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THERYA, 2018, Vol. 9 (1): 7-13 DOI: 10.12933/therya-18-501 ISSN 2007-3364
Intestinal parasites of the bobcat (Lynx rufus) in areas surrounding
Queretaro, Mexico
Brenda CamaCho-maCías1, norma hernández-CamaCho1*, Germinal JorGe Cantó alarCón2, Claudia irais muñoz-GarCía3, ruBén Pineda-lóPez1,
raúl FranCisCo Pineda-lóPez1, salvador zamora-ledesma1 and marCo antonio moreno-Pérez1.
1 Licenciatura en Biología, Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Av. de las Ciencias s/n, CP. 76230,
Querétaro. Querétaro, México. E-mail: norma.hernandez@uaq.mx (NHC), camachomacb@gmail.com (BCM), rpineda62@
hotmail.com (RPL), rpineda@uaq.mx (FRPL), szamora1405@gmail.com (SZL), biomamp1988@gmail.com (MAMP).
2 Licenciatura en Medicina Veterinaria y Zootecnia. Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Av. de
las Ciencias s/n, CP. 76230, Querétaro. Querétaro, México. E-mail: gcanto07@uaq.mx (GJCA).
3 Departamento de Producción Agrícola y Animal. Universidad Autónoma Metropolitana. Unidad Xochimilco. Calzada del Hueso
1100. Col. Villa Quietud, Delegación Coyoacán CP. 04960, Ciudad de México. México. E-mail: cimunoz@correo.xoc.uam.mx
(CIMG).
* Corresponding author
The bobcat (Lynx rufus) is one of the carnivores most widely distributed in North America, coexisting with wild and domestic animals.
Parasites reported for the bobcat in the United States and Canada are generalists typical of the order Carnivora. In Mexico, studies on parasites
of carnivorous mammals are scarce due to their elusive nature, which makes dicult to obtain biological samples. Considering the available
information about the bobcat in its northern distribution range, the community of intestinal parasites of this species was expected to comprise
generalist parasites. The primary aim of this study was to determine the composition of the community of intestinal parasites in the bobcat
(Lynx rufus) inhabiting areas surrounding the city of Queretaro, and investigate whether seasonal dierences exist. The study was carried out
in four sampling sites where Lynx rufus had been previously reported. Tracks were surveyed for scats in the rainy and dry seasons. Scats were
analyzed using the Ritchie method supplemented with coprocultures and larval migrations. Parasites were identied based on specialized
literature and prevalence was expressed in percentage. A X2 test and a non-metric multidimensional scaling analysis were conducted to com-
pare parasite species composition between sites and between seasons. A total of 83 scat samples were collected, 53 in the rainy season and 30
in the dry season. A total of seven parasite species were identied: Trichuris vulpis, Physaloptera praeputialis, Toxascaris leonina, Toxocara cati,
Strongyloides stercolaris, Ancylostoma sp. and Uncinaria stenocephala. The prevalence of parasitized scats in both seasons was 75.9 %, with 73.6
% and 80 % in the rainy and dry seasons, respectively. The X2 test showed no signicant dierences between seasons (X2 = 0,553, d. f. = 1, P =
0.457). No dierences were found in parasite species composition, either between seasons or between localities, according to the nonmetric
multidimensional scaling analysis. The parasitic load of the bobcat in areas surrounding Querétaro is composed of generalist nematodes that
are typical of carnivores. T.vulpis is recorded for the rst time in L. rufus for Mexico. A high prevalence of S. stercolaris was observed, suggesting
an interaction with human populations and domestic and wild animals, as reported in other studies on this same carnivore. This study is one
of the rst reports published on intestinal parasites of L. rufus in anthropic areas of Mexico, nding that the composition and structure of the
parasite communities of this carnivore may indicate tolerance to disturbance derived from human activities.
