Polyp bailout in Pocillopora damicornis following thermal stress

Introduction

Coral reefs around the world are facing increasingly frequent acute thermal stress events (Ainsworth et al., 2016; Hughes et al., 2017). As such there has been a corresponding increase in research into how corals respond to high temperatures, how these responses vary within individuals and communities, and how variation influences the resilience, recovery and structure of coral communities. Understanding this variation helps predict patterns of bleaching-induced mortality and reef-wide degradation. As the possibility of frequent, severe bleaching events increases (van Hooidonk et al., 2016), it is important to understand the drivers of variability in order to improve management and target restoration efforts. Polyp bailout is a possible source of variation that may influence the survival of individual genotypes and recruitment at local scales.

Polyp bailout has been observed in at least six species of scleractinian coral (Serrano et al., 2017) and involves the withdrawal of individual polyps from the coenosarc followed by their detachment from the skeleton (Sammarco, 1982). The detachment of individual polyps from a parent coral colony has previously been recorded in response to poor water quality (Sammarco, 1982; Serrano et al., 2017), large changes in pH (Kvitt et al., 2015), changes in salinity (Shapiro et al., 2016) and following competition from macroalgae (Sin et al., 2012). As polyps often retain their endosymbiotic dinoflagellates (zooxanthellae) and are able to re-settle, polyp bailout is thought to be a generalised escape response from detrimental conditions (Kvitt et al., 2015; Sammarco, 1982). It may therefore constitute rapid migration away from local sources of mortality.

Despite increasing temperatures being arguably the most significant threat to coral reefs (Hughes et al., 2017), this response has yet to be described during thermal stress. Here we present the first qualitative observation of polyp bailout following thermal stress in Pocillopora damicornis during an ex situ mesocosm study.

Methods

Fragments of P. damicornis were collected from the Heron Island reef flat in January 2017, from a maximum depth of two metres. They were housed in four 500 litre aquaria as part of an outdoors, semi-closed system supplied by a continuous flow of unfiltered seawater from the reef flat. During the week preceding simulated thermal stress, all fragments were acclimated to the aquaria and subjected to ambient conditions (ca. 7.980 – 8.020 pH; conductivity of 53 – 54 μS/m; temperature of 26 – 30°C; and PAR of 0 – 3875 K). Following this, temperature was gradually increased in two mesocosms on top of natural variation for six days up to a peak daytime temperature of 34°C to simulate a severe bleaching event (as previously reported by Ainsworth et al., 2016). Two control mesocosms continued to be exposed to ambient conditions, differing from treatments in temperature only. Fragments were monitored throughout the day and when polyps were observed to bail out, they were collected using a wide-ended pipette and examined under an Olympus SZX16 stereomicroscope.

Results

On the fifth day of the simulated bleaching event, polyps were observed to begin bailing out at approximately 09:30 (Figure 1; Dataset 1, Fordyce et al., 2017). At this time, peak daytime temperature was 33°C, which is the equivalent of 13 degree heating days, a measure of accumulated heat stress used in the prediction of mass bleaching events. By the end of day six, at peak temperature of 34°C, reflecting 18 degree heating days, all polyps had detached (Dataset 1, Fordyce et al., 2017). At the end of the bailout period, polyps began to detach in sheets rather than as individuals. This suggests that thermal stress was too severe to allow successful withdrawal of all polyps from the coenosarc. In contrast, fragments in the control mesocosms showed no signs of bleaching or polyp bailout (Supplementary Material 1).

Figure 1. Photographs of polyps dropping off the skeleton of Pocillopora damicornis.

Macrophotograph of polyps, having withdrawn from the connective coenosarc, dropping off the skeleton of the fragments of Pocillopora damicornis. Photograph taken with an Olympus Stylus Tough TG-4.

