Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan

Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina... Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana, Ark Shell Scapharca kagoshimensis, and Manila Clam Ruditapes philippinarum in West Japan <meta name="citation_title" content="Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan"/> <meta name="dc.title" content="Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan"/> div.banner_title_bkg div.trangle { border-color: #9E6C84 transparent transparent transparent; opacity:0.77; /*new styles start*/ -ms-filter:"progid:DXImageTransform.Microsoft.Alpha(Opacity=77)" ;filter: alpha(opacity=77); /*new styles end*/ } div.banner_title_bkg_if div.trangle { border-color: transparent transparent #9E6C84 transparent ; opacity:0.77; /*new styles start*/ -ms-filter:"progid:DXImageTransform.Microsoft.Alpha(Opacity=77)" ;filter: alpha(opacity=77); /*new styles end*/ } div.banner_title_bkg div.trangle { width: 249px; } #banner { background-image: url('http://images.hindawi.com/journals/jmb/jmb.banner.jpg'); background-position: 50% 0;} Hindawi Publishing Corporation Home Journals About Us Journal of Marine Biology About this Journal Submit a Manuscript Table of Contents Journal Menu About this Journal · Abstracting and Indexing · Advance Access · Aims and Scope · Article Processing Charges · Articles in Press · Author Guidelines · Bibliographic Information · Citations to this Journal · Contact Information · Editorial Board · Editorial Workflow · Free eTOC Alerts · Publication Ethics · Reviewers Acknowledgment · Submit a Manuscript · Subscription Information · Table of Contents Open Special Issues · Published Special Issues · Special Issue Guidelines Abstract Full-Text PDF Full-Text HTML Full-Text ePUB Linked References How to Cite this Article Journal of Marine Biology Volume 2015 (2015), Article ID 593032, 5 pages http://dx.doi.org/10.1155/2015/593032 Research Article Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan Tatsuya Yurimoto Japan International Research Center for Agricultural Sciences, Ohwashi, Tsukuba 305-8686, Japan Received 8 August 2014; Revised 10 January 2015; Accepted 28 January 2015 Academic Editor: Tatsuya Sakamoto Copyright © 2015 Tatsuya Yurimoto. This is an open access article distributed under the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract The types of tissues accumulating glycogen and seasonal changes in glycogen content were investigated in the following shell species: pen shell Atrina lischkeana , ark shell Scapharca kagoshimensis , and Manila clam Ruditapes philippinarum . Comparison of the results showed that the adductor muscle or foot was the main glycogen reservoir and the levels varied seasonally. The adductor muscle in the pen shell showed higher glycogen content during spring and lower content during autumn. The ark shell, on the other hand, showed higher content during winter and spring and lower content during summer and autumn, while the Manila clam showed higher glycogen content during spring and summer and lower content during autumn and winter. These results revealed that the adductor muscle in pen shells and the foot in ark shells and Manila clams act as the main storage tissues for glycogen in the three species studied and that these tissues are suitable to analyze glycogen prevalence to estimate individual physiological condition. 1. Introduction Glycogen is a water-soluble polysaccharide, composed by polymerized glucose molecules joined through glycosidic bonds, forming a network-like structure [ 1 ]. It represents the main form of energy storage in the animal bodies along with body fat. In particular, bivalves present higher percentage of glycogen compared to fat, and its contents are influenced by internal factors, such as growth and sexual maturation, and external factors, such as food availability and other environmental factors [ 2 – 6 ]. Thus, glycogen content varies depending on the physiological state of the organism, and it can be used to evaluate physiological condition in different bivalve species, including Pacific oysters ( Crassostrea gigas ), pearl oysters ( Pinctada fucata martensii ), Manila clams ( Ruditapes philippinarum ), and ark shells ( Scapharca kagoshimensis ) [ 7 – 11 ]. Ariake Bay is a one of the most famous fishery grounds for bivalves such as pen shells ( Atrina lischkeana ), ark shells, and Manila clams in West Japan. However, landings of these species have remained at low levels for recent years, due to environmental changes that coastal development is considering to contribute the frequently occurrence of red tide and hypoxic water. Therefore population stabilization of these in the bay has become a pressing issue for local fisheries [ 12 , 13 ]. Set against this background, identifying a maker able to provide information on bivalve physiological condition in situ would facilitate reaching stable fishing production for these species. So far, glycogen content and its variation have been assessed in pen shells as an important taste component of the adductor muscle [ 14 ]. In addition, previous studies have assessed the relationship between sexual maturation and annual variation in adductor muscle, mantle, and digestive gland glycogen content in pen shells [ 6 ], and the organism nutritional status based on the variations in glycogen in the foot of ark shells [ 10 , 11 ]. In the Manila clam, few studies have also assessed the effect of annual and seasonal variations in soft tissues on its taste [ 15 , 16 ] and the glycogen variability associated with growth and sexual maturation [ 17 ]. However, whether glycogen content varies