Aquaculture Research, 2006, 37, 538^542 doi:10.1111/j.1365-2109.2006.01451.x

SHORT COMMUNICATION Studies on the recently discovered crayfish, Austropotamobius torrentium (Shrank, 1803), in Turkey: morphological analysis and meat yield

Muza¡er Mustafa Harlıogfl lu1 &UtkuGˇner2 1Fisheries Faculty, Firat University,Elazigfl ,Turkey 2Department of Biology,Faculty of Arts & Sciences, Trakya University,Edirne, Turkey

Correspondence: M Mustafa Harliogfl lu, Fisheries Faculty, Firat University,23119 Elazigfl ,Turkey. E-mail: mharlioglu@¢rat.edu.tr

The only native freshwater cray¢sh species of Turkey ci Schikora) whose presence was reported by several is the narrow-clawed cray¢sh, Astacus leptodactylus authors (Rahe & Soylu1989; Oray1990). Astacus lepto- (Esch., 1823) (Geldiay & KocataS1970; E re ncin & K˛k- dactylus has been introduced to many freshwaters in sal 1977; K˛ksal 1988; Holdich 2002; Skurdal & Taug- Turkey after 1985 because of its commercial impor- bol 2002; Harliogfl lu 2004). This species was ¢rst tance and declining catches from traditional good ¢sh- identi¢ed from Kayseri, Bursa and I˙stanbul (Bott eries. Today, there are 33 important A. leptodactylus 1950). It is naturally and widely distributed in lakes, harvesting areas throughout Turkey (Harliogfl lu, Bar- ponds and rivers in di¡erent parts of Turkey, and im,Tˇrkgˇlˇ & Harliogfl lu 2004). The total harvest va- some very large populations exist. According to Gel- lue from these areas in 2002 was reported to be diay and KocataS (1970) three subspecies of Astacus 1850 tonnes (Anonymous 2002). However, culture of exist in Turkey.These are A. leptodactylus leptodacty- this species in captivity is not practiced inTurkey. lus, A. leptodactylus salinus and A. colchicus. However, The stone cray¢sh, A. torrentium, is indigenous to Albrecht (1983) considered A. colchicus to be a sub- Europe and is mainly con¢ned to central and south- species of A. astacus. Therefore, A. astacus may also eastern countries. It reaches its northerly limit in be present in Turkey, but up to now there have been Germany and the Czech Republic, westerly limit in no reports of it (Holdich 2002). Starobogatov (1995) Luxembourg, southerly limit in Greece, and easterly also mentioned that A. colchicus might be found in limit in Bulgaria (Holdich 2002). It had not been pre- the vicinity of I˙stanbul, and it could have been intro- viously recorded fromTurkey (Erencin & K˛ksal 1977; duced in eastern Turkey. K˛ksal1988; Holdich 2002; Skurdal & Taugbol 2002). Freshwater cray¢sh is a popular luxury food in However, its presence has recently been noted in the many West European countries. Since the domestic Velika River (a tributary of the Rezovska River) in consumption of cray¢sh inTurkey was very low (Eren- European Turkey by Trontelj,Yoichi and Boris (2005). cin & K˛ksal 1977),Turkey was the largest supplier of Little is known about this cray¢sh in European Tur- A. leptodactylus toWestern Europe from1970 (or possi- key so it was decided to undertake an analysis of its bly earlier) until 1986 (K˛ksal 1988; Oray 1990). The morphology and abdominal meat yield in order to as- peak cray¢sh production was reached in the early sess it potential for aquaculture in this study. 1980s, with over 5000 tonnes being exported in 1984. Cray¢shwere exported to a number of European coun- Materials and methods tries, of which France and Sweden were the main buyers (K˛ksal 1988). After 1985, cray¢sh production Sixty males and 224 females of A. torrentium (size was reduced dramatically in most Turkish lakes as a range: 20^45 for males and 20^40 mm carapace result of the cray¢sh plague fungus (Aphanomyces asta- length (CL) for females) were caught from the Velika

