Deep-Sea Research II 96 (2013) 50–55

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Deep-Sea Research II

0967-06http://d

n CorrE-m

journal homepage: www.elsevier.com/locate/dsr2

Coral degradation and ability of rehabilitation of coral reefsin Co To Archipelago, Quang Ninh province, Vietnam

Nguyen Dang Ngai n, Nguyen Duc Cu, Dao Anh TuyetInstitute of Marine Environment and Resources (IMER), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet Str., Cau Giay Distr., Hanoi,Viet Nam

a r t i c l e i n f o

Available online 25 April 2013

Keywords:Coral degradationRecoveryGrowth rateTransplant

45/$ - see front matter & 2013 Elsevier Ltd. Ax.doi.org/10.1016/j.dsr2.2013.04.017

esponding author.ail addresses: ngaind@imer.ac.vn, ngaind@yah

a b s t r a c t

Serious degradation of coral reefs in the Co To Archipelago occurred from 2002 to 2006. Nearly 80% ofthe species and over 90% of living coral cover were lost and some reefs were completely dead. Currently,the highest coral cover is only 7.5% where previously most of the reefs had over 50% live coral cover. Thecause of the reef degradation has been identified to be residues of cyanide used by local fishermen forfishing on reefs. To overcome the consequences transplantation corals on natural and artificial shelterswere attempted. Survival rate on artificial shelters was 88.3% after 2 years and growth rate averaged2.3 cm/year. Transplanted corals on natural shelters had lower survival rate, 55.9%. The natural recoveryof coral on degraded reefs was also monitored periodically in this study. No coral recruitment was seenon completely dead reefs whereas there was little new coral recruitment on reefs with some remaininglive corals.

& 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Serious degradation has been observed on many coral reefsworldwide. For more than a decade area, coverage and number ofspecies have been reduced (McClanahan, 2002; Wilkinson, 2004,2008; Lough and Van Oppen, 2009). Many causes for this declinehave been described from different regions, e.g. increasing seawatertemperature (Anthony et al., 2007), sedimentation (Hernandez et al.,2009), freshwater runoff (Tuan et al., 2008), dynamite fishing(McManus et al., 1997). Following these phenomena some reefs canself-recover (Hughes et al., 2010; Sheppard et al., 2008; Halford et al.,2004) some need help from artificial restoration and others wereunable to restore because substrate or environment was not suitablefor coral growth (Fabricius, 2005; Scheffer et al., 2001, Hughes, 1994,Hughes et al., 2010). Application of transplanting on artificial andnatural shelters for coral restoration has been successful in manyareas of the world (Clark and Edwards, 1994; Rinkevich, 2005; Quanand Ngai, 2008). The restoration methods included: physical, biolo-gical, and dual restoration (combination of biological and physicalrestoration) (Job et al., 2003). Depending on the specific conditions ofeach area the most suitable methods for rehabilitation may bechosen. The most widely used methods are the reefball and naturalshelters (Rinkevich, 2000).

Almost all coral reefs in Co To Islands died between 2002 and2006. In recent years, though the water seems clean, the bottomsubstrate is dead coral rock and sand and very little coral has

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oo.com (N.D. Ngai).

recruited here. The purpose of this study was to examine thenatural recovery of coral on degraded reefs and carry out experi-ments to test for survival and growth rate of corals on natural andartificial shelters in order to develop a management plan foreffective protection and restoration of coral reefs.

2. Research methods

2.1. Study area

Co To Archipelago belongs to Quang Ninh province, in northernVietnam, about 50 km from the mainland (20156′00″–21104′00″Nand 107144′00″–107152′00″E), with more than 15 islands. The totalarea of Co To Islands is 46.2 km². A population of 5195 people (in2006) live mainly on capture fishery and agriculture. This area hasfavorable natural conditions for reef development such as: warm andclear water, high salinity, hard substrate. Therefore, coral ecosystemsare developed with over 100 species of hard corals, high coverageand the biggest reef in northern Vietnam. The Islands have highbiodiversity including many valuable and commercial species forexample reef fishes, abalone, sea cucumber, pearl oyster. Additionallythis area is an important fishing ground and seed is dispersed tonearby coastal areas (WWF, 1994). Therefore, Co To Islands have beenconsidered for a list of 15 marine protected areas in Vietnam.

