Long-spined Sea Urchin Research Articles

First Record and Massive Spread of Tropical Long-Spined Sea Urchin Diadema antillarum in the Mediterranean Sea (Syrian Coast)

The biological structure of the Syrian marine environment still shows a rapid and steady increase in the number of warm water species, many of which have become dominant and invasive. In the latest field data during 2020-2021, the presence of the black sea urchin Diadema antillarum (Philippi, 1845) was recorded for the first time in several locations in Latakia and Ras al-Bassit coast, and its massive spread at depths of 5-8 m, accompanied by invasive species of macroalgae, sponges, crustaceans and mollusks.. It is noteworthy that this species is one of the most widespread and important species of sea urchins in some tropical areas, and this is the first record in the Mediterranean Sea and the Syrian coast It is important as it prey on macroalgae and has an effective role in the health of some of the most important areas of biodiversity in the world.

The role of algal chemical defenses in the feeding preferences of the long-spined sea urchin Diadema antillarum

The role of algal chemical defenses in the feeding preferences of the long-spined sea urchin Diadema antillarum

A novel system for intensive Diadema antillarum propagation as a step towards population enhancement

The long-spined sea urchin Diadema antillarum was once an abundant reef grazing herbivore throughout the Caribbean. During the early 1980s, D. antillarum populations were reduced by > 93% due to an undescribed disease. This event resulted in a lack of functional reef herbivory and contributed to ongoing ecological shifts from hard coral towards macroalgae dominated reefs. Limited natural recovery has increased interest in a range of strategies for augmenting herbivory. An area of focus has been developing scalable ex situ methods for rearing D. antillarum from gametes. The ultimate use of such a tool would be exploring hatchery origin restocking strategies. Intensive ex situ aquaculture is a potentially viable, yet difficult, method for producing D. antillarum at scales necessary to facilitate restocking. Here we describe a purpose-built, novel recirculating aquaculture system and the broodstock management and larval culture process that has produced multiple D. antillarum cohorts, and which has the potential for practical application in a dedicated hatchery setting. Adult animals held in captivity can be induced to spawn year-round, with some evidence for annual and lunar periodicity. Fecundity and fertilization rates are both consistently very high, yet challenges persist in both late stage larval development and early post-settlement survival. Initial success was realized with production of 100 juvenile D. antillarum from ~ 1200 competent larvae. While the system we describe requires a significant level of investment and technical expertise, this work advances D. antillarum culture efforts in potential future hatchery settings and improves the viability of scalable ex situ production for population enhancement.

The ecological importance of habitat complexity to the Caribbean coral reef herbivore Diadema antillarum: three lines of evidence

When Caribbean long-spined sea urchins, Diadema antillarum, are stable at high population densities, their grazing facilitates scleractinian coral dominance. Today, populations remain suppressed after a mass mortality in 1983–1984 caused a loss of their ecosystem functions, and led to widespread declines in ecosystem health. This study provides three lines of evidence to support the assertion that a lack of habitat complexity on Caribbean coral reefs contributes to their recovery failure. Firstly, we extracted fractal dimension (D) measurements, used as a proxy for habitat complexity, from 3D models to demonstrate that urchins preferentially inhabit areas of above average complexity at ecologically relevant spatial scales. Secondly, controlled behaviour experiments showed that an energetically expensive predator avoidance behaviour is reduced by 52% in complex habitats, potentially enabling increased resource allocation to reproduction. Thirdly, we deployed a network of simple and cost-effective artificial structures on a heavily degraded reef system in Honduras. Over a 24-month period the adult D. antillarum population around the artificial reefs increased by 320% from 0.05 ± 0.01 to 0.21 ± 0.04 m−2 and the juvenile D. antillarum population increased by 750% from 0.08 ± 0.02 to 0.68 ± 0.07 m−2. This study emphasises the important role of habitat structure in the ecology of D. antillarum and as a barrier to its widespread recovery.

