Predatory behavior of Synthesiomyia nudiseta larvae (Diptera: Muscidae) on several necrophagous blowfly species (Diptera: Calliphoridae)
Abstract
Intraguild interactions play a prominent role in sarcosaprophagous communities, so intraspecific and interspecific competition phenomena between fly larvae take place. Synthesiomyia nudiseta is a species that has recently been recorded on human corpses in Europe, and it has been cited in forensic cases in Spain and Italy. The mature larvae are known to be facultative predators on necrophagous fly larvae, but their role as predators is unknown. The aim of this paper is to investigate the predatory behavior of S. nudiseta on the most abundant blowfly larvae in sarcosaprophagous communities in southwestern Europe (i.e., Chrysomya albiceps, Lucilia sericata, and Calliphora vicina). Intraspecific and interspecific competition experiments were carried out to study the effect of this species in the necrophagous diptera community. First-instar larvae were placed in plastic cups with the same amount of pig liver (15 g) at different densities (50, 100, 150, and 300 individuals/cup). Mortality in blowflies increased when S. nudiseta larvae were present: up to 98.40% in Ch. albiceps, 89.60% in L. sericata, and 84.93% in C. vicina. Pre-imaginal developmental time and adult wing size were analyzed and compared under each of the intraspecific and interspecific conditions; both variables were affected by competition in all cases. The implications of the presence of S. nudiseta for sarcosaprophagous community dynamics and its effect on the estimation of postmortem interval (PMI) are discussed.
Keywords
Calliphora vicina Chrysomya albiceps Lucilia sericata Synthesiomyia nudiseta Intraspecific competition Interspecific competitionNotes
Acknowledgments
This work belongs to Tania Ivorra PhD and was partially supported by the projects GV/2011/039 (Generalitat Valenciana) and GRE09-27 (University of Alicante). We are very grateful to F.J. Jiménez, S. García, and A. González for their help in the maintenance of colonies and with the laboratory experiments in this work.
References
- 1.James MT (1947) The flies that cause myiasis in man. Misc Pub US Dept Agric 631:1–182Google Scholar
- 2.Cole FR (1969) The flies of western North America. University of California Press, Berkeley, CA 694 ppGoogle Scholar
- 3.Greenberg B (1991) Flies as forensic indicators. J Med Entomol 28:565–577CrossRefGoogle Scholar
- 4.Velásquez Y, Ivorra T, Grzywacz A, Martínez-Sánchez A, Magaña C, García-Rojo A, Rojo S (2013) Larval morphology, development and forensic importance of Synthesiomyia nudiseta (Diptera: Muscidae) in Europe: a rare species or just overlooked? Bull Entomol Res 103:98–110CrossRefGoogle Scholar
- 5.Wells JD, Greenberg B (1994) Resource use by an introduced and native carrion flies. Oecologia 99:181–187CrossRefGoogle Scholar
- 6.Segura NA, Usaquén W, Sánchez MC, Chuaire L, Bello F (2009) Succession pattern of cadaverous entomofauna in a semi-rural area of Bogotá, Colombia. Forensic Sci Int 187:66–72CrossRefGoogle Scholar
- 7.Bowden J (1997) Synthesiomyia nudiseta (Wulp) (Dipt., Muscidae) in Europe. Entomologist’s Monthly Magazine 133: 224Google Scholar
- 8.Lo Pinto S, Giordani G, Tuccia F, Ventura F, Vanin S (2017) First records of Synthesiomyia nudiseta (Diptera: Muscidae) from forensic cases in Italy. Forensic Sci Int 276:e1–e7CrossRefGoogle Scholar
- 9.Siddons LB, Roy DN (1942) On the life history of Synthesiomyia nudiseta van der Wulp (Diptera, Muscidae), a myiasis-producing fly. Parasitology 34:239–245CrossRefGoogle Scholar
- 10.Skidmore P (1985) The biology of the Muscidae of the world. Springer Science & Business Media, BerlinGoogle Scholar
- 11.Byrd JH, Castner JL (2001) Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, Boca Raton, 681 ppGoogle Scholar
- 12.Kumara TK, Hassan AA, Che-Salmah MR, Bhupinder S (2009) Larval growth of the muscid fly, Synthesiomyia nudiseta (Wulp), a fly of forensic importance, in the indoor fluctuating temperatures of Malaysia. Trop Biomed 26:200–205Google Scholar
