Abstract

Introduction

The Indian mackerel Rastrelliger kanagurta (Cuvier) forms an important fishery along east and west coasts of India appearing in line and trawler catches almost throughout the year. Especially during the months February to May, it dominates the fish landings along these coasts. Vast information is available on the biology of this fish including food and feeding habits (Bhimachar and George 1952; Rao and Rao 1957; Kuthalingam 1959; Venkataraman 1961; Luther 1973; Sivadas and Bhaskaran 2009), reproductive biology (Pradhan 1956) and population biology Jayasankar et al. 2004).

Despite its common occurrence in the Indian waters, the parasite fauna has not been subjected to any detailed study. The available information deals with descriptions or reports of single or few parasite species belonging to Monogenea (Tripathi 1954; Unnithan 1964; Gupta and Krishna 1977; Raju and Rao 1978, Murugesh 1995), Digenea (Madhavi 1972, 1977, 1982; Gupta and Govind 1981; Gupta and Puri 1981; Gupta and Ahmad 1976; Madhavi et al. 1986; Gupta and Gupta 1987); Crustacea (Gnanamuthu 1951; Pillai 1961, 1962, 1965, 1967; Tripathi 1962; Bennet 1967) and Isopoda (Ravichandran et al. 2009; Ramesh Kumar and Ravichandran 2010). Rohde (1989) published a comprehensive account on Monogenea of Rastrelliger sp. collected from different geographic areas.

During our studies on metazoan parasite communities of marine fishes of Visakhapatnam coast, an analysis was made on the species composition of metazoan parasites of Rastrelliger kanagurta. This paper deals with the various parasite species found in Rasterlliger kanagurta of Visakhapatnam coast of Bay of Bengal and discusses the role of the mackerel as a host for various metazoan parasites.

Materials and methods

One hundred and eighty-four individuals of R. kanagurta ranging in size from 120 to 240 mm and collected between January 2006 and January 2007 from fish landings at Fishing Harbour of Visakhapatnam were examined. Standard methods were followed for collection, fixation and identification of parasites. Monogeneans and digeneans were fixed in AFA, stained with alum carmine and mounted in balsam. Copepods were fixed in 10% formalin, cleared in lactic acid and dissected using fine needles. Diagrams were drawn with the help of a camera lucida. For each species data on prevalence and mean intensity to infection were recorded. The definitions for ecological terms were followed from Bush et al. (1997).

Results

Fifteen species of metazoan parasites including three species of Monogenea, seven species of Digenea and five species of Copepoda were found infecting the fish (Table 1). Infections with cestodes and acanthocephalans were not found. The few Larval cestodes and nematodes found were not included here because of their rare occurrence.

Digenea

Family LEPOCREADIIDAE

Opechona bacillaris (Molin, 1859) Dollfus, 1927 (Fig. 1)

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Fig. 1

Opechona bacillaris

Synonyms: Distomum bacillare Molin, 1859; Distomum (Dicrocoelium) bacillare of Barbagallo and Drago (1903); Pharyngora bacillaris (Molin, 1859) Nicoll, 1910; Distomum increscens Olsson, 1868; Pharyngora retractilis Lebour, 1908; Distomum sp. Nicoll, 1909; Pharyngora olssoni Yamaguti, 1934; Neopechona olssoni (Yamaguti, 1934); Lepidapedon elongatum Chernyshenko, 1949; Opechona sp., Mackenzie, 1974; Lepocreadium guptai Gupta and Gupta, 1987.

Remarks

O. bacillaris has earlier been reported from R. kanagurta of Visakhapatnam and Kalingapatnam coasts (Bay of Bengal) by Madhavi (1972) and Madhavi et al. (1986). The species is characterized by somewhat elongated body narrowed anteriorly, presence of eye-spot pigment, infundibuliform oral sucker, small ventral sucker, pseudo-oesophagus shorter than oesophagus, gonads in posterior third of the body, vitellarium follicles extending to near the posterior border of ventral sucker, post testicular space 348–742 long and eggs measuring 78–80 by 36–40.

