Scalloped hammerhead sharks swim on their side with diel shifts in roll magnitude and periodicity

Great hammerhead sharks (Sphyrna mokarran) routinely swim on their sides and periodically roll from side to side. A previous study used wind tunnel tests with a rigid model hammerhead shark to demonstrate that the rolling behavior could improve swimming efficiency using the tall first dorsal fin as a lift-generating surface. Scalloped hammerhead sharks (Sphyrna lewini) also have proportionally taller dorsal fins compared to pectoral fins than most shark species and similar to that of great hammerhead sharks, and thus might exhibit similar rolling behavior. This was assessed by deploying multi-sensor accelerometer instrument packages on free-swimming adult scalloped hammerhead sharks to directly measure swimming depth, body orientation and swimming performance. Specific objectives were to (1) determine whether scalloped hammerhead sharks exhibit side swimming and rolling behavior, (2) characterize the patterns of these behaviors, and (3) evaluate the purpose of these behaviors. We obtained 196.7 total days (4720 h) of data from 9 free-swimming adult scalloped hammerhead sharks equipped with multi-instrument biologgers with deployment durations ranging from 7 to 29 days. All sharks exhibited rolling behavior throughout the entire period of observation. The roll angle magnitude and periodicity of rolling showed a clear diel pattern. During daytime, the sharks spent an average of 48% of the time swimming at a roll angle > 30°, with an average roll angle of 41° and rolling periodicity of around 4 min. At night, the sharks spent an average 82% of their time at an angle > 30°, with an average roll angle of 60° and rolling periodicity of around 13 min. In addition to an increase in degree of roll and roll duration, overall dynamic body acceleration (ODBA) also increased at night, and tailbeat frequency was more regular and consistent than during daytime. We observed rolling behavior in scalloped hammerhead sharks similar to that observed in great hammerhead sharks. The diel changes in roll angle and periodicity were accompanied by other changes in swimming behavior. These changes are possibly due to interplay between reducing cost of transport and social interactions with conspecifics.


Background
Most shark species swim in an upright posture with lateral body oscillations, utilizing the dorsal fin for lateral stability and pectoral fins for horizontal stability as well as anterior lift generators that counteract the posterior lift generated by the caudal fin [1][2][3][4]. A study by Payne

Open Access
Animal Biotelemetry *Correspondence: royerm@hawaii.edu 1 Hawai'i Institute of Marine Biology, University of Hawai'i at Mānoa, 46-007 Lilipuna Rd., Kaneohe, HI 96744, USA Full list of author information is available at the end of the article et al. [5] using multi-sensor accelerometer instrument packages observed great hammerhead sharks (Sphyrna mokarran) spend up to 90% of their time swimming on their sides at a roll angle of between 50 and 75°. Great hammerhead sharks are unusual among sharks in having a dorsal fin longer than their pectoral fins, and it was hypothesized that they use this tall first dorsal fin as a liftgenerating surface during side swimming, thus increasing the effective span of the lifting surfaces [5]. Hydrodynamic modeling using empirical data from a rigid model of a great hammerhead shark in a wind tunnel demonstrated that this side swimming behavior could reduce drag relative to lift generation, thus reducing the cost of transport (defined as energy expenditure per distance swum) by about 10% compared to conventional upright swimming [5]. Scalloped hammerhead sharks (Sphyrna lewini) have a similar body plan to great hammerhead sharks, including a tall first dorsal fin that may be longer than their pectoral fins and thus, in theory, could also exhibit side swimming behavior to reduce their transport costs. We deployed multi-sensor accelerometer biologging packages on free-swimming adult scalloped hammerhead sharks to directly measure swimming depth, body orientation and swimming performance. Our objectives were to determine whether scalloped hammerhead sharks exhibit rolling behavior and if so, whether there are any patterns in that behavior and any interplay between rolling behavior and other aspects of swimming performance.

