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Changes in spinescence across leaf ontogeny support the optimal defence hypothesis in blackberries (Rubus adenotrichos)

Published online by Cambridge University Press:  10 July 2023

Alejandro Farji-Brener Open the ORCID record for Alejandro Farji-Brener [Opens in a new window] ,
Débora Elías Díaz Open the ORCID record for Débora Elías Díaz [Opens in a new window] ,
Isabelle Holanda Open the ORCID record for Isabelle Holanda [Opens in a new window] ,
Andrés Sierra Ricaurte Open the ORCID record for Andrés Sierra Ricaurte [Opens in a new window] ,
Kenneth Barrantes Open the ORCID record for Kenneth Barrantes [Opens in a new window]  and
Pablo José Gutiérrez-Campos Open the ORCID record for Pablo José Gutiérrez-Campos [Opens in a new window]
Alejandro Farji-Brener*
Affiliation:
LIHO, Inibioma, Conicet-Universidad Nacional del Comahue, Argentina
Débora Elías Díaz
Affiliation:
Universidad de El Salvador, Facultad Multidisciplinaria de Occidente, El Salvador
Isabelle Holanda
Affiliation:
Laboratorio de interacción planta-animal, Universidad Federal de Pernambuco, Brasil
Andrés Sierra Ricaurte
Affiliation:
Universidad Nacional de Colombia, Colombia
Kenneth Barrantes
Affiliation:
Universidad de Costa Rica, Costa Rica
Pablo José Gutiérrez-Campos
Affiliation:
Universidad Nacional de Costa Rica, Costa Rica
*
Corresponding author: Alejandro Farji-Brener; Email: alefarji@yahoo.com
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Abstract

Hypotheses based on allocation theory and herbivore selection offer opposite predictions about how defence levels against herbivores change as the plant tissue grows. The growth differentiation balance hypothesis (GDBH) assumes that defences will be resource-limited in immature tissues and predict that defence levels increase as the plant tissue grows. Conversely, the optimal defence hypothesis (ODH) proposes that plants would have the highest level of defences in the parts that have the highest value in terms of fitness and/or are more frequently attacked by herbivores, such as young tissues. We examine whether spinescence in the shrub Rubus adenotrichos (blackberry) change as the leaf grows, and if this change is consistent with the GDBH or the ODH. We compare the petiole area occupied by prickles, the prickles density and the individual prickle area in mature versus young petioles from Rubus adenotrichos. Our results show that, in R. adenotrichos, young tissues are more protected than mature tissues. Prickles density and the petiole area occupied by prickles were up to 25% higher in young petioles than in mature ones. These results support the ODH, reinforcing the idea that extrinsic factors such as herbivores pressure might drive the change of structural defences level across leaf ontogeny.

