1 Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Av. Brasil, 4365, 21040-360, Rio de Janeiro, RJ, Brasil.

2IBEx- Instituto de Biologia do Exército, Rua Francisco Manuel, 102, 20911-270, Rio de Janeiro, RJ, Brasil.

3 Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) research fellow.

Neotrop. Helminthol., 4(2), 2010

2010 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

Palabras clave: Brasil - cascabel - Crotalus durissus - nemátodos.

Resumen

Cuarenta y seis muestras de nemátodos recuperados en especímenes brasileños de Crotalus durissus

Linnaeus, 1758, comúnmente conocida como cascabel fueron estudiadas. Las serpientes o se sacrificaban en

cautiverio para la producción de suero o fueron encontradas muertas en la naturaleza. Otras muestras de

nemátodos de este huésped preservadas en la Colección Helmintológica del Instituto Oswaldo Cruz

(CHIOC) fueron también analizadas. Los nematodos mas prevalentes fueron aquellos del género

Ophidascaris Baylis, 1920: O. arndti Sprehn, 1929, O. durissus Panizzutti, Santos, Vicente, Muniz-Pereira

& Pinto, 2003, O. O. sicki Freitas, 1951, O. tuberculatum Siqueira, Panizzutti, Muniz-Pereira & Pinto, 2005 y

Ophidascaris sp., seguidas por otros incluidos en Hexametra Travassos, 1920: H. boddaertii (Baird, 1860)

Kreis, 1944, y Kalicephalus Molin, 1861: K. inermis macrovulvus Caballero, 1954 y Kalicephalus sp.

Además, fueron identificados especímenes representados en los géneros Hastospiculum Skrjabin, 1923:

Hastospiculum sp., Physaloptera Rud, 1819: Physaloptera sp. y Travassosascaris Sprent, 1978: T. araujoi

(Schneider, 1866) Sprent, 1978. Las especies Ophidascaris arndti, O. sicki, O. tuberculatum, K. inermis

macrovulvus y Physalopera sp., representan nuevos registros en este huésped. Las especies son brevemente

presentadas y ilustradas con énfasis en las estructuras bucales, por medio de cortes transversales.

Key words: Brazil - Crotalus durissus - nematodes - rattlesnake.

Abstract

Forty-six samples of nematodes recovered from Brazilian specimens of Crotalus durissus Linnaeus, 1758,

commonly named rattlesnake were studied. Snakes either died in captivity, under which they were kept for

production of serum, or were found dead in nature. Other samples of nematodes from this host and preserved

in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) were also analyzed. The most

prevalent species were those of the genus Ophidascaris Baylis, 1920: O. arndti Sprehn, 1929, O. durissus

Panizzutti, Santos, Vicente, Muniz-Pereira & Pinto, 2003, O. sicki Freitas, 1951, O. tuberculatum Siqueira,

Panizzutti, Muniz-Pereira & Pinto, 2005 and Ophidascaris sp., followed by specimens allocated in

Hexametra Travassos, 1920: H. boddaertii (Baird, 1860) Kreis, 1944, and Kalicephalus Molin, 1861: K.

inermis macrovulvus Caballero, 1954, Kalicephalus sp. Also, specimens representing the genera

Hastospiculum Skrjabin, 1923: Hastospiculum sp., Physaloptera Rud, 1819: Physaloptera sp. and

Travassosascaris Sprent, 1978: T. araujoi (Schneider, 1866) Sprent, 1978 were identified, as well. The

species Ophidascaris arndti, O. sick, O. tuberculatum, K. inermis macrovulvus and Physalopera sp.,

represent new occurrences in this host. Species are briefly presented and figured, with emphasis in the cross

sections of buccal structures.

NEMATODE PARASITES OF THE NEOTROPICAL RATTLESNAKE,

CROTALUS DURISSUS LINNAEUS, 1758 (OPHIDIA, VIPERIDAE)

FROM BRAZIL: NEW RECORDS AND GENERAL ASPECTS

NEMATODOS PARÁSITOS DE LA CASCABEL NEOTROPICAL,

CROTALUS DURISSUS LINNAEUS, 1758 (OPHIDIA, VIPERIDAE)

EN BRASIL: NUEVOS REGISTROS Y ASPECTOS GENERALES

1,3* 1 1,2 1

Roberto Magalhães Pinto , Luís C. Muniz-Pereira , Marcia Helena Martins Panizzutti & Dely Noronha

ORIGINAL ARTICLES /ARTÍCULOS ORIGINALES

Suggested citation: Pinto, R.M.; Muniz-Pereira, L.C.; Panizzutti, M.M.H.& Noronha, D. Nematode parasites of the neotropical

rattlesnake, Crotalus durissus linnaeus, 1758 (Ophidia, viperidae) from Brazil: new records and general

aspects. 2010. Neotropical Helminthology, vol. 4, nº 2, pp. 137-147.

