Coral reef restoration

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A science dive on coral reefs in Karimunjawa Karimunjawa shallow reef.jpg
A science dive on coral reefs in Karimunjawa

Coral reef restoration strategies use natural and anthropogenic processes to restore damaged coral reefs. [1] Reefs suffer damage from a number of natural and man-made causes, and efforts are being made to rectify the damage and restore the reefs. This involves the fragmentation of mature corals, the placing of the living fragments on lines or frames, the nurturing of the fragments as they recover and grow, and the transplantation of the pieces into their final positions on the reef when they are large enough.

Contents

Background

Coral reefs are important buffers between the land and water and help to reduce storm damage and coastal erosion. [2] They provide employment, recreational opportunities and they are a major source of food for coastal communities. [2] It is estimated that $375 billion dollars come from ecosystem services provided by coral reefs each year. [3]

The most prevalent coral in tropical reefs are the stony corals Scleractinia that build hard skeletons of calcium carbonate which provide protection and structure to the reef. [4] [5] Coral polyps have a mutualistic relationship with single-celled algae referred to as zooxanthellae. These algae live in the tissue of coral polyps and provide energy to the coral through photosynthesis. In turn, the coral provides shelter and nutrients to the zooxanthellae. [4]

Half the world's coral since 1970 have disappeared, and all reefs being threatened with extinction by 2050. [6] In order to ensure the existence of coral reefs in the future, new methods for restoring their ecosystems are being investigated. Fragmentation is the most common strategy for restoring reefs; often used to establish artificial reefs like coral trees, line nurseries, and fixed structures. [7]

Threats to coral reefs

Some anthropogenic activities, such as coral mining, bottom trawling, canal digging, and blast fishing, cause physical disruption to coral reefs by damaging the corals' hard calcium carbonate skeletal structure.

Another major threat to coral reefs comes from chemical degradation. Marine pollution from sunscreens, paints, and inland mining can introduce chemicals that are toxic to corals, leading to their decay. Coral disease is often prevalent in areas where coral are stressed, and has increased in severity in recent decades. [8] Often a result of pollution, eutrophication can occur in coral reef ecosystems, limiting nutrients from the corals. With changes happening on coastal lands such as deforestation, mining, farm soil tiling and erosion, much more sediments are entering the water column. This is known as sediment loading, which can directly smother the coral, or block UV light, effectively blocking the coral from photosynthesizing.

Additionally, increased CO2 emissions from human activities such as fossil fuel burning can effect the acidity of ocean waters. Ocean acidification occurs when excess CO2 reacts with ocean water and lowers the pH. Under acidic conditions, corals cannot produce their calcium carbonate skeletons, and certain zooxanthellae are not able to survive. [9]

Perhaps the biggest threat to coral reefs comes from rising global temperatures. Most corals can only tolerate a 4-5 °C range in water temperatures. Under these adverse conditions, corals may expel their zooxanthellae and become bleached. As ocean waters warm beyond the tolerated temperature range, corals are dying. [10] One study of the Great Barrier Reef found the reef mortality rate to be 50% after an extreme heatwave with 3-4 °C temperature increase. [11] Due to bleaching events similar to this one, injured corals continue to die after the event due to increased disease susceptibility, it takes decades after bleaching events for the reef to recover, and the slow growing corals are put under an immense amount of stress. [11] The rising global temperature is a consequence of releasing high amounts of greenhouse gases into the atmosphere. A study showed that about 655 million people live close to coral reefs, accounting for 91% of the world's population who are part of developed countries such as The United States of America, the Middle East and China. The same study also revealed that of the 655 million people, 75% of the population living in close proximity to coral reefs are from poorly developing countries and even though these low-developing countries depend on the coral reef ecosystem they only contribute to a small fraction of greenhouse emissions. Emission statistics have shown that developed countries contribute to about 11 times more greenhouse gas emissions than poor developing countries. [12]

Propagation methods

Marine Based

Image of a coral polyp. Polypen einer Gorgonie.jpg
Image of a coral polyp.

The process of cultivating coral polyps to aid in the regeneration of reefs worldwide is known as coral gardening. Growing small coral fragments through asexual reproduction until they are fully mature is the fundamental technique of coral gardening, with ocean-based or land-based nurseries being the two primary methods utilized.

