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Life cycle and early development of the thecosomatous pteropod Limacina retroversa in the Gulf of Maine, including the effect of elevated CO2 levels

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Abstract

Thecosomatous pteropods are pelagic molluscs with aragonitic shells. They are considered to be especially vulnerable among plankton to ocean acidification, but to recognize changes due to anthropogenic forcing a baseline understanding of their life history is needed. In the present study, adult Limacina retroversa were collected on five cruises from multiple sites in the Gulf of Maine (between 42°22.1′–42°0.0′N and 69°42.6′–70°15.4′W; water depths of ca. 45–260 m) from October 2013 to November 2014. They were maintained in the laboratory under continuous light at 8 °C. There was evidence of year-round reproduction and an individual life span in the laboratory of 6 months. Eggs laid in captivity were observed throughout development. Hatching occurred after 3 d, the veliger stage was reached after 6–7 d, and metamorphosis to the juvenile stage was after ~1 month. Reproductive individuals were first observed after 3 months. Calcein staining of embryos revealed calcium storage beginning in the late gastrula stage. Staining was observed in the shell gland, shell field, mantle and shell margin in later stages. Exposure of two batches of larvae at the gastrula stage to elevated CO2 levels (800 and 1200 ppm) resulted in significantly increased mortality in comparison with individuals raised under ambient (~400 ppm) conditions and a developmental delay in the 1200 ppm treatment compared with the ambient and 800 ppm treatments.

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Acknowledgments

We would like to thank R. Galat, D. McCorkle, M. White and C. Zakroff for assisting in the setup of the culturing and CO2 exposure facilities. We greatly appreciate the insight of D. McCorkle and the collaboration of Z.A. Wang and K. Hoering on the carbonate chemistry measurements. We much appreciate the hard work and dedication of Captain K. Houtler and Mate I. Hanley and would like to thank them for excellent support aboard the R/V Tioga. At sea, sampling was supported by P. Alatalo, A. Bergan, L. Blanco Bercial, S. Chu, N. Copley, T. Crockford, S. Crosby, M. Edenius, K. Hoering, R. Levine, M. Lowe, C. Pagniello, A. Schlunk, Z.A. Wang, T. White and P. Wiebe. A special thanks is owed to P. Alatalo, for critical assistance in maintaining long-term cultures of pteropods and phytoplankton, providing insight and advice, and for consistent hard work during experiments. L. Kerr provided expertise with SEM and confocal microscopy at the Marine Biological Laboratory Central Microscopy Facility. We are grateful for advice from S. Gallager whose experience with pteropod rearing and visualization were profoundly helpful. A. Thabet is grateful for a fellowship from the Egyptian Culture and Education Bureau and for mentoring from Drs. S.A. Saber, M.M. Sarhan and M.M. Fouda. Funding for this research was provided by a National Science Foundation grant to Lawson, Maas, and Tarrant (OCE-1316040). Additional support for field sampling was provided by the WHOI Coastal Ocean Institute and Pickman Foundation to Wang, Maas and Lawson. This paper is contribution number 3001 of the Bermuda Institute of Ocean Sciences.

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Authors and Affiliations

  1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    Ali A. Thabet, Amy E. Maas, Gareth L. Lawson & Ann M. Tarrant

  2. Zoology Department, Faculty of Science, Al-Azhar University in Assiut, Assiut, Egypt

    Ali A. Thabet

  3. Bermuda Institute of Ocean Sciences, St. George’s, GE01, Bermuda

    Amy E. Maas

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  1. Ali A. Thabet
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  2. Amy E. Maas
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Correspondence to Amy E. Maas.

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Thabet, A.A., Maas, A.E., Lawson, G.L. et al. Life cycle and early development of the thecosomatous pteropod Limacina retroversa in the Gulf of Maine, including the effect of elevated CO2 levels. Mar Biol 162, 2235–2249 (2015). https://doi.org/10.1007/s00227-015-2754-1

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