PARASITISM ASSOCIATED WITH LENGTH AND GONADAL MATURITY STAGE OF THE

FRESHWATER FISH METYNNIS LIPPINCOTTIANUS (CHARACIDAE)

PARASITISMO ASOCIADO A LA LONGITUD Y AL ESTADO DE MADUREZ GONADAL DEL

PEZ DE AGUA DULCE METYNNIS LIPPINCOTTIANUS (CHARACIDAE)

Neotrop. Helminthol., 6(2), 2012

2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

Fábio Hideki Yamada*, Luís Henrique de Aquino Moreira, Tiago Lopes Ceschini, Maria de los Angeles Perez Lizama,

Ricardo Massato Takemoto & Gilberto Cezar Pavanelli

Laboratório de Ictioparasitologia/Nupelia, Universidade Estadual de Maringá, Bloco G-90, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brasil.

*e-mail: fhyamada@hotmail.com

247

Abstract

Parasitism was observed in 72.7% of 44 specimens of Metynnis lippincottianus (Cope, 1870) (Characidae)

caught in the Upper Paraná River floodplain, Brazil. One species of digenean, Dadayus pacupeva Lacerda,

Takemoto & Pavanelli, 2003, and four species of nematodes, Spinoxyuris oxydoras Peter, 1994,

Contracaecum sp. Railliet & Henry, 1912 (larval stage), Procamallanus (Spirocamallanus) inopinatus

Travassos, Artigas & Pereira, 1928 and Raphidascaris (Sprentascaris) mahnerti Petter & Cassone, 1984

were identified. The prevalence of D. pacupeva was correlated with the host's standard length. Correlations

between the host's standard length and the abundance of S. oxydoras, P. (S.) inopinatus and D. pacupeva

were observed. In addition, fish length was correlated with the diversity of parasites. D. pacupeva and S.

oxydoras had their abundances influenced by the host's gonadal maturity stage. According to gonadal

maturity stage, the host may or may not have an increased susceptibility to parasites, suggesting a

cumulative process causing higher parasite abundance in larger fish and in the mature stage (more time of

exposure) than the immature stage (young fish).

Keywords: Brazil - Characidae - digeneans - endoparasites - Metynnis lippincottianus - nematodes.

Resumen

Basado en el examen de 44 especímenes de Metynnis lippincottianus (Cope, 1870) (Characidae)

muestreados en la llanura de inundación del Alto rio Paraná, Brasil, el parasitismo fue observado en 72,7%

de los peces. Una especie de digeneo, Dadayus pacupeva Lacerda, Takemoto & Pavanelli, 2003, y cuatro

especies de nemátodos, Peter, 1994, Contracaecum sp. Railliet & Henry, 1912 (forma larval),

Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 y Raphidascaris

(Sprentascaris) mahnerti Petter & Cassone, 1984 fueron identificados. La prevalencia de D. pacupeva se

correlacionó con la longitud estándard del huésped. Se observaron correlaciones entre las longitudes

estándard del huésped y la abundancia de S. oxydoras, P. (S.) inopinatus y D. pacupeva. Además la longitud

del pez estubo correlacionada con la diversidad de los parásitos. D. pacupeva y S. oxydoras tuvieron sus

abundancias influenciadas por el estado de madurez gonadal. De acuerdo con el estado de madurez

gonadal, el húesped puede o nó tener un aumento de la susceptibilidad a los parásitos, lo que sugiere un

proceso acumulativo causando elevada abundancia de parásitos en los peces mayores y en el estado

maduro (mayor tiempo de exposición) que en el estado inmaturo (peces jóvenes).

Palabras clave: Brasil - Characidae - digeneos - endoparásitos - Metynnis lippincottianus - nemátodos.

Suggested citation: Yamada, FH, Moreira, LHA, Ceschini, TL, Lizama, MAP, Takemoto, RM & Pavanelli, GC.

2012. Parasitism associated with length and gonadal maturity stage of the freshwater fish Metynnis lippincottianus

(Characidae). Neotropical Helminthology, vol. 6, N° 2, pp. 247-253.

INTRODUCTION

Yamada et al.

