Deep-Sea Research II 96 (2013) 50–55 Contents lists available at ScienceDirect Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2 Coral degradation and ability of rehabilitation of coral reefs in Co To Archipelago, Quang Ninh province, Vietnam Nguyen Dang Ngai n, Nguyen Duc Cu, Dao Anh Tuyet Institute of Marine Environment and Resources (IMER), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet Str., Cau Giay Distr., Hanoi, Viet Nam art ic l e i nf o a b s t r a c t Available online 25 April 2013 Serious degradation of coral reefs in the Co To Archipelago occurred from 2002 to 2006 Nearly 80% of the 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 The cause of the reef degradation has been identified to be residues of cyanide used by local fishermen for fishing on reefs To overcome the consequences transplantation corals on natural and artificial shelters were attempted Survival rate on artificial shelters was 88.3% after years and growth rate averaged 2.3 cm/year Transplanted corals on natural shelters had lower survival rate, 55.9% The natural recovery of coral on degraded reefs was also monitored periodically in this study No coral recruitment was seen on completely dead reefs whereas there was little new coral recruitment on reefs with some remaining live corals & 2013 Elsevier Ltd All rights reserved Keywords: Coral degradation Recovery Growth rate Transplant Introduction Serious degradation has been observed on many coral reefs worldwide For more than a decade area, coverage and number of species have been reduced (McClanahan, 2002; Wilkinson, 2004, 2008; Lough and Van Oppen, 2009) Many causes for this decline have been described from different regions, e.g increasing seawater temperature (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 can self-recover (Hughes et al., 2010; Sheppard et al., 2008; Halford et al., 2004) some need help from artificial restoration and others were unable to restore because substrate or environment was not suitable for coral growth (Fabricius, 2005; Scheffer et al., 2001, Hughes, 1994, Hughes et al., 2010) Application of transplanting on artificial and natural shelters for coral restoration has been successful in many areas of the world (Clark and Edwards, 1994; Rinkevich, 2005; Quan and Ngai, 2008) The restoration methods included: physical, biological, and dual restoration (combination of biological and physical restoration) (Job et al., 2003) Depending on the specific conditions of each area the most suitable methods for rehabilitation may be chosen The most widely used methods are the reefball and natural shelters (Rinkevich, 2000) Almost all coral reefs in Co To Islands died between 2002 and 2006 In recent years, though the water seems clean, the bottom substrate is dead coral rock and sand and very little coral has recruited here The purpose of this study was to examine the natural recovery of coral on degraded reefs and carry out experiments to test for survival and growth rate of corals on natural and artificial shelters in order to develop a management plan for effective protection and restoration of coral reefs Research methods 2.1 Study area Co To Archipelago belongs to Quang Ninh province, in northern Vietnam, about 50 km from the mainland (20156′00″–21104′00″N and 107144′00″–107152′00″E), with more than 15 islands The total area of Co To Islands is 46.2 km² A population of 5195 people (in 2006) live mainly on capture fishery and agriculture This area has favorable natural conditions for reef development such as: warm and clear water, high salinity, hard substrate Therefore, coral ecosystems are developed with over 100 species of hard corals, high coverage and the biggest reef in northern Vietnam The Islands have high biodiversity including many valuable and commercial species for example reef fishes, abalone, sea cucumber, pearl oyster Additionally this area is an important fishing ground and seed is dispersed to nearby coastal areas (WWF, 1994) Therefore, Co To Islands have been considered for a list of 15 marine protected areas in Vietnam 2.2 Method of determining the status and degradation of coral n Corresponding author E-mail addresses: ngaind@imer.ac.vn, ngaind@yahoo.com (N.D Ngai) 0967-0645/$ - see front matter & 2013 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.dsr2.2013.04.017 The overall status of coral reefs in the Co To was surveyed by using a small boat pulling the observer on the water surface above N.D Ngai et al / Deep-Sea Research