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Impacts of human activities on coral reef ecosystems of southern Taiwan: A long-term study
Marine Pollution Bulletin 64 (2012) 1129–1135
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Impacts of human activities on coral reef ecosystems of southern Taiwan: A long-term study Pi-Jen Liu a,b, Pei-Jie Meng a,b,⇑, Li-Lian Liu c, Jih-Terng Wang d, Ming-Yih Leu a,b,⇑ a
National Museum of Marine Biology and Aquarium, Checheng, Pingtung 944, Taiwan Graduate Institute of Marine Biodiversity and Evolutionary Biology, National Dong Hwa University, Checheng, Pingtung 944, Taiwan c Institute of Marine Biology and Asia-Pacific Ocean Research Center-Kuroshio Research Group, National Sun Yat-Sen University, Kaohsiung 80424, Taiwan d Tajen University, Pingtung 907, Taiwan b
a r t i c l e
i n f o
Keywords: Anthropogenic impact Coral reef Kenting National Park Long-Term Ecological Research (LTER) Seawater quality Taiwan
a b s t r a c t In July 2001, the National Museum of Marine Biology and Aquarium, co-sponsored by the Kenting National Park Headquarters and Taiwan’s National Science Council, launched a Long-Term Ecological Research (LTER) program to monitor anthropogenic impacts on the ecosystems of southern Taiwan, specifically the coral reefs of Kenting National Park (KNP), which are facing an increasing amount of anthropogenic pressure. We found that the seawater of the reef flats along Nanwan Bay, Taiwan’s southernmost embayment, was polluted by sewage discharge at certain monitoring stations. Furthermore, the consequently higher nutrient and suspended sediment levels had led to algal blooms and sediment smothering of shallow water corals at some sampling sites. Finally, our results show that, in addition to this influx of anthropogenically-derived sewage, increasing tourist numbers are correlated with decreasing shallow water coral cover, highlighting the urgency of a more proactive management plan for KNP’s coral reefs. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction The coral reefs of Kenting National Park (KNP) are characterized by a biodiversity that is among the highest of Taiwan’s marine environments, and, as such, the park, which also includes an extensive terrestrial component (sea and land areas are 15,206 and 18,084 ha, respectively), is justifiably popular among both domestic and international tourists. However, increasing tourist numbers threaten to place an excessive burden on the natural environment by way of increasing coastal development, fisheries activities, sewage and other pollutant discharge, and consequent eutrophication (Meng et al., 2007a,b, 2008). Physical disturbance by typhoons (Ault and Johnson, 1998; Jan et al., 2001; Kaufman, 1983; Kuo et al., 2011; Lassig, 1983; Letourneur, 1996; Mah and Stern, 1986), coral disease outbreaks (Liao et al., 2007), coral bleaching episodes, sea anemone outbreaks (Hung et al., 1998), sedimentation, habitat modification (Fabricius, 2005; Rogers, 1990; Sakai and Nishihira, 1991; Slam and Clark, 1982; Wittenberg and Hunte, 1992), ship wrecks and the accompanying oil pollution (Fingas, 2001; Jan et al., 1994), overfishing and illegal fishing (Polunin and Roberts, 1996), and snorkeling-induced coral destruction (Meng et al., 2007a,b) have also contributed to the deterioration of KNP’s coral ⇑ Corresponding authors. Tel.: +886 8 8825034; fax: +886 8 8825066 (P.-J. Meng), tel.: +886 8 8825385; fax: +886 8 8825066 (M.-Y. Leu). E-mail addresses: [email protected] (P.-J. Meng), [email protected] (M.-Y. Leu). 0025-326X/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2012.03.031
reef ecosystems. Furthermore, the thermal effluent of Taiwan’s ‘‘Maanshan’’ Nuclear Power Plant is released into a small bay that is also popular with tourists, and, given the poor swimming skills of the majority of these snorkelers, who inadvertently destroy coral through direct physical impact by standing on them or breaking them with their fins, the corals of this bay, the ‘‘Outlet,’’ are particularly threatened. Collectively, the coral reefs of KNP are under assault from a variety of both natural and anthropogenic impacts, a fact that has received surprisingly little attention. Recently, the increase in the average Taiwanese standard of living has created a demand for leisure activities that is unparalleled in Taiwan’s history. Tourists are more and more frequently taking a brief holiday, which has resulted in increased pressure to local terrestrial and coastal environments (Meng et al., 2006, 2007a,b, 2008). In addition, the ‘‘Chichi’’ earthquake on September 21, 1999 in Nantou, Taiwan, which was the largest natural disaster in Taiwan in over a century, damaged many scenic areas in central Taiwan. Consequently, tourists chose, instead, to visit the nonimpacted KNP, and tourist numbers have been on a steady rise since that point. This in turn has led to an increase in domestic sewage, and these potentially untreated municipal wastes are often dumped directly into the nearby creeks and rivers. The excessive nutrients from the sewage, which also includes chemical fertilizers and pesticides used in local agriculture, eventually discharge into coastal waters during periods of heavy rainfall. Nanwan Bay, the southernmost bay of Taiwan, is also characterized by excessive suspended sediments during these heavy rains.
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(Meng et al., 2008), and these sediments could bury corals and other benthic organisms (Bastidas et al., 1999; Riegl et al., 1996; Thomas and Ridd, 2005; Thomas et al., 2003). Furthermore, high levels of nutrient and sediment loadings along the coast creates further challenges for these coral reef ecosystems (Hodgson, 1990; Riegl and Branch, 1995; Rosemond et al., 2002; Umar et al., 1998). To prevent continual degradation of the coral reef environment, it is important to take a composite look at the potential factors that may cause harm to this fragile ecosystem (Fabricius et al., 2005; Wang et al., 2008). Herein, we introduce the impacts of human activities on the coral reef ecosystems of KNP as documented by a long-term marine environmental monitoring program, with a special emphasis on water quality and the impact of increasing tourism, in order to draw greater attention to such threats. 2. Materials and methods 2.1. Sampling techniques Seawater samples were taken from 23 collection sites around Nanwan Bay from 2001 to 2008. The exact location of the sampling sites was recorded with GPS (Fig. 1). Quality control (QC) for sampling equipment and field measurement procedures, including those for temperature, salinity, pH, and dissolved oxygen (DO), were conducted in situ following government QA/QC regulations (Meng et al., 2008). The remaining water samples were preserved at 4 °C and returned to the laboratory for analysis of the following parameters: pH, five days of biochemical oxygen demand (BOD5), nutrients (nitrite, nitrate and phosphate, ammonia) chlorophyll-a, suspended solids, and turbidity. 2.1.1. Analysis of water quality The measurements of temperature and salinity were carried out in situ with a CTD (conductivity, temperature, and depth [pressure]) instrument (Sea-Bird Electronics Model 19 plus) on the research vessel Ocean Research III and/or by the EPA/ROC (Taipei) technique on fishing boats. The precision for temperature was ±0.05 °C and the accuracy and precision for salinity were ±0.003 and ±0.023 psu, respectively. DO was measured by the Winkler method with an accuracy of ±0.04 mg/L and a precision of ±1.2%. The precision and accuracy (recovery of a spiked glucose standard) of BOD (five days) measurements were ±2.38% and 98.3 ± 7.7%, respectively, and the values were subsequently checked with the control chart.
