Morphophysiological Differences between the Metapleural Glands of Fungus-Growing and Non–Fungus-Growing Ants (Hymenoptera, Formicidae)

Parasites and their hosts use different strategies to overcome the defenses of the other, often resulting in an evolutionary arms race. Limited animal studies have explored the differential responses of hosts when challenged by differential parasite loads and different developmental stages of a parasite. The fungus-growing ant Trachymyrmex sp. 10 employs three different hygienic strategies to control fungal pathogens: Grooming the antibiotic-producing metapleural glands (MGs) and planting or weeding their mutualistic fungal crop. By inoculating Trachymyrmex colonies with different parasite concentrations (Metarhizium) or stages (germinated conidia or ungermianted conidia of Metarhizium and Escovopsis), we tested whether ants modulate and change hygienic strategies depending on the nature of the parasite challenge. There was no effect of the concentration of parasite on the frequencies of the defensive behaviors, indicating that the ants did not change defensive strategy according to the level of threat. However, when challenged with conidia of Escovopsis sp. and Metarhizium brunneum that were germinated or not-germinated, the ants adjusted their thygienic behavior to fungal planting and MG grooming behaviors using strategies depending on the conidia germination status. Our study suggests that fungus-growing ants can adjust the use of hygienic strategies based on the nature of the parasites.

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Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2009.0184 ◽

2009 ◽

Vol 276 (1665) ◽

pp. 2263-2269 ◽

Cited By ~ 81

Author(s):

Hermógenes Fernández-Marín ◽

Jess K. Zimmerman ◽

David R. Nash ◽

Jacobus J. Boomsma ◽

William T. Wcislo

Keyword(s):

Biological Control ◽

Exocrine Glands ◽

Relative Importance ◽

Fungal Symbiont ◽

Metapleural Glands ◽

Spectrum Activity ◽

Fungus Growing Ants ◽

Antimicrobial Metabolites ◽

And Control ◽

Broad Spectrum Activity

To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria ( Pseudonocardia ) that are cultured on the ants' exoskeletons and chemical cocktails from exocrine glands, especially the metapleural glands (MG). Previous work has hypothesized that (i) Pseudonocardia antibiotics are narrow-spectrum and control a fungus ( Escovopsis ) that parasitizes the ants' fungal symbiont, and (ii) MG secretions have broad-spectrum activity and protect ants and brood. We assessed the relative importance of these lines of defence, and their activity spectra, by scoring abundance of visible Pseudonocardia for nine species from five genera and measuring rates of MG grooming after challenging ants with disease agents of differing virulence. Atta and Sericomyrmex have lost or greatly reduced the abundance of visible bacteria. When challenged with diverse disease agents, including Escovopsis , they significantly increased MG grooming rates and expanded the range of targets. By contrast, species of Acromyrmex and Trachymyrmex maintain abundant Pseudonocardia. When challenged, these species had lower MG grooming rates, targeted primarily to brood. More elaborate MG defences and reduced reliance on mutualistic Pseudonocardia are correlated with larger colony size among attine genera, raising questions about the efficacy of managing disease in large societies with chemical cocktails versus bacterial antimicrobial metabolites.

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The metapleural glands of fungus-growing and non-fungus-growing ants: Ultrastructural study

Animal Biology ◽

10.1163/15707563-00002446 ◽

2014 ◽

Vol 64 (3) ◽

pp. 277-294

Author(s):

Alexsandro Santana Vieira ◽

Odair Correa Bueno ◽

Maria Izabel Camargo-Mathias

Keyword(s):

