Marine silviculture: Incorporating ecosystem ...

See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/276366223

Marine silviculture: Incorporating ecosystem engineering properties into reef restoration acts ARTICLE in ECOLOGICAL ENGINEERING · SEPTEMBER 2015 Impact Factor: 2.58 · DOI: 10.1016/j.ecoleng.2015.04.104

READS

41

7 AUTHORS, INCLUDING: Y.B. Horoszowski-Fridman

Baruch Rinkevich

Israel Oceanographic and Limnological Res…

Israel Oceanographic and Limnological Res…

3 PUBLICATIONS 13 CITATIONS

298 PUBLICATIONS 5,852 CITATIONS

SEE PROFILE

SEE PROFILE

Available from: Y.B. Horoszowski-Fridman Retrieved on: 13 October 2015

Ecological Engineering 82 (2015) 201–213

Contents lists available at ScienceDirect

Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng

Marine silviculture: Incorporating ecosystem engineering properties into reef restoration acts Yael B. Horoszowski-Fridman a,b, * , Jean-Claude Brêthes b , Nathaële Rahmani c, Baruch Rinkevich a a b c

Israel Oceanography and Limnological Research, Tel-Shikmona, Haifa 31080, Israel Universite du Quebec a Rimouski, ISMER, Rimouski, Québec, Canada The French Scientific Office for Cooperation, Tel Aviv 63572, Israel

A R T I C L E I N F O

A B S T R A C T

Article history: Received 2 March 2014 Received in revised form 10 February 2015 Accepted 5 April 2015 Available online xxx

In the gardening approach for reef restoration, coral stocks are farmed in underwater nurseries (phase I) prior to their transplantation onto degraded reefs (phase II). The phase I aspects were already evaluated in the literature, but very little is known about the phase II outcomes. Assessing phase II feasibility, we transplanted 554 nursery-farmed colonies of two branching species (Stylophora pistillata, Pocillopora damicornis) onto five denuded knolls in Eilat (Red Sea). The performance of the transplants was compared for 17 months with 76 natal colonies and 217 colonies maintained at the coral-nursery. At the natural reef, rates of full/partial mortalities, detachment and fish herbivory were considerably higher than the nursery values. While corallivory on Pocillopora transplants was comparable to that observed in natal colonies, herbivory on Stylophora transplants increased 2.2 fold compared to natal controls. Their survivorship was similar to the survivorship observed in natal colonies in the 9 months post transplantation, but was 30% higher after 17 months. In contrast, no enhanced mortality was documented in Pocillopora transplants throughout the entire period. The detachment levels of the Stylophora and Pocillopora transplants were 3 and 10 times higher, respectively, than those observed in natal colonies, and the growth rates of the transplants were identical to the rates observed in the nursery control groups. Transplants showed a 2.5–3.3 fold increase in colonial ecological-volumes, resulting in enhanced acquired space/habitats for coral-dwelling species like Trapezia, Alpheus, Spirobranchus and Lithophaga. The successful integration of farmed transplants in Eilat’s degraded reef and their provision of new ecological niches for reefassociated fauna, coupled with economic assessments, indicate that transplantation of farmed corals is an easy, cost-effective mean to counteract degradation of coral reefs. Results also imply that the selection of coral species for reef restoration should take into consideration their autogenic/allogenic engineering properties, particularly if the aims are to restore the whole reef community, rather than simply focus on coral coverage. ã 2015 Elsevier B.V. All rights reserved.

Keywords: Coral Gardening approach Eilat Ecosystem engineers Nursery Transplantation.

