Rebuilding coral reefs: does active reef restoration lead tosustainable reefs?Baruch Rinkevich

Available online at www.sciencedirect.com

ScienceDirect

The coral reefs worldwide are exposed to multiple

anthropogenic threats and persisting global change impacts,

causing continuous degradation, also calling for the

development of novel restoration methodologies. Of the most

promising emerging approaches, deriving its rationale from

silviculture, is the low-cost ‘gardening concept’, guided by a

two-step restoration operation: (a) mid-water nursery phase,

where coral-nubbins are farmed and (b) transplantation of

nursery-farmed colonies. Tested worldwide, at least 86 coral-

species and over 100 000 colonies were successfully farmed in

different archetype nurseries, and several novel transplantation

methodologies were developed. A number of unanticipated

emerged outcomes were the immediate establishment of coral

infaunal biodiversity in nurseries, the development of nurseries

into ‘larval dispersion hubs’ and the enhanced reproduction of

transplanted coral colonies. Altogether, and in addition to

envisaged results (e.g., high survivorship, fast coral growth),

results attest that the gardening-toolbox could serve as a

ubiquitous ecological engineering platform for restoration on a

global scale.

Addresses

National Institute of Oceanography, Tel Shikmona, PO Box 8030, Haifa

31080, Israel

Corresponding author: Rinkevich, Baruch (buki@ocean.org.il)

Current Opinion in Environmental Sustainability 2014, 7:28–36

This review comes from a themed issue on Environmental change

issues

Edited by Georgios Tsounis and Bernhard Riegl

For a complete overview see the Issue and the Editorial

Available online 20th December 2013

1877-3435/$ – see front matter, # 2013 Elsevier B.V. All rights

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http://dx.doi.org/10.1016/j.cosust.2013.11.018

IntroductionThe ominous status of coral reefs worldwide and active

reef restoration

Once acknowledging the vital ecological importance of

coral reefs and their fundamental roles in sustaining

hundreds of millions of people, it is dismaying to realize

that over the last four decades ca. 40% of the global

coral-reef system has been lost, a process galloping at 1–2% per year [1], not considering the developing global

change impacts that are exacerbated by severe anthro-

pogenic pressures. Thus, coral reefs, while exhibiting

exceptional species diversity, are poorly protected,

Current Opinion in Environmental Sustainability 2014, 7:28–36

highly degraded, and exposed to multiple persisting

and envisaged threats [2,3]. The stressors, and notwith-

standing all traditional conservation management

measures implemented [4], would lead to loss of up

to 70% of reef area within four decades or to phase shift

[1].

The above causes that have led to progressive impair-

ment of the normal course of coral-reefs life and their

global contribution to humans, without proper damage

control or repair, have prompted the demand for

alternative active reef restoration measures, beyond the

traditionally employed conservation. Restoration is

defined by the Society of Ecological Restoration as ‘the

process of assisting the recovery of an ecosystem that has

been degraded, damaged, or destroyed’ [5]; it has

also been acknowledged that restoration activities

may complement [6], even substitute conservation

efforts. Whereas the restoration rationale is rooted in

active approaches to solve ecosystem degradation (‘Eco-

logical restoration is an engaging and inclusive process’;

[5]), conservation biology endeavors preservation, count-

ing on long-term ecological succession as the major

repairing mechanism for impacted ecosystems. The lit-

erature documents that ecological restoration is a fast

developing scientific discipline. Heeding the invaluable

lessons gathered from the failures of traditional conser-

vation, the declaration of the Convention on Biological

Diversity that restoration of terrestrial, inland water and

marine ecosystems is essential for rehabilitating the

ecosystem’s functioning, goods and services [6], confirms

the wide scientific support of ecological restoration

efforts. In fact, the extent of anthropogenic and global

change impacts on coral reefs worldwide renders their

active restoration as a major conceptual and practical

approach, not just as assistant act to traditional conserva-

tion acts [4,7,8].