- 13.Fuller ME (1934) The insect inhabitants of carrion: A study in animal ecology. Bulletin of the Council for Scientific and Industrial Research, Australia (82), 62 ppGoogle Scholar
- 14.Baumgartner DL (1993) Review of Chrysomya rufifacies (Diptera: Calliphoridae). J Med Entomol 30:338–352CrossRefGoogle Scholar
- 15.Omar AH (1995) Cannibalism and predation behaviour of the blowfly, Chrysomya albiceps (Wiedemann) larvae (Diptera: Calliphoridae). J Egypt Soc Parasitol 25:729–743Google Scholar
- 16.Faria LDB, Orsi L, Trinca LA, Godoy WAC (1999) Larval predation by Chrysomya albiceps on Cochliomyia macellaria, Chrysomya megacephala and Chrysomya putoria. Entomol Exp Appl 90:149–155CrossRefGoogle Scholar
- 17.Faria LDB, Godoy WAC (2001) Prey choice by facultative predator larvae of Chrysomya albiceps (Diptera: Calliphoridae). Mem Inst Oswaldo Cruz 96:875–878CrossRefGoogle Scholar
- 18.Faria LDB, Godoy WAC, Reis SF (2004) Larval predation on different instars in blowfly populations. Braz Arch Biol Technol 47:887–894CrossRefGoogle Scholar
- 19.Reigada C, Godoy WAC (2005) Dispersal and predation behavior in larvae of Chrysomya albiceps and Chrysomya megacephala (Diptera: Calliphoridae). J Insect Behav 18:543–555CrossRefGoogle Scholar
- 20.Rosa GS, De Carvalho LR, Dos Reis SF, Godoy WAC (2006) The dynamics of intraguild predation in Chrysomya albiceps Wied. (Diptera: Calliphoridae): interactions between instars and species under different abundances of food. Neotrop Entomol 35:775–780CrossRefGoogle Scholar
- 21.Faria LDB, Reigada C, Trinca LA, Godoy WAC (2007) Foraging behaviour by an intraguild predator blowfly, Chrysomya albiceps (Diptera: Calliphoridae). J Ethol 25:287–294CrossRefGoogle Scholar
- 22.Brundage AL, Benbow ME, Tomberlin JK (2014) Priority effects on the life-history traits of two carrion blow fly (Diptera, Calliphoridae) species. Ecol Entomol 39:539–547CrossRefGoogle Scholar
- 23.Smith KE, Wall R (1997) Asymmetric competition between larvae of the blowflies Calliphora vicina and Lucilia sericata in carrion. Ecol Entomol 22:468–474CrossRefGoogle Scholar
- 24.Martínez-Sánchez A (2003) Biología de la comunidad de Dípteros necrófilos en ecosistemas del sureste de la península Ibérica. PhD Dissertation. Alicante, University of AlicanteGoogle Scholar
- 25.Martínez-Sánchez A, Marcos-García MA, Rojo S (2005) Biodiversidad de la comunidad de dípteros sarcosaprófagos en ambientes insulares del sudeste Ibérico (Diptera, Calliphoridae, Muscidae, Sarcophagidae). Nouvelle Revue d'Entomologie 22:251–265Google Scholar
- 26.Hanski I, Kuusela S (1977) An experiment on competition and diversity in the carrion fly community. Ann Zool Fennici 43:108–115Google Scholar
- 27.Wells JD, Greenberg B (1992) Interaction between Chrysomya rufifacies and Cochliomyia macellaria (Diptera, Calliphoridae) – the possible consequences of an invasion. Bull Entomol Res 82:133–137CrossRefGoogle Scholar
- 28.Benbow ME, Tomberlin JK, Tarone AM (2015) Carrion ecology, evolution, and their applications. CRC Press, Boca RatonCrossRefGoogle Scholar
- 29.Ullyett GC (1950) Competition for food and allied phenomena in sheep blowfly populations. Philos Trans R Soc Lond Ser B Biol Sci 234(B):77–174Google Scholar
- 30.Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
- 31.Polis GA, Myers CA (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330CrossRefGoogle Scholar
- 32.Smith KGV (1986) A manual of forensic entomology. Ithaca, British museum (natural history), London, and. Cornell University Press, IthacaGoogle Scholar
- 33.Erzinçlioğlu Z (1996) Blowflies. Richmond Publishing Company, RichmondGoogle Scholar
- 34.Mackerras MJ (1933) Observations on the life-histories, nutritional requirements and fecundity of blowflies. Bull Entomol Res 24:353–362CrossRefGoogle Scholar
- 35.Carter DO, Tomberlin JK, Benbow ME, Metcalf JL (2017) Forensic microbiology. Wiley Edition, HobokenCrossRefGoogle Scholar
- 36.Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University PressGoogle Scholar
