John A. Burt

The Growing Need for Sustainable Ecological Management of Marine Communities of the Persian Gulf

The Persian Gulf is a semi-enclosed marine system surrounded by eight countries, many of which are experiencing substantial development. It is also a major center for the oil industry. The increasing array of anthropogenic disturbances may have substantial negative impacts on marine ecosystems, but this has received little attention until recently. We review the available literature on the Gulf’s marine environment and detail our recent experience in the United Arab Emirates (U.A.E.) to evaluate the role of anthropogenic disturbance in this marine ecosystem. Extensive coastal development may now be the single most important anthropogenic stressor. We offer suggestions for how to build awareness of environmental risks of current practices, enhance regional capacity for coastal management, and build cooperative management of this important, shared marine system. An excellent opportunity exists for one or more of the bordering countries to initiate a bold and effective, long-term, international collaboration in environmental management for the Gulf.

Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf

Coral reefs are in rapid decline on a global scale due to human activities and a changing climate. Shallow water reefs depend on the obligatory symbiosis between the habitat forming coral host and its algal symbiont from the genus Symbiodinium (zooxanthellae). This association is highly sensitive to thermal perturbations and temperatures as little as 1°C above the average summer maxima can cause the breakdown of this symbiosis, termed coral bleaching. Predicting the capacity of corals to survive the expected increase in seawater temperatures depends strongly on our understanding of the thermal tolerance of the symbiotic algae. Here we use molecular phylogenetic analysis of four genetic markers to describe Symbiodinium thermophilum, sp. nov. from the Persian/Arabian Gulf, a thermally tolerant coral symbiont. Phylogenetic inference using the non-coding region of the chloroplast psbA gene resolves S. thermophilum as a monophyletic lineage with large genetic distances from any other ITS2 C3 type found outside the Gulf. Through the characterisation of Symbiodinium associations of 6 species (5 genera) of Gulf corals, we demonstrate that S. thermophilum is the prevalent symbiont all year round in the worlds hottest sea, the southern Persian/Arabian Gulf.

Tropical harmful algal blooms: an emerging threat to coral reef communities?

Tropical harmful algal blooms (HABs) are increasing in frequency and intensity and are substantially affecting marine communities. In October/November 2008 a large-scale HAB event (> 500 km(2), dinoflagellate Cochlodinium polykrikoides) in the Gulf of Oman caused the complete loss of the branching corals, Pocillopora and Acropora spp., and substantial reductions in the abundance, richness and trophic diversity of the associated coral reef fish communities. Although the causative agents of this C. polykrikoides bloom are unknown, increased coastal enrichment, natural oceanographic mechanisms, and the recent expansion of this species within ballast water discharge are expected to be the main agents. With rapid changes in oceanic climate, enhanced coastal eutrophication and increased global distribution of HAB species within ballast water, large-scale HAB events are predicted to increase dramatically in both intensity and distribution and can be expected to have increasingly negative effects on coral reef communities globally.

Locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals as detected by green fluorescent protein (GFP)-like pigments

Homologs of the green fluorescent protein (GFP) are a prevalent group of host pigments responsible for the green, red and purple-blue colours of many reef-building corals. They have been suggested to contribute to the striking coloration changes of different corals species in response to wounding and infestation with epibionts/parasites. In order to elucidate the physiological processes underlying the potentially disease-related colour changes, we have analysed spatial and temporal expression patterns of GFP-like proteins and other biomarkers in corals from the Red Sea, the Arabian/Persian Gulf and Fiji both in their natural habitat and under specific laboratory conditions. The expression of distinct GFP-like proteins and the growth marker proliferating cell nuclear antigen was upregulated in growing branch tips and margins of healthy coral colonies as well as in disturbed colony parts. Furthermore, phenoloxidase activity increased in these proliferating tissues. It is thus demonstrated that locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals and, moreover, these processes can be detected utilizing the excellent biomarker properties of GFP-like proteins. Finally, the results of this work suggest an additional vulnerability of corals in predicted future scenarios of increased ocean acidification, warming and eutrophication that are anticipated to reduce coral growth capacity.

Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Significance Reef corals in the Persian/Arabian Gulf (PAG) withstand exceptionally high salinity and regular summer temperatures of ∼35 °C that kill conspecifics elsewhere. These thermotolerant communities established themselves within only ∼6,000 y under the pressure of rapid climate change and can therefore inform how other coral reefs may respond to global warming. One key to the thermotolerance of PAG corals is their symbiosis with Symbiodinium thermophilum. Phylogeographic evidence indicates that this symbiont represents a stress-tolerant subpopulation of an ancestral taxonomic group with surprising genetic diversity that exists at barely detectable levels outside the PAG. Our results highlight the critical importance of present-day biodiversity for future adaptation to climate change for coral reefs and ecosystems in general. Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world’s warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.

