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Disentangling the effects of foliar vs. floral herbivory of leaf-cutting ants on the plant reproductive success of Miconia nervosa (Smith) Triana (Family Melastomataceae)

Published online by Cambridge University Press:  13 June 2019

T. Câmara ,
X. Arnan Open the ORCID record for X. Arnan [Opens in a new window] ,
V.S. Barbosa ,
R. Wirth ,
L. Iannuzzi  and
I.R. Leal
T. Câmara
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, 50670-901, Recife, PE, Brazil
X. Arnan*
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, 50670-901, Recife, PE, Brazil CREAF, Cerdanyola de Vallès, Catalunya, Spain
V.S. Barbosa
Affiliation:
Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Cidade Universitária, 50670-901, Recife, PE, Brazil Centro de Formação de Professores, Universidade Federal de Campina Grande, Rua Sérgio Moreira de Figueiredo, s/n, Casas Populares, CEP: 58900-000, Cajazeiras, Paraíba, Brasil
R. Wirth
Affiliation:
Plant Ecology & Systematics, University of Kaiserslautern, PO-Box 3049, 67663 Kaiserslautern, Germany
L. Iannuzzi
Affiliation:
Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/no, 50670-901 Recife, PE, Brazil
I.R. Leal
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/no, 50670-901 Recife, PE, Brazil
*
*Author for correspondence Phone: +34 93 581 1312 Fax: +34 93 581 4151 E-mail: [email protected]
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Abstract

Flower and leaf herbivory might cause relevant and negative impacts on plant fitness. While flower removal or damage by florivores produces direct negative effects on plant fitness, folivores affect plant fitness by reducing resource allocation to reproduction. In this study, we examine the effects of both flower and leaf herbivory by leaf-cutting ants on the reproductive success of the shrub species Miconia nervosa (Smith) Triana (Family Melastomataceae) in a fragment of Atlantic Forest in Northeast Brazil. We conducted a randomized block-designed field experiment with nine replicates (blocks), in which three plants per block were assigned to one of the three following treatments: undamaged plants (ant exclusion), leaf-damaged plants (ant exclusion from reproductive organs, but not from leaves), and flower + leaf-damaged plants (no exclusion of ants). We then measured flower production, fruit set, and fruit production. Our results showed that flower + leaf-damaged plants reduced flower production nearly twofold in relation to undamaged plants, while flower set in leaf-damaged plants remained constant. The number of flowers that turned into fruits (i.e., fruit set), however, increased by 15% in flower + leaf-damaged plants, while it slightly decreased in leaf-damaged compared to undamaged plants. Contrastingly, fruit production was similar between all treatments. Taken together, our results suggest a prominent role of ant floral herbivory across different stages of the reproductive cycle in M. nervosa, with no consequences on final fruit production. The tolerance of M. nervosa to leaf-cutting ant herbivory might explain its high abundance in human-modified landscapes where leaf-cutting ants are hyper-abundant.

Keywords

Atlantic forestAtta cephalotesAtta sexdensplant fitnessresource allocationtolerance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 77 - 83
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Copyright
Copyright © Cambridge University Press 2019 

