Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-18T00:16:29.121Z Has data issue: false hasContentIssue false
  • English
  • Français

Physiological trade-offs of forming maggot masses by necrophagous flies on vertebrate carrion

Published online by Cambridge University Press:  18 May 2011

D.B. Rivers ,
C. Thompson  and
R. Brogan
D.B. Rivers*
Affiliation:
Department of Biology, Loyola University Maryland, 4501 North Charles Street, Baltimore, Maryland 21210, USA
C. Thompson
Affiliation:
Department of Biology, Loyola University Maryland, 4501 North Charles Street, Baltimore, Maryland 21210, USA
R. Brogan
Affiliation:
Department of Biology, Loyola University Maryland, 4501 North Charles Street, Baltimore, Maryland 21210, USA
*
*Authors for correspondence Fax: +01 410 617 5682 E-mail: drivers@loyola.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Necrophagous flies that colonize human and animal corpses are extremely efficient at locating and utilizing carrion. Adult flies deposit eggs or larvae on the ephemeral food resource, which signals the beginning of intense inter- and intra-species competition. Within a short period of time after egg hatch, large larval aggregations or maggot masses form. A period of intense larval feeding ensues that will culminate with consumption/decomposition of all soft tissues associated with the corpse. Perhaps the most distinctive feature of these feeding aggregations is heat production; that is, the capacity to generate internal heat that can exceed ambient temperatures by 30°C or more. While observations of maggot mass formation and heat generation have been described in the research literature for more than 50 years, our understanding of maggot masses, particularly the physiological ecology of the aggregations as a whole, is rudimentary. In this review, an examination of what is known about the formation of maggot masses is presented, as well as arguments for the physiological benefits and limitations of developing in feeding aggregations that, at times, can represent regions of intense competition, overcrowded conditions, or a microclimate with elevated temperatures approaching or exceeding proteotoxic stress levels.

Keywords

larval aggregationsforensic entomologyproteotoxic stressheterothermylarval crowdingblow flies
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 5 , October 2011 , pp. 599 - 611
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akre, R.D., Greene, A., MacDonald, J.F., Landolt, P.J. & Davis, H.G. (1981) The yellow jackets of America north of Mexico. Agriculture Handbook, 552. Washington DC, USA, United States Department of Agriculture, Science and Education Administration.Google Scholar
Al-Misned, F.A.M. (2002) Effects of larval population density on the life cycle of flesh fly, Wohlfahrtia nuba (Wiedemann) (Diptera: Sarcophagidae). Saudi Journal Biological Science 9, 140–147.Google Scholar
Amendt, J., Krettek, R., Niess, C., Zehner, R. & Bratzke, H. (2000) Forensic entomology in Germany. Forensic Science International 113, 309–314.CrossRefGoogle ScholarPubMed
Anderson, G.S. (2010) Factors that influence insect succession on carrion. pp. 201–250in Byrd, J.H. & Castner, J.L. (Eds) Forensic Entomology: The Utility of Using Arthropods in Legal Investigations. 2nd edn.Boca Raton, FL, USA, CRC Press.Google Scholar
Anderson, G.S. & VanLaerhoven, S.L. (1996) Initial studies on insect succession on carrion in southwestern British Columbia. Journal of Forensic Science 41, 617–625.CrossRefGoogle Scholar
