Impact of Bleaching on the Coral Cladocora Caespitosa in the Eastern Adriatic Sea

Vol. 509: 193–202, 2014 MARINE ECOLOGY PROGRESS SERIES Published August 27 doi: 10.3354/meps10962 Mar Ecol Prog Ser

Impact of bleaching on the coral Cladocora caespitosa in the eastern Adriatic Sea

Petar Kruži´c1,*, Lovrenc Lipej2, Borut Mavriˇc2, Petra Rodi´c3

1Laboratory for Marine Biology, Department of Zoology, Faculty of Science, University of Zagreb, Rooseveltov trg 6, 10000 Zagreb, Croatia 2Marine Biological Station Piran, National Institute of Biology, Fornaˇce 41, 6330 Piran, Slovenia 3State Institute for Nature Protection, Trg Mažurani´ca 5, 10000 Zagreb, Croatia

ABSTRACT: Thermal anomalies during the last 15 yr caused bleaching in the zooxanthellate scleractinian coral Cladocora caespitosa (Linnaeus, 1767) in the eastern part of the Adriatic Sea. In this study, we assessed the long-term response of this temperate coral to warming seawater in the Adriatic Sea and described, for the first time, the relationship between recurrent coral bleaching events and local seawater temperature regimes. These were also the first coral bleaching events reported for the Mediterranean Sea. Coral bleaching was recorded in the period from 1997 to 2012 in Veliko Jezero within Mljet National Park (NP), Croatia. The most severe bleaching in Veliko Jezero was observed during the summer of 2003, when C. caespitosa colonies were exposed to temperatures >29°C for 46 d. A total of 426 colonies experienced partial bleaching and 133 colonies died due to complete bleaching. Bleaching results during 2011 were compared with bleaching events in the Piran area (Slovenia) over this same temporal interval. The highest seawater temperatures were recorded in the period from August to October of 2011 (28.8°C in Piran, 30.3°C at Mljet NP). Severe bleaching was observed on 54 (29.3%) colonies within the Mljet coral bank, while 39 colonies with complete bleaching died. In the Piran area, severe bleaching was observed on 26 (34.7%) colonies, while complete bleaching occurred in 8 (10.6%) colonies. Under the present climate-warming trend, the coral bleaching reported here could lead to a severe decline in the abundance of the surveyed populations of C. caespitosa.

KEY WORDS: Cladocora caespitosa · Coral bleaching · Coral mortality · Adriatic Sea

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INTRODUCTION bleaching and subsequent mortality as they have become increasingly exposed to higher-than-normal During the last 2 decades, the Mediterranean Sea sea water temperatures (Glynn 1991, Brown 1997, has experienced warming at a rate higher than nor- Hoegh-Guldberg 1999, McWilliams et al. 2005, Gar- mal (Garrabou et al. 2009, Lejeusne et al. 2010, Kruži´c rabou et al. 2009, van Woesik et al. 2011, Kruži´c et et al. 2012, Kersting et al. 2013). These increases in al. 2012). Mass coral mortality is common in tropical seawater temperature in the Mediterranean vary re - seas, where major bleaching events coincide with the gionally, and temperature oscillations seem to onset of elevated seawater temperatures within areas change with time (Garrabou et al. 2009). As a result such as the Caribbean Sea and the Pacific and Indian of these recent climatic trends, significant changes Oceans (Brown 1997). Elevated seawater tempera- have occurred in marine ecosystems, such as an in - tures predicted for the future may increase the fre- crease in mass mortality within coastal ecosystems. quency of coral bleaching events and subsequent Corals have experienced increased frequency of mass mortality.

*Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 194 Mar Ecol Prog Ser 509: 193–202, 2014

Reef formations like those in warm tropical waters caespitosa to warming seawater was described in also occur in higher latitudes, but with lower diver- studies conducted in the Columbretes Islands (NW sity and abundance (Zibrowius 1982, Bianchi 2001, Mediterranean) (Kersting et al. 2013). The relation- 2009). One of the major carbonate producers in ship between recurrent mortality events and local the Mediterranean Sea is the zooxanthellate and sea surface temperature regimes in the Mediterran- colonial scleractinian coral Cladocora caespitosa ean Sea resulted in mortality from tissue necrosis (Linnaeus, 1767) (Peirano et al. 2001a,b, Kružić & without polyp bleaching. Požar-Domac 2003). The hemispherical bush-like The central objective of this study was to investi- colonies of C. caespitosa live solitarily or form ‘beds’ gate the impact of mass bleaching events on C. cae- (numerous colonies living more or less close to each spitosa in the eastern Adriatic Sea from 1997 to 2012. other) or ‘banks’ (colonies connected together in a The effects of the 2011 mass bleaching event on C. large formation more than 1 m high and covering caespitosa at 2 locations in the eastern Adriatic Sea several square meters) (Zibrowius 1980, Kühlmann were also studied. At each location, we quantified et al. 1991, Schiller 1993, Morri et al. 1994, Peirano et bleached colonies, bleaching intensity, depth range al. 1998, Kružić & Požar-Domac 2003, Kružić & affected, and timing of the bleaching event. Benković 2008). C. caespitosa is well adapted to the seasonality of the Mediterranean Sea, which experiences large MATERIALS AND METHODS variations in seawater temperature (Morri et al. 2001, Rodolfo-Metalpa et al. 2006a). In the Adriatic Sea, Sampling locations for example, sea surface temperatures range from 8°C during the winter in the north (with strong influ- We evaluated Cladocora caespitosa populations in ence of north-eastern bora wind during Feb ruary Veliko Jezero in Mljet NP on the island of Mljet, in and March), to up to 29°C in the summer in the south the southern part of the Adriatic Sea (Croatia) (42° 46’ (Schiller 1993, Kružić & Benković 2008). Several mor- 0’’ N, 17° 22’ 8’’ E), and in the Cape Madona marine tality events have coincided with high-temperature natural monument near the town of Piran (45° 31’ anomalies in seawater temperature, affecting a range 50’’ N, 13° 33’ 49’’ E) in the northern part of the Adri- of sessile invertebrates including C. caespitosa in atic Sea (Slovenia) (Fig. 1). The first site is located in the Ligurian and Adriatic Sea (Rodolfo-Metalpa et Veliko Jezero, a ‘lake’ depression that was flooded al. 2000, Kružić & Benković 2008). When exposed to by seawater during the most recent postglacial pe- these thermal anomalies, C. caespitosa often suffers riod. The ‘lake’ is open to the surrounding sea extensive tissue loss directly through tissue necrosis through a narrow channel (Soline channel). The C. or after bleaching, resulting in the total or partial caespitosa bank is situated near the entrance of the mortality of colonies. The long-term response of C. saline lake and extends for approximately 650 m2, at

Fig. 1. Study sites at Piran (Slovenia) and Mljet National Park (Croatia), where Cladocora caespitosa bleaching events were observed Kruži´c et al.: Coral bleaching in the Adriatic Sea 195

a depth of 6 to 18 m (Kruži´c & Požar-Domac 2002, centage of the colony area affected by bleaching 2003). Colony sizes ranged from 15 to 60 cm in diam- was quantified from the estimated number of colony eter. Strong sea currents, which occur as a result of polyps. tidal exchange in the Soline channel, appear to favor the growth of the C. caespitosa bank. The second site, the marine natural monument Cape Madona, is Quantification of seawater temperature situated at the very end of Cape Madona, where the oldest part of the historic town of Piran is located. Seawater temperatures at the investigated loca- Coral colonies (15 to 30 cm in diameter) spread as tions were recorded (with accuracy ±0.2°C) at 1 h a coral bed about 50 m from the cape, at 3 to 8 m intervals using HOBO Pendant temperature loggers depth, on a rocky substrate affected by moderate sea (Onset Computers Corporation). Data loggers were currents. set at a depth of 3 m in Piran (central part of coral bed) and at a depth of 8 m at Mljet NP (central part of coral bank) fixed on the nearby rock with metal pins. Quantification of bleaching in C. caespitosa The data were downloaded annually.

