ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
CRUORIFILARIA TUBEROCAUDA EBERHARD, MORALES & ORIHEL, 1976 (SPIRURIDA:
FILARIOIDEA) IN CAPYBARAS (HYDROCHOERUS HYDROCHAERIS LINNAEUS, 1766)
FROM VENEZUELAN LLANOS
CRUORIFILARIA TUBEROCAUDA EBERHARD, MORALES & ORIHEL, 1976 (SPIRURIDA:
FILARIOIDEA) EN CAPIBARAS (HYDROCHOERUS HYDROCHAERIS LINNAEUS, 1766) DE
LOS LLANOS DE VENEZUELA
1Instituto de Zoología y Ecología Tropical. Facultad de Ciencias, Universidad Central de Venezuela. Apartado Postal 47058.
Caracas 1041-A, Venezuela. israel.canizales@ciens.ucv.ve
2Instituto de Zoología y Ecología Tropical. Facultad de Ciencias, Universidad Central de Venezuela. Apartado Postal 47058.
Caracas 1041-A, Venezuela. ricardo.guerrero@ciens.ucv.ve
1 2
Israel Cañizales & Ricardo Guerrero
ABSTRACT
Keywords: Capybara – Cruorifilaria – Filarias – Kidney – Size
The occurrence of a previously known parasite of capybara in Venezuela a new type of lesion in the
kidneys host produced by the presence of filarioid worms of the species Cruorifilaria tuberocauda
Eberhard, Morales & Orihel, 1976 (Spirurida, Filarioidea) are described, including and evaluation if the
burden of filaroids affect the weight of the kidneys and the size of capybaras. A total of 200 filaroid
nematodes identified as C. tuberocauda parasitizing kidney blood vessels were obtained in 13 of 41
capybaras (Hydrochoerus hydrochaeris Linnaeus, 1766) (Rodentia, Hydrochaeridae) sacrificed during
the 2014 annual harvest in Alto Apure, Venezuela. Cortical cysts of varying sizes, between 0.5 cm and 2.5
cm in diameter, were found in each of these animals. The overall prevalence in the present study was
31.71%, with a mean intensity of 4.88 parasites per host and values of 15.38 parasites per mean abundance
2
host. The coefficient of determination R for each sex attributes to the ratio of foot length and parasitic
burden a value of 0.03 to 19.27%, and to the ratio of kidney weight and parasite burden a value of 0.16 to
14.42%, suggesting that the relationship between these variables is weak. The analysis of variance
determined that these variables are not significantly different (P = 0.46). No significant relationship was
found by sex between growth (foot length) or kidney weight and intensity of worm infections.
Neotropical Helminthology
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Neotropical Helminthology, 2017, 11(2), jul-dic: 331-341
INTRODUCTION
332
RESUMEN
Palabras claves: Capibara – Cruorifilaria – Filarias – Riñón – Tamaño
Se describe la presencia de un parásito previamente conocido en capibaras en Venezuela, un nuevo tipo de
lesión en los riñones del hospedador producido por la presencia del nematodo filarioideo Cruorifilaria
tuberocauda Eberhard, Morales y Orihel, 1976 (Spirurida, Filarioidea) y se evalúa si la carga de estos
afecta el peso de los riñones y el tamaño de los capibaras. Se obtuvo un total de 200 nematodos filaroideos
identificados como Cruofilaria tuberocauda Eberhard, Morales y Orihel, 1976 (Spirurida, Filarioidea)
parasitando los vasos sanguíneos de riñón en 13 de 41 chigüires (Hydrochoerus hydrochaeris Linnaeus,
1766) (Rodentia, Hydrochaeridae) sacrificados durante la cosecha anual 2014 en el Alto Apure,
Venezuela. Se hallaron quistes corticales de tamaño variables, entre 0,5 cm y 2,5 cm de diámetro en cada
uno de estos animales. La Prevalencia general en el presente estudio fue 31,71%, con una densidad
absoluta de 4,88 parásitos por hospedador y valores de densidad relativa de 15,38 parásitos por
2
hospedador. El coeficiente de determinación R para cada sexo atribuye a la relación longitud del pie y
carga parasitaria un valor de 0,03 a 19,27% y a la relación peso del riñón y carga parasitaria un valor de
0,16 a 14,42% por lo que se considera que la relación entre estas variables es débil. El análisis de varianza
determinó que estas variables no son significativamente diferentes (P = 0,46). No se encontró relación
significativa entre el sexo y el crecimiento (longitud del pie) o el peso y la intensidad de la infección
parasitaria.
owned lands in the Apure, Barinas, Cojedes and
Portuguesa states (Fig. 1).
