Resilience of a Red Sea Fringing Coral Reef Under Extreme Environmental Conditions: A Four Year Study

Part of the Young Naturalist Awards Curriculum Collection.

by Zaki, Grade 12, Florida - 2008 YNA Winner
Figure 1: Red Sea fringing reef is relatively shallow and lies just a short distance from the shore. This photo, taken from offshore of the reef in approximately 4 meters of water, depicts the mountainous landscape and new construction onshore. Future inhabitants are just one of the many recent influences that poses a direct threat to the health of the reef.

A four-year study, which began in the summer of 2004, collected the first comprehensive time series of measurements from a 0.5 km x 0.1 km fringing reef in the Gulf of Suez (29° 32' N and 32° 24' E), in the Red Sea. This reef occurs near the northernmost extreme latitude for subtropical coral reefs. Here, corals are exposed to daily water temperature changes of 2°C to 4°C, and seasonal variations that exceed 15°C to 20°C. Salinities are among the highest in the world and are considered extreme, ranging from 44 to 45 psu. This reef has been subjected to many new stresses over the past four years, including a newly built major shipping port, rapid coastal urbanization, bleaching, and an oil spill in 2005.
Annual reef surveys include random photo quadrats plus fish and coral video transects, supported by a suite of environmental measurements. Results indicate that between 2005 and 2007, there was a statistically significant decline in reef health indicators, including a 50% increase in dead and diseased coral, a 58% increase in sea urchins, and decreases in biodiversity and sediment constituent indices, fish abundance, and water quality. Of the approximately 40 known coral species hardy enough to survive in this region, six species make up 94% of the reef's coral cover. Given the extreme natural environmental conditions in which this fringing reef has thrived, the resilience of this community appears to be very high. Unfortunately, this reef and others in the area are now threatened by local anthropogenic impacts. This study establishes a reference point for comparison with similar reefs and will be key to any future conservation and restoration efforts.

Figure 2: Sketch depicting Zaki's reef and the location of the five 10m transects that were monitored over four years using digital video survey to assess coral and a separate survey to estimate fish population diversity and abundance.
Figure 3: Raft containing typical supplies used while sampling Zaki's Reef. The raft was towed behind two snorkeling researchers. It held drinking water, camera gear, waterproof log books, nylon rope, water sampling bottles, electronic handheld sensors to monitor pH, temperature, salinity, and dissolved oxygen, and a few other essentials. A global positioning system (GPS) was used to return to previously sampled locations and where sensors had been left.

I sat gazing out at the Red Sea's distinct and beautiful waters, majestic mountains jutting upwards from the desert landscape behind me (Figure 1). Little did I know that that day would bring a higher sense of meaning and accomplishment to the next four years of my life. It was that day that I uncovered a hidden treasure by discovering the existence of a pristine coral reef just a block away from the beach I been coming to every summer. Since that moment, I've satisfied my passion for science and my love of the ocean by collecting the first known extensive time-series monitoring of a fringing coral reef in the Red Sea's Gulf of Suez.
Reefs are considered an early warning system for the world's oceans, and it is estimated that 70% of the world's coral reefs will be destroyed within the next few decades (Onaga 2001). This reef (dubbed "Zaki's Reef," after my grandfather) is located at the northernmost latitude for a tropical or semi-tropical reef (Figure 2). It lies at the edge of an extremely arid desert where rainfall is nominal, evaporation rates are high, and freshwater inputs are low due to persistent trade winds and extreme temperatures. Only a few species of coral can successfully live in these extreme conditions. A 2000 study (Moustafa 2000) estimates that 335 species of corals are found in the Red Sea, yet only approximately 35 species have been identified in the Gulf of Suez. The water in the Gulf of Suez is very shallow (averaging 50 to 80 meters in depth), allowing for excessive salinity (43 to 45 ppt) and large daily and seasonal temperature fluctuations. The high temperature and salinity reduce oxygen solubility, making it unsuitable for many species of reef-dwelling organisms. The corals and organisms that do reside and thrive here must be able to tolerate these extreme environmental conditions.

