Skip to main content

Advertisement

Log in

Whale Shark Tourism: Impacts on Coral Reefs in the Philippines

  • Published:
Environmental Management Aims and scope Submit manuscript

Abstract

Reef-based tourism has been developing rapidly in recent decades yet its impacts on reef ecosystems are often overlooked. In Tan-awan, Oslob, Philippines, whale sharks are attracted to the shallow reefs where they are provisioned up to 50 tons y−1 of feed and this phenomenon in turn attracts >300,000 y−1 visitors. Given the intensive provisioning and concentrating tourism activities, we hypothesized that the whale shark tourism-impacted site (IS) will have greater impacts on reef degradation and higher anthropogenic nitrogen pollution level compared to its reference site (RS). Ecological surveys revealed that relative to the RS, the IS had 36% higher relative abundance of Pocillopora and Porites coral over other genera, >2.5-fold lower coral density, and 20% higher macroalgal cover, which we concluded are signs of reef degradation. Also, we conducted stable nitrogen isotope analysis on gorgonian skeletons to trace nitrogen sources at both sites through time. Although an average 1‰ isotope enrichment found in the IS relative to the RS could indicate anthropogenic nitrogen inputs in the IS, this enrichment was consistent over time and existed before the tourism developed. Despite that, we cautioned against the imminent threat of local eutrophication caused by the continued inputs of nitrogen derived from provisioning and tourism activities. In summary, this study provided the first documentation of the impacts of provisioned whale shark tourism on the local reefs in Tan-awan and established an ecological baseline for future comparisons. Such assessments can offer important information on reef health, coastal development, and tourism management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Araujo G, Lucey A, Labaja J et al. (2014) Population structure and residency patterns of whale sharks, Rhincodon typus, at a provisioning site in Cebu, Philippines. PeerJ 2:e543. https://doi.org/10.7717/peerj.543

    Article  Google Scholar 

  • Araujo G, Snow S, So CL et al. (2017) Population structure, residency patterns and movements of whale sharks in Southern Leyte, Philippines: results from dedicated photo-ID and citizen science: Whale sharks of Southern Leyte. Aquat Conserv Mar Freshw Ecosyst 27:237–252. https://doi.org/10.1002/aqc.2636

    Article  Google Scholar 

  • Archana A, Li L, Shuh-Ji K, Thibodeau B, Baker DM (2016) Variations in nitrate isotope composition of wastewater effluents by treatment type in Hong Kong. Mar Pollut Bull 111:143–152

    Article  CAS  Google Scholar 

  • Baker DM, Kim K, Andras JP, Sparks JP (2011) Light-mediated 15N fractionation in Caribbean gorgonian octocorals: implications for pollution monitoring. Coral Reefs 30:709–717. https://doi.org/10.1007/s00338-011-0759-x

    Article  Google Scholar 

  • Baker DM, Murdoch TJT, Conti-Jerpe I, Fogel M (2017) Investigating Bermuda’s pollution history through stable isotope analyses of modern and museum-held gorgonian corals. Mar Pollut Bull 114:169–175. https://doi.org/10.1016/j.marpolbul.2016.08.069

    Article  CAS  Google Scholar 

  • Baker DM, Rodríguez-Martínez RE, Fogel ML (2013) Ecotourism’s nitrogen footprint on a Mesoamerican coral reef. Coral Reefs 32:691–699

    Article  Google Scholar 

  • Bozec YM, Acosta-González G, Núñez-Lara E, Arias-González JE (2008) Impacts of coastal development on ecosystem structure and function of Yucatan coral reefs, Mexico. In: Proceedings of the 11th International Coral Reef Symposium, 691–695

  • Bruno JF, Selig ER, Casey KS et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:e124. https://doi.org/10.1371/journal.pbio.0050124

    Article  CAS  Google Scholar 

  • Connell JH, Hughes TP, Wallace CC et al. (2004) A long-term study of competition and diversity of corals. Ecol Monogr 74:179–210

    Article  Google Scholar 

  • Craven S (2012). A report on the status of the whale sharks watching tourist industry in Tan-awan, Oslob, Cebu. Retrieved from: Large Marine Vertebrates Project (LAMAVE), Philippines, http://www.lamave.org/wp-content/uploads/2014/11/September-2012-Physalus-Report-on-the-Oslob-whale-shark-interaction.pdf

