105
Neotrop. Helminthol., 7(1), 2013
2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
ECOLOGICAL ASPECTS OF MONOGENEAN GILL PARASITES (PLATYHELMINTHES)
FROM HOPLIAS AFF. MALABARICUS (BLOCH, 1794) (PISCES, ERYTHRINIDAE) IN A
NEOTROPICAL FLOODPLAIN
ASPECTOS ECOLÓGICOS DE MONOGENEOS PARÁSITOS BRANQUIALES
(PLATYHELMINTHES) DE HOPLIAS AFF. MALABARICUS (BLOCH, 1794) (PISCES,
ERYTHRINIDAE) EN UNA PLANICIE DE INUNDACIÓN NEOTROPICAL
Abstract
We analyzed 54 specimens of Hoplias aff. malabaricus (Bloch, 1794) collected between March
2010 and March 2011 from the upper Paraná river Neotropical floodplain, Brazil. All hosts were
parasitized by at least one species of Monogenea. The parasites species with higher prevalence
were Urocleidoides cuiabai Rosim, Mendoza-Franco & Luque, 2011 (96.29 %) and U.
malabaricusi Rosim, Mendoza-Franco & Luque, 2011 (92.59%). The community of gill
ectoparasites examined showed an aggregated pattern. Urocleidoides cuiabai was the dominant
species in the sample (C > 0.25). The parasitic abundance showed significant positive correlation
with the standard length of the host for U. malabaricusi and U. eremitus Kritsky, Thatcher &
Boeger, 1986. There were significant differences in the abundance values between male and
female fish to the species of parasites Urocleidoides brasiliensis Rosim, Mendoza-Franco &
Luque, 2011 and U. cuiabai. The gonad maturation stages of the host did not influence the levels
of parasitism. Four species of parasites showed positive and significant correlation with parasitic
abundance and the relative condition factor. The Ivinheima river presented higher abundance of
parasitism in relation to other subsystems. The ecological study of monogeneans can provide a
greater knowledge of the biology of these parasites and their hosts, the collection site, and even
how the host responds to the presence of these parasites. We discuss the factors that were
fundamental in the levels of parasitism in this important fish species in the floodplain of the upper
Paraná river.
Keywords: Ancyrocephalinae - Brazil - Dactylogyridae - fish ectoparasites - “traíras” - upper Paraná River foodplain.
Suggested citation: Graça, RJ, Costa, APL & Takemoto, RM. 2013. Ecological aspects of monogenea gill parasites
(Platyhelminthes) from Hoplias aff. malabaricus (Bloch, 1794) (Pisces, Erythrinidae) in a neotropical floodplain. Neotropical
Helminthology, vol. 7, N°1, jan-jun, pp. 105 - 116.
1Laboratório de Ictioparasitologia, Núcleo de Pesquisas em Limnologia, Ictiologia e Aqüicultura (Nupélia), Universidade Estadual de Maringá (UEM) - Bloco
G-90, Av. Colombo, 5790, CEP 87020-900. Maringá, PR, Brasil.
2Programa de Pós-Graduação em Biologia Comparada (PGB), Centro de Ciências Biológicas (CCB), Universidade Estadual de Maringá (UEM).
*Autor para correspondência: Rodrigo Junio da Graça, e-mail: rjgrodrigo@gmail.com
1,2,* 1 1
Rodrigo Junio da Graça ; Ana Paula Lula Costa & Ricardo Massato Takemoto
106
Resumen
Palabras clave: Ancyrocephalinae - Brasil - cuenca del alto rio Paraná - Dactylogyridae - ectoparásitos de pez -“traíras”.
Analizamos 54 especímenes de Hoplias aff. malabaricus colectados entre marzo de 2010 y marzo
de 2011 en la planicie de inundación Neotropical del alto rio Paraná, Brasil. Todos los hospederos
fueron parasitados por lo menos con una especie de Monogenea. Las especies de parásitos con las
mayores prevalencias fueran Urocleidoides cuiabai (96,29 %) y U. malabaricusi (92,59%). La
comunidad de ectoparásitos de branquias ha presentado patrón de distribución agregado.