Bailed polyps were slightly negatively buoyant, sinking slowly, but could easily be re-suspended with mild disturbance. The detached, individual polyps retained their zooxanthellae and many were observed to extend coiled mesenterial filaments (as described in Richmond, 1985; Figure 2). Clusters of detached polyps were also observed, however these lacked calcified tissue and so did not resemble the larval clusters described by Richmond (1985) (Figure 2).

Figure 2. Single polyps and clusters of polyps with zooxanthellae and extended filaments.

Micrograph of single polyps and clusters of polyps placed in a glass petri dish, taken using an Olympus SZX16 stereomicroscope with a computer-linked 2.0x objective lens. Total magnification is 17.0x. Small brown dots in the polyp tissue are endosymbiotic zooxanthellae. Coiled filaments are adhesive mesenterial filaments, presumed to aid in rapid settlement.

Implications and future research

In past observations of polyp bailout, corals have been subjected to extreme aquarium conditions such as high salinity (up to 54 parts per thousand; Shapiro et al., 2016), low pH (7.2; Kvitt et al., 2015) or little to no water replacement resulting in anoxic and low nutrient conditions (Serrano et al., 2017; Sin et al., 2012). This makes it difficult to apply these results to the context of natural systems and elucidate the possible role of this response during environmental stress. The present observation was in aquaria with near-natural conditions. The peak daily temperature of 34°C was sustained over several days, reflecting severe thermal stress. However, accumulated heat stress amounted to between two and three degree heating weeks (14–21 degree heating days). This is becoming widely reported during bleaching events on the Great Barrier Reef (Ainsworth et al., 2016; Hughes et al., 2017). Therefore, this observation suggests that polyp bailout can occur in natural reef environments, in response to currently observed temperature increases. For coral species that utilise this response, the present record has implications for coral recruitment and recovery on local scales, and also suggests that these processes can occur independent of sexual reproduction and the impact of thermal stress on reproductive potential.

Detached polyps appear to be viable, able to settle near the parent colony and capable of being dispersed short distances in a reef environment. Sammarco (1982) previously described low (< 5%) settlement and survival rates of detached polyps on settlement tiles contained in jars but survival of individual polyps within a simulated or natural reef environment has yet to be investigated, particularly how it is affected by reef degradation. If polyps were to ‘escape’ into cooler conditions with higher food availability, it may boost their survival and settlement success rates beyond the 5% observed by Sammarco. In the current study, we noted that each parent colony detached a large population of individual polyps (>50 per fragment), showing that even survival of 5% has the potential to allow from some immediate re-seeding of the local reef habitat. Furthermore, an obvious source of nearby refugia are neighbouring reef slope and mesophotic reef environments (Bridge et al., 2013; Smith et al., 2014), down to which these negatively buoyant polyps may slowly sink. However, light attenuation may limit viable settlement depths as individual polyps would need to rapidly acclimate to lower light conditions in order to settle and successfully begin asexual division.

Clearly, extensive future research is needed to explore the survival of individual polyps in both simulated refugia and within the reef habitat following thermal stress events. This will lead to greater understanding of the ecology and wider implications of this stress response and its potential role in coral recruitment and reef recovery following bleaching events. We additionally lack in situ observations of this phenomenon. Time-intensive ecological surveying during a predicted bleaching event is needed to reveal whether this is a widespread response to thermal stress. Subsequent use of mass mark and recapture of coral polyps, tagged with stable heavy isotopes, would then allow the tracking of the fate of coral polyps following bailout. Despite being a well-established response to stress, little research has focused on how polyp bailout may influence the survival and recovery of local coral populations.

Data availability

Dataset 1. Table of qualitative observations of polyp bailout in control and heat-treated mesocosms. Indicated is the peak daytime temperature (± 0.5°C) of the four treated mesocosms, the accumulated heat stress corals are exposed to and any observations during the four day bleaching period, including at the beginning and end of polyp bailout.

DOI, 10.5256/f1000research.11522.d161213 (Fordyce et al., 2017)