BULLETIN OF MARINE SCIENCE. 88(4):10751098.

2012

1075
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A REVIEW OF REEF RESTORATION AND CORAL
PROPAGATION USING THE THREATENED GENUS ACROPORA
IN THE CARIBBEAN AND WESTERN ATLANTIC
CN Young, SA Schopmeyer, and D Lirman
ABSTRACT
Coral reef restoration has gained recent popularity in response to the steady
decline of corals and the recognition that coral reefs may not be able to recover
naturally without human intervention. To synthesize collective knowledge about
reef restoration focused particularly on the threatened genus Acropora in the
Caribbean and western Atlantic, we conducted a literature review combined
with personal communications with restoration practitioners and an online
questionnaire to identify the most eective reef restoration methods and the major
obstacles hindering restoration success. Most participants (90) strongly believe
that Acropora populations are severely degraded, continue to decline, and may not
recover without human intervention. Low-cost methods such as coral gardening
and fragment stabilization were ranked as the most eective restoration activities
for this genus. High nancial costs, the small footprint of restoration activities,
and the potential damage to wild populations were identied as major concerns,
while increased public awareness and education were ranked as the highest benets
of coral reef restoration. Tis study highlights the advantages and outlines the
concerns associated with coral reef restoration and creates a unique synthesis of
coral restoration activities as a complementary management tool to help guide
best-practices for future restoration eorts throughout the region.
Worldwide coral reef degradation has reached a point where local conservation
strategies and natural recovery processes alone may be ineective in preserving and
restoring the biodiversity and long-term integrity of coral reefs (Goreau and Hilbertz
2005). Faced with the prospect of limited natural recovery due to low rates of sexual
recruitment, low recruit survivorship, and highly variable reproductive and settle-
ment events (Kojis and Quinn 2001, Bruckner 2002, Acropora Biological Review
Team 2005, Quinn and Kojis 2005), researchers and managers are turning to active
reef restoration as a potential mechanism to both mitigate declining patterns and
enhance potential recovery of damaged or depleted coral populations (Guzman 1991,
Rinkevich 2005, Precht 2006, Edwards and Gomez 2007). While active restoration
is a widely accepted practice for wetlands (Zedler 2000), saltmarshes (Laegdsgaard
2006), oyster reefs (Coen 2000, Coen et al. 2007), mangroves (Field 1999, Lewis 2005),
and seagrasses (Torhaug 1986), the eld of coral reef restoration is relatively new,
highlighting the pressing need to formulate, evaluate, and disseminate eective and
cost-ecient methodologies and management strategies to interested stakeholders.
During its infancy, reef restoration focused mostly on structural or engineering so-
lutions to repair natural breakwaters that protect valuable coastlines from erosion or
restoring structural integrity and topographical complexity to reefs damaged by ship
groundings and blast shing (Precht 2006). Articial structures, such as Reef Balls
(www.reefball.org), have been designed to provide shoreline protection and prevent
KZ>Z&WWZ
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1076
beach erosion while also creating substrate for natural recruitment and attachment
of benthic organisms such as corals and sponges. However, in the 1970s1980s, res-
toration eorts began to focus on restoring the biological and ecological function of
coral reefs by transplanting coral fragments or colonies (Maragos 1974, Bouchon et
al. 1981, Abelson 1982, Harriott and Fisk 1988). Large-scale ecological coral restora-
tion projects were rst conducted in the Indo-Pacic and the Red Sea in the 1990s
(Rinkevich 1995, Oren and Benayahu 1997, Treeck and Schuhmacher 1997).
At present, one of the most commonly used coral propagation and restoration
methods is coral gardening (Rinkevich 1995, Bowden-Kerby 2001, Epstein et al.
2003, Shar et al. 2006, Shar and Rinkevich 2008, Shaish et al. 2008). Tis meth-
od, adapted from terrestrial silviculture, consists of removing a limited amount of
tissue and skeleton (from a few polyps to small branches) from healthy wild coral
populations and propagating an initial stock within in situ or ex situ coral nurser-
ies. Nursery-grown colonies produce a sustainable stock of corals which can then
be transplanted to degraded reefs (Rinkevich 1995, 2005, Epstein et al. 2001, 2003,
Soong and Chen 2003). Developed initially in the Indo-Pacic and Red Sea regions,
coral gardening methods have been increasingly implemented in the Caribbean
(see Table 1), where eorts have targeted almost exclusively the branching corals
Acropora cervicornis (Lamarck, 1816) and Acropora palmata (Lamarck, 1816), which
were once the dominant reef-building taxa in the region. Due to the combination
of biological and anthropogenic stressors, Acropora has suered signicant degra-
dation with estimated population declines of up to 95 in some areas (Porter and
Meier 1992, Bruckner 2002), leading to their listing as threatened in the US under
the Endangered Species Act in 2006 (Hogarth 2006) and as critically endangered in
the International Union for Conservation of Nature (IUCN) Red List of Treatened
Species in 2008 (Aronson et al. 2008, Carpenter et al. 2008).