El Hato El Cedral, located in Apure state, is
incorporated into the program of Sustainable
Management of natural populations of capybaras
in 1991, since 1996 is the largest producer in
Venezuela. Population censuses have allowed the
allocation of annual harvest quotas of just less than
1.000 to 4.000. The years 1995 and 1997, as well as
the period 2008 - 2012 did not realize the annual
harvest; the activity is restarted in 2013 with a
quota of 3,000 individuals for the seasons 2013 -
2014.
On the other hand, Cañizales & Guerrero (2013)
indicated at least 80 different species of parasites
(ecto and endo) that have been described for
capybaras throughout its natural distribution range.
Ojasti (1973, 2011) in his studies on capybara in
Venezuela, refers to the presence of a type of
endoparasite helminth affecting the lung and
kidney in 55.4% of 139 adult animals, while
Rodríguez et al. (1975) in 38% of 16 adult animals
in Colombia. Eberhard et al. (1976) taxonomically
classified these filarial-type nematodes as
Cruorifilaria tuberocauda gen. et sp. n (Nematoda:
Among the species of wildlife in Venezuela,
capybara (Hydrochaerus hydrochaeris Linnaeus,
1766) has been exploited since the colony
(Humboldt, 1826) and is the main alternative
source of animal protein for human consumption in
several states of the country, on the other hand the
use of their skin is restricted to the residents in the
rural area of Venezuela. Commercial use of the
species begins in the late 1950s (Fergusson, 1990).
Between 1962 and 1967 a general prohibition for
the use of the wild fauna in Venezuela was decreed.
It was during the closure that Ojasti (1973) carried
out the studies that allowed knowing the biological
information necessary for the structuring and
proposal of a management plan according to the
characteristics of the resource, which has been
adapted and modified over time (González
Jiménez, 1995). At present, the program of
commercial exploitation of the species in
Venezuela, is based on biological information and a
management plan that specifies that the extraction
is allowed up to a maximum of 20% of the total
population of individuals, with a higher live weight
to 35 kg and can only be carried out on privately
Neotropical Helminthology, 2017, 11(2), jul-dic Cañizales & Guerrero
Filarioidea). This species has been reported in
Colombia (Eberhard et al., 1976), Venezuela
(Campos-Aasen & Planas, 1986) and Brazil (Costa
& Catto, 1994, Nascimento et al., 2000).
Microfilariae circulate in the peripheral blood
vascular system been found in the skin of top of the
head, back an ears (Eberhard et al., 1976, Yates &
Jorgenson, 1983) demonstrating peak
concentrations between 600 to 1000 hours (Yates
& Hellner, 1989). These finding suggest that
natural vector may display biting activity on these
skin areas and in the morning hours.
Ojasti (1973) observed injuries in the kidneys of
capybaras, produced by filarias. C. tuberocauda
produces a severe arterial injury at the level of
kidney and lung, which could generate the
formation of arterial thrombosis and areas of
degeneration and ischemia. The presence of adult
parasites in the blood vessels of the kidney causes
an inflammatory response with thickening of the
inner walls characterized by the growth of hairy
projections towards the lumen as in an attempt to
keep the parasite away from the walls (Planas &
Campo-Aasen, 1978, Morales et al., 1978). This
type of alterations cause chronic renal failure,
although it has not documented in capybaras, it is
well known in domestic animals as well in
laboratory rodents, this disorder specifically
affects the growth plate, located at the ends of the
long bones, which is formed by cartilage and
adjacent bone. Causing variations in the secretion
of growth hormone, largely explained by the
reduced food intake and nutritional deficiencies
characteristically accompanying chronic renal
disease and non-specific "per se" of this pathology
(Ettinger, 2007). Also, Ojasti (2011) points to foot
length as an important indicator of growth in
capybaras. We could then assume that the presence
of C. tuberocauda has an effect on body
dimensions in both male and female H.
hydrochaeris.