among different tissues and the seasonal changes in these bivalves has never been assessed. Then we have restricted the detailed estimation using the glycogen contents on physiological conditions of these species. Thus, in order to understand accumulation and seasonality of glycogen at the tissue level, seasonal variation in the amount of glycogen stored in different tissues was assessed in the three most commercially important bivalve species in the Ariake Bay: the pen shell, the ark shell, and the Manila clam. 2. Materials and Methods Pen shells (shell length 120–155 mm) and ark shells (shell length 22–33 mm) were collected from station 1 (St 1 in Figure 1 ), a tidal flat offshore from Yanagawa City, Fukuoka Prefecture, at four independent time points: in January (winter), April (spring), July (summer), and October (autumn), 2003. Manila clams (shell length 25–35 mm) were collected from station 2 (St 2 in Figure 1 ), a tidal flat offshore from Konagai Town, Isahaya City, Nagasaki Prefecture, in January, April, July, and October, 2007. After collection, the specimens were transported back to the laboratory, where all the shells were open after shell length was measured, and the different tissues were excised and stored frozen at −40°C until further analysis. The glycogen contents of the mantle, gill, adductor muscle, digestive gland, foot, kidney, and gonad were measured in pen shells. In ark shells, the glycogen contents of the mantle, gill, adductor muscle, digestive gland, foot, and gonad were measured, whereas in Manila clams, the glycogen contents in the mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad were measured. Figure 1: Sampling locations in Ariake Bay, West Japan. Glycogen analysis was performed following the anthrone method as previously described [ 18 ]. Through this method, 0.1–0.5 g of wet weight from various bivalve tissues is isolated and boiled in 1.5 mL solution of 30% potassium hydroxide for 20 minutes until all the tissue is dissolved. Subsequently, the samples were centrifuged, and 2.0 mL 95% ethanol solution and 0.25 mL of saturated sodium sulfate were added to each sample after cooling. The precipitate resulting from centrifuging the sample was resuspended in distilled water and boiled in anthrone reagent, and the absorbance at 620 nm was measured after cooling. Commercially available glycogen (Wako Pure Chemical Industries, Ltd., Japan) was used for the glycogen standard curve. The glycogen content was expressed per 1 g wet weight of bivalve tissue. Multiple comparison of the glycogen content in each tissue on each month was analyzed to make clear main storage tissues on each month and the seasonality on each tissue for glycogen by the Tukey-Kramer test with α set at . 3. Results and Discussion 3.1. Pen Shells Glycogen was detected in all the tissues (the mantle, gill, adductor muscle, digestive gland, foot, kidney, and gonad), and the glycogen contents measured throughout the study period were 2–13, 4–8, 8–33, 3–5, 9–15, 7–14, and 2–9 mg/g, respectively (Figure 2 ). In addition, glycogen was clearly present in the adductor muscle throughout the year. In this tissue, glycogen content increased in January and April and decreased in July and October. Similar variation was also observed in the other tissues, but it was not as pronounced due to the low amounts of glycogen detected compared to the adductor muscle. On the other hand, glycogen content in April, when it showed highest level in the adductor muscle, varied among tissues, decreasing from the adductor muscle, followed by the foot, kidney, mantle, gonad, gill, and digestive gland in this order. Yurimoto et al. [ 6 ] monitored annual changes in glycogen content in adductor muscle, digestive gland, and mantle in pen shells from the Ariake Bay and showed an almost lack of seasonal variation in the digestive gland glycogen content, which remains low, below 10 mg/g throughout the year. The content in the adductor muscle and mantle, on the other hand, showed a clear variation from a few to 78 mg/g and from a few to 23 mg/g, respectively. In both of these organs, glycogen content peaked in spring (April) and remained low, around only few mg/g, in the autumn season (October to December) after spawning. In the present study, only a small seasonal variation was observed in gill, digestive gland, foot, and kidney, where the glycogen content remained nearly constant throughout the year. On the other hand, glycogen contents in the mantle, adductor muscle, and gonad showed large variations, increasing in spring (April) and decreasing in autumn (October). In addition, glycogen content in the adductor muscle in April was significantly higher, by twofold, than that of the other tissues during the same period. These results also revealed that the adductor muscle in pen shells was the main storage tissue for glycogen and it was peaked during spring. Figure 2: Seasonal changes in glycogen content in different tissues collected from the pen shell, Atrina lischkeana . Bars represent means and whiskers represent standard deviation. 