Acroporid corals are critically important for reef growth, island formation, sh-
eries habitats, and coastal buering. Both acroporid species exhibit particularly
high growth rates relative to other corals (Goreau and Goreau 1959, Shinn 1966,
Glynn 1973, Gladfelter et al. 1978), enabling sustained reef growth during previous
sea level changes. Additionally, both species exhibit unique branching morpholo-
gies, providing essential habitat for other reef organisms. Tus, it is unlikely that any
other Caribbean reef-building species is capable of fullling these specic ecosystem
functions. Terefore, it is probable that the continued decline of Acropora will cause
considerable losses in reef function and structure (Acropora Biological Review Team
2005).
To combat the decline of Caribbean acroporid corals and assist in their recovery,
an increasing number of practitioners are conducting restoration and propagation
activities with this genus (Bruckner and Bruckner 2001, Quinn et al. 2005, Quinn
and Kojis 2006, Herlan and Lirman 2008) and extensive, albeit largely unpublished
or undocumented, collective knowledge exists on the eectiveness of such activities.
Acropora species are considered good candidates for use in restoration or population
enhancement projects due to their high growth rates, natural use of fragmentation
for asexual reproduction, ability to heal rapidly from wounds, and high survivorship
of fragments as compared to other coral species (Gladfelter et al. 1978, Tunniclie
1981, Bak and Criens 1982, Highsmith 1982, Lirman et al. 2010). In the present study,
we use a combination of literature and case-study reviews, personal communications
with restoration practitioners, and an online questionnaire to formally compile the
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1077
collective knowledge of the coral restoration community on the status of reef resto-
ration activities in the Caribbean region. We concentrate on Acropora restoration
and propagation projects to provide a review of methods used, as well as lessons
learned from these activities.
While reviews and manuals based on reef restoration projects in the Pacic have
been already published (Jaap 2000, Omori et al. 2004, Rinkevich 2005, Edwards and
Gomez 2007, Edwards 2010), only one restoration manual exists for the Caribbean
(Johnson et al. 2011). Our study complements this manual by providing a full review
and analysis of reef restoration projects in the Caribbean, and more specically, proj-
ects related to the threatened Caribbean Acropora species. Due to the unfortunate
paucity of published literature and data regarding reef restoration in the Caribbean,
this study lls important knowledge gaps by collecting information from any and
all available sources (published and gray literatures). By synthesizing this collective
information, we determined the restoration methods that have proven the most cost-
eective and ecient, as well as which factors are having the highest impact on reef
restoration success rates.
Mv:noos
Te present study included two main activities: (1) a literature review of propagation and
restoration projects with an emphasis on those focused on the threatened genus Acropora in
the Caribbean, and (2) an online questionnaire developed to compile up-to-date collective
knowledge and opinions of reef restoration researchers and practitioners.
Te literature review was conducted to identify dierent types of coral reef restoration
projects implemented in the Caribbean. Information was gathered using database mining
of the web, review of published materials and gray literature, postings in email groups, and
personal communications. Practitioners received identical emails requesting project sum-
mary information (i.e., site location, species used, methods, highlights, recommendations,
concerns, and disturbance factors) and lessons learned (what worked and what did not work).
Basic summary statistics were compiled to identify patterns and trends in topics such as
propagation and restoration methodologies, coral reef restoration concerns, and recommen-
dations. Personal contacts (conducted in the native language of the respondent) were made
only in cases where basic project information (i.e., location, dates, species used, methods,
survivorship and growth, disturbance factors) were missing or not available from the sources
reviewed, and only missing data were requested during these communications.
Finally, an online questionnaire was drafted to elicit expert opinions among Caribbean coral
reef restoration researchers, scientists, managers, and gain perspective from other restoration
participants such as students, volunteers, and industry professionals (Online Appendix 1). Te
instrument was posted on email list-servers, including the Caribbean Conservation group,
Acropora group, and the National Oceanic and Atmospheric Administration (NOAA) Coral
List. In addition, this instrument was introduced at the Acropora Conservation and Restoration
Workshop in Washington, DC (November 1213, 2009), to encourage practitioners to partic-
ipate. Te questionnaire requested information such as personal background and education
level, coral reef restoration experience, familiarity with propagation and restoration methodolo-
gies, restoration concerns, and recommendations. Te questionnaire was designed to identify
emergent issues and concerns and provide recommendations from restoration practitioners
that may aect the outcomes of coral restoration projects.
Every eort was made to distribute the questionnaire to a wide audience, and not only
target practitioners that were actively working in this eld, but also those who were critical of
restoration eorts. Te questionnaire was posted twice during a period of 3 mo after which all
responses were analyzed. Responses were statistically analyzed (one-way ANOVA on ranks)
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1078
to determine if answers were potentially inuenced by respondent aliation [i.e., academic,
government, non-government organization (NGO), etc.] or level of experience based on num-
ber of years involved in reef restoration. If no statistical dierences were detected among
groups, data were pooled for further analyses.