1. Introduction Coral reefs are paramount marine ecosystems, providing vital goods and services for hundreds of millions of people worldwide and functioning as focal biomes that serve as spawning, nursery,

* Corresponding author at: Israel Oceanography and Limnological Research, TelShikmona, Haifa 31080, Israel. Tel.: +972 4 8565273. E-mail addresses: [email protected] (Y.B. Horoszowski-Fridman), [email protected] (J.-C. Brêthes), [email protected] (N. Rahmani), [email protected] (B. Rinkevich). http://dx.doi.org/10.1016/j.ecoleng.2015.04.104 0925-8574/ ã 2015 Elsevier B.V. All rights reserved.

breeding and feeding grounds for a myriad of marine organisms. Overexploitation of reef resources, anthropogenic activities and intensifying global changes have led to alarming worldwide degradation (Rogers et al., 2015). This resulted in the loss of important seascapes and the shelter, reproduction and larval settlement sites of reef-dwelling invertebrates and fish (Baker et al., 2008), leading to permanent shifts in reef communities and to changes in biotic and abiotic conditions (Hughes et al., 2010; Graham et al., 2014). Degrading coral reefs do not often recover naturally without human intervention (Rinkevich, 1995, 2005a, 2008), as regaining pre-disturbance coral cover, species-diversity and framework

202

Y.B. Horoszowski-Fridman et al. / Ecological Engineering 82 (2015) 201–213

complexity requires decades to centuries (Baker et al., 2008). Properly implemented conservation measures have the potential to enable the natural recovery of reefs systems; however, the current management efforts and legislations (termed ‘passive restoration’) do not achieve the conservation objectives in reefs severely transformed by anthropogenic induced changes, in which resilience capacities have been substantially reduced (Rinkevich, 2008; Sale, 2008; Hughes et al., 2010). With the obvious need to assist and accelerate the recovery of threatened biodiversity and ensure the future provision of ecosystem services, reef managers and policy makers must supplement passive restoration tools with active ones (i.e., coral farming, coral transplantation, reef seeding; Rinkevich, 1995, 2005a,b, 2008; Cooper et al., 2014). Until recently, active reef restoration initiatives (with the exception of ship grounding restoration operations) have relied on direct transplantation of coral colonies/fragments collected from donor reef sites (Plucer-Rosario and Randall, 1987; Guzman, 1991; Clark and Edwards, 1995; Yap et al., 1998; Nagelkerken et al., 2000; Lindahl, 2003; Okubo et al., 2005). But the ongoing worldwide decline, the damages caused by the removal of corals, the stress inflicted when fragmenting donor colonies and the scarcity of donor sites have all raised questions regarding the sustainability of such practices. To overcome the above-mentioned drawbacks, the marine silviculture approach ‘gardening coral reefs’ (Rinkevich, 1995, 2005a, 2006, 2008) was developed. Inspired by forest restoration rationales, this two-step approach consists of farming large amounts of corals of plantable size from minute fragments in underwater nurseries and then transplanting the farmed colonies onto degraded reefs. The

first step has been intensely investigated in the last decade (Becker and Mueller, 2001; Soong and Chen, 2003; Omori, 2005; Shafir et al., 2006; Amar and Rinkevich, 2007; Shafir and Rinkevich, 2008, 2010; Shaish et al., 2008, 2010a,b; Okamoto et al., 2008; Levy et al., 2010; Lirman et al., 2010; Mbije et al., 2010; Bongiorni et al., 2011; Linden and Rinkevich, 2011; Schopmeyer et al., 2012; Iwao et al., 2014 nurseries established in Red Sea Philippines, Tanzania, Thailand, Jamaica, Florida, Japan, Singapore). The optimal conditions for coral survival/growth that prevail in underwater nurseries, together with intensive maintenance protocols, generate considerable coral stocks from a wide range of source materials, including corals of opportunity (loose fragments collected on reefs), minute fragments (nubbins; 1–10 polyps) and sexual recruits. The use of coral-nubbins substantially diminishes the stress inflicted to donor colonies (Shafir et al., 2006), allowing the propagation of rare and endangered species. Likewise, coral stockpiles reared in nurseries can be re-pruned, allowing intensified production of new coral colonies of selected genotypes, and the transplantation of farmed adult-colonies, rather than coralfragments, can enhance acclimatization on degraded reefs (Forrester et al., 2012). Transplanted corals are also able to contribute to local coral reproduction long after transplantation (Horoszowski-Fridman et al., 2011). Due to the novelty of the marine silviculture concept, the second step of the gardening methodology has not yet been fully explored. Likewise, a detailed follow-up study evaluating the ecological engineering properties of transplants has not yet been done. In this article, we focus on the second step of the gardening

