Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T09:54:04.878Z Has data issue: false hasContentIssue false

Females restrict the position of domatia and suffer more herbivory than hermaphrodites in Myriocarpa longipes, a neotropical facultative myrmecophyte

Published online by Cambridge University Press:  28 December 2021

Mario A. Sandoval-Molina*
Affiliation:
Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomous University of the State of Mexico, Mexico, Carretera Toluca-Tlachaloya, km 18, Cerrillo Piedras Blancas, CP 50200Toluca, Estado de México, México
Bernardo Rafael Lugo-García
Affiliation:
Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomous University of the State of Mexico, Mexico, Carretera Toluca-Tlachaloya, km 18, Cerrillo Piedras Blancas, CP 50200Toluca, Estado de México, México
Alan Daniel Mendoza-Mendoza
Affiliation:
Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomous University of the State of Mexico, Mexico, Carretera Toluca-Tlachaloya, km 18, Cerrillo Piedras Blancas, CP 50200Toluca, Estado de México, México
Mariusz Krzysztof Janczur
Affiliation:
Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomous University of the State of Mexico, Mexico, Carretera Toluca-Tlachaloya, km 18, Cerrillo Piedras Blancas, CP 50200Toluca, Estado de México, México
*
Author for correspondence: Mario A. Sandoval-Molina, Email: sandoval.m@hotmail.com