3–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 3.2. Ark Shells Glycogen was also detected in all the tissues analyzed in ark shells (mantle, gill, adductor muscle, digestive gland, foot, and gonad), and the amount measured throughout the study period in each of these tissues was 9–22, 6–16, 10–30, 7–16, 13–36, and 5–14 mg/g, respectively (Figure 3 ). In addition, seasonal variation in glycogen content followed a similar pattern in all the tissues, with the glycogen increasing markedly in January and April, and decreasing in July and slightly in October. On the other hand, glycogen content varied among tissues, being larger in the foot in January, to decrease in the adductor muscle, mantle, digestive gland, gill, and gonad in this order. Yurimoto et al. [ 10 ] assessed the nutritional status of ark shells reared in captivity and its association with foot glycogen content. They showed that glycogen content in between spring and autumn (April to October) varied between 17 mg/g and 61 mg/g, showing the highest and lowest values in April and July, respectively. In addition, Yurimoto et al. [ 11 ] revealed that glycogen was present in different organs, including mantle, gill, adductor muscle, digestive gland, and foot in ark shells from the Ariake Bay, measured in April. In the same study, the shell foot showed a significantly higher amount of glycogen (60 mg/g over) compared to the other tissues, varying between about 20 mg/g in the summer and 40 mg/g or higher in the spring. However, Yurimoto et al. [ 10 , 11 ] did not estimate seasonal variation in glycogen content in any of the other tissues. In this study, seasonal variation in the glycogen content was measured in six different organs, including gill, adductor muscle, digestive gland, foot, and gonad, in ark shells from a tidal flat in Ariake Bay. Glycogen was detected in all the tissues measured, presenting its higher concentration in the foot, following in the adductor muscle and mantle. In addition, the amount of glycogen accumulated in gill, digestive gland, and gonad in was lower than the amount detected from the other three organs, although, quantitatively, the differences among these tissues remained unclear. Following the results by Yurimoto et al. [ 10 , 11 ], the glycogen content measured from all the tissues, including the foot, decreased in summer (July). In this study, the glycogen content remained constant in the different tissues measured in ark shells between winter and spring, and decreased in summer; however, the extent of the decrease varied among tissues. The foot appeared as the main storage location for glycogen in this species. Figure 3: Seasonal changes in glycogen content in different tissues from ark shells, Scapharca kagoshimensis . Bars represent means and whiskers represent standard deviation. 4–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 3.3. Manila Clams Glycogen was also detected in all Manila clam tissues (mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad), and the amounts measured in these tissues throughout the study period were 7–17, 5–8, 15–34, 11–14, 12–46, 6–12, and 12–15 mg/g, respectively (Figure 4 ). In addition, glycogen was clearly present in the adductor muscle and foot throughout the year, increasing in both tissues in April and July, and decreasing in January and October. Glycogen prevalence was not observed in other tissues, where the content remained nearly constant through the year. Glycogen content also varied among tissues in this species, being higher in the foot in July, to decrease in the adductor muscle, mantle, gonad, digestive gland, siphon, and gill, in this order. Takagi and Simidu [ 15 ] analyzed the amount of glycogen in soft tissues of Manila clams from Maizuru Bay, in West Japan in January, March, June, September, and November. The proportion of glycogen, in wet weight of soft tissue, varied between 1.0% and 2.5%, increasing in June and decreasing in November. In a similar study, Shiraishi et al. [ 16 ] sampled Manila clams throughout a full year in the Fukuoka coast, Fukuoka Prefecture, West Japan. The proportion of glycogen, in wet weight of the soft tissue, ranged between 0.5% and 5.2%, showing its highest values in August and minimum values in December. Robert et al. [ 17 ] collected Manila clams in the inner part and the mouth of Arcachon Bay, a section of the Bay of Biscay in France. They monitored monthly variation in glycogen content in soft tissues and showed that glycogen content significantly decreased with sexual maturity. However, they did not assess seasonal variation in glycogen in different tissues. In this study, data on seasonal variation in glycogen content were collected from seven organs, including mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad, from Manila clams collected in Ariake Bay. Glycogen was detected from all the tissues analyzed. In addition, high levels of glycogen and a marked seasonal variation were observed in foot, adductor muscle, and mantle. On the other hand, the gill, digestive gland, siphon, and gonad showed lower glycogen contents and less marked seasonal variation than the foot, adductor muscle, and mantle. In addition, the seasonal variation in glycogen contents among tissues was high in April and July and low in January and October. These results agree with the seasonal variation in glycogen content from Manila clam soft tissues reported by Takagi and Simidu [ 15 ] and Shiraishi et al. [ 16 ]. In addition, the foot was shown as the main glycogen reservoir in this species. Figure 4: Seasonal changes in glycogen content in different tissues removed from Manila clams, Ruditapes philippinarum . Bars represent mean and whiskers represent standard deviation. 