Diversity of gall-inducing insect associated with a superhost plant species: Plant architecture, resource availability and interspecific interactions
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Abstract. Fagundes M, Santos EML, Duarte KLR, Santos LM, Vieira JS, Oliveira CHD, Silva PS. 2020. Diversity of gall-inducing insect associated with a superhost plant species: Plant architecture, resource availability and interspecific interactions. Biodiversitas 21: 1182-1189. The role of interspecific competition in the organization of herbivorous insect communities may vary depending on resource availability. Trees are structurally more complex and have greater resource availability for herbivorous insects than shrubs. In this study, we evaluated the roles of plant architecture and interspecific interactions on community organization of the gall-inducing insect associated with trees (adult plants) and shrubs (young plants) of Copaifera langsdorffii. Our results showed that the species composition of gall-inducing insect communities associated with C. langsdorffii differed statistically between trees and shrubs. In addition, the trees presented greater diversity of gall-inducing insects than the shrubs, corroborating the hypothesis of plant architecture. The results of the analysis of null models showed that the co-occurrence of gall-inducing insect species associated with trees not differ from the co-occurrence predicted by chance. Thus, interspecific interactions cannot be used to explain the community organization of the gall-inducing insects on C. langsdorffii trees. On the other hand, the co-occurrence of gall-inducing insect species differed from the co-occurrence predicted by chance when shrubs plants were analyzed, indicating that biotic interactions can shape the structure of the gall-inducing insect community on shrubs. The lower availability of oviposition sites probably generates a dispute for these resources among females of different species of gall-inducing insects only in the shrubs. Therefore, the role of competition in the organization of herbivore insect communities on their host plant may vary depending on the ontogenetic stage of the host plant.
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References
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Araújo, WSD, Silva, IPA, Santos, BBD, Gomes-Klein, VL. 2013. Host plants of insect-induced galls in areas of cerrado in the state of Goiás, Brazil. Acta Bot Brasilica 27: 537-542. http://dx.doi.org/10.1590/S0102-33062013000300011
Carneiro, MAA, Borges, RAX, Araújo, APA, Fernandes, GWA. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev Bras Entomol 53: 570-592. http://dx.doi.org/10.1590/S0085-56262009000400007.
Cody, ML, Diamond, JM. 1975. Ecology and evolution of communities. Press, Havard.
Cornelissen, T, Stiling, P. 2008. Clumped distribution of oak leaf miners between and within plants. Basic App Ecol 9: 67-77. https://doi.org/10.1016/j.baae.2006.08.007
Cornelissen, TCG, Viana, JPR, Silva, B. 2013. Interspecific competition influences the organization of a diverse sessile insect community. Acta Oecol 52: 15-18. https://doi.org/10.1016/j.actao.2013.07.001
Costa, FV, Fagundes, M, Neves, FS. 2010. Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffi (Fabaceae). Ecología Austral 20: 9-17.
Costa, FV, Neves, FS, Silva, JO, Fagundes, M. 2011. Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod Plant Interact 5: 9-18. https://doi.org/10.1007/s11829-010-9111-6.
Costa, VF, Medeiros de Queiroz, AC, Bicalho, MML, Reis Júnior, R, Fagundes, M. 2016. Resource allocation in Copaifera langsdorffii (Fabaceae): how supra-annual fruiting affects plant traits and herbivory? Rev Biol Trop 64: 507-520.
Coutinho, RD, Cuevas-Reyes, P, Fernandes, GW, Fagundes, M. 2019. Community structure of gall-inducing insects associated with a tropical shrub: regional, local and individual patterns. Trop Ecol 60: 74-82. http://dx.doi.org/10.1007/s42965-019-00010-7
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Fagundes, M, Xavier, RCF, Faria, ML, Lopes, LGO, Cuevas?Reyes, P, Reis?Junior, R. 2018. Plant phenological asynchrony and community structure of gall?inducing insects associated with a tropical tree species. Ecol Evol 8: 10687-10697. http://dx.doi.org/10.1002/ece3.4477
Fagundes, M, Barbosa, EM, Oliveira, JBBS, Brito, BGS, Freitas, KT, Reis-Junior, R. 2019. Galling inducing insects associated with a tropical invasive shrub: the role of resource concentration and species interactions. Ecología Austral 29: 12-19.
