Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-27T11:06:41.063Z Has data issue: false hasContentIssue false

Scaling of indirect defences in Central American swollen-thorn acacias

Published online by Cambridge University Press:  13 July 2022

Sabrina Amador-Vargas*
Affiliation:
Smithsonian Tropical Research Institute, Panamá, Republic of Panamá
Yorlenis González
Affiliation:
Smithsonian Tropical Research Institute, Panamá, Republic of Panamá
Maikol Guevara
Affiliation:
Smithsonian Tropical Research Institute, Panamá & Universidad de Panamá, Panamá, Republic of Panamá
Finote Gijsman
Affiliation:
Smithsonian Tropical Research Institute, Panamá & Princeton University, USA
*
Author for correspondence: Sabrina Amador-Vargas, Email: [email protected]

Abstract

Myrmecophytes may adjust the investment on ant rewards, depending on tree size and ant defence level. In swollen-thorn acacias (Vachellia collinsii), we tested whether the level of protection provided by the resident ants (defending vs. non-defending) influenced the relation between tree size and ant rewards, or between types of ant rewards (housing and food). We quantified ant rewards in trees occupied by defending and by non-defending ants. We predicted: (1) a positive relation between plant diameter and ant reward investment, with a steeper slope for defending than for non-defending ant species; and (2) that if there is any tradeoff between ant rewards, it should be aggravated (steeper slope) when inhabited by non-defending ants. We found that most structures for ants grew according to plant diameter, but contrary to our first prediction it was independent of the level of ant defence. Most ant rewards did not show a tradeoff between them, besides a weak negative relation between spine length and number of pinnules, which contrary to the prediction occurred when occupied by defending ants. The evidence shows that the interacting ants had a weaker influence on the scaling of defence structures in myrmecophytes than the habitat (location).

