The Vulnerability of Pollen and Fungal Spores to Ant Secretions: Evidence and Some Evolutionary Implications

Abstract

The quality of Brassica and Acacia pollen is adversely affected by exposure to secretions drawn from the metapleural gland of the ant Myrmecia nigriscapa. Ultrastructural studies show that the apparently lipoidal secretions destroy both the plasma membranes and those of the cytoplasmic organelles. Exposure to the integument of this ant prevents the normal hydration of pollen grains. Exposure to the integument of a species of Camponotus, which does not appear to possess metapleural gland openings, also reduces pollen quality. Mycelial development in seven species of soil‐dwelling fungi is inhibited by secretions of the metapleural gland. Two fungal species that are normally entomogenous are most vulnerable to the secretion. It is suggested that the metapleural gland is producing a powerful antibiotic and that the antibiosis that results from its activity, on one hand, alleviates the attacks of microorganisms in nest cavities, while on the other, incidentally kills pollen grains, possibly blocking the evolution of ant pollination systems.

Mutualistic bacteria and a possible trade-off between alternative defence mechanisms in Acromyrmex leaf-cutting ants

“…The paired exocrine metapleural glands are located laterally at the rear of the mesosoma (Hölldobler and Engel-Siegel, 1984). The secretions of these glands are known to inhibit the growth of bacteria, fungal mycelia, and the germination of fungal spores (Maschwitz et al, 1970;Beattie et al, 1985;Beattie et al, 1986;Ortius-Lechner et al, 2000;Bot et al, 2001 b). Minor leaf-cutting ant workers have large metapleural glands relative to their body size compared to major workers, indicating that this defence function is most important in ants specialised on fungus garden maintenance (Wilson, 1980;Bot and Boomsma, 1996;Bot et al, 2001b).…”

“…The top of the garden contains a relatively large amount of substrate compared to the biomass of the mutualistic fungus, and is therefore likely to harbour a significantly higher abundance of a variety of non-specialised competing microbes that enter the fungus garden on leaf material incorporated by the ants (Fisher et al, 1996). The metapleural glands are particularly effective as a general defence mechanism against these kinds of microbes (Beattie et al, 1985, Beattie et al, 1986Poulsen et al, in review), which is consistent with our result presented here that the minor workers, with their relatively large metapleural glands (Wilson, 1980;Bot and Boomsma, 1996), are most abundant in the top section of the fungus garden. The high abundance of minors in the top section of the fungus garden is thus likely to be a consequence of the role they play both in food preparation and in the general defence via the metapleural glands.…”

Differential resistance and the importance of antibiotic production in Acromyrmex echinatior leaf-cutting ant castes towards the entomopathogenic fungus Aspergillus nomius

“…These glands produce a secretion containing more than 20 different compounds in Acromyrmex octospinosus (do Nascimento et al, 1996;Ortius-Lechner et al, 2000), and these are known to have bactericidal and fungicidal properties (Maschwitz, 1974, Beattie et al, 1985Ortius-Lechner et al, 2000;Bot et al, 2002;Poulsen et al, 2002a). The spread of gland secretion over the ant cuticle has previously been thought to be passive, but recent findings suggest that ants actively groom and apply the antibiotic secretion, especially in events of fungal infection (Bot et al, 2001b;Fernández-Marín et al, 2003, making it of hygienic importance for both the individual and the colony (Beattie et al, 1985(Beattie et al, , 1986Koob, 1970, 1971;Maschwitz et al, 1970;do Nascimento et al, 1996;Bot et al, 2002;Poulsen et al, 2002b). Angus et al (1993) examined the relationship between metapleural gland cell number and ant size and found a strong positive association between the two.…”

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

“…Almost all ants have paired exocrine metapleural glands located at the posterolateral end of the mesosoma (Hölldobler and EngelSiegel 1984), which have repeatedly been hypothesised to fulfil general defence functions against common diseases (e.g. Maschwitz 1974;Beattie et al 1985Beattie et al , 1986Ortius-Lechner et al 2000;Bot et al in print), but direct experimental evidence for this hypothesis has never been obtained (Currie 2001). The present study presents such evidence by experimentally manipulating metapleural gland function and investigating the effects on ant mortality after exposure to a common insect pathogenic fungus.…”