2.2. Method of determining the status and degradation of coral

The overall status of coral reefs in the Co To was surveyed byusing a small boat pulling the observer on the water surface above

N.D. Ngai et al. / Deep-Sea Research II 96 (2013) 50–55 51

the reefs to observe and record the data on living coral, dead coral,soft coral and macro-benthos (English et al., 1997) and then selectsites to beused for specific survey by point transect method to getdata on each component of substrate, coral fishes and otherbenthic communities (Hodgson et al., 2004). During the surveywe focused on the status of coral death and the cause of death.

−

TabWa(Sou

P

pDTCBCANNP

Local fishermen were internviewed to find out the cause ofdeath of corals in this area. Questionnaires focused on produc-tion, the target species of exploitation, exploitation methods,fishing gears, etc.

−

The environmental parameters were periodically monitored atthree study sites (Trau Khe, Thanh Mai, Dang Van Chau) in 2008,2009 and 2010. Each year the three sites were monitored for threedays. Measurement directly and samples for analysis werecollected at the surface and bottom 6 times/24 h. Field parameterssuch as salinity were measured by refractometer, temperatureand DO was measured by a DO meter, pH was measured by pHmeter OKATON, transparency was measured by secchi disk. Thesamples for nutrient, cyanide, pesticide and other water qualitymeasurements were collected at each site at both surface andbottom layer, fixed by suitable chemicals and analyzed in thelaboratory. In order to assess status of water environmentalquality, measurements were compared to promulgated standardsof Vietnam and Asian countries (Table 1).

2.3. Method of monitoring the natural recovery

−

Growth of natural corals was monitored by attaching labels onseveral colonies and measures them periodically. A total of 12coral colonies were marked and measured one time a year byfiberglass ruler over colony at each site from 2008 to 2010.

−

The recruitment of coral juveniles was monitored and observedon transect lines with length of 20 m at 5 reefs (Fig. 1), observingand counting the number of small coral colonies, less than 5 cmof coral, within 2.5 m on each side of the transect. The reefs wereselected for monitoring at different places (in and outside Co Tobay, on reefs with living coral and without living coral).

2.4. Transplanting coral

Two types of shelters were applied for transplanting corals

−

Concrete reefballs (Reef Ball Foundation, 2008; Precht, 2006)were designed for transplanting coral colonies with measure-ments: 1 m in diameter, 0.8 m high, with 14–16 holes, diameterof holes from 5 to 12 cm of which eight holes were used forplanting corals and the remaining 6–8 holes were left fororganisms to get in and out. The reefball can be placed onsand or rubble bottom. Coral pieces were tied on the shelter byfishing line and then the reefball was dropped into the sea.

le 1ter quality criteria for coastal environment and aquaculture.rce: Ministry of Environment and Resources, 2008).

arameters Unit Vietnam ASEANa

H 6.5–8.5 –

issolved oxygen (DO) mg/L ≥5 4SS mg/L 50 10% increaseOD mg/L 3 –

OD5 mg/L 4–6 –

yanide mg/L 0.005 0.007mmonium (NH4

+–N) mg/L 0.1 0.07itrate (NO3–N) mg/L 2 0.06itrite (NO2–N) mg/L 0.01 0.055hosphate (PO4

3−–P) mg/L 0.1 0.015

a ASEAN¼Association of South East Asian Nations.

−

Natural shelter: This kind of shelter took advantage of the deadcoral rock. Steel nails about 15 cm long and pointed at one endwere driven 5–10 cm into coral rock, and coral fragments weretied on by plastic rope.

