271

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

DIVERSITY OF NEMATODES OF RED-TAIL-LAMBARI ASTYANAX AFF. PARANAE

(TELEOSTEI: CHARACIDAE) FROM POLLUTED SITES OF A TROPICAL RIVER SYSTEM

DIVERSIDAD DE LOS NEMATODOS DE TETRA COLA ROJA ASTYANAX AFF. PARANAE

(TELEOSTEI: CHARACIDAE) DE SITIOS CONTAMINADOS DE UN SISTEMA DE RÍO

TROPICAL

1* 1 2 3 2

Thamy S. Ribeiro , Nédia C. Ghisi , Alberto J. Prioli , Elton C. Oliveira & Ricardo M. Takemoto

Abstract

Keywords: bioindicators - environmental alteration – fish - parasites.

Suggested citation: Ribeiro, TS, Ghisi, NC, Prioli, AJ, Oliveira, EC & Takemoto, RM. 2013. Diversity of nematodes of red-tail-

lambari Astyanax aff. paranae (Teleostei: Characidae) from polluted sites of a tropical river system. Neotropical Helminthology,

vol. 7, n°2, jul-dec, pp. 271 - 281.

1Post-Graduation Program in Ecology of Aquatic and Inland Environment; State University of Maringá (UEM), Paraná, Brazil. Fax:+554430114642

2Biological Institute Center; CNPq Scientific Researcher on Nupélia, State University of Maringá (UEM), Maringá, Paraná, Brazil.

3Environmental Engineer Coordinator, Federal Technologic University of Paraná (UTFPR), Campo Mourão Campus, Paraná, Brazil.

*thamysantos@yahoo.com.br

Neotrop. Helminthol., 7(2), 2013

2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

Aquatic systems are affected by a great variety of anthropogenic activities that alter the water

quality through the introduction of organic and inorganic pollutants, consequently impacting all

trophic levels of a biological community. The relationship between parasite species diversity and

organic pollution in the high Paraná River basin, Paraná, Brazil was investigated during two

seasons (Winter and Summer) of 2011. A total of 114 red-tail-lambari (Astyanax aff. paranae

Eigenmann, 1914) were sampled from a non-impacted location (Perobas Reserve) and from

impacted regions (agricultural and urban regions, upstream and downstream the city of Campo

Mourão, respectively). The nematode Spinitectus yorkei Travassos, Artigas & Pereira, 1928 was

found on the preserved area, while the nematode Procamallanus (Spirocamallanus) inopinatus

Travassos, Artigas & Pereira, 1928 was found only on the severely polluted areas. The variability

of the prevalence index suggests that the structure of the parasite community is affected at

different ways by the same levels of pollutants on the water. The observed results assume that the

alteration in parasite diversity can be related to increased organic pollution, and that the

differences in the parasite community from different environments can be related to biotic stress.

Resumen

Palabras clave: bioindicadoras - alteración del medio ambiente – pescado - parasitos.

Los sistemas acuáticos se ven afectados por una gran variedad de actividades antropogénicas que

alteran la calidad del agua a través de la introducción de contaminantes orgánicos e inorgánicos,

por consiguiente, afectan a todos los niveles de la comunidad biológica. De esta forma, la relación

entre la diversidad de especies de parásitos y la contaminación orgánica en la cuenca del alto

Paraná, Paraná, Brasil, se investigó en dos temporadas (invierno y verano) de 2011. Un total de

114 tetra cola roja (Astyanax aff. paranae Eigenmann, 1914) se muestrearon en un sitio no

impactado (Reserva Perobas) y en regiones impactadas (zonas agrícolas y urbanas, aguas arriba y

aguas abajo de la ciudad de Campo Mourão, respectivamente). El nematodo Spinitectus yorkei

Travassos, Artigas y Pereira, 1928 se encuentran en la zona protegida, mientras que el nematodo

Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas y Pereira, 1928 se encuentran

sólo en las zonas gravemente contaminadas. La variabilidad del índice de prevalencia sugiere que

la estructura de la comunidad de parásitos se ve afectada en diferentes formas por el mismo nivel

de contaminantes en el agua. Los resultados observados asumen que la alteración en la diversidad

parasitaria puede estar relacionada con el aumento de la contaminación orgánica, y que la

respuesta de la comunidad de parásitos a las tensiones ambientales puede ser utilizada como

bioindicadora.

