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Caveat observator: the many faces of pre-spawning atresia in marine bivalve reproductive cycles

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Abstract

Of the hundreds of publications on bivalve reproductive cycles, only a handful reports the presence of pre-spawning oocyte autolysis, or atresia. This is at variance with the author’s practical experience, in which pre-spawning oocyte atresia has been found in every bivalve reproductive cycle investigated. Failure to identify pre-spawning atresia will lead to over-estimations of fecundity, reproductive effort, and anticipated larval density and recruitment. On the intuition that the phenomenon is under-reported due to unfamiliarity with the histological characteristics of atresia, it is presented here within the context of the study of bivalve reproductive cycles, the reported incidence of pre-spawning atresia, and the histological profiles of this phenomenon in several commercially important bivalve families. Despite superficial variability, the assembled data allow the presentation of underlying common characteristics. It is postulated that pre-spawning oocyte atresia is a widespread, yet seldom-identified phenomenon in marine bivalves, which probably affects previous and current data on fecundity and reproductive effort, both in wild and cultured populations. The information presented here is intended to both increase awareness of this process, and lead to more realistic interpretations of bivalve reproductive cycles, fecundity, and reproductive effort.

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Fig. 1

Re-interpreted from Suárez et al. (2005)

Fig. 2

From Camacho-Mondragón et al. (2015a, b)

Fig. 3
Fig. 4

From Dutertre et al. (2009), re-interpreted and re-labelled

Fig. 5

From Saucedo et al. (2001), re-interpreted and re-labelled

Fig. 6

Similar content being viewed by others

References

  • Albertini C (1985) Recherches cytologiques et expérimentales sur l’ovogénèse chez la moule (Mytilus edulis L., Mollusque Bivalve). Thèse de 3e cycle, Université de Caen, Caen, France. 117 pp

  • Andersen S, Christophersen G, Magnesen T (2011) Spat production of the great scallop (Pecten maximus): a roller coaster. A review. Can J Zool 89:579–598

    Article  Google Scholar 

  • Andrews JD (1979) Pelecypoda: Ostreidae. In: Giese AC, Pearce JS (eds) Reproduction of marine invertebrates, vol V. Molluscs: Pelecypods and lesser classes. Academic Press, New York, pp 293–341

    Chapter  Google Scholar 

  • Aranda DA, Díaz ME, Reynoso FL, Brulé T, Montero J, Cárdenas EB (2014) Reproductive strategies of the eastern oyster Crassostrea virginica (Gmelin 1791) in tropical lagoons of the Mexican Gulf of Mexico. J Shellfish Res 33:145–152

    Article  Google Scholar 

  • Avendaño M, Le Pennec M (1997) Intraspecific variation in gametogenesis in two populations of the Chilean molluscan bivalve, Argopecten purpuratus (Lamarck). Aquacult Res 28:175–182

    Article  Google Scholar 

  • Baba K, Tada M, Kawajiri T, Kuwahara Y (1999) Effects of temperature and salinity on spawning of the brackish water bivalve Corbicula japonica in Lake Abashiri, Hokkaido, Japan. Mar Ecol Prog Ser 180:213–221

    Article  Google Scholar 

  • Barber BJ, Blake NJ (2016) Reproductive physiology. In: Shumway SE, Parsons GJ (eds) Scallops: biology, ecology, aquaculture, and fisheries, 3rd edn. Elsevier, Amsterdam, pp 253–299

    Chapter  Google Scholar 

  • Bayne BL, Holland DL, Moore NM, Lowe DM, Widdows J (1978) Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J Mar Biol Ass UK 58:825–841

    Article  Google Scholar 

  • Bayne BL, Salkeld PN, Worrall CM (1983) Reproductive effort and value in different populations of the marine mussel, Mytilus edulis L. Oecologia 59:18–26

    Article  CAS  Google Scholar 

  • Beesley A, Lowe DM, Pascoe CK, Widdicombe S (2008) Effects of CO2-induced seawater acidification on the health of Mytilus edulis. Clim Res 37:215–225

    Article  Google Scholar 

  • Beninger PG (1984) Seasonal variations of the major lipid classes in relation to the reproductive activity of two species of clams raised in a common habitat: Tapes decussatus L. (Jeffreys, 1863) and Tapes philippinarum (Adams and Reeve, 1850). J Exp Mar Biol Ecol 79:79–90

