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Inhibition of the fungal pathogen Metarhizium anisopliae in the alimentary tracts of five termite (Isoptera) species.

There are more than 2,600 described species of termites, from 7 families, and they are adapted to a wide range of habitats resulting in high diversity in morphology, physiology, behavior, nesting ecology, and associated microbial community (Abe et al. 2000). Sociality is thought to be a key factor in their ecological success and diversity, but how termites evolved to resist the increased pressure from pathogens as they moved from the solitary lifestyle of the wood roach-like ancestor towards eusociality remains poorly understood (Fefferman et al. 2007). Chouvenc and Su (2010) showed that the subterranean termite Reticulitermes flavipes (Kollar) has the capacity to prevent epizootics of the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin due to synergy among defense mechanisms. Chouvenc et al. (2009a) described in vivo the antifungal activity of the alimentary tract in R. flavipes and showed that after grooming and ingestion of conidia of M. anisopliae, germination did not occur in the alimentary tract of living termites. In dead termites, this antifungal activity remained strong at least 2 d post mortem throughout all gut regions.

We hypothesized that gut antifungal activity is an ancestral feature and was maintained during the radiation of the isopteran lineage. To test this, we extended our observations to determine if this mechanism exists in 5 additional termite species from 5 different families. Histological preparation was identical to Chouvenc et al. (2009a) and was performed on selected specimens described in Chouvenc et al. (2009c). Histological analysis included 25 Hodotermopsis sjoestedti Holmgren (Termopsidae), 8 Hodotermes mossambicus (Hagen) (Hodotermitidae), 13 Kalotermes flavicollis (Fabricius) (Kalotermitidae), 10 Prorhinotermes canalifrons (Sjoestedt) (Rhinotermitidae), and 2 Nasutitermes voeltzkowi (Wasmann) (Termitidae). The presence or absence of conidia in the gut was recorded in all specimens, and the presence of fungal hyphae was examined in healthy, moribund, and dead specimens. Full histological observations for each species are available in the supplemental information.

After exposure to a solution of M. anisopliae conidia, grooming was performed by the termites and conidia were subsequently found in the alimentary tracts of the groomers for all 5 termite species (Fig. 1A). For each species, conidia in the alimentary tract did not germinate, as previously described in R. flavipes (Chouvenc et al. 2009a). In all the specimens that were fixed after their death (usually 2-5 d after fungal exposure) for histological preparation, the fungal hyphae quickly spread in the hemocoel, the muscles (Fig. 1B) and the fat body within the 24 h post mortem, but did not readily invade the salivary glands. The fungus did not penetrate the salivary glands until at least after 1 d post mortem. In addition, M. anisopliae hyphae did not penetrate the gut lumen until at least after 2 d post mortem. We confirmed that the fungistatic activity of the alimentary tract was present in all tested species and that this activity remained strong in the alimentary tract at least 2 d post mortem (Figs. 1C and ID), although the salivary glands were already invaded by the fungus at this time (Fig. 1E). Therefore, all conidia found in the digestive tract of live termites did not germinate and the fungistatic activity of the gut in all termite species remained active for several days after the death of the termites, as previously showed in R. flavipes (Chouvenc et al. 2009a). We suggest that gut fungistatic activity is an ancestral trait that has been conserved during the radiation of the Isoptera. However, we previously showed that all termites studied had a variable mortality rate when exposed to M. anisopliae (Chouvenc et al. 2009c). The present results suggest that this difference of susceptibility among species may depend on other physiological factors, such as the cellular immunity (Chouvenc et al. 2009b), or other behavioral and physiological factors (Cremer et al. 2007). It has been suggested that part of this fungistatic activity is due to the production of antimicrobial peptides in the salivary glands (Lamberty et al. 2001; Bulmer & Crozier 2004), but our results showed that in all species the salivary glands were invaded by the fungus much faster than the gut lumen, indicating that the antimicrobial compounds contained in the salivary glands may have a limited activity inside the digestive tract, or that the fungistatic activity of the gut is due to a range of various compounds.

