ORIGINAL ARTICLE /ARTÍCULO ORIGINAL
OCCURRENCE OF HETEROPRIAPULUS HETEROTYLUS (MONOGENOIDEA:
DACTYLOGYRIDAE), ECTOPARASITE OF TWO INVASIVE SAILFIN CATFISHES
(SILURIFORMES: LORICARIIDAE) FROM THE SOUTHEASTERN MEXICO
OCURRENCIA DE HETEROPRIAPULUS HETEROTYLUS (MONOGENOIDEA:
DACTYLOGYRIDAE), ECTOPARASITO DE DOS PECES GATO INVASORES
(SILURIFORMES: LORICARIIDAE) EN EL SURESTE DE MEXICO
1,2* 3,4 5 2
María Amparo Rodríguez-Santiago , Mayra I. Grano-Maldonado , Enrique Ávila & Samuel Gómez
1Catedras CONACyT, Universidad Autónoma del Carmen, Facultad de Ciencias Naturales, Centro de Investigación de
Ciencias Ambientales (CICA), Av. Laguna de Términos s/n Col. Renovación 2da Sección, C.P. 24155 Ciudad del Carmen,
Campeche, México. Tel. 938 93811018 EXT 180. *Current address corresponding author: marodriguez@conacyt.mx ,
amparoshalom@hotmail.com
2Instituto de Ciencias del Mar y Limnología, Unidad Académica Mazatlán, Universidad Nacional Autónoma de México, Joel
3
Montes Camarena s/n, 82040. Mazatlán, Sinaloa. samuelgomez@ola.icmyl.unam.mx Departamento de Ecofisiología,
Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa. Paseo Claussen s/n. A.P. 610. Mazatlán, Sinaloa.
4
México. CCMAR-CIMAR L.A., Centro de Ciências do Mar; Universidade do Algarve, Faro, Portugal
grano_mayra@hotmail.com; mgmaldonado@ualg.pt
5Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Estación El Carmen, Carretera
Carmen-Puerto Real km. 9.5, 24157, Ciudad del Carmen, Campeche, México. kike@ola.icmyl.unam.mx
Neotropical Helminthology, 2015, 9(1), jan-jun: 55-64.
ABSTRACT
Keywords: Dactylogyridae – Heteropriapulus - invasive fish – Loricariidae – Mexico - non-native fish.
The present study reports the presence of the dactylogyrid parasite Heteropriapulus heterotylus
on the gills of the invasive Amazon sailfin catfishes Pterygoplichthys pardalis and P. disjunctivus
from freshwater ecosystems in Southeastern Mexico. This represents a new host record for this
parasite and a new geographical record of parasites for P. disjunctivus and P. pardalis.
Furthermore, the ecological aspects of the prevalence, mean abundance and mean intensity of H.
heterotylus were examined throughout an annual cycle. A total of 223 fish were collected,
including 94 of P. disjunctivus and 129 of P. pardalis. A total of 148 (66.3%) fish were found to be
infected with this dactylogyrid, 79 of P. pardalis and 69 of P. disjunctivus. H. heterotylus was
found exclusively in the gill arches in both hosts. In both fish, the mean abundance of this parasite
showed significant changes during the year. Likewise, prevalence and mean intensity showed
similar values in both hosts. The present study demonstrates that parasitological studies in non-
native fish can be helpful in designing control strategies for the importation of non-native fish and
should be regarded as necessary before encouraging fish consumption as a control strategy in
regions where these invasive fish proliferate excessively.
