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Strategies for integrating sexually propagated corals into Caribbean reef restoration: experimental results and considerations

Authors:
Joseph Henry at Triton Society
Joseph Henry
  • Triton Society
Keri L. O’Neil
Keri L. O’Neil
Keri L. O’Neil
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Aaron Pilnick at University of Florida
Aaron Pilnick
Joshua T. Patterson
Joshua T. Patterson
Joshua T. Patterson
  • This person is not on ResearchGate, or hasn't claimed this research yet.
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Abstract and Figures

Caribbean hard coral cover has decreased by more than 80% in the last 40 years. In response, active coral restoration has grown in popularity as a management tool to sustain degraded reefs. To date, the majority of coral outplanting has employed asexually propagated ramets derived from wild donor colonies. Unfortunately, this strategy is incapable of increasing genetic diversity and limits the adaptive potential of restored coral populations. Methods for sexual propagation in land-based systems offer increasing potential to enhance genetic diversity of target species. However, questions regarding coral performance once placed back into the dynamic marine environment must be considered. Thus, focused experiments to optimize the integration of land reared corals and novel genetic diversity are of immense value. For this reason, we designed a study using two Acropora cervicornis year classes produced in a land-based system and concurrently relocated to an inshore patch reef, a back reef, and placed in an ocean-based nursery (n = 80 sexually propagated colonies per location). A deliberate monitoring strategy measured growth and survival five times over a 480-day period. Major findings were 1) high survival rates (~ 73%) across all 160 outplanted colonies 2) significant differences in survival between outplanting locations and coral recruit year class, and 3) very high survival of sexually propagated corals relocated to the ocean-based nursery (~ 93% overall), with 40-fold greater growth than direct-outplanted colonies. Our study suggests that ex situ sexual coral propagation offers a tractable tool to meet the need for increased A. cervicornis genetic diversity. Lastly, we offer insight and considerations for managing the high input of novel genotypes into restoration systems and suggest further research to maximize the adaptive potential of coral populations.
Photographs of four sexually propagated Acropora cervicornis colonies at the initiation (a–d) and conclusion (e–h) of the experiment. These examples exhibited greater than average growth (see Table 2). Colonies from the 2018 and 2017 year classes, respectively, were outplanted (a, pictured colony = 1.3 cm³ and b, pictured colony = 13.1 cm³) and hung in a tree nursery (c; pictured colony = 2.4 cm³ and d, pictured colony = 10.9 cm³). The same colonies are pictured after 480 days of growth (e, pictured colony = 274.9 cm³; f, pictured colony = 544.5 cm³; g, pictured colony = 9110.6 cm³; h, pictured colony = 28,651.3 cm³)
Photographs of four sexually propagated Acropora cervicornis colonies at the initiation (a–d) and conclusion (e–h) of the experiment. These examples exhibited greater than average growth (see Table 2). Colonies from the 2018 and 2017 year classes, respectively, were outplanted (a, pictured colony = 1.3 cm³ and b, pictured colony = 13.1 cm³) and hung in a tree nursery (c; pictured colony = 2.4 cm³ and d, pictured colony = 10.9 cm³). The same colonies are pictured after 480 days of growth (e, pictured colony = 274.9 cm³; f, pictured colony = 544.5 cm³; g, pictured colony = 9110.6 cm³; h, pictured colony = 28,651.3 cm³)
… 
Survival of sexually propagated Acropora cervicornis across three experimental locations in the Florida Keys for the duration of the 480-day study (Kaplan–Meier X² = 50.6 df = 2, p < 0.01). Data were pooled to include 2017 and 2018 year classes and letters indicate differences among location as determined by a log-rank test
Survival of sexually propagated Acropora cervicornis across three experimental locations in the Florida Keys for the duration of the 480-day study (Kaplan–Meier X² = 50.6 df = 2, p < 0.01). Data were pooled to include 2017 and 2018 year classes and letters indicate differences among location as determined by a log-rank test
… 
