Temperature is the evil twin: Effects of increased temperature and ocean acidification on reproduction in a reef fish

Reproduction in many organisms can be disrupted by changes to the physical environment, such as those predicted to occur during climate change. Marine organisms face the dual climate change threats of increasing temperature and ocean acidification, yet no studies have examined the potential interactive effects of these stressors on reproduction in marine fishes. We used a long-term experiment to test the interactive effects of increased temperature and CO2 on the reproductive performance of the anemonefish, Amphiprion melanopus. Adult breeding pairs were kept for 10 months at three temperatures, 28.5°C (+0.0°C), 30.0°C (+1.5°C) and 31.5°C (+3.0°C), cross-factored with 3 CO2 levels, a current day control (417 µatm) and moderate (644 µatm) and high (1134 µatm) treatments consistent with the range of CO2 projections for the year 2100 under RCP8.5. We recorded each egg clutch produced during the breeding season, the number of eggs laid per clutch, average egg size, fertilization success, survival to hatching, hatchling length and yolk provisioning. Adult body condition, hepatosomatic index, gonadosomatic index, and plasma 17beta-estradiol concentrations were measured at the end of the breeding season to determine the effect of prolonged exposure to increased temperature and elevated CO2 on adults, and to examine potential physiological mechanisms for changes in reproduction. Temperature had by far the stronger influence on reproduction, with clear declines in reproduction occurring in the +1.5°C treatment and ceasing altogether in the +3.0°C treatment. In contrast, CO2 had a minimal effect on the majority of reproductive traits measured, but caused a decline in offspring quality in combination with elevated temperature. We detected no significant effect of temperature or CO2 on adult body condition or hepatosomatic index. Elevated temperature had a significant negative effect on plasma 17beta-estradiol concentrations, suggesting that declines in reproduction with increasing temperature were due to the thermal sensitivity of reproductive hormones rather than a reduction in energy available for reproduction. Our results show that elevated temperature exerts a stronger influence than high CO2 on reproduction in A. melanopus. Understanding how these two environmental variables interact to affect the reproductive performance of marine organisms will be important for predicting the future impacts of climate change.

诸多生物的繁殖过程均可因物理环境改变而受到干扰，其中就包括气候变化背景下预计会出现的环境变化。海洋生物面临着气候变化带来的双重胁迫：海水升温与海洋酸化，但目前尚无研究探讨这两类胁迫因子对海洋鱼类繁殖的潜在交互影响。本研究通过长期实验，探究了升温与二氧化碳浓度升高对公子小丑鱼（Amphiprion melanopus）繁殖性能的交互影响。实验将成年繁殖配对个体置于三个温度梯度（28.5℃（增温0.0℃）、30.0℃（增温1.5℃）、31.5℃（增温3.0℃））下饲养10个月，并与三个二氧化碳浓度梯度进行交叉处理设置：当前环境对照（417 µatm）、中度胁迫组（644 µatm）与高度胁迫组（1134 µatm），其中高浓度处理与RCP8.5情景下2100年的二氧化碳浓度预测范围相符。研究记录了繁殖季内每窝产出的鱼卵、每窝产卵数、平均卵径、受精成功率、孵化存活率、初孵幼体体长与卵黄供给量。于繁殖季结束时测定成体体况、肝体指数（hepatosomatic index）、性腺指数（gonadosomatic index）以及血浆17β-雌二醇（17beta-estradiol）浓度，以明确长期暴露于升温与高二氧化碳环境对成体的影响，并探究繁殖性能变化的潜在生理机制。相较而言，温度对繁殖的影响更为显著：增温1.5℃处理组的繁殖性能出现明显下降，而增温3.0℃处理组的繁殖活动完全终止。与之相对，二氧化碳浓度升高对多数测定的繁殖性状影响极小，但在与升温共同作用时会导致后代品质下降。本研究未观测到温度或二氧化碳浓度升高对成体体况及肝体指数存在显著影响。升温对血浆17β-雌二醇浓度存在显著负向影响，这表明升温导致的繁殖性能下降源于生殖激素的热敏感性，而非繁殖可用能量的减少。本研究结果表明，相较于高二氧化碳浓度，升温对公子小丑鱼（A. melanopus）的繁殖性能影响更强。明确这两类环境因子的交互作用如何影响海洋生物的繁殖性能，对于预测气候变化的未来影响具有重要意义。