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Community structure of gall-inducing insects associated with a tropical shrub: regional, local and individual patterns

  • Ritiely Durães Coutinho
  • Pablo Cuevas-Reyes
  • G. Wilson Fernandes
  • Marcílio FagundesEmail author
Research Article

Abstract

The organization of gall-inducing insect communities can be affected by environmental factors and host plant traits that may operate at different spatial scales. Using Copaifera oblongifolia (Fabaceae), we evaluated the organization of their associated gall-inducing insect species in different spatial scales considering the following hypotheses: (i) the community of gall-inducing insects will be different between different populations of C. oblongifolia; (ii) plant individuals with a greater number of neighbours (host plant density) will have a greater diversity of gall-inducing insects; (iii) and more structurally complex plants will support a greater diversity of gall-inducing insects. Data were collected from the three different populations of C. oblongifolia located in abandoned pastures of three different municipalities in northern Minas Gerais, Brazil. We recorded a total of 17,843 galls belonging to 15 different gall-inducing insect species associated to 60 C. oblongifolia plants sampled in the three populations (20 individuals per population). Abundance, richness and composition of gall-inducing insect species were different between the populations, suggesting that local environmental conditions influenced the gall-inducing insect community at a regional scale. Host plant density negatively affected the richness and abundance of gall-inducing insects per plant. Our data did not corroborate the hypothesis of resource concentration, perhaps due to the effect of resource dilution. The biomass of the host plant positively influenced the abundance of gall-inducing insects per plant. However, the interaction between plant density and biomass of the plant suggests that plants with greater structural complexity are more attacked by gall-inducing insects in plots with lower number of neighbours.

Keywords

Community organization Environmental filtering Gall-inducing insect diversity Plant architecture Resource dilution effects Specialist herbivores 

Notes

Acknowledgements

The authors would like to thank the trainees of the Laboratório de Biologia da Conservação of Unimontes for the support during the field works. The authors also acknowledge CNPq and FAPEMIG for research grants. The Pos-graduated Programme of Biodiversity (PPG-BURN) of Unimontes and the Projeto Jequitaí (CODEVASF/SEAPA-MG) provide all logistical support during field work.

