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Environmental Management (2016) 57:637–648 DOI 10.1007/s00267-015-0628-4

Recreational Diver Behavior and Contacts with Benthic Organisms in the Abrolhos National Marine Park, Brazil

1,2 3 4 Vinicius J. Giglio • Osmar J. Luiz • Alexandre Schiavetti

Received: 23 April 2015 / Accepted: 17 November 2015 / Published online: 27 November 2015 Ó Springer Science+Business Media New York 2015

Abstract In the last two decades, coral reefs have the provision of pre-dive briefing including ecological become popular among recreational divers, especially aspects of corals and beginning dives over sand bottoms or inside marine protected areas. However, the impact caused places with low coral abundance. Gathering data on diver by divers on benthic organisms may be contributing to the behavior provides managers with information that can be degradation of coral reefs. We analyzed the behavior of used for tourism management. 142 scuba divers in the Abrolhos National Marine Park, Brazil. We tested the effect of diver profile, reef type, use Keywords Dive tourism Á Marine protected area Á of additional equipment, timing, and group size on diver Management Á Scuba divers Á South Atlantic Á Tourism behavior and their contacts with benthic organisms. Eighty- management eight percent of divers contacted benthic organism at least once, with an average of eight touches and one damage per dive. No significant differences in contacts were verified Introduction among gender, group size, or experience level. Artificial reef received a higher rate of contact than pinnacle and Coral reefs are important habitats along tropical coastlines, fringe reefs. Specialist photographers and sidemount users providing humans with economic resources and services had the highest rates, while non-users of additional through cultural values, fishing, coastal protection, and equipment and mini camera users had the lowest contact tourism (Moberg and Folk 1999). This ecosystem is also a rates. The majority of contacts were incidental and the popular destination for scuba diving, one of the world’s highest rates occurred in the beginning of a dive. Our fastest growing recreational sports (Van Treeck and findings highlight the need of management actions, such as Schuhmacher 1998; Hasler and Ott 2008). Scuba diving is considered to be a low-impact activity and provides an economic alternative to fishing through a non-extractive use of marine wildlife (Davis and Tisdell 1995; Tapsuwan & Vinicius J. Giglio and Asafu-Adjaye 2008). However, coral reefs are globally [email protected] threatened by a wide range of anthropogenic activities, such as fishing, pollution, and unplanned tourism (Bell- 1 ´ Programa de Pos-graduaçaõ em Ecologia e Conservaçaõda wood et al. 2004). These activities act in synergy with the Biodiversidade, Universidade Estadual de Santa Cruz, Ilheús, Brazil high vulnerability of corals to climate change (Hughes et al. 2003), rendering the sustainable use of coral reefs a 2 Present Address: Programa de Po´s-graduaçaõ em Ecologia, Universidade Federal do Rio de Janeiro, Rio De Janeiro, complex task. The recent growth of diving tourism has Brazil raised concern among managers and scientists regarding its 3 Department of Biological Sciences, Macquarie University, impacts. For instance, in Eilat reefs, Israel, visitation rates Sydney 2109, NSW, Australia account for 250,000–300,000 divers and 400,000 instances 4 Departamento de Cieˆncias Agra´rias e Ambientais, of coral damage per year (Zakai and Chadwick-Furman Universidade Estadual de Santa Cruz, Ilheús, Brazil 2002). 123 Author's personal copy

