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Four-year-old Caribbean Acropora colonies reared from field-collected gametes are sexually mature

Authors:
  • SECORE International
  • SECORE International
  • Ripley's Aquarium of Canada
BULLETIN OF MARINE SCIENCE. 00(0):000–000. 0000
doi:10.5343/
105
Bullen of Marine Science
© 2011 Rosensel School of Marine and Atmospheric Science
of the University of Miami
Bulletin of Marine Science
© 2016 Rosenstiel School of Marine & Atmospheric Science of
the University of Miami Portraits of Marine Science
Bull Mar Sci. 92(2):000–000. 2016
http://dx.doi.org/10.5343/bms.2015.1074
Four-year-old Caribbean Acropora colonies reared
from eld-collected gametes are sexually mature
VF Chamberland 1, 3, 4 *, D Petersen 1, 2, KRW Latijnhouwers 4,
S Snowden 1, 5, B Mueller 3, MJA Vermeij 3, 4
1 SECORE Intern ational, c/o Colu mbus Zoo and Aquar ium, 9990 Riversid e Drive, Powell, Ohi o 43065.
2 SECORE International, Arensburgstraße 40, Bremen, Germany.
3 Carmabi Foundation, Piscaderabaai z/n, Willemstad, Curaçao.
4 Aquatic Mi crobiology, Inst itute for Biodive rsity and Ecosyst em Dynamics, U niversity of Amst erdam, Science Par k 700,
1098 XH Amster dam, Netherla nds.
5 Pittsbu rgh Zoo & PPG Aquarium , One Wild Place, Pi ttsburgh, Penn sylvania 15206.
* Corresponding author email: <chamberland.f.valerie@gmail.com>.
Rehabilitating populations of Caribbean coral species that have declined in recent
decades has become a management priority throughout the region, stimulating the
development of new methodologies to artificially reseed degraded reefs. Rearing lar-
vae of ecologically important coral species appears a particularly attractive method
to aid the recovery of degraded populations because genetic recombination could
yield new genotypes better capable of coping with the altered conditions on modern
Caribbean reefs. Well-developed elkhorn coral (Acropora palmata Lamarck, 1816)
populations form dense thickets that contribute to the maintenance of healthy and
productive reefs by providing shelter to a variety of other reef organisms (Gladfelter
and Gladfelter 1978). After >95% of A. palmata populations were decimated by a
disease beginning in the mid-1970s, this species was listed as critically endangered
under the Red List of reatened Species (IUCN 2013) and restoration efforts were
initiated throughout the region to assist its recovery (Young et al. 2012). In 2011, we
collected gametes from eight A. palmata colonies in situ off Curaçao, which were
subsequently cross-fertilized to generate larvae. Competent larvae were settled on
clay tiles (Panel A) and reared in a flow-through land-based nursery for one year
(Panels B–C), after which they were outplanted to a breakwater at 2–5 m depth
Fas t Track
publication
BULLETIN OF MARINE SCIENCE. VOL 00, NO 0. 0000106 Bulletin of Marine Science. Vol 92, No 2. 2016
B
M
S
(Panel D) [refer to Chamberland et al. (2015) for details on methodology]. Seven out
of nine outplanted colonies survived and continued to grow in situ (Panels D–E),
reaching a size of 30–40 cm diameter and 20–30 cm height after 4 yrs (Panel F). On
8 and 10 September, 2015, nine and 11 d after the full moon, two colonies were ob-
served releasing gametes between 155 and 175 min after sunset (Panels G–H). is is
the first time that an endangered Caribbean Acropora coral species was raised from
larvae and grown to sexual maturity in the field. Indeed, only one other study has
documented age and colony size at reproductive onset in a broadcast spawning scler-
actinian coral reared from larvae (Baria et al. 2012). e relatively short time until
onset of spawning (≤4 yrs) observed for A. palmata shows that recovery of degraded
coral populations by enhancing natural recruitment rates may be practicable if out-
planted colonies are able to rapidly contribute to the natural pool of larvae.
A
is research was supported by the European Union Seventh Framework Programme
(FP7/2007-2013) under grant agreement no 244161 (Future of Reefs in a Changing Environ-
ment), the National Oceanic and Atmospheric Administration (NOAA), the Green Founda-
tion, the Walton Family Foundation, TUI Cruises/ Futouris e.V., the Clyde and Connie Wood-
burn Foundation, and the Montei Foundation. We are grateful to the Curaçao Sea Aquarium
staff and all participants from the 2011 and 2012 editions of the SECORE workshop for their
assistance in the field.
