Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

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Patterns of herbivory in Vassobia breviflora (Solanaceae): variation in foliar damage and natural selection mediated by herbivores
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Keywords

plant-animal interactions
phenotypic selection
functional groups
leaf traits
herbivory levels
damage patterns.
interacciones planta-animal
selección fenotípica
grupos funcionales
rasgos foliares
niveles de herbivoría
patrones de daño.

How to Cite

Valoy, M., Ordano, M., Bernacki, F., Palacio, F. X., López-Acosta, J. C., & Varela, O. (2018). Patterns of herbivory in Vassobia breviflora (Solanaceae): variation in foliar damage and natural selection mediated by herbivores. Revista De Biología Tropical, 66(4), 1683–1700. https://doi.org/10.15517/rbt.v66i4.31869

Abstract

Herbivore mediated-selection shapes the evolution of defensive plant traits. Knowledge about the role of herbivores as mediators of selection is scarce and even more if herbivore functional groups are considered. The objectives of this work were (1) to describe the variation in foliar traits between populations and both between and intra-plants within a population, (2) to explore the relationship between the variation in the herbivory level and foliar traits, (3) to determine the relationship between leaf traits and damage patterns and (4) estimate the selection regimes by different herbivore functional groups. We conducted this study in four populations of Vassobia breviflora in Northwestern Argentina (Yungas). The foliar traits considered were size, leaf area (af), shape (leaf length / width ratio; laf) and proportion of leaf area removed (pafr) (N = 1 582 leaves, 57 plants). The herbivores consumed 15.6 % of the leaf area and 76.8 % of the variation in the pafr occurred at the sub-individual level. The damage pattern was dominated by cutter herbivores (70 %), followed by a dotted herbivory pattern (22 %), mixed 5 % and 1 % miner. Nonlinear selection was detected for laf (γii = -0.180; EE = 0.76; P < 0.05), and correlational selection between the cutter damage and af (γij = -1.297; SE = 0.62; P < 0.05) and between the dotted damage and af (γij = -1.130; SE = 0.76; P < 0.05). Natural selection favored plants with small leaves and high foliar removal and large leaves with less damage and selection against larger leaves with greater damage was detected. In addition, deduced from the relationship between the damage type and the relative fitness, the selection would favor the dotted damage over the cutter one. The plants would resolve the conflict with the herbivores according to the damage type and natural selection would regulate the foliar display as a strategy to deal with the herbivore diversity.

https://doi.org/10.15517/rbt.v66i4.31869
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References

Agrawal, A. A., & Weber, M. G. (2015). On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecology Letters, 18, 985-991.

Anton, A. M., & Zuloaga, F. O. (2013). Recuperado de http://www.floraargentina.edu.ar

Ågren, J., Hellström, F., Toräng, P., & Ehrlén, J. (2013). Mutualists and antagonists drive among-population variation in selection and evolution of floral display in a perennial herb. Proceedings of the National Academy of Sciences, 110, 18202-18207.

Avila- Sakar, G., Leist, L. L., & Stephenson, A. G. (2003). Effects of the spatial pattern of leaf damage on growth and reproduction: nodes and branches. Journal of Ecology, 91, 867-879.

Ayarde, H. (2005). Hidrología en bosques subtropicales de montaña en Argentina. En M. Ataroff, & J. Silva (Eds.), Dinámica Hídrica en Sistemas Neotropicales (pp. 37-42). Mérida, Venezuela: ICAE, Universidad de Los Andes.

Badenes-Perez, F. R., Reichelt, M., Gershenzon, J., & Heckel, D. G. (2014). Using plant chemistry and insect preference to study the potential of Barbarea (Brassicaceae) as a dead-end trap crop for diamondback moth (Lepidoptera: Plutellidae). Phytochemistry, 98, 137-144.

Baldwin, I. T., & Schultz, J. C. (1983). Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science, 221, 277-279.

Bernacki F. G. (2014). Biología floral y frutal de Vassobia breviflora (Sedtn.) Hunz. (Solanaceae) en el noroeste argentino (Tesis de licenciatura). Universidad Nacional de Tucumán, Argentina.

