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Litomosoides brasiliensis (Nematoda: Onchocercidae) infecting chiropterans in the Legal Amazon region, Brazil

Litomosoides brasiliensis (Nematoda: Onchocercidae) em morcegos na Amazônia Legal, Brasil

Abstract

Chiropterans play an important role in the maintenance of the environmental balance, since they are pollinators, seed dispersers and predators. They contribute to transmission and spreading of microorganisms such as helminths, fungi, protozoa, bacteria and virus. The aim of the present study was to investigate natural filariid infection among bats in the Legal Amazon region, Brazil, by means of parasitological and molecular analyses. Blood samples were collected from 82 bats for blood smears and for DNA extraction via the polymerase chain reaction (PCR) assay. Microfilariae were observed in blood smears from Carollia perspicillata (2), Artibeus lituratus (1), Artibeus fimbriatus (2), Dermanura gnoma (2) and Glossophaga soricina (1). Five positive samples were detected through the PCR assay and four of these were also positive in blood smears. From genome sequencing and comparative analysis with sequences deposited in GenBank, one sample showed 99.31% similarity to the species Litomosoides brasiliensis. The present study expands the geographical distribution of L. brasiliensis, to include the state of Maranhão as an area of occurrence of this species and includes D. gnoma and A. fimbriatus as hosts in Brazil.

Keywords:
Nematoda; bats; filariids; Brazil

Resumo

Os quirópteros desempenham um papel importante na manutenção do equilíbrio ambiental, pois são polinizadores, dispersores de sementes e predadores. Contribuem para a transmissão e disseminação de microrganismos, como helmintos, fungos, protozoários, bactérias e vírus. O objetivo do presente estudo foi investigar a infecção natural por filariídeos em morcegos na região da Amazônia Legal, Brasil, por meio de análises parasitológicas e moleculares. Amostras de sangue foram coletadas de 82 morcegos para confecção de esfregaços e para extração de DNA para a Reação em Cadeia da Polimerase (PCR). Microfilárias foram observadas em esfregaços sanguíneos de Carollia perspicillata (2), Artibeus lituratus (1), Artibeus fimbriatus (2), Dermanura gnoma (2) e Glossophaga soricina (1). Cinco amostras positivas foram detectadas por meio do ensaio de PCR, e quatro destas também foram positivas em esfregaços de sangue. A partir do sequenciamento do genoma e análise comparativa com sequências depositadas no GenBank, uma amostra apresentou 99,31% de similaridade com a espécie Litomosoides brasiliensis. O presente estudo expande a distribuição geográfica de L. brasiliensis, abrangendo o estado do Maranhão como área de ocorrência desta espécie, e inclui D. gnoma e A. fimbriatus como hospedeiros no Brasil.

