Anthropogenic disturbances to foraging and resting green turtles around Oahu: potential effects and assessment of harassment
Anthropogenic disturbances to foraging and resting green turtles (Chelonia mydas) around O`ahu: potential effects and assessment of harassment
Robert H. Schmidt
Abstract: Hawaiian green turtles are listed as a threatened species under the U.S. Endangered Species Act. The Hawaiian population of green turtles is rather unique in that the nesting site (French Frigate Shoals) is protected, usually uninhabited, and without many terrestrial predators. Juveniles and adults over 35 cm SCL reside in the nearshore habitats surrounding the populated islands, including O`ahu. These animals are the future breeders who have survived the initial high-mortality pelagic stage. I reviewed non-lethal, anthropogenic factors that could compromise their energy intake, predation risk, or risk of being subjected to detrimental human contact. My findings were inconclusive. Green turtle behavior and turtle responses to human activities are too variable to make definitive predictions regarding the positive or negative consequences of non-lethal human-turtle interactions. I recommend continued enforcement of existing laws prohibiting harassment, and suggest that educational programs would be of assistance in making sure that people interacting with green turtles are aware of potential negative impacts.
Green turtles (Chelonia mydas) in the Pacific Basin, like many populations of sea turtles in our oceans, face a suite of management and conservation concerns. Destruction or degradation of natal beaches, increased egg or hatchling loss through animal predation or human harvests, toxic chemical and debris encounters, loss of foraging habitat, and intentional and accidental mortality of adults and juveniles through fishing or trawling activities, development, or harvesting all play a role in affecting turtle populations (summarized by Eckert 1995, Lutcavage et al. 1997). Emerging issues, such as green turtle fibropapillomatosis and increasing demands on the world’s fisheries, beaches, and near-shore habitats will continue to challenge green turtle conservation programs (Ehrhart 1998).
Green turtle populations in the Hawaiian Archipelago have the luxury of nesting exclusively on uninhabited sand islands at French Frigate Shoals, part of the Hawaiian Islands National Wildlife Refuge. Numbers of nesting females here ranged from 94 to 248 during the period 1973-1979 (Balazs 1995a), and 504 in 1997 (Rillero 1999) and terrestrial predation on eggs and hatchlings is minimal. Juveniles and adults greater than 35 cm SCL forage and rest in near-shore habitats of the populated islands, including O`ahu (Balazs 1995b, Balazs et al. 2000).
Hawai`i hosted nearly 7 million visitors in 2000, and the average daily visitor census for O`ahu was 84,911 (State of Hawaii 2001). An unknown number of these visitors, in addition to Hawai`i’s residents, recreate in green turtle foraging and resting habitats. These visitors are not distributed randomly throughout the coastline, and are probably concentrated in areas devoted to housing and feeding them (especially Honolulu). Murakawa et al. (2000) noted that, of 2377 recorded green turtle strandings in Hawai`i, 75% had occurred on O`ahu, although O`ahu accounts for only 15% of the 1200 km of coastline of the inhabited islands. Strandings occurred evenly throughout the year with no seasonal variation. A number of commercial dive shops specifically emphasize snorkeling and SCUBA dives in proximity to green turtles (Balazs et al.1987; R. Schmidt, personal observation), and Hawaiian turtles have been studied in areas with high tourist use (Balazs et al. 1994).
In the absence of people, it is assumed that turtles would select appropriate foraging, resting, and predator avoidance sites, and that turtles would make appropriate foraging decisions (what to eat, time spent foraging, time spent in a particular patch, travel pattern between patches, etc.), resting decisions (time spent foraging versus resting, selection of resting sites, contending with potential competition for a site, etc.), and predator avoidance decisions (time spent near to shore, time spent close to bottom, time spent looking for predators, time spent out of the water, etc.). In the presence of people, green turtles may utilize these habitats in some altered fashion, both spatially and temporally.
The consequences of these altered behaviors are unknown. If human-induced changes in turtle behavior exist, the result could be a reduced energetic intake, higher vulnerability to predation or other mortality/stressing factors, altering nesting frequency, or increasing competition between turtles for habitats left available (foraging, resting), with resultant individual or population effects. Bjorndal (1997:221), in reviewing turtle foraging ecology, concluded “… the negative effects of human activities on the foraging habitats of sea turtles and their diet quality and availability must be quantified and controlled. Such quantification will be difficult because many of the negative effects are sublethal or are indirect results of changes in the delicate balance of marine ecosystems, and thus difficult to trace.” Positive effects may occur as well, such as the development of new turtle habitats (Balazs 1995c).