Keywords

Costa Ricaherbivorytropical montane forestplant physical defences
Type
Research Article
Information
Journal of Tropical Ecology , Volume 39 , 2023 , e30
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Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Archibald, S and Bond, WJ (2003) Growing tall vs growing wide: tree architecture and allometry of Acacia karroo in forest, savanna, and arid environments. Oikos 102(1), 3–14.CrossRefGoogle Scholar
Armani, M, Charles-Dominique, T, Barton, KE and Tomlinson, KW (2019) Developmental constraints and resource environment shape early emergence and investment in spines in saplings. Annals of Botany 124(7), 1133–1142.CrossRefGoogle Scholar
Armani, M, Goodale, UM, Charles-Dominique, T, Barton, KE, Yao, X and Tomlinson, KW (2020) Structural defence is coupled with the leaf economic spectrum across saplings of spiny species. Oikos 129(5), 740–752.CrossRefGoogle Scholar
Barto, EK and Cipollini, D (2005) Testing the optimal defence theory and the growth-differentiation balance hypothesis in Arabidopsis thaliana . Oecologia 146(2), 169–178.CrossRefGoogle ScholarPubMed
Barton, KE and Koricheva, J (2010) The ontogeny of plant defence and herbivory: characterizing general patterns using meta-analysis. The American Naturalist 175(4), 481–493.CrossRefGoogle ScholarPubMed
Boege, K, Dirzo, R, Siemens, D and Brown, P (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecology Letters 10(3), 177–187.CrossRefGoogle ScholarPubMed
Boege, K and Marquis, RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution 20(8), 441–448.CrossRefGoogle ScholarPubMed
Bryant, JP, Reichardt, PB, Clausen, TP, Provenza, FD and Kuropat, PJ (1992) Woody plant-mammal interactions. In Rosenthal, GA and Berenbaum, MR (eds). Herbivores: their interactions with secondary plant metabolites. 2nd ed. Vol. 2: evolutionary and ecological processes. Academic Press.Google Scholar
Castro, J and Cerdas, M (2005) Mora (Rubus spp) Cultivo y Manejo Pos-cosecha. San José, Costa Rica: MAG (Ministerio de Agricultura).Google Scholar
Charles-Dominique, T, Barczi, JF, Le Roux, E and Chamaillé-Jammes, S (2017) The architectural design of trees protects them against large herbivores. Functional Ecology 31(9), 1710–1717.CrossRefGoogle Scholar
Clark, LL and Burns, KC (2015) The ontogeny of leaf spines: progressive versus retrogressive heteroblasty in two New Zealand plant species, New Zealand Journal of Botany 53(1), 15–23. https://doi.org/10.1080/0028825X.2014.997254 CrossRefGoogle Scholar
Coley, PD and Barone, JA (1996) Herbivory and plant defences in tropical forests. Annual Review of Ecology and Systematics 27(1), 305–335.CrossRefGoogle Scholar
Cooper, SM and Owen-Smith, N (1986) Effects of plant spinescence on large mammalian herbivores. Oecologia 68(3), 446–455.CrossRefGoogle ScholarPubMed
Cornelissen, JH, Lavorel, S, Garnier, E, Díaz, S, Buchmann, N, Gurvich, DE, … Poorter, H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51(4), 335–380.CrossRefGoogle Scholar
Coverdale, TC (2019) Defence emergence during early ontogeny reveals important differences between spines, thorns and prickles. Annals of Botany 124(7), iii–iv.CrossRefGoogle Scholar
Crofts, SB and Stankowich, T (2021) Stabbing spines: a review of the biomechanics and evolution of defensive spines. Integrative and Comparative Biology 61(2), 655–667.CrossRefGoogle ScholarPubMed
Cronin, G and Hay, ME (1996) Within-plant variation in seaweed palatability and chemical defences: optimal defence theory versus the growth-differentiation balance hypothesis. Oecologia 105(3), 361–368.CrossRefGoogle ScholarPubMed
Fenner, M, Hanley, ME and Lawrence, R (1999) Comparison of seedling and adult palatability in annual and perennial plants. Functional Ecology 13(4), 546–551.CrossRefGoogle Scholar
Fordyce, JA and Agrawal, AA (2001) The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. Journal of Animal Ecology 70(6), 997–1005.CrossRefGoogle Scholar
Gowda, JH (1996) Spines of Acacia tortilis: what do they defend and how? Oikos, 279–284.CrossRefGoogle Scholar
Gowda, JH and Palo, RT (2003) Age-related changes in defensive traits of Acacia tortilis Hayne. African Journal of Ecology 41, 218–223.CrossRefGoogle Scholar
Hammel, EB, Grayum, MH, Herrera, C and Zamora, N (2014) Manual De Plantas De Costa Rica . St. Louis, Mo.: Missouri Botanical Garden.Google Scholar
