Journal of Asian Earth Sciences 114 (2015) 457–466

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Journal of Asian Earth Sciences

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Impact on the coral reefs at Yongle Atoll, Xisha Islands, South Sea from a strong typhoon direct sweep: Wutip, September 2013 ⇑ Hongqiang Yang b, Kefu Yu a,b, , Meixia Zhao b, Qi Shi b, Shichen Tao b, Hongqiang Yan b, Tianran Chen b, Guohui Liu b a Coral Reef Research Centre of China, Guangxi University, Nanning 530004, PR China b Key Laboratory of Marginal Sea Geology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, PR China article info abstract

Article history: Relatively little is known about the extent and distribution of damage to coral reefs by typhoons in the Received 3 October 2014 South China Sea, especially in remote reefs where typhoons occur frequently. A strong Typhoon, Wutip Received in revised form 25 March 2015 (JTWC Category 3), directly struck the Yongle Atoll on 29 September 2013, causing 62 deaths and sinking Accepted 1 April 2015 dozens of ships in the Yongle Atoll maritime area, Xisha Islands, South China Sea. Surveys on coral reefs at Available online 18 April 2015 Yongle Atoll were conducted using scuba diving before (July 2013) and after (8 days) the typhoon sweep. The results show that the effects of Wutip on coral reefs were patchy as a result of varying coral reef geo- Keywords: morphology and depth. The typhoon caused significant damage to reef associated depths on the passage Typhoon Wutip of the atoll, where currents generated by the typhoon produced the strongest energy. Coral destruction Coral reefs Yongle Atoll was most spectacular at the 2 m depth (46% living scleractinian corals were damaged). At 6 m and 15 m Xisha Islands depths, damage to the coral reefs were minimal. The shallow fore-reef area on the steep slopes, the upper region of the outer slopes with depths between 2 and 6 m, were the principal zones of the typhoon effect. However, the vertical part of the steep slopes were mainly damaged indirectly waves rolling boulders or corals, which were less severely affected than the shallow fore-reef steep slope area. On the low angle slopes, the correlation between the typhoon damage to coral reefs and depth was low because the wave and current energy induced by the typhoon were homogenously attenuated along gentle slopes. Under the stress of global warming, destructive damage to coral reefs on the Xisha Islands is expected to increase, and will require frequent monitoring to determine trends in the near future. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction coral reef communities directly, by generating physical devastation or indirectly as a result of stresses, such as enhanced turbidity, dis- Coral reefs are suffering from a variety of natural and anthro- ease outbreak, changes in predator behaviour or fresh water pogenic disturbances, including coral bleaching, ocean acidifica- inflow. On coral reefs, tropical storms cause small to large reduc- tion, coral diseases, tropic storms, over-fishing, pollution and tions in the abundance, area of coverage and species richness of tourism; these disturbances have resulted in significant degenera- corals. tion of complex coral reef ecosystems (Carpenter et al., 2008; The magnitude of damage to coral reefs by tropical cyclonic Comeau et al., 2014; Graham et al., 2013; Hoegh-Guldberg et al., storms at regional and local scales has been well studied (Done, 2007; Hughes et al., 2003; Johns et al., 2014; Nystrom et al., 1992; Gardner et al., 2005; Woodley et al., 1981). The scale and 2000; Osborne et al., 2014; Roff and Mumby, 2012; Yang et al., spatial degree of tropical storm effects on coral reefs vary widely, 2014; Yu, 2012; Zhao et al., 2012). Among them, ocean acidifica- from cases of negligible disturbance to the great devastation of a tion, coral bleaching and increased tropical storm intensity, which three-dimensional reef structure. A large amount of studies have are associated with climatic change, are currently acknowledged as also documented typhoon damage from direct mechanical disrup- having a severe negative impact on coral reefs. Severe tropical tion, sedimentation, salinity changes and turbidity (Cheal et al., storms, which are interrelated with climatic change, influence 2002; Harmelin-Vivien, 1994; Harmelin-Vivien and Laboute, 1986; VanWoesik et al., 1995). Direct physical disturbances not only include the effects of waves induced by tropical storms, such ⇑ Corresponding author at: Coral Reef Research Centre of China, Guangxi University, Nanning 530004, PR China. as dislodgement, overturning, coral breakage and the horizontal E-mail address: [email protected] (K. Yu). movement of debris (Bries et al., 2004; Fabricius et al., 2008; http://dx.doi.org/10.1016/j.jseaes.2015.04.009 1367-9120/Ó 2015 Elsevier Ltd. All rights reserved. 458 H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466