Decision support for the Ecosystem-Based Management of a Range-Extending Species in a Global Marine Hotspot Presents Effective Strategies and Challenges

Climate-driven changes in ocean currents have facilitated the range extension of the long-spined sea urchin (Centrostephanus rodgersii) from Australia’s mainland to eastern Tasmania over recent decades. Since its arrival, the destructive grazing of the urchin has led to widespread formation of sea urchin ‘barrens’. The loss of habitat, biodiversity and productivity for important commercial reef species in conjunction with the development of an urchin fishery has led to conflicting objectives among some stakeholders that pose complex challenges for regional management. Stakeholders representatives and managers were engaged via a participatory workshop and subsequent one-on-one surveys to trial a structured decision making process to identify effective ecosystem-based management strategies. We directly and indirectly elicited each preferences for nine alternative management strategies by presenting them with the 10-year consequences of each strategy estimated from an ecosystem model of Tasmanian reef communities. These preferences were included in cost-effectiveness scores that were averaged (across stakeholders) to enable strategy ranking from most to least cost-effective. Rankings revealed strategies that included sea urchin removal or translocation of predatory lobsters were the most cost-effective. However, assessment of stakeholders’ individual cost-effectiveness scores showed some disparity among preferences in high ranking strategies. Additionally, inconsistencies in strategy preferences using alternative (direct or indirect) ranking scores reveal conflicting objectives as the most plausible explanation. Our study illustrates how structured decision making can effectively facilitate ecosystem-based management by engaging stakeholders step-by-step towards management strategy implementation and promoting collective learning.

Shelter use interactions of invasive lionfish with commercially and ecologically important native invertebrates on Caribbean coral reefs.

Indo-Pacific lionfish have become invasive throughout the western Atlantic. Their predatory effects have been the focus of much research and are suggested to cause declines in native fish abundance and diversity across the invaded range. However, little is known about their non-consumptive effects, or their effects on invertebrates. Lionfish use shelters on the reef, thus there is potential for competition with other shelter-dwelling organisms. We demonstrate similar habitat associations between invasive lionfish, native spiny lobsters (Panulirus argus) and native long-spined sea urchins (Diadema antillarum), indicating the potential for competition. We then used a laboratory experiment to compare activity and shelter use of each species when alone and when lionfish were paired with each native species. Spiny lobsters increased their activity but did not change their shelter use in the presence of a lionfish, whilst long-spined sea urchins changed neither their activity nor shelter use. However, lionfish reduced their shelter use in the presence of spiny lobsters and long-spined sea urchins. This study highlights the importance not only of testing for the non-consumptive effects of invasive species, but also exploring whether native species exert non-consumptive effects on the invasive.

Stomopneulactone D from long-spined sea urchin Stomopneustes variolaris: Anti-inflammatory macrocylic lactone attenuates cyclooxygenase-2 expression in lipopolysaccharide-activated macrophages

Cyclooxygenase-2 is one of the prominent enzymes to cause an increased production of prostaglandins during inflammation and immune responses. Cyclooxygenase-2 expression is up-regulated in inflammatory conditions owing to the induction by different inflammatory stimuli including cytokines, and therefore, the expression studies of cyclooxygenase-2 in lipopolysaccharide-induced macrophage cells (RAW 264.7 cell line) could be used for screening of the compounds with anti-inflammatory potential. The present study evaluated the anti-inflammatory properties of four homologous stomopneulactones A-D, classified under the class of macrocyclic lactones isolated from the solvent extract of the long-spined sea urchin Stomopneustes variolaris (familyStomopneustidae) in the lipopolysaccharide-induced macrophages. The structures of these isolated compounds were assigned using detailed spectroscopic techniques. Stomopneulactone D bearing 5-butyl-4-hydroxy-12-oxo-1-oxa-5,9-cyclododecadienyl moiety exhibited relatively greater anti-inflammatory potentials against cyclooxygenase-2 (IC50 ~ 2 mM) and 5-lipoxygenase (IC50 2.6 mM) than those displayed by other macrocyclic lactones. The studied compounds displayed higher selectivity index values (anti-cyclooxygenase-1IC50/anti-cyclooxygenase-2IC50 > 1), which designated the selective anti-inflammatory potentials of the macrocyclic lactones against inducible inflammatory mediators than those exhibited by the anti-inflammatory agent ibuprofen (0.43). The in silico molecular modelling analyses of the stomopneulactones with cyclooxygenase-2/5-lipoxygenase enzymes recorded lowest binding energy (−7.71 and −9.60 kcal mol−1, respectively) and docking score (−8.82 and −11.12 kcal mol−1, respectively) for stomopneulactone D along with its higher electronic parameter (topological polar surface area of 72.83), which further confirmed its greater anti-inflammatory potential than other compounds in the series. Stomopneulactone D also inhibited the generation of inducible nitric oxide synthase, intracellular reactive oxygen species, along with 5-lipoxygenase and cyclooxygenase-2 in the lipopolysaccharide-stimulated macrophage cells. Additionally, the studied macrocyclic lactone decreased the mRNA expression of cyclooxygenase-2 in the inflammatory cells in dose-dependent manner, which demonstrated the therapeutic potential of stomopneulactone D in down-regulating the inflammatory pathogenesis.

