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Abstract

Locomotory muscle function of ectothermic fishes is generally depressed in cold waters, making them vul-nerable to avian and mammalian predators whose body temperature remains high. Paradoxically, Greenland sharks Somniosus microcephalus exhibit the reverse of this usual predator–prey thermal pattern by apparently hunting seals in Arctic waters. To examine whether this species possesses cold-adaptations that enhance its swimming performance, we used data-logging tags to measure swim speed and tail-beat frequency (which reflects muscle-shortening speed) of six free-swimming sharks (204–343 kg). For comparison, we compiled these parameters for wild fishes from the literature over a wide body mass range (0.2–3900 kg) and examined the scaling relationships using phylogenetically informed statistics. The sharks cruised at 0.34 m·s − 1 with a tail-beat frequency of 0.15 Hz, both of which were the lowest values for their size across fish species. The mean and maximum speed (0.74 m·s − 1) and acceleration during burst swimming (0.008 m·s − 2) were much lower than those of seals. Our results indicate that the swimming performance of Greenland sharks is limited by cold waters (~2 °C) and insufficient to catch swimming seals. However, Arctic seals sleep in water to avoid predation by polar bears Ursus maritimus, which may leave them vulnerable to this cryptic slow-swimming predator.

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... The swimming speed is thus intrinsically linked to the oscillation frequency, but unlike the aforementioned scaling laws that follow clear and widely documented trends over several orders of magnitude in length, no consensus has been reached on the law that sets the tail beat frequency. Most studies agree that the frequency decreases with the length [5] and scaling laws f ∼ L −n with an exponent n ranging between 0.5 and 1 are often reported together with models referring to biological constraints, to the hydrodynamic interactions of the swimmer with its environment or even to the effect of gravity [15][16][17][18][19]. The difficulty of establishing a clear law and identifying the mechanisms at play is related to the fact there is only a factor of 100 between the highest frequency recorded in the smallest fish and the lowest frequency recorded in the largest cetaceans, typically 20 and 0.2 Hz respectively ( Fig. 1), while measurements show a large dispersion for a given length. ...
... Finally, we now understand why there are so many different exponents in the literature resulting from attempts to describe the frequency-length relationship as a scaling law (e.g., in [15][16][17][18][19]). Special attention must be paid to the analysis of a range of lengths, because 1) the scaling laws are only valid in either of the two limiting regimes and 2) the data must be measured at the same activity level for the comparison to be meaningful. ...
... This can lead to deviations from the main trend at extreme temperatures. This is probably the main explanation of the surprising low tail beat frequency of Greenland sharks in Arctic waters (L 3 m and f 0.15 Hz in Fig. 1), a factor of 2-3 below the fit of the slow bound [17]. Conversely, there are examples of thermal acclimation of fish in warm waters that could lead to f 0 values as high as 50 Hz [47]. ...
Preprint
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Due to its great efficiency and maneuverability, undulatory swimming is the predominant form of locomotion in aquatic vertebrates. A myriad of animals of different species and sizes oscillate their bodies to propel themselves in aquatic environments with swimming speed scaling as the product of the animal length by the oscillation frequency. Although frequency tuning is the primary means by which a swimmer selects its speed, there is no consensus on the mechanisms involved. In this article, we propose scaling laws for undulatory swimmers that relate oscillation frequency to length by taking into account both the biological characteristics of the muscles and the interaction of the moving swimmer with its environment. Results are supported by an extensive literature review including approximately 1200 individuals of different species, sizes and swimming environments. We highlight a crossover in length around 0.5-1 m. Below this value, the frequency can be tuned between 2-20 Hz due to biological constraints and the interplay between slow and fast muscles. Above this value, the fluid-swimmer interaction must be taken into account and the frequency is inversely proportional to the length of the animal. This approach predicts a maximum swimming speed around 5-10 m.s$^{-1}$ for large swimmers, consistent with the threshold to prevent bubble cavitation.
... Despite the predicted high abundance of Greenland sharks throughout Baffin Bay and their vulnerability to incidental capture by commercial and Inuit community fisheries (Idrobo and Berkes, 2012;Bryk et al., 2018;Madigan et al;in press), Greenland shark distribution and the timing of movements throughout the basin remain unknown. While exhibiting the slowest observed mean swim speed (0.34 ms -1 ) and tailbeat frequency (0.15 Hz) relative to body size for any fish species (Watanabe et al., 2012), Greenland sharks are capable of undertaking extensive horizontal movements (Campana et al., 2015a;Hussey et al., 2018) and maintain a broad distribution throughout the coastal and offshore waters of Baffin Bay (MacNeil et al., 2012). Given their current designation as the world's longest-lived vertebrate (Nielsen et al., 2016), and the fact that they possess other Kselected life history traits such as low fecundity, slow growth (0.5 cm yr -1 ; Hansen, 1963), and an extremely low metabolic rate (Ste-Marie et al., 2020), appropriate management of this species is a priority (Davis et al., 2013;Edwards et al., 2019). ...