Abstract

Domatia are hollow structures in plants occupied by ant colonies, in turn ants provide protection against herbivores. In plants, competition for resources has driven sex-related changes in the patterns of resource allocation to life-history traits and defence traits. The resource-competition hypothesis (RCH) proposes that female plants due to their higher investment in reproduction will allocate fewer resources to defence production, showing greater herbivore damage than other sexual forms. We hypothesise the existence of sex-related differences in defensive traits of domatia-bearing plants, being female plants less defended due to differences in domatia traits, such as size, number of domatia and their position, exhibiting more herbivore damage than hermaphrodite plants of Myriocarpa longipes, a facultative neotropical myrmecophyte. We found eight species of ants inhabiting domatia; some species co-inhabited the same plant, even the same branch. Our results are consistent with the predictions of RCH, as female plants had ant-inhabited domatia restricted to the middle position of their branches and exhibited greater herbivore damage in leaves than hermaphrodites. However, we did not find differences in domatia size and leaf area between sexual forms. Our study provides evidence for intersexual differences in domatia position and herbivory in a facultative ant–plant mutualism in M. longipes. We highlight the importance of considering the plant sex in ant–plant interactions. Differences in resource allocation related to sexual reproduction could influence the outcome of ant–plant interactions.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beattie, AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, England.CrossRefGoogle Scholar
Beaumont, KP, Mackay, DA and Whalen, MA (2016) Ant defence of a dioecious shrub, Adriana quadripartita (Euphorbiaceae), with extrafloral nectaries. Australian Journal of Botany 64, 539546.CrossRefGoogle Scholar
Coley, PD and Aide, TM (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Plant-animal interactions: evolutionary ecology in tropical and temperate regions (eds. Price, PW, Lewinsohn, TM, Fernandes, GW & Benson, WW). Willey & Sons NY, pp. 2549.Google Scholar
Coley, PD and Barone, JA (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27, 305335.CrossRefGoogle Scholar
Cornelissen, T and Stiling, P (2005) Sex-biased herbivory: a meta-analysis of the effects of gender on plant-herbivore interactions. Oikos 111, 488500.CrossRefGoogle Scholar
Davidson, DW (1993) The evolutionary ecology of symbiotic ant-plant relationships. Journal of Hymenoptera Research 2, 1383.Google Scholar
Del-Claro, K, Berto, V and Reu, W (1996) Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae). Journal of Tropical Ecology 12, 887892.CrossRefGoogle Scholar
Del-Claro, K, Rico-Gray, V, Torezan-Silingardi, HM, Alves-Silva, E, Fagundes, R, Lange, D et al. (2016) Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies. Insectes Sociaux 63, 207221.CrossRefGoogle Scholar
Delph, LF (1999) Sexual Dimorphism in Life History. In: Gender and Sexual Dimorphism in Flowering Plants (eds. Geber, MA, Dawson, TE & Delph, LF). Springer Berlin Heidelberg Berlin, Heidelberg, pp. 149173.CrossRefGoogle Scholar
Dziedzic, K, Szopa, A, Waligórski, P, Ekiert, H and Ślesak, HJABCSB (2020) Sex-related differences in the dioecious species Rumex thyrsiflorus Fingerh: analysis of the content of phenolic constituents in leaf extracts. 62.Google Scholar
Eckhart, VM and Seger, J (1999) Phenological and developmental costs of male function in hermaphroditic plants. In: Life history evolution in plants (eds. Vuorisalo, T & Mutikainen, P.) Kluwer, pp. 195213.CrossRefGoogle Scholar
Edwards, DP, Frederickson, ME, Shepard, GH and Yu, DW (2009) A Plant Needs Ants like a Dog Needs Fleas: Myrmelachista schumanni Ants Gall Many Tree Species to Create Housing. The American Naturalist 174, 734740.CrossRefGoogle Scholar
Edwards, DP, Hassall, M, Sutherland, WJ and Yu, DW (2006) Selection for protection in an ant–plant mutualism: host sanctions, host modularity, and the principal–agent game. Proceedings of the Royal Society B 273, 595602.CrossRefGoogle Scholar
Fagundes, R, Dáttilo, W, Ribeiro, SP, Rico-Gray, V, Jordano, P and Del-Claro, K (2017) Differences among ant species in plant protection are related to production of extrafloral nectar and degree of leaf herbivory. Biological Journal of the Linnean Society 122, 7183.CrossRefGoogle Scholar
Fiala, B and Maschwitz, U (1992) Domatia as most important adaptations in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Systematics and Evolution 180, 5364.CrossRefGoogle Scholar
Fisher, BL, Cover, SP, Kirsch, G, Kane, J and Nobile, A (2007) Ants of North America. A Guide to the Genera. 1 edn. University of California Press.CrossRefGoogle Scholar
Frederickson, ME, Ravenscraft, A, Arcila Hernández, LM, Booth, G, Astudillo, V and Miller, GA (2013) What happens when ants fail at plant defence? Cordia nodosa dynamically adjusts its investment in both direct and indirect resistance traits in response to herbivore damage. Journal of Ecology 101, 400409.CrossRefGoogle Scholar
González Soriano, E, Dirzo, R and Vogt, RC (1997) Historia natural de los Tuxtlas. Universidad Nacional Autónoma de México, Instituto de Ecología, México.Google Scholar
Hartig, F (2018) DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models.Google Scholar
Heil, M (2008) Indirect defence via tritrophic interactions. New Phytologist 178, 4161.CrossRefGoogle ScholarPubMed
