diptera as predators and parasitoids of terrestrial ... · the nematocera include generally small,...

Diptera as Predators and ParasitoidsJ.B. Coupland and G.M. Barker

3 Diptera as Predators andParasitoids of TerrestrialGastropods, with Emphasison Phoridae, Calliphoridae,Sarcophagidae, Muscidae andFanniidae

JAMES B. COUPLAND1 AND GARY M. BARKER2

1Science Research Foundation, University Gate East, Park Row,Bristol BS1 5UB, UK; 2Landcare Research, Private Bag 3127, Hamilton,New Zealand

Introduction

The Diptera (true flies) is one of the most species-rich clades of insects,and includes many familiar insects such as house-flies, blow-flies,black-flies, midges, fruit-flies and mosquitoes. Diptera probably arose inthe Permian, as the main lineages are known from Upper Triassic depositsof the Mesozoic period (Evenhuis, 1994). The estimated 125,000described extant species represent about one half of the probable globalspecies diversity in the order (Yeates and Wiegmann, 1999). That thisdiversity has been classified into at least 130 families is indicative of thelong evolutionary history and diversification in Diptera. Primarily, adultflies feed on nectar and pollen, and their larvae are detritivores in aquaticand semi-aquatic environments (McAlpine et al., 1981, 1987; Ferrar,1987; Colless and McAlpine, 1991). However, the Diptera have becomeremarkably diverse ecologically, with some diversification in adultfeeding behaviours (such as haemophagy in various Psychodoidea,Culicoidea, Tabanoidea, Empidoidea and Calyptratae), but, more signifi-cantly, a great range of media are utilized for development of the larvalstages. A great many Diptera have adopted a carnivorous predatory orparasitoid life strategy in the larval stage. Askew (1971, p. 186) notes that‘although the parasitic Diptera are not quite so biologically diverse as theparasitic Hymenoptera, their hosts come from more animal groups. Otherinsects are the most usual hosts, but slugs, earthworms, snails, centipedesand spiders are also attacked . . .’. Eggleton and Belshaw (1992)

CAB International 2004. Natural Enemies of Terrestrial Molluscs(ed. G.M. Barker) 85

85A4784 - Barker - First Revise VP10 DA #G.prnZ:\Customer\CABI\A4743 - Barker\A4784 - Barker - First Revise VP10 DA #G.vpTuesday, May 18, 2004 11:55:49 AM

Color profile: DisabledComposite 150 lpi at 45 degrees

recognized parasitoids in 21 families of Diptera, and Feener and Brown(1997) estimate that the Diptera account for 16,000 described species orabout 20% of all known parasitoids.

The Diptera feeding on gastropods can be divided biologically intothree groups: (i) saprophages, feeding on the bodies of dead gastropods;(ii) epizoic forms feeding on the body secretions of living gastropods, butnot killing them; (iii) parasitoids and predators, which kill one or moregastropods during their development. It is the epizoic, predatory andparasitoid forms that are of interest here. While the family Sciomyzidaehas held the limelight as being the dipteran family most closelyassociated with molluscs and thus most interesting from the viewpoint ofbiological control, several other families have also exploited gastropodMollusca as a resource, albeit mainly in terrestrial environments. Thischapter focuses on these non-sciomyzid dipteran associates of molluscs,namely Phoridae, Sarcophagidae, Calliphoridae, Muscidae andFanniidae. The Sciomyzidae are specifically addressed in the nextchapter of this volume.

Features of Diptera, and Emergence of the MalacophagousStrategy

Diptera are holometabolous insects, i.e. their life cycle involves a majorchange in form (metamorphosis) from a soft-bodied larval stage to ahardened, usually winged adult. The major morphological feature thatdistinguishes adult flies from other insects is their reduced hindwings,termed halteres. Thus adult flies have only one pair of functional wings,hence their scientific name Diptera, derived from di = two, and pteron =wing. Because of the reliance on the forewings for flight, the mesothoraxhas become enlarged to contain powerful flight muscles, and the pro- andmetathorax are correspondingly reduced. The halteres are small, club-likeand function as balancing structures during flight. A few flies have losttheir wings (and halteres).

The mouthparts of adult flies are characteristically suctorial, andmany have large fleshy pads with drainage canals termed pseudotracheaefor efficient liquid uptake. Adult dipterans feed on liquids associatedwith decaying organic matter, and on honeydew and nectar. Some flieshave mouthparts modified for stabbing or piercing other invertebrates,plant tissues or vertebrate skin. In relatively few cases have themouthparts in adult Diptera been modified for a predaceous life style.

The transformation of the hindwings into halteres and the develop-ment of the mouthparts for sponging liquids represent synapomorphiesthat well collaborate the monophyly of the Diptera (Hennig, 1973; Woodand Borkent, 1989; Kristensen, 1991; Yeates and Wiegmann, 1999).

The larvae of Diptera lack true legs and move by peristaltic waves ofmuscular contraction through the body. The larvae of most species of flieshave a reduced head capsule and all that remains are the chitinous

86 J.B. Coupland and G.M. Barker



mandibles or mouthhooks and some associated sclerites, whichcollectively are called the cephalopharyngeal skeleton. Often thecephalopharyngeal skeleton is partially or completely sclerotized darkbrown to black. The morphology of the cephalopharyngeal skeletonrelates strongly to diet. Ferrar (1987, p. 23) concluded that ‘predaceousspecies tend to have long, slender mouthhooks, very curved and sharplypointed, dental sclerites fused to a single median ventral arch, and a pha-ryngeal sclerite that is long, slender and streamlined in lateral view . . .Endoparasites tend to have short, squat mouthhooks, with a small butsharp point (though some hooks may be large and squat), and rather squatpharyngeal sclerites with widely separated cornua . . . Carrion feedershave saprophagous-type pharyngeal sclerites (with or without ventralpharyngeal ridges), and stout mouthhooks with sharp points for cuttingthe flesh.’ Ferrar (1987) provides a discussion on the terminology appliedto the cephalopharyngeal skeleton and the homology of its components.

The Diptera have traditionally been divided into two suborders, theNematocera and Brachycera (Fig. 3.1). The Nematocera include generallysmall, delicate adult insects with long antennae, such as crane-flies(Tipulidae), mosquitoes (Curculidae) and midges (Chironomidae). TheBrachycera include more compact, robust adult flies with short antennae.There appears to be little doubt that the Brachycera is a monophyletic

Diptera as Predators and Parasitoids 87

Fig. 3.1. Cladogram showing the relationships between higher-level taxa in Diptera, synthesizedfrom the literature, primarily McAlpine (1989), Wood and Borkent (1989), Woodley (1989), Wiegmannet al. (1993), Cumming et al. (1995), Oosterbroek and Courtney (1995), Griffiths (1996), Yeates andWiegmann (1999). The topology of the tree varies greatly among published studies. Only a few nodes,indicated by bold internodes, have strong empirical support. Note also that under this classification,Psychodomorpha and Tipulomorpha are paraphyletic with respect to Brachycera; Tabanomorpha,Xylophagomorpha and Stratiomyomorpha are paraphyletic with respect to higher Brachycera; andPlatypezoidea and Syrphoidea (collectively often referred to as Aschiza) are paraphyletic with respectto Schizophora. The dipterans of particular interest in this chapter are all included in the Cyclorrhapha.



group, characterized by a suit of undisputed synapomorphies (Hennig,1973; Woodley, 1989; Sinclair, 1992; Sinclair et al., 1994; Yeatesand Wiegmann, 1999). The earliest brachyceran fossils are those fromthe Lower Jurassic, indicating that the group probably arose in theTriassic (208–245 million years ago) (Kovalev, 1979; Woodley, 1989).

As summarized by Yeates and Wiegmann (1999), Cyclorrhapha is anassumed monophyletic lineage within the Brachycera, characterized by:(i) a pupa enclosed in the hardened skin (puparium) of the last larvalinstar; (ii) larva with a cephalopharyngeal skeleton; (iii) anterior positionof the larval head capsule; (iv) larva with a pharyngeal filter; (v) larvalcentral nervous system peg-like; (vi) adult wing vein R4+5 unbranched;(vii) male adult ejaculatory apodeme and sperm pump separated frombase of the phallus; (vii) male adult hypopygium rotated 360° duringmetamorphosis in the puparium; (viii) adult male gonocoxal apodemesabsent, adult male surstyli present; and (ix) adult abdominal plaquesreduced. The Cyclorrhapha are further divided into two groups based onthe presence or absence of the ptilinum and associated fissure on thehead. The ptilinum is a sac that is everted during the emergence to assistthe adult fly to break free of the puparium. The aschizan flies lack theptilinum whereas the schizophoran flies possess it. The dipteran familiesof interest in this chapter are all cyclorrhaphan (Fig. 3.2), with Phoridaeclassified in the Aschiza, and the Sarcophagidae, Calliphoridae,Muscidae and Fanniidae, together with the Sciomyzidae, in theSchizophora.

Schizophora comprises the majority of family-level diversity in theDiptera. Traditionally this taxon is subdivided into Calyptratae andAcalyptratae, based respectively on the strong or reduced developmentof the lower calypter. McAlpine (1989) considered the Acalyptratae asa monophyletic sister-group to Calyptratae, with the following majorsynapomorphies: (i) male dichoptic; (ii) reduced lower calypter; (iii) lossof the postclypeus; (iv) two of the three spermathecae in the female with acommon duct; (v) loss of pupal prothoracic respiratory horns; (vi) trachealair sacs reduced; and (vii–xvi) loss of vestiture, pre- and postsuturalinter-alars, presutural dorsocentrals, pre- and postsutural acrostichals,ventral scutellar hairs, katepimeral hairs, meral hairs and laterotergalhairs. A monophyletic clade within the Acalyptratae, inclusive of theSciomyzoidea, is characterized by a reduced sternite 6 in the male.

Calyptratae is a group well supported by morphological synapo-morphies (McAlpine, 1989), including: (i) dorsolaterally placed cleft orseam in the antennal pedicel; (ii) presence of lower fronto-orbital bristles;(iii) development of prestomal teeth; (iv) well-developed lower calypter;(v) abdominal spiracles 2–5 found in the tergites; and (vi) male sternite 5with two posterior processes.

In the past few decades there has been much interest in thephylogenetics of Diptera and critical re-examination of the higher-levelrelationships and taxonomy within a cladistic framework. This work hasrevealed that many of the traditional categories such as the Nematocera




and Aschiza are not natural monophylogenetic lineages, but ratherparaphyletic assemblages (see review by Yeates and Wiegmann, 1999).The most comprehensive treatment of dipteran phylogeny based onmorphological characters can be found in McAlpine and Wood (1989),but there are numerous more recent examples addressing the systematicsof taxa at various levels.

There is increasing employment of molecular techniques (especiallyDNA sequence analyses) to address the evolutionary relationships withinthe Diptera (e.g. Friedrich and Tautz, 1997; Bernasconi et al., 2000a,b;Wiegmann et al., 2000; Nirmala et al., 2001). These studies have generallysupported the higher-level cyclorrhaphan systematics founded onmorphology. None the less, the Calyptratae–Acalyptratae division isnot always supported (e.g. Bernasconi et al., 2000b).

Carnivory is widespread in Diptera, with the larval stages varyingfrom predatory generalists taking a broad range of prey species through tohighly prey-specific parasitoids. The predatory strategy is particularlyevident in Apioceridae, Athericidae, Cecidomyiidae, Chamaemyiidae,Chaoboridae, Dolichopodidae, Dryomyzidae, Empididae, Mydidae,Rhagionidae, Scenopinidae, Syrphidae, Tabanidae, Therevidae andSciomyzidae, with the latter family involving malacophagy.

The parasitoid life strategy, a specialized form of carnivory with highprey specificity and intimate prey–predator relationship, arose numeroustimes in the Diptera – more than 100 times according to the estimatesof Eggleton and Belshaw (1992). It is the predominant form of theassociation of Diptera with living gastropods. The parasitoid strategy isdependent on maintenance of the prey in a living state for part or all of thelarval development. Often this prey maintenance requires specializedadaptations by the parasitoid to reduce the chances of premature preydeath, both at the time when parasitism is being established and duringthe development of the parasitoid larva. Under these conditions theprey is generally termed the host. The close relationship that parasitoidsenter into with their hosts favours specialization, which can lead tocoevolution, high rates of speciation, and adaptive radiation (Price, 1980).

Most dipteran parasitoids are endoparasitoids, as the larvae developwithin the body of their host and feed on the host tissues from within. Thenotable exception is the family Bombyliidae, where parasitoid speciesdevelop externally on the bodies of their hosts, and thus can be regardedas ectoparasitoids. Askew and Shaw (1986) classified hymenopteranparasitoids based on whether a parasitoid permits the host to grow and/ormetamorphose beyond the stage attacked. Koinobionts in this classifica-tion are parasitoids that allow their host to continue to develop afteroviposition, whereas idiobionts are parasitoids that paralyse or kill theirhost before oviposition. Because no dipteran parasitoids paralyse theirhost or arrest its development with venom, all would have to be classifiedas koinobionts under this scheme (Feener and Brown, 1997). However, asnoted by Belshaw (1994), there is much variation among Diptera in theamount of host development permitted after parasitism is established by




90J.B

. Coupland and G

.M. B

arker

90

A4784 - Barker - First Revise VP10 DA #G.prn

Z:\Customer\CABI\A4743 - Barker\A4784 - Barker - First Revise VP10 DA #G.vp

Tuesday, May 18, 2004 11:55:53 AM

Color profile: Disabled

Composite 150 lpi at 45 degrees

Diptera as P

redators and Parasitoids

91

Fig. 3.2. Cladogram showing the relationships between family-level taxa in the dipteran Cyclorrhapha, based on a tree presented by McAlpine (1989). Thefamilies that include malacophagous species, and discussed in this chapter, are indicated in bold.

91



Tuesday, May 18, 2004 11:55:55 AM



oviposition or larviposition. It should also be noted that several species inthe sciomyzid genus Tetanocera Duméril, on attaining instar III, switchfrom the parasitoid strategy of the early instars to a predatory feedingbehaviour, and immobilize their gastropod prey by introducing aneurotoxic saliva during the initial attack (Trelka and Foote, 1970; Trelkaand Berg, 1979).

As noted by Feener and Brown (1997), dipteran parasitoids do notinject venom to incapacitate the prey’s immune system. Larvae of manydipteran parasitoids (e.g. Acrocidae, Bombyliidae, Cryptochetidae, someCalliphoridae and most Tachinidae) maintain respiratory exchange withair external to the host by attaching their posterior spiracles to the host’stracheal system or projecting them through a hole in the integument(Clausen, 1940; Askew, 1971; Eggleton and Belshaw, 1993). This rendersany host encapsulation response ineffective. In many cases the dipteranlarvae turn the immune response of their host to their own advantageby building a tubular respiratory duct from products of the host’simmune response (Salt, 1968). In some dipteran parasitoids (e.g. someTachinidae), larvae establish within specific tissues (nerve ganglia,muscles, glands) and do not elicit an immune response from the host.These larvae remain in these protected locations until they are ready toconsume the host.

The interactions between larval parasitoids and their hosts have notbeen fully investigated and remain entirely unknown for the majority ofdipteran parasitoid species.

In most dipterans, potential prey or hosts are located by two distinctphases. Firstly the adult females locate the microhabitat of potential prey,using cues from the microhabitat and/or the intended victims. Once in thegeneral vicinity of prey, females scatter eggs or larvae on the surface of thesubstrate and then leave the area. Actual contact with the prey individ-ual(s) occurs in the second phase and is effected by the immature stages.There are three basic mechanisms by which such dispersed immaturesmay contact prey (see Hagen, 1964, for discussion on parasites generally),each well represented in the Diptera (Feener and Brown, 1997): (i) thedipteran egg may be ingested by the animal that is to become the host; (ii)the dipteran larva may wait in ambush for passing prey or host; or (iii) thedipteran larva may actively search for suitable prey or host. Most dipter-ans that rely on immatures for prey/host contact produce actively search-ing larvae. Such actively searching larvae have evolved independentlyin numerous dipteran families (Feener and Brown, 1997), includingCalliphoridae and Sciomyzidae. As noted by Feener and Brown (1997),actively searching larvae allow many species to utilize prey that live inplaces inaccessible to adult flies (e.g. soil, interiors of rotten wood, water).

Many parasitoid Diptera have developed a strategy whereby searchfor and contact with larval hosts is made by the adult fly. In these casesthe fly oviposits or larviposits directly on to the intended larval host. Thisstrategy has the obvious advantage of reducing the mortality of larvae thatresult from failures to locate a suitable prey or host.




The macro- and microhabitat of potential hosts and the associatedmanner of host location by adult females has generally been considered akey determinant of host range in dipteran parasitoids (Lawton, 1986;Schlinger, 1987; Yeates and Greathead, 1997). Host specificity is moreoften determined by the events leading up to oviposition/larviposition,rather than by events occurring after oviposition.

Dipteran parasitoids use a wider array of hosts than any other insectgroup of parasitoids. While Hymenoptera are more species rich, they arerestricted to arthropod hosts. Feener and Brown (1997, p. 86) suggest that:

Host associations unique to the parasitic Diptera include terrestrialflatworms [Platyhelminthes: Tricladida], earthworms [Clitellata:Haplotaxida], freshwater and terrestrial pulmonate snails [Gastropoda:Basommatophora and Stylommatophora], woodlice [Isopoda], scorpions[Arachnida: Scorpionida], termites [Isoptera: Termitidae], and frogs[Amphibia: Anura]. In some instances exploitation of these unusual hostsevolved more than once. Terrestrial snails, for example, serve as hosts forspecies in the Phoridae, Sciomyzidae, Calliphoridae, and Sarcophagidae.

While publication in an entomological journal may excuse their focuson insects, these authors clearly did not take into consideration thehelminths (e.g. Nematoda, Trematoda), acari and various protozoans,groups that obviously exploit a broader array of hosts, including terres-trial and freshwater molluscs. Feener and Brown (1997) go on to suggest:

All of these unusual noninsect hosts [of Diptera] are associated withsubstrate-zone habitats (e.g. soil, leaf litter, or other organic matter onthe ground) and reflect the important role that these habitats play in theevolution of the parasitoid life style within the Diptera (Eggleton andBelshaw, 1992). In contrast, evolution of the parasitoid life style in theHymenoptera is closely tied to vegetation-zone habitats (Gauld, 1988;Gauld and Bolton, 1988; Eggleton and Belshaw, 1992), which offer littleopportunity for the exploitation of such soil-dwelling hosts.

Such an analysis may hold true as a broad generalization but itfails to recognize the broad overlap in zones of activity in dipteran andhymenopteran parasitoids. Examples of convergent utilization of similarhosts are: (i) dipteran (Phoridae, Pyrgotidae, Sarcophagidae andTachanidae) and various hymenopteran (e.g. Braconidae, Chalcididae,Eulophidae, Pteromalidae, Scelionidae) endoparasitoids in lepidopteranand coleopteran larvae (in both substrate-zone and vegetation-zonehabitats); (ii) dipteran (e.g. Acroceridae, Phoridae) and hymenopteran(e.g. Ichneumonidae, Scelionidae) parasitoids of spider (Araneae) eggs(in substrate-zone habitats); and (iii) dipteran (e.g. Bombyliidae) andhymenopteran (e.g. Mymaridae, Trichogrammatidae) parasitoids oflepidopteran eggs. Furthermore, a number of dipteran parasitoids ofterrestrial gastropods utilize hosts in vegetation-zone habitats, oftenat some height above the ground.

Phoridae (Brown, 1992; Disney, 1994; Feener and Brown, 1997),Bombyliidae (e.g. Hull, 1973; Yeates and Greathead, 1997; Yeates et al.,




1999), Sarcophagidae (Ferrar, 1987; Eggleton and Belshaw, 1992) andTachinidae (e.g. O’Hara, 1985; Wood, 1987; Belshaw, 1993, 1994) utilize aremarkably wide range of hosts. These groups are rather speciose.Furthermore, they have not only diversified to exploit a wide range ofhosts, but often contain individual species which themselves exhibitextreme polyphagy, often utilizing many species across several families,and in some cases across several Phyla. The families Phoridae and Sarco-phagidae contain numerous saprophagous species and it is clear that theparasitoid life style arose repeatedly. By contrast, the family Tachinidae isentirely parasitic, so diversification of host use must have followed theacquisition of the parasitoid life style (Feener and Brown, 1997).

Other families of dipteran parasitoids are more restricted in theirbreadth of hosts, with Acroceridae specializing on spiders, Conopidae onHymenoptera, Pipunculidae on Homptera, Rhinophoridae on Isopoda,Pyrgotidae on scarabaeid Coleoptera, and Nemestrinidae on acrididOrthoptera. The Sciomyzidae have specialized on molluscs, althoughseveral species have, secondarily, adapted to feeding on oligochaetes(Vala et al., 2000; Barker et al., Chapter 4, this volume). In this dipteranfamily, the feeding strategy varies from predators and facultativelynecrophagous to endoparasitoid (Barker et al., Chapter 4, this volume).

While the association between certain dipterans and molluscs hasbeen known for a long time, the actual trophic relationships of mostspecies are still unknown today. Ferrar (1987) correctly noted that itis often difficult to determine the true nature of the association ofthe cyclorrhaphan larva and its medium. This is particularly the casefor families comprising species that may have scavenging, parasitic orparasitoid relationships. He comments (p. 38):

A substantial number are true parasitoids, and often this is quite clear-cut,but when one finds a dead grasshopper or large beetle or particularly a snail,it is not at all clear whether a larva in it is a parasitoid in the final stage ofattack, or one of a number of larvae that breed particularly in this type ofinvertebrate carrion. Dead snails in particular are attractive to a number offamilies of Diptera. In a family such as Sarcophagidae both true parasitoidsand saprophagous feeders on invertebrate carrion occur.

It is probable that the occurrence of parasitism of gastropods hasbeen underestimated for families such as Phoridae, Sarcophagidae andCalliphoridae. Equally, there are some species that are assumed to bepredators with little or no knowledge of their life history – the evidencefor the parasitoid relationship is circumstantial and insufficient detailsare available to determine whether they are true parasitoids or merelynecrophagous (Mead, 1979; Disney, 1994).

Gastropod hosts represent discrete resource patches, and thesepatches are ephemeral in that most gastropods, once parasitized andkilled, decay and/or dehydrate rather rapidly. Furthermore, the cadaverscan often be colonized by necrophagous Diptera and other organisms.Sacrophagids often exhibit a specialization on parasitism of aestivatingpulmonata snails. Sealed to the substrate by the epiphragm, these snails




would probably offer hosts that are less liable to dehydrate and withreduced competition from opportunist necrophages. The same conditionsare probably provided when operculate caenogastropods are the hosts.Sciomyzids with predatory-type larvae quickly consume the prey, andwhile there is an element of necrophagy on the tissues after prey death,they generally attack a series of living prey individuals to completedevelopment. When parasitoid, the sciomyzid early larval instarsare completed before host death, and the adoption of predatory ornecrophagous behaviours occurs in the last instar.

For Diptera, interspecific competitive interactions, and parasitism byhymenopteran parasitoids, occur almost exclusively in the larval stages.It is competition (Beaver, 1977) and parasitism (e.g. Legner et al., 1967;Legner and Olton, 1968; Disney, 1994) during the larval period thatdefines community structure. Such aspects have been most thoroughlyinvestigated for sarcophagid and calliphorids of veterinary and forensicinterest. The community ecology of Diptera breeding in dead gastropodshas received some attention (e.g. Beaver, 1972, 1973, 1977; Kneidel, 1983,1984a,b; Kühlhorn, 1986; Woodcock et al., 2002). However, with theexception of a few notable studies on the Sciomyzidae (e.g. Mello andBredt, 1978; Vala, 1984), there has been little attention given to communityecology of predatory or parasitoid Diptera utilizing gastropods.

Superparasitism is the deposition of eggs or larvae in a host alreadyparasitized by a member of the same species (van Dijken and Waage,1987; Godfray, 1993). Because the progeny of a superparasitizing femaleare normally at a competitive disadvantage relative to the progeny of theprevious parasitoid, natural selection should favour females with theability to discriminate parasitized from unparasitized hosts. Feener andBrown (1997, p. 81) point out that, ‘In contrast to parasitic Hymenoptera,superparasitism in the parasitic Diptera appears to be both widely distrib-uted across species and common within populations.’ These authors notethat superparasitism has been reported in Conopidae, Phoridae andTachinidae, and is suspected for several other families. They go onto stress that within dipteran populations ‘superparasitism may occurregularly and sometimes reach high levels’, and conclude (p. 82) ‘Thewidespread occurrence of superparasitism in the parasitic Diptera sup-ports the impression that the ability to discriminate between parasitizedand unparasitized hosts is entirely lacking or severely limited in thisgroup.’ Feener and Brown (1997) argue on evolutionary grounds that hostdiscrimination should occur in dipteran parasitoids in which the femalemakes direct contact with hosts, and indeed refer to several knownexamples of such discrimination.

Coupland and Baker (1994) suggest that the reason females of the soli-tary snail parasitoid Sarcophaga (Heteronychia) penicillata Villeneuveremain on the host for 5–65 min after larviposition is to protect againstsubsequent superparasitism. Feener and Brown (1997) argue that, ratherthan directly protecting against superparasitism, this ‘post-ovipositionalhost-guarding’ behaviour in S. penicillata allows the larva to gain enough




of a growth advantage to prevent development of any subsequent larvaedeposited on the same host.

Phoridae

The Phoridae are commonly known as scuttle or humpbacked flies,reflecting, respectively, the walking behaviour and general body form ofthe adult flies. Phoridae are represented in all regions of the world beyondthe polar regions. The family comprises approximately 3000 describedspecies in some 250 genera. However, the true world fauna is of the orderof 10,000 species (Brown, 1992).

The systematics of Phoridae is far from stable. Even at the subfamilylevel there has been little agreement among phylogenetic hypotheses andtaxonomic schemes. Six subfamily groups may be provisionally recog-nized, namely Hypocerinae, Phorinae, Aenigmatiinae (including thauma-toxenines), Conicerinae, Metopininae and Termitoxeniinae (includingalamirines). Brown (1992) proposed a phylogenetic hypothesis for therelationships among the five subfamilies represented in the Nearcticregion. A world catalogue of Phoridae was published by Borgmeier(1968, 1971), which continues to be updated electronically (B.V. Brown,personal communication). There is presently little agreement amongresearchers on rank, nomenclature and composition of tribal, generic andsubgeneric categories. Disney (1994) provides separate keys to a selectionof nominal genera based on males and females. None the less, a largeproportion of nominal genera are still known only from one sex becausethe high frequency of sexual dimorphism means that males and females ofthe same species cannot be matched using morphological criteria alone.Presently females may be confidently associated with males only when incopula, which is rare in field collecting, or if reared from eggs of knownparentage. However, Cook and Mostovski (2002) demonstrated that DNAsequencing can be employed to match males with previously crypticfemales and thus aid in the identification of morphological characters thatallow identification of females without recourse to further molecularstudy.

Adult Phoridae (Fig. 3.3A) are small (1.0–6.0 mm) humpbacked fliesof a black, brown or yellow colour. The wings are folded flat over theabdomen at rest – some have apterous or brachypterous females. Thelegs, particularly the hind femora, are strongly developed. Adults have acharacteristic quick, jerky movement when running, and some speciesdisplay a swarming, up-and-down flight behaviour.

