Neotrop. Helminthol., 8(1), 2014

2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

MICROHABITAT PREFERENCE AND SEASONALITY OF GILL MONOGENEANS IN

NILE TILAPIA REARED IN SOUTHERN BRAZIL

PREFERENCIA DE MICROHÁBITAT Y ESTACIONALIDAD DE MONOGENEOS

BRANQUIALES DE LA TILAPIA DEL NILO CULTIVADA EN EL SURESTE DE BRASIL

Mauricio Laterça Martins, Ana Rosa Santana de Sá,

Gabriela Tomas Jerônimo, Karen Roberta Tancredo, Eduardo Luis Tavares Gonçalves,

Daniela Bampi, Giselle Mari Speck & Alexandre Mattos Sandin

Abstract

Few studies have been done to evaluate the monogenean microhabitat preference. This study

evaluated the monogenean distribution among different gill arches of Nile tilapia Oreochromis

niloticus and seasonality. A total of 89 fish were captured in a pond located in Chapecó, Santa

Catarina, for parasitological analysis. After fish euthanasia, the gill arches were removed,

separated from the most external to the most internal and named as I, II, III and IV. Transparency,

pH, oxygen, temperature, alkalinity, conductivity, ammonia, iron, orthophosphate, sulfide, nitrite

and nitrate of water pond were measured. In spring 2008 the mean abundances of the

monogeneans (Scutogyrus longicornis, Cychlidogyrus sclerosus, C. thurstonae and C. tilapiae) in

the arches I, II, III and IV were, respectively, 11.45, 14.45, 13.8, 13.15, in summer 2008 theywere

13.12, 12.25, 14.94, 21.53, in summer 2009 they were 2.75, 3.25, 2.45, 2.45, in autumn 2009 they

were 13.44, 18.78, 11.78, 9.22 and in winter 2009 they were 0.35, 0.5, 0.3, 0.5. Monogenean

preference for microhabitat in the gills of farmed Nile Tilapia was not observed. A significant

increase of parasites in spring and summer 2008 and autumn 2009 was observed. The highest

number of parasites coincided with seasons of high water temperature. The lack of microhabitat

preference among the gill arches suggest homogenous distribution of parasites combined with

water quality parameters.

Keywords: Oreochromis – monogenean parasites - gills - season.

Suggested citation: Martins, ML, Sá, ARS, Jerônimo, GT, Tancredo, KR, Gonçalves, ELT, Bampi, D, Speck, GM & Sandin, AM.

2014. Microhabitat preference and seasonality of gill monogenean in Nile Tilapia reared in southern Brazil. Neotropical

Helminthology, vol. 8, n°1, jan-jun, pp. 47 - 58.

AQUOS - Aquatic Organisms Health Laboratory, Aquaculture Department, CCA, Federal University of Santa Catarina (UFSC), Rod. Admar Gonzaga 1346,

88040-900, Florianópolis, SC, Brasil.

E-mail: mauricio.martins@ufsc.br, anarosa.sa@gmail.com, gabrielatj@gmail.com, roberta.tancredo@gmail.com, eltgoncalves@gmail.com,

danielabampi@hotmail.com, giselle_speck@yahoo.com.br, alexandre_sandin@hotmail.com

Martins et al.

Microhabitat preference and seasonality of gill monogenean

Resumen

Palabras clave: branquias - estacion Oreochromis - parásitos.

Pocos estudios han sido hechos para evaluar la preferencia por el microhabitat de monogenea.

Este estudio evaluó la distribución y estacionalidad de monogenea entre los diferentes arcos

branquiales de tilapia del Nilo. Un total de 89 peces fueron capturados en una laguna en la ciudad

de Chapecó, Santa Catarina, para el análisis parasitológico. Después de la eutanasia de los peces,

fueron extraídos los arcos branquiales separadamente a partir de la región externa hasta la interna

y numerados como I, II, III e IV. Fueron evaluadas la transparencia del agua, el pH, el oxigeno

disuelto, la temperatura, la alcalinidad, la conductividad, el amonio, el hierro, el ortofosfato, el

sulfato, el nitrito y el nitrato. En la primavera de 2008 las abundancias promedio de monogenea

(Scutogyrus longicornis, Cychlidogyrus sclerosus, C. thurstonae y C. tilapiae) en los arcos I, II,

