Changes in Diel Diving Patterns Accompany Shifts Between Northern Foraging and Southward Migration in Leatherback Turtles

Home , Gelatinous zooplankton

754 Changes in diel diving patterns accompany shifts between northern foraging and southward migration in leatherback turtles

M.C. James, C.A. Ottensmeyer, S.A. Eckert, and R.A. Myers

Abstract: Diel diving patterns have been widely documented among plankton-feeding marine vertebrates. In many cases, these patterns have been interpreted as a response to the diel vertical migrations of prey. The leatherback turtle, Dermochelys coriacea (Vandelli, 1761), is a large marine predator that exploits gelatinous plankton in disparate foraging areas. Indi- viduals of this species spend extended periods at northern latitudes before moving southward through pelagic waters. To identify and compare potential diel patterns of diving behaviour in temperate areas, where foraging has been observed, versus during southward migration, 15 subadult and adult leatherbacks were equipped with satellite-linked time–depth recorders off Nova Scotia, Canada. We observed variation in nocturnal versus diurnal behaviour, both at northern latitudes and during migration; however, diel differences in both diving and surface activity were much less pronounced while leatherbacks were in the north. We interpret the difference in leatherback diel diving regimen to reflect a response to changing resource conditions at these times, with leatherbacks foraging throughout the day and night at high latitudes, then changing to a bimodal pattern of diving during southward migration, with generally lon- ger, deeper diving occurring during the night versus during the day. By quantifying diel changes in leatherback behaviour, we provide the first surface time correction factors based on multiple individuals for use in estimating abundance from aerial surveys. Re´sume´ : Les patrons journaliers de plongeé chez les verte´bre´s marins planctonophages ont e´te´ bien e´tudie´s. Souvent, les patrons sont interpre´te´s comme des reáctions aux migrations verticales journalie`res des proies. La tortue luth, Dermochelys coriacea (Vandelli, 1761), est un pre´dateur marin de grande taille qui exploite le plancton ge´latineux dans des aires d’alimentation disparates. Les individus de cette espe`ce passent de longues pe´riodes dans les latitudes nordiques avant de se de´- placer vers le sud dans les eaux pe´lagiques. Dans le but d’identifier et de comparer les patrons journaliers potentiels du comportement de plongeé dans les zones tempe´reés ou` on observe de l’alimentation (par rapport aux patrons observe´s durant la migration vers le sud), nous avons muni 15 tortues subadultes et adultes d’enregistreurs de temps et de profondeur relie´sa` des satellites au large de la Nouvelle-E´ cosse, Canada. Nous avons observe´ une variation entre les comportements nocturne et diurne, tant dans les latitudes nordiques que durant la migration; les variations journalie`res d’activite´ en plon- geé et en surface sont, cependant, beaucoup moindres lorsque les tortues sont dans le nord. Nous interpre´tons les diffe´ren- ces dans le re´gime journalier de plongeé des tortues luth comme des reáctions aux conditions changeantes des ressources a` ce moment; aux latitudes e´leveés, les tortues s’alimentent tout au long de la journeé et de la nuit; durant la migration vers le sud, elles adoptent un patron bimodal de plongeé, avec geńe´ralement des plongeés plus profondes et plus prolongeés durant la nuit que durant le jour. En quantifiant les changements journaliers du comportement des tortues luth, nous fournis- sons les premiers facteurs de correction du temps passe´ en surface base´s sur l’observation de plusieurs individus pour servir a` estimer l’abondance a` partir d’inventaires ae´riens. [Traduit par la Re´daction]

Introduction diverse range of taxa that includes small benthic herbivores (Rogers et al. 1998) and large pelagic vertebrates (Musyl et A common pattern among marine organisms, diel vertical al. 2003; Weng and Block 2004). However, such diel move- migration (DVM), normally involves descent to deeper ments, which are often mediated by light levels, have been waters at dawn, followed by an ascent towards the surface most widely reported in zooplankton (e.g., Forward 1988). at dusk (Hays 2003). DVM has been documented across a DVM has been interpreted as a means by which organisms avoid predators or maximize feeding efficiency, with a Received 19 October 2005. Accepted 3 March 2006. Published trade-off between these motivations shaping DVM in some on the NRC Research Press Web site at http://cjz.nrc.ca on species (Loose and Dawidowicz 1994; Bollens 1996). Inter- 14 June 2006. pretation of movement data collected from several plankti- M.C. James,1 C.A. Ottensmeyer, and R.A. Myers. Department vores has, therefore, been enhanced by understanding DVM of Biology, Dalhousie University, 1355 Oxford Street, Halifax, in their prey. It has been suggested that diel dive patterns in NS B3H 4J1, Canada. whale sharks, Rhincodon typus Smith, 1828, may represent S.A. Eckert. Marine Laboratory, Duke University, 135 Duke the tracking of zooplankton prey (Graham et al. 2005) and Marine Lab Road, Beaufort, NC 28516-9721, USA. diel changes in the depth preferences of basking sharks, Ce- 1Corresponding author (e-mail: [email protected]). torhinus maximus (Gunnerus, 1765), are consistent with a

