Suggested Citation: Magalhães-Pinto, R.; Knoff, M.; Queiroga-Gonçalves, A.; Sanches, M.; Noronha, D. 2009. First report of

Taenia mustelae (Eucestoda, Taeniidae) parasitizing the bushy-tailed olingo, Bassaricyon gabbii (Carnivora,

Procyonidae) in South America with an updated checklist of cestodes from other american procyonid hosts.

Neotropical Helminthology, vol. 3, nº 1, pp. 7-14.

Resumen

Palabras clave: Amazonas - Américas - Bassaricyon gabbii - Cestodos - Chosna pericote - Floresta húmeda -

Infección natural - Procyonidae - Taenia mustelae

Se describe el primer caso de infección natural por el cestodo Taenia mustelae en un ejemplar del prociónido

chosna pericote, Bassaricyon gabbii, procedente de la localidad de Barcelos, Estado do Amazonas, Brasil.

Un inventario de 15 especies de cestodos parásitos de otros hospederos prociónidos en las Américas entre

1958 y 2009 es incluido, con la finalidad de actualizar datos anteriores. En el período considerado, no hay

registros en México y países de América Central. Esta es la primera citación de T. mustelae en América del

Sur y B. gabbii, es un nuevo hospedero para esta especie de cestodo.

Key words: Amazonas - Americas - Taenia mustelae - Bushy-tailed olingo - Cestodes -

Natural infection - Procyonidae - Rain forest - Bassaricyon gabbii

Abstract

The first case of a natural helminth infection with the cestode Taenia mustelae in a specimen of the procyonid

Bassarycion gabbii, the bushy-tailed olingo, from the municipality of Barcelos, State of Amazonas, Brazil is

reported here. A checklist of 15 cestode species parasitizing other procyonid hosts in the Americas, between

1958 and 2009 is included in order to update previous data. In the considered period there are no records in

Mexico and Central America countries. This is the first report of T. mustelae in South America and B. gabbii

is a new host record for this cestode species.

Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz. Av. Brasil, 4365, 21040-900 Rio de Janeiro, Rio de Janeiro, Brasil.

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Research Fellow.

Laboratório de Doenças Parasitárias, Instituto Oswaldo Cruz, Rio de Jsneiro, Brasil.

Instituto Leonidas e Maria Deane, Fiocruz, Manaus, Amazonas, Brasil.

Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) fellow.

Neotrop. Helminthol., 3(1), 2009

2009 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

FIRST REPORT OF TAENIA MUSTELAE (EUCESTODA, TAENIIDAE) PARASITIZING THE

BUSHY-TAILED OLINGO, BASSARICYON GABBII (CARNIVORA, PROCYONIDAE) IN

SOUTH AMERICA WITH AN UPDATED CHECKLIST OF CESTODES FROM OTHER

AMERICAN PROCYONID HOSTS

PRIMER REPORTE DE TAENIA MUSTELAE (EUCESTODA, TAENIIDAE) PARASITANDO

LA CHOSNA PERICOTE, BASSARYCION GABBII (CARNIVORA, PROCIONYDAE), EN SUD

AMÉRICA CON UNA LISTA ACTUALIZADA DE CESTODOS DE OTROS HOSPEDEROS

PROCIÓNIDOS AMERICANOS

1,2* 1 3,4 5 1

Roberto Magalhães Pinto ; Marcelo Knoff ; Alessandra Queiroga Gonçalves ; Magda Sanches ; Dely Noronha

INTRODUCTION

The bushy-tailed olingos (Bassaricyon gabbii

Allen, 1876), have a restricted geographical

distribution, since they are typically found from

Nicaragua to Bolivia, where they are locally

abundant in the latter locality although sparsely

distributed in the western Amazon basin. The bushy-

tailed olingo, is found in evergreen forests, and on

forest edges; they prefer the upper canopy of the

forest and are rarely seen on the ground. Specimens

of B. gabbii are nocturnal and arboreal animals,

found alone or in groups of six, at the most, feeding

together in large fruit trees. Usually, they avoid

kinkajous [Potos flavus (Schreber, 1774)], since the

closely related kinkajous will chase them out of

trees. Because they are nocturnal, olingos do not

compete directly with most primates and feed on

fruits, nectar, flowers, insects, and small vertebrates.

