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Trophic Ecology of the Armadillo Ant, Tatuidris Tatusia

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Trophic Ecology of the Armadillo Ant, Tatuidris Tatusia Trophic Ecology of the Armadillo Ant, Tatuidris tatusia, Assessed by Stable Isotopes and Behavioral Observations Author(s): Justine Jacquemin, Thibaut Delsinne, Mark Maraun, Maurice Leponce Source: Journal of Insect Science, 14(108):1-12. 2014. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1673/031.014.108 URL: http://www.bioone.org/doi/full/10.1673/031.014.108 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Insect Science: Vol. 14 | Article 108 Jacquemin et al. Trophic ecology of the armadillo ant, Tatuidris tatusia, assessed by stable isotopes and behavioral observations Justine Jacquemin1,2a*, Thibaut Delsinne1b, Mark Maraun3c, Maurice Leponce1d 1Biodiversity Monitoring and Assessment, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium 2Evolutionary Biology & Ecology, Université Libre de Bruxelles, Belgium 3J.F. Blumenbach Institute of Zoology and Anthropology, Animal Ecology, Georg August University of Göttingen, Germany Abstract Ants of the genus Tatuidris Brown and Kempf (Formicidae: Agroecomyrmecinae) generally oc- cur at low abundances in forests of Central and South America. Their morphological peculiarities, such as mandibular brushes, are presumably linked with specialized predatory hab- its. Our aims were to (1) assess the Tatuidris abundance in an evergreen premontane forest of Ecuador; (2) detail morphological characteristics and feeding behavior of Tatuidris; and (3) de- fine the position of Tatuidris in the food web. A total of 465 litter samples were collected. For the first time, live Tatuidris individuals were observed. Various potential food sources were offered to them. A nitrogen stable isotope ratio analysis (15N/14N) was conducted on Tatuidris tatusia, other ants, and common organisms from the leaf-litter mesofauna. We found a relatively high abundance of T. tatusia in the site. Live individuals did not feed on any of the food sources of- fered, as usually observed with diet specialist ants. The isotope analysis revealed that T. tatusia is one of the top predators of the leaf-litter food web. Keywords: food web, Formicidae, Hymenoptera, predation, trophic biology Correspondence: a [email protected], b [email protected], c [email protected], d [email protected], *Corresponding author Editor: Jurgen Ziesmann was editor of this paper. Received: 3 September 2012 Accepted: 6 February 2013 Published: 12 August 2014 Copyright: This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, pro- vided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 14, Number 108 Cite this paper as: Jacquemin J, Delsinne T, Maraun M, Leponce M. 2014. Trophic ecology of the armadillo ant, Tatuidris tatusia, assessed by stable isotopes and behavioral observations. Journal of Insect Science 14(108). Available online: http://www.insectscience.org/14.108 Journal of Insect Science | http://www.insectscience.org 1 Journal of Insect Science: Vol. 14 | Article 108 Jacquemin et al. Introduction variability of the isotopic signature (Tillberg and Breed 2004). Ants of the genus Tatuidris Brown and Kempf (Formicidae: Agroecomyrmecinae) are rare Stable isotopes have already been successfully inhabitants of soil and leaf-litter layers of Ne- used for assessing the trophic ecology of ants otropical forests from Mexico to French (Blüthgen et al. 2003; Feldhaar et al. 2009), Guiana, central Brazil, and Peru (Donoso their degree of omnivory (Tillberg and Breed 2012; Lacau et al. 2012). In his recent revision 2004; Jacquemin et al. 2012), and the change of the genus, Donoso (2012) considers the ge- in their dietary habits across habitats (Gibb nus Tatuidris as monotypic, and he and Cunningham 2011) or between their na- synonymized the recently described T. kapasi tive and introduced ranges (Tillberg et al. Lacau and Groc, 2012, from French Guiana, 2007). Stable isotopes also provided infor- under T. tatusia (first described by Brown and mation on the position of ants in food webs, Kempf, 1968). relative to other ants and other taxa (Tillberg et al. 2006; Hyodo et al. 2010; Jacquemin et T. tatusia possesses a series of morphological al. 2012). peculiarities, such as modified mandibles, In the current