473

Neotrop. Helminthol., 8(2), 2014

2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

RESEARCH NOTE / NOTA CIENTÍFICA

FREQUENCY OF ANTIBODIES AGAINST TOXOPLASMA GONDII IN WILD CARNIVORES

AND MARSUPIALS IN NORTHEAST MEXICO

FRECUENCIA DE ANTICUERPOS CONTRA TOXOPLASMA GONDII EN CARNIVOROS Y

MARSUPIALES SILVESTRES EN EL NORESTE DE MEXICO

1 2 3

Emilio Rendón-Franco *; Arturo Caso ; Nayelly Gabriela Jiménez-Sánchez ;

2 4

Sasha Carvajal-Villarreal & Hector Zepeda-López ;

Abstract

Resumen

Keywords: canidae - felidae - mustelidae - procionidae.

Palabras clave: canidae – felidae – mustelidae – procionidae.

Suggested citation: Rendón-Franco, E, Caso, A, Jiménez-Sánchez, NG, Carvajal-Villarreal, S & Zepeda-López, H 2014.

Frequency of antibodies against Toxoplasma gondii in wild carnivores and marsupials in northeast Mexico. Neotropical

Helminthology, vol. 8, n°2, jul-dec, pp. 473-478.

1 Departamento de Producción Agrícola y Animal. Universidad Autónoma Metropolitana – Unidad Xochimilco, Calzada del Hueso 1100, Col. Villa Quietud,

Delegación Coyoacán, D.F. México, C.P. 04960, México. emilio.rendon.franco@gmail.com

2 Caesar Kleberg Wildlife Research Institute. Texas A&M University-Kingsville 700 University Blvd., MSC 218, Kingsville, Texas 78363-8202, Texas, USA.

3 Academia de Biología. Centro de Estudios Científicos y Tecnológicos No. 6 "Miguel Othón de Mendizabal" Instituto Politécnico Nacional. Avenida Jardín y

calle 4 s/n, Col. Del Gas, Delegación Azcapotzalco, D.F. México, C.P. 2950, México.

4 ZELOR Instituto de Medicina de la Conservación. SAPI calle Romano No. 13525-C Fracc. Alcala La Mesa Tijuana B.C. México C.P. 22106.

* Correspondence should be to Emilio Rendón-Franco Calzada del Hueso 1100, Col. Villa Quietud, Delegación Coyoacán, C.P. 04960, D.F. México, 00 55 54 83

70 00 ext. 3658.

There is little previous information about the wild cycle of Toxoplasma gondii in wild carnivores

and marsupials in Mexico. The objective of this study was to determine the presence of antibody

against T. gondii in wild carnivores and marsupials in northeast Mexico. Frequency of T. gondii in

captured specimens was: margay (Leopardus wiedii; n=3; 33%), jaguarundi (Puma

yagouaroundi; n=2; 0%), bobcat (Lynx rufus; n= 1; 100%), coatimundi (Nasua narica; n=7;

42%), coyote (Canis latrans; n=4; 25%), gray fox (Urocyon cinereoargenteus; n=3; 66%), hog-

nosed skunk (Conepatus leuconotus; n=1; 0%), and opossum (Didelphis sp.; n=5; 20%).

Therefore, natural infection with T. gondii in wild carnivores and marsupials in northeast Mexico

was present.

Existe poca información acerca del ciclo silvestre de Toxoplasma gondii en carnívoros y

marsupiales silvestres en México. El objetivo de este estudio fue determinar la presencia de

anticuerpos contra T. gondii en carnívoros y marsupiales silvestres en el noreste de México. La

frecuencia de T. gondii en los especímenes capturados fue: margay (Leopardus wiedii; n=3; 33%),

jaguarundi (Puma yagouaroundi; n=2; 0%), lince (Lynx rufus; n= 1; 100%), coatí (Nasua narica;

n=7; 42%), coyote (Canis latrans; n=4; 25%), zorra gris (Urocyon cinereoargenteus; n=3; 66%),

zorrillo (Conepatus leuconotus; n=1; 0%), y tlacuache (Didelphis sp.; n=5; 20%). Se comprueba

la infección natural con T. gondii en carnívoros y marsupiales silvestres en el noreste de México.

Rendón-Franco et al.

Toxoplasma gondii in carnivores and opossum

Toxoplasma gondii (Nicolle, Manceaux and

Splendore 1908) is an intracellular parasite that

affects all homeothermic vertebrate. In the

domestic cat, the complete cycle of the parasite

occurs because the cat is the only definitive host.

