Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan
Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan
Park, Joo Myun; Hashimoto, Hiroaki; Jeong, Jae Mook; Kim, Hyeon Ji; Baeck, Gun Wook
2013-08-01 00:00:00
Animal Cells and Systems, 2013 Vol. 17, No. 4, 290297, http://dx.doi.org/10.1080/19768354.2013.826281 Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan a b c c c Joo Myun Park , Hiroaki Hashimoto , Jae Mook Jeong , Hyeon Ji, Kim and Gun Wook Baeck * a b Korea Inter-University Institutes of Ocean Science, Pukyong National University, Busan 608-737, Korea; Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8528, Japan; Department of Marine Biology & Aquaculture, Institute of Marine Industry, College of Marine Science, Gyeongsang National University, 445 Inpyeong-dong, Tongyeong 650-160, Korea (Received 27 April 2013; received in revised form 22 June 2013; accepted 14 July 2013) This study provides data on the age and growth of the robust tonguefish, Cynoglossus robustus in the western part of the Hiuchi-Nada Sea in the Seto Inland Sea, Japan. Fish samples consisting of 299 robust tonguefish were collected monthly from June 2000 to May 2001. Maximum total length (TL) was larger for females than males. Growth was modeled using age estimates obtained from sagittal otoliths. The lengthweight relationship followed an allometric growth pattern (b " 3.0). Estimated ages ranged from 0.5 to 5.5 years for females and from 0.5 to 3.5 years for males. Von Bertalanffy growth equation parameters were derived from back-calculated TL fitted to TL at age; estimated values for females, were L 46.0 cm, k0.278 year ,and t 1.033 years, and values for males, were L 43.4 cm, k0.281 year ,and t 1.171. The growth performance index values for females and males were F2.77 and F2.72, respectively. Keywords: robust tonguefish; Cynoglossus robustus; age and growth; Seto Inland Sea; von Bertalanffy growth equation Introduction that were caught along the South Pacific Ocean and the Southern Sea of Korea. The robust tonguefish, Cynoglossus robustus is a Age and growth studies provide important informa- member of the family Cynoglossidae; it is usually tion that is needed for assessing and managing fish found on sandy and/or muddy bottoms at a depth of stocks (Cailliet et al. 2001; Campana 2001). In the 2085 meters in the coastal waters of China, Korea, present study, otoliths were removed from the robust and Japan (Yamada et al. 1986). Tonguefishes include tonguefish specimens caught in the Seto Inland Sea, approximately 100 species in 4 genera and are dis- Japan, to clarify the age and growth of this species. tributed throughout the world; 15 species in 4 genera It was previously reported that robust tonguefish are occur in Japanese waters (Masuda et al. 1984). mainly distributed in the East China Sea, including the Tonguefishes represent relatively abundant fishery waters of southern Korea (Yamada et al. 1986). resources and are important commercial fishes in the However, areas in the Seto Inland Sea also appear to Seto Inland Sea (Yamada et al. 1986; Inaba 1988). be used mainly by this species. In spite of its main However, the tonguefish community in the Seto Inland distribution area, little is known about the ecology and Sea has experienced overexploitation and intensive biology of the robust tonguefish in the Seto Inland Sea. fishing for several decades, which have caused dramatic Therefore, we collected the new and essential informa- shifts in community composition (Inaba 1988). Although tion on the age and growth of the robust tonguefish in a number of taxonomical and biological studies on this sea. Then we compared our age and growth tonguefishes have been published, little information is estimates with values obtained in other studies. We available about the ecology of the robust tonguefish discuss the factors responsible for the differences in age (Ochiai 1966; Kim & Choi 1994;Aceves et al. 1999; and growth. Terwilliger & Munroe 1999; Baeck et al. 2011). Several studies have examined the age and growth in Cynoglossus species, including C. semilaevis (Meng & Ren 1988), Materials and methods C. macrolepidotus (Kutty 1967), C. arel (Lin 1982; Robust tonguefish specimens were collected monthly Rajaguru 1992), C. lida (Rajaguru 1992), C. semifasciatus between June 2000 and May 2001 using a bottom trawl. (Seshappa & Bhimachar 1954), C. abbreviates (Zhu & The fishing grounds were located in the western part Ma 1992;Baeck &Huh 2004a), and C. joyneri (Baeck & of the Hiuchi Nada Sea in the Seto Inland Sea, Huh 2004b). However, the studies of age and growth in Japan (Figure 1). Robust tonguefish were packed in robust tonguefish have only been conducted by Ochiai ice immediately after collection. Fish were taken to (1966) and Seo et al. (2007) using scales from specimens the laboratory where the total length (TL) and wet *Corresponding author. Email: gwbaeck@gnu.ac.kr # 2013 Korean Society for Integrative Biology ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems 291 Figure 1. Location of the sampling area (black circle) in the Seto Inland Sea, Japan. weight (BW) were measured to the nearest centimeter Alternating opaque and translucent bands were visible (0.1 cm) and gram (g), respectively. Then each specimen on the entire otolith with a 1040 microscope, and was dissected, its sex was determined from direct the alternating opaque bands were counted as the examination of gonads, and the gonad weight (GW) annuli. The number of annual rings in each otolith was was determined to the nearest 0.01 g. Sagittal otoliths independently confirmed by both the authors. The were removed from the vestibular apparatus and dry- otoliths were