Acantocephala group as an indicator, by

accumulation, of metal pollution (Sures, 2003,

2004).

The fact that parasites possess complex life

cycles makes them extremely valuable

information units about environmental

conditions, because their presence/absence, as

their ecological indexes, tell us a great deal not

only about their host ecology but also about the

ecosystem biodiversity and food web

interactions, and about the environmental stress

that may be occurring on the system (Overstreet,

1997; Marcogliese, 2003, 2004; Madanire-

Moyo & Barson, 2010). Each parasite species

reflects the presence of different organisms that

participate in its life cycle; together, all these

parasite species in a host reflect the presence of a

plethora of host organisms and the trophic

interactions in the environment (Marcogliese &

Pietrcock, 2011). Given that pollution may have

impacts on populations and communities, and

thus on food web structure, parasites may be

used as natural biological tags of ecosystem

health. The species composition of parasite

communities is clearly impacted by

environmental stress, and species richness and

Most of the human impacts on the aquatic

environment affects all the levels of a biological

community, including the parasites populations;

this have been confirmed with many

observations about changes in parasite

abundance or richness as a consequence of

environmental impacts that interfere on free-

living stages of the parasites and/or on the hosts

populations (intermediate, definitive or

paratenic) (Poulin, 1992; Marcogliese & Cone

1997; Sures, 2004; Costa et al., 2012).

The relative abundance of endo- and

ectoparasites of fish in a particular aquatic

system can be used as an indicator of

environmental stress (Avenant-Oldewage,

2001). Ectoparasites, for having direct contact

with water, present the same responses of free-

living organisms, while protozoic endoparasites

seems to be too small to provide sufficient

material to analysis (Sures et al., 1999; Sures,

2001, 2003, 2008; Sures & Reimann, 2003;

Vidal-Martínez et al., 2009). As a general

pattern, the cestodes and nematodes seem to be

good as sentinel species, specially the

INTRODUCTION

272

Diversity of nematodes of Astyanax Ribeiro et al.

Neotrop. Helminthol., 7(2), 2013

basin, Northwest of Paraná state, South of

Brazil. On the Concórdia stream one sample

point has been established and it was considered

the positive control area owing to the absence of

intensive agricultural, industrial and mining

activities close to the river. The headspring of the

Concórdia stream is located on the Perobas

Biological Reserve damping area and heads to

the referred conservation unity. The Perobas

Biological Reserve (RE) (23°51'16"S,

52°45'2"O) belongs to the Tuneiras do Oeste and

Cianorte counties, and it was established on

2005, representing, according to the Federal

Law 9985 of 2000, a full protection unity,

objectifying the biodiversity protection, with

restricted use to scientific researches and

management actions (Fig.1).

The other two collection points were placed on

the Campo River (24°10' S, 52°31' O): 1- the

Upstream Point (UP), that is surrounded only by

agriculture areas, not crossing the urban area; 2-

the Downstream Point (DP), that is located right

after the urban area and is characterized by the

influx of different effluents from the Campo

Mourão city, including wastes from industries

and from the sewer treatment. The collection

sites are presented on Figure 1.

Fish and parasite collection

Fishes were collected over two seasons: the first

one on July (Winter) 2011, which correspond to

the plantation of corn and wheat; the second

period was on November (Summer) 2011, which

correspond to the plantation of soybean.

To evaluate the impact of the industrial, sewage

and agricultural activity on the water quality,

several analyses have been performed. Surface

water temperature ( C) and Dissolved Oxygen

(DO, mg/L) content were measured using a

HACH oxygen meter; the conductivity (µS/cm)

was measured by a WTW conductivity meter

and pH using a HACH pH meter. Subsurface

water samples were collected in 1L plastic

containers rinsed in deionized water. The

samples were taken to the laboratory where they

were analyzed for the following compounds:

copper, zinc, aluminum and total phosphorus,

according Standard Methods of APHA, AWWA,

abundance tends to change under degraded

conditions (Sures, 2008).

