Available online at www.izor.hr/acta/eng Online ISSN:1846-0453
International Journal of Marine Sciences
ISSN: 0001-5113 AADRAY 47 (1) 1-88 A1-A2 2006 UDK 551.46+58+59 (262)
Acta Adriat. Vol. 47 No. 1 1-88 Split 2006 A1-A2 PUBLICATION INFORMATION
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Editor-in-Chief Dr. Mira Zore-Armanda
ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.5:591.134(282.24 Neretva) AADRAY 47 (1): 5 - 11, 2006 Original scientific paper
Maturation, reproduction and recruitment of the sand smelt, Atherina boyeri Risso, 1810 (Pisces:Atherinidae) in the estuary of Mala Neretva River (southeastern Adriatic, Croatia)
Vlasta BARTULOVIĆ1*, Branko GLAMUZINA1, Alexis CONIDES2, Ana GAVRILOVIĆ 1 and Jakov DULČIĆ3
1 University of Dubrovnik, Department of Aquaculture, Ćira Carića 4, 20000 Dubrovnik, Croatia
2 Hellenic Centre for Marine Research, Agios Kosmas, Hellinikon, 16604 Athens, Greece
3 Institute of Oceanography and Fisheries, P.O. Box 500, 21000 Split, Croatia
*Corresponding author, e-mail: [email protected]
Characteristics of maturation and recruitment of the sand smelt, Atherina boyeri, from the Mala Neretva River estuary in the southeastern Adriatic, Croatia in 2001/2, are presented. The average gonadosomatic index (GSI) during a 12-month period was 1.59% for females and 2.1% for males. The highest value was in April, 5.4% for females and 4.7% for males. The smallest mature female was 5.2 cm total length. Fifty percent of the females were mature at 7.75 cm total length. New juveniles began to recruit in June and July and later appeared in fewer numbers. In general, the GSI was lower than in other sand smelt populations. The reasons are difficult to determine but might be partly explained by the high and unpredictable temperature and salinity variations in the researched area that have led to previously described disturbances of the sand smelt life cycle, as in feeding and a high incidence of spinal deformities.
Key words: sand smelt, Atherina boyeri, maturation, recruitment, Mala Neretva River
INTRODUCTION atherinid fish that mainly inhabits coastal and estuarine waters including coastal lagoons, salt The sand smelt, Atherina boyeri Risso 1810, marshes, and, more rarely, inland waters, over is common in the Mediterranean and adjacent seas a wide range of salinities from freshwater to and in the northeast Atlantic from the Azores to hypersaline conditions (HENDERSON & BAMBER, the northwestern coast of Scotland (QUIGNARD & 1987). Sand smelt mature in the first year of PRAS, 1986). It is a small, short-lived, euryhaline life and spawn in the second half of spring 6 ACTA ADRIATICA, 47(1): 5-11, 2006 and the beginning of summer (JARDAS, 1996; MATERIAL AND METHODS PALLAORO et al., 2002). The spawning season in brackish lagoons of southern France extends The present study was carried out in the from February to September, with a peak in estuary of the Mala Neretva River situated on April-June (TOMASINI et al., 1996). the southeastern Adriatic coast (Fig.1). The BARTULOVIĆ et al. (2004a) presented data on mouth of the river is closed by a dam that the diet and BARTULOVIĆ et al. (2004b) on the age, prevents the inflow of salt water into the upper growth, mortality, and sex ratio of the sand smelt agricultural part of the estuary. The sampling from the Mala Neretva River estuary. The sand site was downstream from the dam, where smelt usually inhabits ecosystems with unstable marine conditions dominate but the inflow of living conditions where temperature, salinity, fresh water and polluted water pumped from the turbidity, currents, and quality and quantity agricultural complex is constant. This leads to of food greatly vary. Therefore, reproduction daily and seasonal changes of temperature and characteristics are specific to each population. salinity at the sampling site. Average monthly The recruitment process is affected by unstable temperatures varied from 9˚C in February to conditions (BARTULOVIĆ, 2003) and success depends on the availability of suitable surfaces, 25˚C in August. The winter water temperatures such as sublittoral filamentous algae, for egg were affected by the inflow of the fresh water attachment (HENDERSON et al., 1984). that was colder (7.4˚C) than the sea water In this study we present characteristics of (11.4˚C) during this period. Salinity varied maturation and recruitment of the sand smelt from 4 to 38 psu during the winter but, due to from the Mala Neretva River estuary in the the low freshwater inflow, only from 30 to 38 southeastern Adriatic, Croatia. psu in the summer.
Fig. 1. Map of the study area BARTULOVIĆ, GLAMUZINA, CONIDES, GAVRILOVIĆ & DULČIĆ: Sand smelt in the Neretva estuary 7
Atherina boyeri (n = 1200) were collected GSI = wt gonads/total wt x 100 (WOOTON, monthly from March 2001 to February 2002 at 1990). The GSI was computed for each month the station near the dam. The fish were collected and in total, for females, males, and both sexes with a small net (5 mm mesh) used locally for together. the sand smelt fishery. It is one square meter of net on a metal frame, connected by ropes to a RESULTS main rope; when the fish appear above the net, it is lifted out of the water. Temperature and The smallest mature female was 5.2 cm (TL) salinity were measured before sampling with a and 50% of the females were mature at 7.75 cm mercury thermometer and a laboratory inductive (TL). Maturation, represented by the percentage salinometer. Fresh specimens were transported of females with a GSI above the average yearly to the laboratory where total (TL) and standard GSI of the total female sample, significantly length (SL) were measured to the nearest 0.1 correlated with total length (r2=0.887; Fig. 2). mm and body weight to the nearest 0.01 g. The average GSI during the 12-month period Gonads were examined to determine sex and was 1.59% for females and 2.1% for males. The reproductive stage. GSI began to rise in March (1.55% for females Gonads from all 1068 sexually mature fish and 4.6% for males; Fig. 3), peaked in April were dissected, dried from water and blood using (5.4% for females and 4.7% for males), and paper, and weighed to the nearest 0.01 g. The dropped in June (females 2.27% and males gonadosomatic index (GSI) was calculated as: 3.1%) and July (females 2.54% and males
Fig. 2. Percentage and length of mature sand smelt females from the Mala Neretva River. Vertical bar represents length at which 50% of the females in the sample were mature 8 ACTA ADRIATICA, 47(1): 5-11, 2006
Fig. 3. Average gonadosomatic index of males, females, and both sexes in monthly samples of sand smelt from the Mala Neretva River
3.17%). During March-May, over 90% of all was highest in June and July, 19% and 12% females were mature, i.e., had an above average respectively (Fig. 5). The number slowly value GSI (Fig. 4). No specimens of either decreased from August to October and no new sex with an above average GSI were found in recruits were found in November-May. Average August-February. total lengths of the new recruits were 3.91 cm in The percentage of newly recruited juveniles June, 4.3 cm in July, and 4.1 cm in August.
Fig.4. Percentage of mature females in monthly samples of sand smelt BARTULOVIĆ, GLAMUZINA, CONIDES, GAVRILOVIĆ & DULČIĆ: Sand smelt in the Neretva estuary 9
100
80
60 juveniles undetermined females 40 males Sample composition (%) composition Sample 20
0 MAMJ JASONDJ F Months
Fig. 5. Percentages of males, females, juveniles, and specimens of undetermined sex, per month
DISCUSSION AND CONCLUSIONS were recorded in sand smelt from the Suez Canal with a maximum of 5.3% for females The smallest mature female in the mouth of in February and 4.4% and 4.5% for males in Mala Neretva River was 5.2 cm (TL) and 4.3 February and March, respectively (FOUDA, 1994). cm (SL). The smallest female with ripe oocytes The maximum average GSI in females (8%) was in the Mauguio, Mejean, and Perols lagoons, twice as high as in males (4%) in the estuary of south France, was 3.8 cm SL (TOMASINI et al., the Guadalquivir River (FERNANDEZ-DELGADO 1996). Sexual maturity was attained by females et al., 1988). Sand smelt spawned in that area from in Aberthaw Lagoon in the Bristol Channel at March to June with a maximum in April. The 3.9 cm SL (CREECH, 1992). Sand smelt from monthly mean GSI of female sand smelt from Guadalquivir River in Spain were sexually Camargue Lagoon in southeastern France rose mature at 4.0 cm SL (FERNANDEZ-DELGADO & from January onwards, increased more rapidly HERNANDO, 1982) and sand smelt from Bardawil from March to May when the GSI reached Lagoon at 3.4 cm SL (GON & BEN-TUVIA, 1983). 13.3%, and dropped from June onwards. In The smallest mature female in the Suez Canal males, the GSI reached a plateau over the same was no more than 2.7 cm SL (FOUDA, 1994) period with a maximum of 9.16% in April and sand smelt from Mesolongi and Etolikon (ROSECCHI & CRIVELLI, 1992). The GSI of sand lagoons (west Greece) matured at a 3.4 cm TL smelt males from brackish lagoons of southern (LEONARDOS & SINIS, 2000). France was lowest in September (0.17%) and The GSI began to rise in March and the peaked in April (10.60%) TOMASINI & LAUGIER, highest values were in April. Values remained 2002). high in May and decreased in June. The period In the Aberthaw Lagoon, development of with high GSI values indicates the extensive ovaries starts in March, but the maximum GSI reproductive period of sand smelt in the mouth was reached in May for two-year-old fish and in of Mala Neretva River. Similar GSI values July for one-year-olds (CREECH, 1992). 10 ACTA ADRIATICA, 47(1): 5-11, 2006
The annual GSI cycle and values of sand (BARTULOVIĆ, 2003) that leads to disturbances of smelt in the mouth of Mala Neretva River are the sand smelt life cycle. Such disturbances can similar to those of the Suez Canal population affect feeding (BARTULOVIĆ et al., 2004a) or cause but significantly lower than those of some a high incidence of spinal deformities (TUTMAN French lagoon and other populations. The et al., 2000). The instability in the ecosystem reasons are difficult to determine, but could be could significantly influence the reproductive partly explained by the high and unpredictable potential of sand smelt in the Neretva River variation of temperature and salinity in study area estuary, compared to other researched areas.
REFERENCES
BARTULOVIĆ, V. 2003. Morphometry and GON, O. & A. BEN-TUVIA. 1983. The biology of Population Dynamics of Sand Smelt, Boyer´s sand smelt, Atherina boyeri Risso in Atherina boyeri Risso, 1810 (Pisces) in the the Bardawil Lagoon on the Mediterranean Estuary of Mala Neretva River (in Croatian). coast of Sinai. J. Fish Biol., 22:537-547. Thesis, University of Zagreb, Croatia, 125 HENDERSON, P.A. & R.N. BAMBER. 1987. On the pp. reproductive biology of the sand smelt BARTULOVIĆ, V., D. LUČIĆ, A. CONIDES, B. Atherina boyeri Risso (Pisces, Atherinidae) GLAMUZINA, J. DULČIĆ, D. HAFNER & M. and its evolutionary potential. Biol. J. Linn. BATISTIĆ. 2004a. Food of sand smelt, Atherina Soc., 32(4):395-415. boyeri Risso, 1810 (Pisces: Atherinidae) HENDERSON, P.A., A.W.H. TURNPENNY & R.N. in the estuary of the Mala Neretva River BAMBER. 1984. Long term stability of a sand (middle-eastern Adriatic, Croatia). Sci. Mar., smelt (Atherina presbyter Cuvier) population 68(4):597-603. subject to power station cropping. J. Appl. BARTULOVIĆ, V., B. GLAMUZINA, A. CONIDES, J. Ecol., 21:1-10. DULČIĆ, D. LUČIĆ, J. NJIRE & V. KOŽUL. 2004b. JARDAS, I. 1996. Jadranska ihtiofauna (Adriatic Age, growth, mortality and sex ratio of sand ichthyofauna). Školska Knjiga, Zagreb. 536 smelt, Atherina boyeri Risso, 1810 (Pisces: pp. Atherinidae) in the estuary of the Mala LEONARDOS, I. & A. SINIS. 2000. Age, growth and Neretva River (middle-eastern Adriatic, mortality of Atherina boyeri Risso, 1810 Croatia). J. Appl. Ichthyol., 20:427-430. (Pisces: Atherinidae) in the Mesolongi and CREECH, S. 1992. A study of the population of Etolikon Lagoons (W. Greece). Fish. Res., Atherina boyeri Risso, 1810 in the Aberthaw Lagoon, on the Bristol Channel, in south 45:81-91. Wales. J. Fish Biol., 41:277-286. PALLAORO, A., M. FRANIČEVIĆ & S. MATIĆ. 2002. FERNANDEZ-DELGADO, C. & J.A. HERNANDO. Age, growth and mortality of big-scale sand 1982. Relaciones morfometricas de Atherina smelt, Atherina (Hepsetia) boyeri Risso, boyeri Risso (Pisces: Atherinidae) de la 1810 in the Pantana Lagoon, Croatia. Per. laguna de Zonar (Cordoba, España). Donana Biol., 104(2):175-183. Acta Vertebrata, 9:13-25. QUIGNARD, C.J. & A. PRAS. 1986. In: P.J.P. FERNANDEZ-DELGADO, C., J.A. HERNANDO & M. Whitehead, M.L. Bauchot, J.C. Hureau, HERRERAAND BELLIDO. 1988. Life history J. Nielsen and E. Tortonese (Editors). patterns of the sandsmelt Atherina boyeri Atherinidae in Fishes of the North-Eastern Risso, 1810 in the estuary of the Guadalquivir Atlantic and the Mediterranean, UNESCO, River, Spain. Est. Coast. Shelf Sci., 27:697- Paris, 1207-1210 pp. 706. ROSSECHI, E. & A.J. CRIVELLI. 1992. Study of a FOUDA, M.M. 1994. Life history strategies of four sand smelt (Atherina boyeri Risso, 1810) small-size fishes in the Suez Canal, Egypt. J. population reproducing in fresh water. Ecol. Fish Biol., 46:687-702. Freshw. Fish, 1(2):77-85. BARTULOVIĆ, GLAMUZINA, CONIDES, GAVRILOVIĆ & DULČIĆ: Sand smelt in the Neretva estuary 11
TOMASINI, J.A. & T. LAUGIER. 2002. Male TUTMAN, P., B. GLAMUZINA, B. SKARAMUCA, V. reproductive strategy and reserve allocation KOŽUL, N. GLAVIĆ & D. LUČIĆ. 2000. Incidence in sand smelt from brackish lagoons of of spinal deformities in natural populations southern France. J. Fish Biol., 60:521-531. of sandsmelt, Atherina boyeri (Risso, 1810) TOMASINI, J.A., D. COLLART & J.P. QUIGNARD. in the Neretva River estuary middle Adriatic. 1996. Female reproductive biology of the Fish. Res., 45:61-64. sand smelt in brackish lagoons of southern WOOTON, R.J. 1990. Ecology of Teleost Fishes. France. J. Fish Biol., 49(4):594-612. Chapman and Hall, 404 pp.
Received: 23 March 2005 Accepted: 19 February 2006
Dozrijevanje i novačenje olige, Atherina boyeri Risso 1810 (Pisces: Atherinidae) na ušću Male Neretve (jugoistočni Jadran, Hrvatska)
Vlasta BARTULOVIĆ1*, Branko GLAMUZINA1, Alexis CONIDES2, Ana GAVRILOVIĆ1 i Jakov DULČIĆ3
1 Sveučilište u Dubrovniku, Odjel akvakulture, Ćira Carića 4, 20000 Dubrovnik, Hrvatska
2 Helenski Centar za morska istraživanja, Agios Kosmas, Hellinikon, 16604 Atena, Grčka
3 Institut za oceanografiju i ribarstvo, p.p. 500, Split, Hrvatska
*e-mail:[email protected]
SAŽETAK
Prikazane su karakteristike dozrijevanja i novačenja olige, Atherina boyeri na ušću Male Neretve, na srednjem dijelu istočne obale Jadrana, Hrvatska u 2001 i 2002. Prosječni gonadosomatski indeks tijekom 12-mjesečnog razdoblja za ženke je iznosio 1,59%, a za mužjake 2,1%. Najveća vrijednost je bila u travnju, za ženke 5,4%, a za mužjake 4,7%. Najmanja zrela ženka je zabilježena pri ukupnoj dužini 5,2 cm, a 50% ženki je bilo zrelo pri ukupnoj dužini 7,75 cm. Nova mlađ se počinje novačiti u lipnju i srpnju, a pojavljuje se i kasnije, ali u manjem broju. Vrijednosti GSI su uglavnom manje nego kod ostalih istraživanih populacija olige. Teško je zaključiti koji je razlog, ali djelomično se može objasniti velikim i nepredvidljivim kolebanjima temperature i slanosti, kod kojih su već opisani različiti poremećaji životnog ciklusa olige na istraživanom području, u ishrani i visokoj učestalosti deformacija kralješnice.
Ključne riječi: oliga, Atherina boyeri, dozrijevanje, novačenje, rijeka Mala Neretva
ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.553.1(261+262) 591.152(261+262).597.553.1 AADRAY 47 (1): 13 - 22, 2006 Original scientific paper
Population – genetic structure on European anchovy (Engraulis encrasicolus, Linnaeus, 1758) (Osteichthyes: Engraulide) from Mediterranean Basin and Atlantic Ocean
Petya P. IVANOVA* and Ivan S. DOBROVOLOV
Institute of Fisheries and Aquaculture, Primorski Blvd. 4, P.O. Box 9000, Varna, Bulgaria *Corresponding author, e-mail: [email protected]
Muscle proteins of the European anchovy Engraulis encrasicolus L. were analyzed using starch gel electrophoresis and isoelectric focusing on thin polyacrylamide ampholine gel. Twenty-two protein loci were analyzed and polymorphism was found in six of them. Based on genetic-biochemical data, we hypothesize that there are two anchovy subspecies, European and African. The former inhabits the Atlantic Ocean, the Mediterranean coast of Europe, and the Aegean, Marmora, Black, and Azov Seas. The latter is found in the Cape Blank region of the Atlantic Ocean and, probably, along the northwestern part of the African coast. The Aegean anchovy consists of hybrid populations, resulting from introgressive hybridization between the European and the African populations. No evidence for subspecies differentiation between the populations from the European coast of the Mediterranean and the Atlantic Ocean was found. Genetic distances between the Azov and Black Sea populations show that the former probably entered the Black Sea during the Karangad period and the latter during the last connection of the Black Sea to the Mediterranean. The genetic distance between the Black Sea anchovy and the Azov anchovy shows that they could be specified as two different populations. Probably some earlier subspecies differences disappeared as a result of introgressive hybridization.
