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Spatial and temporal variation in community composition of herbivorous insects on Neoboutonia macrocalyx in a primary tropical rain forest

Published online by Cambridge University Press:  02 April 2013

Kaisa Heimonen ,
Jeremiah S. Lwanga ,
Marko Mutanen ,
Tommi Nyman  and
Heikki Roininen
Kaisa Heimonen*
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, 80101 Joensuu, Finland
Jeremiah S. Lwanga
Affiliation:
Department of Forestry, Biodiversity and Tourism, Makerere University, P. O. Box 7062, Kampala, Uganda
Marko Mutanen
Affiliation:
Department of Biology, University of Oulu, P.O. Box 3000, 90014 Oulu, Finland
Tommi Nyman
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, 80101 Joensuu, Finland Institute for Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland
Heikki Roininen
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, 80101 Joensuu, Finland
*
1Corresponding author. Email: kaisa.heimonen@uef.fi
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Abstract:

Spatial and temporal variation of tropical insect communities has rarely been studied, although such variation influences estimates of global species richness. Therefore, we compared spatial and temporal variation of herbivorous insect communities on Neoboutonia macrocalyx trees among seven sites over 1 y in a primary tropical rain forest in Kibale National Park, Uganda. The distance between the study sites varied from 4.8 to 31.2 km and altitudinal differences ranged from 20 to 242 m. Permutational multivariate analysis of variance (PERMANOVA) revealed significant spatial changes in community composition of the herbivorous insects and study sites differed also in insect abundance (6.9–26.2 individuals m−2 of leaf area). This is likely to be caused by differences in vegetation, altitude and microclimate among the study sites. The similarity of insect species composition was negatively correlated with geographic and altitudinal distances among sites and positively correlated with the similarity of tree community composition. Species richness varied significantly between sampling dates, ranging from 33 to 41 species. Also community compositions changed between sampling dates, which likely follows from marked seasonal changes in climate and the phenology of other host plants used by the generalist insect species also living on Neoboutonia macrocalyx. In general our study supports the idea of high variability of herbivorous insect communities in primary rain forests even at a small spatial scale. This should be considered when estimations of insect biodiversity are made.

Keywords

Afrotropical rain forestinsect communitiesKibale National ParkNeoboutonia macrocalyxspecies compositionUganda
Type
Research Article
Information
Journal of Tropical Ecology , Volume 29 , Issue 3 , May 2013 , pp. 229 - 241
Copyright
Copyright © Cambridge University Press 2013 

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References

LITERATURE CITED

BAIRSTOW, K. A., CLARKE, K. L., MCGEOCH, M. A. & ANDREW, N. R. 2010. Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate. Oecologia 163:437–448.CrossRefGoogle ScholarPubMed
BARTLETT, R., PICKERING, J., GAULD, I. & WINDSOR, D. 1999. Estimating global biodiversity: tropical beetles and wasps send different signals. Ecological Entomology 24:118–121.CrossRefGoogle Scholar