The objectives proposed in this study were: to
identify the macroscopic findings present in the
kidneys parasitized by C. tuberocauda, to evaluate
the prevalence, absolute density, relative density
and infection index of C. tuberocauda parasitic
populations, and to determine the potential
association between the foot length and the kidney
weight of the hosts with the parasite burden of C.
tuberocauda.
MATERIALS AND METHODS
333
The work area known as the Alto Apure, is
characterized by being flooded savannahs during
the rainy season. Its physiognomy is mostly open
grassland with almost continuous grassland
coverage, the canyons and larger rivers are flanked
by gallery forests. The main climatic characteristic
of this region is the alternation of dry or summer
seasons (November to April) and rainy season or
winter (May to October), with annual rainfall close
to 1.500 mm. The annual average temperature is 27
° C, and the daily variation is between ± 9.5 ° C.
The warmest month is April with an average
temperature of 29 ° C.
All samples collected come from adult animals (n =
41) during the beginning of the annual harvest
season (March 2014) on Hato El Cedral grounds
(7º 23 'N, 69º 20' W) administered by the Instituto
Nacional de Tierras with an area of 53,000
hectares, which is located to the west of Apure
state, between the towns of Mantecal and Elorza
(Fig. 1). This ranch has a system of dikes that
diminishes the effect of the seasons when retaining
water during the summer and to diminish the
extension of the flood in the winter.
The killing takes place in the open air. Once an
animal has died, evisceration is performed.
Simultaneously, the kidneys were separated by
cutting blood vessels and the perirenal capsule, and
the foot length (right hind limb) was obtained by
measuring from the tip of the middle finger to the
base of the heel using a 1:100 scale metal ruler
adjusted to one millimeter. The organs were placed
in plastic bags and were closed and labeled with sex
and foot length. This material was transferred to the
field laboratory for initial processing. First, the
kidneys were washed in running water to remove
unwanted tissue and traces of blood and a first
visual inspection was performed to determine
some distinctive feature present in the organ.
Individual weighing of each kidney was performed
using a manual scale weighing 1 milligram, and
stored in a clean plastic bag with 4% formalin
solution. At a later stage, the organs were
macroscopically reviewed in the laboratory, both
externally and internally, to record their status and
perform the corresponding dissections to collect
the filarias. All adult parasites collected were
Neotropical Helminthology, 2017, 11(2), jul-dic Cruorilaria tuberocauda in Hydrochoerus
334
RESULTS
washed in isotonic saline solution and fixed in 70°
Ethanol later. For identification, the criteria of
Eberhard et al. (1976) were followed. All
measurements are given in micrometers (µm), to
measurements and figures a Microscope Nikon
Labophot YF-21E with Camera DS-Fi1 and
Control Unit DS-L2 with software to
measurements, an ocular micrometric to verify
measurements was used. All parasites were
deposited in the parasitology collection of the
Museum of Biology of the Central University of
Venezuela.
Analysis of data
For the determination of the parasite indices of
Prevalence, Mean Intensity, Mean Abundance
(Morales & Pino, 1991; Bush et al., 1997) and
Infection Index (Guerrero, 2007) were used. The
Infection Index is known as number of individuals
of a particular parasite species in a single infected
host. It estimates the presence of rare but very
abundant species and species very frequent but
little abundant. For the calculation, the number of
individuals of a parasite species present in the total
number of both infected and non-infected hosts
multiplied by the number of infected hosts divided
by 100.
In order to know if there is a relationship between
the weight of both kidneys and foot length with
parasite burden, simple linear regression and an
analysis of variance (ANOVA) were used to
determine if there were significant differences in
these biometric variables between the sexes.
