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First report of myiasis caused by Cochliomyia hominivorax in free-ranging giant otter (Pteronura brasiliensis)

Primeiro relato de miíase causada por Cochliomyia hominivorax em ariranha (Pteronura brasiliensis) de vida livre

Nathalie Foerster Grazielle Soresini Fernando Paiva Fabiano Aguiar da Silva Caroline Leuchtenberger Guilherme Mourão About the authors

Abstract

Giant otters are territorial semi-aquatic mammals. It is common to find several individuals exhibiting wounds and scars due to intraspecific conflicts. Myiasis is a parasitic infestation on living tissues of vertebrates caused by dipterous larvae, that usually develops in freshly open wounds and can seriously threaten the host’s health. Ectoparasites seem to be rare among giant otters and myiasis had not been recorded in this species until now. Here, is presented one record of myiasis in a free-ranging giant otter found dead in the Pantanal, Brazil. An ulcerative lesion was found in the frontoparietal region, from which 22 larvae were recovered and identified as Cochliomyia hominivorax. The low occurrence of ectoparasites in giant otters might reflect their semi-aquatic habits and their grooming behavior, which makes it difficult for parasites to remain on the skin. The injured otter probably got the larvae after an intraspecific fight. Agonistic encounters between groups of giant otters have been reported before and these fights can result in serious wounds or even death. It was hypothesized that the myiasis caused by C. hominivorax deteriorated the health of the infested giant otter, which prevented recovery and accelerated its death.

Keywords:
Mustelid; ectoparasite; Lutrinae; Pantanal; neotropical wetland

Resumo

As ariranhas são mamíferos semiaquáticos habitantes do território brasileiro. É comum encontrar vários indivíduos apresentando feridas e cicatrizes devido a conflitos intraespecíficos. A miíase é uma infestação parasitária em tecidos vivos de vertebrados, causada por larvas de dípteros que, geralmente, se desenvolvem em feridas recém-abertas, podendo ameaçar seriamente a saúde do hospedeiro. Ectoparasitos parecem ser raros em ariranhas e, até o presente, não há relatos de miíase nesta espécie. Aqui, é apresentado um registro de miíase em uma ariranha de vida livre, encontrada morta no Pantanal, Brasil. Foi encontrada uma lesão ulcerativa na região frontoparietal, na qual foram recuperadas 22 larvas identificadas como Cochliomyia hominivorax. A baixa ocorrência de ectoparasitos em ariranhas pode refletir seus hábitos semiaquáticos e seu comportamento de limpeza, o que dificulta a permanência dos parasitos na pele. A ariranha ferida, provavelmente, se infestou com as larvas após uma briga intraespecífica. Encontros agonísticos entre grupos de ariranhas já foram relatados antes, e essas lutas podem resultar em ferimentos graves ou até mesmo em morte. Foi hipotetizado que a miíase causada por C. hominivorax deteriorou a saúde da ariranha infestada, o que impediu a recuperação e acelerou sua morte.

Palavras-chave:
Mustelídeo; ectoparasito; Lutríneos; Pantanal; áreas úmidas neotropicais

Introduction

Giant otters (Pteronura brasiliensis) are semi-aquatic mammals and the largest members of the family Mustelidae. They are social and territorial. Giant otters scent-mark and vocalize a wide repertoire to mark their territories and to avoid agonistic encounters with other groups (Leuchtenberger & Mourão, 2009Leuchtenberger C, Mourão G. Scent-marking of giant otter in the southern Pantanal, Brazil. Ethology 2009; 115(3): 210-216. http://dx.doi.org/10.1111/j.1439-0310.2008.01607.x.
http://dx.doi.org/10.1111/j.1439-0310.20...
). However, during the dry season their territories shrink, and the conflicts tend to increase (Ribas & Mourão, 2004Ribas C, Mourão G. Intraspecific agonism between giant otter groups. IUCN Otter Spec Group Bull 2004; 21(2): 89-93.; Leuchtenberger & Mourão, 2009Leuchtenberger C, Mourão G. Scent-marking of giant otter in the southern Pantanal, Brazil. Ethology 2009; 115(3): 210-216. http://dx.doi.org/10.1111/j.1439-0310.2008.01607.x.
http://dx.doi.org/10.1111/j.1439-0310.20...
), and it is common to find several individuals exhibiting wounds and scars (Rosas & Mattos, 2003Rosas FCW, Mattos GE. Natural deaths of giant otters (Pteronura Brasiliensis) in Balbina hydroelectric lake, Amazonas, Brazil. IUCN Otter Spec Group Bull 2003; 20(2): 62-64.).

