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A study based on monthly sampling of catches in Anambra river system (Otuocha station) was carried out between May 2013 and April 2014 to investigate the parasitofauna of wild clariid catfishes with reference to their prevalence, mean intensity and abundance; and also to ascertain the impact of these parasites on the physiology of its fish hosts. A total of 360 fish hosts, comprising of Clarias gariepinus (231) and Clarias anguilaris (129)were examined for parasites. Blood samples were collected from the caudal peduncle for haematological and biochemical enzymes assay using standard procedures. Six parasite species including two protozoans (Trichodina acuta and Epistylis sp.), two cestodes (Polyonchobothrium clarias and Monobothroides woodlandi) and two nematodes (Procamallanus laeviconchus and Rhabdocona congolensis) were recovered. The overall parasite prevalence is 41.1%, with protozoan parasites having the highest prevalence (25.5%), cestode (15.0%). Whereas nematode has the least parasite prevalent, infecting only 4.72% of the fish hosts. The relatively high overall parasite prevalence may be attributed to the relatively high level of domestic effluent into the river. Analysis of prevalence of parasitic infection of fish species by body weight and total length showed that parasite loads increased with increase in body weight and total length fish hosts. The study revealed that male fishes accumulate more parasites (P<0.05) than the female fishes. Monthly/seasonal patterns of parasite occurrence varied from one parasite to another. Whereas some parasites were found throughout the year, others were highly pronounced either in the rainy season or in the dry months. The influence of parasite prevalence on the condition factor (K) and hepatosomatic index (HSI) were highly significant (P<0.05). Whereas, condition factor showed negative correlations with increase in parasite intensity, HSI showed positive correlation with increase in parasite intensity. The study recorded a significant decrease in the mean values of red blood cell count (RBC), Haemoglobin concentration (Hb) and packed cell volume (PCV) (P<0.05) and significant increase in the mean values of white blood count (WBC) of the infected fishes when compared to the uninfected ones (P<0.05). Moreso, significant increase were observed in the mean values of aspartate transaminase (AST), alanine transaminase (ALT), alkaline phosphatase (ALP), urea and creatinine of the infected fishes when compared to the uninfected fishes (P<0.05). The haematological and biochemical alterations observed in the infected fishes reflect anemia and tissue damages caused by parasites invasion.




TITLE                                                                                                                                  PAGES

Title page        –           –           –           –           –           –           –           –           –           –           –    i

Dedication      –           –           –           –           –           –           –           –           –           –           –   ii

Certification    –           –           –           –           –           –           –           –           –           –           –   iii

Acknowledgements    –           –           –           –           –           –           –           –           –           –   iv

Table of contents        –           –           –           –           –           –           –           –           –           –   v

List of figures –           –           –           –           –           –           –           –           –           –           –   viii

List of tables   –           –           –           –           –           –           –           –           –           –           –   ix

List of plates   –           –           –           –           –           –           –           –           –           –           –   x

Abstract          –           –           –           –           –           –           –           –           –           –           –   xi


1.1 Introduction          –           –           –           –           –           –           –           –           –           –    1

1.1.1 Justification of the Study          –           –           –           –           –           –           –           –    4

1.1.2 Objectives of the study  –           –           –           –           –           –           –           –           –    5

1.2 Literature Review –           –           –           –           –           –           –           –           –           –    5

1.2.1 Parasites and their effect on freshwater fish host         –           –           –           –           –     5

1.2.2 Protozoa                   –           –           –           –           –           –           –           –           –           –     6

1.2.3 Myxozoa                  –           –           –           –           –           –           –           –           –           –     8

1.2.4 Trematoda     –           –           –           –           –           –           –           –           –           –     9

1.2.5 Cestoda                    –           –           –           –           –           –           –           –           –           –     10

1.2.6 Nematoda     –           –           –           –           –           –           –           –           –           –     11

1.2.7 Acanthocephala        –           –           –           –           –           –           –           –           –           –    12

1.2.8 Crustacea      –           –           –           –           –           –           –           –           –           –            –     13

1.2.9 Hirudinea                  –           –           –           –           –           –           –           –           –           –     14

1.2.10 Factors affecting parasite assemblages in fish hosts    –           –           –           –           –     14 Fish size (age)           –           –           –           –           –           –           –           –           –    15 Fish diet                    –           –           –           –           –           –           –           –           –    16 Fish sex                     –           –           –           –           –           –           –           –           –    16 Fish immune status   –           –           –           –           –           –           –           –           –    17 Condition of the environment          –           –           –           –           –           –           –    18



2.1 Study area –           –           –           –           –           –           –           –           –           –           –    20

2.2 Fish sampling        –           –           –           –           –           –           –           –           –           –    22

2.3 Examination of parasites   –           –           –           –           –           –           –           –           –    22

2.3.1 Examination of ectoparasite      –           –           –           –           –           –           –           –    22

2.3.2 Examination of endoparasites    –           –           –           –           –           –           –           –    23

2.4 Treatment, preservation and fixation of parasites.            –           –           –           –           –    23

2.4.1 Microscopic parasites     –           –           –           –           –           –           –           –           –    23

2.4.2 Cestodes:           –           –           –           –           –           –           –           –           –           –    23

2.4.3 Nematodes         –           –           –           –           –           –           –           –           –           –    23