Bernacki, F. G., Albornoz, P., Valoy, M., & Ordano, M. (2015). Anatomía de flor y fruto de Vassobia breviflora (Solanaceae) en el sur de las Yungas Australes (Argentina). Phyton-International Journal of Experimental Botany, 82, 478-487.

Bernays, E., & Graham, M. (1988). On the evolution of host specificity in phytophagous arthropods. Ecology, 69, 886-892.

Bianchi, A. R., & Yáñez, C. E. (1992). Las Precipitaciones en el Noroeste Argentino. Salta, Argentina: Ediciones Guadarrama Madrid.

Brennan, E. B., & Weinbaum, S. A. (2001). Performance of adult psyllids in nochoice experiments on juvenile and adult leaves of Eucalyptus globulus. Entomologia Experimentalis et Applicata, 100, 179-185.

Brennan, E. B., Weinbaum, S. A., Rosenheim, J. A., & Karban, R. (2001). Heteroblasty in Eucalyptus globulus (Myricales:Myricaceae) affects ovipositional and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera:Psyllidae). Environmental Entomology, 30, 1144-1149.

Breheny, P., & Burchett, W. (2015). Visualization of regression models using visreg. Recuperado de https://cran.r-project.org/web/packages/visreg/index

Brown, V. K., Lawton, J. H., & Grubb, P. J. (1991). Herbivory and the evolution of leaf size and shape [and discussion]. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 333(1267), 265-272.

Brown, A. D., & Corcuera, J. (1999). Donación de nuevas áreas protegidas en las Yungas de la Argentina (Informe Técnico). Argentina: LIEY/FVSA.

Brown, A. D., Grau, A., Lomáscolo, T., & Gasparri, N. I. (2002). Una estrategia de conservación para las selvas subtropicales de montaña (Yungas) de Argentina. Ecotropicos, 15, 147-159.

Cabrera, A. L. (1976). Territorios fitogeográficos de la Republica Argentinas. En W. F. Kugler (Eds.), Enciclopedia Argentina de Agricultura y Jardinería, 2, 1-85.

Cabrera, A. L. (1979). Solanaceae. En A. Burkart (Eds.), Flora Ilustrada de Entre Ríos V (Argentina) (pp. 346-452). Buenos Aires, Argentina: Instituto Nacional de Tecnología Agropecuaria.

Campitelli, B. E., Simonsen, A. K., Wolf, A. R., Manson, J. S., & Stinchcombe, J. R. (2008). Leaf shape variation and herbivore consumption and performance: a case study with Ipomoea hederacea and three generalists. Arthropod-Plant Interactions, 2, 9-19.

Canto Aguilar, M. A. (2004). Herbivoría crecimiento y reproducción de Anthurium schlechtendalii Kunth (Araceae) en ecosistemas diferentes (Tesis doctoral). Xalapa, Veracruz, México.

Cárdenas, R. E., Valencia, R., Kraft, N. J., Argoti, A., & Dangles, O. (2014). Plant traits predict inter-and intraspecific variation in susceptibility to herbivory in a hyperdiverse Neotropical rain forest tree community. Journal of Ecology, 102, 939-952.

Carmona, D., Lajeunesse, M. J., & Johnson, M. T. J. (2011). Plant traits that predict resistance to herbivores. Functional Ecology, 25, 358-367.

Chen, Y. S., Chesson, P., Wu, H. W., Pao, S. H., Liu, J. W., Chien, L. F., … Sheue, C. R. (2017). Leaf structure affects a plant’s appearance: combined multiple-mechanisms intensify remarkable foliar variegation. Journal of Plant Research, 130, 311-325.

Coley, P. D., Bryant, J. P., & Chapin, F. S. (1985). Resource Availability and Plant Antiherbivore Defense. Science, 230, 895-899.

Crawley, M. J. (1997). Plant-herbivore dynamics. In M. J. Crawley (Eds.), Plant Ecology (pp. 401-474). Oxford, England: Blackwell Science.

Crawley, M. J. (2007). The R book. West Sussex, England: John Wiley & Sons.

