Original Article Plant Stress in Determining Attack Rates of Herbivorous Chewing Insects
DOI:
10.46551/ruc.v26n2a16Palabras clave:
Cerrado, Herbivoria, Estresse, AssimetriaResumen
Plants in stressful environments tend to be more asymmetrical, have reduced defenses, and are more vulnerable to herbivory. Stressful conditions are also detrimental to free-living herbivorous insects, which are sensitive to climatic variations like extreme temperatures and dry periods. In the Cerrado, different phytophysiognomies range from open to closed and structurally complex areas, simulating a gradient of environmental harshness. This study examines the relationship between fluctuating asymmetry (FA) and herbivory in Qualea parviflora and Eugenia dysenterica across five Cerrado areas. We tested the Plant Stress Hypothesis (PSH) and the Environmental Harshness Hypothesis (EHH), investigating their interaction. Specifically, we assessed how stressful conditions influence plants, herbivory rates, and the richness and abundance of herbivorous insects, considering species composition variation among phytophysiognomies. Results showed significant differences in structural complexity among areas, with campo rupestre < cerrado sensu stricto < cerradão. FA per plant varied with increasing complexity for Q. parviflora but not for E. dysenterica. Leaf area removed differed between species but did not vary significantly with complexity. Leaf area removed decreased with increasing FA in Q. parviflora but increased with FA and complexity interaction in E. dysenterica. Contrary to predictions, free-living herbivore richness and abundance were higher in the most stressed phytophysiognomy, with species composition variation mainly influenced by the substitution process.
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WHITE, Thomas C. An Index to Measure Weather-Induced Stress of Trees Associated With Outbreaks of Psyllids in Australia. Ecology, Washington, D.C, v. 50, p. 905-909, set., 1969.
WHITE, Thomas C. The abundance of invertebrate herbivores in relation of the availability of nitrogen in stressed food plants. Oecologia, Londres, v. 63, n. 1, p. 93-105, jul., 1984.
RHOADES, David F. Evolution of plant chemical defense against herbivores. In: Herbivores: their interaction with plant secondary metabolites. Academic Press, Nova York, p. 3-54, 1979.
PERKOVICH, Cindy; WARD, David. Differentiated plant defense strategies: Herbivore community dynamics affect plant–herbivore interactions. Ecosphere, Washington, D.C., v. 13, n. 2, p. 1-12, fev., 2022.
CASTAGNEYROL, Bastien; JACTEL, Hervé; MOREIRA, Xoaquín. Anti-herbivore defences and insect herbivory: Interactive effects of drought and tree neighbours. Journal of Ecology, Oxford Londres, v. 106, p. 1767-2146, set., 2018.
PRICE, Peter W. The Plant Vigor Hypothesis and Herbivore Attack. Oikos, Copenhagen, v. 62, n. 2, p. 244-251, nov., 1991.
ZAKHAROV, Vladimir M.; SHADRINA, Elena G.; TROFIMOV, Ilya E. Fluctuating Asymmetry, Developmental Noise and Developmental Stability: Future Prospects for the Population Developmental Biology Approach. Symmetry, v. 12, p. 1-24, 2020. Disponível em: 10.3390/sym12081376. Acesso em: 15 abr. 2024.
VACA-SÁNCHEZ, Marcela S. et al. Patterns in Wing Morphology and Fluctuating Asymmetry in Eulaema nigrita along an Altitudinal Gradient in the Brazilian Rupestrian Grassland. Neotropical Entomology, Londrina, v. 52, p. 837–847, ago., 2023.
PALMER, Arthur R.; STROBECK, Curtis. Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zoologica Fennica, Helsinki, v. 191, p. 55-70, 1992.
CORNELISSEN, Tatiana G.; STILING, Peter. Perfect is best: lowle affluctuating asymmetry reduces herbivory by leafminers. Oecologia, Londres, v. 142, n. 1, p. 46-56, jan., 2005.