... An average swim speed of 0.34 ms -1 (range <0.17-0.73 ms -1 ) for Greenland sharks (Watanabe et al., 2012). iii. ...
... Given the nominal delay of our acoustic tags and the average swimming speed of Greenland sharks (0.34 ms -1 , range = <0.17 -0.73 ms -1 ; Watanabe et al., 2012), the predicted time for an individual to transit on a linear path through the widest point of the detection radius of a receiver was calculated to be 4,717.65 sec (~1.31 h, range = 2,167.57 ...
Article
Full-text available
Variable movement strategies can complicate the conservation and management of mobile species. Given its extreme life history traits as a long-lived, deep-water species, the Greenland shark ( Somniosus microcephalus ) is vulnerable to fisheries bycatch, but little is known over its long-term movements across a spatially and seasonally variable Arctic environment. To address this knowledge gap, the movements of Greenland sharks in coastal fjords and offshore waters of Baffin Bay were examined using seven years of acoustic telemetry data. Seasonal patterns in broad-scale movements and inshore-offshore connectivity were compared among 155 sharks (101 males, 54 females [mean LT = 2.65 ± 0.48 m, range 0.93-3.5 m]) tagged in 6 discrete coastal locations spanning from Grise Fiord to Cumberland Sound (Nunavut). Sharks exhibited transient movements throughout coastal and offshore regions with some evidence of seasonally recurring hotspots revealed by repeat detections of individuals at sites over multiple years. Shark presence in coastal fjords occurred exclusively during the coastal ice-free period (July to November), regardless of the location of tagging or detection, while presence in the offshore was recorded during the period of ice re-formation and cover (November to July). Through multi-year telemetry, it was possible to reveal repetitive patterns in broad-scale habitat use for a complex marine predator with direct relevance for understanding the seasonal distribution of mobile Arctic consumers and informing regional fisheries management.
... We then integrated FMR estimates with published diet and abundance data to estimate the prey consumption rates of this Arctic predator on locally and commercially valuable species at both the individual and local population level. Given their generally lethargic lifestyle (Watanabe et al., 2012), we predicted that individual sharks would have relatively low FMRs and that this would translate into low prey consumption needs, especially when compared with their tropical counterparts or local endothermic predators. ...
... The effect of TBF on oxygen consumption rate for Greenland sharks was approximated using the mass-specific slope (20.22) of an interpolated linear relationship connecting the active routine metabolic rate for one individual (aRMR at TBF=0.18 Hz) studied in a large circular respirometer to its rRMR (i.e. its oxygen consumption rate at TBF=0 Hz; Ste-Marie et al., 2020). Though activity cost equations for other shark species have been derived using data for multiple individuals across a range of swim speeds, we opted to use one derived from the limited Greenland shark data because of the highly variable effect of activity on the energetics of different species (Lear et al., 2017), as well as the differing fin morphology and swimming behaviour of our focal species (Watanabe et al., 2012;Iosilevskii and Papastamatiou, 2016). Moreover, the shark used to derive our activity scaling slope was closer in body size (126 kg) to the wild sharks for which we were estimating FMR (range 33-367 kg). ...
... Conversely, a large and slow moving ectothermic predator such as the Greenland shark, requiring much less energy to fuel its metabolism, may be able to survive extended periods of time between feeding events (Furey et al., 2016), allowing it to thrive in areas with scarce or unpredictable resource availability, and possibly accounting for a presumably much lower success rate in cases of active predation (Norberg, 1977). While scavenging is generally considered the primary foraging strategy for Greenland sharks consuming large mobile prey, anecdotal accounts from indigenous harvesters, evidence from closely related pacific sleeper sharks, and the biologged burst-swimming events lasting several minutes recorded here (Fig. 3, assessed by TBF) suggest active predation may also represent an important foraging strategy (MacNeil et al., 2012;Watanabe et al., 2012;Horning and Mellish, 2014). ...
