Twenty-three Years of Sea Turtle Stranding/ bycatch Research in Taiwan

© 2019 Academia Sinica, Taiwan Open Access Twenty-three Years of Sea Turtle Stranding/ bycatch Research in Taiwan I-Jiunn Cheng*, Hua-Yan Wang, Wen-Yi Hsieh, and Yin-Ting Chan Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwan. *Correspondence: [email protected] Received 30 April 2019 / Accepted 4 December 2019 / Published 19 December 2019 Communicated by Benny K.K. Chan Coastal sea turtle stranding and bycatch are common phenomena worldwide and have received more attention in recent years. They are caused by both natural and anthropogenic factors. One thousand and seventy-two turtles were reported to be victims of these phenomena from March 1997 to November 2019 in Taiwan. Number of stranding/bycatch were variable and infrequent for the first 14 years, but increased each year after 2012 and peaked in 2019 with 217 cases. Most turtles were juveniles to subadults. All five of Taiwan’s species were reported in stranding and bycatch records, and the green turtle was reported the most common. The main reported seasons lasted from winter to spring, when the weather changes dramatically. The sex ratio (female: male) ranged from 7 in the hawksbill turtle to 0.7 in the olive ridley, with an average of 2.4 for all species. Green turtles were the dominant stranded species, and more loggerhead turtles were by-caught. The hotspots were the towns of Dougou and Tochen in Yilan County, and Gongliao District in New Taipei City, located in NE coast of Taiwan respectively. Stranding was the more common of the two phenomena reported, and 80% of all stranded turtles were subadult green turtles. Eighty percent of all stranded/bycaught turtles were dead. Pond-nets were the fishing gear that accounted for the most bycatch, and captured mainly living young and subadult green turtles as well as subadult loggerhead turtles. The hotspots for bycatch were the towns of Dongou and Tochen in Yilan County. The Coast Guard and concerned citizen were the main sources of reports. This is the first study to analyze the long-term stranding/bycatch of sea turtles in Taiwan. Key words: Stranding and bycatch, Green turtle, Temporal and spatial distribution, Report type, Bycatch type, Gender, Juvenile to subadult turtles. BACKGROUND Coastal sea turtle stranding/bycatch is a common phenomenon worldwide and a burning issue in marine conservation (Hamann et al. 2010). It can be caused by anthropogenic activities such as debris ingestion (Schuyler et al. 2014 2015; Stacy et al. 2018), coastal pollution (Barbieri 2009; Clucky et al. 2017; Gardner et al. 2006), boat strike (Denkinger et al. 2013; Lester et al. 2013), fishery bycatch (Koch et al. 2013; Moriya 2010; Nicolau et al. 2016; Tomás et al. 2008), and ghost net entanglement (Wilcox et al. 2013 2014). It can also be caused by natural occurrences such as disease (Orós et al. 2005), weather conditions (e.g., cold stunned, extreme weather) (Flint et al. 2017; Innis et al. 2007; Witherington and Ehrhart 1989), and shark bite (Bornatowski et al. 2012; Poli et al. 2014; Chaloupka et al. 2008). Both factors can result in the turtle either being stranded ashore or drifting in the oceans (Flint et al. 2015; Poli et al. 2014). Stranded and bycaught turtles will die unless they are rescue and rehabilitated. In order to improve the viability of live turtles and determine the possible causes of death, it is necessary to strengthen the sea turtle stranding/bycatch network (Baker et al. 2015; Ullmann and Stachowitsch 2015). The stranding/bycatch network can provide Citation: Cheng IJ, Wang HY, Hsieh WY, Chan YT. 2019. Twenty-three years of sea turtle stranding/bycatch research in Taiwan. Zool Stud 58:44. doi:10.6620/ZS.2019.58-44. Zoological Studies 58: 44 (2019) doi:10.6620/ZS.2019.58-44 1 © 2019 Academia Sinica, Taiwan information such as species and size compositions, temporal and spatial distribution, stranding hotspots, gender, and stranding types. Long-term records thus provide important demography information on sea turtles in the nearshore waters, and help develop management strategies and assess the impact of global climate change (Flint et al. 2017; Still et al. 2005; Stacy et al. 2018). There are five species of sea turtles in Taiwan: green, loggerhead, hawksbill, olive ridley, and leatherback (Chen and Cheng 1995). All can be found stranded or by-caught along the coast. The purpose of this study was to analyze the data collected from stranding and bycatch in Taiwan from March 1997 to November 2019 to determine the trends and possible causes of stranding/bycatch. MATERIALS AND METHODS Sample collection and data processing Upon received a phone call from Coast Guards, concerned citizens or county official regarding turtle stranding or by-catchment, photos of the turtle were collected for species identification and body condition assessment. The curved carapace length (CCL) was