Herms, DA and Mattson, WJ (1991) Does reproduction compromise defense in woody plants? In: Forest insect guilds: patterns of interaction with host trees (eds. Baranchikov, YN, Matison, WJ, Hain, FP & Payne, TL). U.S. Dep. Agric. For. Serv. Gen.Google Scholar
Ibarra-Manríquez, G, Martínez-Ramos, M, Dirzo, R and Nunez-Farfan, J (1997) La vegetación. In: Historia Natural de Los Tuxtlas (ed. Gonzalez-Soriano, E., Dirzo, R., Vogt, R.C.). Universidad Nacional Autónoma de México Mexico, pp. 6185.Google Scholar
Iszkuło, G, Kosiński, P and Hajnos, M (2013) Sex influences the taxanes content in Taxus baccata. Acta Physiologiae Plantarum 35, 147152.CrossRefGoogle Scholar
Janczur, MK, González-Camarena, E, León-Solano, HJ, Sandoval-Molina, MA and Jenner, B (2021) Impact of the female and hermaphrodite forms of Opuntia robusta on the plant defence hypothesis. Scientific Reports 11, 12063.CrossRefGoogle ScholarPubMed
Kassambara, A (2019) ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.2.3.Google Scholar
Katabuchi, M (2015) LeafArea: an R package for rapid digital image analysis of leaf area. Ecological Research 30, 10731077.CrossRefGoogle Scholar
Kokolo, B, Attéké Nkoulémbéné, C, Ibrahim, B, M’Batchi, B and Blatrix, R (2020) Phenotypic plasticity in size of ant-domatia. Scientific Reports 10, 20948.CrossRefGoogle ScholarPubMed
Lenth, RV (2019) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.3.01. 2016, 69, 33.Google Scholar
Lloyd, DG and Webb, CJ (1977) Secondary sex characters in plants. The Botanical Review 43, 177216.CrossRefGoogle Scholar
Longino, JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491, 163.CrossRefGoogle Scholar
Longino, JT (2009) Additions to the taxonomy of new world Pheidole (Hymenoptera: Formicidae). Zootaxa 2181, 190.CrossRefGoogle Scholar
Machado, BB, Orue, JPM, Arruda, MS, Santos, CV, Sarath, DS, Goncalves, WN et al. (2016) BioLeaf: A professional mobile application to measure foliar damage caused by insect herbivory. Computers and Electronics in Agriculture 129, 4455.CrossRefGoogle Scholar
Mackay, WP and Mackay, EE (1989) Clave de los géneros de hormigas en México (Hymenoptera: Formicidae). In: Memorias del II Simposio Nacional de Insectos Sociales. Memorial. Oaxtepec. Morelos, pp. 1–82.Google Scholar
Mayer, VE, Frederickson, ME, McKey, D and Blatrix, R (2014) Current issues in the evolutionary ecology of ant–plant symbioses. New Phytologist 202, 749764.CrossRefGoogle ScholarPubMed
McKey, D (1979) The distribution of secondary compounds within plants. In: Herbivores: their interaction with secondary plant metabolites (eds. Rosenthal, GA & Janzen, DH). Academic Press, New York, pp. 55133.Google Scholar
Miller, TEX (2007) Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116, 500512.CrossRefGoogle Scholar
Mithöfer, A and Boland, W (2012) Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology 63, 431450.CrossRefGoogle ScholarPubMed
Monro, AK (2009a) Two new species and a nomenclatural synopsis of Myriocarpa (Urticaceae) from Mesoamerica. Novon: A Journal for Botanical Nomenclature 19, 8595.CrossRefGoogle Scholar
Monro, AK (2009b) Urticaceae. Flora Mesoamericana 1, 192.Google Scholar
Nicotra, AB, Chazdon, RL and Montgomery, RA (2003) Sexes show contrasting patterns of leaf and crown carbon gain in a dioecious rainforest shrub. American Journal of Botany 90, 347355.CrossRefGoogle Scholar
Niño, J, Correa, YM, Cardona, GD and Mosquera, OM (2011) Antioxidant and antitopoisomerase activities in plant extracts of some Colombian flora from La Marcada Natural Regional Park. Revista de Biología Tropical 59, 10891097.Google ScholarPubMed
Nishida, S, Naiki, A and Nishida, T (2005) Morphological variation in leaf domatia enables coexistence of antagonistic mites in Cinnamomum camphora . Canadian Journal of Botany 83, 93101.CrossRefGoogle Scholar
Oliveira, PS and Freitas, AV (2004) Ant-plant-herbivore interactions in the neotropical cerrado savanna. Naturwissenschaften 91, 557570.CrossRefGoogle ScholarPubMed
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.Google Scholar
Rhoades, DF (1979) Evolution of plant chemical defense against herbivores. In: Herbivores: their interaction with secondary plant metabolites (eds. Rosenthal, GA & Janzen, DH). Academic Press, New York, pp. 354.Google Scholar
Rico-Gray, V and Thien, LB (1989) Effect of different ant species on reproductive fitness of Schomburgkia tibicinis (Orchidaceae). Oecologia 81, 487489.CrossRefGoogle Scholar
RStudioTeam (2020) RStudio: Integrated Development Environment for R. RStudio, PBC, Boston, MA.Google Scholar
Rzedowski, J (1986) Vegetación de México. Editorial Limusa, México.Google Scholar
Sandoval-Molina, MA (2018) Interacción entre hormigas, insectos herbívoros y nectarios extraflorales en Opuntia robusta: una prueba de la función defensiva. M.Sc. Thesis, Instituto de Ecología, A.C., Xalapa, MexicoGoogle Scholar
Steinmann, VW (2005) Flora del Bajío y de regiones adyacentes. Fascículo 134. Familia Urticaceae. Instituto de Ecología A. C. Centro Regional del Bajío Pátzcuaro, Michoacán, México. 74 pp.Google Scholar
WFO (2020) Myriocarpa longipes Liebm. Available at: http://www.worldfloraonline.org/taxon/wfo-0000451784. Last accessed 05 Jun 2020.Google Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.CrossRefGoogle Scholar
Young, TP, Stanton, ML and Christian, CE (2003) Effects of natural and simulated herbivory on spine lengths of Acacia drepanolobium in Kenya. Oikos 101, 171179.CrossRefGoogle Scholar
Supplementary material: File

Sandoval-Molina et al. supplementary material

Figures S1-S3

Download Sandoval-Molina et al. supplementary material(File)
File 1 MB
Supplementary material: Link

Sandoval-Molina et al. Dataset

Link