137

INTRODUCTION

The first report of helminths from Brazilian reptiles

occurred far back in the XVII century, when some

parasites of iguanas were referred by Piso &

Marcgrave (1648). From this date on, studies of the

parasitism affecting reptiles in Brazil have been

relatively few and scarce. However, in the last

century, complete surveys of nematodes recovered

from Brazilian vertebrates have been made

available by Vicente & Pinto (1999) and Vicente et

al. (1985, 1991, 1993, 1995, 1997).

Taking into account that the catalogue of

nematodes from Brazilian reptiles (Vicente et al.

1993) permits an easier identification of the species

parasitizing snakes, the present investigation aimed

at the updating of data related to the nematodes

collected in specimens of Crotalus durissus

Linnaeus, 1758 presently captured in different

Brazilian localities together with other nematode

samples previously recovered from the same host

and deposited in the Helminthological Collection

of the Oswaldo Cruz Institute (CHIOC). The

present findings also complement those already

reported by Araujo et al. (1969 a-b), Araújo et al

(1999), Silva et al. (2001, 2007), Panizzutti et al.

(2003), Dias et al. (2004) and Panizzutti (2005),

specifically related to the nematodes from C.

durissus in Brazil, together with data after

Rossellini (2007), listing the helminths parasitizing

Brazilian snakes.

Forty-six samples of nematodes recovered from

specimens of C. durissus captured in the States of

Mato Grosso, Minas Gerais, Pará, Paraná, Rio de

Janeiro and São Paulo were studied. Parasites were

either collected from animals found dead in nature,

or from those captured during the flood of the

Represa Itaipu Binacional (Binational Itaipu Dam),

in the State of Paraná and that died before the

donation for institutional maintenance for research

and/or anti-ophidic serum production; some

samples derived from contaminated feces or from

regurgitation of some specimens that have died

under captivity in the Instituto de Biologia do

Exercito, IBEx (Army Institute of Biology) in the

city of Rio de Janeiro, that is an institution

registered and licensed by the IBAMA, the

Instituto Brasileiro do Meio Ambiente e dos

Recursos Naturais Renováveis (Brazilian Institute

of the Environment and Natural Renewable

Resources) to develop specific scientific research

activities and to produce hyper immune equine

plasma. Also, other samples recovered from

rattlesnakes and previously deposited in the

Helminthological Collection of the Oswaldo Cruz

Institute (CHIOC) were examined.

Captivity conditions at the IBEx: snakes are

maintained to supply the Fundação Nacional de

Saúde (National Health Foundation) with

antiophidic sera. At the time they come from

nature, snakes are submitted to a quarantine period

to be evaluated for sex, coprological examinations

and other procedures to determine their health

conditions to improve their survival under

captivity.

Concomitantly, the contamination with parasites

and other pathogens from the other already

maintained specimens is avoided. Snakes are kept

in plastic or polypropylene boxes with corrugated

paper bedding and are weekly fed on mice (Mus

musculus Linnaeus, 1758) in an amount that

represents 10% of the animal weight and water is

available ad libidum. In despite of the taken

actions, some specimens do not adapt to the new

conditions and die, to be further submitted to

necropsy and investigated for parasites. Nematodes

studied here were already fixed and kept as wet

material in different solutions: 70 ethanol GL, AFA

(93% ethanol 70 GL; 5% formaldehyde, 2%

glacial acetic acid), 10% formalin or ethanol with

glycerin. Nematodes were dehydrated in a crescent

o o

alcoholic series (70 GL-100 GL), clarified in

acetic acid and phenol and preserved as whole

mounts in balsam and beechwood creosote, 1:3,

respectively.Some specimens were clarified in

glycerin for the en face cross sections, in

accordance with the methodology of Anderson

(1968). Depending on the necessity, some females

were dissected on Petri dishes with paraffin,

according to Travassos (1950) for the counting of

uterine branches.

