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Bee (Hymenoptera: Apoidea) diversity within apple orchards and old fields in the Annapolis Valley, Nova Scotia, Canada

Published online by Cambridge University Press:  13 December 2012

Cory S. Sheffield*
Affiliation:
Royal Saskatchewan Museum, 2340 Albert Street, Regina, Saskatchewan, Canada S4P 2V7
Peter G. Kevan
Affiliation:
School of Environmental Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1
Alana Pindar
Affiliation:
Department of Biology, York University, 4700 Keele Street, Toronto, Ontario, Canada M3J 1P3
Laurence Packer
Affiliation:
Department of Biology, York University, 4700 Keele Street, Toronto, Ontario, Canada M3J 1P3
*
1Corresponding author (e-mail: cory.sheffield@gov.sk.ca).

Abstract

Bees are important within terrestrial ecosystems, providing pollination, which facilitates plant reproduction. Agricultural regions are large landscapes containing varying proportions of cropland, natural, and semi-natural habitats. Most bees are not restricted to any of these and move freely throughout, exploiting food and nesting resources in favourable locations. Many factors affect bee diversity, and knowledge of these is crucial for promoting healthy bee communities. The main objectives of this study were to compare diversity and guild structure of bee communities across a range of land disturbance levels within the Annapolis Valley, Nova Scotia, Canada, in habitats ranging from managed apple orchards to old fields. The two habitat extremes differed significantly; intensely managed orchards had significantly lower species richness (∼50%) than observed/estimated in old fields, but orchards with intermediate levels of adjacent natural/semi-natural habitat showed affinities to either extreme depending on the metrics used for estimating species richness. Species assemblages in orchards had lower proportions of several guilds, particularly cavity-nesters, bumble bees, and cleptoparasites, than other habitats. These guilds accounted for over 30% of bees collected in old fields but only 3–10% in orchards, increasing with habitat complexity. The use of guilds for assessing the health of bee communities is discussed.

Résumé

Les abeilles jouent un rôle important dans les écosystèmes terrestres par la pollinisation qui facilite la reproduction des plantes. Les régions agricoles présentent de grands paysages contenant des proportions variables d'habitats agricoles, naturels et semi-naturels. Les abeilles ne sont pas restreintes à l'un ou l'autre de ces habitats et se déplacent librement dans tout l'espace pour y exploiter les ressources de nourriture et de nidification dans les sites favorables. Plusieurs facteurs affectent la diversité des abeilles et il est absolument nécessaire de les connaître si on veut favoriser des peuplements d'abeille en santé. L'objectif principal de notre étude est de comparer la diversité et la structure en guildes des peuplements d'abeilles le long d'un gradient de terres perturbées, allant de pommeraies aménagées à des champs abandonnés, au sein de la vallée d'Annapolis, Nouvelle-Écosse, Canada. Les deux habitats extrêmes diffèrent significativement: les pommeraies à aménagement intensif possèdent une richesse spécifique significativement plus basse (environ 50%) que celle observée/estimée dans les champs abandonnés; toutefois, les pommeraies à niveau intermédiaire d'aménagement montrent des affinités avec l'un ou l'autre des extrêmes selon la métrique utilisée pour estimer la richesse spécifique. Les peuplements des pommeraies contiennent des proportions plus basses de plusieurs guildes, en particulier d'abeilles nichant dans les cavités, de bourdons et de cleptoparasites que ceux des autres habitats. Ces guildes représentent 30% des abeilles récoltées dans les champs abandonnés, mais seulement 3–10% dans les pommeraies, pourcentage qui augmente avec la complexité de l'habitat. Nous discutons de l'utilisation des guildes pour évaluer la santé des peuplements d'abeilles.

