ISSN: 0001-5113 ACTA ADRIAT., Editorial note AADRAY 45 (1): 3-8, 2004
This volume is dedicated to Dr. RADOSNA MUŽINIĆ, fishery biologist, who devoted the whole life to fishery research for benefit of the Croatian fishery and this Institute.
Dr. sc. Radosna Mužinić 1916-2004 4 ACTA ADRIATICA, 45(1): 3-8, 2004
Dr sc. RADOSNA MUŽINIĆ died at the age of 87 on 5 April 2004. She was an internationally renowned and highly respected Fisheries scientist and Ichthyologist as well as leading scientist in small pelagic fish studies in Croatia. Dr. Mužinić was born on 15 November 1916 in Metković. She has obtained her degree in bio- logy in 1940, while in 1953 she got her PhD degree. She became scientific counsellor in 1967. From 1946 up to her retirement, Dr. Mužinić has worked in the Institute of Oceanography and Fisheries. She has continued to work for IOF until the end of 1990 as outside collaborator. During 1956 she worked in the Great Britain sponsored by the British Council at Fisheries Laboratory in Lowestoft and Marine Laboratory in Aberdeen. The scientific work of Dr. Radosna Mužinić is of a great importance not only for the Croatian, but also for the international scientific community. Her research referred to biology and ecology of commercially interesting Adriatic fish species, especially sardine, sprat, anchovy, Atlantic mackerel, Spanish mackerel, horse mackerel, red mullet, hake and grey mullet, and to some extent even the North Sea herring. The main field of her research was focused on sardine. The scientific work of Dr. Radosna Mužinić covered different issues such as sub-population of sardine in the Adriatic (taking into account importance of this matter for better fishery management), biology of sardine and surmullet as well as ecology of sardine. Especially important studies she has conducted were her pioneer research on sardine migration (with tagging method) and its causality in relation to fish physiological state, daylight, salinity, temperature, sea currents and zooplankton quantity and composition. Significant studies were led on distribution of pelagic and other fish species together with their relation towards environment, comparative analysis of their distribution as well as predator’s preferences of these species in different parts of the Adriatic. Especially important are the studies on sardine and anchovy behavior in aquarium conditions together with research related to their possibilities of preservation of the species in captivity conditions. Nevertheless important are the studies referring to the sardine search for food, studying of its initial and mortality during the preservation experiment, fish growth and condition during experiment, analysis of mortality causes, light and temperature impact on the fish, formation of the groups – schools and aggregations, as well as fin damage, scale erosion, parasitism and other deformations. Behavior during experiment was compared with behavior in the nature. She has also studied catch of pelagic fish, their composition, space distribution, coincidences and alternations, long term and seasonal fluctuations. Among methodological problems outstanding are the following: study on sardine scales and otholits in order to determine the age, the first apply of tagging method for sardine, preservation of the sardine and anchovy in captivity conditions, anesthesia of sardine for the tagging and other interventions. Dr. Radosna Mužinić has exerted herself on studying of Adriatic fish resources. With her intensive scientific work she has contributed to the better knowledge of these resources that before the World War II was poor and fragmentary. She was the Head of Laboratory for Ichthyology and she led the Group for pelagic fish within the Institute of Oceanography and Fisheries until her retirement. She was the member of the following associations: - Croatian Biological Society - Ecological Society - Yugoslav Society for Research and Promotion of Maritime Affairs - Commision internationale pour l’Exploration scientifique de la Mer Méditerranée (CIESM) - General Fisheries Council for the Mediterranean (GFCM-FAO) Dr. Radosna MUŽINIĆ Editorial note 5
Dr. Mužinić was the President of an International group for sardine and related species. She also, led the seminar on sardine tagging held in Split in 1964. Dr. Mužinić was a member of Administrative Board of the World scientific meeting on the biology of sardine and related species, held in Rome in 1959. Up to 1982 she lead working group of the Institute under the project “Research on pollutant effects on sea organisms and their populations” (FAO/UNEP). Her papers are inevitable literature for all scientists and especially for ichthyologists. With her devoted and dedicated work she has marked fishery research of this Institute which is very important for the fishery management and economy. In her research on pelagic fish she was very versatile and thus knew how to join fieldwork (that she has participated herself) with experimental and laboratory work. Her great experience allowed her to participate in creation of scientific policy of the Institute. Dr. Mužinić has unselfishly transferred her knowledge to the younger colleges in order to maintain the continuity of research in this important domain. She has published 73 scientific papers, internationally reviewed, often with colleges from other countries and also 41 professional paper that make significant contribution to the Fishery Science and Ichthyology. Her paper results were cited worldwide. She was respected by everyone who met her. Her death is a great loss to Croatia and to the world of Fisheries Science and Ichthyology. The cherished memories of Dr. sc. Radosna Mužinić will forever remain in the hearts of her friends, institutional colleagues and those national and international scientists who were fortunate to work with her and to know her.
Dr. sc. Gorenka SINOVČIĆ
Radosna MUŽINIĆ
BIBLIOGRAPHY OF SELECTED PAPERS 1948/49. First tagging experiments on the sardi- 1955. Sur l’ étude des déplacements de la ne (Clupea pilchardus Walb.) in the Adriatic. sardine (Sardina pilchardus Walb.) dans Acta Adriat., 3(10):1-26. l’Adriatique orientale. Proc. gen. Fish. 1950. Tagging of sardine (Clupea pilchardus Coun. Medit., 3:255-260. Walb.) in the Adriatic in 1949. Acta Adriat., 1955a. Résumé de nos connaissances actuelles 4(7):1-30. sur la sardine (Sardina pilchardus Walb.) de 1950a. /M. KRVARIĆ/. Investigation into the l’Adriatique. Proc. gen. Fish. Coun. Medit., fat content in the sardine tissues (Clupea 3:307-314. pilchardus Walb.). Acta Adriat., 4(8):1-26. 1955b. Istraživanja o kretanju srdele (Clupea 1952. Tagging of sardine (Clupea pilchardus pilchardus Walb.) u Jadranu. Glasnik biol. Walb.) in the Adriatic in 1950 and 1951. sek., Ser. 2/B.T. Zbornik I kongresa biologa Acta Adriat., 4(11):1-22. Jugoslavije, Zagreb, 1955, 7(99):275-277. 1952. Remarques sur le développement et la 1956. Some observations on the habits of the croissance des otolithes de la sardine sardine. Papers Internat. techn. conference (Clupea pilchardus Walb.). Acta Adriat., conservation of the living resources of the sea, Rome, 1955, pp. 95-97. 4(13):1-22. 1956a. Quelques observations sur la sardine, 1953. Tagging of the sardine in the Adriatic. l’anchois et le maquereau des captures au Bull sci., 1(2): p.45. chalut dans l’Adriatique. Acta Adriat., 7(13): 1954. Contributon à l’étude de l’oecologie de 1-39. la sardine (Sardina pilchardus Walb.)dans 1957. Sur la croissance de la jeune sardine l’Adriatique orientale. Acta Adriat., 5(10): (Sardina pilchardus Walb.) dans les eaux 1-219. 6 ACTA ADRIATICA, 45(1): 3-8, 2004 de Split. Bilješ.-Notes. Inst. oceanogr. ribar., 1960e. On the schooling and feeding habits Split, 12:1-4. of sardine (Sardina pilchardus Walb.) in 1958. /P.BOUGIS/. Sur la croissance de Mullus aquarium (preliminary observations). Proc. barbatus (L.) dans les eaux de Split. Acta World scientific meeting on the biology of Adriat., 8(9):1-14. sardines and related species, Rome, 1959. 3, 1958a. Prilog izučavanju odnosa srdele (Sardina Experience Paper, 17, pp. 1119-1123. pilchardus Walb.) i njezine sredine. 1960f. /J.C. MARR/. Report of section 1. Acta Adriat., 8(10):1-19. Population identification. Proc. World sci- 1958b. Preliminarna opažanja o srdeli (Sardina entific meeting on the biology of sardines pilchardus Walb.) sa zapadne obale Istre. and related species, Rome, 1959, 1:3-6. Acta Adriat., 8(11):1-27. 1961. On the formation of rings and growth 1958c. Preliminarna istraživanja o broju nema- zones on sardine scales (Sardina pilchardus toda kod šnjura, Trachurus trachurus L. Walb.). Proc. gen. Fish. Coun. Medit., 6: Bilješ.-Notes. Inst. oceanogr. ribar., Split, 71-83. 13:1-3. 1961a. Nematod haringe uzročnik bolesti čovje- 1958d. /D.RICHARDSON/. On the appearance ka. Priroda, 2:p.58. on herring scales. J. Cons. int. Explor. Mer, 1964. Kolebanje veličine srdele i njezina ulova 24(1):120-134. u srednjem dijelu istočnog Jadrana. Acta 1958e. Sur la coïncidence et l’alternance dans Adriat., 11(29):215-218. la pêche de quelques poissons pélagiques. Rapp. Comm. int. Mer Médit., 14:313-315. 1964a. Neka opažanja o reagiranju srdele 1959. On the rings on sardine scales. Proc. gen. (Sardina pilchardus Walb.) na svje- Fish. Coun. Medit., 5:341-350. tlo u eksperimentalnim uvjetima. Acta 1960. /B.B. PARRISH, J.A.POPE). Some Adriat.,11(30):219-226. observations on the body proportions of 1964b. Comparative study of scales and oto- North Sea autumn spawning herring. Cons. liths in sardines (Sardina pilchardus Walb.). Int. Explor. Mer., 25(2):191-203. Proc. gen. Fish. Coun. Medit., 7:171-189. 1960a. Identification of populations. Proc. 1964c. Further observation on schooling and World scientific meeting on the biology of aggregating behaviour of sardines (Sardina sardine and related species, Rome, 1959. 3, pilchardus Walb.). Proc. gen. Fish. Coun. Methodological Paper 2, pp. 1287-1305. Medit., 319-323. 1960b. Sardina pilchardus Walb. – 1964d. Mortalitet srdele (Sardina pilchardus Mediterranean nad Black Sea. Proc. World Walb.) u eksperimentlnim uslovima. scientific meeting on the biology of sardines Arhiv biol. nauka, 16(1-2):83-98. and related species. Rome, 1959. 3, Stock 1964e. The value of sharp rings for the age and Area paper, 4, pp. 793-805. determination of sardine (Sardina pilchar- 1960c. Annual changes in the size of sardine dus Walb.). Stud. Rev. gen. Fish. Coun. and in the yield of the fishery in the Medit., 25:1-3. central part of the eastern Adriatic. Proc. World scientific meeting on the biology of 1965. Fish condition, method of capture, han- sardines and related species. Rome, 1959. 3, dling of fish for tagging and their influence Experience Paper, 6, pp. 977-981. on tag return tags. FAO/GFCM Seminar on 1960d. On the identification of populations of sardine tagging, Split, Yugoslavia, 1964, sardine (Sardina pilchardus Walb.) in the Report and lectures, Rep. 1995, pp. 31-33. Adriatic. Proc. World scientific meeting on 1966. Initial mortality of the sardine under the biology of sardines and related species, experimental conditions and in the tagging Rome, 1959. 3, Experience Paper, 7, pp. work. Stud. Rev. gen. Fish. Coun. Medit., 31: 983-988. 1-20. Dr. Radosna MUŽINIĆ Editorial note 7
1966a. Daljnja opažanja o mogućnostima odr- 1972. O horizontalnoj raspodjeli srdele i brgljuna žavanja srdele u eksperimentalnim uslovi- u Jadranu. Pomorski zbornik, 10:603-611. ma. Arhiv biol. nauka, 18:91-96. 1973. O horizontalnoj raspodjeli skuše u 1967. Comparison between some behaviour Jadranu. Ekologija, 8(1):177-198. features of sardine in captivity and natural 1973a. A preliminary comparative study of habitat. Proc. gen. Fish. Coun. Medit., 8: the horizontal distribution of some pelagic 287-294. fishes in the Adriatic. Ichthyologia, 5(1): 1967a. O kolebanju i prostornoj raspodjeli jugo- 99-112. slavenskog ulova srdele, papaline, brgljuna, 1973b. Migrations of adult sardines in the cen- sluše i plavice. Acta Adriat., 13(3):1-29. tral Adriatic. Netherlands J. Sea Res., 7: 1967b. O raspodjeli jugoslavenskog ulova srde- 19-30. le, papaline, brgljuna, skuše i plavice u toku 1974. O prostornim i vremenskim karakteristi- godine. I Alterniranje sezone ulova papaline kama nekih pelagičnih resursa Jadrana. i ostalih vrsta, posebno srdele. Ekologija, Acta Adriat., 16(16):251-304. 2(1-2):61-72. 1975. /O.KARLOVAC). On food preferences 1967c. Peliminary aquarium tagging expe- of the Adriatic hake, Merluccius merluccius riments on sardine with anchor tags. IX (L.). Acta Adriat., 17(7):1-48. Session, Gen. Fish. Coun. Medit., WD-A1: 1977. On the shoaling behaviour of sardines 1-12. (Sardina pilchardus Walb.) in aquaria. J. 1967d. Further aquarium tagging experiments Cons. int. Explor. Mer, 37(2):147-155. on sardines with anchor tags. IX Session, 1979. On species composition and length cha- Gen. Fish. Coun. Medit., WD-A1-Suppl.1: racteristics in mixed species catches of 1-14. pelagic fshes in the Adriatic. Acta Adriat., 1967e. On the use of tricaine methane sulpho- 19(11):1-44. nate (MS 222) in tagging and transpor- 1979. Neka opažanja o ekologiji plavice ting sardines. IX Session, Gen. Fish. Coun. (Scomber japonicus Houtt.) u srednjem Medit., TP 21, p. 1. Jadranu. Acta biol.JAZU,8(1-19):115-122. 1968. Aquarium tagging experiments on sardine 1979a. O nekim pelagičkim ribama u sred- with anchor tags by use of tricaine methan njo dalmatinskom otočnom području. sulfonate. Stud. Rev. gen. Fish. Coun. Prirodoslovna istraživanja 43, Acta biol., Medit., 36:1-31. 8(1-10):123-176. 1969. Coincidence and alternation in Yugoslav 1979b. O plavici (Scomber japonicus Houtt.) u pelagic fisheries. Stud. Rev. gen. Fish. Jadranu. Pomorski zbornik, 17:613-632. Coun. Medit., 28:25-32. 1980. O srdeli vanjskih voda srednjodalmatin- 1969a. Observations on the reactions of the skog otočnog područja. Pomorski zbornik, sardine (Sardina pilchardus Walb.) to inter- 18:453-480. mittent white light. Proc. FAO Conference 1981. Summary of present knowledge of the on fish behaviour in relation to fishing Spanish mackerel (Scomber japonicus techniques and tactics. Bergen, 1967. FAO Houtt.) in the Adriatic. Rapp. Comm. int. Fish. Rep., 62(3):861-871. Mer Médit., 27(5):95-96. 1969b. O raspodjeli jugoslavenskog ulova srde- 1982. On long-term and seasonal fluctuations le, papaline, brgljuna, skuše i plavice u toku in the catch of some pelagic fishes in the godine. II Karakteristike raspodjele ulova eastern Adriatic. Ichthyologia, 14(1):59-86. srdele, brgljuna, skuše i plavice u njihovoj 1983. O srdeli, brgljunu i skuši u širem području sezoni lova. Ekologija, 4(1):23-59. Palagruže. Acta biol. JAZU, 9(9):119-144. 1983a. Skuša (Scomber scombrus L.) u Jadranu. 1970. On the use of anaesthetics in the tran- Pomorski zbornik, 21:477-504. sportation of sardines. Stud. Rev. gen. Fish. Coun. Medit., 47:1-23. 8 ACTA ADRIATICA, 45(1): 3-8, 2004
1984. Oslić (Merluccius merluccius /L./, ugotica 1986c. /G. SINOVČIĆ, M. TUDOR/. Research dubinka (Micromesistius poutassou /Risso/ i on the effects of pollutants on marine orga- ugotica mala (Trisopterus minutus capela- nisms and their populations (MED POL nus /Lac./ u širem području Palagruže. Rad IV, UNEP/FAO). Final reports of princi- JAZU, 411:105-119. pal investigators, MAP Technical Reports 1985. Summary of present knowledge of the Series, 4:109-116. mackerel (Scomber scombrus L.) in the 1987. Opažanja o srdeli (Sardina pilchardus Adriatic. Rapp. Comm. int. Mer Médit., Walb.) u akvariju. Pomorski zbornik, 25: 29(8):53-56. 517-545. 1986. O nekim ribama iz demerzalnog lova u širem području Palagruže. Rad JAZU, 424: 1988. The relations of the hake (Merluccius 69-84. merluccius /L./, the blue whiting 1986a. Šnjuri (rod Trachurus) u Jadranu. (Micromesistius poutassou /Risso/ and the Pomorski zbornik, 24:359-385. poor cod (Trisopterus minutus capelanus 1986b. On the relations of some fishes to the /Lac./) to the depth and bottom in the depth and bottom in the Adriatic. Rapp. Adriatic. Rapp. Comm. int. Mer Médit., Comm. int. Mer Médit., 30(2):p.239. 31(2): p.280. ISSN: 0001-5113 ACTA ADRIAT., UDC: 591.4 (262.53)”1990/1999” 551.463(262.53) AADRAY 45 (1): 9-26, 2004 Original scientific paper
Bivalvia (Mollusca) fauna of the Sea of Marmara
Serhat ALBAYRAK, Hüsamettin BALKIS and Neslihan BALKIS
Department of Biology, Faculty of Science, Istanbul University, 34118 Vezneciler - Istanbul, Turkey E-mail: [email protected]
The aim of this study was to determine which Bivalvia fauna exist in the Sea of Marmara and some of the ecological characteristics of their habitats. Eighty-six of 254 stations that were studied between 1990 and 1999 were sampled and 59 species belonging to 49 genera and 28 families were identified. These species are listed together with 205 previously recorded species. Also listed are the primary hydrographic conditions (salinity, temperature, dissolved oxygen) of the stations at the moment of sampling. The fact that fewer species were found than in earlier reports indicates the negative impact on species richness of habitats damaged by new ports and motorways on the edge of the sea plus domestic and industrial pollution.
Key words: Bivalvia, Mollusca, Sea of Marmara
INTRODUCTION fauna has been negatively influenced by human and natural factors for many years. The Sea of Marmara is a small basin with an Although, the biological diversity increases approximate size of 70 x 250 km, surface area of from the Black Sea towards the Mediterranean, 11500 km2, and maximum depth of 1390 m. It the number of bivalve species in the Sea of Marmara is greater than on Turkish coasts of is located between Europe and Asia (BEŞİKTEPE the Aegean and Mediterranean Seas (ÖZTÜRK et al., 1995) and, together with the Bosphorus ÇEVİK, 2000). Yet the biological diversity of this and the Dardanelles, forms the “Turkish Straits region is facing threats of decreasing because of System”. It connects to the Black Sea through the high levels of pollution and human activity. the Bosphorus in the northeast and to the Aegean Many studies have collected data on bivalves Sea via the Dardanelles in the southwest. There in the Sea of Marmara (COLOMBO, 1885; are two distinctly different water masses in the OSTROUMOFF, 1896; MARION, 1898; PALLARY, basin (ÜNLÜATA et al., 1990; TUĞRUL & POLAT, 1917; NINNI, 1923; DEVEDJIAN, 1926; DEMİR, 1952; 1995). The surface water is brackish, originating KANEVA-ABADJIEVA, 1959; TORTONESE, 1959; in the Black Sea (22-26 psu), and the bottom CASPERS, 1968; OBERLING, 1969-1971; PINAR, layer originates in Mediterranean subhalocline 1974; OKUŞ, 1989; YÜKSEK, 1989; BALKIS, 1992; waters (38.5-38.6 psu). As a result of containing ALBAYRAK & BALKIS, 1996; ERYILMAZ, 1997; both brackish and sea water, the Sea of Marmara UYSAL et al., 1998; DEMİR, 2003) but there are few may have a rich variety of fauna. However, the recent studies on the current situation. Further, 10 ACTA ADRIATICA, 45(1): 9-26, 2004 ecological characteristics of the habitats in and the bottom structure of the stations are which the species were found were not always given in Table 1. adequately recorded in earlier studies. The samples were rinsed through a 0.5 mm The aim of this study is to report on mesh sieve. Bivalve specimens were removed the present situation of Bivalvia in the Sea from the samples and fixed and preserved in of Marmara and some of the ecological a 5% formaldehyde solution prepared in sea characteristics of their habitats. water. TEBBLE (1966), PARENZAN (1974, 1976), POUTIERS (1987), POPPE & GOTO (1993) were used to identify the bivalves, SABELLI et al. (1990) MATERIALS AND METHODS and CLEMAM (2003) database were followed in classification of species. Coastal fauna were collected with a scoop After identifying the species in our net. Deep sea fauna were collected by the R/V laboratory, all specimens were sent to the ARAR from various depths using trawl, beam- Museum National d’Histoire Naturelle, Paris, trawl and dredging. Data were collected during and the Istituto di Scienze Ambientali Marine, 1990-1999 at 86 of 254 studied stations (Fig. 1). Genova, for confirmation of identification and Depth, temperature, salinity, dissolved oxygen comparison with their collections.
Fig. 1. Map of Sea of Marmara showing sampling stations ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 11
Table 1. Data about sampling stations
Sampling Depth Temperature Salinity Dissolved Bottom structure Station date (m) (ºC) (psu) oxygen number (Day/Mo/Yr) (mgl-1) 1 17.09.1998 1 20.0 21.1 10.6 Mud&Sand 2 19.10.1992 63 15.0 38.3 1.6 Mud 3 16.07.1992 60 14.9 38.2 1.3 Mud&Shell 4 19.10.1992 18 15.4 32.1 3.4 Shell 511.07.1991 45 14.7 36.6 1.4 Mud 611.07.1991 67 14.7 38.2 2.1 Mud 7 19.10.1992 71 14.6 38.4 1.6 Mud 8 17.09.1998 1 22.0 19.9 8.9 Mud&Gravel 9 17.07.1992 56 14.8 38.4 1.4 Mud 10 17.07.1992 83 14.9 38.6 1.3 Mud 11 20.10.1992 91 14.7 38.5 1.5 Mud 12 12.07.1991 83 14.9 38.4 1.2 Mud 13 17.07.1992 29 15.1 35.6 1.9 Mud 14 28.06.1993 16 14.6 32.2 3.6 Sand 15 28.06.1993 79 14.6 38.3 2.2 Mud 16 20.10.1992 18 15.6 34.3 3.2 Shell 17 20.10.1992 16 15.7 34.0 3.4 Sand 18 18.07.1992 29 14.9 36.6 2.7 Mud 19 20.10.1992 77 14.7 38.4 1.6 Rock 20 28.06.1993 84 14.6 38.4 2.3 Sand 21 18.07.1992 38 14.9 38.3 2.5 Sand 22 18.07.1992 63 14.9 38.6 1.1 Mud 23 18.07.1992 58 14.9 38.2 2.3 Mud 24 13.07.1991 57 14.9 38.2 2.2 Mud 25 18.07.1992 82 14.9 38.6 1.6 Mud&Shell 26 13.07.1991 85 15.0 38.5 1.7 Mud 27 21.10.1992 85 14.8 38.6 2.0 Mud 28 16.04.1992 63 14.6 38.4 2.7 Mud 29 08.08.1999 1 23.4 22.7 7.1 Sand 30 13.07.1991 53 14.9 37.9 2.8 Mud 31 21.10.1992 13 16.4 24.2 6.7 Mud 32 21.10.1992 13 16.2 24.9 6.0 Sand 33 19.07.1992 13 17.5 24.7 6.8 Sand 34 29.06.1993 19 15.8 31.7 5.4 Sand &Shell 35 29.06.1993 52 14.6 38.4 2.1 Mud&Shell 36 29.06.1993 65 15.0 38.0 1.2 Mud 12 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 1. cont’d
37 13.07.1991 45 14.9 38.2 2.3 Mud 38 22.10.1992 14 17.1 24.4 4.3 Mud 39 23.10.1997 32 14.5 37.0 2.8 Mud 40 17.04.1992 33 14.1 36.8 3.8 Mud 41 23.10.1997 13 18.9 24.2 7.0 Mud 42 14.07.1991 27 15.0 36.1 4.5 Mud 43 23.10.1997 12 19.0 24.1 6.6 Mud 44 23.10.1992 28 15.0 36.5 3.3 Mud 45 15.07.1991 30 14.9 36.1 6.3 Mud 46 20.07.1992 42 14.8 37.4 2.8 Mud&Shell 47 20.07.1992 42 14.8 37.5 3.0 Mud&Stone 48 14.07.1991 43 14.9 37.4 2.4 Mud 49 23.10.1992 41 14.8 37.3 3.1 Mud 50 30.06.1993 42 14.7 37.5 1.8 Mud 51 17.04.1992 18 13.5 33.7 7.2 Mud&Shell 52 10.08.1999 1 23.3 20.1 8.3 Sand 53 14.07.1991 65 14.8 38.5 2.0 Mud 54 14.07.1991 64 14.8 38.5 2.0 Mud&Shell 55 21.10.1992 15 16.0 27.9 4.1 Sand 56 15.04.1992 63 14.6 38.3 2.2 Mud 57 01.07.1993 24 15.2 36.0 4.5 Sand 58 15.07.1991 20 15.3 36.0 4.2 Sand 59 24.10.1992 13 16.0 24.4 5.3 Sand 60 15.07.1991 46 14.9 37.5 2.4 Mud 61 24.10.1992 45 14.9 37.5 3.7 Sand 62 15.07.1991 42 14.8 37.6 2.2 Mud 63 15.07.1991 105 14.7 38.6 1.3 Mud 64 22.07.1992 96 14.7 38.7 1.6 Mud 65 22.07.1992 52 14.8 38.3 2.2 Mud 66 24.10.1992 52 14.7 38.2 2.2 Mud 67 15.07.1991 52 14.9 38.2 2.1 Mud 68 15.07.1991 52 14.9 38.3 2.1 Mud 69 15.07.1991 24 15.1 35.0 4.3 Sand 70 22.07.1992 24 15.0 34.9 4.4 Mud 71 01.07.1993 22 15.1 34.7 4.7 Mud 72 22.07.1992 21 15.2 31.2 5.1 Mud 73 24.10.1992 14 16.4 24.5 5.2 Sand 74 01.07.1993 59 14.8 38.1 1.4 Mud 75 22.07.1992 43 14.9 37.1 1.6 Sand 76 16.07.1991 53 14.6 38.4 1.4 Mud ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 13
Table 1. cont’d
77 02.07.1993 42 15.1 37.3 1.8 Mud 78 16.07.1991 15 16.5 28.0 5.0 Sand 79 02.07.1993 82 14.7 38.4 1.1 Mud&Shell 80 16.07.1996 18 15.2 33.2 3.6 Sand 81 23.07.1992 88 14.6 38.6 0.9 Mud 82 16.07.1996 25 14.4 37.8 1.2 Mud 83 17.07.1996 20 15.0 34.6 1.4 Mud 84 17.07.1996 18 15.2 33.3 1.7 Mud 85 13.06.1999 1 22.7 20.3 10.0 Mud&Gravel 86 13.06.1999 1 22.7 20.3 10.0 Sand
RESULTS belonging to 49 genera and 28 families were identified during the course of this study. The Two hundred and five species belonging species, station numbers at which they were to 126 genera and 56 families were reported in found, and ecological characteristics of the find previously conducted studies. Fifty-nine species sites are provided in Table 2.
