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Revista mexicana de ciencias forestales
versión impresa ISSN 2007-1132
Rev. mex. de cienc. forestales vol.14 no.79 México sep./oct. 2023 Epub 06-Oct-2023
https://doi.org/10.29298/rmcf.v14i79.1362
Research note
First record of Cuterebra sp. (Diptera: Oestridae) in rodents (Rodentia: Cricetidae) in Northeastern Mexico
1
*
http://orcid.org/0000-0002-9782-1803
1
http://orcid.org/0000-0002-9298-0645
1Universidad Autónoma de Nuevo León, Facultad de Ciencias Forestales. México.
The Cuterebra genus (Diptera: Oestridae) includes species of dermic parasites infecting wild rodents and lagomorphs. In Mexico, 14 species of this parasite have been recorded and most of the reports of this interaction are from southern Mexico. This study describes the first record of Cuterebra sp. parasitizing three rodent species from Tamaulipan Thorny Scrub (TTS) in northeastern Mexico. From March to October 2020 and March to September 2021, rodents were captured within a preserved TTS fragment in Linares municipality, Nuevo Leon. Four rodent species were recorded: Heteromys irroratus, Onychomys leucogaster, Neotoma albigula and Peromyscus leucopus. Infected individuals were detected exclusively in the last three species. One male of O. leucogaster was captured with one Cuterebra sp. larva in the genital area, while from 12 N. albigula individuals were captured, only one adult female presented a larva in the pectoral region. From 86 captured individuals of P. leucopus, 15 were infected: five females (four adults and one juvenile) and 10 males (seven adults and three juveniles). The highest number of infected individuals was detected in October: four individuals of P. leucopus and one O. leucogaster. Although they are usually specific in their interaction, these parasites can also affect the natural predators of their hosts, domestic animals (cattle or pets) and humans. These new records provide relevant information on parasite-rodent interactions and their incidence and distribution in Mexico.
Key words: Host; myiasis; botfly; Nuevo León; parasitism; rodents
El género Cuterebra (Diptera: Oestridae) incluye especies de parásitos dérmicos que infectan a roedores y lagomorfos silvestres. En México, se han registrado 14 especies de dicho parásito y la mayoría de los datos de esta interacción provienen del sur del país. El presente estudio describe el primer registro de Cuterebra sp. en tres especies de roedores del Matorral Espinoso Tamaulipeco (MET) en el noreste de México. De marzo a octubre de 2020 y de marzo a septiembre de 2021 se capturaron roedores dentro de un fragmento conservado de MET en Linares, Nuevo León. Se identificaron cuatro especies de roedores: Heteromys irroratus, Onychomys leucogaster, Neotoma albigula y Peromyscus leucopus. Exclusivamente en las tres últimas especies se detectaron individuos infectados. Se capturó un macho adulto de O. leucogaster con una larva de Cuterebra sp. en el área genital, mientras que de 12 individuos de N. albigula, solo una hembra adulta presentó una larva en la región pectoral. Se capturaron 86 individuos de P. leucopus de los cuales 15 resultaron infectados (17.44 %): cinco hembras (cuatro adultas y una juvenil) y 10 machos (siete adultos y tres juveniles). En octubre se detectó el mayor número de individuos infectados: cuatro de P. leucopus y uno de O. leucogaster. Aunque suelen ser específicos en su interacción, estos parásitos pueden también afectar a los depredadores naturales de sus hospederos, a los animales domésticos (ganado o animales de compañía) y al humano. Estos nuevos registros brindan información relevante sobre las interacciones parásito-roedor y su distribución en México.
Palabras clave Hospedero; miasis; moscardón; Nuevo León; parasitismo; roedores
Parasitic interactions known as myiasis occur between living vertebrates and the larval stages of some dipteran species (Francesconi and Lupi, 2012; Páez and Villa, 2017; Salazar-Saavedra and Medina-Fitoria, 2021, Kaufman and Wood, 2015). These larvae can feed on live or dead tissue of the host, which causes an injury in the affected area (Colwell et al., 2006; Francesconi and Lupi, 2012; Orduña-Sumarán et al., 2022).