Coral reefs are being restored through the use of ocean-based and land-based nurseries. Ocean-based nurseries involve growing coral fragments underwater, attaching them to steel structures and monitoring their growth for 6–12 months until they reach maturity. Once mature, the new polyp colonies can be transferred to damaged reefs. Land-based nurseries, on the other hand, grow coral fragments in laboratories or farms, which allows for faster processes like micro fragmenting. Since most corals grow only about an inch per year, faster-growing practices are important for the restoration of the reefs. Additionally, growing corals on land protect them from changing temperatures, predators, and other problems that can interfere with the restoration process. [14] Additionally with the help of the NOAA, over 40,000 coral reefs have been restored throughout the Caribbean region. [15]

Fragmentation is a method used to divide a wild colony of coral into smaller fragments, and these smaller pieces are grown into additional coral colonies. These fragmented colonies are genetically identical to the host colony. [16] Up to 75% of the host colony may be removed without negative effect on its growth rate. [17] This allows researchers to move forward with restoration projects with minimal impact, if any at all, on the growth rate or survivorship of the original colony. Fragmentation practices are used in virtually every kind of coral restoration strategy used today. Several different methods of growing fragmented corals are outlined below. [17]

Fragmentation allows for about an 8x increase in productivity compared to that of the original donor coral. The amount of fragmentation done to the donor coral is determined based on the amount of space available for attachment. [17] Although fragmentation has great potential, it should be avoided when risk for disease and storms are high as it increases the potential risks from these stressors. This strategy may not be optimal for certain species that are less adapted to fragmentation or have slower growth rates. [17]

In vertical line nurseries, coral fragments are tied to a line suspended in the water. One end of the line is attached to a buoy while the other is anchored to the seafloor. The corals in this type of nursery are linked directly to the vertical line in the water column. [18]

Planted corals near the Maldives island Planted corals near Maldives island after 6 months.jpg
Planted corals near the Maldives island

In suspended line nurseries, two vertical line nurseries are placed apart from each other so they are parallel vertically in the water column. They are then connected together with rope tied perpendicularly between the two. Coral is then attached to this rope, but it is partially dangling off the lines so there is less contact with the rope itself. Less contact between the coral and the suspension lines leads to lower the partial mortality of the corals. [18] Although these structures have some partial mortality, studies show high survival of the whole nursery (in both vertical and suspended). Raising corals on line structures increases the distance between the coral colonies and potential predators, benthic diseases, and there is less space to compete for. Corals grown in line nurseries need to be moved to fixed substrates after an initial growth period, while those propagated on fixed structures can grow indefinitely. [18]

Fixed structure nurseries are frames attached to the seafloor. These nurseries are often made from materials like PVC, plastic mesh, and cinder blocks. [19]

There are likely no differences in growth rates between corals grown horizontally in fixed nurseries, versus those grown vertically in line nurseries. [1] Although, the survival rate of these nurseries are lower than line nurseries. A 2008 study found that fixed structure nurseries had a 43% survival rate, while line nurseries had a 100% survival rate. [18] Initial mortality of fixed structure nurseries is also likely dependent on the time of year that the corals are transplanted. It is important to limit stressors that newly grafted corals are exposed to. [1]

A “coral tree” is the first type of nursery of its kind where coral is completely suspended in the water column. [20] Low cost and availability of materials to create these coral trees make them an ideal method for propagation. [20] These nurseries are less susceptible to damage from wave action, there is less interaction between benthic predators and disease, and reduced entanglement risk for other marine life (compared to line nurseries). Because these nurseries are only anchored in one place, there is minimal impact to the seafloor, they are portable and easily transported by one person, and they can be easily adjusted if depth is an issue. [20]

Land-based

Land-based coral nursery with growing coral micro-fragments Coral Nursery.jpg
Land-based coral nursery with growing coral micro-fragments

Land-based coral nurseries allow coral to grow to a reasonable size before out-planting. Tanks filled with circulating sea water provide an artificial place for coral seedlings to grow. [21] Similar to plant nurseries, a coral nursery provides protection from storms, predation and other stressors as they grow. It is also a place to selectively breed for resistant genotypes. Techniques in growing coral on land can involve sexual and asexual reproduction of coral. When used together, coral specimen can be grown with higher resilience to stressors and fast growth rates. [22]