Anderson, O.D. (1982) Enzyme activities in the larval secretion of Calliphora erythrocephala. Comparative Biochemistry and Physiology B 72, 569–575.CrossRefGoogle Scholar
Anderson, R.S. & Peck, S.B. (1985) The insects and arachnids of Canada: part 13. The carrion beetles of Canada and Alaska, Coleoptera: Siliphidae and Agyrtidae. Publication 1778. Ottawa, Ontario, Canada, Research Branch and Agri-Food Agriculture Canada.Google Scholar
Ashworth, J.R. & Wall, R. (1994) Responses of the sheep blowflies Lucilia sericata and L. cuprina to odour and the development of semiochemical baits. Medical and Veterinary Entomology 8, 303–309.CrossRefGoogle ScholarPubMed
Barton Browne, L., Bartell, R.J. & Shorey, H.H. (1969) Pheromone-mediated behaviour leading to group oviposition in the blowfly Lucilia cuprina. Journal of Insect Physiology 15, 1003–1014.CrossRefGoogle Scholar
Baumgartner, D.L. (1993) Review of Chrysomya rufifacies (Diptera: Calliphoridae). Journal of Medical Entomology 30, 105–113.CrossRefGoogle ScholarPubMed
Bernstein, C. (2000) Host-parasitoid models: the story of a successful failure. pp. 41–57in Hochberg, M.E. & Ives, A.R. (Eds) Parasitoid Population Biology. Princeton, NJ, USA, Princeton University Press.CrossRefGoogle Scholar
Bland, R.G. & Jaques, H.E. (1978) How to Know the Insects. Dubuque, Iowa, USA, W.C. Brown.Google Scholar
Bowles, V.M., Carnegie, P.R. & Sandeman, R.M. (1988) Characterization of proteolytic and collagenolytic enzymes from the larvae of Lucilia cuprina, the sheep blowfly. Australian Journal of Biological Science 41, 269–278.CrossRefGoogle ScholarPubMed
Buck, S., Nicholson, M., Dudas, S., Wells, R., Force, A., Baker, G.T. & Arking, R. (1993) Larval regulation of adult longevity in a genetically-selected long-lived strain of Drosophila. Heredity 71, 23–32.CrossRefGoogle Scholar
Byrd, J.H. & Butler, J.F. (1996) Effects of temperature on Cochliomyia macellaria (Diptera: Calliphoridae) development. Journal of Medical Entomology 33, 901–905.CrossRefGoogle ScholarPubMed
Byrd, J.H. & Butler, J.F. (1998) Effects of temperature on Sarcophaga haemorrhoidalis (Diptera: Sarcophagidae) development. Journal of Medical Entomology 35, 694–698.CrossRefGoogle ScholarPubMed
Byrd, J.H. & Castner, J.L (2010) Insects of forensic importance. pp. 39–126in Byrd, J.H. & Castner, J.L. (Eds) Forensic Entomology: The Utility of Using Arthropods in Legal Investigations. 2nd edn.Boca Raton, FL, USA, CRC Press.Google Scholar
Campobasso, C.P., Di Vella, G. & Introna, F. (2001) Factors affecting decomposition and Diptera colonization. Forensic Science International 120, 18–27.CrossRefGoogle ScholarPubMed
Chen, C.-P., Lee, R.E. Jr & Denlinger, D.L. (1990) A comparison of the responses of tropical and temperate flies (Diptera: Sarcophagidae) to cold and heat stress. Journal of Comparative Physiology B 160, 543–547.CrossRefGoogle Scholar
Christopherson, C. & Gibo, D.L. (1996) Foraging by food deprived larvae of Neobellieria bullata (Diptera: Sarcophagidae). Journal of Forensic Science 42, 71–73.CrossRefGoogle Scholar
Cianci, T.J. & Sheldon, J.K. (1990) Endothermic generation by blowfly larvae Phormia regina developing in pig carcasses. Bulletin of the Society of Vector Ecology 15, 33–40.Google Scholar
Clark, K., Evans, L. & Wall, R. (2006) Growth rates of the blowfly, Lucilia sericata, on different body tissues. Forensic Science International 156, 145–149.CrossRefGoogle ScholarPubMed