measured along the antero-lateral axis, as preserved for later analysis. shown in Figure 2. The otolith radius (R) was measured The gonadosomatic index (GSI) was used to as the distance between the focus and the edge of the ascertain the spawning season of the robust tonguefish. anterior of the otolith, and annulus radii (r )werethe GSI was calculated using the following equation: distance between the focus and the antero-lateral annulus. To examine the month of annulus formation, monthly changes in the occurrence frequency of an GSI ¼ðGW=BWÞ 10 annulus at the outer otolith margin were analyzed. The Within an individual, the right and left otoliths were marginal index (MI) of the otolith was calculated by: different from each other in size and structure. The right otolith was used for age and growth determination MI ¼ðR r Þ=ðr r Þ n n n1 because the increments were more easily distinguished. where R is the otolith radius (mm), r is the annulus Before observation, the otoliths were immersed in a radius of nth annulus, and n is the number of annuli. solution of glycerine, ethanol, and water for one day and The total lengthweight relationship was deter- they were read at the following day. Then, the whole mined by least-squares linear regression with logarith- otoliths were embedded in an epoxy resin, and mounted mically transformed data: on a glass slides by crystal bond adhesive. After that, surface of otoliths was sanded with 400-, 800-, and 1000- BW ¼ a TL grit sandpaper, and polished with alumina powder. 292 J.M. Park et al. Female Male 0 10 20 30 40 50 Fish size (cm, TL) Figure 3. Length-frequency distribution by sex of robust tonguefish in the Seto Inland Sea, Japan. 305.41 g for males. Age estimates ranged between 0.5 and 5.5 years for females and between 0.5 and 3.5 years for males (Table 1). The 1.5 years age group included Figure 2. Photograph showing the measuring axis and marks the highest numbers of both females (33.79%) and of robust tonguefish sagittal otolith. males (37.98%). Focus, core; R, otolith radius; r , distance between the focus Monthly changes in the marginal increment (MI) and the antero-lateral annulus. are shown in Figure 4. MI changes reached minimum values in February and then gradually increased from where a is the intercept of the regression line, which March to next January when they reached their represents a coefficient that is related to the body shape maximum and an annual ring was formed. Figure 5 of the species, and b is the regression coefficient, which shows monthly fluctuations in GSI values that were indicates isometric (b3.0) or allometric growth (b " calculated using mature robust tonguefish that were 3.0) (Wootton 1990; Anderson & Neumann 1996). longer than 20 cm in TL. The peak of the GSI for Total length-at-age was modeled using the three- robust tonguefish occurred in July. Therefore, the first parameter specialized von Bertalanffy growth equation annual ring forms approximately 6 months after birth. (Bertalanffy 1938): Lengthweight relationships were estimated using the least-squares approach with a log-linear model, and TL ¼ TL ½1 expfk ðt t Þg t 1 0 the resulting curves can be expressed by the following 2.89 2 where TL is total length (cm) at time t (years), TL is equations: females, BW0.0078 TL (r 0.99, n the asymptotic total length, k is the growth coefficient 2.90 2 145) and males, BW0.0077 TL (r 0.99, n129) and t is theoretical age at zero length. (Figure 6). The weight of robust tonguefish increased The growth performance index (F2log TL allometrically with size, regardless of sex (b " 3.0). log k) (Munro & Pauly 1983), was used to compare the The linear regression equations between body growth of this species and other Cynoglossus species. size (TL) and otolith radius R were as follows: female Table 1. Age and sex composition of robust tonguefish Results sampled off the Seto Inland Sea, Japan. In total, 299 robust tonguefish specimens were col- Females Males lected and used in this research. We were able to satisfactorily read the otoliths from 274 (91.6%) out of Age (year) n (%) n (%) the 299 specimens. The length frequency distributions 0.5 39 (26.90) 37 (28.68) of 145 females and 129 males were pooled and are 1.5 49 (33.79) 49 (37.98) summarized in Figure 3. The sex ratio did not differ 2.5 27 (18.62) 32 (24.81) significantly from 1:1 (x 10.455, df11, p0.05). 3.5 20 (13.79) 11 (8.53) Females attained larger sizes than males, with females 4.5 6 (4.14) 0 (0.00) ranging from 7.6 to 43.5 cm and males ranging from 5.5 4 (2.76) 0 (0.00) 8.2 to 37.4 cm. Individual fish weights varied between Total 145 (100.00) 129 (100.00) 2.32 and 580.96 g for females and between 3.21 and Frequency (%) Animal Cells and Systems 293 1.0 Female, n = 106 0.5 0.0 1.0 Male, n = 92 9 8 2 7 0.5 0.0 JF M A M J J A S O N D -- Month Figure 4. Monthly changes in marginal index (MI) of the robust tonguefish in the Seto Inland Sea, Japan. Female, n = 145 2 6 10 16 0.5 Male, n = 129 0.4 7 14 0.3 13 34 0.2 0.1 0.0 JF M A M J J A S O N D -- Month Figure 5. Monthly changes in gonadosomatic index (GSI) of the robust tonguefish in the Seto Inland Sea, Japan. MI [( R-r )/(r -r ) GSI n n n–1 294 J.M. Park et al. 700 400 2.90 2.89 Female, BW = 0.0078TL Male, BW = 0.0077TL 2 2 r = 0.99, n = 129 r = 0.99, n = 145 010 20 30 40 50 010 20 30 40 50 Total length (cm) Total length (cm) Figure 6. Relationship between total length and body weight of the robust tonguefish in the Seto Inland Sea, Japan. Female, TL = 19.41R – 12.59 Male, TL = 18.29R – 9.71 50 2 r = 0.90, n = 145 r = 0.86, n = 129 30 30 10 10 0 0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Radius of otolith (mm) Radius of otolith (mm) Figure 