Monitoring of coastal coral reefs near Dahab (Gulf of Aqaba, Red Sea) indicates local eutrophication as potential cause for change in benthic communities

  • Malik S. Naumann
  • Vanessa N. Bednarz
  • Sebastian C. A. Ferse
  • Wolfgang Niggl
  • Christian Wild
Article

Abstract

Coral reef ecosystems fringing the coastline of Dahab (South Sinai, Egypt) have experienced increasing anthropogenic disturbance as an emergent international tourism destination. Previous reports covering tourism-related impacts on coastal environments, particularly mechanical damage and destructive fishing, have highlighted the vital necessity for regular ecosystem monitoring of coral reefs near Dahab. However, a continuous scientific monitoring programme of permanent survey sites has not been established to date. Thus, this study conducted in situ monitoring surveys to investigate spatio-temporal variability of benthic reef communities and selected reef-associated herbivores along with reef health indicator organisms by revisiting three of the locally most frequented dive sites during expeditions in March 2010, September 2011 and February 2013. In addition, inorganic nutrient concentrations in reef-surrounding waters were determined to evaluate bottom-up effects of key environmental parameters on benthic reef community shifts in relation to grazer-induced top-down control. Findings revealed that from 2010 to 2013, live hard coral cover declined significantly by 12 % at the current-sheltered site Three Pools (TP), while showing negative trends for the Blue Hole (BH) and Lighthouse (LH) sites. Hard coral cover decline was significantly and highly correlated to a substantial increase in turf algae cover (up to 57 % at TP) at all sites, replacing hard corals as dominant benthic space occupiers in 2013. These changes were correlated to ambient phosphate and ammonium concentrations that exhibited highest values (0.64 ± 0.07 μmol PO43− l−1, 1.05 ± 0.07 μmol NH4+ l−1) at the degraded site TP. While macroalgae appeared to respond to both bottom-up and top-down factors, change in turf algae was consistent with expected indications for bottom-up control. Temporal variability measured in herbivorous reef fish stocks reflected seasonal impacts by local fisheries, with concomitant changes in macroalgal cover. These findings represent the first record of rapid, localised change in benthic reef communities near Dahab, consistent with indications for bottom-up controlled early-stage phase shifts, underlining the necessity for efficient regional wastewater management for coastal facilities.

Keywords

Top-down and bottom-up control Inorganic nutrient enrichment Herbivory Coral-algal interactions Tourism South Sinai Egypt 

Introduction

In comparison to many other oceanic regions, where in recent decades tropical coral reef ecosystems have declined significantly due to impacts from an array of global (e.g. ocean warming) and often local (e.g. overfishing, eutrophication) stressors, shallow water reefs of the Red Sea may currently be considered comparably intact (Hoegh-Guldberg et al. 2007; Kotb et al. 2008; Wilkinson 2008). Except for the 1998 global mass coral bleaching event, which caused severe damage in reefs of the Southern Red Sea (Wilkinson 2004) and findings of reduced coral calcification in the Central Red Sea due to ocean warming (Cantin et al. 2010), impacts of global climate change until now appear remarkably low. Recently, this even gave rise to the theory of the Gulf of Aqaba in the Northern Red Sea being a potential future refuge for scleractinian corals from threats of global change (Fine et al. 2013). Nevertheless, there is existing evidence for severe Red Sea coral reef degradation, highlighted by a decline of >30 % in living hard coral cover at particular sites, also in the Gulf of Aqaba (Riegl and Velimirov 1991; Jameson et al. 1999; Wilkinson 2004, 2008). Main reasons for this decline during past decades were local impacts of intense coastal development (construction, sewage discharge, solid waste and sedimentation) and direct mechanical damage (coral breakage by divers, snorkelers and shipping activities) associated with an expanding regional tourism industry (Rinkevich 2005; Wilkinson 2008).

Tourism was initially introduced along the Egyptian Gulf of Aqaba coastline in the 1970s and experienced exponential growth since the late 1980s, becoming the prime regional source of income (Hawkins and Roberts 1994; PERSGA 2001; Rinkevich 2005). Until the Arab Spring revolution of 2011, tourism represented the major foreign exchange earning sector in Egypt, with coastal tourism as its major subsector reaching two million tourists at the Gulf of Aqaba in 2003 (Cesar 2003; OECD 2006). About 60 % of these visited local reef environments as divers or snorkelers, causing significant ecosystem degradation (SEAM 2004a; Rinkevich 2005; Jobbins 2006). While initial tourism development focussed on the Sharm el-Sheikh area located at the southern end of the Gulf of Aqaba, Dahab became a world-renowned dive destination for an increasing (non-quantified) number of tourist visitors by the late 1990s. Since then, tourism-related activities, especially extensive diving and snorkelling, promoting mechanical damage and sediment resuspension, have been identified as major threats to the coastal reef environments of Dahab. In this area, accepted site sustainability limits (5000–6000 dives a−1) have been exceeded by far, reaching >30,000 dives a−1 for popular dive sites (Hawkins and Roberts 1997; Cesar 2003; Hasler and Ott 2008).

The Dahab reef sites investigated by the present study are located within the Nabq and Abu Galum Managed Resources Protected Area, for which authorities issue fishing permits exclusively to resident Bedouin tribes. However, actual fishing regulations are unenforced and practiced techniques, including destructive net fishing and trampling, are impacting coastal reefs in the Dahab area (Hannak 2008; Samy et al. 2011; Hannak et al. 2011). Eutrophication and pollution of coastal waters may represent another potential, yet underinvestigated, local impact on the reefs near Dahab, resulting from intense construction of on-shore hotel and gastronomic facilities in direct reef vicinity, mostly without connection to the public sewage treatment systems. Information concerning this topic is sparse, except for one previous study reporting that up to 60 % of Dahab residents may not be serviced by the public sewage system due to insufficient infrastructure and maintenance, while poorly treated sewage may be released into the desert from pools of biological oxidation treatment systems (EcoConServ 2005). The same study suggested seepage of untreated sewage from septic tanks operated by remotely located tourism facilities to coastal waters and its use for coastal plant irrigation as potential threats to fringing coral reef environments.