It is important to highlight some caveats of this questionnaire and its interpretation. While
every eort was made for the questionnaire to reach a wide audience, no information is avail-
able on the actual size of the population of restoration practitioners and, thus, it is impossible
to know the proportion of the total population that the 79 respondents represent. Terefore,
it is unclear how representative of the whole population this sample is. Also, common survey
design errors such as sampling, non-response, and non-coverage errors could not be quanti-
ed, precluding the implementation of correction factors and weighing techniques applied in
more formal surveys (Dillman 1991, 2007). While these issues limit the extrapolation of gen-
eral conclusions about the value and benets of reef restoration beyond the group sampled, we
believe that the review of methodologies is robust and represents the best-available compila-
tion of collective knowledge on the topic of reef and Acropora restoration in the Caribbean
region. By asking practitioners to limit their rankings of methodologies to those that each
respondent had actually tested, we are able to provide a synthesis of expert knowledge on
these issues.
Rvsui:s
Cvinnv A Rvs:ov:io Pvoivc:s.Over 60 Acropora restoration
projects were identied from 14 Caribbean countries and island nations as part of
this review (Fig. 1, Table 1). Of these projects, 48 used A. cervicornis, 12 used A.
palmata, and 40 used both Acropora species. Te coral gardening methodology
was the pre-eminent method used in 63 of projects for the propagation of this ge-
nus. Within coral nurseries, Acropora fragments have been grown on frames, ropes,
cinderblock platforms, Reef Balls, oating structures, and through electrolysis pro-
cesses known as the BioRock method (Table 2, Figs. 2A, 3). Te use of metal frames in
propagation projects was the most common methodology since stainless steel mesh
is readily available, relatively inexpensive, experiences reduced corrosion, and is resis-
tant to storm damage. Te propagation of Acropora on metal frames has been shown
to be successful with most projects documenting 6395 survival. Additionally,
increased survival (8697.5), coral growth (up to 21.0 cm
1
), and reduced preda-
tion have been documented when propagating fragments on suspended mid-water
line nurseries, which were used in 42 of projects (Bowden-Kerby et al. 2005, Quinn
and Kojis 2006, Johnson et al. 2011, Nedimyer et al. 2011, Fig. 3B). Practitioners of-
ten recommended that prevention of predation and regular maintenance are vital to
coral survival within coral nurseries.
While some projects (12.5) focused on simple fragment stabilization or trans-
plantation of corals onto natural reefs after physical disturbances such as ship
groundings or storms (Garrison and Ward 2008, Bruckner et al. 2009), almost 60 of
projects outplanted nursery-grown corals onto degraded reefs or articial structures
as a nal restoration step (Hernndez-Delgado et al. 2001, Johnson et al. 2011). A va-
riety of attachment platforms were used for outplanting corals, including Reef Balls,
cement pucks, and concrete rosettes (Table 1, Fig. 3). In addition, coral fragments or
colonies were transplanted directly onto the reef substrate using cement, underwater
epoxy, plastic cable ties, metal wire, nails, bolts, or direct wedging into crevices (Fig.
2B). Many studies found the use of small plastic cable ties to be a cheap, quick, and
eective method for attaching corals to articial or reef substrate (Bruckner et al.
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1079
2009, Forrester et al. 2010, Williams and Miller 2010, Johnson et al. 2011, Garrison
and Ward 2012). In the Caribbean, Reef Balls have been used specically for trans-
planting Acropora in 22 of projects. Larval seeding (5 of projects) has only been
used in a limited number of studies to restore depleted reefs, but is often expen-
sive, time consuming, and with limited success (Sammarco et al. 1999, Precht 2006).
Many projects in the Caribbean have used more than one propagation method to
culture coral fragments and multiple attachment methods to ensure restoration suc-
cess based on specic local environmental conditions (Bowden-Kerby et al. 2005,
Quinn et al. 2005, Williams and Miller 2010, Johnson et al. 2011).
Due to the paucity of published literature documenting the status of Acropora
nursery programs in the Caribbean, most available information was mined from
project pages provided by nursery and restoration practitioners (see Table 1). Overall,
nursery programs throughout the Caribbean have been highly successful in increas-
ing the biomass of Acropora after limited tissue collections from wild donor popu-
lations. High survivorship (>70) of coral fragments has been found within coral
nurseries during the rst year of propagation. Coral mortality was often due to storm
damage or other disturbances such as temperature anomalies (Hernndez-Delgado
et al. 2001, Quinn and Kojis 2006, Schopmeyer et al. 2011), although predation and
poor water quality have also been identied as factors leading to mortality of nursery
corals indicating that success rates of nurseries are highly site-specic. For exam-
ple, in Puerto Rico and the Dominican Republic, cumulative survival of A. cervi-
cornis propagated on metal A-frames was 6595 during the rst year, whereas a
coral nursery established using the same methods in Guanaja, Honduras, suered
Figure 1. Map of the Caribbean, western Atlantic, and Gulf of Mexico with the location of
Acropora restoration and propagation sites identifed in this review.
