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Rebuilding coral reefs: does active reef restoration lead to

sustainable reefs?
Baruch Rinkevich

The coral reefs worldwide are exposed to multiple highly degraded, and exposed to multiple persisting
anthropogenic threats and persisting global change impacts, and envisaged threats [2,3]. The stressors, and notwith-
causing continuous degradation, also calling for the standing all traditional conservation management
development of novel restoration methodologies. Of the most measures implemented [4], would lead to loss of up
promising emerging approaches, deriving its rationale from to 70% of reef area within four decades or to phase shift
silviculture, is the low-cost ‘gardening concept’, guided by a [1].
two-step restoration operation: (a) mid-water nursery phase,
where coral-nubbins are farmed and (b) transplantation of The above causes that have led to progressive impair-
nursery-farmed colonies. Tested worldwide, at least 86 coral- ment of the normal course of coral-reefs life and their
species and over 100 000 colonies were successfully farmed in global contribution to humans, without proper damage
different archetype nurseries, and several novel transplantation control or repair, have prompted the demand for
methodologies were developed. A number of unanticipated alternative active reef restoration measures, beyond the
emerged outcomes were the immediate establishment of coral traditionally employed conservation. Restoration is
infaunal biodiversity in nurseries, the development of nurseries defined by the Society of Ecological Restoration as ‘the
into ‘larval dispersion hubs’ and the enhanced reproduction of process of assisting the recovery of an ecosystem that has
transplanted coral colonies. Altogether, and in addition to been degraded, damaged, or destroyed’ [5]; it has
envisaged results (e.g., high survivorship, fast coral growth), also been acknowledged that restoration activities
results attest that the gardening-toolbox could serve as a may complement [6], even substitute conservation
ubiquitous ecological engineering platform for restoration on a efforts. Whereas the restoration rationale is rooted in
global scale. active approaches to solve ecosystem degradation (‘Eco-
Addresses logical restoration is an engaging and inclusive process’;
National Institute of Oceanography, Tel Shikmona, PO Box 8030, Haifa [5]), conservation biology endeavors preservation, count-
31080, Israel ing on long-term ecological succession as the major
repairing mechanism for impacted ecosystems. The lit-
Corresponding author: Rinkevich, Baruch (buki@ocean.org.il)
erature documents that ecological restoration is a fast
developing scientific discipline. Heeding the invaluable
Current Opinion in Environmental Sustainability 2014, 7:28–36 lessons gathered from the failures of traditional conser-
This review comes from a themed issue on Environmental change
vation, the declaration of the Convention on Biological
issues Diversity that restoration of terrestrial, inland water and
Edited by Georgios Tsounis and Bernhard Riegl
marine ecosystems is essential for rehabilitating the
ecosystem’s functioning, goods and services [6], confirms
For a complete overview see the Issue and the Editorial
the wide scientific support of ecological restoration
Available online 20th December 2013 efforts. In fact, the extent of anthropogenic and global
1877-3435/$ – see front matter, # 2013 Elsevier B.V. All rights change impacts on coral reefs worldwide renders their
reserved. active restoration as a major conceptual and practical
http://dx.doi.org/10.1016/j.cosust.2013.11.018 approach, not just as assistant act to traditional conserva-
tion acts [4,7,8].

Introduction Restoration practices for degraded reefs can be broadly

The ominous status of coral reefs worldwide and active categorized into passive or active restoration [4,7,8].
reef restoration Active restoration, or active human intervention in
Once acknowledging the vital ecological importance of degraded reef sites, disputes passive restoration, the
coral reefs and their fundamental roles in sustaining dependency on natural regeneration and repair with
hundreds of millions of people, it is dismaying to realize minimal human surrogacy. Indeed, when analyzing glob-
that over the last four decades ca. 40% of the global ally employed passive restoration measures, it is evident
coral-reef system has been lost, a process galloping at 1– that the reef management acts have been imperfect,
2% per year [1], not considering the developing global failed to ascertain the right responses to key threats,
change impacts that are exacerbated by severe anthro- failed to yield a quantifiable return and are ineffective
pogenic pressures. Thus, coral reefs, while exhibiting in ameliorating long-term impairments [summarized in
exceptional species diversity, are poorly protected, 4,7,8]. More pressing is the realization that regardless of

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 Active reef restoration and sustainable reefs Rinkevich 29

Figure 1 coral colonies, improved state of health of transplants,

year round availability of transplants). This strategy,
Restoration scenarios which derives its rationale from silviculture, is guided
by a two-step restoration operation. The first step entails
Primeval
Restored ?? 1 characters rearing stocks of small coral fragments in specially
?? 3
6 designed mid-water floating nurseries, and upon reach-
Replacement status ??
??
ing suitable sizes, applying the second step, the trans-
Reef services

