Marine Science

ICES Journal of Marine Science Advance Access published January 30, 2014

ICES Journal of

Marine Science ICES Journal of Marine Science; doi:10.1093/icesjms/fst228

Community-based, low-tech method of restoring a lost thicket of Acropora corals Dexter W. dela Cruz1†*, Ronald D. Villanueva 1, and Maria Vanessa B. Baria 1‡ 1

The Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City 1101, Philippines

*Corresponding Author: tel: +61 2 6620 3650; fax: +61 2 6620 2669; e-mail: [email protected]

Received 13 March 2013; accepted 4 December 2013.

Due to unregulated blast fishing and episodic bleaching events, the back-reef zone near Barangay Lucero in Bolinao, Pangasinan, Philippines, was reduced to a barren area of unconsolidated sand and coral rubble. Anecdotal accounts from local inhabitants, scientific reports, and examination of rubble on the substratum revealed that the area had been dominated by staghorn Acropora corals prior to degradation. With no significant signs of natural recovery, a low-tech restoration method that is both transferable to the community and cost-effective was devised and implemented. Through the help of local inhabitants, 450 fragments of two staghorn coral species (Acropora intermedia and A. pulchra) were transplanted, without using SCUBA equipment, in a total of six 4 × 4 m plots. There were two transplant density treatments: low and high, receiving 25 and 50 fragments of each coral species, respectively. Survivorship and growth of transplants, as well as the assemblage of fishes and macroinvertebrates inside the transplantation and control plots, were monitored periodically for up to 19 months. Transplant survivorship was generally high (68– 89%) at the end of the study. There was also an average of a 15-fold increase in ecological volume of the transplants (from 1784.25 + 162.75 to 26 540.765 + 4547.25 cm3). Consequently, a significantly higher number of fish and of macroinvertebrates was recorded inside the transplantation plots than in the control plots, indicating signs of restoration success with the reintroduction of the two coral species. Exhibiting significant differences in coral cover, fish biomass and abundance, high-density is more cost-effective than low-density treatment, attaining optimal effects on key reef recovery parameters. The total cost of restoring a thicket of Acropora in a sandy-rubble field using this low-tech rehabilitation method with community participation was estimated to be US$9198.40 ha21 (US$0.90 m22), and thus 60% cheaper than without community involvement. Community involvement not only reduced the cost of the restoration activity but also provided the community with a sense of ownership and responsibility for their resources, thus ensuring the long-term success of the intervention. Keywords: Acropora, Bolinao, community-based coral restoration, low-tech coral restoration, Philippines.

Introduction The advancements in coral reef restoration science and technology in the past decade have greatly improved our understanding of and strategy for effectively restoring damaged reefs. Various restoration methods have been developed in order to address the continuous decline of coral reefs worldwide (Precht, 2006). Several protocols have been recommended in order to reduce the risk associated with restoration, increase the restored reef area, and decrease the damage to the reef where the coral transplant materials were

sourced (Precht et al., 2001; Shaish et al., 2008; Edwards, 2010; Lirman et al., 2010; Mbije et al., 2010). The proper choice of restoration method is essential in order to maximize success (Edwards and Clark, 1998). Overall, the most common restoration approach for restoring reef types degraded by various anthropogenic and natural disturbances over a range of localities involves coral transplantation (Rinkevich, 2005). Understanding the underlying cause of the degradation and the current state of the reef to be restored are fundamental considerations

Present Address: †Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, Lismore, New South Wales 2480, Australia ‡ Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, 3422, Motobu, Okinawa 905 0227, Japan # International Council for the Exploration of the Sea 2014. All rights reserved. For Permissions, please email: [email protected]

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dela Cruz, D. W., Villanueva, R. D., and Baria, M. V. B. Community-based, low-tech method of restoring a lost thicket of Acropora corals. ICES Journal of Marine Science, doi.10.1093/icesjms/fst228.