III y IV fueron, respectivamente, 11,45; 14,45; 13,8; 13,15; en el verano de 2008 de 13,12; 12,25;

14,94; 21,53; en el verano de 2009 de 2,75; 3,25; 2,45; 2,45; en el otoño de 2009 de 13,44; 18,78;

11,78; 9,22 y en el invierno de 2009 de 0,35; 0,5; 0,3; 0,5. No fue observada preferencia por

monogenea por el microhabitat en las branquias de la tilapia del Nilo en cultivo. Fue observado un

aumento significativo de los helmintos en la primavera y verano de 2008 y otoño de 2009. El

mayor número de parásitos coincidió con las estaciones de mayor temperatura del agua. La falta

de preferencia por microhabitat entre los arcos branquiales sugiere una distribución homogénea

de los parásitos combinados con los parámetros de calidad de agua.

culminates in disease outbreaks (Bergh, 2007).

Few studies relate the microhabitat preference of

fish parasites (Hanek & Fernando, 1978;

Buchmann, 1989; Oliva & Luque, 1998; Dzika,

1999; Ramasamy et al., 1985; Koskivaara et al.,

1992; Rubio-Godoy, 2008; Iannacone &

Alvariño, 2012).

In Brazil, few studies regarding the gill

microhabitat preference of parasites in farmed

fish are found. Jerônimo et al. (2013) have

reported higher mean intensity of the

monogeneans Mymarothecium viatorum

Boeger, Piasecki & Sobecka, 2002 and

Anacanthorus penilabiatus Boeger, Husak &

Martins, 1995 in the gill arch I than in the arch IV

of pacu (Piaractus mesopotamicus Holmberg,

1887) native farmed fish.

On this view, the aim of this work was to

evaluate the monogenean preference for gill

microhabitat in Nile tilapia, Oreochromis

niloticus Linnaeus 1758 (Cichlidae) reared in

ponds in Southern Brazil and its occurrence in

each season of the year.

Monogenean helminthes are among the major

parasites on Nile tilapia, even though in Brazil

there are few cases of mass mortalities caused by

high parasite number. They are responsible for

significant economical losses, especially when

present with both bacterial and parasitic

concurrent infections (Xu et al., 2007). Its

reproduction is favored by water quality,

stocking density and temperature (Moraes &

Martins, 2004). The parasite may inhabit and

live well adapted to the host with no mortality

outbreaks. On the other hand, if fish are exposed

to stressful conditions, disease can occur

(Buchmann & Bresciani, 1997).

According to Overstreet (1997), parasitological

data may act as indicator of fish welfare and

environmental health. Jerônimo et al. (2011)

have demonstrated the importance of fish

assessment in the different production systems.

They argued that water quality might influence

the number and diversity of fish ectoparasites.

Aquaculture improves the possibility of fish

parasite dissemination and sometimes it

INTRODUCTION

between seasons, monogenean counting data

were transformed to x and submitted to

factorial analysis of variance (ANOVA).

Principal components analysis was also used as

an exploratory technique to assess relation

between seasons and every measured parameter.

All analysis were performed using StatSoft's

Statistica 7.0 software, using Bartlett's test to

verify homogeneity of variances and Tukey`s

test used for mean comparison.

The means and standard deviation of weight (g)

and total length (cm) were as follows: spring

2008 (357.5+97.4 and 27.2+2.3), summer 2008

(520.7+72.7 and 30.3+1.6), summer 2009

(110.1+32 and 20.6+1.8), autumn 2009

(152.2+95.3 and 22.1+3.5) and winter 2009

(251.6+51.2 and 23.8+1.8).

Almost all water quality parameters were

constant during the whole collection period

(Figure 1). As expected, the highest water

temperature was found in summer and depletion

of dissolved oxygen occurred in autumn. Water

transparency was between 20 and 30 cm as

measured with Secchi disc.

The monogenean helminthes were identified as

Scutogyrus longicornis Paperna et Thurston

1969, Cichlidogyrus sclerosus Paperna et

Thurston 1969, Cichlidogyrus thurstonae

Ergens 1981 and Cichlidogyrus tilapiae Paperna

1960.

Prevalence rate of parasitism of all monogenean

was high in all seasons, except in winter 2009

(Table 1). ANOVA data comparison showed no

difference (P>0.05) in monogenean intensity

between gill arches (Figure 2), despite of season,

indicating there was no microhabitat preference

in the current study. When gill arches were

compared among seasons (Figure 3),

significantly higher numbers of helminthes were

found in spring 2008, summer 2008 and autumn

2009. Factorial ANOVA showed no significant

interaction between seasons and gill arches

preference (Figure 4).