Feeny, P. 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry. (eds). JW Wallace & RL Mansell. Plenum Press.
Flaherty, L, Quiring, D. 2008. Plant module size and dose of gall induction stimulus influence gall induction and galler performance. Oikos 117: 1601-1608. http://dx.doi.org/10.1111/j.1600-0706.2008.16555.x
Fleck, T, Fonseca, CR. 2007. Hypotheses for the richness of gall insects: a review considering the intraespecific, interespecific and community levels. Neotropical Biology and Conservation 2: 36-45.
Gotelli, NJ, Entsminger, GL, 2001. EcoSim: Null Models Software for Ecology. Version 7.0. Acquired Intelligence Inc & Kesey-Bear.
Hammer, Ø, Harper, DA, Ryan, PD. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 9.
Haysom, KA, Coulson, JC. 1998. The Lepidoptera fauna associated with Calluna vulgaris: effects of plant architecture on abundance and diversity. Ecol Entomol 23: 377-385. https://doi.org/10.1046/j.1365-2311.1998.00152.x
Höglund, S, 2014. Timing of growth determines fitness and performance of a galling insect on willow. Ecol Entomol 39: 159-167. https://doi.org/10.1111/een.12078
Hood, GR, OTT, JR. 2010. Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore. Oecologia 162: 673-683. https://doi.org/10.1007/s00442-009-1492-9
Horner, JD, Abrahamson, WG. 1992. Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore. Oecologia 90: 323-332. https://doi.org/10.1007/BF00317688
Jeffries, M J, Lawton, JH. 1984. Enemy free space and the structure of ecological communities. Biol J Linn Soc 23: 269-286. https://doi.org/10.1111/j.1095-8312.1984.tb00145.x
Johansson, J, Kristensen, NP, Nilsson, JÅ, Jonzén, N. 2015. The eco-evolutionary consequences of interspecific phenological asynchrony–a theoretical perspective. Oikos 124: 102-112. https://doi.org/10.1111/oik.01909
Kaplan, ID, Robert, F. 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10: 977-994. https://doi.org/10.1111/j.1461-0248.2007.01093.x
Kelch, NS, Neves, FS, Fernandes, GW, Wirth, R. 2016. Mechanisms driving galling success in a fragmented landscape: synergy of habitat and top-down factors along temperate forest edges. PloS One 11: e 0157448. https://doi.org/10.1371/journal.pone.0157448.t002
Kuchenbecker, J, Fagundes, M. 2018. Diversity of insects associated with two common plants in the Brazilian Cerrado: Responses of two guilds of herbivores to bottom-up and top-down forces. Eur J Entomol 115: 354-363. https://doi.org/10.14411/eje.2018.035
Lara, DP, Oliveira, LA, Azevedo, IF, Xavier, MF, Silveira, FA, Carneiro, MAA, Fernandes, GW. 2008. Relationships between host plant architecture and gall abundance and survival. Rev Bras Entomol 52: 78-81. http://dx.doi.org/10.1590/S0085-56262008000100014
Larson, KC, Whitham, TG. 1997. Competition between gall aphids and natural plant sinks: plant architecture a vects resistance to galling. Oecologia 109: 575-582. https://doi.org/10.1007/s004420050119
Lawton, JH, Strong, DR. 1981. Community patterns and competition in folivorous insects. Am. Nat.118: 317–338. https://doi.org/10.1086/283826
Lawton, JH. 1983. Plant architecture and the diversity of phytophagous insect. Annul Rev Entomol 28: 23-39. https://doi.org/10.1146/annurev.en.28.010183.000323
Mopper S.2005. Phenology - how time creates spatial structure in endophagous insect populations. A Zool Fenn 42: 327-333.