Figures were obtained with a camera lucida

connected to bright-field Zeiss or Olympus

microscopes. Measurements are in millimeters

(mm) and range appears in parentheses. The

studied samples were deposited in the CHIOC.

Nematodes of Crotalus

Pinto et al.

MATERIALS AND METHODS

138

papillae, an unpaired papilla near the cloacal

opening; the number of post-cloacal papillae varies

from five to six pairs. Females: didelphic,

opistodelphic, oviparous. Vulvar opening located

at the middle-third of the body, frequently anterior

to the half of its total length. From the vulva, the

ovijector (vagina vera) reaches an undivided

portion of the uterus from which two straight

uterine branches arise. Ovaries sinuous, not

reaching the vulvar level. Eggs sub-spherical,

0.061-0.076 long, 0.057-0.051 wide. Tail long,

conical, without mucron.

Sites of infection: esophagus, stomach; localities:

Itaipu Binational Reserve, Foz do Iguaçu, Brazil-

Paraguay border, State of Paraná (24º05'45''S,

54º35'07”W), Valença, State of Rio de Janeiro,

(22º14'44''S, 43º42'01''W), São João Del Rey, State

of Minas Gerais (21º08'00''S, 44º15'40''W);

deposited samples: CHIOC: 35326, 35336, 35337,

35333, 35343, 35344, 36487 a-e, 36488 (a-c),

36489, 36490 (a-c), 36492 a-e, 36493 (a-b).

Remarks: The species Ophidascaris travassosi

Vaz, 1938 and O. sprenti Araujo, 1969, were

considered synonyms of O. arndti by Sprent

(1988). This proposition was overlooked by

Vicente et al. (1993).

Ophidascaris durissus Panizzutti, Santos,

Vicente, Muniz-Pereira & Pinto, 2003

(Figs 8-14)

Morphometrics based on eighteen specimens, nine

males, nine females. Males 60.8 (52-68) long, 0.67

(0.61-0.76) wide; females 67.8 (56-93) long, 0.70

(0.56-0.83) wide. General: mouth with three lips

with dentigerous ridges extending to the inner

border; the dorsal lip presents two large papillae

and the latero-ventral possess one papilla each.

Interlabia absent. Esophagus club-shaped.

Esophageal ventriculus and intestinal cecum

absent. Males: with subequal spicules, alate, 2.53

(2.48-2.90) long. Gubernaculum absent. Caudal

alae narrow. Seventy pairs of pre-cloacal papillae,

one pair ad-cloacal and six pairs post-cloacal.

Females: didelphic, opistodelphic and oviparous.

st nd

Vulvar opening situated between the 1 and 2 third

of middle body. From the vulva a short ovijector

joins an undivided portion of the uterus, from

which two uterine branches arise. Eggs sub-

spherical, 0.05-0.07 long, 0.068-0.084 wide. Tail

conical.

Investigated snakes were parasitized only with

nematodes. A total amount of 46 samples were

studied. Approximately, 80% were represented by

ascaridoids distributed among the Ophidascaris

Baylis, 1920 (50%), Hexametra Travassos, 1920

(30%) and Travassosascaris Sprent, 1978 (20%).

The remaining 20% of the total amount of samples

consisted of specimens included in Hastospiculum

Skrjabin, 1923, Kalicephalus Molin, 1861 and

Physalopera Rudolphi, 1819, with 6.6%, each. At

first sight, ascaridoids from snakes are very much

alike; curiously, their prior identification on the

basis of the nature of the hosts only, in the case the

ophidians, has frequently been adopted by those

not so well acquainted with the morphology of

nematodes. This fact alone, has most of the times,

induced to the general and erroneous nomination of

Ophidascaris sensu lato for different species,

included in Hexametra, Ophidascaris, Polydelphis

Baylis, 1920 and Travassosascaris; thus, efforts

have to be made so that apical views of buccal

structures of the ascaridoid nematodes can be

obtained, whenever possible, together with the

analysis of other morphological distinguishing

characters, aiming at an accurate generic/specific

diagnosis of the worms.

