Adaptive strategies to increase fitness after thermal stress in the reef-building coral Acropora

doi:10.21203/rs.3.rs-1751930/v1

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Adaptive strategies to increase fitness after thermal stress in the reef-building coral Acropora

https://doi.org/10.21203/rs.3.rs-1751930/v1

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Elevated temperatures cause coral bleaching and reef degradation. However, coral may have strategies to survive for the next generation. We examined thermal stress's direct and carryover effects on fecundity and fitness in the reef-building coral, Acropora tenuis. Fragments from the same colony were subjected to control temperature (28 °C) or heat stress (31 °C) to cause bleaching. We then examined the fecundity of adults (egg number and size) and the thermal tolerance of larvae (larval survival and settlement rates) and juveniles to evaluate the fitness of stressed corals. As a result of bleaching, the thermal stress-induced changes in egg production by adults led to increased larval production and potentially higher rates of survival for larvae and juveniles. In addition, symbiotic relationships may assist the survival of larval stages with lower lipid content. Collectively, heat-vulnerable corals have developed adaptive strategies that may help them deal with the challenges of global warming.

Alternative tactics

Consecutive thermal stress

coral

fecundity

fitness

Juveniles

Acropora tenuis

Global warming represents a widespread threat to a variety of communities, including coral reefs (1, 2). In recent decades, coral reef communities worldwide have experienced mass bleaching and mortality owing to temperature anomalies (3, 4), leading to reef decline (5). Coral bleaching was especially heavy from 2014 to 2017 (4), and more than 70% of coral reefs worldwide have experienced heat stress due to a temperature increase of 1–2 °C (4). Severe bleaching is expected to become ubiquitous within the next few decades (1, 6), leading to the potential collapse of coral reefs (5, 7, 8).

Recent findings indicate that corals can acclimate to higher water temperatures and become more tolerant to thermal stress (9-12). Although heat-tolerant species can survive thermal stress, this may ultimately have negative consequences (13, 14), such as declining physiological performance (15), reproduction (16, 17), number and size of oocytes (18, 19), larval settlement (20), and recruitment (21, 22). These factors can ultimately reduce the capacity for coral reef recovery (16) and influence the population dynamics of the ecosystem (23, 24). In addition, although young corals in early life stages are more sensitive to stressors than adults (25, 26), the acclimation potential of coral species at different life stages has not been evaluated systematically. Investigations in this regard may reveal critical ecological issues, especially in cases where tolerances vary across life cycles due to future global warming.

The early life stages of reef-building corals are crucial for reef maintenance and the replenishment and persistence of degraded coral reefs (27, 28). These life stages are also affected by surrounding water temperatures. Given the widespread degradation of coral reefs (1, 29), the thermal stress history of parents can influence the thermotolerance of early life stages in corals and other marine organisms (30, 31). Some coral species release gametes and larvae each month (32). Thus, it is highly likely that some larvae were released and settled by adult colonies, resulting in high-temperature conditions (33, 34). The coral species Acropora tenuis inhabits shallow reefs with temperature fluctuations, and these fluctuating temperatures may affect both larval settlement and juveniles (24). Responses to temperature (such as larval recruitment) also vary across species (35), and the effects of thermal stress on adults, larvae, and juveniles have been reported in previous studies. However, the effects of successive thermal stress on adults and the subsequent effects on their fecundity, the larval stage, and juveniles have not been examined.

In this study, we examined the effects of heat stress on the reproduction and early life stages (oocytes, larvae, larval settlement, and early juveniles) of corals (Fig. 1).

Physiological responses of adult colony fragments to thermal stress

Brightness was significantly higher in stressed fragments (SF) than in control fragments (CF) (Fig. 2A, p=0.0064). We also measured the photosynthetic efficiency of coral fragments in two different treatments over the experimental period. The dark-adapted quantum yield of photosystem II (Fv/Fm) was significantly lower in SF than in CF, as estimated using a linear mixed model (LMM, F=27.65, p<0.0001). There was an apparent reduction in Fv/Fm from day 5 of exposure to elevated temperatures. In contrast, CF maintained stable Fv/Fm values during the experiment (Fig. 2B).

Symbiotic algal density was measured in the SF and CF in all treatments before and after thermal stress. SF lost >35% of their initial algal cell density (Fig. 2D), whereas CF exhibited the highest algal density. After 10 d of exposure to elevated temperatures, there was a significant difference in algal density between the treatments (unpaired two-sample t-test, p=0.006). Chlorophyll a and c₂ contents per surface area decreased in SF during the experimental period. Although the chlorophyll content per surface area was not significantly different between groups (unpaired two-sample t-test, p=0.09), chlorophyll c₂ levels were significantly lower in SF than in CF (unpaired two-sample t-test, p=0.02).