O. bacillaris is cosmopolitan in distribution. Bray and Gibson (1990) have furnished details of hosts, geographic distribution and synonyms of O. bacillaris and provided a key for separation of valid species of the genus Opechona Looss, 1907. They considered Lepocreadium guptai Gupta and Gupta, 1987 as a synonym of O. bacillaris and regarded many Indian species of the genus namely O. siddiqui Ahmad, 1984 from R. kanagurta,O. ahmadi Gaevskaya, 1990 from Pomadaysmaculatus, O. moshina Ahmad, 1984 from Scomberoides tala, O. vinodae Ahmad, 1984 from Pampus argenteus and O. travassosi Ahmad, 1991 from Fistularia villosa as speciesinquirendae, since clarification is required as to the presence or absence of a uroproct, an important character used for the separation of Prodistomum spp from Opechona spp.

During the present study several specimens of O. bacillaris were collected from R. kanagurta the prevalence and mean intensity to infection were 33% and 3.4 respectively. The specimens agreed in all details with the description provided by Bray and Gibson (1990) for the species from North-East Atlantic region except for the following differences: Body is narrow anteriorly where as in N-E Atlantic forms it is more or less of uniform width. External seminal vesicle is surrounded by numerous prostatic gland cells, their presence not reported in N-E Atlantic forms. Vitellarian follicles are less dense and extended anteriorly only up to the base of cirrus sac rather than just posterior to ventral sucker as reported for N-E Atlantic forms. Testes are more anteriorly located and are contiguous.

Prodistomum waltairensis (Madhavi, 1972) Bray and Gibson, 1990.

Synonym: Opechona waltairensis Madhavi, 1972.

Remarks

This species was originally described as O. waltairensis by Madhavi (1972) but Bray and Gibson (1990) included it under the genus Prodistomum Linton, 1910 on the basis of the absence of a uroproct.

P. waltairensis is characterized by the long slender body, sub-equal suckers, pre-pharynx and oesophagus more or less of equal size, lobed gonads, vitellarium extending to the level of bifurcation and excretory vesicle to the level of pharynx. It closely resembles P. hynnodi Yamaguti, 1938, but differs mainly in having lobed gonads.

Prodistomum orientalis (Layman, 1930) Bray and Gibson, 1990 (Fig. 2).

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Fig. 2

Prodistomum orientalis

Synonyms: Pharyngora orientalis (Layman, 1930); Opechona orientalis (Layman, 1930); Opechona scomberi (Yamaguti, 1938); Lepocreadium puriensis Gupta and Gupta, 1987.

This species originally included under the genus Opechona has been transferred to Prodistomum as P. orientalis by Bray and Gibson (1990) based on the absence of an uroproct.

Bray and Gibson (1990) furnished details of the synonyms, the hosts and geographic distribution as well as the characteristic features of the species. The present specimens agreed fully with the description given by Bray and Gibson. A few prostatic cells that occurred surrounding external seminal vesicle were not reported by Bray and Gibson. The present specimens also keyed to P. orientalis in the key provided by Raychard et al. (2008) for differentiation of specie of the genus Prodistomum.

P. orientalis has been recorded from R. kanagurta from Aden (Indian Ocean) by Parukhin (1976). Records from the related hosts include those from Sulawes (N-W Pacific ocean) by Yamaguti (1953) and North-west Australia by Korotaeva (1974) and Bay of Bengal by Zhukov (1960). Taking into consideration the preference to scombrid hosts and also the morphological features, Bray and Gibson considered Lepocreadium puriensis Gupta and Gupta, 1987 from R. brachysoma from Puri coast, Bay of Bengal as a synonym of P. orientalis.

Family GORGODERIDAE

Phyllodistomum sp.

Remarks

Fairly large sluggish flukes measuring 4-6 mm, appearing deep brown in colour and the gut engorged with blood were found in the kidneys of R. kanagurta during the months of Nov–Jan. Only 5 out of 184 fish examined showed the infection each infected fish harbored two flukes, giving a prevalence of 2.7% and mean intensity of 2.0. The organization of the body suggested the genus Phyllodistomum. The species is yet to be identified.