Palavras-chave:
Nematoda; morcegos; filarídeos; Brasil

Introduction

Brazil has a diverse chiropteran fauna that includes 9 families, 68 genera and 179 species (Feijó et al., 2015Feijó ARA, Rocha PA, Althoff S. New species of Histiotus (Chiroptera: Vespertilionidae) from northeastern Brazil. Zootaxa 2015; 4048(3): 412-427. http://dx.doi.org/10.11646/zootaxa.4048.3.4.
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; Nogueira et al., 2014Nogueira MR, de Lima IP, Moratelli R, Tavares VC, Gregorin R, Peracchi AL. Checklist of Brazilian bats, with comments on original records. Check List 2014; 10(4): 808-821. http://dx.doi.org/10.15560/10.4.808.
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; Paglia et al., 2012Paglia AP, Fonseca GAB, Rylands AB, Herrmann G, Aguiar LMS, Chiarello AG, et al. Annotated checklist of Brazilian mammals. 2nd ed. Arlington, VA: Conservation International; 2012. (Occasional Papers in Conservation Biology; no. 6).). These form an important component of the mammalian fauna of Neotropical ecosystems, with regard to their richness and species diversity (Kalko, 1998Kalko EKV. Organisation and diversity of tropical bat communities through space and time. Zoology 1998; 101: 281-297.; Marinho-Filho & Gastal, 2001Marinho-Filho J, Gastal ML. Mamíferos das Matas Ciliares dos Cerrados do Brasil Central. In: Rodrigues RR, Leitão-Filho HF, editors. Matas ciliares: conservação e recuperação. 2. ed. São Paulo: EDUSP; 2001. p. 209-221.). Moreover, bats play an important role in maintaining the environmental balance, since they are pollinators, seed dispersers and predators (Bianconi et al., 2004Bianconi GV, Mikich SB, Pedro WA. Diversidade de morcegos (Mammalia, Chiroptera) em remanescentes florestais do município de Fênix, noroeste do Paraná, Brasil. Rev Bras Zool 2004; 21(4): 943-954. http://dx.doi.org/10.1590/S0101-81752004000400032.
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; Kalko, 1998Kalko EKV. Organisation and diversity of tropical bat communities through space and time. Zoology 1998; 101: 281-297.; Menezes et al., 2015Menezes LF Jr, Duarte AC, Contildes MD, Peracchi AL. Comparação da quiropterofauna em área florestada e área aberta da RPPN Fazenda Bom Retiro, Rio de Janeiro, Brasil. Iheringia Ser Zool 2015; 105(3): 271-275. http://dx.doi.org/10.1590/1678-476620151053271275.
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; Pedrozo et al., 2016Pedrozo AR, Gomes LAC, Guimarães M, Uieda W. Quiropterofauna da Fazenda Santo Antônio dos Ipês, Jaú, estado de São Paulo, Brasil. Biotemas 2016; 29(1): 97-107. http://dx.doi.org/10.5007/2175-7925.2016v29n1p97.
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). They are also considered to be important reservoirs of emerging and re-emerging zoonotic pathogens. Therefore, continuous surveillance and monitoring of these animals is essential in order to prevent pandemics (Brook & Dobson, 2015Brook CE, Dobson AP. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol 2015; 23(3): 172-180. http://dx.doi.org/10.1016/j.tim.2014.12.004.
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; Kadam et al., 2021Kadam SB, Sukhramani GS, Bishnoi P, Pable AA, Barvkar VT. SARS-CoV-2, the pandemic coronavirus: molecular and structural insights. J Basic Microbiol 2021; 61(3): 180-202. http://dx.doi.org/10.1002/jobm.202000537.
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; León et al., 2021León B, González SF, Solís LM, Ramírez-Cardoce M, Moreira-Soto A, Cordero-Solórzano JM, et al. Rabies in Costa Rica - next steps towards controlling bat-borne rabies after its elimination in dogs. Yale J Biol Med 2021; 94(2): 311-329.).

Bats’ characteristics of high flight mobility, great diversity of shelters, interaction among species in the same environment and remarkable social behavior make them interesting subjects for scientific studies. They contribute to transmission and spreading of microorganisms such as helminths, fungi, protozoa, bacteria and virus (Cabral et al., 2013Cabral AD, Gama AR, Sodré MM, Savani ESMM, Galvão-Dias MA, Jordão LR, et al. First isolation and genotyping of Toxoplasma gondii from bats (Mammalia: chiroptera). Vet Parasitol 2013; 193(1-3): 100-104. http://dx.doi.org/10.1016/j.vetpar.2012.11.015.
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; Frick et al., 2016Frick WF, Puechmaille SJ, Willis CK. White-nose syndrome in bats. In: Voigt CC, Kingston T, editors. Bats in the anthropocene: conservation of bats in a changing world. Cham, Switzerland: Springer; 2016. p. 245-262. http://dx.doi.org/10.1007/978-3-319-25220-9_9.
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; Roque & Jansen, 2014Roque AL, Jansen AM. Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl 2014; 3(3): 251-262. http://dx.doi.org/10.1016/j.ijppaw.2014.08.004.
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; Savani et al., 2009Savani ESMM, de Almeida MF, de Oliveira Camargo MCG, D’Auria SRN, Silva MMS, de Oliveira ML, et al. Detection of Leishmania (Leishmania) amazonensis and Leishmania (Leishmania) infantum chagasi in Brazilian bats. Vet Parasitol 2009; 168(1-2): 5-10. http://dx.doi.org/10.1016/j.vetpar.2009.10.019.
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; Zetun et al., 2009Zetun CB, Hoffmann JL, Silva RC, Souza LC, Langoni H. Leptospira spp. and Toxoplasma gondii antibodies in vampire bats (Desmodus rotundus) in Botucatu region, SP, Brazil. J Venom Anim Toxins Incl Trop Dis 2009; 15(3): 546-552. http://dx.doi.org/10.1590/S1678-91992009000300014.
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).