    Article  CAS  Google Scholar 

  • Beninger PG (1987) A qualitative and quantitative study of the reproductive cycle of the giant scallop Placopecten magellanicus in the Bay of Fundy (New Brunswick, Canada). Can J Zool 65:495–498

    Article  Google Scholar 

  • Beninger PG, Le Pennec M (2016) Structure and function in scallops. In: Shumway SE, Parsons GJ (eds) Scallops: their biology, ecology, aquaculture, and fisheries, 3rd edn. Elsevier, Amsterdam, pp 85–159

    Chapter  Google Scholar 

  • Beninger PG, Lucas A (1984) Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussatus L. (Jeffreys) and Tapes philippinarum (Adams and Reeve). J Exp Mar Biol Ecol 79:19–38

    Article  CAS  Google Scholar 

  • Beninger PG, Cannuel R, Blin J-L, Pien S, Richard O (2001) Reproductive characteristics of the archaeogastropod Megathura crenulata. J Shellfish Res 20:301–307

    Google Scholar 

  • Beninger PG, Valdizan A, Decottignies P, Cognie B (2010a) Field reproductive dynamics of the invasive slipper limpet, Crepidula fornicata. J Exp Mar Biol Ecol 390:179–187

    Article  Google Scholar 

  • Beninger PG, Valdizan A, Decottignies P, Cognie B (2010b) Corrigendum to ‘Field reproductive dynamics of the invasive slipper limpet, Crepidula fornicata’ [J. Exp. Mar. Biol. Ecol. 390: 179–187]. J Exp Mar Biol Ecol 393:193–194

    Article  Google Scholar 

  • Briarty LG (1975) Stereology: methods for quantitative light and electron microscopy. Sci Progr 62:1–32

    CAS  Google Scholar 

  • Cáceres-Puig JI, Cáceres-Martínez C, Saucedo PE (2009) Annual reproductive effort of Pacific winged pearl oyster Pteria sterna and its relation with the timing for planning pearl seeding operations. J Shellfish Res 28:471–476

    Article  Google Scholar 

  • Camacho-Mondragón MA, Arellano-Martínez M, Ceballos-Vázquez BP (2012) Particular features of gonadal maturation and size at first maturity in Atrina maura (Bivalvia: Pinnidae). Sci Mar 76:539–548

    Article  Google Scholar 

  • Camacho-Mondragón MA, Ceballos-Vázquez BP, Uría-Galicia E, López-Villegas EO, Pipe R, Arellano-Martínez M (2015a) Ultrastructural and histological study of oogenesis and oocyte degeneration in the penshell Atrina maura (Bivalvia: Pinnidae). Malacologia 59:1–12

    Article  Google Scholar 

  • Camacho-Mondragón MA, Ceballos-Vázquez BP, Uría-Galicia E, López-Villegas EO, Pipe R, Arellano-Martínez M (2015b) Ultrastructural and histological study of oogenesis and oocyte degeneration in the penshell Atrina maura (Bivalvia: Pinnidae). Malacologia 59:1–12

    Article  Google Scholar 

  • Cantillanez M, Avendano M, Thouzeau G, Le Pennec M (2005a) Reproductive cycle of Argopecten purpuratus (Bivalvia: Pectinidae) in La Rinconada marine reserve (Antofagasta, Chile): response to environmental effects of El Nino and La Nina. Aquaculture 246:181–195

    Article  Google Scholar 

  • Cantillanez M, Avendaño M, Thouzeau G, Le Pennec M (2005b) Reproductive cycle of Argopecten purpuratus (Bivalvia: Pectinidae) in La Rinconada marine reserve (Antofagasta, Chile): response to environmental effects of El Niño and La Niña. Aquaculture 246:181–195

    Article  Google Scholar 

  • Casas SM, Villalba A (2012) Study of perkinsosis in the grooved carpet shell clam Ruditapes decussatus in Galicia (NW Spain). III. The effects of Perkinsus olseni infection on clam reproduction. Aquaculture 356–357:40–47

    Article  Google Scholar 

  • Castagna M (2001) Aquaculture of the hard clam, Mercenaria mercenaria. In: Castagna M, Kraueter J (eds) Biology of the hard clam. Elsevier, Amsterdam, pp 675–693

    Chapter  Google Scholar 

  • Castaños C, Pascual M, Camacho AP (2009) Reproductive biology of the nonnative oyster, Crassostrea gigas (Thunberg, 1793), as a key factor for its successful spread along the rocky shores of Northern Patagonia, Argentina. J Shellfish Res 28:837–847