Figure 4: Sketch of Zaki's 0.5 km x 0.1 km fringing reef in the Gulf of Suez located (29¡ 32' N and 32¡ 24' E). Reef showing approximate location of the five 10-m coral transects that were monitored annually to evaluate change, and the delineation of the reef into three arbitrary sub-regions for purposes of determining spatial variability.

Zaki's Reef is a small fringing reef (a reef of less than 1 km by 0.5 km) that averages only one to two meters in depth, and can be accessed by a short swim from the beach (Figure 1). Due to its remote desert location the reef had remained pristine, but pollution from shipping and oil spillage pose a significant threat (Spalding et al. 2001). The gaps in our scientific knowledge of coral reefs in extreme locations are large, and the exact thermal limits for reefs remain unknown (Grimsditch and Salm 2006). I hypothesized that as man encroaches, this coral reef would be more resilient to external stresses compared to tropical reefs, given the extreme environmental conditions this reef normally experiences.

Figure 5: Zaki sampling on Zaki's Reef (named after my grandfather). Sampling occurred over several weeks during the summer for four consecutive years. The reef lies swimming distance from shore (approximately 100 m). Long twelve-hour days were spent in the field taking photographs, gathering measurements, and collecting data with the support of my father, mother, sister, and brother.

Purpose Of The Research 
The main goals of my research were to document the effects of both natural and man-made influences on a unique, pristine, isolated fringing coral reef located at an extreme northernly latitude over a four-year period. My specific objectives were to: 1) determine the reef's health and identify the dominant coral species; 2) assess the reef's resilience to recent natural and man-made influences; 3) identify the impacts of local natural and man-made influences, 4) conduct fish surveys; 5) evaluate reef sediment distributions and biogenic components; 6) determine water-quality characteristics, and 7) share the results, since data on this region is either lacking or nonexistent.
The first-year data provided the baseline conditions necessary to characterize the reef and observe interannual changes. Since sampling in 2004, a major shipping port was constructed approximately five kilometers north of this reef, causing an increase in local shipping traffic, seaside housing, oil offloading, and local population. Through a quantitative comparison, I was able to statistically compare baseline conditions with annual measurements taken of the reef community using underwater digital photography and movies. Trends in coral coverage, species abundance, and diversity were calculated. Cause-and-effect relationships are suggested based on the ecosystem's response to changing environmental conditions.

The methodologies used to sample this reef coincide with universally accepted protocols (Hill and Wilkinson 2004). Field gear included snorkel equipment, digital still and video underwater digital cameras, water measurement sensors, a GPS sensor, and a raft (Figure 3). Between 2004 and 2007, I spent several weeks each summer at the reef collecting data, using my brother, sister, and parents as my field support.

Figure 4: Quadrat photo analysis method. A 0.5 m2 PVC square dropped from the surface encompasses the randomly selected area to be photographed. Whatever corals types lay within each quadrat are identified and its coverage area within the quadrat calculated using CPCe software (Kohler, 2006) with each digital image.

Video Transect Survey 

To assess reef health and community structure, underwater video photography (Page et al. 2001) documented the changes along five 10-meter-long transects located across the reef (Figure 4). Video transect surveys were repeated each year. Fish surveys were also conducted by logging and digitally recording species type and abundance occurring over a five-minute period at three of the 10-meter transects (Figure 5).

Photo Quadrat Survey 
An extensive random photo quadrat survey captured bottom substrate photos from across the reef to establish percent coral coverage, diversity, and species dominance (Figure 6). The percentage of bottom coverage and coral type statistics were derived from the analysis of approximately 120 random quadrat photos each year (Figure 7).

Water-Quality Sampling and Accessory Data 
Water temperature, salinity, dissolved oxygen, and pH values were regularly measured across the reef (Figure 8). Additional water samples were collected to perform water-quality analysis and to examine reef water for coliform bacteria. Coral mucus, commonly excreted by corals as a protection and known to trap particulate matter, was also tested for coliform bacteria (Kellogg 2004). Underwater temperature sensors measured water temperature at five locations across the reef. Since the summer of 2006, a 15-minute time series of temperatures is being measured at five locations across the reef using Onset underwater temperature sensors to collect temperature and determine spatial variability. Air temperature and basic meteorological data are also being collected. Local tides, waves, wind data, ship traffic, and oil offloading were regularly logged during fieldwork.