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No-take Marine Protected Areas (MPAs) have recently Dearden et al. (2007) verified that only 30 % of divers were become widely recognized as a key tool for biodiversity aware of negative environmental impacts created by their conservation and fisheries management, especially in coral dive group. In summary, there is not a general pattern of reefs (Jones 2001). The reduction in fishing pressure relationships among diver behavior and rate of contacts on through the closure of selected areas has led to the reap- reefs. Patterns of diver impacts are generally site-specific, pearance of rare or absent species and substantially so further studies and dive site management should be increases the biomass of apex predators (Anderson et al. narrowly focused to be of maximum practical use. 2014; Edgar et al. 2014). There are also positive effects for Understanding diver behavior is important to subsidize the coral reefs, such as increase of coral cover and structural carrying capacity and verify management strategies to complexity (Selig and Bruno 2010). Increases in fish reduce impacts of recreational diving. abundance and coral cover make MPAs highly attractive to Previous studies have demonstrated that underwater the diving industry. Today, scuba diving is one of the most photographers inflicted high rates of damages to corals important commercial uses of MPAs (Green and Donnelly (Rouphael and Inglis 2001; Chung et al. 2013). Photogra- 2003). However, in some cases, large numbers of dives phers stay close to the substrate and may accidentally come have resulted in decline in the health of coral reefs (Davis into direct contact with the reef or deliberately hold on the and Tisdell 1995; Uyarra and Coˆte´ 2007). corals to stabilize themselves to photograph a subject. Divers can damage corals through direct (physical Rouphael and Inglis (2001) evaluate the behavior of spe- contact) or indirect contact (via sediment deposition) with cialist and non-specialist photographers and verified that their hands, body, scuba gear, and fin kicks (Harriot et al. specialists caused higher rates of damage than non-spe- 1997; Rouphael and Inglis 1997). Due to the delicate cialists. However, since then, several models of easy-to-use structure of corals, contacts often result in breakage, underwater cameras have recently been developed and the abrasion, or tissue removal (Hawkins et al. 1999). Dam- effect on diver behavior of these snapshot cameras has not aged corals are more susceptible to predation, competition yet been evaluated, as well as the use of new diving gear interference, and disease, which can result in death of the configurations. colony (Guzner et al. 2010). Algal colonization on corals To mitigate diving impacts, studies have proposed the may soon follow tissue damage. Algae compete for space establishment of carrying capacity approaches (Davis and with corals and can act as a sediment trap, hindering coral Tisdell 1995;Rıós-Jara et al. 2013) and the use of pre- recovery (Hall 2001). Fin kicks on the bottom disturb and dive educational briefings (Medio et al. 1997; Camp and re-suspend sediment that can settle nearby, including on Fraser 2012). However, diver’s behavior and compliance corals (Zakai and Chadwick-Furman 2002). When sedi- to the norms vary according to diver’s profile, objectives, ment covers the coral surface in excess, coral recruitment, and characteristics of the dive site (Smith et al. 2010; feeding, and photosynthesis are inhibited (Hasler and Ott Giglio et al. 2015). For example, the use of pre-dive 2008). briefings reduced 60 % of diver’s contacts with corals in Since the 1990s, studies have investigated the dynamics Egypt (Medio et al. 1997). On the other hand, in Santa of diver and benthic organisms contacts (e.g., Hawkins and Lucia (Lesser Antilles, Caribbean), group leader inter- Roberts 1992; Hawkins et al. 1999; Plathong et al. 2000; vention was the only effective method to reduce coral Barker and Roberts 2004; Lucrezi et al. 2013). The char- damage (Barker and Roberts 2004). The use of artificial acteristics that affected the rates of diver contacts on reefs reefs has been proposed as a strategy to reduce impacts on were related to diver’s profile, such as their experience (Di natural reefs (Polak and Shashar 2012). Shipwrecks are Franco et al. 2009), gender (Rouphael and Inglis 2001), often used as a diving attraction, mainly due to their dive purpose (Uyarra and Coˆte´ 2007), use of additional esthetic appeal (Leeworthy et al. 2006). These structures equipment (e.g., cameras, gloves and lanterns; Rouphael generate revenue through diving tourism and consequently and Inglis 2001; Uyarra and Coˆte´ 2007; Poonian et al. assist in local economic development (Pendleton 2005). 2010), and biophysical characteristics of dive site (e.g., reef Historical shipwrecks represent an important cultural type and coral cover; Rouphael and Inglis 1997; Hawkins heritage and are fragile, non-renewable resources, gener- et al. 1999). Sites with complex topographies can make it ally protected by law (Jewell 2004). However, the impact difficult for divers avoid touching corals on vertical caused by scuba divers on its benthic fauna incrusted structures (Rouphael and Inglis 1995). However, the cor- remains little understood. To implement and adequate relation between coral damage and reef topography is artificial reef program, it is essential to understand diver unclear (Zakai and Chadwick-Furman 2002). The lack of impacts on historical structures and its fauna, and awareness by divers of their own impacts on reefs has assessing potential impacts of artificial structures on contributed to a substantial amount of human-induced marine biota, such as phase shifts of benthic assemblages damage on corals (Rouphael and Inglis 1995). In Thailand, (Work et al. 2008). 123 Author's personal copy