Restored
5 Restored
plantation of nursery-farmed coral colonies onto
4 denuded reef areas. As restoration ecology is rooted in
forestation, it is therefore not surprising that silviculture
??
principles, concepts and theories, are intermingled
Degraded
reef
within the ‘gardening’ notion and its associated activi-
2
7 ties. During the almost two decades from their first
presentation [9], the two gardening tenet steps have
Degraded status Ecological complexity Replacement status been tested in various reefs worldwide (Table 1 dis-
Low High cusses the nursery step; studies performed in the Red
Sea, Thailand, Singapore, Philippines, Tanzania,
Current Opinion in Environmental Sustainability Mauritius, Seychelles, Caribbean sites [Jamaica, Florida
keys, Colombia, Belize, and more], Japan, Taiwan,
Figure depicts multiple ‘restored reef-state’ scenarios (circles no 3–7) Hawaii; much of the outcomes is still unpublished
showing paths from a degraded reef (low ecological complexity and [3,11,12,13,14,15,16–23]).
minimal reef services; circle 2) toward a healthy reef (circle 1), passing
through two types of unsuccessful measures (circles 6, 7) and several
restored status (circles 3–5). The unsuccessful measures represent The nursery phase of the ‘gardening concept’ has been
attempts (a) aiming to boost reef services (such as installing artificial drawing the most scientific investigation, conceptually
reefs for fisheries; circle 6) or whole colonies transplantation acts [9] and and technically addressed in detail, with at least 86 coral
(b) aiming to increase biodiversity, such as the concept of ‘assisted species farmed in underwater nurseries, worldwide (117
colonization’ [10] (circle 7). In both scenarios it is more likely that reef
environments will revert to their degraded status than advance toward a
species when total farmed species in all nurseries is
better state (marked by question marks). Three different scenarios considered, Table 1; only species from literature and
employing the ‘gardening concept’ [4,7–9,12,13,14,15,16–23] are personal communication are listed). Issues, such as nur-
defined. These may result in rehabilitated reefs at different complexity/ sery structure, nursery types, nursery’s set-up, shape and
reef services states (circles 3–5) that could develop into other states and
construction, nursery location, maintenance subjects,
possibly (question marks) will culminate with the primeval reef status.
coral species cultured (types, numbers) and genotypic
considerations, spacing of farmed coral colonies, realistic
number of generated and farmed colonies, duration of the
the implication of either practice, the restored ‘reefs of nursery phase, growth rates of farmed corals, longevity of
tomorrow’ will be different from the current or past reefs’ farmed colonies, pest control and economic consider-
constructions (Figure 1). ations are some of the topics studied recently. The second
phase of transplantation, which is still in its infancy, has
The gardening tenet also revealed promising results ([12,13,14,15], unpub-
Several approaches for active restoration have been lished). The major conclusion which emerged from the
suggested; some have been subjected to intensive above studies is that the application of active restoration
research manipulations. One of the first advocated meth- protocols may enhance reef recovery [4,7,8].
odologies was the direct transplantation of coral material
(entire coral colonies and/or fragments), an approach The results obtained from various reefs worldwide
subjected to a wide range of limitations and pitfalls, such cumulatively have revealed that the gardening tenet,
as negative impacts on donor reefs and on transplanted with modifications and adjustments per local conditions,
coral colonies [8,9]. A comparable, more recent approach can be used as a ubiquitous management instrument
is the controversial tool of ‘assisted colonization’ or ‘man- for rescuing reefs from the on-going degradation
aged relocation’ [reviewed in 10], claiming active trans- (Box 1).
location of groups of species outside the species’ historic
range for conservation purposes. What has been learnt recently from
nursery/transplantation acts?
One of the most promising active restoration approaches Studies [11,12,14,15,16–23,24] have already revealed
is the ‘gardening concept’ [4,7–9], which has surfaced as a that farmed corals not only compete successfully with
means to avoid the pitfalls associated with the traditional natural colonies’ performance, but also exhibit improved
management for coral reefs (e.g., reduced negative health status, being free of parasites and diseases (devel-
impacts on donor reefs, high survivorship of transplanted oped and maintained under controlled conditions), with

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30 Environmental change issues

Table 1

List of coral species farmed in coral nurseries worldwide ([13,14,18–23,24,37–51], unpublished). C, Caribbean sites (pooled); E, Eilat, Red
Sea; H, Hawaii; J, Japan; M, Mauritius; P, Bolinao, the Philippines; Se, Seychelles, Si, Singapore; T, Taiwan; TP, Phuket Island, Thailand;
ZM, Zanzibar and Mafia Islands, Tanzania

