MPB-08144; No of Pages 9 Marine Pollution Bulletin xxx (2016) xxx–xxx
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Ecological impacts and management implications of reef walking on a tropical reef flat community Jane E. Williamson ⁎, Evan E. Byrnes 1, Jennalee A. Clark 1, David M. Connolly 1, Sabine E. Schiller 1, Jessica A. Thompson 1, Louise Tosetto 1, Julieta C. Martinelli, Vincent Raoult Department of Biological Sciences, Macquarie University, NSW 2109, Australia
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Article history: Received 3 August 2016 Received in revised form 10 October 2016 Accepted 31 October 2016 Available online xxxx Keywords: Trampling Human impact Nature-based tourism Holothuria atra Great Barrier Reef Marine Park Australia
a b s t r a c t Continued growth of tourism has led to concerns about direct and indirect impacts on the ecology of coral reefs and ultimate sustainability of these environments under such pressure. This research assessed impacts of reef walking by tourists on a relatively pristine reef flat community associated with an ‘ecoresort’ on the Great Barrier Reef, Australia. Heavily walked areas had lower abundances of live hard coral but greater amounts of dead coral and sediment. Abundances of macroalgae were not affected between sites. Coral-associated butterflyfish were less abundant and less diverse in more trampled sites. A manipulative experiment showed handling holothurians on reef walks had lasting negative impacts. This is the first study to show potential impacts of such handling on holothurians. Ecological impacts of reef walking are weighed against sociocultural benefits of a first hand experience in nature. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction Coral reefs are among the most biodiverse and ecologically productive ecosystems globally (Connell, 1978) and are of high economic value in terms of goods and services (Brander et al., 2007). Associated ecosystem services of coral reefs are valued at over US$30 billion annually (Hannak et al., 2011), and over 500 million people rely on coral reefs for provision of goods and services (Hoegh-Guldberg et al., 2007). Much of the economic activities associated with coral reefs relate to the burgeoning industry of tourism. In 2013, for example, tourism activity on the Great Barrier Reef Marine Park contributed AUD$5.2 billion to the Australian economy, and accounted for approximately 2.09 million visitors (Deloitte Access Economics, 2013, GBRMPA 2014). Common activities associated with marine tourism on coral reefs include water sports (e.g., parasailing and jet skiing), motor boating, recreational fishing, wildlife watching, snorkeling, SCUBA diving, and reef walking (Gladstone et al., 2013). While the ecological impacts of many of these activities are well studied, those of reef walking are less understood. Nevertheless, walking on the reef can cause breaks to coral and an increase in suspended matter, which can lead to an overall reduction in coral cover and changes to community structure (Woodland and Hooper, 1977; Liddle and Kay, 1987; Kay and Liddle, 1989; Hawkins and Roberts, 1993; Rodgers et al., 2003; Leujak and Ormond, 2008). ⁎ Corresponding author. E-mail address:
[email protected] (J.E. Williamson). 1 Author names listed in alphabetical order.