Asexual Coral Reproduction

Coral are able to reproduce asexually when one polyp undergoes budding to produce another clonal polyp. A technique called micro-fragmentation was developed by Dr. David Vaughan in 2006, which uses the coral's ability to clone itself for coral production. [23] Micro-fragmentation is the process of creating small (>1 cm) pieces of live coral from a parent coral colony. [21] These pieces are then affixed to a ceramic or cement base called a plug and placed in land nursery tanks. [21]

Massive reef-building coral are the prime species used in this method, because it speeds up their growth rate. Rather than waiting decades for a coral to grow to a robust size, months are needed to see viable specimen. [24] This is due to the quick healing response of coral. During micro-fragmentation, wounded edges are created where the colony is severed. These heal quickly by expanding their size radially outward, colonizing their plugs and eventual out-planting sites in the ocean. Fusion of multiple fragments of the same genotype can result in a larger area of coral cover. [24]

Sexual Coral Reproduction

Coral reproduce sexually through broadcast spawning. Coral larvae are formed in the water column through the fertilization of suspended gamete bundles. [21] In a land-based nursery, control over which specimen reproduce can allow for selective breeding of more resilient coral.

Availability of coral gametes in the wild is highly dependent on environmental factors. Studies have shown that most spawning happens at the same time of evening, and depends on lunar cycles. [21] Recent work has been attempting to trigger coral spawning in the nursery environment by mimicking these environmental controls.

Restoration strategies

Coral restoration has been occurring for over 40 years. [21] When determining which restoration strategy is best for a given location, it is important to compare and contrast all methods. [18] The effectiveness of a strategy can be dependent on the habitat a nursery resides in, the conditions of the environment, how the conditions vary annually, and the structure of the nursery chosen. [18]

Coral gardening for reef restoration, on any scale, may not be capable of saving a depleted species. Instead, restoration strategies should be used to aid natural recovery in the re-establishment of a larger genetic pool of a species of coral. This allows corals to sexually reproduce and recover naturally with time. Coral gardening and propagation of corals is important because it is much easier for a fragment of coral to survive than it is for the early life-stage of coral to establish itself in reef environments. [19]

Creating repositories for corals can aid in species reintroduction after coral die-off events. Not only do these repositories serve as a method for recovery, but they can also greatly enhance the genetic pool of isolated populations of corals. [25] Through enhancing these genetic pools, we can expect higher future survival rates for the corals. [19] One study found used an Acropora cervicornis (A. cervicornis) nursery as a repository after an extreme cold-water event occurred that wiped out roughly 43% of its population in the area. The reintroduction of corals from these repositories reintroduced healthy coral tissues to the coral population, aiding in natural reproduction. [25]

These practices should be used simultaneously with practices such as watershed management, sustainable fishing practices, and the establishment of Marine Protected Areas. Coral gardening also offers indirect benefits, like the rapid creation of new fish and invertebrate habitat on depleted reefs. These reef restoration methods also create citizen science opportunities, getting the community involved in coral restoration and conservation. [19]

See also

Related Research Articles

<span class="mw-page-title-main">Coral</span> Marine invertebrates of the class Anthozoa

Corals are colonial marine invertebrates within the class Anthozoa of the phylum Cnidaria. They typically form compact colonies of many identical individual polyps. Coral species include the important reef builders that inhabit tropical oceans and secrete calcium carbonate to form a hard skeleton.

<span class="mw-page-title-main">Coral reef</span> Outcrop of rock in the sea formed by the growth and deposit of stony coral skeletons

A coral reef is an underwater ecosystem characterized by reef-building corals. Reefs are formed of colonies of coral polyps held together by calcium carbonate. Most coral reefs are built from stony corals, whose polyps cluster in groups.

<span class="mw-page-title-main">Anthozoa</span> Class of cnidarians without a medusa stage

Anthozoa is a class of marine invertebrates which includes the sea anemones, stony corals and soft corals. Adult anthozoans are almost all attached to the seabed, while their larvae can disperse as part of the plankton. The basic unit of the adult is the polyp; this consists of a cylindrical column topped by a disc with a central mouth surrounded by tentacles. Sea anemones are mostly solitary, but the majority of corals are colonial, being formed by the budding of new polyps from an original, founding individual. Colonies are strengthened by calcium carbonate and other materials and take various massive, plate-like, bushy or leafy forms.

