Chelonian Conservation and Biology, 2010, 9(1): 8–17 g 2010 Chelonian Research Foundation The Development of Early Diving Behavior by Juvenile Flatback Sea (Natator depressus)

1 2 1 MICHAEL SALMON ,MARK HAMANN , AND JEANETTE WYNEKEN

1Department of Biological Sciences, Florida Atlantic University, Boca Raton, Florida 33426 USA [[email protected]; [email protected]]; 2School of Earth and Environmental Sciences, James Cook University, Townsville 4811, , [[email protected]]

ABSTRACT. – The flatback is the only of marine turtle that lacks an oceanic phase of development in its early life history. Instead, the turtles grow to maturity in shallow turbid shelf waters of tropical to subtropical Australia. We studied the development of diving behavior in neonate flatbacks to determine whether diving under those ecological conditions resulted in differences from leatherbacks (Dermochelys coriacea) and green turtles (Chelonia mydas) at the same age when diving in clear, deep oceanic waters. Data were obtained from flatbacks that varied in both age (1–7 weeks) and mass (38–100 g). Each turtle towed a miniature time–depth tag during a single 30-minute trial in shallow (# 12 m) turbid shelf waters near Townsville, Queensland, Australia. In total, 192 dives were recorded from 22 turtles from 4 nests. Most dives were short (, 100 seconds) and shallow (, 4 m), but even young turtles could dive to the bottom. The most common flatback dives had V- or W-profiles, whereas, in leatherbacks, most dives were V-profiles, and, in green turtles, the dives were either V- or U-profiles. Routine flatback dives were accomplished by swimming slowly (like leatherbacks), but, when sufficiently motivated, flatbacks could swim faster (. 1 m/s) than green turtles. They could also make repeated deep dives after surfacing only briefly to replenish their oxygen supply. Changes in performance (longer, shallower dives) were correlated with increases in mass but not age. We hypothesize that, as neonates, flatback dives enable the turtles to 1) search efficiently for prey throughout the water column under conditions of limited visibility, 2) minimize surface time so that even in murky water the turtles can return to previously attractive locations, and 3) swim rapidly to evade their predators.

KEY WORDS. – Reptilia; Testudines; ; Natator depressus; dive profiles; behavioral development; swimming; hatchling

