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Arquivo Brasileiro de Medicina Veterinária e Zootecnia

versão impressa ISSN 0102-0935versão On-line ISSN 1678-4162

Arq. Bras. Med. Vet. Zootec. v.53 n.2 Belo Horizonte abr. 2001

https://doi.org/10.1590/S0102-09352001000200004 

Would Chrysomya albiceps (Diptera: Calliphoridae) be a beneficial species?

[Seria Chrysomya albiceps (Diptera: Calliphoridae) uma espécie benéfica?]

 

N.G. Madeira

Instituto de Biociências da UNESP
Caixa Postal 510
18 618-000 - Botucatu, SP

 

Recebido para publicação, após modificações, em 29 de setembro de 2000.
E-mail: nmadeira@ibb.unesp.br

 

 

ABSTRACT

Chrysomya albiceps (Widemann) develops on animal carcasses and may cause secondary myiases. An adult female Merino sheep presented a lesion of roughly circular shape with a 7.5cm radius in the anterior part of the thorax. A large number of second-instar larvae was removed from the lesion in addition to first-instar larvae from the wool. A third-instar larva was also obtained from the same lesion site and in the laboratory gave origin to a Cochliomyia hominivorax (Coquerel) adult insect. The larvae retrieved from the lesion were nurtured in laboratory. Pairs consisting of 100 individuals were formed with the adult specimens obtained from the larvae and kept in two cages. In all of the 800 adults reared in the laboratory and examined (100 per generation) the propisternal seta was absent in the spiracle on both sides, this trait was highly stable. The 200 larvae examined, 15 per generation, did not present spines in the column of the ventral process of the penultimate abdominal segment and the column of the ventral process was triangular and the apex of the column process presented numerous spines. These characteristics allowed identifying these specimens as C. albiceps. However, since C. albiceps has the ability to damage intact tissues, it may be causing relevant aggravation when associated with C. hominivorax and can not be considered innocuous.

Keywords: Chrysomya albiceps, myiasis, species associations, Diptera

 

RESUMO

Chrysomya albiceps (Widemann) é uma mosca que se desenvolve em carcaças e opcionalmente pode causar miíase secundária. Larvas de segundo estádio foram removidas de uma lesão existente em uma ovelha da raça Merino em Botucatu. Entre a lã, ao redor da lesão, foram encontradas larvas de primeiro estádio. Também no interior da lesão foi obtida uma larva de terceiro estádio. As larvas foram mantidas em laboratório e delas obtidos insetos adultos, com 50 casais formados e mantidos em gaiolas por oito gerações. De cada geração, 100 adultos eram sacrificados e examinados morfologicamente, com os seus caracteres confrontados com os de Chrysomya rufifacies. A larva de terceiro estádio deu origem a Cochliomyia hominivorax e as demais a C. albiceps. Foi verificado que C. albiceps, além de ser capaz de danificar tecido integro, é também uma possível predadora de larvas de C. hominivorax. A importância de C. albiceps para os animais domésticos e sua associação com C. hominivorax é aqui discutida.

Palavras-chave: Chrysomya albiceps, miíase, associação de espécies, Diptera

 

 

INTRODUCTION

Until the beginning of the 1970’s Chrysomya albiceps (Wiedemann) was restricted to Africa, southern Europe and Asia, whereas by the end of the decade it started to be found in the Neotropical region, being first detected in Brazil (Guimarães et al., 1978), Argentina and Paraguay (Mariluis, 1983), Peru and Colombia (Baumgartner & Greenberg, 1985). At that time, another species closely similar to the first one, Chrysomya rufifacies (Macquart), started to be detected in Central (Jirón, 1979) and North America (Baumgartner, 1993). In South America, C. rufifacies was detected only once (Mariluis & Schnack, 1989) but did not become established, in contrast to C. albiceps which in some studies was even found to predominate over the other Calliphoridae species in Brazil (Madeira, 1985; Costa et al. 1992; Campos & Barros, 1995; Souza & Linhares, 1997; Vianna et al., 1998).