Article
Field metabolic rate (FMR) is a holistic measure of metabolism representing the routine energy utilization of a species living within a specific ecological context, thus providing insight into its ecology, fitness and resilience to environmental stressors. For animals which cannot be easily observed in the wild, FMR can also be used in concert with dietary data to quantitatively assess their role as consumers, improving understanding of the trophic linkages that structure food webs and allowing for informed management decisions. Here we modeled the FMR of Greenland sharks (Somniosus microcephalus) equipped with biologger packages or pop-up archival satellite tags (PSATs) in two coastal inlets of Baffin Island (Nunavut) using metabolic scaling relationships for mass, temperature and activity. We estimated that Greenland sharks had an overall mean FMR of 21.67±2.30 mgO2h−1kg−0.84 (n=30; 1-4 day accelerometer package deployments) while residing inside these cold-water fjord systems in the late summer, and 25.48±0.47 mgO2h−1kg−0.84 (n=6; PSATs) over an entire year. When considering prey consumption rate, an average shark in these systems (224kg) requires a maintenance ration of 61-193g of fish or marine mammal prey daily. As a lethargic polar species, these low FMR estimates, and corresponding prey consumption estimates suggest Greenland sharks require very little energy to sustain themselves under natural conditions. These data provide the first characterization of the energetics and consumer role of this vulnerable and understudied species in the wild, essential given growing pressures from climate change and expanding commercial fisheries in the Arctic.
... rostratus (Risso, 1827). The most well-studied species within the genus is the Greenland shark S. microcephalus, which is distributed in the North Atlantic and adjacent Arctic with a wide vertical distribution range from the surface to the deep sea and a maximum habitat depth of 2992 m (Watanabe et al., 2012;Mecklenburg et al., 2018). The species reaches up to 375 cm in total length (TL) for males and 550 cm TL for females (Mecklenburg et al., 2018). ...
... The swimming speed of the Greenland sharks has been analysed using several different techniques. Watanabe et al. (2012) measured it using data loggers attached to shark bodies. The sharks cruised at 0.34 m s −1 with a tail-beat frequency of 0.15 Hz, both of which were the lowest values across all fish species, adjusted for their size; reportedly, the swimming performance of Greenland sharks was limited by cold waters (∼2°C) (Watanabe et al., 2012). ...
... Watanabe et al. (2012) measured it using data loggers attached to shark bodies. The sharks cruised at 0.34 m s −1 with a tail-beat frequency of 0.15 Hz, both of which were the lowest values across all fish species, adjusted for their size; reportedly, the swimming performance of Greenland sharks was limited by cold waters (∼2°C) (Watanabe et al., 2012). The swimming speed of Greenland sharks was also estimated from video analyses, which showed the average swimming speed of 0.27 m s −1 (SD = 0.07; range 0.15-0.42 ...
Article
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The Pacific sleeper shark Somniosus pacificus is one of the largest predators in deep Suruga Bay, Japan. A single individual of the sleeper shark (female, ~300 cm in total length) was observed with two baited camera systems deployed simultaneously on the deep seafloor in the bay. The first arrival was recorded 43 min after the deployment of camera #1 on 21 July 2016 at a depth of 609 m. The shark had several remarkable features, including the snout tangled in a broken fishing line, two torn anteriormost left-gill septums, and a parasitic copepod attached to each eye. The same individual appeared at camera #2, which was deployed at a depth of 603 m, ~37 min after it disappeared from camera #1 view. Finally, the same shark returned to camera #1 ~31 min after leaving camera #2. The distance between the two cameras was 436 m, and the average groundspeed and waterspeed of the shark were 0.21 and 0.25 m s ⁻¹ , respectively, which were comparable with those of the Greenland shark Somniosus microcephalus (0.22–0.34 m s ⁻¹ ) exhibiting the slowest comparative swimming speed among fish species adjusted for size. The ambient water temperature of the Pacific sleeper shark was 5.3 °C, which is considerably higher than that of the Greenland shark (~2 °C). Such a low swimming speed might be explained by the ‘visual interactions hypothesis’, but it is not a consequence of the negative effects of cold water on their locomotor organs.
... One important aspect that has not yet been very well studied is the swimming capabilities of deep-sea sharks. The swimming capability of an organism in the ocean has essential implications in survival behaviors such as hunting, escaping, migrating, and mating (Watanabe et al., 2012;Wilson et al., 2005). Swimming capability will also largely dictate the home range of a species (Sainte-Marie and Hargrave, 1987). ...
... Shadwick et al. (2016) split the swimming speeds of fishes into two main types: The first is linked to burst activitieswhen fishes reach their maximum velocity quickly during hunting or escaping behaviors. The second is linked to cruise activities, and is used by fishes to travel long distances during the most common locomotion activities such as foraging, dispersal, locating a mate or circadian migration (Ryan et al., 2015;Watanabe et al., 2012). ...
