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Effects of elevated water temperature, reduced salinity and nutrient enrichment on the metabolism of the coral Turbinaria mesenterina
Estuarine, Coastal and Shelf Science 88 (2010) 482e487
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Effects of elevated water temperature, reduced salinity and nutrient enrichment on the metabolism of the coral Turbinaria mesenterina Suzanne Faxneld*, Tove L. Jörgensen, Michael Tedengren Department of Systems Ecology, Stockholm University, SE-106 91 Stockholm, Sweden
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Article history: Received 17 November 2009 Accepted 18 May 2010 Available online 2 June 2010
Water quality is declining in many coastal areas, which has caused coral degradation worldwide. In addition, reduced water quality may aggravate the impacts of seawater temperature. In this study the effects of increased temperature (31 C), nitrate enrichment (þ5 mM NO3), low salinity (20) and combinations of these stressors were investigated compared to ambient water (25 C, 30, 0.3 mM NO3) on the metabolism and survival of the coral Turbinaria mesenterina from the Tonkin Gulf, Vietnam. The results showed that all specimens exposed to a combination of all three stressors (i.e. high temperature þ high nitrate þ low salinity) died after 24 h exposure, while those that had been exposed to high nitrate þ low salinity at ambient temperature did not show any effects on the metabolism or survival. Furthermore, corals exposed to low salinity þ high temperature displayed a decrease in gross primary production/respiration (GP/R) ratio and the mortality rate was 50%. In addition, all corals exposed to increased temperature, alone or in combination with another stressor, displayed a GP/R24h ratio below 1.0, suggesting that they depend on stored energy to cover their metabolic requirements. The results showed that corals may tolerate short-term exposure to stressors such as low salinity þ high nitrate concentration in ambient temperature, while additional increased temperature lead to rapid mortality, hence suggesting a synergistic effect. Thus, the effect of climate change might be more severe in nearshore coastal areas where corals already are exposed to several disturbances. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: temperature increase salinity nutrients corals metabolism stress
1. Introduction Human activities have caused increases in land run-off and deterioration of the water quality world-wide (McCulloch et al., 2003; Devlin and Brodie, 2005). High levels of nutrients, pollution and sedimentation have shown to lead to increased coral mortality (see Fabricius, 2005 for review), reduction in coral richness (Fabricius et al., 2005), inhibition of coral recruitment (Hunte and Wittenberg, 1992), reduced coral growth rate (Tomascik and Sander, 1985) and increased macroalgae cover (Fabricius and De’ath, 2004). Also, salinity stress can in the long-term affect coral growth and reproduction, and can eventually cause mortality (Coles and Jokiel, 1992). Furthermore, the combination of enhanced nutrients and decreased salinity has shown to lead to decreased coral reproduction (Humphrey et al., 2008). In addition to these disturbances, the effects from climate change will most likely put further stress on the environment (IPCC, 2007), and large-scale bleaching events are predicted
* Corresponding author. E-mail address: [email protected] (S. Faxneld). 0272-7714/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2010.05.008
to be more common during the next decades (Donner et al., 2005). This in turn may cause synergistic effects in combination with other disturbances (Hughes et al., 2003). Coral bleaching has been shown to lead to coral mass mortality (Wilkinson, 2000). This opens a window for establishment of opportunistic algae (McClanahan et al., 2001), which eventually could cause a shift from a coral dominated to macroalgae-dominated state (Done, 1992), especially in combination with high levels of nutrients and the absence of herbivores (McCook, 1999). It has been predicted that climate change will not only lead to increases in temperature, but also more precipitation (IPCC, 2007). Thus, this may cause declining water quality when episodic rainfalls transport nutrients and sediment into coastal areas (Hoegh-Guldberg et al., 2007), and nearshore reefs may suffer from reduced salinity. Furthermore, intensive rainfall can also directly cause lowered salinities at shallow reef areas, especially during low tides (Kerswell and Jones, 2003). Hence, these effects may be even more severe during episodes of elevated seawater surface temperatures. For instance, Berkelmans and Oliver (1999) found that nearshore corals that had been exposed to decreased salinities experienced more bleaching during periods of warmer water than offshore reefs.
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Studies have investigated synergistic, additive or antagonistic effects from increased temperature and a second stress factor on the metabolism of corals: nutrients (Nordemar et al., 2003), heavy metals (Nyström et al., 2001), sedimentation (Anthony et al., 2007) and salinity (Coles and Jokiel, 1978). To our knowledge, no studies have experimentally investigated the effects of multiple factors affecting water quality negatively, in combination with increased temperature, even though several of these disturbances most likely occur and act together. For instance, nutrient addition from land is often accompanied by other changes in water quality, such as decreased salinity (McClanahan et al., 2002). The aim of this study was to investigate how corals respond to different stressors that may occur on nearshore reefs (e.g. high nutrient load and low salinity due to heavy rainfall and land runoff) and if the physiological responses were stronger in combination with elevated water temperatures. Hence, the physiological effects on the coral Turbinaria mesenterina exposed to (a) nitrate enrichment, (b) decreased salinity, (c) nitrate enrichment þ decreased salinity was studied at 25 C (ambient) and 31 C (temperature increase) in order to investigate the interactive effects of these stress factors. 2. Methods 2.1. Collection of corals The study was conducted in May 2008 in an outdoor laboratory at Tram Bien Research Station, in Do Son, northern Vietnam. Pieces (e8 4 cm) of the coral species Turbinaria mesenterina were collected close to Co To Island (N 20 58’39”, E 10747’16”), northern Vietnam, at a depth ofe4e8 m. T. mesenterina was chosen since it was the most common coral on the reef, and known to be a very robust species (Marshall and Baird, 2000; Anthony, 2006; Sofonia and Anthony, 2008). After collection, corals were transported to the outdoor laboratory under low light condition and with continuous aeration. Epiphytes and boring organisms were carefully removed before the corals were put in aerated aquaria (20 litre each) with filtered and UV-treated seawater, which were placed in larger water-filled tanks (1 m3) in order to minimise temperature fluctuations (Nordemar et al., 2003). Since T. mesenterina is a foliaceus species, the proportion of tissue affected by the fragmentation during collection was very low, and mucus production was not stimulated. Increased mucus production is a general stress response in corals and commonly used to indicate and exclude damaged specimens of fragmented corals from experimental set-ups. Corals were allowed to acclimate for 48 h in ambient temperature (25 C), under reduced light conditions (154 20 mE m2 s1) and with extra air supply before the experiment started. 2.2. Experimental setup Each coral replicate was put in a 1.5 litre transparent plastic jar; the jars were then placed randomly in the 20-litre aquaria (4 jars in each aquarium), which in turn were placed in four larger waterfilled tanks (1 m3) representing the heat exposure- and control tank respectively. Two tanks for each treatment were used. Aeration pumps mixed the seawater in both the jars and the tanks, thus maintaining high oxygen concentrations and distributing water temperature evenly. The water temperature in the exposure tanks was increased using heating regulators (ZEBO 300 W or FLUVAL Tronic 200 W). In total 24 coral pieces were used in the heat exposed and ambient treatments respectively, thus resulting in 6 replicates for each of the 8 treatments.
