Neotrop. Helminthol., 6(1), 2012

2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

1 1 2

Antonio Mataresio Antonucci , Ricardo Massato Takemoto , Fernanda Menezes França ,

3 2

Patrícia CoelhoTeixeira & Cláudia Maris Ferreira

LONGIBUCCA CATESBEIANAE (NEMATODA: CYLINDROCORPORIDAE) OF THE BULLFROG,

LITHOBATES CATESBEIANUS (ANURA: AMPHIBIA) FROM FROG FARMS IN THE STATE OF

SÃO PAULO, BRAZIL

LONGIBUCCA CATESBEIANAE (NEMATODA: CYLINDROCORPORIDAE) EN LA RANA-TORO

LITHOBATES CATESBEIANUS (ANURA: AMPHIBIA) DE LAS GRANJAS DE

RANAS EN EL ESTADO DE SÃO PAULO, BRASIL

Suggested citation: Antonucci, AM, Takemoto, RM, França, FM, Teixeira, PC & Ferreira, CM. 2012. Longibucca catesbeianae

(Nematoda: Cylindrocorporidae) of the bullfrog Lithobates catesbeianus (Anura: Amphibia) from frog farms in the state of São

Paulo, Brazil. Neotropical Helminthology, vol. 6, nº1, pp. 75 - 83.

Abstract

Most parasites represent a serious socioeconomic problem, because they affect pets, commercially raised,

wild, and zoonotic animals. Weight loss, growth retardation, predisposition to other diseases and death are

symptoms presented by the parasitized animals. The aim of this study was to evaluate the helminth fauna in

bull-frog Lithobates catesbeianus raised for sale. We worked with five frog farms in the Vale do Paraíba, São

Paulo, Brazil, and examined a total of 185 animals. The autopsies were performed, and all bodies that may

have parasites were examined. Diagnostic parasitology tests were also performed. We found one species of

nematode, Longibucca catesbeianae, with a prevalence of 1.7%, mean abundance of 14.16 and an average

intensity of 850 (with a range of 729 to 1014). Given that most studies of parasitology in amphibians is

conducted in free-living animals, more research on frogs in captivity should be performed to better understand

these pests and prevent future problems in the operations frog farm.

Key words: Bullfrog – infection - Lithobates catesbeianus – Nematode - parasite - Rana catesbeiana.

Resumen

Palabras clave: Infección – Lithobates catesbeianus - Nematodos - parasitos, rana-toro - Rana catesbeiana.

La mayoría de los parásitos representan un problema socioeconómico grave, porque afectan a las mascotas, a

los animales criados para la venta y a los animales salvajes, y algunos también son zoonóticos. La pérdida de

peso, retraso del crecimiento, la predisposición a otras enfermedades y la muerte son los síntomas presentados

por los animales parasitados. El objetivo de este estudio fue evaluar la helmintofauna en la rana-toro

Lithobates catesbeianus criada para la venta. Se trabajó con cinco granjas de rana en el Vale do Paraíba, São

Paulo, Brasil, y se examinaron un total de 185 animales. Las necropsias se realizaron, y todos los órganos que

pueden tener parásitos fueron examinados. Exámenes de diagnóstico coproparasitológico también fueron

realizados. Se encontró una sola espécie de nematodo y se identificó como Longibucca catesbeianae, con una

prevalencia de 1,7%, abundancia media de 14,16 y una intensidad media de 850 (con un rango de 729 a 1.014).

Teniendo en cuenta que la mayoría de los estudios de parasitología en los anfibios se llevan a cabo en animales

de vida libre, más investigación en ranas en cautiverio se debe realizar con el fin de comprender mejor a estos

parásitos y evitar futuros problemas en las operaciones comerciales de granjas de rana.

1Laboratório de Ictiopatologia, NUPELIA, Universidade Estadual de Maringá, PR, Brazil. Avenida Colombo, 5790 - Bloco G90 - CEP 87020-900 - Maringá –

Paraná. endorana@yahoo.com.br Fone: (44) 3261-4642; (44)99503810 - Fax: (44) 3261-4625

2 Instituto de Pesca, APTA, SAA.-Av. Francisco Matarazzo, 455. São Paulo, SP, Brazil.

3 Centro de Aqüicultura da Universidade Estadual de São Paulo, Jaboticabal, São Paulo, Brazil.

Antonucci et al.