Infected hosts may be in an infectious stage all

their lives and this helps the worldwide

distribution of the disease (Frenkel, 1990; Della,

1999; Wolfe, 2003). The wild felids are also

considered definitive hosts since this parasite

have been found in different species of wild cats

(Dreesen, 1990; Wolfe, 2003; Cañon-Franco et

al., 2013). Even though these animals have been

the definitive hosts, there are a few studies about

their role on the wild cycle of the parasite. A

recent revision reported that in the only

neotropical small felid species that this parasite

has been found is in ocelot (Leopardus pardalis;

Linné,1758), Geoffroy´s Cat (L. geoffroyi;

D´Orbigny and Gervais, 1844) and Oncilla (L.

tigrinus; Schreber, 1775) (Cañon-Franco et al.,

2013).

There are also a few records of the presence of

antibodies of this parasite in other wild

neotropical carnivores. A research on

neotropical mammals, included in its analysis

the coatimundi (Nasua nasua Linnaeus, 1766)

and common opossum (Didelphis marsupialis

Linnaeus, 1758) (Thoisy et al., 2003). Other

carnivores such as canids have been used as

indicators for T. gondii, however these studies

have been done in the neartic regions (Dubey et

al., 1999). In Mexico, studies about T. gondii in

wildlife are in small numbers and also focused

on neartic species (Kikuchi et al., 2004; Suzan &

Ceballos, 2005; Rendón-Franco et al., 2012). In

areas where domestic cats are not present, wild

felids are the final hosts; therefore it is very

important to evaluate which role they play in the

wild cycle of the parasite. In the other hand, it is

important to determine if other carnivores or

marsupials participate in the wild cycle of T.

gondii as an infectious host for the felids or even

for humans, since some carnivores such as the

coatimundi, skunk, and opossum are consumed

by people in rural areas (Naranjo et al., 2004;

Tlapaya & Gallina, 2010; Contreras-Moreno et

al., 2012).

The objective of this study is to determine the

presence of T. gondii antibodies in wild

carnivores and marsupials in a neotropical area

within northeast Mexico.

As a part of a felid ecological project developed

by Caso, captures were done with the use of box

traps (Tomahawk live Trap model No. 109.5,

Tomahawk Live Trap Company, Hazelhurst,

Wisconsin 54531,USA; Caso, 2013). Blood was

obtained from jaguarundis (Puma yagouaroundi

É. Geoffroy, 1803), coyotes (Canis latrans Say,

1823), coatimundis (Nasua narica Linnaeus,

1766), bobcats (Lynx rufus Schreber, 1777),

hog-nosed skunks (Conepatus leuconotus;

Lichtenstein, 1832), and common opossums

(Didelphis sp.) at Los Ebanos and Los Pericos

(23º 27' N, 97º 48' W) cattle ranches from 1998

to 2006 (Caso, 2013). In the other hand, captures

of margays (Leopardus wiedii Schinz, 1821),

gray foxes (Urocyon cinereoargenteus

Schreber, 1775) and coatimundis were done at El

Cielo Biosphere Reserve (23º03'N, 90º13'W) in

2003 (Carvajal-Villarreal et al., 2012). Both

study areas are in the state of Tamaulipas,

Mexico. P. yagouaroundi and L. wiedii are

protected by Mexican laws under category of

near threatened and risk of extinction

respectively (SEMARNAT, 2010). All

carnivores in this study are considered as least

concern by the UICN, except L. wiedii, which is

considered near threatened (UICN, 2014).

Samples were obtained after chemical

immobilization, and serum was maintained

frozen at -20 Cº until lab analysis (Caso et al.,

2005; Caso, 2013). Each individual was safely

handled according to the recommendations of

the American Society of Mammalogists (Sikes

& Gannon, 2007) and all were released at the

same capture point when the effects of

immobilization were not present.

Antibody detection was done through a test latex

INTRODUCTION

MATERIAL AND METHODS

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Neotrop. Helminthol., 8(2), 2014

agglutination test (Toxotest-MT, Eiken

Chemical Co. LTD, Tokyo 110-8408, Japan)

accordingly with lab specifications. This test

has been used before in wild felids to test the

presence of T. gondii (Ramos et al., 2001;

Kikuchi et al., 2004; Rendón-Franco et al.,

2012). Titers > 1:32 were considered positives

for felines while titers > 1:16 were considered

positives for the other species according with

manufacture recommendations. We calculated

the frequencies and confidence intervals 95%

for each species using epidemiological software

(Epidat 3.1 ® software, Servicio de

Epidemiología Dirección Xeral de Innovación e

Xestión de Saúde Pública, Santiago de

Compostela, Coruña, Spain).

