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Fruit–frugivore interactions in Amazonian seasonally flooded and unflooded forests

Published online by Cambridge University Press:  26 June 2014

Joseph E. Hawes  and
Carlos A. Peres
Joseph E. Hawes*
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
Carlos A. Peres
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
*
1Corresponding author. Current address: Coordenação de Botânica, Museu Paraense Emílio Goeldi, CP 399, CEP 66040-170 Belém, Pará, Brazil. Email: j.hawes@uea.ac.uk
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Abstract:

Constructing community fruit–frugivore networks has proved challenging in tropical forests to date, particularly in lowland Amazonia, which hosts the most diverse spectrum of frugivorous vertebrates and morphological fruit types worldwide. We assessed data on fruit resource production, frugivore assemblages and corresponding fruit–frugivore networks in two contrasting forest types along the Rio Juruá of western Brazilian Amazonia: seasonally flooded várzea (VZ) and unflooded terra firme forest (TF). Over 2 y we conducted monthly surveys of fruit patches and medium- to large-bodied vertebrate frugivores within three 100-ha plots (two TF, one VZ), supplemented by fruit surveys along 67 5-km transects distributed across two contiguous forest reserves (41 TF, 26 VZ). Observations of trophic interactions were supplemented by semi-structured interviews with experienced hunters and fishermen from 16 local communities. The resultant binary networks contained low proportions of all potential interactions (TF: 25.7%, VZ: 19.4%) between 36 functional groups of frugivores and 152 plant genera and, while we report significant heterogeneity in fruit resource use among broad frugivore guilds within each forest type, recursive partitioning analysis failed to clearly match differences in fruit selection to fruit traits. The annual flood pulse in várzea forests had an overriding influence on the species turnover of both fruit resources and frugivores between the two forest types, with higher-order effects on network structure.

Keywords

birdsBrazilcommunitydietfeeding ecologyfishnetworksprimatesterra firmevárzea
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 5 , September 2014 , pp. 381 - 399
Copyright
Copyright © Cambridge University Press 2014 

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References

LITERATURE CITED

ALVES-COSTA, C. P. & ETEROVICK, P. C. 2007. Seed dispersal services by coatis (Nasua nasua, Procyonidae) and their redundancy with other frugivores in southeastern Brazil. Acta Oecologica 32:77–92.CrossRefGoogle Scholar
AYRES, J. M. 1986. Uakaris and Amazonian flooded forest. PhD thesis, Cambridge University, Cambridge.Google Scholar
BALENSIEFER, D. C. & VOGT, R. C. 2006. Diet of Podocnemis unifilis (Testudines, Podocnemididae) during the dry deason in the Mamirauá Sustainable Development Reserve, Amazonas, Brazil. Chelonian Conservation and Biology 5:312–317.CrossRefGoogle Scholar
BASCOMPTE, J. & JORDANO, P. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics 38:567–593.CrossRefGoogle Scholar
BLÜTHGEN, N., MENZEL, F. & BLÜTHGEN, N. 2006. Measuring specialization in species interaction networks. BMC Ecology 6:9.CrossRefGoogle ScholarPubMed
BLÜTHGEN, N., MENZEL, F., HOVESTADT, T., FIALA, B. & BLÜTHGEN, N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17:341–346.CrossRefGoogle ScholarPubMed
BLÜTHGEN, N., FRÜND, J., VÁZQUEZ, D. P. & MENZEL, F. 2008. What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399.CrossRefGoogle ScholarPubMed