Marine turtles are diving specialists that as larger phase of their development. This deficiency occurs juveniles and adults can submerge to depths and for because small turtles disperse over vast and largely durations that rival many marine mammals. Those diving unknown oceanic areas and, therefore, are unavailable for capabilities are the result of physiological (Kooyman study (Musick and Limpus 1997). Western Atlantic 1989; Lutcavage and Lutz 1997), morphological (Wyne- loggerheads (Caretta caretta) are the exception because ken 1997), and behavioral (Hays 2008) adaptations that for the first few weeks after they enter the sea, they can be together enable rapid gas exchange during typically brief found at ‘‘downwelling’’ sites adjacent to coastlines (Carr surface breathing episodes, enhanced mechanisms for 1987). Weeks to months later, they are transported oxygen storage and release, a streamlined body shape, and eastward by oceanic surface currents to ‘‘nursery’’ sites efficient propulsion (predominantly lift-based, ‘‘aquatic near the Azores, Canary Islands, and Madiera (Bolten flight’’; Wyneken 1997; Renous et al. 2008) during the 2003). But as small turtles, even surface-dwelling dive. Previous studies focused particularly on the dive loggerheads are difficult to locate and challenging to profiles of adult turtles, especially during long-distance observe while they reside in weed lines because they are migration between foraging sites and internesting behav- camouflaged and rarely move. This behavior probably ior near nesting beaches (Hays et al. 2006; James et al. promotes their survival as ‘‘float and wait’’ predators 2006; Rice and Balazs 2008) and by juvenile turtles (Witherington 2002) and also reduces their vulnerability foraging within circumscribed home ranges (van Dam and to predators. At this stage of development, diving in open Diez 1998; Seminoff et al. 2002; Makowski et al. 2006; water occurs infrequently. Seminoff and Jones 2006), where activity is typically These gaps in our knowledge are unfortunate because concentrated around important core areas (the best the survival strategies and associated adaptations of feeding and resting sites). young turtles in open water are certainly In contrast to the relative wealth of data available for important and probably differ from those shown by larger large juvenile and adult marine turtles, little is known juveniles and adults in coastal waters that are less about diving frequencies, functions of dives, or types of vulnerable to a smaller subset of predators. The behavior dive profiles shown by young juveniles during the oceanic of young turtles is also of interest from a developmental SALMON ET AL. — Flatback Turtle Diving Ontogeny 9 perspective. With an increase in size, young turtles are (streamlined body shape, large flippers) and vigorous likely to become more competent as swimmers and activity shown by flatbacks after entering the sea (Salmon divers, which enables them to change how (and where) et al. 2009), coupled with a high probability of they search for food, what kind of prey they select, and encountering predators (Walker 1991a) should select for how they defend themselves against predators. Unfortu- a turtle capable of (3) rapid and powerful swimming nately, we know virtually nothing about any of these movements. A similar prediction was made earlier by aspects of their behavior. Walker and Parmenter (1990), who speculated that How can this situation be remedied? One possibility neonate flatbacks would be more powerful swimmers is to carry out ‘‘staged’’ experiments, that is, to introduce than the neonates of other marine turtle species. young turtles of particular size or age classes into an open-water environment and observe what they do. METHODS Studies of this kind must be done with care because there is always the possibility that environmental conditions Turtles. — We reared 33 hatchlings (6–11 per nest will be inappropriate and result in behavioral artifacts. from 4 nests) obtained from a rookery in Mackay, However, small turtles seem amazingly impervious even Queensland, Australia (lat 21u089S, long 149u119E). to highly simplified and artificial laboratory conditions. In Turtles were captured during January and February, either fact, they behave in ways that seem consistent with what as they emerged naturally or from the sand column above little we know about their ecology in the open ocean (e.g., the hatched eggs during the late afternoon just before their orientation relative to locations in gyre currents, Lohmann evening emergence. Hatchlings were immediately placed et al. 1997; migratory activity, Wyneken and Salmon into covered buckets that contained a shallow layer of 1992; Witherington 1995). moist sand and were transported within a few hours to In one such study, Salmon et al. (2004) compared the screened outdoor pools located in the Marine and development of diving and feeding behavior between Aquaculture Research Facilities Unit on the campus of young leatherbacks and green turtles. The turtles were James Cook University, Townsville, Queenland, Australia reared in the laboratory and, at 2-week intervals, several (lat 19u159S, long 146u459E). Each turtle was isolated in a were released offshore in deep water for a single, brief rectangular plastic container (34 cm 3 24 cm 3 18 cm trial before they were released. Observers recorded deep) that was continuously supplied with filtered behavior associated with each dive while dive profile (recirculating) seawater. The turtles began feeding within data were stored on miniature time–depth recorders a day after capture. They were provided with an in-house (TDR) that the turtles towed. These studies showed that manufactured diet composed of ground fish, gelatin, the 2 species differed in the type and frequency of dive human infant formula, freshwater turtle food pellets, and profiles, fed on different prey, and as they developed, vitamins. The food was cut into small cubes that older leatherbacks made deeper dives whereas older green were dropped into the plastic containers; turtles dove to turtles made longer dives. These changes were apparent the bottom to consume the food (10%–15% of their body even over a relatively short (8–10 week) period of growth. weight daily). At capture and every 7–10 days thereafter, Here, we use similar methods to describe the diving we measured growth (straight-line carapace length [SCL]) behavior of young flatback turtles (Natator depressus) with vernier calipers (nearest 0.1 mm) and mass with an during the first 7 weeks of development. This species is of electronic scale (nearest 0.1 g). particular interest because, unlike other marine turtles, the Diving Trials. — Diving trials generally were carried hatchlings do not disperse into open oceanic waters; out during the morning and early afternoon to avoid late instead, they remain within the relatively shallow afternoon thunderstorms. A subset (n 5 22) of the 33 Australian continental shelf waters (Walker and Parmen- turtles we reared was used in these trials. Turtles were not ter 1990). Diving profiles of the adults were recently fed on the day of their trial. described (Sperling 2008), but no information is available Using a small boat, turtles were transported up to on the diving performance of neonates (defined by 12 km offshore to 1 of 6 sites located between Townsville Witherington [2002] as posthatchlings that have matured Port and Magnetic Island, or on the opposite (northwest- beyond the period of frenzied swimming). ern) side of Magnetic Island (Fig. 1). The turtles were We hypothesized that flatback dives, unlike those of kept in shaded buckets during transport. No more than 4 developing leatherbacks and green turtles in the open turtles from 2 clutches were tested on any one day. Each ocean, would (1) show few changes in profile, because the turtle was released after its trial. Water temperature at the turtles have little opportunity to vertically expand their surface varied between 29uC and 30uC and declined by no niche in shallow (coastal) waters. Flatbacks consume a more than one degree with depth. Depth at our trial sites variety of prey found at the surface, in the water column, ranged between 9.0 and 12.5 m. Our intent was to test the and on the bottom in turbid waters (Zangerl et al. 1988). turtles at regular (2-week) intervals. However, storms that We predicted that they would use (2) V- or W-shaped lasted for several days made it impossible to follow an dives to search for prey and detect predators over a wide exact schedule. We instead opted to test the turtles as swath in the vertical plane. Finally, the morphology weather permitted. 10 CHELONIAN CONSERVATION AND BIOLOGY, Volume 9, Number 1 – 2010