3–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 4. Conclusion Glycogen accumulation and seasonal variation in different tissues in pen shells, ark shells, and Manila clams collected in Ariake Bay were examined throughout a year. The adductor muscle appeared as the main glycogen reservoir in pen shells, while foot appears as the main reservoir organ in ark shells and Manila clams. The periods of higher and lower accumulation of glycogen in the reservoirs also varied among species. Pen shells showed a glycogen peak in spring and the lowest values in autumn, ark shells showed a peak in winter-spring and the lowest values in summer-autumn, while Manila clams showed a peak in spring-summer and the lowest values in autumn-winter. These results revealed as useful organs to assess individual physiological condition based on glycogen content variation on the three species. Conflict of Interests The author declares that there is no conflict of interests regarding the publication of this paper. Acknowledgment This study was partially supported by the ordinary research budget of the Seikai National Fisheries Research Institute, Fisheries Research Agency in Japan, when the author was a researcher of the institute. References M. M. Bloomfield, Chemistry and the Living Organism , Maruzen-Wiley, Tokyo, Japan, 5th edition, 1995. T. Imai, Aquacultures in Shallow Water , Kouseishya-Kouseikaku, Tokyo, Japan, 1971. E. Gosling, Bivalve Mollusks Biology-Ecology and Culture , Fishing News Books, Oxford, UK, 2003. N. Uzaki, M. Kai, H. Aoyama, and T. Suzuki, “Changes in mortality rate and glycogen content of the Manila clam Ruditapes philippinarum during the development of oxygen-deficient waters,” Fisheries Science , vol. 69, no. 5, pp. 936–943, 2003. View at Publisher · View at Google Scholar · View at Scopus K. Brokordt and H. Guderley, “Binding of glycolytic enzymes in adductor muscle of Iceland scallop Chlamys islandica is altered by reproductive status,” Marine Ecology Progress Series , vol. 268, pp. 141–149, 2004. View at Publisher · View at Google Scholar · View at Scopus T. Yurimoto, Y. Maeno, S. Matsui, N. Yoshioka, and Y. Watanabe, “The relationship between sexual maturation and glycogen contents in visceral organs of the pen shell Atrina pectinata in Ariake Bay, Japan,” Aquaculture science (Suisanzoshoku) , vol. 53, pp. 397–404, 2005. Y. Yamamura and T. Watanabe, “Seasonal changes of glycogen content in oysters in Matsushima Bay, Japan,” Bulletin of the Tohoku Branch of the Japanese Society of Scientific Fisheries , vol. 16, pp. 22–26, 1964. S. Akashige and T. Fushimi, “Growth, survival, and glycogen content of triploid Pacific oyster Crassostrea gigas in the waters of Hiroshima, Japan,” Bulletin of the Japanese Society for the Scientific Fisheries , vol. 58, no. 6, pp. 1063–1071, 1992. View at Publisher · View at Google Scholar Y. Shinomiya, S. Iwanaga, T. Yamaguchi, K. Kohno, and Y. Uchimura, “Relationship between autumn mortality, glycogen content, and carbohydrate metabolism enzyme activity in Japanese pearl oyster Pinctada fucata martensii ,” Aquaculture Science (Suisanzoshoku) , vol. 45, pp. 47–53, 1997. T. Yurimoto, H. Nasu, N. Tobase, and Y. Maeno, “Growth, survival and feeding of ark shell Scapharca kagoshimensis with hung and settled culture in Ariake Bay, Japan,” Aquaculture Science (Suisanzoshoku) , vol. 55, pp. 535–540, 2007. T. Yurimoto, Y. Mori, S. Ito, and Y. Maeno, “Reproductive cycle of the subcrenated ark shell Scapharca kagoshimensis (Tokunaga, 1906) in Ariake Bay, Japan,” Journal of Shellfish Research , vol. 27, no. 5, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus H. Sekiguchi and R. Ishii, “Drastic decreasing of annual catch yields of the Manila clam Ruditapes philippinarum in Ariake Sound, southern Japan,” Oceanography in Japan , vol. 12, pp. 21–36, 2003. S. Ito, “The status and recovery of marine resources in the Ariake sound,” Bulletin of Saga Prefectural Ariake Fisheries Research and Development Center , vol. 22, pp. 69–80, 2004. M. Ogushi and R. Harada, “Taste-active components in adductor muscle extracts from pen shell ( Atrina japonica ) and hen clam ( Mactra chinensis ),” Journal of Sagami Women's University B , vol. 58, pp. 95–101, 1994. I. Takagi and W. Simidu, “Studies on muscle of aquatic animals-XXXV: seasonal variation of chemical constituents and extractive nitrogens in some species of shellfish,” Bulletin of the Japanese Society of Scientific Fisheries , vol. 29, pp. 66–70, 1963. A. Shiraishi, S. Cho, and K. Mishima, “Seasonal changes of biochemical composition in muscular and visceral parts of short-neck clam, Ruditapes philippinarum ,” Journal of Home Economics of Japan , vol. 46, pp. 313–319, 1995. R. Robert, G. Trut, and J. L. Laborde, “Growth, reproduction and gross biochemical composition of the Manila clam Ruditapes philippinarum in the Bay of Arcachon, France,” Marine Biology , vol. 116, no. 2, pp. 291–299, 1993. View at Publisher · View at Google Scholar · View at Scopus H. Kamada and T. Hamada, “Comparison of anthrone and enzymatic methods for hepatic glycogen analyses,” Bulletin of National Institute of Animal Industry , vol. 43, pp. 85–91, 1985. (function (i, s, o, g, r, a, m) { i['GoogleAnalyticsObject'] = r; i[r] = i[r] || function () { (i[r].q = i[r].q || []).push(arguments) }, i[r].l = 1 * new Date(); a = s.createElement(o), m = s.getElementsByTagName(o)[0]; a.async = 1; a.src = g; m.parentNode.insertBefore(a, m) })(window, document, 'script', '//www.google-analytics.com/analytics.js', 'ga'); ga('create', 'UA-8578054-2', 'auto'); ga('send', 'pageview'); http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Marine Biology Hindawi Publishing Corporation

Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan

Journal of Marine Biology , Volume 2015 (2015) – Feb 24, 2015

Loading next page...
 
/lp/hindawi-publishing-corporation/seasonal-changes-in-glycogen-contents-in-various-tissues-of-the-edible-oYyOZpGYNb

References

References for this paper are not available at this time. We will be adding them shortly, thank you for your patience.

Publisher
Hindawi Publishing Corporation
Copyright
Copyright © 2015 Tatsuya Yurimoto.
