Many Acropora corals at Scott Reef spawn biannually, but most individuals spawn either in autumn or in spring (not in both seasons) and are thus temporally isolated from one another with respect to reproduction10,25. Gametogenesis takes ~ 4 to 6 months in Acropora corals at Scott Reef10. While it is unknown whether gametogenesis occurs at different rates in the different seasons, coral colonies experience different environmental conditions through the gametogenic period, leading up to spawning in the spring and autumn spawning seasons. Gametogenesis occurs through austral winter and early spring prior to the spring spawning (October/November), when water temperatures are cooler and days are shorter. Conversely, gametogenesis occurs through summer prior to the autumn spawning (March/April), when water temperatures are warmest (potentially stressfully warm), the days are longest, and tropical cyclones occur. Both spring and autumn spawning correspond with seasonal minimums in wind speed26,27. Within the thermal tolerance limits of the coral, warmer water temperatures and longer days theoretically increase energy availability for reproductive processes through increased metabolic activity and elevated photosynthesis28,29. Despite the different environmental conditions through gametogenesis, there were no seasonal differences in fecundity and eggs size observed in the biannually spawning Acropora corals studied here. There are several possibilities for the lack of seasonality observed in reproductive output. Firstly, fecundity and egg size varied widely within species, which confounded inferences about whether reproductive output was higher in a particular season. Other studies have similarly reported high variability, particularly in fecundity. Fecundity can vary widely with season22,30 and between years31, but there is also high variation between colonies, within a single colony22, with colony age30 and between colonies at different depths13. Fecundity can also vary in response to stressors13, however, there was no evidence of environmental stress, such as damaging waves from cyclones or heat stress causing coral bleaching32, before or during the period when samples were collected for this study. Adaptive plasticity in egg size (in response to conditions parents are exposed to), is discussed further below. Secondly, Scott Reef is situated in the tropics (14°S) with relatively small seasonal variations in temperature and day length, and has a light regime that is affected by high cloud cover during the summer cyclone season. Water temperatures are 2–4 °C cooler in the winter months leading up to spring spawning than in the summer months prior to autumn spawning. Day length is 1–2 h shorter in winter compared to summer, however summer cyclones and rainfall mean that overall sunshine hours are higher in the winter months. Consequently, there are cooler temperatures with more sunshine hours in the months leading to the spring spawning and warmer temperatures with less sunshine hours in the months leading to the autumn spawning, which may result in comparable available energy for reproduction during both spawning events. Thirdly, seasonal differences in environmental conditions may indeed drive some seasonal differences in energetics, but these could be channeled into other life history processes, such as calcification12,33, rather than fecundity and egg size. Variation in available energy may also affect egg quality rather than size or number. For example, in other invertebrates (greenlip abalone), while the size of the eggs do not increase, the density of protein and lipids increase throughout the spawning season34 and may indicate an increase in the quality over size of the egg. However, a study on the reef-building coral Montipora capitata, reported stable egg quality (lipids and antioxidants) regardless of the environmental conditions the parent colonies were exposed to, although egg sizes were not presented in this work35. The higher polyp fecundity in spring observed in A. microclados may have been an adaptive response to cooler (less favourable) conditions in spring. That is, an increase in parental investment to increase survival in less favourable conditions36. Alternatively, more sunshine hours during winter gametogenesis may have provided additional energy to produce more eggs in this species.
