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Predatory beetles in cacao agroforestry systems in Brazilian Atlantic forest: a test of the natural enemy hypothesis

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Abstract

The natural enemy hypothesis predicts a positive correlation between plant species diversity and natural enemy control. This study aimed to evaluate the role of traditional cacao agroforests, known as “cabrucas,” on the conservation of the predatory beetle community compared to that of monodominant rubber agroforests. Predatory beetles were sampled in three habitats in Southeastern Bahia, Brazil: cabrucas and rubber agroforests and native Atlantic forests. In each habitat, 18 10 m2 plots were established, in which canopy cover was measured and beetles were sampled with a modified Malaise/window trap. Land use intensification did not affect the composition of predatory beetles, with the presence of widely distributed species that are also capable of colonizing simpler environments such as the rubber agroforest. Canopy cover had a positive effect on generalist predator diversity and we observed a reduction in the abundance and species richness of generalist predators with increasing habitat homogenization. Despite the simplified structure of the habitat, the remaining tree diversity and canopy cover in cabrucas supported a community of generalist predators similar to the one found in the native forest. Species diversity of bark beetle predators was higher in cabrucas, which may be due to the high diversity of bark beetles and the favorable abiotic conditions, whereas the low abundance of prey in the native forest and severe abiotic conditions in the rubber agroforest probably determined the lower diversity of generalist predators in these habitats. Cabrucas play an important role in the conservation, supporting a community of predatory beetles more similar to the one found in native forest and that is more effective at controlling populations of herbivores than in homogeneous rubber agroforests.

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References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Basset Y (1988) A composite interception trap for sampling arthropods in tree canopies. J Aust Entomol Soc 27:213–219

    Article  Google Scholar 

  • Basset Y, Novotny V, Miller SE, Kitching RL (2003) Arthropods of Tropical Forests: spatio-temporal dynamics & resource use in the canopy. Cambridge University Press, Cambridge

    Google Scholar 

  • Basset Y, Cizek L, Cuénoud P, Didham RK et al (2012) Arthropod diversity in a tropical forest. Science 338(6113):1481–1484

    Article  CAS  PubMed  Google Scholar 

  • Bhagwat S, Willis K, Birks H, Whittaker R (2008) Agroforestry: a refuge for tropical biodiversity? Trends Ecol Evol 23:261–267

    Article  PubMed  Google Scholar 

  • Bos MM, Steffan-Dewenter I, Tscharntke T (2007) The contribution of cacao agroforests to the conservation of lower canopy ant and beetle diversity in Indonesia. Biodivers Conserv 16(8):2429–2444

    Article  Google Scholar 

  • Cassano CR, Schroth G, Faria D, Delabie JHC, Bede L, Oliveira LC, Mariano-Neto E (2014) Desafios e recomendações para a conservação da biodiversidade na região cacaueira do sul da Bahia., Boletim técnico n° 205CEPLAC/CEPEC, Ilhéus

    Google Scholar 

  • Coddington JA, Agnarsson I, Miller JA, Kuntner M, Hormiga G (2009) Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. J Anim Ecol 78(3):573–584

    Article  PubMed  Google Scholar 

  • Crawley MJ (2013) The R Book, 2nd edn. Willey, New York

    Google Scholar 

  • DaRocha WD, Ribeiro SP, Neves FS, Fernandes GW, Leponce M, Delabie JHC (2015) How does bromeliad distribution structure the arboreal ant assemblage (Hymenoptera: Formicidae) on a single tree in a Brazilian Atlantic forest agroecosystem? Myrmecol News 21:83–92

    Google Scholar 

  • Faria D, Paciencia MLB, Dixo M, Laps RR, Baumgarten J (2007) Ferns, frogs, lizards, birds and bats in forest fragments and shade cacao plantations in two contrasting landscapes in the Atlantic forest, Brazil. Biodivers Conserv 16:2335–2357

    Article  Google Scholar 

  • Fonseca GAB, Alger K, Pinto LP, Araujo M, Cavalcanti R (2004) Corredores de biodiversidade: o corredor central da Mata Atlântica. In: Arruda MB, Sá LFSN (eds) Corredores Ecológicos: uma Abordagem Integradora de Ecossistemas no Brasil. IBAMA, Brasília, pp 47–65

    Google Scholar 

  • Frazer G, Canham C, Lertzman K (1999) Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University, The Institute of Ecosystem Studies, Burnaby, Millbrook

    Google Scholar 

  • Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JM, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12(10):1029–1039

    Article  PubMed  Google Scholar 

  • Klein AM, Steffan-Dewenter I, Buchori D, Tscharntke T (2002a) Effects of land-use intensity in tropical agroforestry systems on flower-visiting and trap-nesting bees and wasps. Conserv Biol 16:1003–1014

    Article  Google Scholar 

  • Klein AM, Steffan-Dewenter I, Tscharntke T (2002b) Predator–prey ratios on cocoa along a land-use gradient in Indonesia. Biodivers Conserv 11(4):683–693

    Article  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  • Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139(1):1–10