Scoffin, 1993; Woodley et al., 1981), but also the damage caused by et al., 2012). These simulations indicate that the mean magnitude rolling coral rubble or boulders from steep slopes (Fabricius et al., of tropical storms will increase markedly in the immediate future. 2008; Harmelin-Vivien and Laboute, 1986). During tropical storm Scoffin (1993) indicated that the South China Sea reef areas are events, a considerable quantity of sediment is transported and frequently exposed to tropical storm disturbances, but more recent deposited. Some debris rolls into deeper sub-reef environments work shows that past tropical storms occurred frequently for the along steep slopes or is propelled onto beaches above sea level last several thousand years. Using high-precision ageing of across reef-flats (Done, 1992; Harmelin-Vivien and Laboute, storm-transported large Porites blocks on the Yongshu Reef, Yu 1986). The surface salinity changes rapidly, induced by river flood- et al. (2004, 2009) recognized six strong storm events with an aver- ing and torrential rainfall related to tropical storms, which may age period of 160 years during the last millennium. Yu et al. (2009) result in the death of coral colonies living in the shallow sea also found that storm activities in the South China Sea increased (Harmelin-Vivien, 1994; Williams and Bunkley-Williams, 1990). over the last 4000 years by analysing both lagoon sediments and Intense water movements induced by tropical storms stir sediment wave-transported coral blocks. However, in contrast to abundant material in lagoons and reefs. In addition, heavy rainfall results in scientific achievements on the possible effects of modern tropical turbid waters flowing into the reef area. These lead to an increase storms on coral reefs from the Great Barrier Reef and the in water turbidity that may decrease the available light for coral Caribbean Sea, there is still little known about how typhoons influ- colonies (Riddle, 1988). ence coral reefs in the South China Sea. When Typhoon Wutip One of the predictable results of global climate change is an struck the Yongle Atoll, we were conducting field investigations enhancement in the tropical storm intensity and possibly the fre- on the atoll, which provided an excellent opportunity to directly quency over the next 100 years (Knutson and Tuleya, 2004; observe the effects of the typhoon on the coral reefs. Trenberth, 2005; Walsh and Ryan, 2000; Webster et al., 2005). Recent analysis indicates that following global climate change, 2. Study site the proportion of Category 4–5 hurricanes (super typhoons) will rise at a rate of approximately 40% in proportion per °C increase The Yongle Atoll, a remote near-continuous annular coral atoll, in the Anthropogenic Climate Change Index (ACCI) (Holland and is located in the Xisha Islands, South China Sea, 300 km southeast Bruyere, 2014). Numerical modelling of the influence of global of Island and 80 km southwest of Yongxing Island (Fig. 1). changes may predict the incidence of tropical storms intensity, dis- Twelve islands and reefs developed on the reef rim that encom- tribution, and frequency (Davis and Bosart, 2002; Gopalakrishnan passes a lagoon of approximately 200 km2. Around the atoll rims

Fig. 1. Maps of the Xisha Islands, Yongle Atoll, showing their location in the South China Sea and the sampling sites. (a) Site of the Xisha Islands, South China Sea. Track of Wutip through the South China Sea from 27 to 30 September, 2013 (Purple line). (b) The location of the Yongle Atoll, the Xisha Islands. Typhoon Wutip stuck directly on 29 September, 2013 (Purple line). (c) Site of the Yongle Atoll (16°21042.4900 N, 111°26058.2200 E 16°38020.2300 N, 111°48050.2200 E, Google Earth 2014). 1. Lingyang Reef, 2. Ganquan Island, 3. Shanhu Island, 4. Quanfu Island, 5. Yinyu Reef, 6. Jinqing Island, 7. Chenhang Island, 8. Jinyin Island. Typhoon Wutip stuck directly on 29 September, 2013 (White dashed). Survey sites after typhoon Wutip from October 6–12, 2013. Station 1: Western side of Lingyang Reef; Station 2: Northern side of Lingyang Reef; Station 3: Southern side of Shanhu Island; Station 4: Northern side of Shanhu Island; Station 5: Northern side of Quanfu Island; Station 6: Eastern side of Yinyu Reef; Station 7: Western side of Yinyu Reef. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466 459 there are several deep and wide passages that allow for an other benthic component covers, including dead scleractinian exchange between lagoon water and the open ocean (Fig. 1c). coral, algae, soft coral, reef-rock, rubble and sand were quantified, The climate in the Yongle Atoll region is dominated by the measuring the living scleractinian coral and other benthic compo- northeast monsoon from November to February, with a mean daily nents in centimetre length underlying the line transect. The dam- wind speed peaking in January. Winds become variable from June age to scleractinian corals was divided into the following to October as typhoon and southwest monsoon prevail. The Yongle categories: (a) dislodged—corals that were moved away from their Atoll has been affected by 1.4 typhoons (wind velocity >32.6 m/s) habitat (Fig. 2a); (b) overturned—corals were rotated away from per year, on average, from 1945 to 2014. their habitat; (c) broken—skeletal damage resulting in breakage The mean spring and neap tidal range are 1.22 m and 0.78 m, into two or more parts, mostly affecting branching coral colonies respectively, and the maximum range is 2.0 m (Wang, 2001). The (Fig. 2b); (d) minor damage—corals that were struck by waves Yongle Atoll experiences an irregular semidiurnal microtidal and currents causing minor breakage of parts of corals (Fig. 2c); regime. The circulation of the lagoon is driven by both currents (e) scrape—corals scraped by rubble and boulder movement that and tides. Currents within the deep passages are usually directed was induced by typhoon induced waves and currents (Fig. 2d). from the ocean to the lagoon. On a rising tide, tidal waves enter the passages toward the lagoon. On a falling tide, the lagoon drains through passages around the atoll. 4.2. Data analyses