GARCÍA‑JAIN, Silvia E. et al. Efects of forest fragmentation on plant quality, leaf morphology and herbivory of Quercus deserticola: is fuctuating asymmetry a good indicator of environmental stress?. Trees, Londres, v. 36, p. 553–567, 2021. Available at: https://doi.org/10.1007/s00468-021-02228-2. Accessed: 15 april, 2024.
FERNANDES, Geraldo W.; PRICE, Peter W. The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia, Londres, v. 90, n, 1, p. 14-20, abr., 1992.
WARDHAUGH, Carl W. The spatial and temporal distributions of arthropods in forest canopies: uniting disparate patterns with hypotheses for specialisation. Biological Reviews, Cambridge, v. 89, n. 4, p. 1021-1041, nov., 2014.
FERNANDES, Geraldo W.; PRICE, Peter W. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia, Londres, v. 76, n. 2, p. 161-167, jul.-set., 1988.
FRANCO, André L. et al. Drought suppresses soil predators and promotes root herbivores in mesic, but not in xeric grasslands. Proceedings of the National Academy of Sciences, Washington, D.C., v. 116, n. 26, p. 12883-12888, jun., 2019.
KIMBERLING, Diana N.; SCOTT, Eric R.; PRICE, Peter W. Testing a new hypothesis: plant vigor and phyloxera distribution on wild grape in Arizona. Oecologia, Londres, v. 84, v. 1, p. 1-8, ago., 1990.
HAN, Peng et al. Plant nutrient supply alters the magnitude of indirect interactions between insect herbivores: From foliar chemistry to community dynamics. Journal of Ecology, Oxford, v. 108, n. 4, p. 1497–510, jul., 2020.
ALVARES, Clayton A. et al. Modeling monthly mean air temperature for Brazil. Theoretical and Applied Climatology, Londres, v. 113, p. 407-427, 2013. Available at: https://doi.org/10.1007/s00704-012-0796-6. Accessed: 15 march. 2024.
INSTITUTO NACIONAL DE METEOROLOGIA (INMET). Portal do Instituto Nacional de Meteorologia. Available at: http://www.inmet.gov.br/. Accessed: 20 march, 2024.
CUEVAS-REYES, Pablo et al. Effects of generalist and specialist parasitic plants (Loranthaceae) on the fluctuating asymmetry patterns of ruprestrian host plants. Basic and Applied Ecology, Jena, v. 12, n. 5, p. 449-455, ago., 2011.
CUEVAS-REYES, Pablo et al. Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along na urban gradient in Brazil. Ecological Indicators, Amsterdã, v. 24, p. 557-561, jan., 2013.
BASSET, Yves. Diversity and abundance of insect herbivores collected on Castanopsis acuminatissima (Fagaceae) in New Guinea: Relationships with leaf production and surrounding vegetation. European Journal of Entomology, Praga, v. 96, n. 4, p. 381-391, dez., 1999.
PAST (PAleontological STatistics), versão 3.14. 2016. Available at: https://folk.uio.no/ohammer/past/. Accessed: 20 march, 2024.
R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing. R Foundation for Statistical Computing, 2015. Available at: http://www.R-project.org. Accessed: 20 march, 2024.
BASELGA, Andrés. Partitiooning the turnover and nestedness componentes of beta diversity. Global Ecology and Biogeography, Hoboken, v. 19, n.1, p. 134-143, jan., 2010. Available at: https://doi.org/10.1111/j.1466-8238.2009.00490.x. Accessed: 21 march, 2024.
LEGENDRE, Pierre. Interpreting the replacement and richness difference componentes of beta diversity. Global Ecology and Biogeography, Hoboken, v. 23, n. 11, p. 1324–1334, nov., 2014. Available at: https://doi.org/10.1111/geb.12207. Accessed: 21 march, 2024.
BASELGA, Andrés. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods in Ecology and Evolution, Londres, v. 4, n. 6, p. 552–557, jun., 2013. Available at: https://doi.org/10.1111/2041-210X.12029. Accessed: 21 march, 2024.
