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1 This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier s archiving and manuscript policies are encouraged to visit:
2 Journal of Experimental Marine Biology and Ecology 381 (2009) Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: Changes in diving behaviour during the internesting period by green turtles Cheng I-Jiunn Institute of Marine Biology, National Taiwan Ocean University, Keelung , Taiwan, ROC article info abstract Article history: Received 18 June 2009 Received in revised form 31 August 2009 Accepted 31 August 2009 Keywords: Biotelemetry Green turtle Reproduction Resting dive U-dive Wan-an Island Time-depth-recorders were used to determine the contribution of U-dives in 5 green turtles (Chelonia mydas) during the internesting interval at Wan-an Island, Penghu Archipelago, Taiwan in 2004 and All turtles had a high incidence of long U-dives (dive duration up to 68 min), characterized by constant bottom depth that indicated turtles residing on the seabed. In many cases, these U-dives were inferred to serve a resting function. While there were differences in the incidence of U-dives among individuals, a consistent feature was that U-dive frequency and depth decreased in the days immediately preceding their nesting event. This pattern suggests that preparation for the subsequent nesting event may be a normal process. This observation seems to occur widely among sea turtle species Elsevier B.V. All rights reserved. 1. Introduction Sea turtles only emerge on beaches to nest, or in some cases to bask (Whittow and Balazs, 1982). Consequently, there has been considerable effort in recent decades to develop techniques to record the free-living behaviour of turtles at sea (e.g. Hays, 2008). During the internesting interval, sea turtles perform various diving patterns for different purposes (Sakamoto et al., 1993; Hochscheid et al., 1999; Hays et al., 2000a; Houghton et al., 2002, 2008; Rice and Balazs, 2008). In some cases, evidence from dive patterns suggests that turtles forage where food is available (e.g. Houghton et al., 2008). In other cases, turtles seem to spend long periods resting on the seafloor where food is absent, particularly at night (Hays et al., 2000b; Storch et al., 2005). As well as this broad dichotomy between feeding and resting, there may be other key behaviours performed during the breeding season (Schofield et al. 2006). For example, loggerhead turtles in Greece actively search out warm water in semi-enclosed bays, presumably to raise their body temperature and metabolic rate, allowing faster egg maturation prior to oviposition (Schofield et al., 2009a). Among the various dive trajectories that have been recorded for sea turtles, the U-dive is often the predominant one, accounting for up to 46% of all dives (Hochscheid et al., 1999). For some populations, this dive type has been suggested to serve a resting function to minimize energy expenditure and maximize reproductive output (Hays et al., 2000b; Houghton et al., 2008; Minanikawa et al., 2000; Reina et al., 2005). Elsewhere, it has been suggested that not all U-dives are for resting, as evidenced by movement during the bottom phase of these dives. The erratic bottom profile of Tel.: x5303; fax: address: b0107@mail.ntou.edu.tw. such U-dives indicates that the turtles might perform other activities such as feeding, or slow movement along the seabed (Hochscheid et al., 1999; Houghton et al., 2002). Similarly a carapace-mounted video camera system (Crittercam) showed that green turtles performed three different foraging strategies during the internesting interval, suggesting that not all U-dives were resting dives (Seminoff et al., 2006). These results suggest that the variation in depth readings during the bottom phase of U-dives may provide a crude proxy for the extent of benthic resting. In addition to different extents of benthic resting among populations as related to food availability, patterns of activity also may change during internesting periods. In short, several populations of sea turtles change their diving behaviour in the days preceding nesting, which may be related to selection the nesting-beach (Hays et al., 1991, 1999; Houghton et al., 2008). Because of the central role of diving in sea turtle ecology, I recorded the diving behaviour of green turtles at a nesting ground in Taiwan. I objectively assessed the extent of the variation in the bottom phase of U-dives, from which I inferred dive function (e.g. rest vs. activity). Then, I examined if turtles in this population conformed to the emerging general paradigm of increased activity as nesting events approached. 2. Materials and methods 2.1. Nesting events on Wan-an Island Wan-an ( N, E) Island is approximately 7.4 km 2 in area and located in the southern Penghu Archipelago about 18mi from Penghu Island (Fig. 1) off the coast of Taiwan. The total length of the green turtle nesting beach is about 4 km (Chen and Cheng, 1995; Cheng, 2006). Green turtles have a discrete nesting season on this island from the beginning of May until the end of October. Turtles made an average /$ see front matter 2009 Elsevier B.V. All rights reserved. doi: /j.jembe
