Resumen

Palabras clave: endoparásitos - comunidad de parásitos – llanura de inundación de la parte superior del río Paraná - Brasil.

219

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

ECOLOGICAL RELATIONSHIPS BETWEEN ENDOPARASITES AND THE FISH SALMINUS

BRASILIENSIS (CHARACIDAE) IN A NEOTROPICAL FLOODPLAIN

RELACIONES ECOLÓGICAS ENTRE ENDOPARASITOS Y EL PEZ SALMINUS

BRASILIENSIS (CHARACIDAE) EN UNA LLANURA DE INUNDACIÓN NEOTROPICAL

1 2 1,3 1,3,4

Letícia Cucolo Karling , Ana Carolina Figueiredo Lacerda , Ricardo Massato Takemoto & Gilberto Cezar Pavanelli

Abstract

Keywords: endoparasite - community of parasites - the upper Parana River floodplain - Brazil.

Suggested citation: Karling, LC, Lacerda, ACF, Takemoto, RM & Pavanelli, GC. 2013. Ecological relationships between

endoparasites and the fish Salminus brasiliensis (Characidae) in a Neotropical floodplain. Neotropical Helminthology, vol. 7,

n°2, jul-dec, pp. 219 - 230.

1 2 3

Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais (UEM); Programa de Pós-graduação em Ecologia (POSECO/UFSC); Programa

de Pós-graduação em e Biologia Comparada (UEM); Programa de Pós-graduação em Aquicultura e Desenvolvimento Sustentável (UFPR-Palotina).

Universidade Estadual

Maringá, Laboratório de Ictioparasitologia, CEP: 87020900, Maringá, Paraná, Brazil.

　E-mail: lekarling@hotmail.com

Neotrop. Helminthol., 7(2), 2013

2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

El presente estudio tuvo como objetivo caracterizar la estructura de la comunidad de parásitos de

Salminus brasiliensis en el curso superior del río Paraná a lo largo de las diferentes estaciones del

año, entre los niveles de parasitismo y las diferentes características de los huéspedes. La

comunidad de parásitos de S. brasiliensis no possuía ninguna especie dominante. Cuatro de las

cinco especies de parásitos más prevalentes mostraron distribución agregada. En relación a otros

aspectos de la comunidad, cada grupo presentó su parásito en particular, lo que destaca las

diferencias inherentes al ciclo de la biología y de la vida de cada especie.

The present study was designed to characterize the community structure of parasites of Salminus

brasiliensis in the upper Paraná River during different seasons, and to examine the levels of

parasitism of this hosts. The community of parasites of S. brasiliensis did not have a dominant

species. Four of the five most prevalent parasite species showed aggregate distribution. In relation

to other aspects of the community, each group encompassed their particular parasite, which

highlights the differences inherent in the biology and life cycle of each species.

Karling et al.

Host-parasite relationship Salminus brasiliensis

220

2013). The others are records of species, such as:

Monogenea (Jainus sp., Anacanthorus sp. and

Rhinoxenus bulbovaginatus Boeger,

Domingues, Pavanelli, 1995), a species of

Cestoda (Monticellia coryphicephala

Monticelli,1892), two species of Digenea

(Cladocystis intestinalis Vaz,1932 and

Prosthenhystera obesa Diesing, 1850),

Nematoda (Eustrongylides ignotus

Jäegerskiold, 1909 in the larval stage and

Anisakidae) and Branchiura (Dolops

longicauda (Heller, 1857) and Dolops sp.)

(Takemoto et al., 2009).

Thus, the present study aimed to characterize the

community structure of parasites of S.

brasiliensis in the upper Paraná River along the

different seasons, as well as regarding parasitism

levels and features of the hosts.

The study area is part of the floodplain of the

upper Paraná River. Located near the town of

Porto Rico, State of Paraná (22 ° 43'S and 53 º

10'W), where is the Laboratory for Advanced

Research, State University of Maringa - Nupelia

(Center for Research in Limnology, Ichthyology

and Aquaculture). Samples were collected at

several of the channels environments, such as

rivers and lagoons as part of the project PELD-

CNPq (Long Term Ecological Projects) - Site 6.

Specimens of S. brasiliensis were collected

quarterly between March 2009 and August 2010.