C. albiceps and C. rufifacies are biologically equivalent, both developing on animal carcasses and optionally preying on larvae of other species. This predation is favorable for adult individuals since the act of C. albiceps larvae preying on Phaenicia sericata (Meigen) larvae favors the emergence of C. albiceps adults capable of producing a larger number of eggs compared to adults maintained in pure culture during the larval phase (Ullyett, 1950). Phaenicia eximia (Wiedemann) adults that emerge from carcasses where C. albiceps is predominat are of much smaller size than adults occurring in nature, suggesting the occurrence of competition for the substrate between the two species during the larval phase (Madeira,1985). C. albiceps has predatory behaviour and in laboratory preys preferentially Cochliomyia macellaria (Fabricius) (Faria et al., 1999). In South Africa, P. sericata larvae are preyed upon and eliminated from the environment in the presence of C. albiceps (Ullyett, 1950). The impact on the primitive New World Calliphoridae fauna after the establishment of the exotic Chrysomya species is still poorly understood in most aspects, but has been suggested as a cause of dislocation of autochthonous species that gave origin to behavioral changes leading to the exploitation of living tissues of animals (Azeredo-Espin & Madeira, 1996). Another property attributed to these species is the induction of secondary myiases in domestic animals (Zumpt, 1965; Baumgartner, 1993). In Brazil, C. albiceps was detected in cattle and sheep (Leite et al., 1983; Oliveira, 1985), appearing in association with Cochliomyia hominivorax (Coquerel) in sheep. The incidence of C. albiceps in a region of the Rio Grande do Sul State (Brazil) was 50% and the mortality rate was 30% in Corriedale and Polwarth races (Prates et al., 1999).

The adults of C. albiceps and C. rufifacies show morphological characteristics that divide them into two distinct species (Holdaway, 1933). However, due to the variability of these morphological characteristics between populations, C. albiceps and C. rufifacies have been considered as a single species, with C. albiceps having C. rufifacies as a subspecies (Zumpt, 1965). The larvae of the two species were indistinguishable until Erzinclioglu (1987) and Tantawi & Greenberg (1993) proposed morphological differences that separate third instar larvae. It has been proposed that the analysis of mitochondrial DNA may distinguish the two species (Wells & Sperling, 1999)

The objective of the present study was to explore the association between two species of larvae causing myiasis in sheep and to evaluate the morphological characteristics used for the determination of the species and their constancy along eight generations.

 

MATERIALS AND METHODS

Larvae were taken from a roughly circular 7.5cm radius lesion in the right anterior part of the thorax of a female Merino sheep. A large number of second-instar larvae was removed with forceps from the lesion and placed in a flask containing 200g ground beef and 10ml citrated bovine blood. A third-instar larva was also obtained from the same site and placed on 50g of meat and blood. Adjacent to lesion and localized at the base of the wool coat many first-instar larvae were collected and placed in a flask containing 200g blood and meat. The remaining larvae present in the wool were killed with an insecticide applied to the site and the lesion was treated with an antiseptic. In the laboratory, the larvae were maintained on ground beef and blood until they reached full development. Pupation occurred on a tray containing sand and placed below the container where the larvae were reared. The pupae were transferred to fly-rearing cages containing water and a dry mixture of powdered milk, sucrose and yeast extract (3:3:1).

Pairs consisting of 100 individuals were formed with the adult specimens of C. albiceps kept in two cages (25 pairs per cage). The ovipositing medium used was a mouse carcass (60g) on which the larvae were also reared. The pupation site was a tray containing sand placed below the container for larval rearing.

 

RESULTS

The larvae retrieved from the lesion developed into C. albiceps adults, while the single third-instar larva also removed from the lesion gave origin to a C. hominivorax female. The first instar larvae retrieved from the wool gave origin to C. albiceps. A total of 147 adults emerged, all of them being C. albiceps (Fig. 1 and 2).

 

 

 

 

In all of the 800 adults reared in the laboratory and examined (100 per generation) the propisternal seta was absent in the spiracle on both sides. The 200 larvae examined, 15 per generation, did not present spines in the column of the ventral process of the penultimate abdominal segment. The column of the ventral process was triangular in shape and the apex of the column of the dorsomedial process presented numerous spines.