Figure 1. Inset, outline of Australia showing location of the Townsville area (square box) in northern Queensland. Below, the 7 testing sites where flatback diving trials took place. One site on the northwest side of Magnetic Island was used to avoid large waves generated by strong winds. Water depth varied between 9 and 12.5 m.

During trials, each turtle towed a Lotek miniature period, the turtle distanced itself from the boat approx- TDR (LTD 1100, 11 3 32 mm, sampling interval 5 imately 50 m. At this distance, the turtle gave no 14 seconds; LAT 1500, 11 3 35 mm, sampling inter- indication that it reacted to the presence of the boat. val 5 10 seconds), which we previously calibrated by The driver adjusted the boat’s forward progress to match submergence at 2-m increments to a maximum depth of that of the turtle so that this distance was maintained 12 m. TDRs were made slightly positive in buoyancy by during the entire 30-minute trial after acclimation. encasing them inside a thin foam covering shaped to Unfortunately, underwater visibility was severely restrict- minimize drag (Fig. 2). Slight positive buoyancy allowed ed (, 1 m), which made it impossible to directly observe the TDR to reach the surface (and mark the end of each how the turtles behaved during their dives. dive) near the time when the turtle surfaced to breathe but Data Analysis and Statistics. — Dive profiles (shape, also enabled the device to be easily submerged by the depth [m], and duration [seconds]) were measured from turtle during each dive. the TDR records and downloaded to a computer. A dive Each TDR was attached to the turtle by an was defined as any submergence to a depth $ 0.5 m. approximately 1-m length of light (2-kg test) monofila- Profiles were classified by using the criteria of Hoch- ment line threaded through the keratinous part of a scheid et al. (1999). supracaudal scute with a fine needle. If a predator took the Individual turtles varied considerably in growth rates. turtle, then this line broke to release the TDR. The TDR We divided the turtles into 2 groups to determine whether was attached by stronger (9-kg test monofilament) line to diving behavior changed most as a function of age or a plastic ‘‘handline’’ spool held by an observer at the mass. These were ‘‘younger’’ (# 3 weeks) and ‘‘older’’ front of the boat. This line was released as the turtle dove (4–7 weeks after emergence) turtles, and ‘‘small’’ and and retrieved while it was on the surface so that there was ‘‘large’’ turtles. Small turtles were those of any age whose always sufficient slack for the turtles to swim, dive, and mass at the time of their dive trial fell within the range surface without restriction or excessive drag. (38.0–62.4 g) shown by the turtles at the end of 1 week in Each trial began by gently releasing the turtle in the captivity. Large turtles were individuals that, during their water in front of the boat and by paying out sufficient dive trial, weighed between 63.0 and 100.2 g. (The latter slack to permit an initial, relatively long and deep was the heaviest turtle we used in our field trials.) ‘‘escape’’ dive. During an initial 5-minute acclimation Comparisons between the groups focused on possible SALMON ET AL. — Flatback Turtle Diving Ontogeny 11