study, our aims were to (1) as- suggesting that Tatuidris are specialist preda- sess Tatuidris species abundance in an tors (Brown and Kempf 1968). Nevertheless, evergreen premontane forest of Ecuador; (2) their feeding habits and trophic position re- detail its morphological characteristics, behav- main unknown. It is very difficult to find and ior, and dietary habits through a feeding observe these ants, but techniques such as experiment on a live colony; and (3) define its DNA analysis of gut content or stable isotope position in the food web using an isotopic ap- analysis may help to study the diet of these proach. cryptic organisms. Nitrogen stable isotope analysis is of particular value for such an Materials and Methods analysis because it makes it possible to define the trophic position of an organism in a food Study site web and that organism’s degree of omnivory. The study was conducted in an evergreen premontane forest located in Copalinga Pri- The measurement of the heavy to light isotope vate Reserve (4.0912° S, 78.9607° W), on the ratio (15N/14N) in an animal’s tissue provides eastern slope of the Ecuadorian Andes, 1000 information on its diet and trophic position m above sea level. High precipitation occurs (DeNiro and Epstein 1981; Minagawa and from February to June, while from August to Wada 1984). Indeed, the N isotopic signature December it is drier (average annual rainfall: of a consumer is typically enriched by ≈3.4‰ 2000 mm ± 387 SD; average annual tempera- relative to its diet (Post 2002; Maraun et al. ture: 22.3°C ± 0.9 SD; C. Vits, Copalinga 2011). Hence, the higher the position of an private reserve, personal communication, pe- animal in the trophic chain, the higher the riod: 2003–2011). Soil is sandy clay loam abundance of nitrogen stable isotope in its tis- (proportion of sand, silt and clay is 43%, 20%, sue. Primary consumers have low signatures, and 37%, respectively) with mean pH = 3.6 (± and top predators the highest ones. The degree 0.2 SD, n = 100 soil samples). of omnivory is reflected by the intraspecific Journal of Insect Science | http://www.insectscience.org 2 Journal of Insect Science: Vol. 14 | Article 108 Jacquemin et al. Species abundance high gradient extractor (Macfadyen 1961) for The calculation of species abundance was four days. Ants were extracted from 465 sam- based on 220 Winkler extractions performed ples of leaf litter (total extracted area = 176.75 in November 2009 (dry season) and 245 in m²) using mini-Winkler extractors for 48 hr. March 2010 (early rainy season) in Copalinga. Between 1 and 31 ant workers and between 1 Morphology and 121 mesofauna individuals were pooled High-resolution digital photographs of into tin capsules to obtain sufficient amounts Tatuidris tatusia habitus, mandibles, sting, of material. Samples were dried at 60°C for 24 and setae on the protibia are presented, along hr, weighed, and stored in a desiccator until with scanning electron micrographs (SEM) for analysis (n = 2–5 replicates). Samples were mandibles and setae. High-resolution digital analyzed with an elemental analyzer (NA images were taken using a Leica DFC290 1500, Carlo Erba, camera attached to a Leica Z6 APO stereomi- www.carloerbareagents.com) coupled to a croscope (www.leica-microsystems.com). mass spectrometer (Finnigan MAT 251, Series of images were taken by focusing the Thermo Fisher Scientific, sharpness on different levels of the structure www.thermoscientific.com). The abundance using the Leica Application Suite v38 (2003– of heavy stable isotopes (δ15N) was calculated 2011), and combined with the “Align and bal- as follows: ance used frame (quick)” and “Do stack” 15 commands of CombineZP (Hadley 2010). Fi- δ N (‰) = (Rsample - Rstandard)/Rstandard x 1000 nal editing of images was done in Adobe 15 14 Photoshop CS5 (www.adobe.com). SEM pho- Rsample and Rstandard represent the N/ N ratios tographs of gold-coated specimens were taken corresponding to the samples and standard using an FEI Quanta 200 (www.fei.com) (atmospheric nitrogen), respectively. Acetani- scanning electron microscope. lide (C8H9NO, Merck, www.merckgroup.com) was used for internal Voucher specimens of Tatuidris tatusia were calibration. deposited at the Royal Belgian Institute of Natural Sciences, Brussels, Belgium (RBINS). Limits between the different
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