The selected host, Astyanax aff. paranae,

popular known as “red-tail-lambari”, is a

common species of the Paraná River basin

(Garutti & Britski 2000) and its occurrence was

registered as very abundant on the Paraná river

tributaries (Luiz et al., 2003). It is characterized

by an omnivorous food habitat and sexual

dimorphism, females being more robust than the

males (Eigenmann, 1914; Godoy, 1975; Barbieri

1992; Ferreira, 2004). The characteristics used

to its identification are described on Garutti &

Britski (2000). The host selection was afforded

by the studies of Overstreet (1997), Sures (2004)

and Lewis & Hoole (2003). According to these

researchers, the host must have a restricted home

range, abundant populations of easy sampling

and identification, wide geographic distribution

and a great number of parasites – preferentially

parasite species that present abundant numbers

of hosts on their cycles.

This study intended to establish the relationship

between the metazoan parasites and the

pollution levels in the sampled places. The

specific objectives of this study were to

determine the biodiversity of metazoan parasite

communities of Astyanax aff. paranae

Eigenmann, 1914 in the upper Paraná River

basin and to compare the diversity of metazoan

parasite fauna along defined pollution gradients,

assessing the suitability of using parasites as

predictors of environmental change. Due to the

great diversity of the stress effects on the hosts

and on the parasites populations, it is believed

that the metazoan community of A. aff. paranae

of the affected areas, whether by agricultural or

urban pollutants, will present lower levels of

parasite richness, but an increase on the

prevalence and abundance of the species

resistant to the environmental stressors.

Study area

The data used on the present work were collected

in two hydric systems of the high Paraná River

MATERIALS AND METHODS

273

parameters previously stipulated and analyzed

on each collection (Vanzolini, 1993).

The bifactorial ANOVA was performed on the

STATISTICA software (version 5.5), right

before the Tukey test. The points and the seasons

of each collection were the factors considered on

these analyses. Parasite prevalence and

abundance were measured and calculated as

defined by Bush et al. (1997).

Voucher specimens of some collected

individuals were accommodated on the

Ichthyological Collection of the Limnology,

Ichthyology and Aquiculture Research Center:

the UP and DP fishes NUP 13381 and Field:

NCG2011103101; the RE fishes NUP13382 and

Field NCG2011071701.

Water quality

The glyphosate analysis on the water samples

revealed that this compound concentrations

were below the minimum detection levels

commercially available and, for this reason,

couldn`t be obtained. The results of the chemical

analysis performed on the three locations water

samples are on the Table 1.

The water temperature varied with the time of

sampling, ranging from 17.0 to 21.25 C. The

highest level of DO was at RE during the Winter

(8.34 mg/l), and the lowest level was at DP

during the Summer (5.78 mg/l). The highest

level of conductivity readings was at the DP (42-

86µS/cm). Water pH presented a light and

continuous increase from the preserved area

(RE) to the disturbed collection points (pH

range: 6.67–7.5). All the nutrients analyzed were

quite low on the control area (RE) and higher on

the UP and DP, probably indicating an

eutrophication process. All the water sampled on

the UP and DP had higher levels of nutrients

(Table 1). It was observed an increased level of

heavy metals (aluminum, copper and zinc),

phosphates, conductivity and a reduced DO

observed on the urban area of Campo Mourão

(DP), while the RE remained comparatively

WEF (2005). On these same water samples

analyses have been made to determine the

glyphosate concentration, as this is the main

compound of the fertilizers used on the

geographic area, by gas chromatography/mass

spectrometry performed the São Paulo

University Chemistry Laboratory.

The RE collection was performed by the sieving

methodology, owing to the few individuals

observed on the reserve stream. The sieves nets

had the dimensions of 0.60 X 1.2 m and 0.30 cm;

the sieving was performed through active

overhaul on the macrophyte banks and on the

marginal micro-habitats. The fish collection on

the UP and DP was made using a seine net with a

dimension of 1,2 m x 5 m, which was installed

parallel to the river, overhauled from hour to

hour.