L C
Baria MVB, Villanueva RD, Guest JR. 2012. Spawning of three year-old Acropora millepora cor-
als reared from larvae in northwestern Philippines. Bull Mar Sci. 88:61–62. http://dx.doi.
org/10.5343/bms.2011.1075
Chamberland VF, Vermeij MJA, Brittsan M, Carl M, Schick M, Snowden S, Schrier A, Petersen
D. 2015. Restoration of critically endangered elkhorn coral (Acropora palmata) popula-
tions using larvae reared from wild-caught gametes. Glob Ecol Cons. 4:526–553. http://
dx.doi.org/10.1016/j.gecco.2015.10.005
Gladfelter WB, Gladfelter EH. 1978. Fish community structure as a function of habitat struc-
ture on West Indian patch reefs. Rev Biol Trop. 26(1):65–84.
International Union for Conservation of Nature (IUCN). 2013. IUCN Red List of reatened
Species. Version 2013.2. Accessed August 2015. Available from: http://www.iucnredlist.org
Young CN, Schopmeyer SA, Lirman D. 2012. A review of reef restoration and coral propaga-
tion using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Mar
Sci. 88(4):1075–1098. http://dx.doi.org/10.5343/bms.2011.1143
Date Submitted: 23 October, 2015.
Date Accepted: 4 January, 2016.
Available Online: 28 January, 2016.
... We calculated the percentage coverage of each class inside each hexagon and then defined all hexagons as A. palmata that contained at least 0.2% (0.2 m 2 ) of the species. Our rationale was that this area conservatively equals a colony of 40 cm in diameter, which is the size at which the species has been observed to spawn (Chamberland et al. 2016). Any hexagon that exhibited less than the given area was classified as other reef substrate or sand, dependant on the dominant class within. ...
... These results imply that the initial distribution of biogenic structures greatly influences the potential of a location to serve as a structurally important restoration site and defines the spatio-temporal characteristics of each outplanting event. Allowing for adequate time of up to four years, or for outplants to show signs of sexual maturity, between restoration activities with A. palmata is important (Garcia-Urueña et al. 1996;Chamberland et al. 2016), though time span will certainly vary by species. Furthermore, outplant survival should be assessed on a rigorous basis, as well as any major changes to the overall distribution of the focal species. ...
Article
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Context Restoration is an effective measure to counteract declines of reef-building coral populations. Despite decades of coral restoration research and practice, very little emphasis has been placed on how the spatial distribution of restoration sites influences ecosystem recovery and connectivity. Objectives Combining image classification of aerial data with geoinformatics, we aim to identify priority restoration sites to increase the structural connectivity and fertilization potential of coral keystone species. Methods We focus on Acropora palmata at two natural reefs with contrasting spatial distributions of the species and include a hypothetical reef with a random distribution as a comparative baseline to represent a highly structurally degraded system. Priority sites are then identified at each reefscape through spatial modelling using three connectivity metrics from classical landscape ecology. Results Our models suggest that restoration sites joining or bordering major patches of A. palmata have the greatest potential to increase structural connectivity. Reefs of more degraded status are favourable for restoration because they exhibit a greater increase in connectivity metrics per area restored, while also maximizing the fertilization potential between colonies. Furthermore, the spatial extent that needs to be restored to achieve maximum efficiency is greatly dependent on the initial coverage and distribution of the species. Conclusions Our study demonstrates the importance of including spatial planning in the site selection process of coral restoration and provides a methodological framework that can aid in tailoring related strategies in accordance with the spatial arrangement of the target species.
... Remnant colonies-potentially representing genetically distinct individuals (genets, Box 1)-may survive via clonal reproduction but cannot fuel rapid adaptation to a changing climate unless sexual reproduction resumes. Restoration efforts (or, more precisely, rehabilitation efforts, (8)) are increasingly successful in generating sexually produced offspring from surviving genets (9), creating an opportunity to reinvigorate coral populations by allowing selection to act on recombined genotypes. However, it remains unclear exactly how to apply breeding to maximize the long-term success of coral restoration, in part because goals vary, from shifting mean trait values of a population in a certain direction (e.g., breeding a heat-tolerant or disease-resistant coral), to demographic rescue through increased fecundity (regardless of other traits), or reversing the loss of genetic (allelic) diversity (Box 1). ...
... 8. Develop multi-stress assays to evaluate success of managed breeding programs. 9. Identify and then reduce unintended genetic bottlenecks during managed breeding. ...