Longibucca catesbeianae the bullfrog Lithobates catesbeianus

The American bullfrog (Rana catesbeiana

Shaw, 1802), recently reclassified as Lithobates

catesbeianus Frost et al., 2006, was introduced

in Brazil in the 1930s from specimens brought

from Canada and was established in a frog farm

known as Ranário Aurora in the state of Rio de

Janeiro (Ferreira et al., 2002). Until the 1970s,

the frog rearing and fattening tanks were called

multiple tanks, in which various types of food

were offered, such as slaughterhouse leftovers to

attract insects (flies) with developing larvae for

attracting frogs. However, the unpleasant odor

caused a negative impact on production that

culminated in the development of several other

systems of rearing and fattening.

Notwithstanding the existence of a full range of

rearing structures, Brazilian producers typically

modify or mix systems so as to adapt these

structures for a variety of purposes, giving rise to

the so-called hybrid systems (Teixeira et al.,

2001; Ferreira et al., 2002). Currently, frog

farming in Brazil constitutes an alternative

agroindustrial enterprise, particularly to

producers with restricted area availability, due to

its minimal space requirements (Dias et al.,

2008, 2009).

Large concentrations of animals constitute a

factor favoring the emergence of disease through

the inherent creation of a favorable environment

for epizootic outbreaks due to the presence of

different pathogens that, under natural

conditions, would have a minimal presence

(Pavanelli et al., 2002). According to Hipolito

(2004), most parasites do not cause the death of

the animal; however, they can seriously

compromise the host's development. Parasitism

includes actions in which one organism, the

parasite, is metabolically dependent on another,

the host, and depending on numerous factors,

may or may not cause damage leading to the

emergence of parasitic disease.

Many protozoa and metazoa found in

INTRODUCTION

amphibians are not associated with disease

u n l e s s t h e h o s t i s s t r e s s e d o r

immunocompromised. Amphibians most

susceptible to parasitism are those that are newly

captured, transported or maintained under poor

hygienic conditions and outside of their optimal

thermal zone of activity (Wright & Whitaker,

2008). According to these authors, the parasites

with an indirect life cycle tend to die if the

amphibian used as an intermediate or definitive

host is not in its native environment. With respect

to parasites with a direct life cycle, the infections

can be intensified in closed environments.

The main helminths with socioeconomic

interest, due to their high prevalence in domestic

and wild animals, belong to the phylum

Nemathelminthes, which includes nematodes,

and to the phylum Platyhelminthes, which

comprises cestodea, trematodea and monogenea

(Almeida & Ayres, 1996). According to Fagonde

Costa (2005), most nematodes produce adverse

effects that are dependent on the parasite load in

the animal. Thus, the mere presence of some

worms does not indicate that the hosts are being

harmed. The pathological action of the parasite

depends on the affected organ, perforating

injuries, parasitism intensity and secondary

bacterial contamination (Hipolito, 2004).

The study of parasitic diseases that affect

amphibians in captivity is still incipient. Within

the specialized literature, articles are mainly

restricted to case references and surveys of the

prevalence of parasites, with few studies on the

parasite-host relationship. A review by Hipolito

(2004) catalogued the occurrence of infestation

by crustaceans (Lernaea cyprinacea

Linnaeu,1758), insects (myiasis caused by the

Notochaeta sp. fly larva), acanthocephala and

nematodes, such as Longibucca catesbeianae

Souza Junior, Artigas & Martins, 1993, in Brazil.

In the international literature, rare cases of

infestation by nematodes have been referenced,

and include infestations by Eustrongylides sp,

Neotrop. Helminthol., 6(1), 2012

which is considered a zoonotic parasite and has

been found encysted in the muscles of farmed

bullfrogs in Cuitzeo Lake, Mexico (Lezama &

Sarabia, 2001).

The aim of this study was to understand the

possible parasitoses suffered by commercially

raised bullfrogs in the State of São Paulo and to

assess the sanitary conditions of farms.

The helminthofauna survey was performed in

five frog farms in different municipalities in

the region of Vale do Paraíba, São Paulo,

Brazil. These frog farms were designated A, B,

C, D and E, and this region was chosen for

having the largest number of active frog farms

in the state.