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Despite the increasing interest in coral reef conserva- Divers were unaware that they were being observed to tion, assessments of recreational dive damage have not yet avoid influencing their behavior. Observers blended in the been carried out on benthic organisms (e.g., scleractinian dive party and remained inconspicuously behind their corals, fire corals, gorgonians, and sponges), and how subjects, within visual contact (usually 2–4 m away). Each divers contributes to these impacts in Brazil. In this study, sample period began when divers approached the reef and we examined scuba diver behavior through direct obser- ended when they return to the boat, moving away from the vations in order to identify factors that may influence their reef. We quantified four types of dive contacts, according contacts with benthic organisms in the Abrolhos National to the part of the diver body or gear with which they tou- Marine Park (ANMP), a no-take MPA in eastern Brazil. ched, damaged, or raising sediment onto benthic organ- The ANMP is part of the largest and most biodiverse coral isms: fin, knee, hand, and scuba gear (e.g., spare regulator reef complex in the South Atlantic (Leaõ et al. 2003) and is and air tank). Diver contacts were recorded on a PVC slate considered one of the best diving destinations in Brazil. We and classified as touch, damage (when physical damage verified the rate of scuba divers’ contacts with benthic occurs), or raising sediment onto corals. Timing was organisms according to (1) divers’ profile (gender, age, and grouped into categories (e.g., 0–10, 11–20, 21–30, and experience); (2) reef type; (3) use of additional equipment [30 min). We recorded the number of divers in the group (e.g., camera and sidemount); (4) divers’ group size; and and the number of interventions made by the dive leader (5) dive time. We also estimated the rate of contacts under when divers contacted benthic organisms or raised sedi- current visitation rates and suggested management mea- ment onto corals. Corals were categorized to one of three sures to reduce coral reef damage in the ANMP. categories: (a) branching (e.g., fire coral Millepora alci- cornis), (b) massive (e.g., Mussismilia braziliensis, M. hispida, M. harttii, and Favia leptophylla), and (c) gor- Materials and Methods gonians (e.g., Phyllogorgia dilatata). Contacts with other organisms (e.g., invertebrates) were also recorded. Diver Study Area behavior was classified as intentional or unintentional. An intentional contact is one the divers were clearly aware of. Comprising an area of 965.67 km2, the ANMP was created For instance, divers putting their hands on the coral to get in 1983 aiming to conserve biodiversity and to promote closer to an organism near the substrate. sustainable tourism, educational, and research activities. Eighteen coral species occur in ANMP and of these, eight Diver Profile are endemic to South Atlantic, and one endemic to eastern Brazil (Leaõ and Kikuchi 2001). In the 1990s, unofficial Age, gender, certification level, and experience were estimates suggested that ANMP received approximately recorded through registration forms required by the dive 10,000 visitors per year. However, annual visitation has operator or by an interview at the end of the visit. We decreased by one-third when compared with 2002 estimate require to divers an oral authorization to include their data (Alvarenga and Fleck 2011). At the time of writing, ANMP in the survey. The experience (number of dives completed received an average of 3500 visitors per year, peaking in a lifetime) was grouped into four categories: (a) 1–25 during the austral summer, due to good dive conditions and dives; (b) 26–50 dives; (c) 51–100 dives; or (d)[100 dives. higher underwater visibility. Certification was categorized as one of the follow cate- Fishing or collection of organisms is forbidden within gories: (a) open water; (b) advanced open water; (c) rescue the ANMP, as well as the use of gloves and knives. The diver; or (d) dive master or instructor. first dive in each tourism operation is restricted to shallow reefs (\10 m depth), focusing equipment and buoyancy Reef Types control adjustments. Group leaders take a maximum of eight divers in a group. The behavior of divers was quantified at six dive sites, each categorized as one of the following three reef types: Diver Behavior (a) three shallow fringing reefs; Mato Verde, Portinho Sul, and Lıńgua da Siriba sites, maximum depth of 7 m; (b) two The underwater behavior of scuba divers was assessed pinnacle reefs: Faca Cega and Chapeiraõ da Sueste sites, through direct observation. Observers sampled two divers maximum depth of 20 m; and (c) one artificial reef; the at a time. Three distinct dive operators were sampled over Rosalinda shipwreck, a 102 m length steel freighter 7 weeks during the austral summers (January to March) of wrecked in 1955 in good conservation status, maximum 2012 and 2013. We sampled all divers on 20 liveaboards depth of 20 m. We do not verify reef complexity; however, trips that performed generally eight dives along 3 days. there are obvious differences in the topography of the three 123 Author's personal copy