  • Darling ES, Alvarez-Filip L, Oliver TA et al. (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386. https://doi.org/10.1111/j.1461-0248.2012.01861.x

    Article  Google Scholar 

  • DeGeorges A, Goreau TJ, Reilly B (2010) Land-sourced pollution with an emphasis on domestic sewage: lessons from the caribbean and implications for coastal development on indian ocean and pacific coral reefs. Sustainability 2:2919–2949

    Article  Google Scholar 

  • Edinger EN, Risk MJ (1998) Reef degradation and coral biodiversity in Indonesia: Effects of land-based pollution, destructive fishing practices and changes over time. Mar Pollut Bull 36:14

    Article  Google Scholar 

  • Gil MA, Renfro B, Figueroa-Zavala B et al. (2015) Rapid tourism growth and declining coral reefs in Akumal, Mexico. Mar Biol 162:2225–2233. https://doi.org/10.1007/s00227-015-2748-z

    Article  Google Scholar 

  • Gladstone W, Curley B, Shokri MR (2013) Environmental impacts of tourism in the Gulf and the Red Sea. Mar Pollut Bull 72(2):375–388

    Article  CAS  Google Scholar 

  • Gohar A, Kondolf GM (2016) Sustainable tourism along the red sea: still possible? Civ Eng Archit 4:39–46. https://doi.org/10.13189/cea.2016.040201

    Article  Google Scholar 

  • Hall CM (2001) Trends in ocean and coastal tourism: the end of the last frontier? Ocean Coast Manag 44:601–618. https://doi.org/10.1016/S0964-5691(01)00071-0

    Article  Google Scholar 

  • Hashimoto W, Matsumaru K, Kurihara K, David PP, Balce GR (1977) Larger foraminiferal assemblages useful for the correlation of the Cenozoic marine sediments in the mobile belt of the Philippines. Geol Paleontol Southeast Asia 18:103–123

    Google Scholar 

  • Hasler H, Ott JA (2008) Diving down the reefs? Intensive diving tourism threatens the reefs of the northern Red Sea. Mar Pollut Bull 56:1788–1794. https://doi.org/10.1016/j.marpolbul.2008.06.002

    Article  CAS  Google Scholar 

  • Hawkins JP, Roberts CM, Van't Hof T, De Meyer K, Tratalos J, Aldam C (1999) Effects of recreational scuba diving on Caribbean coral and fish communities. Conserv Biol 13(4):888–897

    Article  Google Scholar 

  • Kendall C, Elliott EM, Wankel SD (2007) Tracing anthropogenic inputs of nitrogen to ecosystems, Chapter 12, In: Michener RH and Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Publishing, p 375–449

  • Kuffner I, Walters L, Becerro M et al. (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117. https://doi.org/10.3354/meps323107

    Article  Google Scholar 

  • Lamb JB, True JD, Piromvaragorn S, Willis BL (2014) Scuba diving damage and intensity of tourist activities increases coral disease prevalence. Biol Conserv 178:88–96

    Article  Google Scholar 

  • Lamb JB, Willis BL (2011) Using coral disease prevalence to assess the effects of concentrating tourism activities on offshore reefs in a tropical marine park. Conserv Biol 25(5):1044–1052

    Article  Google Scholar 

  • Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms and coral reefs. Limnol Ocean 44:1586–1592

    Article  Google Scholar 

  • Leinfelder RR, Seemann J, Heiss GA, Struck U (2012) Could “ecosystem atavisms” help reefs to adapt to the Anthropocene. In: Proceedings of the 12th International Coral Reef Symposium ICCS2012_2B_2 Vol.5

  • Leujak W, Ormond RF (2008) Quantifying acceptable levels of visitor use on Red Sea reef flats. Aquat Conserv 18(6):930–944

    Article  Google Scholar 

  • Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  • McCook L, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417. https://doi.org/10.1007/s003380000129