Ascaridoidea

Ascarididae Baird, 1853

Ophidascaris arndti Sprehn, 1929

(= Ophidascaris travassosi Vaz, 1938, O. sprenti

Araujo, 1969)

(Figs 1-7)

Morphometrics based on sixteen specimens, nine

males, seven females. Males 56.6 (47-64) long,

0.63 (0.52-0.75) wide; females 68.9 (64-77) long,

0.62 (0.50-0.81) wide. General: mouth provided

with three quadrangular lips with thin dentigerous

ridges on the inner border; interlabia present. A

large papilla together with another small, are

observed on each ventro-lateral lip; on the dorsal

lip there are two large papillae. Esophagus club-

shaped, esophageal ventriculus and intestinal

cecum absent. Males: with subequal spicules with

short alae, 2.1 (1.89-2.38) long, gubernaculum

absent. Caudal alae reduced; terminal caudal

mucron present. Thirty-six pairs of pre-cloacal

RESULTS

139

Neotrop. Helminthol., 4(2), 2010

0.76 (0.62-0.93) wide. General: mouth with three

quadrangular lips, 0.15 long, 0.17 wide showing

dentigerous ridges on the inner border; interlabia

short. One prominent labial papilla is present on

each dorso-lateral lip; dorsal lip with two papillae.

Esophagus club-shaped. Ventriculus and intestinal

cecum absent. Males: spicules equal, with narrow

alae, 0.76 (0.48-0.91) long. Gubernaculum and

caudal alae absent, tail with mucron, presenting up

to forty pairs of pre-cloacal papillae and three post-

cloacal. Females: didelphic, opistodelphic and

oviparous. Vulva slit-shaped, located at the

posterior third of the body. The ovijector joins the

undivided portion of the uterus, from which arise

two uterine branches that run straight to the origin

of coiled ovaries not reaching the vulvar region.

Eggs sub-spherical, 0.07-0.084 long, 0.056-0.07

long. Tail short and blunt. Mucron absent.

Site of infection: stomach; locality: Itaipu

Binational Reserve, Foz do Iguaçu, Brazil-

Paraguay border State of Paraná; deposited

samples: CHIOC: 34687, 34937, 34937 b-f.

Remarks: Considering that O. durissus is the only

Brazilian species of the genus devoid of interlabia,

the status of this species should be further

reevaluated, taking into account that the

absence/presence of interlabia is a generic

character and may not be regarded as an isolate

specific variation among the representatives of

Ophidascaris.

Ophidascaris sicki Freitas, 1951

(Figs 15-21)

Morphometrics based on seven specimens, four

males and three females. Males 63.25 (55-78) long,

0.71 (0.67-0.75) wide; females 70 (52-86) long,

140

Nematodes of Crotalus

Pinto et al.

Figures 8-14. Ophidascaris durissus. Fig. 8. Anterior of

male, lateral view. Fig. 9. Head, en face view. Fig. 10.

Posterior of male, ventral view. Fig. 11. Vulva, vagina,

ovijector and uterine bifurcation, lateral view. Fig. 12.

Posterior of male, ventral view. Fig. 13. Posterior of

male, lateral view. Fig. 14. Male, posterior extremity,

lateral view. Bar (common to Figs 8-14) = 0.7 in Figs 8,

11, 12; 0.08 in Fig. 9; 0.5 in Figs 10, 12, 13 (in mm).

Figures 1-7. Ophidascaris arndti. Fig. 1. Anterior of

male, dorsal view. Fig. 2. Head, en face view. Fig. 3.

Vulva, vagina, ovijector and uterine bifurcation, lateral

view. Fig. 4, Female genitalia (partial), frontal view. Fig.

5. Posterior of male, lateral view. Fig. 6. Posterior of

male, ventral view. Fig. 7. Posterior of female, lateral

view. Bar (common to Figs 1-7) = 0.04 in Fig. 2; 0.4 in

Figs 1, 3; 0.5 in Figs 4, 5; 0.2 in Figs 6, 7 (in mm).

Site of infection: esophagus; locality: Itaipu

Binational Reserve, Foz do Iguaçu, Brazil-

Paraguay border, State of Paraná); deposited

sample: CHIOC: 34.779 a-f.

Type material of O. sicki, recovered from

Waglerophis merremii (Wagler, 1824) [=Xenodon

merremii] captured in Xavantina, State of Mato

Grosso (14º40'09''S, 52º20'09''W), previously

deposited was revised (CHIOC no. 19120, 19121,

19122, 19123).

Remarks: This is the first occurrence of the species

parasitizing specimens of Crotalus durissus, since,

as informed, O. sicki had been reported only from

the Wagler's snake in Brazil.