Cragg, J.B. (1956) The olfactory behaviour of Lucilia species (Diptera) under natural conditions. Annals of Applied Biology 44, 467–471.CrossRefGoogle Scholar
Darling, D.C. & Werren, J.H. (1990) Biosystematics of two new species of Nasonia (Hymenoptera: Pteromalidae) reared from birds’ nests in North America. Annals of the Entomological Society of America 83, 352–370.CrossRefGoogle Scholar
Day, D.M. & Wallman, J.F. (2006) A comparison of frozen/thawed and fresh food substrates in development of Calliphora augur (Diptera Calliphoridae) larvae. International Journal of Legal Medicine 120, 391–394.CrossRefGoogle ScholarPubMed
Denlinger, D.L. (2002) Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
Denno, R.F. & Cothran, W.R. (1976) Competitive interactions and ecological strategies of sarcophagid and calliphorid flies inhabiting rabbit carrion. Annals of the Entomological Society of America 69, 109–113.CrossRefGoogle Scholar
Deonier, C.C. (1940) Carcass temperatures and their relation to winter blowfly populations and activity in the southwest. Journal of Economic Entomology 33, 166–170.CrossRefGoogle Scholar
DeVaney, J.A., Eddy, G.W., Ellis, E.M. & Harrington, R. Jr (1973) Attractancy of inoculated and incubated bovine blood fractions to screwworm flies (Diptera: Calliphoridae): role of bacteria. Journal of Medical Entomology 10, 591–595.CrossRefGoogle ScholarPubMed
Disney, R.H.L. & Munk, T. (2004) Potential use of Braconidae (Hymenoptera) in forensic cases. Medical and Veterinary Entomology 18, 442–444.CrossRefGoogle ScholarPubMed
Donovan, S.E., Hall, M.J., Turner, B.D. & Moncrieff, C.B. (2006) Larval growth rates of the blowfly, Calliphora vicina, over a range of temperatures. Medical and Veterinary Entomology 20, 106–114.CrossRefGoogle Scholar
dos Reis, S.F., von Zuben, C.J. & Godoy, W.A.C. (1999) Larval aggregation and competition for food in experimental populations of Chrysomya putoria (Wied.) and Cochliomyia macellaria (F.) (Dipt., Calliphoridae). Journal of Applied Entomology 123, 485–489.CrossRefGoogle Scholar
Edney, E.B. (1977) Water Balance in Land Arthropods. New York, UK, Springer Verlag.CrossRefGoogle Scholar
Eisemann, C.H. & Rice, M.J. (1987) The origin of sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae), attractants in media infested with larvae. Bulletin of Entomological Research 77, 287–294.CrossRefGoogle Scholar
Erzinclioglu, Z. (1996) Blowflies. Slough, UK, Richmond Publishing Co., Ltd.Google Scholar
Feder, M.E. (1996) Ecological and evolutionary physiology of stress proteins and the stress response. pp. 79–102in Johnston, I.A. & Bennett, A.F. (Eds) Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Feder, M.E., Blair, N. & Figueras, H. (1997) Natural thermal stress and heat shock protein expression in Drosophila larvae and pupae. Functional Ecology 11, 90–100.CrossRefGoogle Scholar
Float, K., Khan, B. & Gibson, G. (1999) Hymenopterous parasitoids of filth fly (Diptera: Muscidae) pupae in cattle feedlots. Canadian Entomologist 131, 347–362.CrossRefGoogle Scholar
Gennard, D.E. (2007) Forensic Entomology: An Introduction. West Sussex, UK, Wiley.Google Scholar
Gomes, L., Godoy, W.A.C. & Von Zuben, C.J. (2006) A review of post-feeding larvae dispersal in blowflies: implications for forensic entomology. Naturwissenschaften 93, 207–215.CrossRefGoogle Scholar