Figure 7: Analysis of quadrat data using CPCe total area calculation or random point generation method to calculate total coral coverage on quadrat photos which represent a half square meter of reef. One method looks at total coverage area and the second uses a specified number of randomly generated points on each frame from which percent coverage of each bottom type can be inferred.

Sediment Sampling and Analysis 

Surface sediment samples were collected—by taking hand grabs from the beach to just offshore of the reef—to determine the sediments' biogenic composition and grain size distributions. The biogenic composition of approximately 100 sand-size grains from each sample was identified under a microscope (Figure 9). The number of coral grains, forams, coralline red algae, gastropods, calcareous algae, echinoid spines, worm tubes, and other skeletal fragments was tabulated, and then the SEDCON Index (SI) (Daniels and Hallock 2006) was calculated as a measure of reef health. Sediment grain-size analysis was performed by manually sieving dried sediment into size classes and calculating class percentages.

Computer Data Analysis 

Figure 8: Field sampling on the reef includes measuring water temperature, salinity, dissolved Oxygen and pH. Underwater cameras recorded movies and digital photos of the reef. A handheld GPS was used to return to stations where sensors had been placed.

The sharpest digital images were extracted from transect and quadrat survey data to identify coral species and calculate the percentage of benthic coverage. To identify the observed fish and coral types, a Red Sea comprehensive guidebook (Lieske and Myers 2004) was used. Coral Point Count (CPCe) software (Kohler 2006) was employed to evaluate coverage along each 10-meter transect by extracting approximately 0.5-by-2-meter-wide swaths on 25 frames. Coral coverage was determined by identifying the bottom coverage at 60 computer-generated random points, which were projected onto each image. Sixty points were found to be statistically significant during earlier analysis trials. CPCe software also determined the total area (in cm 2 ) covered by each coral species from each 0.5 m quadrat photo. Analysis included identifying and counting sea urchins, fish, and other organisms in each photo.

In 2004, the study site was extraordinarily healthy at the outset of this research, and the reef would be characterized as pristine by experts. Unfortunately, in 2005 a major oil spill occurred just three kilometers offshore of the reef during summer sampling (Figure 10). Although environmentally tragic, this event provided an opportunity to document the reef before and after an oil spill, a very rare and unlikely occurrence in reef studies.

Figure 9: Example of biogenic sediment analysis under a photo-microscope. Identified fragments are used to evaluate reef health using the SEDCON Index (Daniels and Hallock, 2004). Statistically significant changes occurred in the biogenic composition of the sediment since 2004. Indicators suggest a decline in overall reef health.

Coral Types and Coral Coverage 
Each year, the total percentage of bottom coverage and general reef health were compared to the 2004 baseline survey data (Figure 11). Of the 30 or so coral species identified in the Gulf of Suez, six of these make up 94% of Zaki's Reef, with approximately 80% being hard corals and 20% soft. Dominant hard coral species include staghorn, Neptheidae, finger, and anemone (Porites) corals. On average, in 2004, 25% of the coral (mainly staghorn) was dead, most likely from past bleaching events. The percentage of dead coral has varied over time, and the dominant bottom-coverage types have shifted depending on the location on the reef. In general, spatial patterns of coral coverage and health indicate that the offshore regions of the reef where the water is deepest are healthiest.
Averaged over four years, random quadrat survey results indicate that staghorn is the dominant reef species (22.23% ± 5.08 SE), followed by finger coral (16.13% ± 1.14 SE), Nephtheidae (13.54% ± 1.92 SE), and anemone coral (11.87% ± 2.31 SE). Dead coral bottom coverage over the four-year study had a mean value of 22.82% (± 4.3 SE). The remaining major species, Faviidae and crystal corals, covered equal amounts, averaging 5.5% (± 2.78 SE) and 4.9% (± 2.13 SE), respectively.
Based on quadrat survey results, staghorn was the dominant species (25%) at the outset of this research and continued to grow/increase to more than 35% in 2005. However, there was a huge decline in both staghorn (down to 14% from 35%) and crystal coral (down to < 0.3% from 7%) between 2005 and 2006. yet there was no observed change in the percentage of dead coral that year, suggesting that the loss of staghorn was compensated for by the growth of other species.