The production of wingless females has evolved repeatedly inPhoridae. Flightlessness is especially characteristic of species whosefemales inhabit the nests of ants (Hymenoptera, Formicidae) and termites.The flightless condition has been attained in two distinct ways, namely:(i) by shedding part of the wing soon after adult emergence (the wings arein part deciduous (caducous)); and (ii) by evolutionary reduction of the





Fig. 3.3. Habitis illustrations of the adult and larval stages of dipteran families addressedin this chapter. (A) Phora Latreille (Phoridae) adult (drawing by Idema, from J.F. McAlpine,Soil Biology Guide). (B) Megaselia Rondani (Phoridae) larva (drawing from H.J. Teskey, SoilBiology Guide. Reprinted with permission of John Wiley & Sons, Inc.). (C) Sarcophaga Meigen(Sarcophagidae) adult (drawing by Idema, from J.F. McAlpine, Soil Biology Guide. Reprintedwith permission of John Wiley & Sons, Inc.). (D) Sarcorohdendorfia Baranov adult (Sarco-phagidae) (drawing by T. Binder, reproduced with permission from CSIRO). (E) CalliphoraRobineau-Desvoidy (Calliphoridae) adult (drawing by D. Helmore, reproduced with permissionfrom Landcare Research). (F) Melinda Robineau-Desvoidy (Calliphoridae) (drawing by H.Kurahashi, reproduced with permission from Pacific Insects). (G) Musca Linnaeus (Muscidae)adult (drawing by Idema, from J.F. McAlpine, Soil Biology Guide. Reprinted with permissionof John Wiley & Sons, Inc.). (H) Potamia Robineau-Desvoidy (Muscidae) larva (drawing fromH.J. Teskey, Soil Biology Guide. Reprinted with permission of John Wiley & Sons, Inc.).(I) Fannia Robineau-Desvoidy (Fanniidae) larva (drawing from H.J. Teskey, Soil BiologyGuide. Reprinted with permission of John Wiley & Sons, Inc.).



wing. The four basic conditions encountered in other flightless insects(Hackman, 1964) are all to be found in Phoridae: brachypterous, in whichthe wing is reduced by shortening; stenopterous, where the wing isreduced by narrowing; micropterous, wing reduced to a rudiment;apterous, wing represented by a bristle at most. Normally in Phoridaethe males retain fully functional wings, but the males in the Afrotropicalgenera Aptinandria Schmitz and Arrenaptenus Schmitz are flightless.Hackman (1964) has emphasized that flying males make gene flowpossible over a wider geographic range than is possible when both sexesare flightless. In some phorids, the flightless females are transported bythe males, especially during mating.

There is a prevalence in Phoridae for the female to take protein-richmeals, and in some cases even involves the females inflecting wounds onother insects in order to feed on the haemolymph. Such a habit reducesthe need to accumulate resources in the pre-adult stages in order tosupply the nutrients to the eggs to be laid by the female. This may be afactor in the evolutionary trend for smaller adult size in the Phoridae andthe evolution of the termitophilous and myrmecophilous life strategies(Disney, 1994). Adults of some species feed on honeydew and visitflowers to obtain nectar and/or pollen (summarized by Disney, 1994).

Pupation occurs in the food, often in contact with semi-liquidmaterials and with the ventral surface of the puparium attached to thesubstrate. A number of phorid species, especially in the Termitoxeniinaeand other genera associated with termites, emerge from the puparium asstenogastric forms, in which the abdomen is of normal proportions, andsubsequently develop into physogastric forms with greatly enlargedabdomen. While the bulk of the abdomen in the physogastric phase isoccupied by the greatly enlarged ovaries, there is evidence to indicateenlargement also occurs in other organs (Mergelsberg, 1935). Thephenomenon of physogastric development has been reviewed by Kistner(1982). As noted by Disney (1994), there is little doubt that the primefunction of the physogastric enlargement of the abdomen is to accommo-date the relatively large eggs. Enlargement of the eggs, relative to otherphorids, is in turn related to their long incubation period and curtailmentof the free-living larval stage, and to the mimicry of their host termite’seggs.

Most Phoridae oviposit directly on to or into the food to be utilizedby the larvae. In some cases where the adult female is flightless (e.g.Puliciphora africana Brues, Metopininae), the winged males transportthe gravid female to suitable media. The ovipositor morphology andoviposition behaviour varies greatly among phorids, reflecting the greatdiversity of the media utilized as oviposition sites. Data on fecundityexists for only a few species. None the less, it is apparent that fecundityvaries greatly among phorid species. Eggs may be deposited singly or inclutches up to c. 100 eggs. As pointed out by Disney (1994), a low clutchsize would seem to be associated with two distinct phenomena. In somecases it is correlated with specialist predatory or parasitic life strategies –




the high chance of success compensates for the risks associated witha concentrated investment. The other phenomenon associated with areduced clutch size is accelerated larval development and suppressionof the free-living larval stage. In Assmutherium Schmitz (Metopininae),apparently only three eggs are matured in the ovarioles at a time, and theembryos start to develop before the eggs are laid (Disney, 1991a). Inthe more extreme case of Clitelloxenia Kemner (Termitoxeniinae), theincubation period in the egg stage is prolonged, and associated withthis the larva takes no food after emerging from the egg (Kemner, 1926;Franssen, 1933).

Peterson (1987) noted that, while the Phoridae, with few exceptions,are among the most easily recognized Diptera, information on the biologyof the adults and larvae are scattered and complete life histories areknown for only a few species. As stressed by Brown (1992), few larvaehave been described and thus the immature stages of almost all phoridscurrently are not assignable to species. Disney (1994, p. 203) laments ‘Theprincipal impediment to the study of the natural history of scuttle flieshas been the difficulty of identifying specimens with confidence.’ Keilin(1911), Schmitz (1938–58), Hennig (1952), Robinson and Foote (1968),Robinson (1971), Kaneko and Furukawa (1977), Kloter et al. (1977), Ferrar(1987), Peterson (1987), Smith (1989) and Disney (1994) are the majorreferences to both immature structure and ways of larval life.

Typically there are three larval instars (Fig. 3.3B), with duration ininstar III tending to be somewhat longer than that of instars I and II.As noted above, there are cases, especially in the Termitoxeniinae, wherethe larval stages are greatly curtailed. The mouthparts of phorid larvaetypically have paired mandibles (mouth hooks) and a median toothsupported by a cephopharyngeal skeleton behind. In saprophagousspecies the mandibles tend to have several teeth. In the predatory speciesthe mandibles are generally heavily sclerotized and the terminal tooth ofeach is enlarged.

Life histories of phorids are extremely diverse. Numerous speciesfeed in decaying material. While many can develop successfully in anyorganic medium, some saprophages evidently develop only in specificmedia such as fungi or dead gastropods. Some species are pests, suchas the notorious spoilers of cultivated mushrooms Megaselia halterata(Wood) and Megaselia tamilnaduensis Disney (Metopininae) (e.g. Hussey,1960; Robinson, 1977; Mohan et al., 1995). Many phorids have evolvedassociations with other organisms. Larvae of many species are specializedpredators or parasitoids, recorded from gastropod eggs, caddisfly(Trichoptera) eggs, spider eggs, various Diptera larvae, gall-forming androot aphids (Hemiptera, Aphidae), beetle adults and larvae (Coleoptera),earthworms, millipedes (Diplopoda), and gastropods. Many others, as lar-vae, are parasitoids or symbionts of social insects, especially termites andants, but also bees and wasps (Hymenoptera). Some are involved in casesof myiasis in both humans and livestock, while others are useful in foren-sic entomology because of their propensity to colonize human corpses.




Perhaps the primitive larval habit of Phoridae was either saprophagyor fungivory. Feener and Brown (1997, p. 76) concluded ‘general trendsfound in the Phoridae are the apparent acquisition of parasitoid behaviorfrom a scavenger host association . . . and the predisposition of taxaassociated with burrowing social insects to become parasitoids of thoseinsects . . .’. Disney (1994) suggests that probably most larval Phoridaetoday are specialized predators or parasitoids, with such specializationoccurring repeatedly and independently in several clades. Such trendsare also present within the larval life stages of individual species. In somespecies the early instar(s) are saprophagous, but the subsequent instar(s)are predatory. In some species the corresponding trend is from predatoryto parasitoid, and in yet others, the trend is in reverse, from initiallyparasitoid to later instars being predatory.

There has been a renewed interest in Phoridae with the realizationthat these dipterans may prove to be useful biological control agents forinvasive ant species (e.g. Morrison and Gilbert, 1999; Morrison, 2000;Folgarait et al., 2002; and references therein).

The Hypocerinae, the most basal clade amongst extant Phoridae, arerepresented worldwide. Within the subfamily, the genus Hyocera Lioyis evidently composed of saprophages (M. Buck in Feener and Brown,1997), with several species reared from mollusc carrion (e.g. Schmitz,1916a, 1917). In Peromitra Enderlein, the only other hypocerine genus forwhich larval biology is known, the immature stages of several speciesoccur as parasitoids in bibionid fly larvae (Morris, 1922; Gemesi andDisney, 1991). Several other hypocerinae genera are suspected parasitoidsof bees (Feener and Brown, 1997).

Aenigmatiinae occur worldwide. Many species are saprophagous,including several Dohrniphora Dahl species that have been bred frommollusc carrion (e.g. Schmitz, 1914; Bohart and Gressitt, 1951; Beaver,1987). Several species in Diplonevra Lioy are parasitoids of earthworms(Colyer, 1950; Disney, 1991b). The predominant life strategy in aenigma-tiine genera is association with burrowing social insects and manycan be regarded as termitophilous or myrmecophilous. Some of theseassociations are parasitoid.

Phorinae occur in most parts of the world but are notably absent fromAustralia. The ecology of Phora Latreille is unknown but for one species,namely Phora holosericea Schmitz, which predates on root aphids(Yarkulov, 1972). Anevrina Lioy species live in mammal burrows (Brown,1992 and references therein), whereas larvae of ChaetopleurophoraSchmitz, Spiniphora Malloch and Plethysmochaeta Schmitz commonlydevelop in carrion, including dead molluscs (e.g. Brues, 1903; Schmitz,1916a, 1917, 1929a, 1938, 1938–58, 1940; Lundbeck, 1920, 1922;Colyer, 1955; Grensted, 1956; Disney, 1972, 1980b; van Achterberg andBin, 1981). Beaver (1987, p. 190) thought that ‘all species of Spiniphoradevelop in dead snails, and appear to be confined to this habitat for breed-ing (Schmitz, 1917, 1941).’ None the less, in addition to gastropod carrion(e.g. Mik, 1864), the Holarctic–Neotropical Spiniphora bergenstammi




(Mik) breeds in other situations such as bird (Aves) nests (Disney, 1994)and has been reared as a parasitoid from various helicids, includingArianta arbustorum (Linnaeus), Cepaea hortensis (Müller), Cepaea nem-oralis (Linnaeus) and Helix pomatia Linnaeus (Helicidae) (Bergenstamm,1864; Keilin, 1911; Schmitz, 1917). Thus, while primarily a saprophage,S. bergenstammi evidently exhibits facultative parasitism. Lundbeck(1920) reported Spiniphora excisa Becker, a species distributed through-out the Holarctic, as having been reared from live-collected terrestrialgastropods C. hortensis, C. nemoralis, Helicigona lapicida (Linnaeus), andthe freshwater planorbid Planorbis corneus (Linnaeus). Kidd and Brindle(1959) similarly recorded the Palaearctic Spiniphora helicivora Dufourfrom Helix Linnaeus species and from Planorbis Müller species. Whilethese records for S. excisa and S. helicivora from helicids suggest aparasitoid association with gastropods, the records from Planorbisundoubtedly relate to cases of saprophagy or opportunistic pseudo-parasitism in dying gastropods in the strand line of freshwater bodies.Previous records of these two Spiniphora species reared from dead gastro-pods (e.g. Schmitz, 1908) have been interpreted as saprophagy by Disney(1994) but some may have been the product of parasitism in livinggastropods. Spiniphora maculata (Meigen), a European species, has beenrecorded from both dead (Dufour, 1841; Lundbeck, 1922; Beaver, 1972;Disney, 1972) and live-collected gastropods (Keilin, 1911; Coupland,1994). Chaetopleurophora bohemanni (Becker), a Palaearctic species, wasrecorded as a parasitoid of H. pomatia by Lundbeck (1920), and subse-quently reared from dead gastropods by Schmitz (1941). The parasitoidbehaviour of these phorines requires confirmation and further study. Theecology of the great majority of phorine species is presently not known.

Conicerinae are distributed throughout the world. Most have sapro-phagous larvae, and include several species that breed in mollusc carrion(Beaver, 1987). Larvae of Gymnoptera Lioy are scavengers, with adultsof Gymnoptera molluscovora (Bohart) and Gymnoptera orientalis (deMeijere) attracted to and oviposting on rotting molluscs, on which larvaedevelop (Bohart and Gressitt, 1951; Beaver, 1987). Several species ofGymnoptera breed in the nests of Hymenoptera, but information on theirway of life within these nests is presently lacking.

The subfamily Metopininae contains the greater majority of describedphorid genera and species, including the vast paraphyletic genusMegaselia Rondani. Metopininae occur worldwide. Saprophagy is themost prevalent larval feeding strategy – a number of species occur assaprophages in mollusc carrion (e.g. Grimshaw, 1901; Keilin, 1911, 1919,1921; Malloch, 1912, 1935; Brues, 1915, 1919, 1942, 1950; Schmitz,1916b, 1917, 1925, 1929a, 1938–58; Lundbeck, 1922; Senior-White, 1924;Bezzi, 1928; Smedley, 1928; Bohart and Gressitt, 1951; Borgmeier, 1963,1967; Hardy and Beyer, 1964; Beyer, 1967; Robinson, 1971; Beaver, 1972,1977, 1986a, 1987; Disney, 1979, 1988, 1994; Kneidel, 1983, 1984a,b;Brown, 1987). However, a large number of metopinines have developedassociations with burrowing social insects (ants and termites) – while the




exact nature of the association is unknown for many, none-too-few areknown to be parasitoids (Rettenmeyer and Akre, 1968; Brown, 1992; Dis-ney et al., 1998). Additional metopinine species are parasitoids of otherinvertebrate groups (Brown, 1992; Disney, 1994, and references therein) –species in the genus Myriophora Brown utilize myriapods and harvest-men (Arachnida: Chelicerata: Opiliones); Kerophora brunnea Brown isa parasitoid of scale insects (Hemiptera); species of PhalacrotophoraEnderlein exhibit diverse life histories, with many associated withHymenoptera, but others are parasitoids in spider egg sacs or larvae ofcoccinellid Coleoptera; Apocephalus Coquillett generally parasitize ants,but many utilize other groups of arthropods as hosts, including beetles(Coleoptera), spiders and vespid Hymenoptera. There are a number ofcases of confirmed malacophagy involving metopinine species.

The genus Megaselia as presently recognized occurs worldwide.Disney (1994) notes that at least 45% of the known Phoridae are presentlyassigned to this nominal genus, with nearly 1400 described species cur-rently recognized. Brown (1992) and Disney (1994) discuss the problemsof recognition of monophyletic lineages within Megaselia. Disney (1994,p. 280) concludes ‘it will be many years before a phylogenetic classifica-tion of the subgroups within Megaselia can be achieved.’ Robinson andFoote (1968), Ferrar (1987) and Disney (1994) summarized the knowninformation on the biology of Megaselia species – in short, they are themost biologically varied group in Phoridae, ranging from phytophagesand saprophages, to predators and parasitoids of various invertebrates, toagents of myiasis in humans.

Brues (1942) and Beyer (1959) described Megaselia biformis Bruesfrom Hawaii and Megaselia javicola (Beyer) from Java, respectively, asparasitoids of Achatina fulica Bowdich (Achatinidae). Little is knownabout the biology of these metopinine phorids. A. fulica is surely not thenatural host in both cases, as this gastropod species is native to Africa andwas introduced to Java and Hawaii during the middle part of the 20thcentury.

Megaselia perdita (Malloch) is widely distributed in the Americas.Muma (1954) reported that the larva of Megaselia sp. – later determined tobe M. perdita by W. Robinson – is predaceous on the arboreal Drymaeusdormani (Binney) (Bulimulidae). Pierce et al. (1912) and Wildermuth(1915) reared M. perdita from insect larvae. Borgmeier (1964) speculatedthat the male of M. perdita was myrmecophilous, as the adults were foundin association with ants. Robinson (1971) recorded adults of this speciesvisiting bird faeces, and in traps baited with dead gastropods or cheese.Robinson also reported M. perdita reared from cotton (Gossypiumhirsutum Linnaeus; Malvaceae) squares. Gregor (1977) found M. perditato be readily caught in traps baited with mammalian flesh. Robinson(1981) trapped this species with rotten cheese as bait and subsequentlyreared it on cheese in the laboratory. Thus these observations indicatethat M. perdita is able to utilize diverse media and occurs as a facultativeparasitoid in invertebrates.




Borgmeier (1967) reported on Megaselia spiracularis Schmitz fromBradybaena seiboldiana (Pfeiffer) (Bradybaenidae). Disney (1982, 1994)reported on Megaselia fuscinervis (Wood) parasitizing Vitrea crystallina(Müller) and Vitrea contracta (Westerlund), two minute, ground-dwellingzonitids in England. The biology of these species has yet to be thoroughlyinvestigated.

Robinson (1965), Stephenson (1965), and Stephenson and Knutson(1966) made the initial reports of phorids feeding on gastropod eggs. Thephorid pertaining to the observations in North America was subsequentlyidentified as Megaselia aequalis (Wood) by Robinson and Foote (1968),and shown to be restricted to feeding on the eggs of the HolarcticDeroceras laeve Müller (Agriolimacidae). The European reports weresubsequently confirmed by Disney (1977), who found, in a collectionmade in England, several gastropod eggs (probably of the genus DerocerasRafinesque Schmaltz) attacked by Megaselia ciliata (Zetterstedt), aspecies recognized as closely related to M. aequalis. Several years later,Disney (1979) recorded M. ciliata from Arion de Férussac (Arionidae) andDeroceras eggs. Disney (1977) suggested that the association of thesetwo Megaselia species with gastropod eggs may be a characteristic of allspecies of the ciliata group. The larvae of Megaselia nasoni (Malloch), anassumed closely related species, was later shown to predate on spidereggs (Disney and Evans, 1980).

Robinson and Foote (1968) describe in some detail the biology ofM. aequalis. Laboratory-reared females, confined with males, had a pre-oviposition period of about 24 h. The female oviposited her eggs, eithersingly or in clutches of two to three, directly on to the eggs of D. laeve oroccasionally on to nearby vegetation. The fecundity of the females variedfrom three to 12, with an average of two eggs per day per female. Theincubation period of the eggs was 2–4 days. The newly hatched larvapenetrated the outer covering of the egg, passed through the gelatinousmatrix, and began feeding on the perivitelline fluid. The first-instar larvadid not attack the developing Deroceras embryo. The first larval stagerequired 1 or 2 days, and moulting occurred within the egg. The second-instar larva also remained within the egg, but usually destroyed theembryo. The second-instar stage took 2 days to complete, with moultingtaking place outside the egg. The early third-instar larva fed within thegelatinous matrix surrounding the egg capsule. Later it became morepredatory and usually destroyed at least four additional eggs and the con-tained embryos. The third larval stadium required between 3 and 5 days.When fully grown, the larva abandoned the egg clutch and pupated in thesoil. The prepupal and pupal stages combined required about 11–13 days.

Robinson and Foote (1968) note that while M. aequalis is widelydistributed in the Holarctic region, it is not commonly collected. In north-eastern Ohio, USA, M. aequalis adults are present from late May (spring)through to mid-September (autumn), with the species completing at leastthree generations over that period. Adults were found most abundantlyin stands of cattail (Typha Linnaeus, Typhaceae) and in partly shaded




seepage areas in lowland forests. Robinson and Foote noted that theseflies are not active fliers and were uncommon at higher levels in the vege-tation, apparently preferring the tangled, moist plant litter at groundlevel; the microhabitat of the fly thus closely matches that of the larvalhost. The adults have been repeatedly collected from the nests of birds,mammal and hymenopteran social insects (references in Robinson, 1971).

Both M. aequalis and M. ciliata occur in forests and woodlands ofEurope (summarized by Disney, 1994), where they overwinter as adultsunder bark and moss or within rotten timber (Malloch, 1910, 1911;Herbert and Braun, 1958; Disney, 1994). These hibernating adult fliesexhibit significant levels of fat body reserves (Schmitz, 1929b; Disney,1994). Malloch (1911) recorded M. ciliata adults as a frequent visitor offlowers. As summarized by Robinson (1971), M. ciliata adults have beenrepeatedly collected from the nests of birds, mammals and ants. Baumann(1977) found these flies to be common visitors to the burrows ofmammals, presumably related to the presence of gastropod eggs in suchsituations. Disney (1994) found M. ciliata to be active in the canopy oftrees in English woods. M. aequalis and M. ciliata also occur in pastures,arable crops, horticultural land and other modified habitat in the UK andmainland Europe (e.g. Boness, 1958; Disney, 1980a, 1989; Disney andGunn, 1980; Disney et al., 1981a,b; Froese, 1992a–c), indicating at leastsome persistence of the adult stage in these managed systems. However, itis presently not known to what degree M. aequalis and M. ciliata are ableto parasitize Deroceras eggs in these environments. The fact that thesespecies attack species in the family Agriolimacidae, many of which arepestiferous in agricultural systems, portends a potential use in integratedpest management. However, until we understand more of their popula-tion ecology and host preferences, we cannot readily comment on theirappropriateness. The agriolimacid and arionid egg hosts of theseMegaselia species occur on the ground and thus the larvae of M. aequalisand M. ciliata occupy the substrate-zone habitat referred to by Feener andBrown (1997).

Based on a study of phorids of forests of the Rhine River, Baumann(1979) postulated that the European species of the genus GymnophoraMacquart are parasitoids of dying gastropod slugs, especially in the gen-era Lehmannia Heynemann (Limacidae) and Arion. For oviposition thefemales follow the dying gastropods into the soil. However, rearing stud-ies by Brown (1987, 1992) and W.H. Robinson (in Brown, 1992) show thatthese phorids are saprophages, breeding in carrion and other decayingmaterial.

Puliciphora borinquenensis Wheeler, a Nearctic synanthrope, wastreated as a saprophage by Disney (1994) but had been reocorded fromlive gastropods by Borgmeier (1963).

Wandolleckia Cook is evidently a monotypic genus of tropical Afri-can Metopininae. The various nominal species have been synonomizedwith Wandolleckia achatinae Cook. Wandolleck (1898) described andfigured W. achatinae and added the following remark: ‘They seem to feed




on the slime of the snails. They are swift runners; when disturbed theyleave their host very quickly, but return to it later.’ According to Schmitz(1917), these phorids have lost their larval and pupal stages and becomeametabolic, this loss being compensated for by a certain degree ofdevelopment during the imaginal stage. Schmitz found the adult femalesto be dimorphic, with stenogaster females possessing a retracted, weaklychitinized abdomen, while physogaster females possess a normallychitinized, well-extended abdomen. Males were unknown to Schmitz(1917). Keilen (1919) states that the existence of steno- and physogasterforms does not demonstrate the ametaboly of an insect and mentionsPuliciphora Dahl species in which, while steno- and physogaster formsoccur, the larval and pupal stages are known.

Bequaert (1925, p. 205) observed 16 Wandolleckia on a single largeachatinid in the Belgian Congo, running swiftly over the mantle andunder the shell and entering the pallial cavity. Bequaert (1925) also notedthe dimorphism in the females, remarking:

As both kinds of individuals are females and as their morphological struc-ture is the same, dimorphism is evidently due to further development of thebody during the adult or imaginal stage . . . In the case of Wandolleckia theincrease of the abdomen results from the hypertrophy of the reproductiveorgans, probably in connection with some ethological peculiarity.

As noted earlier, heterochrony is now well known in phorids.Baer (1953) reared W. achatinae from the faeces of the achatinids

A. fulica and Archachatina ventricosa (Gould). The eggs were sometimesfound attached to the foot of the host snail, but more often were depositedin the faeces, which constituted the usual medium for larval develop-ment. Baer (1953) recorded three larval instars. Males were associaedwith the faeces, while the adult females were found running about on thelarge snails. Disney (1994) termed the association of W. achatinae withachatinids as ectotrophic phoresy.

Sarcophagidae

Sarcophagidae comprises a species-rich family, with some 2500described species distributed worldwide. As noted by Pape (1996), thisdiversity is markedly concentrated in warmer climates, and the family ispoorly represented at high latitudes. These flies have often been treated asa subfamily in Calliphoridae but are today generally regarded as a distinctfamily. While the subfamily division of the Sarcophagidae is stable, withsubfamilies Macronychiinae, Miltogrammatinae, Paramacronychiinaeand Sarcophaginae recognized, there is presently little agreement amongresearchers on rank, nomenclature and composition of tribal, genericand subgeneric categories. Pape (1996) presented a world catalogue ofthe Sarcophagidae and it is his taxonomic nomenclature that we haveadopted here for taxa at generic through species level. For tribal affinities




of malacophagous species we follow de Souza Lopes (1982a) and Povolnyand Verves (1997).

Sarcophagid adults (Fig. 3.3c,d) are mostly grey, with the abdomengenerally chequered grey and black. The eyes are often bright red. Theseflies feed at flowers for nectar. The males are said to have ‘stations’, wherethey wait for passing females.

The immature stages of Sarcophagidae have been described byThompson (1920), Greene (1925), Schumann (1954), Sanjean (1957),Povolny and Groschaft (1959), Zumpt (1965), de Souza Lopes (1966,1982a), Ishijima (1967), Ramachandran Nair (1968), Draber-Moñko(1973a,b), Oldroyd and Smith (1973), Denno and Cothran (1975), Tibana(1976), Nandi (1980), O’Flynn and Moorhouse (1980), Cantrell (1981),Zhang (1982), de Souza Lopes and Tibana (1984), Ferrar (1987), Shewell(1987b), Smith (1989) and others. There is great diversity of larval lifestrategies evident in the family – see Rohdendorf (1967), Ferrar (1987),Povolny (1992), Pape (1996), and Povolny and Verves (1997) for reviewsthe larval biology. Povolny (1992) recognized five groups in Sarco-phagidae based on their larval feeding habits: (i) decomposers of animalcarcasses; (ii) decomposers of faeces, in which they may act as predatorsof other dipteran larvae; (iii) parasitoids of the large caterpillars ofbomycoid moths; (iv) parasitoids of earthworms; and (v) parasitoids ofgastropod snails. That both saprophagous and parasitoid sarcophagidsutilize gastropods has frequently led to uncertainty of the true nature ofassociation for species reared on gastropod cadavers. This uncertaintyis accentuated by the facultative interchange of necrophagous andparasitoid life strategies in many species. Sarcophagidae are knownas flesh flies because many of them feed as larvae on the soft tissues ofanimal bodies, often as agents of myiasis in vertebrates.

According to Rohdendorf (1967) the relationship between parasitoidSarcophagidae and their larval hosts indicates that they developed astrophic competitors with Calliphoridae. The primary status of the larvalfeeding in both families is necrophagy, but the sarcophagids prefersmall animal carrion (Denno and Cothran, 1975; Beaver, 1977; Hanskiand Kuusela, 1980; Verves and Narchuk, 1986; Pape, 1987). In generalCalliphoridae are oviparous, and larvae hatch from the eggs not priorto but after (several hours) oviposition has taken place. All species ofSarcophagidae are viviparous or (rarely) ovoviviparous, which providesa competitive advantage in small, ephemeral carrion. Furthermore,sarcophagid larvae will often aggressively exclude calliphorids and otherdipteran competitors from carrion (Denno and Cothran, 1975; Blackithand Blackith, 1984; Blackith, 1990).

The biology of the species-depaurate Macronychiinae is poorlyknown. Macronychia Rondani and Brachicoma Rondani are associatedwith social Hymenoptera (Séguy, 1941; van Emden, 1954; Smith, 1989).Thompson (1978) found larvae of Macronychia sp. as a parastoid of adultTabanidae (Diptera). The larvae of Miltogrammatinae, a somewhat largergroup, are predominantly kleptoparasites (food-parasites) in the nests of




solitary wasps and bees (Hymenoptera), especially those of fossorialspecies. A few miltogrammines are associated with termites, eitheras internal parasites or as predators. Others are parasites of variousOrthoptera, Diptera and bees. In many cases the first- and second-instarlarvae feed as parasitoids but the third-instar larvae are necrophagous.In the genus Eumacronychia Townsend several species are predators oflizard (Reptilia: Squamata, Sauria) and turtle (Reptilia: Testudines) eggs.The only known instance of Miltogrammatinae being associated with gas-tropods is that of a Miltogramma Meigen species recorded by Marikovskiy(1974) as a parasitoid of Bradybaena Beck sp. (Bradybaenidae).

The Paramacronychiinae comprises more than 100 species, mostlydistributed in the temperate northern hemisphere, with a few, evidentlyrelict species in the southern hemisphere. The subfamily is absent fromAustralia, New Guinea and New Zealand, and but for a single endemicspecies in the Galápagos Islands, is absent also from the entire Neotropi-cal region. Larvae are predominantly predators or parasitoids of insectsor pulmonate gastropods, although some are facultative scavengers ornecrophages. The genus Wohlfahrtia Brauer & Bergenstamm containsseveral species whose larvae are apparently obligate feeders in mamma-lian tissues, yet other species in the genus are saprophagous and attractedto carrion (e.g. Hegazi et al., 1991).

Eurychaeta muscaria (Meigen), a necrophagous-facultative parasitoidof helicid snails (Table 3.1), is often treated as a member of the Calli-phoridae (Rognes, 1986). Povolny and Verves (1997) recognized affinitieswith paramacronychiine Helicoboscini. The species is widely distributedin central and southern Europe to the Ukraine in the east, and in NorthAfrica to the south (Povolny and Verves, 1997). Little is known of itsbiology.