Urocleidoides cuiabai fue la especie dominante en la muestra (C > 0,25). La abundancia del
parasitismo ha presentado correlación positiva y significativa con la longitud estándar del
hospedero para las especies U. malabaricusi y U. eremitus Kritsky, Thacher & Boeger, 1986.
Hubo diferencia significativa en la abundancia de parasitismo entre peces machos y hembras para
los parásitos U. brasiliensis y U. cuiabai. La fase de maduración gonadal del hospedero no influyó
los niveles de parasitismo. Cuatro especies de parásitos han presentado una correlación positiva y
significativa con la abundancia de parasitismo y el factor de condición relativo. El rio Iviñeima ha
presentado alta abundancia de parasitismo en relación a otros subsistemas. El estudio ecológico
de monogeneas puede proveer un gran conocimiento de la biología de estos parásitos y sus
hospederos, el sitio de colecta, y hasta como el hospedero responde a la presencia de estos
parásitos. Este artículo presenta los factores que fueron fundamentales en los niveles de
parasitismo en esta importante especie de pez en la planicie de inundación del alto rio Paraná.
Ecological aspects of monogenea gill parasites from Hoplias Graça et al.
Among the species of fish cataloged in the upper
Paraná river floodplain is Hoplias aff.
malabaricus (Bloch, 1794). This is a species
widely distributed in rivers of South America
and popularly known as “traíras” or “lobó”
(Oyakawa, 2003). “Traíras” are carnivorous and
sedentary, occur in fluvial and lakes
environments (Nakatani et al., 2001). In the
larval stage these fish feed on plankton and when
adult mainly feed on other fish, with low greed
and high resistance to fasting periods (Paiva,
1974).
Along with the fish collected over the years in
the upper Paraná river floodplain is the
symbiotic fauna, composed of micro and macro
organisms, between which the parasites are
mainly represented by protozoa, helminths and
microcrustaceans. Several studies on taxonomy
and ecology of fish parasites have been
conducted in the region, and according to
Takemoto et al. (2009), 337 species of fish
parasites have been cataloged between the years
2000 to 2007, of which 12 were new species.
INTRODUCTION Monogenea was the group of parasites that
presented more new species, describing eight
new species.
The seasonal occurrence of monogeneans in fish
seems to be influenced by several factors, biotic
and abiotic. The biotic factors, such as age, size,
sex and migratory behavior habits of the host can
influence the prevalence and intensity of
parasitic infection throughout the year. Among
the abiotic factors, temperature is apparently
what seems to have a greater influence on the
seasonal distribution of monogeneans (Eiras,
1994). Although the aquatic environment
facilitates access of parasites to their hosts.
Lentic environments are more favorable to
transmission the diseases than lotic (Thatcher,
1981). For monogeneans, this type of
environment favors the ciliated larvae finding
the host .
The relation parasite/host is part of a complex
structural network ecosystems and particularly
in aquatic systems, these relationships are key
indicators of the structure of these networks
(Silva-Souza et al., 2006). Thus, the study of fish
Neotrop. Helminthol., 7(1), 2013
parasites allows to obtain important information
not only about the hosts, but also the
environment in general (Takemoto et al., 2005 a,
b).
This paper presents a study about the component
community of monogeneans gill parasites of
Hoplias aff. malabaricus collected in the upper
Paraná River Neotropical floodplain, Brazil, in
order to evaluate the relationship of parasitism
with biotic factors such as the standard length
and sex of hosts, interspecific relationships,
similarities and the possible influence of
parasitism on the welfare of the host.
The study area is part of the upper Paraná river
floodplain in the Paraná and Mato Grosso do Sul
States from Brazil (22º43'S, 53º10'W). It is
located near to Porto Rico, Paraná, where are the
Field Station of the Universidade Estadual de
Maringá - Nupélia (Núcleo de pesquisas em
Ictiologia, Limnologia e Aquicultura) (Fig. 1).
The sampling points correspond to those used by
the program "Long Term Ecological Research"
(LTER site 6).