References

  1. Araújo WS, Santos BB, Guilherme FAG, Scareli-Santos C (2014) Galling insects in the brazilian cerrado: ecological patterns and perspectives. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Dordrecht, pp 257–272Google Scholar
  2. Arriola ÍA, Melo-Jr JCF, Isaias RMS (2015) Questioning the environmental stress hypothesis for gall diversity of restinga vegetation on dunes. Rev Biol Trop 63:959–970CrossRefGoogle Scholar
  3. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annul Rev Entomol 47:817–844CrossRefGoogle Scholar
  4. Bailey R, Schönrogge K, Cook JM, Melika G, Csóka G, Thuróczy C, Stone GN (2009) Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol 7:e1000179CrossRefGoogle Scholar
  5. Bazzaz FA (1991) Habitat selection in plants. Am Nat 137:116–130CrossRefGoogle Scholar
  6. Blanche KR (1994) Insect induced galls on Australian vegetation. In: Price PW, Mattson WJ, Baranchikov YN (eds) The ecology and evolution of gall-forming insects. United States Department of Agriculture, Saint Paul, pp 49–55Google Scholar
  7. Carneiro MAA, Borges RAX, Araújo APA, Fernandes GW (2009) Gall inducing insects from southern portion of the Espinhaço Range, Minas Gerais, Brazil. Rev Brasileira de Entomol 539:570–592CrossRefGoogle Scholar
  8. Coelho MS, Carneiro MAA, Branco CA, Borges RAX, Fernandes GW (2017) Galling insects of the Brazilian Páramos: species richness and composition along high-altitude grasslands. Environ Entomol 46:1243–1253CrossRefGoogle Scholar
  9. Collevatti RG, Sperber CF (1997) The gall maker Neopelma baccharidis Burck. (Homoptera: Psyllidae) on Baccharis dracunculifolia. (Asteraceae): individual, local, and regional patterns. An Soc Entomol Brasil 26:45–53CrossRefGoogle Scholar
  10. Cornell HV, Lawton JH (1992) Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. J Anim Ecol 61:1–12CrossRefGoogle Scholar
  11. Costa FV, Fagundes M, Neves FS (2010) Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Ecol Austral 20:9–17Google Scholar
  12. Costa FV, Queiroz ACM, Maia MLB, Reis-Júnior R, Fagundes M (2016) Resource allocation in Copaifera langsdorffii (Fabaceae): how a supra-annual fruiting affects plant traits and herbivory? Rev Biol Trop 64:507–520CrossRefGoogle Scholar
  13. 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 92:707–716CrossRefGoogle Scholar
  14. 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 12:411–422CrossRefGoogle Scholar
  15. Egan SP, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2868–2879CrossRefGoogle Scholar
  16. 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 153:353–364CrossRefGoogle Scholar
  17. Fagundes M, Fernandes GW (2011) Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): responses of gall-forming and free-feeding insects to latitudinal variation. Rev Biol Trop 59:1419–1432Google Scholar
  18. 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 30:28–35CrossRefGoogle Scholar
  19. Fagundes M, Xavier RCF, Faria ML, Cuevas-Reyes P, Lopes LG, Reis-Junior R (2018) Plant phenological asynchrony and community structure of gall-inducing insects in a super-host tropical tree species. Ecol Evol 8:10687–10697CrossRefGoogle Scholar
  20. 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 29:12–19Google Scholar
  21. Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interactions between plants and insects. Recent advances in phytochemistry. Springer, Boston, pp 1–40Google Scholar
  22. Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness. Oecologia 76:161–167CrossRefGoogle Scholar
  23. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20CrossRefGoogle Scholar
  24. Fernandes GW, Paula AS, Loyola R (1995) Distribuição diferencial de insetos galhadores entre habitats e seu possível uso como bioindicadores. Vida Silvestre Neotropical 4:133–139Google Scholar
  25. Floate KD, Fernandes GW, Nilsson JA (1996) Distinguishing intrapopulational categories of plants by their insect faunas: galls on rabbit brush. Oecologia 105:221–229CrossRefGoogle Scholar
  26. Gomez JP, Robinson S, Ponciano JM (2018) Asymmetric effects of environmental filtering on the assembly of tropical bird communities along a moisture gradient. bioRxiv.  https://doi.org/10.1101/251249 Google Scholar
  27. Gonçalves-Alvim SJ, Fernandes GW (1991) Galling insect (Insecta) communities in different “cerrado” physiognomies in Minas Gerais, Brazil. Rev Bras Zool 18:289–305CrossRefGoogle Scholar
  28. Grandez-Rios JM, García-Villacorta R, Cuevas-Reyes P, Araújo WS (2015) Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Rev de Biol Neotrop 12:92–103CrossRefGoogle Scholar
  29. Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  30. Inbar M, Doostdar H, Mayer RT (2001) Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94:228–235CrossRefGoogle Scholar
  31. Joy JB, Crespi BJ (2007) Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61:784–795CrossRefGoogle Scholar
  32. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994CrossRefGoogle Scholar
  33. 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:e0157448CrossRefGoogle Scholar
  34. Kraft NJB, Adler PB, Godoy O, James EC, Fuller S, Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599CrossRefGoogle Scholar
  35. Kuchenbecker J, Fagundes M (2018) Diversity of insects associated with two common plants of the Brazilian Cerrado: responses of two guilds of herbivores to bottom-up and top-down forces. Eur J Entomol 115:354–363CrossRefGoogle Scholar
  36. Lara DP, Oliveira LA, Azevedo IFP, Xavier MF, Silveira FA, Carneiro MAA, Fernandes GW (2008) Relationships between host plant architecture and gall abundance and survival. Rev Brasileira de Entomol 52:78–81CrossRefGoogle Scholar
  37. Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant? Oikos 72:155–160CrossRefGoogle Scholar
  38. Lawton JH (1984) Herbivore community organization: general models and specific tests with phytophagous insects. In: Price PW, Slobodchikoff CN, Gaud WS (eds) A new ecology: novel approaches to interactive system. Wiley, New York, pp 329–352Google Scholar