Preprint
As climate change intensifies, a primary role of coral restoration is to maintain genetic diversity and ecosystem function while preventing species extinction, at least until global measures to slow the rate of climate change take effect. Recently, the idea of selectively breeding corals with higher heat tolerance (sometimes called “super corals”), and using them to repopulate reefs, has gained wide attention. We outline several reasons why selective breeding for heat tolerance alone is unlikely to yield corals that could be used universally for restoring natural reefs. We propose a managed breeding strategy where a range of traits is considered when choosing corals for breeding and where success is more likely when young offspring bred for these traits are exposed to natural selection in the wild, rather than to artificial selection in nurseries or tanks. However, as extinction risk increases, managing to increase population size becomes the primary goal and all causes of mortality may need to be minimized. In light of these considerations, there is an urgent need to formulate genetic management plans that consider demographic and genetic information for each population under restoration.
... In the Caribbean Diploria labyrinthiformis is a common and frequently encountered coral species. Depending on its location, this species can spawn from April to October before sunset, having a wider and earlier spawning window compared to most broadcast spawning corals in the region (Weil and Vargas, 2010;Chamberland et al., 2016). D. labyrinthiformis was selected for this study due to its ability to build 3D structures in reefs, its early and multiple spawning events throughout the year, its high spawning predictability, and the contribution to recent and ongoing research regarding its reproductive potential and early life history stages (Chamberland et al., 2016). ...
... Depending on its location, this species can spawn from April to October before sunset, having a wider and earlier spawning window compared to most broadcast spawning corals in the region (Weil and Vargas, 2010;Chamberland et al., 2016). D. labyrinthiformis was selected for this study due to its ability to build 3D structures in reefs, its early and multiple spawning events throughout the year, its high spawning predictability, and the contribution to recent and ongoing research regarding its reproductive potential and early life history stages (Chamberland et al., 2016). FUNDEMAR has been monitoring and documenting spawning events of this species at the Playita reef site since May 2017, producing a spawning prediction calendar for 2020 including this and 7 other coral species (Sellares-Blasco et al., 2021). ...
... To date, published observations of spawning in outplanted Atlantic acroporid species have only been reported in the Caribbean (Carne et al., 2016;Chamberland et al., 2016;Calle-Triviño et al., 2018). However, there have been no reports in Florida of spawning activity by outplanted A. palmata. ...
... In 2022, we observed spawning activity among A. palmata colonies outplanted in March 2018, indicating that nursery-raised fragments outplanted to Florida reefs can become reproductively mature in as little as four years and four months (52 months) after outplanting. This is consistent with the observation of A. palmata outplants spawning~60 months post outplanting in Belize (Carne et al., 2016) and four-year-old (48 months) sexual recruits of A. palmata being reproductively mature in Curacao (Chamberland et al., 2016) and other species of acroporids spawning at 4-5 years old (Calle-Triviño et al., 2018;Ligson and Cabaitan, 2021). ...
Article
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Here, we provide the first reports of spawning activity by Acropora palmata colonies outplanted to reefs in Florida, USA. In 2020, we observed light spawning from A. palmata colonies five years after they had been outplanted on two Florida reefs. In 2021 and 2022, we observed outplanted A. palmata colonies spawning synchronously with other nearby (<3 m) outplants and wild colonies more than 100 m away. During the 2022 spawning event, some colonies spawned in as few as four years after they had been outplanted. Among all spawning seasons, gametes collected from the outplanted colonies yielded high fertilization rates and viable larvae. These observations are promising for A. palmata restoration as they indicate fragments of A. palmata can spawn four years after outplanting and that efforts to restore A. palmata may be close to achieving the first step towards self-sustaining populations that can produce viable larvae, resulting in an increase in the population’s genotypic diversity upon successful recruitment to the reef.
... Coral nurseries therefore also provide a time and cost-effective approach to augment sexual reproduction through accelerated maturation, but whether this comes at a cost to other life-history traits such as propagule or egg energetics remains unknown. Both asexually and sexually generated propagules (herein also known as coral material) can be returned to the reef through restoration workflows, such as outplanting (Boström-Einarsson et al. 2020;Suggett et al. 2019) or larval "seeding" (Heyward et al. 2002;Omori 2005), but also naturally via fragmentation or sexual reproduction of mature outplanted colonies (Chamberland et al. 2016;Guest et al. 2023). As such, it is important to understand reproductive and physiological traits of coral material propagated for restoration to validate how this biomass can contribute to reef resistance, recovery and function of any given coral population. ...