538 r 2006 The Authors. Journal Compilation r 2006 Blackwell Publishing Ltd Aquaculture Research, 2006, 37, 538^542 Studies on the recently discovered cray¢sh in Turkey MMHarliogfl lu&UGˇner

River, Kirklareli,Turkey. Although a few larger cray- The regression analysis of body weight versus CL ¢sh (53 and 62 mm CL for males and 48 and 68 mm yielded regression coe⁄cients (slopes) lower than 3, CL for females) were caught, these were not included indicating negative allometric growth in male and fe- in the study because of their extreme values.The spe- male A. torrentium (slopes: 2.89 for males and 0.73 for cimens were sorted by their sex, washed and then females). frozen at À 20 1C for further processing. A signi¢cant sexual dimorphism was observed in Measurements of carapace width, abdomen the body weight, abdomen width, chelae width, che- length, abdomen width, chelae length, chelae width lae length and cheliped length between male and and cheliped length were documented and used to female of A. torrentium ofthesamesize.Malesof determine sexual dimorphism between males and fe- A. torrentium had signi¢cantly heavier body weight males. The positions, from which the measurements than the females (mean body weight 512.29 Æ 5.98 g were taken, based upon the techniques of Rhodes for males and 9.92 Æ 3.04 g for females). Males also and Holdich (1979). Measurements were made to the had signi¢cantly longer cheliped and chelae, and sig- nearest1mm using a £exible metal ruler. For abdom- ni¢cantly wider chelae than those of the females inal meat yields, cray¢sh and tissue were weighed to (Po0.001for each case). However, females had signif- the nearest 0.001g. After opening the abdomen by icantly (Po0.001) wider abdomen than males (mean slitting, the meat was carefully removed using a scal- abdomen width 515.03 Æ 2.40 mm for males and pel and forceps. Because the claws of A. torrentium 16.73 Æ 1.84 mm for females). In addition, males had are relatively small, economic meat recovery is prob- wider carapace than did females (16.30 Æ 2.93mm for ably not viable; hence, meat yield from the claws was males and 15.95 Æ 2.51for females), and females had not examined. In order to determine allometric rela- longer abdomen than males (36.69 Æ 3.73 mm for tionship and to observe whether or not abdominal females and 36.01 Æ 4.84 mm for males). (tail) meat yield and/or body weight increased at a Regression analysis of abdomen meat yield versus rate greater than the cube of the CL with growth, CL showed that the abdominal meat yield of males slopes were investigated by applying regression ana- and females does not increase at a greater rate than lysis of log transformed variables in the form: log the cube of the CL (slopes: 2.61for males and 1.19 for y 5log (a)1log (b) x, where a value of 43.0 for the females; N< 5 26, N, 5 47). The formulae for regres- constant b was taken to indicate that the abdominal sion analyses are (abdomen meat yield versus CL) as meat yield (or body weight) increased at a greater rate follows: (positive allometry) than the cube of CL (Romaire, Forester & Avault 1977). Analysis of variance and log y 5log (a) Duncan’s new multiple range test were also used for 1log (b) xr2 Slope the statistical analysis of the data to show the di¡er- ences between sexes in morphology and abdominal log male meat y 5 À 4.0579 0.621 2.6128 meat yield (signi¢cant di¡erence, a 50.05). yield versus 12.6128 x log CL Results log female meat y 5 À 1.8487 0.073 1.1857 yield versus 11.1857 x In both sexes, a linear relation was observed between log CL CL and body weight (r2 50.89 for males and r2 50.79 for females). The formulae of regression analyses are There was a signi¢cant di¡erence in the abdomen (sample no. 560 for males and 224 for females): meat yield between males and females (Po0.001). It was 1.183 Æ 0.45 g for males (mean CL 5 37.60 m m) log y 5log (a) and 0.86 0.32 g for females (mean CL 31.20 m m). 2 Æ 5 1log (b) xr Slope In addition, big sized males (37^44 mm CL) had sig- ni¢cantly (Po0.001) more abdomen meat yield than log male CL y 5 À 3.2932 0.888 2.8895 thesmallsizedones(30^36mmCL)(1.45Æ 0.30 g for versus log 12.8895 x the big size males and 0.97 Æ 0.23 g for the small size body weight males). There was not a signi¢cant di¡erence log female CL y 5 À 13.213 0.7821 0.7299 (P40.05) in the abdomen meat yield of males and fe- versus log 10.7299 x males of the same size (30^36 mm CL). It was body weight 0.91 Æ 0.33 g for males and 0.97 Æ 0.23 g for females.