One-way repeated-measures analysis of variance (ANOVA) was 3. Typhoon Wutip applied to analyse transect data and to examine statistically signif- icant differences in the mean percentage cover of living hard coral, On September 23, 2013, the China Meteorological Agency dead coral, algae, soft coral, reef-rock rubble, and sand between (CMA) reported that a tropical disturbance had developed approx- pre-Wutip and post-Wutip time points using software SPSS18. imately 800 km to the east south of Hainan Island. Enhanced by tropical storm Pabuk nearly, it became a tropical depression and slowly moved westward on September 25. Over the next two days, 5. Results the system gradually strengthened into a tropical storm and was named Wutip on September 27. As it moved westwards the next The mean coverage of living coral significantly decreased after day, Wutip became a severe tropical storm. After a brief time over typhoon Wutip (F = 16.20, P < 0.05, from 16.05% to 13.40%) the Zhongsha Islands, it rapidly became a typhoon. On September (Table 1). There was an evident increase in the mean coverage of 29, Wutip turned into a strong typhoon and formed a perfect dead coral in every transect after Wutip (F = 36.37, P < 0.05, from typhoon eye and moved towards (Fig. 1a). The United 1.30% to 2.72%) (Table 1). The composition of the benthic sub- States Navy Joint Typhoon Warning Center (JTWC) defined it as a stances also displayed considerable changes before and after Category 3 (Saffir–Simpson scale) typhoon. Wutip was quickly Wutip (Table 2), as follows: the mean coverage of rock decreased demoted to a tropical storm after it landed Vietnam on from 57.10% to 51.45% (F = 20.17, P < 0.05) (Table 1), the mean cov- September 30. It ultimately dissipated on October 2, 2013. erage of rubble increased from 14.39% to 18.15% (F = 18.80, The eye of the typhoon passed directly over the Yongle Atoll on P < 0.05) and sands increased from 7.94% to 9.62% (F = 6.98, the afternoon of September 29 (Fig. 1b), accompanied by 49 m/s P < 0.05) (Table 1). However, observations showed that typhoon- sustained winds and 948 h Pa atmospheric pressure (Robert, induced damage on the coral reefs varied greatly between the atoll 2014). The Shanhu Island Meteorological Observatory recorded channel, steep slopes and gentle slopes. Within any area, the cate- the 58 m/s wind gusts. The intensity of Wutip was strongest when gory and quantity of damage enforced on corals strongly depended it passed through the Yongle Atoll. JTWC documented this record- on their sizes, shapes and mechanical characteristics. breaking typhoon as the second strongest typhoon to directly The typhoon also caused significant damage at the reef associ- strike the Yongle Atoll since the Western Pacific typhoon’s track ated depths on the passages in the atoll (Table 2). Large-scale dis- observations were started in 1945. Swells generated by the storm turbances were observed on the reef flat (2 m) of Station 2 and were large enough to break above 8–10 m high. The typhoon led Station 3 on the channel of the atoll. The mean coverage of living to the deaths of 62 people, and dozens of ships sank in the area coral decreased significantly (from 16.69% to 9.03%) (Table 1) after around the Yongle Atoll. The typhoon had significant economic Wutip (Fig. 3a), such that the total amount of intact coral after and infrastructure effects (Kleinen, 2007), notably on the coral reef Wutip was 54.00% compared to 46.00% damaged coral (Fig. 3b). lands. As Wutip progressed across the Yongle Atoll, the central The types of damaged coral included dislodged, broken, minor pressure descended rapidly to 955 h Pa and sustained winds damage and scrape (Fig. 4); dislodged and broken were the most decreased quickly to 42 m/s. Wutip landed on September 30, kill- common types. In addition to these categories of damage, some ing 12 people in Vietnam. bleaching corals were found after Wutip indicating the deteriora- tion of coral health. The mean percentage of dislodged corals was 4. Methods pronouncedly higher in shallower waters. At Station 2, many mas- sive corals that were over 1 m were found to have been dislodged, 4.1. Data collection and some tabular corals (Acropora spp.) had been toppled (Fig. 2a). Some of these corals were completely buried by newly aggregated To evaluate the spatial distribution of coral damage, based on sand and rubble. The robust Pocillopora spp. corals were damaged pre-typhoon surveys conducted in July 2013, we performed a by current-swept reef boulders that scarred and broke the branch- SCUBA survey of typhoon damage to the coral reef at 7 sites along ing corals at Station 3 (Fig. 2b). However, at 6 m and 15 m depths, the windward side of the Yongle Atoll from October 6 to 12, 2013 transects at Station 2 and Station 3 revealed that none of the (Fig. 1c). Each transect was 50 m long along depth contours parallel changes in the mean cover of living coral and dead coral were sig- to the coastline. The most inshore transect was laid out on the reef nificant. The mean coverage of living coral at the 6 m transect at flat at a depth of 2 m. Two parallel transects were consecutively Station 2 decreased slightly (from 11.00% to 10.58%) (Table 1) after located at depths of 6 m and 15 m respectively. Using these parallel Wutip. Slightly damaged and rarely broken corals were found spo- intercept transects, the total living scleractinian coral cover and radically on the 6 and 15 m transects. 460 H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466