From spring 2008 to winter 2009, a total of 89

Nile tilapia were captured with nets in a fish

pond located in Chapecó in the State of Santa

Catarina, Southern Brazil (27° 5' 48” S and 52°

37' 7” W) for parasitological diagnosis. Fish

were kept in 2000 m earthen ponds at a stocking

density of 2 to 3 fish/m and fed twice a day with

commercial diet. In each season 20 fish were

examined, except in autumn 2009 when only 9

animals were captured. Parasitological analysis

was made in situ and fixed material was stored

and transported to the laboratory. In the

sampling day pH (Alfakit phmeter),

transparency (Secchi disc), dissolved oxygen

(Alfakit oxymeter at-150), water temperature,

electrical conductivity (PHTEK CD203),

alkalinity, ammonia, iron, ortophosphate,

sulfide, nitrite and nitrate (measured with

colorimetric kit Alfakit) of pond water were

measured in the morning and afternoon.

After anesthetizes in a benzocaine solution (75

-1

mg·L ) and euthanasia (Ethic Committee

number 23080.019034/2008-98/CEUA/UFSC),

smears of the gill filaments were examined

under microscope between a glass slide and a

cover slip (Jerônimo et al., 2011). Gill arches

were carefully separated from the most external

to the most internal, named as I, II, III and IV,

embedded into 60 C hot water to relax parasites

and fixed in 5% formalin solution for further

quantification in the laboratory using marked

Petri dishes. The parasites were mounted using

the Hoyer's method for identification through

the esclerotized parts of the parasites (Kritsky et

al., 1995; Eiras, 1994) and identified according

to Paperna & Thurston (1969), Ergens (1981),

Douëllou (1993), Pariselle & Euzet (1995) and

Pariselle et al. (2003). The monogeneans are

deposited in the Laboratory AQUOS, Santa

Catarina, Brazil collection under the numbers

ARS 1-5. The data of prevalence, mean intensity

and mean abundance for all monogenean joined

were calculated as suggested by Bush et al.

(1997).

In order to evaluate microhabitat preference

among gill arches and differences in parasitism

MATERIAL AND METHODS

Neotrop. Helminthol., 8(1), 2014

RESULTS

Martins et al.

Microhabitat preference and seasonality of gill monogenean

relation between sulfide and nitrite, opposed to

water temperature and monogenean as well as

relation between transparency and dissolved

oxygen, opposed to conductivity. All toxic

components, ammonia, nitrite, nitrate and

sulfide, grouped in the same region of axis.

Regarding seasons, summer 2008 and spring

2008 were more related with monogenean and

water temperature, while summer 2009 was

related to toxic components and autumn 2009 to

transparency and dissolved oxygen.

Both prevalence and number of parasites were

lower (P<0.05) in winter than that observed in

the other seasons (Figure 3). Despite the high

prevalence rate in summer 2009 (89%) mean

intensity and mean abundance showed low

values (3.1 and 2.7, respectively).

In the principal components analysis (Figure 5 a-

b), the score and loading plots summarizes data

influence over two factors, also called principal

components (PC), which represent 71.81% of

variance among samples. It shows a strong

Water Temperature (

Transparency (cm)

Ammonia (mg/L)

Nitrite (mg/L)

Nitrate (mg/L)

Dissolved oxygen (mg/L)

Sulfide (mg/L)

Conductivity (µS/cm)

Orthophosphate (mg/L)

Iron (mg/L)

Spring 2008

20.15

6.63

0.1

0.05

3.985

0.75

Summer 2008

26.9

7.375

8.665

Summer 2009

19.05

8.45

22.5

1.025

0.03

0.85

0.025

0.75

0.25

Autumn 2009

20.45

7.2

27.5

0.45

0.03

0.4

0.025

0.75

0.9

Winter 2009

12. 6

6.965

22.5

0.1

0.005

1 .035

10.655

0.0125

1 .25

0.5

Figure 1. Water quality parameters from the pond in Chapecó, Santa Catarina State, Southern Brazil.

Table 1. Parasitological indexes of Oreochromis niloticus cultured in Chapecó. Santa Catarina State. Southern

Brazil, along the seasons and in each gill arch. IG: infected gills, EG: examined gills, IF: infected fish, EF: examined

fish.