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Material and methods The degraded back-reef (2 –3 m deep) off Lucero, a village on the western part of Santiago Island, Bolinao, Pangasinan, northwestern Philippines (16824’58"N 119854’26"E; Figure 1) was the restoration

Figure 1. Location of the source site for transplants (Cory) and restoration plots (Lucero) in the Bolinao – Anda Reef Complex, northwestern Philippines. site chosen. As indicated by careful scrutiny of the rubble present on the substratum, local accounts, and a scientific published report (Yap and Gomez, 1983), this area used to be dominated by staghorn corals, viz., Acropora spp. But as a consequence of blast fishing and episodic bleaching events, this back-reef had been reduced to a barren area of unconsolidated substrate—sand and coral rubble (Figure 2a). And even though blast fishing in the area had been controlled for more than a decade, the reef had not been able to recover naturally. A total of nine 4 × 4 m experimental plots were established and demarcated using bamboo stakes and monofilament line. The experimental plot size was determined in relation to the number of community participants and the duration of the transplantation activity. The plots were divided into three clusters, with three plots per cluster and a distance of at least 50 m between the clusters. In each cluster, plots were at least 5 m apart and assigned as either high-transplant-density or low-transplant-density treatment plots or control plots. Effectively, there were three replicates of each type of plot. All plots were adjacent to a small giant clam nursery being managed and protected by the villagers, which reduced the likelihood of the transplants being damaged or dislodged by fishing activities. Locals were invited to participate in the coral transplantation activity. They were villagers and barangay (village) officials at Lucero and nearby barangays, volunteer overseers of village-level marine protected areas, fishers, and representatives from the local government unit and people’s organizations. A lecture on basic coral biology and reef ecology, concepts of coral reef restoration, the activity objectives, transplantation techniques and criteria for choosing the transplant materials and restoration site was conducted prior to the transplantation to raise awareness and facilitate understanding among the participants. The lecture was delivered by the authors at the village hall and lasted for 3 h. A few days prior to the scheduled transplantation activity, fragments (of at least 25 cm) of Acropora pulchra and A. intermedia suitable for this transplantation technique were collected by the authors


in restoration (Pastorok et al., 1997). Climate change –related stressors, such as elevated seawater temperature and ocean acidification, are some of the global disturbances that can potentially cause a decline in live coral cover. During the 1998 bleaching event, it was estimated that 16% of the world’s coral reefs were severely damaged (Burke et al., 2011). At the local level, one of the most serious threats to coral reefs is destructive fishing (Burke et al., 2011) and most notably the use of dynamite explosives (Alcala and Gomez, 1987; McManus et al, 1997; Fox et al., 2003), which kill not only targeted fish species but also non-target animals (Marcus et al., 2007). Blast fishing destroys the structural complexity of the reef by shattering corals into pieces (Riegl and Luke, 1999). Some fragments will survive after the blast, but after several days or weeks most will eventually die (Fox et al., 2003). In the absence of larvae supply, reefs tend not to recover naturally (Nzali et al., 1998). In this situation, phase shift often occurs due to conditions favourable for soft coral and macroalgal colonization (Hughes, 1994; Ceccarelli et al., 2011), which inhibits the settlement of coral larvae (Birrell et al., 2008). Moreover, post-settlement mortality is high because of the movement of rubble where coral spat or juveniles are attached (Fox, 2004). Other destructive techniques related to dynamite fishing include ship grounding, coral mining, storm activity, tsunamis and large-scale bleaching of thickets of staghorn corals (Acropora spp.), often leaving an unconsolidated rubble field (Clark and Edwards, 1995; Lirman, 2000). Among the available active restoration techniques, substrate stabilization aids the recovery of damaged reefs with unconsolidated substrate. Some of the materials that have been found to be effective in consolidating loose substrates are plastic and wire mesh (Bowden-Kerby, 2001; Raymundo et al., 2007), ArmorflexTM concrete matting (Clark and Edwards, 1995), rock piles (Fox, 2004) and polythene string in grid configuration (Lindahl, 2003). However, these materials often leave unnatural or foreign materials on the reef and may also significantly increase the operational cost of the restoration. One issue in reef restoration that is currently getting much attention is the high operational cost (including materials and labour) (Spurgeon and Lindahl, 2000; Edwards, 2010). A possible way to address this is to involve the community in restoring their own reef, which would minimize the restoration cost by about 17% if the community puts in labour as their contribution (Edwards, 2010). This would also give the community a sense of ownership, responsibility and accountability for the reef resources that they heavily depend upon for their food and livelihood (Edwards et al., 2010). Considering that blast fishing is rampant in many underdeveloped or developing countries in Southeast Asia and East Africa (Baticados, 2004; Wells, 2009), there is a need for a cheap and effective restoration method for blasted reefs (Fox, 2004; Raymundo et al., 2007). In this study, a low-tech restoration method that is both transferable to the community and cost-effective was developed and implemented. Over a period of 19 months, the results of the restoration project were periodically evaluated in terms of coral, reef fish and mobile macroinvertebrate assemblage parameters. In addition, the effects of transplant density on these parameters were also assessed.