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The treatments were: (a) ambient (25 C, 30, 0.3 mM NO 3 ), (b) high nitrate (þ5 mM NO 3 ), (c) low salinity (20), (d) high nitrate þ low salinity, (e) high temperature (31 C), (f) high temperature þ high nitrate, (g) high temperature þ low salinity, (h) high temperature þ high nitrate þ low salinity. The salinity was measured using the Practical Salinity Scale. The heaters were put on and the low salinity was obtained by diluting natural seawater with purified freshwater (to mimic dilution with rainwater). This design lead to a rather rapid increase in temperature and decrease in salinity (experimental conditions within a few hours), but no increased mucus production or retraction of polyps could be observed at this stage, and other studies have shown that salinity can drop very rapid in nearshore areas after heavy rainfalls (from 30 to 15 psu within 24 h; Jokiel et al., 1993). It is also well known that daily temperatures can undergo drastic changes on nearshore reef flats and in coastal lagoons, e.g. 25e33 C within hours (Semesi et al., 2009). The temperature range used in this study is, however, reported to be “normal summer temperatures” in the area (Latypov, 2005). Nitrate was then added to the nutrient enriched treatments as NaNO3. The used concentration has been shown to be ecologically relevant during rainy seasons (Devlin and Brodie, 2005; Costa et al., 2008). Nitrate was used since that is the main form of nitrogen available in tropical waters (Marubini and Davies, 1996) and nitrogen is a common nutrient in land run-off due to agricultural practices (Devlin and Brodie, 2005). The experiment was conducted outdoors under reduced light conditions during the exposure (154 20 mE m2 s1), in order to minimise synergistic effects with high light conditions (Fitt et al., 2001). Corals were exposed for 24 h before their metabolism were measured. 2.3. Productivity measurements The net production and respiration were measured during midday in natural ambient sunlight without additional air supply. During the production measurements, the light intensity was measured every five minutes and varied between 1500 and 2200 mE m2 s1 throughout the measurements, but did not differ between treatments. It should be noted that this irradiance is measured above the water surface (under water meter not available) and that it is lower at the surface of the submerged corals at approximately 0.5 meters depth. However, 2200 mE m2 s1 can be considered “normal” at sea surface in tropical waters (Chalker, 1981). Other studies also report production measurements at 1500e2000 mE m2 s1 (Nyström et al., 2001; Nordemar et al., 2003) above sea surface, and Semesi et al. (2009) report corresponding light values at 1e4 meters to be 300e500 mE m2 s1. According to Chalker et al. (1983), sun exposed corals from shallow waters reach light saturation ate340 mE m2 s1 and we thus assume that the corals used in this experiment are light saturated, i.e. produce at maximum rate. Furthermore, since the increase in light intensity before the measurements was synchronised to the actual sunrise, it can be argued that light should not be considered as an additional stress factor in this experiment. In order to keep a stable temperature during the measurement (i.e. 25 and 31 C respectively), the jars, with the individual corals, were placed inside foam boxes with surrounding water of the accurate temperatures (no light reduction occurred in the boxes). The surrounding water was stirred and temperatures measured every five minutes during the production measurements in the foam boxes, and when necessary, small pieces of ice were added to maintain a stable temperature. Changes in dissolved oxygen concentration in light (net production) and darkness (respiration) were measured according to Moberg et al. (1997) using an oximeter (WTW OXI 330). Between
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2.4. Statistical analyses A three-way ANOVA could not be conducted since all corals in one of the treatment groups died during exposure, therefore a oneway ANOVA was used to analyse the effects of the different treatments. The coral replicates that died during the treatment were excluded from the statistical analyses. Where differences were found, Tukey HSD was used as a post hoc test (p < 0.05). All data were tested for homogeneity of variances using Levene’s test (p < 0.05) before the ANOVA was carried out. For the statistical analyses SPSS 16.0 for Mac OS X was used. 3. Results 3.1. Mortality All corals exposed to the multiple stressors high temperature þ high nitrate þ low salinity died after 24 h exposure, whereas those exposed to high nitrate þ low salinity at ambient water temperature did not show any stress response in GP/R ratio, respiration rate or gross primary production rate (Fig. 1aed) and no mortality occurred. Corals exposed to increased temperature þ low salinity experienced a 50% (n ¼ 3) mortality rate and there was a 33.3% (n ¼ 2) mortality rate for the corals exposed to high temperature þ high nitrate. Only 16.7% (n ¼ 1) of the corals exposed to high temperature alone were dead after the exposure. In contrast, there was no mortality at all among corals exposed to a single stressor at ambient temperature (i.e. low salinity or high nitrate). 3.2. GP/R ratio There were significant differences in GP/R ratio between treatments (GLM ANOVA df ¼ 6, F ¼ 2.676, p < 0.05), where high
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measurements the jars were sealed with tight-fitting lids. An earlier pilot test showed that the most stable and reliable values were obtained after a 1-hour and 1.5 h acclimation period in light and darkness for production and respiration, respectively. Dissolved oxygen concentration was initially measured in light and then again after 1 h. Corals were then placed in darkness and after 1.5 h the oxygen concentration was measured once more and respiration rates calculated. For the statistical analyses respiration rates were converted to 1-hour values. Two water controls (without corals) of each treatment were used. The oxygen saturation levels never dropped below 70% during the measurements. After the experiment was terminated the coral surface area was determined using the aluminium foil method (March, 1970) and to compensate for volume dependent differences in dissolved oxygen concentration, the volumes of the corals were measured by submerging the coral into a graded beaker filled with a known volume of water. Net production rate and respiration rate data were calculated per hour and cm2 coral surface area. Respiration rate was added to the net production value in order to achieve gross primary production rate. Due to the lack of laboratory facilities no biomass of the corals could be measured and neither could the chlorophyll concentrations be analysed, therefore the gross production and respiration are expressed as per cm2 coral surface area according to Moberg et al. (1997). Gross primary production/respiration (GP/R) ratios over both 1 h and 24 h (12 h light, 12 h darkness) were also calculated to get a dimensionless estimate of the physiological status of the corals. GP/R24h estimates the autotrophic capabilities and if GP/R24h 1 it indicates that an organism is self-supporting while a value below 1 indicates that the organism needs to import energy to fulfil their energy demands (Hopkinson and Smith, 2005).