Restoration practices for degraded reefs can be broadly

categorized into passive or active restoration [4,7,8].

Active restoration, or active human intervention in

degraded reef sites, disputes passive restoration, the

dependency on natural regeneration and repair with

minimal human surrogacy. Indeed, when analyzing glob-

ally employed passive restoration measures, it is evident

that the reef management acts have been imperfect,

failed to ascertain the right responses to key threats,

failed to yield a quantifiable return and are ineffective

in ameliorating long-term impairments [summarized in

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

Ree

f se

rvic

es

Ecological complexity

Restoration scenarios

High

1Primevalcharacters

Degraded status

Low

6

2

4

7

3??

??

5

Replacement status

Restored

Restored

Restored

??

????

Degradedreef

Replacement status

Current Opinion in Environmental Sustainability

Figure depicts multiple ‘restored reef-state’ scenarios (circles no 3–7)

showing paths from a degraded reef (low ecological complexity and

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

attempts (a) aiming to boost reef services (such as installing artificial

reefs for fisheries; circle 6) or whole colonies transplantation acts [9] and

(b) aiming to increase biodiversity, such as the concept of ‘assisted

colonization’ [10�] (circle 7). In both scenarios it is more likely that reef

environments will revert to their degraded status than advance toward a

better state (marked by question marks). Three different scenarios

employing the ‘gardening concept’ [4,7–9,12��,13,14,15�,16–23] are

defined. These may result in rehabilitated reefs at different complexity/

reef services states (circles 3–5) that could develop into other states and

possibly (question marks) will culminate with the primeval reef status.

the implication of either practice, the restored ‘reefs of

tomorrow’ will be different from the current or past reefs’

constructions (Figure 1).

The gardening tenetSeveral approaches for active restoration have been

suggested; some have been subjected to intensive

research manipulations. One of the first advocated meth-

odologies was the direct transplantation of coral material

(entire coral colonies and/or fragments), an approach

subjected to a wide range of limitations and pitfalls, such

as negative impacts on donor reefs and on transplanted

coral colonies [8,9]. A comparable, more recent approach

is the controversial tool of ‘assisted colonization’ or ‘man-

aged relocation’ [reviewed in 10�], claiming active trans-

location of groups of species outside the species’ historic

range for conservation purposes.

One of the most promising active restoration approaches

is the ‘gardening concept’ [4,7–9], which has surfaced as a

means to avoid the pitfalls associated with the traditional

management for coral reefs (e.g., reduced negative

impacts on donor reefs, high survivorship of transplanted

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coral colonies, improved state of health of transplants,

year round availability of transplants). This strategy,

which derives its rationale from silviculture, is guided

by a two-step restoration operation. The first step entails

rearing stocks of small coral fragments in specially

designed mid-water floating nurseries, and upon reach-

ing suitable sizes, applying the second step, the trans-

plantation of nursery-farmed coral colonies onto

denuded reef areas. As restoration ecology is rooted in

forestation, it is therefore not surprising that silviculture

principles, concepts and theories, are intermingled

within the ‘gardening’ notion and its associated activi-

ties. During the almost two decades from their first

presentation [9], the two gardening tenet steps have

been tested in various reefs worldwide (Table 1 dis-

cusses the nursery step; studies performed in the Red

Sea, Thailand, Singapore, Philippines, Tanzania,

Mauritius, Seychelles, Caribbean sites [Jamaica, Florida

keys, Colombia, Belize, and more], Japan, Taiwan,

Hawaii; much of the outcomes is still unpublished

[3,11,12��,13,14,15�,16–23]).