Myiasis is a parasitic infestation on living or necrotic tissues of vertebrates caused by dipterous larvae (Hope, 1837Hope FW. On insects and their larvae occasionally found in the human body. Trans R Entomol Soc Lond 1837; 2: 256-271.; Zumpt, 1965Zumpt F. Myiasis in man and animals in the Old World: a textbook for physicians veterinarians, and zoologists. Michigan: Butterworth; 1965.). Myiasis can involve heavy infestation of freshly open wounds causing swelling, inflammation, pain, and thus seriously threat the host’s health (Hall, 1997Hall MJR. Traumatic myiasis of sheep in Europe: a review. Parassitologia 1997; 39(4): 409-413. PMid:9802103.; Yan et al., 2019Yan L, Zhang M, Tang LP, Ente M, Ma XP, Chu HJ, et al. First reports of nasal and traumatic myiasis infection in endangered Przewalski’s horses (Equus ferus przewalskii). Int J Parasitol Parasites Wildl 2019; 9: 21-24. http://dx.doi.org/10.1016/j.ijppaw.2019.03.018. PMid:30976513.
http://dx.doi.org/10.1016/j.ijppaw.2019....
). The North American river otter (Lontra canadensis) is susceptible to myiasis (Kimber & Kollias, 2000Kimber KR, Kollias GV 2nd. Infectious and parasitic diseases and contaminant-related problems of North American river otters (Lontra canadensis): a review. J Zoo Wildl Med 2000; 31(4): 452-472. http://dx.doi.org/10.1638/1042-7260(2000)031[0452:IAPDAC]2.0.CO;2. PMid:11428392.
http://dx.doi.org/10.1638/1042-7260(2000...
). However, it was unknown if the giant otter was susceptible to myiasis.

There are a few records of myiasis in free-ranging mammals in Brazil, including in maned wolf (Chrysocyon brachyurus) (Cansi et al., 2011Cansi ER, Bonorino R, Ataide HS, Pujol-Luz JR. Myiasis by screw worm Cochliomyia hominivorax (Coquerel) (Diptera: Calliphoridae) in a wild maned wolf Chrysocyon brachyurus (Mammalia: Canidae), in Brasilia, Brazil. Neotrop Entomol 2011; 40(1): 150-151. http://dx.doi.org/10.1590/S1519-566X2011000100025. PMid:21437499.
http://dx.doi.org/10.1590/S1519-566X2011...
), porcupine (Coendou prehensilis) (Lacey & George, 1981Lacey LA, George TK. Myiasis in an Amazonian porcupine. Entomol News 1981 [cited 2022 Oct 27]; 92(2): 79-80. Available from: https://biostor.org/reference/77199
https://biostor.org/reference/77199...
), opossum (Didelphis marsupialis) (Reis et al., 2008Reis FS, Barros MC, Fraga EC, Penha TA, Teixeira WC, Santos ACG, et al. Ectoparasitos de pequenos mamíferos silvestres de áreas adjacentes ao rio Itapecuru e área de preservação ambiental do Inhamum, estado do Maranhão, Brasil. Rev Bras Parasitol Vet 2008; 17(Suppl 1): 69-74. PMid:20059819.) and gracile mouse opossum (Gracilinanus sp.) (Reis et al., 2008Reis FS, Barros MC, Fraga EC, Penha TA, Teixeira WC, Santos ACG, et al. Ectoparasitos de pequenos mamíferos silvestres de áreas adjacentes ao rio Itapecuru e área de preservação ambiental do Inhamum, estado do Maranhão, Brasil. Rev Bras Parasitol Vet 2008; 17(Suppl 1): 69-74. PMid:20059819. ). Recently, May-Júnior et al. (2021)May-Junior JA, Fagundes-Moreira R, Souza VB, Almeida BA, Haberfeld MB, Sartorelo LR, et al. Dermatobiosis in Panthera onca: first description and multinomial logistic regression to estimate and predict parasitism in captured wild animals. Braz J Vet Parasitol 2021; 30(1): e023820. http://dx.doi.org/10.1590/s1984-29612021003. PMid:33787735.
http://dx.doi.org/10.1590/s1984-29612021...
captured 13 jaguars in the Pantanal presenting subcutaneous nodules due to parasitism by Dermatobia hominis larvae. In some of these jaguars, myiasis caused by Cochliomyia hominivorax was also found. In mustelids, only two records of myiasis infestation have been reported in Brazil. One occurred in a captive lesser grison (Galictis cuja) (Figueiredo et al., 2010Figueiredo MA, Santos ACG, Guerra RMSNC. Ectoparasitos de animais silvestres no Maranhão. Pesq Vet Bras 2010; 30(11): 988-990. http://dx.doi.org/10.1590/S0100-736X2010001100013.
http://dx.doi.org/10.1590/S0100-736X2010...
), and the other in a neotropical otter (Lontra longicaudis) that was rescued exhibiting health problems on the banks of a lake in southern Brazil (Michelazzo et al., 2022Michelazzo M, Martinelli T, Amorim V, Silva L, Silva FH, Xavier A, et al. Canine distemper virus and canine adenovirus type-2 infections in neotropical otters (Lontra longicaudis) from southern Brazil. Braz J Microbiol 2022; 53(1): 369-375. http://dx.doi.org/10.1007/s42770-021-00636-7. PMid:34709597.
http://dx.doi.org/10.1007/s42770-021-006...
). A report of myiasis in the North American river otter resulted in death three days after it was captured due to extensive damage caused by the dipteran larvae, which were not specifically identified (Serfass et al., 1993Serfass T, Peper R, Whary M, Brooks R. River otter (Lutra canadensis) reintroduction in Pennsylvania: prerelease care and clinical evaluation. J Zoo Wildl Med 1993; 24: 28-40.).