3 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) Fig. 1. Bathymetry map around Wan-an Island, Penghu Archipelago, Taiwan, with an insert of Wan-an Island. Nesting beaches are labeled A to I. Map of Penghu Archipelago from the Maptool program of 30 nests annually, ranging from 9 to 55 nests; the average clutch size was 107 eggs (82 to 126 eggs per clutch; Cheng, unpublished data). Five TDRs (time-depth recorder; Model MK-9, Wildlife Computers, Inc.) were deployed on gravid green turtles on Wan-an Island during the nesting season in 2004 and I tracked 3 turtles in 2004, 2 for 1 internesting interval each and 1 for 2 internesting intervals, and 2 turtles in 2005 for 1 internesting interval each. All turtles were tagged after they laid at least one clutch (Table 1). The monitored turtles in 2004 were Table 1 The size, the first and last nesting dates, the maximum and minimum water temperatures during the internesting interval, deployment and recovery dates as well as internesting interval of the turtles tagged with TDR that nested on Wan-an Island, Penghu Archipelago, Taiwan in 2004 and Year Turtle code Size (cm) First Last Deployment Recovery Temperature ( C) nesting nesting date date SCL a CCL a Min Max date date 2004 A Jun 3-Sep 6-Jul 19-Jul B Jul 10-Sep 28-Jul 11-Aug C Aug 18-Sep 20-Aug 3-Sep C-2 a Aug 18-Sep 4-Sep 18-Sep Jun 4-Sep 22-Jul 4-Aug Jul 20-Sep 8-Aug 22-Aug Turtle C-2 is the same animal as C-1 on subsequent TDR deployment. a SCL; straight carapace length, CCL; curved carapace length. Internesting interval (day)
4 20 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) coded as A, B, and C. The diving data of turtle C was downloaded after she laid her third clutch without removing the tag. Thus, the consecutive 2-dive cycles obtained from this turtle were separated by C-1 and C-2 respectively. The tagged turtles in 2005 were coded as 1 and 2. The temperature loggers on the TDRs were not calibrated against each other; therefore, possible differences in temperature readings among TDRs were not determined. Turtles 2004-A, 2004-C1 and -C2, and turtle were captured for TDR deployment on Beach A, turtle 2004-B on Beach H, and turtle on Beach C (Fig. 1). In total, diving was recorded over 6 temporally different internesting intervals. Air temperature from 1 July to 23 September in both 2004 and 2005 ranged from 25.1 to 29.6 C (Fig. 2); no significant difference was found between two years (paired t-test; p=0.791, n=85). Thus, while each turtle was studied during a different internesting interval, in fact the datasets are comparable. Carapace size, the first and last nesting dates, the maximum and minimum water temperature during the internesting interval, the tag deployment and recovery dates, and the internesting interval of each turtle are listed in Table 1. Each tag was programmed to record depth (range 0 to 100 m, resolution 0.5 m) and temperature (range 20 to +35 C, resolution 0.5 C). In 2004, one TDR (turtle 2004-A) was set to record both parameters every 5 s; all other TDRs were set to record every 1 s. A dive was defined as when the depth was below 2 m, the vertical speed faster than 0.03 ms 1, and the dive lasting more than 30 s (Hochscheid et al., 1999; Houghton et al., 2002). A U-dive was determined when the turtle dove to a fixed depth, remained there for a long period, and had a steep ascent phase (Hays et al., 2000a; Houghton et al., 2002). A turtle made a resting dive when stationary at a fixed depth for an extended period of time. Furthermore, animals remained motionless or moved very little during resting dives. This would result in a low standard deviation (s.d.) in the depths during the bottom profile. In contrast, animals performing active dives tended to move more and stay at a specific depth for a short period of time. This would result in an erratic bottom profile with a high s.d. in the depths during the bottom phase. Fig. 3. Standard deviation (s.d.) of the bottom depth profile vs. diving interval of A U-dive of one green sea turtle. The rectangle represents the upper and lower limits of the diving interval and of the s.d. of the bottom profile for the resting dives. In this study, both resting and active dives occurred in the U-dive profiles (Fig. 4a, b). The dive duration at maximum dive depth of each U- dive of 5 turtles showed that the turtles in 2005 dove to shallower depths than did the turtles in 2004 (Fig. 5). Turtles in 2005 spent more time at maximum depths of 10 to 13 m (Fig. 5e, f). Turtles in 2004 spent more time at maximum depths of 16 to 20 m or deeper (Fig. 5a d). Turtles in 2004 also had a much wider range of dive depths than in Furthermore, data indicated that turtles first conducted shallow dives 3. Results The standard deviation (s.d.) of the depth green turtles occupied during the bottom phase of a U-dive and the duration at depth were used to determine whether turtles were resting (low s.d.) or active (high s.d.) during the dive (Fig. 3). The majority of U-dives were resting dives, of which 55% lasted for more than 30 min. Resting dives were categorized as long dives with small s.d. in bottom depth (points in the rectangle, Fig. 3). Points with large s.d. in bottom depth and/or short dive duration were categorized as active dives. Fig. 2. Air temperature on Wan-an Island during 1 July and 23 September in 2005 and Fig. 4. U-dive profiles that were classified as (a) resting dive, and (b) active dive during the internesting interval of green sea turtles in Taiwan.
