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FOCUS OF FLIES FACILITY RESEARCH: Animal carcasses represent nutrient rich resources, or food-falls, for many organisms ranging from microbes, such as those previously discussed, to vertebrate scavengers. Microbes were initially thought of only as nutrient recyclers (Lindeman 1942). However, Jenzen (1977) suspected that microbes were competitors with other consumers including insects for these resources. Microbes may alter food resources and produce toxins that affect the “appeal” of the resources, and themselves, to other consumers. Microbes colonizing fish carrion in tidal estuaries will compete with other consumers for these resources (Burkepile et al. 2006). These microbes release noxious chemicals that deterred consumption of the fish remains by higher level consumers, such as crustaceans (Burkepile et al. 2006).
Higher order scavengers are selected to have mechanisms countering competition strategies used by microbes also colonizing food-falls. These responses could be behavioral (Lam et al. 2007) or physiological (Haine et al. 2008, Rozen et al. 2008). The burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae), which depends on small carrion as a breeding site, have evolved counterstrategies to suppress microbial communities in order to reduce competition for these resources (Rozen et al. 2008). In turn, the presence of some microbes was detrimental to immature development and reproductive success of the burying beetle (Rozen et al. 2008). The blow fly L. sericata will colonize and feed on necrotic tissue in wounds on living individuals, and their salivary excretions have antimicrobial activity against Staphylococcus aureus, Streptococcus A and B, as well as Pseudomonas sp. (Jones and Wall 2008). Similarly, house fly larvae in target food-falls reduce the growth of competing fungi (Lam et al. 2007). However, interactions between fly and microbe species can be quite diverse depending on the parties involved. In some cases, these interactions are beneficial while in others they are detrimental depending on parameters, such as the microbe and fly species or strains involved, population density, and genetic diversity.
Microbes alter, or releasing noxious compounds, on food sources to avoid predators. Many saprophagous insects feed directly on microbes associated with decomposing material as part of their diet. House fly larval development is dependent upon bacteria associated with the larval resource (Zurek et al. 2000). Black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), which is another colonizer of decomposing chicken carcasses, can reduce carcass E. coli counts by a log of four (Erickson et al. 2004). We determined that black soldier fly larvae reared in dairy manure for 72 hr reduced E. coli by a log of eight (Liu et al. 2008), and it is hypothesized that the bacteria serve as nutrients for larval development.
Competition between microbes and insects for ephemeral resources has resulted in selection towards coexistence (Dale et al. 2001, Vandermeer et al. 2002) or symbiosis (Keller 2002). Such interactions are common in the insect world. Volatiles emitted by microbes, proliferating on decomposing remains (Vass et al. 2002), are used by blow flies to locate these resources (Ashworth and Wall 1994, Woolridge et al. 2007). Bovine blood inoculated with bacteria isolated from wounds infested with C. homnivorax release volatiles that attract intraspecific adults (Chaudhury et al. 2002). House fly eggs, when deposited, are coated with microbes which potentially produce defensive compounds which offer protection from predators and pathogens (Keller 2002). Once deposited, house flies respond to volatiles emitted by these microbes (Lam et al. 2007). Volatile concentrations below a specific threshold attract individuals that will oviposit, while concentrations above the threshold repel these same individuals (Lam et al. 2007). In addition, volatile concentration positively correlated with microbial population density. Colonization attempts when volatiles were above the threshold resulted in reduced survivorship of these eggs to the adult stage, while the opposite was determined for eggs deposited when volatiles were below the identified threshold (Lam et al. 2007). Many microbes, both pathogenic and non-pathogenic, are ingested by developing house flies (Banjo 2005), and larvae surviving to the adult stage are inoculated with these microbes which are then dispersed to other resources during subsequent fly oviposition (Lam et al. 2007). In some instances, individuals consuming microbes receive nutritional benefits, such as essential amino acids and vitamins. Tsetse flies, Glossina sp., are provided B vitamins by Wigglesworthia (Keller 2002). Furthermore, Buchnera aphidicola, which is an endosymbiont of aphids, provides essential amino acids to their hosts (Keller 2002).