2.5 Identification of parasites           – –           –           –           –           –           –           –           –    23

2.6 Haematological examination         –           –           –           –           –           –           –           –    24

2.6.1 Haemoglobin estimation (Hb)    –           –           –           –           –           –           –           –    24

2.6.2 Blood haematocrit estimation (PCV)    –           –           –           –           –           –           –    25

2.6.3 Red blood cell count (RBC)      –           –           –           –           –           –           –           –    25

2.6.4 Total white blood cell count (WBC)     –           –           –           –           –           –           –    26

2.7 Biochemical Parameters    –           –           –           –           –           –           –           –           –    26

2.7.1 Determination of aspartate transaminase (AST)            –           –           –           –           –    26

2.7.2 Determination of alanine transaminase (ALT)   –           –           –           –           –           –    27

2.7.3 Determination of alkaline phosphatase (ALP)   –           –           –           –           –           –    27

2.7.4 Determination of blood urea      –           –           –           –           –           –           –           –    28

2.7.5 Determination of serum creatinine         –           –           –           –           –           –           –    28

2.8 Statistical Analysis            –           –           –           –           –           –           –           –           –    29



3.1 Fish Species          –           –           –           –           –           –           –           –           –           –    30

3.2 Parasite Species     –           –           –           –           –           –           –           –           –           –    30

3.3 Morphological features of the Parasites Recovered –       –           –           –           –           –    30

3.4 Comparative Prevalence of Parasites in some Clariid Species of the Anambra

River System.        –           –           –           –           –           –           –           –           –           –    33

3.5 Parasitic infections of some Clariid fish hosts      –           –           –           –           –           –    35

3.6 Monthly/Seasonal prevalence of parasites of some Clariid species of the

Anambra River system.     –           –           —          –           –           –           –           –           –    37

3.7 Monthly/Seasonal Patterns of Parasitic Infection of Fish Hosts. –           –           –           –    39

3.8 Prevalence of Parasites of Some Clariid Species of the Anambra River System in

relation to sex        –           –           –           –           –           –           –           –           -.          –    41

3.9 Abundance of Parasites of some Clariid Species of the Anambra River System in

Relation to Sex.   –           –           –           –           –           –           –           –           –           –    43

3.10 Intensity of Parasites in some Clariid species of the Anambra River System –  –           –    45

3.11 Parasitic Infestations of Fish Hosts (Clarridae) by Sex –            –           –           –           –    47

3.12 Effect of Parasite Intensity on the Condition Factor K, and Hepatosomatic Index,

HSI of some Clariid species of the Anambra River System.      –           –           –           –    49

3.13 Parasite Infection of Fish Hosts by Body Weight          –           –           –           –           –    52

3.14 Parasite Infection of Fish Hosts by Total Length of Fish          –           –           –           –    54

3.15 Site of Infection of Parasites in the Fish Hosts –           –           –           –           –           –    56

3.16 Effect of Parasite on the Haematological Profile of some Clariid Species of the

Anambra River System –           –           –           –           –           –           –           –           –    58

3.17 Effect of Parasites on the Biochemical Parameters of some Clariid Species of the

Anambra River System  –           –           –           –                       –           –           –           –    60



4.1 Prevalence, Mean Intensity and Abundance of Parasites             –           –           –           –    63

4.1.1 Protozoan           –           –           –           –           –           –           –           –           –           –    63

4.1.2 Cestodes            –           –           –           –           –           –           –           –           –           –    64

4.1.3 Nematodes         –           –           –           –           –           –           –           –           –           –    65

4.2 Influence of Body Weight and Total Length on Parasitic Infection        –           –           –    65

4.3 Influence of Fish Hosts Sex on Parasitism           –           –           –           –           –           –    66

4.4 Influence of Season on the Patterns of Parasite Occurrence        –           –           –           –    67

4.5 Effect of Parasite on the Condition Factor and Hepatosomatic Index    –           –           –    68

4.6 Effects of Parasites on the Haematological Profile of Fishes       –           –           –           –    69

4.7 Influence of Parasites on the Biochemical Parameters of Clariid Fishes

of the Anambra River System     –           –           –           –           –           –           –           –    71

4.8 Conclusion            –           –           –           –           –           –           –           –           –           –    73

4.9 Recommendations            –           –           –           –           –           –           –           –           –    74






  • Introduction

Fish is an important and cheap source of protein supply in human diet (Usip et al., 2010; Bichi and Dawaki, 2010). Its digestibility, amino acid contents, and low cholesterol content rank it amongst the superior protein foods (Agbamu and Orhorhoro, 2007). According to El-Seify et al. (2011), people obtain about one-fourth (25%) of their animal protein world-wide from fin and shell fishes. More than forty percent (40%) of the protein diet of two-third of the global population is obtained from fish (Agbamu and Orhorhoro, 2007). Fish is especially important in the diet of people in the developing countries where malnutrition constitutes a major problem (Omeji et al., 2010). Thus in Nigeria today, fish is the major source of affordable animal protein. Due to the enormous demand on fish and other limiting factors, the demand and supply gap of fish for this country stands at about 1 mmt per annum (Atanda, 2007) with a current demand of 1.5 mmt (Abolagba and Omorodion, 2006).