Fig. 1. Locations of sampling sites along the coast of Kenting National Park. The dotted line indicates the boundary of Kenting National Park.
(Tourists in the morning + tourists in the afternoon)/2 (weekend days and holidays in the month) = A (Tourists in the morning + tourists in the afternoon)/2 (weekdays) = B A + B = recreational density. 2.1.4. Analysis of coral and macroalgae cover Coral and macroalgae cover were estimated sensu Tkachenko et al. (2007). Briefly, coral and macroalgae surveys were conducted at 24 popular snorkeling sites by the line intercept transect method (Fig. 1). The 50 m transect line was laid perpendicular to the shore, from the first appearance of coral to 2 m depth. We counted the length (in cm) of the transect tape covering coral colonies and macroalgae and then recorded the shape of a coral colony every 5 m. 2.1.5. Statistical analysis Data are presented as mean ± standard error (or, in some cases, standard deviation), and individual means were analyzed with student’s t-tests with an a = 0.05. 3. Results and discussion 3.1. Water quality parameters
2.1.2. Analysis of nutrients and ammonium Immediately after collection, water samples were stored in a cooler at 4 °C and returned to the laboratory for analysis of ammonia and nutrients. A Flow Injection Analyzer (FIA) and spectrophotometer (Hitachi model U-3000) were used to conduct analysis of ammonia, nitrate, nitrite, phosphate and silicate (Pai and Riley, 1994; Pai and Yang, 1990a,b; Pai et al., 2001). 2.1.3. Analysis of tourist density Ten coastal recreational activities at 17 stations were surveyed, and observational data were collected. These activities were skin diving, scuba diving, beach activities, personal watercraft (PWC), boating, jet boating, surfing, sightseeing, swimming, and fishing. Two weekdays and two weekend days were surveyed every month to estimate the number of tourists partaking in each activity. Researchers quantified the number of tourists engaging in each activity in the morning and afternoon on the surveyed day (Meng et al., 2007a). The recreational density of a certain activity at each station was calculated as follows:
We analyzed temperature, salinity, pH, DO, BOD, suspended solid levels, turbidity, and chlorophyll-a, nutrient, and ammonia concentrations along the coast of Nanwan Bay from 2001 to 2008 (Table 1). In general, high standard errors, indicative of unstable water quality, were documented at stations near creeks and rivers (S1, S16, S17, S19, and S26). Conversely, small standard errors, indicative of more stable water quality, were recorded at stations located a greater distance from the outlets of freshwater. Low levels of salinity, pH, and DO were observed along with high levels of nutrients (nitrite, nitrate, ammonia and phosphate), BOD, turbidity, suspended solids, and chlorophyll-a in the water around the coastal areas near the outlets of channels or creeks. While the episodic upwelling that characterizes Nanwan Bay (Chen et al., 2004, 2005) could have driven some of the observed spatiotemporal variation in these water quality parameters, freshwater input from heavy rains may have caused the high nutrient levels measured near estuary stations (Meng et al., 2008), particularly those near river outlets, such as S1, S26 and S16. Normally, the
Table 1 Seawater quality (mean ± SE) at 27 stations along the coast of Nanwan Bay from 2001 to 2008. Temp. (°C)
Salinity (psu)
pH
DO (o/o)
BOD5 (mg/L)
NO2–N (mg/L)
NO3–N (mg/L)
NH3–N (mg/L)
PO4–P (mg/L)
SiO2 (mg/L)
SS (mg/L)
Turbidity (ntu)
Chl.a (lg/L)
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15 S16 S17 S18 S19 S20 S21 S22 S23 S24 S25 S26 S27
27.08 ± 0.46 28.12 ± 0.39 28.39 ± 0.38 28.08 ± 0.31 28.01 ± 0.32 28.30 ± 0.36 29.17 ± 0.35 29.24 ± 0.51 28.89 ± 0.38 28.45 ± 0.34 29.43 ± 0.60 29.42 ± 0.70 29.55 ± 0.47 29.88 ± 0.49 29.13 ± 0.46 28.59 ± 0.45 28.97 ± 0.59 28.44 ± 0.53 29.24 ± 0.54 28.64 ± 0.37 28.01 ± 0.32 28.28 ± 0.32 27.91 ± 0.32 28.28 ± 0.45 27.83 ± 0.32 28.66 ± 0.46 27.48 ± 0.31
12.46 ± 1.45 32.44 ± 0.23 33.53 ± 0.20 33.92 ± 0.09 33.75 ± 0.14 32.49 ± 0.58 33.61 ± 0.11 31.80 ± 0.81 34.07 ± 0.08 33.65 ± 0.12 33.17 ± 0.31 33.23 ± 0.64 33.65 ± 0.18 33.04 ± 0.78 33.68 ± 0.19 6.29 ± 1.15 2.15 ± 0.72 30.80 ± 0.96 0.86 ± 0.14 31.92 ± 0.52 33.53 ± 0.14 31.25 ± 0.40 33.47 ± 0.17 33.71 ± 0.14 32.32 ± 0.59 2.55 ± 0.98 33.66 ± 0.20
7.98 ± 0.03 8.29 ± 0.02 8.42 ± 0.02 8.27 ± 0.02 8.25 ± 0.01 8.35 ± 0.02 8.38 ± 0.02 8.18 ± 0.03 8.24 ± 0.02 8.28 ± 0.02 8.31 ± 0.04 8.25 ± 0.03 8.27 ± 0.03 8.28 ± 0.02 8.28 ± 0.03 8.40 ± 0.05 7.77 ± 0.05 8.20 ± 0.04 8.04 ± 0.03 8.19 ± 0.02 8.24 ± 0.02 8.32 ± 0.02 8.30 ± 0.02 8.20 ± 0.03 8.22 ± 0.01 8.38 ± 0.03 8.26 ± 0.02
