Contribution of cocoa plantations to the conservation of native ants (Insecta: Hymenoptera: Formicidae) with a special emphasis on the Atlantic Forest fauna of southern Bahia, Brazil
Tóm tắt
By maintaining a forest-like structure, shaded cocoa plantations contribute to the conservation of ants that usually live in the soil, leaf litter or canopy of tropical forests. Here we synthesize the available information on the diversity and community structure of ants in shaded cocoa plantations in the Atlantic forest region of Brazil, compare ant assemblages in cocoa agroforests with forests and other forms of agriculture, and discuss how these shaded plantations contribute to the conservation of the ants in the Atlantic Forest region. We also discuss ants of economical importance and of special interest, including Camponotus, Dolichoderus, Gnamptogenys, Pachycondyla, Pseudomyrmex and other litter dwelling genera. We discuss the situation of the tramp ant Wasmannia auropunctata in the Bahian cocoa-producing region where it is considered as native, and that of the two cryptobiotic genera Thaumatomyrmex and Typhlomyrmex, as well as that of proven and possible endangered army ant and Ponerini species. A total of 192 ant species from four strata were found in extensive sampling of a cocoa plantation with a relatively simple shade canopy (comprised primarily of Erythrina). Species richness in the cocoa plantations corresponded roughly to that of low diversity native forests, and species composition of cocoa plantations was most similar to native habitats (forest and mangroves) while ant composition in other agricultural habitats was most similar to that of urban areas. Although occurrences of Wasmannia auropunctata were similar in cocoa plantations and forests, abundance of Thaumatomyrmex and Typhlomyrmex, generally thought to be rare ants, was relatively high in cocoa plantations. These results, from cocoa plantations with relatively simple shade, demonstrate the importance of cocoa for ant conservation in the Atlantic forest region of Brazil. It is likely that cocoa plantations with a greater number of vegetation strata and higher tree species richness (such as traditional cabruca plantations) provide even more important habitat for ants generally and for ant species of conservation concern.
Từ khóa
Tài liệu tham khảo
Alger K, Caldas M (1994) The declining cocoa economy and the Atlantic forest of southern Bahia, Brazil: conservation attitudes of cocoa planters. Environmentalist 14(2):107–119
Andersen AN (1991) Responses of ground-foraging ant communities to three experimental fire regimes in a Savanna forest of tropical Australia. Biotropica 23(4):575–585
Baroni Urbani C, De Andrade ML (2003) The ant genus Thaumatomyrmex in Cuba (Hymenoptera: Formicidae) with description of two new species. Mitt Dtsch Entomol Ges 76: 263–277
Belshaw R, Bolton B (1993) The effect of forest disturbance on leaf litter ant fauna in Ghana. Biodiv Conserv 2:656–666
Bestelmeyer BT, Agosti D, Alonso LE, Brandão CRF, Brown Jr. WL, Delabie JHC, Silvestre R (2000) Field techniques for the study of ground-living ants: an overview, description, and evaluation. In: Agosti D, Majer JD, Tennant de Alonso L, Schultz T (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution, Washington USA, pp 122–144
Brandão CRF, Diniz J, Tomotake E (1991) Thaumatomyrmex strips millipedes for prey: a novel predatory behaviour in ants, and the first case of sympatry in the genus (Hymenoptera: Formicidae). Insectes Sociaux 38:335–344
Brown Jr KS (1991) Conservation of neotropical environments: insects as indicators. In: Collins NM, Thomas JM (eds), The conservation of insects and their habitats. Academic Press, London, pp 349–404
Colwell RK (2000) Estimates: statistical estimation of species richness and shared species from samples. Version 6.0b1. User’s guide and application published at: http://viceroy.eeb.uconn.edu/estimates. Cited 20 Sep 2006
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Massachussets, USA
Dean W (1995) With broadax and firebrand—the destruction of the Brazilian Atlantic Forest. University of California Press, Berkeley USA
Dejean A, Corbara B, Fernández F, Delabie JHC (2003) Mosaicos de hormigas arbóreas en bosques y plantaciones tropicales. In: Fernández F. (ed.) Introducción a las hormigas de la región Neotropical, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá, Colombia, pp. 149–158
Delabie JHC (1990) The ant problems of cocoa farms in Brazil. In: Vander Meer RK, Jaffe K, Cedeño A (eds) Applied myrmecology: a world perspective, Westview Press, Boulder, Colorado USA, pp 555–569
Delabie JHC (1993) Formigas exóticas na Bahia. Bahia, Análise e Dados 3(1):19–22
Delabie JHC (1999) Comunidades de formigas (Hymenoptera; Formicidae): métodos de estudo e estudos de casos na Mata Atlântica. Resumos, XII Encontro de Zoologia do Nordeste, Feira de Santana, Bahia, Brazil, 31/01–05/02/1999.
Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neot Entomol 30(4):501–516
Delabie JHC, Agosti D, Nascimento IC (2000a) Litter ant communities of the Brazilian Atlantic rain forest region. In: Agosti D, Majer JD, Alonso LT, Schultz T (eds) Sampling ground-dwelling ants: case studies from the world’s rain forests. Curtin University, School of Environmental Biology Bulletin 18, Perth, Australia, pp 1–17
Delabie JHC, Encarnação AMV, Cazorla IM (1993) Impact d’une fourmilière d’Atta cephalotes (L.) (Formicidae; Myrmicinae; Attini) sur une cacaoyère en formation. Actes des Colloques Insectes Sociaux 8:63–71
Delabie JHC, Encarnação AM, Mauricio C, I (1994) Relations between the little fire ant, Wasmannia auropunctata, and its associated mealybug, Planococcus citri, in Brazilian cocoa farms. In: Williams DF (ed) Exotic ants: biology, impact and control of introduced species. Westview Press, Boulder Colorado USA, pp 91–103
Delabie JHC, Fisher BL, Majer JD, Wright IW (2000b) Sampling effort and choice of methods. In: Agosti D, Majer JD, Tennant de Alonso L, Schultz T (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution, Washington USA, pp 145–154
Delabie JHC, Fresneau D, Pezon A (2000c) Notes on the ecology of Thaumatomyrmex spp. (Hymenoptera: Formicidae: Ponerinae) in southeast Bahia, Brazil. Sociobiology 36(3):571–584
Delabie JHC, Mantovani JE, Cazorla IM (1991) Observações sobre a biologia de duas espécies de Acropyga (Formicidae, Formicinae, Plagiolepidini) associadas à rizosfera do cacaueiro. Rev Brasil Biol 51(1):185–192
Delabie JHC, Mariano CSF, Nascimento IC (1998) As formigas do Município de Ilhéus (Insecta: Hymenoptera: Formicidae). Especiaria 1(2):133–152
Delabie JHC, Nascimento IC, Mariano CSF (1999) Importance de l’agriculture cacaoyère pour le maintien de la biodiversité: étude comparée de la myrmécofaune de différents milieux du sud-est de Bahia, Brésil (Hymenoptera; Formicidae). In: Proceedings of the XII International Cocoa Research Conference (Salvador, BA, Brazil), Cocoa Producer’s Alliance Publisher Lagos, Nigéria 17–23 November 1996
Delabie JHC, Nascimento IC, Fonseca EC, Sgrillo RB, Soares PAO, Casimiro AB, Furst M (1997) Biogeografia das formigas cortadeiras (Hymenoptera; Formicidae; Myrmicinae; Attini) de importância econômica no leste da Bahia e nas regiões periféricas dos Estados vizinhos. Agrotrópica 9(2):49–58
Delabie JHC, Paim VRLM, Nascimento IC, Campiolo S, Mariano CSF (2006) As formigas como indicadores biológicos do impacto humano em manguezais da costa sudeste da Bahia. Neot Entomol 35(5):602–615
Errard C, Delabie JHC, Jourdan H, Hefetz A (2005) Intercontinental chemical variation in the invasive ant Wasmannia auropunctata (Roger) (Hymenoptera, Formicidae): a key to the invasive success of a tramp species. Naturwissenschaften 92:319–323
Faria DM, Baumgarten J (2007) Shade cacao plantations (Theobroma cacao) and bat conservation in southern Bahia, Brazil. Biodiv Conserv 16:291–312
Faria DM, Santos BS, Sampaio E (2006) Bats from the Atlantic rainforest of southern Bahia, Brazil. Biota Neotropica 6(2):1–13