    Article  Google Scholar 

  • Naumann MS, Bednarz VN, Ferse SCA, et al (2015) Monitoring of coastal coral reefs near Dahab (Gulf of Aqaba, Red Sea) indicates local eutrophication as potential cause for change in benthic communities. Environ Monit Assess 187. https://doi.org/10.1007/s10661-014-4257-9

  • Philippines Statistics Authority (PSA) (2015) "Region VII (CENTRAL VISAYAS)". Census of Population: Total Population by Province, City, Municipality and Barangay (Report). PSA. https://www.psa.gov.ph/sites/default/files/attachments/hsd/pressrelease/R07.xlsx Retrieved 20 April 2018***

  • Phillips MR, Jones AL (2006) Erosion and tourism infrastructure in the coastal zone: problems, consequences and management. Tour Manag 27(3):517–524

    Article  Google Scholar 

  • Pisapia C, Anderson K, Pratchett MS (2014) Intraspecific variation in physiological condition of reef-building corals associated with differential levels of chronic disturbance. PLoS One 9:e91529. https://doi.org/10.1371/journal.pone.0091529

    Article  CAS  Google Scholar 

  • Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS One 9(7):e102498

    Article  Google Scholar 

  • Portugal AB, Carvalho FL, de Macedo Carneiro PB et al. (2016) Increased anthropogenic pressure decreases species richness in tropical intertidal reefs. Mar Environ Res 120:44–54. https://doi.org/10.1016/j.marenvres.2016.07.005

    Article  CAS  Google Scholar 

  • Raymundo LJ, Couch CS, Harvell CD (eds) (2008) Coral disease handbook: guidelines for assessment, monitoring & management. Coral Reef Targeted Research and Capacity Building for Management Program, Centre for Marine Studies, University of Queensland, St. Lucia, Qld

  • Raymundo LJ, Diaz R, Miller A, Reynolds T (2011) Baseline surveys of proposed and established Marine Sanctuaries on Bantayan Island, Northern Cebu. UOG Marine Lab Tech Rep 141

  • Raymundo LJ, Halford AR, Maypa AP, Kerr AM (2009) Functionally diverse reef-fish communities ameliorate coral disease. Proc Natl Acad Sci 106:17067–17070. https://doi.org/10.1073/pnas.0900365106

    Article  Google Scholar 

  • Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Organ 64:181–191

    Article  Google Scholar 

  • Redding JE, Myers-Miller RL, Baker DM et al. (2013) Link between sewage-derived nitrogen pollution and coral disease severity in Guam. Mar Pollut Bull 73:57–63. https://doi.org/10.1016/j.marpolbul.2013.06.002

    Article  CAS  Google Scholar 

  • Renfro B, Chadwick NE (2017) Benthic community structure on coral reefs exposed to intensive recreational snorkeling. PLoS One 12:e0184175. https://doi.org/10.1371/journal.pone.0184175

    Article  CAS  Google Scholar 

  • Reopanichkul P, Schlacher TA, Carter RW, Worachananant S (2009) Sewage impacts coral reefs at multiple levels of ecological organization. Mar Pollut Bull 58:1356–1362. https://doi.org/10.1016/j.marpolbul.2009.04.024

    Article  CAS  Google Scholar 

  • Riegl B, Berumen M, Bruckner A (2013) Coral population trajectories, increased disturbance and management intervention: a sensitivity analysis. Ecol Evol 3:1050–1064

    Article  Google Scholar 

  • Risk MJ, Burchell M, Brunton DA, McCord MR (2014) Health of the coral reefs at the US Navy Base, Guantánamo Bay, Cuba: a preliminary report based on isotopic records from gorgonians. Mar Pollut Bull 83:282–289. https://doi.org/10.1016/j.marpolbul.2014.03.026

    Article  CAS  Google Scholar 

  • Risk MJ, Lapointe BE, Sherwood OA, Bedford BJ (2009) The use of δ15N in assessing sewage stress on coral reefs. Mar Pollut Bull 58:793–802. https://doi.org/10.1016/j.marpolbul.2009.02.008

    Article  CAS  Google Scholar 

  • Sandin SA, Smith JE, DeMartini EE et al. (2008) Baselines and degradation of coral reefs in the northern line Islands. PLoS One 3:e1548. https://doi.org/10.1371/journal.pone.0001548