Studies on parasite biodiversity are important for species management and conservation, since parasitism plays an essential role in ecosystems, through regulating host density, stabilizing food chains and structuring communities of animals (Poulin & Morand, 2000Poulin R, Morand S. The diversity of parasites. Q Rev Biol 2000; 75(3): 277-293. http://dx.doi.org/10.1086/393500.
http://dx.doi.org/10.1086/393500...
). Because of the high relevance of parasite diversity to ecosystems, any report on parasite infection provides understanding about ecology and environmental impacts (Rendón-Franco et al., 2019Rendón-Franco E, López-Díaz O, Martínez-Hernández F, Villalobos G, Muñoz-García CI, Aréchiga-Ceballos N, et al. Litomosoides sp. (Filarioidea: Onchocercidae) Infection in Frugivorous Bats (Artibeus spp.): Pathological Features, Molecular Evidence, and Prevalence. Trop Med Infect Dis 2019; 4(2): 77. http://dx.doi.org/10.3390/tropicalmed4020077.
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).

In Brazil, 59 species of helminths have been reported as infecting bats: 28 species of nematodes, 23 of trematodes, 6 of cestodes and 2 of acanthocephalans (Cardia et al., 2015Cardia DFF, Tebaldi JH, Nascimento AA, Hoppe LG, Bresciani DS. Helminths of Brazilian bats. In: Jenkins OP, editor. Advances in Animal Science and Zoology. New York: Nova Science Publishers; 2015. p. 71-84.; Santos & Gibson, 2015Santos CP, Gibson DI. Checklist of the helminth parasites of South American bats. Zootaxa 2015; 3937(3): 471-499. http://dx.doi.org/10.11646/zootaxa.3937.3.3.
http://dx.doi.org/10.11646/zootaxa.3937....
). The state of Maranhão is located in the Legal Amazon region, with a strategic position at the confluence of the Cerrado, Caatinga and Brazilian Amazon biomes, and comprises a mosaic of landscapes that are rich in fauna and flora. In this Neotropical region, studies have been conducted to provide data on chiropteran species (Bernard et al., 2011Bernard E, Tavares VC, Sampaio E. Compilação atualizada das espécies de morcegos (Chiroptera) para a Amazônia Brasileira. Biota Neotrop 2011; 11(1): 35-46. http://dx.doi.org/10.1590/S1676-06032011000100003.
http://dx.doi.org/10.1590/S1676-06032011...
; Cruz et al., 2007Cruz LD, Martínez C, Fernandes FR. Comunidades de morcegos em hábitats de uma Mata Amazônica remanescente na Ilha de São Luís, Maranhão. Acta Amaz 2007; 37(4): 613-619. http://dx.doi.org/10.1590/S0044-59672007000400017.
http://dx.doi.org/10.1590/S0044-59672007...
; Olímpio et al., 2016Olímpio APM, Ventura MCS, Mascarenhas MDJO, Nascimento DC, Andrade FAG, Fraga EC, et al. Bat fauna of the Cerrado savanna of eastern Maranhão, Brazil, with new species occurrences. Biota Neotrop 2016; 16(3): e20150089. http://dx.doi.org/10.1590/1676-0611-BN-2015-0089.
http://dx.doi.org/10.1590/1676-0611-BN-2...
). However, despite the high species diversity, studies on internal parasites in these biomes are scarce.

The aim of the present study was to investigate filariid species among chiropterans in the Legal Amazon region, in order to contribute to knowledge about the biodiversity of filariids among bats in Brazil.

Materials and methods

Study area

This study was carried out in the municipalities of Turiaçu (1°39’44’’ S; 45°23’30’’ W), Cândido Mendes (1°26’34’’ S; 45°43’19’’ W), Godofredo Viana (1°24’19’’ S; 45°46’49’’ W) and Carutapera (1°12’11’’ S; 46°01’60’’ W), which are in the Gurupi microregion of the state of Maranhão, northeastern Brazil (Figure 1).

Figure 1
Municipalities of Turiaçu, Cândido Mendes, Godofredo Viana and Carutapera, in the Gurupi microregion of the state of Maranhão, northeastern Brazil.

Sample collection

Sampling periods were selected based on the lunar calendar and were concentrated in April 2017 in Godofredo Viana and Cândido Mendes and in March 2018 in Turiaçu and Carutapera.

Bats were collected between 18:00 and 00:00, over 5-day periods, with the aid of mist nets. They were then anesthetized with ketamine, at a dose according to their weight, photographed and identified. Specimen identification was performed based on specialized classification (Dos Reis et al., 2007Dos Reis NR, Peracchi AL, Pedro WA, de Lima IP. Morcegos do Brasil. Londrina: Universidade Estadual de Londrina; 2007.; Miranda et al., 2011Miranda JMD, Bernardi IP, Passos FC. Chave ilustrada para determinação dos morcegos da Região Sul do Brasil. Curitiba: João M.D. Miranda; 2011.; Uieda, 2008Uieda W. História natural dos morcegos hematófagos no Brasil. História natural dos morcegos hematófagos no Brasil. In: Pacheco S, Marques R, Esberard CEL, editors. Morcegos no Brasil: biologia, sistemática, ecologia e conservação. Porto Alegre: Editora Armazém Digital; 2008. p. 510.). Approximately 2 mL of blood were collected from each specimen by means of cardiac puncture, for blood smears and molecular assays.