Fig. 1. The Study site and the transplantation procedure. (a) A map of the northern Gulf of Eilat. Coral-nursery: CN; Fish farms: FF; Restoration site: DB; Navy port: NP; commercial port: CP. (b) The location of the transplanted and reference knolls at Dekel Beach. Oval white circles represent knolls not included in the research. (c) A plastic peg cleaned of fouling organisms prior to transplantation. (d) Drilling the substrate at the restoration site. (e) Transplantating a Pocillopora colony.


203

Table 1 Characteristics of experimental (T1-T5) and reference knolls (C1-C6) at Dekel Beach. Knoll

Height (m)

Basal perimeter (m)

Surface area (m2)a

Depth (m)

T1 T2 T3 T4 T5 C1 C2 C3 C4 C5 C6

2.5 1.9 2.0 1.1 2.2 1.2 1.1 1.9 1.0 0.4 1.5

17.0 11.6 8.0 6 .8 11.0 3.8 17.0 11.0 4.5 9.0 9.5

48 30 19 9 34 9 40 42 5 14 21

6.6 8.8 8.3 13.0 8.1 9.8 8.6 6.5 12.1 9.7 12.0

a

Hard coral cover (%)a Before transplantation

After transplantation

26 10 5 10 19 1 45 18 8 34 51

28 25 12 23 24

Calculated from digital photographs according to Belmaker et al., 2007.

methodology, in which 554 nursery-grown colonies of two branching species that were transplanted on a degraded reef in Eilat, Israel, were followed for over 17 months. Survivorship, partial tissue loss, fish attacks, zooxanthellae parameters and growth of farmed transplants, as well as their impacts on key coralassociated invertebrates, were monitored during this time. The labor and costs associated with farmed-coral transplantation are evaluated and silvicultural insights that could substantially advance coral reef restoration are discussed below.

the transplantation and the reference (control) groups (Fig. 1b; see Table 1 for the knolls’ characteristics). A floating in situ coral-nursery (6 m depth, 14 m above seafloor), located 2.7 km northeast of Dekel Beach, was the source of the coral transplants. The nursery was situated in an area enriched with nutrients from fish farm installations, where cultured corals grew at remarkably fast rates (Bongiorni et al., 2003a,b; Shafir et al., 2006).

2. Materials and methods

We used coral colonies of two common Red Sea branching species, Stylophora pistillata (Esper, 1797) and Pocillopora damicornis (Linnaeus, 1758), which were farmed in the nursery for 8–14 months (each initiated from a 1–2 cm fragment). During November 2005, 554 nursery-farmed colonies of both species were randomly selected from nursery stocks (6–9 cm diameter; sizes did not reflect age) and prepared for transplantation by volunteers. The plastic pegs on which the corals grew were manually cleaned of fouling organisms using scrub sponges and scratching tools (Fig. 1c). If present, corallivorous snails (Drupella, Coralliophila) were removed individuality with forceps. Averaging 15 colonies/ hour per volunteer, 37 person-hours were required to prepare 554 transplants (Table 2a).