No Coral species E P TP Si Se ZM M H C J T
1 Acanthastrea brevis +
2 Agaricia agaricites +
3 Acropora aspera +
4 Acropora austrea +
5 Acropora cervicornis +
6 Acropora cytherea + +
7 Acropora digitifera +
8 Acropora eurystoma +
9 Acropora formosa + + + +
10 Acropora grantis +
11 Acropora hemprichii + +
12 Acropora humilis +
13 Acropora hyacinthus + + +
14 Acropora intermedia +
15 Acropora irregularis +
16 Acropora lamarcki +
17 Acropora macrostoma +
18 Acropora millepora +
19 Acropora muricata +
20 Acropora nasuta +
21 Acropora palmata +
22 Acropora pharaonis +
23 Acropora pulchra + +
24 Acropora selago +
25 Acropora squarrosa +
26 Acropora tenuis +
27 Acropora valida + + +
28 Acropora variabilis +
29 Caulastrea furcata +
30 Cyphastrea microphthalma +
31 Diploastrea heliopora +
32 Diploria labyrinthiformis +
33 Echinopora hirsutissima +
34 Echinopora lamellosa + +
35 Eusmilia fastigiata +
36 Favia favus +
37 Galaxea fascicularis + +
38 Goniastrea aspera +
39 Goniopora savignyi +
40 Heliopora coerulea + +
41 Hydnophora exesa +
42 Hydnophora rigida +
43 Madracis mirabilis +
44 Merulina scabricula +
45 Millepora complanata +
46 Millepora dichotoma + +
47 Montastraea annularis +
48 Montastraea cavernosa +
49 Montipora aequituberculata + +
50 Montipora capitata +
51 Montipora digitata + + +
52 Mycedium sp. +
53 Oulastrea crispata +
54 Oxypora sp. +
55 Pachyseris speciosa +
56 Pavona cactus + + + +
57 Pavona danai +
58 Pavona decussata +
59 Pavona frondifera +
60 Pectinia lactuca +
61 Physogyra lichtensteini +
62 Platygyra sinensis +

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 Active reef restoration and sustainable reefs Rinkevich 31

Table 1 (Continued )
No Coral species E P TP Si Se ZM M H C J T
63 Pocillopora cylindrica +
64 Pocillopora damicornis + + + + + + + +
65 Pocillopora eydouxi +
66 Pocillopora verrucosa + +
67 Podabacia sp. +
68 Porites astreoides +
69 Porites compressa +
70 Porites cylindrica +
71 Porites deformis +
72 Porites divaricata +
73 Porites lobata +
74 Porites lutea + +
75 Porites palmata +
76 Porites porites +
77 Porites rus + +
78 Porites sillimaniana +
79 Psammocora digitata +
80 Psammocora digitifera +
81 Seriatopora hystrix +
82 Siderastrea siderea +
83 Stylocoeniella sp. +
84 Stylophora pistillata + +
85 Turbinaria peltata +
86 Turbinaria sp. +
Species/locality 21 14 8 26 10 9 10 3 13 2 1

high survivorship under natural reef conditions, and year- various forms (branching, massive and encrusting species)
round availability, circumventing the need to explore have already been farmed in these nurseries, worldwide,
sites for harvesting additional material [3,12,24]. showing minor mortalities and enhanced growth rates.
These nurseries are usually installed in a protected site,
The mid-water floating nurseries have already been away from major natural reef structures, away from the
established as a successful farming tool. It is estimated afflictions of recreational activities and corallivorous
that >100 000 colonies from 86 coral species (Table 1) of organisms. Under these excellent conditions, fragments
from many coral species grew to large colonies within
1–1.5 years [7,15,16–23]. Furthermore, floating coral
Box 1 Major considerations when approaching reef restoration
project under the ‘gardening concept’ nurseries (Figure 2) unexpectedly revealed: (a) that
swinging in all directions enhances food and oxygen
supplies and facilitates clearing of debris and sediment
What is needed to know?
 Primeval local reefs’ status
particles that might accumulate on farmed coral colonies
 Getting acquainted with key/dominant species biological patterns [3,19]; (b) reduced sedimentation fluxes, since nurseries
 Population genetics of local species are above substrate; (c) depth adjustment, ‘tailored’ for
 Past bleaching events and disease outbreaks, including any species-specific needs, also allowing acclimatization
consequences
of farmed corals to conditions in their designated trans-
 Conferring on connectivity trajectories, resistance/resilience
attributes, top-down/bottom-up controls plantation site [3]; (d) mid-water nursery attracts com-
 Quantified reef services; defined reef stakeholders mensals and coral inhabiting species arriving from the
 List of natural/anthropogenic threats plankton, for the establishment of the entire coral infau-
 Anticipated climate change impacts nal biodiversity [19]; and (e) early onset of sexual repro-
 Evaluation of current conservation acts
Issues to be considered:
duction in farmed corals, changing the nursery into ‘larval
 Some reefs might not need active restoration (highly resilient/ dispersion hub’ that can be used as a management tool for
resistant reefs) natural recruitment enhancement [11]. Above themes
 Some reefs should not be restored (reefs under severe attest that the tool of a floating nursery could serve as
anthropogenic impacts) a ubiquitous platform for developing restoration protocols
 Vision for the status of the ‘reef of tomorrow’ for each locality
 Pre-planning of nursery/transplantation scenarios and colonies/
applicable on a global scale.
genotypes/species numbers
 Different spatial/temporal reef-features require different The transplantation phase has further benefitted from
restoration methodologies developing a wide array of new methodologies, like
 Close monitoring of each of the restoration acts
 Flexible to revise/change approaches not successfully developed
transplantation into drilled holes, transplantation on
wire mesh, chiselling holes in softer substrate, lining of

