Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement

Locating appropriate settlement habitat is a crucial step in the life cycle of most benthic marine animals. In marine fish, this step involves the use of multiple senses, including audition, olfaction and vision. To date, most investigations of larval fish audition focus on the hearing thresholds to various frequencies of sounds without testing an ecological response to such sounds. Identifying responses to biologically relevant sounds at the development stage in which orientation is most relevant is fundamental. We tested for the existence of ontogenetic windows of reception to sounds that could act as orientation cues with a focus on vulnerability to alteration by human impacts. Here we show that larvae of a catadromous fish species (barramundi, Lates calcarifer) were attracted towards sounds from settlement habitat during a surprisingly short ontogenetic window of approximately 3 days. Yet, this auditory preference was reversed in larvae reared under end-of-century levels of elevated CO2, such that larvae are repelled from cues of settlement habitat. These future conditions also reduced the swimming speeds and heightened the anxiety levels of barramundi. Unexpectedly, an acceleration of development and onset of metamorphosis caused by elevated CO2 were not accompanied by the earlier onset of attraction towards habitat sounds. This mismatch between ontogenetic development and the timing of orientation behaviour may reduce the ability of larvae to locate habitat or lead to settlement in unsuitable habitats. The misinterpretation of key orientation cues can have implications for population replenishment, which are only exacerbated when ontogenetic development decouples from the specific behaviours required for location of settlement habitats.

寻找适宜的定居栖息地是大多数底栖海洋动物生命周期中的关键步骤。对于海洋鱼类而言，这一步骤涉及多种感官的运用，包括听觉、嗅觉与视觉。迄今为止，多数关于仔鱼听觉的研究聚焦于其对不同频率声音的听觉阈值，却未测试此类声音引发的生态响应。在定向行为最关键的发育阶段，识别仔鱼对生物学相关声音的响应至关重要。我们测试了仔鱼是否存在对可作为定向线索的声音的接收发育窗口（ontogenetic windows of reception），并重点关注其易受人类活动影响而改变的脆弱性。研究发现，一种降海产卵鱼类（尖吻鲈，Lates calcarifer）的仔鱼在一个时长仅约3天的极短发育窗口内，会被定居栖息地的声音所吸引。然而，在本世纪末预测的高二氧化碳浓度环境中饲养的仔鱼，其听觉偏好发生逆转，转而会被定居栖息地的线索所排斥。此类未来环境条件还会降低尖吻鲈仔鱼的游泳速度，并加剧其焦虑程度。出乎意料的是，高二氧化碳浓度导致的发育加速与变态开始，并未伴随对栖息地声音吸引反应的提前出现。这种发育过程与定向行为时机之间的不匹配，可能会降低仔鱼定位栖息地的能力，或导致其定居于不适宜的环境中。对关键定向线索的误判会影响种群补充，而当发育过程与定居栖息地定位所需的特定行为脱钩时，这一影响会进一步加剧。