Received Date: November 07, 2016; Accepted Date: December 14, 2016; Published Date: December 20, 2016
Citation: Siciliano A, Jimenez C, Petrou A (2016) Recreational Diving and Its Effects on the Macroalgal Communities of the Unintentional Artificial Reef Zenobia Shipwreck (Cyprus). J Oceanogr Mar Res 4:151.
Copyright: © 2016 Siciliano A, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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The ecological role of shipwrecks as artificial reefs is well established and often is prime and exclusive destinations for diving tourism. But they are also extremely delicate and sensitive environments. For this reason, the impact of recreational diving on shipwrecks should be taken in consideration since diver’s experience can strongly affect their associated benthic communities. The aim of this study was to verify the impact of anthropogenic activities (scuba divers) on the macroalgal coverage, here considered as indicator of physical disturbance, on the modern shipwreck Zenobia, in Cyprus (east Mediterranean Sea). Divers behaviour was investigated in the wreck and the macroalgal coverage was determined (photo-quadrat method) in three areas differently exposed to physical contact of divers. Our results suggest that diving is having a significant negative effect on the macroalgae coverage of the shipwreck, especially in areas subject to high levels of use (e.g., meeting stations) when compared to control sites in the same wreck. Divers’ behaviour and popular dive routes at the wreck are factors associated to the observed decrease in macroalgae benthic cover. It is important that relevant stakeholders utilizing the Zenobia wreck agree on basic management planning in order to protect and enhance the wreck’s biodiversity. In addition, this study provides for the first time evidence of ecological deterioration of one of the most emblematic shipwreck of the Mediterranean Sea.
Artificial reefs are defined as submerged structures accidentally or deliberately sunk in aquatic environments , mimicking some features typical of natural reefs  and built with concrete blocks [3,4], tires, oil platforms , submarines, planes and vessels (e.g., shipwrecks) . Common uses of artificial reefs are well documented [7-10] and are summarized in Table 1.
|Research: recruitment studies, habitat variability, species interactions||Rio de Janeiro, Brazil||Concrete modules|||
|Rio de Janeiro, Brazil||Concrete modules|||
|Pernambuco, Brazil||Rubber and concrete modules|||
|Israel||Ceramic and brick fired tiles|||
|Sydney, Australia||Sandstone and concrete blocks|||
|Sydney, Australia||Sandstone blocks|||
|Sydney, Australia||Sandstone blocks|||
|Adriatic Sea, Italy||Concrete blocks|||
|British Columbia, Canada||Floating structures|||
|Sydney, Australia||Sandstone blocks|||
|Recruitment facilitation||Gulf of Mexico||Offshore platform|||
|New York Bight||Concrete|||
|St. Thomas, U.S. Virgin Islands||Concrete blocks|||
|Rio de Janeiro, Brazil||Rubber and concrete modules|||
|Rio de Janeiro, Brazil||Concrete, metal and rubber block|||
|Rio de Janeiro, Brazil||Concrete blocks|||
|Rio de Janeiro, Brazil||Concrete blocks|||
|Adriatic Sea, Italy||Concrete blocks|||
|Sicily, Italy||Concrete blocks|||
|Gulf St. Vincent, South Australia||Tyres|||
|Louisiana||Oil and gas platforms|||
|Provision of sheltering, additional substrates, nursery areas, resources||Delaware Bay, New Jersey||Concrete modules||[120,121]|
|Pernambuco State, Brazil||Shipwreck|||
|Tourism and recreational opportunity||South Carolina|||
|Colonization||Italy||Pulverized fuel ash (PFA)|||
|Tioman Island, Malaysia||Concrete blocks|||
|United Kingdom||Pulverized fuel ash (PFA)|||
Table 1: Summary of the most common uses of artificial reefs worldwide.
Shipwrecks represent a particular type of artificial reefs, not only for their ecological role but also for their value for the scuba diving industry. A particularly important scenario is represented by a shipwrecks located on a soft bottom habitat since its ecological role is further enhanced due to the diversification of the environment thanks to the introduction of hard and heterogeneous substrate in the soft-bottom habitat [11,12] representing an ‘oasis’ for biodiversity and abundance of local communities . Furthermore, numerous shipwrecks represent definitely unique, spectacular and breath-taking diving experiences [14,15] and their recreational value has massively increased in the last 30 years [16-18] in coincidence with the development of diving activities and related safety precautions [14,19-21].