Table 2. Bivalve species found in the Sea of Marmara in previous studies and in this study*
Station no. Depth Temperature Salinity Dissolved Bottom (m) (ºC) (psu) oxygen substance (mgl-1) Solemyidae Solemya togata (Poli, 1795) Nuculidae Ennucula aegeensis (Forbes, 1844) Ennucula tenuis (Montagu, 1808) Nucula nitidosa (Winckworth, 1930) *Nucula nucleus (Linnaeus, 1, 8, 23, 47, 1-58 14.8-22.0 19.9-38.3 2.2-10.6 mud, muddy 1758) 65 sandy bottom *Nucula sulcata (Bronn, 1831) 9, 49, 65 41-56 14.8 37.3-38.4 1.4-3.1 mud bottom Nuculanidae Nuculana commutata (Philippi, 1844) Nuculana pella (Linnaeus, 1767)
Yoldiidae Yoldiella philippiana (Nyst, 1845) 14 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 2. cont’d
Arcidae Anadara corbuloides (Monterosato, 1878) *Anadara diluvii (Lamarck, 1805 2, 3, 5, 7, 9, 41-96 14.6-15.0 36.6-38.7 0.9-3.1 mud, sand 10, 11, 12, bottom 15, 22, 23, 24, 25, 27, 47, 48, 49, 50, 54, 60, 62, 64, 65, 66, 67, 68, 74, 75, 76, 79, 81 *Arca noae (Linnaeus, 1758) 47, 51 18-42 13.5-14.8 33.7-37.5 3.0-7.2 on stone and shell *Arca tetragona (Poli, 1795) 54 64 14.8 38.5 2.0 on shells Barbatia barbata (Linnaeus, 1758) Bathyarca grenophia (Risso, 1826) *Scapharca inaequivalvis (Bruguiere, 1789) Noetiidae Striarca lactea (Linnaeus, 1758) 8, 85 1 22.0-22.7 19.9-20.3 8.9-10.0 mud&gravel bottom Glycymerididae Glycymeris bimaculata (Poli, 1795) *Glycymeris glycymeris 33, 73 13-14 16.4-17.5 24.5-24.7 5.2-6.8 sand bottom (Linnaeus, 1758) Glycymeris insubrica (Brocchi, 1814) Glycymeris pilosa (Linnaeus, 1767) Mytilidae Lithophaga lithophaga (Linnaeus, 1758) Modiolarca subpicta (Cantraine, 1835) *Modiolula phaseolina (Philippi, 16 18 15.6 34.3 3.2 on shells 1844) *Modiolus adriaticus (Lamarck, 21, 33, 40 13-38 14.1-17.5 24.7-38.3 2.5-6.8 mud, sand 1819) bottom *Modiolus barbatus (Linnaeus, 35, 46 42-52 14.6-14.8 37.4-38.4 2.1-2.8 on shells 1758) ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 15
Table 2. cont’d
*Musculus costulatus (Risso, 80 18 15.2 33.2 3.6 on corals 1826) Mytilaster lineatus (Gmelin, 1791) Mytilaster minimus (Poli, 1795) Mytilus edulis (Linnaeus, 1758) *Mytilus galloprovincialis 1, 3, 4, 8, 1-79 13.5-23.4 19.9-38.3 1.3-10.6 mud, sand, (Lamarck, 1819) 14, 15, 29, muddy 31, 32, 38, sand, shell, 41, 43, 51, mud&shell, 52, 55, 59, mud&gravel 70, 71, 72, bottoms 80, 84, 85 Pinnidae Atrina pectinata (Linnaeus, 1767) *Pinna nobilis (Linnaeus, 1758) 3, 5, 7, 9, 20-83 14.4-15.1 34.6-38.6 1.1-1.8 mud bottom 10, 77, 79, 82, 83 Pinna rudis (Linnaeus, 1758) Pteriidae *Pteria hirundo (Linnaeus, 1758) 3, 19, 36, 60-82 14.7-15.0 38.0-38.4 1.1-1.6 on rock and 79 shells Pectinidae *Aequipecten opercularis 9, 13, 21, 20-56 14.1-15.3 34.9-38.4 1.4-4.4 mud, sand (Linnaeus, 1758) 40, 58, 70 bottom *Delectopecten vitreus (Gmelin, 36014.9 38.2 1.3 on shells 1791) Hyalopecten similis (Laskey, 1811) Lissopecten hyalinus (Poli, 1795) Chlamys flexuosa (Poli, 1795) Chlamys multistriata (Poli, 1795) Chlamys pesfelis (Linnaeus, 1758) Chlamys proteus (Dillwyn, 1817) *Chlamys varia (Linnaeus, 1758) 47, 48 42-43 14.8-14.9 37.4-37.5 2.4-3.0 mud bottom *Flexopecten glaber (Linnaeus, 5, 9, 14, 21, 16-56 14.6-15.3 32.2-38.4 1.4-4.2 mud, sand 1758) 58 bottom
Palliolum incomparabile (Risso, 1826) Palliolum striatum (Muller O.F., 1776) Pecten jacobeus (Linnaeus, 1758) 16 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 2. cont’d
Propeamussium fenestratum (Forbes, 1844) *Pseudamussium clavatum (Poli, 6, 10, 11, 41- 14.6-15.0 37.3-38.7 1.2-3.7 mud, sand 1795 ) 12, 25, 26, 105 bottom 30, 47, 49, 53, 61, 63, 64, 76 Spondylidae Spondylus gaederopus (Linnaeus, 1758) Spondylus gussonii (Costa O.G., 1829) Anomiidae *Anomia ephippium (Linnaeus, 1, 85 1 20.0-22.7 20.3-21.1 10.0-10.6 on algae 1758) Pododesmus aculeatus (Mueller O.F., 1776) Pododesmus patelliformis (Linnaeus, 1761) Pododesmus squamus (Gmelin, 1791) Limidae Lima lima (Linnaeus, 1758) Limaria hians (Gmelin, 1791) *Limaria tuberculata (Olivi, 33, 51 13-18 13.5-17.5 24.7-33.7 6.8-7.2 mud, sand 1792) bottom Limatula subauriculata (Montagu, 1808) Limea loscombii (Sowerby G.B.I., 1823) Ostreidae Crassostrea gigas (Thunberg, 1793) *Ostrea edulis (Linnaeus, 1758 ) 2, 3, 9, 10, 1-105 13.5-23.3 20.1-38.7 1.1-10.0 mud, sand, 11, 15, 22, mud&shell, 23, 24, 25, mud&gravel 26, 27, 28, bottom 47, 48, 49, 51, 52, 63, 64, 65, 66, 67, 68, 76, 79, 82, 85 Gryphaeidae Neopycnodonte cochlear (Poli, 1795) ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 17
Table 2. cont’d
Lucinidae Anadontia fragilis (Philippi, 1836) Ctena decussata (Costa O.G., 1829) Divaricella angulifera (Von Martens, 1880) *Loripes lacteus (Linnaeus, 8, 29, 85 1 22.0-23.4 19.9-22.7 7.1-10.0 sand, 1758) mud&gravel bottom Lucinella divaricata (Linnaeus, 1758) Lucinoma boreale (Linnaeus, 1767) *Myrtea spinifera (Montagu, 3, 9, 47, 63, 1-105 14.7-22.7 20.3-38.6 1.3-10.0 mud, sand, 1803) 85, 86 mud&gravel bottom Thyasiridae Leptaxinus eumyarius (Sars M., 1870) Thyasira flexuosa (Montagu, 1803) Thyasira granulosa (Monterosato, 1874) Ungulinidae Diplodonta brocchii (Deshayes, 1850) Diplodonta rotundata (Montagu, 1803) Chamidae Chama circinata (Monterosato, 1878) *Chama gryphoides (Linnaeus, 19, 25 77-82 14.7-14.9 38.4-38.6 1.6 on rock and 1758) shell Pseudochama gryphina (Lamarck, 1819) Galeommatidae Galeomma politum (Deshayes, 1855) Galeomma turtoni (Turton, 1825) Kelliidae Bornia sebetia (Costa O.G., 1829) 18 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 2. cont’d
Kellia suborbicularis (Montagu, 1803) Lasaeidae Hemilepton nitidum (Turton, 1822) Leptonidae Lepton squamosum (Montagu, 1803) Montacutidae Mancikellia pumila (Sowerby J. de C., 1846) Mysella bidentata (Montagu, 1803) Tellimya ferruginosa (Montagu, 1808) Neoleptonidae Neolepton sulcatulum (Jeffreyes, 1859) Sportellidae Sportella recondita (Fischer P., 1872) Carditidae Cardita calyculata (Linnaeus, 1758) Glans aculeata (Poli, 1795) Glans trapezia (Linnaeus, 1767) Venericardia antiquata (Linnaeus, 1758) Astartidae Astarte fusca (Poli, 1795) Gonilia calliglypta (Dall, 1903) Cardiidae Acanthocardia aculeate (Linnaeus, 1758) Acanthocardia deshayesi (Payraudeau, 1826) *Acanthocardia echinata 35, 37, 46, 18-52 14.6-15.2 33.3-38.4 1.7-3.1 mud bottom (Linnaeus, 1758) 47, 49, 50, 62, 67, 68, 84 Acanthocardia mucronata (Poli, 1795) ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 19
Table 2. cont’d
*Acanthocardia paucicostata 8, 31, 32, 1-82 14.5-22.7 19.9-38.4 1.1-10.0 mud, sand, (Sowerby G.B.II, 1834) 35, 38, 39, mud&shell, 41, 43, 44, mud&gravel 57, 71, 79, bottom 85 Acanthocardia spinosa (Solander, 1786) *Acanthocardia tuberculata 8, 12, 29, 1-83 14.9-23.4 19.9-38.4 1.2-8.9 mud, sand, (Linnaeus, 1758) 32, 38, 43, mud&gravel 52, 59, 61, bottom 75 Cerastoderma edule (Linnaeus, 1758) *Cerastoderma glaucum (Poiret, 1, 8, 29, 52, 1 20.0-23.4 19.9-22.7 7.1-10.6 mud, sand, 1789) 85 muddy sand bottom *Laevicardium crassum (Gmelin, 57, 62 24-42 14.8-15.2 36.0-37.6 2.2-4.5 mud, sand 1791) bottom Laevicardium oblongum (Gmelin, 1791) *Parvicardium exiguum (Gmelin, 52 1 23.3 20.1 8.3 sand bottom 1791) Parvicardium minimum (Philippi, 1836) Parvicardium ovale (Sowerby G.B.II, 1840) Parvicardium roseum (Lamarck, 1819) Parvicardium scabrum (Philippi, 1844) *Plagiocardium papillosum 32, 43, 55 12-15 16.0-19.0 24.1-27.9 4.1-6.6 mud, sand (Poli, 1795) bottom Mactridae Mactra glauca (Born, 1778) Mactra stultorum (Linnaeus, 1758) Spisula solida (Linnaeus, 1758) *Spisula subtruncata (Da Costa, 1, 8, 29, 31, 1-42 14.8-23.4 19.9-37.5 3.0-10.6 mud, sand, 1778 ) 47, 52, 86 muddy sand bottom Mesodesmatidae Donacilla cornea (Poli, 1795) Solenidae *Solen marginatus (Pulteney, 29, 31, 45, 1-82 14.7-23.4 22.7-38.4 1.1-7.1 mud, sand 1799) 69, 70, 79 bottom 20 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 2. cont’d
Pharellidae *Ensis ensis (Linnaeus, 1758 ) 29, 52, 57, 1-105 14.7-23.4 20.1-38.6 1.1-10.0 mud, sand 58, 59, 63, bottom 70, 79, 85 Ensis minor (Chenu, 1843) Ensis siliqua (Linnaeus, 1758) Phaxas adriaticus (Coen, 1933) Phaxas pellucidus (Pennant, 1777) Tellinidae *Gastrana fragilis (Linnaeus, 29 1 23.4 22.7 7.1 sand bottom 1758) Tellina balaustina (Linnaeus, 1758) Tellina distorta (Poli, 1791) Tellina donacina (Linnaeus, 1758) Tellina fabula (Gmelin, 1791) Tellina incarnata (Linnaeus, 1758) Tellina nitida (Poli, 1791) Tellina planata (Linnaeus, 1758) Tellina pulchella (Lamarck, 1818) Tellina pygmaea (Loven, 1846) *Tellina serrata (Brocchi, 1814) 18 29 14.9 36.6 2.7 mud bottom *Tellina tenuis (Da Costa, 1778) 1, 29, 52, 1 20.0-23.4 20.1-22.7 7.1-10.6 sand, muddy 86 sand bottom Donacidae *Donax trunculus (Linnaeus, 1, 8, 29, 52, 1 20.0-23.4 19.9-22.7 7.1-10.6 mud, sand, 1758 ) 86 muddy sand bottom Donax variegatus (Gmelin, 1791) Donax venustus (Poli, 1795) Psammobiidae Gari costulata (Turton, 1822) *Gari depressa (Pennant, 1777) 33, 52, 85 1-13 17.5-23.3 20.1-24.7 6.8-10.0 sand, mud&gravel bottom *Gari fervensis (Gmelin, 1791) 86 1 22.7 20.3 10.0 sand bottom Scrobiculariidae Scrobicularia plana (Da Costa, 1778) ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 21
Table 2. cont’d
Semelidae *Abra alba (Wood W., 1802 ) 1 1 20.0 21.1 10.6 muddy sand bottom Abra longicallus (Scacchi, 1834) *Abra nitida (Mueller O.F., 56 63 14.6 38.3 2.2 mud bottom 1776) Abra prismatica (Montagu, 1808) Abra renierii (Bronn, 1831) Abra segmentum (Recluz, 1843) Solecurtidae *Azorinus chamasolen (Da 39, 43, 47, 12-42 14.5-19.0 24.1-37.5 2.8-6.6 mud, sand Costa, 1778) 57 bottom Solecurtus multistriatus (Scacchi, 1834) Solecurtus scopula (Turton, 1822) Solecurtus strigilatus (Linnaeus, 1758) Kelliellidae Kelliella abyssicola (Forbes, 1844) Trapeziidae *Coralliophaga lithophagella 20 84 14.6 38.4 2.3 in holes of (Lamarck, 1819) corals Glossidae Glossus humanus (Linnaeus, 1758) Veneridae Callista chione (Linnaeus, 1758) *Chamelea gallina (Linnaeus, 1, 8, 14, 17, 1-18 14.6-23.4 19.9-34.0 1.7-10.6 mud, sand, 1758) 29, 43, 52, muddy sand 55, 84, 86 bottom Chamelea striatula (Da Costa, 1778) *Clausinella fasciata (Da Costa, 18, 62 29-42 14.8-14.9 36.6-37.6 2.2-2.7 mud bottom 1778) *Dosinia exoleta (Linnaeus, 17, 73 14-16 15.7-16.4 24.5-34.0 3.4-5.2 sand bottom 1758) Dosinia lupinus (Linnaeus, 1758) Globivenus effosa (Philippi ex Bivona ms., 1836) *Gouldia minima (Montagu, 1, 17, 32, 1-16 15.7-22.7 20.3-34.0 3.4-10.6 sand, 1803) 85 muddy sand, muddy&gravel bottom 22 ACTA ADRIATICA, 45(1): 9-26, 2004
Table 2. cont’d
Irus irus (Linnaeus, 1758) Pitar mediterranea (Tiberi, 1855) *Pitar rudis (Poli, 1795) 1, 8, 14, 17, 1-82 14.6-23.4 19.9-38.4 1.1-10.6 mud, sand, 29, 33, 41, muddy sand, 42, 43, 45, muddy&gravel, 57, 71, 72, mud&shell 73, 78, 79, bottom 80, 83, 84 *Paphia aurea (Gmelin, 1791) 43, 55 12-15 16.0-19.0 24.1-27.9 4.1-6.6 mud, sand bottom Paphia lucens (Locard, 1886) *Paphia rhomboides (Pennant, 29 1 23.4 22.7 7.1 sand bottom 1777) *Ruditapes decussatus 29 1 23.4 22.7 7.1 sand bottom (Linnaeus, 1758) Timoclea ovata (Pennant, 1777) Venerupis geographica (Gmelin, 1791) Venus casina (Linnaeus, 1758) Venus nux (Gmelin, 1791) *Venus verrucosa (Linnaeus, 8, 14, 18, 1-29 14.6-23.4 19.9-36.6 2.7-10.0 mud, sand, 1758) 29, 43, 52, mud&gravel 85 bottom Petricolidae *Mysia undata (Pennant, 1777) 29 1 23.4 22.7 7.1 sand bottom Petricola lithophaga (Retzius, 1786) Myidae Mya arenaria (Linnaeus, 1758) Sphenia binghami (Turton, 1822) Corbulidae *Corbula gibba (Olivi, 1792) 8, 9, 30, 32, 1-56 14.8-23.3 19.9-38.4 1.4-8.9 mud, sand, 41, 47, 52, mud&gravel 71 bottom Lentidium mediterraneum (Costa O.G., 1839)
Gastrochaenidae Gastrochaena dubia (Pennant, 1777) Hiatellidae *Hiatella arctica (Linnaeus, 1767) 34 19 15.8 31.7 5.4 on shells *Hiatella rugosa (Linnaeus, 1767) 14, 16, 51 16-18 13.5-15.6 32.2-34.3 3.2-7.2 in crevices of shells ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 23
Table 2. cont’d
Saxicavella jeffreysi (Winckworth, 1930) Pholadidae Barnea candida (Linnaeus, 1758) Pholas dactylus (Linnaeus, 1758) Teredinidae Bankia carinata (Gray J.E., 1827) Lyrodus pedicellatus (Quatrefages, 1849) Nototeredo norvegica (Spengler, 1792) Teredo navalis (Linnaeus, 1758) Xylophagidae Xylophaga dorsalis (Turton, 1819) Thraciidae Thracia convexa (Wood W., 1815) Thracia corbuloides (Deshayes, 1830) Thracia distorta (Montagu, 1803) Thracia papyracea (Poli, 1791) Thracia pubescens (Pulteney, 1799) Pandoridae Pandora inaequivalvis (Linnaeus, 1758) Pandora pinna (Montagu, 1803 Poromyidae Poromya granulata (Nyst and Westendorp, 1839) Cuspidariidae Cardiomya costellata (Deshayes, 1835) Cuspidaria abbreviata (Forbes, 1843) Cuspidaria cuspidata (Olivi, 1792) *Cuspidaria rostrata (Spengler, 9, 10, 63 56- 14.7-14.9 38.4-38.6 1.3-1.4 mud bottom 1793) 105
* Ecological characteristics are given for sites at which species were found in this study. 24 ACTA ADRIATICA, 45(1): 9-26, 2004
DISCUSSION AND CONCLUSIONS Venus verrucosa, Ruditapes decussatus, Hiatella arctica, Pholas dactylus, Lyrodus pedicellatus, The Bivalvia class is represented by 409 Bankia carinata, Cuspidaria rostrata) are species in the Mediterranean region (SABELLI cosmopolitan, 4 (Hemilepton nitidum, Mya et al., 1990) and 244 species in the Turkish seas arenaria, Hiatella rugosa, Xylophaga dorsalis) (ÖZTÜRK & ÇEVİK, 2000; DEMİR, 2003). So far, are boreal and 1 (Scapharca inaequivalvis) is 205 bivalve species have been identified in the Indo-Pacific. Sea of Marmara and its straits. Eleven of the Of the 244 species in the Turkish seas, 29 are 205 species (Solemya togata, Mytilus edulis, Mediterranean endemic, 15 are cosmopolitan, 4 Pinna rudis, Atrina pectinata, Crassostrea are boreal and 12 are Indo-Pacific. Only one gigas, Lucinoma boreale, Cerastoderma Indo-Pacific species is known to exist in the edule, Spisula solida, Ensis siliqua, Chamelea Sea of Marmara although all the cosmopolitan striatula, Pitar mediterranea) appear in our list and boreal species and a great portion of the although their presence in the Sea of Marmara Mediterranean endemic that exist in Turkish is questionable. In this study, 59 species were seas are also present in the Marmara. identified. Bivalvia fauna of the Sea of Marmara Approximately half of the Mediterranean could not be contributed, but, detailed data about species have been found in the Sea of Marmara. ecological characteristics of these 59 species DEMİR (2003) determined that 145 species were were provided. present but he collected material from 1951 to Most of the 205 species known to exist in the 1982. Therefore, his findings do not necessarily Sea of Marmara are of Atlanto-Mediterranean represent the present situation in the Sea of origin whereas 24 species (Nuculoma aegeensis, Marmara. Only 59 species were found in our Anadara corbuloides, Glycymeris bimaculata, current study, indicating that species richness G. pilosa, Mytilaster lineatus, M. minimus, has been negatively impacted by habitats Pinna nobilis, Delectopecten vitreus, Spondylus damaged by the construction of new ports and gussonii, Pododesmus aculeatus, Thyasira motorways along the edge of the sea and by granulosa, Bornia sebetia, Mancikellia pumila, domestic and industrial pollution. Sportella recondita, Gonilia calliglypta, Acanthocardia deshayesi, A. mucronata, A. spinosa, Phaxas adriaticus, Tellina fabula, ACKNOWLEDGEMENTS Abra renierii, Solecurtus multistriatus, Kelliella The authors are grateful to Dr. J.M. POUTIERS abyssicola, Lentidium mediterraneum) are from Museum National d’Histoire Naturelle, endemic to the Mediterranean, 15 (Bathyarca Paris, and Dr. S. SCHIAPARELLI from Istituto di grenophia, Lithophaga lithophaga, Lima lima, Scienze Ambientali Marine, Genova, for their Crassostrea gigas, Divaricella angulifera, Kellia valuable help in confirmation of determined suborbicularis, Cerastoderma edule, Ensis ensis, species and in providing some literature. ALABAYAK, BALKIS & BALKIS: Bivalvia (Molluca) fauna of the Sea of Marmara 25
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Received: 8 January 2002 Accepted: 9 December 2003
Fauna školjkaša (mekušaca) Mramornog mora
Serhat ALBAYRAK, Hüsamettin BALKIS i Neslihan BALKIS
Sveučilište u Istanbulu, Fakultet Znanosti, Odsjek Biologije, 34118 Vezneciler-Istanbul, Turska E-mail: [email protected]
SAŽETAK
Cilj ovih istraživanja je bio odrediti faunu školjkaša u Mramornom moru kao i neke njihove ekološke karakteristike. Materijal je prikupljen na 86 od 254 proučavane postaje u periodu od 1990. do 1999. godine. Pronađeno je 59 vrsta iz 49 rodova i 28 porodica. Popis ovih vrsta je dat zajedno s 205 prethodno nađenih vrsta. Iznose se podaci o hidrografskim uvjetima kao što su salinitet, temperatura i otopljeni kisik. Zabilježen je manji broj vrsta u usporedbi s prethodnim uzorkovanjima, iz čega se zaključuje da gradnja luka i cesta uz obalu doprinosi uništavanju habitata kao što to također čine industrijski i urbani otpad.
Ključne riječi: Bivalvia, mekušci, Mramorno more ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.585.1 (262.4) AADRAY 45 (1): 27-33, 2004 Preliminary report
Preliminary determination of batch fecundity of Grass goby (Zosterisessor ophiocephalus Pallas, 1811) in Izmir Bay (Aegean Sea)
Okan AKYOL, Tülin ÇOKER and Ali KARA
Faculty of Fisheries, Ege University, 35100 Bornova, Izmir, Turkey
In Izmir Bay (Aegean Sea), the grass goby (Zosterisessor ophiocephalus) reproduces between February and May. In February, the maximum batch fecundity of hydrated oocytes was 16272. The relationship between total length and batch fecundity was F = 4.5423L2.4236 (r = 0.306) according to the oocyte size-frequency method and F = 2.9005L1.6576 (r = 0.073) according to the hydrated oocyte method. The relationship between gonad free weight and batch fecundity was F = 1340.5 + 92.695W (r = 0.328) and F = -2866 + 163.15W (r = 0.528), according to the above methods, respectively. The correlation between the relationships was low. The oocyte and yolk compact mass diameters were 43-1376 µ and 301-774 µ, respectively. The length at earliest maturity for females was 9.8 cm.
Key words: Grass goby, Zosterisessor ophiocephalus, batch fecundity, oocyte diameter, Izmir Bay, Aegean Sea
INTRODUCTION sardine, Sardina pilchardus (CIHANGIR, 1996), the common sole, Solea vulgaris (HOSSUCU & The grass goby, Zosterisessor ophiocephalus ÇOKER, 1997) and the John Dory, Zeus faber, is one of 56 Gobiid species found throughout the (AKYOL & ÇOKER, 2001). Mediterranean Sea. It is a predator that inhabits This study aims to determine oocyte diameters, first maturity length and batch coastal sea areas, estuaries, sandy and muddy fecundity of the grass goby using samples taken biotopes of lagoons, sea meadows and roots of from the shore of Izmir Bay during the goby marine plants (MILLER, 1986; PATZNER, 2000). reproduction period. The grass goby is found throughout the Black Sea where it reproduces in April-May in the Tuzlov estuaries and in July along the Varna MATERIAL AND METHODS coast (MILLER, 1986). The grass goby reproduces in March-May in the northern Adriatic Sea One hundred forty-one grass goby (PATZNER et al., 1991) and February-May in Izmir (Zosterisessor ophiocephalus) females (mean Bay (AKYOL, 2003). total length 134±2.14 mm, mean weight The few studies concerning the number 27.9±15.4 g) were obtained using fyke nets (24 of eggs spawned in the Aegean Sea by serial mm mesh size) from depths of 0.5-1 m along the spawners include the anchovy, Engraulis Bostanlõ coast of Izmir Bay (Fig. 1) in February- encrasicolus (CIHANGIR & USLU, 1992), the April 2000. 28 ACTA ADRIATICA, 45(1): 27-33, 2004
Fig. 1. The sampling area
The mature gonads of twenty-six of the females had ripe gonads. The length were removed and fixed in a 4% buffered that corresponded with this proportion was formaldehyde solution. The batch fecundity considered the earliest maturity length (KOHLER, was estimated by the “oocyte size frequency” 1960; WAIWOOD & BUZETA, 1989). and the “hydrated oocyte” methods (HUNTER et al., 1985). Three samples (3 g each) were taken from the middle, the front and the back of the RESULTS each gonad (ovary). Samples were spread with µ glycerine in a glass PETRI dish. Oocytes were Oocyte diameters ranged 43-1376 (Fig. counted (n = 12822) and their diameters (yolk 2). The fact that small oocytes and hydrated compact mass n = 589) were measured under oocytes are seen together in this species a binocular microscope (x 20). Oocytes greater indicates that there it is a group synchronous than 430 µ diameter were defined as “large ovary. According to the KRUSKAL-WALLIS test, oocytes”. Statistical differences between oocyte there were statistical differences between oocyte diameters in the sampling months were tested diameters in sampling months (p≤0.05). Yolk with the KRUSKAL-WALLIS nonparametric test compact mass diameters in hydrated oocytes µ (SUMBULOGLU & SUMBULOGLU, 2000). ranged 301-774 (Fig. 3). Total length:batch fecundity (F) and gonad The total length:batch fecundity relationship free weight:batch fecundity relationships was F = 4.5423L2.4236 (r = 0.306) and F = were calculated by power (F = aLb) and linear 2.9005L1.6576 (r = 0.073) according to the (F = c + dW) regressions, respectively, where L “oocyte size frequency” (Fig. 4) and “hydrated is total length (cm), W is weight without gonad oocyte” (Fig. 5) methods, respectively. The (g), and a, b, c and d are constants. gonad free weight:batch fecundity relationship The gonads in 141 females were examined was F = 1340.5 + 92.695W (r = 0.328) and F = and classified as ripening or ripe. Earliest -2866 + 163.15W (r = 0.528) according to the maturity was determined when at least 50% same two methods (Figs. 6, 7), respectively. AKYOL, ÇOKER & KARA: Preliminary determination of batch fecundity of Grass goby 29
Fig. 2. Oocyte diameters of grass goby, by month Fig. 3. Yolk compact mass diameters at the vegetal pole of maturing oocytes in grass goby, by month
Fig. 4. Total length:batch fecundity relationship according to oocyte size-frequency method
Fig. 5. Total length:batch fecundity relationship according to hydrated oocyte method 30 ACTA ADRIATICA, 45(1): 27-33, 2004
Fig. 6. Gonad free weight:batch fecundity relationship according to oocyte size-frequency method
Fig. 7. Gonad free weight:batch fecundity relationship according to hydrated oocyte method
The first maturity length of female grass goby was 9.8 cm (Table 1, Fig. 8).
Table 1. Frequency of ripe and ripening ovaries of grass goby, by length
Total length Number Ripening Ripe Ripe Consisting of three (cm) (no.) (no.) (%) fluid means 9 2 2 0 0 44.2 10 11 4 7 63.6 65 11 29 9206965 12 24 9 15 62.5 66.4 13 27 10 17 63 71.5 14 19 5 14 73.7 75.5 15 9 2 7 77.8 76 16 8 2 6 75 73.3 17 8 2 6 75 91.7 18 2 0 2 100 100 19 2 0 2 100 100 Total 141 45 96 AKYOL, ÇOKER & KARA: Preliminary determination of batch fecundity of Grass goby 31
Fig. 8. Earliest maturity length of female grass goby in the Bay of Izmir
DISCUSSION AND CONCLUSIONS faber) in the Aegean Sea as r = 0.539 for length according to the hydrated oocyte method and Oocyte diameters of the grass goby ranged r = 0.30 for body weight. 43-1376 µ; yolk compact mass diameters of The earliest maturity length of grass goby is hydrated oocytes ranged 301-774 µ. Maximum 9.8 cm in Izmir Bay. MILLER (1986) reported that batch fecundity was 16272 in February. MILLER the age at earliest maturity is 2-3 years. (1986) reported that the oocyte diameter of this Grass goby is the most important live species when spawning is approximately 2.6 bait for coastal longline fisheries for sea bass x 0.8 mm and its fecundity is 10000-45000. (Dicentrarchus labrax) in the Aegean Sea. The oocyte diameter found by MILLER is much Sustaining grass goby depends on knowing its greater than our findings because it referred to first maturity length and reproduction period. fertilized oocytes. As far as we know, no scientific studies have There was low correlation between body previously been conducted on this species length or weight and batch fecundity. Low in this area. Further, there are no seasonal correlation was not unexpected and similar closure or minimum landing size regulations findings were reported by URBAN (1988) for the in the fisheries records or circular. It is of great common sole (Solea solea) in German Bight as importance that the reproduction biology and r = 0.12, by HOSSUCU & ÇOKER (1997) in the other population parameters of grass goby be same species in Izmir Bay as r = 0.56, and by investigated in detail to ensure that this species AKYOL & ÇOKER (2001) for the John Dory (Zeus will remain in Izmir Bay.
REFERENCES
AKYOL, O. 2003. Age, growth and reproduction CIHANGIR, B. 1996. Reproduction of European period of grass goby (Zosterisessor pilchard, Sardina pilchardus (Walbaum, ophiocephalus Pallas, 1811) in the Bay of 1792) in the Aegean Sea (in Turkish). Tr. J. Izmir (Aegean Sea). Arch. Fish. Mar. Res., of Zoology, 20: 33-50. CIHANGIR, B. & B. USLU. 1992. A preliminary 50(2): 220-224. study on determination of batch fecundity of AKYOL, O. & T. ÇOKER. 2001. A preliminary study anchovy (Engraulis encrasicolus L., 1758) on determination of batch fecundity of John in the Aegean Sea (in Turkish). Doğa-Tr. J. Dory (Zeus faber L., 1758) in the Aegean of Zoology, 16: 301-310. Sea (in Turkish). Anadolu Üniversitesi Bilim HOSSUCU, B. & T. ÇOKER. 1997. Determination of batch fecundity of common sole (Solea ve Teknoloji Dergisi, 2(1): 167-172. 32 ACTA ADRIATICA, 45(1): 27-33, 2004
vulgaris Quensel, 1806) in Izmir Bay (in PATZNER, R. A. 2000. Mediterranean Gobies. Turkish). E.Ü. Su Ürünleri Dergisi, 14(1-2): Inst. of Zool. Univ. of Salzburg, Austria, 13-17. www.zoologie.sbg.ac.at/Patzner/Gobiidae. HUNTER, J.R., N. C. H. LO & R. J. .H. LEONG. 1985. PATZNER, R. A., M. SEIWALD, S. ANGERER, E. A. Batch fecundity in multiple spawning fishes. FERRERO & P. G. GIULIANINI. 1991. Genital In: An egg production method for estimating system and reproductive cycle of the male biomass of pelagic fish: Application to the grass goby, Zosterisessor ophiocephalus (Teleostei, Gobiidae), in the northern northern anchovy, Engraulis mordax, R. Adriatic Sea. Zool. Anz., 226 (5/6): 205- Lasker (Editor). NOAA Tech. Rep. NFMS, 219. 36, pp. 67-77. SUMBULOGLU, K. & V. SUMBULOGLU. 2000. KOHLER, A. C. 1960. The growth, length-weight Biostatistics (in Turkish). Hatiboğlu relationship and maturity of haddock Yayõnlarõ 53, 9. Baskõ, Ankara, 269 pp. (Melanogrammus aeglefinus L.) from the URBAN, J. 1988. Determination of batch region of Lockeport, N.S. J. Fish. Res. Bd. fecundity in plaice, Pleuronectes platessa, Canada, 17 (1): 41-60. and sole, Solea solea from the German MILLER, P. J. 1986. Gobiidae. In: P.J.B. Bight. ICES, CM., 51: 1-6. Whitehead, M.L. Bauchot, J.C. Hureau, WAIWOOD, K. G. & M. I. BUZETA. 1989. J. Nielsen and E. Tortonese (Editors). Reproductive biology of southwest Scottian Fishes of the Northeastern Atlantic and the shelf haddock (Melanogrammus aeglefinus). Mediterranean. UN, Paris, pp.1019-1085. Can. J. Fish. Aquat. Sci., 46: 153-170.