D. W. dela Cruz et al.

Community-based coral restoration

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using hammer and chisel from the donor reef beside Cory sandbar, Anda, Pangasinan (16819’38"N 120801’58"E; Figure 1), 21 km from the restoration site. Although the area has a vast thicket of staghorn corals, a hydrological study showed that it is a sink rather than a source of larvae in the Bolinao –Anda Reef Complex (BARC, unpublished data). For this reason and because of the considerable distance, natural reseeding of staghorn larvae is limited on the restoration site. To avoid collateral damage to the donor reef, less than 10% of each colony was fragmented (sensu Epstein et al., 2001). As observed on the source reef, these fast-growing staghorn corals are capable of colonizing sandy and rubble substrate. Upon removal from the source reef, the harvested fragments were placed in bins of seawater, immediately transported using a speed-boat, and temporarily laid down on a rubble area (2m deep) next to the restoration plots. During this time, calm water conditions were experienced and the coral fragments remained stable in their holding area. With the help of 30 local participants, and without SCUBA gear (Figure 2b), 450 fragments of A. pulchra and A. intermedia were transplanted. Each of the low- and high-density transplant treatment plots received 25 and 50 fragments per species respectively, with fragments within the plots being distributed haphazardly. Control plots received no transplants. Transplantation was performed by inserting the coral fragments into the sand, facilitated by boring a hole using a bamboo stake. The fragments were then secured to a 40 cm bamboo stake (driven into the substrate to half its length) with an insulated wire (Figure 2c) to prevent

dislodgement during rough water conditions. The field activity (including boat transport, transplantation and on-site discussions) lasted for 3 h. Photographs of each plot were taken using a 1 × 1 m frame (total of 16 frames per plot) and analysed using CPCe (Kohler and Gill, 2006) for benthic cover analysis. For one year, all 450 transplants were monitored for survivorship every 2 months, and additional monitoring was conducted 19 months post-transplantation. Corals were considered alive unless no living tissue was observed. For growth rates, 10 randomly selected transplants of each coral species per plot were tagged and measured at two to three month intervals till 12 months and after 19 months. The length (l ), width (w) and height (h) of each of the corals were measured with calipers, and the ecological volume (EV) was calculated following the cylindrical volume formula: EV ¼ pr 2h, where r ¼ (l + w)/4 (Levy et al., 2010). The growth rate (ecological volume change per month) was also calculated, using the formula Gr ¼ [EVf – EVi]/m, where Gr is the standardized growth rate, EVf and EVi are final and initial ecological volumes, respectively, and m is the number of months elapsed. Only the tagged corals alive at 12 months and 19 months post-transplantation were included in the growth rate determination. The coral-associated macroinvertebrates (viz. Coralliophila spp., Cronia spp., Drupella spp., Holothuria spp., Trochus spp. and Vasum spp.) found in each plot were recorded through visual surveys before transplantation as well as after 12 and 19 months. Fish visual censuses (5-min duration) within each plot were also conducted


Figure 2. (a) Unconsolidated rubble field at the restoration site. (b) A participant from the village transplanting Acropora. (c) Newly transplanted Acropora fragments on an experimental plot. Note the bamboo stake used to secure the newly transplanted corals (with insulated wire). (d) Thicket of transplanted Acropora after 19 months; blue-tipped coral colonies are A. intermedia, brown colonies are A. pulchra.

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Results A benthic survey of experimental plots before the transplantation activity revealed a high cover of abiotic benthic categories, comprised of 47.04 + 7.89% (mean + s.d.) rubble and 46.61 + 5.05% sand. The remaining components were generally made up of a small percentage of macroalgae, mainly Sargassum spp. (6.35 + 2.94%). Coral cover was nil in all plots. However, a total of 12 natural coral recruits (,5 cm in diameter) attached to loose rubble were found inside the nine plots, consisting of Montipora digitata (n ¼ 5), Porites lutea (n ¼ 3), Pocillopora damicornis (n ¼ 3) and Pavona sp. (n ¼ 1). Immediately after the transplantation, coral cover in both low- and high-density plots significantly increased to 3.76 + 0.63% and 12.11 + 1.92%, respectively (ANOVA: F ¼ 108.56, p ¼ 0.0005; F ¼ 119.51, p ¼ 0.0004). After 19 months, coral cover in low- and high-density plots was 23.97 + 11.56% and 54.06 + 9.48%, respectively, while that in the control plots was 2.51 + 1.67%, attributable to non-transplant species (viz. Montipora digitata), which recruited either naturally or were dislodged fragments/colonies from adjacent areas. RM-ANOVA revealed significant variations in coral cover over time (F ¼ 28.20, p ¼ 0.0001) and between treatments (F ¼ 22.58, p ¼ 0.003; high density . low density . control). Transplant survivorship was generally high (68–89%) after 19 months. An abrupt decline in transplant survivorship was recorded 12 months post-transplantation due to the observed infestation of muricid snails (Drupella sp.) that happened 10 months after transplantation. Followed by the demise of corals in the affected plots, the muricid snails died, possibly due to starvation. Survival analysis