This review assesses the potential impact of human activities on resident juvenile and adult green turtles around O`ahu, Hawai`i. For the purpose of this review, I am defining a significant impact as one that has a measurable effect on daily energy intake, predation risk, or resting time of individual green turtles. I am not reviewing intentional and unintentional mortality through fishing, boating, beach replenishment activities, poaching, chemical spills, net entanglement, plastic ingestion, or other sources that cause mortality in Hawaiian green turtles (Work and Balazs 1998). The focus will by on harassment of individual turtles by people in the water (swimmers, snorkelers, free divers, and SCUBA divers) and people enjoying water activities (kayaking, paddling, surfing, windsurfing, boating).
Characteristics of the green turtle population in the Hawaiian Archipelago
Balazs (1995b) indicated that green turtles measuring less than 35 cm SCL were not found in coastal foraging areas, so resident animals consisted of adults and juveniles over 35 cm. He noted that green turtles on undisturbed islands came ashore to bask or rest (Balazs 1995b, Whittow and Balazs 1982). Green turtles have been observed basking on the Island of Hawai`i since 1990 (Rellero 1999, Davis et al. 2000). The growth rate of tagged juvenile green turtles on O`ahu (Kaneohe Bay) was approximately 2 cm/yr (Balazs 2000), or about twice as fast as juvenile turtles on remote, sparsely populated islands in the northern part of the chain (Balazs (1995b). Slow growth rates in green turtles are the result of nutritional as opposed to genetic factors, and lowered growth rates will correspondingly result in delayed sexual maturity (Bjorndal 1980). Balazs et al. (1994) calculated growth rates for 2 turtles off Waikiki Beach; a 57.6 cm SCL and a 69.3 cm SCL turtle had calculated growth rates of 3.7 cm/yr and 3.0 cm/yr, respectively, after recapture. While higher growth rates imply better foraging areas, turtles along Waikiki Beach have been discovered with propeller-caused injuries, entangled in nets and fishing line, with attached fishhooks and spear wounds, and with shark-related wounds (Balazs et al. 1994).
Green turtles, predation risk, and human disturbance
Heithaus et al. (2002) conducted observations on tiger shark (Galeocerdo cuvier) predation on green turtles in Australia and on green turtle escape behaviors. They concluded that green turtles had a lower risk of tiger shark predation than loggerhead sea turtles (Caretta caretta), primarily because of their faster speed and their use of sharp turns while being pursued, even though green turtles spent more time in habitats favored by tiger sharks. It is unknown to what extent anthropogenic activities modify this risk (shark predation) in Hawaiian waters.
Losey et al. (1994:685) noted that turtles at cleaning stations were disturbed easily by divers. However, Balazs et al. (1994:15) reported that green turtles along the reef at Waikiki Beach regularly surfaced near tourists “… swimming, wading, or floating on air mattresses.” SCUBA divers, surfers, and sailors commonly encounter turtles here (Balazs et al. 1994; R. Schmidt, personal observation). Balazs et al. (1994:16) speculated “…turtles at several sites throughout the Hawaiian Islands have demonstrated a surprising tameness to swimmers, divers, and people walking along the shoreline. The reason for this phenomenon is unknown, but could be due to protective regulations and their generally effective enforcement.” Balazs (1995c) noted a number of documented changes in green turtle behavior in Hawai`i. These included utilization of foraging sites not known to be utilized in prior years, a shift in feeding time from primarily nocturnal to primarily diurnal, the use of power plant-related warm water discharges, and increased tolerance to human presence. Boats can affect turtle behavior, but some turtles spent considerable time in areas with heavy boat traffic (Brill et al. 1995).
Green turtle behavior
Hawai`i’s green turtles show variability in how they allocate their feeding and resting times. Davis et al. (2000) monitored 2 turtles for 6 and 13 months, respectively, and measured resting and foraging periods temporally and spatially. These turtles were monitored intensively with computerized time and depth recorders, and with visual observations. Turtles foraged both day and night, and averaged 10 and 5 hours resting during a 24-hour period, and demonstrated strong site fidelity in these resting and foraging areas. Brill et al. (1995) monitored 12 turtles within a single foraging area in Hawaii (Kaneohe Bay) and developed baseline information on turtle daily movement patterns and submergence intervals. They compared turtles with fibropapillomatosis with those with no tumors. Both groups of turtles varied in their daily use of resting and foraging areas, as well as whether they foraged during the night or not. A 72.5 cm SCL juvenile green turtle monitored by Rice et al. (2000), monitored electronically for 249 days at Punalu`u, Hawai`i, averaged 12 hours of resting dives, 9 hours of foraging behavior, 1 hour of basking behavior, and 2 hours of surface/travel time daily. There was great variability in this turtle’s daily behavior patterns, with some days apparently devoted entirely to resting dives and no foraging, and other days with up to 20 hours of continuous foraging. I know of no studies comparing movement and submergence patterns of turtles in undisturbed and disturbed locations. In summary, green turtle behavior, as a baseline, is variable.