Antimicrobial Properties ◽

Secretory Cells ◽

Metapleural Gland ◽

Transmission Electron ◽

Metapleural Glands ◽

Feeding Type ◽

Leaf Cutting ◽

Fungus Growing Ants ◽

Secretory Capacity

The metapleural glands are considered an autapomorphic structure to ants and probable have an antibiotic or antifungal function. The present study was aimed at investigating the ultrastructural morphology of the metapleural glands in ants which have different feeding types: from fungus-growing ants, the higher and lower attine, and non-fungus-growing ants from the tribes Blepharidattini and Ectatommini analyzed by transmission electron microscopy. Plasma membrane invaginations in secretory cells of both fungus-growing and non-fungus-growing ants facilitate absorption of extracellular material from hemolymph. Higher and lower attines differed slightly from non-fungus-growing ants, by the presence of oval secretory cells and well-developed RER in the metapleural glands, which indicates a higher production of secretion in attines. Also, well-developed Golgi regions in the leaf-cutting ants and Ectatommini probably modify the secretions, produced by the secretory cell or coming of the hemolymph, into pheromone or antimicrobial compounds, the latter mainly in leaf-cutting ants. Still, the secretory cells of the metapleural gland of leaf-cutting ants exhibited several mitochondria near microvilli of the intracytoplasmic portion of the canaliculus, indicating an important role of the metapleural gland in the production and transport of secretion in metapleural gland of leaf-cutting ants. Thus, our work corroborates other findings, however our results add that the slight ultrastructural difference in the metapleural glands of leaf-cutting ants can be due to the feeding type (fungus-growing ants), resulting in greater secretory capacity and antimicrobial properties to combat pathogens (for example, micro-fungi parasites Escovopsis).

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Microsatellite primers for fungus-growing ants

Molecular Ecology Notes ◽

10.1046/j.1471-8286.2002.00229.x ◽

2002 ◽

Vol 2 (3) ◽

pp. 320-322 ◽

Cited By ~ 1

Author(s):

P. Villesen ◽

P. J. Gertsch ◽

J. J. Boomsma

Keyword(s):

Microsatellite Primers ◽

Fungus Growing Ants

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The Larvae of the Fungus-Growing Ants

The American Midland Naturalist ◽

10.2307/2421490 ◽

1948 ◽

Vol 40 (3) ◽

pp. 664 ◽

Cited By ~ 8

Author(s):

George C. Wheeler

Keyword(s):

Fungus Growing Ants

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Fungus-growing ants use antibiotic-producing bacteria to control garden parasites

Nature ◽

10.1038/19519 ◽

1999 ◽

Vol 398 (6729) ◽

pp. 701-704 ◽

Cited By ~ 484

Author(s):

Cameron R. Currie ◽

James A. Scott ◽

Richard C. Summerbell ◽

David Malloch

Keyword(s):

Fungus Growing Ants

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Antimicrobial mode of action of secretions from the metapleural gland ofMytmecia gulosa(Australian bull ant)

Canadian Journal of Microbiology ◽

10.1139/m95-018 ◽

1995 ◽

Vol 41 (2) ◽

pp. 136-144 ◽

Cited By ~ 23

Author(s):

J. A. Mackintosh ◽

J. E. Trimble ◽

A. J. Beattie ◽

D. A. Veal ◽

M. K. Jones ◽

...

Keyword(s):

Candida Albicans ◽

Antimicrobial Agents ◽

Structural Integrity ◽

Phospholipid Bilayer ◽

Active Components ◽

Cytoplasmic Matrix ◽

Metapleural Glands ◽

Total Leakage ◽

Membrane Bound ◽

And Function

Secretions from exocrine metapleural glands of Myrmecia gulosa (Australian bull ant) exhibit broad-spectrum antimicrobial activity. Treatment of the yeast Candida albicans with metapleural secretion resulted in the rapid and total leakage of K+ions from cells within 10 min. Ultrastructural analysis of the bacteria Bacillus cereus, Escherichia coli, and Pseudomonas aeruginosa, and cells and protoplasts of Candida albicans demonstrated gross damage of the cell membrane and aggregation of the cytoplasmic matrix of treated cells. Degradation of membrane-bound organelles was also observed in Candida albicans. The antimicrobially active components of metapleural secretions were nonpolar and interacted with the phospholipid bilayer, causing damage to the structural integrity of liposomes and the release of carboxyfluorescein. The data suggest that the antimicrobial agents in metapleural secretion act primarily by disrupting the structure and function of the phospholipid bilayer of the cytoplasmic membrane.Key words: ant metapleural secretion, antimicrobial, Candida albicans, cytoplasmic membrane.

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