Digilio, A. P., & Legname, P. R. (1966). Los árboles indígenas de la Provincia de Tucumán. Opera Lilloana, 15, 1-107.

Dirzo, R. (1984). Herbivory: a phytocentric overview. In R. Dirzo, & J. Sarukhán (Eds.), Perspectives on plant population ecology (pp. 141-165). Sunderland, USA: Sinauer Associates Inc.

Edwards, P. B. (1982). Do waxes on Eucalyptus leaves provide protection from grazing insects? Australian Journal of Ecology, 7, 347-352.

Feeny, P. (1976). Plant apparency and chemical defense. In J. Wallace, & R. L. Mansell (Eds.), Biochemical interaction between plants and insects. Recent advances in phytochemistry (pp. 1-40). USA: Springer.

Ferrari, S. L. P., & Cribari-Ñeto, F. (2004). Beta Regression for Modeling Rates and Proportions. Journal of Applied Statistics, 31, 799-815.

Geber, M. A., & Griffin, L. A. (2003). Inheritance and natural selection on functional traits. International Journal of Plant Sciences, 164, S21-S42.

Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/ hierarchical models. Cambridge, UK: Cambridge University Press.

Gerasymenko, V. (2017). The Model of Fitness in a Heterogeneous Environment on Reaction Norms. Proceedings of the Latvian Academy of Sciences, 71(4), 303-306.

Giannini, N. P. (1999). La interacción de aves-murciélagos-plantas en el sistema de frugivoría y dispersión de las semillas en San Javier, Tucumán, Argentina (Tesis doctoral). Universidad Nacional de Tucumán, Tucumán, Argentina.

Gilbert, L. E. (1979). Development of theory in the analysis of insect-plant interactions. Analysis of Ecological Systems, 117-154.

Givnish, T. J. (1990). Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage. Functional Ecology, 463-474.

Hare, D. (2012). How insect herbivores drive the evolution of plants. Science, 338, 50-51.

Heinrich, B. (1979). Foraging strategies of caterpillars. Oecologia, 42, 325-337.

Hendrix, S. D. (1988). Herbivory and its impact on plant reproduction. Plant Reproductive Ecology, 246-263.

Herrera, C. M. (2009). Multiplicity in unity: plant subindividual variation and interaction with animals. Chicago, USA: University of Chicago Press.

Hikosaka, K. (2005). Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Annals of Botany, 95, 521-533.

Honêk, A., & Martinková, Z. (2002). Factors of between- and within- plant distribution of Metopolophium dirhodum (Homoptera: Aphididae) on small grain cereals. Journal of Applied Entomology, 126, 378-383.

Hueck, K. (1978). Los bosques de Sudamérica. Ecología composición e importancia económica. Eschborn, República Federal de Alemania: GTZ.

Johnson, S. N., Clark, K. E., Hartley, S. E., Jones, T. H., McKenzie, S. W., & Koricheva, J. (2012). Aboveground-belowground herbivore interactions: a meta-analysis. Ecology, 93, 2208-2215.

Karban, R., Agrawal, A. A., Thaler, J. S., & Adler, L. S. (1999). Induced plant responses and information content about risk of herbivory. Trends in Ecology & Evolution, 14, 443-447.

Kovalev, A. E., Filippov, A. E., & Gorb, S. N. (2013). Insect wet steps: loss of fluid from insect feet adhering to a substrate. Journal of the Royal Society Interface, 10, 201-239.

Kurokawa, H., & Nakashizuka, T. (2008). Leaf herbivory and decomposability in a Malaysian tropical rain forest. Ecology, 89, 2645-2656.

Kursar, T. A., & Coley, P. D. (2003). Convergence in defense syndromes of young leaves in tropical rainforests. Biochemical Systematics and Ecology, 31, 929-949.

Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 1210-1226.

Lehndal, L. & Ågren, J. (2015). Latitudinal variation in resistance and tolerance to herbivory in the perennial herb Lythrum salicaria is related to intensity of herbivory and plant phenology. Journal of Evolutionary Biology, 28, 576-589.

Lehtilä, K. (1999). Impact of herbivore tolerance and resistance on plant life histories. In T. Vuorisalo, & P. Mutikainen (Eds.), Life-history Evolution in Plants (pp. 303-328). Dordrecht, Netherlands: Kluwer Academic Publishers.