89.8 ± 2.4 125.8 ± 2.9 142.9 ± 3.2 105.1 ± 2.2 101.1 ± 0.7 110.6 ± 1.8 129.4 ± 3.0 107.0 ± 2.9 98.4 ± 0.9 107.9 ± 1.6 125.5 ± 6.7 130.2 ± 10.5 121.3 ± 5.8 126.7 ± 4.4 109.6 ± 3.4 123.8 ± 4.8 82.2 ± 9.0 102.9 ± 3.5 93.7 ± 4.1 97.0 ± 0.7 102.9 ± 1.1 120.6 ± 2.3 110.4 ± 1.6 97.7 ± 2.0 96.6 ± 0.6 111.2 ± 2.6 102.7 ± 1.5
3.6 ± 0.4 1.3 ± 0.1 1.1 ± 0.1 1.1 ± 0.1 1.2 ± 0.1 1.3 ± 0.1 0.9 ± 0.1 1.3 ± 0.1 1.0 ± 0.1 1.1 ± 0.1 1.1 ± 0.1 1.2 ± 0.3 1.1 ± 0.1 1.0 ± 0.1 1.0 ± 0.1 3.6 ± 0.5 11.0 ± 2.2 1.6 ± 0.2 5.9 ± 1.2 1.4 ± 0.1 1.0 ± 0.1 0.9 ± 0.1 1.0 ± 0.1 1.1 ± 0.1 1.3 ± 0.1 2.3 ± 0.4 1.0 ± 0.1
0.079 ± 0.008 0.007 ± 0.004 0.002 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.004 ± 0.002 0.001 ± 0.000 0.004 ± 0.001 0.002 ± 0.000 0.001 ± 0.000 0.002 ± 0.001 0.003 ± 0.001 0.002 ± 0.000 0.001 ± 0.000 0.002 ± 0.001 0.284 ± 0.056 0.069 ± 0.015 0.007 ± 0.002 0.194 ± 0.039 0.009 ± 0.002 0.002 ± 0.000 0.002 ± 0.000 0.001 ± 0.000 0.003 ± 0.000 0.001 ± 0.000 0.003 ± 0.000 0.001 ± 0.000
0.313 ± 0.043 0.053 ± 0.009 0.035 ± 0.007 0.029 ± 0.005 0.039 ± 0.008 0.095 ± 0.035 0.027 ± 0.005 0.071 ± 0.020 0.035 ± 0.009 0.031 ± 0.007 0.021 ± 0.011 0.023 ± 0.011 0.014 ± 0.004 0.049 ± 0.038 0.011 ± 0.002 0.446 ± 0.120 0.429 ± 0.217 0.084 ± 0.021 0.511 ± 0.179 0.057 ± 0.010 0.057 ± 0.009 0.100 ± 0.011 0.052 ± 0.010 0.054 ± 0.014 0.032 ± 0.006 0.181 ± 0.091 0.033 ± 0.007
0.370 ± 0.050 0.063 ± 0.021 0.032 ± 0.003 0.057 ± 0.016 0.036 ± 0.004 0.041 ± 0.005 0.048 ± 0.016 0.023 ± 0.005 0.037 ± 0.005 0.046 ± 0.011 0.014 ± 0.002 0.012 ± 0.004 0.014 ± 0.003 0.011 ± 0.002 0.012 ± 0.003 2.978 ± 0.484 1.460 ± 0.491 0.302 ± 0.141 3.068 ± 0.504 0.158 ± 0.029 0.040 ± 0.006 0.034 ± 0.004 0.036 ± 0.005 0.017 ± 0.003 0.042 ± 0.006 0.049 ± 0.009 0.039 ± 0.005
0.042 ± 0.013 0.009 ± 0.003 0.003 ± 0.001 0.002 ± 0.001 0.002 ± 0.001 0.005 ± 0.002 0.003 ± 0.001 0.004 ± 0.002 0.005 ± 0.002 0.003 ± 0.001 0.001 ± 0.001 0.001 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.210 ± 0.049 0.148 ± 0.048 0.007 ± 0.002 0.774 ± 0.101 0.026 ± 0.005 0.006 ± 0.001 0.006 ± 0.001 0.008 ± 0.003 0.002 ± 0.000 0.004 ± 0.001 0.006 ± 0.001 0.011 ± 0.009
4.10 ± 0.80 0.40 ± 0.08 0.14 ± 0.02 0.08 ± 0.01 0.11 ± 0.02 0.32 ± 0.10 0.16 ± 0.04 0.44 ± 0.08 0.10 ± 0.01 0.14 ± 0.02 0.13 ± 0.01 0.15 ± 0.08 0.07 ± 0.01 0.16 ± 0.10 0.67 ± 0.59 1.54 ± 0.25 4.76 ± 0.31 0.60 ± 0.14 4.83 ± 0.24 0.39 ± 0.08 0.14 ± 0.01 0.44 ± 0.05 0.13 ± 0.02 0.09 ± 0.01 0.28 ± 0.07 4.68 ± 0.23 0.18 ± 0.05
578.0 ± 280.0 12.2 ± 2.0 7.8 ± 0.7 6.9 ± 0.4 13.9 ± 4.6 7.6 ± 0.4 7.4 ± 0.4 32.1 ± 6.0 7.4 ± 0.4 18.0 ± 2.7 19.9 ± 4.5 13.6 ± 2.8 7.7 ± 0.6 6.4 ± 0.5 10.0 ± 1.9 74.8 ± 27.0 102.8 ± 59.0 30.5 ± 10.7 402 ± 333.0 40.5 ± 6.2 9.0 ± 0.7 7.1 ± 0.3 6.7 ± 0.5 6.5 ± 0.8 67.5 ± 2.0 136.7 ± 46.7 12.6 ± 5.1
249.0 ± 115.0 3.3 ± 0.8 1.5 ± 0.3 1.1 ± 0.1 4.2 ± 1.9 1.4 ± 0.2 1.3 ± 0.2 13.3 ± 2.9 1.4 ± 0.2 5.7 ± 1.1 5.8 ± 1.2 4.3 ± 1.2 2.0 ± 0.3 0.8 ± 0.1 2.4 ± 0.8 36.8 ± 13.9 46.5 ± 24.2 13.7 ± 5.9 174.0 ± 136.0 15.6 ± 2.6 2.0 ± 0.3 1.3 ± 0.1 1.1 ± 0.2 1.1 ± 0.3 26.1 ± 8.9 63.3 ± 20.1 3.4 ± 2.1
2.78 ± 0.57 0.25 ± 0.03 0.15 ± 0.01 0.16 ± 0.02 0.17 ± 0.02 0.30 ± 0.04 0.13 ± 0.01 0.39 ± 0.12 0.11 ± 0.02 0.30 ± 0.04 0.43 ± 0.14 0.36 ± 0.15 0.18 ± 0.03 0.34 ± 0.14 0.37 ± 0.12 5.33 ± 2.12 5.47 ± 2.92 0.46 ± 0.09 0.83 ± 0.27 0.42 ± 0.06 0.18 ± 0.04 0.25 ± 0.06 0.19 ± 0.03 0.11 ± 0.02 0.24 ± 0.04 0.36 ± 0.06 0.18 ± 0.02
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Station
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Fig. 2. The recreational densities (expressed as percentages of the average values) observed along the coast of Kenting National Park. PWC, personal watercraft.
park’s peak tourist season. Consequently, high levels of nutrients, BOD5, suspended solids, and turbidity were found in the water collected along the KNP effluent area, such as the heavily visited S20 coastline. Compared to the other stations, significantly higher nutrient, BOD5, turbidity, and chlorophyll-a levels were found in water sampled at site S16, which is located near the confluence of Shir-Neou stream with Nanwan Bay. Anthropogenic nutrient enrichment can stimulate algal blooms (Fabricius et al., 2005; Lapointe et al., 2004), and, in February 2002, we found the first incidence of a ‘‘green tide’’ caused by nutrient pollution along the S16 coastal area, which receives freshwater input from Shir-Neou stream. The chlorophyll-a content of phytoplankton in the water was extremely high, 339 and 15.3 lg/L in February 2002 and May 2002, respectively.