For its capture were used rods with reel and nets

of different mesh sizes (2, 4, 3, 4, 5, 6, 7, 8, 10,

12, 14:16 cm between opposite knots), which

were exposed during 24 h in each collection

point (revised every 8 h). The fish were

sacrificed by deep anesthesia with benzocaine: 3

g of benzocaine dissolved in 10 ml of ethanol to

30 l of water (Lizama et al., 2007). Date of

sampling, total and standard length, total weight,

sex and stage of gonadal maturity of each fish

were recorded.

After the taxonomic identification and decision

The knowledge of the parasitic fauna of

Brazilian fish has received increasing attention

from researchers, in particular as regards the

relationship of parasites and their hosts.

Accordingly, the object of study was the

freshwater fish Salminus brasiliensis (Cuvier,

1816) (Characiformes: Characidae), popularly

known as dourado. This species of fish is found

only in South America, the basins of the Paraná,

Paraguay and Uruguay, in the drainages of the

Patos Lagoon and the Mamore River in Bolivia

(Lima et al., 2003). In the floodplain of the upper

Paraná River until 2003 Salminus brasiliensis

was identified as S. maxillosus (Valenciennes

1850) (Pavanelli & Grace, 2007).

Besides its ecological importance, the dourado

fish is a much appreciated in sport fishing,

presenting a high price in trade due to the

excellent quality of its meat (Zaniboni-Filho et

al., 2003). Studies characterizing the

relationship between helminth parasites and

their hosts should consider the availability of

related information: the environment (water

quality, pH, ammonia concentration, dissolved

oxygen availability, temperature, water level

and seasonal effects ), the host (habitat, feeding

behavior, physiology, age and sex) and the

parasite (availability of infective larvae of

individual hosts, the host immune response to

the establishment of the larva and the natural

mortality of parasites) (Dogiel, 1961; Takemoto

et al., 2004).

Some work on Salminus brasiliensis parasites

have been performed, however, mostly

taxonomic (Boeger et al., 1995; Petter, 1995;

Kohn et al., 1997; Molnar et al., 1998). In

addition, Rodrigues et al. (2002) studied the

histopathological changes caused by the

nematode Neocucullanus neocucullanus

Travassos, Artigas et Pereira, 1928 in dourado in

Mogi Guacu, SP.

For the floodplain of the upper Paraná River,

only two articles were recorded referring to the

ecological aspects Prosthenhystera obesa

Diesing, 1850 (Isaac et al., 2000; Karling et al.,

INTRODUCTION

MATERIALS AND METHODS

Neotrop. Helminthol., 7(2), 2013

The relative condition factor (Kn) was

calculated for each host, which corresponds to

the ratio between the observed weight (Wo) and

the weight theoretically expected for a given

length, that is, Kn = Wo / We (Le Cren, 1951).

The constants a and b of length to weight ratios

were used to estimate theoretically expected

values of the body weight (We) by the formula

a.Ls We = b, where Ls is the length standard.

The tests mentioned above were applied only to

the parasite species with prevalence greater than

10%.

In the total sample, 56 specimens of S.

brasiliensis were necropsied, and collected and

processed 828 helminths belonging to four

groups: Digenea, Nematoda, Acanthocephala

and Cestoda. The most abundant group was

Digenea, composed of a single species, C.

intestinales with 623 specimens.

Species with prevalence greater than 10% in the

total sample: C. intestinales, M.

coryphicephala, Octospiniferoides incognita

Schmidt & Hugghins; 1973, Contracaecum sp.

larva, Contracaecum sp. larvae type 2 by

Moravec, Kohn and Fernandes 1993 (found in

the mesentery). It was not possible to quantify

the Cestoda cysts present in the mesentery.

The prevalence values, mean intensity, mean

abundance and average amplitude for each

suprapopulation obtained are shown in Table 1.

The parasite community of S. brasiliensis

showed no concentration for dominance (C =

0.22), but showed a typical pattern of

aggregation, with the exception of Cestoda M.

coryphicephala, which showed a random

distribution. As the values of the Green Index

parasite species that was more aggregate was O.

incognita (Table 1).

of biometric data of the hosts, a longitudinal

incision was made on the ventral surface of the

individual and every organ and or structures

were removed and separated. The visceral cavity

and each organ were examined under a

stereomicroscope to collect endoparasites.

According to the methodology described by

Eiras et al. (2006).

