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. 2014 Nov 25;(457):339–353. doi: 10.3897/zookeys.457.6817

Multiple parasitic crustacean infestation on belonid fish Strongylura strongylura

Panakkool-Thamban Aneesh 1, Kappalli Sudha 1, Ameri Kottarathil Helna 1, Gopinathan Anilkumar 2, Jean-Paul Trilles 3
PMCID: PMC4283380  PMID: 25561846

Abstract Abstract

Simultaneous multiple infestation of parasitic crustacean species involving a cymothoid isopod, Cymothoa frontalis Milne Edward, 1840 and four species of copepods such as Lernanthropus tylosuri Richiardi, 1880, Caligodes lacinatus Kroyer, 1863, Bomolochus bellones Burmeister, 1833 and Dermoergasilus coleus Cressey & Collette, 1970 was frequently noticed on spot-tail needlefish, Strongylura strongylura (Belonidae) captured from the Malabar coast (Kerala, India) during the period from April 2011 to March 2012. All the 43 fishes (Strongylura strongylura) collected, were under the hyper-infection with parasitic crustaceans; a total of 388 parasitic crustaceans including 57 Cymothoa frontalis, 252 Lernanthropus tylosuri, 31 Caligodes lacinatus, 24 Bomolochus bellones and 32 Dermoergasilus coleus were recovered from the host fish. 4 members (9.30%) of host fish were under quadruple parasitism, in two different combinations. Seventeen (39.53%) host fishes showed triple parasitism and 20 (46.51%) members exhibited double parasitism, with four and five parasitic combinations respectively. Remaining two (4.65%) fishes were parasitized only by the copepod, Lernanthropus tylosuri. The infestations by all recovered parasitic crustaceans were highly site specific. The damage caused by the parasitic crustaceans was also discussed.

Keywords: Isopod, Copepod, quadruple parasitism, triple parasitism, double parasitism, Strongylura strongylura

Introduction

Parasitic diseases in fish seriously limit aquaculture production and its economic viability; knowledge of fish parasites, therefore, is an essential requirement for successful aquaculture (Elshahawy and Desouky 2012). Parasitic crustaceans infesting the fishes generates considerable parasitological interest and is of great economic importance inasmuch as it could adversely affect the health of food fishes (Karlsbakk et al. 2001, Johnson et al. 2004, Trilles et al. 2011, 2012, Aneesh et al. 2013a). They feed on the host mucus, tissues and blood and inflict fatal injuries through secondary infection (Margolis et al. 1975, Margolis and Kabata 1988; Oktener and Sezgin 2000). With the increased development of semi-intensive and intensive, freshwater, brackish water and marine aquaculture, the importance of the study of parasitic crustaceans as a major pest has become more evident inviting the attention of many investigators throughout the world (Johnson et al. 1996, 2004, Williams and Williams 1998; Izawa and Choi 2000, Ho et al. 2000, Karlsbakk et al. 2001, Hadfield et al. 2010, 2011, 2013).

Most of the parasitic crustaceans belong to Isopoda, Branchiura and Copepoda (Margolis et al. 1975, Oktener and Sezgin 2000). Cymothoids are oligoxenous isopods and often induce deleterious effects on the host (Overstreet 1978, Kabata 1985, Trilles and Hipeau-Jacquotte 1996, 2012, Aneesh et al. 2013a). Significant proportion of the parasitic copepods is known to be parasitizing fishes (Kabata 1979, Love and Moser 1983, Hogans and Dadswell 1985, Pillai 1985, Benz 1986, Oldewage and Smale 1993, Benz et al. 2003, Cheng et al. 2009, 2011, Ho et al. 2010, El-Rashidy and Boxshall 2010, 2012). Indian fishes have been shown to possess high rate of susceptibility for parasitization by isopods and copepods as well (Pillai 1985, Aneesh et al. 2012, 2013b; Trilles et al. 2011, 2012, Helna et al. 2013, Vijayakumar et al. 2013, Bharadhirajan et al. 2013).

Reports are scanty on the simultaneous occurrence of multiple parasitism involving exclusively parasitic crustaceans. Daniel and Rao (1967) and Daniel and Premkumar (1967) reported the simultaneous infestation of flying fish (Cypselurus speculiger) by a copepod, Pennella sp. and the cirriped, Conchoderma virgatum. Hewitt (1979) and Benz et al. (2003) observed the multiple infestation of Pacific white shark (Carcharodon carcharias) by 5–8 different siphonostomatoid (copepod) species. In India, incidence of double parasitism involving the isopod, Nerocila phaiopleura and the copepod, Lernaeenicus sprattae was reported in anchovy fish, Stolephorus commersonii (Rajkumar et al. 2006). Another Indian fish (Hemiramphus far) also showed simultaneous infestation by the isopod, Mothocya plagulophora and the copepod, Lernaeenicus hemiramphi (Gopalakrishnan et al. 2010). The simultaneous multiple infestations by four parasitic crustacean species on banded needle fish, Strongylura leiura was recently reported by Aneesh et al. (2013b).

The present study reports the frequent occurrence of double and triple parasitism and also the few incidence of quadruple parasitism exclusively by the species of parasitic crustaceans including isopod and copepods on the host fish, Strongylura strongylura (Belonidae) distributed along the Malabar coast (Kerala, India).