El gato montés (Lynx rufus) es uno de los carnívoros con mayor distribución en Norteamérica, coexistiendo con animales domésticos y
silvestres. Los parásitos que han sido reportados para el gato montés en Estados Unidos y Canadá son generalistas típicos del orden Carni-
vora. En México, los estudios sobre los parásitos de mamíferos carnívoros son escasos por su naturaleza elusiva que diculta la obtención de
muestras biológicas. Considerando la información disponible del gato montés para el norte de su distribución, se esperaba encontrar que la
comunidad de parásitos intestinales de esta especie estuviera compuesta por parásitos generalistas. El objetivo general de este estudio fue
conocer la composición de la comunidad de parásitos intestinales del gato montés (Lynx rufus) en la zona conurbada de Querétaro, así como
determinar diferencias estacionales. El estudio se realizó en cuatro puntos de colecta donde se ha registrado previamente Lynx rufus. Se rea-
lizaron recorridos para búsqueda y colecta de excretas durante las temporadas de lluvias y secas. Las excretas se analizaron con la técnica de
Ritchie, complementando con coprocultivos y migraciones larvarias. La identicación de parásitos se realizó con literatura especializada y su
prevalencia fue expresada en porcentaje. Se hizo una prueba de X2, así como un análisis de escalamiento multidimensional no métrico para
comparar la composición de especies entre sitios y entre temporadas. Se colectaron 83 excretas en total, 53 en lluvias y 30 durante secas. Se
identicaron en total siete especies: Trichuris vulpis, Physaloptera praeputialis, Toxascaris leonina, Toxocara cati, Strongyloides stercolaris, Ancylos-
toma sp. y Uncinaria stenocephala. La prevalencia de excretas parasitadas en ambas temporadas fue de 75.9%, en lluvias 73.6% y en secas el
80%. La prueba de X2 no demostró diferencia signicativa entre temporadas (X2 = 0.553, g. l. = 1 P = 0.457). No se encontró diferencia en la
composición de especies entre temporadas ni entre localidades de acuerdo al análisis de escalamiento multidimensional no métrico. La carga
parasitaria del gato montés en la zona conurbada de Querétaro está constituida por nemátodos generalistas de carnívoros. Se registra por
vez primera a T. vulpis en L. rufus para México. Se encontró una alta prevalencia de S. stercolaris que podría signicar una interacción con las
poblaciones humanas, animales domésticos y silvestres según lo establecido en otros estudios con este mismo carnívoro. Este estudio es uno
de los primeros publicados sobre parásitos intestinales de L. rufus en ambientes antropizados de México, en donde se encontró que la compo-
sición y estructura de las comunidades parasitarias de este carnívoro podría indicar la tolerancia a la perturbación por las actividades humanas.
Key words: Bobcat; Nematodes; Parasites; Querétaro; Trichuris vulpis.
© 2018 Asociación Mexicana de Mastozoología,www.mastozoologiamexicana.org
8 THERYA Vol. 9 (1): 7-13
HELMINTHS OF BOBCAT IN MEXICO.
reported in several mesocarnivores inhabiting the Ajusco,
including L. rufus (Gallardo 2014).
The scarce biological information available on parasites
of wildlife hinders the development of prevention and con-
trol strategies and measures in the event of potential zoo-
noses of importance for humans. Toxocara cati is consid-
ered as a species with zoonotic potential. Previous studies
have reported a higher prevalence of this species in areas
where wild and domestic animals are found in sympatry, in
turn increasing the likelihood of contact with humans (Bev-
ins et al. 2012).
The objective of this study was to determine the compo-
sition of the parasite community in the faeces of the bobcat
(Lynx rufus) inhabiting areas surrounding the city of Quere-
taro, and testing for signicant dierences in parasite com-
position and prevalence between seasons. Based on the
available information on the composition and structure of
the parasite communities of the bobcat living in disturbed
environments in the United States. We expected to nd a
community of intestinal parasites dominated by generalist
species, typically associated with the presence of domestic
animals and habitat loss, in areas surrounding the city of
Queretaro.
Materials and Methods
Study Area. The study was carried out in four collection
sites in areas surrounding the city of Queretaro: El Cima-
tario National Park (PANEC), Joya-La Barreta Recreational
Area, ExHacienda La Machorra and the area adjacent to Los
Angeles dam in Mompani, all sites where the presence of
Lynx rufus has been reported (Figure 1).