Fishes are important to man as a good source of protein in man’s diet and as a vector of some human disease pathogens. One of the scientific importance of identifying a fish properly is to tell to some reliable extent the health condition of the fish, and certain parasitic infections present with some symptoms that bear on the external treatment of the fish (Ayanda, 2009a). All species of fish are vulnerable to various parasitic infections depending on the species of fish and the type of stream inhabited (Edema et al., 2008).

Some of the factors that enhance parasitic infection in fishes include reduced oxygen content of water, increase in organic matter in the water and poor environmental conditions (Ayanda, 2009b).

Parasites are organisms that are metabolically dependent on other organisms (hosts) for their continual existence (Symth, 1994). They obtain their basic requirements such as nutrients, shelter and enzymes from their host (Smyth, 1994; Okafor and Ubachukwu, 2009). They are a major concern not only to maritime but to freshwater fishes all over the world, and of particular importance in the Tropics (Bichi and Yelwa, 2010; Ekanem et al., 2011). Their effects on fishes include, nutrient devaluation (Hassan et al., 2010; Ekanem et al., 2011); alteration of biology and behavior (Lafferty, 2008); lowering of immune capability, morbidity and mortality (Nmor et al., 2004; Ekanem et al., 2011); growth and fecundity reduction (Nmor et al., 2004) and injuries depending on the parasite species and load. Studies on the parasites of fishes is a major concern in Africa presently (Akinsanya et al., 2007), Nigeria inclusive.

In Africa, a checklist of helminth parasites of freshwater fishes has been published by Khalil (1971) and various reports also exist from different parts (countries) of Africa, highlighting on intensities, prevalence, epidemiology and pathology of such parasitic infections. Paperna (1996) reported that the cichlids harbour majority of the infection which includes the adult digenea infecting different tissues of the body; trematode metacercaria of the family Clinostomidae encysting in tissue (Echi et al., 2009); and adult monogenea of the families Pousopothocotylidae, Dactylogyridae and Gyrodactylidae infecting the gills and skin.

The emanating need to culture fishes for protein consumption for the teeming rapidly growing populations in the developing countries have made it necessary to intensify studies on the parasite fauna of African freshwater fishes (Akinsanya et al., 2007). There is appreciable documentation of parasite fauna of catfish in Nigeria. One of the earliest reports in Nigeria in inland waters concerning fish parasites was that of Awachie (1966) who documented preliminary information on the parasites of fish in the Kainji Reservoir. He observed that not many fishes were infected. However in a similar study, Ukoli (1969) observed heavy parasitic infection of fish species from the same reservoir. Similar works have also been done in Nigeria by Yakubu et al. (2002) in Plateau State, Oniye et al. (2004) in Zaria, Ibiwoye et al. (2004) in Bida, Akinsanya and Otubanjo (2006) in Lagos, Edema et al. (2008) in Benin city, Ayanda (2008) in Ilorin, Echi et al. (2009) in Opi lake, Awharitoma and Ehigiator (2012) in Edo and Delta States, Eyo and Iyaji (2013) in Kogi State and Eyo et al. (2014) at Warri river.

The Anambra River is the largest tributary of the lower Niger River below Lokoja, and often regarded as a component part of the lower Niger lowlands (Udo, 1975). Thus considering its importance as commercial fishing center supplying fishes to populace from Southern Nigeria and beyond, a considerable biological and ecological studies have been undertaken and documented on some economically important tropical fish fauna from the river basin (Awachie and Hare, 1977; Awachie and Ezenwaji, 1981; Eyo and Mgbenka, 1992; Mgbenka and Eyo, 1992; Nwani, 1998; Ezenwaji, 1999; 2002; Nwani, 2004; 2006; Odo, 2004; Odo et al., 2012).

Azugo (1978) studied the ecology of the helminth parasite of the fishes of Anambra River system. Ezenwaji et al. (2005) studied the endo-helminth parasites of morchokid fishes of Anambra river basin. However, there is paucity of information on the impact of parasites on the haematology and the serum chemistry of the clariid family of the Anambra River System.

Therefore, as part of the study on the improvement of fishery and fish production in Anambra River basin, more so, because of the importance of catfish in aquaculture industry (Food and Agricultural Organisation, 2006), a study on the abnormalities of the blood and serum chemistry of the fishes of the river caused by parasite infestation is necessary.



1.1.1 Justification of the Study

Fish health management is the concept of proactively regulating the host, pathogen and environment to maximize the optimal condition for sustained growth and health. In order to get better nutrition from fishes, they must be free from diseases and mishandling. Fish diseases may be due to parasitic or non-parasitic causes. Among the parasites that infect freshwater fishes, helminthes form the most diversified group (Pinky et al., 2012).

Parasites are a major concern to freshwater and marine fishes all over the world, and of particular importance in the tropics (Iyaji and Eyo, 2008; Bichi and Dawaki, 2010; Ekanem et al., 2011). They constitute a major limiting factor to the growth of farmed fish in Nigeria (Bichi and Yelwa, 2010). The effects of parasites on fish include nutrient devaluation (Hassan et al., 2010); alteration of biology and behaviour (Lafferty, 2008); lowering of immune capability, induction of blindness (Echi et al., 2009 a, b); morbidity, mortality, growth and fecundity reduction (Nmor et al., 2004) and mechanical injuries depending on the parasite species and load (Echi et al., 2009 a, b). Most supply of fish in Nigeria comes from the Riverian ecosystem (Ekanem et al., 2011). Anambra State, where the Anambra River is located, is a traditional fishing district with a vast coastal land mass in the eastern area of the Niger River.

