Exposure to chronic and high dissolved copper concentrations impedes meiospore development of the kelps Macrocystis pyrifera and Undaria pinnatifida (Ochrophyta)

Abstract:

Copper in low natural concentrations is essential for cell metabolism but in excess it becomes extremely toxic to aquatic life, including to the early life stages of marine macroalgae. This work determined the effects of copper exposure on meiospore development of two kelp species, the native Macrocystis pyrifera and invasive Undaria pinnatifida. After settlement, meiospores were exposed to nominal copper concentrations of control (no added copper), 100, 200, 300 and 400 μg L⁻¹ Cu for 9 days. Inductively coupled plasma mass spectrometry of total dissolved copper (Cu_T) concentrations in the blanks showed that nominal copper concentrations were reduced to 54, 91, 131 and 171 μg L⁻¹ Cu_T, respectively, indicating that > 50% of the dissolved copper was adsorbed onto the culture vessel walls. In the media with meiospores, the dissolved copper concentrations decreased to 39, 86, 97 and 148 μg L⁻¹ Cu_T in M. pyrifera and to 39, 65, 97 and 146 μg L⁻¹ Cu_T in U. pinnatifida, indicating that 6–15% of the dissolved copper was adsorbed by the cells. For both species, meiospores germinated in all copper treatments, with germination decreasing with increasing copper concentration. However, gametophyte growth and sexual differentiation were arrested under all copper treatments. The effective copper concentration causing 50% of arrested germination (Cu-EC₅₀) was 157 and 231 μg L⁻¹ Cu_T for M. pyrifera and U. pinnatifida, respectively. The higher Cu-EC₅₀ for U. pinnatifida suggests ecological success for the invasive species in copper-polluted environments; however, the subsequent inhibition of gametogenesis under all copper treatments indicated no difference in copper tolerance between both kelp early life stages. We compare our results with the literature available on the effects of copper on the development of early life stages of brown seaweed (Laminariales and Fucales) and discuss the importance of reporting actual experimental dissolved copper concentrations and the necessity of standardizing the response variables measured in macroalgal copper ecotoxicology.

Key Words::

• Dissolved concentration
• Effective concentration
• Gametophyte
• Germination
• Invasive kelp
• Nominal concentration

ACKNOWLEDGEMENTS

We thank BECASCHILE-CONICYT, the Royal Society of New Zealand Mardsen grant (UOO0914) and the New Zealand MBIE programme C01X1005 for funding. We thank Pamela Fernández and Rocio Suárez for the assistance during field sampling. We thank the two anonymous reviewers for their thoughtful and constructive comments.