ISSN: 0001-5113 ACTA ADRIAT., UDC: 574.583 : 597.5 (262.4/.5) AADRAY 51(1): 103 - 110, 2010

Myripristis murdjan (: ) a new host record for Cymothoa indica (Crustacea, Isopoda, Cymothoidae)

Ismail S. El-Shahawy 1* and Abdel-Razek Y. Desouky2

1) Department of Parasitology, Faculty of Veterinary Medicine, South Valley University, Egypt

2) Department of Parasitology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt

* Corresponding author, e-mail: [email protected]

Cymothoa indica, a cymothoid isopod, is reported for the first time parasitizing murdjan (Pinecone soldierfish), a reef-associated Indo-pacific fish, collected from the Red Sea, Egypt. The specimens observed are mature females and males. It is distinguishable from the other members in the genus principally by having a poorly developed amphicephalic process, oblong body, pyriform cephalon and presence of well-developed lobe on ischium of pereopod VII. Parasites were found in greater numbers in the buccal cavity (62.5%) than in the branchial cavity (18.75%) of with a total prevalence of 81.3%. In addition to the infection prevalence, mean intensity and site specificity are discussed.

Key words: Cymothoa indica, Egypt, Myripristis murdjan, prevalence, Red Sea

Introduction inhabit freshwater, brackish water and the sea environment as ectoparasites of various fish spe- Myripristis murdjan, the Pinecone soldier- cies with a short free-living planktonic phase. fish, is a common coral-reef species usually Adults are exclusively parasitic and the presence found in shallow lagoons and seaward reefs, is of a few individuals can cause damage to hosts nocturnal, and feeds mainly on larger (Papapanagiotou et al., 1999). They are observed of the zooplankton. It is widely distributed from on the body, in the buccal cavity and/or gill cav- the Red Sea, including the gulf of Oman and east ity of the hosts. They feed on host blood and of Africa, to Oceania, being one of the important tissue, as well as inducing tissue damage due to commercial species in Egyptian markets. the mechanical pressure of the parasites body In aquatic systems parasites play an impor- (Trilles, 1969; Romestand, 1978, 1979). tant role in the ecology of coastal and marine Several recent studies have focused on ecosystems as well as in mariculture. Isopods Cymothoidae, one of them reporting thirteen are one of the most diverse orders of crustaceans cymothoid species belonging to six genera (Ani- and live in a wide variety of environments, from locra, Nerocila, Ceratothoa, Emetha, Livoneca terrestrial habitats to marine and fresh waters, and Mothocya) in Turkey (Öktener & Trilles, though are most commonly found in shal- 2004). In the coastal waters at Ponta Negara, low marine waters. The suborder Flabellifera Natal, Brazil, Thatcher et al. (2007) described contains almost exclusively parasitic families a new species Cymothoa spinipalpa from the such as Cymothoidae. The Cymothoid isopods mouth of Oligoplites saurus. Alas et al. (2008) 108 ACTA ADRIATICA, 51(1): 103 - 110, 2010 stated Parablennius sanguinolentus as a new Trilles (1975), Veerapan & Ravichandran host record for Nerocila bivittata in the Black (2000) and Rajkumar et al. (2004, 2005). The Sea, Turkey. Species of genus Cymothoa Fab- prevalence was calculated according to Bush ricius 1793 are widely distributed and mostly et al. (1997) and abundance and mean intensity found in marine fish; from the Mediterranean according to Margolis et al. (1982). Sea and other areas of the world, e.g. French Statistical Analysis Polynesia (Trilles & Galzin, 1969); Australia (Avdeev, 1979); eastern Pacific (Brusca, 1981); Tests of independence, Chi Squares (χ2), Kuwait (Bowman & Tareen, 1983); northwest were used for the analytical assessment for host Africa (Rokicki, 1986); Puerto Rico (Williams gender and site differences according to Snedi- & Williams, 1994); Parangipettai coast, India cor & Cochran (1980). (Veerapan & Ravichandran, 