Ophidascaris tuberculatum Siqueira, Panizzutti,

Muniz-Pereira & Pinto, 2005

(Figs 22-28)

Morphometrics based on eleven specimens, four

males and seven females. Males 62 (40-70) long,

0.85 (0.77-0.94) wide. Females 87 (74-132) long,

1.37 (0.94-1.53) wide. General: mouth with three

slightly quadrangular lips, with well developed

dentigerous ridges along the internal border and

interlabia short, reaching about 1/3 of the lips in

length. Esophagus club-shaped. Ventriculus and

Figures 22-28. Ophidascaris tuberculatum. Fig. 22.

Anterior of female, dorsal view. Fig. 23. Vulva, vagina,

ovijector and uterine bifurcation, lateral view. Fig. 24.

Male, anterior extremity, dorsal view. Fig. 25. Female,

posterior extremity, lateral view. Fig. 26. Male, posterior

extremity, ventral view. Fig. 27. Posterior of male,

lateral view. Fig. 28. Detail of male posterior extremity,

ventral view. Bar (common to Figs 22-28) = 0.3 in Figs

22, 23; 0.09 in Fig. 24; 0.4 in Figs 25, 26, 27; 0.25 in Fig.

28 (in mm).

Figures 15-21. Ophidascaris sicki. Fig. 15. Anterior of

male, ventral view. Fig. 16. Head, en face view. Fig. 17.

Female, anterior extremity, ventral view. Fig. 18.

Posterior of male, ventral view. Fig. 19. Posterior of

male, lateral view. Fig. 20. Male, anterior extremity,

dorsal view. Fig. 21. Female, posterior extremity, ventral

view. Bar (common to Figs 15-21) = 0.5 in Fig. 15; 0.04

in Fig. 16; 0.4 in Figs 17, 20; 0.2 in Figs 18, 19, 21 (in

mm).

Neotrop. Helminthol., 4(2), 2010

141

intestinal cecum absent. Males: with subequal

spicules and narrow alae, 2.85 (2.63- 2.87) long.

Gubernaculum and caudal alae absent. Twenty-six

pairs of pre-cloacal papillae, one pair ad-cloacal,

five pairs post-cloacal and one umpaired papilla.

Tail long, conical, presenting a conspicuous

mucron. Females: didelphic, opitodelphic,

oviparous. Vulva slit-shaped, either in the middle

third or in the anterior third of the body. From the

vulva, extends a sinuous ovijector to join the

undivided uterine portion, from which arise two

uterine branches to reach the coiled ovaries. Eggs

sub-spherical, 0.085 long, 0.070 wide. Tail with a

prominent muscular post-anal protuberance, easily

observed that appears as a tubercle.

Site of infection: stomach; locality: State of Minas

Gerais (Municipality not informed); samples

deposited: CHIOC: 8132, 36494 (a-d).

Remarks: Crotalus durissus is a new host record for

the species previously described by Siqueira et al.

(2005) parasitizing specimens of Bothrops

jararaca Wied, 1832.

Ophidascaris sp.

Sites of infection: esophagus, stomach, body cavity

(?), feces; localities: Itaipu Binational Reserve, Foz

do Iguaçu, Brazil-Paraguay border State of Paraná,

PR, Valença, State of Rio de Janeiro, Três

Corações, State of Minas Gerais (21º58'10''S,

45º22'20''W); deposited samples: CHIOC: 34894,

34897, 35330, 35334, 35338.

Hexametra boddaertii (Baird, 1860) Kreis, 1944

(Figs 29-34)

Morphometrics based on thirty-six specimens,

thirteen males, twenty-three females. Males 86

Figures 35-39. Kalicephalus inermis macrovulvus. Fig.

35. Dorsal ray of the copulatory bursa, ventral view. Fig.

36. Anterior of female, ventral view. Fig. 37. Female,

posterior extremity, lateral view. Fig. 38. Posterior of

male, lateral view. Fig. 39. Vulvar region, lateral view.

Bar (common to Figs 35-39) = 0.08 in Fig. 35; 0.1 in Figs

36-39 (in mm)

Figures 29-34. Hexametra boddaertii. Fig. 29. Anterior

of male, showing the intestinal cecum (arrow), ventral

view. Fig. 30. Head, en face view. Fig. 31. Vulva, vagina,

ovijector and the six uterine branches, frontal view. Fig.

32. Esophageal-intestine junction, with the intestinal

cecum (arrow), dorsal view. Fig. 33. Posterior of male,

ventral view. Fig. 34. Male, posterior extremity, lateral

view. Bar (common to Figs 36-41) = 0.7 in Fig. 29; 0.05

in Fig. 30; 0.3 in Figs 31, 32; 0.2 in Figs 33, 34 (in mm).