2.1. Study sites Eilat's reef (Red Sea Israel) has been deteriorating over the past decades due to rapid urban development, recreational and tourist activities and pollution (Rinkevich, 2005b). The restoration site (Dekel Beach; 29 300 N; 34 570 E), located between the navy and the commercial ports and home to a popular diving center (Fig. 1a), has been particularly affected. The shallow reef ( 0.05 for both species). Partial tissue mortality was attributed to known culprits, such as fish (Scaridae, Chaetodontidae) predation and gastropod (Drupella, Coralliophila) grazing, but in a considerable number of cases, it developed without any identifiable agent. In both species, the three experimental groups exhibited different trends of partial mortality over time (repeated-measures ANOVA, Stylophora: F6.84,47.91 = 4.578, p < 0.05; Pocillopora: F8.86,62.05 = 2.364, p < 0.05; Fig. 5a,b). Partial mortality was common in Stylophora colonies at the Dekel Beach (up to 72.9 8.3% transplants/knoll and 55.2 8.3% natal-controls/knoll), but transplants’ partial tissue loss was comparable to that of the natal controls (Fig. 5a). In contrast, partial mortality was very low at the coral-nursery


c) S. pistillata

a) S. pistillata 100

14

Transplanted knolls

*

Reference knolls

80 60 40 20

Reference knolls

10 8 6

*

4 2

0

0

b) P. damicornis

d) P. damicornis

100

Transplanted knolls

14

Transplanted knolls

Reference knolls

12

Reference knolls

80

Fish bites / colony

Colonies damaged [%]

Transplanted knolls

*

12 Fish bites / colony

Colonies damaged [%]

*

207

60 40

*

20

10 8 6

*

4

*

*

2

0

0 50

100 150

200

250 300

350 400

450 500 533

Days after transplantation

50

100 150

200

250 300

350 400

450

500 533


Fig. 4. The percentage of (a) Stylophora and (b) Pocillopora colonies damaged by fish, and the number of fish bites per each (c) Stylophora and (d) Pocillopora colony in transplanted and natal control colonies. Mean SE. In each panel, a monthly one-way ANOVA was performed. Asterisks denote statistically significant monthly groups (p < 0.05 after Bonferroni adjustment).

(maximum of 8.8 2.9% colonies/frame). The percentage of Pocillopora colonies that exhibited partial mortality did not differ significantly between the three experimental groups during most of the observed period (Fig. 5b). Interspecies comparisons revealed less partial mortality in natal Pocillopora colonies compared to Stylophora colonies (a maximum of 35 4.5% transplants/knoll and 49.7 11.4% controlcolonies/knoll vs. maximum of 72.9 8.3% transplants/knoll and 55.2 8.3% control-colonies/knoll, respectively; Fig. 5a,b). In contrast, more Pocillopora colonies exhibited partial mortality at the nursery than Stylophora colonies (a maximum of 28 2.3% Pocillopora/tray vs. a maximum of 8.8 2.9% Stylophora/tray). Considering the magnitude of tissue loss (i.e. the proportion of bare skeleton due to tissue loss within a colony), the Stylophora transplants showed higher levels of tissue loss/colony than the natal and nursery controls (a maximum of 38.0 8.4%/ transplant vs. a maximum of 17.5 4.0%/natal-control and 2.3 1.6%/nursery-control; Fig. 5c). This contradicted the Pocillopora tissue loss/colony levels, which were mostly comparable among the three experimental groups, not exceeding 13.7 7.4%/ colony (Fig. 5d). Fish preyed on Stylophora and Pocillopora transplants during the 17-month monitoring period and the damage to the corals varied with time for both species (repeated-measures ANOVA, Stylophora: F3.33,30 = 8.198, p < 0.001; Pocillopora: F2.05,18.49 = 7.005, p = 0.005; Fig. 4a,b). Following the massive fish feeding on Stylophora transplants during the acclimatization period, the affected colonies as well as the bites/colony ratios decreased thereafter to the natal