In paramacronychiine Paramacronychiini only two species areknown as parasitoids of gastropods, namely Nyctia halterata (Panzer) andSarcophila latifrons (Fallén). Both involve cases of facultative parasitism.The females splash their larvae into the respiratory opening of the snail(Verves, 1976) or deposit them specifically on the epiphragm of aestiva-ting snails (Neck and de Souza Lopes, 1973). Nyctia Robineau-Desvoidy isvery widely distributed in the Palaearctic. Pape (1996) recognized twospecies, while Povolny and Verves (1997) considered the genus mono-typic. N. halterata frequents humid forests, shrublands and meadows.This species has been reared from the hygromiid Xeropicta krynikii(Andrzejowski) in Iran (Povolny and Verves, 1997) and is known asa parasitoid of weevils in the genus Lixus Fabricius (Coleoptera:Curculionidae) (Smith, 1989). Pape (1996) catalogues seven species inthe genus Sarcophila Rondani, distributed throughout the Palaearcticand India. Povolny and Verves (1997) indicated that S. latifrons occursprimarily in mesophylic bushland. Larvae develop primarily in live anddead insects (Orthoptera, Coleoptera, Lepidoptera – see Povolny andVerves, 1997, for summary), but have also been reared from the helicid C.nemoralis in France (Richet, 1990). S. latifrons is occasionally implicated




108J.B

. Coupland and G

.M. B

arker

Dipteran Gastropod hosts RegionDipteran lifestrategy References

CalliphoridaeAmeniinae

Amenia leonina (Fabricius)

Amenia leonina albomaculata(Macquart)

Formosiomima nigromaculata(Malloch)

Paramenia semiauricepsBrauer & Bergenstamm

Calliphorinae, CalliphoriniMelinda caerula Meigen

Melinda gentilis Robineau-Desvoidy

Melinda itoi Kano

Pollenia rudis Fabricius

MelanomyinaeMelanomya obscura (Townsend)

Melanomya ordinaria (West)

Melanomya cyrtoneurina (Zetterstedt)

Melanomya pecchiolii (Rondani)

Camaenidae: Xanthomelon pachystylumPfeiffer

‘Snails’

Bulimulidae: Bothriembryon balteolus Iredale,Bothriembryon bulla (Menke),Bothriembryon glauerti Iredale

Camaenidae: Meridolum gulosum (Gould)

Helicidae: Theba pisana (Müller), Trichiahispida (Linnaeus); Discidae: Discusrotundatus (Müller); Hygromiidae:Cernuella virgata (da Costa), Helicella itala(Linnaeus). Zonitidae: Retinella Fischer sp.

Arionidae: Arion de Férussac sp.; Limacidae:Limax Linnaeus sp.; Hygromiidae:Candidula unifasciata (Pouret), Cernuellavirgata (da Costa), Helicella itala(Linnaeus)

Philomycidae: Incilaria bilineata (Benson);Bradybaenidae: Acusta despectasieboldiana (Pfeiffer)

Hygromiidae: Cernuella virgata (da Costa)

Succineidae: Succinea luteola Gould,Oxyloma retusa (Lea)

Succineidae: Succinea ovalis Say,Oxyloma retusa (Lea)

Succineidae: Oxyloma elegans (Risso),Oxyloma retusa (Lea)

‘Snail’

Australia

Australia

Australia

Australia

Europe

Europe

Japan

France

USA

USA

Europe, USA

Britain

Suspectedparasitoid

Suspectedparasitoid

Suspectedparasitoid

Suspectedparasitoid

Parasitoid

Parasitoid

Parasitoid

Facultativeparasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Hardy (1951), van Emden (1953)

Ferrar (1976)

Ferrar (1976)

Ferrar (1976)

Keilin (1919, 1921), Shipley (1920),Bequaert (1925), Schumann (1973),Godan (1983), Coupland (1994),Hopkins and Baker (1994)

Keilin (1919), Enderlein (1933),Schumann (1973), Godan (1983)

Ito (1962), Kano and Shinonaga(1968), Hori and Yamaguchi (1984)

Coupland (1994)

Reinhard (1929), Neck and De SouzaLopes (1973), Downes (1986),Ferrar (1987), Foote (1996)

Downes (1986), Foote (1996)

Cepelák and Rozkosn7 (1968),Downes (1986)

Keilin (1921), Audcent (1942), vanEmden (1954), Askew (1971),Chandler et al. (1978), Downes(1986)

Table 3.1. List of host records sourced from the literature for malacophagous Diptera in the families Calliphoridae, Rhinophoridae, Phoridae, Muscidae,Fanniidae and Sarcophagidae.

108



Tuesday, May 18, 2004 11:56:01 AM



Diptera as P


109

RhinophoridaeMelanophora helicivora Goureau

PhoridaePhorinae

Chaetopleurophora bohemanni(Becker)

Spiniphora bergenstammi (Mik)

Spiniphora excisa Becker

Spiniphora helicivora Dufour

Spiniphora maculata (Meigen)

MetopininaeMegaselia aequalis (Wood)

Megaselia biformis Brues

Megaselia ciliata (Zetterstedt)

Megaselia fuscinervis (Wood)

Megaselia javicola (Beyer)

Megaselia perdita (Malloch)

Megaselia spiracularis Schmitz

Megaselia Rondani sp.

Megaselia Rondani sp.

Hygromiidae: Xerotricha conspurcata(Draparnaud)

Helicidae: Helix pomatia Linnaeus

Helicidae: Arianta arbustorum (Linnaeus),Cepaea hortensis (Müller), Cepaeanemoralis (Linnaeus), Helix pomatiaLinnaeus

Helicidae: Cepaea hortensis (Müller),Cepaea nemoralis (Linnaeus),Helicigona lapicida (Linnaeus)

Helicidae: Helix Linnaeus spp.

Helicidae: Cantareus aspersus (Müller),Eobania vermiculata (Müller), Thebapisana (Müller); Hygromiidae: Cernuellavirgata (da Costa)

Agriolimacidae: Deroceras laeve (Müller)eggs

Achatinidae: Achatina fulica Bowdich

Agriolimacidae: Deroceras RafinesqueSchmaltz sp. eggs; Arionidae: Arion deFérussac sp. eggs.

Zonitidae: Vitrea contracta (Westerlund),Vitrea crystallina (Müller)

Achatinidae: Achatina fulica Bowdich

Bulimulidae: Drymaeus dormani (Binney)

Bradybaenidae: Bradybaena seiboldiana(Pfeiffer)

Agriolimacidae: Deroceras laeve (Müller)eggs

Agriolimacidae: Deroceras reticulatum(Müller) eggs

France

Europe

Europe

Europe

Europe

Europe, NorthAfrica

USA

HawaiianIslands

Britain

Britain

Indonesia

USA

Orient

North America

Europe


Suspectedfacultativeparasitoid





Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitic

Facultativepredator

Parasitoid

Parasitoid

Parasitoid

Goureau (1843)

Lundbeck (1920), Robinson and Foote(1968), Godan (1983)

Bergenstamm (1864), Mik (1864),Keilin (1911), Schmitz (1917),Robinson and Foote (1968), Godan(1983)

Lundbeck (1920), Robinson and Foote(1968), Godan (1983)

Kidd and Brindle (1959), Robinsonand Foote (1968), Godan (1983)

Dufour (1841), Keilin (1911), Taylor(1914), Robinson and Foote (1968),Godan (1983), Coupland (1994)

Stephenson (1965), Stephenson andKnutson (1966), Robinson andFoote (1968), Robinson (1971,1981), Godan (1983), Disney (1994)

Brues (1942), Robinson and Foote(1968), Godan (1983)

Disney (1977, 1979, 1994)

Disney (1982, 1994)

Beyer (1959), Hardy and Beyer(1964), Disney (1994)

Muma (1954, 1955), Robinson (1981),Disney (1994)

Borgmeier (1967), Robinson andFoote (1968), Godan (1983)

Robinson (1965)

Stephenson (1965)

continued

109



Tuesday, May 18, 2004 11:56:01 AM



110J.B

. Coupland and G

.M. B

arker


Puliciphora borinquenensis Wheeler

Wandolleckia achatinae Cook

MuscidaeMuscinae, Muscini

Musca domestica Linnaeus

Reinwardtiinae, ReinwardtiiniCharadrella malacophaga

de Souza Lopes

Muscina levida (Harris)(= assimilis Fallén)

Muscina stabulans (Fallén)

Phaoniinae DichaetomyiiniAlluaudinella bivittata (Macquart)

Ochromusca trifaria Bigot

FanniidaeFannia scalaris (Fabricius)

Fannia canicularis (Linnaeus)

SarcophagidaeMittogrammatinae Mittogrammatini

Miltogramma Meigen sp.

‘Snails’

Achatinidae: Achatina de Lamarck sp.,including Achatina achatina (Linnaeus),Achatina variegata Roissy, Archachatinaventricosa (Gould), Pseudotrochus Adams& Adams sp.

Helicidae: Helix Linnaeus sp.

Bulimulidae: Thaumastus taunaysi (deFérussac); Streptaxidae: StreptaxisGray sp.

Helicidae: Cepaea nemoralis (Linnaeus)

Helicidae: Cantareus aspersus (Müller);Hygromiidae: Perforatella bidentata(Gmelin)

Achatinidae: Achatina de Lamarck sp.,Butroa nilotica (Pfeiffer)

Achatinidae: Achatina de Lamarck sp.,Achatina craveni Smith

Helicidae: Cantareus aspersus (Müller)

Helicidae: Cantareus aspersus (Müller),Cepaea hortensis (Müller), Cepaeanemoralis (Linnaeus), Helix pomatiaLinnaeus, Theba pisana (Müller);Hygromiidae: Cernuella virgata (da Costa)

Bradybaenidae: Bradybaena Beck sp.

North America

Belgian Congo,Liberia,Tanzania

Europe

Brazil

Europe

Europe

Africa

Africa

Europe

Europe

Russia

Parasitoid

Parasitic

Facultativepredator

Parasitoid

Facultativepredator


Suspected predatoror parasitoidbut probablysaprophagous

Suspectedfacultativeparasitoidbut possiblysaprophagous



Parasitoid

Borgmeier (1963), Robinson andFoote (1968), Godan (1983)

Cook (1897), Wandolleck (1898),Brues (1903), Schmitz (1916, 1917,1929a, 1958), J. Bequaert inPilsbry (1919), Bequaert (1925),Baer (1953)

Keilin (1919), Anon. (1920), Séguy(1921)

de Souza Lopes (1938), de OliveiraAlbuquerque (1947), de Carvalho(1980), Skidmore (1985)

Keilin (1917), Beaver (1972)

Séguy (1921), Mokrzecki (1923),Skidmore (1985)

Rodhain and Bequaert (1916), J.Bequaert in Pilsbry (1919), Keilin(1919), Paterson (1958), Skidmore(1985)

van Emden (1949, 1956), Paterson(1958), Disney (1970, 1973), Pontand Dear (1976), Skidmore (1985),Beaver (1986a)

Séguy (1921), Mokrzecki (1923)

Keilin (1911, 1919), Coupland (1994)

Marikovskiy (1974)

Table 3.1. Continued.

110



Tuesday, May 18, 2004 11:56:02 AM



Diptera as P


111

Paramacronychiinae, HelicobosciniEurychaeta muscaria (Meigen)

Paramacronychiinae, ParamacronychiiniNyctia halterata (Panzer)

Sarcophila latifrons (Fallén)

Sarcophaginae CuculomyiniTitanogrypa (Sarconeiva) fimbriata

(Aldrich) (= larvivorax de SouzaLopes)

Udamopyga cubana de Souza Lopes

Udamopyga malacophila de SouzaLopes

Udamopyga neivai de Souza Lopes

Udamopyga setigena (Enderlein)

Sarcophaginae JohnsoniiniLepidodexia (Johnsonia) sp.

cf. frontalis AldrichLepidodexia (Johnsonia) elegans

Coquillett

Lepidodexia (Notochaetisca)malacophaga (de Souza Lopes)

Lepidodexia (Johnsonia) rufitibia (Wulp)Malacophagula neotropica Bequaert

Sarcodexiopsis biseriata (Aldrich)Sarcophaginae Sarcodexiini

Helicobia morionella (Aldrich)

Helicobia rapax (Walker)(= helicis Townsend)

Peckiamyia expuncta de Souza Lopes

Helicidae: Arianta arbustorum (Linnaeus),Theba pisana (Müller)

Hygromiidae: Xeropicta krynikii(Andrzejowski)

Helicidae: Cepaea nemoralis (Linnaeus)

Bradybaenidae: Bradybaena similaris(de Férussac)

Bulimulidae: Lopesianus crenulatusWeyrauch

Bulimulidae: Thaumastus taunaysi(de Férussac)

Bulimulidae: Thaumastus taunaysi(de Férussac)

Acavidae: Strophocheilus intertextus Pilsbry;Ampullariidae: Pomacea insularum(d’Orbigny)


Bulimulidae: Drymaeus dormani (Binney);Succineidae: Succinea ovalis Say,Succinea cf. indiana Pilsbry, Succinealuteola floridana Pilsbry

Bulimulidae: Peltella Webb & vanBeneden sp.

Polygyridae: Polygyra texasiana (Moricand)Bulimulidae: Bulimulus tenuissima de

FérussacBulimulidae: Rabdotus mooreanus (Pfeiffer)


Bulimulidae: Orthalicus reses reses (Say);Helicidae: Cepaea hortensis (Müller);Polygyridae: Polygyra thyroides (Say)

Bradybaenidae: Bradybaena similaris(de Férussac); Bulimulidae: Thaumastustaunaysi (de Férussac)

Europe

Iran

Europe

Brazil

Cuba

Brazil

Brazil

Paraguay

USA

USA

Brazil

USABrazil

USA

USA

USA

Brazil



Suspectedparasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

ParasitoidParasitoid

Parasitoid



Parasitoid

Perris (1850), Schmitz (1910, 1917),Godan (1983), Povoln7 and Verves(1997)

Povoln7 and Verves (1997)

Richet (1990)

de Souza Lopes (1940)





Muma (1954, 1955), Stegmaier (1972)

Aldrich (1916), Muma (1954, 1955),Downes (1965), Stegmaier (1972),Reeves et al. (2000)


Neck and de Souza Lopes (1973)Bequaert (1925), de Souza Lopes

(1940)Neck and de Souza Lopes (1973)

Muma (1954, 1955), Stegmaier (1972)

Townsend (1892), Aldrich (1916),Keilin (1919), Godan (1983), Deisler(1987)


continued

111



Tuesday, May 18, 2004 11:56:02 AM



112J.B

. Coupland and G

.M. B

arker


Sarcodexia lambens (Wiedemann)(= sternodontis Townsend)

Sarcophaginae RaviniiniRavinia pernix (Harris) (= striata

Fabricius; haematodes Meigen)Sarcophaginae Sarcophagini

Sarcophaga (Baranovisca) nr banksiSenior-White

Sarcophaga (Bellieriomima) subulata(Pandellé)

Sarcophaga (Bercaea) africa(Wiedemann) (= crueuntata Meigen)

Sarcophaga (Bercaea) footei Dodge

Sarcophaga (Discachaeta) arcipesPandellé

Sarcophaga (Discachaeta) cucullansPandellé

Sarcophaga (Discachaeta) pumilaMeigen

Sarcophaga (Helicophagella) agnataRondani

Sarcophaga (Helicophagella)crassimargo Pandellé

Sarcophaga (Helicophagella) hirticrusPandellé

Sarcophaga (Helicophagella) maculataMeigen

Bulimulidae: Drymaeus dormani (Binney),Orthalicus reses reses (Say);Streptaxidae: Plagiodentes meieriWeyrauch, Plagiodentes multiplicatus(Doering), Spixia juradoi Parodiz, Spixiapseudosexdentatus Doering


Achatinidae: Achatina fulica Bowdich*;Ariophantidae: Ariophanta belangeri(Deshayes), Ariophanta bistrialis (Beck),Cryptozona semirugata (Beck); Enidae:Rachis punctatus (Anton)*

‘Snails’

Helicidae: Cantareus asperasus (Müller),Cepaea nemoralis (Linnaeus), Eobaniavermiculata (Müller), Theba pisana (Müller);Hygromiidae: Cernuella virgata (da Costa)

Polygyridae: Triodopsis notata (Deshayes)

Hygromiidae: Euomphalia strigella(Draparnaud), Xerolenta obvia (Menke)

Helicidae: Theba pisana (Müller);Hygromiidae: Cernuella virgata (da Costa)

Helicidae: Theba pisana (Müller);Hygromiidae: Cernuella virgata (da Costa)


Hygromiidae: Cernuella virgata (da Costa)

Helicidae: Cantareus aspersus (Müller),Theba pisana (Müller); Hygromiidae:Cernuella virgata (da Costa)

Terrestrial gastropods; Helicidae: Thebapisana (Müller)

Argentina,USA

Afghanistan,Europe

India

Europe

USA

Europe,Ukraine

France,Spain

Israel

Europe

Europe

Europe

Afghanistan,England,France

Possible facultativeparasitoid


Parasitoid



Suspectedparasitoid

Parasitoid

Parasitoid

Suspectedparasitoid

Necrophagous topseudoparasitoid

Necrophagous tosecondaryparasitoid



Muma (1954, 1955), de Souza Lopes(1969a), Deisler (1987)

Séguy (1921), Verves (1980)

Ramachandran Nair (1968)


Berner (1960, 1973), Povoln7 andVerves (1990, 1997), Hopkins andBaker (1993)

Dodge (1963)

Povoln7 and Groschaft (1959), Vervesand Kuzmovich (1979), Povoln7and Verves (1990)

Lehrer (1966), Hopkins and Baker(1993), Coupland (1994)

Harpaz and Oseri (1961)

van Emden (1954), Povoln7 andVerves (1990)

Keilin (1919), Povoln7 and Verves(1990)

Barfoot (1969), Beaver (1972),Hopkins and Baker (1993),Coupland (1994), Povoln7 andVerves (1997)

Verves (1980), Coupland (1994)


112

A4784 - 112.prn

Z:\Customer\CABI\A4743 - Barker\A4784 - Barker - Voucher Proofs #J.vp

Monday, June 07, 2004 11:22:11 AM



Diptera as P


113

Sarcophaga (Helicophagella) melanuraMeigen

Sarcophaga (Helicophagella) novercaRondani

Sarcophaga (Heteronychia) balaninaPandellé

Sarcophaga (Heteronychia) bezzianaBöttcher

Sarcophaga (Heteronychia)boettcheriana (Rohdendorf)

Sarcophaga (Heteronychia) dissimilisMeigen

Sarcophaga (Heteronychia) fertoniVilleneuve

Sarcophaga (Heteronychia) filiaRondani

Sarcophaga (Heteronychia) graeca(Rohdendorf)

Sarcophaga (Heteronychia)haemorrhoa Meigen

Sarcophaga (Heteronychia)haemorrhoides Böttcher

Sarcophaga (Heteronychia) mutilaVilleneuve

Sarcophaga (Heteronychia)nigricaudata Povoln7 & Slamecková(= rohdendorfiana Mihályi)

Sarcophaga (Heteronychia) penicillataVilleneuve

Arionidae: Arion hortensis de Ferussac;Helicidae: Cantareus aspersus (Müller)

Helicidae: Caucasotachea atrolabiata(Krynicki), Helix pomatia Linnaeus, HelixLinnaeus sp.

Helicidae: Eobania vermiculata (Müller),Theba pisana (Müller)

Chondrinidae: Chondrina Reichenbach spp.;Clausiliidae: Clausilia Draparnaud spp.

Helicoid snails, including Helicidae: HelixLinnaeus sp. and Cepaea hortensis(Müller)

Hygromiidae: Monachoides Gude &Woodward sp.

Hygromiidae: Trochoidea simulata(Ehrenberg)

Helicidae: Helix Linaeus spp., Theba pisana(Müller); Hygromiidae: Cernuella virgata(da Costa)

Helicidae: Theba pisana (Müller);Hygromiidae: Cernuella virgata (da Costa),Cochlicella acuta (Müller), Trochoideaelegans (Gmelin)

Helicoid snails, including Helicidae: HelixLinnaeus sp. and Cepaea hortensis (Müller)

Helicidae: Cantareus aspersus (Müller),Cepaea nemoralis Linnaeus, Eobaniavermiculata (Müller)

Helicidae

Helicidae: Arianta arbustorum (Linnaeus),Hygromiidae: Monachoides incarnata(Müller); Bradybaenidae: Bradybaenafruticum (Müller)

Hygromiidae: Cochlicella acuta (Müller),Prieticella barbara (Linnaeus)

France

Maastricht,Russia

France, Spain

Bulgaria

Bulgaria

Europe

Israel

France

France,Portugal,Spain

Europe

France

Balkancountries

Bratislava

France, Italy,Morocco,Portugal,Spain



Parasitoid

Parasitoid

Parasitoid

Parasitoid

Suspectedparasitoid

Parasitoid

Suspectedparasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Keilin (1919, 1921), Baer (1921),Séguy (1921, 1941), Stephensonand Knutson (1966), Godan (1983),Povoln7 and Verves (1990)

Portschinskij (1887a), Schmitz (1910,1917), Povoln7 and Verves (1990)

Hopkins and Baker (1993), Coupland(1994), Baker (2002)



Povoln7 and Verves (1990, 1997)

J. Heller in Coupland and Baker(1994)

Rostand (1920), Keilen (1921),Povoln7 and Verves (1990), Hopkinsand Baker (1993), Coupland (1994)

Coupland (1994), Coupland and Baker(1994)

Mik (1890), Portschinskij (1894),Schmitz (1917), Keilin (1919),Godan (1983), Povoln7 and Verves(1990, 1997)

Berner (1973), Verves (1976), Povoln7and Verves (1990), Povoln7 (1992)

Povoln7 and Verves (1990, 1997)

Povoln7 (1982)

Povoln7 (1992), Hopkins and Baker(1993), Coupland and Baker (1994),Coupland (1994), Baker (2002)

continued

113



Tuesday, May 18, 2004 11:56:02 AM



114J.B

. Coupland and G

.M. B

arker


Sarcophaga (Heteronychia)portschinskyana (Rohdendorf)

Sarcophaga (Heteronychia) proximaRondani

Sarcophaga (Heteronychia) siciliensisBöttcher

Sarcophaga (Heteronychia) uncicurvaPandellé

Sarcophaga (Heteronychia) vagansMeigen

Sarcophaga (Heteronychia) vicinaMacuart

Sarcophaga (Krameromyia) anacesWalker

Sarcophaga (Liosarcophaga) emdeni(Rohdendorf)

Sarcophaga (Liosarcophaga) kirgizica(Rohdendorf)

Sarcophaga (Liosarcophaga)portschinskyi Rohdendorf

Sarcophaga (Liosarcophaga)teretirostris Pandellé

Sarcophaga (Liosarcophaga)tuberosa Pandellé

Sarcophaga (Myorhina) nigriventrisMeigen

Helicidae: Theba pisana (Müller)

Hygromiidae: Euomphalia strigella(Draparnaud)

‘Snails’

Helicidae: Eobania vermiculata (Müller),Theba pisana (Müller); Hygromiidae:Cernuella virgata (da Costa)

Helicidae: Eulota maacki Gerstfeldt;Succineidae: Succinea Draparnaud spp.

‘Snails’

Helicidae: Cepaea nemoralis (Linnaeus),Theba pisana (Müller); Hygromiidae:Cernuella explanata (Muller), Cernuellavirgata (da Costa), Cochlicella acuta(Muller)

Helicidae: Cepaea nemoralis (Linnaeus);Hygromiidae: Xerolenta obvia (Menke)



Helicidae: Cepaea nemoralis (Linnaeus),Otala lactea (Müller), Theba pisana(Müller); Hygromiidae: Cernuella virgata(da Costa), Xerolenta obvia (Menke)

Enidae: Brephulopsis cylindrica (Menke);Helicidae: Cantareus aspersus (Müller),Eobania vermiculata (Müller), Helixpomatia Linnaeus, Cepaea nemoralis(Linnaeus), Eobania Hesse sp., Theba

Europe,includingFrance,Spain

CzechRepublic,Russia

France, Spain

EasternRussia

Not given

Europe

Europe

ZayliyskiyAlatau Mts

Bulgaria,France

Europe

Russia

England,France,Spain,CentralEurope

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Parasitoid

Facultativeparasitoid/predator






Povoln7 and Verves (1990), Coupland(1994)

Povoln7 and Groschaft (1959), Povoln7and Verves (1990), Y. Verves inPovoln7 and Verves (1997)

Povoln7 (1992)

Coupland (1994), Baker (2002),Coupland and Baker (1994)

Verves (1976), Artamonov (1985),Povoln7 and Verves (1990)


Böttcher (1912), Richet (1990),Povoln7 and Verves (1990),Hopkins and Baker (1993),Coupland (1994)

Verves and Kuzmovich (1979), Richet(1990)

Marikovskiy (1974)

Povoln7 and Verves (1990), Hopkinsand Baker (1993)

Keilin (1919), de Souza Lopes (1940),Séguy (1941), Beaver (1972, 1973),Richet (1990), Coupland (1994)

Rohdendorf (1937), Artamonov (1987)

Böttcher (1913), Bowell (1917), Keilen(1919, 1921), (Taylor, 1921), Séguy(1941, 1953, 1965), van Emden(1954), Miles (1968), Barfoot(1969), Askew (1971), Beaver


114



Tuesday, May 18, 2004 11:56:03 AM



Diptera as P


115

Sarcophaga (Myorhina) sororcula(Rohdendorf)

Sarcophaga (Myorhina) sorror Rondani

Sarcophaga (Pandelleisca) similisMeade

Sarcophaga (Paraethiopisca) misera(Walker)

Sarcophaga (Poecilometopa)spilogaster (Wiedemann)

Sarcophaga (Sarcophaga) variegata(Scopoli) (=S. carnaria auct. not L.)

Sarcophaga (Sarcorohdendorfia)megafilosia Pape, Mckillup & McKillup

Sarcophaga (Sarcorohdendorfia)meiofilosia Pape, Mckillup & McKillup

Sarcophaga (Thyrsocnema)incisilobata Pandellé

Sarcophaga Meigen sp.

Sarcophaga Meigen sp.

Sarcophaga (Bercaeopsis) parallelaAldrich

Sarcophaga (Bercaeopsis) mimorisReinhard

Sarcophaga (Bercaeopsis) fortisaReinhard (= helicivora Dodge)

pisana (Müller); Hygromiidae: Cernuellavirgata (da Costa), Helicella itala(Linnaeus), Xerolenta obvia (Menke),Candidula intersecta (Poiret), Monachacantiana (Montagu)



Succineidae: Succinea Draparnaud sp.

Planorbidae: Indoplanorbis exustusDeshayes

Helicidae: Cantareus aspersus (Müller),Caucasotachea atrolabiata (Krynicki),Eobania vermiculata (Müller), Thebapisana (Müller); Succineidae: SuccineaDraparnaud spp.

Littorinidae: Littoraria filosa (Sowerby)

Littorinidae: Littoraria filosa (Sowerby)

Helicidae: Otala lactea (Müller)

Ariophantidae: Ariophanta bistrialis (Beck)*,Ariophanta belangeri (Deshayes)*,Cryptozona semirugata (Beck)*;Enidae: Rachis punctatus (Anton)


Polygyridae: Polygyra thyroides (Say)

Zonitidae: Ventridens ligera (Say)

Zonitidae: Ventridens ligera (Say)

ZayliyskiyAlatau Mts

France,Russia

EasternRussia,Europe

India

Africa

France,Caucasus

Australia

Australia

Europe

India

Israel

New York,USA

Michigan,USA

Michigan,USA

Parasitoid, probablyfacultative



Parasitoid



Parasitoid

Parasitoid


Parasitoid

Suspectedparasitoid

Suspectedparasitoid

Suspectedparasitoid

Suspectedparasitoid

(1972), Richardson (1974),Cameron and Disney (1975), Pape(1987), Povoln7 and Verves (1990,1997), Richet (1990), Hopkins andBaker (1993), Coupland (1994)

Marikovskiy (1974)

Séguy (1921), Rohdendorf (1937),Povoln7 and Verves (1990)

Artamonov (1983), Povoln7 andVerves (1990)

Parashar et al. (1997)

Cuthbertson (1938), Ferrar (1987)

Mik (1890), Portchinskji (1887b),Séguy (1921), Berner (1960, 1973)

McKillup et al. (2000), Pape et al.(2000), McKillup and McKillup(2000, 2002)

McKillup et al. (2000), Pape et al.(2000), McKillup and McKillup(2000, 2002)

Meade (1897), Keilin (1919), Povoln7and Verves (1990)

Ramachandran Nair (1968)

Moran (1987)

W.T. Davis in Bequaert (1925),Hallock (1942), Dodge (1956)

Dodge (1956)

Dodge (1956)

*Experimental hosts.