Fig. 2. Damaged scleractinia coral features caused by typhoon Wutip (a) Dislodged tabular Acropora sp. Caused by typhoon induced waves or currents (2 m transect at Station 2) on the passage of the atoll. (b) Broken sturdy Pocillopora sp. directly damaged by waves or rolling coral rubble (2 m transect at Station 3) on the passage of the atoll. (c) Minor damage to Acropora sp. struck by rolling sands or waves (6 m transect at Station 6) on low-angle slopes. (d) Scraped crustaceous scleractinia coral from rolling coral rubble or boulder (15 m transect at Station 4) on the steep to vertical slopes.

Table 1 Coverage of coral reefs in benthic constituents before and after the typhoon. B – Before typhoon, A – After typhoon. Stations as shown in Fig. 1c.

Site Depth Living corals Dead corals Rock Rubble Sand Alage Soft corals Other m Coverage (%) Coverage (%) Coverage (%) Coverage (%) Coverage (%) Coverage (%) Coverage (%) Coverage (%) BABABABABABABABA Station 1 2 6.32 5.39 1.12 2.03 77.08 74.14 14.40 15.52 0.52 2.13 0.20 0.55 0.00 0.00 0.36 0.24 6 34.22 31.97 0.42 1.56 60.94 55.83 1.80 6.92 1.21 1.78 0.00 0.00 1.26 1.21 0.15 0.73 15 7.98 8.07 0.00 1.45 80.36 75.43 9.50 11.05 0.00 0.95 0.16 1.47 1.28 1.45 0.72 0.13 Station 2 2 12.12 5.90 1.60 4.45 35.40 23.34 20.63 32.83 24.36 28.48 2.40 3.50 0.00 0.00 3.49 1.50 6 11.84 11.55 4.50 5.27 51.46 49.30 17.50 18.37 11.98 12.29 0.00 0.00 0.00 1.10 2.72 2.12 15 2.42 2.21 0.40 0.61 20.26 19.02 65.48 65.65 11.14 12.01 0.00 0.00 0.00 0.39 0.30 0.11 Station 3 2 21.25 12.15 0.50 3.52 50.02 40.07 14.73 25.83 6.28 9.48 3.00 4.50 2.50 4.00 1.72 0.45 6 2.44 2.60 0.00 0.50 48.78 47.25 33.88 33.45 14.90 15.20 0.00 0.00 0.00 0.50 0.00 0.50 15 3.26 2.94 0.00 1.50 48.82 46.25 24.52 25.45 20.18 18.25 0.56 1.45 0.30 1.10 2.36 3.06 Station 4 2 16.32 13.22 0.00 3.60 71.06 61.30 0.56 4.80 6.88 11.77 0.12 0.98 0.00 0.00 5.06 4.33 6 10.56 8.76 5.74 6.50 72.34 61.15 4.20 9.55 6.76 8.84 0.00 2.00 0.14 0.00 0.26 3.20 15 26.58 24.56 0.64 1.78 66.72 62.35 4.26 5.45 0.44 1.25 0.68 1.80 0.58 1.31 0.10 1.50 Station 5 2 24.54 17.92 2.00 3.85 41.40 31.35 25.92 33.82 5.48 9.35 0.00 1.38 0.00 0.56 0.66 1.77 6 12.16 9.61 2.84 4.45 61.28 52.24 5.82 12.68 17.48 18.17 0.00 1.03 0.36 0.95 0.06 0.87 15 21.80 19.85 0.64 1.01 75.54 73.16 0.00 0.79 0.00 0.95 0.00 0.79 1.60 2.37 0.42 1.08 Station 6 2 34.54 30.02 0.96 2.05 62.48 59.45 0.00 2.19 0.36 2.56 0.18 1.21 0.60 0.80 0.88 1.72 6 24.46 21.12 0.78 2.13 46.78 43.13 1.46 4.19 7.08 10.06 17.42 16.07 1.16 1.80 0.86 1.50 Station 7 2 8.24 4.14 48.45 25.78 7.56 0.80 2.58 2.45 6 7.31 3.48 44.57 23.78 14.56 1.32 2.96 2.02