Lev-Yadun, S. (2016). Plants are not sitting ducks waiting for herbivores to eat them. Plant Signaling & Behavior, 11(5), e1179419.

Li, W., Luo, J., Tian, X., Peng, C., & Zhou, X. (2012). Patterns of defoliation and their effect on the plant growth and photosynthetic characteristics of Ipomoea cairica. Weed Biology and Management, 12, 40-46.

Linhart, Y. B., & Grant, M. C. (1996). Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics, 27, 237-277.

Marquis, R. J. (1991). Herbivore fauna of Piper (Piperaceae) in a Costa Rican wet forest: Diversity, specificity and impact. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes, & W. W. Benson (Eds.), Plant- Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions (pp. 197-208). New York, USA: Wiley & Sons.

Marquis, R. J. (1992). The selective impact of herbivores. In R. S Fritz, & E. L Simms (Eds.), Plant resistance to herbivores and pathogens (pp. 301-325). Chicago, USA: University of Chicago Press.

Marquis, R. J., Salazar, D., Baer, C., Reinhardt, J., Priest, G., & Barnett, K. (2016). Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation. Ecology, 97, 2939-2951.

Mauricio, R., Bowers, M. D., & Bazzaz, F. A. (1993). Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology, 2066-2071.

MacColl, A. D. (2011). The ecological causes of evolution. Trends in Ecology & Evolution, 26, 514-522.

Meyer, S. T., Roces, F., & Wirth, R. (2006). Selecting the drought stressed: effects of plant stress on intraspecific and within- plant herbivory patterns of the leafcutting ant Atta colombica. Functional Ecology, 20, 973-981.

Morrison, K. D., & Reekie, E. G. (1995). Pattern of defoliation and its effect on photosynthetic capacity in Oenothera biennis. Journal of Ecology, 83, 759-767.

Nguyen, D., Rieu, I., Mariani, C., & van Dam, N. M. (2016). How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Molecular Biology, 91(6), 727-740.

O’Neill, G. A., Aitken, S. N., King, J. N., & Alfaro, R. I. (2002). Geographic variation in resin canal defenses in seedlings from the Sitka spruce x white spruce introgression zone. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 32, 390-400.

Palacio, F. X., Valoy, M., Bernacki, F., Sánchez, M. S., Núñez-Montellano, M. G., Varela, O., & Ordano, M. (2017). Bird fruit consumption results from the interaction between fruit-handling behaviour and fruit crop size. Ethology Ecology & Evolution, 29, 24-37.

Pigliucci, M. (2003). Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecology Letters, 6, 265-272.

Pilson, D. (2000). The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evolutionary Ecology, 14, 457-489.

Pinehiro, J., Bates, D., DebRoy, S., & Sarkar, D. (2012). NLME: Linear and nonlinear mixed effects models. Recuperado de http://cran.r-project.org/web/packages/nlme/nlme.pdf

Powell, J. S., & Raffa, K. F. (1999). Sources of variation in concentration and composition of foliar monoterpenes in tamarack (Larix laricina) seedlings: roles of nutrient availability, time of season, and plant architecture. Journal of Chemical Ecology, 25, 1771-1797.

Propoky, R. J., & Owens, E. D. (1983). Visual detection of plants by herbivorous insects. Annual Review of Entomology, 28, 337-364.

R Core Team (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Recuperado de http://www.R-project.org/

Rasband, W. (1997). ImageJ. National Institutes of Health, USA. Recuperado de http://rsb.info.nih.gov/ij

Rhoades, D. F. (1979). Evolution of plant chemical defense against herbivores. In G. A Rosenthal, & D. H Janzen (Eds.), Herbivores: Their Interactions with Secondary Plant Metabolites (pp. 3-54). New York, USA: Academic Press.

Royer, D. L. (2012). Leaf Shape Responds to Temperature but not CO 2 in Acer rubrum. PloS one, 7, e49559.