Figure 2. Flatback with a time–depth recorder (TDR) at the surface between dives. Inset, flatback with TDR covered by a foam sheath used to make the device slightly positive in buoyancy. changes in dive-profile frequency, as well as changes in Dive Profiles. — Records were obtained for 192 dive depth and duration. Comparisons were made by dives by 22 turtles; one turtle swam vigorously but did not using the Fisher’s exact and x2 tests (the latter corrected dive (Table 1). Dives fell into 1 of 3 profiles: U, W, and V for continuity; Zar 1999). Swimming speeds (cm/s) were (Fig. 4). Profiles differed in their frequencies and in their estimated from the time it took the turtles on the surface spatio-temporal characteristics (Fig. 5). U-dives (n 5 11) to reach depth while performing the most common (V- shaped) dives. Comparisons between the swimming speeds of the different groups of turtles were made by using nonparametric (Kruskal-Wallis and Mann-Whitney; Zar 1999) tests. Time intervals between consecutive dives were estimated by the number of TDR readings at the surface multiplied by the recording interval (either once every 10 or 14 seconds) of the TDR. In all statistical tests, significance was set at p # 0.05.

RESULTS

Growth. — At capture, the turtles were (mean ± SD) 45.94 ± 6.77 g mean ± SD in mass and 6.66 ± 0.60 cm mean ± SD in SCL (n 5 33 turtles from 4 clutches). By the end of their first week in captivity, the turtles averaged 50.90 ± 4.41 g mean ± SD in mass (range, 38–62.4 g) and 7.09 ± 0.34 cm mean ± SD in SCL (Fig. 3). By 7 weeks Figure 3. Change in mass with age (days since nest emergence after emergence, they averaged 91.86 ± 8.38 g mean ± SD at 0) by 33 neonate flatbacks from 4 nests. The dives of 22 of in mass and 9.43 ± 0.34 cm mean ± SD in SCL (Fig. 3). these turtles were analyzed in this study. 12 CHELONIAN CONSERVATION AND BIOLOGY, Volume 9, Number 1 – 2010

Table 1. Number and profile of dives performed during 30- minute trials by the 22 flatbacks used in this study. The turtles were divided into 2 groups so that changes in diving behavior could be separately analyzed as a function of age (young turtles, numbers 1–11; older turtles, numbers 12–22) and mass (small turtles, 38–62.4 g, n 5 13; larger turtles, 63.0–100.2 g, n 5 9).

Turtle no. Mass (g) W-dives V-dives U-dives Total 1 42.8 1 8 4 13 2 46.2 5 6 1 12 3 46.6 0 5 0 5 4 38.0 0 1 0 1 5 44.6 0 0 0 0 6 53.0 3 2 1 6 7 50.1 2 5 1 8 8 48.8 4 5 1 10 9 67.8 5 6 0 11 10 64.3 8 1 0 9 11 62.2 2 1 0 3 12 89.5 6 2 2 10 13 72.5 1 5 0 6 14 73.5 2 8 0 10 15 63.8 1 5 1 7 16 62.4 1 6 0 7 17 65.5 2 1 0 3 18 60.1 0 20 0 20 19 59.9 5 27 0 32 20 62.1 1 6 0 7 21 100.2 1 5 0 6 22 78.4 1 5 0 6 Totals: 51 130 11 192 were least commonly performed (7 of the 21 diving turtles; Table 1). They were of short duration (80– 125 seconds) and, with one exception, shallow (# 4 m). W-dives (n 5 51) were more common (18 of 21 turtles) and spanned a broad range of durations (25–350 seconds) at typically shallow (# 4 m) depths. V-dives (n 5 130) were most commonly performed (21 turtles), typically of short duration (# 150 seconds), and spanned a broad depth range (0.5 to . 11 m). Two of the turtles in our study (turtles 18 and 19, Table 1), both from the same clutch and tested at the same location on the same day, performed more V-dives Figure 5. Depth vs. duration plots of the 3 dive types. U-dives (n 5 20, n 5 27, respectively) than any of their siblings were short and shallow; W and V dives were longer and deeper.