Received: 26 July 2002 Accepted: 13 January 2004 AKYOL, ÇOKER & KARA: Preliminary determination of batch fecundity of Grass goby 33
Preliminarno izvješće o jednokratnom fekunditetu glavoča (Zosterisessor ophiocephalus Pallas, 1811) u Izmirskom zaljevu (Egejsko more)
Okan AKYOL, Tülin ÇOKER i Ali KARA
Egejsko Sveučilište, Ribarstveni fakultet, 35100 Bornova, Izmir, Turska
SAŽETAK
Glavoč (Zosterisessor ophiocephalus) se u Izmirskom zaljevu višekratno mrijesti u periodu između veljače i svibnja. Maksimalni pojedinačni fekunditet hidriranih oocita je iznosio 16272 u veljači. Odnos između ukupne duljine i jdenokratnog fekunditeta je iznosio F=4.5423L2.4236 (r=0.306) i F=2.9005L1.6576 (r=0.073) prema “metodi veličine-zastupljenosti oocita” te “metodi hidracije oocita”. Težina gonada u odnosu na višekratni (serijski) fekunditet iznosila je F=1340.5+92.695W (r=0.328) i F=-2866+163.15W (r=0.528) prema gore navedenim metodama. Korelacije između ovih odnosa su slabe. Promjer oocita i kompaktne mase žumanjčane kesice varirao je od 43 µ do 1376 µ, odnosno 301 µ - 774 µ. Pri prvom mriješćenju u Izmirskom zaljevu (Egejsko more) duljina ženki je iznosila 9.8 cm.
Ključne riječi: Glavoč, Zosterisessor ophiocephalus, višekratni fekunditet, promjer oocita, Izmirski zaljev, Egejsko more
ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.5: (595.1) AADRAY 45 (1): 35-41, 2004 Original scientific paper
Parasite Fauna of Greater weever (Trachinus draco Linnaeus, 1758)
Ahmet AKMIRZA
University of İstanbul, Faculty of Fisheries, İstanbul, Turkey e-mail: [email protected]
A lot of 87 greater weever ( Trachinus draco Linnaeus, 1758 ) caught in the period April - May 2002 around the Gökçeada were investigated parasitologically. In 57 ( 65.52 % ) of these fish, 5 species of parasites were observed. The parasites were determined as Aspinatrium trachini (Monogenea), Helicometra fasciata (Digenea), Contracaecum fabri (Nematoda), Botriocephalus scorpii (Cestoda) and Stibadobdella loricata (Hirudinea).
Key words: Gökçeada, Greater weever, Monogenea, Digenea, Nematoda, Certoda, Hirudinea
INTRODUCTION thorns on its dorsal fins that are strong enough to cause serious injuries. The demand for food is increasing with the There are some studies of Gökçeada in the increase of the world population, so countries literature (TARKAN, 2000; AVŞAR & ERGIN, 1988; are taking measures to meet this need. One of DEDE, 1998; AKMIRZA, 2002), but there are no these measures is to utilize water resources to studies of the parasite fauna of the greater the utmost. Fishing and farming are the major weever. Our objective is to fill this gap. ways of usage. Parasites and their effects, which are not noticed in their habitat despite MATERIALS AND METHODS of causing many problems and being frequently encountered during growth, adversely affect this Greater weever samples caught by gill nets progress. and long-line in April and May 2002 were put Approximately, 300 fish species are living in aquariums in the laboratory and were kept in the Aegean Sea (KOCATAŞ & BILECIK, 1992) alive until its sacrifice and dissection. Firstly which forms a rich biotope for fisheries, and ectoparasite and then endoparasites were 144 species around Gökçeada (ULUTÜRK, 1987). studied in these investigations. Ectoparasites The greater weever, which is a commercially and endoparasites were put in Petri dishes with important fish in many countries, is not seawater and physiologic water respectively. considered commercially interesting in Turkey, These parasites were observed in vivo: despite its delicious meat (YÜCE, 1998). The Monogenea samples were placed in 70 % major reason for this is the presence of poisonous alcohol solution Digenea, Nematoda and 36 ACTA ADRIATICA, 45(1): 27-33, 2004
Cestoda samples were placed in AFA solution Cestoda, and Hirudinea group. 33, 22, and 2 to be used for further investigations. All found fish were parasitized upon by species 1, 2, and parasites were processed by standard methods 3, respectively. The parasite species detected in (BYLUND et al. 1980; KRUSE & PRITCHARD, 1982) the greater weever and their infection rates are for examination by light microscopy. Latter on given in the Table 1. The data of polyparasitism samples were also prepared as permanent slides are given in the Table 2. The systematic, and photographed. The following papers of morphologic and anatomic properties and BYKHOSKAYA-PAVLOVSKAYA et. al. 1964; PETTER original photographs of these parasites are & MAILLARD, 1987; YAMAGUTI,1958,1959,1962, shown below. 1963; DEMIRSOY,1998 were used for identification of the parasites. The paper of AKŞIRAY, 1987 Systematic accounts was used for identification of the fish. The measurements were carried out by using a Class : Trematoda micrometric ocular. Order : Monogenea RESULTS Family : Microcotylidae Aspinatrium trachini (Parona & In total 87 of the greater weever caught Perugia,1889) around the Gökçeada were investigated Synonym : Microcotyle trachini Parona & parasitologically. The parasites were found Perugia, 1889 in 57 of them (65.52 %), 5 species of which belong to Monogenea, Digenea, Nematoda, Microcotyle draconis Briot, 1904
Table 1. Parasites species detected in the greater weever caught around Gökçeada and their infection rates (N.F.I.: Number of Fish Investigated; N.F.P.: Number of Fish with Parasite; T.N.P: Total Number of Parasites)
Species of parasites Habitat N.F.I. N.F.P. T.N.P. Prevalence Abundance found Min. Max. Ave. Aspinatrium trachini Gill 87 6 9 6.90 1 3 1.5 Helicometra fasciata Intestine 87 19 73 21.84 2 9 3.84 Contracaecum fabri Intestine 87 52 461 59.77 1 23 8.87 Bothriocephalus scorpii Intestine 87 5 26 5.75 2 11 5.2 Stibarobdella loricata Skin 87 1 1 1.15 1 1
Table 2. The data of polyparasitism in Greater weever
N.F.I. Number of fish with With one With two species With tree species parasite species
N%N%N%N% 87 57 65.52 33 37.93 22 25.29 2 2.30
AKMIRZA: Parasite fauna of great weever 37
Fig. 1. Aspinatrium trachini Fig. 2. Helicometra fasciata
Length 3.2 (2.7 – 4.1) mm, width 0.7 Body is oval: 2.2 (1.9-2.6) mm in length, (0.62 – 0.79) mm, mouth located subterminally 0.67 (0.61-0.70) mm in width. Mouth sucker is subterminal, circular ( diameter: 0.17 mm). and ventrally, testes are approximately 50-55 Prepharynx and esophagus are short. Ceca in number, clamps consist of two raws in the terminating at posterior extremity. Ventral sucker prohaptor are approximately symmetric and are is in the anterior region, and has a diameter of number approximately 18-26 and similar in 0.25 mm. Two testes (length about 0.33 (0.3 size (0.09 mm). –0.4) mm) with lobes are localized tandem. Ovary also with lobes is placed in front of the testes. Uterus is winding between ovary and Order : Digenea ventral sucker. The pear shaped eggs are 0.075 Family : Opecoelidae mm in length and 0.03 mm in width.
Helicometra fasciata (Rudolphi, 1819 ) Class : Nematoda Synonym : Distoma fasciatum Rudolphi, Order : Ascarida 1819 nec Stossich,1885 Family : Anisakidae Allocreadium fasciatum (Rudolphi,1819) Contracaecum fabri ( Rudolphi,1819 ) Odhner,1902 Synonym : Ascaris fabri Rudolphi,1819 Helicometra mutbilis Stossich, 1903 In the larval phase, the species is of 18 (10- 28) mm in length and the esophagus 0.62 38 ACTA ADRIATICA, 45(1): 35-41, 2004
Fig. 3. Contracaecum fabri
(0.32-1.42) mm. The intestinal caecum is short Family: Bothriocephalidae 0.069 (0.055 - 0.082 mm) and the esophageal Bothriocephalus scorpii ( Müller, 1779 ) caecum is long (0.87 (0.59 - 1.48) mm. Synonym: Bothriocephalus punctatus (Rudolphi,1802 ) Class: Cestoda Bothriocephalus bipunctatus (Zeder, 1800) Order: Pseudophyllidea
Fig. 4. Botriocephalus scorpii AKMIRZA: Parasite fauna of great weever 39
Fig. 5. Stibarobdella loricata
This species is characteristic with its long, DISCUSSION AND CONCLUSIONS flat, almost rectangular head with apical discs, In this study, 570 parasites belonging to 5 and two lobes. The head is 1.5 (0.85-2.6) mm in species was encountered in 57 greater weever lenght and 0.39 (0.31-0.47) mm in width. There from a sample of 87. The species most often isn’t any neck. Segmentation starts at backside observed was Contracaecum fabri of head. Strobila has many proglotis, which (Nematode) with a prevalence of 59,77%. are narrow near the head, and more and more This parasite is not host specific, but is seen in enlarged approaching to the end. many species of fish. This parasite was found
in 23 fish species around the Adriatic Sea Class : Hirudinea (PETTER & RADUJKOVIĆ, 1989). Near Gökçeada Order : Rynchobdella 2 fish species that belong to the Sparidae family Family : Piscicolidae (Diplodus annularis, Spondyliosoma cantharus) Stibarobdella loricata (Schmarda, 1861) also were observed carrying this parasite (AKMIRZA, 2000). This parasite has a trunk that can be flung Helicometra fasciata (Digenea) is the second out at the front end of the digestive system, there most prevalent parasite after Contracaecum is evidence of oral and caudal suckers, and a fabri with a prevalence of 21,84 % and is cylindrical body. There are three annuli per observed in many fish species (RADUJKOVIĆ et segment. This parasite has not eyespot on the al., 1989). This parasite was found in 7 different caudal sucker, but has a lot of photoreceptors. fish species around the Gökçeada besides the This parasite is 6.95 mm in length and 0.61 mm greater weever (AKMIRZA, 2001). in width. The lengths of front and rear suckers Aspinatrium trachinii, a monogenetic are 0.33 and 0.22 mm respectively, and the trematod, is specific to the greater weever and width of both is 0.28 mm. 40 ACTA ADRIATICA, 45(1): 35-41, 2004 was observed on Trachinus radiatus as well as between 200-400, whereas the abundance value on Trachinus aeraneus (PAPOUTSOGLOU, 1976, is much lower for the greater weever encountered RADUJKOVIĆ,1989). in Turkey (PORA, 1979). The abundance values The damage caused by parasites in fish of the other parasites are also low, therefore it differs not only with the species of parasite, but can be concluded that the parasitic risk is very also with the abundance of these parasites. The low around the Gökçeada. abundance of nematode parasites in some fish is
REFERENCES
AKMIRZA, A. 2000. Seasonal Distribution of DEMIRSOY, A. 1998. The basic Principles of Life. Parasites Detected in Fish Belonging to the Invertebrata (In Türkish). II (1): Ankara, Sparidae Family Found near Gökçeada (in pp. 682-693. Turkish). T. Parazitol. Derg. 24 (4): 435- KOCATAŞ, A. & N. BILECIK. 1992. Aegean Sea and 441. its living Resources. (in Turkish ). Bodrum AKMIRZA, A. 2001. The Samples from Metazoon Su Ürünleri Araştõrma Enstitüsü Yayõnlarõ. Parasites Detected in Fish around Gökçeada Ser. A, No 7, 88 pp. (in Turkish ). Ulusal Ege Adalarõ 2001 KRUSE, G. O. W. & M. H. PRITCHARD. 1982. The Toplantõsõ Bildiriler Kitabõ. TÜDAV Yayõn Collection and Preservation of Animal No. 7: 85-96. Parasites. Technical Bulletin. The Harold W. AKMIRZA, A. 2002. Parasites of the Wanter Laboratory. 12:1-82. Acanthocephala and Cestoda Species Found PAPOUTSOGLOU, S.E. 1976. Metazoon Parasites in Fishes Caugth near Gökçeada (in Turkish). of Fishes from Saronicos Gulf, Athens, T. Parazitol. Derg. 26(1) : 93-98. Greece. Thalasogr., 1: 69-102. AKŞIRAY, F. 1987. Identification of Turkish PETTER, J.A.& C. MAILLARD. 1987. Ascarides Marine Fish (in Turkish). İ.Ü. Rektörlüğü de Poissons de Méditerranée occidentale. Yayõnlarõ. No. 3490 İstanbul, pp. 565-572. Bull.Mus.natn.Hist.nat.,Paris, 4e ser. 9: 773- AVŞAR, N. & M. ERGIN. Spatial Distribution 798. of Holocene Bentic Foraminifera at the PETTER, A. & B. M. RADUJKOVIĆ. 1989. Parasites Gökçeada-Bozcaada-Çanakkale Triangle des Poissons Marins du Montenegro: (NE Aegean Sea). 1998 . Third International Nematodes. Acta Adriat., 30 (1/2): 195-236. Turkish Geology Symposium. 31 August- 4 PORA, E. 1979. Le Chinchard de la mer Noire September, 1998. METU, Ankara-Turkey, (Trachurus mediterraneus ponticus ) Abstract, 117 pp. Institut Roumain de Recherches Marines, BYKHOVSKAYA-PAVLOVSKAYA, I. E. et al. 1964. Constantsa, pp. 625-641. Key to Parasites of Freshwater of the USSR. RADUJKOVIĆ, B. M., P. ORECCHIA & L. PAGGI. Translated from Russian. Israel Program for 1989: Parasites des Poissons Marõns du Scientific Translations. Jerusalem. pp.615- Montenegro: Digenes. Acta Adriat., 30(1/ 627. 2): 137-187. BYLUND, G., H.P. FAGERHOLM, G. CALENIUS & B.J. RADUJKOVIĆ, B. M. & L. EUZET. 1989. Parasites WINGREN. 1980 . Parasites of Fish in Finland des Poõssons Marins du Montenegro: II. Metods for Studying Fauna In Fish. Acta Monogenes. Acta Adriat., 30(1/2): 51-135. Academiae. Se.B. Vol. 40 (2) 23 pp. TARKAN, A.N. 2000. Abundance and Distrbution DEDE, A. 1998. Investigation on the of Zooplankton in Coastral Area of Mediterranean Monk Seal (Monachus Gökçeada Island (Northern Aegean Sea). monachus (Hermann,1779) in Gökçeada Türkish J.Mar. Sci., 6(3): 201-214. Island (Northern Aegean Sea ). Rapp. ULUTÜRK, T. 1987. Fish Fauna and Environmental Comm. Int. Mer. Médit. 35 : 534-535 Fon Radioactity of Gökçeada Area (in AKMIRZA: Parasite fauna of great weever 41
Turkish ). İ.Ü. Su Ürünleri Derg. 1(1) : 95- YAMAGUTI, S. 1962. Systema Helminthum. 119. Nematodes. Inst.Sc.Pbl. New York-London. YAMAGUTI, S. 1958. Systema Helminthum. pp.22-31. The Digenetic Trematodes of Vertebrates. YAMAGUTI, S. 1963. Systema Helminthum. Monogenea and Aspidocotylea. Inst.Sc.Pbl. Inst.Sc.Pbl. New York-London, pp. 22-145. New York-London, pp. 95-145. YAMAGUTI, S. 1959. Systema Helminthum. The YÜCE, R. 1998. The Fishes living in Turkish Cestodes of Vertebrates. Inst.Sc.Pbl. New Seas (in Turkish). Marmara Üniversitesi York-London, pp. 43-48. İstanbul, 633: 360-361.
Received: 28 October 2002 Accepted: 9 December 2003
Parazitska fauna pauka bijelca (Trachinus draco Linnaeus, 1758)
Ahmet AKMIRZA
Sveučilište u Istanbulu, Ribarstveni Fakultet, Istanbul, Turska
e-mail: [email protected]
SAŽETAK
Između travnja i svibnja 2000. godine uhvaćeno je oko otoka Gökçeada 87 primjeraka pauka bijelca (Trachinus draco Linnaeus, 1758) na kojima je izvršena parazitološka analiza. U 57 riba ( 65.52 % ), pronađeno je 5 vrsta parazita, a to su Aspinatrium trachini (Monogenea), Helicometra fasciata (Digenea), Contracaecum fabri (Nematoda), Botriocephalus scorpii (Cestoda) i Stibadobdella loricata (Hirudinea).
Ključne riječi: Gökçeada, pauk bijelac, Monogenea, Digenea, Nematoda, Cestoda, Hirudinea
ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.58:591.13(262.3-191.2) AADRAY 45 (1): 43-50, 2004 Original scientific paper
Diet composition and feeding intensity of Mediterranean horse mackerel, Trachurus mediterraneus (Osteichthyes: Carangidae), in the central Adriatic Sea
Mate ŠANTIĆ1, Ivan JARDAS 2 and Armin PALLAORO2
1Department of Biology, Faculty of Science, University of Split, 21000 Split, Croatia e-mail: [email protected]
2 Institute of Oceanography and Fisheries, 21000 Split, Croatia e-mail: [email protected]; e-mail: [email protected]
Diet composition and feeding intensity of the Mediterranean horse mackerel, Trachurus mediterraneus, collected in the central Adriatic Sea were examined. Stomach contents of 1200 specimens, taken at monthly intervals (January-December, 1996) were analyzed. The stomach contents consisted of six major prey groups: Crustacea (Euphausiacea, Mysidacea, Decapoda), Cephalopoda, Polychaeta and Teleostei. Euphausiacea constituted the most important food resource by weight, number and frequency. Teleosts were the second most important food category, while Mysidacea, Decapoda, Cephalopoda and Polychaeta were occasional foods. Euphausicea were dominant during all seasons, and especially abundant in summer and autumn. Feeding intensity varied throughout the year. The lowest feeding intensity was recorded in winter at lower sea temperatures and during spawning (May, June). Feeding activity increased just prior to (April) and after (July, August) spawning. Feeding intensity also varied during the diurnal cycle. The highest feeding intensity was recorded at night and during early morning hours.
Key words: Trachurus mediterraneus, food composition, feeding intensity, Adriatic Sea
INTRODUCTION statistical data on T. mediterraneus landings in the Adriatic Sea but the annual catch can Mediterranean horse mackerel, Trachurus be tentatively estimated at 400 tons. In the mediterraneus (STEINDACHNER, 1868), is Mediterranean, however, it constitutes a large distributed throughout the Mediterranean, portion of pelagic and demersal fisheries and the Black, and the northeastern Atlantic landings, and fluctuated from 5 120 to 109 560 (SMITH-VANIZ, 1986) seas. In the Adriatic, T. tons in 1989-98 (FAO, 2000). In the Adriatic, the mediterraneus is a schooling semi-pelagic species has remained abundant compared to species, most commonly found at depths of economically important and over-fished species 20-200 m (JARDAS, 1996). It spawns in late (VRGOČ, 2000). Despite its abundance, very little spring and early summer (ARNERI & TANGERINI, is known about the trophic ecology of this 1984; VIETTE et al., 1997). There are no reliable species in the Adriatic. Information on the diet 44 ACTA ADRIATICA, 45(1): 43-50, 2004 of T. mediterraneus in the Adriatic indicates were collected from January to December that its main diet comprises crustaceans and 1996 and 1200 specimens (100 specimens per fish (LIPSKAJA, 1966; BINI, 1968; TORTONESE, month), ranging 11.6-38.0 cm, were examined. 1975). BEN-SALEM (1988) and KYRTATOS (1998) The fish were measured to the nearest 0.1 cm presented more detailed information about the (total length) and 0.1 g. The fish were dissected diet of this species in the Mediterranean. immediately after capture and the gut was The purpose of the present study was to removed and preserved in a 4% formaldehyde determine diet composition and feeding intensity solution to prevent further digestion. Evidence of Mediterranean horse mackerel during the year of regurgitation was never observed in any of and during the day in the eastern Adriatic. the fish. Identification of the prey was carried out MATERIALS AND METHODS in the laboratory, to the species level whenever possible. We registered their number and the wet Samples of Mediterranean horse mackerel weight of the food items to the nearest 0.001 g, were taken from five localities in the eastern after removing surface water by blotting on Adriatic (Fig. 1): near the islands of Vis and tissue paper. Gonads of all specimens were Svetac (A), south of Šolta Island (B), Split dissected and weighed to the nearest 0.001 g Channel (C), Blitvenica fishing area (D) and to calculate the gonadosomatic index (GSI = Jabuka Island (E), at the continental shelf weight of gonads/fish weight × 100). between depths of 60 (locality A) and 175 Numerous indices quantitatively express the (locality E) meters. relative importance of different prey in fish diets Samples were taken from commercial (BERG, 1979; HYSLOP, 1980). Those used in the bottom-trawl catches carried out with a cod-end present study included: (a) frequency of occur- net of 22 mm mesh (stretched) at a trawling rence (%F), based on the number of stomachs speed of 2-3 knots. The nets were hauled three in which a food item was found, expressed as times a day: from 04:00 to 10:00, from 11:00 to the percentage of the total number of non-empty 16:00, and from 17:00 to 22:00. Monthly samples stomachs, (b) numerical abundance (%Cn), the
Fig. 1. Study area and sampling localities of Mediterranean horse mackerel (Trachurus mediterraneus) in the eastern Adriatic: A - near Vis and Svetac islands, B - south of Šolta Island, C - Split Channel, D - Blitvenica fishing area, E - Jabuka Island ŠANTIĆ, JARDAS & PALLAORO: Diet and feeding intensity of Mediterranean horse mackerel 45 number of each kind of prey, expressed as the index (%Jr = weight of digested prey/fish weight percent of the total number of food items in ×100; HUREAU, 1970) were used to determine all non-empty stomachs in the sample, and (c) feeding intensity. gravimetric composition (%Cw), the wet weight The variations in vacuity index during the of each kind of prey, expressed as the percent of seasonal and diurnal cycles were tested by chi- the total weight of the stomach contents in the square test (SOKAL & ROHLF, 1981). sample. The main food items were identified using RESULTS the index of relative importance (IRI) of PINKAS et al. (1971), modified by HACUNDA (1981): Of the 1200 examined stomachs, 606 were IRI = %F × (%Cn + %Cw) empty (50.5%). Table 1 shows the %F, %Cn, A vacuity index (%VI = empty stomachs/ %Cw and IRI of the prey groups and species total number of stomachs ×100) and a fullness found in the non-empty stomachs.
Table 1. Prey groups and species in the diet of Trachurus mediterraneus (%F = frequency of occurrence; %Cn = numerical composition; %Cw = gravimetric composition according to weight; IRI = index of relative importance) Food item (%F) (%Cn) (%Cw) IRI TELEOSTEI Gadiculus argenteus 6.73 0.46 14.55 101.01 Maurolicus muelleri 6.06 0.69 12.83 81.93 Engraulis encrasicolus 6.56 0.79 5.46 41.00 Helicolenus dactylopterus 1.01 0.05 5.20 5.30 Arnoglossus laterna 1.17 0.08 2.40 2.90 Lesueurigobius friesii 2.35 0.15 2.29 5.73 Aphia minuta 1.01 0.07 0.89 0.96 Other and non-identified Teleostei 13.37 0.35 2.34 35.96 CRUSTACEA Euphausiacea: Nyctiphanes couchii 29.46 52.94 19.46 2132.9 Euphausia krohni 14.30 25.62 9.53 502.6 Meganyctiphanes norvegica 8.24 4.65 3.36 66.0 Non-identified Euphausiacea 7.07 6.22 1.73 56.2 Mysidacea: Lophogaster typicus 1.51 5.75 2.14 11.9 Decapoda: Parapenaeus longirostris 2.18 0.13 1.86 4.33 Munida rugosa 1.01 0.04 1.16 1.21 Other and non-identified Decapoda 1.34 0.07 0.71 1.05 Total Decapoda 1.43 0.35 4.67 7.23 CEPHALOPODA Sepiola sp. 1.01 0.03 0.96 1.00 Illex illecebrosus 0.67 0.03 2.33 1.58 POLYCHAETA Non-identified Polychaeta 0.67 0.12 0.95 0.71 46 ACTA ADRIATICA, 45(1): 43-50, 2004
The stomach contents of the Mediterranean to the IRI, there was little seasonal variation in horse mackerel consisted of six major the diet (Table 2). Euphausiids were dominant systematic groups: Teleostei, Euphausiacea, during all seasons, particularly in summer and Mysidacea, Decapoda, Cephalopoda and autumn. Teleosts were present throughout the Polychaeta. According to the IRI, euphausiid year, however, were highest during spring. crustaceans were the most important prey Decapods and cephalopods were present in the followed by various developmental stages of diet during all seasons while mysids were absent fish species. Other taxa found in the stomach in autumn and polychaets were found only in contents (Mysidacea, Decapoda, Cephalopoda autumn and winter. and Polychaeta) were of lesser importance in Figs. 2 and 3 show the feeding intensity the diet. At the species level, two euphausiids during the year. Low values for prey biomass Nyctiphanes couchii and Euphausia krohni and high values for vacuity index were were the most important (IRI), followed by recorded in May-June, during the spawning three teleosts: Gadiculus argenteus, Maurolicus of T. mediterraneus (Fig. 2). During these two muelleri and Engraulis encrasicolus. According
Table 2. Index of relative importance (IRI) of the major prey groups, by season
Prey group Winter Spring Summer Autumn IRI IRI IRI IRI Teleostei 228.38 924.09 240.50 292.54 Euphausiacea 2472.59 2609.52 3620.71 3212.46 Mysidacea 83.67 6.70 2.67 - Decapoda 6.35 25.17 10.04 4.19 Cephalopoda 3.33 1.75 1.27 8.08 Polychaeta 5.95 - - 0.99
month Fig. 2. Biomass of prey (g) and vacuity index (%VI) of Mediterranean horse mackerel (Trachurus mediterraneus) throughout the year ŠANTIĆ, JARDAS & PALLAORO: Diet and feeding intensity of Mediterranean horse mackerel 47
month Fig. 3. Gonosomatic index (GSI) and fullness index (%Jr) of Mediterranean horse mackerel (Trachurus mediterraneus) throughout the year months, the gonadosomatic index peaked and Table 3. Fullness index (% Jr) and vacuity index (%VI), the fullness index was very low (Fig. 3). by season When spawning terminated in July/August, the fullness index reached its highest value while Season Fullness index Vacuity the vacuity index reached its lowest (Table 3). (%Jr) index (%VI) Feeding intensity decreased in winter (January Winter 0.32 55.3 and February). The vacuity index reached its Spring 0.28 66.0 highest value in April, just prior to spawning and Summer 0.38 35.3 indicates significantly lower feeding intensity in winter and spring ( 2 = 31.3, P<0.05). Autumn 0.36 45.0
Fig. 4. Diurnal fullness index (%Jr) and vacuity index (%VI) of Mediterranean horse mackerel (Trachurus mediterraneus) 48 ACTA ADRIATICA, 45(1): 43-50, 2004
Feeding intensity was measured after each a significant proportion of the stomach contents haul. The vacuity indices showed that feeding of T. mediterraneus in Lyon Bay and Gascone intensity was significantly higher during the Bay, while in Tunisian waters fish belonging night and morning and decreased during the to Gobiidae are the main food items (BEN- course of the day ( 2 = 11.3, P<0.05; Fig. 4). SALEM, 1988). The data recorded in this work This was confirmed by the fullness index. generally coincide with the above-mentioned references, showing that planktonic crustaceans DISCUSSION and fish dominate the diet of Mediterranean horse mackerel. Differences in food habits of T. T. mediterraneus is essentially plankto- mediterraneus between the Mediterranean and phagous. According to our data, its main prey is the central Adriatic are mainly due to different euphausiid plankton (N. couchii, E. krohni and, distribution, abundance, density, availability and less often, Meganyctiphanes norvegica). This accessibility of prey. group represents over 50% of the total IRI and The feeding intensity of Mediterranean horse was thus the main food (ROSECCHI & NOUAZE, mackerel changed during the year, probably 1987). G. argenteus, M. muelleri, E. encrasicolus related to spawning and water temperature. and other less important teleosts were the Feeding intensity increased in March and April secondary food. Other prey, i.e., mysids, (prior to spawning) and reached its lowest decapods, cephalopods and polychaets, were of during spawning (May-June). It is assumed that minor importance and an occasional food. during reproduction T. mediterraneus reduces N. couchii and E. krohni are common in the the energy spent on catching prey and directs central Adriatic especially in the areas of Vis it to gamete production. Expended energy is Island, Jabuka pit and the Blitvenica fishing replaced by intensified feeding after spawning area, while M. norvegica is more frequent in (July-September). This is confirmed by data on the south Adriatic pit (ŠIPOŠ, 1977; GAMULIN, T. mediterraneus ponticus from the Black Sea, 1979; NOŽINA, 1979). The different distribution where feeding intensity increased from 80 to patterns of these zooplankton are probably the 90% after spawning (SIROTENKO & ISTOMIN, reason why N. couchii and E. krohni were more 1978). The high sea temperatures in July- abundant in the stomachs of central Adriatic September accelerate metabolism, resulting in T. mediterraneus than M. norvegica. Since an increased food demand. WARREN & DAVIS these euphausiid crustaceans are present in the (1967) discussed the profound effects of tem- study area year-round (GAMULIN, 1979), they perature and seasonality on food consumption constituted the main food for T. mediterraneus rates. More food is consumed in summer than year-round. in winter, as demonstrated in an experiment Data on the food of T. mediterraneus with Cottus perplexus (DAVIS & WARREN, 1965). in the Adriatic Sea are scant. BINI (1968) and In many fishes, the feeding rate drops as the TORTONESE (1975) only mention that fish and temperature drops (TYLER, 1971). In the study small crustaceans are its food. In Albanian area, the water temperature reaches a minimum waters the species prefers fish (particularly during the winter (February) and beginning of anchovies), amphipods, mysids and decapods spring (ZORE-ARMANDA et al., 1991). Because of in the summer (LIPSKAJA, 1966). In the Aegean the reduced abundance of prey and the lowered Sea, fish larvae and postlarvae (particularly of metabolism of the fish, predation was probably Pagellus acarne, Diplodus vulgaris and Spicara at a minimum during the winter. ŠIPOŠ (1977) maena) constitute the dominant biomass in T. and GAMULIN (1979) showed that in the Adriatic mediterraneus stomachs, followed by crustacean Sea euphausiids were more abundant and denser copepods and mysids (KYRTATOS, 1998). during the warm part of the year (spring and Mysidacea and Copepoda crustaceans constitute summer). ŠANTIĆ, JARDAS & PALLAORO: Diet and feeding intensity of Mediterranean horse mackerel 49
Vacuity and fullness indices revealed that crustaceans (Euphausiacea), the dominant prey. the Mediterranean horse mackerel consumed Zooplankton inhabit deeper layers during the prey during the night and in the early morning. Possibly, feeding activity is higher in low light day and rise towards the surface during the night due to the vertical migration of zooplankton to feed (HURE, 1961; VUČETIĆ, 1961).