Parasitism of Metynnis lippincottianus

A parasitological study was conducted with

Metynnis lippincottianus (Cope, 1870)

(Characidae) from the Upper Paraná River

floodplain, collected from March 2006 to

December 2007. M. lippincottianus is a freshwater

fish native to South American basins that lives in

waters with temperatures between 20 and 28ºC

(Froese & Pauly, 2009). This species has

commercial (ornamental fish) and ecological

importance, because it belongs to the second

trophic level in the local food web (herbivorous);

its diet consists of plant pieces and sporadically of

arthropods and detritus (Dias et al., 2005). The

host's standard length and maturity stage can

determine high or low levels of parasitism.

Changes in the diet of fish between young and

adults allied to accumulative processes result in

different levels of parasitism for different fish

lengths. The exposure to parasites and the host

health are also influenced by gonadal maturity

stage (GMS) (Bush et al., 2001). This paper aims

to provide information about the accumulative

process of parasites influenced by the host's

standard length and GMS in M. lippincottianus.

Forty-four specimens of M. lippincottianus were

collected, between March 2006 and December

2007, in the Upper Paraná River floodplain

(22°43'S and 53°10'W), Brazil. Fishes were

captured using gill nets. The standard length and

GMS of each fish were registered, and the internal

organs and visceral cavity were analysed under a

stereomicroscope. The collected parasites were

treated according to Eiras et al. (2006) and

identified according to Travassos et al. (1969);

Yamaguti (1971); Moravec (1998) and Lacerda et

al. (2003). Prevalence and abundance were

determined for all identified parasite species. GMS

was determined following the scale proposed by

Vazzoler (1996).

Data analyses were made using the following

statistical tests: Spearman's rank correlation (rs)

and the Pearson linear correlation (r) were used to

verify correlations between the host's standard

length and the abundance and prevalence of

parasites, respectively. Fish were separated into

length classes, with angular transformation (arc

sine √x) of prevalence data prior to using

Pearson's linear correlation (r). Diversity of the

parasite community was evaluated using the

Brillouin index, and Spearman's rank correlation

was used to correlate the diversity of parasites and

the host's length. The Kruskal–Wallis test was used

to verify the variation of parasite abundance

according to the host's GMS (Zar, 1996). Statistical

analysis was applied to parasite species with over

10% of prevalence and the results were considered

significant when p ≤ 0.05. The ecological terms

were suggested by Bush et al. (1997).

Of the 44 examined hosts, 32 (72.7%) were

infected by at least one species of helminth

248

MATERIAL AND METHODS

Table 1. Number of specimens (N), prevalence (P), mean abundance (MA), mean intensity (MI) and amplitude of

infection (A) of the parasitic helminthes of Metynnis lippincottianus collected in the Upper Paraná River floodplain,

Paraná, Brazil.

Parasite N P(%) MA MI A

Digenea

Dadayus pacupeva

3568 61.4 81.09 132.1 1-575

Nematoda

Spinoxyuris oxydoras

2879 63.6 65.43 102.8 1-479

Procamallanus

(Spirocamallanus) inopinatus 44 43.2 1.00 2.3 1-9

Raphidascaris (Sprentascaris) mahnerti 1 2.3 0.02 1.0 -

Contracaecum sp.

(larval)

8 11.4 0.18 1.6 1-4

RESULTS

Neotrop. Helminthol., 6(2), 2012

249

endoparasite. One digenean, Dadayus pacupeva

(Lacerda, Takemoto & Pavanelli, 2003) and four

nematode species, Spinoxyuris oxydoras (Petter,

1994), Contracaecum sp. (larval stage; Railliet &

Henry, 1912), Procamallanus (Spirocamallanus)

inopinatus (Travassos, Artigas & Pereira, 1928)

and Raphidascaris (Sprentascaris) mahnerti

(Petter & Cassone, 1984) were identified. The

number of collected specimens, prevalence, mean

abundance, mean intensity and amplitude of

infection for each parasite species are presented in

Table 1.

The host's standard length varied from 1.4 to 13.4

cm. Significant positive correlation between the

host's standard length and the prevalence of D.

pacupeva and S. oxydoras (r = 0.83; p = 0.04 and r

= 0.81; p = 0.05, respectively) was observed (Fig.

1).

There was a significant positive correlation

between standard length and abundance of the

following parasite species: S. oxydoras, P. (S.)

inopinatus and D. pacupeva from the Upper Paraná

River floodplain (Fig. 2).

The average infracommunity diversity of the

parasites of M. lippincottianus in the Upper Paraná

River floodplain was 0.3371 (Brillouin index). A

positive correlation was found between the

diversity of parasites and the host's standard length

(rs = 0.68; p < 0.001).