Fig. 3. Average numbers of tourists (expressed as monthly means ± standard error) at the different stations along the coast of Kenting National Park.
3.2. Recreational densities around Kenting National Park Common recreational activities along the coast of KNP include skin diving, SCUBA diving, beach activities, personal watercraft activities, ‘‘banana’’ boating, jet boating, surfing, sightseeing cruises, swimming, and fishing (Meng et al., 2007a). The recrea-
Fig. 4. Total number of tourists observed monthly along the coast of Kenting National Park from 2001 to 2008.
rainy season in the Hengchun Peninsula of Taiwan, in which KNP is located, is from May to September, and this coincides with the
Fig. 5. The average number of skin divers (±standard error) at the different stations of Kenting National Park from 2002 to 2008.
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3.3. The relationship between water quality and macroalgal cover Accumulation of nutrients varied across seasons in this study. For instance, higher nutrient levels tended to accumulate in the river water and sediments during the dry season, becoming diluted by rainwater in the summer monsoon season. Consequently, algal blooms occurred almost every year during the dry seasons, except for the times in which typhoons occurred during the dry season, in which case no algal blooms occurred. There were significant positive correlations between nitrite, phosphate, and ammonia concentrations and macroalgal cover (r2 = 0.94, 0.89, 0.58, respectively, n = 5, p < 0.01). As we mentioned before, an increase in domestic wastewaters, which carry excessive nutrients, flows into Nanwan Bay without being treated in the wet season or following rains, leading to increases in macroalgal cover (Liu et al., 2009). This has also been shown in field experiments on the Great Barrier Reef (Fabricius et al., 2005) and South Florida (Lapointe et al., 2004). Fig. 6. Coral cover of reef flats at different stations along the coast of Kenting National Park.
tional densities (expressed as percentages of the averages) observed along the coast of KNP (Fig. 2) indicate that, of the 10 types of coastal activities observed, most tourists prefer beach activities, skin diving, and swimming during their vacations. While the numbers of tourists varied from station to station and between years (Fig. 3), the results indicate that S10, S7, and S20 were the preferred coastal recreational areas. The peak season for tourism was from June to September in all years sampled (Fig. 4). The peak number of skin divers was also documented during this period (Fig. 5), and the preferred snorkeling sites were S7, S21, and S22.
3.4. The relationship between water quality and coral cover Coral cover of the reef flats at the different stations was variable (Fig. 6). The average coral cover along the coast of KNP was approximately 30% and ranged from 5.6% to 60.0%. The correlations between nitrite, phosphate, ammonia, macroalgal cover, and suspended solid concentrations and coral cover were negative and statistically significant (Fig. 7, r2 = 0.25, 0.26, 0.36, 0.65, 0.28, respectively, n = 16, p < 0.05). Effects of water quality deterioration (e.g., sedimentation, thermal stress, and eutrophication) on coral reef ecosystems have been widely studied (Bruno et al., 2007; Crossland et al., 1984; Gilmour, 1999; James et al., 2005; Liao et al., 2007; Manzello et al., 2007; Miller and Cruise, 1995; Nugues and Roberts, 2003; Thomas and Ridd, 2005; Thomas et al., 2003;
Fig. 7. The correlations between levels of nitrite, phosphate, ammonia, macroalgal cover, and suspended solids and coral cover.
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Woolfe and Larcombe, 1999) and suggest that an increase in domestic wastewater, which carries excessive nutrients, may have led to the observed increases in macroalgal cover (Liu et al., 2009). As macroalgae compete with coral for the same substrate (Liu et al., 2009), macroalgal cover typically increases when coral cover decreases. 3.5. The relationship between numbers of tourists and coral cover The inverse relationship between numbers of skin divers and coral cover (r2 = 0.62, n = 24, p < 0.01) suggests that skin divers have negatively influenced the survival of shallow water corals due to physical destruction. In fact, tourists and skin diver numbers show a positive correlation with algal cover. When divers step carelessly on or collect coral colonies, they cause the destruction of both the colony and the associated habitat, which is used by a plethora of other organisms (Meng et al., 2007a). In sum, our results confirm that increasing numbers of tourists and skin divers were one of the dominant factors that led to the drop in coral cover (Ho et al., 2011). 4. Conclusions Most of the coral reefs in Taiwan are fringing reefs that are located in shallow areas near the coast; hence they are readily influenced by human activities (Dai, 1988, 1991a,b, 1993, 1996; Yang, 1985). Coral reef ecosystems are interconnected given the lack of significant barriers to water flow in marine environments, and so if point-source pollution is documented at one site, it is possible that its detrimental influence may spread. For example, improper stabilization of a hill near KNP has resulted in a local increase in seawater turbidity. Furthermore, tourists produce a great deal of both trash and sewage, the latter of which migrates to coastal waters after heavy rains. This turbid, nutrient-rich water has led to increases in algal cover in shallow areas previously occupied by corals and other invertebrates (Meng et al., 2007a,b, 2008). On the other hand, physical disturbances caused by snorkelers and divers, such as inadvertent contact with coral, during July–August summer vacations may have had as great an impact as the decreased seawater quality. In summary, the water quality of the reef flats of KNP has been deteriorating since 2001 and requires greater attention (Chang et al., 2008). Our results show that increasing numbers of tourists, suspended solids, nutrients, and ammonia were the dominant factors leading to the decline in coral cover. We urge continued research on both potential sources of degradation, as was done herein, and the ability of corals to recover to such disturbances. Acknowledgements This study was financially supported by Grants from the National Science Council of Taiwan (NSC 97-2621-B-291-002-MY3; NSC95-2621-B-291-003; NSC 94-2621-B-291-003; NSC 93-2621B-291-001; NSC 92-2621-B-291-004) and the Headquarters of the Kenting National Park to P.J.M. We would like to thank Anderson Mayfield for critical comments on the manuscript as well as a thorough proofreading of the English. References Ault, T.R., Johnson, C.R., 1998. Spatially and temporally predictable fish communities on coral reefs. Ecol. Monogr. 68, 25–50. Bastidas, C., Bone, D., Garcia, E.M., 1999. Sedimentation rates and metal content of sediments in a Venezuelan coral reef. Mar. Pollut. Bull. 38 (1), 16–24. Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D., Sweatman, H., Melendy, A.M., 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5 (6), e124.
