Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-28T16:09:25.040Z Has data issue: false hasContentIssue false
  • English
  • Français

Moonsnail hatching success, development timing and early feeding behaviour at the high-latitude White Sea

Published online by Cambridge University Press:  24 November 2020

Dmitriy Aristov Open the ORCID record for Dmitriy Aristov [Opens in a new window] ,
Lyudmila Flachinskaya  and
Marina Varfolomeeva Open the ORCID record for Marina Varfolomeeva [Opens in a new window]
Dmitriy Aristov*
Affiliation:
Zoological Institute of the Russian Academy of Sciences, Universitetskaya emb., 1, St.-Petersburg, 199034, Russia
Lyudmila Flachinskaya
Affiliation:
Zoological Institute of the Russian Academy of Sciences, Universitetskaya emb., 1, St.-Petersburg, 199034, Russia
Marina Varfolomeeva
Affiliation:
Saint-Petersburg State University, Universitetskaya emb., 7/9, St.-Petersburg, 199034, Russia
*
Author for correspondence: Dmitriy Aristov, E-mail: amauropsis@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

As predators, Naticidae (Gastropoda) can shape marine soft-sediment communities. Thus understanding of the reproductive biology and development of moonsnails is of great importance. Most moonsnails lay large egg masses, known as sand or egg collars, which are freely distributed on sand or muddy sediments. Here we report upon the abundance of egg collars of two naticid species, Amauropsis islandica and Euspira pallida, from the high-latitude White Sea, as well as describe the morphology of egg collars and hatching success, with a brief description of juvenile feeding in A. islandica. While in the subtidal zone, the egg collars of E. pallida were 10 times more abundant than of A. islandica, the egg collars of the latter species were the only ones that occur in the intertidal zone. The morphology of an egg collar of E. pallida differed from the literature descriptions by having a plicated basal margin. The number of egg capsules inside the collars was twice as high in A. islandica compared with E. pallida, but they were smaller. Amauropsis islandica hatchlings were larger and hatching success was more than twice that in E. pallida. We suggest that these characteristics promote the high abundance of A. islandica populations observed on some tidal flats of the White Sea. Surprisingly, A. islandica juveniles could perform non-drilling feeding in the first month after hatching. This study fills the gap in the knowledge of naticid reproductive biology at high latitudes.

Keywords

Amauropsis islandicaegg collarsEuspira pallidanaticidswitch feeding modeWhite Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 7 , November 2020 , pp. 1071 - 1078
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

We dedicate this paper to the memory of our co-author, who unfortunately succumbed to Covid-19.

