Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T14:39:11.225Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrating host plant phylogeny, plant traits, intraspecific competition and repeated measures using a phylogenetic mixed model of field behaviour by polyphagous herbivores, the leaf-cutting ants

Published online by Cambridge University Press:  17 February 2020

Manasee Weerathunga  and
Alexander S. Mikheyev Open the ORCID record for Alexander S. Mikheyev [Opens in a new window]
Manasee Weerathunga
Affiliation:
Ecology and Evolution Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Tancha, Okinawa, Japan
Alexander S. Mikheyev*
Affiliation:
Ecology and Evolution Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Tancha, Okinawa, Japan Evolutionary Genomics Research Group, Australian National University, Canberra, Australian Capital Territory, Australia
*
Author for correspondence: *Alexander S. Mikheyev, Email: alexander.mikheyev@anu.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Herbivores use a wide range of factors to choose their host, including their own physiological states, physical characteristics of plants and the degree of competition. Field observations of herbivores in their native habitats provide a means for simultaneously estimating the relative importance of these factors, but statistical analysis of all these factors may be challenging. Here we used a 7-week dataset of leaf-cutting ant (Atta cephalotes) foraging in a diverse Neotropical arboretum containing 193 tree species (822 trees) to examine the relative role of tree phylogeny, territoriality and tree functional characteristics using a phylogenetic generalized least squares (PGLS) model. We observed that 54 tree species (117 trees) were foraged by the ants. This pattern was not random, but reflected known features of leaf-cutting ant foraging behaviour, such as a preference for larger trees and the decreased likelihood of foraging at the periphery of a colony’s territory. However, random effects such as tree phylogeny, the identity of individual trees and colony-specific effects explained most of the variation in foraging data. A significant phylogenetic effect on foraging likelihood (λ = 0.28), together with repeated measures of foraging on the same tree species, allowed estimation of relative palatability for each plant species. PGLS models can be flexibly scaled to include other covariates for even more complex investigation of foraging behaviour, and the link function can be modified to include the amount of plants foraged. As a result, PGLS can be used as a flexible framework for the study of LCA foraging.

Keywords

Foragingleaf-cutting antsneotropicspalatabilityPGLSphylogenetic models
Type
Research Article
Information
Journal of Tropical Ecology , Volume 36 , Issue 2 , March 2020 , pp. 80 - 86
Copyright
© The Author(s) 2020. 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