Type
Biodiversity & Evolution
Copyright
Copyright © Entomological Society of Canada 2013

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References

Banaszak, J. 2000. Effect of habitat heterogeneity on the diversity and density of pollinating insects. In Interchanges of insects between agricultural and surrounding landscapes. Edited by B. Ekbom, M.E. Irwin and Y. Robert. Kluwer Academic Publishers, Dordrecht, Netherlands. pp. 123140.CrossRefGoogle Scholar
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., et al. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313: 351354.CrossRefGoogle ScholarPubMed
Blanche, K.R., Ludwig, J.A., Cunningham, S.A. 2006. Proximity to rainforests enhances pollination and fruit set in orchards. Journal of Applied Ecology, 43: 11821187.CrossRefGoogle Scholar
Blondel, J. 2003. Guilds or functional groups: does it matter? Oikos, 100: 223231.CrossRefGoogle Scholar
Brittain, W.H. 1933. Apple pollination studies in the Annapolis Valley, Nova Scotia. Canadian Department of Agriculture Bulletin, New Series, 162: 1198.Google Scholar
Brosi, B.J., Daily, G.C., Ehrlich, P.R. 2007. Bee community shifts with landscape context in a tropical countryside. Ecological Applications, 17: 418430.CrossRefGoogle Scholar
Brosi, B.J., Daily, G.C., Shih, T.M., Oviedo, F., Durán, G. 2008. The effects of forest fragmentation on bee communities in tropical countryside. Journal of Applied Ecology, 45: 773783.CrossRefGoogle Scholar
Büchs, W., Harenberg, A., Zimmermann, J., Weiß, B. 2003. Biodiversity, the ultimate agri-environmental indicator? Potential and limits for the application of faunistic elements as gradual indicators in agroecosystems. Agriculture, Ecosystems & Environment, 98: 99123.CrossRefGoogle Scholar
Calvillo, L.M., Ramírez, V.M., Parra-Tabla, V., Navarro, J. 2010. Bee diversity in a fragmented landscape of the Mexican neotropic. Journal of Insect Conservation, 14: 323334.CrossRefGoogle Scholar
Cane, J.H., Minckley, R., Roulston, T., Kervin, L.J., Williams, N.M. 2006. Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecological Applications, 16: 632644.CrossRefGoogle ScholarPubMed
Carré, G., Roche, P., Chifflet, R., Morison, N., Bommarco, R., Harrison-Cripps, J., et al. 2009. Landscape context and habitat type as drivers of bee diversity in European annual crops. Agriculture, Ecosystems & Environment, 133: 4047.CrossRefGoogle Scholar
Chao, A., Ma, M.-C., Yang, M.C.K. 1993. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika, 80: 193201.CrossRefGoogle Scholar
Colwell, R.K. 2005. EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5 [online]. Available from http://viceroy.eeb.uconn.edu/EstimateS [accessed 12 October 2012].Google Scholar
Colwell, R.K.Coddington, J.A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London, Series B, 345: 101118.Google ScholarPubMed
Corbet, S.A. 1995. Insects, plants and succession: advantages of long-term set aside. Agriculture, Ecosystems and Environment, 53: 201217.CrossRefGoogle Scholar
Craig, W. 1998. Tree fruit census of the Annapolis Valley. Production Technology Branch, Nova Scotia Department of Agriculture and Marketing, Kentville, Nova Scotia, Canada.Google Scholar
Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J., Walker, B., et al. 2003. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment, 1: 488494.CrossRefGoogle Scholar
Gardner, K.E.Ascher, J.S. 2006. Notes on the native bee pollinators in New York apple orchards. Journal of the New York Entomological Society, 114: 8691.CrossRefGoogle Scholar