115

A4784 - 115.prn

Z:\Customer\CABI\A4743 - Barker\A4784 - Barker - Voucher Proofs #J.vp

Monday, June 07, 2004 11:23:07 AM



in cases of cutaneous myiasis in mammals (Portschinskij, 1876; Séguy,1941).

The subfamily Sarcophaginae is both highly speciose (c. 1600 speciesknown) and biologically diverse. It is best represented in the Neotropics,and remarkably poorly in the Afrotropical and Australasian/Oceaniaregions. The subfamily comprises mostly large (up to 23 mm), robustflies, although in species of the genera Tricharaea Thomson and Sarco-phagula Wulp the adults are small. Larvae of some Sarcophaginae areassociated with dung as either coprophages or predators of coprophagousDiptera. Similarly in carrion or decaying vegetation. While predationis generally facultative, a number of Sarcophaginae such as Sarconeivade Souza Lopes and Cucullomyia Roback, in Johnsoniini, have becomeobligate predators. The victims are killed by extra-intestinal neurotoxins(de Souza Lopes, 1973). Many Sarcophaginae are parasitoids of insects,spiders or gastropods. Several species produce myiasis in vertebratessuch as turtles, lizards, amphibians and mammals – a number of speciesin the genus Sarcophaga Meigen and allies have been implicated inintestinal and other types of myiasis in humans. The dual necrophagous–predatory or necrophagous–parasitic feeding strategies of numerousspecies enable them to feed in different trophic substrates accordingto their availability.

The sarcophagine Raviniini comprise more than 130 species, widelydistributed in the Americas and Oceania, and less well represented else-where. The single Palaearctic species Ravinia pernix (Harris) (= striataFabricius), with range extending into the northern Oriental region, haslarvae that principally develop in animal excreta and carrion, butfacultatively predate on coprophilous insect larvae, or parasitize variousinsects. It is also known to produce myiasis in humans (see Povolny andVerves, 1997, for summary). Verves (1980) mentions a case of parasitismin Afghanistan gastropods (Table 3.1).

Among Cuculomyini, parasitism in gastropods is known in theNeotropic–South American Titanogrypa (Sarconeiva) fimbriata (Aldrich),Udamopyga cubana de Souza Lopes and Udamopyga malacophila deSouza Lopes, Udamopyga neivai de Souza Lopes and Udamopygasetigena (Enderlein) (Table 3.1). The biology of these species is, however,poorly known. The South American Malacophagomyia filamenta (Dodge)is evidently a saprophage, having been repeatedly reared from larvaeoccurring in dead terrestrial and freshwater gastropods in Brazil, and bredin the laboratory on decaying mammal flesh (de Souza Lopes, 1966).

The sarcophagine tribe Johnsoniini comprises more than 150 species.They occur primarily in the Neotropics, but 20 species are known fromthe Nearctic, one from the Holarctic and one from Australia. Larvae aregenerally parasites of insects, earthworms, gastropods, amphibians andreptiles, and are facultatively necrophagous in bird nests. Malacophagyis known in the American genera Lepidodexia Brauer & Bergenstamm(including subgenera Notochaetisca de Souza Lopes and JohnsoniaCoquillett), Malacophagula Bequaert and Sarcodexiopsis Townsend




(Table 3.1). Of these malacophagous Johnsoniini, the biology is bestknown for members of Lepidodexia (Johnsonia), which occur throughoutthe temperate and tropical Americas. Lepidodexia (Johnsonia) elegansCoquillett occurs naturally in the southern USA. Aldrich (1916) reportedthis species from Succinea ovalis Say (Succineidae) on citrus (CitrusLinnaeus, Rutaceae) in Mexico, Muma (1954, 1955) reported rearing thisspecies from the bulimulid D. dormani infesting citrus trees in Florida,and Stegmaier (1972) recorded parasitism of Succinea luteola Gouldon dead ragweed (Amrosia Linnaeus, Asteraceae) in Florida. Mumaobserved parasitism in immature D. dormani 6–12.5 mm in shell height.The larva fed primarily in the apex of the shell, consuming visceral tis-sues. The parasitized hosts were always observed tightly attached to thesubstrate. Before pupation, the larva cleaned out the interior of the host’sshell by forcing remnant host tissues to the exterior. Pupation of this flyoccurred within the shell of the host, with the anterior spiracles directedtoward the shell aperture.

Lepidodexia (Johnsonia) rufitibia (Wulp) parasitizing Polygyratexasiana (Moricand) generally leaves the host’s shell to pupate, a factthat Neck and de Souza Lopes (1973) attribute to the smallness of the shelland the presence of apertural teeth.

The records of Sarcophaginae Sarcodexiini from terrestrial gastropodsare restricted to Helicobia morionella (Aldrich), Helicobia rapax (Walker)(= helicis Townsend), Peckiamyia expuncta de Souza Lopes and Sarco-dexia lambens (Wiedemann) (= sternodontis Townsend) (Table 3.1). Thegenus Helicobia Coquillett occurs throughout the Americas, albeit mostdiverse and abundant in the Neotropics. H. morionella ranges from south-ern USA to Argentina, while H. rapax occurs from Canada to Argentina.Stegmaier (1972, p. 237) regarded H. morionella as a ‘general saprophage’,but acknowledged that the species had been reared from terrestrial gastro-pods. Muma (1954, 1955) reported rearing of H. morionella from livingD. dormani in Florida. The larvae occurred as solitary parasitoids thatexited the shell of the host to pupate in the soil. Parasitism occurred fromMay through August (spring–summer). H. rapax has been repeatedlyreared from terrestrial gastropods (Townsend, 1892; Aldrich, 1916;Keilin, 1919; Godan, 1983; Deisler, 1987) in a manner suggestive of aparasitoid relationship. Aldrich (1916) reported H. rapax from variouslive arthropods, including Orthoptera. None the less, Helicobia adults arereadily attracted to carrion (e.g. Gregor, 1972; Cornaby, 1974; Goff et al.,1986) and H. rapax has been reared from larvae occurring in variousinvertebrate carrion, including that of gastropods (Stegmaier, 1972), andtherefore must be regarded as a facultative parasitoid.

S. lambens, widespread in the Americas from southern USA toArgentina, has been reared from a number of insects (Greene, 1925;Callan, 1946; Downes, 1965; Dodge, 1968; Stegmaier, 1972) and gastropodspecies (Muma, 1954, 1955; de Souza Lopes, 1969a; Stegmaier, 1972;Deisler, 1987) (Table 3.1). Dodge (1968) referred to this species asa parasitoid but at best this species must be regarded as a facultative




parasitoid as it is readily reared on artifical media in the laboratory.S. lambens developing in gastropod snails leaves the shell of the host topupate in the soil. Adult flies are attracted to carrion and faeces (Gregor,1972; Cornaby, 1974).

Amongst Sarcophagini, subgenera of the large genus Sarcophaga aregenerally defined on perceived similarities in the structurally complexmale genitalia which, as noted by Pape et al. (2000), are not easily put intodescriptive terms and unambiguous diagnoses. The few modern attemptsat explicit phylogenetic definitions of selected subgenera have obtainedweak support for monophyly (e.g. Blackith et al., 1998, for the Palaearcticsubgenus Helicophagella Enderlein). Supra-specific classification withinthe Sarcophagini, and probably the entire Sarcophaginae, is thus to beconsidered tentative.

A number of Sarcophaga are facultative parasitoids or predatorsof terrestrial gastropods. Sarcophaga s. str. comprises about 19 speciesconfined to the western Palaearctic. According to Povolny and Verves(1997) these species primarily are parasitoids of earthworms, although thelarval biology of a number of species has yet to be investigated. Severalspecies in Sarcophaga s. str. are indeed parasitoids of earthworms butfacultatively utilize other substrates. Sarcophaga subvicina Rohdendorf,for example, parasitizes earthworms (Kirchberg, 1954, 1961), but has alsobeen reared as a saprophage from a dead Limax Linnaeus sp. (Limacidae)and maintained on mammal flesh in the laboratory (Pollock, 1972;Baudet, 1982; Blackith and Blackith, 1984; Pape, 1987). Sarcophaga(Sarcophaga) variegata (Scopoli) (= carnaria auct. not of Linnaeus),the only species in the subgenus recorded as a facultative parasitoid ofterrestrial gastropods, is also a parasitoid of earthworms (Eberhard andSteiner, 1952; Kirchberg, 1954, 1961; Pape, 1987). As summarized byPovolny and Verves (1997), S. variegata has also been reared as a para-sitoid of the pupal stage of various Lepidoptera and has been successfullybred in the laboratory on mammalian flesh. Povolny and Verves (1997)express doubt about the validity of earlier records of this speciesoccurring in Orthoptera and causing myiasis in vertebrates. The recordsof S. variegata as a parasitoid of terrestrial gastropods (Table 3.1) arepresently restricted to members of the Helicidae, Hygromiidae andSuccineidae (Mik, 1890; Portchinskji, 1887b; Séguy, 1921; Berner, 1960,1973). S. variegata occurs widely in the Palaearctic, in a range of lowlandto alpine habitats.

There are numerous other cases of facultative parasitism of gastro-pods by Sarcophaga reported in the literature (Table 3.1). Sarcophaga(Bercaea) Robineau-Desvoidy is a small group of sarcophagini, mostdiverse in the Afrotropical region but extending throughout the Holarcticand into the Oriental and Neotropical regions. According to Povolnyand Verves (1997) species in this subgenus are primarily coprophagousand predaceous. Sarcophaga (Bercaea) africa (Wiedemann) (= crueuntataMeigen; haemorrhoidalis auct., not of Fallén), with a distributionapproaching that of the entire subgenus and with strong synanthropic




tendencies, is undoubtedly the best-known species. The adult flies feedon carrion, faeces and other decaying matter. S. africa has been bred fromhuman faeces and other animal excreta, terrestrial mammal carrion, andbeached cephalopod and echinoid carrion (references in Povolny andVerves, 1997). The species is known for producing myiasis in humans andother animals (Patton and Evans, 1929; Zumpt, 1965; Khan and Khan,1984) and as a vector of bacteria, protozoa and helminths of human healthsignificance (Sychevskaya and Petrova, 1958; Sychevskaya et al., 1959;Trofimov and Engelhardt, 1965; Nadzhafarov, 1967; Greenberg, 1971).Additionally, S. africa has been documented as a parasitoid of Orthoptera(Baer, 1921; Rees, 1973; Povolny and Verves, 1990), Lepidoptera (Povolnyand Verves, 1990) and various helicoid gastropods (Berner, 1960, 1973;Povolny and Verves, 1990, 1997; Hopkins and Baker, 1993) (Table 3.1).Sarcophaga (Bercaea) footei Dodge, a North American species, has beenreared from a polygyrid gastropod (Dodge, 1963) (Table 3.1), but thebiology of the species remains largely unknown.

According to Povolny and Verves (1997), the known species of thesubgenus Helicophagella are necrophagous, predaceous and pseudo-parasitoid on terrestrial snails. Sarcophaga (Helicophagella) crassimargoPandellé, a species widely distributed in the northern Palaearctic, haslarvae that are essentially copro-necrophagous (Sychevskaya, 1965). Nonethe less, it has been reared from Cernuella virgata (da Costa) (Hygro-miidae), in which it evidently occurred as an opportunistic parasitoid(Keilin, 1919). Povolny and Verves (1997) state that S. crassimargo avoidsforests, rather preferring open landscapes and very dry habitat withsparse vegetation. The adult flies feed at flowers and are readily attractedto decaying organic material. Sarcophaga (Helicophagella) novercaRondani is distributed over a greater part of Europe, associated with lowand mid-elevation forests. Adults feed at flowers and are attracted todecaying mammalian flesh and various types of animal excreta. Larvaefrequently develop in dead snails and are facultative parasitoids in Helixspecies (Portschinskij, 1887a; Schmitz, 1910, 1917; Povolny and Verves,1990). Eberhardt (1955) maintained S. noverca in the laboratory onmammalian flesh. Sarcophaga (Helicophagella) maculata Meigen occursin Europe, where it breeds in vertebrate faeces, and vertebrate and inver-tebrate carrion. This species has also been reared as a parasitoid fromColeoptera (Povolny and Verves, 1990) and terrestrial gastropods (Taylor,1914; Verves, 1980; Coupland, 1994).

Perhaps the best-known and biologically most-diverse species inthe subgenus Helicophagella is Sarcophaga (Helicophagella) melanuraMeigen. It occurs widely in the Holarctic, extending northward to theArctic Circle and south to the northern parts of the Orient, with prefer-ence for shrubland. Adults feed at flowers, faeces and decaying organicmatter, and, being strongly synanthropic, is regarded as a vector ofbacteria and helminths of human health significance (Akakhwedyanzand Zakharova, 1961; Greenberg, 1971). Larvae of S. melanura are mostlycoprophagous, and less frequently necrophagous (Povolny and Verves,




1997 and references therein). Additionally the larvae have been recordedas saprophagous and parasitoid in insects (Baer, 1921; Draber-Moñko,1973a), and as agents of myiases in birds and mammals (James, 1947; vanEmden, 1954). S. melanura has been reported as a facultative parasitoid ofArion hortensis de Férussac (Arionidae) and Cantareus aspersus (Müller)(Helicidae) (Keilin, 1919, 1921; Baer, 1921; Séguy, 1921, 1941; and others)(Table 3.1).

Larvae of Sarcophaga (Liosarcophaga) Enderlein are mostly sapro-phagous or coprophagous, with some species occurring as facultativepredators or parasitoids of invertebrates, including terrestrial gastropods.The subgenus comprises about 90 species represented in most regions ofthe world, but the only literature records available to us indicating afacultative to obligate parasitoid relationship with gastropods pertainedto species of the Palaearctic. Sarcophaga (Liosarcophaga) emdeni(Rohdendorf) occurs extensively in mid-latitude Europe eastward toSiberia and northwestern China, generally confined to lowland forestsand xeric shrublands. Its larvae are necrophagous and facultativeparasitoids of Lepidoptera (Khitzova, 1967; Trofimov, 1969; Povolny andVerves, 1990) and helicoid gastropods (Verves and Kuzmovich, 1979;Richet, 1990). Sarcophaga (Liosarcophaga) portschinskyi Rohdendorfoccurs extensively in the Palaearctic, from Europe, including Scandina-via, to southern Siberia, Asia Minor, Mongolia and China. It tends toprefer dry to xeric shrublands and warm lowland deciduous forests.S. portschinskyi adults feed at flowers and decaying organic matter, whilethe larvae develop as predators in faeces and animal carcasses (Trofimov,1969; Zhang, 1982; Artamonov, 1987; Pape, 1987; Povolny and Verves,1990, 1997). Rearing records from lepidopteran pupae (Girgfanova, 1962)and helicids (Povolny and Verves, 1990; Hopkins and Baker, 1993)indicate a probable facultative parasitoid life strategy in this species.Sarcophaga (Liosarcophaga) tuberosa Pandellé occurs widely in thePalaearctic, extending into the Orient and to North America. It is gener-ally an inhabitant of lowland deciduous forests. In brief summaries of thebiology, Povolny and Verves (1990, 1997) indicate that the adult flies visitflowers, ripe fruits and decaying organic matter, while the larvae arefacultative parasitoids of lepidopteran pupae. These authors suggest thatS. tuberosa probably also develops in other insects and that rearingrecords by Rohdendorf (1937) and Artamonov (1987) point to a facultativeparasitoid association with terrestrial gastropods. James (1947) mentionsthe participation of S. tuberosa in cutaneous myiases in humans.Sarcophaga (Liosarcophaga) teretirostris Pandellé is restricted to WesternEurope. Larvae develop in carrion (Povolny and Verves, 1997), includinggastropods (e.g. Beaver, 1972, 1973, 1977). None the less, rearing records(Keilin, 1919; de Souza Lopes, 1940; Séguy, 1941; Richet, 1990;Coupland, 1994) indicate a probable facultative parasitoid relationshipwith helicid and hygromiid gastropods (Povolny and Verves, 1997). Therates of parasitism can be high (Coupland, 1994). Marikovskiy (1974)records parasitism in Bradybaena sp. by the eastern Palaearctic species




Sarcophaga (Liosarcophaga) kirgizica (Rohdendorf). Several otherspecies, including Sarcophaga (Liosarcophaga) jacobsoni (Rohdendorf),are saprophagous scavengers or predators and readily utilize carrion,which includes dead gastropods (Richet, 1990).

Sarcophaga (Pandelleisca) similis Meade is widely distributed acrossthe Palaearctic and Oriental regions, from the British Isles to Japan.Povolny and Verves (1997) state that the adult flies are locally common inmesic forest habitats, feeding at flowers and on decaying organic material.The larvae are necrophagous, coprophagous and parasitoid. As facultativeparasitoids the larvae of S. similis occur in a range of invertebrates(Rohdendorf, 1937; Tiensuu, 1939; Kirchberg, 1954; Mihályi, 1965; Kanoet al., 1967), including succineid gastropods (Artamonov, 1983), and incases of myiasis in humans (James, 1947; Kano et al., 1967; Park, 1977).

Sarcophaga (Myorhina) Robineau-Desvoidy, with about 30 species, isdistributed widely in the Palaearctic, to the Orient and western Pacific.Povolny and Verves (1997) state that the majoity of these species arenecrophagous or are parasitoids of arthropods and gastropods. Some arethought to be obligate parasitoids of gastropods. Sarcophaga (Myorhina)nigriventris Meigen has been cited as a parasitoid of gastropod snails byAskew (1971), based largely on a note by Bowell (1917), who reared thespecies from dead and moribund Helicella itala (Linnaeus) (Hygromiidae).Keilin (1921), in contrast, only reared this species from snails that hadpreviously been killed by calliphorid parasitoids (see below). Addition-ally, several authors have demonstrated that S. nigriventris is able toutilize various types of carrion, including dead gastropods (e.g. Beaver,1972, 1973, 1977) as saprophagous larvae. None the less, rearing of S.nigriventris from live-collected gastropods, for example by Miles (1968),Cameron and Disney (1975), Hopkins and Baker (1993) and Coupland(1994), confirmed the parasitoid association of this species with gastro-pods. Furthermore, S. nigriventris has been reared as a parasitoid of vari-ous arthropods (e.g. Séguy, 1932; van Emden, 1950; Pape, 1987; Povolnyand Verves, 1990). According to Pape (1987) the viviparous S. nigriventrisfemales sustain the larvae in the uterus with nourishment from accessoryglands, to larviposit the second-instar larvae directly on to a suitablehost. This is one of the most specialized reproductive strategies knownin Sarcophaginae and points to a primarily parasitoid life strategy, withfacultative development as a saprophage. S. nigriventris is widely distrib-uted through the mid-latitude regions of the Palaearctic. Accordingto Povolny and Verves (1997), the species occurs especially in dry,sunlit habitat, with adult flies feeding at various flowers. Sarcophaga(Myorhina) sorror Rondani has been reared from both dead gastropods asa saprophage (Rohdendorf, 1937) and live C. aspersus as a parasitoid(Séguy, 1921). Sarcophaga (Myorhina) sororcula (Rohdendorf) has beenreared as a parasitoid of Bradybaena sp., but further biological data islacking. Both S. sorror and S. sororcula have a more restricted Europeandistribution relative to that of S. nigriventris. Povolny and Verves (1997)indicate that S. sorror exhibits a preference for limestone habitat.




Sarcophaga (Thyrsocnema) incisilobata Pandellé is perhaps the bestknown of the small group of about nine Palaearctic sarcophaginispecies presently assigned to the subgenus Thyrsocnema Enderlein.S. incisilobata is widely distributed throughout the western section of thePalaearctic, from the British Isles to western Siberia, and from NorthAfrica to southern Scandinavia. As summarized by Povolny and Verves(1997), the adult flies feed at flowers, fruit, meat and faeces. The larvae arecoprophagous predators, but also occur as predators and/or parasitoids ofacridoid Orthoptera (Séguy, 1941), lepidopteran pupae (Komárek, 1938)and terrestrial gastropods (Keilin, 1919). Povolny and Pospísil (1989)indicate that this species may cause urinary myiasis in humans.

Sarcophaga (Paraethiopisca) misera (Walker) occurs in theAustralasian region, from India to Australia. Its larvae have been shown toattack the bovine schistosomiasis vector Indoplanorbis exustus Deshayes(Planorbidae) in India (Parashar et al., 1997). Indeed, in contrast to othersarcophagids the larvae of this fly would attack and kill up to six snailsper day in a petri dish. This high attack rate indicates a good potentialfor controlling I. exustus during the dry season, when these gastropodsare exposed by the receeding waters and thus susceptible to attack.However, the biology of the predatory larvae has not yet been adequatelystudied under field conditions. S. misera is known to breed in vertebratecarrion (Kano et al., 1967).

Obligatory parasitism in gastropods is known in the Sarcophagasubgenera Baranovisca de Souza Lopes, Discachaeta Enderlein, Hetero-nychia Brauer & Bergenstamm, Krameromyia Verves, and Sarcorohden-dorfia Baranov. Species of Sarcophaga (Baranovisca) occur in Indiathrough to the Philippines, New Guinea and Australia. Several species areknown to be parasitoids in the egg sacs of spiders (de Souza Lopes, 1985).

Ramachandran Nair (1968) found Sarcophaga (Baranovisca) nr banksiSenior-White to be a parasitoid of the ariophantids Ariophanta belangeri(Deshayes), Ariophanta bistrialis (Beck) and Cryptozona semirugata (Beck)in Mysore State, India. Three to 12% of snails collected from the fieldwere parasitized, with 4–15 fly larvae in each individual. In the labora-tory, gravid females deposited a series of five to ten larvae in quick success-ion on the shell of prey individuals, in the vicinity of the shell aperture.The larvae immediately penetrated the prey’s soft tissues. Attack by thelarvae was seen to stimulate excessive mucus production and loss of bodyfluids. Host death occurred on the subsequent day and the larvae devel-oped as saprophages on the decaying tissues. On completion of larvalgrowth, S. nr banksi leave the host’s cadaver to pupate in the soil. Inaddition to the ariophantids, Ramachandran Nair (1968) found that thissarcophagid would readily attack Rachis punctatus (Anton) (Enidae)and A. fulica in the laboratory. Owing to its small size, individualR. punctatus prey generally supported the development of a single larva.A. fulica was found to be an unfavourable prey species. Large individualswere able to repel the attack from most S. nr banksi larvae by productionof copious quantities of mucus, and while some larvae did successfully




establish parasitism in smaller A. fulica, they subsequently suffered highmortality and only 20–42% of prey were killed by larval feeding.

Ramachandran Nair (1968) also found Sarcophaga sp., of presentlyunknown subgeneric affinity, as a solitary parasitoid of R. punctatus inMysore. On average, 9.3% of R. punctatus were parasitized in the field,with peak parasitism of 28% in September. In the laboratory, gravidfemales generally deposited two or more larvae on prey individuals, witha minimum of 3 min between successive larvipositions on the shell in thevicinity of the apertural opening. Only one larva successfully establishedwithin a single R. punctatus, which was killed within 2 days. The larvathen adopting a saprophagous existence on the decaying tissues. Withdevelopment complete the larva occludes the shell aperture with rem-nants of the prey’s soft tissues and forms a puparium within the shell.Ramachandran Nair (1968) discovered that Sarcophaga sp. was unable todevelop on juvenile A. fulica. However, with about a 50% success rate,Sarcophaga sp. was able to parasitize and complete development in theariophantids C. semirugata, A. bistrialis and A. belangeri. In cases of para-sitism in these hosts, the larvae exited the shell to pupate in the soil asthey were unable to consume the decayed tissues of the host completelyand thus unable to secure a dry site for pupation within the shell.

Sarcophaga (Discachaeta) comprises five species distributed inEurope and North Africa. Of these species Sarcophaga (Discachaeta)arcipes Pandellé is best known biologically. It occurs extensively in warmshrublands in Europe from the British Isles to the Ukraine, where itparasitizes terrestrial gastropods in the family Hygromiidae (Povolny andGroschaft, 1959; Verves and Kuzmovich, 1979). Povolny and Verves(1997) suggest that nothing is presently known of the ecology of Sarco-phaga (Discachaeta) cucullans Pandellé, widespread in Europe to west-ern Russia and neighbouring countries, and Sarcophaga (Discachaeta)pumila Meigen, of Western Europe and North Africa, although the formerwas predicted to be a parasitoid of gastropods. S. cucullans has indeedbeen reared as a parasitoid from the gastropod Theba pisana (Muller)(Helicidae) and C. virgata in France (Lehrer, 1966; Hopkins and Baker,1993; Coupland, 1994). Similarly, S. pumila has been reared as asuspected parasitoid from T. pisana and C. virgata in Israel (Harpazand Oseri, 1961).

Sarcophaga (Heteronychia) comprises about 80 species distributed inAfrica (including Madagascar) and the Palaearctic. While the ecology ofmany species remains to be elucidated, the predominate association withgastropods in all reared species led Povolny and Verves (1997, p. 161)to conclude that Sarcophaga (Heteronychia) ‘are usually parasitoidsof snails’. The records of Sarcophaga (Heteronychia) species with aconfirmed or suspected parasitoid relationship to terrestrial gastropodsare summarized in Table 3.1. It should be noted that while an obligateparasitoid life strategy is generally indicated for Sarcophaga (Hetero-nychia) species, this may not always be the case as additional specieshave been demonstrated to be saprophages breeding within gastropod




carrion. For example, the Western Europe–North African Sarcophaga(Heteronychia) hirticrus Pandellé has been reared by Beaver (1972, 1973,1977) from C. nemoralis killed in the laboratory and experimentallyexposed in the field. Earlier Barfoot (1969) had reared S. hirticrus fromdead C. aspersus, and Povolny and Verves (1997) report this sarcophaginifrom dead swallows (Aves, Hirundinidae). Coupland (1994) reported thisspecies as an apparent parasitoid in live-collected T. pisana, C. virgataand C. aspersus from southern France. Thus, contrary to Povolny andVerves (1997), S. hirticrus may primarily be a carrion fly, with facultativeparasitism in gastropods. Additionally, the African Sarcophaga (Hetero-nychia) benefactor Malloch has been reared from the locust Schistocercagregaria Forskål (Orthoptera, Acrididae) by Zumpt (1972) and from deadLimicolaria Schumacher sp. (Achatinidae) experimentally exposed in thefield by Beaver (1986a).

Perhaps the best known of the Sarcophaga (Heteronychia) specieswith parasitoid association in terrestrial gastropods are Sarcophaga(Heteronychia) bezziana Böttcher, Sarcophaga (Heteronychia) filiaRondani, Sarcophaga (Heteronychia) haemorrhoa Meigen, Sarcophaga(Heteronychia) haemorrhoides Böttcher, Sarcophaga (Heteronychia)proxima Rondani, Sarcophaga (Heteronychia) vagans Meigen, and S. (H.)penicillata. S. bezziana is predominately a montane species of the Euro-pean Alps, and generally associated with montane forests or shrublandson limestone (Povolny and Verves, 1997). The larvae occur as parasitoidsof the gastropod genera Chondrina Reichenbach (Chondrinidae) andClausilia Draparnaud (Clausiliidae) (Povolny and Verves, 1990). S. filiais common in Europe, extending eastward to the Caucasian region. Itprefers dry habitat. Keilin (1921) stated that S. filia can be assumed to bea parasitoid of gastropods, based on the study of Rostand (1920), whodiscovered larvae attacking supposedly healthy snails in the genus Helixin the south of France. Povolny and Verves (1990), Hopkins and Baker(1993), and Coupland (1994) have recorded this species from severalhelicid and hygromiid species (Table 3.1), confirming its parasitoid lifestrategy. S. haemorrhoa occurs extensively throughout the lowlandsof Europe, generally associated with woodland and forest margins(Povolny and Verves, 1997). This species parasitizes helicids (Mik, 1890;Portschinskij, 1894; Schmitz, 1917; Keilin, 1919; Godan, 1983; Povolnyand Verves, 1990, 1997). S. haemorrhoides occurs extensively in mid-latitude Palaearctic, from western mainland Europe to Asia Minor,Siberia and Iran. As a parasitoid of various helicids (Berner, 1973; Verves,1976; Povolny and Verves, 1990; Povolny, 1992), S. haemorrhoides occu-pies warm forest and shrubland habitats. S. proxima occurs in northernmainland Europe and Scandinavia east to western regions of Siberiaand China, generally occupying woodlands and shrublands. Its larvaeparasitize helicids (Povolny and Groschaft, 1959; Povolny and Verves,1990; Y. Verves in Povolny and Verves, 1997). The distributional rangeof S. vagans extends in mid- to high latitudes from western Europe(British Isles and Scandinavia) to Japan, generally in lowland forests and




shrublands. It is a locally common parasitoid of various Succineidae andHelicidae (Verves, 1976; Artamonov, 1985; Povolny and Verves, 1990).

