B. 1997. Densidades poblacionales de la comunidad de Crácidos en el Parque Na‐cional Manú (Perú). Pages 376–400 in , S. Beaujon, D. M. Brooks, A. J. Begazo, G. Sedaghatkish, and F. Olmos, editors. The Cracidae: their biology and conservation. Hancock House Publishers, Blaine, Washington, USA.
[41] Denis, T., B. Hérault, G. Jaouen, O. Brunaux, S. Guitet, and C. Richard‐Hansen. 2016. Black Curassow habitat relationships in terra firme forests of the Guiana Shield: a multiscale approach. Condor: Ornithological Applications 118:253–273.
[42] Skogland, T. 1991. What are the effects of predators on large ungulate populations? Oikos 61:401–411.
[43] Sólymos, P., S. M. Matsuoka, D. Stralberg, N. K. Barker, and E. M. Bayne. 2018. Phylogeny and species traits predict bird detectability. Ecography 41:1595–1603.
[44] Valiente‐Banuet, A., and M. Verdú. 2007. Facilitation can increase the phylogenetic diversity of plant communities. Ecology Letters 10:1029–1036.
[45] Denis, T., B. Hérault, O. Brunaux, S. Guitet, and C. Richard‐Hansen. 2018. Weak environmental controls on the composition and diversity of medium and large‐sized vertebrate assemblages in Neotropical rainforests of the Guiana Shield. Diversity and Distributions 24:1545–1559.
[46] Delor, C., et al. 2003. Transamazonian crustal growth and reworking as revealed by the 1:500,000‐scale geological map of French Guiana. Second edition. Bureau de Recherches Géologiques et Minières, Orléans, France.
[47] Cornillon, P.‐A., A. Guyader, F. Husson, N. Jégou, J. Josse, M. Kloareg, E. Matzner‐Løber, and L. Rouvière. 2012. R for statistics. Chapman & Hall/CRC Press, Boca Raton, Florida, USA.
[48] Palminteri, S., and C. A. Peres. 2012. Habitat selection and use of space by bald‐faced sakis (Pithecia irrorata) in southwestern Amazonia: lessons from a multiyear, multigroup Study. International Journal of Primatology 33:401–417.
[49] Peres, C. A., T. Emilio, J. Schietti, S. J. M. Desmoulière, and T. Levi. 2016. Dispersal limitation induces long‐term biomass collapse in overhunted Amazonian forests. Proceedings of the National Academy of Sciences of the United States of America 113:201516525.
[50] Peres‐Neto, P. R., J. D. Olden, and D. A. Jackson. 2001. Environmentally constrained null models: site suitability as occupancy criterion. Oikos 93:110–120.
[51] Guitet, S., B. Hérault, Q. Molto, O. Brunaux, and P. Couteron. 2015a. Spatial structure of above ground biomass limits accuracy of carbon mapping in rainforest but large scale forest inventories can help to overcome. PLoS ONE 10:e0138456.
[52] Stachowicz, J. J. 2001. Mutualism, facilitation, and the structure of ecological communities. BioScience 51:235–246.
[53] Guitet, S., R. Pélissier, O. Brunaux, G. Jaouen, and D. Sabatier. 2015b. Geomorphological land‐scape features explain floristic patterns in French Guiana rainforest. Biodiversity and Conservation 24:1215–1237.
[54] Peres‐Neto, P. R. 2004. Patterns in the co‐occurrence of fish species in streams: the role of site suitability, morphology and phylogeny versus species interactions. Oecologia 140:352–360.
[55] Stevenson, P. R., M. J. Quiiones, and J. A. Ahurnada. 2000. Influence of fruit availability on ecological overlap among four Neotropical primates at Tinigua National Park, Colombia. Biotropica 32:533–544.
[56] Guitet, S., et al. 2018. Disturbance regimes drive the diversity of regional floristic pools across Guianan rainforest landscapes. Scientific Reports 8:3872.
[57] Stensland, E., A. Angerbjörn, and P. Berggren. 2003. Mixed species groups in mammals. Mammal Review 33:205–223.
[58] Steen, D. A., et al. 2014. Snake co‐occurrence patterns are best explained by habitat and hypothesized effects of interspecific interactions. Journal of Animal Ecology 83:286–295.
[59] Guitet, S., D. Sabatier, O. Brunaux, B. Hérault, M. Aubry‐Kientz, J. Molino, and C. Baraloto. 2014. Estimating tropical tree diversity indices from forestry surveys: a method to integrate taxonomic uncertainty. Forest Ecology and Management 328:270–281.
[60] Chave, J., R. Condit, S. Lao, J. P. Caspersen, R. B. Foster, and S. P. Hubbell. 2003. Spatial and temporal variation of biomass in a tropical forest: results from a large census plot in Panama. Journal of Ecology 91:240–252.
[61] Cavender‐Bares, J., K. H. Kozak, P. V. A. Fine, and S. W. Kembel. 2009. The merging of community ecology and phylogenetic biology. Ecology Letters 12:693–715.
[62] Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18:119–125.
[63] Périquet, S., H. Fritz, and E. Revilla. 2015. The Lion King and the Hyaena Queen: large carnivore interactions and coexistence. Biological Reviews 90:1197–1214.