REFERENCES ARNERI, E. & P. TANGERINI. 1984. Biological data JARDAS, I. 1996. The Adriatic ichthyofauna. collected during the Pipeta Expeditions on Školska knjiga d.d., Zagreb (in Croatian), Trachurus mediterraneus (Steindachner) 553 pp. in the Adriatic Sea. FAO Fish. Rep., 290: KYRTATOS, N.A. 1998. Contribution à la 127-130. connaissance da la nourriture de Trachurus BEN-SALEM, M. 1988. Régime alimentaire de mediterraneus (Steind.) et de son influence Trachurus trachurus (Linnaeus, 1758) et sur les chaînes alimentaries de la Mer Égée de Trachurus mediterraneus (Steindachner, centrale. Rapp. Comm. Int Mer Médit., 35: 1868) (Poissons, Téleostéens, Carangidae) 452-453. de la province Atlantico-Méditerranéenne. LIPSKAJA, N.J. 1966. Pitanie stavridy (Trachurus Cybium, 12: 247-253. mediterraneus Steind.) v Adriatičeskom BERG, J. 1979. Discussion of the methods i Černom morjah. Issledovania planktona of investigating the food of fishes with južnyh morej. Nauka, 210: 109-114. reference to a preliminary study of the food NOŽINA, I. 1979. Biogenic deep scattering layers of Gobiusculus flavescens (Gobiidae). Mar. in the Adriatic mesopelagial. Ph.D.Thesis, Biol., 50: 263-273. University of Ljubljana, 151 pp. BINI, G. 1968. Atlante dei pesci delle coste PINKAS, L., M.S. OLIPHANT & I.L.K. IVERSON. Italiane. V Mondo Sommerso, Milano, 1971. Food habits of albacore, bluefin tuna 175 pp. and bonito in California waters. Fish. Bull., DAVIS, G.E. & C.E. WARREN. 1965. Trophic 152: 1-105. relations of a sculpin in laboratory stream ROSECCHI, E. & Y. NOUAZE. 1987. Comparaison communities. J. Wildl. Mgmt., 29: 846-871. de cinq indices alimentaires utilisés dans FAO, 2000. Fishery statistics. Capture production. l’analyse des contenus stomacaux. Rev. In: FAO Yearbook Vol. 86/1. FAO, Rome, Trav. Inst. Pêch. Marit., 49:111-123. 713 pp. SMITH-VANIZ, W.F. 1986. Carangidae. pp. 815- GAMULIN, T. 1979. Zooplankton of the eastern 844. In: Fishes of the north-eastern Atlantic Adriatic coast. Acta Biol., 8: 177-270 (in and Mediterranean. Whitehead, P.J., Croatian, French summary). Bauchot, M-L., Hureau, J.-C., Nielsen J. HACUNDA, J.S. 1981. Trophic relationships Tortonese E. (Editors). UNESCO, Paris. among demersal fishes in coastal area of the SIROTENKO, M. & A. ISTOMIN. 1978. Seasonal Gulf of Main. Fish. Bull., 79: 775-788. variations in the feeding of the Black Sea HURE, J. 1961. Diurnal migration and seasonal Trachurus mediterraneus ponticus Aleev. J. vertical distribution of zooplankton in the Ichthyol., 18: 424-431. deepest sea. Acta Adriat., 9 (6): 1-59. SOKAL, R.R. & ROHLF, F.J. 1981. Biometry. W.H. HUREAU, J.C. 1970: Biologie comparée de Freeman and Company (Editors). San quelques Poissons antarctiques. Bull. Inst. Francisco, 776 pp. Océanogr., 68: 185-203. ŠIPOŠ, V. 1977. Distribution of euphausiids in HYSLOP, E.J. 1980. Stomach contents analysis - a the Adriatic Sea in autumn 1974 and spring review of methods and their application. J. 1975. Rapp. Comm. int. Mer Medit., 24: Fish Biol., 17: 411-429. 10-11. 50 ACTA ADRIATICA, 45(1): 43-50, 2004
TORTONESE, E. 1975. Osteichthyes (Pesci ossei). VUČETIĆ, T. 1961. Vertical distribution of Fauna d′ Italia. XI Calderini (Editor). zooplankton in the Big lake from the island Bologna, 636 pp. Mljet. Acta Adriat., 6 (9): 1-20. TYLER, A.Y. 1971. Monthly changes in WARREN, C.E. & G.E. DAVIS. 1967. Laboratory stomach contents of demersal fishes in studies on the feeding bioenergetics and Passamaquoddy Bay (N.B.). Fish. Res. growth of fish. pp. 123-135. In: The Board Can. Techn. Pap., 288: 114 pp. biological basis of freshwater fish production. VIETTE, M., P.G. GULIANINI & E.A. FERRERO. 1997. Gerking, S.D. (Editor). Blackwell Scientific Reproductive biology of scad Trachurus Publications, London. mediterraneus (Teleostei, Carangidae) from the ZORE-ARMANDA, M., M. BONE, V. DADIĆ, M. Gulf of Trieste. J. Mar. Sci., 54 (2): 267-272. MOROVIĆ, D. RATKOVIĆ, L. STOJANOSKI & VRGOČ, N. 2000. Structure and dynamics of I. VUKADIN. 1991. Hydrography properties demersal fish communities of the Adriatic of the Adriatic Sea in the period from 1971 Sea. Thesis, University of Zagreb, 197 pp. through 1983. Acta Adriat., 32: 6-554. Received: 4 December 2002 Accepted: 14 October 2003
Sastav hrane i intenzitet ishrane šnjura pučinara, Trachurus mediterraneus, (Osteichthyes: Carangidae) u srednjem Jadranu
1Mate ŠANTIĆ, Ivan JARDAS2 i Armin PALLAORO2
1Fakultet prirodoslovno-matematičkih znanosti i odgojnih područja, Sveušilište u Splitu, 21000 Split, Hrvatska e-mail: [email protected] 2Institut za oceanografiju i ribarstvo, 21000 Split, Hrvatska e-mail: [email protected]; [email protected]
SAŽETAK
Istražen je sastav hrane i intenzitet ishrane šnjura pučinara, Trachurus mediterraneus (STEINDACHNER, 1868.) sakupljenog u srednjem Jadranu. Analiziran je sadržaj želuca kod 1200 primjeraka sakupljenih u mjesečnim intervalima od siječnja do prosinca 1996. U hrani je determinirano 6 glavnih skupina plijena: Rakovi (Euphausiacea, Mysidacea i Decapoda), ribe (Teleostei), glavonožci (Cephalopoda) i mnogočetinjaši (Polychaeta). S obzirom na frekvenciju, brojnost i biomasu, eufauzidni račići bili su glavna hrana. Ribe (Teleostei) su predstavljale sekundarnu hranu, dok su ostale skupine plijena bile slučajnja hrana. Eufauzidni račići bili su dominantna hrana tijekom cijele godine, a posebno u ljetno-jesenskom razdoblju. Intenzitet ishrane kolebao je tijekom godine. Niske vrijednosti intenziteta ishrane zabilježene su tijekom zime kada je snižena temperatura mora kao i u razdoblju mrijesta (svibanj i lipanj). Najviši intenzitet hranjenja zabilježen je u razdoblju neposredno prije (travanj) i nakon mrijesta (srpanj, kolovoz i rujan). Intenzitet ishrane šnjura pučinara mijenja se tijekom dnevnog ciklusa. Najveća aktivnost hranjenja zabilježena je tijekom noći i ranih jutarnih sati.
Ključne riječi: Trachurus mediterraneus, sastav hrane, intezitet ishrane, Jadransko more ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.582: 591.13 AADRAY 45 (1): 51-63, 2004 Original scientific paper
Effects of three diets on growth and body composition of gilthead sea bream, Sparus aurata (L.)
Miro KRALJEVIĆ1, Mladen TUDOR1, Jakov DULČIĆ1 and Boško SKARAMUCA2
1Institute of Oceanography and Fisheries, P.O. Box 500, 21000 Split, Croatia E-mail: [email protected]
2Institute of Oceanography and Fisheries, Split, Laboratory for Ecology and Aquaculture, P.O. Box 83, 20000 Dubrovnik, Croatia
Wild gilthead sea bream fingerlings (4.3±1.8 g) were reared to portion size (250 g) in an ambient seawater system with varying temperature (10.3-24.3°C) for 15.0-16.6 months. They were fed commercial crumbles and pellets alone (F1), or mixed with 35% chicken eggs (F2), or mixed with 35% blue mussel flesh (F3). The daily feeding rate, daily protein feeding rate, daily growth rate, feed efficiency (FE), protein efficiency ratio (PER), protein productive value (PPV) and specific growth rate (SGR) were calculated monthly after weighing. Fish fed diet F3 grew to 250 g significantly (P<0.05; ANOVA) faster than those fed F2 or F1, in 15.0 months rather than 16.6 months. The daily feeding rates significantly differed (P<0.05) between groups and was highest in group F3 (3.80±0.18%) and lowest in group F1 (1.72±0.34%). There were no significant differences in daily growth rate (P = 0.58-0.11). The daily growth rate, FE, PER and PPV were negative in winter. The final body composition of the tested fish had significantly less moisture (65.0-68.5%) and higher lipids (8.4-10.3%) than initially and than specimens from a native environment (73.6- 76.1% and 0.6-3.7%, respectively).
Key words: Sparus aurata, juvenile, nutrition, growth, body composition
INTRODUCTION et al., 1999; CANAVATE & FERNANDEZ-DIAZ, 2001; NAVARO et al., 2001; PAPANDROULAKIS et al., 2002; The gilthead sea bream (Sparus aurata) is PITA et al., 2002; PEREIRA & OLIVIA-TELES, 2003). commonly farmed in countries bordering the Until recently, prepared diets were Mediterranean Sea. Marine farming of S. aurata successfully used to establish the nutritional began in the 1980s and expanded rapidly in Spain, requirements of S. aurata. A number of authors Italy, Turkey and, especially, Greece during the (KISSIL et al., 1981, 1982, 2000; KISSIL & GROPP, last decade. Since there are many hatcheries 1984; KISSIL & KOVEN, 1987; PEREIRA, et al. 1987) researched amino acids, fatty acids and and fish farms in the Mediterranean, studies of pyridoxines, food energy and their impact on artificial spawning and rearing in experimental growth and survival of this species. conditions are numerous (KALOGEROPOULOS et al., 1992; KENTOURI et al., 1994; NAVARO & Studies of the chemical composition of SARASQUETE, 1998; NENGAS et al., 1999; YUFERA gilthead sea bream from the natural environment 52 ACTA ADRIATICA, 45(1): 51-63, 2004 are rare (WASSEF & SHEHATA, 1991). Some authors (P>0.05, t-test of proportion, SOKAL & ROHLF, (KALOGEROPOULOS et al., 1992; NENGAS et al., 1969), results were presented as mean values. 1999) studied the effect of long-term artificial The experiment began on July 20. food intake on the chemical tissue composition of the gilthead sea bream. Rearing conditions In the present study, the food conversion Ninety survived juveniles averaging 6.9±0.9 budget of S. aurata fingerlings, fed one of three cm (total length) and 4.3±1.8 g were randomly diets, was studied. Hen eggs were used because distributed into six aquaria, in groups of 15 per of their good food fixing properties in previous aquarium. Fish were placed in 250-l plastic studies (KRALJEVIĆ, 1984) and because the best tanks; on April 20, they were transferred to 1200- growth rate of gilthead sea bream was obtained l plastic tanks. Both types of tanks were supplied with diets that had an amino acid profile similar with running sea water (34.6-39.5‰ NaCl) at to that of hen eggs (KISSIL & KOVEN, 1987). ambient temperatures (10.3-24.3°C), under the Blue mussel meat was used because gilthead natural photoperiod (44°30.5'N; 16°23.5'E). sea bream had the best growth and survival in Dissolved oxygen was kept at 7.6±0.4 mg l-1, an earlier study (KRALJEVIĆ, 1984, 1995). The while the seawater flow was maintained at about daily feeding rate (f), daily protein feeding rate 0.7-3.1 l min-1 (approximately 4 changes per (f ), daily growth rate (GR), feed efficiency p day; according to very low density). There were (FE), protein efficiency ratio (PER), protein no incidences of pathogens, mortality or other productive value (PPV) and specific growth rate adverse circumstances during the study, except (SGR) were calculated and gilthead sea bream those related to the quality of the different tissue was chemically analyzed at the beginning foods. and end of the experiment and compared with Dietary treatments bream from the natural environment. An artificial high-protein feed (supplied by MATERIALS AND METHODS ALMA Futter Ltd.) was used (Table 1). The crumbles and extruded pellets were given alone A small number (ca 120) of wild gilthead (diet F1) or mixed with 35% hen eggs (F2) or sea bream juveniles were captured from the 35% blue mussel meat (F3). Before use, the hen Makirina Cove (mideastern Adriatic coast) at the eggs were homogenized and the mussel meat beginning of July with a small beach seine (50 was minced. m long, 2.5 m high, 8 mm wings and 4 mm sack Table 1. Composition of the commercial extruded crumbles mesh). The were allowed to adapt to aquaria and pellets (% wet weight) conditions in a 250-l plastic tank, supplied with running sea water (36.7-37.9‰ NaCl) at ambient Ingredient Crumbles Pellets temperatures (17.1-19.3°C) under a natural Moisture 10.0 9.6 photoperiod. The bream were fed commercial Protein mix 42.5 42.0 crumbles and pellets, together with mussels Vitamin mix 1.0a 1.0b (Mytilus galloprovincialis) and fish (Sardina pilchardus, Engraulis encrasicolus, Atherina Lysine 3.5 3.3 hepsetus). At catch, twelve bream died. The Lipidsc 9.5 9.5 following day they were divided into two groups Crude fiber 2.0 2.8 of six. Fragments of the head, central body Ashes 12.0 12.5 muscle and tail muscle were taken from each NFE 19.5 19.3 fish for chemical tissue analysis. The fragments d taken from each group were blended together Mineral mix 0.2 0.2 for analysis in two replicates. Since differences a Vitamins supplied per kg mix: vitamin A, 30,000 in tissue components within the replicates or IU; vitamin D3, 2000 IU; vitamin E, 100 mg; vitamin between groups were not statistically significant K, 4 mg; vitamin C (ascorbic acid), 250 mg; vitamin KRALJEVIĆ, TUDOR, DULČIĆ & SKARAMUCA: Growth and body composition of Sparus aurata (L.) 53
B1 (thiamin), 25 mg; vitamin B2 (riboflavin), 15 mg; and 18:00) until satiation. During the winter vitamin B6 (pyridoxine), 4 mg; vitamin B12, 80 mg; (Dec 21-April 20), the fish were fed only twice nicotinic acid, 60 mg; Ca-pantotenate, 20 mg; choline a day (at 8:00 and 15:00). Each meal lasted chloride, 300 mg; folic acid, 3 mg about 15-20 min (25 in winter) according to b Vitamins supplied per kg mix: vitamin A, 25,000 APOSTOLOPOULOS & KLAOUDATOS (1986). The IU; vitamin D 2000 IU; vitamin E, 85 mg; vitamin 3, amount of food was weighed at the beginning K, 4 mg; vitamin C, 200 mg; vitamin B , 25 mg; 1 and end of the feeding to calculate the weight vitamin B2, 15 mg; vitamin B6, 4 mg; vitamin B12, 80 mg; nicotinic acid, 60 mg; Ca-pantotenate, 20 mg; of the food consumed. The experiment lasted choline chloride, 280 mg; folic acid, 3 mg until the end of a productive cycle (15.0-16.6 c Lipids supplied by cod liver oil (6.5%) and soybean months) when the mean fish weight reached oil (3.0%) about 250 g (portion-size fish). Once a month, d Minerals supplied per kg mix: Mg, 60 mg; Zn, 40 fish were slowly anesthetized (4-amino benzoic mg; Fe, 18 mg; CuO, 12 mg; Mn, 7 mg; I, 0.5 mg; acid ethyl ester C9H11NO2) and measured (total Se, 0.02; Co, 0.02 mg length and weight).
The fingerlings were fed commercial Growth parameters crumbles at the beginning of the experiment. When they attained approximately 9.5 The daily feeding rate (f), daily protein cm and 12.0 g, they were fed commercial feeding rate (fp), daily growth rate (GR), feed extruded pellets with a diameter of 2 mm. The efficiency (FE), protein efficiency ratio (PER), commercial crumbles and pellets contained protein productive value (PPV) and specific adequate amounts of vitamins and minerals. growth rate (SGR) were calculated according to The proximate composition of the diets is given the equations in Table 3. Values did not differ in Table 2. The diets were prepared at ambient significantly between replicates. temperature and stored in a deep freeze (-20oC). Amounts needed for a feeding were thawed Chemical tissue analysis when needed. At the end of the experiment (after The fish were fed by hand seven days a completion of one productive cycle, i.e., 15.0- week, 3 times a day (usually at 8:00, 13:00 16.6 months), the smallest, middle and biggest
Table 2. Proximate composition of the diets (% wet weight)
Component F1 F2 F3 Commercial crumbles/ Commercial crumbles/ Commercial crumbles/ pellets (100%) pellets (65%) and hen pellets (65%) and blue eggs (35%) mussel flesh (35%) Crude protein 41.4a 31.4b 31.9b Crude lipid 10.2a 10.5a 7.8b Moisture 6.3a 30.0b 30.1b Ash 10.4a 7.2b 6.7b Cellulose 2.5 1.4 1.6 Non-nitrogen 29.2 19.5 21.9 materials Values with the same superscript are not significantly different (P>0.05) 54 ACTA ADRIATICA, 45(1): 51-63, 2004
Table 3. Formulae for computing growth parameters in gilthead sea bream
Parameter Abbreviation Formula* [ ] Daily feeding rate f f = F x 100/t (Wo+ W’+ Wt)/2
Daily protein feeding rate fp fp = pfood x f [ ] Daily growth rate GR GR = (Wt+ W’- Wo) x 100/t (Wo+ W’+ Wt)/2 Food efficiency FE FE = GR/f
Protein efficiency ratio PER PER = GR/fp
Protein productive value PPV PPV = 100 x (pfish x FE /pfood )
Specific growth rate SGR SGR = (lnWt - lnWo) x 100/days
* F = total amount of food consumed (in g), t = experimental period (in days), Wo= total initial body weight (in g), W’ = total body weight of dead fish (in g), Wt = total final body weight (in g), pfood = protein fraction in food, pfish = protein fraction in fish fish of each replicate were sampled for chemical summer and autumn of the first (August 19- body analysis. The body tissue (head, central November 21) and second (July 21-October 20) body muscle, tail muscle) of the three fish from years, gradually decreased as winter approached each group were mixed together for analysis in (November-December) and stagnated in two replicates. Since there were no statistically January-April (Fig. 1a). The S. aurata on F3 significant differences (P<0.05) between the diet reached 250 g 1.5 months earlier than fish replicates, values are presented as the means fed the other diets. Fish fed diet F3 had the best for each dietary treatment. To compare the survival. Throughout most of the experiment, chemical composition with that of fish raised the G-test of independence for total mortality in nature, two S. aurata (ca 300 g) were caught (SOKAL & ROHLF, 1969) revealed significant from the natural environment near the Institute, differences (P<0.05) in survival between group samples were taken from the same three body F3 and the other groups. locations as described above and the chemical The condition factor (Fig. 1b) followed composition was analyzed in the same way. temperature changes (Fig. 1a), with a lag of about 1.5 months. The difference between RESULTS the condition factor measured in September- November of the first year (1.48) and that Changes in body length and weight and of the second year (1.59) suggests that it is condition factor influenced not only by temperature but also by Growth parameters are shown in Table fish size and is not an isometric length-weight 4. At the beginning of the experiment there relationship. In the winter (February-April), were no significant differences (ANOVA; the fish grew relatively slower in weight than P>0.05) between lengths and weights. During in length, especially in the F2 treatment where the experiment, there were no significant the condition factor was lower (1.29) than at differences (ANOVA; P>0.05) in length any other time during the experiment, except (F = 0.05-3.41; F.05,1,30 = 4.17; F.05,1,21 = 4.32, the beginning (1.26). The highest condition according to the later survival) or weight factors were recorded in the first (1.46-1.48) (F = 0.54-3.68) between replicates fed the same and second (1.57-1.59) autumns. The condition < diet, but fish fed F3 differed (P 0.05, Lt-F = factors for the F1 treatment were significantly 3.89-8.84; W-F = 3.56-13.54; F.05,2.68 = 3.15) lower (WILCOXON matched pairs test) than from those fed F1 or F2 from the first October those of the F2 (P<0.001) and F3 (P<0.005) until the end of experiment. The weight increase treatments, while it was lower for F2 than for was higher in all three treatments during F3 (P<0.001). KRALJEVIĆ, TUDOR, DULČIĆ & SKARAMUCA: Growth and body composition of Sparus aurata (L.) 55
Table 4. Effects of feeding diets with different protein and lipid contents for 504 days on the growth and survival of juvenile gilthead sea bream, means±SEM (n)
Diet Parameter F1 F2 F3 Commercial Commercial crumbles Commercial crumbles crumbles and and pellets (65%) with and pellets (65%) with pellets hen eggs (35%) blue mussel flesh (35%)
Avg initial wt (g) 4.2±0.33 (30)a 4.6±0.29 (30)a 4.2±0.29 (30)a Avg final wt (g) 250±11 (21)a 248±9 (26)a 268±8 (29)b Wt gain (g) 245.8 243.4 263.8 Avg initial total length (cm) 6.8±0.16 (30)a 7.0±0.16 (30)a 6.8±0.14 (30)a Avg final total length (cm) 25.1±0.30 (21)a 25.1±0.29 (26)a 25.7±0.24 (29)b Length gain (cm) 19.0 18.1 18.9 Survival (%) 70.0a 86.7b 96.7c Daily feeding rate (%) 1.72±0.34 (17)a 3.01±0.60 (17)b 3.80±0.18 (17)c Daily protein feeding rate 0.71±0.14 (17)a 0.95±0.19 (17)b 1.21±0.24 (17)c Daily growth rate (%) 0.75±0.20 (17)a 0.73±0.21 (17)a 0.87±0.23 (17)a Food efficiency 0.39±0.05 (17)a 0.12±0.07 (17)b 0.19±0.02 (17)b Protein efficiency ratio 0.94±0.12 (17)a 0.38±0.22 (17)b 0.59±0.06 (17)b Protein productive value 18.1±2.4 (17)a 7.3±4.2 (17)b 11.3±1.2 (17)b Specific growth rate (%) 0.79±0.22 (17)a 0.77±0.24 (17)a 0.90±0.25 (17)a
Values with the same superscript are not significantly different (P>0.05)
Fig. 1. Body weight (a) and condition factor (b) of Sparus aurata reared on different foods 56 ACTA ADRIATICA, 45(1): 51-63, 2004
Effect of diet on growth parameters
At the beginning of the experiment, the daily feeding rate (f) was highest for the F3 diet (11.74% of the mean body weight), and lowest for the F1 (4.35%; Fig. 2a). The WILCOXON matched pair test showed that the difference in daily feeding rates for diets F1 and F2 was statistically significant (P<0.001) as were the differences between F1 and F3 (P<0.001) and F2 and F3 (P<0.01). The daily protein feeding rate (fp) had a similar curve as the daily feeding rate, but was one-third to one-half (Fig. 2b) the value throughout the experimental period. The WILCOXON matched pair test showed statistically significant differences in daily protein feeding rate between all diets (P<0.01). There were no significant differences in daily growth rate (Fig. 2c) between diets F1 and F2 (P = 0.58), F1 and F3 (P = 0.17) or F2 and F3 (P = 0.11). The highest values (3.50, 3.31, 3.15%) were measured at the beginning of the experiment and the lowest were negative (-0.03, -0.04, -0.08%) in February and March. Daily GR values were very similar to the daily feeding rate (Fig. 2a) and daily protein feeding rate (Fig. 2b) and followed the temperature curve (Fig. 1a) throughout the experiment. The overall SGR was lower for diets F1 and F2 than for diet F3, but not significantly (P = 0.36, 0.39, 0.09). The monthly SGR, like fish weight, followed the temperature curve in all Fig. 2. Daily feeding rate (a), daily protein feeding rate (b) three treatments. and daily growth rate (c) of Sparus aurata reared on There were significant differences in FE different foods (Fig. 3a) between diets F1 and F2 (P<0.001) and F1 and F3 (P<0.02). According to the
WILCOXON matched pairs test, FE did not FE, PER and PPV were similar to those of f, fp significantly differ (P = 0.36) between diets and GR, with minimums in February-March. F2 and F3. The same statistical results were obtained for PER (Fig. 2b) and PPV (Fig. 2c), Chemical tissue analysis i.e., there were no significant differences (P = 0.28) between diets F2 and F3, while PER The chemical analysis of the body tissue at differed significantly between F1 and F2 (P the beginning and end of the experiment were = 0.001) and F1 and F3 (P = 0.002) and PPV measured and compared with specimens from differed significantly between F1 and F2 (P = the wild (Table 5). The composition of the 0.001) and F1 and F3 (P = 0.006). The curves of experimentally-fed fish did not significantly KRALJEVIĆ, TUDOR, DULČIĆ & SKARAMUCA: Growth and body composition of Sparus aurata (L.) 57
DISCUSSION
WASSEF & SHEHATA (1991) studied the chemical composition of wet tissue from gilthead sea bream of different sizes and sexes from the natural environment of the southern Mediterranean, near Alexandria, at the different times of the year. Their results perfectly match ours for juvenile (initial) and two-year-old (K1, K2) gilthead sea bream from the natural Adriatic environment. Our results for fish fed commercial pellets strikingly differ from the natural results but are similar to those cited for the same species, experimentally fed with commercial artificial food (KALOGEROPOULOS et al., 1992; NENGAS et al., 1999), demonstrating that short (84 days) and long-term (150-504 days) artificial nutrition modifies chemical body tissue composition. If artificial nutrition has such an impact on S. aurata tissue (muscles), it probably affects other artificially reared fish in the same way. In our experiment, the F1 diet had a significantly larger proportion of protein and ash and less moisture than the F2 and F3 diets. Likewise, the body tissues of the fish fed F1 had higher fat, ash and protein contents and less moisture than those fed F2 and F3. The diet consisting of 100% commercial pellets (F1) contained more protein than the diets containing pellets plus hen eggs (F2) or blue mussel flesh (F3). This is probably the reason why the fish Fig. 3. Food efficiency (a), protein efficiency ratio (b) and fed F1 contained slightly more fat than the protein production value (c) of Sparus aurata reared others, as confirmed by KALOGEROPOULOS et on different foods al.,(1992) and NENGAS et al., (1999). The fish fed F1 and, to a lesser degree, the fish fed F2 had a higher amount of stored mesenteric fat in the differ from those of the initial (0.8-year-old abdomen. A similar occurrence was recorded juveniles) or 300 g gilthead sea bream from by DENDRINOS & THORPE (1985) in the tissue of the natural environment (2.2-year-old; K1, K2) sea bass after 12 months of feeding on a trout in protein, carbohydrate or ash but moisture pellet diet, at the constant temperature of 19oC was significantly lower and fat and energy and varying salinity (5-33‰ NaCl). DENDRINOS significantly higher in the experimentally-fed & THORPE (1985) determined similar levels in fish. The moisture content rose with the level sea bass from the natural environment, as did of moisture in the diets, while proteins, fat and STIRLING (1972). COWEY et al. (1972) found a energy dropped. All diets satisfied the nutrient similar composition of fat in the tissues of test- needs of the gilthead sea bream. fed turbot Scophtalmus maximus (L.). 58 ACTA ADRIATICA, 45(1): 51-63, 2004 Nature ., 1992 et al Shehata, 1991 ., 1994 Author ., 1999 et al et al , 1999 & Wassef (84 days) Kalogeropoulos Kentouri et al. 2 2 Nengas Initial Experimental , 1.43-1.61 0.13)-3.88 This study - monthly values
(- 1992 et al. 1 eared at different but constant temperatures, compared with the compared but constant temperatures, at different eared r
(150 days) Parameter 2.46)-1.75 (------Sparus aurata 2.7 8.4-9.8 8.7 6.8-10.2 1.6-4.9 Kalogeropoulos 74.5 66.7-70.1 74.5 67.7-73.0 71.2-78.8 FE PER SGR a c ad present trial present 0.77)-0.72 1.5 (- - 73.6 404 a c d From nature 0.6 75.9 386 (Days) a fed experimental diets, sampled from the natural environment or taken from the literature or taken from the natural environment a fed experimental diets, sampled from
b Length of b c experiment 8.4 68.5 676 b b bc Sparus aurat
C) 9.4 o 67.5 715 ( emperature b b b T This study 0.3 0.3 0.2 -
65.0 10.3 769 a a a (1996) Initial F1 F2 F3 K1 K2 Initial Experimental weight (g) et al. ble 5. Body composition (%) of Ta Energy (kJ/100 g)Energy 464 LipidsChloride 3.7 - ProteinCarbohydrates 19.3 0.0 22.5 0.3 21.4 0.2 21.1 0.4 21.4 0.2 20.7 0.4 15.6 - 17.6-19.4 16.7 15.3-17.7 - 17.6-22.5 - - - Moisture 76.1 Ash 1.2 1.6 1.4 1.3 1.3 1.7 7.1 4.1-4.8 5.5 4.7-4.9 1.1-1-6
Calculated by present authors According to Tibaldi Tibaldi According to
able 6. Food efficiency (FE), protein efficiency ratio(PER) and specific growth rate (SGR) of efficiency ratio(PER) and specific growth able 6. Food efficiency (FE), protein Fingerling-adult 6.5-230.0 15.5 ~ 18.0 43/49 - - 0.13-0.73 Fingerling 1.23 20.0±1.0 150 0.52-0.68 1.10-1.30 Stage Initial Older juvenileFingerling 100FingerlingFingerling 1.55 18 & 22 4.3±1.8 4.3±1.8 22.0±0.5 10.3-24.3 10.3-24.3 112 0.94-1.05 504 84 504 0.12-0.39 0.43-0.69 0.38-0.94 0.89-1.40 - 0.77-0.90 1.56-2.40 This study - whole experiment Nengas - Kaushik, 1998
T 1 2 KRALJEVIĆ, TUDOR, DULČIĆ & SKARAMUCA: Growth and body composition of Sparus aurata (L.) 59
Juvenile Dentex dentex (TIBALDI et al., 1996), the lower FE at lower temperatures as the of the same family as S. aurata and reared on slowing down of all metabolic processes, which food with a much higher percentage of proteins is confirmed by our negative values during (44.3-55.9%) and slightly higher percentage winter. Energetically poor food results in a of lipids (11.7-17.5%) than ours, had a higher lower FE (MARAIS & KISSIL, 1979), which could moisture content (70.5-71.8%) and lower protein explain the lower values for diets F2 and F3. content (18.0-18.9%). This can be explained by Our mean PER values were lower than those the lengths of the experiments; their experiment of the same species at similar weights (1.23, was only 60 days while ours was 504 days. 1.55 g), reared at higher temperatures (20.0; The lowest daily feeding rate was for diet 22.0°C) in other studies (Table 6). The negative F1, which had the highest protein content, and PER in the winter (February-March) were diet F3 had a higher feeding rate than diet F2. comparable to the negative values (-2.9) of Nile Although diets F2 and F3 had the same amount tilapia with a similar body weight (KAUSHIK et of protein, the diets differed in lipid content. It al., 1995). Research on PPV value is very scarce is known that, in fish, the voluntary intake of in the literature. food with lower energetic value is higher than that of food with higher energetic value, i.e., the Our SGR values differed from those consumption of food is inversely proportional to reported for juveniles currently farmed in the the energetic value (MARAIS & KISSIL, 1979). PAGE Mediterranean area, such as gilthead sea bream ANDREWS (1973) and found that higher levels of (Table 6) and dentex (1.18-1.32, TIBALDI et energy and protein in foods result in lower food al., 1996). HIDALGO and ALLIOT (1988) obtained consumption. From the equation describing the similar results on sea bass (0.55-0.99) given relationship between feeding rate, temperature practical diets and probably kept at a similar and body weight, it can be predicted that the water temperature of 20°C. SGR in our study maximum feeding rate will be reached for diet rapidly decreased in the first year and slowly F1 at 20oC, for diet F2 at 23oC and for diet F3 decreased in the second year of the experiment, at 27oC, and that gilthead sea bream would stop following the temperature curve and body feeding at 11.8oC (KRALJEVIĆ, 1995). weight. According to KAUSHIK (1995, 1998), the The feed efficiency ratio of fish fed F1 SGR decreased rapidly and parabolically with was significantly higher than those of the other an increase in body weight especially in the groups, although the lipid concentrations were earliest juvenile stages of sea bream, sea bass, relatively the same, because fish take most of rainbow trout, and common carp, agreeing the energy they need for maintenance from with our results. SGR values of different protein (GERKIN, 1955). The FE of all three diets species slowly increase with body weight, but was influenced more by temperature than by body weight, especially in the winter (February- the values differ depending on body size and March). FE depends on environmental species. The negative SGR in February and conditions such as temperature and salinity March were consistent with results of Nile (KINNE, 1960; KLAOUDATOS & APOSTOLOPOULOS, tilapia (-0.1; KAUSHIK et al., 1995). The SGR has 1986) and increases with temperature (GOOLISH often been related to some diet components, & ADELMAN, 1984; HIDALGO et al., 1987; RUSSEL mainly protein or fat (PÉREZ et al., 1997), but et al., 1996), as in our experiment. FE decreases seawater temperature is a major environmental with fish size and age (PALOHEIMO & DICKIE, influence (BUREL et al., 1996) on metabolic rate 1966; PANDIAN, 1967; PAULY, 1986), increased and food intake (CHO, 1992), as confirmed by our feeding frequency (TSEVIS et al., 1992), lower low and negative SGR values in winter when lipid contents (KALOGEROPOULOS et al., 1992) the seawater temperature was less than 11.8°C, or higher lipid contents (PERES & OLIVA-TELES, although we maintain that body weight is more 1999). GOOLISH and ADELMAN (1984) explained influential than seawater temperature. The SGR 60 ACTA ADRIATICA, 45(1): 51-63, 2004 value positively correlated to the food intake amino acid composition was much better in the (BUREL et al., 1996). diet containing 35% blue mussel flesh than in There was a significantly slower weight the other two diets. increase in November at the temperature of 15°C and growth was inhibited until April ACKNOWLEDGEMENTS when the temperature began to rise. During that We are very grateful to ALMA Futter, period, the length increase was greater than the Friedrich BOTZENHARDT KG, Kempten, weight increase, causing the condition factor to Germany, that provided us the artificial food drop. used in this experiment. Thanks also to Jadranka The results of the present experiment showed MARUŠIĆ M.Sc., Laboratory for Chemical that diets F1 and F2 were less satisfactory for Analysis, Institute of Public Health, Split, for growth of gilthead sea bream juveniles than chemical analysis of the food and Miss Neda diet F3. Fish fed diet F3 had the best weight SKAKELJA and Miss Iva MILIĆ-ŠTRKALJ for help gain and survival. Obviously, the quantities of in English. The authors thank two anonymous protein and fat were not responsible for the referees for their helpful and useful comments better performance of diet F3. Probably, the on the manuscript.