ISSN
1687-9481
eISSN
1687-949X
Publisher site
See Article on Publisher Site

Abstract

Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana, Ark Shell Scapharca kagoshimensis, and Manila Clam Ruditapes philippinarum in West Japan <meta name="citation_title" content="Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan"/> <meta name="dc.title" content="Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan"/> div.banner_title_bkg div.trangle { border-color: #9E6C84 transparent transparent transparent; opacity:0.77; /*new styles start*/ -ms-filter:"progid:DXImageTransform.Microsoft.Alpha(Opacity=77)" ;filter: alpha(opacity=77); /*new styles end*/ } div.banner_title_bkg_if div.trangle { border-color: transparent transparent #9E6C84 transparent ; opacity:0.77; /*new styles start*/ -ms-filter:"progid:DXImageTransform.Microsoft.Alpha(Opacity=77)" ;filter: alpha(opacity=77); /*new styles end*/ } div.banner_title_bkg div.trangle { width: 249px; } #banner { background-image: url('http://images.hindawi.com/journals/jmb/jmb.banner.jpg'); background-position: 50% 0;} Hindawi Publishing Corporation Home Journals About Us Journal of Marine Biology About this Journal Submit a Manuscript Table of Contents Journal Menu About this Journal · Abstracting and Indexing · Advance Access · Aims and Scope · Article Processing Charges · Articles in Press · Author Guidelines · Bibliographic Information · Citations to this Journal · Contact Information · Editorial Board · Editorial Workflow · Free eTOC Alerts · Publication Ethics · Reviewers Acknowledgment · Submit a Manuscript · Subscription Information · Table of Contents Open Special Issues · Published Special Issues · Special Issue Guidelines Abstract Full-Text PDF Full-Text HTML Full-Text ePUB Linked References How to Cite this Article Journal of Marine Biology Volume 2015 (2015), Article ID 593032, 5 pages http://dx.doi.org/10.1155/2015/593032 Research Article Seasonal Changes in Glycogen Contents in Various Tissues of the Edible Bivalves, Pen Shell Atrina lischkeana , Ark Shell Scapharca kagoshimensis , and Manila Clam Ruditapes philippinarum in West Japan Tatsuya Yurimoto Japan International Research Center for Agricultural Sciences, Ohwashi, Tsukuba 305-8686, Japan Received 8 August 2014; Revised 10 January 2015; Accepted 28 January 2015 Academic Editor: Tatsuya Sakamoto Copyright © 2015 Tatsuya Yurimoto. This is an open access article distributed under the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract The types of tissues accumulating glycogen and seasonal changes in glycogen content were investigated in the following shell species: pen shell Atrina lischkeana , ark shell Scapharca kagoshimensis , and Manila clam Ruditapes philippinarum . Comparison of the results showed that the adductor muscle or foot was the main glycogen reservoir and the levels varied seasonally. The adductor muscle in the pen shell showed higher glycogen content during spring and lower content during autumn. The ark shell, on the other hand, showed higher content during winter and spring and lower content during summer and autumn, while the Manila clam showed higher glycogen content during spring and summer and lower content during autumn and winter. These results revealed that the adductor muscle in pen shells and the foot in ark shells and Manila clams act as the main storage tissues for glycogen in the three species studied and that these tissues are suitable to analyze glycogen prevalence to estimate individual physiological condition. 1. Introduction Glycogen is a water-soluble polysaccharide, composed by polymerized glucose molecules joined through glycosidic bonds, forming a network-like structure [ 1 ]. It represents the main form of energy storage in the animal bodies along with body fat. In particular, bivalves present higher percentage of glycogen compared to fat, and its contents are influenced by internal factors, such as growth and sexual maturation, and external factors, such as food availability and other environmental factors [ 2 – 6 ]. Thus, glycogen content varies depending on the physiological state of the organism, and it can be used to evaluate physiological condition in different bivalve species, including Pacific oysters ( Crassostrea gigas ), pearl oysters ( Pinctada fucata martensii ), Manila clams ( Ruditapes philippinarum ), and ark shells ( Scapharca kagoshimensis ) [ 7 – 11 ]. Ariake Bay is a one of the most famous fishery grounds for bivalves such as pen shells ( Atrina lischkeana ), ark shells, and Manila clams in West Japan. However, landings of these species have remained at low levels for recent years, due to environmental changes that coastal development is considering to contribute the frequently occurrence of red tide and hypoxic water. Therefore population stabilization of these in the bay has become a pressing issue for local fisheries [ 12 , 13 ]. Set against this background, identifying a maker able to provide information on bivalve physiological condition in situ would facilitate reaching stable fishing production for these species. So far, glycogen content and its variation have been assessed in pen shells as an important taste component of the adductor muscle [ 14 ]. In addition, previous studies have assessed the relationship between sexual maturation and annual variation in adductor muscle, mantle, and digestive gland glycogen content in pen shells [ 6 ], and the organism nutritional status based on the variations in glycogen in the foot of ark shells [ 10 , 11 ]. In the Manila clam, few studies have also assessed the effect of annual and seasonal variations in soft tissues on its taste [ 15 , 16 ] and the glycogen variability associated with growth and sexual maturation [ 17 ]. However, whether glycogen content varies among different tissues and the seasonal changes in these bivalves has never been assessed. Then we have restricted the detailed estimation using the glycogen contents on physiological conditions of these species. Thus, in order to understand accumulation and seasonality of glycogen at the tissue level, seasonal variation in the amount of glycogen stored in different tissues was assessed in the three most commercially important bivalve species in the Ariake Bay: the pen shell, the ark shell, and the Manila clam. 2. Materials and Methods Pen shells (shell length 120–155 mm) and ark shells (shell length 22–33 mm) were collected from station 1 (St 1 in Figure 1 ), a tidal flat offshore from Yanagawa City, Fukuoka Prefecture, at four independent time points: in January (winter), April (spring), July (summer), and October (autumn), 2003. Manila clams (shell length 25–35 mm) were collected from station 2 (St 2 in Figure 1 ), a tidal flat offshore from Konagai Town, Isahaya City, Nagasaki Prefecture, in January, April, July, and October, 2007. After collection, the specimens were transported back to the laboratory, where all the shells were open after shell length was measured, and the different tissues were excised and stored frozen at −40°C until further analysis. The glycogen contents of the mantle, gill, adductor muscle, digestive gland, foot, kidney, and gonad were measured in pen shells. In ark shells, the glycogen contents of the mantle, gill, adductor muscle, digestive gland, foot, and gonad were measured, whereas in Manila clams, the glycogen contents in the mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad were measured. Figure 1: Sampling locations in Ariake Bay, West Japan. Glycogen analysis was performed following the anthrone method as previously described [ 18 ]. Through this method, 0.1–0.5 g of wet weight from various bivalve tissues is isolated and boiled in 1.5 mL solution of 30% potassium hydroxide for 20 minutes until all the tissue is dissolved. Subsequently, the samples were centrifuged, and 2.0 mL 95% ethanol solution and 0.25 mL of saturated sodium sulfate were added to each sample after cooling. The precipitate resulting from centrifuging the sample was resuspended in distilled water and boiled in anthrone reagent, and the absorbance at 620 nm was measured after cooling. Commercially available glycogen (Wako Pure Chemical Industries, Ltd., Japan) was used for the glycogen standard curve. The glycogen content was expressed per 1 g wet weight of bivalve tissue. Multiple comparison of the glycogen content in each tissue on each month was analyzed to make clear main storage tissues on each month and the seasonality on each tissue for glycogen by the Tukey-Kramer test with α set at . 3. Results and Discussion 3.1. Pen Shells Glycogen was detected in all the tissues (the mantle, gill, adductor muscle, digestive gland, foot, kidney, and gonad), and the glycogen contents measured throughout the study period were 2–13, 4–8, 8–33, 3–5, 9–15, 7–14, and 2–9 mg/g, respectively (Figure 2 ). In addition, glycogen was clearly present in the adductor muscle throughout the year. In this tissue, glycogen content increased in January and April and decreased in July and October. Similar variation was also observed in the other tissues, but it was not as pronounced due to the low amounts of glycogen detected compared to the adductor muscle. On the other hand, glycogen content in April, when it showed highest level in the adductor muscle, varied among tissues, decreasing from the adductor muscle, followed by the foot, kidney, mantle, gonad, gill, and digestive gland in this order. Yurimoto et al. [ 6 ] monitored annual changes in glycogen content in adductor muscle, digestive gland, and mantle in pen shells from the Ariake Bay and showed an almost lack of seasonal variation in the digestive gland glycogen content, which remains low, below 10 mg/g throughout the year. The content in the adductor muscle and mantle, on the other hand, showed a clear variation from a few to 78 mg/g and from a few to 23 mg/g, respectively. In both of these organs, glycogen content peaked in spring (April) and remained low, around only few mg/g, in the autumn season (October to December) after spawning. In the present study, only a small seasonal variation was observed in gill, digestive gland, foot, and kidney, where the glycogen content remained nearly constant throughout the year. On the other hand, glycogen contents in the mantle, adductor muscle, and gonad showed large variations, increasing in spring (April) and decreasing in autumn (October). In addition, glycogen content in the adductor muscle in April was significantly higher, by twofold, than that of the other tissues during the same period. These results also revealed that the adductor muscle in pen shells was the main storage tissue for glycogen and it was peaked during spring. Figure 2: Seasonal changes in glycogen content in different tissues collected from the pen shell, Atrina lischkeana . Bars represent means and whiskers represent standard deviation. 