The nursery phase of the ‘gardening concept’ has been

drawing the most scientific investigation, conceptually

and technically addressed in detail, with at least 86 coral

species farmed in underwater nurseries, worldwide (117

species when total farmed species in all nurseries is

considered, Table 1; only species from literature and

personal communication are listed). Issues, such as nur-

sery structure, nursery types, nursery’s set-up, shape and

construction, nursery location, maintenance subjects,

coral species cultured (types, numbers) and genotypic

considerations, spacing of farmed coral colonies, realistic

number of generated and farmed colonies, duration of the

nursery phase, growth rates of farmed corals, longevity of

farmed colonies, pest control and economic consider-

ations are some of the topics studied recently. The second

phase of transplantation, which is still in its infancy, has

also revealed promising results ([12��,13,14,15�], unpub-

lished). The major conclusion which emerged from the

above studies is that the application of active restoration

protocols may enhance reef recovery [4,7,8].

The results obtained from various reefs worldwide

cumulatively have revealed that the gardening tenet,

with modifications and adjustments per local conditions,

can be used as a ubiquitous management instrument

for rescuing reefs from the on-going degradation

(Box 1).

What has been learnt recently fromnursery/transplantation acts?Studies [11,12��,14,15�,16–23,24�] have already revealed

that farmed corals not only compete successfully with

natural colonies’ performance, but also exhibit improved

health status, being free of parasites and diseases (devel-

oped and maintained under controlled conditions), with

Current Opinion in Environmental Sustainability 2014, 7:28–36

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 +

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

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-

round availability, circumventing the need to explore

sites for harvesting additional material [3,12��,24�].

The mid-water floating nurseries have already been

established as a successful farming tool. It is estimated

that >100 000 colonies from 86 coral species (Table 1) of

Box 1 Major considerations when approaching reef restoration

project under the ‘gardening concept’

What is needed to know?

� Primeval local reefs’ status

� Getting acquainted with key/dominant species biological patterns

� Population genetics of local species

� Past bleaching events and disease outbreaks, including

consequences

� Conferring on connectivity trajectories, resistance/resilience

attributes, top-down/bottom-up controls

� Quantified reef services; defined reef stakeholders

� List of natural/anthropogenic threats

� Anticipated climate change impacts

� Evaluation of current conservation acts

Issues to be considered:

� Some reefs might not need active restoration (highly resilient/

resistant reefs)

� Some reefs should not be restored (reefs under severe

anthropogenic impacts)

� Vision for the status of the ‘reef of tomorrow’ for each locality

� Pre-planning of nursery/transplantation scenarios and colonies/

genotypes/species numbers

� Different spatial/temporal reef-features require different

restoration methodologies

� Close monitoring of each of the restoration acts

� Flexible to revise/change approaches not successfully developed

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various forms (branching, massive and encrusting species)

have already been farmed in these nurseries, worldwide,

showing minor mortalities and enhanced growth rates.

These nurseries are usually installed in a protected site,

away from major natural reef structures, away from the

afflictions of recreational activities and corallivorous

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

nurseries (Figure 2) unexpectedly revealed: (a) that

swinging in all directions enhances food and oxygen

supplies and facilitates clearing of debris and sediment

particles that might accumulate on farmed coral colonies

[3,19]; (b) reduced sedimentation fluxes, since nurseries

are above substrate; (c) depth adjustment, ‘tailored’ for

any species-specific needs, also allowing acclimatization

of farmed corals to conditions in their designated trans-

plantation site [3]; (d) mid-water nursery attracts com-

mensals and coral inhabiting species arriving from the

plankton, for the establishment of the entire coral infau-

nal biodiversity [19]; and (e) early onset of sexual repro-

duction in farmed corals, changing the nursery into ‘larval

dispersion hub’ that can be used as a management tool for

natural recruitment enhancement [11]. Above themes

attest that the tool of a floating nursery could serve as

a ubiquitous platform for developing restoration protocols

applicable on a global scale.

The transplantation phase has further benefitted from

developing a wide array of new methodologies, like

transplantation into drilled holes, transplantation on

wire mesh, chiselling holes in softer substrate, lining of

Current Opinion in Environmental Sustainability 2014, 7:28–36

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,

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

Active reef restoration and sustainable reefs Rinkevich 33

rope-nursery grown corals on soft and hard substrates,

and more ([12��,15�,21,22]; Figure 2). By using these

methods, not only is the coral community rehabilitated,

but its entire carrying capacity also increases due to the

new ecological and spatial niches added to the site.