7. The relationships between the total length and the otolith radius in both sexes of the robust tonguefish in the Seto Inland Sea, Japan. TL19.41 R12.59 (r 0.90, n145), male TL difference in regression slope between the sexes (AN- 18.29 R9.71 (r 0.86, n129) (Figure 7). This COVA; F1.521, p0.001). The theoretical asymptotic TL (female 46.0 cm and analysis found no significant difference in the slope male 43.4 cm) produced results that were larger than of the regression of TL on R between the sexes the largest specimens which were caught in this study (ANCOVA; F9.845, p0.001). (female 43.5 cm and male 37.4 cm). The growth The parameters of the estimated von Bertalanffy performance index values for females and males were growth equations that were derived from back- F2.77 and F2.72, respectively. calculated TL fitted to TL at age were as follows: 0.278(t1.033) female, L 46.0 (1e ), male, L 43.4 t t 0.281(t1.171) (1e ), females, TL 46.0 cm, k0.278 Discussion year , and t 1.033 years, and males, TL To analyze the age and growth, we used sagittal 43.4 cm, k0.281 year , and t 1.171 (Table 2 otoliths. Sagittal otoliths are the hard structure and Figure 8). This analysis found no significant which are most commonly used to determine the age of fish (Baker & Timmons 1991). Sagittal otoliths Table 2. von Bertalanffy growth parameters and derived have been used to determine the age of the genus growth performance index (F) for females and males of Cynoglossus,suchas C. semilaevis (Meng & Ren 1988), robust tonguefish from the Seto Inland Sea, Japan. C. abbreviates (Baeck & Huh 2004a), C. joyneri (Baeck & Sex L (cm) k (year ) t (year) F Huh 2004b), and so on. Also, Meng and Ren (1988) explained that the sagittal otolith is suitable for Females 46.0 0.278 1.033 2.77 determining age and estimating the growth rate. The Males 43.4 0.281 1.171 2.72 annulation patterns of sagittal otoliths of robust Length (cmTL) Body weight(g) Animal Cells and Systems 295 (1966) and Seo et al. (2007). Maximum age can differ among the geographic areas, as was found in Bilgin Female and C¸ elik (2009). Life spans of fishes in the genus 40 Male Cynoglossus are reported to be between 3 and 14 years: 3 years old for C. arel (Lin 1982; Rajaguru 1992) 30 and C. lida (Rajaguru 1992), 4 years old for C. joyneri (Baeck & Huh 2004b), 5 years old for C. abbreviates (Baeck & Huh 2004a), 7 years old for C. macrolepidotus (Kutty 1967), 10 years old for C. dubius (Seshappa 1976), and 14 years old for C. semilaevis (Meng & Ren 1988). The robust tonguefish seems to be a relatively slow-growing and medium-lived species. From our age- reading results, the size and longevity of females appear to be greater than in males. A tendency for sexual 0 0.5 1.5 2.5 3.5 4.5 5.5 6.5 7.5 dimorphism, in which females are larger than males at a Age (years) given size and age, is clear in the robust tonguefish, as is the caseinmostmembers of Cynoglossus,e.g. C. arel Figure 8. von Bertalanffy growth curve of female and male of and C. lida from Indian waters (Rajaguru 1992), the robust tonguefish in the Seto Inland Sea, Japan. C. semilaevis from the east coast of China (Meng & Ren 1988), and C. abbreviates from Jiaozhou Bay and tonguefish nearly resembled those observed in other the Southern Sea of Korea (Zhu & Ma 1992;Baeck & genus Cynoglossus and in general in teleosts, with Huh 2004a). translucent zones alternated by opaque zones laid When comparing the L parameters obtained down around an opaque nucleus, whose thickness in this study, with values obtained by other studies increasingly decreased toward the otolith outside (Table 3), we become aware of the small differences in (Baeck & Huh 2004a, 2004b; La Mesa et al. 2005; L . In the South Pacific Ocean and the southern sea of Figure 2). Each translucent and opaque zone appeared Korea, the L of robust tonguefish is around 39.0 cm to be of the regular width, such as C. abbreviates and (sexes combined), and 44.3 cm for females and 37.3 cm C. joyneri (Baeck & Huh 2004a, 2004b). for males. However, in the present study, L was The present study provides new information about 46.0 cm for females and 43.4 cm for males. These the age and growth of robust tonguefish in the Seto differences may be due to the differences in environ- Inland Sea. The maximum TL of robust tonguefish was mental factors, productivity, the age analysis method, 43.5 cm for females and 37.4 cm for males, which latitude, or fishing pressure (Park et al. 2008; Sequeira corresponded to otolith derived ages of 5.5 years for et al. 2009). Reproductive effort, considering the females and 3.5 for males, even if only a few samples bioenergetic constraints of an organisms energy bud- were specimens of more than 5.5 years. The maximum get, implies that females have reduced growth rates fish size was larger than that reported for the Southern (Gunderson 1997). However, the results of this study Sea of Korea by Seo et al. (2007). Consoli et al. (2010) showed that there was no significant difference in concluded that differences in fish size among collec- growth rate between the sexes in robust tonguefish, tions could be due to the differences in fishing pressure such as have been found by other researchers (Seo et al. among areas, maximum sampling depth, and the 2007). Sex differences in growth rates have been fishing gear used. Our findings with these conclusions: attributed to viviparity with internal fertilization this suggests that the difference in fish size was due to (Sequeira et al. 2003). Also, sexual dimorphism in differences in fishing pressure and the sampling method growth rate appears to depend on the species itself and used. its habitat. The index of growth performance (F)is The lengthweight relationship for robust tongue- considered as a useful tool for comparing the growth fish followed an allometric growth pattern (b " 3.0), as curves between populations of the same species and/or Seo et al. (2007) reported for the Southern Sea of different species that belong to the same family (Sparre Korea. In this study, the slope (b) did not differ et al. 1987). In the genus Cynoglossus, growth perfor- significantly between females (b2.89) and males mance ranged from 2.20 for females and 2.11 for males (b2.90), suggesting that fish condition did not differ in C. Joyneri, to 2.43 for females and 2.40 for males between the sexes. in C. lida, 2.49 for females and 2.40 for males in Maximum fish age in our sample was 5.5 years, C. abbreviatus, 2.58 for females and 2.57 for males in with six rings observed in the otolith, which was larger C. robustus (Korean waters), 2.76 for the sexes com- than the maximum ages that were recorded by Ochiai bined in C. robustus (South Pacific Ocean), 2.77 for Total length (cm) 296 J.M. Park et al. Table 3. von Bertalanffy growth parameters and derived growth performance (F) for genus Cynolossus in different geographical areas. L (cm) k (year ) t (year) F Species Females Males Females Males Females Males Females Males Sampling area Data source C. arel 61.5 57.0 0.315 0.238 0.265 0.776 3.08 2.89 Indian waters Rajaguru (1992) C. lida 34.0 33.5 0.233 0.223 1.803 1.635 2.43 2.40 Indian waters Rajaguru (1992) C. abbreviatus 44.5 41.5 0.155 0.145 2.691 3.342 2.49 2.40 Korean waters Baeck and Huh (2004a) C. joyneri 29.1 27.4 0.186 0.170 2.399 2.840 2.20 2.11 Korean waters Baeck and Huh (2004b) C. robustus 39.0 (sexes 0.381 (sexes 2.76 (sexes South Pacific Ochiai (1966) combined) combined) combined) Ocean 44.3 37.3 0.192 0.266 2.077 1.890 2.58 2.57 Korean waters Seo et al (2007) 46.0 43.4 0.278 0.281 1.033 1.171 2.77 2.72 This study Bilgin S, C¸ elik ES¸. 2009. Age, growth and reproduction of the female and 2.72 for male in C. robustus (present study) black scorpionfish, Scorpaena porcus (Pisces, Scorpaeni- and 3.08 for female and 2.89 for male in C. arel, dae), on the Black Sea coast of Turkey. J Appl Ichthyol. indicating that there is a direct relationship between 25:5560. fish size and growth performance (Table 3). When Cailliet GM, Andrews AH, Burtion EJ, Watters DL, Kline DE, Ferry-Graham LA. 2001. Age determination and comparing our results to those from other areas for validation studies of marine fishes: do deep-dwellers live Cynoglossus fishes, the index of growth performance linger? Exp Gerontol. 36:739764. for robust tonguefish (present study) was higher than Campana SE. 2001. Accuracy, precision and quality control values for other Cynoglossus fishes, except C. arel.In in age determination, including a review of the use and abuse of age validation methods. J Fish Biol. 59:197242. addition, the index was higher in females than in males, Consoli P, Battaglia P, Castriota L, Esposito V, Romeo T, as has been observed in other Cynoglossus fishes. Andaloro F. 2010. Age, growth and feeding habits of the Relationship between these growth performances was bluemouth rockfish, Helicolenus dactylopterus dactylopterus observed that larger species attain higher growth (Delaroche 1809) in the central Mediterranean (southern Tyrrhenian Sea). J Appl Ichthyol. 26:583591. performance and older age (La Mesa et al. 2005). Gunderson DR. 1997. Trade-off between reproductive effort However, these differences may be due to the differ- and adult survival in oviparous and viviparous fishes. ences in environmental factors, such as temperature, Can J Fish Aquat Sci. 54:990998. salinity, etc. of study water and variability in the life Inaba A. 1988. Fauna and flora of the Seto Inland Sea. 2nd ed. Mukaishima Marine Biological Station. span between study areas (Taylor 1958). Hiroshima: Hiroshima University Press; 475 p. Kim IS, Choi Y. 1994. A taxonomic revision of the family Cynoglossidae (Pisces, Pleuronectiformes) from Korea. 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J du Conseil and growth of the robust tonguefish, Cynoglossus International pour I’Exploration de la Mer. 23:366370. robustus in the Southern Sea of Korea. Korean J Ichthyol. Terwilliger MR, Munroe TA. 1999. Age, growth, longevity, 19:324331. (in Korean) and mortality of blackcheek tonguefish, Symphurus Sequeira V, Figueiredo I, Mun˜oz M, Gordo LS. 2003. New plagiusa (Cynoglossidae: Pleuronectiformes), in Chesapeake approach to the reproductive biology of Helicolenus Bay, Virginia. Fish Bull. 97:340361. dactylopterus. J Fish Biol. 62:12061210. Wootton RJ. 1990. Ecology of teleost fishes. London: Sequeira V, Neves A, Vieira AR, Figueiredo I, Gordo LS. Chapman and Hall Press; 404 p. 2009. Age and growth of bluemouth, Helicolenus Yamada U, Tagawa M, Kishida S, Honjo K. 1986. Fishes of dactylopterus, from the Portuguese continental slope. the East China Sea and the Yellow Sea. Nagasaki: Seikai ICES J Mar Sci. 66:524531. Reg Fish Res Lab; 501 p. Seshappa G, Bhimachar BS. 1954. 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Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan
Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan
Abstract
This study provides data on the age and growth of the robust tonguefish, Cynoglossus robustus in the western part of the Hiuchi-Nada Sea in the Seto Inland Sea, Japan. Fish samples consisting of 299 robust tonguefish were collected monthly from June 2000 to May 2001. Maximum total length (TL) was larger for females than males. Growth was modeled using age estimates obtained from sagittal otoliths. The length–weight relationship followed an allometric growth pattern (b ≠ 3.0)....