Although the objective of assessing compliance
with the criteria for the selection of animals for
commercial use was not formulated, it was possible
to verify on the spot (during the harvests 2012,
2013 and 2014) that the selection criteria for adult
or old animals were not applied.
A total of 81 kidneys were obtained from 41
individuals sacrificed, one of the animals presented
unilateral kidney atresia. The parasitized kidneys
externally had no macroscopically visible damage
or alteration in size, shape or coloration. By touch,
the kidneys had typical consistency. The most
important macroscopic findings were observed
internally in the sagittal sections of the kidney, (1)
thickening and calcification of the walls of blood
vessels in the same way as described by Morales et
al. (1978), Planas & Campo-Aasen (1978), Matos
Vieira et al. (2006), and Silva et al. (2015). For
more detailed information of anatomic pathology
see the above-mentioned authors. (2) Presence of
corticomedullary cysts of sizes between 0.5 cm and
2.5 cm in diameter closely attached to the renal
parenchyma with translucent serous fluid
delimited by a thin wall (≤0.1 mm) of whitish
fibrous tissue. There were no changes in color in
the surrounding tissue. All cysts were located
between the anterior pole and the middle third of
the affected kidneys. No parasitic forms were
observed in any of the cysts. These structures have
not been previously reported in capybaras.
Therefore this constitutes the first known report
(Fig. 2).
A total of 200 nematodes were found parasitizing
the blood vessels of the kidneys of 13 animals.
Females with 150 nematodes were the ones with
the highest parasite load against 50 in males.
Although the infection was bilateral, the greatest
number of parasites (154) was found in the left
kidney, the remaining 46 were located in the right
kidney. number of filarioids found In relation to the
per kidney these ranged from 3 to 64 parasites.
These nematodes were identified as C.
tuberocauda following the criteria defined by
Eberhard et al. (1976) as follows: males have two
spicules, a large spicule of between 290.00 and
315.00 μm (306.66 ± 14.43) and a small one of
between 50.00 and 60.00 μm (55.00 ± 5.00). Total
length between 17.72 and 19.02 mm (18.15 ±
0.75), esophageal length between 1.43 and 1.56
mm (1.47 ± 0.07), and a tail length between 145.00
and 155.00 μm (150.00 ± 5.00), females generally
have a total length of between 27.50 and 31.00 mm
(28.91 ± 1.62), the length of the esophagus between
1.55 and 1.79 mm (1.67 ± 0.16) and a tail length of
between 200.00 and 230.00 μm (218.75 ± 14.36)
(Fig. 3).
Values of prevalence (%), , mean intensity mean
abundance, and infection index by sex are
presented in Table 2.
Neotropical Helminthology, 2017, 11(2), jul-dic Cañizales & Guerrero
335
Figure 1. Implementation area of the Capybara Commercial Use Program in Venezuela. = Ranch location.
Figure 2. Kidney cross section. The location in the renal cortex is observed. Photo: I. Cañizales. 12X
Neotropical Helminthology, 2017, 11(2), jul-dic Cruorilaria tuberocauda in Hydrochoerus
336
Figure 3. Cruorilaria tuberocauda (A) anterior end (B) tail of the male. Photos: R. Guerrero. 1000X
(A) (B)
Figure 4. Dispersion diagram of parasite burden and foot length of the hosts by sex.
Neotropical Helminthology, 2017, 11(2), jul-dic Cañizales & Guerrero
337
Figure 5. Dispersion diagram of parasite burden and kidney weight of hosts by sex.
Table 1. Biometric data of kidneys and foot length of Capybara.
Weight (g) Size(mm)
Left kidney
(Mean
± SD)
Right kidney
(Mean
± SD) Both
(Mean
± SD)
Foot length
(Mean ± DE)
This study
(n = 41)
94,71 ± 37,33
89,90 ± 39,41 181,54 ± 71,33
229,88 ± 9,39
Ojasti, 1973
(n = 110) 188,58 ± 52,95 233,08 ± 7,85
SD = Standar Deviation, n = sample size
Neotropical Helminthology, 2017, 11(2), jul-dic Cruorilaria tuberocauda in Hydrochoerus
Sexual dimorphism in capybaras manifests in
males of larger size compared to females,
therefore, one could expect variation in parasite
burden with respect to sex host in response to this
characteristic. Regressions between the foot length
and kidney weight of the hosts were made for both
sexes. Figures 4 and 5 show the distribution of the
2
data and its trend line. The corresponding R
determination coefficients are reported for each
sex.