Here, is presented one record of myiasis caused by the larval stage of Cochliomyia hominivorax, in a free-ranging giant otter in the Pantanal, a large wetland located near the center of South America. To the author’s knowledge, this is the first report of myiasis in giant otters.

Methods

On the morning of September 4, 2021, a dead giant otter was found floating at the side of the Miranda River (19° 31' 13.95” S 57° 7' 12.96” W), in the state of Mato Grosso do Sul, Brazil. The animal was near the entrance of a former den. The carcass was collected and taken straight to a field lab (license SISBIO/ICMBio 79173-1). Judging from the fresh condition of the carcass, the time of death was estimated as only a few hours before the animal was found.

It was a young male, in poor body condition, measuring 116 cm in total length and weighing 18.77 kg. This individual had several injuries along its body, most of them probably due to bites and other wounds from a possible fight (Figure 1A and 1B). At the necropsy, it was observed that the animal no longer had any fat tissue remaining and the internal organs had normal macroscopic appearance. In a skin lesion measuring 8.5 x 6 cm, in the frontoparietal region with many cavitations on the edges, dipteran larvae were found. All the larvae were collected and stored in 70° GL ethyl alcohol for subsequent identification.

Figure 1
Carcass of a giant otter (Pteronura brasiliensis) found in the wild with myiasis lesion. A - General view of the animal; B - Details of the lesion, with third-instar larva; C - Third-instar larva of Cochliomyia hominivorax (Coquerel, 1858) recovered from skin; lateral view and ventral view (bar = 1 mm).

The larvae were cleaned with the aid of a brush and then were examined for their taxonomic characteristics by means of light microscopy, under a Leica M205 C™ stereomicroscope or a Leica DM5500 B™ microscope, both equipped with Leica cameras, models DFC 420 and 490, respectively (Leica Microsystems™, Wetzlar and Mannheim, Germany). Images were registered in the Leica Application Suite image analysis system (LAS™ 3.8; Leica Microsystems™, Wetzlar and Mannheim, Germany). Two specimens were randomly selected and passed through a clarification process, using a solution of potassium hydroxide (KOH) (10% w/v) (Zumpt, 1965Zumpt F. Myiasis in man and animals in the Old World: a textbook for physicians veterinarians, and zoologists. Michigan: Butterworth; 1965.), and were placed in an oven at 46°C until translucent (approximately five hours). The specimens were dehydrated in a progressive ethyl alcohol series, from 70 to 99° GL, at one-hour intervals between each dilution (70, 80, 90 and 99° GL). Then they were immersed in hexamethyldisilazane (cat. number 440191; Sigma-Aldrich™) for 10 minutes, followed by deposition onto carbon conductive tabs (12 mm OD, Pelco Tabs™; Ted Pella®, Inc., USA) attached to Pelco® Q pin stubs of dimensions 12.7 × 12.7 mm (Ted Pella®, Inc., USA). The images were documented using a Hitachi® model TM3000™ scanning electron microscope (Hitachi, Tokyo, Japan) in the analysis mode. The specimens were deposited in the Zoological Reference Collection of the Federal University of Mato Grosso do Sul (ZUFMS-DIP01276).