However, the increased demand on fish as a ready and safe source of protein to humans has necessitated the continuous studies on fish fauna and parasites. Therefore, the present study is necessary to fill the gap in the current knowledge on the parasitofauna of catfishes from Anambra River with regards to their effects on the haematology and serum chemistry of these species.



1.1.2 Objectives of the Study

The general objective of this study is to investigate the parasitofauna of wild clariid catfishes harvested from the Anambra River System, Nigeria.

The specific objectives are to:

  • investigate the prevalence, intensity and abundance of parasitic infection in the catfishes of the Anambra River System;
  • study the haematological abnormalities in the catfish fauna of Anambra River System due to parasitic infections;
  • compare the biochemical enzyme activities of parasite infected and uninfected catfishes of Anambra River System and
  • study the influence of parasite on the condition factor and hepatosomatic index of infected catfishes of Anambra River System.

1.2 Literature Review

1.2.1 Parasites and their Effect on Freshwater Fish Host

The effects of parasites on fish hosts in the wild may be difficult to isolate and quantify. However, studies of fish in captivity or under culture conditions have provided much information about the effects of parasites on fish survival (Iyaji and Eyo, 2008). It is evident that parasites can act as severe pathogens causing direct mortality or rendering the fish more vulnerable to predators (Kunz and Pung, 2004). Other effects of parasites on fish hosts, according to Sindermann (1987) include muscles degeneration, liver dysfunction, interference with nutrition, interference with respiratory functions, cardiac disruption, nervous system impairment, castration or mechanical interference with spawning, weight loss and gross distortion of the body.

According to Iyaji and Eyo (2008), the economic important of freshwater parasites are grouped into microparasites and macroparasites. The microparasites include protozoans – microsporideans and myxozoans while the macroparasites are comprised of helminthes such as monogenea and the diageneas, trematodes (flukes), cestodes (tapeworms), nematodes (roundworms) and acanthocephalans (thorny headed worms). The arthropod parasites are represented mainly by the copepods (Marcogliese, 2002), while annelid parasites are the leeches.

1.2.2 Protozoa

The Protozoans represent a vast assemblage of eukaryotic unicellular organisms. Protozoans are the most commonly encountered fish parasites, and can be the easiest to identify and control (Klinger and Francois-Floyd, 2009). According to Klinger and Francois-Floyd (2009), they can build up to very high numbers when fish are crowded causing weight loss, debilitation and mortality. This is because they exhibit a direct life cycle. Studies have established the presence of ecto- and endo-parasitic protozoans among freshwater fishes in Nigeria (Bichi and Dawaki, 2010; Bichi and Yelwa, 2010; Abidemi-Iromini and Eze, 2011; Omeji et al., 2011; Adeyemo and Daunemugham, 2012) and other countries (Nikolic and Simonovic, 1996; Molnar et al., 2004; Dove and O’donoghue, 2005; Hussein et al., 2010). Bichi and Dawaki (2010) reported the presence of the protozoa Ichthyopthirius and Myxobolus from the survey of ectoparasites of the gills, fins and skin of Oreochromis niloticus in Bagauda Fish Farm in Kano, Nigeria. Omeji et al. (2011) in Benue State, Nigeria, reported infestation of Clarias gariepinus in the wild and cultured environment by the protozoan parasites, Ichthyobodo sp., Ichthyopthirius multifiliis, Chilodonella sp. Trichodina sp. and Cryptobia iubilans. Adeyemo and Daunemughan (2012) while, investigating parasites of wild Parachanna obscura in Bayelsa, Nigeria, recorded the presence of Microsporidian parasite.   

The main groups of protozoan parasites of freshwater fishes are the ciliates, flagelletes, coccidians and microsporidia (Klinger and Francois-Floyd, 2009). Ciliates are protozoan parasites with cilia. Symptoms associated with infection depend on parasite load and species. Most ciliates do not appear to trouble host until numbers become excessive (Klinger and Francois-Floyd, 2009). Ciliates affecting freshwater fishes include Ichthyopthirius multifilis, Chilodonella sp., Tetrahymena sp., Trichodina sp.Apiosoma sp., Ambiphyra (formerly Scyphidia sp.), Epistylis sp. and Capriniana sp. (Pouder et al., 2011). According to Alvarez-Pellitero (2004) symptoms of ciliate infestation include spots of different colours on skin, hyperplasia, degeneration and necrosis of the gills, weakening of fish, loss of appetite, restlessness and breathing problems. Ciliates have been reported in freshwater fishes in the wild (Nikolic and Simonovic, 1996; Molnar et al., 2004; Omeji et al., 2010) and cultured (Hoffman et al., 1975; Abidemi-Iromini and Eze, 2011; Tang et al., 2012) environment. Abidemi-Iromini and Eze (2011) recovered I. multifiliis and Trichodina acuta from assessment of parasite fauna of Tilapia zilli and O. niloticus from different water bodies in Akure, Nigeria.

