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Bottom-up impact on the cecidomyiid leaf galler and its parasitism in a tropical rainforest

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Abstract

The relative importance of host-plant resources, natural enemies or their interactions in controlling the population of galling insects and their parasitism is poorly known for tropical gallers. In this study, we assessed the impacts of plant quality and density of host trees in regulating the densities of a galler species, the cecidomyiid leaf galler (Cecidomyiini sp. 1EJV) and its parasitoids and inquilines on Neoboutonia macrocalyx trees in Uganda. We manipulated the nutritional quality (or vigour) and the resource concentration with four levels each of fertilization and the group size of host tree. We then recorded the effects of these treatments on the growth rate and total leaf area of host plants, the density of gallers and their mortality by parasitoids and inquilines. Higher levels of fertilization and host density resulted in significantly higher total leaf area than did ambient nutrient levels, and lowest tree densities, respectively. Fertilization also caused significant change in the growth rate of leaf area. Both higher fertilization and host density caused higher density of gallers. Total leaf area was positively associated with galler density, but within galled replicates, the galled leaves were larger than the ungalled leaves. Although highest levels of fertilization and density of host trees caused significant change in the densities of parasitoids, the rate of parasitism did not change. However, tree-density manipulations increased the rate of inquilinism, but on a very low level. Our results demonstrate a trophic cascade in the tropical galler and its parasitoids as a response to bottom-up effects.

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References

  • Araújo APA, De Paula JDA, Carneiro MAA, Schoereder JH (2006) Effects of host plant architecture on colonization by galling insects. Austral Ecol 31:343–348. doi:10.1111/j.1442-9993.2006.01563.x

    Article  Google Scholar 

  • Auslander M, Nevo E, Inbar M (2003) The effects of slope orientation on plant growth, developmental instability and susceptibility to herbivores. J Arid Environ 55:405–416. doi:10.1016/S0140-1963(02)00281-1

    Article  Google Scholar 

  • Caballero PP, Lorini H (2000) Does resource concentration affect attack by galling and folivorous insects on Schinus polygamus (Cav.) Cabr. (Anacardiaceae)? Rev Chil Entomol 26:89–92

    Google Scholar 

  • Capman WC, Batzli GO, Simms LE (1990) Responses of the common sooty wing skipper to patches of host plants. Ecology 71:1430–1440. doi:10.2307/1938280

    Article  Google Scholar 

  • Chapman CA, Chapman LJ, Kaufman L, Zanne AE (1999) Potential causes of arrested succession in Kibale National Park, Uganda: growth and mortality of seedlings. Afr J Ecol 37:81–92. doi:10.1046/j.1365-2028.1999.00159.x

    Article  Google Scholar 

  • Chapman CA, Chapman LJ, Struhsaker TT, Zanne AE, Clark CJ, Poulsen JR (2005) A long term evaluation of fruiting phenology: importance of climate change. J Trop Ecol 21:31–45. doi:10.1017/S0266467404001993

    Article  Google Scholar 

  • Cornelissen T, Stiling A (2006) Responses of different herbivore guilds to nutrient addition and natural enemy exclusion. Ecoscience 13:66–74. doi:10.2980/1195-6860(2006)13[66:RODHGT]2.0.CO;2

    Article  Google Scholar 

  • Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:1691–1699. doi:10.2307/1938103

    Article  Google Scholar 

  • 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. doi:10.1111/j.0022-0477.2004.00896.x

    Article  Google Scholar 

  • Cuevas-Reyes P, De Oliveira-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 27:631–640. doi:10.1017/S0266467411000368

    Article  Google Scholar 

  • De Bruyn L, Scheirs J, Verhagen R (2002) Nutrient stress, host plant quality and herbivore performance of a leaf-mining fly on grass. Oecologia 130:594–599. doi:10.1007/s00442-001-0840-1

    Article  Google Scholar 

  • Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458. doi:10.2307/3071956

    Article  Google Scholar 

  • Faria ML, Fernandes GW (2001) Vigour of a dioecious shrub and attack by a galling herbivore. Ecol Entomol 26:37–45. doi:10.1046/j.1365-2311.2001.00291.x

    Article  Google Scholar 

  • Fischer E, Killman D (2008) Illustrated field guide to the plants of Nyungwe National Park, Rwanda, 1st edn. Koblenz, Germany