They are primarily frugivores but actively hunt

warm-blooded animals. Five species of the genus

Bassaricyon Allen, 1876, are currently recognized

by most authorities. However, some think that these

five species should be demoted to the rank of

subspecies of a single species. Natives of the

Amazon consider the olingos dangerous and kill

them on sight (Nowak, 1999; Kays, 2000; Pontes &

Chivers, 2002). Natural infections with ecto and

endoparasites of the olingo, B. gabbii are very few

and restricted to the thick Ixodes rubidus Neumann,

1901 and the protozoan Leishmania brasiliensis

panamensis Lainson & Shaw, 1972, both referred in

Panama (Wenzel, 1996, Christensen et al. 1983).

Considering the peculiar geographical distribution,

behavioral, ecological approaches and feeding

habits of the olingos the present report of the first

natural helminth infection in an Amazonian

specimen of B. gabbii with Taenia mustelae Gmelin,

1790, adds important new data to the biology of this

poorly known endangered group of hosts.

A single cestode worm was recovered from the

small intestine of one specimen of the olingo,

Bassaricyon gabbii Allen, 1876, killed on March,

10, 2001, in the settlement Sitio da Mamãe,

Japomeri waterway, Padauiri River, Barcelos

o o

municipality, (00 20'51”N, 64 00'28”W),

Amazonas, Brazil. The olingo was shot by a local

hunter and immediately after, transferred to one of

the authors (A.Q.G.) to be investigated for

helminths during an official fieldwork. The animal

was identified and deposited in the National

Museum of Rio de Janeiro, Brazil, after the carcass

was prepared by taxidermists. Worm briefly rinsed

alive in a 0.85% NaCl solution, was fixed in hot

AFA (70º GL ethanol, 93%; formaldehyde, 5%;

glacial acetic acid, 2%) and stored as wet material

in the same solution. The cestode was further

dehydrated in an ethanol series, stained with

Langeron's carmine clarified in phenol and

preserved as whole mount in Canada balsam.

Classification of the host follows Novack (1999)

and that of the cestode, is in accordance with Khalil

et al. (1994) and Loos-Frank (2000). Figures were

obtained with a drawing tube connected to a

bright-field BX41 Olympus microscope.

Measurements are in micrometers (µm) unless

otherwise indicated. Shooting and necropsy of the

host specimen were authorized by the IBAMA

(Instituto Brasileiro de Meio Ambiente e Recursos

Renováveis) [Brazilian Institute of Environment

and Renewable Resources], Brazil, process nº

02001.002659/97-02, permits nº 056/2000 –

DIFAS/DIREC (validity 01/04/00 to 01/04/01)

and nº 012/2002-COEFA (validity 22/01/02 to

22/04/02). NHR and NGD refer to New Host

Record and New Geographical Distribution,

respectively. The cestode was deposited in the

Helminthological Collection of the Oswaldo Cruz

Institute (CHIOC), Rio de Janeiro, Brazil.

Taenia mustelae Gmelin, 1790 (= T. tenuicollis

Rudolphi, 1819) (Figs. 1-3)

Description based on one adult, mounted and

measured specimen. Strobila 8.11 mm long, with

numerous proglottids, wider than longer, largest

proglottid 175.1 long, 333.6 wide. Scolex 260 long,

360 wide, with 56 hooks in two rows of 28 hooks

each. Large hooks 22.5-23.7 (23.4) long, 22.5 (22.5)

wide (base); small hooks 18.7-20 (19.7) long, 18.7-

20 (19.4) wide (base). Rostellum everted 97.5 long,

widest at the level of rostellar hooks, 97.5-107.5

long. Rostellum receptacle 172.5 long, 100 wide.