Seasons IG/EG P (%) Mean Intensity Mean Abundance

Spring 2008 80/80 100 13.2+11.2 13.2+11.2

Summer 2008 79/80 98 15.5+10.0 15.7+9.9

Summer 2009 71/80 89 3.1+1.8 2.7+1.9

Autumn 2009 35/36 97 13.7+9.6 13.3+9.7

Winter 2009 24/80 30 1.4+0.6 0.4+0.7

Gill arches IF/EF P (%) Mean Intensity Mean Abundance

Arch 1 71/89 80 9.8+8.3 7.8+8.4

Arch 2 74/89 83 10.5+10.3 8.7+10.1

Arch 3 69/89 77 10.7+8.9 8.2+9.0

Arch 4 75/89 84 10.9+12.8 9.2+12.4

Neotrop. Helminthol., 8(1), 2014

Figure 2. ANOVA comparison of transformed ( x ) Monogenean count data between gill arches of Oreochromis niloticus

cultured in Chapecó, Santa Catarina State, Southern Brazil.

Figure 3. ANOVA comparison of transformed ( x ) Monogenoidea count data between seasons in Chapecó, Santa Catarina

State, Southern Brazil.

Martins et al.

Microhabitat preference and seasonality of gill monogenean

Figure 4. Factorial ANOVA comparison of transformed ( x ) Monogenean count data between seasons and gill arches of

Oreochromis niloticus cultured in Chapecó, Santa Catarina State, Southern Brazil.

Water temperature, which presents an important

role in fish development by influencing directly

its metabolic rates and also, several times,

influencing parasite reproduction (Moraes &

Martins, 2004), was a strong component related

to monogenean, especially for 2008`s summer

and spring.

Water quality parameters were kept within

tolerance levels for fish maintenance (Sipaúba-

Tavares, 1998). According to Pereira &

Mercante (2005) ammonia may cause damage in

fish production system and its levels depends of

the amount fish, feeding rate, diet quality and

temperature. In summer 2008 and especially in

summer 2009 higher levels of ammonia were

observed due to enhanced fish metabolism and

increase of feeding related to higher water

temperatures. Despite the low levels of oxygen

in autumn 2009 and high ammonia

concentration in summer 2008 and 2009 no

abnormal fish behavior was observed. It could

be explained due to lower water temperature in

Southern Brazil when compared to Southeastern

region (Tavares-Dias et al., 2008).

Parasitological analysis showed highest

prevalence rates in spring and summer and the

lowest in winter, results that confirmed the

observations of Koskivaara et al. (1992) who

found greater abundance of Dactylogyrus

Diesing, 1850 in the gills of roach in spring and

summer. As demonstrated in this study and

compared to other Brazilian regions, water

temperature has a strong influence on the

parasite settlement (Buchmann & Bresciani,

1997). Garcia et al. (2003) related negative

correlation between temperature and

Urocleidoides sp. (Mizelle & Price, 1964)

Kritsky, Thatcher & Boeger, 1986 in sword tail

DISCUSSION

Spring 2008

Summer 2008

Summer 2009

Autumn 2009

Winter 2009

Neotrop. Helminthol., 8(1), 2014

Figure 5. Principal component analysis (PCA) of water quality parameters and Monogenean count data obtained from a fish pond

located in Chapecó, Santa Catarina State, Southern Brazil. DO = dissolved oxygen; TR = transparency; WT = water temperature;

CT = electrical conductivity; AK = alkalinity; AM = ammonia; IR = iron; OP = orthophosphate; SF = sulphide; NI = nitrite; NA =

nitrate; MO = Monogenoidea.

Martins et al.

Microhabitat preference and seasonality of gill monogenean

and platy fish (Xiphophorus hellerii Heckel,

1848 and X. maculatus Gunther, 1866). It must

be added that not only the water temperature, but

also other factors like oxygen concentration

(Molnar, 1994) and handling management

(Jerônimo et al., 2011) are responsible for

modulating the parasite life cycle.

Seasonal occurrence of monogenean helminthes

was mostly studied in reservoirs (Rawson &

Rogers, 1973; Ranzani-Paiva et al., 2005) and

lakes (Ozturk & Altunel, 2006). The population

of Gyrodactylus macrochiri Hoffman et Putz,

1964 on largemouth bass (Micropterus

salmoides Lacepède, 1802) increased as the

water temperature reached 28 C (Rawson &

Rogers, 1973). Except for autumn 2009 our

results are in agreement with Koskivaara et al.