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32 Environmental change issues

Figure 2

(a) (b)

(c) (d)

(e) (f)

Current Opinion in Environmental Sustainability

The nursery (a,b,c) and transplantation (d,e,f) phases of the ‘gardening notion’. (a) Eilat’s (Red Sea) underwater prototype coral nursery at the
beginning [16,17]. This nursery is located at 6 m depth, 14 m above sea bottom in blue, clear water. The nursery is made with rope net
(10 m  10 m size) as the nursery basis (may be situated at various depths, according to the specific needs). Coral nubbins are glued onto
plastic pins (9 cm long, 0.3–0.6 cm width leg and 2 cm diameter ‘head’) which are inserted into plastic nets stretched over PVC frames
(30 cm  50 cm). The frames carrying corals are tied to the nursery base (photograph by D. Gada); (b) the novel prototype of the rope nursery in
Bolinao, the Philippines [20]. This nursery accommodated small coral fragments attached to a rope, creating an easily constructed nursery bed
that is rapid and inexpensive. The coiling force of the ropes adequately held fragments without adhesives, and the minimal surface area of rope
nursery beds provided not only improved water flux around farmed corals, but also reduced proliferation of fouling organisms. Above two
nursery prototypes have been used under various conditions and demands, making the construction of large scale nurseries a very feasible
target (photograph by G. Levi); (c) coral stocking in a vertical rope nursery (Eilat, Red Sea). Corals are growing on the rope and are often clipped
for developing daughter colonies that are farmed in other nursery types (insert photo — a Stylophora pistillata colony growing on the rope). This
nursery further attests to the wide range of nurseries recently developed, each adapted for a specific need (photograph by A. Lazarus). (d,e) two
transplantation methodologies developed recently (out of several) for transplantation of nursery farmed corals on hard and soft substrates. In
Eilat, Dekel Beach (d), the farmed coral colonies were secured to the hard substrates by the attaching devices (plastic pegs and masonry
anchors), inserted into pre-drilled holes, secured with a minuscule amount of epoxy glue. The holes were drilled using underwater driller,

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 Active reef restoration and sustainable reefs Rinkevich 33