640 Environmental Management (2016) 57:637–648 reef types surveyed. For instance, pinnacle is predomi- Table 1 Summary of diver profile nantly a ‘‘wall reef’’ and shipwreck is a ‘‘tridimensional’’ Fringe Pinnacle Artificial reef Total reef. The differences in topography can be an influential variable in diver behavior and contacts with the reefs Gender (%) because the reef angle with respect to the diver can vary Male 26.8 16.1 16.2 59.1 (Rouphael and Inglis 1997). Female 14.1 18.3 8.5 40.9 Experience (%) Use of Additional Equipment 1–25 dives 11.8 7.9 7.2 27 26–50 dives 15.1 9.9 2.6 27.6 We assigned divers to one of five categories based on the 51–100 dives 9.2 7.9 5.3 22.4 type of equipment they used, in addition to the regular [100 dives 7.2 7.9 7.9 23 scuba set: (1) mini camera user (divers using small action Age (%) Certification level cameras, e.g., GoPro); (2) non-specialist photographer (divers using compact digital cameras); (3) specialist 10–20 6.8 Open water 63 photographer (divers using professional cameras with 21–30 23 Advanced open water 37 external flash greater bulk than compact cameras); (4) 31–40 31.8 Rescue diver 19 sidemount users (divers using a gear configuration in which 41–50 20.3 Dive master 9 two cylinders are mounted alongside the diver, below the [50 18.2 Instructor 14 shoulders and along the hips, instead of on the back of the diver); and (5) non-additional equipment users.

Data Analysis certifications. Diver experience ranged between 2 and 700 dives. The modal diver experience category was 26 to 50 Poisson regression and Kruskal–Wallis test were used to dives, followed by 1 to 25 dives (27.6 and 27 %, respec- verify relationships between diver profile, dive site char- tively; see Table 1). Fifty-eight percent (N = 83) of divers acteristics, and contact rates. A multivariate analysis of used additional equipment. Of these, 28.9 % were mini variance was used to explore relationships between both camera users, 32.5 % non-specialist photographers, 20.5 % the rates of touches and breakages on benthic organisms were specialist photographers, and 18.1 % were sidemount per minute, using seven independent variables: (A) certifi- users. The experience of mini camera users varied between cation; (B) diver’s experience; (C) gender; (D) type of reef; 10 and 550 dives, with an average of 138 ± 18.5 (±SE), of (E) use of additional equipment; (F) group size: 2–4 divers; non-specialist photographers varied between 6 and 1200 5–6 divers, and 7–9 divers; and (G) dive timing 0–10, dives (average = 113 ± 23), of specialist photographers 11–20, 21–30, and [ 30 min. To find the best set of varied between 10 and 550 dives (average = 141 ± 17.1), explanatory variables, we used the model selection proce- and of sidemount users varied between 10 and 500 dives dure of stepwise backward elimination of non-significant (average = 156 ± 19.2). factors. The selection started with a model with all vari- Most divers (88 %, N = 126) contacted benthic organ- ables, and then dropped one variable at a time to test if the isms at least once during each dive. Of these, 46 % of variable deletion improved the model. We repeated this divers touched, 37 % damaged, and 17 % raised sediment process until no further improvement was possible (Zuur onto benthic organisms. The overall average of contacts per et al. 2007). All tests were performed at a significance level minute was 0.26 (SD = 0.25), and considering that a single of P \ 0.05. Statistical analyses were performed using R dive lasted on average 39 min, each diver contacted ben- 2.15.0 software (R Development Core Team 2012). thic organisms 10.4 times per dive, represented by 8.19 touches, 1.04 damages, and 1.17 raising sediment. Additional equipment users accounted for 54 % of all Results contacts. Overall, a minority of divers accounted for the highest contact rates (Fig. 1). Ninety-two percent of all Diver Profile and Contacts with Benthic Organisms contacts (N = 1324) were unintentional. Most of contacts occurred during the first 20 min of dive (69 %, N = 67). We observed 142 divers (57 on fringe reefs, 50 on pinna- Divers contacted benthic organisms with their fins (79 % of cles reefs, and 35 on the artificial reef). The total obser- total, 7.5 ± 0.6 contacts per dive); hands (11 %, vation time was 87 h and 16 min. The majority of divers 1.06 ± 0.09), scuba gear (6.5 %, 0.55 ± 0.04 contacts per were male (59 %; Table 1). Seventy percent of divers dive); and knees (3.6 %, 0.36 ± 0.04 contacts per dive). possessed open water or advanced open water diving Intentional contacts were caused mainly with hands (85 %, 123 Author's personal copy

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Fig. 1 Frequency of diver contact rate with benthic organisms (N = 142)