Marquis, RJ, Lill, T, Piccinni, A. 2002. Effect of plant architecture on colonization and damage by leaftying caterpillars of Quercus alba. Oikos 99: 531-537. https://doi.org/10.1034/j.1600-0706.2002.11897.x
Morin, X, Fahse, L, Scherer-Lorenzen, M, Bugmann, H. 2011. Tree species richness promotes productivity in temperate forests through strong complementarity between species. Ecol Lett 14: 1211-1219. https://doi.org/10.1111/j.1461-0248.2011.01691.x
Neves, FS, Araújo, LS, Espírito-Santo, MM, Fagundes, M, Fernandes, GW, Sanchez-Azofeifa, GA, & Quesada, M. 2010. Canopy herbivory and insect herbivore diversity in a dry forest–savanna transition in Brazil. Biotropica 42: 112-118. https://doi.org/10.1111/j.1744-7429.2009.00541.x
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Price, PW, Fernandes, GW, Waring, GL. 1987. Adaptive nature of insect galls. Environ Entomol16: 15-24. https://doi.org/10.1093/ee/16.1.15
Price, P, Roininen, H, Zinovjev, AG. 1998. Adaptive radiation of gall-inducing sawflies in relation to architecture and geographic range of willow host plants. In: G. Csóka; W. J. Mattson;G. N. Stone & P. W. Price (eds). Biology of gall-inducing arthropods. United States Department ogf Agriculture Forest Service.
Queiroz, ACM, Costa, FV, Neves, FS, Fagundes, M. 2013. Does leaf ontogeny lead to changes in defensive strategies against insect herbivores?. Arthropod Plant Interact 7: 99-107. https://doi.org/10.1007/s11829-012-9224-1
Ramos LF, Solar RRC, Santos HT, Fagundes M. 2019. Variation in community structure of gall-inducing insects associated with a tropical plant supports the hypothesis of competition in stressful habitats. Ecol Evol 19: 1-12. https://doi.org/10.1002/ece3.5827
Ribas, CR, Schoereder, JH. 2002. Are all ant mosaics caused by competition? Oecologia 131: 606-611. https://doi.org/10.1007/s00442-002-0912-x
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Araújo, WSD, Silva, IPA, Santos, BBD, Gomes-Klein, VL. 2013. Host plants of insect-induced galls in areas of cerrado in the state of Goiás, Brazil. Acta Bot Brasilica 27: 537-542. http://dx.doi.org/10.1590/S0102-33062013000300011
Carneiro, MAA, Borges, RAX, Araújo, APA, Fernandes, GWA. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev Bras Entomol 53: 570-592. http://dx.doi.org/10.1590/S0085-56262009000400007.
Cody, ML, Diamond, JM. 1975. Ecology and evolution of communities. Press, Havard.
Cornelissen, T, Stiling, P. 2008. Clumped distribution of oak leaf miners between and within plants. Basic App Ecol 9: 67-77. https://doi.org/10.1016/j.baae.2006.08.007
Cornelissen, TCG, Viana, JPR, Silva, B. 2013. Interspecific competition influences the organization of a diverse sessile insect community. Acta Oecol 52: 15-18. https://doi.org/10.1016/j.actao.2013.07.001
Costa, FV, Fagundes, M, Neves, FS. 2010. Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffi (Fabaceae). Ecología Austral 20: 9-17.
Costa, FV, Neves, FS, Silva, JO, Fagundes, M. 2011. Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod Plant Interact 5: 9-18. https://doi.org/10.1007/s11829-010-9111-6.
Costa, VF, Medeiros de Queiroz, AC, Bicalho, MML, Reis Júnior, R, Fagundes, M. 2016. Resource allocation in Copaifera langsdorffii (Fabaceae): how supra-annual fruiting affects plant traits and herbivory? Rev Biol Trop 64: 507-520.