El Cimatario National Park is surrounded by peripheral
suburbs of the city of Queretaro. It is located at 20.474° to
20.556° N, and -100.326° to -100.386° W, with a reported
area of 2,447 ha. It is a protected natural area dominated
Introduction
The bobcat (Lynx rufus) is one of the carnivores with the
broadest distribution in North America, stretching from
southern Canada to the Baja California peninsula and Oax-
aca in Mexico (Hall 1981; Romero 1993; Larivière and Wal-
ton 1997; Romero 1993). This carnivore inhabits a range of
environments, from pine, pine-oak and tropical deciduous
forests, scrubs and grasslands, to areas with high human
density, coexisting with domestic animals and wildlife
(Gehrt et al. 2010). The bobcat has shown tolerance to frag-
mented environments (Riley et al. 2004), hence increasing
the likelihood of contact with dogs and cats, with which
it may potentially share the parasitic load (Harrison 1998;
Medellín and Bárcenas 2009; Prough et al. 2009; Carver et
al. 2012; Kole et al. 2012; Valencia-Herverth and Valencia-
Herverth 2012; Hiestand et al. 2014).
Parasites reported for the bobcat are generalists of wild
and domestic mammals of the Order Carnivora, including
Alaria marcianae, Taenia rileyi, Physaloptera Cylicospirura
praeputialis, Felineus, Toxascaris leonina, T. mystax and Ancy-
lostoma tubaeforme for West Texas (Stone and Pence 1978),
while Paragonimus kellicotti, Spirometra mansonoides, T.
macrocystis, T. leonina, T. mystax, A. tubaeforme, Oslerus ros-
tratus, Molineus barbatus, Physaloptera rara and Troglostron-
gylus wilsoni were reported as typical components of the
bobcat parasitic community for West Virginia and Georgia
(Watson 1981). In a recent study, T. leonina, A. caninum,
Ancylostoma spp., and Taenia spp. were reported as parasite
species shared with other wild carnivores, such as coyotes
(Canis latrans) and pumas (Puma concolor) (Hiestand et al.
2014), while L. rufus shares Toxocara cati with dogs and cats,
mainly when the former lives in urbanized areas where con-
tact with domestic animals has been reported (Riley et al.
2004; Keesing et al. 2006; Carver et al. 2012; Mino-Botello
et al. 2016).
In recent years, a number of ecological studies have
been conducted on the bobcat in Mexico, making it pos-
sible to broaden its distribution range with new records
(Valencia-Herverth and Valencia-Herverth 2012), identify-
ing dierences in feeding patterns (Medellín and Bárcenas
2009), or evaluating the eect of landscape attributes on
its presence (Botello et al. 2006; Monroy and Briones-Salas
2012; García- Prieto et al. 2014; López-González et al. 2015;
Espinosa-Flores and Lopez-González 2016), to mention a
few examples. In Mexico, only three parasite species have
been formally registered for the bobcat, according to the
information available in the National Collection of Hel-
minths at the Institute of Biology, UNAM. These records
correspond to two nematodes, Toxascaris leonina and Phy-
saloptera praeputialis, and one cestode, Echinococcus oli-
garthra (Salinas-Lopez et al. 1996; García-Prieto et al. 2012).
Specically, for the study area, there is one study on the
presence of a cyst in the intestinal mucosa of a bobcat, and
the presence of the nematode P. praeputialis is reported for
the rst time for the state of Querétaro (Lopez-González
et al. 2012). Last, the presence of endoparasites has been Figure 1. Scat collection sites in areas surrounding the city of Queretaro, Mexico.
www.mastozoologiamexicana.org 9
Camacho-Macías et al.
by crasicaule (thick-stemmed) scrub and tropical deciduous
forest (Baltasar et al. 2004; López-González et al. 2015). The
PANEC is listed as a protected natural area where grazing,
reforestation, rewood collection, hiking and cycling activi-
ties take place.
