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Multiple phenotypic traits as triggers of host attacks towards ant symbionts: body size, morphological gestalt, and chemical mimicry accuracy

von Beeren, Christoph and Brückner, Adrian and Hoenle, Philipp O. and Ospina-Jara, Bryan and Kronauer, Daniel J. C. and Blüthgen, Nico (2021) Multiple phenotypic traits as triggers of host attacks towards ant symbionts: body size, morphological gestalt, and chemical mimicry accuracy. Frontiers in Zoology, 18 . Art. No. 46. ISSN 1742-9994. PMCID PMC8451089. doi:10.1186/s12983-021-00427-8. https://resolver.caltech.edu/CaltechAUTHORS:20211014-170600011

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Abstract

Background. Ant colonies are plagued by a diversity of arthropod guests, which adopt various strategies to avoid or to withstand host attacks. Chemical mimicry of host recognition cues is, for example, a common integration strategy of ant guests. The morphological gestalt and body size of ant guests have long been argued to also affect host hostility, but quantitative studies testing these predictions are largely missing. We here evaluated three guest traits as triggers of host aggression—body size, morphological gestalt, and accuracy in chemical mimicry—in a community of six Eciton army ant species and 29 guest species. We quantified ant aggression towards 314 guests in behavioral assays and, for the same individuals, determined their body size and their accuracy in mimicking ant cuticular hydrocarbon (CHC) profiles. We classified guests into the following gestalts: protective, myrmecoid, staphylinid-like, phorid-like, and larval-shaped. We expected that (1) guests with lower CHC mimicry accuracy are more frequently attacked; (2) larger guests are more frequently attacked; (3) guests of different morphological gestalt receive differing host aggression levels. Results. Army ant species had distinct CHC profiles and accuracy of mimicking these profiles was variable among guests, with many species showing high mimicry accuracy. Unexpectedly, we did not find a clear relationship between chemical host similarity and host aggression, suggesting that other symbiont traits need to be considered. We detected a relationship between the guests’ body size and the received host aggression, in that diminutive forms were rarely attacked. Our data also indicated that morphological gestalt might be a valuable predictor of host aggression. While most ant-guest encounters remained peaceful, host behavior still differed towards guests in that ant aggression was primarily directed towards those guests possessing a protective or a staphylinid-like gestalt. Conclusion. We demonstrate that CHC mimicry accuracy does not necessarily predict host aggression towards ant symbionts. Exploitation mechanisms are diverse, and we conclude that, besides chemical mimicry, other factors such as the guests’ morphological gestalt and especially their body size might be important, yet underrated traits shaping the level of host hostility against social insect symbionts.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1186/s12983-021-00427-8DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8451089/PubMed CentralArticle
ORCID:
AuthorORCID
von Beeren, Christoph0000-0002-0072-5795
Brückner, Adrian0000-0002-9184-8562
Hoenle, Philipp O.0000-0001-8160-8859
Ospina-Jara, Bryan0000-0003-2668-1177
Kronauer, Daniel J. C.0000-0002-4103-7729
Blüthgen, Nico0000-0001-6349-4528
Additional Information:© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Received 07 May 2021. Accepted 19 August 2021. Published 19 September 2021. We thank two anonymous reviewers for their valuable input, the Ecological network group at the TU Darmstadt for valuable discussions, Sebastian Pohl for helpful comments on an earlier draft of the manuscript, Sebastian Schmelzle for help with SRµCT scans (Additional file 3), Jana Wieschollek and Ana Ailín Paul for help with dry weight measurements, as well as Adrián Pinto Tomás, Carlos de la Rosa, Bernal Matarrita Carranza and Danilo Brenes Madrigal, and the entire staff of La Selva Biological Station for their generous support throughout the project. CvB was supported by the German Science Foundation (BE 5177/4–1 & BE 5177/4–2). DJCK was supported by a Carl & Marian Rettenmeyer Ant-Guest Endowment Award. AB & POH were supported by the German National Academic Foundation (Studienstiftung des deutschen Volkes). Contributions. CvB designed and supervised the study. CvB, AB, POH, BOJ, and DJCK carried out the field work. CvB wrote the initial draft of the manuscript, and all authors reviewed the manuscript. CvB and AB carried out chemical analyses. CvB, POH, and BOJ carried out behavioral assays. CvB, AB, and NB carried out statistical analyses. All authors read and approved the final manuscript. Availability of data and materials. The datasets supporting the conclusions of this article are included within the article and its additional files. Ethics approval and consent to participate. The present study complies with institutional, national, and international ethical guidelines. Research and specimen export permits for Costa Rica were issued by the ‘Ministry of the Environment, Energy and Technology’ (MINAET; permit numbers: 192-2012-SINAC and R-009-2014-OT-CONAGEBIO). The authors declare that they have no competing interests.
Funders:
Funding AgencyGrant Number
Deutsche Forschungsgemeinschaft (DFG)BE 5177/4-1
Deutsche Forschungsgemeinschaft (DFG)BE 5177/4–2
Carl & Marian Rettenmeyer Ant-Guest EndowmentUNSPECIFIED
Studienstiftung des Deutschen VolkesUNSPECIFIED
PubMed Central ID:PMC8451089
DOI:10.1186/s12983-021-00427-8
Record Number:CaltechAUTHORS:20211014-170600011
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211014-170600011
Official Citation:von Beeren, C., Brückner, A., Hoenle, P.O. et al. Multiple phenotypic traits as triggers of host attacks towards ant symbionts: body size, morphological gestalt, and chemical mimicry accuracy. Front Zool 18, 46 (2021). https://doi.org/10.1186/s12983-021-00427-8
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:111440
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:14 Oct 2021 18:03
Last Modified:14 Oct 2021 18:03

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