- 37.Ludoški J, Djurakic D, Pastor B, Martínez-Sánchez A, Rojo S, Milankov V (2014) Phenotypic variation of the housefly, Musca domestica: amounts and patterns of wing shape asymmetry in wild populations and laboratory colonies. Bull Entomol Res 104:35–47CrossRefGoogle Scholar
- 38.Gobbi P, Martínez-Sánchez A, Rojo S (2013) The effects of larval diet on adult life-history traits of the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). Eur J Entomol 110:461–468CrossRefGoogle Scholar
- 39.Dujardin JP, Slice DE (2006) Contributions of Morphometrics to medical entomology. In: Ostroff SM (ed) (2008)Encyclopedia of infectious diseases: Modern Methodologies. John Wiley & Sons, Hoboken, pp 435–447Google Scholar
- 40.Grzywacz A, Ogiela J, Tofilski A (2017) Identification of Muscidae (Diptera) of medico-legal importance by means of wing measurements. Parasitol Res 116:1495–1504CrossRefGoogle Scholar
- 41.Jiménez-Martín FJ (2017) Morfometría Geométrica alar para la identificación de dípteros de importancia forense (Calliphoridae) de la Península Ibérica. M.S. Thesis. Madrid, Universidad Complutense de MadridGoogle Scholar
- 42.Grzywacz A, Hall MJR, Pape T, Szpila K (2017) Muscidae (Diptera) of forensic importance – an identification key to third instar larvae of the western Palearctic region and a catalogue of the muscid carrion comunity. Int J Legal Med 131:855–866CrossRefGoogle Scholar
- 43.Lee HL, Krishnasamy M, Abdullah AG, Jeffery J (2004) Review of forensically important entomological specimens in the period of 1972-2002. Trop Biomed 21:69–75Google Scholar
- 44.Benbow ME, Lewis AJ, Tomberlin JK, Pechal JL (2013) Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol 50:440–450CrossRefGoogle Scholar
- 45.Tomberlin JK, Mohr R, Benbow ME, Tarone AM, VanLaerhoven S (2011) A roadmap for bridging basic and applied research in forensic entomology. Annu Rev Entomol 56:401–442CrossRefGoogle Scholar
- 46.Rabinovich JE (1970) Vital statistics of Synthesiomyia nudiseta (Diptera: Muscidae). Ann Entomol Soc Am 63:749–752CrossRefGoogle Scholar
- 47.Krüger RF, Ribeiro PB, Carvalho CJB, Costa PRP (2002) Desenvolvimento de Synthesiomyia nudiseta (Diptera, Muscidae) em laboratório. Iheringia Ser Zool 92:25–30CrossRefGoogle Scholar
- 48.Queiroz MMC (1991) Aspectos da Bioecologia de Chrysomya albiceps (Wiedemann, 1819) (Diptera, Calliphoridae), em condições de laboratório. PhD Dissertation. Rio de Janeiro, Universidade Federal Rural do Rio de JaneiroGoogle Scholar
- 49.Reid CLM (2012) The role of community composition and basal resources in a carrion community. M.S. thesis. University of WindsorGoogle Scholar
- 50.Flores M (2013) Life-history traits of Chrysomya rufifacies (Macquart) (Diptera: Calliphoridae) and its associated non-consumptive effects on Cochliomyia macellaria (Fabricius) (Diptera: Calliphoridae) behaviour and development. PhD Dissertation. Texas A&M UniversityGoogle Scholar
- 51.Anderson GS (2000) Minimum and maximum development rates of some forensically important Calliphoridae (Diptera). J Forensic Sci 45:824–832CrossRefGoogle Scholar
- 52.Marchenko MI (2001) Medicolegal relevance of cadaver entomofauna for the determination of the time of death. Forensic Sci Int 120:89–109CrossRefGoogle Scholar
- 53.Martínez-Sánchez A, Smith KE, Rojo S, Marcos-García MA, Wall R (2007) Geographic origin affects larval competitive ability in European populations of the blow fly, Lucilia sericata. Entomol Exp Appl 122:93–98CrossRefGoogle Scholar
- 54.Calderón-Arguedas O, Troyo A, Solano ME (2005) Larval quantification of Synthesiomyia nudiseta (Diptera: Muscidae) as a criterion in analysis of the post-mortem interval in an experimental model. Parasitol Lationam 60:138–143Google Scholar
- 55.D’Almeida JM, Garcia-Piana ML, Tebaldi-Selem C (1997) Comportamento reprodutivo de Synthesiomyia nudiseta (Diptera: Muscidae) sob condições de laboratório. Mem Inst Oswaldo Cruz 92:563–564CrossRefGoogle Scholar
- 56.Cianci TJ, Sheldon JK (1990) Endothermic generation by blowfly larvae Phormia regina developing in pig carcasses. Bulletin of the Society of Vector. Ecology 15:33–40Google Scholar