It were collected 54 “traíras” between the period
of March 2010 to March 2011 in three different
subsystems of the upper Paraná river foodplain;
Paraná, Baia and Ivinheima rivers through
gillnets of different mesh sizes (2,4; 3; 4; 5; 6; 7;
8; 10; 12; 14 e 16 cm). Were anesthetized with
Benzocaine 10%, killed, identified,
enumerated, measured (cm) and weighed (g),
and also recorded the sex, stage of maturation,
the total weight , total and standard length. After
“traíras” had their gills removed and fixed in
formalin solution 5%.
Gills arches were removed and examined
individually in Petri dishes with water under a
stereomicroscope for the collection of parasites.
The parasites were fixed, prepared and
assembled as Eiras et al. (2006).
To obtain the total number of parasites count was
made under a dissecting microscope in a Petri
dish. For identification, specimens were
prepared in Hoyer medium, for observation
under an optical microscope (Eiras et al., 2006).
The identification was made according to
Kritsky et al. (1986), Thatcher (2006) and Rosim
et al. (2011). The terminology of parasite
ecology were used according to Bush et al.
(1997).
The Brillouin's index of diversity and uniformity
was used to determine the diversity of the
infracommunities of ectoparasites on gill in the
differents subsystems (Stone & Pence, 1978).
The Berger Parker index of dominance was used
to check if there was a dominance concentration
among species. This index expressed the
proportionate importance of the species more
abundant of parasite in the sample (Magurran,
1988).
The dispersion index (DI) and Green index (GI)
were used to examine the pattern of dispersion
and aggregation of the species of ectoparasites.
The dispersion index was tested using statistical
d, being considered random distribution when d
<1.96, uniform distribution when d < -1.96 and
aggregate when d > 1.96. The degree of
aggregation was measured by Green index
which ranges from 0 (at random) and 1
(maximum aggregation) (Ludwig & Reynolds,
1988).
The Pearson correlation coefficient "r" was
calculated to determine the correlation between
the prevalence of parasitism and host standard
length, with previous angular transformation of
data on prevalence and separation of samples
from the hosts at intervals of length classes. The
Spearman's correlation coefficient "rs" was used
to determine possible correlations between host
standard length and abundance of parasites, and
to investigate correlations of the abundances of
parasites with the relative condition factor (Kn)
of the hosts (Zar, 1996).
The test "G" log-likelihood, using the 2 x 2
contingency table was used to determine the
effect of host sex on prevalence of each parasite
species (Zar, 1996). The Mann-Whitney (U) was
used to determine the effect of host sex in the
MATERIALS AND METHODS
107
Ecological aspects of monogenea gill parasites from Hoplias Graça et al.
abundance of infestation (Siegel, 1975).
The Student "t" was used to determine if the
standard length of the males and females hosts
are similar. This test also verified the possible
influence of the length of the host, in parasitism
levels. The Kruskal-Wallis (H) test was used to
verify that the different maturation stages are
influencing levels of parasitism (Zar, 1996).
The relative condition factor (Kn) was
calculated based on the weight and length of the
fish (LeCren, 1951).
The gonadal maturation stages of the fish were
determined according to Vazzoler et al. (1997).
The tests mentioned above were applied only for
parasite species with prevalence higher than
10%. Statistical analyzes were performed on 5.0
BioEstat and Past programs. Voucher specimens
were deposited at Coleção Helmintológica do
Instituto Oswaldo Cruz (CHIOC), Rio de
Janeiro, Rio de Janeiro, Brazil.
This project was analyzed and approved by
committee of Ethics of the Universidade
Estadual de Maringá (CEAE) number
(123/2010).
All fishes analyzed were parasitized by at least
one species of monogeneans. The total number
of parasites found was 3640 specimens, the
species most prevalent was Urocleidoides
cuiabai Rosim, Mendoza-Franco & Luque,
2011 with 96.29% followed by U. malabaricusi
Rosim, Mendoza-Franco & Luque, 2011 with
92.59%. The data obtained are listed in Table 1.
Of the 54 fish examined 16 were parasitized by
six of parasites species and only three hosts were
parasitized by one species (Fig. 2).