Current awareness of potential local stressors and existing evidence for local coral reef degradation emphasise the vital necessity for regular ecosystem monitoring in Dahab to enable detection of rapid reef community shifts and identification of driving factors. However, a continuous scientific monitoring programme of permanent study sites has not been established to date. The few previous studies including reef ecosystem assessments conducted in the Dahab region each have generated snapshots of individual reef sites in time only or have focussed on selected benthic community categories (e.g. hard corals), while the application of different survey techniques unfortunately impedes the comparison of their findings (Ammar et al. 2006; Hasler and Ott 2008; Tilot et al. 2008; Ammar 2009). Indeed, generating quantitative information for the detection of spatio-temporal variability in coral reef communities necessitates reassessments of identical monitoring parameters at permanent study sites by applying identical survey techniques over time (e.g. Sweatman et al. 2008).

Thus, the aims of the present study were (1) to establish the first continuous scientific reef ecosystem monitoring of identical survey sites within the Dahab region investigating benthic and reef fish communities for spatio-temporal variability and (2) to identify relevant bottom-up and top-down factors controlling benthic reef community composition. To this end, three reef sites were surveyed during three expeditions to Dahab from 2010 to 2013 to assess benthic and fish community composition, the occurrence of coral-algae contacts, abundance of herbivorous sea urchins and inorganic nutrient concentrations in reef-surrounding waters.

Materials and methods

Study sites

Three of the most frequented coral reef dive sites (i.e. ‘Blue Hole’, ‘Lighthouse’ and ‘Three Pools’; Fig. 1) located on the coastline of Dahab (Gulf of Aqaba, Red Sea) were selected for continuous reef ecosystem monitoring and assessed accordingly during three expeditions carried out in March 2010 (winter), September 2011 (autumn) and February 2013 (winter). The study site Lighthouse (LH) is located close to Dahab City Center, while Blue Hole (BH) and Three Pools (TP) both are remotely located ca. 9 km north and south of LH, respectively. All monitored reef sites are situated close to shore (<100 m) but differ regarding their distinct bathymetry and local current exposure. Dahab experiences nearly year-round north-northwest winds of variable strength that drive southwards-directed long-shore currents (EcoConServ 2005). BH and LH are characterised by steep reef slopes facing oceanic waters and exposed to long-shore surface currents up to 50 cm s−1 flow velocity suggesting short water residence times, while the shallow bathymetry of TP is expected to experience low long-shore current velocities (<12 cm s−1) due to its sheltered positioning south off the Dahab headland (EcoConServ 2005; Fig. 1). All three sites have experienced significant coastal development. The planar area covered by tourism-related facilities approximately doubled at the sites BH (ca. 3050 to 6500 m2) and LH (ca. 4850 to 10,050 m2) between the years 2004 and 2013, while at TP a 4.6-fold increase (ca. 1970 to 8990 m2) occurred within the same period (derived from Google Earth© software, Google Inc.). Facilities at the remote sites BH and TP are not connected to the Dahab City Center sewage treatment system, and restaurants on-site maintain restroom facilities with independent septic tank systems. In close vicinity (<300 m) to TP, a large hotel resort with extensive, irrigated gardens was established between 2002 and 2010 (personal observation M. Naumann).
Fig. 1

Location map of the three monitored reef sites within the Dahab region (Southern Sinai, Egypt) with general map of the Sinai Peninsula (small panel). Exact study site coordinates are provided in Table 1

Benthic surveys

Benthic reef community composition was assessed for each study site along three transects at 7-m water depth according to the line-point intercept (LPI) transect survey method (Loya 1978; Nadon and Stirling 2006) using SCUBA. For each of the triplicate LPIs, a 50-m measuring tape was rolled out on the seafloor and the type of substrate for a point directly beneath the transect line was recorded every 0.5 m, resulting in 101 data points. The start and end coordinates of all LPIs are presented in Table 1. Prior to all LPIs, methodological consistency in substrate identification among surveyors was ensured by conducting trial transects including subsequent joint identification training. The substrate was categorised as ‘hard coral’ (including scleractinian and hydrozoan corals), ‘soft coral’, ‘macroalgae’, ‘turf algae’ or ‘crustose coralline red algae’ (CCA). Stable biogenic reef rock never occurred completely uncovered but was either overgrown by turf algae or CCA. Therefore, the category turf algae also included stable substrate with sparse overgrowth by filamentous turf algae. Sandy carbonate sediments without visible turf algae overgrowth was recorded as ‘sand’, while all other substrate types (also animal and plant taxa) were recorded as ‘others’. The percentage benthic cover for each substrate category was subsequently derived by relating the substrate-specific counts to the total number of points for all individual LPIs.
Table 1

Transect start and end coordinates of benthic and reef fish surveys conducted at the three Dahab reef sites between 2010 and 2013

Site

Start

End

Blue Hole

28° 34′ 18.83″ N, 34°32′ 14.39″ E

28°34′ 14.79″ N, 34°32′ 11.28″ E

Lighthouse

28°29′ 54.57″ N, 34°31′ 14.45″ E

28°29′ 57.63″ N, 34°31′ 17.86″ E

Three Pools

28°26′ 5.54″ N, 34°27′ 26.96″ E

28°26′ 9.16″ N, 34°27′ 30.50″ E

Length of line-point intercept transects is three times 50 m each. Water depth of transects is 7 m. Coordinates are derived from the mapping software Google Earth© (Google Inc.)