Flagellates are characterized by the presence of one or more flagella. These include Ichthyobodo spp (also known as Costia) which causes costiasis, a disease of the skin and gills. Fish affected by Ichthyobodo necator appear lethargic and thin, and may show grey-whitish pellicles on the skin, epidemic erosion, haemorhages or ulcers, and gill hyperplasia, and oedema (Alvarez-Pellitero, 2004 ). Cryptobia sp. and Piscinoodinium sp. are other ectoparasitic flagellates of freshwater fishes. Hexamita (Spironucleus) sp., Trypanosoma sp. and intestinal and haemoparasitic Cryptobia sp., are some endo-parasitic flagellates.

The coccidian parasites which are mainly intestinal, found in freshwater fishes are members of the genera Gaussia (Molnar et al., 2004), Eimeria and Cryptosporidium (Eli et al., 2011).

Microsporidia are strictly intracellular parasites that utilize host tissue for reproduction. In some species, the infected cell becomes hypertrophic, accommodating proliferating parasites (xenoma) (FAO, 1991). The development cycle of microsporidians include merogony and schizogony (proliferative phase) producing an enormous number of parasites, and sporogomy which generates mature spores. The major pathological sign is associated with hypertrophy. Adeyemo and Daunemughan (2012), investigating parasites of wild Parachanna obscura in Bayelsa, Nigeria, recorded the presence of microsporidian parasite.

  • Myxozoa

Myxozoa parasites are spore-forming metazoans that have a two-host life cycle. Myxosporidia are almost exclusively parasites of fish (Fomena et al., 2008). Some species are of economic importance as they can cause chronic weakening disease (Klinger and Francois-Floyd, 2009). 2,180 myxopsorean species distributed in 62 genera have been established so far (Lom and Dykova, 2006) and it is not unlikely that many more remain undiscovered. In Africa, more than 135 species are known today, which affect freshwater as well as marine fishes (Kostoingue et al., 2001; Fomena et al., 2007; Fomena et al., 2008). About a 100 species in freshwater fishes in Africa belonging to the genera Myxobolus (BUTSHLI, 1882), Henneguya (THELOHAN, 1892), Myxobilatus (DAVIS, 1994), Chloromyxum (MINGAZZINI, 1890) and Parahenneguya (SEKITI, 1997), has been established (Fomena et al., 2007). Cichlidae and Cyprinidae are some common freshwater hosts (Paperna, 1996).

Myxospora cause coelozoic (in internal cavities e.g. urinary bladder) and histozoic infections (Paperna, 1996). Infections by Myxobolus sp. and Henneguya sp. have been reported in Central, East and West Africa (Paperna, 1996; Kostoingue et al., 2001; Fomena et al., 2007; Abowei and Ezekiel, 2011). Fomena et al. (2007) reported three new species of Myxosporea of genus Myxobolus in Cameroon. Bichi and Yelwa (2010) recorded Henneguya sp. from examination of Clarias gariepinus in Bagauda Fish Farm, Kano, Nigeria.

  • Trematoda

Trematodes are flatworms also referred to as flukes. The class Trematoda consists of the Monogenea, Digenea and Aspidogastrea with the last being of little parasitological significance as most are free living. Monogeneans are mostly ecto-parasitic platyhelminths and typically parasitize the gills, skins and fins of fishes (Reed et al., 2009). They are highly host-and site-specific and also exhibit a direct life cycle (Reed et al., 2009). The opisthaptor, a posterior adhesive apparatus, is the most recognizable morphological character of the group. Monogenea includes two main groups, Monopistocotylea (with a simple adhesive disc) and Polyopistocotylea (with a complex adhesive disc) (Olson, 1974). Gyrodactylus sp., Dactylogyrus sp., Furnestinia sp. and Diplectanum spp. are the most significant monopisthocotyleans species for cultured fishes (Alvarez–Pellitero, 2004). Polyopisthocotylea includes several species of pathological concern for fish cultures, and most of them belong to the family Microcotylidae, and some to Heteraxinidae. Several studies have reported monogeneans in freshwater fishes (Jean-Francois and Alain, 1991; Mendoza-Franco et al., 1999; Tombi and Bilong, 2004; Salgado-Maldonado, 2008; Soliman and Ibrahim, 2012). Mendoza-Franco et al. (1999) reported the presence of monogeneans in cichlid, Pimelodid, characid and Poeciliid fishes. Data about Monogenea in Nigeria fishes appear to be limited.

Lethargy, anoxia, loss of appetite, excess mucus secretion, scratching and haemorrhage are some chemical signs associated with monogenean infection (Alvarez-Pellitero, 2004).

Digenean trematodes are endoparasitic platyhelminths with complex (indirect) life cycle involving a series of hosts (the first of which is almost always a mollusk) (Cox, 1993, Smyth, 1994). Gastrointestinal tract, coelom and blood vessels are some sites occupied by the adult digenean trematodes. Over 50 species of digenetic trematodes from 15 families occur in freshwater fish species in Africa (Iyaji and Eyo, 2008). Fishes may act as either intermediate or definitive host depending on the digenean species. Okaka and Akhigbe (1999) reported the presence of the trematodes (Clinostomum spp., Allocreadium spp. and Diplostomum tragenna) in freshwater fishes in River Osse in Benin, a Niger Delta area of Nigeria. The trematode Clinostomum metacercaria had been observed in Parachanna obscura from Lekki Lagoon, Lagos, Nigeria (Akinsanya et al., 2010).