The bleaching of C. caespitosa was investigated by SCUBA-diving. At the C. caespitosa bank in Veliko Statistical methods Jezero, 50 m long transect lines marked at 5 m intervals were used to make 25 m2 frames. We counted all Differences in the densities of bleached colonies bleached coral colonies within these frames and clas- at different depth ranges were analyzed using a sified the extent of their bleaching. The frame was 1-way ANOVA. Tukey tests were used for post-hoc moved along the bank until all bleached corals were comparisons. Prior to analysis, the homogeneity of identified and counted. Each bleached colony was variances was verified by Cochran’s test. We used marked with a metal stick flag to avoid repetitive nonparametric analysis because the data followed counting. Bleaching was quantified within the C. neither normality nor homogeneity of variances caespitosa bank in Veliko Jezero from 1997, when after different transformations. The Kruskal-Wallis the first bleaching events were ob served in summer analysis was used to test for differences in bleach- and autumn (July, August, September and October), ing depending on colony size (diameter size to 2012. Coral bleaching on the Piran coral bed was classes: <25, 25−50, >50 cm). The Kolmogorov- quantified within 1 m on either side of each 10 m Smirnov 2-sample tests were used to determine transect in summer and autumn (August, September whether there were significant differences in coral and October) of 2011. By moving the transect every bleaching between months in which bleaching was 2 m we covered all coral bed areas. Each bleached observed during 2011 in both researched areas. colony was marked, the size of colonies quantified Significant differences were assessed at p < 0.05 and then colonies were photo graphed with an under- or at p <0.01. Results are presented as mean ± SD water camera for determination of possible polyp throughout. A regression analysis between the recovery. number of bleached colonies and seawater tem- Coral bleaching leads to a change in coloration of peratures from 1997 to 2012 in Mljet NP was coral tissue due to a decrease in abundance of the performed to explore the potential role of the symbiont Symbiodinium or the decline in photo - high temperatures in the C. caespitosa bleaching. synthetic pigments (Brown 1997, Glynn 1991, Hoegh- The analyses were carried out using Statistica 10.0 Guldberg 1999). The maximum bleached surface software. area within each coral colony was assigned one of 3 categories—(a) minor bleaching: less than 30% of the colony surface area was bleached, (b) severe RESULTS bleaching: 30 to 99% of the colony surface area was bleached, and (c) complete bleaching: 100% of the Bleaching of Cladocora caespitosa in Mljet NP colony surface area was bleached. Coral recovery was defined as the re-coloring of the bleached Research on the bleaching of C. caespitosa in Mljet colonies. The number of bleached polyps per colony NP began in 1997, when bleached polyps were first was estimated in situ by counting the number of recorded and studied (Fig. 2). During that year, polyps in 10 replicated 5 × 5 cm squares. The per- 269 colonies bleached and a total of 119 colonies 196 Mar Ecol Prog Ser 509: 193–202, 2014

that experienced severe bleaching died. Bleaching August or the beginning of September. In the 15 yr rates within the coral bank showed high variability since 1997, coral bleaching was observed in the Mljet between colonies, as affected and unaffected colonies coral bank in all but 3 years (2000, 2005 and 2010). were commonly found next to each other. The first There was a positive relationship between the num- signs of bleaching were usually detected during ber of days when seawater temperatures exceeded 28°C, and years with evident coral bleaching (Fig. 2). In 1997, 1999, 2003, and 2006, summer maximum temperatures measured at 8 m depth, along with number of days with temperatures >28°C, were among the highest values recorded in Mljet NP over the studied interval (Fig. 3a, Table 1). The most severe bleaching was observed during the summer of 2003 (Fig. 3b, Table 1). During the 2003 event bleached polyps represented, on average, 27% (27.14 ± 7.02%) of each ob served colony. Extensive coral bleaching was also recorded during the summers of 1997, 1999 and 2006 (Table 1). No significant differences Fig. 2. Prevalence of bleaching and mortality of the coral Cladocora caespitosa in polyp bleaching among various throughout the study in comparison to average summer seawater temperature (at 8 m depth) in Veliko Jezero (Mljet National Park) in the southern Adriatic depth ranges were found during the Sea. Arrows: years without coral bleaching events study period within the C. caespitosa bank (1-way ANOVA, F2,152 = 0.522, p = 0.681). Also, no significant differences were found between polyp bleaching and colony size (Kruskal- Wallis test, H = 9.27, df = 7, p = 0.506). The number of bleached colonies within the Mljet NP coral population was positively correlated (r = 0.88113, p < 0.01) with seawater tempera tures from 1997 to 2012 in Mljet NP (Fig. 4). A higher impact on coral populations was observed in areas experiencing a greater amount of time above a maximum temperature threshold.