(1992). The authors also observed high mean

abundance of Dactylogyrus species in spring

and summer.

The present results are supported by these

authors where the highest mean intensity and

abundance were found in spring and summer.

Similarly to Ozturk & Altunel (2006) in autumn

2009 the majority of fish (97%) were infected

and in consequence the mean intensity and

abundance were statistically similar to spring

and summer.

The water temperature has an important

influence on the parasite abundance and egg

production in monogenean life cycle (Tinsley &

Jackson, 2002). The low infection observed in

summer 2009 might be related not only to the

water temperature (similar to autumn) but also

other environmental factors, like toxic

components as ammonia.

The seasonal variation of monogenean

infections in intensive fish farming is poorly

known, especially in Brazil. Flores-Crespo et al.

(1992) observed high infection by Dactylogyrus

sp. in reared tilapia. Later, Ranzani-Paiva et al.

(2005) confirmed high mean intensity of

monogenean in spring, peaking in summer.

Although the highest prevalence rates observed

in this study, the abundance of Cichlidogyrus

species was similar to that found by Lizama et al.

(2007). Kadlec et al. (2003) found Dactylogyrus

carpathicus Zachvatkin, 1951 as the most

abundant parasite in the gills of barbel (Barbus

barbus Linnaeus, 1758) in August. Contrarily,

Dactylogyrus malleus Linstow, 1877 showed

significant higher abundance in April. It's

necessary to remember that Kadlec et al. (2003)

obtained their results from the Danube River. In

a fish pond system, where stocking density and

feeding conditions are relatively stable, the

parasite abundance may not be affected, as here

demonstrated.

In terms of microhabitat, 68 to 73% of

Diclidophora merlangi Nordmann, 1832 found

on whiting (Gadus merlangus Linnaeus, 1758)

from the Irish Sea were in the first gill arch

(Arme & Halton, 1972). These authors

explained that in a single infection the majority

of worms could be located on the arch I, but in

multiple infections the parasites would be found

on the other arches. In part, this comment could

be applied to our research in which the

community of parasites was composed by

infrapopulations. Buchmann (1989) has

demonstrated preference of P. bini for arches I

and II and P. anguillae preference for arches III

and IV in European eel (Anguilla anguilla

Linnaeus, 1758). Although, in this study,

parasite species were not analyzed separately,

the results suggest that monogenean

infrapopulation in tilapia reared in ponds may

not vary among gill arches.

In the studies of Ramasamy et al. (1985)

parasites Scomberoides species from the Bay of

Bengal, India. Polyopisthocotyleans Vallisia

indica Unnithan, 1962 showed preference for

arch I, but, when low parasite intensities were

observed, they were also found on arches II and

III. In the present work, parasite intensity can be

considered lower than those normally observed

in cultured fish (Tavares-Dias et al., 2001),

supporting the hypothesis of Ramasamy et al.

(1985).

El Hafidi et al. (1998) reported the preference of

microhabitat in two species of Monogenea,

Metamicrocotyla cephalus Azim 1939 and

Neotrop. Helminthol., 8(1), 2014

Microcotyle mugilis Vogt, 1878 in the gills of

Mugil cephalus Linnaeus, 1758. They found that

when two species coexist, the intensity of

infection is higher than that in monospecific

infection. Both species showed preference for

gill arch I. It's normally reported that two species

coexisting may cause more damage on the host

than monospecific infections (Koskivaara et al.,

1992, Moraes & Martins, 2004). On the other

hand, the second arch was the most preferred

location by Pseudodactylogyrus in eel

(Matejusová et al., 2003). According to Kadlec

et al. (2003) the preference for microhabitat

within gills is modulated by the parasite

abundance. They found that the overlap between

species increased in cases of greatest

abundances. This could also be explaining the

lack of difference among the gill arches in the

present study.

The preference for the middle arches may be

related, among other factors, to greater surface

area (Ramasamy et al., 1985). According to

Geets et al. (1997) Pseudohaliotrema Yamaguti,

1952 was more abundant in the first two arches

of rabbit fish (Siganus sutor Valenciennes, 1835)

while Microcotyle mouwoi Ishii et Sawada, 1938

did not show preference for gill arch. Even

though, other factors are involved in the parasite

distribution on the gills such as health status,

parasite density and diversity. Another point that

must be emphasized is the distinct environment

where fish were captured.

