By creating complex 3-dimensional calcium carbonate frameworks, reef building corals support the most productive and biologically diverse marine ecosystems on Earth. Coral reefs are not only a critical habitat for a wide variety of species, but also provide indispensable ecosystem services for millions of people (Burke et al., 2011). Despite their great importance, coral reefs are facing significant challenges due to human activities (e.g., pollution, overfishing, and the physical destruction of reefs) (Burke et al., 2011). In addition, changes in environmental features determined by ocean warming and seawater acidification are seriously threatening the survival of entire coral reef ecosystems (Hoegh-Guldberg et al., 2017). Coral losses are particularly pronounced on shallow water reef systems, where corals and their dinoflagellate symbionts live close to their physiological thermal maximum, and as a result, warming of 1°C or more can significantly reduce their fitness and cause whole-colony mortality (Hoegh-Guldberg, 1999; Jones, 2008). However, coral reefs extend far beyond the well-studied shallow reef zones into Mesophotic Coral Ecosystems (MCEs) ranging from 30 m depth down to depths potentially greater than 170 m (Hinderstein et al., 2010; Rouzé et al., 2021). In the last few years, MCEs have gained significant interest as they appear not to have experienced the same trend in coral decline as their shallow-water counterparts, displaying relatively stable coral populations over time (Bak et al., 2005). Thus, it is hypothesized that MCEs may act as refugia for corals, serving as potential sources to reseed shallower reefs through larval exchange and thereby increasing overall reef resilience [termed the Deep Reef Refugia Hypothesis “DRRH”; (Bongaerts et al., 2010; Lesser et al., 2018)].

Resilience of ecosystems under rapid environmental change relies, in part, on the capacity of organisms to adapt and/or acclimatize to new conditions. From shallow to mesophotic depths, wide variations in light intensity shape different physiological, morphological and gene expression patterns in both the coral and the algal symbiont (Mass et al., 2007; Einbinder et al., 2016; Goodbody-Gringley and Waletich, 2018; Martinez et al., 2020; Malik et al., 2021). For instance, differences in photosynthetic efficiency have been observed in the algal endosymbionts between shallow and mesophotic corals (Bongaerts et al., 2011). Moreover, coral larvae and recruits from different light environments significantly differ in size (Turner et al., 2018; Scucchia et al., 2020) and possess differential recruitment patterns (Turner et al., 2018). These wide variations among conspecifics are recurrently suggested to result from plasticity in response to differing environmental conditions at depth, such as light intensity changes (Goodbody-Gringley and Waletich, 2018). Nevertheless, there is still limited knowledge of the physiological and morphological contributors that underlie such plasticity, particularly in early life stages. This reduces our capacity to adequately assess the ability of mesophotic larvae to survive under higher light intensities and replenish shallower reefs.

If MCEs are in fact an important lifeboat for coral survival, it is imperative to evaluate the degree of physiological plasticity of coral larvae that would enable them to successfully migrate and settle across wide depth gradients, as successful settlement is fundamental to coral population dynamics as well as reef community structure (Piniak et al., 2005). We assessed this plasticity in the reef-building coral Porites astreoides, a hermaphroditic, brooding species (Brazeau et al., 1998) that inhabits large environmental clines (Elizalde-Rendón et al., 2010) and exhibits high phenotypic plasticity at various life stages (Green et al., 2008). This Atlantic coral is common throughout the Caribbean and Western Atlantic with a broad depth distribution, ranging from 0 to 50 m (Fricke and Meischner, 1985; Chornesky and Peters, 1987). In Bermuda, P. astreoides is a main contributor to reef community structure and is ubiquitously distributed across the lagoon and rim reef zones, with relative frequency decreasing with increasing depth beyond 20 m (Fricke and Meischner, 1985; de Putron and Smith, 2011; Goodbody-Gringley et al., 2019). Due to the high levels of fecundity and settlement success, P. astreoides is considered a resilient species (Bak and Engel, 1979; Chornesky and Peters, 1987). Additionally, variable bleaching responses and different host gene expression patterns between inshore and offshore populations exposed to heat stress suggest that P. astreoides may be able to acclimatize or adapt to thermal stress (Kenkel et al., 2013a,b; Wong et al., 2021). Across a depth gradient, this species was also found to have similar thermal tolerance ranges, despite variable thermal histories, suggesting high levels of plasticity to temperature (Gould et al., 2021). Consequently, P. astreoides is expected to increase in relative abundance compared to other Atlantic scleractinian species (Green et al., 2008), and is therefore an ideal study species as it will likely be an important contributor to the future community composition of Caribbean and Western Atlantic reefs. Importantly, this species was also found to maintain high degrees of genetic connectivity in Bermuda across inshore and offshore sites that ranged in depth from 4 to 26 m (Serrano et al., 2016), and multiple studies have described Symbiodinium spp. [ITS2 type A4; (LaJeunesse et al., 2018)] as the dominant symbiont in P. astreoides in Bermuda (Venn et al., 2006; Serrano et al., 2016; Zhang et al., 2016; Reich et al., 2017). Thus, there is strong support for host and symbiont homogeneity in Bermuda across depths enabling comparisons of phenotypic response to environmental conditions.