Survivorship was significantly different between CF and SF (Fig. 2C; Kaplan-Meier log-rank test, p<0.002). The survival percentage was 100% in CF but 83.33% in SF (Fig. 2C).

Gamete characteristics of adults

One SF did not spawn at all during the spawning period. However, the number of eggs per bundle increased after thermal stress treatment. The number of eggs per bundle was higher in SF (10.79±0.48; mean±standard error of the mean [SE]) than in CF (9.08±0.36) (Fig. 3A), and the difference was statistically significant (unpaired two-sample Wilcoxon test, p=0.003). In contrast, egg volume decreased significantly after thermal stress. The mean egg volume was significantly (unpaired two-sample Wilcoxon test, p=0.0002) higher in CF (0.7±0.04 μm³; range, 0.52–1.17 μm³) than in SF (0.52±0.02 μm³; range, 0.34–0.83 μm³) (Fig. 3 B).

Larval responses to thermal stress

SF larvae exhibited substantial thermal tolerance. During the 21 d of thermal stress treatment, survival rates were lowest in CF larvae under thermal stress (CS; 66.6±16.45%) and SF larvae under thermal stress (SS; 66.6±16.45%). Survivorship was not significantly different between CS and SS (Kaplan-Meier log-rank test, p=0.08). In contrast, survival rates were higher in CF larvae under control conditions (CC; 92.6±1.29%) and SF larvae under control conditions (SC; 91.4±0.75%). Survival rates were not significantly different between CC and SC (Fig. 3E). However, the results of the log-rank test showed that survival rates differed significantly between larvae in high-temperature versus control conditions (Table 1).

To estimate differences in larval size, we measured 30 larvae in each treatment. CF larvae (1087.82±51.58 μm) were larger than SF larvae (868.33±19.16 μm), and the difference was significant (generalized linear model, p=0.0001; Fig. 3C).

Lipid depletion rates in 5-d-old A. tenuis planula varied among the treatments (SF and CF larvae). Lipid contents were significantly lower in SF larvae than in CF larvae (linear model (LM), p=0.02). On average, the initial lipid contents were 13.72±0.36 μg in SF larvae and 17.33±0.57 μg in CF larvae (Fig. 3D). After 21 d of exposure to control and thermal stress conditions, the lipid contents of the larvae decreased significantly in all treatments (LM, p<0.01) (Fig. 3D). Lipid content was lower in larvae exposed to thermal stress than in those exposed to control treatments; however, there was no significant difference between the groups. Lipid depletion rates were highest in the control treatments (CC, 32.3%; SC, 29.62%) and relatively lower in the stress treatments (CS, 23.91%; SS, 19.8%).

Effect of thermal stress on larval size and settlement rate

On day 1 of the larval settlement period, larval settlement rates were significantly higher in thermal stress treatments than in control treatments. The cumulative settlement rates in CS (82.6±1.54%) were higher than those in the other treatments. The settlement rate was lowest in SS (69.2±8.17%). Among the control treatments, SC larvae (81.8±3.31%) exhibited a higher settlement rate than CC larvae (74.4±2.14%). Overall, the cumulative number of settled larvae did not differ significantly among treatments (LM, p>0.05) over the settlement period (Fig. 4A). In each treatment, we measured the size of 30 early recruits. Early recruits in the control treatments were larger than those in the stress treatments. In particular, early recruits in CC were significantly larger than those in the corresponding stress treatments, including CS (LM, p<0.0001), SC (LM, p<0.004), and SS (LM, p<0.0001) (Fig. 4B). The sizes of early recruits did not differ significantly between the SC and SS groups (LM, p=0.1).

Effect of thermal stress on post-settlement survival

After 21 d of exposure to thermal stress, the survival rates of recruits were highest in the control treatments, including SC (87.04±4.74%) and CC (85.46±2.53%). The survivorship of recruits was significantly lower in stress treatments compared with that in the corresponding control treatments (Kaplan-Meier log-rank test; CS vs. CC, p<0.0001; SS vs. SC, p<0.0001) (Table 2). However, recruit survival rates were significantly higher in SS (72.31±10.77%) than in CS (66.2±12.45%) (Kaplan-Meier log-rank test, p<0.0001).