Data Analysis: the prevalence (P), mean

intensity (IM) and mean abundance (AM)

infection of parasites were obtained according to

Bush et al. (1997). The Simpson Index was

calculated to determine the dominance

concentration, based on the proportion of

infected fish is assumed for the dominance

values greater than or equal to 0.25 (Stone &

Pence, 1978). The dispersion index (ratio

between the variance and mean abundance) and

Green index were used to assess the pattern of

dispersion and aggregation, and the dispersion

index was tested by the statistic d, where the

distribution is considered random when d <1.96,

even when d <-1.96 and aggregate when d> 1.96

(Ludwig & Reynolds, 1988). The chi-square test

with Yates correction was used to determine

possible interspecific associations between pairs

of co-occurring species (Ludwig & Reynolds,

1988). The covariation of abundance of parasites

were tested using the correlation coefficient by

Spearman ranks "rs".

The Pearson correlation coefficient "r" was

calculated to determine the correlation between

the prevalence and host standard length, prior to

angular transformation of data on prevalence

and separation of samples from the host at

intervals of length classes. The correlation

coefficient "rs" was used to determine possible

correlations between host standard length and

abundance of parasite species, and to investigate

correlations of the abundances of parasites with

the Kn of hosts (Zar, 1996).

The Kruskal-Wallis test was used to determine

the seasonal abundance of infection and to

determine the influence of gonadal maturity

stages of fish (immature, maturing, advanced

maturation, recovery, rest and semi exhausted)

on the abundance of parasites (Zar, 1996).

RESULTS

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Karling et al.

Host-parasite relationship Salminus brasiliensis

Table 1. Parasites and parasitism levels of Salminus brasiliensis in the floodplain of the upper Paraná River (P%=

prevalence, IM= mean intensity; AM = average abundance, AV = range of variation of abundance) and Index of

dispersion (ID), Green Index (IG) estimated for the main species of parasites.

Species P(%) IM AM AV ID dIG Distribution

Cladocystis intestinales 67.85 16.39 11.12 1 – 161 53.8 65.88 0.08 Aggregate

Monticellia coryphicephala 10.71 1.16 0.12 1 – 2 1.18 0.978 0.03 Random

Octospiniferoides incognita 10.71 3.66 0.39 1 – 15 10.61 23.73 0.45 Aggregate

Acanthocephala larvae 7.14 1.75 0.12 1 – 3 - - - -

Contracaecum spp. l arvae 16.07 2.33 0.37 1 – 6 3.44 9.036 0.12 Aggregate

Contracaecum sp. larvae type 2 39.28 6.72 2.64 1 – 56 24.77 41.76 0.16 Aggregate

Monticellia coryphicephala cyst 50 - - - - - - -

and Contracaecum sp. larvae was associated

positively and significantly with their

abundances also positively correlated (Table 2).

The five most prevalent species (above 10%)

were divided into pairs to detect possible

interspecific relationships. The pair O. incognita

Table 2. Associations of species of the parasite Salminus brasiliensis collected in the floodplain of the upper Paraná

River. (X = chi-square test with Yates' correction; rs = correlation coefficient by Spearman posts between the

abundances of species in each pair).

Species 1 2 3 4 5

(1) Cladocystis intestinales - (+) (+) (+) (+)

0.23 0.55 0.76 0.03

(2) Monticellia coryphicephala 0.043 - (+) (-) (+)

0.11 0.54 0.11

(3) Octospiniferoides incognita 0.21 0.07 - (+) (+)

4.67 2.84

(4) Contracaecum spp. larvae 0.17 -0.15 0.32 * - (+)

0.16

(5) Contracaecum sp. larvae type 2 0.01 0.05 0.33* 0.17 -

*Significant values

and two with indeterminate sex were parasitized

by one or more species of parasites.

There was no difference in the abundance of

parasitism between the sexes of hosts except for

O. incognita and Contracaecum sp. larvae,

where females were more parasitized (Table 3).

The fish had standard length ranging from 18.3

to 68.5 cm (eight classes, with an interval of 7 cm

each). There was no correlation between the

standard length of hosts and the abundance and

prevalence of parasite species found (Table 3).