Family DIDYMOZOIDAE

Renodidymocystis yamagutii Madhavi, 1982

Remarks

The genus Renodidymocystis was erected by Madhavi (1982) with R.yamagutii from the kidneys of R. kanagurta, Bay of Bengal as the type species. During the present study, infections with the didymozoid occurred in the kidneys and also blood vessels, the prevalence of infection were fairly high being 45.6%. The forms agreed fully with the original description, except that the eggs were 12 by 6–8 μm rather than 8–10 by 4 μm in the type specimens.

Family HEMIURIDAE

Lecithocladium angustiovum Yamaguti, 1953 (Fig. 3).

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Fig. 3

Lecithocladium angustiovum

Synonyms: L. scomberi Yamaguti, 1953; L. bulbolabrum Reid et al., 1966; L. indicum Gupta and Gupta, 1981; L. manteri Gupta and Puri, 1982; L. microlepidotusi Gupta and Govind, 1981; L. siddiqui Gupta and Gupta, 1987; L. tewari Gupta and Gupta, 1987; L. unibulbolabrum Fischthal and Thomas, 1997; L. cibium Gupta and Jain, 1992. Clupenurus thynensis Bilqees et Knight, 1985; Clupenurus scomberomori Wang, 1982; L. jagannath Ahmad, 1981.

Remarks

In the genus Lecithocladium as many as 32 species were recorded from marine fish of Indian region. Most of these are not well defined and many of them may not be valid species. Gibson and Bray (1986) in an attempt to clear the confusion reduced the number of species recorded from Indo- Malayan region from 40 to 6. Further, it is also felt that some of the hemiurid genera erected from Indian region such as Clefticolletta Sahai and Srivastava, 1978; Bengalotrema Malhotra, Nanda, Mukherjee, Ghosh, Sukul and Capoor, 1989 may be synonymous to Lecithocladium (see Gibson 2002).

L. angustiovum is the most dominant digenean found in R. kanagurta in the present locality, occurring with a prevalence of 88.5%.

Family LECITHASTERIDAE

Aponurus laguncula Looss, 1907 (Fig. 4)

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Fig. 4

Aponurus laguncula

Synonyms: Aponurus spp. of Linton, 1940; A. trachinoti Manter, 1940; A. trachinoti (Yamaguti, 1971); A. elongatus Siddiqi and Cable, 1960; A. orientalis Ahmad, 1981; A. waltairensis Hussain, Rao and Shyamasundari, 1985.

Bray and Mackenzie (1990) furnished details of the hosts, geographic distribution and earlier reports of A. laguncula. This species is highly polyxenic and has a wide geographic distribution. A notable feature of the species is the wide range in egg size, 24–42 × 10–21. The egg shape is also considered distinctive with narrow more or less pointed anopercular end.

In view of the wide variation in egg size and the euryxenic nature, Bray and Mackenzie (1990) expressed the view that many of the species reported under genus Aponurus would fall synonyms to A. laguncula. They examined the validity of the various species reported under the genus and discussed the characters used for separating them from A. laguncula. The most significant features for separation of species are considered to be the size of sinus sac, sucker proportions and the alignment of gonads.

Four species of Aponurus have been recorded from marine fishes of India, A. breviformis Srivastava, 1939, A. bengalensis Srivastava, 1939, A. orientalis Ahmad, 1981 and A. waltairensis Hussain, Rao and Shyama Sundari, 1984. Bray and Mackenzie expressed the view that all these four species may be synonymous to A. laguncula. During the present study infections with A. laguncula are noted in R. kanagurta as well as in other marine fish hosts such as carangids, lutianids, polynemids, Arius spp, Terapon spp and Nemipterus sp., thus confirming the euryxenic nature of A. lagancula. The flukes occurred attached to buccal cavity or anterior part of stomach and appeared in small numbers in gill washings. The prevalence of infection is 16.8%.