... In contrast, few studies have looked at swimming behaviors of deep-water sharks. These sharks are often described as slow and listless swimmers (Condon et al., 2012;Treberg et al., 2003;Bagley et al., 1994), as for the Greenland shark recorded as the slowest (Watanabe et al., 2012) but some of them still perform long vertical migration such as Centrophorus squamosus (Rodríguez-Cabello et al., 2016;Rodriguez and Sanchez, 2014). Two main hypotheses have been put forward to explain this. ...
Article
Currently the ecology of deep-water sharks is poorly documented, especially in situ information for these elusive species are lacking. In this study, stereo-Baited Remote Underwater Videos (stereo-BRUVs) were deployed to collect ecological data from New Zealand deep-sea sharks. The results showed differences in abundance between species, with Etmopterus granulosus (Etmopteridae) found in greatest numbers. Moreover, the known depth range increased for Scymnodon macracanthus (Centrophiridae). Deep-sea shark species were generally found to swim at slower cruise speeds (0.36 ± 0.04 m s⁻¹) than their shallow-water counterparts (0.63 ± 0.05 m s⁻¹). However, the swimming speed of deep-sea sharks was clearly not uniform, with some species displaying higher cruise swimming speeds than others. The fastest sharks (Centrophorus harrissoni, Etmopterus granulosus and Etmopterus molleri) had swimming abilities comparable to benthic shallow water sharks (0.48 ± 0.02 m s⁻¹). The higher cruise swimming speed in the family Etmopteridae could be an advantage for these luminous sharks if they follow isolumes to match their ventral light intensity with the down-welling light of their environment. This study revealed that alternative non-destructive methods can be effective for ecological studies of deep-sea marine fauna.
... Accelerometers attached to animals can provide fine scale tri-axial data on organismal movements to examine animal interactions when combined with location data streams such as GPS satellite tags. The majority of accelerometer work to date has focused on biomechanical research, activity budgets and intricate behaviours such as feeding (Broell et al., 2013;Noda et al., 2013;Yedsen et al., 2014), swimming (e.g., Sato et al., 2007;Watanabe et al., 2012;Broell et al., 2015), or post release/survival behaviour (Brownscombe et al., 2014). Limited work has used accelerometers to examine the behavioural response to aquatic animal interactions (but see Wilson et al., 2015) largely as a result of the difficulty of either tagging sufficient individuals within a group (with GPS location data) or knowing the accurate locations of animals and/or contact ranges between individuals (when using acoustic telemetry). ...
... The biologging package consisted of a VMT (18 cm x 3 cm, 180 g in air, VEMCO), an accelerometer (2.54 cm x 8 cm, 67 g in air; 100 Hz sampling frequency, ±6 g 0 , Maritime bioLoggers Inc, Halifax, Nova Scotia) and a temperature-pressure tag (DST-TD, 4.6 cm x 1.3 cm, 19 g in air; 1/3 Hz sampling, Star:Oddi, Iceland), along with an instrument-recovery package (Fig. S1) that included a timescheduled release mechanism (11.5 g, Little Leonardo Co., Tokyo, Japan; Watanabe et al., 2004), high-density float (10 cm x 9.5 cm x 5.5 cm, 166g), VHF transmitter (55 mm x 0.7 cm, 18g, ATS Track, Isanti, Minnesota, USA) and an ARGOS transmitter (SPOT-5, 10.6 cm x 4.5 cm x 1.9 cm, 53g, Wildlife Computers, Redmond, Seattle, USA). The total package weight in air was 514 g or 0.13 -0.31% of the estimated body mass of the Greenland sharks according to Watanabe et al., (2012). To attach the package, the skin anterior to the head of the shark was pierced shallowly using a metal needle, and a plastic cable (4 mm in width) was passed through the hole and around the data package to secure it firmly against the animal (Supporting Information Fig. S1). ...
... Following the release of the package, it floated to the surface, transmitted an ARGOS satellite signal and produced a detectable VHF signal. A maximum three-day deployment period was chosen to ensure a feasible search area (< 60 km from the tagging region) based on previously documented movements and swimming speeds of Greenland sharks (Hussey unpublished data; Watanabe et al., 2012). ...