Bleaching of C. caespitosa in Mljet NP and Piran during 2011

During 2011, the highest seawater temperatures in the Adriatic Sea oc - curred from August to October (Fig. 5). The maximum seawater temperature values during the summer period in 2011 in Mljet NP and Piran are sum- marized in Table 2. In Veliko Jezero Fig. 3. (a) Days per year with temperatures above 26, 27, 28 and 29°C and (b) percentage of bleached polyps per colony (mean + SE) detected in Mljet (Mljet NP) the highest seawater tem- National Park from 1997 to 2012 perature was measured during August Kruži´c et al.: Coral bleaching in the Adriatic Sea 197

Table 1. Years with Cladocora caespitosa bleaching events, number of days that corals experienced water temperatures above >28°C, total number of bleached colonies, dead col - onies as a result of bleaching, and the mean (±SE) percentage of bleached polyps in each observed colony at Mljet National Park, Croatia, between 1997 and 2006

Year >28°C No. of No. of Bleached (d) bleached dead polyps (%) colonies colonies

1997 93 269 119 22.16 ± 7.34 1999 101 187 63 26.28 ± 5.19 2003 89a 426 133 27.14 ± 7.02 2006 93 201 76 16.07 ± 3.16 aTemperature was >29°C for 46 d

(30.3°C) in the central part of the coral bank, while in the Piran area, the highest seawater temperature was measured at the end of August (28.8°C). During the summer of 2011, coral colonies in Mljet NP were exposed to temperatures >27°C for 103 d, and to tem- Fig. 5. Sea temperature oscillations measured in (a) Veliko peratures >28°C for 69 d, while colonies in the Piran Jezero (Mljet National Park) (8 m depth) and (b) Piran (3 m area were exposed to temperatures >27°C for 19 d depth) during the summer and autumn of 2011. Arrows: high seawater temperature periods (temperature anomalies) and to temperatures >28°C for 5 d (Fig. 6a). Summer temperature conditions were much warmer in Mljet NP than in Piran in 2011, with a considerably higher area (Fig. 6b). In October 2011, there were fewer number of days per year with temperatures above 26, recorded bleaching events in both areas (20.18 ± 27 and 28°C occurring in Mljet NP. 12.27%, and 19.19 ± 7.04% in Mljet NP and Piran, In the Piran area, coral bleaching substantially respectively). In Mljet NP, 21.2% of all C. caespitosa affected C. caespitosa colonies for over 3 mo (from colonies in the Mljet bank suffered coral bleaching; August to October), whereas the colonies from the 39 colonies experienced complete bleaching and Mljet bank were affected for over 5 mo (from July to died during 2011 (Table 2). There was no evidence of November). In August 2011, average coral bleaching coral disease within the monitored C. caespitosa (bleached polyps per colony ± SE) was 31.29 ± bank during this study. Minor bleaching was ob - 14.01% in Mljet NP and 37.31 ± 17.56% in the Piran Table 2. Timing of Cladocora caespitosa bleaching and maximum values of seawater temperature (°C) during 2011. All numbers represent newly affected colonies during this period