Methods

The present study was conducted during the period from April 2011 to March 2012. Living or fresh fishes, Strongylura strongylura were collected from the Ayyikkara fish landing center (Lat. 11°51'N, Long. 75°22'E, Malabar coast, Kerala, India). Soon after collection, the fishes were taken to the laboratory and were examined various parts of the body (such as the general body surface, the lateral line region, base of the pectoral fin, posterio-ventral side, branchial cavity, beak, gill filament, inner wall of the operculum etc.) thoroughly for the presence of parasitic crustaceans using hand lens. Recovered parasitic crustaceans were removed from the host and preserved in 70% ethanol for further detailed examination. The identification was performed, using a dissection microscope and a stereo microscope Leica-S6D, according to Milne Edwards (1840), Cressey and Collette (1970) and Pillai (1985). The (P) and mean (I) was calculated according to Margolis et al. (1982) and Bush et al. (1997). The host nomenclature and fish taxonomy were done according to Fish Base (Froese and Pauly 2013).

Voucher specimens of all parasites, collected by Aneesh, Helna and Sudha, from the fish, Strongylura strongylura, were deposited in the Parasitic Crustacean Museum, Crustacean Biology Research Laboratory, Sree Narayana College, Kannur, Kerala, India. Abbreviations used: PCM; LT.

Cymothoa frontalis (Milne Edward, 1840): Juvenile (LT. 8 mm) (PCM N° CF-07),13 April 2011; Transitional (LT. 20mm) (PCM N° CF-08), 25 April 2011; ovigerous female (LT. 26 mm) with manca larva in the brood pouch (PCM N° CF-09 ), 12 July 2011; 30 Manca larva released by the specimen PCM N° CF-09 (3.4 mm), (PCM N° CF-10), 12 July 2011; Male (LT. 13 mm) (PCM N° CF-14), 08 January 2012.

Caligodes lacinatus (Kroyer, 1863): Ovigerous female (LT, 10.3 mm) with egg sac (PCM N° Cl-09), 07 May 2011; ovigerous female (LT, 6 mm) without egg sac (PCM N° Cl-13), 23 July 2011.

Lernanthropus tylosuri Richiardi, 1880: Ovigerous female (LT, 5.5 mm) with egg sac (PCM N° Lt-01), 07 May 2011; ovigerous female (LT, 5.5 mm) without egg sac and a male (LT, 1.8 mm) clinging on Ovigerous female (PCM N° Lt-13), 23 March 2012.

Bomolochus bellones Burmeister, 1833: Ovigerous female (LT, 1.9 mm) with egg sac (PCM N° Bb-09), 18 June 2011; ovigerous female (LT, 1.8 mm) with egg sac (PCM N° Bb-11), 23 June 2011; ovigerous female (LT, 1.4 mm) without egg sac (PCM N° Bb-12), 23 June 2011.

Dermoergasilus coleus (Cressey & Collette, 1970): Ovigerous female (LT, 0.6 mm) with egg sac (PCM N° Dc-05), 19 July 2011; ovigerous female (LT, 0.5 mm) without egg sac (PCM N° Dc-12), 19 January 2012.

Results

Forty three Strongylura strongylura (Fig. 1A) collected during April 2011 to March 2012, were found to be infested with five species of parasitic crustaceans. Recovered parasitic crustaceans were identified as cymothoid isopod, Cymothoa frontalis (Milne Edward, 1840) and four copepods (such as Lernanthropus tylosuri Richiardi, 1880, Caligodes lacinatus Kroyer, 1863, Bomolochus bellones Burmeister, 1833 and Dermoergasilus coleus (Cressey & Collette, 1970) (Tables 1, 2 and 3) (Figs 1B–I).

Figure 1.

Figure 1.

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A Host fish Strongylura strongylura B–E Cymothoa frontalis B male C transitional D female E juvenile F Lernanthropus tylosuri – female G Bomolochus bellones – female H Caligodes lacinatus – female I Dermoergasilus coleus.

Table 1.

Multiple parasitism by crustaceans on Strongylura strongylura.

Month Host fish series Number of Parasitic Crustaceans Remarks
Isopod Copepods
Cymothoa frontalis Lernanthropus tylosuri Caligodes lacinatus Bomolochus bellones Dermoergasilus coleus
Female Male Female Male Female Male Female Male Female Male
April
2011		 1 1 1 12 3 1 - - - - - Triple
2 1 1 7 1 - - 2 - - - Triple
3 1 1 - - - - 1 - - - Double
4 1 - 4 1 - - - - - - Double
5 - - 4 - 2 - - - - - Double
May
2011		 6 - - 8 - - - 1 - - - Double
7 1 - 4 - - - - - - - Double
8 1** 1** - - 2 - - - - - Double
June
2011		 9 1 1 11 2 2 - - - - - Triple
10 - - 4 - - - - - - - Single
11 1 1 - - - - 2 - - - Double
12 1 - 3 - - - - - - - Double
July
2011		 13 1** 1** 9 9 2 - - - - - Triple
14 1 1 - - - - 1 - - - Double
15 - - 3 3 - - - - - - Single
Aug
2011		 16 1* 1 - - 2 - 2 - 4 - Quadruple
17 1 1 5 1 - - - - - - Double
18 - - 10 - 1 - - - - - Double
19 1 - 8 - - 1 4 Quadruple
20 - - 6 1 2 - - - - - Double
21 1 1 4 - - - - - - - Double
September
2011		 22 1 1 9 2 - - 2 - - - Triple
23 1* 1 3 - 2 - - - - - Triple
October
2011		 24 - - 9 - 1 - - - 3 - Triple
25 1 1 7 - - - - - 3 - Triple
26 1 1 2 1 - - 1 - - - Triple
November
2011		 27 - - 11 2 2 - - - - - Double
28 1 - 2 - - - 2 - - - Triple
29 1 1 6 - - - - - - - Double
December
2011		 30 1 1 7 - 2 - - - - - Triple
31 1 - 3 - - - 2 - - - Triple
32 1** 1** 8 2 2 - - - - - Triple
33 1 1 - - 2 - 1 - 3 - Quadruple
January
2012		 34 1 1 - - 2 - - - - - Double
35 1* - 7 2 - - - - 3 - Triple
36 - - 5 - - - 2 - - - Double
February
2012		 37 - - 4 - 2 - - - - - Double
38 1 1 12 4 - - - - 2 - Triple
39 1* 1 - - - - - 2 - - Double
40 1 1 3 - - - - - 4 - Triple
March
2012		 41 - - 9 - 2 - - - - - Double
42 1** 1** 5 - - - 2 - 4 - Quadruple
43 1 1 4 - - - - - 2 - Triple
43 24
** - 4
* - 4		 21
** - 4		 218 34
 29 0 23 0 29
 0 Single – 2 Double – 20
Triple – 17 Multiple – 4
32(57)
* – Transitional stage = 4
** – Juvenile = 8		 35 (252) 17(31) 15(24) 10(32)
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Table 2.