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Received: 25 September 2003 Accepted: 10 February 2004 KRALJEVIĆ, TUDOR, DULČIĆ & SKARAMUCA: Growth and body composition of Sparus aurata (L.) 63
Učinci triju različitih vrsta hrane na rast i kemijski sastav tkiva komarče, Sparus aurata (L.)
Miro KRALJEVIĆ1, Mladen TUDOR1, Jakov DULČIĆ1 i Boško SKARAMUCA2
1Institut za oceanografiju i ribarstvo, P.P. 500, 21000 Split, Hrvatska
2Institut za oceanografiju i ribarstvo, Split, Laboratorij za ekologiju i akvakulturu, P.P. 83, 20000 Dubrovnik, Hrvatska
SAŽETAK
Divlja je mlađ komarče (Lt=6,9±0,9cm; W=4,3±1,8g) bila uzgajana u bazenima s otvorenim sustavom protočne morske vode pri promjenjivoj temperaturi (24,5-10,3oC) tijekom 15,0-16,6 mjeseci s tri različite vrste hrane. Komercijalni su starteri i peleti (F1) bili miješani s 35% kokošjega jaja (F2) i 35% usitnjenog mesa dagnje (F3). Riba uzgajana na F3 hrani je dobila 268g u 15,0, a ona na F1 i F2 hrani oko 250g u 16,6 mjeseci. Dnevna je stopa hranjenja (f) bila najviša u grupi F3 (11,74%), a najniža u grupi F1 (4,35%), dok su mjesečne krivulje vrijednosti dnevnih stopa uzimanja proteina (fp) bile vrlo slične onima od dnevnih stopa hranjenja. WILCOXON matched pairs test je pokazao statistički značajnu razliku (P < 0.001-0.01) za oba izračunata čimbenika (f; fp) između testiranih vrsta hrane. Međutim, ne postoji statistički značajna razlika (P = 0.11-0.58) u vrijednostima dnevnih stopa rasta (g) između ovih vrsta hrane. Razlike u ukupnoj učinkovitosti hrane (FE) između F1 i F2 grupe je statistički značajna (P < 0.001), upravo kao i između F1 i F3 (WILCOXON matched pairs test; P < 0.02). Neke su vrijednosti dnevne stope rasta (g), ukupne učinkovitosti hrane (FE), djelotvornosti ugradnje proteina (PER) i proizvodnje proteina (PPV) pokazale negativne vrijednosti u veljači i ožujku. Nije zabilježena statistički značajna razlika (P = 0.09-0.39) u vrijednostima specifične stope rasta (SGR) između testiranih vrsta hrane, dok su njihove mjesečne vrijednosti slijedile krivulju promjenjive godišnje temperature tijekom trajanja eksperimenta. Kemijski je sastav tkiva testiranih riba statistički značajno odstupao u nižem sadržaju vlage (65.0-68.5%) i višim sadržajem masti (8.4-10.3%) od onih iz prirodne sredine na početku (76.1; 3.7%) i kraju (73.6-75.9; 0.6-1.5%) eksperimenta.
Ključne riječi: Sparus aurata, mlađ, rast, kemijski sastav tkiva
ISSN: 0001-5113 ACTA ADRIAT., UDC: 595.1 (262.3) AADRAY 45 (1): 65-73, 2004 Original scientific paper
Monogenean parasites in Adriatic cage-reared fish
Ivona MLADINEO
Institute of Oceanography and Fisheries, P.O. Box 500, 21000 Split, Croatia E-mail: [email protected]
Monogenean parasites are the most ubiquitous and abundant parasites in the aquatic environment. In confined and stressful rearing conditions, their population easily can overpass their usual balance, proliferate and induce serious and hard-to-eradicate diseases. During a 9- month period, seven facilities along the Adriatic coast were monitored for the presence, prevalence and abundance of these parasites. Only three monogenean species - Diplectanum aequans, Lamellodiscus elegans and Sparicotyle chrysophrii - were isolated from only three cage-reared hosts - Dicentrarchus labrax, Sparus aurata and Diplodus puntazzo - but without clinically visible symptoms. Parasite population dynamics showed a strong relationship with environmental factors such as salinity and temperature and marked host specificity.
Key words: Monogenean infections, cage-reared fish, Adriatic Sea
INTRODUCTION Among the members of the monogenean group there are generalist genera with an Monogenean trematodes are the most affinity for diverse hosts while, as in case of numerous group of parasites. Because of Adriatic cage-reared fish monogeneans, there their primitive life cycle, rapid reproduction are specialist genera (DESDEVISES et al., 2002a). and prevalence in the host and geographical Generally, it is accepted that specific genera distributions, they are very suitable for have an affinity for a particular group of fish, mathematical modeling in ecology. The for example Monocotylidae are specific to highest number of monogenean species has chondroichthyes (CHISHOLM & WHITTINGTON, been isolated from fish populations, while the 1998). remaining species were found on amphibians The monogenean body consists of two and reptiles (exceptionally cephalopods and isopods). Around 95% of the monogenean parts: the anterior prohaptor and the posterior species are ectoparasites on gills and skin, an opisthaptor (Fig 1). archaic type of life, but a smaller proportion Species are identified mainly by the has exchanged their external habitats for mezzo morphology and accessory adhesive organs of or endoparasitism in the nasal or mouth cavity, the opisthaptor. The prohaptor also has adhesive esophagus, stomach, urinary bladder, cloaca, structures such as paired or unpaired suckers, coelom, rectal glands, ovaries, visceral wall or paired pseudosuckers or sucking grooves and heart (EUZET & COMBES, 1998). glandular structures. The mouth is (sub)terminal, 66 ACTA ADRIATICA, 45(1): 65-73, 2004
Fig. 1. A detail of lamelodisc of L. elegans (400 x) an esophagus is usually present and the caeca MATERIAL AND METHODS are bifurcated. The morphology of the reproductive system Seven fish farms in the Adriatic Sea were also helps identify species. Monogeneans are monitored from June 2001 to March 2002. hermaphrodites with one or more testicles, The farms were located at: I - Kaldonta Bay enveloped by a curled vas deferens. (Cres Island), II - Vela Luka Bay (Šolta Island), A copulatory male organ (the cirrus) can be III - Peleš Bay (near Primošten), IV - Žižanj present, simple or complex, with or without Island, V - Žižanj Island, VI - Maslinovac spiculi. The same is true for the genital porus. Island (Pelješac peninsula) and VII - Tajan Ovaries are compact, connected to a short Island (Pelješac peninsula). Sampling in winter uterus. A receptaculum seminis is present, but 2002 was conducted only in facilities II and III there may not be a vagina. In species with a because of weather conditions. vagina, sclerotization with thorns is very usual The same fish population was followed for (Fig 2). nine months. Fish were collected once every The parasites are mostly oviparous with a three months from offshore net pens, always direct life cycle (GELNAR, 2001). from the same cages. Samples included 30 sea This is the first study of the prevalence and bass (Dicentrarchus labrax), sea bream (Sparus abundance of monogeneans amongst Adriatic aurata), sharp-snout bream (Diplodus puntazzo) cage-reared fish. and red sea bream (Pagellus bogaraveo), all MLADINEO: Study of monogean parasites in the Adriatic cage reared fish 67
Fig. 2. An egg of S. chrysophrii in uterus with a detail of vaginal armature (lower left corner) (400 x) aged over one year. During the samplings, For every fish and fish species from a temperature, salinity, nutrient salts and oxygen particular facility, the prevalence and abundance were measured. were calculated according to BUSH et al. (1997). Sampled fish were put on ice and brought to the laboratory within hours, where they were RESULTS autopsied and measured. Fish gills and fins Diplectanum aequans (Monogenea, were placed in Petri dishes, while scrapings of Diplectanidae) skin and nasal cavities were mounted on slides for examination under a dissecting microscope As one of the most ubiquitous monogeneans at 20x magnification. Monogeneans were in cage-reared fish, D. aequans was found detached with dissecting needles, counted and in all the monitored farms, but with marked collected in watch glasses. For fixation, the differences in prevalence and abundance (Table 1). It showed a high specificity for sea bass and parasites were ruptured between the slide and was located mostly on the first gill arch. Gross cover slip by finger pressure and a mixture of pathologies were easily noticed as hemorrhagic 4% formaldehyde and glycerin (5:1) was placed to yellowish necrotic areas, with subsequent on the edge of the cover slip. After evaporation depletion of changed lamellae. In fresh mounts, of the excess fixative, the edges were sealed eggs were noticed throughout the year, being with DU-NOYER sealant. most abundant in summer. The mean prevalence 68 ACTA ADRIATICA, 45(1): 65-73, 2004 of D. aequans at all the facilities throughout the Sparicotyle chrysophrii (Monogenea, nine months was 62.03±23.63% with a mean Microcotylidae) abundance of 1.98±1.62. Although S. chrysophrii was the largest Lamellodiscus elegans (Monogenea, monogenean in the Adriatic cage-reared fish, it Lamellodiscinae) made no marked changes or gross pathologies in the host because of its low prevalence and L. elegans showed specificity for members abundance. It was ubiquitous, specific to sparids of the Sparidae family, especially sharp-snout (especially the sharp-snout bream), and present bream. It was ubiquitous and present throughout throughout the year. Mixed infections with the year, having the highest abundance among the more abundant L. elegans were frequent, all the isolated monogeneans. It preferred mainly in the sharp-snout bream. S. chrysophrii the first gill arch and peripheral parts of the was isolated mostly from the central part of the lamellae, however, in mass infections, it was lamellae, with opisthaptor hooks attached to distributed throughout the length of the lamella rows of neighboring lamellae (Figs. 4, 5). (Fig 3). The mean prevalence was 35.50±27.23% The mean prevalence of L. elegans was with a mean abundance of 2.44±6.86. 64.95±33.13% with a mean abundance of No monogenean species were isolated from 13.00±21.45. red sea bream.
Fig. 3. Posterior part with attaching apparatus of L. elegans (400 x) embedded in lamellar epithelia (400 x) MLADINEO: Study of monogean parasites in the Adriatic cage reared fish 69
Fig. 4. Posterior part of S. chrysophrii with attaching apparatus (100 x)
Fig. 5. Numerous hamuli of S. chrysophrii (400 x) 70 ACTA ADRIATICA, 45(1): 65-73, 2004
Table 1. Prevalence and abundance of monogeans in cage-raised fish in seven Adriatic facilities
Facility Summer Fall Winter Spring Prevalence Abundance Prevalence Abundance Prevalence Abundance Prevalence Abundance Diplectanum aequans in Dicentrarchus labrax I 100 3.58 85.71 4.07 - - 60 2.8 II 85.71 3.21 93.33 5.13 66.66 1 46.14 0.7 III 71.42 1.21 46.66 1.6 64.28 1 30 0.4 IV 100 4.21 78.57 4.78 - - 66.66 1.22 V 57.14 0.86 92.85 4.29 - - 60 1.9 VI 28.57 0.36 35.71 0.43 - - 44.44 1.33 VII 50 0.71 42.85 0.58 - - 20 0.2 Lamellodiscus elegans in Sparus aurata(*) and Diplodus puntazzo I 100 19.25 100 28.5 - - 100; 60* 14.2; 1.2* II 21.48* 1.71* 53.33* 1.73* 3.33* 0.3* 50* 0.9* III 0 0 0 0 0 0 30* 0.5* 85.71; 12.14; IV 100 80 100 20 - - 45.45* 0.64* V0 000--60* 0.8* VI 0 0 0 0 - - 0 0 VII 0 0 0 0 - - 0 0 Sparicotyle chrysophrii in Sparus aurata(*) and Diplodus puntazzo 6.13; 7.14; I 16.66* 0.58; 0.25* 42.85* 28.5; 0.5* - - 30 1.1 II 42.85* 0.64* 66.67* 1.33* 10* 0.1* 20* 0.2* III 0 0 0 0 0 0 10* 0.1* IV 100 1.67 71.42 3 - - 14.28 0.14 V0 057.14* 0.71* - - 30* 0.3* VI 0 0 0 0 - - 0 0 VII 0 0 0 0 - -- 0 0
DISCUSSION fish families (HAYWARD, 1996; KRITSKY et al., 2000). The only record of Diplectanidae among Diplectanum aequans is an almost wild Adriatic Sea fish concerns Sciena umbra unavoidable parasite in sea bass cage and Umbrina cirrosa, in which RADUJKOVIĆ populations, causing mortalities mainly in & RAIBAUT (1989) found five Diplectanidae juvenile fish. During mass infections in species. summer months, mortalities complicated with D. aequans is greatly impacted by Photobacterium damselae subsp. piscicida often environmental factors, especially temperature. occur (MLADINEO, 2002). In rearing conditions, CECCHINI et al. (1998) noticed that developing it was isolated only from sea bass, while in the oncomiracidia are preserved for quite some time wild it parasitizes hosts from a wide range of at 5°C, allowing the proliferation of the parasite MLADINEO: Study of monogean parasites in the Adriatic cage reared fish 71 in early spring when temperatures are still low as Diplectanum sp.; the highest values were and other parasites are absent (CECCHINI et al., recorded during summer, when a major gross 2001). This pattern was noticed in our study, as pathology occurred but without mortality. D. aequans was present throughout the year. Sparicotyle chrysophrii had the lowest The peak season of infection was the end of prevalence and abundance of the three parasites summer/beginning of fall, when the temperature but the same seasonal pattern. It was not found in was around 25°C. This temperature allows the facilities near freshwater in-flows and preferred parasite to develop a numerous population sharp-snout bream. RADUJKOVIĆ & RAIBAUT in fall, which survives in winter at a lower (1989) isolated the parasite in the wild only from abundance and prevalence. Salinity is another sea bream; CAFFARA et al. (1998) isolated it from important environmental factor for D. aequans sea bream in lagoon rearing systems. development. Less saline locations near river Similar to other studies (COGNETTI VARRIALE deltas (VI and VII) have considerably lower et al., 1993; OLIVA & LUQUE, 1998), all isolated prevalence and abundance values. Although species preferred the central part of the first gill the prevalence of this monogenean was high, arch lamellae. its abundance was not high enough (maximum Only the red sea bream had no monogenean 5.13) to threaten a serious disease outbreak in infections even captured from the wild and kept more or less controlled rearing conditions. for rearing, perhaps due to the very low density Lamellodiscus elegans has both seasonality of hosts in the net pen. and a strong specificity for sparid species. L. elegans, a member of the subfamily CONCLUSIONS Lamellodiscinae, has been subjected to many studies of co-evolution trends between hosts Monogenean parasitofauna of Adriatic and parasites (DESDEVISES et al., 2002b). This cage-reared fish did not show marked species monogenean is the most prevalent and abundant richness; only three monogenean species were species in Adriatic cage-rearing systems isolated from only three fish species. The most while, in wild fish populations, RADUJKOVIĆ parasitized was the sharp-snout bream, where & RAIBAUT (1989) found moderate infection all sampled fish often harbored monogeneans. (22.2-50% prevalence; 4.65-19 abundance). However, the sharp-snout bream is not widely Even when the abundance was higher than 80 reared in the Adriatic. parasites per host, L. elegans was restricted only While the prevalence, abundance and to sparid species, especially the sharp-snout host specificity differed, the three parasites bream. DESDEVISES et al. (2002a) explain this as had a similar and well-established pattern of a preference of the parasite for larger hosts, in population dynamics throughout the year. this case, the sharp-snout bream. On the other Mixed infections and same microhabitat hand, CARO et al. (1997), although their study did preferences were not unusual, proving intra- and not include Diplectanidae, did not find a strong interspecific tolerance of the monogeneans. Low correlation between trematodes and host size. salinity affected all three species. There have been Lamellodiscus sp. does not show no reports of mortality related to monogeneans, interspecific competency as mixed infections even in cases with obviously gross pathological with monocotylid monogenean are frequent, changes on the gills. Thus, it can be concluded although at a lower abundance and prevalence. that the monogenean populations in this rearing Intraspecific competency also does not exist system are still tolerable. as, in extreme cases of infection, two to five individuals could be isolated at the same site. ACKNOWLEDGEMENTS The same environmental factors that have an impact on D. aequans affect L. elegans, though The author thanks two anonymous referees L. elegans is more sensitive to low salinity. for their helpful and useful comments on the L. elegans followed the same seasonal pattern manuscript. 72 ACTA ADRIATICA, 45(1): 65-73, 2004
REFERENCES
BUSH, A.O., K.D. LAFFERTY, J.M. LOTZ & A.W. in the genus Lamellodiscus (Monogenea). SHOSTAK. 1997. Parasitology meets Biol. J. Linn. Soc., 77: 431-443. ecology on its own terms: Margolis et al. DESDEVISES, Y., S. MORAND, O. JOUSSON & P. revisted. J. Parasitol., 83: 575-583. LEGENDRE. 2002b. Coevolution between CAFFARA, M., R. GALUPPI, S. GIANNETTO, C. Lamellodiscus (Monogenea: Diplectanidae) MINELLI & M.P. TAMPIERI. 1998. Sparicotyle and Sparidae (Teleostei): the study of a (Microcotyle) chrysophrii (Monogenea, complex host-parasite system. Evol., 56(12): Microcotylidae) parasite in seabream 2459-2471. (Sparus aurata). 20 Congresso di Società EUZET, L. & C. COMBES. 1998. The selection Italiana di Parassitologia: La parassitologia of habitats among the monogenea. Int. J. italiana tra storia ed attualità, Roma, Italy. Parasitol., 28: 1645-1652. 17-20 June 1998. GELNAR, M. 2001. Monogenea. Workshop CARO, A., C. COMBES & L. EUZET. 1997. and Training Course on Fish Parasites. What makes a fish a suitable host for Biological Station Neusiedler See, Austria, Monogenea in the Mediterranean. J. April 28-May 4. Helminth., 71: 203-210. HAYWARD, C.J. 1996. Revision of diplectanid CECCHINI, S., M. SAROGLIA, P. BERNI & A.M. monogeneans (Monopisthocotylea, COGNETTI VARRIALE. 1998. Influence of Diplectanidae) in sillaginid fishes, with temperature on the life cycle of Diplectanum the description of a new species of aequans (Monogenea, Diplectanidae), Monoplectanum. Zool. Scripta, 25(3): 203- parasitic on sea bass, Dicentrarchus labrax 213. (L.). J. Fish Dis., 21: 73-75. KRITSKY, D.C., F.A. JIMENÉZ-RUIZ & O. SEY. CECCHINI, S., M. SAROGLIA, A.M. COGNETTI 2000. Diplectanids (Monogenoidea: VARRIALE, G. TEROVA & G. SABINO. 2001. Dactylogyridea) from the gills of marine Effect of low environmental temperature on fish of the Persian Gulf off Kuwait. Comp. embryonic development and egg hatching Parasitol., 67(2): 145-164. of Diplectanum aequans (Monogenea, Diplec tanidae) infecting European sea bass, MLADINEO, I. 2002. A case study of pasteurellosis Dicentrarchus labrax. Fish Pathol., 36(1): epizootic and heavy parasite infection in 33-34. Adriatic. In: Abstracts, Recent Findings on CHISHOLM, L.A. & I. D. WHITTINGTON. 1998. the Development of New Vaccines against Morphology and development of haptors Fish Pasteurellosis, Udine, Italy, November among the Monocotylidae (Monogenea). 23. Hydrobiol., 383: 251-261. OLIVA, M.E. & J.L. LUQUE. 1998. Distribution COGNETTI VARRIALE, A.M., A. CASTELLI, S. patterns of Microcotyle nemadactylus CECCHINI & M. SAROGLIA. 1993. Study (Monogenea) on gill filaments of of Diplectanum aequans (Monogenea), Cheilodactylus variegatus (Teleostei). Mem. parasite of sea bass (Dicentrarchus labrax) Inst. Oswaldo Cruz., 93(4): 477-478. in intensive farming. Prod. Environ. Qual., RADUJKOVIĆ, B.M. & A. RAIBAUT. 1989. Faune 18: 143-153. des parasites de poissons marins des côtes DESDEVISES, Y., S. MORAND & P. LEGENDRE. 2002a. du Monténégro (Adriatique Sud). Acta Evolution and determinants of host specificity Adriat., 30(1/2): 5-319.
Received: 21 August 2003 Accepted: 11 February 2004 MLADINEO: Study of monogean parasites in the Adriatic cage reared fish 73
Istraživanje jednorodnih metilja kavezno uzgojene ribe Jadranskoga mora
Ivona MLADINEO
Institut za oceanografiju i ribarstvo, P.P. 500, 21000 Split, Hrvatska E-mail: [email protected]
SAŽETAK
Jednorodni metilji predstavljaju najrasprostranjeniju i najabundantniju skupinu nametnika u vodenom okolišu. U ograničenim i stresnim uvjetima uzgoja njihova populacija lako prelazi njihovu uobičajenu populacijsku ravnotežu, proliferirajući i inducirajući ozbiljnu bolest, tešku za iskorjenjivanje. Tijekom devetomjesečnog razdoblja, sedam uzgajališta uz obalu Jadranskoga mora praćeno je s obzirom na prisutnost, prevalenciju i abundanciju ovih nametnika. Samo tri vrste jednorodnih metilja - Diplectanum aequans, Lamellodiscus elegans i Sparicotyle chrysophrii, izolirane su s tri vrste uzgojenih ribljih domaćina - Dicentrarchus labrax, Sparus aurata i Diplodus puntazzo, ali bez indukcije klinički vidljivih znakova invazije. Njihova populacijska dinamika ovisi jako o okolišnim čimbenicima kao što su slanost i temperatura te specifičnosti prema domaćinu.
