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

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

Ismail S. EL-SHAHAWY '* and Abdel-Razek Y. DESOUKY^

" Department of Parasitology, Faculty of Veterinary Medicine, South Valley University, Egypt

^'Department of Parasitology, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt

* Corresponding author, e-mail: är.ismailjpara(ayahoo.com

Cymothoa indica, a cymothoid isopod, is reported for the ftrst time parasitizing niurdjan (Pinecone soldierjish). a reef-associated ¡ndo-pacific fish, collected from the Red Sea. Egypt. The specimens ohserved are mature females and males. It /'.ç distinguishahle from the other memhers in the genus principally hy having a poorly developed amphicephalic process, ohlong hody. pyriform cephalon and presence of well-developed lohe on ischiitm ofpereopod VII. Parasites were fotmd in greater numhers in the huccal cavity (62.5%) than in the hranchial cavity (18.75%) of Myripristis murdjan with a totalprevalenee of 81.3%. In addition to the infection prevalence, mean intensity and site speciftcity 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 mttrdjan, the Pinecone soldier- cies with a short free-living planktonie phase. fish, is a common eoral-reef species usually Adults are exclusively parasitic and the presenee found in shallow lagoons and seaward reefs, is of a few individuals ean eause damage to hosts nocturnal, and feeds mainly on larger (PAPAPANAGIOTOU et at.. 19')9), They are observed ofthe Zooplankton. It is widely distributed from on the body, in the buccal cavity and/or gill cav- the Red Sea, ineluding the gulf of Oman and east ity of the hosts. They feed on host blood and of Africa, to Oceania, being one ofthe important tissue, as well as inducing tissue damage due to commercial species in Egyptian markets. the meehanieal pressure of the parasites body In aquatic systems parasites play an impor- (TRILLHS. 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 ofthe 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) deseribed contains almost exclusively parasitic families a new species Cymothoa spinipalpa from the such as Cymothoidae. The Cymothoid isopods mouth of Oligoplites saurus. ALAS ei at. (2008) 108 ACTAADRIATICA, 51(1): 103 - 110.2010

Stated Parablennius .sanguinolentus as a new TRILLES (1975), VEERAPAN & RAVICHANDRAN host record for Nerocila biviltala 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 ct al. (1997) and abundance and mean intensity found in marine fish; from the Mediterranean according to MARUOLiS c/«/. (1982). Sea and other areas of the world, e.g. French Polynesia (TRILLES & GALZIN, 1969); Australia Statistical Analysis (AVDEEV, 1979); eastem Pacific (BRUSCA, 1981); Tests of independence, Chi Squares (x^), Kuwait (BOWMAN & TAREEN. 19S3}; northwest were used for the analytical assessment for host Africa (ROKICKL 1986); Puerto Rico (WILLIAMS gender and site differences according to SNEDI- & WILLIAMS, 1994); Parangipettai coast, India COR & COCHRAN (1980J. (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 soldicrfish) from the Red Locality: Red Sea, Egypt Sea, with reference to its prevalence, location Prevalence: 81.3% (r95/240) on the host, abundance and the intensity ofthe 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 (x' = 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 (x" =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 (%' =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 lef\ were cleared and mounted according to the branchial cavity ofthe host. In 11.Wo 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 cany 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 & DKSOUKY: Myripristis murdjan a new host reeord for Cymothoa indica 109 the parasite was found attached to the anterior- Abundance: 0.85 ventral portion ofthe 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 (SCHIOBDTE & 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 ct at.. 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 52 31 14

Table I. Prevalence ofC. indica in relation to the host .sex and their location on the host fish B