Parasitological index of the parasitic crustaceans on Strongylura strongylura under multiple parasitism.

Parasites Prevalence and Intensity Site of infestation
Cymothoa frontalis Milne Edward, 1840 74.42; 1.78 floor of the buccal cavity
Lernanthropus tylosuri Richard, 1880 81.4; 7.2 on the gill filament
Caligodes lacinatus Kroyer, 1863 39.53; 1.82 penetrating the fleshy part of the lower beak
Bomolochus bellones Burmeister 1835 34.88; 1.6 attached on the inner side of the operculum
Dermoergasilus coleus (Cressey in Cressey & Collette, 1970) 23.26; 3.2 on the gill filament
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Table 3.

Different parasitic combinations of multiple parasitism.

NFO Single Parasitism Double Parasitism Triple Parasitism Quadruple Parasitism
L CL CCl CB LCl LB CLCl CLB CLD LClD CLBD CClBD
43 2 6 3 3 5 3 6 5 5 1 2 2
Total – 20 Total – 17 Total – 4
Total: 43
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(Legends: CL – Cymothoa frontalis and Lernanthropus tylosuri; CCl – Cymothoa frontalis and Caligodes lacinatus; CB – Cymothoa frontalis and Bomolochus bellones; LCl – Lernanthropus tylosuri and Caligodes lacinatus; LB – Lernanthropus tylosuri and Bomolochus bellones; CLCl – Cymothoa frontalis, Lernanthropus tylosuri and Caligodes lacinatus; CLB – Cymothoa frontalis, Lernanthropus tylosuri and Bomolochus bellones; CLD – Cymothoa frontalis, Lernanthropus tylosuri and Dermoergasilus coleus; LClD – Lernanthropus tylosuri, Caligodes lacinatus and Dermoergasilus coleus; CLBD – Cymothoa frontalis, Lernanthropus tylosuri, Bomolochus bellones and Dermoergasilus coleus; CClBD – Cymothoa frontalis, Caligodes lacinatus, Bomolochus bellones and Dermoergasilus coleus)

Among the five parasitic crustaceans recovered from Strongylura strongylura, the Lernanthropus tylosuri exhibited highest prevalence (81.4%); out of 43 fish (Strongylura strongylura) observed 35 member were found to be infested with this lernanthropid copepod (Figs 1F and 2A). A total of 252 (218 females and 34 males) members of Lernanthropus tylosuri were recovered from 35 infested fishes and the intensity being 7.2 (Table 2). All females were reproductively active, evidenced by the presence of growing ovaries and/or egg sacs. The recovered males were not independent, but found to be in a clinging/copulatory position, attaching the genital segment of the females with their maxilliped. Lernanthropus tylosuri shows strict site specificity by infesting only the gill filament of the host.

Figure 2.

Figure 2.

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A Simultaneous occurrence of parasitic crustaceans (Cymothoa frontalis, Lernanthropus tylosuri, Caligodes lacinatus and Bomolochus bellones, Dermoergasilus coleus) parasitizing the fish Strongylura strongylura B Levels of single, double, triple and quadruple crustacean parasitism on the fish Strongylura strongylura C Double parasitism on the fish Strongylura strongylura – different combinations is represented in percentage D Triple parasitism on the fish Strongylura strongylura – different combinations is represented in percentage E Quadruple parasitism on the fish Strongylura strongylura – different combinations is represented in percentage. Legends: CL – Cymothoa frontalis and Lernanthropus tylosuri; CCl – Cymothoa frontalis and Caligodes lacinatus; CB – Cymothoa frontalis and Bomolochus bellones; LCl – Lernanthropus tylosuri and Caligodes lacinatus; LB – Lernanthropus tylosuri and Bomolochus bellones; CLCl – Cymothoa frontalis, Lernanthropus tylosuri and Caligodes lacinatus; CLB – Cymothoa frontalis, Lernanthropus tylosuri and Bomolochus bellones; CLD – Cymothoa frontalis, Lernanthropus tylosuri and Dermoergasilus coleus; LClD – Lernanthropus tylosuri, Caligodes lacinatus and Dermoergasilus coleus; CLBD – Cymothoa frontalis, Lernanthropus tylosuri, Bomolochus bellones and Dermoergasilus coleus; CClBD – Cymothoa frontalis, Caligodes lacinatus, Bomolochus bellones and Dermoergasilus coleus.

Among the recovered parasitic crustacean species, the isopod Cymothoa frontalis exhibited the second highest prevalence (74.42%) (Table 2; Figs 1B–E and 2A) by infesting 32 (out of 43) host fishes (Strongylura strongylura); the intensity being equal to 1.78 (Table 2). Of 57 members of Cymothoa frontalis, there were 21 males and 24 females, 8 juveniles and the remaining 4 were under the transitional phase. Fifty members of this cymothoid parasite were appeared in pairs with three different combinations during their infestation on the fish (Strongylura strongylura) such as male–female (18+18=36), juvenile–juvenile (4+4=8) and male–transitional stage (3+3=6); invariably, member in the pair being settled at the floor of either of the branchial cavity of the host fish. The remaining unpaired 7 (57–50) members of Cymothoa frontalis, including 6 females and one transitional stage were also found to be settled the specific site (floor of the host buccal cavity).