controls’ levels (17.5 8.2% to 90.8 3.6% harmed transplants/ knoll vs. 11.1 5.7% to 65.4 9.6% damaged control colonies/knoll, Fig. 4a; 0.78 0.3 to 11.4 2 bites/transplant vs. 0.5 0.2 to 4.7 3.7 bites/control, Fig. 4c). Nevertheless, although all Stylophora natal controls (100%) and the majority of the Stylophora transplants (97.4 1.6) experienced at least one fish attack during these 17 months, most (94.9 2.5%) transplants had already suffered fish attacks in the first two months following transplantation, a significant difference from the natal controls (repeatedmeasures ANOVA, F1.88,16.91 = 10.654, p = 0.001; Fig. 6a). During this period, the amount of attacked Pocillopora transplants and the amount of attacked natal colonies varied in a similar way (repeated-measures ANOVA, F2.05,18.49 = 2.346, p = 0.123), and, like the number of recorded bites/colony, was comparable throughout most of the surveys (fluctuating between 4.0 1.0% and 17.1 6.0% damaged-transplants/knoll vs. 0% and 46.1 10.3% damagedcontrols/knoll, Fig. 4b; 1.2 0.5 to 4.1 1.3 bites/transplant vs. 0 to 4.6 1.9 bites/natal-control, Fig. 4d). A gradual increase in fish assaults was documented in transplanted and natal colonies over time (repeated-measures ANOVA, F1.58,14.19 = 2.806, p = 0.103), although the percentage of natal controls attacked was eventually higher (78.1 11.8% of natal-colonies vs. 52.5 7.7% of transplants after 17 months; Fig. 6b). Examination of both species' natal groups revealed that the number of colonies injured by fish peaked in springtime (Fig. 4a,b). Most damaged corals underwent regeneration processes and regained colonial spatial complexity (Fig. 3e,f). Mortality was not linked to fish predation, as damaged colonies did not die.

208


a) S. pistillata

50

Transplanted knolls Reference knolls on site

80

a

a

Control trays at nursery

a a

a

60

a

a

a

a

a

a

a

a

b

aa

b

40

b

a

b

20 b

b

c

c

0

c

b

b

b

b

Tissue loss / colony [%]

Partial colonies mortality [%]

60 a

40 a

a c

a

bb

a

a a

a ab

b

20 10

b b

a

b

b

b

a a a a b b b b b

b b b b

bb

b

b

b

b

b

b

b


40


30 20 a

10

a

b

b

200

ab

ab

250 300

350 400

450 500 533

b

b

0

0 100 150

a

a


30

50


50

a a

a

d) P. damicornis

Transplanted knolls

20

40

0

Reference knolls on site 80


c

b) P. damicornis 100

Tissue loss / colony [%]

Partial colonies mortality [%]

100

c) S. pistillata

50

100 150

200

250 300

350 400

450 500 533



Fig. 5. The percentage of (a) Stylophora and (b) Pocillopora colonies suffering from partial tissue death, and the average magnitude of tissue loss due to partial mortality recorded in transplants, natal controls colonies and nursery controls per colony, for both the (c) Stylophora and (d) Pocillopora colonies. Mean SE. In each panel, a monthly one-way ANOVA was performed. Letters denote statistically significant monthly groups (Bonferroni multiple comparison post-hoc, p < 0.05).

3.3. Zooxanthellae densities and chlorophyll concentrations

a

S. pistillata [%]

100 90

After 16 months in the reef, the Stylophora transplants had lower numbers of zooxanthellae (22.0 3.3 103 mm2; Fig. 7) than the nursery controls (36.0 5.2 103 mm2; Fig. 7). No significant difference was found in the total chlorophyll (a + c) / zooxanthella cell between nursery controls (8.8 1.3 106 mg/ cell) and transplants (8.6 1.3 106 mg/cell; Fig. 7).