Figure 10: Oil covered the beach directly behind Zaki's Reef, (A) one day after the oil spill in July of 2005. Two years later, evidence of this spill still prevails in the sediment on the beach (B), on reef organisms (C) and in the sediment (D). Human carelessness and oil tankers offloading their tanks in the vicinity are responsible for careless spills of this nature occurring.
Figure 11: Percent change in coral coverage over the four years based on the random 0.5 m squared quadrat survey of the reef conducted each year. Note the increase in dead corals by 2007.

Video Transects 
Table 1 summarizes the net percentage change in each coral type for all years sampled. At all five transects, Faviidae, anemone, finger, Neptheidae, and staghorn were the dominant species. When the 2007 coral coverage is compared to previous years, a net loss in coral was observed at Transects 2 and 4, while overall growth was observed at the other three transects. The Kruskal-Wallis statistical test for population equality (Conover 1999) validated the null hypothesis that there was not a significant difference (a = 0.05) in coral coverage at all transects. Therefore, despite noted differences in species coverage between years (Table 1), differences remain statistically insignificant (a = 0.05); as some species declined, others may have grown.

Coral Diversity 
The Simpson Weaver biodiversity index (Shannon 1948) is an indicator of the number of species and their evenness. Data from each transect and between transects indicated that biodiversity varied significantly between years in every instance (a = 0.05) (Figure 12).

Biogenic Indicators 
Bottom hand-grab sediment samples from across the reef indicate that grain-size distributions remained consistent over time, although their biogenic composition changed. After the oil spill, sediments showed a statistically significant increase in the SI index due to an increase in coral fragments and fewer foram fragments, suggesting increasing mortality and ecosystem decline.

Sea Urchins 
Long- and short-spine urchins were counted in quadrat photos, with short-spine urchins being the most abundant. Urchins feed on excess nutrients, thereby preventing algal smothering of corals. As nutrient levels rise, urchin populations typically increase and can eventually become detrimental to coral health. An algae biomass increase is often caused by the presence of wastewater and high nutrient levels. While the sea urchin population counts remained constant in 2004 and 2005, a notable 42% increase in short-spine urchins was observed between 2005 and 2006, and a statistically significant increase of 58% between 2006 and 2007 (Table 2).

Table 1: Percent change in coral coverage at each of the five permanent transects monitored since 2004 or 2005. Transects 1, 3, and 5 show a net increase in coral coverage, while Transects 2 and 4 indicate an overall decrease.

Fish Transects 
Annual fish surveys were performed by collecting video and observational logs of organisms from three of the permanent reef transect locations. Among the most abundant fish species documented were lizardfish, bluestreak cleaner wrasse, Indo-Pacific sergeant, yellowbar angelfish, and Red Sea anemone fish. Based on these annual surveys, there was a noticeable decline in fish community abundance and diversity after the 2005 oil spill.

2005 Oil Spill 
A 2005 oil spill occurred less than three kilometers away, dumping thousands of gallons of heavy crude oil onto Zaki's Reef. Immediate effects to the area included increased turbidity, a clumping of oil in sediment and on rock faces, and a gummy residue on urchin spines. More than two years later, the effects of the 2005 oil spill are still widespread on the reef and beach. Thick oil remains caked on rocks on the upper beach face and a few centimeters below the surface sediment on the lower beach and reef. Petroleum hydrocarbons present in the sediment and on coral tissue will prolong injury and may continue to for years to come.