BODMER, R. E. 1990. Ungulate frugivores and the browser-grazer continuum. Oikos 57:319–325.CrossRefGoogle Scholar
BOLLEN, A., ELSACKER, L. VAN & GANZHORN, J. U. 2004. Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. Journal of Tropical Ecology 20:599–612.CrossRefGoogle Scholar
BOUBLI, J. P. 1999. Feeding ecology of black-headed uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil. International Journal of Primatology 20:719–749.CrossRefGoogle Scholar
BREIMAN, L., FRIEDMAN, J., OLSHEN, R. & STONE, C. 1984. Classification and regression trees. Chapman & Hall, New York. 368 pp.Google Scholar
CAMPBELL, D. G., DALY, D. C., PRANCE, G. T. & MACIEL, U. N. 1986. Quantitative ecological inventory of terra firme and várzea tropical forest on the Rio Xingu, Brazilian Amazon. Brittonia 38:369–393.CrossRefGoogle Scholar
CARLO, T. A. & YANG, S. 2011. Network models of frugivory and seed dispersal: challenges and opportunities. Acta Oecologica 37:624–619.CrossRefGoogle Scholar
CARLO, T. A., COLLAZO, J. A. & GROOM, M. J. 2003. Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal. Oecologia 134:119–131.CrossRefGoogle Scholar
CASPER, B. B., HEARD, S. B. & APANIUS, V. 1992. Ecological correlates of single-seededness in a woody tropical flora. Oecologia 90:212–217.CrossRefGoogle Scholar
CORNEJO, F. & JANOVEC, J. 2010. Seeds of Amazonian plants. Princeton University Press, Princeton. 155 pp.CrossRefGoogle Scholar
CORREA, S. B., WINEMILLER, K. O., LÓPEZ-FERNANDEZ, H. & GALETTI, M. 2007. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience 57:748–756.CrossRefGoogle Scholar
DONATTI, C. I., GUIMARÃES, P. R., GALETTI, M., PIZO, M. A., MARQUITTI, F. M. D. & DIRZO, R. 2011. Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecology Letters 14:773–781.CrossRefGoogle ScholarPubMed
FISCHER, K. E. & CHAPMAN, C. A. 1993. Frugivores and fruit syndromes: differences in patterns at the genus and species level. Oikos 66:472–482.CrossRefGoogle Scholar
FLEMING, T. H. & KRESS, W. J. 2011. A brief history of fruits and frugivores. Acta Oecologica 37: 521–530.CrossRefGoogle Scholar
FLEMING, T. H., BREITWISCH, R. & WHITESIDES, G. H. 1987. Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecology and Systematics 18:91–109.CrossRefGoogle Scholar
FLÖRCHINGER, M., BRAUN, J., BÖHNING-GAESE, K. & SCHAEFER, H. M. 2010. Fruit size, crop mass, and plant height explain differential fruit choice of primates and birds. Oecologia 164:151–161.CrossRefGoogle ScholarPubMed
FRAGOSO, J. M. V. 1998. Home range and movement patterns of white-lipped peccary (Tayassu pecari) herds in the northern Brazilian Amazon. Biotropica 30:458–469.CrossRefGoogle Scholar
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. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate. Oecologia 65:324–337.CrossRefGoogle Scholar
GENTRY, A. H. 1996. A field guide to the families and genera of woody plants of northwest South America (Columbia, Ecuador, Peru). University of Chicago Press, Chicago. 895 pp.Google Scholar
GOULDING, M. 1980. The fishes and the forest: explorations in Amazonian natural history. University of California Press, Berkeley. 280 pp.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2005a. Tree phenology in adjacent Amazonian flooded and unflooded forests. Biotropica 37:620–630.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2005b. Mammal assemblage structure in Amazonian flooded and unflooded forests. Journal of Tropical Ecology 21:133–145.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2006. Floristic, edaphic and structural characteristics of flooded and unflooded forests in the lower Rio Purús region of central Amazonia, Brazil. Acta Amazonica 36:25–35.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2007. Vertebrate responses to fruit production in Amazonian flooded and unflooded forests. Biodiversity and Conservation 16:4165–4190.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2008. Population abundance and biomass of large-bodied birds in Amazonian flooded and unflooded forests. Bird Conservation International 18:87–101.CrossRefGoogle Scholar