Santillán de Andrés, S., Barbieri de Santamarina, E., Ricci, T. R., & Würschmidt, E. J. (1967). La región de las Sierras del Nordeste de la provincia de Tucumán. Tucumán: Universidad Nacional de Tucumán, Departamento de Geografía, Facultad de Filosofía y Letras. Serie Monográfica, 16, 1-89.

Sarkar, D. (2015). Lattice: Multivariate Data Visualization with R. New York, USA: Springer.

Schmitt, T. M., Hay, M. E., & Lindquist, N. (1995). Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology, 107-123.

Schowalter, T. D., Hargrove, W., & Crossley, D. A. (1986). Herbivory in forested ecosystems. Annual Review of Entomology, 31, 177-196.

Schuldt, A., Bruelheide, H., Durka, W., Eichenberg, D., Fischer, M., & Kröber, W. (2012). Plant traits affecting herbivory on tree recruits in highly diverse subtropical forests. Ecology Letters, 15, 732-739.

Schultz, J. C., Appel, H. M., Ferrieri, A. P., & Arnold, T. M. (2013). Flexible resource allocation during plant defense responses. Frontiers in Plant Science, 4.

Shimada, T., Takahashi, A., Shibata, M., & Yagihashi, T. (2015). Effects of within plant variability in seed weight and tannin content on foraging behaviour of seed consumers. Functional Ecology, 29, 1513-1521.

Simas, A. B., & Rocha, A. V. (2015). betareg: Beta Regression. R package version 3.0-5, URL. Recuperado de http://r-project.org/src/contrib/Archive/betareg

Sobral, M., Guitián, J., Guitián, P., & Larrinaga, A. R. (2013). Selective pressure along a latitudinal gradient affects subindividual variation in plants. PloS one, 8, e74356.

Strauss, S. Y., Conner, J. K., & Lehtilä, K. P. (2001). Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. The American Naturalist, 158, 496-504.

Strauss, S. Y., Rudgers, J. A., Lau, J. A., & Irwin, R. E. (2002). Direct and ecological costs of resistance to herbivory. Trends in Ecology & Evolution, 17, 278-285.

Taura, H. M., & Laroca, S. (2004). Biologia da polinização: interações entre as abelhas (Hym., Apoidea) e as flores de Vassobia breviflora (Solanaceae) [Pollination biology: interactions between bees and flowers of Vassobia breviflora (Solanaceae)]. Acta Biologica Paranaense, 33, 143-162.

Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. Chicago, USA: University of Chicago Press.

Valoy, M., Ordano, M., & Benavídez, A. (2012). Herbivoría foliar y autonomía de ramas en Psychotria carthagenensis (Rubiaceae). Lilloa, 49, 68-77.

Valverde, P. L., Fornoni, J., & Núñez-Farfán, J. (2001). Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. Journal of Evolutionary Biology, 14, 424-432.

Warner, P. J., & Cushman, H. J. (2002). Influence of herbivores on a perennial plant: variation with life history stage and herbivore species. Oecologia, 132, 77-85.

Wade, M. J., & Kalisz, S. (1990). The causes of Natural Selection. Evolution, 44, 1947-1955.

Weis, A. E., & Gorman, W. L. (1990). Measuring selection on reaction norms: an exploration of the Eurosta Solidago system. Evolution, 44, 820-831.

Weis, A. E., Abrahamson, W. G., & Andersen, M. C. (1992). Variable selection on Eurosta's gall size, I: the extent and nature of variation in phenotypic selection. Evolution, 46, 1674-1697.

Whitham, T. G. (1983). Host manipulation of parasites: within-plant variation as a defense against rapidly evolving pests. In R. F. Denno, & M. S. McClure (Eds.), Variable Plants and Herbivores in Natural and Managed Systems (pp. 15-41). New York, USA: Academic Press.

Wilson, D., & Faeth, S. H. (2001). Do fungal endophytes result in selection for leafminer ovipositional preference? Ecology, 82, 1097-1111.

Winn, A. A. (1996). The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutinary Biology, 9, 737-752.

Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., & Smith, G. M. (Eds.) (2009). In Mixed effects modelling for nested data. Mixed effects models and extensions in ecology with R (pp. 101-142). New York, USA: Springer.

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