Table 2: Changes in four-year urchin count on Zaki's fringing Red Sea coral reef show an overall 51% increase in the urchin population since 2004.


Air and water temperature time series records were collected, as previously mentioned. On average, daily air-temperature lows reached 21ºC while maximums were around 39ºC, a difference of 18ºC. Underwater sensors at each transect exhibited daily water temperature differences ranging from 0.3ºC to 4.4ºC. Annual water temperatures on the reef fluctuate widely, ranging from a low of 14 o C in February to a maximum of 34ºC in September. Shallower regions of the reef were warmer and displayed wider daily temperature ranges than those in deeper water, which experience stronger currents that allow for greater water exchange. In 2005, evidence of a global bleaching event, caused by water temperatures going more than 2°C above their average maximum, were documented by our U/W temperature sensors.

Coral Disease and Bleaching 
Annual digital photos across the reef led me to capture various coral diseases and document an increase in coral fish bites. Observations of coral disease increased greatly in 2006, the year after the oil spill (Figure 13). With the help of coral disease experts, I soon discovered that these photos documented the first occurrence of certain coral diseases in this region of the world, and that many of the coral diseases remain unknown, especially their causes. In 2007, nearly all water and mucus samples tested positive for enterococcus, a potential cause for the increase in diseases (Kellogg 2004). Since 2004, many reef regions have become overgrown by algae and algal mats, and with the zoanthids that typically colonize coral rubble, reducing the space for new coral colonies to settle.

Table 3: The known stresses affecting Zaki's Reef were ranked (1-10) based on their observed significance in 2007.

Water Quality 

Near-surface water samples from across the reef indicated the following average values: pH 8.13, salinity 44 ppt (average ocean salinity is 34 to 35 ppt), and dissolved oxygen (DO) was 0.271 ml/l. Annual water-quality analysis included total phosphorus (TP), soluble reactive phosphorus (SRP), total organic carbon (TOC), and dissolved inorganic nitrogen (DIN). SRP and DIN were compared to values reported in the literature (i.e., Lapointe et al. 1997). SRP concentrations were close to or lower than the literature-reported values, while DIN observations exceeded the literature's values by a factor of 10 or more.
Table 3 summarizes the known man-made and natural influences thought to be affecting this reef. The response of the reef community to recent stresses is mixed. In 2007, some positive signs were evident, as three of the five monitored transects indicated a net increase in coral growth since 2004. Despite these hopeful signs, the reef's health has deteriorated over the past four years. The quadrat survey showed a 50% increase in dead coral across the reef between 2006 and 2007, and a 33% increase since the 2004 survey. Results suggest that corals stressed by oil appear more susceptible to epidemic disease and appear to have a harder time recovering from fish bites and bleaching (Goreau and Hilbertz 2004). Since 2004, based on quadrat surveys, a statistically significant increase in dead corals was found. Urchin abundance also showed a significant increase, as did the calculated sediment biogenic index. The documented increases in coral disease, fish bites, water turbidity, and sedimentation on corals, and declines in water quality and fish abundance and diversity, can be interpreted as a decline in overall reef health.

Figure 13: Incidences of coral disease and fish bites on the reef have increased dramatically since the oil spill in 2005.


The survival of this reef, which is thriving in extreme environmental conditions, clearly demonstrates its resilience through the years. At the start of the experiment in 2004, photos indicated that the reef was healthy and considered in pristine condition. Visibility was high, the water was clear, and sea urchin population counts were relatively moderate. The sediment biogenic index initially suggested a healthy reef, and little evidence of coral disease was noted. Data from 2004/2005, prior to the oil spill, serves as a reference for baseline conditions, not only for this study, but also for any future coral reef studies in this region.
As man encroaches, human impact is no longer in question. Fishermen have relocated closer to the reef, beach houses that were under construction are now occupied, and with the newly constructed major shipping port, local shipping and oil offloading traffic has increased significantly. Enormous tanker ships transiting in very shallow water are displacing large amounts of sediment that appears to be ending up on the reef and suffocating the corals. The Red Sea coastline here is being developed at an alarming rate without concern for the impact this will have on the local environment.