Figure 3. Kaplan– Meier survival curves of transplants. (a) Survivorship of combined A. intermedia and A. pulchra in each density treatment. (b) Survivorship of the two coral species with both density treatments combined. revealed no significant difference between density treatments (logrank test, x2 ¼ 1.48, p ¼ 0.14; Figure 3a). However, A. pulchra survived significantly better than A. intermedia, regardless of density (logrank test, x2 ¼ 2 3.29, p ¼ 0.01; Figure 3b). At 19 months the coral transplants in both high- and low-density plots had significantly grown from an initial ecological volume of 1918.09 + 172.50 to 30 875.88 + 3373.00 cm3 and from 1650.40 + 153.00 to 22 205.65 + 5721.50 cm3, respectively (F ¼ 76.06, p ¼ 0.0001; F ¼ 60.07, p ¼ 0.0002, respectively; Figure 4). RM-ANOVA also revealed significant differences in transplant ecological volume between density treatments (F ¼ 7.45, p ¼ 0.03; high density . low density) and transplant species (F ¼ 7.04, p ¼ 0.03; A. pulchra . A. intermedia). The average growth rates of A. pulchra and A. intermedia were 1333.20 + 222.77 and 934.20 + 77.55 cm3 month21 respectively (Figure 5), within a 19-month period. The growth rate of transplants in the high-density treatment was significantly higher than in the low-density treatment plots (Tukey test, a ¼ 0.05), while A. pulchra had a significantly higher growth rate than A. intermedia in both densities (Tukey test, a ¼ 0.05). Before transplantation, fish abundance, species richness and biomass did not differ significantly among the two treatment levels and the control (F ¼ 2.30, p ¼ 0.18; F ¼ 3.27, p ¼ 0.11; F ¼ 1.96, p ¼ 0.22; respectively; Figure 6). Overall, the fish composition did not differ significantly between the treatment plots (Figure 7a; ANOSIM, R: 0.09, p ¼ 0.28).


before the transplantation and again after 7, 12 and 19 months. Census data (Appendix A) were used to generate fish abundance, species richness and biomass. The latter was calculated using length –weight relationship constants per species obtained from FishBase (Froese and Pauly, 2012). All monitoring of the parameters was performed by the authors. Transplant survivorship were compared between species and density treatments using survival analysis, a non-parametric pairwise comparison test based on the Kaplan –Meier function (Lee, 1992). Transplants that had been alive at the last monitoring period, then been detached and died from a confirmed cyanide fishing incident, were scored as censored observations in the analysis. Variations in growth rate were examined using two-way ANOVA, with transplant density and species as the independent variables. Changes in coral cover, transplant ecological volume, fish abundance, richness and biomass, and macroinvertebrate abundance and richness through time were analysed using repeated measures ANOVA (RM-ANOVA). To determine the effect of transplant density on these parameters at different monitoring times, one-way ANOVA was performed, with the Tukey test for post hoc comparisons. Furthermore, the variability in the assemblage of fish and macroinvertebrates among transplant treatment plots before the experimental restoration and 19 months thereafter was examined graphically in a non-metric multidimensional scaling (MDS) ordination plot using the Bray – Curtis similarity index, with the use of PAST version 1.93 (Hammer et al., 2001). An analysis of similarities (ANOSIM) was performed to test significant differences between treatments. The cost of the restoration activity was estimated following the computation of Edwards (2010). Using this estimate, costs per transplant and per unit area (ha) were calculated.



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Figure 4. Ecological volume (mean + s.d.; n ¼ 3) of Acropora intermedia and A. pulchra transplants in low- (L) and high-density (H) plots. Corals were transplanted in July 2010.


