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Mexican Gall-Inducing Insects: Importance of Biotic and Abiotic Factors on Species Richness in Tropical Dry Forest

  • Pablo Cuevas-Reyes
  • Norma Angélica Espinosa-Olvera
  • Maldonado-López Yurixhi
  • Ken Oyama
Chapter

Abstract

In this chapter we provide a brief overview of the major abiotic and biotic factors that influence the diversity of gall-inducing insects in a Mexican tropical dry forest. We tested some current hypotheses (plant species richness, plant structural complexity, plant age, resource concentration and soil fertility) that seek to explain the variation in gall-inducing insect species richness in plant communities of deciduous and riparian habitats. Gall-inducing insect species maintain a great specificity on their host plant species; each gall-inducing insect species is associated with a different plant species. A significant positive correlation was found between gall-inducing insect species richness and plant species richness in both habitats. This suggests that radiation of gall-inducing insect species may be associated with plant species richness. Most of the galling species occurred on trees and shrubs but not on herbs and climbers. The structural complexity of these life forms may provide more potential sites to be colonized by gall insects. The frequency of gall-inducing insects was greater on saplings of most host plants, suggesting that early ontogenetic stages hold more sites with undifferentiated tissues or meristems susceptible to gall induction.

In addition, we analyze the spatial distribution of gall-inducing insect species under different geomorphologic units of soils in a Mexican tropical dry forest. Gall-inducing insect species richness was negatively correlated with phosphorous and nitrogen availability. We found low frequency and abundance of galls in fertile soils suggesting that soil fertility affect the spatial distribution of gall-inducing insect favoring incidence, abundance and species richness.

Keywords

Gall-inducing insects Biotic factors Abiotic factors Tropical dry forest 

Notes

Acknowledgements

We thank Alfredo Pérez for plant species identification, Nidia Pérez Nasser for technical support. We thank Paul Hanson for gall-inducing insect identification and the authorities of Chamela and Cuixmala Biosphere reserve for their permission to conduct this study.

