First record of Anopheles konderi Galvão & Damasceno (Diptera: Culicidae) carrying eggs of Dermatobia hominis (Linnaeus Jr.) (Diptera: Oestridae), from Oriximiná municipality, Pará, Brazil

Abstract

INTRODUCTION:  The muscoid fly Dermatobia hominis causes cutaneous myiases in mammals. Females of this species use a vector to carry their eggs to the host. This note describes Anopheles konderi acting as phoretic vector for D. hominis.

METHODS:  A female A. konderi carrying D. hominis was collected using light traps in Oriximiná, Pará, Brazil. The A. konderi specimen was identified at morphological and molecular levels.

RESULTS:  Eight eggs of D. hominis were observed on the Anopheles konderi female.

CONCLUSIONS:  Anopheles konderi, only the third Anopheles species recorded as a phoretic vector, may be a potential vector of D. hominis.

Keywords: Phoretic vector; Dermatobiasis; Reserva Estadual do Trombetas; Myiasis

Dermatobia hominis is a muscoid fly endemic to the Neotropical region. In Brazil, it is popularly known as mosca do berne. The larvae of this species cause cutaneous myiasis, also known as dermatobiasis, in a wide range of mammalian hosts, including humans. It is particularly important as a parasite of domestic animals, such as cattle and birds. Several wild animals are also infected¹. Dermatobiasis is of considerable economic importance, since affected cattle produce poor quality leather, as well as less meat and milk². In humans, the infections are painful but generally benign, even if the larvae reach maturity, but can be lethal in infants if the larvae penetrate the brain via the fontanelle³.

The females of D. hominis exhibit a characteristic reproductive behavior, namely, the use phoretic vectors to transmit their eggs to the host. This reproductive behavior was first recorded by Raphael Morales in Guatemala in 1911, and has subsequently been reported in several publications^1,4. In general, these vectors are zoophilous Diptera, particularly calyptrate flies of the families Calliphoridae, Muscidae, Tabanidae, Fanniidae, Anthomyiidae, Sarcophagidae, Tipulidae, Syrphidae, Asilidae, Dolichopodidae, Drosophilidae, Ephydridae, Tachinidae, Otitidae, Stratiomyidae, and Trupaneidae. Among non-calyptrate flies, species of Simuliidae and Culicidae have been recorded as vectors¹. In the latter, the genera Psorophora, Aedes, Mansonia, Haemagogus, Limatus, Onirion, Wyeomyia, Culex, Trichoprosopon, Johnbelkinia, and Anopheles have been recorded as phoretic vectors^1,4-6.

Recent studies have reported new phoretic vectors of D. hominis^2,7,8, which are generally calyptrate flies. In this note, we report for the first time the exploitation of Anopheles konderi, a dipterous non-calyptrate fly, as a phoretic vector of D. hominis.

During sorting of the specimens collected using CDC (Center for Disease Control) miniature light traps in July 2011 in Floresta Estadual do Trombetas [Sistema de Autorização e Informação em Biodiversidade (SISBIO) License Number 14054-3], Oriximiná municipality, Pará, Brazil (1°28′S; 56°22′W), a single female specimen of A. konderi, among several examined, was observed carrying eggs of D. hominis. The material was preserved in 80% ethanol and then carefully examined under a stereomicroscope (SV11; Zeiss) at ×66 magnification. As females of A. konderi are morphologically similar to those within the Anopheles oswaldoi complex⁹, the identification was molecularly confirmed by deoxyribonucleic acid (DNA) barcode analysis, using a 663-base pair region of the mitochondrial cytochrome oxidase subunit I (COI) gene. The specimen was photographed using a Celestron® model 44330 imaging system. The processes of sorting, microscopic analysis, taxonomic and molecular identification, and photography were conducted in the Laboratório de Genética de Populações e Evolução de Mosquitos Vetores de Malária e Dengue of Instituto Nacional de Pesquisas da Amazônia (INPA).

Eight eggs of D. hominis were found adhered to the ventral abdomen of the female A. konderi (Figure 1A, Figure 1B and Figure 1C), some of which had already hatched and were empty, whereas others were intact and contained visible larvae or were partially hatched. During handling of the material, some of the larvae became detached from their eggs (Figure 1D).

FIGURE 1
Anopheles konderi carrying the eggs and larvae of Dermatobia hominis: (A): and (B): Dorsal and ventral views, respectively, of a female A. konderi with eggs and partially hatched larvae attached to its abdomen (see arrows). (C):. Eggs of D. hominis attached to the abdomen of A. konderi. (D): Newly hatched larva of D. hominis. PHE: partially hatched eggs; UE: unhatched eggs; HE: hatched egg; A.: Anopheles; D.: Dermatobia .

Generally, a D. hominis female selects a phoretic vector that is of similar size to itself or smaller^4,7, and the number of eggs deposited is directly proportional to the body size of the vector¹⁰. For example, in Fanniidae, a family of dipterous muscoids, an average of 16.4 eggs of D. hominis has been reported per vector specimen⁷. In our study, the number of eggs found on A. konderi corroborates this information. Compared with other dipterous muscoids with bulkier bodies, which are the main disseminators of D. hominis eggs, the anopheline mosquitoes are smaller and thinner⁶.