r 2006 The Authors. Journal Compilation r 2006 Blackwell Publishing Ltd, Aquaculture Research, 37, 538^ 542 539 Studies on the recently discovered cray¢sh in Turkey MMHarliogfl lu&UGˇner Aquaculture Research, 2006, 37, 538^ 542

However, the abdomen meat yields as percentage of weight of males is considerably heavier than that of body weight of males and females were 6.61% and females because of the greater mineralization of the 9.40% respectively. shell (exoskeleton), particularly the chelipeds. In per- centage terms, the amount of abdomen meat yield for several di¡erent species has been reported to be be- Discussion and conclusion tween 10% and 40% of body weight (Lee & Wickins In general, isometric and negative allometric 1992). For example, this value was found to be 19.6% growths have been observed for female cray¢sh. For for male A. astacus and 17.5% for female A. astacus example, for Cherax destructor (slopewet weigth versus (Lindqvist & Louekari 1975), 14.79% for male

CL 5 2.61), C. quadricarinatus (slope 5 2.92) and for P. leniusculus and 12.34% for female P. leniusculus, C. tenuimanus (slope 5 2.76) (Austin 1995); for and 12.60% for male A. leptodactylus and 12.45% for A. leptodactylus (slope 5 2.82) (K˛ksal 1988), female A. leptodactylus (Harliogfl lu & Holdich 2001), (slope 5 2.74) (Harliogfl lu 1996); for Pacifastacus trow- 27.40% for male A. pallipes and 23.20% for female bridgii (slope 5 3.07) (Mason 1975); for P. leniusculus A. pallipes (Rhodes & Holdich 1984). In our study, (slope: 2.89) (Harliogfl lu 1996). On the other hand, slope values of o3 for abdomen meat yield for male positive allometric and isometric growths have and female A. torrentium in the regression analysis been observed in general for male cray¢sh. For indicated that meat content did not increase at a rate example, for A. astacus (slope 5 3.83) (Pursiainen, greater than the cube of CL as the cray¢sh grew. Saarela & Westman 1988); for C. quadricarinatus Negative allometry for abdomen meat yield was also (slope 5 3.29) and C. destructor (slope 5 3.22) (Austin observed for the males and females of A. leptodactylus 1995); fo r P. trowbridgii (slope 5 3.59) (Ma s on 1975); and P. leniusculus (Harliogfl lu 1996). In a study, Huner for A. leptodactylus (slope 5 3.13) (K˛k sa l 1988) a nd (1993) studied the meat yield in some species belong- (slope 5 3.25) (Harliogfl lu 1996); for P. leniusculus ing to Cambaridae and only the abdomen meat was (slope 5 2.97) (Harliogfl lu 1996). Our study indicates considered. He found that meat yield ranged that both male and femaleA. torrentium exhibit nega- from 1.79 to 3.91g for the most popular species tive allometric growth. This is thought to be a conse- and P. zonangulus. Similar levels quence of the heavy exoskeleton (shell) in this of tail meat for P.clarkii were also found in a di¡erent species. Even, body weights of small sized male and study (Harliogfl lu 1996). In a study, Harliogfl lu and female individuals of A. torrentium that have heavy Holdich (2001) found that the mean abdomen meat body skeletons do not increase faster than the cube yield of male and female P. leniusculus ranged of their CLs. between 2.75^3.03 g for males and 2.28^2.76 g for Sexualdimorphism hasbeenobserved intheabdo- females. Those of male and female A. leptodactylus men size, carapace width and chelipeds (claws) in were 2.32^3.26 g and 2.53^2.91g respectively. many mature cray¢sh species (Lowery1988). In gen- However, K˛ksal (1988) found that maleA. leptodacty- eral, male cray¢sh have larger and heavier chelipeds lus produced an average of 4.25 g of tail meat and that than females, and female cray¢sh have a bigger and of females was 4.41g. These di¡erences in the meat wider abdomen. In addition, males are heavier than yield content might be due to the state of maturity, females (Romaire et al. 1977; Rhodes & Holdich 1979; size, condition and location as well as the way the Harliogfl lu1996). Our study also showed that males of meat was prepared for analysis.When compared with A. torrentium had signi¢cantly heavier body weight the above-mentioned species, considerably lower ab- than females. The males also had signi¢cantly bigger domen meat yield content was observed forA. torren- cheliped, chela, and wider chela than those of the fe- tium (mean 1.18g for males and 0.86 g for females). males, whereas the females had signi¢cantly wider Similarly, Obradovic, Sekulic and Rac (1988) found abdomen than did the males. However, meat extrac- that the abdomen meat yield was not the same for tion from the chelipeds appears uneconomic because males and females, i.e. a greater increase in weight of their overall relatively small size. was found in the abdomen meat yield of males than In the present study,the abdominal meat yield pro- in those of females. duced by male A. torrentium was found to be signi¢- Austropotamobius torrentium is of little commercial cantly higher than that of female A. torrentium. interest because it only reaches a maximum size of However, when expressed as a percentage of the body about 11cm and a maximum weight of about 70 g weight, that of females (9.40%) was found to be high- (Troschel, Schulz & Berg 1995). According to Lowery er than that of males (6.61%).This is because the body (1988), some populations of A. torrentium are not