<span class="mw-page-title-main">Scleractinia</span> Order of Hexacorallia which produce a massive stony skeleton

Scleractinia, also called stony corals or hard corals, are marine animals in the phylum Cnidaria that build themselves a hard skeleton. The individual animals are known as polyps and have a cylindrical body crowned by an oral disc in which a mouth is fringed with tentacles. Although some species are solitary, most are colonial. The founding polyp settles and starts to secrete calcium carbonate to protect its soft body. Solitary corals can be as much as 25 cm (10 in) across but in colonial species the polyps are usually only a few millimetres in diameter. These polyps reproduce asexually by budding, but remain attached to each other, forming a multi-polyp colony of clones with a common skeleton, which may be up to several metres in diameter or height according to species.

<i>Lophelia</i> Species of cnidarian

Lophelia pertusa, the only species in the genus Lophelia, is a cold-water coral that grows in the deep waters throughout the North Atlantic ocean, as well as parts of the Caribbean Sea and Alboran Sea. Although L. pertusa reefs are home to a diverse community, the species is extremely slow growing and may be harmed by destructive fishing practices, or oil exploration and extraction.

<span class="mw-page-title-main">Fire coral</span> Genus of hydrozoans

Fire corals (Millepora) are a genus of colonial marine organisms that exhibit physical characteristics similar to that of coral. The name coral is somewhat misleading, as fire corals are not true corals but are instead more closely related to Hydra and other hydrozoans, making them hydrocorals. They make up the only genus in the monotypic family Milleporidae.

<span class="mw-page-title-main">Elkhorn coral</span> Species of coral

Elkhorn coral is an important reef-building coral in the Caribbean. The species has a complex structure with many branches which resemble that of elk antlers; hence, the common name. The branching structure creates habitat and shelter for many other reef species. Elkhorn coral is known to grow quickly with an average growth rate of 5 to 10 cm per year. They can reproduce both sexually and asexually, though asexual reproduction is much more common and occurs through a process called fragmentation.

<i>Millepora dichotoma</i> Species of hydrozoan

Millepora dichotoma, the net fire coral, is a species of hydrozoan, consisting of a colony of polyps with a calcareous skeleton.

<span class="mw-page-title-main">Deep-water coral</span>

The habitat of deep-water corals, also known as cold-water corals, extends to deeper, darker parts of the oceans than tropical corals, ranging from near the surface to the abyss, beyond 2,000 metres (6,600 ft) where water temperatures may be as cold as 4 °C (39 °F). Deep-water corals belong to the Phylum Cnidaria and are most often stony corals, but also include black and thorny corals and soft corals including the Gorgonians. Like tropical corals, they provide habitat to other species, but deep-water corals do not require zooxanthellae to survive.

<i>Porites astreoides</i> Species of coral

Porites astreoides, commonly known as mustard hill coral or yellow porites, is a colonial species of stony coral in the family Poritidae.

<span class="mw-page-title-main">Coral reef protection</span> Modifying human activities to reduce impact on coral reefs.

Coral reef protection is the process of modifying human activities to avoid damage to healthy coral reefs and to help damaged reefs recover. The key strategies used in reef protection include defining measurable goals and introducing active management and community involvement to reduce stressors that damage reef health. One management technique is to create Marine Protected Areas (MPAs) that directly limit human activities such as fishing.

<i>Pavona duerdeni</i> Species of coral

Pavona duerdeni, the porkchop coral, is a coral that forms clusters of cream-colored lobes or discs. They grow in large colonies, divided into ridges or hillocks. The coral is considered to be uncommon due to its low confirmed abundance, yet they are more commonly found in Hawaii, the Indo-Pacific, and the Tropical Eastern Pacific. They make up some of the largest colonies of corals, and have a slow growth rate, as indicated by their dense skeletons. Their smooth appearance is due to their small corallites growing on their surface.

<span class="mw-page-title-main">Aquaculture of coral</span> Cultivation of coral for commercial purposes

Coral aquaculture, also known as coral farming or coral gardening, is the cultivation of corals for commercial purposes or coral reef restoration. Aquaculture is showing promise as a tool for restoring coral reefs, which are dying off around the world. The process protects young corals while they are most at risk of dying. Small corals are propagated in nurseries and then replanted on the reef.

<i>Porites lobata</i> Species of coral

Porites lobata, known by the common name lobe coral, is a species of stony coral in the family Poritidae. It is found growing on coral reefs in tropical parts of the Indian and Pacific Oceans.