−

Coral seed was taken from donor reefs around the Co To area,most of them were massive, encrusting and laminae. Nobranching corals were included because they were completelydead in the area. Coral seed was placed in water containerswith aero pump. Coral colonies were then cut into small pieceswith a size of 5–15 cm.

3. Results and discussion

3.1. The degradation and current status of coral in Co To

Co To Archipelago has natural and environmental conditionssuitable for the growth of coral. A total of 114 species, 37 generaand 13 families have been found in the area (WWF, 1994).According to WWF′s experts, at that time, corals had high speciesrichness and abundance, and the most common species belongedto the branching coral genus Acropora, which are rapid growingand dominant on reef. Hong Van reef was the largest coral reef notonly in Co To but also in the North of Vietnam with a length of5 km and 1 km in width with high coral cover. The area around theDang Van Chau Island and southwest Thanh Lan Island had thehighest coral coverage (classified as very good and excellent reef).Biological resources on the reefs were also very rich, notably seacucumbers, cone snails, pearl oysters, and abalone.

When the survey was repeated in 2003 on most reefs manynewly dead corals that still retained their shape were seen, most ofwhich were branching corals. Live coral cover and species numberwere reduced when compared to previous results. At the sametime the number of species of valuable economic resources, seacucumber and abalone were also greatly reduced.

In 2008 most coral reefs in this area had died completely, only afew reefs with sparse coral cover were left. Generally loss wasabout 80% of the number of species and about 90% of the reef area(Fig. 2). This is the greatest and fastest degradation recorded in thecoastal areas of Vietnam. On the reef only coral rock and sand wasfound, some covered with seaweed. The Hong Van, Bac Van reef,which has been considered the biggest and most beautiful reef inthe north of Vietnam was now completely dead, and the otherreefs around the island Co To Lon, Dang Van Chau, Khe Trau werein the same condition. Especially, no branching corals were foundin the region—the most common species in the Co To before. Somesurviving corals were massive, encrusting and laminae that werescattered in the south of Khe Trau, Thanh Mai, Dang Van Chau,Co To Con with a very low density. Distance between remainingcolonies was between 3 and 4 m, and colonies were small size,about 20–40 cm.

The number of coral species in the Co To at present is very low,in total 24 species of hard corals and one species of soft coral werefound. The distribution of species varied among reefs, most reefshad only single species. In Dang Van Chau Island the only specieswere Turbinaria peltata and Goniopora lobata, in Thanh Mai it wasPlesiastrea versipora. The North Trau Khe was more varied, speciesincluded Galaxea, Favia, Goniopora, Porites but Goniastreawas mostabundant. At this time six reefs were surveyed for coral cover buttwo reefs had no living coral (Hong Van and North Khe Trau), tworeefs were very sparse in living coral of small size (Dang Van Chauand Thanh Mai). Coral cover was higher south of Khe Trau and CoTo Con Island (from 3.5 to 7.5%), most colonies were small. On allreefs the coverage of dead coral was high, 40–85% (Table 2, Fig. 4).

Fig. 1. Location of Co To Archipelago and studied sites.

0

10

20

30

40

50

60

70

Livi

ng c

oral

cov

er (

%)

In 1994 In 2003 In 2008

Fig. 2. Decrease of living coral cover over time.

N.D. Ngai et al. / Deep-Sea Research II 96 (2013) 50–5552

3.2. Causes of coral degradation

To find the cause of coral death, the results of field studies,monitoring of environmental factors and information from fisher-men on the archipelago have been combined:

Analysis of water quality in this area showed that the tempera-ture over two seasons ranged from 21.1 to 31 1C, average 25.0 1C insurface water and at the bottom ranged from 21.3 to 30.3 1C,average 24.3 1C. Salinity was high and relatively stable, rangingfrom 30.0 to 33.0‰ for surface water and from 31.5 to 33.0‰ at thebottom; pH ranged from 8.00 to 8.36. Dissolved oxygen concen-tration was high, surface values ranged between 6.38 and6.64 mgO2/L, average 6.49 mgO2/L, bottom values from 5.79 to6.42 mgO2/L, average 6.14 mgO2/L. Turbidity was low, surface layerranged from 1.00 to 6.61 NTU, 3.72 NTU on average, and bottomrange from 2.19 to 14.22 NTU, average 7.05 NTU.