The studies of Rubio-Godoy & Tinsley (2002)

showed that the parasites migrate from the site of

initial attachment to the most favorable place on

the gill arches. In contrast, this study did not

show any difference among the gill arches.

Possibly this could be related to low parasite

abundance when compared to those observed by

Rubio-Godoy (2008) and even to parasite

species.

This study suggests that parasitic fauna in

cultured tilapia may not vary considerably in

low water temperature. On the other hand, the

pond management such as feeding rate, water

flow, fish stocking density and the presence or

not of swine manure has a strong influence on

the parasitic life cycle. Further studies must be

carried out in other Brazilian fish farming

facilities to verify the parasite population in each

gill arch, which varies in morphology according

to fish species. Moreover, not only studies with

the Brazilian wild fishes must be encouraged to

improve the knowledge of the host parasite

environment system but also experimental trials

with different parasite density in controlled

conditions.

The authors thank CNPq (National Council for

Scientific and Technological Development for

financial support (CNPq/MAPA/SDA

577657/2008-9) and grant to the first author

(CNPq 301072/2008-7), and EMBRAPA –

Macroprograma 1 – AQUABRASIL.

ACKNOWLEDGEMENTS

BIBLIOGRAPHIC REFERENCES

Arme, C & Halton, DW. 1972. Observations on

the occurrence of Diclidophora merlangi

(Trematoda: Monogenea) on the gills of

whiting, Gadus merlangus. Journal of Fish

Biology, vol. 4, pp. 27-32.

Bergh, O. 2007. The dual myths of the healthy

wild fish and the unhealthy farmed fish.

Diseases of Aquatic Organisms, vol. 75,

pp. 159-164.

Buchmann, K. 1989. Microhabitats of

monogenean gill parasites on European

e e l ( A ngu ill a an gui lla ) . F oli a

Parasitologica, vol. 36, pp. 321-329.

Buchmann, K & Bresciani, J. 1997. Parasitic

infections in pond-reared rainbow trout

Oncorhynchus mykiss in Denmark.

Diseases of Aquatic Organisms, vol. 28,

pp. 125-138.

Bush, AO, Lafferty, KD, Lotz, JM & Shostak, W.

1997. Parasitology meets ecology on its

own terms: Margolis et al. revisited.

Journal of Parasitology, vol. 83, pp. 575-

583.

Douëllou, L. 1993. Monogeneans of the genus

C i c h l i d o g y r u s P a p e r n a , 1 9 6 0

(Dactylogyridae: Ancyrocephalinae)

Martins et al.

Microhabitat preference and seasonality of gill monogenean

from cichlid fishes of Lake Kariba

(Zimbabwe) with descriptions of five new

species. Systematic Parasitology, vol. 25,

pp. 159-186.

D zi ka , E . 1 9 99 . M i c ro h a b i t a t s o f

Pseudodactylogyrus anguillae and P. bini

(Monogenea: Dactylogyridae) on the gills

of large-size European eel Anguilla

anguilla from Lake Gaj, Poland. Folia

Parasitologica, vol. 46, pp. 33-36.

E i r a s , J . C . 1 9 9 4 . E l e m e n t o s d e

ictioparasitologia. 1ª ed. Porto: Fundação

Eng. Antônio de Almeida, 339p.

El Hafidi, F, Berrada-Rkhami, O, Benazzou, T &

Gabrion, C. 1998. Microhabitat

di st ri bution and coexistence o f

Microcotylidae (Monogenea) on the gills

of the striped mullet Mugil cephalus:

chance or competition? Parasitology

Research, vol. 84, pp. 315-320.

Ergens, R. 1981. Nine species of the genus

C i c h l i d o g y r u s P a p e r n a , 1 9 6 0

(Monogenea: Ancyrocephalinae) from

Egyptian fishes. Folia Parasitologica, vol.

28, pp. 205-214.

Flores-Crespo, J. Velarde, FI. Flores-Crespo, R

& Vazquez-Pelaez, C.G. 1992. Variación

estacional de Dactylogyrus sp. em dos

unidades productoras de tilapia del

Estado de Morelos. Técnica Pecuaria en

México, vol. 30, pp. 109-118.