Can portunid crabs protect massive coral against the attack by long-spined sea urchins?

Sea urchin grazing can damage corals, but little is known how such damage can be remediated. We conducted three caging experiments in the field to determine the relationships among the portunid crab Thalamita prymna, the long-spined sea urchin Diadema setosum and the massive coral Platygyra carnosa. Experiment 1 showed that urchins caused coral tissue loss and reduced coral weight, and such effects were stronger at higher urchin densities. Experiment 2 showed that crabs could be effective urchin predators. Experiment 3 revealed that, when a rock with fouling organisms (an alternative food source) was available, some urchins managed to survive, but they did not cause appreciable coral damage. Together, our results indicate that, crab predation, an overlooked relationship in coral reefs, can be exploited to help control urchin corallivory and bioerosion. Prohibiting fish trapping in reef areas could reduce the by-catch of these crabs and protect reefs against urchin attack.

Diagnostic Methods for the Comprehensive Health Assessment of the Long-Spined Sea Urchin, Diadema antillarum

This 55-page document contains a wealth of information on the long-spined sea urchin, which is an important animal in coral reef ecosystems. The publication discusses diagnostic methods for Diadema antillarum and provides reporting forms for laboratory and diagnostic work. Written by Ruth Francis-Floyd, Jan Landsberg, Roy Yanong, Yasu Kiryu, Shirley Baker, Deborah Pouder, William Sharp, Gabriel Delgado, Nicole Stacy, Tom Waltzek, Heather Walden, Roxanna Smolowitz, and Greg Beck, and published by the UF/IFAS Veterinary Medicine—Large Animal Clinical Sciences Department, May 2020.

Lack of recovery of the long-spined sea urchin Diadema antillarum Philippi in Puerto Rico 33 years after the Caribbean-wide mass mortality.

Caribbean populations of the long-spined black sea urchin Diadema antillarum Philippi were decimated by a disease-induced mass mortality in the early 1980’s. The present study provides an updated status of the D. antillarum recovery and population characteristics in La Parguera Natural Reserve, Puerto Rico. The last detailed study to assess population recovery in 2001, indicated a slow, and modest recovery, albeit densities remained far below pre-mass mortality levels. Population densities were assessed along three depth intervals in six reef localities and one depth in three lagoonal sea-grass mounds using ten 20 m2 (10 × 2 m) belt-transects at each depth interval. Most of these were previously surveyed in 2001. All individuals encountered along the belt transects were sized in situ with calipers and rulers to characterize the size (age) structure of each population and get insight into the urchin’s population dynamics and differences across localities in the area. Habitat complexity (rugosity) was assessed in all depth intervals. No significant differences in population densities between reef zones (inner shelf and mid-shelf) were observed, but significantly higher densities were found on shallow habitats (<5 m depth; 2.56 ± 1.6 ind/m2) compared to intermediate (7–12 m; 0.47 ± 0.8 ind/m2) and deep (>12 m; 0.04 ± 0.08 ind/m2) reef habitats in almost all sites surveyed. Habitat complexity had the greatest effect on population densities at all levels (site, zone and depth) with more rugose environments containing significantly higher densities and wider size structures. Comparison between survey years revealed that D. antillarum populations have not increased since 2001, and urchins seem to prefer shallower, more complex and productive areas of the reef. Populations were dominated by medium to large (5–9 cm in test diameter) individuals and size-frequency distributions indicated that smaller juveniles were virtually absent compared to 2001, which could reflect a recruitment-limited population and explain in part, the lack of increase in population densities. The limited temporal scale of this study, high horizontal movement of individuals along the complex, shallower reef and inshore habitats could also explain the general decline in mean densities. Other extrinsic factors affecting reproductive output and/or succesful recruitment and survival of juveniles likely contribute to the high variablility in population densities observed over time.