Due to their popularity for recreational activities and the consequent high frequentation, shipwrecks are ecologically sensitive sites  and the potentially negative impact of these activities on shipwrecks and the associated biota are well documented [22,23], especially for epibenthic or fouling organisms, which are the most exposed and consequently affected by divers . For the purpose of this study, we consider “disturbance” as an unbalanced event that affect natural communities destabilizing their equilibrium and providing additional source of spatial and temporal heterogeneity compared to the undisturbed condition [25,26].
Divers’ impact can be summarized into two main categories: Direct and indirect. Mechanical damage due to the direct contact of part of the divers’ body (e.g., hands, knees) or gear (tanks, fins, regulators) with the bottom is very common [27-34]. This type of damage is generally caused by inexperience and/or poor buoyancy control [14,35] and the advent of underwater photography seems to contribute with an additional source of damage when divers try to remain still for taking pictures laying down to the sea bottom  (pers. obs.) or grabbing and anchoring themselves to irregularities that are usually biogenic substrates.
The indirect effect of diving, otherwise, is mainly due to air bubbles but consequences have usually been related to the shipwreck’s structure [22,37-41] and there are only a few studies about the potential consequences of air bubbles on benthic assemblages . Depending on the substrate and type of epibenthic organisms, the disturbance of a single diver can virtually be negligible but the impact on epibenthic assemblages is definitely ecologically more significant when a high number of divers are concentrated in a small area [24,43-45]. This is usually known as ‘cumulative effect’ .
Note that the distinction in “direct” and “indirect” effect is strictly dependent on the level at which the problem is analysed. In fact, considering the problem from a wider and general point of view (e.g., recreational diving worldwide) and according with general models of biodiversity conservation [26,46], the direct and indirect effects previously considered can now be joined into a new “direct” threat concept (the general negative effects of divers) while the “indirect” threat (defined as “underlying factors, drivers or root cases” [26,46]) can be represented by management [46,47]. Based on these new definitions, direct and indirect threats are no longer two different sources of damage at small scale but a consecutive series of related steps in conservation planning (indirect effect-direct effect-impact) .
Overall, anthropogenic disturbance can negatively affect distribution, abundance and taxonomic richness of one or more benthic species, remarking differences between areas exposed and not exposed to a particular disturbance source . In addition, there is evidence of the suitability of benthic communities or species as indicators of human impacts [34,50,51] and, in particular, composition and abundance of benthic macroalgae can be considered as indicators of physical disturbance [24,52].
The purpose of this study is: (i) Describing the average behaviour of divers on the wreck, (ii) Verifying the presence of a potential impact due to recreational diving on the macroalgae coverage of the Zenobia shipwreck, and (iii) Quantifying the effect of the impact using the macroalgal coverage as indicator of stress. The photo-quadrat method was applied on three different sites of the shipwreck subject to different physical anthropogenic disturbance and their macroalgal coverage was compared.
The Zenobia shipwreck is a large steel ferry (172 m max length) located 800 m off Larnaca harbour (34°53’50.441’’N, 33°39’28.26’’E), in the oligotrophic south-eastern coast of Cyprus, on a muddy-sandy bottom environment; it sunk in 1980 and lies on its port side at -42 m (Figure 1). Recreational diving on the Zenobia occurs without interruptions throughout the year and reaches its peak between June and October, with about two hundred dives per day, mostly repetitive (Larnaca Sea-Cruises, pers. comm.). By some estimates, the yearly visitation to Zenobia is 35-45,000 divers per year . Zenobia hosts well-developed fouling assemblages with a high benthic coverage of sponges, scleractinian corals, bryozoans that contribute to the high biodiversity associated with the wreck . The survey was carried out between mid-August and mid-October 2011, along the starboard side of the shipwreck (Figure 1), which is the most exposed and almost parallel to the sea surface limiting any environmental differences in factors (such as exposure to sunlight, currents and temperature) between -17/-20 m.