also used as an indication for size. Furthermore, the stranding and bycatch site and type of stranding (drift, stranded ashore, fisheries bycatch, etc.) were also requested. Case reports were separated into fisheries bycatch, drift, stranded and miscellaneous. Drift is defined as a turtle, dead or alive, floating on the surface water and drifting passively. Stranded is defined as a turtle found on the seaside, and if alive, motionless. Fisheries bycatch is defined as a turtle caught unintentionally by a fishing gear. Miscellaneous was defined here by other methods, such as coastal fish ponds, seized during illegal trading, etc. Due to the fact that sea turtles can be bycaught by more than one gear type, fisheries bycatch is further separated into pond-net, drift net, trawl, hooks/longlines, and undetermined gear types, based on the major coastal fishing gears in Taiwan. The hook/ longline is used for both sport fishing and commercial longline fishing, and represented here as line. The unidentified type includes those that failed to report the type of fishing gear. For turtles that died or starting decomposing (e.g., lost its head or flipper, swollen, or remains of carapace and bone), the person who reported the case, the Coast Guard in most cases, was asked to take photos, measure the body length (curved carapace length), and bury the body at the scene. When the carcass appeared intact, even with minor injuries, a team from the corresponding author’s laboratory was sent to perform necropsy at the scene to determine the possible causes of death. We also measured the CCL and determined the gender using the gross morphology of the sex organ with trained personnel. The maturity status was determined by the external morphology of the tail and overall size described in Eckert (1993). For live turtles, when the animal was in good health and had excellent body conditions – such as good gross morphology, minor injuries, vigorous responses (such as flippers beating, crawling, diving, response to eye poke, etc.), photos from whole body, front, rear, and both sides were taken, body length was measured, and a biopsy of the skin tissue was sampled, stored in an ethanol preserve solution for a population genetic study. The turtle was released back to the sea at the same location where it was found under the supervision of the county authorities. When a turtle was determined to not be in excellent condition, i.e., it was injured and did not respond to body contact, it was sent to veterinarians for clinical inspection. Turtle rehabilitation was carried out under the cooperation of the research team and veterinarians. If the turtle died during the rehabilitation, a necropsy was carried out by the veterinarians. Turtles that were rehabilitated were released back into the sea under the supervision of the same county authorities. The treatment for reported stranding in Taiwan was divided in the northern and southern regions. The northern region ranged Hualien County in eastern Taiwan to Miaoli or even Taichung County in western Taiwan, and the southern region ranged from Taitung County in eastern Taiwan to Changhua County in western Taiwan (Fig. 1). The corresponding authors’ laboratory – Marine Ecology and Conservation laboratory of the National Taiwan Ocean University – is responsible for the stranding/bycatch in northern Taiwan, and the National Museum of Marine Biology and Aquarium in Kenting region, Pintung County, Taiwan is responsible for the reports in southern Taiwan. In northern Taiwan, the research team carried out both necropsy and rehabilitation works. We cooperated with veterinarians from the School of Veterinary Medicine, National Taiwan University to rehabilitate the sea turtles. In southern Taiwan, only the living turtles are accepted for rehabilitation. Dead turtles were buried at the scene. However, when analyzing the reported data for the whole of Taiwan, the reports from southern region were also included. Statistical analysis Two-way ANOVA was used to determine the differences in gear or report type for each species on a yearly basis. One-way ANOVA was used to determine the yearly differences in gear or report type among five page 2 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan species (Sokal and Rholf 1982). RESULTS Reports A total of 1072 turtles from all around Taiwan were reported from March 1997 to November 2019. The yearly variation showed that (Fig. 2) the number of reports were variable and low over the first 14 years (i.e., from 0 to fewer than 5 reports in some years), then increased sharply after 2012 until peaking in 2019 at 217 cases. All five species were reported. The most common species was the green turtle (83%), followed by the hawksbills (7%), loggerheads (7%), olive ridleys (2%) and leatherbacks (0.6%; Fig. 3). Size The majority of turtles ranged from 35 to 55 cm CCL, representing juveniles to subadults (Fig. 4). The