Concentrations of nutrients (ammonium, phosphate, nitrate,nitrite), organic matter (BOD5, COD), pesticide were within accep-table limits according to Vietnam′s water quality standards. The

most notable exception was the concentration of cyanide in thewater, which was very high, sometime exceeding the permittedstandards (5 μg/L). Specifically, at the monitoring stations thecyanide concentration ranged from 4.13 to 5.72 μg/L, average4.95 μg/L, bottom concentration higher than in the surface layer.While cyanide concentration in water based on standard fromdeveloped countries is 1 μg/L. Cyanide is one of the most poiso-nous chemicals and is highly toxic to both humans and animals,causing death even in trace amounts. Cyanide does not occur innature, but is created by technology and industry and mostlyapplied in large volumes for ferrous metallurgy such as gold oreand metal plating technology (Fig. 3).

The information obtained from interviewing fishermen on theisland show that during the years 2002–2006 about 100 divingboats would regularly exploit fishes around the islands. Especiallythey used cyanide to catch fish on the reefs. There are nomonitoring data from this period, but each diver used several to10 kg of cyanide powder per day. Residue of cyanide in the waterhas killed high numbers of corals, particular sensitive species likeAcropora. In recent years fishermen have not used cyanide to catchfish so the trend of cyanide concentration in the water should begoing down but is still high.

In the survey trips we observed dead corals still retaining theirshapes and unbroken unlike those killed by explosion or strongwaves. Combined with the above findings it can be concluded thatdead coral in Co To is due to the exploitation of marine resourcesby toxic cyanide in the period 2002–2006. Presently the fishermendo not use this method because fish stocks have been depletedand coral ecosystems have been killed so the fishes have lost theirhabitat.

3.3. Natural recovery

Results of monitoring the coral recovery through recruitment ofjuveniles at five reefs have been compiled in Table 3. Reefs with

0

5

10

15

20

25

30

35

Mar2008

Jul 2008 Dec2008

Mar2009

Aug2009

Dec2009

Mar2010

Sep2010

ToC DO (mg/l) pH S‰

0

10

20

30

40

50

60

Mar

2008

Jul 2

008

Dec 2

008

Mar

200

9

Aug 2

009

Dec20

09

Mar

201

0

Sep 2

010

N - NO2-(μg/l) N - NO3-(μg/l)N - NH4+ (μg/l) P - PO43-(μg/l)

0

1

2

3

4

5

6

7

Mar2008

Jul 2008 Dec2008

Mar2009

Aug2009

Dec2009

Mar2010

Sep2010

BOD5 (mg/l) COD (mg/l) CN-(µg/l)

Fig. 3. Concentration of environmental parameters monitored at field from2008–2010.

Fig. 4. Dead coral reef in Co To Islands.

Fig. 5. Settlement of juveniles on bottom.

Fig. 6. Coral colonies transplanted on reefball after 3 months.

Table 2Coverage (%) of substrate on the reef in 2008.