Five GMS were reported: immature, rest,

maturing, ripe and semi-spent, according to

Vazzoler (1996). There was significant influence

of the GMS on parasite abundance only in D.

pacupeva (H = 24.67; p < 0.001) and S. oxydoras

(H = 24.50; p < 0.001).

Dadayus pacupeva

0 2 4 6 8 10 12 14

Length Classes (cm)

100 r = 0.83

p = 0.04

Spinoxyuris oxydoras

0 2 4 6 8 10 12 14

Length Classes (cm)

100 r = 0.81

p = 0.05

Procamallanus (Spirocamallanus) inopinatus

0 2 4 6 8 10 12 14

Length Classes (cm)

100 r = 0.64

p = 0.17

Contracaecum sp.

0 2 4 6 8 10 12 14

Length Classes (cm)

100 r = 0.38

p = 0.45

Figure 1. Correlation between the standard length of Metynnis lippincotianus and the prevalence of Dadayus pacupeva;

Spinoxyuris oxydoras; Procamallanus (Spirocamallanus) inopinatus; and Contracaecum sp. in the Upper Paraná River

floodplain, Paraná, Brazil (r = Pearson's linear correlation, p = significance level).

Yamada et al.

Parasitism of Metynnis lippincottianus

Spinoxyuris oxydoras

0 2 4 6 8 10 12 14

Standard Length (cm)

100

200

300

400

rs = 0.72

p < 0.001

Dadayus pacupeva

0 2 4 6 8 10 12 14

Standard Length (cm)

100

200

300

400 rs = 0.82

p < 0.001

Procamallanus (Spirocamallanus) inopinatus

0 2 4 6 8 10 12 14

Standard Length (cm)

Abundance

rs = 0.36

p = 0.02

Contracaecum sp.

0 2 4 6 8 10 12 14

Standard Length (cm)

rs = 0.16

p = 0.32

Abundance

Abundance Abundance

Figure 2. Correlation between standard length of Metynnis lippincottianus and abundance of Dadayus pacupeva; Spinoxyuris

oxydoras; Procamallanus (Spirocamallanus) inopinatus and Contracaecum sp. in the Upper Paraná River floodplain, Paraná,

Brazil (rs = Spearman's rank correlation, p = significance level).

DISCUSSION

During ontogeny, changes occur in the behaviour

and biology of fish (Takemoto et al., 1996).

Probably the diet of M. lippincottianus, which is

mainly composed of vegetation, allowed its

infection (ingestion of parasite structures) and the

fish became the definitive host of D. pacupeva, S.

oxydoras, P. (S.) inopinatus and R. (S.) mahnerti.

However, Contracaecum sp. used the fish to reach

higher trophic levels (piscivorous fishes and

birds), making M. lippincottianus act as an

intermediate host. The nematodes identified are

reported in several fishes due to their low

specificity (Moravec, 1998). Some changes in the

diet or habitat can make the adults more vulnerable

(Dogiel, 1961; Hanek & Fernando, 1978) to the

parasite D. pacupeva.

Positive correlations between the standard length

of the host and prevalence were reported

previously in the floodplain with proteocephalid

cestodes in Paulicea luetkeni (Humboldt, 1821)

(=Zungaro zungaro) (Takemoto & Pavanelli,

1994), Proteocephalus microscopicus (Woodland,

1935), Proteocephalus macrophallus (Diesing,

1850) and Sciadocephalus megalodiscus Diesing,

1850 in Cichla monoculus Kullander & Ferreira,

2006 (=Cichla kelberi) (Machado et al., 2000),

Goezeella paranaensis Pavanelli & Rego, 1989,

Spatulifer maringaensis Pavanelli & Rego, 1989

and Mariauxiella piscatorum Chambrier &

Vaucher, 1999 in Hemisorubim platyrhynchos

(Valenciennes, 1840) (Guidelli et al., 2003) and the

nematode Rondonia rondoni Travassos, 1920 in

Pterodoras granulosus (Valenciennes, 1821)

(Dias et al., 2004).