HAWES, J. E. 2012. Fruits and frugivory in neotropical primates and in Amazonian flooded and unflooded forests. PhD thesis, University of East Anglia, Norwich.Google Scholar
HAWES, J. E. & PERES, C. A. 2013. Ecological correlates of trophic status and frugivory in neotropical primates. Oikos 123:365–377.CrossRefGoogle Scholar
HAWES, J. E., PERES, C. A., RILEY, L. B. & HESS, L. L. 2012. Landscape-scale variation in structure and biomass of Amazonian seasonally flooded and unflooded forests. Forest Ecology and Management 281:163–176.CrossRefGoogle Scholar
HERRERA, C. M. 1998. Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecological Monographs 68:511–538.Google Scholar
HOORN, C. & WESSELINGH, F. 2010. Amazonia, landscape and species evolution: a look into the past. Wiley-Blackwell, Chichester. 464 pp.Google Scholar
HORN, M. H., CORREA, S. B., PAROLIN, P., POLLUX, B. J. A., ANDERSON, J. T., LUCAS, C., WIDMANN, P., TJIU, A., GALETTI, M. & GOULDING, M. 2011. Seed dispersal by fishes in tropical and temperate fresh waters: the growing evidence. Acta Oecologica 37: 561–577.CrossRefGoogle Scholar
JANSON, C. H. 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219:187–189.CrossRefGoogle Scholar
JORDANO, P. 1995. Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. American Naturalist 145:163–191.CrossRefGoogle Scholar
JORDANO, P., FORGET, P.-M., LAMBERT, J. E., BÖHNING-GAESE, K., TRAVESET, A. & WRIGHT, S. J. 2011. Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7:321–323.CrossRefGoogle ScholarPubMed
JUNK, W. J. 1989. Flood tolerance and tree distribution in central Amazonian floodplains. Pp. 47–64 in Holm-Nielsen, L. B., Nielsen, I. C. & Balslev, H. (eds.). Tropical forests: botanical dynamics, speciation, and diversity. Academic Press, New York.CrossRefGoogle Scholar
JUNK, W. J. 1997. General aspects of floodplain ecology with special reference to Amazonian floodplains. Pp. 3–20 in Junk, W. J. (ed.). The central Amazon floodplain: ecology of a pulsing system. Ecological Studies 126. Springer-Verlag, Berlin.CrossRefGoogle Scholar
KAYS, R. W. 1999. Food preferences of kinkajous (Potos flavus): a frugivorous carnivore. Journal of Mammalogy 80:589–599.CrossRefGoogle Scholar
KELLY, C. K. 1995. Seed size in tropical trees: a comparative study of factors affecting seed size in Peruvian angiosperms. Oecologia 102:377–388.CrossRefGoogle Scholar
KISSLING, W. D., BÖHNING-GAESE, K. & JETZ, W. 2009. The global distribution of frugivory in birds. Global Ecology and Biogeography 18:150–162.CrossRefGoogle Scholar
KITAMURA, S., YUMOTO, T., POONSWAD, P., CHAUILUA, P., PLONGMAI, K., MARUHASHI, T. & NOMA, N. 2002. Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia 133:559–572.CrossRefGoogle Scholar
LINK, A. & STEVENSON, P. R. 2004. Fruit dispersal syndromes in animal disseminated plants at Tinigua National Park, Colombia. Revista Chilena de Historia Natural 77:319–334.CrossRefGoogle Scholar
LOH, W.-Y. 2011. Classification and regression trees. Wiley Interdisciplinary Reviews: Data Mining and Knowledge Discovery 1:14–23.Google Scholar