However, transplantation methodologies are still chal-

lenged by scientific and technical defies. The scientific

part focuses on issues, such as genetics, species combi-

nations, landscape manipulations, biological engineering

and key species. One point to consider and test is spacing

of transplants. Transplants require sufficient space for

growth in order to avoid intraspecific or interspecific

disturbances. Allogeneic and xenogeneic interactions

can cause damage and growth abatement, influence

reproductive activities or cause death. Clearly, studies

on the second phase of the gardening tenet are still very

limited and should be increased.

The ‘gardening concept’ as an adaptive tool tocombat climate change impactsThe literature attests that global climate changes occur

and that they differentially alter regional ecosystems,

causing unprecedented degradation to coral reefs [25].

Climate changes present new challenges to coral reef

scientists and policy makers by creating novel coral

assemblages, whose ecological properties, goods and ser-

vices differ from those characterizing preceding reef

ecosystems (Figure 1). The exacerbated impacts on the

reefs lead to the conclusion that current conservation

methodologies are failing to support biodiversity and reef

services; clearly insufficient for averting reef degradation

[4].

These impacts of climate change necessitate the devel-

opment of unorthodox approaches, led by the notion that

‘restoration efforts once focused on past conditions should

become more forward-looking’ [26]. On the basis of this

rationale, restoration activities should highlight climate

change scenarios, focusing on adaptation strategies that

had not been considered in past reef management set-

tings. This may raise suggestions for more radical

approaches like ‘assisted colonization’ [reviewed in 10�]or for focusing only on sites that are, and predicted to

remain, under conditions suitable for current coral assem-

blages. Both approaches deviate conceptually from the

‘reef gardening’ notion.

The gardening concept is using proactive responses

to global changes, incorporating major amendments

in current restoration methodologies. While past restor-

ation studies have focused on establishing key group

(Figure 2 Legend Continued) powered by pressured air from diving tan

were attached on wire metal mesh construction (insert figure) by plastic t

used environmental friendly materials, like bamboo canes (photograph by

Beach), five years after coral transplantation. Many fish and reef-associa

patch reef (photograph by Y. Horoszowski-Friedman).

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communities, the gardening concept supports use of coral

species/genotypes that would be favorable in the anticip-

ated climate change conditions, overlooking coral species/

genotypes that are less tolerant to climatic conditions;

therefore reassembling novel coral reef communities that

are robust to global change conditions [27]. Other tools

incorporate selected ecological engineering aspects

[12��,28], taking into account corals functioning as

primary reef ecosystem engineers. These tools rehabili-

tate coral reefs with larvae released from nursery-farmed

corals, from transplanted coral colonies, considering var-

ious techniques for coral transplantation, coral coverage,

assorted coral species compositions and engineered

seascape [2,3,4,11,12��,20,21]. Whereas neoteric in the

coral restoration discipline, the ecosystem engineering

approach is deeply rooted in terrestrial restoration

measures, revealing, for example, increased bird visita-

tions in reforestation [29] or enriched forest species in

grazer-enclosure regenerating forests [30].

Paramount to the success of the gardening concept is the

proficiency to harness genetic backgrounds of farmed

colonies as an applied tool for restoration that targets

global change. Minimal insight is available for the ways

genotypic variation influence adaptive global changes

competence [31��]. However, recent scientific interest

in the relationships between genotypes and gene expres-

sion, as to the kaleidoscope of responses to various stress

conditions, has revealed that genetic legacy may serve as a

prime applied tool for combating global change impacts

[32], further suggesting the accommodation of climate

change contingencies in reef restoration practices.