3–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 3.2. Ark Shells Glycogen was also detected in all the tissues analyzed in ark shells (mantle, gill, adductor muscle, digestive gland, foot, and gonad), and the amount measured throughout the study period in each of these tissues was 9–22, 6–16, 10–30, 7–16, 13–36, and 5–14 mg/g, respectively (Figure 3 ). In addition, seasonal variation in glycogen content followed a similar pattern in all the tissues, with the glycogen increasing markedly in January and April, and decreasing in July and slightly in October. On the other hand, glycogen content varied among tissues, being larger in the foot in January, to decrease in the adductor muscle, mantle, digestive gland, gill, and gonad in this order. Yurimoto et al. [ 10 ] assessed the nutritional status of ark shells reared in captivity and its association with foot glycogen content. They showed that glycogen content in between spring and autumn (April to October) varied between 17 mg/g and 61 mg/g, showing the highest and lowest values in April and July, respectively. In addition, Yurimoto et al. [ 11 ] revealed that glycogen was present in different organs, including mantle, gill, adductor muscle, digestive gland, and foot in ark shells from the Ariake Bay, measured in April. In the same study, the shell foot showed a significantly higher amount of glycogen (60 mg/g over) compared to the other tissues, varying between about 20 mg/g in the summer and 40 mg/g or higher in the spring. However, Yurimoto et al. [ 10 , 11 ] did not estimate seasonal variation in glycogen content in any of the other tissues. In this study, seasonal variation in the glycogen content was measured in six different organs, including gill, adductor muscle, digestive gland, foot, and gonad, in ark shells from a tidal flat in Ariake Bay. Glycogen was detected in all the tissues measured, presenting its higher concentration in the foot, following in the adductor muscle and mantle. In addition, the amount of glycogen accumulated in gill, digestive gland, and gonad in was lower than the amount detected from the other three organs, although, quantitatively, the differences among these tissues remained unclear. Following the results by Yurimoto et al. [ 10 , 11 ], the glycogen content measured from all the tissues, including the foot, decreased in summer (July). In this study, the glycogen content remained constant in the different tissues measured in ark shells between winter and spring, and decreased in summer; however, the extent of the decrease varied among tissues. The foot appeared as the main storage location for glycogen in this species. Figure 3: Seasonal changes in glycogen content in different tissues from ark shells, Scapharca kagoshimensis . Bars represent means and whiskers represent standard deviation. 4–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 3.3. Manila Clams Glycogen was also detected in all Manila clam tissues (mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad), and the amounts measured in these tissues throughout the study period were 7–17, 5–8, 15–34, 11–14, 12–46, 6–12, and 12–15 mg/g, respectively (Figure 4 ). In addition, glycogen was clearly present in the adductor muscle and foot throughout the year, increasing in both tissues in April and July, and decreasing in January and October. Glycogen prevalence was not observed in other tissues, where the content remained nearly constant through the year. Glycogen content also varied among tissues in this species, being higher in the foot in July, to decrease in the adductor muscle, mantle, gonad, digestive gland, siphon, and gill, in this order. Takagi and Simidu [ 15 ] analyzed the amount of glycogen in soft tissues of Manila clams from Maizuru Bay, in West Japan in January, March, June, September, and November. The proportion of glycogen, in wet weight of soft tissue, varied between 1.0% and 2.5%, increasing in June and decreasing in November. In a similar study, Shiraishi et al. [ 16 ] sampled Manila clams throughout a full year in the Fukuoka coast, Fukuoka Prefecture, West Japan. The proportion of glycogen, in wet weight of the soft tissue, ranged between 0.5% and 5.2%, showing its highest values in August and minimum values in December. Robert et al. [ 17 ] collected Manila clams in the inner part and the mouth of Arcachon Bay, a section of the Bay of Biscay in France. They monitored monthly variation in glycogen content in soft tissues and showed that glycogen content significantly decreased with sexual maturity. However, they did not assess seasonal variation in glycogen in different tissues. In this study, data on seasonal variation in glycogen content were collected from seven organs, including mantle, gill, adductor muscle, digestive gland, foot, siphon, and gonad, from Manila clams collected in Ariake Bay. Glycogen was detected from all the tissues analyzed. In addition, high levels of glycogen and a marked seasonal variation were observed in foot, adductor muscle, and mantle. On the other hand, the gill, digestive gland, siphon, and gonad showed lower glycogen contents and less marked seasonal variation than the foot, adductor muscle, and mantle. In addition, the seasonal variation in glycogen contents among tissues was high in April and July and low in January and October. These results agree with the seasonal variation in glycogen content from Manila clam soft tissues reported by Takagi and Simidu [ 15 ] and Shiraishi et al. [ 16 ]. In addition, the foot was shown as the main glycogen reservoir in this species. Figure 4: Seasonal changes in glycogen content in different tissues removed from Manila clams, Ruditapes philippinarum . Bars represent mean and whiskers represent standard deviation. 3–6 samples (replicates) were used for the analysis of each organ. No common letters out of parentheses indicate significant differences of glycogen contents in different tissues on each month and no common letters in parentheses indicate significant differences of seasonal changes on each tissue ( ; Tukey-Kramer test). 