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Dev. Reprod. Vol. 14, No. 1, 7-11 (2010)

Germ Cell Aspiration (GCA) Method as a Non-fatal Technique for Sex Identification in Two Bivalves

(Gomphina veneriformis and Tegillaca granosa)

Jung Sick Lee1, Sun Mi Ju1, Ji Seon Park1, Young Guk Jin2, Yun Kyung Shin3 and Jung Jun Park4

1Dept. of Aqualife Medicine, Chonnam National University, Yeosu 550-749, Korea
2South Sea Fisheries Research Institute, National Fisheries Research and Development Institute, Yeosu 556-823, Korea 3Aquaculture Management Division, National Fisheries Research and Development Institute, Busan 619-705, Korea
4Pathology Division, National Fisheries Research and Development Institute, Busan 619-705, Korea

ABSTRACT : This study attempted to verify the possibility of using germ cell aspiration (GCA) method as a non-fatal technique in studying the life-history of equilateral venus, Gomphina veneriformis (Veneridae) and granular ark, Tegillarca granosa (Arcidae). Using twenty-six gauge 1/2" (12.7㎜) needle, GCA was carried out in equilateral venus through external ligament. In granular ark, GCA was performed by preventing closure of the shells by inserting a tongue depressor between the shells while still open. The success rate of sex identification using the GCA method was 95.6% for the equilateral venus (n=650/680) and 94.3% for the granular ark (n=707/750). Mortality of equilateral venus, which spent 33 days under wild conditions, was 13.8% (n=90/650) while the mortality of granular ark, which spent 390 days under wild conditions, was 2.4% (n=17/707). Although we believe that GCA does not appear to cause death in equilateral venus or granular ark, the success rate in employing of this methodology may differ depending on the level of proficiency of the researcher and reproductive stage of the bivalve. This study concludes that GCA is a convenient non-fatal methodology, which can be employed to identify sex and investigate gonadal maturity in Gomphina veneriformis and Tegillarca granosa.
Key words : Germ cell aspiration, Gomphina veneriformis, Tegillarca granosa, Sex identification, Gonadal maturity.

(Wright & Lindberg, 1979), Mytilus edulis (Jabbar &

Davies, 1987; Burton et al., 1996) and M ytilus galloprovincialis

  • (Mikailov et al., 1995).
  • Information on sex, gonadal maturity and spawning

periodicity are equally important in artificial seed production of these organisms. Reproductive history and sexual maturation of bivalves differ in accordance with various environmental factors, including water temperature (Eversole, 2001).
Sex identification and gonadal maturity of bivalves are, in general, have been assessed through histological and microscopic analysis. However, such methods cannot be applied without sacrificing the organism. Previous studies have attempted to investigate the possibility of sex determination without killing the organisms in patellacean gastropods
Equilateral venus, Gomphina veneriformis and granular ark, Tegillarca granosa were selected as the case-study species for this investigation. These are ecologically dominant bivalves in eastern and southern coastal waters of Korea, in addition to being economically valuable. This study attempted to verify the possibility of using germ cell aspiration (GCA) method as a non-fatal technique in studying the life-history and reproduction of bivalves.

1. Experimental Bivalves

Corresponding author: Jung Jun Park, National Fisheries Research and Development Institute, Pathology Division, 152-1 Haean-ro, Gijangeup, Gijang-gun, Busan 619-705, Korea. Tel: +82-51-720-2487, Fax: +82-51-720-2498, E-mail: [email protected]

Equilateral venus, Gomphina veneriformis (Bivalvia:

Veneridae) and granular ark, Tegillarca granosa (Bivalvia:

8

Lee JS, Ju SM, Park JS, Jin YG, Shin YK, Park JJ Dev. Reprod. Vol. 14, No. 1 (2010)

(Figs. 2G, H and 3G, H).