A

Fig. I. Cymothoa indica (A) and (B) Pereopod VII. .showing the characteristic lobe on the postem- angle of ischium (fresh specimen) (circle). (Scale bar Smm) no ACTA ADRIATICA. 51 ( I ): 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 litoralts in Bra- remain completely undescribed. This was the zil (THATCHHR et ai. 2003). RAJKUMAR et al. (2004) situation in the Red Sea, particularly in Egypt, as observed severe infection by C indica in tbe there is a paucity of infonnation on fish associ- buccal cavity of tbe spot-tail needlefisb 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 eastem 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 tbe body of Sphyraena chrysotae- it was reported from several fish species such nia (TRILLES & BARICHE, 2006). This preference as Cichlidae: Etroplus maculatits, E. suraten- might be attributed to genetic or environmental sis (PANIKKAR & AIYAR, 1937); Gobiidae: Glos- differences (BELLO er «/., 1997). SOgobius giuris (CHILTON. 1924; PANIKKAR & In general, speeies of genus Cymothoa can AIYAR. 1937); Sphyraenidae: Sphyraena obtusata be divided into two groups according to the size and Synodontidae: Trachinocephalus tnyops and shape of antero-lateral angles of the first (VEERAPAN & RAVICHANDRAN. 2000); Belonidae: pereon segment. The first group includes about Strongylura strongylura (MISRA & NANDl, 1986; 27 species, which possess moderate to strongly RAJKUMAR et ai. 2004): cultured Mystus gulio wide amphicephalic proeesses of pereonite I. (Bagridae) and Lates calcarifer (Latidae) (RAJ- Furthemiore, the remaining species, referred to KUMAR et ai, 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 tbis study might be a secondary result ofthe 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 ofthe host population from C curta observed on the gills of Anablepis (GROSHOLZ & RUIZ. 1995; CARVALHO et al.. 2003). tetrophthalmi (SCHIOEDTE & MEINERT, 18X4) due Moreover, the high level of infection suggests to a less stocky body (L8 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- {11.1%) and Glossogobius giuris (50%), respec- skii is also distinct, with a body clearly more tively. elongated (2.38 times more long than wide), with poorly developed processes of pereonite In this study, females were more frequently I being distinctly aeute and the cephalon being infected than males, which is in agreement with abruptly narrowed at the level of ihe antennae. the results of LEONARDOS & TRILLES (2003) in a The posterior margin of pleonite V is bisinuate. study of Mothocya epimerica on the sand smelt pleotelson possesses a notch at the distal margin Atherina boyeri in the Mesolongi and Etolikon and the pereopod VII does not possess a lobe on Lagoons (western Greece). The main reason for postero-distal angle of ischium. C. frontal is dif- the differences in parasitic load with respect to fers mainly due to the possession of a less stocky host gender is thought to be physiological. body (2.66 times more long than wide) and the The parasites seem to prefer to infect the pleon is distinctly narrower than the pereon. buccal cavity and the right branchial cavity com- '".'WWM»*^''

EL-SHAHAWY & DESOUKY: Myripristis murdjan a new host record for Cymothoa indica 111