The occurrence of coral contacts with adjoining benthic algae taxa was inspected for every hard coral colony recorded during the 2010 expedition. Only contact zones visible vertically above the coral colonies were included. The type of benthic algae involved (i.e. macroalgae, turf algae or CCA) and the type of contact (i.e. ‘overgrowth’, ‘coral damage’, ‘equilibrium’ or ‘bulge formation’) were noted. ‘Overgrowth’ described the overgrowth by algae on dead or living coral tissue with or without any visible physiological response by the coral. If no overgrowth of the coral was observed, but pigmentation changes, damaged or dead tissue were visible, the contact was categorised as coral damage. If no overgrowth or coral damage were observed, the contact was noted as either equilibrium or bulge formation. Bulge formation was specified as the development of a bulge towards the adjoining algae, potentially functioning as a physical barrier (Haas et al. 2010), while equilibrium specified a stable co-existence of coral and algae.

The abundance of herbivorous sea urchin taxa (i.e. Phyllacanthus imperialis, Echinothrix diadema, Echinometra cf mathaei, Heterocentrotus mammillatus, Microcyphus rousseaui) was quantified within 1 m on each side of all benthic LPI surveys conducted during the 2011 and 2013 expeditions to investigate their potential as top-down control parameter for changes in local benthic reef communities.

Reef fish surveys

Pelagic fish surveys were conducted on the same dates (expeditions 2010–2013) and locations of all benthic LPIs applying the line transect technique (English et al. 1997). All reef fish surveys took place between 10 am and 3 pm and focussed on quantifying the abundance of known herbivorous families (i.e. Acanthuridae, Scaridae and Siganidae) and families comprising potential reef health indicator species (i.e. Chaetodontidae and Pomacanthidae). Fishes were identified according to the Reef Check survey manual specified for the Red Sea region (Hodgson et al. 2006). Prior to all reef fish surveys, identification trials were performed among surveyors in order to ensure data quality. Before the onset of each line transect, surveyors withdrew from the survey area for a minimum of 5 min to allow fishes to resume normal behaviour (Fowler 1987). One surveyor out of a three to six person SCUBA team swam slowly (ca. 5 m min−1) along the 50-m line transect and counted all individuals of target fish families within 1 m on either side and within the water column 5 m above the transect. Surveys were repeated three to six times to minimise observer bias variance. Fish abundance was normalised to the number of individuals per 250-m2 reef area.

Inorganic nutrients

Inorganic nutrient concentrations in surface waters of the three study sites were measured during the 2010 and 2013 expeditions to investigate spatial variability and to evaluate the potential site-specific impact of sewage discharge from coastal tourism-related facilities (i.e. hotels and on-shore restaurants). Sampling was carried out once per site during each expedition on the same date and location of the respective transect surveys. In 2010, ammonium (NH4+) and phosphate (PO43−) concentrations were determined on-site from sterile-filtered triplicate water samples (20 ml) using a Genesys 10 UV spectrophotometer with ammonium and phosphate test kits (Spectroquant, Merck®). The specified lower determination limit for ammonium was 0.76 μmol NH4+ l−1, while the regression-derived phosphate determination limit was 0.05 μmol PO43− l−1 (R2 = 0.998, n = 6). In 2013, nitrate (NO32−) and nitrite (NO2) concentrations were analysed in addition to ammonium and phosphate applying improved laboratory-based techniques. To this end, triplicate seawater samples (50 ml) were filtered through pre-combusted (450 °C, 5 h) GF/F filters into sterile HDPE vials and stored frozen pending analysis. Ammonium was analysed fluorometrically (Holmes et al. 1999), while nitrate, nitrite (Strickland and Parsons 1968) and phosphate (Murphy and Riley 1962) concentrations were quantified photometrically (Trilogy Laboratory Fluorometer plus modules, Turner Designs).

Data analyses

Spatial and temporal trends in all benthic, reef fish and inorganic nutrient data sets were analysed statistically using one-way ANOVA with Tukey or Holm-Sidak post hoc tests, unless mentioned otherwise, after testing for equal variances (Levene test) and normal distribution (Kolmogorov-Smirnov test). If assumptions for parametric analysis were not met, the Kruskal-Wallis test was applied. Correlations between benthic substrate types, fish abundance and inorganic nutrient concentrations were tested for individual expedition years and temporal change between expeditions using the Pearson product-moment (PPM) correlation and multiple linear regression (MLR) analysis. All statistical analyses were carried out using SigmaPlot software packages (v. 12.5, Systat Software Inc.). Regional mean values for “overall Dahab” (DH) were calculated as the average of all three study sites. For certain analyses, the fish families Acanthuridae, Scaridae and Siganidae were grouped as ‘total herbivorous fishes’.

Results

Benthic community

At the start of monitoring in 2010, hard corals represented the dominant benthic substrate in fringing reefs of Dahab (mean ± SD 36 ± 5 %) and showed similar percentages of benthic cover at all three study sites (Table 2). Turf algae covered the second largest benthos fraction at all sites and DH (mean ± SD 27 ± 7 %), except for BH, where turf algae cover was significantly lower in 2010 (ANOVA, F(2,6) = 8.376, P = 0.018) and soft corals dominated compared to LH and TP (ANOVA, F(2,6) = 11.688, P = 0.009). While sand cover was significantly higher at TP compared to LH and BH (ANOVA, F(2,6) = 27.261, P < 0.001), macroalgae, CCA and other substrates were similar at all sites. From 2010 to 2011, hard coral cover decreased significantly (by 11 %) at TP only (ANOVA, F(2,6) = 104.484, P < 0.001), and thereafter was significantly lower at this site compared to LH and BH (ANOVA, F(2,6) = 8.113, P = 0.020). Soft coral cover decrease from 2010 to 2011 was significant at all sites (DH mean 9 %, Table 2) but most pronounced at BH (ANOVA, F(2,6) = 5.955, P = 0.038). Turf algae cover showed no significant temporal change and was similar at all sites in 2011, while macroalgae increased (by 18 %) at TP (ANOVA, F(2,6) = 159.931, P < 0.001) to significantly higher cover than at LH and BH (ANOVA, F(2,6) = 38.087, P < 0.001).
Table 2