Long term impacts of coral decline can put the 7.5% of humanity that depend on those reefs (Barbier et al., 2011) in jeopardy. Tourism on the Great Barrier Reef (GBR) in Australia represents both a threat and an incentive for its conservation. With approximately one third of the GBR protected under no-take zones, and activities within these areas monitored to facilitate sustainability (Osmond et al., 2010), the opportunity for tourism expanding to more pristine marine areas has arisen. Many of the resorts on the GBR advertise under the category of ‘ecotourism’, which is generally perceived by the public to relate to ecologically sustainable tourism, with an assumed focus on conservation awareness and minimal human impact (Bjork, 2000). One such destination is the resort on Heron Island. Heron Island, on the Capricorn group, southern GBR, is a sand cay surrounded by a biodiverse fringing reef that is considered to be one of the more pristine fringing reefs on the GBR. A resort was established on the island in 1932 and has remained a tourist destination since then. It is now marketed as an ecotourist destination. Heron Island Resort maintains that an increase in conservation awareness in guests is achieved by promoting educational and nature-based activities, such as reef walking. Here, guests can follow educated guides on set tours, or explore the reef individually. The resort provides guests with walking shoes and poles, along with information on organisms residing on the reef flat. Guests are encouraged to pick up and handle non-dangerous marine animals such as asteroids (sea stars) and holothurians (sea cucumbers) as part of the educational experience. While education and involvement in a high-quality experience in nature can promote longterm environmental stewardship in the visitors (Ross and Wall, 1999),
http://dx.doi.org/10.1016/j.marpolbul.2016.10.069 0025-326X/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article as: Williamson, J.E., et al., Ecological impacts and management implications of reef walking on a tropical reef flat community, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.10.069
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the ecological impacts of these tourists walking on the reef remain unknown. Here we examined the ecological impacts of reef walking by tourists on the structure and composition of a reef flat on Heron Island. Specifically, we assessed the impact of this activity on the abundance of living and dead hard corals (Scleractinia), and macroalgae on the reef flat where the majority of reef walking is thought to occur (Heron Island Resort, personal communication). We predicted that the abundance of live hard corals would be lower in areas more impacted by trampling by reef walkers. As more disturbed reef flats are more predisposed to phase shifts from coral to algae (Bellwood et al., 2004), we also predicted that the abundance of macroalgae, dead coral and areas of bare sand would correspondingly increase in areas more impacted by trampling. Many species of teleosts rely on coral for sustenance and shelter, such as butterflyfishes of the genus Chaetodon, which feed on the hard coral (Cole et al., 2008). We thus also predicted that the abundance and diversity of butterflyfishes would decrease if the relative abundance of the live hard coral decreased. Finally, a laboratory experiment was done to assess the impact of handling stress of the most common species of holothurian on the reef flat, Holothuria atra. We predicted that handling stress would result in decreased rates of feeding and defecation in the holothurians, and that impacts associated with handling stress would increase with increasing handling times. 2. Materials and methods 2.1. Study site The study was done in April 2014 on the northern fringing reef flats at Heron Island (23°30′S, 152°05′E) on the Great Barrier Reef, Australia. The reef surrounding Heron Island has varying levels of protection including Conservation Park, Marine National Park and Scientific Research
Zones. The fringing reef flat community is typical of offshore fringing reefs at similar latitudes on the GBR (Ringeltaube and Harvey, 2000; De'ath et al., 2012; Dean et al., 2015). Fringing reef on the northern side of the island occurs adjacent to Heron Island Resort and is frequented by tourists. Reef on the southern side of the island is zoned for research only and is thought to only receive minimal visitation by tourists (Fig. 1).
2.2. Reef walker survey To determine the pattern of reef use by walkers near the resort, the northern fringing reef on Heron Island was arbitrarily divided into 24 grid sections using geographic landmarks, in a six by four pattern. Landmarks included large boulders on the shore, high outcrops of coral, and star picket markers used by the resort. Reef walking was offered on a daily basis by the resort. The number of reef walkers present in each grid section was recorded every 5 min by an observer on the deck area of the resort, starting 2 h before the low tide until either (a) 2 h after the low tide, (b) sunset, or (c) all reef walkers had left the reef flat. The survey was repeated during daytime low tides over five consecutive days, for at least 4 h per day. The deck area offered uninterrupted views of the entire grid area, including landmarks. Data on the number of reef walkers were pooled across days and times, and a goodness-of-fit Poisson distribution test was used to determine if the number of reef walkers differed between sections. If differences were found between grid sections, a further Welch two-sample t-test was used to assess the significance of these differences. No attempt was made to identify, categorise or track individuals along their walk as it was not possible to accurately follow so many individuals over such a large expanse. It was also not possible with this design to gain an adequate estimate of the length of time reef walkers spent in a
Scale 500m
Study Sites
Heron Reef
Fig. 1. Satellite image of Heron Island and the surrounding reef, and the general area of study sites designated. Heron Island Resort is located on the northern side of the island.