Several species of the families Helicidae and Hygromyiidae, ofMediterranean–European origin, have become pests in pastoral andarable agriculture in Australia (Baker, 1986, 2002). A search for suitablebiological control agents for these pests started in 1989, led by CSIROEntomology and funded by the Grains Research and Development Corpo-ration and the Woolmark Company. Most of the research was centred onCSIRO’s European laboratory in Montpellier, France, within the nativerange of the snails concerned. The Mediterranean S. penicillata wasreared from Cochlicella acuta (Müller) and Prietocella barbara (Linnaeus)(Hygromiidae) (Coupland, 1994) and identified as a suitable control agentof C. acuta. This discovery coincided with a report by Povolny (1992) ofS. penicillata as a parasitoid of helicoid gastropods. Studies in Franceby Coupland and Baker (1994) revealed S. penicillata attacking C. acutaresting on vegetation. During parasitism the adult female places a larvain the aperture of the snail shell – larvipositing adults were observedto fabricate a hole in the epiphragm of resting snails, in which theydeposited one larva. The larva penetrated the host to the apex of the shelland fed towards the shell aperture, the site at which pupation occurs.New-generation adult flies emerge about 18 days after the initial attack.Several generations of S. penicillata occur during the summer. Duringwinter, S. penicillata occur in diapause, where the pupal stage remainswithin the host shell for up to 6 months.

Coupland and Baker (1994) found S. penicillata to prefer largeC. acuta resting on tall meadow vegetation to smaller snails aestivating onrocks or low vegetation. Of C. acuta sampled from vegetation, 4% wereparasitized by S. penicillata.

Research by the South Australian Research and DevelopmentInstitute (SARDI) and CSIRO has shown S. penicillata to be sufficientlyspecific to C. acuta and P. barbara that permission has been granted forits release in South Australia (Baker and Charwat, 2000). The details ofthe host range evaluations, involving 38 gastropod species indigenous toAustralia, have yet to be published. From releases made over the period2000 to 2002, S. penicillata has become established in South Australia.

The subgenus Sarcophaga (Krameromyia) is monotypic, beingrepresented by the Holarctic Sarcophaga (Krameromyia) anaces Walker.This species prefers dry, warm open habitat. In Europe, S. anaces hasbeen bred from a number of helicid and hygromiid gastropods (Böttcher,1912; Richet, 1990; Povolny and Verves, 1990; Hopkins and Baker, 1993;Coupland, 1994) (Table 3.1), indicating a parasitoid life strategy.

Sarcophaga (Sarcorohdendorfia) occur in Asia (China, India andSri Lanka, Thailand, to Japan) through Indonesia, to New Guinea, NewBritain, Solomon Islands and Australia. Sarcophaga (Sarcorohdendorfia)megafilosia Pape, Mckillup & McKillup and Sarcophaga (Sarcorohden-dorfia) meiofilosia Pape, Mckillup & McKillup occur sympatrically incoastal Queensland, Australia, and parasitize Littoraria filosa (Sowerby)




(Littorinidae) occupying mangroves (McKillup et al., 2000; Pape et al.,2000; McKillup and McKillup, 2000, 2002). Larviposition behaviour wassimilar in these two species, except that S. megafilosia only attackedsnails with shells ≥ 10 mm, while S. meiofilosia only attacked those from4 to < 10 mm. Females of both species mounted the shell and stood withlegs outstretched sideways on the body whorl, possibly as a way of assess-ing the size of the intended larval host. Female flies deposited one ormore larvae close to a live snail. The larvae vigorously probed the spacebetween the operculum and shell, and once a larva succeeded in gainingentry to the shell interior, it began burrowing into the soft tissues ofthe snail. The attacked snail responded violently by producing largeamounts of mucus and strongly retracted into its shell. The mucusentrapped and prevented other larvae present outside from entering theshell of the parasitized L. filosa. McKillup and McKillup (2002) noted thatoccasionally the larva was ejected and the L. filosa survived, but mostattacks were successful and the snail died within an hour, after which theexuded mucus dried in a ring that formed a seal around the aperture andglued the shell to the substratum. This ring of dried mucus provided a sealto the aperture of the shell sufficient to protect the developing larva orpupa during tidal submersion. Only one larva completed its developmentwithin an L. filosa individual. The larval and pupal stages were observedto be completed within the shell, and the adult emerged after breakingthe mucus seal. Parasitized L. filosa die within 5 mm of where theyare attacked and their shells remain glued to the mangrove substratumuntil adult fly emergence. L. filosa is polymorphic in shell coloration(as in many littorinids), and McKillup and McKillup (2002) found thatS. megafilosia killed a significantly greater than expected proportion ofsnails that did not match their backgrounds. In contrast, these authorscould find no evidence of selective attack by S. meiofilosia.

McKillup et al. (2000) could find no evidence for larval or pupaldiapause in S. megafilosia and S. meiofilosia, with adult flies present inthe field during most months of the year. These sarcophagids apparentlyexert a strong influence on the metapopulation structure of L. filosa(McKillup and McKillup, 2000). Up to 100% of L. filosa within largepatches of mangrove forest were killed by flies during summer. Incontrast, L. filosa within smaller patches were less likely to be foundand killed by the flies.

The rearing records for three North American species in the subgenusSarcophaga (Bercaeopsis) Townsend, namely Sarcophaga (Bercaeopsis)fortisa Reinhard (= helicivora Dodge), Sarcophaga (Bercaeopsis) mimorisReinhard and Sarcophaga (Bercaeopsis) parallela Aldrich, strongly pointto a parasitoid association with terrestrial gastropods (Table 3.1). Nonethe less, the ecology of these sarcophagini is poorly known.

The species-rich Microcerellini are American, mostly Andean. Thebiology of most species is not known. De Souza Lopes (1982b) concludedthat the structure of the first-instar larvae known from a few speciessuggests that all species are scavengers, feeding in nature on invertebrate




carrion. Microcerella acrydiorum (Weyenbergh) has been reared fromOrthoptera and terrestrial gastropods (de Souza Lopes, 1969b, 1982b), butCrouzel (1947) demonstrated that this species is a saprophage rather thana true parasitoid. Microcerella weyrauchi de Souza Lopes, MicrocerellaMacquart sp., and Comasarcophaga texana Hall have similarly beenreared from terrestrial gastropods (Downes, 1965; Neck and de SouzaLopes, 1973; de Souza Lopes, 1982a) and, in the absence of information tothe contrary, must be regarded as cases of saprophagy.

A few anthropophilic Sarcophagidae have distributions that stronglysuggest human-aided dispersal. Some of these invasive species aremalacophagous. Pape (1996) indicates, for example, that the Nearcticoccurrence of S. melanura is probably a case of dispersal from thePalaearctic region. L. elegans has recently been recorded in Hawaii(Beardsley et al., 1998) and probably represents an introduction. Povolnyand Verves (1997) highlight the decline of European sarcophagids,evidently driven by human-induced habitat degradation.

Calliphoridae

The Calliphoridae (blowflies) are a rather heterogenous assemblage ofcalyptrate flies well represented in all zoogeographic regions and com-prising about 1100 species. In recent catalogues, Calliphoridae are usuallydeemed to comprise the subtaxa Auchmeromyiinae, Mesembrinellinae,Ameniinae, Chrysomyinae, Phormiinae (often regarded as a subgroup ofChrysomyinae), Calliphorinae (varyingly comprising the tribes Luciliini,Calliphorini, Phumosiini, Polleniini and Bengaliini), Toxotarsinae,Polleniinae, Rhiniinae, Helicoboscinae and Melanomyinae (James,1970, 1977; Pont, 1980; Rognes, 1986; Schumann, 1986; Kurahashi, 1989).Mesembrinella Gglio-Tos and its allies were elevated to a separate familyMesembrinellidae by Guimarbes (1977). Hennig (1973), Griffiths (1982)and Pape (1992) questioned the monophyly of the Calliphoridae becauseof lack of satisfactory characterization by autapomorphic characters.Based on a study of morphological characters in adults and larvae, Rognes(1997) had to conclude that the Calliphoridae is indeed not a mono-phyletic clade. Many of the nominal subfamilies probably should beelevated to family status in recognition of their evolutionary history.However, in the absence of a family-level revision, we will here treatCalliphoridae in the traditional sense.

The adult flies (Fig. 3.3E,F) are generally stoutly built and of moderatesize. Many possess metallic green and/or blue coloration. Adult calli-phorids are predominantly day flying, although a few species appearat light traps. They are strongly attracted to moisture, and feed mainlyon nectar, honeydew and other sugar-containing liquids, and on theliquid products of organic decomposition – the latter provide the proteinessential for egg maturation. Reproduction is oviparous, ovoviviparous orviviparous. Under conditions of scarce food, oviparous species may retain




their eggs and produce instar-I larvae. At least some (e.g. some species inRhyncomya Robineau-Desvoidy in Rhiniinae; apparently all Ameniinae)are macrolarviparous. Calliphoridae are generally characterized by overhalf of the larval life being spent as an instar III (Greenberg, 1991).

The immature stages of Calliphoridae have been described by Keilin(1919), Thompson (1934), Hall (1948), Hennig (1952), Schumann (1954,1973), Kano (1958, 1959), Zumpt (1965), Ishijima (1967), Roberts (1971),Bedding (1973), Oldroyd and Smith (1973), O’Flynn and Moorhouse(1980), Prins (1982), Greenberg and Szyska (1984), Erzinçlioglu (1985,1987), Holloway (1985, 1991), Ferrar (1987), Shewell (1987a), Liu andGreenberg (1989), Smith (1989), Wallman (2001) and others. The ecologyof species of economic and public health importance has been extensivelystudied (see reviews by Norris, 1965, Ferrar, 1987 and others).

Ferrar (1987) suggests that carrion is the primary larval medium.Rognes (1991, p. 27) was of the opinion that blowflies ‘primitively . . . laytheir eggs on the exposed dead bodies of various animals, especiallyvertebrates, irrespective of size’. Pape (1992, p. 77) suggests ‘it is verylikely that the groundplan calliphorid breeding strategy was one ofsmall-carrion-exploitation, e.g. dead invertebrates (especially snails) andsmall vertebrates’. While the biology is still lacking for many species, itseems that while carrion is the preferred medium, the larvae of manysaprophagous species also utilize other forms of decaying organic mattersuch as dung, faeces and plant residues. Several species have been bredfrom gastropod carrion (e.g. Annandale, 1919; Séguy, 1921; G.M. Barker,personal observation). In the majority of cases, these saprophages proba-bly feed principally on the bacteria associated with decay (Roberts, 1971).A number of calliphorids have adopted the predaceous life style, special-izing in predation of other dipteran larvae, as evident in some species ofChrysomya Robineau-Desvoidy in Chrysomyinae and some StomorhiniaRondani in Rhiniinae. However, the parasitic life style has also developedrepeatedly and independently in several calliphorid groups, even withingenera where the majority of species have retained the necrophagous lar-val habit. Firstly there has been a strong trend towards attack on necrotictissue in wounds of living vertebrates, including secondary and tertiaryinfestation of myiases already initiated by other dipterans, and ultimatelyhas led to obligate primary myiasis of healthy tissue. Myiasis is causedby a diverse assemblage of calliphorids, including species in CalliphoraRobineau-Desvoidy, Bufolucilia Townsend, Lucilia Robineau-Desvoidyand Phaenicia Robineau-Desvoidy in Calliphorinae, Booponus Aldrichin Auchmeromyiinae, Chrysomya in Chrysomyinae, and ProtophormiaTownsend in Phormiinae. In some genera at least, the ectoparasitichabit has arisen repeatedly and independently among species (Stevensand Wall, 1997). Various calliphorids parasitize vertebrates, withthe larvae burrowing under the host’s skin. Protocalliphora Houghin Phormiinae and Auchmeromyia Brauer & Bergenstamm inAuchmeromyiinae are haematophagous, parasitizing nestling birds andmammals respectively.




Other calliphorids have developed a parasitoid association withvarious invertebrate groups. In Calliphorinae Bengalia Robineau-Desvoidy larvae feed in termite nests, while the adults rob immaturestages and food being carried by ants. A number of genera in Rhiniinae,including Borbororhinia Townsend and some members of Stomorhinia,have independently developed a life strategy associated with the imma-ture stages of Hymenoptera. Pollenia Robineau-Desvoidy in Polleniinae,Onesia Robineau-Desvoidy in Calliphorinae, and some Calliphora inCalliphorinae, have likewise independently become obligate parasitoidsof earthworms. Malacophagy among calliphorids has been adoptedby various members of the Melanomyine genus Melanomya Rondani,apparently by all members of the calliphorine genus MelindaRobineau-Desvoidy, and possibly by all members of the Ameniinae.

The genus Melinda was most recently revised by Schumann (1973).These flies occur in the Old World tropics, the Palaearctic region in NorthAfrica, Europe, through to China, Japan and SE Asia, and extend intoIndonesia and the Pacific. The biology of most Melinda species ispresently poorly known. The adult flies are rarely abundant and mostfrequently encountered in wooded mountain habitat. Adults visit flowers.Oviparous and viviparous species are known. Melinda itoti Kano ofJapan and Taiwan, and Melinda caerula Meigen (= cognata Meigen) andMelinda gentilis Robineau-Desvoidy of Europe, are known to parasitizeterrestrial gastropods (Table 3.1). Of these species, the biology is knownin some detail only for M. caerula.

M. caerula is rather common in northern Europe. Keilin (1919)described the life history of this calliphorid occurring as a true parasitoidof C. virgata near Cambridge, UK. M. caerula lays 1–3 eggs in the pallialcavity of individual snails. Only one M. caerula larva can develop withina single C. virgata host. The neonate larva bores its way into the kidney ofthe host to lie with its posterior end protruding into the pallial cavity.Throughout the first instar, the larva feeds upon the fluid of the kidneyand destroys renal epithelium. Keilin (1919) was unable to detect any signof distress in hosts containing these first instars. Following its first moultthe larva takes up a position in the pallial cavity and, with further feedingon the renal fluids and tissues, grows rapidly. The host may still retainsome activity, but more frequently it fixes itself to a plant and remainsretracted within the shell. On attaining the third-instar stage the larvabecomes very active and voracious, entirely destroying the host’s kidneyand then the digestive gland. The host no longer moves about, beinginvariably retracted within its shell, which is fixed upon a plant or lyingloose upon the ground. The larva grows rapidly and soon occupies thewhole length of the pallial cavity, with its posterior end projectingthrough the pneumostome. While initially carnivorous, the rapid deathand decay of the host at this stage means the larva completes its develop-ment as a saprophage. During the saprophagous period, the posterior endof the larva is directed towards the shell aperture such that the posteriorspiracles remain in communication with the external air. The larva, when




fully grown, leaves the host cadaver to pupate in the soil. Keilin (1919)suggests that the presence of pupae during the whole year is indicative ofoverwintering hibernation (diapause) in that stage.

Keilin (1919) found that other gastropod species living sympatricallywith parasitized C. virgata were free of parasitism by M. caerula. How-ever, while no studies have been carried out specifically to evaluate hostspecificity, Keilin (1919) notes that M. caerula had been reared from othergastropod species. These rearing records available to Keilin (1919) andthose that have been reported subsequently are summarized in Table 3.1.M. caerula is reputed to be a significant source of mortality in C. virgatain northern Europe (E.A. Woodruffe-Peacock in Keilin, 1921), althoughquantitative data is wanting.

The fact that M. caerula preferentially attacks the species C. virgatasuggests the potential for biological control of this gastropod species inAustralia, where it is an agricultural pest (Baker, 2002). However, surveysby CSIRO Entomology staff in Mediterranean southern Europe, corre-sponding to native habitat of similar character to the areas infested insouthern Australia, has yielded only a single parasitized C. virgata (J.B.Coupland, unpublished data). Thus M. caerula appears not to be animportant parasitoid of C. virgata in southern Europe.

Melanomya and allies comprise a small, poorly known clade of fliesbest represented in the western Palaearctic region and in South Africa.None are known from the Australasian region. They have variously beenplaced in Calliphoridae, Rhinophoridae, Sarcophagidae and Tachinidae.Placement and limits are still uncertain, but Downes (1986) in a revisionof Melanomya and its Old World and New World allies, concluded thatthese flies have greatest affinities with the Calliphoridae. At least fourspecies in Melanomyinae are thought to be malacophagous parasitoids,based on rearing records, namely Melanomya obscura (Townsend),Melanomya ordinaria (West), Melanomya cyrtoneurina (Zetterstedt) andMelanomya pecchiolii (Rondani) (Séguy, 1928; Thompson, 1934; Askew,1971) (Table 3.1). All recorded hosts appear to be snail forms. Melanomyais reputed to attack both slugs and snails (Chandler et al., 1978), butconfirmed host records for slugs could not be located in the literatureavailable to the present authors. These species are rarely common andtheir biology remains poorly studied. Some members of Melanomya arethought to be oviparous (Downes, 1986), but M. pecchiolii is known to beviviparous (Thompson, 1921).

Ameniinae occur in Australia, Philippines, Burma, Malaysia, Indone-sia, New Guinea, and the Bismarck Archipelago (Crosskey, 1965, 1969;James, 1977; Rueda, 1985; Kurahashi and Magpayo, 2000). Their relation-ships have long been considered enigmatic. For some time the Ameniinaewere regarded as belonging to the Tachinidae. Crosskey (1965) discussedthe relationships and systematic status in his revision of these flies; heconsidered them best placed as a subfamily of Calliphoridae, but possiblydeserving separate family status if biological evidence warrants this. Healso pointed out that Ameniinae show some affinities to Sarcophagidae.




The subfamily as generally recognized comprises three tribes, namely:Ameniini with the genera Amenia Robineau-Desvoidy, FormosiomimaEnderlein, Paraplatytropesa Crosskey, Platytropesa Macquart, SilbomyiaMacquart and Stilbomyella Malloch; Parameniini comprising ParameniaBrauer & Bergenstamm; and Catapicephalini comprising CatapicephalaMacquart. The cladistic analyses of Rognes (1997) point to a close rela-tionship to calliphorine Phumosiini (inclusive of Euphumosia Malloch)and Mesembrinellidae.

Crosskey (1965) reviewed the breeding records available to that date.He pointed out that reports of these flies parasitizing scarabaeid beetles(Coleoptera: Scarabaeidae, Melolonthinae) were based on error, and thatthe only definite record was that of Hardy (1951), confirmed by vanEmden (1953), that larvae of Amenia leonina (Fabricius) occur in gastro-pods. Crosskey (1969) subsequently reported that at Keravat, East NewBritain, Papua New Guinea, he observed Stilbomyella nitens Malloch andPlatytropesa dubia (Malloch) strongly attracted to A. fulica in a mannersuggesting some sort of biological association between the flies and thesegastropods. Ferrar (1976) noted that material in Australian collectionscontained material of Amenia and Paramenia reared from gastropods(Table 3.1), providing further indication that Ameniinae are malaco-phagous parasitoids. Ferrar confirmed earlier reports by Crosskey (1965,1969) that the females of Ameniinae are macrolarviparous. Despite thepaired ovaries, each comprising two ovarioles and containing numerousfollicles, a single egg is produced at a time and this passes into a largemuscular uterus, where embryonic development is completed. The egghatches in the uterus to a small, soft, white larva, which is capable of onlyweak movement. This larva grows and moults to a very active second-instar larva, which is slender, heavily spined, and possesses a slendercephalopharyngeal skeleton armed with long, curved mouthhooks. Ferrarconcluded that it was this second-instar larva that attacks the gastropodhost, as it is structurally adapted for such a purpose and older larvae hadnot been found in utero. However, Ferrar (1976) was not able to furnishproof of the predatory or parasitoid malacophagous habit of the ameniinelarvae. Amenia adults were not responsive to the presence of C. aspersus,and larvae would not attack this gastropod species.

Crosskey (1969, p. 328) noted that Platytropesa and Stilbomyella ofthe Bismarck Archipelago were ‘common at certain times and alight andrest conspicuously on low level vegetation . . .’. According to Ferrar(1976), adult Amenia in Australia are found mostly in well-forestedlandscapes, but much more in wet sclerophyll forest than in rainforest.The adults are readily attracted to faeces and traps baited with meat.Ferrar (1976) noted that while very active, diurnal fliers, adult flightactivity was strikingly correlated with the occurrence of bright sunshine.This activity in sunny weather would indicate that attack on activegastropods is not the usual behaviour and would suggest that if ameniinesare indeed malacophagous, the larvae are deposited on or near restingsnails.




Muscidae

The family Muscidae has a worldwide distribution, with well over 4000described species in some 170 genera. Several groups of flies previouslyregarded as muscids are now treated as families in their own right, includ-ing Eginiidae and Fanniidae. Skidmore (1985) recognized ten subfamilies.

Adult muscids (Fig. 3.3G) are generally day-flying, robust flies. Manyvisit flowers, and feed on liquids associated with decaying organic matter.The adults of some Muscidae, including Coenosiinae, are predaceous onsmaller insects. The mouthparts in adult Stomoxyinae are modified into apiercing organ – the flies pierce the skin and suck blood from mammals.

The immature stages of Muscidae (Fig. 3.3H) have been described bynumerous authors, including Hewitt (1914), Keilin (1917), Keilin andTate (1930), de Oliveira Albuquerque (1947), Schumann (1954), Paterson(1958), Ranade (1965), Zumpt (1965), Ishijima (1967), Kleynhans (1969),Roberts (1971), Oldroyd and Smith (1973), Skidmore (1973b, 1985), Ferrar(1975, 1979, 1987), Iwasa (1983, 1984), Iwasa and Nishijima (1984),Erzinçlioglu (1987), Liu and Greenberg (1989), and Smith (1989). Severalspecies occur as larvae in gastropod carrion (e.g. Paterson, 1958; Disney,1970, 1973; Beaver, 1986b).

Apart from the haematophagous Reinwardtiinae (Reinwardtiini),the coprophagous Muscinae (Muscini) and Stomoxyinae, and the phyto-phagous Atherigona Rondani s. str. in Atherigoninae, the vast majorityof muscid larvae are at least partially carnivorous in the final instar ifthe opportunity arises. Even normally non-carnivorous species may bepredatory on rare occasions. Like most cyclorrhaphous Diptera, mostmuscids are oviparous and the larvae hatch from the egg as first instars topass through three instars and thus may be regarded as trimorphic. Nonethe less, many muscids exhibit vivipary or larvipary. In these viviparousspecies, hatching from the egg occurs in the parental oviduct but larvi-position may occur in any instar. Thus the subfamilies Phaoniinae,Mydaeinae, Limnophorinae and Coenosinae are known to have the post-oviduct larval phase of the life cycle reduced to two (dimorphic) orone (monomorphic) free-living instar. Skidmore (1973a) divided thelarval life of Muscidae into four types, namely trimorphic saprophagous,trimorphic facultative carnivorous, dimorphic obligatory carnivorous andmonomorphic obligatory carnivorous. According to Skidmore (1973a,1985), saprophagous forms are always trimorphic, and monomorphicand dimorphic larvae are unable to mature on a pure vegetarian diet.However, Ferrar (1979) found two Helina Robineau-Desvoidy specieswhose larvae are dimorphic saprophages. Iwasa (1984) reported on twomonomorphic species in the Muscini genus Myospila Rondani, withone species carnivorous, the other coprophagous. Thus monomorphismis a phenomenon not necessarily correlated with the carnivorous modeof life.

The speciose genus Musca Linnaeus in the subfamily Muscinae has aworldwide distribution and is particularly common and dominant in




tropical Asia and Africa. Most species in the genus are oviparous, andhave three larval instars. Some species are macrolarviparous, however,and retain a larva in the uterus to the end of instar I, or occasionally tolater instars. Like most Muscini, the larvae of Musca are saprophagous,breeding in dung and other forms of decaying organic matter. Bacteriaassociated with decomposition are the principal food for thesesaprophages (Levinson, 1960).

Musca domestica Linnaeus is now almost cosmopolitan, having beentransported by commerce. Its native range is uncertain but possibly thesouthern Palaearctic or the Middle East (Skidmore, 1985). Throughout itsrange M. domestica is almost invariably associated with human activity.Adults are day active, attracted to both moist and dry organic foods, andtheir mouthparts are equipped for ingestion of liquid foods. The femalesare oviparous. M. domestica is extremely polyphagous, primarily devel-oping as larvae in animal excrement and decaying vegetable matter(Skidmore, 1985). It also breeds in carrion (e.g. Suenaga, 1959). Instancesof intestinal, aural, urino-genital and ocular myiasis occur in humans(references in Smith, 1989). Furthermore, the species is associated withtransmission of food-spoilage microbes and various microbial andhelminth parasites. Thus there is a massive literature on this species,including a text devoted to its biology (West, 1951). While primarilysaprophagous, M. domestica larvae are known to occasionally adopta predaceous behaviour. Larvae generally migrate from their breedingmedium to pupate in cool, dry places.

Keilin (1919) reported on the observations by M.E. Séguy on parasit-ism of an unspecified gastropod species by M. domestica. Keilin (1919,p. 451–452) summarizes a letter from Séguy:

He collected several snails, having the shell closed by the epiphragm,and examined them, breaking the latter, in the hope of finding the Phoridlarvae. The snails secreted another epiphragm, but ten days later they weredestroyed by the larvae of M. domestica.

Keilin goes on,

Living snails, closed with epiphragms, were put in a jar containing thelarvae of M. domestica. In eight days the snails were completely eaten upby the larvae. The latter burrowed their way through the epiphragm andcompletely penetrated into the foot of the Mollusca. The penetrationoccupied about eight hours, and the abundant secretion of mucus bythe snail did not seem to disturb the larva. . . . The larvae, after theyhave destroyed one snail, pass easily into another living or deadspecimen . . .

and

Living snails were placed under a bell-jar containing several pairs ofM. domestica and 12 days later they were all devoured by the maggots.In the middle of January, 50 snails were collected from the wall close tothe military hospital, they were separated in tightly closed jars whichwere placed at 25°C., 9 of the 50 Molluscs yielded M. domestica larvae.




Adult M. domestica is readily attracted to and oviposits on carrion,including gastropod cadavers (G.M. Barker, unpublished observations).The larvae will develop as saprophages. It is probable that under somecircumstances the larvae will adopt a facultative parasitoid behaviour,attacking living gastropods in the close vicinity of the cadavers of deadcongenerics.

The Reinwardtiinae utilize very diverse larval foods – many breed indung or carrion, often as facultative predators, others are obligate para-sites of invertebrates. Some Reinwardtiini, such as Passeromyia Rodhain& Villeneuve and Philornis Meinert, are obligate to facultatively haemato-phagous parasites on birds. In the Reinwardtiinae genus MuscinaRobineau-Desvoidy various media are utilized by the larvae, includingfungi, and invertebrate and vertebrate carrion. Some are obligate carni-vores on larvae of other dipterans occupying the same medium, particu-larly in instar III (Skidmore, 1985; Ferrar, 1987). Keilin (1917) foundlarvae of Muscina levida (Harris) (= assimilis Fallén) in dead snails, butdid not record the species of snail. Keilin (1917) and Skidmore (1973a)regarded this species as a facultative predator in instar III, with the preygenerally being larvae of other dipterans. Beaver (1977) reared M. levidafrom dead C. nemoralis. He found a maximum of five larvae completingdevelopment in a single C. nemoralis cadaver, with the larvae pupatingeither within the Cepaea shell or in adjacent soil. Kneidel (1983) foundthat M. levida utilized Limax maximus Linnaeus carcasses. M. levidanaturally occurs widely in the Holarctic.

Muscina stabulans (Fallén) has a distribution that is now nearlycosmopolitan, having been spread by commerce. Its native range isunknown. Larvae of M. stabulans typically prey on larvae of other Dipterain carrion (Hewitt, 1914; Siverly and Schoof, 1955). However, it can breedin animal excrement, fungi and living plant tissue, and can cause myiasisin various vertebrates. Séguy (1921) reared M. stabulans from deadhelicids, suggesting that this species might be a true parasitoid. Greenberg(1971) and Draber-Moñko (1966) give records of M. stabulans from insectlarvae (esp. Lepidoptera), indicating a facultatively parasitoid strategy.None the less, records of Muscina larvae as parasites of other insects wereconsidered incorrect by Ferrar (1987), and the true nature of associationwith living gastropods, if any, is still be determined.