  • Cestoda

Cestodes (tapeworms) are endoparasitic flat worms with indirect life cycle involving at least one intermediate host. There is variation in the life cycle of cestodes with fish acting as the primary, intermediate or paratenic host. Cestodes parasitize fishes in both culture and wild environments and are of variable economic importance (Ayanda, 2009a; Bichi and Yelwa, 2010). Adult cestodes are usually found in the gastrointestinal tract, while larval stages may be isolated from a variety of organs. Larval cestodes unlike adults, are not highly host-specific.

Most species causing diseases in fish of economic significance fall within three orders: Caryophyllidea (e.g. Carophyllaeus), Pseudophyllidea (e.g. Bothnocephalus, Ligula and Diphyllobothrium) and Proteocephalidea (e.g. Proteocephalus) (Alvarez-Pellitero, 2004). Mechanical damage or obstruction and interference with nutrient absorption may characterize the presence of adult cestodes in the gastrointestinal tract, but the most serious pathology is caused by migrating larva. The plerocercoid larvae of cestodes constitute the most damaging parasites of freshwater fishes; the problem associated with infection results when larvae damage vital organs such as brain, heart and eye (Klinger and Francis-Floyd, 2009).

Several studies have reported the presence of cestodes in freshwater fishes in the wild and culture environments in Nigeria (Ezeri, 2002; Yakubu et al., 2002; Nmor et al., 2004; Akinsanya and Otubanjo, 2006; Ayanda, 2009a; Bichi and Yelwa, 2010; Ekanem et al., 2011Ogbulie et al., 2011).  The presence of the cestode, Polyonchobothrium was reported by Okaka and Akhigbe (1999), Akinsanya and Otubanjo (2006) and Ayanda (2009a) in freshwater fishes in Nigeria. Ezeri (2002) reported the presence of the larval cestode, Paradilepsis in cultured Oreochromis niloticus in Ogun State, Nigeria. Anomotaemia sp., Protoeocephalus sp., Stocksia pujehuni and Wenyonia acuminate are other species of cestode that have been isolated from freshwater fishes in Nigeria (Okaka and Akhigbe, 1999; Akinsanya and Otubanjo, 2006; Ayanda, 2009a).

  • Nematoda

Nematodes (or round worms) are endoparasites in animals. Most species which infect fish have indirect life cycle with a single intermediate host and one or more paratenic hosts. Fish may serve as primary, intermediate or paratenic host (Marina, 2008). They can infect all organs of the host causing loss of function to damaged area (Klinger and Francois – Floyd, 2009). Adults are usually found in the gastrointestinal tract and larvae in a variety of organs including skin, body cavity, gastrointestinal tract and visceral of the fish hosts. Emaciation, anaemia, unthriftness and reduced vitality are some symptoms of nematode infection in fishes (Klinger and Francois-Floyd, 2009).

Nematodes have been reported in various freshwater systems in Nigeria (Okaka and Akhigbe, 1999; Nmor et al., 2004; Olofintoye, 2006; Akinsanya et al., 2008; Ayanda, 2009a). Olofintoye (2006) reported the presence of the nematode, Cuculanus in freshwater fishes in Ekiti State, Nigeria. Camallanus sp., Procamallanus sp., Spirocamallanus sp., Spinitectus sp., Serradactnitis sp. and Spironoura sp. (nematodes) were isolated by Okaka and Akhigbe (1999) from freshwater fish in Osse River, Edo State, Nigeria.

  • Acanthocephala

Acanthocephalan parasites are endoparasitic helminthes with in-direct life cycle involving arthropod intermediate hosts and vertebrate final host. Fish may act as the definitive host, harbouring adult worm in its gastrointestinal tract, or as intermediate host harbouring the second stage larvae (cystecanth) with its retracted proboscis, in other extra-intestinal sites (Lyndon and Kennedy, 2001). Acanthocephalan parasites are recognized by their recurved hooks-crowned evaginable proboscis. Pathogenic effects are due to attachment of the adult to the gastrointestinal tract by means of the proboscis, and also to the encapsulation of the larva stages in the tissues (Paperna, 1996). Pathological sign depends on the acanthoceplan species and location. Extensive inflammation, granuloma, peritonitis, and obstruction of the alimentary canal may be observed (Paperna, 1996). Acanthocephalan parasites have been reported in freshwater fishes in Nigeria (Okaka and Akigbe, 1999; Nwani et al., 2008; Ayanda, 2009a; Usip et al., 2010). Nwani et al. (2008) isolated Rhadinorhynchus horridus and Gnathonemus petersi (Acanthocephala) from the fish, Hyperopisus bebe bebe in Anambra River, Nigeria. Onyedineke et al. (2010) recovered the acanthocephalan parasites, Pomphorhynchus, Quadrigidae and Neochinorhynchus in freshwater fishes from River Niger at Illushi, Edo State, Nigeria.

  • Crustacea

Parasitic crustaceans are ectoparasites on fish and are usually blood feeders on the gills, skin and fins; and large numbers can cause serious pathogenic effects (Marina et al., 2008). Parasitic crustaceans are increasingly serious problems in wild and cultured fish (Piasecki et al., 2004; Klinger and Francis – Floyd, 2009). Depending on the fish species and degree of invasion, parasitic crustaceans may cause fish mortality (Oktener et al., 2008). Oktener et al. (2008) reported mortality of the fish, Cyprinus carpio and Capoeta trutta due to infestation by Lamproglena pulchella (Lernaeidae).