Key words: anchovy, population structure, genetic distance, Mediterranean Basin, Atlantic Ocean
INTRODUCTION and southern groups, and the Mediterranean anchovy into western and eastern groups. The The European anchovy, Engraulis latter group included anchovies from the Aegean, encrasicolus L., is a shoaling clupeoid that Marmora, Black, and Azov Seas. is distributed along the eastern Atlantic coast According to ALEXANDROV (1927), the Black from Scandinavia to west Africa. It is also Sea anchovy inhabited the western part of the found in the Mediterranean, Black, and Azov Black Sea while the Azov anchovy inhabited Seas (WHITEHEAD et al., 1988). FAGE (1911, 1920) the eastern part of the Black Sea, entering subdivided the European anchovy into two races, the Azov Sea for reproduction and nurture. the Atlantic and the Mediterranean, and further POUSANOV (1936) combined the Black Sea and subdivided the Atlantic anchovy into northern the Mediterranean anchovy into one race and 14 ACTA ADRIATICA, 47(1): 13-22, 2006 considered the Azov anchovy another species, 1993; CRONIN et al., 1993; MARGOULAS & ZOUROS, Engraulis maeoticus. 1993; CHAPMAN et al., 1994, cited after BEMBO et al., Based on immunological analyses, 1995). BEMBO et al. (1995) studied the mtDNA ALTUCHOV (1974) found differences between the variation in E. encrasicolus in the northwestern Black Sea and the Azov anchovies. SHEVCHENKO Mediterranean. Their DNA data were in (1980) considered the Azov anchovy a relict form accordance with their earlier allozyme and from the Karangatian period and the Black meristic results. MARGOULAS & ZOUROS (1993) Sea anchovy a subsequent immigrant from the and MARGOULAS et al. (1996) studied mtDNA contemporary Mediterranean period. KALNINA variation in E. encrasicolus and found two main & KALNIN (1984), KALNIN et al. (1984), KALNIN, anchovy mtDNA phylads in the Mediterranean: & KALNINA (1985) examined introgressive phylad A dominated in the Black and Aegean hybridization, population structure, biochemical Seas while phylad B was more numerous in polymorphism, genetic differentiation, and western waters. reproductive isolation of two anchovy races in The present paper aims to summarize long- the Black and Azov Seas using biochemical- term genetic-biochemical data for clarifying genetic methods. the intraspecific divergence of anchovy from DOBROVOLOV (1976, 1978, 1987, 1992) and different populations: the Black Sea (western DOBROVOLOV et al. (1980) studied the phylogenetic and eastern part), the Azov, Marmora, Aegean, relationship between E. encrasicolus from the Adriatic, and Mediterranean Seas, Canary Atlantic Ocean and from the Mediterranean Islands and Cape Blank (Africa) using two Basin on the basis of allozyme analyses. elctrophoretical techniques. GARCIA et al. (1994, cited after BEMBO et al., 1995) reported an absence of genetic structuring of anchovy inhabiting the western Mediterranean MATERIAL AND METHODS after an allozyme study. SPANAKIS et al. (1989) Sampling distinguished anchovy stocks from the Ionian and Aegean Seas by morphometric and allozyme A total of 3 520 specimens of anchovy analyses. (Еngraulis encrasicolus) were collected from MtDNA markers can be used for species 11 localities during 1973-2004 (Table 1, Fig.1). identification and detection of intraspecific Samples for electrophoretic analysis were variation in E. encrasicolus stocks (CHOW et al., captured by fishing vessels and trap-nets. The
Table 1. Еngraulis encrasicolus samples collected during 1973-2004
Region No. Year Region No. specimens 1 1973 Atlantic Ocean (Cape Blank) 84 2 1980 Atlantic Ocean (Grand Canary) 98 3 1994 Mediterranean Sea (Valencia) 72 4 1994 Mediterranean Sea (Nice) 32 5 1988 Adriatic Sea (near Venice) 100 6 1978 Aegean Sea (near Piraeus) 41 7 1993 Aegean Sea (near Thessalonica) 68 8 1983, 1991 Sea of Marmora (Istanbul) 352 9 1973, 1975-1980, 1982, 1988, 1994, 1997 Black Sea (Bulgarian coast) 1841 10* 1975, 1981, 1989 Sea of Azov 593 11 1989 Black Sea (near Poti) 239 * Identified as ‘Portuguese’ in our previous papers IVANOVA & DOBROVOLOV: Genetic structure of anchovy from the Mediterranean and Atlantic 15
Fig. 1. Sampling locations of anchovy E. encrasicolus, collected for electrophoresis study fish were frozen immediately after catch and similarity and genetic distance were performed brought to the laboratory in portable refrigerators according to NEI (1972). Nomenclature or dry ice at -20°C. Samples from the Black Sea for loci and alleles essentially follows the were frozen in the Institute of Fisheries and recommendations of SHAKLEE et al. (1990). Aquaculture (IFA) laboratory in Varna. RESULTS AND DISCUSSION Starch gel electrophoresis Several authors have suggested the Proteins were separated by horizontal starch existence of anchovy subspecies (races) in gel electrophoresis according to SMITHIES the Mediterranean on the basis of variation in (1955), modified by DOBROVOLOV (1973). Muscle proteins were stained with Amido morphological characters but the taxonomic Black 10B. Buffer systems of DOBROVOLOV status of these divisions remains doubtful (1976) and CLAYTON & GEE (1969) were used for (SPANAKIS et al., 1989). Polymorphism of general the elecrophoresis. muscle proteins (PROT) could be used to determinate taxonomic differences in the Isoelectric focusing (IEF) anchovy population. Four polymorphic zones were found after LKB (Stockholm) equipment was used for analysis of general muscle proteins using isoelectric focusing (IEF) on thin polyacrilamide starch gel electrophoresis (DOBROVOLOV, ampholine gel with pH gradients of 3.5-10. 1978, 1992; DOBROVOLOV et al., 1980). Since Muscle proteins were stained with Coomassie Brilliant Blue R-250. When several forms of the second polymorphic zone (PROT-2*) the same protein (enzyme) were observed, covered the first (PROT-1*) on the starch loci were identified by number, beginning gel electrophoregrams, they could not be with one for the locus closest to the cathode. accurately differentiated and the application Gene frequencies of the polymorphic loci of other electrophoretical techniques was were calculated using the HARDY-WEINBERG necessary. By using isoelectric focusing (IEF equilibrium. Calculations of indices of genetic on thin polyacrilamide ampholine gel), six 16 ACTA ADRIATICA, 47(1): 13-22, 2006
Fig. 2. Isoelectric focusing (IEF) of anchovy muscle proteins on thin polyacrylamide ampholine gel with pH 3.5-10 (1500V, 25mA, 30W, 120 min); PROT-1*, 2*, 3*, 4*, 5*, and 6* = polymorphic loci; АА, ВВ, АВ, and АА′ = genotypes; Overlapping polymorphic zones are marked as: • PROT-1*, PROT-2*, ▲PROT-3*, ▬ PROT-4*, ■ PROT-5*, ○ PROT-6*; O = origin polymorphic zones were found (Figs. 2, 3). lactate dehydrogenase expression (LDH- The use of two electrophoretical methods A* polymorphism; DOBROVOLOV, 1976, 1978). enabled us to obtain more precise information The other two polymorphic zones, PROT-5*, about the above-mentioned polymorphism. The 6*, were found by using IEF. The observed polymorphic zones PROT-1*, 2*, 3* had lipase polymorphism follows the HARDY-WEINBERG activity while most of the monomorphic protein equilibrium where χ2 is lower than 3.84 (df = 1). fractions had esterase activity (DOBROVOLOV, χ2 digression was found only in the samples from 1987). The fourth polymorphic zone had the Aegean Sea (Kavala) where the χ2 value IVANOVA & DOBROVOLOV: Genetic structure of anchovy from the Mediterranean and Atlantic 17
Fig. 3. Scheme of isoelectric focusing (IEF) of general muscle proteins from anchovy on thin polyacrylamide gels with pH 3.5 - 10; PROT-1*, 2*, 3*, 4*, 5*, and 6* = polymorphic loci; АА, ВВ, АВ, АА′, and А′А′ = genotypes; 0 = origin was 3.928 in the first polymorphic zone (PROT- data are not included in Tables 2 and 3. 1*; p>0.005). The reason for this high value The genetic-biochemical analyses show that probably was that samples from two populations the Azov anchovy appears sporadically near the were mixed (mechanically). Therefore, these Bulgarian coast. The Aegean population stands
Table 2. Estimated allele frequencies of polymorphic loci on general muscle proteins (PROT) 1 in anchovy from 11 inves- tigated regions (locations given in Table 1) Region no. Locus Allele 1234567891011 a* 0.975 0.977 0.881 0.882 0.634 0.552 0.965 0.953 0.840 0.954 0 PROT-1* b* 0.025 0.023 0.119 0.118 0.366 0.448 0.035 0.047 0.160 0.046 1 a* 0.874 0.879 0.961 0.866 0.829 0.546 0.720 0.625 0.639 0.740 0.980 PROT-2* b* 0.126 0.121 0.039 0.134 0.171 0.454 0.280 0.375 0.361 0.260 0.020 a* 0.721 0.728 0.607 0.768 0.817 0.877 0.685 0.859 0.813 0.694 0.401 PROT-3* b* 0.279 0.272 0.393 0.232 0.183 0.123 0.315 0.141 0.187 0.306 0.599 a* 0.915 0.928 0.902 0.875 0.707 0.750 0.705 0.803 0.771 0.735 0.325 PROT-4* b* 0.085 0.072 0.098 0.125 0.293 0.250 0.295 0.187 0.229 0.265 0.625
1 Eighteen fractions with common electrophoretical mobility were observed on the PROT electrophoregrams. Polymorphic zones PROT-5* and PROT-6* were decoded only in the last few years (in the Black Azov and Adriatic Seas) and are not included in calculations of INei in Table 3 18 ACTA ADRIATICA, 47(1): 13-22, 2006
Table 3. Genetic distance (DNei; above asterisks) and genetic identity (INei; below asterisks) based on 22 loci for European anchovy (Engraulis encrasicolus) from 11 populations (locations given in Table 1)
Region 1 2 3 4 5 6 7 8 9 10 11 no. 1 * 0.0000 0.0015 0.0005 0.0088 0.0192 0.0034 0.0051 0.0050 0.0024 0.0740 2 1.0000 * 0.0017 0.0005 0.0080 0.0190 0.0040 0.0052 0.0051 0.0027 0.0752 3 0.9985 0.9983 * 0.0020 0.0087 0.0210 0.0072 0.0099 0.0107 0.0040 0.0630 4 0.9995 0.9995 0.9980 * 0.0050 0.0140 0.0030 0.0042 0.0040 0.0022 0.0692 5 0.9912 0.9920 0.9913 0.9950 * 0.0060 0.0069 0.0080 0.0050 0.0064 0.0460 6 0.9810 0.9810 0.9790 0.9863 0.9940 * 0.0136 0.0090 0.0062 0.0130 0.0545 7 0.9966 0.9960 0.9928 0.9970 0.9931 0.9870 * 0.0030 0.0020 0.0001 0.0641 8 0.9949 0.9950 0.9900 0.9960 0.9920 0.9910 0.9970 * 0.0008 0.0027 0.0800 9 0.9950 0.9950 0.9893 0.9960 0.9950 0.9920 0.9980 0.9992 * 0.0021 0.0690 10 0.9976 0.9973 0.9960 0.9978 0.9936 0.9870 0.9999 0.9970 0.9979 * 0.0649 11 0.9287 0.9280 0.9390 0.9331 0.9550 0.9470 0.9379 0.9228 0.9330 0.9372 * midway between the African and European the Aegean Sea it is 0.366-0.448. The frequency populations, probably as a result of introgressive of this allele north of Canary Island is 0.046, hybridization between them. A gene flow of and varies from 0.023 in the Black Sea to 0.160 about 50% from the African population to the near Valencia. This is a proof of the penetration Aegean population was established. of the European anchovy from the Atlantic Evidence for the gene flow from the Ocean along the European coast (northern part northwestern part of the African coast of Mediterranean and Black Sea). The analyzed (Mediterranean) to the Aegean Sea (in the remote populations from the Black, Marmora, Azov, past) is the frequency of the allele B in the first Adriatic, and Mediterranean Seas (Nice and polymorphic zone, (q PROT-1*B). In the Cape Valencia) are genetically close to the European Blank population, the frequency is 1 while in anchovy caught to the north of Canary Island
Fig. 4. UPGMA tree, derived from allozyme data for 22 loci using NEI’S genetic distance (DNei), illustrating the relation- ships among 11 anchovy populations IVANOVA & DOBROVOLOV: Genetic structure of anchovy from the Mediterranean and Atlantic 19
No genetic-biochemical evidence for the with the Mediterranean. The data for the existence of two anchovy subspecies (races), genetic distances and the time of divergence Atlantic and Mediterranean, has been found. be obtained had confirmed conclusions of Such evidence is found only for the European SHEVCHENCO (1980). anchovy and this from the Cape Blank (African The genetic divergence (DNei) between the anchovy). Presumably the European anchovy Azov and the Black Sea anchovy populations populations are well diverged from the African shows that they belong to two different one (Fig. 4). populations, i.e., the Azov anchovy is not a DOBROVOLOV (1987, 1992) recognized that Tercier relict as supposed by POUSANOV (1936). the Black and Azov anchovy populations had Probably some subspecies differences between a common ancestor, the Atlantic anchovy that them existed in the past but disappeared as a inhabits the European coast. A short genetic result of introgressive hybridization. distance (DNei) between the Black Sea and the Marmara Sea anchovy was also found. CONCLUSIONS In the late Miocene (about 6 million years ago), prolonged movements of the African No evidence for the existence of subspecies continental plate northward broke the link differentiation between anchovy populations between the Mediterranean and the Atlantic from the European coast of the Mediterranean Ocean in the Gibraltar area (HSŰ, 1978). and the Atlantic Ocean was found. However, Communication with the Atlantic was closed based on genetic-biochemical data, the and the Mediterranean was converted into a existence of two anchovy subspecies, European series of saline lakes. Very few marine species and African, is suggested. The former inhabit seem to have survived this salinity crisis that the Atlantic and Mediterranean coasts of lasted several hundred thousands of years (HSŰ, Europe and the Aegean, Marmora, Black, and K.J. 1978; POR & DIMENTMAN 1985; SELLI, 1985). Azov Seas. The latter inhabits the Cape Blank The great bulk of present-day Mediterranean region in the Atlantic Ocean and, probably, species entered the region during the early the northwestern part of the African coast Pliocene, slightly less than 5 million years (Mediterranean). ago, when communication with the Atlantic The Aegean anchovy is a hybrid population was reestablished and Atlantic waters rushed as a result of introgressive hybridization between through the Gibraltar into the Mediterranean the European and the African anchovies. (SARA, 1985; POR, 1989). It is supposed that the The Black, Marmora, Azov, Adriatic, and African anchovy occupied areas with warmer Mediterranean (Nice and Valencia) populations water along the Mediterranean coast of Africa, are genetically close to the European anchovy, while the anchovy from the European coast caught north of the Canary Island. The genetic of the Atlantic Ocean, being adapted to colder distance between the Azov and Black Sea waters, settled along the European coast of the populations show that the former probably Mediterranean. entered the Black Sea during the Karangad At the end of Pliocene, a connection was period and the latter during the last connection established between the Black and Aegean of the Black Sea to the Mediterranean. Seas through the Dardanelle and Bosporus Straits (BACESCU, 1985, TORTONESE, 1985). The ACKNOWLEDGEMENTS insignificant genetic distance between the Black Sea and the Atlantic anchovy, and between The authors are obliged to Prof. K. PRODANOV and Dr. Zh. MANOLOV (IFA-Varna), the Black Sea and the Adriatic populations, is Dr. A.K. CHASHCHIN (AzNIRKh), Prof. V.N. evidence of the entry of the European anchovy ZALATARJEV, the Kovalevsky Institute of Biology into the Black Sea through its last connection of the Southern Seas, NASU, Fotis ARAPOGLU 20 ACTA ADRIATICA, 47(1): 13-22, 2006
(INAGREF) for supplying the anchovy samples Genetics, Institute of Animal Physiology and from Canary Island, Nice (France), Azov Sea, Genetics, Academy of Science of the Czech the eastern part of the Black Sea, and the Aegean Republic) for preparation of the UPGMA Sea, and Dr. Petr KOTLIK (Laboratory of Fish phylogenetic tree.
REFERENCES
ALEXANDROV, A.I. 1927. Anchovy from Azov- Commercial Fish Species from Bulgarian Black Sea basin and it origin and taxonomy. Waters and World Oceans. Ph.D. Thesis, Proc. Kerch Fish. Stn., 1/2 and 3:43 pp. Institute of Zoology, Bulgarian Academy of ALTUCHOV, J. P. 1974. Fish Population Genetics. Science, 533 pp. Moscow, 245 pp. DOBROVOLOV, I.S. 1992. Study of the intraspecific BACESCU, P. 1985. The effects of geological divergence of anchovy Engraulis encrasicolus and physicochemical factors on the L. Comptes Rendus de l’Academie Bulgare distribution of marine plants and animals des Sciences, 45(2):63-65. in the Mediterranean. In: MORAITOU- DOBROVOLOV, I., C. YANNOPOULOS & S. APOSTOLOPOLOU and V. KIORTSIS (Editors). DOBROVOLOVA. 1980. Biochemical genetic Mediterranean Marine Ecosystems. Plenum variation in anchovy Engrauluis encrasicolus Press, New York and London, pp.195-212. L. Comptes Rendus de l’Academie Bulgare BEMBO, D., G. CARVALHO, M. SNOW, N. CINGOLINI des Sciences, 33(6):869-872. & T. PITCHER. 1995. Stock discrimination FAGE, L. 1911. Recherches sur la biologie de among European anchovies E. encrasicolus, l’anchois Engraulis encrasicolus (L.) Ann. by means of PCR-amplified mitochondrial Inst. Oceanography, Monaco, 2(4):1-40. DNA analyses. Fish. Bull., 94:31-40. FAGE, L. 1920. Engraulidae. Report. Danish Ocean. CLAYTON, J.W. & G.H. GEE. 1969. Lactate Expedition 1908-1910 to the Mediterranean dehydrogenase isozymes in long nose and and Adjacent Seas, 2, Biology, A9:1-33. black nose Dace (Rhinichthys cataractae HSŰ, K.J. 1978. When the Black Sea was drained. and R. atratulus) and their hybrid. J. Fish. Sci. Am., 238:52-63. KALNINA, O.V. & V.V. KALNIN. 1984. Genetic Res. Bd. Can., 26(11):3049-3053. differentiation and reproductive relationship DOBROVOLOV, I.S. 1973. Micro starch gel between the Black Sea race and Azov electrophoresis (in Bulgarian, with English Sea race of European anchovy. 2. Genetic summary). Proc. Inst. Oceanogr. Fish., differences between the Black Sea race Varna, 12:157-162 and the Azov Sea race and their intrarace DOBROVOLOV, I.S. 1976. Multiple forms of tactate- heterogeny. Genetics, 20(2):309-313 . dehydrogenase in anchovy (Engraulis KALNIN, V.V. & O.V. KALNINA. 1985. Genetic encrasicolus L.) from the Black Sea, the Sea differentiation and reproductive relationship of Azov and the Atlantic Ocean. Comptes between the Azov and Black Sea races of Rendus de l’Academie Bulgare des Sciences, anchovy. 3. Introgressive race hybridization 29(6):877-880. and population structure of the Black Sea DOBROVOLOV, I.S. 1978. Polymorphism of muscle anchovy (in Russian). Genetics, 21(8):1352- proteins of anchovy Engraulis encrasicolus 1360 (L.) from Azov-Black Sea basin and Atlantic KALNIN, V.V., O.V. KALNINA & M.B. DASHOVA. Ocean (in Russian). J. Ichthyol., 18(3/ 1984. Genetic differentiation and reproductive 110):534-539 relationship in the Azov and Black Sea races DOBROVOLOV, I.S. 1987. Biochemical and of anchovy. 1. Biochemical polymorphism Population-genetic Investigations of (in Russian). Genetics, 20(2):303-308 IVANOVA & DOBROVOLOV: Genetic structure of anchovy from the Mediterranean and Atlantic 21
MARGOULAS, A. & E. ZOUROS. 1993. Restriction- Basin. Springer-Verlag, Berlin, pp. 131- site heteroplasmy in anchovy (Engraulis 151. encrasicolus) indicates incidental biparental SHAKLEE, J., F.W. ALLENDORF, D.C. MORIZOT & inheritance of mitochondiral DNA. Mol. G.S WHITT. 1990. Gene nomenclature for Biol. Evol., 10(2):319-325. protein-coding loci in fish. Trans. Am. Fish. MARGOULAS, A., N. TSIMENIDES & E. ZOUROS. Soc., 119:2-15. 1996. Mitochondrial DNA phylogeny and reconstruction of the population history of a SMITHIES, O. 1955. Zone electrophoresis in species: The case of the European anchovy starch gels: group variations in the serum (Engraulis encrasicolus). Mol. Biol. Evol., proteins of normal human adults. Biochem. 13(1):178-190. J., 61:629-641.
NEI, M. 1972. Genetic distance between popula- SPANAKIS, E., N. TSIMENIDES & E. ZOUROS. 1989. tions. Am. Naturalist, 106:283-292. Genetic differences between populations of POR, F.D. 1989. The Legacy of Tethys. An Aquatic sardine Sardina pilchardus and anchovy Biogeography of the Levant. Kluwer Acad. Engraulis encrasicolus in the Aegean and Publ., Dodrecht, 127 pp. Ionian Seas. J. Fish Biol., 35:417-437. POR, F.D. & C. DIMENTMAN. 1985. Continuity of Messinian biota in the Mediterranean basin. SHEVCHENKO, N.F. 1980. Geographical changing In: D.J. STANLEY and F.C. WEZEL (Editors). of anchovy Engraulis encrasicolus (L.) Geological Evolution of the Mediterranean in the Mediterranean basin (in Russian). Basin. Springer-Verlag, Berlin, pp. 545-557. Icthyol. J., 20(1/120):20-30. POUSANOV, І.I. 1936. Anchovy. Scientific- TORTONESE, E. 1985. Distribution and ecology of commercial monography. Notes of Gorkij endemic elements in the Mediterranean fauna Univ., 5:101. (fishes and echinoderms). In: MORAITOU- SARA, M. 1985. Ecological factors and their bio- APOSTOLOPOLOU and V. KIORTSIS (Editors). geographic consequences in the Mediter- ranean ecosystems. In: Mediterranean Mediterranean Marine Ecosystems. Plenum Marine Ecosystems. Plenum Press, New Press, New York and London, pp. 57-83. York and London, pp. 1-17. WHITEHEAD, P.J.P., G.J. NELSON & T. WONGRATANA. SELLI, R. 1985. Evolution of the Tyrrhenian Sea. 1988. FAO Species Catalogue, ver. 7, part 2: In: D.J. STANLEY and F.C. WEZEL (Editors). Clupeoid Fishes of the World. FAO Fish. Geological Evolution of the Mediterranean Synopsis, 125:546 pp.
Received: 31 August 2005 Accepted: 7 March 2006 22 ACTA ADRIATICA, 47(1): 13-22, 2006
Genetske strukturne populacije brgljuna (Engraulis encrasicolus Linnaeus, 1758) (Osteichthyes: Engraulide) iz Mediterana i Atlantskog oceana
Petya P. IVANOVA* i Ivan S. DOBROVOLOV
Institut za ribarstvo i akvakulturu, Primorski Blvd. 4, P.P. 9000, Varna, Bugarska * e-mail: [email protected]
SAŽETAK
Analizirani su mišićni proteini europskog brgljuna (Engraulis encrasicolus L.) upotrebom škrobno gelne elektroforeze i izoelektričnog fokusiranja na tankom poliakrilamidnom gelu. Analizirana su 22 proteinska položaja i kod šestorice je dobiven polimorfizam. Postavljena je hipoteza na osnovi genetsko-biokemijskih podataka da postoje 2 podvrste brgljuna: europska i afrička. Prva naseljava Mediteran, mediteranske obale Europe, te Egejsko, Mramorno, Crno i Azovsko more. Druga je nađena u području Cape Blank u Atlantskom oceanu i vjerojatno uzduž sjeverozapadnog dijela afričke obale. Egejski brgljun se sastoji od hibridnih populacija koje su rezultat introgresivne hibridizacije. Nema uvida u diferencijaciju podvrsta između populacija s europske obale Mediterana i Atlantskog oceana. Genetske udaljenosti između populacija Azovskog i Crnog mora ukazuju da je prva ušla u Crno more tijekom karangadskog razdoblja, a druga tijekom zadnje veze Crnog mora i Mediterana. Genetska udaljenost između brgljuna iz Crnog mora i brgljuna iz Azovskog mora upućuje na to da se mogu razlikovati različite populacije. Vjerojatno su neke razlike u podvrstama nastale kao rezultat introgresivne hibridizacije.
Ključne riječi: brgljun, strukturna populacija, genetička udaljenost, Mediteranski bazen, Atlantski ocean ISSN: 0001-5113 ACTA ADRIAT., UDC: 591.69:[597:693.32](262.3) 597:639.2](262.3):591.69 AADRAY 47 (1): 23 - 28, 2006 Original scientific paper
Parasites of Adriatic cage reared fish
Ivona MLADINEO
Institute of Oceanography and Fisheries, P.O. Box 500, 21 000 Split, Croatia e-mail: [email protected]
With the rapid development of aquaculture in the Mediterranean, a number of parasitic diseases have emerged in cage-reared fish. In confined rearing conditions, the diseases can induce mortality and economic losses related to suppressed growth. With diversification of aquaculture products and the introduction of new fish species into the rearing system, new parasitic pathogens have found their way into new environments, resulting in adaptation of the parasite, new colonization on resident aquaculture species (primarily sea bass and sea bream), or increased parasite prevalence and abundance on the newly cultivated fish species. The parasitofauna of reared fish is impoverished in terms of species richness and has greater population values than in the wild fish population. While the parasitofauna of fish reared in the Mediterranean is discussed in numerous publications, only occasional findings specifically refer to the Adriatic Sea. Wild fish populations in the Adriatic Sea have been sampled for parasite isolation and identification but an overview of reared fish parasitofauna has never been reported. This was the main goal of this study.