Blow flies and microbes occurring on food-falls have evolved a mutualistic relationship. Microbes consumed by immature blow flies feeding on a resource (Ahmad et al. 2000), survive larval molting and pupation, and are present in emergent adult insects which serve as a dispersal mechanism (Ahmad et al. 2006). The microbes release volatiles that attract blow flies to resources and resulting progeny disperse microbes to new habitats (Zurek et al. 2000). However, consumption by the wrong saprophage results in microbial mortality (Zurek et al. 2000). We hypothesize that while one bacterial species survives digestion and pupation with one fly species, it will not with another fly species. Therefore, bacterial proliferation and dispersal is mitigated by colonization patterns of fly species. However, such an association could prove detrimental to both species as the volatiles emitted could also attract predators (Thomas et al. 2008), such as C. rufifacies, to their prey, which would be C. macellaria larvae in this case.
References Cited
Ahmad, A., A. Broce, and L. Zurek. 2006. Evaluation of significance of bacteria in larval development of Cochliomyia macellaria (Diptera: Calliphoridae). J. Med. Entomol. 43: 1129-1133.
Burekpile, D.E., J.D. Parker, C.B. Woodson, H.J. Mills, J. Kubanek, P.A. Sobecky, and M.E. Hay. 2006. Chemically mediated competition between microbes and animals: microbes as consumers in food webs. Ecology 87: 2821-2831.
Dale, C., Young, S.A., Haydon, D.T., Welburn, S.C. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasions. Proc. Natl. Acad. Sci. USA 98: 1883-1888.
Erickson, M.C., M. Islam, C. Sheppard, J. Liao, and M.P. Doyle. 2004. Reduction of Escherichia coli O157:H7 and Salmonella enterica serovar enteritidis in chicken manure by larvae of the black soldier fly. J. Food. Protect. 67: 685-690.
Haine, E.R., Y. Moret, M.T. Siva-Jothy, and J. Rolff. 2008. Antimicrobial defense and persistent infection in insects. Science 322: 1257-1259.
Janzen, D.H. 1977. Why fruits rot, seeds mold, and meat spoils. Amer. Natl. 111: 691-713.
Jones, G. and R. Wall. 2008. Maggot-therapy in veterinary medicine. Research Vetern. Sci. 85: 394-398.
Keller, R.L. 2002. The Role of Microorganisms for Eggs and Their Progeny. In Chemoecology of Insect Eggs and Egg Deposition. M. Hiker and T. Meiners [eds.]. Blackwell Publishing, Berlin, Germany. Pp. 149-167.
Lam, K., D. Babor, B. Duthie, ElM. Babor, M. Moore, and G. Gries. 2007. Proliferating bacterial symbionts on house fly eggs affect oviposition behavior of adult flies. Ani. Behav. 74: 81-92.
Lindeman, R. L. 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399-418.
Liu, Q., J.K. Tomberlin, J.A. Brady, M.R. Sanford, and Z. Yu. 2008. Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environ. Entomol. 37: 1525-1530.
Rozen, D.E., D.J.P. Engelmoer, and P.T. Smiseth. 2008. Antimicrobial strategies in burying beetles breeding on carrion. Proc. Natl. Acad. Sci. USA 105: 17890-17895.
Thomas, R.S., D.M. Glen, and W.O.C. Symondson. 2008. Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus melanarius. 40: 207-216.
Vandermeer, J., M.A. Evans, P. Foster, T. HööK, M. Reiskind, and M. Wund. 2002. Increased competition may promoe species coexistence. Proc. Natl. Acad. Sci. USA 99: 8731-8736.
Zurek, L., C. Schal, and D.W. Watson. 2000. Diversity and contribution of the intestinal bacterial community to the development of Musca domestica (Diptera: Muscidae) larvae. J. Med. Entomol. 37: 924-928.