The copepod species, Caligodes lacinatus was collected from 17 out of 43 Strongylura strongylura examined; the prevalence being 39.53%. A total of 31 parasites were recovered from the infested host fishes, the intensity being equal to 1.82 (Table 2; Figs 1H and 2A). All the recovered members of this parasite were exclusively females carrying growing ovaries and egg sacs as well. Caligodes lacinatus was found to penetrate the fleshy part of the lower beak of the host fish; swelling and tissue damages were frequently observed at the penetration site.

Fifteen of 43 Strongylura strongylura examined were also infested by 24 members of the copepod Bomolochus bellones. The prevalence and intensity reach 34.88% and 1.6 respectively (Table 2; Figs 1G and 2A). All specimens were females and reproductively active by possessing egg sacs or maturing ovaries. The inner side of the operculum forms the specific site for the attachment of this species.

Dermoergasilus coleus showed the lowest prevalence (23.26%), only 10 of the 43 Strongylura strongylura examined being infested; 32 parasites were recovered from the gill filament of infested host fishes, the intensity being equal to 3.2 (Table 2; Figs 1I and 2A). All females were reproductively active possessing growing ovaries and/or egg sacs. Dermoergasilus coleus also showed strict site specificity by infesting only the gill filament of the fish. The infestation of Dermoergasilus coleus is found to be restricted to certain months (August, October and December–March) only.

Interestingly, the host fish (Strongylura strongylura) was under frequent and simultaneous multi infestation (quadruple/triple/double) by any four/three/two of these five parasitic crustaceans (Cymothoa frontalis, Lernanthropus tylosuri, Caligodes lacinatus, Bomolochus bellones and Dermoergasilus coleus) throughout the study period (April 2011 to March 2012) (Table 1; Fig. 2B–E).

Quadruple parasitism

Approximately 9% of the observed (4 out of 43) fishes showed the presence of quadruple parasitism, being simultaneously infested by any of the four species of parasitic crustaceans in two different combinations (1. Cymothoa frontalis, Lernanthropus tylosuri, Bomolochus bellones and Dermoergasilus coleus (CLBD) (50%; 2 out of 4) and 2. Cymothoa frontalis, Caligodes lacinatus, Bomolochus bellones and Dermoergasilus coleus (CClBD) (50%; 2 out of 4)) only during the months of August, December and March (Tables 1 and 3; Fig. 2B and E).

Triple parasitism

Seventeen (out of 43; 39.53%) members of Strongylura strongylura showed triple parasitism by simultaneous infestation by any of the three parasitic crustacean species in following four possible combinations: 1) Cymothoa frontalis, Lernanthropus tylosuri and Caligodes lacinatus (CLCl), 2) Cymothoa frontalis, Lernanthropus tylosuri and Bomolochus bellones (CLB), 3) Cymothoa frontalis, Lernanthropus tylosuri and Dermoergasilus coleus (CLD) and 4) Lernanthropus tylosuri, Caligodes lacinatus and Dermoergasilus coleus (LClD). The rates of these combinations were 35.29% (CLCl), 29.41% (CLB), 29.41% (CLD) and 5.88% (LClD) respectively (Tables 1 and 3; Fig. 2B and D). Instances of triple parasitism were observed throughout the study period except May and August (Table 1).

Double parasitism

The instance of double parasitism in Strongylura strongylura was relatively high. Twenty (out of 43; 46.51%) members of the host fish were under simultaneous infestation with any of the two crustacean species. Five possible combinations of double parasitism were detected 1) Cymothoa frontalis and Lernanthropus tylosuri (CL), 2) Cymothoa frontalis and Caligodes lacinatus (CCl) 3) Cymothoa frontalis and Bomolochus bellones (CB) 4) Lernanthropus tylosuri and Caligodes lacinatus (LCl), 5) Lernanthropus tylosuri and Bomolochus bellones (LB). CL and LCl combinations were found to be significantly high amounting 30% and 25% respectively. The percentage of CCl, CB and LB combinations were found to be equal (15% each) (Table 3; Figs 2B and C). No incidence of double parasitism was noticed in September, October and December (Table 1).

Single parasitism

Unlike triple and double parasitism noticed in the studied host fish Strongylura strongylura, infestation with only one species of parasitic crustacean (single parasitism) was uncommon during the entire study period; only two fishes (out of 43; 4.65%) showed single parasitism with Lernanthropus tylosuri, one in June and other in July (Tables 1 and 3; Fig. 2B).

