Coral bleaching, loss of symbiotic algae (zooxanthellae) and/or their photosynthetic pigments by zooxanthellate reef-builders is considered a major threat for coral reefs worldwide (Lesser 2011), especially because large-scale bleaching events have been related to global warming (Goreau and Hayes 1994, 2005). Mortality related to coral bleaching has caused global decline in coral cover (Goreau et al. 2005, Wilkinson 2008) and local extinction of several species (Riegl 2002, Sheppard 2006).

Coral bleaching events have increasingly affected coral reefs on a global scale in recent years (Goreau and Hayes 1994, 2005, Coles and Brown 2003, Meissner et al. 2012). Bleaching can be predicted with high accuracy when seawater temperature anomalies exceed 1°C above the maximum normal monthly average summer temperature for one month; its severity increases according to the extent and duration of the anomaly (Goreau and Hayes 1994, 2005). For example, a 3-4°C temperature anomaly for a few days can lead to coral death (Buchheim 2005).

The most destructive global coral bleaching events reported have occurred worldwide in the last three decades (Goreau and Hayes 1994, 2005, Goreau et al. 2000, Wilkinson 2004, 2008, Riegl et al. 2011, Guest et al. 2012), including in the Persian Gulf (Rezai et al. 2004, Riegl and Purkis 2009, Riegl et al. 2011).

The Persian Gulf, a semi-closed sea (Fig. 1), is known as one of the most extreme environments for coral reefs, with high salinity (up to >39psu), high sea surface temperature fluctuations from 12°C in winter (Sheppard et al. 1992) to 38°C in summer (Baker et al. 2004), a high sedimentation rate and low water circulation, particularly in the southern part of the Gulf (Riegl and Purkis 2012). The Persian Gulf is considered the hottest coral sea in the world. Temperature conditions associated with coral bleaching in the Persian Gulf are higher than in any other region in the world (Goreau and Hayes 1994, 2005, Sheppard 2003), so some corals in the Persian Gulf can stand summer temperatures up to 10°C higher than corals elsewhere (Coles and Riegl 2013). Nevertheless, the coral reefs in the Persian Gulf are also vulnerable to temperature anomalies and their long-term impacts (Burt et al. 2011).

This paper studies the spatial variation in bleaching susceptibility of corals from some Iranian islands in the northern and central Persian Gulf during a coral bleaching event observed in 2012. To this end, we examined the responses of coral communities and reefs based on the bleaching status of individual colonies (i.e. fully bleached, mostly bleached, partially bleached or healthy). We also compared genus-specific responses. Moreover, from the analysis of temperature data sets available, we suggest 33.5 to 34°C as the coral bleaching threshold temperature in the northern Persian Gulf, which is about 1.5 to 2.5°C lower than the threshold suggested for the southern part of the Gulf (35 to 36°C). This work, which is the first quantitative assessment of a bleaching event in the northern Persian Gulf and Bu-Musa Island, provides valuable data which can be used as a baseline for studies on ecological and physiological changes in the coral communities and their responses to future bleaching events in this region.

The 2012 coral bleaching in the northern Persian Gulf, including Larak, Hormuz and Qeshm Islands, had a great incidence, affecting about 84% of the coral colonies surveyed. Monthly average SSTs were warmer in 2012 than in previous years (Table 1). Although SSTs are not always an accurate indicator of changes in temperature in submerged coral reefs because of significantly cooler temperatures in deeper waters (Sheppard 2009), shallow depth (3 to 5 m during the study), and high wave and tidal current mixing of the surface and bottom waters, there were almost no differences between SSTs and seabed temperatures based on in situ data recorded by dive computers (Fig. 2).

Although Coles and Riegl (2013) mentioned 35 to 36°C as a coral bleaching threshold temperature in the Persian Gulf, the coral bleaching threshold temperature in the northern Persian Gulf is likely 1.5°C to 2.5°C lower. Cooler waters, higher water circulation, connection to the Straits of Hormuz and fewer disturbances have been suggested as explanations for different maximum average summer temperatures (Thoppil and Hogan 2010) and probably for different coral bleaching threshold temperatures in the southern and northern Persian Gulf.

The 2012 bleaching event described in this study was concomitant with temperature highs of 34°C on many days over an approximate one-and-a-half-month period (Fig. 2), resulting in massive coral bleaching at all study sites in the northern Persian Gulf (Fig. 3). Kavousi et al. (2011) reported that reef-building corals of Qeshm Island experienced 33°C temperatures in August and September 2009 with no bleaching event. These temperature conditions coincided with SST data in this study and show that from late July to mid-September temperatures were about 33°C on the majority of days (Fig. 2).

In contrast with 2012, monthly average SSTs at our study area in August and September 2010 were 1 and 0.6°C higher than the highest temperatures in the same months of other years (Table 1), but no coral bleaching was reported in the northern Persian Gulf whereas more than 60% of corals in the southern and central parts were bleached (Riegl et al. 2011). Field observations at Larak Island during the summer and autumn of 2010 confirmed that there was no massive bleaching, but there were three partially-bleached colonies and a few colonies with discolouration were recorded (Parviz Tavakoli-Kolour, personal observation). Temperature anomalies based on the monthly average temperatures were probably 1.6 and 1.2°C for July and August 2012, with no anomaly for September (Table 1).