    Article  Google Scholar 

  • Chávez-Villalba J, Barret J, Mingant C, Cochard J-C, Le Pennec M (2002a) Autumn conditioning of the oyster Crassostrea gigas: a new approach. Aquaculture 210:171–186

    Article  Google Scholar 

  • Chávez-Villalba J, Pommier J, Andriamiseza J, Pouvreau S, Barret J, Cochard JC, Le Pennec M (2002b) Broodstock conditioning of the oyster Crassostrea gigas: origin and temperature effect. Aquaculture 214:115–130

    Article  Google Scholar 

  • Chávez-Villalba J, Cochard JC, Le Pennec M, Barret J, Enríquez-Díaz M, Cáceres-Martínez C (2003) Effects of temperature and feeding regimes on gametogenesis and larval production in the oyster Crassostrea gigas. J Shellfish Res 22:721–731

    Google Scholar 

  • Chávez-Villalba J, Villelas-Ávila F, Cáceres-Martínez C (2007) Reproduction, condition, and mortality of the Pacific oyster Crassostrea gigas (Thunberg) in Sonora, México. Aquac Res 38:268–278

    Article  Google Scholar 

  • Chipperfield P (1953) Observations on the breeding and settlement of Mytilus edulis L. in British waters. J Mar Biol Ass UK 32:449–476

    Article  Google Scholar 

  • Christiansen HR, Olivier SR (1971) Sobre el hermaproditismo de Chlamys tehuelcha D’orb. 1846. (Pelecypoda, Filibranchia, Pectinidae). An Soc Cient Argent 3:115–127

    Google Scholar 

  • De Gaulejac B, Henry H, Vicente N (1995) An ultrastructural study of gametogenesis of the marine bivalve Pinna nobilis (Linnaeus 1758). I. Oogenesis. J Moll Stud 61:375–392

    Article  Google Scholar 

  • Dorange G, Le Pennec M (1989) Ultrastructural study of oogenesis and oocytic degeneration in Pecten maximus from the Bay of St. Brieuc Mar Biol 103:339–348

    Article  Google Scholar 

  • Duprat-Bertazzi G, García-Domínguez F (2005) Reproductive cycle of the rock oyster Hyotissa hyotis (Linné, 1758) (Griphaeidae) at the La Ballena island, Gulf of California, México. J Shellfish Res 24:987–993

    Article  Google Scholar 

  • Dutertre M, Beninger PG, Barillé L, Papin M, Rosa P, Barillé AL, Haure J (2009) Temperature and seston quantity and quality effects on field reproduction of farmed oysters, Crassostrea gigas, in Bourgneuf Bay, France. Aquat Liv Res 22:319–329

    Article  Google Scholar 

  • Dutertre M, Beninger PG, Barillé L, Papin M, Haure J (2010) Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast. Mar Environ Res 69:1–9

    Article  CAS  Google Scholar 

  • Elias H, Hennig A, Schwartz DE (1971) Stereology: applications to biomedical research. Physiol Rev 51:158–200

    CAS  Google Scholar 

  • Fearman JA, Bolch CJS, Oltschaniwskyj NA (2009) Energy storage and reproduction in mussels, Mytilus galloprovincialis: the influence of diet quality. J Shellfish Res 28:305–312

    Article  Google Scholar 

  • Gómez-Robles E, Saucedo PE (2009) Evaluation of quality indices of the gonad and somatic tissues involved in reproduction of the pearl oyster Pinctada mazatlanica with histochemistry and digital image analysis. J Shellfish Res 28:329–335

    Article  Google Scholar 

  • González-Araya R, Quillien V, Robert R (2013) The effects of eight single microalgal diets on sex-ratio and gonad development throughout European flat oyster (Ostrea edulis L.) conditioning. Aquaculture 400:1–5

    Article  Google Scholar 

  • Gosling E (2015) Reproduction, settlement and recruitment. In: Marine Bivalve Molluscs. Fishing News Books, Oxford pp 157-202

  • Hardardotti K, Kjesbu OS, Marteinsdottir G (2001) Relationship between atresia, fish size and condition in Icelandic cod (Gadus morhua L.). ICES/CIEM working paper 2001/J: 19: 1–18

  • Heffernan PB, Walker RL (1989) Quantitative image analysis methods for use in histological studies of bivalve reproduction. J Moll Stud 55:135–137

    Article  Google Scholar 

  • Hsueh AJW, Billig H, Tsafriri A (1995) Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 15:707–724