II 96 (2013) 50–55 the reefs to observe and record the data on living coral, dead coral, soft coral and macro-benthos (English et al., 1997) and then select sites to beused for specific survey by point transect method to get data on each component of substrate, coral fishes and other benthic communities (Hodgson et al., 2004) During the survey we focused on the status of coral death and the cause of death − Local fishermen were internviewed to find out the cause of death of corals in this area Questionnaires focused on production, the target species of exploitation, exploitation methods, fishing gears, etc − The environmental parameters were periodically monitored at three study sites (Trau Khe, Thanh Mai, Dang Van Chau) in 2008, 2009 and 2010 Each year the three sites were monitored for three days Measurement directly and samples for analysis were collected at the surface and bottom times/24 h Field parameters such as salinity were measured by refractometer, temperature and DO was measured by a DO meter, pH was measured by pH meter OKATON, transparency was measured by secchi disk The samples for nutrient, cyanide, pesticide and other water quality measurements were collected at each site at both surface and bottom layer, fixed by suitable chemicals and analyzed in the laboratory In order to assess status of water environmental quality, measurements were compared to promulgated standards of Vietnam and Asian countries (Table 1) 2.3 Method of monitoring the natural recovery − Growth of natural corals was monitored by attaching labels on several colonies and measures them periodically A total of 12 coral colonies were marked and measured one time a year by fiberglass ruler over colony at each site from 2008 to 2010 − The recruitment of coral juveniles was monitored and observed on transect lines with length of 20 m at reefs (Fig 1), observing and counting the number of small coral colonies, less than cm of coral, within 2.5 m on each side of the transect The reefs were selected for monitoring at different places (in and outside Co To bay, 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 measurements: m in diameter, 0.8 m high, with 14–16 holes, diameter of holes from to 12 cm of which eight holes were used for planting corals and the remaining 6–8 holes were left for organisms to get in and out The reefball can be placed on sand or rubble bottom Coral pieces were tied on the shelter by fishing line and then the reefball was dropped into the sea Table Water quality criteria for coastal environment and aquaculture (Source: Ministry of Environment and Resources, 2008) Parameters Unit Vietnam ASEANa pH Dissolved oxygen (DO) TSS COD BOD5 Cyanide Ammonium (NH4+–N) Nitrate (NO3–N) Nitrite (NO2–N) Phosphate (PO43−–P) mg/L mg/L mg/L mg/L mg/L mg/L mg/L mg/L mg/L 6.5–8.5 ≥5 50 4–6 0.005 0.1 0.01 0.1 – 10% increase – – 0.007 0.07 0.06 0.055 0.015 a ASEAN ¼ Association of South East Asian Nations 51 − Natural shelter: This kind of shelter took advantage of the dead coral rock Steel nails about 15 cm long and pointed at one end were driven 5–10 cm into coral rock, and coral fragments were tied on by plastic rope − Coral seed was taken from donor reefs around the Co To area, most of them were massive, encrusting and laminae No branching corals were included because they were completely dead in the area Coral seed was placed in water containers with aero pump Coral colonies were then cut into small pieces with a size of 5–15 cm Results and discussion 3.1 The degradation and current status of coral in Co To Co To Archipelago has natural and environmental conditions suitable for the growth of coral A total of 114 species, 37 genera and 13 families have been found in the area (WWF, 1994) According to WWF′s experts, at that time, corals had high species richness and abundance, and the most common species belonged to the branching coral genus Acropora, which are rapid growing and dominant on reef Hong Van reef was the largest coral reef not only in Co To but also in the North of Vietnam with a length of km and km in width with high coral cover The area around the Dang Van Chau Island and southwest Thanh Lan Island had the highest coral coverage (classified as very good and excellent reef) Biological resources on the reefs were also very rich, notably sea cucumbers, cone snails, pearl oysters, and abalone When the survey was repeated in 2003 on most reefs many newly dead corals that still retained their shape were seen, most of which