Article
Interactions between animals structure food webs and regulate ecosystem function and productivity. Quantifying sub‐surface behavioural interactions among marine organisms is challenging, but technological advances are promoting novel opportunities. Here, we present a framework to estimate when there is a high likelihood that aquatic animal sub‐surface interactions occur and test for a movement‐related behavioral response to those interactions over short temporal scales (days) using a novel multi‐sensor biologging package on a large marine predator, the Greenland shark (Somniosus microcephalus). We deployed a recoverable biologging package combining a VEMCO Mobile Transceiver (VMT), accelerometer and a Temperature‐Depth (TD) tag to quantitatively assess fine‐scale behaviour during detection events, i.e. when sharks carrying the novel VMT package (animalR, n = 3) detected sharks independently tagged with transmitters in the system (animalT, n = 29). Concurrently, we developed simulations to estimate the distances between animalR and animalT by accounting for their swim speed, the estimated detection efficiency of the VMT, and the number of consecutive transmissions recorded. Accelerometer‐derived activity indices were then used as a means to test for response to potential interactions when animals are expected to be in close proximity. Based on this approach, the three VMT equipped Greenland sharks exhibited higher body acceleration and greater depth changes during detections, suggesting a potential behavioural response to the presence of other sharks. A Generalized Additive Model (GAM) indicated a moderate increasing relationship in activity associated with a greater number of animalT detections. Through the proposed framework, detection events with varying probabilities of interaction likelihoods can be derived and those data isolated and explicitly tested using acceleration data to quantify behavioral interactions. Through inputting known parameters for a species of interest, the framework presented is applicable for all aquatic taxa and can guide future study design.
... An increase in foliation is correlated with an increase in cerebellum size, brain size, and body size (Table S3) across this group, where S. microcephalus, in particular, showed a marked deviation from expectation (Fig. 5). The lack of cerebellar complexity may reflect a reduction in fine-tuned motor behavior 26,30 , as Greenland sharks exhibit the slowest swimming speed for their body size compared to other representative cartilaginous fishes 59 . Tail beat frequency data also suggests a sluggish cruising speed of between 0.22 and 0.34 m/s 58,59 and a maximum speed of 0.74 m/s 59 for S. microcephalus, which is much slower than those estimated for species such as C. carcharias 120,138 and G. cuvier 139,140 . ...
... Previous studies speculated that S. microcephalus may actively feed at ice holes (e.g. on over wintering Delphinapterus leucas 46 ) and could be attracted to seal ice holes via a suite of olfactory, acoustic and visual cues, possibly using stealth and camouflage to approach and capture seals at the surface 58 . Other research suggest that Somniosus sp. may ambush sleeping seals 59,68 . Arctic seals often sleep in water, either underwater or at the surface 141,142 . ...
... Arctic seals often sleep in water, either underwater or at the surface 141,142 . It has been hypothesized that this sleeping behavior allows them to avoid predation by polar bears (Ursus maritimus) that feed on seals primarily on the sea ice 59,68 . However, unlike cetaceans or otariids, who employ unique unihemispheric sleep patterns as a means to remain active while one half of the brain is in a sleeping state 143,144 , phocid seals exhibit bilaterally symmetrical (bihemispheric) sleep patterns, characteristic of terrestrial mammals 141 . ...
Article
Full-text available
In cartilaginous fishes, variability in the size of the brain and its major regions is often associated with primary habitat and/or specific behavior patterns, which may allow for predictions on the relative importance of different sensory modalities. The Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic and are among the longest living vertebrates ever described. Despite a presumed visual impairment caused by the regular presence of parasitic ocular lesions, coupled with the fact that locomotory muscle power is often depressed at cold temperatures, these sharks remain capable of capturing active prey, including pinnipeds. Using magnetic resonance imaging (MRI), brain organization of S. microcephalus and S. pacificus was assessed in the context of up to 117 other cartilaginous fish species, using phylogenetic comparative techniques. Notably, the region of the brain responsible for motor control (cerebellum) is small and lacking foliation, a characteristic not yet described for any other large-bodied (>3 m) shark. Further, the development of the optic tectum is relatively reduced, while olfactory brain regions are among the largest of any shark species described to date, suggestive of an olfactory-mediated rather than a visually-mediated lifestyle.
... The water depth of the shark's habitat is assumed to be chosen actively and dependent on the ambient water temperature (Stokesbury et al., 2005). According to measurements from data loggers that were attached to Greenland sharks (Watanabe et al., 2012), specimens longer than 2.5 m prefer water temperatures between À1.2 and 3.4°C, which correspond to water depths <270 m. Dietary studies based on stable isotopes, ubiquitous pollutants and stomach contents imply that the Greenland shark feeds at a high trophic level which can vary with size (Fisk et al., 2002). ...
... The shark focuses on pelagic and benthic resources (Fisk et al., 2002;McMeans et al., 2010) and occasionally feeds on terrestrial animals such as polar bears (McMeans et al., 2010). Following the concept of aerobic red muscle (RM) endothermy (Watanabe et al., 2015), the Greenland shark's slow cruising speed (Watanabe et al., 2012;their Fig. 3) suggests a low heat production. Teeth from ectothermic sharks are interpreted to reflect the ambient water temperature because of their permanent exposure to seawater during growth. ...