Reef name Hardcoral

Softcoral

Deadcoral

Rock Sand Rubble Sponge

Hong Van 0 0 40 0 58 0 2Thanh Mai 0.6 0 64.4 0 35 0 0Dang Van Chau 0.6 0 84.4 0 15 0 0Northwest KheTrau

0 0 80 0 20 0 0

South Khe Trau 3.5 0 52 0 44.5 0 0Co To Con 7.5 0 68.7 0 22.5 1.3 0

N.D. Ngai et al. / Deep-Sea Research II 96 (2013) 50–55 53

few live coral colonies had low settlement rate from 1–2 colonies/year, while reefs which had more living coral had higher rates ofcoral recruitment from 23–28 colonies/100 m2/year (Fig. 5). Three

reefs with no living corals had no recruitment of juvenile coralsafter two monitoring years as seen in North Khe Trau, Thanh Maiand Dang Van Chau. The most likely reason for this is that therewas no in-situ source of larvae so that they must depend on ex-sitularvae supply and only small coral areas are available nearby. Onthe other hand these reefs may be seriously affected by cyanide insediment and dead coral rock and the available coral larvae mayhave died after settlement on bottom.

The natural recovery of the coral colonies is still going on atalmost all of the surveyed sites through slow growth of thesurviving coral colonies. Monitoring the growth rate of some coralcolonies on reefs showed that growth of coral in this area was thesame as in other areas and as growth of corals in general. Mostcorals have growth rates from 2 to 3 cm/year (Table 4). The lowestgrowth rate is about 1 cm/year in the genus Porites. Particularlyslow growth is seen in the species Pseudosiderastrea tayami whichonly grows 0.5 cm/year due to the small size of this species, thelargest colony having a maximum size of only about 16 cm (Veron,2000).

Although concentration of cyanide in the water remains highthe natural recovery of coral reefs through growth of remaining

N.D. Ngai et al. / Deep-Sea Research II 96 (2013) 50–5554

colonies and recruitment of new juveniles still occurs at slowspeed. Unfortunately, the branching coral species which haverapid growth rates do not exist anymore in the Co To region andthus rehabilitation will happen slowly by massive, encrusting,laminae corals.

3.4. Artificial restoration on shelters

A total of 130 reefballs were used for transplanting coral at3 sites (Fig. 6). Survival rate and growth of corals were monitireson 29 reefballs with 231 colonies. The survival rate of coralsgrowing on reefballs was very high, reaching over 95% in the firstyear and 88.3% after 2 years (Table 5). Coral colonies died mainlyfrom shock during the separation processing into smaller coloniesand some colonies were lost from the shelters due to poorattachment in the first year. In the second year the transplanted

Table 3Number of juvenile coral settlement on reef.

Site In 8/2008 In 9/2009 In 9/2010

North Khe Trau 0 0 0South Khe Trau 2 1 0Dang Van Chau 0 0 0Thanh Mai 0 0 0Co To Con 27 28 23

Table 4Measurement of natural coral colonies (cm).

Species name Originsize8/2008

Increase9/2009a

Increase9/2010a

Goniopora lobata 18.5 2.5 2.521 2.5 2.5

Turbinaria peltata 57 3 350 2.5 3

Porites lutea 68 1 1Pavona decussata 39 3 2.5

30 2.5 2Goniastrea favulus 25.5 2.5 2.5

31 3 2.5Pseudosiderastreatayami

7.5 0.5 0.5

Plesiastrea versipora 22 2.5 217 2.2 2

a Measured by fiberglass tape over colonies.

Table 5Ratio (%) of live coral transplanted on reefball.

Species name Number of coralcolony

Averagemeasurement (cm)a

Echinophyllia aspera 21 9.1Galaxea fascicularis 3 9.96Goniopora columna 13 9.3Pavona decussata 2 12.5Goniastrea favulus 42 9.42Porites lutea 2 11.24Turbinaria peltata 79 10.9Favites sp 1 10.5Plesiastrea versipora 68 10.9

Total 231 10.4

a Measured by fiberglass tape over colonies.

coral had grown normally, they were adhering to shelters andcovering plastic rope tightly. Unfortunately, a bloom of the coralpredator, the snail Drupella sp., occurred in the Co To area. Theyoften assemble in small groups of 5–10 individuals and eat coraltissue and therefore survival rate of coral was reduced in thesecond year.