Figure 14: A Four-year comparison along Transect One taken each year at the same location. The degradation over time is seen.

The statistically significant increase in the urchin population in 2007 can most likely be attributed to the tremendous increase in algae coverage observed on the reef. The increase in algae coverage can in turn be attributed to the excess amount of nutrients measured in the water. Excess nitrogen (DIN) levels, whose probable sources are human sewage, greatly exceed expected values. The source of excess phosphorus (SRP) in water samples is uncertain, but the infectious agents that cause diseases may feed off these extra nutrients and coliform bacteria. Examination of the sediment indicates an increase in the percentage of coral fragments and increasing mortality among coral species.

Based on the survival of reefs in this region for so many years, we can infer that select corals and their inhabitants can successfully thrive under extreme conditions of temperature and salinity. Comparison with other available reef data suggests that these ecosystems have adapted and appear more resilient to large daily, seasonal, and interannual temperature variations than more southerly reefs, or northern reefs in less extreme environments. Anthropogenic stressors are believed to be responsible for the recent degradation to this and neighboring reefs. The reef is rapidly becoming surrounded by man-made influences that will inevitably affect reef health. Threats include: a) increased shipping traffic, especially from oil tankers, b) continued growth of the new shipping port, c) increased nutrient loading from ships dumping waste, fertilizer factories, and outdated water treatment systems, d) increased tourism and urbanization, e) increased sedimentation and runoff caused by urbanization, f) physical damage from careless boaters or swimmers, g) and continued beachfront construction. As these man-made factors intensify, the fate of the reef becomes increasingly questionable.

Photos of staghorn coral patch from 2004 to 2007: from healthy state, to signs of stress and damage, to smothered in algae, to dead and breaking apart.
Figure 15: A Four-year comparison along Transect two taken each year at the same location. The degradation over time is seen.


Based on four years of data, the fate of this reef is uncertain, although the resilience of this reef community appears to be very strong. Population statistics of coral coverage indicate no significant difference over four years, yet bio-indicators show statistically significant changes in the biogenic composition of the sediment and the sea urchin population, and mixed results from the corals' biodiversity index calculated along each transect. It is speculated that the measured decline in reef health and documented increase in coral disease across the reef since 2005 (Figures 14 and 15) were strongly influenced by the oil spill. This trauma may have made the reef community less resistant to the natural stresses it normally tolerates.

Figure 16: The Simpson Index measures biodiversity and population evenness based on the amount and number of species present. This index varies greatly depending on a transects location on the reef with deeper transects tending to be healthier. The water depth ranged from 0.5 to 3.0 m along the ten-meter transects. Changes in the index can be attributed to shifts in coral coverage and type.

The shifting of corals and bottom coverage on the reef and the notable increase in coral fish bites, bleaching, and diseases suggest an inability of the coral to heal from the sudden onslaught of many anthropogenic stresses. The decline in fish abundance and diversity observed in 2006 and 2007 is thought to have been caused by oil damaging or depleting the reef of healthy corals that are necessary as food and habitat. Whatever it is, the extensive data suggest that the decline in reef health is occurring from man-made factors rather than natural causes. Zaki's Reef may soon reach a point at which equilibrium within this ecosystem can no longer be achieved, and a community that has thrived for hundreds if not thousands of years will be gone in less than a decade.

This study has established a reference point for comparison with local reefs, or those experiencing similar conditions, and will be key to any future conservation and restoration efforts in the area. Future plans include continuing to monitor this reef and making comparisons with other reefs worldwide. The culmination of this research will establish a data set that can be used by decision makers to implement future restoration and marine conservation measures for similar reefs. Disease types, and potential causes for the increased occurrence of coral diseases and fish bites, will be looked at in greater detail.
I plan to share my results from this extensive time series of measurements for this Gulf of Suez fringing reef. My effort includes making the local population aware of how they can reduce damage to local reefs by educating them about the simple preventative measures they can undertake to maintain local reef health and hopefully extend the lives of these stressed communities for future generations.

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