Goodbrod, J.R. & Goff, M.L. (1990) Effects of larval populations density on rates of development and interactions between two species of Chrysomya (Diptera: Calliphoridae) in laboratory culture. Journal of Medical Entomology 27, 338–343.CrossRefGoogle ScholarPubMed
Grassberger, M. & Reiter, C. (2001) Effect of temperature on Lucilia sericata (Diptera: Calliphoridae) development with special reference to the isomegalen- and isomorphen-diagram. Forensic Science International 120, 32–36.CrossRefGoogle Scholar
Grassberger, M. & Reiter, C. (2002) Effect of temperature on development of the forensically important holarctic blow fly Protophormia terraenovae (Robineau-Desvoidy) (Diptera: Calliphoridae). Forensic Science International 128, 177–182.CrossRefGoogle ScholarPubMed
Greenberg, B. (1990) Behaviour of postfeeding larvae of some Calliphoridae and a muscid (Diptera). Annals of the Entomological Society of America 83, 1210–1214.CrossRefGoogle Scholar
Greenberg, B. & Kunich, J.C. (2002) Entomology and the Law. Cambridge, UK, Cambridge University Press.Google Scholar
Hammack, L. (1990) Protein feeding and oviposition effects on attraction of screwworm flies (Diptera: Calliphoridae) to host fluids. Annals of the Entomological Society of America 83, 97–102.CrossRefGoogle Scholar
Hammack, L., Bromel, M., Duh, F.M. & Gassner, G. (1987) Reproductive factors affecting responses of the screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae), to an attractant of bacterial origin. Annals of the Entomological Society of America 80, 775–780.CrossRefGoogle Scholar
Hanski, I. (1976) Assimilation by Lucilia illustris (Diptera) larvae in constant and changing temperatures. Oikos 27, 288–299.CrossRefGoogle Scholar
Hanski, I. (1977) An interpolation model of assimilation by larvae of the blowfly, Lucilia illustris (Calliphoridae) in changing temperatures. Oikos 28, 187–195.CrossRefGoogle Scholar
Hanski, I. (1987) Carrion fly community dynamics: patchiness, seasonality and coexistence. Ecological Entomology 12, 257–266.CrossRefGoogle Scholar
Hanski, I. & Kuusela, S. (1977) An experiment on competition and diversity in the carrion fly community. Annales Entomologica Fennici 43, 108–115.Google Scholar
Higley, L.G. & Haskell, N.H. (2010) Insect development and forensic entomology pp. 389–406in Byrd, J.H. & Castner, J.L. (Eds) Forensic Entomology: The Utility of Using Arthropods in Legal Investigations. 2nd edn.Boca Raton, FL, USA, CRC Press.Google Scholar
Hunter, A.F. (2000) Gregariousness and repellant defences in the survival of phytophagous insects. Oikos 91, 213–224.CrossRefGoogle Scholar
Ireland, S. & Turner, B. (2006) The effects of larval crowding and food type on the size and development of the blowfly, Calliphora vomitoria. Forensic Science International 159, 175–181.CrossRefGoogle ScholarPubMed
Ives, A.R. (1991) Aggregation and coexistence in a carrion fly community. Ecological Monographs 61, 75–94.CrossRefGoogle Scholar
Joplin, K.H., Yocum, G.D. & Denlinger, D.L. (1990) Cold shock elicits expression of heat shock proteins in the flesh fly Sarcophaga crassipalpis. Journal of Insect Physiology 36, 825–834.CrossRefGoogle Scholar
Joy, J.E., Liette, N.L. & Harrah, H.L. (2006) Carrion fly (Diptera: Calliphoridae) larval colonization of sunlit and shaded pig carcasses. Forensic Science International 164, 183–192.CrossRefGoogle ScholarPubMed
