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Parasitism in gills of Centropomus undecimalis (Pisces, Centropomidae) from a protected area in Sao Luis, Maranhao, Brazil.


Lesions in gills can be caused by chemical, physical and biological agents, ranging from environmental pollutants to various types of biological agents. These agents induce reactions of the body, such as circulatory disorders, proliferative, inflammatory and degenerative diseases, and congestion, telangiectasia, hemorrhages, and edemas, epithelial hyperplasia and mucous cells, inflammation and necrosis (Meyers & Hendricks, 1985; Roberts, 2001). Fish are susceptible to parasites, including various species groups which damage the gill tissue, such as Ichthyophthirius multifiliis, Trichodina sp., Chilodonella sp., Henneguya sp., Dolops sp., Lernaea cyprinacea, Monogeneans, Nematodes, and Ergasilidae (Schalch et al., 2006; Ueda et al., 2013). These parasites or symbionts are normally present in the environment or in the body of the fish, and when there is an imbalance in the environment-host-parasite relationship, outbreaks of disease occur (Martins et al., 2000, 2002). Fish diseases cause serious economic damage and often lead to high mortality rates. Monogenean parasites are notable etiological agents (Eiras et al., 2010). According to Adriano et al. (2005), these changes can partially impair the functions of the gills and consequently reduce respiratory capacity and ion exchange. Morphological parameters can be a useful tool for assessing the effects of environmental contamination on the quality of fish stocks. Among estuarine environment fish, the Centropomus undecimalis (Bloch, 1972) species is of great economic importance to the city of Sao Luis, Maranhao. It is commonly found in the Jansen Lagoon, a brackish water environment with a poor sewage infrastructure, and causes a reduction in the environmental quality of the lagoon, making the environment anoxic due to the high content of organic decaying matter, which has left the lagoon in a progressive state of eutrophication (Castro et al., 2002). In view of such impacts, the aim of the present study was to determine the frequency of parasitism and histological changes in the gills of C. undecimalis from the Jansen Lagoon Ecological Park in Sao Luis, Maranhao, Brazil.


Fish collection

Based on selection criteria of economic importance and significance as a bioindicator, the Centropomus undecimalis (Bloch, 1972) (Perciformes, Centropomidae) species, popularly known as snook fish, which is abundant in estuarine environments, was chosen. The specimens were collected by artisanal fishing techniques using cast nets from March to June 2012 in the Jansen Lagoon Ecological Park, which is characterized as a depression formed by brackish water. Located in a metropolitan area on the coast, it communicates with the sea through a channel and is considered as an almost salt water lake (Fig. 1). The fish were stored in sterilized plastic bags and immersed in ice until they were euthanized. Thirty-three specimens were collected.

Histopathological analysis

The first right branchial arch was removed from each animal, and fixed in 10% formalin for 24 h. These were subsequently decalcified in 10% nitric acid, dehydrated in increasing concentration of alcohols, clarified in xylene and impregnated with and embedded in paraffin. Five-[micro]m thick sections were stained with hematoxylin and eosin (Luna, 1968) for histological description and to determine parasite frequency. The parasites were identified to family level following the guidelines of Rohde (1993), Noga (1996) and Thatcher (2006).

Histological alterations were semi-quantitatively evaluated for each fish by calculating the histological alteration index (HAI), in accordance with Poleksic & Mitrovic-Tutundzic (1994), based on the severity of each lesion and classified in progressive stages of tissue damage using the formula HAI = 1 x [SIGMA] I + 10 x [SIGMA] II + 100 x [SIGMA] III, where I: stage I alterations, II: stage II alterations, III: stage III alterations (Table 1).


The gill arch and gill filament structures of C. undecimalis are the same as those from the gills of other teleost fishes (Fig. 2a). The fish caught were apathetic with excessive mucus production on the body surface and in the gills. Of the fish collected, 50% had parasitic alterations associated with alterations in the gill structure (Fig. 2b).

The main lesions observed were epithelial hyperplasia with interlayer space filling, congestion, and necrosis. In the C. undecimalis specimens, excess mucus was observed on the gills and Myxosporean cysts were located in the central part of the filament. Several monogeneans were scattered among the lamellae; in such cases, there was epithelial hyperplasia and mucus (Figs. 3-4).