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Impacts of human activities on coral reef ecosystems of southern Taiwan: A long-term study Pi-Jen Liu a,b, Pei-Jie Meng a,b,⇑, Li-Lian Liu c, Jih-Terng Wang d, Ming-Yih Leu a,b,⇑ a
National Museum of Marine Biology and Aquarium, Checheng, Pingtung 944, Taiwan Graduate Institute of Marine Biodiversity and Evolutionary Biology, National Dong Hwa University, Checheng, Pingtung 944, Taiwan c Institute of Marine Biology and Asia-Pacific Ocean Research Center-Kuroshio Research Group, National Sun Yat-Sen University, Kaohsiung 80424, Taiwan d Tajen University, Pingtung 907, Taiwan b
a r t i c l e
i n f o
Keywords: Anthropogenic impact Coral reef Kenting National Park Long-Term Ecological Research (LTER) Seawater quality Taiwan
a b s t r a c t In July 2001, the National Museum of Marine Biology and Aquarium, co-sponsored by the Kenting National Park Headquarters and Taiwan’s National Science Council, launched a Long-Term Ecological Research (LTER) program to monitor anthropogenic impacts on the ecosystems of southern Taiwan, specifically the coral reefs of Kenting National Park (KNP), which are facing an increasing amount of anthropogenic pressure. We found that the seawater of the reef flats along Nanwan Bay, Taiwan’s southernmost embayment, was polluted by sewage discharge at certain monitoring stations. Furthermore, the consequently higher nutrient and suspended sediment levels had led to algal blooms and sediment smothering of shallow water corals at some sampling sites. Finally, our results show that, in addition to this influx of anthropogenically-derived sewage, increasing tourist numbers are correlated with decreasing shallow water coral cover, highlighting the urgency of a more proactive management plan for KNP’s coral reefs. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction The coral reefs of Kenting National Park (KNP) are characterized by a biodiversity that is among the highest of Taiwan’s marine environments, and, as such, the park, which also includes an extensive terrestrial component (sea and land areas are 15,206 and 18,084 ha, respectively), is justifiably popular among both domestic and international tourists. However, increasing tourist numbers threaten to place an excessive burden on the natural environment by way of increasing coastal development, fisheries activities, sewage and other pollutant discharge, and consequent eutrophication (Meng et al., 2007a,b, 2008). Physical disturbance by typhoons (Ault and Johnson, 1998; Jan et al., 2001; Kaufman, 1983; Kuo et al., 2011; Lassig, 1983; Letourneur, 1996; Mah and Stern, 1986), coral disease outbreaks (Liao et al., 2007), coral bleaching episodes, sea anemone outbreaks (Hung et al., 1998), sedimentation, habitat modification (Fabricius, 2005; Rogers, 1990; Sakai and Nishihira, 1991; Slam and Clark, 1982; Wittenberg and Hunte, 1992), ship wrecks and the accompanying oil pollution (Fingas, 2001; Jan et al., 1994), overfishing and illegal fishing (Polunin and Roberts, 1996), and snorkeling-induced coral destruction (Meng et al., 2007a,b) have also contributed to the deterioration of KNP’s coral ⇑ Corresponding authors. Tel.: +886 8 8825034; fax: +886 8 8825066 (P.-J. Meng), tel.: +886 8 8825385; fax: +886 8 8825066 (M.-Y. Leu). E-mail addresses: [email protected] (P.-J. Meng), [email protected] (M.-Y. Leu). 0025-326X/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2012.03.031
reef ecosystems. Furthermore, the thermal effluent of Taiwan’s ‘‘Maanshan’’ Nuclear Power Plant is released into a small bay that is also popular with tourists, and, given the poor swimming skills of the majority of these snorkelers, who inadvertently destroy coral through direct physical impact by standing on them or breaking them with their fins, the corals of this bay, the ‘‘Outlet,’’ are particularly threatened. Collectively, the coral reefs of KNP are under assault from a variety of both natural and anthropogenic impacts, a fact that has received surprisingly little attention. Recently, the increase in the average Taiwanese standard of living has created a demand for leisure activities that is unparalleled in Taiwan’s history. Tourists are more and more frequently taking a brief holiday, which has resulted in increased pressure to local terrestrial and coastal environments (Meng et al., 2006, 2007a,b, 2008). In addition, the ‘‘Chichi’’ earthquake on September 21, 1999 in Nantou, Taiwan, which was the largest natural disaster in Taiwan in over a century, damaged many scenic areas in central Taiwan. Consequently, tourists chose, instead, to visit the nonimpacted KNP, and tourist numbers have been on a steady rise since that point. This in turn has led to an increase in domestic sewage, and these potentially untreated municipal wastes are often dumped directly into the nearby creeks and rivers. The excessive nutrients from the sewage, which also includes chemical fertilizers and pesticides used in local agriculture, eventually discharge into coastal waters during periods of heavy rainfall. Nanwan Bay, the southernmost bay of Taiwan, is also characterized by excessive suspended sediments during these heavy rains.
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(Meng et al., 2008), and these sediments could bury corals and other benthic organisms (Bastidas et al., 1999; Riegl et al., 1996; Thomas and Ridd, 2005; Thomas et al., 2003). Furthermore, high levels of nutrient and sediment loadings along the coast creates further challenges for these coral reef ecosystems (Hodgson, 1990; Riegl and Branch, 1995; Rosemond et al., 2002; Umar et al., 1998). To prevent continual degradation of the coral reef environment, it is important to take a composite look at the potential factors that may cause harm to this fragile ecosystem (Fabricius et al., 2005; Wang et al., 2008). Herein, we introduce the impacts of human activities on the coral reef ecosystems of KNP as documented by a long-term marine environmental monitoring program, with a special emphasis on water quality and the impact of increasing tourism, in order to draw greater attention to such threats. 2. Materials and methods 2.1. Sampling techniques Seawater samples were taken from 23 collection sites around Nanwan Bay from 2001 to 2008. The exact location of the sampling sites was recorded with GPS (Fig. 1). Quality control (QC) for sampling equipment and field measurement procedures, including those for temperature, salinity, pH, and dissolved oxygen (DO), were conducted in situ following government QA/QC regulations (Meng et al., 2008). The remaining water samples were preserved at 4 °C and returned to the laboratory for analysis of the following parameters: pH, five days of biochemical oxygen demand (BOD5), nutrients (nitrite, nitrate and phosphate, ammonia) chlorophyll-a, suspended solids, and turbidity. 2.1.1. Analysis of water quality The measurements of temperature and salinity were carried out in situ with a CTD (conductivity, temperature, and depth [pressure]) instrument (Sea-Bird Electronics Model 19 plus) on the research vessel Ocean Research III and/or by the EPA/ROC (Taipei) technique on fishing boats. The precision for temperature was ±0.05 °C and the accuracy and precision for salinity were ±0.003 and ±0.023 psu, respectively. DO was measured by the Winkler method with an accuracy of ±0.04 mg/L and a precision of ±1.2%. The precision and accuracy (recovery of a spiked glucose standard) of BOD (five days) measurements were ±2.38% and 98.3 ± 7.7%, respectively, and the values were subsequently checked with the control chart.