Understanding the epidemiology of dermatobiasis in the Neotropics depends on knowledge of the biological, ecological, and ethological parameters of phoretic vectors implicated in the transmission of the D. hominis ectoparasite. To date, Anopheles konderi is the third species of Anopheles that has been reported as a phoretic vector of D. hominis, only preceded by A. boliviensis and A. intermedius^1,4. Little is known about these parameters regarding A. konderi. This is mainly due to problems associated with the taxonomic status of this species. Anopheles konderi is morphologically similar to A. oswaldoi, with which it was synonymized in the past, although the males of these two species can be distinguished based on subtle differences in their genitalia. Subsequently, studies have reported that these two species differ in terms of their behavioral patterns and ITS2 (Internal Transcribed Spacer) and COI molecular markers, and also possibly as malaria vectors^11,12. Currently, A. konderi is recognized as a distinct species from A. oswaldoi s.l., although it is a member of a group of cryptic species within the A. oswaldoi complex^11-13.

Dermatobia hominis occurs primarily in forests, thereby avoiding dehydration and excessive heat¹⁴. Their phoretic vectors are predicted to have, among other characteristics, diurnal and zoophilic habits^4,7. Specimens belonging to the A. oswaldoi complex have zoophilic behavior, generally inhabiting forests, but also show exophilic behavior⁹. Others have been observed to exhibit vespertine crepuscular and nocturnal activities, including biting humans, and it has been collected in human habitations¹⁵. As diurnal habit is one of the characteristics of D. hominis vectors, it is possible that the typically nocturnal A. konderi also has diurnal and/or crepuscular activities.

Although in the current study, we did not demonstrate that A. konderi routinely acts as a phoretic vector for the eggs of D. hominis, our observations indicate that this anopheline can potentially play this role, being one among the various dipteran species responsible for maintaining the incidence of dermatobiasis in wild animals.

REFERENCES

• ¹ Guimarães JH, Papavero N. Myiasis and in the Neotropical region: bibliographic database. São Paulo: Editora Plêidade; 1999. 308p.
• ² Marinho CR, Barbosa LS, Azevedo ACG, Queiroz MMC, Valgode MA, Aguiar-Coelho VM. Hemilucilia segmentaria (Fabricius, 1805) (Diptera: Calliphoridae) as New Biological Vector of Eggs of Dermatobia hominis (Linnaeus Jr., 1781) (Diptera: Oestridae) in Reserva Biológica do Tinguá, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 2003;98(7):937-38.
• ³ Dunn LH. Rearing the larvae of Dermatobia hominis Linn. in man. Psyche. 1930;37(4):327-42.
• ⁴ Bates M. Mosquitos as vectors of Dermatobia in eastern Colombia. Ann Entomol Soc Am. 1943;36(1):21-4.
• ⁵ Barreto P, Lee VH. Artrópodos hematófagos del Rio Raposo, Valle, Colombia. Caldasia. 1969;10(49):407-40.
• ⁶ Marchi MJ, Pereira PA, Menezes RMT, Tubaki RM. New records of mosquitoes carrying Dermatobia hominis eggs in the State of São Paulo, Southeastern Brazil. J Am Mosq Control Assoc. 2012;28(2):116-8.
• ⁷ Gomes A, Honer MR, Koller WW, Silva RL. Vetores de ovos de Dermatobia hominis (L. Jr., 1781) (Diptera: Cuterebridae) na região de cerrados do Mato Grosso do Sul, Brasil. Rev Bras Parasitol Vet. 1998;7(1):37-40.
• ⁸ Espindola CB, Couri MS. Fannia flavicinta Stein (Diptera, Fanniidae: a new vector of Dermatobia hominis (Linnaeus Jr.) (Diptera: Cuterebridae). Rev Bras Zool. 2004;21(1):115-16.
• ⁹ Faran M, Linthicum K. A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosq Syst. 1981;13:1-81.
• ¹⁰ Mateus G. El nuche y su ciclo de vida. Revista ICA. 1967;2(1):3-19.
• ¹¹ Marrelli MT, Malafronte RS, Flores-Mendoza C, Lourenco-De-Oliveira R, Kloetzel JK, Marinotti O. Sequence analysis of the second internal transcribed spacer of ribosomal DNA in Anopheles oswaldoi (Diptera: Culicidae). J Med Entomol. 1999;36(6):679-84.
• ¹² Scarpassa VM, Conn JE. Molecular differentiation in natural populations of Anopheles oswaldoi sensu lato (Diptera: Culicidae) from the Brazilian Amazon, using sequences of the COI gene from mitochondrial DNA. Genet Mol Res. 2006;5(3):493-502.
• ¹³ Ruiz F, Quiñones ML, Erazo HF, Calle DA, Alzate JF, Linton YM. Molecular differentiation of Anopheles (Nyssorhynchus) benarrochi and An (Nys) oswaldoi from Southern Colômbia. Mem Inst Oswaldo Cruz . 2005;100(2):155-60.
• ¹⁴ Schönhorst EO. Revisão de bibliografia sobre a larva da Dermatobia hominis: o berne. Hora Vet. 1988;7(41):47-50.
• ¹⁵ Klein TA, Lima JB, Tada MS. Comparative susceptibility of anopheline mosquitoes to Plasmodium falciparum in Rondonia, Brazil. Am J Trop Med Hyg. 1991;44(6):598-603.

• Financial support: This study was funded by Ministério da Ciência, Tecnologia, Inovações e Comunicações-(MCTIC)/INPA and by grants (process numbers 1501/2008) from the Amazonas Research Foundation [Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM)] to VMS.

Publication Dates

• Publication in this collection
  May-Jun 2017

History

• Received
  21 Oct 2016
• Accepted
  10 Feb 2017