The present study shows that coral colonies under thermal stress can develop strategies to increase their fitness. Based on our results, we predict a trade-off between egg size and the number of eggs per bundle. Thermal stress can have significant effects on egg size and fecundity (36, 37). In the present study, egg volumes were smaller in SF treatments than in CF treatments (Fig. 3B), but the number of eggs per bundle was significantly higher in SF than in CF. Other studies have shown that thermal stress or bleaching can reduce the number of eggs and larvae (38, 39). This indicates a relationship between egg size and egg number (fecundity) in corals (40, 41) and suggests that larger eggs result in a reduced number of gametes (42). Conversely, another study has reported no relationship between egg size and number of eggs (43). Nevertheless, overall findings suggest that egg size and fecundity depend on parent colony conditions and energy reserves.

Regardless of thermal stress, the lipid content of coral eggs differed with egg size. However, the reduced lipid content of eggs did not affect their survival rate. The lipid content of CF larvae was higher than that of SF larvae after fertilization, but there was no significant difference in survivorship between treatments under thermal stress conditions. In contrast with this finding, other studies have suggested that lipid levels in larvae may be associated with energy allocation in larvae (44) and the sizes of eggs and larvae (37), indicating that smaller eggs would have fewer energetic reserves (lipids) than larger eggs and larvae (18, 36, 37). Nevertheless, in this study, the lipid content of coral eggs was positively correlated with their survival rates, and the rate of lipid consumption was lower in SF larvae than in CF larvae under thermal stress after 21 d. Collectively, the stressed coral fragments produced smaller larvae, which were not vulnerable to thermal stress.

After dispersal with lower levels of lipid, SF larvae tended to settle rapidly, and the juveniles were more tolerant to high water temperatures. There were no significant differences in larval settlement between SF and CF larvae. However, larval development and metamorphosis are known to utilize energy from lipids (45, 46). In contrast to our findings, previous studies have reported adverse effects of high temperature on larval settlement (13, 47). Larvae with low lipid levels develop associations with symbiotic algae (46), which may facilitate the survival of juveniles descended from SF parents.

Previous studies have reported the undesirable effects of thermal stress on the growth of other marine invertebrates (48, 49). The thermal stress condition is predicted to have a negative impact on juveniles descended from SF parents due to smaller polyps in the SF (likely a result of polyp formation at high temperatures). In addition, thermal stress may also influence the larval phenotype, as larval development is faster under thermal stress than under normal conditions.

This study showed that thermal stress influenced reproduction and the early life stages of corals without causing any changes in energy investment. We also found that colonies that experienced heat stress developed tactics to increase their fitness. For example, colonies under heat stress produced smaller eggs in larger numbers, which can improve the chances of larval settlement and recovery in disturbed ecosystems. Corals also exhibited thermal acclimation under thermal stress. The acclimation potential of a subsequent generation identified in this study indicates the possibility that future coral generations may survive conditions of thermal stress. However, further research is required to understand the relationship between warm ocean temperatures, coral recruitment survival, and recovery potential over successive generations.

Coral collection and experimental design: effects of thermal stress on different life stages

In this study, we examined the effects of thermal stress on the following life stages and functions in the coral Acropora tenuis: adults (Experiment 1), adult fecundity (egg number and size) (Experiment 2), larval settlement rates (Experiment 3), and early recruitment (Experiment 4) (Fig. 1). To examine thermal stress and its carryover effects, we used coral fragments from the same colony to ensure a uniform genetic background, (Fig. 1, Supplementary Information 1). Coral fragments were exposed to two temperatures—28 °C (control) and 31 °C (stress)—for 10 d in a flow-through system. In the stress experiment, we placed a heater in each tank, and the temperature was gradually increased from 28 °C to ~31 °C over the course of 1.5 d (~0.5 °C every 6 h). We maintained the temperature at 31 °C until the fragments started to show visible bleaching. During this experiment, the fragments were maintained under 12-h light (160 µmol quanta m^–2 s^–1) and 12-h dark conditions.

We photographed the fragments to monitor their color and the maximum quantum yield of photosystem II (Fv/Fm) throughout the experiment (see below). We also measured their physiological parameters (including the symbiotic algal density and chlorophyll content) before and after the experiment (see below). Finally, all fragments were transplanted back to the reef until spawning occurred the following year.

In the spring of 2019, we examined the effects of thermal stress on larval stages, larval settlement, and early recruitment in corals (Fig. 1). One week before the anticipated spawning date, fragments from the previous year’s thermal stress experiment were retrieved from the reef. They were transported to an outdoor tank supplied with a flow-through seawater system and kept there until spawning. We set two treatment conditions (thermal stress and control) and used stressed fragments (SF) and controlled fragments (CF) for measurements. First, we collected gamete bundles from one coral fragment per aquarium at 19:30–20:40 hrs on June 12, 2019. We then mixed gametes from the same treatment groups (not from other treatments) for cross-fertilization. For Expriments 2, 3, and 4, we divided the larvae from each treatment into two groups (thermal stress and control). The thermal stress experiments on larvae were followed by the measurement of larval settlement rates and early recruitment under thermal stress (~31 °C) or control (28 °C) conditions. The temperature in the thermal stress treatment was increased at a rate of ~0.5 °C every 6 h and then maintained for 21 d. The water temperature was monitored every 10 min and recorded using a temperature logger (HOBO Water Temp Pro v2, Onset Computer Corporation, Bourne, MA, USA) throughout the experiment. Each treatment included three replicates, and all tanks were filled with seawater and equipped with a heater.