The taxonomic characteristics considered were those previously described by Laake et al. (1936)Laake EW, Cushing EC, Parish HE. Biology of the primary screw worm fly, Cochliomyia americana, and a comparison of its stages with those of C. macellaria. U S Dept Agr Tech Bui 1936 [cited 2022 Oct 27]; 500: 24. Available from: https://www.nal.usda.gov/exhibits/speccoll/items/show/7338
https://www.nal.usda.gov/exhibits/specco...
, Knipling (1939)Knipling EF. A key for blowfly larvae concerned in wound and cutaneous myiasis. Ann Entomol Soc Am 1939; 32(2): 376-383. http://dx.doi.org/10.1093/aesa/32.2.376.
http://dx.doi.org/10.1093/aesa/32.2.376...
, James (1947)James MT. The flies that cause myiasis in man. USDA Misc Pub 1947; 631: 175. http://dx.doi.org/10.5962/bhl.title.65688.
http://dx.doi.org/10.5962/bhl.title.6568...
, Zumpt (1965)Zumpt F. Myiasis in man and animals in the Old World: a textbook for physicians veterinarians, and zoologists. Michigan: Butterworth; 1965. and Shewell (1981)Shewell GE. Calliphoridae. In: McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockertoth JR, Wood DM, editors. Manual of Nearctic Diptera. Ottawa: Biosystematics Research Centre; 1981. p.1133-1145..

Results and Discussion

During the necropsy examination of the giant otter 22 live larvae were recovered. Macroscopically, the larvae were whitish, cylindrical, and tapered anteriorly, with 12 visible segments surrounded by band spines (Figure 1C). The lesion was characterized as typical primary ulcerative myiasis (Laake et al., 1936Laake EW, Cushing EC, Parish HE. Biology of the primary screw worm fly, Cochliomyia americana, and a comparison of its stages with those of C. macellaria. U S Dept Agr Tech Bui 1936 [cited 2022 Oct 27]; 500: 24. Available from: https://www.nal.usda.gov/exhibits/speccoll/items/show/7338
https://www.nal.usda.gov/exhibits/specco...
; Knipling, 1939Knipling EF. A key for blowfly larvae concerned in wound and cutaneous myiasis. Ann Entomol Soc Am 1939; 32(2): 376-383. http://dx.doi.org/10.1093/aesa/32.2.376.
http://dx.doi.org/10.1093/aesa/32.2.376...
; James, 1947James MT. The flies that cause myiasis in man. USDA Misc Pub 1947; 631: 175. http://dx.doi.org/10.5962/bhl.title.65688.
http://dx.doi.org/10.5962/bhl.title.6568...
).

All the larvae were in the third stage and were identified as Cochliomyia hominivorax (Coquerel, 1858). They showed the following characteristics: anterior portion armed with a pair of strong mouth hooks (Figure 2A and 2B); peritremes of posterior spiracle incomplete and not defined enclosing the button poorly; encircling three straight subparallel opening lined up diagonally (Figure 2C and 2D); cephalopharyngeal apparatus well developed and highly sclerotized, with conspicuous paired of mandibular hooks (Figure 3A and 3B); tracheal trunks lightly blackened, pigmented from the posterior spiracle (Figure 3C); dorsal region of the cornua not incised (Figure 3D); and anterior spiracle with short flattened stalk, with 10 nodular branches arranged fanwise (Figure 3E) (Knipling, 1939Knipling EF. A key for blowfly larvae concerned in wound and cutaneous myiasis. Ann Entomol Soc Am 1939; 32(2): 376-383. http://dx.doi.org/10.1093/aesa/32.2.376.
http://dx.doi.org/10.1093/aesa/32.2.376...
; James, 1947James MT. The flies that cause myiasis in man. USDA Misc Pub 1947; 631: 175. http://dx.doi.org/10.5962/bhl.title.65688.
http://dx.doi.org/10.5962/bhl.title.6568...
; Shewell, 1981Shewell GE. Calliphoridae. In: McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockertoth JR, Wood DM, editors. Manual of Nearctic Diptera. Ottawa: Biosystematics Research Centre; 1981. p.1133-1145.). The length of the larvae ranged from 10 to 15 mm.