BASSET, Y. 1991. The seasonality of arboreal arthropods foraging within an Australian rainforest tree. Ecological Entomology 16:265–278.CrossRefGoogle Scholar
BASSET, Y., SAMUELSON, G. A., ALLISON, A. & MILLER, S. E. 1996. How many species of host-specific insects feed on a species of tropical tree? Biological Journal of the Linnean Society 59:201–216.CrossRefGoogle Scholar
BASSET, Y., CIZEK, L., CUÉNOUD, P., DIDHAM, R. K., GUILHAUMON, F., MISSA, O., NOVOTNY, V., ØDEGAARD, F., ROSLIN, T., SCHMIDL, J., TISCHECHKIN, A. K., WINCHESTER, N. N., ROUBIK, D. W., ABERLENC, H-P., BAIL, J., BARRIOS, H., BRIDLE, J. R., CASTAÑO-MENESES, G., CORBARA, B., CURLETTI, G., DUARTE, DA, ROCHA, W., DE BAKKER, D., DELABIE, J. H. C., DEJEAN, A., FAGAN, L. L., FLOREN, A., KITCHING, R. L., MEDIANERO, E., MILLER, S. E., GAMA, DE, OLIVEIRA, E., ORIVEL, J., POLLET, M., RAPP, M., RIBEIRO, S. P., ROISIN, Y., SCHMIDT, J. B., SØRENSEN, L. & LEPONCE, M. 2012. Arthropod diversity in a tropical forest. Science 338: 1481–1484.CrossRefGoogle Scholar
BREHM, G., HOMEIER, J. & FIEDLER, K. 2003. Beta diversity of geometrid moths (Lepidoptera: Geometridae) in an Andean montane rainforest. Diversity and Distributions 9:351–366.CrossRefGoogle Scholar
CHAPMAN, C. A., CHAPMAN, L. J., WRANGHAM, R., ISABIRYE-BASUTA, G. & BEN-DAVID, K. 1997. Spatial and temporal variability in the structure of a tropical forest. African Journal of Ecology 35:287–302.CrossRefGoogle Scholar
CHAPMAN, C. A., CHAPMAN, L. J., KAUFMAN, L. & ZANNE, A. 1999. Potential causes of arrested succession in Kibale National Park, Uganda: growth and mortality of seedlings. African Journal of Ecology 37:81–92.CrossRefGoogle Scholar
CHAPMAN, C. A., CHAPMAN, L. J., STRUHSAKER, T. T., ZANNE, A. E., CLARK, C. J. & POULSEN, J. R. 2005. A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21:31–45.CrossRefGoogle Scholar
CLARKE, K. R. & GORLEY, R. N. 2006. PRIMER v6: User manual/tutorial. PRIMER-E Ltd, Plymouth. 190 pp.Google Scholar
CLEARY, D. F. R. & GENNER, M. J. 2006. Diversity patterns of Bornean butterfly assemblages. Biodiversity and Conservation 15: 517–538.CrossRefGoogle Scholar
CONDIT, R., PITMAN, N., LEIGH, E. G., CHAVE, J., TERBORGH, J. & FOSTER, R. B. 2002. Beta-diversity in tropical forest trees. Science 295:666–669.CrossRefGoogle ScholarPubMed
CORDS, M. 1990. Mixed-species associations of East African guenons: general patterns or specific examples? American Journal of Primatology 21:101–114.CrossRefGoogle ScholarPubMed
CRIST, T. O., PRADHAN-DEVARE, S. V. & SUMMERVILLE, K. S. 2006. Spatial variation in insect community and species responses to habitat loss and plant community composition. Oecologia 147:510–521.CrossRefGoogle ScholarPubMed
DALBEM, R. V. & MENDONÇA, M. DE S. 2006. Diversity of galling and host plants in a subtropical forest of Porto Alegre, Southern Brazil. Neotropical Entomology 35:616–624.CrossRefGoogle Scholar
DAVIES, J. G., STORK, N. E., BRENDELL, M. J. D. & HINE, S. J. 1997. Beetle species diversity and faunal similarity in Venezuelan rainforest tree canopies. Pp. 85–103 in Stork, N. E., Adis, J. & Didham, R. K. (eds.). Canopy arthropods. Chapman & Hall, London. 567 pp.Google Scholar