Suckers 92.5-95 (93.7) long, 90- 92.5 (91.2) wide.

MATERIAL AND METHODS

Taenia mustelae in Brazilian Bassaricyon gabbi Magalhães Pinto et al.

RESULTS

Mature proglottids, 58.4-175.1 (132.2) long, 191.8-

333.6 (132.2-260.3) wide. Large, protruding,

irregularly alternating genital cones (pores)

containing the conspicuous genital atrium at the

lateral margin of mature proglottids, anterior to the

middle portion. Testes rounded, extending to the

middle of the ovary until the anterior margin of the

proglottid 80-120 in number, 8.3-16.7 (12.5) in

diameter. Cirrus pouch (in mature proglottids), 83.4-

120 (104.7) long, 25-41.7 (41.3) wide. Ovary

bilobed, of similar size, at posterior region of

proglottid. Vitellaria imediatelly posterior to the

ovary. Vagina opening posterior to the cirrus pouch;

no vaginal sphincter before genital atrium. Uterus

saccular, elongate. Gravid proglottids absent.

Taxonomic summary

Host: Bassaricyon gabbii (NHR).

Site of infection: intestine.

Locality: Sítio da Mamãe, Japomeri waterway,

Padauiri River, Barcelos, Amazonas, Brazil, South

America (NGD).

Specimen deposited: CHIOC n. 37.227 (whole

mount).

The following data on cestodes infecting other

procyonid hosts in the Americas complement those

of Yamaguti (1959). Parasites appear in alphabetical

order followed by host (s), locality (ies) and

bibliographical reference (s).

Atriotaenia procyonis (Chandler, 1942) Gallati,

1956 (= Oochoristica procyonis Chandler, 1942),

Procyon lotor (L., 1758), Arkansas, South Dakota,

Florida, Illinois, Georgia, Kentucky, North

Carolina, Kansas, Ohio, South Carolina, Tennessee,

Texas, Virginia, U.S.A., (Gallati, 1959; Jordan &

Hayes, 1959; Harkema & Miller, 1964; Boddicker

& Progulske, 1968; Barnstable & Dyer, 1974;

Bafundo et al., 1980; Schaffer et al., 1981; Smith et

al., 1985; Snyder & Fitzgerald, 1985; Cole & Shoop

1987; Robel et al., 1989; Richardson et al., 1992;

Kelley & Norman 2008; Kresta et al., 2009),

Procyon lotor hirtus Nelson & Goldman, 1930,

Saskatchewan, Canada (Hoberg & McGee, 1982),

Procyon lotor litoreus Nelson & Goldman, 1930, St.

Catherines Island, Georgia, U.S.A., (Price &

Harman, 1983), raccoon [unindentified], Georgia,

U.S.A (Babero & Shepperson, 1958); Atriotaenia

sandgroundi (Baer, 1935), Nasua nasua (L., 1758),

Brazil (Vieira et al. 2008); Cestoda (unindentified),

Procyon lotor, Maryland and other states (not

named), U.S.A (Clark & Herman, 1959),

Metropolitan Toronto Zoo, Canada ( Cranfield et al.,

1984); Diphyllobothrium trinitatis (Cameron,

1936), Procyon cancrivorus (G. Cuvier, 1798), São

Paulo, Brazil (Vieira et al., 2008);

Diphyllobothrium sp., Procyon cancrivorus,

Argentina, Rio de Janeiro, Brazil (Martinez et al.,

2000, Vieira et al., 2008); Mesocestoides lineatus

(Goeze, 1782) Railliet, 1893, raccoon

[unidentified], Georgia, U.S.A (Babero &

Shepperson, 1958); Mesocestoides variabilis

Mueller, 1927, Procyon lotor, Florida, Georgia,

Kentucky, North Carolina, South Carolina,

Tennessee, Texas, Virginia, Illinois, U.S.A

(Harkema & Miller, 1964; Bafundo et al., 1980;