Results obtained were the following: margay 1

of 3 (33%), jaguarundi 0 of 2 (0%), bobcat 1 of 1

(100%), coatimundi 3 of 7 (42%), coyote 1 of 4

(25%), gray fox 2 of 3 (66%), hog-nosed skunk 0

of 1 (0%) and common opossum 1 of 5 (20%).

Titers in positive animals were from 1:16 in

carnivores to 1:256 in coatimundis, and positive

for opossum 1:16 titer (Table 1).

RESULTS

Table 1. Frequencies and antibodies titer against Toxoplasma gondii in wild carnivores and marsupials.

Specie/serum dilution

>1:16

1:16b

1:32a 1:64 1:128 1:256 n Positive Frequency

% (CI 95%)

Margay

(Leopardus wiedii

)

1 3 1 33 (1-90)

Jagurundi

(Puma yagouaroundi)

2 0 0 (ND)

Bobcat

(Lynx rufus)

1 1 1 100 (ND)

Coatimundi

(Nasua narica)

2 7 3 42 (10-81)

Coyote

(Canis latrans)

4 1 25 (1-80)

Gray fox

(Urocyon cinereoargenteus)

1 1 3 2 66 (9-99)

Hog-nosed skunk

(Conepatus leuconotus)

1 0 0 (ND)

Opossum

(Didelphis sp) 4

5 1 20 (0-72)

a=positive feline b= positive other than feline, ND=no done.

DISCUSSION

There are not previous reports of antibodies

prevalence of T. gondii in margay and

jaguarundi; however, in jaguarundis it has been

found that they can excrete oocytes naturally or

during experiments (Jewell et al., 1972; Pizzie et

al., 1978). In this study, we did not find any

evidence of anti-Toxoplasma antibodies in

jaguarundis, but because to the small sample size

(n = 2), is not possible to say that jaguarundis

could not be infected by the parasite in the wild.

Even though the small number of individual

margays, these results are important since they

ensure that margays could be infected by T.

gondii in the wild. In the case of the gray fox,

there have been reports that indicate that the

prevalence of T. gondii in this species is high in

the U.S. since it runs from 25% to 75%

depending on the area, and this is consistent with

the present study. Same research also found that

the prevalence of T. gondii in coyotes is 59%,

however in the present study it is lower. It is

important to mention that sample size of this

study for both species is low; therefore is not

possible compare these results with the ones in

U.S (Dubey et al., 1999).

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Rendón-Franco et al.

Toxoplasma gondii in carnivores and opossum

This is the study that has obtained the best

sample size for wild coatimundis (n = 7). These

results indicate that the prevalence found of 42%

is lower of what was found by the only previous

study of 72% of prevalence (Thoisy et al., 2003).

Due to the small simple size in hog-nosed skunk

(n = 1), is not conclusive that they could not be

infected by T. gondii. In the case of opossums,

20% of prevalence was record, that is within the

rank (13-29%) reported for the U.S., but it is

higher with the one reported (10%) for central

Mexico, where mean ambient humidity is lower

(Smith & Frenkel, 1995; Hill et al., 1998; Suzan

& Ceballos, 2005; Mitchell et al., 2006). This

could explain the differences since in

neotropical regions there is more humidity and

this helps the parasite to remain viable for longer

periods. In French Guyana, it was found 15%

(n=34) of prevalence in common opossums and

20% (n=15) in white-eared opossum (D.

albiventris; Thoisy et al., 2003). In Brazil, it

was found 20.4% (n=396) of prevalence in

common opossums (Yal et al., 2003).

The prevalence of T. gondii found in

coatimundis and opossums have an important

zoonotic risk, since as it was mentioned earlier;

these species are hunted and consumed as food

by people in rural areas of Mexico (Naranjo et

al., 2004; Mitchell et al., 2006; Tlapaya &

Gallina, 2010; Contreras-Moreno et al., 2012).

The role of wild cats on the cycle of T. gondii is

important particularly in areas where domestic

cats coexist with them. In the case of other wild

carnivores, there is little information about what

is their role in the wild cycle of T. gondii.

However, it is important to know their role as

hosts since they compete for the infected prey

and therefore they can lower the prevalence of

the disease. Since opossums are commonly

depredated by different carnivores including

felids, it is important to determine the prevalence

in them to know which is the parasite's infectious

cycle. It is also important to generate studies

that include intermediate hosts with the

objective of identifying how the parasite cycle

closes in the wild (ferraroni et al., 1980).

