Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-04T21:00:35.913Z Has data issue: false hasContentIssue false

Abundance of gall-inducing insect species in sclerophyllous savanna: understanding the importance of soil fertility using an experimental approach

Published online by Cambridge University Press:  30 September 2011

Pablo Cuevas-Reyes*
Affiliation:
Laboratorio de Ecología de Interacciones Bióticas, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Morelia, Michoacán, México, C. P. 58060 Ecologia Evolutiva & Biodiversidade/DBG, C P 486, ICB/Universidade Federal de Minas Gerais, 31270 901 Belo Horizonte, MG, Brazil
Fabricio T. De Oliveira-Ker
Affiliation:
Ecologia Evolutiva & Biodiversidade/DBG, C P 486, ICB/Universidade Federal de Minas Gerais, 31270 901 Belo Horizonte, MG, Brazil
Geraldo Wilson Fernandes
Affiliation:
Ecologia Evolutiva & Biodiversidade/DBG, C P 486, ICB/Universidade Federal de Minas Gerais, 31270 901 Belo Horizonte, MG, Brazil
Mercedes Bustamante
Affiliation:
Departamento de Botânica, Universidade de Brasília, Brasília DF, Brazil
*
1Corresponding author. Email: [email protected]

Abstract:

Although many studies have now demonstrated that both richness and abundance of gall-inducing insect species are directly and indirectly (via the host plant) influenced by soil quality, the empirical evaluation of it in the field remains anecdotal at best. The effects of soil fertility on richness and abundance of gall-inducing insects associated with a widespread savanna species, Eremanthus glomerulatus, were evaluated under experimental field conditions in Brasilia, central Brazil. The effect of soil fertility on gall-inducing insects species richness was evaluated using three treatments: (1) plots fertilized with nitrogen; (2) plots fertilized with phosphorus; and (3) control plots: soils without fertilization. Species richness of gall-inducing insects (six species of Cecidomyiidae) did not differ among the treatments. Leaves with galls had higher nitrogen concentrations (mean = 15.0 ± 0.5 mg g−1), compared with leaves without galls (mean = 9.0 ± 0.7 mg g−1) on plants that occurred in soils with addition of nitrogen. Similarly, leaves with galls had higher foliar phosphorus concentration (mean = 1.0 ± 0.04 mg g−1) than leaves without galls (mean = 0.6 ± 0.05 mg g−1) in plots with addition of phosphorus. In galled leaves, a negative relationship between gall density and nitrogen concentration was found for one gall-inducing insect species, while three species showed a positive relationship between gall density and leaf nitrogen concentration. A negative relationship between gall density and concentration of leaf phosphorus was observed for four of the six gall-inducing insect species studied. No relationship was found between gall density and leaf nitrogen and phosphorus concentration in ungalled leaves. We argue that foliar nitrogen and phosphorus concentration respond to gall density in galled leaves and therefore, gall-inducing insect species are capable of manipulating their host plant, modifying the foliar nutrients of E. glomerulatus in sclerophyllous savanna.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ABRAHAMSON, W. G. & MCCREA, K. D. 1985. Seasonal nutrient dynamics of Solidago altissima (Compositae). Bulletin of the Torrey Botanical Club 112:414420.CrossRefGoogle Scholar
AERTS, R. & CHAPIN, F. S. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30:167.Google Scholar
ANANTHAKRISHNAN, T. N. 1984. Adaptative strategies in cecidogenous insects. Pp. 19 in Ananthakrishnan, T. N. (ed.). The biology of gall insects. Oxford and IBH, New Delhi.Google Scholar
ANDRADE, L. A. Z., FELFILI, J. M. & VIOLATTI, L. 2002. Fitosociologia de uma área de cerrado denso na recor-IBGE, Brasília, DF. Acta Botanica Brasileira 16:225240.CrossRefGoogle Scholar
BLANCHE, K. R. & LUDWIG, A. J. 2001. Species richness of gall-inducing insects and host plants along and altitudinal gradient in Big Bend National Park, Texas. American Midland Naturalist 145:219232.CrossRefGoogle Scholar
BLANCHE, K. R. & WESTOBY, M. 1995. Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76:23342337.CrossRefGoogle Scholar
BOBBINK, R. K., HICKS, K., GALLOWAY, J., SPRANGER, T., ALKEMADE, R., ASHMORE, M., BUSTAMANTE, M., CINDERBY, S., DAVIDSON, E., DENTENER, F., EMMETT, B., ERISMAN, J. W., FENN, M., GILLIAM, F., NORDIN, A., PARDO, L. & DE VRIES, W. 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications 20:3059.CrossRefGoogle ScholarPubMed