Fisher BL (1998) Ant diversity patterns along an elevational gradient in the Réserve Spéciale d’Anjanaharibe-Sud and on the western Masoala Peninsula, Madagascar. Fieldiana: Zoology (n.s.) 90:39–67
Fisher BL, Malsch AKF, Gadagkar R, Delabie JHC, Vasconcelos HL, Majer JD (2000) Applying the ALL protocol: selected case studies. In: Agosti D, Majer JD, Tennant de Alonso L, Schultz T (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution, Washington, USA, pp 207–214
Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1235
Fowler HG, Delabie JHC (1995) Resource partitioning among epigaeic and hypogaeic ants (Hymenoptera: Formicidae) of a Brazilian cocoa plantation. Ecol Austral 5:117–124
Fowler HG, Forti LC, Brandão CRF, Delabie JHC, Vasconcelos HL (1991) Ecologia Nutricional de formigas. In: Panizzi AR, Parra JRP (eds) Ecologia Nutricional de Insetos e suas Implicações no Manejo de Pragas, Editora Manole e CNPq São Paulo, pp 131–223
Fraga NJ, Delabie JHC, Mello VRL, Nery AS, Campos CS (1999) Diversidade de Pseudomyrmex spp (Formicidae: Pseudomyrmecinae) em manguezais no sudeste da Bahia. Naturalia 24(n.esp.): 103–105
Franks N (1989) Army-ants: a collective intelligence. Am Scientist 77(2):138–145
Freitas AVL, Leal IR, Uehara-Prado M, Iannuzzi L (2006) Insetos como indicadores da conservação da paisagem. In: Rocha CFD, Bergallo HG, Van Sluys M, Alves MA (eds) Biologia da Conservação, Essências Rima Editora, São Carlos, SP (Brazil), pp 357–384
Galindo-Leal C, Camara IG (2005) Mata atlântica: diversidade, ameaças e perspectivas. São Paulo, Fundação SOS Mata Atlântica/ Belo Horizonte, Conservação Internacional
Gutiérrez JL, Jones CG (2006) Physical ecosystem engineers as agents of biogeochemical heterogeneity. Bioscience 56(3):227–236
Haffer J (1974) Avian speciation in tropical South America. Publ. Nuttall Ornithol. Club, No. 14
Hölldobler B, Wilson EO (1990) The Ants. Cambridge Massachusetts Harvard University Press
Jackson JF (1978) Seasonality of flowering and leaf-fall in a Brazilian Subtropical Lower Montane Moist Forest. Biotropica 10:38–42
Johns ND (1999) Conservation in Brazil’s chocolate forest: the unlikely persistence of the traditional cocoa agroecosystem. Environ Manage 23:31–47
Johnson C, Agosti D, Delabie JHC, Dumpert K, Williams DJ, Von Tschirnhaus M, Maschwitz U (2001) Acropyga and Azteca ants (Hymenoptera: Formicidae) with scale insects (Sternorrhyncha: Coccoidea): 20 million years of intimate symbiosis. Am Mus Novit 3335
Jourdan H (2003) Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a New Caledonian rainforest. Austral Ecology 28(2):204–209
Kempf WW (1975) A revision of the Neotropical ponerine ant genus Thaumatomyrmex Mayr (Hymenoptera: Formicidae). Studia Entomologica (N.S.) 18:95–126
Lacau S (2005) Morphologie et Systématique du genre Typhlomyrmex Mayr, 1862 (Formicidae: Ectatomminae). PhD thesis, Muséum National d’Histoire Naturelle, Paris, 243 pp
Lacau S, Fresneau D, Delabie J, Jahyny B, Montreuil O, Villemant C (2001) Uma nova associação entre as larvas mirmecófilas de duas espécies de Lampyridae (Insceta: Coleoptera) e a formiga Typhlomyrmex rogenhoferi Mayr, 1862 (Formicidae, Ponerinae). Anais do XV Encontro de Mirmecologia, IAPAR, Londrina, Paraná, Brazil, 22–25 October 2001