Thank to the Dallas Zoo, the Oklahoma City Zoo,

and Los Ebanos Ranch, for their funding and

support for this project. Also thank to the

Dirección General de Vida Silvestre and the State

of Tamaulipas to provide the necessary permits to

develop this study.

ACKNOWLEDGEMENTS

BIBLIOGRAPHIC REFERENCES

Cañon-Franco, WA, Araújo, FAP & Gennari,

SM. 2013.

Carvajal-Villarreal, S, Caso, A, Downey, P,

Moreno, A, Tewes, ME & Grassman Jr,

LI. 2012.

Caso, A. 2013.

Caso, A, Carvajal-Villarreal, S, Downey, P, &

Moreno, A. 2005.

Contreras-Moreno, FM, De la Cruz-Félix, K, &

Bello-Gutíerrez, J. 2012.

Della, MG. 1999.

Toxoplasma gondii in small

neotropical wild felids. Brazilian Journal

of Veterinary Research and Animal

Science, vol. 50, pp. 50-67.

Spattial patterns of the margay

(Leopardus wiedii, Felidae, Carnivora) at

“El Cielo” Biosphere Reserve,

Tamaulipas, Mexico. Mammalia, vol. 76,

pp. 237-244.

Spatial differences and local

avoidance of Ocelot (Leopardus pardalis)

and Jaguarundi (Puma yagouaroundi) in

Northeast Mexico. Tesis de Doctor en

Ciencias Biológicas, Texas A&M

University-Kingsville, Kingsville, Texas.

Técnica de captura y

manejo del margay (Leopardus wiedii) en

la Reserva de la Biosfera El Cielo. In:

Sánchez-Ramos, G, Reyes-Castillo, P &

Dirzo, R, (eds.). Historia Natural de la

Reserva de la Biosfera "El Cielo",

Tamaulipas. México. Universidad

Autónoma de Tamaulipas, Instituto de

Ecología A. C., UNAM. Toppan printing

inc. Vol. 55, pp. 538-542.

Uso patrones de

cacería y preferencia de presas en dos

sitios del parque estatal La Sierra,

Tabasco, México. Etnobiología, vol. 10,

pp. 1-9. Toxoplasmosis in zoo animals.

In: Fowler, ME, & Miller RE (eds.). Zoo

and Wild Animal Medicine, 4 ed. W.B.

476

Neotrop. Helminthol., 8(2), 2014

Sauders Co., Philadelphia, Pennsylvania.

pp. 131-135. Toxoplasma gondii

infections in wildlife. Journal of the

American Veterinary Medical

Association, vol. 196 pp. 274-276.

Toxoplasma gondii

antibodies in naturally exposed wild

coyotes, red foxes, and gray foxes and

serologic diagnosis of toxoplasmosis in

red foxes fed T. gondii oocysts and tissue

cysts. The Journal of Parasitology, vol. 85,

pp. 240-243.

Prevalence of Toxoplasma antibodies in

humans and various animals in the

A m a z o n . P r o c e e d i n g s o f t h e

Helminthological Society of Washington,

vol. 47, pp. 148-150.

Transmission of

toxoplasmosis and the role of immunity in

limiting transmission and illness. Journal

of the American Veterinary Medical

Association, vol. 196, pp. 233-240.

Seroprevalence of

antibodies aginst Toxoplasma gondii in

free-ranging mammals in Iowa. Journal of

Wildlife Diseases, vol. 34, pp. 811-815.

Development of

Toxoplasma oocysts in neotropical

felidae. The American Journal of Tropical

Medicine and Hygiene, vol. 21, pp. 512-

517.

Seroprevalence of Toxoplasma

gondii in American free-ranging or

captive pumas (Felis concolor) and

bobcats (Lynx rufus). Veterinary

Parasitology, vol. 120, pp. 1-9.

Prevalence of agglutinating

antibodies to Toxoplasma gondii in

striped skunks (Mephitis mephitis),

opossums (Didelphis virginiana), and

raccoons (Procyon lotor) from

Connecticut. The Journal of Parasitology,

Dreesen, DW. 1990.

Dubey, JP, Storandt, ST, Kwok, OC, Thullinez, P

& Kazacos, KR. 1999.

Ferraroni, JJ, Reed, SG & Speer, CA. 1980.

Frenkel, JK. 1990.

Hill, RE, Zimmerman, JJ, Wills, RW, Patton, S &

Clark, WR. 1998.