Kamal, A.S. (1958) Comparative study of thirteen species of sarcosaprophagous Calliphorida and Sarcophagidae (Diptera). I. Bionomics. Annals of the Entomological Society of America 51, 261–270.CrossRefGoogle Scholar
Kaneshrajah, G. & Turner, B. (2004) Calliphora vicina larvae grow at different rates on different body tissues. International Journal of Legal Medicine 118, 242–244.CrossRefGoogle ScholarPubMed
Kneidel, K.A. (1984) Competition and disturbance in communities of carrion-breeding Diptera. Journal of Animal Ecology 53, 849–865.CrossRefGoogle Scholar
Kneidel, K.A. (1985) Patchiness, aggregation and the coexistence of competitors for ephemeral resources. Ecological Entomology 10, 441–448.CrossRefGoogle Scholar
Korsloot, A., van Gestel, C.A.M. & van Straalen, N.M. (2004) Environmental Stress and Cellular Response in Arthropods. Boca Raton, FL, USA, CRC Press.CrossRefGoogle Scholar
Kouki, J. & Hanski, I. (1995) Population aggregation facilitates coexistence of many competing carrion fly species. Oikos 72, 223–227.CrossRefGoogle Scholar
Krebs, J.R. & Davies, N.B. (1996) Introduction to Behavioural Ecology. Oxford, UK, Blackwell Publishing.Google Scholar
LéBlanc, H.N. & Logan, J.G. (2010) Exploiting insect olfaction in forensic entomology. pp. 205–221in Amendt, J., Campobasso, C.P., Goff, M.L. & Grassberger, M. (Eds) Current Concepts in Forensic Entomology. London, UK, Springer.Google Scholar
Legner, E.F. (1977) Temperature, humidity and depth of habitat influencing host destruction and fecundity of muscoid fly parasites. Entomophaga 22, 199–206.CrossRefGoogle Scholar
Levot, G.W., Brown, K.R. & Shipp, E. (1979) Larval growth of some calliphorid and sarcophagid diptera. Bulletin of Entomological Research 69, 469–475.CrossRefGoogle Scholar
Lints, F.A. & Lints, C.V. (1969) Influence of preimaginal environment on fecundity and ageing in Drosophila melanogaster hybrids. Experimental Gerontology 4, 231–244.CrossRefGoogle ScholarPubMed
Manjo, G. & Joris, I. (1995) Apoptosis, oncosis, and necrosis: an overview of cell death. American Journal of Pathology 146, 3–15.Google Scholar
Marchenko, M.I. (2001) Medicolegal relevance of cadaver entomo-fauna for the determination of the time since death. Forensic Science International 120, 89–109.CrossRefGoogle Scholar
Martinez-Sánchez, A., Rojo, S. & Marcos-Garcia, M.A. (2000) Annual and spatial activity of dung flies and carrion in a Mediterranean holm-oak pasture ecosystem. Medical and Veterinary Entomology 14, 56–63.CrossRefGoogle Scholar
Matsuura, M. & Sakagami, S.F. (1973) A bionomic sketch of the giant hornet, Vespa mandarinia, a serious pest for Japanese apiculture. Journal of the Faculty of Science of Hokkaido University, Series VI, Zoology 19, 125–162.Google Scholar
Micozzi, M.S. (1986) Experimental study of postmortem change under field conditions: effects of freezing, thawing, and mechanical injury. Oecologia 99, 181–187.Google Scholar
Muharsini, S., Dalrymple, B., Vucolo, T., Hamilton, S., Willadsen, P. & Wijffels, G. (2001) Biochemical and molecular characterization of serine proteases from larvae of Chrysomya bezziana, the Old World screwworm fly. Insect Biochemistry and Molecular Biology 31, 1029–1040.CrossRefGoogle ScholarPubMed
Norris, K.R. (1965) The bionomics of blowflies. Annual Review of Entomology 10, 47–68.CrossRefGoogle Scholar
Olton, G. & Legner, E. (1974) Biology of Tachinaephagus zealandicus Hymenoptera Encyrtidae parasitoid of synanthropic Diptera. Canadian Entomologist 106, 785–800.CrossRefGoogle Scholar