Key words: sea bass, sea bream, parasitofauna, Adriatic Sea
INTRODUCTION index, the mesenterial accumulation of adipose tissue makes the fish unsuitable for much of the There are four well-established species in market. Adriatic aquaculture: sea bass (Dicentrarchus labrax), sea bream (Sparus aurata), sharpsnout The most recently introduced and com- bream (Diplodus puntazzo), and red sea mercially valuable fish in Adriatic aquaculture bream (Pagellus bogaraveo) with the last two is the northern bluefin tuna (also called the comprising a minor part of the total production. Atlantic bluefin tuna; Thunnus thynnus) whose Sharpsnout bream culture was devastated by pathology is still being revealed. Only recently, severe mortalities caused by Enteromyxum leei an excellent review of the pathology of diverse (ex. Myxidium leei; Myxozoa: Myxosporidia) tuna species was published, with an abundant and its market appeal and value never reached those of sea bass and sea bream. Therefore, number of parasitological findings (MUNDAY et the reared population is decreasing. Red sea al., 2003), but most of the information deals with bream is reared only after capture from the wild fish populations from (sub)tropical waters wild and, despite having a good conversion and, therefore, does not apply to the Adriatic. 24 ACTA ADRIATICA, 47(1): 23-28, 2006
Parasites that have a low prevalence and abundance and minor pathological effects on their hosts in the wild can easily spread in populations confined to rearing systems, causing serious outbreaks of epizootic diseases (ATHANASSOPOULOU et al., 1999; COMPANY et al., 1999). Epidemics are optimized by the high stocking density of the host and its usually compromised immunity resulting from daily stress. Most parasites are very hard to eradicate, especially if the therapy must be applied in semi or offshore net pans. The spectrum of chemotherapeutics is very narrow and most useful compounds are not licensed for aquaculture. The key solution lies in prevention based on optimal husbandry and zootechniques where appropriate stocking density, frequent changes of nets, and diet regulation play the biggest roles. The scope of this report was to collect data from previous findings, add new information gathered by the author, and combine them in an overview that can be used as basic information Fig. 1. Map of the Adriatic Sea with locations of sampled in future studies. facilities
MATERIAL AND METHODS duct (pyloric area, middle intestine, and rectal part), and from the spleen, liver, gonads, and Seven fish farms in the eastern part of the kidney. If positive, smears were stained by Adriatic were monitored from June 2001 to May-Grünwald Giemsa. Myxosporeans were March 2002 (Fig. 1): Kaldonta Bay (Cres Island; measured and identified according to LOM & F1), Vela Luka Bay (Šolta Island; F2), Peleš ARTHUR (1989). Bay (near Primošten; F3), Žižanj Island (F4), Gill monogeneans were counted on the Žižanj Island (F5), Maslinovac Island (Pelješac middle third of the first gill arch. Cut gills and Peninsula; F6), and Tajan Island (Pelješac fins were placed in PETRI dishes while scrapings Peninsula; F7). of skin and nasal cavities were mounted on slides Fish were collected every three months for examination under a dissecting microscope from offshore net pens at each facility, always with 20x magnification. Monogeneans were from the same cage, for nine months. Samples detached with dissecting needles, counted, comprised 9-15 sea bass (Dicentrarchus labrax), sea bream (Sparus aurata), sharpsnout and collected in a watch glass. For fixation, bream (Diplodus puntazzo), and red sea bream parasites were ruptured between the slide and (Pagellus bogaraveo) of at least one year. In coverslip by finger pressure and a mixture of total, 673 individuals were examined. 4% formal-dehyde and glycerin (5:1) was added Collected fish were put on ice and brought to the edge of a coverslip. After evaporation of to the laboratory within hours where they the remaining fixative, edges were sealed with were autopsied and biometrical measures were DU-NOYER sealant. recorded. Fresh smears were taken from the gills, In addition, 62 northern bluefin tuna were skin, and fins, from three parts of the alimentary sampled at an eighth facility on the northwestern MLADINEO: Parasites of Adriatic cage reared fish 25 part of Brač Island during harvest in January Upon arrival in the laboratory, fresh smears 2003 and when daily mortality occurred in of gills, kidney, spleen, liver, gall bladder, July 2003. Prior to rearing, these tuna had intestinal and stomach mucosa, and endocardial been caught in May 2002 in the waters near tissue from the ventriculus were examined Jabuka Island and transported to the farm where under a light microscope. Digenean cysts from they were fed mixed fish and frozen imported gills, cartilaginous parts of gill arches, stomach herrings from small boats. layers, pyloric ceca, skin, and intestine were Prior to washing the fish trunks, the body collected, measured, and excysted with fine surface was inspected for the presence of any needles under a stereomicroscope. Individuals were stained in Borax carmine, mounted in changes. Because of the value of the carcasses, Canada balsam, and fixed under a coverslip. no incisions on the fins, skin, or eyes were Remaining cysts were collected and fixed in made. Visceral organs and gill arches were 70% alcohol. Myxosporidians and helminthes collected. Viscera samples were individually were collected as in the other cage reared fish. collected in plastic bags and transported to the laboratory. Blood samples were collected before evisceration from the incision made beneath RESULTS the pectoral fins and through the heart. Sodium Parasites isolated from fish sampled at eight citrate was used as an anticoagulant. cage facilities are shown in Table 1.
Table 1. Parasites in cage reared fish in the Adriatic Sea
Mean Mean Parasite Host Parasitic form Host status Infection site Facility prevalence abundance (%) MASTIGOPHORA Amyloodinium ocellatum sea bass trophont no signs gill 1, 2, 4-7 30.84 0.38 sea bream trophont no signs gill 1, 2, 4-6 74.67 1.05 sharpsnout trophont no signs gill 1, 4 73.57 1.13 bream red sea bream trophont no signs gill 3 20 0.2 CILIOPHORA Cryptocaryion irritans sea bass teront no signs gill 2 13.33 0.13 sea bream teront no signs gill 2 60 1.8 Trichodina sp. sea bream adult no signs gill 5 10 0.1 MYXOZOA Ceratomyxa sparusaurati sea bass spore, disporoblast no signs gall bladder 2 6.66 0.33 sea bream spore, disporoblast no signs gall bladder 1, 4 14.55 0.48 sharpsnout spore, disporoblast no signs gall bladder 1 30 0.9 bream red sea bream spore, disporoblast no signs gall bladder 3 21.55 0.49 C. thunni tuna spore, disporoblast no signs gall bladder 8 23.33 1.9 intestine, gall Sphaerospora dicentrarchi sea bass spore, disporoblast no signs 1-7 54.13 1.04 bladder Polysporoplasma sparis sea bass spore, disporoblast no signs kidney 6, 7 33.93 0.68 sea bream spore, disporoblast no signs kidney 1, 2, 4, 5 42.02 0.76 sharpsnout spore, disporoblast no signs kidney 1 20 0.6 bream sharpsnout Myxobolus sp. spore, disporoblast no signs intestine 1 10 0.1 bream 26 ACTA ADRIATICA, 47(1): 23-28, 2006
Table 1. Cont’d Mean Mean Parasite Host Parasitic form Host status Infection site Facility prevalence abundance (%) MONOGENEA Diplectanum aequans sea bass adult, eggs gill necrosis gill 1-7 62.03 2.07 Lamellodiscus elegans sea bream adult, eggs no signs gill 1-5 40.06 0.97 sharpsnout adult, eggs no signs gill 1, 3, 4 97.62 29.01 bream Sparicotyle chrisophrii sea bream adult, eggs no signs gill 1-3, 5 33.9 0.46 sharpsnout adult, eggs no signs gill 1, 4, 5 32.21 1.09 bream DIGENEA gill, heart, Cardicola forsteri tuna eggs inflammation 8 63.34 14 kidney Coeliodidymocystis among tuna encysted adult no signs 8 63.16 3.79 abdominalis pyloric ceca Didymocystis wedli tuna encysted adult no signs gill 8 73.68 13.26 Platocystis alalongae tuna encysted adult no signs skin 8 21.05 0.95 Koellikerioides stomach tuna encysted adult no signs 8 21.05 0.32 internogastricus layers K. apicalis tuna encysted adult no signs cartilage 8 73.68 6.79 intestinal K. intestinalis tuna encysted adult no signs 8 57.89 12.47 mucosa NEMATODA Hysterothylacium aduncum red sea bream third stage larvae no signs submesentery 1 12.5 0.11 Anisakis simplex tuna third stage larvae no signs submesentery 8 11.5 0.15 pyloric ceca Oncophora melanocephala tuna adult hemorrhages 8 57.89 1.74 mucosa CESTODA stomach Hepatoxylon trichiuri tuna plerocercoid hemorrhages 8 12.4 0.12 mucosa COPEPODA Caligus minimus tuna adult no signs gill 1 8.57 0.09 ISOPODA Ceratothoa oestroides sea bream adult emaciation buccal cavity 2.4 8.89 0.15 adult emaciation buccal cavity 2 30.24 0.41
DISCUSSION AND CONCLUSIONS reared in the Adriatic Sea, ŠARUŠIĆ (1990) reports only four pathogens: Trichodina sp., There are a number of excellent and detailed Amyloodinium ocellatum, D. aequans, and reviews of parasites in cultured and feral Caligus minimus, noting that A. ocellatum is the fish (CHRISTOFILOGIANNIS, 1992; RODGERS & most pathogenic, especially for sea bass larvae FURONES, 1998; LE BRETON, 1999; SCHOLZ, 1999; in which mortality can reach 90%. PAPERNA & MUNDAY et al., 2003). The parasitofauna of reared fish differs in different regions and a complete BAUDIN LAURENCIN (1979) reported a similar review of data from the Adriatic are lacking. composition of parasitofauna in French facilities In our study, in sea bass, the monogenean with the addition of Colponema sp. in sea bass Diplectanum aequans was the most prevalent gills that was not reported in the Adriatic review. and most abundant parasite; Sphaerospora Their report of Myxidium sp. in sea bass is dicentrarchii was second. The parasite with interesting as it, together with the occurrence of the lowest prevalence was Ceratomyxa sp. this species in the Adriatic sharpsnout bream, is In the first review of diseases of sea bass very rare. Wild populations have a much greater MLADINEO: Parasites of Adriatic cage reared fish 27 parasitofaunal richness than reared sea bass. Red sea bream is reared at only two of the The most common species are the same as in monitored facilities. Its parasitofauna comprised rearing systems: D. aequans and S. dicentrarchii the major parasites found in the other two (SANTOS, 1993). sampled sparids, i.e., A. ocellatum and C. In the Adriatic sea bream, the most prevalent sparusaurati, and Hysterothylacium aduncum species was A. ocellatum and the most abundant which is ubiquitous in wild populations. was Cryptocaryion irritans. The species with the In Adriatic conditions there is evidence of lowest prevalence was Trichodina sp. PAPERNA & host switching and exchange of parasites between BAUDIN LAURENCIN (1979) reported finding only sparid hosts (sea bream, sharpsnout bream, and Trichodina, A. ocellatum, and Colponema sp. in red sea bream; MLADINEO & MARŠIĆ-LUČIĆ, specimens from France, roughly corresponding 2006). The majority of parasites present in sea to the gill parasitofauna of Adriatic fish. A much bream can be found in sharpsnout bream with greater number of parasite species was isolated different prevalence or abundance values. These from sea bream in a range of culture systems species are never maintained in monoculture in Spain (ALVAREZ-PELLITERO et al., 1995), and so the passage of the parasites is eased by high the report differs from the Adriatic only by stock density of mixed species. the presence of coccidian (Eimeria sp.) and Sampled tuna were host to a group of myxosporidian species (Leptotheca sp.). Didymocystis parasites, reported for the first In sharpsnout bream, the monogenean time in the Adriatic Sea, and a newly isolated Lamellodiscus elegans was the most prevalent myxosporidian (MLADINEO & BOČINA, 2006). and abundant parasite and Caligus minimus Although Didymocystis has high prevalence was the least. After increases in sharpsnout and abundance values, no gross pathological bream production in the Adriatic during the changes were noticed. The only potential threat past decade, there are now only two farms that is infection with Oncophora melanocephala sp. maintain sharpsnout bream rearing systems. The In conclusion, sea bass parasitofauna in main reason for this decline was the devastation the Adriatic is similar to earlier reports while of most stocks by an E. leei (Myxozoa) sparid parasitofauna differs in the diversity of infection, but a second reason was the low myxosporidians and the presence of coccidian appreciation and value of sharpsnout bream on species. Tuna parasitofauna is unique in the the Croatian market. Most sharpsnout bream are diversity of digenean species, characteristic produced in Greece and reports list only two of populations where the food web makes myxosporidia (Myxidium leei, Ceratomyxa sp.), possible the accumulation of a large number of a coccidian (Eimeria sp.), and two monogeneans intermediate hosts, a situation that does not exist (Lamellodiscus sp., Sparicotyle sp.) as regular amongst hatchery-raised fish. Research into tuna parasitofauna (COMPANY et al., 1999). However, diseases is young and developing. Therefore, the total parasite load is greater in Adriatic there are no earlier and appropriate studies sharpsnout bream than in the other sampled carried out in the Mediterranean with which the species, except for tuna. results of the current study can be compared.
REFERENCES
ALVAREZ-PELLITERO, P., A. SITJÀ-BOBADILLA, in marine aquaculture systems in Greece. J. A. FRANCO-SIERRA & O. PALENZUELA. 1995. Fish Dis., 27: 215-218. Protozoan parasites of gilthead sea bream, CHRISTOFILOGIANNIS, P. 1992. The veterinary Sparus aurata L., from different culture approach to sea-bass and sea-bream. In: systems in Spain. J. Fish Dis., 18: 105-115. Aquaculture for Veterinarians. L. Brown ATHANASSOPOULOU, F., T. PRAPAS & H. RODGER. (Editor). Pergamon Press, Oxford, pp. 379- 1999. Diseases of Puntazzo puntazzo Cuvier 395. 28 ACTA ADRIATICA, 47(1): 23-28, 2006
COMPANY, R., A. SITJÀ-BOBADILLA, M.J. PUJALTE, MUNDAY, B.L., Y. SAWADA, T. CRIBB & C.J. P. ALVAREZ-PELLITERO & J. PÉREZ-SÁNCHEZ. HAYWARD. 2003. Diseases of tunas, Thunnus 1999. Bacterial and parasitic pathogens in spp. J. Fish Dis., 26: 187-206. cultured common dentex, Dentex dentex L. PAPERNA, I. & F. BAUDIN LAURENCIN. 1979. J. Fish Dis., 22: 299-309. Parasitic infections of sea bass, Dicentrarchus LE BRETON, A.D. 1999. Mediterranean finfish labrax, and gilthead sea bream, Sparus pathologies: present status and new aurata, in mariculture facilities in France. developments in prophylactic methods. Aquaculture, 16: 173-175. Bull. Eur. Assoc. Fish Pathol., 19:250-253. RODGERS, C.J. & M.D. FURONES. 1998. Disease LOM, J. & J.R. ARTHUR. 1989. A guideline for problems in cultured marine fish in the the preparation of species descriptions in Mediterranean. Fish Pathol., 33:157-164. Myxosporea. J. Fish Dis. 12: 151-156. SANTOS, M.J. 1994. Observations on the MLADINEO, I. & I. BOČINA. 2006. First report of parasitofauna of wild sea bass (Dicentrarchus Ceratomyxa thunni sp. nov. from northern labrax L.) from Portugal. Bull. Eur. Assoc. bluefin tuna Thunnus thynnus. Zootaxa. (in Fish Pathol., 16(3):77-79. press). ŠARUŠIĆ, G. 1990. Bolesti lubina (Dicentrarchus MLADINEO, I. & J. MARŠIĆ-LUČIĆ. 2006. Host labrax L.) u uvjetima intenzivnog uzgoja switching of Lamellodiscus elegans (Diseases of the cage reared sea bass (Monogenea: Monopisthocotylea) and (Dicentrarchus labrax L.)). Vet. Stanica, Sparicotyle chrysophrii (Monogenea: 21:159-164. Polypisthocotylea) between cage reared SCHOLZ, T. 1999. Parasites in cultured and feral sparids. Vet. Res. Comm. (in press). fish. Vet. Parasitol., 84:317-335.
Received: 21 December 2005 Accepted: 13 March 2006
Nametnici na kavezno uzgojenoj ribi u Jadranu
Ivona MLADINEO
Institut za oceanografiju i ribarstvo, P.P. 500, 21 000 Split, Hrvatska e-mail: [email protected]
SAŽETAK
Brzim razvojem marikulture na Mediteranu, pojavile su se brojne bolesti uzrokovane nametnicima na kavezno uzgojenoj ribi. U ograničenim uzgojnim uvjetima, bolesti mogu prouzročiti mortalitet i ekonomske gubitke zbog usporenog rasta. Uvođenjem novih proizvoda u marikulturi, te novih ribljih vrsta u uzgojnom sistemu, novi nametnički patogeni su pronašli svoj put u novim okružjima adaptirajući se i kolonizirajući tako novo uzgojene vrste (pretežito lubina i arbuna) ili su povećali rasprostranjenost nametnika na novo uvedenim vrstama u uzgoju. Parazitofauna uzgojene ribe je osiromašena sa stanovišta bogatstva vrsta i ima veće populacijske vrijednosti nego parazitofauna divlje ribe. Iako je parazitofauna uzgojene ribe u Mediteranu istraživana u brojnim publikacijama, tek povremeni nalazi se odnose na Jadransko more. Populacija divlje ribe u Jadanskom moru je bila uzorkovana za izolaciju i identifikaciju nametnika, ali pregled parazitofaune uzgojene ribe do sada nije objavljen. Ovo je bio glavni cilj istraživanja.
Ključne riječi: lubin, komarča, parazitofauna, Jadransko more ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.33 AADRAY 47 (1): 29 - 36, 2006 Original scientific paper
Biological observations on the nursehound, Scyliorhinus stellaris (Linnaeus, 1758) (Chondrichthyes: Scyliorhinidae) in captivity
Christian CAPAPÉ1*, Yvan VERGNE1, Régis VIANET2, Olivier GUÉLORGET1, and Jean-Pierre QUIGNARD1
1 Laboratoire d’Ichtyologie, Case 104, Université Montpellier II, Sciences et Techniques du Languedoc, 34095 Montpellier Cedex 05, France
2 Parc Naturel Régional de Camargue, Mas du Pont de Rousty, 13200 Arles, France
* Corresponding author, e-mail: [email protected]
Observations conducted over two years on nursehounds, Scyliorhinus stellaris, in captivity provided data on the number of eggs laid per year, embryonic development, size at hatching, length growth following hatching, and estimated fecundity.