Percentage cover of dominant benthic substrates and abundances of selected reef fish families and herbivorous sea urchins in three fringing coral reefs of Dahab (South Sinai, Egypt) monitored from 2010 to 2013

 

2010—March

2011—September

2013—February

Site

BH

LH

TP

DH

BH

LH

TP

DH

BH

LH

TP

DH

Benthic cover (%)

 Hard corals

40 ± 7

38 ± 6

31 ± 2

36 ± 5

44 ± 10

39 ± 9

20 ± 1

34 ± 13

34 ± 3

29 ± 3

19 ± 1

28 ± 7

 Soft corals

21 ± 6

12 ± 4

3 ± 3

12 ± 9

7 ± 3

2 ± 3

0

3 ± 4

13 ± 5

9 ± 1

1 ± 1

8 ± 6

 Turf algae

18 ± 6

32 ± 3

30 ± 4

27 ± 7

24 ± 10

30 ± 6

31 ± 4

29 ± 4

39 ± 5

44 ± 5

57 ± 11

47 ± 9

 Macroalgae

5 ± 2

7 ± 6

10 ± 2

7 ± 3

10 ± 4

12 ± 3

28 ± 2

16 ± 10

1 ± 1

3 ± 5

1 ± 2

2 ± 1

 CCA

10 ± 3

8 ± 3

7 ± 3

8 ± 2

10 ± 5

8 ± 3

10 ± 5

9 ± 1

6 ± 1

6 ± 6

3 ± 1

5 ± 2

 Sand

5 ± 2

3 ± 2

17 ± 3

8 ± 7

6 ± 1

9 ± 12

10 ± 4

8 ± 2

6 ± 2

6 ± 11

16 ± 8

10 ± 6

 Others

<1

<1

2 ± 1

1 ± 1

0

<1

1 ± 1

1 ± 1

0

4 ± 4

2 ± 1

2 ± 2

Fish abundance (250 m2 reef)−1

 Acanthuridae

18 ± 1

9 ± 3

32 ± 3

20 ± 12

10 ± 1

12 ± 6

6 ± 2

10 ± 3

21 ± 6

12 ± 4

20 ± 2

18 ± 4

 Chaetodontidae

10 ± 2

6 ± 2

12 ± 4

10 ± 3

12 ± 1

14 ± 5

8 ± 3

11 ± 3

11 ± 1

16 ± 1

10 ± 3

12 ± 3

 Scaridae

6 ± 3

6 ± 3

9 ± 2

7 ± 2

2 ± 1

2 ± 1

0

1 ± 1

5 ± 3

5 ± 3

4 ± 1

5 ± 1

 Siganidae

<1

5 ± 2

0

2 ± 3

0

<1

0

<1

1 ± 1

<1

1 ± 1

1 ± 1

 Pomacanthidae

1 ± 1

2 ± 2

3 ± 1

2 ± 1

2 ± 1

4 ± 1

4 ± 1

3 ± 1

<1

<1

1 ± 1

1 ± 1

Total herbivorous fishes

24 ± 4

20 ± 1

41 ± 5

28 ± 11

12 ± 1

14 ± 6

6 ± 2

11 ± 4

27 ± 6

19 ± 6

25 ± 4

23 ± 4

Herbivorous sea urchins (250 m2 reef)−1

336 ± 98

416 ± 72

397 ± 44

383 ± 74

267 ± 88

518 ± 199

352 ± 130

379 ± 168

All values are presented as mean ± SD. Fish and sea urchin abundances are normalised to (250 m2 reef)−1

BH Blue Hole, CCA crustose coralline red algae, DH overall Dahab, LH Lighthouse, TP Three Pools

In 2013, hard coral cover showed no significant change compared to 2011 at each of the sites, but a negative trend was observed for all individual sites and for DH (mean −8 %). Hard coral cover was significantly lower at TP than at LH and BH (ANOVA, F(2,6) = 21.671, P = 0.002), while likewise soft coral cover was significantly higher at LH and BH compared to TP (ANOVA, F(2,6) = 11.745, P = 0.008), showing a positive trend for both sites from 2011 to 2013. Turf algae showed a significant increase at all sites (ANOVA, F(2,6) = 6.855, P = 0.028), resulting in the highest turf algae cover (57 %) at TP (ANOVA, F(2,6) = 13.591, P = 0.006) and replacing hard corals as dominant benthic substrate type at all investigated Dahab reef sites (Table 2). Macroalgae showed significant decline at TP (ANOVA, F(2,6) = 159.931, P < 0.001) and BH (ANOVA, F(2,6) = 8.980, P = 0.016) reaching similar, yet low, percentage cover at all sites. CCA, sand and other substrates showed no temporal variability between 2010 and 2013.

During the 2010 expedition, 13 ± 7 % of all hard corals at the investigated Dahab reef sites were in direct contact with benthic reef algae. Of those corals, 97 % were in contact with turf algae and 3 % with macroalgae (Table 3). While the absolute number of coral-algal contacts was similar among sites, the percentage of hard corals in contact with benthic algae was significantly higher at TP (21 ± 3 %) compared to LH (6 ± 2 %) and BH (11 ± 2 %) (ANOVA, F(2,6) = 24.228, P = 0.001). The relative frequencies of coral-algal contact types for all sites and DH are shown Table 3. The overall most frequent type was equilibrium, followed by damage and overgrowth. Damage was pronounced in LH, whereas overgrowth was most frequent at TP; however, these differences were not statistically significant.
Table 3

Relative contribution of coral-algae contact types and percentage of turf algae involved in contacts for the three Dahab study sites during the 2010 expedition

Contact type

BH

LH

TP

DH

Equilibrium

73

57

59

63

Damage

12

43

3

19

Overgrowth

12

0

38

16

Bulge formation

4

0

0

1

Turf algae

100

93

97

97

Total contacts

13

7

16

36

Values are given as percent of the respective total number of contacts recorded at each site

BH Blue Hole, DH overall Dahab, LH Lighthouse, TP Three Pools

Bulk abundances of herbivorous sea urchin taxa recorded at the study sites in 2011 and 2013 are presented in Table 2. Except for LH, which showed a positive temporal trend, all sites and DH displayed a weak negative trend in abundance, averaging 379 ± 168 sea urchins (250 m2 reef)−1 (mean ± SD) in 2013. However, no statistically significant spatial or temporal differences were determined, neither in the comparison of each of the study sites nor among the expedition periods.