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Fig. 1. Turbinaria mesenterina (mean values SE). a) GP/R ratios (1 h). b) GP/R ratios (24 h). The dashed line indicates GP/R ¼ 1. c) Respiration rates. d) Gross primary production rates. A ¼ ambient temperature, HT ¼ high temperature, HN ¼ high nitrate, LS ¼ low salinity. The dark colour represents all treatments in combinations with high temperature and the light colour represents all treatments in ambient temperature. *p < 0.05, **p < 0.01, ***p < 0.001. y ¼ All specimens in the HT þ HN þ LS combination died.
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temperature þ low salinity had a lower GP/R ratio compared to low salinity (Tukey HSD p ¼ 0.025; Fig. 1a), and ambient water (Tukey HSD p ¼ 0.041; Fig. 1a), and a strong trend for a lower GP/R ratio compared to high nitrate (Tukey HSD p ¼ 0.058; Fig. 1a). There was no difference between high nitrate and high temperature þ high nitrate, and no differences between ambient water temperature and any of the single stressor treatments were found. GP/R24h ratio (Fig. 1b) showed that the corals in ambient water, high nitrate and low salinity had a GP/R24h ratio of 1.0 or slightly above that, indicating that these were energetically self-supporting during the study. In comparison, the corals exposed to high temperature or high temperature þ high nitrate had a GP/R24h ratio of 0.75 and the corals exposed to high temperature þ low salinity had a GP/R24h ratio of 0.30, demonstrating consumption of stored energy for maintenance. 3.3. Respiration and gross primary production rates There were differences in respiration rates between treatments (GLM ANOVA df ¼ 6, F ¼ 6.198, p < 0.001). The high temperature þ low salinity had a higher respiration rate compared to the ambient water temperature (Tukey HSD p ¼ 0.002; Fig. 1c), low salinity (Tukey HSD p ¼ 0.002; Fig. 1c), high nitrate (Tukey HSD p ¼ 0.003; Fig. 1c) and high nitrate þ low salinity (Tukey HSD p ¼ 0.001; Fig. 1c). Moreover, there were no differences between high temperature or high temperature þ high nitrate and any of the treatments in 25 C. In contrast, there were no differences whatsoever in gross primary production rates between any of the treatments (see Fig. 1d), but the variation in the high temperature þ low salinity group seemed to increase. 4. Discussion Our results showed that while those corals that were exposed to low salinity in combination with high nitrate at ambient temperature all survived and were not affected physiologically, the treatment with multiple stressors e high temperature in combination with low salinity and high nitrate e caused mortality to all the specimens within 24 h of exposure. The combination of high temperature and low salinity resulted in a decrease in GP/R ratio, which was explained by an increase in respiration rates. Moreover, a GP/R24h ratio of 0.3 indicated that these corals would have needed a net import of energy corresponding to at least 70% of their energy demand, while on the other hand the corals exposed to low salinity alone had a GP/R24h ratio of slightly above 1.0. Thus, indicating that corals exposed to salinity stress alone can still meet their energy demands through autotrophic production, while corals exposed to the combination of salinity stress and increased water temperature must use their own reserves or import energy for their maintenance (Hopkinson and Smith, 2005). Furthermore, 50% of the corals in the treatment low salinity in combination with high temperature died. It would therefore seem that the effect of low salinity was aggravated by elevated temperature. This is in accordance to Coles and Jokiel (1978) who reported similar results, where the mortality rate increased when corals were exposed to both high temperature and low salinity compared to only high temperature. While there were no initial physiological effects in the treatment with the combination high temperature and high nitrate in this study, the corals exposed to increased temperature alone or in combination with increased nitrate concentration or low salinity all showed a GP/R24h ratio below 1. This indicates that the corals at increased water temperature experience increased energy demand, demonstrated through increased respiration rates, and thus
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became more dependent on stored energy reserves (or feeding) in order to adapt and survive. Other authors have found a more pronounced effect in the combination of high nitrate and high temperature on the gross primary production rate, in comparison to the effects of single stressors (Nordemar et al., 2003), however, both the nitrate concentration was higher and the exposure time longer in that study. Moreover, there was no decrease in the corals’ GP/R ratio when exposed to a single stressor alone: low salinity, high nitrate or high temperature respectively, which indicates that the mode of stress factor application did not per se significantly affect the specimens. Both Moberg et al. (1997) and Alutoin et al. (2001) found a negative effect in terms of decreased GP/R ratio and/or production rates when