The Joya-La Barreta Recreational Area, located in the
Santa Rosa Jauregui delegation, is part of the Santa Catarina
micro-watershed in the boundary between the States of
Queretaro and Guanajuato (20.809° N, - 100.528° W). It com-
prises six vegetation types, mainly oak forest, natural grass-
land, petrophytic vegetation (in ravines and gullies) and cra-
sicaule scrub. Its primary functions are ecological conserva-
tion and special protection, but subsistence activities such
as grazing and soil and rewood extraction are conducted
in the area, as well as recreational activities like camping and
hiking. The area of inuence of the park includes locations
such as La Barreta, La Carbonera and La Joya, where primary-
production activities such as maize cultivation, nomadic
livestock raising and rewood collection for domestic use
are performed (Hernández-Sandoval et al. 2005).
Mompani is a rural town where the “Los Angeles” dam
is located, in coordinates 20.711° N, -100.506° W. It is sur-
rounded by secondary vegetation, crasicaule scrubs, agri-
cultural areas and hills covered with tropical deciduous
forest where livestock raising and rewood collection for
domestic use are conducted (Pineda-Lopez et al. 2010).
Ex-Hacienda “La Machorra” is located in the municipality
El Marqués between communities El Rosario and Los Cués,
in coordinates 20.554° N, -100.286° W. The land is covered
by crasicaule scrub vegetation where livestock raising is
not practiced but materials such as gravel and stone are
extracted. To note, groups of feral dogs were observed in
and around collection sites during sampling periods, due to
the proximity of human settlements.
Scat Collection and Examination. Tracks were surveyed
weekly in search of scats and latrines during the rainy sea-
son (late May, July, September and October 2015) and the
dry season (early March and May 2016). Surveys were per-
formed at 1-week intervals to ensure the independence
of individual scats collected, as suggested in Hernández-
Camacho et al. (2011).
Scat samples were identied in the eld based on shape
(cylindrical and in clusters), size (approx. 1.5 to 2.5 cm wide
by 10.0 to 15.0 cm long), color (usually light gray or blackish
when fresh), composition (mostly hair and bone remains),
and association with lynx tracks adjacent to scats (Aranda
2012). Only fresh scats that did not break apart upon han-
dling were sampled, to avoid weathering and ensure the
potential presence of parasite dispersal stages. Scat sam-
ples were split into two halves, one was placed inside a
polyethylene bag with zipper and xed with 10 % forma-
lin following the methodology of Hernández-Camacho et
al. (2011). The other half was placed in a paper bag to be
tested for coproculture and as source of replicate samples.
Scat samples were labeled with the respective collection
data (sample number, date, collection site and georefer-
ence), and were stored at 4 °C until analysis.
Stool ova, parasite and coproculture tests. Stool samples
were analyzed with the Ritchie oat or formalin-ether test
to extract protozoan eggs, cysts and oocysts (Medina et al.
1994; Hernández-Camacho et al. 2011; Aranda et al. 2013).
Parasite eggs were identied based on morphometry under
a LEICA ICC50 HD light microscope using the software LAS
EZ Leica Application Suite version 3.1.1. Scat cultures and
larval migration tests were conducted aiming to obtain L3
larvae (Medina et al. 1994). The taxonomic identication of
eggs was conrmed under the microscope, by comparison
with the specialized literature (Taylor et al. 2007; Bowman
et al. 2011).
Statistical analysis. The total prevalence of parasites by
locality was expressed in percentage and was quantied
as the number of scat samples infected with any parasite
divided by the total number of scats per collection local-
ity and multiplied by 100. A Chi-square (X2) test was per-
formed to assess potential dierences between the collec-
tion seasons. The species composition of parasite commu-
nities was compared between sites and between seasons
through a non-metric multidimensional scaling (NMDS)
analysis, which is usually the method of choice for the
graphical representation of relationships at the community
level (Clarke 1993). This analysis was performed using the
Jaccard similarity index and the software PAST 2.17c (Ham-
mer et al. 2001).
Results
A total of 83 scat samples were collected for both seasons,
53 and 30 during the rainy and dry seasons, respectively.