N = 94). Table 2 details the number of contacts and how minute on fringe reefs (Poisson regression I =-1.57, they occurred. Massive corals were the most touched, and P = 0.7), pinnacle reefs (I =-1.51, P = 0.9), and on the branching corals the most damaged (74 and 59 %, artificial reef (I =-0.86, P = 0.6; Fig. 2). However, in respectively). Both were contacted mainly by fin kicks. All the artificial reef, the rate of contacts tended to increase events of raising sediments were caused by fin kicks, with greater experience. For all reef types, specialist mainly in massive corals (79 %). Sixty-six percent of photographers and sidemount users obtained significantly damages occurred in branching corals and 21 % in massive more contact rates than mini camera users and non- corals. Dive leader intervention was observed in only 2 % specialist photographers (Kruskal–Wallis test P \ 0.01) (N = 29) of contacts. and non-additional equipment users (P \ 0.001; Fig. 3a). Mini camera users caused the lowest contact rates, Effects of Reef Type, Additional Equipment Use, (0.15 min-1 ± 0.02), even lower than non-additional Timing, and Group Size on Diver Behavior equipment users (0.18 min-1 ± 0.02). Specialist photographers and sidemount users caused highest contact rates The highest rates of diver contacts with benthic organisms (0.38 min-1 ± 0.06 and 0.50 min-1 ± 0.07). A similar were observed on the artificial reef, followed by pinnacle pattern was verified when contact type was analyzed reefs (Table 3). Artificial reefs had the shorter dive time according to additional equipment. For instance, specialist average (* 4 min) than dives on the natural reefs, but photographers and sidemount users caused the highest rates received the highest rates of touch, damage, and raising of touch and damage over all reef types. sediment events per dive. No significant relationship was Multiple analysis of variance revealed that reef type, use verified between diver experience and contact rates per of additional equipment, and dive timing were important

Table 2 Diver contact rate Branching coral Massive coral Gorgonians Other organisms with benthic organisms in the Abrolhos National Marine Park N Per dive N Per dive N Per dive N Per dive

Touch Fin 164 1.15 720 5.07 23 0.16 77 0.54 Hand 17 0.12 108 0.76 3 0.02 14 0.10 Knee 1 0.01 44 0.31 0 0 4 0.03 Scuba gear 4 0.03 53 0.37 3 0.02 3 0.02 Total 186 1.31 925 6.51 29 0.20 98 0.69 Damage Fin 88 0.62 16 0.11 1 0.01 8 0.06 Hand 86 0.04 0 0 0 0 2 0.01 Knee 1 0.01 0 0 0 0 0 0 Scuba gear 2 0.01 9 0.06 0 0 4 0.03 Total 97 0.68 25 0.18 1 0.01 14 0.10

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Table 3 Diver contact rate with benthic organisms according to reef types Frequency (per minute) Average number of contacts over a dive Fringe Pinnacle Artiﬁcial reef Fringe (average dive Pinnacle (average dive Artiﬁcial reef (average (mean ± SE) (mean ± SE) (mean ± SE) time of 41 min) time of 39 min) dive time of 37 min)

Touch 0.13 ± 0.013 0.17 ± 0.02 0.33 ± 0.04 5.33 6.63 12.21 Damage 0.01 ± 0.003 0.02 ± 0.004 0.05 ± 0.009 0.41 0.78 1.85 Raising 0.03 ± 0.006 0.02 ± 0.006 0.05 ± 0.02 1.23 0.78 1.48 sediment

(X2 = 24.5, df = 3, P \ 0.05), pinnacle (X2 = 56.8, P \ 0.05), and the artificial reef (X2 = 14.4, P \ 0.05). Divers in the first 10 min caused more than four times as many contacts as fringe and pinnacle reef types, and more than twice compared with the end stage of the dive (Fig. 3b). Group size did not reveal significant differences to contact rates.

Discussion

In this study of diver contacts on benthic organisms, we found that on an average dive, divers contacted the reef 10.4 times. However, our analysis indicates that variability in contact rates was inﬂuenced mainly by additional equipment use, reef type, and timing. In the sections below we discuss the inﬂuence of each variable on diver contacts with benthic organisms.