Measurement of body orientation and swimming behavior
To measure body orientation and swimming behavior in scalloped hammerhead sharks, we used an instrument package consisting of a tri-axial accelerometer tag combined with a depth and temperature archiving tag housed in a syntactic foam float (2000 m depth rating) equipped with a timed-release mechanism and Argos satellite-linked telemetry tag to facilitate recovery. The tri-axial accelerometer tag was either a TDR10-XB-340 (56 × 38 × 24 mm 69 g; Wildlife Computers., Redmond, WA) or a TDR10-Daily Diary-278 (74 × 57 × 36 mm, 117 g; Wildlife Computers., Redmond, WA). Tri-axial acceleration was sampled at either 16 Hz or 32 Hz, triaxial magnetometry at 1 Hz, and depth every 5 s using an MK9 archival tag (Wildlife Computers, Redmond, WA). Each package also contained an SPOT5 or SPOT6 Argos satellite-linked transmitter (80 × 20 × 11 mm, 30 g; Wildlife Computers., Redmond, WA) to indicate the package position when it floated to the surface following release from the tagged animal and a VHF transmitter (MM130B; 16 mm diameter, 60 mm length, 20 g; ATS, USA) to facilitate package recovery. Two packages deployed on two separate sharks were equipped with a Little Leonardo video logger (20 × 11 × 52 mm, 16 g; Little Leonardo Co., Tokyo, Japan). The video logger on HH11 was duty-cycled to record for 3 h each day from 5:50 to 8:50 on May 21, 22, 23, 24 and an additional 13 min from 5:50 to 6:03 on the 25th.

Shark capture and handling
All sharks were caught using baited hooks on demersal longlines inside Kāneʻohe Bay (N 21.45°, W 157.80°) on the island of Oʻahu (Hawaiʻi, USA). To ensure captured sharks were in good condition, longlines were checked every 30 min and soak times were kept to less than 2 h. Captured sharks were brought alongside a 5 m skiff and secured with a rope around the caudal peduncle. A hose connected to an in-water bilge pump was inserted into the mouth to provide constant water flow across the gills while the shark was being measured and instrumented. The tag package was attached by a fusible stainless steel cable tie (360 mm, 8 g; Little Leonardo Co., Tokyo, Japan) passed through two holes drilled through the base of the dorsal fin and secured around the syntactic foam float package. Each package contained a timed-release mechanism with a pre-programmed duration (RT-4, 16 mm diameter × 19 mm length 10 g; RT-5, 20 mm diameter × 38 mm length, 20 g; Little Leonardo Co., Tokyo, Japan). Packages were programmed to release after 7 (n = 2), 21 (n = 1), or 23 (n = 8) days. When the countdown timer reached zero, a fusible capsule severed the stainless steel band allowing the package to detach from the shark and float to the surface. Package recovery was accomplished through initial position estimates from Argos satellite transmissions followed by the use of a handheld directional radio receiver tuned to the Argos and VHF transmitter frequencies to guide a chase boat to the floating package. Contact information was also displayed on the packages in case members of the general public found them.
Fin measurements were collected from two of the tagged sharks (HH10, HH11) and two additional opportunistically sampled individuals of similar size. Fin height refers to the perpendicular distance from the fin baseline to the tip of the fin and fin length refers to the distance from the fin origin to the end of the free rear tip (sensu [6]).
Tagging procedures were approved by the ethics committee at the University of Hawaii (Institutional Animal Care and Use Committee Protocol #05-053).