Garcia, F, Fujimoto, RY, Martins, ML & Moraes,

FR. 2003. Parasitismo de Xiphophorus

spp. por Urocleidoides sp. e sua relação

com os parâmetros hídricos. Boletim do

Instituto de Pesca, vol. 29, pp. 123-131.

Geets, A, Coene, H & Ollevier, F. 1997.

Ectoparasites of the whitespotted

rabbitfish, Siganus sutor (Valenciennes,

1835) off the Kenyan Coast: distribution

within the host and site selection on the

gills. Parasitology, vol. 115, pp. 69-79.

Hanek, G & Fernando, CH. 1978. Spatial

distribution of gill parasites of Lepomis

gibbosus (L.) and Ambloplites rupestris

(Raf.). Canadian Journal of Zoology, vol.

56, pp. 1235-1240.

Iannacone, J & Alvariño, L. 2012. Microecology

of the monogenean Mexicana sp. on the

gills of Anisotremus scapularis (Tschudi,

1846) (Osteichthyes, Haemulidae) of the

marine coast of Lima, Peru. Neotropical

Helminthology, vol. 6, pp. 277-285.

Jerônimo, GT, Speck, GM, Cechinel, MM,

Gonçalves, ELT & Martins, ML. 2011.

Seasonal variation on the ectoparasitic

communities of Nile tilapia cultured in

three regions in Southern Brazil. Brazilian

Journal of Biology, vol. 71, pp. 1-9.

Jerônimo, GT, Gonçalves, ELT, Bampi, D,

Paseto, A, Pádua, SB, Ishikawa, MM &

Martins, ML. 2013. Microhabitat of

monogenea and copepodids of Lernaea

cyprinacea on the gills of four Brazilian

f r e s h w a t e r f i s h . N e o t r o p i c a l

Helminthology, vol. 7, pp. 65-74.

Kadlec, D, Simková, A, & Gelnar, M. 2003. The

microhabitat distribution of two

Dactylogyrus species parasitizing the

gills of the barbell, Barbus barbus. Journal

of Helminthology, vol. 77, pp. 317-325.

Koskivaara, M, Valtonem, ET & Vuori, KM.

1992. Microhabitat distribution and

coexistence of Dactylogyrus species

(Monogenea) on the gills of roach.

Parasitology, vol. 104, pp. 273-281.

Kritsky, DC, Boeger, WA & Popazoglo, F. 1995.

Neotropical Monogenoidea. 22. Variation

in Scleroductus species (Gyrodactylidea,

Gyrodactylidae) from siluriform fishes of

so ut he astern Br az il . Journal of

Helminthology, vol. 62, pp. 53-65.

Lizama, M De Los AP, Takemoto, RM, Ranzani-

Paiva, MJT, Ayroza, LMS & Pavanelli,

GC. 2007. Relação parasito-hospedeiro

em peixes de pisciculturas da região de

Assis, Estado de São Paulo, Brasil. 1.

Oreochromis niloticus (Linnaeus, 1757).

Acta Scientiarum Biological Sciences,

vol. 29, pp. 223-231.

Matejusová, I, Simková, A, Sasal, P & Gelnar,

M. 2003. Microhabitat distribution of

Pseudodactylogyrus anguillae and

Pseudodactylogyrus bini among and

within gill arches of the European eel

(Anguilla anguilla L.). Parasitology

Research, vol. 89, pp. 290-296.

Molnár, K. 1994. Effect of decreased water

oxygen content on common carp fry with

Dactylogyrus vastator (Monogenea)

Neotrop. Helminthol., 8(1), 2014

infection of varying severity. Diseases of

Aquatic Organisms, vol. 20, pp. 153-157.

Moraes, FR & Martins, ML. 2004. Condições

predisponentes e principais enfermidades

de teleósteos em piscicultura intensiva.

In: Cyrino, JEP, Urbinati, EC, Fracalossi,

DM & Castagnolli, N. Tópicos especiais

em piscicultura de água doce tropical

intensiva. São Paulo: TecArt, pp. 343-

383.

Oliva, ME & Luque, JL. 1998. Distribution

patterns of Microcotyle nemadactylus

(Monogenea) on gill filaments of

Cheilodactylus variegatus (Teleostei).

Memórias do Instituto Oswaldo Cruz, vol.

93, pp. 477-478.

Overstreet, RM. 1997. Parasitological data as

monitors of environmental health.

Parassitologia, vol. 39, pp. 169-175.