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References

Agrawal, A.A., Hastings, A.P., Johnson, M.T., Maron, J.L. & Salmien, J.P. (2012) Insect herbivores drive real time ecological and evolutionary change in plant populations. Science 338, 113–116.Google Scholar
Antonini, R.D. & Nunes-Freitas, A.F. (2004) Estrutura populacional e distribuição espacial de Miconia prasina D.C. (Melastomataceae) em duas áreas de Floresta Atlântica na Ilha Grande, RJ, Sudeste do Brasil. Acta Botanica Brasilica 18, 671–676.Google Scholar
Barber, N.A., Milano, N.J., Tiers, E.T., Bartolo, V., Hazzard, R.V. & Adler, L.S. (2015) Root herbivory indirectly affects above- and below-ground community members and directly reduces plant performance. Journal of Ecology 103, 1509–1518.Google Scholar
Barbosa, V.S. (2009) Influência da herbivoria de formigas-cortadeiras no sucesso reprodutivo de espécies arbustivas-arbóreas da Floresta Atlântica Nordestina. PhD thesis, Universidade Federal de Pernambuco, Brazil.Google Scholar
Bates, D.M., Mächler, M., Bolker, B.M. & Walker, S.C. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bazzaz, F.A. & Carlson, R.W. (1982) Photosynthetic acclimation to variability in the light environment of early and late successional plants. Oecologia 54, 313–316.Google Scholar
Boege, K. (2005) Influence of plant ontogeny on compensation to leaf damage. American Journal of Botany 92, 1632–1640.Google Scholar
Boege, K., Dirzo, R., Siemens, D. & Brown, P. (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecology Letters 10, 177–187.Google Scholar
Botto-Mahan, C., Ramírez, P.A., Ossa, C.G., Medel, R., Ojeda-Camacho, M. & González, A.V. (2011) Floral herbivory affects female reproductive success and pollinator visitation in the perennial herb Alstroemeria ligtu (Alstroemeriaceae). International Journals of Plant Sciences 172, 1130–1136.Google Scholar
Bruinsma, M., Lucas-Barbosa, D., tem Broeke, C.J., van Dam, N.M., Dick, M. & Van Loon, J.J. (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. Journal of Chemical Ecology 40, 39–49.Google Scholar
Cardel, Y.J. & Koptur, S. (2010) Effects of florivory on the pollination of flowers: an experimental field study with perennial plant. International Journal of Plant Sciences 171, 283–292.Google Scholar
Coley, P.D. & Barone, J.A. (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology, Evolution, and Systematics 27, 305–335.Google Scholar
Côrrea, M.M., Bieber, A.G., Wirth, R. & Leal, I.R. (2005) Occurrence of Atta cephalotes (L.) (Hymenoptera: Formicidae) in Alagoas, northeastern Brazil. Neotropical Entomology 34, 695–698.Google Scholar
Costa, A.N., Vasconcelos, H.L., Vieira-Neto, E.H.M. & Bruna, E.M. (2008) Do herbivores exert top-down effects in Neotropical savannas? Estimates of biomass consumption by leaf-cutter ants. Journal of Vegetation Science 19, 849–854.Google Scholar
Costa, A.N., Vasconcelos, H.L. & Bruna, E.M. (2017) Biotic drivers of seedling establishment in Neotropical savannas: selective granivory and seedling herbivory by leaf-cutter ants as an ecological filter. Journal of Ecology 105, 132–141.Google Scholar
Crawley, M.J. (1983) Herbivory: The Dynamics of Animal Plant Interactions. Oxford, Blackwell Science.Google Scholar
Dalling, J. & Wirth, R. (1998) Dispersal of Miconia argentea seeds by leaf-cutting ant Atta colombica. Journal of Tropical Ecology 14, 705–710.Google Scholar
Dirzo, R. (1984a) Insect-plant interactions: some ecophysiological consequences of herbivory. pp. 209–224 in Medina, E., Mooney, H.A. & Vázquez-Yánes, C. (Eds) Physiological Ecology of Plants of the wet Tropics. Dordrecht, Springer.Google Scholar
Dirzo, R. (1984b) Herbivory, a phytocentric review. pp. 141–65 in Dirzo, R. & Sarukhan, J. (Eds) Perspectives in Plant Population Biology. Sunderland, MA, Sinauer.Google Scholar
Dohm, C., Leal, I.R., Tabarelli, M., Meyer, S.T. & Wirth, R. (2011) Leaf-cutting ants proliferate in the Amazon: an expected response to forest edge? Journal of Tropical Ecology 27, 645–649.Google Scholar
Falcão, P.F. (2004) Efeito da fragmentação florestal na diversidade de plantas cortadas pela formiga cortadeiras Atta cephalotes. Master thesis, Universidade Federal de Pernambuco, Brazil.Google Scholar
Falcão, P.F., Pinto, S.R.R., Wirth, R. & Leal, I.R. (2011) Edge-induced narrowing of dietary diversity in leaf-cutting ants. Bullettin Entomological Research 101, 305–311.Google Scholar
Farji-Brener, A.G. & Tadey, M. (2017) Consequences of leaf-cutting ants on plant fitness: integrating negative effects of herbivory and positive effects from soil improvement. Insectes Sociaux 64, 45–54.Google Scholar
Fornoni, J. (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Functional Ecology 25, 399–407.Google Scholar
García, M.B. & Ehrlén, J. (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population level. American Journal of Botany 89, 1295–1302.Google Scholar
Goldenberg, R. & Shepherd, G.J. (1998) Studies on reproductive biology of Melastomataceae in ‘cerrado’ vegetation. Plant Systematics and Evolution 211, 13–29.Google Scholar
Haines, B. (1975) Impact of leaf-cutting ants on vegetation development at Barro Colorado Islands. pp. 99–111 in Golley, F.G. & Medina, E. (Eds) Tropical Ecology Systems. Berlin, Springer Verlag.Google Scholar