Animal Cells and Systems, 2013 Vol. 17, No. 4, 290297, http://dx.doi.org/10.1080/19768354.2013.826281 Age and growth of the robust tonguefish Cynoglossus robustus in the Seto Inland Sea, Japan a b c c c Joo Myun Park , Hiroaki Hashimoto , Jae Mook Jeong , Hyeon Ji, Kim and Gun Wook Baeck * a b Korea Inter-University Institutes of Ocean Science, Pukyong National University, Busan 608-737, Korea; Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8528, Japan; Department of Marine Biology & Aquaculture, Institute of Marine Industry, College of Marine Science, Gyeongsang National University, 445 Inpyeong-dong, Tongyeong 650-160, Korea (Received 27 April 2013; received in revised form 22 June 2013; accepted 14 July 2013) This study provides data on the age and growth of the robust tonguefish, Cynoglossus robustus in the western part of the Hiuchi-Nada Sea in the Seto Inland Sea, Japan. Fish samples consisting of 299 robust tonguefish were collected monthly from June 2000 to May 2001. Maximum total length (TL) was larger for females than males. Growth was modeled using age estimates obtained from sagittal otoliths. The lengthweight relationship followed an allometric growth pattern (b " 3.0). Estimated ages ranged from 0.5 to 5.5 years for females and from 0.5 to 3.5 years for males. Von Bertalanffy growth equation parameters were derived from back-calculated TL fitted to TL at age; estimated values for females, were L 46.0 cm, k0.278 year ,and t 1.033 years, and values for males, were L 43.4 cm, k0.281 year ,and t 1.171. The growth performance index values for females and males were F2.77 and F2.72, respectively. Keywords: robust tonguefish; Cynoglossus robustus; age and growth; Seto Inland Sea; von Bertalanffy growth equation Introduction that were caught along the South Pacific Ocean and the Southern Sea of Korea. The robust tonguefish, Cynoglossus robustus is a Age and growth studies provide important informa- member of the family Cynoglossidae; it is usually tion that is needed for assessing and managing fish found on sandy and/or muddy bottoms at a depth of stocks (Cailliet et al. 2001; Campana 2001). In the 2085 meters in the coastal waters of China, Korea, present study, otoliths were removed from the robust and Japan (Yamada et al. 1986). Tonguefishes include tonguefish specimens caught in the Seto Inland Sea, approximately 100 species in 4 genera and are dis- Japan, to clarify the age and growth of this species. tributed throughout the world; 15 species in 4 genera It was previously reported that robust tonguefish are occur in Japanese waters (Masuda et al. 1984). mainly distributed in the East China Sea, including the Tonguefishes represent relatively abundant fishery waters of southern Korea (Yamada et al. 1986). resources and are important commercial fishes in the However, areas in the Seto Inland Sea also appear to Seto Inland Sea (Yamada et al. 1986; Inaba 1988). be used mainly by this species. In spite of its main However, the tonguefish community in the Seto Inland distribution area, little is known about the ecology and Sea has experienced overexploitation and intensive biology of the robust tonguefish in the Seto Inland Sea. fishing for several decades, which have caused dramatic Therefore, we collected the new and essential informa- shifts in community composition (Inaba 1988). Although tion on the age and growth of the robust tonguefish in a number of taxonomical and biological studies on this sea. Then we compared our age and growth tonguefishes have been published, little information is estimates with values obtained in other studies. We available about the ecology of the robust tonguefish discuss the factors responsible for the differences in age (Ochiai 1966; Kim & Choi 1994;Aceves et al. 1999; and growth. Terwilliger & Munroe 1999; Baeck et al. 2011). Several studies have examined the age and growth in Cynoglossus species, including C. semilaevis (Meng & Ren 1988), Materials and methods C. macrolepidotus (Kutty 1967), C. arel (Lin 1982; Robust tonguefish specimens were collected monthly Rajaguru 1992), C. lida (Rajaguru 1992), C. semifasciatus between June 2000 and May 2001 using a bottom trawl. (Seshappa & Bhimachar 1954), C. abbreviates (Zhu & The fishing grounds were located in the western part Ma 1992;Baeck &Huh 2004a), and C. joyneri (Baeck & of the Hiuchi Nada Sea in the Seto Inland Sea, Huh 2004b). However, the studies of age and growth in Japan (Figure 1). Robust tonguefish were packed in robust tonguefish have only been conducted by Ochiai ice immediately after collection. Fish were taken to (1966) and Seo et al. (2007) using scales from specimens the laboratory where the total length (TL) and wet *Corresponding author. Email: gwbaeck@gnu.ac.kr # 2013 Korean Society for Integrative Biology ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems 291 Figure 1. Location of the sampling area (black circle) in the Seto Inland Sea, Japan. weight (BW) were measured to the nearest centimeter Alternating opaque and translucent bands were visible (0.1 cm) and gram (g), respectively. Then each specimen on the entire otolith with a 1040 microscope, and was dissected, its sex was determined from direct the alternating opaque bands were counted as the examination of gonads, and the gonad weight (GW) annuli. The number of annual rings in each otolith was was determined to the nearest 0.01 g. Sagittal otoliths independently confirmed by both the authors. The were removed from the vestibular apparatus and dry- otoliths were measured along the antero-lateral axis, as preserved for later analysis. shown in Figure 2. The otolith radius (R) was measured The gonadosomatic index (GSI) was used to as the distance between the focus and the edge of the ascertain the spawning season of the robust tonguefish. anterior of the otolith, and annulus radii (r )werethe GSI was calculated using the following equation: distance between the focus and the antero-lateral annulus. To