Parasite eggs were identied to the lowest taxonomic level
possible, identifying a total of seven nematode species for
the bobcat: Trichuris vulpis, P. praeputialis, T. leonina, T. cati,
S. stercolaris, Uncinaria stenocephala and Ancylostoma sp.
A total prevalence of 75.9 % (n = 63) was observed in
the two collection seasons. For the rainy season, 73.6 %
of scat samples (n = 39) tested positive for at least one of
the six nematode species. S. stercolaris was the species
with the highest prevalence in the four sites (33.3 % in La
Machorra and 100 % in El Cimatario); the species with the
lowest prevalence were T. leonina (13.3%) and T. vulpis (20
%), which were found in only one site (La Machorra). For
the dry season, 80 % of scats tested positive (n = 24), with T.
cati and S. stercolaris as the most prevalent parasites, both
with a 100 % prevalence in El Cimatario; T. vulpis showed a
very low prevalence, observed only in Mompani (12.5 %).
The X2 test showed no signicant dierences in nematode
species between seasons (X2 = 0.553, d. f. = 1, P = 0.457).
The non-metric multidimensional scaling (NMDS) analysis
revealed no dierences in species composition between
seasons (Figure 2). Hence, this parameter was similar across
collection sites. T. leonina was found only during the rainy
10 THERYA Vol. 9 (1): 7-13
HELMINTHS OF BOBCAT IN MEXICO.
season, and U. stenocephala, during the dry season; both
parasite species were found only in La Machorra.
Discussion
The parasitic load of the bobcat in areas surrounding the
city of Querétaro consists of nematodes; this diers from
what is recorded for scat samples collected in the United
States, where a greater parasite diversity has been observed,
for the rst time in L. rufus for Mexico at La Machorra and
Mompani; this parasite was previously observed in scat of
gray fox at El Cimatario (Hernández-Camacho et al. 2011).
Strongyloides stercoralis showed a 100 % prevalence
in the dry season at El Cimatario National Park. This nd-
ing may indicate the contact of bobcats with humans and
domestic animals, as suggested in the study of Mino-Botello
et al. (2016) in the Tehuacán-Cuicatlán Biosphere Reserve.
In the specic case of El Cimatario, the presence of packs of
feral dogs has been documented (Hernández-Camacho et
al. 2016), which interact with wild carnivores (Hernández-
Camacho pers. com. 2017). This is similar to the situation
mentioned by Mino-Botello et al. (2016).
The identication of Ancylostoma sp. to species level
was not possible, despite the observation of distinctive
characters in eggs and larvae obtained from scat cultures.
However, A. tubaeforme and A. caninum have been recorded
in bobcats in the United States (Stone and Pence 1978;
Watson 1981; Hiestand et al. 2014). In the area adjacent to
Santiago de Queretaro, A. caninum has been observed in
stools of feral dogs and gray foxes; therefore, the Ancylos-
toma eggs and larvae found in this study likely correspond
to this species.
Toxocara cati is the most prevalent parasite in wild and
domestic cats (Bowman 2011). In this study, its prevalence
was low relative to the other nematodes found. This para-
site can be transmitted directly when eggs are ingested or
through paratenic hosts such as mice of the genus Peromys-
cus (Aranda et al. 2002; Bowman et al. 2002; García-Prieto et
al. 2012).
No signicant dierences were found in the composi-
tion of the parasite community between seasons, except
for T. leonina and U. stenocephala in La Machorra. The pres-
ence of T. leonina in the rainy season may be due to its life
cycle being favored by moisture and low temperatures, as
well as by the presence of eggs and L3 larvae in tissues of
rodents of the genus Peromyscus (Anderson 2000; Bowman
et al. 2011). The species recorded during the dry season
may be fostered by the presence of articial water bodies
in the study sites, which are favorable for the survival of
the dispersal stages. Other studies have reported that the
eggs of Toxocara sp. and Trichuris sp. are resistant to various
environmental factors, and hence remain viable in soil for
months (Mizgajska 2001; Rendón-Franco et al. 2013), until
there are suitable conditions for completing their life cycle.