2. Syringe

Disposable syringes were employed in this experiment.
Two needle sizes were used; 29 gauge 1/2" (12.7 ㎜) (Becton Dickinson, U.S.A.) and 26 gauge 1/2" (12.7 ㎜) (Sung Shim Medical Co., Ltd., Korea). The size of the syringe needle was identified with considerations to clam size, inner diameter and length of the needle. Consequently, we identified that 29 gauge 1/2" (12.7 ㎜) needle was not appropriate for extraction of oocyte due to its narrow inner diameter. Accordingly, the 26 gauge 1/2" (12.7 ㎜) needle

Fig. 1. Sampling area of the experimental bivalves.

was used in most cases.
Arcidae) were used in the experiment. Equilateral venus was collected from the coastal region of Goseong on the eastern coast, while granular ark was collected from Jangsu Bay in Yeosu on the southern coast of Korea (Fig. 1). In relation to appropriate organism size and experimental timing the methodology of Park et al. (2003) and Lee (1997) were followed. Adults of 25.0-34.9 ㎜ in shell length were used (Figs. 2A, 3A), while experiments began in July to coincide with the ripe and spawning season

3. Germ Cell Aspiration

Equilateral venus, Gomphina veneriformis has a welldeveloped dorsal external ligament in the posterior portion of the umbo (Fig. 2B, C), which enables the needle to be inserted into the mantle cavity. Insert the syringe needle into the gonad of the visceral mass through the external ligament of the hinge line in a single thrust at an angle of approximately 45° (Fig. 2D). The shells of the granular ark, Tegillarca granosa are normally opened within the

Fig. 2. Equilateral venus, Gomphina veneriformis. (A) and (B) External morphology and external ligament (El). (C) Morphology of socket and teeth arrangement. (D) Syringe needle insertion through the external ligament. (E) Aspirated oocytes by syringe needle aspiration. (F) Aspirated spermatozoa by syringe needle aspiration. (G) Ovary of ripe stage. (H) Testis of ripe stage. Ct, cardinal tooth; Lt, lateral tooth; Oc, oocyte; S, socket; Sp, sperm.

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  • Dev. Reprod. Vol. 14, No. 1 (2010)
  • Sex Identificatioin by Germ Cell Aspiration (GCA) Method in Bivalves

Fig. 3. Granular ark, Tegillarca granosa. (A) and (B) External morphology and external ligament (El). (C) Morphology of socket and teeth arrangement. (D) Syringe needle insertion through between shells. (E) Aspirated oocytes by syringe needle aspiration. (F) Aspirated spermatozoa by syringe needle aspiration. (G) Ovary of ripe stage. (H) Testis of ripe stage. Oc, oocyte; S, socket; Sp, sperm; Sr, syringe; T, tooth; Td, tongue depressor.

aquarium (Fig. 3A). Although the external ligament of the granular ark is explicit and located in the umbo (Fig. 3B), needle insertion is prohibited by teeth which are regularly arranged in clusters (Fig. 3C). Accordingly, insert the tongue depressor into the area near the boundary of the shell for the organisms with their shells opened in order to prevent the shell from closing. Insert the syringe needle into the gonad of the visceral mass through the opened shells with a single thrust (Fig. 3D). observed over 390 days (July 7, 2006-August 1, 2007). The disparity in the experimental period between the two species was as a result of damage to the equilateral venus cage brought on by heavy wave action, thus making further continuation impractical.

5. Histological Technique

For light microscopy, the tissues were fixed in aqueous
Bouin’s solution for 18 hours and rinsed in running water for 36 hours. The tissues were dehydrated in ascending grades of ethyl alcohols and then embedded in paraplast (McCormick, USA). Embedded tissues were transversely sectioned at 5 ㎛ thickness and routinely stained with Mayer's hematoxylin - 0.5% eosin.

4. Mortality

Experimental organisms were reared in an indoor plastic aquarium for 3 days, where the 500ℓ seawater capacity was adequately filtered, aerated and kept at a salinity of 32.5‰ and a temperature of 20.5℃. Subsequently, the rearing experiment was carried out under wild conditions close to the collection area of the organisms. A cage where the bivalves could be prevented from escaping was installed. The bottom of the cage was securely inserted into the sediment in order to allow the organisms to be able to burrow. Equilateral venus was reared for 33 days (August 20, 2006-September 22, 2006), while granular ark was
Morphological and anatomical terminologies of Stachowitsch
(1992) were used.