[FIGURE 1 OMITTED]

Finally, we observed in the midgut of a K. flavicollis specimen the presence of a fragment of external cuticle with a cellular encapsulation (Fig. 1F), as described by Chouvenc et al. (2009b). This observation suggests that the termite performed necrophagy on a dead nestmate that

has been previously infected by M. anisopliae, and that the passage through the gut lumen did not allow this ingested fungal particles to grow while in the alimentary tract. Therefore, cannibalism of an infected cadaver may aid in preventing M. anisopliae from completing its life cycle in a termite group. Grooming and necrophagy in association with gut antifungal activity provides an environment that reduces the chances for the fungus to produce an epizootic into the termite nest. This mechanism appeared to be conserved in all tested species from 5 different families.

SUMMARY

We previously showed that in the subterranean termite Reticulitermes flavipes conidia of Metarhizium anisopliae did not germinate in the alimentary tract of living termites and the antifungal activity remained for 2 d post mortem in the gut. We have confirmed that this mechanism is common throughout the termite phylogeny by extending our observations to 5 additional species, from 5 different families. Grooming and ingestion of microorganisms from the cuticle of nestmate was found to be consistent in all the species and none of the conidia found in the alimentary tracts germinated.

REFERENCES CITED

ABE, T. 1987. Evolution of life types in termites, pp. 125148 In S. Kawano, J. H. Connell, and T. Hidaka (eds.), Evolution and Coadaptation: Biotic Communities. University of Tokyo Press, Tokyo.

BULMER, M., AND CROZIER, R. H. 2004. Duplication and diversifying selection among termite antifungal peptides. Mol. Biol. Evol. 21: 2256-2264.

CHOUVENC, T., AND SU, N.-Y. 2010. Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events The limits and potential for biological control. J. Econ. Entomol. In press.

CHOUVENC, T., SU, N.-Y., AND ROBERT, A. 2009a. Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J. Invertebr. Pathol. 101: 130-136.

CHOUVENC, T., SU, N.-Y., AND ROBERT, A. 2009b. Cellular encapsulation in the eastern subterranean termite, Reticulitermes flavipes (Isoptera), against infection by the entomopathogenic fungus Metarhizium anisopliae. J. Invertebr. Pathol. 101: 234-241.

CHOUVENC, T., SU, N.-Y., AND ROBERT, A. 2009c. Susceptibility of seven termite species (Isoptera) to the entomopathogenic fungus Metarhizium anisopliae. Sociobiology 54, 723-748.

CREMER, S., ARMITAGE, S. A. O., and Schmid-Hempel, P. 2007. Social immunity. Curr. Biol. 17: 693-702.

CULLINEY, T. W., AND GRACE, J. K. 2000. Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bull. Entomol. Res. 90: 9-21.

FEFFERMAN, N. H., TRANIELLO, J. F. A., Rosengaus, R. B., and Calleri II, D. V. 2007. Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behav. Ecol. Sociobiol. 61, 565-577.

LAMBERTY, M., ZACHARY, D., LANOT, R., BORDEREAU, C., ROBERT, A., HOFFMANN, J. A., AND BULET, P. 2001. Insect immunity constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J. Biol. Chem. 276: 4085-4092.

THOMAS CHOUVENC (1) *, NAN-YAO SU (1) AND ALAIN ROBERT (2,3)

(1) Department of Entomology and Nematology, Ft. Lauderdale Research and Education Center, University of Florida, Institute of Food and Agricultural Sciences, 3205 College Ave, Ft. Lauderdale, FL 33314, USA

(2) UMR 5548 Communication chimique et developpement chez les insectes, Universite de Bourgogne, 6 Bd Gabriel, 2100 Dijon, France

(3) Current address: Centre IRD France Nord, 32 avenue Varagnat, 93143 Bondy, France

* Corresponding author

Supplemental material online at http://www.fcla.edu/ FlaEnt/fe93(3).htm#InfoLink1
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Title Annotation:Scientific Notes
Author:Chouvenc, Thomas; Su, Nan-Yao; Robert, Alain
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1USA
Date:Sep 1, 2010
Words:1319
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