Figure 2
Third-instar larva of Cochliomyia hominivorax (Coquerel, 1858) recovered from skin lesion in giant otter (Pteronura brasiliensis) in the Pantanal, Brazil. A and B - Details of the anterior portion; C and D - View of the posterior portion. Scale bars: A and C = 250 µm; B and D = 1 mm.
Figure 3
Third-instar larva of Cochliomyia hominivorax (Coquerel, 1858) recovered from skin lesion in giant otter (Pteronura brasiliensis) in the Pantanal, Brazil. A, B and C - specimen cleared with 10% solution of potassium hydroxide (KOH) (bar = 1 mm); A - Anterior portion in lateral view; B - Anterior portion in ventral view; C - Posterior portion in ventral view, highlighting the pigmentation of the tracheal trunks. D - Diagrammatic drawing of cephalopharyngeal apparatus in the lateral view (bar = 200 µm); and E - Diagrammatic drawing of anterior spiracle (bar = 250 µm).

Cochliomyia hominivorax, commonly known as the New World screwworm (NWS), is a dipteran species of the family Calliphoridae. The NWS is one of the main causes of myiasis in livestock, wildlife, and humans in tropical and subtropical parts of the Americas where it has not been eradicated, including Brazil (Wyss, 2000Wyss JH. Screwworm eradication in the americas. Ann N Y Acad Sci 2000; 916(1): 186-193. http://dx.doi.org/10.1111/j.1749-6632.2000.tb05289.x. PMid:11193620.
http://dx.doi.org/10.1111/j.1749-6632.20...
; Zumpt, 1965Zumpt F. Myiasis in man and animals in the Old World: a textbook for physicians veterinarians, and zoologists. Michigan: Butterworth; 1965.). Gravid adult female C. hominivorax lay their eggs in open wounds on the host. Upon hatching, the fly larvae, or maggots, also known as screwworms, feed on living dermal or subdermal tissues of the parasitized host (Knipling, 1939Knipling EF. A key for blowfly larvae concerned in wound and cutaneous myiasis. Ann Entomol Soc Am 1939; 32(2): 376-383. http://dx.doi.org/10.1093/aesa/32.2.376.
http://dx.doi.org/10.1093/aesa/32.2.376...
).

Myiasis is very rare in aquatic vertebrates, with only a few records in fish (Bristow et al., 1990Bristow GA, Berland B, Fosså SA. A first case of myiasis in fish. J Parasitol 1990; 76(2): 256-257. http://dx.doi.org/10.2307/3283026. PMid:2319427.
http://dx.doi.org/10.2307/3283026...
; Öktener & Alas, 2009Öktener A, Alaş A. Cases of external myiasis caused by Diptera (Sarcophaga sp.) on three cyprinid species. Rev Fish Sci 2009; 17(1): 68-69. http://dx.doi.org/10.1080/10641260802178818.
http://dx.doi.org/10.1080/10641260802178...
; Zumpt, 1965Zumpt F. Myiasis in man and animals in the Old World: a textbook for physicians veterinarians, and zoologists. Michigan: Butterworth; 1965.). The low occurrence of ectoparasites in giant otters, especially dipterans, might reflect their semi-aquatic habits, but also their grooming and allogrooming behavior, which makes it difficult for parasites to remain on the skin.

The NSW cannot develop in carrion; it feeds only on living tissues. The time taken for the larvae to reach the third stage is 5 to 7 days (Hall, 1997Hall MJR. Traumatic myiasis of sheep in Europe: a review. Parassitologia 1997; 39(4): 409-413. PMid:9802103.). Thus, the otter probably acquired the NSW after being injured either by an accident or even intraspecific fights. Agonistic encounters between groups of giant otters have been reported before (Ribas & Mourão, 2004Ribas C, Mourão G. Intraspecific agonism between giant otter groups. IUCN Otter Spec Group Bull 2004; 21(2): 89-93.). These fights can result in serious wounds or even death (Rosas & Mattos, 2003Rosas FCW, Mattos GE. Natural deaths of giant otters (Pteronura Brasiliensis) in Balbina hydroelectric lake, Amazonas, Brazil. IUCN Otter Spec Group Bull 2003; 20(2): 62-64.; Leuchtenberger et al., 2015Leuchtenberger C, Magnusson WE, Mourão G. Territoriality of giant otter groups in an area with seasonal flooding. PLoS One 2015; 10(5): e0126073. http://dx.doi.org/10.1371/journal.pone.0126073. PMid:25955248.
http://dx.doi.org/10.1371/journal.pone.0...
), even though many individuals can show rapid recovery from injuries in the wild (Foerster, person. obs.). It was hypothesized that the myiasis caused by C. hominivorax deteriorated the health of the infested giant otter, which prevented recovery and accelerated its death.