Mellgren and Mann (2000) suggested that green turtles can learn about food sources from conspecifics. Balazs et al. (1987:19) observed that movement by a single turtle on the bottom fleeing from a diver would serve as a signal for other turtles to flee, even if the other turtles could not see the approaching diver. Turtles learn the location of “turtle cleaning stations” (Losey et al. 1994), a behavior that probably requires social facilitation. These are interesting patterns, especially in that turtles learning from other turtles are at best only remotely related, with no obvious advantage to inclusive fitness.
As stated above, Balazs (1995) outlined recent changes in turtle tolerance of humans. He noted “Tolerance to humans… ranges from being virtually tame with no apparent fear (i.e., swimming right up to divers even when there is no history of hand-feeding), to turtles exhibiting guarded caution and only swimming away when approached too close.” It is assumed (but not documented) that unpleasant harassment would reduced tolerance for human presence, but researchers have noted that the handling associated with capture, weighing, measuring, and the attachment of transmitters to turtles produces only “transient behavioral effects” (Brill et al. 1995:206).
Impacts of turtle tourism
Most published accounts of the relationships between tourists actively or passively interacting with turtles deal with organized turtle watches on nesting beaches. Johnson et al. 1996) reported that organized turtle watches resulted in loggerhead turtles spending significantly less time in camouflaging their nest sites, but concluded that there was no overall reduction in hatchling production. Jacobson and Lopez (1994) noted that tourists disturbed nesting green turtles in Costa Rica with flashlights and flash cameras, physically blocking or touching turtles, digging near nests, and handling hatchlings. However, they concluded that a tour guide program would solve these issues. Tourism and its associated development caused a reduction in poaching of hawksbill turtles (Eretmochelys imbricata) in Barbados due to increased lighting and security personnel (Horrocks et al. 2000). Since green turtles do not nest on O`ahu, organized turtle watches are not well developed. Educational programs are considered very important in integrating sea turtle conservation programs with the needs of local people and tourists (e.g., Mortimer 2000). In Hawai`i, Rebelo (1994) sampled tourists with an intercept survey at 2 sites in O`ahu and reported that there was great interest in sea turtles, suggesting a role for the development of educational materials and signage.
Conclusion: what are the effects of turtle harassment?
There can be no doubt that non-lethal anthropogenic activities affect turtles. The question is whether these activities result in significant impacts to individual green turtles or to the Hawaiian green turtle population. My review is inconclusive, as sublethal effects of these interactions has not been investigated. Depending on the intensity of a disturbance event, and the intervals between disturbance events, turtles could leave favored foraging and resting areas. However, the variability in daily activity patterns of green turtles makes any specific prediction vague. In addition, the non-random distribution of human activities in nearshore habitats means that most green turtles will not be exposed to harassment.
Nevertheless, for a threatened species, juveniles and adults are critical components of the Hawaiian green turtle population. All harassment activities that can be prevented and avoided should be prevented and avoided. A danger to avoid is complacency; if some turtles seem to tolerate or ignore harassment, it must not be assumed that all turtles tolerate the same activities. Since the US Endangered Species Act prohibits the “taking” of a threatened species (the term "take" means to harass, harm, pursue, hunt, shoot, wound, kill, trap, capture, or collect, or to attempt to engage in any such conduct; US Fish and Wildlife Service 2001), these restrictions should be publicized, explained, and enforced. Research should continue to elucidate the sublethal and indirect results of changes in the delicate balance of marine ecosystems (Bjorndal 1997).
Balazs, G. H. 1995a. Status of sea turtles in the central Pacific Ocean. Pages 243-252 in K. A. Bjorndal, editor. Biology and Conservation of Sea Turtles. Smithsonian Institution Press, Washington. 615 pp.
Balazs, G. H. 1995b. Growth rates of immature green turtles in the Hawaiian Archipelago. Pages 117-125 in K. A. Bjorndal, editor. Biology and Conservation of Sea Turtles. Smithsonian Institution Press, Washington. 615 pp.
Balazs, G. 1995c. Behavioral changes within the recovering Hawaiian green turtle population. Proceedings of the Annual Symposium on Sea Turtle Biology and Conservation 15:16-21.
Balazs, G., R. Miya, and M. Finn. 1994. Aspects of green turtles in their feeding, resting, and cleaning areas off Waikiki Beach. Proceedings of the Annual Symposium on Sea Turtle Biology and Conservation 13:15-18.
Balazs, G., R. Forsyth, A. Kam. 1987. Preliminary assessment of habitat utilization by Hawaiian green turtles in their resident foraging pastures. National Marine Fisheries Service, NOAA, Southwest Fisheries Center Honolulu Laboratory, NOAA-TM-NMFS-SWFC-71. 107 pp.