55
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
INTRODUCTION
56
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015
The introduction of exotic or non native
aquatic species is one of the most critical
environmental risks currently facing native
species, aquatic habitats and biodiversity in
general (Torres-Orozco & Pérez-Hernández,
2011). This phenomenon is responsible for the
extinction of 54% of the world's native aquatic
fauna, 70% of fish in North America and 60%
of Mexican fish (IMTA et al., 2007). Amazon
sailfin catfishes (Siluriformes: Loricariidae)
are among the exotic fish that pose the most
serious threat to tropical and subtropical
freshwater regions (Liang et al., 2005, Chavez
et al., 2006; Nico, 2010). Native to South
America, these fish have been introduced
across the world by the aquarium trade and
occasional escapes due to owner carelessness
and have now established themselves in
tropical and subtropical freshwater bodies. For
example, Pterygoplichthys pardalis
(Castelnau, 1855) and Pterygoplichthys
disjunctivus (Weber, 1991) are reportedly
destroying cages and nets and causing a
decline in native, more desirable fish in
Laguna de Bay, Philippines (Chavez et al.,
2006). P. disjunctivus attaches to the skin of the
Endangered native Florida manatee
(Trichechus manatus ssp. latirostris) and feeds
on their epibiota. In some instances dozens of
P. disjunctivus and manatees appeared
agitated. This interaction may be detrimental
to manatee but remains unclear (Nico et al.,
2009). P. pardalis damage fishing gear and gill
nets in various locations of Mexico (Wakida-
Kusunoki et al., 2007). The introduction and
subsequent establishment of the amazon
sailfin catfish species P. pardalis and P.
disjunctivus in extraneous ecosystems has
been demonstrated. Recently, these fish
species were listed among the top 30 invasive
species in Taiwan (Lee et al., 2006). They prey
on and compete with native species (Hill &
Lodge, 1999), spread parasites and pathogens
(Torchin et al., 2003; Torchin & Mitchell,
2004), cause unexpected hybridization
RESUMEN
Palabras clave: Dactylogyridae – Heteropriapulus – Loricariidae – México - peces invasores - peces no nativos.
El presente estudio reporta la presencia del parásito dactylogirido Heteropriapulus heterotylus en
las branquias de peces invasivos Pterygoplichthys pardalis y P. disjunctivus en ecosistemas de
agua dulce del sureste de México. Este studio representa un nuevo registro de hospederos para
este parásito y un nuevo registro geográfico de parasitos en P. disjunctivus y P. pardalis. Además,
se examinaron los aspectos ecológicos de la prevalencia, abundancia media e intensidad media de
H. heterotylus a través de un ciclo anual. Se recolectaron un total de 223 peces, incluyendo 94 de
P. disjunctivus y 129 de P. pardalis. Se encontró un total de 148 (66.3%) peces que estaban
infectados con este monogeneo, 79 de P. pardalis y 69 de P. disjunctivus. H. heterotylus se
registró exclusivamente en los arcos branquiales en ambos peces. En ambos peces la abundancia
media de este parasito mostró cambios significativos a través del año. Asimismo, la prevalencia e
intensidad media mostraron valores similares en ambos hospederos. El presente estudio
demuestra que los estudios parasitológicos en peces exóticos o no nativos pueden ser útiles en el
diseño de estrategias de control para la importación de estos peces y deben ser considerados como
necesarios antes de fomentar el consumo de peces como una estrategia de control en las regiones
donde estos peces invasores proliferan en exceso.
Rodríguez-Santiago et al.
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015
(Gaskin & Schaal, 2002; Mallet, 2007) and
economic loss to fisheries (Chavez et al., 2006;
Nico, 2010), and may ultimately cause a
decrease in local biodiversity by eliminating
local species (Chapin et al., 2000; Dick &
Platvoet, 2000).
In Mexico, the presence of Loricariids in wild
environments was first reported in the mid-90s
(Guzman & Barragán, 1997). In 2007, Wakida-
Kusunoki et al. reported the presence of P.
disjunctivus and P. pardalis (Actinopterygii,
Loricariidae) in freshwater ecosystems of
Southeastern Mexico. Currently, these species
are listed as one of the top invasive species in
Mexico (Mendoza-Alfaro et al., 2011), and
they continue to spread through wild
environments (rivers, streams, reservoirs and
lakes) in several parts of the country,
proliferating excessively. The main impact of
the introduction of these fish is the competition
for space and food with native species,
including commercial fish species (Martínez-
Palacios et al., 2010a, 2010b; Wakida-
Kusunoki et al., 2011; Sandoval-Huerta et al.,
2012). Despite the threat P. disjunctivus and P.