2000) and recent- ly Lebanon (Trilles & Barchie, 2006). Despite Results that, there are still several parts of the world where cymothoid fauna is poorly known or even The recovered isopod from Myripristis completely unknown. Therefore, the objective murdjan was identified as Cymothoa indica of the present study was to identify the isopod (Schioedte & Meinert, 1884). parasite, which has been recorded from M. Host: Myripristis murdjan murdjan (Pinecone soldierfish) from the Red Locality: Red Sea, Egypt Sea, with reference to its prevalence, location Prevalence: 81.3% (195/240) on the host, abundance and the intensity of the C. indica is mainly found in the buccal and infection. the branchial cavities of the examined host. Of 240 M. murdjan, 195 specimens were found Material and Methods to carry 205 parasites, equivalent to an overall prevalence of 81.3%. The prevalence of the A total of 240 (150 females and 90 males) parasite with respect to the host gender was specimens of Myripristis murdjan, the Pine- 54.2% and 27.1% in females and males respec- cone soldierfish (commercially named murjan), tively. Although females generally had a higher weighing 180g ± 10.5 (150-190 g) with total infection rate than males, it was not statistically length of 20cm ± 2.4 (18-22 cm) each were significant (χ2 = 0.8144, P>0.05). obtained from El-Obour fish market, Cairo, Site of infection: Buccal cavity (62.5%) Egypt. The fish were transported to the labo- branchial cavity (18.75%). This difference was ratories of the Departments of Parasitology of found to be highly significant (χ2 =44.024, Kafrelsheikh and South Valley Universities of P<0.01). Moreover, the percentage occurrence Egypt, preserved in cold icebox and individually of the parasite in relation to the branchial posi- inspected for the presence of isopod parasite. tion for the right and left branchial chambers The recovered parasitic isopods were was found to be highly significant (χ2 =22.27, removed from the mouths and gill chambers P<0.01). of the infected fish. Their sizes were measured A total of 150 parasites were found in the after being washed in physiological saline solu- buccal cavity and 45 parasites were found in tion and fixed in 70% ethyl alcohol. Parasites the right branchial cavity and 10 in the left were cleared and mounted according to the branchial cavity of the host. In 77.1% cases one method described by Thatcher (1991). Parasites pair of adult parasites was found, and 10 (4.2%) appendages were dissected with a needle in pure were found to carry 2 parasites, one in each phenol for the study of temporary mount. branchial cavity. The parasite in the host buccal The recovered parasites were morphologi- cavity occupied the bottom, attached firmly to cally identified according to available litera- the tongue with cephalic part directed towards ture; Schioedte & Meinert (1884), Pillai (1954), to the mouth opening. In the branchial cavity, El-Shahawy & Desouky: Myripristis murdjan a new host record for Cymothoa indica 109 the parasite was found attached to the anterior- Abundance: 0.85 ventral portion of the host’s gill chambers. Para- Intensity: 1.08 parasites/fish sites cephalon were always directed towards the Distribution: Previous reliable records are host ventral side. The parasite body was bent to entirely from the Indian Ocean; Bangkok, Thai- the right when it occupied the right branchial land (Schioedte & Meinert, 1884) and India, cavity or to the left when it occupied the left Chilka Lake (Chilton, 1924), Madras (Panikkar branchial cavity. In most cases, the parasite was & Aiyar, 1937), Parangipettai (Veerapan & Ravi- located between the second and third branchial chandran, 2000; Rajkumar et al., 2004, 2005a, b) arches. The percentage of occurrence of female and recently from Lebanon (Trilles & Barchie, parasites with respect to gender and site is shown 2006). in Parasite location Buccal cavity Right branchial cavity Left branchial cavity