On steep slopes, the survey results showed significant differ- than after Wutip (17.92%) (Table 1). At Station 4, the mean coral ences in typhoon damage to the coral ecology between each of cover of living coral was reduced from 16.32% to 13.22%, and bro- the three different depth transects (2 m, 6 m, 15 m) (Table 2). For ken corals were common in the 2 m transect (Fig. 5a). Adjacent to Stations 4 and 5 located on the steep slopes, at a depth of 2 m, a the transect some bleached corals were found (Fig. 5b). On the 6 m significant increase in dead coral cover was observed before and transects on steep slopes, a moderate decrease in living coral cover after the typhoon. The mean cover of living coral in the 2 m tran- was found after Wutip. Living coral at Station 5 decreased from sect at Station 5 before Wutip (24.54%) was significantly higher 12.16% to 9.61% (Table 1) of bottom cover (Fig. 6a); the damage left H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466 461

Table 2 Status of the reefs around the Yongle Atoll.

Station Depth Location Status of coral reefs Extent of (m) damage 1 2 Western side of Lingyang Reef (Steep Pocillopora spp. predominate. A few broken corals were found Slight 6slopes) Scraped coral appeared. Scars on living coral surfaces were occasionally found Slight 15 Reef rock predominate. Little damage to living coral Nil 2 2 Northern side of Lingyang Reef Sediment shifted horizontally. Overturned corals. Broken corals are common. Buried corals Severe (Passage of atoll) found 6 Mainly covered with reef rock and coral sand Nil 15 Living coral was scarce. Mainly covered with coral rubble and reef rock Nil 3 2 Southern side of Shanhu Island Large massive corals were dislodged. Broken corals were accumulated Severe 6(Passage of atoll) Coral rubble and reef rock predominated. Living coral were rare Nil 15 Little effects to benthic constituents. Living coral cover was low Nil 4 2 Northern side of Shanhu Island (Steep Some broken corals were found. A few foliose corals were damaged Moderate 6slopes) Scars on living coral surfaces were common. Coral bleaching appeared occasionally Moderate 15 Scars on living coral surfaces were common. Little dislodged coral Slight 5 2 Northern side of Quanfu Island (Steep Living coral cover was high. Broken branches coral were common. Overturned coral appeared Moderate 6slopes) Dislodged coral appeared occasionally. Broken coral predominated Moderate 15 Intact coral showed mainly minor damage. Scraped coral was common Slight 6 2 Eastern side of Quanfu Island (Gentle Living coral cover was the highest. Broken corals predominated. Dislodged occasionally Slight 6slopes) Broken and dislodged corals were mainly damaged types Slight 7 2 Western side of Quanfu Island Living coral cover was low. Damaged fragile branched coral Slight 6(Gentle slopes) Mainly damage with fragile branched Acroporidae Slight

DC 40 100 Other 30 LC 80 20 10 60 Sand 0 SC 40 20

0 Rubble Alage Intact coral Damaged coral Rock rao 54 46 (a) (b)

Fig. 3. Different percentage of the coral benthic components before and after typhoon Wutip at the Yongle Atoll in the 2 m transects at Stations 2 and 3. (a) Each spoke in the radar chart represents the relative contribution of benthic components. The data length of a spoke is the mean cover of the variable benthic components groups. The blue line represents pre-typhoon, and the red line represents post-typhoon. 1. DC, Dead scleractinia coral; 2. LC, Living scleractinia coral; 3. SC, Soft coral. (b) Damaged coral in proportion to intact coral.