Can. J. Zool. 84: 754–765 (2006) doi:10.1139/Z06-046 # 2006 NRC Canada James et al. 755 response to DVM in zooplankton (Sims et al. 2003). Simi- iour of leatherback turtles equipped with satellite tags off lar findings have been reported in Atlantic redfishes, genus Nova Scotia, Canada. In particular, we aimed (i) to identify Sebastes Cuvier, 1829 (Gauthier and Rose 2002). Among potential consistent differences in day and night behaviours, predators of gelatinous zooplankton, the ocean sunfish, (ii) to compare diel behaviour patterns between northern Mola mola (L., 1758), also exhibits patterns of DVM that areas where foraging is known to occur and more pelagic may parallel those of their prey (Cartamil and Lowe 2004). waters during southward movements of leatherbacks, and Patterns of DVM observed in planktivorous species may (iii) to estimate the proportion of time leatherbacks spend at not only reflect changing prey availability, but also selec- and near the surface to identify optimal areas for aerial cen- tion for environmental conditions such as ambient light sus of this species and to guide the choice of sighting cor- (Nelson et al. 1997). In addition, patterns of DVM in rection factors for use in aerial surveys. planktivores can be variable across a species’ range. For example, assumption of ‘‘normal’’ or ‘‘reverse’’ (ascent at Methods dawn, descent at dusk) DVM in basking sharks appears to be habitat-specific (Sims et al. 2005). During the summers of 2001–2003, we captured leather- The leatherback turtle, Dermochelys coriacea (Vandelli, back turtles at the surface in waters off Nova Scotia, Can- 1761), is a large marine vertebrate that exploits gelatinous ada, using a breakaway hoop net operated from a 10.5 m zooplankton (primarily members of phyla Cnidaria and Cte- commercial fishing boat (for methods see James et al. nophora) (Bleakney 1965; den Hartog and van Nierop 2005a). We attached satellite-linked time–depth recorders 1984). The leatherback is the only marine turtle to specialize (SLTDR; models SSC3 (n = 13) and SDR-T16 (n =2); on gelatinous prey as an adult. It is also unique among sea Wildlife Computers, Redmond, Washington) to the carapace turtles in its ability to inhabit cold northern waters (James using a custom-fitted harness made of nylon webbing and and Mrosovsky 2004), with some adult and subadult leather- polyvinyl tubing (modified after Eckert 2002). Harnesses in- backs completing annual round-trip migrations from tropical corporated corrodible links to ensure their eventual release. waters to temperate waters (James et al. 2005a) to forage on Leatherbacks were repeatedly doused with buckets of sea large jellyfish (James and Herman 2001). Distinct ‘‘phases’’ water while aboard and were normally released within of the migratory cycle have been delineated by dramatic 30 min of capture. All procedures were in accordance with changes in suites of behaviours (James et al. 2005b), but the principles and guidelines of the Canadian Council on only at a resolution of 24 h periods. Diel dive patterns have Animal Care, approved by the Dalhousie University Com- been described for female leatherbacks during internesting mittee on Laboratory Animals, and licensed by Fisheries intervals in tropical waters (Eckert et al. 1989, 1996; Eckert and Oceans Canada. 2002) and during departure from nesting areas (Hays et al. SLTDRs collected and relayed data on time at depth, time 2004). However, analyses of diel patterns of diving behav- at temperature, maximum dive depth, and dive duration that iour have been reported neither for leatherbacks in northern were binned within 14 user-defined data ranges over 6 h foraging areas nor for leatherbacks during southward migra- collection periods. Periods were set so that one consistently tion from these habitats. encompassed night and one encompassed day — night: Unfortunately, very little is known about the distribution 2100–0300; morning: 0300–0900; day: 0900–1500; evening: and movements of gelatinous zooplankton (Graham et al. 1500–2100; Atlantic daylight time. Time at depth and time 2003), particularly in the open ocean (cf. Harbison et al. at temperature reflected all time when SLTDRs were sub- 1978). Instead, most research has focused on the biology of merged, whereas dives were registered only when leather- these organisms in coastal and shelf waters (Brewer 1989; backs descended below 4 m (n = 12 tags) or 6 m (n =3 Purcell 1992; Olesen et al. 1994; Buecher et al. 2001) and tags). While SLTDRs simultaneously record data from dif- in aquaria (Mackie et al. 1981; Mills 1983; Costello and ferent channels (e.g., depth, temperature), data are transmit- Colin 1994; Hansson 1997). Both field and experimental ted in histogram format to increase ease of transfer via the studies of gelatinous plankton suggest that, like other plank- limited bandwidth of the Argos satellite system (Fedak et ton groups, DVM is normally light-dependent and usually al. 2002). This decreases the resolution of the data; however, involves upward movement in the water column at dusk patterns of depth utilization and dive duration can be readily and downward movement at dawn (e.g., Mills 1983; Arkett identified and related to the spatial and temporal character- 1984, 1989; Schuyler and Sullivan 1997; Ba˚mstedt et al. istics of horizontal movements. SLTDRs also transmitted 2003; Benovic et al. 2005). In many cases, this pattern of the combined proportion of each 6 h period that the leather- movement may serve to optimize prey encounters by match- back was at the surface or very close to the surface (<2 m: ing jellyfish movements with those of their zooplankton n = 12; <3 m: n = 3). These surface values were matched to prey (e.g., Arkett 1984). Since reverse vertical migrations median daily locations for each leatherback to create com- (e.g., Yasuda 1973) or an absence of vertical migration posite maps divided into hexagonal areas (see below). The have been reported for some gelatinous species (e.g., Mills colour of each hexagonal area reflects the median surface 1983; Benovic et al. 2005), and these patterns can vary time corresponding to a specific 6 h time period for daily even within species in different regions (e.g., Arai 1997; Ki- turtle positions falling within that area. deys and Romanova 2001), or with changes in community SLTDRs were located with the Argos system (http://www. structure (Graham et al. 2001), it is very difficult to predict argosinc.com). Argos assigns location class, an index of po- the distribution and (or) movements of gelatinous species sitional accuracy, to all derived locations. The analyses pre- based on oceanographic features alone. sented here used all positions with location classes 3, 2, or 1 In this study, we analyzed the diving and surface behav- (categorized to lie within 150, 150–350, or 350–1000 m, re-

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Table 1. Results of mixed models for leatherback turtles, Dermochelys coriacea, during northern foraging.

