Parasitism of Pennella instructa on indo-pacific sailfish Istiophorus platypterus and its commensality relation with goose barnacle, Conchoderma virgatum along Eastern Arabian Sea

Introduction

Global reports of Pennella (Copepoda: Siphonostomatoida: Pennellidae) infestations include pelagic fishes, cephalopods, marine mammals, and sea turtles, Kabata, 1979 & 1984 [27,28] ; Pascual et al., 1997 [42] ; Morales-Serna et al., 2012 [32] ; Nina et al., 2002 [39] . This parasite infestation primarily affects the muscle tissue of the host, without infiltrating internal organs during its copepodid life stage, also known as a mesoparasitic life stage. The genus Pennella life cycle stages include two naupliar stages, followed by a copepodid stage, then a chalimus stage, and finally an adult stage. Pennella's inseminated females use fish and marine mammals as their second host to produce fertile eggs, which they then release into the water (Garcia et al., 2010; Mugetti et al., 2021) [18,33] . Conchoderma virgatum, an Epibionts pelagic bio fouling organism, attaches itself to a variety of marine species, including sea snakes, sharks (Beckett, 1968) [3] , fish (Nagasawa et al., 2020; Mesaglio et al., 2022) [36,31] , penguins (Nascimento et al., 2010) [37] , whales Minke whale (Lafsdóttir & Shinn, 2013) [41] , sea turtles (Angulo-Lozano et al., 2007) [1] , and whale barnacles (Coronula spp.). It prefers hard substrates or body structures, rough skin, carapace ridges, or epidermal abrasions for attachment, Eckert & Eckert, 1987 [11] ; Beckett, 1968 [3] ; Félix et al., 2006 [14] . Pennella spp. globally host species of the family Istiophoridae (Marlins, Spearfish, and Sailfish), such as Istiophorus platypterus (Causey, 1960) [6] ; Kajikia albida, K. audax (Hernandez-Trujillo, 2014) [21] ; Tetrapturus angustirostris (Ho and Nagasawa, 2001); Makaira mazara (Ho and Nagasawa, 2001) [22] ; and Xiphidae (Swordfish) such as Xiphias gladius, Hogans et al., 1985 [25] ; Castro-Pampillon et al., 2002 [5] ; Tanrikul and Akyol, 2011 [46] . P. instructa was infested with I. platypterus collected from India's south-east and south-west coasts (Devaraj and Bennet, 1972) [10] . Varghese et al., (2009) [50] have reported P. instructa parasitic on I. platypterus from the north-west coast of India. Daniel and Premkumar (1967) [9] reported the occurrence of Conchoderma virgatum on Pennella sp., parasitic on Cypsilurus speculiger. However, Natarajan and Nair (1970) [38] reported an incident of C. virgatum attachment on a copepod parasite, Lernaeenicus hemiramphi Kirtisinghe. Fernando and Ramamoorthy (1974) discovered C. virgatum barnacle parasitism on a scyphozoan medusa, Rhopilema sp., in their umbrella region on the Tranquebar coast of the Bengala Gulf in Tamil Nadu. Lazarus and Sreenivasan (1980) reported the presence of C. virgatum on Pennella diodontis Oken. Pradeep et al., (2016) [43] documented a parasitic infestation of P. instructa on I. platypterus in the Andaman Sea, with C. virgatum attached.