In this study, we examined physiological and morphological characteristics of P. astreoides larvae released from shallow (8–10 m) and mesophotic (45 m) adults and, through a reciprocal ex situ transplantation experiment, we assessed differences in survival, settlement patterns and size among recruits depending on settlement light conditions. With this approach, we elucidated the mechanisms underlying the plasticity of P. astreoides early life stages that enables them to survive across broad depth gradients. The existence of such plasticity increases the probability of effective connectivity between shallow and mesophotic depths, ultimately advancing our understanding of these ecosystems and the potential for MCEs to serve as refugia.

The persistence of coral reefs under global environmental change is built upon larval survival and settlement success. Evaluating the phenotypic diversity and plasticity of coral larvae is fundamental to understand their range of environmental tolerance. P. astreoides larvae originating from shallow and mesophotic corals show clear differences in physiological and morphological traits, likely stemming from adaptation to different light environments experienced during the brooding period. Larvae released from mesophotic colonies have significantly lower respiration rates per unit biomass than those derived from shallow colonies (Figure 3). Decreased coral respiration rate appears to be linked to lower availability of photosynthetically fixed carbon at light-limited mesophotic depths (McCloskey et al., 1984). Low metabolic rates of coral larvae are proposed to significantly extend dispersal potential, enhancing population connectivity (Graham et al., 2013). Likewise, a larger larval size allows for longer planktonic periods, enabling coral larvae to disperse farther (Isomura and Nishihira, 2001; Hartmann et al., 2013; Chamberland et al., 2017). In this study, larvae released from mesophotic colonies were found to be significantly larger than those released from shallow colonies (Figure 2), which suggests higher content of energetic resources in larvae of mesophotic origin, as larval size often correlates with energetic content in the form of maternally derived lipids (Wendt, 2000; Hartmann et al., 2013; de Putron et al., 2017). Active swimming represents the major energetic cost during marine invertebrates’ larval stages (Marshall and Keough, 2003), and in coral larvae this energy may be acquired from lipid catabolism (Harii et al., 2007). In addition, lipids within coral larvae are used for buoyancy and as an energy source to sustain longer periods in the plankton (Harii et al., 2007; Figueiredo et al., 2012). Considering that phytoplankton availability and light-dependent productivity markedly decrease with depth (Lesser et al., 2010), a high content of maternally derived lipid stores could significantly support metabolic requirements of mesophotic larvae. Collectively, these observations suggest that P. astreoides larvae of mesophotic origin possess a greater dispersal potential compared to their shallow counterparts. In fact, as previously hypothesized for P. astreoides larvae in Bermuda, the smaller size of shallow larvae may infer a shortage of energetic reserves, which could lead to lower rates of competency and survival (de Putron et al., 2017; Goodbody-Gringley et al., 2018). However, P. astreoides larvae acquire Symbiodinium through vertical transmission, enabling direct translocation of photosynthate as an energy source that can likely sustain the higher metabolic rates of shallow larvae (Putnam and Gates, 2015). Further examinations of larval lipid content and stable isotopes to determine rates of reliance on heterotrophy versus autotrophy in larvae from differing parental depths may help elucidate variations in larval duration and dispersal potential.