pardalis pose, there is currently little
information available about their parasitic
fauna (Mendoza-Franco et al., 2012). Some
species of monogenea, such as Gyrodactylus
cichlidarum, Dactylogyrus vastator (Caspeta
et al., 2009) and G. anguillae (Grano-
Maldonado et al., 2011), are regarded as high
risk in aquaculture because they are associated
with native fish mortalities. In this study, we
report for the first time the presence of H.
heterotylus, a dactylogyrid ectoparasite
specific to the gills of P. pardalis and P.
disjunctivus, in the freshwater ecosystems of
Southeastern Mexico and compare the
abundance and prevalence of the
monogenoidean in these coexisting congener
hosts and determine whether the inter-annual
variability in the abundance of this parasite in
each fish is related to the water temperature
and/or the host size and weight.
In 2012, invasive sailfin catfish specimens
were captured from freshwater ecosystems in
Campeche in Southeastern Mexico. Fish
specimens were sacrificed by decapitation to
ensure a fast dead, which is according to
Mexican laws (NOM-033-ZOO-1995). The
fishing area was located in the Palizada River
within the Flora and Fauna Protection Area
o
Laguna de Terminos (la Rivera: 18 20'01”N,
o
91 41'55”W). The fish were caught
(bimonthly) between February and December
2012 with fishing nets (mesh = 76 mm) and
transported alive (individually) to the
laboratory in plastic containers. At each
sampling site, the bottom water temperature
w a s r e c o r d e d u s i n g a
salinity/conductivity/temperature meter (YSI-
30, Ohio 45387 USA). For each fish, the
results of the parasitological examination as
well as the fish's total length (cm), standard
length (cm) and weight (g) was recorded. The
parasitological survey included a revision of
external organs: eyes, fins, skin, and gill
cavities. The gill cavities were individually
separated and subsequently checked by
compression between two 10 x 10 x 1.0 cm
glasses (Guzman-Cornejo et al. 2012). The
parasites were preserved in individual labeled
vials with 96% alcohol until definitive
identification. The monogenoideans were
individually mounted on a slide, and the
proteolytic digestion method was used to
release the surrounding tissue of the haptoral
sclerites (see detailed method in Harris &
Cable, 2000). Complete specimens were
mounted in Gray and Wess media to clear the
tissue and visualize the sclerites and male
copulatory organ. The specimens were
examined under an Olympus BX-51
microscope. The identification of the
dactylogyrid species was based on the
characteristics of the sclerotized hard parts of
the haptor and the male copulatory organ. The
body morphology and sclerotized organs of
Heteropriapulus ectoparasite of two invasive sailfin
MATERIALS AND METHODS
57
58
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
each individual were photographed using a
digital camera (Olympus C-5050 Zoom)
attached to a microscope. These ectoparasites
were stained with Gomori's trichrome or
Mayer's carmine to determine the internal
features as described by Kritsky et al. (1986).
The parasites were identified using keys
proposed by Jogunoori et al. (2004) and
Kritsky (2007). The parasitological material
was deposited in the National Helminths
Collection of the Institute of Biology of the
National Autonomous University of Mexico
(CNHE-IBUNAM). The prevalence (%),
mean intensity (total number of parasites of a
particular species found in a sample/the
number of hosts infected with that parasite)
and mean abundance (number of
individuals/host) of the parasites were
determined as described by Bush et al. (1997).
To assess significant variations in the mean
abundance of parasites over seasons, a
Kruskal-Wallis non-parametric analysis of
variance was performed, which was followed
by Tukey HSD post hoc test (Steel & Torrie,
1986). To assess significant differences
between mean abundance and mean intensity
of parasites between both fish hosts Mann-
Whitney U test was used. Spearman rank
correlations were used to assess relationships
between the abundance and intensity of
parasites and host size and weight, fish
condition and bottom water temperature. The
Fulton's Condition Factor (KLP) was
calculated as K = [W/TL3] 10,000, where: W =
weight (g) and TL = total length (mm), to
describe the physiological condition of each
individual fish (Ricker 1975).