DENNO, R. F., LEWIS, D. & GRATTON, C. 2005. Spatial variation in the relative strength of top-down and bottom-up forces: causes and consequences for phytophagous insect populations. Annales Zoologici Fennici 42:295–311.Google Scholar
DEVRIES, P. J., MURRAY, D. & LANDE, R. 1997. Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in an Ecuadorian rainforest. Biological Journal of the Linnean Society 62:343–364.CrossRefGoogle Scholar
DEVRIES, P. J., ALEXANDER, L. G., CHACON, I. A. & FORDYCE, J. A. 2012. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. Journal of Animal Ecology 81:472–482.CrossRefGoogle ScholarPubMed
DYER, L. A., SINGER, M. S., LILL, J. T., STIREMAN, J. O., GENTRY, G. L., MARQUIS, R. J., RICKLEFS, R. E., GREENEY, H. F., WAGNER, D. L., MORAIS, H. C., DINIZ, I. R., KURSAR, T. A. & COLEY, P. D. 2007. Host specificity of Lepidoptera in tropical and temperate forests. Nature 448:696–700.CrossRefGoogle ScholarPubMed
ERWIN, T. L. 1982. Tropical forests: their richness in Coleoptera and other arthropod species. The Coleopterists’ Bulletin 36:74–75.Google Scholar
ERWIN, T. L. 1991. How many species are there?: revisited. Conservation Biology 5:330–333.CrossRefGoogle Scholar
ERWIN, T. L., PIMIENTA, M. C., MURILLO, O. E. & ASCHERO, V. 2005. Mapping patterns of β–diversity of beetles across the western Amazon basin: a preliminary case for improving inventory methods and conservation strategies. Proceedings of the California Academy of Sciences 56:72–85.Google Scholar
FONSECA, C. R. 2009. The silent mass extinction of insect herbivores in biodiversity hotspots. Conservation Biology 23:1507–1515.CrossRefGoogle ScholarPubMed
GASTON, K. J. & GAULD, I. D. 1993. How many species of pimplines (Hymenoptera: Ichneumonidae) are there in Costa Rica? Journal of Tropical Ecology 9:491–499.CrossRefGoogle Scholar
GOTELLI, N. J. & COLWELL, R. K. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4:379–391.CrossRefGoogle Scholar
GRØTAN, V., LANDE, R., ENGEN, S., SÆTHER, B.-E. & DEVRIES, P. J. 2012. Seasonal cycles of species diversity and similarity in a tropical butterfly community. Journal of Animal Ecology 81:714–723.CrossRefGoogle Scholar
HAMILTON, A. C. 1991. A field guide to Uganda forest trees. Makerere University Printery, Kampala. 280 pp.Google Scholar
HEBERT, P. D. N., CYWINSKA, A., BALL, S. L. & DEWAARD, J. R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270:313–321.CrossRefGoogle ScholarPubMed
HOLLOWAY, J. D. 1994. The moths of Borneo: family Geometridae, subfamily Ennominae. Malayan Nature Journal 47:1–309.Google Scholar
HORNER-DEVINE, M. C., DAILY, G. C., EHRLICH, P. R. & BOGGS, C. L. 2003. Countryside biogeography of tropical butterflies. Conservation Biology 17:168–177.CrossRefGoogle Scholar
HOWARD, P., DAVENPORT, T. & MATTHEWS, T. 1996. Kibale National Park, Biodiversity Report. Forest Department, Kampala, Uganda. 115 pp.Google Scholar
INTACHAT, J., HOLLOWAY, J. D. & STAINES, H. 2001. Effects of weather and phenology on the abundance and diversity of geometroid moths in a natural Malaysian tropical rain forest. Journal of Tropical Ecology 17:411–429.CrossRefGoogle Scholar
KALEMA, J. & BEENTJE, H. 2012. Conservation checklist of the trees of Uganda. Royal Botanical Gardens, Kew. 235 pp.Google Scholar
KASENENE, J. M. & ROININEN, H. 1999. Seasonality of insect herbivory on the leaves of Neoboutonia macrocalyx in the Kibale National Park, Uganda. African Journal of Ecology 37:61–68.CrossRefGoogle Scholar