Visualization of colony size across time of Acropora cervicornis at three locations in the Florida Keys. These locations include a Cheeca Rocks, b Tennessee Reef and c) the Coral Restoration Foundation nursery in Tavernier Florida. Data are presented as mean ± SEM. All live colonies, including those that experienced breakage, are included in these data. Due to differences in initial colony morphology, statistical comparisons were made only on final ellipsoid volume (see Table 2). Pairwise comparisons of year class within reef sites were not made due to factorial analysis indicating differences between year classes across sites with no significant interaction. Nursery data were analyzed separately
Visualization of colony size across time of Acropora cervicornis at three locations in the Florida Keys. These locations include a Cheeca Rocks, b Tennessee Reef and c) the Coral Restoration Foundation nursery in Tavernier Florida. Data are presented as mean ± SEM. All live colonies, including those that experienced breakage, are included in these data. Due to differences in initial colony morphology, statistical comparisons were made only on final ellipsoid volume (see Table 2). Pairwise comparisons of year class within reef sites were not made due to factorial analysis indicating differences between year classes across sites with no significant interaction. Nursery data were analyzed separately
… 
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REPORT
Strategies for integrating sexually propagated corals
into Caribbean reef restoration: experimental results
and considerations
Joseph A. Henry
1
•Keri L. O’Neil
2
•Aaron R. Pilnick
3
•Joshua T. Patterson
1,2
Received: 3 March 2021 / Accepted: 30 June 2021 / Published online: 14 July 2021
ÓThe Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract Caribbean hard coral cover has decreased by
more than 80% in the last 40 years. In response, active
coral restoration has grown in popularity as a management
tool to sustain degraded reefs. To date, the majority of coral
outplanting has employed asexually propagated ramets
derived from wild donor colonies. Unfortunately, this
strategy is incapable of increasing genetic diversity and
limits the adaptive potential of restored coral populations.
Methods for sexual propagation in land-based systems
offer increasing potential to enhance genetic diversity of
target species. However, questions regarding coral perfor-
mance once placed back into the dynamic marine envi-
ronment must be considered. Thus, focused experiments to
optimize the integration of land reared corals and novel
genetic diversity are of immense value. For this reason, we
designed a study using two Acropora cervicornis year
classes produced in a land-based system and concurrently
relocated to an inshore patch reef, a back reef, and placed
in an ocean-based nursery (n= 80 sexually propagated
colonies per location). A deliberate monitoring strategy
measured growth and survival five times over a 480-day
period. Major findings were 1) high survival rates
(*73%) across all 160 outplanted colonies 2) significant
differences in survival between outplanting locations and
coral recruit year class, and 3) very high survival of sex-
ually propagated corals relocated to the ocean-based
nursery (*93% overall), with 40-fold greater growth than
direct-outplanted colonies. Our study suggests that ex situ
sexual coral propagation offers a tractable tool to meet the
need for increased A. cervicornis genetic diversity. Lastly,
we offer insight and considerations for managing the high
input of novel genotypes into restoration systems and
suggest further research to maximize the adaptive potential
of coral populations.
Keywords Coral outplanting Acropora Genetic
diversity Adaptive management Threatened species
Introduction
Coral reefs are disappearing globally at an alarming rate
(Burke et al. 2013; Pratchett et al. 2014). Disease (Walton
et al. 2018; Muller et al. 2020), elevated ocean tempera-
tures (De’ath et al. 2012), extreme weather events
(Woodley et al. 1981; Dahlgren and Sherman 2020), and
pollution (Bak 1987; Edinger et al. 1998) have led to a
precarious and uncertain future for coral reefs. Continued
degradation of these ecosystems could have extensive
consequences as they provide a multitude of environmental
and economic benefits including coastal protection, tour-
ism, and a source of food (Burke et al. 2013; Massel and
Gourlay 2000; Cinner 2014). In the Caribbean, hard coral
cover has decreased by more than 80% in the last 40 years
(Gardner et al. 2003; Maynard et al. 2017, NOAA 2018).