5 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) Fig. 5. Dive duration vs. maximum dive depth of 5 green sea turtles during their internesting intervals; (a) 2004-A, (b) 2004-B, (c) 2004-C1, (d) 2004-C2, (e) , and (f) turtles that nested on Wan-an Island, Penghu Archipelago, Taiwan C1 and C2 are the same turtles during different internesting intervals. after nesting, with dives becoming deeper and then shallow again close to the next nesting event. In total, dive duration (min) increased linearly with the maximum dive depth (m) according the following equation [(duration)= (maximum depth); n=2255, r=0.37, p<0.001]. Individual turtles experienced very consistent temperatures, with overall temperature ranges of 0.01 to C during monitoring periods during internesting intervals of 14 to 15 days; however, there was as much as a 2.42 C difference in temperature recorded among individuals. Because 2004-C1 and -C2 were the same turtle using the same logger, this may not be due to a seasonal difference but a change in location or depth used (Table 1). The green sea turtles usually showed a diel variation in the incidence of resting dives (Fig. 6). In spite of high variation among turtles, they appeared to spend more time resting at night. There was a significant diel difference in the incidence of resting dives (data were arcsine-transformed, p =0.033, df=143, one-way ANOVA). Tukey HSD pair-wise tests between any 2h in a day showed that animals spent less time resting from 08:00 to 19:00 than 02:00 and from 12:00 to 19:00 than 04:00 (p=0.02 to 0.04 for all comparisons). All turtles decreased their proportion of U-dives 4 to 5 days prior to nest (Fig. 7). Meanwhile, the proportion of shallow dives increased substantially in most cases. Statistical analysis showed that there was a significant difference in the proportion of daily U-dives during the internesting interval (one-way ANOVA, p=0.001, df=89). Tukey HSD test showed that the U-dives were significantly fewer during the last
6 22 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) Fig. 6. Diel differences in the percentages of U-dives classified as resting dives for 5 green sea turtles during their internesting intervals in 2004 and two days than during the other days (p=0.04 to 0.001). There were fewer U-dives on day 13 than on days 8 to 10 (p=0.02 to 0.04). 4. Discussion The U-dive pattern of 5 turtles monitored over 6 internesting intervals showed that even though the depths of most of the bottom profiles had low standard deviations (s.d.) (e.g. Fig. 4a), the shorter dives tended to be shallower and had higher s.d. (e.g. Fig. 4b). This suggests that the turtles performed activities other than resting during the shorter U-dives. Because U-dives were the predominant dive type in most cases, with average values ranging from 44 to 56% of all dives, the relatively shallow depths and short durations of U-dives with high s.d. in the bottom depth profile can be considered as an active dive, i.e. animals were engaged in searching, travelling, feeding, and so forth (Blumenthal et al., 2009). This conclusion is supported by a carapace-mounted video camera (Crittercam) study (Seminoff et al., 2006). Turtles usually performed resting dives at a certain depth. Hays et al. (2000b) found that the depth of neural buoyancy for the green turtles is around 19 m. In this study, green turtles on Wan-an Island were more likely to use depths >18 m in 2004 and <18 m in 2005 (Fig. 5). Although the TDRs used in this study were unable to determine the locations of the turtles during their internesting intervals, as can the recently developed GPS transmitters (e.g. Rutz and Hays, 2009; Schofield et al., 2009b), the bathymetry map around Wan-an Island (Fig. 1) showed that the water to the west and south of the island is shallower than to the east. In 2004, turtles reached depths of close to 40 m, which means they would be utilizing