Key words: Scyliorhinidae, Scyliorhinus stellaris, eggs, hatching, length growth, captivity
INTRODUCTION marine areas it inhabits (QUÉRO, 1984). Informa- tion was provided about the spawning period The small-spotted catshark, Scyliorhinus for specimens from Plymouth in the British canicula (Linnaeus, 1758), was the focus of Isles (GARSTAND, 1893-1895; FORD, 1921), the several articles concerning free-swimming Adriatic Sea (SYRSKI, 1876; GRAEFFE, 1888), (FORD, 1921; LELOUP & OLIVEREAU, 1951; and off Naples in southern Italy (LO BIANCO, MELLINGER, 1962ab, 1964; CAPAPÉ, 1977; CRAIK, 1909; MASCHLANKA, 1955). In the Adriatic Sea, 1978; CAPAPÉ et al., 1991; ELLIS & SHACKLEY, JARDAS (1979) noted that S. stellaris is found in 1997) and captive specimens (MELLINGER, 1989, shallow coastal waters at depths up to 60 m, 1994; HOUZIAUX & VOSS, 1997; DOMI et al., 2000). while GRUBIŠIĆ (1982) reported its occurrence In contrast, its close relative, the nurse- throughout the area at depths of 40-100 m, and hound, Scyliorhinus stellaris (Linnaeus, 1758), rarely over 200 m. Aspects of the reproductive is lesser known, probably due to its scarcity; biology of the nursehound were reported by the species is not abundantly caught in the ŽUPANOVIĆ (1961ab) for the middle Adriatic, 30 ACTA ADRIATICA, 47(1): 29-36, 2006
BINI (1967) for the Italian Seas, CAPAPÉ (1977) suspended or deposited on a grating. Water for the Tunisian coast, and CAPAPÉ et al. (2000) temperature ranged 15-25.5°C. Salinity was for the Languedoc coast of southern France. maintained at 32 psu. The hatching period was reported by MOREAU (1881), EHREBAUM (1927), and CAPAPÉ (1974a) Tank 4 while MELLINGER & WRISEZ (1989) described Soon after hatching, the neonates were moved embryonic development and MELLINGER et al. to Tank 4, also 60 liters. Water temperature (1989) compared lipid contents in eggs and neonates. SKARAMUCA & PRTENJAČA (1985) varied 16-21°C. Four to five days after hatching, described the first stages of development in the neonates were fed small pellets, 3-5 mm newly hatched specimens in tanks in diameter, made of crushed teleost pieces. Observations conducted on captive nurse- The pellets were quickly consumed by the hounds during two years allow us to report on neonates from the first days. The pellets were eggs, hatching, and first growth stages. progressively enlarged as the size of the neonates increased. When the neonates reached 300 mm TL, they were fed pieces of teleosts as were the MATERIAL AND METHODS adults. Observations were carried out in four tanks at the aquarium of La Grande Motte, 20 km east of Montpellier in southern France. The RESULTS first tank contained mature specimens (Tank 1), two others contained eggs (Tanks 2 and 3), Copulatory behavior and a fourth, neonates (Tank 4). The tanks were No copulatory or pre-copulatory behavior supplied with water drawn directly from the sea (DOMI et al., 2000) was observed during daytime. at a flow of 150 l/h. The tanks were illuminated Adults rested on the sandy substrate throughout with fluorescent tubes (36 watts, each), from the illuminated period. At the end of the afternoon, 10:00 to 18:00 hrs in October-April and from they began to move and pre-copulatory behavior 10:00 to 23:00 hrs in May-September. The total was observed. lengths (TL) of neonates and specimens was measured to the nearest millimeter following Egg laying COMPAGNO (1984). Generally, egg laying occurred throughout Tank 1 the year except in December and January. The number of eggs produced were 27, 41, Four adult specimens were kept in a 6 m3 tank, and 31 in 1987, 1988, and 1989, respectively. together with a loggerhead sea turtle, Caretta Unfortunately, there were three females in the caretta (Linnaeus, 1758), and a stone bass, tank, so we were unable to assess the number of Polyprion americanus (Bloch and Schneider, eggs produced by each female. 1801). The specimens were fed pieces of teleosts and penaeid shrimps once a day at 17:30 hrs. Hatching Egg laying occurred February-December 1987 when the water temperature was 15-22.5°C and Only 20 of the 27 eggs placed in Tanks 2 the salinity was 28-33 psu. and 3 completed embryonic development until hatching. The length of embryonic development Tanks 2 and 3 was 9-12 months. No embryonic development The eggs were removed to two 60 liters was observed in eggs deposited directly on the tanks as soon as they were laid. The eggs were floor. CAPAPÉ, VERGNE, VIANET, GUÉLORGET & QUINGARD: Biological observations on the nursehound 31
Growth of neonates occurred at night. This is conjuncture and remains difficult to explain. It does not agree Only six neonates survived. Dates and sizes with observations of captive S. canicula by (TL, mm) at birth are given in Table 1 and HOUZIAUX & VOSS (1997) and DOMI et al. (2000), length increases are given in Table 2. When the who described copulatory behavior occurring specimens were considered too large for the during daytime. Further, shark mating occurs tanks, they were released into the sea. in the best environmental conditions in spring Table 1. Dates and sizes at hatching of six Scyliorhinus or early summer when adult males and females stellaris specimens generally approach the coast (MUÑOZ-CHAPULI, Date Size at hatching 1984; CAPAPÉ et al., 2003, 2004; BRADAÏ et al., 2005), (TL, mm) however, to our knowledge, these authors did not mention whether copulatory behavior takes 17 April 1988 110 place during daytime or at night. 19 August 1988 106 The sample of HOUZIAUX & VOSS (1997) was 27 September 1988 110 larger than ours and contained thirty captive S. canicula. The sex ratio was the same in 06 October 1988 105 both samples: one male to three females. The 08 October 1988 110 presence of a single male in our sample prevented 28 October 1988 106 male competition. This suggests that copulatory behavior depends on the number of males in the DISCUSSION small-spotted catshark. The number of eggs produced each year The absence of mating behavior during by a single female could not be determined. the illuminated period and the pre-copulatory If each female produced the same number of behavior at late afternoon suggest that mating eggs per year, then each produced 9-13. If
Table 2. Total length (mm) following hatching and periodically measured in six specimens
Date 123456 (Day, Mo, Yr) 17/05/1988 110 17/06/1988 190 17/07/1988 210 17/08/1988 220 17/09/1988 240 160 17/10/1988 250 180 165 115 120 17/11/1988 255 190 170 130 140 120 19/12/1988 260 220 215 160 210 140 19/01/1989 265 230 220 170 215 200 09/ 02/1989 280 240 230 180 220 210 17/06/1989 320 310 305 300 295 295 12/08/1989 370 350 320 310 300 305 26/09/1990 530 520 460 480 470 500 32 ACTA ADRIATICA, 47(1): 29-36, 2006
Table 3. Linear growth of six specimens versus duration of captivity Specimens Captivity in Initial Final TL (mm) Growth days TL (mm) (TL, mm) 1 899 110 530 420 2 772 106 520 414 3 729 110 460 350 4 720 105 480 375 5 718 110 470 350 6 706 106 500 394 only one female produced eggs, the number After 60 days, the mean length of the Adriatic ranged 27-41. Consequently, the number of specimens was 188.5 mm for females and 184.5 eggs annually produced by the female(s) in mm for males (SKARAMUCA & PRTENJAČA, 1985). Tank 1 could range 9-41. Based on the number The six specimens in our study reached 170-215 of yolky oocytes ready to be ovulated in mature mm (mean 192.5 mm) after 60 days, similar females caught off the Tunisian coast, CAPAPÉ to results of SKARAMUCA & PRTENJAČA (1985). (1977) determined that 77-109 eggs per year (Table 3). Nevertheless, intraspecific differences could be produced. However, in both oviparous related to area cannot be excluded, especially in (CAPAPÉ, 1974b, 1977) and viviparous (CAPAPÉ et regard to scyliorhinids (LELOUP & OLIVEREAU, al., 2003, 2004; SAÏDI et al., 2005) elasmobranchs, 1951). The six specimens were kept in Tank 4 some yolky oocytes are not ovulated and enter for 706-899 days during which they increased atresia. Therefore, CAPAPÉ (1977) probably by 375-420 mm with a daily increment of 0.46- overestimated the fecundity of S. stellaris in the 0.56 mm. The specimens remained juveniles. natural environment. Captivity can influence Sexual maturity occurs at 770-790 mm TL in S. elasmobranch fecundity. For example, free- stellaris from the Tunisian coast (CAPAPÉ, 1977) swimming pelagic stingrays, Dasyatis violacea and the Languedoc coast (CAPAPÉ et al., 2000). (HEMIDA et al., 2003) were slightly more prolific Consequently, if the growth rate in S. stellaris than specimens maintained in tanks (MOLLET et is constant and does not differ significantly al., 2002). between populations, sexual maturity would Hatching ranged 10-12 months, in agreement be reached at the age of four years (BOUGIS, with MOREAU (1881) and EHRENBAUM (1927) 1989), however this hypothesis needs further for S. stellaris from the Atlantic and North investigation. Seas, respectively. Only two of ten eggs from Although the hydrobiological parameters in Salammbô (Tunisia) suspended in tanks at the our study probably differed from those in the Institut National des Sciences et Technologies natural environment, our work shows that the de la Mer (INSTM) produced neonates of 107 nursehound could be a good biological model and 108 mm TL, respectively, after hatching for ethobiological study. As in the case of its periods of 198 and 201 days, or seven months, relative, the small-spotted catshark, it appears slightly less than observations cited above that acclimatization of nursehounds in tanks is (CAPAPÉ, 1974a). Neonates from the Adriatic possible by providing appropriate conditions. were larger at hatching, 13.0-16.3 mm (mean 14.6 mm; SKARAMUCA & PRTENJAČA, 1985). This difference may be due to the fact that the ACKNOWLEDGEMENTS embryos at La Grande Motte and Salammbô developed in egg capsules deposited in the tanks The authors thank two anonymous referees while embryos in the Adriatic developed in the for useful and helpful comments on the natural environment. manuscript. CAPAPÉ, VERGNE, VIANET, GUÉLORGET & QUINGARD: Biological observations on the nursehound 33
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de deux Sélaciens ovipares, les roussettes Nielsen and E. Tortonese. (Editors). Fishes Scyliorhinus canicula et Scyliorhinus of the North-western Atlantic and the stellaris. Evolution de la matière sèche, Mediterranean, Vol. I. UNESCO, Paris, pp. de l’eau et des ions (Cl-, Na+, K+) dans 95-100. le vitellus de S. canicula au cours du SAÏDI, B., M.N. BRADAÏ, A. BOUAÏN, O. GUÉLORGET développement (Compared biology and & C. CAPAPÉ. 2005. Reproductive biology of physiology of development in two oviparous the sandbar shark, Carcharhinus plumbeus selachians. Dry matter, water and ions (Cl-, (Chondrichthyes: Carcharhinidae) from the Na+, K+) in vitellus of S. canicula during Gulf of Gabès (southern Tunisia, central development). Bull. Soc. Zool. France, Mediterranean). Acta. Adriat., 46(1):47-62. 114:51-62. SKARAMUCA, B. & I. PRTENJAČA, 1985. A MELLINGER, J., F. WRISEZ, C. LERAY & B. HAYE, contribution to the study of biological and 1989. A comparison of egg and newborn lipids ecological characteristics of the catfish in the oviparous dogfishes, Scyliorhinus (Scyliorhinus stellaris L, 1758). Biol. Notes, canicula and S. stellaris (Chondrichthyes). 65:1-8. Preliminary data. Biol. Struct. Morpho., SYRSKI, S. 1876. Riguardo al Tempo della Frega 2:44. dei Animali Esistenti nel Mare Adriatico MOLLET, H.F., J.M. EZCURRA & J.B. O’ SULLIVAN. (Observations of mating period in animals 2002. Captive biology of the pelagic stingray, occurring in the Adriatic Sea). Trieste, 165 Dasyatis violacea (Bonaparte, 1832). Mar. pp. Freshwater Res., 53:531-541. ŽUPANOVIĆ, S. 1961a. Analyse quantitative- MOREAU, E. 1881. Histoire Naturelle des Poissons qualitative des populations de poissons de la France (Life history of fishes from des canaux de l’Adriatique moyenne France).Vol. 1. Masson, Paris. 478 pp. (Quantitative-qualitative analysis of fish MUÑOZ-CHAPULI, R. 1984. Ethologie de la populations from channels of the middle reproduction chez quelques requins de Adriatic). Acta Adriat., 9(3):1-151. l’Atlantique-Nord (Ethology of reproduction ŽUPANOVIĆ, S. 1961b. Contribution à la in some sharks from North-Atlantic). connaissance de la biologie des poissons de Cybium, 8(4):1-14. l’Adriatique (Contribution to the knowledge QUÉRO, J.C. 1984. Scyliorhinidae. In: J.P. of the biology of the fishes from the Adriatic). Whitehead, M.L. Bauchot, J.C. Hureau, J. Acta. Adriat., 9(4):1-84.
Received: 14 July 2005 Accepted: 14 March 2006 36 ACTA ADRIATICA, 47(1): 29-36, 2006
Biološka zapažanja na mački mrkulji, Scyliorhinus stellaris (Linnaeus, 1758) (Chondrichthyes: Scyliorhinidae) u kaptivitetu
Christian CAPAPÉ1*, Yvan VERGNE1, Régis VIANET2, Olivier GUÉLORGET1, i Jean-Pierre QUIGNARD1
1 Laboratorij za ihtiologiju, P.P. 104, Sveučilište u Montpellier-u II, Znanost i tehnika Languedoc- a, 34095 Montpellier cedex 05, Francuska
2 Regionalni prirodni park Camargne, Mas du Pont Rousty, 13200, Arles, Francuska
*e-mail: [email protected]
SAŽETAK
Preko dvije godine su vršena opažanja na mački mrkulji Scyliorhinus stellaris u kaptivitetu. Dobiveni su podaci o godišnje izleglom broju jaja, embrionalnom razvoju, veličini kod leženja, rastu dužine nakon leženja i procjeni plodnosti.
Ključne riječi: Scyliorhinidae, Scyliorhinus stellaris, jaja, leženje, porast dužine, kaptivitet ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.33:591.156 591.156:597.33 AADRAY 47 (1): 37 - 47, 2006 Original scientific paper
Sexual dimorphism in the head, mouth, and body morphology of the smallspotted catshark, Scyliorhinus canicula (Linnaeus, 1758) (Chondrichthyes: Scyliorhinidae) from Turkey
Halit FİLİZ and Ertan TAŞKAVAK*
Ege University, Faculty of Fisheries, Department of Basic Sciences, 35100 İzmir, Turkey *Corresponding author, e-mail: [email protected]
Males of the smallspotted catshark, Scyliorhinus canicula, have a longer and narrower mouth than females, resulting in pronounced sexual dimorphism. The length/width ratio of the mouth is 0.55 in males and 0.50 in females. Other head measurements also significantly differ between the sexes, i.e., the snout-spiracle and snout-pectoral distances. Body measurements that differ between the sexes include pelvic to anal, pectoral inner edge, pelvic to median tip, upper caudal, and total body lengths. Reasons for these differences are discussed.
Key words: Scyliorhinus canicula, Elasmobranchii, sexual dimorphism, meristic, nanism
INTRODUCTION JARDAS, 1979; CIHANGIR et al., 1997), age and growth (RODRIGUEZ-CABELLO et. al., 1997; RODRI- The smallspotted catshark, Scyliorhinus GUEZ-CABELLO & SÁNCHEZ, 2002), reproduction canicula Linnaeus, 1758 (Family: Scylio rhi- (HARRIS, 1952; CRAIK, 1978; SUMPTER & DODD, nidae), is an Atlantic-Mediterranean demersal 1979; MELLINGER, 1983; ELLIS & SHACKLEY, 1997; species that inhabits continental shelves and RODRIGUEZ-CABELLO et. al., 1998), and feeding uppermost slopes. It is found on sandy, coralline, (MACPHERSON et al., 1989; ELLIS et al., 1996; SIMS algal, gravel, or muddy bottoms at depths of 3- et al., 1996; OLASO et al., 1998, 2002; KABASAKAL, 400 m (HUREAU & MONOD, 1973; CAPAPÉ, 1977; 2001, 2002; VELASCO et al., 2001). JARDAS, 1979; WHITEHEAD et al., 1984; FROESE Differences in the selective pressures & PAULY, 2004). The species is common in the experienced by the sexes can result in the Mediterranean (CAPAPÉ, 1977; JARDAS, 1979; evolution of sexual dimorphism of morphological CIHANGIR et al., 1997; BERTRAND et al., 2000; BAINO traits (CASSELMAN & SCHULTE-HOSTEDDE, 2004). & SERENA, 2000; DE MADDALENA & BAENSCH, Sexual dimorphism with respect to body size 2005) and widespread in the northeast Atlantic is common among shark species in which the (WHITEHEAD et al., 1984). females are viviparous or ovoviviparous (SIMS, Studies of the lesser spotted dogfish relate 2003). ELLIS & SHACKLEY (1995) and ERDOGAN et to biology (FAURE-FREMIET, 1942; CAPAPÉ, 1977; 38 ACTA ADRIATICA, 47(1): 37-47, 2006
al. (2004) demonstrated that sexual dimorphism onset of maturity (BROUGH, 1937). Morphometric can also occur in oviparous sharks such as S. studies of S. canicula from the Mediterranean canicula. have shown negative allometric growth of the Morphological and dental differences are head (BAS, 1964) and that males have longer useful criteria for identifying the taxonomy heads than females (JARDAS, 1979; ERDOGAN et of elasmobranch fish (ELLIS & SHACKLEY, al., 2004). 1995). However, intraspecific variations due to The purpose of the present study was to growth, sexual dimorphism, and geographical determine the extent of sexual variation in the and individual differences have been little morphometrics of S. canicula and to assess studied (STEFFENS & D’AUBREY, 1967; TANIUCHI, possible functional significance. 1970; BASS, 1973; SIQUEIROS-BELTRONES, l990; KAJIURA & TRICAS, 1996; KAJIURA, 2001). In S. canicula, the head and mouth are narrower and MATERIAL AND METHODS the intermandibular separation is smaller in We collected 296 S. canicula specimens males than in females (BROUGH, 1937). Changes from the Foca trawl area in Izmir Bay (Aegean in the lower jaw structure correlate with sexual Sea, Turkey) in September and November 2002 maturity and these sexually dimorphic characters at depths of 40-120 m with two commercial are more pronounced during the breeding season bottom trawls (Fig. 1). The sex, total length and not present in sexually immature specimens (TL), mouth length (ML), and mouth width (BROUGH, 1937). Sexual dimorphism in the (MW) of the 123 females and 173 males length/width ratio of the mouth of S. canicula were measured to the nearest millimeter. All was briefly described by ARTHUR (1950). Sexual measurements were converted to percentages of dimorphism occurs relatively suddenly at the the total length (%TL) and analyzed following
Fig. 1. Collection sites of smallspotted catshark, Scyliorhinus canicula, specimens FİLİZ & TAŞKAVAK: Sexual dimorphism of smallspotted catshark from Turkey 39 the methodology of ELLIS & SHACKLEY (1995). groups within each sex, and between the same Significant differences between the sexes in TL groups of both sexes. mean ML/TL, MW/TL, and ML/MW were In addition, eight measurements of the calculated by t test (SOKHAL & ROHLF, 1981). The head region and seventeen measurements of data were divided into six groups according to the body were taken to the nearest millimeter TL (<275, 275-324, 325-374, 375-424, 425- and converted to %TL for statistical analysis as 474, >474 mm) and similar tests were used to above (Fig. 2; BASS et al., 1975). determine significant differences between TL
Fig. 2. Some of the measurements taken in the present study. Aa: snout to nostrils; Ab: snout to mouth; Ag: snout to pelvic; Aj: snout to lower caudal lobe; F: pectoral to pelvic; ML: mouth length; MW: mouth width; Na: pectoral base; Nb: pectoral inner edge; Nc: pectoral length; Oa: pelvic to lateral lobe; Ob: pelvic to median tip; Pa: upper caudal; Pc: lower caudal (according to BASS et al., 1975) 40 ACTA ADRIATICA, 47(1): 37-47, 2006
RESULTS significantly decreased for females and increased for males after length group 4 (375-424 mm; The mouth was significantly longer (4.02 Fig. 3). In group 4, ML significantly differed vs 3.75%TL; p<0.000l) and narrower (7.42 vs between sexes but MW and ML/MW did not. 7.51%TL; p<0.0001) in males than in females, In group 5 (425-474 mm), ML and ML/MW resulting in significantly different ML/MW ratios significantly differed between sexes. In group (0.55 for males and 0.50 for females; p<0.000l; 6 (>474 mm), all three variables significantly Table 1). ML/MW was almost constant in the differed (Table 2). three smallest length groups for both sexes, then
Table 1. Differences between male and female smallspotted catshark, Scyliorhinus canicula, specimens in mouth length (ML), mouth width (MW), and ratio of mouth length to width (ML/MW), expressed as percentages of total length, means± SD, with ranges in parentheses Males Females TL group n ML MW ML/MW n ML MW ML/MW (mm) <275 15 3.85±0.59 8.16±1.91 0.49±0.12 16 3.69±0.42 7.60±1.11 0.49±0.07 (3.11-5.60) (5.83-14.20) (0.25-0.74) (2.78-4.48) (4.63-9.85) (0.38-0.63) 275-324 26 3.81±0.39 7.50±0.57 0.51±0.07 29 3.84±0.69 7.59±0.73 0.51±0.09 (2.97-4.55) (6.67-9.02) (0.34-0.65) (2.67-5.97) (5.87-9.09) (0.36-0.85) 325-374 35 3.84±0.37 7.51±0.59 0.51±0.06 28 3.75±0.38 7.51±0.83 0.51±0.07 (3.22-4.86) (5.48-8.49) (0.40-0.65) (3.06-4.51 (5.03-8.82) (0.36-0.70) 375-424 30 4.19±0.65 7.50±1.12 0.57±0.11 21 3.85±0.38 7.25±0.76 0.53±0.05 (3.21-6.31) (5.98-12.59) (0.32-0.90) (3.05-4.45) (5.94-8.32) (0.44-0.67) 425-474 46 4.17±0.48 7.30±0.49 0.57±0.06 20 3.68±0.38 7.42±0.64 0.50±0.05 (3.32-6.24) (6.28-8.94) (0.44-0.84) (3.12-4.42) (6.17-8.37) (0.39-0.63) >474 21 4.12±0.32 6.80±0.65 0.61±0.07 9 3.59±0.37 7.85±0.48 0.46±0.05 (3.59-4.84) (5.46-7.80) (0.49-0.77) (3.04-4.17) (6.84-8.42) (0.41-0.55) Total 173 4.02±0.50 7.42±0.92 0.55±0.09 123 3.75±0.47 7.51±0.79 0.50±0.07 (2.97-6.31) (5.46-14.20) (0.25-0.90) (2.67-5.97) (4.63-9.85) (0.36-0.85)
Fig.3. Relationship between mean ratio of mouth length to mouth width (ML/MW; ± SD) and size group in (A) female and (B) male Scyliorhinus canicula. Size groups are 1: <275 mm, 2: 275-324 mm, 3: 325-374 mm, 4: 375-424 mm, 5: 425-474 mm, 6: >474 mm FİLİZ & TAŞKAVAK: Sexual dimorphism of smallspotted catshark from Turkey 41
Table 2. Probability values showing statistical differences groups 1-3 significantly differed from the ML of between mouth length (ML), mouth width (MW) and ML/MW between male and female Scyliorhinus of males in groups 4-6 (p<0.005) while the MW canicula of different size groups (measurements of males in group 1 significantly differed from converted to percentages of total length) the MW of the other five groups (p<0.005). In females, ML and MW changed very little. Size group ML MW ML/MW ML and MW positively correlated with TL <275 mm 0.382 0.317 0.975 in both males and females (Fig. 4). The linear 275-324 mm 0.880 0.628 0.850 relationships are described by the following 325-374 mm 0.317 0.992 0.573 equations. For females: ML = 0.035TL + 0.738 375-424 mm 0.033* 0.374 0.175 (r2 = 71.99, n = 123) and MW = 0.074TL + 425-474 mm 0.001* 0.403 0.000* 0.452 (r2 = 79.26, n = 123). For males: ML = 2 >474 mm 0.000* 0.001* 0.000* 0.047TL – 2.505 (r = 76.99, n = 173) and MW = 0.060TL + 5.174 (r2 = 67.28, n = 173). Total 0.000* 0.417 0.000*
* significantly different at p<0.05 Among the head measurements, the distances from the snout to the spiracle and from the snout to the pectoral fin were significantly greater Significant size-based differences were observed within each sex, more so for male fish. in males than in females (Table 3). The length ML/MW in males ranged 0.49-0.61 (Table 1), between the snout and the first gill-slit tended to with significant differences occurring between be shorter in females, although this difference the smallest size (group 1) and the three largest was not statistically significant (p = 0.057). Five sizes (groups 4-6; p = 0.0005, 0.0004, and other measurements (total body length, pelvic to 0.0001, respectively). This difference can be anal, pectoral inner edge, pelvic to median tip, attributed to an increase in the ML and decrease upper caudal) significantly differed between in MW as the males grew. The ML of males in males and females (Table 4).