Pocillopora damicornis and Porites lutea were exposed to the same amplitude of decrease in salinity as in our study. On the other hand Muthiga and Szmant (1987) did not find any effects on gross production or respiration rates of Siderastrea siderea exposed to the same salinity decrease. Thus, this indicates that the effects of a salinity decrease may vary among coral species (Moberg et al., 1997) and/or local area, which might be due to corals being differently adapted to salinity changes. There were no physiological effects from nitrate enrichment alone in this study, which is in accordance with Ferrier-Pagès et al. (2001), who found no effects on zooxanthellae density or photosynthesis with nitrate enrichment (2 mM). Similarly, Marubini and Davies (1996) did not find any effects on gross primary production rates on corals exposed to 1 mM nitrate, but corals exposed to 5 mM showed an increase in gross primary production rates. However, the effect was evident only after 30 days of exposure. A possible reason for the lack of response to nutrient enrichment alone of the corals in this study could be the relatively low dose (which was however ecologically relevant and triggered responses in the study in combination with other stress factors) in relation to the short (24 h) exposure time, or it might be due to temporal differences in the natural nitrate exposure in the Tonkin Gulf, which could have caused acclimatization of the corals and their zooxanthellae to increased nutrient availability. In general, corals can suffer substantial mass mortality during periods of increased water temperature (Wilkinson, 2000). However, some coral species are more tolerant to increased water temperatures than others, e.g. massive Porites (McClanahan, 2000), Pavona spp. (McClanahan et al., 2004), Galaxea spp. (McClanahan et al., 2004) and Goniopora spp. (McClanahan et al., 2004). Turbinaria spp. have also been found to be tolerant to elevated water temperatures (Marshall and Baird, 2000), which might explain why there was no significant decrease in GP/R ratio to the single stress factor increased temperature in this study. However, when recalculating the GP/R ratio to a 24 h basis, it is clear that all high temperature treatments have GP/R24h ratios below 1, which indicate that the corals are not self-maintained through primary production. Furthermore, one of the specimens died after exposure to heat alone, which may be explained by individual variation in temperature tolerance. At least during short periods of time it seems that corals can withstand acute exposure from land-based pollution (e.g. decreased salinity and/or nitrate enrichment), however in combination with elevated seawater temperatures, it can lead to mortality within 24 h, as it did in this study. Freshwater inflow, enhanced nutrients and increased water temperatures usually correlate in the field, e.g. during the rainy season (Lapointe, 1997). In this study the temperature used was e0.5 C above normal summer maximum temperature in the study area (Dr Cu unpubl. data). Hence, this suggests that when corals are exposed to land run-off and heavy rainfall, only a slightly higher temperature than normal summer maximum might be enough to cause coral bleaching and eventually mass mortality.
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5. Conclusion It has been suggested that areas where local anthropogenic stressors (e.g. overfishing and land-based pollution) are kept to a minimum will have a higher resilience (i.e. higher recovery rate) after a bleaching event than areas subjected to multiple stressors (Sandin et al., 2008; Smith et al., 2008; but see Graham et al., 2006). It is therefore important to eliminate factors that may aggravate the effects of climate change, since the highest extinction risk will most likely be in areas were local anthropogenic disturbances are more frequent (Carpenter et al., 2008). Furthermore, non-point source pollution is predicted to increase in the future, due to more nutrient use in the agricultural ecosystems, urbanization and a growing human population (Carpenter et al., 1998). While this study only focus on one coral species, T. mesenterina, it is quite possible that the results may be applicable also to other coral species. Especially since this species have been found to be tolerant not only to increased water temperature (Marshall and Baird, 2000) but also turbidity (Anthony, 2006; Sofonia and Anthony, 2008), and other coral genera might be more sensitive to rapid environmental fluctuations. If so, good water quality may be of utter importance, since elevated temperature may cause lethal synergistic effects on corals exposed to other disturbances. Indeed, improved water quality has been suggested to enhance the resilience in corals to increased water temperatures (HoeghGuldberg et al., 2007; Hughes et al., 2007).
Acknowledgements This study was financed by Stockholm Marine Research Center (SMF) and Swedish International Development Cooperation Agency (Sida). Thanks to the staff at Tram Bien Research Station in Do Son for assistance. Thanks to M. Nyström, M. Björk and M. Gullström for valuable comments.