95% CI Response variable Transformation* No. of leatherbacks Period Estimate Lower Upper P{ Mean depth (m) log 8 Night 7.1 5.8 8.7 <0.0001 Day 8.6 7.0 11 Percentage of time in 0–6 m logit 7 Night 67 60 73 0.005 Day 62 55 69 Maximum depth (m) log 8 Night 28 21 37 <0.0001 Day 34 25 45 Range of dive durations (min) None 7 Night 5.8 4.4 7.2 ns Day 5.9 4.5 7.3 Maximum duration (min) None 7 Night 8.3 6.9 9.8 ns Day 8.1 6.6 9.5 Minimum duration (min) None 8 Night 2.4 2.2 2.7 ns Day 2.4 2.2 2.7 Percentage of dives 0–4 min in duration logit 8 Night 26 18 36 ns Day 23 16 33 Mean duration (min) log 7 Night 4.9 4.3 5.5 ns Day 4.7 4.2 5.3 Mean temperature (8C) None 8 Night 16.7 15.0 18.6 ns Day 17.0 15.2 18.7 . *Some response variables were transformed before fitting to models; results presented were back-transformed to original units. None of the transformations affected the inferences. {P values show the results of a Wald test for significant differences between periods; ns indicates no significant difference (P > 0.05). spectively, of the tag’s true position). We also used location depth, time, or temperature ranges, we used midpoints of classes A, B, and 0 (categorized to lie >1000 m from the each range for relevant calculations on variables such as tag’s true position) if they yielded rates of travel £5 km/h, means, ranges, maximums, and minimums. For percen- which is consistent with 99% of travel rates calculated for tages, we used a logit transformation and report logit 38 leatherbacks tracked for an average of 218 days (James back-transformed results. For other response variables, log et al. 2005a). We omitted positions of location quality Z. transformations were made when it was found that this im- From these filtered locations, we calculated median daily lo- proved the normality of the residuals; we report model re- cations for each leatherback, interpolating positions assum- sults back-transformed to the original units in these cases. ing constant speed and direction for days in which no In all cases, the transformations did not change the conclu- positions were obtained for a given turtle. sions of the modeling. Confidence intervals (CI) for each estimated parameter are presented as 95%. Statistical methods Mixed models were fitted separately to data correspond- To identify potential diel differences in leatherback diving ing to two phases of the migratory cycle: when leatherbacks behaviour and ambient temperature among 6 h periods, we were in northern foraging areas (7 days after tagging, to fit linear mixed-effects models in SAS (Littell et al. 1996). avoid including data affected by potential capture effects, to For each model, period (night, morning, day, or evening) 7 days before start of sustained southward movements) and was considered a fixed effect, while the effect of leatherback when they were traveling southward (between 368 and 218N was considered to be a normal random variable, as was the latitude) in the first season after tagging (Fig. 1). While the error term. Hence, data from individual leatherbacks were migrations of many of the leatherbacks we tagged included given equal weight. movement to waters south of 218N, we conservatively used this latitude as a cutoff so as to encompass southward mi- Our mixed-effects models followed a similar general form. gratory behaviour of all turtles. Eight of the 15 tags trans- For example, the mean depth y in period p for leatherback pid mitted in the north long enough (i.e., >14 days) to be i and day d was modeled as included in the models. Some analyses included only seven of these leatherbacks to exclude, where appropriate, one ypid ¼ þ i þ pid p SLTDR programmed with different data range bins. Thirteen where p is the mean depth for period p and the variability of 15 tags transmitted during southward migration; some among leatherbacks is a normal random variable i (i.e., analyses included only 10 leatherbacks with identical tag 2 i iid Nð0;Þ), which was also the case for the errors settings. We focussed on the differences between night and 2 (pid iid Nð0; Þ). Of interest is p and whether it differs day periods, since the morning and evening periods each en- between periods. To test for differences between periods, compassed dramatically different light levels. we used a Wald test (Littell et al. 1996). The dependent variables modeled are listed in Tables 1–3; the values for Results model parameters were found using restricted maximum likelihood. Since the SLTDR tags present data binned into Fifteen leatherbacks were equipped with SLTDRs: seven

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Table 2. Results of mixed models for leatherback turtles during southward migration (368N–218N).

95% CI Response variable Transformation* No. of leatherbacks Period Estimate Lower Upper P{ Mean depth (m) log 13 Night 40 32 50 <0.0001 Day 18 14 23 Percentage of time in 0–6 m logit 10 Night 20 14 28 <0.0001 Day 82 75 88 Maximum depth (m) None 13 Night 112 96 128 <0.0001 Day 155 139 172 Range of dive durations (min) None 10 Night 15 10 19 <0.0001 Day 21 17 26 Maximum duration (min) None 10 Night 34 31 37 <0.0001 Day 26 23 29 Minimum duration (min) None 13 Night 19 16 22 <0.0001 Day 5.3 2.4 8.4 Percentage of dives 0–4 min in duration logit 13 Night 0.08 0.02 0.2 <0.0001 Day 17 6 40 Mean duration (min) None 10 Night 28 25 31 <0.0001 Day 13 10 16 Mean temperature (8C) None 11 Night 25.0 24.4 25.6 <0.02 Day 25.3 24.6 25.9 . *Some response variables were transformed before fitting to models; results presented were back-transformed to original units. None of the transformations affected the inferences. {P values show the result of a Wald test for significant differences between periods.

Table 3. Results of mixed models estimating the average percentage of time that leatherback turtles spent at or near the surface (0–2 or 0–3 m).

95% CI Leg of track Transformation No. of leatherbacks Period Estimate Lower Upper Northern foraging logit 7 Night 43 40 47 Morning 43 40 47 Day 50 46 53 Evening 52 48 55 Southward migration logit 10 Night 18 13 25 Morning 29 21 38 Day 77 69 84 Evening 29 22 38 Note: Models were fitted separately for northern foraging time and southward migration. Values were logit back-transformed to original units. Statistical differences are night = morning < day = evening for northern foraging and night < morning = day < evening for southward migration, where ‘‘=’’ is not significantly smaller at p > 0.05 and ‘‘<’’ is significantly smaller at p < 0.0001. One leatherback tag reported time between 0 and 3 m, while all others reported time between 0 and 2 m; all tags included time at the surface. off mainland Nova Scotia (~448N, 648W), and eight off tagging). While in these northern waters, leatherbacks exhib- Cape Breton Island (~478N, 608W). These included three ited similar depth use and dive durations through all of the subadults (curved carapace length (CCL) < 140 cm), nine 6 h periods (see Fig. 2 for a representative turtle). Most of mature females, and three mature males. We show data each period was spent in the top 6 m of the water column from representative turtles in the supporting figures for illus- during all four periods (e.g., mixed-model estimates — night trative purposes; the models included all leatherbacks with period: 67%, day period: 62%; for day–night comparison see identical tag settings. Numbers reported in the text are param- Table 1 and Fig. 3). Mean leatherback depth (calculated eter values estimated in the mixed models; see tables for based on time at depth) during this northern phase was very complete values, including 95% CI and sample sizes. shallow (night: 7.1 m; day: 8.6 m) and maximum depth per period averaged close to 30 m (night: 28 m; day: 34 m). Northern foraging Statistically, mean depth, maximum depth, and the propor- Twelve of the 15 leatherbacks remained in shelf and slope tion of time spent within 0–6 m of the surface each differed waters off eastern Canada and northeastern USA between 5 significantly between night and day periods, but by quite and 121 days after tagging before migrating south (the other small absolute amounts (Table 1). 3 leatherbacks showed directed movements southward upon Leatherbacks made dives of similar average duration

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Fig. 1. Satellite-derived positions of leatherback turtle, Dermo- long dives (mixed-model estimate for maximum duration: chelys coriacea, A (mature female, curved carapace length (CCL) = 34 min; Table 2, Figs. 2, 3), but with a fairly limited range 141.5 cm) tagged on 16 August 2001 off Nova Scotia, Canada. of dive durations (modeled range: 15 min; Table 2, Figs. 2, Broken horizontal lines show latitudinal boundaries of region in- 3). During the day period, leatherbacks made similarly long cluded in the analyses of southward migration (218 and 368N). Ar- dives, but also made many short dives, so that the range of row indicates direction of movement. Final transmission received durations during the day was wider (21 min) and the mean on 30 March 2002. Inset: enlargement of region marked by the duration lower (13 min; Table 2) than the mean duration broken-line box. Track between point 1 (7 days after tagging) and during the night period (28 min). The differences between point 2 (7 days before the start of migration behaviour) included in night and day periods presented here were all significantly analyses of northern foraging. Dotted line is the 1000 m depth con- different (Wald test on modeled parameters: p < 0.0001; Ta- tour. ble 2). Water temperature sampled by leatherbacks increased as 50 they moved south. Mean temperatures during the day and 1 night periods were similar (night: 25.0 8C; day: 25.3 8C; Ta- North ble 2, Fig. 3). America 2 40 Surface time Time at or near the surface (0–2 m (n = 12 tags) or 0–3 m (n = 3 tags)) for all leatherbacks corroborated the diel trends outlined above (Fig. 4). While in shelf and slope waters of northeastern USA and eastern Canada, leatherbacks spent a