Padilha, M.H.P., Pimentel, A.C., Ribeiro, A.F. & Terra, W.R. (2009) Sequence and function of lysosomal and digestive cathepsin D-like proteinases of Musca domestica midgut. Insect Biochemistry and Molecular Biology 39, 782–791.CrossRefGoogle ScholarPubMed
Parrish, J.K. & Edelstein-Keshet, L. (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284, 99–101.CrossRefGoogle ScholarPubMed
Parsell, D.A. & Lindquist, S. (1994) Heat shock proteins and stress tolerance. pp. 467–494in Morimoto, R.I., Tissieres, A. & Georgopoulos, C. (Eds) The Biology of Heat Shock Proteins and Molecular Chaperons. Cold Spring Harbor, NY, USA, Cold Spring Harbor Laboratory Press.Google Scholar
Paulie, D., Arrigo, A.-P. & Tissieres, A. (1992) Heat shock response in Drosophila. Experientia 48, 623–628.CrossRefGoogle Scholar
Pendola, S. & Greenberg, B. (1975) Substrate-specific analysis of proteolytic enzymes in the larval midgut of Calliphora vicina. Annals of the Entomological Society of America 68, 341–345.CrossRefGoogle Scholar
Prange, H.D. (1995) Evaporative cooling in insects. Journal of Insect Physiology 42, 493–499.CrossRefGoogle Scholar
Prange, H.D. & Modi, J. (1990) Comparative evaporative cooling in grasshoppers and beetles. Physiologist 33, A–88.Google Scholar
Price, G.M. (1974) Protein metabolism by the salivary glands and other organs of the larva of the blowfly, Calliphora erythrocephala. Journal of Insect Physiology 20, 329–347.CrossRefGoogle ScholarPubMed
Putman, R.J. (1983) Carrion and dung: the decomposition of animal wastes. Institute of Biology's Studies in Biology, No. 156. London, UK, Edward Arnold Publishers.Google Scholar
Reznik, S.Y., Chernoguz, D.G. & Zinovjeva, K.B. (1992) Host searching, oviposition preferences and optimal synchronization in Alysia manducator (Hymenoptera: Braconidae), a parasitoid of the blowfly, Calliphora vicina. Oikos 65, 81–88.CrossRefGoogle Scholar
Richards, C.S. & Villet, M.H. (2008) Factors affecting accuracy and precision of thermal summation models of insect development used to estimate post-mortem intervals. International Journal of Legal Medicine 122, 401–408.CrossRefGoogle ScholarPubMed
Richards, C.S., Price, B.W. & Villet, M.H. (2009) Thermal ecophysiology of seven carrion-feeding blowflies (Diptera: Calliphoridae) in southern Africa. Entomologia Experimentata et Applicata 131, 11–19.CrossRefGoogle Scholar
Rivers, D.B. (2004) Evaluation of host responses as means to assess ectoparasitic pteromalid wasp's potential for controlling manure-breeding flies. Biological Control 30, 181–192.CrossRefGoogle Scholar
Rivers, D.B. (2007) Host responses to envenomation by ectoparasitic wasps as predictive indicators of biological control of manure breeding flies. pp. 161–178in Rivers, D.B. & Yoder, J.A. (Eds) Recent Advances in the Biochemistry, Toxicity, and Mode of Action of Parasitic Wasp Venoms. Kerala, India, Research Signposts.Google Scholar
Rivers, D.B. & Denlinger, D.L. (1995) Fecundity and development of the ectoparasitoid Nasonia vitripennis are dependent upon the host nutritional and physiological condition. Entomologia Experimentalis et Applicata 76, 15–24.CrossRefGoogle Scholar
Rivers, D.B., Ciarlo, T., Spelman, M. & Brogan, R. (2010) Changes in development and heat shock protein expression in two species of flies (Sarcophaga bullata [Diptera: Sarcophagidae] and Protophormia terraenovae [Diptera: Calliphoridae] reared in different sized maggot masses. Journal of Medical Entomology 47, 677–689.CrossRefGoogle ScholarPubMed
