Taxonomía y sistemática

 

Parasitism of Cuterebra sp. (Diptera: Oestridae s.l.) on rodents of Central Panama

 

Parasitismo de Cuterebra sp. (Diptera: Oestridae s.l.) en roedores de Panamá Central

 

Sergio E. Bermúdez C.^{1 *}, Publio González², Mario Ávila^{2, 3}, Roberto Miranda¹, Aníbal Armién⁴ and Blas Armién^{2, 5}

 

¹ Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado postal 0816–02593, Panamá, Panamá.

² Proyecto Hantavirus, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado postal 0816–02593, Panamá, Panamá.

³ Departamento de Control de Vectores, Ministerio de Salud.

⁴ Department of Veterinary Medicine, Gortner Ave., St. Paul, University of Minnesota. 55108 USA.

⁵ Genómica y Proteómica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado postal 0816–02593, Panamá, Panamá.

 

^*Correspondent:
bermudezsec@gmail.com; sbermudez@gorgas.gob.pa

 

Recibido: 06 febrero 2009
Aceptado: 07 agosto 2009

 

Abstract

In this study, which we carried out between January 2007 and July 2008 on populations of 3 species of wild mammals in Tonosí, Los Santos province, Panama, we report the presence of larvae of Cuterebra sp. parasitizing Zygodontomys brevicauda, Liomys adspersus, and Oligoryzomys fulvescens; the prevalence values recorded in these rodent species were 1.77, 2.15, and 1.17, respectively. This is the first record of Cuterebra sp. as parasite of rodents in Panama, and L. adspersus represents a new host record.

Key words: myiasis, Cuterebra, rodents, Panama.

 

Resumen

Entre enero 2007 y julio 2008 se desarrolló una investigación en las poblaciones de roedores silvestres de la localidad de Tonosí (Los Santos, Panamá central), encontrándose larvas de Cuterebra spp. parasitando a los roedores Zygodontomys brevicauda, Liomys adspersus y Oligoryzomys fulvescens, con una prevalencia de 1.77%, 2.15% y 1.71%, respectivamente. Este es el primer reporte de Cuterebra sp., parasitando roedores en Panamá, y el primero en presentar a L. adspersus como hospedero.

Palabras clave: miasis, Cuterebra, roedores, Panamá.

 

Introduction

The genus Cuterebra s.s. includes obligate dermal parasites of New World mammals, especially lagomorphs and rodents (Wood, 1987; Pape 2001), as well as raccoons (Slansky and Huckabee, 2006), cats (Slansky, 2007), and humans (Cornet et al. 2003; Plotinsky, et al. 2007). According to Catts (1982) and Wood (1987), this genus comprises 60 species, which mainly have been studied in the Nearctic.

As in other species of Oestridae, myiasis is very complicated; females do not directly oviposit eggs onto the hosts. Instead, the females place the eggs on grass, shrubs, stones or soil near rodent burrows. These eggs then become attached to the rodents when they walk over the sites (Catts, 1982; Baird, 1997). Hatching is stimulated by body heat and enter the host through openings (mouth, nose, eyes or anus) (Hunter and Webster, 1973; Gringrich, 1981; Catts, 1982; Slansky, 2006). When the maggots complete their development in the host, the larvae exit through the skin and continue the pupal stage in the soil (Catts, 1982; Wood, 1987).

In the Neotropics, there is little known about Cuterebra species, specifically about their principal host or their impact on rodent population dynamics. The aim of this work is to provide more information on the behavior and host for this genus in Panama.

 

Materials and methods

This study was carried out in January 2007 and July 2008, as part of field activities of a project dealing with hantavirus in several sites in Central Panama. We selected 6 sample sites in Tonosí County (Los Santos Province, Panama) (Fig. 1). These sites contained various seasonal crops (rice, corn, Cucurbitaceae), as well as secondary forest, pastures, stubble fields, and nearby towns. Samples were taken monthly in 4 day periods, using 600 Sherman traps and bait of corn, rice, sorghum, honey and peanut butter. Traps were placed in lines of 10, each one separated by 10 meters; collecting sites included towns, fields and forest.

Traps were placed between 15:00 hrs. to 07:00 hrs. Identification of captured rodents followed Reid (1997), and reproductive age was determined. Larvae were extracted and placed in containers of 75% alcohol. In addition, 3 bots from Z. brevicauda were bred in the laboratory. These bots were placed in a terrarium (15 cm wide × 22 cm large and 18 cm high) with soil. The warble and the fly were identified with the key of Wood (1987).

 

Results

A total of 2 699 rodents were caught, representing 5 species and 2 families (Muridae and Heteromyidae). Zygodontomys brevicauda was the most abundant species with 2 084 individuals (77.2% of total). We recovered 48 bots that infested 43 rodents. Only 3 species of rodents were infested by Cuterebra sp: Z. brevicauda, Oligoryzomys fulvescens and Liomys aspersus, with a prevalence of 1.77%, 1.71% and 2.15%, respectively (Table 1). In addition, 97% of the infested rodents were parasitized with 1 larva, usually in the neck, scapular area, lower abdomen or hind legs. No warbles were found on Sigmodon hispidus and Oryzomys concolor.