Ihe pleotelson is fairly less wide (1.5 times as BUSH, A.O., K.D. LAFFERTY, J.M. LOTZ & A.W. wide as long) and possesses a notch at the distal SHOSTAK. 1997. Parasitology meets ecol- margin and pereopod VII does not possess a ogy on ternis: Margolis ct ai. revisited. J. lobe on ischium. On the other hand.. C. indica Parasitol., 83(4): 575-583. from Egypt is similar to those species described CARVALHO. L.N., K. DEL-CLARO & R.M. TAKEMO- by TRILLES & BARICHE (2006) found parasitizing TO. 2003. Host parasite interaction between mainly barracudas (Sphyraenidae) from Leba- branchiurans (Crustacea: Argulidae) and non, from which it differs in being longer and piranhas (Osteichthyes: Serrasalminae) in more protracted. Pantanal wetland of Brazil. Environ. Biol. Fish., 67(3): 289-296. ACKNOWLEDGEMENTS CHILTON, C. 1924. Fauna of the Chilka Lake: Tanaidacea and Isopoda. Memoirs of the We thank the reviewers for their time spent Indian Museum, 5: 875-895. carefully reviewing our manuscript. We believe GROSHOLZ, E.D. & G.M. RUIZ. 1995. Does spatial that their positive comments substantially heterogeneity and genetic variation in improved this article. We appreciate the assist- population of the xanthid crab Rhitropan- opeus harrisii (Gold) intluence the preva- ance of Dr. Mohamed Abd EL-BARY MANDOUR, Husbandry and Animal Wealth Devel- lence of an introduced parasitic castrator? opment Department, Faculty of Veterinary Med- J. Exp. Mar. Biol. Ecol., 187: 129-145. icine, Alexandria University, for his kind col- HIEKAL. F.A. & M.Y. EL-SOKJCARY. 1990. Morphol- laboration regarding the statistical assessment. ogy of Telotha sp. (Crustacea: Isopoda) from El Kahia fish "^Oblada melanura'" in Alexandria. Assiut Vet. Med. J., 22(44): REFERENCES 75-97. LEONARDOS, 1. & J.P. TRILLES. 2003. Host-parasite ALAS, A., A. ÖKTENER. A. ISCIMEN & .I.P. TRILLES. relationships: occurrence and effect of the 2008. New host record, Parablennius san- parasitic isopod Mothocya epimerica on guinolentus (Teleostei., Perciformes., Blen- sand smelt Atherina boyeri in the Meso- niidae) for Nerocila bivittata (Crustacea, longi and Etolikon Lagoons (W. Greece). Isopoda.. Cymothoidae). Parasitol. Res., Dis. Aquat. Org., 54: 243-251. 102:645-646. MARGOLIS, L., G.W. ESCH, J.C. HOLMES, A.M. AVDEEV, vv. 1979. New species of the genus KURIS & G.A. SCHAD. 1982. The USe of Cymothoa (Isopoda, Cymothoidae) from ecological terms in Parasitology (report the coastal regions of Northern and North- of an ad hoc committee of the American Wcstcni Australia (in Russian). Parazi- Society of Parasitologists). J. Parasitol., tologiya, 13: 50-55. 68: 131-133. BELLO, G., A. VAGLIO & G. PISCITELLL 1997. The MISRA, A. & NC. NANDl. 1986. A new host record reproductive cycle oí Mothocya epimerica of Cymothoa indica Schioedte and Mcin- (Isopoda: Cymothoidae) a parasite of the ert (Crustacea; Isopoda) from Sundar- sand smelt, Atherina boyeri (Osteich- bans, West Bengal. Indian J. Fish., 33: thyes: Atherinidae), in the Lésina Lagoon, 229-231. Italy. J. Nat. Hist., 31: 1055-1066. ÖKTENER, A. & J.P. TRILLES. 2004, Report on BOWMAN, T.E. & I.U. TAREEN. 1983. Cymothoidae cymothoids (Crustacea, Isopoda) collect- from fishes of Kuwait (Arabian Gulf) ed from marine fishes in Turkey. Acta (Crustacea, isopoda). Smithson. Contrib. Adriat., 45:145-154. Zool., 382: 1-30. PANIKKAR, N.K. & R.G. AIYAR. 1937. On a cymoth- BRUSCA, R.C. 1981. A monograph on Isopoda oan parasitic on some brackish water fish- Cymothoidae (Crustacea) of the eastern es from Madras. Curr. Sei., 5: 429-430. Pacitlc. Zool. J. Linn. Soc, 73: 117-199. PAPAPANAGIOTOU, E.P., J.P. TRILLES & G. PHOTIS. 112 ACTAADRIATICA, 51(1): Iü3- 110. 2010

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Polynésie Française (On the presence of Series, Annamalai University, Parangipet- Cytnothoa pulchrum Lanchester, 1902 tai, 24p. (Isopoda, Flabellifera, Cymothoidae) in WILLIAMS. L.B. & E.H. WILLIAMS. 1994. Parasites French Polynesia). Cmstaceana, 36: 257- of Puerto Rican freshwater sport fishes. 266. Puerto Rico Dept. of Natural and F.nviron- VEERAPAN. N. & S. RAVICHANDRAN. 2000. lsopod mental Resources, San Juan, PR & Dept. parasites from marine fishes of Paran- of Marine Sciences, University of Puerto gipettai eoast. UGC-SAP Monograph Rico, Mayaguez, 99-103.

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

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

Ismail S. EL-SHAHAWY'* i Abdel-Razek Y. DESOUKY^

' Odsjek parazitologije. Veterinarski faku¡tet, Sveuciliste South Valley, Egipat

^ Odsjek parazitoiogije, Veterinarski fakultet, Sveuciliste Kafrelsheikh, Egipat

'Kontakt adresa, e-mail: dr.ismailj}[email protected]

SAZETAK

Cymothoa indica., racic jednakonozac je pronaden po prvi put na domacinu, crvcnoj vojni- kinji Myripristis murdjan, Indo-pacifickoj grebenskoj ribi ulovjenoj u Crvenom moru, u Egiptu. Istrazivani primjerci su bili zrele zenke i muzjaci. Razlikuje se od ostalih pripadnika roda po slabo razvijenom amflcefalnom procesu, duguljastom tijelu, piriformnom obliku glave i dobro razvijcnoj resici na ischiumu pereopoda VII. Veci broj parazita je pronaden u usnoj supljini (62.5%) nego u skrznom otvoru (18.75%) crvene vojnikinje, Myripristis murdjan, s ukupnom zastupljenoscu od 81.3%. U radu se raspravljavlja o zastupljenosti, jacini i posebnostima infekcije.

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