LOMÁSCOLO, S. B. & SCHAEFER, H. M. 2010. Signal convergence in fruits: a result of selection by frugivores? Journal of Evolutionary Biology 23:614–624.CrossRefGoogle ScholarPubMed
MALCOLM, J. R., PATTON, J. L. & DA SILVA, M. N. F. 2005. Small mammal communities in upland and floodplain forests along an Amazonian white water river. Pp. 335–380 in Lacey, E. I. & Myers, P. (eds.). Mammalian diversification: from chromosomes to phylogeography (a celebration of the career of James L. Patton). University of California, Berkeley.Google Scholar
MELLO, M. A. R., MARQUITTI, F. M. D., GUIMARÃES, P. R. JR., KALKO, E. K. V., JORDANO, P. & DE AGUIAR, M. A. M. 2011. The modularity of seed dispersal: differences in structure and robustness between bat- and bird-fruit networks. Oecologia 167:131–140.CrossRefGoogle ScholarPubMed
MUSCARELLA, R. & FLEMING, T. H. 2007. The role of frugivorous bats in tropical forest succession. Biological Reviews 82:573–590.CrossRefGoogle ScholarPubMed
OLESEN, J. M., BASCOMPTE, J., DUPONT, Y. L., ELBERLING, H., RASMUSSEN, C. & JORDANO, P. 2011. Missing and forbidden links in mutualistic networks. Proceedings of the Royal Society B: Biological Sciences 278:725–732.CrossRefGoogle ScholarPubMed
PAROLIN, P., FERREIRA, L. V., ALBERNAZ, A. L. K. M. & ALMEIDA, S. S. 2004. Tree species distribution in várzea forests of Brazilian Amazonia. Folia Geobotanica 39:371–383.CrossRefGoogle Scholar
PAROLIN, P., WITTMANN, F. & SCHÖNGART, J. 2010. Tree phenology in Amazonian floodplain forests. Pp. 105–126 in Junk, W., Piedade, M., Wittmann, F., Schöngart, J. & Parolin, P. (eds.). Amazonian floodplain forests: ecophysiology, biodiversity and sustainable management. Springer, Berlin.CrossRefGoogle Scholar
PATTON, J. L., DA SILVA, M. N. F. & MALCOM, J. R. 2000. Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History 244:1–306.2.0.CO;2>CrossRefGoogle Scholar
PERES, C. A. 1996. Population status of white-lipped Tayassu pecari and collared peccaries T. tajacu in hunted and unhunted Amazonian forests. Biological Conservation 77:115–123.CrossRefGoogle Scholar
PERES, C. A. 1997. Primate community structure at twenty western Amazonian flooded and unflooded forests. Journal of Tropical Ecology 13:381–405.CrossRefGoogle Scholar
PERES, C. A. 1999. Nonvolant mammal community structure in different Amazonian forest types. Pp. 564–581 in Eisenberg, J. F. & Redford, K. H. (eds.). Mammals of the neotropics: the central neotropics. University of Chicago Press, Chicago.Google Scholar
PERES, C. A. & CUNHA, A. 2011. Line-transect censuses of large-bodied tropical forest vertebrates: a handbook. Wildlife Conservation Society, Brazilia.Google Scholar
PERES, C. & VAN ROOSMALEN, M. G. M. 2002. Primate frugivory in two species-rich Neotropical forests: implications for the demography of large-seeded plants in overhunted areas. Pp. 407–422 in Levey, D. J., Silva, W. R. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford.Google Scholar
PETERSON, D. 2010. Quantitative ethnobotany of forest dwellers: drivers of congruence in vernacular nomenclature of Amazonian trees. MSc dissertation, University of East Anglia, Norwich.Google Scholar
RAY, J. & SUNQUIST, M. E. 2001. Trophic relations in a community of African rainforest carnivores. Oecologia 127:395–408.CrossRefGoogle Scholar
RIBEIRO, J. E. L. DA S., HOPKINS, M. J. G., VICENTINI, A., SOTHERS, C. A., COSTA, M. A. DA S., BRITO, J. M. DE, SOUZA, M. A. D. DE, MARTINS, L. H. P., LOHMAN, L. G., ASSUNÇÃO, P. A. C. L., PEREIRA, E. DA C., SILVA, C. F. DA, MESQUITA, M. R. & PROCÓPIO, L. C. 1999. Flora da Reserva Ducke: guia de identificacao das plantas vasculares de uma floresta de terra-firme na Amazónia central. INPA-DFID, Manaus. 799 pp.Google Scholar