and all of the other older turtles combined. Their V-dives were also deeper and shorter in duration than those of the other turtles. For those reasons their V-dives are analyzed separately from the 83 V-dives of the other turtles. Changes in Dive Frequency and Profile During Development. — We found no statistical differences between small and large turtles, or between younger and older turtles, in diving frequency on a per turtle basis (77 dives by 12 smaller vs. 68 dives by 9 larger turtles, x2 5 0.03, not significant [n.s.]; 78 dives by 11 younger vs. 67 dives by 9 older turtles; x2 5 0.01, n.s.). Neither the small vs. large nor the younger vs. older turtles differed statistically in the proportion of W-dives (23 dives by the 12 small and 28 by 9 large turtles; x2 5 0.62, Figure 4. The 3 types of dive profiles (W, V, and U) shown by neonate flatbacks. These dives were made by turtle 8 at 3 weeks n.s.; 23 dives by the 11 younger and 30 by the 11 older after emergence. Time between marks 5 14 seconds. turtles; x2 5 0.24, n.s.), V-dives (45 by the small and 38 SALMON ET AL. — Flatback Turtle Diving Ontogeny 13

Figure 6. Depth vs. duration plots for groups of turtles differing in mass (above) and age (below). The V-dives of turtles 18 and 19 are excluded from these plots (and presented in Fig. 7). by the larger turtles; x2 5 0.04, n.s.; 40 by the younger Z 5 5.9, p , 0.0001). The mean and median descent and 43 by the older turtles; x2 5 0.09, n.s.), or U-dives (8 speeds shown by turtles 18 and 19 (Fig. 7) were small and 3 larger turtles; 8 younger and 3 older turtles) significantly faster (mean and median 53.5 and 54.0 cm/ that they performed. s, respectively) than those of the 2 mass subgroups Changes in Dive Duration and Depth During (Kruskal-Wallis H 5 95.11, p , 0.0001). Development. — The turtles of small mass (Fig. 6, upper graphs) made proportionally more deep ($ 4 m; 14 of 77) DISCUSSION dives than did the turtles of large mass (2 of 68; p , 0.003 by the Fisher’s exact test). However, the Characteristics of Neonate Flatback Diving.— larger turtles made proportionally more long ($ 200 sec- Flatbacks released in open water are active swimmers onds; 13 of 68) dives than the smaller turtles (1 of 77; capable of diving for time periods in excess of 5 minutes p , 0.0003 by the Fisher’s exact test). Comparisons and to depths . 8 m, even within the first 3 weeks of age. between the age subgroups when using the same criteria However, the majority of their dives are shorter (# 2min- (Fig. 6, lower graphs) revealed no statistical differences utes) and shallower (, 4 m) in depth, regardless of profile in either dive depth (x2 5 0.37, n.s.) or dive duration (Figs. 5 and 6). Even young flatbacks can dive in excess of (x2 5 0.05, n.s.). 11 m (Fig. 6) or close to depths (12–13 m) where somewhat Descent Swimming Speeds During V-Dives. — The larger juvenile flatbacks (11–20 cm SCL) were most descent speeds (Table 2) of the turtles of smaller mass frequently captured as in trawls (Walker 1991a) (mean and median, 8.93 and 8.00 cm/s, respectively) were before the introduction of turtle excluder devices (TED). significantly faster than those shown by the larger turtles Although our knowledge of flatback migration at an (3.58 and 2.86 cm/s, respectively; Mann-Whitney early age is meager, current thinking suggests it consists

Table 2. Descent speeds (in cm/s) during the V-dives shown by small and large flatbacks, and the 2 small turtles (turtles 18 and 19) that performed many deep V-dives. See Table 1 for the individual dive counts.

Speed range Group No. V-dives Low High 95% CIa Mean Median Small (n 5 11) 45 1.07 20.00 7.82–10.04 8.77 8.00 Large (n 5 9) 38 1.19 8.57 2.38–4.79 3.54 2.86 Turtles 18, 19 47 8.00 113.00 48.53–59.40 53.50 54.00 a CI 5 confidence interval. 14 CHELONIAN CONSERVATION AND BIOLOGY, Volume 9, Number 1 – 2010

