Literature Review of Parasitoids of Filth Flies in Thailand: a List of Species with Brief Notes on Bionomics of Common Species

Southeast Asian J Trop Med Public Health

LITERATURE REVIEW OF PARASITOIDS OF FILTH FLIES IN THAILAND: A LIST OF SPECIES WITH BRIEF NOTES ON BIONOMICS OF COMMON SPECIES

Chamnarn Apiwathnasorn

Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand

Abstract. We reviewed the literature for surveys of parasitoid of filth flies in Thai- land. We found 5 families, with 9 genera and 14 species identified in Thailand. We describe the ecological niches and biology of common species, including Spalangia cameroni, S. endius, S. nigroaenea and Pachycrepoideus vindemmiae. Keywords: pupal parasitoids, synanthropic flies, garbage dump, Thailand

INTRODUCTION are among the most important and common natural enemies of filth flies associ- Human activities produce large quan- ated with animals and humans (Rutz tities of organic waste suitable as breeding and Patterson, 1990). Parasitoids are of sites for calyptrate fly species. Synan- interest due to the emergence of pesticide thropic flies and their association with resistance among fly populations and a unsanitary conditions are important for growing demand by the public for more public health reasons since they may be environmentally safe methods of control carriers of enteric pathogens (Greenberg, (Meyer et al, 1987; Scott et al, 1989; Cilek 1971; Olsen, 1998; Graczyk et al, 2001; Ber- and Greene, 1994; Legner, 1995). Bio- nard, 2003, Banjo et al, 2005). During their logical control includes release of natural lifecycle, flies are exposed to a wide range enemies into the ecosystem to reduce fly of natural enemies (Legner and Brydon, populations to below annoyance levels. 1966; Morgan et al, 1981; Axtell, 1986). Thai hymenopterous parasitoids of filth There are 23 hymenopterous parasitoids, flies have received little attention. They insects that are parasitic only during im- have been the subject of investigations mature stages and eventually kills their since 1978. Information about their diver- hosts (Jenkins, 1960). Pupal stages often sity, distribution, host ranges and extent represent less than 1% of the total eggs in different habitats which fly populations deposited by the previous generation of are suppressed has yet to be determined flies (Jenkins, 1960). Pupal parasitoids for these natural parasitoids to be integrated into fly control programs. No at- Correspondence: Chamnarn Apiwathnasorn, Department of Medical Entomology, Faculty tempt has yet been made to use them for of Tropical Medicine, Mahidol University, 420/6 fly control. Therefore, we reviewed the Ratchawithi Road, Bangkok 10400, Thailand. litterature surveyed filth fly parasitoids in Tel: 66 (0) 2306 9177; Fax: 66 (0) 2643 5582 Thailand and neighboring areas to better E-mail: [email protected] understand their niche characteristics in

48 Vol 43 No. 1 January 2012 Parasitoids of Filth Flies in Thailand order to assist in identification, selection sitoids that emerged from or died in the and the process of matching candidate puparia. The emerged parasitoids were parasitoid species with filth fly habitats. preserved in 70% ethyl alcohol for species determination based on the key of Boucek MATERIALS AND METHODS (1963) with subsequent species confirma- tion made by Dr Zdenek Boucek [Depart- The information presented here was ment of Entomology, the British Museum derived from four postgraduate disserta- (Natural History), United Kingdom]. tions at Mahidol University (Pichayakul, 1978; Apiwathnasorn, 1979; Pratchyan- RESULTS usorn, 1981; Samung, 2000) of parasitoid biology and diversity. The list of parasit- A total of approximately 16,000 pupal oids was obtained from a 1-year survey specimens of flies were obtained from of native parasitoids of filth flies breeding municipal garbage dumps comprising in municipal garbage dumping areas of representatives of only 2 fly species,Musca 31 provinces of Thailand: Ang Thong, domestica (Linnaeus) and Chrysomya mega- Bangkok, Chachoengsao, Chanthaburi, cephala (Fabricius). Chiang Mai, Chon Buri, Chumphon, Kalasin, Kanchanaburi, Khon Kaen, Lam- Fourteen parasitoid species of filth pang, Maha Sarakham, Nakhon Pathom, flies have been reported in Thailand. They Nakhon Ratchasima, Nakhon Si Tham- occur in two orders: Coleoptera (1 species) marat, Narathiwat, Nong Khai, Pattani, and Hymenoptera (13 species) compris- Phayao, Ratchaburi, Rayong, Roi Et, ing 5 families: Chalcididae, Diapriidae, Sakon Nakhon, Samut Prakan, Saraburi, Encyrtidae, Pteromalidae and Scelionidae. Si Sa Ket, Suphan Buri, Surin, Trat, Ubon Spalangia endius was the most widely Ratchathani and Udon Thani (Apiwath- distributed, found in 85.3% of collection nasorn, 1979). The dumping areas each sites, followed by S. nigroaenea (44.1%), occupied an area of 1.0 hectare and were Pachyerepoideus vindemmiae (23.5%), Di- located at least 10 km from their respec- rhinus crythocerus (8.8%), S. cameroni, S. tive city centers in scrublands, forests, gemina and Trichopria sp (5.9%) and less fruit orchards along rivers or roadsides. than 3.0% for the rest. Several species Most garbage dumps consisted of refuse were distinguished easily but some were from households, and included fecal mat- rare and presented identification difficul- ters, organic residue and decomposed ties; for instance, specimens in the Family carcasses. Viable fly puparia were hand Diapriidae and Scelionidae could not be collected with forceps in 4 to 7 day old identified to the species level. A checklist garbage heaps. Parasitism was observed of pupal parasitoids of filth-breeding flies in the laboratory at room temperature in Thailand with their classification is after the collected pupae were sorted compiled in Table 1. and allowed to complete development of It was remarkable that S. endius alone or the parasitoids and identification of the a combination of S. endius and S. nigroaenea fly species. The percent parasitism was accounted for the majority of the observed calculated by dividing the total number parasitization at most localities. The only of pupae that produced either a fly or a beetle, Aleochara trivialis was collected parasitoid by the total number of para- from M. domestica pupae at 3.0% of sites.