From February to December 2012, a total of
223 fish specimens of P. pardalis and P.
disjunctivus were collected and examined.
During the study period, the average water
temperature ranged from 24ºC (in February) to
30.8ºC (in August). Of the total fish examined,
only 148 (66.3%) were infected with
ectoparasites.
A total number of 604 parasite individuals
were found in P. pardalis and P. disjunctivus.
The parasite species found was identified as
Heteropriapulus heterotylus (P. pardalis n =
408, P. disjunctivus n = 196). This monogenean
was found specifically in the gill arches.
The mean abundance of H. heterotylus in P.
pardalis and P. disjunctivus showed significant
variations over the course of the study
(ANOVA, P < 0.01). The mean abundance ±
SE of H. heterotylus was of 1.56 ± 0.58
-1
ind.host in P. pardalis and 1.20 ± 0.20
-1
ind.host in P. disjunctivus. In both hosts, this
parasite was relatively high between June and
September (Table 1) and absent in December
for P. disjunctivus.
The prevalence of H. heterotylus was of 61.6%
in P. pardalis and 64.6% in P. disjunctivus.
This population descriptor had a peaked twice
between April and November (Table 1). The
mean intensity of H. heterotylus was higher in
P. pardalis (3.7 ± 1.2) than in P. disjunctivus
(2.4 ± 0.6), although this difference was not
statistically significant (Mann-Whitney U test,
P > 0.05). Moreover, in P. pardalis, the mean
intensity of infection of H. heterotylus was
higher in September (10.7 ± 2.3) and lower in
January (1.0 ± 0.0). In P. disjunctivus, the mean
intensity was also higher in September (4.6 ±
0.4) and lower in December (0.0 ± 0.0).
For P. pardalis, significant relationships were
found between the water temperature and both
the mean intensity and the mean abundance of
H. heterotylus (mean intensity-temperature, r
s
= 0.77, P < 0.05; mean abundance-
temperature, r = 0.85, P < 0.01). In P.
s
disjunctivus, a significant relationship was
found between the mean abundance of H.
heterotylus and water temperature (r = 0.77, P
s
< 0.05). Moreover, no significant relationships
RESULTS
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Heteropriapulus ectoparasite of two invasive sailfin
were found between the host size, weight and
condition factor of the hosts and the
community descriptors of parasites (mean
abundance, prevalence and mean intensity).
Table 1. Prevalence (P%), mean abundance (MA) and mean intensity (MI) of H. heterotylus in the invasive Amazon
sailfin catfishes P. pardalis and P. disjunctivus from a freshwater ecosystem of Southeastern Mexico (n = 223). Total
number of host individuals and size range in cm (H), total number of parasites (PT).
Parasites H PT P (%) MA MI
Pterigoplichthys pardalis
Jan 16 (19-40) 5 31.2 0.16 ± 0.70 1.0 ± 0.0
Feb
21 (27-39) 37 69.1 1.23 ± 0.44 2.92 + 0.3
Mar
13 (24-32) 8 24 0.47 ± 0.20 1.60 ± 0.2
Apr
Jun
Sep
Nov
Dec
16 (26-49)
14 (26-39)
17 (17-38)
22 (24-43)
10 (27-40)
39
91
191
31
6
75
93
71
95.4
40
1.3 ± 0.37
3.5 ± 0.85
4.42 ± 0.96
0.96 ± 0.29
0.46 ± 0.22
3.25 ± 0.6
6.50 ± 1.0
10.7 ± 2.3
2.50 ± 0.5
1.50 ± 0.2
Pterigoplichthys disjuntivus Jan
14 (26-39) 5 36 0.33 ± 0.17 1.0 ± 0.0
Feb
9 (27-40) 23 89 1.58 ± 0.81 2.86 ± 0.6
Mar
3 (25-29) 5 56 0.3 ± 0.22 1.67 ± 0.5
Apr
Jun
Sep
Nov
Dec
14 (19-40)
12 (25-41)
15 (25-37)
24 (18-48)
3 (31-43)
47
45
57
14
0
100
83
53
100
0
1.74 ± 0.40
3 ± 1.54
2.38 ± 0.40
0.3 ± 0.11
0.0 ± 0.0
3.36 ± 0.4
4.50 ± 0.6
4.57 ± 0.4
1.43 ± 0.2
0.0 ± 0.0
DISCUSSION
The present study provides new data on the
prevalence and abundance of monogenean H.