RIBEIRO, José F.; WALTER, Bruno M. T. As principais fitofisionomias do bioma Cerrado. In: SANO, S. M.; ALMEIDA, S. P. (Eds.). Cerrado: Ecologia e Flora. Embrapa-CPAC, Planaltina, 2008. p. 151–212.
JIANG, Zihan; MA, Keming; ANAND, Madhur. Can the physiological tolerance hypothesis explain herb richness patterns along an elevational gradient? A trait-based analysis. Community Ecology, Budapeste, v. 17, n. 1, p. 17-23, dez., 2016.
VAN ZELM, Eva; ZHANG, Yanxia; TESTERINK, Christa. Salt tolerance mechanisms of plants. Annual Review of Plant Biology, Palo Alto, v. 71, p. 403-433, mar., 2020.
GIULIETTI, Ana M. et al. Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Boletim de Botânica, São Paulo, v. 9, p. 1-152, 1987. DOI: 10.11606/issn.2316-9052.v9i0p1-151. Available at: https://www.revistas.usp.br/bolbot/article/view/57726. Accessed: 16 april, 2024.
RONQUIM, Carlos C.; PRADO, Carlos H. A.; SOUZA, João P. Estabelecimento e crescimento de plantas jovens de Vochysia tucanorum Mart (Vochysiaceae) em área aberta e sombreada sob dossel florestal. Scientia Forestalis, Piracicaba, v. 41, n. 97, p. 121-130, mar., 2013.
DELGADO, Liliana F.; BARBEDO, Claudio J. Water potential and viability of seeds of Eugenia (Myrtaceae), a tropical tree species, based upon different levels of drying. Brazilian Archives of Biology and Technology, Curitiba, v. 55, n. 4, p. 583-590, jul.-ago., 2012.
MATHEWS, Sally; BONSER, Stephen P. Life histories, ecological tolerance limits, and the evolution of geographic range size in Eucalyptus (Myrtaceae). Australian Journal of Botany, Camberra, v. 53, n. 6, p. 501-508, jan., 2005.
MACARTHUR, Robert H.; MACARTHUR, James W. On bird species diversity. Ecology, Washington, D.C, v. 42, n. 3, p. 594-598, jul., 1961.
OLIVIER, Richard S. et al. Effects of environmental heterogeneity in the composition of insect tropphic guilds. Applied Ecology and Environmental Research, Budapeste, v. 12, n. 1, p. 209-220, jul., 2014.
CORNELISSEN, Tatiana; STILING, Peter. Similar responses of insect herbivores to leaf fluctuating asymmetry. Arthropod-Plant Interactions, v. 5, n. 1, p. 59-69, mar., 2011. Available at: https://doi.org/10.1007/s11829-010-9116-1. Accessed: 16 april, 2024.
PÉREZ-SOLACHE, Abel et al. Changes in land use of temperate forests associated to avocado production in Mexico: Impacts on soil properties, plant traits and insect-plant interactions. Agricultural Systems, Amsterdã, v. 204, p. 1-15, jan. 2023.
ALVES-SILVA, Estevão. The influence of Ditylenchus (Nematoda) galls and shade on the fluctuating asymmetry of Miconia fallax (Melastomataceae). Ecología Austral, Buenos Aires, v. 22, n. 1, p. 53-61, abr., 2012.
ALVES-SILVA, Estevão; DEL-CLARO, Kleber. Herbivory-induced stress: Leaf developmental instability is caused by herbivore damage in early stages of leaf development. Ecological Indicators, v. 61, p. 359-365, 2016. Available at: https://doi.org/10.1016/j.ecolind.2015.09.036. Accessed: 16 april, 2024.
MOURA, Renan F.; ALVES-SILVA, Estevão; DEL-CLARO, Kleber. Patterns of growth, development and herbivory of Palicourea rigida are affected more by sun/shade conditions than by Cerrado phytophysiognomy. Acta Botanica Brasilica, Feira de Santana, v. 31, n. 2, p. 286-294, abr.-jun., 2017.