Gibbs, J. 2010. Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa, 2591: 1382.CrossRefGoogle Scholar
Gotelli, N.J.Entsminger, G.L. 2003. EcoSim: Null models software for ecology version 7.72 [computer program]. Jericho, Vermont, United States of America.Google Scholar
Greenleaf, S.S.Kremen, C. 2006. Wild bee species increase tomato production and respond differently to surrounding land use in northern California. Biological Conservation, 133: 8187.CrossRefGoogle Scholar
Griswold, T., Parker, F.D., Tepedino, V.J. 1997. The bees of the San Rafael Desert: implications for the bee fauna of the Grand Staircase-Escalante National Monument. In Proceedings of the Grand Staircase-Escalante National Monument Science Symposium, Cedar City, Utah. Edited by L.M. Hill. United States Department of the Interior Bureau of Land Management, Salt Lake City, Utah, United States of America. pp. 175186.Google Scholar
Grixti, J.C.Packer, L. 2006. Changes in the bee fauna (Hymenoptera: Apoidea) of an old field site in southern Ontario, revisited after 34 years. The Canadian Entomologist, 138: 147164.CrossRefGoogle Scholar
Grundel, R., Frohnapple, K.J., Jean, R.P., Pavlovic, N.B. 2011. Effectiveness of bowl trapping and netting for inventory of a bee community. Environmental Entomology, 40: 374380.CrossRefGoogle Scholar
Hagen, M.Kraemer, M. 2010. Agricultural surroundings support flower-visitor networks in an Afrotropical rain forest. Biological Conservation, 143: 16541663.CrossRefGoogle Scholar
Hill, J.K.Hamer, K.C. 1998. Using species abundance models as indicators of disturbance in tropical forests. Journal of Applied Ecology, 35: 458460.CrossRefGoogle Scholar
Holzschuh, A., Steffan-Dewenter, I., Kleijn, D., Tscharntke, T. 2007. Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. Journal of Applied Ecology, 44: 4149.CrossRefGoogle Scholar
Hubbell, S.P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Hughes, R.G. 1986. Theories and models of species abundance. American Naturalist, 128: 879899.CrossRefGoogle Scholar
Jauker, F., Diekötter, T., Schwarzbach, F., Wolters, V. 2009. Pollinator dispersal in an agricultural matrix: opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landscape Ecology, 24: 547555.CrossRefGoogle Scholar
Kevan, P.G., Clark, E.A., Thomas, V.G. 1990. Pollination: a crucial ecological and mutualistic link in agroforestry and sustainable agriculture. Proceeding of the Entomological Society of Ontario, 121: 4348.Google Scholar
Kevan, P.G., Greco, C.F., Belaoussoff, S. 1997. Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystem health: pesticide stress on pollinators on blueberry heaths. Journal of Applied Ecology, 34: 11221136.CrossRefGoogle Scholar
Kevan, P.G.Imperatriz-Fonseca, V.L. 2002. Pollination bees: the conservation link between agriculture and nature. Ministry of Environment, Secretariat for Biodiversity and Forests, Brasília-DF, Brazil.Google Scholar
Klein, A.M., Vassiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., et al. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society, Series B, 274: 303313.Google ScholarPubMed
Krebs, C.J. 1998. Ecological methodology, 2nd ed.Harper and Row, New York, New York, United States of America.Google Scholar
Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W. 2004. The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecology Letters, 7: 11091119.CrossRefGoogle Scholar
Kremen, C., Williams, N.M., Thorp, R.W. 2002. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences, 99: 1681216816.CrossRefGoogle ScholarPubMed
Larsen, T.H., Williams, N.M., Kremen, C. 2005. Extinction order and altered community structure rapidly disrupts ecosystem functioning. Ecology Letters, 8: 538547.CrossRefGoogle ScholarPubMed