rope-nursery grown corals on soft and hard substrates, communities, the gardening concept supports use of coral
and more ([12,15,21,22]; Figure 2). By using these species/genotypes that would be favorable in the anticip-
methods, not only is the coral community rehabilitated, ated climate change conditions, overlooking coral species/
but its entire carrying capacity also increases due to the genotypes that are less tolerant to climatic conditions;
new ecological and spatial niches added to the site. therefore reassembling novel coral reef communities that
However, transplantation methodologies are still chal- are robust to global change conditions [27]. Other tools
lenged by scientific and technical defies. The scientific incorporate selected ecological engineering aspects
part focuses on issues, such as genetics, species combi- [12,28], taking into account corals functioning as
nations, landscape manipulations, biological engineering primary reef ecosystem engineers. These tools rehabili-
and key species. One point to consider and test is spacing tate coral reefs with larvae released from nursery-farmed
of transplants. Transplants require sufficient space for corals, from transplanted coral colonies, considering var-
growth in order to avoid intraspecific or interspecific ious techniques for coral transplantation, coral coverage,
disturbances. Allogeneic and xenogeneic interactions assorted coral species compositions and engineered
can cause damage and growth abatement, influence seascape [2,3,4,11,12,20,21]. Whereas neoteric in the
reproductive activities or cause death. Clearly, studies coral restoration discipline, the ecosystem engineering
on the second phase of the gardening tenet are still very approach is deeply rooted in terrestrial restoration
limited and should be increased. measures, revealing, for example, increased bird visita-
tions in reforestation [29] or enriched forest species in
The ‘gardening concept’ as an adaptive tool to grazer-enclosure regenerating forests [30].
combat climate change impacts
The literature attests that global climate changes occur Paramount to the success of the gardening concept is the
and that they differentially alter regional ecosystems, proficiency to harness genetic backgrounds of farmed
causing unprecedented degradation to coral reefs [25]. colonies as an applied tool for restoration that targets
Climate changes present new challenges to coral reef global change. Minimal insight is available for the ways
scientists and policy makers by creating novel coral genotypic variation influence adaptive global changes
assemblages, whose ecological properties, goods and ser- competence [31]. However, recent scientific interest
vices differ from those characterizing preceding reef in the relationships between genotypes and gene expres-
ecosystems (Figure 1). The exacerbated impacts on the sion, as to the kaleidoscope of responses to various stress
reefs lead to the conclusion that current conservation conditions, has revealed that genetic legacy may serve as a
methodologies are failing to support biodiversity and reef prime applied tool for combating global change impacts
services; clearly insufficient for averting reef degradation [32], further suggesting the accommodation of climate
[4]. change contingencies in reef restoration practices.
Because of stochastic reproduction and dispersal pro-
These impacts of climate change necessitate the devel- cesses, genetic repertoires presented by marine organisms
opment of unorthodox approaches, led by the notion that at any specific time/location may not reach equilibrium
‘restoration efforts once focused on past conditions should with today’s climate, providing the opportunity to search
become more forward-looking’ [26]. On the basis of this for genotypes that are not perfectly adapted to current
rationale, restoration activities should highlight climate conditions but better suited for future environmental
change scenarios, focusing on adaptation strategies that settings and farm them within underwater coral nurseries.
had not been considered in past reef management set- This is further important as accelerating global change
tings. This may raise suggestions for more radical rates, which are notoriously exceeding the evolutionary
approaches like ‘assisted colonization’ [reviewed in 10] capacity of corals to acclimatize [33], are primarily
or for focusing only on sites that are, and predicted to relevant to long-lived coral species. Coral bleaching, for
remain, under conditions suitable for current coral assem- example, is conspicuously patchy between different gen-
blages. Both approaches deviate conceptually from the otypes, representing a signature of true genetic hetero-
‘reef gardening’ notion. geneity and revealing an acclimatization response rooted
in epigenetics. Therefore, genetic variation should be a
The gardening concept is using proactive responses potential reservoir of resilience to climate change,
to global changes, incorporating major amendments a characteristic that can be actively amplified when
in current restoration methodologies. While past restor- developing coral farming/breeding protocols under in situ
ation studies have focused on establishing key group nursery conditions.

(Figure 2 Legend Continued) powered by pressured air from diving tanks (photograph by Y. Horoszowski-Friedman). In Thailand (e), corals
were attached on wire metal mesh construction (insert figure) by plastic ties, which is cheap and fast for attaching. Other studies (unpublished)
used environmental friendly materials, like bamboo canes (photograph by G. Levi). (f) A denuded reef patch in the northern Gulf of Eilat (Dekel
Beach), five years after coral transplantation. Many fish and reef-associated invertebrates were attracted and recruited to this restored small
patch reef (photograph by Y. Horoszowski-Friedman).

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34 Environmental change issues

Underwater coral nurseries may also serve as genetic genome-wide transcriptional plasticity may underlie
repositories for coral reef restoration, combating the whole organism adaptation to novel environmental
impacts of major natural catastrophes [22,34]. The use insults, like those presented by global change [36] and
of the ‘reef gardening’ rationale as global change mediator can be used as an applied tool in coral nurseries.
through nurseries [20,21,22,24,34] has already revealed
two novel strategic roles of this instrument, (a) reducing Acknowledgements
coral mortality during events, such as massive coral
bleaching, hurricanes and fresh water floods, the creation This study was supported by a project funded in partnership with NAF-
IOLR and JNF-USA, by a grant from the Israeli Ministry of Infrastructure,
of climatic refugia and (b) preserving and propagating by the INCO-DEV project (REEFRES, no. 510657), the CORALZOO, an
diverse coral genotypes from various source materials for EC Collective Research project, the AID-CDR (C23-004) program, by the
the establishment of regional/local ‘gene stocks’ for use in World Bank/GEF project (reef remediation/restoration working group) and
by the Ministry of Science & Technology, Israel & the Ministry of
restoration activities, with an eye to initiation of breeding Education, France.
programs. The ‘reef gardening’ rationale has further
disclosed strategic considerations of this instrument References and recommended reading
([12,15,22], unpublished), including re-shaping of coral Papers of particular interest, published within the period of review,
have been highlighted as:
reefs types, changing of reef rugosity, engineering of coral
seeding processes, reducing of fleshy algae allotment in  of special interest
restored reefs and sustaining of ecosystem processes.  of outstanding interest