Each of the four localities in this study show some
degree of anthropization, from El Cimatario National Park,
an area under conservation strategies, to areas with intense
human activity in La Machorra, associated with the extrac-
tion of construction materials, and Mompani, related to the
Santiago de Queretaro landll. All the localities studied
recorded parasite species that are generalists and resilient
to environmental disruption, which may point to the histor-
ical presence of human activities in these sites (Hernández-
Camacho et al. 2016).
Figure 2. Plot of the non-metric multidimensional scaling of the species
composition between the two seasons. White boxes indicate parasites recorded during
the rainy season; crosses, parasites recorded in the dry season. Polygons represent
seasons, the overlap shows that the composition of parasite communities is similar across
sites, regardless of season.
including trematodes, cestodes, protozoans, and acantho-
cephalans (Stone and Pence 1978; Watson 1981; Tiekotter
1985; Larivière and Walton 1997; Hiestand et al. 2014); how-
ever, all the nematode species recorded are generalists of
carnivores, which is consistent with our expectations. The
technique used for the analysis of stools is suitable for the
detection of the dispersal stages of many parasites (Hernán-
dez-Camacho et al. 2011). The presence of nematodes as
the only parasite group may be the result of the dierent
dispersal and transmission strategies used by these organ-
isms, favoring their survival in anthropic environments, as
is the case of the host-infection strategy or larva migrans,
which penetrates through the skin of foot pads, as well as
transplacental and transmammary transmissions (Ander-
son 2000). This great variety of options contrasts with those
in other parasite groups, such as trematodes, cestodes and
acanthocephalans, all of which require trophic transmis-
sion via intermediate hosts to complete their life cycle in
the denitive host (Bush et al. 2001).
Some of the nematode species found in this study have
also been recorded in feral dogs from the outskirts of Queré-
taro, such as S. stercoralis and Ancylostoma sp. (Fernández et
al. 2002; Cantó et al. 2011), and in the gray fox (Urocyon cine-
reoargenteus), also with S. stercoralis (Hernández-Camacho
et al. 2011), to mention a few examples. T. vulpis is recorded
www.mastozoologiamexicana.org 11
Camacho-Macías et al.
The parasite species found are generalists typical of
carnivores, with life strategies that allow them to survive
and persist in environments with anthropic activities. This
could indicate that the areas surveyed in this study have
undergone a steady long-term loss of biodiversity, where
the intermediary hosts of several parasite species are no
longer in the area (Laerty 1992; Laerty 2012, Hernández-
Camacho et al. 2016). On the other hand, domestic and wild
carnivores interact as predators and competitors. This leads
to a signicant impact on wild populations, with a negative
eect on the trophic structure of the remaining ecosystems
in the areas around cities. This may have negative health
eects on local inhabitants, by being increasingly closer
to zoonotic parasites (Riley et al. 2004; Gehrt et al. 2010;
Sepúlveda et al. 2014).
Acknowledgments
Thanks to M. T. Ponce Gaxiola and F. Smith Beltran for their
support in eld work; to S. L. Sosa Gallegos, a technician
of the Microbiology Laboratory at the Faculty of Veterinary
Medicine and Animal Sciences, Universidad Autónoma de
Queretaro for the advice; as well as to E. Romero Callejas
for guidance in the identication of the parasite eggs in
the Parasite Diagnosis Laboratory at Universidad Nacional
Autónoma de México during the stay of the rst author in
September 2016. This study was nanced by Red Temática
de Biología, Conservación y Manejo de la Fauna Nativa en
Ambientes Antropizados (Thematic Network for Biology,
Conservation and Management of the Native Fauna in
Anthropized Environments, REFAMA). Special thanks to M.
C. Pantoja Hernández for the elaboration of the map. This
study was partially funded by the project PRODEP UAQ-
PTC-313 DSA/103.5/16/10199. María Elena Sánchez-Salazar
translated the manuscript into English.
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Associated editor: Rafael Avila
Submitted: May 31, 2017; Reviewed: July 15, 2017;
Accepted: November 11, 2017; Published on line: January 15, 2018.
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