Ključne riječi: Invazije jednorodnim metiljima, kavezno-uzgojena riba, Jadransko more
ISSN: 0001-5113 ACTA ADRIAT., UDC:543.3:594.1]:504.054 (262.3) AADRAY 45 (1): 75-81, 2004 Original scientific paper
Testing quality of sea water from the Adriatic coast of Croatia with toxicity, genotoxicity and DNA integrity tests
Nevenka BIHARI, Milena MIČIĆ, Maja FAFANĐEL, Bojan HAMER, Željko JAKŠIĆ and Renato BATEL
Laboratory for Marine Molecular Toxicology, Center for Marine Research, Institute “Ruđer Bošković”, G. Paliaga 5, 52210 Rovinj, Croatia
The quality of sea water along the Adriatic coast of Croatia was evaluated three times during 1.5 years at 16 sites located in protected, urban, industrial, harbor or brackish areas. Samples of sea water (30 l) were tested by the Microtox test for toxicity and the umu-test for genotoxicity. Samples of mussel gills (5 individuals, Mytilus galloprovincialis) were collected from each sampling site and the Fast Micromethod® was used to test DNA integrity, which may have been altered by water contaminants. According to the Microtox text, 75% of the water samples were potentially toxic. According to the umu-test, 40% were potentially genotoxic. Alteration of DNA integrity was detected in 40% of the mussel gill samples.
Key words: Toxicity, genotoxicity, DNA damage, Microtox, SOS/umu-test, Fast Micromethod®
INTRODUCTION In this study, the Microtox test for toxicity measurements (BULICH & ISENBERG, 1981; The need to detect and assess the impact BIHARI et al., 1989), the umu-test for genotoxicity of pollutants, particularly low concentrations measurements (ODA et al., 1985; HAMER et al., of complex mixtures, on environmental quality 2000) and the Fast Micromethod® for DNA has led to the development of several assay integrity measurements (BATEL et al., 1999) methods. Monitoring of water by chemical were performed. They appeared to be simple, analysis requires a precise knowledge of the fast and inexpensive methods for in vitro and contaminants being looked for, is limited in vivo evaluation of pollution in the marine by sensitivity of the detection method, environment. The Microtox test is based on the measures only some xenobiotics, and gives fact that luminescence of the marine bacterium no information about biological effects. In Vibrio fischeri is inhibited when the organism contrast, biomonitoring takes advantage of is exposed to toxic substances. The umu-test the fact that organisms combat pollution by is based on the ability of genotoxins to induce accumulating xenobiotics under less toxic forms expression of the umuC gene, measured as the or in spatial compartments and/or by inducing increase of ß-galactosidase activity in Salmonella typhimurium (TA1535/pSK1002 tester strain). biotransformation mechanisms that can be The data obtained by these tests indicate water assayed to show the presence and effects of quality at the time the water samples were known and unknown contaminants. collected. Reflection of long-term genotoxicity 76 ACTA ADRIATICA, 45(1): 75-81, 2004 in the marine environment can be detected by and genotoxic effects on the marine environment in vivo tests such as the Fast Micromethod®, can be expected. Such so-called “hot spots”, as which estimates potential genotoxicity by well as presumably pristine waters in protected measuring genetic endpoints (such as strand areas, were monitored from August 1998 to breaks) that show primary DNA damage. October 1999 under a national monitoring This is a quick and convenient procedure for program. Preliminary results are presented in determining DNA damage in cell suspensions this paper. Analyses for contaminants were not and solid tissues on single microplates. performed since, due to complex biological However, because the Fast Micromethod® responses to mixed pollution, they would reveal measures only single strand breaks and alkali- nothing about potential adverse effects of the labile sites, it can miss DNA alterations water quality. Our approach in this study was involving processes such as cross-linkage to collect information on water quality in “hot induction, nucleotide substitution and adduct spots” along the Adriatic coast of Croatia that formation. Mussels (Mytilus galloprovincialis) would allow us to focus on chemical analysis are good indicator organisms for identifying in the future. environmental changes of unknown origin resulting from mixtures of contaminants, e.g., MATERIALS AND METHODS industrial effluents (VUKMIROVIĆ et al., 1994). Earlier studies confirm that Mytilus spp. is a Sampling sites useful organism for studying pollution (BAYNE, Seawater quality along the Adriatic coast of 1976; GOSLING, 1992). In the present study, DNA Croatia was evaluated at 16 sites in protected strand breaks were measured in mussel gills by (sites 1,2), harbor (sites 3,4,5,6,16), urban (sites the Fast Micromethod®. 7,8,9,10,11,13), industrial (site 12) or brackish There is scarcity of data regarding the quality (site no 14,15) areas (Fig. 1). Seawater samples of the marine environment along the Croatian (30 l) and mussels (5 individuals) were collected Adriatic coast. Some areas are influenced by from each site in August 1998, August 1999 and urban, industrial or harbor wastes, therefore toxic October 1999.
Fig. 1. Sampling sites along the Adriatic coast, Croatia BIHARI, MIČIĆ, FAFANĐEL, HAMER, JAKŠIĆ & BATEL: Sea water quality of the Adriatic coast 77
Seawater extraction saline. Eight dilutions corresponding to 1250, 625, 312, 156, 78, 39, 20 and 10 ml of sea Non-polar compounds from seawater water and a saline blank were tested. Equivalent samples (30 l) were concentrated at the time of volumes (ml) of sea water for each dilution collection on amberlite XAD-7 resin columns were obtained from the equation: Equivalent -1 (20 ml) by gravity at a flow rate of 200 ml min volume of sea water (in ml) = original volume and transported to the laboratories of the Center of water collected (30 l) x volume of extract (in for Marine Research in Rovinj. Adsorbed µl) total extract volume (300 µl), where volume compounds were eluted with 150 ml acetone, of extract = volume of extract in starting evaporated until nearly dry and extracted with dilution (12.5 µl)/dilution factor. After 15 min 70 ml dichloromethane. Dichloromethane incubation in the extract, the bioluminescence extracts were evaporated to dryness, dissolved of the bacteria was measured, compared to the in 300 µl dimethylsulfoxide (DMSO) and stored blank samples and corrected for spontaneous at -20°C prior to toxicity (Microtox test) and decline in photoactivity. Results are expressed genotoxicity (umu-test) assays. 12.5 µl of total as ml of sea water that caused a 50% reduction extracts (300 µl), diluted in 0.5 ml 2% saline, of bioluminescence in 15 min (EC50). Estimates were used as starting sample concentrations of EC50 were obtained using linear regression for the toxicity assay while 20 µl aliquots were analysis (SCHIEWE et al., 1985; BIHARI et al., 1989). used in the genotoxicity assay. Higher amounts 2.5 µgml-1 4-nitroquinoline-N-oxide reduced were not tested due to possibly false positive bacterial bioluminescence by 50% and was, results induced by the solvent (DMSO). therefore, used as a positive control. The toxic potential of seawater samples was reported Tissue preparation in cases where less then 1250 ml of seawater caused the same effect. Gills of mussels Mytilus galloprovincialis Lmk. (Mollusca: Bivalvia) were removed from 10-g mussels at the place of collection, stored in SOS/umu-test liquid nitrogen and transported to the laboratory. The SOS/umu test was performed according 100 mg of gill tissue were homogenized in 2 ml to ODA et al. (1985) and HAMER et al. (2000) with TE buffer (1 mM EDTA, 10 mM Tris-HCl, pH a slight modification. Briefly, an overnight 7.4) and DMSO (9:1) in liquid nitrogen with a culture was diluted 50-fold with TGA medium mortar and pestle pre-cooled in liquid nitrogen. and incubated at 37°C until the bacteria reached The pellets were collected in test tubes and the exponential growth stage. The incubation stored at -80°C. mixture consisted of 800 µl bacterial culture, 180 µl 0.1 M phosphate buffer pH 7.4 and 20 Microtox test µl of the seawater sample. After 2 h incubation at 37°C, the bacterial suspension was diluted The luminescence of marine bacterium 5-fold with warm TGA medium and incubated Vibrio fischeri NRRL B-11177 (DIN EN ISO at 37°C for an additional two hours. Bacterial 11348-3, BioFix® Lumi, MACHERY-NAGEL, growth was measured as turbidity at 600 nm and Düren, Germany), exposed to a series of dilutions as the level of ß-galactosidase activity at 420 with water extracts, was measured in a PACKARD nm, using o-nitrophenyl-ß-D-galactopyranoside Tri-Carb 2500 TR liquid scintillation analyzer as the substrate (MILLER, 1972). Genotoxic for toxicity assay (Microtox test). Briefly, 0.5 activity was expressed as the ratio of induction ml of a 2% saline suspension containing 106 of enzyme units in the tested sample to exponentially growing luminescent bacteria induction of enzyme units in the control, which was diluted (1:2) with 0.5 ml of extracted sea contained only DMSO. Induction ratios above water, starting with 12.5 µl extract in 0.5 ml 2% 1.5 are considered sufficiently positive by DIN 78 ACTA ADRIATICA, 45(1): 75-81, 2004 and ISO standards. Genotoxicity results are sites were grouped according to characteristic expressed as ml of sea water that resulted in an contamination into five groups: protected, induction ratio of at least 1.5. Six serial dilutions harbor, urban, industrial and brackish areas. The (1:2) with seawater extracts corresponding to toxicity, genotoxicity and DNA integrity results 2000, 1000, 500, 250, 125, and 63 ml of sea did not follow the grouping according to type of water and the blank (DMSO) were tested. As a contamination. positive control, 30 ngml-1 4-nitroquinoline-N- oxide was used. DISCUSSION
Fast Micromethod® Toxicity, genotoxicity and DNA integrity differed with time of collection and site. The DNA integrity assay (Fast Since significant recovery of pollutants can Micromethod®) detected changes in the pattern be achieved by concentrating seawater on of DNA denaturation. Directly altering DNA XAD columns (PAOLA et al., 1993), we used integrity in mussel gills lysates at alkaline this procedure to analyze toxicity in up to pH and the time dependence were measured 1250 ml and genotoxicity in up to 2000 ml of in a Fluoroscan Ascent microplate reader sea water. According to the Microtox assay, (Labsystems, Finland). Briefly, 25 µl of a lysing 75% of the analyzed samples were potentially solution (4.5 M urea, 0.1% SDS, 0.2 M EDTA, toxic. According to the SOS/umu-test, 40% pH 10) supplemented with PicoGreen (20 µl of the samples were potentially genotoxic. of the original stock dye/P-7581, Molecular Alteration of DNA integrity in mussel gills Probes Inc., Eugene, Oregon/per ml of lysing was detected in 40% of the samples with the solution) was added to 25 µl gill homogenate Fast Micromethod®. Half of the affected mussel (100 ng DNA/ml). The microplates were kept samples were collected in October 1999. in darkness for 30 min. DNA denaturation Correlation analysis between toxicity, conditions were achieved at pH 11.5 with 250 genotoxicity and changes in DNA integrity was µl NaOH-EDTA solution. The extent of DNA performed. Values that were not toxic at the denaturation was followed in the microplate highest concentration tested were excluded from by measuring the decline in fluorescence the calculation and the correlation assessment of the dsDNA-PicoGreen complex at room was limited to samples with quantifiably temperature every 30 sec for at least 20 min. definable endpoints. No correlation (toxicity vs The number of strand breaks in DNA of genotoxicity r2 = 0.029, n = 11; toxicity vs DNA mussel gills was expressed as strand scission integrity r2 = 0.003, n = 31; genotoxicity vs DNA 2 factors (SSF) and calculated as: SSF = log10 integrity r = 0.11, n = 18) was observed, which (% dsDNAsite x sample/% dsDNAsite 1 sample) after 5 can be explained by the collective effect of the min denaturation. DNA integrity was expressed pollutants that differed from site to site (BEG as the increase in number of DNA strand breaks, et al., 2001). Further, water genotoxicity data relative to the effect of 1 µg 4-nitroquinoline-N- depend on sampling time and site which are oxide/g mussel, considered 1.0 (SSF = 0.17). influenced by currents, winds, tides, frequency of wastewater inputs, etc., while DNA integrity RESULTS in mussel gills reflects the acute and chronic effects of exposure. This may be the reason that Forty-eight seawater samples taken along there was no correlation between genotoxicity the Adriatic coast of Croatia were analyzed for and DNA integrity. toxic and genotoxic potential. Two hundred and According to the Microtox test, extractable forty mussels were analyzed for DNA integrity organic compounds of 12 seawater samples (5 mussels per sampling per site). The results (from sites 1,2,6,7,9,10 in August 1998, 5, 7, 8, for all samples are shown in Table 1. Sampling 15 in August 1999 and 2,12 in October 1999) BIHARI, MIČIĆ, FAFANĐEL, HAMER, JAKŠIĆ & BATEL: Sea water quality of the Adriatic coast 79
Table 1. Toxicity, genotoxicity and DNA integrity data for sampling sites along the Adriatic coast of Croatia Site type Site Toxicity1 Genotoxicity2 DNA integrity3 No Aug 98 Aug 99 Oct 99 Aug 98 Aug 99 Oct 99 Aug Aug Oct 98 99 99 Protected 1 >1250 208 547 >2000 890 896 0.0 0.0 0.1 2 >1250 60 >1250 387 968 953 1.0 0.7 2.6 Harbor 3 184 154 56 >2000 >2000 >2000 1.3 0.3 0.3 4 625 76 763 >2000 >2000 416 1.1 0.6 2.5 5 1000 >1250 ++ >2000 >2000 209 0.6 0.3 2.1 6 >1250 52 187 >2000 >2000 1466 2.0 1.3 2.4 16 123 103 226 89 >2000 >2000 0.7 0.8 2.5 Urban 7 >1250 >1250 ++ 1461 >2000 >2000 1.8 0.1 2.4 8++>1250 ++ 105 >2000 >2000 0.6 1.0 0.7 9 >1250 572 1243 >2000 >2000 444 0.4 1.5 2.1 10 >1250 817 73 96 >2000 >2000 0.0 0.7 3.4 11 718 1200 1080 >2000 >2000 762 2.3 1.4 1.8 13 131 617 112 >2000 >2000 976 0.6 1.5 2.6 Industrial 12 297 749 >1250 107 >2000 >2000 0.8 0.1 3.0 Brackish 14 325 1100 863 87 >2000 >2000 0.7 0.6 2.2 15 869 >1250 ++ >2000 >2000 888 0.2 1.2 0.5
1 Microtox test: ml sea water that caused a 50% reduction of bacterial bioluminescence in 15 min (EC50). ++ = increase in bacterial luminescence 2 umu-test: ml sea water that caused a 1.5-fold increase in bacterial ß-galactosidase activity compared to control samples 3 Fast Micromethod®: increase in number of DNA strand breaks in mussel gills, relative to the effect of 1 µg/g NQO, considered 1.0
were not potentially toxic (EC50 >1250 ml). The material content commonly present at each highest toxicity (EC50 <100 ml) was detected sampling site. at sites 2, 4, 6 in August 1999 and 3, 10 in According to the SOS/umu-test, extractable October 1999 while bacterial luminescence organic compounds from less than 100 ml increased in five samples (site 8 in August 1998 of sea water that induced a 1.5-fold increase in ß-galactosidase activity were detected and 5,7,8,15 in October 1999). Unexpectedly, in three samples (sites 10,14, 16 in August the extracts from protected areas were highly 1998). For comparison, 160 ml of waste-water toxic, raising questions regarding the pristine taken near a spill from a tobacco factory, and status of protected waters that could serve as viewed as industrial pollution, caused more reference or control sites. Toxicity testing could than a 1.5-fold increase in ß-galactosidase be improved by determining the total organic activity (HAMER et al., 2000). In August 1999, 80 ACTA ADRIATICA, 45(1): 75-81, 2004 only two samples (sites 1,2) were genotoxic variability in DNA damage related to a specific but two months later, in October 1999, eight site or time of mussel collection could not be samples (sites 1,2,4,5,9,11,13,15) contained determined by this study. sufficient genotoxins in less than 1000 ml of Our findings, although preliminary, show sea water to be genotoxic. Such irregular and the potential usefulness of toxicity, genotoxicity weak mutagenic effects of seawater samples and DNA integrity testing for seawater quality on Salmonella typhimurium have already been assessment. They enhance the necessity for reported (PAOLA et al., 1993). further and more frequent monitoring that is The gills of 240 mussels were examined currently being undertaken in our laboratory. More frequent monitoring will allow better for DNA integrity. DNA was altered in mussel statistical analysis and we expect that variations gills collected at five sites (3,4,6,7,11) in in toxicity, genotoxicity and DNA integrity data August 1998 and five sites (6,9,11,13,15) in among sampling areas will differ significantly August 1999. An increase in the level of DNA from the variations at the same sampling sites. damage two months later (October 1999) at 12 of the 16 sites indicates seasonal influences on DNA integrity in mussel gills. DNA damage ACKNOWLEDGMENTS in samples from sites 6 and 11 was detected This study was funded by the CROATIAN at all three sampling times. It appears that the MINISTRY OF SCIENCE AND TECHNOLOGY input of contaminants at those sites was stable (PROJECT “JADRAN”). throughout the study period. The cause(s) of the
REFERENCES
BATEL, R., Ž. JAKŠIĆ, N. BIHARI, B. HAMER, M. assessment of aquatic toxicity. Trans. Am. FAFANĐEL, C. CHAUVIN, H.C. SCHRÖDER, Instrument Soc., 20: 29-33. W.E.G. MÜLLER & R.K. ZAHN. 1999. DIN 38415-3. German standard methods for A microplate assay for DNA damage the examination of water, waste water and determination (Fast Micromethod®) in sludge - Sub-animal testing (group T) - Part cell suspensions and solid tissues. Anal. 3: Determination of the genotoxic potential Biochem., 270: 195-200. of water with the umu-test (T3). BAYNE, B.L. 1976. Marine Mussels: Their HAMER B., N. BIHARI, G. REIFFERSCHEID, Ecology and Physiology. Cambridge Univ. R.K. ZAHN, W.E.G. MÜLLER & R. BATEL. Press, London. 2000. Evaluation of the SOS/umu-test BEG, M.U., S. AL-MUZAINI, T. SAEED, P.G. JACOB, post-treatment assay for the detection of K.R. BEG, M. AL-BAHLOUL, M. AL- MATROUK & genotoxic activities of pure compounds and T. AL-OBAID. 2001. Chemical contamination complex environmental mixtures. Mutat. and toxicity of sediment from a coastal area Res., 466: 161-171. receiving industrial effluents in Kuwait. GOSLING, E.M. 1992. The Mussel Mytilus: Arch. Environ. Contam. Toxicol., 41: 289- Ecology, Physiology, Genetics and Culture. 297. Elsevier, Amsterdam. BIHARI N., M. NAJDEK, R. FLORIS, R. BATEL & R.K. ISO/CD 13829: Water quality - Determination of ZAHN. 1989. Sediment toxicity assessment the genotoxicity of water and wastewater using bacterial bioluminescence: effect of using the umu-test. an unusual phytoplankton bloom. Mar. Ecol. MILLER, J.H. 1972. In: Experiments in Molecular Prog. Ser., 57: 307-310. Genetics. Cold Spring Harbor Laboratory, BULICH A.A. & D.L. ISENBERG. 1981. Use of the New York, pp. 352-355. luminescent bacterial system for the rapid BIHARI, MIČIĆ, FAFANĐEL, HAMER, JAKŠIĆ & BATEL: Sea water quality of the Adriatic coast 81
ODA Y., S. NAKAMURA, I. OKI, T. KATO & H. SCHIEWE, M.H., E.G. HAWK, D.I. ACTOR & SHINAGAWA. 1985. Evaluation of the M.M. KRAHN. 1985. Use of bacterial new system (umu-test) for detection of bioluminescence assay to assess toxicity of environmental mutagens and carcinogens. contaminated marine sediments. Can. J. Fish Mutat. Res., 147: 219-229. Aquat. Sci., 42: 1244-1248. PAOLA, V., B. ANTONELLA, N. GIANCARLO & VUKMIROVIĆ, M., N. BIHARI, R.K. ZAHN, W.E.G. L.A. GINO. 1993. Detection of mutagenic, MÜLLER & R. BATEL. 1994. DNA damage in pollutants of inland and coastal waters by marine mussel Mytilus galloprovincialis as a means of the Salmonella microsome assay. biomarker of environmental contamination. Environ. Technol., 14: 543-553. Mar. Ecol. Prog. Ser., 109: 165-171.
Received: 19 February 2003 Accepted: 13 February 2004
Kvaliteta morske vode uzduž jadranske obale bazirane na osnovi rezultata toksičnosti, genotoksičnosti i cjelovitosti DNA
Nevenka BIHARI, Milena MIČIĆ, Maja FAFANĐEL, Bojan HAMER, Željko JAKŠIĆ i Renato BATEL
Laboratorij za morsku molekularnu toksikologiju, Zavod za istraživanje mora, Instituta “Ruđer Bošković”, Obala G. Paliagta 5, 52210 Rovinj, Hrvatska
SAŽETAK
Uzorci morske vode i škrge školjkaša uzimani su sa 16 lokacija zaštićenog i bočatog područja, kao i s područja s urbanim, industrijskim i lučkim utjecajem uzduž jadranske obale. Za određivanje toksičnosti koristio se Microtox test, za određivanje genotoksičnosti SOS/umu - test, te za određivanje cjelovitosti DNA molekule tzv. Fast Micromethod® test. 75% analiziranih uzoraka vode pokazalo je toksičnost, 40% uzoraka vode pokazalo je genotoksičnost, dok je 40 % uzoraka škrga dagnji pokazalo oštećenje DNA.
Ključne riječi: Toksičnost, genotoksičnost, oštećenje DNA, Microtox, SOS/umu-test, Fast Micromethod®
ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.:591.13(81)(26.04 Guaratuba) AADRAY 45 (1): 83-94, 2004 Original scientific paper
Trophic organization and functioning of fish populations in the Bay of Guaratuba, Brazil, on the basis of a trophic contribution factor
Paulo CHAVES1 and Jean-Luc BOUCHEREAU2
1Dept. de Zoologia, Universidade Federal do Paraná, P. O. Box 19020, 81531-990, Curitiba, Brésil E-mail: [email protected] 2Lab. de Biologie Marine, E.A. 926, Université Antilles-Guyane, BP 592, F-97159, Pointe-à-Pitre Cedex, France E-mail: [email protected]
Trophic organization and seasonal development in the Bay of Guaratuba (Brazil) are characterized, based on feeding habits of fish species taken from the literature and on a factor that combines biomass and species richness to determine to what extent detritus and primary production contribute to the trophic network. The Bay of Guaratuba contains all trophic categories of fish: herbivores, plankton-eaters, consumers of invertebrates with occasional supplementation of plants and fish, and fish-eaters. Resident and migrant species occupy different trophic ranges, depending on whether their food sources are available on a permanent or seasonal basis. Residents tend to feed on benthic invertebrate meiofauna and macrofauna, using relatively more detritus than primary production sources. Migrants time their presence in the bay with seasonal productivity, especially of plants. Most occasional visitors consume invertebrates plus fish or primarily fish. The fish-eaters could explain the lower number of fish in this estuary in winter. The Trophic Contribution Factor is a useful tool for characterizing the input of basic elements to the trophic network, monitoring how the occupancy status of species affects their time-space variations, and comparing different localities and ecosystems.
Key words: Trophic structure, trophic contribution factor, fishes, estuary, mangrove
INTRODUCTION invertebrates. In New Caledonia, THOLLOT (1996) found that detritus-eating species dominate over Excluding the effects of population macro-carnivorous and herbivorous species, movements and variations in abundance, fish a situation also noted by FLORES-VERDUGO et species respond to the abiotic cycle in their al. (1990) in Mexico. A great many estuary fish environment with strikingly constant feeding species are remarkably adaptable (BOUCHEREAU habits. This fact has often been noted in the et al., 1991; BOUCHEREAU, 1994; BOUCHEREAU & ecosystems of mangrove estuaries (KENNISH, GUELORGET, 1998) and opportunistic (ALBARET, 1990; THOLLOT, 1996). In West Africa, LONGHURST 1994) in their feeding habits. So how important (1957) observed a large number of piscivorous are crabs, polychaetes, gastropods and other species feeding on epifaunal and endofaunal invertebrate detritus-eaters in relation to 84 ACTA ADRIATICA, 45(1): 83-94, 2004
Fig. 1. The Bay of Guaratuba, southern Brazil (in circle in the inset), and the extent of the mangrove
plankton and plants in the diet of fish in a 1998; CHAVES & SERENATO, 1998; VENDEL & mangrove estuary? Do resident species, migrants CHAVES, 1998), evidently due to the availability and occasional visitors avail themselves of of different categories of prey as a result of different sources? The aim of this study was abiotic changes in the estuary. to characterize the trophic organization of the In this study, the trophic organization is permanent and temporary fish populations in analyzed according to level and feeding habits the Bay of Guaratuba, Brazil. of the fish populations, based on whether the The Bay of Guaratuba, southern Brazil species is resident, migrant or occasionally (25°52’S; 48°39’W; Fig. 1), is surrounded by visits the bay. a mangrove ecosystem fed by several medium- sized rivers from the surrounding mountains. The estuaries are subject to the abiotic variations MATERIAL AND METHODS common to subtropical paralic environments and the ichthyofauna organization is more A quantitative inventory of the ichthyofauna affected by the rainfall on the catchment in Guaratuba Bay (CHAVES & BOUCHEREAU, area than by temperature (CHAVES et al., 2000). 1999) was made during monthly bottom Several ichthyological studies were carried trawling operations from 1993 to 1996. Sixty- out in Guaratuba to create a database for fish- one species were recorded. Information on the farming and fish management. They deal with diet of 57 of them can be found in the literature. reproductive activity (CHAVES & BOUCHEREAU, The 57 species can be divided into six groups 2000) and variations in population numbers according to the trophic source consumed, based (CHAVES & BOUCHEREAU, 1999), showing that on an adaptation of the scale used by BOUCHON- most of the fish populations do not permanently NAVARO et al. (1992) for West Indian plant bed live in the bay, but only spend an eco-stage in fish. The six categories are: (I) herbivores that their life cycle there or enter it sporadically. consume algae and higher plants; in the case of CHAVES & PICHLER (2000) reported that the grey mullet, a fairly high amount of detritus was trophic activity of fish populations in Guaratuba found in the stomach; (II) plankton-eaters; (III) is more intense in the innermost part of the bay omnivores that consume invertebrates of all than elsewhere. This activity peaked in autumn sizes and plants; (IV) first-order carnivores that and some species changed their diet by targeting consume mostly small benthic invertebrates; other kinds of prey (CHAVES & VENDEL, 1996, (V) second-order carnivores that consume CHAVES & BOUCHEREAU: Trophic organisation of fish populations in the Bay of Guaratuba, Brazil 85
Table 1. Random values attributed to the factor of trophic usage of the initial energy source in detritus and primary production by each trophic category
Trophic category Examples of prey composition Detritus Primary production Herbivores Leaves, seeds, plant debris, aquatic plants 2 2 Plankton-eaters Phytoplankton and zooplankton 0 2 Omnivores Polychaetes, mollusks, crustaceans, aquatic plants 2 2 First-order carnivores Polychaetes, mollusks, crustaceans 2 1 Second-order carnivores Polychaetes, mollusks, crustaceans, fish 1 0 Fish-eaters Fish 0 0 mainly invertebrates of all sizes and fish; and Contribution Factor (TCF). The TCF for the (VI) carnivores that consume over 80% fish. source in detritus (s = d) or primary production We estimated the proportion of species that (s = pp) combines biomass or species richness belongs to each category and the proportion for each trophic category and a usage factor according to occupancy status (resident, for the initial source of energy (d or pp) used migrant or occasional; QUIGNARD, 1984) which by each trophic category. The TCF can be was possible for most of the inventoried species calculated according to season or occupancy (CHAVES et al., 2000; VENDEL & CHAVES, 2001; status and is calculated as: BOUCHEREAU & CHAVES, 2002). In addition, for Σ the 14 species representing 75% of the total TCFsi= 100 . cI→cVI (Ai,c . Fc) / Σ Σ biomass over the study period, we studied i1→in cI→cVI(Ai,c . Fc) the availability of trophic sources in terms where i is the season (summer is January- of relative biomass by season and occupancy March) or occupancy variable (r for resident, m status. Finally, to compare seasons and for migrant, o for occasional), n is the number occupancy status, we quantified the relative of units in the variable (i.e., 4 for season and amounts of detritus (d) and primary production 3 for occupancy status), A is the abundance (pp) used as initial sources (s) of energy in (density or species richness) in the trophic each trophic category (c) by devising a Trophic category (c), and F is the factor of trophic
Table 2. TCF calculation for detritus according to occupancy status; A: hypothetic biomass in each trophic category; F: Factor of trophic usage.
Trophic category F value for detritus* Resident Migrant Occasional AAFA AF AAF Herbivores 2 8 16 6 12 4 8 Plankton-eaters 0 6 0 5 0 8 0 Omnivores 2 4 8 1 2 10 20 First-order carnivores 2 7 14 4 8 8 16 Second-order carnivores 1 5 5 2 2 10 10 Fish-eaters 0 9 0 2 0 8 0 Total 43 24 54 % of total 35.6 19.8 44.6 * From Table 1 86 ACTA ADRIATICA, 45(1): 83-94, 2004 usage in each trophic category of the studied source (s), i.e., detritus or primary production. We randomly attributed the values 0, 1 or 2 (Table 1) to the degree of direct contribution of the initial energy source for a trophic category. When members of a category have a very close trophic link to detritus or primary production, the value attributed to F is 2. Conversely, when fish in a category make no direct use of detritus or primary production, the F value is zero. F Fig. 2. Relative biomass of the 14 most abundant equals 1 when then a contribution exists but is species in the Bay of Guaratuba, according to partial. trophic category TCF values range 0-100. As a theoretical example, we propose that the TCF calculation (omnivores, first and second-order carnivores; for comparing the three occupancy statuses Table 3). Second-order carnivores is the largest according to exploitation of detritus be as category (38.6%). The second most numerous shown in Table 2. A similar calculation can be categories are omnivores (24.6%) and first-order made for primary production. carnivores (19.3%). Only 14% of the species are plankton-eaters (7%) or fish-eaters (7%) and herbivores are the least common (3.5%). Also RESULTS amongst the 14 species that constitute 75% Proportion of trophic categories of the inventoried ichthyofauna abundance, omnivores, first-order and second-order The 57 species for which dietary habits carnivores are most common, followed by fish- are known feed mainly on invertebrates with eaters (Fig. 2). Herbivores and plankton-eaters or without supplemental plant matter or fish are not found in the group of 14.