Schaffer et al., 1981; Smith et al., 1985; Cole &

Shoop, 1987; Birch et al., 1994); Mesocestoides

spp., Procyon lotor, Bassariscus astutus

(Lichtenstein, 1830) Coues, 1887, Arkansas,

Illinois, Kansas, Texas, U.S.A (Boddicker &

Progulske, 1968; Pence & Willis, 1978; Snyder &

Fitzgerald, 1985; Robel et al., 1989; Richardson et

al., 1992; Kelley & Horner, 2008); Procercoid

(unidentified), Procyon lotor, British Columbia,

Canada, (Ching et al., 2000), Spargana (Spirometra

mansonoides), Procyon lotor, Florida, Texas,

Virginia, U.S.A (Schaffer et al., 1981), Spirometra

mansonoides (Mueller, 1935), Procyon lotor,

Florida, U.S.A (Harkema & Miller, 1964); Taenia

crassipora Rudolphi, 1819, Nasua nasua, Brazil

(Vieira et al., 2008); Taenia martis (Zeder, 1803)

Wahl, 1967, Bassariscus astutus, Texas, U.S.A.

(Pence & Willis, 1978); Taenia pencei Rausch,

2003, Bassariscus astutus, Texas, U.S.A (Raush,

2003); Taenia pisiformis Bloch, 1780, Procyon

lotor, Texas, U.S.A (Kelley & Horner, 2008), Taenia

taeniformis (Batsch, 1786) Wolffügel, 1911

[=Hydatigera taeniformis (Batsch, 1786) Lamark,

1816], Procyon l. lotor, South Dakota, U.S.A

(Boddicker & Progulske, 1968).

Overstreet (1970) in a study of the nematode

Baylisascaris procyonis (Stefánsky and

Zarkowiski, 1951) from the Colombian kinkajou

(P. flavus) refers to the parasitism of a specimen of

B. gabbii with a single worm of B. procyonis with

no information related to the geographical location

of the host and the nature of the infection with the

statement that “…A single male worm, identical to

those from the kinkajou, was obtained from a

bushy-tailed olingo, B. gabbii, after it was fed

infective eggs from the worms of the kinkajou. It is

not known if this infection was natural or

DISCUSSION

Neotrop. Helminthol., 3(1), 2009

experimental.” Kazacos (2001) referring to B.

procyonis and related species only reproduces data

after Overstreet (1970) in a table, with no further

comments. Thus, taking these facts into account

and also considering the impossibility to check and

enlighten those previous data, it is to be assumed

that the first confirmed natural helminth infection

represented by the cestode T. mustelae in the

bushy-tailed olingo is reported now. The early

attempt to catalogue cestodes infecting vertebrate

hosts in Brazil was that of Travassos (1965); these

species had already been referred by Yamaguti

(1959) and those reported in wild carnivore

mammals from Brazil were recently surveyed by

Vieira et al. (2008). In the present paper, data on

cestode species recovered from Procyonidae hosts

in the Americas is updated. Most of the references

in the checklist are related to cestodes parasitizing

specimens of raccoons (P. lotor) in the U.S.A. and,

interestingly, the animals, except for those from

South Dakota (Boddicker & Proglske, 1968), were

captured in states sharing common or close

political borders, namely Florida, Georgia, South

Carolina, North Carolina, Virginia, Maryland,

Kentucky, Ohio, Illinois, Tennessee, Kansas,

Arkansas, and Texas, thus explaining the

occurrence of the same cestode species in these

neighboring areas. It was suggested that the low

diversity of the helminth fauna as well as the low

worm burdens recovered from raccoons in Canada

were due to unsuitable conditions affecting the life

cycles of helminths that commonly parasite

specimens of these hosts elsewhere (Hoberg &

McGee, 1982). Miller (1992) summarized the

literature on helminths occurring in specimens of

P. lotor in the southeastern United States,

presenting a dichotomous key to some common

forms in that area. Briefly, in the present survey of

28 cases related to cestode infections occurring in

procyonid hosts in the Americas, specimens of P.

lotor (subspecies not considered) appeared in 20

cases (16 in the U.S.A, 04 in Canada), P.

cancrivorus in 03 (02 in Brazil, 01 in Argentina),

B. astutus in 02 (U.S.A), N. nasua in 02 (Brazil),

and raccoons (unidentified) in 01 (U.S.A). In the

period that has been taken into account (51 years),

there are no records of cestodes parasitizing

procyonids in Mexico as well as in Central

America countries.