small, neritic phase turtles are capable of searching for food on the bottom at the shallower habitats they later occupy as juvenile turtles. Flatback turtles forage in habitats characterized as turbid (Limpus et al. 1983; Zangerl et al. 1988). Walker (1991a) provides some general data on underwater visibility. For neritic turtles foraging inside the lagoon, visibility (as determined by secchi disk measurements) ranges between 2.2 and 8.8 m. By comparison, in the outer shelf (ocean side of the Barrier Reef), it ranges between 15 and 20 m and is probably comparable with the visibility experienced by other species of marine turtles during their oceanic phase. For flatbacks that have returned as juveniles to inshore waters, visibility probably varies with the season. During the ‘‘wet’’ (rainy season between December and February), outflow from rivers contributes an increased volume of suspended material to shallow bays, estuaries, and mangroves where flatbacks are often found (Zangerl et al. 1988). We completed our study between February and April. During that time period, we were unable to see turtles that dove . 1.0 m below the surface. Under those conditions of restricted visibility, most flatback dives were (as predicted) V- and W-shaped in profile. Most dives were also shallow (4 m or less), with only occasional dives to deeper (up to 10 m) depths (Fig. 5). Figure 7. Dives performed during trials by turtles 18 (above) This pattern suggests that during the neritic phase the and 19 (middle). Time marks are at 10-second intervals. Below, turtles most often scan the environment for objects of depth vs. duration plot for the V-dives (n 5 47) of these 2 turtles. Compare this distribution to the distribution of V-dives interest in the upper portion of water column (prey such as shown by all other neonates (Fig. 5). The latter were, on macroplankton; predators such as sharks; Limpus 2007). average, shallower in depth and longer in duration. An alternative hypothesis is that this distribution of dive depths most efficiently enables the turtles to search for of 2 stages. After hatchlings from eastern Queensland their prey under reduced visibility (see next section, swim offshore and consume their yolk supply, they below). assume ‘‘a surface water dwelling, planktonic life . . . over We postulated that because neonate flatbacks during the continental shelf . . . inside the Great Barrier Reef their neritic phase are found in much the same habitats lagoon’’ (Limpus 2007, p. 20). How long this neritic stage (shallow, turbid coastal waters; Zangerl et al. 1988; lasts is unknown. It terminates when the turtles as larger Walker 1991a), their diving behavior would show few juveniles move to subtidal soft-bottomed habitats at changes during the first few weeks of growth and shallower depths, without otherwise changing their development. To a large extent, those predictions were geographic distribution as coastal organisms (Limpus confirmed because our data did not reveal any significant 2007). These slightly larger turtles are preyed upon by changes in either the type of dive profile shown or in their white-bellied sea eagles (Haliaeetus leucogaster). Curved frequencies of occurrence during development. Instead, carapace lengths (CCL) of flatback skeletons at sea eagle we found that significant changes in diving depth and middens range between 12.2 and 20.3 cm at a site in the duration were correlated with change in mass but not age Gulf of Carpentaria and between 11.3 and 20.5 cm at a (Fig. 6). We cannot explain why turtles of larger mass site in the Great Barrier Reef (Cullen Island and Arch should make proportionally more shallow dives than Rock; Walker 1991b). Although we lack a conversion of smaller turtles. Their tendency to dive for longer durations CCL to SCL for this species, CCL is generally about 7%– may very well be a function of an increase in blood 10% longer than the SCL in the sister species, C. mydas volume (and oxygen-storage capacity; Lutcavage and (J. Wyneken, unpubl. data). The smallest turtles taken by Lutz 1997) that accompanies their increase in mass. sea eagles were not much larger than the average size of On the basis of their body mass at emergence, body our turtles at 7 weeks of age (9.4 cm SCL). These shape, and ecological circumstances we hypothesized that comparisons suggest that in nature (where growth rates flatbacks would swim rapidly. However, the descent can be slower than in captivity), the neritic phase is likely speeds shown by the turtles (excluding turtles 18 and 19) short in duration (months rather than years). The dive ranged between 1 and 20 cm/s, with averages , 9.00 cm/s depths achieved by our turtles also suggest that even (Table 2). These relatively slow descent speeds were SALMON ET AL. — Flatback Turtle Diving Ontogeny 15 comparable with those shown by neonate leatherbacks do in conspecific adults. W-dives were observed when (3.4–16 cm/s, with a mean of 7.1 cm/s; Salmon et al. young leatherbacks found jellyfish, began feeding, and 2004) of comparable age (2–10 weeks) but of greater moved up and down in the water column as they length and mass (60–126 g). We concluded that neonate repeatedly approached the same prey for another attack. flatbacks during their ‘‘routine’’ dives swim slowly, As neonate leatherbacks grow, the majority of their dives especially as they increase in mass. Doing so may be continue to be relatively shallow, but their deepest dives advantageous for several reasons, for example, to become deeper (Salmon et al. 2004), a change that conserve energy by reducing drag and to more effectively probably reflected their increasing physiological capacity detect prey (or predators) under conditions where water to store oxygen as well as the potential benefits that clarity is poor. accrue with niche expansion toward a greater variety of Turtles 18 and 19, however, behaved differently. deeper-dwelling gelatinous prey. This hypothesis is also These turtles were tested at the same site on the same day. supported by how the turtles dive; they descend almost Both completed many more V-dives during their 30- directly downward and then ascend almost directly minute trial than any of the other turtles. A large upward, maximizing their vertical but minimizing their proportion of these dives was deep (up to 11.5 m) and horizontal dive displacement. Because these movements many dives were remarkably short (# 20 seconds; are accomplished with little change in swimming speed, Fig. 7). Descent speeds averaged approximately 50 cm/s, the profiles of their dives generated a significant but some were . 1 m/s (Table 2), even while towing a relationship between depth and duration (Fig. 8, top TDR. Relationships between depth and duration during graph; statistical analysis reported in Salmon et al. 2004). these dives (Fig. 7) were clearly different from those A similarly tight relationship between depth and made by other turtles during their routine V-dives duration also occurs in green turtles (Fig. 8, middle (Fig. 5). The speeds involved were also faster than those graph). With growth, larger neonate green turtles tend to recorded for any small juvenile marine turtle. For dive significantly longer and deeper, but the magnitude of example, green turtles of comparable age but smaller change between younger (2–4 weeks) and older (6– mass (2–8 weeks; 35–70 g) had descent speeds that 8 weeks) turtles is small because few of the routine dives ranged between 8.2 and 41 cm/s and averaged 21.3 cm/s by any turtle exceed 5 m. Green turtles also shift from (Salmon et al. 2004). Green turtles were, until this study, mostly V-dives at 2–4 weeks to mostly U-dives at 6– considered the fastest of the marine turtles whose 8 weeks of development (Salmon et al. 2004). As a result, swimming speeds had been quantified (data summarized the dives of the older turtles do not change much in depth, in Wyneken 1997). even though they last longer. Thus, in contrast to Because we were unable to observe the turtles during leatherbacks, the behavior of neonate green turtles their dives, we can only speculate as to what might have suggests that the resources they require for survival induced turtles 18 and 19 to swim so rapidly. The (food; shelter in the form of Sargassum rafts [Smith and presence of predators near the surface was an unlikely Salmon 2009]) are located close to the surface. Young cause because dives were shorter than usual and the green turtles are capable of making much deeper dives turtles returned to the surface (and potential danger) (down to 18 m during the acclimation period) but do not frequently. Similarly, the presence of predators near the dive deeply after the acclimation period (Salmon et al. bottom was also unlikely because the turtles repeatedly 2004). made deep dives that also would have increased their Flatback neonates show entirely different relation- vulnerability. Another possibility is that the 2 turtles ships between dive depth and duration (Fig. 8, bottom). We behaved atypically because both came from the same nest hypothesize that those differences arise as a consequence of and either possessed unique genes or were exposed to hunting for food (and avoiding predators) in waters of unique conditions during development. However, three of limited visibility, an ecological condition that is unique for their siblings were tested at different times and at other neonate marine turtles. Young leatherbacks and green locations; they showed ‘‘routine’’ dives. We, therefore, turtles, for example, are found in an open ocean hypothesized that turtles 18 and 19 were by chance environment where water clarity is usually excellent. Not released at a site where they were exposed to an attractive surprisingly, both species during this stage of development stimulus (perhaps food) that elicited exceptionally depend primarily upon vision to locate food (Constantino vigorous diving activity. and Salmon 2003; unpubl. obs. on green turtles by M. Comparisons of Diving Behavior Among Species.— Salmon). Leatherbacks also possess a specialized foveal How does flatback diving behavior and development region in their retina that may be designed to detect prey in compare with other species? Can the differences observed the water column beneath them (Oliver et al. 2000). be correlated with ecology? Neonate diving behavior has Neonate flatbacks, however, must search for prey now been studied in 3 marine turtle species, and in each, whose location (either in the water column or on the dive profiles vary in frequency, type, and temporal bottom) under most conditions cannot be determined from characteristics. In leatherbacks, 2–10 weeks of age, for the surface. Even when food is located, flatbacks face example, V-dives dominate (Salmon et al. 2004) as they another problem: how to find that site again after 16 CHELONIAN CONSERVATION AND BIOLOGY, Volume 9, Number 1 – 2010