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1080
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)
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1081
T
a
b
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1
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BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1084
100 mortality within the rst year due to poor water quality. Biomass increases of
60219 have been recorded within coral nurseries and practitioners have found
that utilizing larger Acropora fragments (>5 cm) promotes higher survivorship and
productivity than with smaller fragments (Bowden-Kerby 2001, Herlan and Lirman
2008, Lirman et al. 2010). With the success of such propagation techniques, many
restoration practitioners are expanding the size of coral nurseries and some cur-
rently house >10,000 corals providing a large source of corals for use in restoration
activities (K Nedimyer, Coral Restoration Foundation, pers comm).
Te literature review revealed high variability in the level of success of restoration
activities throughout the Caribbean. In studies including coral transplantation as
part of their restoration strategy, fragment survival ranged between 43 and 95
during the rst year with some studies documenting an increase in biomass of up to
250 for transplanted Acropora (Quinn and Kojis 2006, Table 1). In other studies,
>50 fragment mortality was observed within the rst year typically due to fragment
dislodgement or storm damage, and mortality often increased to 80100 after 5
yrs (Bruckner et al. 2009, Garrison and Ward 2012). However, fragment stabilization,
especially with cable ties or underwater epoxy, signicantly increases the survival
of transplanted corals (Williams and Miller 2010) and most corals were observed
to begin sheeting live tissue over attachment substrates within 3 mo of transplant-
ing. Similar to propagating fragments within coral nurseries, transplanting larger
fragments (>5 cm) resulted in higher growth rates and survivorship of outplanted
acroporids. Mortality rates of transplanted corals were similar to those of reference
or wild colonies showing that once transplanted, nursery-reared corals respond to
environmental factors just as wild colonies (Garrison and Ward 2008, Forrester et
al. 2010). Tus, many studies stressed the need to identify the underlying causes of
coral mortality and reef degradation and address such issues to ensure the success of
restoration activities.
Te top three concerns presented by practitioners for the fragment stabilization or
nursery phases of reef restoration activities were: (1) physical damage caused by waves
and storms, (2) predation, and (3) competition by algae and other space competitors
(i.e., sponges, bryozoans, tunicates, etc., Fig. 2C). Increased wave action and storms
can cause fragment breakage and dislodgement as well as damage to the restoration
structures (Bowden-Kerby 2001, Franklin et al. 2006, Wells et al. 2010). Strategic
placement of nurseries in areas with reduced wave exposure was suggested as a way
to mitigate physical damage. Te use of rope nurseries that can be moved to deeper
water in advance of a major hurricane also provides protection to nursery stocks
(Johnson et al. 2011). Predation by corallivorous snails [Coralliophila abbreviata
(Lamarck, 1816)] and reworms [Hermodice carunculata (Pallas, 1766)] and coral
mortality caused by the gardening activities of territorial damselsh were highlight-
ed as major causes of mortality to corals and most studies recommended periodic
removal of predators to limit coral mortality during both nursery and outplanting
phases (Hernndez-Delgado et al. 2001, Miller et al. 2010). Utilizing mid-water rope
nurseries that provide limited access for benthic predators was also suggested as a
method to help minimize predation. Macroalgal overgrowth was highlighted as a
concern in most projects and active removal of macroalgae and other fouling or-
ganisms (i.e., cyanobacteria, sponges, hydroids) was highly recommended to ensure
survival of coral fragments andior transplants (Forrester et al. 2010, Johnson et al.
2011). Other sources of concern for reef restoration ascertained from the literature
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1085
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BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1086
review included coral diseases and temperature anomalies, as well as increased nu-
trients and sedimentation. Some of these issues can be addressed by strategically
placing nurseries and restoration sites away from land-based sources of pollution,
within marine protected areas, andior in deeper habitats where temperature impacts
may be lessened (Johnson et al. 2011, Schopmeyer et al. 2011). Additionally, studies
show that avoiding fragmentation and outplanting activities during warm summer
months when water temperatures and bleaching prevalence are higher increases
fragment survival.
Rvvr Rvs:ov:io Quvs:ioivv.Seventy-nine coral reef restoration prac-
titioners responded to the questionnaire. Te most common participants were in-
dividuals associated with academic institutions and private organizations (39.3),
government employees (30.4), or members of NGOs (18.9). Other participants
identied themselves as members of the diveitourismiresort industry, volunteers, or
marineienvironmental consultants and contractors (11.4). Most respondents (60)
indicated at least 5 yrs of reef restoration experience and 20 indicated 15+ yrs of
experience. For most questions, no statistical dierences were found between the
background of the respondent or the level of experience. Terefore, all responses
were combined for analysis except when noted. Respondents were explicitly asked to
only rate the reef restoration methods they had tried, thus questions with fewer than
ve responses prevented us from statistically comparing dierences between groups.