CAMPBELL, C. R. & PLANK, O. C. 1998. Preparation of plant tissue for laboratory analysis. Pp. 3749 in Kalra, Y. P. (ed.). Handbook of reference methods for plant analysis. CRC Press, Boca Raton.Google Scholar
CHAPIN, F. S. 1991. Integrated responses of plants to stress: a centralized system of physiological responses. Bioscience 41:2936.CrossRefGoogle Scholar
CHAPIN, F. S., JOHNSON, D. A. & MACKENDRICK, J. D. 1980. Seasonal movement of nutrients in plants of differing growth form in an Alaskan tundra ecosystem: implications for herbivory. Journal of Ecology 68:189209.Google Scholar
COBB, N. S., MOPPER, S., GEHRING, C. A., CAOUETTE, G. M., CHRISTENSEN, K. M. & WHITHAM, T. G. 1997. Increased moth herbivory associated with environmental stress of pinyon pine at local and regional levels. Oecologia 109:389397.CrossRefGoogle ScholarPubMed
COLEY, P. D., BRYANT, J. P. & CHAPIN, F. S. 1985. Resource availability and plant antiherbivore defense. Science 230:895899.CrossRefGoogle ScholarPubMed
CRAIG, T. P., ITAMI, J. K. & PRICE, P. W. 1989. A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:16911699.CrossRefGoogle Scholar
CRAWLEY, M. J., JOHNSTON, A. E., SILVERTOWN, J., DODD, M., DE MAZANCOURT, C., HEART, M. S., HENMAN, D. F. & EDWARDS, G. R. 2005. Determinants of species richness in the park grass experiment. American Naturalist 165:179192.CrossRefGoogle ScholarPubMed
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. Biodiversity and Conservation 12:411422.CrossRefGoogle Scholar
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. Journal of Ecology 92:707716.CrossRefGoogle Scholar
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 107:181189.CrossRefGoogle Scholar
CUEVAS-REYES, P., QUESADA, M. & OYAMA, K. 2006. Abundance and leaf damage caused by gall-inducing insects in a Mexican tropical dry forest. Biotropica 38:107115.CrossRefGoogle Scholar
DREGER-JAUFFRET, J. D. & SHORTHOUSE, J. D. 1992. Diversity of gall-inducing insects and their galls. Pp. 834 in Shorthouse, D. & Rohfritsch, O. (eds.). Biology of insect-induced galls. Oxford University Press, New York.Google Scholar
ECKSTEIN, R. L., KARLSSON, P. S. & WEIH, M. 1999. Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytologist 143:177189.CrossRefGoogle Scholar
FERNANDES, G. W. & CARNEIRO, M. A. A. 2009. Galhadores. Pp. 1164 in Panizzi, A. R. & Parra, J. R. P. (eds.). Bioecologia e nutrição de insetos–base para o manejo integrado de pragas. Editora Embrapa. Brasília DF.Google Scholar
FERNANDES, G. W. & PRICE, P. W. 1988. Biogeographical gradients in galling species richness: test of hypotheses. Oecologia 76:161167.CrossRefGoogle Scholar
FERNANDES, G. W. & PRICE, P. W. 1991. Comparison of tropical and temperate galling species richness: the roles of environmental harshness and plant nutrient status. Pp. 91115 in Price, P. W., Lewinsohn, T. M., Fernandes, G. W. & Benson, W. W. (eds.). Plant–animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley and Sons, New York.Google Scholar
FERNANDES, G. W. & PRICE, P. W. 1992. The adaptative significance of insect gall distributions: survivorship of species in xeric and mesic habitats. Oecologia 90:1420.CrossRefGoogle ScholarPubMed
FERNANDES, G. W., LARA, C. F. L. & PRICE, P. W. 1994. The geography of galling insects and the mechanisms that result in patterns. Pp. 4248 in Price, P. W., Mattson, W. J. & Barranchikov, Y. (eds.). The ecology and evolution of gall-forming insects. United States Department of Agriculture. Forest Service, St. Paul, Minnesota.Google Scholar
FREEMAN, B. E. & GEOGHAGEN, A. 1987. Size and fecundity in the Jamaican gall-midge Asphondylia boerhaaviae. Ecological Entomology 12:239249.CrossRefGoogle Scholar
FRITZ, R. S., CRABB, B. A. & HOCHWENDER, C. G. 2000. Preference and performance of gall-inducing sawfly: a test of the plant vigor hypothesis. Oikos 89:555563.CrossRefGoogle Scholar
GOUGH, L., OSENBERG, C. W., GROSS, K. L. & COLLINS, S. L. 2000. Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89:428439.CrossRefGoogle Scholar
HARIDASAN, M. 2001. Nutrient cycling as a function of landscape and biotic characteristic in the cerrado of central Brazil. Pp. 6883 in McClain, M. E., Victoria, R. L. & Richey, J. R. (eds.). The biogeochemistry of the Amazon basin. Oxford University Press, New York.Google Scholar
HARTLEY, S. E. & LAWTON, J. H. 1992. Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology 61:113119.CrossRefGoogle Scholar