According with the index Berger-Parker there
was a dominance of species U. cuiabai
(42.08%). The dispersion of the parasite species
presented itself aggregate (Table 2).
RESULTS
Figure 1. The upper Paraná river Neotropical floodplain, Brazil showing the Area of Long Term Ecological Research (ALTER).
108
Neotrop. Helminthol., 7(1), 2013
Table 2. The dispersion index (DI) and aggregation index of Green (IG) estimated for species of monogeneans of
Hoplias aff. malabaricus in the upper Paraná river floodplain, PR / MS, from March 2010 to March 2011.
Parasites
DI
D IG Distribution
Urocleidoides malabaricusi
17.89 32.99 0.029 Aggregate
Urocleidoides eremitus
59.04 70.15 0.076 Aggregate
Urocleidoides cuiabai
4.41
75.0 0.044 Aggregate
Urocleidoides brasiliensis
12.8
26.58 0.049 Aggregate
Anacanthorus sp.
11.61 615.59 0.049 Aggregate
Dactylogyridae gen. 1. sp. 16.87 32.04 0.071 Aggregate
and positive correlation between host standart
length with prevalence (Table 3). There was no
significant correlation between the hosts
standart length with the results of diversity
obtained by the Index Brillouin (rs = - 0.1320 p>
0.05).
The average standart length of the fish analyzed
was 24.35 cm (14.7 to 35.5). Urocleidoides
malabaricusi showed significant and positive
correlation between abundance and host standart
length. Urocleidoides eremitus Kritsky,
Thatcher & Boeger, 1986 showed significant
Table 1. Acess Number CHIOC (AN); Number of fish infested (NI), Number of parasites collected (NP), prevalence
(P%), mean intensity (MI) Mean Abundance (MA) Amplitude of parasitism (AP) of monogenean gill parasites of
Hoplias aff. malabaricus in the upper Paraná river Neotropical floodplain, PR / MS, from March 2010 to March
2011.
Parasites
AN NI NP P MI MA AP
Urocleidoides malabaricusi
CHIOC 37791 50 691 92.59 13.82 12.79 1 - 117
Urocleidoides eremitus
CHIOC 37790 35 736 64.81 21.02 13.62 1 - 143
Urocleidoides cuiabai
CHIOC 37793 52 1532 96.29 29.46 28.37 1 - 193
Urocleidoides brasiliensis
CHIOC 37795 37 240 68.51 6.48 4.44 1 - 42
Anacanthorus sp.
CHIOC 37800 30 215 55.55 7.16 3.98 1 - 29
Vancleaveus janauacaensis
CHIOC 37797 2 2 3.7 1 0.037 1 - 2
Cosmetocleithrum bulbocirrus
CHIOC 37799 1 1 1.85 1 0.018 -
Dactylogyridae gen. 1 sp.
CHIOC 37802
a-b
26 222 48 8.53 4.11 1 - 47
Dactylogyridae gen. 2 sp.
CHIOC 37803 1 1 1,85 1 0.018 -
Table 3. Values of the Spearman's rank correlation coefficient "rs" correlating host standard length and abundance
of parasites, and the Pearson correlation coefficient "r" correlating the prevalence of parasitism and the standard
length of Hoplias aff. malabaricus in the upper Paraná river Neotropical floodplain, PR / MS, from March 2010 to
March 2011. p = significance level, * significant value.
Parasites rs p r p
Urocleidoides malabaricusi 0,244 0,050* 0,307 0,614
Urocleidoides eremitus 0,012 0,928 0,894
0,040*
Urocleidoides cuiabai 0,188 0,171 -0,000
0,999
Urocleidoides brasiliensis 0,048 0,728 0,720 0,169
Anacanthorus sp. -0,131 0,343 -0,876
0,051
Dactylogyridae gen. 1. sp. -0,158 0,251 -0,847
0,070
109
The fish studied were in different stages of
maturation (rest, initial maturation, advanced
maturation, partially spawn/spent, totally
spawn/spent). The Kruskal-Wallis test was use
to verify the possible influence of maturation
stages in the levels of parasitism, but it was
found no significant correlation (p>0.05).