Fig. 1. Locations of sampling sites along the coast of Kenting National Park. The dotted line indicates the boundary of Kenting National Park.
(Tourists in the morning + tourists in the afternoon)/2 (weekend days and holidays in the month) = A (Tourists in the morning + tourists in the afternoon)/2 (weekdays) = B A + B = recreational density. 2.1.4. Analysis of coral and macroalgae cover Coral and macroalgae cover were estimated sensu Tkachenko et al. (2007). Briefly, coral and macroalgae surveys were conducted at 24 popular snorkeling sites by the line intercept transect method (Fig. 1). The 50 m transect line was laid perpendicular to the shore, from the first appearance of coral to 2 m depth. We counted the length (in cm) of the transect tape covering coral colonies and macroalgae and then recorded the shape of a coral colony every 5 m. 2.1.5. Statistical analysis Data are presented as mean ± standard error (or, in some cases, standard deviation), and individual means were analyzed with student’s t-tests with an a = 0.05. 3. Results and discussion 3.1. Water quality parameters
2.1.2. Analysis of nutrients and ammonium Immediately after collection, water samples were stored in a cooler at 4 °C and returned to the laboratory for analysis of ammonia and nutrients. A Flow Injection Analyzer (FIA) and spectrophotometer (Hitachi model U-3000) were used to conduct analysis of ammonia, nitrate, nitrite, phosphate and silicate (Pai and Riley, 1994; Pai and Yang, 1990a,b; Pai et al., 2001). 2.1.3. Analysis of tourist density Ten coastal recreational activities at 17 stations were surveyed, and observational data were collected. These activities were skin diving, scuba diving, beach activities, personal watercraft (PWC), boating, jet boating, surfing, sightseeing, swimming, and fishing. Two weekdays and two weekend days were surveyed every month to estimate the number of tourists partaking in each activity. Researchers quantified the number of tourists engaging in each activity in the morning and afternoon on the surveyed day (Meng et al., 2007a). The recreational density of a certain activity at each station was calculated as follows:
We analyzed temperature, salinity, pH, DO, BOD, suspended solid levels, turbidity, and chlorophyll-a, nutrient, and ammonia concentrations along the coast of Nanwan Bay from 2001 to 2008 (Table 1). In general, high standard errors, indicative of unstable water quality, were documented at stations near creeks and rivers (S1, S16, S17, S19, and S26). Conversely, small standard errors, indicative of more stable water quality, were recorded at stations located a greater distance from the outlets of freshwater. Low levels of salinity, pH, and DO were observed along with high levels of nutrients (nitrite, nitrate, ammonia and phosphate), BOD, turbidity, suspended solids, and chlorophyll-a in the water around the coastal areas near the outlets of channels or creeks. While the episodic upwelling that characterizes Nanwan Bay (Chen et al., 2004, 2005) could have driven some of the observed spatiotemporal variation in these water quality parameters, freshwater input from heavy rains may have caused the high nutrient levels measured near estuary stations (Meng et al., 2008), particularly those near river outlets, such as S1, S26 and S16. Normally, the
Table 1 Seawater quality (mean ± SE) at 27 stations along the coast of Nanwan Bay from 2001 to 2008. Temp. (°C)
Salinity (psu)
pH
DO (o/o)
BOD5 (mg/L)
NO2–N (mg/L)
NO3–N (mg/L)
NH3–N (mg/L)
PO4–P (mg/L)
SiO2 (mg/L)
SS (mg/L)
Turbidity (ntu)
Chl.a (lg/L)
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15 S16 S17 S18 S19 S20 S21 S22 S23 S24 S25 S26 S27
27.08 ± 0.46 28.12 ± 0.39 28.39 ± 0.38 28.08 ± 0.31 28.01 ± 0.32 28.30 ± 0.36 29.17 ± 0.35 29.24 ± 0.51 28.89 ± 0.38 28.45 ± 0.34 29.43 ± 0.60 29.42 ± 0.70 29.55 ± 0.47 29.88 ± 0.49 29.13 ± 0.46 28.59 ± 0.45 28.97 ± 0.59 28.44 ± 0.53 29.24 ± 0.54 28.64 ± 0.37 28.01 ± 0.32 28.28 ± 0.32 27.91 ± 0.32 28.28 ± 0.45 27.83 ± 0.32 28.66 ± 0.46 27.48 ± 0.31
12.46 ± 1.45 32.44 ± 0.23 33.53 ± 0.20 33.92 ± 0.09 33.75 ± 0.14 32.49 ± 0.58 33.61 ± 0.11 31.80 ± 0.81 34.07 ± 0.08 33.65 ± 0.12 33.17 ± 0.31 33.23 ± 0.64 33.65 ± 0.18 33.04 ± 0.78 33.68 ± 0.19 6.29 ± 1.15 2.15 ± 0.72 30.80 ± 0.96 0.86 ± 0.14 31.92 ± 0.52 33.53 ± 0.14 31.25 ± 0.40 33.47 ± 0.17 33.71 ± 0.14 32.32 ± 0.59 2.55 ± 0.98 33.66 ± 0.20
7.98 ± 0.03 8.29 ± 0.02 8.42 ± 0.02 8.27 ± 0.02 8.25 ± 0.01 8.35 ± 0.02 8.38 ± 0.02 8.18 ± 0.03 8.24 ± 0.02 8.28 ± 0.02 8.31 ± 0.04 8.25 ± 0.03 8.27 ± 0.03 8.28 ± 0.02 8.28 ± 0.03 8.40 ± 0.05 7.77 ± 0.05 8.20 ± 0.04 8.04 ± 0.03 8.19 ± 0.02 8.24 ± 0.02 8.32 ± 0.02 8.30 ± 0.02 8.20 ± 0.03 8.22 ± 0.01 8.38 ± 0.03 8.26 ± 0.02