1. Success Rate of Sex Identification using Germ
Cell Aspiration (GCA) Method

The success rate of sex identification using the GCA

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Lee JS, Ju SM, Park JS, Jin YG, Shin YK, Park JJ Dev. Reprod. Vol. 14, No. 1 (2010)

Table 1. Success rate of sex identification and mortality with GCA

  • Sex identification
  • Mortality

Species
Success rate

(n)

  • No. of
  • No. of
  • Indoor
  • Wild

  • inactive stage
  • spent stage
  • aquarium
  • condition

Gomphina veneriformis  95.6% (n=650/680) Tegillarca granosa  94.3% (n=707/750)

  • 2
  • 28

32
0% (n=0/650) 0% (n=0/707)
13.8% (n=90/650)

  • 2.4% (n=17/707)
  • 11

method was 95.6% for the equilateral venus (n=650/680) and 94.3% for the granular ark (n=707/750). Results of histological analysis of the 30 equilateral venus, for which sex identification was uncertain, revealed that 2 were in inactive reproductively while the remaining 28 were in the spent stage. Among the 43 granular ark for which sex identification was uncertain, 11 were inactive while the remaining 32 were spent reproductively (Table 1). was employed in this study as a possible alternative nonintrusive technique.
It is generally very difficult to identify sex in organisms for which sexual dimorphism is not definitive, without having to sacrifice the subject. Previous studies have attempted to investigate the possibility of sex identification in shelled molluscs without killing the organisms. Wright and & Lindberg (1979) verified the sex of patellacean gastropods by extracting germ cells through syringe insertion into the internal organs. For these gastropods, the abdominal portion gets exposed when detached from the substratum, thus making insertion of the syringe easier in comparison to bivalves. Furthermore, insertion locations for bivalves are complicated by their shape and consequent linkage of the hinge at the apex of the shell.

2. Mortality with GCA

In order to find out the effect of GCA on the death of these bivalves, experimental organisms were reared in an indoor plastic aquarium and wild condition.
Mortality for both species, after having been cultured for 3 days in the indoor aquarium, was 0%. Mortality of equilateral venus, which spent 33 days under wild conditions, was 13.8% (n=90/650) while the mortality of granular ark, which spent 390 days under wild conditions, was 2.4% (n=17/707) (Table 1).
The equilateral venus has a well-developed dorsal external ligament in the posterior portion of the umbo, on the basis of the right valve. The arrangement of teeth on the inner socket portion of apex of the shell is a heterodont type displaying definitive distinction between cardinal and lateral teeth. The external ligament covers the empty space between the rear portions of the lateral teeth, thus making it possible to insert the needle into the mantle cavity.
The external ligament of the granular ark is located in the umbo, and is wide and definitive. However, the arrangement of teeth on the inner socket portion of the external ligament is a taxodont type. With the regularly arranged teeth in clusters, insertion of the syringe needle is problematic. Accordingly, needle was inserted after having prevented closure of the shells by inserting a tongue depressor between the shells while still open.
Extraction of tissues from the internal organs while the organism is still alive, is very difficult, especially for molluscs such as gastropods or bivalves with thick exoskeleton. Currently, fine needle aspiration (FNA) is applied widely as a methodology in pathological diagnosis of human beings. However, there are technical difficulties and consequent cost-effectiveness issues associated with non-proficient researchers that maybe working with a large number of subjects. The germ cell aspiration (GCA) method using syringe

11

  • Dev. Reprod. Vol. 14, No. 1 (2010)
  • Sex Identificatioin by Germ Cell Aspiration (GCA) Method in Bivalves

Confirmation of oocyte in bivalves is relatively easier than sperm. However, if the oocyte is not detected, definitive identification of whether the extracted tissues are somatic cell debris or sperm becomes difficult. In such cases, confirmation of sex is possible through the addition of seawater, which allows sperm to display active mobility. Although confirmation of sperm is much easier under a phase contrast microscope, observation under a general microscope is also possible with a low light level.
No mortality was observed for organisms reared in the indoor aquarium for 3 days, illustrating that GCA method can be successfully applied to bivalves. There were also relatively low levels of mortality for equilateral venus (13.8%) and granular ark (2.4%), both of which were reared for 33 days and 390 days respectively under wild conditions, following the application of GCA.
Burton SA, Johnson GR, Davidson TJ (1996) Cytologic sexing of marine mussels (Mytilus edulis). J Shellfish Res 15:345-347.
Eversole AG (2001) Reproduction in Mercenaria mercenaria.
In: Kraeuter JN, Castagna M (eds.), Biology of the Hard Clam. Elsevier, New York, pp 221-260.
Jabbar A, Davies JI (1987) A simple and convenient biochemical method for sex identification in the marine mussel, Mytilus edulis L. J Exp Mar Biol Ecol 107: 39-44.
Lee JH (1997) Studies on the gonadal development and gametogenesis of the granulated ark, Tegillarca granosa (Linne). Korean J Malacol 13:55-64.
Mikailov AT, Torrado M, Mendez J (1995) Sexual differentiation of reproductive tissue in bivalve molluscs: identification of male associated polypeptide in the

mantle of Mytilus galloprovincialis Lmk. Int J Dev

Biol 39:545-548.
The possibility that the 13.8% mortality for the equilateral venus and 2.4% for the granular ark were due to the GCA application cannot be ruled out. However, we are confident that even if this methodology was partially responsible, in addition to other environmental factors, to mortality, the relative high survival rates of studied bivalves make it an appropriate technique.
Park JJ, Lee JY, Lee JS, Chang YJ (2003) Gonadal development and gametogenic cycle of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae). J

