Corethrella

Published, First, 2008, The Frog-Biting Midges of the World (Corethrellidae: Diptera), Zootaxa 1804, pp. 1-456 : 250-251

Corethrella as Vectors of Species of Trypanosoma

Species of Trypanosoma are blood parasites that occur in all classes of vertebrates and most are vectored by blood-sucking arthropods (insects and ticks) or leeches. Two species are the cause of severe diseases in humans, Chagas’ disease and Sleeping Sickness.

There are over 80 species of Trypanosoma recorded from anurans but the taxonomy is confused, with the features of many species uncertain ( Bardsley and Harmsen 1973; Miyata 1978; Delvinquier and Freeland 1989; Werner 1993; Desser 2001). In addition, there are almost certainly many more species which are unnamed. The genus is distributed nearly worldwide, likely wherever anurans are found. The vectors for most of these species are unknown but at least some are transmitted by leeches; experimental studies and the presence of Trypanosoma in some tadpoles supports this hypothesis ( Martin and Desser 1991; Miyata 1978). Bardsley and Harmsen (1973) suggested blood-sucking insects as probable vectors, and Anderson and Ayala (1968) found that Bufo boreas acquired trypanosomes by eating infected Lutzomyia vexator (Coquillett) (as Phlebotomus vexator occidentis Fairchild and Hertig ). After McKeever (1977) showed that calling frogs attracted female Corethrella, Johnson et al. (1993) studied trypanosomes found in Hyla cinerea and their associated frog-biting midges in Florida. They discovered that 70% of 215 male frogs were infected with an unnamed trypanosome and none of 31 female frogs were infected. Infection rates of male frogs rose from 7.7 –70.7% in April and May, at the beginning of the frog’s breeding season, to a constant 100% during June-September in two consecutive years. Examination of female C. wirthi collected both just approaching and after biting these frogs revealed conspecific trypanosomes in their mid and hindguts. Although no trypanosomes could be found in the salivary glands of the midges, infection of previously uninfected frogs was observed after these had been bitten by C. wirthi in the field. It is uncertain exactly how the trypanosomes are being transmitted from the midges to the frogs but transmission directly from the mouthparts, through fecal material ( Corethrella excrete a drop of fluid while or immediately after feeding, pers. obs.) or through ingestion of the whole fly (very unlikely in Corethrella ) are known in other insects. Female C. brakeleyi , biting in low numbers, did not have the trypanosomes in their guts, suggesting that only some species of Corethrella act as vectors, at least of particular frog species.

The presence of trypanosomes in just males of a given frog species is likely a diagnostic indication that one or more species of Corethrella are vectors of that trypanosome species. Bernal et al. (2006), for example, found trypanosomes in male Physalaemus pustulosus in Panama and considered female Corethrella to be the likely vectors. However, the presence of trypanosomes in both males and females may not exclude Corethrella as a vector as there are records of female Corethrella biting female frogs when males are in amplexus and yet calling (Bourne and Boege Tobin, pers. comm.).

The various frog species bitten by a particular species of Corethrella (see “Host Specificity”) will likely be important in understanding both the distribution and taxonomy of species of Trypanosoma . It would not be surprising, for example, to discover the same Trypanosoma species discovered in Hyla cinerea and C. wirthi , to also be present in other frogs being bitten by C. wirthi (i.e. Hyla versicolor , H. avivcoca , H. femoralis , H. chrysoscelis ).

Because Trypanosoma are most closely related to other protozoans which are insect parasites, it is generally considered that transmission by blood-sucking insects is the plesiotypic condition for the genus and that vectoring by leeches is secondary. Within the genus, phylogenetic analyses indicates that those species which infect aquatic vertebrate taxa (i.e. fish, amphibians, turtles) form a single clade which is the sister group to all remaining species of Trypanosoma ( Hamilton et al., 2007) . Based on the presence of distantly related trypanosomes in the Old and New World, Stevens et al. (1999) hypothesized that Trypanosoma likely evolved before the split of South America and Africa and that an origin of 100 million years ago or older is reasonable. Unfortunately, the fossil record is relatively recent and sparse, with only a single record, in Dominican amber ( Poinar 2005), providing no further clues about the age of the genus.

There is evidence that at least one species of Trypanosoma is closely tied to the feeding habits of a species of Corethrella . Johnson et al. (1993) found that trypanosomes in male Hyla cinerea were present in high numbers in peripheral tissue only at night, indicating a coordination between the life cycle of the trypanosomes and the vector C. wirthi (which feed only at night).

Trypanosomes in anurans seem to be primarily non-pathological, with few literature records of actual symptoms attributable to infection ( Brumpt 1924; Bardsley and Harmsen 1973; Delvinquier and Freeland 1989; Flynn 1973). Furthermore, trypanosomes may be present in great numbers in frog blood, with no apparent adverse affects.

The geological ages of the origins of Corethrella , anurans, and their Trypanosoma parasites, the presence of coordinated behaviors of all three groups, and the widespread presence of non-pathological species of Trypanosoma , all suggest that these three groups have been interacting and coevolving since at least the Lower Cretaceous and possibly even the late Jurassic. Early members of Corethrella may have been the primary vectors of trypanosomes of Jurassic and Cretaceous frogs, with leeches subsequently acting as vectors for fully aquatic stages (tadpoles) or taxa (fish). The restriction of Corethrella to smaller aquatic habitats, similar to those of anurans, may have been another important component of them becoming vectors of trypanosomes.

There is a possibility that another ancient group of biting flies, the Psychodidae , are involved in the transmission of trypanosomes to vertebrate hosts. However, the study by Anderson and Ayala (1968) was based on laboratory ingestion of infected flies by a species of toad and the presence of low levels of trypanosome occurrence in both toads and the fly in nature. It seems unlikely that the psychodid, Lutzomyia vexator , is normally readily available to the toad (females normally suck blood from lizards) and the transmission by ingestion is likely, at best, to be a weak mechanism for transmission.

Although it may be that species of Corethrella are vectors of anuran trypanosomes throughout most tropical and subtropical regions (Fig. 139), it is clear that extant species of Corethrella cannot be the primary vectors of trypanosomes for all anurans. Trypanosoma occur in anurans well outside the range of any species of Corethrella . For example, at least four forms of Trypanosoma occur in four species of toads in Lithuania ( Zickus 2002) while there are no extant Corethrella known from Europe (Fig. 139).