References

  1. Ananthakrishan TN (1984) Adaptive strategies in cecidogenous insects. In: Ananthakrishan TN (ed) The biology of gall insects. Oxford and IBH, New Delhi, pp 1–9Google Scholar
  2. Askew RR (1984) The biology of gall-wasps. In: Anathakrishnan TN (ed) The biology of gall-insects. Oxford and IBH, New Delhi, pp 223–271Google Scholar
  3. Basset Y (2001) Communities of insect herbivores foraging on saplings versus mature trees of Pourouma bicolor (Cecropiaceae) in Panama. Oecologia 129:253–260CrossRefGoogle Scholar
  4. Bearsley WJ (1982) On taxonomy of the genus Pseudopsylla Froggatt, with a redescription of the type species (Homoptera: Coccoidea). Proc Hawaiian Entomol Soc 24:31–35Google Scholar
  5. Blanche KR (1994) Insect induced galls on Australian vegetation. In: Price PW, Mattson WJ, Baranchikov Y (eds) The ecology and evolution of gall-forming insects. Forest service US department of agriculture, St. Paul, pp 49–55Google Scholar
  6. Blanche KR, Ludwig AJ (2001) Species richness of gall-inducing insects and host plants along and altitudinal gradient in Big Bend National Park. Texas Am Midl Nat 145:219–232CrossRefGoogle Scholar
  7. Blanche KR, Westoby M (1995) Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76:2334–2337CrossRefGoogle Scholar
  8. Bullock SH (1985) Breeding systems in the flora of tropical deciduous forest in Mexico. Biotropica 4:287–301CrossRefGoogle Scholar
  9. Castellanos I, Cuevas-Reyes P, Rios-Casanova L, Oyama K, Quesada M (2006) Abundance of two gall midges insects on Poulsenia armata (Moraceae): importance of host plant size and local light environment in a Mexican tropical rain forest. Biotropica 38:569–563CrossRefGoogle Scholar
  10. Clinebell RR, Phillip OL, Gentry AH, Stark N, Zuuring H (1995) Prediction of Neotropical tree and liana species richness from soil and climatic data. Biodiv Conserv 4:56–90CrossRefGoogle Scholar
  11. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Ann Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  12. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  13. Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by Cynipinae (Hymenoptera): Why and how? Am Midl Nat 110:225–234CrossRefGoogle Scholar
  14. Cornell HV (1990) Survivorship, life history, and concealment: a comparison of leaf miners and gall formers. Am Nat 136:581–597CrossRefGoogle Scholar
  15. 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
  16. Cotler E, Durán E, Siebe C (2003) Caracterización morfo-edafológica y calidad de sitio de un bosque tropical caducifolio. In: Noguera FA, Vega RHJ, García ANA, Quesada M (eds) Historia natural de Chamela. Universidad Nacional Autónoma de México, Instituto de Biología, México, pp 17–47Google Scholar
  17. Cuevas-Reyes P, Siebe C, Martínez-Ramos M, Oyama K (2003) Species richness of gall-forming insects in a tropical rain forest: correlations with plant diversity and soil fertility. Biodiv Conserv 3:411–422CrossRefGoogle Scholar
  18. Cuevas-Reyes P, Quesada M, Hanson P, Dirzo R, Oyama K (2004a) Diversity of gall-forming 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
  19. Cuevas-Reyes P, Quesada M, Siebe C, Oyama K (2004b) Spatial patterns of herbivory by gall-forming insects: a test to the soil fertility hypothesis in a Mexican tropical dry forest. Oikos 107:181–189CrossRefGoogle Scholar
  20. Cuevas-Reyes P, Quesada M, Oyama K (2006) Abundance and leaf damage caused by gall-inducing insects in a Mexican tropical dry forest. Biotropica 38:107–115Google Scholar
  21. Cuevas-Reyes P, De Olivera-Ker FT, Fernandes GW, Bustamante M (2011) Abundance of gall-inducing insect species in sclerophyllous savanna: understanding the importance of soil fertility using an experimental approach. J Trop Ecol 27:1–10CrossRefGoogle Scholar
  22. De Souza MM (2001) Galling insect diversity patterns: the resource synchronization hypothesis. Oikos 95:171–176CrossRefGoogle Scholar
  23. Dodson G, George SB (1986) Examination of two morphs of gall-forming Aciurina (Diptera: Tephritidae): ecological and genetic evidence for species. Biol J Linn Soc 29:63–79CrossRefGoogle Scholar
  24. Feeny P (1976) Plant apparency and the diversity of phytophagous insects. Rec Adv Phytochem 10:1–22Google Scholar
  25. Fernandes GW, Lara ACF (1993) Diversity of Indonesian gall-forming herbivores along altitudinal gradients. Biodiv Lett 1:186–192CrossRefGoogle Scholar
  26. Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76:161–167CrossRefGoogle Scholar
  27. Fernandes GW, Price PW (1991) Comparisons of tropical and temperate galling species richness: the roles of environmental harshness and plant nutrient status. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 91–115Google Scholar