Lacau S, Villemant C, Delabie JHC, Jahyny B, Ramos LS (2003) Observações preliminares sobre a ecologia nutricional de Typhlomyrmex sp. (Ponerinae: Typhlomyrmecini). Anais do XVI Simpósio de Mirmecologia, UFSC, Florianópolis, Santa Catarina, Brazil, 14–19 September 2003
Lacau S, Villemant C, Delabie JHC (2004) Typhlomyrmex meire, a remarkable new species endemic to Southern Bahia, Brazil (Formicidae: Ectatomminae). Zootaxa 678:1–23
Le Breton J, Chazeau J, Jourdan H (2003) Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a New Caledonian rainforest. Austral Ecol 28(2):204–209
Le Breton J, Delabie JHC, Chazeau J, Dejean A, Jourdan H (2004) Experimental evidence of large scale unicoloniality in the tramp ant Wasmannia auropunctata (Roger). J Insect Behav 17(4):263–271
Leston D (1978) A Neotropical ant mosaic. Ann Entomol Soc Am 71:649–653
Longino J (1988) Notes on the taxonomy of the Neotropical ant genus Thaumatomyrmex Mayr (Hymenoptera: Formicidae). In: Trager JC Advances in Myrmecology. Brill EJ, Leiden, pp 35–42
Longino JT, Coddington J, Colwell RK (2002) The ant fauna of a tropical rain forest: Estimating species richness three different ways. Ecology 83(3):689–702
Majer JD (1993) Comparison of the arboreal ant mosaic in Ghana, Brasil, Papua New Guinea and Australia: its structure and influence of ant diversity. In: LaSalle J, Gauld ID (eds) Hymenoptera and Biodiversity. CAB International, Wallingford, pp 115–141
Majer JD, Delabie JHC (1993) An evaluation of Brazilian cocoa farm ants as potential biological control agents. J Plant Prot Trop 10(1):43–49
Majer JD, Delabie JHC (1999) Impact of tree isolation on arboreal and ground ant communities in cleared pasture in the Atlantic rain forest region of Bahia, Brazil. Insectes Soc 46(3):281–290
Majer JD, Delabie JHC, Smith MRB (1994) Arboreal ant community patterns in Brazilian cocoa farms. Biotropica 26(1):73–83
Medeiros MA, Delabie JHC (1991) O mosaico de formigas arborícolas na região cacaueira da Bahia: estudo por olfatometria das relações entre espécies. Resumos do XIII Congresso Brasileiro de Entomologia, Sociedade de Entomológica do Brasil, Recife -PE
Medeiros MA, Fowler HG, Delabie JHC (1999) Formiga ataca pragas do cacau. Cienc Hoje 26(152):59–61
Ministério do Meio Ambiente, dos Recursos Hídricos e da Amazônia Legal (1998) Primeiro relatório Nacional para a Convenção sobre a Diversidade Biológica: Brasil
Mittermeier RA, Coimbra-Filho AF, Constable ID, Rylands AB, Valle C (1982) Conservation of primates in the Atlantic forest region of Brazil. Int Zoo Yearbook 22:2–17
Morellato LPC, Haddad CFB (2000) Introduction: the Brazilian Atlantic forest. Biotropica 32(4b):786–792
Moutinho P, Nepstad DE, Davidson EA (2003) Leaf-cutting ant nest (Atta sexdens) influence on soil, root distribution and tree growth in a secondary forest of eastern Amazonia. Ecology 84(5):1265–1276
Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in Southeastern Brazil and the influence of climate. Biotropica 32(4b):793–810