Observations on the divers’ behaviour were primarily carried out on the boat, interviewing dive leaders (operators) about planned routes, depths and dive time, and on divers-customers, about their level of experience and the most attractive areas of the shipwreck. Secondarily, groups of divers were followed along the planned and most common routes, recording the areas visited and the related divers’ activities. Excluded from this study were the routes normally used to penetrate the shipwreck; however, the entry and exit points were recorded.
Preliminary tests for macroalgal cover
Prior to the sampling, the minimum area, defined as the minimum area able to contain a representative number of species of the population , was determined creating a species/area curve [55,56]. We started counting the number of species using an initial 25 cm × 25 cm plot, then doubling the sampling area up to 1 m × 1 m. Results from this method drove us to choose an area of 50 cm × 50 cm as sampling unit, being a good compromise between information obtained and sampling effort.
Sampling areas for macroalgal cover
Preliminary observations based on the route typically undertaken by divers and their behaviour, lead us to choose three areas of interest: A control area, located along the stern (R), and two impacted areas (A and B), respectively at the top middle part and the upper part of the bow (Figure 1).
Sampling procedure and data analysis
A digital camera Canon PowerShot G12 with underwater housing was mounted on a 20 mm PVC pipe framework (40 cm height) with a 25 cm × 25 cm quadrat mounted at the bottom and a plexiglass plate on the top ensured that pictures were taken perpendicular and at constant distance from the bottom. The choice of using a 25 cm × 25 cm frame, instead than 50 cm × 50 cm, was due to the manoeuvrability of a small framework compared to a larger one and the shorter distance between the lens and the substrate allowing higher resolution pictures. Then for each 50 cm × 50 cm plot, which represents our sampling area, we sub-sampled four 25 cm × 25 cm sub-plots. In each area a 15 m transect was haphazardly placed and pictures were taken continuously along the transect and replicated three times using the photo-quadrat method [24,50,57-59]. A total of 1080 photos were produced for the analysis. Using image post-processing software (e.g., Adobe Photoshop), pictures were cropped to the internal frame border, colours were adjusted, brightness and contrast were increased as well as colour saturation. Coral Point Count with Excel extensions  was used to analyse the macroalgal cover by replacing build-in codes according to our needs. The macroalgal coverage was estimated using 100 points randomly overlaid over each picture, according with literature , for a total of 400 random points for each sampling unit. At each point the presence/ absence of macroalgae was assigned, and points positioned above any other substrate were discarded. The final macroalgal coverage for each sampling unit was the average of its four sub-plots.
Data were square-root transformed and ANOVA test was performed to compare the macroalgal coverage among the three areas, followed by a Tukey’s pairwise post-hoc test, using the statistical package PAST v3.12 . Since it was not possible to identify small-sized algal species due to image resolution, presence of suspended material (e.g. mucilage) and organic matter deposited on the macroalgae, we focused the study on three species (Sargassum sp., Peyssonnelia sp., and Padina pavonica) for which we calculate the specific coverage. These species were chosen because large enough to be easily identified in the pictures compared with other species and widely distributed.
Several types of diver behaviour were observed and linked to the different level of interest for the different areas of the shipwreck and in conjunction with the dynamic of the dive. The top middle part of the shipwreck represented the starting point of the majority of dives. Mooring ropes for diving boats are directly attached to the shipwreck’s handrails here, making it a good spot for starting the dive following the ropes for a correct and oriented drop off. At the bottom, divers usually stationed in the area awaiting the arrival of the rest of the group and/ or for general pre-dive checks. In both cases, divers usually wait lying down or kneeling on the bottom rather than maintaining a correct buoyancy control 1-2 m apart the shipwreck surface. In addition, in this area fish-feeding by divers is a common activity; divers gather from different groups into a larger group (10-15 divers simultaneously). The process is repeated several times during a period of about three hours until the first charter vessels depart the site of the wreck. In this area of the wreck the erosion of the macroalgal coverage is evident.