Botfly larvae (Diptera: Oestridae) are parasites of the skin tissue of wild vertebrates that cause myiasis in their hosts (Colwell et al., 2006; Lara-Lagunes et al., 2017; Orduña-Sumarán et al., 2022). Within this family is the Cuterebra genus, which includes species of skin parasites in mammals from the New World. They infect mainly wild rodents and lagomorphs (Manrique-Saide et al., 2000; Slansky et al., 2008). This genus has been recorded infecting species of six genera of rodents (Sabrosky, 1986) and 14 species of this parasite have been found in Mexico (Guimarães and Papavero, 2009).
Studies on myiasis by Cuterebra species in Mexico include the group of rodents in the states of Yucatán (Manrique-Saide et al., 2000) and Baja California Sur (Arnaud et al., 2016), in some lagomorphs from Puebla (Ramírez and Hernández-Ortiz, 2016) and Sonora (Orduña-Sumarán et al., 2022), a species of primate (Cristobal-Askarate et al., 2012) and a canid (Lara-Lagunes et al., 2017) described in Veracruz. This indicates the lack of publications on this parasite-host interaction to know and understand the causes and effects of the presence and incidence of these parasitic infections at national level.
From March to October 2020 and March to September 2021, the rodent community of a preserved fragment of Tamaulipan Thorny Scrub (TTS) (24°47'50" N and -99°32'19" W) was studied monthly. The fragment is part of the "Efraím Hernández Xolocotzi" Botanical Garden, which is registered as a Management Unit for the Conservation of Wildlife (PVSNL-UMA-IN-1270-NL) that belongs to the Facultad de Ciencias Forestales of the Universidad Autónoma de Nuevo León (UANL), Linares municipality, Nuevo León State, Mexico. The study area has an altitude of 350 m (Estrada and Marroquín, 1988), a warm sub-humid climate with rains present in summer (García, 2004) and an average annual rainfall of 805 mm (Martínez-Adriano et al., 2021). The annual average temperature is 21 °C, with an extreme maximum temperature in summer greater than 40 °C and less than 0 °C in winter (Martínez-Adriano et al., 2021).
The rodents were captured with 87 Sherman-type traps (23×8×9 cm), baited with a mixture of sunflower seeds and oats, which were placed at an equidistance of 10 m. From the captures of the rodents and their processing and release in situ, some rodents infected with Cuterebra sp. larvae were detected by direct observation. All parasitized individuals presented a single larva, the location of the infection was recorded, and some specimens were extracted (in situ) directly from the hole caused by the parasite by means of dissecting forceps, which were preserved in round-bottom microtubes model 111568 Globe Scientific® with 70% alcohol. The taxonomic identification of the rodents was carried out by field guides and taxonomic keys (Jiménez-Guzmán et al., 1999; Álvarez-Castañeda et al., 2015), and in the case of the larvae, they were identified with specialized literature at the time they were extracted in the field and their subsequent corroboration in the laboratory (Stojanovich et al., 1966; Lara-Lagunes et al., 2022).
Four species of rodents were recorded: Heteromys irroratus (J. E. Gray, 1868) (family Heteromyidae), Peromyscus leucopus (Rafinesque, 1818), Neotoma albigula (Hartley, 1894), and Onychomys leucogaster (Wied-Neuwied, 1841), (family Cricetidae); parasitized individuals were found exclusively in the last three species. Eighty-six specimens of P. leucopus were captured, of which 15 were infected (17.44 %): five were females (four adults and one juvenile) and 10 males (seven adults and three juvenile) (Figure 1A and 1B).
A) Infected population by sex; B) Population classified by age between males (M) and females (H); Hembras = Females; Machos = Males; H adultos = Adults females; M adultos = Adults males; H juveniles = Juvenile females; M juveniles = Juvenile males.
Figure 1 Incidence of infection of Cuterebra sp. in Peromyscus leucopus (Rafinesque, 1818).