Reef fish community

In 2010, Acanthuridae represented the most abundant herbivorous fish family (Table 2) and were significantly more abundant at TP than LH (Kruskal-Wallis, H = 7.2, df = 2, P = 0.004). Siganidae (Kruskal-Wallis, H = 6.764, df = 2, P = 0.011) and abundance of total herbivorous fishes (Kruskal-Wallis, H = 6.489, df = 2, P = 0.011) likewise were elevated at TP compared to LH, while Scaridae showed no significant spatial variability. Chaetodontidae and Pomacanthidae were similar at all sites during 2010 and 2011 (Table 2). From 2010 to 2011, total herbivorous fishes decreased significantly at TP (ANOVA, F(2,6) = 57.954, P < 0.001) and BH (ANOVA, F(2,6) = 11.363, P = 0.009), while LH showed no temporal change in total herbivorous fishes but a significant decrease in Siganidae (Kruskal-Wallis, H = 7.261, df = 2, P = 0.004). Total herbivorous fishes and the individual families were similar in 2011 at all sites, while Pomacanthidae showed a positive trend from 2010 to 2011.

From 2011 to 2013, total herbivorous fishes increased significantly at BH (ANOVA, F(2,6) = 11.363, P = 0.010) and TP (ANOVA, F(2,6) = 57.954, P = 0.003), reaching similar abundances at all sites, which for BH and LH were comparable to 2010 values (Table 2). In 2013, TP abundances of total herbivorous fishes (ANOVA, F(2,6) = 57.954, P = 0.006) and Acanthuridae (ANOVA, F(2,6) = 82.156, P = 0.002) were significantly lower than those measured in 2010. Chaetodontidae abundance showed no change in 2013 and was similar at all sites, while Pomacanthidae decreased significantly at TP (ANOVA, F(2,6) = 5.749, P = 0.034) and LH (ANOVA, F(2,6) = 5.387, P = 0.046), reaching similar levels comparable to values recorded during the 2010 monitoring at all sites.

Inorganic nutrients

Results from ammonium and phosphate analyses during the 2010 expedition were below the method determination limit of 0.76 μmol NH4+ l−1 and 0.05 μmol PO43− l−1 at all study sites. During 2013, nitrate (0.8 ± 0.1 μmol NO32− l−1) and nitrite (0.18 ± 0.03 μmol NO2 l−1) concentrations were similar for all sites and, except for nitrate (0.5 ± 0.2 μmol NO32− l−1) at LH, within the range expected for the Gulf of Aqaba (Naumann et al. 2010) during winter season (Fig. 2). For ammonium and phosphate, only BH (0.39 ± 0.06 μmol NH4+ l−1, 0.08 ± 0.10 μmol PO43− l−1) was found to be in the expected seasonal range, while LH showed elevated concentrations (0.84 ± 0.33 μmol NH4+ l−1, 0.27 ± 0.13 μmol PO43− l−1), which were however not significantly different from BH (NH4+: ANOVA, F(2,6) = 8.705, P = 0.062; PO43−: ANOVA, F(2,6) = 21.814, P = 0.065). Significantly elevated concentrations compared to expected seasonal ranges were determined for TP (1.05 ± 0.07 μmol NH4+ l−1, 0.64 ± 0.07 μmol PO43− l−1), where ammonium was higher than at BH (ANOVA, F(2,6) = 8.705, P = 0.019), yet similar to LH (P = 0.244), while phosphate was significantly higher than at BH (ANOVA, F(2,6) = 21.814, P = 0.002) and LH (P = 0.011).
Fig. 2

Inorganic nutrient concentrations measured in fringing coral reefs of Dahab during the 2010 and 2013 expeditions. Long-dashed lines indicate expected regional winter season concentration ranges (Naumann et al. 2010). Dotted lines indicate method determination limits of 2010 analyses. Letters (A, B, AB) indicate significant differences as determined in post hoc tests. Values are given as mean ± SD. BH Blue Hole, LH Lighthouse, TP Three Pools

Correlation analysis

Decline of hard coral cover between 2010 and 2013 was significantly and highly correlated to the increase of turf algae cover measured during the same period across all study sites (PPM, R = −0.962, P < 0.001; Fig. 3). From 2010 to 2011, hard coral decline also showed a significant negative correlation to macroalgae increase at TP (PPM, R = −0.965, P = 0.002) and DH (PPM, R = −0.869, P = 0.025). Across all study sites in 2013, among all potential top-down, bottom-up and competing organism parameters (i.e. herbivorous fishes, herbivorous sea urchins, macroalgae, turf algae, ambient ammonium and phosphate concentrations), only ambient phosphate concentrations significantly predicted hard coral cover (MLR, P = 0.029). Accordingly, the site with the highest phosphate concentration (TP) showed the lowest hard coral cover. Likewise, soft coral cover in 2013 was significantly and negatively correlated to phosphate (PPM, R = −0.926, P < 0.001) and ammonium (PPM, R = −0.717, P = 0.030) concentrations reflecting lower soft coral cover under elevated inorganic nutrient levels, as found at TP (Fig. 2).
Fig. 3

Correlation of living hard coral cover and turf algae cover including all benthic data sets collected for the three Dahab fringing reef monitoring sites during three expeditions (2010, 2011 and 2013). Values are given as mean ± SE of percentage benthic cover. Hard coral cover includes scleractinian and hydrozoan corals