Before and after a disease outbreak: Tracking a keystone species recovery from a mass mortality event

Mass mortality events involving marine taxa are increasing worldwide. The long-spined sea urchin Diadema africanum is considered a keystone herbivore species in the northeastern Atlantic due to its control over the abundance and distribution of algae. After a first registered mass mortality in 2009, another event off the coasts of Madeira archipelago affected this ecologically important species in summer 2018. This study documented the 2018 D. africanum mass mortality event, and the progress of its populations on the southern coast of Madeira island. A citizen science survey was designed targeting marine stakeholders to understand the extent and intensity of the event around the archipelago. Underwater surveys on population density prior, during and after the mass mortality, permitted an evaluation of the severity and magnitude of the event as well as urchin population recovery. A preliminary assessment of causative agents of the mortality was performed. The event was reported in the principal islands of the archipelago reducing the populations up to 90%. However, a fast recovery was registered during the following months, suggesting that the reproductive success was not compromised. Microbiological analyses in symptomatic and asymptomatic individuals, during and after the event, was not conclusive. Nevertheless, the bacteria Aeromonas salmonicida, or the gram-negative bacteria, or the interaction of different types of bacteria may be responsible for the disease outbreak. Further studies are needed to assess the role of pathogens in sea urchin mass mortalities and the compound effects that sea urchins have in local habitats and ecological functioning of coastal marine ecosystems.

RETRACTED ARTICLE: Structured Decision-Making Identifies Effective Strategies and Potential Barriers for Ecosystem-Based Management of a Range-Extending Species in a Global Marine Hotspot

The authors are retracting this article [1] because of confidentiality reasons. The article has been removed to protect the privacy of an individual. All authors agree to this retraction.

Mortality associated with ingestion of sea urchins in loggerhead sea turtles (Caretta caretta): A case series.

AimsThe aims of this study were: a) to describe the pathological and laboratory findings in a case series of stranding and mortality associated with ingestion of large amounts of sea urchins in loggerhead turtles (Caretta caretta), and b) to alert veterinarians and biologists involved in sea turtle conservation of this cause of stranding and/or death.MethodsThe six loggerheads studied were stranded on the coasts of Gran Canaria, Canary Islands, Spain, between 2008 and 2015. Post mortem studies included pathological, microbiological, and sea urchin species identification procedures.ResultsAll turtles showed severe intestinal impaction caused by large amounts of sea urchins, mainly affecting the colon and the caudal half of the small intestine. Histologically, severe focal fibrinonecrotic enteritis was diagnosed in two turtles. In the remaining turtles, lesions ranged from mild desquamation of the intestinal epithelium to severe congestion of the blood vessels of lamina propria, submucosa, muscular and serosa, and edema. Vibrio sp. was isolated from the spleen and intestinal mucosa of a loggerhead in which focal fibrinonecrotic enteritis had been diagnosed. In five turtles, all the remains were fragments from long-spined sea urchins (Diadema africanum); the last turtle contained a mixture of long-spined sea urchin (90%) and purple sea urchin (Sphaerechinus granularis) (10%) remains.ConclusionsAlthough the prevalence of this cause of stranding was low (< 1.6%) compared to other mortality causes, continued overfishing and anthropogenic climate change could increase its incidence. Intestinal impaction with large amounts of sea urchins should be included in the differential diagnosis of gastrointestinal diseases in sea turtles, and the possible toxic effect of some sea urchin species on sea turtles should also be investigated.

Establishing a Diagnostic Technique for Coelomocentesis in the Long-Spined Sea Urchin Diadema antillarum.

Coelomic fluid aspiration has been utilized in echinoderms in research and clinical settings. Detailed procedural descriptions for coelomic fluid sampling in sea urchins (class Echinoidea) are lacking, and samples are prone to contamination. The objectives of this study were to (1) standardize a technique for coelomic fluid collection in long-spined sea urchin Diadema antillarum that optimizes the diagnostic quality of the sample utilizing diagnostic imaging, (2) identify coelomic fluid bacterial isolates (using Biolog GEN III MicroLog and 16s rDNA sequencing), and (3) compare positive cultures to animal weight, holding time prior to sampling, water temperature, and gross fluid appearance. Seventy Diadema antillarum from the Florida Keys collected in two groups (March and September 2015) were utilized. Positive cultures for bacterial contamination were identified in 5% and 44%, respectively, of animals in the sampling groups. Vibrio spp. was the predominant genus identified. Positive cultures were more frequent in the group with smaller-sized animals, increased holding times, and elevated water temperatures. Deviation from clear-pink gross coelomic fluid appearance did not reliably predict bacterial contamination. A standardized technique for coelomocentesis was defined. The use of the proposed coelomocentesis methodology may facilitate improved health evaluations of sea urchins and may be applicable to research, conservation efforts, and disease investigations.