<i>Millepora alcicornis</i> Species of hydrozoan

Millepora alcicornis, or sea ginger, is a species of colonial fire coral with a calcareous skeleton. It is found on shallow water coral reefs in the tropical west Atlantic Ocean. It shows a variety of different morphologies depending on its location. It feeds on plankton and derives part of its energy requirements from microalgae found within its tissues. It is an important member of the reef building community and subject to the same threats as other corals. It can cause painful stings to unwary divers.

<i>Acropora pulchra</i> Species of coral

Acropora pulchra is a species of colonial staghorn coral in the family Acroporidae. It is found on the back fringes of reefs in shallow water in the western Indo-Pacific Ocean. The oldest fossils of this species date back to the Pleistocene.

<i>Astrangia poculata</i> Species of coral

Astrangia poculata, the northern star coral or northern cup coral, is a species of non-reefbuilding stony coral in the family Rhizangiidae. It is native to shallow water in the western Atlantic Ocean and the Caribbean Sea. It is also found on the western coast of Africa. The International Union for Conservation of Nature lists this coral as being of "least concern". Astrangia poculata is an emerging model organism for corals because it harbors a facultative photosymbiosis, is a calcifying coral, and has a large geographic range. Research on this emerging model system is showcased annually by the Astrangia Research Working Group, collaboratively hosted by Roger Williams University, Boston University, and Southern Connecticut State University

<i>Porites cylindrica</i> Species of coral

Porites cylindrica, commonly known as hump coral, is a stony coral belonging to the subclass Hexacorallia in the class Anthozoa. Hexacorallia differ from other subclasses in that they have 6 or fewer axes of symmetry. Members of this class possess colonial polyps which can be reef-building, secreting a calcium carbonate skeleton. They are dominant in both inshore reefs and midshelf reefs.

<i>Porites lutea</i> Species of coral

Porites lutea is a species of stony coral in the family Poritidae. It is found growing in very shallow water on reefs in the Indo-Pacific region. It sometimes forms "microatolls" in the intertidal zone and these massive structures have been used to study trends in sea levels and sea water temperature.