    Article  CAS  Google Scholar 

  • Sawall Y, Jompa J, Litaay M et al. (2013) Coral recruitment and potential recovery of eutrophied and blast fishing impacted reefs in Spermonde Archipelago, Indonesia. Mar Pollut Bull 74:374–382. https://doi.org/10.1016/j.marpolbul.2013.06.022

    Article  CAS  Google Scholar 

  • Schleimer A, Araujo G, Penketh L et al. (2015) Learning from a provisioning site: code of conduct compliance and behaviour of whale sharks in Oslob, Cebu, Philippines. PeerJ 3:e1452. https://doi.org/10.7717/peerj.1452

    Article  Google Scholar 

  • Sherwood OA, Heikoop JM, Scott DB, Risk MJ, Guilderson TP, McKinney RA (2005) Stable isotopic composition of deep-sea gorgonian corals Primnoa spp.: a new archive of surface processes. Mar Ecol Prog Ser 301:135–148

    Article  CAS  Google Scholar 

  • Spalding M, Burke L, Wood SA et al. (2017) Mapping the global value and distribution of coral reef tourism. Mar Policy 82:104–113. https://doi.org/10.1016/j.marpol.2017.05.014

    Article  Google Scholar 

  • Thomson JA, Araujo G, Labaja J et al. (2017) Feeding the world’s largest fish: highly variable whale shark residency patterns at a provisioning site in the Philippines. R Soc Open Sci 4:170394. https://doi.org/10.1098/rsos.170394

    Article  Google Scholar 

  • Uyarra MC, Watkinson AR, Cote IM (2009) Managing dive tourism for the sustainable use of coral reefs: validating diver perceptions of attractive site features. Environ Manag 43(1):1–16

    Article  Google Scholar 

  • Vega Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR (2013) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Chang Biol. https://doi.org/10.1111/gcb.12450

  • Vermeulen S, Sturaro N, Gobert S, Bouquegneau JM, Lepoint G (2011) Potential early indicators of anthropogenically derived nutrients: a multiscale stable isotope analysis. Mar Ecol Prog Ser 422:9–22

    Article  Google Scholar 

  • Ward-Paige C, Risk M, Sherwood O (2005) Reconstruction of nitrogen sources on coral reefs: δ15N and δ13C in gorgonians from Florida Reef Tract. Mar Ecol Prog Ser 296:155–163

    Article  CAS  Google Scholar 

  • Wielgus J, Chadwick-Furman NE, Dubinsky Z (2004) Coral cover and partial mortality on anthropogenically impacted coral reefs at Eilat, northern Red Sea. Mar Pollut Bull 48:248–253. https://doi.org/10.1016/j.marpolbul.2003.08.008

    Article  CAS  Google Scholar 

  • Willis BL, Page C, Dinsdale EA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y editors. Coral Health and Disease. Springer, Berlin, p 69–104

    Chapter  Google Scholar 

  • Worachananant S, Carter RW, Hockings M, Reopanichkul P (2008) Managing the Impacts of SCUBA Divers on Thailand’s Coral Reefs. J Sustain Tour 16:645. https://doi.org/10.2167/jost771.0

    Article  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Large Marine Vertebrates Research Institute Philippines (LAMAVE) for the logistical support during our expedition in Tan-awan. We are grateful to be granted an export commodity clearance from the Bureau of Fisheries and Aquatic Resources—Region 7, Department of Agriculture, Republic of the Philippines. We also thank Mr. Ronald Guaren, the municipal mayor of Oslob, Cebu, for permitting the collection of samples for this study. We would like to acknowledge Ms. Holly Wong from the Department of Earth Sciences at the University of Hong Kong for assistance with stable isotope analyses as well as Dr. Nicolas Duprey, Jeffrey Yuen, and Arthur Chung for their support in laboratory work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David M. Baker.

Ethics declarations

conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wong, C.W.M., Conti-Jerpe, I., Raymundo, L.J. et al. Whale Shark Tourism: Impacts on Coral Reefs in the Philippines. Environmental Management 63, 282–291 (2019). https://doi.org/10.1007/s00267-018-1125-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00267-018-1125-3

Keywords

Navigation