4. Conclusion Glycogen accumulation and seasonal variation in different tissues in pen shells, ark shells, and Manila clams collected in Ariake Bay were examined throughout a year. The adductor muscle appeared as the main glycogen reservoir in pen shells, while foot appears as the main reservoir organ in ark shells and Manila clams. The periods of higher and lower accumulation of glycogen in the reservoirs also varied among species. Pen shells showed a glycogen peak in spring and the lowest values in autumn, ark shells showed a peak in winter-spring and the lowest values in summer-autumn, while Manila clams showed a peak in spring-summer and the lowest values in autumn-winter. These results revealed as useful organs to assess individual physiological condition based on glycogen content variation on the three species. Conflict of Interests The author declares that there is no conflict of interests regarding the publication of this paper. Acknowledgment This study was partially supported by the ordinary research budget of the Seikai National Fisheries Research Institute, Fisheries Research Agency in Japan, when the author was a researcher of the institute. References M. M. Bloomfield, Chemistry and the Living Organism , Maruzen-Wiley, Tokyo, Japan, 5th edition, 1995. T. Imai, Aquacultures in Shallow Water , Kouseishya-Kouseikaku, Tokyo, Japan, 1971. E. Gosling, Bivalve Mollusks Biology-Ecology and Culture , Fishing News Books, Oxford, UK, 2003. N. Uzaki, M. Kai, H. Aoyama, and T. Suzuki, “Changes in mortality rate and glycogen content of the Manila clam Ruditapes philippinarum during the development of oxygen-deficient waters,” Fisheries Science , vol. 69, no. 5, pp. 936–943, 2003. View at Publisher · View at Google Scholar · View at Scopus K. Brokordt and H. Guderley, “Binding of glycolytic enzymes in adductor muscle of Iceland scallop Chlamys islandica is altered by reproductive status,” Marine Ecology Progress Series , vol. 268, pp. 141–149, 2004. View at Publisher · View at Google Scholar · View at Scopus T. Yurimoto, Y. Maeno, S. Matsui, N. Yoshioka, and Y. Watanabe, “The relationship between sexual maturation and glycogen contents in visceral organs of the pen shell Atrina pectinata in Ariake Bay, Japan,” Aquaculture science (Suisanzoshoku) , vol. 53, pp. 397–404, 2005. Y. Yamamura and T. Watanabe, “Seasonal changes of glycogen content in oysters in Matsushima Bay, Japan,” Bulletin of the Tohoku Branch of the Japanese Society of Scientific Fisheries , vol. 16, pp. 22–26, 1964. S. Akashige and T. Fushimi, “Growth, survival, and glycogen content of triploid Pacific oyster Crassostrea gigas in the waters of Hiroshima, Japan,” Bulletin of the Japanese Society for the Scientific Fisheries , vol. 58, no. 6, pp. 1063–1071, 1992. View at Publisher · View at Google Scholar Y. Shinomiya, S. Iwanaga, T. Yamaguchi, K. Kohno, and Y. Uchimura, “Relationship between autumn mortality, glycogen content, and carbohydrate metabolism enzyme activity in Japanese pearl oyster Pinctada fucata martensii ,” Aquaculture Science (Suisanzoshoku) , vol. 45, pp. 47–53, 1997. T. Yurimoto, H. Nasu, N. Tobase, and Y. Maeno, “Growth, survival and feeding of ark shell Scapharca kagoshimensis with hung and settled culture in Ariake Bay, Japan,” Aquaculture Science (Suisanzoshoku) , vol. 55, pp. 535–540, 2007. T. Yurimoto, Y. Mori, S. Ito, and Y. Maeno, “Reproductive cycle of the subcrenated ark shell Scapharca kagoshimensis (Tokunaga, 1906) in Ariake Bay, Japan,” Journal of Shellfish Research , vol. 27, no. 5, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus H. Sekiguchi and R. Ishii, “Drastic decreasing of annual catch yields of the Manila clam Ruditapes philippinarum in Ariake Sound, southern Japan,” Oceanography in Japan , vol. 12, pp. 21–36, 2003. S. Ito, “The status and recovery of marine resources in the Ariake sound,” Bulletin of Saga Prefectural Ariake Fisheries Research and Development Center , vol. 22, pp. 69–80, 2004. M. Ogushi and R. Harada, “Taste-active components in adductor muscle extracts from pen shell ( Atrina japonica ) and hen clam ( Mactra chinensis ),” Journal of Sagami Women's University B , vol. 58, pp. 95–101, 1994. I. Takagi and W. Simidu, “Studies on muscle of aquatic animals-XXXV: seasonal variation of chemical constituents and extractive nitrogens in some species of shellfish,” Bulletin of the Japanese Society of Scientific Fisheries , vol. 29, pp. 66–70, 1963. A. Shiraishi, S. Cho, and K. Mishima, “Seasonal changes of biochemical composition in muscular and visceral parts of short-neck clam, Ruditapes philippinarum ,” Journal of Home Economics of Japan , vol. 46, pp. 313–319, 1995. R. Robert, G. Trut, and J. L. Laborde, “Growth, reproduction and gross biochemical composition of the Manila clam Ruditapes philippinarum in the Bay of Arcachon, France,” Marine Biology , vol. 116, no. 2, pp. 291–299, 1993. View at Publisher · View at Google Scholar · View at Scopus H. Kamada and T. Hamada, “Comparison of anthrone and enzymatic methods for hepatic glycogen analyses,” Bulletin of National Institute of Animal Industry , vol. 43, pp. 85–91, 1985. (function (i, s, o, g, r, a, m) { i['GoogleAnalyticsObject'] = r; i[r] = i[r] || function () { (i[r].q = i[r].q || []).push(arguments) }, i[r].l = 1 * new Date(); a = s.createElement(o), m = s.getElementsByTagName(o)[0]; a.async = 1; a.src = g; m.parentNode.insertBefore(a, m) })(window, document, 'script', '//www.google-analytics.com/analytics.js', 'ga'); ga('create', 'UA-8578054-2', 'auto'); ga('send', 'pageview');

Journal

Journal of Marine BiologyHindawi Publishing Corporation

Published: Feb 24, 2015

There are no references for this article.