Parasitological detection of filariids

Blood smears were made in triplicate, fixed with methanol, stained with Giemsa and analyzed under an optical microscope at 40x and 100x magnification. The blood smears were scanned to search for microfilariae.

Molecular assay

Genomic DNA was extracted from blood, in accordance with the protocol established for use in the Genejet Genomic DNA purification kit (Thermo Scientific, UAB, Lithuania), with previous incubation of 0.5 g of tissue, 20 μL of proteinase enzyme K (20 mg/ml) and 700 μL of lysis solution. Fragments of the gene 12S rDNA were amplified by means of the polymerase chain reaction (PCR), using the primer pairs Fila12SF (5’-CGGGAGTAAAGTTTTGTTTAAACCG-3’) and Fila12SR (5’-CATTGACGGATGGTTTGTACCAC-3’), as described by Otranto et al. (2011)Otranto D, Brianti E, Dantas-Torres F, Weigl S, Latrofa MS, Gaglio G, et al. Morphological and molecular data on the dermal microfilariae of a species of Cercopithifilaria from a dog in Sicily. Vet Parasitol 2011; 182(2-4): 221-229. http://dx.doi.org/10.1016/j.vetpar.2011.05.043.
http://dx.doi.org/10.1016/j.vetpar.2011....
, which amplify fragments of 330 bp from preserved filariids.

The amplified products were subjected to horizontal electrophoresis at 50 V/100 mA in Tris-acetate-EDTA (TAE) buffer, on 1.5% agarose gel stained with SYBR Safe (Invitrogen). The bands were viewed and photographed using a UV light transilluminator. The amplified products were purified using the ExoSAP-IT commercial product (USB Corporation), consisting of Exonuclease I (Exo I) to digest excess primers and shrimp alkaline phosphatase (SAP) to degrade excess nucleotides from the PCR. After purification, sequencing was performed using the Big Dye Terminator kit (Perkin Elmer), in accordance with the manufacturer’s specifications, in an ABI PRISM 3500 automated sequencer (Life Technologies). The sequences obtained were edited in the SeqMan software (Lasergene, DNAstar, Madison, Wisconsin, United States) and were subjected to similarity analysis using the Basic Local Alignment Search Tool (BLAST two-sequence analysis) to verify their homology with corresponding sequences available in GenBank (Altschul et al., 1990Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215(3): 403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
http://dx.doi.org/10.1016/S0022-2836(05)...
).

Results

Among the 82 bat specimens that were caught, 24 (29.26%) were obtained from the municipality of Godofredo Viana (23 from the family Phyllostomidae and one from Vespertilionidae). In Turiaçu, 14 (17.07%) were caught, all of them from the family Phyllostomidae; 26 (31.70%) from Candido Mendes (25 Molossidae and 1 Phyllostomidae); and 18 (21.95%) from Carutapera (all of them in the family Phyllostomidae).

In this study the following genera/species were identified: Artibeus fimbriatus, Dermanura gnoma, Uroderma bilobatum, Glossophaga soricina, Molossus molossus, Molossus sp., Artibeus sp., Carollia sp., Dermanura sp. and Myotis nigricans. Among the bats recorded in all areas, the most frequent were Artibeus sp. (26/82) and Molossus molossus (24/82) (Table 1).

Table 1
Distribution of bat genera/species captured in the Municipalities of Godofredo Viana, Turiaçu, Cândido Mendes e Carutapera, Maranhão, Brazil.

Microfilariae (Figure 2) were observed in blood smears from bats of the species Carollia perspicillata (2 specimens), Artibeus lituratus (1), Artibeus fimbriatus (2), Dermanura gnoma (2) and Glossophaga soricina (1). Except for G. soricina, which is a nectar-feeding bat, the other species are fruit bats.

Figure 2
Microfilariae in blood smears from bats, state of Maranhão, northeastern Brazil. (A) [x400] and (B) [x1000].

From the PCR assays, five positive samples were detected; four of these were also found to be positive through blood smears. From genome sequencing and comparative analysis with sequences deposited in GenBank, one was found to show 99.31% similarity to the species Litomosoides brasiliensis (accession number: MW471081.1).