Fig.4. Relationships between (A) mouth length and total length and (B) mouth width and total length for male and female Scyliorhinus canicula 42 ACTA ADRIATICA, 47(1): 37-47, 2006
Table 3. Comparison between males (n = 173) and females (n = 123) of eight measurements in the head region, values are converted to percentages of total length, means± SD, with ranges in parentheses
Measurement Male Female p Snout to nostrils (Aa) 2.44±0.39 2.46±0.40 0.653 (1.79-3.73) (1.70-4.71) Snout to mouth (Ab) 3.91±0.37 3.96±0.37 0.298 (2.33-5.48) (2.54-5.16) Snout to eye (Ac) 5.68±0.50 5.60±0.56 0.113 (3.15-7.80) (3.28-7.19) Snout to first gill-slit (Ad) 12.48±0.89 12.25±1.18 0.057 (10.17-18.40) (9.94-21.82) Snout to pectoral (Ae) 16.55±1.47 16.20±1.13 0.026* (7.39-24.00) (13.70-20.06) Snout to spiracle (As) 9.50±0.55 9.33±0.83 0.037* (7.22-13.40) (3.92-11.11) Eye diameter (B) 3.68±0.75 3.65±0.65 0.744 (0.96-6.58) (2.18-5.24) Spiracle length (S) 0.85±0.15 0.84±0.17 0.824 (0.53-1.40) (0.42-1.48) * significantly different at p<0.05
Table 4. Comparison between males (n = 173) and females (n = 123) of eighteen body measurements, values are converted to percentages of total length, means± SD, with ranges in parentheses
Measurement Males Females p Total length (TL) 385.83±73.70 357.89±72.59 0.001* (210.00-525.00) (210.00-508.00) Snout to first dorsal (Af) 49.51±2.14 49.32±3.10 0.533 (45.46-70.00) (45.20-76.27) Snout to pelvic (Ag) 39.29±2.08 39.81±3.02 0.083 (27.65-56.00) (35.00-58.68) Standard length (Ah) 79.90±3.64 79.54±2.02 0.311 (68.66-114.00) (76.09-93.14) Snout to lower caudal lobe (Aj) 78.06±3.03 77.98±3.22 0.820 (68.00-110.00) (72.36-102.63) First to second dorsal (D) 18.20±1.19 18.14±1.01 0.648 (15.09-26.80) (14.88-21.57) Between dorsal bases (E) 12.78±1.05 12.90±0.99 0.338 (10.50-19.20) (10.79-17.11) Pectoral to pelvic (F) 23.54±1.73 23.79±1.46 0.193 (18.52-36.00) (20.00-27.78) Pelvic to anal (G) 19.30±1.27 18.91±1.42 0.013* (16.67-26.00) (15.24-23.26) FİLİZ & TAŞKAVAK: Sexual dimorphism of smallspotted catshark from Turkey 43
Table 4. Cont’d Measurement Males Females p Second dorsal to upper caudal 12.44±1.02 12.62±1.26 0.176 (H) (10.19-16.80) (9.36-16.67) Anal to lower caudal (I) 20.17±1.25 20.26±1.24 0.576 (16.67-29.20) (17.05-24.00) Pectoral base (Na) 5.20±0.60 5.24±0.59 0.571 (3.88-8.00) (3.68-7.46) Pectoral inner edge (Nb) 5.95±0.71 6.18±0.80 0.008* (4.00-8.22) (4.32-9.47) Pectoral length (Nc) 12.13±0.98 12.19±0.84 0.576 (9.33-15.71) (10.29-15.03) Pelvic to lateral lobe (Oa) 5.97±0.64 5.97±0.61 0.966 (4.27-8.40) (4.14-8.37) Pelvic to median tip (Ob) 12.63±1.23 10.76±0.81 0.000* (9.43-17.20) (8.24-12.67) Upper caudal (Pa) 20.49±1.43 21.11±2.06 0.003* (16.81-28.00) (17.78-34.72) Lower caudal (Pc) 9.32±1.29 9.39±1.15 0.619 (4.67-14.80) (4.12-11.63)
* significantly different at p<0.05 DISCUSSION dimorphism in ML/MW is due to the increase in mouth length and decrease in mouth width Sexual dimorphism with respect to body in males as the fish grow. If this change in size appears more common among shark morphology is related to reproductive changes, it species in which the females are viviparous or can be considered a secondary sex characteristic ovoviviparous (SIMS, 2003). Although S. canicula (ELLIS & SHACKLEY, 1995). In the present study, is oviparous, earlier studies have shown that ML/MW significantly differed between sexes such dimorphism can occur in this species also only in the larger size groups and not for fish (BROUGH, 1937; ARTHUR, 1950; BAS, 1964; JARDAS, under 425 mm. Differences in intermandibular 1979; ELLIS & SHACKLEY, 1995; ERDOGAN et al., separation have been related to sexual maturity 2004), and our findings support these studies. (BROUGH, 1937). In S. canicula, both sexes attain The ML/MW values in the present study maturity at 57-60 cm (FORD, 1921). Assessing (0.55 for males and 0.50 for females) coincide maturity by clasper length, nidamental gland with the values of 0.59 for males and 0.53 for width and weight, and appearance of gonads, females given by ARTHUR (1950) and 0.67 for ELLIS & SHACKLEY (1997) suggested that males males and 0.57 for females given by ERDOGAN et and females mature at approximately 52 and al. (2004) for S. canicula. Thus sexual dimorphism 55 cm, respectively. ELLIS & SHACKLEY (1995) in ML/MW is statistically confirmed by the suggested that the changes in mouth morphology present study. The values given by ARTHUR of male fish and subsequent sexual dimorphism (1950) and ERDOGAN et al. (2004) significantly in ML/MW are related to sexual maturity, since differ from those of ELLIS & SHACKLEY 1995; fish below 500 mm were immature, those within (0.49 for males and 0.43 for females) who 500-549 mm were maturing, and larger fish were claimed that this might be because ARTHUR mature. In Schroederichthys bivius (Smith), the (1950) had used a small sample size. Sexual ML/MW in females and juvenile males was 0.50 44 ACTA ADRIATICA, 47(1): 37-47, 2006 while in mature males it was 0.80 (GOSZTONYI, Regarding body measurements, the pelvic- 1973). anal and pelvic-median tip distances were longer Both ML and MW positively correlated with in males than in females while the pectoral inner TL in both sexes, however, the present study edge and upper caudal lengths were shorter lacks information on specimens below 210 in males. ELLIS & SHACKLEY (1995) recorded a mm and above 525. BASS (1973), who studied total body length of 586 for males and 555 mm the relationship between ML and TL, reported for females. Sexual dimorphism in total body an initial decrease and subsequent increase in length was confirmed in our study, however, the ML for larger fish in a sample of 119 male and mean values given by ELLIS & SHACKLEY (1995) female Carcharhinus leucas. ELLIS & SHACKLEY are significantly higher than those obtained in (1995) suggested that the initial decrease in ML the present study (385 for males, 357 mm for after birth was probably due to the head region females). Apparently, S. canicula are much being better developed at birth than the rest of smaller in the Aegean Sea than in the Swansea the body. and Oxwich Bays of the Bristol Channel and According to ELLIS & SHACKLEY (1995), the the Irish Sea. By studying the length range and mouth dimensions in male S. canicula change lengths at sexual maturity of S. canicula in the during maturation and males have longer teeth northern Aegean, CIHANGIR et al. (1997) suggested than females, perhaps due to differential feeding that Mediterranean dogfish grow more slowly habits or adaptations for reproductive behavior. than Atlantic dogfish and that they reach sexual The diet of S. canicula is composed primarily maturity at a smaller length. Compared to the of decapod crustaceans, mollusks, and teleosts Atlantic, Mediterranean marine communities have more species with generally smaller (FORD, 1921; LYLE, 1983) with no significant individuals (Mediterranean nanism; ZENETOS dietary differences between males and females et al., 2002). The smaller lengths observed in this in Isle of Man waters (LYLE, 1983). On the other study could be a result of the nanism observed hand, precopulatory behavior and copulation in in eastern Mediterranean species (MACHIAS et scyliorhinids may involve the male biting the al., 1998). LITVINOV (2003), who studied sexual fins and body of the female (CASTRO et al., 1988) dimorphism as an index of the isolation of and the mouth of the male may have adapted to West African populations of S. canicula, noted this function by changing shape and dentition significant morphological differences between (ELLIS & SHACKLEY, 1995). west African catsharks and west European and We could not determine any statistical Mediterranean catsharks and suggested that difference between pre-oral lengths (snout to comparative morphological studies on these mouth) of males and females. However, ELLIS populations are needed to determine whether the & SHACKLEY (1995) and ERDOGAN et al. (2004) west African catshark is an independent species found that pre-oral length was significantly or a subspecies. shorter in males and suggested it was a result of the increased mouth length. Similarly, they ACKNOWLEDGEMENTS suggested that significant differences in pre- branchial lengths, head lengths, and head widths No data could have been collected without might be due to sexual differences in the pattern the help and cooperation of fishermen who of growth of the whole head region. Our snout allowed us their ships and Mr. Harun GÜCLÜSOY to spiracle measurements almost coincide with from the UNDERWATER RESEARCH SOCIETY, results of ELLIS & SHACKLEY (1995). Although MEDITERRANEAN SEAL RESEARCH GROUP (SAD- the pre-branchial lengths of males and females AFAG). We are also grateful to F.F. LITVINOV, C. did not statistically differ, the snout to first gill- RODRIGUEZ-CABELLO, F. SÁNCHEZ, J.-Y. SIRE and slit and snout to pectoral distances were longer C. CAPAPÉ who kindly commented on an early in males than in females. version of the manuscript. FİLİZ & TAŞKAVAK: Sexual dimorphism of smallspotted catshark from Turkey 45
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Received: 11 November 2005 Accepted: 14 February 2006
Spolni dimorfizam glave, ustiju i tijela mačke bljedice, Scyliorhinus canicula Linnaeus, 1758 iz Turske
Halit FİLİZ i Ertan TAŞKAVAK*
*e-mail: [email protected]
SAŽETAK
Mužjaci mačke bljedice imaju dužu i užu gubicu od ženki što ukazuje na naglašen spolni dimorfizam. Odnos dužina/širina gubice je 0,55 kod mužjaka i 0,50 kod ženki. Druga mjerenja glave su također signifikantno različita kod spolova, tj. gubica-dišni otvor i udaljenost gubica-prsne peraje. Mjerenja tijela, koja su različita kod spolova, uključuju prsni do analnog dijela, prsni nutarnji rub, prsni do srednjeg dijela, gornju repnu i ukupnu dužinu tijela. U radu je diskutirano o razlozima tih razlika.
Ključne riječi: Scyliorhinus canicula, Elasmobranchii, spolni dimorfizam, meristika, nanizam
ISSN: 0001-5113 ACTA ADRIAT., UDC: 594.1:591.5 AADRAY 47 (1): 49 - 64, 2006 Review paper
The basket shell, Corbula gibba Olivi, 1792 (Bivalve Mollusks) as a species resistant to environmental disturbances: A review
Mirjana HRS-BRENKO
Ruđer Bošković Institute, Center for Marine Research, Paliaga 5, 52210 Rovinj, Croatia e-mail: [email protected]
Structural changes in bottom communities in many coastal and offshore areas result from enhanced eutrophication and are characterized by the presence of species that are tolerant to a wide range of environmental disturbances. In soft bottom communities that are degraded or recovering from stress, Corbula gibba appears to be a highly abundant, ecologically important species and, therefore, an interesting subject for investigation. The literature compiled in this review reveals that, Corbula is a short-lived species with high fecundity, enormous production of small eggs, and a prolonged spawning season. The fertilization of spawned eggs in open waters is followed by pelagic development of larvae, accompanied by dispersal sometimes far from the mother population. High larvae settlement frequently appears as a “recruitment boom” in a new community after a catastrophe, making Corbula a short-term dominant species until the perished invertebrate species repopulate. As a dominant suspension feeder with rapid juvenile and adult growth, Corbula becomes an important element in the food chain as a transferor of organic matter from plankton to benthos. In a relatively stable soft-bottom community, the size of the Corbula population is mainly limited by the activity of competitors and predators. Dense Corbula populations may occur in a community with low species diversity in constantly and occasionally eutrophic areas. Generally, Corbula is considered an indicator of environmental instability caused by pollution, low oxygen content, or increased turbidity.
Key words: Bivalvia, Corbula gibba
INTRODUCTION REVIEW
The basket shell, Corbula gibba (Olivi, 1792), Taxonomic position is a small marine bivalve frequently sampled from soft-bottom communities in European GINANNI (1757) published the first short notice seas. Due to its ecological importance in marine on the common basket shell under the name ecosystems, information about Corbula appears Tellina gibba, sampled about 14 nautical miles in many publications. This review is an attempt offshore from the Adige estuary in the northwest to amalgamate this information. Adriatic Sea. The name Corbula gibba was 50 ACTA ADRIATICA, 47(1): 49-64, 2006 established later by OLIVI (1792). The species is grained sandstone in the Late Oligocene in located taxonomically as follows, according to Hungary (DÁVID, 1999a), and in Middle Miocene the Check List of European Marine Mollusca Korytnica clays of Poland (ZŁOTNIK, 2001). (CLEMAM, MNHN, Paris). Geographic distribution Phylum: Mollusca Linné, 1758 Today, this species is widely distributed in Class: Bivalvia Linné, 1758 European seas (Table 1), from the Norwegian Subclass: Heterodonta Neumayr, 1884 Sea southward to the Mediterranean and Black Order: Myoida Stoliczka, 1870 Seas (only near the Bosporus) (YONGE, 1946; Family: Corbulidae Lamarck, 1818 TEBBLE, 1966; NORDSIECK, 1969; SKARLATO & Species: Corbula gibba (Olivi, 1792: STAROBOGATOV, 1972; FREDJ, 1974; POPPE & Tellina) GOTO, 1993). Corbula populations are distributed Synonyms: Tellina gibba Olivi, 1792 from low intertidal zones to considerable depths Mya inaequivalvis Montagu, 1803 (Table 2). Individuals can penetrate down to Corbula nucleus Lamarck, 1818 Tellina olimpica Costa O.G. 1829 250 m (POPPE & GOTO, 1993; SALAS, 1996) and Corbula ovata Forbes 1838 even deeper to 2200 m (NORDSIECK, 1969; Corbula nautica Brusina 1870 FREDJ, 1974), but usually are found at depths to Corbula curta Locard, 1886 approximately 36 m. In the late 1980s, Corbula was introduced to Evolutionary history Australia where, in Port Phillip Bay, it became abundant in benthic communities (WILSON et The evolutionary history of the Corbulidae al., 1998; TALMAN & KEOUGH, 2001). In some family began in the Tithonian stage of the Late areas of this bay, Corbula reaches densities Jurassic period (DÁVID, pers. comm.). Fossil C. -2 gibba shells were found in Miocene sediments in up to 2600 indididuals m in sandy-muddy marine Badenial marl facies in perturbed coastal sediments at depths of 7-22 m (see Introduction areas of Croatia (KOCHANSKY, 1944; SREMAC, in TALMAN & KEOUGH, 2001), similar to normal 1999), in molluscan clay and marine silty fine Corbula habitats in Europe.
Table 1. Selected literature on Corbula gibba distribution in European seas
Sea References Mediterranean BONVICINI-PAGLIAI et al. (1985); BAKALEN & ROMANO (1988); THEODOROU (1994); SALAS (1996); ZENETOS (1996); BERNASCONI & STANLEY (1997); GIACOBBE & RINELLI (2002); ALBAYRAK et al. (2004) Adriatic VATOVA (1949); GAMULIN-BRIDA et al. (1968); SPECCHI & OREL (1968); ZAVODNIK (1971); HRS-BRENKO (1981, 1997, 2003); LEGAC & HRS-BRENKO (1982); STJEPČEVIĆ et al. (1982); SENEŠ (1988); OREL et al. (1989); CREMA et al. (1991); ALEFFI et al. (1992); VIO & DE MIN (1996); ZENETOS (1996); ADAMI et al. (1997); HRS-BRENKO et al. (1998); MOODLEY et al. (1998); ALEFFI & BETTOSO (2000); PEHARDA et al. (2002); SOLIS-WEISS et al. (2004) Atlantic Coast YONGE (1946); TEBBLE (1966); KITCHING et al. (1976); PEARSON & ELEFTHERIOU (1981); JENSEN (1988, 1990); SALAS (1996); PRUVET (2000); RUEDA et al. (2001) Kattegat and ROSENBERG (1972, 1973, 1974, 1977); ARNTZ (1981), WEIGELT & RUMOHR (1986); Baltic BADEN et al.(1990), WEIGELT (1990); JOSEFSON & JENSEN (1992); ROSENBERG et al. (1992) HRS-BRENKO: The basket shell Corbula gibba as aspieces resistant to environmental disturbances 51
Table 2. Selected literature on population densities, sampling depth, and sediment type for Corbula gibba in various European localities Density Depth Locality Sediment type Reference (ind/m-2 ) (m) Northern Adriatic Northern Adriatic 22400* 34-36 Loam ŠIMUNOVIĆ et al. (1999) Pula harbor 605** 8 ... HRS-BRENKO (1981) Umag area (Istra) 470 16 ... HRS-BRENKO (1981) ZI-012 (Istra) 1113** 23 Silty sand HRS-BRENKO (present study) Muggia Bay 2570 8-20 Mud SOLIS-WEISS et al. (2004) Northern Italian coast 4086*** 12 Pelite ALEFFI & BETTOSO (2000) SJ-101 (Po River) 1217** 31 Clay HRS-BRENKO (present study) SJ-10 (Po River) >1600 30 Silt HRS-BRENKO (1981) Ravena area 1001** 15 ... CREMA et al. (1991) Ravena area 1800 18 Silty clay MOODLEY et al. (1998) Other European Seas Saltkällefjord (Sweden) 490 10 Sandy clay ROSENBERG (1972) Byfjord (Sweden) 4458 8 Silt ROSENBERG (1977) Oresund (Denmark) 1200 juv 18 Silty sand MUUS (1973) Limfjord (Denmark) 53000 3-8 Muddy clay JENSEN (1990) Limfjord (Denmark) 67000 juv 3-6 Clay JENSEN (1988) Dunkerque (France) 1090 ... Muddy sand PRUVOT et al. (2000) Off Cádiz (Spain) 166 26 Mud SALAS (1996) Elefsis Bay (Greece) 1396 20 ... THEODOROU (1994)
*individuals hour-1 by trawl ** mean individuals m-2 *** individuals 50 l-1
Population density uses byssal thread to attach to gravel, pebbles, or shell fragments (YONGE, 1946; TEBBLE, 1966; The population density of C. gibba (number YONGE & THOMPSON, 1976; JENNSEN, 1988; POPPE of individuals per area) varies in space and time. & GOTO, 1993). Due to interstitial spaces, such Literature shows that dense Corbula populations sediments create convenient sheltered niches are well represented in unstable environments for settlement of Corbula larvae and protection such as constantly polluted bays and harbors and from predators. LEGAC & LEGAC (1989) found in coastal and offshore areas exposed to seasonal live individuals inside unbroken amphoras filled or occasional environmental disturbances. The with silt and rough sand, collected at depths density in the northern Adriatic is in good of 17-31 m. In areas with coarser and clean agreement with data in the literature (Fig. 1). sandy sediments, Corbula populations are rare or absent (HRS-BRENKO, 1981; ŠIMUNOVIĆ et al., Habitat 1999; ALEFFI & BETTOSO, 2000). Having a short siphon, Corbula burrows Corbula, an infaunal species with a sedentary vertically and embeds itself into the upper 0-5 mode of life, inhabits soft bottom sediments cm of the sediment (YONGE, 1946; ROSENBERG mixed with molluscan shell fragments. Corbula 1974; YONGE & THOMPSON, 1976; MOODLEY et 52 ACTA ADRIATICA, 47(1): 49-64, 2006
Fig. 1. Population density (individuals m-2) of Corbula gibba in the northern Adriatic Sea and seasonal surface sea currents (marked by arrows; ZORE-ARMANDA & VUČAK, 1984). Corbula data for stations (st.) 4, 5, 8, 10, 12, 14, 17, 18, 21, 23, 26, 27, and 31 were obtained by van VEEN grab (original data shown in individuals 0.5 m-2 are converted to individuals m-2; ALEFFI & BETTOSO, 2000) and for stations (SJ) 005, 007, 101, 103, 107, 108, 301, 311 and (ZI) 012, 032, 052 by van VEEN grab (HRS-BRENKO, 2003, and unpublished data) HRS-BRENKO: The basket shell Corbula gibba as aspieces resistant to environmental disturbances 53 al., 1998). The burrowing process is slow and Larvae development and dispersion described in detail by YONGE (1946). Corbula Corbula has a long pelagic larval stage. seldom emerge from the sediment unless The length of larvae development in bivalves is disturbed (YONGE, 1946). PISAROVIĆ et al. (2000) usually 2-4 weeks depending on the temperature recorded irregular Corbula movements in small and available food. In poor food conditions finger bowls on the sediment surface prior to and at low temperatures, larval development burrowing. The burrowing furrows are 3-5 mm is prolonged and often accompanied by high in height and width. Individuals bury themselves losses due to predation (THORSON, 1950). Until one-third, two-thirds, or entirely. The authors now, few studies focused on larvae development observed that individuals may change position in Corbula. Larvae were found in plankton after embedding; they move and bury themselves between March and June in the Rovinj harbor at night or in darkness during the day. and the Limski Kanal in northern Adriatic (ODHNER, 1914). Corbula larvae were observed Spawning season in Danish waters (MUUS, 1973) in October (JØRGENSEN, 1946; SCHRAM, 1962), July-August, Corbula produces a large number of small October-November, and January-February, with eggs (60 μm diameter), fertilized in open waters a maximum in July (FOSSHAGEN, 1965). The (JØRGENSEN, 1946; THORSON, 1950). Information finding of larvae in plankton in so many months on the Corbula spawning season is scarce. clearly indicates a prolonged reproductive and GRAEFFE (1903) found many ripe individuals in larvae development season. the Trieste harbor in September while YONGE A long larvae development period promotes (1946) registered spawning in early October spatial distribution by sea currents, sometimes to at the Isle of Cumbrae. BONVICINI-PAGLIAI & considerable distances from parent populations SERPAGLI (1988) discovered that June-September (THORSON, 1950; GIANGRANDE et al., 1994). In such is the spawning season, based on complex micro a manner, planktonic larvae constantly expand growth patterns with marked growth breaks in existing populations in stable and damaged thin sections of the shell. communities and colonize new zones, extending BOON et al. (1998) reviewed the relationship their distribution area. between invertebrate reproduction and spring In a large and relatively enclosed area such phyto plankton bloom. Polyunsaturated fatty as the northern Adriatic Sea, larval distribution acids, derived from phytoplankton in sedi- (except for diurnal migration between bottom mentary and near-bottom particles, are essential and surface levels) depends on complex water circulation. In the spring, there is an imaginary compounds for reproduction and growth of east-west line between the Po River delta and many benthic species (BOON & DUINEVELD, 1996). Rovinj, north of which a cyclonic circulation Reproductive potential, growth, and abundance system transports low salinity waters with silt in the bivalve Abra alba increased in eutrophic from the vicinity of the Po River eastwards. environments, resulting in three spawning This transversal current is accompanied by seasons per year instead of two as in oligotrophic a southward current from the Po along the conditions (DAUVIN & GENTIL, 1989). After an Italian coast (ZORE-ARMANDA & VUČAK, 1984; extraordinarily high phytoplankton bloom in the KRAJCAR, 2003). Both currents create ideal northern Adriatic Sea in 1989 (DEGOBBIS et al., bottom conditions for the establishment of 2000), Corbula probably increased its fecundity dense Corbula populations. The cyclonic water and prolonged spawning and settlement seasons circulation encircles a zone north of the Po throughout almost all of the following year River-Rovinj line that is often eutrophic with (HRS-BRENKO et al., 1994; HRS-BRENKO, 2003), stagnant water and soft bottoms highly populated suggesting that Corbula may behave similarly by Corbula. This zone is assumed to be the main to Abra. source of Corbula larvae dispersion throughout 54 ACTA ADRIATICA, 47(1): 49-64, 2006 the entire northern Adriatic, which is also true (ROSENBERG, 1977; OREL et al., 1989; BADEN et for other invertebrates with long pelagic larvae al., 1990; ALEFFI et al., 1992, 1993; HRS-BRENKO et development periods. SPECCHI & OREL (1968) al., 1992b, 1994), and after cessation of industrial found that the renewal of Corbula populations in waste water discharges (ROSENBERG, 1972, Muggia Bay depends on immigration of larvae 1973). In such circumstances, Corbula tends to from offshore zones. aggregate thanks to the low species diversity in Similarly, owing to the local current regime, the bottom community (ROSENBERG, 1977). Corbula populations are dense in the inner zones The boom phenomenon characterizes of closed bays, canals, fjords, and harbors char- Corbula as an opportunistic bivalve that, acterized by unstable environmental conditions together with some invertebrates, immediately and polluted freshwater inflows. In such cases, colonizes destroyed communities. In general, the majority of Corbula individuals must come abundant Corbula juveniles indicate areas where from local sources, especially when Corbula an environmental disaster recently happened populations are negligible in neighboring zones and damaged communities are in the early (ROSENBERG, 1972, 1973; HRS-BRENKO, 1981; PRU- recovery phase. BONVICINI-PAGLIAI & SERPAGLI VOT et al., 2000). (1988) called Corbula an environmental stress species and a “time recorder” that indicates the Recruitment beginning of macrofaunal succession after a Recruitment is the process of larvae settle- catastrophe. ment and survival to 1 mm (JENSEN, 1988; DAME 1996). In species with long larvae develop- Growth and life span ment, such as Corbula, the length of the settle- JØRGENSEN (1946) and MUUS (1973) recorded ment season and its intensity significantly vary the length of Corbula in the prodissoconch between years, depending on food supply, larval stage (0.24-0.25 mm), at metamorphosis (0.25- dispersion, predation, availability of appropriate 0.33 mm), and after settlement (0.30-0.60 bottoms, and environmental conditions (THOR- mm). Settled bivalves smaller than 2 mm are SON, 1950; GIANGRANDE et al., 1994). meiofauna, staying in this assemblage for about In high latitudes, MUUS (1973) recorded Corbula spat from mid-August to early January, one month (THORSON, 1966). ROSENBERG (1977) observed heavy and successful The distribution of mean shell lengths of larvae settlement from September to November, Corbula in Limfjord, Denmark (JENSEN, 1990) and JENSEN (1988) reported on August and and length frequencies in the northern Adriatic September. In the northern Adriatic, after the (HRS-BRENKO, 2003) show that Corbula grow 1989 oxygen crisis, the settlement season of rapidly in spring and early summer. According Corbula extended throughout the entire year to JENSEN (1990), Corbula growth ceases at of 1990 with a peak in summer at offshore and temperatures below 13°C (October-May) coastal stations (HRS-BRENKO et al., 1994; HRS- while HRS-BRENKO (2003) observed the same BRENKO, 2003). ALEFFI et al. (1993) postulated phenomenon in winter. The increase in length that prolonged settlement seasons of Corbula during spring corresponds to the increased results from high autumn temperatures and low abundance of resuspended organic matter near competition for space after oxygen depletion. the bottom and the bottom-living diatoms and Many studies have shown that Corbula bacteria that Corbula siphons from the bottom settlements boom in favorable environmental surface (YONGE, 1946; JENSEN, 1990). As an active conditions following the cessation of a particular suspension feeder, Corbula is an important stress agent. Corbula booms were observed transferor of organic matter to the benthos. This after dredging canals (SPECCHI & OREL, 1968; was evident during the early recovery period BONVICINI PAGLIAI et al., 1985), in the aftermath in 1990 when Corbula dominated the bottom of oxygen crises and in oxygen deficient areas community (HRS-BRENKO, 2003). HRS-BRENKO: The basket shell Corbula gibba as aspieces resistant to environmental disturbances 55