examine the month of annulus formation, monthly changes in the occurrence frequency of an GSI ¼ðGW=BWÞ 10 annulus at the outer otolith margin were analyzed. The Within an individual, the right and left otoliths were marginal index (MI) of the otolith was calculated by: different from each other in size and structure. The right otolith was used for age and growth determination MI ¼ðR r Þ=ðr r Þ n n n1 because the increments were more easily distinguished. where R is the otolith radius (mm), r is the annulus Before observation, the otoliths were immersed in a radius of nth annulus, and n is the number of annuli. solution of glycerine, ethanol, and water for one day and The total lengthweight relationship was deter- they were read at the following day. Then, the whole mined by least-squares linear regression with logarith- otoliths were embedded in an epoxy resin, and mounted mically transformed data: on a glass slides by crystal bond adhesive. After that, surface of otoliths was sanded with 400-, 800-, and 1000- BW ¼ a TL grit sandpaper, and polished with alumina powder. 292 J.M. Park et al. Female Male 0 10 20 30 40 50 Fish size (cm, TL) Figure 3. Length-frequency distribution by sex of robust tonguefish in the Seto Inland Sea, Japan. 305.41 g for males. Age estimates ranged between 0.5 and 5.5 years for females and between 0.5 and 3.5 years for males (Table 1). The 1.5 years age group included Figure 2. Photograph showing the measuring axis and marks the highest numbers of both females (33.79%) and of robust tonguefish sagittal otolith. males (37.98%). Focus, core; R, otolith radius; r , distance between the focus Monthly changes in the marginal increment (MI) and the antero-lateral annulus. are shown in Figure 4. MI changes reached minimum values in February and then gradually increased from where a is the intercept of the regression line, which March to next January when they reached their represents a coefficient that is related to the body shape maximum and an annual ring was formed. Figure 5 of the species, and b is the regression coefficient, which shows monthly fluctuations in GSI values that were indicates isometric (b3.0) or allometric growth (b " calculated using mature robust tonguefish that were 3.0) (Wootton 1990; Anderson & Neumann 1996). longer than 20 cm in TL. The peak of the GSI for Total length-at-age was modeled using the three- robust tonguefish occurred in July. Therefore, the first parameter specialized von Bertalanffy growth equation annual ring forms approximately 6 months after birth. (Bertalanffy 1938): Lengthweight relationships were estimated using the least-squares approach with a log-linear model, and TL ¼ TL ½1 expfk ðt t Þg t 1 0 the resulting curves can be expressed by the following 2.89 2 where TL is total length (cm) at time t (years), TL is equations: females, BW0.0078 TL (r 0.99, n the asymptotic total length, k is the growth coefficient 2.90 2 145) and males, BW0.0077 TL (r 0.99, n129) and t is theoretical age at zero length. (Figure 6). The weight of robust tonguefish increased The growth performance index (F2log TL allometrically with size, regardless of sex (b " 3.0). log k) (Munro & Pauly 1983), was used to compare the The linear regression equations between body growth of this species and other Cynoglossus species. size (TL) and otolith radius R were as follows: female Table 1. Age and sex composition of robust tonguefish Results sampled off the Seto Inland Sea, Japan. In total, 299 robust tonguefish specimens were col- Females Males lected and used in this research. We were able to satisfactorily read the otoliths from 274 (91.6%) out of Age (year) n (%) n (%) the 299 specimens. The length frequency distributions 0.5 39 (26.90) 37 (28.68) of 145 females and 129 males were pooled and are 1.5 49 (33.79) 49 (37.98) summarized in Figure 3. The sex ratio did not differ 2.5 27 (18.62) 32 (24.81) significantly from 1:1 (x 10.455, df11, p0.05). 3.5 20 (13.79) 11 (8.53) Females attained larger sizes than males, with females 4.5 6 (4.14) 0 (0.00) ranging from 7.6 to 43.5 cm and males ranging from 5.5 4 (2.76) 0 (0.00) 8.2 to 37.4 cm. Individual fish weights varied between Total 145 (100.00) 129 (100.00) 2.32 and 580.96 g for females and between 3.21 and Frequency (%) Animal Cells and Systems 293 1.0 Female, n = 106 0.5 0.0 1.0 Male, n = 92 9 8 2 7 0.5 0.0 JF M A M J J A S O N D -- Month Figure 4. Monthly changes in marginal index (MI) of the robust tonguefish in the Seto Inland Sea, Japan. Female, n = 145 2 6 10 16 0.5 Male, n = 129 0.4 7 14 0.3 13 34 0.2 0.1 0.0 JF M A M J J A S O N D -- Month Figure 5. Monthly changes in gonadosomatic index (GSI) of the robust tonguefish in the Seto Inland Sea, Japan. MI [( R-r )/(r -r ) GSI n n n–1 294 J.M. Park et al. 700 400 2.90 2.89 Female, BW = 0.0078TL Male, BW = 0.0077TL 2 2 r = 0.99, n = 129 r = 0.99, n = 145 010 20 30 40 50 010 20 30 40 50 Total length (cm) Total length (cm) Figure 6. Relationship between total length and body weight of the robust tonguefish in the Seto Inland Sea, Japan. Female, TL = 19.41R – 12.59 Male, TL = 18.29R – 9.71 50 2 r = 0.90, n = 145 r = 0.86, n = 129 30 30 10 10 0 0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Radius of otolith (mm) Radius of otolith (mm) Figure 7. The relationships between the total length and the otolith radius in both sexes of the robust tonguefish in the Seto Inland Sea, Japan. TL19.41 R12.59 (r 0.90, n145), male TL difference in regression slope between the sexes (AN- 18.29 R9.71 (r 0.86, n129) (Figure 7). This COVA; F1.521, p0.001). The theoretical asymptotic TL (female 46.0 cm and analysis found no significant difference in the slope male 43.4 cm) produced results that were larger than of the regression of TL on R between the sexes the largest specimens which were caught in this study (ANCOVA; F9.845, p0.001). (female 43.5 cm and male 37.4 cm). The growth The parameters of the estimated von Bertalanffy performance index values for females