Four of the six parasites species studied had
abundance significantly and positively
correlated with the relative condition factor
(Table 5).
110
Ecological aspects of monogenea gill parasites from Hoplias Graça et al.
Table 5. Values of the Spearman's rank correlation coefficient "rs" correlating the relative condition factor and
abundance of parasitism of Hoplias aff. malabaricus in the upper Paraná river Neotropical floodplain, PR / MS from
March 2010 to March 2011. p = significance level, * significant value.
Parasites
rs p
Urocleidoides malabaricusi 0.264 0.0530
Urocleidoides eremitus 0.567 0.0001*
Urocleidoides cuiabai 0.252 0.0650
Urocleidoides brasiliensis 0.475 0.0003*
Anacanthorus sp.
0.353 0.0088*
Dactylogyridae gen. 1. sp. 0.518 0.0001*
Table 4. Test values "G" log-likelihood for detecting differences between the males and females in the prevalence of
parasitism and the Mann-Whitney test with normal approximation "Z" to verify differences between the males and
females in the abundance of parasitism of Hoplias aff. malabaricus in the upper Paraná river Neotropical floodplain,
PR / MS, from March 2010 to March 2011. p = significance level, * significant value.
Parasites Z PGP
Urocleidoides malabaricusi 1,005 0,157 0,578
0,446
Urocleidoides eremitus 1,207 0,113 3,277
0,070
Urocleidoides cuiabai 1,670 0,047* 2,276
0,131
Urocleidoides brasiliensis 1,731 0,041* 0,546
0,459
Anacanthorus sp. 0,096 0,461 0,196
0,657
Dactylogyridae gen. 1. sp. 0,487 0,313 0,260 0,610
showed a significant difference in abundance
between male and female fish. Females were
most affected by these species than the males.
There were no significant differences in the
prevalence of parasitism between males and
females (Table 4).
Of the 54 fish analyzed 31 were males and 23
females. According to the t test there was no
significant difference in the standard length
between males and females hosts (t = -0.805 p >
0.05). Urocleidoides cuiabai and U. brasiliensis
Rosim, Mendoza-Franco & Luque, 2011
111
Figure 2. The gill parasites richness in Hoplias aff. malabaricus collected in the upper Paraná river floodplain, PR / MS, from
March 2010 to March 2011.
be in the high density of fish species in the
collection points, which according to Júlio Jr. et
al. (2008) was a fish specie with higher
abundance and biomass in the subsystems Baía
and Ivinheima rivers in the upper Paraná river
Neotropical floodplain. Takemoto et al. (2005 b)
studied the influence of host density in the
endoparasites diversity and found significant
correlation as well as in the present study,
possibly monogenetic showed increased levels
of parasitism with the high population density of
fish, as this may facilitate transmission of
parasites.
Monogeneans, when present in fish farms,
provokes high fish mortality rates, causing
considerable damage (Eiras, 1994), however
there are no records of high mortality caused by
these parasites in fish of natural environments in
Brazil (Thatcher, 1981). This probably occurs
because of the difficulty in proving the cause of
fish death and also by the fact that some fishes
debilitated by parasites are easily preyed upon.
In the present study the distribution of species of
monogeneans showed an aggregation pattern
which, according to Abdallah et al. (2005) is
characteristic of parasitic systems. Poulin
(1998) argued that the distribution of parasites is
due to processes that are not constant and
Eiras (1994) stated that biotic factors such as
host biology, behavior and migratory habits can
interfere in the prevalence and intensity of
infestation by monogeneans throughout the
year. The fact that all “traíras” are parasitized of
monogeneans, may be related to the behavior of
these hosts, which according Graça & Pavanelli
(2007) are sedentary, living in lentic
environments such as lakes and canals. Pavanelli
et al. (2008) mentioned that aquatic
environments lentic or of confinement can favor
the infestation by monogeneans this is because
these parasites possess monoxenic cycle,
finding facility to complete its life cycle,
especially in environments with high densities
of fish. Graça & Machado (2007) studying
cichlids collected from an artificial lake in the
city of Maringá in the Paraná State, Brazil, also
observed that all fish were parasitized by at least
one species of monogeneans, and justified this
high prevalence by the fact that these fish feed on
the lake bottom, which would facilitate the
suspension of eggs and thus infestation by these
parasites.