89.8 ± 2.4 125.8 ± 2.9 142.9 ± 3.2 105.1 ± 2.2 101.1 ± 0.7 110.6 ± 1.8 129.4 ± 3.0 107.0 ± 2.9 98.4 ± 0.9 107.9 ± 1.6 125.5 ± 6.7 130.2 ± 10.5 121.3 ± 5.8 126.7 ± 4.4 109.6 ± 3.4 123.8 ± 4.8 82.2 ± 9.0 102.9 ± 3.5 93.7 ± 4.1 97.0 ± 0.7 102.9 ± 1.1 120.6 ± 2.3 110.4 ± 1.6 97.7 ± 2.0 96.6 ± 0.6 111.2 ± 2.6 102.7 ± 1.5
3.6 ± 0.4 1.3 ± 0.1 1.1 ± 0.1 1.1 ± 0.1 1.2 ± 0.1 1.3 ± 0.1 0.9 ± 0.1 1.3 ± 0.1 1.0 ± 0.1 1.1 ± 0.1 1.1 ± 0.1 1.2 ± 0.3 1.1 ± 0.1 1.0 ± 0.1 1.0 ± 0.1 3.6 ± 0.5 11.0 ± 2.2 1.6 ± 0.2 5.9 ± 1.2 1.4 ± 0.1 1.0 ± 0.1 0.9 ± 0.1 1.0 ± 0.1 1.1 ± 0.1 1.3 ± 0.1 2.3 ± 0.4 1.0 ± 0.1
0.079 ± 0.008 0.007 ± 0.004 0.002 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.004 ± 0.002 0.001 ± 0.000 0.004 ± 0.001 0.002 ± 0.000 0.001 ± 0.000 0.002 ± 0.001 0.003 ± 0.001 0.002 ± 0.000 0.001 ± 0.000 0.002 ± 0.001 0.284 ± 0.056 0.069 ± 0.015 0.007 ± 0.002 0.194 ± 0.039 0.009 ± 0.002 0.002 ± 0.000 0.002 ± 0.000 0.001 ± 0.000 0.003 ± 0.000 0.001 ± 0.000 0.003 ± 0.000 0.001 ± 0.000
0.313 ± 0.043 0.053 ± 0.009 0.035 ± 0.007 0.029 ± 0.005 0.039 ± 0.008 0.095 ± 0.035 0.027 ± 0.005 0.071 ± 0.020 0.035 ± 0.009 0.031 ± 0.007 0.021 ± 0.011 0.023 ± 0.011 0.014 ± 0.004 0.049 ± 0.038 0.011 ± 0.002 0.446 ± 0.120 0.429 ± 0.217 0.084 ± 0.021 0.511 ± 0.179 0.057 ± 0.010 0.057 ± 0.009 0.100 ± 0.011 0.052 ± 0.010 0.054 ± 0.014 0.032 ± 0.006 0.181 ± 0.091 0.033 ± 0.007
0.370 ± 0.050 0.063 ± 0.021 0.032 ± 0.003 0.057 ± 0.016 0.036 ± 0.004 0.041 ± 0.005 0.048 ± 0.016 0.023 ± 0.005 0.037 ± 0.005 0.046 ± 0.011 0.014 ± 0.002 0.012 ± 0.004 0.014 ± 0.003 0.011 ± 0.002 0.012 ± 0.003 2.978 ± 0.484 1.460 ± 0.491 0.302 ± 0.141 3.068 ± 0.504 0.158 ± 0.029 0.040 ± 0.006 0.034 ± 0.004 0.036 ± 0.005 0.017 ± 0.003 0.042 ± 0.006 0.049 ± 0.009 0.039 ± 0.005
0.042 ± 0.013 0.009 ± 0.003 0.003 ± 0.001 0.002 ± 0.001 0.002 ± 0.001 0.005 ± 0.002 0.003 ± 0.001 0.004 ± 0.002 0.005 ± 0.002 0.003 ± 0.001 0.001 ± 0.001 0.001 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.001 ± 0.000 0.210 ± 0.049 0.148 ± 0.048 0.007 ± 0.002 0.774 ± 0.101 0.026 ± 0.005 0.006 ± 0.001 0.006 ± 0.001 0.008 ± 0.003 0.002 ± 0.000 0.004 ± 0.001 0.006 ± 0.001 0.011 ± 0.009
4.10 ± 0.80 0.40 ± 0.08 0.14 ± 0.02 0.08 ± 0.01 0.11 ± 0.02 0.32 ± 0.10 0.16 ± 0.04 0.44 ± 0.08 0.10 ± 0.01 0.14 ± 0.02 0.13 ± 0.01 0.15 ± 0.08 0.07 ± 0.01 0.16 ± 0.10 0.67 ± 0.59 1.54 ± 0.25 4.76 ± 0.31 0.60 ± 0.14 4.83 ± 0.24 0.39 ± 0.08 0.14 ± 0.01 0.44 ± 0.05 0.13 ± 0.02 0.09 ± 0.01 0.28 ± 0.07 4.68 ± 0.23 0.18 ± 0.05
578.0 ± 280.0 12.2 ± 2.0 7.8 ± 0.7 6.9 ± 0.4 13.9 ± 4.6 7.6 ± 0.4 7.4 ± 0.4 32.1 ± 6.0 7.4 ± 0.4 18.0 ± 2.7 19.9 ± 4.5 13.6 ± 2.8 7.7 ± 0.6 6.4 ± 0.5 10.0 ± 1.9 74.8 ± 27.0 102.8 ± 59.0 30.5 ± 10.7 402 ± 333.0 40.5 ± 6.2 9.0 ± 0.7 7.1 ± 0.3 6.7 ± 0.5 6.5 ± 0.8 67.5 ± 2.0 136.7 ± 46.7 12.6 ± 5.1
249.0 ± 115.0 3.3 ± 0.8 1.5 ± 0.3 1.1 ± 0.1 4.2 ± 1.9 1.4 ± 0.2 1.3 ± 0.2 13.3 ± 2.9 1.4 ± 0.2 5.7 ± 1.1 5.8 ± 1.2 4.3 ± 1.2 2.0 ± 0.3 0.8 ± 0.1 2.4 ± 0.8 36.8 ± 13.9 46.5 ± 24.2 13.7 ± 5.9 174.0 ± 136.0 15.6 ± 2.6 2.0 ± 0.3 1.3 ± 0.1 1.1 ± 0.2 1.1 ± 0.3 26.1 ± 8.9 63.3 ± 20.1 3.4 ± 2.1
2.78 ± 0.57 0.25 ± 0.03 0.15 ± 0.01 0.16 ± 0.02 0.17 ± 0.02 0.30 ± 0.04 0.13 ± 0.01 0.39 ± 0.12 0.11 ± 0.02 0.30 ± 0.04 0.43 ± 0.14 0.36 ± 0.15 0.18 ± 0.03 0.34 ± 0.14 0.37 ± 0.12 5.33 ± 2.12 5.47 ± 2.92 0.46 ± 0.09 0.83 ± 0.27 0.42 ± 0.06 0.18 ± 0.04 0.25 ± 0.06 0.19 ± 0.03 0.11 ± 0.02 0.24 ± 0.04 0.36 ± 0.06 0.18 ± 0.02
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Fig. 2. The recreational densities (expressed as percentages of the average values) observed along the coast of Kenting National Park. PWC, personal watercraft.
park’s peak tourist season. Consequently, high levels of nutrients, BOD5, suspended solids, and turbidity were found in the water collected along the KNP effluent area, such as the heavily visited S20 coastline. Compared to the other stations, significantly higher nutrient, BOD5, turbidity, and chlorophyll-a levels were found in water sampled at site S16, which is located near the confluence of Shir-Neou stream with Nanwan Bay. Anthropogenic nutrient enrichment can stimulate algal blooms (Fabricius et al., 2005; Lapointe et al., 2004), and, in February 2002, we found the first incidence of a ‘‘green tide’’ caused by nutrient pollution along the S16 coastal area, which receives freshwater input from Shir-Neou stream. The chlorophyll-a content of phytoplankton in the water was extremely high, 339 and 15.3 lg/L in February 2002 and May 2002, respectively.