Table. 3. Mean length at about one year and maximum length in second year of Corbula gibba Mean length Maximum length Locality Author (mm) (mm) Isle of Man 8 12.0 JONES (1956) see: MUUS (1973) Limfjord 6-7 10.8 JENSEN (1988, 1990) Northern Adriatic 7-10 13.5 ALEFFI & BETTOSO (2000) Northern Adriatic 6-8 14.7 HRS-BRENKO (2003)
Corbula reaches its maximum length at 16 anaerobic conditions of starfish stomachs mm (NORDSIECK, 1969). In the northern Adriatic, (CHRISTENSEN, 1970). the longest Corbula specimen measured 14.7 mm In a comprehensive review on the effects of (HRS-BRENKO, 2003). The scarce data on mean hypoxia on benthic fauna, only Corbula survived and maximum lengths of Corbula show similar mass mortality events (DIAZ & ROSENBERG, 1995). growth patterns in various study areas during a This was true in a sea loch, Lough Ine; (KITCHING two-year period (Table 3). Corbula, like other et al., 1976) and in the innermost part of a fjord in small benthic species, has a short life span of the Shetland Isles (PEARSON & ELEFTHERIOU, about two years with natural mortality beginning 1981). Corbula survived together with a few at 10 mm in the second year (ROSENBERG, 1977; other species in Kiel Bay (ARNTZ, 1981; WEIGELT JENSEN, 1990; ALEFFI et al., 1993; HRS-BRENKO, & RUMOHR, 1986; WEIGELT, 1990) and the Kattegat 2003). area (BADEN et al., 1990; JOSEFSON & JENSEN, 1992; ROSENBERG et al., 1992). Corbula dominated in Survival: abiotic stress agents hypoxic water layers that covered anoxic layers in the Byfjord Estuary (ROSENBERG, 1977) while Corbula, an inhabitant of unstable envi- only Corbula was recorded in polluted Elefsis ronments, tolerates anthropogenic and natural Bay in the Mediterranean in summer during disturbances. In bays, fjords, and harbors with strong thermal stratification accompanied by excessive organic matter (domestic and industri- anoxic conditions (THEODOROU, 1994). Corbula al wastes, oil, etc.), Corbula can develop dense survived frequent oxygen disasters in a sensitive populations because of the low species diversity northern Adriatic ecosystem (ALEFFI et al., 1992; in the community (GRAEFFE, 1903; ROSENBERG, HRS-BRENKO et al., 1992a, 1992b, 1994). Numerous 1972, 1973, 1977; HRS-BRENKO, 1981; BAKALEM & live Corbula individuals were found among ROMANO, 1988; JENSEN, 1990; THEODOROU, 1994; bottom deposited bivalve shells in the Malo ADAMI et al., 1997; BORJA et al., 2000; PRUVOT et Jezero salt lake (southern Adriatic) that is al., 2000; SOLIS-WEISS et al., 2004). For this reason, unpolluted but occasionally stressed with sulfide Corbula is a bioindicator of pollution of sea bot- (PEHARDA et al., 2002). tom communities (FAO/UNEP, 1986) and belongs Corbula is resistant to high turbidity thanks to the ecological group of r-selected species to its ctenidia that efficiently separate organic (GRAY, 1979; GIANGRANDE et al., 1994). from inorganic particles in resuspended bottom In addition to its pollution tolerance, Corbula material (KIØRBOE & MØHLENBERG, 1981). is an oxygen resistant species (ROSENBERG, 1977; Further, the asymmetric construction of the DIAZ & ROSENBERG, 1995). It survives well for Corbula shell provides for better outflow of large certain periods in low oxygen conditions but amounts of pseudofeces (YONGE, 1946; YONGE & may diminish in prolonged hypoxia (BADEN THOMPSON, 1976). Such features enable Corbula et al., 1990). This high oxygen resistance was to form dense populations and survive in soft confirmed in laboratory experiments in which bottoms in closed bays with high sedimentation adult Corbula survived several days in the and reduced hydrodynamism (SOLIS-WEISS et al., 56 ACTA ADRIATICA, 47(1): 49-64, 2006
2004) as well as in silted transversal currents in plays an important role in structuring benthic the northern Adriatic (HRS-BRENKO, 2003). communities. Most bivalve species protect themselves In spite of scarce evidence relating to from temporary environmental stress by tightly meiofaunal and macrofaunal exterminators of closing their valves. Corbula does this well Corbula, it is possible to speculate about its fate thanks to its special valve construction that in the environment by considering the bivalve- allows hermetic shell closure (YONGE, 1946; predator and bivalve-competitor interactions YONGE & THOMPSON, 1976; BONVICINI-PAGLIAI mentioned above. Larger meiofaunal species & SERPAGLI, 1988). Shells formed in such a way may be active predators on recently settled keep the valves fast even after death. Many Corbula larvae. If so, the reduced abundance Corbula individuals sampled in the Adriatic with of meiofaunal species (TRAVIZI, 2000) after closed shells were either empty or filled with the oxygen disaster in the Adriatic may have mud. This finding calls for careful inspection of partly contributed to the simultaneous increase whether Corbula individuals were alive at the of the Corbula population during the ensuing time of sampling. six-month recovery period (HRS-BRENKO et al., In addition to closing shells, bivalves have 1994). a protective mechanism that switches them to At the macrofaunal level, in a stable bottom anaerobic metabolism by increasing the lactate community, suspension feeders may accidentally inhale Corbula larvae during intensive filtration, concentration in the tissues (PISAROVIĆ et al., 2000; decimating them prior to settlement. The ŽERJAV MEIXNER, 2000). Later, when normoxic ophiuroid Amphiura filliformis, a suspension conditions return, Corbula increases oxygen feeder, may ingest larvae and newly settled consumption for a short period of time to cover juveniles of many invertebrates (CROWE et al., its “oxygen debt” during which accumulated 1987). The question is whether the period spent anaerobic metabolic products are eliminated. within the body of a suspension feeder is fatal for Corbula larvae. In the absence of numerous Survival: biotic stress agents suspension feeders, Corbula may benefit from the low competition for space between survived Predation and competition are important biotic invertebrates and among settling Corbula causes of losses of bivalve larvae, juveniles, and larvae. As with the bivalve suspension feeder, adults. During planktonic life, Corbula larvae Cerastoderma edule (ANDRÉ et al., 1993), Corbula can be preyed upon by ctenophores, jellyfish, may eliminate its own settling larvae and thus copepods, invertebrate larvae, and pelagic fish. limit settlement intensity in areas where adults Mature larvae swimming near the bottom or are abundant (JENSEN, 1988, 1990). It seems that crawling on the sediment are eliminated by such an adult-juvenile interaction occurred after suspension feeders. Surface and subsurface the 1989 oxygen crisis in the northern Adriatic carnivores, deposit feeders, and omnivores where the dominant adult population of 800 m-2 prey on Corbula juveniles and adults. Finally, may have postponed the larvae settlement peak intra and interspecies competition for food and to the summer; meanwhile, at another station, space significantly regulates species abundance the adult density of only 153m-2 allowed high in a bottom community (THORSON, 1950, 1966; recruitment already in February. In this case, MUUS, 1973; MILEIKOVSKY, 1974; CROWE et al., of course, other suspension feeders were also 1987; JENSEN, 1988; KELLEY, 1988; MORTON, 1991; limiting settlement factors. AMBROSE, 1993; ANDRÉ et al., 1993; SEED, 1993; Competition for food and space can limit the GIANGRANDE et al., 1994; ÓLAFSON et al., 1994; Corbula population. For example, the bottom- DAME, 1996; HRS-BRENKO, 1998; MOODLEY et al., dwelling C. gibba competes for food and space 1998, ZŁOTNIK, 2001). All these aspects create with another suspension feeding species, the off- a complex interaction of biotic factors that bottom amphipod Amphelisca sp. (MOODLEY HRS-BRENKO: The basket shell Corbula gibba as aspieces resistant to environmental disturbances 57 et al., 1998). When present in dense populations, Euspira (Polynices) sp., have attacked infaunal Amphelisca consume detritus before it reaches suspension feeding mollusks including Corbula the Corbula at the bottom, limiting the Corbula by drilling holes in their shells (JEFFREYS, 1865, population. After widely occupying its new in YONGE, 1946; KOCHANSKY, 1944; KELLEY, 1988; environment in Australia, Corbula significantly MORTON, 1991; DÁVID, 1999a, b; SREMAC, 1999; affected the juvenile size and growth of the ZŁOTNIK, 2001). The drilling process is described native scallop Pecten fumatus, as both species in ZIEGELMEIER (1954), YONGE & THOMPSON (1976), are suspension feeders (TALMAN & KEOUGH, and others (see ZŁOTNIK, 2001). Large naticids 2001). Another example of food competition was prefer to attack the right valve of Corbula in the observed during the heavy Corbula settlement central-ventral region, while small naticids drill in February 1990, which was followed by more or less equally into both valves (ZŁOTNIK, mortality up to 45% in the 2.5 mm length class 2001). DÁVID (1999b) found more boreholes in in March. Shells of sampled individuals were the right valve and rounded boreholes were closed, empty, tiny, transparent, but undamaged. more common than sickle perforations. Round Without doubt, they were not eaten by predators boreholes were made by Natica sp. (YONGE but apparently died due to food limitation in the & THOMPSON, 1976; DÁVID, 1999a; PISAROVIĆ new densely populated community. ÓLAFSON et al., 2000; ZŁOTNIK, 2001). Although Corbula et al. (1994) proposed that food limitation is a dominate over other invertebrate species in more important cause of mortality in newly fossils and recent bottom samples, only 8% settled invertebrates than in adults. JENSEN (PISAROVIĆ et al., 2000) to 17-20% (ZŁOTNIK, (1988) attributed the high mortality of Corbula 2001) were attacked by boring gastropods. All juveniles (up to 31% in the first month after sizes of Corbula were attacked, but completely settling) to epibenthic predation while JENSEN perforated boreholes were relatively rare. On the (1990) attributed adult mortality to weakness shell of a 2.7 mm Adriatic Corbula, only one after spawning. of three boreholes was completely perforated. Carnivorous gastropods, mobile crustaceans, Owing to variation in shell thickness and a dense starfishes, fishes, and birds are among the inner calcareous shell layer, Corbula is better destructive bivalve predators. Predator-prey protected against gastropod acid secretion than studies have mostly focused on commercial other bivalve species (YONGE, 1946; BONVICINI- bivalves from shallow coastal and estuarine PAGLIAI & SERPAGLI 1988; KELLEY, 1988; DÁVID, areas (MORTON, 1991; SEED, 1993; ÓLAFSON et al., 1999b; ZŁOTNIK, 2001). 1994; DAME, 1996). Little data related to predators The crustaceans Carcinus means and of Corbula have been published. Crangon crangon may also prey on Corbula Starfishes are voracious Corbula predators (JENSEN, 1988) by smashing or chipping their and frequently contain Corbula individuals in shells. Fish from the Sparidae family and flat their stomachs (CHERBONNIER, 1966; SPECCHI & fishes from the Heterosomata order (KOVAČIĆ, OREL, 1968; CHRISTENSEN, 1970; MILEIKOVSKY, pers. comm.) may swallow whole Corbula 1974; JENSEN, 1988; POPPE & GOTO, 1993). In individuals. Many of these predators disappear laboratory experiments, Astropecten irregularis from bottom communities when the oxygen level excreted live Corbula adults several days after begins to drop. In such cases, the fish species they were swallowed, which was not the case either die or escape to normoxic areas, increasing with juveniles of 2-3 mm (CHRISTENSEN, 1970). fish catches there (STEFANON & BOLDRIN, 1982; Asterias rubens and Ophiotrix texturata are DYER et al., 1983; ŠIMUNOVIĆ et al., 1999). In the also possible predators of juvenile Corbula interim, until predator fish species repopulate immediately after settlement (JENSEN, 1988). the damaged bottom communities either by Since the Paleozoic era, carnivorous returning as adults or by new recruitment, gastropods from the Muricidae and Naticidae opportunistic species such as Corbula may families, predominantly Natica sp. and proliferate. 58 ACTA ADRIATICA, 47(1): 49-64, 2006
CONCLUSIONS As a suspension feeder, Corbula uses mainly decomposed and resuspended organic Corbula gibba (Olivi, 1792) is a widespread matter to increase its fecundity and juvenile European bivalve with an evolutionary history and adult growth rates. Thus, Corbula is an dating back to the Paleozoic era. Dense important participant in the flow of energy to Corbula populations are established in soft the benthos, particularly when it is dominant in bottom communities with low species diversity the community. and in constantly or occasionally unbalanced Corbula tolerates a wide range of abiotic environments. The populations are distributed environmental disturbances. For this reason from low intertidal zones to considerable depths, Corbula is a bioindicator of pollution, turbidity, but optimally down to approximately 36 m. and low oxygen content in benthic communities. In deeper coarser and clean sandy sediments, Biotic factors, such as competition and predation, Corbula populations are rare or absent. are the main factors that limit the expansion of As an infaunal sedentary species, Corbula Corbula populations in a stable community. In inhabits soft sediments mixed with gravel and stressed environments, Corbula dominates until its molluscan shell fragments that are necessary for most sensitive competitor and predator recovers it byssal thread attachment. Having a short siphon, own population. Voracious macrofaunal predators Corbula burrows vertically near the sediment are starfishes, demersal fishes, and crabs, while surface and emerges when disturbed. Corbula carnivorous gastropods attack Corbula only displays a light/dark reaction and burrows in occasionally, thanks to its hard shell and dense dark conditions. inner calcareous shell layer that is resistant to The scarce literature indicates Corbula has the acidic secretions of gastropods. a prolonged reproductive season during which it produces many small eggs that are fertilized ACKNOWLEDGEMENTS in open water. The pelagic larvae development period extends throughout the year. Corbula The author thanks Dr. Stjepan KEČKEŠ and take advantage of favorable sea currents and Dr. Nastjenka SUPIĆ for critical reading of the human activities to expand existing populations, manuscript and useful comments, anonymous increase populations in damaged communities, referees for constructive suggestions on the and colonize new areas. The potential of Corbula text and language improvement, and Mr. Željko recruitment is evident in damaged, degraded, STIPIĆ for preparing Fig. 1. This research and newly occupied areas where “recruitment was supported by the MINISTRY OF SCIENCE, booms” may occur in summer and autumn. As EDUCATION AND SPORT OF THE REPUBLIC OF such, Corbula functions as an indicator of the CROATIA (Project No. 00981302). recovery of the bottom community.
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Received: 28 January 2005 Accepted: 11 January 2006 64 ACTA ADRIATICA, 47(1): 49-64, 2006
Školjkaš korbula, Corbula gibba (Olivi, 1792) (Bivalve Mollusks), otporna vrsta na poremećaje u okolišu. Pregledan rad
Mirjana HRS-BRENKO
Institut Ruđer Bošković Centar za istraživanje mora, Paliaga 5, 52210 Rovinj Hrvatska e-mail: [email protected]
SAŽETAK
Školjkaš korbula, Corbula gibba (Olivi, 1792), je rasprostranjena vrsta u evropskim morima i često je obilna u nestabilnim i eutrofiziranim sredinama. Zapažena kao ekološki važna vrsta u obnovi pridnenih zajednica u sjevernom Jadranu, nakon učestalih ugibanja vrsta makrobentosa uzrokovanih nestašicama kisika, korbula se smatrala zanimljivom vrstom za istraživanja populacijskih karakteristika. Pregled do sada objavljenih radova o korbuli ukazuje da je to mala kratko živuća vrsta visokog reprodukcijskog potencijala s obilnom proizvodnjom malih spolnih stanica tijekom produžene sezone mriješćenja. Oplodnja jajnih stanica i razvoj ličinki u planktonskoj zajednici omogućuje njeno širenje u nova područja, kao i u područja osiromašena vrstama nakon katastrofalnih ugibanja. Slobodni prostori, nastali nakon ugibanja brojnih vrsta u pridnenoj zajednici, omogućuju korbuli intenzivno naseljavanje novacima, u prvoj fazi obnove makrobentosa. Tada kao dominirajuća «suspension feeding» vrsta korbula postaje važnim prenosnikom proizvedene organske tvari iz fitoplanktona u bentos. U kasnijem periodu obnove pridnenih zajednica znatno se smanjuje veličina populacije korbule. Čini se da tome pridonosi kratak životni vijek korbule kao i obnova predatorskih vrsta. Sažeto rečeno korbula se zbog svoje otpornosti prema učestalim promjenama sredine smatra indikatorom nestabilnosti, najčešće uzrokovanim sniženjem slanoće morske vode, te pojačanim turbiditetom i zagađivačima, u okolišu snižene bioraznolikosti.
Ključne riječi: Bivalvia, Corbula gibba
ISSN: 0001-5113 ACTA ADRIAT., UDC: 582.273(26.05)(450Venecija) AADRAY 47 (1): 65 -72, 2006 Short communication
First report of Lomentaria hakodatensis (Lomentariaceae, Rhodophyta) from the lagoon of Venice (Adriatic Sea, Mediterranean)
Daniele CURIEL1*, Giorgio BELLEMO1, Mario SCATTOLIN2 and Mara MARZOCCHI3
1 SELC Soc. Coop., Via dell’Elettricità 3d, 30175 Marghera-Venezia, Italy
2 Comune di Venezia, Assessorato all’Ecologia, S. Marco 4136, 30100 Venezia, Italy
3 Dipartimento di Biologia, Università di Padova, Via Trieste 75, 35121 Padova, Italy * Corresponding author, e-mail: [email protected]
Lomentaria hakodatensis Yendo, known from China, Japan, Korea, and the Pacific coasts of North America, was recorded for the first time in the lagoon of Venice on the Adriatic Sea in 2000. Specimens in the reproductive stage had tetrasporophytes, male, and female gametophytes. Morphological, anatomical, and reproductive features of the thalli are described and the occurrence of the species in the lagoon is discussed. Data on associated algae are presented. This species was recently found in France, Spain, Russia, the Hawaiian Islands, and Australia.
Key words: marine algae, Rhodophyta, Lomentaria hakodatensis, Venice Lagoon, Adriatic Sea
INTRODUCTION Thalli of a Rhodophyta determined to be L. hakodatensis were found on Chioggia Island Lomentaria hakodatensis Yendo was (southern basin) during a survey of marine originally recorded in the East China Sea, Japan, benthic flora of the hard substrata of the lagoon Korea (HOWE, 1924; OKAMURA, 1932; KANG, 1966), of Venice in spring and autumn 2000. The and the Pacific coasts of British Columbia, first vegetative and reproductive anatomy of Washington and southern California (DAWSON, Mediterranean specimens is described in the 1944; ABBOTT & HOLLENBERG, 1976; HAWKES & present work. SCAGEL, 1986). This species has been reported as an alien DESCRIPTION species in Europe on the Atlantic shores of France (CABIOCH & MAGNE, 1987) and Spain The brownish-purple thalli are spherical (ICES, 1992; BÁRBARA & CREMADES, 1996), in or hemispherical, formed by cylindrical, the Mediterranean Sea (VERLAQUE & RIOUALL, gelatinous, flaccid, hollow, and somewhat 1989; ROMAGNOLI & SOLAZZI, 2003), in Russia flattened branches. Ramifications occur three to (PERESTENKO, 1994), in the Hawaiian Islands five times, in opposite or occasionally alternate (ABBOTT, 1999), and in Australia (PHILLIPS, 1997). or verticillate directions (Fig. 1). 66 ACTA ADRIATICA, 47(1): 65-72, 2006
Fig. 1. Typical Lomentaria hakodatensis Yendo from the Fig. 2. Septa in the apical branches (scale bar = 400 μm) lagoon of Venice (scale bar = 2 cm)
The thalli are intertangled, 5-10 cm high are indiscernible but in the branchlets or young and 0.8-1.3 mm wide, and attached to the branches are distinct and evident (Fig. 2). The substratum by a stoloniferous discoid holdfast. inter-septa in the lower part of the thalli are The lower branches are longer than the upper much longer than in the upper. ones, giving a pyramidal appearance to the The main branches in the transverse section mature thalli. Branches rise with a divergence consist of a single external layer of isodiametric of about 45°. The constrictions and septa in the or slightly oblong pigmented cells (diameter main axis, primary, and secondary branches 5-13 μm) and a medulla of 3-5 layers of round
Fig. 3. Vegetative anatomy in transverse section with tube Fig. 4. Inner wall of cavity with axial filaments of elon- cavity (arrow) and axial filaments in section (double gated cells (arrows) and gland cells (double arrows; arrows; scale bar = 50 μm) scale bar = 40 μm) CURIEL, BELLEMO, SCATTOLIN & MARZOCCHI: First report of L. hakodantensis in Venice lagoon 67
Fig. 5. Longitudinal section at the multi-cellular septum Fig. 6. Anastomous of two branches (scale bar = 350 μm) level with gland cells (arrows; scale bar = 100 μm) to elliptical cells which become larger inwards of polygonal cells with several gland cells (Fig. (diameter 30-38 μm; Fig. 3). The outer medullary 5). The anastomous among the thalli or branches cells are slightly pigmented, the inner are hyaline of a thallus are numerous and originate from the and elongated in a longitudinal section. The resumption of growth of the cortical cells (Fig. 6). medullary cells have scattered filamentous Fertile tetrasporophytes and female and longitudinal rows of cells (diameter 5-7 μm) and male gametophytes were found from April to gland cells (diameter 9-12 μm; Fig. 4). September. The tetrasporophytes are similar to The transverse septa of the branches and sterile specimens and tetrasporangia (60-68 μm branchlets are composed of 3-4 irregular rows in length) and borne in small swollen branchlets
Fig. 7. Tetrasporangia (scale bar = 150 μm) Fig. 8. Mature cystocarp (scale bar = 600 μm) 68 ACTA ADRIATICA, 47(1): 65-72, 2006
in the upper portions of the lateral branches (diameter 300-850 μm) and appear to be solitary or in groups of two or three (Fig. 8). The sessile cystocarps are spherical to pear-shaped, with prominent pores (diameter 150-300 μm). The spermatangia extend over the whole surface of the gametophytes except for the basal part of the axis. Mature spermatangia are elliptical, 4-6 μm high, and 3 μm wide (Fig. 9).