Fifty–eight percent of the parasitized rodents were males. All infested rodents were captured during the rainy season (May–December). One of the 3 bred larvae completed its development after 24 days in the pupal stage.

 

Discussion

Specimens collected in this study were similar to C. austeni; nevertheless, to the best of our knowledge there are no keys for identifying adults or larvae of Neotropical Cuterebra, and we prefer do not assign it to species.

We report infestations of Cuterebra on 3 species of rodents and the first record of L. adspersus as host of a Cuterebra warble. It is possible that L. adspersus also acts as a natural host for botflies. However, there is no evidence of this due to the limited research on rodents in Panama and to the restricted distribution of this rodent (Gonzalez et al., 2004). Other Liomys species (L. irroratus) has been reported as a host of Cuterebra fontinella in United States (Parker and Chaney, 1979). With regard to Z. brevicauda, previous reports implicate Cuterebra apicalis as parasitizing this species in Trinidad (Everad and Aitken, 1972).

The low prevalence of parasitism in the rodents studied is consistent with previous studies. In a study conducted in New Mexico, Wilson et al. (1997) found 3.1% C. austeni parasitism on Peromyscus truei and 1% on P. leucopus, while Bowman (2000) determined a 2.3% of infestation on P. maniculatus and 5.4% on Clethirionomys gapperi in Canada.

Although the climate and species of flies and hosts in the Neotropics are very different from those in the Nearctic, levels of parasitism are similar. Low levels have been reported by Disney (1969) in Belize (1.4% of C. chiquibulensis in Ototylomys phyllotis and 2.1% of C. flaviventris in Sigmodon hispidus), by Manrique–Saide et al. (2000) in southern Mexico (13.1% for Cuterebra sp. in O. phyllotis), and recently by Adler et al. (2003) in Panama (4.6% for Cuterebra sp infesting Proechymis semispinosus).

In contrast, studies on populations of P. leucopus from Tennessee and Kentucky islands reported high levels of infestations varying from 0–82% (Kollar, 1995). Likewise, in South America, Brigada et al. (1992) reported prevalences of 2.8–25% in Akodon molinae infested by Rogenhofera bonaerensis, while Vieira (1993), determined values of 11% for this fly in Thalpomys cerradensis and Bolomys lastrurus, and 7% in Oryzomys subflavus by Metacuterebra (=Cuterebra) apicalis from Brazil. Mid–level infestation (25.7%) was found in Oryzomys russatus caused by Metacuterebra (=Cuterebra) apicalis from Brazil (Bergallo et al., 2000).

Previous records suggest an evolutionary tension between fly population levels and the impact on host populations. The number of parasitized rodents increased relative to the number of captures (and vice versa); this could suggest that the response of flies is density depended on the host population. Nevertheless, more studies are necessary to conclude this point. On the other hand, even though the larvae can kill some rodents, the effect on the population is low because of the low level of prevalence and mortality. This is best understood by considering that the bots need live animals for their development, at least until the end of their third stage (Wood, 1987; Slansky, 2007).

Information about the effects of parasites on rodents is scarce; nevertheless, rodent mortality attributed to botflies is not very common (Catts, 1982; Wood, 1987). Death occurs due to tissue and muscle damage, especially in young animals. Botflies can also cause behavioral effects; diminished mobility increases starvation and the ability to obtain food. Smith (1978), who found traces of Cuterebra tissues in owl pellets and fox scats, explained that there are various behavioral implications associated with this phenomenon.

The highest number of parasitized rodents captured occurred during the wet season, in contrast to Adler et al. (2003), who captured parasitized rodents throughout the whole year, but with increases during the dry season. Such differences could be attributed to the anthropogenic influences observed in our sampling sites, where agricultural activities associated with rain determine the increase of resources, which promote a rise in the rodent population, and consequently, in the Cuterebra population. However, the lack of information about the duration of each stage, preclude establishing the recruitment period, and we cannot determine if infestation was during the last weeks of the dry season or during the beginning of wet season.

 

Acknowledgments

We are grateful for the support of the Ministry of Health (MINSA), Gorgas Memorial Institute of Studies for Health and National Environment Authority (ANAM). To the Financial support in the International Centers for Infectious Diseases Research, number U–19–AI 45452. A large number of individuals from the communities and several state organization provided support during fieldwork. We thank the rodent ecology team of MINSA and Hantavirus Project and especially to Sr. Daniel Gonzalez, Ricardo Rodriguez, Miguel Vergara, Santiago Bosch, Carlos Falconett, Augusto Robles, José Montenegro and Juan Navarro. Additionally, we thanks to Maria Zambrano and R. Philip Scheibel for the corrections in English, and Thomas Pape and Frank Slansky to provide papers.