KOCHUMMEN, K. M., LAFRANKIE, J. V. & MANOKARAN, N. 1992. Diversity of trees and shrubs in Malaya at regional and local level. Malayan Nature Journal 45:545–554.Google Scholar
LOPEZ-VAAMONDE, C., GODFRAY, C. J. & COOK, J. M. 2003. Evolutionary dynamics of host-plant use in a genus of leaf-mining moths. Evolution 57:1804–1821.Google Scholar
LOVETT, J. C., RUFFO, C. K., GEREAU, R. E. & TAPLIN, J. R. D. 2006. Field guide to the moist forest trees of Tanzania. York Publishing Services Ltd, York. 303 pp.Google Scholar
LUCKY, A., ERWIN, T. L. & WITMAN, J. D. 2002. Temporal and spatial diversity and distribution of arboreal Carabidae (Coleoptera) in a western Amazonian rain forest. Biotropica 34:376–386.CrossRefGoogle Scholar
MOLLEMAN, F., KOP, A., BRAKEFIELD, P. M., DE VRIES, P. J. & ZWAAN, B. J. 2006. Vertical and temporal patterns of biodiversity of fruit-feeding butterflies in a tropical forest in Uganda. Biodiversity and Conservation 15:93–107.CrossRefGoogle Scholar
NOVOTNY, V. & BASSET, Y. 2000. Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89:564–572.CrossRefGoogle Scholar
NOVOTNY, V. & WEIBLEN, G. D. 2005. From communities to continents: beta diversity of herbivorous insects. Annales Zoologici Fennici 42:463–475.Google Scholar
NOVOTNY, V., BASSET, Y., MILLER, S. E., WEIBLEN, G. D., BREMER, B., CIZEK, L. & DROZD, P. 2002a. Low host specificity of herbivorous insects in a tropical forest. Nature 416:841–844.CrossRefGoogle Scholar
NOVOTNY, V., BASSET, Y., MILLER, S. E., DROZD, P. & CIZEK, L. 2002b. Host specialization of leaf-chewing insects in a New Guinea rainforest. Journal of Animal Ecology 71:400–412.CrossRefGoogle Scholar
NOVOTNY, V., MILLER, S. E., BASSET, Y., CIZEK, L., DROZD, P., DARROW, K. & LEPS, J. 2002c. Predictably simple: assemblages of caterpillars (Lepidoptera) feeding on rainforest trees in Papua New Guinea. Proceedings of the Royal Society of London B 269:2337–2344.CrossRefGoogle ScholarPubMed
NOVOTNY, V., MILLER, S. E., BASSET, Y., CIZEK, L., DARROW, K., KAUPA, B., KUA, J. & WEIBLEN, G. D. 2005. An altitudinal comparison of caterpillar (Lepidoptera) assemblages on Ficus trees in Papua New Guinea. Journal of Biogeography 32:1303–1314.CrossRefGoogle Scholar
NOVOTNY, V., MILLER, S. E., HULCR, J., DREW, R. A. I., BASSET, Y., JANDA, M., SETLIFF, G. P., DARROW, K., STEWART, A. J. A., AUGA, J., ISUA, B., MOLEM, K., MANUMBOR, M., TAMTIAI, E., MOGIA, M. & WEIBLEN, G. D. 2007. Low beta diversity of herbivorous insects in tropical forests. Nature 448:692–695.CrossRefGoogle ScholarPubMed
NUMMELIN, M. 1989. Seasonality and effects of forestry practices on forest floor arthropods in the Kibale Forest, Uganda. Fauna Norvegica Ser. B 36:17–25.Google Scholar
ØDEGAARD, F., DISERUD, O. H., ENGEN, S. & AAGAARD, K. 2000. The magnitude of local host specificity for phytophagous insects and its implications for estimates of global species richness. Conservation Biology 14:1182–1186.CrossRefGoogle Scholar
PIMM, S. L. & RAVEN, P. 2000. Extinction by numbers. Nature 403:843–845.CrossRefGoogle ScholarPubMed
PITMAN, N. C. A., TERBORGH, J. W., SILMAN, M. R. & NUÑEZ, P. 1999. Tree species distributions in an upper Amazonian forest. Ecology 80:2651–2661.CrossRefGoogle Scholar
