ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2018, 12(2), jul-dic:153-159.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

MARACAYA BELEMENSIS ADAMSON & BACCAM, 1988 (ATRACTIDAE, ASCARIDIDA)

PARASITIZING CROTALUS DURISSUS LINNAEUS, 1758 (SERPENTES, VIPERIDAE) IN BRAZIL

MARACAYA BELEMENSIS ADAMSON & BACCAM, 1988 (ATRACTIDAE, ASCARIDIDA)

PARASITANDO UNA CROTALUS DURISSUS LINNAEUS, 1758 (SERPENTES, VIPERIDAE) EN

BRASIL

MARACAYA BELEMENSIS ADAMSON & BACCAM, 1988 (ATRACTIDAE, ASCARIDIDA)

PARASITANDO UMA CROTALUS DURISSUS LINNAEUS, 1758 (SERPENTES, VIPERIDAE) NO

BRASIL

1Universidade Federal de Minas Gerais (UFMG), Instituto de Ciências Biológicas, Belo Horizonte, Minas Gerais, Brasil.

2Centro de Controle de Zoonoses, Belo Horizonte, Minas Gerais, Brasil.

3Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brasil.

Corresponding author: E-mail: ericabiologia@gmail.com

1,2 3

Érica Munhoz de Mello & Reinaldo José da Silva

ABSTRACT

Keywords: Crotalus durissus – Ectopic infection – Nematode – Maracaya belemensis – Reptile disease

Maracaya Díaz-Ungría, 1964 is an obscure genus of amphisbaenian nematodes. In this study was

described a rattlesnake Crotalus durissus Linnaeus, 1758 parasitized by two specimens of Maracaya

belemensis Adamson & Baccam, 1988 in Southeast Brazil. The present study records a new host and

extends the geographical distribution for this nematode.

Neotropical Helminthology

153

Volume12,Number2(jul-dec2018)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

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VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

RESUMO

Palabras clave: Crotalus durissus – Enfermedad de reptiles – Infección ectópica – Nematodo – Maracaya belemensis

Maracaya Díaz-Ungría, 1964 es un género poco conocido de nematodo en anfibios. En este estudio se

describe una serpiente de cascabel Crotalus durissus Linnaeus, 1758 parasitada por dos especímenes de

Maracaya belemensis Adamson & Baccam, 1988 en el sureste de Brasil. El presente estudio registra un

nuevo hospedero y amplía la distribución geográfica de este nematodo.

The necropsy revealed a couple of Maracaya

belemensis in copulation inside the aorta artery in

the rattlesnake's heart. The specimens presented

whitish color, rhabditoid esophagus, isthmus well-

differentiated, evidenced bulb. Corpus and isthmus

well-demarcated. Excretory pore prominent, at

level of isthmus in male and level of bulb in female.

Cuticle striated transversely from base of lip to

posterior end. Tail straight, conical and thin. Male:

oral opening surrounded by three lips well-

chitinized. Spicules similar, equal, simple and

slightly arcuate. Gubernaculum short than spicules

and tapering gradually. Four pairs of precloacal

papillae, and three pairs postcloacal. Female:

anterior end without lips well-developed.

Monodelphic, vulva after middle of body, well-

developed vagina musculature. Eggs large, thin-

shelled and larvae (Fig. 1). The measures are

presented in Table 1.

Maracaya includes four valid species: Maracaya

graciai Diaz-Ungria, 1963 in Amphisbaena alba

Linnaeus, 1758 from Venezuela; Maracaya pusilla

(Miranda, 1924) in Amphisbaena sp. from Brazil

(Bahia State); M. belemensis in A. alba from Brazil

(Pará State); and Maracaya africana Bouamer &

Morand, 2006 in Chamaeleo inturensis Schmidt,

1919 from Congo.

The morphological analysis of the nematodes

found in the present study permitted us to conclude

that the species involved in the parasitism was M.

belemensis. This conclusion is supported

especially the shape of the spicules and

gubernaculum. The male specimen differs from M.

africana by present lips more developed and anal

region smaller than the rest of the body; from M.

pusilla by present non-bifid spicules; and from M.

graciai by gubernaculum shape. In relation to the

female, it was considered as an adult because

presented larval eggs. However, the specimen

presented different lips than male. Based on the

drawings of Adamson & Baccam (1988), the

154

Neotropical Helminthology, 2018, 12(2), jul-dic

INTRODUCTION

Maracaya Díaz-Ungría, 1964 includes small

nematodes parasites of amphisbaenian and lizard

intestines. Three species are described in

amphisbaenians in Brazil and one species in

chameleon in Congo (Miranda, 1924; Diaz-

Ungria, 1963; Adamson & Baccam, 1988;

Bouamer & Morand, 2006; Ávila & Silva, 2010).