Data processing and analysis
Archived data were downloaded from nine recovered tag packages. All 32-Hz tri-axial acceleration data were resampled at 16 Hz to facilitate analyses. Acceleration and depth data were analyzed using Igor Pro 8 (Wav-eMetrics Inc., Portland, OR, USA) with the 'Ethographer' package [7]. A low-pass filter of 0.3 Hz was used to estimate the static (gravitational) and the dynamic (tail stroking) components of the acceleration signal for each axis. The static acceleration components from the x, y, and z axes were used to calculate the roll angles of the shark, where x is the surge axis, y sway axis, and z the heave axis [8]: To correct for the attachment angle of the tag to each shark, the roll angle data were corrected to 0° centered [9,10]. The mask function in the Ethographer package was used to separate deployment periods into daytime and nighttime observations based on local sunrise and sunset times (Astronomical Applications Department of the U.S. Naval Observatory [11]).
For the purposes of this analysis, we define rolling periodicity as the time taken to transition from upright (vertical) to one side (to a minimum of 30°), back through vertical to the other side at a minimum angle of 30° and back to vertical. This is analogous to the definition of a tailbeat cycle. We used the following metrics to quantify diel variation in rolling behavior during swimming; (1) percent of time spent at a roll angle greater than 30°, (2) the dominant absolute roll angle, and (3) the roll cycle period. The percent of time spent at a roll angle greater than 30° was calculated using the mask feature in Ethographer. An additional mask was used to select all roll data where the absolute roll angle exceeded 30°. The duration of the 30° mask was divided by the total data duration for both the daytime and nighttime. The dominant absolute roll angle was calculated using a probability density histogram plot with 1° bins, with the peak bin designated as the dominant roll angle. The dominant roll period was calculated using a power spectral density plot of the roll data with the peak as the dominant roll frequency which was subsequently converted to roll period. We used paired t tests to compare the mean rolling behavior characteristics during day versus night. Normality was assessed using histograms of mean differences between day and night for each behavior characteristic.
We evaluated potential diel changes in shark swimming activity by comparing day versus nighttime overall dynamic body acceleration (ODBA) and tailbeat frequencies. Both ODBA and tailbeat frequency have been used as proxies for energy expenditure [12][13][14][15][16][17]. We calculated ODBA by summing the absolute values of the dynamic acceleration from all three [surge (x), heave (y), sway (z)] axes [12,13]. Overall day and night averages for ODBA were calculated for each individual by first calculating average ODBA for each day and night and then calculating the overall average and standard deviation across each repeated measure. Tailbeat frequency was calculated from the dynamic component of x-axis (surge) acceleration as this provided the cleanest signal from the three axes. The tailbeat signal was evident in all three axes but the traditionally used sway axis signal was noisier (composite waveform with multiple frequencies) than the surge axis. Tag package wobble and phase differences of between anterior and posterior swaying are possible explanations for the complexity of the dynamic component of the y-axis (sway) acceleration signal. The overall dominant tailbeat frequencies for day and night were calculated using the peak in power spectral density plots for each individual. Tailbeat frequency was further analyzed by generating continuous wavelet transformation spectrograms of the swaying acceleration across the entire deployment (no separation of day and night) for each shark. Sharks periodically made multiple (up to 7) steep nocturnal dives to 600-900 m depth with intense swimming activity (high ODBA, tailbeat frequency and amplitude) occurring during these events. We omitted these deep dive events from our analysis to facilitate comparison of dominant (i.e. non-deep diving) daytime and nighttime swimming behavior. Paired t tests were used to test for significant diel differences in mean ODBA and tailbeat frequency. Normality was assessed using histograms of mean differences between day and night for ODBA and tailbeat frequency.

Instrument deployments and fin measurements
We deployed biologging packages on 11 adult male scalloped hammerhead sharks ranging in size from 204 cm to 270 cm Total Length (TL, Table 1) of which 10 were successfully recovered and 9 recorded accelerometer data. In total, we obtained 196.7 total days (4720 h) of accelerometer and depth data with individual deployment durations ranging from 7 to 29 days (Table 1). For recovered tag packages, horizontal distance from tagging location to pop-up point ranged from 8.1 to 51.1 km, and all packages surfaced within 5 km of the coast of Oʻahu. The package timer for HH11 was set for 7 days but it stayed on the animal for 29 days, possibly due to damage sustained to the wires connecting the stainless belt and release timer. The package for HH3 was programmed for 21 days but was knocked off prematurely 14 days into the deployment. The package from HH11 failed to transmit any satellite or VHF positions due to damaged sustained during deployment but was discovered 248 km away from the tagging location on the shore of the island of Niʻihau approximately 320 days after the expected pop-up time.
We measured the fin sizes of four adult male scalloped hammerhead sharks (two of which were tagged), and all four had dorsal fin heights exceeding pectoral fin heights (Table 2), and indeed larger dorsal to pectoral fin height ratios (1.17:1 average) than great hammerhead sharks [5] (1.07:1,).