Roback, S.S. (1951) A classification of the muscoid calyptrate Diptera. Annals of the Entomological Society of America 44, 327–361.CrossRefGoogle Scholar
Rodriguez, W.C. & Bass, W.M. (1985) Decomposition of buried bodies and methods that may aid in their location. Journal of Forensic Science 30, 836–852.CrossRefGoogle ScholarPubMed
Rohlfs, M. & Hoffmeister, T.S. (2004) Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies? Oecologia 140, 654–661.CrossRefGoogle ScholarPubMed
Sandeman, R.M., Feehan, J.P., Chandler, R.A. & Bowles, V.M. (1990) Tryptic and chymotryptic proteases released by larvae of the blowfly, Lucilia cuprina. International Journal of Parasitology 20, 1019–1023.CrossRefGoogle ScholarPubMed
Saunders, D. & Bee, A. (1995) Effects of larval crowding on size and fecundity of the blowfly Calliphora vicina (Diptera: Calliphoridae). European Journal of Entomology 92, 615–622.Google Scholar
Scheiring, J.F., Davis, D.G., Ranasinghe, A. & Teare, C.A. (1984) Effects of larval crowding on life history parameters in Drosophila melanogaster Meigen (Diptera: Drosophilidae). Experimental Gerontology 77, 329–332.Google Scholar
Schmidt-Nielsen, K. (1964) Desert Aanimals: Physiological Problems of Heat and Water. Oxford, UK, Clarendon Press.Google Scholar
Schmidt-Nielsen, K. (1997) Animal Physiology: Adaptation and Environment. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Slone, D.H. & Gruner, S.V. (2007) Thermoregulation in larval aggregations of carrion-feeding blow flies (Diptera; Calliphoridae). Journal of Medical Entomology 44, 516–523.CrossRefGoogle ScholarPubMed
Smith, K.G.V. (1986) A Manual of Forensic Entomology. London, UK, London and Cornell University Press.Google Scholar
So, P.-M. & Dudgeon, D. (1990) Interspecific competition among larvae of Hemipyrellia ligurriens (Calliphoridae) and Boettcherisca formosensis (Sarcophagidae) (Diptera). Research in Population Ecology 32, 337–348.CrossRefGoogle Scholar
Sørensen, J.G. & Loeschcke, V. (2001) Larval crowding in Drosophila melanogaster induces Hsp70 expression, and leads to increased adult longevity and adult thermal stress resistance. Journal of Insect Physiology 47, 1301–1307.CrossRefGoogle ScholarPubMed
Storey, K.B. (2004) Biochemical adaptation. pp. 383–414in Storey, K.B. (Ed.) Functional Metabolism: Regulation and Adaptation. Hobocken, NJ, USA, Wiley-Liss.CrossRefGoogle Scholar
Terra, W.R. & Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology B 109, 1–62.CrossRefGoogle Scholar
Tomberlin, J.K. (2008) Arthropods associated with decomposing remains. pp. 40–70in Haskell, N.H. & Williams, R.E. (Eds) Entomology & Death: A Procedural Guide. Clemson, SC, USA, Forensic Entomology Partners.Google Scholar
Turchetto, M. & Vanin, S. (2004) Forensic evaluations on a crime scene with monospecific necrophagous fly population infected by two parasitoid species. Aggrawal's International Journal of Forensic Medicine and Toxicology 5, 12–18.Google Scholar
Turner, B. & Howard, T. (1992) Metabolic heat generation in dipteran larval aggregations: a consideration for forensic entomology. Medical and Veterinary Entomology 6, 179–181.CrossRefGoogle ScholarPubMed
Ullyett, G.C. (1950) Competition for food and allied phenomena in sheep blowfly populations. Philosophical Transactions of the Royal Society of London, Series B 234, 77–175.Google Scholar