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Effects of hypo-osmosis on the coral Stylophora pistillata: nature and cause of ‘low-salinity bleaching’. Marine Ecology Progress Series 253, 145e154. Lapointe, B.E., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnology and Oceanography 42, 1119e1131. Latypov, Y.Y., 2005. Reef-building corals of Vietnam as a part of the Indo-Pacific reef ecosystem. Russian Journal of Marine Biology 31, s34es40. March, J.A., 1970. Primary productivity of reef-building calcareous red algae. Ecology 51, 255e263. Marshall, P.A., Baird, A.H., 2000. Bleaching of corals on the Great Barrier reef: differential susceptibilities among taxa. Coral Reefs 19, 155e163. Marubini, F., Davies, P.S., 1996. Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Marine Biology 127, 319e328. McClanahan, T.R., Muthiga, N.A., Mangi, S., 2001. Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs 19, 380e391. McClanahan, T.R., Polunin, N., Done, T., 2002. Ecological states and resilience of coral reefs. Conservation Ecology 6, 18. McClanahan, T.R., Baird, A.H., Marshall, P.A., Toscano, M.A., 2004. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Marine Pollution Bulletin 48, 327e335. McClanahan, T.R., 2000. Bleaching damage and recovery potential of Maldivian coral reefs. Marine Pollution Bulletin 40, 587e597. McCook, L.J., 1999. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357e367. McCulloch, M., Fallon, S., Wyndham, T., Hendy, E., Lough, J., Barnes, D., 2003. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. 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S. Faxneld et al. / Estuarine, Coastal and Shelf Science 88 (2010) 482e487 Moberg, F., Nyström, M., Kautsky, N., Tedengren, M., Jarayabhand, P., 1997. Effects of reduced salinity on the rates of photosynthesis and respiration in the hermatypic corals Porites lutea and Pocillopora damicornis. Marine Ecology Progress Series 157, 53e59. Muthiga, N.A., Szmant, A.M., 1987. The effects of salinity stress on the rates of aerobic respiration and photosynthesis in the hermatypic coral Siderastrea siderea. Biological Bulletin 173, 539e551. Nordemar, I., Nyström, M., Dizon, R., 2003. Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Marine Biology 142, 669e677. Nyström, M., Nordemar, I., Tedengren, M., 2001. Simultaneous and sequential stress from increased temperature and copper on the metabolism of the hermatypic coral Porites cylindrica. Marine Biology 138, 1225e1231. Sandin, S.A., Smith, J.E., DeMartini, E.E., Dinsdale, E.A., Donner, S.D., Freidlander, A. M., Konotchick, T., Malay, M., Maragos, J.E., Obura, D., Pantos, O., Paulay, G., Richie, M., Rohwer, F., Schroeder, R.E., Walsh, S., Jackson, K.B.C., Knowlton, N.,
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Effects of elevated water temperature, reduced salinity and nutrient enrichment on the metabolism of the coral Turbinaria mesenterina Suzanne Faxneld*, Tove L. Jörgensen, Michael Tedengren Department of Systems Ecology, Stockholm University, SE-106 91 Stockholm, Sweden
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 November 2009 Accepted 18 May 2010 Available online 2 June 2010
Water quality is declining in many coastal areas, which has caused coral degradation worldwide. In addition, reduced water quality may aggravate the impacts of seawater temperature. In this study the effects of increased temperature (31 C), nitrate enrichment (þ5 mM NO3), low salinity (20) and combinations of these stressors were investigated compared to ambient water (25 C, 30, 0.3 mM NO3) on the metabolism and survival of the coral Turbinaria mesenterina from the Tonkin Gulf, Vietnam. The results showed that all specimens exposed to a combination of all three stressors (i.e. high temperature þ high nitrate þ low salinity) died after 24 h exposure, while those that had been exposed to high nitrate þ low salinity at ambient temperature did not show any effects on the metabolism or survival. Furthermore, corals exposed to low salinity þ high temperature displayed a decrease in gross primary production/respiration (GP/R) ratio and the mortality rate was 50%. In addition, all corals exposed to increased temperature, alone or in combination with another stressor, displayed a GP/R24h ratio below 1.0, suggesting that they depend on stored energy to cover their metabolic requirements. The results showed that corals may tolerate short-term exposure to stressors such as low salinity þ high nitrate concentration in ambient temperature, while additional increased temperature lead to rapid mortality, hence suggesting a synergistic effect. Thus, the effect of climate change might be more severe in nearshore coastal areas where corals already are exposed to several disturbances. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: temperature increase salinity nutrients corals metabolism stress
1. Introduction Human activities have caused increases in land run-off and deterioration of the water quality world-wide (McCulloch et al., 2003; Devlin and Brodie, 2005). High levels of nutrients, pollution and sedimentation have shown to lead to increased coral mortality (see Fabricius, 2005 for review), reduction in coral richness (Fabricius et al., 2005), inhibition of coral recruitment (Hunte and Wittenberg, 1992), reduced coral growth rate (Tomascik and Sander, 1985) and increased macroalgae cover (Fabricius and De’ath, 2004). Also, salinity stress can in the long-term affect coral growth and reproduction, and can eventually cause mortality (Coles and Jokiel, 1992). Furthermore, the combination of enhanced nutrients and decreased salinity has shown to lead to decreased coral reproduction (Humphrey et al., 2008). In addition to these disturbances, the effects from climate change will most likely put further stress on the environment (IPCC, 2007), and large-scale bleaching events are predicted
* Corresponding author. E-mail address: [email protected] (S. Faxneld). 0272-7714/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2010.05.008
to be more common during the next decades (Donner et al., 2005). This in turn may cause synergistic effects in combination with other disturbances (Hughes et al., 2003). Coral bleaching has been shown to lead to coral mass mortality (Wilkinson, 2000). This opens a window for establishment of opportunistic algae (McClanahan et al., 2001), which eventually could cause a shift from a coral dominated to macroalgae-dominated state (Done, 1992), especially in combination with high levels of nutrients and the absence of herbivores (McCook, 1999). It has been predicted that climate change will not only lead to increases in temperature, but also more precipitation (IPCC, 2007). Thus, this may cause declining water quality when episodic rainfalls transport nutrients and sediment into coastal areas (Hoegh-Guldberg et al., 2007), and nearshore reefs may suffer from reduced salinity. Furthermore, intensive rainfall can also directly cause lowered salinities at shallow reef areas, especially during low tides (Kerswell and Jones, 2003). Hence, these effects may be even more severe during episodes of elevated seawater surface temperatures. For instance, Berkelmans and Oliver (1999) found that nearshore corals that had been exposed to decreased salinities experienced more bleaching during periods of warmer water than offshore reefs.