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Coral restoration efforts have rapidly increased worldwide, including the development of several programmes on the Great Barrier Reef (GBR) in recent years. While many restoration programmes utilise in-water nurseries to accelerate coral biomass yields, the impact of nursery environments on propagule quality has not been examined despite the importance of coral fitness for ensuring resistant populations. Here, we investigated two fitness indicators (lipid diversity and tissue protein abundance) of Acropora millepora adults and eggs grown on coral nurseries versus native reef on the GBR, with adults assessed at two sites (Blue Lagoon and Rayban) and eggs assessed at one site (Blue Lagoon). Lipid profiles of adult colonies varied by site and origin (nursery versus wild reef), with adult nursery corals exhibiting an elevated relative abundance of storage lipids (diacylglycerols and triacylglycerols) and lipid classes responsible for regulating membrane structure (phosphatidylcholines and sterol esters), while wild corals were characterised by a greater relative abundance of fatty acids and classes involved in immunoregulation. Comparing eggs from different origins, nursery offspring were richer in energy-storing triacylglycerols, as well as ceramides and phosphatidylcholines essential for membrane structure, while wild eggs had a greater relative abundance of wax ester species also important for energy storage. No differences were found in total protein abundance (adult or eggs) or egg physical characteristics (count and size) between nursery and wild origins. Variations in lipid profiles are consistent with differences in environmental conditions between reef sites and origin (nursery versus wild), highlighting the need to consider site selection and propagation conditions when planning restoration projects. Importantly, these findings demonstrate that the lipid classes with the highest relative abundance in A. millepora nursery and wild eggs differed from those in adults from the same origin, suggesting that propagation origin is more important for driving lipid profiles in coral eggs compared to parental effects.
... Moreover, A. palmata is one of the fastest-growing Caribbean coral species (Gladfelter et al. 1978), can proliferate clonally to occupy large areas of reef (i.e. 100s m 2 ; Baums et al. 2005), and can reach sexual maturity at the age of 4 (Chamberland et al. 2016). The 23 juveniles generated over the course of this study are therefore expected to rapidly form structurally complex habitats (≥1 m 2 surface area) and to participate in natural spawning events within 5 yr. ...
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The functional extinction of the herbivorous sea urchin Diadema antillarum in the 1980s has contributed to the degradation of Caribbean coral reefs. In the early 2000s, recovering populations of D. antillarum were observed in several locations with mixed consequences for coral recruitment: D. antillarum improved habitat quality for settling coral larvae and recruits, but also contributed to settler mortality through (incidental) predation. To determine the relative importance of both mechanisms, tiles were deployed in the absence and presence of naturally occurring D. antillarum aggregations (2.0-2.8 sea urchins m ⁻² ) in Curaçao, after which benthic community composition, ex situ settlement, and long-term (2.5 yr) in situ post-settlement survival of Acropora palmata larvae were quantified. After 3 mo, the presence of D. antillarum resulted in 44% more crustose coralline algae and 52% less turf algae, and a 75% canopy height reduction on the tiles’ exposed habitats. On the cryptic undersides of the tiles, the presence of D. antillarum was linked to lower abundances of sessile invertebrates and macroalgae. Larval settlement was almost 2 times higher on tiles conditioned in the presence of D. antillarum , with a strong preference (>70%) for the cryptic sides of tiles. Settlers returned to areas of reef encompassing D. antillarum populations were twice as likely to survive to the age of 2.5 yr. These findings support the beneficial role of D. antillarum in promoting coral recruitment by creating preferred settlement habitat and by increasing settler survival, and could be leveraged to improve coral restoration practices through dual-species conservation and/or co-culture strategies.
... Subsequent culturing within facilities may facilitate larger scale production of larvae for restoration in the future. Despite demonstrated success in producing breeding Acropora corals with these methods (Baria et al., 2012;Chamberland et al., 2016;Harrison et al., 2021) there remains a dearth of long-term data that demonstrates the overall efficacy of these techniques in contributing to self-sustaining populations for most coral species. We recommend immediate investments to determine the rate of recruitment, post-recruitment survival, and demographic effects on local populations resulting from large-scale, multiple species techniques including larval slick relocation, as these data are critical in evaluating the return on these efforts. ...
... Coral larval propagation may involve seeding competent larvae directly to reef substratum (Heyward et al. 2002;Edwards et al. 2015;dela Cruz and Harrison 2017) or settling larvae onto appropriate substrates for rearing and subsequent outplant (Nakamura et al. 2011;Villanueva et al. 2012;Guest et al. 2014;Chamberland et al. 2017). The feasibility of producing a first filial generation (F1) and rearing these until maturity in situ has been demonstrated for several competitive coral taxa (e.g., Iwao et al. 2010;Baria et al. 2012;Chamberland et al. 2016;Ligson and Cabaitan 2021). While research is ongoing to develop coral larval propagation for other life history groups (e.g., Marhaver et al. 2015;O'Neil et al. 2021), only one study to date has reported long-term outcomes of sexual propagation for a massive coral (Bonilla et al. 2021). ...
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