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

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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.
... Reproduction in corals consists of a sequence of events which include gametogenesis, spawning (for spawning species), fertilization, embryogenesis, planulation, dispersal, settlement, and recruitment (e.g., Harrison and Wallace, 1990;Baird et al., 2009;Harrison, 2011). These events have been described from different perspectives, including histological (e.g., Duerden, 1902;Fadlallah, 1983;Szmant, 1986;Richmond and Hunter, 1990;Soong, 1991;Steiner, 1998;Morales, 2006;Ritson-Williams et al., 2009;Weil and Vargas, 2010;Harrison, 2011;Soto and Weil, 2016), observational (e.g., Vermeij et al., 2003;Levitan et al., 2004;Van Woesik et al., 2006;Vize, 2006;Bastidas et al., 2012;Chamberland et al., 2016;Keith et al., 2016;Fogarty and Marhaver, 2019), and experimental (e.g., Morse et al., 1988;Webster et al., 2004;Kuffner et al., 2006Kuffner et al., , 2007Nugues and Szmant, 2006;Vermeij et al., 2009;Ritson-Williams et al., 2010;Marhaver et al., 2015;Sharp et al., 2015) studies. ...
... Currently, Coralium lab at the National Autonomous University of Mexico, SECORE International and the Caribbean Research and Management of Biodiversity (CARMABI) are three leading institutions in the Caribbean on this subject. These institutions have played an important role in expanding larval propagation across geographies, improving capacity building, and developing cutting edge technology and protocols applied for coral restoration (e.g., Marhaver et al., 2015;Chamberland et al., 2016Chamberland et al., , 2017Banaszak pers. comm.). ...
... We find these 3 points to be essential to create a robust and scalable program: (1) alliances with private and local stakeholders, (2) financial stability, and (3) adoption of novel technology supported by pertinent training to implement them. In our view, the balance between these components allowed FUNDEMAR to build the laboratory and produce results comparable to others in the Caribbean (Chamberland et al., 2016(Chamberland et al., , 2017. Local engagement and key alliances between different stakeholders and the scientific community has been shown to be a strong pillar that supports conservation actions aimed to preserve coastal marine ecosystems (White and Vogt, 2000;Lundquist and Granek, 2005;Reyes-García et al., 2019). ...
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Coral assisted fertilization, larval rearing and recruit propagation success in significant ecological scales, largely depend on scaling up and replicating these efforts in as many regions as possible. The Dominican Foundation for Marine Studies (FUNDEMAR) has become a pioneer of these efforts in the Dominican Republic, being the first institution to successfully implement coral sexual reproduction techniques in the country and establishing the first mobile larvae culturing facility. Here we share our perspective on three main components behind the success of FUNDEMAR’s program: (1) a self-sustainable program in alliance with local and international organizations, (2) the design and construction of the first Coral Assisted Reproduction Laboratory in the country, and a (3) clearly defined scalable structure for outcome performance. Two years after program implementation, FUNDEMAR has successfully produced an annual regional coral spawning prediction calendar, cultured seven coral species, and seeded over 4,500 substrates with more than 268,200 sexual coral recruits in approximately 1,880 m2 reef areas. Here, we provide a detailed description of a fully functional assisted coral reproduction program, including the lessons learned during its implementation as well as a series of specific solutions. We hope this work will help and inspire other countries and small institutions to replicate FUNDEMAR’s coral assisted reproduction program components and contribute to the expansion of sexual coral restoration efforts in the Caribbean.
... While high survival of sexually propagated A. cervicornis reared on land is a recent development (Henry et al. 2019), coral recruits of varying origin have been used in restoration for over 30 years (Fucik et al. 1984;Richmond and Hunter 1990;Chamberland et al. 2015Chamberland et al. , 2016Doropoulos et al. 2019). Historically, several methodologies have used coral recruits to restore degraded reefs. ...
... These include transplantation of nearly gravid corals to degraded reefs (Fucik et al 1984;Richmond and Hunter 1990) and harvesting wild spawn slicks (Doropoulos et al. 2019;Tabalanza et al. 2020). Furthermore, sexually propagated A. palmata has been used for restoration in the Southern Caribbean (Chamberland et al. 2015(Chamberland et al. , 2016. ...
... Although survival was low for Chamberland et al. (2015), associated cost was greatly reduced by minimizing the land-based period (outplanting two weeks after settlement) and distributing corals on clay tripods affixed using nylon rope and zip-ties. The same group also raised A. palmata on land for one year and had several of these colonies survive and spawn three years after being outplanted (Chamberland et al. 2016). In comparison, we found up to 95% survival 16 months post-outplant in corals reared ex situ for eight months. ...
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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.
... However, for most coral species, little is known about corals' early life stages i.e., the period when these organisms have higher mortality rates (Vermeij and Sandin 2008;Doropoulos et al. 2016).This is especially true for the pre-settlement period, when larvae swim in the water column seeking an appropriate substrate to settle, since they can perish due to energy storage depletion (Vermeij 2006). Studying the early life stage ecology of speci c coral species is key for understanding its contribution to the current and future composition of reefs (Chamberland et al. 2016). Therefore, identifying the factors that affect larval recruitment success can inform management decisions aimed at reducing the decline of coral reefs and improve restoration efforts through sexual propagation. ...
... Diploria labyrinthiformis is a common coral species in the Caribbean and, depending on its location, 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. 2017). 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). ...