Materials and Methods

Twenty specimens of Indo-Pacific Sailfish I. platypterus were examined from January to December 2023 from the fish landings of Harne, Anandwadi, Mirkarwada, and Sakri Nate fish landing centres on the Ratnagiri coast of Maharashtra, Eastern Arabian Sea. At the fishing landing centers in Harne, Anandwadi, and Sakri Nate-Mirkarwada, fishermen catch sailfish using hook and line, drift gillnet, and purse seine, respectively. Single-day fishing involves hook and line and drift gillnet, whereas multiday fishing uses purse seine (3-4 days). The Harne Fish landing centre practices hook-and-line fishing at a depth of 35 to 60 metres west of the Harne coast. The Anandwadi fish landing centre conducts drift gillnet fishing at a depth of 40 to 50 meters west of the coast. To the west and southwest of their shore, Sakri Nate and Mirkarwada purse seiners practice fishing at depths of 30 to 60 metres. Hook-and-line and drift gillnet fishing methods, which primarily target seer fish, incidentally take sailfish as by catch. Similarly, purse seine fishing targets Indian mackerel and oil sardines, capturing sailfish as by catch. Observed specimens of P. instructa and C. virgatum, preserved them in 5% formalin, and brought 10 specimens of P. instructa and C. virgatum to the laboratory for further analysis. Identifications and morphometric measurements of the specimens (copepod and barnacle) were done by following the studies of Danial and Premkumar (1967) [9] , Yamaguti (1963) [52] , Devaraj and Bennet (1972) [10] , Hastings (1972) [20] , Kabata (1979) [27] , Kabata (1984) [28] , Hogans (1986) [24] , Nagasawa et al. (2020) [36] , and Nascimento et al. (2010) [37] .

Results

The copepod parasite Pennella instructa is visible in various parts of the sailfish's body, mostly in the ventral area. The dorsal side of the body and the caudal peduncle area exhibit some infections. Out of the 20 sailfish specimens, we found 23 specimens of the P. instructa copepod parasite and 14 specimens of Conchoderma virgatum adhering to P. instructa. Between January and December 2023, we found copepod parasites with associated barnacles (C. virgatum) infesting sailfish landings from Harne and Anandwadi fish landing centres. On the other hand, the Mirkarwada and Sakri Nate fish landing centres reported sailfish that had copepod parasite infections but no Conchoderma barnacle attachment. The year 2023 also revealed that these landing centres had year-round copepod parasite infections in their sailfish landings. On the Harne Coast, hook-and-line fishing caught 15% of the sailfish with parasitic P. instructa infestations. Drift gillnet fishing at Anandwadi fish landings reported 19% of the sailfish caught with P. instructa infestation. The fish landings from the Sakri Nate purse seine revealed that 5% of the sailfish catch had P. instructa parasitism. Mirkarwada purse seine accounted for 8% of sailfish landings with P. instructa infections. On sailfish landings in Harne and Anandwadi, C. virgatum's commensality attachment to P. instructa was estimated at 4% and 7%, respectively.

Pennella instructa Wilson C.B., 1917

P. instructa is a hematophagous marine copepod parasite from the family Pennellidae. In the current study, the total length of P. instructa ranged from 38 mm to 114.02 mm. In the majority of cases, thick fibrous cysts form in the host's flesh in the infection area. The parasite had a bulbous cephalosome with two long, unbranched horns on each side that extended posteriorly and parallel to the neck. The horns serve to secure the host. The cephalosome's flat anterior section is partially covered by papillae. The cephalosome and neck are yellow-coloured. The trunk is dark brownish in hue and connects the neck to the abdomen. The abdomen ends with feather-like structures known as plumules. The abdomen bears extended egg strings (Figure 1). The egg strings were yellow-coloured. Morphometric measurements of 10 specimens of P. instructa in this study are shown in Table 1. The photo of P. instructa and its infestation on I. platypterus is shown in Figures 2 and3, respectively.

Conchoderma virgatum Spengler, 1789

Conchoderma virgatum, the striped goose barnacle, of family Lepadidae, subclass Cirripedia was found adherent to P. instructa's trunk in the present study. The total number of barnacle associations per parasite ranged from two to fourteen (Figure 4). The body (capitulum) and base stem (peduncle) meld closely. The capitulum has brown striations on a white background. The parasite attaches itself to the host using an extremely sticky, cement-like material. The barnacle's overall length ranges from 15 mm to 27.5 mm. P. instructa showed no obvious consequences of infestation other than attachment site inflammation by C. virgatum. The photo of C. virgatum attachment on P. instructa is shown in Figures 3 and4.

