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Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics

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Abstract

Social groups are at particular risk for parasite infection, which is heightened in eusocial insects by the low genetic diversity of individuals within a colony. To combat this, adult ants have evolved a suite of defenses to protect each other, including the production of antimicrobial secretions. However, it is the brood in a colony that are most vulnerable to parasites because their individual defenses are limited, and the nest material in which ants live is also likely to be prone to colonization by potential parasites. Here, we investigate in two ant species whether adult workers use their antimicrobial secretions not only to protect each other but also to sanitize the vulnerable brood and nest material. We find that, in both leaf-cutting ants and weaver ants, the survival of the brood was reduced and the sporulation of parasitic fungi from them increased, when the workers nursing them lacked functional antimicrobial-producing glands. This was the case for both larvae that were experimentally treated with a fungal parasite (Metarhizium) and control larvae which developed infections of an opportunistic fungal parasite (Aspergillus). Similarly, fungi were more likely to grow on the nest material of both ant species if the glands of attending workers were blocked. The results show that the defense of brood and sanitization of nest material are important functions of the antimicrobial secretions of adult ants and that ubiquitous, opportunistic fungi may be a more important driver of the evolution of these defenses than rarer, specialist parasites.

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Acknowledgments

We thank P. Chappell, C. Frost, R. Mitchell, and J. Parkinson for the technical assistance, V. Norman and two anonymous reviewers for their constructive comments which improved the manuscript, IBAMA for the permission to collect and export the leaf-cutting ant colonies, Martin Sebesta for providing the weaver ant colonies, and the Royal Society, BBSRC, and Leverhulme Foundation for the funding.

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Authors and Affiliations

  1. School of Life Sciences, University of Sussex, Brighton, BN1 9QG, UK

    C. Tranter, P. Graystock & W. O. H. Hughes

  2. School of Biology, University of Leeds, Leeds, LS2 9JT, UK

    C. Shaw

  3. Pós-Graduação Comportamento e Biologia Animal, Instituto de Ciências Biológicas, Campus Universitário de Martelos, 36.036-330, Juiz de Fora, MG, Brazil

    J. F. S. Lopes

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  1. C. Tranter
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  2. P. Graystock
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Correspondence to C. Tranter.

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Communicated by D. Naug

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Fig. S1

Details of treatment structure and subject assignment for Experiment 1. 120 leaf-cutting ants (a) were used in total, split between two equal cohorts. Each of the cohorts consisted of 20 ants from each of the three colonies, giving a total of 60 ants for each cohort. Within each cohort, ants from individual colonies were divided evenly into four treatment groups, consisting of five ants. This gave a total of 30 replicate ants per treatment across all colonies and cohorts. 160 weaver ants (b) were used in total, split between two equal cohorts. Each of the cohorts consisted of 40 ants from each of the two colonies, giving a total of 80 ants for each cohort. Within each cohort, ants from individual colonies were split evenly into four treatment groups, consisting of 10 ants. This gave a total of 40 replicate ants per treatment across all colonies and cohorts. (JPEG 186 kb)

High resolution image (TIFF 10989 kb)

Fig. S2

Details of treatment structure and subject assignment for Experiment 2. 120 leaf-cutting ants (a) were used in total, consisting of 40 ants from each of the three colonies. Ants from individual colonies were divided evenly into four treatment groups, consisting of 10 ants. This gave a total of 30 replicate ants per treatment across all colonies. Fifteen additional blank trials were conducted in the absence of any ant. 60 weaver ants (b) were used in total, consisting of 30 ants from each of the two colonies. Ants from individual colonies were divided evenly into two treatment groups, consisting of 15 ants each. This gave a total of 30 replicate ants per treatment across all colonies. Fifteen additional blank trials were conducted in the absence of any ant. (JPEG 140 kb)

High resolution image (TIFF 10372 kb)

Fig. S3

Results of experiment comparing brood-care behaviour and survival of nurse ants with blocked and unblocked glands. Both leaf-cutting ants (a; Wald = 5.6, d.f. = 1, p = 0.45) and weaver ants (b; Wald = 2.1, d.f. = 1, p = 0.15) showed no difference in survival of nurses with (open circles) or without (black circles) functional antimicrobial glands, whilst caring for brood treated with either Metarhizium parasite (solid lines) or control solution (dashed lines), over the course of the experiment. Additionally neither leaf-cutting ants (c) or weaver ants (d) showed any differences in the duration of time spent interacting with brood (U = 39, d.f. = 9, z = 0.84, p = 0.4, and U = 41.5, d.f. = 9, z = 0.64, p = 0.52, respectively), the incidences of contact with brood (U = 46, d.f. = 9, z = 0.36, p = 0.72, and U = 43, d.f. = 9, z = 0.54, p = 0.59, respectively), or incidences of brood-grooming (U = 49.5, d.f. = 9, z = 0.54, p = 0.96, and U = 46.5, d.f. = 9, z = 0.27, p = 0.79, respectively), between nurse ants with blocked (dark bars) and unblocked glands (light bars). (PNG 274 kb)

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Tranter, C., Graystock, P., Shaw, C. et al. Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics. Behav Ecol Sociobiol 68, 499–507 (2014). https://doi.org/10.1007/s00265-013-1664-9

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