Discussion

The present study revealed that the spot tail needle fish, Strongylura strongylura is a potential host for accommodating five parasitic crustacean species. 396 parasitic crustaceans including 57 cymothoid isopod (Cymothoa frontalis) and 339 copepods (252 Lernanthropus tylosuri, 31 Caligodes lacinatus, 24 Bomolochus bellones and 32 Dermoergasilus coleus) were recovered from 43 examined fish, Strongylura strongylura. The highest prevalence (P = 81.4%) was exhibited by the copepod, Lernanthropus tylosuri throughout the study period. The parasitic cymothoid, Cymothoa frontalis was recovered from 32 (P = 74.42%) host fishes (Strongylura strongylura). The parasitic copepod, Caligodes lacinatus was collected from 17 host fishes, its prevalence being 39.53%. The prevalence of Bomolochus bellones, infesting only 15 of 43 examined fishes, being 34.88 %. Dermoergasilus coleus parasitizing 10 Strongylura strongylura exhibited lowest prevalence (23.26%). The mean intensity vary according to the parasitic species. The highest intensity was observed in Lernanthropus tylosuri (I = 7.2), the second highest intensity was exhibited by Dermoergasilus coleus (I = 3.2). Caligodes lacinatus and Cymothoa frontalis have an intensity reaching 1.82 and 1.78 respectively. The lowest intensity was observed in Bomolochus bellones (1.6). Among the four copepod species recovered during the present study, the species such as Lernanthropus tylosuri, Caligodes lacinatus and Bomolochus bellones were also reported to be the members in simultaneous multiple infestation on Strongylura leiura (Aneesh et al. 2013b). But the intensity and prevalence of Lernanthropus tylosuri is found to be higher in Strongylura strongylura than Strongylura leiura, suggesting that Strongylura strongylura is a more suitable host fish for Lernanthropus tylosuri. The prevalence of Caligodes lacinatus, on the other hand, found to be very low in the present host (Strongylura strongylura). The prevalence and intensity of Bomolochus bellones was found to be more or less equal in both fishes, Strongylura strongylura (present study) and Strongylura leiura (Aneesh et al. 2013b).

Interestingly, these five parasitic crustaceans showed site specific attachment, apparently for avoiding the inter-parasitic competition for space and food. The blood feeding parasite, Cymothoa frontalis, prefers floor of the buccal cavity and the copepods, Lernanthropus tylosuri and Dermoergasilus coleus, prefer the gill filament for their infestation. On the other hand, the tissue feeding, Caligodes lacinatus penetrates the tissue lining of the lower beak and Bomolochus bellones clings the operculum. The site specific attachment of parasitic crustaceans involved in the simultaneous infestation was also reported in the previous study on Strongylura leiura from which Lernanthropus tylosuri, Caligodes lacinatus and Bomolochus bellones were recovered from the gill filament, the tissue lining of the lower beak and the operculum respectively of the host fish (Strongylura leiura) (Aneesh et al. 2013b), suggesting that the site of attachment of parasitic copepods is highly specific even though their hosts are different.

In the present study, all the collected parasitic copepods belonging to the species, Caligodes lacinatus (31) and Bomolochus bellones (24) and Dermoergasilus coleus (32), were invariably matured females carrying egg sac. No single instance of parasitization was noticed by male members of these copepod species (Caligodes lacinatus, Bomolochus bellones and Dermoergasilus coleus) apparently due to the existence of sex specific parasitization. Like in Strongylura leiura, 34 out of 252 members of recovered copepod species of Lernanthropus tylosuri were males, clinging the genital segments of their parasitic females, apparently in copulatory position. Reports show that only reproductively mature female copepods are parasitic and the males dye after copulation (Jithendran et al. 2008).

Despite the few reports on double parasitism, our knowledge on the occurrence of simultaneous multiple parasitism involving crustaceans is very poor. The occurrence of double parasitism with a copepod, Pennella sp. and a cirriped, Conchoderma virgatum was reported from the flying fish, Cypselurus speculiger (Daniel and Premkumar 1967). The simultaneous infestation of Nerocila phaiopleura and the copepod, Lernaeenicus sprattae on the engraulidaen fish Stolephorus commersonii was reported from Parangipettai (India) (Rajkumar et al. 2006). Double parasitism with the isopod, Mothocya plagulophora and the copepod, Lernaeenicus hemiramphi was noticed in Hemiramphus far (Gopalakrishnan et al. 2010). Daniel and Rao (1967) reported the parasitization of the flying fish by isopod, copepod and cirriped. Recently from our laboratory, the occurrence of double, triple and quadruple parasitism with an isopod Mothocya renardi and three copepods such as Lernanthropus tylosuri, Caligodes lacinatus and Bomolochus bellones was reported in the banded needle fish. In the present study, 46.51% (20 out of 43) members of fish, Strongylura strongylura showed the occurrence of double parasitism involving one isopod and four copepods in five different combinations. The degree of the occurrence of the combinations Cymothoa frontalis and Lernanthropus tylosuri (CL) (30%; 6 out of 20), Lernanthropus tylosuri and Caligodes lacinatus (LCl) (25 %; 5 out of 20) and remaining three combinations, Cymothoa frontalis and Caligodes lacinatus (CCl), Cymothoa frontalis and Bomolochus bellones (CB) and Lernanthropus tylosuri and Bomolochus bellones (LB) 15 % each. In three combinations (CL, LCl and LB), the copepod, Lernanthropus tylosuri was found to be common; similarly the isopod, Cymothoa frontalis was the common member in the combinations such as CL, CCl and CB, signifying its high rate of infestation on the host. In two double parasitic combinations (LCl and LB), all members are copepods.

Apart from previous report from our laboratory, no further information is available on triple parasitism by crustaceans. The present study revealed that 17 members (39.5%) of Strongylura strongylura had been under triple parasitism with crustacean species. Out of four combinations (CLCl, CLB, CLD and LClD) noticed in the triple parasitism, CLCl (Cymothoa frontalis, Lernanthropus tylosuri and Caligodes lacinatus) scored the highest percentage (35.29) (Tables 1 and 3). Interestingly, the existence of quadruple parasitism being simultaneously infested by any of the four species of parasitic crustaceans in two different combinations on the fish, Strongylura strongylura was also exposed through the present study. However, its frequency was relatively less (9%) occurring only during the months of August, December and March (Tables 1 and 3; Figs 2B and E). The isopod, Cymothoa frontalis and copepods, Bomolochus bellones and Dermoergasilus coleus are found to be the common members in two combinations.