7 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) Fig. 7. Changes in the U-dives throughout the internesting intervals of 5 green turtles on Wan-an Island, Penghu Archipelago, Taiwan. the north or east of the island, because bottom depths are shallower than 40 m on the west and south sides of the island. In 2005, the turtles could have used any area around the island. Dive duration tended to increase with dive depth, presumably because of the increase in oxygen storage with larger lung (Minanikawa et al., 1997; Hochscheid et al., 2003; Hays et al., 2004a,b). A similar result was found in this study. Green turtles experienced 25 to 27.5 C water temperature most of the time during the internesting intervals in this study. These values correlated to the relationship found by Hays et al. (2002), whereby higher sea temperatures relate to shorter internesting intervals which is similar to the green turtles breeding at Cyprus and Ascension Islands. This is because water temperature strongly influences the body temperature (Sato et al., 1995), and consequently, the clutch development during the internesting interval. The non-significant relationship between the water temperatures and the length of internesting intervals found for the green turtles nesting on Wan-an Island suggested that there was little behavioural thermoregulation there. Many studies have suggested that sea turtles are more active during the daytime, but less active or resting at night (Eckert et al., 1986; vandam and Diez, 1996; Gitschlag, 1996; Hays et al., 2000b; Storch et al., 2005; Rice and Balazs, 2008; Blumenthal et al., 2009). Similar results were found in this study; turtles were more active during the daytime than the night, especially at the beginning of the day (Fig. 6). Thus, the turtles might spend more time at rest during the night to save energy, which is important to the female turtles during the internesting interval (Minanikawa et al., 2000; Houghton et al., 2002; Storch et al., 2005; Houghton et al., 2008; Blumenthal et al., 2009). The proportion of U-dives serving as rest for each turtle fluctuated on a daily basis (Fig. 7). This suggests that the female green turtles nesting on Wan-an Island
8 24 C. I-Jiunn / Journal of Experimental Marine Biology and Ecology 381 (2009) have no finite rest pattern during their internesting interval. In shallow waters with extensive coral reefs as in Penghu waters (Dai, 1991), turtles might not necessarily rest on the seabed at night. The application of IMASEN (Inter-Mandibula Angle Sensor) will be able to determine the diving behaviour of gravid females during the internesting interval, as used by Houghton et al. (2008) at Seychelles. All turtles decreased their U-dives 4 to 5days before the subsequent nesting event (Fig. 7). At the same time, the proportion of shallow dives increased substantially in most cases. In three cases (turtles 2004-B, 2004-C1 and 2004-C2), turtles stopped resting during the last day of the internesting interval. Statistical analysis showed that turtles decreased their U-dives 3days before the subsequent nesting event. Thus, the animals might increase their activities during this period to search for the correct beach for nesting; field records of both years showed that all but one turtle (2005-2) nested on the same nesting beach as it had previously, and turtle nested on the neighboring beach. There are 6 nesting beaches on Wan-an Island on the west and south sides of the island separated from each other by rocky outcrops (Wang and Cheng, 1999). Green turtles are known to have high nest site fidelity, even to the same beach (Allard et al., 1994; Mortimer and Porter, 1999). Thus, the turtles might decrease their resting dives and spent last few days conducting extensive shallow dives to find the previous nesting beach. The patrol team spotted the turtles swimming in the nearshore waters 1 to 2days before nesting. This presents further evidence of strong natal homing by green sea turtles. In this study, green turtles that nested on Wan-an Island made U-dives over long periods with consistent bottom phases during their internesting intervals, presumably to rest on the seabed. Furthermore, there was also no finite resting dive pattern among turtles during their internesting intervals, even within the same turtle (e.g C). Despite this difference, all turtles decreased their U-dives a few days prior to the subsequent nesting event. This might be related to the active searching behaviour for their previously-used nesting beach. Acknowledgements The author thanks Ms. S-C Kuo, Mr. M-D Chang, Mr. J-S, Hwang, Mr. J-L Chen and volunteers for the field assistance. The administrative assistance provided by the Penghu County Government was highly appreciated. This study is supported by grants from Penghu County Government (No. 98H32402), National Science Council (NSC m ) and I-Mei Environmental Protection Foundation. 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