 

Literature cited

Adler, G., D. Shannon and A. Carvajal. 2003. Bots (Diptera: Oestridae) infesting a Neotropical forest rodents Proechimys semispinosus (Rodentia: Echimyidae) in Panama. Journal of Parasitology 89:693–697.        [ Links ]

Baird, C. 1997. Bionomics of Cuterebra austeni (Diptera: Cuterebridae) and its association with Neotoma albigula (Rodentia: Cricetidae) in the southwestern United States. Journal of Medical Entomology 34:690–95        [ Links ]

Bergallo, H., F. Martins–Hatano, J. Juca and D. Gettinger D. 2000. The effect if botfly parasitism of Metacuterebra apicalis (Diptera) on reproduction, survival and general health of Oryzomys russatus (Rodentia) in southeastern Brazil. Mammalia 64:439–446.        [ Links ]

Brigada, A., E. Tripole and A. Zuleta. 1992. Cuterebrid parasitism (Rogenhofera bonaerensis) on the shrub land mouse (Akodon molinae), in Argentina. Journal of Wildlife Diseases 28:646–650.        [ Links ]

Bowman, J. 2000. Forest components associated with parasitism of small mammals by botflies (Cuterebra). Mammalia 64:243–247.        [ Links ]

Catts, E. 1982. Biology of NewWorld bot flies: Cuterebridae. Annual Review Entomology 27:313–38.        [ Links ]

Cornet, M; M. Florent, A. Lefebvre, C. Wertheimer, C. Perez–Eid, M. Bangs and A. Bouvet. 2003. Tracheopulmonary myiais caused by mature third–instar Cuterebra larva: case report and review. Journal Clinical of Microbiology 41:5810–5812.        [ Links ]

Disney, H. 1969. Notes on rodent warble–flies from British Honduras including the description of a new species of Cuterebra Clark (Dipt., Cuterebridae). Entomologist's Monthly Magazine 104:189–197.        [ Links ]

Everard, C. and T. Aitken. 1972. Cuterebrid flies from small mammals in Trinidad. Journal of Parasitology 58:189–190.        [ Links ]

Gingrich, R. 1981. Migratory kinetics of Cuterebra fontinella (Diptera: Cuterebridae) in the white–footed mouse, Peromyscus leucopus. Journal of Parasitology 67:398–402.        [ Links ]

González, M, B. Armien, A. Armien and J. Salazar–Bravo. 2004. Liomys adspersus. Mammalian Species 159:1–3.        [ Links ]

Hunter, D. and J. Webster. 1973. Determination of the migratory route of botfly larvae, Cuterebra grisea (Diptera: Cuterebridae) in deermice. International Journal of Parasitology 3:311–16.        [ Links ]

Kollar, T. 1995. Factors affecting distribution of Botflies (Diptera: Oestroidea) on islands in Lake Barkley, Kentucky and Tennessee. Journal of Entomology Science 30:513–518.        [ Links ]

Manrique–Saide, P., S. Hernández–Bethancourt and M. Quintero. 2000. First record of Cuterebra sp. (Diptera: Cuterebridae) infection in Ototylomys phyllotis (Rodentia: Muridae). Florida Entomology 83:487–488.        [ Links ]

Pape T. 2001. Phylogeny of Oestridae (Insecta: Diptera). Systematic Entomology 26:133–171.        [ Links ]

Parker, O. and A. Chaney. 1979. Liomys irroratus (Rodentia: Heteromyiidae), a new host for Cuterebra fontinella (Diptera: Cuterebridae). Journal of Medical Entomology 15:573.        [ Links ]

Plotinsky, R., E. Talbot and H. Davis. 2007. Cuterebra cutaneous myiasis, New Hampshire, 2004. American Journal of Tropical Medicine and Hygiene 76:596–597.        [ Links ]

Reid, F. 1997. A field guide to the Mammals of Central America and Southeast Mexico. Oxford University Press, London. 334 p.        [ Links ]

Slansky, F. 2006. Cuterebra Bot fly (Diptera: Oestroidea) and their host indigenous host and potential host in Florida. Florida Entomology 89:152–150        [ Links ]

Slansky, F. 2007. Insect/Mammal associations: effects of Cuterebrid Bot fly parasites on their host. Annual Review Entomology 52:17–36.        [ Links ]

Slansky, F. and J. Huckabee. 2006. First records of rodents–infesting Cuterebra bot flies parasitizing raccoons (Procyon lotor) in North America. Journal of Parasitology 92:1364–1373.        [ Links ]

Smith, D. 1978. Vulnerability of bot fly (Cuterebra) infected Peromyscus maniculatus to shorttail weasel predation in the laboratory. Journal of Wildlife Diseases 14:40–51        [ Links ]

Vieira, E. 1993. Occurrence and prevalence of Botflies, Metacuterebra apicalis (Diptera: Cuterebridae) in Rodents of Cerrado from Central Brazil. Journal of Parasitology 79:792–795.        [ Links ]

Wilson, W, J. Hnida and D. Duszynski. 1997. Parasites of mammals on the Sevilleta National Refuge, Socorro, New Mexico: Cuterebra austeni and C. neomexicana (Diptera: Oestridae) from Neotoma and Peromyscus (Rodentia: Muridae), 1991–1994. Journal of Medical Entomology 34:359–367.        [ Links ]

Wood, D. M. 1987. Oestridae. In Manual of Nearctic Diptera. Vol .2, J. F. McAlpine (edit.). Ottawa. p. 1147–1158.        [ Links ]