As for soft corals, turf algae cover in 2013 showed significant correlation to ambient ammonium concentrations (PPM, R = 0.737, P = 0.0234) across all reef sites. The substantial increase of turf algae measured between 2011 and 2013 around Dahab was significantly correlated to ambient phosphate concentrations (PPM, R = 0.687, P = 0.041), and likewise showed positive correlation to abundances of Acanthuridae (PPM, R = 0.863, P = 0.027), Scaridae (PPM, R = 0.818, P = 0.046) and total herbivorous fishes (PPM, R = 0.837, P = 0.038) at the site TP. Significant correlations were found for macroalgae and total herbivorous fish abundances across all study sites for changes from 2010 to 2013 (PPM, R = −0.435, P = 0.023) and more specifically at BH for macroalgae and total herbivorous fishes (PPM, R = −0.707, P = 0.033) as well as Siganidae (PPM, R = −0.722, P = 0.028). The recorded macroalgae increase between 2010 and 2011 was correlated to decreases of Scaridae at LH (PPM, R = −0.866, P = 0.0259), as well as decreased Acanthuridae (PPM, R = −0.993, P < 0.001), Scaridae (PPM, R = −0.983, P < 0.001) and total herbivorous fish (PPM, R = −0.993, P < 0.001) abundances at TP. The subsequent decrease in macroalgae cover from 2011 to 2013 showed correlation to increasing abundances at all study sites for total herbivorous fishes (PPM, R = −0.904, P = 0.014), Acanthuridae (PPM, R = −0.840, P = 0.037) and Scaridae (PPM, R = −0.893, P = 0.017), at TP for Acanthuridae (PPM, R = −0.974, P < 0.001), Scaridae (PPM, R = −0.974, P = 0.005) and total herbivorous fishes (PPM, R = −0.959, P = 0.002), as well as at LH for Siganidae (PPM, R = −0.813, P = 0.049). For all remaining possible comparisons of spatio-temporal variability in benthic and reef fish categories, as well as ambient inorganic nutrient parameters, no significant correlations were found.

Discussion

The present study provides the first spatio-temporal coral reef monitoring data set resulting from a 3-year reassessment of benthic and reef fish communities at permanent study sites near the world-renowned tourism destination Dahab at the Gulf of Aqaba (Red Sea). To our knowledge, we present here the first combined generation and analysis of in situ data sets for bottom-up (i.e. inorganic nutrients) and top-down (i.e. benthic and pelagic herbivorous grazers) controlling parameters for benthic reef communities in the Southern Gulf of Aqaba. Our findings reveal a negative trend in hard coral cover at all Dahab study sites and a significant rapid hard coral decline at the current-sheltered site TP over the monitoring period (2010–2013). Temporal decline in hard coral cover shows strong correlation to a substantial increase in turf algae cover all over Dahab, eventually replacing hard corals as dominant benthic substrate at the majority of investigated reefs. This finding is consistent with what would be expected of longer-term phase shifts in benthic reef communities. These trends appear to be largely driven by elevated ambient inorganic nutrient concentrations (i.e. phosphate and ammonium), which were strongly correlated to the increase in turf algae cover as well as to low and high percentage contributions by hard corals and turf algae to benthic cover, respectively. These findings are consistent with expectations of inorganic nutrient enrichment acting as principle bottom-up control of turf algae biomass and suggest eutrophication of coastal reef-surrounding waters as likely main responsible cause for benthic community change towards turf algae dominance and concomitant ecosystem degradation observed in fringing coral reefs near Dahab.

Initial monitoring results for benthic fringing reef communities near Dahab in 2010 revealed a comparable community composition at all study sites, with hard corals as the dominant functional group covering on average 36 %, similar to the combined cover by the two next most abundant groups, turf algae (27 %) and soft corals (12 %). Overall hard coral contribution to benthic cover in 2010 is within the range previously reported for reefs near Dahab (33–37 %; Hasler and Ott 2008; Tilot et al. 2008) and for the wider Gulf of Aqaba (35–43 %, Kotb et al. 2008; Naumann et al. 2012), even for the lowest hard coral cover measured at the site TP (31 ± 2 %). Spatial variability in hard coral cover may result from an array of distinct biotic (e.g. predation/grazing pressure, settlement and recruitment success) and/or abiotic factors (e.g. inorganic nutrients and light availability), likewise affecting spatial variability in turf algae and soft corals (Van den Hoek et al. 1978; Sheppard 1982). However, to some extent, spatial trends in hard coral cover are likely promoted by site-specific bathymetric and hydrodynamic settings. The site TP is characterised by shallow, current-sheltered reef slopes, while BH and LH feature steep sloping environments exposed to the regional long-shore current regime. Low current velocities at TP may enhance sediment deposition of fine particulate matter, which is supported by our findings of higher sand cover at TP. Sedimentation reduces larval settlement and recruitment success for hard corals significantly, while likewise increasing physiological stress (Rogers 1990; Hodgson 1990, 1996). It furthermore reduces herbivory on algal turfs, thus exacerbating the threat posed by nutrient-enhanced growth of turf algae (Bellwood and Fulton 2008). Site-specific differences in hydrodynamic settings likely induce variable exchange rates of reef-surrounding with more oligotrophic oceanic waters (Rasheed et al. 2002). This may explain the higher cover of soft coral taxa that prefer habitats with enhanced water movement (Fabricius et al. 1995; Kremien et al. 2013; Wild and Naumann 2013), while suggesting nutrient-limited growth of low turf algae at the current-exposed (likely more oligotrophic) site BH in 2010.