We collected 36 apparently healthy bullfrogs

(L. catesbeianus) from each property, for a

total of 180 individuals, between March and

June 2008. The post-metamorphosis animals

were collected randomly and redistributed in

the laboratory into three groups of 12 animals

each, according to their stage of development

within the frog farm rearing (Lima &

Agostinho, 1992).

Five wild bullfrogs (invaders) were also

collected from the dependencies of frog farm

B (dam) that inhabited this site in the absence

of any husbandry, sanitation or food control.

The frogs were taken to the Pathology

Laboratory of Aquatic Organisms of the

Fisheries Institute in São Paulo, where they

remained in vivaria adapted for bullfrogs

(Bueno-Guimarães, 1999) for a maximum of

four days. The water was changed daily, and

the animals were force-fed with extruded feed

containing 40% crude protein.

Prior to sacrifice, the animals were

anesthetized by hypothermia and inspected to

detect any injury or ectoparasites.

Subsequently, they were desensitized and

sacrificed by medullar section and bleeding at

the level of the atlas vertebra in the cervical

region, using methods described by Cornel

University (2005) that eliminate suffering.

Necropsies were performed on newly

sacrificed animals under a stereoscopic

microscope, via an incision made with scissors

starting at the cloaca, exposing the entire

coelomic cavity and viscera. All organs likely

to be parasitized were removed and observed

separately in Petri dishes. The oral cavity and

tongue were also observed.

The gastric and intestinal contents were

isolated for further analysis, and a portion of

the final third of the intestine was used for

copro-parasitological examination. This

examination followed the Ritchie method for

detection of helminth eggs and possible

protozoa (Figueira de Mello, 1973).

Additionally, we used another method to

detect helminth eggs with lighter densities,

using a sucrose-saturated solution

(density=1.203) instead of water. In this

centrifugal flotation method, similar to that of

Ritchie, ether was not used (Figueira de Mello,

1973).

The gastric mucosa and the anterior portion of

the intestine were scraped with a spatula and

the scrapings placed on a glass slide with a

cover slip for detection of parasites by light

microscopy (Souza Junior et al., 1993).

The helminths found were collected and fixed

in 4% formaldehyde heated to approximately

65°C, according to Eiras et al. (2006), and

taken to the NUPELIA Ictioparasitology

Laboratory (Research Nucleus in Limnology,

Ichthyology and Aquaculture) at Maringá

State University - UEM (Universidade

Estadual de Maringá) for identification. The

helminths were dehydrated in a series of

MATERIALS AND METHODS

Antonucci et al.

Longibucca catesbeianae the bullfrog Lithobates catesbeianus

alcohol baths and cleared with beech wood

creosote, and the slide was mounted with

Canada balsam. The identification of parasite

specimens was performed using an optical

microscope at a magnification of 1000x and by

comparing what was observed with figures

presented in the literature (Souza Junior et al.,

1993).

Parasite counting was performed on the

McMaster chamber used in clinical laboratories

for the quantification of helminth eggs

(Nascimento et al., 2009). Given that each

reading field of the camera carries a volume of

0.15 mL and that the camera has two fields, the

number of helminths found could be

approximated. The liquid containing the

parasites was homogenized, and three different

readings of the same host were made, recording

parasite counts and chamber volume. The total

volume of formaldehyde with helminths was

determined using a measuring cylinder. With

this total volume and using a simple rule of three,

the total volume of formaldehyde in which the

helminths were fixed was used to estimate the

total number of parasites. Calculations of

amplitude, incidence, prevalence and parasite

abundance followed the protocols proposed by

Bush et al. (1997).

The only helminth found was the nematode

Longibucca catesbeianae described by Souza

Junior et al. (1993). This is a small nematode

measuring 520-707 µm that is usually located in

the gastric mucosa, although it can also be found

in the intestinal mucosa.

Among the five frog farms examined, only two

presented parasitized animals, and even then,

not all individuals were infested (low

prevalence). Only one frog originating from frog

farm D and two frogs from frog farm E exhibited

infestation by L. catesbeianae in the stomach,

indicating a prevalence of 1.66%, a mean

abundance of 14.16%, an average intensity of

850 parasites and an amplitude of 729-1014

parasites for all captive animals studied.