Villet, M.H., MacKenzie, B. & Muller, W.J. (2006) Larval development of the carrion-breeding flesh fly, Sarcophaga (Liosarcophaga) tibialis Macquart (Diptera: Sarcophagidae), at constant temperatures. African Entomology 14, 357–366.Google Scholar
Villet, M.H., Richards, C.S. & Midgley, J.M. (2010) Contemporary precision, bias and accuracy of minimum post-mortem intervals estimated using development of carrion-feeding insects. pp. 109–137in Amendt, J., Campobasso, C.P., Goff, M.L. & Grassberger, M. (Eds) Current Concepts in Forensic Entomology. London, UK, Springer.Google Scholar
Voss, S.C., Spafford, H. & Dadour, I.R. (2009) Hymenopteran parasitoids of forensic importance: host associations, seasonality and prevalence of parasitoids of carrion flies in Western Australia. Journal of Medical Entomology 46, 1210–1219.CrossRefGoogle ScholarPubMed
Waterhouse, D.F. (1947) The relative importance of live sheep and of carrion as breeding grounds for the Australian sheep blowfly Lucilia cuprina. CSIRO Bulletin 217.Google Scholar
Wertheim, B., Vet, L.E.M. & Dicke, M. (2003) Increased risk of parasitism as ecological costs using aggregation pheromones: laboratory and field study of Drosophila-Leptopilina interaction. Oikos 100, 269–282.CrossRefGoogle Scholar
Whiting, A. (1967) The biology of the parasitic wasp Mormoniella vitripennis. Quarterly Review of Biology 42, 333–406.CrossRefGoogle Scholar
Wigglesworth, V.B. (1967) The Principles of Insect Physiology. London, UK, Methuen.Google Scholar
Williams, H. & Richardson, A.M.M. (1983) Life history responses to larval food shortages in four species of necrophagous flies (Diptera: Calliphoridae). Australian Journal of Ecology 8, 257–263.CrossRefGoogle Scholar
Williams, H. & Richardson, A.M.M. (1984) Growth energetics in relation to temperature for larvae of four species of necrophagous flies (Diptera: Calliphoridae). Australian Journal of Ecology 9, 141–152.CrossRefGoogle Scholar
Willmer, P., Stone, G. & Johnston, I. (2000) Environmental Physiology of Animals. Oxford, UK, Blackwell Science Ltd.Google Scholar
Withers, P.C. (1992) Comparative Animal Physiology. New York, USA, Saunders College Publishing.Google Scholar
Yocum, G.D., Zdarek, J., Joplin, K.H., Lee, R.E. Jr, Smith, D.C., Manter, K.D. & Denlinger, D.L. (1994) Alteration of the eclosion rhythm and eclosion behaviour in the flesh fly, Sarcophaga crassipalpis, by low and high temperature stress. Journal of Insect Physiology 40, 13–21.CrossRefGoogle Scholar
Yoder, J.A., Benoit, J.B., Denlinger, D.L. & Rivers, D.B. (2006) Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata Parker (Diptera: Sarcophagidae): Evidence indicating anti-desiccant and cyroprotectant functions for this polyol during aseasonal stress. Journal of Insect Physiology 52, 202–214.CrossRefGoogle Scholar
Young, A.R., Meeusen, E.N.T. & Bowles, V.M. (1996) Characterization of ES products involved in wound initiation by Lucilia cuprina larvae. International Journal of Parasitology 26, 245–252.CrossRefGoogle ScholarPubMed
Zdárek, J. & Sláma, K. (1972) Supernumerary larval instars in cyclorrhaphous Diptera. Biological Bulletin 142, 350–357.CrossRefGoogle ScholarPubMed
Zwaan, B.J., Bijlsma, R. & Hoekstra, R.F. (1991) On the developmental theory of ageing. I. Starvation resistance and longevity in Drosophila melanogaster in relation to pre-adult breeding conditions. Heredity 66, 29–39.CrossRefGoogle ScholarPubMed