Herz, H., Beyschlag, W. & Hölldobler, B. (2007) Herbivory rate of leaf-cutting ants in a tropical moist in Panama at the population and ecosystem scales. Biotropica 39, 482–488.Google Scholar
Huntly, N. (1991) Herbivores and the dynamics of communities and ecosystems. Annual Review of Ecology and Systematics 22, 477–503.Google Scholar
IBGE (1992) Manual técnico da vegetação brasileira. Rio de Janeiro, Brasil, IBGE.Google Scholar
Krupnik, G.A. & Weis, A.E. (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80, 135–149.Google Scholar
Leal, I.R., Wirth, R. & Tabarelli, M. (2014) The multiple impacts of leaf-cutting ants and their novel ecological role in human-modified neotropical forests. Biotropica 46, 516–528.Google Scholar
Lehtilä, K. & Strauss, S.Y. (1999) Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphnus raphanistrum. Ecology 80, 116–124.Google Scholar
Maron, J.L. (1998) Herbivore above- and belowground: individual and joint effects on plant fitness. Ecology 79, 1281–1293.Google Scholar
Maron, J.L. & Crone, E. (2006) Herbivory effects on plant abundance, distribution and plant growth. Proceeding Royal Society Biological Sciences 273, 2575–2584.Google Scholar
Marquis, R.J. (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226, 537–539.Google Scholar
Marquis, R.J. (1992) A bite is a bite is a bite? Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73, 143–152.Google Scholar
Meyer, S., Leal, I.R. & Wirth, R. (2009) Persisting hyper-abundance of leaf-cutting ants (Atta spp.) at the edge of an old Atlantic forest fragment. Biotropica 41, 711–716.Google Scholar
Mothershead, K. & Marquis, R.J. (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81, 30–40.Google Scholar
Mundim, F.M., Bruna, E.M., Vieira-Neto, E.H.M. & Vasconcelos, H.L. (2012) Attack frequency and the tolerance to herbivory of Neotropical savanna trees. Oecologia 168, 405–414.Google Scholar
Poveda, K., Steffan-Dewenter, I., Scheu, S. & Tscharntke, T. (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601–605.Google Scholar
Prokopy, R.J. & Owens, E.D. (1983) Visual detection of plants by herbivorous insects. Annual Review of Entomology 28, 337–364.Google Scholar
Puentes, A. & Agren, J. (2012) Additive and non-additive effects of simulated leaf and inflorescence damage on survival, growth and reproduction of the perennial herb Arabidopsis lyrata. Oecologia 169, 1033–1042.Google Scholar
R Development Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing.Google Scholar
Rausher, M.D. & Feeny, P. (1980) Herbivory, plant density, and plant reproductive success: the effect of Battus philenor on Aristolochia reticulata. Ecology 61, 905–917.Google Scholar
Rockwood, L.L. (1973) The effect of defoliation on seed production of six Costa Rican tree species. Ecology 54, 1363–1369.Google Scholar
Silva, P.D., Leal, I.R., Wirth, R. & Tabarelli, M. (2007) Harvesting of Protium heptaphyllum (Aubl.) March. Seeds (Burseraceae) by leaf-cutting ant Atta sexdens L. promotes seed aggregation and seedling mortality. Revista Brasileira de Botânica 30, 553–560.Google Scholar
Siqueira, F.F.S., Ribeiro-Neto, J.D., Tabarelli, M., Andersen, A.N., Wirh, R. & Leal, I.R. (2017) Leaf-cutting ants populations also profit from human disturbances in dry forests. Journal of Tropical Ecology 33, 337–344.Google Scholar
Strauss, S.Y. (1997) Floral characters link herbivores, pollinators and plant fitness. Ecology 78, 179–185.Google Scholar
Tabarelli, M. & Mantovani, W. (1999) Clareiras naturais e riqueza de espécies pioneiras em uma floresta Atlântica Montana. Revista Brasileira de Biologia 59, 251–261.Google Scholar
Tito, R., Castellani, T.T., Fáveri, S.B., Lopes, B.C. & Vasconcelos, H.L. (2016) From over to undercompensation: variable responses to herbivory during ontogeny of a Neotropical monocarpic plant. Biotropica 48, 608–617.Google Scholar
Trumble, J.T., Kolodny-Hirsch, D.M. & Ting, I.P. (1993) Plant compensatory for arthropod herbivory. Annal Review of Entomology 38, 93–119.Google Scholar
Urbas, P., Araújo Júnior, M.V., Leal, I.R. & Wirth, R. (2007) Cutting more from cut forests – edge effects on foraging and herbivory of leaf-cutting ants. Biotropica 39, 489–495.Google Scholar
Veloso, H.P., Rangel, A.L.R. & Lima, J.C.A. (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. Rio de Janeiro, Brasil, IBGE.Google Scholar
Wirth, R., Beyschlag, W., Ryel, R.J. & Hölldobler, B. (1997) Annual foraging of the leaf-cutting ant Atta colombica in a semidecidious rain forest in Panama. Journal of Tropical Ecology 13, 741–757.Google Scholar
Wirth, R., Herz, H., Ryel, R.J., Beyschlag, W. & Hölldobler, B. (2003) Herbivory of Leaf-Cutting Ants – A Case Study on Atta colombica in the Tropical Rainforest of Panama. Berlin, Heidelberg, Springer.Google Scholar
Wirth, R., Meyer, S.T., Almeida, W.R., Araújo, M.V., Barbosa, V.S. & Leal, I.R. (2007) Increasing densities of leaf-cutting ants (Atta sp.) with proximity to the edge in a Brazilian Atlantic Forest. Journal of Tropical Ecology 23, 501–505.Google Scholar
Wise, M.J. & Cummins, J.J. (2006) Strategies of Solanum corolinense for regulating maternal investment in response to foliar and floral herbivory. Journal of Ecology 94, 629–636.Google Scholar
Wise, M.J. & Abrahamson, W.G. (2007) Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models. American Naturalist 169, 443–454.Google Scholar