30 Α 9 modeled average of 43% of the night period at the surface (Table 3). During the day period, the modeled average sur- Latitude (°N) face time was 50%, although these levels were quite variable from day to day within and between leatherbacks 20 (Fig. 5). Modeling of the mean surface time per period revealed significantly higher surface times in the day and evening periods than in the night and morning periods (pairwise comparisons, Wald test; p < 0.0001; Table 3). 10 During southward migration through pelagic waters, South America leatherbacks showed much larger differences in surface 80 70 60 50 40 time between periods. Once leatherbacks had left continental Longitude (°W) shelf and slope waters, the average percentage of time they spent at or near the surface was very high during the day (night: 4.9 min; day: 4.7 min) and showed a similar range of period (77%) and was much lower during the other periods, dive durations (Table 1; Figs. 2, 3) between night and day particularly during the night (night: 18%; morning: 29%; periods during this northern phase (no statistical difference). evening: 29%; Table 3). Mean water temperature sampled by the turtles did not dif- fer statistically between day and night (mixed-model esti- Discussion mates — night: 16.7 8C; day: 17.0 8C; Table 1; Figs. 2, 3). At the resolution of 6 h periods, we identified diel pat- Southward migration terns in leatherback turtle behaviour that are consistent After leaving northern foraging areas, diel differences in among turtles. We found that the magnitude of diel differen- diving behaviour became pronounced among all 13 leather- ces in behaviour varied greatly between when leatherbacks backs tracked during southward movements (tags from two were in known northern foraging areas (waters off eastern leatherbacks stopped transmitting while they were still in Canada and northeastern USA) versus when they were trav- northern foraging areas). During the day period, turtles spent eling through pelagic waters during southward movements. substantial amounts of time in the top 6 m of the water col- A greater challenge is the interpretation of this diel variation, umn (mixed-model estimate: 82% of day period; see Table 2, since only limited information is available on potentially Figs. 2, 3). However, they also tended to make their deepest critical factors that may influence leatherback behaviour. dives (often >400 m) during the day period. The deepest re- In particular, the vertical, geographic, and temporal distri- corded dives were limited to the morning, day, and evening butions of the leatherback’s gelatinous prey are not yet periods (13/13 turtles). During the night period, leatherbacks understood in most offshore areas. spent significantly less time in the top 6 m (20% of night period) than during the day period and they showed more Northern areas concentrated use of depths between 24 and 100 m (night The diving behaviour of leatherbacks in northern foraging mean depth from mixed models: 40 m; day mean depth areas revealed very minor diel differences, with modeled from mixed models: 18 m; Table 2, Figs. 2, 3). mean and maximum dive depths changing by only several Dive durations during southward migration increased with metres during the night versus during the day. In multiple decreasing latitude, but exhibited marked diel differences measures of dive duration, no statistical difference was (e.g., Fig. 2). During the night period, leatherbacks made found between day and night periods. Together, these find-

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Fig. 2. Time at depth, dive duration, water temperature, and latitudinal position of leatherback turtle B (subadult, CCL = 134.0 cm) from 16 August 2003 to 21 January 2004. Colour panels generated from a tag that reported data within 14 user-defined ranges for each variable. Coloured lines in each range (separated by dotted lines) indicate percentage of time or dives in that range over a 6 h period. Night: 2100– 0300; morning: 0300–0900; day: 0900–1500; evening: 1500–2100. Left column: percentage of time (6 h period) spent at different depth ranges. Middle column: percentage of dives (per 6 h period) of different durations. Right column: percentage of time (6 h period) spent in different temperature ranges (8C). Bottom row: latitudinal movement, with broken lines in each panel showing timespans of data used in the mixed models (Tables 1–3, Fig. 3) for foraging time (left) and southward migration (right). Depth (m) Dive duration (min) Temperature (°C)

> 52 Day 48 44 40 36 32 28 24 20 16 12 8 4 0

16/7 27/8 8/10 19/11 31/12 16/7 27/8 8/10 19/11 31/12 16/7 27/8 8/10 19/11 31/12

0% 20% 40% 60% 80% 100% 0% 20% 40% 60% 80% 100% 0% 20% 40% 60% 80% 100%

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Fig. 3. Back-to-back histograms of measures of diving behaviour and water temperature sampled during the night period (solid bars, 2100– 0300) and the day period (open bars, 0900–1500) for three leatherback turtles: B (subadult, CCL = 134.0 cm), C (mature female, CCL = 155.0 cm), and D (mature male, CCL = 168.5 cm). The three left columns show mean data during time spent in northern foraging areas and the three right columns show mean data for southward migration as defined for mixed models. Asterisks indicate bars with values between 0.005 and 0.05. (a) Proportion of time (6 h period) spent in user-defined depth ranges. (b) Proportion of dives whose maximum depth fell in user-defined depth ranges. (c) Proportion of dives in user-defined duration ranges. (d) Proportion of time (6 h period) spent in user-defined temperature ranges. Northern Foraging Southward Migration Turtle Turtle Turtle Turtle Turtle Turtle (a) B C D B C D 06 06 12 12 * * * * * * 18 * * 18 * * * * * * 24 * * * * 24 * * * * * * 50 * * * * 50 * * * 78 78 * * 102 102 * * 154 154 * * * * 202 202 * * * 252 252 * * 300 300 * 352 352 * 400 400 400+ 400+ * * 101101101101101101 (b)

06 06 * 12 12 * 18 18 * * * 24 * 24 * * * * 50 * 50 * * * * * *

Depth (m)78 * * Depth (m) 78 * 102 102 * * 154 154 202 202 * * * * 252 252 * * 300 300 * * 352 352

Maximum * 400 400 400+ 400+ * * * 101101101101101101 (c)

52+ 52+ * 52 52 48 48 * * 44 44 * * * 40 40 * * * 36 36 32 32 28 28 * * 24 24 * * 20 20 * * 16 * 16 *