Coutinho, RD, Cuevas-Reyes, P, Fernandes, GW, Fagundes, M. 2019. Community structure of gall-inducing insects associated with a tropical shrub: regional, local and individual patterns. Trop Ecol 60: 74-82. http://dx.doi.org/10.1007/s42965-019-00010-7
Cuevas-Reys, P, Siebe, C, Martinez-Ramos, M, Oyama, K. 2003. Species richness of gall-forming insects in a tropical rain forest: correlations with plant diversity and soil fertility. Biodivers Conserv 12: 411-422. https://doi.org/10.1023/A:1022415907109
Cuevas-Reyes, P, Quesada, M, Hanson, P, Dirzo, R, Oyama, K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life-forms, host plant age and plant density. J Ecol 92:707-716. https://doi.org/10.1111/j.0022-0477.2004.00896.x
Development Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing,Vienna. http://www.R-project.org
Dwyer, JD. 1951. The central American, west Indian, and South American species of Copaifera (Caesalpiniaceae). Brittonia 7: 143-172. http://doi.org/10.2307/2804703
Egan, SP, Ott, JR. 2007. Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88: 2868-2879. http://doi.org/10.1890/06-1303.1
Espírito-Santo, MM, Neves, FS, Andrade-Neto, FR., Fernandes, GW. 2007. Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia 153: 353-364. https://doi.org/10.1007/s00442-007-0737-8
Fagundes, M, Neves, FS, Fernandes, GW. 2005. Direct and indirect interactions involving ants, insect herbivores, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae). Ecol Entomol 30: 28-35. https://doi.org/10.1111/j.0307-6946.2005.00668.x
Fagundes, M, Wilson, FG. 2011. Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): responses of gall-forming and free-feeding insects to latitudinal variation. Rev Biol Trop 59: 1419-1432. https://doi.org/10.15517/rbt.v0i0.3408
Fagundes, M. 2014. Galling Insect Community Associated with Copaifera langsdorffii (Fabaceae): The Role of Inter- and Intra-annual Host Plant Phenology. In: Fernandes G., Santos J. (eds). Neotropical Insect Galls. Springer, Dordrecht. http://dx.doi.org/10.1007/978-94-017-8783_11
Fagundes, M, Xavier, RCF, Faria, ML, Lopes, LGO, Cuevas?Reyes, P, Reis?Junior, R. 2018. Plant phenological asynchrony and community structure of gall?inducing insects associated with a tropical tree species. Ecol Evol 8: 10687-10697. http://dx.doi.org/10.1002/ece3.4477
Fagundes, M, Barbosa, EM, Oliveira, JBBS, Brito, BGS, Freitas, KT, Reis-Junior, R. 2019. Galling inducing insects associated with a tropical invasive shrub: the role of resource concentration and species interactions. Ecología Austral 29: 12-19.
Feeny, P. 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry. (eds). JW Wallace & RL Mansell. Plenum Press.
Flaherty, L, Quiring, D. 2008. Plant module size and dose of gall induction stimulus influence gall induction and galler performance. Oikos 117: 1601-1608. http://dx.doi.org/10.1111/j.1600-0706.2008.16555.x
Fleck, T, Fonseca, CR. 2007. Hypotheses for the richness of gall insects: a review considering the intraespecific, interespecific and community levels. Neotropical Biology and Conservation 2: 36-45.
Gotelli, NJ, Entsminger, GL, 2001. EcoSim: Null Models Software for Ecology. Version 7.0. Acquired Intelligence Inc & Kesey-Bear.
Hammer, Ø, Harper, DA, Ryan, PD. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 9.
Haysom, KA, Coulson, JC. 1998. The Lepidoptera fauna associated with Calluna vulgaris: effects of plant architecture on abundance and diversity. Ecol Entomol 23: 377-385. https://doi.org/10.1046/j.1365-2311.1998.00152.x
Höglund, S, 2014. Timing of growth determines fitness and performance of a galling insect on willow. Ecol Entomol 39: 159-167. https://doi.org/10.1111/een.12078
Hood, GR, OTT, JR. 2010. Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore. Oecologia 162: 673-683. https://doi.org/10.1007/s00442-009-1492-9
Horner, JD, Abrahamson, WG. 1992. Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore. Oecologia 90: 323-332. https://doi.org/10.1007/BF00317688
Jeffries, M J, Lawton, JH. 1984. Enemy free space and the structure of ecological communities. Biol J Linn Soc 23: 269-286. https://doi.org/10.1111/j.1095-8312.1984.tb00145.x