    Google Scholar 

  • Jennings S, Kaiser MJ, Reynolds JD (2001) Marine fisheries ecology. Blackwell Publishing, Malden, pp 39–69

    Google Scholar 

  • Kaipia A, Hsueh AJW (1997) Regulation of ovarian follicle atresia. Ann Rev Physiol 59:349–363

    Article  CAS  Google Scholar 

  • Kennedy VS, van Huekelem LE (1985) Gametogenesis and larval production in a population of the introduced Asiatic clam, Corbicula sp. (Bivalvia: Corbiculidae) in Maryland. Biol Bull 168:50–60

    Article  Google Scholar 

  • Krakauer DC, Mira A (1999) Mitochondria and germ-cell death. Nature 400:125–126

    Article  CAS  Google Scholar 

  • Lango-Reynoso F, Chávez-Villalba J, Cochard JC, Le Pennec M (2000) Oocyte size, a means to evaluate the gametogenic development of the Pacific oyster, Crassostrea gigas (Thunberg). Aquaculture 190:183–199

    Article  Google Scholar 

  • Le Pennec M, Beninger PG, Dorange G, Paulet YM (1991) Trophic sources and pathways to the developing gametes of Pecten maximus (Bivalvia: Pectinidae). J Mar Biol Ass UK 71:451–463

    Article  Google Scholar 

  • Linares-Casenave J, Van Eenennaam JP, Doroshov SI (2002) Ultrastructural and histological observations on temperature-induced follicular ovarian atresia in the white sturgeon. J Appl Ichthyol 18:382–390

    Article  Google Scholar 

  • Lowe DM (1988) Alterations in cellular structure of Mytilus edulis resulting from exposure to environmental contaminants under field and experimental conditions. Mar Ecol Prog Ser 46:91–100

    Article  CAS  Google Scholar 

  • Lowe DM, Pipe RK (1985) Cellular responses in the mussel Mytilus edulis following exposure to diesel oil emulsions: reproductive and nutrient storage cells. Mar Envir Res 17:234–237

    Article  CAS  Google Scholar 

  • Lowe DM, Pipe RK (1986) Hydrocarbon exposure in mussels: a quantitative study of the responses in the reproductive and nutrient storage cell systems. Aquat Toxicol 8:265–272

    Article  CAS  Google Scholar 

  • Lowe DM, Pipe RK (1987) Mortality and quantitative aspects of storage cell utilization in mussels, Mytilus edulis following exposure to diesel oil hydrocarbons. Mar Envir Res 22:243–251

    Article  CAS  Google Scholar 

  • Lowe DM, Moore DL, Bayne BL (1982) Aspects of gametogenesis in the marine mussel Mytilus edulis L. J Mar Biol Ass UK 62:133–145

    Article  Google Scholar 

  • Lubet P (1959) Recherches sur le cycle sexuel et l’émission des gamètes chez les Mytilidés et les Pectinidés (Mollusques bivalves). Rev Trav Inst Pêches Marit 23:387–548

    Google Scholar 

  • Lubet P, Albertini L, Robbins I (1986) Recherches expérimentales au cours des cycles annuels sur l’action gonadotrope exercée par les ganglions cérébroïdes sur la gamétogenèse femelle chez la moule Mytilus edulis L. (mollusque bivalve). C R Acad Sci Paris Ser III 303:575–580

    CAS  Google Scholar 

  • Lucas A (1965) Recherche sur la sexualité des Mollusques bivalves. Bull Biol Fr Belg 99:115–247

    Google Scholar 

  • Lucas A (1982) Evaluation of reproductive effort in bivalve molluscs. Malacologia 22:183–187

    Google Scholar 

  • MacDonald BA, Thompson RJ (1986) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus. III. Physiological ecology, the gametogenic cycle and scope for growth. Mar Biol 93:37–48

    Article  Google Scholar 

  • Mackie GL (1984) Bivalves. In: Tompa AS, Verdonk NH, Van den Biggelaar JAM (eds) The Mollusca, vol 7. Reproduction. Academic Press, Orlando, pp 351–418

    Google Scholar 

  • Marroquin-Mora DC, Rice MA (2008) Gonadal cycle of northern quahogs, Mercenaria mercenaria (Linne, 1758), from fished and non-fished subpopulations in Narragansett Bay. J Shellfish Res 27:643–652

    Article  Google Scholar 

  • Martı́nez G, Pérez H (2003) Effect of different temperature regimes on reproductive conditioning in the scallop Argopecten purpuratus. Aquaculture 228:153–167