were branching corals Live coral cover and species number were reduced when compared to previous results At the same time the number of species of valuable economic resources, sea cucumber and abalone were also greatly reduced In 2008 most coral reefs in this area had died completely, only a few reefs with sparse coral cover were left Generally loss was about 80% of the number of species and about 90% of the reef area (Fig 2) This is the greatest and fastest degradation recorded in the coastal areas of Vietnam On the reef only coral rock and sand was found, some covered with seaweed The Hong Van, Bac Van reef, which has been considered the biggest and most beautiful reef in the north of Vietnam was now completely dead, and the other reefs around the island Co To Lon, Dang Van Chau, Khe Trau were in the same condition Especially, no branching corals were found in the region—the most common species in the Co To before Some surviving corals were massive, encrusting and laminae that were scattered in the south of Khe Trau, Thanh Mai, Dang Van Chau, Co To Con with a very low density Distance between remaining colonies was between and 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 were found The distribution of species varied among reefs, most reefs had only single species In Dang Van Chau Island the only species were Turbinaria peltata and Goniopora lobata, in Thanh Mai it was Plesiastrea versipora The North Trau Khe was more varied, species included Galaxea, Favia, Goniopora, Porites but Goniastrea was most abundant At this time six reefs were surveyed for coral cover but two reefs had no living coral (Hong Van and North Khe Trau), two reefs were very sparse in living coral of small size (Dang Van Chau and Thanh Mai) Coral cover was higher south of Khe Trau and Co To Con Island (from 3.5 to 7.5%), most colonies were small On all reefs the coverage of dead coral was high, 40–85% (Table 2, Fig 4) 52 N.D Ngai et al / Deep-Sea Research II 96 (2013) 50–55 Fig Location of Co To Archipelago and studied sites 70 Living coral cover (%) 60 50 40 30 20 10 In 1994 In 2003 In 2008 Fig Decrease of living coral cover over time 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 fishermen on the archipelago have been combined: Analysis of water quality in this area showed that the temperature over two seasons ranged from 21.1 to 31 1C, average 25.0 1C in surface water and at the bottom ranged from 21.3 to 30.3 1C, average 24.3 1C Salinity was high and relatively stable, ranging from 30.0 to 33.0‰ for surface water and from 31.5 to 33.0‰ at the bottom; pH ranged from 8.00 to 8.36 Dissolved oxygen concentration was high, surface values ranged between 6.38 and 6.64 mgO2/L, average 6.49 mgO2/L, bottom values from 5.79 to 6.42 mgO2/L, average 6.14 mgO2/L Turbidity was low, surface layer ranged from 1.00 to 6.61 NTU, 3.72 NTU on average, and bottom range 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 acceptable limits according to Vietnam′s water quality standards The most notable exception was the concentration of cyanide in the water, which was very high, sometime exceeding the permitted standards (5 μg/L) Specifically, at the monitoring stations the cyanide concentration ranged from 4.13 to 5.72 μg/L, average 4.95 μg/L, bottom concentration higher than in the surface layer While cyanide concentration in water based on standard from developed countries is μg/L Cyanide is one of the most poisonous chemicals and is highly toxic to both humans and animals, causing death even in trace amounts Cyanide does not occur in nature, but is created by technology and industry and mostly applied in large volumes for ferrous metallurgy such as gold ore and metal plating technology (Fig 3) The information obtained from interviewing fishermen on the island show that during the years 2002–2006 about 100 diving boats would regularly exploit fishes around the islands Especially they used cyanide to catch fish on the reefs There are no monitoring data from this period, but each diver used several to 10 kg of cyanide powder per day Residue of cyanide in the water has killed high numbers of corals, particular sensitive species like Acropora In recent years fishermen have not used cyanide to catch fish so the trend of cyanide concentration in the water should be going down but is still high In the survey trips we observed dead corals still retaining their shapes and unbroken unlike those killed by explosion or strong waves Combined with the above