majority of green turtles were also 35 to 55 cm CCL, representing juveniles to subadults. There was no shift in range between the first 10 years (1997 to 2007) and the last 10 years (2009 to 2019), except the size range was wider for the last 10 years (25.5 to 110 cm for the first 10 years, 4.5 to 125 cm for the last 10 years). The majority of hawksbill turtles were 20-35 cm CCL and all were young juveniles. There was also no shift in range between the first 10 years (1997 to 2007) and the last 10 years (2009 to 2019), except the size range was wider for the last 10 years (28 to 54 cm for the first 10 years, 8.8 to 84 cm for the last 10 years). The loggerhead turtles, on the other hand, ranged from 65-85 cm CCL, and included only subadults. Again, there was also no shift in range between the first 10 years (1997 to 2007) and the last 10 years (2009 to 2019), except the size range was wider for the last 10 years (69 to 86 cm for the first 10 years, 51.5 to 110 cm for the last 10 years). The numbers of olive ridley and leatherback individuals were too low to determine major size ranges (Fig. 4). Sex ratio Due to the fact that no necropsy was carried out in southern region of Taiwan, the sex ratio of sea turtles was determined only based on the data from northern Taiwan. The results showed that the sex ratio (female: male) ranged from 7 in hawksbills to 0.7 in Fig. 1. Map of Taiwan marked with the location of each county. The two thick lines shows the separate between the surveys of northern from southern Taiwan. See text for explanation. Taipei City Keelung Taoyuan New Taipei Hsinchu Yilan Miaoli Taichung Changhua Nantou Chiayi Tainan Taitung km 0 72 Pingtung Hualien Yunlin Kaohsiung page 3 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan olive ridleys (Table 1). The sex ratio was not available for the leatherback turtle because only one individual was collected. The very high and very low ratios might relate to the low sample size (n < 7). Season Over the 23 years the study was conduct, 9-12% of the total records were made from December to April and 4-8% were made from May to November, suggesting the majority of stranded/bycatch turtles were reported during the seasons when the weather changes dramatically (Fig. 5). The average air temperature for the time period ranged from 18℃ in January to 21℃ in March. Air temperature was 20℃ in December and 23℃ in April. Average air temperature ranged from 23 to 28℃ from May to November (Central Weather Bureau 1997 to 2019). Green, hawksbill, and loggerhead turtle stranding/bycatch were most prevalent from December to April, which is close to the peak months of Fig. 2 Number of yearly stranded/bycaught turtles from 1997 to 2019 in Taiwan. Fig. 3 Percentage of each species of sea turtle in the total stranding/bycatch records. page 4 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan stranding/bycatch for these turtles. The number of olive ridley and leatherback turtles was too low to determine their major stranding seasons. Spatial distribution Sea turtles were found stranded/bycaught in every coastal county in Taiwan. The Northern coast includes Keelung City, New Taipei City, Taoyuan County, Hsinchu County, Miaoli County. The northeast coast includes Yilan County. The eastern coast includes Hualien County and Taitung County. The west coast includes Taichung County, Yunlin County, Chiayi County. The southern coast includes Tainan County, Kaohsiung City and Pingtung County. The outlying island in the Taiwan Strait includes Penghu County, Kinmen County and Lianjang County. Of all the counties, New Taipei City and Yilan County had the highest records (Fig. 6). Green turtles were most abundant in New Taipei City, Yilan County and Penghu County. The most loggerhead turtles were found in Yilan County. Most hawksbill turtles were found in Penghu County, while the records of the olive ridleys and leatherbacks were too low to determine the highest record sites (Fig. 6). Strandings, drift and by-catch in fishrey activities This study identified four major types of reports: bycatch, drift, stranding, and miscellaneous. Among four types, stranding was the most abundant (57%), followed by bycatch (28%), then drift (13%), and miscellaneous (6%, Fig. 7). One-way ANOVA showed that more reports were from green than from olive ridley turtles (p = 0.007). Eighty percent of all reports were carcasses. Ninety-three percent of the stranded individuals were immature (35 to 55 cm CCL) female green turtles. The main stranding season was from winter to spring (December to April). The highest record Fig. 4 Number of stranded/salvaged turtles of different size range of the total and of each species from 1997 to 2019 in Taiwan. Table 1. Sex ratio (female: male) of the five species of sea turtle Species Sex ratio Green 2.3 Loggerheads 4 Olive ridleys 0.7 Hawksbills 7 Leatherbacks NA* Total 2.4 *: No data available. page 5 