    Article  Google Scholar 

  • Martı́nez G, Aguilera C, Mettifogo L (2000) Interactive effects of diet and temperature on reproductive conditioning of Argopecten purpuratus broodstock. Aquaculture 183:149–159

    Article  Google Scholar 

  • Mayhew TM (2000) 3D structure from thin sections: applications of stereology. Eur Micro Anal 11:17–20

    Google Scholar 

  • Miranda ACL, Bazzolia N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tiss Cell 31:480–488

    Article  CAS  Google Scholar 

  • Morales-Alamo R, Mann R (1989) Anatomical features in histological sections of Crassostrea virginica (Gmelin 1791) as an aid in measurements of gonad area for reproductive assessment. J Shellfish Res 8:71–82

    Google Scholar 

  • Motavkine PA, Varaksine AA (1983) Histophysiologie du système nerveux et régulation de la reproduction chez les Mollusques Bivalves. Translated from the Russian by C. Bellon-Humbert, Editions INFREMER 10, Paris, 208p

  • Newell RIE, Bayne BL (1980) Seasonal changes in the physiology, reproductive condition, and carbohydrate content of the cockle Cardium (=Cerastoderma) edule (Bivalvia: Cardiidae). Mar Biol 56:11–19

    Article  CAS  Google Scholar 

  • Newell RIE, Hilbish TJ, Koehn RK, Newell CJ (1982) Temporal variation in the reproductive cycle of Mytilus edulis L. (Bivalvia, Mytilidae) from localities on the east coast of the United States. Biol Bull 162:299–310

    Article  Google Scholar 

  • Ortiz-Zarragoitia M, Cajaville MP (2010) Intersex and oocyte atresia in a mussel population from the Biosphere’s Reserve of Urdaibai (Bay of Biscay). Ecotoxicol Environ Safety 73:693–701

    Article  CAS  Google Scholar 

  • Ozanai K (1975) Seasonal gonad development and sex alteration in the scallop, Patinopecten yessoensis. Bull Mar Biol Stn Asamushi 15:81–88

    Google Scholar 

  • Paulet YM, Dorange G, Cochard JC, Le Pennec M (1992) Reproduction et recrutement chez Pecten maximus (L.). Ann Instit Océanogr Paris 68:45–64

    Google Scholar 

  • Pazos AJ, Román G, Acosta CP, Abad M, Sánchez JL (1996) Stereological studies on the gametogenic cycle of the scallop, Pecten maximus, in suspended culture in Ria de Arousa (Galicia, NW Spain). Aquaculture 142:119–135

    Article  Google Scholar 

  • Pipe RK (1985) Seasonal cycles in and effects of starvation on egg development in Mytilus edulis. Mar Ecol Prog Ser 24:121–128

    Article  Google Scholar 

  • Pipe RK (1987) Oogenesis in the marine mussel Mytilus edulis: an ultrastructural study. Mar Biol 95:405–414

    Article  Google Scholar 

  • Reddiath K (1962) The sexuality and spawning of Manx pectinids. J Mar Biol Ass UK 42:683–703

    Article  Google Scholar 

  • Rideout RM, Burton MPM, Rose GA (2000) Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland. J Fish Biol 57:1429–1440

    Article  Google Scholar 

  • Rodríguez-Jaramillo C, Hurtado MA, Vivas E, Ramírez JL, Manzano M, Palacios E (2008) Gonadal development and histochemistry of the tropical oyster, Crassostrea corteziensis (Hertlein, 1951) during an annual reproductive cycle. J Shellfish Res 27:1–13

    Article  Google Scholar 

  • Rogan E, Culloty SC, Cross TF et al (1991) The detection of Bonamia ostreae (Pichot,1980) in frozen oysters (Ostrea edulis L.) and the effect of the parasite on condition. Aquaculture 97:311–315

    Article  Google Scholar 

  • Sastry AN (1979) Pelecypoda (excluding Ostreidae). In: Giese AC, Pearce JS (eds) Reproduction of marine invertebrates, vol V. Molluscs. Academic Press, New York, pp 113–292

    Chapter  Google Scholar 

  • Sause BL, Gwyther D, Burgess D (1987) Larval settlement, juvenile growth and the potential use of spatfall indices to predict recruitment of the scallop Pecten alba Tate in Port Phillip Bay, Victoria, Australia. Fish Res 6:81–92