Another possible explanation for the high
prevalence of monogeneans of “traíras” would
DISCUSSION
Neotrop. Helminthol., 7(1), 2013
Ecological aspects of monogenea gill parasites from Hoplias Graça et al.
Mymarothecium Kritsky, Boeger & Jégu, 1996,
observed a significant positive correlation
between abundance and the standard length of
their hosts, with increasing length of fish was
increased abundance of this parasite species.
However this same work for other species of
monogeneans was found negative correlation
between length and abundance of the
monogeneans Anacanthorus penilabiatus
Boeger, Husak & Martins, 1995, in this case the
larger fish had a lower abundance of this parasite
species. Lizama et al. (2007) justified that these
variations in levels of parasitism in their study is
possibly due to different characteristics of the
sample points of their hosts.
Dogiel (1961) mentions that the length of the
host is a major factor in the size range of parasitic
infrapopulations. This is probably because the
body surface and gill cavity can accommodate
larger number of parasites, being more
pronounced in monoxenic cycle of ectoparasites
(Rohde, 1993). Luque et al. (1996) make a point
of attention to avoid generalizations about the
influence of the length of the host on the
qualitative and quantitative composition of
infracommunities of parasites. The fact that the
hosts have a great length does not mean they will
have a higher concentration of parasites, due to a
longer exposure to infections. Still, according to
Luque & Chaves (1999) in the case of
ectoparasites, besides the size of the host the
parasitism level may be influenced by the degree
of specialization of the fasteners structure of the
parasites and by the availability of infective
forms to certain population groups of hosts.
In the present work, U. brasiliensis and U.
cuiabai showed a significant difference in
abundance correlated to host sex, but no
significant differences in the prevalence of
parasites between male and female fish. Luque
& Cezar (2004) when working with
ectoparasites of marine fish found no relation
between levels of parasitism and host sex. This
fact was also observed by Graça & Machado
(2007). Similar results were observed by Rosim
(2010) studying the parasite fauna of H. aff.
malabaricus collected in different rivers of
Brazil, noting that females had more parasites.
therefore is a dynamic event. There are several
biotic and abiotic factors that may affect the
distribution of parasites among hosts, these
factors can increase the aggregation or even
produce a more uniform distribution. Also
according to this author, the composition of
ectoparasite communities is strongly linked to
the biology of the hosts. According to Zuben
(1997) the aggregated distribution pattern acts to
increase the density dependent regulation, the
abundance of both host and parasite, and reduce
the level of competition among parasite species.
Bagge et al. (2005) studying aggregation in carp
monogenetic observed that by increasing the
abundance parasitic there was a decrease in
aggregation, and explained this result stating
that with a greater abundance of parasites
decreases the distance between these parasites
increasing the chances of cross-fertilization
between them.
The index of Berger - Parker indicated that U.
cuiabai was dominant in relation to other species
of parasites in the sample. Azevedo et al. (2007)
when studying parasites of cichlids from
Guandu river, observed that the monogeneans
Gussevia sp. showed dominance in almost all
studied specimens of fish, which the authors
justified by the fact that these fish have
preference for lentic environments, which
facilitate infestation by this parasite. As the
species of monogeneans found in “traíras” have
similar biological characteristics and the hosts
came from the same environments, the
dominance of U. cuiabai studied in fish can be
treated for greater efficiency of this species to
colonize their host or because it presents features
which causes it to be less susceptible to the host
immune system. Another hypothesis is the
competitive strength of this species and
consequently a greater ecological niche than
other species of Monogenea.