Needle in a haystack-genetic evidence confirms the expansion of the alien echinoid Diadema setosum (Echinoidea: Diadematidae) to the Mediterranean coast of Israel.

Diadema setosum (Leske, 1778), a widespread tropical echinoid and key herbivore in shallow water environments is currently expanding in the Mediterranean Sea. It was introduced by unknown means and first observed in southern Turkey in 2006. From there it spread eastwards to Lebanon (2009) and westwards to the Aegean Sea (2014). Since late 2016 sporadic sightings of black, long-spined sea urchins were reported by recreational divers from rock reefs off the Israeli coast. Numerous attempts to verify these records failed; neither did the BioBlitz Israel task force encounter any D. setosum in their campaigns. Finally, a single adult specimen was observed on June 17, 2017 in a deep rock crevice at 3.5 m depth at Gordon Beach, Tel Aviv. Although the specimen could not be recovered, spine fragments sampled were enough to genetically verify the visual underwater identification based on morphology. Sequences of COI, ATP8-Lysine, and the mitochondrial Control Region of the Israel specimen are identical to those of the specimen collected in 2006 in Turkey, unambiguously assigning the specimen to D. setosum clade b. This lends support to the hypothesis of a single introduction event and fits well with the habitat suitability and distribution model for D. setosum published recently. The more rapid and larger range extension along a south-eastern, counter-current trajectory may reflect a strong habitat preference for D. setosum in this area of the Levantine Basin as predicted by the model.

The sea urchin Diadema africanum uses low resolution vision to find shelter and deter enemies.

Many sea urchins can detect light on their body surface and some species are reported to possess image-resolving vision. Here, we measure the spatial resolution of vision in the long-spined sea urchin Diadema africanum, using two different visual responses: a taxis towards dark objects and an alarm response of spine-pointing towards looming stimuli. For the taxis response we used visual stimuli, which were isoluminant to the background, to discriminate spatial vision from phototaxis. Individual animals were placed in the centre of a cylindrical arena under bright down-welling light, with stimuli of varying angular width placed on the arena wall at alternating directions from the centre. We tracked the direction of movement of individual animals in relation to the stimuli to determine whether the animals oriented towards the stimulus. We found that D. africanum responds by taxis towards isoluminant stimuli with a spatial resolution in the range of 29-69 deg. This corresponds to a theoretical acceptance angle of 38-89 deg, assuming a contrast threshold of 10%. The visual acuity of the alarm response of D. africanum was tested by exposing animals to different sized dark looming and appearing stimuli on a monitor. We found that D. africanum displays a spine-pointing response to appearing black circles of 13-25 deg angular width, corresponding to an acceptance angle of 60-116 deg, assuming the same contrast threshold as above.

Genetic structure of natural and broodstock populations of the long-spined sea urchin, Diadema antillarum, throughout the Florida Keys

Caribbean populations of the long-spined sea urchin, Diadema antillarum (Philippi, 1845), have undergone two mass mortality events since the 1980s that have caused 93%–100% of individuals on any given reef to perish. Subsequently, coral recruitment and survival declined, in part due to algal overgrowth and an increase in secondary metabolites associated with macoalgae. For long-term macroalgal biomass removal, supplementation of D. antillarum via translocation, captive-rearing and release, or both, must be considered. This project aimed to (1) compare genetic diversity of Diadema antillarum (Philippi, 1845) from six reef locations in south Florida ranging from Biscayne National Park to the Dry Tortugas, and (2) determine whether two broodstock populations of mixed ancestry contain variation indicative of natural Florida populations. We found little genetic differentiation among natural locations and between natural and broodstock populations (highest pairwise F ST was 0.0066). Moreover, genetic diversity was similar among all natural and broodstock populations (allelic richness and heterozygosity ranged from 22.6–24.4 and 0.937–0.956, respectively). Additionally, a Structure analysis suggested that all samples compose a single genetic cluster. These data suggest that natural populations of D. antillarum are genetically similar throughout the Florida Keys, from Dry Tortugas National Park through Biscayne National Park, and that captive-bred individuals could be used for reintroduction as part of a plan to re-establish healthy urchin populations throughout the Florida Keys.