Because of stochastic reproduction and dispersal pro-

cesses, genetic repertoires presented by marine organisms

at any specific time/location may not reach equilibrium

with today’s climate, providing the opportunity to search

for genotypes that are not perfectly adapted to current

conditions but better suited for future environmental

settings and farm them within underwater coral nurseries.

This is further important as accelerating global change

rates, which are notoriously exceeding the evolutionary

capacity of corals to acclimatize [33], are primarily

relevant to long-lived coral species. Coral bleaching, for

example, is conspicuously patchy between different gen-

otypes, representing a signature of true genetic hetero-

geneity and revealing an acclimatization response rooted

in epigenetics. Therefore, genetic variation should be a

potential reservoir of resilience to climate change,

a characteristic that can be actively amplified when

developing coral farming/breeding protocols under in situnursery conditions.

ks (photograph by Y. Horoszowski-Friedman). In Thailand (e), corals

ies, which is cheap and fast for attaching. Other studies (unpublished)

G. Levi). (f) A denuded reef patch in the northern Gulf of Eilat (Dekel

ted invertebrates were attracted and recruited to this restored small

Current Opinion in Environmental Sustainability 2014, 7:28–36

34 Environmental change issues

Underwater coral nurseries may also serve as genetic

repositories for coral reef restoration, combating the

impacts of major natural catastrophes [22,34�]. The use

of the ‘reef gardening’ rationale as global change mediator

through nurseries [20,21,22,24�,34�] has already revealed

two novel strategic roles of this instrument, (a) reducing

coral mortality during events, such as massive coral

bleaching, hurricanes and fresh water floods, the creation

of climatic refugia and (b) preserving and propagating

diverse coral genotypes from various source materials for

the establishment of regional/local ‘gene stocks’ for use in

restoration activities, with an eye to initiation of breeding

programs. The ‘reef gardening’ rationale has further

disclosed strategic considerations of this instrument

([12��,15�,22], unpublished), including re-shaping of coral

reefs types, changing of reef rugosity, engineering of coral

seeding processes, reducing of fleshy algae allotment in

restored reefs and sustaining of ecosystem processes.

Would the coral ‘gardening tenet’ lead tosustainable reefs?Theoretical and empirical aspects of active reef restor-

ation are still in their nascent stages, awaiting further

work. Active reef restoration holds a number of challen-

ging issues and uncertainties, such as the issues of pre-

dicting the scale of transplantation impacts, the responses

of transplanted colonies in their new ‘homes’ and the

suitability of these acts to combat reef degradation.

The progression of the ‘gardening notion’ has sur-

mounted four major obstructions, all are satisfactorily

deciphered: (a) developing the needed credentials for

farming a wide variety of coral species in mid-water

nursery (Table 1); (b) the ability to develop stocks of

coral colonies, employing the ‘nubbins’ methodology

[16,19]; (c) documentation that nursery farmed coral

colonies perform well in their ‘new homes’, following

transplantation ([12��,15�,22], unpublished); and (d) ver-

ification of the low cost gardening approach (down to 0.17

and 0.19 US$/coral colony for farming and transplan-

tation, phases, respectively [15�,20]. Now, the ‘gardening

notion’ is facing its fifth challenge, performing a large,

ecologically profound restoration act (hundreds of thou-

sands of coral colonies/site) to reveal the ecological

engineering capacities of large-scale transplantation acts.

This challenge is the most imperative because it would

demonstrate that the gardening approach is supporting

the initiation of sustainable coral reefs.

The gardening toolbox may further be used for testing

novel approaches, such as developing of improved corals

through epigenetics. Studies (e.g., [35]) have revealed

that under a wide range of ecological insult scenarios,

organisms modify levels of genome epigenetics that may

coincide with increased tolerance to otherwise lethal

conditions, further showing that these epigenetic changes

may be stable across multiple generations. Therefore,

Current Opinion in Environmental Sustainability 2014, 7:28–36

genome-wide transcriptional plasticity may underlie

whole organism adaptation to novel environmental

insults, like those presented by global change [36�] and

can be used as an applied tool in coral nurseries.