Figure 5. Mean growth rates (n ¼ 3) of A. intermedia and A. pulchra transplants in low- and high-density plots as determined 12 months post-transplantation. Error bars represent standard deviation. After 19 months, fish abundance in the high-density transplant plots was 50% higher compared with the low-density and control plots (high density . low density ¼ control, Tukey test, a ¼ 0.05; Figure 6a). Coincidently, fish species richness in plots with lowand high-density transplants was significantly higher than in the controls (Tukey test, a ¼ 0.05), though there was no significant difference between the two density levels (F ¼ 4.11, p ¼ 0.14; Figure 6b). The fish composition remained similar between treatment plots (Figure 7b; ANOSIM, R: 0.19, p ¼ 0.15). On the other hand, fish biomass emerged to be significantly higher in the high-density plots than in the low-density and control plots at 19 months posttransplantation (Tukey test, a ¼ 0.05; Figure 6c). Over time, a significant variation in all fish parameters (abundance, richness and biomass) was recorded (RM-ANOVA, F ¼ 15.75, p ¼ 0.0001, F ¼ 17.02, p ¼ 0.0001, F ¼ 7.75, p ¼ 0.0001, respectively). Macroinvertebrate abundance and species richness did not differ significantly among treatments and control before transplantation (F ¼ 0.29, p ¼ 0.76; F ¼ 0.05, p ¼ 0.95, respectively; Figure 8). Multivariate analysis detected no significant difference in macroinvertebrate composition among treatment plots at this time (Figure 9a; ANOSIM, R: 20.07, p ¼ 0.58). However, after 12 months macroinvertebrate abundance emerged to be higher in the high- and low-density compared with the control plots (Tukey test, a ¼ 0.05; Figure 8a). At the end of the experiment, no significant difference in species richness was recorded between treatments (F ¼ 0.19, p ¼ 0.83; Figure 8b), though abundance was still significantly higher in the high- and low-density plots compared with the control plots (high ¼ low . control; Tukey test, a ¼ 0.05). Also, no

Figure 6. Fish abundance (a), species richness (b), and biomass (c) in high- and low-density transplant plots and control plots (n ¼ 3). Error bars represent standard deviation. The July 2010 monitoring was conducted just before transplantation. significant difference in macroinvertebrate composition was found during this monitoring time (Figure 9b; ANOSIM, R: 0.16, p ¼ 0.21). There was, however, a significant variation in macroinvertebrate

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Figure 7. Non-metric multidimensional scaling (nMDS) ordination of the reef fish assemblage in different transplant treatment plots: high-density (cross), low-density (open circle), and control (open square) before transplantation in July 2010 (a), and at the end of experimental observation in February 2012 (b).

abundance and species richness through time, as detected by RM-ANOVA (F ¼ 84.61, p ¼ 0.0001; F ¼ 55.11, p ¼ 0.0004, respectively). The total cost of this community-based coral restoration (for high-density treatment comprising of 62 500 fragments ha21) was calculated to be US$9198.40 ha21 (US$0.90 m22) or US$0.15 per coral transplant (Table 1). The total cost is almost 60% cheaper than the intervention without community participation (US$22 839.74 ha21, Table 1). The bulk of this amount was mainly spent on hired labour and boat rentals that were free in this communitybased coral restoration project, in which personal boats and snorkelling gear owned by the volunteer participants were deployed.

Discussion The coral reefs of Bolinao, Philippines are an important fishing ground that directly supports more than 70 000 fisher folk (Ahmed et al., 2007). The reefs did not recover naturally from episodic


Figure 8. Macroinvertebrate abundance (a), and species richness (b) in high- and low-density transplant plots and control plots (n ¼ 3). Error bars represent standard deviation. The July 2010 monitoring was conducted just before transplantation.