Discussion

The family Phyllostomidae was the most representative (68%) among the bats sampled, followed by Molossidae (30.66%). The high frequency of catching specimens of Phyllostomidae was due to its diversity in Brazil: this family accounts for approximately 57% of all bat species in this country.

According to Anderson & Bain (2009)Anderson RC, Bain O. Spirurida: Diplotriaenoidea, Aproctoidea e Filaroidea. In: Anderson RC, Chabaud AG, Willmott S, editors. Keys to the nematode parasites of vertebrates. Wallingford: CAB International; 2009. p. 391-448. http://dx.doi.org/10.1079/9781845935726.0391.
http://dx.doi.org/10.1079/9781845935726....
, the family Onchocercidae is composed of seven subfamilies, in which five genera have already been identified in bats: Litomosoides, Migonella, Chiropterofilaria, Josefilaria and Litomosa (Bain et al., 2002Bain O, Babayan S, Gomes J, Rojas G, Guerrero R. First account on the larval biology of a Litomosoides filaria, from a bat. Parassitologia 2002; 44(1-2): 89-92.). The genus Litomosoides, which includes at least 31 species (Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
), and the genus Migonella are found in bats in South America (Santos & Gibson, 2015Santos CP, Gibson DI. Checklist of the helminth parasites of South American bats. Zootaxa 2015; 3937(3): 471-499. http://dx.doi.org/10.11646/zootaxa.3937.3.3.
http://dx.doi.org/10.11646/zootaxa.3937....
).

In studies conducted in Brazil, parasitism by species of Litomosoides in bats of the genus Artibeus and Carollia has also been reported (Albuquerque et al., 2015Albuquerque ACA, Moraes MFD, Silva AC, Tebaldi JH, Lux Hoppe EG. Diversidade de parasitas em quirópteros do bioma Amazônia. Ars Vet 2015; 31(2): 48. http://dx.doi.org/10.15361/2175-0106.2015v31n2p48.
http://dx.doi.org/10.15361/2175-0106.201...
; Cardia 2012Cardia DFF. Helmintos de quirópteros da região Centro-Oeste do Estado de São Paulo [tese]. Jaboticabal: Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista; 2012.; Costa et al., 2021Costa MAT, Santos BMR, Alves DCL, Oliveira HHA, Silva GD, de Moura Pires S, et al. Endoparasitos de morcegos da floresta Nacional de Palmares (Flona), Altos–Piauí, Brasil. Braz J Develop 2021; 7(3): 22852-22871. http://dx.doi.org/10.34117/bjdv7n3-143.
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; Mello, 2017Mello EM. Interações taxonômicas entre parasitos e morcegos de alguns municípios do estado de Minas Gerais [tese]. Belo Horizonte: Universidade Federal de Minas Gerais; 2017.; Vicente et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: nematóides de mamíferos. Rev Bras Zool 1997; 14(suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
). However, these studies consisted of reports on adult parasites and not microfilaria in blood samples. In the present study, the diagnosis was based on findings of microfilaria in blood smears and on PCR-positive samples and genome sequencing.

Presence of microfilaria in peripheral blood allows transmission of the parasite within the bat population, both though hematophagous arthropods and transplacentally (Gazarini et al., 2012Gazarini J, Pesenti L, Takemoto RM. Primeira evidência de transmissão transplacentária de Nematoda (Litomosoides sp.) na ordem Chiroptera (Microchiroptera: phyllostomidae). The Biologist 2012; 10(2): 31.; Williams, 1948Williams RW. Studies on the life cycle of Litomosoides carinii, filariid parasite of the cotton rat, Sigmodon hispidus litoralis. J Parasitol 1948; 34(1): 24-43. http://dx.doi.org/10.2307/3273239.
http://dx.doi.org/10.2307/3273239...
). Transmission is facilitated through the bats’ habits, since they live in groups and use caverns and trees as shelters (Melaun et al., 2014Melaun C, Werblow A, Busch MW, Liston A, Klimpel S. Bats as potential reservoir hosts for vector-borne diseases. In: Klimpel S, Mehlhorn H, editors. Bats (Chiroptera) as vectors of diseases and parasites. Berlin, Heidelberg: Springer; 2014. p. 25-61. http://dx.doi.org/10.1007/978-3-642-39333-4_3.
http://dx.doi.org/10.1007/978-3-642-3933...
; Sekiama et al., 2013Sekiama ML, Rocha VJ, Peracchi AL. Subfamília Desmodontinae. In: Reis NR, Fregonezi MN, Peracchi AL, Shibata AO, editors. Morcegos do Brasil - Guia de Campo. Rio de Janeiro: Technical Books; 2013. p. 48-51.).