The genus Charadrella Wulp is Neotropical. Charadrella malaco-phaga de Souza Lopes is a viviparous Brazilian species that depositseither late second- or early third-stage larvae. De Oliveira Albuquerque(1947) records C. malacophaga parasitizing and breeding in Thaumastustaunaysi (de Férussac) (Bulimulidae) and Streptaxis Gray sp.(Streptaxidae).

The Phaoniinae genus Ochromusca Malloch is distributed in theAfrotropical region and currently comprises two recognized species.Early reports on the biology of Ochromusca trifaria Bigot indicatedthat the larvae are parasitic on achatinid snails (van Emden, 1949).


134A4784 - 134.prnZ:\Customer\CABI\A4743 - Barker\A4784 - Barker - Final Voucher Proofs #K.vpMonday, June 07, 2004 11:32:55 AM


Subsequently, larvae have been reared from dead or dying gastropodsin the genus Achatina de Lamarck (van Emden, 1956; Paterson, 1958;Disney, 1970, 1973; Pont and Dear, 1976; Skidmore, 1985). As noted bySkidmore (1985), it is not known whether the larvae are carnivorousor whether the adults are viviparous. Beaver (1986a) reared this speciesfrom Limicolaria killed and exposed in farmland near Lusaka, Zambia.This confirms that adult O. trifaria will deposit immatures on gastropodcarrion and the larvae are able to complete development as saprophages.However, Skidmore (1985) notes that the remarkable form of thepuparium, with massive anal spiracles, is evidently an adaptation tothe specialized larval habit, enabling the spiracles to project above theautolysed gastropod tissues upon which the larvae feed. This wouldsuggest a parasitoid relationship. Pupation occurs within the shell of thegastropod. As explained by Beaver (1986a, p. 197)

It attaches itself to the shell by its ventral side, the dorsal side contracts, andthe anterior and posterior ends of the body curve upwards and towards eachother. This raises the anterior and posterior spiracles of the puparium outof any fluid that may remain in the snail, and enables aerial respiration tocontinue throughout the pupal and pharate adult stages.

Initial reports suggested that the related Afrotropical Alluaudinellabivittata (Macquart) is a predator or parasitoid in Achatindae. Rodhainand Bequaert (1916, p. 248) state ‘The genus Mydaea exists in centralAfrica and its larvae are carnivorous; one of us bred at Kivou a greatnumber of a species allied to M. bivittata Macq. . . . from the larvaedevouring a big terrestrial Mollusc (Burtoa nilotica Pfeiff.).’ J. Bequaert (inPilsbry, 1919, p. 86) suspected a parasitoid relationship, although the factthat ‘numerous specimens’ were reared ‘from one of these (Butroa niloticaPfeiffer) snails which was found dead’ rather suggests a saprophagoushabit as dipteran parasitoids tend to be solitary or of low abundancewithin individual hosts. Based on the report of Rodhain and Bequaert(1916) and reports of predatory or parasitoid habits in the genus Mydaea,Keilin (1919) considered this species carnivorous. That A. bivittata is nowrecognized as being not closely related to species in Mydaea largelynegates Keilin’s argument. Paterson (1958) found eggs on the bodies andshells of Achatina killed 8 h earlier and placed in scrubland, suggestingthis species is saprophagous. In the light of these earlier reports, Skidmore(1985) considered the trimorphic larval stages of A. bivittata saprophagesliving in gastropod cadavers. This is further supported by reports by Dis-ney (1970, 1973) that the congeneric species, Alluaudinella fulvovittataMalloch, has reared from dead Achatinidae. None the less, it remainsto be disproved that A. bivittata, and possibly other AlluaudinellaGiglio-Tos, is not a facultative parasitoid of achatinids.

Paterson (1959) and Skidmore (1984) considered members of theAfrotropical genus Aethiopomyia Malloch as parasites or saprophagesliving in gastropods. However, little is known of their biology.




Fanniidae

Fanniidae comprise a small clade of some 265 species in fivegenera, namely Azelia Robineau-Desvoidy, Fannia Robineau-Desvoidy,Euryomma Stein, Australofannia Pont and Piezura Rondani. These fliesare best represented in the Palaearctic and Nearctic regions. Fanniidaebreed in a wide range of decaying organic media of plant origin, withadditional records from mammal burrows, dung, fungi and invertebrate/vertebrate carrion. Four species have been recorded as causing humanmyiasis. The larval stages of the Fanniidae (Fig. 3.3I) have been describedby Roback (1951), Lyneborg (1970), Ferrar (1979) and Smith (1989).

About 220 species are known in the genus Fannia. Fannia scalaris(Fabricius), the latrine fly, develops as larvae in a wide range of media,especially fresh animal excreta, but also including carrion (Ferrar, 1987).This species is known to cause urino-genital and intestinal myiasis inhumans, and fly strike in sheep. Ferrar (1987) makes no mention of apossible association with gastropods despite earlier reports by Séguy(1921) and Mokrzecki (1923) of F. scalaris having been reared as apossible facultative parasitoid of C. aspersus.

Under a heading ‘saprophagous larvae and doubtful parasites’, Keilin(1919) reported Fannia canicularis (Linnaeus) reared from helicid gastro-pods. Beaver (1972, 1977) reported this species from dead C. nemoralisand showed that utilization of cadavers generally did not occur until thesecond week, suggesting a true saprophagous life style. Coupland (1994)reared a species tentatively identified as F. canicularis from T. pisana andC. virgata collected alive in southern France. F. canicularis, often referredto as the lesser house-fly, is a very common synathropic fly in many partsof the world, with larvae associated with fungi, decaying plant material,birds’ nests, various types of carrion, and the nests of social Hymenoptera.

Conclusions

The greatest part of the literature on mollusc-associated Diptera concernsthe Sciomyzidae. As noted by Mead (1979), this has largely emanatedfrom C.O. Berg and his colleagues, with the initial discovery of malaco-phagy (Berg, 1953) the catalyst for a large series of investigations into thelarval predatory–parasitoid habits of these flies, driven in part by the needfor biological control of pestiferous gastropods, and in part by interests inevolutionary biology of host–parasitoid relationships in Diptera.

While there is already a considerable body of information, it must beadmitted that our understanding of the ecology of the dipteran familiesof interest in this chapter, namely Calliphoridae, Fanniidae, Muscidae,Phoridae and Sarcophagidae, is in its infancy. Only a small part of thespecies diversity has been formally described; there is presently littleagreement among authorities concerning the supra-specific relationships,and very skeletal understanding of the ecology of communities and way


136A4784 - 136.prnZ:\Customer\CABI\A4743 - Barker\A4784 - Barker - Voucher Proofs #J.vpMonday, June 07, 2004 11:25:08 AM


of life of the larval stages. We have attempted to draw together thedisparate information on malacophagy in these dipterans, but it is clearthat the information is fragmentary and provisional. Their role in thepopulation ecology of terrestrial gastropods remains largely unknown.Their interaction with Sciomyzidae has not received any attention fromresearchers. Furthermore, the prospects for use in classical biologicalcontrol of pestiferous gastropods looks somewhat tenuous becausethe ecological information available to date paints a picture of almostuniversal polyphagy and thus offers little reassurrance to pest managersand regulators interested in mitigating against adverse environmentalimpacts. Species in Calliphoridae, Fanniidae, Muscidae, Phoridae andSarcophagidae known from gastropod prey are often saprophages, withopportunist, facultative tendency for predation or parasitoid association.Among those with more obligate parasitoid life strategies, speciesgenerally utilize a range of gastropod species and, in many cases, a rangeof other animals.

References

Alakhverdyanc, S.A. and Zakharova, N.F. (1961) The investigation ofsarcophagids at presence of helminth eggs. Meditsinskaya Parazitologiya iParazitarnye Bolezni Moscow 30, 360–361 [in Russian].

Aldrich, J.M. (1916) Sarcophaga and Allies in North America. Thomas SayFoundation, La Fayette.

Annandale, N. (1919) Mortality among snails and appearance of blue-bottle flies.Nature 104, 412–413.

Artamonov (1983) The biology of mass species of sarcophagid flies – consumers ofdecaying matter (Diptera, Sarcophagidae) in Southern Primorye. In: Arefin,V.S. (ed.) Fauna and Ecology of Invertebrates of the Far-East (Pests andEntomophages). Insects Primorye and Kamtshatka. Institute of Biology andPedology, Academy of Sciences of the USSR, Vladivostok, pp. 11–21 [inRussian].

Artamonov, S.D. (1985) Predatory and parasitic sarcophagids (Diptera,Sarcophagidae) of southern Far East. In: Arefin, V.S. (ed.) Fauna and Ecologyof Invertebrates of the Far-East (Pests and Entomophages). Insects Primoryeand Kamtshatka. Institute of Biology and Pedology, Academy of Sciences ofthe USSR, Vladivostok, pp. 11–24 [in Russian].

Artamonov, S.D. (1987) Grey flesh flies (Fam. Sarcophagidae). In: Soboleva, R.G.(ed.) The Insects and Mites of Far East, Which are of Medical and VeterinaryImportance. Nauka Publisher, Leningrad, pp. 102–119 [in Russian].

Askew, R.R. (1971) Parasitic Insects. American Elsevier, New York.Askew, R.R. and Shaw, M.R. (1986) Parasitoid communities; their size, structure

and development. In: Waage, J.K. and Greathead, D. (eds) Insect Parasitoids.Academic Press, London, pp. 225–264.

Audcent, H. (1942) A preliminary list of the hosts of some British Tachinidae(Diptera). Transactions of the British Entomological Society 8, 1–42.

Baer, J.G. (1953) Notes de faunistique éburnéene. III. Contribution à l’étudemorphologique et biologique de Wandolleckia achatinae Cook, Phoridae




(Diptera) commensal d’Achatines de la forêt tropicale. Acta Tropica, Basel 10,73–79.

Baer, N. (1921) Die Tachiniden als Schmarotzer der schädlichen Insecten.Zeitschrift für Angewandte Entomologie 7, 349–423.

Baker, G.H. (1986) The biology and control of white snails (Mollusca: Helicidae),introduced pests in Australia. Commonwealth Scientific and IndustrialResearch Organization, Division of Entomology, Technical Paper 25.

Baker, G.H. (2002) Helcidae and Hygromiidae as pests in cereal crops and pasturesin southern Australia. In: Barker, G.M. (ed.) Molluscs as Crop Pests. CABInternational, Wallingford, UK, pp. 193–215.

Baker, G.[H.] and Charwat, S. (2000) Release of fly spells disaster for snails.Farming Ahead 105, 49.

Barfoot, S.D. (1969) Sarcophaga nigriventris Meigen and S. hirticrus Pandellé(Dipt., Calliphoridae) both bred from Helix aspersa Müller (Mollusca,Helicidae). The Entomologist’s Monthly Magazine 105, 144.

Baudet, J.L. (1982) Contribution à la faunistique régionale du genre Sarcophaga(Insectes diptères); critères de reconnaissance des femelles inventoriées.Bulletin de la Société de Science Naturelle de l’Ouest de la France 4,134–144.

Baumann, E. (1977) Untersuchungen über die Dipterenfauna subterranerGangsysteme und Nester von Wühlmäusen (Microtus, Clethrionomys) aufWiesen der montanen Region im Naturpark Hoher Vogelsberg. ZoologischesJahrbächer, Abteilung für Systematik 104, 368–414.

Baumann, E. (1979) Rennfliegen aus den Auenwäldern des Naturschutzgebietes‘Hördter Rheinaue’. II. Die Gattung Gymnophora mit Anmerkungen zurSystematik und Biologie (Diptera: Phoridae). Mitteilungen der Pollichia desPfälzischen Vereins für Naturkunde und Naturschutz 67, 184–193.

Beardsley, J.W., Arakaki, K.T., Uchida, G.K., Kumashiro, B.R. and Perreira, W.D.(1998) New records for Diptera in Hawai‘i. Bishop Museum OccasionalPapers No. 58, 51–57.

Beaver, R.A. (1972) Ecological studies on Diptera breeding in dead snails. 1.Biology of the species found in Cepaea nemoralis (L.). The Entomologist 105,41–52.

Beaver, R.A. (1973) The effects of larval competition on puparial size inSarcophaga spp. (Diptera, Sarcophagidae) breeding in dead snails. Journal ofEntomology, A 48, 1–9.

Beaver, R.A. (1977) Non-equilibrium ‘island’ communities: Diptera breeding indead snails. Journal of Animal Ecology 46, 783–798.

Beaver, R.A. (1986a) Some Diptera and their parasitoids bred from dead snails inZambia. The Entomologist’s Monthly Magazine 122, 195–199.

Beaver, R.A. (1986b) Biological studies of muscoid flies (Diptera) breeding inmollusc carrion in Southeast Asia. Japanese Journal of Sanitary Zoology 37,205–211.

Beaver, R.A. (1987) Biological studies of non-muscoid flies (Diptera) bred frommollusc carrion in Southeast Asia. Japanese Journal of Sanitary Zoology 38,187–195.

Bedding, R.A. (1973) The immature stages of Rhinophorinae (Diptera:Calliphoridae) that parasitise British woodlice. Transactions of the RoyalEntomological Society of London 125, 27–44.

Belshaw, R. (1993) Tachinid Flies (Diptera: Tachinidae). Royal EntomologicalSociety of London, London.




Belshaw, R. (1994) Life history characteristics of Tachinidae (Diptera) and theireffect on polyphagy. In: Hawkins, B.A. and Sheehan, W. (eds) ParasitoidCommunity Ecology. Oxford University Press, Oxford, pp. 145–162.

Bequaert, J. (1925) The arthropod enemies of mollusks, with description of a newdipterous parasite from Brazil. Journal of Parasitology 11, 201–212.

Berg, C.O. (1953) Sciomyzid larvae (Diptera) that feed on snails. The Journal ofParasitology 39, 630–636.

Bergenstamm, J. (1864) Ueber die Metamorphose von Discomyza incurva(Fall.). Verhandlungen der Kaiserlich-Königlichen Zoologisch-BotanischenGesellschaft in Wein 14, 713–716.

Bernasconi, M.V., Pawlowski, J., Valsangiacomo, C., Piffaretti, J.-C. and Ward, P.I.(2000a) Phylogeny of the Scathophagidae (Diptera, Calyptratae) based onmitochondrial DNA sequences. Molecular Phylogenetics and Evolution 16,308–315.

Bernasconi, M.V., Valsangiacomo, C., Piffaretti, J.-C. and Ward, P.I. (2000b)Phylogenetic relationships among Muscoidea (Diptera: Calyptratae) based onmitochondrial DNA sequences. Insect Molecular Biology 9, 67–74.

Berner, L. (1960) Les myiases des helicides. Bulletin du Société d’HistoireNaturelle de Doubs 62, 9–12.

Berner, L. (1973) Sur le parasitisme des helicides par des mouches du genreSarcophaga. Bulletin du Muséum d’Histoire Naturelle de Marseille 33, 87–91,93–94.

Beyer, E.M. (1959) Gattung Pericyclocera Schmitz in Ostasien. EntomologischeZeitschrifgt, Stuttgart 69, 167–169.

Beyer, E.M. (1967) Diptera Phoridae. Insects of Micronesia 13, 329–360.Bezzi, M. (1928) Diptera Brachycera and Athericera of the Fiji Islands. British

Museum (Natural History), London.Blackith, R.M. (1990) Flesh-flies (Sarcophagidae) of northern Sulawesi. In:

Knight, W.J. and Holloway, J.D. (eds) Insects and the Rain Forests of SouthEast Asia (Wallacea). The Royal Entomological Society of London, London,pp. 297–299.

Blackith, R.M. and Blackith, R.E. (1984) Larval aggression in Irish flesh-flies(Diptera; Sarcophagidae). Irish Naturalist’s Journal 21, 255–257.

Blackith, R.M., Blackith, R.E. and Pape, T. (1998) Taxonomy and systematics ofthe taxon Helicophagella Enderlein, 1928 (Diptera: Sarcophagidae), with thedescription of a new species. Studia Dipterologica 4, 383–434.

Bohart, G.E. and Gressitt, J.L. (1951) Filth-inhabiting flies of Guam. Bulletin of theBishop Museum, Honolulu 204, 1–152.

Boness, M. (1958) Biocoenotische untersuchungen über die Tierwelt von Klee-und Luzernefeldern. Zeitschrift für Morphologie und Ökologie der Tiere 47,309–373.

Borgmeier, T. (1963) Revision of the North American phorid flies. Part I.The Phorinae, Aenigmatiinae and Metopininae, except Megaselia (Diptera,Phoridae). Studia Entomologica 6, 1–256.

Borgmeier, T. (1964) Revision of the North American phorid flies. Part II. Thespecies of the genus Megaselia, subgenus Aphiochaeta. Studia Entomologica7, 257–416.

Borgmeier, T. (1967) Studies on Indo-Australian phorid flies, based mainlyon material of the Museum of Comparative Zoology and the UnitedStates National Museum (Part II) (Diptera, Phoridae). Studia Entomologica9, 129–328.




Borgmeier, T. (1968) A catalogue of the Phoridae of the world (Diptera, Phoridae).Studia Entomologica 11, 1–367.

Borgmeier, T. (1971) Supplement to a catalogue of the Phoridae of the world(Diptera, Phoridae). Studia Entomologica 14, 177–224.

Böttcher, G. (1912) Die männlichen Begattungswerkzeuge bei dem GenusSarcophaga Meig. und ihre Bedeutung für die Abgrenzung der Arten.Deutsche Entomologische Zeitschrift (1912), 525–544, 705–736.

Böttcher, G. (1913) Die männlichen Begattungswerkzeuge bei dem Genus Sarco-phaga Meig. und ihre Bedeutung für die Abgrenzung der Arten. DeutscheEntomologische Zeitschrift (1913), 1–16, 115–130, 239–254, 351–377.

Bowell, E.W. (1917) Larva of a dipterous fly feeding on Helicella itala. Proceedingsof the Malacological Society of London 12, 308.

Brown, B.V. (1987) Revision of the Gymnophora (Diptera: Phoridae) of theHolarctic Region: classification, reconstructed phylogeny and geographichistory. Systematic Entomology 12, 271–304.

Brown, B.V. (1992) Generic revision of Phoridae of the Nearctic Region andphylogenetic classification of Phoridae, Sciadoceridae, and Ironomyiidae(Diptera: Phoridea). Memoirs of the Entomological Society of Canada 164,1–144.

Brues, C.T. (1903) A monograph of North American Phoridae. Transactions of theAmerican Entomological Society 29, 331–404.

Brues, C.T. (1915) Some flies of the family Phoridae obtained by the expedition,with notes on a species possibly associated with external myiasis in man.In: Strong, R.P., Tyzzer, E.E., Brues, C.T., Sellards, A.W. and Gastiaburu, J.C.(eds) Report of First Expedition to South America, 1913. Harvard School ofTropical Medicine, Cambridge, Massachusetts.

Brues, C.T. (1919) The occurrence of wingless Phoridae on the Fiji Islands. Psyche26, 49.

Brues, C.T. (1942) A species of Phoridae bred in Hawaii from the immigrantAfrican land snail (Achatina fulica). Proceedings of the HawaiianEntomological Society 11, 410–411.

Brues, C.T. (1950) Guide to the insects of Connecticut. Part 6. The Diptera or trueflies of Connecticut. Fourth fascicle: Tabanidae and Phoridae. Bulletin of theConnecticut State Geological and Natural History Survey 75, 33–85.

Callan, E.M. (1946) A note on Sarcophaga lambens (Wied.), a parasite of the SouthAmerican bollworm, Sacadodes pyralis Dyar. Revista de Entomologia 17,474–475.

Cameron, R.H.D. and Disney, R.H.L. (1975) Two further cases of parasitism by flySarcophaga nigriventris Meigen (Dipt., Sarcophagidae). The Entomologist’sMonthly Magazine 111, 45.

Cantrell, B.K. (1981) The immature stages of some Australian Sarcophaginae(Diptera: Sarcophagidae). Journal of the Australian Entomological Society 20,237–248.

Cepelák, J. and Rozkosny, R. (1968) Zur Bionomie der Art Angioneura cyrto-neurina Zetterstedt, 1859 (Rhinophorinae, Diptera). Acta Zootechnica, Nitra17, 189–191.

Chandler, P., Cranston, P., Disney, H. and Stubbs, A.E. (1978) Association withother animals and microorganisms. Slugs, snails and bivalves (Mollusca).In: Stubbs, A. and Chandler, P. (eds) A Dipterists’ Handbook. The AmateurEntomologist 15, 190–192.

Clausen, C.P. (1940) Entomophagous Insects. MacGraw-Hill, New York.




Colless, D.H. and McAlpine, D.K. (1991) Diptera (flies). In: The Insects ofAustralia. Melbourne University Press, Melbourne, pp. 717–786.

Colyer, C.N. (1950) Notes on the breeding of Diploneura pilosella Schmitz andMegaselia rufipes Mg. (Dipt., Phoridae) and on the puparium of the former.The Entomologist’s Monthly Magazine 86, 320–322.

Colyer, C.N. (1955) A new species of Spiniphora (Dipt., Phoridae) from Ceylon:notes on Spiniphora genitalis Schmitz. The Entomologist’s Monthly Magazine91, 48–50.

Cook, C.E. and Mostovski, M.B. (2002) 16S mitochondrial sequences associatemorphologically dissimilar males and females of the family Phoridae(Diptera). Biological Journal of the Linnean Society 77, 267–273.

Cook, O.F. (1897) A new wingless fly from Liberia. Science 6, 886.Cornaby, B.W. (1974) Carrion reduction by animals in contrasting tropical

habitats. Biotropica 6, 51–63.Coupland, J.B. (1994) Diptera associated with snails collected in South-Western

and West-Mediterranean Europe. Vertigo 3, 19–25.Coupland, J.B. and Baker, G. (1994) Host distribution, larviposition behaviour

and generation time of Sarcophaga penicillata (Diptera: Sarcophagidae),a parasitoid of conical snails. Bulletin of Entomological Research 84,185–189.

Crosskey, R.W. (1965) A systematic revision of the Ameniinae (Diptera: Calli-phoridae). Bulletin of the British Museum of Natural History, Entomology 16,33–140.

Crosskey, R.W. (1969) The Ameniinae (Diptera: Calliphoridae) of the Noona DanExpedition, with other new records from the Bismarck Archipelago, NewGuinea and Moluccas. Entomologiske Meddelelser 37, 327–338.

Crouzel, I.S. (1947) Falta de parasitismo en Doringia acridiorum (Weyemb.)(Diptera, Sarcophagidae). Cienca e Investigación, Buenos Aires 3, 434.

Cumming, J.M., Sinclair, B.J. and Wood, D.M. (1995) Homology and phylo-genetic implications of male genitalia in Diptera-Eremoneura. EntomologicaScandinavica 26, 120–151.

Cuthbertson, A. (1938) Biological notes on some Diptera in Southern Rhodesia.Transactions of the Rhodesia Scientist Association 36, 115–132.

De Carvalho, C.J.B. (1980) Estudo sobre Charadrella Wulp, 1896 (Diptera,Muscidae, Cyrtoneurininae). Dusenia 12, 57–62.

Deisler, J. (1987) The ecology of the Stock Island tree snail Orthalicus reses reses(Say). Bulletin of the Florida State Museum, Biological Sciences 31, 107–145.

Denno, R.F. and Cothran, W.R. (1975) Niche relationships of a guild of necro-phagous flies. Annals of the Entomological Society of America 68, 741–754.

de Oliveira Albuquerque, D. (1947) Contribuição ao conhecimento de Charadrellamalacophaga Lopes, 1938 (Muscidae, Diptera). Revista de Entomologia, Riode Janeiro 18, 101–112.

de Souza Lopes, H. (1938) Sur une espèce du genre Charadrella Wulp trouvé auBresil et vivant au dépens de Bulimus taunaysi Fer. Comptes Rendus Societede Biologie, Rio de Janeiro 128, 926–928.

de Souza Lopes, H. (1940) Contribução ao conhecimento do genero UdamopygaHall de outros Sarcophagideos que vivem em molluscas no Brasil (Diptera).Revista de Entomologia, Rio de Janeiro 11, 924–954.

de Souza Lopes, H. (1966) Sôbre ‘Malacophagomyia’ g. n. (Diptera, Sarco-phagidae) cujas larvas vivem em cadáveres de ‘Gastropoda’ (Mollusca).Revista Brasileira de Biologia 26, 315–321.




de Souza Lopes, H. (1969a) Neotropical Sarcophagidae reared from Gastropoda byDr. W. Weyrauch (Diptera). Studia Entomologica 12, 133–160.

de Souza Lopes, H. (1969b) Family Sarcophagidae. In: A Catalogue of the Dipteraof the Americas South of the United States 103. Departmento de Zoologia,Secretaria de Agricultura, São Paulo, p. 1–88.

de Souza Lopes, H. (1973) Collecting and rearing sarcophagid flies (Diptera) inBrasil during forty years. Anais da Academia Brasileira de Ciências, Rio deJaneiro 45, 279–291.

de Souza Lopes, H. (1982a) The importance of the mandible and clypeal arch ofthe first instar larvae in the classification of the Sarcophagidae (Diptera).Revista Brasileira de Entomologia 26, 293–326.

de Souza Lopes, H. (1982b) The genera of Microcerellini (Diptera, Sarcophagidae).Revista Brasileira de Biologia 42, 359–369.

de Souza Lopes, H. (1983) On Notochaetomima (Diptera, Sarcophagidae) withdescription of four new species, one of them living on Beltela sp. (Mollusca,Gastropoda). Revista Brasileira de Entomologia 27, 259–266.

de Souza Lopes, H. (1985) A new genus of Sarcophagidae (Diptera) based on anAustralia species living on spider egg cases. Australian Entomology Magazine12, 51–53.

de Souza Lopes, H. and Tibana, R. (1984) Chilopodomyia boraceana, gen.n., sp.n.,a parasitoid fly from Brazil (Diptera, Sarcophagidae). Revista Brasileira deEntomologia 28, 417–420.

Disney, R.H. (1970) A note on Discomyza similis Lamb (Dipt., Ephydridae) andother flies reared from dead snails in Cameroon. The Entomologist’s MonthlyMagazine 105, 250–251.

Disney, R.H. (1972) Flies reared from pupae found in shells of garden snails. TheEntomologist’s Monthly Magazine 108, 87.

Disney, R.H. (1973) A note on some filth-inhabiting flies of Cameroon. TheEntomologist’s Monthly Magazine 108, 212–213.

Disney, R.H. (1977) A further case of a scuttle fly (Dipt., Phoridae) whose larvaeattack slug eggs. The Entomologist’s Monthly Magazine 112,174.

Disney, R.H. (1979) Natural history notes on some British Phoridae (Diptera:Phoridae) with comments on a changing picture. The Entomologist’s Gazette30, 141–150.

Disney, R.H. (1980a) Some soil-inhabiting scuttle flies (Dipt., Phoridae). TheEntomologist’s Monthly Magazine 115, 231–232.

Disney, R.H. (1980b) Chaetopleurophora bohemanni (Becker) (Diptera: Phoridae)added to the British List. The Entomologist’s Gazette 31, 245.

Disney, R.H. (1982) A scuttle fly (Diptera: Phoridae) that appears to be a parasitoidof a snail (Stylommatophora: Zonitidae) and is itself parasitised by a braconid(Hymenoptera). The Entomologist’s Record and Journal of Variation 94,151–154.

Disney, R.H. (1988) Biology and taxonomy of Old World Puliciphora (Diptera:Phoridae) with descriptions of nine new species. Oriental Insects 22, 267–286.

Disney, R.H. (1989) Scuttle flies – Diptera Phoridae genus Megaselia. In:Dolling, W.R. and Askew, R.R. (eds) Handbooks for the Identificationof British Insects, 10(8). Royal Entomological Society of London, London,pp. 1–155.

Disney, R.H. (1991a) Convergent and parallel evolution and the supra-genericclassification of the Phoridae (Diptera). Giornale Italiano di Entomologia 5,263–287.




Disney, R.H. (1991b) Scuttle flies (Diptera: Phoridae) as parasites of earthworms(Oligochaeta: Lumbricidae). British Journal of Entomology and NaturalHistory 4, 11–13.