Nematodes of Crotalus

Pinto et al.

142

(66-108) long, 1.0 (0.71-1.51) wide; females 123

(72-173) long, 1.17 (0.79-2.1) wide. General:

mouth with three lips, dentigerous ridges extending

along anterior border of lip and round anterior

angles of lip to level of double papillae; interlabia

absent. Labial papillae consisting of double

papillae on each ventro-lateral lip and two on the

dorsal lip. Esophagus club-shaped. Ventriculus

absent, intestinal cecum present or absent. Males:

with subequal spicules, with narrow alae, 1.29

(0.98-1.58) long. Tail almost rounded, ending in a

tip presenting an inconspicuous mucron. A variable

number of pre-cloacal papillae, one pair ad-cloacal

and two to three pairs post-cloacal. Females:

opistodelphic, oviparous. Vulvar aperture slit-like,

at the end of the middle third or at the posterior third

of the body From the vulva, extends a sinuous

ovijector to join the undivided uterine portion, from

which arise six uterine branches to reach the coiled

ovaries that extend to the vulvar region. Eggs sub-

spherical, 0.080-0.086 long, 0.070-0.080 wide.

Sites of infection: intestine, body cavity, stomach;

localities: Foz do Iguaçu, State of Paraná

(municipality not informed), State of São Paulo

(municipality not informed), Valença, State of Rio

de Janeiro; deposited samples CHIOC: 8179,

34685, 34780 a-e, 34781 a-g, 34810, 34895, 34896,

34899, 35327, 35329, 35331, 36192, 36194 a-b,

36191 a-b.

Travassosascaris araujoi ((Schneider, 1866)

Sprent, 1978

(Figs 44, 45)

Morphometrics based on a single immature female

specimen. Body 110 long, 1.06 wide. Mouth with

three quadrangular lips, shallow interlabia present;

dentigerous ridge extending around whole border

of lips to posterior corner. Vulva without salient

lips, vagina short, extending posteriorly to join

undivided uterus, leading to four uterine brnches.

Tail with conical tip, without mucron, phasmids

near tip.

Site of infection: stomach; locality: Valença, State

of Rio de Janeiro; deposited sample CHIOC:

36491.

Remarks: Data reported by Sprent (1978) and

Araújo (1969 a, b) on the material previously

studied by Schneider (1866), reinforce the

statement that ascaridid females that occur in

specimens of Crotalus durissus and that present

more than two uterine branches are included in the

genera Hexametra Travassos, 1920 (6 uterine

branches and absence of interlabia) Polydelphis

Dujardin, 1845 (4 uterine branches and absence of

interlabia) and Travassosascaris Sprent, 1978 (4

uterine branches and presence of interlabia).

Diaphanocephaloidea

Diaphanocephalidae Travassos, 1920

Kalicephalus inermis macrovulvus Caballero,

1954

(Figs 35-39)

Morphometrics based on five specimens, two

males and three females. Males 12.94 long, 0.32

wide; females 13.94 (12.40-16.32) long, 0.39

(0.33-0.49) wide. General: anterior extremity

slightly bent. Buccal capsule 0.22 (0.16-0.23) long,

0.25 (0.17-0.31) wide. Esophagus club-shaped

with a posterior bulb, 0.42 long, 0.22 wide. Teeth

absent. Males: with equal and slender spicules,

0.84 (0.81-0.86) long. Gubernaculum present.

Copulatory bursa broad and oblique. Dorsal rays

somewhat close to each other and splitting at the

extremities (“V” pattern). The externo-lateral rays

are short and with rounded tips. Females:

amphidelphic, vulva with salient lips, followed by

divergent muscular ovijectors. Eggs 0.065-0.072

long, 0.036-0.039 wide. Tail elongate with rounded

tip.

Site of infection: stomach; locality: Peixoto de

Azevedo, State of Mato Grosso (10º13'12''S,

54º58'08''W); deposited samples: CHIOC: 35341,

35342.