  28. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distributions: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20CrossRefGoogle Scholar
  29. Fernandes GW, Lara ACF, Price PW (1994) The geography of galling insects and the mechanisms that result in patterns. In: Price PW, Mattson WJ, Baranchikov YN, Yuri N (eds) The ecology and evolution of gall forming insects USDA Forest Service Tech. Report NC-174. USDA Forest Service, Minnesota, pp 49–55Google Scholar
  30. Fernandes GW, Araujo RC, Araujo SC, Lombardi JA, Paula AS, Loyola JR, Cornelissen TG (1997) Insects galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia (Sao Paulo) 22:221–244Google Scholar
  31. Floate KD, Fernandes GW, Nilsson JA (1996) Distinguishing intrapopulation categories of plant by their insect faunas: galls on rabbitbrush. Oecologia 105:221–229Google Scholar
  32. Fonseca CR, Fleck T, Fernandes GW (2006) Processes driving ontogenetic succession of galls in a canopy tree. Biotropica 38:514–521CrossRefGoogle Scholar
  33. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–899CrossRefGoogle Scholar
  34. Gagné RJ (1994) The gall midges of the Neotropical region. Cornell University Press, IthacaGoogle Scholar
  35. Gagné RJ (2004) A catalog of the Cecidomyiidae (Diptera) of the world. Mem Entomol Soc Wash 25:1–408Google Scholar
  36. Gilbert LE, Smiley JT (1978) Determinants of local diversity in phytophagous insects: hosts specialists in tropical environments. In: Mound LA, Walo N (eds) Diversity of insect faunas. Symposium of Real Entomologic Society of London, London, pp 89–105Google Scholar
  37. Goncalves-Alvim S, Fernandes GW (2001) Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiv Conserv 10:79–98CrossRefGoogle Scholar
  38. Goncalves-Alvim S, Lana TC, Ranieri BD, Fernandes GW (2006) Test of hypotheses about herbivory and chemical defences of Qualea parviflora (Vochysiaceae) in Brazilian Cerrado. Rev Brasil Bot 34:223–230CrossRefGoogle Scholar
  39. Hartley SE (1988) The inhibition of phenolic biosynthesis in damaged and undamaged birch foliage and its effect on insect herbivores. Oecologia 76:65–70Google Scholar
  40. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compound controlled by the gall-former? Oecologia 113:492–501CrossRefGoogle Scholar
  41. Hartley SE (1999) Are gall insects large rhizobia? Oikos 84:333–339CrossRefGoogle Scholar
  42. Hartley SE, Lawton JH (1992) Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. J Anim Ecol 61:113–119CrossRefGoogle Scholar
  43. Holbrook NM, Whitebeck JL, Mooney HA (1995) Drought responses of neotropical dry forest tress. In: Bullock SH, Mooney HA, Medina E (eds) Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 243–276CrossRefGoogle Scholar
  44. Huston MA (1999) Local processes and regional patterns: appropriate scales for understanding variation in the diversity of plants and animals. Oikos 86:393–401CrossRefGoogle Scholar
  45. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 940:501–528CrossRefGoogle Scholar
  46. Jaramillo VJ, Sanford RL (1995) Nutrient cycling in tropical deciduous forests. In: Bullock SH, Money HA, Medina E (eds) Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 346–361CrossRefGoogle Scholar
  47. Jauffret FD, Shorthouse JD (1998) Diversity of gall-inducing insects and their galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of gall insects-induced galls. Oxford University Press, Oxford, pp 8–33Google Scholar
  48. Koach J, Wool D (1977) Geographic distribution and host specificity of gall-forming aphids (Homoptera, Fordinae) on Pistacia trees in Israel. Marcellia 40:207–216Google Scholar
  49. Lara ACF, Fernandes GW (1996) The highest diversity of galling insects: Serra do Cipó, Brazil. Biodiv Lett 3:111–114CrossRefGoogle Scholar
  50. Larson KC, Whitham TC (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:15–21CrossRefGoogle Scholar
  51. Lawton JH (1983) Plant architecture and diversity of phytophagous insects. Annu Rev Entomol 28:23–29CrossRefGoogle Scholar
  52. Leather SR (1986) Insects species richness of the British Rosaceae: the importance of host range, plant architecture, age of establishment, taxonomic isolation and species-area relationships. J Anim Ecol 55:841–860CrossRefGoogle Scholar
  53. Lott EJ, Bullock SH, Solis-Magallanes JA (1987) Floristic diversity and structure of upland and arroyo forests of Coastal Jalisco. Biotropica 3:228–235CrossRefGoogle Scholar
  54. Mani MS (1964) Ecology of plant galls. Junk, The Hague, 434 ppCrossRefGoogle Scholar
  55. Marquis RJ, Braker HE (1994) Plant-herbivore interactions: diversity, specificity, and impact. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a neotropical rain forest. University of Chicago, Chicago, pp 261–294Google Scholar