540 r 2006 The Authors. Journal Compilation r 2006 Blackwell Publishing Ltd, Aquaculture Research, 37, 538^542 Aquaculture Research, 2006, 37, 538^542 Studies on the recently discovered cray¢sh in Turkey MMHarliogfl lu&UGˇner exploited because of their small size.Therefore, it was the potential or actual impacts that A. torrentium concluded that the exploitation of A. torrentium can could be having on associated ecosystems. thus be considered to be negligible. On the other hand, Laurent (1988) also stated that A. torrentium is sympatric with the largerA. astacus and in the coun- tries where they both live, ¢shermen do not bother References with it, preferring the larger cray¢sh. Based on the results of this investigation, in conjunction with the Albrecht H. (1983) Besiedlungsgeschichte und ursprˇnglich fact that A. torrentium only reaches a maximum size holozneVerbreitung der europischen Flusskrebe. Spixi- of about11cm and maximum weight of about 70 g, it ana 6,61^77. would appear that this species in Turkey would not Anonymous (2002) Fisheries Statistics of Prime Ministry appear to be an economically exploitable resource. State Planning Organization, Republic of Turkey,Ankara, Turkey It has been suggested that there has been a reduc- Austin C.M. (1995) Length-weigth relationships of cultured tion in the range of A. torrentium. Therefore, like species of Australian freshwater cray¢sh of the genus other native European cray¢sh species (A. astacus Cherax. Freshwater Cray¢sh10,410^418. and A. pallipes), A. torrentium is also considered to be Bott R. (1950) Die Flusskrebse Europas. Abhandlungen der a threatened species (Taylor 2002). Consequently, it Senckenbergischen naturforschungenden Gesellschaft 483, has been listed under an‘endangered’category in the 1^36. Austrian Red List of endangered species and the An- Erencin Z. & K˛ksal G. (1977) On the cray¢sh, Astacus nex IV of European Community Directives for the leptodactylus, in Anatolia. Freshwater Cray¢sh 3,187^192. Conservation of Natural habitats and wild Flora and Geldiay R. & KocataS A. (1970) The preliminary report Fauna (97/62/EU) as a species requiring special con- about the and distribution of Astacus () servation measures (Streissl & H˛dl 2002). of Turkey (in Turkish with english summary).Scienti¢c Reports of the Faculty Science, Ege University No: 94, Austropotamobius torrentium occupies the middle pp.1^11. of Europe in the upper tributaries of the right side of Harliogfl lu M.M. (1996) Comparative biology of the signal cray- the Rhine in Germany, till the con£uence with the ¢sh, P. leniusculus (Dana), and the narrow-clawed cray¢sh, Lahn, and the left side till