Johansson, J, Kristensen, NP, Nilsson, JÅ, Jonzén, N. 2015. The eco-evolutionary consequences of interspecific phenological asynchrony–a theoretical perspective. Oikos 124: 102-112. https://doi.org/10.1111/oik.01909
Kaplan, ID, Robert, F. 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10: 977-994. https://doi.org/10.1111/j.1461-0248.2007.01093.x
Kelch, NS, Neves, FS, Fernandes, GW, Wirth, R. 2016. Mechanisms driving galling success in a fragmented landscape: synergy of habitat and top-down factors along temperate forest edges. PloS One 11: e 0157448. https://doi.org/10.1371/journal.pone.0157448.t002
Kuchenbecker, J, Fagundes, M. 2018. Diversity of insects associated with two common plants in the Brazilian Cerrado: Responses of two guilds of herbivores to bottom-up and top-down forces. Eur J Entomol 115: 354-363. https://doi.org/10.14411/eje.2018.035
Lara, DP, Oliveira, LA, Azevedo, IF, Xavier, MF, Silveira, FA, Carneiro, MAA, Fernandes, GW. 2008. Relationships between host plant architecture and gall abundance and survival. Rev Bras Entomol 52: 78-81. http://dx.doi.org/10.1590/S0085-56262008000100014
Larson, KC, Whitham, TG. 1997. Competition between gall aphids and natural plant sinks: plant architecture a vects resistance to galling. Oecologia 109: 575-582. https://doi.org/10.1007/s004420050119
Lawton, JH, Strong, DR. 1981. Community patterns and competition in folivorous insects. Am. Nat.118: 317–338. https://doi.org/10.1086/283826
Lawton, JH. 1983. Plant architecture and the diversity of phytophagous insect. Annul Rev Entomol 28: 23-39. https://doi.org/10.1146/annurev.en.28.010183.000323
Mopper S.2005. Phenology - how time creates spatial structure in endophagous insect populations. A Zool Fenn 42: 327-333.
Marquis, RJ, Lill, T, Piccinni, A. 2002. Effect of plant architecture on colonization and damage by leaftying caterpillars of Quercus alba. Oikos 99: 531-537. https://doi.org/10.1034/j.1600-0706.2002.11897.x
Morin, X, Fahse, L, Scherer-Lorenzen, M, Bugmann, H. 2011. Tree species richness promotes productivity in temperate forests through strong complementarity between species. Ecol Lett 14: 1211-1219. https://doi.org/10.1111/j.1461-0248.2011.01691.x
Neves, FS, Araújo, LS, Espírito-Santo, MM, Fagundes, M, Fernandes, GW, Sanchez-Azofeifa, GA, & Quesada, M. 2010. Canopy herbivory and insect herbivore diversity in a dry forest–savanna transition in Brazil. Biotropica 42: 112-118. https://doi.org/10.1111/j.1744-7429.2009.00541.x
Ozaki, K, Yukawa, J, Ohgushi, T, Price, PW. 2014. Galling Arthropods and Their Associates. Springer Verlag, Japão. https://doi.org/10.1007/4-431-32185-3
Price, PW, Fernandes, GW, Waring, GL. 1987. Adaptive nature of insect galls. Environ Entomol16: 15-24. https://doi.org/10.1093/ee/16.1.15
Price, P, Roininen, H, Zinovjev, AG. 1998. Adaptive radiation of gall-inducing sawflies in relation to architecture and geographic range of willow host plants. In: G. Csóka; W. J. Mattson;G. N. Stone & P. W. Price (eds). Biology of gall-inducing arthropods. United States Department ogf Agriculture Forest Service.
Queiroz, ACM, Costa, FV, Neves, FS, Fagundes, M. 2013. Does leaf ontogeny lead to changes in defensive strategies against insect herbivores?. Arthropod Plant Interact 7: 99-107. https://doi.org/10.1007/s11829-012-9224-1
Ramos LF, Solar RRC, Santos HT, Fagundes M. 2019. Variation in community structure of gall-inducing insects associated with a tropical plant supports the hypothesis of competition in stressful habitats. Ecol Evol 19: 1-12. https://doi.org/10.1002/ece3.5827
Ribas, CR, Schoereder, JH. 2002. Are all ant mosaics caused by competition? Oecologia 131: 606-611. https://doi.org/10.1007/s00442-002-0912-x
Richards, LA, Dyer, LA, Forister, ML, Smilanich, AM, Dodson, CD, Leonard, MD, Jeffrey, CS. 2015. Phytochemical diversity drives plant-insect community diversity. Proc Natl Acad Sci 112: 10973-10978. https://doi.org/10.1073/pnas.1504977112
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