  56. Mendonça M d S Jr (2007) Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42:347–357Google Scholar
  57. Mooney HA, Bullock SH, Medina E (1995) Introduction. In: Bullock SH, Money HA, Medina E (eds) Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 1–8CrossRefGoogle Scholar
  58. Novotny V, Missa O (2000) Local versus regional species richness in tropical insects: one lowland site compared with the island of New Guinea. Ecol Entomol 25:445–451CrossRefGoogle Scholar
  59. Nyman T, Widmer A, Roininen H (2000) Evolution of gall morphology and host-plant relationships in willow feeding sawflies (Hymenoptera:Tenthredinidae). Evolution 54:526–533PubMedCrossRefGoogle Scholar
  60. Opler PA, Frankie GH, Baker HG (1980) Comparative phenological studies of treelet and shrubs species in tropical wet and dry forests in the lowlands of Costa Rica. J Anim Ecol 68:167–188CrossRefGoogle Scholar
  61. Oyama K, Pérez-Pérez M, Cuevas-Reyes P, Luna R (2003) Regional and local species richness of gall-forming insects in two tropical rain forest in Mexico. J Tropical Ecol 19:595–598CrossRefGoogle Scholar
  62. Pascual-Alvarado E, Cuevas-Reyes P, Quesada M, Oyama K (2008) Interactions between galling insects and leaf-feeding insects: the role of plant phenolic compounds and their possible interference with herbivores. J Trop Ecol 24:329–336CrossRefGoogle Scholar
  63. Price PW (1991) Patterns in communities along latitudinal gradients. In: Price PW, Lewinson TM, Fernandes GW, Benson WW (eds) Plant animal interactions: evolutionary ecology of tropical and temperate regions. Wiley, New York, pp 51–68Google Scholar
  64. Price PW, Clancy KM (1986) Interaction among three trophic levels: gall size and parasitoid attack. Ecology 67:1593–1600CrossRefGoogle Scholar
  65. Price PW, Fernandes GW, Lara AC, Brawn J, Barrios H, Wright MG, Ribeiro S, Rothcliff N (1998) Global patterns in local number of insect galling species. J Bio 25:581–591Google Scholar
  66. Raupp MJ, Denno RF (1979) The influence of patch size on a guild of sap-feeding insects that inhabit the salt marsh grass Spartina patens. Environ Entomol 8:412–417Google Scholar
  67. Reich PB, Borchert R (1984) Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J Ecol 72:61–74CrossRefGoogle Scholar
  68. Ribeiro KT, Madeira JA, Monteiro RF (1998) Does flooding favour galling insects? Ecol Entomol 23:491–494CrossRefGoogle Scholar
  69. Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171PubMedCrossRefGoogle Scholar
  70. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleraceae). Ecol Monogr 43:95–124CrossRefGoogle Scholar
  71. Rossi AM, Stiling P (1998) The interactions of plant clone and abiotic factors on gall-making midge. Oecologia 116:170–176CrossRefGoogle Scholar
  72. Rzedowski J (1978) Vegetación de México. Editorial Limusa, MéxicoGoogle Scholar
  73. SAS (2000) Categorical data analysis using the SAS system. SAS Institute, CaryGoogle Scholar
  74. Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS, CaryGoogle Scholar
  75. Waring GL, Price PW (1989) Parasitism pressure and radiation of gall forming group (Cecidomyiidae: Asphondylia spp.) on creosote bush (Larrea tridentata). Oecologia 79:293–299Google Scholar
  76. Waring GL, Price PW (1990) Plant water stress and gall formation (Cecidomyiidae: Asphondylia spp.) on creosote bush. Ecol Entomol 15:87–95CrossRefGoogle Scholar
  77. 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
  78. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105CrossRefGoogle Scholar
  79. White TCR (1993) The inadequate environment: nitrogen and abundance of animals. Springer, BerlinCrossRefGoogle Scholar
  80. Williams WM, Benson RN (1966) Transfer of C14 component from Psylla pyricola for to pear seedlings. J Inst Physiol 12:251–254CrossRefGoogle Scholar
  81. Wright MG, Samways MJ (1996) Gall-insect species richness in African Fynbos and Karoo vegetation: the importance of plant species richness. Biodiv Lett 3:151–155CrossRefGoogle Scholar
  82. Wright MG, Samways MJ (1998) Insect species richness tracking plant species richness in a diverse flora: gall-insects in the Cape floristic region, South Africa. Oecologia 115:427–433CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Pablo Cuevas-Reyes
    • 1
  • Norma Angélica Espinosa-Olvera
    • 1
  • Maldonado-López Yurixhi
    • 2
  • Ken Oyama
    • 2
  1. 1.Laboratorio de Ecología de Interacciones Bióticas, Facultad de BiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Escuela Nacional de Estudios Superiores Unidad MoreliaUNAMMoreliaMexico

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