Dive Duration (min) Dive 12 * * * 12 * * 8 8 * * * 04 04 * * 101101101101101101 (d) >31.8 >31.8 31.8 31.8 29.9 29.9 27.9 27.9 25.8 25.8 23.9 23.9 21.8 * 21.8 * * * * * 20.0 * * 20.0 * * 17.9 17.9 * 15.8 15.8 13.9 * 13.9 11.9 * * * 11.9 Temperature (°C) Temperature 10.0 * * * 10.0 <7.9 * <7.9 1 0 1 1 0 1 1 0 1 1 0 1 1 0 1 1 0 1 ings support an absence of strong diel changes in northern through field observations of leatherbacks swallowing Cyanea activity for the leatherbacks in this study. Foraging behaviour capillata (L., 1758) at the surface (James and Herman 2001; in northern waters during daylight hours has been confirmed James et al. 2005a). The relatively shallow depths used by

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Fig. 4. Median surface times of leatherback turtles (<2 m: n = 12 turtles; <3 m: n = 3 turtles) during (a) the night period and (b) the day period within hexagonal area bins (width: 0.9178 longitude; largest height: 1.0018 latitude). ( a ) ( b ) 100%

88%

75%

63%

50%

Latitude (°N) 38%

26%

13%

1% 80 70 60 50 40 30 Longitude (°W) Longitude (°W) leatherbacks in northern foraging areas, and particularly tia, we regularly see leatherbacks resting or swimming at the shelf waters, suggests that leatherbacks do not have to under- surface from late morning through dusk. These activities take deep dives to locate jellyfish prey in these areas. may reflect basking behaviour, which may be important in Captive Aurelia aurita (L., 1758) (another species of jel- digesting large volumes of cold prey in temperate waters lyfish consumed by leatherbacks) collected off the coast of (James et al. 2005b). Alternatively, resting or traveling Nova Scotia revealed a pattern of reverse vertical migration slowly at the surface may reflect recovery from daytime bouts in aquaria, migrating towards the surface during the day and of searching for and handling prey at depth, as has been away from it at night (Mackie et al. 1981). Analogous re- observed in some marine mammals (e.g., Acevedo-Gutie´rrez sults were reported for wild specimens (Yasuda 1973). How- et al. 2002). However, given the relatively short dive dura- ever, given the plasticity shown by this species (Lucas tions and cool ambient temperatures recorded in northern 2001), extrapolation of these movement patterns to the areas waters, it is unlikely that the aerobic dive limits of leather- where the leatherbacks in this study foraged may not be backs are shorter than typical submergence times. warranted. Given the similarity of diving behaviour shown between day and night, we suggest that leatherbacks can Southward migration profitably exploit patches of jellyfish prey in these areas In contrast to their behaviour in northern foraging areas, throughout the day and night once they have been located. leatherbacks showed pronounced diel differences in behav- The small vertical changes in leatherback depth use here iour while moving southwards. Leatherbacks spent a greater may represent tracking of the DVMs of their gelatinous proportion of time at and near the surface during the day; planktonic prey, which has been suggested as an explanation however, the deepest dives also occurred during the day. of diving behaviour in tropical waters (Eckert et al. 1989; During the night, the amount of time spent at and near the Hays et al. 2004). However, if this is the case, DVM in surface decreased markedly and leatherbacks spent much C. capillata, A. aurita, or other jellyfish forage species in more time at depths below 24 m. Thus, even at the resolu- this area is likely occurring at the scale of metres, or at most, tion of 6 h periods, it appears that leatherbacks exhibit dis- tens of metres, rather than hundreds of metres as shown in tinct diel patterns of behaviour. These diel patterns appear to some other species (Graham et al. 2001; Lucas 2001). Cor- change greatly between times of broader behavioural shifts, roborating results from in situ studies of jellyfish are not termed ‘‘phases’’ (James et al. 2005b) of the leatherback mi- available for shelf waters off eastern Canada. However, even gratory cycle. if such work were conducted there, DVMs in jellyfish that mi- Although Southwood et al. (1999) did not find consistent grate only short distances may be missed altogether by diel patterns in depth use among female leatherbacks during conventional plankton net sampling studies (Arkett 1984). internesting movements off the Pacific coast of Costa Rica, While using northern waters, leatherbacks spent slightly at the 6 h resolution of our data the diel patterns shown dur- more time near the surface (0–6 m, satellite tag submerged) ing southward movements from temperate waters of the during the night than during the day. However, surface time northwest Atlantic are consistent with the DVMs of female itself (time spent at 0–2 m or at 0–3 m) was significantly leatherbacks in tropical waters reported by others (Eckert et higher during the day than during the night. Off Nova Sco- al. 1989; Hays et al. 2004). Hays et al. (2004) found that

# 2006 NRC Canada 762 Can. J. Zool. Vol. 84, 2006

Fig. 5. Percentage of time spent at the surface for two leatherback turtles during the 6 h periods. Left column: turtle A between 0 and 3 m; right column: turtle B between 0 and 2 m. Night: 2100–0300; morning: 0300–0900; day: 0900–1500; evening: 1500–2100. Bottom row: latitudinal movement, with broken lines in each panel showing timespans of data used in the mixed models (Table 3) for foraging time (left) and southward migration (right). Turtle A Turtle B

ace

100 80 60 40 20 0 Day

Percentage of 6 h period spent at surf 16/7 13/8 10/9 8/10 5/11 3/12 31/12

Latitude (°N)

leatherbacks spent the most time diving below 10 m during time. If this scenario holds true, we would also expect the the middle of the night and, while they found that the deep- occasional very deep dives made during the morning, day, est dives recorded were exclusively diurnal, these turtles and evening by leatherbacks on their way southward to be predominantly used waters less than 10 m from the surface ‘‘scouting’’ dives — attempts by the turtles to ascertain the during the day. Hays et al. (2004) interpreted this pattern of depth of vertically migrating prey and to assess whether to diving as being representative of leatherbacks responding to attempt foraging at that time. a ‘‘normal pattern’’ of DVM by their gelatinous prey (dusk However, one must be cautious in drawing parallels be- ascent, dawn descent), with turtles dedicating more time to tween the behaviour of female leatherbacks in the first sev- nocturnal foraging when prey have ascended to depths eral months following their nesting season (Hays et al. where they can be most profitably exploited. If this infer- 2004) and that of juvenile and adult leatherbacks of both ence is correct, and if the gelatinous prey found on south- sexes as they depart northern waters following several ward migration routes of leatherbacks follow a similar months of foraging (as presented here). Leatherbacks leav- behavioural strategy of ‘‘normal’’ DVM, we would expect ing northern seasonal foraging areas are approximately 30% leatherbacks to be foraging at night. This would imply that heavier than females of the same carapace length weighed the depths most used by leatherbacks at night correspond to during the nesting season (James et al. 2005a), and are the depths at which gelatinous prey are concentrated at that likely less in need of immediate foraging opportunities. The