Long-term impacts of coral bleaching events on the world’s warmest reefs

The southern Arabian Gulf houses some of the most thermally tolerant corals on earth, but severe bleaching in the late 1990s caused widespread mortality. More than a decade later, corals still dominated benthos (mean: 40 ± 3% cover on 10 sites spanning > 350 km; range: 11.0-65.6%), but coral communities varied spatially. Sites to the west generally had low species richness and coral cover (mean: 3.2 species per transect, 31% cover), with Porites dominated communities (88% of coral) that are distinct from more diverse and higher cover eastern sites (mean: 10.3 species per transect, 62% cover). These patterns reflect both the more extreme bleaching to the west in the late 1990s as well as the higher faviid dominated recruitment to the east in subsequent years. There has been limited recovery of the formerly dominant Acropora, which now represents <1% of the benthos, likely as a result of recruitment failure. Results indicate that severe bleaching can have substantial long-term impacts on coral communities, even in areas with corals tolerant to environmental extremes.

Fish communities on the world's warmest reefs: what can they tell us about the effects of climate change in the future?

To examine the role of climatic extremes in structuring reef fish communities in the Arabian region, reef fish communities were visually surveyed at four sites within the southern Persian Gulf (also known as the Arabian Gulf and The Gulf), where sea-surface temperatures are extreme (range: 12-35° C annually), and these were compared with communities at four latitudinally similar sites in the biogeographically connected Gulf of Oman, where conditions are more moderate (range: 22-31° C annually). Although sites were relatively similar in the cover and composition of coral communities, substantial differences in the structure and composition of associated fish assemblages were apparent. Fish assemblages in the southern Persian Gulf held significantly lower estimates of abundance, richness and biomass, with significantly higher abundances of smaller sized individuals than Gulf of Oman assemblages. Functionally, southern Persian Gulf sites held significantly lower abundances of nearly all the common fish trophic guilds found on Gulf of Oman sites, although higher abundances of herbivorous grazers were apparent. These results suggest the potential for substantial changes in the structure of reef-associated fish communities, independent of changes in habitat within an environment of increasing fluctuations in oceanic climate.

Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/ Arabian Gulf

The symbiotic association of corals and unicellular algae of the genus Symbiodinium in the southern Persian/Arabian Gulf (PAG) display an exceptional heat tolerance, enduring summer peak temperatures of up to 36 °C. As yet, it is not clear whether this resilience is related to the presence of specific symbiont types that are exclusively found in this region. Therefore, we used molecular markers to identify the symbiotic algae of three Porites species along >1000 km of coastline in the PAG and the Gulf of Oman and found that a recently described species, Symbiodinium thermophilum, is integral to coral survival in the southern PAG, the world’s hottest sea. Despite the geographic isolation of the PAG, we discovered that representatives of the S. thermophilum group can also be found in the adjacent Gulf of Oman providing a potential source of thermotolerant symbionts that might facilitate the adaptation of Indian Ocean populations to the higher water temperatures expected for the future. However, corals from the PAG associated with S. thermophilum show strong local adaptation not only to high temperatures but also to the exceptionally high salinity of their habitat. We show that their superior heat tolerance can be lost when these corals are exposed to reduced salinity levels common for oceanic environments elsewhere. Consequently, the salinity prevailing in most reefs outside the PAG might represent a distribution barrier for extreme temperature-tolerant coral/Symbiodinium associations from the PAG.

Multiple environmental factors influence the spatial distribution and structure of reef communities in the northeastern Arabian Peninsula

Multivariate analysis revealed distinct sub-regional coral communities among the southern Persian Gulf, Strait of Hormuz, and Gulf of Oman. Differences in community structure among locations were associated with considerable spatial heterogeneity in oceanic conditions, and strong directional environmental gradients. Despite clear community differences, considerable changes to coral community structure have occurred throughout the northeastern Arabian Peninsula as compared with previous studies. The most dramatic of these are the apparent changes from Acropora dominated to poritid and faviid dominated communities, particularly in the southern Persian Gulf and Strait of Hormuz. Although temperature and salinity have previously been cited as the major environmental factors structuring coral communities around the region, additional environmental parameters, including chlorophyll-a, surface currents and winds are shown to be important in structuring reef communities throughout the northeastern Arabian Peninsula.

Urban breakwaters as reef fish habitat in the Persian Gulf

Breakwaters and related structures dominate near-shore environments in many Persian Gulf countries, but little is known of their ecology. To examine the influence of wave exposure on fish communities we surveyed exposed and sheltered breakwaters seasonally over 2 years and compared these with natural reef assemblages. Species richness and adult, juvenile, and total abundance were generally comparable among the three habitat types each season. However, differences in multivariate community structure indicated that each habitat contained a distinct assemblage, with strongest difference between sheltered breakwaters and the exposed natural reef. All communities were characterized by marked seasonality; abundance and richness were generally higher in the warmer seasons (summer, fall) than during cooler periods (winter, spring), and there were related seasonal changes in community structure, particularly on the natural reef. Results indicate that breakwaters are important fish habitats, but that breakwater communities vary with wave exposure and are distinct from natural reefs.