The histological alterations observed in the gills and associated with the parasites were classified according to the degree of severity and impairment of gill function, and are shown in Table 2. The lifting of the lamellar epithelium was observed in all the gills analyzed (100%), followed by lamellar epithelium hyperplasia (96.9%), excessive proliferation of the filament epithelium cells causing complete fusion of various lamellae (82%) and vascular congestion (60%). The presence of parasites was observed in 50% of the collected fish. Hyperplasia of the mucous cells was also observed, as well as lamellar epithelium disruption, uncontrolled thickening of the proliferative tissue and aneurysms of various sizes in the lamellae.

The histopathological alteration index (HAI) per individual ranged from 3 to 138. The average HAI value obtained was 53.3, demonstrating that the gills of the individuals of the C. undecimalis species collected exhibited severe modifications in the tissue.


The microscopic tests identified the presence of parasites on the gills of C. undecimalis specimens of the Monogenean group (Van Beneden, 1858) Monopisthocotylea. According to Rohde (1993), Monopisthocotylea is considered a subclass of the Monogenean group, capable of parasitizing the gills of teleost fish and infecting a variety of microenvironments. It can move quickly, feed on epithelial cells and has a haptor that forms a single fixing unit. The parasites of the Monopisthocotylea class observed are part of the Ancyrocephalinae (Bychowsky, 1937), Capsalidae (Baird, 1853) and Dactylogyroidea (Bychowsky, 1933) families.

Fish with monogenean and other gill parasite infections exhibit epithelial hyperplasia and mucous cells in response to this aggression, with the latter resulting in increased mucus production. This acts as a defense element thanks to its antimicrobial properties, through the action of lysozymes, antibodies and low molecular weight fatty acids (Noga, 1996; Roberts, 2001). The increased mucus production, combined with cephalic gland secretions, causes a reduction in the respiratory capacity of the host (Thatcher & Brites-Neto, 1994).

These parasites can be found in all the fish organs, including the gills, causing serious structural damage (Takashima & Hibiya, 1995). Campos et al. (2011) found alterations caused by parasites in the gills of Piaractus mesopotamicus and Prochilodus lineatus from the Aquidauana River in the municipal region of Aquidauana, Mato Grosso do Sul. According to Moraes & Martins (2004), infections in fish caused by parasites occur due to the parasite-host-environment imbalance generally associated with a poor quality environment. Carvalho (2010) also observed infection in the gills of Geophagus brasiliensis acquired from the Guandu River and Trichiurus lepturus from Guanabara Bay, both in Rio de Janeiro, by parasites from the Dactylogyridae and Ancyrocephalinae families.

Given that the gill respiratory epithelium is in direct contact with the external environment and physiological stress-inducing factors, and has a large surface area, poor quality of water (Mallatt, 1985; Hinton & Lauren, 1990), irritating toxic agents, infectious agents and the presence of parasites (Pavanelli et al., 2004) lead to functional impairment of the filaments and gill lamellae.

The most frequent lesions found in the gills of C. undecimalis were the lifting of the lamellar epithelium, lamellar epithelium hyperplasia, and lamellar fusion. Gills fusion resulted from epithelial cell hyperplasia. The degree of fusion depends on the intensity and location of the hyperplasia. The fusion will be partial if the hyperplasia is restricted to the filament base or only the lamellae portion. However, if the hyperplasia is present throughout the filaments, the fusion will be total (Meletti et al, 2003). The lifting of the lamellar epithelium, the proliferation of filament epithelium and the fusion of the lamellae observed in large quantities in the gills of C. undecimalis function as a defense mechanism as they reduce the surface area of the gills and/or increase the diffusion barrier to pollutants (Erkmen & Kolankaya, 2000), impairing oxygen absorption.

Regarding the filament and lamellar proliferative tissue thickening, stage II alterations were more frequent and were present in 48.4% of the gills analyzed. Stage II alterations are more severe and impair gill function. When water quality improves these lesions can be repairable, but if the level of pollution increases, they can progress to the stage III (Poleksic & Mitrovic-Tutundzic, 1994).

The gill lamellae of the C. undecimalis collected also exhibited stage II vascular changes, with an overall parasitism rate of 39.3% and 70% of lamellae with aneurysms. Aneurysms generally result from the system collapse of the pillar cells, which impairs vascular integrity by releasing large amounts of blood, pushing the lamellar epithelium outward (Hinton & Lauren, 1990). They may be associated with chemical contaminants or parasitic lesions. Stage III alterations do not allow the restoration of the gill structure, even in cases of water quality improvement.

