(This article is part 2 in a series about coral spawning research. If you’re interested, read part 1 - “Spawning the Future of Caribbean Coral Reefs” - here!)
A healthy reef with a variety of hard coral species off the coast of Bocas del Toro, Panama. Few reefs in the Caribbean remain this healthy.
Coral reefs worldwide are under threat from multiple stressors including ocean warming, ocean acidification, nutrient pollution, and overfishing – just to name a few. To combat the decline of coral cover, scientists and citizens have established active reef restoration programs that act as coral “farms”, growing and propagating corals in nurseries before outplanting them onto degraded reefs. However, the majority of these programs propagate corals through asexual reproduction – fragmentation of an adult colony to create multiple new, genetically identical colonies – a strategy which alone may not maintain diverse, resilient populations because it doesn’t introduce novel genetic information or alternative allele combinations. In order to capture adequate genetic variation to maximize diversity and survival in the face of changing oceans, it is important for restoration practitioners to incorporate sexual coral reproduction into their efforts.
A Pseudodiploria strigosa colony spawning off the coast of Eleuthera in the Bahamas.
Hence, the significance of researching and taking advantage of coral spawning events to generate hundreds of thousands of new coral individuals, each with their own unique genetic information. This is exactly what the research team at SECORE International is pioneering with a variety of scleractinian (hard coral) species throughout the Caribbean. The corals that the SECORE raises and outplants will inject much-needed diversity into the region’s struggling coral populations, hopefully enhancing their ability to respond to changing environmental conditions.
Why do we interfere at all? Why don’t we just let the corals reproduce in the wild without putting all this time, money, and effort into collecting their gametes, caring for coral larvae, and raising baby corals?
The short answer is that of the billions of gametes released during mass spawning events and the millions of larvae produced, very, very few offspring make it to maturity. Several population bottlenecks exist during the early life stages of corals, resulting in high mortality and preventing sexual reproduction from quickly enhancing coral cover on struggling Caribbean reefs.
Gamete bundles (eggs and sperm packaged together) accumulate in the top of a collector net as they waft upwards through the water column. The bundles will soon break apart into separate egg and sperm cells, and researchers will mix them with gametes of other colonies for fertilization.
Fertilization
Although corals release billions of gametes during mass spawning events, relatively few of them are actually fertilized. Many predators roam the reefs on spawning nights, picking off the nutritious, energy-rich gamete bundles that polyps release or gobbling them in bulk when they aggregate at the surface. On top of predation risk, sperm has to be in a very particular concentration for fertilization to occur. In the vast three-dimensional space of the ocean, this is part of the reason corals have evolved to release their gamete bundles in such synchrony, to give their gametes a better chance of reaching the proper concentration and fertilizing each other (Oliver & Babcock, 1992).
O. faveolata eggs under a microscope, about 10 hours after collection. The fuzzy/bumpy ones are fertilized embryos that have begun the process of cell division, while the smooth, round ones are unfertilized eggs.
Achieving the proper sperm concentration in the wild is becoming even more challenging on degraded reefs due to the “Allee effect”, a decline in individual fitness when population size or density is low. In this case, the “decline in individual fitness” manifests as a failure to mate successfully; with greater distance between colonies comes lower fertilization (Teo & Todd, 2018). Decreasing coral cover throughout the Caribbean is likely reducing the number of spawning colonies in a given area, thus diluting the concentration of gametes and inhibiting fertilization. Because many Caribbean species are simultaneous hermaphrodites that produce both eggs and sperm, self-fertilization is possible. However, crossing eggs and sperm from the same colony results in lower fertilization rates and less genetic diversity than crossing gametes from two different colonies (Heyward and Babcock, 1986). Thus, colonies of different genotypes need to be relatively close together on a reef to produce maximally viable offspring (Teo & Todd, 2018). Finally, climate change is predicted to directly impact fertilization success. Studies have shown that increased temperature and ocean acidification reduce fertilization success (Negri et al., 2007; Albright & Mason, 2013).
A few hours after collecting them from the wild, I examine the coral gametes for newly-formed embryos. Photo: Paul Selvaggio
To help mitigate these fertilization challenges, researchers can (1) collect gametes as they are released to prevent predation; (2) concentrate collected sperm to maximize successful fertilization; (3) control fertilization by separating eggs and sperm as bundles break apart, then selectively crossing gametes from different colonies, thus yielding higher fertilization and greater genetic diversity than self-fertilized offspring (Heyward and Babcock, 1986); and (4) control temperature and pH of seawater to ensure optimal conditions for fertilization.
A 3-day-old, swimming Diploria labyrinthiformis larva under a microscope.