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Studies have investigated synergistic, additive or antagonistic effects from increased temperature and a second stress factor on the metabolism of corals: nutrients (Nordemar et al., 2003), heavy metals (Nyström et al., 2001), sedimentation (Anthony et al., 2007) and salinity (Coles and Jokiel, 1978). To our knowledge, no studies have experimentally investigated the effects of multiple factors affecting water quality negatively, in combination with increased temperature, even though several of these disturbances most likely occur and act together. For instance, nutrient addition from land is often accompanied by other changes in water quality, such as decreased salinity (McClanahan et al., 2002). The aim of this study was to investigate how corals respond to different stressors that may occur on nearshore reefs (e.g. high nutrient load and low salinity due to heavy rainfall and land runoff) and if the physiological responses were stronger in combination with elevated water temperatures. Hence, the physiological effects on the coral Turbinaria mesenterina exposed to (a) nitrate enrichment, (b) decreased salinity, (c) nitrate enrichment þ decreased salinity was studied at 25 C (ambient) and 31 C (temperature increase) in order to investigate the interactive effects of these stress factors. 2. Methods 2.1. Collection of corals The study was conducted in May 2008 in an outdoor laboratory at Tram Bien Research Station, in Do Son, northern Vietnam. Pieces (e8 4 cm) of the coral species Turbinaria mesenterina were collected close to Co To Island (N 20 58’39”, E 10747’16”), northern Vietnam, at a depth ofe4e8 m. T. mesenterina was chosen since it was the most common coral on the reef, and known to be a very robust species (Marshall and Baird, 2000; Anthony, 2006; Sofonia and Anthony, 2008). After collection, corals were transported to the outdoor laboratory under low light condition and with continuous aeration. Epiphytes and boring organisms were carefully removed before the corals were put in aerated aquaria (20 litre each) with filtered and UV-treated seawater, which were placed in larger water-filled tanks (1 m3) in order to minimise temperature fluctuations (Nordemar et al., 2003). Since T. mesenterina is a foliaceus species, the proportion of tissue affected by the fragmentation during collection was very low, and mucus production was not stimulated. Increased mucus production is a general stress response in corals and commonly used to indicate and exclude damaged specimens of fragmented corals from experimental set-ups. Corals were allowed to acclimate for 48 h in ambient temperature (25 C), under reduced light conditions (154 20 mE m2 s1) and with extra air supply before the experiment started. 2.2. Experimental setup Each coral replicate was put in a 1.5 litre transparent plastic jar; the jars were then placed randomly in the 20-litre aquaria (4 jars in each aquarium), which in turn were placed in four larger waterfilled tanks (1 m3) representing the heat exposure- and control tank respectively. Two tanks for each treatment were used. Aeration pumps mixed the seawater in both the jars and the tanks, thus maintaining high oxygen concentrations and distributing water temperature evenly. The water temperature in the exposure tanks was increased using heating regulators (ZEBO 300 W or FLUVAL Tronic 200 W). In total 24 coral pieces were used in the heat exposed and ambient treatments respectively, thus resulting in 6 replicates for each of the 8 treatments.
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The treatments were: (a) ambient (25 C, 30, 0.3 mM NO 3 ), (b) high nitrate (þ5 mM NO 3 ), (c) low salinity (20), (d) high nitrate þ low salinity, (e) high temperature (31 C), (f) high temperature þ high nitrate, (g) high temperature þ low salinity, (h) high temperature þ high nitrate þ low salinity. The salinity was measured using the Practical Salinity Scale. The heaters were put on and the low salinity was obtained by diluting natural seawater with purified freshwater (to mimic dilution with rainwater). This design lead to a rather rapid increase in temperature and decrease in salinity (experimental conditions within a few hours), but no increased mucus production or retraction of polyps could be observed at this stage, and other studies have shown that salinity can drop very rapid in nearshore areas after heavy rainfalls (from 30 to 15 psu within 24 h; Jokiel et al., 1993). It is also well known that daily temperatures can undergo drastic changes on nearshore reef flats and in coastal lagoons, e.g. 25e33 C within hours (Semesi et al., 2009). The temperature range used in this study is, however, reported to be “normal summer temperatures” in the area (Latypov, 2005). Nitrate was then added to the nutrient enriched treatments as NaNO3. The used concentration has been shown to be ecologically relevant during rainy seasons (Devlin and Brodie, 2005; Costa et al., 2008). Nitrate was used since that is the main form of nitrogen available in tropical waters (Marubini and Davies, 1996) and nitrogen is a common nutrient in land run-off due to agricultural practices (Devlin and Brodie, 2005). The experiment was conducted outdoors under reduced light conditions during the exposure (154 20 mE m2 s1), in order to minimise synergistic effects with high light conditions (Fitt et al., 2001). Corals were exposed for 24 h before their metabolism were measured. 2.3. Productivity measurements The net production and respiration were measured during midday in natural ambient sunlight without additional air supply. During the production measurements, the light intensity was measured every five minutes and varied between 1500 and 2200 mE m2 s1 throughout the measurements, but did not differ between treatments. It should be noted that this irradiance is measured above the water surface (under water meter not available) and that it is lower at the surface of the submerged corals at approximately 0.5 meters depth. However, 2200 mE m2 s1 can be considered “normal” at sea surface in tropical waters (Chalker, 1981). Other studies also report production measurements at 1500e2000 mE m2 s1 (Nyström et al., 2001; Nordemar et al., 2003) above sea surface, and Semesi et al. (2009) report corresponding light values at 1e4 meters to be 300e500 mE m2 s1. According to Chalker et al. (1983), sun exposed corals from shallow waters reach light saturation ate340 mE m2 s1 and we thus assume that the corals used in this experiment are light saturated, i.e. produce at maximum rate. Furthermore, since the increase in light intensity before the measurements was synchronised to the actual sunrise, it can be argued that light should not be considered as an additional stress factor in this experiment. In order to keep a stable temperature during the measurement (i.e. 25 and 31 C respectively), the jars, with the individual corals, were placed inside foam boxes with surrounding water of the accurate temperatures (no light reduction occurred in the boxes). The surrounding water was stirred and temperatures measured every five minutes during the production measurements in the foam boxes, and when necessary, small pieces of ice were added to maintain a stable temperature. Changes in dissolved oxygen concentration in light (net production) and darkness (respiration) were measured according to Moberg et al. (1997) using an oximeter (WTW OXI 330). Between