the con£uence with the A. leptodactylus Esc., Ph.D. Thesis, University of Notting- Mosel. It has been observed in the vicinity of Stras- ham, 435 pp. bourg and from many locations in the north-east of Harliogfl lu M.M. (2004) The present situation of freshwater Switzerland in tributaries of the Rhine. It has also cray¢sh, Astacus leptodactylus (Eschscholtz, 1823) in Tur- been caught in the Danube system from the springs key. Aquaculture 230,181^187. to the lron Doors in Romania and from Bavaria, Aus- Harliogfl lu M.M. & Holdich D.M. (2001) Meat yields in the in- tria, Bohemia, the northern part of Hungary, former troduced cray¢sh, Pacifastacusleniusculus and A. leptodac- Yugoslavia and Albania. More to the south, it was tylus, from British waters. Aquaculture Research 32,411^ 417. present in the Vardar system inYugoslavian Macedo- Harliogfl lu M.M., Barim ., Tˇrkgˇlˇ I˙.&Harliogfl lu A.G. nia (Laurent 1988). Therefore, it was stated that the (2004) Potential fecundity of an introduced population of 1 distribution of A. torrentium extends from 50 N freshwater cray¢sh, Astacus leptodactylus leptodactylus in Germany to 411N in Macedonia and 81Eonthe (Eschscholtz, 1823). Aquaculture 230, 189 ^ 195. Rhine to about 241E in Romania (Laurent 1988). Holdich D.M. (2002) Present distribution of cray¢sh in Eur- However, the present study shows that the range ope and some adjoining countries. Bulletin Francais de la of A. torrentium extends into the European part of Peche et de la Pisciculture 367,611^650. Turkey. However, whether this is a natural extens- Huner J.V. (1993) Recovery of edible products from some ion of its range, or if it has been introduced into common North American orconectic and procambarid European Turkey by man is not known. A recent cray¢sh (Cambaridae) with emphasis on Procambarus study of13 rivers and brooks close to theVelika River clarkii (Girard) and Procambarus zonagulus Hobbs & Hobbs. Freshwater Cray¢sh 9, 28^37. has not revealed any other populations (U. Gˇner, K˛ksal G. (1988) A. leptodactylus in Europe. In: Freshwater personal observation, 2005). Cray¢sh: Biology, Management and Exploitation (ed. by In conclusion, because of its relatively small size, D.M. Holdich & R.S. Lowery), pp. 365^400. Croom Helm low abdominal meat yield and limited distribution in Press, London. European Turkey, it is clear that A. torrentium is of Laurent P.J. (1988) A. pallipes and A. torrentium with obser- limited exploitation interest. However, ecological re- vations on their interactions with other species in Europe. search should be conducted in the area to determine In: Freshwater Cray¢sh: Biology, Management and Exploi-