... Teeth from ectothermic sharks are interpreted to reflect the ambient water temperature because of their permanent exposure to seawater during growth. According to the size of the investigated specimen and logger data (Watanabe et al., 2012) the temperature of mineral precipitation is considered to be 1 ± 2°C. ...
Article
Clumped isotope data from carbonated apatite from in vivo and in vitro samples are presented to refine the relationship between mineral growth temperature and carbonate clumped isotopic composition (Δ 47 ). Δ 47 , δ ¹⁸ O and δ ¹³ C data were obtained from phosphoric acid digestion (T = 110 °C) of chemically untreated teeth from an African elephant, Greenland sharks, sand tiger sharks and synthetic apatites. These data cover a temperature range between 1 °C and 80 °C and enlarge the calibration dataset presented in Wacker et al. (2016) by a factor of five. Taxon-specific analyses of tooth enamel(oid) and dentine reveal that both tissues show identical Δ 47 values even though the content of organic matter differs by an order of magnitude. The following Δ 47 temperature calibration for (bio)apatite is derived (R ² = 0.9924, p-value < 0.0001, n = 122; 8 samples): Δ 47CDES110 =0.0325(±0.0012)×10 ⁶ /T ² +0.2137(±0.0124)(withTinKandΔ 47 in‰) This calibration becomes indistinguishable from a reprocessed empirical calibration of calcite made in the same laboratory if a difference of the acid fractionation factors (AFF) of 0.110‰ between 25 °C and 110 °C is considered. The measured AFF for bioapatite matches the one that is extrapolated from experimental data on calcite and aragonite. The oxygen isotope fractionation between structural carbonate in the synthesized carbonated hydroxylapatites (CHAP) and water between 7 °C and 80 °C closely follows the temperature dependence for the calcite-water system. It is described by the following (CHAP-water) equation (R ² = 0.997, p-value < 0.04, n = 17; 3 samples): 1000ln(α CHAP-water )=17.23±0.59×10 ³ ×T ⁻¹ -27.28(±1.73)(withTinK) Both calibrations are applied to shark teeth from a modern Greenland shark and a fossil megatooth shark (Carcharodon megalodon) specimen to reconstruct the apparent Δ 47 -based habitat temperature of C. megalodon (19 ± 4 °C) and the oxygen isotopic compositions of seawater.
... For decades, scientists have emphasized the discrepancy between the lethargic appearance of the 239 Greenland shark and the fast swimming animals found in its stomach, and further speculated if Greenland 240 sharks mainly catch their prey actively or by scavenging Hansen 241 1963. Greenland sharks are indeed slow swimmers (Watanabe et al. 2012) and will feed on carcasses 242 whenever possible (Beck & Mansfield 1969, Leclerc et al. 2011). Yet many studies conclude that Greenland 243 sharks must be capable of catching live seals and fast-swimming fishes despite the lack of any concrete 244 evidence or direct observations (see Leclerc et al. 2012, Lucas & Natanson 2010, 245 Nielsen et al. 2014. ...
... Neither did we observe any scavenging fauna in the 254 sharks' stomachs, such as brittle stars, lysianassid amphipods, hagfish, snails or crabs, which could be 255 expected if the seals had been found by the shark as carcasses on the ocean floor (Leclerc et al. 2012, 256 Nielsen et al. 2014. We therefore hypothesize that these two seals were hunted actively by the Greenland 257 shark, although it raises the question; how is a slowly swimming Greenland shark (Watanabe et al. 2012) 258 routinely capable of catching fast swimming fishes, seals and small whales in open and ice-covered waters? 259 Leclerc et al. 2012 suggest predation on sleeping seals in the water column but such still remains to be 260 verified. ...
... On a daily basis, vertical excursions of sharks 290 from Graedefjord typically ranged 150-250 m, whereas sharks from Bredefjord and Julianehåbsfjord 291 typically ranged from 350-500 m in depth. One shark exhibited as much as 896 m in daily depth difference 292 while covering a total of 9,273 vertical meters (Shark #9, 13 June 2017, Fig 2d) suggesting that Greenland 293 sharks might be slow swimmers (Watanabe et al. 2012), but can be very active when searching for prey. For 294 ...