Lee, S.-M.Chao, A. 1994. Estimating population size via sample coverage for closed capture-recapture models. Biometrics, 50: 8897.CrossRefGoogle ScholarPubMed
MacKenzie, K.E.Winston, M.L. 1984. Diversity and abundance of native bee pollinators on berry crops and natural vegetation in the lower Fraser Valley, British Columbia. The Canadian Entomologist, 116: 965974.CrossRefGoogle Scholar
Magurran, A.E. 2004. Measuring biological diversity. Blackwell Publishing, Malden, Massachusetts, United States of America.Google Scholar
Magurran, A.E.Henderson, P.A. 2003. Explaining the excess of rare species in natural species abundance distributions. Nature, 422: 714716.CrossRefGoogle ScholarPubMed
Marshall, S.A., Anderson, R.S., Roughley, R.E., Behan-Pelletier, V., Danks, H.V. 1994. Terrestrial arthropod biodiversity: planning a study and recommended sampling techniques. Supplement to the Bulletin of the Entomological Society of Canada, 26: 133.Google Scholar
Matteson, K.C., Ascher, J.S., Langellotto, G.A. 2008. Bee richness and abundance in New York City urban gardens. Annals of the Entomological Society of America, 101: 140150.CrossRefGoogle Scholar
Michener, C.D. 1979. Biogeography of the bees. Annals of the Missouri Botanical Garden, 66: 277347.CrossRefGoogle Scholar
Michener, C.D. 2007. The Bees of the world, 2nd ed.Johns Hopkins University Press, Baltimore, Maryland, United States of America.CrossRefGoogle Scholar
National Research Council. 2007. Status of pollinators in North America. National Academies Press, Washington, DC, United States of America.Google Scholar
Neily, P.D., Quigley, E., Benjamin, L., Stewart, B., Duke, T. 2003. Ecological land classification for Nova Scotia. Vol. 1 – Mapping Nova Scotia's terrestrial ecosystems. Report DNR, 2003–2. Nova Scotia Department of Natural Resources, Truro, Nova Scotia, Canada.Google Scholar
Nielsen, A., Steffan-Dewenter, I., Westphal, C., Messinger, O., Potts, S.G., Roberts, S.P.M., et al. 2011. Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques. Ecological Research, 26: 969983.CrossRefGoogle Scholar
Oertli, S., Muller, A., Dorn, S. 2005. Ecological and seasonal patterns in the diversity of a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes). European Journal of Entomology, 102: 5363.CrossRefGoogle Scholar
O'Neill, R.V., Krummel, J.R., Gardner, R.H., Sugihara, G., Jackson, B., DeAngelis, D.L., et al. 1988. Indices of landscape pattern. Landscape Ecology, 1: 153162.CrossRefGoogle Scholar
Packer, L. 2010. Keeping the bees: why all bees are at risk and what we can do to save them. HarperCollins Publishers Ltd, Toronto, Canada.Google Scholar
Peterson, G., Allen, C.R., Holling, C.S. 1998. Ecological resilience, biodiversity, and scale. Ecosystems, 1: 618.CrossRefGoogle Scholar
Potts, S.G., Vulliamy, N., Dafni, A., Ne'eman, G., Wilmer, P. 2003. Linking bees and flowers: how do floral communities structure pollinator communities? Ecology, 84: 26282642.CrossRefGoogle Scholar
Preston, F.W. 1948. The commonness, and rarity, of species. Ecology, 29: 254283.CrossRefGoogle Scholar
Preston, F.W. 1980. Noncanonical distributions of commonness and rarity. Ecology, 61: 8897.CrossRefGoogle Scholar
Pywell, R.F., Warman, E.A., Hulmes, L., Hulmes, S., Nuttall, P., Sparks, T.H., et al. 2006. Effectiveness of new agri-environment schemes in providing foraging resources for bumblebees in intensively farmed landscapes. Biological Conservation, 129: 192206.CrossRefGoogle Scholar