The life-cycle of T. mustelae was previously

studied and several definitive and intermediate

hosts from Europe, North America and Japan have

been reported. The former are represented by

species of the genera Martes Pinel, 1792 and

Mustela Linnaeus, 1758 whereas the latter by a

wide range of rodents and lagomorphs (Freeman,

1956, Dollfus 1961, Iwaki et al., 1996, Loos-

Frank, 2000). Mustelids occurring in the Brazilian

Amazon, are represented by the Amazon weasel

Mustela africana Desmarest, the tayara Eira

barbara (L.), the grison Galictis vitatta

(Schreber), the river otter Lontra longicaudis

(Olfers) and the giant otter Pteronura brasiliensis

(Gmelin). Considering that olingos feed on small

vertebrates (Kays, 2000) it is to be supposed that

they ingest some small rodents that can act as

intermediate hosts for T. mustelae.

Taking into account that mainly in the last three

decades unauthorized necropsies of wild animals

are strongly discouraged worldwide, it seems more

likely that T. mustelae so far investigated may be

infecting other South American hosts; nevertheless,

under the above circumstances, these occurrences

have probably remained unreported to date.

Morphological data on the specimen studied here

are in agreement with previous descriptions of this

species, mainly considering the number, and length

of the large and small rostellar hooks that in the

present studied sample was of 56, 22.5-23.7 and

18.7-20, respectively, when compared to early data

on other specimens of T. mustelae, with referred

values of 22-74, 12-38 and 12-38, respectively;

dimensions of internal structures of male and female

apparatus were also taken into consideration for the

proper specific identification (Verster, 1969; Loos-

Frank, 2000). Although small variations related to

the diameter of testes and smaller width of cirrus

pouches were observed in our single specimen

devoid of gravid proglottids, the species was easily

identified to T. mustelae that is referred for the first

time in South America and in a new host. Specimens

of T. mustelae are the only to share rostelar hooks of

this size, since Taenia brachiachanta Baer & Fain,

1951, parasitizing the mustelid Poecilogale

albinucha (Gray, 1864) [White naped weasel], from

the Republic of South Africa, although presenting

rostellar hooks with similar dimensions is to be

regarded as a junior synonym or a subspecies of T.

mustelae in accordance with Verster.

Taenia mustelae in Brazilian Bassaricyon gabbi Magalhães Pinto et al.

Neotrop. Helminthol., 3(1), 2009

Taenia mustelae. Figure 1. Scolex, ventral view. Figure 2. Rostellar larger hooks (a), smaller hooks (b). Figure 3.

Mature proglottid, ventral view. Bar = 200 in Figure 1, 25 in Figure 2 (a-b), 100 in Figure 3.

ACKNOWLEDGEMENTS

To Cibele R. Bonvicino, from the Cancer National

Institute, Rio de Janeiro, Brazil, for the identification of

the host species.

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*Correspondence to author:

Roberto Magalhães Pinto

Laboratório de Helmintos Parasitos de Vertebrados,

Instituto Oswaldo Cruz. Av. Brasil, 4365, 21040-900

Rio de Janeiro, Rio de Janeiro, Brasil

E-mail: rmpinto@ioc.fiocruz.br

Telefax: 55 (21) 2562-1511

Neotrop. Helminthol., 3(1), 2009

Taenia mustelae in Brazilian Bassaricyon gabbi Magalhães Pinto et al.