Of the 56 fish analyzed (38 females, 15 males

and three indeterminate), 34 females, 12 males

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Neotrop. Helminthol., 7(2), 2013

Table 3. Values of the correlation coefficient "rs" for stations to determine Spearman correlations between the host

standard length and abundance of parasite species; the Pearson correlation coefficient "r" to correlate the prevalence

of parasitism and the standard length and test "G "Log-likelihood for detecting differences between hosts males and

females in the prevalence of parasitism and with Z test to check for differences between males and females in hosts

abundance of parasitism Salminus brasiliensis, collected in the floodplain of the upper Paraná River (p =

significance level).

Species rs p r p Z p G p

Cladocystis intestinales 0.12 0.35 -0.49 0.21 0.07 0.94 0.09 0.75

Monticellia coryphicephala -0.01 0.91 -0.04 0.91 0.18 0.85 0.19 0.65

Octospiniferoides incognita 0.25 0.06 0.41 0.32 0.88 0.38 4.28 0.04*

Contracaecum spp. larvae -0.11 0.42 -0.31 0.45 1.19 0.23 5.86 0.01*

Contracaecum sp. larvae type 2 0 0.97 -0.35 0.38 0.55 0.58 0.35 0.55

*Significant values

stage, two in early-maturing, one in advanced

maturation one in three in recoveries, 26 at rest

and one semi exhausted. The stage of gonadal

maturation did not affect the prevalence and

abundance of groups of parasites, only O.

incognita was found in fish in the resting stage.

The values of the statistical tests are listed in

Table 4.

Contracaecum sp. larvae type 2 showed

significant differences in abundance values

between seasons (Table 4), with the summer

season with the highest mean abundance of this

parasite (16 parasites per fish).

With regard to the stage of gonadal

development, five fish were not identified.

Among the others, 18 were in the immature

Table 4. Values of the Kruskal-Wallis test to check the influence of gonadal maturity stages (immature, mature,

breeding and resting) on the abundance of parasitism (H1) and values of the Kruskal-Wallis test to check the

influence of seasonal variation (H2) in the abundance of parasites in Salminus brasiliensis collected in the floodplain

of the upper Paraná River (p = significance level).

Species H1 p1 H2 p2

Cladocystis intestinales 1.74 0.63 9.57 0.08

Monticellia coryphicephala 0.87 0.83 0.64 0.98

Octospiniferoides incognita - - 2.55 0.77

Contracaecum spp. larvae 0.11 0.75 0.68 0.98

Contracaecum sp. larvae type 2 1.61 0.65 14.92 0.010*

*Significant values

0.97) (Table 8). This same parasite species,

showed significant negative correlation between

their abundances and relative condition factor of

hosts (Table 5).

The relative condition factor differed between

parasitized and non-parasitized hosts only for

Contracaecum sp. larvae type 2, where the fish

parasitized by this species showed Kn average of

0.86, lower than the non parasitized fish (Kn =

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Karling et al.

Host-parasite relationship Salminus brasiliensis

Table 5. Values of the "U" test, Mann-Whitney, with normal approximation "Z", to check for differences between the

relative condition factor of parasitized and non-parasitized individuals and analysis values of the correlation

coefficient "rs", relative condition factor and abundance of parasitism of Salminus brasiliensis collected in the

floodplain of the upper Paraná River (p = significance level).

Species Z p rs p

Cladocystis intestinales 0.81 0.41 0.04 0,75

Monticellia coryphicephala 0.64 0.52 -0.09 0.51

Octospiniferoides incognita 0.55 0.58 0.08 0.55

Contracaecum spp.larvae 1.24 0.21 -0.16 0.22

Contracaecum spp. larvae type 2 2.61 0.00* -0.33 0.01*

*Significant values

The number of species of parasites in the

infracommunities may vary between hosts

according to the degree of the success of

infection of the parasite (Poulin, 1996). The

same author mentions that this probability is

directly related to the parasite reproductive rates

and their ability to disperse and settle. Even in

rich component communities, the co-occurrence

of species in a single infracommunity is unlikely,

unless the prevalences of all species are very

high. To Salminus brasiliensis, no parasite

species showed concentration for dominance,

probably because there is no competition in the

infracommunity.