Larval (pelagic) stage
Of the eggs that are successfully fertilized in nature, only a small fraction will survive the several days to weeks they spend floating and swimming in the water column as larvae (Graham et al., 2008). As part of the plankton, these tiny larvae are vulnerable to predation by other zooplankton and filter-feeders. Also they can actively swim after a few days, pelagic coral larvae are primarily at the whim of ocean currents and winds, so they might get swept into unsuitable habitat. For instance, suspended sediments in the water column significantly reduce larval survival (Gilmour, 1999) so being transported to an area with high turbidity and sedimentation could result in high mortality. Furthermore, parents may not provision each gamete with equal energy reserves (Gagliano and McCormick, 2007), meaning that the less-provisioned larvae will likely lack the energy reserves to survive until settlement (Graham et al., 2008).
To enhance the survival of coral larvae, researchers can keep them in carefully controlled, closed or semi-closed systems to (1) eliminate predators and (2) maintain optimal environmental conditions for survival.
Newly-settled coral recruits on the sea floor are highly vulnerable to predation or out-competition due to their small size and relatively slow growth.
Settlement
One-month-old Orbicella faveolata recruits fluorescing under violet light. The red dots are the algal symbionts living in their tissues.
Once it comes time for larvae to select their permanent homes and settle onto the ocean floor, they need to identify suitable substrate to settle on. Hardbottom reef substrates of limestone with crustose coralline algae (CCA) are preferable – sandy, muddy, or grassy bottoms are not. Happening upon the correct substrate type requires some luck, because the swimming larvae have traveled with the ocean currents during their time in the water column. If they cannot find an appropriate place to settle by the time their energy reserves run out, they will not survive (Graham et al., 2008). Coral larvae cannot settle on macroalgae, which are increasing in abundance on many reefs worldwide primarily due to overfishing of herbivores and nutrient loading (Hughes et al., 2007). As such, areas that may have served as suitable substrate in the past may now be colonized by macroalgae, reducing the space available to larvae for settlement (Mumby et al., 2007). Many factors in nature have been shown to reduce settlement rates and interfere with selection of appropriate substrate type, including low seawater pH (Albright et al., 2010) and suspended sediments and accumulated sediments (Gilmour, 1999).
Five-month-old Orbicella faveolata recruits from Eleuthera in the Bahamas. As larvae, they settled on one of the pre-conditioned ceramic plugs that I provided in their tanks.
To increase the likelihood of larvae locating suitable substrate when they are ready to settle, researchers can rear them in closed systems - such as laboratory tanks or inflatable in-water pools (see photos below) - with optimal conditions until they are ready to settle. In the closed systems, researchers can then provide 3D-printed substrates or terra-cotta tiles that have been preconditioned with reef biofilm or crustose-coralline algae (CCA) to attract larvae. Once they have settled and metamorphosed, the coral juveniles can be transferred to local reefs on their substrates in controlled recruitment efforts (dela Cruz and Harrison, 2017). Alternatively, researchers can release large quantities of ready-to-settle larvae over appropriate substrate on the reef to boost natural recruitment (dela Cruz and Harrison, 2017). Indeed, experiments have shown significant increases in settlement to reefs when larvae are reared in a controlled system and given appropriate substrates to settle on (Heyward et al., 2002).
Coral researchers in the Bahamas setting up the in-water pools (designed by SECORE International) that will soon host swimming coral larvae. Photo: Paul Selvaggio
Coral researchers hold pre-conditioned, 3D-printed substrates (designed by SECORE International) upon which coral larvae will settle. Photo: Paul Selvaggio
In summary, our intervention enhances fertilization, ensures the creation of new genetic diversity, increases larval survivorship, and boosts settlement success. Raising coral juveniles without the risk of predation, competition, or environmental stress will hopefully get them through the bottleneck of extremely high mortality that occurs in the wild, thus maximizing survival, growth, and the impact they can make for conservation and restoration efforts (Quigley et al., 2018). These efforts require a LOT of time, money, and manpower, but since genetic variation is arguably the fuel of resilience and sexual reproduction has the potential to create thousands to millions of new coral individuals with distinctive genetic material, we feel it is worth the investment to give them the very best chances at survival that we can.
Acropora coral recruits growing on pre-conditioned, 3-pronged substrates created by SECORE International. Photo: SECORE International (www.secore.org)
My research
My research is also focused on helping juvenile corals through this survival bottleneck. My focus is on the stage immediately after settlement, when recently-metamorphosed larvae – no called “recruits” – are fixed to the benthos, begin growing tentacles, and begin to grow and establish themselves as new colonies.
One-month-old Orbicella faveolata recruit under a microscope. The brown dots are the algal symbionts living in its tissues.
Even after corals settle successfully and metamorphose into polyps (at which point they are called “recruits”), they experience high post-settlement mortality. As tiny recruits, they are vulnerable to predation or damage from grazers as they scrape the benthos. Macroalgae, sponges, or any number of encrusting benthic organisms that grow more quickly than they do may smother them. Additionally, increased CO2 under climate change is predicted to reduce juvenile growth rates (Albright et al., 2010), further limiting their ability to establish themselves on a reef without being outcompeted.