80 70 60 50 40 30 20

Transplanted knolls

10 0

Reference knolls

b

P. damicornis [%]

100 90 80 70 60 50 40 30 20

Transplanted knolls

10 0

Reference knolls

50

100

150

200

250

300

350

400

450

500 533

3.4. Coral growth Stylophora and Pocillopora colonies showed a comparable net increase in weight (around a 1.8 fold increase), height (1.3–1.5 fold) and diameter (1.3–1.5 fold) at the nursery and at Dekel Beach (onetailed t test, P > 0.05 for all parameters; Table 3). After 18 months, the net ecological volume increased, on average, by 3.3 fold in Stylophora colonies and by 2.5 fold in Pocillopora colonies (Fig. 8; Table 3). The computed growth rate constant (k) was comparable between both localities, between the reference and the transplant groups, and between both species, revealing an average k of 0.17% day1 and 0.20% day1 at the nursery and at the reef, respectively, for Stylophora colonies, and an average k of 0.17% day1 and 0.14% day1 at the nursery and at the reef, respectively, for Pocillopora colonies (test for equality between 2 percentages, p > 0.05 for both comparisons). 3.5. Coral dwelling invertebrates

Days after transplantation Fig. 6. The acumulated percentage of (a) Stylophora and (b) Pocillopora colonies that were damaged by fish. Mean SE.

Settlement of obligate associates in transplants of both species had started shortly following transplantation and continued


209

Transplanted colonies

one-tailed t test, t6=2.202, p=0.003

two-tailed t test, t6=0.122, p=0.907

1.2

45 40

1.0

35

0. 8

30 25

0. 6

20

0. 4

15 10

0. 2

5

0

0 [Chlorophyll (a+c)] / zooxanthella cell

Zooxanthellae cells / mm2 (x103)

μg Chlorophyll / algal cell (x10-5)

Control colonies at the coral nursery

Zooxanthellae cells / surface area

Fig. 7. Average chlorophyll (a + c) concentrations and zooxanthellae numbers (SE) for both the transplanted Stylophora colony and the control nursery colony, 16 months after transplantation. t test scores are indicated.

during the 533 day observation period. Overall, more Pocillopora transplants were colonized by coral-associated invertebrates than Stylophora transplants, displaying higher numbers of specimen/ colony (Fig. 9a–d). Transplants inhabiting Trapezia crabs increased linearly over time, from 4.9 2.3% to 31.8 6.2% in Stylophora transplants and from 68.3 6.2% to 92.8 3.5% in Pocillopora (Fig. 9a,b). Likewise, transplants inhabiting Spirobranchus worms rose linearly from 2.0 1.5% to 19.7 3.9% in Stylophora and from 7.9 5.4% to 57.9 3.1% in Pocillopora. Alpheus shrimps were seen only on Pocillopora transplants (although spotted in natal-colonies of both coral species at Dekel Beach), and inhabited colonies increased linearly, reaching 53.7 8.4% after 17 months (Fig. 9b). Five months after transplantation (day 179), we witnessed the first settlement and metamorphosis of the boring bivalve Lithophaga lessepsiana larvae on three Stylophora and 31 Pocillopora transplants (Fig. 9a,b). In the following month, the number of infested colonies increased considerably and continued to rise. After 17 months, 21.9 5.1% of the Stylophora transplants and 90.7 2.6% of the Pocillopora transplants were infested by Lithophaga. The average number of residing invertebrates/transplant correlated strongly with time (Fig. 9c,d). After 17 months we recorded 0.6 0.3 and 1.9 0.1 Trapezia/coral colony, and 0.3 0.1 and 0.9 0.01 Spirobranchus/coral colony, for Stylophora

and Pocillopora transplants, respectively. Moreover, each of the Pocillopora transplants was home to one Alpheus shrimp (Fig. 9d). Based on the equations of best fit, the predicted time required for all Pocillopora transplants to be inhabited by Trapezia and by Spirobranchus is 1.7 and 2.4 years, respectively, 2.5 times shorter than the time period required for Stylophora transplants (4.5 and 6.2 years, respectively; Table 4). Similarly, the time required for a Trapezia pair to appear in all transplanted colonies is three times shorter in Pocillopora (1.8 years) than in Stylophora (5.75 years; Table 4). 4. Discussion Restoration initiatives that seek to address worldwide coral reef degradation are still in their infancy. This study is among the first works that focus on the transplantation phase of the marine silviculture approach. Here we explored the use of nursery-grown corals from two branching species (S. pistillata and P. damicornis) for coral transplantation, and monitored the integration of these transplants for up to 17 months, including parameters linked to coral-associated fauna and ecological engineering. The transplantation stage is cost-effective (about US$1/colony for 10,000 transplants; further reduced to US$0.19/colony in low-