SCELZA, G. C. 2008. Desobriga: o movimento de contra-opressão ao sistema dos seringais no Médio Juruá – AM (1970–2008). MSc dissertation, Universidade Federal do Rio de Janeiro, Rio de Janeiro.Google Scholar
SCHLEUNING, M., BLÜTHGEN, N., FLÖRCHINGER, M., BRAUN, J., SCHAEFER, H. M. & BÖHNING-GAESE, K. 2011. Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 92:26–36.CrossRefGoogle Scholar
SCHLEUNING, M., FRÜND, J., KLEIN, A.-M., ABRAHAMCZYK, S., ALARCÓN, R., ALBRECHT, M., ANDERSSON, G. K. S., BAZARIAN, S., BÖHNING-GAESE, K., BOMMARCO, R., DALSGAARD, B., DEHLING, D. M., GOTLIEB, A., HAGEN, M., HICKLER, T., HOLZSCHUH, A., KAISER-BUNBURY, C. N., KREFT, H., MORRIS, R. J., SANDEL, B., SUTHERLAND, W. J., SVENNING, J.-C., TSCHARNTKE, T., WATTS, S., WEINER, C. N., WERNER, M., WILLIAMS, N. M., WINQVIST, C., DORMANN, C. F. & BLÜTHGEN, N. 2012. Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology 22:1925–31.CrossRefGoogle ScholarPubMed
SNOW, D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1–14.CrossRefGoogle Scholar
TER STEEGE, H. & HAMMOND, D. S. 2001. Character convergence, diversity, and disturbance in tropical rain forest in Guyana. Ecology 82:3197–3212.CrossRefGoogle Scholar
TER STEEGE, H., PITMAN, N. C. A., SABATIER, D., BARALOTO, C., SALOMAO, R. P., GUEVARA, J. E., PHILLIPS, O. L., CASTILHO, C. V., MAGNUSSON, W. E., MOLINO, J.-F., MONTEAGUDO, A., NUNEZ VARGAS, P., MONTERO, J. C., FELDPAUSCH, T. R., CORONADO, E. N. H., KILLEEN, T. J., MOSTACEDO, B., VASQUEZ, R., ASSIS, R. L., TERBORGH, J.et al. 2013. Hyperdominance in the Amazonian tree flora. Science 342:1243092.CrossRefGoogle ScholarPubMed
VALIDO, A. & OLESEN, J. M. 2007. The importance of lizards as seed dispersers. Pp. 124–147 in Dennis, A. J., Schupp, E. W., Green, R. J. & Westcott, D. W. (eds.). Seed dispersal: theory and its application in a changing world. CAB International, Wallingford.CrossRefGoogle Scholar
VAN DER PIJL, L. 1982. Principles of dispersal in higher plants. (Third edition). Springer-Verlag, Berlin. 214 pp.CrossRefGoogle Scholar
VAN ROOSMALEN, M. G. M. 1985. Fruits of the Guianan flora. Institute of Systematic Botany, Utrecht University, Utrecht. 483 pp.Google Scholar
VOIGT, F. A., BLEHER, B., FIETZ, J., GANZHORN, J. U., SCHWAB, D. & BÖHNING-GAESE, K. 2004. A comparison of morphological and chemical fruit traits between two sites with different frugivore assemblages. Oecologia 141:94–104.CrossRefGoogle ScholarPubMed
WHEELWRIGHT, N. T. 1985. Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818.CrossRefGoogle Scholar
WITTMANN, F., SCHÖNGART, J., MONTERO, J. C., MOTZER, T., JUNK, W. J., PIEDADE, M. T. F., QUEIROZ, H. L. & WORBES, M. 2006. Tree species composition and diversity gradients in white-water forests across the Amazon basin. Journal of Biogeography 33:1334–1347.CrossRefGoogle Scholar
WITTMANN, F., SCHÖNGART, J., DE BRITO, J. M., WITTMANN, A. DE O., PIEDADE, M. T. F., PAROLIN, P., JUNK, W. J. & GUILLAUMET, J.-L. 2010a. Manual of trees in central Amazonian várzea floodplains: taxonomy, ecology, and use. Editora INPA, Manaus. 298 pp.Google Scholar
WITTMANN, F., SCHÖNGART, J. & JUNK, W. J. 2010b. Phytogeography, species diversity, community structure and dynamics of central Amazonian floodplain forests. Pp. 61–102 in Junk, W., Piedade, M., Wittmann, F., Schöngart, J. & Parolin, P. (eds.). Amazonian floodplain forests: ecophysiology, biodiversity and sustainable management. Springer, Berlin.CrossRefGoogle Scholar