Fig. 3. Average numbers of tourists (expressed as monthly means ± standard error) at the different stations along the coast of Kenting National Park.
3.2. Recreational densities around Kenting National Park Common recreational activities along the coast of KNP include skin diving, SCUBA diving, beach activities, personal watercraft activities, ‘‘banana’’ boating, jet boating, surfing, sightseeing cruises, swimming, and fishing (Meng et al., 2007a). The recrea-
Fig. 4. Total number of tourists observed monthly along the coast of Kenting National Park from 2001 to 2008.
rainy season in the Hengchun Peninsula of Taiwan, in which KNP is located, is from May to September, and this coincides with the
Fig. 5. The average number of skin divers (±standard error) at the different stations of Kenting National Park from 2002 to 2008.
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3.3. The relationship between water quality and macroalgal cover Accumulation of nutrients varied across seasons in this study. For instance, higher nutrient levels tended to accumulate in the river water and sediments during the dry season, becoming diluted by rainwater in the summer monsoon season. Consequently, algal blooms occurred almost every year during the dry seasons, except for the times in which typhoons occurred during the dry season, in which case no algal blooms occurred. There were significant positive correlations between nitrite, phosphate, and ammonia concentrations and macroalgal cover (r2 = 0.94, 0.89, 0.58, respectively, n = 5, p < 0.01). As we mentioned before, an increase in domestic wastewaters, which carry excessive nutrients, flows into Nanwan Bay without being treated in the wet season or following rains, leading to increases in macroalgal cover (Liu et al., 2009). This has also been shown in field experiments on the Great Barrier Reef (Fabricius et al., 2005) and South Florida (Lapointe et al., 2004). Fig. 6. Coral cover of reef flats at different stations along the coast of Kenting National Park.
tional densities (expressed as percentages of the averages) observed along the coast of KNP (Fig. 2) indicate that, of the 10 types of coastal activities observed, most tourists prefer beach activities, skin diving, and swimming during their vacations. While the numbers of tourists varied from station to station and between years (Fig. 3), the results indicate that S10, S7, and S20 were the preferred coastal recreational areas. The peak season for tourism was from June to September in all years sampled (Fig. 4). The peak number of skin divers was also documented during this period (Fig. 5), and the preferred snorkeling sites were S7, S21, and S22.
3.4. The relationship between water quality and coral cover Coral cover of the reef flats at the different stations was variable (Fig. 6). The average coral cover along the coast of KNP was approximately 30% and ranged from 5.6% to 60.0%. The correlations between nitrite, phosphate, ammonia, macroalgal cover, and suspended solid concentrations and coral cover were negative and statistically significant (Fig. 7, r2 = 0.25, 0.26, 0.36, 0.65, 0.28, respectively, n = 16, p < 0.05). Effects of water quality deterioration (e.g., sedimentation, thermal stress, and eutrophication) on coral reef ecosystems have been widely studied (Bruno et al., 2007; Crossland et al., 1984; Gilmour, 1999; James et al., 2005; Liao et al., 2007; Manzello et al., 2007; Miller and Cruise, 1995; Nugues and Roberts, 2003; Thomas and Ridd, 2005; Thomas et al., 2003;
Fig. 7. The correlations between levels of nitrite, phosphate, ammonia, macroalgal cover, and suspended solids and coral cover.
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Woolfe and Larcombe, 1999) and suggest that an increase in domestic wastewater, which carries excessive nutrients, may have led to the observed increases in macroalgal cover (Liu et al., 2009). As macroalgae compete with coral for the same substrate (Liu et al., 2009), macroalgal cover typically increases when coral cover decreases. 3.5. The relationship between numbers of tourists and coral cover The inverse relationship between numbers of skin divers and coral cover (r2 = 0.62, n = 24, p < 0.01) suggests that skin divers have negatively influenced the survival of shallow water corals due to physical destruction. In fact, tourists and skin diver numbers show a positive correlation with algal cover. When divers step carelessly on or collect coral colonies, they cause the destruction of both the colony and the associated habitat, which is used by a plethora of other organisms (Meng et al., 2007a). In sum, our results confirm that increasing numbers of tourists and skin divers were one of the dominant factors that led to the drop in coral cover (Ho et al., 2011). 4. Conclusions Most of the coral reefs in Taiwan are fringing reefs that are located in shallow areas near the coast; hence they are readily influenced by human activities (Dai, 1988, 1991a,b, 1993, 1996; Yang, 1985). Coral reef ecosystems are interconnected given the lack of significant barriers to water flow in marine environments, and so if point-source pollution is documented at one site, it is possible that its detrimental influence may spread. For example, improper stabilization of a hill near KNP has resulted in a local increase in seawater turbidity. Furthermore, tourists produce a great deal of both trash and sewage, the latter of which migrates to coastal waters after heavy rains. This turbid, nutrient-rich water has led to increases in algal cover in shallow areas previously occupied by corals and other invertebrates (Meng et al., 2007a,b, 2008). On the other hand, physical disturbances caused by snorkelers and divers, such as inadvertent contact with coral, during July–August summer vacations may have had as great an impact as the decreased seawater quality. In summary, the water quality of the reef flats of KNP has been deteriorating since 2001 and requires greater attention (Chang et al., 2008). Our results show that increasing numbers of tourists, suspended solids, nutrients, and ammonia were the dominant factors leading to the decline in coral cover. We urge continued research on both potential sources of degradation, as was done herein, and the ability of corals to recover to such disturbances. Acknowledgements This study was financially supported by Grants from the National Science Council of Taiwan (NSC 97-2621-B-291-002-MY3; NSC95-2621-B-291-003; NSC 94-2621-B-291-003; NSC 93-2621B-291-001; NSC 92-2621-B-291-004) and the Headquarters of the Kenting National Park to P.J.M. We would like to thank Anderson Mayfield for critical comments on the manuscript as well as a thorough proofreading of the English. References Ault, T.R., Johnson, C.R., 1998. Spatially and temporally predictable fish communities on coral reefs. Ecol. Monogr. 68, 25–50. Bastidas, C., Bone, D., Garcia, E.M., 1999. Sedimentation rates and metal content of sediments in a Venezuelan coral reef. Mar. Pollut. Bull. 38 (1), 16–24. Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D., Sweatman, H., Melendy, A.M., 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5 (6), e124.
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