For coral colonies that were transplanted on coral rock by usingsteel nails driven into the substrate and tied by plastic rope, about93 colonies were monitored for survival rate. The fraction ofsurviving coral was low, the main reason being that fixation ofcoral pieces on to shelter was not tight enough and tying was moredifficult for massive and laminae shape when tying under water.On the other hand the appearance of the snail Drupella was thebiggest threat to the new coral transplanted on this substratebecause they are easy to access and the injuries of the coralcolonies after the separation process attracted the snail predators.The rate of survival of these corals was 55.9% after 2 years(Table 6).

Therefore, artificial coral restoration can be carried out on alarge scale on the degraded reefs in the Co To archipelago both onnatural and artificial shelters. Growth of corals on the reefball hasmany advantages when compared to the natural shelter: highsurvival rate, easier to handle, lower rate of detachment andpredation by snails. When carrying out transplanting on largescale it should be noted that the donor reefs are now sparse in livecorals so that transplantation may affect the donor reef, and the

Growth rate/year(cm)a

Number of colonyeaten by predatorand detached

Survival ratio (%)

2.7 2 90.52.6 1 66.72.4 0 100.02.15 1 50.02.58 9 78.61 1 50.02.75 11 86.12.1 0 1002.66 2 97.1

2.3 27 88.3

Table 6Survival ratio of transplanted coral on natural shelters.

Name Numberof coralcolony

Averagemeasurement(cm)a

Growthrate/year(cm)

Number ofcolony eaten bypredator anddetached

Survivalratio (%)

Plesiastreaversipora

33 11.2 2.46 16 51.5

Echinophylliaaspera

6 9.4 2.95 4 33.3

Gonioporacolumna

2 12 2.4 1 50

Turbinariapeltata

34 10.5 2.5 11 67.6

Galaxeafascicularis

1 8.2 1 0.0

Goniastreafavulus

17 9.28 2.75 8 52.9

Total 93 10.1 2.612 41 55.9

a Measured by fiberglass tape over colonies.

N.D. Ngai et al. / Deep-Sea Research II 96 (2013) 50–55 55

outbreak of the predator snail Drupella sp. is the biggest threat totransplanted corals.

4. Conclusions

The degradation of coral reefs in the Co To Archipelago wasvery serious. It occurred mainly in the period from 2002 to 2006and has reduced the number of species from 127 to 25. Nearly 80%of species, 90% of live coral cover, and 100% of some reefs werelost. Currently the highest coral coverage in the Co To area is 7.5%whereas previously most of the reefs had coverage of at least 50%.Research results have identified the cause of coral death to be coralfishermen using cyanide poison to catch coral fishes for a longtime. Residues of cyanide also killed coral on a large scaleespecially branching coral Acropora that are very sensitive toenvironmental changes has been killed completely. Monitoringshowed that the natural recovery of corals is taking place slowly.On the completely dead reefs there is no recovery of corals due tono source of larvae within these reefs, whereas on some livingcoral reefs the coral recruitment is high. Restoration of corals bytransplanting on two types of shelters resulted in significantdifferences in survival rates. For corals growing on the reefballssurvival rate was higher than on natural substrates (88.3% and55.9% respectively) because it was easier to tie the massive andlaminae corals on reefballs than on natural shelters, whichreduced the accessibility of attack of predator. This opens upprospects for artificial restoration of coral reefs in this area if wecan control the amount of predation by the snail Drupella sp.

Acknowledgments

This work is supported by KC.09.07/11-15 program (Littoralecosystems in the north of Vietnam Project) and People′s Com-mittee of Quang Ninh province. We are very grateful to all ourcolleagues for their hard work in the field to install experimentsand monitor water environment in Co To Islands. We also thankProf. Jing Zhang, who is leader of CoReCAP Project (IOC/WESTPAC)encouraged us to submit this paper. And many thanks to Dr. KatheRose Jensen for editing the English language. We also thank theanonymous reviewers for their pertinent and helpful comments.

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