# 2006 NRC Canada James et al. 763 high rates of travel characteristic of leatherbacks leaving refining surface time correction factors and thereby improv- northern waters (James et al. 2005b), combined with their ing estimates of abundance from aerial survey data. recently acquired adipose stores, suggest that these animals may be able to primarily focus on returning promptly to Synthesis breeding (James et al. 2005c) and (or) foraging areas in dis- Our analysis has identified strong differences between the tant tropical waters (James et al. 2005b), rather than forag- diel dive patterns of leatherback turtles associated with north- ing continuously along the way. Hence, until the seasonal ern foraging and southward migratory behaviours, phases and vertical distribution of gelatinous plankton in pelagic which temporally span more than half of this species’ an- waters is better documented, we must also consider alterna- nual migratory cycle (James et al. 2005b). We expect that tive hypotheses to explain leatherback diving behaviour. For less marked changes in diel dive patterns occur at finer example, occasional very deep dives during the day may spatial and temporal scales within these phases. In part, serve a thermoregulatory function (James et al. 2005b). In- like diel dive patterns found in basking sharks (Sims et al. creased near-surface time during the day may also reflect 2005), these changes may reflect heterogeneity in habitat. an opportunity to receive solar navigational cues for their For example, leatherbacks using northern waters may ex- southward travel in the form of a time-compensated sun hibit different diel behaviour patterns depending on compass, as has been shown in some amphibians (e.g., Adler whether they focus foraging activity in slope waters, shelf 1976) and suggested for loggerhead turtles (Caretta caretta waters, or both of these habitats. In addition, leatherbacks (L., 1758)) (Avens and Lohmann 2003) and leatherbacks may modify diel dive patterns if opportunistically exploit- (Eckert 2002). ing localized densities of jellyfish versus transiting between them, as these prey may be ephemeral and patchily distrib- Implications for aerial surveys uted in waters on and off the continental shelf (James et There are considerable challenges inherent in estimating al. 2005b). We also expect finer scale temporal patterns leatherback abundance in foraging areas. Aerial surveys are within the observed 6 h periods. This variability would be the most commonly used method for locating leatherbacks consistent with the results of this study and earlier ones over large areas of ocean. However, they are costly, rarely (e.g., Hays et al. 2004) that suggest a high degree of be- conducted far from shore, and must be limited to those days havioural plasticity in this wide-ranging species. when both weather and sea conditions are favorable for de- While we have compared leatherback biotelemetry data to tecting leatherbacks at or near the surface. Moreover, while the most common pattern of DVM described for gelatinous large-scale aerial survey programs in northwestern Atlantic planktonic organisms, testing hypotheses regarding how waters have collected observations of leatherbacks over peri- leatherback behaviour may be influenced by the distribution ods of several years, there has been little confidence in the and movements of their prey will require additional re- resulting estimates of leatherback abundance because sur- search. We must improve our understanding of the diet of face time correction factors have not been available (Shoop leatherbacks in different parts of their range, particularly in and Kenney 1992). those relatively inaccessible pelagic areas where leather- In a separate analysis, data from a different group of backs are known to migrate or aggregate, and establish leatherbacks showed that, over 24 h periods, turtles spent when, at what depths, and on what species, feeding occurs. less time at the surface once they moved from temperate Faced with similar questions, biologists studying other div- foraging areas to lower latitudes (James et al. 2005b). How- ing organisms have employed various telemetry systems to ever, the present results indicate that the highest surface ac- detect feeding events using drops in stomach or esophageal tivity actually occurs from 0900 to 1500 during migration temperatures (Ancel et al. 1997) and have used animal- through pelagic waters. Leatherbacks may be most visible borne video systems and data recorders (Davis et al. 1999) during this time, yet are potentially spread over vast areas to study prey species composition, ingestion rates, and how (James et al. 2005a). Therefore, we propose that aerial sur- prey is located and handled. Assessing abundance of jelly- veys may be most appropriate in summer and autumn in fish through trawl sampling (e.g., Purcell et al. 1999) is in- shelf and slope waters off Canada and northeastern USA, herently difficult, as associated damage to these organisms because leatherbacks aggregate in these areas at those times makes counting them challenging (Graham et al. 2003). (James et al. 2005a) and spend substantial amounts of time However, acoustic (Purcell et al. 2000) and video technol- at the surface (~50% of the day and evening). Furthermore, ogies (Tamburri et al. 2000; Graham et al. 2003) now offer in these areas the relative proximity of leatherbacks to shore much promise for mapping the distributions of these organ- would enhance the feasibility of aerial survey programs isms (for a review see Ba˚mstedt et al. 2003). We urge fur- (e.g., Shoop and Kenney 1992). ther research on jellyfish species composition, distribution, By quantifying diel changes in leatherback behaviour in and abundance in both coastal and pelagic habitats used by northern waters, we provide the first surface time correction leatherbacks to explain both the role of jellyfish in the factors for leatherback aerial survey abundance estimates ecosystem and their relationship to leatherback turtles. De- based on multiple individuals and have identified day and termining, with certainty, if and when leatherbacks feed evening (0900–2100) as periods during which leatherbacks during migratory periods will be critical to further clarify- spend the most time (CI for day mean: 46%–53%, CI for ing the basis of diel behavioural patterns. evening mean: 48%–55%) at the surface. Our results suggest We have shown that leatherbacks spend a relatively high that there is considerable variability in surface time both proportion of time at and near the surface in northern forag- within and among leatherbacks. Analysis of surface activity ing areas. Such behaviour puts them at risk for collisions recorded at finer temporal and spatial scales will be key to with vessels, particularly in waters adjacent to large urban