NEWBOLD, Tim et al. Global effects of land use on biodiversity differ among functional groups. Functional Ecology, Londres, v. 34, n. 3, p. 684-693, mar. 2020.
COLEY, Phyllis D.; BRYANT, John P.; CHAPIN, Francis Stuart. Resource availability and plant antiherbivore defense. Science, Washington, D.C., v. 230, p. 895-899, nov., 1985. Disponível em: DOI: 10.1126/science.230.4728. Acesso em 16 de abril de 2024.
GONÇALVES-ALVIM, Silmary J. et al. Test of hypotheses about herbivory and chemical defences of Qualea parviflora (Vochysiaceae) in Brazilian Cerrado. Brazilian Journal Botany, São Paulo, v. 34, n. 2, p. 223-230, abr.-jun., 2011.
RANDLKOFER, Barbara et al. Vegetation complexity—the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic and Applied Ecology, v. 11, n. 5, p. 383-395, ago., 2010. Available at: https://doi.org/10.1016/j.baae.2010.03.003. Accessed: 16 april, 2024.
LOWMAN, Margaret D. Temporal and spatial variability in insect grazing of the canopies of five Australian rainforest tree species. Australian Journal of Ecology, Melbourne, v. 10, n. 1, p. 7-24, mar., 1985.
ARAÚJO, Walter S. et al. Comparing galling insect richness among Neotropical savannas: effects of plant richness, vegetation structure and super-host presence. Biodiversity and Conservation, Dordrecht, v. 22, n. 4, p. 1083-1094, mar., 2013.
NOBRE, Paola A. et al. Host-plant specialization mediates the influence of plant abundance on host use by flower head-feeding insects. Environmental Entomology, Lanham, v. 45, n. 1, p. 171-177, fev., 2016.
KUCHENBECKER, Juliana; FAGUNDES, Marcílio. 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. European Journal of Entomology, Praga, v. 115, p. 354-363, ago., 2018. Available at: DOI:10.14411/eje.2018.035. Accessed: 17 april, 2024.
FAGUNDES, Marcílio. et al. Diversity of Gall-Inducing Insects Associated With a Widely Distributed Tropical Tree Species: Testing the Environmental Stress Hypothesis. Environmental Entomolog, Lanham, v. 49, n. 4, p. 838-847, ago., 2020.
OLIVEIRA, Jefferson B. B. S. et al. Comparing the plant-herbivore network topology of different insect guilds in Neotropical savannas. Ecological Entomology, Oxford, v. 45, n. 3, p. 406-415, jun., 2020.
ZVEREVA, Elena L.; KOZLOV, Mikhai V. Avoidance of willows from moderately polluted area by leaf beetle, Melasoma lapponica: effects of emission or induced resistance?. Entomologia experimentalis et applicata, Oxford, v. 79, n. 3, p. 355-362, jun., 1996.
COLEY, Phillis D. Rates of herbivory on different tropical trees. In: LEIGH, E.G.; RAND, A.S.; WINDSOR, D.M. (Eds.). Ecological of a tropical forest: seasonal rhythms and long-term changes. Washington: Smithsonian Institution Press, p. 123-132, 1982.
RHOADES, Dwight F.; CATES, Raymond G. Toward a general theory of plant antiherbivore chemistry. In: Biochemical interaction between plants and insects. Boston: Springer, p. 168-213, 1976.
FARIA, Maurício Lopes; FERNANDES, Geraldo Wilson. Vigour of a dioecious shrub and attack by a galling herbivore. Ecological Entomology, Oxford, v. 26, n. 1, p. 37-45, fev., 2001.
LIPIEC, Janusz et al. Effect of drought and heat stresses on plant growth and yield: a review. International Agrophysics, Lublin, v. 27, p. 463-477, dez., 2013.
MONTEIRO, Graziella F. et al. Ecological interactions among insect herbivores, ants and the host plant Baccharis dracunculifolia in a Brazilian mountain ecosystem. Austral Ecology, Richmond, v. 45, n. 2, p. 158-167, dez., 2019.