Right after the collection, the fishes were

sacrificed through benzocaine hydrochloride

overdose, and the standard and total lengths

(mm) and mass (g) of each fish were recorded.

The fishes were kept in alcohol 96% and were

then transported to the laboratory, where the

specific identification was confirmed and, after

ventral incision, the sex was recorded and

portions of the muscles, viscera and the

gastrointestinal tract were dissected and

examined under stereomicroscope for internal

parasites. The nematodes and digeneans were

fixed in formaldehyde and then preserved in

70% alcohol. They were then cleared and

mounted according to Eiras et al. (2006), and

identified according Moravec (1998).

Data analysis

To the evaluation of the interactions between the

collected specimens and the biotic and abiotic

factors, the allometric factor condition (K) was

calculated, according the following equations:

W = a * L ; where: W = total weight, L = total

weight, a = intercept e b = angular coefficient

(Le-Cren, 1951). The “a” and “b” parameters

were estimated after weight and length

logarithmic transformation, and subsequent

adjust through least mean square analysis

technique (Vanzolini, 1993). The K was

estimated by K=W/L*b, using the same

RESULTS

274

Diversity of nematodes of Astyanax Ribeiro et al.

Neotrop. Helminthol., 7(2), 2013

Parasite composition, richness and distribution

A total of 22 “red-tail-lambari” out of the 114

fishes caught were infected with parasites. Five

species of metazoan parasites were observed on

the 22 infected fishes collected from the three

collection points (Table 2). The endoparasites

included four nematode species (larval

Contracaecum, adult Procamallanus

(Spirocamallanus) inopinatus Travassos,

Artigas & Pereira, 1928, adult Cucullanus

(Cucullanus) brevispiculus Moravec, Kohn &

Fernandes, 1993 and adult Spinitectus yorkei

Travassos, Artigas & Pereira, 1928). Parasite

species richness increased as the chemical

compounds levels increased (Table 2). The less

altered location, the RE point collection,

presented only one species of parasite (S.

yorkei), while the location with higher levels of

nutrients, the DP, had three species of parasites

(P. inopinatus, C. brevispiculus and larval

Contracaecum). On the UP, during the Winter, it

has not been observed any species of parasites

(Table 2).

unimpacted; the agricultural local (UP)

presented intermediary levels (Table 1).

Hosts` condition

The bifactorial ANOVA, performed with the K

fish values, revealed an interaction among the

period of the year and the collection points

(p<0.05), demonstrating that season and locality

did not act independently on the fishes`

condition. Consequently, the group analyzes of

these factors have been obligatorily performed.

The Tukey test revealed that the K values during

the winter were significantly inferior than the

Summer values. During the winter, significant

differences between the collection points have

not been visualized. The highest K values have

been observed on the DP during the summer, but,

during this same period, the fishes from UP and

RE also presented high K values. Significant

differences have been observed among all the

collection points during the summer (Fig. 2).

Figure 1. Localization of Campo Mourão county on the State of Paraná, Brazil. Visualization of the collection points (*) on the

Biological Reserve of Perobas and on Upstream and on Downstream of Campo Mourão city - PR. Source: SEMA Campo

Mourão.

275

sites with higher eutrophication levels (Table 2).

The distribution of P. inopinatus and C.

brevispiculus was limited to DP, the most altered

collection site. The C. brevispiculus have been

observed only on the UP collection point during

the Summer. The severely altered site (DP)

demonstrated close association with P.

inopinatus and C. brevispiculus.

The S. yorkei seems to be sensitive to

eutrophication as its presence has not been

recorded on the most altered site (DP), but more

studies are necessary to confirm this punctual

observation (Table 2). The other nematodes (P.

inopinatus, C. brevispiculus and larval

Contracaecum) seem to be very tolerant to

organic pollution as they are associated with the

Figure 2. Mean and confidence interval of the hosts Condition Factor (K) values by collection point and by collection season.

a,b,c = Tukey`s test results (different letters represent statistical differences p<0.05); Perobas Biological Reserve (RE), Upstream

Point (UP), Downstream Point (DP).