  39. Lázaro-González A, Hódar JA, Zamora R (2017) Do the arthropod communities on a parasitic plant and its hosts differ? Eur J Entomol 114:215–221CrossRefGoogle Scholar
  40. Leite GLD, Veloso RVS, Zanuncio JC, Azevedo AM, Silva JL, Wilcken CF, Soares MA (2017) Architectural diversity and galling insects on Caryocar brasiliense trees. Sci Rep 7:1–7CrossRefGoogle Scholar
  41. Maia VC, Magenta MAG, Martins SE (2008) Occurrence and characterization of insect galls at restinga areas of Bertioga (São Paulo, Brazil). Biota Neotrop 8:167–197CrossRefGoogle Scholar
  42. Marques ESDA, Price PW, Cobb NS (2000) Resource abundance and insect herbivore diversity on woody fabaceous desert plants. Environ Entomol 29:696–703CrossRefGoogle Scholar
  43. Oliveira DC, Mendonça-Jr MS, Moreira ASFP, Lemos-Filho JP, Isaias RMS (2013) Water stress and phenological synchronism between Copaifera langsdorffii (Fabaceae) and multiple galling insects: formation of seasonal patterns. J Plant Interact 8:225–233CrossRefGoogle Scholar
  44. Oliveira DC, Isaias RMS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L (2016) Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J Insect Physiol 84:103–113CrossRefGoogle Scholar
  45. Otway SJ, Hector A, Lawton JH (2005) Resource dilution effects on specialist insect herbivores in a grassland biodiversity experiment. J Anim Ecol 74:234–240CrossRefGoogle Scholar
  46. Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24CrossRefGoogle Scholar
  47. Price PW, Fernandes GW, Lara ACF, Brawn J, Barrios H, Wright MG, Ribeiro SP, Rothcliff N (1998) Global patterns in local number of insect galling species. J Biogeogr 25:581–591CrossRefGoogle Scholar
  48. Raman A, Schaefer CW, Withers TM (2005) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Enfield, pp 240–271Google Scholar
  49. Rhainds M, English-Loeb G (2003) Testing the resource concentration hypothesis with tarnished plant bug on strawberry: density of hosts and patch size influence the interaction between abundance of nymphs and incidence of damage. Ecol Entomol 28:348–358CrossRefGoogle Scholar
  50. Richardson RA, Body M, Warmund MR, Schultz JC, Appel HM (2017) Morphometric analysis of young petiole galls on the narrow-leaf cottonwood, Populus angustifolia, by the sugarbeet root aphid, Pemphigus betae. Protoplasma 254:203–216CrossRefGoogle Scholar
  51. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124CrossRefGoogle Scholar
  52. Rossi MN, Rodrigues LM, Ishino MN, Kestring D (2011) Oviposition pattern and within-season spatial and temporal variation of pre-dispersal seed predation in a population of Mimosa bimucronata trees. Arthropod Plant Interact 5:209–217CrossRefGoogle Scholar
  53. Santos IM, Lima VP, Soares EKS, Paula Santos IM, Lima VP, Soares EKS, Paula M, Calado DC (2018) Insect galls in three species of Copaifera L.(Leguminosae, Caesalpinioideae) occurring sympatrically in a Cerrado area (Bahia, Brazil). Biota Neotropica 18:e20170356Google Scholar
  54. Shorthouse JD (1993) Adaptations of gall wasps of the genus Diplolepis (Hymenoptera: Cynipidae) and the role of gall anatomy in cynipid systematics. Mem Entomol Soc of Can 125:139–163CrossRefGoogle Scholar
  55. Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insect—nature’s most sophicticated herbivores. Basic Appl Ecol 6:407–411CrossRefGoogle Scholar
  56. Silva LL, Santos RC, Fernandes M (2017) Linking Avicennia germinans (Acanthaceae) architecture to gall richness and abundance in Brazilian Amazon mangroves. Biotropica 49:784–791CrossRefGoogle Scholar
  57. Souza ML, Fagundes M (2016) Seed predation of Copaifera langsdorffii (Fabaceae): a tropical tree with supra-annual fruiting. Plant Species Biol 32:66–73CrossRefGoogle Scholar
  58. Stireman JO, Nason JD, Heard SB (2005) Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59:2573–2587CrossRefGoogle Scholar
  59. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522CrossRefGoogle Scholar
  60. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL: http://www.R-project.org/Google Scholar
  61. Toma TS, Fernandes GW, de Souza DG, Tabarelli M, Santos JC (2014) Galling insects as indicators of habitat quality. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Dordrecht, pp 143–150Google Scholar
  62. Veldtman R, McGeoch MA (2003) Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28:1–13CrossRefGoogle Scholar
  63. Veloso AC, Silva PS, Siqueira WK, Duarte KL, Gomes IL, Santos HT, Fagundes M (2017) Intraspecific variation in seed size and light intensity affect seed germination and initial seedling growth of a tropical shrub. Acta Bot Brasilica 31:736–741CrossRefGoogle Scholar
  64. Waring GL, Price PW (1990) Plant water stress and gall formation (Cecidomyiidae: Asphondylia spp.) on creosote bush. Ecol Entomol 115:87–95CrossRefGoogle Scholar
  65. Weis AE, Walton R, Crego CL (1988) Reactive plant tissue sites and the population biology of gall makers. Annu Rev Entomol 33:467–486CrossRefGoogle Scholar
  66. Whipple AV, Abrahamson WG, Khamiss MA, Heinrich PL, Urian AG, Northridge EM (2009) Host-Race formation: promoted by fhenology, constrained by heritability. J Evol Biol 22:793–804CrossRefGoogle Scholar
  67. Yamamura K (2002) Biodiversity and stability of herbivore populations: influences of the spatial sparseness of food plants. Popul Ecol 44:33–40CrossRefGoogle Scholar

Copyright information

© International Society for Tropical Ecology 2019

Authors and Affiliations

  • Ritiely Durães Coutinho
    • 1
  • Pablo Cuevas-Reyes
    • 2
  • G. Wilson Fernandes
    • 3
  • Marcílio Fagundes
    • 1
    Email author
  1. 1.Laboratório de Biologia da ConservaçãoDBG/CCBS/Universidade Estadual de Montes ClarosMontes ClarosBrazil
  2. 2.Laboratorio de Ecología de Interacciones Bióticas, Facultad de BiologíaUniversidad Michoacana de San Nicolás de Hidalgo, Ciudad UniversitariaMoreliaMexico
  3. 3.Ecologia Evolutiva & Biodiversidade/DBGICB/Universidade Federal de Minas GeraisBelo HorizonteBrazil

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