  • Korean Fish Soc 36:352-357.
  • Although the success rate of GCA method may differ

depending on the level of proficiency of the researcher and reproductive stage of the bivalves, it has been assessed, through this investigation, to be a convenient, practical, and non-fatal method of identifying sex, gonadal maturity and spawning periodicity of Gomphina veneriformis and

Tegillarca granosa.

Stachowitsch M (1992) Mollusca; Bivalvia (Lamellibranchia,
Pelycypoda). In: The Invertebrates; An Illustrated Glossary. Wiley-Liss Inc., New York, pp 227-237.
Wright WG, Lindberg DR (1979) A non-fatal method of sex determination for patellacean gastropods. J Mar Biol Assoc UK 59:803.

(received 15 January 2009, received in revised form 28 February 2010, accepted 2 March 2010)

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    Prioritized Species for Mariculture in India

    Prioritized Species for Mariculture in India Compiled & Edited by Ritesh Ranjan Muktha M Shubhadeep Ghosh A Gopalakrishnan G Gopakumar Imelda Joseph ICAR - Central Marine Fisheries Research Institute Post Box No. 1603, Ernakulam North P.O. Kochi – 682 018, Kerala, India www.cmfri.org.in 2017 Prioritized Species for Mariculture in India Published by: Dr. A Gopalakrishnan Director ICAR - Central Marine Fisheries Research Institute Post Box No. 1603, Ernakulam North P.O. Kochi – 682 018, Kerala, India www.cmfri.org.in Email: [email protected] Tel. No.: +91-0484-2394867 Fax No.: +91-0484-2394909 Designed at G.K. Print House Pvt. Ltd. Rednam Gardens Visakhapatnam- 530002, Andhra Pradesh Cell: +91 9848196095, www.gkprinthouse.com Cover page design: Abhilash P. R., CMFRI, Kochi Illustrations: David K. M., CMFRI, Kochi Publication, Production & Co-ordination: Library & Documentation Centre, CMFRI Printed on: November 2017 ISBN 978-93-82263-14-2 © 2017 ICAR - Central Marine Fisheries Research Institute, Kochi All rights reserved. Material contained in this publication may not be reproduced in any form without the permission of the publisher. Citation : Ranjan, R., Muktha, M., Ghosh, S., Gopalakrishnan, A., Gopakumar, G. and Joseph, I. (Eds.). 2017. Prioritized Species for Mariculture in India. ICAR-CMFRI, Kochi. 450 pp. CONTENTS Foreword ................................................................................................................. i Preface .................................................................................................................
  • Species Fact Sheets Anadara Granosa (Linnaeus, 1758)

    Species Fact Sheets Anadara Granosa (Linnaeus, 1758)

    Food and Agriculture Organization of the United Nations Fisheries and for a world without hunger Aquaculture Department Species Fact Sheets Anadara granosa (Linnaeus, 1758) Anadara granosa: (click for more) Synonyms Arca (Tegillarca) granosa Linnaeus, 1758 Anadara bisenensis Shrenck & Reinhart, 1938 Anadara obessa Kotaka, 1953 Anadara granosa kamakurensis Noda, 1966 FAO Names En - Blood cockle, Fr - Arche granuleuse, Sp - Arca del Pacífico occidental. 3Alpha Code: BLC Taxonomic Code: 3160407101 Scientific Name with Original Description Arca granosa Linnaeus, 1758. Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Edition 10, Tomus 1, Holmiae. 824 pp. Diagnostic Features Shell equivalve, thick and solid, ovate, strongly inflated, slightly longer than high and feebly inequilateral (Poutiers, 1998). Umbones strongly protruding, cardinal area rather large. About 18 radial ribs (15 to 20) with wide interstices at each valve. Ribs stout and distinctly rugose, bearing regular,often rectangular nodules. Periostracum rather thin and smooth. Internal margins with strong crenulations corresponding with the external radial ribs. No byssal gape. Outside of shell white under the yellowish brown periostracum. Inner side white, often tinged light yellow towards the umbonal cavity. Geographical Distribution Widespread in the Indo-West Pacific, from East Africa to Polynesia. North to Japan and south to northern and FAO Fisheries and Aquaculture Department eastern Australia. Launch the Aquatic Species Distribution map viewer Habitat and Biology A. granosa can live in 20m water depth but concentrates in the littoral area (time for ground drying: 6 - 10 hs/day and night). (see Tran Hoang Phuc Fisheries Review No-6/1997) A.
  • Molluscan Composition at Vellar Estuary, Portonovo Coast