disturbances (e.g. blast fishing and elevated temperature during el Ninõ events) experienced since the mid 1980s (McManus et al., 1997). A good example of a degraded reef in this area is the back-reef off Lucero, where extensive thickets of Acropora corals, particularly of A. pulchra, used to dominate, but not a single staghorn coral colony could be found there before the intervention implemented in this study. This community-based restoration project demonstrates that a degraded coral reef with an unstable substrate can be repopulated with staghorn corals through a low-tech coral transplantation technique and without initial substrate stabilization. The results of this study are promising and resource managers, conservationists and coastal community organizations are encouraged to apply the same method in damaged reefs with similar conditions. The physical restoration of blasted reefs through substrate stabilization is supposed to be the preliminary intervention prior to coral transplantation. Though expensive, this intervention is necessary to jumpstart the recovery process in high wave energy reef areas. However, for low wave energy reef areas like the back-reef and lagoonal environments, substrate stabilization is not necessary. In these cases, the suitability of substrate for the recovery process to occur naturally through initial coral recruitment and assisted by coral transplantation, is the prime consideration. The coral community that was restored in this study is unique as the habitat is of sandy-rubbly substrate. Staghorn Acropora corals that comprise such a community may have colonized the area through dislodgement of large fragments or whole colonies. These dislodged corals then grow and anchor themselves by burying basal colony portions into the substrate and spreading to form thickets. Consequently, any intervention to restore lost Acropora thickets should incorporate this colonization strategy, as demonstrated in this study. Success in any restoration work done is also due to sound choice of the coral species involved in the transplantation. In this instance, a published account of the coral species (particularly A. pulchra, see Yap and Gomez, 1983) in the damaged reef provided the lead in this study in terms of the identity of the corals chosen to populate the area. Additional means that helped determine the species of corals that were used to populate the damaged reef included the morphological and taxonomic examination of the rubble in the area and eyewitness information from local inhabitants. The other coral species transplanted to the project area (viz. A. intermedia) was chosen as it was earlier observed to be tolerant of bleaching during elevated temperature events in the study site (E. D. Gomez,

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Figure 9. Non-metric multidimensional scaling (nMDS) ordination of the macroinvertebrate assemblage in different transplant treatment plots: high-density (cross), low-density (open circle), and control (open square) before transplantation in July 2010 (a), and at the end of experimental observation in February 2012 (b).

With Community Participation Activity I. Collection of fragments A. Materials

B. Boat

C. Labour II. Transplantation A. Materials

B. Boat

C. Labour

Without Community Participation

Item

Chisel Hammer Cutter Plastic drum Snorkelling gear rental SUBTOTAL Rental Gasoline SUBTOTAL Hired labour SUBTOTAL Bamboo stakes Insulated wire Snorkelling gear rental SUBTOTAL Rental Gasoline SUBTOTAL Hired labour SUBTOTAL TOTAL

Unit cost

Quantity

Total cost

3 4 3.5 12.2 0

20 pcs 20 pcs 20 pcs 80 pcs 20 sets × 7 d

60 80 70 976 0 1 186.00 0 512.4 512.4 0 0

0 1.22

2 big boats × 7 d 60 la × 7 d

0

20 persons × 7 d

0.05 0.07 0

62 500 pcs 62 500 pcs 60 sets × 7 d

0 0

10 small boats × 7 d 0

0

60 persons × 7 d

3 125.00 4 375.00 0 7 500.00 0 0 0 0 0 9 198.40

Unit cost 3 4 4 12 7.32 121.95 1.22 13

Quantity 20 pcs 20 pcs 20 pcs 80 pcs 20 sets × 7 d 2 big boats × 7 d 60 la × 7 d 20 persons × 7 d

0.05 0.07 7.32

62 500 pcs 62 500 pcs 60 sets × 7 d

7.32 1.22

10 small boats × 7 d 5 lb × 7 d

13

60 persons × 7 d

Total cost 60 80 70 976 1 024.80 2 210.80 1 707.30 512.4 2 219.70 1 820.00 1 820.00 3 125.00 4 375.00 3 074.40 10 574.40 512.14 42.7 554.84 5 460.00 5 460.00 22 839.74

The distance between the source reef and restoration site is 20 km. bThe distance between the shore (village) and restoration site is 0.5 km

a

personal observation) as well as being part of the thicket assemblage in the source site. The results show that this species exhibited lower survivorship than A. pulchra, signifying the importance of identifying the right species of coral in the site prior to disturbance and incorporating it in the restorative intervention. Staghorn and other branching corals are ideal transplant materials specifically for community-based coral transplantation projects as they can be collected and transplanted easily in shallow reef areas, even without the use of SCUBA. The unique topographic and geographic profile of the restoration area (i.e. near the shore, shallow, sandy-rubbly substrate and sheltered habitat) facilitated the logistic feasibility of this low-cost transplantation technique, which suited

the local villagers who were able to reach the restoration site from the shore using simple bamboo rafts. Using their improvised masks and fins (made of wood), a local participant can transplant 20 –30 fragments per hour (without SCUBA equipment). In addition, locally available materials such as bamboo stakes were utilized to effectively prevent the corals from being dislodged during occasional typhoons and monsoonal winds by providing an additional anchor for the transplant. Experience has shown that unattached coral fragments may tumble around, causing abrasion and death (Bowden-Kerby, 2001), whereas there were no missing or drifting fragments found outside the plots in this project. The wire used to tie the corals to the bamboo stake was encrusted with living coral


Table 1. Cost estimates of restoration intervention for high-density treatment (62 500 fragments in one hectare) with and without community participation. All amounts are in US dollars.