Barrer, PM and Cherrett, JM (1972) Some factors affecting the site and pattern of leaf-cutting activity in the ant Atta cephalotes L. Journal of Entomology Series A 47, 15–27.Google Scholar
Berish, CW (1986) Leaf-cutting ants (Atta cephalotes) select nitrogen-rich forage. American Midland Naturalist 115, 268–276.CrossRefGoogle Scholar
Blanton, CM and Ewel, JJ (1985) Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology 66, 861–869.CrossRefGoogle Scholar
Bowers, MA and Porter, SD (1981) Effect of foraging distance on water content of substrates harvested by Atta columbica (Guerin). Ecology 62, 273–275.CrossRefGoogle Scholar
Bürkner, PC (2017) brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80, 1–28.CrossRefGoogle Scholar
Carson, WP and Root, RB (2000) Herbivory and plant species coexistence: community regulation by an outbreaking phytophagous insect. Ecological Monographs 70, 73–99.CrossRefGoogle Scholar
Cherrett, JM (1968) The foraging behaviour of Atta cephalotes L. (Hymenoptera, Formicidae). Journal of Animal Ecology 37, 387–403.CrossRefGoogle Scholar
Cherrett, JM (1972) Some factors involved in the selection of vegetable substrate by Atta cephalotes (L.) (Hymenoptera: Formicidae) in tropical rain forest. Journal of Animal Ecology 41, 647–660.CrossRefGoogle Scholar
Cherrett, JM (1986) History of the leaf-cutting ant problem. In Lofgren, CS and Vander Meer, RK (eds), Fire Ants and Leaf-cutting Ants. Boulder, CO: Westview Press, pp. 10–17.Google Scholar
Cherrett, JM and Seaforth, CE (1970) Phytochemical arrestants for the leaf-cutting ants, Atta cephalotes (L.) and Acromyrmex octospinosus (Reich), with some notes on the ants’ response. Bulletin of Entomological Research 59, 615–625.CrossRefGoogle Scholar
Coley, PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53, 209–233.CrossRefGoogle Scholar
Coley, PD and Barone, JA (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27, 305–335.CrossRefGoogle Scholar
Costa, AN, Vasconcelos, HL, Vieira-Neto, EHM and Bruna, EM (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.CrossRefGoogle Scholar
Costa, AN, Vasconcelos, HL and Bruna, EM (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.CrossRefGoogle Scholar
Costa, AN, Vasconcelos, HL, Vieira-Neto, EHM and Bruna, EM (2019) Adaptive foraging of leaf-cutter ants to spatiotemporal changes in resource availability in Neotropical savannas. Ecological Entomology 2, 227–238.CrossRefGoogle Scholar
Covarrubias-Pazaran, G (2016) Genome-assisted prediction of quantitative traits using the R package sommer. PLoS ONE 11, e0156744.CrossRefGoogle Scholar
Farji-Brener, AG (2001) Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis. Oikos 92, 169–177.CrossRefGoogle Scholar
Farji-Brener, AG and Illes, AE (2000) Do leaf-cutting ant nests make ‘bottom-up’ gaps in neotropical rain forests? A critical review of the evidence. Ecology Letters 3, 219–227.CrossRefGoogle Scholar
Farji-Brener, AG, Chinchilla, F, Umaña, MN, Ocasio-Torres, ME, Chauta-Mellizo, A, Acosta-Rojas, D, Marinaro, S, de Torres Curth, M and Amador-Vargas, S (2015) Branching angles reflect a trade-off between reducing trail maintenance costs or travel distances in leaf-cutting ants. Ecology 96, 510–517.CrossRefGoogle ScholarPubMed
Freckleton, RP, Harvey, PH and Pagel, M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160, 712–726.CrossRefGoogle Scholar
Fowler, HG (1983) Distribution patterns of Paraguayan leaf-cutting ants (Atta and Acromyrmex) (Formicidae: Attini). Studies on Neotropical Fauna and Environment 18, 121–138.CrossRefGoogle Scholar
Gerhold, P, Ribeiro, EMS, Santos, BA, Sarapuu, J, Tabarelli, M, Wirth, R and Leal, IR (2019) Phylogenetic signal in leaf-cutting ant diet in the fragmented Atlantic rain forest. Journal of Tropical Ecology 35, 144–147.CrossRefGoogle Scholar
Hadfield, JD (2010) MCMC Methods for multi-response generalized linear mixed models: the MCMCglmm R Package. Journal of Statistical Software 33, 1–22.CrossRefGoogle Scholar
Hölldobler, B and Wilson, EO (1990) The Ants. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Hooge, PN and Eichenlaub, B (1997) Animal movement extension to ArcView. Version 1.1. Alaska Biological Science Center. US Geological Survey, Anchorage, Alaska, USA.Google Scholar
Howard, JJ (1987) Leafcutting ant diet selection: the role of nutrients, water, and secondary chemistry. Ecology 68, 503–515.CrossRefGoogle Scholar
Howard, JJ (1990) Infidelity of leafcutting ants to host plants: resource heterogeneity or defense induction? Oecologia 82, 394–401.CrossRefGoogle ScholarPubMed
Janz, N and Nylin, S (1998) Butterflies and plants: a phylogenetic study. Evolution 52, 486–502.CrossRefGoogle ScholarPubMed
Kost, C, de Oliveira, EG, Knoch, TA and Wirth, R (2005) Spatio-temporal permanence and plasticity of foraging trails in young and mature leaf-cutting ant colonies (Atta spp.). Journal of Tropical Ecology 21, 677–688.CrossRefGoogle Scholar
Meyer, ST, Leal, IR and Tabarelli, M (2011) Ecosystem engineering by leaf-cutting ants: nests of Atta cephalotes drastically alter forest structure and microclimate. Ecological Entomology 36, 14–24.CrossRefGoogle Scholar
