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Living within constraints: irreversible chemical build-up and seasonal temperature-mediated die-off in a highly acidic (H2SO4) annual seaweed (Desmarestia viridis)

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Abstract

Seaweeds exhibit a number of adaptations to cope with strong selective pressures imposed by shallow marine environments. The exceptional ability of the annual, brown seaweed Desmarestia viridis, to produce and store high concentrations of sulfuric acid (H2SO4) in intracellular vacuoles, makes it a particularly compelling model for studies of causes and consequences of acid production in seaweeds. We used two laboratory experiments, as well as measurements of intracellular pH of sporophytes and sea salinity and temperature over an entire growth season at one site in Newfoundland and Labrador (Canada), to test hypotheses about effects of salinity and temperature on acid production and die-off in D. viridis. We show that the acid is continuously and irreversibly accumulated (resulting in an intracellular pH as low as 0.53) as the seaweed grows from recruit to adult (March–June) and that this build-up inevitably culminates into dramatic mass releases of acid and die-offs. Progressive, synchronous death among individuals is under the predominant control of sea temperature (death systematically occurred around 12 °C in both laboratory and field), which suggests the evolution of a life-history strategy in which death occurs at a time when individuals reach a size that may correspond to reproductive maturity. The seaweed exhibits a low tolerance to changes in salinity (death was inevitable below 29 psu), which likely imposes severe limitations on its distribution range throughout its existence as a sporophyte. Our findings suggest that major phenological events and survival in D. viridis are intimately linked to synergistic effects of oceanographic controls, which either impair the ability of the seaweed to retain the acid in its tissues (seasonal sea warming), or contribute to dissipating the acid that is released to the environment (wave and current action). They also provide novel insights into the ecophysiological and evolutionary constraints within which marine organisms adapt.

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Acknowledgments

We are grateful to Scott Caines, Kyle Matheson, Alicia Morry, Travis Nielsen, and Andrew Perry for help with field and laboratory work, as well as four anonymous reviewers for constructive comments that helped improve the manuscript. Johanne Vad received financial support from École Normale Supérieure de Paris (ENS, France) to conduct a graduate research internship in a foreign country. This research was funded by NSERC (Discovery Grant) and Canada Foundation for Innovation (CFI-Leaders Opportunity Funds) grants to Patrick Gagnon.

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  1. Department of Ocean Sciences, Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Patrick Gagnon & Caitlin Blain

  2. Département de Biologie, École Normale Supérieure de Paris, 75230, Paris, France

    Johanne Vad

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  1. Patrick Gagnon
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  2. Caitlin Blain
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Correspondence to Patrick Gagnon.

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Communicated by K. Bischof.

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Gagnon, P., Blain, C. & Vad, J. Living within constraints: irreversible chemical build-up and seasonal temperature-mediated die-off in a highly acidic (H2SO4) annual seaweed (Desmarestia viridis). Mar Biol 160, 439–451 (2013). https://doi.org/10.1007/s00227-012-2101-8

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