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of the expenses is usually attributed to the materials used to consolidate the rubble field and to enhance topographic complexity, such as TM the use of Reefballs and ceramic stoneware modules. In this experiment, where no substrate stabilization was performed and some cost streams were in-kind contributions from the local community, the total cost of restoring a thicket of Acropora corals that had crumbled to rubble and sand was estimated to be US$9198.40 ha21 (US$0.90 m22). Involving the local community has also been found to be effective in other conservation and restoration disciplines such as sea cucumber ranching, sea urchin restocking, and the establishment and management of marine protected areas (Ferrer et al., 1996; Men˜ez et al., 1998; Russ and Alcala, 1999; Men˜ez et al., 2012). However, no study has yet demonstrated that community-participated coral restoration activities can work and have practical advantages. Community involvement not only reduces the cost of the restoration intervention itself, but it may also ensure long-term success, as the activity will provide the community with a sense of ownership and responsibility. Additionally, training in the basics of coral biology and the rationale of restoration allows the community to understand the importance of taking care of their resources (Russ and Alcala, 1999). This in turn may then encourage and inspire them to take the initiative to look after the site and carry out activities that will protect their work. As an immediate benefit, they may also showcase their restoration sites to tourists, an additional benefit that could develop into an alternative livelihood (Cadiz and Calumpong, 2000). In conclusion, rehabilitation intervention is likely to succeed when reef-users are involved (as also observed in related studies, e.g. Men˜ez et al., 1998, 2012) and when it is affordable and cost-effective for the community.

Acknowledgements We thank the villagers of Barangay Lucero, people’s organizations and the local government unit of the Municipality of Bolinao, Pangasinan, and all participants in this community-based coral restoration project. We deeply appreciate the help and support of M. Ponce, F. Castrence Jr., R. de Guzman, C. Angelito, S. DeMars, R. Dizon, H. T. Yap and E. Gomez. We thank Gabriele Conrad for the language check in the final version of the manuscript. This is MSI Contribution No. 423.

Funding We thank the Australian Centre of International Agricultural Research for financial assistance during the preparation of the manuscript. This study was funded by the Philippines’ Department of Science and Technology through the Philippine Council for Agriculture, Aquatic and Natural Resources Research and Development.

References Ahmed, M., Umali, G. M., Chong, C. K., Rull, M. F., and Garcia, M. C. 2007. Valuing recreational and conservation benefits of coral reefs – the case of Bolinao, Philippines. Ocean and Coastal Management, 50: 103– 115. Alcala, A. C., and Gomez, E. D. 1987. Dynamiting coral reefs for fish: a resource-destructive fishing method. In Human Impacts on Coral Reefs: Facts and Recommendations, pp. 52 – 60. Ed. by B. Salvat. National Museum of Natural History, Moorea, French Polynesia. 253 pp. Baticados, D. B. 2004. Fishing cooperatives’ participation in managing nearshore resources: the case in Capiz, central Philippines. Fisheries Research, 67: 81– 91.