When asked about the status and trends of Caribbean Acropora populations, 90
and 85 of respondents stated that A. cervicornis and A. palmata are either degraded
or severely degraded, respectively (Fig. 4A). Moreover, the majority of respondents
believe wild populations of A. cervicornis (55.6) and A. palmata (85.3) continue
to decline, are not recovering naturally, and their threatened status is therefore war-
ranted (Fig. 4B). When asked to rank how important active reef restoration is to the
future of coral reefs on a scale from 1 (not important) to 5 (extremely important), re-
spondents indicated active reef restoration was either important or extremely impor-
tant [mean rank = 3.9 (SD 1.1), median rank = 4]. Moreover, active reef restoration
was ranked as either important or extremely important for the future of Caribbean
acroporid corals [mean = 4.3 (SD 1.0), median = 5]. Additionally, participants indi-
cated that active coral reef restoration could be an ecient coral reef management
Figure 2. Percentage of Caribbean Acropora restoration sites (A) using various propagation meth-
ods, (B) utilizing various fragment attachment methods, and (C) experiencing common restora-
tion concerns.
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1087
Figure 3. (A) Wire frames, (B) ropes, (C) cinder-block platforms, and (D) Reef Balls used as arti-
fcial structures for propagating coral fragments within coral nurseries. Photos courtesy of (A) T
Thyberg, (B) V Galvan, and (D) E DAlessandro.
Figure 4. Percentage of respondents that ranked the (A) status and (B) trends of Acropora palmata
and Acropora cervicornis populations as (A) degraded (1) to pristine (5) and (B) declining (1) to
expanding (5).
tool [mean = 3.5 (SD 1.3), median = 4]. Statistical dierences between groups were
detected in responses to the question of Acropora recovery potential without human
intervention [mean = 2.5 (SD 1.3), median = 2]. Members of NGOs rated Acropora
as less likely to recover on its own [mean = 1.5 (SD 0.7), median = 1] than members
from academic institutions [mean = 2.5 (SD 1.2), median = 2] or government agen-
cies [mean = 3.3 (SD 1.5), median = 2, one-way ANOVA: P = 0.008]. Additionally,
respondents with 610 yrs of experience [mean = 1.9 (SD 1.0), median = 2] thought
Acropora is less likely to recover without human intervention than respondents with
>15 yrs of experience [mean = 3.3 (SD 1.3), median = 3, one-way ANOVA: P = 0.024].
A B
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1088
Te most common restoration methods used by participants were fragment stabi-
lization (practiced by 62.3 of respondents) and coral gardening (practiced by 74.0
of respondents, dened in the questionnaire as coral fragment propagation within
nursery environments for use in outplanting). Larval seeding and electrolysis were
among the least common methodologies used by participants (19.5 and 1.3, re-
spectively). Coral gardening [mean = 4.0 (SD 1.0), median = 4] and fragment stabili-
zation [mean = 3.9 (SD 1.0), median = 4] were ranked as the most eective methods
of reef restoration (Fig. 5A). In contrast, electrolysis was considered the least eec-
tive method [mean = 2.0 (SD 1.4), median rank = 1.5]. Respondents believed that
coral gardening and fragment stabilization were signicantly more eective than
electrolysis, larval seeding, and coral reef care (i.e., fragment stabilization, preda-
tor removal, algal weeding, sediment removal, Kruskal-Wallis one-way ANOVA on
ranks: H = 48.0. P < 0.001, Table 3). Te highest-ranked coral reef care method was
the rescue of broken colonies andior coral fragments after disturbance events such
as ship groundings and storms [mean = 4.1 (SD 0.9), median = 4].
Te highest-ranked outplanting (transplanting nursery-grown corals to the reef)
method was securing fragments or colonies to the reef substrate using cement andi
or epoxy [mean = 3.8 (SD 1.1), median = 4] or with cable ties andior wire [mean =
3.5 (SD 1.3), median = 4]. Wedging corals directly into holes and crevices in the reef
framework [mean = 2.6 (SD 1.0)], attaching corals to lines, ropes or mesh secured
to the substrate [mean = 2.9 (SD 1.2)], or axing corals to nails driven into the sub-
strate [mean = 3.2 (SD 1.2)] were considered the least eective methods (median = 3
each). Te use of cement andior epoxy and cable ties andior wire was considered sig-
nicantly more eective than direct wedging by restoration practitioners (Kruskal-
Wallis one-way ANOVA on ranks: H = 30.8, P = < 0.001, Table 2).
Among the potential benets that coral reef restoration can provide, the highest-
ranked benet was increased public awareness and education [mean = 4.3 (SD 0.9),
median = 5, Fig. 5B]. Enhanced sheries habitat [mean = 4.0 (SD 1.1)], increased coral
population expansion [mean = 3.9 (SD 1.1)], improved reef structure [mean = 3.9
(SD 1.1)], and increased genotypic diversity [mean = 3.9 (SD 1.1)] were also highly
rated as potential benets of reef restoration (median = 4 each). Overall, these cor-
al reef restoration benets were ranked signicantly higher than the least valuable
Figure 5. Mean ranking by respondents on (A) the effectiveness of various restoration methods,
(B) the potential benefts of reef restoration, and (C) concerns facing coral reef restoration efforts.