Balazs, G., S. Murakawa, D. Ellis, and A. Aguirre. 2000. Manifestation of fibropapillomatosis and rates of growth of green turtles at Kaneohe Bay in the Hawaiian Islands. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 18:112-113.
Bjorndal, K. 1980. Nutrition and grazing behavior of the green turtle Chelonia mydas. Marine Biology 56:147-154.
Bjorndal, K. 1997. Foraging ecology and nutrition of sea turtles. Pages 199-231 in P. Lutz and J. Musick, editors. The Biology of Sea Turtles. CRC Press, Boca Raton, FL. 432 pp.
Brill, R., G. Balazs, K. Holland, R. Chang, S. Sullivan, and J. George. 1995. Daily movements, habitat use, and submergence intervals of normal and tumor-bearing juvenile green turtles (Chelonia mydas L.) within a foraging area in the Hawaiian islands. Journal of Experimental Marine Biology and Ecology 185:203-218)
Davis, E., M. Rice, K. Harrington, and G. Balazs. 2000. Green turtle diving and foraging patterns at Puako, Hawaii. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 19:153-154.
Eckert, K. L. 1995. Anthropogenic threats to sea turtles. Pages 611-612 in K. A. Bjorndal, editor. Biology and Conservation of Sea Turtles. Smithsonian Institution Press, Washington. 615 pp.
Ehrhart, L. 1998. Habitat protection revisited: debunking the Noah solution. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 17:46-49.
Heithaus, M., A. Frid, and L. Dill. 2002. Shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles. Marine Biology 140:229-236.
Horrocks, J., S. Hertzlieb, and V. Copeman. 2000. Mortality rates of nesting hawksbill turtles in Barbados: a positive impact of tourism on sea turtles. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 18:138-139.
Jacobson, S., and A. Lopez. 1994. Biological impacts of ecotourism: tourists and nesting turtles in Tortugero National Park, Costa Rica. Wildlife Society Bulletin 22:414-419.
Johnson, S., K. Bjorndal, and A. Bolten. 1996. Effects of organized turtle watches on loggerhead (Caretta caretta) nesting behavior and hatchling production in Florida. Conservation Biology 10:570-577.
Losey, G., G. Balazs, and L. Privitera. 1994. Cleaning symbiosis between the wrasse, Thalassoma dupery, and the green turtle, Chelonia mydas. Copeia 1994:684-690.
Lutcavage, M., P. Plotkin, B. Witherington, and P. Lutz. 1997. Human impacts on sea turtle survival. Pages 387-409 in P. Lutz and J. Musick, editors. The Biology of Sea Turtles. CRC Press, Boca Raton, FL. 432 pp.
Mellgren, R., and M. Mann. 2000. Do green sea turtles learn about foraging from conspecifics? Proceedings of the international symposium on sea turtle biology and conservation 19:6-7.
Mortimer, J. 2000. Sea turtles in the Republic of Seychelles: an emerging conservation success story. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 18:24-27.
Murakawa, S., G. Balazs, D. Ellis, S. Hau, and S. Eames. 2000. Trends in fibropapillomatosis among green turtles stranded in the Hawaiian Islands, 1982-98. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 19:239-241.
Rebelo, T. 1994. Evaluating the possibility of making turtle watching an ecotourist attraction. University of Hawaii, Manoa. Marine Option Program. 33 pp.
Rice, M., G. Balazs, L. Hallacher, W. Dudley, G. Watson, K. Krusell, and B. Larson. 2000. Diving, basking, and foraging patterns of a sub-adult green turtle at Punalu`u, Hawaii. Proceedings of the International Symposium on Sea Turtle Biology and Conservation 18:229-231.
Rillero, A. 1999. The return of Kauila. National Wildlife, June/July, p. 40-47.
State of Hawaii. 2001. Summary of 2000 visitors to Hawaii. Department of Business, Economic Development & Tourism. http://www.hawaii.gov/dbedt/00vrr/index.html. Accessed 16 May 2002.
US Fish and Wildlife Service. 2001. The Endangered Species Act of 1973. http://endangered.fws.gov/esa.html#Lnk03. Accessed 20 May 2002.
Whittow, G., and G. Balazs. 1982. Basking behavior of the Hawaiian green turtle (Chelonia mydas). Pacific Science 36:129-139.
Work, T., and G. Balazs. 1998. Cause of green turtle (Chelonia mydas) morbidity and mortality in Hawaii. Proceedings of the Annual Symposium on Sea Turtle Biology and Conservation 17:291-292.
Robert H. Schmidt
Department of Environment and Society
Utah State University
Logan UT 84322-5215
June, 2002 (and rediscovered in 2022)