Larvae in the water column can change buoyancy in response to light intensity, in order to maximize the chance of finding the substratum at the optimal depth for recruitment (Mundy and Babcock, 1998). This indicates that the light environment varying with depth is a crucial element controlling the survival and successful settlement of coral larvae. In this study, P. astreoides larvae of both shallow and mesophotic origin exhibit the potential to adjust to wide differences in light intensity, by displaying the capacity to survive and successfully settle under reciprocal light settlement conditions (Figure 4). Furthermore, their phenotypic plasticity allowed larvae of both shallow and mesophotic parental origin to develop differential juvenile size based on the light environment encountered upon settlement (Figure 5).

Coral depth distribution largely correlates with light gradients and is highly influenced by the differing light tolerance and photosynthetic properties of their endosymbiotic algae (Iglesias-Prieto et al., 2004; LaJeunesse et al., 2004). Previous studies on the same species in Bermuda found that while densities of zooxanthellae cells within larvae of upper-mesophotic origin (30 m) were higher than those of shallow inshore patch reef origin (5 m), zooxanthellae densities did not differ between larvae from upper-mesophotic and rim reef origin (10 m) (Goodbody-Gringley et al., 2018). The ability of P. astreoides larvae to successfully adjust to differing light environments observed in this study, therefore, might stem from the endosymbionts’ photo-acclimatory potential. In fact, corals hosting symbionts in the genus Symbiodinium (formerly clade A; LaJeunesse et al., 2018), which is the dominant type in P. astreoides in Bermuda across depths (Venn et al., 2006; Serrano et al., 2016; Zhang et al., 2016; Reich et al., 2017), have been shown to possess high resistance to light variations (Reynolds et al., 2008) and to be less susceptible to bleaching (Warner et al., 1999). In addition, Symbiodinium spp. symbionts abundantly produce UV-protective amino acids that prevent damage to the photosynthetic apparatus due to changes in light intensity (Banaszak et al., 2006). The colonization of a wide range of light environments may not only be determined by the endosymbionts’ photosynthetic plasticity, but also from the ability of corals to modulate their tissue light field by either filtering out excess light that can be harmful to the algae (i.e., in high-light conditions), or by increasing the photon flux reaching the algae (i.e., in low-light conditions) (Lichtenberg et al., 2016). As such, a combination of host-symbiont phenotypic plasticity might be at the root of the capacity of P. astreoides larvae to colonize highly different light environments.

Overall, low light conditions appear to promote both higher survival and settlement of P. astreoides larvae (Figure 4). Under shallow light conditions, larvae from shallow adults experienced lower survival and settlement success compared to those from mesophotic adults, in accordance with previous observations by Goodbody-Gringley et al. (2018). Coral recruitment is known to be influenced by several physical characteristics varying with depth, with light representing one of the most critical factors (Babcock and Mundy, 1996; Mundy and Babcock, 1998). Sufficient light quality and intensity are required for photosynthesis, however, at shallow depths, light levels may be too high for young coral settlers (Gleason and Hofmann, 2011) leading to settlement in more cryptic sites (Babcock and Mundy, 1996). In addition, larval settlement is significantly influenced by recruit density, with fewer larvae settling in preferred locations as density increases (Cameron and Harrison, 2020). Thus, if larval densities are too high, cryptic and shaded space availability might be limited, leading to fewer larvae settling. As such, the higher density of larvae in the shallow settlement chambers may have negatively affected settlement success. However, this is unlikely as previous experiments using similarly sized chambers and available substrate with equal larval densities found analagous results, with higher settlement by upper-mesophotic larvae compared to shallow larvae (Goodbody-Gringley et al., 2018). Larval settlement is also documented to be driven in part by the benthic community, specifically the presence of crustose coralline algae (Morse et al., 1988; Ritson-Williams et al., 2009) and a bacterial film (Sneed et al., 2014). Shlesinger and Loya (2021) found that substrate type significantly influenced settlement choice by shallow and mesophotic larvae in the Red Sea, where larvae preferentially settled onto tiles conditioned at the corresponding depth of parental origin. Settlement tiles used in the present study, however, were all conditioned in a common garden environment on a nearshore shallow patch reef where conditions did not directly correspond to either site of parental origin, thereby reducing potential effects associated with tile conditioning.