In fish with few parasites, basal and mucous cell hyperplasia is mild to moderate, whether associated or not with the congestive process. In severe infections, there is marked basal and mucous cell hyperplasia and increased mucus production, associated with circulatory disorders such as congestion, telangiectasia and interstitial hemorrhage (Schalch et al., 2006), signs similar to those observed in the present study.

By impairing blood flow and increasing the distance between the water and the blood, the lesions observed in the gill tissue impair the primary function of the gills, namely the gas exchange process, in addition to negatively influencing the maintenance of the acid-base balance and fish osmosis.

The results show that parasitism causes structural damage to the gill tissue. This damage can impair the physiology of the organ, and therefore harm the health of the fish. The data obtained in the present study serve as a warning to the riverine population, as C. undecimalis is sold locally.

DOI: 10.3856/vol46-issue2-fulltext-13


The authors would like to thank the Foundation for Research and Scientific and Technological Development of Maranhao (FAPEMA), for the opportunity to carry out this study, with the support of the Scientific Initiation Scholarship Program.


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Received: 16 January 2017; Accepted: 28 November 2017

Sildiane Martins Cantanhede (1), Vivian Cristina Sodre Campos (1), Dayane Pestana Pereira (1) Almerinda Macieira Medeiros (1), Raimunda Nonata Fortes Carvalho Neta (2) Ligia Tchaicka (3) & Debora Martins Silva Santos (1)

(1) Laboratorio de Morfofisiologia Animal, Departamento de Quimica e Biologia Universidade Estadual do Maranhao, Sao Luis, MA, Brazil

(2) Laboratorio de Biomarcadores e Organismos Aquaticos, Departamento de Quimica e Biologia Universidade Estadual do Maranhao, Sao Luis, MA, Brazil

(3) Laboratorio de Biodiversidade Molecular, Departamento de Quimica e Biologia Universidade Estadual do Maranhao, Sao Luis, MA, Brazil

Corresponding author: Sildiane Martins Cantanhede (

Corresponding editor: Enrique Dupre

Captions: Figure 1. Jansen Lagoon Ecological Park, Sao Luis, Maranhao, Brazil.

Captions: Figure 2. a) Normal gill filaments of C. undecimalis: 1. Secondary lamella, 2. Venous sinus, 3. Filament epithelium, b) monogenean parasite-arrow.

Captions: Figure 3. Gill filaments of C. undecimalis parasitized by monogeneans (a, b, c-stars), d) myxosporean cyst.

Captions: Figure 4. Histological changes in C. undecimalis gills. a) Arrow- aneurysm, b) 1-total fusion of secondary lamellae caused by hyperplasia of the epithelial cells, 2-aneurysm, c) 1-mucus cells; 2-uncontrolled thickening of the filament and lamellae, d) arrow-lifting of the lamellar epithelium; M: Myxosporidia.
Table 1. Categories of Histological Alteration Index
(HAI) values.

HAI      Lesion

0-10     Without alterations
11-20    Mild alterations
21-50    Moderate alterations
51-100   Severe alterations
>100     Irreversible alterations

Table 2. Classification of histological alterations of
Centropomus undecimalis gills collected from the Jansen Lagoon
Ecological Park, Sao Luis, Maranhao, Brazil. * Progressive
stages of tissue damages: I: mild to moderate alteration, II:
moderate to severe alteration, III: irreparable alteration.

Gill histological changes                             Stage *

Hyperplasia/hypertrophy of the lamellar epithelium
Lifting of the lamellar epithelium
Disorganization of lamellae
Incomplete fusion of several lamellae                    I
Complete fusion of several lamellae
Vascular congestion

Presence of parasites
Rupture of the lamellar epithelium
Hyperplasia and hypertrophy of mucous cells             II
Uncontrolled thickening of the filament
Lamellar proliferative tissue
Lamellar aneurysm                                       III
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Title Annotation:Research Article
Author:Cantanhede, Sildiane Martins; Campos, Vivian Cristina Sodre; Pereira, Dayane Pestana; Medeiros, Alme
Publication:Latin American Journal of Aquatic Research
Date:May 1, 2018
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