References

Ansell, AD (1961) Egg capsules of the dogfish (Scylliorhinus canicula, Linn.) bored by Natica (Gastropoda, Prosobranchia). Proceedings of the Malacological Society of London 34, 248–249.Google Scholar
Ansell, AD (1981) Experimental studies of a benthic predator-prey relationship. I. Feeding, growth, and egg-collar production in long-term cultures of the gastropod drill Polinices alderi (Forbes) feeding on the bivalve Tellina tenuis da Costa. Journal of Experimental Marine Biology and Ecology 56, 235–255.CrossRefGoogle Scholar
Ansell, AD (1982) Experimental studies of a benthic predator-prey relationship. II. Energetics of growth and reproduction, and food-conversion efficiencies, in long-term cultures of the gastropod drill Polinices alderi (Forbes) feeding on the bivalve Tellina tenuis da Costa. Journal of Experimental Marine Biology and Ecology 61, 1–29.CrossRefGoogle Scholar
Aristov, DА and Granovitch, АI (2011) The diet of predatory mollusk Amauropsis islandica (Müller, 1776) (Caenogastropoda: Naticidae) on the White Sea intertidal zone. Vestnik Sankt-Peterburgskogo Universiteta (Ser. 3) 4, 10–18. [In Russian]Google Scholar
Aristov, DA and Varfolomeeva, MA (2019) Moon snails Amauropsis islandica can shape the population of Baltic clams Limecola balthica by size-selective predation in the high-latitude White Sea. Polar Biology 42, 2227–2236.CrossRefGoogle Scholar
Aristov, D, Varfolomeeva, M and Puzachenko, G (2015) All's good in a famine? Hydrobia ulvae as a secondary prey for juveniles of Iceland moonsnails Amauropsis islandica at the White Sea sandflats. Journal of the Marine Biological Association of the United Kingdom 95, 1601–1606.CrossRefGoogle Scholar
Berg, CJ (1976) Ontogeny of predatory behaviour in marine snails (Prosobranchia: Naticidae). Nautilus 90, 1–4.Google Scholar
Bernard, FR (1967) Studies on the biology of the naticid clamdrill Polinices lewisi (Gould) (Gastropoda, Prosobranchiata). Fisheries Research Board of Canada, Technical Report 42, 1–41.Google Scholar
Carriker, MR (1981) Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20, 403–422.Google Scholar
Casey, MM, Fall, LM and Dietl, GP (2016) You are what you eat: stable isotopic evidence indicates that the naticid gastropod Neverita duplicata is an omnivore. Frontiers in Ecology and Evolution 4, 1–14.CrossRefGoogle Scholar
Clements, JC and Rawlings, TA (2014) Ontogenetic shifts in the predatory habits of the northern moonsnail (Lunatia heros) on the Northwestern Atlantic Coast. Journal of Shellfish Research 33, 755–768.CrossRefGoogle Scholar
Culver, SJ and Lipps, JH (2003) Predation on and by Foraminifera. In Kelley, PH, Kowalewski, M and Hansen, TA (eds), Predator–Prey Interactions in the Fossil Record. New York, NY: Kluwer Academic/Plenum Press, pp. 113–139.Google Scholar
Fretter, V and Graham, A (1994) British Prosobranch Molluscs: Their Functional Anatomy and Ecology. London: The Ray Society.Google Scholar
Giglioli, M (1955) The egg masses of the Naticidae (Gastropoda). Journal of the Fisheries Research Board of Canada 12, 287–327.CrossRefGoogle Scholar
Golikov, AN (1987) Class Gastropoda. In Starobogatov, YaI and Naumov, AD (eds), Molluscs of the White Sea. Leningrad: Nauka, pp. 41–204. [In Russian]Google Scholar
Golikov, AN and Kusakin, OG (1978) Shell-bearing gastropods of the intertidal zone of the seas of the USSR. Opredelitely po faune SSSR 116, 1–292. [In Russian]Google Scholar
Huelsken, T (2011) First evidence of drilling predation by Conuber sordidus (Swainson, 1821) Gastropoda: Naticidae) on soldier crabs (Crustacea: Mictyridae). Molluscan Research 31, 125–132.Google Scholar
Huelsken, T, Marek, C, Schreiber, S, Schmidt, I and Hollmann, M (2008) The Naticidae (Mollusca: Gastropoda) of Giglio island (Tuscany, Italy): shell characters, live animals, and a molecular analysis of egg masses. Zootaxa 1770, 1–40.CrossRefGoogle Scholar
Jensen, AS (1951) Do the Naticidae drill by mechanical or by chemical means? Nature 167, 901–902.CrossRefGoogle Scholar
Kabat, AR (1990) Predatory ecology of naticid gastropods with a review of shell boring predation. Malacologia 32, 155–193.Google Scholar
Kang, D-R, Tan, KS and Liu, L-L (2018) Egg-collar morphology and identity of nine species of Naticidae (Gastropoda) in Taiwan, with an assessment of their phylogenetic relationships. Journal of Molluscan Studies 84, 354–378.Google Scholar
Kingsley-Smith, PR, Richardson, CA and Seed, R (2003) Size-related and seasonal patterns of egg collar production in Polinices pulchellus (Gastropoda: Naticidae) Risso 1826. Journal of Experimental Marine Biology and Ecology 295, 191–206.CrossRefGoogle Scholar
Korsun, S, Hald, M, Golikova, E, Yudina, A, Kuznetsov, I, Mikhailov, D and Knyazeva, O (2014) Intertidal foraminiferal fauna and the distribution of Elphidiidae at Chupa inlet, western White Sea. Marine Biology Research 10, 153–166.CrossRefGoogle Scholar
Kulikova, VA, Kolbin, KG and Kolotukhina, NK (2007) Reproduction and larval development of the prosobranch mollusk Cryptonatica janthostoma (Gastropoda: Naticidae). Russian Journal of Marine Biology 33, 374–378. [In Russian]CrossRefGoogle Scholar
Kuznetsov, VV (1960) The White Sea and Biological Peculiarities of its Flora and Fauna. Moscow: Nauka. [In Russian]Google Scholar