Disney, R.H. (1994) Scuttle Flies: The Phoridae. Chapman & Hall, London.Disney, R.H. and Evans, R.E. (1980) Phoridae (Diptera) whose larvae feed on eggs

of spiders (Araneida). The Entomologist’s Monthly Magazine 115, 21–22.Disney, R.H. and Gunn, L.C. (1980) Some scuttle flies (Dipt., Phoridae) from

emergence traps over raspberry stools in Scotland. The Entomologist’sMonthly Magazine 115, 23–25.

Disney, R.H.L., Coulson, J.C. and Butterfield, J. (1981a) A survey of the scuttle flies(Diptera: Phoridae) of upland habitats in northern England. The Naturalist106, 53–66.

Disney, R.H., Henderson, I.F., Perry, J.N. and Clements, R.O. (1981b) Phoridae(Diptera) from English pasture soils. Pedobiologia 22, 366–378.

Disney, R.H.L., Weissflog, A. and Maschwitz, U. (1998) A second species oflegless scuttle fly (Diptera: Phoridae) associated with ants (Hymenoptera:Formicidae). Journal of Zoology, London 246, 269–274.

Dodge, H.R. (1956) A new sarcophagid genus with descriptions of fifteen new spe-cies (Diptera). Annals of the Entomological Society of America 49, 242–263.

Dodge, H.R. (1963) New Sarcophagine flies (Diptera: Sarcophagidae). Journal ofthe New York Entomological Society 71, 238–243.

Dodge, H.R. (1968) The Sarcophagidae of Barro Colorado Island, Panama(Diptera). Annals of the Entomological Society of America 61, 421–450.

Downes, W.L. (1965) Family Sarcophagidae. In: A Catalog of the Dipteraof America North of Mexico. US Department of Agriculture AgriculturalHandbook 276, pp. 933–961.

Downes, W.L. (1986) The Nearctic Melanomya and relatives (Diptera:Calliphoridae): a problem in Calyptrate classification. New York StateMuseum, New York.

Draber-Moñko, A. (1966) Materialy do zanajomotci Muscinae (Diptera) Polski.Fragmenta Faunistica 12, 303–331.

Draber-Moñko, A. (1973a) Przegldd krajowych gatunków z rodziny Sarcophagidae(Diptera). Fragmenta Faunistica 19, 157–225.

Draber-Moñko (1973b) Einige Bemerkungen über die Entwicklung von Sarco-phaga carnaria (L.) (Diptera, Sarcophagidae). Polskie Pismo Entomologiczne43, 301–308.

Dufour, L. (1841) Recherches sur les metamorphoses du genre Phora etdescription de deux especes nouvelles de ces Dipteres. Memoires de laSociété des Sciences, de l’Agriculture et des Arts de Lille 8, 414–424.

Eberhardt, A.I. (1955) Untersuchungen über das Schmarotzen von Sarcophagacarnaria an Regenwürmern und Vergleich der Biologie einiger Sarcophaga-Arten. Zeitschrift für Morphologie und Ökologie der Tiere 43, 616–647.

Eberhardt, A.I. and Steiner, G. (1952) Untersuchungen über das Schmarotzen vonSarcophaga spp. in Regenwürmern. Zeitschrift für Morphologie und Ökologieder Tiere 41, 147–160.

Eggleton, P. and Belshaw, R. (1992) Insect parasitoids: an evolutionary overview.Philosophical Transactions of the Royal Society of London, Series B,Biological Sciences 337, 1–20.

Eggleton, P. and Belshaw, R. (1993) Comparisons of dipteran, hymenopteran andcoleopteran parasitoids: provisional phylogenetic explanations. BiologicalJournal of the Linnean Society 48, 213–226.




Enderlein, G. (1933) Neue paläarktische Calliphoriden, darunter Schnecken-parasiten (Dipt.). Mitteilungen der Deutschen Entomologischen GesellschaftBerlin 4, 120–128.

Erzinçlioglu, Y.Z. (1985) Immature stages of British Calliphora and Cynomya,with a re-evaluation of the taxonomic characters of larval Calliphoridae(Diptera). Journal of Natural History 19, 69–96.

Erzinçlioglu, Y.Z. (1987) The larvae of some blowflies of medical and veterinaryimportance. Medical and Veterinary Entomology 1, 121–125.

Evenhuis, N.L. (1994) Catalogue of the Fossil Flies of the World (Insecta: Diptera).Backhuys, Leiden.

Feener, D.H. and Brown, B.V. (1997) Diptera as parasitoids. Annual Review ofEntomology 42, 73–97.

Ferrar, P. (1975) Life-history and larviparous reproduction of Musca fergusoni J. &B. (Diptera, Muscidae). Bulletin of Entomological Research 65, 187–198.

Ferrar, P. (1976) Macrolarviparous reproduction in Ameniinae (Diptera:Calliphoridae. Systematic Entomology 1, 107–116.

Ferrar, P. (1979) The immature stages of dung-breeding muscoid flies in Australia,with notes on the species, and keys to larvae and puparia. Australian Journalof Zoology, Supplementary Series 73, 1–106.

Ferrar, P. (1987) A Guide to the Breeding Habits and Immature Stages of DipteraCyclorrhapha, Volumes 1 and 2. Entomonograph 8. Brill/ScandanavianScience Press, Leiden.

Folgarait, P.J., Bruzzone, O.A., Patrock, R.J.W. and Gilbert, L.E. (2002) Develop-mental rates and host specificity for Pseudacteon parasitoids (Diptera:Phoridae) of fire ants (Hymenoptera: Formicidae) in Argentina. Journal ofEconomic Entomology 95, 1151–1158.

Foote, B.A. (1996) Biology and immature stages of snail-killing flies belonging tothe genus Tetanocera (Insecta: Diptera: Sciomyzidae). II. Life histories ofpredators of snails of the family Succineidae. Annals of Carnegie Museum 65,153–166.

Franssen, C.J.H. (1933) Biologische Untersuchungen an Termitoxenia hemicycliaSchmitz, Termitoxenia punctiventris Schmitz und Odontoxenia brevirostrisSchmitz. Biologisches Zentralblatt 53, 337–358.

Friedrich, M. and Tautz, D. (1997) Evolution and phylogeny of the Diptera –a molecular phylogenetic analysis using 28S rDNA sequences. SystematicBiology 46, 674–698.

Froese, A. (1992a) Vergleichende Untersuchungen zur Biologie und Ökologie derDipteren auf integriert und konventionell bewirtschafteten Feldern. Thesis,Eberhard-Karls-Universität, Tubingen.

Froese, A. (1992b) Zur Morphologie und Ökologie von Triphleba nudipalpis(Diptera, Phoridae), einer nekrophagen Buckelfliegen (Diptera: Phoridae).Entomologische Zeitschrifgt mit Insektenbörse 102, 21–30.

Froese, A. (1992c) Zur Morphologie und Ökologie von Metopina oligoneura Mik(Diptera, Phoridae). Zoologisches Jahrbächer, Abteilung für Systematik 119,383–395.

Gauld, I.D. (1988) Evolutionary patterns of host utilization by ichneumonoidparasitoids (Hymenoptera: Ichneumonidae and Braconidae). BiologicalJournal of the Linnean Society 35, 351–377.

Gauld, I.D. and Bolton, B. (1988) The Hymenoptera. Oxford University Press,Oxford.




Gemesi, O. and Disney, R.H.L. (1991) A further case of parasitisation of larvalBibionidae by a scuttle fly (Diptera: Phoridae). The Entomologist’s Gazette 42,67–69.

Girfanova, L.N. (1962) On fauna of parasitic dipterous insects of Bashkiria(Diptera: Larvaevoridae, Sarcophagidae, Calliphoridae). IssledovanieOchagov Vredit. Lesa Bashkirii (2), 113–116 [in Russian].

Godan, D. (1983) Pest Slugs and Snails. Springer-Verlag, Berlin, Heidelberg.Godfray, H.C.J. (1993) Parasitoids: Behavioral and Evolutionary Ecology.

Princeton University Press, Princeton, New Jersey.Goff, M.L., Early, M., Odom, C.B. and Tullis, K. (1986) A preliminary checklist

of arthropods associated with exposed carrion in the Hawaiian Islands.Proceedings of the Hawaiian Entomological Society 26, 53–57.

Goureau (1843) Note sur un Diptère don’t la larve vit dans l’Helix conspurcata(Melanophora helicivora Goureau). Annales de la Société Entomologique deFrance 1, 77–80.

Greenberg, B. (1971) Flies and Disease, Vol 1. Ecology, Classification and BioticAssociations. Princeton University Press, Princeton, New Jersey.

Greenberg, B. (1991) Flies as forensic indicators. Journal of Medical Entomology28, 565–577.

Greenberg, B. and Szyska, M.L. (1984) Immature stages and biology of fifteenspecies of Peruvian Calliphoridae (Diptera). Annals of the EntomologicalSociety of America 77, 488–517.

Greene, C.T. (1925) The puparia and larvae of sarcophagid flies. Proceedings ofthe United States National Museum 66, 1–26.

Gregor, F. (1972) Synanthropy of Sarcophaginae (Diptera) from Cuba. FoliaParasitologica 19, 155–163.

Gregor, F. (1977) Synanthropy and faunistics of some Phoridae (Diptera) fromCuba. Folia Parasitologica 24, 73–80.

Grensted, L.W. (1956) Species of Spiniphora (Dipt., Phoridae) in Gloucestershire.The Entomologist’s Monthly Magazine 92, 405.

Griffiths, G.C.D. (1982) On the systematic position of Mystacinobia (Diptera:Calliphoridae). Memoirs Entomological Society of Washington 10, 70–77.

Griffiths, G.C.D. (1996) Review of papers on the male genitalia of Diptera byD.M. Wood and associates. Studia Dipterologica 3, 107–123.

Grimshaw, P.H. (1901) Part I. Diptera. In: Sharp, D. (ed.) Fauna Hawaiiensis 3,1–77.

Guimarães, J.H. (1977) A systematic revision of the Mesembrinellidae, stat. nov.(Diptera, Cyclorrhapha). Archivos do Zoologiem Saõ Paulo 29, 1–109.

Hackman, W. (1964) On reduction and loss of wings in Diptera. NotulaeEntomologicae 44, 73–93.

Hagen, K.S. (1964) Development stages of parasites. In: DeBach, P. (ed.) BiologicalControl of Insect Pests and Weeds. Reinhold, New York, pp. 168–246.

Hall, D.G. (1948) The Blowflies of North America. Thomas Say Foundation,Washington, DC.

Hallock, H.C. (1938) The Sarcophaginae and their relatives in New York II. Journalof the New York Entomological Society 50, 215–241.

Hanski, I. and Kuusela, S. (1980) The structure of carrion fly communities:differences in breeding seasons. Annales Zoologici Fennici 17, 185–190.

Hardy, D.E. and Beyer, E. (1964) Phoridae. In: Zimmerman, E.C. (ed.) Insects ofHawaii. University of Hawaii Press, Honolulu, pp. 262–302.




Hardy, G.H. (1951) The hosts of Ameniinae (Dipt., Tachinidae). The Entomolo-gist’s Monthly Magazine 88, 96.

Harpaz, I. and Oseri, Y. (1961) Crop Damaging Snails in Israel and Their Control.Hebrew University, Faculty of Agriculture, Rehovot, and Citrus MarketingBoard, Tel Aviv (English summary).

Hegazi, E.M., Shaaban, M.A. and Sabry, E. (1991) Carrion insects of the Egyptianwestern desert. Journal of Medical Entomology 28, 734–739.

Hennig, W. (1952) Die Larvenformen der Dipteren, Vol. 3. Akademie-Verlag, Berlin.Hennig, W. (1973) Diptera (Two-winged flies). In: Beier, M. (editor-in-chief)

Handbuch der Zoologie. Bd. IV: Arthropoda – 2. Halfte: Insecta. ZweiteAuflage. De Gruyter, Berlin and New York.

Herbert, F. and Braun, C. (1958) Moospolster als Winterquartier europäischerPhoriden-Imagines (Phoridae, Diptera). Broteria 27, 17–29.

Hewitt, C.G. (1914) The Housefly (Musca domestica L.). A Study of its Structure,Development, Bionomics and Economy. Cambridge University Press,Cambridge.

Holloway, B.A. (1985) Immature stages of New Zealand Calliphoridae. In:Dear, J.P. (ed.) Calliphoridae (Insecta: Diptera). Fauna of New Zealand 8.Department of Scientific and Industrial Research, Wellington, pp. 12–14,80–83.

Holloway, B.A. (1991) Identification of third-instar larvae of flystrike and carrion-associated blowflies in New Zealand (Diptera: Calliphoridae). The NewZealand Entomologist 14, 24–28.

Hopkins, D.C. and Baker, G. (1993) Biological control of white and conical snails.In: Corey, S.A., Dall, D.J. and Milne, W.M. (eds) Pest Control and SustainableAgriculture. Commonwealth Scientific and Industrial Research Organisation,Canberra, pp. 246–249.

Hori and Yamaguchi (1984) A brief note on the parasitism of the larva of Melindaitoi Kano, 1962 (Calliphoridae, Diptera) to a slug. Japanese Journal of SanitaryZoology 34, 399–400 [in Japanese, with English summary].

Hull, F.M. (1973) Bee flies of the world: the genera of the family Bombyliidae.Bulletin of the United States National Museum 286, 1–687.

Hussey, N.W. (1960) Biology of mushroom phorids. Mushroom Science 4, 260–269.Ishijima, H. (1967) Revision of the third stage larvae of synanthropic flies of

Japan (Diptera: Anthomyiidae, Muscidae, Calliphoridae and Sarcophagidae).Japanese Journal of Sanitary Zoology 18, 47–90.

Ito, S. (1962) The land snail control by parasitic calliphorid fly. Report onAgricultural Research, Ministry of Education 3, 25 [in Japanese].

Iwasa, M. (1983) Studies on the dung-breeding flies in Japan II. Notes onthe immature stages of the genus Gymnodia Robineau-Desvoidy (Diptera:Muscidae). Japanese Journal of Sanitary Zoology 34, 253–262.

Iwasa, M. (1984) Studies on the dung-breeding flies in Japan III. The larvae ofthe genus Myospila Rondani, with remarks on some significant features inrelation to feeding habits (Diptera, Muscidae). Kontyû, Tokyo 52, 341–351.

Iwasa, M. and Nishijima, Y. (1984) Studies on the dung-breeding flies in Japan IV.The immature stages of three muscine species occurring from wild brownbear dung (Diptera: Muscidae, Muscinae). Japanese Journal of SanitaryZoology 35, 381–389.

James, M. (1947) The Flies that Cause Myiasis in Man. United States Departmentof Agriculture Miscellaneous Publications No. 631.




James, M. (1970) Family Calliphoridae. In: Papavero, N. (ed.) A Catalog of theDiptera of the Americas South of the United States. Museu de Zoologia,Universidade de São Paulo, São Paulo, pp. 1–28.

James, M. (1977) Family Calliphoridae. In: Delfinado, M.D. and Hardy, D.E.(eds) A Catalog of the Diptera of the Oriental Region, Volume III, SuborderCyclorrhapa (excluding Division Aschiza). University Press of Hawaii,Honolulu, pp. 526–556.

Kaneko, K. and Furukawa, E. (1977) Studies on phorid flies (Phoridae, Diptera) inJapan. Part II. Morphological notes on larvae and pupae. Journal of the AichiMedical Association 5, 65–72.

Kano, R. (1958) Notes on flies of medical importance in Japan Part XIV.Descriptions of five species belonging to Chrysomyiinae (Calliphoridae)including one newly found species. Bulletin of the Tokyo Medical andDentistry University 5, 465–474.

Kano, R. (1959) Calliphoridae. In: Illustrated Insect Larvae of Japan. Hokuryukan,Tokyo, pp. 695–701 [in Japanese].

Kano, R. and Shinonaga, S. (1968) Calliphoridae (Insecta: Diptera). In: FaunaJaponica. Biogeographical Society of Japan, Tokyo.

Kano, R., Field, G. and Shinonaga, S. (1967) Sarcophagidae (Insecta, Diptera).In: Fauna Japonica 7, Biogeographical Society of Japan, National ScienceMuseum, Tokyo.

Keilin, D. (1911) Recherches sur la morphologie larvaire des Diptères du genrePhora. Bulletin Scientifique de la France et de la Belgique 45, 27–88.

Keilin, D. (1917) Recherches sur les Anthomyides à larves carnivores. Parasitology9, 325–450.

Keilin, D. (1919) On the life-history and larval anatomy of Melinda cognataMeigen (Diptera Calliphorinae) parasitic in the snail Helicella (Heliomanes)virgata Da Costa, with an account of the other Diptera living upon molluscs.Parasitology 11, 430–454.

Keilin, D. (1921) Supplementary account of the dipterous larvae feeding uponmolluscs. Parasitology 13, 180–183.

Keilin, D. and Tate, P. (1930) On certain semi-carnivorous anthomyid larvae.Parasitology 22, 168–181.

Kemner, N.A. (1926) Über die Zucht der Larve einer echten Termitoxenia.International Congress of Entomology (1925) 3, 389–404.

Khan, J.M. and Khan, R.J. (1984) Human myiasis in Pakistan (April 1980 – July1983). Asian Medical Journal 27, 44–50.

Khitzova, L.N. (1967) On the fauna of grey flesh-flies (Diptera, Sarcophagidae) ofVoroniezh region. Transactions of the Voroniezh Research Station 15, 83–85[in Russian].

Kidd, L.N. and Brindle, A. (1959) The Diptera of Lancashire and Cheshire. Part I.T. Buncle, Arbrath.

Kirchberg, E. (1954) Zur Larvennahrung einiger heimischer Sarcophaga-Arten,insbesondere zur Frage, ob S. carnaria L. als obligatorischer Regenwurm-parasit anzusehen sei (Diptera, Tachinidae). Zeitschrift für Morphologie undÖkologie der Tiere 43, 99–112.

Kirchberg, E. (1961) Zucht von Sarcophaga carnaria L. (Diptera, Sarcophagidae)aus einer Freilandpopulation von Regenwürmern des Genus AllolobohoraEisen (Oligochaeta, Lumbricidae). Anzeiger fuer SchaedlingskundePflanzenschutz 34, 6–7.




Kistner, D.H. (1982) The social insects’ bestiary. In: Herman, H.R. (ed.) SocialInsects, Vol. 3. Academic Press, New York, pp. 1–244.

Kleynhans, K.P.N. (1969) Larval morphology in the Musciformia, with specialreference to certain dung-breeding species of the genus Musca L. Thesis,University of Pretoria, Pretoria.

Kloter, K.O., Penner, L.R. and Widmer, W.J. (1977) Interactions between the larvaeof Psychoda alternata and Dohrniphora cornuta in a trickling filter sewagebed, with descriptions of the immature stages of the latter. Annals of theEntomological Society of America 70, 775–781.

Kneidel, K.A. (1983) Fugitive species and priority during colonization incarrion-breeding Diptera communities. Ecological Entomology 8, 163–169.

Kneidel, K.A. (1984a) Competition and disturbance in communities of carrion-breeding Diptera. Journal of Animal Ecology 53, 849–865.

Kneidel, K.A. (1984b) Influence of carcass taxon and size on species compositionof carrion-breeding Diptera. The American Midland Naturalist 111, 57–63.

Komárek, J. (1938) Kritisches Wort über die Bedeutung der Insektenparasiten derNonne. Zeitschrift für Angewandte Entomologie 24, 95–117.

Kovalev, V.G. (1979) The main aspects in the evolution of Diptera Brachycerain the Mesozoic Era. In: Skarlato, O.A., Skufjin, K.V., Narchuk, E.P.,Negrobov, O.P. and Kandybina, M.N. (eds) Ecological and MorphologicalPrinciples of Dipteran Systematics. Zoological Institute of the Akademii NaukSSSR, Leningrad, pp. 35–37.

Kristensen, N.P. (1991) Phylogeny of extant hexapods. In: The Insects of Australia.Melbourne University Press, Melbourne, pp. 125–140.

Kühlhorn, F. (1986) Diptera occurrence on carcasses of Arion rufus (Gastropoda)and its possible sanitary importance. Angewandte Parasitologie 27, 123–130.

Kurahashi, H. (1989) Family Calliphoridae. In: Evenhuis, N.L. (ed.) Catalog of theDiptera of the Australasian and Oceanian Regions. Bishop Museum SerialPublication No. 86, Honolulu, pp. 702–718.

Kurahashi, H. and Magpayo, F.R. (2000) Blow flies (Insecta: Diptera: Calli-phoridae) of the Philippines. The Raffles Bulletin of Zoology, Supplement9, 1–78.

Lawton, J.H. (1986) The effects of parasitoids on phytophagous insectcommunities. In: Waage, J. and Greathead, D. (eds) Insect Parasitoids.Academic Press, London, pp. 265–287.

Legner, E.F. and Olton, G.S. (1968) Activity from parasites from Diptera:Musca domestica, Stomoxys calcitrans, and species of Fannia, Muscina,and Ophyra. II. At sites in the Eastern Hemisphere and Pacific area. Annalsof the Entomological Society of America 61, 1306–1314.

Legner, E.F., Bay, E.C. and White, E.B. (1967) Activity of parasites from Diptera:Musca domestica, Stomoxys calcitrans, Fannia canicularis, and F. femoralis,at sites in the Western Hemisphere. Annals of the Entomological Society ofAmerica 60, 462–468.

Lehrer, A.Z. (1966) Quelques donnees bio-morphologiques sur l’especeDiscachaeta cucullans Pandellé 1896 (Fam. Sarcophagidae, Diptera). Bulletinet Annales de la Société Royale Belge d’Entomologie 102, 197–200.

Levinson, Z.H. (1960) Food of housefly larvae. Nature 188, 427–428.Liu, D. and Greenberg, B. (1989) Immature stages of some flies of forensic

importance. Annals of the Entomological Society of America 82, 80–93.Lundbeck, W. (1920) Remarks on Paraspiniphora maculata Meig., nota Zett.,

bergenstammi Mik, and domestica Wood, together with changes of names of




three newly described species of Aphiochaeta. Videnskabelige Meddeleserfra Dansk Naturhistorik Kobenhaven 71, 125–132.

Lundbeck, W. (1922) Diptera Danica. Genera and Species of Flies Hitherto Foundin Denmark, Vol. 6, Pipunculidae, Phoridae. G.E.C. Gad, Copenhagen.

Lyneborg, L. (1970) Taxonomy of European Fannia larvae (Diptera, Fanniidae).Stuttgarter Beiträge zur Naturkunde 215, 1–28.

Malloch, J.R. (1910) Scottish Phoridae, with tables of all the British speciesand notes of localities. Annals of Scottish Natural History (1910), 15–21,87–92.

Malloch, J.R. (1911) Some observations on the dipterous family Phoridae.Transactions of the Natural History Society of Glasgow 8, 153–156.

Malloch, J.R. (1912) The insects of the dipterous family Phoridae in the UnitedStates National Museum. Proceedings of the United States National Museum43, 411–529.

Malloch, J.R. (1935) Phoridae, Agromyzidae, Micropezidae, Tachinidae andSarcophagidae (supplement). In: Insects of Samoa. Part VI Diptera. BritishMuseum (Natural History), London, pp. 329–366.

Marikovskiy, P.K. (1974) Nasekomvye-uragi bryukhongikh mollyuskovBradybaena. Ekologiya 5, 69–70.

McAlpine, J.F. (1989) Phylogeny and classification of the Muscomorpha.In: McAlpine, J.F. and Wood, D.M. (eds) Manual of Nearctic Diptera,Vol. 3. Research Branch, Agriculture Canada, Monograph 32. Ottawa,pp. 1397–1518.

McAlpine, J.F. and Wood, D.M. (eds) (1989) Manual of Nearctic Diptera, Vol. 3.Research Branch, Agriculture Canada, Monograph 32. Ottawa.

McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J. and Vockeroth, J.R.(eds) (1981) Manual of Nearctic Diptera, Vol. 1. Research Branch, AgricultureCanada, Monograph, Ottawa.

McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J. and Vockeroth, J.R.(eds) (1987) Manual of Nearctic Diptera, Vol. 2. Research Branch, AgricultureCanada, Monograph, Ottawa.

McKillup, S.C. and McKillup, R.V. (2000) The effects of two parasitoids on the lifehistory and metapopulation structure of the intertidal snail Littoraria filosa indifferent-sized patches of mangrove forest. Oecologia 123, 525–534.

McKillup, S.C. and McKillup, R.V. (2002) Flies that attack polymorphic snails oncoloured backgrounds: selection for crypsis by a sarcophagid parasitoid ofLittoraria filosa. Biological Journal of the Linnean Society 77, 367–377.

McKillup, S.C., McKillup, R.V. and Pape, T. (2000) Flies that are parasitoids ofa marine snail: the larviposition behaviour and life cycles of Sarcophagamegafilosia and Sarcophaga meiofilosia. Hydrobiologia 439, 141–149.

Mead, A.R. (1979) Economic malacology with particular reference to Achatinafulica. In: Fretter, V. and Peake, J. (eds) The Pulmonates, Vol. 2B. AcademicPress, London, pp. 1–150.

Meade, R.H. (1897) Flies bred from snails. The Entomologist’s Monthly Magazine7, 251.

Mello, D.M. and Bredt, A. (1978) Estudos populacionais de cinco espécies deSciomyzidae (Diptera-Insecta) no norte de Formosa, Goiás. Ciênciae Cultura30, 1459–1464.

Mergelsberg, O. (1935) Über die postimaginale Entwicklung (Physogastrie) undder Hermaphroditismus bei afrikanischen Termitoxenien (Dipt.). ZoologischeJahrbuchen, Anatomie 60, 345–398.




Mihályi, F. (1965) Rearing flies from faeces and meat, infected under naturalconditions. Acta Zoologica Academiae Scientiarum Hungaricae 11, 153–164.

Mik, J. (1864) Dipterologische Beiträge. Verhandlungen der Kaiserlich-Königlichen Zoologisch-Botanischen Gesellschaft in Wein 14, 793–814.

Mik, J. (1890) Dipterologische Miscellen. 16. Wiener Entomologische Zeitung9, 153–158.

Miles, P. (1968) Sarcophaga nigriventris Meigen (Dipt., Calliphoridae) bred fromHelix aspersa Müller (Mollusca, Helicidae). The Entomologist’s MonthlyMagazine 104, 227.

Mohan, S., Mohan, S. and Disney, R.H.L. (1995) A new species of scuttle fly(Diptera, Phoridae) that is a pest of oyster mushrooms (Agaricales,Pleurotaceae) in India. Bulletin of Entomological Research 85, 515–518.

Mokrzecki, S. (1923) Ueber den Parasitism von Fliegen im Körper vonLandschnecken. Zeitschrift für Wissenschaftliche Insektenbiologie 18,135–137.

Moran, S. (1987) Insect enemies of the landsnail Theba pisana in Israel. IsraelJournal of Entomology 21, 129–130.

Morris, H.M. (1922) On the larva and pupa of a parasitic phorid fly, Hypoceraincrassata Mg. Parasitology 14, 70–74.

Morrison, L.W. (2000) Biology of Pseudacteon (Diptera: Phoridae) ant para-sitoids and their potential to control imported Solenopsis fire ants(Hymenoptera: Phormicidae). Recent Research Developments in Entomology3, 1–13.

Morrison, L.W. and Gilbert, L.E. (1999) Host specificity in two additionalPseudacteon spp. (Diptera: Phoridae), parasitoids of Solenopsis fire ants(Hymenoptera: Formicidae). Florida Entomologist 82, 404–409.

Muma, M.H. (1954) Predators and parasites of the citrus tree snail. CitrusMagazine 16, 8–9.

Muma, M.H. (1955) Observations on the biology of the citrus tree snail. CitrusIndustry (January 1955), 6–9, 21.

Nadzhafarov, I.G. (1967) On role of different species of synanthropic fliesin circulation of oncosphaers of Taeniarhynchus saginatus. MeditsinskayaParasitologiya i Parazitarnye Bolenzi Moscow 34, 144–149 [in Russian, withEnglish summary].

Nandi, B.C. (1980) Studies on the larvae of flesh flies from India (Diptera:Sarcophagidae). Oriental Insects 14, 303–323.

Neck, R.W. and de Souza Lopes, H. (1973) On some North AmericanSarcophagidae and Calliphoridae (Diptera) reared from Gastropoda. RevistaBrasileira de Biologia 33, 183–192.

Nirmala, X., Hypsa, V. and Zurovec, M. (2001) Molecular phylogeny ofCalyptratae (Diptera: Brachycera): the evolution of 18S and 16S ribosomalrDNAs in higher dipterans and their use in phylogenetic inference. InsectMolecular Biology 10, 475–485.