Parasitic crustaceans are found mainly in the class Branchiura, Copepoda and Malocostraca (Marina, 2008); the class Copepoda being a major concern to fresh water fishes (Marcogliese and Parasitology Module Steering Committee, 2011). Copepoda play major roles in freshwater ecosystem which includes serving as food for many fish, acting as fish parasites, micropredator of fish and other organisms, intermediate host of fish parasites, and hosts and vectors of human diseases (Piasecki et al., 2004). According to Piasecki et al. (2004), they serve useful purpose if they are properly managed.

Most of the parasitic crustaceans that have been described are copepods and majority of them constitute a problem to freshwater fish mainly from the families Lernaeidae and Ergasilidae (Ho, 1998; Klinger and Francois-Floyd, 2009). According to Ho (1998), about 110 species of lernaeid copepods are known from 322 species of freshwater fishes belonging to 161 genera in 41 families. Perez-Bote (2005) and Yuniar et al. (2007) are among studies that had reported parasitic copepods in fish. Bichi and Yelwa (2010) had reported the presence of the crustacean Ergasilus sarsi with 24.6% on Clarias gariepinus in Bagauda Fish Farm, Kano, Nigeria.

  • Huridinea

Leeches are occasionally seen in wild and pond raised fish where they act as ectoparasites feeding on blood and body fluid of hosts; and pathology is dependent on infestation intensity (Klinger and Francis Floyd, 2009). Abidemi-Iromini and Eze (2011) had reported the presence of leeches in freshwater fish in Nigeria.

Volonterio et al. (2004) observed the effects of the leech Myzobdella urguayensis infesting the gill filaments of Hoplias alabaricus, (Characiformes, Erythrinidae) and Rhamdia quelen (Siluriformes, Pimelodidae), which resulted in hemorrhage with clot formation and fibrin deposition at the attachment sites. They equally observed inflamed gill filaments which exhibited oedema and infiltration of mononuclear leukocytes. Damages to skin comprised of bite wounds, hemorrhages, erosion of mucus membranes, the epidermis and basal hyperplasia (Food and Agricultural Organisation, 1991; Volonterio et al., 2004). Apart from the mechanical injuries and pathological effects leeches have on fish hosts; they have also been discovered to be vectors of haemoprotozoans (Food and Agricultural Organisation, 1991). For example Piscicola geometrea was shown to transmit viral disease to carp (Ahne, 1985). Bleeding wounds may also become contaminated by opportunistic bacteria and fungi (Kabata, 1985).

1.2.10 Factors Affecting Parasite Assemblages in Fish Hosts

There are numerous biotic and abiotic factors that affect parasite assemblages (Esch, 1982; Kennedy, 1995). These factors include the following: physiological condition of the fish host, host diet, host size, evolutionary history and environmental factors such as season of the year, size and type of water body, altitude, temperature, salinity, oxygen and pH (Poulin, 2004; Rolbiecki, 2006; Sinkova et al., 2008; Alverez – Pellitero, 2008; Iyaji et al., 2009; Lagrue et al., 2011 and Rahman and Saidin, 2011). Though a number of physical and chemical factors are known to affect a wide range of aquatic vertebrates and invertebrate’s life cycles, the effect of biotic factors on abundance and prevalence of parasites has been the major focus of research (Iyaji et al., 2009). The ecological relationship between hosts and parasites are usually influenced by the organisms inter and intra-specific interactions with biotic and abiotic components of the environment (Williams and Jones, 1994). Fish size (age)

Poulin (2000) stated that in fish population, parasitic infection tends to increase with increasing host age and size. He argued that older fish have longer time to accumulate parasites than younger ones and may provide establishment and therefore tend to have heavier worm burdens because they eat more parasitized prey and offer large surface area for skin-attaching parasites. Munoz and Crib (2005) reported that larger host has higher parasites richness, abundance and pattern might be explained by combination of resources, time and prey. In general, large hosts have more space, more flux of energy (i.e. food) and microhabitats for parasites than small hosts. Furthermore, large fish are older than smaller individuals of the same species so that they have more opportunities to become infected (Rhode 1993; Munoz et al., 2002).

Several studies have reported corresponding variation in parasite load and type with increasing fish size (Olofintoye, 2006; Sinkova et al., 2008; Ekanem et al., 2011; Adeyemo and Daunemughan, 2012). While Olofintoye (2006) reported an increase in infection with fish growth in T. zilliiClarias anguilaris and C. gariepinus examined, Adeyemo and Daunemughan (2012) observed higher infection among the smaller sizes of Parachanna obscura in his investigation.  Rolbiecki (2006) in his explanation of the reasons for variation in parasite load with varying fish length was of the view that different length classes of fish differ in their mode of life and thus their degree of exposure to parasites. Variation in food type and increase in the quantity of water consumed were among other reasons given as contributing to the observed size-based parasite variation. He also stated that for parasites that actively penetrate their host such as the monogeneans Ancyrocephalus paradoxus in Zander and Dactylogyrous amphibothrium in ruffe, the trematode Posthodiplostomum and the copepod Anchtheres percanum in Zander, size of the fish is the most important factor facilitating infection. Akinsanya et al. (2007), Akinsanya et al., (2008) and Akinsanya et al. (2010) have, however, reported parasite burdens that were independent on fish age. Length limits in parasite infection have been reported (Rolbiecki, 2006). Increase in parasitic infection with increasing length of fish in fresh water, and decrease in parasites with increasing fish length in marine habitat has been observed (D’Silva et al., 2012). Fish size as it appears, is not an exclusive determinant of parasite prevalence and/or intensity. The nature of the parasite and the fish habitat are other contributing factors. Fish diet