Interestingly, Lernanthropus tylosuri appears as a common parasitic crustacean species infesting Strongylura strongylura irrespective of the type of parasitism (single, double, triple and quadruple parasitism) involved.

Parasitic crustaceans have negative impacts on their host fishes; their attachment and feeding activities are responsible for any primary diseases that develop due to parasitization (Bharadhirajan et al. 2013). As previously reported in Strongylura leiura, the present study, also helped us to identify severe damages induced to the floor of the buccal cavity, the gill filament, the fleshy part of the lower beak, and the inner side of the operculum of the host (Strongylura strongylura). Reports showed that, the infestation by parasitic copepods and isopods induce bacterial and viral diseases in parasitized fishes (Nigrelli 1950, Cusack and Cone 1985, Simudu and Tsummoto 1985, Ravichandran et al. 2001, Ravichandran and Ajithkumar 2008). Recent study showed that, the host (Stolephorus leptolepis) tissues infected by Nerocila depressa were vigorous with disrupted epidermis, damaged muscle fibers and demised collagen matrix; at the pereopod attachment sites, healthy tissues were absent and infested tissues appear to be deteriorated (Rameshkumar and Ravichandran 2013).

In conclusion, the spot-tail needlefish, Strongylura strongylura is a potential host for five parasitic crustacean species which showed site specific attachment, may be for avoiding the inter-parasitic competition for space and food. No single instance of parasitization was noticed by male members of these copepod species signifying female specific parasitization. The frequent occurrence of double and triple parasitism and few instance of quadruple parasitism (at the ratio 5:4:1) by parasitic crustaceans noticed on the fish Strongylura strongylura indicate that it is not an accidental incident. The multi infestation observed in the present study probably leads the high levels of secondary infections and more studies on this aspect is highly warranted.

Acknowledgments

Authors gratefully acknowledge University Grants Commission, New Delhi (F.No:38-218/2009(SR); dated: 24/12/2009) and Kerala State Council for Science Technology and Environment, Government of Kerala (No. (T) 093/SRS/2011/CSTE; dated: 25/06/2011) for financial support to carry out this work.

Citation

Aneesh P-T, Sudha K, Helna AK, Anilkumar G, Trilles J-P (2014) Multiple parasitic crustacean infestation on belonid fish Strongylura strongylura. In: Wehrtmann IS, Bauer RT (Eds) Proceedings of the Summer Meeting of the Crustacean Society and the Latin American Association of Carcinology, Costa Rica, July 2013. ZooKeys 457: 339–353. doi: 10.3897/zookeys.457.6817