The upper part of the bow represented another critical area as it coincides, for the majority of divers, with the halfway through the first dive. Depending on the divers’ experience level, a typical dive at the Zenobia comprise two immersions, a deeper one and a shallower one. Divers diving deeper during the first immersion usually performed a deep stop at -17/-19 m in this area, performing customary communication and checks within the group and before heading back to the decompression station following the starboard side of the shipwreck. The behaviour of divers along the stern side of the shipwreck differed since it is less interesting and attractive than other parts of the shipwreck. The stern side has less structural complexity and it is usually visited at the end of the second dive, when divers have to perform decompression stops or are low on air, limiting their contact with the bottom and starting the ascent to the surface.
The bow, upper decks, life boats, stackers, car deck, ramps and propellers are all areas highly visited and show signs of deterioration. Graffiti is unfortunately common as well as collection of organisms and objects from the wrecks’ structure. The left side of the deck, coinciding with the deeper part of the wreck, represents the salient and most “fascinating” part of the dives. Here at -40 m depth, divers are advised to stay at a safe distance from wires, pipes and other sharp or pointed-edge structures as well as the trucks stacked at the bottom for obvious security reasons.
Results from the survey revealed a highly significant difference among the macroalgal coverage in the three sampled areas (ANOVA, p<0.001). The R transect (control area) reported the highest percentage coverage (86.1 ± 11.7) while the A and B transects (impacted areas) reported respectively a coverage of 28.4 ± 29.1 and 27.2 ± 10.1, respectively (Figure 2). Percentage of cover in transects A and B was similar (Tukey’s pairwise comparison, p<0.001).
Figure 2: Comparison of macroalgal coverage representative quadrats from the control (R) and impacted areas (A, B) and corresponding bar chart (mean + SE). Letters in the bar chart indicate significant differences (Tukey’s pair-wise comparison). Figure 1 shows the location of transects on the shipwreck.
The most common species was Sargassum sp. with an average coverage of 52% in the control transects, compared with P. pavonica (4%) and Peyssonnelia sp. (3.7%). In the impacted areas their specific coverage falls to less than 5% on average for all three species. While Sargassum sp. is absent in transect A, it showed a coverage of 3% in transect B; the species P. pavonica reported lower values (0.08% and 0.11% for transects A and B, respectively) as well as Peyssonnelia sp. (1% and 1.25% for transects A and B, respectively).
The shipwreck Zenobia attracts every year several thousands of divers from the entire world and probably brings about €14 million a year  in revenue to Cyprus, thanks to the easy access and its suitability for divers with different levels of experience. For this reason, it represents a particularly vulnerable site and its associated communities of organisms are susceptible of being affected by recreational diving.
Although scuba diving is considered to be an environmental friendly form of ecotourism, several studies demonstrated the negative impact of divers on marine ecosystems  damaging organisms and/ or habitats regardless of whether they are accidental or deliberate actions, direct or indirect [31,36,64-69]. The damage level has often been linked to the intensity of use [44,70,71] and the level of divers’ experience [72-74].
The majority of damages are usually caused by mechanical breakage [31,33,74,75] and sediments re-suspension [33,70,76]. The most prevalent type of contacts are fin kicks [65,68,75] and it has been noted that divers wearing gloves made contact with the substrate more often than divers with naked hands [65,73,77].
There is evidence that even snorkelers are known to cause effects on the marine environment [33,44,45,70] but the effects are easier to be controlled, for example using informative trails . Supporting this conclusion , remarked that only few snorkelers practice freediving while divers can easily disturb the environment since they can stay closer to the bottom and much longer [28,31,33,35,44,67,68,78].
In the Mediterranean Sea, the negative effect of scuba diving on sub tidal communities has been studied on coralligenous communities , where highly frequented sites showed lower density and smaller size of bryozoans colonies , in marine protected areas, where several key-species are potentially threatened by recreational activities [79- 81], and on submerged marine caves [80,82], where physical contacts and sediment resuspension are the main reason of sessile organisms’ decline [79,82].
Due to the unique experience that shipwrecks are able to offer [14,15], they can be victims of their fame and suffer uncontrolled diving pressure. According to Kirkbride-Smith et al. , among the different type of artificial reefs, shipwrecks and sunken vessels are preferred compared to other artificial shapes, such as tyres, concrete modules, break walls, piers, and platforms. Nevertheless, they remark the strong difference in the preference of diving sites between new and experienced divers: while the first ones prefer to dive on artificial reefs than natural substrates, experienced divers prefer to dive on natural reefs [83,84]. According to Kirkbride-Stolk et al.  and Jakši? et al. , the issue related to negative effect of recreational activities does not concern the tourism itself but tourists’ responsibility and awareness which are at the basis of long-term effects and consequences.