and males were growth equations that were derived from back- F2.77 and F2.72, respectively. calculated TL fitted to TL at age were as follows: 0.278(t1.033) female, L 46.0 (1e ), male, L 43.4 t t 0.281(t1.171) (1e ), females, TL 46.0 cm, k0.278 Discussion year , and t 1.033 years, and males, TL To analyze the age and growth, we used sagittal 43.4 cm, k0.281 year , and t 1.171 (Table 2 otoliths. Sagittal otoliths are the hard structure and Figure 8). This analysis found no significant which are most commonly used to determine the age of fish (Baker & Timmons 1991). Sagittal otoliths Table 2. von Bertalanffy growth parameters and derived have been used to determine the age of the genus growth performance index (F) for females and males of Cynoglossus,suchas C. semilaevis (Meng & Ren 1988), robust tonguefish from the Seto Inland Sea, Japan. C. abbreviates (Baeck & Huh 2004a), C. joyneri (Baeck & Sex L (cm) k (year ) t (year) F Huh 2004b), and so on. Also, Meng and Ren (1988) explained that the sagittal otolith is suitable for Females 46.0 0.278 1.033 2.77 determining age and estimating the growth rate. The Males 43.4 0.281 1.171 2.72 annulation patterns of sagittal otoliths of robust Length (cmTL) Body weight(g) Animal Cells and Systems 295 (1966) and Seo et al. (2007). Maximum age can differ among the geographic areas, as was found in Bilgin Female and C¸ elik (2009). Life spans of fishes in the genus 40 Male Cynoglossus are reported to be between 3 and 14 years: 3 years old for C. arel (Lin 1982; Rajaguru 1992) 30 and C. lida (Rajaguru 1992), 4 years old for C. joyneri (Baeck & Huh 2004b), 5 years old for C. abbreviates (Baeck & Huh 2004a), 7 years old for C. macrolepidotus (Kutty 1967), 10 years old for C. dubius (Seshappa 1976), and 14 years old for C. semilaevis (Meng & Ren 1988). The robust tonguefish seems to be a relatively slow-growing and medium-lived species. From our age- reading results, the size and longevity of females appear to be greater than in males. A tendency for sexual 0 0.5 1.5 2.5 3.5 4.5 5.5 6.5 7.5 dimorphism, in which females are larger than males at a Age (years) given size and age, is clear in the robust tonguefish, as is the caseinmostmembers of Cynoglossus,e.g. C. arel Figure 8. von Bertalanffy growth curve of female and male of and C. lida from Indian waters (Rajaguru 1992), the robust tonguefish in the Seto Inland Sea, Japan. C. semilaevis from the east coast of China (Meng & Ren 1988), and C. abbreviates from Jiaozhou Bay and tonguefish nearly resembled those observed in other the Southern Sea of Korea (Zhu & Ma 1992;Baeck & genus Cynoglossus and in general in teleosts, with Huh 2004a). translucent zones alternated by opaque zones laid When comparing the L parameters obtained down around an opaque nucleus, whose thickness in this study, with values obtained by other studies increasingly decreased toward the otolith outside (Table 3), we become aware of the small differences in (Baeck & Huh 2004a, 2004b; La Mesa et al. 2005; L . In the South Pacific Ocean and the southern sea of Figure 2). Each translucent and opaque zone appeared Korea, the L of robust tonguefish is around 39.0 cm to be of the regular width, such as C. abbreviates and (sexes combined), and 44.3 cm for females and 37.3 cm C. joyneri (Baeck & Huh 2004a, 2004b). for males. However, in the present study, L was The present study provides new information about 46.0 cm for females and 43.4 cm for males. These the age and growth of robust tonguefish in the Seto differences may be due to the differences in environ- Inland Sea. The maximum TL of robust tonguefish was mental factors, productivity, the age analysis method, 43.5 cm for females and 37.4 cm for males, which latitude, or fishing pressure (Park et al. 2008; Sequeira corresponded to otolith derived ages of 5.5 years for et al. 2009). Reproductive effort, considering the females and 3.5 for males, even if only a few samples bioenergetic constraints of an organisms energy bud- were specimens of more than 5.5 years. The maximum get, implies that females have reduced growth rates fish size was larger than that reported for the Southern (Gunderson 1997). However, the results of this study Sea of Korea by Seo et al. (2007). Consoli et al. (2010) showed that there was no significant difference in concluded that differences in fish size among collec- growth rate between the sexes in robust tonguefish, tions could be due to the differences in fishing pressure such as have been found by other researchers (Seo et al. among areas, maximum sampling depth, and the 2007). Sex differences in growth rates have been fishing gear used. Our findings with these conclusions: attributed to viviparity with internal fertilization this suggests that the difference in fish size was due to (Sequeira et al. 2003). Also, sexual dimorphism in differences in fishing pressure and the sampling method growth rate appears to depend on the species itself and used. its habitat. The index of growth performance (F)is The lengthweight relationship for robust tongue- considered as a useful tool for comparing the growth fish followed an allometric growth pattern (b " 3.0), as curves between populations of the same species and/or Seo et al. (2007) reported for the Southern Sea of different species that belong to the same family (Sparre Korea. In this study, the slope (b) did not differ et al. 1987). In the genus Cynoglossus, growth perfor- significantly between females (b2.89) and males mance ranged from 2.20 for females and 2.11 for males (b2.90), suggesting that fish condition did not differ in C. Joyneri, to 2.43 for females and 2.40 for males between the sexes. in C. lida, 2.49 for females and 2.40 for males in Maximum fish age in our sample was 5.5 years, C. abbreviatus, 2.58 for females and 2.57 for males in with six rings observed in the otolith, which was larger C. robustus (Korean waters), 2.76 for the sexes com- than the maximum ages that were recorded by Ochiai bined