Sampling date Seawater Bleaching of colonies (°C) Minor Severe Complete

Mljet (Croatia) 27 July 2011 27.6 16 7 4 25 August 2011 30.3 31 17 12 21 September 2011 28.3 19 12 11 22 October 2011 27.9 15 10 9 15 November 2011 25.8 10 8 3 Total 91 54 39 Piran (Slovenia) 31 August 2011 28.8 3 0 0 Fig. 4. Relationship between the number of bleached Clado- 15 September 2011 26.3 5 5 3 cora caespitosa colonies and seawater temperatures from 06 October 2011 24.1 33 21 5 1997 to 2012 in Mljet National Park. Solid line: regression Total 41 26 8 (r = 0.88), dashed line: 95% CI 198 Mar Ecol Prog Ser 509: 193–202, 2014

served in 91 (49.5%) colonies, while 54 (29.3%) colonies experienced severe bleaching within the Mljet coral bank. At the end of August, an extensive bleaching event was observed in the Mljet coral bank: 12 colonies experienced complete bleaching, 17 colonies experienced severe bleaching, and 31 colonies experienced minor bleaching (Fig. 7a,b, Table 2). In the Piran area, minor bleaching was observed on 41 (54.7%) colonies, with severe bleaching recorded in 26 (34.7%) colonies (Fig. 7c,d, Table 2). Overall, 8 colonies (10.6%) of the C. caespitosa population that were investigated experienced complete bleaching in 2011 (Table 2). There were no records of whole colony mortality (only partial) caused by bleaching in the Piran area. The most substantial bleaching event in the Piran area was observed at the beginning of October, when 5 col - onies suffered complete bleaching, all with sub - sequent complete recovery. Severe bleaching was observed in 21 colonies, while minor bleaching impacted 33 colonies. After 1 mo, colonies began to show signs of apparent recovery (re-coloring) from the bleaching event. There was also no evidence Fig. 6. (a) Days per year with temperatures above 26, 27, 28 and 29°C in 2011 and (b) percentage of bleached polyps per of coral disease in the C. caespitosa colonies within colony (mean + SE) detected in Mljet National Park and Piran the Piran area.

Fig. 7. (a,c) Partially bleached colonies of Cladocora caespitosa (translucent polyps) and (b,d) coral mortality after a bleaching event (white coral skeleton) at (a,b) Mljet National Park and (c,d) Piran Kruži´c et al.: Coral bleaching in the Adriatic Sea 199