Link exists between fish diet and the flow of trophically transmitted parasites (Lagrue et al., 2011). Food–borne parasite species are distributed among fish hosts according to food preference (Rolbiecki, 2006) such that euryphagous (with varied diet) species accommodate wider range of food borne parasite species, specificity in parasitism being the only restriction, while stenophagous (with narrow range of diet) fish species are  restricted to the parasites associated with their food choice. Various parasites especially helminthes (e.g. Euplorchis californiensis and Coitocaecum parvum) utilize trophic interaction among various organisms as a means of transmission from one host to another. Euplorchis carliforniensis, for example, is transmitted from killer fish, Fundulus parvipinnis to bird (final host) through trophic interaction (Lafferty, 2008). The transmission of Coitocaexum pervum to the fish Gobiomorphus cotidianus is another instance ((Lagrue et al., 2011). Fish Sex

Fish sex is one of the parameters that have been widely studied to determine its contribution to parasite assemblage in fish. Explanations of this sex bias in parasitism have focused mainly on two factors: variation among male and female fish in reproductive demand and ecological requirements. According to Skarstein et al. (2001) and Simkova et al. (2008) fishes both male and female invest differently in reproduction; male invest more in mate attraction through the exhibition of sexual ornamentation while females invest in gamete production. The steroid hormones (mainly testosterone) required for ornamentation in males is immunosuppressive (Folstad and Karter, 1992) and thus subjects the male fish to great risk of parasitic infection during spawning. Female fish are susceptible also to parasite during breeding period. Variation in ecological requirements between male and female fish within a population may also contribute to differences in parasite species assemblage (Iyaji et al., 2009).

Observations by several researchers have on the contrary, revealed parasite assemblage not significantly affected by fish sex (Gbankoto et al., 2001; Akinsanya et al., 2007; Bichi and Yelwa, 2010; Rahman and Saidin, 2011; Adeyemo and Daunemughan, 2012). Gbankoto et al. (2001), observed a non-significant difference in the prevalence of Myxobolus sp. in male (20.7%) and female (20.4%) Sarotherodon melanotheron. Rahman and Saidin (2011) in their conclusion stated that fish sex play an important role in influencing the susceptibility of fish to parasites despite the non-significant difference observed in prevalence stratified by sex in fish examined. Fish Immune Status

A system of cells and tissues, biochemical and physiological characteristics of an organism that ensures its protection against foreign invaders (such as parasites) constitute its immune system. Because of the negative consequences of the presence of parasites on or in the host, the host has developed a performing immune system to reduce fitness cost generated by parasitism (Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000). The parasite conversely, attempt to circumvent or weaken the host immune defense. These defense and evasion strategies by both the host and the parasite are a necessity for survival in unfavourable condition (Cornet et al., 2009; Nnadi et al., 2011).

Both innate and adaptive immune responses similar to that found in mammals are mounted by fish to control parasitic infections (Alvarez – Pellitero, 2008; Rohlenova et al., 2011). According to Alvarez –Pellitero (2008), innate immune initiation in fish depends on the recognition of pathogen by pathogen recognizing-receptors (PRRs) (mainly Toll-like receptors). B-lymphocytes and antibodies have also been implicated in adaptive response. The efficiency of host immune response and hence its ability to eliminate and/or prevent infection depends on the host genetic, physiological and environmental conditions such as stress, immaturity or aging, and malnutrition; and also the evasive strategies of the parasite (Smyth, 1994). The Condition of the Environment

The condition of the environment influence the parasites infecting a fish host (Koskivaara, 1992) and the symptoms associated with the infection. Abiotic and biotic factors in the environment such as water temperature, pH, oxygen content, pollution and competitors among other factors affect fish (Thompson and Larsen, 2004) and fish parasitoses (Kenedy, 1995; Vankara et al., 2011). Some of these factors affect fish physiology. Water temperature is considered the strongest abiotic factor which affects fish physiology including immune function (Rohlenova et al., 2011). Unfavourable temperature, as suggested by Rohlenova et al. (2011), lowers fish acquired immunity. Pollution of fish habitat, which reduces water oxygen contents and /or alters its pH level, may offset fish physiology favouring parasite infestation (Kelly et al., 2010). Lewis and Morris (1986) had drawn attention to the hypnoxic effect to fish of nitrite pollution of their habitat. Kelly et al. (2010) reported the synergistic effect of glyphosate formulation, a herbicide, and the trematode parasite Telogaster opisthorchis on the fish Galaxias anomalus; such that the juvenile fish survival which were unaffected by exposure to either glyphosate or Iopiosthorchis infection alone, was significantly reduced by simultaneous exposure to both.

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