References

  1. Aneesh PT, Helna AK, Sudha K, Arshad K, Anilkumar G. (2012) Diversity of Parasitic copepods infesting the Fishes of Malabar. In: Proceedings of National Seminar on Faunal Diversity of Kerala, 23–24 march, 2012, PRNS College, Mattanoor, Kannur, India, 94–95. [Google Scholar]
  2. Aneesh PT, Sudha K, Arshad K, Anilkumar G, Trilles JP. (2013a) Seasonal fluctuation of the prevalence of cymothoids representing the genus Nerocila (Crustacea, Isopoda), parasitizing commercially exploited marine fishes from the Malabar Coast, India. Acta Parasitologica 58(1): 80–90. doi: 10.2478/s11686-013-0112-3 [DOI] [PubMed] [Google Scholar]
  3. Aneesh PT, Sudha K, Helna AK, Arshad K, Anilkumar G, Trilles JP. (2013b) Simultaneous multiple parasitic crustacean infestation on banded needlefish, Strongylura leiura (Belonidae) from the Malabar Coast, India. International Journal of Scientific and Research Publications 3(7): 367–375. [Google Scholar]
  4. Benz GW. (1986) Distributions of siphonostomatoid copepods parasitic upon large pelagic sharks in the western North At1antic. Syllogeus 58: 211–219. [Google Scholar]
  5. Benz GW, Mollet HF, Ebert DA, Davis CR, Van Sommeran SR. (2003) Five Species of Parasitic Copepods (Siphonostomatoida: Pandaridae) from the Body Surface of a White Shark Captured in Morro Bay, California. Pacific Science 57(1): 39–43. doi: 10.1353/psc.2003.0002 [Google Scholar]
  6. Bharadhirajan P, Gopalakrishnan A, Raja K, Murugan S, Vijayakumar R, Rahman MM. (2013) Prevalence of copepod parasite (Lernaeenicus polynemi) infestation on Eleutheronema tetradactylum from Pazhayar coastal waters, southeast coast of India. Journal of Coastal Life Medicine 1(4): 258–261. [Google Scholar]
  7. Bunkley-Williams L, Jr Williams EH. (1998) Pugheadedness in a largemouth bass/Florida largemouth bass hybrid from Puerto Rico: The fifth record in largemouth basses. Caribbean Journal of Science 34: 318–320. [Google Scholar]
  8. Bush AO, Lafferty KD, Lotz JM, Shostak AW. (1997) Parasitology meets ecology on its own terms. Margolis et al. revised. Journal of Parasitology 83: 575–583. doi: 10.2307/3284227 [PubMed] [Google Scholar]
  9. Cheng YR, Ho JS, Dai CF. (2009) Orstomella yaliuensis n. sp., a xarifiid copepod (Crustacea) parasitic in the polyps of hump coral Porites lutea Milne Edwards & Haime off Taiwan. Systematic Parasitology 74: 17–21. [DOI] [PubMed] [Google Scholar]
  10. Cheng YR, Ho JS, Dai CF. (2011) Four new xarifiid copepods (Poecilostomatoida) associated with the scleractinian coral Pavona explanulata (Lamarck) from off Taiwan. Systematic Parasitology 79: 227–240. doi: 10.1007/s11230-009-9188-4 [DOI] [PubMed] [Google Scholar]
  11. Cusack R, Cone DK. (1985) A report of bacterial microcolonies on the surface of Gyrodactylus (Monogenea). Journal of Fish Diseases 8: 125–127. doi: 10.1111/j.1365-2761.1985.tb01193.x [Google Scholar]
  12. Daniel A, Premkumar VK. (1967) Pedunculate cirripedes, Conchoderma virgatum (Splengler) attached to a pennellid copepod, Pennella sp. parasitic on a flying fish Cypselurus (Hirundichthys) speculiger (Cuv. and Val.). Journal of Bombay Natural History Society 64: 132. [Google Scholar]
  13. Daniel A, Rama Rao KV. (1967) Notes on animal relationships: A flying fish parasitised by an isopod, and a copepod associated with an inquiline cirripede. Current Science 36: 641. [Google Scholar]
  14. El-Rashidy HH, Boxshall GA. (2010) Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Systematic Parasitology 76: 19–38. doi: 10.1007/s11230-010-9230-6 [DOI] [PubMed] [Google Scholar]
  15. El-Rashidy HH, Boxshall GA. (2012) A new copepod (Siphonostomatoida:Lernanthropidae) parasitic on a Red Sea immigrant dragonet (Actinopterygii: Callionymidae), with a review of records of parasitic copepods from dragonets. Systematic Parasitology 81: 87–96. doi: 10.1007/s11230-011-9326-7 [DOI] [PubMed] [Google Scholar]
  16. Elshahawy IS, Desouky AY. (2012) First record of Mothocya melanosticta Schioedte and Meinert, 1884 (Isopoda: Cymothoidae) from Egyptian pinecone soldier fish with special reference to its infestation status. Turkish Journal of Veterinary and Animal Sciences 36(6): 577–584. [Google Scholar]
  17. Froese R, Pauly D. (2013) FishBase. World Wide Web electronic publication. Available from: http://www.Fishbase.org, Version (January 2013).
  18. Gopalakrishnan A, Rajkumar M, Sun Jun, Trilles JP. (2010) Occurrence of double parasitism on black-barred halfbeak fish from the southeast coast of India. Chinese Journal of Oceanology and Limnology 28(4): 832–835. doi: 10.1007/s00343-010-9919-z [Google Scholar]
  19. Hadfield KA, Bruce NL, Smit NJ. (2010) Redescription of the monotypic genus Cinusa Schioedte and Meinert, 1884 (Isopoda, Cymothoidae), a buccal-cavity isopod from South Africa. Zootaxa 2437: 51–68. [Google Scholar]
  20. Hadfield KA, Bruce NL, Smit NJ. (2011) Cymothoa hermani sp. nov. (Isopoda, Cymothoidae, Crustacea), a parasitic isopod, collected off the Zanzibar coast,Tanzania from the mouth of a parrotfish (Scaridae). Zootaxa 2876: 57–68. [Google Scholar]
  21. Hadfield KA, Bruce NL, Smit NJ. (2013) Review of the fish-parasitic genus Cymothoa Fabricius 1793 (Isopoda, Cymothoidae, Crustacea), from the southwestern Indian Ocean, including a new species from South Africa. Zootaxa 3640: 152–176. doi: 10.11646/zootaxa.3640.2.2 [DOI] [PubMed] [Google Scholar]
  22. Helna AK, Aneesh PT, Arshad K, Sudha K. (2013) Occurrence of Caligus sp. a parasitic Copypod (Crustacea) infesting the commercially exploited fishes along the Malabar cost. Journal of Basic and Applied Biology 7(3): 28–30 [Google Scholar]
  23. Hewitt GC. (1979) Eight species of parasitic copepods on a white shark. New Zealand Journal of Marine and Freshwater Research 13: 171. doi: 10.1080/00288330.1979.9515790 [Google Scholar]
  24. Ho JS, Cheng YR, Dai CF. (2010) Hastatus faviae n. gen., n. sp., a xarifiid copepod parasitic in the honeycomb coral of Taiwan. Crustaceana 83: 89–99. doi: 10.1163/001121609X12511103974574 [Google Scholar]