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2.4. Statistical analyses A three-way ANOVA could not be conducted since all corals in one of the treatment groups died during exposure, therefore a oneway ANOVA was used to analyse the effects of the different treatments. The coral replicates that died during the treatment were excluded from the statistical analyses. Where differences were found, Tukey HSD was used as a post hoc test (p < 0.05). All data were tested for homogeneity of variances using Levene’s test (p < 0.05) before the ANOVA was carried out. For the statistical analyses SPSS 16.0 for Mac OS X was used. 3. Results 3.1. Mortality All corals exposed to the multiple stressors high temperature þ high nitrate þ low salinity died after 24 h exposure, whereas those exposed to high nitrate þ low salinity at ambient water temperature did not show any stress response in GP/R ratio, respiration rate or gross primary production rate (Fig. 1aed) and no mortality occurred. Corals exposed to increased temperature þ low salinity experienced a 50% (n ¼ 3) mortality rate and there was a 33.3% (n ¼ 2) mortality rate for the corals exposed to high temperature þ high nitrate. Only 16.7% (n ¼ 1) of the corals exposed to high temperature alone were dead after the exposure. In contrast, there was no mortality at all among corals exposed to a single stressor at ambient temperature (i.e. low salinity or high nitrate). 3.2. GP/R ratio There were significant differences in GP/R ratio between treatments (GLM ANOVA df ¼ 6, F ¼ 2.676, p < 0.05), where high
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measurements the jars were sealed with tight-fitting lids. An earlier pilot test showed that the most stable and reliable values were obtained after a 1-hour and 1.5 h acclimation period in light and darkness for production and respiration, respectively. Dissolved oxygen concentration was initially measured in light and then again after 1 h. Corals were then placed in darkness and after 1.5 h the oxygen concentration was measured once more and respiration rates calculated. For the statistical analyses respiration rates were converted to 1-hour values. Two water controls (without corals) of each treatment were used. The oxygen saturation levels never dropped below 70% during the measurements. After the experiment was terminated the coral surface area was determined using the aluminium foil method (March, 1970) and to compensate for volume dependent differences in dissolved oxygen concentration, the volumes of the corals were measured by submerging the coral into a graded beaker filled with a known volume of water. Net production rate and respiration rate data were calculated per hour and cm2 coral surface area. Respiration rate was added to the net production value in order to achieve gross primary production rate. Due to the lack of laboratory facilities no biomass of the corals could be measured and neither could the chlorophyll concentrations be analysed, therefore the gross production and respiration are expressed as per cm2 coral surface area according to Moberg et al. (1997). Gross primary production/respiration (GP/R) ratios over both 1 h and 24 h (12 h light, 12 h darkness) were also calculated to get a dimensionless estimate of the physiological status of the corals. GP/R24h estimates the autotrophic capabilities and if GP/R24h 1 it indicates that an organism is self-supporting while a value below 1 indicates that the organism needs to import energy to fulfil their energy demands (Hopkinson and Smith, 2005).
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Fig. 1. Turbinaria mesenterina (mean values SE). a) GP/R ratios (1 h). b) GP/R ratios (24 h). The dashed line indicates GP/R ¼ 1. c) Respiration rates. d) Gross primary production rates. A ¼ ambient temperature, HT ¼ high temperature, HN ¼ high nitrate, LS ¼ low salinity. The dark colour represents all treatments in combinations with high temperature and the light colour represents all treatments in ambient temperature. *p < 0.05, **p < 0.01, ***p < 0.001. y ¼ All specimens in the HT þ HN þ LS combination died.
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temperature þ low salinity had a lower GP/R ratio compared to low salinity (Tukey HSD p ¼ 0.025; Fig. 1a), and ambient water (Tukey HSD p ¼ 0.041; Fig. 1a), and a strong trend for a lower GP/R ratio compared to high nitrate (Tukey HSD p ¼ 0.058; Fig. 1a). There was no difference between high nitrate and high temperature þ high nitrate, and no differences between ambient water temperature and any of the single stressor treatments were found. GP/R24h ratio (Fig. 1b) showed that the corals in ambient water, high nitrate and low salinity had a GP/R24h ratio of 1.0 or slightly above that, indicating that these were energetically self-supporting during the study. In comparison, the corals exposed to high temperature or high temperature þ high nitrate had a GP/R24h ratio of 0.75 and the corals exposed to high temperature þ low salinity had a GP/R24h ratio of 0.30, demonstrating consumption of stored energy for maintenance. 3.3. Respiration and gross primary production rates There were differences in respiration rates between treatments (GLM ANOVA df ¼ 6, F ¼ 6.198, p < 0.001). The high temperature þ low salinity had a higher respiration rate compared to the ambient water temperature (Tukey HSD p ¼ 0.002; Fig. 1c), low salinity (Tukey HSD p ¼ 0.002; Fig. 1c), high nitrate (Tukey HSD p ¼ 0.003; Fig. 1c) and high nitrate þ low salinity (Tukey HSD p ¼ 0.001; Fig. 1c). Moreover, there were no differences between high temperature or high temperature þ high nitrate and any of the treatments in 25 C. In contrast, there were no differences whatsoever in gross primary production rates between any of the treatments (see Fig. 1d), but the variation in the high temperature þ low salinity group seemed to increase. 4. Discussion Our results showed that while those corals that were exposed to low salinity in combination with high nitrate at ambient temperature all survived and were not affected physiologically, the treatment with multiple stressors e high temperature in combination with low salinity and high nitrate e caused mortality to all the specimens within 24 h of exposure. The combination of high temperature and low salinity resulted in a decrease in GP/R ratio, which was explained by an increase in respiration rates. Moreover, a GP/R24h ratio of 0.3 indicated that these corals would have needed a net import of energy corresponding to at least 70% of their energy demand, while on the other hand the corals exposed to low salinity alone had a GP/R24h ratio of slightly above 1.0. Thus, indicating that corals exposed to salinity stress alone can still meet their energy demands through autotrophic production, while corals exposed to the combination of salinity stress and increased water temperature must use their own reserves or import energy for their maintenance (Hopkinson and Smith, 2005). Furthermore, 50% of the corals in the treatment low salinity in combination with high temperature died. It would therefore seem that the effect of low salinity was aggravated by elevated temperature. This is in accordance to Coles and Jokiel (1978) who reported similar results, where the mortality rate increased when corals were exposed to both high temperature and low salinity compared to only high temperature. While there were no initial physiological effects in the treatment with the combination high temperature and high nitrate in this study, the corals exposed to increased temperature alone or in combination with increased nitrate concentration or low salinity all showed a GP/R24h ratio below 1. This indicates that the corals at increased water temperature experience increased energy demand, demonstrated through increased respiration rates, and thus