Although the vectors of bat filariids are not well known, certain species of Litomosoides are transmitted by hematophagous mites (Williams, 1948Williams RW. Studies on the life cycle of Litomosoides carinii, filariid parasite of the cotton rat, Sigmodon hispidus litoralis. J Parasitol 1948; 34(1): 24-43. http://dx.doi.org/10.2307/3273239.
http://dx.doi.org/10.2307/3273239...
), such as those in the families Dermanyssidae (Anderson, 2000Anderson RC. Nematode parasites of vertebrates: their development and transmission. Wallingford: CAB International; 2000. http://dx.doi.org/10.1079/9780851994215.0000.
http://dx.doi.org/10.1079/9780851994215....
) and Macronyssidae (Bain et al., 2002Bain O, Babayan S, Gomes J, Rojas G, Guerrero R. First account on the larval biology of a Litomosoides filaria, from a bat. Parassitologia 2002; 44(1-2): 89-92.; Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
). The latter family is also considered to act as vectors for filariids in rodents and marsupials (Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
).

Litomosoides spp. have also been detected through PCR on blood samples from Artibeus jamaicensis and through PCR on genetic material from Trichobius intermedius (Diptera: Streblidae) and Periglischrus iheringi (Acari: Spinturnicidae). However, it was not possible to incriminate these as vectors (Reeves et al., 2016Reeves WK, Beck J, Orlova MV, Daly JL, Pippin K, Revan F, et al. Ecology of bats, their ectoparasites, and associated pathogens on Saint Kitts Island. J Med Entomol 2016; 53(5): 1218-1225. http://dx.doi.org/10.1093/jme/tjw078.
http://dx.doi.org/10.1093/jme/tjw078...
).

Adults of the genus Litomosoides include species that parasitize the thoracic and abdominal cavities of phyllostomid and mormoopid bats; cricetid, sciurid and hystricognath rodents; and didelphid marsupials (Brant & Gardner, 2000Brant SV, Gardner SL. Phylogeny of species of the genus Litomosoides (Nemata [corrected]: Onchocercidae): evidence of rampant host switching. J Parasitol 2000; 86(3): 545-554. http://dx.doi.org/10.1645/0022-3395(2000)086[0545:POSOTG]2.0.CO;2.
http://dx.doi.org/10.1645/0022-3395(2000...
; Forrester & Kinsella, 1973Forrester DJ, Kinsella JM. Comparative morphology and ecology of two species of Litomosoides (Nematoda: Filarioidea) of rodents in Florida, with a key to the species of Litomosoides Chandler, 1931. Int J Parasitol 1973; 3(2): 255-263. http://dx.doi.org/10.1016/0020-7519(73)90031-3.
http://dx.doi.org/10.1016/0020-7519(73)9...
; Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
; Notarnicola & Navone, 2011Notarnicola J, Navone GT. Litomosoides pardinasi n. sp. (Nematoda: Onchocercidae) from two species of cricetid rodents in Northern Patagonia, Argentina. Parasitol Res 2011; 108(1): 187-194. http://dx.doi.org/10.1007/s00436-010-2051-3.
http://dx.doi.org/10.1007/s00436-010-205...
).

In the present study, microfilariae of Litomosoides sp. were found in blood smears from C. perspicillata, A. lituratus, A. fimbriatus, D. gnoma and G. soricine. Reports of Litomosoides sp. in association with the genera Artibeus and Carollia are not uncommon; in fact, among chiropterans, this nematode seems to prefer host of the genus Artibeus (Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
; Jiménez et al., 2017Jiménez FA, Caspeta-Mandujano JM, Ramírez-Chávez SB, Ramírez-Díaz SE, Juárez-Urbina MG, Peralta-Ramírez JL, et al. Checklist of helminths of bats from México and Central América. J Parasitol Biodiversity 2017; 8. http://dx.doi.org/10.13014/K2ZG6QDX.
http://dx.doi.org/10.13014/K2ZG6QDX...
). These parasites are limited to only a few host species and are order specific. Thus, species that occur in bats do not occur in rodents and marsupials, and vice versa (Brant & Gardner, 2000Brant SV, Gardner SL. Phylogeny of species of the genus Litomosoides (Nemata [corrected]: Onchocercidae): evidence of rampant host switching. J Parasitol 2000; 86(3): 545-554. http://dx.doi.org/10.1645/0022-3395(2000)086[0545:POSOTG]2.0.CO;2.
http://dx.doi.org/10.1645/0022-3395(2000...
; Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
; Vogeler et al., 2018Vogeler AVB, Tschapka M, Kalko EKV, Cottontail VM. Litomosoides microfilaria in seven neotropical bat species. J Parasitol 2018; 104(6): 713-717. http://dx.doi.org/10.1645/15-719.
http://dx.doi.org/10.1645/15-719...
).