Öztürk, MO & Altunel, FN. 2006. Occurrence

of Dactylogyrus infection linked to

seasonal changes and host fish size on

four cyprinid fishes in Lake Manyas,

Turkey. Acta Zoologica Academiae

Scientiarum Hungaricae, vol. 52,

pp.407-415.

Paperna, I. & Thurston, J.P. 1969. Monogenetic

trematodes collected from cichlid fish in

Uganda; including the description of five

new species of Cichlidogyrus. Revue de

Zoologie et de Botanique Africaines, vol.

79, pp. 1-2.

Pariselle, A & Euzet, L. 1995. Gill parasites of

the genus Cichlidogyrus Paperna, 1960

(Monogenea, Ancyrocephalidae) from

Tilapia guineensis (Bleeker, 1862), with

descriptions of six new species.

Systematic Parasitology, vol. 30, pp. 187-

198.

Pariselle, A, Bilong, C & Euzet, L. 2003. Four

new species of Cichlidogyrus Paperna,

1960 (Monogenea, Ancyrocephalidae),

al l g il l parasites from Af ri ca n

mouthbreeder tilapias of the genera

Sarotherodon and Oreochromis (Pisces,

Cichlidae), with a redescription of C.

thurstonae Ergens, 1981. Systematic

Parasitology, vol. 56, pp. 201-210.

Pereira, LPF & Mercante, CTJ. 2005. Ammonia

in fish breeding systems and its effects on

the water quality-a review. Boletim do

Instituto de Pesca, vol. 31, pp. 81-88.

Ramasamy, P, Ramalingam, K, Hanna, EB &

Halton, DW. 1985. Microhabitats of gill

parasites (Monogenea and Copepoda) of

tel eos ts ( Scomberomorus s pp. ).

International Journal for Parasitology,

vol. 15, pp. 385-397.

Ranzani-Paiva, MJT, Felizardo, NN & Luque,

JL. 200 5 . P a r a s i t o l o g i cal a n d

hematological analysis of Nile tilapia

Oreochromis niloticus Linnaeus, 1757

from Guarapiranga reservoir, São Paulo

State, Brazil. Acta Scientiarum Biological

Sciences, vol. 27, pp. 231-237.

Rawson, MV & Rogers, WA. 1973. Seasonal

abundance of Gyrodactylus macrochiri

Hoffman and Putz, 1964 on bluegill and

largemouth bass. Journal of Wildlife

Diseases, vol. 9, pp. 174-177.

Rubio-Godoy, M. 2008. Microhabitat selection

of Discocotyle sagittata (Monogenea:

Polyopisthocotylea) in farmed rainbow

trout. Folia Parasitologica, vol. 55, pp.

270-276.

Rubio-Godoy, M. & Tinsley, R.C. 2002. Trickle

and single infection with Discocotyle

s a g i t t a t a ( M o n o g e n e a :

Polyopisthocotylea): effect of exposure

mode on parasite abundance and

development. Folia Parasitologica, vol.

49, pp. 269-278.

Sipaúba-Tavares, LH. 1998. Limnologia dos

sistemas de cultivo. In: Carcinicultura de

água doce. São Paulo. FUNEP, pp. 47-75.

Tavares-Dias, M, Moraes, FR & Martins, ML.

2008. Hematological assessment in four

Brazilian teleost fish with parasitic

infections, collected in feefishing from

Franca, São Paulo, Brazil. Boletim do

Instituto de Pesca, vol. 34, pp. 189-196.

Tavares-Dias, M, Moraes, FR, Martins, ML &

Kronka, SN. 2001. Fauna parasitária de

peixes oriundos de “pesque-pague” do

município de Franca, São Paulo, Brasil.

II. Metazoários. Revista Brasileira de

Zoologia, vol. 18, pp. 81-95.

Tinsley, RC & Jackson, JA. 2002. Host factors

limiting monogenean infections: a case

study. International Journal for

Martins et al.

Microhabitat preference and seasonality of gill monogenean

Received December 17, 2013.

Accepted January 19, 2014.

Parasitology, vol. 32, pp. 353-365.

Xu, DH, Shoemaker, CA & Klesius, PH. 2007.

Evaluation of the link between

gyrodactylosis and streptococcosis of Nile

tilapia, Oreochromis niloticus (L.).

Journal of Fish Diseases, v. 30, p. 233-

238.