5% dislodged

30% broken

20% bleaching 25% 5% minor damage

40% scrape

Fig. 4. Composite pie chart showing the different types of damaged scleractinia coral 2 m transects at Stations 2 and 3. Orange fraction showing minor injury includes minor damage and scrape. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

79% of coral intact (Fig. 6b), with moderate damage in the transect. 26.58% to 24.56% (Table 1). In the sites on steep slopes, the damage Most of these damage categories were minor damage and broken by the typhoon was confined to the shallower reef-flat (2 and 6 m), (Fig. 7). By contrast, the dead coral coverage increased from while in the deeper waters (15 m), damage to the corals was 2.84% to 4.45% (Table 1)(Fig. 6a). On the steep slopes, coral ecology because of overturned boulder and rubble that had been knocked in the 15 m transects was slightly disturbed by typhoon Wutip. The down from shallower zones. Except for these injured corals, no coverage of living coral at Station 4 only decreased only from other significant damage was observed in the 15 m transects. In 462 H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466

Fig. 5. Coral damage in the 2 m transect at Station 4. (a) Fragile branched coral was broken by strong wave or currents. (b) Bleached corals.

DC 80 100 Other 60 LC 80 40 20 60 Sand 0 SC 40 20 0 Rubble Alage Intact coral Damaged coral Rock rao 79 21 (a) (b)

Fig. 6. Different percentages of the coral benthic components before and after typhoon Wutip at the Yongle Atoll in the 6 m transects at Station 5. (a) Each spoke in the radar chart represents the variables the relative contribution of the benthic components groups. The data length of a spoke is the mean cover of the variable benthic components groups. The blue line represents pre-typhoon, red line represents post-typhoon. 1. DC, Dead scleractinia coral; 2. LC, Living scleractinia coral; 3. SC, Soft coral. (b) Damaged coral account for the proportion to intact coral. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

3%

dislodged

35% broken 30% 42% bleaching 12% minor damage

20% scrape

Fig. 7. Composite pie charts showing different types of damaged scleractinia coral (6 m transects at Station 5). Orange fraction showing minor injury includes minor damage and scrape. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) summary, at sites on steep slopes, damage was greatest at the 2 m sites, typhoon damage to coral reefs is often very patchy transect, and the damage decreased with depth. (Harmelin-Vivien, 1994; Woodley et al., 1981). Typhoon damage On low-angle slopes, all of the reef bottom coverage (i.e., living is difficult to predict because reef aspect, geographic location and coral, dead coral, rock, coral rubble and sand) varied homoge- seabed topography have a significant effect on the extent of dam- neously among the different depth transects. Living coral cover age (Bries et al., 2004; Fabricius et al., 2008; Harmelin-Vivien, in the 2 m transect at Station 6 declined by 4.52% during typhoon 1994). Some coral reefs that are far from a known typhoon track Wutip, from 34.54% in June to 30.02% (Table 1) in September, and may be heavily damaged by typhoons, e.g., the coral communities was damaged slightly, leaving 86.9% intact coral. Coverage by the at Kenting, Southern Taiwan Islands suffered coral fatality from living fixed benthos on the 6 m transect decreased by 3.34% during Typhoon Morakot in August 2009, which was a low-intensity the typhoon from 24.46% to 21.12% (Table 1), leaving 86.40% coral typhoon (Category 1 hurricane) with a path more than 200 km intact. The result showed that there were no significant variations from Kenting (Kuo et al., 2011). in damage to the coral ecology in with depth (Table 2). 6.1. Damage to the passage of the atoll 6. Discussion The comprehensive survey around the Yongle Atoll clearly indi- Coral reef geomorphological systems consist of a complex sub- cates the extent of typhoon influence. Damage was serious on 2 m- systems including widely varying geomorphology that are spatially depth transects at Stations 2 and 3, which were located in the pas- inhomogeneous. Hence, with distinct difference between adjacent sage of the atoll (Fig. 1c). The passage is a pathway that connects H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466 463