r 2006 The Authors. Journal Compilation r 2006 Blackwell Publishing Ltd, Aquaculture Research, 37, 538^ 542 541 Studies on the recently discovered cray¢sh in Turkey MMHarliogfl lu&UGˇner Aquaculture Research, 2006, 37, 538^ 542

tation (ed. by D.M. Holdich & R.S. Lowery), pp. 341^364. Rhodes C.P.& Holdich D.M. (1984) Length-weight relationship, Croom Helm, London and Timber Press, Oxford, UK. muscle production and proximate composition of the fresh- Lee D.O’C. & Wickins J.F. (1992) Farming. Black- water cray¢sh A. pallipes. Aquaculture 37, 107^123. well Scient. Publications.392 pp. Romaire R.P., Forester J.S. & Avault J. (1977) Length-weight Lindqvist O.V. & Louekari K. (1975) Muscle and hepatopan- relationships of two commercially important cray¢shes creas weight in Astacus astacus L. in the trapping season of the genus Procambarus. Freshwater Cray¢sh 3, in Finland. Annales Zoologici Fennici12,237^243. 463^470. Lowery R.S. (1988) Growth, moulting and reproduction. In: Skurdal J. & TaugbolT. (2002) Cray¢sh of commercial impor- Freshwater Cray¢sh: Biology, Management and Exploitation tance-Astacus. In: Biology of Freshwater Cray¢sh (ed. by (ed. by D.M. Holdich & R.S. Lowery), pp. 83^114. Croom D.M. Holdich), pp. 467^510. Blackwell Science Company, Helm,Timber Press, Oregon. Oxford, UK. Mason J.C. (1975) Cray¢sh production in a small woodland Starobogatov I.Ya. (1995) Taxonomy and geographical distri- stream. Freshwater Cray¢sh 2,449^479. bution of cray¢shes of Asia and East Europe (Crustacea Obradovic J., Sekulic B. & Rac M. (1988) Muscle and Decapoda Astacoidei). Russian Journal of Arthropoda hepatopancreas participation in the body weight of the Research, Arthropoda Selecta 4, 3^25, Moscow. cray¢sh Austropotamobius torrentium. Aquaculture 72, Streissl F. & H˛dl W. (2002) Growth, morphometrics, size at 329^ 339. maturity, sexual dimorphism and condition index of Oray I. (1990) The cray¢sh stuation in Turkey. In: Aquacul- A. torrentium Schrank. Hydrobidogia 477, 201^208. ture Society Special Publication No: 12, Aquaculture Eur- Taylor C.A. (2002) Taxonomy and conservation of native ope’89_ Business Joins Science (ed. by N. De Pauw & R. cray¢sh stocks. In: Biyology of Freshwater Cray¢sh (ed. by Billard), pp. 250^251. Bredene, Belgium. D.M. Holdich), pp. 236^257. Blackwell Science Pvt. Ltd., Pursiainen M., Saarela M. & Westman K. (1988) Moulting Australia. and growth of noble cray¢sh Astacus astacus in an Trontelj P.,Yoichi M. & Boris S. (2005) Phylogenetic and phylo- oligotrophic lake. Freshwater Cray¢sh 7,155^164. geographic relationships in the cray¢sh genus Austropota- Rahe R. & Soylu E. (1989) Identi¢cation of the pathogenic mobius inferred from mitochondrial COI gene sequences. fungus causing destruction toTurkish cray¢sh stocks (As- Molecular Phylogenetics and Evolution 34, 212^226. tacus leptodactylus). Journal of Invertebrate Pathology 54, Troschel H.J., Schulz V. & Berg R. (1995) Seasonal activity 10 ^ 15. of store cray¢sh A. torrentium. Freshwater Cray¢sh 10, Rhodes C.P. & Holdich D.M. (1979) On size and sexual di- 196 ^ 199. morphism in Austropotamobius pallipes (Lereboullet) ^ A step in assessing the commercial exploitation potential of the native British freshwater cray¢sh. Aquaculture 17, Keywords: meat yield, Austropotamobius torren- 345^358. tium, cray¢sh, distribution, morphology,Turkey

542 r 2006 The Authors. Journal Compilation r 2006 Blackwell Publishing Ltd, Aquaculture Research, 37, 538^542