 

DISCUSSION

The C. albiceps adults retrieved from the lesion and those kept in the laboratory for eight generations maintained the traits used to determine the species described by Holdaway (1933) and Dear (1985). The absence of the stigmal seta persisted throughout the generations on both sides, indicating that this trait was highly stable in the sample collected. Some populations have this seta on one side but not on the other, or on both sides (Tantawi & Greenberg, 1993). This trait has been reported to vary among populations and therefore can not be used to separate and consider C. albiceps and C. rufifacies as distinct species, with C. rufifacies being considered a subspecies of C. albiceps (Zumpt, 1965). The present experiments showed that the traits used were not variable, suggesting that the population analyzed here is homozygous for this trait, since the F1 generation resulting from crosses between these two species gives origin to individuals with the presence of this seta (Ullerich, 1963).

The third-instar larvae examined showed the presence of lateral spines on the column of the dorsal process, in agreement with data reported by Tantawi & Greenberg (1993) but in contrast to data reported by Erzinclioglu (1987) who considered the absence of lateral spines to be a differentiating trait for this species.

The relationship between species causing primary myiasis and their interactions with secondary species is a field still to be explored in tropical America. The cause for C. albiceps oviposition was probably the lesion caused by C. hominivorax, a fly that must obligatorily feed on living tissue to continue its life cycle. An association between C. albiceps and C. hominivorax was observed during artificial infestation of sheep with C. hominivorax larvae, when C. albiceps larvae were detected five days after inoculation of C. hominivorax larvae (Oliveira, 1985). However, this author did not observe differences in lesion size between the animals where the two species were present and the other 11 sheep inoculated in the same experiment but not secondarily infected by another fly species. This may have been due to the age of the larvae, since in this species only L2 and L3 larvae are able to prey on other larvae (Zumpt, 1965). These must also be the stages that destroy tissue since it was observed that the lesion occurred only where there were L2 larvae. Another finding that supports this notion is that this author detected many C. hominivorax larvae, whereas it was obtained only one specimen of this species. Since this larva was not fully developed, it was assumed that the remaining ones were preyed upon by the C. albiceps larvae. Also, in the first report of myiasis caused by C. albiceps in the Americas (Leite et al., 1983), the fact that only L3 larvae of this species were obtained was due to the very late occurrence of the finding, with primary larvae having already suffered predation by C. albiceps. The occurrence of myiasis caused only by C. rufifacies in Australia was attributed to the late retrieval of the sample or to the predation that occurred between retrieval of the larvae and transportation to the laboratory, where fragments of other flies larval cuticles were detected (Watts et al., 1976). The data obtained indicate that the myiases caused by this species in Brazil may be only secondary, with no evidence that might confirm their ability to start a lesion in tissue. Due to their ability to prey on species that cause primary myiasis, these larvae were considered to be beneficial. However, since the extent of the lesion observed was very large and caused considerable discomfort to the animal, this species cannot be considered beneficial for the possible control it may have on C. hominivorax. C. rufifacies is considered to be beneficial by some authors because it controls several species of harmful flies (Baumgartner, 1993). This conclusion is due to the fact that this species reduces the population of other harmful calliphorids that share carcasses with it. However, since C. albiceps also has the ability to damage intact tissues, it is one more fly causing problems when associated with C. hominivorax. The species was also not considered beneficial in Africa by Zumpt (1965).

The association of these two species causes more problems than benefits. During the period of larval collection, four other sheep had already developed myiasis, described by the managing staff as a condition similar to that described above. The introduction of breeds of sheep more susceptible to myiasis may have contributed to an increase of cases, as reported also in Europe, although not conclusively (Hall, 1997). In South Africa, Doper sheep myiasis caused by C. albiceps was more frequent in relation to others breeds (Fourie & Horak, 2000). Since C. hominivorax is very common among sheep flocks in the region (Madeira et al., 1998), a worsening of the myiasis problem is expected.

 

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