Jewell, ML, Frenkel, JK, Johnson, KM, Reed, V

& Ruiz, A. 1972.

Kikuchi, Y, Chomel, BB, Kasten, RW,

Martenson, JS, Swift, PK & O'Brien, SJ.

2004.

Mitchell, SM, Richardson, DJ & Lindsay, DS.

2006.

vol. 92, pp. 664-665.

Subsistence hunting by

three ethnic groups of the Lacandon

forest, Mexico. Journal of Ethnobiology,

Vol. 24, pp. 233-253.

Hallazgo del ciclo ontogenico selvatico

del Toxoplasma gondii en felidos salvajes

(Oncifelis geoffroyi, Felis cocolo y Felis

eira) de la provincia de Cordoba. Revista

Militar de Veterinaria, vol. 25, pp. 293-

300.

Seroprevalence of

Toxoplasma gondii in captive neotropical

felids from brazil. Veterinary

Parasitology, vol.102, pp. 217-224.

Prevalence of anti-Toxoplasma

gondii antibody in free-ranging ocelots

(Leopardus pardalis) from Tamaulipas,

Mexico. Journal of Wildlife Diseases, vol.

48, pp. 829-831.

Norma Oficial

Mexicana NOM-059-SEMARNAT-2010,

protección ambiental, especies nativas de

México de flora y fauna silvestre,

categorías de riesgo y especificaciones

para su inclusión, exclusion o cambio,

lista de especies en riesgo. Diario Oficial

de la Nación. pp. 1–78.

Guidelines of

the American Society Mammalogists for

the Use of Wild Mammals in Research.

Journal of Mammalogy, vol. 88, pp. 809-

23. Prevalence of

antibodies to Toxoplasma gondii in wild

mammals of Missouri and east central

Kansas: biologic and ecologic

considerations of transmission. Journal of

Wildlife Diseases, vol. 31, pp. 15-21.

The role of feral

Naranjo, EJ, Guerra, MM, Bodmer, RE &

Bolaños, JE. 2004.

Pizzie, HL, Rico, CM, & Pessat, OAN. 1978.

Ramos, SJ, Ogassawara, S, Adania, CH,

Ferreira, F, Gennari, SM, & Ferreira-

Neto, JS. 2001.

Rendón-Franco, E, Caso-Aguilar, A, Jiménez-

Sánchez, NG, Sandoval-Sánchez, AL,

Brousset, HJDM, & Zepeda-López, HM.

2012.

SEMARNAT (Secretariìa de Medio Ambiente y

Recursos Naturales). 2010.

Sikes, RS & Gannon, WL 2007. The animal care

and use committee of the American

Society of Mammalogists.

Smith, DD & Frenkel, JK. 1995.

Suzan, G & Ceballos, G. 2005.

477

Rendón-Franco et al.

Toxoplasma gondii in carnivores and opossum

mammals on wildlife infectious disease

prevalence in two nature reserves within

Mexico City limits. Journal of Zoo and

Wildlife Medicine, vol. 36, pp. 479-484.

Ecologic correlates of Toxoplasma

gondii exposure in free-ranging

neotropical mammals. Journal of Wildlife

Diseases, vol. 39, pp. 456-459.

Cacería de

mamíferos medianos en cafetales del

centro de Veracruz, México. Acta

Zoologica Mexicana (n.s.), vol. 26, pp.

259-277.

Red list of

threatened animals. UICN Species

Survival Commission, Glad, Suiza.

Thoisy, B, Demar, M, Aznar, C & Carme, B.

2003.

Tlapaya, L & Gallina, S. 2010.

UICN (Unión Internacional para la

Conservación de la Naturaleza y los

Recursos Natrales). 2014.

A v a i l a b l e o n l i n e :

http://www.iucnredlist.org

Toxoplasmosis. In: Fowler,

ME & Miller, RE (eds.). Zoo and Wild

Animal Medicine. 5 ed. W.B. Saunders

Co., St. Louis Missouri. pp. 745-749.

Seroprealence of

Neospora caninum and Toxoplasma

gondii antibodies in the South American

opossum (Didelphis marsupialis) from the

city of Sao Paulo, Brazil. The Journal of

Parasitology, vol. 89, pp. 870-871.

Wolfe, BA. 2003.

Yal, LEO, Cañon-Franco, WA, Geraldi, VC,

Summa, MEL, Camargo, MCGO, Dubey,

JP & Gennari, SM. 2003.

Received August 1, 2014.

Accepted October 21, 2014.

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