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1089
benets such as enhanced diveritourist experience, employment opportunities, and
improved local livelihoods (Kruskal-Wallis one-way ANOVA on ranks: H = 64.6, P
0.001, Table 3). In addition, 68 of respondents consider MPAs as either important
or extremely important to the success of coral restoration projects [mean = 3.9 (SD
1.2), median = 4], indicating the use of MPAs as sites for reef restoration as an impor-
tant benet to ensure the success of restoration activities and to improve the survival
of Acropora populations.
Respondents were also asked to rank a variety of concerns related to reef restora-
tion practices. High nancial cost was the biggest concern among participants [mean
= 3.7 (SD 1.2), median = 4, Fig. 5C]. Te risk of damage to donor colonies, manipula-
tion of nature, and changes in genotypic diversity, however, were ranked signicantly
lower than high nancial costs (Kruskal-Wallis One-Way ANOVA on ranks: H =
41.8, P 0.001, Table 3). Finally, 58 of Acropora reef restoration practitioners iden-
tied lack of funding as an obstacle experienced during their projects (Fig. 6). Te
next most common obstacles were project continuity and lack of project follow-up
(33 each) along with government red tape and time constraints (32 each).
7DEOH 0HDQ UDQNLQJ DQG VLJQLFDQFH RI WKH HIIHFWLYHQHVV SRWHQWLDO EHQHWV DQG FRQFHUQV RI
coral reef restoration by participants.
Topic
Median
ranking
Mean
ranking SD Kruskal-Wallis test
Effectiveness of coral reef restoration methods H = 48.0; P < 0.001
Coral gardening 4.0 4.0 1.0
Fragment stabilization 4.0 3.9 1.0
$UWLFLDOVWUXFWXUHV 4.0 3.4 1.1
Coral reef care 3.0 3.4 1.0
Larval seeding 2.0 2.1 1.1
Electrolysis 1.5 2.0 1.4
Effectiveness of outplanting methods H = 30.8; P < 0.001
Cement/epoxy 4.0 3.8 1.1
Cable ties/wire 4.0 3.5 1.3
Nails 3.0 3.3 1.2
Wedging 3.0 2.9 1.0
Line/rope 2.0 2.6 1.2
3RWHQWLDOEHQHWVRIUHHIUHVWRUDWLRQ H = 64.6; P < 0.001
Education 5.0 4.3 0.9
(QKDQFHVKHULHVKDELWDW 4.0 4.0 1.1
Coral population expansion 4.0 3.9 1.1
Increase genetic diversity 4.0 3.9 1.1
Improve reef structure 4.0 3.9 1.1
Research opportunities 4.0 3.8 1.2
Increase reproductive output 4.0 3.8 1.2
Reduce secondary disturbances 4.0 3.6 1.2
Improve local livelihoods 3.0 3.3 1.2
Enhance diver/tourist experience 3.0 3.2 1.2
Employment opportunities 3.0 3.2 1.3
Coral reef restoration concerns H = 41.8; P < 0.001
+LJKQDQFLDOFRVW 4.0 3.7 1.2
Small footprint 3.0 3.2 1.2
Changes in genotypic diversity 3.0 2.9 1.3
Secondary damage 3.0 2.9 1.2
Damage to donor colonies 3.0 2.8 1.3
Manipulation of nature 2.0 2.5 1.3
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1090
Discussio
Most recent coral propagation and coral reef restoration activities in the Caribbean
have focused on the threatened genus Acropora (Bruckner 2002, Acropora Biological
Review Team 2005). Tis concentration is mainly due to the historical and contin-
ued decline of this important reef-building genus, and the success of projects using
Acropora for propagation and restoration. One of the most remarkable ndings of
this review is the agreement among coral reef scientists and managers that active
propagation and restoration activities will play an important role in the future re-
covery of Acropora. However, practitioners emphasized the need for active resto-
ration to be conducted in conjunction with robust local and regional management
strategies to mitigate the impacts of anthropogenic and natural disturbances such as
those associated with global climate change, land-based sources of pollution, habitat
destruction, and overshing. Because reef restoration eorts can prove futile if the
initial agent or source of degradation has not been permanently removed from the
impacted area (Jaap 2000, Precht 2006), reef restoration must be considered as a
complement to management tools that address the larger causes of reef degradation.
Te need for an integrated approach to coral reef restoration was highlighted in the
responses by the suggested importance of conducting coral reef restoration activities
within MPAs to provide positive synergisms between coral reef management tools.
In our study, the highest ranked and most eective coral reef propagation and res-
toration techniques were low-tech methodologies, utilizing inexpensive and readily
available materials such as wire mesh, PVC, plastic cable ties, cinder blocks, nails,
shing line, and ropes (Becker and Mueller 2001, Bowden-Kerby 2001, Hernndez-
Delgado et al. 2001, Quinn et al. 2005, Herlan and Lirman 2008). Tis indicates that
propagation and restoration activities using Acropora have the potential to be con-
ducted successfully at low cost. Additionally, it has been shown that these low-tech
Figure 6. Percentage of respondents indicating common obstacles of Caribbean reef restoration
projects.