Physiological parameters of coral adults

We evaluated the photosynthetic activity of coral fragments in each treatment group by measuring the maximum quantum efficiency of photosystem II (Fv/Fm), the color of the fragment, and the symbiotic algal density (Supplementary Information 1). Following the thermal stress experiment, the fragments were transferred to the reef, and their recovery status was monitored. The fragments were photographed monthly using an underwater camera (Canon Powershot G10, Canon Inc., Tokyo, Japan). Survival rates were recorded 10 months after the thermal stress experiment.

Carryover effects of thermal stress on oogenesis and subsequent larvae

We counted the number of eggs per bundle and measured the size of eggs to examine the effects of thermal stress on the fecundity of adult corals (Supplementary Information). We measured the longest and shortest axis (length and width, respectively) of each egg using Image J (50)assuming an elliptical shape. Egg volume (EV) was calculated using the formula EV = 4/3 πab², where a=½ egg length and b=½ egg width. We also measured the amount of lipids in the eggs according to a previously described method (44).

We measured the survival rate, size, and lipid content of the larvae to investigate the carryover effects of thermal stress on the next generation. We set two temperature treatments (control, 28 °C; thermal stress, 31 °C), with five glass containers for each treatment (five replicates × two treatments). We filled the containers with 300 mL of seawater (replaced every day). For survival analysis, we counted the number of live larvae in each treatment daily for 21 d. At 5 days post-fertilization (dpf), we randomly collected 50 larvae from each treatment group and photographed them under a microscope (Olympus BX53, Olympus Corporation, Tokyo, Japan) using a CCD camera (Olympus DP 72) at 10× magnification.

We compared the settlement rates of larvae in each treatment condition (control and stress) and under two temperature treatments (control and thermal stress) in five containers. In addition, we counted metamorphosed planulae as "settled planulae" after 24 and 48 h with a stereomicroscope (Olympus SZ61). We also photographed the spats with a digital camera (Canon G 10) and measured their size using ImageJ.

To evaluate the survival of early recruits in each condition, we maintained early recruits from settled larvae under thermal stress for 21 d. The cells were counted and photographed daily.

Statistical analysis

Before conducting statistical analysis, we examined the normality and homogeneity of the data using the Shapiro–Wilk and Levene's tests, respectively. To assess the differences in brightness and Fv/Fm among adult colonies over the experimental period, we used an LMM. The models were fitted using the 'nlme' package in R statistical software and selected according to Akaike's Information Criterion (51). We examined the symbiotic algal density and chlorophyll content of adult colonies among treatments using an unpaired t-test. In addition, we applied the Kaplan-Meier log-rank test to analyze survivorship in adult colonies, their larvae, and the recruits in different treatment groups. To compare the number of eggs per bundle, egg volume, and larval settlement rates between groups, we used a non-parametric Kruskal-Wallis test or pairwise Wilcoxon test with multiple comparisons. In cases where the assumptions for variance, normality, and homogeneity could not be met, we used a generalized linear model to compare larval sizes and larval settlement rates between treatments. All statistical analyses were performed using R statistical software (v.4.0.4) (51).

Author Contributions: S.H.-K. designed research; S.H.-K. performed research; S.H.-K., and M.M., P.T.-K. analyzed data; S.H.-K., M.M., T.N., P.T.-K., S.K. contributed new reagents/analytic tools; S.H.-K., and M.M. wrote the paper. All authors commented and approved the manuscript.

Competing Interest Statement: Authors have no competing interest.

Acknowledgments

We would like to thank Dr. S. Harii and F.Sinniger for useful comments and the staff of the Sesoko Station for their support. This work was partly supported by the Project Foundation of the Tropical Biosphere Research Center of the University of the Ryukyus and JSPS KAKENHI (21H05304, 22H02369 to MM)

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There is NO Competing Interest.

DataSanazfecundity210811.xlsx
Data set of this study
SupplementaryTable1.pdf
SupplementaryTable2.pdf
Supplementaryinformation1.docx

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Adaptive strategies to increase fitness after thermal stress in the reef-building coral Acropora

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