Would the coral ‘gardening tenet’ lead to 1. Bruno JF, Selig ER: Regional decline of coral cover in the Indo-
sustainable reefs? Pacific: timing, extent, and subregional comparisons. PLoS
ONE 2007, 2:e711.
Theoretical and empirical aspects of active reef restor-
ation are still in their nascent stages, awaiting further 2. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD,
Sweatman H, Melendy AM: Thermal stress and coral cover
work. Active reef restoration holds a number of challen- as drivers of coral disease outbreaks. PLoS Biol 2007,
ging issues and uncertainties, such as the issues of pre- 5:1220-1227.
dicting the scale of transplantation impacts, the responses 3. Shafir S, Rinkevich B: The underwater silviculture approach for
of transplanted colonies in their new ‘homes’ and the reef restoration: an emergent aquaculture theme. In
Aquaculture Research Trends. Edited by Schwartz SH. New York:
suitability of these acts to combat reef degradation. Nova Science Publications; 2008:279-295.
4. Rinkevich B: Management of coral reefs: we have gone wrong
The progression of the ‘gardening notion’ has sur- when neglecting active reef restoration. Mar Pollut Bull 2008,
mounted four major obstructions, all are satisfactorily 56:1821-1824.
deciphered: (a) developing the needed credentials for 5. SER: The SER Primer on Ecological Restoration. Version 2. Society
for Ecological Restoration Science and Policy Working Group;
farming a wide variety of coral species in mid-water 2004 http://www.ser.org.
nursery (Table 1); (b) the ability to develop stocks of
6. Normile D: UN Biodiversity Summit yields welcome and
coral colonies, employing the ‘nubbins’ methodology unexpected progress. Science 2010, 330:742-743.
[16,19]; (c) documentation that nursery farmed coral
7. Rinkevich B: Conservation of coral reefs through active
colonies perform well in their ‘new homes’, following restoration measures: recent approaches and last decade
transplantation ([12,15,22], unpublished); and (d) ver- progress. Environ Sci Technol 2005, 39:4333-4342.
ification of the low cost gardening approach (down to 0.17 8. Rinkevich B: The coral gardening concept and the use of
and 0.19 US$/coral colony for farming and transplan- underwater nurseries; lesson learned from silvics and
silviculture. In Coral Reef Restoration Handbook. Edited by
tation, phases, respectively [15,20]. Now, the ‘gardening Precht WF. Boca Raton, FL: CRC Press; 2006:291-301.
notion’ is facing its fifth challenge, performing a large, 9. Rinkevich B: Restoration strategies for coral reefs damaged by
ecologically profound restoration act (hundreds of thou- recreational activities: the use of sexual and asexual recruits.
sands of coral colonies/site) to reveal the ecological Restor Ecol 1995, 3:241-251.
engineering capacities of large-scale transplantation acts. 10. Chauvenet ALM, Ewen JG, Armstrong DP, Blackburn TM,
 Pettorelli N: Maximizing the success of assisted colonization.
This challenge is the most imperative because it would Anim Conserv 2013, 16:161-169.
demonstrate that the gardening approach is supporting The authors reviewed here the concept of ‘assisted colonization’ and
the initiation of sustainable coral reefs. recent literature that support or negate the application of this restoration
approach.
11. Amar KO, Rinkevich B: A floating mid-water coral nursery as
The gardening toolbox may further be used for testing larval dispersion hub: testing an idea. Mar Biol 2007,
novel approaches, such as developing of improved corals 151:713-718.
through epigenetics. Studies (e.g., [35]) have revealed 12. Horoszowski-Friedman YB, Izhaki I, Rinkevich B: Engineering of
that under a wide range of ecological insult scenarios,  coral larval supply through transplantation of nursery-farmed
gravid colonies. J Exp Mar Biol Ecol 2011, 399:162-166.
organisms modify levels of genome epigenetics that may In this paper, the author showed that transplanted coral colonies release
coincide with increased tolerance to otherwise lethal larvae in an order of magnitude more than natal colonies, years after their
transplantation, indicating that nursery-grown corals may be used to
conditions, further showing that these epigenetic changes enhance reef resilience by contributing to the larval pool. This establishes
may be stable across multiple generations. Therefore, the first engineered larval dispersal instrument for reef restoration.