Rolling behavior
All sharks exhibited rolling behavior throughout the entire observation period. We found significant diel variation in the duration, magnitude and periodicity of scalloped hammerhead shark rolling behavior. Diel differences were characterized by more extreme roll angles, more time spent side swimming, and longer side swimming bouts during night than day (Figs. 1, 2). Nighttime rolling behavior was more consistent whereas daytime rolling behavior was interspersed with varying periods (several minutes to several hours) of upright swimming. The mean proportion of time spent swimming at a > 30º roll angle increased from 48.1% (± 16.1% SD) during daytime to 82% (± 4.7% SD) at night (Table 3). During daytime, three sharks spent less than half of their time side swimming (HH8 40.8%; HH9 13.7%; HH11 35.3%), whereas at night no shark spent less than 74.3% of the time side swimming at a > 30º roll angle (Fig. 2, Table 3). All nine sharks had a significantly greater mean dominant roll angles at night (average 60.2º, ± 3.5 SD) than during the day (average 40.72°, ± 16 SD) (paired t test, t = − 3.39, df = 8, p = 0.0095). The dominant daytime absolute roll angles ranged from 0.5 to 53.5º. Only one individual (HH9) had a dominant daytime roll angle < 30º.
The dominant nighttime absolute roll angles ranged from 55.5 to 66.5º (Table 3). All sharks except HH3 exhibited a longer dominant roll periodicities at night (average 12.2 min, ± 9.5 SD) than during daytime (average 8.8 min, ± 13.9 SD). HH3 was the only individual observed exclusively in the shallow (< 15 m) confines of Kāneʻohe Bay (based on the depth data and tag pop-up location). No significant diel differences in mean dominant roll periodicity (paired t test, t = − 0.55, df = 8, p = 0.5955) were evident with HH3 in the analysis. However, with HH3 excluded from analysis, mean dominant roll periodicity was significantly greater during night (average = 13.1 min ± 9.7) than day (average = 4.3 min ± 1.9 SD), (paired t test, t = − 3.14, df = 7, p = 0.0164). Side swimming and rolling behavior occurred both while sharks were descending and ascending through the water column and also while swimming at constant depth. All sharks in this study demonstrated a transition between their daytime and nighttime rolling behaviors (Fig. 3) at sunrise and sunset each day.

Swimming performance
Each shark exhibited a diel change in swimming performance, with faster and more consistent tailbeat activity as well as significantly higher ODBA values at night. Grand mean ODBA ranged from 1 ± 0.25 m/s 2 at night to 0.82 ± 0.20 m/s 2 during the day (t = − 6.456, p = 0.0002). Mean tail beat frequency was significantly slower and more variable during the day than at night (paired t test, t = 2.71, df = 8, p = 0.026). Spectral analysis showed an increase in the tailbeat frequency and consistency at night (Fig. 4). The weak (low amplitude) signal during the daytime showed less consistent periods of tailbeat activity and occasional gliding behavior (Fig. 4, Additional files 1, 2, 3, 4).

Video logger
Daytime video footage showed HH11 swimming in a tortuous pattern in the water column and near the seafloor at depths between 50 and 100 m. Video from May 22 thru 25 showed the HH11 associating with two other adult male scalloped hammerhead sharks that could be seen side swimming and turning frequently throughout the footage (see Additional files 3, 4, 5).