Seasonal variation

The parasite P. instructa infests Istiophorus platypterus year-round. From April to September, only large P. instructa parasites (over 90 mm) appeared on sailfish. Between October and December, P. instructa, with smaller sizes ranging from 38 mm to 78.9 mm, began to attach to sailfish in a mixed population of both small and large sizes. From February to April, P. instructa attachment on I. platypterus increases in intensity (6 to 14 numbers per sailfish), peaking in April (10 to 14 numbers per sailfish). After that, the density of P. instructa attachment on I. platypterus decreased until January (3 to 5 numbers per sailfish). We observed C. viragatum attachment on P. instructa from February to September 2023, with an increase in its intensity during April and May range from 3 to 14 numbers per parasite. However, there was a complete absence of C. virgatum attachment from October 2023 to January 2024.

Discussions

Fish infections by Pennella sp. or spp. vary across time; in 1983, the highest infection rate in the western North Pacific was over 30%; after 1985, it dropped to less than 1% (Nagasawa et al. 1988; Yamaguchi and Honma 1992) [35,51] . A Pennella pandemic struck in 2012, almost thirty years later, and the infection rates remained somewhat high until 2017 (Suyama et al., 2019) [45] .

In the North Pacific, parasitism was relatively prevalent from May to August (pre-fishing season: May to July; fishing season: August to December), but it never exceeded 10% after September between 2012 and 2015 (Suyama S et al., 2019) [45] . This highlights the importance of monitoring whether such a crisis has originated or is occurring in the waters of the Arabian Sea in Maharashtra in the coming years. Our study shows that the highest incidence of P. instructa on sailfish occurs between April and September. Additionally, we observed that C. virgatum attachment to P. instructa was highest during the months of April and September. The Maharashtra Coast has a lean fishing season from January to May, followed by a peak fishing season from August to November. During the lean fishing season, the occurrence of large size Pennella species parasitism was more prevalent. Penella significantly increases the prevalence of subcutaneous parasite infestations (Speare 1995) [44] . In this investigation, we observed the implanting of the sampled specimen of P. instructa in the subcutaneous tissue of I. platyterus. Numerous authors have documented the high specificity of Pennella spp. with regard to their host spectrum. For instance, studies have demonstrated that Pennella balaenoptera can infect marine mammals such as whales-fin whale, dolphins, porpoises, and pinnipeds (Cicek et al., 2007; Fraija-Fernandez et al., 2018; Marcer et al., 2019; Hogans et al., 1985) [7,17,30,25] . Researchers have found similar reports of Pennella filosa infestations in dolphinfish (Coryphaena hippurus), Indo-Pacific sailfish (Istiophorus platypterus), striped marlin (Kajikia audax), blue marlin (Makaira nigricans), ocean sunfish (Mola mola), Atlantic bluefin tuna (Thunnus thynnus), albacore (T. alalunga), and swordfish (Xiphias gladius). Several Indian coastlines have been found to have P. instructa infestations in Indo-Pacific sailfish (I. platypterus). These include the Andaman Sea (Pradeep et al., 2016) [43] , the North West Coast (Varghese et al., 2009) [50] , the South West Coast (Vizhinjam & Theckhuvadi coast in the Gulf of Mannar), and the South East Coast (Devaraj and Bennet, 1972) [10] . More likely, P. instructa may select I. platypus as their specific host in Indian marine waters. Our study has discovered the occurrence of P. instructa infestation on I. platypterus, as well as the attachment of C. virgatum to P. instructa, from Ratnagiri coast of the Arabian Sea. Globally, sporadically documented Penella species infestations in the deep tissues and internal organs of the host, such as the heart, aorta, blood vessels, ovaries, intestines, and stomach (Suyama et al., 2019; Speare, 1995) [45,44] . In one case, Devaraj and Bennet (1972) [10] documented the presence of P. instructa infestation in the viscera of I. platypterus in Indian waters. Hence, there is a need for a focused research study to investigate the long-term infestation of P. instructa on different body sections of I. platypterus and other marine fish in Indian seas.