Please cite this article as: Williamson, J.E., et al., Ecological impacts and management implications of reef walking on a tropical reef flat community, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.10.069
J.E. Williamson et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
Differences in relative abundance and species diversity of butterflyfishes were assessed using two-tailed t-tests. Data were log transformed and residual plots checked for homogeneity of variance. The diversity for each transect was quantified using the Shannon-Weiner index (H). H was calculated as:
particular grid section and, as such, it should be noted that the number of reef walkers is almost certainly a subset of the visitations recorded.
2.3. Abundance of hard coral and macroalgae, and areas of sediment
X H0 ¼ − pi lnpi
Based on the activity of reef walkers on the northern fringing reef, two sections of the reef that received differing amounts of reef walking were chosen to assess differences in the abundance and diversity of hard coral, macroalgae, and sediment. The first reef section (coined “less disturbed”) received few reef walkers during the above survey. This area aligned with where reef walking is discouraged (resort employees, personal communication). The second reef section (coined “disturbed”) received the majority of reef walker visitations over the five days of sampling. Two areas were sampled within each section: the inner reef and the outer reef, giving a total of four reef sections: less disturbed inner, less disturbed outer, disturbed inner and disturbed outer (Fig. 2). Ten replicate 1 m2 quadrats were randomly placed within each of the four reef sections. All hard coral and macroalgae were identified to genus. Abundances of living hard coral, dead hard coral, macroalgae and exposed sediment (sand) were recorded within each quadrat using methods proposed by Dethier et al. (1993). To assess any differences in relative abundance of these four elements in each reef section, a Kruskal-Wallis rank sum test was done for each group, followed by a Wilcoxon rank sum test, with a significance of 95%. All analyses were done using R (version 3.0.2; R core team 2013).
where pi is the proportion of individuals found in each transect. Wilcoxon Rank Sum tests were done to test for differences between the four reef sections. 2.5. Holothurian survey As a precursor to the holothurian handling experiment, field surveys were done in both the disturbed and less disturbed reef sections of the inner reef to assess which species of holothurians were most abundant at each site. It was assumed that reef walkers were most likely to pick up and handle the most common and obvious species of harmless holothurians while reef walking. Species in this area were compared with those from the less disturbed area to see whether there was a difference in abundance of the species between the two reef sections. Surveys were done at low tide. All holothurians within a 10 m2 quadrat were identified to species, and seven replicate quadrats were done in each reef section. A two-factor ANOVA (site and species as fixed factors) was used to test for differences between species and sites. The most common species within the disturbed site was Holothuria atra, and this species was used for the holothurian handling experiment.
2.4. Butterflyfish survey The number and species of butterflyfish in disturbed and less disturbed sections on the northern fringing reef were surveyed using replicate 50 × 3 m belt transects, with 40 replicates per reef section. Reef sections were approximately 500 m apart. A 50 m transect was laid directly into the current and then left for 5 min to allow fish to acclimate. After acclimation, one pair of snorkelers swam directly over the transect at a pace no faster than 10 m min−1. One snorkeler identified and recorded all butterflyfish within the estimated 1.5 m of both sides of the tape while the other snorkeler videoed the same area. Video was later viewed for confirmation of species identification and to detail any individuals that may have been missed. At the completion of each transect, the tape was then moved to a new site approximately 75 m from the previous transect.
2.6. Holothurian handling experiment An experiment using the flow-through outdoor aquaria at Heron Island Research Station was done to assess the impact of handling on Holothuria atra. Three separate trials of 36 h duration, each 24 h apart, were run. Two handling treatments (duration of 2 min and 4 min) of the same handling intensity were compared to a control (no handling) within each trial (3 replicates per treatment and control per trial). Handling duration was based on information from resort outreach staff, who indicated that reef walkers usually handled the animals for “a couple of minutes”. Personal observation by our authors confirmed this information. Impacts of handling were assessed by the number of ‘bites’ (i.e., the number of times a tentacle laden with sediment moved into
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