Acknowledgements

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,by the INCO-DEV project (REEFRES, no. 510657), the CORALZOO, anEC Collective Research project, the AID-CDR (C23-004) program, by theWorld Bank/GEF project (reef remediation/restoration working group) andby the Ministry of Science & Technology, Israel & the Ministry ofEducation, France.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

1. Bruno JF, Selig ER: Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoSONE 2007, 2:e711.

2. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD,Sweatman H, Melendy AM: Thermal stress and coral coveras drivers of coral disease outbreaks. PLoS Biol 2007,5:1220-1227.

3. Shafir S, Rinkevich B: The underwater silviculture approach forreef restoration: an emergent aquaculture theme. InAquaculture Research Trends. Edited by Schwartz SH. New York:Nova Science Publications; 2008:279-295.

4. Rinkevich B: Management of coral reefs: we have gone wrongwhen neglecting active reef restoration. Mar Pollut Bull 2008,56:1821-1824.

5. SER: The SER Primer on Ecological Restoration. Version 2. Societyfor Ecological Restoration Science and Policy Working Group;2004 http://www.ser.org.

6. Normile D: UN Biodiversity Summit yields welcome andunexpected progress. Science 2010, 330:742-743.

7. Rinkevich B: Conservation of coral reefs through activerestoration measures: recent approaches and last decadeprogress. Environ Sci Technol 2005, 39:4333-4342.

8. Rinkevich B: The coral gardening concept and the use ofunderwater nurseries; lesson learned from silvics andsilviculture. In Coral Reef Restoration Handbook. Edited byPrecht WF. Boca Raton, FL: CRC Press; 2006:291-301.

9. Rinkevich B: Restoration strategies for coral reefs damaged byrecreational activities: the use of sexual and asexual recruits.Restor Ecol 1995, 3:241-251.

10.�

Chauvenet ALM, Ewen JG, Armstrong DP, Blackburn TM,Pettorelli N: Maximizing the success of assisted colonization.Anim Conserv 2013, 16:161-169.

The authors reviewed here the concept of ‘assisted colonization’ andrecent literature that support or negate the application of this restorationapproach.

11. Amar KO, Rinkevich B: A floating mid-water coral nursery aslarval dispersion hub: testing an idea. Mar Biol 2007,151:713-718.

12.��

Horoszowski-Friedman YB, Izhaki I, Rinkevich B: Engineering ofcoral larval supply through transplantation of nursery-farmedgravid colonies. J Exp Mar Biol Ecol 2011, 399:162-166.

In this paper, the author showed that transplanted coral colonies releaselarvae in an order of magnitude more than natal colonies, years after theirtransplantation, indicating that nursery-grown corals may be used toenhance reef resilience by contributing to the larval pool. This establishesthe 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 Acroporatenuis 2 years after egg culture. Coral Reefs 2008, 27:165.

14. Nakamura R, Ando W, Yamamoto H, Kitano M, Sato A,Nakamura M, Kayanne H, Omori M: Corals mass-cultured fromeggs and transplanted as juveniles to their native, remotecoral reef. Mar Ecol Prog Ser 2011, 436:161-168.

15.�

Mbije NEJ, Spanier E, Rinkevich B: A first endeavour in restoringdenuded, post-bleached reefs in Tanzania. Estuar Coast ShelfSci 2013, 128:41-51.

Here, the authors showed, by employing field studies in Tanzania andeconomic evaluations that transplantation of nursery-farmed coloniesinto denuded reef areas might uphold critical ecosystem functions whileused in reversing phase shift states in coral reefs.

16. Shafir S, Van Rijn J, Rinkevich B: Steps in the construction ofunderwater coral nursery, an essential component in reefrestoration acts. Mar Biol 2006, 149:679-687.