efficient method of searching for prey whose location in the water column cannot be predicted from the surface: the Levy walk (Sims et al. 2008). Computer simulations show that such a foraging strategy optimizes the probability of contact with prey and closely approximates the diving patterns shown by many diving predators (sea turtles, penguins, sharks, and some teleost predators) that face the same problem (diving ‘‘blind’’ to the location of prey). It, therefore, would be of interest to quantify enough dives of neonate flatbacks to determine whether they, too, fit the model. Rapid swimming movements might be one mecha- nism used to maintain contact with locations where food is abundant. Another mechanism may be an ability to rapidly replenish oxygen stores while at the surface between dives. The dive records for turtles 18 and 19 indicate that rapid swimming occurs and suggest an ability to make consecutive, relatively deep dives in rapid succession (Fig. 7). Adult flatbacks possess blood hemo- globin with a greater affinity for oxygen at high partial pressures than the hemoglobin of loggerheads and, most likely, green turtles (Sperling et al. 2007). Neonates may also have these capabilities. It might be argued that a better strategy for a small turtle that has located food is to continue feeding at the site for as long as possible before returning to the surface. That could be optimal for turtles that are larger. But, we suspect that, for a small turtle that is vulnerable to many predators, survival may be enhanced by retaining sufficient oxygen to sprint away from harm if it appears, take evasive action, and, in doing so, live to feed another day.