Thesis
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This PhD project has aimed at investigating longevity of the Greenland shark. The largest Greenland sharks measure at least 550 cm, and ever since Poul Marinus Hansen in 1963 presented that a recaptured medium-sized Greenland shark had grown 8 cm in 16 year, longevity of the species has been subject for speculation. Conventional age determination techniques for teleost or elasmobranchs are not applicable on the Greenland shark and its longevity has thus remained a mystery for decades. Inspired by alternative age estimation techniques applied on other sharks and whales, I have used bomb radiocarbon dating and a Bayesian calibration model to estimate longevity of the Greenland shark. The analyzed tissue stems from the eye lens nucleus – unique material which presumably reflects age 0 of the shark, as it has not undergone metabolic changes during the animal’s life. By studying 28 Greenland shark females between 81 cm and 502 cm, I estimate the oldest shark to be between 272 years and 512 years. With an estimated lifespan of at least 272 years, the Greenland shark is the longest living vertebrate animal in the world. In order to produce these age estimates, it has been necessary to study the carbon source of the eye lens nucleus in more detail. The center of the nucleus consists of proteins and the analyzed tissue stems from the diet of the shark’s mother. From feeding ecology and satellite tracking, I have therefore investigated adult females. Sharks of this life stage mainly occupied continental shelf waters in southern Greenland at depths between 200 and 550 m and fed primarily on cod, redfish and seals. From previous investigations of predatory sharks and whales in the north Atlantic, bomb radiocarbon has been widely applied, and I argue that a similar calibration approach is valid to use on the Greenland shark. The main aim of this thesis is to clarify the biological assumptions behind the radiocarbon dating leading to the age estimates of the Greenland shark. These age estimates rest on classical biological feeding ecology studies, chemical isotope analysis and advanced mathematical modelling. This interdisciplinary approach has been crucial for the success of the project. The thesis also illustrates how a novel cross-combination of techniques can be applied on other marine species difficult to age determine, and how the Greenland shark is unique to the arctic ecosystem. Many aspects of the basic biology of the Greenland shark remain mysterious.
... Greenland sharks (Somniosus microcephalus) live in deep, cold water in high northern latitudes, grow to a large size (>5m), have a lifespan of hundreds of years (Hansen, 1963;Nielsen et al., 2016) and appear to be very sluggish with little capacity for sustained high speed swimming (Compagno et al., 2005;Watanabe et al., 2012, Nielsen et al., 2016. Although one of the largest extant marine fish, knowledge of their life history, ecology and physiology is very limited (MacNeil et al., 2012;Herbert et al., 2017, Costantini et al., 2017. ...
... There are virtually no in vivo measurements of physiological parameters from this species, due to the difficulty of obtaining and handling specimens. Field studies using accelerometers reveal very slow sustained swim speeds (< 0.2 body length s -1 ), with tail beat frequencies on the order of only a few per minute (Skomal and Benz, 2004;Watanabe et al., 2012). Based on all these features we expect blood pressure in S. microcephalus to be relatively low compared to other sharks, even low-activity ones such as catsharks. ...
... Combining results from the two methods predicts mean ventral aortic blood pressure for S. microcephalus of 2.3-2.8kPa. We believe this is lower than blood pressures observed in any other elasmobranch, and fits with the expectations that this species is slow moving and has a relatively low aerobic metabolism (MacNeil et al., 2012;Watanabe et al. 2012). For comparison, in vivo studies report ventral aortic blood pressures from slow swimming sharks of 3.9 and 5.3kPa (epaulette shark, Hemiscyllium ocellatum; Speers-Roesch et al., 2012, and catshark, Scyliorhinus canicula;Taylor et al. 1977, respectively), from more active species of 5.1-6.8kPa ...
Article
Full-text available
We conducted in vitro inflations of freshly excised ventral aortas of the Greenland shark, Somniosus microcephalus, and used pressure-diameter data to estimate the point of transition from high to low compliance, which has been shown to occur at the mean blood pressure in other vertebrates including fishes. We also determined the pressure at which the modulus of elasticity of the aorta reached 0.4MPa, as occurs at the compliance transition in other species. From these analyses we predict the average ventral aortic blood pressure in S. microcephalus to be about 2.3-2.8kPa, much lower than reported for other sharks. Our results support the idea that this species is slow moving and has a relatively low aerobic metabolism. Histological investigation of the ventral aorta show that elastic fibres are present in relatively low abundance and loosely connected, consistent with this aorta to have high compliance at a relatively low blood pressure.
... Thus, in some situations in situ analysis of behavior on recently captured sharks that are maintained in an upright orientation may better reflect the natural response to EPMs and magnets. Moreover, placing a shark in a state of tonic immobility may not be required when testing a species like the Greenland shark which has been reported to exhibit lethargic behavior under natural conditions (Watanabe et al., 2012) and no resistance when captured (Bigelow & Schroeder, 1948). ...