It is important to highlight that among the bat species that presented microfilariae, four were fruit bats and one was a nectar-feeding bat. Both of these types of bat are fundamental for the biosystem and ecosystem, since they fly long distances searching for fruits and they disperse seeds along the way and act as pollinators. Hence, they are essential for forest regeneration and maintenance of plant diversity and ecosystem equilibrium (Estrada & Coates-Estrada, 2001Estrada A, Coates-Estrada R. Species composition and reproductive phenology of bats in a tropical landscape at Los Tuxtlas, México. J Trop Ecol 2001; 17(5): 627-646. http://dx.doi.org/10.1017/S026646740100147X.
http://dx.doi.org/10.1017/S0266467401001...
; Medellin & Gaona, 1999Medellin RA, Gaona O. Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, Mexico. Biotropica 1999; 31(3): 478-485. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00390.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
). However, when infected by Litomosoides, they can present signs of weakness, tachypnea and hemorrhage, which leads to decreased efficiency of seed dispersion and pollination (Rendón-Franco et al., 2019Rendón-Franco E, López-Díaz O, Martínez-Hernández F, Villalobos G, Muñoz-García CI, Aréchiga-Ceballos N, et al. Litomosoides sp. (Filarioidea: Onchocercidae) Infection in Frugivorous Bats (Artibeus spp.): Pathological Features, Molecular Evidence, and Prevalence. Trop Med Infect Dis 2019; 4(2): 77. http://dx.doi.org/10.3390/tropicalmed4020077.
http://dx.doi.org/10.3390/tropicalmed402...
).

The molecular analysis on the blood samples showed there was 99.31% similarity to L. brasiliensis. This species has been reported parasitizing the families Phyllostomidae and Vespertilionidae, which are widely distributed in South and Central (Albuquerque et al., 2015Albuquerque ACA, Moraes MFD, Silva AC, Tebaldi JH, Lux Hoppe EG. Diversidade de parasitas em quirópteros do bioma Amazônia. Ars Vet 2015; 31(2): 48. http://dx.doi.org/10.15361/2175-0106.2015v31n2p48.
http://dx.doi.org/10.15361/2175-0106.201...
; Brant & Gardner, 2000Brant SV, Gardner SL. Phylogeny of species of the genus Litomosoides (Nemata [corrected]: Onchocercidae): evidence of rampant host switching. J Parasitol 2000; 86(3): 545-554. http://dx.doi.org/10.1645/0022-3395(2000)086[0545:POSOTG]2.0.CO;2.
http://dx.doi.org/10.1645/0022-3395(2000...
; Costa et al., 2021Costa MAT, Santos BMR, Alves DCL, Oliveira HHA, Silva GD, de Moura Pires S, et al. Endoparasitos de morcegos da floresta Nacional de Palmares (Flona), Altos–Piauí, Brasil. Braz J Develop 2021; 7(3): 22852-22871. http://dx.doi.org/10.34117/bjdv7n3-143.
http://dx.doi.org/10.34117/bjdv7n3-143...
; Guerrero et al., 2002Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comp Parasitol 2002; 69(2): 177-195. http://dx.doi.org/10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2.
http://dx.doi.org/10.1654/1525-2647(2002...
; Jiménez et al., 2021Jiménez FA, Notarnicola J, Gardner SL. Host-Switching events in Litomosoides Chandler, 1931 (Filarioidea: Onchocercidae) are not rampant but clade dependent. J Parasitol 2021; 107(2): 320-335. http://dx.doi.org/10.1645/20-35.
http://dx.doi.org/10.1645/20-35...
; Mourão et al., 2002Mourão ED, Avilla LS, Lent H. Redescrição de Litomosoides brasiliensis Almeida, 1936 (Nematoda: Filariidae) Parasito de Anoura caudifera (Chiroptera: Phyllostomidae). Mem Inst Oswaldo Cruz 2002; 97(4): 495-499. http://dx.doi.org/10.1590/S0074-02762002000400007.
http://dx.doi.org/10.1590/S0074-02762002...
; Vicente et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: nematóides de mamíferos. Rev Bras Zool 1997; 14(suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; Vogeler et al., 2018Vogeler AVB, Tschapka M, Kalko EKV, Cottontail VM. Litomosoides microfilaria in seven neotropical bat species. J Parasitol 2018; 104(6): 713-717. http://dx.doi.org/10.1645/15-719.
http://dx.doi.org/10.1645/15-719...
). In Brazil, presence of L. brasiliensis has been reported in the states of Amapá, Minas Gerais, Mato Grosso, Mato Grosso do Sul, Pará, Piauí, Paraná, Rio de Janeiro and São Paulo (Albuquerque et al., 2015Albuquerque ACA, Moraes MFD, Silva AC, Tebaldi JH, Lux Hoppe EG. Diversidade de parasitas em quirópteros do bioma Amazônia. Ars Vet 2015; 31(2): 48. http://dx.doi.org/10.15361/2175-0106.2015v31n2p48.
http://dx.doi.org/10.15361/2175-0106.201...
; Costa et al., 2021Costa MAT, Santos BMR, Alves DCL, Oliveira HHA, Silva GD, de Moura Pires S, et al. Endoparasitos de morcegos da floresta Nacional de Palmares (Flona), Altos–Piauí, Brasil. Braz J Develop 2021; 7(3): 22852-22871. http://dx.doi.org/10.34117/bjdv7n3-143.
http://dx.doi.org/10.34117/bjdv7n3-143...
; Mourão et al., 2002Mourão ED, Avilla LS, Lent H. Redescrição de Litomosoides brasiliensis Almeida, 1936 (Nematoda: Filariidae) Parasito de Anoura caudifera (Chiroptera: Phyllostomidae). Mem Inst Oswaldo Cruz 2002; 97(4): 495-499. http://dx.doi.org/10.1590/S0074-02762002000400007.
http://dx.doi.org/10.1590/S0074-02762002...
). Now, we register it in the state of Maranhão. This study provides the first report of L. brasiliensis parasitizing D. gnoma and A. fimbriatus in Brazil.