Most of the larvae found in P. leucopus were located in the genital area (Figure 2A). Of 12 N. albigula individuals captured, an adult female presented a larva in the pectoral region (8.3 %, Figure 2B). Only one adult male of O. leucogaster with a larva in the genital area was recorded (100 % incidence of infection, Figure 2C). A total of seven larvae were extracted, which were labeled with the date and the individual of the host mouse and deposited in the Wildlife Laboratory of the Facultad de Ciencias Forestales of the UANL (Figure 3A).
A) Peromyscus leucopus (Rafinesque, 1818) with a larva in the genital region; B) Neotoma albigula (Hartley, 1894) with a larva in the pectoral zone; C) Onychomys leucogaster (Wied-Neuwied, 1841) with a larva in a testicle.
Figure 2 Infection by Cuterebra sp. in three species of rodents from the Tamaulipan Thorny Scrub.
A) Larva of Cuterebra sp. extracted from a male Peromyscus leucopus (Rafinesque, 1818); B) Incidence of infection by Cuterebra sp. (numbers in parentheses) in the three species parasitized during the sampling months of 2020. The numbers within the bars represent infected and uninfected individuals.
Figure 3 Presence of Cuterebra sp. in three species of wild rodents.
The largest number of rodents with myiasis occurred in October: four individuals of P. leucopus and one of O. leucogaster (Figure 3B). A reinfection was recorded in a P. leucopus adult male and it was observed that the incidence of infection was common in this species, since infected examples were obtained in most of sampled months of the year 2020 (Figure 3B). It should be noted that in 2021, only in March and April parasitized rodents were found, which corresponded to P. leucopus, which were four adult males, one juvenile female and one adult.
This study describes the first records of Cuterebra sp. parasitizing TTS rodents in northeastern Mexico. Likewise, the first findings of this interaction in P. leucopus, N. albigula and O. leucogaster in Mexico are referred and it is the third work that documents myiasis in mammals from the northern region of the country (Arnaud et al., 2016; Orduña-Sumarán et al., 2022).
From the direct observations of the infected mice, it was highlighted that the areas with highest predisposition to infection were the lower abdomen and hind limbs, which is consistent with what was observed for other rodent species in Mexico and Panama (Manrique-Saide et al., 2000; Bermúdez et al., 2010).
Most of the individuals infected with P. leucopus were adults, which is consistent with the prevalence observed by Jaffe et al. (2005), who also emphasize that in Peromyscus maniculatus (Wagner, 1845) the prevalence is similar between juvenile and adults.
Derived from the scarcity of works on parasite-host interactions in Mexico (Lara-Lagunes et al., 2022), there is a need to carry out more research on the presence of Cuterebra sp. in other species of the country, both wild and domestic, to know the impact of this parasite on the affected species. Because these parasites, although they tend to be specific in their interaction (Ramírez and Hernández-Ortiz, 2016), can also parasitize the natural predators of their hosts (Lara-Lagunes et al., 2017), domestic animals (livestock or pets), and humans (Colwell et al., 2006; Slansky et al., 2008; Orduña-Sumarán et al., 2022). These new records provide relevant information on the distribution and importance of parasite-rodent interactions in Mexico.
Acknowledgements
The first author thanks the PRODEP program of the Secretaría de Educación Pública for the support of the scholarship 511-6/2019-15979 granted to carry out a postdoctoral stay and the Consejo Nacional de Humanidades, Ciencias y Tecnologías (Conahcyt) for the scholarship 2708258 granted to carry out an academic postdoctoral stay. To the Support Program for Scientific and Technological Research (PAICYT) (project 32-CAT-2022) for the funding granted. To Dr. César Martín Cantú Ayala for the facilities granted to make use of the facilities of the "Efraím Hernández Xolocotzi" Botanical Garden of Facultad de Ciencias Forestales of the Universidad Autónoma de Nuevo León.
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Received: March 16, 2023; Accepted: June 22, 2023
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