250

251

Neotrop. Helminthol., 6(2), 2012

A significant positive correlation between the

standard length of the host and abundance is

expected in parasites that show low damage to the

host; thus the fish can increase in size and weight,

regardless of parasitism, being capable of

harbouring a larger amount of parasites (Poulin,

1998). The relationship between body length of the

host and parasitic abundance can be a result of the

process of temporal accumulation (Isaac et al.,

2000), increase (Zelmer & Arai, 1998) or change

(Machado et al., 2000) of ingested food and the

dimensions of the sites of infection (internal

organs) as a function of growth (Luque et al.,

1996). Diet changes in adult fishes can include a

large number of items used in the life cycle of

parasites, such as intermediate hosts or even

aquatic plants containing parasite structures

(larvae, eggs), resulting in higher abundance in

larger fishes.

Despite being a tropical fish, usually with many

parasites (Lizama et al., 2005), the endoparasite

diversity was low when compared to that in

temperate regions (Hanzelová et al., 2001). A

positive correlation was found between the

diversity of parasites and the host's standard

length. Probably the larger size of the fish indicates

more food variation during its ontogeny, and,

allied to larger sites of infection, results in higher

parasite diversity (Dogiel, 1961). Positive

correlations have been found in other hosts of the

Upper Paraná River floodplain (e.g. Yamada et al.,

2007).

The Gonadal maturity stage can determine higher

or lower exposure of the fish to parasitism

(migration to places presenting parasites) or even

its susceptibility to parasites (due to the lack of

food or stress). The immature stage presented the

lowest abundances of D. pacupeva and S.

oxydoras, possibly because of the low exposure to

parasites or some variation in the feeding of

younger fishes (such as food items that are not part

of their diet, but will be when they become adults)

(Poulin, 1998). This could explain the fact that fish

with more advanced GMS have high abundances

of D. pacupeva and S. oxydoras, even though the

abundance of specimens at the rest stage are a little

higher in maturation. The semi-spent stage, in

which the fish were more debilitated (lack of food,

high stress and hormonal changes) (Vazzoler,

1996), showed the highest parasitic abundance.

Probably the length of time of exposure to

parasites (accumulative process) and the food

shortages of the semi-spent stage of adult fishes

resulted in high abundance.

High values of abundance of D. pacupeva and low

abundance of S. oxydoras in the mature stage may

not reflect reality, because at this stage only one

specimen of S. oxydoras was collected. The study

of the gonadosomatic index is used as a tool to

increase the knowledge of the reproductive

biology of a fish population. Gil de Pertierra &

Ostrowski de Nuñez (1990) showed that the

reproductive phase of the fish Rhamdia sapo

(Valenciennes, 1836) coincided with the

maximum egg production of the cestode

Proteocephalus jandia Woodland, 1934, whereas

the output of gonadotropin by the fish was in

synchrony with the peak of the ovoposition of the

parasite. This may explain the greater abundance

of D. pacupeva and S. oxydoras at the end of the

reproductive period. The absence of mature

specimens and/or in reproduction makes it difficult

to confirm these results.

The gonadal maturity stage data partially

corroborate the data on the standard length of the

host, showing higher abundances of D. pacupeva

and S. oxydoras in hosts with greater standard

length. Other studies have demonstrated that

increased reproductive effort may result in higher

prevalence and intensity of parasitism (e.g.

Gustafsson et al., 1994; Oppliger et al., 1996;

Sorci et al., 1996). Because both reproduction

(Reznick, 1985) and immune responses (Klasing

et al., 1991) are costly, reproduction may increase

susceptibility to parasites by reducing energy

available for immunological defense. Thus, adult

fishes (greater abundance of D. pacupeva and S.

oxydoras) that become reproductive reaching the

semi-spent stage showed the highest abundances

of these parasite species, while the immature

(small fishes) showed low abundances.

The authors thank Nupelia (Center for Research in

Limnology, Ichthyology and Aquaculture),

Maringá State University, for logistic and financial

support and the CNPq (Conselho Nacional de

ACKNOWLEDGEMENTS

252

Yamada et al.

Parasitism of Metynnis lippincottianus

Desenvolvimento Científico e Tecnológico) for its

support and research fellowship.

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Neotrop. Helminthol., 6(2), 2012

Author for correspondence / Autor para

correspondencia

Fábio Hideki Yamada

Laboratório de Ictioparasitologia/Nupelia,

Universidade Estadual de Maringá, Bloco G-90,

Av. Colombo, 5790, 87020-900, Maringá, Paraná,

Brasil.

E-mail /correo electrónico:

fhyamada@hotmail.com

Received, September 26, 2012.

Accepted, December 7, 2012.