PRICE, P. W. 2002. Species interactions and the evolution of biodiversity. Pp. 3–26 in Herrera, C. M. & Pellmyr, O. (eds.). Plant–animal interactions: an evolutionary approach. Blackwell Science, Oxford. 313 pp.Google Scholar
RATNASINGHAM, S. & HEBERT, P. D. N. 2007. BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7:355–364.CrossRefGoogle ScholarPubMed
ROSENZWEIG, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge. 460 pp.CrossRefGoogle Scholar
SAVILAAKSO, S. 2009. The influence of disturbance on lepidopteran larvae and their seasonality on a constant resource – implications for conservation. Ph.D. dissertation, University of Joensuu, Joensuu.Google Scholar
SAVILAAKSO, S., KOIVISTO, J., VETELI, T. O. & ROININEN, H. 2009. Microclimate and tree community linked to differences in lepidopteran larval communities between forest fragments and continuous forest. Diversity and Distributions 15:356–365.CrossRefGoogle Scholar
SKIPPARI, S., VETELI, T. O., KASENENE, J., NIEMELÄ, P. & ROININEN, H. 2009. High temporal variation in the assemblage on lepidopteran larvae on a constant resource. African Journal of Ecology 47:537–545.CrossRefGoogle Scholar
STEVENS, G. C. 1989. The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist 133:240–256.CrossRefGoogle Scholar
STRUHSAKER, T. T. 1975. The Red Colobus Monkey. University of Chicago Press, Chicago. 311 pp.Google Scholar
STRUHSAKER, T. T. 1997. Ecology of an African rainforest: logging in Kibale and the conflict between conservation and exploitation. University Press of Florida, Gainesville. 456 pp.Google Scholar
SUMMERVILLE, K. S. & CRIST, T. O. 2003. Determinants of lepidopteran community composition and species diversity in eastern deciduous forests: roles of season, eco-region and patch size. Oikos 100:134–148.CrossRefGoogle Scholar
SUMMERVILLE, K. S., BOULWARE, M. J., VEECH, J. A. & CRIST, T. O. 2003. Spatial variation in species diversity and composition of forest Lepidoptera in eastern deciduous forests of North America. Conservation Biology 17:1045–1057.CrossRefGoogle Scholar
TAMURA, K., PETERSON, D., PETERSON, N., STECHER, G., NEI, M., & KUMAR, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731–2739.CrossRefGoogle ScholarPubMed
THOMAS, C. D. 1990. Fewer species. Nature 347:237.CrossRefGoogle Scholar
UEHARA-PRADO, M., BROWN, K. S. & FREITAS, A. V. L. 2007. Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic forest: comparison between a fragmented and a continuous landscape. Global Ecology and Biogeography 16:43–54.CrossRefGoogle Scholar
VALTONEN, A., MOLLEMAN, F., CHAPMAN, C. A., CAREY, J. R., AYRES, M. P. & ROININEN, H. In press. Tropical phenology: bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage. Ecosphere.Google Scholar
WHITHAM, T. G., BAILEY, J. K., SCHWEITZER, J. A., SHUSTER, S. M., BANGERT, R. K., LEROY, C. J., LONSDORF, E. V., ALLAN, G. J., DIFAZIO, S. P., POTTS, B. M., FISCHER, D. G., GEHRING, C. A., LINDROTH, R. L., MARKS, J. C., HART, S. C., WIMP, G. M. & WOOLEY, S. C. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nature 7:510–523.Google ScholarPubMed
WOLDA, H. 1992. Trends in abundance of tropical forest insects. Oecologia 89:47–52.CrossRefGoogle ScholarPubMed
YAMAMOTO, N., YOKOYAMA, J. & KAWATA, M. 2007. Relative resource abundance explains butterfly biodiversity in island communities. Proceedings of the National Academy of Sciences USA 104:10524–10529.CrossRefGoogle ScholarPubMed