heterotylus, (Monogenoidea: Dactylogyridae)
parasitizing on two invasive Amazon sailfin
catfishes (Siluriformes, Loricariidae) in
Southeastern Mexico. This monogenean H.
heterotylus is very likely specific to loricariids
of South American origin, and is probably
native to America itself, however, so far it has
been reported only from Asia (India, China,
Japan) and Mexico, into which loricariids
have been introduced (Jogunoori et al., 2004;
Li & Huang, 2012; Mendoza-Franco et al.,
2012; and in the present study). Wild
loricariids from South America need to be
examined for the presence of this parasite. The
fact to find the same parasite species H.
heterotylus in the present study, in the two
species of Pterygoplichthys may suggests a
possible specificity by these host species that
also share the same environment. If so, H.
heterotylus could be regarded as an introduced
species of parasite as the fish host. However,
the possible transfer of this parasite to native
fish species remains unknown. This fact has
widely documented in parasites of ornamental
fishes (with wider host specificity), which may
acquire new host species in a newly invaded
environment (King & Cable, 2007).
This report is the first record of the species
P t e r y g o p l i c h t h y s b y t h e g e n u s
Heteropriapulus. The fish P. pardalis and P.
disjunctivus are natives of the inland waters of
Central and South America, which were
59
introduced to Mexico through aquarium trade
(Wakida-Kusunoki, 2008). This represents a
new host record for this parasite and a new
geographical record for P. disjunctivus and P.
pardalis. The presence of the monogenean H.
heterotylus was highlighted, due of its relative
high abundance and prevalence in both fish
host species during the study. The species of
this genus have been reported before only in
exotic fishes, in aquaria, rearing facilities or
introduced into local lakes and streams, have
frequently been found to host dactylogyrids
that occur on the respective hosts in their native
habitats (Jogunoori et al., 2004, Wakida-
Kusunoki, 2008). The significant positive
relationships found in both hosts between the
mean abundance of parasites and the water
temperature indicated that these parasites,
particularly H. heterotylus, showed a marked
seasonality, likely due to environmental
changes. These findings agree with other
studies that suggest that interannual variability
in the abundance of parasites in a host may be
due to seasonal changes in water temperature
(Chubb, 1977; Scott & Nokes, 1984;
Koskivaara et al., 1991). For example, a
parasitological study on the fish Puntius spp.
(from India) revealed that abundance of
monogeneans showed an increasing or
decreasing trend with rise and fall in
temperature, in general, although some species
were more abundant during the monsoon and
winter seasons (Shrivastava et al., 2012). It
was also suggested that increase of parasites
during monsoon can be explained by the
synchronization of parasite life cycle with the
beginning of host reproduction. Also, during
monsoon conditions there is a low amount of
dissolved oxygen in water, which many fish
are forced to come to the surface to breathe,
increasing the chances of contact with free-
swimming oncomiracidia hatched from
floating eggs (Shrivastava et al., 2012). The
higher abundance of parasites recorded in this
study during June-September (rainy season),
could also be related to a more stressful
conditions for the hosts and therefore be more
vulnerable to parasites, as the water turbidity
increases considerably during this period. In a
previous study conducted within this same
region, Wakida-Kusunoki & Amador del
Ángel (2011) found that the abundance of
these loricariid species was relatively higher
from June to September, which was positively
correlated with the gonadosomatic index and
the river water level. In this sense, it is also
possible that the season of higher abundance of
parasites is related to the reproductive stage of
the host, since it is well known that some fish
species are more susceptible to parasite
infection in periods of higher reproductive
investment (Simková et al,. 2005).
