Impact of ocean warming on a coral reef fish learning and memory

Abstract

Tropical ectotherms are highly sensitive to environmental warming, especially coral reef fishes, which are negatively impacted by an increase of a few degrees in ocean temperature. However, much of our understanding on the thermal sensitivity of reef fish is focused on a few traits (e.g., metabolism, reproduction) and we currently lack knowledge on warming effects on cognition, which may endanger decision-making and survival. Here, we investigated the effects of warming on learning and memory in a damselfish species, Acanthochromis polyacanthus. Fish were held at 28-28.5 °C (control group), 30-30.5 °C (moderate warming group) or 31.5-32 °C (high warming group) for 2 weeks, and then trained to associate a blue tag (cue) to the presence of a conspecific (reward). Following 20 training trials (5 days), fish were tested for associative learning (on the following day) and memory storage (after a 5-days interval). The control group A. polyacanthus showed learning of the task and memory retention after five days, but increasing water temperature impaired learning and memory. A thorough understanding of the effects of heat stress, cognition, and fitness is urgently required because cognition may be a key factor determining animals' performance in the predicted scenario of climate changes. Knowing how different species respond to warming can lead to better predictions of future community dynamics, and because it is species specific, it could pinpoint vulnerable/resilience species.

Keywords: Behavior; Climate change; Cognition; Damselfish; Stress; Temperature.

Figure 1. Schematic views of the tank used for the learning tests in Acanthochromis polyacanthus and Amphiprion percula.

The numbers show the dimensions of the tank in cm. All walls were gray and one of them received a blue card to indicate the hall where the conspecific fish was placed. The start box (10 cm diameter) was placed in the center to serve as a release area. (A) Overview, (B) side view.

Figure 2. Time spent in the non-target and the target halls of the tank during learning and memory test.

Acanthochromis polyacanthus time spent in the non-target halls (mean of hall 1, 2 and 3) and the target hall of the tank during the learning test and the memory test. The data show the percentage of time spent (n = 10). The central area was not considered for the analysis. The target hall was presented with a blue card (stimulus) to orientate the fish. During the training trials, the hall with the blue card showed a conspecific fish to serve as social reward. Fish were allowed to explore the tank for 10 min per day. The learning test (gray bars) was applied after 20 training trials and no reward was presented. The memory test (blue bars) was applied 5 days after the learning test. A. polyacanthus were held at three different water temperature (A) 28–28.5 °C –control, (B) 30–30.5 °C, and (C) 31.5–32 °C. Different lower-case letters indicate statistical significance (a ⁄ = b) at p < 0.05 (GLMM).

Figure 3. Latency to enter the target hall over the training days.

Acanthochromis polyacanthus latency to enter the target hall during the training days, and the learning and the memory test after being held at three different water temperature control: 28–28.5 °C, moderate warming: 30–30.5 °C, and high warming: 31.5–32 °C. Data are shown as median and quartiles (n = 10). (A) During the training days (four trails/fish/day), the target hall was presented with a blue card to orientate the fish and a conspecific served as social reward in the target hall. An asterisk (*) indicates the median value of the box plot. Latency and days were scaled to values between 0-1. (B) During the learning and memory tests, no reward was present but the blue card guided fish behavior. Fish latency to enter the target hall is presented for the learning test and memory test with a line connecting the same individual. Different lower-case letters above plots indicate statistical significance (GLMM) at p < 0.05 (a ⁄ = b ⁄ = c).

Figure 4. Percentage of first choice for the target hall in the experimental tank.

Percentage of Acanthochromis polyacanthus’s first choice for the target hall of the tank during the training days, learning test and the memory test. Fish were held at three different water temperature: (A) 28–28.5 °C (control), (B) 30–30.5 °C (moderate warming), and (C) 31.5–32 °C (high warming). The target hall was presented with a blue card (stimulus) to orientate the fish. During the training trials (four trails/day), the target hall presented a blue card and a conspecific fish inside the target hall served as social reward. Fish were allowed to explore the tank for 10 min per day. The learning test was applied after 20 training trials and no reward was presented. The memory test was applied 5 days after the learning test. Data are shown as percentage of correct first choice (target hall) over the experimental phases. During the training days, each fish was tested four times. During the learning test and memory test, each fish was tested only once (n = 10). Different lower-case letters indicate statistical significance (LMM) at p < 0.05 (a ⁄ = b).

Figure 5. (A–D) Locomotor parameters during the learning and memory tests.

Effects of temperature (28–28.5 °C –control, 30–30.5 °C –moderate warming, and 31.5–32 °C –high warming) on Acanthochromis polyacanthus locomotor parameters during the learning test and the memory test. Data correspond to median values and quartiles (n = 10). Fish behavior was recorded for 10 min. No statistical significance was observed between groups (GLMM, p > 0.05).