Finally, most broadcast spawning corals are born during the warmest months of the year, increasing their chances of experiencing high temperatures that might lead to bleaching or mortality as recruits.
Since coral spawning and settlement in the Caribbean happen in the summer months and thus coincide with the warmest ocean temperatures of the year, and because corals in their early life stages are particularly vulnerable to environmental stress and high mortality, it is important to understand how coral juveniles might become more thermally tolerant from the start.
Orbicella faveolata recruits fluorescing under violet light. The red areas are colonized by algal symbionts in the family Symbiodiniaceae.
Most Caribbean corals take up new algal symbionts (single-celled dinoflagellates in the family Symbiodiniaceae) through “horizontal” transmission; instead of coral parents furnishing their larvae with symbionts before releasing them, each new generation of recruits acquires symbionts from the environment around them upon settlement to the reef. Warming ocean temperatures may favor initial uptake of the thermally tolerant symbiont Durusdinium trenchii (Abrego et al., 2012), although this process is not well studied in Caribbean coral recruits. In adult corals, mass bleaching events have D. trenchii has been shown to increase bleaching thresholds by 1-2°C (Berkelmans & van Oppen, 2006). Moreover, nearby adult corals may influence symbiont availability by continuously discharging symbionts into the environment (Hoegh-Guldberg & Smith, 1989), where they may persist in the sediments and water column (Cunning et al., 2015) and increase the rate of symbiont acquisition by newly settled recruits (Nitschke et al., 2016). Therefore, as thermotolerant symbionts like D. trenchii become more prevalent on reefs due to increasingly frequent mass bleaching events, they may create a positive feedback mechanism that pushes symbiont assemblages on entire reefs – symbiont “metacommunities” - and accelerate symbiont community changes at the ecosystem level. Such reef-wide dynamics could have significant implications for coral fitness, reef resilience, and response to climate change.
These Orbicella faveolata recruits are just starting to acquire their algal symbionts. The brownish rings around their mouths and tentacles show where the algae first start to colonize their previously symbiont-free tissues.
Experimental aquaria where I raise newly-settled coral recruits and expose them to different temperature and symbiont availability treatments.
Since beginning my Ph.D. in August 2017, I have been evaluating metacommunity feedbacks in coral symbiosis ecology by studying whether differences in the local availability of different types of Symbiodiniaceae influence the composition of symbiont communities populating juvenile corals. Focusing on key reef-building species including Orbicella faveolata (mountainous star coral) and Diploria labyrinthiformis (grooved brain coral) collected from various sites across the Caribbean with teams from SECORE and NOAA’s coral research group, I have conducting symbiont uptake experiments in the presence of adult corals with different symbiont assemblages in order to quantify the degree to which the existing symbiont metacommunity on a reef influences the uptake and establishment of symbiosis in coral recruits. Specifically, I have raised recruits in close proximity to adult coral fragments dominated by D. trenchii in order to enhance the initial uptake of this thermotolerant symbiont, thus increasing recruits’ bleaching thresholds and their chances of surviving heat stress early in their lives. My goals are (1) to elucidate potential intergenerational feedbacks that may drive the future trajectory of coral symbiosis ecology in the Caribbean and (2) test a method of increasing thermal tolerance from the beginning of a coral’s life to reduce post-settlement mortality.
To collect data on which symbiont types a recruit is hosting, I have to sacrifice it with a razor blade. A single recruit - approximately 1 millimeter in diameter - is on the end of the razor blade above.
If I find that D. trenchii increases the thermal tolerance of coral recruits like it has been shown to do in adults corals, restoration practitioners that use sexually-produced recruits (like SECORE) may choose to rear recruits in close proximity to D. trenchii-dominated adult colonies, boosting the thermal tolerance of recruits before outplanting them onto the reef.
Diploria labyrinthiformis recruits under normal light.
The same Diploria labyrinthiformis recruits fluorescing under violet light.
Conclusion
Ultimately, the goal of restoration practitioners is to increase the resilience of struggling reefs, so that corals will persist as they face many stressors including ocean warming, ocean acidification, disease, pollution, and overfishing. In my opinion, sexual reproduction provides the best chance of increasing reef resilience by creating and fostering genetic diversity that strengthens the potential for adaptation and population recovery. That’s why it’s so important to “start them young”, to maximize the survival of coral gametes, larvae, and recruits and ensure that the next generation of corals will be robust to whatever the world throws at them.
-Liv
Five-month-old O. faveolata recruits from the Bahamas on a ceramic plug.
(All photographs provided by Liv Williamson unless otherwise noted.)