Remarks: According to Schad (1962), in the

revision of the genus Kalicephalus Molin, 1861,

there is a great intra-specific variability and,

conversely, also an inter-specific homogeneity

among the species of this complex group. In order

to properly identify the samples presently studied

as K. inermis Molin, 1861 some reliable and well

defined characters have been considered, such as

the absence of the corona radiata and the buccal

teeth, amphidelphic females, males with equal and

long spicules and the pattern of rays of the caudal

bursa. In despite of the existence of morphological

differences among the representatives of the

“inermis group”, K. inermis inermis Molin, 1861,

K. inermis coronellae Ortlep, 1923 e K. inermis

macrovulvus Caballero, 1954, that were considered

only as geographic groups by Schad (1962), the

samples studied here were identified to K. inermis

Neotrop. Helminthol., 4(2), 2010

143

macrovulvus. The identification was mainly based

on the “V” pattern of bursal rays, on the aspect of

the female tail that is narrow, elongate, with round

tip, and also on the anterior portion of the buccal

capsule, varying in shape from pointed to straight.

Kalicephalus sp.

Infection site: stomach; locality: Peixoto de

Azevedo, State of Mato Grosso; deposited

samples: CHIOC: 35339, 35340.

Physalopteroidea

Physalopteridae Leiper, 1908

Physaloptera sp.

(Figs 40-42)

Morphometrics based on two female specimens.

Body 106.2 (104.6- 108.9) long, 0.55 wide. Mouth

with two lateral, simple triangular lips, each

bearing either apically or internally, a variable

number of teeth and external papillae. Cuticle

generally bent over the lips, forming a huge

cephalic collar. Esophagus with an anterior

muscular portion, followed by a posterior

glandular, 6.75 (5.9-7.6) in total length and 0.5 in

width. Vulva opening at the posterior portion of the

body. Tail slender.

Site of infection: not informed [frequently in the

stomach]; locality: Foz do Iguaçu, State of Paraná;

deposited samples: CHIOC: 35100, 36195 a-d.

Remarks: This is the first report of a physalopterid

worm in C. terrificus in Brazil. Probably, this

species could be identified to Physaloptera

obtusissima Molin, 1860, recovered from

specimens of Bothrops jararaca (Wied, 1824), the

common jararaca, and Cloelia sp., known as

mussurana in Brazil. The other species of the genus

that occur in Brazilian snakes are: P. monodens

from the stomach of Constrictor constrictor (L.,

1758), the red-tailed boa, P. liophis Vicente &

Santos, 1974, from the stomach of specimens of

Liophis miliaris (L., 1758), the common water

snake, and Physaloptera sp. from the stomach of

specimens of Wagleropsis merremii (Wagler, 1824)

[=Xenodon merremii] the Wagler's snake, and

Phylodrias sp., the green snake. Considering that

females of Physaloptera share many common

characters, the unavailability of male specimens

did not permit a reliable specific diagnosis of the

presently investigated samples.

Diplotriaenoidea

Diplotriaenidae Anderson, 1958

Hastospiculum sp.

(Fig. 43)

Morphometrics unavailable. An overall

description, based on broken females, refers to the

mouth with two outstanding lip-like chitinous

processes in each side of the aperture. Esophagus

clearly divided into two muscular portions, the

anterior short and narrow, the posterior broad and

much longer. Vulva inconspicuous, located near the

end of the anterior esophageal portion. Ovejictor

stout and wide, ending in a single portion of the

uterus that further bifurcates into two branches.

Amphidelphic, oviparous, with embryonated eggs

in utero. Anus terminal.

Site of infection: connective tissue; locality:

Cachimbo, State of Pará (09º20'11''S,

Figures 40-45. Physaloptera sp. Fig. 40. Female,

anterior extremity, ventral view. Fig. 41. Head, en face

view. Fig. 42. Female, posterior extremity, lateral view.

Hastospiculum sp. Fig. 43. Anterior extremity of female,

with vulvar aperture (arrow), lateral view.

Travassosascaris araujoi. Fig. 44. Female, posterior

extremity, lateral view. Fig. 45. Vulva, vagina, ovijector

and uterine bifurcation, lateral view. Bar (common to

Figs 40-45) = 0.4 in Fig. 40; 0.01 in Figs 41, 42, 44; 1.1

in Fig. 43; 0.15 in Fig. 45 (in mm).

Nematodes of Crotalus

Pinto et al.

144

The major restricting aspect of the present study

was mainly related to the source and amount of

investigated rattlesnakes. Considering that animals

were taken from nature into captivity by donators,

the tracking of the proper origin of the specimens

was sometimes unsuccessful. Also, the number of

samples was not statistically standardized taking

into account that rattlesnakes were captured

randomly mostly by the farmers during sowing and

harvest seasons.