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Table 1 List of pupal parasitoids of filth flies in Thailand.

Order Hymenoptera Family Chalcididae Species Brachymeria minuta (Linnaeus) Dirhinus crythrocerus Cameron Dirhinus excavatus Dalman Family Diapriidae Species Psilus Panzer sp Trichopria Ashmead sp Family Encyrtidae Species Exoristobia philippinensis Ashmead Family Pteromalidae Species Pachycrepoideus vindemmiae (Rondani) Spalangia cameroni Perkins Spalangia endius Walker Spalangia gemina Boucek Spalangia nigroaenea Curtis Spalangia sp A (unidentifiable species) Family Scelionidae Species Teleas Latreille sp

Order Coleoptera Family Staphylinidae Species Aleochara trivialis Kraatz

Table 2 Biological summary on common species of hymenopterous fly parasitoids.

Species Life cycle Male: Percentage Host Reference (day) female parasitization

D. crythrocerus 22 1:2.0 80.0 M. domestica Pratchyanusorn, 1981 P. vindemmiae 21 1:1.5 40.1 M. domestica Samung, 2000 S. endius 20 1:4.3 42.5 M. domestica Pichayakul, 1978

Table 2 summarizes the laboratory ratio are fundamental factors determining biology of some common hymenopter- parasitoid potential as a control agent for ous parasitoids of Thailand. S. endius has synanthropic flies. the potential of being a biological control agent against field populations of M. do- DISCUSSION mestica.The results demonstrate develop- mental period, parasitization rate and sex Rueda et al (1997) and Sulaiman et al

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(1998) found the predominant species of maggots (West, 1951). However, garbage flies at garbage dumps wereC. megacephala dumps in Lampang and Phayao Provinces and M. domestica. The parasitization rates were treated by burning and the pupation varied widely from 0 to 55%. The extent to sites were found at a depth of 6 cm below which fly populations are suppressed by the ash soil surface. The parasitization indigenous parasitoids is difficult to de- rates were approximately 33% with 3 termine (Simmonds, 1948), but the results parasitoid species (S. cameroni, S. endius, from several studies indicate parasitoids S. nigroaenea) involved. This aggress with play a significant role in suppression of the observations by Legner (1977) and house fly populations (Legner and Bry- Rueda and Axtell (1985b) that these 3 don, 1966; Legner and Greathead, 1969). species and P. vindemiae are more effective Various field investigations have also at locating buried pupal hosts at various shown parasitism rates vary in different depths of up to 10 cm. fly breeding habitats (Petersen and Meyer, Although S. endius and S. nigroaenea 1983; Rueda and Axtell, 1985a; Smith and were found to co-exist on M. domestica Rutz, 1991a). Moisture and light levels throughout the collection sites, S. endius is can affect microhabitat choices made by usually most abundant in xerophilic habi- species of parasitoids (Smith and Rutz, tats and S. nigroaenea is found principally 1991b; Geden, 1999). in temperate humid habitats (Legner and Although 14 species of pupal para- Brydon, 1966). B. minuta, D. crythrocerus, stioids are reported in this paper, it can E. philippinensis, P. vindemmiae, S. endius be expected that single-sample surveys and S. nigroaenea were recovered from may find undiscovered parasitoid species. laboratory colonies of C. megacephala, S. endius and S. nigroaenea accounted for M. domestica and Parasarcophaga orchidae the majority of observed parasitization at maintained at the Department of Medical most localities, possibly owing to the dis- Entomology; P. vindemmiae was also found tribution of the parasitoids. Muscidifurax parasitizing the oothecae of cockroaches. species has been reported to disperse and E. philippinensis was found to infect the parasitize to distances of 8-100 m from the pupae of flesh flies, Boettcherisca nathani release point (Tobin and Pitts, 1999; Floate and B. peregrina. This observation needs et al, 2000), but female S. cameroni rarely further investigation to determine its po- disperse more than 3 m (Skovgard, 2002). tential as a biological agent for controlling Many species of Aleochara are natu- synanthropic flies. ral enemies of dung-breeding flies, with Gek-Huang and Kailok (1972) dem- adults that prey on fly eggs and maggots onstrated under laboratory conditions E. and larvae that parasitize the puparium philippinensis has several good qualities (Fraenkel and Bhaskaran, 1973). They as a biological control agent for synan- prefer fresh dung and generally parasitize thropic flies, including short life cycle of more than one host species (Klimaszew- two weeks, high fecundity, high female ski, 1984). sex ratio (1:6.6) and non-host specificity. Based on field observations, most However, under field observations E. maggots pupated in clusters on the upper philippinensis had a relatively poor ability layer of garbage, which could be because to reach the buried pupae in contrast to the fermentation heat in the inner part other Spalangia species. of the garbage inhibited development of Regarding the field application of a