No significant differences were found between coral (P. Kruži´c pers. obs.). Thus it was not possible to con- bleaching and colony size in either area (Kruskal- fuse the old bleaching events with the new one. A Wallis test, H = 8.29, df = 6, p = 0.522 for Piran and H similar process was observed after C. caespitosa mor- = 6.73, df = 3, p = 0.493 for Mljet). The average per- tality events in Columbretes Islands (NW Mediter- centage of coral bleaching was significantly higher ranean) (Kersting et al. 2013). during August than October in both areas (Kolmo - During thermo-tolerance experiments with C. cae- gorov-Smirnov test, p <0.01 for both tests). spitosa in aquaria, the first signs of polyp necrosis were detected after 5−7 weeks at 24°C, and all polyps that were exposed to 26 and 28°C died DISCUSSION after the treatments (Rodolfo-Metalpa et al. 2006a,b). Based on these results, those authors proposed that Over the last 2 decades, extensive mass mortalities C. caespitosa lives close to its thermal limit during of at least 25 rocky benthic macroinvertebrate spe- the summer period in the Ligurian Sea and that a cies (mainly gorgonians and sponges) were observed long-term increase to 24°C or above could prove fatal across the entire Mediterranean region (Cerrano et for the Ligurian population. However, short-term al. 2000, Garrabou et al. 2009). Heat waves occurring (48 h) experiments conducted with water tempera- during summer periods in the Mediterranean region tures at 32°C did not result in algal loss or mortality in caused an anomalous warming of seawater, be tween the coral C. caespitosa, confirming that zooxanthellae 1 and 3°C above average climatic values. The tem- can be resistant to temporary increases in tempera- perature anomalies were usually limited to shallow tures (Rodolfo-Metalpa et al. 2006a). The absence of layers (<20 m depth) due to the calm weather condi- bleaching in the short-term exposures is most likely tions between June and September (Spar nocchia et related to the resistance to increased temperatures al. 2006). Mediterranean corals and gorgonians have exhibited by the dinoflagellate symbiont Symbio- been severely affected by temperature-related mor- dinium sp. in C. caespitosa (Rodolfo-Metalpa et al. tality (Cerrano et al. 2000, Rodolfo-Metalpa et al. 2006b). The expulsion of zooxanthellae from C. cae- 2005, 2006a). During the mortality events of the sum- spitosa polyps was recorded in laboratory aquaria mers of 1997 and 1999 in the Ligurian Sea, a total of with seawater temperatures of 30°C, during a 7 d 50% of the C. caespitosa colonies died due to tissue exposure (P. Kruži´c unpubl. data). Longer exposure necrosis, not caused by bleaching events (Rodolfo- times (4 wk) resulted in the loss of almost all Metalpa et al. 2000, 2005). Bleaching events in the symbionts. In the field, coral colonies are naturally Mediterranean were previously found only in inva- subjected to different thermal regimes, and aquaria sive zooxanthellate colonial coral Ocu lina patagonica experiments can only partially simulate natural en - de Angelis, 1908, also caused by a negative impact vironmental conditions, which must be considered of high sea temperatures (Rodolfo-Metalpa et al. when conducting these ex situ experiments. 2006a,b). We detected the same bleaching and mortality pat- In our study, C. caespitosa mortality was observed tern for both study populations (in Mljet NP and in only in areas with mean summer temperatures at the Piran area), even though they were carried out in least 1 to 2°C above those previously recorded along 2 geographically separate areas of the Adriatic the eastern Adriatic coast. Shallow-water popula- Sea. Our observations indicate that temperatures of tions of C. caespitosa were clearly decimated after 26−27°C can be considered the threshold for trig - the 2003 and 2011 outbreaks in Mljet NP and Piran gering C. caespitosa bleaching (Table 2). However, area, respectively, with mortality rates similar to bleaching observed during lower temperatures in those reported for tropical seas (Brown, 1997, Hoegh- November (24−25°C) could be explained as a rem- Guldberg 1999, Hughes et al. 2003, van Woesik et nant of the negative effects of higher temperatures al. 2011). C. caespitosa colonies living at shallower during the earlier summer months. Possible varia- depths were more exposed to thermal stress and tions in coral bleaching could be a result of different showed greater mortality rates. Total mortality of the ecological conditions of the habitat. Different popula- colonies (100% necrosed polyps) was mostly due to a tions that are normally exposed to contrasting tem- single mortality event, rather than to the accumu- perature regimes can exhibit differential resilience to lated necrosis from multiple, recurrent bleaching global warming (Hughes et al. 2003). Thermal stress, events. Within 2 mo after mortality, the denuded like diurnal sea temperature oscillations in summer white skeleton was progressively covered by epi - and winter could be a reason for the occurrence of bionts, mostly by algae, hydrozoans and bryozoans bleached polyps in C. caespitosa colonies. Consider- 200 Mar Ecol Prog Ser 509: 193–202, 2014