Phylogenetic analyses have been used to reconstruct the evolution of Litomosoides and infer its history. Two decades ago, Brant & Gardner (2000)Brant SV, Gardner SL. Phylogeny of species of the genus Litomosoides (Nemata [corrected]: Onchocercidae): evidence of rampant host switching. J Parasitol 2000; 86(3): 545-554. http://dx.doi.org/10.1645/0022-3395(2000)086[0545:POSOTG]2.0.CO;2.
http://dx.doi.org/10.1645/0022-3395(2000...
suggested that this genus was not a monophyletic group, although they identified 22 morphological characteristics with high levels of homoplasy. However, a recent study on a database of DNA sequences demonstrated that Litomosoides showed up as a monophyletic group that originated in Neotropical phyllostomid bats, with strong evidence of at least two events of host changing: one of them involving cricetid rodents and the other, mormoopids. The latter event included simultaneous geographical expansion of the parasite’s range (Jiménez et al., 2021Jiménez FA, Notarnicola J, Gardner SL. Host-Switching events in Litomosoides Chandler, 1931 (Filarioidea: Onchocercidae) are not rampant but clade dependent. J Parasitol 2021; 107(2): 320-335. http://dx.doi.org/10.1645/20-35.
http://dx.doi.org/10.1645/20-35...
). Thus, studies on molecular detection of Litomosoides are relevant, to provide data for reconstructing the phylogeny of supposed changes to hosts and monophyly.

The present study expands the geographical distribution of L. brasiliensis, to include the state of Maranhão as an area of occurrence of this specie. This study also includes D. gnoma and A. fimbriatus as hosts in Brazil.

Acknowledgements

This work was supported by Fundação de Amparo ao Desenvolvimento Científico e Tecnológico do Maranhão/FAPEMA (Grant-003011-2020) and Coordenação de Aperfeiçoamento Técnico de Pessoal de Nível Superior/CAPES (Finance Code 001). To Andrea Teles dos Reis for the map elaboration.

  • How to cite: Costa TF, Coutinho DJB, Simas AKSM, Santos GV, Nogueira RMS, Costa FB, et al. Litomosoides brasiliensis (Nematoda: Onchocercidae) infecting chiropterans in the Legal Amazon region, Brazil. Braz J Vet Parasitol 2022; 31(4): e011722. https://doi.org/10.1590/S1984-29612022059

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Publication Dates

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

History

  • Received
    08 Aug 2022
  • Accepted
    27 Oct 2022
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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