Host N. +Ve % Female Male Female Male Female Male

Female 150 130 54.2 70 40 22 8 4 3 Male 90 65 27.1 28 12 9 6 2 1 Total 240 195 81.3 98 52 31 14 6 4

Table 1. Prevalence of C. indica in relation to the host sex and their location on the host fish

Fig. 1. Cymothoa indica (A) and (B) Pereopod VII, showing the characteristic lobe on the postero- angle of ischium (fresh specimen) (circle). (Scale bar 8mm) 110 ACTA ADRIATICA, 51(1): 103 - 110, 2010

Discussion pared to the left branchial cavity. This difference was statistically significant. Similar results were Marine isopods are poorly studied animals reported previously for C. catarinensis isolated in many regions of the world and some groups from the mouth of Menticirrhus litoralis in Bra- remain completely undescribed. This was the zil (Thatcher et al., 2003). Rajkumar et al. (2004) situation in the Red Sea, particularly in Egypt, as observed severe infection by C. indica in the there is a paucity of information on fish associ- buccal cavity of the spot-tail needlefish Strongy- ated isopods (Hiekal & El-Sokkary, 1990). lura strongylura. In the study of C. indica In this study Cymothoa indica was recorded populations from the eastern Mediterranean Sea for the first time from the Red Sea, Egypt and the parasites were mainly found in the mouth, Myripristis murdjan, the Pinecone soldierfish, is occasionally in the branchial cavities and more a new host recorded for this parasite. Previously rarely on the body of Sphyraena chrysotae- it was reported from several fish species such nia (Trilles & Bariche, 2006). This preference as Cichlidae: Etroplus maculatus, E. suraten- might be attributed to genetic or environmental sis (Panikkar & Aiyar, 1937); Gobiidae: Glos- differences (Bello et al., 1997). sogobius giuris (Chilton, 1924; Panikkar & In general, species of genus Cymothoa can Aiyar, 1937); Sphyraenidae: Sphyraena obtusata be divided into two groups according to the size and Synodontidae: Trachinocephalus myops and shape of antero-lateral angles of the first (Veerapan & Ravichandran, 2000); Belonidae: pereon segment. The first group includes about Strongylura strongylura (Misra & Nandi, 1986; 27 species, which possess moderate to strongly Rajkumar et al., 2004); cultured Mystus gulio wide amphicephalic processes of pereonite I. (Bagridae) and Lates calcarifer (Latidae) (Raj- Furthermore, the remaining species, referred to kumar et al., 2005a, b) and recently from Sphy- as a second group, are characterized by poorly raena chrysotaenia (Trilles & Bariche, 2006). developed or undeveloped amphicephalic proc- The high prevalence of C. indica (81.3%) esses of pereonite I. The Egyptian specimens in this study might be a secondary result of the undoubtedly belong to the second group of migration of exotic fish species from the Medi- Cymothoa since they possess poorly developed terranean Sea to the Red Sea through the Suez amphicephalic processes of pereonite I. Egyp- Canal, in addition to the environmental condi- tian Cymothoa can be readily distinguished tion and spatial structure of the host population from C. curta observed on the gills of Anablepis (Grosholz & Ruiz, 1995; Carvalho et al., 2003). tetrophthalmi (Schioedte & Meinert, 1884) due Moreover, the high level of infection suggests to a less stocky body (1.8 times as long as wide that M. murdjan might under certain condi- for C. curta), presence of a pyriform cephalon tions be a suitable host for C. indica. Panikkar and the posterior margin of pleonite V being & Aiyar (1937) recorded similar observations unsinuate (trisinuate) while the posterior margin from Etrophus maculates, Etrophus suratensis of pleotelson is broadly rounded. C. slusar- (77.7%) and Glossogobius giuris (50%), respec- skii is also distinct, with a body clearly more tively. elongated (2.38 times more long than wide), In this study, females were more frequently with poorly developed processes of pereonite infected than males, which is in agreement with 1 being distinctly acute and the cephalon being the results of Leonardos & Trilles (2003) in a abruptly narrowed at the level of the antennae. study of Mothocya epimerica on the sand smelt The posterior margin of pleonite V is bisinuate, Atherina boyeri in the Mesolongi and Etolikon pleotelson possesses a notch at the distal margin Lagoons (western Greece). The main reason for and the pereopod VII does not possess a lobe on the differences in parasitic load with respect to postero-distal angle of ischium. C. frontalis dif- host gender is thought to be physiological. fers mainly due to the possession of a less stocky The parasites seem to prefer to infect the body (2.66 times more long than wide) and the buccal cavity and the right branchial cavity com- pleon is distinctly narrower than the pereon. El-Shahawy & Desouky: Myripristis murdjan a new host record for Cymothoa indica 111

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Received: 28 May 2009 Accepted: 28 January 2010 114 ACTA ADRIATICA, 51(1): 103 - 110, 2010

Myripristis murdjan, (Beryciformes: Holocentridae) crvena vojnikinja kao novi domaćin parazita Cymothoa indica (Crustacea, Isopoda, Cymothoidae)

Ismail S. El-Shahawy1* i Abdel-Razek Y. Desouky2

1 Odsjek parazitologije, Veterinarski fakultet, Sveučillšte South Valley, Egipat

2 Odsjek parazitologije, Veterinarski fakultet, Sveučilište Kafrelsheikh, Egipat

* Kontakt adresa, e-mail: [email protected]

SAŽETAK

Cymothoa indica, račić jednakonožac je pronađen po prvi put na domaćinu, crvenoj vojni- kinji Myripristis murdjan, Indo-pacifičkoj grebenskoj ribi ulovjenoj u Crvenom moru, u Egiptu. Istraživani primjerci su bili zrele ženke i mužjaci. Razlikuje se od ostalih pripadnika roda po slabo razvijenom amficefalnom procesu, duguljastom tijelu, piriformnom obliku glave i dobro razvijenoj resici na ischiumu pereopoda VII. Veći broj parazita je pronađen u usnoj šupljini (62.5%) nego u škržnom otvoru (18.75%) crvene vojnikinje, Myripristis murdjan, s ukupnom zastupljenošću od 81.3%. U radu se raspravljavlja o zastupljenosti, jačini i posebnostima infekcije.

Ključne riječi: Cymothoa indica, Egipt, Myripristis murdjan, pretežito, Crveno more El-Shahawy & Desouky: Myripristis murdjan a new host record for Cymothoa indica 115 116 ACTA ADRIATICA, 51(1): 103 - 110, 2010