Norris, K.R. (1965) The bionomics of blow flies. Annual Review of Entomology 10,47–68.

O’Flynn, M.A. and Moorhouse, D.E. (1980) Identification of early immaturestages of some common Queensland carrion flies. Journal of the AustralianEntomological Society 19, 53–61.

O’Hara, J.E. (1985) Oviposition strategies in the Tachinidae, a family of beneficialparasitic flies. Agriculture and Forestry Bulletin, University of Alberta 8,31–34.




Oldroyd, H. and Smith, K.G.V. (1973) Eggs and larvae of flies. In: Smith, K.G.V.(ed.) Insects and Other Arthropods of Medical Importance. British Museum ofNatural History, London, pp. 289–323.

Oosterbroek, P. and Courtney, G. (1995) Phylogeny of the nematocerous familiesof Diptera (Insecta). Zoological Journal of the Linnean Society 115, 267–311.

Pape, T. (1987) The Sarcophagidae (Diptera) of Fennoscandia and Denmark.Fauna Entomologica Scandinavica 19, 1–203.

Pape, T. (1992) Phylogeny of the Tachinidae family-group (Diptera: Calyptratae).Tijdschrift voor Entomologie 135, 43–86.

Pape, T. (1996) Catalogue of the Sarcophagidae of the World (Insecta: Diptera).Memoirs on Entomology, International Volume 8. Associated Publishers,Gainesville.

Pape, T., McKillup, S.C. and McKillup, R.V. (2000) Two new species of Sarco-phaga (Sarcorohdendorfia) Baranov (Diptera: Sarcophagidae), parasitoids ofLittoraria filosa (Sowerby) (Gastropoda: Littorinidae). Australian Journal ofEntomology 39, 236–240.

Parashar, B.D., Rao, Y.V.S. and Rao, K.M. (1997) Effect of environmental tempera-ture on development, fecundity, survival and predation of the snail-predatorSarcophaga misera (Dipt., Sarcophagidae). Entomophaga 42, 343–347.

Park, S.H. (1977) Studies on flies in Korea. II. Taxonomical studies in sarcophagidflies (Diptera). Bulletin of the Tokyo Medical and Dental University 24,249–284.

Paterson, H.E. (1958) A new Pyrellia species from Natal, together with miscella-neous notes on other Muscidae (Diptera). Journal of the EntomologicalSociety of South Africa 21, 300–305.

Paterson, H.E. (1959) Notes on the genus Alluaudinella G.-T. with the descriptionof a new species and a key to the known species of the genus (Diptera:Muscidae). Mémoires de l’Institut Scientifique de Madagascar (ser. E) 11,355–367.

Patton, W.S. and Evans, A.M. (1929) Insects, Ticks, Mites and Venomous Animalsof Medical and Veterinary Importance. Part I. Medical. University Press,Croydon.

Perris, E. (1850) Histoire des Métamorphoses de quelques Diptères Sarcophagamuscaria Meig.; Lucina fasciata Meig.; Gymnopoda tomentosa Macq.;Opomyza gracilis Meig.; Chyliza atriseta Meig. Mémoires de le SocieteNationale, de Scientifique l’Agriculture et des Arts de Lille (1850), 118–133.

Peterson, B.V. (1987) Phoridae. In: McAlpine, J.F. (ed.) Manual of Nearctic Diptera,Vol. 2. Research Branch, Agriculture Canada Monograph No. 28, pp. 689–712.

Pierce, W.D., Cushman, R.A. and Hood, C.E. (1912) The insect enemies of thecotton boll weevil. Bulletin of the United States Department of AgricultureBureau of Entomology 100, United States Department of Agriculture.

Pilsbry, H.A. (1919) A review of the land mollusks of the Belgian Congo chieflybased on the collections of the American Museum Congo Expedition,1905–1915. Bulletin of the American Museum of Natural History 40, 1–370.

Pollock, J.N. (1972) Functional morphology of male genitalia in Sarcophaga:a comparative study. The Entomologist 105, 6–14.

Pont, A.C. (1980) Calliphoridae. In: Crosskey, R.W. (ed.) Catalogue of the Dipteraof the Afrotropical Region. British Museum (Natural History), London,pp. 779–800.

Pont, A.C. and Dear, J.P. (1976) A synopsis of the genus Ochromusca Malloch,1927 (Diptera: Muscidae). Annals of the Natal Museum 22, 747–753.




Portschinskij, I.A. (1876) The materials for natural history of flies and their larvae,causing diseases in man and animals, with a review of phenomena of myiasis.Trudy Russkago Entomologicheskogo Obshchestva 9, 210–244 [in Russian].

Portschinskij, I.A. (1887a) Neue und wenig bekannte Dipteren (nebst biologischenAnmerkungen). V. Trudy Russkago Entomologicheskogo Obshchestva 21,3–20.

Portschinskij, I.A. (1887b) Diptera europea et asiatica nova aut minus cognita(Cum notis biologicis), V. Horae Societatis Entomologicae Rossicae 21, 3–20.

Portschinskij, I.A. (1894) On acrididas, pest of the crops and grasses in Perm,Tobol and Orenbourg Provinces. Parasites of grasshoppers, pruss, and locusts.Trudy Bureau Entomological 1, 1–131 [in Russian].

Povolny, D. (1982) Heteronychia (Heteronychia) nigricaudata Povolny etSlamecková nom. n. and notes on its synonomy, taxonomy and distribution.Annotations Zoologicae et Botanicae, Bratislava 150, 1–9.

Povolny, D. (1992) Zum Schneckenparasitismus und zur Taxonomie einigerSarcophagini-Arten (Diptera, Sarcophagidae). Acta Universitatis Agriculture,Brno 40, 169–185.

Povolny, D. and Groschaft, J. (1959) Tri vyznamní musí cizopasnici hlemyzdu zúzemi CSR. Zoologické Listy 8, 131–136.

Povolny, D. and Pospísil, V. (1989) Synanthropic trends in urban and extraurbantaxocenoses of Sarcophaginae (Diptera) in three central European cities.Memorias do Instituto Oswaldo Cruz (Rio de Janeiro) 84, 441–447.

Povolny, D. and Verves (1990) A preliminary list of Bulgarian Sarcophagidae(Diptera). Acta Entomologica Musei Nationalis Pragae 43, 283–329.

Povolny, D. and Verves, Y. (1997) The flesh-flies of Central Europe (Insecta,Diptera, Sarcophagidae). Sixiana Zeitschrift für Zoologie, Supplement 24,1–260.

Price, P.W. (1980) Evolutionary Biology of Parasites. Princeton University Press,Princeton.

Prins, A.J. (1982) Morphological and biological notes on six South Africanblow-flies (Diptera, Calliphoridae) and their immature stages. Annals of theSouth African Museum 90, 201–217.

Ramachandran Nair, K. (1968) Two sarcophagid parasites of phytophagousterrestrial snails in Mysore state, India. Technical Bulletin of theCommonwealth Institute of Biological Control 10, 113–127.

Ranade, D.R. (1965) The anatomy of the tracheal system of the larva of Muscadomestica nebulo Fabr. (Diptera, Muscidae). Indian Journal of Entomology27, 172–181.

Rees, N.E. (1973) Arthropod and Nematode Parasites, Parasitoids, and Predatorsof Acrididae in America North of Mexico. United States Department ofAgriculture Technical Bulletin No. 1460.

Reeves, W.K., Pape, T. and Alder, P.H. (2000) Biological notes on New WorldSarcophagidae (Diptera). Studia Dipterologica 7, 497–500.

Reinhard, H.J. (1929) Notes on the muscoid flies of the genera Opelousia andOpsodexia with the description of three new species. Proceedings of theUnited States National Museum 76, 1–9.

Rettenmeyer, C.W. and Akre, R.D. (1968) Ectosymbiosis between phorid flies andarmy ants. Annals of the Entomological Society of America 61, 1317–1326.

Richardson, A.M.M. (1974) Differential climatic selection in natural population ofland snail Cepaea nemoralis. Nature 247, 572–573.

Richet, R. (1990) Élevage de larves de diptères Sarcophagides. Image 39, 9–13.




Roback, S.S. (1951) A classification of the muscoid calyptrate Diptera. Annals ofthe Entomological Society of America 44, 327–361.

Roberts, M.J. (1971) The structure of the mouthparts of some calypterate dipteranlarvae in relation to their feeding habits. Acta Zoologica AcademiaeScientiarum Hungaricae 52, 171–188.

Robinson, W.H. (1965) Biology of a phorid feeding on slug eggs. Bulletin of theEntomological Society of America 11, 155.

Robinson, W.H. (1971) Old and new biologies of Megaselia species (Diptera,Phoridae). Studia Entomologica 14, 321–348.

Robinson, W.H. (1977) Phoridae (Diptera) associated with cultivated mushroomsin eastern North America. Proceedings of the Entomological Society ofWashington 79, 452–462.

Robinson, W.H. (1981) Terminalia of North American species of Group II Mega-selia (Aphiochaeta), and descriptions of four new species (Diptera: Phoridae).Proceedings of the Entomological Society of Washington 83, 489–504.

Robinson, W.H. and Foote, B.A. (1968) Biology and immature stages of Megaseliaaequalis, a phorid predator of slug eggs. Annual of the Entomological Societyof America 61, 1587–1594.

Rodhain, J. and Bequaert, J. (1916) Matériaux pour une étude monographique desDiptères parasites de l’Afrique. Première partie: histoire de Passeromyiaheterochaeta Villen. et de Stasia (Cordylobia) Rodhani Ged. BulletinScientifique de la France et de la Belgique 49, 236–289.

Rognes, K. (1986) The systematic position of the genus Helicobosca Bezzi witha discussion of the monophyly of the calyptrate families Calliphoridae,Rhinophoridae, Sarcophagidae and Tachinidae (Diptera). EntomologicaScandinavia 17, 75–92.

Rognes, K. (1991) Blowflies (Diptera, Calliphoridae) of Fennoscandia andDenmark. Fauna Entomologica Scandinavica 24, 1–1272.

Rognes, K. (1997) The Calliphoridae (blowflies) (Diptera: Oestroidea) are not amonophyletic group. Cladistics 13, 27–66.

Rohdendorf, B.B. (1937) Fam. Sarcophagidae. I. Sarcophaginae. Fauna SSSR 19,1–501 [in Russian, with German summary].

Rohdendorf, B.B. (1967) The directions of historical development of Sarco-phagidae (Diptera). Trudy Palaeontologii Institut Academy of Science USSR116, 10–91 [in Russian].

Rostand, J. (1920) Sur la biologie de Sarcophaga filia Pandellé [Dipt.]. Bulletin dela Société Entomologique de France 89, 215–216.

Rozkosny, R. (1968) Malacophagie als Lebensweise von Dipterenlarven inMitteleuropa. Abhandlungen und Berichte des Naturkundemuseums Görlitz44, 165–170.

Rueda, L.M. (1985) Some Philippine blowflies (Diptera: Calliphoridae) II. Sub-families Chrysomyinae, Rhiniinae and Ameniinae. Philippine Entomologist6, 362–390.

Salt, G. (1968) The resistence of insect parasitoids to the defence reactions of theirhosts. Biological Review 43, 200–232.

Sanjean, J. (1957) Taxonomic studies of Sarcophaga larvae of New York,with notes on the adults. Memoirs of the Cornell University AgriculturalExperimental Station 349, 1–115.

Schlinger, E.I. (1987) The biology of the Acroceridae (Diptera): true endo-parasitoids of spiders. In: Nentwig, W. (ed.) Ecophysiology of Spiders.Springer-Verlag, Berlin, pp. 319–327.




Schmitz, H. (1908) Helix-huisjes, gevuld met puparia von Phoriden. Tijdschriftvoor Entomologie 51, 57–58.

Schmitz, H. (1910) Zur Lebensweisse von Helicobosca muscaria Mg. Zeitschriftfür Wissenschaftliche Insektenbiologie 6, 107–109.

Schmitz, H. (1914) Dric neue Phoriden aus Afrika. Jaarboek NatuurhistorischGenootschap in Limburg (1914), 105–111.

Schmitz, H. (1916a) Neue phoriden aus Belgisch-Kongo, gesammelt von Dr. Jos.Bequaert. Zoologische Mededeelingen 2, 1–10.

Schmitz, H. (1916b) Zur Kenntnis einiger Phoridenarten und ihrer Synonyme.Wiener Entomologische Zeitung 35, 227–234.

Schmitz, H. (1917) Biologische Beziehungen zwischen Dipteren und Schnecken.Biologischen Zentralblatt 37, 24–43.

Schmitz, H. (1925) Sumatranische Insekten (Beitrag III) Phoriden I.Entomologische Mitteilungen 14, 58–62.

Schmitz, H. (1929a) Zur Kenntnis einiger von Dr. Jos Bequaert gesammelterafrikanischer Phoriden. Revue de Zoologie et de Botanique Africaines 18,37–43.

Schmitz, H. (1929b) Revision der Phoriden. Ferd Dummlers, Berlin.Schmitz, H. (1938) Drei neue aus toten Schnecken gezuechtere japanische

Phoriden. Natuurhistorisch Maandblad 27, 80–83.Schmitz, H. (1938–58) Phoridae. In: Lindner, E. (ed.) Die Fliegen der Palaerk-

tischen Region, Vol. 141. E. Schweizerbart’sche Verlagsbuchhandlung,Stuttgart, pp. 1–512.

Schmitz, H. (1940) Eine neue ostasiatische Spiniphora. NatuurhistorischMaandblad 29, 78–79.

Schmitz, H. (1941) Über die Larve von Chaetopleurophora pygidialis M. ErsteMitteilung. Natuurhistorisch Maandblad 30, 63–66.

Schmitz, H. (1958) Acht neue und einige bekannte Phoriden aus Angola und demBelgischen Kongo (Phoridae, Diptera). Publicacoes Culturais da Companhiade Diamantes de Angola (Museu do Dundo, Estudos Diversos XV) 40, 13–62.

Schumann, H. (1954) Morphologisch-systematische Studien an Larvene vonhygienisch wichtigen mitteleuropaischen Dipteren der FamilienCalliphoridae-Muscidae. Wissenschaftliche Zeitschrift der UniversitatGreifswald 3, Mathematisch-Naturewissenschaftliche Reihe 4/5, 245–274.

Schumann, H. (1973) Revision der palaerktischen Melinda-Arten (Diptera:Calliphoridae). Deutsche Entomologische Zeitschrift 20, 293–314.

Schumann, H. (1986) Family Calliphoridae. In: Soós, Á and Papp, L. (eds) Cata-logue of the Palaearctic Diptera Calliphoridae-Sarcophagidae 12, pp. 11–58.

Séguy, E. (1921) Les Diptères qui vivent aux dépans des escargots. Bulletin duSociété Entomologique de France (1921), 238–239.

Séguy, E. (1928) Etudes sur les mouches parasites. Tome 1. Conopides, Oestrideset Calliphorines de l’Europe occidentale. Recherches sur la morphologie etla distribution géographique des Diptères à larves parasites. EncyclopédieEntomologique (series A) 9, Paul Lechevalier, Paris, pp. 1–25.

Séguy, E. (1932) Études sur les diptères parasites ou prédateurs des sauterelles.Encyclopédie Entomologique, Paris, ser.B. II. Diptera 6, 11–40.

Séguy, E. (1941) Études sur les mouches parasites. 2. Calliphorides. Calliphorines(suite), sarcophagines et rhinophorines de l’Europe occidentale etmeridionale. Encyclopédie Entomologique, Paris, ser. A 21, 1–436.

Séguy, E. (1953) Diptères du Maroc. Encyclopédie Entomologique, Paris, ser. B. II.Diptera 11, 77–92.




Séguy, E. (1965) Le Sarcophaga nigriventris parasite de l’abeille domestiqueen Europe occidentale (Insecte Diptère Calliphoridae). Bulletin du MuséumNational d’Histoire Naturelle Paris (ser. 2) 37, 407–411.

Senior-White, R. (1924) New Ceylon Diptera. Spolia Zeylanica 12, 375–406.Shewell, G.E. (1987a) Calliphoridae. In: McAlpine, J.F. (ed.) Manual of Nearctic

Diptera, Vol. 2. Research Branch, Agriculture Canada Monograph No. 28,pp. 1133–1145.

Shewell, G.E. (1987b) Sarcophagidae. In: McAlpine, J.F. (ed.) Manual of NearcticDiptera, Vol. 2. Research Branch, Agriculture Canada Monograph No. 28,pp. 1159–1186.

Shipley, A.E. (1920) The fly and the snail. Country Life 47, 14–15.Sinclair, B.J. (1992) A phylogenetic interpretation of the Brachycera (Diptera)

based on the larval mandible and associated mouthpart structures. SystematicEntomology 17, 233–252.

Sinclair, B.J., Cumming, J.M. and Wood, D.M. (1994) Homology and phylogeneticimplications of male genitalia in Diptera – lower Brachycera. EntomologicaScandinavica 24, 407–432.

Siverly, R.E. and Schoof, H.F. (1955) Utilization of various production media bymuscoid flies in a metropolitan area III. Fly production in relation to cityblock environment. Annals of the Entomological Society of America 48,325–329.

Skidmore, P. (1973a) Notes on the biology of Palaearctic muscids (1). TheEntomologist 106, 25–48.

Skidmore, P. (1973b) Notes on the biology of Palaearctic muscids (2). TheEntomologist 106, 49–59.

Skidmore, P. (1985) The Biology of the Muscidae of the World. Dr W. JunkPublishers, Dordrecht.

Smedley, N. (1928) Achatina fulica (Fer.), the giant snail, as a possible source ofdisease. Malayan Naturalist 2, 47–48.

Smith, K.G.V. (1989) An introduction to the immature stages of British flies.In: Dolling, W.R. and Askew, R.R. (eds) Handbooks for the Identification ofBritish Insects 10 (14). Royal Entomological Society of London, London.

Stegmaier, C.E. (1972) Notes on some Sarcophagidae (Diptera) reared from snails(Mollusca) in Florida. Florida Entomologist 55, 237–242.

Stephenson, J.W. (1965) Slug parasites and predators. Rothamsted ExperimentalStation Report for 1964, 188.

Stephenson, J.W. and Knutson, L.V. (1966) A resumé of recent studies of inverte-brates associated with slugs. Journal of Economic Entomology 59, 356–360.

Stevens, J. and Wall, R. (1997) The evolution of ectoparasitism in the genus Lucilia(Diptera, Calliphoridae). International Journal for Parasitology 27, 51–59.

Suenaga, O. (1959) Ecological studies of flies. 4. On the flies breeding out from thecarcasses of small animals. Endemic Diseases Bulletin of Nagasaki University1, 343–352 [in Japanese, with English summary].

Sychevskaya, V.I. (1965) On the fauna of synanthropic flies of Tien Shan andAltay. Entomological/Studies in Kirgizia, Frunze (1965), 43–49 [in Russian].

Sychevskaya, V.I. and Petrova, T.A. (1958) On importance of flies in distributionof helminth eggs in Uzbekistan. Zoologicheskii Zhurnal 37, 563–569 [inRussian, with English summary].

Sychevskaya, V.I., Gruditzyna, M.V. and Vyrvikhvost, L.A. (1959a) The epidemio-logical role of synanthropic flies in Buchara. Entomologicheskoe Obozrenie38, 568–578 [in Russian, with English summary].




Sychevskaya, V.I., Skopina, N.P. and Petrova, T.A. (1959b) The pollution ofsynanthropic flies by dysenteric-bacillus and helminth eggs in Fergana.Trudy Uzbekistanskogo Instituta Malarii i Meditsinskoi Parasitologii,Samarkand 4, 225–235 [in Russian].

Taylor, J.W. (1914) Monograph of the Land and Freshwater Mollusca of the BritishIsles. Taylor Brothers, Leeds.

Taylor, J.W. (1921) Monograph of the Land and Freshwater Mollusca of the BritishIsles 24. Helicidae. Taylor Brothers, Leeds.

Thompson, P.H. (1978) Parasitism of adult Tabanus subsimilis subsimilisBellardi (Diptera: Tabanidae) by a miltogrammine sarcophagid (Diptera:Sarcophagidae). Proceedings of the Entomological Society of Washington 80,69–74.

Thompson, W.R. (1920) Recherches sur les Diptères parasites des larves desSarcophagidae. Bulletin Biologique de la France et de la Belgique 54,313–463.

Thompson, W.R. (1921) Contribution a la connaissance des formes larvairesdes Sarcophagides. I. Engyzops Pecchiolii Rond. Bulletin de la SociétéEntomologique de France (1921), 27–31.

Thompson, W.R. (1934) The tachinid parasites of woodlice. Parasitology 26,378–448.

Tibana, R. (1976) Duas novas espécies do gênero Helicobia (Diptera,Sarcophagidae) do Brasil. Revista Brasileira de Biologia 36, 1–6.

Tiensuu, L. (1939) Die Sarcophagiden (Dipt.) Finnlands. Annales EntomologiciFennici 5, 255–266.

Townsend, C.H.T. (1892) Description of a Sarcophaga bred from Helix. Psyche 6,220–221.

Trelka, D.G. and Berg, C.O. (1979) Behavioural studies of the slug-killing larvaeof two species of Tetanocera (Diptera: Sciomyzidae). Proceedings of theEntomological Society of Washington 79, 475–486.

Trelka, D.G. and Foote, B.A. (1970) Biology of slug-killing Tetanocera (Diptera:Sciomyzidae). Annals of the Entomological Society of America 63, 877–895.

Trofimov, G.K. (1969) The species of subfamily Sarcophaginae in synanthropiccomplexes of flies of southeastern part of Great Caucasus and neighbouringplains (Diptera, Sarcophagidae). Trudy Azerbaidzhanskogo NauchnoIssledouatel Skogo Instituta Meditsinskoi Parazitologii I TropicheskoiMeditsiny 7, 147–153 [in Russian, with French summary].

Trofimov, G.K. and Engelhardt, L.S. (1965) The research of synanthropic flies ofBaku city on intestinal protozoa of man. Trudy Azerbaidzhanskogo NauchnoIssledouatel Skogo Instituta Meditsinskoi Parazitologii I TropicheskoiMeditsiny 5, 186–188 [in Russian, with French summary].

Vala, J.-C. (1984) Phenology of Diptera Sciomyzidae in a Mediterranean forestrybiotop. Entomologica Basiliensia 9, 432–440.

Vala, J.-C., Gbedjissi, G., Knutson, L. and Dossou, C. (2000) Extraordinary feedingbehaviour in Diptera Sciomyzidae, snail-killing flies. Comptes Rendus del’Académie des Sciences 323, 299–304.

Van Achterberg, C. and Bin, F. (1981) Notes on two species of Dinotrema Foerster(Hym., Braconidae, Alysiinae) with observations on the hymenopterousparasite-complex of Spiniphora dorsalis Becker (Dipt., Phoridae) indead Helix spp. (Mollusca). Entomologische Berichten, NederlandischeEntomologische, Amsterdam 41, 104–112.




Van Dijken, M.J. and Waage, J.K. (1987) Self and conspecific superparasitism bythe egg parasitoid Trichogramma evanescens. Entomologiae Experimentaliset Applicata 43, 183–192.

Van Emden, F.I. (1949) (Exhibit of the muscid fly Ochromusca trifaria Bigotat meeting on 7 September 1949). Proceedings of the Royal EntomologicalSociety of London C 14, 31.

Van Emden, F.I. (1950) Dipterous parasites of Coleoptera. The Entomologist’sMonthly Magazine 86, 182–206.

Van Emden, F.I. (1953) Host-selection and systematic position of Ameniini(Diptera). The Entomologist’s Monthly Magazine 89, 120.

Van Emden, F.I. (1954) Diptera Cyclorrhapha Calyptrata (1), Section (a).Tachinidae and Calliphoridae. Handbook Identification of British Insects10, 4(a), pp. 1–133.

Van Emden, F.I. (1956) Contributions à l’étude de la faune entomologiquedu Ruanda-Urundi (Mission P. Basilewsky 1953). CVIII. Diptera Muscidae.Annales du Musée Royal du Afrique, Tervuren, Sciences Zoologiques 175,375–404.

Verves, Y.G. (1976) On the study of sarcophagids (Diptera, Sarcophagidae) –parasites of terrestrial gastropods. Vestnik Zoologii 3, 28 [in Russian].

Verves, Y.G. (1980) Some Sarcophagidae (Diptera) from Afghanistan. FoliaEntomologica Hungarica 41, 355–357.

Verves, Y.G. and Kuzmovich, L.G. (1979) Sarcophaginae (Diptera, Sarcophagidae)– parasites of terrestrial gastropods in Ternopol’ region. Vestnik Zoologii 4,16–21 [in Russian, English summary].

Verves, Y.G. and Narchuk, E.P. (1986) The development of trophic connections inthe larvae of Diptera Brachycera Cyclorrhapha Schizophora. Trudy SocietatisEntomologicae USSR 68, 79–85 [in Russian].

Wallman, J.F. (2001) Third-instar larvae of common carrion-breeding blowflies ofthe genus Calliphora (Diptera: Calliphoridae) in South Australia. InvertebrateTaxonomy 15, 37–51.

Wandolleck, B. (1898) Die Stethopathidae eine neue flügel- und schwingerloseFamilie der Diptera. Zoologisches Jahrbächer, Abteilung für Systematik 11,412–439.

West, L.S. (1951) The Housefly. Its Natural History, Medical Importance, andControl. Comstock Publishing Co., Ithaca, New York.

Wiegmann, B.M., Mitter, C. and Thompson, F.C. (1993) Evolutionary origin ofthe Cyclorrhapha (Diptera): tests of alternative morphological hypotheses.Cladistics 9, 41–81.

Wiegmann, B.M., Tsaur, S.C., Webb, D.W., Yeates, D.K. and Cassel, B.K. (2000)Monophyly and relationships of the Tabanomorpha (Diptera: Brachycera)based on 28S ribosomal gene sequences. Annals of the Entomological Societyof America 93, 1031–1038.

Wildermuth, V.L. (1915) The alfalfa caterpillar. Bulletin of the United StatesDepartment of Agriculture Bureau of Entomology 124, United StatesDepartment of Agriculture.

Wood, D.M. (1987) Tachinidae. In: McAlpine, J.F. (ed.) Manual of NearcticDiptera, Vol. 2. Research Branch, Agriculture Canada, Monograph 32. Ottawa,pp. 1193–1269.

Wood, D.M. and Borkent, A. (1989) Phylogeny and classification of theNematocera. In: McAlpine, J.F. and Wood, D.M. (eds) Manual of Nearctic




Diptera, Vol. 3. Research Branch, Agriculture Canada, Monograph 32. Ottawa,pp. 1333–1370.

Woodcock, B.A., Watt, A.D. and Leather, S.R. (2002) Aggregation, habitat qualityand coexistence: a case study on carrion fly communities in slug cadavers.Journal of Animal Ecology 71, 131–140.

Woodley, N.E. (1989) Phylogeny and classification of the ‘Orthorraphous’Brachycera. In: McAlpine, J.F. and Wood, D.M. (eds) Manual of NearcticDiptera, Vol. 3. Research Branch, Agriculture Canada, Monograph 32. Ottawa,pp. 1371–1395.

Yarkulov, F. (1972) Phora holosericea (Diptera, Phoridae), a predator of rootaphids. Zoologicheskii Zhurnal 51, 1415–1418.

Yeates, D.K. and Greathead, D. (1997) The evolutionary pattern of host use in theBombyliidae (Diptera): a diverse family of parasitoid flies. Biological Journalof the Linnean Society 60, 149–185.

Yeates, D.K. and Wiegmann, B.M. (1999) Congruence and controversy: towarda higher-level phylogeny of Diptera. Annual Review of Entomology 44,397–428.

Yeates, D.K., Logan, D.P. and Lambkin, C. (1999) Immature stages of the bee flyLigyra satyrus (F.) (Diptera: Bombyliidae): a hyperparasitoid of canegrubs(Coleoptera: Scarabaeidae). Australian Journal of Entomology 38, 300–304.

Zhang, M. (1982) A study of the larvae of some common sarcophagid flies fromChina. Entomotaxonomia 4, 93–106 [in Chinese, with English summary].

Zumpt, F. (1965) Myiasis of Man and Animals in the Old World. Butterworth andCo., London.

Zumpt, F. (1972) Calliphoridae (Diptera Cyclorrhapha). Part IV. Sarcophaginae.Exploration du Parc National Virunga Mission G. f. de Witte (1933–1935),101, 1–264.




diptera as predators and parasitoids of terrestrial ... · the nematocera include generally small,...

Documents