Reef Type

The artificial reef obtained twice the rate of diver contacts with benthic organisms than fringe or pinnacle reefs. The Rosalinda shipwreck has a complex structure, with a high abundance of corals along its extension. The high complexity and high abundance of corals in the parts of wreck most visited by divers (e.g., the command deck and vessel Fig. 2 Relationship between diver contacts rates with benthic edges) make these areas susceptible to higher contact organisms and diver experience according reef type rates. Another reason for the high rate of contact in the artificial reef is that dive leaders often deliberately con- factors explaining touch and raising sediments rates tacted corals. This behavior was frequently repeated by (Table 4, ANOVA F = 15.44, P \ 0.001, R2 = 0.188) and visitors, resulting in a higher rate of contacts. It is well damage rates (F = 7.721, P \ 0.001, R2 = 0.097). More known that divers tend to mimic the behavior of their specifically, the combination of factors that predicted the dive leaders (Barker and Roberts 2004). When asked to highest rate of touches and damaged was specialist photog- justify this behavior, dive leaders explained that they were raphers, sidemount users, diving in the artificial reef during not as concerned about corals in the shipwreck, as they the beginning of their dive (Table 4). The diving time perceived the artificial reef as a non-natural environment. between 11 and 20 min was also negatively correlated with The Rosalinda shipwreck is one of the main attractions of touch rate. The significant difference in the end stage of ANMP and diving may continue to occur there with or diving (21 min upward) on diver contacts with benthic without the coral presence. However, after a period organisms was consistent over the three reef types: fringe between 8 and 25 years, artificial reefs, if undisturbed,

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Fig. 3 a Number of dive contact rates of non-users of additional containing 50 % of the figures. The line across the box indicates equipment (white box), users of photographic cameras (light gray the median. The dashes represent the 5th and 95th percentiles and the boxes), and users of sidemount (dark gray box). b Contacts made filled circles are the extreme figures according dive timing. Boxes represent the interquartile range, have demonstrated the same level of biodiversity and Additional Equipment Use productivity as other natural reef ecosystems (Burt et al. 2009; Perkol-Finkel et al. 2006). Frequent diver contact It is not surprising that specialist photographers inflicted on shipwrecks not only cause impact on benthic organ- most of the damage to benthic organisms in this ANMP, isms but may also expose the metal framework of the ship since this diver type has previously been shown to cause to the seawater, accelerating corrosion (Jewell 2004; more damages to benthic organisms elsewhere (Wo- McKinnon 2015). Environmental education training for rachananant et al. 2008; Luna et al. 2009). Specialist dive leaders and other management interventions are photographers are often too distracted with their subjects to needed to conserve the benthic organisms of ANMP. A paying attention to the reef. They also use the reef to steady successful initiative that should be used to inspire similar themselves and get closer to their subjects. The contacts action is the National Oceanic and Atmospheric Admin- they made caused more damage than those made by non- istration’s (NOAA) Blue Star programme in Florida, photographers (Rouphael and Inglis 2001; Barker and which trains and incentivizes dive leaders to include Roberts 2004; Krieger and Chadwick 2012). On the other conservation education into their dive briefing, aiming to hand, mini camera users obtained the lowest contact rates. reduce diver impacts on the reefs (Camp and Fraser Mini cameras have become popular in underwater 2012). Dive shops also benefit from this endeavor, videography due of its small size, low-cost, standardized because its positive results (see Camp and Fraser 2012; housing, and widespread availability. Mini camera’s users Krieger and Chadwick 2012) can be used as marketing usually have a rod with the camera attached at the tip, and tool as the society is becoming more environmentally so the diver does not need to approach the bottom to aware. capture a subject.

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Table 4 Multivariate analysis Unstandardzed coefficients Standardised coefficients of variance results showing factors with significant b SE b tP influence on divers’ contact rates with benthic organisms Touch

(Intercept) 0.252 6.892 <0.001 0.036 Reef type Artificial reef 0.198 0.228 5.424 <0.001 0.036 Pinnacle 0.027 0.035 0.853 0.4 0.032 Additional equipment Mini camera user -0.016 -0.017 -0.409 0.7 0.040 Non-specialist photographer 0.062 0.064 1.554 0.12 0.040 Specialist photographer 0.165 0.146 3.566 <0.001 0.046 Sidemount user 0.274 0.235 5.724 <0.001 0.047 Dive timing 11–20 min -0.107 -0.124 -2.687 0.007 0.039 21–30 min -0.178 -0.207 -4.472 <0.001 0.039 [31 min -0.281 -0.323 -6.949 <0.001 0.040 Damage (Intercept) 0.027 3.620 <0.001 0.007 Reef type Artificial reef 0.030 0.180 4.076 <0.001 0.007 Pinnacle 0.004 0.027 0.626 0.5 0.007 Additional equipment Mini camera user 0.003 0.014 0.330 0.7 0.008 Non-specialist photographer 0.004 0.024 0.557 0.5 0.008 Specialist photographer 0.028 0.129 2.994 0.002 0.009 Sidemount user 0.028 0.123 2.834 0.004 0.009 Dive timing 11–20 min -0.007 -0.041 -0.852 0.4 0.008 21–30 min -0.032 -0.192 -3.921 <0.001 0.008 [31 min -0.049 -0.235 -4.796 <0.001 0.008 The best model for touch and damage used the variables reef, additional equipment, and timing. The table shows the coefficient’s estimates of variables (b), standard error (SE), t statistic (t), and probability (P). Coefficients in bold indicate significance (P \ 0.05). Reference level for this regression was set as ‘fringe’ for reef type, ‘non-user’ for use of additional equipment, and ‘0–10 min’ to dive timing. For the analyses purpose, we added raising sediments rates to the category touches