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1091
propagation and restoration activities can be an empowering education tool when
integrated into community-based management (Bowden-Kerby 2001). Tese tech-
niques can be used to assist local coastal communities to restore and manage their
own local reef resources. Tus, the integration of socioeconomic needs and perspec-
tives of local stakeholder groups who depend upon coral reefs in the Caribbean is
an important step in successful coral reef restoration (Bowden-Kerby 2001, Goreau
and Hilbertz 2005). Respondents indicated that project continuity beyond the initial
funding cycle will depend on the involvement of local stakeholders outside the scien-
tic and management community. Tus, the adoption of propagation and restoration
projects by dive shop operators, resort owners, shermen, and local communities
were identied as key components to the long-term success of restoration programs.
With low-tech, cost-ecient methods, people of coastal communities can conduct
restoration activities to restore and protect their local reefs, and therefore promote
community-based management of local resources through continued public educa-
tion and awareness. For example, in Punta Cana, Dominican Republic, an Acropora
nursery and restoration site has resulted in the establishment of a voluntary marine
protected area by local shermen and has become a popular dive and snorkel site due
to the increased biodiversity as a direct result of Acropora restoration activities. Tis
project involves partners from NOAA, various NGOs, and the local community and
dive operators to maintain and manage the site. Additionally, on the island of Utila
in Honduras, the utilization of low-tech and low-cost techniques by local volunteers
in partnership with several NGOs and the Honduras Ministry of Tourism has re-
sulted in the enhancement of approximately 500 linear meters of reef with >500
nursery-reared A. cervicornis colonies with a 50 survival rate >7 yrs. An extraordi-
nary example of the ability and drive of a local community to drastically increase the
quality of their reef ecosystem through the use of inexpensive and easy methodolo-
gies comes from Bolinao, Philippines, where up to 1200 m
2
of reef were outplanted
by hand by local free-divers wearing handmade plywood ippers (Normile 2009). By
involving the local community to participate in coral restoration projects, they can
witness their ability to protect and expand the resources upon which they depend for
both food and income (Goreau and Hilbertz 2005). Furthermore, reef restoration can
be an empowering educational tool to promote public awareness and participation
in coral reef conservation, providing the foundation for community-based manage-
ment and serving as a unication point between sometimes antagonistic stakeholder
groups (i.e., government agencies, NGOs, conservationists, shermen, and the tour-
ism industry, Stepath 2000), which will dramatically improve Caribbean-based reef
restoration eorts.
In addition to the cost of propagation and restoration activities, the lack of contin-
ued funding, limited project follow-up, and lack of project continuity were highlight-
ed as limitations to the establishment and success of long-term restoration programs
in the Caribbean. Restoration activities are often initiated with extramural funding
and struggle to continue beyond the initial 1- to 3-yr funding cycle. In many cases,
this leads to a paucity of publications and lack of project documentation that has
forced practitioners to implement projects with limited prior knowledge. For exam-
ple, in the Caribbean, only two restoration studies including Acropora transplan-
tation and fragment stabilization exist with data exceeding 10 yrs (Bruckner et al.
2009, Garrison and Ward 2012). Hence, the information and sources included here,
as well as the recent publication of restoration manuals (Precht 2006, Edwards and
BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1092
Gomez 2007, Edwards 2010, Johnson et al. 2011), provide collective knowledge and
best practices that can aid practitioners in the development of new, scientic-based
restoration projects.
Another concern raised by respondents was the potential negative impacts on re-
maining donor populations and reefs. However, the potential negative impacts to do-
nor populations are only a concern when collecting colonies or fragments from wild
populations to stock nurseries or when whole corals are transplanted from healthy to
degraded sites. Studies have shown that Acropora fragments can be collected without
causing signicant mortality on donor colonies (Becker and Mueller 2001, Lirman
et al. 2010) and that pruning of branching corals, like A. cervicornis, actually results
in an overall increase in productivity through pruning vigor (Lirman et al. 2010).
Additionally, the direct transplantation of corals or fragments from healthy to dam-
aged sites without an intermediate nursery step is rare given the present condition
of coral reefs around the world. In fact, transplantation of corals from one site to
another is usually only utilized to relocate corals prior to the destruction of a reef site
during projects such as dredging, port and marina expansion, or beach renourish-
ment activities (Gayle et al. 2005, Seguin et al. 2010).
While even the largest reef restoration projects pale in comparison to the scale of
natural processes during a successful sexual recruitment event, establishing multiple
small, genetically diverse populations that will, in time, become sexually reproduc-
tive can contribute to species recovery, especially in areas of signicant parent popu-
lation declines (Baums et al. 2005, Vollmer and Palumbi 2007). Terefore, we suggest
that by strategically restoring populations to ll spatial gaps in species distribution,
small reproductive populations may have the potential to signicantly contribute
to the overall success of gamete fertilization and sexual recruitment of Acropora
populations. For example, an estimated 1500 corals from the Acropora coral nurs-
ery have been outplanted to local reefs by the Coral Restoration Foundation in Key
Largo, Florida, and some of these outplanted corals were reported to spawn in 2009
(Nedimeyer, Coral Restoration Foundation, pers comm). In addition, spawning was
observed in A. palmata fragments 3 yrs after stabilization to reefs near Boca Chica,
Dominican Republic (B Bezy, University of Costa Rica, pers comm). Tese marked
the rst reported spawning events of restored Acropora in the Caribbean.