    Article  Google Scholar 

  • Saucedo P, Rodrıguez-Jaramillo C, Aldana-Aviles C, Monsalvo-Spencer P, Reynoso-Granados T, Villarreal H, Monteforte M (2001) Gonadic conditioning of the calafia mother-of-pearl oyster, Pinctada mazatlanica (Hanley, 1856), under two temperature regimes. Aquaculture 195:103–119

    Article  Google Scholar 

  • Sawusdee A, Jensen AC, Collins KJ, Hauton C (2015) Improvements in the physiological performance of European flat oysters Ostrea edulis (Linnaeus, 1758) cultured on elevated reef structures: implications for oyster restoration. Aquaculture 444:41–48

    Article  Google Scholar 

  • Seed R (1976) Ecology. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge University Press, Cambridge, pp 13–66

    Google Scholar 

  • Skjæraasen JE, Korsbrekke K, Kjesbu OS, Fonn M, Nilsen T, Nash RDM (2013) Size-, energy- and stage-dependent fecundity and the occurrence of atresia in the Northeast Arctic haddock Melanogrammus aeglefinus. Fish Res 138:120–127

    Article  Google Scholar 

  • Slater J (2005) Spawning of King Scallops, Pecten maximus (L.) in Mulroy Bay and the relationship with spatfall intensity. J Shellfish Res 24:951–958

    Article  Google Scholar 

  • Steele S, Mulcahy MF (1999) Gametogenesis of the oyster Crassostrea gigas in southern Ireland. J Mar Biol Assoc UK 70:673–686

    Article  Google Scholar 

  • Suárez MP, Alvarez C, Molist P, San Juan F (2005) Particular aspects of gonadal cycle and seasonal distribution of gametogenic stages of Mytilus galloprovincialis cultured in the estuary of Vigo. J Shellfish Res 24:531–540

    Article  Google Scholar 

  • Sundet JH, Lee JB (1984) Seasonal variation in gamete development in the Iceland scallop, Chlamys islandica. J Mar Biol Ass UK 64:411–416

    Article  Google Scholar 

  • Tang SF (1941) The breeding of the scallop (Pecten maximus L.) with a note on the growth rate. Proc Liverpool Biol Soc 54:9–28

    Google Scholar 

  • Thompson RJ (1984) Production, reproductive effort, reproductive value and reproductive cost in a population of the blue mussel Mytilus edulis from a subarctic environment. Mar Ecol Prog Ser 16:249–257

    Article  Google Scholar 

  • Thompson KJ, Inglis SD, Stokesbury KDE (2014) Identifying spawning events of the sea scallop Placopecten magellanicus on Georges Bank. J Shellfish Res 33:77–87

    Article  Google Scholar 

  • Valdizan A, Beninger PG, Decottignies P, Chantrel M, Cognie B (2011) Evidence that rising coastal seawater temperatures increase reproductive output of the invasive gastropod Crepidula fornicata. Mar Ecol Prog Ser 438:153–165

    Article  Google Scholar 

  • Vaschenko MA, Syasina IG, Zhadan PM, Medvedeva LA (1997) Reproductive function state of the scallop Mizuhopecten yessoensis Jay from polluted areas of Peter the Great Bay, Sea of Japan. Hydrobiologia 352:231–240

    Article  Google Scholar 

  • Vaschenko MA, Hsieh HL, Radashevsky VI (2013) Gonadal state of the oyster Crassostrea angulata cultivated in Taiwan. J Shellfish Res 32:471–482

    Article  Google Scholar 

  • Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30:23–38

    Article  CAS  Google Scholar 

  • Wiborg KF (1963) Some observations on the Iceland scallop, Chlamys icelandica (Müller) in Norwegian waters. Rep Norw Fish Mar Invest 13:38–53

    Google Scholar 

  • Yurimoto T, Mori Y, Ito S, Maeno Y (2008) Reproductive cycle of the subcrenated ark shell Scapharca kagoshimensis (Tokunaga, 1906) in Ariake Bay, Japan. J Shellfish Res 27:1101–1108

    Article  Google Scholar 

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Acknowledgements

I thank D. Cherel for her able assistance with the Tapes philippinarum histology and photomicrography, and for helpful discussions concerning this species. The manuscript was greatly strengthened by the comments of M.A. Vaschenko. This work was financed by the EPAT program of the Conseil Régional des Pays de la Loire, contract 2015 02488.

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Beninger, P.G. Caveat observator: the many faces of pre-spawning atresia in marine bivalve reproductive cycles. Mar Biol 164, 163 (2017). https://doi.org/10.1007/s00227-017-3194-x

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