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Sidemount users also inflict a high rate of damages. This certification and experience may be inefficient. The higher diving configuration, previously restricted primarily to the individual contact rates were influenced mainly by the use technical diving community, is becoming popular among of additional equipment, not experience. recreational divers in Brazil relatively recently and most Group size did not have influence on diver contact rates users may still lack the skills necessary to avoid reef con- with the reef. In a scenario where dive leader intervenes tacts. Clearly, further research is needed to understand the when observe divers touching reefs, we expected that effects of this equipment in divers’ behavior and impacts in smaller groups cause lower contact rates. However, in the marine biota. ANMP, dive leaders intervene or warn divers when they touch organisms only in 2 % of the events. In a previous Dive Timing study, interventions made by dive leaders were successful to reduce diver-coral contacts by as much as 80 % (Barker For all of the reef types analyzed in this study, contact rates and Roberts 2004). However, in dive sites in Florida were higher during the first 10 min of the dive. Previous (Krieger and Chadwick 2012) and in the ANMP, dive studies have verified that the beginning of the dive is con- leaders serve primarily as tour guides and tend to stay at the sidered critical with respect to diver-coral contact rates (Di front of the group, looking ahead. Recreational diving can Franco et al. 2009; Camp and Fraser 2012; Krieger and be more sustainable in the ANMP if dive leaders observe Chadwick 2012). In this stage, divers are performing adjusts divers more closely, and intervening when seeing they are to establish neutral buoyancy and navigation (Di Franco et al. damaging benthic organisms. 2009), and organizing pair formation (VJ Giglio, personal observation). Starting dives over sandy bottom areas or in sites with low coral cover could help mitigate the impacts of Contacts with Benthic Organisms recreational diving. The rate of diver’ contacts with benthic organisms decreased as the time of dive increased, because The high percentage of divers that contacted benthic over time then divers usually established better buoyancy organisms observed in this study (88 %) was consistent control and navigation. with findings at other sites, where most divers made one or more contacts per dive. On Australia’s Great Barrier Reef, Diver Profile and Group Size 70 % of surveyed divers contacted with corals (Rouphael and Inglis 2001). In the Florida,USA, and Bonaire, 75 % of Experienced divers are more familiar with marine envi- divers contacted the reef (Krieger and Chadwick 2012; ronment and have undertaken more extensive training. Uyarra and Coˆte´ 2007). Overall, in ANMP, contact rates This in turn increases their diving skills, such as buoyancy occur at an average of 0.26 min-1, 8.72 touches and 0.9 and swimming control (Ong and Musa 2012;Davisand damages per dive. This result is lower than observed in Tisdell 1995). In this context, we predicted that experi- Florida, US (0.33 contacts min-1 and 17.9 per dive) and enced divers would make fewer contacts with corals. Hong Kong (0.87 contacts min-1 and 14.6 per dive) However, we did not observe a negative relationship (Chung et al. 2013). In Australia, Roberts and Harriot between diver experience and contact rates. A similar (1994) observed an average of 35 contacts and 2.45 dam- finding was reported by Rouphael and Inglis (2001), who ages per dive. The ANMP has a relatively low abundance did not verify such correlation either. This can be of benthic organisms when compared with dive sites sur- explained by inexperienced divers being more fearful of veyed described above that covers between 30 to 70 %. getting close to the bottom during scuba diving activities The benthic organisms cover in ANMP is of approximately andtouchingwhattheyassumetobeharmful.Onthe 10 % for the main coral species, M. braziliensis, 3.5 % for other hand, experienced divers may feel more comfort- Siderastrea sp and 1 % for M. harttii (Francini-Filho et al. able to get close to the substratum and handle organisms. 2013). On the other hand, the lower abundance of benthic However, our results must be interpreted carefully organisms in the ANMP may explain the apparent lower because the relationship between diver experience and rate of diver contacts because they simply have fewer contacts with benthic organisms may vary according to opportunities to contact them. additional equipment type. It was not possible to assess The majority of contacts with benthic organisms in the this parameter because we did not have a wide range of ANMP were through unintentional fin kicks, caused by experiences for all additional equipment and reef types. poor swimming techniques and lack of buoyancy control, Our results highlight a contradiction in the relationship indicating poor diving proficiency. Fin kicks are the main between diver experience and their behavior. Diving cause of scuba diving coral damages (Medio et al. 1997; management strategies with constraints based only on Rouphael and Inglis 1995, 1997; Luna et al. 2009; Chung