Benthic community change

The significant correlation of hard coral decline to the successive rise of turf algae at the investigated Dahab reef sites over the entire monitoring period is consistent with what would be expected as early stage benthic community phase shifts involving the replacement of hard corals as dominant benthic taxa. Benthic phase shifts of formerly coral-dominated reefs towards benthic algae dominance and their concomitant ecosystem degradation have been documented worldwide over the last three decades (Hughes 1994; 2003; 2010; Gardner et al. 2003; Wilkinson 2008; McClanahan and Karnauskas 2010; Jouffray et al. 2014). Hard coral decline due to global and/or local disturbances, competition by rapidly growing benthic algae, and the absence of herbivorous grazers mostly lead to substantial decreases in architectural and functional complexity, severe habitat degradation and eventually loss of important ecosystem engineering capacities (Hughes et al. 1985; Mumby 2006; Alvarez-Filip et al. 2009; Wild et al. 2011; Roff and Mumby 2012). For the Dahab region, and likely the entire Southern Gulf of Aqaba, this is the first record of reef community change with characteristics of an early stage benthic phase-shift, appearing most pronounced at the site TP, where turf algae and hard coral cover in 2013 reach 57 and only 19 %, respectively. The apparent early stage benthic phase shifts observed here seem as an exclusive effect of local stressors, as no indication by records or further evidence of significant local temperature anomalies and bleaching events exist for the present monitoring period (ReefBase database 2013).

Space competition between hard corals and benthic reef algae represents a key ecological process, especially in degrading reef communities (Jompa and McCook 2003; McManus and Polsenberg 2004; Naumann et al. 2013), where contact to adjoining benthic algae may cause coral diseases or mortality, eventually resulting in the replacement of living corals by benthic algae (Nugues et al. 2004; Kline et al. 2006). Recent research suggests that hard corals are rapidly replaced by benthic algae competing for space along hypoxic or anoxic interaction zones generated by enhanced microbial respiration in turn fuelled by algae-derived organic matter release. Coral mortality follows as the consequence of reduced oxygen availability and increased coral pathogen abundance (Smith et al. 2006; Wild et al. 2010; Haas et al. 2011, 2013; Barott and Rohwer 2012). Our findings for types of coral-algae contacts in 2010 support the significant role of turf algae as responsible agent for the overall negative trend in hard coral cover and for its rapid decline at TP in 2011, as turf algae account for 97 % of all coral-algae contacts recorded in 2010. In addition, the percentage of hard corals with associated coral-algae contacts (21 %) and the occurrence of contact type overgrowth are highest at TP, suggesting a direct relation between the rapid 11 % hard coral decline (in 2011) and the 41 % sum of damage and overgrowth coral-algae contacts recorded at TP (in 2010). This is supported by previous findings describing turf algae as the most frequent (77–90 % of coral-algae contacts) and rapidly overgrowing benthic algae group involved in coral-algae contacts in the Gulf of Aqaba (Haas et al. 2010).

Top-down vs. bottom-up control

Growth of benthic algae is either bottom-up controlled by factors such as ambient inorganic nutrient availability or top-down regulated by the abundance of pelagic and benthic herbivorous grazers (e.g. Hughes 1989; Smith et al. 2001). In top-down regulated reefs, a strong negative correlation between benthic algae growth and the abundance of herbivorous grazers is expected, while under bottom-up control a positive correlation of algae biomass and inorganic nutrient concentration has been described (e.g. Russ 2003). Turf algae cover during 2013 and its increase at all Dahab study sites (2011 to 2013) both were significantly correlated to levels of ambient phosphate and ammonium. Together with lacking negative correlation to any of the herbivorous fish groups, this provides evidence consistent with the expectation for bottom-up control of turf algae biomass by ambient inorganic nutrient concentrations. This has particular relevance for the site TP, where phosphate and ammonium were significantly elevated together with the most substantial increase in turf algae cover (26 %) from 2011 to 2013. For the Gulf of Aqaba, bottom-up control of rapid benthic algae growth is confirmed by an unusual deep vertical mixing event of the water column following the eruption of Mount Pinatubo in 1991, causing elevated inorganic nutrient concentrations (1.2 μmol NO32− l−1), while inducing rapid algae growth and mass mortality of corals in reefs of Eilat (Genin et al. 1995). In this context, our findings for elevated inorganic nutrient concentrations during the 2013 winter expedition, coinciding with seasonal vertical mixing events (Wolf-Vecht et al. 1992), show enrichment well above seasonal variability indicated by nitrate and nitrite concentrations conforming with expected seasonal ranges, while exhibiting site-specific enrichment for ammonium and phosphate at the site TP only.

The observed trends in the algal community revealed distinct dynamics of the different functional algae groups, which suggest functional group-specific roles of top-down vs. bottom-up factors. Increases in turf algae cover at TP between 2011 and 2013 were positively correlated to increases in herbivorous fishes, Acanthuridae and Scaridae abundances. This observation may be explained by previous studies demonstrating stimulated benthic algae growth in reefs with high herbivorous grazing and elevated inorganic nutrients (Tanner 1995; Littler et al. 2006). In contrast to turf algae, macroalgae showed no consistent increase but rather seasonal fluctuations. The missing correlation of macroalgae cover with inorganic nutrient concentrations, together with an overall negative correlation to herbivorous fish abundances, suggest effective top-down control of macroalgae cover in reefs near Dahab during the winter season. Thus, top-down control of benthic algae by herbivorous fishes appears exclusively effective for macroalgae, while elevated inorganic nutrient levels apparently drive the rapid growth of turf algae even at higher herbivorous fish abundances during winter, which is consistent with expectation of bottom-up control. In this context, grazing by herbivorous sea urchins appears as a constant and spatially unspecific process that is not correlated to trends in any of the algae groups and thus appears secondary to the effects of nutrients and herbivorous fishes. Negative correlations between macroalgae and herbivorous fishes together with strong seasonal variability for both may reflect seasonality of local fishing pressure (high in summer), only allowing for effective top-down control of macroalgae during winter (low fishing) season (Mabrouk 2007). The role of fishing in influencing fish community structure is further underlined by the fact that Chaetodontidae and Pomacanthidae, which in contrast to the herbivorous fish groups are not targeted by local fisheries (Mabrouk 2007), did not show such marked seasonal fluctuations. Partial recovery of herbivorous fish stocks in 2013 after seasonal decline is only detected at the sites BH and LH, while at TP abundance of herbivorous fishes is found lower than in 2010, suggesting a link to the identified local trends in hard coral cover and lag effects of hard coral depletion on the fish community (Wilson et al. 2006).