The aim of this study is to report the first

occurrence of Maracaya belemensis Adamson &

Baccam, 1988 parasitizing a tropical rattlesnake

Crotalus durissus Linnaeus, 1758.

An adult female of C. durissus from the

municipality of Pouso Alegre (22°13'48"S

45°56'11"W), Minas Gerais State, Brazil, was

euthanatized using 2.5 mL of pentobarbital sodium

-1

30 mg·mL intracoelomically. The necropsy was

performed and each organ was individually

surveyed for parasites under a stereoscopic

microscope. The nematodes found were fixed in

hot 10% formaldehyde and clarified with Amann's

Lactophenol solution. The parasites were

photographed with a digital camera (AxioCam

ERc 5s, Carl Zeiss) coupled to the microscope and

morphological measurements performed through

the photos by AxioVision 4.8 software (Carl Zeiss

Vision). All measurements are in micrometer (μm)

unless otherwise stated. Drawings were made on

CorelDRAW X8 software using the photos as a

background for a more accurate drawing. The

species identification was based on Adamson &

Baccam (1988) and Bouamer & Morand (2006).

The helminths were deposited under the number

CHIBB 8479 in the Helminthological Collection of

the Institute of Biosciences (CHIBB), São Paulo

State University (UNESP), municipality of

Botucatu, São Paulo State, Brazil. This study was

approved by the Ethics Committee in Animal

Experimentation of the Federal University of

Minas Gerais under the protocol number 176/2012.

MATERIAL AND METHODS

DISCUSSION

RESULTS

Munhoz de Mello & Silva

155

Figure 1. Maracaya belemensis from Crotalus durissus. Male: (A) esophagus, (B,C) anterior end, (D) spicule, gubernaculum and

tail. Female: (E) anterior end, (F) muscular vagina, (G) larval egg, (H) tail.

B C

Maracaya parasitizing a Crotalus

Neotropical Helminthology, 2018, 12(2), jul-dic

156

Table 1. Morphometrical data of Maracaya spp.

Species Maracaya belemensis Maracaya belemensis Maracaya graciai Maracaya pusilla Maracaya africana

Reference

Present study

Adamson &

Baccam,

1988

Diaz-Ungria,

1963

Miranda,

1924

Bouamer &

Morand,

2006

Host

Crotalus durissus

Amphisbaena alba

Amphisbaena sp.

Chamaeleo inturensis

Origin

Brazil, Minas Gerais

Brazil, Pará

Venezuela

Brazil, Bahia

Congo

Sex (n)

Male

(n = 1) Female

(n = 1)

Male

(n= 19)

Female

(n = 19)

Female

L4 (n = 3)

Male

Female

Male

Female

Male

(n = 10)AFemale

(n =

10)B

Body

Length (mm)

3.85

2.41

2.49

1.62 1.46 2.0 2.0 2.6 2.48 2.38

Width

120.26

367.47

119

(127.1)

151

(151.14)

74 130 160 240 290 88 81

Esophagus

Length

muscular

515.11

670.43

450 360 500 490 503 522

Width muscular

60 60 56 56

Length Isthmus

65 70

Width Isthmus

15.85

69.58

Length bulb

105 75 92 83 73

Width bulb

58.72

170.9

85 (87.4)

102

(100.5)

57 85 80 92 62 58

Excretory pore

515.17

641.43

565 460 500 560 313 344

Lips

Length

75 75 71 71

Width

48.1

Table 1 (continued)

Neotropical Helminthology, 2018, 12(2), jul-dic Munhoz de Mello & Silva

157

Maracaya parasitizing a Crotalus

Neotropical Helminthology, 2018, 12(2), jul-dic

Nerv ring

265.23

268.69

302

(302.16)

321

(326.18)

200 - - 280 182 213

Tail

165.97

177.6

149

(147.1)

121

(129.9)

113 115 125-160 100 170 116 138

Spicules

90.76; 91.62

99 (98.4)

60 110 - 66

Gubernaculum

50.22

44 (47.3)

- 35 49 - 38

Vulva

2.44

mmC

700D

1.59 mmC

Eggs

Length

105.22

(n=10)

176-202

(190.8)

(n=10)

Width -

67.92

(n=10) -

85-123

(109.11)

(n=10) - - - - - 53

A - Holotype measures, B - Allotype measures, C - From anterior end, D - From posterior end.