Observing the scatter plots corresponding to males
and females, the points show a random type
arrangement. However, when graphing trend lines,
in the case of males has a negative slope. Therefore,
if there is a relationship between the variables, it
will not be linear. In females the trend line has a
positive upward slope. This suggests that there is
some relationship between the variables, although
clearly not linear. In relation to the values reported
by each determination coefficient for each sex,
these vary from 0.0003 to 0.1937, that is 0.03 to
19.27% of the variation in the parasitic burden can
be attributed to relationship with the length of the
foot, so it is considered that the relationship
between these variables is weak.
Scatter plots corresponding to males and females,
the points show a random type arrangement.
However, when plotting trend lines, in both cases
they have a positive upward slope. This suggests
that there is some relationship between the
variables, although clearly not linear. In relation to
the values reported by each determination
coefficient in each sex, these vary from 0.0016 to
0.1442, that is 0.16 to 14.42% of the variation in the
parasitic burden can be attributed to relation with
the weight of the kidney, reason why is considered
that the relation between these variables is weak.
To evaluate whether or not differences between
sexes for foot length and kidney weight with
parasite burden were significant, an analysis of
variance (ANOVA) was performed. The analysis
determined that these variables were not
significantly different (F = 1.03; P = 0.46, Fc =
1.69).
338
Table 2. Prevalence, , , infection index of Cruorilaria tuberocauda.mean intensity mean abundance
Prevalence%
Mean intensity Mean abundance
Infection index
Males 29.41
(5/17)
2.94
10.00 0.87
Females 33.33
(8/24)
6.25
18.75 2.08
General 31.71 (13/41) 4.88 15.38 1.55
(/) = animals parasitized/simple size
DISCUSSION Although injuries caused by C. tuberocauda have
been described in detail by Eberhard et al. (1976),
Morales et al. (1978), Planas & Campo-Aasen
(1978), Nascimento et al. (2000) and Matos Vieira
et al. (2006), in none of these studies is pointed the
presence of cortical renal cysts associated with the
presence of this nematode. Macroscopically, the
cysts are mainly located in the renal cortex and vary
from 0.5 cm to 2.5 cm in diameter with the presence
within of an aqueous and translucent liquid (Fig. 2).
In order to be able to compare our results of total
parasite burden with similar other studies with
The artificial selection of bigger size animals
favoring the survival of smaller or the random
selection of animals below the norm established in
the area of work and that to a certain extent affects
the populations dynamics of capybaras, such as
those associated with reproductive processes,
could explain the observed differences between the
values obtained in kidney weight and foot length by
Ojasti (1973) and this study of 3.73% and 1.37 %
respectively (Table 1).
Neotropical Helminthology, 2017, 11(2), jul-dic Cañizales & Guerrero
339
(Leidy, 1856), Acanthocheilonema reconditum
(Grassi, 1890), in which a hematophagous vector
participates as a transmission mechanism of
microfilariae. In a similar way C. tuberocauda also
is not the only known species whose is present in
the kidney of a definitive mammalian host,
Dioctophyma renale (Goeze, 1782) commonly
referred to as the "giant kidney worm" is a parasitic
roundworm (Ascaridida: Dioctophymatidae)
whose mature form is found in the kidneys of
mammals.
Eberhard et al. (1976) proposed that this rodent is
not the natural host of the parasite due to the
severity with which the parasitized tissue of the
kidney responds to this species, however, the
extent of organ damage by a parasite is not
necessarily evidence of an abnormal host. D.
renale usually destroys the kidney completely and
canids, felids and mustelids serve as the usual
definitive hosts.
Finally, among the hematophagous arthropods
present in the "Hato El Cedral" we can point out
acari (Ixodidae, Macronyssidae), lice
(Menoponidae) and mosquitoes (Culicidae).