in C. robustus (South Pacific Ocean), 2.77 for Total length (cm) 296 J.M. Park et al. Table 3. von Bertalanffy growth parameters and derived growth performance (F) for genus Cynolossus in different geographical areas. L (cm) k (year ) t (year) F Species Females Males Females Males Females Males Females Males Sampling area Data source C. arel 61.5 57.0 0.315 0.238 0.265 0.776 3.08 2.89 Indian waters Rajaguru (1992) C. lida 34.0 33.5 0.233 0.223 1.803 1.635 2.43 2.40 Indian waters Rajaguru (1992) C. abbreviatus 44.5 41.5 0.155 0.145 2.691 3.342 2.49 2.40 Korean waters Baeck and Huh (2004a) C. joyneri 29.1 27.4 0.186 0.170 2.399 2.840 2.20 2.11 Korean waters Baeck and Huh (2004b) C. robustus 39.0 (sexes 0.381 (sexes 2.76 (sexes South Pacific Ochiai (1966) combined) combined) combined) Ocean 44.3 37.3 0.192 0.266 2.077 1.890 2.58 2.57 Korean waters Seo et al (2007) 46.0 43.4 0.278 0.281 1.033 1.171 2.77 2.72 This study Bilgin S, C¸ elik ES¸. 2009. Age, growth and reproduction of the female and 2.72 for male in C. robustus (present study) black scorpionfish, Scorpaena porcus (Pisces, Scorpaeni- and 3.08 for female and 2.89 for male in C. arel, dae), on the Black Sea coast of Turkey. J Appl Ichthyol. indicating that there is a direct relationship between 25:5560. fish size and growth performance (Table 3). When Cailliet GM, Andrews AH, Burtion EJ, Watters DL, Kline DE, Ferry-Graham LA. 2001. Age determination and comparing our results to those from other areas for validation studies of marine fishes: do deep-dwellers live Cynoglossus fishes, the index of growth performance linger? Exp Gerontol. 36:739764. for robust tonguefish (present study) was higher than Campana SE. 2001. Accuracy, precision and quality control values for other Cynoglossus fishes, except C. arel.In in age determination, including a review of the use and abuse of age validation methods. J Fish Biol. 59:197242. addition, the index was higher in females than in males, Consoli P, Battaglia P, Castriota L, Esposito V, Romeo T, as has been observed in other Cynoglossus fishes. Andaloro F. 2010. Age, growth and feeding habits of the Relationship between these growth performances was bluemouth rockfish, Helicolenus dactylopterus dactylopterus observed that larger species attain higher growth (Delaroche 1809) in the central Mediterranean (southern Tyrrhenian Sea). J Appl Ichthyol. 26:583591. performance and older age (La Mesa et al. 2005). Gunderson DR. 1997. Trade-off between reproductive effort However, these differences may be due to the differ- and adult survival in oviparous and viviparous fishes. ences in environmental factors, such as temperature, Can J Fish Aquat Sci. 54:990998. salinity, etc. of study water and variability in the life Inaba A. 1988. Fauna and flora of the Seto Inland Sea. 2nd ed. Mukaishima Marine Biological Station. span between study areas (Taylor 1958). Hiroshima: Hiroshima University Press; 475 p. Kim IS, Choi Y. 1994. A taxonomic revision of the family Cynoglossidae (Pisces, Pleuronectiformes) from Korea. 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Journal
Animal Cells and Systems
– Taylor & Francis
Published: Aug 1, 2013
Keywords: robust tonguefish; Cynoglossus robustus; age and growth; Seto Inland Sea; von Bertalanffy growth equation
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References
Larval development of Symhpurus williamisi (Cynoglossidae: Pleuronectiformes) from the Gulf of California
Age and growth of three-lined tonguefish (Cynoglossus abbreviates) (Soleidae; Teleostei)
Age and growth of red tongue sole (Cynoglossus joyneri) in the Southern Sea of Korea
Feeding ecology of three tonguefishes, genus Cynoglossus (Cynoglossidae) in the Seto Inland Sea, Japan
Precision of ages estimated from five bony structures of arctic char (Salvelinus alpines) from the Wood River system, Alaska
A quantitative theory of organic growth
Age, growth and reproduction of the black scorpionfish, Scorpaena porcus (Pisces, Scorpaenidae), on the Black Sea coast of Turkey
Age determination and validation studies of marine fishes: do deep-dwellers live linger?
Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods
Age, growth and feeding habits of the bluemouth rockfish, Helicolenus dactylopterus dactylopterus (Delaroche 1809) in the central Mediterranean (southern Tyrrhenian Sea)
Trade-off between reproductive effort and adult survival in oviparous and viviparous fishes
A taxonomic revision of the family Cynoglossidae (Pisces, Pleuronectiformes) from Korea
Observations on the growth and mortality of the large scaled tonguefish Cynoglossus macrolepidotus (Bleeker)
Age and growth of Madeira scorpionfish, Scorpaena maderensis Valenciennes, 1833, in the central Mediterranean
Age and growth of north Taiwan tongue sole Cynoglossus arel
Age and growth of Cynoglossus semilaevis Gunther in the Bohai Sea
A simple method for comparing the growth of fishes and invertebrates
Age and growth of the mudskipper, Scartelaos gigas (Perciformes, Gobiidae) from Korea
Biology of two co-occurring tonguefishes, Cynoglossus arel and C. lida (Pleuronectiformes: Cynoglossidae), from Indian waters
Age and growth of the robust tonguefish, Cynoglossus robustus in the Southern Sea of Korea
New approach to the reproductive biology of Helicolenus dactylopterus
Age and growth of bluemouth, Helicolenus dactylopterus, from the Portuguese continental slope
Studies on the age and growth of the Malabar sole, Cynoglossus semifasciatus day
On the fishery biology of the large tongue-sole, Cynoglossus dubius day, at Calicut, Kerala
Introduction to tropical fish stock assessment. Part 1
Cod growth and temperature
Age, growth, longevity, and mortality of blackcheek tonguefish, Symphurus plagiusa (Cynoglossidae: Pleuronectiformes), in Chesapeake Bay, Virginia
Studies on age, growth, and age class structures of the tonguefish, Cynoglossus abbreviatus (Day) in the Jiaozhou Bay waters
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