Te concerns expressed by respondents regarding genetic modications to wild
populations include the possibility of establishing monoclonal populations that
would reduce fertilization success or articially increase the local dominance of cer-
tain genotypes that may depress the genetic contribution of wild genotypes. In the
past, reef restoration and coral propagation activities have not considered genetic or
genotypic diversity explicitly, but recent developments in molecular tools have al-
lowed researchers to assess local and regional coral genotypic diversity of wild popu-
lations as well as identify and track the performance of genetic lineages within coral
nurseries and outplant sites (Baums 2008, Schopmeyer et al. 2011). Tis information
will prove invaluable for use in restoration programs to select appropriate genetic
sources and inuence the spatial arrangement of transplanted populations.
Perhaps the largest debate surrounding the eld of coral reef restoration is whether
the risks and costs of restoration activities exceed the benets and rewards they pro-
vide. On an ecological scale, key losses in coral reef biodiversity have devastating
consequences on resilience and resistance (Bellwood et al. 2004, Palumbi et al. 2009).
Te global value of the goods and services provided by coral reefs has been estimated
YOUNG ET AL.: REVIEW OF CARIBBEAN ACROPORA RESTORATION 1093
at US$375 billion yr
1
(Edwards and Gomez 2007). More specically, Caribbean
reefs have been valued between US$100,000 and US$600,000 km
2
of coral reef to-
taling approximately US$3.1$4.6 billion annually generated through food produc-
tion from sheries (US$310 million), tourism and recreation (US$4.7 billion), and
shoreline protection (US$740 million to US$2.2 billion, Burke and Maidens 2004).
Tus, the continued degradation of Caribbean reef systems may result in signicant
economical losses totaling US$350$870 million annually. Moreover, the socioeco-
nomic importance of reefs in the Caribbean is compounded by the fact that many
of these coral reef nations are small, developing island states, where vulnerability is
often exacerbated by high coastal population densities, scarce resources, geographic
isolation, weak economies, and susceptibility to natural disturbances such as hur-
ricanes, tsunamis, and sea level rise (Burke et al. 2011). Terefore, the potential for
biological and economic losses through the complete degradation of Caribbean reefs
greatly underscores the need for coral reef protection and restoration, particularly of
acroporid corals, which provide the primary foundation of reef structural complex-
ity (Bruckner 2002). Te cost of Caribbean coral reef restoration can be high, with
simple coral transplantation projects costing US$10,000 ha
1
and projects includ-
ing physical restoration of the reef substrate and framework, such as repairing the
reef framework after a ship grounding, costing upwards of US$2.0$6.5 million ha
1

(Spurgeon 2001, Edwards 2010). However, the cost of simple nursery and transplant
techniques appears minimal compared to the compounded annual losses of ecosys-
tem goods and services from damaged and degraded reefs.
Based on our literature review and responses, it appears that the future of reef res-
toration in the Caribbean and western Atlantic relies on two fundamental priorities.
First, utilizing low-cost restoration methodologies is crucial to improving the num-
ber, length, and success of restoration activities. Second, restoration activities must
be conducted in conjunction with ecosystem-based management and conservation
practices (i.e., MPAs and no-take zones) to mitigate the impacts of anthropogenic
and natural disturbances. Terefore, low-cost and low-tech coral reef propagation
and restoration methodologies combined with higher levels of protection and long-
term monitoring will act as potential complementary management tools for future
rehabilitation of Caribbean reefs, and specically, the future recovery of threatened
Caribbean acroporid coral species. While challenges and obstacles still remain in the
eld of active coral propagation and reef restoration, an increasing body of knowl-
edge is now available to support these activities and ensure that the benets of these
programs exceed the potential risks to remaining wild coral populations and coral
reef communities.
Acoivoorv:s
Tis project was funded by Counterpart International and the Frohring Foundation. Te
questionnaire greatly beneted from comments by A Bowden-Kerby, M Estevanez, and M
Shivlani. We appreciate the information graciously provided by the practitioners conducting
reef restoration activities as well as the respondents of the online questionnaire. Tis manu-
script benetted from comments by C Drury, B Huntington, R Santos, and T Tyberg, and
GIS assistance was provided by J Blondeau.
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D:v Sunri::vo: 21 December, 2011.
D:v Accvv:vo: 1 June, 2012.
Aviiniv Oiiv: 2 July, 2012.
Aoovvss: University of Miami, Rosenstiel School of Marine and Atmospheric Science, 4600
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<dlirman@rsmas.miami.edu>.