HELMS, S. E. & HUNTER, E. M. D. 2005. Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids. Oecologia 145:197204.CrossRefGoogle ScholarPubMed
HONEK, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483492.CrossRefGoogle Scholar
KOZOVITS, A. R., BUSTAMANTE, M. M. C., GAROFALO, C. R., BUCCI, S., FRANCO, A. C., GOLDSTEIN, G. & MEINZER, F. C. 2007. Nutrient resorption and patterns of litter production and decomposition in a Neotropical savanna. Functional Ecology 21:10341043.CrossRefGoogle Scholar
LARSSON, S. 1989. Stressful times for the plant stress–insect performance hypothesis. Oecologia 56:277283.Google Scholar
MEIER, M. 1991. Nitratbestimmung in Boden-Proben (N-min-Methode). Laborpraxis 4:244247.Google Scholar
NARDOTO, G. B., BUSTAMANTE, M. M. C., PINTO, A. S. & KLINK, C. A. 2006. Nutrient use efficiency at ecosystem and species level in savanna areas of Central Brazil and impacts of fire. Journal of Tropical Ecology 22:191201.CrossRefGoogle Scholar
OYAMA, K., PÉREZ-PÉREZ, M., CUEVAS-REYES, P. & LUNA, R. 2003. Regional and local species richness of gall-forming insects in two tropical rain forests in México. Journal of Tropical Ecology 19:595598.CrossRefGoogle Scholar
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. Journal of Tropical Ecology 24:329336.CrossRefGoogle Scholar
PEREIRA, B. A., SILVA, M. A. & MENDONÇA, R. 1993. Reserva ecológica do IBGE, Brasilia (DF). Lista das plantas vasculares. DEDIT/CDDI, Brasil. 1–43 pp.Google Scholar
PERRING, M. P., HEDING, L. O., LEVIN, S. A., MACGRODDY, M. & DE MAZANCOURT, C. 2008. Increased plant growth from nitrogen addition should conserve phosphorus in terrestrial ecosystems. Proceedings of the National Academy of Sciences USA – Biological Sciences 105:19711976.CrossRefGoogle ScholarPubMed
PIRES, C. S. S. & PRICE, P. W. 2000. Patterns of host plant growth and attack and establishment of gall-inducing wasp (Hymenoptera: Cynipidae). Environmental Entomology 29:4954.CrossRefGoogle Scholar
PONTES, F. V., MARINHO, F. V., CARNEIRO, M. C., COSTA, L. S., VAITSMAN, D. S., ROCHA, G. P., SILVA, L. I., NETO, A., MONTEIRO, A. & COUTO, M. I. 2009. A simplified version of the total kjeldahl nitrogen method using an ammonia extraction ultrasound-assisted purge-and-trap system and ion chromatography for analyses of geological samples. Analytica Chimica Acta 632:284288.CrossRefGoogle ScholarPubMed
PRICE, P. W. 1991. The plant vigor hypothesis and herbivore attack. Oikos 62:244251.CrossRefGoogle Scholar
PRICE, P. W., COBB, N., CRAIG, T., FERNANDES, G. W., ITAMI, J., MOPPER, S. & PRESZLER, R. W. 1990. Insect herbivore population dynamics on trees and shrubs: new approaches relevant to latent and eruptive species. Pp. 138 in Bernays, E. A. (ed.). Insect–plant interactions. CRC, Boca Raton.Google Scholar
PRICE, P. W., FERNANDES, G. W., LARA, A. C. F., BRAWN, J., BARRIOS, H., WRIGHT, M. G., RIBEIRO, S. P. & ROTHCLIFF, N. 1998. Global patterns in local number of insect galling species. Journal of Biogeography 25:581591.CrossRefGoogle Scholar
SAS 2000. Categorical data analysis using the SAS system. SAS Institute, Cary, North Carolina, USA.Google Scholar
RESENDE, J. 2001. A ciclagem de nutrientes em áreas de Cerrado e a influência de queimadas controladas. PhD thesis, University of Brasília, Brasília-Brazil.Google Scholar
SCHLICHTING, C. D. & PIGLIUCCI, M. 1998. Phenotypic evolution: a reaction norm perspective. Sinauer Press, Sunderland, MA.Google Scholar
SOPOW, S. L. & QUIRING, D. T. 2001. Is gall size a good indicator of adelgid fitness? Entomologia Experimentalis et Applicata 99:267271.CrossRefGoogle Scholar
STONE, G. N. & SCHÖNROGGE, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 13:512522.CrossRefGoogle Scholar
STOKES, M. E., DAVIS, C. S. & KOCH, G. G. 2000. Categorical data analysis using the SAS system. (2nd edition). SAS, Cary, NC.Google Scholar
VAN HEERWAARDEN, L. M., TOET, S. & AERTS, R. 2003. Nitrogen and phosphorous resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. Journal of Ecology 91:10601070.CrossRefGoogle Scholar
VITOUSEK, P. M. 1998. Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1:401407.CrossRefGoogle Scholar
WARING, G. L. & COBB, N. S. 1992. The impact of plant stress on herbivore population dynamics. Pp. 167226 in Bernays, E. (ed.). Insect–plant interactions. CRC, Boca Raton, FL.Google Scholar
WEIS, A. E., WALTON, R. & CREGO, C. L. 1988. Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology 33:467486.CrossRefGoogle Scholar