A comparison among monthly average temperatures (Table 1) suggests that the threshold monthly average temperature was about 33.8°C at our study sites. This finding is based on using the minimum monthly average temperature at which bleaching happened (33.8°C in 2012) compared with the maximum monthly average temperatures at which it did not (33.6°C in September 2010 and 33.7°C in July 2012; Parviz Tavakoli-Kolour, personal observation). However, the 2012 bleaching in the northern Persian Gulf could be because of the longer duration of the 2012 temperature anomaly than in 2010 (two months and one month, respectively). Therefore, it is difficult to suggest an exact temperature as the possible bleaching threshold temperature for corals in the northern Persian Gulf in this study owing to a lack of precise temperature data; however it is probably a temperature between 35.5 and 34°C. It should be noted that temperature records correspond to discrete measurements from SST data and future studies should obtain high temporal resolution data using autonomous temperature data loggers.

The 2012 coral bleaching event bleached more than 84% of coral colonies observed in this study in the northern Persian Gulf, but only 12% of corals recorded from Bu-Musa Island located in the central gulf (Fig. 3; significant difference p<0.05). There was no major bleaching, but discolouration of a few colonies was observed in the southern part of the Persian Gulf (Dr. John Burt, personal communication). Therefore, the northern Persian Gulf was warmer than the southern part (spatial heterogeneity) in 2012 and in 2007 (Wilkinson 2008).

In general, previous bleaching reports have indicated that massive corals tend to have higher survival from thermal stress, especially Porites (Goreau et al. 2000) Favia, Favites and Platygyra (Loya et al. 2001, McClanahan 2004). This contrasts with branching corals, which are among the most vulnerable to thermal stress (Goreau et al. 2000, Loya et al. 2001, McClanahan 2004). Although the bleaching pattern at Bu-Musa Island was coincident with the above information, branching Acropora and Stylophora recorded at Larak Island were less affected by the bleaching than massive Porites (Table 2).

Miller et al. (2011) also reported no bleaching for Acropora palmata at Navassa Island in 2006, whereas other corals studied, including massive corals, were severely bleached. Guest et al. (2012) reported the same phenomenon (more tolerance of susceptible taxa than massive corals) in extremely muddy waters from Singapore. They concluded that it was an adaptive response to anomalous temperatures, but it is difficult to say whether this was because of acclimatization to elevated temperatures or adaptation via more thermally tolerant genotype selection of coral populations (van Woesik et al. 2012) or simply the well-known higher survival rate of these corals in turbid environments (Goreau et al. 2000).

Turbid waters have been noted to reduce coral mortality in severe bleaching events because solar irradiance acts to amplify thermal stress (Goreau et al. 2000, Takahashi et al. 2004, Golbuu et al. 2007, Wagner et al. 2010). However, previous studies have also suggested that turbid-water corals are more vulnerable to local and global stresses (Fabricius et al. 2007, 2008).

The highest incidence of bleaching colonies in this study was found in more turbid waters (about 3 m deep). The most turbid waters were around H-RS, where 80% of corals were fully bleached. Turbid waters can provide protection from light stress during high-temperature bleaching events (Goreau et al. 2000), but in view of our results they may not be a coral refugium against thermal stress and post-bleaching stresses (Fig. 4).

The synergic effects of other factors with temperature conditions are also illustrated by the onset of diseases during and after bleaching events. For instance, Porites colonies, which comprise about 85% of all coral cover at site H-E, were mostly infected by a White Mat Disease that is a result of sediment-microbial interactions (Kavousi et al. 2013). There may be a link between elevated SSTs and outbreak of the White Mat Disease (Fig. 4E, F), as this disease killed about 60% of Porites live tissue at site H-E during the 2012 temperature anomaly (Kavousi et al. 2013).

Dominant coral genera at a majority of our study sites were among those most affected in the 2012 coral bleaching event. The same results were reported by Dalton and Carroll (2011) at high-latitude eastern Australian reefs. This may be an artifact of the low diversity of these sites, and the fact that the more vulnerable coral colonies may have been previously killed in prior bleaching events, leaving behind the more tolerant colonies. In 1998 many Acropora-dominated reefs in the Indian Ocean and Pacific lost almost all their Acropora and wound up being dominated by Porites survivors (Goreau et al. 2000). A similar situation was observed at L-NE but some factors besides bleaching were involved (Mohammadizadeh et al. 2013). The 2012 bleaching may change the dominant coral genera at our study sites in the coming years, especially at sites that were severely affected. Although this bleaching event may not cause local extinction of coral genera, as occurred in the southern Persian Gulf in 1996 (Riegl 2002, Sheppard 2006) and probably at Qeshm Island in 2007 (Kavousi et al. 2011), long-term monitoring programmes are needed because post-bleaching events are sometimes more severely destructive (e.g. Bastidas et al. 2012, Fig. 4).