Discussion
As predicted by the overall similarity in body plan of the two hammerhead species (i.e. long first dorsal fins compared to pectoral fins and laterally compressed bodies), we found that scalloped hammerhead sharks, like great hammerhead sharks, spend a majority of their time swimming on their side [5]. We predict that other hammerhead shark species with high dorsal to pectoral fin ratios and laterally compressed bodies (which can act as lift-generating surfaces) will also exhibit this behavior whereas side swimming behaviors are probably absent from smaller hammerhead shark species which lack high dorsal:pectoral fin ratios [18]. Measurements of the dorsal and pectoral fins from four adult scalloped hammerhead sharks captured during this study (two of which were tagged) revealed a dorsal fin to pectoral . This is in contrast to previous findings from Clark and Von Schmidt [19] where fin measurements were inferred from a taxonomic key that referenced the range of body lengths of adults and had the heights of the dorsal fins expressed as a percentage of body length. It is possible Clark and Von Schmidt [19] combined morphometric measurements from juvenile and adult individuals and consequently obscured the high dorsal fin ratio characteristic of adult scalloped hammerhead sharks. No observations of rolling behavior have been reported for juvenile scalloped hammerhead sharks but ontogenetic changes in characteristics such as buoyancy and fin aspect ratios may gradually shift their hydrodynamic characteristics until this behavior emerges [20,21]. Identifying the ontogenetic onset of side swimming will help to more clearly understand how this behavior is adaptive for hammerhead sharks. We found clear diel rhythms in the swimming posture and gait of adult scalloped hammerheads sharks with more side swimming, greater roll angles, higher activity and more consistent tail beating at night than during the day. Diel changes in swimming behavior may reflect shifts between daytime social interactions [22][23][24] and nocturnal traveling, with the later consisting of more directional swimming. Scalloped hammerhead sharks are known to form large daytime aggregations at fixed locations and then disperse over a more extensive area at night (e.g. [22][23][24]). Maintaining school cohesion and social interactions at a fixed location during daytime may require more tortuous swimming, modulation of rolling behaviors and periods of passive gliding. These daytime behaviors were observed in footage from the video logger on HH11, when it was swimming with a group of conspecifics on 4 consecutive days (Fig. 5, Additional files 1, 2, 3, 4, 5).
Similarities in side swimming behavior and morphology between great hammerhead [5] and scalloped hammerhead sharks [this study] provide interesting insight into the evolution of novel morphological traits and behavior of large hammerheads. The side swimming behavior exhibited in large hammerhead sharks is probably a "recent" locomotor strategy enabled by the derived body plan (including fin size and placement) of these divergent species [5,25]. The ability to maximize locomotor efficiency during sustained swimming and prey capture is crucial for managing energy budgets and exerts strong selective pressure [26,27]. It is likely that the reconfiguration of the fins during locomotion allows for large hammerheads to utilize their morphology for maneuvering events and for efficient directional  swimming. Both species are noted for their maneuverability, making rapid tight turns when chasing and subduing prey [18,[28][29][30][31]. In their upright posture, they can maximize their maneuverability potential, conducting rapid tight turns while keeping their body level, due to their lateral flexure, head shape, anhedral pectoral fin positioning, and large dorsal fin [2,18,28] (Fig. 5).
Both species are also known to conduct long-distance migrations [32][33][34][35][36]. These species, when cruising, swim at a rolled angle, utilizing the dorsal fin and high pectoral fin as lift-generating surfaces and thus increase their effective lift span compared to normal upright swimming. Scalloped hammerhead sharks exhibited nighttime roll angles within the range (between 50° and 70°) of those predicted to provide the lowest cost of transport for great hammerhead sharks [5] ( Table 3, Figs. 1, 2, 3). Given the similar body plans of these two hammerhead shark species, both may be reducing cost of transport by side swimming. This hypothesis could be tested through hydrodynamic modeling using wind tunnel tests on a morphologically accurate model of a scalloped hammerhead shark, such as those conducted by Payne et al. [5].
Other hydrostatic and hydrodynamic properties of the body configuration during side swimming that could be examined include shifts in the center of gravity [21,27], shifts in the dihedral of control surfaces [37,38], and phase relationships of body undulations and control surfaces [27]. Future studies using accelerometer biologgers on other large hammerhead shark species (e.g. smooth hammerhead shark (Sphyrna zygena), Carolina hammerhead shark (Sphyrna gilberti) [39]) will reveal whether side swimming behavior is ubiquitous among all large hammerhead shark species.

Conclusion
Like great hammerhead sharks, scalloped hammerhead sharks swim at a rolled angle. The deployments of highresolution accelerometer tags on 9 adult male scalloped hammerhead sharks for 7 to 29 days revealed distinct diel variation in rolling behavior and swimming performance. At night, the sharks spend a higher proportion of their time side swimming, with longer bouts on each side and more extreme roll angles. Scalloped hammerhead sharks are also more active and swim more steadily during night than day. Swimming behaviors at night are likely driven primarily by reducing cost of transport during steady swimming whereas daytime behavior is likely a compromise between reducing cost of transport and other factors such as social interactions between conspecifics. The suite of changes in posture and swimming performance that occur on a diel basis support the concept that side swimming enhances swimming efficiency by generating lift from the dorsal fin. These phenomena are underpinned by the form and function of the recent derived body plan of large hammerhead sharks.