Staghorn coral Acropora cervicornis was historically a
dominant reef building species throughput this region
Topic Editor Anastazia Teresa Banaszak
&Joseph A. Henry
henry8404@ufl.edu
1
Program in Fisheries and Aquatic Sciences, School of Forest,
Fisheries, and Geomatics Sciences, University of Florida/
IFAS, 7922 NW 71st Street, Gainesville, FL 32653, USA
2
Center for Conservation, The Florida Aquarium, 529 Estuary
Shore Lane, Apollo Beach, FL 33572-2205, USA
3
Interdisciplinary Ecology, School of Natural Resources and
Environment, University of Florida/IFAS, 103 Black Hall,
Gainesville, FL 32611, USA
123
Coral Reefs (2021) 40:1667–1677
https://doi.org/10.1007/s00338-021-02154-2
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... This research stemmed from an initiative to find a means to protect juvenile corals [22] and coral microfragments [45] transplanted from laboratories to the ocean as part of a coordinated effort to restore Florida's coral reef [14] amidst a devastating disease outbreak that began in 2014 and that has spread throughout the entire Florida coral reef tract and the Caribbean [1,2,24,43,62]. Attempts to replenish Florida's coral reef in this manner have been hampered by corallivores predating on the transplanted laboratory corals, causing dislodgment of the corals from their substrate support or tissue loss that often leads to mortality, particularly in small colonies [33]. ...
... Therefore, all of the equations, limits, and figures based on (12) for hollow cylinders also apply for hollow square prisms, provided that D o (0) , D i (0) , and W(0) are now defined by Fig. 14. Using (57) and (58), it is easy to show that (22) is valid, such that = r∕ for arbitrary values of D o (0) , L(0), and W(0) for a hollow square prism. ...
... Therefore, all of the equations, limits, and figures based on (39) for solid cylinders also apply for solid square prisms, provided that D(0) is now defined by Fig. 14. Using (61) and (62) it can be shown that (22) is valid, such that = r∕ for arbitrary values of D(0) and L(0) for a solid square prism. ...
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... Study. This research stemmed from an initiative to find a means to protect juvenile corals [20] and coral microfragments [40] moved from laboratories to the ocean as part of a coordinated effort to restore Florida's Coral Reef [12] amidst a devastating disease outbreak that began in 2014 and which has spread throughout the entire Florida coral reef tract, as well as the Caribbean [1,2,22,38,54]. Attempts to replenish Florida's Coral Reef in this manner have been hampered by corallivores predating on the transplanted laboratory corals, causing dislodgment of the corals from their substrate support or tissue loss that often leads to mortality, particularly in small colonies [29]. ...
... The effect of different wall thicknesses (T /D o ) for the hollow cylinder is shown. Employing the same logic as in Section 4.2,20 this ratio k represents the multiple of time required for the solid cylinder (t S ) to attain the same m ′ /m value as that for the hollow cylinder (t H ) : ...
... These checks verified the accuracy of (A.10) and (A. 20), and that positive values of the discriminant (A.8) yield one real root, that negative values of the discriminant yield three roots, and that a zero value of the discriminant yields three roots, two of which are identical. ...
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... proportional survival is acknowledged, we assume the existence of a relationship [8]. This growth time may impact the post-deployment survival rate, volume yield, or other factors [8,9]. ...
... proportional survival is acknowledged, we assume the existence of a relationship [8]. This growth time may impact the post-deployment survival rate, volume yield, or other factors [8,9]. This proportional post-deployment survival rate determines the required production quantities to meet demand requirements. ...
... Corals can be propagated sexually through larval spawning or asexually by fragmentation. Whilst sexually propagated corals offer the potential to enhance genetic diversity of reefs, further considerations must be made to consider the timing and logistics of coral spawning [8]. Asexual propagation involves pre-settling fragmented corals onto deployment devices, and rearing corals until deployed. ...
