Alteration of cleaner wrasse cognition and brain morphology under marine heatwaves

Heatwaves, exacerbated by global warming, are progressively affecting various ecosystems, with coral reefs among the most susceptible. Within these ecosystems, cleaner wrasses (Labroides dimidiatus), engage in cooperative interactions with client fish by removing ectoparasites, and play an essential role in sustaining client abundance and diversity. In 2016, the northern section of the Great Barrier Reef experienced widespread and intense bleaching due to unparalleled ocean temperatures associated with a marine heatwave. While prior studies have connected changes in fish densities following this heatwave to modifications in cleaner fish cognitive performance, the immediate impact of heatwave exposure on cleaner fish cognition and brain structure has yet to be investigated. Here, we exposed cleaner wrasses to a laboratory-simulated Category 1 marine heatwave for 55 days, mirroring the 2016 Great Barrier Reef event. Cleaners’ cognitive performance was evaluated through a visual discrimination task during the heatwave and after a 14-day recovery phase. This was followed by analysis of brain development 30 days after the cessation of the marine heatwave. Our results demonstrate that although heatwave exposure temporarily hindered cognitive performance, these deficits were recoverable. Interestingly, cleaner fish brain morphology, measured after recovery, underwent significant changes. Specifically, despite cleaners exposed to heatwaves having notably larger brains, their telencephalon was substantially smaller, while their brainstem was enlarged. These findings indicate that while some cognitive effects may be reversible, marine heatwave exposure leads to lasting alterations in brain morphology, particularly in regions associated with higher cognitive functions and social behaviour. This raises questions about the potential impact on more complex tasks that rely on these brain regions. We argue that the significant disruptions in cleaners' cognitive performance observed months after the 2016 due to neurological impairments linked to brain morphological changes. If so, a mere recovery of fish densities may not necessarily lead to a restoration of cognitive performance, as experiencing marine heatwaves might induce life-long morphological alterations in fish. Our results underscore marine heatwaves' intricate and enduring impact on cleaner fish, emphasising the need for comprehensive strategies to safeguard these vital components of coral reef ecosystems.

Methods
The dataset was collected from a laboratory experiment involving Bluestreak cleaner wrasses (Labroides dimidiatus; n=20), which were wild-caught in the Maldives and housed in flow-through aquaria at Laboratório Marítimo da Guia, Cascais, Portugal. Cleaners were exposed to two experimental treatments: control (28.8°C) and a simulated Category I marine heatwave (29.8°C). After a 5-day acclimation period, temperature was increased over 6 days to reach the target temperature for the heatwave treatment, and exposure lasted for 55 days. Afterward, a 30-day recovery period followed before brain dissection.

Behavioral trials, using an associative learning task (FAP test), were conducted at the end of the heatwave exposure and after a 14-day recovery period. Cleaners were tested individually on their ability to learn colour cues to locate a food reward, with up to 100 trials per fish.

Brain development was analyzed 30-days post exposure, with brains dissected into five regions and weighed for further analysis. Statistical analyses were performed using R, including survival analysis for learning tasks and weighted linear models for brain development.

The dataset includes variables on experimental treatments, task performance, body weight, brain weight, and brain region measurements.

全球变暖加剧的海洋热浪正持续影响各类生态系统，其中珊瑚礁是受影响最显著的生态系统之一。在这类生态系统中，裂唇鱼（Labroides dimidiatus）通过清除宿主鱼类体表寄生虫的方式与其形成互利共生关系，在维持宿主鱼类种群丰度与多样性方面发挥关键作用。2016年，大堡礁北部海域因一场海洋热浪引发的极端海水温度，发生了大规模严重的珊瑚白化事件。此前已有研究将此次热浪后鱼类种群密度的变化与裂唇鱼认知能力改变相关联，但海洋热浪暴露对裂唇鱼认知能力及脑结构的即时影响尚未得到探究。本研究中，我们将裂唇鱼置于实验室模拟的1级海洋热浪环境中暴露55天，以复刻2016年大堡礁的热浪事件。我们通过视觉辨别任务，分别在热浪暴露期间及14天恢复阶段后评估裂唇鱼的认知表现，并在海洋热浪暴露结束30天后对其脑发育情况进行分析。研究结果显示，尽管海洋热浪暴露会暂时损害裂唇鱼的认知能力，但这类认知缺陷是可恢复的。值得注意的是，恢复阶段后测得的裂唇鱼脑形态发生了显著变化：尽管热浪暴露组的裂唇鱼整体脑体积显著更大，但其端脑（telencephalon）体积明显更小，而脑干（brainstem）体积则有所增大。上述结果表明，尽管部分认知影响可逆转，但海洋热浪暴露会导致脑形态出现永久性改变，尤其是与高级认知功能及社会行为相关的脑区。这引发了一个疑问：此类变化可能会对依赖这些脑区的复杂行为任务产生何种潜在影响。我们认为，2016年热浪发生数月后观测到的裂唇鱼认知能力严重受损，可能与脑形态改变引发的神经功能损伤有关。若果真如此，仅恢复鱼类种群密度未必能使认知能力得到恢复，因为经历海洋热浪可能会导致鱼类产生终身性的脑形态改变。本研究结果凸显了海洋热浪对裂唇鱼的复杂且持久的影响，强调了需制定综合策略以保护珊瑚礁生态系统中这类关键物种。
方法
本数据集来源于一项针对蓝带裂唇鱼（Labroides dimidiatus；n=20）的实验室实验：实验个体均在马尔代夫野外捕获，饲养于葡萄牙卡斯卡伊斯的瓜亚海洋实验室（Laboratório Marítimo da Guia）的流水水族箱中。实验设置两组处理：对照组（水温28.8℃）与模拟1级海洋热浪组（水温29.8℃）。经过5天的驯化期后，实验组在6天内逐步升温至目标温度，热浪暴露时长为55天。暴露结束后，设置30天的恢复期，随后进行脑组织解剖。
行为测试采用联想学习任务（FAP测试），分别在热浪暴露结束时及14天恢复期后开展。实验以单尾裂唇鱼为测试对象，评估其学习颜色线索以获取食物奖励的能力，每尾鱼最多完成100次测试。
在暴露结束30天后对脑发育情况进行分析：将脑组织解剖为五个区域并称重，用于后续分析。统计分析使用R语言完成，包括针对学习任务的生存分析以及针对脑发育的加权线性模型。
本数据集包含实验处理组、任务表现、体重、脑重以及脑区测量等相关变量。