Species Maracaya belemensis Maracaya belemensis Maracaya graciai Maracaya pusilla Maracaya africana

Reference

Present study

Adamson &

Baccam,

1988

Diaz-Ungria,

1963

Miranda,

1924

Bouamer &

Morand,

2006

Host

Crotalus durissus

Amphisbaena alba

Amphisbaena sp.

Chamaeleo inturensis

Origin

Brazil, Minas Gerais

Brazil, Pará

Venezuela

Brazil, Bahia

Congo

Sex (n)

Male (n = 1)

Female

(n = 1)

Male

(n = 19)

Female

(n = 19)

Female

L4 (n = 3)

Male

Female

Male

Female

Male

(n =

10)A Female

(n =

10)B

Table 1 (continued)

158

amphisbaenians in South America (Ávila & Silva,

2010).

female lips reported in the present study were

similar to lips of immature females of the fourth

larval stage of M. belemensis, but without cuticular

expansion.

Maracaya spp. cycles are not known. However, in

all records of Maracaya, the specimens were found

parasitizing the host intestines (Miranda, 1924;

Diaz-Ungria, 1963; Adamson & Baccam, 1988;

Bouamer & Morand, 2006; Ávila & Silva, 2010).

In the present study, the nematodes were found in

the host´s aorta. We have no idea how this

nematode couple reaches this site of infection, but

ectopic infection with nematode species have been

reported (De Ruiter et al., 1962; Tanabe et al.,

1990; Oliveira-Júnior et al., 2004). We believe that

the occurrence of Maracaya belemensis in snakes

is accidental, a fact that could be related to the

unusual labial characteristics of the female,

suggesting an incomplete development, and the

location of the specimens in the host.

Crotalus durissus is a snake widely distributed in

Brazil, being found in all the states of the country

(Costa & Bérnils, 2018), and presenting a

discontinuous distribution in Central and South

Americas (Uetz & Hallermann, 2018). Although

widely distributed, this species inhabits

preferentially open habitats, as Cerrado biome, and

deforested areas where shade occurrence and

vegetation cover are similar to those in Cerrado

(Tozetti & Martins, 2008). Thus, habitat

modification, deforestation, and habitat

fragmentation have favored the expansion of this

species in Brazil (Bastos et al., 2005; Duarte &

Menezes, 2013). The diet of C. durissus is

composed of small rodents and marsupials, and

occasionally of birds and lizards. Ameiva ameiva

Linnaeus, 1958 is the main lizard species preyed on

by C. durissus (Sant'anna & Abe, 2007; Hoyos &

Almeida-Santos, 2016; Santos & Germano, 1996),

without records of predation of the genus

Amphisbaena in the literature.

Among amphisbaenids, A. alba is the one with the

largest distribution in South America (Vanzolini,

2002) and presents a generalist diet. In Cerrado,

this species primarily eats ants, beetles,

grasshoppers, crickets, insect larvae, scorpions,

termites, and other invertebrates (Colli &

Zamboni, 1999). Based on the literature, it is

probable that Maracaya spp. are specific from

Adamson, ML & Baccam, D. 1988. Systematic

position of the Atractidae sensu Chabaud

(1978) (Nematoda: Cosmocercoidea):

Maracaya belemensis n. sp. and Aplectana

albae n. sp. from Amphisbaena alba in

Brazil. Canadian Journal of Zoology, vol.

66, pp.1857-1864.

Ávila, RW & Silva, RJ. 2010. Checklist of

helminths from lizards and amphisbaenians

(Reptilia, Squamata) of South America.

Journal of Venomous Animals and Toxins

including Tropical Diseases, vol. 16, pp.

543-572.

Bastos, EG, Araújo, AFB & Silva, HR. 2005.

Records of the rattlesnakes Crotalus

durissus terrificus (Laurenti) (Serpentes,

Viperidae) in the State of Rio de Janeiro,

Brazil: a possible case of invasion

facilitated by deforestation. Revista

Brasileira de Zoologia, vol. 22, pp. 812-815.

Bouamer, S & Morand, S. 2006. A new nematode

(Nematoda: Cosmocercidae) from the

lizard, Chamaeleo inturensis (Squamata:

Chamaeleonidae) from the Democratic

R e pu b l ic o f C o n g o . J o urn a l o f

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Colli, GR & Zamboni, DS. 1999. Ecology of the

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Neotropical Helminthology, 2018, 12(2), jul-dic