Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants

Abstract

The paired exocrine metapleural glands present in the large majority of ant species produce compounds with antibiotic properties. In the leaf-cutting ant, Acromyrmex octospinosus, the secretion consists of more than 20 different compounds and it has generally been assumed that the glands serve as a general defence against various infectious microbes of fungal and bacterial origin. We present results illuminating the direct costs and benefits of these metapleural gland defences in A. octospinosus. We show that major workers of this leaf-cutting ant experience a significant reduction in their respiration rate when the metapleural glands are experimentally closed, indicating that metapleural gland secretion incurs a substantial cost and that the production of compounds from these glands is terminated when the ants are incapable of secreting them. In another set of experiments, we show that the ability to secrete antibiotic compounds from the metapleural glands is of significant importance when ants are exposed to a general but potentially virulent insect pathogen, Metarhizium anisopliae. Infection with this fungus is lethal within a few days when ants have their metapleural glands experimentally closed, but relatively harmless when the metapleural glands are functional. These findings support experimentally the view that the metapleural glands play an important hygienic role in leaf-cutting ants.

Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants

“…It is a defence system unique for and shared by all ants, except for a few isolated cases in which the gland was secondary lost (Hölldobler and Engel-Siegel, 1984). The results obtained by Ortius-Lechner et al (2000), Poulsen et al (2002b) and in the present study clearly show that the metapleural gland defence in Acromyrmex leaf-cutting ants is both elaborate and effective.…”

“…These metapleural glands produce secretions that flow out over the body surface where they exert anti-bacterial (Maschwitz et al, 1970;Veal et al, 1992) and anti-fungal (Beattie et al, 1985(Beattie et al, , 1986Maschwitz et al, 1970;Nascimento et al, 1996;Schildknecht and Koob, 1971;Poulsen et al, 2002 b) properties and from where they possibly spread to other individuals in the nest or to the nest environment (Maschwitz et al, 1970). Metapleural gland secretions are therefore considered to be important for keeping ant colonies free from infections with harmful micro-organisms Wilson, 1990, Maschwitz et al, 1970;Poulsen et al, 2002b).…”

Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection

“…The first is that all male ants lack metapleural glands (Höll-dobler and Wilson, 1990). These glands are known to be important in disease defence (Bot et al, 2002;Hughes et al, 2002;Poulsen et al, 2002a), and are large and costly (Poulsen et al, 2002a). Male ants have thus eliminated investment in this costly disease defence mechanism, presumably because disease resistance is less important to them than traits that increase the number of matings they obtain.…”

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

“…The manner in which parasite density acts is likely to itself vary between different resistance mechanisms. In leaf-cutting ants, resistance mechanisms include self-grooming, the production of antibiotic secretion, and both humoral and cellular components of the immune system (Kermarrec et al 1986;Gillespie et al 1999; Hughes et al 2002;Poulsen et al 2002a;Sumner et al 2003).…”

“…anisopliae as the model parasite. Metarhizium is a virulent generalist parasite of many insect species, including both Atta and Acromyrmex leaf-cutting ants (Alves and Sosa Gómez 1983;Humber 1992;Jaccoud et al 1999;Hughes et al 2002;Poulsen et al 2002a;. It is semelparous and produces transmission stages (spores) only after host death.…”