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Brooding strategy in fluctuating salinity environments: oxygen availability in the pallial cavity and metabolic stress in females and offspring in the Chilean oyster Ostrea chilensis

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Abstract

Organisms that encounter stressful situations in nature often cope using behavioral (e.g., avoidance) or physiological tactics. In sessile mollusks, the only available behavioral option in dealing with salinity stress is to “clam up”, isolating their tissues from the environment. Though effective in the short term, prolonged isolation can have detrimental physiological consequences, particularly for females brooding embryos in a mantle cavity that is isolated from the external environment. In the Quempillén estuary, the Chilean oyster, Ostrea chilensis, spent nearly one-third of its brooding season at salinities low enough to cause female isolation. When females thus isolated themselves, the dissolved oxygen in their mantle cavity fluid dropped to hypoxic levels within 10 min. In females that were brooding embryos, this depletion of oxygen was not uniform: oxygen was depleted more quickly in the palp region (where embryos accumulate) than in the inhalant region. Additionally, oxygen was reduced even more quickly in the palp region when females were brooding late-stage embryos, which consumed oxygen significantly more quickly than embryos in earlier developmental stages. Finally, O. chilensis used anaerobic metabolism to cope with the hypoxia induced by isolation, as lactate accumulated in the tissues of both females (brooding > non-brooding) and embryos (late stage > early stage). Our findings demonstrate the trade-off between an adaptive avoidance behavior (clamming up) and the potentially detrimental consequences brought on by such a behavior (hypoxia). Cycling of embryos throughout the mantle cavity by deliberate female pumping keeps them from accumulating in the area between the palps, forestalling the creation of hypoxic conditions there. In addition, the capacity for anaerobic metabolism by both females and their embryos should help them tolerate the low oxygen levels that do eventually arise when the pallial cavity is isolated from the surrounding environment during long periods of reduced ambient salinity.

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Acknowledgments

We would like to thank Mrs. Olga Rodriguez for her help collecting oysters at the Quempillén field station (Universidad Austral de Chile), where a part of this study was performed. This research was supported by the Fondecyt-Chile 1100335 and 1141052 (Fondo Nacional de Investigación Científica y Tecnológica, Chile) and Enlace grant from Dirección de Investigación y Desarrollo from Universidad Austral de Chile to ORC.

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Authors and Affiliations

  1. Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile

    Cristian J. Segura, Jaime A. Montory, Victor M. Cubillos & Oscar R. Chaparro

  2. Biology Department, Tufts University, Medford, MA, 02155, USA

    Casey M. Diederich & Jan A. Pechenik

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  1. Cristian J. Segura
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  2. Jaime A. Montory
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  3. Victor M. Cubillos
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  4. Casey M. Diederich
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  6. Oscar R. Chaparro
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Correspondence to Oscar R. Chaparro.

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Communicated by I. D. Hume.

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Segura, C.J., Montory, J.A., Cubillos, V.M. et al. Brooding strategy in fluctuating salinity environments: oxygen availability in the pallial cavity and metabolic stress in females and offspring in the Chilean oyster Ostrea chilensis . J Comp Physiol B 185, 659–668 (2015). https://doi.org/10.1007/s00360-015-0908-6

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