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became more dependent on stored energy reserves (or feeding) in order to adapt and survive. Other authors have found a more pronounced effect in the combination of high nitrate and high temperature on the gross primary production rate, in comparison to the effects of single stressors (Nordemar et al., 2003), however, both the nitrate concentration was higher and the exposure time longer in that study. Moreover, there was no decrease in the corals’ GP/R ratio when exposed to a single stressor alone: low salinity, high nitrate or high temperature respectively, which indicates that the mode of stress factor application did not per se significantly affect the specimens. Both Moberg et al. (1997) and Alutoin et al. (2001) found a negative effect in terms of decreased GP/R ratio and/or production rates when Pocillopora damicornis and Porites lutea were exposed to the same amplitude of decrease in salinity as in our study. On the other hand Muthiga and Szmant (1987) did not find any effects on gross production or respiration rates of Siderastrea siderea exposed to the same salinity decrease. Thus, this indicates that the effects of a salinity decrease may vary among coral species (Moberg et al., 1997) and/or local area, which might be due to corals being differently adapted to salinity changes. There were no physiological effects from nitrate enrichment alone in this study, which is in accordance with Ferrier-Pagès et al. (2001), who found no effects on zooxanthellae density or photosynthesis with nitrate enrichment (2 mM). Similarly, Marubini and Davies (1996) did not find any effects on gross primary production rates on corals exposed to 1 mM nitrate, but corals exposed to 5 mM showed an increase in gross primary production rates. However, the effect was evident only after 30 days of exposure. A possible reason for the lack of response to nutrient enrichment alone of the corals in this study could be the relatively low dose (which was however ecologically relevant and triggered responses in the study in combination with other stress factors) in relation to the short (24 h) exposure time, or it might be due to temporal differences in the natural nitrate exposure in the Tonkin Gulf, which could have caused acclimatization of the corals and their zooxanthellae to increased nutrient availability. In general, corals can suffer substantial mass mortality during periods of increased water temperature (Wilkinson, 2000). However, some coral species are more tolerant to increased water temperatures than others, e.g. massive Porites (McClanahan, 2000), Pavona spp. (McClanahan et al., 2004), Galaxea spp. (McClanahan et al., 2004) and Goniopora spp. (McClanahan et al., 2004). Turbinaria spp. have also been found to be tolerant to elevated water temperatures (Marshall and Baird, 2000), which might explain why there was no significant decrease in GP/R ratio to the single stress factor increased temperature in this study. However, when recalculating the GP/R ratio to a 24 h basis, it is clear that all high temperature treatments have GP/R24h ratios below 1, which indicate that the corals are not self-maintained through primary production. Furthermore, one of the specimens died after exposure to heat alone, which may be explained by individual variation in temperature tolerance. At least during short periods of time it seems that corals can withstand acute exposure from land-based pollution (e.g. decreased salinity and/or nitrate enrichment), however in combination with elevated seawater temperatures, it can lead to mortality within 24 h, as it did in this study. Freshwater inflow, enhanced nutrients and increased water temperatures usually correlate in the field, e.g. during the rainy season (Lapointe, 1997). In this study the temperature used was e0.5 C above normal summer maximum temperature in the study area (Dr Cu unpubl. data). Hence, this suggests that when corals are exposed to land run-off and heavy rainfall, only a slightly higher temperature than normal summer maximum might be enough to cause coral bleaching and eventually mass mortality.
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5. Conclusion It has been suggested that areas where local anthropogenic stressors (e.g. overfishing and land-based pollution) are kept to a minimum will have a higher resilience (i.e. higher recovery rate) after a bleaching event than areas subjected to multiple stressors (Sandin et al., 2008; Smith et al., 2008; but see Graham et al., 2006). It is therefore important to eliminate factors that may aggravate the effects of climate change, since the highest extinction risk will most likely be in areas were local anthropogenic disturbances are more frequent (Carpenter et al., 2008). Furthermore, non-point source pollution is predicted to increase in the future, due to more nutrient use in the agricultural ecosystems, urbanization and a growing human population (Carpenter et al., 1998). While this study only focus on one coral species, T. mesenterina, it is quite possible that the results may be applicable also to other coral species. Especially since this species have been found to be tolerant not only to increased water temperature (Marshall and Baird, 2000) but also turbidity (Anthony, 2006; Sofonia and Anthony, 2008), and other coral genera might be more sensitive to rapid environmental fluctuations. If so, good water quality may be of utter importance, since elevated temperature may cause lethal synergistic effects on corals exposed to other disturbances. Indeed, improved water quality has been suggested to enhance the resilience in corals to increased water temperatures (HoeghGuldberg et al., 2007; Hughes et al., 2007).
Acknowledgements This study was financed by Stockholm Marine Research Center (SMF) and Swedish International Development Cooperation Agency (Sida). Thanks to the staff at Tram Bien Research Station in Do Son for assistance. Thanks to M. Nyström, M. Björk and M. Gullström for valuable comments.
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