Early work on egg size and number of eggs suggests a simple trade-off model. That is, assuming resources for reproduction are limited, then an increase in gamete size should result in a reduction in the number of gametes37. Correspondingly, earlier studies of different coral species, genera and morphologies reported an inverse relationship between coral egg sizes and the number of eggs (fecundity)21,22,23, also suggesting that energy is channelled to either fewer large eggs or many small eggs19,20. However, in these cases, the reductions in fecundity with egg size among genera were attributed to the differences in polyp morphology (and sometimes reproductive mode i.e. brooder vs spawner). That is, differences in polyp size and structure can also affect egg size and fecundity38,39 independently of energetics. In our between species comparison, we did not see an inverse relationship between egg size and number of eggs (Fig. 3), but there were also no large differences in corallite size for the seven Acropora species studied here (see Supplementary Table S4 for corallite sizes of our species). However, it is important to note that the differences in reproductive mode and morphology (including polyp structure and size) between genera and species, interferes with the egg size versus number of eggs comparison in the context of a trade-off model. In order to determine if there is a trade-off between egg size and number of eggs, we need to look at individuals within a species. That is, do individuals with large eggs have fewer eggs than individuals with smaller eggs of the same species? We have been unable to locate any other dataset providing a within species comparison. Our study demonstrates that there is no direct relationship between egg size and fecundity, within these species of Acropora, and suggests that there is more than just a simple trade-off in resources influencing these measures.
Egg size has been shown to be a phenotypically plastic trait, regulated by the conditions the parent colony is exposed to. For example, a study on the broadcast spawning ascidian, Styela plicata, demonstrated that parents maintained at high densities produced smaller eggs, presumably reflecting the higher sperm concentrations expected at high adult densities, and therefore reduced requirement for a large target40. While the study was unable to measure the number of gametes, and provide an egg size versus number of eggs comparison, it did suggest that egg size is an adaptive plastic response, rather than a simple energetic constraint. Several studies have also reported varying effects of stress on the number and size of eggs. Under temperature stress sufficient to cause bleaching, corals within the same species can produce either fewer eggs (and maintain size) or smaller eggs (and maintain numbers) depending on their zooxanthellae clade and lipid levels15. Corals exposed to elevated nutrients levels also adjusted their reproductive output, with nitrogen reducing both egg size and number of eggs, and phosphorus producing smaller, but more eggs41. Furthermore, when coral colonies are transplanted to different latitudes, they adjust their egg size to be similar to local colonies. A transplant study conducted in Taiwan reported that coral colonies transplanted to higher latitudes and cooler waters, developed larger eggs, similar to local colonies, as an increased investment response to unfavourable conditions36. This phenotypic plasticity may allow for a type of maternal ‘bet-hedging’, where parents increase within clutch variation in offspring phenotype in response to unpredictable environmental conditions42. The results of our study showed high within species natural variability, but this variability was not consistent with the trade-off model. That is, while there may have been both large and small mature eggs within a species, the large eggs did not necessarily correspond with fewer eggs in a polyp. Within species size variation amongst offspring has traditionally been underestimated43, however, since offspring size can affect dispersal potential, producing a range of sizes, could spread offspring through a range of habitats, thereby spreading the risk of reproductive failure44.
It is often assumed that if resources are limited for reproduction, then an increase in egg size should result in a reduction in the number of eggs37. However, there are no datasets directly comparing egg size and number within coral species. We have shown that in seven Acropora coral species this trade-off between size and number did not occur. We also did not see any seasonal differences in these measures. We recorded high natural variability in both mature egg size and fecundity, a factor that should not be overlooked when using these measures to gauge or compare reproductive output (e.g. between seasons, years, locations). Since egg size and fecundity are affected by parent colony energy reserves, energy allocation to a range of other life history processes (e.g. growth and repair), polyp size and morphology, responses to environmental conditions, and the interaction of these factors, it is unlikely that there is a simple trade-off between size and number of eggs. It is also unlikely that these measures are constrained only by energetics, given the adaptive phenotypic plasticity reported in other studies36, 40. Furthermore, parental investment can come in the form of increased egg quality (e.g. lipids or antioxidants), rather than size or number of eggs. More research into coral energetics, natural variability, and adaptive plasticity is required to determine the mechanisms behind some of the patterns we observed, but our study doesn’t support a simple trade-off model in coral reproduction.
Source: Ecology - nature.com