Villarroel & Navarro (2014) report the genus
Mansonia, Anopheles and Culex which are
involved in the transmission of D. immitis, Setaria
labi a t opapi l l osa (Alessandrini, 1838),
Acanthocheilonema reconditum among others, as
well as Mansonia and Coquillettidia that have been
involved in the transmission of different
arboviruses such as Venezuelan Equine
Encephalitis Epizootic and West Nile Virus,
Aedomyia squamipennis (Lynch Arribálzaga,
1878) which is a vector of Gamboa virus and avian
malaria (Machado-Allison 1982). Anopheles
nuneztovari (Gabaldón, 1940), the most important
vector of human malaria in the Venezuelan plains,
especially in Barinas and Apure, would be
reasonable to consider that one of the species
representing these genera participates as potential
vectors of C. tuberocauda. However, Lefoulon,
Bain, Bourret, Junker, Guerrero, Cañizales et al.
(2015) in a study of the phylogeny and evolution of
filarias, mention C. tuberocauda as part of a clade
composed by the genera Dipetalonema,
A c a n t h o c h e i l o n e m a , M o n a n e m a ,
Cercopithifilaria, Yatesia and Litomosoides that
show adaptation for its transmission to a more
appropriate group of vectors: ticks and mites. In
sample size, a in an area with ge-composition
similar characteristics, we must mention that we
did not find published works that complied with
these requirements. When we compared the data of
this study, 200 parasites in 41 adults' animals, with
the findings of Nascimento et al. (2000) of 380
parasites in 36 animals in Mato Grosso in Brazil, it
could be concluded that the parasitic burden in our
case is lower however the influence by the age-
composition of the host sample must be considered
(25 individuals adults and 11 individuals of six
months old). This gives us a mean of 4.88
parasites/host in this study compared to the 10.56
parasites/host study Nascimento et al. (2000). The
overall prevalence in the present study was
31.71%, lower than the 55.4% reported by Ojasti
(1973), 52.7% by Nascimento et al. (2000) and
38% by Rodríguez et al. (1975). Likewise, the
mean intensity values of C. tuberocauda in the
present study were 4.88 parasites per host and
differ from that found by Costa & Catto (1994) in
Pantanal chigüires from the state of Mato Grosso
do Sul of 8 parasites per host, and Nascimento et al.
(2000) who observed a mean intensity of 20.70
parasites per host. On the other hand, the mean
abundance values of C. tuberocauda in the present
study were 15.38 parasites per host, exceeding
Nascimento et al. (2000) of 10.94 parasites per host
finding. Likewise, the infection rate with an overall
value of 1.55 allows us to conclude that in general
the natural populations of capybaras in this study
are less parasitized than the natural populations in
other countries within the natural range of the
species.
Much has been discussed about the effect that sex
and host size may have on parasite burden (Folstad
& Karter, 1992; Schalk & Forbes, 1997; Krasnov
et.al., 2005; Gorrell & Schulte-Hostedde, 2008) in
capybaras sexual dimorphism manifests in males
of larger size compared to females, so some
variation in response might be expected to this
characteristic. In this study the results obtained
from the corresponding analyzes determined that
there is no direct relationship between the
variables.
On the other hand, the definitive location of
nematodes adult form in circulatory system in a
mammalian host is not unique of C. tuberocauda,
there are other species of the Onchocercidae family
that live in arteries such as Dirofilaria immitis
Neotropical Helminthology, 2017, 11(2), jul-dic Cruorilaria tuberocauda in Hydrochoerus
340
summary, so far the vector responsible for the
transmission of C. tuberocauda is not known.
ACKNOWLEDGEMENT
To the Institute of Zoology and Tropical Ecology
and to the Research Coordination of the Faculty of
Sciences of the Central University of Venezuela. To
the Management of the Social Agroecological
Company Bravos de Apure (Hato El Cedral). To the
National Land Institute. To the staff of the Matiyure
camp, workers and staff of Hato El Cedral. Without
the help of all of them, this work could not have
been done.
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