# 2006 NRC Canada 764 Can. J. Zool. Vol. 84, 2006 coastal communities with heavy recreational boat traffic. medusarum. J. Plankton Res. 23: 1073–1080. doi:10.1093/ Examination of leatherbacks found stranded along the coast plankt/23.10.1073. of northeastern USA (Dwyer et al. 2003) corroborates this Ba˚mstedt, U., Kaartvedt, S., and Youngbluth, M. 2003. An evalua- suggestion. By continuing to investigate leatherback behav- tion of acoustic methods to estimate the abundance and vertical iour at northern latitudes, we can proceed with identifying distribution of jellyfish. J. Plankton Res. 25: 1307–1318. doi:10. and eventually addressing sources of anthropogenic injury 1093/plankt/fbg084. and mortality. Cartamil, D.P., and Lowe, C.G. 2004. Diel movement patterns of ocean sunfish Mola mola off southern California. Mar. Ecol. Acknowledgements Prog. Ser. 266: 245–253. Costello, J.H., and Colin, S.P. 1994. Morphology, fluid motion and We are grateful for the collaborative efforts of the com- predation by the scyphomedusa Aurelia aurita. Mar. Biol. mercial fishermen in Nova Scotia who made this work (Berl.), 121: 327–334. possible, especially H. Fricker, B. Fricker, J. Fricker, Davis, R.W., Fuiman, L.A., Williams, T.M., Collier, S.O., Hagley, B. Mitchell, M. Rideout, and K. Duffy. We thank W. Blan- W.P., Kanatous, S.B., Kohin, S., and Horning, M. 1999. Hunting chard for statistical advice and C. Harvey-Clark for initiating behavior of a marine mammal beneath the Antarctic fast ice. leatherback studies in Nova Scotia. We also thank K. Martin, Science (Washington, D.C.), 283: 993–996. doi:10.1126/science. C. Ryder, B. Schroeder, J. Loch, J. McMillan, D. Bowen, and 283.5404.993. PMID: 9974394. R. Merrick for advice and support, as well as two anonymous den Hartog, J.C., and van Nierop, M.M. 1984. A study on the gut reviewers for their help in improving the manuscript. Funding contents of six leathery turtles Dermochelys coriacea (Linnaeus) for this study was provided by Fisheries and Oceans Canada, (Reptilia: Testudines: Dermochelyidae) from British waters and National Marine Fisheries Service (USA), World Wildlife from the Netherlands. Zool. Verh. (Leiden), 209: 1–36. Fund Canada, Environment Canada, George Cedric Metcalf Dwyer, K., Ryder, C.E., and Prescott, R. 2003. Anthropogenic mor- Charitable Foundation, the Future of Marine Animal Popu- tality of leatherback turtles in Massachusetts waters. NOAA lations program (funded by the Sloan Foundation), and the Tech. Memo. NMFS-SEFSC-503. p. 260. Natural Sciences and Engineering Research Council of Eckert, S.A. 2002. Swim speed and movement patterns of gravid Canada (scholarship to M.C.J. and grants to R.A.M.). leatherback sea turtles (Dermochelys coriacea) at St. Croix, U.S. Virgin Islands. J. Exp. Biol. 205: 3689–3697. PMID: 12409495. References Eckert, S.A., Eckert, K.L., Ponganis, P., and Kooyman, G.L. 1989. Diving and foraging behavior of leatherback sea turtles (Dermo- Acevedo-Gutie´rrez, A., Croll, D.A., and Tershy, B.R. 2002. High chelys coriacea). Can. J. Zool. 67: 2834–2840. feeding costs limit dive time in the largest whales. J. Exp. Biol. Eckert, S.A., Liew, H.-C., Eckert, K.L., and Chan, E.-H. 1996. 205: 1747–1753. PMID: 12042333. Shallow water diving by leatherback turtles in the South China Adler, K. 1976. Extraocular photoreception in amphibians. Photo- Sea. Chelonian Conserv. Biol. 2: 237–243. chem. Photobiol. 23: 275–298. Fedak, M., Lovell, P., McConnell, B.J., and Hunter, C. 2002. Over- Ancel, A., Horning, M., and Kooyman, G.L. 1997. Prey ingestion coming the constraints of long range radio telemetry from ani- revealed by oesophagus and stomach temperature recordings in mals: getting more useful data from smaller packages. Integr. cormorants. J. Exp. Biol. 200: 149–154. PMID: 9023995. Comp. Biol. 42: 3–10. Arai, M.N. 1997. A functional biology of Scyphozoa. Chapman Forward, R.B. 1988. Diel vertical migration: zooplankton photo- and Hall, London. biology and behaviour. Oceanogr. Mar. Biol. Annu. Rev. 26: Arkett, S.A. 1984. Diel vertical migration and feeding behaviour of 361–393. a demersal hydromedusan (Polyorchis penicillatus). Can. J. Fish. Gauthier, S., and Rose, G.A. 2002. Acoustic observation of diel ver- Aquat. Sci. 41: 1837–1843. tical migration and shoaling behaviour in Atlantic redfishes. J. Fish Arkett, S.A. 1989. Hydromedusan photophysiology: an evolution- Biol. 61: 1135–1153. doi:10.1111/j.1095-8649.2002.tb02461.x. ary perspective. In Evolution of the first nervous systems. Graham, R.T., Roberts, C.M., and Smart, C.R. 2005. Diving beha- Edited by P.A.V. Anderson. Plenum Press, New York. viour of whale sharks in relation to a predictable food pulse. J. pp. 373–388. R. Soc. Interface, 3: 109–116. doi:10.1098/rsif.2005.0082. Avens, L., and Lohmann, K.J. 2003. Use of multiple orientation Graham, W.M., Page`s, F., and Hamner, W.M. 2001. A physical con- cues by juvenile loggerhead sea turtles Caretta caretta. J. Exp. text for gelatinous zooplankton aggregations: a review. Hydro- Biol. 206: 4317–4325. doi:10.1242/jeb.00657. PMID: 14581601. biologia, 451: 199–212. doi:10.1023/A:1011876004427. Benovic, A., Lucic, D., Onofri, V., Batistic, M., and Njire, J. 2005. Graham, W.M., Martin, D.L., and Martin, J.C. 2003. In situ quanti- Bathymetric distribution of medusae in the open waters of the fication and analysis of large jellyfish using a novel video profi- middle and south Adriatic Sea during spring 2002. J. Plankton ler. Mar. Ecol. Prog. Ser. 254: 129–140. Res. 27: 79–89. Hansson, L.J. 1997. Capture and digestion of the scyphozoan jelly- Bleakney, J.S. 1965. Reports of marine turtles from New England fish Aurelia aurita by Cyanea capillata and prey response to and Eastern Canada. Can. Field-Nat. 79: 120–128. predator contact. J. Plankton Res. 19: 195–208. Bollens, S.M. 1996. Diel vertical migration in marine zooplakton: Harbison, G.R., Madin, L.P., and Swanberg, N.R. 1978. On the nat- trade-offs between predators and food. Oceanus, 39: 19–28. ural history and distribution of oceanic ctenophores. Deep-Sea Brewer, R.H. 1989. The annual pattern of feeding, growth, and Res. 25: 233–256. sexual reproduction in Cyanea in the Niantic River estuary, Hays, G.C. 2003. A review of the adaptive significance and ecosystem Connecticut. Biol. Bull. (Woods Hole), 176: 272–281. consequences of zooplankton diel vertical migrations. Hydrobio- Buecher, E., Sparks, C., Brierley, A., Boyer, H., and Gibbons, G. logia, 503: 163–170. doi:101023B:HYDR000000847623617b0. 2001. Biometry and size distribution of Chrysaora hysoscella Hays, G.C., Houghton, J.D.R., Isaacs, C., King, R.S., Lloyd, C., (Cnidaria, Scyphozoa) and Aequorea aequorea (Cnidaria, Hy- and Lovell, P. 2004. First records of oceanic dive profiles for drozoa) off Namibia with some notes on their parasite Hyperia leatherback turtles, Dermochelys coriacea indicate behavioural