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

Aljbory, Z and Chen, M-S (2018) Indirect plant defense against insect herbivores: a review. Insect Science 25, 223.CrossRefGoogle ScholarPubMed
Amador-Vargas, S (2019) Plant killing by Neotropical acacia ants: ecology, decision-making, and head morphology. Biotropica 51, 692699.CrossRefGoogle Scholar
Amador-Vargas, S, Dyer, J, Arnold, N, Cavanaugh, L and Sánchez-Brenes, E (2020) Acacia trees with parasitic ants have fewer and less spacious spines than trees with mutualistic ants. The Science of Nature 107, 3.CrossRefGoogle Scholar
Amador-Vargas, S, Orribarra, VS, Portugal-Loayza, A and Fernández-Marín, H (2021) Association patterns of swollen-thorn acacias with three ant species and other organisms in a dry forest of Panama. Biotropica 53, 560566.CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Blatrix, R, Renard, D, Djieto-Lordon, C and McKey, D (2012) The cost of myrmecophytism: insights from allometry of stem secondary growth. Annals of Botany 110, 943951.CrossRefGoogle ScholarPubMed
Brouat, C and McKey, D (2001) Leaf-stem allometry, hollow stems, and the evolution of caulinary domatia in myrmecophytes. The New Phytologist 151, 391406.CrossRefGoogle Scholar
Chanam, J, Sheshshayee, MS, Kasinathan, S, Jagdeesh, A, Joshi, KA and Borges, RM (2014) Nutritional benefits from domatia inhabitants in an ant–plant interaction: interlopers do pay the rent. Functional Ecology 28, 11071116.CrossRefGoogle Scholar
Coley, PD, Bryant, JP and Chapin, FS (1985) Resource availability and plant antiherbivore defense. Science (New York, N.Y.) 230, 895899.CrossRefGoogle ScholarPubMed
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
Frederickson, ME, Greene, MJ and Gordon, DM (2005) “Devil’s gardens” bedevilled by ants. Nature 437, 495496.CrossRefGoogle ScholarPubMed
Gijsman, F, Guevara, M, González, Y and Amador-Vargas, S (2021) Short-term plasticity and variation in acacia ant-rewards under different conditions of ant occupancy and herbivory. The Science of Nature 108, 112.CrossRefGoogle ScholarPubMed
González-Teuber, M and Heil, M (2015) Comparative anatomy and physiology of myrmecophytes: ecological and evolutionary perspectives. Research and Reports in Biodiversity Studies 2015, 2132.CrossRefGoogle Scholar
González-Teuber, M, Silva Bueno, JC, Heil, M and Boland, W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PloS One 7, e46598.CrossRefGoogle ScholarPubMed
Heil, M, Delsinne, T, Hilpert, A, Schürkens, S, Andary, C, Linsenmair, KE, Sousa, SM and McKey, D (2002) Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis. Oikos 99, 457468.CrossRefGoogle Scholar
Heil, M, Fiala, B, Linsenmair, KE, Zotz, G and Menke, P (1997) Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via symbiotic ant partners. Journal of Ecology 85, 847861.CrossRefGoogle Scholar
Heil, M, González-Teuber, M, Clement, LW, Kautz, S, Verhaagh, M and Bueno, JCS (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proceedings of the National Academy of Sciences 106, 1809118096.CrossRefGoogle ScholarPubMed
Heil, M, Hilpert, A, Fiala, B and Linsenmair, KE (2001) Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 126, 404408.CrossRefGoogle Scholar
Heil, M, Staehelin, C and McKey, D (2000) Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences? Naturwissenschaften, 87, 555558.CrossRefGoogle ScholarPubMed
Herms, DA and Mattson, WJ (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology 67, 283335.CrossRefGoogle Scholar
Janzen, DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249275.CrossRefGoogle ScholarPubMed
Janzen, DH (1974) Swollen-thorn acacias of Central America. Smithsonian Contributions to Botany 13, 1131.CrossRefGoogle Scholar
Koricheva, J and Romero, GQ (2012) You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants. Biology Letters 8, 628630.CrossRefGoogle ScholarPubMed
Leichty, AR and Poethig, RS (2019) Development and evolution of age-dependent defenses in ant-acacias. Proceedings of the National Academy of Sciences 116, 1559615601.CrossRefGoogle ScholarPubMed
Longino, JT (2003) The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica. Zootaxa 151, 1150.CrossRefGoogle Scholar
Markesteijn, L, Poorter, L and Bongers, F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. American Journal of Botany 94, 515525.CrossRefGoogle ScholarPubMed
Ness, JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113, 506514.CrossRefGoogle Scholar
Quintero, C, Barton, KE and Boege, K (2013) The ontogeny of plant indirect defenses. Perspectives in Plant Ecology, Evolution and Systematics 15, 245254.CrossRefGoogle Scholar
Rico-Gray, V and Oliveira, PS (2007) The Ecology and Evolution of Ant-plant Interactions. Chicago, USA: University of Chicago Press.CrossRefGoogle Scholar
Rudgers, JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant–plant mutualism. Ecology 85, 192205.CrossRefGoogle Scholar
Sobrinho, TG, Schoereder, JH, Rodrigues, LL and Collevatti, RG (2002) Ant visitation (Hymenoptera: Formicidae) to extrafloral nectaries increases seed set and seed viability in the tropical weed Triumfetta semitriloba . Sociobiology 39, 353372.Google Scholar
Val, ED and Dirzo, R (2003) Does ontogeny cause changes in the defensive strategies of the myrmecophyte Cecropia peltata? Plant Ecology 169, 3541.CrossRefGoogle Scholar
Warton, DI, Duursma, RA, Falster, DS and Taskinen, S (2012) Smatr 3– an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3, 257259.CrossRefGoogle Scholar
Webber, BL and McKey, D (2009) Cyanogenic myrmecophytes, redundant defence mechanisms and complementary defence syndromes: revisiting the neotropical ant-acacias. New Phytologist 182, 792794.CrossRefGoogle ScholarPubMed
Wolfe, BT and Kursar, TA (2015) Diverse patterns of stored water use among saplings in seasonally dry tropical forests. Oecologia 179, 925936.CrossRefGoogle ScholarPubMed
Young, TP and Okello, BD (1998) Relaxation of an induced defense after exclusion of herbivores: spines on Acacia drepanolobium . Oecologia 115, 508513.CrossRefGoogle ScholarPubMed
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: PDF

Amador-Vargas et al. supplementary material

Amador-Vargas et al. supplementary material

Download Amador-Vargas et al. supplementary material(PDF)
PDF 723.9 KB