In our study the abundance of U. malabaricusi
showed significant positive correlation with
standard length of the host, U. eremitus its
prevalence was also correlated with the host
standard length. Lizama et al. (2007) when
s t u d y i n g t h e m o n o g e n e a n s g e n u s
112
In this study it was observed that the Kn of H. aff.
malabaricus had significant and positive
correlation with the abundance of parasitic
species U. eremitus, U. brasiliensis,
Anacanthorus sp., Dactylogyridae gen. 1 sp., or
fish with a higher Kn were infected by these
species of parasites. Cone (1995) stated that
larger fish and a better Kn can withstand higher
intensities of infection by monogeneans
parasites despite being pathogenic. This is
possibly the reason for the significant and
positive correlation between Kn studied fish and
abundance of parasitism by monogeneans.
The ecological study of monogeneans can
provide a greater understanding of the biology of
these parasites and their hosts, the collection
site, and even how the host responds to the
presence of these parasites. In this work we
presented several factors that were crucial to the
parasitism of monogeneans in Hoplias aff.
malabaricus in the upper Paraná river
floodplain, but we are far from understanding all
the factors that influence the relation parasite /
host. So we propose new ecological studies of
fish parasites in the region, noting that there is no
isolated factor favoring parasitism in fish, but
rather a set of biotic and abiotic factors, and that
generalizations can lead to erroneous
interpretations that would undermine the studies
on Ichthyoparasitology.
The authors wish to thank to Nupélia/UEM,
Núcleo de Pesquisas em Limnologia, Ictiologia
e Aquicultura, and to Project A Planície Alagável
do Rio Paraná: Estrutura e Processos Ambientais
- PELD/CNPq for logistic and financial support.
This were supported by a Research fellowship
from CNPq (Conselho Nacional de
Desenvolvimento Científico e Tecnológico).
The course of pos graduation in Biologia
Comparada and Universidade Estadual de
Maringá by the structure provide and Fabrício
Hiroiuki Oda by contributions in this paper.
The fact that females of H. aff. malabaricus
present a greater abundance of parasites may be
related to differences in habits between males
and females. Querol et al. (2003) stated that this
fish species have parental care and, after
breeding, the male cares for the eggs, getting
closer to the nest. This characteristic of the male
would leave them theoretically more exposed to
monogeneans, but it was not what we found in
our study. Thus, the factor that may have
influenced the difference in parasitism between
males and females is the reproductive period,
which changes the physiology of the females,
what may lower the immune defenses and thus
increasing the susceptibility to parasites.
According to Le Cren (1951), the relative
condition factor (Kn) is a quantitative indicator
of the degree of welfare of fish, reflecting recent
feeding conditions, given by the length / weight
relation of the individual. The Kn takes into
consideration the expected and observed weight,
and the ideal value equal to one. Variations in Kn
may be related to changes in the environment,
lack of food or even by parasitism. By
correlating Kn hosts with the abundance of
parasitism, it is expected that most infected fish
have a lower Kn, which is not necessarily true,
because there are other factors that may
influence the levels of parasitism.
Yamada et al. (2008) found significant and
positive correlation to correlate the Kn of
cichlids with the abundance of a species of
monogeneans. Lizama et al. (2007) found
negative and significant relation when relating
the Piaractus mesopotamicus (Holmberg, 1887)
Kn of fish farming with the levels of parasitism
of two species of monogeneans. Tozato (2011)
found no differences in Kn of Corydoras aeneus
(Gill, 1858) parasitized and not parasitized by
monogeneans, and concludes that these
parasites did not affect the welfare of the host.
The author also stated that the parasite
community of fish studied has low pathogenicity
to the host in the different environments of the
basin, indicating the proper response of fish
against parasitism.
ACKNOWLEDGMENTS
Neotrop. Helminthol., 7(1), 2013
113
Ecological aspects of monogenea gill parasites from Hoplias Graça et al.
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Received February 12, 2013.
Accepted April 11, 2013.
Correspondence to author/ Autor para
correspondencia:
Rodrigo Junio da Graça
Laboratório de Ictioparasitologia, Núcleo de
Pesquisas em Limnologia, Ictiologia e
Aqüicultura (Nupélia), Universidade Estadual de
Maringá (UEM) - Bloco G-90, Av. Colombo,
5790, CEP 87020-900. Maringá, PR, Brasil.
E-mail / Correo electrónico:
rjgrodrigo@gmail.com
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