Table 3. Classification of species for which dietary habits are known into trophic categories. The first 14 constitute 75% of the biomass in the bay, according to samples taken by a benthic trawler
TROPHIC SPECIES STATUS REFERENCE ECOSYSTEM CATEGORY Stellifer rastrifer Resident Menezes and Figueiredo, 1980 Unspecified First-order carnivore Chaves and Vendel, 1998 Guaratuba First-order carnivore Pomadasys covinaeformis Migrant Menezes and Figueiredo, 1980 Unspecified Omnivore Costa et al., 1995 North Brazil Omnivore Chaves and Corrêa, 2000 Guaratuba Omnivore Bairdiella ronchus Resident Menezes and Figueiredo, 1980 Unspecified Omnivore Garcia and Nieto, 1978 Cuba Omnivore Vendel and Chaves, 1998 Guaratuba Second-order carnivore Genidens genidens Resident Chaves and Vendel, 1996 Guaratuba Second-order carnivore Diapterus rhombeus Migrant Menezes and Figueiredo, 1980 Unspecified Omnivore Santos and Araujo, 1997 East Brazil Omnivore Chaves and Otto, 1998 Guaratuba Omnivore Cynoscion leiarchus Migrant Menezes and Figueiredo, 1980 Unspecified Carnivore Chaves and Umbria, 2003 Guaratuba Carnivore Isopisthus parvipinnis Migrant Menezes and Figueiredo, 1980 Unspecified Carnivore Chaves and Umbria, 2003 Guaratuba Carnivore Citharichthys arenaceus Resident Chaves and Serenato, 1998 Guaratuba Second-order carnivore CHAVES & BOUCHEREAU: Trophic organisation of fish populations in the Bay of Guaratuba, Brazil 87
Table 3. cont`d
Eucinostomus argenteus Migrant Menezes and Figueiredo, 1980 Unspecified Omnivore Chaves and Otto, 1999 Guaratuba Omnivore Micropogonias furnieri Migrant Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Chaves and Umbria, 2003 Guaratuba Second-order carnivore Eucinostomus gula Migrant Menezes and Figueiredo, 1980 Unspecified Omnivore Santos and Araujo, 1997 East Brazil Omnivore Chaves and Otto, 1999 Guaratuba Omnivore Chaetodipterus faber Migrant Menezes and Figueiredo, 1985 Unspecified First-order carnivore Hayse, 1990 South Caroline, Atl. First-order carnivore Menticirrhus americanus Migrant Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Chaves and Umbria, 2003 Guaratuba Second-order carnivore Diplectrum radiale Migrant Personal observation Guaratuba First-order carnivore Rhinobatos percellens Occasional Figueiredo, 1977 Unspecified First-order carnivore Gymnothorax ocellatus Occasional Randall, 1967 (G. moringa) West Indies Second-order carnivore Harengula clupeola Migrant Figueiredo and Menezes, 1978 Unspecified Plankton-eater Opisthonema oglinum Migrant Figueiredo and Menezes, 1978 Unspecified Second-order carnivore Pellona harroweri Migrant Figueiredo and Menezes, 1978 Unspecified Plankton-eater Cetengraulis edentulus Migrant Personal observation Guaratuba Plankton-eater Lycengraulis edentulus ?Figueiredo and Menezes, 1978 Unspecified Carnivore Cathorops spixii Migrant Figueiredo and Menezes, 1978 Unspecified First-order carnivore Netuma barba Migrant Figueiredo and Menezes, 1978 Unspecified First-order carnivore Sciadeichthys luniscutis Migrant Personal observation Guaratuba First-order carnivore Synodus foetens ?Figueiredo and Menezes, 1978 Unspecified Second-order carnivore Hippocampus reidi ? Personal observation Guaratuba Omnivore Prionotus punctatus ?Figueiredo and Menezes, 1980 Unspecified Second-order carnivore Dactylopterus volitans ?Figueiredo and Menezes, 1980 Unspecified Second-order carnivore Centropomus parallelus Migrant Figueiredo and Menezes, 1980 Unspecified Second-order carnivore C. undecimalis Migrant Figueiredo and Menezes, 1980 Unspecified Second-order carnivore Epinephelus itajara Occasional Figueiredo and Menezes, 1980 Unspecified Second-order carnivore E. niveatus Occasional Personal observation Unspecified Second-order carnivore Rypticus randalli ? Randall, 1967 Puerto Rico Second-order carnivore Pomatomus saltator ? Juanes et al., 1993 South Africa Second-order carnivore Caranx hippos ? Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Sierra et al., 1994 Cuba Second-order carnivore C. latus ? Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Sierra et al., 1994 Cuba Second-order carnivore Chloroscombrus chrysurus Migrant Menezes and Figueiredo, 1980 Unspecified Plankton-eater Selene vomer Migrant Personal observation Guaratuba First-order carnivore Trachinotus carolinus ? Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Eucinostomus Migrant Chaves and Otto, 1999 Guaratuba Omnivore melanopterus Genyatremus luteus ? Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Archosargus rhomboidalis ? Menezes and Figueiredo, 1980 Unspecified Omnivore Cynoscion acoupa Occasional Menezes and Figueiredo, 1980 Unspecified Second-order carnivore Larimus breviceps Occasional Menezes and Figueiredo, 1980 Unspecified Omnivore Lopes and Silva, 1999 North Brazil Omnivore 88 ACTA ADRIATICA, 45(1): 83-94, 2004
Table 3. cont`d
Menticirrhus littoralis Occasional Menezes and Figueiredo, 1980 Unspecified Omnivore Lunardon, 1990 East Brazil Omnivore Paralonchurus brasiliensis Migrant Menezes and Figueiredo, 1980 Unspecified First-order carnivore Mugil curema Migrant Albaret and Legendre, 1985 Ivory Coast Herbivore M. gaimardianus Migrant Personal observation Guaratuba Herbivore Bathigobius soporator Resident Sano et al., 1984 (B. fuscus) Okinawa Islands Omnivore Trichiurus lepturus Occasional Figueiredo and Menezes, 2000 Unspecified Carnivore Citharichthys spilopterus Resident Chaves and Serenato, 1998 Guaratuba First-order carnivore Etropus crossotus Resident Chaves and Serenato, 1998 Guaratuba Omnivore Symphurus tessellatus Resident Chaves and Serenato, 1998 Guaratuba Second-order carnivore Achirus lineatus Resident Chaves and Serenato, 1998 Guaratuba First-order carnivore Chylomicterus spinosus Resident Personal observation Guaratuba Omnivore Lagocephalus laevigatus Resident Personal observation Guaratuba Omnivore Sphœroides testudineus Resident Personal observation Guaratuba Omnivore
Trophic and occupancy habits No occasional visitors were found among the 14 most abundant species. Amongst the resident We estimate that 12 of the 57 inventoried species (which correspond to 51% of the biomass species are residents of the bay whereas 25 are of the 14 most abundant species), nearly half the migrants, 8 occasional visitors and 12 unknown. biomass consumes an exclusively invertebrate For the 45 species whose occupancy is known, diet, while the other half feeds on invertebrates invertebrates dominate the diet as all resident plus fish (Fig. 4). Of the migrants (49% of the and most migrant and occasional species biomass of the 14 most abundant species), 60% of the biomass feed on invertebrates plus algae are omnivores, first-order or second-order and higher plants. Fish capture reaches a fairly carnivores (Fig. 3). Herbivores and plankton- highly level, given that fish-eaters account for eaters were only found in migrant species. 20% of the total abundance in this category and Piscivores, absent among residents, were more second-order carnivores for 10%. Further, the common in occasional visitors than in migrants percentage of exclusively invertebrate diets in (Fig. 3). migrant species is very low (10%) compared to that of residents (45%).
Fig. 3. Distribution (%) of the 45 species in the Bay of Fig. 4. Distribution (%) of biomass of the 14 most Guaratuba, according to occupancy status (resident, abundant species in the Bay of Guaratuba, migrant, occasional visitor) and trophic category according to trophic category CHAVES & BOUCHEREAU: Trophic organisation of fish populations in the Bay of Guaratuba, Brazil 89
Seasonal variation in migrants, they increase from a minimum (TCFd = 8.4; TCFpp = 7.6) in summer to a Omnivores, first-order and second-order maximum (TCFd = 44.0; TCFpp = 43.1) in carnivores make up 80% of the biomass of winter. For the 45 species whose occupancy the 14 most abundant species in winter. In status is known and regardless of their relative other seasons, they make up 91-97% (Fig. abundance, the detritus TCF is greater than the 5). Omnivores represent 36% and 39% of the primary production TCF for residents (d = 34.5; biomass in winter and spring, respectively, pp = 28.3) and occasional visitors (d = 17.2; pp while only 11% and 20.7% in summer and = 10.9), while the opposite holds for migrants autumn, respectively. The biomass of first- (d = 48.3; pp = 60.9). order carnivores varies widely depending on the season. It is greater in autumn (54.5%) than during the rest of the year (8.9% in winter, 28.1% in summer).
Fig. 5. Seasonal distribution (%) of biomass of the 14 most abundant species in the Bay of Guaratuba, classified by trophic category Fig. 6. Seasonal TCF values of detritus and primary pro- duction for the 14 most abundant species in the Bay of Guaratuba
Trophic Contribution Factor For each season, the TCF values for detritus and primary production of the 14 most abundant species do not significantly differ from each other (Χ2 = 0.05; Fig. 6). Both are lowest in summer (TCFd = 17.1; TCFpp = 11.2) and highest in winter (TCFd = 30.3; TCFpp = 33.8). There are also no significant differences (Χ2 = 0.05) between TCF detritus and primary production in any season for resident (Fig. 7) and migrant species (Fig. 8) when each occupancy status is examined separately. However, the seasonal trends of detritus and primary production TCF differ according to occupancy status. In resident species, they reach a maximum (TCFd Fig. 7. Seasonal distribution of TCF values of detritus and = 33.0; TCFpp = 47.0) in autumn and minimum primary production in resident species in the 14 most (TCFd = 18.0; TCFpp = 8.6) in winter, while abundant species in the Bay of Guaratuba 90 ACTA ADRIATICA, 45(1): 83-94, 2004
continental waters rich in nutritious salts just after the rainy season. It was also in autumn that this situation was noted in Guaratuba by CHAVES et al. (2000). Resident species hold a pivotal position in the trophic network because they are fodder (food web) species in the “energy reactor” and constitute part of the wealth of this type of semi-closed aquatic ecosystem. Migrants are found in all trophic categories. As they live in the bay during only one eco-stage of their life cycle, they time their presence with the estuary’s seasonal productivity, particularly of the plants consumed by herbivores and plankton-eaters. At the end of the migrants’ food chain, there are fish-eaters that feed not only on Fig. 8. Seasonal distribution of TCF values of detritus and primary production in migrant species in the 14 fodder species but also on other migrants and most abundant species in the Bay of Guaratuba occasional visitors. In occasional visitors, species are present irregularly throughout the year and are most DISCUSSION often carnivores and fish-eaters. THOLLOT (1996) showed that, in the New Caledonian The dominance of general-diet species mangrove, fish-eaters are more common with strong carnivorous tendencies (especially amongst occasional visitors than among invertebrates) over herbivorous or piscivorous migrants and even more than among residents. species agrees with the findings of studies They are usually large individuals that wander of other estuary ecosystems (KENNISH, 1990). passively into the bay (BOUCHEREAU et al., 2000) However, the samples in our study did not or enter the bay to take advantage of the food involve larval, post-larval and juvenile stages, supply (CHAVES et al., 1998). Could the relative or fish living in shoreline vegetation zones wintertime increase in fish-eating predators liable to flooding, which might have restricted observed in this study explain the decrease in the scope of our analysis. fish numbers in winter, observed by CHAVES Information on the trophic habits of & BOUCHEREAU (1999), just after their peak in species with regard to their kind of occupancy autumn? illustrates the functional dynamics of the estuary Bay occupancy habits become very clear environment, which provides a very hospitable after determining the seasonal changes in habitat for fishes since all the trophic categories detritus and primary production sources among are found there. resident and migrant species. THOLLOT (1996), Resident species, which feed year-round DIOUF (1996) and others have already noted mainly on a diet of invertebrate benthic the important part played by detritus in the meiofauna and macrofauna, profit more trophic network of resident species. Seasonal from the supply of detritus than the supply changes in the biomass of invertebrate eaters of primary production. Their preference for are closely related to those of detritus and primary production in autumn may be due to primary production contribution for residents. the increase in photosynthetic activity at this In migrants, the same applies to the biomass time of the year. YÁÑEZ-ARANCÍBIA et al. (1993) of invertebrates and plant eaters, which are and DUFOUR et al. (1994) noted an increase in related to detritus and primary production. We the phytoplankton biomass in several estuaries therefore conclude that these two groups of when clear waters of marine origin blend with fish avail themselves of different trophic ranges CHAVES & BOUCHEREAU: Trophic organisation of fish populations in the Bay of Guaratuba, Brazil 91 depending on whether the source is available and functioning in fish populations. However, permanently or seasonally. in a TCF comparison, we may receive varying In this study, the TCF was used to results for a given location or ecological status, characterize the contribution of the basic owing to different values assigned to abundance elements in the trophic network – detritus and (factor A) and use (factor F) in the formula. primary production – and examine them in This should be taken into consideration when interpreting TCF results. Another advantage relation to season and occupancy status of the of TCF is that the diet, if already known, can fish species. TCF can also be used to compare be used to quickly quantify the contribution of locations within an ecosystem or between energy sources in the environment consumed by ecosystems, using the variable i as a location in fish populations. the above formula. Likewise, vertical occupancy (pelagic, demersal or benthic) can be examined. ACKNOWLEDGEMENTS TCF can also be used to examine changes in diet due to the age of the fish, whose biomass This study was carried out in the framework in each trophic category can be determined. of agreements 5397 CNRS-CNPq and 376/ These examples show how versatile TCF is for 02 CAPES-COFECUB between France and analyzing and interpreting trophic organization Brazil.
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FIGUEIREDO, J.L. & N.A. MENEZES. 2000. Manual Universidade de São Paulo, São Paulo, pp. de Peixes Marinhos do Sudeste do Brasil. 96. VI. Teleostei (5). Museu de Zoologia, MENEZES, N.A. & J.L. FIGUEIREDO. 1985. Manual Universidade de São Paulo, São Paulo, pp. de Peixes Marinhos do Sudeste do Brasil. 116. V. Teleostei (4). Museu de Zoologia, FLORES-VERDUGO, F., F. GONZALEZ-FARIAS, O. Universidade de São Paulo, São Paulo, pp. RAMIREZ-FLORES, F. AMEZCUA-LINARES, 105 . A. YÁÑEZ-ARANCIBIA, M. ALVAREZ-RUBIO & J.W. DAY, JR. 1990. Mangrove ecology, QUIGNARD, J.-P. 1984. The biological and aquatic productivity, and fish community environmental characteristics of lagoons as dynamics in the Teacapan-Agua Brava the biological basis of fisheries management. Laggon-Estuarine System (Mexican In: Management of coastal lagoon fisheries Pacific). Estuaries, 13: 219-230. Kapetsky and Lasserre (Editors), Studies and Reviews FAO, 61 (1): 3-38. GARCIA, T. & E. NIETO. 1978. Alimentation de Bairdiella ronchus (Cuvier) (Pisces: RANDALL, J.E. 1967. Food habits of reef fishes Sciaenidae) en dos areas de la plataforma of the West Indies. Stud. Trop. Ocean. cubana. Ciencias. Investigaciones Marinas, Miami: 5, 665-847. Universidad de la Habana, 8 (38): 11-28. SANO, M., M. SHIMIZU & Y. NOSE. 1984. Food HAYSE, J.W. 1990. Feeding habits, age, growth, habits of teleostean reef fishes in Okinawa and reproduction of Atlantic spadefish Island, southern Japan. University of Tokyo Chaetodipterus faber (Pisces: Ephippidae) Press, Tokyo, Japan, 128 pp. in South Carolina. Fish. Bull., 88 (1): 67- SANTOS, A.C. & F.G. ARAUJO. 1997. Hábitos 83. alimentares de três espécies de Gerreidae JUANES, F., R.E. MARKS, K.A. McKOWN & D.O. (Osteichthyes, Perciformes) na Baía de CONOVER. 1993. Predation by age-0 bluefish Sepetiba, RJ. Arq. Biol. Tecnol., 40 (2): on age-0 anadromous fishes in the Hudson 359-368. River estuary. Trans. Am. Fish. Soc., 122 SIERRA, L.M., R. CLARO & O.A. POPOVA. 1994. (3): 348-356. Alimentacion y relaciones tróficas. In: KENNISH, M.J. 1990. Ecology of Estuaries. Vol. Rodolfo Claro (Editor). Ecología de los II. Biological Aspects. CRC Press, Boca Peces Marinos de Cuba. Instituto de Raton, Florida, 391 pp. Oceanología Academia de Ciencias de Cuba LONGHURST, A.R. 1957. The food of the demersal and Centro de Investigaciones de Quintana fish of a West African estuary. J. An. Ecol., Roo, Mexico, pp. 263-284. 26: 369-387. THOLLOT, P. 1996. Les poissons de mangrove LOPES, P.R.D. & J.T.O. SILVA. 1999. Nota sobre a du lagon sud-ouest de Nouvelle-Calédonie. alimentação de Larimus breviceps (Cuvier, Orstom, Collection Études et Thèses, Paris, 1830) (Actinopterygii: Sciaenidae) na 321 pp. Praia de Jaguaribe (Ilha de Itamaracá), VENDEL, A.L. & P.T.C. CHAVES. 1998. Alimentação Pernambuco. Acta Biol. Leopold., 21 (1): de Bairdiella ronchus (Cuvier) (Teleostei, 161-168. Sciaenidae) na Baía de Guaratuba, Paraná, LUNARDON, M.J. 1990. Hábitos alimentares de Brasil. Revta Bras. Zool., 15 (2): 297-305. Menticirrhus littoralis (Holbrook, 1860) VENDEL, A.L. & P.T.C. CHAVES. 2001. Baia de (Perciformes -Sciaenidae) na Baía de Guaratuba, Parana: um estudo de caso Paranaguá e adjacências - Paraná - Brasil. sobre ictiofauna em estuarios. In: Reuniao Arq. Biol. Tecnol., 33 (3): 717-725. Técnica sobre Ictiologia em Estuarios. MENEZES, N.A. & J.L. FIGUEIREDO. 1980. Manual P.T.C. Chaves, A.L. Vendel (Editors). de Peixes Marinhos do Sudeste do Brasil. Universidade Federal do Parana, Curitiba, IV. Teleostei (3). Museu de Zoologia, pp. 91-102. 94 ACTA ADRIATICA, 45(1): 83-94, 2004
YÁÑEZ-ARANCÍBIA, A., A.L. LARA-DOMINGUEZ by estuarine nekton assemblages: coupling & J.W. DAY JR.1993. Interactions between of primary and secondary production. mangrove and seagrass habitats mediated Hydrobiol., 264: 1-12.
Received: 11 April 2003 Accepted: 1 March 2004
Trofička organizacija i funkcioniranje riblje populacije u zaljevu Guaratuba, Brazil, na osnovi doprinosa trofičkog faktora
Paulo CHAVES1 i Jean-Luc BOUCHEREAU2
1Zoološki odsjek, Federalno Sveučilište Paraná, P.P. 19020, 81531-990, Curitiba, Brazil E-mail:[email protected] 2Laboratiorij za biologiju mora, E.A. 926, Sveučilište Antili - Gvajana, P.P. 592, F-97159, Pointe-à-Pitre cedex, Francuska E-mail: [email protected]
SAŽETAK
U zaljevu Guaratuba je određen trofički sustav i njegov sezonski razvoj. U obzir su uzeti podaci o prehrambenim navikama iz literature kao i jedan faktor koji sjedinjuje biomasu i bogatstvo vrsta kako bi se mogao odrediti doprinos detritusa i primarne proizvodnje u trofičkom lancu. Zaljev ima, s obzirom na ishranu, sve kategorije riba: herbivore, planktonofage, potrošače beskralježnjaka (nadopunom s biljem i ribom), te one koje se hrane ribom. Ribe koje su stalno nastanjene u zaljevu, te migratorne ribe zauzimaju različite trofičke nivoe, ovisno da li su izvori hrane pristupačni stalno ili samo u određenoj sezoni. Stalne vrste se hrane pretežito bentoskim beskralježnjacima (meio - i makrofaunom) te koriste više detritus negoli izvore primarne proizvodnje. Prisustvo migratornih riba ovisno je naročito o sezonskoj biljnoj proizvodnji. Većina povremenih posjetitelja hrani se beskralježnjacima i ribom ili uglavnom ribom. Prisustvo ihtiofaga moglo bi objasniti manje količine ribe zimi u tom zaljevu. Faktor trofičke kontribucije može korisno poslužiti kao prikaz ulaska osnovnih elemenata u prehrambeni lanac i razumijevanju kako zastupljenost vrste utječe na vremensko-prostorne varijacije, te omogućava usporedbu različitih lokaliteta i ekosistema.
Ključne riječi: Trofička struktura, trofički faktor kontribucije, ribe, ušće, mangrove ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.32: 591.16(262) AADRAY 45 (1): 95-106, 2004 Original scientific paper
Reproductive biology of the Bluntnose sixgill shark Hexanchus griseus (Bonnaterre, 1788) (Chondrichthyes: Hexanchidae) from the Mediterranean Sea: a review
Christian CAPAPÉ 1, Farid HEMIDA 2, Olivier GUÉLORGET 1, Joan BARRULL3, Isabel MATE 3, Jamila BEN SOUISSI 4 and Mohamed Nejmeddine BRADAÏ 5
1 Laboratoire d’Ichtyologie, case 104, Université Montpellier II, Sciences et Techniques du Languedoc, 34095Montpellier Cedex 05, France E-mail: [email protected] 2 Laboratoire Halieutique, Institut des Sciences de la Nature, Université des Sciences et Techniques Houari Boumedienne, B.P. 32, El Alia, 16111 Bab Ezzouar, Algiers, Algeria 3Laboratorio Vertebrats, Seccio Ictiologia, Museu de Zoologia, Apartat de Correus 593, 08080 Barcelona, Spain 4 Département des Ressources Animales, Halieutiques et des Technologies Alimentaires, Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, Cité Mahrajène, 1082 Tunis, Tunisie E-mail: [email protected] 5 Institut National des Sciences et Technologies de la Mer, Centre de Sfax, B.P. 1035, 3018 Sfax, Tunisia E-mail: [email protected]
Adult bluntnose sixgill shark (Hexanchus griseus) males and females from the Mediterranean were over 3000 mm TL and 3940 mm. Size at birth was 556-680 mm TL. Ripe oocytes ranged between 68 and 75 mm TL (mean 71.71±2.6) in diameter and 127-147 g (mean 134±8.4) in weight. The reproductive cycle lasted at least one year, but probably more. The chemical balance of development (dry weight of newborn pup/dry weight of ripe oocyte) was 3. One adult female contained 57 ripe oocytes; a second contained 100. Hexanchus griseus is probably able to live and reproduce in the Mediterranean Sea, however, further observations are needed to confirm that a sustainable bluntnose sixgill shark population has been established here, especially off the Maghrebin coast.
Key words: Chondrichthyes, Hexanchidae, Hexanchus griseus, reproductive biology, Mediterranean Sea, Maghrebin shore
INTRODUCTION Atlantic coasts, and in the Mediterranean Sea (BASS et al., 1975). A historical survey of The bluntnose sixgill shark Hexanchus Mediterranean reports since 1892 showed that griseus is widely distributed in temperate and H. griseus has been captured in restricted areas, tropical waters. It can be found in the Pacific more commonly in the western than in the and Indian Oceans, off the eastern and western eastern basin (CAPAPÉ et al., 2003a). 96 ACTA ADRIATICA, 45(1): 95-106, 2004
Fig. 1. Mediterranean fishing sites (*) where Hexanchus griseus in our samples were captured
The biology of H. griseus in the shore (the Algerian and Tunisian coasts). It Mediterranean is poorly known and there is comprises 167 Mediterranean bluntnose sixgill little published information that deals with shark records (Fig. 1). ichthyological treatises (CAPAPÉ et al., 2003a). Fifty-nine specimens were from the Review of records of specimens collected from northern coast including six caught off France, the coasts of France, Spain, Italy, Malta, Algeria 32 off Spain, 20 in the Italian Seas and one off and Tunisia provide the opportunity to increase Malta. Ten specimens, captured by trawling our current knowledge on the reproductive and longlines between 1976 and 2002, were biology of the Mediterranean H. griseus and recorded off the southern Mediterranean coast compare it with H. griseus in other marine areas near Tunisia. Another 98 specimens were (VAILLANT, 1901; DESBROSSES, 1938; BIGELOW & captured between 1996 and 2002 by longlines SCHROEDER, 1948; EBERT, 1986a,b, 1990, 1996, 2002). at a depth of 30-700 m off the Algerian coast (Fig. 2). Unfortunately, they were eviscerated MATERIALS AND METHODS by fishermen when landed on the boat deck. Our paper is based on a literature review The specimens caught off Sète (France) and observations conducted off the Maghrebin and the Maghrebin shore were measured to
Fig. 2. The Maghrebin shore (redrawn from Capapé et al., 2003), showing where one or more Hexanchus griseus were cap- tured. Squares - off the Algerian coast; stars - off the Tunisian coast; A - eastern area; B - central area; C - western area; BE - Bank of Esquerquis; GG - Gulf of Gabès CAPAPÉ, HEMIDA, GUÉLORGET, BARRULL, MATE, BEN SOUISSI & BRADAÏ: Biology of H. griseus 97 the nearest millimeter for total length (TL) chemical balance of development (CBD) was following BASS et al. (1975; STEVENS & LYLE calculated according to CBD = mean dry weight (1989) and weighed to the nearest gram. The of newborn pups/ mean dry weight of fertilized clasper (Fig. 3) was measured following eggs or ripe oocytes. Standard values for water COLLENOT (1969). content are 50% in ripe oocytes and 75% in new Morphological structures of bluntnose born pups, based on chemical analyses of the sixgill shark claspers were compared with those small spotted catshark, Scyliorhinus canicula by MELLINGER & WRISEZ (1989). CBD is a tentative estimate. The relationships between eviscerated weight or total weight and total length were studied. The linear regression was expressed in decimal logarithmic coordinates. Correlations were assessed by least-squares regression. Comparisons of curves were made by ANCOVA.