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... In addition, the minimal increase in the number of SNPs that deviate from Hardy-Weinberg expectations may suggest that overall there has not been a great deal of selection or allele frequency changes due to other factors in one generation. This may bode well for out planting aquarium-bred corals into the wild, and indeed it has been shown that aquarium-bred corals can survive and grow successfully in the wild (Henry et al., 2021), in contrast with studies that have demonstrated fitness and phenotype changes in hatchery-raised fish within one generation (Kostow, 2004;Wakiya et al., 2022). ...
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... The latter, meanwhile, represents a sustainable and cost-effective ecological approach for coral reef restoration [10,11]. The use of sexual propagation strategies can promote genetic diversity and species evolution, thereby allowing corals to adapt to a changing environment [12][13][14]. ...
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Full-text available
Significant population declines in Acropora cervicornis and A. palmata began in the 1970s and now exceed over 90%. The losses were caused by a combination of coral disease and bleaching, with possible contributions from other stressors, including pollution and predation. Reproduction in the wild by fragment regeneration and sexual recruitment is inadequate to offset population declines. Starting in 2007, the Coral Restoration Foundation™ evaluated the feasibility of outplanting A. cervicornis colonies to reefs in the Florida Keys to restore populations at sites where the species was previously abundant. Reported here are the results of 20 coral outplanting projects with each project defined as a cohort of colonies outplanted at the same time and location. Photogrammetric analysis and in situ monitoring (2007 to 2015) measured survivorship, growth, and condition of 2419 colonies. Survivorship was initially high but generally decreased after two years. Survivorship among projects based on colony counts ranged from 4% to 89% for seven cohorts monitored at least five years. Weibull survival models were used to estimate survivorship beyond the duration of the projects and ranged from approximately 0% to over 35% after five years and 0% to 10% after seven years. Growth rate averaged 10 cm/year during the first two years then plateaued in subsequent years. After four years, approximately one-third of surviving colonies were ≥ 50 cm in maximum diameter. Projects used three to sixteen different genotypes and significant differences did not occur in survivorship, condition, or growth. Restoration times for three reefs were calculated based on NOAA Recovery Plan (NRP) metrics (colony abundance and size) and the findings from projects reported here. Results support NRP conclusions that reducing stressors is required before significant population growth and recovery will occur. Until then, outplanting protects against local extinction and helps to maintain genetic diversity in the wild.
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Spatial Epidemiology of the Stony-Coral-Tissue-Loss Disease in Florida
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  • Mar 2020
The stony-coral-tissue-loss disease (SCTLD) has recently caused widespread loss of coral along the Florida reef tract. Yet little is known about where, when, and why this coral disease outbreak occurred. In the absence of a definitive pathogen, it is essential to characterize the ecology of the disease and document the spatio-temporal dynamics of the outbreak. Here, we investigate the epizootiology of the SCTLD at multiple spatial and temporal scales along the Florida reef tract from May 2014 to December 2017. We used spatial interpolation to characterize the disease hotspots, Ripley’s K analysis to examine contagion, a spatio-temporal model to assess rates of spread, and a Bayesian model to examine ecological and environmental covariates that may have influenced the occurrence and severity of the outbreak. Our results show that the disease affected reefs at the scale of hundreds of kilometers, with significant clusters of up to 140 km. The epizootic clearly followed a contagion model, suggesting that the disease was highly contagious. The rate of spread of the epizootic was linear and moved slightly faster to the north (∼100 m d–1) than to the south (∼92 m d–1). The difference in rate of spread between the north and south direction may indicate currents facilitated transmission. The analyzed dataset showed that the epizootic affected at least 19 coral species and that deep and diverse sites were at greater risk of the disease than shallow and low diversity sites.