The infected animal from frog farm D weighed

357.1 g, making it the largest in the group, and

according to farm reports, it was an animal from

an older lot, above the normal age and weight for

slaughter. In frog farm E, parasitized frogs

weighed 201.4 g and 167.7 g, the former being

the largest of the group and the latter of

intermediate weight; both were within the

normal weight and age for the frog fattening

sector of commercial frog farming (Ferreira et

al., 2002).

The three parasitized animals presented worms

only in the stomach that were adhered to the

gastric mucosa. The other viscera and cavities

did not show any lesions or structures suggestive

of parasite fixation or migration, indicating that

the animals were kept under appropriate

husbandry conditions (Fontanello et al., 1993).

The coproparasitology methods used did not

reveal helminth eggs or protozoan cysts in the

fecal samples analyzed.

The fact that larger animals are more highly

parasitized may be due to a cumulative effect

because these are, theoretically, the older

animals such that they have had more

opportunities to acquire parasites.

According to Measures (1994), the genus

Longibucca was described in the 1930s in four

species of bats in North America. The same study

proposed that two of the nematode species,

namely, Longibucca eptesica and Longibucca

lasiura, are synonymous. The genus Longibucca

has also been described in South American

snakes, such as the Muçuranas, Pseudoboa

RESULTS DISCUSSION

Neotrop. Helminthol., 6(1), 2012

cloelia and Clelia clelia Daudin, 1803,

according to Souza Junior et al. (1993). The

presence of L. catesbeianae causes gastric and

intestinal lesions, bleeding and apathy in the

hosts (Hipolito, 2004). However, this was not

observed in this study.

The invading individuals showed a higher

prevalence of parasites than did animals in farms

D and E, which can be explained by the both the

adoption of appropriate sanitary and feed

management in farmed animals (Fontanello et

al.,1993) and by the greater possibilities for

parasite cycle completion in the natural

environment.

Campos et al. (2007) and Tavares-Dias et al.,

(2001), found no significant differences between

the total parasite count and the count performed

using a McMaster chamber, indicating the

efficiency of this technique. These procedures to

identify parasites, eggs and cysts in live animals

need to be standardized and validated for aquatic

organisms to avoid the sacrifice of animals and

facilitate the collection of material.

Few studies in Brazil have described parasites

affecting the commercially bred bullfrog, L.

catesbeianus. One of these studies was the re-

description of the nematode Gyrinicola

chabaudi Araujo & Artigas, 1982, collected in

the gastrointestinal tract of tadpoles from a

nursery (Souza Junior & Martins, 1996).

Another study was conducted in Mexico on

skeletal muscle injuries of bullfrogs

commercially raised in the Cuitzeo Lake, and

reported the presence of the zoonotic nematode

Eustrongylides sp, whose larvae not only cause

injury but can also encyst (Lezama & Sarabia,

2001). These authors corroborate the relevance

of the objective of this study of parasites in frogs

with commercial importance that are primarily

destined for human consumption, given that

these can harbor zoonotic parasites such as those

mentioned above.

Most reports on amphibian parasites are

performed on wild animals that have been

collected from ecological reserves, parks and

other locations (McAlpine & Burt, 1998; Bursey

& William, 1998). Invading frog farm

amphibians in close proximity to the farmed

bullfrogs were captured and analyzed for the

observation of existing parasites (Souza Junior

& Martins, 1996; Souza Junior et al., 1993).

McAlpine & Burt (1998), while conducting a

field study in New Brunswick, Canada, collected

Rana catesbeiana, R. clamitans Latreille, 1801

and R. pipiens Schreber,1782 and observed four

species of cestodes, 14 species of digeneans, five

species of nematodes and two species of

Acanthocephala. Similar work performed by

Brusey & Willian (1998) in Ohio, USA,

described, in bullfrogs, the digenean

Haematoloechus longiplexus Stafford, 1902 and

nematode Rhabdias ranae Walton,1929 in the

lung, the cestode Ophiotaenia gracilis Jones,

Cheng and Gillespie, 1958 in the small intestine,

the nematode Cosmocercoides variabilis

Harwood, 1930 in the large intestine,

Physaloptera sp Rudolphi, 1919 nematode

larvae in the stomach and the nematode

Gyrinicola batrachiensis Walton, 1929 in

bullfrog tadpole intestines.