RESULTS
Onset of sexual maturity in males
The following observations were made on males captured off France, Tunisia and Algeria. During the juvenile stage, the males had short Fig. 3. Clasper of a Hexanchus griseus caught off the flexible claspers and the testes and genital duct Algerian coast (photo F. Hemida) were membranous and undeveloped. At the beginning of maturation, the claspers became of closely related species such as the sharpnose elongated and rigid and the testes increased sevengill shark Heptranchias perlo studied by in size. In adults, the clasper sheath was TANAKA et al. (1975), CAPAPÉ (1980) and FRENTZEL- very developed and a mucus substance was BEYNE & KÖSTER (2002) and the sevengill shark elaborated at the clasper tip, which transferred Notorynchus cepedianus by EBERT (1986b). into a pocket or expansion of the clasper. The Onset of sexual maturity in males was determined by the relationship between clasper length (CL, mm) and TL following BASS et al. (1975) and STEVENS & LYLE (1989) who noted that claspers of juveniles are short and flexible and adult claspers are rigid, elongated and calcified. In addition, aspects of the testes and the genital organs were examined. The size of females at sexual maturity was determined by the condition of the ovaries and the morphology of the reproductive tract. Males and females were classified into two categories, juveniles and adults. To investigate embryonic development Fig. 4. Clasper-length (CL) vs total length (TL) in and the role of the female during gestation, a Hexanchus griseus from the Mediterranean Sea 98 ACTA ADRIATICA, 45(1): 95-106, 2004 mucus contained spermatozoa. The testes were caught off Sète (France), 625 and 603 mm TL developed, and spermatocysts were visible. and 860 and 785 g (CAPAPÉ et al., 2000b), had The genital duct was conspicuously developed unhealed scars on the ventral surface and a and the ductus deferens (sensu HAMLETT et al., residual vitellin vesicle; they probably were 1999) was clearly twisted. The clasper length vs neonates. Of the 35 specimens from Spain, one total length is plotted in Fig. 4. Together with caught off Marbella was 556 mm TL (LOZANO the above observations, we suggest that males REY, 1928) and another caught off Barcelona reached adulthood at 3000 mm TL. Forty-four was 560 mm TL (BARRULL & MATE, 2000). Their specimens were juveniles and seven were sizes suggest they also were neonates. adults. Onset of sexual maturity in females Weight-total length relationships Juvenile females had whitish ovaries with For specimens from the Algerian coast, microscopic oocytes and inconspicuous oviducal eviscerated weight vs total length (Fig. 5) was glands. The smallest juvenile was a newborn log EW = 2.98 log TL - 5.25, r = 0.99 for males pup. Females entering the maturation stage had (n = 9) and log EW = 3.137 log TL - 5.879, translucent oocytes and a differentiated genital r = 0.98 for females (n = 20). There were no duct. They were 3000-3500 mm TL. The smallest significant differences in intercept or slope adult female was caught in Tunisian waters. It between the sexes (p>0.05). was less than 3000 mm and contained developing Total weight (TW) vs total length for males oocytes. A second female was 3940 mm TL and and females (n = 29) from the Mediterranean contained ripe oocytes. All females over 4000 coast was log TW = 3.13 log TL - 8.61, r = 0.95 mm TL were adult. Of the 117 observed females, (CAPAPÉ et al., 2003a). 95 were adult and 2 were juvenile. The heaviest specimen recorded in the Size and mass at birth Mediterranean was a male, 4000 mm TL, caught off Izmir, Turkey, which weighed 1000 Eight small free-swimming specimens, five kg (MATER et al., 2000). According to CAPAPÉ et al. off Spain and three off France, ranged 556-680 (2003a), this weight suggests an overestimation mm TL (CAPAPÉ et al., 2003a). Two specimens because larger specimens of 5000 mm TL,
Fig. 5. Eviscerated weight (EW) vs total length (TL) expressed in logarithmic co-ordinates for female and male Hexanchus griseus from the Algerian coast CAPAPÉ, HEMIDA, GUÉLORGET, BARRULL, MATE, BEN SOUISSI & BRADAÏ: Biology of H. griseus 99 recorded off Naples and Sardinia, did not exceed 2000; BRADAÏ & CAPAPÉ, 2001; CAPAPÉ et al., 2001a, 600 kg. These two specimens are the largest H. 2003a,b; ENNAJAR et al., 2002). griseus recorded to date. With regard to onset of sexual maturity, EBERT (1986a) recorded 4210 mm TL for a female from Female reproduction and fecundity the northeastern Pacific. In southern African waters, EBERT (2002) noted that “determination Three females with developing or ripe of maturity for females was problematic, but oocytes were captured in Tunisian waters. One, most were fully mature by at least 4200 mm caught off the northern coast, was 4650 mm TL TL”. Females were adult above 4500 mm TL and contained 57 fully yolked oocytes. Two in the Bay of Biscay (DESBROSSES, 1938), in females were caught in the Gulf of Gabès: one the western Atlantic (BIGELOW & SCHROEDER, (>3000 mm TL) contained many developing 1948) and off the Bahamas where SPRINGER oocytes but the exact number could not be & WALLER (1969) recorded an immature male determined since some probably spilled out at 3480 mm TL. EBERT (1986b) recorded the during capture and handling; the second (3940 capture of a mature male measuring 3250 mm mm TL) contained 100 fully yolked oocytes TL and 211 kg in the northern Gulf of Mexico. which were neither measured nor weighed. He noted, “development of its claspers and Two of the females were caught in April and clasper sac was similar to that of the sevengill probably were about to ovulate. Neonates were shark”. EBERT (2002) reported that males mature captured off France and Spain in November and at about 3100 mm TL in South African waters. April. Therefore, the reproductive cycle seems Our observations suggest that H. griseus to last at least one year. matures at a smaller size in the Mediterranean than elsewhere, in agreement with MORENO Chemical balance of development (1995), although the largest recorded specimens of H. griseus were from the Mediterranean Of the 57 yellow yolked oocytes counted (CAPAPÉ et al., 2003a). Female bluntnose sixgill in a female caught in Tunisian waters (4650 shark matured at a larger size than males in mm TL), 14 were measured and weighed. all areas, similar to other hexanchids such Their diameters ranged 68-75 mm TL (mean as sevengill sharks (Heptranchias perlo) off 71.71±2.6) and weights 127-147 g (mean northern Tunisia (CAPAPÉ, 1980) and in the 134±8.4). The smallest free-swimming female central eastern Atlantic (FRENTZEL-BEYME & specimens caught off France weighed 860 and KÖSTER, 2002) and Notorynchus cepedianus off 785 g (mean 822.5±53.03). Therefore, the CBD California (EBERT, 1986a,b, 2002) and southern was 3. Africa (EBERT, 1996). In the Bay of Biscay, VAILLANT (1901) DISCUSSION reported that TL ranged 680-736 mm for near- CAPAPÉ et al. (2003a) showed that H. griseus term embryos in a gravid female. DESBROSSES was relatively abundant in the Mediterranean (1938) reported that size at birth is less than Sea, and that the species is more abundant in 720 mm TL and recorded three near-term the western basin than in the eastern. They fetuses, ranging 650-680 mm TL. EBERT (1986a) suggested the abundance may be due to the noted that near-term embryos off the coast of development of fisheries in the area, especially California ranged 680-736 mm TL. EBERT along the Maghrebin shore, that began in (2002) recorded newborns in southern African 1996, about the same time as the beginning of waters ranging 610-930 mm TL and added research on elasmobranch species off Algeria that the smallest free-swimming specimen (HEMIDA, 1998; HEMIDA & LABIDI, 2001; HEMIDA was 610 mm TL. DESBROSSES (1938) recorded & CAPAPÉ, 2002, 2003; HEMIDA et al., 2002a,b; large variations in size at birth within an area, 2003b) and Tunisia (BRADAÏ, 2000; BRADAÏ et al., however, he collected both bluntnose sixgill 100 ACTA ADRIATICA, 45(1): 95-106, 2004 shark (H. griseus) and bigeyed sixgill shark (H. coast of Senegal (CAPAPÉ et al., 2000a, 2001b), nakamurai) in his sample and it was probably which are not strictly lecithotrophic (sensu the second species that was illustrated in his WOURMS, 1977, 1981). In contrast, the CBD article. BIGELOW & SCHROEDER (1948) reported reaches high values in strictly matrotrophic free-swimming specimens of 429-720 mm species. The CBD of C. limbatus (69) is the TL from the northwestern Atlantic but the highest value ever observed in an elasmobranch near-term embryo of 429 mm TL is probably species (unpubl. data) and is close to that of a bigeyed sixgill shark, whose TL at birth is the sympatric species C. brevipinna (65.8; about 430 mm (COMPAGNO, 1984). The gravid CAPAPÉ et al., 2003b) and higher than that of females reported by DESBROSSES (1938) ranged Mediterranean D. violacea, (47; HEMIDA et al., 4500-4650 mm TL and were H. griseus. The 2003), the butterfly ray Gymnura altavela from maximum TL reached by H. nakamurai is 1800 Tunisian waters (30.6; CAPAPÉ et al., 1992), and mm COMPAGNO (1984). the bull ray Pteromylaeus bovinus from the A literature review shows that H. griseus coast of Senegal (31.12; SECK et al., 2002). can reproduce once (RISSO, 1810; CANESTRINI, In elasmobranch species that produce 1861 in TORTONESE, 1956) or twice (NINNI, 1912) heavier eggs, the female’s role during gestation per year. Mediterranean neonates were caught is usually reduced. However in squatinids throughout the year (CAPAPÉ et al., 2003a). The and centrophorids, gestation is longer than two adult females with fully yolked oocytes one year (MELLINGER, 1989, 2002; CAPAPÉ et were caught in April, probably at the time of al., 1990; GUALLART & VINCENT, 2001). This ovulation. No embryos were found in the uteri. could confirm a long gestation period in No vitellogenetic activity was reported in gravid hexanchids, especially the bluntnose sixgill, in females bearing embryos in different stages of agreement with EBERT (1986a,b, 2002). In strictly development (EBERT, 1986b), suggesting that lecithotrophic species, the female protects only vitellogenic activity does not proceed together embryonic development, providing inorganic with embryonic development in H. griseus, nutrients to the embryos (MELLINGER, 1989; but this hypothesis requires confirmation by HAMLETT et al., 1998a,b). This was observed further observations. A similar pattern was not in squatinids (CAPAPÉ et al., 1990, 2002) and clearly observed in sevengills (CAPAPÉ, 1980; centrophorids (RANZI, 1932, 1934; GUALLART & EBERT, 1986b, 1989, 1996, 2002; FRENTZEL-BEYNE VICENT, 2001). In matrotrophic elasmobranchs, & KÖSTER, 2002). It appears that the reproductive the contribution of female-derived organic cycle in hexanchids is rather long and exceeds molecules is very important (WOURMS, 1981; one year. According to EBERT (1986b), for HAMLETT & WOURMS, 1984; HAMLETT et al. example, in N. cepedianus, “after first 1985a,b,c,d,e, 1993a,b, 2002; HAMLETT, 1987, 1989; parturition adult females would give birth every FISHELSON & BARANES, 1998). These species 18 to 24 months”. This is a possible hypothesis produce an egg mass that is clearly less than the for H. griseus as well. mass of fully developed embryos. Matrotrophy The CBD of 3 showed that H. griseus is is characteristic of dasyatids, rhinopterids and not a pure lecithotrophic species according gymnurids (WOURMS, 1977, 1981; MELLINGER, to the definition of WOURMS (1977, 1981) and 1989; CAPAPÉ et al., 1992; SECK et al., 2002). that the female’s role is not negligible during H. griseus may be a transition between gestation. In pure lecithotrophic species such as lecithotrophic and matrotrophic species and squatinids, the CBD is low (0.5-0.8; CAPAPÉ et considered a semi-lecithotrophic species. al., 1990, 2002). The CBD of H. griseus is higher In the Bay of Biscay, VAILLANT (1901) than the CBD (1.0) of the blackchin guitarfish numbered 108 near-term embryos in a female of Rhinobatos cemiculus from Tunisian waters 4800 mm TL. BOLIVAR (1907) found 47 fetuses (CAPAPÉ & ZAOUALI, 1994) and the torpedinids in a female of 4800 mm TL. Off California, a Torpedo torpedo and T. marmorata from the female of 4210 mm TL contained 51 near-term CAPAPÉ, HEMIDA, GUÉLORGET, BARRULL, MATE, BEN SOUISSI & BRADAÏ: Biology of H. griseus 101 embryos (EBERT, 1986a). One of the two females large TL and the lengthy reproductive cycle caught in Tunisian waters had 57 fully yolked considerably reduces recruitment. The wide oocytes; the other had 100. There is insufficient distribution suggests large migrations of H. data to state if ovarian fecundity is related to griseus. It is relatively common in the eastern female TL. EBERT (1986b) noted: “Therefore, tropical Atlantic (FISCHER et al., 1981) and its the actual number of young carried by this abundance off the Maghrebin shore may be due specimens was uncertain. The tendency of near- to migrations through the Strait of Gibraltar. term females to abort their young upon capture With regard to some elasmobranch and account for the wide discrepancy reported by teleost species, QUIGNARD & TOMASINI (2000) SPRINGER & WALLER (1969) for sixgill shark noted: “The discovery of a large number of fecundity”. N. cepedianus had 82-96 eggs per other species outside of their usual area of female and EBERT (1986b) found 82 near-term distribution may be due to an increase of embryos in a gravid female. Litter sizes were traditional prospection, or to the use of newer high in the sixgill and, like other hexanchid techniques which allow the exploration of species, can be considered a relatively prolific otherwise unaccessible habitat”. This agrees elasmobranch. Litters were lower than in the with GOLANI (1996), GOLANI & SONIN (1996) whale shark Rhyncodon typus where JOUNG et al. and HEMIDA et al. (2002b, 2003a) and must not be (1996) reported on 300 fully developed embryos in a “megamamma supreme”. ignored. Records regarding the Mediterranean reveal a non-negligible density population of sixgill ACKNOWLEDGEMENTS sharks (CAPAPÉ et al., 2003a). Stock decrease seems to be a possible hypothesis (DELATTRE The authors wish to thank two anonymous & MAIGRET, 1986). The species is relatively referees for their helpful and useful comments prolific but size at maturity is reached at a on the manuscript.
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Received: 27 January 2004 Accepted: 21 April 2004 106 ACTA ADRIATICA, 45(1): 95-106, 2004
Reprodukcija psa volonje šestoškrgaša Hexanchus griseus (Bonnaterre, 1788) (Chondrichthyes: Hexanchidae) u Mediteranu: pregled
Christian CAPAPÉ 1, Farid HEMIDA 2, Olivier GUÉLORGET 1 Joan BARRULL3, Isabel MATE 3, Jamila BEN SOUISSI 4 i Mohamed Nejmeddine BRADAÏ 5
1 Laboratorij za ihtiologiju, P.P. 104, Sveučilište u Montpellier-u II, Sveučilište znanosti i tehnike Languedoc-a, 34095 Montpellier Cedex 05, Francuska E-mail: [email protected]
2 Laboratorij za ribarstvo, Institut prirodnih znanosti, Sveučilište znanosti i tehnike Houari Boumedienne, P.P. 32, El Alia, 16111 Bab Ezzouar, Algiers, Alžir
3Laboratorij za biologiju kralježnjaka, Ihtiološki odsjek, Zoološki muzej, Apartat de Correus 593, 08080 Barcelona, Španjolska 4 Odjel za Životinjske resurse, ribarstvo i prehrambenu tehnologiju, Tuniski nacionalni isntitut za agronomiju, 43 Avenue Charles Nicolle, Cité Mahrajène, 1082 Tunis, Tunis E-mail: [email protected]
5 Nacionalni institut znanosti i tehnologije mora, Centar u Sfax-u, P.P. 1035, 3018 Sfax, Tunis E-mail: [email protected]
SAŽETAK
Ukupna duljina (TL) odraslih mužjaka psa volonje šestoškrgaša u Mediteranu iznosila je preko 3500 mm, dok je duljina ženki iznosila 3940 mm. Ukupna duljina (TL) novorođenih primjeraka kretala se između 556 i 680 mm. Promjer zrelih oocita kretao se između 68-75 mm, ukupna duljina (TL) iznosila je (71.71±2.6), dok je težina varirala od 127 do 147 g. (134±8.4). Reproduktivni ciklus je trajao minmalno godinu dana, a vjerojatno i dulje. Izračunata kemijska ravnoteža između srednje suhe težine oocita i novorođenih (CBD) iznosila je 3. Dvije odrasle ženke imale su 57 i 100 zrelih oocita. Podaci prikazani u ovom radu ukazuju na to da je Hexanchus griseus vjerojatno sposoban živjeti i razmnožavati se u Mediteranu. Međutim, neophodna su daljnja promatranja prije nego se konačno potvrdi da dostatna populacija psa šestoškrgaša volonje naseljava ovo područje, posebno priobalje Magreba.
Ključne riječi: Chondrichthyes, Hexanchidae, Hexanchus griseus, reprodukcija, Mediteran, obala Magreba ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.35: 591.9(262)(569.4) AADRAY 45 (1): 107-113, 2004 Short comunication
First records of the blue stingray, Dasyatis chrysonota (Smith, 1828) (Chondrichthyes: Dasyatidae), off the coast of Israel (eastern Mediterranean)
Daniel GOLANI1 and Christian CAPAPÉ2
1 Department of Evolution, Systematics and Ecology, The Hebrew University of Jerusalem, Jerusalem 91904, Israel
2 Laboratorie d’Ichthyologie, case 104 Université Montpellier II, Sciences and Techniques du Languedoc, 34095 Montpellier Cedex 05, France
Two blue stingrays, Dasyatis chrysonota (Smith, 1828), caught off the Mediterranean coast of Israel, are the first recorded for the Levant. The species was hitherto known in the Mediterranean Sea only in the Gulf of Gabès in southern Tunisia. The distribution of this western Atlantic species is discussed below.
Key words: Chondrichthyes, Dasyatidae, Dasyatis chrysonota, Mediterranean Sea, Southern Tunisia, Coast of Israel
INTRODUCTION In this paper, we describe two D. chrysonota specimens collected off the Mediterranean coast Two specimens of the blue stingray Dasyatis of Israel and comment on the distribution of the chrysonota (Smith, 1828) off the coast of Israel species in the area and in the Mediterranean are hereby reported for the first time. Prior to Sea. this record, four species of the genus Dasyatis were known in the eastern Levant: the common stingray Dasyatis pastinaca (Linnaeus, 1758), MATERIALS AND METHODS the roughtail stingray D. centroura (Mitchill, The first specimen was captured off the 1815), the pelagic stingray D. violacea Haifa-Nahariya coast (Fig. 1) on May 18, 1985, (Bonaparte, 1832) and the Tortonese stingray D. by a trawl on a sandy muddy substrate at 50 m. tortonesei Capapé, 1977. The common stingray It was a juvenile male, 150 mm disk length, 369 is the most abundant in the area (BEN-TUVIA, mm total length and 149 g in mass. The second 1971; GOLANI, 1996, 1997). Previous records of D. was captured on June 16, 1987, off Haifa by a chrysonota in the Mediterranean were reported trawl at an unknown depth. It was also a juvenile only in the Gulf of Gabès, southern Tunisia, male, 195 mm disk length, 445 mm total length central Mediterranean (Fig. 1) by MAURIN & and 445 g in mass. Both specimens are preserved BONNET (1970) and QUIGNARD & CAPAPÉ (1971). in alcohol in the ichthyological fish collection 108 ACTA ADRIATICA, 45(1): 107-113, 2004
Fig. 1. Map of the Mediterranean Sea showing the capture sites of Dasyatis chrysonota: 1. Gulf of Gabès in southern Tunisia. 2. Coast of Israel of the Hebrew University of Jerusalem. The follow COMPAGNO & ROBERTS (1984), COWLEY first specimen received catalogue number HUJ & COMPAGNO (1993) and CAPAPÉ et al. (2002). The 13768 and the second specimen, HUJ 12450 claspers were measured according to COLLENOT (Fig. 2). Measurements (Table 1) and counts (1969).
Fig. 2. Dasyatis chrysonota, 230 mm disc width (HUJ 12450), Haifa. Photo: Dr. David DAROM GOLANI & CAPAPÉ: First records of the blue stingray, D. chrysonota, off the coast of Israel 109
Table 1. Measurements (in mm) and proportional measurements expressed as a percent of disk width (% of DW) from the two Dasyatis chrysonota captured off the Mediterranean coast of Israel
Reference HUJ 13768 HUJ 12450 Measurement mm % of DW mm % of DW Disk width 171 100 230 100 Disk length 150 87.7 195 84.8 Disk depth 25 14.6 46 20.0 Total length 369 215.7 445 193.4 Eyeball length 13 7.6 17 7.4 Cornea 10 5.8 12 5.2 Pre-orbital length 34 19.9 44 19.1 Interorbital width 33 19.3 42 18.2 Spiracle width 10 5.8 13 5.6 Spiracle length 14 8.2 18 7.8 Nasal curtain 23 13.4 28 12.1 Interspiracular width 30 17.5 33 14.3 Preoral length 37 21.6 47 20.4 Mouth width 21 12.3 23 10.0 First gill slit 4 2.3 5 2.1 Second gill slit 7 4.1 9 3.9 Third gill slit 6 3.5 8 3.4 Fourth gill slit 6 3.5 7 3.0 Fifth gill slit 5 2.9 6 2.6 Width between first gill slit 36 21.0 44 19.1 Width between fifth gill slit 19 11.1 27 11.7 Snout tip to eye 33 19.3 43 18.7 Snout tip to mouth 32 18.7 43 18.7 Snout tip to first gill slit 50 29.0 60 26.0 Snout tip to fifth gill slit 71 41.5 96 41.7 Snout tip to pelvic fin 132 77.2 175 76.1 Snout tip to vent 124 72.5 166 72.1 Snout tip to sting 231 135.1 265 115.2 Pectoral fin anterior margin 117 68.4 149 64.8 Pectoral fin posterior margin 101 59.0 130 56.5 Pectoral fin inner margin 24 14.0 29 12.6 Pelvic fin anterior margin 30 17.5 41 17.8 Pelvic fin base 27 15.8 34 14.8 Span of pelvic fins 60 35.1 73 31.7 Clasper length 31 18.1 39 16.9 Tail base width 18 10.5 21 9.1 110 ACTA ADRIATICA, 45(1): 107-113, 2004
Table 1. cont’d
Tail base depth 9 5.2 11 4.8 Tail length 235 137.4 267 116.1 Ventral tail fold length 58 33.9 75 32.6 Dorsal tail fold length 55 32.1 66 28.7 Sting length 49 28.6 63 27.4
DESCRIPTION OF THE SPECIMENS gray margin, that spreads along the central part of the back from between the eyes to just before the beginning of the tail. The caudal sting is The disk rhomboid has slightly convex beige and the belly off-white to beige. The anterior margins at the level of the eyes while ventral surface is uniformly whitish to beige the posterior margins are anteriorly straight and with a gray to slightly brownish margin at the posteriorly convex. The snout is pointed. The tip of the snout. pelvic fins are quadrangular with rounded outer corners. The tail is slender and slightly depressed dorso-ventrally. The dorsal and ventral surfaces DISCUSSION of the tail have a fold posterior to the sting but it does not extend to the end of the tail. Dasyatis chrysonota is closely related to The disk depth is 14.6-20.0%, disk length D. pastinaca (Linnaeus, 1758) and, therefore, 84.8-87.7%, preoral length 20.0-21.6%, pelvic the two are often confused and misidentified. span 31.7-35.1%, pelvic fin anterior margin According to COWLEY & COMPAGNO (1993), 17.5-17.8% and ventral tail fold 32.6-33.9% of these species can be distinguished by the ratio the disk width. The pre-orbital length is 103.0- between the disk length and disk width and by 104.7% and the width between the first gill slits the snout to vent length/disk width, which is is 11.9-12.1% of the interorbital length. The smaller in D. pastinaca. In addition, the species eyeball length is 39.4-40.1%, spiracle length differ in coloration: the dorsal surface of D. 42.4-42.8% and distance between the fifth pair pastinaca is grayish-green to olive brown. D. of gill slits 14.3-15.1% of the interorbital width. chrysonota was reported for the first time in the The snout angle is 115-125°. The mouth is Mediterranean in the Gulf of Gabès (southern slightly arched, the skin flap on the upper jaws Tunisia) by MAURIN & BONNET (1970) as D. has 24 oral papillae. There are five elongated pastinaca var. marmorata. This occurrence was papillae, on the mouth floor three central and confirmed under the same taxon by QUIGNARD a single papilla on each side. Total tooth rows & CAPAPÉ (1971). Referring probably to earlier contain 36-38 in the upper and lower jaws, taxonomical papers (see COWLEY & COMPAGNO, each. The pelvic span is 31.7-35.1%, pelvic fin 1993) such as FREDJ & MAURIN (1987) and anterior margin 17.5-17.8%, and ventral tail fold CAPAPÉ & DESOUTTER (1990), QUIGNARD & 32.6-33.9%, all of the disk width. TOMASINI (2000) considered D. chrysonota = The dorsal surface is beige along the margin (D. marmorata) a valid species and included of the pectoral fin and toward the snout. The it among the chondrichthyan fishes of the pelvic fins are also beige. It is slightly darker Mediterranean Sea and the eastern tropical between the eyes, and along the center of the Atlantic. body and the length of the tail. Irregularly Several papers provide information on the shaped, gray to slate blue blotches, some ecology (CAPAPÉ, 1989), food and feeding habits interconnected, bordered by a thin dark flint (CAPAPÉ & ZAOUALI, 1992) and reproductive GOLANI & CAPAPÉ: First records of the blue stingray, D. chrysonota, off the coast of Israel 111 biology of D. chrysonota (D. marmorata). Key to Dasyatidae species in the CAPAPÉ (1989) suggested that in southern Mediterranean Tunisian waters, D. chrysonota undergoes 1a. Tail shorter than disk width; membranous competitive pressure from related dasyatid fold on the posterior ventral surface of tail species. Consequently, it inhabits restricted reaching its tip ...... Taeniura grabata areas in the Gulf of Gabès, entering a closed 1b. Tail longer than disk width; if membranous hyperhaline lagoon, the Bahiret el Biban fold present, it does not reach tip of tail ...... 2 (CAPAPÉ & ZAOUALI, 1992, 1993, 1995). CAPAPÉ & ZAOUALI (1993, 1995) estimated 2a. Tail more than 2.5 times longer than disk that disk width (DW) at birth is 108-115 mm width ...... 3 and that sizes at sexual maturity for males and 2b. Tail length less than 2.5 times in disk females are close to 300 mm and 320 mm DW, width ...... 4 respectively. The two specimens from Israel are 3a. Pointed snout; upper surface light-brown 171 and 230 mm DW and their sizes, especially with numerous dark brown with regard to the first specimen, indicate that spots ...... Himantura uarnak they were born in Israeli waters. 3b. Round snout; upper surface uniformly violet In the eastern tropical Atlantic, D. chrysonota to brownish-blue ...... Dasyatis violacea is widely distributed from southern Morocco to 4a. Tail length more than twice disk width South Africa (COWLEY & COMPAGNO, 1993). This ...... Dasyatis centroura pattern of zoological distribution, whereby a 4b. Tail length less than twice disk width ...... 5 species is found in the Mediterranean only along 5a. Three papillae on the mouth floor; upper the southern coasts and in the Levant, is known surface without blotches or spots in other species, e.g., Encheylcore anatina, Arius ...... Dasyatis tortonesei parkii and Acanthurus monroviae (see GOLANI et 5b. Five papillae on the mouth floor; upper al., 2002). It is possible that D. chrysonota is surface with blotches and spots ...... 6 generally rare or that many cases of this species 6a. Disk length more than 80% and snout- have been confused with D. pastinaca. to-vent length more than 70% of disk With the addition of Dasyatis chrysonota to width ...... Dasyatis chrysonota the Levantine ichthyofauna it seems appropriate to present a key to the family in the region and 6b. Disk length less than 80% and snout-to- vent length less than 70% of disk the entire Mediterranean width ...... Dasyatis pastinaca
REFERENCES
BEN-TUVIA, A. 1971. Revised list of the Check-list of the Fishes of the Eastern Mediterranean fishes of Israel. Isr. J. Zool., Tropical Atlantic. 1. JNICT/ EIU/UNESCO, 20: 1-39. Lisbon. CAPAPÉ, C. 1989. Les Sélaciens des côtes CAPAPÉ, C. & J. ZAOUALI. 1992. Le régime Méditerranéennes: aspects généraux de alimentaire de la pastenague marbrée, leur écologie et exemples de peuplements. Dasyatis marmorata (Steindachner, 1892) Océanis, 15(3): 309-331. (Pisces, Rajiformes, Dasyatidæ) des eaux CAPAPÉ, C. & M. DESOUTTER. 1990. Dasyatidae. tunisiennes. Vie Milieu, 42(3-4): 269-276. pp. 59-63. In: J.C. Quéro, J.C. Hureau, CAPAPÉ, C. & J. ZAOUALI. 1993. Nouvelles C. Karrer, A. Post, L. Saldanha (Editors). données sur la biologie de la reproduction de 112 ACTA ADRIATICA, 45(1): 107-113, 2004
la pastenague marbrée, Dasyatis marmorata Dasyatidae). S. Afr. Mar. Sci., 13: 135-149. (Steindachner, 1892) (Pisces, Rajiformes, FREDJ, G. & C. MAURIN. 1987. Les poissons dans la Dasyatidæ) des côtes méridionales banque de données MEDIFAUNE. Application de la Tunisie (Méditerranée centrale). à l’étude des caractéristiques de la faune Ichtyophysiol. Acta, 16: 1-34. ichtyologique Méditerranéenne. Cybium, CAPAPÉ, C. & J. ZAOUALI. 1995. Reproductive 11(3): 218-299. biology of the marbled stingray, Dasyatis GOLANI, D. 1996. The marine ichthyofauna of marmorata (Steindachner, 1892) (Pisces: the eastern Levant. History, inventory and Dasyatidæ) in the Tunisian waters. J. characterization. Isr. J. Zool., 42: 15-55. Aquaricult. Aquatic Sci., 7: 108-119 GOLANI, D. 1997. Handbook of the Fishes of CAPAPÉ C., R. HAMPARIAN, A. MARQUÈS & J.L. Israel. Keter Publ. House, Jerusalem., 269 BOUCHEREAU. 2002. First biometrical data in pp. (in Hebrew) a gravid female southern stingray, Dasyatis GOLANI, D., L. ORSI-RELINI, E. MASSUTI & J. P. americana Hildebrand and Schroeder, 1928, QUIGNARD. 2002. F. Briand (Editor). CIESM (Chondrichthyes: Dasyatidae) in Guadelupe Atlas of Exotic Species in the Mediterranean. waters (French West Indies). Acta Adriat., Vol. 1. Fishes. CIESM Publ., Monaco, 256 43(2): 99-106. pp. COLLENOT, G. 1969. Etude biométrique de la MAURIN, C. & M. BONNET. 1970. Poissons des croissance relative des ptérygopodes chez la côtes nord-ouest africaines (campagnes de roussette Scyliorhinus canicula L. Cah. Biol. la Thalassa), (1962 et 1968). Rev. Trav. Inst. Mar., 10: 309-329. Sci. Tech. Pêch. Marit., 34: 125-170. COMPAGNO, L.V.J. & T.R. ROBERTS. 1984. Marine QUIGNARD, J.P. & C. CAPAPÉ. 1971. Liste and freshwater stingrays (Dasyatidae) of commentée des Sélaciens de Tunisie. Bull. West Africa, with description of a new Inst. Nat. Sci. Tech. Océanogr. Pêche, species. Proc. Calif. Acad. Sci., 43: 283- Salammbô, 2: 131-141. 300. QUIGNARD J.P. & J.P. TOMASINI. 2000. COWLEY, P.D. & L.V.J. COMPAGNO. 1993. A Mediterranean fish biodiversity. Biol. Mar. taxonomic re-evaluation of the blue stingray Medit., 7(3): 1-66. from southern Africa (Myliobatiformes:
Received: 28 December 2003 Accepted: 27 April 2004 GOLANI & CAPAPÉ: First records of the blue stingray, D. chrysonota, off the coast of Israel 113
Prvi podaci o pronalsku žutulje, Dasyatis chrysonota (Smith, 1828) (Chondrichthyes: Dasyatidae), u izraelskom priobalju (istočni Mediteran)
Daniel GOLANI1 i Christian CAPAPÉ2
1 Odjel za evoluciju,sistematiku i ekologiju, Hebrejsko Sveučilište u Jeruzalemu, Jeruzalem 91904, Izrael
2 Laboratorij za ihtiologiju P.P. 104, Sveučilište u Montpellier-u II, Sveučilište znanosti i tehnike Languedoc-a, 34095 Montpellier Cedex 05, Francuska
SAŽETAK
Dva primjerka žutulje, Dasyatis chrysonota (SMITH, 1828), su ulovljena na mediteranskoj obali Izraela kao prvi zabilježeni nalaz na Levantu. Ova vrsta je poznata u tuniskom zaljevu Gabès. U ovom radu je razmatrana rasprostranjenost ove zapadno-atlantske vrste.
Ključne riječi: Chondrichthyes, Dasyatidae, Dasyatis chrysonota, Mediteran, južni Tunis, izraelska obala