ACKNOWLEDGMENTS

We thank Fay and Kenneth Griffin from Mackay and District Turtle Watch and the Blacks Beach Turtle Monitors. Jason Schaffer, Andrea Phillott, Jillian Grayson, and Mariana Fuentes provided field assistance. We thank Figure 8. Depth vs. duration plots for all of the dives Chlo¨e Schauble and Colin Limpus for technical assis- performed by neonate leatherbacks (top, n 5 86 dives by 21 tance. Comments by Larisa Avens, 2 referees, and the turtles) and green turtles (middle, n 5 299 dives by 33 turtles) in editor improved the article. This study was supported by a previous study (Salmon et al. 2004) and by neonate flatbacks (n 5 192 dives by 21 turtles) in this study. James Cook University (JCU) through the Marine and Tropical Sciences Research Facility, by contributions to the Nelligan Fund for Research at Florida surfacing to breathe. Currents near the surface can Atlantic University (FAU), and by personal funds. This displace the turtles horizontally in directions that are study was done while JW was on sabbatical and supported difficult (if not impossible) to determine. For these by FAU. It was permitted under JCU Ethics Permit reasons, we believe that water turbidity has shaped A1265 and under FAU IACUC authorization A07–28. flatback diving to optimize searches for food patches and to reduce the probability of losing contact with food once it is found. LITERATURE CITED We hypothesize that the ‘‘routine dives’’ of flatbacks function primarily to search for food. They are organized BOLTEN, A. 2003. Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz, P.L., as mostly shallow V- and W-dives of relatively short Musick, J.A., and Wyneken, J. (Eds.). The Biology of Sea duration interspersed with occasional deeper dives of Turtles. Boca Raton, FL: CRC Press, pp. 243–257. variable duration (Figs. 5 and 6). This combination of CARR, A. 1987. New perspectives on the pelagic stage of sea shallow and deeper dives resembles a model of the most turtle development. Conservation Biology 1:1–22. SALMON ET AL. — Flatback Turtle Diving Ontogeny 17

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