Table 3 Weight and size measurements of control nursery colonies and transplanted colonies (Dekel Beach). Coral species

Group

S. pistillata Nursery controls Transplanted colonies – P. damicornis 453.3 99.7 543 1163.1 189.7 Transplanted colonies

N Day

4 3

0 543 0 543

Parameter measured

Growth rate constant (%day1)

Weight (g)

Height (mm)

Diameter (mm)

Ecological volume (cm3)

Weight

119.8 40.1 185.0 44.1 101.0 16.8 177.0 12.3

82.9 9.4 118.8 9.8 74.2 6.1 100.6 4.1

77.0 14.5 109.5 10.8 72.2 4.6 108.2 5.1

465.3 196.2 1186.8 291.3 307.8 48.9 922.5 51.3

1.8 0.2 1.5 0.1 1.5 0.2

3.4 0.8

0.17

1.8 0.2 1.4 0.1 1.5 0.1

3.2 0.6

0.20

85.2 4.5 0.17

79.9 7

1.5 0.1

Nursery 5 0 controls 1.8 0.1 198.6 22.1 109.6 5.2 5

Size augmentation (x)

0 94.2 26.4 543 175.4 66

62.7 6.3 79.3 8.7

76.9 10.4 99.8 14.1

118.2 19.7 1.3 0.1

Height

Diameter Ecological volume

2.8 0.3

114.6 6.6 346.6 133.4 753.6 327

1.8 0.3 1.3 0.1 1.3 0.1

2.3 0.4

0.14

210


Fig. 8. A nursery-grown Pocillopora colony analyzed for growth 18 months after transplantation. The pink Alizarin in the coral’s skeleton reveals the colony’s dimensions prior to transplantation (day 0). The white portions located above the Alizarin are products of growth at the restoration site.

income countries; Mbije et al., 2013), especially in light of the recorded high survivorship rates. This calculation, combined with

the nursery costs at different locations worldwide (Shaish et al., 2008; Shafir and Rinkevich, 2008; Levy et al., 2010; Mbije et al., 2010), provides a basis for estimating the total costs of restoration programs that involve the ‘gardening’ strategy, which should take into consideration the chosen site's characteristics and the targeted species. Nursery-born colonies of both species showed a high adaptability to Eilat's degraded reef conditions, despite the potential trauma involved in moving them from supportive nursery conditions into the harsh natural environment of Dekel Beach. This further attests to the efficiency of the underwater coralnursery as a practical provider of source material for reef replenishment, as opposed to direct transplantation, which is typically characterized by initial stress impacts on the transplanted corals (Yap et al., 1998; Fahy et al., 2006). Rearing corals in the nursery improved their survival/partial-mortality/growth/attachment and reduced corallivorous impacts, compared to naturally growing colonies (as shown by the nursery control groups of both species), and minimized the transplantation/acclimatization stress experienced by the transplants, as indicated by the high survivorship rates (>95%) observed during the first three-month period. Unexpectedly, during the 17 post-transplantation months, the Pocillopora nursery-‘pampered’ transplants, did not differ (parameters studied: survivorship, partial mortality, fish predation) from the natal colonies, which represented the most successful naturally-recruited genotypes that were the survivors of selection pressures and anthropogenic activities. Moreover, whereas reduced growth rates following direct transplantation is the norm

c) S. pistillata

a) S. pistillata

2.5

80

r=0.974, p