Fig. 8. Schematic diagram of the reef system showing steep reef profiles at Stations 4 and 5. Direct mechanical damage caused by waves or currents occurs in the shallow fore-reef area. The indirect damage of scraping coral colonies occurs by a rolling boulder or corals, particularly by globular and massive colonies. the lagoon and open sea water through the atoll reef rims. In gen- largely erosional in origin. Some grooves may always remain open eral in reef systems, passages between individual reefs result in a at both the landward and seaward ends, and thus act as blowholes reef chain, and this is a significant geomorphic characteristic of during typhoon events. Where severely damaged corals were the Yongle Atoll (Fig. 1c). The Polynesian word for deep and wide encountered, branches of unidirectional colonies that expand passages between reef islands is ava. Shallow and narrow passages toward and into and alongside grooves are normally smashed off are called hoa (Kench and McLean, 2004). Passages in the Yongle during a typhoon. However, branch colonies that are oriented Atoll are the former and are approximately are about 20–30 m shoreward away from the direction of the water flow are the least deep and hundreds of meters to kilometers wide and have steep damaged during a typhoon. Furthermore, in the shallow fore-reef slopes on either side. Passages are the most significant channels area, the high waves and strong currents forced by typhoons gen- for sea water exchange between the ocean and the lagoon. erated intense water movements, that have high rotational effects, Hence, strong currents are quite common in Stations 2 and 3 which and exhibit rapid changes in direction and intensity (Monismith are located in the passages of the atoll. Strong currents generated et al., 2013). Typhoon waves furiously break in the shallow zone, by winds, tides, eddies and gyres through passages close to coral generating a unidirectional shoreward current (Harmelin-Vivien, islands are regarded to be mechanical factors that cause sea water 1994). The strong water movements bring about an increase in fast movements (Kench and McLean, 2004; Madin and Connolly, the mechanical forces to cause lateral and vertical damage on the 2006; Wang, 2001), and that exert some stress to the benthic com- reef benthic community and substrate. Thus, the shallow fore-reef munity in the passage. Although strong currents with a certain area, the upper region of the outer slopes, become the principal damage power alone are not enough to induce such an extensive location of typhoon effects. Most analyses demonstrate that the influence (Hearn, 1999), the existence of such intensive current shallow reef benthic community and substrate often experience action with the addition of other factors, such as the typhoon in more severe damage from typhoon waves than those in deeper the passages, could have a conspicuous effect, especially in acting water. Most of the direct mechanical damages occur in 3–8 m shal- on benthic coral communities in shallow water. Typhoon-gener- low water zones. On the 15 m transects at Stations 4 and 5, almost ated currents that force water across passage surfaces may produce vertical steep slopes can experience low typhoon wave energy a vertical hydraulic gradient that affects coral reefs on the basis of because most of the energy is dissipated by the upper slopes depth so that severe damage occurred in the shallow zones (Hearn, (Monismith et al., 2013). Almost vertical slopes were less severely 1999; Page-Albins et al., 2012). Most of the overturned and dis- affected than slopes or level reef surfaces at West Rio Bueno, where lodged corals were relocated towards the current direction at the reef is vertical below a depth of 8 m; little damage was Stations 2 and 3. The current directions are essentially restrained observed in mostly foliaceous corals at depths of 10, 15, and by the geomorphology and therefore the exact current patterns 20 m compared with the overturning of the more massive corals are unique to each passage. observed at corresponding depths on the West Fore Reef slopes (Woodley et al., 1981). Hence, direct mechanical damage from typhoon waves is relatively rare. Indirect wave damage to coral 6.2. Impact on the steep slopes colonies may be a result of scraping by a rolling boulder or corals, particularly by globular and massive colonies that may tumble At Stations 4 and 5, the outer slopes can be subdivided into long distances from the upper reef slopes. Injury and damage to three adjacent geomorphologic units that are defined by this paper reef benthic communities and the substrate on these transects with regards to the slope angle, depth range, and physical environ- may result from those indirect effects, such as striking by rolling mental factors: (1) shallow fore-reef zone (2–8 m), (2) almost ver- massive coral, scraping by coral rubble at full speed and burying tical steep slopes (9–20 m) and (3) underwater platform (deeper under new coral sands from the upper slopes. than 15 m) (Fig. 8). Stations 4 and 5 have very steep windward margins with waves or surges having little relevant interaction with the benthic community perched in the steep slopes. The shal- 6.3. Effects on low-angle gentle slopes low fore-reef area frequently has spur and groove systems that are generally in parallel with the direction of the dominant waves, At Stations 6 and 7, where the substratum is slopes more gently where the wave energy is usually high (Gischler, 2010; Sheppard, (Fig. 9), the reef may build an extensive low angle slope extending 1981); on the Yongle Atoll, the spur and grooves systems are hundreds of meters offshore. In contrast to Stations 4 and 5, the 464 H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466