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... Colony age and size determine the sexual maturity in corals (Hall & Hughes 1996). In the present study, most of the remaining A. verweyi coral outplants were reproductively mature at four years post-outplantation, which is within the range of 3 -5 years that is observed in various acroporid species (Iwao et al. 2010;Baria et al. 2012;Chamberland et al. 2016;dela Cruz & Harrison 2017). Interestingly, the smallest size (mean diameter) of sexually mature A. verweyi coral outplants in this study was 11.8 cm. ...
... Several of the larger colonies were likely larger than 11.8 cm diameter at age 3 and thus might have matured the previous year. The results here further support other studies suggesting sexual maturation is achieved upon reaching a specific size, which varies among species (Iwao et al. 2010;Baria et al. 2012;Chamberland et al. 2016;dela Cruz & Harrison 2017). Upon reaching sexual maturity, these coral outplants become valuable sources of gametes, especially with their high fecundity (Harrison 2011). ...
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Most coral reef restoration efforts are carried out over 1–2 years, and few have assessed long term (over 3 years) outcomes. Although, studies of outplantation of sexually propagated corals have reported promising initial results, few studies have followed outplanted corals to maturity. Here, we monitored sexually propagated Acropora verweyi corals for four years post‐outplantation to determine their survival and sexual maturity. These corals were outplanted when four months old in two size classes (small = 0.3–0.5 cm; large = 1.0–1.5 cm) at two sites in the northwestern Philippines. Four years after outplantation, the 240 colonies of A. verweyi exhibited 17.9% survival, with mean diameters ranging from 7.48–26.8 cm. Most of the surviving outplants were gravid (81.4% of the 43 colonies) with mean diameters of at least 11.8 cm. Higher survivorship was detected in the initial large size class outplants than in the small ones at the natal site, but not at the other site. However, four years after outplantation there was no significant difference in terms of geometric mean diameter between the initial size classes or between the sites. Results show that 4‐mo old outplants of sexually propagated corals can survive until sexual maturity and are already capable of contributing gametes for the potential recovery of degraded coral communities at age four years. This article is protected by copyright. All rights reserved.
... Losses of genetic diversity over the course of larval development in ex situ cultures are well illustrated in a lab-bred Acropora palmata cohort on the Caribbean island of Curaçao. This now 10-year-old restored and sexually mature (Chamberland et al. 2015;Chamberland et al. 2016) population of 11 colonies is partially composed of half-siblings and full siblings (Kitchen et al. 2020, Conn et al., unpublished data, Fig. 3.1). That is despite the initial mixing of hundreds of thousands of wild-caught gametes spawned by at least seven colonies on three different nights and on two reefs. ...
Chapter
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... Coral growth rates, however, can vary considerably making it difficult to establish both age and size at sexual maturity in naturally occurring colonies. Only a few studies have sexually propagated corals and reared them until sexual maturity to establish the exact age at onset of maturity, and to date, this has only been done for fast-growing Acropora Baria et al. 2012;Guest et al. 2014;Chamberland et al. 2016;dela Cruz and Harrison 2017;Craggs et al. 2020). Information on colony size and age at first reproduction of most slow-growing massive species as well as fecundity across different size classes are mostly lacking despite their important implications on coral population dynamics and demography. ...
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... Still, the knowledge about the bacterial population structures during larval development of Acropora humilis in the Southeast Asia has not been deciphered. The cultivation of corals using sexual reproduction technique is relatively new in the past decade with different levels of success depending on sites [33][34][35][36][37] , and we are one of the pioneer groups who have actually been successfully cultivating corals using gametes and have successfully been using our cultured baby corals to restore degraded reefs in Thailand. Here, A. humilis can be a model coral species since this species is a predominant species not only in Thailand but also in the tropical regions, particular in the Southeast Asia. ...
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Polyp age and colony size determine the onset of sexual maturity in scleractinian corals (Hall and Hughes 1996), and this has important ecological and evolutionary implications as it influences rates of adaptation and trade-offs between growth and reproduction. Colony age is normally estimated based on size (e.g., Wallace 1985); however, corals have highly variable growth rates and may undergo fission and fusion, making it difficult to accurately determine age based on size alone (Hughes and Jackson 1985). Here we examined sexual maturity in a single cohort of 3-yr-old colonies of Acropora millepora (Ehrenberg, 1834) that had been reared at Bolinao Marine Laboratory from larvae (A, arrows: newly settled spat reared in 2008) settled to artificial substrates in an outdoor hatchery, and subsequently transferred to an in situ nursery. By 2011, three out of 12 colonies transplanted to natural reef after 6 mo of rearing in the nursery and 17 out of 19 colonies that remained in the nursery (B) were sexually mature (C, arrow: mature pigmented oocytes visible in fractured branches). Gravid colonies had mean diameters ranging from 14.4 to 28.3 cm in the nursery and from 12.3 to 13.7 cm on the reef, whereas colony mean diameters in non-gravid colonies ranged from 11.8 to 13.5 cm in the nursery and 7.8 to 11.0 cm on the reef, indicating that spawning can occur at 3 yrs of age provided colony mean diameter is ≥ 14.4 cm in the nursery and ≥ 12.3 cm on the reef. Four gravid colonies were collected from the nursery and observed to spawn synchronously on the night of the full moon (20 March, 2011) between 20:30 and 21:30 hrs at the land based hatchery (D). This is the first report to confirm Wallace's (1985) estimate of onset of sexual maturity in Acropora at 3 yrs of age, 1 yr sooner than the previous observation for Acropora tenuis (Dana, 1846) colonies reared from gametes (Iwao et al. 2010). Our finding further demonstrates the potential for relatively short generation times in Acropora and highlights the difficulties in estimating age from