Parasites may or may not present a pattern of

patchy distribution in their hosts. The aggregate

distribution occurs when most hosts shelter no or

few parasites and few hosts shelter many

parasites (Poulin, 1998). The aggregate

distribution pattern observed for endoparasites

of S. brasiliensis was also found by other authors

in the Floodplain of the Upper Paraná River

working with other families of fish like cichlids,

pimelodids and prochilodontids (Machado et al.,

2000 Guidelli et al., 2003; Lizama et al., 2005).

This type of distribution tends to increase the

stability of the host-parasite relationship, since

regulatory mechanisms (host mortality, reduced

fecundity and survival of the density dependent

parasite) influence the proportion of their

DISCUSSION populations (Dobson, 1990). Only M.

coryphicephala showed random distribution.

This distribution may be due to reduced

opportunity to colonize the host, or whether this

parasite presents a major pathogenic effect.

Negative associations may be a result of

competition between species in a host.

Competition occurs when two or more species

use the same resources and these are depleted

(Piankas, 1983). In this study, there was a

positive association between the species O.

incognita and Contracaecum sp. larvae. This

may be related to infection strategies and not

direct interaction of these species since they

have different infection sites: Acanthocephala

inhabits the intestine, while Nematoda inhabits

the mesentery. This hypothesis is consistent with

Dobson (1990), which concluded that the

abundance and distribution of parasites are a

direct result of the characteristics of the life

cycles of parasites and species interactions.

The hosts with larger body size are generally

older and usually more heavily parasitized due

to higher nutritional needs (Mccornmick &

Nickol, 2004). Also, higher values of intensity of

infection in larger specimens may be related to

the accumulation of larvae in the host by

repeated processes of infection (Luque et al.,

1996). Factors such as the quantity and type of

food consumed, prey size, exposure time,

increasing surface area of the body and habitat

changes may be responsible for the increase in

224

Neotrop. Helminthol., 7(2), 2013

the prevalence and abundance of infection with

increasing age of the host (Dogiel, 1961;

Pennycuick, 1971; Hanek & Fernando, 1978).

Thus, it is expected that the trophically acquired

parasites are abundant in larger fish.

Studying the structure and diversity of the

community of endoparasites of Piaractus

mesopotamicus Holmberg 1887 and their

interactions with the host, in the Pantanal (MS),

Fields et al. (2009) observed that the species of

Nematoda Spectatus spectatus Travassos, 1923

showed significant positive correlation between

total length and parasite abundance. The same

results were reported by Machado et al. (2000);

Lizama et al. (2008) and Ceschini et al. (2010) in

the floodplain of the upper Paraná River. In this

study there was no correlation between the

standard length and the prevalence and

abundance of parasites of S. brasiliensis. Based

on this result, we can infer that the host-parasite

relationship is tightly adjusted.

Distinctions in parasitism in hosts males and

females may be an important factor when energy

needs unequal, different eating habits or

physiological differences occur among both

sexes (González-Acuña, 2000). Parasites tend to

have more access to individuals whose gender

have higher nutritional needs (Riffo & George-

Nascimento, 1992).

Several studies relating the host sex and the

infracommunity of endoparasites have been

performed. Lizama et al. (2008), Albuquerque et

al. (2008) and Moreira et al. (2009) observed no

influence of sex on prevalence and intensity of

parasitism. The lack of relationship between

parasite indexes with host sex has been

interpreted as a consequence of the similarity of

the biological parameters of fish (Luque et al.,

1996).

According Guidelli et al. (2003) many species of

endoparasites of Hemisorubim platyrhynchos

(Valenciennes, 1840) presented positive

correlation with the size and sex of the host,

which may be due to the volume of food ingested

and possible behavioral changes between the

sexes, with females more parasitized. This same

correlation was reported by Carvalho et al.

(2003) for the parasites of Acestrorhynchus

lacustris (Lütken, 1875), and Isaac et al. (2004)

studying Gymnotus spp.

In this study only two species (O. incognita and

Contracaecum sp. larvae) were influenced by

host sex on the prevalence of parasitism, the

females being the most affected, but there were

no significant influences regarding abundance

of parasitism. This indicates that differences

may exist between behavioral and physiological

hosts males and females.

During the development of a fish, several factors

may interfere directly on the constitution of their

parasite fauna. The maturation for example,

hormonal conditions can trigger behavioral and

physiological differences between male and

female host, allowing different patterns of

parasitic infection (Esch et al., 1988; Guégan &

Hugueny, 1994; Takemoto et al., 2005a).