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan Fig. 6. Number of stranded/bycaught turtles in different counties of the total and of each species from 1997 to 2019 in Taiwan. The region of each county belongs are underlined with thick line. Keelung N. Taipei Taoyuan Hsinchu Miaoli Taichung Changhua Yunlin Chiayi Tainan Kaohsiung Pingtung Taitung Hualien Yilian Penghu Kinmen Lianjiang Fig. 5 Monthly changes in stranding/bycatch turtles from 2015 to 2019 in Taiwan. Data of total and each species showed in mean and standard deviation, and n = 60. Jan Feb March April May June July Aug Sept Oct Nov Dec Number of stranding/bycatch 0 5 10 15 20 25 30 35 total greens loggerhead olive ridley hawksbill leatherback Number of record 300 250 200 150 100 50 0 page 6 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan was in New Taipei City (25%), with the hotspot in Gongliao District (Fig. 8), located at the base of Mo-O Bay, northeast corner of Taiwan. For the drift report, 74% were immature (35 to 55 cm CCL) female green turtles and 57% were carcasses. The most reports were made in December and mainly occurred in New Taipei City, northern Taiwan and Penghu County, the outlying island in the Taiwan Strait. Two-way ANOVA on different report types and different years (Table S1) showed that, for green turtles, the most reports were from stranding (p < 0.01), there were more reports from 2019 than from 1997 and 1999 to 2012 (p < 0.01). For loggerhead turtle, more reports were from by-catch than from drift and miscellaneous (p < 0.001), and more report from 2019 than from 1997, 1999, 2000, 2001, 2006 and 2007 (p = 0.037). For olive ridley turtles, there was no difference among report types (p = 0.05), there were more reports from 2019 than from 1997 to 2007, 2009 to 2013 and 2015 (p < 0.001). For hawksbill turtle, the most reports were from stranding (p = 0.003). Even though there was a significant difference among years (p = 0.005), there was no difference among report types or years. No difference in both report types and among years for leatherback turtles (p = 0.265 for report type, p = 0.549 for years). One-way ANOVA among different species on the same report type showed that, for fishery bycatch, except loggerhead turtle, reports from green turtle were highest, and the loggerhead turtle was higher than the leatherback turtle (H = 42.948, d.f. = 4, p < 0.001). For the drift type, the green turtle was higher than the leatherback turtle (H = 17.905, d.f. = 4, p = 0.003). For the stranded type, the green turtle was higher than the olive ridley and leatherback turtles (H = 21.935, d.f. = 4, p < 0.001). For the miscellaneous type, there were significant differences among species. However, no difference was detected between any two species (H = 14.552, d.f. = 4, p = 0.006). Bycatch gear types Five major coastal fishing gear types were identified: pond nets, driftnets, trawlers, line, and undetermined. Among them, pond nets were the most prevalent, accounting for 49% of gear types, followed by the gillnet (12%) (Fig. 9). The other two fishing gears accounted for 6% or less of the reports. Undetermined contributed 28% of fishery bycatchment. Ninety-eight percent of pond net bycatch consisted of green (73%) and loggerhead (25%) turtles. All bycatch turtles were alive and most were immature. Two peak size ranges were identified: 35 to 45 cm CCL (juvenile) and 75 to 85 cm CCL (subadult). Eighty-five percent of driftnet bycatch consisted of green turtles, of which 70% were alive. All gillnet-caught turtles were immature (35 to 55 cm CCL). Two-way ANOVA on different gear types and years showed that (Table S2), for green turtles, more Report type bycatch drift stranding miscellenous Number of record 0 10 20 30 40 50 60 70 total greens loggerheads olive ridley hawksbill leatherback Fig. 7. Number of the total and each species of sea turtle for each report type in Taiwan from 1997 to 2019. Data on total and each species showed in mean and standard deviation, and n = 23. page 7 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan Fig. 8. Distribution of stranded/bycaught sea turtles in different districts in New Taipei City. Location of each coastal district in New Taipei City is showed in the upper right figure. Fig. 9. Number of the total and each species of sea turtle from bycatch by coastal fishing gears from 1997 to 2019 in Taiwan. Data on total and each species showed in mean and standard deviation, and n = 23. Gear type pond net drift net trwal line undetermine Number of records 0 2 4 6 8 10 12 14 total green loggerhead olive ridley hawksbill leatherback Bali Shanzhi Jinshan Wanli Ruifang Gongliao Linkuo Shimen Danshui page 8 of 14Zoological Studies 58: 44 (2019) © 2019 Academia Sinica, Taiwan reports were from pond net than from line or trawl (p = 0.003). Even though a significant yearly difference was found (p = 0.005), no difference was detected between any two years. For