Discussion

The study based on examination of 184 R. kanagurta collected as monthly samples from Visakhapatnam coast, Bay of Bengal revealed the metazoan parasite fauna of the scombrid fish to be fairly rich comprising of 15 species of parasites including three species of monogeneans, seven species of digeneans and five species of copepods. Cestodes, nematodes and acanthocephalans were not found. The parasite fauna of R. kanagurta is dominated by digeneans belonging to Hemiuridae and Lepocreadiidae and this situation would be related to the feeding behaviour of R. kanagurta which comprises planktonic organisms, crustaceans etc. Information available on the life cycles of Lecithocladium spp. and Aponurus spp. indicates that planktonic organisms such as medusae and copepods serve as intermediate hosts (Koie 1991). Similarly the life cycle of O. bacillaris also involves medusae as second intermediate hosts (Koie 1975). Although the complete life cycle of didymozoids is still not known, the available knowledge indicates that the copepods serve as second intermediate hosts (Cable and Nahhas 1962 and Madhavi 1968). Thus the parasite fauna of R.kanagurta is a clear reflection of its planktonivorous diet. The scarcity of larval cestode and nematode infections suggests that R. kanagurta might be occupying the peak trophic level in the food web and may not constitute an important food item for the larger carnivorous fish. Examples such as these indicate the importance of the status of the fish in the food web as a determinant of species richness and diversity of parasites in the marine ecosystem (Marcogliese 2001).

Some of the parasite species like L. angustiovum, O. bacillaris, Prodistomum spp. and R. yamagutii that occurred with high prevalence and mean intensity are to be regarded as typical parasites of this fish. In general the parasite fauna exhibited a high degree of host specificity. Except for A.laguncula which is found to be polyxenic, all the other species showed specificity to R.kanagurta or other species of scombrid fish. The low number of generalist parasites observed may reflect the reduced exchange of parasites between R. kanagurta and other marine fish. A high degree of adaptability, both physiological and ecological, is thus seen between the host R. kanagurta and its parasite fauna.

The three species of monogeneans and five species of copepods occurred with low prevalence and intensity indicating that R. kanagurta from this locality is not a suitable host for these ectoparasites. Out of the five species, three species Orbitocolax aculeatus, Nothobomolochus kanagurta, and Peniculus scomberi are specific to R. kanagurta. Caligus kanagurta and Lernanthropus kanagurta occurred not only on Rastrelliger but also on carangid fish.

The parasite fauna of R. kanagurta also shows a distribution parallel to the host distribution. Rohde (1989) undertook a detailed study of monogenean fauna of Rastrelliger spp, and reported all the three species of monogeneans recorded during the present study. Four of the seven species of digeneans reported during the present study namely O.bacillaris, P. orientalis, L. angustiovum and A. laguncula were also recorded from other parts of Indo-Pacific region. Further P. waltairensis is closely related to Prodistomum hynnodi Yamaguti, 1938 recorded from scombrid fish from off the coast of Japan. Three out of five species of parasitic copepods have also been recorded from the other regions of Indo-Pacific region especially off the coast of China and Taiwan. It is evident that the lack of endemicity, the high degree of host specificity and probably also the high degree of predictability are characteristic features of the parasite fauna of R. kanagurta.

The preliminary studies carried out by earlier workers on biology and genetic population structure of R. kanagurta from different geographical areas revealed the possibility of existence of different stocks (Jones and Silas 1962; Luther 1973; Menezes et al.1993; Jayasankar et al.2004). The stock from Andaman coast for instance differs significantly from the stock at Arabian sea in details of the seasonal breeding cycle. The genetic studies also revealed the occurrence of different stocks in R. kanagurta (Jayasankar et al.2004). Parasites are now increasingly used as indicators for the differentiation of stocks in marine fish (Mckenzie 2002). Although qualitative differences may not exist in the parasite fauna of R.kanagurta from different regions there is a possibility that quantitative differences exist in the occurrence of various species of parasites. For example Rohde (1989) provided data on the prevalence of monogenean species on R. kanagurta off the coast of Penang and a comparison with the present data collected at Bay of Bengal, revealed that the prevalence of infection with various monogeneans at Penang is very low (Rohde 1989) as compared to the situation prevailing in the present locality. The data suggests that the monogeneans are better adapted to warm tropical waters of Bay of Bengal. A detailed study of the parasite fauna of this fish from different geographical areas would be expected to provide valuable information.

Acknowledgement

References