The NSW is very important in economic terms where endemic, since it infests cattle and other livestock species (Vargans-Terán, 2020). In Brazil, the economic loss caused by NWS infestation on the livestock industry was estimated to be USD 380 million annually (Grisi et al., 2014Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, et al. Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 2014; 23(2): 150-156. http://dx.doi.org/10.1590/S1984-29612014042. PMid:25054492.
http://dx.doi.org/10.1590/S1984-29612014...
). Although information regarding its impact on wildlife populations is scant, Vargas-Terán (1991)Vargas-Terán M. The New World screwworm in Mexico and Central America. World Anim Rev 1991 [cited 2022 Oct 27]. Available from: https://www.fao.org/3/u4220t/u4220t0d.htm
https://www.fao.org/3/u4220t/u4220t0d.ht...
reported an 80% loss among fawns of the white-tailed deer (Odocoileus virginianus) in Texas, in the United States, duet to NSW infestation.

The records of myiasis in endangered species such as jaguars (May-Junior, 2021), giant otters reported herein, and invasive vertebrate species like feral hogs (Altuna et al., 2021Altuna M, Hickner PV, Castro G, Mirazo S, Pérez de León AA, Arp AP. New World screwworm (Cochliomyia hominivorax) myiasis in feral swine of Uruguay: one Health and transboundary disease implications. Parasit Vectors 2021; 14(1): 26. http://dx.doi.org/10.1186/s13071-020-04499-z. PMid:33413607.
http://dx.doi.org/10.1186/s13071-020-044...
), demonstrate the importance of studies on the impact of these parasites on wildlife.

Acknowledgements

The authors are very grateful to all the employees of the Pantanal Study Base of the Federal University of Mato Grosso do Sul for the support during the field work and necropsy. The study was funded by Fundação de Ciência e Tecnologia do Estado de Mato Grosso do Sul (Fundect/CNPq grant PRONEX 006/2015) and by Houston Zoo. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided a scholarship to NF (88887.311430/2018-00) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) awarded a productivity fellowship to GM (308934/2017-2).

  • How to cite: Foerster N, Soresini G, Paiva F, Silva FA, Leuchtenberger C, Mourão G. First report of myiasis caused by Cochliomyia hominivorax in free-ranging giant otter (Pteronura brasiliensis). Braz J Vet Parasitol 2022; 31(4): e009522. https://doi.org/10.1590/S1984-29612022058

References

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    » http://dx.doi.org/10.1186/s13071-020-04499-z
  • Bristow GA, Berland B, Fosså SA. A first case of myiasis in fish. J Parasitol 1990; 76(2): 256-257. http://dx.doi.org/10.2307/3283026 PMid:2319427.
    » http://dx.doi.org/10.2307/3283026
  • Cansi ER, Bonorino R, Ataide HS, Pujol-Luz JR. Myiasis by screw worm Cochliomyia hominivorax (Coquerel) (Diptera: Calliphoridae) in a wild maned wolf Chrysocyon brachyurus (Mammalia: Canidae), in Brasilia, Brazil. Neotrop Entomol 2011; 40(1): 150-151. http://dx.doi.org/10.1590/S1519-566X2011000100025 PMid:21437499.
    » http://dx.doi.org/10.1590/S1519-566X2011000100025
  • Figueiredo MA, Santos ACG, Guerra RMSNC. Ectoparasitos de animais silvestres no Maranhão. Pesq Vet Bras 2010; 30(11): 988-990. http://dx.doi.org/10.1590/S0100-736X2010001100013
    » http://dx.doi.org/10.1590/S0100-736X2010001100013
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    » http://dx.doi.org/10.1590/S1984-29612014042
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  • Kimber KR, Kollias GV 2nd. Infectious and parasitic diseases and contaminant-related problems of North American river otters (Lontra canadensis): a review. J Zoo Wildl Med 2000; 31(4): 452-472. http://dx.doi.org/10.1638/1042-7260(2000)031[0452:IAPDAC]2.0.CO;2 PMid:11428392.
    » http://dx.doi.org/10.1638/1042-7260(2000)031[0452:IAPDAC]2.0.CO;2
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Publication Dates

  • Publication in this collection
    21 Nov 2022
  • Date of issue
    2022

History

  • Received
    07 July 2022
  • Accepted
    26 Oct 2022
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