Vol 43 No. 1 January 2012 51 Southeast Asian J Trop Med Public Health pupal parasitoid to control filth fly popu- Poultry Sci 1986; 65: 657-67. lations, Spalangia is the most important Banjo AD, Lawal OA, Adeduji OO. Bacteria genera for biological control of house and fungi isolated from house fly (Musca and stable flies (Geden, 2006). S. endius domestica L.) larvae. Afr J Biotechnol 2005; was used in mass releases to suppress 4: 780-4. fly populations by Legner and Brydon Bernard DR. Control of fly-borne diseases. (1966) and Morgan et al (1981). Sangeetha Pesticide Outlook 2003; 14: 222-8. and Jebanesan (2010) demonstrated S. Boucek Z. A study of Spalangia Latr. (Hymenop- cameroni and S. endius were the most ef- tera, Chalcidoidea). Acta Entomol Mus Nat ficient parasitoids againstM. domestica for Pragae 1963; 35: 429-512. biological control. More emphasis should Cilek JE, Greene GL. Stable fly (Diptera: Musci- be placed on biological study and use of dae) insecticide resistance in Kansas cattle the hymenopterous parasitoids for filth feedlots. J Econ Entomol 1994; 87: 275-79. fly integrated control. Fraenkel G, Bhaskaran G. Pupariation and pu- In conclusion, the present paper pro- pation in cyclorrhaphous flies (Diptera): terminology and interpretation. Ann En- vides information about diversity and tomol Soc Am 1973; 66: 418-22. prevalence of naturally occurring parasi- Floate KD, Coghlin P, Gibson GAP. Dispersal toids found parasitizing pupae of filth of the filth fly parasitoid Muscidifurax flies inhabiting garbage dumps. Three raptorellus (Hymenoptera: Pteromalidae) species were common in the collection following mass releases in cattle confine- sites; some species always parasitize labo- ments. Biol Control 2000; 18:172-8. ratory colonies of flies. More species may Geden CJ. Host location by house fly parasit- be added to this list in the future if more oids (Hymenoptera: Pteromalidae and extensive surveys are carried out. S. endius Chalcididae) in poultry manure at dif- and S. nigroaenea are promising candidates ferent moisture levels and host densities. for inundative biological control of filth Environ Entomol 1999; 18: 755-60. flies in Thailand. Geden CJ. Biological control of pests in livestock production. In: Hansen LS, Enkegaard A, ACKNOWLEDGEMENTS Steenberg T, Ravnskov S, Larsen J, eds. Implementation of biocontrol in practice I wish to extend my sincere thanks in temperate regions–present and near to Dr Zdenek Boucek, Department of En- future. Flakkebjerg, Denmark: Proceedings tomology, The Natural History Museum, of the International Workshop at Research England, for his kind assistance in con- Centre, 2006: 45-60. firming the identification of hymenopter- Gek-Huang AS, Kailok C. Exoristobia philip- ous parasitoids. pinensis Ashmead (Hymenoptera: Encyr- tidae) as a biological agent for the control REFERENCES of synanthropic flies. Singapore: The Southeast Asian Ministers of Education Apiwathanasorn C. Surveys of hymenopter- Organization, Tropical Medicine and Pub- ous parasitoids of medically important lic Health (SEAMEO TROPMED), Vector flies found breeding in garbage heaps in Control Workshop, 1972: 8 pp. Thailand. Bangkok: Mahidol University, Greenberg B. Flies and disease. Vol 1. Ecology, 1979. 100 pp. MS thesis. classification and biotic associations. New Axtell RC. Fly management in poultry produc- Jersey: Princeton University Press, 1971: tion: cultural, biological and chemical. 896 pp.

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