Table 1.Chemical analyzes of the water samples collected on the Perobas Biological Reserve (RE), on the Upstream

of the Campo river (UP) and on the Downstream of this same river (DP), on June (Winter) and on November

(Summer). Aluminum (Al), Copper (Cu), Zinc (Zn), Phosphorus (P), Dissolved Oxygen (DO), Temperature (T).

RE UP DP

Chemical

Compounds

analyzed

Winter

Summer

Winter

Summer

Al (mg/L)

0.77

0.89

1.04

0.945

0.74

0.868

Cu (µg/L)

1.6

7.3

1.9

0.5

4.2

Zn (µg/L)

1.7

3.7

5.2

3.45

3.7

4.8

P (µg/L)

0.0124

< 0.01

0.091

0.945

0.0183

0.054

DO (mg/L)

8.34

7.16

6.36

6.09

7.99

5.78

6.67

6.83

6.9

6.81

7.21

7.5

T (oC)

18.89

18.01

21.25

19.92

Conductivity

(µS/cm) 25 40 20 29 86 42

276

Diversity of nematodes of Astyanax Ribeiro et al.

Neotrop. Helminthol., 7(2), 2013

Table 2. Parasite species found on the Perobas Biological Reserve (RE), on the Upstream of the Campo river (UP)

and on the Downstream of this same river (DP), with the respective values of Prevalence (Prev.) and Mean

Abundance (MA).

Collection

sites

Pollution

class

Collection

period

Collected

fishes

Parasitized

fishes Parasites Prev.

Winter

6 S. yorkei (n=9) 32% 0.18

Non-polluted

Summer

1 S. yorkei (n=2) 6,7%

0.33

Polluted

Winter

Summer

0 S. yorkei (n=1)

0.12

P. inopinatus (n=4) 18% 0.18

Winter

4 Contracaecum sp. (n=1) 4% 0.2

P. inopinatus (n=4) 21% 0.33

Severely

polluted

Summer 33 10 C. brevispiculus (n=4) 9% 0.12

DISCUSSION Summer, there was a phosphorus concentration

increase in all the three collection points, which

is explained by the discharge of decomposition

products by the summer rains. It is clear that the

agricultural and urban wastes contribute to the

nutrient loading to the Campo River.

Hosts` condition

The K values significantly inferior during the

Winter could reflect a natural stress situation,

when the temperature is lower and the system

productivity is diminished. Probably the

specimens are more influenced by these factors,

independently the location they are collected.

On the Summer, the availability of nutrients

increases mainly because the high levels of

temperature, rainfall and the higher activity of

decomposers during this period (Jobling, 1995).

However, local factors seems to also influence

the fishes' condition, as observed to the

specimens collected on DP, where the urban run-

offs finds its way into the Campo river – what

can explain the higher nutrient levels at the water

samples and the better nutritional situation of the

fishes.

Usually, organic polluted environments present

higher levels of productivity (Colinvaux, 1993),

what can be advantageous to species with more

plasticity, making the accumulation of energetic

reserve easier and, consequently, improving

their Condition Factor (Alberto et al., 2005). On

the present study it was not observed a negative

relation between the inorganic pollutants

observed on the water (aluminum, zinc and

Water quality

Despite the fact that the RE water samples

presented high concentrations of some of the

evaluated compounds, the highest values of

phosphorus, conductivity, pH, temperature, zinc

and copper were observed on the Campo River,

which confirms the assumption that the UP and

DP would be the most altered locations.

According to the National Council of

Environment (CONAMA), the water from all

the three collecting points is inappropriate to

human consumption; however, the high

aluminum concentrations in all the collection

sites are explained by the characteristic soil of

the region, which presents great quantity of this

compound (Pavan et al., 1985).

The higher conductivity at the UP and at the DP

may be attributed to urban and agricultural

effluent saturating these locations, while the

slight decrease in conductivity during the

Summer on both locations could be correlated to

different plantations during this period.

Different plant`s production leads to the

different agrotoxic needs, what will unleash

different compounds on the water, especially the

ionic factors – the main elements responsible for

the water conductivity (Kunze et al., 1968).