Surprisingly, the same situation has been
documented for H. heterotylus, which has been
found in other exotic members of the family
Loricariidae (Hypostomus sp.; Jogunoori et
al., 2004, Kritsky, 2007; Wu et al., 2011).
These findings agree with Poulin et al. (2011)
who suggested that sympatric or
phylogenetically related hosts with similar
ecologies should have similar parasite
communities. The parasite H. heterotylus is
very likely specific to loricariids and is
probably native to South America; however, its
distribution has expanded to Asia, including
India, China, and Japan (Nitta & Nagasawa,
2013).
The identification of the same parasite, H.
heterotylus, in both P. pardalis and P.
disjunctivus suggests a possible common
specificity by these host species that also share
the same environment. If so, H. heterotylus
could be regarded as an introduced parasite
species. However, the transfer of this parasite
to native fish species has not yet been
demonstrated. Certainly, the transfer of
parasites of ornamental species with wider
host specificity to native species in newly
invaded environments has been widely
documented (King & Cable, 2007). In Mexico,
some species of parasites such as G.
cichlidarum and D. vastator have been
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
60
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Heteropriapulus ectoparasite of two invasive sailfin
regarded as high risk in aquaculture because
they are associated with fish mortalities
(Caspeta et al., 2009). Therefore, we strongly
recommend assessing the possible routes of
propagation of these fish species throughout
the country as well as analyzing other
coexisting fish species to determine whether
these parasites have been transferred to other
species.
In summary, this study documents the parasite
community of the Amazon sailfin catfish
species P. pardalis and P. disjunctivus which
are known to be highly invasive in many
regions worldwide. In general, the parasite
species richness in these invasive fishes was
relatively low. The monogenean H.
heterotylus are species which shared these fish
hosts, which seems to be specific of loricariids
as also occur with its congener H. heterotylus
found in other loricariid species from India
(Jogunoori et al., 2004). Also, interannual
variations in the overall mean abundance and
intensity of monogenean were detected, which
were positively related to the water
temperature.
Finally, the present work shows that
parasitological studies in exotic fish can also
be useful to design control strategies, and
should be regarded as necessary before
encourage its consumption as a control
strategy in those regions where these invasive
fish species proliferate excessively. It is
strongly recommended to conduct further
studies about the possible incidence of these
parasites on native species, which share the
same environment with these loricariid
species.
to Alvarez-Guillén H, Reda-Deara A. and
Gómez-Ponce A. for their help in the field
samplings. To Gerardo Perez-Ponce de Leon
by providing us materials and equipment in the
laboratory of Helmintología, UNAM. MARS
and MIGM thanks to CONACyT (Consejo
Nacional de Ciencia y Tecnología) and the
Instituto de Ciencias del Mar y Limnologia
Unidad Academica Mazatlan by the
Postdoctoral Fellow and support.
ACKNOWLEDGEMENTS
We would like to thank to Erik Hoberg and
Patricia Pilitt from the USNPC for the pictures
of type and voucher specimens of Heterotylus
heterotylus from India. We would like to thank
Caspeta-Mandujano, J, Cabañas-Carranza, G
& Mendoza-Franco, E. 2009.
Chapin, FIII, Zavaleta, E, Eviner, V, Naylor, R,
Vitousek, P & Reynolds, H. 2000.
Chavez, J, De La Paz, R, Manohar, S,
Pagulayan, R & Carandang, J. 2006.
Dick, J & Platvoet, D. 2000.
Gaskin, J & Schaal, B. 2002.
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Received, March 6, 2015
Accepted, April 18, 2015
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