findings it can be concluded that dead coral in Co To is due to the exploitation of marine resources by toxic cyanide in the period 2002–2006 Presently the fishermen not use this method because fish stocks have been depleted and coral ecosystems have been killed so the fishes have lost their habitat 3.3 Natural recovery Results of monitoring the coral recovery through recruitment of juveniles at five reefs have been compiled in Table Reefs with 53 N.D Ngai et al / Deep-Sea Research II 96 (2013) 50–55 35 30 25 20 15 10 Mar Jul 2008 Dec 2008 2008 Mar 2009 ToC Aug 2009 Dec 2009 DO (mg/l) Mar 2010 pH Sep 2010 S‰ Fig Settlement of juveniles on bottom 60 50 40 30 20 10 20 p Se ar 20 10 10 09 M ec D 20 Au g ar N - NO2-(µg/l) N - NH4+ (µg/l) 20 09 09 20 08 M D ec 20 00 l2 Ju M ar 20 08 N - NO3-(µg/l) P - PO43-(µg/l) Fig Coral colonies transplanted on reefball after months Table Coverage (%) of substrate on the reef in 2008 Reef name Hard coral Soft coral Dead coral Rock Sand Rubble Sponge Hong Van Thanh Mai Dang Van Chau Northwest Khe Trau South Khe Trau Co To Con 0.6 0.6 0 0 40 64.4 84.4 80 0 0 58 35 15 20 0 0 0 3.5 7.5 0 52 68.7 0 44.5 22.5 1.3 0 Mar Jul 2008 Dec 2008 2008 BOD5 (mg/l) Mar 2009 Aug 2009 COD (mg/l) Dec 2009 Mar 2010 Sep 2010 CN-(µg/l) Fig Concentration of environmental parameters monitored at field from 2008–2010 Fig Dead coral reef in Co To Islands few live coral colonies had low settlement rate from 1–2 colonies/ year, while reefs which had more living coral had higher rates of coral recruitment from 23–28 colonies/100 m2/year (Fig 5) Three reefs with no living corals had no recruitment of juvenile corals after two monitoring years as seen in North Khe Trau, Thanh Mai and Dang Van Chau The most likely reason for this is that there was no in-situ source of larvae so that they must depend on ex-situ larvae supply and only small coral areas are available nearby On the other hand these reefs may be seriously affected by cyanide in sediment and dead coral rock and the available coral larvae may have died after settlement on bottom The natural recovery of the coral colonies is still going on at almost all of the surveyed sites through slow growth of the surviving coral colonies Monitoring the growth rate of some coral colonies on reefs showed that growth of coral in this area was the same as in other areas and as growth of corals in general Most corals have growth rates from to cm/year (Table 4) The lowest growth rate is about cm/year in the genus Porites Particularly slow growth is seen in the species Pseudosiderastrea tayami which only grows 0.5 cm/year due to the small size of this species, the largest colony having a maximum size of only about 16 cm (Veron, 2000) Although concentration of cyanide in the water remains high the natural recovery of coral reefs through growth of remaining 54 N.D Ngai et al / Deep-Sea Research II 96 (2013) 50–55 colonies and recruitment of new juveniles still occurs at slow speed Unfortunately, the branching coral species which have rapid growth rates not exist anymore in the Co To region and thus 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 at sites (Fig 6) Survival rate and growth of corals were monitires on 29 reefballs with 231 colonies The survival rate of corals growing on reefballs was very high, reaching over 95% in the first year and 88.3% after years (Table 5) Coral colonies died mainly from shock during the separation processing into smaller colonies and some colonies were lost from the shelters due to poor attachment in the first year In the second year the transplanted Table Number of juvenile coral settlement on reef Site In 8/2008 In 9/2009 In 9/2010 North Khe Trau South Khe Trau Dang Van Chau Thanh Mai Co To Con 0 27 0 28 0 0 23 Table Survival ratio of transplanted coral on natural shelters Table Measurement of natural coral colonies (cm) Species name Origin size 8/2008 Increase 9/2009a Increase 9/2010a Goniopora lobata 18.5 21 57 50 68 39 30 25.5 31 7.5 2.5 2.5 2.5 2.5 2.5 0.5 2.5 2.5 3 2.5 2.5 2.5 0.5 22 17 2.5 2.2 2 Turbinaria peltata Porites lutea Pavona decussata Goniastrea favulus Pseudosiderastrea tayami Plesiastrea versipora a coral had grown normally, they were adhering to shelters and covering plastic rope tightly Unfortunately, a bloom of the coral predator, the snail Drupella sp., occurred in the Co To area They often assemble in small groups of 5–10 individuals and eat coral tissue and therefore survival rate of coral was reduced in the second year