# 2006 NRC Canada James et al. 765

plasticity associated with long-distance migration. Anim. Behav. puscular diel vertical migrator. Environ. Biol. Fishes, 49: 389– 67: 733–743. 399. doi:10.1023/A:1007369619576. James, M.C., and Herman, T.B. 2001. Feeding of Dermochelys cor- Olesen, N.J., Frandsen, K., and Riisgard, H.U. 1994. Population dy- iacea on medusae in the northwest Atlantic. Chelonian Conserv. namics, growth and energetics of jellyfish Aurelia aurita in a Biol. 4: 202–205. shallow fjord. Mar. Ecol. Prog. Ser. 105: 9–18. James, M.C., and Mrosovsky, N. 2004. Body temperatures of Purcell, J.E. 1992. Effects of predation by the scyphomedusan leatherback turtles (Dermochelys coriacea) in temperate waters Chrysaora quinquecirrha on zooplankton populations in Chesa- off Nova Scotia, Canada. Can. J. Zool. 82: 1302–1306. doi:10. peake Bay, USA. Mar. Ecol. Prog. Ser. 87: 65–76. 1139/z04-110. Purcell, J.E., White, J.R., Nemazie, D.A., and Wright, D.A. 1999. James, M.C., Ottensmeyer, C.A., and Myers, R.A. 2005a. Identifi- Temperature, salinity and food effects on asexual reproduction cation of high-use habitat and threats to leatherback sea turtles and abundance of the scyphozoan Chrysaora quinquecirrha. in northern waters: new directions for conservation. Ecol. Lett. Mar. Ecol. Prog. Ser. 180: 187–196. 8: 195–201. doi:10.1111/j.1461-0248.2004.00710.x. Purcell, J.E., Brown, E.D., Stokesbury, K.D.E., Haldorson, L.H., James, M.C., Myers, R.A., and Ottensmeyer, C.A. 2005b. Beha- and Shirley, T.C. 2000. Aggregations of the jellyfish Aurelia la- viour of leatherback turtles, Dermochelys coriacea, during the biata: abundance, distribution, association with age-0 walleye migratory cycle. Proc. R. Soc. Lond. B Biol. Sci. 272: 1547– pollock, and behaviors promoting aggregation in Prince William 1555. doi:10.1098/rspb.2005.3110. Sound, Alaska, USA. Mar. Ecol. Prog. Ser. 195: 145–158. James, M.C., Eckert, S.A., and Myers, R.A. 2005c. Migratory and Rogers, C.N., Williamson, J.E., Carson, D.G., and Steinberg, P.D. reproductive movements of male leatherback turtles (Dermo- 1998. Diel vertical movement by mesograzers on seaweeds. chelys coriacea). Mar. Biol. (Berl.), 147: 845–853. doi:10.1007/ Mar. Ecol. Prog. Ser. 166: 301–306. s00227-005-1581-1. Schuyler, Q., and Sullivan, B. 1997. Light responses and diel mi- Kideys, A.E., and Romanova, Z. 2001. Distribution of gelatinous gration of the scyphomedusa Chrysaora quinquecirrha in meso- macrozooplankton in the southern Black Sea during 1996–1999. cosms. J. Plankton Res. 19: 1417–1428. Mar. Biol. (Berl.), 139: 535–547. Shoop, C.R., and Kenney, R.D. 1992. Seasonal distributions and Littell, R.C., Milliken, G.A., Stroup, W.W., and Wolfinger, R.D. abundances of loggerhead and leatherback sea turtles in waters 1996. SAS system for mixed models. SAS Institute Inc., Cary, of the northeastern United States. Herpetol. Monogr. 6: 43–67. N.C. Sims, D.W., Southall, E.J., Richardson, A.J., Reid, P.C., and Loose, C.J., and Dawidowicz, P. 1994. Trade-offs in diel vertical Metcalfe, J.D. 2003. Seasonal movements and behaviour of migration by zooplankton: the costs of predator avoidance. Ecol- basking sharks from archival tagging: no evidence of hiberna- ogy, 75: 2255–2263. tion. Mar. Ecol. Prog. Ser. 248: 187–196. Lucas, C.H. 2001. Reproduction and life history strategies of Sims, D.W., Southall, E.J., Tarling, G.A., and Metcalfe, J.D. 2005. the common jellyfish, Aurelia aurita, in relation to its ambi- Habitat-specific normal and reverse diel vertical migration in the ent environment. Hydrobiologia, 451: 229–246. doi:10.1023/ plankton-feeding basking shark. J. Anim. Ecol. 74: 755–761. A:1011836326717. doi:10.1111/j.1365-2656.2005.00971.x. Mackie, G.O., Larson, R.J., Larson, K.S., and Passano, L.M. 1981. Southwood, A.L., Andrews, R.D., Lutcavage, M.E., Paladino, F.V., Swimming and vertical migration of Aurelia aurita (L.) in a West, N.H., George, R.H., and Jones, D.R. 1999. Heart rates and deep tank. Mar. Behav. Physiol. 7: 321–329. diving behaviour of leatherback sea turtles in the eastern Pacific Mills, C.E. 1983. Vertical migration and diel activity patterns of Ocean. J. Exp. Biol. 202: 1115–1125. PMID: 10101109. hydromedusae: studies in a large tank. J. Plankton Res. 5: 619– Tamburri, M.N., Halt, M.N., and Robison, B.H. 2000. Chemically 635. regulated feeding by midwater medusa. Limnol. Oceanogr. 45: Musyl, M.K., Brill, R.W., Boggs, C.H., Curran, D.S., Kazama, 1661–1666. T.K., and Seki, M.P. 2003. Vertical movements of bigeye tuna Weng, K.C., and Block, B.A. 2004. Diel vertical migration of the (Thunnus obesus) associated with islands, buoys, and seamounts bigeye thresher shark (Alopia superciliosus), a species posses- near the main Hawaiian Islands from archival tagging data. Fish. sing orbital retia mirabilia. Fish. Bull. (Washington, D.C.), 102: Oceanogr. 12: 152–169. doi:10.1046/j.1365-2419.2003.00229.x. 221–229. Nelson, D.R., McKibben, J.N., Strong, W.R., Lowe, C.G., Sisneros, Yasuda, T. 1973. Ecological studies on the jellyfish, Aurelia aurita: J.A., Schroeder, D.M., and Lavenberg, R.J. 1997. An acoustic diel vertical migration of the medusa in early fall 1969. Publ. tracking of a megamouth shark, Megachasma pelagios: a cre- Seto Mar. Biol. Lab. 20: 491–500.

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