Reef fish associations with sea urchins in an Atlantic oceanic island

Many reef fish are known to be associated with particular microhabitats that provide food and refuge, such as branching corals, gorgonians, macroalgal beds and sea urchins. We investigate the association of reef fishes with the long-spined sea urchin Diadema antillarum in shallow reefs of Trindade Island, southeastern Brazil. A total of 1283 fish individuals from seven families and nine species were associated with 495 sea urchins. Sea urchins provide important shelter especially for juveniles of the Noronha wrasse, Thalassoma noronhanum. Larger fishes were found at higher densities associated to sea urchins with larger spines. At reefs lacking structurally complex organisms, such as branching corals, sea urchins can be an important refuge for juveniles or small-bodied reef fish species, influencing their distribution and acting as ecosystem engineers.

Interacting effects of temperature, habitat and phenotype on predator avoidance behaviour in Diadema antillarum: implications for restorative conservation

Caribbean long-spined sea urchin Diadema antillarum populations crashed following a mass mortality event in 1983-1984 with cascading effects on reef health. Population restoration efforts may be hampered by unknown effects of short- and long-term elevated sea surface temperature (SST). We investigated how a key behavioural trait, predator avoidance behaviour (PAB; percentage of long defensive spines that moved in response to shadow stimuli), was affected by elevated SST in 180 individuals from 2 contrasting Honduran reefs: Utila (flattened reef structure, dearth of predation refugia) and Banco Capiro (complex reef structure, abundant refugia). Initiation of PAB is mediated by melanin, which breaks down at elevated water temperatures; thus, as SST rises, D. antillarum may become vulnerable to predation. We compared local current SST (CSST; 29.7°C) with 2 IPCC predicted long-term climate change scenarios under laboratory conditions. PAB decreased by 13.98-15.37% at CSST +1.4°C and 31.67-42.44% at CSST +3.1°C. Trial temperatures were similar to maxima recorded in the Caribbean during the 2016 El Nino, so our results also represent likely responses to worst-case short-term acute temperature anomalies. Juveniles maintained higher PAB than adults, indicating increased reliance on anti-predation behaviours. White-spined phenotypes from Utila’s flattened reef maintained higher PAB than black-spined counterparts, likely due to increased conspicuousness to visual predators. Habitat complexity may mitigate temperature-driven losses in natural behavioural defences. D. antillarum may be resilient to near-term (<2039) SST increases and periodic temperature stresses but may struggle under long-term, worst-case scenario conditions. Restoration of D. antillarum populations must be coupled to augmented reef complexity to improve future resilience.

Reproduction of the long-spined sea urchin Diadema setosum in the Gulf of Aqaba - implications for the use of gonad-indexes

As global warming and climate-change proceeds ever more rapidly, organisms depending on seasonal cues to synchronize reproduction face an unclear future. Reproduction in Diadema setosum in the Gulf of Aqaba (Red Sea) is seasonal, with mature individuals occurring from July to October. Gonad indexes (GI), in contrast, indicate that spawning occurs from August through December and suggests two main spawning events. Histological analysis, however, indicate that the second peak of GI values cannot be related to spawning, but rather correspond to recovering individuals. In Diadema, examination of GI values alone may thus lead to erroneous conclusions. GI was moderately-strong positively correlated with sea-surface temperatures, but not with chlorophyll-a concentrations or photoperiod. Spawning coincides with the onset of the annual chlorophyll-a increase, however, which might be advantageous for nutrition of the developing larvae. First significant GI increase coincides with the shortening of day-length, which may act as a cue for D. setosum gametogenesis. Gametogenesis is highly synchronised between sexes, although the mature phase of females exceeds that of males. The non-complete overlap may represent sampling bias or represent an adaptive strategy for enhancing fertilisation success. Skewed sex ratios (♀:♂ 1:0.59, n = 360) in the Gulf of Aqaba may be related to pollution.