Parr CL, Chown SL (2001) Inventory and bioindicator sampling: testing pitfall and winkler methods with ants in a South African Savanna. J Insect Conserv 5(1):27–36
Passera L, Aron S (2006) Les fourmis, comportement, organisation sociale et evolution. Presses Scientifiques du CNRC, Canada
Peeters C, Crewe R (1984) Insemination controls the reproductive division of labour in a ponerine ant. Naturwiss 71:50–51
Philpott SM, Armbrecht I (2006) Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecol Entomol 31: 369–377
Ribas CR, Schoereder JH (2002) Are all ant mosaics caused by competition? Oecologia 131(4):606–611
Roberts DL, Cooper RJ, Petit LJ (2000a) Use of premontane moist forest and shade coffee agroecosystems by army ants in western Panama. Conserv Biol 14:192–199
Roberts DL, Cooper RJ, Petit LJ (2000b) Flock characteristics of ant-following birds in premontane moist forest and coffee agroecosystems in western Panama. Ecol Applications 10:1414–1425
Rocha R (2002) O futuro da Mata Atlântica, um olhar sobre o sul da Bahia. World Watch 14(6):40–46
Rolim SG, Chiarello AG (2004) Slow death of Atlantic forest trees in cocoa agroforestry in southeastern Brazil. Biodiv Conserv 13:2679–2694
Ruf F, Forget M, Gasparetto A (1994) Production de cacao et replantation à Bahia (Brésil). Les Bibliographies du CIRAD 5.
Saatchi S, Agosti D, Alger K, Delabie J, Musinski J (2001) Examining fragmentation and loss of primary forest in the southern Bahian Atlantic Forest of Brazil with radar imagery. Conserv Biol 15(4):867–875
Sanders NJ, Crutsinger GM, Dunn RR, Majer JD, Delabie JHC (2007) An ant mosaic revisited: dominant ant species disassemble arboreal ant communities but co-occur randomly. Biotropica 39(3):422–427
Silva P (1955) A formiga caçarema e o cacaueiro. IB da Bahia, Junta Executiva de Combate às Pragas e Doenças do Cacau, Ministério da Agricultura, Salvador, Bahia
Sperber CF, Nakayama K, Valverde MA, Neves FS (2004) Tree species richness and density affect parasitoid diversity in cocoa agroforestry. Basic Appl Ecol 5:241–245
Southwood TRE (1978) Ecological methods, with particular reference to the study of insect populations, 2nd edn. Chapman & Hall, London
Souza ALB, Delabie JHC, Fowler HG (1998) Wasmannia spp. (Hym., Formicidae) and insect damages to cocoa in Brazilian farms. J Appl Entomol 122:339–341
Thomas WMM, Carvalho AMV, Amorim AMA, Garrison J, Arbeláez AL (1998) Plant endemism in two forests in southern Bahia, Brazil. Biodivers Conserv 7:311–322
Underwood EC, Fisher BL (2006) The role of ants in conservation monitoring: If, when, and how. Biol Conserv 132: 166–182.
Way MJ, Khoo KC (1992) Role of ants in pest-management. Ann Rev Entomol 37:479–503
Wiens JA (1996) Wildlife in patchy environments: Metapopulations, mosaics, and management. In: McCullough DR (ed) Metapopulations and wildlife conservation. Island Press, Washington DC, pp 53–84
Willis EO, Oniki Y (1978) Birds and army ants. Ann Rev Ecol Syst 9:243–263
Winder JA (1978) The role of non-dipterous insects in the pollination of cocoa in Brazil. Bull Entomol Res 68:559–574