17. Shafir S, van Rijn J, Rinkevich B: A mid-water coral nursery.Proc 10th Int Coral Reef Symp. 2006:1674-1679.

18. Shaish L, Levy G, Gomez E, Rinkevich B: Fixed and suspendedcoral nurseries in the Philippines: establishing the first step inthe ‘gardening concept’ of reef restoration. J Exp Mar Biol Ecol2008, 358:86-97.

19. Shafir S, Rinkevich B: Integrated long term mid-water coralnurseries: a management instrument evolving into a floatingecosystem. Mauritius Res J 2010, 16:365-379.

20. Levi G, Shaish L, Haim A, Rinkevich B: Mid-water rope nursery –testing design and performance of a novel reef restorationinstrument. Ecol Eng 2010, 36:560-569.

21. Shaish L, Levi G, Katzir G, Rinkevich B: Employing a highlyfragmented, weedy coral species in reef restoration.Ecol Eng 2010, 36:1424-1432.

22. Shaish L, Levi G, Katzir G, Rinkevich B: Coral reef restoration(Bolinao, the Philippines) in the face of frequent naturalcatastrophes. Restor Ecol 2010, 18:285-299.

23. Bongiorni L, Giovanelli D, Rinkevich B, Pusceddu A, Chou LM,Danovaro R: First step in the restoration of a highly degradedcoral reef (Singapore) by in situ coral intensive farming.Aquaculture 2011, 322–323:191-200.

24.�

Linden B, Rinkevich B: Creating stocks of young colonies frombrooding-coral larvae amenable to active reef restoration.J Exp Mar Biol Ecol 2011, 398:40-46.

This paper depicted a novel and efficient approach for establishing a largestock of coral colonies from larvae of a brooding coral species.

25. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English C,Galindo H, Grebmeier J, Hollowed AB, Knowlton N, Polovina J,Rabalais NN, Sydeman WJ, Talley LD: Climate changeimpacts on marine ecosystems. Annu Rev Mar Sci 2012,4:11-37.

26. Tepe TL, Meretsky VJ: Forward-looking forest restorationunder climate change – are us nurseries ready? Rest Ecol 2011,19:295-298.

27. Gillson L, Dawson TP, Jack S, McGeoch MA: Accommodatingclimate change contingencies in conservation strategy.Trends Ecol Evol 2013, 28:135-142.

28. Raymundo LJ, Maypa AP: Getting bigger faster: mediation ofsize-specific mortality via fusion in juvenile coral transplants.Ecol Appl 2004, 14:281-295.

29. Zahawi RA, Augspurger CK: Tropical forest restoration: treeislands as recruitment foci in degraded lands of Honduras.Ecol Appl 2006, 16:464-478.

30. Aerts R, Lerouge F, November E, Lens L, Hermy M, Muys B: Landrehabilitation and the conservation of birds in a degradedAfromontane landscape in northern Ethiopia. BiodiversConserv 2008, 17:53-69.

31.��

Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD: Will variationamong genetic individuals influence species responses toglobal climate change? Oikos 2011, 120:675-689.

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Studying ecologically relevant processes of growth and reproduction,the authors demonstrated the existence of relevant levels of variationamong genetic individuals, which may enable future adaptation vianon-mutational natural selection to global change impacts.

32. Evans TG, Hoffman GE: Defining the limits of physiologicalplasticity: how gene expression can assess and predict theconsequences of ocean change. Philos Trans R Soc Lond B2012, 367:1733-1745.

33. Howells EJ, Berkelmans R, van Oppen MJH, Willis BL, Bay LK:Historical thermal regimes define limits to coralacclimatization. Ecology 2013, 94:1078-1088.

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Schopmeyer SA, Lirman D, Bartels E, Byrne J, Gilliam DS, Hunt J,Johnson ME, Larson EA, Maxwell K, Nedimyer K, Walter C: In situcoral nurseries serve as genetic repositories for coral reefrestoration after an extreme cold-water event. Restor Ecol2011, 20:696-703.