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 Active reef restoration and sustainable reefs Rinkevich 35

13. Omori M, Iwao K, Tamura M: Growth of transplanted Acropora Studying ecologically relevant processes of growth and reproduction,
tenuis 2 years after egg culture. Coral Reefs 2008, 27:165. the authors demonstrated the existence of relevant levels of variation
among genetic individuals, which may enable future adaptation via
14. Nakamura R, Ando W, Yamamoto H, Kitano M, Sato A, non-mutational natural selection to global change impacts.
Nakamura M, Kayanne H, Omori M: Corals mass-cultured from
eggs and transplanted as juveniles to their native, remote 32. Evans TG, Hoffman GE: Defining the limits of physiological
coral reef. Mar Ecol Prog Ser 2011, 436:161-168. plasticity: how gene expression can assess and predict the
consequences of ocean change. Philos Trans R Soc Lond B
15. Mbije NEJ, Spanier E, Rinkevich B: A first endeavour in restoring 2012, 367:1733-1745.
 denuded, post-bleached reefs in Tanzania. Estuar Coast Shelf
Sci 2013, 128:41-51. 33. Howells EJ, Berkelmans R, van Oppen MJH, Willis BL, Bay LK:
Here, the authors showed, by employing field studies in Tanzania and Historical thermal regimes define limits to coral
economic evaluations that transplantation of nursery-farmed colonies acclimatization. Ecology 2013, 94:1078-1088.
into denuded reef areas might uphold critical ecosystem functions while
used in reversing phase shift states in coral reefs. 34. Schopmeyer SA, Lirman D, Bartels E, Byrne J, Gilliam DS, Hunt J,
 Johnson ME, Larson EA, Maxwell K, Nedimyer K, Walter C: In situ
16. Shafir S, Van Rijn J, Rinkevich B: Steps in the construction of coral nurseries serve as genetic repositories for coral reef
underwater coral nursery, an essential component in reef restoration after an extreme cold-water event. Restor Ecol
restoration acts. Mar Biol 2006, 149:679-687. 2011, 20:696-703.
The authors documented in this paper that coral nurseries could be
17. Shafir S, van Rijn J, Rinkevich B: A mid-water coral nursery. used as genetic repositories for future coral reef restoration acts, com-
Proc 10th Int Coral Reef Symp. 2006:1674-1679. bating the impacts of major natural catastrophes, creating of climate
18. Shaish L, Levy G, Gomez E, Rinkevich B: Fixed and suspended refugia.
coral nurseries in the Philippines: establishing the first step in 35. Stern S, Fridmann-Sirkis Y, Braun E, Soen Y: Epigenetically
the ‘gardening concept’ of reef restoration. J Exp Mar Biol Ecol heritable alteration of fly development in response to toxic
2008, 358:86-97. challenge. Cell Rep 2012, 1:528-542.
19. Shafir S, Rinkevich B: Integrated long term mid-water coral 36. Cebrian E, Kipson S, Garrabou J: Does thermal history influence
nurseries: a management instrument evolving into a floating  the tolerance of temperate gorgonians to future warming?
ecosystem. Mauritius Res J 2010, 16:365-379. Mar Environ Res 2013, 89:45-52.
20. Levi G, Shaish L, Haim A, Rinkevich B: Mid-water rope nursery – This work revealed the role of thermal history in shaping the thermo-
testing design and performance of a novel reef restoration tolerance responses of Mediterranean gorgonians dwelling under con-
instrument. Ecol Eng 2010, 36:560-569. trasting temperature environments. Although not addressing the concept
of epigenetics, the results highly suggested this phenomenon.
21. Shaish L, Levi G, Katzir G, Rinkevich B: Employing a highly
fragmented, weedy coral species in reef restoration. 37. Soong K, Chen T: Coral transplantation: regeneration and
Ecol Eng 2010, 36:1424-1432. growth of Acropora fragments in a nursery. Restor Ecol 2003,
11:62-71.
22. Shaish L, Levi G, Katzir G, Rinkevich B: Coral reef restoration
(Bolinao, the Philippines) in the face of frequent natural 38. Omori M: Success of mass culture of Acropora corals from egg
catastrophes. Restor Ecol 2010, 18:285-299. to colony in open water. Coral Reefs 2005, 24:563.