For coral colonies that were transplanted on coral rock by using steel nails driven into the substrate and tied by plastic rope, about 93 colonies were monitored for survival rate The fraction of surviving coral was low, the main reason being that fixation of coral pieces on to shelter was not tight enough and tying was more difficult for massive and laminae shape when tying under water On the other hand the appearance of the snail Drupella was the biggest threat to the new coral transplanted on this substrate because they are easy to access and the injuries of the coral colonies after the separation process attracted the snail predators The rate of survival of these corals was 55.9% after years (Table 6) Therefore, artificial coral restoration can be carried out on a large scale on the degraded reefs in the Co To archipelago both on natural and artificial shelters Growth of corals on the reefball has many advantages when compared to the natural shelter: high survival rate, easier to handle, lower rate of detachment and predation by snails When carrying out transplanting on large scale it should be noted that the donor reefs are now sparse in live corals so that transplantation may affect the donor reef, and the Name Number of coral colony Average measurement (cm)a Growth rate/ year (cm) Number of colony eaten by predator and detached Survival ratio (%) Plesiastrea versipora Echinophyllia aspera Goniopora columna Turbinaria peltata Galaxea fascicularis Goniastrea favulus 33 11.2 2.46 16 51.5 9.4 2.95 33.3 12 2.4 50 34 10.5 2.5 11 67.6 8.2 0.0 17 9.28 2.75 52.9 2.612 41 55.9 Total a Measured by fiberglass tape over colonies 93 10.1 Measured by fiberglass tape over colonies Table Ratio (%) of live coral transplanted on reefball Species name Echinophyllia aspera Galaxea fascicularis Goniopora columna Pavona decussata Goniastrea favulus Porites lutea Turbinaria peltata Favites sp Plesiastrea versipora Total a Growth rate/year Average measurement (cm)a (cm)a Number of colony eaten by predator and detached Survival ratio (%) 21 13 42 79 68 9.1 9.96 9.3 12.5 9.42 11.24 10.9 10.5 10.9 2.7 2.6 2.4 2.15 2.58 2.75 2.1 2.66 1 11 90.5 66.7 100.0 50.0 78.6 50.0 86.1 100 97.1 231 10.4 2.3 27 88.3 Number of coral colony Measured by fiberglass tape over colonies N.D Ngai et al / Deep-Sea Research II 96 (2013) 50–55 outbreak of the predator snail Drupella sp is the biggest threat to transplanted corals Conclusions The degradation of coral reefs in the Co To Archipelago was very serious It occurred mainly in the period from 2002 to 2006 and has reduced the number of species from 127 to 25 Nearly 80% of species, 90% of live coral cover, and 100% of some reefs were lost 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 coral fishermen using cyanide poison to catch coral fishes for a long time Residues of cyanide also killed coral on a large scale especially branching coral Acropora that are very sensitive to environmental changes has been killed completely Monitoring showed that the natural recovery of corals is taking place slowly On the completely dead reefs there is no recovery of corals due to no source of larvae within these reefs, whereas on some living coral reefs the coral recruitment is high Restoration of corals by transplanting on two types of shelters resulted in significant differences in survival rates For corals growing on the reefballs survival rate was higher than on natural substrates (88.3% and 55.9% respectively) because it was easier to tie the massive and laminae corals on reefballs than on natural shelters, which reduced the accessibility of attack of predator This opens up prospects for artificial restoration of coral reefs in this area if we can control the amount of predation by the snail Drupella sp Acknowledgments This work is supported by KC.09.07/11-15 program 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Location of Co To Archipelago and studied sites 70 Living coral cover (%) 60 50 40 30 20 10 In 1994 In 2003 In 2008 Fig Decrease of living coral cover over time 3.2 Causes of coral degradation To find... encrusting and laminae No branching corals were included because they were completely dead in the area Coral seed was placed in water containers with aero pump Coral colonies were then cut into small... 2000 Corals of the World Institute of Marine Science, Australia vols 1, 2, and Wilkinson, C., 2004 Status of Coral Reefs of the World: 2004 Vol 1,2 Global Coral Reef Monitoring Network and Reef and