Mikheyev, AS (2007) History, genetics and pathology of a leaf-cutting ant introduction: a case study of the Guadeloupe invasion. Biological Invasions 10, 467–473.CrossRefGoogle Scholar
Moutinho, P, Nepstad, DC and Davidson, EA (2003) Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia. Ecology 84, 1265–1276.CrossRefGoogle Scholar
Mundim, FM, Costa, AN and Vasconcelos, HL (2009) Leaf nutrient content and host plant selection by leaf-cutter ants, Atta laevigata, in a Neotropical savanna. Entomologia Experimentalis et Applicata 130, 47–54.CrossRefGoogle Scholar
Novotny, V, Basset, Y, Miller, SE, Weiblen, GD, Bremer, B, Cizek, L and Drozd, P (2002) Low host specificity of herbivorous insects in a tropical forest. Nature 416, 841–844.CrossRefGoogle Scholar
Olsson, O, Brown, JS and Helf, KL (2008) A guide to central place effects in foraging. Theoretical Population Biology 74, 22–33.CrossRefGoogle ScholarPubMed
Orme, D, Freckleton, R, Thomas, G and Petzoldt, T (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R package version 5, 1–36.Google Scholar
Poelman, EH and Kessler, A (2016) Keystone herbivores and the evolution of plant defenses. Trends in Plant Science 21, 477–485.CrossRefGoogle ScholarPubMed
Revell, LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.CrossRefGoogle Scholar
Rocha, SL, Evans, HC, Jorge, VL, Cardoso, LAO, Pereira, FST, Rocha, FB, Barreto, RW, Hart, AG and Elliot, SL (2017) Recognition of endophytic Trichoderma species by leaf-cutting ants and their potential in a Trojan-horse management strategy. Royal Society Open Science 4, 160628.CrossRefGoogle Scholar
Rockwood, LL (1976) Plant selection and foraging patterns in two species of leaf-cutting ants (Atta). Ecology 57, 48–61.CrossRefGoogle Scholar
Shepherd, JD (1985) Adjusting foraging effort to resources in adjacent colonies of the leaf-cutter ant, Atta colombica. Biotropica 17, 245–252.CrossRefGoogle Scholar
Silva, PSD, Bieber, AGD, Knoch, TA, Tabarelli, M, Leal, IR and Wirth, R (2013) Foraging in highly dynamic environments: leaf-cutting ants adjust foraging trail networks to pioneer plant availability. Entomologia Experimentalis et Applicata 147, 110–119.CrossRefGoogle Scholar
Smith, JE, Hunter, CL and Smith, CM (2010) The effects of top–down versus bottom–up control on benthic coral reef community structure. Oecologia 163, 497–507.CrossRefGoogle ScholarPubMed
Soper, FM, Sullivan, BW, Osborne, BB, Shaw, AN, Philippot, L and Cleveland, CC (2019) Leaf-cutter ants engineer large nitrous oxide hot spots in tropical forests. Proceedings of the Royal Society B 286, 20182504.CrossRefGoogle ScholarPubMed
Speight, MR, Hunter, MD and Watt, AD (1999) Ecology of Insects: Concepts and Applications. Oxford: Blackwell.Google Scholar
Vasconcelos, HL (1997) Foraging activity of an Amazonian leaf-cutting ant: responses to changes in the availability of woody plants and to previous plant damage. Oecologia 112, 370–378.CrossRefGoogle ScholarPubMed
Vasconcelos, HLD and De Vasconcelos, HL (1990) Habitat selection by the queens of the leaf-cutting ant Atta sexdens L. in Brazil. Journal of Tropical Ecology 6, 249–252.CrossRefGoogle Scholar
Volf, M, Hrcek, J, Julkunen-Tiitto, R and Novotny, V (2015) To each its own: differential response of specialist and generalist herbivores to plant defence in willows. Journal of Animal Ecology 84, 1123–1132.CrossRefGoogle ScholarPubMed
Volf, M, Pyszko, P, Abe, T, Libra, M, Kotásková, N, Šigut, M, Kumar, R, Kaman, O, Butterill, PT, Šipoš, J, Abe, H, Fukushima, H, Drozd, P, Kamata, N, Murakami, M and Novotny, V (2017). Phylogenetic composition of host plant communities drives plant-herbivore food web structure. Journal of Animal Ecology 86, 556–565.CrossRefGoogle ScholarPubMed
Waller, DA (1982) Leaf-cutting ants and avoided plants: defences against Atta texana attack. Oecologica 52, 400–403.CrossRefGoogle ScholarPubMed
Wan, H, Bai, Y, Hooper, DU, Schönbach, P, Gierus, M, Schiborra, A and Taube, F (2015) Selective grazing and seasonal precipitation play key roles in shaping plant community structure of semi-arid grasslands. Landscape Ecology 30, 1767–1782.CrossRefGoogle Scholar
Webb, CO and Donoghue, MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5, 181–183.CrossRefGoogle Scholar
Winkler, IS and Mitter, C (2008) The phylogenetic dimension of insect-plant interactions: a review of recent evidence. In Tilmon, KJ (ed.), Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, CA: University of California Press, California, pp. 240–263.Google Scholar
Wirth, R, Beyschlag, W, Ryel, RJ and Hölldobler, B (1997) Annual foraging of the leaf-cutting ant Atta colombica in a semideciduous rain forest in Panama. Journal of Tropical Ecology 13, 741–757.CrossRefGoogle Scholar
Wirth, R, Herz, H, Ryel, RJ, Beyschlag, W and Hölldobler, B (2003) Herbivory of Leaf Cutting Ants: A Case Study in the Tropical Rainforest of Panama. Cham: Springer.CrossRefGoogle Scholar
Zanne, AE, Tank, DC, Cornwell, WK, Eastman, JM, Smith, SA, FitzJohn, RG, McGlinn, DJ, O’Meara, BC, Moles, AT, Reich, PB, Royer, DL, Soltis, DE, Stevens, PF, Westoby, M, Wright, IJ, Aarssen, L, Bertin, RI, Calaminus, A, Govaerts, R, Hemmings, F, Leishman, MR, Oleksyn, J, Soltis, PS, Swenson, NG, Warman, L and Beaulieu, JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92.CrossRefGoogle ScholarPubMed