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Coral restoration – A systematic review of current methods, successes, failures and future directions
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Coral reef ecosystems have suffered an unprecedented loss of habitat-forming hard corals in recent decades. While marine conservation has historically focused on passive habitat protection, demand for and interest in active restoration has been growing in recent decades. However, a disconnect between coral restoration practitioners, coral reef managers and scientists has resulted in a disjointed field where it is difficult to gain an overview of existing knowledge. To address this, we aimed to synthesise the available knowledge in a comprehensive global review of coral restoration methods, incorporating data from the peer-reviewed scientific literature, complemented with grey literature and through a survey of coral restoration practitioners. We found that coral restoration case studies are dominated by short-term projects, with 60% of all projects reporting less than 18 months of monitoring of the restored sites. Similarly, most projects are relatively small in spatial scale, with a median size of restored area of 100 m². A diverse range of species are represented in the dataset, with 229 different species from 72 coral genera. Overall, coral restoration projects focused primarily on fast-growing branching corals (59% of studies), and report survival between 60 and 70%. To date, the relatively young field of coral restoration has been plagued by similar ‘growing pains’ as ecological restoration in other ecosystems. These include 1) a lack of clear and achievable objectives, 2) a lack of appropriate and standardised monitoring and reporting and, 3) poorly designed projects in relation to stated objectives. Mitigating these will be crucial to successfully scale up projects, and to retain public trust in restoration as a tool for resilience based management. Finally, while it is clear that practitioners have developed effective methods to successfully grow corals at small scales, it is critical not to view restoration as a replacement for meaningful action on climate change.
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Native Herbivores Improve Sexual Propagation of Threatened Staghorn Coral Acropora cervicornis
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  • Nov 2019
Staghorn coral Acropora cervicornis was once spatially dominant on Caribbean reefs but is now threatened throughout its range. In recent years, advancements in ex situ sexual propagation of Caribbean corals have increased the viability of this management strategy. Thus, improving culture methods for sexually propagated corals is important to bolster the overall coral restoration portfolio and increase genetic diversity in restored populations. In both natural systems and culture scenarios, algae proliferation negatively impacts coral growth and survival. Growing coral with native herbivores may represent a strategy for increased efficiency. We tested A. cervicornis recruits raised in replicate aquaria with identical densities of juvenile Lithopoma americanum or juvenile Batillaria minima snails plus a no-snail control. Each of three replicates per treatment contained tiles with similar numbers of recently settled, visually healthy, A. cervicornis. Tiles were photographed every 3 weeks for 5 months and coral growth, survivability, turf algae cover, and crustose coralline algae (CCA) cover were quantified. Labor time for cleaning was carefully recorded for each treatment. Results indicated improved growth and survival when A. cervicornis recruits were raised with either snail species in comparison to a no-herbivore control. Further, including snails decreased labor and eliminated turf algae cover. Interestingly, L. americanum significantly reduced CCA cover relative to the other treatments. We report some of the highest survival rates observed to date for sexually propagated Atlantic corals. Ultimately, results suggest that rearing sexually propagated A. cervicornis with native herbivores could improve the ability to employ these corals in reef restoration.
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Ex situ co culturing of the sea urchin, Mespilia globulus and the coral Acropora millepora enhances early post-settlement survivorship
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  • Sep 2019
Reef restoration efforts, utilising sexual coral propagation need up-scaling to have ecologically meaningful impact. Post-settlement survival bottlenecks, in part due to competitive benthic algae interactions should be addressed, to improve productivity for these initiatives. Sea urchins are keystone grazers in reef ecosystems, yet feeding behaviour of adults causes physical damage and mortality to developing coral spat. To investigate if microherbivory can be utilised for co-culture, we quantitatively assessed how varying densities of juvenile sea urchins Mespilia globulus (Linnaeus, 1758), reared alongside the coral Acropora millepora (Ehrenberg, 1834) effected survival and growth of coral recruits. Spawning of both species were induced ex situ. A comparison of A. millepora spat reared in three M. globulus densities (low 16.67 m−2, medium 37.50 m−2, high 75.00 m−2) and a non-grazed control indicated coral survival is significantly influenced by grazing activity (p < 0.001) and was highest in the highest density treatment (39.65 ± 10.88%, mean ± s.d). Urchin grazing also significantly (p < 0.001) influenced coral size (compared to non-grazing control), with colonies in the medium and high-densities growing the largest (21.13 ± 1.02 mm & 20.80 ± 0.82, mean ± s.e.m). Increased urchin density did however have a negative influence on urchin growth, a result of limited food availability.