The authors documented in this paper that coral nurseries could beused as genetic repositories for future coral reef restoration acts, com-bating the impacts of major natural catastrophes, creating of climaterefugia.

35. Stern S, Fridmann-Sirkis Y, Braun E, Soen Y: Epigeneticallyheritable alteration of fly development in response to toxicchallenge. Cell Rep 2012, 1:528-542.

36.�

Cebrian E, Kipson S, Garrabou J: Does thermal history influencethe tolerance of temperate gorgonians to future warming?Mar Environ Res 2013, 89:45-52.

This work revealed the role of thermal history in shaping the thermo-tolerance responses of Mediterranean gorgonians dwelling under con-trasting temperature environments. Although not addressing the conceptof epigenetics, the results highly suggested this phenomenon.

37. Soong K, Chen T: Coral transplantation: regeneration andgrowth of Acropora fragments in a nursery. Restor Ecol 2003,11:62-71.

38. Omori M: Success of mass culture of Acropora corals from eggto colony in open water. Coral Reefs 2005, 24:563.

39. Chou LM, Yeemin T, Abdul Rahim BGY, Si Tuan VO, Alino PM:Suharsono: coral reef restoration in the South China Sea.Galaxea J Coral Reef Stud 2009, 11:67-74.

40. Putchim L, Thongtham N, Hewett A, Chansang H: Survival andgrowth of Acropora spp. in mid-water nursery and aftertransplantation at Phi Phi Islands, Andaman Sea, Thailand.Proc 11th Int Coral Reef Symp. 2009:19-22.

41. Iwao K, Omori M, Taniguchi H, Tamura M: TransplantedAcropora tenuis spawned initially 4 years after egg culture.Galaxea J Coral Reef Stud 2010, 12:47.

42. Lirman D, Thyberg T, Herlan J, Hill C, Young-Lahiff C,Schopmeyer S, Huntington B, Santos R, Drury C: Propagation ofthe threatened staghorn coral Acropora cervicornis: methodsto minimize the impacts of fragment collection and maximizeproduction. Coral Reefs 2010, 29:729-735.

43. Mbije NEJ, Spanier E, Rinkevich B: Testing the first phase ofgardening concept as applicable tool in restoring denudedreefs of Tanzania. Ecol Eng 2010, 36:713-721.

44. Okubo N, Yamamoto HH, Nakayama F, Okaji K: Reproduction incultured versus wild coral colonies: fertilization, larvaloxygen consumption, and survival. Biol Bull 2010,218:230-236.

45. Bowden-Kerby A, Carne L: Thermal tolerance as a factor inCaribbean Acropora restoration. Proc 12th Int Coral Reef Symp;Cairns, Australia: 2012. (in press).

46. Griffin S, Spathias H, Moore TD, Baums I, Griffin BA: Scaling upAcropora nurseries in the Caribbean and improvingtechniques. Proc 12th Int Coral Reef Symp; Cairns, Australia:2012. (in press).

47. Kiel C, Huntington BE, Miller MW: Tractable field metrics forrestoration and recovery monitoring of staghorn coralAcropora cervicornis. Endang Species Res 2012,19:171-176.

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36 Environmental change issues

48. Moothien-Pillay R, Bacha-Gian S, Bhoyroo V, Curpen S: Adaptingcoral culture to climate change: the Mauritian experience.Western Indian Ocean J Mar Sci 2012, 10:155-167.

49. Ng CSL, Ng SZ, Chou LM: Does an ex situ coral nurseryfacilitate reef restoration in Singapore’s waters? Contrib MarSci 2012:95-100.

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

Current Opinion in Environmental Sustainability 2014, 7:28–36

areas in Bolinao-Anda Reef Complex, Philippines. Mar Biol Res2012, 8:877-884.

51. Young CN, Schopmeyer SA, Lirman D: A review of reefrestoration and coral propagation using the threatened genusAcropora in the Caribbean and western Atlantic. Bull Mar Sci2012, 88:1075-1098.

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