Rathcke, B.J.Jules, E.S. 1993. Habitat fragmentation and plant–pollinator interactions. Current Science, 65: 273277.Google Scholar
Rehan, S.M.Sheffield, C.S. 2011. Morphological and molecular delineation of a new species in the Ceratina dupla species-group (Hymenoptera: Apidae) of eastern North America. Zootaxa, 2873: 3550.CrossRefGoogle Scholar
Richards, A.J. 2001. Does low biodiversity resulting from modern agricultural practice affect crop pollination and yield? Annals of Botany, 88: 165172.CrossRefGoogle Scholar
Roulston, T.H.Goodell, K. 2011. The role of resources and risks in regulating wild bee populations. Annual Review of Entomology, 56: 293312.CrossRefGoogle ScholarPubMed
Roulston, T.H., Smith, S.A., Brewster, A.L. 2007. A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. Journal of the Kansas Entomological Society, 80: 179181.CrossRefGoogle Scholar
Rowe, J.S. 1972. Forest regions of Canada. Department of the Environment, Canadian Forestry Service, Ottawa, Ontario, Publication 1300: 1–172.Google Scholar
Scott-Dupree, C.D.Winston, M.L. 1987. Wild bee pollinator diversity and abundance in orchard and uncultivated habitats in the Okanagan Valley, British Columbia. The Canadian Entomologist, 119: 735745.CrossRefGoogle Scholar
Scrosati, R.A., van Genne, B., Heaven, C.S., Watt, C.A. 2011. Species richness and diversity in different functional groups across environmental stress gradients: a model for marine rocky shores. Ecography, 34: 151161.CrossRefGoogle Scholar
Seaby, R.M.H., Henderson, P.A., Prendergast, J.R. 2004. Community analysis package Version 3.2 [computer program]. Pisces Conservation Ltd, Lymington, United Kingdom.Google Scholar
Sheffield, C.S., Dumesh, S., Cheryomina, M. 2011. Hylaeus punctatus (Hymenoptera: Colletidae), a bee species new to Canada, with notes on other non-native species. Journal of the Entomological Society of Ontario, 142: 2943.Google Scholar
Sheffield, C.S., Hebert, P.D.N., Kevan, P.G., Packer, L. 2009. DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Molecular Ecology Resources, 9 (s1), 196207.CrossRefGoogle ScholarPubMed
Sheffield, C.S., Kevan, P.G., Smith, R.F., Rigby, S.M., Rogers, R.E.L. 2003. Bee species of Nova Scotia, Canada, with new records and notes on bionomics and floral relations (Hymenoptera: Apoidea). Journal of the Kansas Entomological Society, 76: 357384.Google Scholar
Sheffield, C.S., Kevan, P.G., Westby, S.M., Smith, R.F. 2008a. Diversity of cavity-nesting bees (Hymenoptera: Apoidea) within apple orchards and wild habitats in the Annapolis Valley, Nova Scotia, Canada. The Canadian Entomologist, 140: 235249.CrossRefGoogle Scholar
Sheffield, C.S., Westby, S.M., Smith, R.F., Kevan, P.G. 2008b. Potential of bigleaf lupine for building and sustaining Osmia lignaria populations for pollination of apple. The Canadian Entomologist, 140: 589599.CrossRefGoogle Scholar
Shepherd, M., Buchmann, S.L., Vaughan, M., Black, S.H. 2003. Pollinator conservation handbook. The Xerces Society, Portland, Oregon, United States of America.Google Scholar
Sokal, R.R.Rohlf, F.J. 1995. Biometry. W.H. Freeman and Co., New York, New York, United States of America.Google Scholar
Steffan-Dewenter, I., Münzenberg, U., Bürger, C., Thies, C., Tscharntke, T. 2002. Scale-dependent effects of landscape context on three pollinator guilds. Ecology, 83: 14211432.CrossRefGoogle Scholar
Tabor, G.M.Aguirre, A.A. 2004. Ecosystem health and sentinel species: adding an ecological element to the proverbial “canary in the mineshaft”. EcoHealth, 1: 226228.CrossRefGoogle Scholar