able sea temperature oscillations observed in the quickly acclimate and begin to recover, as opposed Mljet coral bank could be related to the strong tidal to heat-stressed corals (P. Kružić pers. obs.). This exchange present within the saline lake. These events ability of corals to recover after cold-water bleaching were measured during the whole year, especially in suggests that C. caespitosa is better adapted to summer and autumn (Kružić & Benković 2008). The withstand low temperature than high temperature highest sea temperature oscillations were measured anomalies. These findings indicate that C. caespitosa in Veliko Jezero during the summer in August (up to colonies react differently to temperature differences, 5.9°C during the 1 d period) and during the winter in which is critical for future management of corals in January (up to 3.6°C during the 1 d period). the realm of climate change. Tropical corals can recover after experiencing High-temperature conditions can be concurrent bleaching, but their recovery from a bleaching event with observations of mass mortalities (Bianchi 2007, may take several years or decades (Porter et al. 1989, Lesser et al. 2007). Similarly, seawater temperature Brown 1997, Suzuki et al. 2003). In the Mljet coral was one of the main factors triggering C. caespitosa bank, all colonies that suffered complete bleaching bleaching events in the present study. However, the died and recovery of bleached polyps was not ob- differences found in bleaching extent among years served. However, most bleached colonies in the Piran with similar thermal anomalies indicate that other area did not show tissue necrosis and were able to re- ecological factors (e.g. high irradiance) could also cover. This may be explained by the high food avail- have an effect on this process. A decrease in the pho- ability (mostly organic matter), which could modulate tosynthetic efficiency of the zooxanthellae usually the effects of heat stress on photosynthetic capacity occurs under conditions of elevated temperature and for symbionts within the coral. Several studies have light (Rodolfo-Metalpa et al. 2006a). Light has been shown the importance of coral heterotrophy as a po- demonstrated to stimulate coral growth rates, but tential mechanism for colony survival through bleach- high level of irradiance decrease skeletal extension ing events (Borell et al. 2008, Hoogenboom et al. rate (Jones et al. 2000, Grottoli 2002). Under ex- 2012). The extreme temperature conditions present tremely high light intensity the photoinhibition of during these bleaching events could have been re- zooxanthellae can be a significant problem and lead sponsible for a delayed physiological re sponse within to bleaching events (Hoegh-Guldberg 1999). the colonies, influencing the mortalities recorded the The coral C. caespitosa could be used as an indica- following summers, when tem perature anomalies were tor species for future research regarding the chang- relatively low. This could explain why we recorded ing Mediterranean climate, allowing for the study of different responses in C. caespitosa bleaching in the influence of climate cycles on species from tem- summers with similar temperature anomalies. perate seas (Peirano et al. 2004). However, only Coral mortality due to low temperatures has also continued monitoring of the populations affected by been observed (Glynn & D’Croz 1990, Coles & climate changes will help us to elucidate the long- Fadlallah 1991), but it has only recently been shown term consequences of these events. A long-term that cold stress also leads to bleaching, by impairing series (over several decades) of biological and tem- the function of photosystem II (LaJeunesse et al. perature data will allow for better establishment of 2007). In the Piran area, a few bleached C. caespitosa the linkages between bleaching events and tempera- colonies were found during the winter season. This ture conditions, and for prediction of future tempera- bleaching could have been related to cold stress that ture dependent population development. The ongo- occurs during the winter season, when the area is ing bleaching event is the most severe reported to exposed to cold winds for an extended period of date in the Mediterranean. Under the present cli- time, a typical occurrence in the northern Adriatic. mate warming trend, new mass mortality events of In Mljet NP, similar cold bleaching events could be sessile marine invertebrate fauna may occur even seen during the winter season, but also during the more frequently during the next several decades, summer. Due to the tidal exchange, the thermocline possibly causing a major biodiversity crisis in the in the Veliko Jezero saline lake varies in depth, and Mediterranean Sea. cold layers occasionally reach the lower part of the coral bank (16 m depth), lowering the surrounding water temperature from 26 to 9°C. The cold-bleached Acknowledgements. We express our gratitude to all our colleagues and staff from the Mljet National Park, Marine Bi- corals seem to cope much better with prolonged ology Laboratory, Faculty of Science, Zagreb (Croatia), and exposure to cold temperatures than heat-bleached the Marine Biological Station Piran − National Institute of Bio - corals do during prolonged hot temperatures. They logy Piran (Slovenia) for their fieldwork and laboratory help. Kružić et al.: Coral bleaching in the Adriatic Sea 201

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Editorial responsibility: Brian Helmuth, Submitted: March 11, 2013; Accepted: July 22, 2014 Nahant, Massachusetts, USA Proofs received from author(s): July 30, 2014