Specimens of C. durissus are animals that assumed

great importance circa 1901, when Vital Brazil

began with the studies related to ophidic venoms,

already referring to the higher toxicity of the

crotalic venom, when compared to others and the

necessity in obtaining specific sera.

54º57'36''W); deposited samples: CHIOC: 21647,

36495.

Remarks: Considering that no males were

available, only the generic diagnosis was obtained.

Two other species of the genus are referred in

Brazil: Hastospiculum digiticaudum Freitas, 1956,

from the body cavity of specimens of Philodrias

aestivus Dumeril, Bibron & Dumeril, 1854

captured in the State of Rio de Janeiro and H.

onchocercum Chitwood, 1932, from Crotalus

durissus terrificus (Laurenti, 1768), in Recife,

State of Pernambuco (Vicente et al. 1993).

Final remarks: Other nematode species not found

in the present study, and referred by Vicente et al.

(1993), parasitizing Brazilian specimens of C.

durissus are Ascaridia flexuosa (Schneider, 1866)

Railliet & Henry, 1914, Capillaria crotali

(Rudolphi, 1819) Travassos, 1915, Hastospiculum

onchocercum Chitwood, 1932, Kalicephalus

costatus costatus (Rudolphi, 1819) Yorke &

Maplestone, 1926, K. inermis inermis (Molin,

1861) and Ophidascaris trichuriformis Vaz, 1935.

Except for the pentastomid Cephalobaena

tetrapoda Heimans, 1922 cited by Rego, (1983)

from the lungs of Crotalus terrificus (Laurenti,

1 7 5 8 ) a n d t h e d i g e n e t i c t r e m a t o d e

Ophiodiplostomum spectabile Dubois, 1936, from

the intestine of the same host, referred by Rosselini

(2007), there are no reports of other metazoan

endoparasites infecting rattlesnakes in Brazil so far.

DISCUSSION

According to Cardoso (2003), from 1950 to 1980,

when systematical investigations regarding

ophidism were undertaken, mainly in the Brazilian

southeastern region, the official institutes, namely

Butantan, Vital Brazil and Ezequiel Dias and the

private laboratory Syntex do Brasil, were the only

to produce anti-ophidic sera. Until 1985, those sera

were not considered a priority by the National

Immunization Program of the Health Ministry.

Thus, when the private facility finished with its

production in 1983, the public institutions had no

capacity to support the demand for sera in the

country. Following the collapse of sera distribution,

press releases informed the population about the

occurrence of several deaths due to the lack of sera

supplies. Further administrative efforts were made

aiming at the support of the already existing and at

the establishment of new ophidiology centers to

promote the capture, maintenance, reception of the

snakes, training of staff and the identification of

snakes responsible for human accidents. Therefore,

it was necessary to improve the knowledge of the

physiology, behavior and pathologies related to

snakes, taking into account that the production of

sera depends on the venom extracted from these

reptiles maintained in serpentariums and/or animal

houses.

Captive specimens of C. durissus have a

remarkable importance in the development of

pharmacological studies aiming at the isolation of

venom peptides; the required quality and volume of

this venom depend on the health and adaptation of

the animals submitted to the extraction procedure.

It is widely known that under captivity the stress to

which animals are submitted can induce the

settlement of several pathologies, mainly those

related to parasites (Leinz et al. 1989, Santos et al.

2008, Siqueira et al. 2009). The former authors

describe the “Poor Adaptation Syndrome” to the

captivity, as the most important cause of mortality

of snakes in the two first years of imprisonment,

considering that animals develop remarkable

susceptibility to pathogenic agents in this period of

adaptation. Thus, it is necessary to provide

additional data on the helminth fauna of Brazilian

reptiles, in order to permit, among other

approaches, the establishment of prophylactic

procedures, adequate handling and effective

treatment to properly reduce the mortality of

captive animals.

Neotrop. Helminthol., 4(2), 2010

145

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* Correspondence to author/Autor para

correspondencia

Roberto Magalhães Pinto

Laboratório de Helmintos Parasitos de Vertebrados,

Instituto Oswaldo Cruz.

Av. Brasil, 4365, 21040-360 Rio de Janeiro, Brasil

E-mail/correo electrónico:

rmpinto@ioc.fiocruz.br/rmpinto@globo.com

Received November 14, 2010.

Accepted November 28, 2010.

Neotrop. Helminthol., 4(2), 2010

147