ECOLOGY Lomentaria hakodatensis was found from March to October in the lower intertidal and upper subtidal zones from 0.20 m above sea level to 1.0 m below, on the vertical canal banks of Chioggia Island. They were more common and had higher coverage and biomass values Fig. 9. Spermatangia in surface view (scale bar = 40 μm) in autumn samples than in spring. Lomentaria hakodatensis is associated with the dominant deep in the cortex (Fig. 7). The elliptical to round alien brown algae Sargassum muticum (Yendo) tetrasporangial sori are dispersed on branch Fensholt and Undaria pinnatifida (Harvey) intersepta in the middle portions of secondary Suringar. The main algae occurring on the and tertiary branches. Procarps were not hard vertical banks where L. hakodatensis was observed. Female gametophytes bear cystocarps collected are presented in Table 1. CURIEL, BELLEMO, SCATTOLIN & MARZOCCHI: First report of L. hakodantensis in Venice lagoon 69
The limited local distribution of L. hako- sori in the cortex (ABBOTT & HOLLENBERG, datensis may indicate a recent introduction, 1976; LEE, 1978; IRVINE, 1983; HAWKES & SCAGEL, possibly associated with shellfish culture since 1986). These thalli are distinct from others of aquaculture farms on Chioggia Island import the same genus that exist in Venice lagoon, mollusks and fish. The spread of alien species namely, Lomentaria clavaeformis Ercegovic, along the Atlantic and Mediterranean coasts of L. chylocladiella Funk, L. ercegovicii Verlaque, Europe has been linked with aquaculture farming Boudouresque, Meinesz, Giraud et Marcot- and intensive shipping (ICES, 1992; VERLAQUE, Coqueugniot, L. clavellosa (Turner) Gaillon, L. 1994; OCCHIPINTI, 2000), so it is of no surprise that articulata (Hudson) Lyngbye (DE TONI & LEVI, L. hakodatensis, like U. pinnatifia, S. muticum, 1888, as L. phalligera J. Agardh), and L. uncinata and Antithamnion pectinatum, was first reported Meneghini ex Zanardini. in the shellfish raising lagoons Thau (France) The only species from the Venice lagoon with and Venice (Italy). similar morphological characteristics is L. firma A recent survey (SFRISO & LA ROCCA, 2005) (J. Agardh) Falkenberg (SCHIFFNER & VATOVA found L. hakodatensis in the southern lagoon 1937, VATOVA 1940). In common with L. firma, L. of Venice, 2-10 km from Chioggia Island, but hakodatensis sometimes has flattened cylindrical not in the central lagoon or canals. Similarly S. axes, anastomosized intricate branches, and muticum, introduced in the lagoon near Chioggia well-developed cortication formed of a single (GARGIULO et al., 1992), required several years to layer of pigmented cells and 3-4 inner layers spread into the central lagoon (MARZOCCHI et of polygonal subcortical cells. The original al., 2003). If the ecological requirements of L. description of L. firma as Chrysymenia firma hakodatensis are similar to those of other species (AGARDH, 1842) and subsequent publications of the same genus that exist in the lagoon (marine as Chondrosiphon mediterraneus Kützing water, low turbidity, good hydrodynamics), it (KÜTZING, 1865) and C. firma J. Agardh and could gradually spread to areas with seawater C. polycarpa Zanardini (ZANARDINI, 1871) do inflow but not to more interior areas where the not correspond to L. hakodatensis, as these water turbidity is high. species are reported to have irregular branching Lomentaria hakodatensis joins the list of (alternate, opposite, or unilateral) rather than the alien algae recently recorded in the Venice strictly opposite, verticillate, or rarely alternate Lagoon (GARGIULO et al. 1992; RISMONDO et al. branching in L. hakodatensis. In addition, 1993; CURIEL et al. 1996ab, 1999, 2002; BELLEMO et branchlets are apically thin and flexuous rather al. 2001). The abundance of L. hakodatensis in than slightly curved inwards and tapering as in Chioggia is low. The most abundant species are L. hakodatensis. The description of L. firma by the alien U. pinnatifida and S. muticum, though ERCEGOVIĆ (1956) resembles the figures of L. their biomass is lower in Chioggia than in other firma of KYLIN (1931; Tables 13, 14; Figs. 31, parts of the lagoon (400-1200 g dry wt/m2 for 32) and are quite different from the specimens U. pinnatifida and 200-1100 g dry wt/m2 for S. illustrated by ZANARDINI (1871; Table 110a). muticum (CURIEL et al., 1995, 1998, 2001). The above authors failed to report the constrictions in young branches and septa so DISCUSSION typical of L. hakodatensis. In fact, ZANARDINI (1871) placed his material in the genus Chylocladia The organization of the thalli was similar to and not in Lomentaria because of its continual the recent description of the genus Lomentaria: tubular structure without septa. (a) terete or slightly flattened thalli with hollow In his description of Japanese specimens, branches and multilayered cellular septa at YENDO (in LEE, 1978) noted that his species was intervals, (b) septa identified by constriction intermediate between L. linearis Zanardini and only in young branchlets, (c) cortical layers and L. articulata (Hudson) Lyngbye, but mentioned rows of medullary cells bearing gland cells, species currently considered synonymous and (d) tetrahedrally-divided tetrasporangia in with L. firma: C. polycarpa Zanardini, C. 70 ACTA ADRIATICA, 47(1): 65-72, 2006 firma J. Agardh, and C. compressa (Kützing) compete with smaller species. The occurrence of Zanardini. A comparison between L. firma and reproductive specimens in the lagoon of Venice, L. hakodatensis is needed to resolve the question as in Brittany (CABIOCH & MAGNE, 1987), suggests of possible synonymy. that the lagoon has appropriate environmental The morphological, anatomic, and conditions for reproduction of the species. In reproductive features of the species collected other locations, introduced populations maintain in the Venice lagoon correspond well with L. themselves primarily by vegetative propagation hakodatensis Yendo in Japan (LEE, 1978), British (SOUTH, 1968; HAWKES & SCAGEL, 1986; MILTON Columbia and Washington (HAWKES & SCAGEL, et al., 2002). 1986), California (ABBOTT & HOLLENBERG, 1976), and along the Atlantic coast of France (CABIOCH ACKNOWLEDGEMENTS & MAGNE, 1987). The Chioggia survey targeted areas with low The authors would like to thank Professor M. coverage of aliens, as large algae successfully CORMACI for his observations and suggestions.
REFERENCES
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SOUTH, G.R. 1968. Observations on the occurrence repercussions onto environment and human of a species of Lomentaria in southern British activities). Oceanologica Acta, 17:1-23. Columbia and northern Washington. Can. J. VERLAQUE, M. & R. RIOUALL. 1989. Introduction de Bot., 46(6):727-732 Polysiphonia nigrescens et d’Antithamnion SFRISO, A. & B. LA ROCCA. 2005. Aggiornamento nipponicum (Rhodophyta, Ceramiales) sulle macroalghe presenti lungo i litorali sur le litoral Méditerranéen Français e sui bassofondali della laguna di Venezia (Introduction of Polysiphonia nigrescens and (Update on macro algae present on littoral d’Antithamnion nipponicum (Rhodophyta, and shallow waters of Venetian lagoon). Ceramiales) on the French Mediterranean Lavori Soc. Ven. Sc. Nat., 30:45-56. littoral). Cryptogam. Algol., 10:313-323 VATOVA, A. 1940. Distribuzione geografica delle ZANARDINI, G. 1871. Iconographia phycologica alghe della laguna di Venezia e fattori che Mediterraneo-Adriatica ossia scelta di ficee la determinano (Geographical distribution nuove o più rare dei mari Mediterraneo e of algae from Venetian lagoon and its Adriatico figurate, descritte ed illustrate da determination factors). Thalassia, 4:1-37. G. Zanardini (Phycology of Mediterranean VERLAQUE, M. 1994. Inventaire des plantes and Adriatic or selected new algae rare introduites en Méditerranée: origines et in the Mediterranean and Adriatic, drawn, répercussions sur l’environnement et les described and illustrated by G. Zanardini). activités humaines (Inventory of plants Tipografia G. Antonelli, Vol. III, Tavv. introduced in the Mediterranean: origins and LXXXI-CXII.
Received: 19 July 2005 Accepted: 7 March 2006
Prvo izvješće o algi Lomentaria hakodatensis (Lomentariaceae, Rhodophyta) u venecijanskoj laguni (Jadran, Sredozemlje)
Daniele CURIEL1*, Giorgio BELLEMO1, Mario SCATTOLIN2 i Mara MARZOCCHI3
1 SELC Soc. Coop., Via dell’Elettricità 3d, 30175 Marghera-Venezia, Italija 2 Općina Venecija, Povjerenstvo za ekologiju, S. Marco 4136, 30100 Venecija, Italija 3 Odsjek biologije, Sveučilište u Padovi, Via Trieste 75, 35121 Padova, Italija *e-mail: [email protected]
SAŽETAK
Lomentaria hakodatensis Yendo nalazimo u Kini, Koreji i na obalama Tihog oceana u Sjevernoj Americi. Po prvi puta je zabilježena u reproduktivnom stadiju u venecijanskoj laguni, Jadransko more. U 2000. godini pronađene su tetrasporofite i muške i ženske gamete L. hakodatensis. Opisana su morfološka, anatomska i reproduktivna svojstva talusa i njihova učestalost u venecijanskoj laguni. Također su izneseni podatci o vegetaciji algi. Nalazi ove vrste se u posljednje vrijeme javljaju u Francuskoj, Španjolskoj, Rusiji, na Havajskom otočju i Australiji.
Ključne riječi: morske alge, Rhodophyta, Lomentaria hakodatensis, venecijanska laguna, Jadransko more ISSN: 0001-5113 ACTA ADRIAT., UDC: 597.35(447Languedoc)(262) AADRAY 47 (1): 73 - 78, 2006 Short communication
An unusual nine-ocellated common torpedo, Torpedo torpedo (Linnaeus, 1758) (Chondrichthyes: Torpedinidae), from southern France
Christian CAPAPÉ*, Olivier GUÉLORGET, Yvan VERGNE and Jean-Pierre QUIGNARD
Laboratoire d’Ichtyologie, Case 104, Université Montpellier II, Sciences et Techniques du Languedoc, 34095 Montpellier Cedex 05, France * Corresponding author, e-mail: [email protected]
A nine-ocellated Torpedo torpedo, caught off the Languedoc coast in southern France (northern Mediterranean) is described in this paper. This is the greatest number of ocellae recorded to date in this species.
Key words: Chondrichthyes, Torpedinidae, Torpedo torpedo, Languedoc, northern Mediterranean
INTRODUCTION common torpedos off the coast of Languedoc report on a specimen having nine ocellae. This Three torpedinid species are recorded off the specimen is herein described and compared with coast of Languedoc (southern France, northern specimens having five and six ocellae, that were Mediterranean; QUIGNARD et al., 1962): the caught in the same area. marbled torpedo, Torpedo marmorata (Risso 1810), the black torpedo, T. nobiliana (Bonaparte DESCRIPTION OF THE SPECIMENS 1835), and the common torpedo, T. torpedo (Linnaeus 1758). The first species is abundantly The three specimens were caught by gill-net and frequently landed. In contrast, the other two on sandy bottoms at depths of 10-20 m off the are rarely observed. coast of Languedoc between Sète and Palavas Torpedo torpedo is generally distinguished (Fig. 1). They are preserved in the Ichthyological from T. marmorata and T. nobiliana by the Collection of the Laboratoire d’Ichtyologie occurrence of five characteristic large eye- of the Université Montpellier II, Sciences et spots or ocellae on the dorsal surface. Different Techniques du Languedoc. One was an adult numbers of ocellae were described by CAPAPÉ male caught on 21 February 2004 (catalogue & DESOUTTER (1981) in specimens caught in no. Torp torp. 1; Fig. 2). Another specimen was Tunisian waters. They counted none to eight a pregnant female at the beginning of gestation, ocellae, but mostly five. Recent records of carrying fertilized eggs in uteri, caught on 11 74 ACTA ADRIATICA, 47(1): 73-78, 2006
pelvic was quite separate from the pectoral fins, subtriangular, and acute at the distal end. The tail was distinct with two dorsal fins and a well-developed caudal fin, the latter with a low careen on each side. The posterior tip of the pelvic fin was located before the origin of the second dorsal fin. Spiracles had eight short tentacles or knobs. Measurements and counts are summarized in Table 1. Disk width was 61.1-62.5%, disk length 43.1-47.0%, pre-oral length 9.7-9.9%, span of pelvic fins 26.6- 28.5%, pelvic anterior margin 12.0-13.1%, and caudal careen 16.3-17.2% of the total length. Pre-orbital length was 2.3-2.4 times the width Fig. 1. Map of French Mediterranean coast showing capture site (black star) of three Torpedo torpedo between the first gill-slits. Interorbital length specimens was 2.1-2.6 the width between the fifth gill- slits. Spiracles were 0.8-1.0 times the eye-ball April 2004 (Torp. torp 2; Fig. 3). The third was length. Tail length was 38.0-39.7% of the total an adult male caught on 23 May 2005 (Torp. length, 1.1-1.2 times the disk length, and 1.6 torp. 3; Fig. 4). Total lengths were 368, 383, and times the disk width. Total number of teeth in 267 mm, respectively, and weights were 690, upper and lower jaws were 22-24 and 20-22, 960, and 329 g, respectively. respectively. Dorsal and ventral surfaces were In all three specimens, the disk was rather entirely smooth. Dorsal surface was brownish rounded and subcircular, with an enlarged with whitish notches, belly was beige and pectoral confluent on the sides of the head. dark on margins. Ocellae were dark blue in the The snout was short and subtroncate, the center, encircled, dark, and yellowish.
Table 1. Measurements and counts carried out in three Torpedo torpedo caught off the coast of Languedoc References Torp. torp. 1 Torp. torp. 2 Torp. torp. 3 Sex Male Female Male Total mass (grammes) 690 732 329 Total length (millimetres) 368 383 267 Disc length 169 180 115 Disc width 225 240 167 Disc depth 5 6 4 Eyeball length 9 12 6 Cornea 8 9 6 Pre-orbital length 23 25 17 Inter-orbital length 19 22 13 Spiracle diameter 8 9 6 Interspiracular width 23 24 17 Space between eye and spiracle 4 5 3 Pre-oral length 36 38 26 Mouth width 25 28 18 First gill-slit 8 11 7 Second gill-slit 8 10 7 Third gill-slit 9 10 7 Fourth gill-slit 9 10 7 CAPAPÉ, GUÉLORGET, VERGNE & QUIGNARD: An unusual nine-ocellated torpedo from southern France 75
Table 1. Cont’ d Fifth gill-slit 8 9 6 Width between first gill-slit 53 56 40 Width between fifthgill-slit 43 46 33 Snout tip to eye 27 30 22 Snout tip to mouth 40 43 29 Snout tip to first gill-slit 80 84 63 Snout tip to fifth gill-slit 122 128 91 Snout tip to pelvic fin 180 184 128 Snout tip to vent 195 203 150 Pectoral fin anterior margin 113 118 83 Pectoral fin posterior margin 160 166 117 Pectoral fin inner margin 33 36 26 Pelvic fin anterior margin 44 47 35 Pelvic fin posterior margin 46 49 38 Pelvic fin inner margin 24 27 17 Span of pelvic fins 98 106 76 Clasper length 42 - 36 Tail base width 30 32 23 Tail base depth 25 27 17 Tail length 140 150 106 Snout tip to first dorsal 200 206 165 Snout tip to second dorsal 240 271 193 Snout tip to birth of caudal dorsal 275 312 225 Snout tip to birth of caudal ventral 272 310 220 Caudal superior 61 65 47 Caudal inferior 46 49 36 Caudal posterior 58 62 45 First dorsal anterior edge 47 49 36 First dorsal posterior edge 31 33 24 First dorsal inner edge 9 11 7 Second dorsal anterior edge 34 38 27 Second dorsal posterior edge 23 27 18 Second dorsal inner edge 9 12 7 Interdorsal distance 24 27 18 Second dorsal-caudal birth 29 33 22 Caudal careen length 60 66 46 Number of ocellae 5 6 9 Number of tooth rows in upper jaw 24 24 22 Number of tooth rows in lower jaw 22 22 20
Torp. torp. 1 had five ocellae classically 2 had four fertilized eggs in the left uterus and arranged in two lines, i.e., an anterior line with six in the right. The eggs weighed 11.4-12 g three ocellae, the middle one being slightly (mean 11.8±0.3). Torp. torp. 3 had nine ocellae, more anterior than the other two, and a posterior six ocellae arranged as in Torp. torp. 2, and line with two ocellae (Fig. 2). The five ocellae three smaller ocellae on the anterior part of the were similar in diameter. Torp. torp. 2 had six disk (Fig. 4). Of the three anterior ocellae, the ocellae, five arranged in two lines as in Torp. two smallest were near the outer margins of the torp. 1, and a sixth in the center (Fig. 3). The spiracles and the slightly larger one was on the six ocellae were similar in diameter. Torp. torp. left side of the disk. 76 ACTA ADRIATICA, 47(1): 73-78, 2006
Fig. 2. Adult male caught on 21 February 2004 Fig. 3. Adult female caught on 11 April 2004
Fig. 4. Adult male caught on 23 May 2005 CAPAPÉ, GUÉLORGET, VERGNE & QUIGNARD: An unusual nine-ocellated torpedo from southern France 77
DISCUSSION & DESOUTTER, 1981; CAPAPÉ et al., 2000). In contrast, the sixth ocellae in Torp. torp. 2 Morphology, measurements, and counts was located in the center of the five; such an are in agreement with TORTONESE (1956), BINI arrangement was recorded for the first time. (1967), QUIGNARD & CAPAPÉ (1974), CAPAPÉ & Nine ocellae is the most ocellae recorded to DESOUTTER (1981), FISCHER et al. (1987), and date, the previous record was eight ocellae in MEJRI 2004 et al. ( ). a male caught in Tunisian waters (CAPAPÉ & CAPAPÉ & DESOUTTER (1981) reported that DESOUTTER, 1981). the most recorded specimens had five ocellae The eggs carried by Torp. torp. 2 were and the next frequently reported had 0-4 ocellae. heavier than those carried by specimens from Specimens with more than five ocellae were Tunisian waters that ranged 2-7 g (QUIGNARD significantly less abundant. In specimens from & CAPAPÉ, 1974) and from Senegalese waters Tunisian and Senegalese waters with more than that ranged 6.2-8 g (CAPAPÉ et al., 2000). These five ocellae, the supernumerary ocellae were differences should be further investigated to be arranged outside the five ocellae (CAPAPÉ confirmed.
REFERENCES
BINI, G. 1967. Leptocardi, Ciclostomi, Selaci. In: MEJRI, H., J. BEN SOUISSI, J. ZAOUALI, A. EL Atlante dei pesci delle coste Italiane. Mondo ABED, O. GUÉLORGET & C. CAPAPÉ. 2004. Sommerso, Milano, pp. 1-206. On the recent occurrence of elasmobranch CAPAPÉ, C. & M. DESOUTTER. 1981. Nouvelle species in a perimediterranean lagoon: the description de Torpedo (Torpedo) torpedo Tunis southern lagoon (northern Tunisia). (Linné, 1758) (Pisces, Torpedinidae). Bull. An. Ser. Hist. Nat., 14(2):143-158. Mus. Natl. Hist. Nat., Paris, 7A, 4:1205- QUIGNARD, J.P. & C. CAPAPÉ. 1974. Recherches 1217. sur la biologie d’un Sélacien du golfe CAPAPÉ, C., A.A. SECK. & Y. DIATTA. 2000. de Tunis, Torpedo torpedo Linné, 1758 Reproductive biology of the common (ecologie, sexualité, reproduction). Bull. torpedo, Torpedo torpedo (Linnaeus, 1758) Inst. Océanogr. Pêche Salammbô, 3(1- from the coast of Senegal. Misc. Zool., 4):99-129. 23(1):9-21. QUIGNARD, J.P., A. RAIBAUT & J.P. TRILLES. 1962. FISCHER, W., M.L. BAUCHOT & M. SCHNEIDER. Contribution à la faune ichtyologique sétoise. 1987. Fiches FAO d’identification des Nat. Monspel. Série Zool., 4:61-85. espèces pour les besoins de la pêche. In: TORTONESE, E. 1956. Leptocardia, Ciclostoma, Révision Méditerranée et Mer Noire. Zone Selaci. In: Calderini (Editor). Fauna d’Italia, de Pêche 37, vol. II. Vertébrés. FAO, Rome, Bologna, pp. 1-334. pp. 761-1530.
Received: 26 January 2006 Accepted: 22 March 2006 78 ACTA ADRIATICA, 47(1): 73-78, 2006
Neuobičanjeni nalaz devetopjegne drhtulje Torpedo torpedo (Linnaues, 1758) (Chondrichthyes: Torpedinidae), u vodama južne Francuske
Christian CAPAPÉ*, Olivier GUÉLORGET, Yvan VERGNE i Jean-Pierre QUIGNARD
Laboratorij za ihtiologiju, P.P. 104, Sveučilište u Montpellier-u II, Znanost i tehnika Languedoc-a, 34095 Montpellier cedex 05, Francuska
*e-mail: [email protected]
SAŽETAK
U ovom radu se opisuje primjerak drhtulje, Torpedo torpedo iz obalnih voda Laguedoc-a (južna Francuska, sjeverni Mediteran) koja je imala 9 pjega što je do sada za ovu vrstu najveći zabilježeni broj.