References

  1. 1 2 3 Drury, Crawford; Paris, Claire B.; Kourafalou, Vassiliki H.; Lirman, Diego (2018-04-05). "Dispersal capacity and genetic relatedness in Acropora cervicornis on the Florida Reef Tract". Coral Reefs. 37 (2): 585–596. Bibcode:2018CorRe..37..585D. doi:10.1007/s00338-018-1683-0. ISSN   0722-4028. S2CID   253816402.
  2. 1 2 "Coral reef ecosystems | National Oceanic and Atmospheric Administration". www.noaa.gov. Retrieved 2021-03-18.
  3. "We believe in coral reefs". Coral Reef Alliance. Retrieved 2022-11-17.
  4. 1 2 "Coral Reefs and Corals | Smithsonian Ocean". ocean.si.edu. 30 April 2018. Retrieved 2021-03-19.
  5. Stanley, George D. (2003-02-01). "The evolution of modern corals and their early history". Earth-Science Reviews. 60 (3): 195–225. Bibcode:2003ESRv...60..195S. doi:10.1016/S0012-8252(02)00104-6. ISSN   0012-8252.
  6. "2020 Report – GCRMN" . Retrieved 2022-11-17.
  7. MSc, Amy Wilson (2018-09-18). "Microfragmentation: a breakthough[sic] for coral reef restoration". Medium. Retrieved 2023-03-01.
  8. Page, CA; Baker, DM; Harvell, CD; Golbuu, Y; Raymundo, L; Neale, SJ; Rosell, KB; Rypien, KL; Andras, JP; Willis, BL (2009-11-16). "Influence of marine reserves on coral disease prevalence". Diseases of Aquatic Organisms. 87 (1–2): 135–150. doi: 10.3354/dao02112 . ISSN   0177-5103. PMID   20095248.
  9. Anthony, K. R. N.; Kline, D. I.; Diaz-Pulido, G.; Dove, S.; Hoegh-Guldberg, O. (2008-11-11). "Ocean acidification causes bleaching and productivity loss in coral reef builders". Proceedings of the National Academy of Sciences. 105 (45): 17442–17446. Bibcode:2008PNAS..10517442A. doi: 10.1073/pnas.0804478105 . ISSN   0027-8424. PMC   2580748 . PMID   18988740.
  10. Schoepf, Verena; Stat, Michael; Falter, James L.; McCulloch, Malcolm T. (2015-12-02). "Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment". Scientific Reports. 5 (1): 17639. Bibcode:2015NatSR...517639S. doi:10.1038/srep17639. ISSN   2045-2322. PMC   4667274 . PMID   26627576.
  11. 1 2 Hughes, Terry P.; Kerry, James T.; Baird, Andrew H.; Connolly, Sean R.; Dietzel, Andreas; Eakin, C. Mark; Heron, Scott F.; Hoey, Andrew S.; Hoogenboom, Mia O.; Liu, Gang; McWilliam, Michael J. (2018). "Global warming transforms coral reef assemblages". Nature. 556 (7702): 492–496. Bibcode:2018Natur.556..492H. doi:10.1038/s41586-018-0041-2. ISSN   0028-0836. PMID   29670282. S2CID   4931103.
  12. Donner, Simon D.; Potere, David (2007-03-01). "The Inequity of the Global Threat to Coral Reefs". BioScience. 57 (3): 214–215. doi: 10.1641/b570302 . ISSN   1525-3244. S2CID   84200257.
  13. Gorgonian polyps. Photographed in the reef aquarium of aquarist Mike Giangrasso., 2006-08-03, retrieved 2023-03-01
  14. "How Coral Gardening Is Saving Reefs". Sciencing. Retrieved 2023-03-01.
  15. Fisheries, NOAA (2021-09-27). "Restoring Coral Reefs | NOAA Fisheries". NOAA. Retrieved 2023-03-01.
  16. "Traditional Fragmentation | Reef Resilience" . Retrieved 2021-04-07.
  17. 1 2 3 4 Lohr, Ke; Bejarano, S; Lirman, D; Schopmeyer, S; Manfrino, C (2015-04-29). "Optimizing the productivity of a coral nursery focused on staghorn coral Acropora cervicornis". Endangered Species Research. 27 (3): 243–250. doi: 10.3354/esr00667 . hdl: 1834/32632 . ISSN   1863-5407.
  18. 1 2 3 4 5 6 Goergen, Elizabeth A.; Ostroff, Zachary; Gilliam, David S. (2018). "Genotype and attachment technique influence the growth and survival of line nursery corals". Restoration Ecology. 26 (4): 622–628. doi:10.1111/rec.12545. S2CID   90639031.
  19. 1 2 3 4 Lirman, Diego; Schopmeyer, Stephanie (2016-10-20). "Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic". PeerJ. 4: e2597. doi: 10.7717/peerj.2597 . ISSN   2167-8359. PMC   5075686 . PMID   27781176.
  20. 1 2 3 Kenneth, Nedimeyer (2011). "Coral tree nursery: an innovative approach to growing corals in an ocean-based field nursery". Aacl Bioflux. S2CID   130379671.
  21. 1 2 3 4 5 6 "Vaughan, D (2021). Active Coral Restoration: techniques for a changing planet".
  22. Forsman, Zac H.; Page, Christopher A.; Toonen, Robert J.; Vaughan, David (2015-10-20). "Growing coral larger and faster: micro-colony-fusion as a strategy for accelerating coral cover". PeerJ. 3: e1313. doi: 10.7717/peerj.1313 . ISSN   2167-8359. PMC   4614846 . PMID   26500822.
  23. Morin, Richard (2014-11-23). "A Lifesaving Transplant for Coral Reefs". The New York Times. ISSN   0362-4331 . Retrieved 2022-11-22.
  24. 1 2 Page, Christopher A.; Muller, Erinn M.; Vaughan, David E. (2018). "Microfragmenting for the successful restoration of slow growing massive corals". Ecological Engineering. 123: 86–94. doi: 10.1016/j.ecoleng.2018.08.017 . ISSN   0925-8574. S2CID   106389447.
  25. 1 2 Schopmeyer, Stephanie A.; Lirman, Diego; Bartels, Erich; Byrne, James; Gilliam, David S.; Hunt, John; Johnson, Meaghan E.; Larson, Elizabeth A.; Maxwell, Kerry; Nedimyer, Ken; Walter, Cory (2012). "In Situ Coral Nurseries Serve as Genetic Repositories for Coral Reef Restoration after an Extreme Cold-Water Event". Restoration Ecology. 20 (6): 696–703. doi:10.1111/j.1526-100X.2011.00836.x. S2CID   32470321.