    Article  PubMed  Google Scholar 

  • Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592

    Article  Google Scholar 

  • Marques JRB, Monteiro WR (2006) Adoção do sistema agroflorestal cacau x seringa-melhoria de condições de cultivo e agregação de valores. 28a Semana do Fazendeiro. CEPLAC/CENEX/EMARC, Itabuna, pp 9–14

    Google Scholar 

  • McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14(11):450–453

    Article  CAS  PubMed  Google Scholar 

  • Mori SA (1989) Eastern Extra-Amazonian Brasil. In: Campbell DG, Hammond HD (eds) Floristic inventory of Tropical Countries: the status of plant systematics, collections, and vegetation, plus recommendations for the future. The New York Botanical Garden, New York, pp 427–455

    Google Scholar 

  • Novais SMA, Macedo-Reis LE, DaRocha WD, Neves FS (2016) Effects of habitat management on different feeding guilds of herbivorous insects in cacao agroforestry systems. Int J Trop Biol Conserv 64(1)

  • Pardini R, Faria D, Accacio GM, Laps RR, Mariano-Neto E, Paciencia MLB, Dixo M, Baumgarten J (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia. Biol Conserv 142:1178–1190

    Article  Google Scholar 

  • Pemberton RW, Vandenberg NJ (1993) Extrafloral nectar feeding by ladybird beetles (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 95:139–151

    Google Scholar 

  • Perfecto I, Mas A, Dietsch T, Vandermeer J (2003) Conservation of biodiversity in coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodivers Conserv 12:1239–1252

    Article  Google Scholar 

  • Philpott SM, Armbrecht I (2006) Biodiversity in tropicalagroforests and the ecological role of ants and ant diversity in predatory function. Ecol Entomol 31:369–377

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 813-846

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. Version 3.1.1. User’s guide and application published: http://www.R-project.org

  • Rafael JA, Melo GAR, Carvalho CJB, Casari SA, Constantino R (2012) Insetos do Brasil: Diversidade e Taxonomia. Ribeirão Preto, Holos Editora

    Google Scholar 

  • Rice RA, Greenberg R (2000) Cacao cultivation and the conservation of biological diversity. Ambio 29:167–173

    Article  Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–120

    Article  Google Scholar 

  • Russell EP (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ Entomol 18(4):590–599

    Article  Google Scholar 

  • Sambuichi RH, Vidal DB, Piasentin FB, Jardim JG et al (2012) Cabruca agroforests in southern Bahia, Brazil: tree component, management practices and tree species conservation. Biodivers Conserv 21(4):1055–1077

    Article  Google Scholar 

  • Sanchez-Azofeifa, GA, Kalacska MER, Gamon J, Rodriguez JP et al (2007) Ecological and Biophysical Dimension of Tropical Dry Forest. Manual Method 48-104

  • Schroth G, Faria D, Araujo M, Bede L, Van Bael SA, Cassano CR, Oliveira LC, Delabie JHC (2011) Conservation in tropical landscape mosaics: the case of the cacao landscape of southern Bahia, Brazil. Biodivers Conserv 20:1635–1654

    Article  Google Scholar 

  • Sperber C, Nakayama K, Valverde MJ, Neves FS (2004) Tree species richness and density affect parasitoid diversity in cacao agroforestry. Basic Appl Ecol 5:241–251

    Article  Google Scholar 

  • Steffan-Dewenter I, Kessler M, Barkmann J, Bos MM et al (2007) Tradeoffs between income, biodiversity, and ecosystem functioning during tropical rainforest conversion and agroforestry intensification. Proc Natl Acad Sci USA 104(12):4973–4978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas WW (2003) Natural vegetation types in Southern Bahia. In: Prado PI, Landau EC, Moura RT, Pinto LPS, Fonseca GAB, Alger K (eds) Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia. Publicação em CD Rom, IESB/CI/CABS/UFMG/UNICAMP, Ilhéus, pp 1–4

    Google Scholar 

  • Vanderwel MC, Malcolm JR, Smith SM, Islam N (2006) Insect community composition and trophic guild structure in decaying logs from eastern Canadian pine-dominated forests. Forest Ecol Manag 225(1):190–199

    Article  Google Scholar 

  • Wäckers FL, van Rijn PCJ, Bruin J (eds) (2005) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

We thank H. Brant, R. Mello, F. Pacelhe and G. Monteiro for field help. We thank the Coordination of Improvement of Higher Education Personnel for research grants awarded during the development of this study. Finally, we thank the Una Biological Reserve/Chico Mendes Institute for Biodiversity Conservation for all the physical structure and logistical support. This work was in fulfillment for the master dissertation of SMAN, and was financially supported by Brazilian National Research Council, Minas Gerais Research Support Foundation and Bahia Research Support Foundation DTE0036/2013 (5334/2013).

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Correspondence to Samuel M. A. Novais.

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Novais, S.M.A., Macedo-Reis, L.E. & Neves, F.S. Predatory beetles in cacao agroforestry systems in Brazilian Atlantic forest: a test of the natural enemy hypothesis. Agroforest Syst 91, 201–209 (2017). https://doi.org/10.1007/s10457-016-9917-z

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