Ključne riječi: Chondrichthyes, Torpedinidae, Torpedo torpedo, Languedoc, sjeverni Mediteran ISSN: 0001-5113 ACTA ADRIAT., UDC:597.587.2:639.32](261.1):595.12 595.12:[597.587.2:639.32](261.1) AADRAY 47 (1): 79 - 83, 2006 Short communication
Hepatoxylon trichiuri (Cestoda: Trypanorhyncha) plerocercoids in cage-reared northern bluefin tuna, Thunnus thynnus (Osteichthyes: Scombridae)
Ivona MLADINEO
Institute of Oceanography and Fisheries, P.O. Box 500, 21000 Split, Croatia e-mail: [email protected]
Northern bluefin tuna (Thunnus thynnus) were caught by purse seine boats and brought to a farm for a rearing cycle of 1.5 years. Mortalities occurred in the first weeks of acclimatization at the facility. Parasitological examination revealed plerocercoids of the cestode Hepatoxylon trichiuri embedded in the stomach mucosa. The larvae were found in 28.4% of the fish and the mean abundance was 3.12 per fish. Histopathology revealed disseminated erosion at the site of attachment, atrophy of fundic glands, lymphocytic migration, and hyperplasia of connective tissue in the lamina propria. These symptoms, however, together with the parasite abundance, could not have triggered the mortalities. This is the first record of this parasite in northern bluefin tuna.
Key words: histopathology, bluefin tuna, Hepatoxylon trichiuri, Cestoda
INTRODUCTION pathogens are parasitological reports from wild tuna populations or recent findings in farmed Cage rearing of northern bluefin tuna (Thun- fish (MUNDAY et al., 2003; MLADINEO & TUDOR, nus thynnus) in the Adriatic Sea is a relatively 2004; DEVENEY et al., 2005; MLADINEO, 2006). recent and growing type of aquaculture. Tuna Hepatoxylon trichiuri (Cestoda: Trypano- are caught from the wild and raised intensively rhyncha) has been isolated from diverse geo- in floating semi-offshore cages for six months to graphic areas and environmental conditions: 1.5 years. Fish are fed fresh anchovies and other from deep-water fish (KLIMPEL et al., 2001) to mixed small pelagic fish or frozen imported her- northern sea fishes such as redfish (Sebastes rings. Mortality is usually observed during the mentella) in Irminger Sea (BAKAY & MELNIKOV, acclimatization period and is presumed to be 2002), Atlantic salmon (Salmo salar; BAKKE & due to the lengthy transportation and handling HARRIS, 1998), and swordfish (ROSSO et al., 1997). period during transfer to the cages. Sudden or It is mainly regarded as a biological tag for iden- severe changes in abiotic parameters such as tification of fish stock arriving from southern temperature, weather conditions, and oxygen parts (SEWELL & LESTER, 1995; OLIVA & BALLÓN, also can induce mortality and, so far, only a 2002), while no histopathology associated with small proportion of mortalities in farmed tunas infection has been reported. have been attributed to pathogens (SAWADA et al., Merluccids (Macruronus magellanicus, 2002). The majority of studies concerning tuna Merluccius hubbis, M. gayi, M. capensis, 80 ACTA ADRIATICA, 47(1): 79-83, 2006
Macromesistius poutassou) harbor plerocercoids caused the mortality since these parasites had of H. trichiuri in the visceral cavity in a not previously been observed in bluefin tuna. variety of prevalence and abundance ranges Infected tissue was fixed in modified (KRZEPTOWSKI, 1980; KUSZ & TREDER, 1980; DAVIDSON’s fixative and processed for routine SARDELLA & TIMI, 1996; OLIVA, 2001). The parasite histology. Tissue was dehydrated in increasing was found encapsulated in the mesenteries of concentrations of ethanol, embedded in paraffin orange roughy (Hoplostethus atlanticus) from (Histowax, Leica), cut into 5-8 μm sections, and Australian waters (LESTER et al., 1988). Among stained with hematoxylin and eosin. Each section tuna species, H. trichiuri has been recorded was examined under a compound microscope at only from albacore (T. alalunga; JONES, 1991) 100 and 400x magnification. Photographs were and yellowfin tuna (T. albacares; BUSSIERAS & made using an Olympus C-4040 digital camera BAUDIN-LAURENCINE, 1973), species not found in and processed with Olympus DP-Soft software. the Mediterranean. RESULTS MATERIAL AND METHODS Hepatoxylon trichiuri larvae were found in Bluefin tuna (12-15 kg) were caught near 28.4% of the examined tuna. Mean abundance Jabuka Island, Adriatic Sea, at a depth of 20 was 3.12 per fish. Parasites were easily visible, m by commercial fishers and brought to the pale yellow, 20.2±3.1 by 0.4±0.2 mm, and farm on the northwestern part of Brač Island. difficult to detach from the tissues in which Mortalities occurred during the capture and they were found (Fig 1). They were found towing process, the transfer to cages, and the first mostly in the fundic region of the stomach. week at the facility. Dead fish were collected for Histological sections had erosions and parasitological examination. Plerocercoids of the deterioration of the mucosal columnar cestode H. trichiuri were isolated from stomach epithelium at the attachment site of the mucosa and identified according to KHALIL et al. plerocercoids (Fig. 2). At sites where (1994). It was suggested that the plerocercoids bothridial hooks penetrated the gastric glands,
Fig. 1. Hepatoxylon trichiuri from the stomach wall of northern bluefin tuna (Thunnus thynnus) MLADINEO: H. trychuri, plerocercoids in cage-reared northern bluefin tuna, Thunnus thynnus 81 the glands were atrophied and had sloughed abundance detected in this study, it is extremely off. Neighboring glands had compensatory unlikely that the infection led to the mortalities. hypertrophy and evidence of extensive mucus The stomach erosions did not involve deep production. Surface erosion was apparent, with stomach layers, so no ulcerations could be an overlying mass of detritus and secondary expected to have formed. Haemorrhages were bacterial infection. Focal hemorrhages focal and present in the early stage of infection were observed in younger processes but (during attachment of the plerocercoids) and connective tissue layers were not thickened. appeared to cease in later stages. Later, only a The submucosa under these erosions were minor connective tissue reaction and lymphocyte thickened and numerous lymphocytes were infiltration were observed. The atrophy of gastric present, however, the erosions did not penetrate glands was limited to the attachment site and did the submucosal stomach layer. The reaction in not impede ongoing secretion processes in non- the lamina propria consisted of hyperplastic infected stomachs. thickening of its layers. The parasite did The plerocercoids induced local changes not induce formation of a connective tissue in the stomachs with a mild inflammatory pseudocyst or capsule and there was no response. In stressful rearing conditions, such observable macrophage accumulation. shallow erosions can become the entry site for secondary pathogens (particularly bacteria) DISCUSSION and thereby threaten the health of the host. Pathological effects, combined with secondary Based on the histological changes associated infections that may occur during the 1.5 year with the H. trichiuri infection and the level of rearing cycle, require assessment, though in this
Fig. 2. Changes in stomach layers at the Hepatoxylon trichiuri. attachment site: disruption of the epithelial layer with slaughtered columnar epithelium (s), atrophied fundic glands (ag), compensatory hyper- trophied fundic glands in a deeper layer (hg), and lymphocyte infiltration (ly) 82 ACTA ADRIATICA, 47(1): 79-83, 2006 case mortalities were probably related to post- capsule was formed at the attachment site as capture trauma and stress. usual in chronic parasitic infections. It is worth noting the very nonspecific infection site of the plerocercoids. Pelagic fish usually harbor plerocercoids in the visceral ACKNOWLEDGEMENTS cavity after the parasite penetrates the stomach The preliminary study and collected data wall. In the studied case, they were found could not have been achieved without the mostly in the fundic region of the stomach. One possible explanation is that the plerocercoids enormous technical support of the staff at the were isolated during the penetration process, tuna facility, especially its former employees however no parasites were recovered from the Mr. Ivor JEFTIMIADES and Ms. Ivana MILETIĆ. visceral cavity, suggesting that the parasite The study was part of the project “Biological actually lives and inhabits the stomach and Ecological Characteristics of New Species without migrating in the viscera. However, the in Aquaculture” founded by the MINISTRY OF histological changes are not strong evidence SCIENCE, EDUCATION AND SPORT of the REPUBLIC for a prolonged process since no connective OF CROATIA.
REFERENCES
BAKAY, Y.I. & S.P. MELNIKOV. 2002. Vertical Hepatoxylon trichiuri, and parasitic copepod structure of Sebastes mentella concentrations Parabrachiella australis in juvenile Merluc- in the pelagic open part of the Irminger cius capensis off Namibia. Acta Ichthiol. Sea. Scientific Council Meeting, June 2002. Pisc., 10(2): 35-44. NAFRO SCR Doc. 02/10, pp. 1-21. KUSZ, W. & A. TREDER. 1980. Parasitic fauna BAKKE, T.A. & P.D. HARRIS. 1998. Diseases and of European blue whiting, Micromesistius parasites in wild Atlantic salmon (Salmo poutassou (Risso, 1810). Acta Ichthiol. salar) populations. Can. J. Fish. Aquat. Sci., Piscat., 10(2): 45-58. 55 (Suppl. 1):247-266. LESTER, R.J.G., K.B. SEWELL, A. BARNES & K. BUSSIERAS, J. & F. BAUDIN-LAURENCIN. 1973. Les EVANS. 1988. Stock discrimination of orange helminthes parasites des thons tropicaux roughy, Hoplostethus atlanticus, by parasite (Helminthic parasites of tropical tuna). Rev. analysis. Mar. Biol., 99: 137-143. Elev. Med. Vet. Pay Trop., 26:13-19. MLADINEO, I. 2006. Histopathology of five DEVENEY, M.R., T.J. BAYLY, C.K. JOHNSTON & B.F. species of Didymocystis spp. (Digenea: NOWAK. 2005. A parasite survey of farmed Didymozoidae) in cage reared Atlantic southern bluefin tuna Thunnus maccoyii bluefin tuna (Thunnus thynnus thynnus). (Castelnau). J. Fish Dis., 28:279-284. Vet. Res. Comm. (in press). JONES, J.B. 1991. Movements of albacore tuna MLADINEO, I. & M. TUDOR. 2004. Digenea of (Thunnus alalunga) in the south Pacific: Adriatic cage-reared bluefin tuna Thunnus evidence from parasites. Mar. Biol., 111:1- thynnus thynnus. Bull. Eur. Assoc. Fish 9. Pathol., 24(3): 144-153. KHALIL, L.F., A. JONES & R.A. BRAY. 1994. Keys MUNDAY, B.L., Y. SAWADA, T. CRIBB & C.J. to the cestode parasites of vertebrates. CAB HAYWARD. 2003. Diseases of tunas, Thunnus Int., Hertfordshire, UK. pp 51-148. spp. J. Fish Dis., 26: 187-206. KLIMPEL, S., A. SEEHAGEN, H.W. PALM & H. OLIVA, M.E. 2001. Metazoan parasites of ROSENTHAL. 2001. Deep-water Metazoan Macruronus magellanicus from southern Fish Parasites of the World, 1st ed. Logos Chile as biological tags. J. Fish Biol., 58: Verlag, Berlin, 1316 pp. 1617-1622. KRZEPTOWSKI, M. 1980. Occurrence of larval OLIVA, M.E. & I. BALLÓN. 2002. Metazoan parasites nematode Anisakis simplex larval cestode of the Chilean hake Merluccius gayi gayi as MLADINEO: H. trychuri, plerocercoids in cage-reared northern bluefin tuna, Thunnus thynnus 83
a tool for stock discrimination. Fish. Res., SAWADA, Y., S. MIYOSHITA, O. MURATA & H. KUMAI. 56:313-320. 2002. Problems in the seedling production of ROSSO, F., G. GANDINI & M.T. MANFREDI. 1997. northern BFT, Thunnus orientalis, Temmnich Parasites of imported swordfish (Xiphias and Schlegel. In: Proc. Seafarming Today & gladius L). Boll. Soc. Ital. Patol. Itt., Tomorrow. Eur. Aquacult. Soc. Trieste, Italy, 9(21):39-44. pp. 464-465. SARDELLA, N.H. & J.T. TIMI. 1996. Parasite SEWELL, K.B. & R.J.G. LESTER. 1995. Stock communities of Merluccius hubbis from composition and movement of gamefish, the Argentinian-Uruguayan common fishing Rexea solandri, as indicated by parasites. zone. Fish. Res., 27:81-88. Can. J. Fish. Aquat. Sci., 52(1):225-232.
Received: 26 January 2006 Accepted: 27 March 2006
Nalaz plerocerkoidne trakavice Hepatoxylon trichiuri (Cestoda:Trypanorhyncha) u kavezno uzgojenoj sjevernoatlantskoj plavoperajnoj tuni Thunnus thynnus
Ivona MLADINEO
Institut za oceanografiju i ribarstvo, P.P. 500, 21000 Split, Hrvatska e-mail: [email protected]
SAŽETAK
Plavoperajne tune (Thunnus thynnus) ulovljene su plivaricama i tegljene do uzgajališta za uzgojni ciklus u trajanju od godine i pol dana. Parazitološka pretraga je provedena na uginućima nastalim tijekom prvih tjedana aklimatizacijskog razdoblja na uzgajalištu, otkrivajući plerocerkoide trakavice Hepatoxylon trichiuri uklopljene u sluznicu želuca. Ličinke su izolirane u 28.4 % riba, srednje abundancije od 3.12 po ribi. Cilj istraživanja je bio utvrđivanje poveznosti uginuća i količine nametnika, odnosno histopatološki učinak plerocerkoidna na domaćina. Histopatološki nalaz otkrio je diseminirane erozije na mjestu prihvaćanja nametnika, atrofiju fundusnih žlijezda, migraciju limfocita i hiperplaziju vezivnog tkiva lamine proprie želuca. Međutim, ove promjene zajedno s nađenom abundancijom nametnika nisu mogle potaknuti uginuća. Ovo je također i prvi nalaz ovog nametnika u plavoperajnoj tuni.
Ključne riječi: histopatologija, plavoperajna tuna, Hepatoxylon trichiuri, Cestoda
ISSN: 0001-5113 ACTA ADRIAT., UDC: 595.384(497.5 Rijeka) (262.3) AADRAY 47 (1): 85 - 88, 2006 Scientific note
First record of Hippolyte prideauxiana Leach, 1817 (Crustacea, Decapoda, Caridea) in the Adriatic Sea
Marin KIRINČIĆ
Natural History Museum Rijeka, Lorenzov Prolaz 1, 51000 Rijeka, Croatia
During the last ten years, several decapod species were recorded in the Adriatic Sea for the first time. Such a rapid increase in the number of recorded species of decapod crustaceans is the result of the increased number of carcinologists engaged in SCUBA diving. In 2002, during the routine Natural History Museum of Rijeka SCUBA fieldwork, the caridean shrimp, Hippolyte prideauxiana Leach, 1817, was collected at Kostrena near the city of Rijeka in the northern Adriatic. This record, the first for the Adriatic Sea, widens the previously known geographic distribution of this species.
Key words: Decapoda, Hippolyte prideauxiana, Adriatic Sea, first finding
INTRODUCTION surface-operated gears. Earlier research was mostly based on material collected with trawl In recent years, the number of decapod species gears and grabs on circa-littoral and lower infra- recorded in the Adriatic Sea has continually littoral soft grounds. increased despite the fact that the Adriatic Sea is one of the most thoroughly explored METHODS AND RESULTS regions in the Mediterranean (HELLER, 1863; PESTA, 1918; ŠTEVČIĆ, 1990, 1995, 2002; KIRINČIĆ, The 2002 field research was conducted by 2003). The main reason for the recent finding the Natural History Museum of Rijeka in the of previously unrecorded species in this area northern Adriatic (Fig.1). The shrimps were is the use by carcinologists of SCUBA diving collected by SCUBA diving across the transect equipment to collect decapods. This technology at a depth of 9 m where the bottom is composed allows investigation of previously unexplored of sparse rocks and pebbles with the biocenosis microhabitats of the infra-littoral zone. Such of “infra-littoral algae of shaded areas” (PERES habitats include marine caves and holes as well & PICARD, 1964). The dominant macroalgae there as pebbly and rocky interstitia. This method, are the green alga, Halimeda tuna, and the brown together with various SCUBA accessories, is algae of low thalli, Dictyota dichotoma and D. also useful for collecting miniature decapods linearis, while the red algae, Laurencia obtusa of the Anapagurus, Hippolyte, and Salmoneus and Peyssonnelia squamaria, are somewhat genera that are rarely caught with traditional rarer. At 20 m, the rocky bottom turns into a 86 ACTA ADRIATICA, 47(1): 85-88, 2006
Fig. 1. Map of the investigated locality with the location of the newly-found specimens marked by an arrow
muddy, sandy, and detritic bottom with the A. bifida (NOUVEL, 1953; LEONARD & JEAL, biocenosis of “coastal detritic bottoms” and its 1984; D’UDEKEM D’ACOZ, 1996). The specimens surface is covered by algae of the Polysiphonia were gathered together with A. mediterranea genus. to which they were clinging. Three specimens The research resulted in the collection of were collected, but only one was preserved. a newly discovered decapod species (Fig.2), The preserved specimen is the largest ever Hippolyte prideauxiana Leach, 1817, near recorded for this species (total length 24 mm) Stara Voda (45°17.586’N; 14°30.356’E) and is kept in the crustacea collection of the in the Žurkovo (Kostrena) municipality in Natural History Museum in Rijeka, under the February 2002. Identification was based on registration number C1324. the key and description in a monograph on the Hippolyte genus (D’UDEKEM D’ACOZ, 1996). The DISCUSSION characteristic color pattern and commensalism with the crinoid Antedon mediterranea left no The present record, the first for the Adriatic doubt about its identity. The species is sometimes Sea, considerably widens the known geograph- found in commensalism with the crinoid ic distribution of the species. Hippolyte pride- KIRINČIĆ: First record of H. prideauxiana Leach, 1817 in the Adriatic Sea 87
Fig. 2. Hippolyte prideauxiana Leach,1817 (total length 24 mm), discovered in Stara Voda, Kostrena (northern Adriatic) auxiana is a species with an Atlantic-Mediter- the discovery of other previously unrecorded ranean distribution (D’UDEKEM D’ACOZ, 1999). species in these areas. Since it had already been recorded in the Aegean and Ionian Seas (D’UDEKEM D’ACOZ, ACKNOWLEDGEMENTS 1996), it was only a matter of time until it would be found in the Adriatic as well. However, as I would like to express my sincere gratitude previous investigations in this area did not for cooperation in the identification of the record it, it is presumed to be an uncommon specimen as well as helpful suggestions in species here. the writing of this paper to Cédric D’UDEKEM Future systematic biological expeditions D`ACOZ and Zdravko ŠTEVČIĆ. Also, I am in other Adriatic under-explored habitats such very grateful to Milvana ARKO-PIJEVAC for as estuaries, marine caves, submarine springs, her assistance in the fieldwork and for the and bathyal grounds could most likely result in references of biological descriptions.
REFERENCES
D’UDEKEM D’ACOZ, C.D. 1996. The genus Hippolyte Méditerranée et des eaux continentales Leach, 1814 (Crustacea: Decapoda: Caridea: adjacentes au nord de 25°N. (Inventory and Hippolytidae) in the east Atlantic Ocean and distribution of the Crustacea Decapoda in the Mediterranean Sea, with a checklist of northeastern Atlantic Ocean, Mediterranean all species in the genus. Zool. Verh. Leiden, Sea and adjacent continental waters, north 303:1-133. of 25°N.) Patrimoines Naturels (MNHN/ D’UDEKEM D’ACOZ, C.D. 1999. Inventaire et SPN), 40:1-383. distribution des crustacés décapodes HELLER, C. 1863. Die Crustaceen des Südlichen de l’Atlantique nord-oriental, de la Europa. Crustacea Podophthalmia. (The 88 ACTA ADRIATICA, 47(1): 85-88, 2006
Crusta ceans of Southern Europe. Crus- de bionomie bentique de la Méditerranée. tacea Podopphthalmia). W. Braumüller, (The new manual for the bionomy of the Wien, 336 pp. Meditterannean Sea benthos). Recl. Trav. KIRINČIĆ, M. 2003. Brachycarpus biunguiculatus Sta. Mar. Endoume, 31, Fasc. 23:5-114. (Lucas, 1846): a new species of shrimp PESTA, O. 1918. Die Decapodenfauna der Adria. for the Adriatic Sea (Decapoda, Caridea). Versuch einer Monographie (The decapod Crustac. Int. J. Crustac.Res., 76(7):891-894. fauna for the Adriatic Sea. An attempt of a LEONARD, A. & F. JEAL. 1984. Hippolyte huntii momograph). Deuticke, Leipzig and Vienna, (Gosse, 1877), a first record from the east 500 pp. coast of Ireland with notes on other animals ŠTEVČIĆ, Z. 1990. Check list of the Adriatic associated with the crinoid Antedon. Ir. Nat. J., decapod Crustacea. Acta Adriat., 31:183- 21(8):357-358. 274. NOUVEL, H. 1953. Un Hippolyte (Crust-Décap. ŠTEVČIĆ, Z. 1995. Contribution to the faunistic Nat.) méconnu, nouveau pour les côtes de list of Adriatic decapod Crustacea. Nat. France et commensal de la comatule Antedon bifida. (New data for the genus Hippolyte Croat., 4(2):113-115. (Crust-Decap. Nat.) of the French coast, ŠTEVČIĆ, Z. 2002. New observations on the commensals of crinoid Antedon bifida). Adriatic decapod fauna (years 1990-2000). Arch. Zool. Expér. Gén., 90:71-86. Crustac. Int. J. Crustac.Res., 75(3-4):643- PERES, J.M. & J. PICARD. 1964. Nouveau manuel 647.
Received: 23 May 2005 Accepted: 02 December 2005
Prvi nalaz kozice Hippolyte prideauxiana Leach, 1817 za Jadransko more (Crustacea, Decapoda, Caridea)
Marin KIRINČIĆ
Prirodoslovni muzej Rijeka, Lorenzov prolaz 1, 51000 Rijeka, Hrvatska
SAŽETAK
Zadnjih desetak godina u Jadranu je zabilježeno nekoliko novih vrsta desetonožnih rakova. Rast broja nalaza dekapoda u kratkom vremenskom roku možemo zahvaliti većoj aktivnosti znanstvenika karcinologa istraživanju podmorja metodom autonomnog ronjenja. Terenskim radom Prirodoslovnog muzeja Rijeka 2002. godine pronađen je primjerak kozice Hippolyte prideauxiana Leach, 1817, na lokaciji Stare vode u Kostreni pored Rijeke. Ovaj nalaz, prvi za Jadransko more, proširio je dosad poznatu geografsku rasprostranjenost spomenute vrste.
Ključne riječi: Decapoda, Hippolyte prideauxiana, Jadransko more, prvi nalaz A1
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