Studying isopods ectoparasites of

Scomberomorus brasiliensis Collette, Russo &

Zavala-Camin, 1978, Lima et al. (2005)

observed that these parasites have a preference

for younger fish and was attributed these results

to the energy reserves, because mature fish have

fewer energy resources due to mobilization for

gonadal maturation and reproduction.

To S. brasiliensis there was no relationship

between the level of parasitism and stage of

gonadal maturation of the host, this probably

occurred by the small number of specimens in

each maturity stage.

Numerous factors affect the abundance and

prevalence of parasites, and temperature is one

of the most important in the host-parasite

relationship and the environment (Kennedy,

1982). Seasonal events, like most ecological

parameters, have varying effects that depend on

the species involved and the combination of

parameters in a particular area of study

(Lawrence, 1970). The summer months

generally have higher abundances of parasites

since is the same period the fish feeds more

actively (Dogiel, 1961).

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Karling et al.

Host-parasite relationship Salminus brasiliensis

Kadlec et al. (2003) studied the parasite

community of three species of fish (Rutilus

rutilus (Linnaeus, 1758), Rhodeus sericeus

amarus (Bloch, 1782) and Perca fluviatilis

Linnaeus,1758) during a major flood. The

authors concluded that the three species respond

differently to changes in water level with an

increase of parasitism in P. fluviatilis in the

summer.

In the present study, there was an increase in the

abundance of Contracaecum sp. larvae type 2 in

S. brasiliensis in the warmer months. Pertierra &

Nuñes (1995) observed that the temperature

triggers physiological processes for the

development of the parasite. This result can also

be related to the fact that breeding season of the

species, between October and January (Suzuki et

al., 2004), which should be influencing the

hormonal variation of the host, resulting in a

greater abundance of this parasite.

In natural environments parasites usually do not

cause significant damage to their hosts with rare

records of high mortality rates. Under these

conditions, the prospect is that over time there is

an equilibrium between coevolutive host-

parasite interactions, because there is no

advantage to the parasite to damage the host to

the point of being harmed himself (Chisholm &

Whittington, 2008). This equilibrium can be

destabilized by interference from natural or

artificial processes such as atypical variations of

physico-chemical parameters of the

environment, polluting processes, health of the

host and greater predation pressure and

interspecific competition.

The welfare of fish can be measured by

condition factor (K). According to Le Cren

(1951), this factor is a quantitative indicator of

the degree of healthiness and wellness of fish,

reflecting recent dietary conditions, given by the

length / weight relationship of the individual.

But the relative condition factor (Kn) takes into

account the expected and the observed weight.

Variations are influenced by the environment,

lack of food or even parasitism cause changes in

this value, and under normal conditions the

optimal value is one.

Studies on the condition factor of parasitized

fish show that parasitism may be related to low

values (Tavares-Dias et al., 2000) or high values

of the condition factor of hosts (Lizama et al.,

2006; Moreira et al., 2010), and also may not

provide correlation (Ranzani-Paiva et al., 2000;

Dias et al., 2004; Moreira et al., 2005; Tavernari

et al., 2005).

Analyzing the differences of Kn of parasitized

and non-parasitized individuals of S.

brasiliensis, we observed a significant

difference just in Contracaecum sp. larvae type

2. This suggests that non parasitized fish have a

better condition factor, since they are not

influenced by parasitism.

The Kn of S. brasiliensis and abundance

Contracaecum sp. larvae type 2 covaried

negatively, demonstrating that most infected

individuals have lower Kn. This negative

covariance can be explained by the

pathogenicity of the parasite.

In conclusion, the community of parasites of S.

brasiliensis did not have a dominant species.

Four of the five most prevalent parasite species

showed aggregated distribution. In relation to

other aspects of the community, each group

presented their particular parasite, which

highlights the differences inherent in the biology

and life cycle of each species.

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Correspondence to author/ Autor para

correspondencia:

Letícia Cucolo Karling

Programa de Pós-graduação em Ecologia de

Ambientes Aquáticos Continentais (UEM).

Universidade Estadual Maringá, Laboratório de

Ictioparasitologia, CEP: 87020900, Maringá,

Paraná, Brazil.

E-mail / Correo electrónico:

lekarling@hotmail.com

Received August 12, 2013.

Accepted September 24, 2013.

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