Leonov, A, Filatov, N, Zdorovennov, R and Zdorovennova, G (2004) Functioning of the White Sea ecosystem: studying the transformations of organogenic substances using a mathematical model. Water Resources 31, 511–530.CrossRefGoogle Scholar
Moffat, J (1975). Fecal Pellet Production by Macoma balthica and Pellet Transport in Cobequid Bay, Nova Scotia (Bachelor's thesis). McMaster University, Ontario, Canada.Google Scholar
Montiel, Y, Chaparro, O and Segura, C (2005) Changes in feeding mechanisms during early ontogeny in juveniles of Crepidula fecunda (Gastropoda, Calyptraeidae). Marine Biology 147, 1333–1342.CrossRefGoogle Scholar
Murray, FV (1969) A brief account of the spawn of Conuber incei (Philippi, 1853) (Gastropoda: Naticidae). Journal of the Malacological Society of Australia 1, 49–52.CrossRefGoogle Scholar
Naumov, A (2013) Long-term fluctuations of soft-bottom intertidal community structure affected by ice cover at two small sea bights in the Chupa inlet (Kandalaksha bay) of the White sea. Hydrobiologia 706, 159–173.CrossRefGoogle Scholar
Page, LR and Pedersen, RVK (1998) Transformation of phytoplanktivorous larvae into predatory carnivores during the development of Polinices lewisii (Mollusca, Caenogastropoda). Invertebrate Biology 117, 208–220.CrossRefGoogle Scholar
Paine, RT (1963) Trophic relationships of 8 sympatric predatory gastropods. Ecology 44, 63–73.CrossRefGoogle Scholar
Pastorino, G, Averbuj, A and Penchaszadeh, PE (2009) On the egg masses, eggs and embryos of Notocochlis isabelleana (d'Orbigny, 1840) (Gastropoda: Naticidae) from Northern Patagonia. Malacologia 51, 395–402.CrossRefGoogle Scholar
Pedersen, R and Page, L (2000) Development and metamorphosis of the planktotrophic larvae of the moon snail, Polinices lewisii (Gould, 1847) (Caenogastropoda: Naticoidea). Veliger 43, 58–63.Google Scholar
Perry, LM (1940) Marine shells of the southwest coast of Florida. Bulletin of American Paleontology 26, 1–260.Google Scholar
Przeslawski, R (2004) A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Research 24, 43–63.CrossRefGoogle Scholar
Riisgård, HU, Egede, PP and Barreiro Saavedra, I (2011) Feeding behaviour of the mussel, Mytilus edulis: new observations, with a minireview of current knowledge. Journal of Marine Biology. https://doi.org/10.1155/2011/312459CrossRefGoogle Scholar
Rossignol, L, Dupuy, C, Pascal, P and Debenay, JP (2007). Hydrobia ulvae: a deposit-feeder for cleaning living hard-shelled foraminifera. Journal of Foraminiferal Research 37(1), 8–11.CrossRefGoogle Scholar
Saidova, K and Beklemishev, KV (1963) On finding foraminifers drilled by gastropod fry in the marine sediments. Doklady Academii Nauk SSSR 92, 1061–1063. [In Russian]Google Scholar
Sato, SI, Chiba, T and Hasegawa, H (2012) Long-term fluctuations in mollusk populations before and after the appearance of the alien predator Euspira fortunei on the Tona coast, Miyagi Prefecture, northern Japan. Fisheries Science 78(3), 589–595.CrossRefGoogle Scholar
Thorson, GAW (1935) Studies of the egg capsules and development of Arctic marine prosobranchs. Meddelelser om Grønland 100, 1–71.Google Scholar
Thorson, GAW (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larva in the Sound, Øresund. Meddelelser fra Kommissionen for Danmarks Fisken -og Havundersøgelser, serie: Plankton 4, 1–523.Google Scholar
Tomiyama, T (2013) Timing and frequency of egg-collar production of the moonsnail Euspira fortunei. Fisheries Science 79, 905–910.CrossRefGoogle Scholar
Underwood, AJ (1980) The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46, 201–213.CrossRefGoogle ScholarPubMed
Underwood, AJ and Keough, MJ (2001) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In Bertness, MD, Gaines, SD and Hay, ME (eds), Marine Community Ecology. Sunderland, MA: Sinauer Associates, pp. 183–200.Google Scholar
Valentine, JW, Roy, K and Jablonski, D (2002) Carnivore/non carnivore ratios in northeastern Pacific marine gastropods. Marine Ecology Progress Series 22, 153–163.CrossRefGoogle Scholar
Visaggi, CC, Dietl, GP and Kelley, PH (2013) Testing the influence of sediment depth on drilling behaviour of Neverita duplicata (Gastropoda: Naticidae), with a review of alternative modes of predation by naticids. Journal of Molluscan Studies 79(4), 310–322.CrossRefGoogle Scholar
Wessel, P and Smith, WHF (1996) A global, self-consistent, hierarchical, high-resolution shoreline database. Journal of Geophysical Research 101(B4), 8741–8743.CrossRefGoogle Scholar
Yakovlev, YuM and Kolotukhina, NK (1996) Reproduction of gastropod mollusks Cryptonatica janthostoma (Deshayes, 1841) and Lunatia pila (Pilsbry, 1911) (Gastropoda, Naticidae) in the Sea of Japan. Bulletin of the Russian Far East Malacological Society 1, 61–68. [In Russian]Google Scholar
Yoshida, K, Sato, T, Narita, K and Tomiyama, T (2017) Abundance and body size of the moonsnail Laguncula pulchella in the Misuji river estuary, Seto Inland Sea, Japan: comparison with a population in northern Japan. Plankton and Benthos Research 12, 53–60.CrossRefGoogle Scholar
Ziegelmeier, E (1961) Zur fortpflanzungsbiologie der Naticiden (Gastropoda Prosobranchia). Helgoländer Wissenschaftliche Meeresuntersuchungen 8, 94–118.CrossRefGoogle Scholar
Supplementary material: PDF

Aristov et al. supplementary material

Aristov et al. supplementary material

Download Aristov et al. supplementary material(PDF)
PDF 72.4 KB