Tilman, D.Lehman, C. 2001. Biodiversity, composition, and ecosystem processes: theory and concepts. In The functional consequences of biodiversity: empirical progress and theoretical extensions. Edited by A.P. Kinzig, S.W. Pacala and D. Tilman. Princeton University Press, Princeton, New Jersey, United States of America. pp. 941.Google Scholar
Toler, T.R., Evans, E.W., Tepedino, V.J. 2005. Pan-trapping for bees (Hymenoptera: Apiformes) in Utah's west desert: the importance of color diversity. Pan-Pacific Entomologist, 81: 103113.Google Scholar
Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C. 2005. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecology Letters, 8: 857874.CrossRefGoogle Scholar
Tuell, J.K., Ascher, J.S., Isaacs, R. 2009. Wild bees (Hymenoptera: Apoidea: Anthophila) of the Michigan highbush blueberry agroecosystem. Annals of the Entomological Society of America, 102: 275287.CrossRefGoogle Scholar
Vincent, C., de Oliveira, D., Bélanger, A., Chiasson, H. 1994. Aménagement des insects pollinisateurs et régie des insects ravageurs du fraisier. In Colloque sur l'apiculture et al pollinisation. Edited by Conseil des Productions Végétales du Québec, Inc. Montréal, Québec, Canada. pp. 81–92.Google Scholar
Walker, B.H. 1992. Biological diversity and ecological redundancy. Conservation Biology, 6: 1823.CrossRefGoogle Scholar
Walker, B.H., Kinzig, A.P., Langridge, J. 1999. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems, 2: 95113.CrossRefGoogle Scholar
Watson, J.C., Wolf, A.T., Ascher, J.S. 2011. Forested landscapes promote richness and abundance of native bees (Hymeoptera: Apoidea: Anthophila) in Wisconsin apple orchards. Environmental Entomology, 40: 621632.CrossRefGoogle Scholar
Webb, K.T.Marshall, L.B. 1999. Ecoregions and ecodistricts of Nova Scotia. Crops and Livestock Research Centre, Research Branch, Agriculture and Agri-Food Canada, Truro, Nova Scotia; Indicators and Assessment Office, Environmental Quality Branch, Environment Canada, Hull, Québec, Canada.Google Scholar
Westerkamp, C.Gottsberger, G. 2000. Diversity pays in crop pollination. Crop Science, 40: 12091222.CrossRefGoogle Scholar
Westphal, C., Bommarco, R., Carré, G., Lamborn, E., Morison, N., Petanidou, T., et al. 2008. Measuring bee diversity in different European habitats and biogeographical regions. Ecological Monographs, 78: 654671.CrossRefGoogle Scholar
Westphal, C., Steffan-Dewenter, I., Tscharntke, T. 2003. Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters, 6: 961965.CrossRefGoogle Scholar
Williams, N.M., Crone, E.E., Roulston, T.H., Minckley, R.L., Packer, L., Potts, S.G. 2010. Ecological and life-history traits predict bee species responses to environmental disturbances. Biological Conservation, 143: 22802291.CrossRefGoogle Scholar
Williamson, M.Gaston, K.J. 2005. The lognormal distribution is not an appropriate null hypothesis for the species-abundance distribution. Journal of Animal Ecology, 74: 409422.CrossRefGoogle Scholar
Wilson, J.S., Griswold, T., Messinger, O.J. 2008. Sampling bee communities (Hymenoptera: Apiformes) in a desert landscape: are pan traps sufficient? Journal of the Kansas Entomological Society, 81: 288300.CrossRefGoogle Scholar
Winfree, R. 2010. The conservation and restoration of wild bees. Annals of the New York Academy of Sciences, 1195: 169197.CrossRefGoogle ScholarPubMed
Winfree, R., Griswold, T., Kremen, C. 2007. Effect of human disturbance on bee communities in a forested ecosystem. Conservation Biology, 21: 213223.CrossRefGoogle Scholar
Zar, J.H. 1999. Biostatistical analysis, 4th ed.Prentice Hall, Upper Saddle River, New Jersey, United States of America.Google Scholar