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646 Environmental Management (2016) 57:637–648 et al. 2013). Many divers are not aware that they had Diver pressure and contacts with benthic organisms touched the reef, particularly with their fins (Poonian et al. made by ANMP divers are lower than observed in other 2010) or do not know about diving impacts on corals studies. Despite this, it is evident that the promotion of (Walters and Samways 2001). Unfortunately, most dive sustainable use is a necessary approach within dive tour- tourism destinations lack information on acceptable levels ism management. Long-term monitoring of corals health of contacts with the reef. Sites with higher densities of and visitation rates is one way to effectively assess diver branching corals are more susceptible to diving damage impacts and to introduce regulation as necessary. We because they break easily (Worachananant et al. 2008). A suggest the adoption of five management measures to lower visitation rate is recommended for sites with a reduce coral damage caused by divers in ANMP: (1) greater abundance of branching corals than sites that establishment of a diving carrying capacity, through a mainly consist of massive corals (Riegl and Riegl 1996; study that considers diver profile and site-specific bio- Schleyer and Tomalin 2000). physical characteristics of the reef; (2) provide pre-dive briefings that include ecological aspects of corals, alerting Is Diving Pressure in the ANMP Sustainable? divers on impacts that diving can cause, and alerting specialist photographers and sidemount divers to take Approximately, 1300 scuba divers annually visit the ANMP extra care; (3) increase the number of dive leader inter- and each diver performing on average seven dives, totalling ventions when divers contacted corals, especially careless 9100 dives per year divided between 15 dive sites. Using this or unskilled divers; (4) conduct trainings with dive leader visitation rate and the contact rates determined in this study, with focus on recreational diver impacts and cultural and we estimate that divers touch on corals 74,529 times cause environmental importance of historical artificial reefs; and damage 9464 times and raising sediment onto corals 10,647 (5) start dives over sand bottom or areas of low coral times per year. Diving pressure in ANMP lies below limits abundance. Sites with the highest coral vulnerability (ex. considered to be sustainable (5000–6000 dives per year; high cover of branching corals) should be visited when Hawkins and Roberts 1997), with a maximum of approxi- divers have demonstrated good buoyancy control. These mately 2500 annual dives per site. However, despite the wide strategies could be implemented with cooperation and adoption of proposed diving carrying capacity for reefs support of recreational diving stakeholders such as gov- worldwide, this number varies according to diver behavior ernmental agencies, MPAs managers, and diving opera- and site-specific biophysical characteristics of the reef. tors. The future of recreational diving is largely dependent These characteristics include use intensity, coral growth, the on the health of reef resources and their management is presence of vulnerable species, and reef topography (Haw- essential to conserve the biodiversity of coral reefs. kins and Roberts 1997; Zakai and Chadwick-Furman 2002; Barker and Roberts 2004). Thus, the resilience of coral reefs Acknowledgments We thank dive shops Horizonte Aberto, Ape- can vary substantially, even within the same MPA (Hughes catu Expediço˜es, and Paru´ Divers for the support; dive guides V. Albanez, M. Lana, J. Andrade, M. Affonso, T. Ramon, T. Bonelli, R. and Connell 1999). Coral reefs of ANMP consist of a relic Santoro, D. Cajueiro, M. Kipgem, and E. Said. J. Adelir-Alves for coral fauna with Brazilian endemic forms dating back to the support in data collection; Abrolhos National Marine Park (through R. Tertiary time (Leaõ and Kikuchi 2005). Some species have Jerozolimski) for research permission and support; and C. Sampaio, adapted to water turbidity caused by carbonate and silici- C. Cassano, and W. Goodell for suggestions on manuscript. The first author was supported by the Brazilian Ministry of Education clastic sedimentation (Leaõ and Ginsburg 1997; Leaõ et al. (CAPES) and AS was supported by Ministry of Science and Tech- 2003). Therefore, the determination of a carrying capacity nology (CNPq). that considers site-specific characteristics is an essential strategy to managing diving tourism. 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