tissue a few months after transplantation, and whilst the stakes disintegrated after 1 year, the fragments were at that point large and dense enough for self-anchorage. Though competition for space and light is expected among coral transplants (Sleeman et al., 2005), spacing seems to have had no effect on transplant survivorship in this study. A significant difference between high- and low-density treatments was, however, found for transplant growth (ecological volume). The higher transplant growth for high-density treatment may have been due to enhanced localized conditions (e.g. water flow and fish/macroinvertebrate assemblage maintaining coral health). However, density dependence of transplant growth may be experienced during the initial stages of community development only, as the amount of free space will decrease with accumulating growth (Tanner et al., 2009). Both survivorship and growth of transplanted corals were promising, though A. pulchra, the original species occurring on the restoration site, was performing better than A. intermedia, regardless of density. High survivorship was evident after more than 1.5 years, overcoming all seasonal stressors, which demonstrates that the proper choice of species with respect to the restoration site will clearly reduce the chance of intervention failure. However, even previously non-occurring but associated and identical species may also display high survivorship (but relatively lower than that of the formerly occurring species), as demonstrated in this instance by A. intermedia. The high survival rates may also be attributed to the large size of fragments used in transplantation (Highsmith, 1982; Bowden-Kerby, 2001). Coral patches created through transplantation have been reported to increase fish abundance (Lindahl et al., 2001). Immediately after transplantation, a number of fish and macroinvertebrate taxa colonized the plots, and this number increased significantly as the transplanted corals continued to increase in size. The fluctuation in the number of fish and macroinvertebrates inside the plots may also be attributed to the seasonal recruitment cycle. The spillover effect was shown in the control plots, as the number of fishes and macroinvertebrates was also significantly higher there a year later (during the same monitoring month), and considering the short distance to the treatment plots. Determining the appropriate density of transplants in coral restoration is as important as selecting the suitable method and coral species to be used (Muko and Iwasa, 2011). Generally, these factors will also determine the total cost of rehabilitation intervention (from days of collecting and transplanting the corals, as well as manpower needed; Gomez et al., 2011). The results of this study suggest that high-density (six fragments m22) is more costeffective than low-density (three fragments m22) treatment, with significant differences in coral cover and fish (biomass and abundance). This suggests that a certain coral density threshold is needed in order to effectively attract other biota into the restored reef. It needs to be remembered that the central goal of coral transplantation is not only to establish a viable and persistent coral community but also to enhance other benthic organisms and fish assemblages (Jaap, 2000; Cabaitan et al., 2008). Therefore, for the purpose of cost-effectiveness, determining the lowest density possible that has maximal effects on key reef recovery parameters (i.e. fish and macroinvertebrates) is recommended. The restoration approach applied in this study is relatively cheap compared with previously used methodologies to restore reefs with unstable substrates (i.e. impacted by blast fishing and ship grounding), which cost from US$5 –10 000 m22 (Fox et al., 2005). The bulk



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Handling editor: Mitsutaku Makino

Family Apogonidae Apogonidae Apogonidae Blenniidae Bothidae Bothidae Carangidae Chaetodontidae Chaetodontidae Chaetodontidae Chaetodontidae Chaetodontidae Fistularidae Gobiidae Gobiidae Gobiidae Gobiidae Labridae Labridae Labridae Labridae Labridae Labridae Labridae Labridae Labridae Lethrinidae Monacanthidae

Species Apogon compressus Apogon hartzfeldii Cheilodipterus quinquelineatus Salarias obscurus Bothus pantherinus Pardachirus pavoninus Caranx sp. Chaetodon auriga Chaetodon kleinii Chaetodon lunulatus Chaetodon octofasciatus Heniochus chrysostomus Fistularia commersoni Amblygobius phalaena Ctenogobiops sp. Istigobius decoratus Valenciennea strigata Cheilinus chlorourus Choerodon anchorago Coris batuensis Halichoeres melanurus Halichoeres scapularis Halichoeres trimaculatus Oxycheilinus bimaculatus Stethojulis strigiventer Thalassoma lunare Lethrinus harak Acreichthys tomentosus Continued

Appendix A Continued Family Mullidae Mullidae Mullidae Mullidae Mullidae Nemipteridae Nemipteridae Nemipteridae Nemipteridae Pinguipedidae Pomacentridae Pomacentridae Pomacentridae Pomacentridae Pomacentridae Scaridae Scaridae Scorpaenidae Scorpaenidae Serranidae Serranidae Siganidae Siganidae Siganidae Syngnathidae Synodontidae Tetraodontidae Tetraodontidae Tetraodontidae Tetraodontidae

Species Mulloidichthys flavolineatus Parupeneus barberinus Parupeneus multifasciatus Parupeneus pleurostigma Upeneus tragula Scolopsis bilineatus Scolopsis ciliatus Scolopsis lineatus Scolopsis temporalis Parapercis cylindrica Dascyllus aruanus Dascyllus melanurus Dascyllus reticulatus Dascyllus trimaculatus Pomacentrus adelus Chlorurus sordidus Scarus globiceps Dendrochirus zebra Synanceia horrida Epinephelus maculatus Epinephelus merra Siganus fuscescens Siganus spinus Siganus virgatus Corythoichthys intestinalis Synodus variegatus Arothron manilensis Canthigaster amboinensis Canthigaster compressa Canthigaster rivulata


Appendix A Inventory of coral reef associated fishes monitored inside the experimental plots during the entire experiment. The 59 species belong to 21 families.