    Google Scholar 

  • Fritz RS, Crabb BA, Hochwender CG (2000) Preference and performance of a gall-inducing sawfly: a test of the plant vigor hypothesis. Oikos 89:555–563. doi:10.1034/j.1600-0706.2000.890315.x

    Article  Google Scholar 

  • Goulet H, Huber JT (1993) Hymenoptera of the world: an identification guide to families. Centre for Land and Biological Resources Research. Ottawa, Ontario

    Google Scholar 

  • Grez AA, González RH (1995) Resource concentration hypothesis effect of host patch size on density of herbivorous insects. Oecologia 103:471–474. doi:10.1007/BF00328685

    Article  Google Scholar 

  • Hamilton A (1991) A field guide to Ugandan forest trees. Makerere University Press, Kampala

    Google Scholar 

  • Hartley SE, Gardner SM (1995) The response of Philaenus spumarius (Homoptera: Cercopidae) to fertilizing and shading its moorland host-plant (Calluna vulgaris). Ecol Entomol 20:396–399. doi:10.1111/j.1365-2311.1995.tb00474.x

    Article  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152. doi:10.1890/0012-9658(1997)078[2145:PPAPAM]2.0.CO;2

    Article  Google Scholar 

  • Heimonen K, Lwanga JS, Mutanen M, Nyman T, Roininen H (2013) Spatial and temporal variation in community composition of herbivorous insects on Neoboutonia macrocalyx in a primary tropical rain forest. J Trop Ecol 29:229–241. doi:10.1017/S0266467413000151

    Article  Google Scholar 

  • Huang MY, Huang WD, Chou HM, Lin KH, Chen CC, Chen PJ, Chang YT, Yang CM (2014) Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiol Plant. doi:10.1111/ppl.12186 (in press)

    Google Scholar 

  • Hunter MD (2003) Effects of plant quality on the population ecology of parasitoids. Agric For Entomol 5:1–8. doi:10.1046/j.1461-9563.2003.00168.x

    Article  Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732. http://www.jstor.org/stable/1940152

  • Jaenike J (1978) Optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356. doi:10.1016/0040-5809(78)90012-6

    Article  PubMed  CAS  Google Scholar 

  • Kagata H, Ohgushi T (2006) Bottom-up trophic cascades and material transfer in terrestrial food webs. Ecol Res 21:26–34. doi:10.1007/s11284-005-0124-z

    Article  Google Scholar 

  • Kasenene JM, Roininen H (1999) Seasonality of insect herbivory on the leaves of Neoboutonia macrcocalyx in the Kibale National Park, Uganda. Afr J Ecol 37:61–68. doi:10.1046/j.1365-2028.1999.00162.x

    Article  Google Scholar 

  • Kimberling DN, Scott ER, Price PW (1990) Testing a new hypothesis: plant vigor and phylloxera distribution on wild grape in Arizona. Oecologia 84:1–8. doi:10.1007/BF00665587

    Article  Google Scholar 

  • Legrand A, Barbosa P (2003) Plant morphological complexity impacts foraging efficiency of adult Coccinella septempunctata L. (Coleoptera: Coccinellidae). Environ Entomol 32:1219–1226. doi:10.1603/0046-225X-32.5.1219

    Article  Google Scholar 

  • Leite GLD, Veloso RVS, Silva FWS, Guanabens REM, Fernandes GW (2009) Within tree distribution of a gall-inducing Eurytoma (Hymenoptera, Eurytomidae) on Caryocar brasiliense (Caryocaraceae). Rev Bras Entomol 53:643–648

    Article  Google Scholar 

  • Low C, Wood SN, Nisbet RM (2009) The effects of group size, leaf size, and density on the performance of a leaf-mining moth. J Anim Ecol 78:152–160. doi:10.1111/j.1365-2656.2008.01469.x

    Article  PubMed  Google Scholar 

  • Malinga GM, Valtonen A, Nyeko P, Roininen H (2014) Bottom-up manipulations alter the community structures of galling insects and gall morphs on Neoboutonia macrocalyx trees in a moist tropical rainforest. Agric For Entomol 16:314–320.doi:10.1111/afe.12061

  • Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. doi:10.1146/annurev.es.11.110180.001003

    Article  Google Scholar 

  • McKinnon ML, Quiring DT, Bauce E (1999) Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid. Funct Ecol 13:859–867. doi:10.1046/j.1365-2435.1999.00376.x

    Article  Google Scholar 

  • Nakamura M, Utsumi S, Miki T, Ohgushi T (2005) Flood initiates bottom-up cascades in a tri-trophic system: host plant regrowth increases densities of a leaf beetle and its predators. J Anim Ecol 74:683–691. doi:10.1111/j.1365-2656.2005.00960.x

    Article  Google Scholar 

  • Nichols JD, Ofori DA, Wagner MR, Bosu P, Cobbinah JR (1999) Survival, growth and gall formation by Phytolyma lata on Milicia excelsa established in mixed-species tropical plantations in Ghana. Agric For Entomol 1:137–141. doi:10.1046/j.1461-9563.1999.00014.x

    Article  Google Scholar 

  • Prada M, Marini OJ, Price PW (1995) Insects in flower heads of Aspilia foliacea (Asteraceae) after a fire in a central Brazilian savanna: evidence for the plant vigor hypothesis. Biotropica 27:513–518. doi:10.2307/2388965

    Article  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251. doi:10.2307/3545270

    Article  Google Scholar 

  • Price PW, Hunter MD (2005) Long-term population dynamics of a sawfly show strong bottom-up effects. J Anim Ecol 74:917–925. doi:10.1111/j.1365-2656.2005.00989.x

    Article  Google Scholar 

  • Price PW, Ohgushi T (1995) Preference and performance linkage in a Phyllocolpa sawfly on the willow, Salix miyabeana, on Hokkaido. Res Popul Ecol 37:23–28. doi:10.1007/BF02515757

    Article  Google Scholar 

  • Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insects ecology, behaviors, populations and communities. Cambridge University Press, New York

    Book  Google Scholar 

  • Rehill BJ, Schultz JC (2001) Hormaphis hamamelidis and gall size: a test of the plant vigor hypothesis. Oikos 95:94–104. doi:10.1034/j.1600-0706.2001.950111.x

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392. doi:10.2307/2937116

    Article  Google Scholar 

  • 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 28:348–358. doi:10.1046/j.1365-2311.2003.00508.x

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. doi:10.2307/2409177

    Article  Google Scholar 

  • Roininen H, Danell K (1997) Mortality factors and resource use of the bud-galling sawfly, Euura macronata (Hartig), on willows (Salix spp.) in artic Eurasia. Polar Biol 18:325–330. doi:10.1007/s003000050195

    Article  Google Scholar 

  • Roininen H, Price PW, Tahvanainen J (1993) Colonization and extinction in a population of the shoot-galling Sawfly, Euura amerinae. Oikos 68:448–454. doi:10.2307/3544912

    Article  Google Scholar 

  • Roininen H, Price PW, Tahvanainen J (1996) Bottom-up and top-down influences in the trophic system of a willow, a galling sawfly, parasitoids and inquilines. Oikos 77:44–45. doi:10.2307/3545583

    Article  Google Scholar 

  • Root RB (1973) Organization of a plant–arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124. doi:10.2307/1942161

    Article  Google Scholar 

  • Santos JC, Silveira FAO, Fernandes GW (2008) Long term oviposition preference and larval performance of Schizomyia macrocapillata (Diptera : Cecidomyiidae) on larger shoots of its host plant Bauhinia brevipes (Fabaceae). Evol Ecol 22:123–137. doi:10.1007/s10682-007-9162-z

    Article  Google Scholar 

  • Santos JC, Tavares CB, Almeida-Cortez JS (2011) Plant vigor hypothesis refuted: preference-performance linkage of a gall-inducing weevil on small-sized host plant resources. Braz J Biol 71:65–69. doi:10.1034/j.1600-0706.2003.12473.x

    Article  PubMed  CAS  Google Scholar 

  • Savilaakso S, Koivisto J, Veteli TO, Roininen H (2009) Microclimate and tree community linked to differences in lepidopteran larval communities between forest fragments and continuous forest. Divers Distrib 15:356–365. doi:10.1111/j.1472-4642.2008.00542.x