23. Bongiorni L, Giovanelli D, Rinkevich B, Pusceddu A, Chou LM, 39. Chou LM, Yeemin T, Abdul Rahim BGY, Si Tuan VO, Alino PM:
Danovaro R: First step in the restoration of a highly degraded Suharsono: coral reef restoration in the South China Sea.
coral reef (Singapore) by in situ coral intensive farming. Galaxea J Coral Reef Stud 2009, 11:67-74.
Aquaculture 2011, 322–323:191-200.
40. Putchim L, Thongtham N, Hewett A, Chansang H: Survival and
24. Linden B, Rinkevich B: Creating stocks of young colonies from growth of Acropora spp. in mid-water nursery and after
 brooding-coral larvae amenable to active reef restoration. transplantation at Phi Phi Islands, Andaman Sea, Thailand.
J Exp Mar Biol Ecol 2011, 398:40-46. Proc 11th Int Coral Reef Symp. 2009:19-22.
This paper depicted a novel and efficient approach for establishing a large
stock of coral colonies from larvae of a brooding coral species. 41. Iwao K, Omori M, Taniguchi H, Tamura M: Transplanted
Acropora tenuis spawned initially 4 years after egg culture.
25. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English C, Galaxea J Coral Reef Stud 2010, 12:47.
Galindo H, Grebmeier J, Hollowed AB, Knowlton N, Polovina J,
Rabalais NN, Sydeman WJ, Talley LD: Climate change 42. Lirman D, Thyberg T, Herlan J, Hill C, Young-Lahiff C,
impacts on marine ecosystems. Annu Rev Mar Sci 2012, Schopmeyer S, Huntington B, Santos R, Drury C: Propagation of
4:11-37. the threatened staghorn coral Acropora cervicornis: methods
to minimize the impacts of fragment collection and maximize
26. Tepe TL, Meretsky VJ: Forward-looking forest restoration production. Coral Reefs 2010, 29:729-735.
under climate change – are us nurseries ready? Rest Ecol 2011,
19:295-298. 43. Mbije NEJ, Spanier E, Rinkevich B: Testing the first phase of
gardening concept as applicable tool in restoring denuded
27. Gillson L, Dawson TP, Jack S, McGeoch MA: Accommodating reefs of Tanzania. Ecol Eng 2010, 36:713-721.
climate change contingencies in conservation strategy.
Trends Ecol Evol 2013, 28:135-142. 44. Okubo N, Yamamoto HH, Nakayama F, Okaji K: Reproduction in
cultured versus wild coral colonies: fertilization, larval
28. Raymundo LJ, Maypa AP: Getting bigger faster: mediation of oxygen consumption, and survival. Biol Bull 2010,
size-specific mortality via fusion in juvenile coral transplants. 218:230-236.
Ecol Appl 2004, 14:281-295.
45. Bowden-Kerby A, Carne L: Thermal tolerance as a factor in
29. Zahawi RA, Augspurger CK: Tropical forest restoration: tree Caribbean Acropora restoration. Proc 12th Int Coral Reef Symp;
islands as recruitment foci in degraded lands of Honduras. Cairns, Australia: 2012. (in press).
Ecol Appl 2006, 16:464-478.
46. Griffin S, Spathias H, Moore TD, Baums I, Griffin BA: Scaling up
30. Aerts R, Lerouge F, November E, Lens L, Hermy M, Muys B: Land Acropora nurseries in the Caribbean and improving
rehabilitation and the conservation of birds in a degraded techniques. Proc 12th Int Coral Reef Symp; Cairns, Australia:
Afromontane landscape in northern Ethiopia. Biodivers 2012. (in press).
Conserv 2008, 17:53-69.
47. Kiel C, Huntington BE, Miller MW: Tractable field metrics for
31. Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD: Will variation restoration and recovery monitoring of staghorn coral
 among genetic individuals influence species responses to Acropora cervicornis. Endang Species Res 2012,
global climate change? Oikos 2011, 120:675-689. 19:171-176.

www.sciencedirect.com Current Opinion in Environmental Sustainability 2014, 7:28–36

36 Environmental change issues

48. Moothien-Pillay R, Bacha-Gian S, Bhoyroo V, Curpen S: Adapting areas in Bolinao-Anda Reef Complex, Philippines. Mar Biol Res
coral culture to climate change: the Mauritian experience. 2012, 8:877-884.
Western Indian Ocean J Mar Sci 2012, 10:155-167.
51. Young CN, Schopmeyer SA, Lirman D: A review of reef
49. Ng CSL, Ng SZ, Chou LM: Does an ex situ coral nursery restoration and coral propagation using the threatened genus
facilitate reef restoration in Singapore’s waters? Contrib Mar Acropora in the Caribbean and western Atlantic. Bull Mar Sci
Sci 2012:95-100. 2012, 88:1075-1098.

50. Villanueva RD, Baria MVB, dela Cruz DW: Growth and
survivorship of juvenile corals outplanted to degraded reef

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