  25. Ho JS, Lin CL, Chen SN. (2000) Species of Caligus Müller, 1785 (Copepoda: Caligidae) parasitic on marine fishes of Taiwan. Systematic Parasitology 46: 159–179. doi: 10.1023/A:1006342120411 [DOI] [PubMed] [Google Scholar]
  26. Hogans WE, Dadswell MJ. (1985) Parasitic copepods of the white shark (Carcharodon carcharius L.) from the Bay of Fundy. Canadian Journal of Zoology 63: 740–741. doi: 10.1139/z85-106 [Google Scholar]
  27. Izawa K, Choi KH. (2000) Redescription of Caligus latigenitalis Shiino, 1954 (Copepod, Siphonostomatoida, Caligidae), parasitic on Japanese black sea bream, Acanthopagrus schlegeli (Bleeker, 1854). Crustaceana 73: 995–1005. doi: 10.1163/156854000505047 [Google Scholar]
  28. Jithendran KP, Natarajan M, Azad IS. (2008) Crustacean parasites and their management in brackishwater finfish culture. Marine Finfish Aquaculture Network, 47–50.
  29. Johnson SC, Blaylock RB, Elphick J, Hyatt K. (1996) Disease caused by the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) in wild sockeye salmon (Oncorhynchus nerka) stocks of Alberni Inlet, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 53: 2888–2897. [Google Scholar]
  30. Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z. (2004) A review of the impact of parasitic copepods on marine aquaculture. Zoological Studies 43: 229–243. [Google Scholar]
  31. Kabata Z. (1979) Parasitic Copepoda of British fishes. The Ray Society, London. [Google Scholar]
  32. Kabata Z. (1985) Parasites and Disease of Fish Cultured in the Tropics. Isopoda. Taylor and Francis, London, 265–271. [Google Scholar]
  33. Karlsbakk E, Otterlei E, Hoie H, Nylund A. (2001) Parasites of cultured cod (Gadus morhua) postlarvae fed natural zooplankton. Bulletin of European Association of Fish Pathologist 21: 63–70. [Google Scholar]
  34. Love MS, Moser M. (1983) A Checklist of Parasites of California, Oregon, and Washington Marine and Estuarine Fishes. NOAA Tech. Rep. NMFS SSRF-777.
  35. Margolis L, Kabata Z, Parker RR. (1975) Catalogue and synopsis of Caligus, a genus of Copepoda (Crustacea) parasitic on fishes. Bulletin of the Fisheries Research Board of Canada 192: 1–117. [Google Scholar]
  36. Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA. (1982) The use of ecological terms in parasitology (Report of an ad hoc Committee of the American Society of Parasitologists). Journal of Parasitology 68: 131–133. doi: 10.2307/3281335 [Google Scholar]
  37. Milne Edwards H. (1840) Histoire Naturelle des Crustacés comprenant l.anatomie, la physiologie et la classification de ces animaux. Vol. III Librairie Encyclopédique de Roret, Paris. [Google Scholar]
  38. Nigrelli RE. (1950) Lympocytis disease and Ergasilid parasites in fishes. Journal of Parasitology 36: 36. [Google Scholar]
  39. Oktener A, Sezgin MB. (2000) Mothocya epimerica Costa (1851) (Flabellifera: Cymothoidae), an isopod Parasie in the branchial cavities of the Black Sea Silverfish Atherina boyeri Risso, 1810. Journal of Turkish Marine Science 6: 23–29. [Google Scholar]
  40. Oldewage WH, Smale MJ. (1993) Occurrence of piscine parasitic copepods (Crustacea) on sharks taken mainly off Cape Recife, South Africa. South African Journal of Marine Sciences 13: 309–312. doi: 10.2989/025776193784287310
  41. Overstreet RM. (1978) Marine Maladies Worms Germs and Other Symbionts from the Northern Gulf of Mexoci Mississippi, Alabama Sea. Grant Consortium, 140 pp. [Google Scholar]
  42. Pillai NK. (1985) The Fauna of India: Copepod Parasites of Marine Fishes. Zoological Survey of India, Calcutta. [Google Scholar]
  43. Rajkumar M, Perumal P, Trilles JP. (2006) A note on the double parasitism (Copepod and Isopod) in Commerson’s Anchovy fish (India). Journal of Environmental Biology 27: 613–614. [PubMed] [Google Scholar]
  44. Rameshkumar G, Ravichandran S. (2013) Histopathological changes in the skins and gills of some marine fishes due to parasitic isopod infestation. Asian Pacific Journal of Tropical Biomedicine (2012): 1–5.23570009
  45. Ravichandran S, Ajithkumar TT. (2008) Secondary microbial infestation in Ilisha melastoma due to isopod fish parasite. Journal of fisheries and aquatic science 3(1): 92–96. [Google Scholar]
  46. Ravichandran S, Ranjit Singh AJA, Veerappan N. (2001) Parasite-induced vibriosis in Chirocentrus dorab off Parangipettai coastal waters. Current Science 80(5): 622–623. [Google Scholar]
  47. Cressey RF, Collette BB. (1970) Copepods and needle fishes: A study in host-parasitic relationships. Fishery Bulletin 68: 8, 347–432. [Google Scholar]
  48. Simudu V, Tsummoto K. (1985) Habitat segregation and biochemical activities of marine members of the family vibryionaceae. Applied Environmental Microbiology 180: 781–790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Trilles JP, Hipeau-Jacquotte R. (1996) Associations et parasitisme chez les Crustacés. In: Traité de Zoologie, Anatomie, Systématique, Biologie, publié sous la direction de Pierre-P. Grassé, Tome VII, Crustacés, Fascicule 2, Généralités (Suite) et Systématique, sous la direction de J. Forest, Masson Ed., Paris, 187–234. [Google Scholar]
  50. Trilles JP, Hipeau-Jacquotte R. (2012) Symbiosis and parasitism in the Crustacea. In: Grassé PP, Forest J, von Vaupel Klein C. (Eds) Traité de zoologie The Crustacea 1(3): 239–319.
  51. Trilles JP, Ravichandran S, Rameshkumar G. (2011) A checklist of the cymothoidae (Crustacea, Isopoda) recorded from Indian fishes. Acta Parasitologica 56(4): 445–459. doi: 10.2478/s11686-011-0077-z [Google Scholar]
  52. Trilles JP, Ravichandran S, Rameshkumar G. (2012) Catoessa boscii (Crustacea, Isopoda, Cymothoidae) parasitic on Carangoides malabaricus (Pisces, Carangidae) from India. Taxonomy and host-parasite relationships. Acta Parasitologica 57(2): 179–189. doi: 10.2478/s11686-012-0020-y [DOI] [PubMed] [Google Scholar]
  53. Vijayakumar R, Raja K, Velvizhi S, Sinduja K, Gopalakrishnan A. (2013) Occurrence of heavy copepod infestation on Hemiramphus lutkei and double parasitisms on Hemiramphus far with copepod (Lernaeenicus hemiramphi) and isopod (Mothocya plagulophora). Journal of Parasitic Disease 2013. doi: 10.1007/s12639-012-0222-0 [DOI] [PMC free article] [PubMed]

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