Hanley, ME, Lamont, BB, Fairbanks, MM and Rafferty, CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8(4), 157–178.CrossRefGoogle Scholar
Hay, ME, Kappel, QE and Fenical, W (1994) Synergisms in plant defences against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75(6), 1714–1726.CrossRefGoogle Scholar
Herms, DA (1999) Physiological and abiotic determinants of competitive ability and herbivore resistance. Phyton 39, 53–64.Google Scholar
Herms, DA and Mattson, WT (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology, 67(3), 283–335.CrossRefGoogle Scholar
Herms, DA and Mattson, WT (1994) Plant growth and defence. Trends Ecology Evolution 9, 488.CrossRefGoogle Scholar
Holdridge, LR (1967) Life zone ecology. San José, Costa Rica: Tropical Science Center, 206 pp.Google Scholar
Kandylis, K, Hadjigeorgiou, I and Harizanis, P (2009) The nutritive value of mulberry leaves (Morus alba) as a feed supplement for sheep. Tropical Animal Health and Production 41(1), 17–24.CrossRefGoogle ScholarPubMed
Kappelle, M, & Horn, SP (2016) The Páramo ecosystem of Costa Rica’s highlands. Costa Rican Ecosystems 744.CrossRefGoogle Scholar
Kariñho-Betancourt, E, Agrawal, A, Halitschke, R and Núñez-Farfán, J (2015) Phylogenetic correlations among chemical and physical plant defenses change with ontogeny. New Phytologist 206(2), 796–806.CrossRefGoogle ScholarPubMed
Kellogg, AA, Branaman, TJ, Jones, NM, Little, CZ and Swanson, JD (2011) Morphological studies of developing Rubus prickles suggest that they are modified glandular trichomes. Botany 89(4), 217–226.CrossRefGoogle Scholar
Marquis, RJ (1992) A bite is a bite is a bite? Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73(1), 143–152.CrossRefGoogle Scholar
Matsuki, S, Sano, Y and Koike, T (2004) Chemical and physical defence in early and late leaves in three heterophyllous birch species native to northern Japan. Annals of Botany 93(2), 141–147.CrossRefGoogle ScholarPubMed
McCall, AC and Fordyce, JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? Journal of Ecology 98, 985–992.CrossRefGoogle Scholar
Mithöfer, A and Boland, W (2012) Plant defence against herbivores: chemical aspects. Annual Review of Plant Biology 63, 431–450.CrossRefGoogle ScholarPubMed
Moreira, X, Abdala-Roberts, L, Galmán, A, Bartlow, AW, Berny-Mier y Teran, JC, Carrari, E, … Rasmann, S (2020) Ontogenetic consistency in oak defence syndromes. Journal of Ecology 108, 1822–1834.CrossRefGoogle Scholar
Moreira, X, Zas, R and Sampedro, L (2012) Differential allocation of constitutive and induced chemical defences in pine tree juveniles: a test of the optimal defence theory. PLoS One 7(3), e34006.CrossRefGoogle Scholar
Obeso, JR (1997) The induction of spinescence in European holly leaves by browsing ungulates. Plant Ecology 129(2), 149–156.CrossRefGoogle Scholar
Ochoa-López, S, Damián, X, Rebollo, R, Fornoni, J, Domínguez, CA and Boege, K (2020) Ontogenetic changes in the targets of natural selection in three plant defences. New Phytologist 226(5), 1480–1491.CrossRefGoogle Scholar
Ochoa-López, S, Villamil, N, Zedillo-Avelleyra, P and Boege, K (2015) Plant defence as a complex and changing phenotype throughout ontogeny. Annals of Botany 116(5), 797–806.CrossRefGoogle ScholarPubMed
Ohnmeiss, TE and Baldwin, IT (2000) Optimal defence theory predicts the ontogeny of an induced nicotine defence. Ecology 81, 1765–1783.CrossRefGoogle Scholar
Rasband, WS (1997) Image J1: Image processing and analysis in Java. Maryland, National Institute of Health. Available at https://imagej.net/ImageJ1 Google Scholar
Rhoades, DF (1979) Evolution of plant chemical defence against herbivores. In: Rosenthal, GA and Janzen, DH (eds) Herbivores: their interaction with secondary plant metabolites . New York and London: Academic Press, 4–53.Google Scholar
Wolfson, JL and Murdock, LL (1990) Growth of Manduca sexta on wounded tomato plants: role of induced proteinase inhibitors. Entomologia Experimentalis et Applicata 54, 257–264.CrossRefGoogle Scholar
Woodman, RL and Fernandes, GW (1991) Differential mechanical defense: herbivory, evapotranspiration, and leaf-hairs. Oikos 60(1), 11–19.CrossRefGoogle Scholar
Zangerl, AR and Bazzaz, FA (1992) Theory and pattern in plant defence allocation. In Fritz, RS and Simms, EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago, EEUU, 610 pp.Google Scholar
Zangerl, AR and Rutledge, CE (1996) The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. The American Naturalist 147(4), 599–608.CrossRefGoogle Scholar