Fig. 9. Damage pattern on low-angle slopes at Stations 6 and 7. The wave energy induced by the typhoon was homogeneously attenuated along the gentle slopes, so that the extent of the typhoon effect is nearly the same at different depths. slopes appear to have sloped more gently towards the seaward side without steep slope transition. In any typhoon-affected area, Typhoon 70 the dissipation of wave damage depended on the conditions of Strong Typhoon the local reef geomorphology, including the slope angle, width 60 and depth (Monismith et al., 2013). A comparison of the pre- and Super Typhoon post-typhoon ratio of damaged to living coral along different 50 depths of transects indicates that the extent of typhoon effect is nearly the same in different places at each depth. It may also be 40 inferred that the wave energy induced by a typhoon is homoge- neously attenuated along the gentle slopes. In contrast to the situ- 30 ation on the steeper slopes reef, little or no rolling rubble or 20 massive coral debris from the upper slopes was found in deeper reef environments. Thus, avalanching of coral debris does not 10 appear on the gentle slopes (Harmelin-Vivien and Laboute, 1986; Vanwoesik et al., 1991). However, at these sites on Stations 6 0 and 7, which were completely located in the typhoon central path, Typhoon Strong Typhoon Super Typhoon where the wind was the most ferocious, except for occasionally Fig. 10. Frequency distribution of typhoons within 200 km of the Xisha Islands spectacular damage, the damage was amazingly limited. from 1945 to 2014 (typhoon best-track data from United States Navy Joint Typhoon Warning Center). 6.4. Increased risk to coral reefs on Xisha Islands

Recent successive catastrophic events such as Super (2013) and Rammasun (2014) have prompted scientists 25% to ask whether super strong tropical storms have been increasing since the beginning of the 21st century. Super typhoon Haiyan showed wind gusts of 315 km/h (195 mph), lasting up to one min- 1972-2004 ute (Robert, 2014), which made it the strongest tropical storm on 75% record to landfall in world meteorological history (Mori et al., 2005-2014 2014). The measured pressure of Super Typhoon Rammasun was 909 h Pa on 18 July, 2014 (data from CMA), making it the typhoon with the least amount of measured pressure to land on China since 1945. Several recent model predictions have shown that the fre- Fig. 11. Pie chart showing the proportion of super typhoons in two time periods, quency of global tropical storms could decrease with global warm- demonstrating the super typhoon increase in recent years. ing (IPCCAR5, 2013; Knutson et al., 2008). Some models also indicate that the frequency of super typhoon and category 4 and 5 hurricanes will increase dramatically by the end of the century 1 super typhoon occurred within 200 km of the Xisha Islands from (Bender et al., 2010; Holland and Bruyere, 2014; IPCCAR5, 2013). 1972 to 2004 (Fig. 11), but there were 3 super typhoons from 2005 Analysis of typhoons, that passed within 200 km of the Xisha to 2014 (Fig. 11). The IPCCAR5 report (2013) also shows an increase Islands from 1945 to 2014 (data from JTWC), shows that the fre- in the intensity and frequency of the strongest tropical storms quency of typhoons crossing the Xisha Island is high. Of these 98 since the 1970s in the Caribbean and Northwestern Pacific Ocean typhoons, on average 1.4 typhoons yr1 (typhoon, strong typhoon, regions (IPCCAR5, 2013). Consistent with the above studies, and super typhoon), the frequency of cyclones of categories from Emanuel (2005) also found that destructive tropical cyclones weak to strong was 65%, 26%, and 9%, respectively (Fig. 10). Only increased quickly over the past 30 years. If destructive tropical H. Yang et al. / Journal of Asian Earth Sciences 114 (2015) 457–466 465 storms (super typhoon or category 4 and 5 hurricanes) directly Done, T.J., 1992. Effects of tropical cyclone waves on ecological and struck coral reefs, damage to scleractinian corals would be very geomorphological structures on the Great-Barrier-Reef. Continental Shelf Res. 12, 859–872. high (Bries et al., 2004; Fabricius et al., 2008; Woodley et al., Emanuel, K., 2005. Increasing destructiveness of tropical cyclones over the past 30 1981). Fortunately, records do not show that the Xisha Islands have years. Nature 436, 686–688. experienced a direct attack by a super typhoon. With global warm- Fabricius, K.E., De’ath, G., Puotinen, M.L., Done, T., Cooper, T.F., Burgess, S.C., 2008. Disturbance gradients on inshore and offshore coral reefs caused by a severe ing, the risk of a super typhoon directly hitting the Xisha Islands tropical cyclone. Limnol. Oceanography 53, 690–704. could be greatly increased in the future. Gardner, T.A., Cote, I.M., Gill, J.A., Grant, A., Watkinson, A.R., 2005. Hurricanes and caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86, 174–184. 7. Conclusions Gischler, E., 2010. Indo-pacific and Atlantic spurs and grooves revisited: the possible effects of different Holocene sea-level history, exposure, and reef accretion rate in the shallow fore reef. Facies 56, 173–177. 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