Recruitment success of lecithotrophic coral larvae is largely influenced by larval size, with smaller larvae (i.e., less energetic reserves) translating to lower competency and survival (de Putron et al., 2017), and lower recruit sizes leading to decreased post-settlement survivorship (Raymundo and Maypa, 2004). Collectively, our results indicate that offspring quality and settlement success are deeply interconnected, and show an increase in larval fitness with increasing reef depth and decreasing light. These results suggest that differential quality of larvae released from shallow and mesophotic adults may be related to latent effects of parental history. For many animals, the environment experienced by parents influences the phenotype and fitness of their offspring, in a process known as “parental effects” (Marshall, 2008; Badyaev and Uller, 2009; Torda et al., 2017). Such parental effects influence the development of coral larvae and the recruits’ fitness (Dixon et al., 2015; Kenkel et al., 2015; Quigley et al., 2016; Putnam et al., 2020; Wong et al., 2021). Therefore, the increased performance of mesophotic offspring observed in this study may be due to the higher stability of environmental conditions experienced by mesophotic parental colonies during the brooding period, compared to consistently higher temperatures experienced by the adults on shallow reefs (Figure 1; Goodbody-Gringley et al., 2018). Furthermore, shallow reefs in Bermuda are more likely impacted by anthropogenic activities (Smith et al., 2013), which can also reduce the fitness of shallow adult colonies. Parental effects have been indicated as major factors limiting coral larval dispersal across depths as larvae may be adapted to the conditions experienced by their parent (Shlesinger and Loya, 2021), however, our findings show that offspring plasticity also plays a crucial role in shaping coral capacity to colonize differing environments. Yet, the density of adult P. astreoides colonies on shallow and mesophotic reefs in Bermuda does not reflect a pattern of increased recruitment to mesophotic depth, as adult colony frequency is documented to decrease with increasing depth (Fricke and Meischner, 1985). This apparent disconnect may be related to post-recruitment mortality and the adaptive potential of individual settlers, which were not assessed in this study. Future studies that follow post-recruitment survival in situ and examine variations in genomic responses through early life history stages at differing depths may better elucidate the mechanisms underlying these discrepancies and potential influences of parental effects.

A greater dispersal potential combined with the ability to survive and settle under a range of light conditions indicates that P. astreoides larvae from mesophotic reefs are likely capable of reseeding shallow reefs in Bermuda, thereby supporting the Deep Reef Refugia Hypothesis. Importantly, the higher settlement success of mesophotic larvae under shallow light conditions compared to shallow larvae under mesophotic light conditions suggests that recruitment may preferentially occur up the slope (mesophotic to shallow) rather than down the slope (shallow to mesophotic). These results oppose previous observations of asymmetric gene flow (Prada and Hellberg, 2013; Serrano et al., 2014; Bongaerts et al., 2017) and larval settlement patterns (Shlesinger and Loya, 2021) occurring from shallow to deeper reefs. Nevertheless, the higher reproductive success observed for mesophotic corals in the Western Atlantic (Holstein et al., 2015; Goodbody-Gringley et al., 2018) and subsequent larval effective recruitment found in the present study suggest that mesophotic reefs likely represent a significant source of propagules across the depth gradient and may aid in the recovery of degraded shallow reefs in Bermuda. Thus, mesophotic corals appear to be important contributors to the resilience of Bermuda’s reef ecosystems, which highlights the importance of establishing management strategies aimed at protecting mesophotic reefs. Future research assessing larval dispersal potential and recruitment success in situ is warranted to provide accurate data on population dynamics for mesophotic and shallow corals. Such studies will inform effective management of the ecological functions and ecosystem services provided by connected coral reef communities.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

GG-G and TM designed and conducted the research. HN, GG-G, SM, SE, AC, and TM performed the underwater collection and ex situ experiments. RJ carried out the respiration experiments. GG-G, FS, and TM wrote the manuscript. All authors contributed to improving, revision, and approval of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.