    Article  Google Scholar 

  • Skippari S, Veteli TO, Kasenene J, Niemelä P, Roininen H (2009) High temporal variation in the assemblage of lepidopteran larvae on a constant resource. Afr J Ecol 47:537–545. doi:10.1111/j.1365-2028.2008.00986

    Article  Google Scholar 

  • SPSS (2010) SPSS for Windows, IBM version.19.0.1. SPSS, Chicago

  • Stiling P, Moon DC (2005) Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies. Oecologia 142:413–420. doi:10.1007/s00442-004-1739-4

    Article  PubMed  Google Scholar 

  • Stiling P, Rossi AM (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78:1602–1606. doi:10.1890/0012-9658(1997)078[1602:EMOTDA]2.0.CO;2

    Article  Google Scholar 

  • Struhsaker TT (1997) Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. University Press of Florida, Gainesville

    Google Scholar 

  • Tanner EVJ, Viteousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22. doi:10.1890/0012-9658(1998)079[0010:EIONLO]2.0.CO;2

    Article  Google Scholar 

  • Tuller J, Queiroz ACM, Luz GR, Silva JO (2013) Gall-forming insect attack patterns: a test of the plant vigor and the resource concentration hypotheses. Biotemas 26:45–51. doi:10.5007/2175-7925.2013v26n1p45

    Article  Google Scholar 

  • Utsumi S, Nakamura M, Ohgushi T (2009) Community consequences of herbivore-induced bottom–up trophic cascades: the importance of resource heterogeneity. J Anim Ecol 78:953–963. doi:10.1111/j.1365-2656.2009.01570.x

    Article  PubMed  Google Scholar 

  • Vieira EM, Andrade I, Price PW (1996) Fire effects on a Palicourea rigida (Rubiaceae) gall midge: a test of the plant vigor hypothesis. Biotropica 28:210–217. doi:10.2307/2389075

    Article  Google Scholar 

  • Walker M, Hartley SE, Jones TH (2008) The relative importance of resources and natural enemies in determining herbivore abundance: thistles, tephritids and parasitoids. J Anim Ecol 77:1063–1071. doi:10.1111/j.1365-2656.2008.01406.x

    Article  PubMed  Google Scholar 

  • Weis AE, Kapelinski A (1984) Manipulation of host plant development by the gall-midge Rhabdophaga strobiloides. Ecol Entomol 9:457–465. doi:10.1111/j.1365-2311.1984.tb00844.x

    Article  Google Scholar 

  • White TCR (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33:71–86. doi:10.1007/BF00376997

    Article  Google Scholar 

  • Williams MA, Cronin JT (2004) Response of a gall-forming guild (Hymenoptera : Cynipidae) to stressed and vigorous prairie roses. Environ Entomol 33:1052–1061

    Article  Google Scholar 

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Acknowledgments

This study was funded by the Finnish Academy of Sciences (SA 138899 to H. R.). We thank the office of the Ugandan President, the Uganda National Council of Science and Technology and the Uganda Wildlife Authority for permission to access the study site. We thank J. Koojo and L. Balyega for assistance in fieldwork. The authors wish to thank Utsumi Shusuke for comments on an earlier version of the manuscript, and the handling editor and two anonymous reviewers whose comments and suggestions greatly improved this paper.

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Authors and Affiliations

  1. Department of Biology, University of Eastern Finland, P.O. Box 111, 80101, Joensuu, Finland

    Geoffrey M. Malinga, Anu Valtonen & Heikki Roininen

  2. Department of Forestry, Biodiversity and Tourism, Makerere University, P.O. Box 7062, Kampala, Uganda

    Philip Nyeko

  3. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

    Eero J. Vesterinen

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  1. Geoffrey M. Malinga
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  2. Anu Valtonen
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  3. Philip Nyeko
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  4. Eero J. Vesterinen
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  5. Heikki Roininen
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Correspondence to Geoffrey M. Malinga.

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Communicated by George Heimpel.

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Malinga, G.M., Valtonen, A., Nyeko, P. et al. Bottom-up impact on the cecidomyiid leaf galler and its parasitism in a tropical rainforest. Oecologia 176, 511–520 (2014). https://doi.org/10.1007/s00442-014-3024-5

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