Increased urbanization and poorly treated

effluent discharged into the Campo river are

probably responsible for the high conductivity,

especially on the DP collection point. During the

277

The eutrophication process may also act directly

on intermediate hosts and definitive hosts. The

results are consistent with the general patterns

found by Poulin (1992), Hartman and Numann

(1977), Beer & German (1993), Lafferty &

Kuris (1999), Lafferty (1997) and with the study

performed by Valtonen et al. (1997), all

suggesting a positive relationship between

eutrophication and fish parasitism.

Eutrophication often raises parasitism because

the associated increased productivity can

increase the abundance of intermediate hosts

(Lafferty & Kuris, 1999).

The eutrophic nature of the DP contributed to the

observed high prevalence values of the helminth

community of A. aff. paranae at the polluted

sites. The eutrophication probably increased the

abundance of the intermediate hosts, a result of

the sewage outflows; this eutrophic process is

also reflected on organic enrichment of the

sediments, providing excellent habitat for the

alternative hosts (Weisberg et al., 1986; Sibley et

al., 2000). The presence of the nematodes in the

polluted sites is also made possible by their

possession of a cuticle, which enables them to

withstand the harsh conditions, as the water

pollution can influence aquatic endoparasites

both directly and indirectly by acting on their

intermediate hosts.

There is still missing a significant quantity of

information about promisors bioindicative

processes, such as biomarkers, and about the use

of parasites as bioindicators (Williams &

Mackenzie, 2003; Vidal-Martinez et al., 2009;

Sures, 2008) but the accumulation of data by

serious researches performed along the years

could reveal how each parasite species respond

to environmental alterations. The initial

hypothesis was not corroborated, as the affected

areas presented higher species richness, but this

could be related to the short collection period or

to the few hosts analyzed. However, the results

here presented possibly indicate that the parasite

assemblages may be good indicators of

environmental stress because they reflect the

presence of many different types of organisms,

based on the variety of complex life cycles

displayed by the different parasite taxa.

copper) and the K values of the hosts, what

possibly indicates use of Astyanax aff. paranae

as an accumulation bioindicator, but more

studies and experiments are necessary to

confirm the absence of morpho-physiological

alterations after the exposure to high

concentrations of the inorganic compounds.

Therefore, it is possible to assume that the

alterations observed on the parasite population

indexes are not due to the diminished

immunological hosts` capacity, as the K values

did not reveal any condition loss by the hosts.

Analyzing the information obtained on this

work, the responses to environmental alterations

is not restrained to the ichthyologic community,

but it is also observed on the parasite

community. Despite the fact that the K values

were not affected by the high inorganic

compounds concentration, the hosts` parasite

infracommunities from the RE e from DP were

entirely different, a clear evidence that the

parasite community responds to the

environmental alterations and can be used as a

bioindicator.

Parasite composition, richness and

distribution

Two parasite species presented bioindicator

capacity – Spinitectus yorkei and

Procamallanus (Spirocamallanus) inopinatus.

The first one has not been found in severely

altered locations, so this sensitiveness probably

indicates its importance as Effect Bioindicator.

P. inopinatus may also represent a bioindicator

species, specifically an Accumulation

Bioindicator, for its toleration to the prejudicial

effects that could occur after the exposure to the

organic and inorganic compounds found on

some of the collection points.

The presence of S. yorkei on UP during the

winter could be explained by the similar water

concentrations between this collection point on

this period and the RE. Except for the copper

concentration, all the other parameters analyzed

on the UP are similar to the reserve values.

Possibly, the copper concentration belatedly

acted, which can explain the complete absence

of parasites on UP during the summer.

278

Diversity of nematodes of Astyanax Ribeiro et al.

Neotrop. Helminthol., 7(2), 2013

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Diversity of nematodes of Astyanax Ribeiro et al.

Neotrop. Helminthol., 7(2), 2013

Correspondence to author/ Autor para

correspondencia:

Thamy S. Ribeiro

Post-Graduation Program in Ecology of Aquatic

and Inland Environment; State University of

Maringá (UEM), Paraná, Brazil.

Fax:+554430114642.

E-mail / Correo electrónico:

thamysantos@yahoo.com.br

Received September 4, 2013.

Accepted September 29, 2013.

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