Impact of eutrophication

The observed changes in benthic reef communities near Dahab are consistent with indications of early-stage phase shifts which appear to be driven by ambient inorganic nutrient enrichment likely resulting from sewage discharge by intense tourism-related coastal development. Eutrophication caused by sewage discharge to coastal waters occurs commonly as a consequence of relatively poor sewage treatment facilities in coastal provinces of the Southern Sinai Peninsula, often amounting to little more than open settling pools for biological oxidation (EcoConServ 2005). Urban provinces, like Sharm-el-Sheikh, are connected to modern sewage treatment facilities, while smaller regions like Dahab are still not fully serviced due to insufficient infrastructure or lack of maintenance, in particular at remote coastal locations. Consequently, insufficiently or non-treated sewage is being released into the environment or being used for irrigation, causing potential seepage to coastal waters (EcoConServ 2005). This may generate elevated inorganic nutrient concentrations and cause a general decline in ambient water quality. Site-specific eutrophication levels may be significantly affected by local current exposure controlling exchange rates of the reef-surrounding water body with oligotrophic oceanic waters. Sheltered sites with low current exposure such as TP may thus experience increased nutrient enrichment due to potential accumulation of locally discharged sewage compared to current-exposed sites with comparable sewage discharge. Our site-specific findings for elevated phosphate and ammonium levels and personal communications with local responsible parties confirm these observations and point to seepage from septic tanks and/or irrigation of poorly or untreated sewage water from remotely located coastal facilities as responsible drivers of ecosystem degradation of fringing coral reefs near Dahab.

Records of regional eutrophication impacts exist for the developed urban area of Eilat at the Northern tip of the Gulf of Aqaba, where coastal coral reefs have been affected by intense sewage discharge and fish mariculture causing up to 76 % loss of hard coral cover at impacted sites between 1986 and 2000 (Loya 2004). Shallow warm-water coral reefs are regarded as highly oligotrophic, nitrogen and phosphorus-limited marine environments, where rapid uptake and utilisation processes for surplus-available inorganic nutrient sources are expected (Smith 1984). In this context, our findings of elevated phosphate (0.6 μmol PO43− l−1) and ammonium (1.1 μmol NH4+ l−1) concentrations above seasonal range, in reef waters approximately 100 m from shore in 7-m water depths, appear even more substantial, and put in question actual concentration maxima close to the origin of local eutrophication. Previous studies conducted in Eilat reveal significant hard coral decline and increased partial coral mortality in reefs exposed to total oxidised nitrogen (TON, NO2 + NO32) concentrations above a threshold of 0.4 μmol TON l−1 (annual mean, Wielgus et al. 2004). The range of TON concentrations (0.7 to 1.0 μmol TON l−1, means of all sites) measured here during winter 2013 (peak season) thus indicates that some coastal reefs near Dahab may already be close to this threshold, while others (e.g. TP) may have crossed it. Taking into account our 2010 inorganic nutrient values (i.e. the method determination limits), a noticeable increase in ambient concentrations of ammonium and phosphate at the eutrophicated site TP over the entire study period becomes evident. This evidence for increasing local eutrophication further supports our lead regarding indicative bottom-up control of benthic community change observed at TP.

Recovery of impacted coastal reefs near Dahab appears unlikely in the light of continuing eutrophication combined with the apparent seasonal peaks of fishing impacts. However, the Arab Spring Revolution of 2011 and its resulting regional political instability have caused drastic declines of touristic visitor numbers in Egypt, in particular in tourism destinations such as Dahab (CAPMAS 2014). Contemporary lower tourism levels may eventually reduce eutrophication in reef-surrounding waters and provide the crucial opportunity for local reef ecosystem recovery. Local capacity for recovery from severe coral mortality (up to 25 %) caused by outbreaks of crown-of-thorns starfish Acanthaster planci populations in isolated reefs of Dahab between 1998 and 2002 has been observed, with growth of juvenile hard corals within only a few years after these events (Salem 1999; Ammar et al. 2006; Tilot et al. 2008). Nevertheless, neither the duration of the current period of relief from intense tourism impacts, nor the actual duration of continuing eutrophication by seepage of remaining sewage from coastal sediments and groundwater can precisely be determined. Consequently, a precautionary approach to any further tourism development and coherent strategies to improve the currently inadequate wastewater infrastructure seem highly warranted. Remedy to counteract the potential renaissance of booming international tourism may be found in tourism management planning for the Egyptian Gulf of Aqaba coastline developed a decade ago, but not implemented to date (Cesar 2003; SEAM 2004b). The need for implementing these appropriate, already existing management strategies for the sustainable use of coral reef resources in Dahab and elsewhere along the Gulf of Aqaba is strongly underlined by the results of this monitoring exercise.

Notes

Acknowledgments

We want to thank A. Haas, C. Haacke, A. Gabrenya, C. Williamson, K. Korczyk, the student participants of the 2011 and 2013 excursions, C. Alter and L. Wagenknecht for their support on site. We are also grateful to two anonymous reviewers and topic editor A. Elvir for helpful comments. This study was supported by grant Wi 2677/6-1 of the German Research Foundation (DFG) and the Leibniz Association.

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Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Malik S. Naumann
    • 1
  • Vanessa N. Bednarz
    • 1
  • Sebastian C. A. Ferse
    • 1
  • Wolfgang Niggl
    • 1
  • Christian Wild
    • 1
    • 2
  1. 1.Coral Reef Ecology Group (CORE)Leibniz Center for Tropical Marine Ecology (ZMT)BremenGermany
  2. 2.Faculty of Biology and ChemistryUniversity of BremenBremenGermany

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