    Molluscan Composition at Vellar Estuary, Portonovo Coast

    NOTE ZOOS' PRINT JOURNAL 22(1): 2546 From the study it was observed that almost all the gastropods and bivalves were abundant during premonsoon, postmonsoon MOLLUSCAN COMPOSITION AT VELLAR and summer months. The maximum numbers of Meretrix spp. and Katelysia opima were recorded during premonsoon and ESTUARY, PORTONOVO COAST postmonsoon because of favourable environmental conditions like nutrient rich coastal waters. Jayabal (1984) and Kalyanasundaram S. Arularasan 1 and R. Kasinathan 2 (1982) have suggested that Meretrix meretrix, M. casta and Katelysia opima were abundant during premonsoon and postmonsoon. 1,2 Centre of Advanced Study in Marine Biology, Annamalai Umbonium vestiarium were dominating near the mouth of the estuary University, Parangipettai, Tamil Nadu 608502, India during all seasons, except monsoon, because of the downfall of Email: 1 [email protected] salinity. Cerithidea (Cerithideopsilla) cingulata are abundant during premonsoon, postmonsoon and summer seasons at high water The seasonal variation of gastropods and bivalves in the mark, at the same time during monsoon, it is found minimum due Vellar estuary of Portonovo (11030'N-79049'E) coast was studied to heavy floods. The peak breeding occurs from May to August during July 2004 to June 2005. The study was carried out near the mouth of Vellar estuary and biological station which seasonally during premonsoon (July-September), monsoon have higher salinity, suitable habitat and soil texture which (October-December), postmonsoon (January-March) and summer influence the diverse population and also help in breeding. (April-June). During the course of the study, it was noticed that Kalyanasundaram (1982) reported that observation on the gonad the distribution of organisms showed marked differences in of bivalves revealed that they have extended spawning period relation to water level.
  • Blood Cockles Tegillarca Granosa Growth Performance

    Blood Cockles Tegillarca Granosa Growth Performance

    International Journal of Fisheries and Aquatic Studies 2020; 8(5): 269-276 E-ISSN: 2347-5129 P-ISSN: 2394-0506 (ICV-Poland) Impact Value: 5.62 Blood cockles Tegillarca granosa growth performance (GIF) Impact Factor: 0.549 IJFAS 2020; 8(5): 269-276 © 2020 IJFAS Mohd Lazim Mohd Saif, Abu Bakar Tumin, Fadzilah Yusof, Azmi Rani, www.fisheriesjournal.com Received: 22-06-2020 Azlina Apandi and Zainoddin Jamari Accepted: 07-08-2020 Abstract Mohd Lazim Mohd Saif Blood cockles Tegillarca granosa culture in natural habitat is one of the way to increase national Brackish Aquaculture Research production in addition to harvesting natural resources today, but culture in pond is rare to Malaysia. Division, FRI Gelang Patah, Many factors need to be considered before the study of blood cockles in the pond is to be carried out. The 81550 Johor, Malaysia presence of plankton as a food source is a key factor in obtaining optimal blood cockles growth. The Abu Bakar Tumin study was conducted in two ponds with different treatments. Pond one used commercial probiotic for Brackish Aquaculture Research water treatment and pond two was as a control. Fertilization was carried out weekly while water Division, FRI Gelang Patah, exchange was carried out monthly. Measurement of water quality and chlorophyll a content were 81550 Johor, Malaysia performed once a month. As a result of 12 month of culture, blood cockles from pond one average length was 22.85+1.80mm and for pond two average length was 25.36+3.00mm. Blood cockles length growth Fadzilah Yusof rate for pond one was 0.66mm/month while for pond two was 0.99mm/month.