loggerhead turtles, more reports were from pond net than from other gear type (p < 0.001). No yearly difference was found (p = 0.547). For olive ridley turtles, there were no difference across gear types or years (p = 0.198 for gear type and p = 0.11 for year). Although no difference was found among gear types in both hawksbill and leatherback turtles (p = 0.061 for hawksbill turtle, p = 0.156 for leatherback turtle), there was significant difference among years for hawksbill turtle (p = 0.017). However, no difference was detected between any two years. There was no yearly difference for leatherback turtles (p = 0.509). One-way ANOVA among different species for the same gear type showed that, for the pond net, except the loggerhead turtle, the green turtle had the most reports than the other species (H = 42.948, d.f. = 4, p < 0.001). For the drift net, line and undetermined gears, even though significant different was found (H = 19.64, d.f. = 4, p < 0.001 for drift net, H = 13.121, d.f. = 4, p = 0.011 for the line, H = 14.607, d.f. = 4, p = 0.006 for undetermined gear), no difference was detected between any two species. No difference was found among species for the trawl (H = 8.773, d.f. = 4, p = 0.067). DISCUSSION In 1997, two green turtles with fibropapillomatosis were found in Tamsui District, New Taipei City, nothern coast of Taiwan. The turtles were then euthanized and necropsied by veterinarians. This case initiated the sea turtle stranding/bycatch works in Taiwan, and data have been collected ever since then. This study is the first long-term study of sea turtle stranding/bycatch conducted in Taiwan. Reports The variable and infrequent reports over the first 14 years was due to the long coastline, insufficient marine conservation awareness, lack of proper stranding/bycatch reporting system, and lack of proper coordination between the Coast Guard and local authorities. Flint et al. (2017) suggested that, in general, an increase in stranding reports indicates that the environment has changed. Corsini-Foka et al. (2013) suggested that this pattern can be explained by an increase in human activities. However, this do not seem to be the case in Taiwan. That the number of reports increased continuously and peaked in 2019 might be due to the increase in environmental awareness in recent years (e.g., more beach cleaning). In addition, the Forestry Bureau, Council of Agriculture, Executive Yuan initiated a sea turtle stranding/bycatch network in 2014, and the Coast Guard has actively participated in the system since then. In 2016, the cell phone social media application “LINE” (similar to Facebook) establish a “Sea Turtle Stranding Report Line Group.” This group allows members to edit and send photos, upload/ download videos to/from YouTube, and invite people to join the group. It speeds up the reporting process and provides useful hints from experts on how to treat sick, wounded, and dead turtles at the scene. The percentage strand/bycatch reported for each species is similar to those found in East Queensland, Australia (Flint et al. 2015), Japan (Moriya 2010), Brazil (Mascarenhas et al. 2005; Poli et al. 2014), and Turkey (Sönmez 2018, also see Sönmez 2019). The high number of reports of green turtles may simply be due to the fact that this species is most abundant in the nearshore waters of Taiwan (Cheng et al. 2008). Similar results were found in stranding and pond net reports. The higher reports of the olive ridley than the leatherback turtles was simply due to the low number of leatherback turtles reported. Size The majority of size ranges were juvenile to subadult, which were similar to those reported from Japan (40 to 60 cm CCL, Moriya 2010), Turkey (40 to 45 cm CCL, Sönmez 2018), Texas, USA (32.8 to 57.5 cm CCL, Shaver 1995), and Brazil (56.5 cm mean CCL, Mascarenhas et al. 2005; 31.5 to 56 cm CCL, Tourinho et al. 2010). The major size ranges of hawksbill and loggerhead turtles were similar to those reported from Texas, USA (Shaver 1995) and the western Mediterranean (Domènech et al. 2009). The difference in the size range suggests that the different species recruit to the coastal waters of Taiwan at different ages. Green and hawksbill turtles are recruited as juveniles, hawksbills are recruited younger, and loggerheads are recruited as subadults. There was no shift in the size range between 1997 to 2007 and 2009 to 2019 for the green hawksbill and loggerhead turtles, except that the number of reports increased during the second 10 year (47 vs. 842 turtles for green turtle, 4 vs. 71 turtles for hawksbill turtle, and 19 vs. 50 turtles for the loggerhead turtle). The wider size range was mainly due to more reports from 2009 to 2019 (1048 reports) compared to 1997 to 2017 (76 reports). Sex ratio The female:male sex ratio of the green turtles was 2.3 and the average of all turtles was 2.4. This suggests page 9 of 14Zoological Studies 58: 44 (2019)