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Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic
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Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.
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Differential disturbance effects and phenotypic plasticity among outplanted corals at patch and fore reef sites
Article
  • Apr 2020
  • J NAT CONSERV
Practitioners have outplanted tens of thousands of nursery-reared coral colonies for restoration purposes, and interest in outplanting is increasing. However, restoration outcomes on natural reefs can be variable, and genotype- and site-specific differences have been reported. To systematically explore these differences, performance of restored corals was compared at two site types, and intraspecific variation in phenotype among six genotypes previously characterized in a nursery was simultaneously assessed. Nursery-reared Acropora cervicornis colonies were outplanted to geographically paired fore reef (n = 2) and patch reef (n = 2) sites. Colony growth and condition were monitored over one year. After the first monitoring visit, Hurricane Irma passed directly over outplant sites, providing an opportunity to examine disturbance effects across sites. In contrast to nursery results, growth did not vary among genotypes or sites either pre- or post-hurricane. Plasticity in pre-hurricane growth among sites was observed for one of the six genotypes examined. Stark differences in post-hurricane survival were observed between fore reef and patch reef sites: while 51.04 ± 9.38% of outplanted colonies survived at patch reef sites, no colonies could be located at either fore reef site. Records from additional sites monitored by practitioners indicated higher outplant survival following hurricane disturbance at patch reef sites compared to fore reef sites. The lack of site or genotype effects on growth in A. cervicornis contrasts with a number of previous studies, however growth results were likely confounded by Hurricane Irma. Reduced structural complexity on Caribbean reefs may contribute to differential hurricane impacts between restored fore reefs and patch reefs. These results suggest that restoration practitioners should consider increasing effort on patch reef sites in restoration programs while also developing new strategies to foster resilience at fore reef sites.
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Successfully cultured and reared coral embryos from wild caught spawn slick in the Philippines
Article
  • Aug 2020
  • AQUACULTURE
Various coral propagation techniques, including utilization of spawn slicks, have been developed to help restore degraded coral communities. Although, it has been demonstrated that embryos from spawn can be used for sexual propagation of corals, few have quantified fertilization, survival, settlement, post-settlement mortality, and long term survival of transplanted corals, grown from spawn slick. Spawn slicks were collected at night off Anda, northwestern Philippines, following a mass spawning of Acropora spp. The collected spawn, which contained ~4,100,000 developing embryos, was highly viable (96% actively dividing) at 12 h post-mixing. Based on assays, 2-day old larvae exhibited high survival in culture (87.9%), and subsequent settlement competency (92%). All 3330 settlement substrates (coral plug-ins), seeded with approximately 2,100,000 3-day old coral larvae, had at least one settled coral after one month. Forty-five pieces of these plug-ins, which were randomly tagged, had settled coral spats ranging from 3 to 88 spats per plug-in (26.7 ± 3.4 spats per plug-in, mean ± SE). Two and four months after the initial settlement on plug-ins, 76.3 ± 1.2% and 42.5 ± 1.2% of the spats survived, respectively. Two hundred seventy (270) coral plug-ins were then transplanted at six sites. Transplanted corals exhibited varying survival in different sites, from 11 to 62%, five months post-transplantation. Thirty-one months post-transplantation, only two of the six sites had surviving transplanted corals, i.e., four colonies of Acropora millepora, three A. divaricata, and one A. cf. austera. However, setbacks in the survival of transplants highlight the need to further examine drivers affecting long term performance of coral transplants, which is vital in establishing different generations of parent colonies that can be used for sustainable mariculture of corals.
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