Our results suggest that diving is having a significant impact on the macroalgae coverage of the shipwreck, especially in areas subject to high levels of use, and those differences in coverage and biological composition may be used as an important and significant indicator of health status.
Macroalgal coverage was significantly lower in highly visited (impacted) areas, as in the middle area of the shipwreck, where the consequences of the effects of recreational diving are visible to the naked eye: the coverage in some cases was thin to the point of showing the bare wreck’s hull, and it gradually becomes higher moving away from the mooring points, and relates to divers starting to dive with a correct buoyancy.
Several studies state that level of experience is directly linked to the potential damage caused to subtidal communities, attributed mainly to novice divers coming into contact with the bottom more often than the experienced ones [70,73,74,87,88] (pers. obs.) and in some cases it can play a more relevant role than the actual number of divers visiting a site [66,70,87].
From a wide point of view, the majority of conservation actions aimed to protecting biodiversity can be grouped in four categories:
Direct protection and management, law and policy, education and awareness, and changing incentives . In the last two decades, several ways have been introduced to handle damages due to recreational diving on artificial reefs, such as shipwrecks, aimed to preserve the structure itself and the related biodiversity. All these measures are fundamentally aimed to reducing the effects of divers, then focused directly or indirectly on the actions of divers (changing behaviour vs management strategies) . They mainly consist in two different kinds of initiatives:
Directed towards changing the behaviour of divers  through: (i) A better environmental education , (ii) Promoting environmentally friendly behaviour by diving tourism operators, (iii) Briefing divers about the vulnerability of organisms attributable to visiting divers, (iv) Encouraging underwater photographers to be more aware of their actions when taking photographs , (v) Underwater supervision ;
Using management strategies such as: (i) Introducing charges/ transferable permits to reduce the number of dives and/or divers on sensitive sites [22,89,90], (ii) Resting some sites from all diving activity  or increasing the number of sites in order to avoid overcrowding of hot-spots , (iii) Using specific shipwrecks protection and management approaches (i.e., Commonwealth Historic Shipwrecks Act 1976, in Australia), (iv) Adoption of specific regulations for photographers , (v) Establishing specific trails for snorkelers and divers , (vi) Installing permanent and environmental friendly mooring .
According with the IUCN-CMP classification of direct threat to biodiversity , both direct and indirect effects above-mentioned fall within the area of “human intrusion and disturbance” (1st level of classification) and “recreational activities” (2nd level). This classification represents an efficient, unique and standardized way to classify potential damages and conservation measures related to any generic problem threating biodiversity worldwide, allowing an easy way to share information, experiences, successful solutions, but also improving the efficiency of conservation efforts through cross-project learning .
It has been demonstrated that exhaustive pre-dive briefings and underwater interventions are two of the best and easiest ways to reduce coral damage [65,92-95] reducing the number of contacts by 20-80% [70,93]. Similarly, Di Franco et al.  propose to start the dives in low vulnerability habitats to give divers enough time to make their comfortable and managing with their buoyancy control. Supporting this approach, it has recently been demonstrated that physical contacts are more likely during the first 10 min of dives .
It is interest of most of the stakeholders utilizing the Zenobia, one of the most emblematic shipwrecks in the Mediterranean Sea, adopting similar approaches. The conservation of the associated biodiversity as well as the wreck itself have to consider the management of the diving activities; this practice eventually has to be implemented to all sites subject to high diving tourism in Cyprus and elsewhere, in order to preserve the ecological heritage that makes them very attractive sites .
This project was economically and technically supported by AP Marine Environmental Consultancy Ltd., Larnaca Sea-Cruises, Mr Nick Galea (ENALIA Research Program), and Mr and Mrs Siciliano. Thanks are also due to Antonino Milana, for field assistance, Julia Hartingerova for the sketch of the Zenobia shipwreck, and all AP Marine team in Cyprus (Kyproula Chrysanthou, Maria Patsalidou, Louis Hadjioannou and Kalia Aristidou).