C. virgatum is commonly found attached to genus Pennella and other Lernaeid copepods that parasitize fish in the Indian Ocean, Pacific Ocean, Atlantic Ocean, and Mediterranean Sea (Balakrishnan, 1969) [2] . In their 1987 study, Eckert and Eckert determined that the period of barnacle attachment to the copepod can extend beyond 100 days, with a range of 9.5 to 128 days depending on the size of the barnacle. Hernandez-Trujillo et al. (2014) [21] proposed that the infestation of larger P. filosa copepods on Marlin fish might persist for a duration exceeding 4 months. Hence there is need of such studies on the attachment duration of these organisms on sailfish in the Arabian Sea of Indian waters. Members of the Istiophoridae family had a swimming velocity exceeding 100 kilometres per hour. The presence of parasitic copepods and barnacles on fast-swimming sailfish leads to a decrease in their maximum swimming speed (6.5 km/s), requiring more muscular effort and increased energy expenditure. This also results in the weakening of both the swimming muscles and heart muscles of the sailfish (Holts and Bedford, 1990; Block et al., 1992) [26,4] . The presence of Pennella parasites on cultured tuna fish, which causes skin lesions and can lead to bacterial infections by Aeromonas sp., has a negative impact on the economic profitability of commercial fish farming (Toksen et al., 2012; Munday et al., 2003) [47,34] . This also raises concerns regarding food safety. Observations in Indian markets so far revealed that sailfish affected by copepodiasis (Eissa et al., 2012) [12] do not experience a significant decrease in their selling prices compared to non-infested sailfish. This is primarily due to the general public's lack of awareness regarding copepod infestation, the ignorance of infestation by wholesale dealers and marketing channels, the practice of selling sailfish chunks with the skin removed, which hides the infestation and removal of parasite by the fisherfolk at the time of harvest. Estimated average landings of I. platypterus in the Maharashtra coast for five years from 2019 to 2023 were found to be 101.54 t, with the highest in 2019 at 295.66 t (FRAD, CMFRI 2019) and the latest in 2023 at 99.62 t (FRAD, CMFRI 2023). Varghese et al. (2004) estimated the I. platypterus catch rate in the EEZ of the north-western coast of India in the exploratory tuna long lining survey to be 39.42 kg/1000 hooks as by catch that constitutes 15% of the total catch. This shows that I. platypterus fish stock has the potential to contribute economically to the commercial fishing of the north-west coast of India, comprising the Maharashtra and Gujarat coasts, either as by catch or main catch. Hence, it is very essential to study the copepodid parasitism (Pennella sp. or P. instructa) impact on the sailfish resources, with an emphasis on the sailfish recruitment dynamics, mean size, and its potential yield.

Acknowledgments

We acknowledge the ICAR-CMFRI Mumbai Regional Station and Director, ICAR-CMFRI, for their support in providing access to funds for sampling and lab facility utilisation.

Conclusion

This study highlights the significant presence of Pennella instructa and its epibiont Conchoderma virgatum on Indo-Pacific sailfish (Istiophorus platypterus) along the Ratnagiri coast of Maharashtra, Eastern Arabian Sea. The year-round infestation of P. instructa and the seasonal attachment of C. virgatum were notable, with higher rates observed from April to September. These parasitic copepods and barnacles can impact sailfish health and swimming efficiency, potentially affecting commercial fishing yields. The study emphasizes the need for continuous monitoring and focused research on the parasitic dynamics and their implications on marine fisheries, ensuring the sustainability and economic viability of sailfish resources in Indian waters.

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