Abstract
Insects might impact communities and ecosystems through processes that are not trophic, via ecosystem engineering. In this study, we experimentally evaluated the role of the caterpillars Pandemis sp. as habitat modifiers in the tropical liana Trigonia rotundifolia. Specifically, we examined their effects on the abundance and richness of arthropods that secondarily colonize leaf-rolls (shelters) built by the caterpillars, as well as indirect effects that influence plant herbivory. Two experiments were conducted in the field to evaluate the role of natural and artificial rolls on community structure and plant damage. Plants with artificial leaf-rolls hosted 2.2 times more arthropods than plants without shelters and they had 1.5 times higher richness compared to control plants. Plants with natural shelters exhibited significantly lower arthropod richness than plants with artificial shelters or control plants, but arthropod abundance did not differ among treatments. Although plants with leaf-rolls hosted significantly more arthropods, arthropod species composition did not differ amongst treatments, as Formicidae was the most frequent group in all treatments. Herbivory was almost 3 times higher in plants with leaf-rolls compared to plants with no rolled leaves, indicating that the effect of increased arthropod abundance, and especially herbivore abundance, might influence leaf damage in plants with leaf-rolls. We demonstrate the strong impact of Pandemis as a habitat modifier on community structure as well as on community processes through indirect effects.
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References
Askew RR (1980) The diversity of insect communities in leaf mines and plant galls. J Anim Ecol 49:817–829
Brescovit AD, Rheims CA, Bonaldo AB (2007) Araneomorphae. Identification key to Brazilian spiders. Instituto Butantan
Calderón-Cortés N, Quesada M, Escalera-Vázquez (2011) Insects as stem engineers: interactions mediated by the twig-girdler Oncideres albomarginata chamela enhance arthropod diversity. PLoS ONE 6:e19083
Calderón-Cortés N, Uribe-Mu CA, Martinez-Mendez AK, Escalera-Vázquez LH, Cristobal-Perez EJ, Garcia-Oliva F, Quesada M (2016) Ecosystem engineering and manipulation of host plant tissues by the insect borer Oncideres albomarginata chamela. J Insect Physiol 84:128–136
Carrano-Moreira AF (2015) Insects: sampling and identification. Technical Books, Brazil
Cornelissen T, Cintra F, Santos JC (2016) Shelter-building insects and their role as ecosystem engineers. Neotrop Entomol 45:1–12
Crutsinger GM, Habenicht MN, Classe AT, Sanders NJ (2008) Galling by Rhopalomyia solidaginis alters Solidago altissima architecture and litter nutrient dynamics in an old-field ecosystem. Plant Soil 303:95–103
Cuddington K, Hastings A (2007) Balancing the engineer-environment equation: the current legacy. In: Cuddington K, Byers JE, Wilson WG, Hastings A (eds) Ecosystem engineers: plants to protists. Academic Press, NewYork, pp 253–274
Dátillo W, Rico-Gray V (2018) ecological networks in the tropics. Springer, New York. https://doi.org/10.1007/978-3-319-68228-0
Del-Claro K, Torezan-Silingardi H (2009) Insect-plant interactions: new pathways to a better comprehension of ecological communities in Neotropical savannas. Neotrop Entomol 38:159–164
Dyer L, Coley P (2002) Tri-trophic interactions in tropical versus temperate communities. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University press, Cambridge, pp 67–88
Fernandes GW, Boecklen WJ, Martins RP, Castro AG (1989) Ants associated with a coleopterous leaf-bud gall on Xylopia aromatica (Annonaceae). Proc Entomol Soc Wash 91:81–87
Hastings A, Byers JE, Crooks JA, Cuddington K, Jones CG, Lambrinos JA, Talley TS, Wilson WG (2007) Ecosystem engineering in space and time. Ecol Lett 10:153–164
Hedges LV, Gurevitch J, Curtis P (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156
Johnson SN, Lopaticki G, Bernett K, Facey SL, Powell JR, Hartley SE (2016) An insect ecosystem engineer alleviates drought stress in plants without increasing plant susceptibility to an above-ground herbivore. Funct Ecol 30:894–902
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jones CG, Gutiérrez JL, Byers JE, Crooks JA, Lambrinos JG, Talley TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119:1862–1869
Kozlov M, Zvereva E (2017) Background insect herbivory: impacts, patterns and methodology. Prog Bot. https://doi.org/10.1007/124_2017_4
Kozlov M, Lanta V, Zverev V, Zvereva E (2015) Global patterns in background losses of woody plant foliage to insects. Glob Ecol Biogeogr 24:1126–1135
Kozlov M, Zverev V, Zvereva E (2016) Shelters of leaf-tying herbivores decompose faster than leaves damaged by free-living insects: implications for nutrient turnover in polluted habitats. Sci Total Environ 15:946–951
Lill JT, Marquis RJ (2007) Microhabitat manipulation: ecosystem engineering by shelter-building insects. In: Cuddington K, Byers JE, Hastings A, Wilson WG (eds) Ecosystem engineers: plants to protists. Academic Press, New York, pp 107–138
Lill JT, Marquis RJ, Walker MA, Peterson L (2007) Ecological consequences of shelter-sharing by leaf-tying caterpillars. Entomol Exper et Applic 124:45–53
Lleras E (1978) Trigoniaceae. Flora Neotrop 19: 1–73
Magura T, Lövei GL (2017) Environmental filtering is the main assembly rule of ground beetles in the forest and its edge but not in the adjacent grassland. Insect Sci. https://doi.org/10.1111/1744-7917.12504
Negrele RRB (2002) The Atlantic forest in the Volta Velha Reserve: a tropical rain forest site outside the tropics. Biodiver Conserv 11:887–919
Novais SMA, DaRocha WD, Caldéron-Cortes N, Quesada M (2017) Wood-boring beetles promote ant nest cavities: extended effects of a twig-girdler ecosystem engineer. Basic Appl Ecol 24:53–59
O’Dowd DJ, Wilson MF (1991) Leaf domatia and mites on Australian plants: ecological and evolutionary implications. Biol J Linn Soc 37:191–236
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing [Internet]. R Foundation for Statistical Computing, Viena
Romero GQ, Gonçalves-Souza T, Vieira C, Koricheva J (2015) Ecosystem engineering effects on species diversity across ecosystems: a meta-analysis. Biol Rev 90:877–890
Rosemberg MS, Adams D, Gurevitch J (2000) MetaWin: Statistical software for meta-analysis
Stam JM, Kroes A, Li Y, Gols R, vanLoon JA, Poelman EH, Dickes M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713
Vieira C, Romero GQ (2013) Ecosystem engineers on plants: indirect facilitation of arthropod communities by leaf-rollers at different scales. Ecology 94:1510–1518
Wetzel WC, Screen RM, Li I, McKenzie J, Philips KA, Cruz M, Zhang W, Greene A, Lee E, Singh N, Tran C, Yang LH (2016) Ecosystem engineering by a gall-forming wasp indirectly suppresses diversity and density of herbivores on oak trees. Ecology 97:427–438
Acknowledgements
The authors thank ECMVS/UFMG, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - Grant #307210/2016-2) for financial support.
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Henriques, N.R., Cintra, F., Pereira, C.C. et al. Indirect effects of ecosystem engineering by insects in a tropical liana. Arthropod-Plant Interactions 13, 499–504 (2019). https://doi.org/10.1007/s11829-018-9661-6
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DOI: https://doi.org/10.1007/s11829-018-9661-6