ROSA, Elena et al. Moderate plant water stress improves larval development, and impacts immunity and gut microbiota of a specialist herbivore. Plos One, São Francisco, v. 14, n. 2, p. 1-13, fev., 2019.
MOTA, Graciene et al. Changes in species composition, vegetation structure, and life forms along an altitudinal gradient of rupestrian grasslands in south-eastern Brazil. Flora, v. 229, p. 1-42, jan., 2017. Available at: https://doi.org/10.1016/j.flora.2017.03.010. Accessed: 22 april, 2024.
SILVA, Jhonathan O.; ESPÍRITO-SANTO, Mário M.; MELO, Geraldo A. Herbivory on Handroanthus ochraceus (Bignoniaceae) along a successional gradient in a tropical dry forest. Arthropod Plant Interactions, Dordrecht, v. 6, n.1, p. 45-57, out., 2012.
BARBOSA, Milton et al. Canopy herbivory and succession in a Brazilian tropical seasonally dry forest. Arquivos do Museu de História Natural e Jardim Botânico, Belo Horizonte, v. 29, p. 33-52, 2020.
HARVEY, Jeffrey A.; HEINEN, Robin; GOLS, Rieta; THAKUR, Madhav P. Climate change-mediated temperature extremes and insects: From outbreaks to breakdowns. Global Change Biology, Oxford, v. 26, n. 12, p. 6685-6701, dez., 2020.
ALMEIDA, Sabrina S. P. de; LOUZADA, Júlio N. C. Estrutura da Comunidade de Scarabaeinae (Scarabaeidae: Coleoptera) em Fitofisionomias do Cerrado e sua Importância para a Conservação. Neotropical Entomology, Londrina, v. 38, n. 1, p. 32-43, 2009. Available at: https://doi.org/10.1590/S1519-566X2009000100003. Accessed: : 22 april, 2024.
EVANGELISTA, Juliane; OLIVEIRA, Charles M.; FRIZZAS, Marina R. Open vegetation formations (grasslands and savannahs) support a higher diversity of Cetoniidae (Insecta: Coleoptera) than forest formations in the Brazilian Cerrado. Biodiversity and Conservation, Dordrecht, v. 31, p. 2875–2892, ago., 2022. Available at: https://doi.org/10.1007/s10531-022-02467-w. Accessed: 27 april, 2024.
HALFFTER, Gonzalo; MORENO, Claudia E. Significado biológico de las diversidades alfa, beta y gamma. In: Sobre diversidad biológica: el significado de las diversidades alfa, beta y gamma. Zaragoza: Ed.: Monografías Tercer Milenio, p. 5-18, 2005.
COELHO, Marcel S. et al. Species turnover drives β-diversity patterns across multiple spatial scales of plant-galling interactions in mountaintop grasslands. Plos One, São Francisco, v. 13, n. 5, mai., 2018. Available at: https://doi.org/10.1371/journal.pone.0195565. Accessed: 16 april, 2024.
RICHTER, Aline et al. Microclimatic Fluctuation throughout the Day Influences Subtropical Fruit-Feeding Butterfly Assemblages between the Canopy and Understory. Diversity, Basel, v. 15, n. 4, p. 1-14, abr., 2023.
FREIRE JR. Geraldo Brito et al. Horizontal and vertical variation in the structure of fruit-feeding butterfly (Nymphalidae) assemblages in the Brazilian Cerrado. Insect Conservation and Diversity, Oxford, v. 15, n. 2, p. 226-235, out., 2021. Available at: https://doi.org/10.1111/icad.12547. Accessed: 02 de may, 2024.
FREIRE JR. Geraldo Brito et al. Habitat heterogeneity shapes multiple diversity dimensions of fruit-feeding butterflies in an environmental gradient in the Brazilian Cerrado. Forest Ecology and Management, Amsterdã, v. 558, n. 1, p. 1-22, fev., 2024. Available at: https://doi.org/10.1016/j.foreco.2024.121747. Accessed: 02 de may, 2024.