Pryor & Bjorndal (2005) hatched bullfrog eggs

in the laboratory for subsequent studies of the

effects of the nematode Gyrinicola batrachiensis

on the development of tadpoles after

experimental infestation. They concluded that

the relationship between these animals is one of

mutualism because intestinal development and

fermentation are favored in the presence of

nematodes.

In a survey of wild bullfrog parasites,

Marcogliese et al., (2000) described the

occurrence of digeneans of the genus

Diplostomum sp Nordmann, 1832 in bullfrog

tadpoles inhabiting the St. Lawrence River in the

region of Quebec, Canada. Studies were also

performed to assess intra-specific variation of

Antonucci et al.

Longibucca catesbeianae the bullfrog Lithobates catesbeianus

the digenean Haematoloechus floedae

Harwood, 1832, collected from the lungs of wild

amphibians of the genus Rana in North and

Central America (León-Règagnon et al., 2005).

Yildirimhan et al., (2006) referenced the

infestation of the urinary bladder of Rana

macrocnemis Boulenger, 1885 by monogenea

Polystoma macrocnemis Vaucher, 1990 and also

described the presence of digenea,

acanthocephala and nematoda in these frogs. All

these studies show that L. catesbeianus are

susceptible to infestation by helminths,

especially in the wild, because the completion of

the parasite cycle can occur under these

conditions.

Distinct biological and ecological

characteristics between hosts generate

differences in the exposure and rates of

infection/infestation, as well as differences in

the degree of post-infection compatibility and

susceptibility (Guidelli et al., 2006). In most

cases, the host possesses genetic and

immunological mechanisms against helminths

because most of the immunological processes

are under genetic control. Antibodies mainly act

against helminths located on the mucosa of the

digestive tract. With the evolution of

relationships between parasites and hosts,

helminths have evolved mechanisms to evade

the immune system that are essential for their

survival and proliferation (Araujo & Madruga,

2001).

The host animal has several immunological

mechanisms against pathogens, infectious

agents and parasites. Natural protective barriers,

such as the skin, secretions and various

biologically active substances, must be

overcome by these agents. Helminths can

overcome all these barriers (Soares, 2001).

Hipolito (2004) reported that in a survey of

producers, most stated that they had adopted

preventive measures. In the questionnaire

administered to producers in this study, they

stated that such measures, such as invader

control and daily bay cleaning, were performed.

However, the use of medication as a preventive

measure was inappropriately reported and

observed in three of the frog farms visited. At

two of the facilities, water quality control was

not observed and crossed other locations before

arriving at the farm. In all frog farms, domestic

animals had access to the bullfrog-fattening

enclosure, and there was no site for cleaning of

employee shoes and clothes. Only one farm used

an effluent settling pond before effluent was

released into the stream.

Studies should be conducted to clarify the L.

catesbeianae life cycle because the invading

animals, which lacked sanitation or food control,

were much more highly parasitized. The

parasite/host relationship must also be better

elucidated because one can assume that

bullfrogs, an exotic species in Brazil, are

resistant to most existing parasites, as is the case

for other introduced and farmed animals.

Even though the prophylactic and preventive

measures were not ideal for biosecurity in the

frog farms assessed, these measures proved

effective because there was a low incidence of

infections by helminths and other parasites. Only

one nematode species was found to be infecting

the bullfrogs, and this infection occurred with

low prevalence.

To the frog breeders, who kindly provided the

animals for the development of the study. To

NUPÉLIA, for providing the structure and

support for the analysis of the collected material

and to CAPES, for the awarded fellowship.

ACKNOWLEDGEMENTS

Neotrop. Helminthol., 6(1), 2012

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Author for correspondence / Autor para

correspondencia:

Antonio Mataresio Antonucci

Laboratório de Ictiopatologia, NUPELIA,

Universidade Estadual de Maringá, PR, Brazil.

Avenida Colombo, 5790 - Bloco G90 - CEP 87020-

900 - Maringá – Paraná.

Fone:(44) 3261-4642; (44)99503810 - FAX: (44)

3261-4625

E-mail / correo electrónico:

endorana@yahoo.com.br

Received January 23, 2012.

Accepted February 15, 2012.