... For example, pelagic excursions of Greenland sharks are well documented (Skomal & Benz, 2004;Stokesbury et al., 2005;Campana, Fisk & Klimley, 2015), they have been captured at the surface of the ocean (Beck & Mansfield, 1969;Kondyurin & Myagkov, 1983), and during our multiyear gear comparison study we observed Greenland sharks at the surface of the ocean preying on Greenland halibut captured on longlines. The Greenland shark belongs to the family Somniosidae commonly referred to as sleeper sharks and the slow swimming, low activity level, and non-aggressive behavior of Greenland sharks is well documented (Bigelow & Schroeder, 1948;Watanabe et al., 2012). Further, free swimming Greenland sharks in the St. Lawrence Estuary have been described as docile during over 100 close encounters with divers and their tolerance to physical contact with sport divers including being captured by hook and line and lassoed by the tail has led to the development of a diver code of conduct (Greenland Shark and Elasmobranch Education and Research Group (GEERG), 2009). ...
... The increase in gape size and increased bulging of the pharyngeal cavity observed in this study would increase inertial suction forces during a feeding event and are likely to increase feeding success. Stealthy cryptic approaches and powerful suction would also explain how such a slow swimming shark (Watanabe et al., 2012) is able to consume Greenland halibut and small seals, especially when these animals are consumed whole and with no external damage. For example, stomach content analysis of a large (>4 m) Greenland shark captured on longlines set through the ice in Pond Inlet, Nunavut revealed the presence of a fully intact (i.e., no external wounds) and recently consumed 60 cm Greenland halibut and a fully intact 50-60 cm ringed seal (Pusa hispida) (R. Sullivan, 2006, personal observation). ...
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The Greenland Shark ( Somniosus microcephalus ) is the most common bycatch in the Greenland halibut ( Reinhardtius hippoglossoides ) bottom longline fishery in Cumberland Sound, Canada. Historically, this inshore fishery has been prosecuted through the ice during winter but winter storms and unpredictable landfast ice conditions since the mid-1990s have led to interest in developing a summer fishery during the ice-free season. However, bycatch of Greenland shark was found to increase substantially with 570 sharks captured during an experimental Greenland halibut summer fishery (i.e., mean of 6.3 sharks per 1,000 hooks set) and mortality was reported to be about 50% due in part to fishers killing sharks that were severely entangled in longline gear. This study investigated whether the SMART (Selective Magnetic and Repellent-Treated) hook technology is a practical deterrent to Greenland shark predation and subsequent bycatch on bottom longlines. Greenland shark feeding behavior, feeding kinematics, and variables affecting entanglement/disentanglement and release are also described. The SMART hook failed to deter Greenland shark predation, i.e., all sharks were captured on SMART hooks, some with more than one SMART hook in their jaw. Moreover, recently captured Greenland sharks did not exhibit a behavioral response to SMART hooks. In situ observations of Greenland shark feeding show that this species uses a powerful inertial suction mode of feeding and was able to draw bait into the mouth from a distance of 25–35 cm. This method of feeding is suggested to negate the potential deterrent effects of electropositive metal and magnetic alloy substitutions to the SMART hook technology. The number of hooks entangled by a Greenland shark and time to disentangle and live-release a shark was found to increase with body length.
... All sharks known to the authors from orders Carcharhiniformes and Lamniformes contain centra whose cartilage is reinforced with biomineral, albeit a few species are only partially mineralized. These vertebrae experience tens of millions of cycles of swimming-related loading [3], this loading alternates compression of the left side of the centra with compression of the right side (figure 1a) and strain magnitudes can reach 3-8% [5], an enormous level for mineralized tissue 1 , especially considering that the centra do not appear to have a remodelling mechanism like that in bone for removing accumulated microdamage. ...
... After azimuthal integration, the discrete bioapatite WAXS peaks 00.2, 22.2, 00.4 and 21.3 were fit with a pseudoVoigt function with a mixture of 50% Lorentzian-50% Gaussian character, and d 20.1 , d 00.2 , d 22.2 , d 00.4 and d 21.3 were calculated from the peak positions for both ω = 0°and ω = 180°. 3 The average of d(ω = 0°) and d(ω = 180°) was computed in order to eliminate any effect of slight variation between each sample's centre of mass and the rotation centre [23]. After these data were tabulated, an unusually large variation in d 00.2 was noted, and fitting was repeated including the nearby 20.1 peak. ...
Article
Members of subclass Elasmobranchii possess cartilage skeletons; the centra of many species are mineralized with a bioapatite, but virtually nothing is known about the mineral's organization. This study employed high-energy, small-angle X-ray scattering (SAXS) and wide-angle X-ray scattering (WAXS, i.e. X-ray diffraction) to investigate the bioapatite crystallography within blocks cut from centra of four species (two carcharhiniform families, one lamniform family and 1-ID of the Advanced Photon Source). All species' crystallographic quantities closely matched and indicated a bioapatite closely related to that in bone. The centra's lattice parameters a and c were somewhat smaller and somewhat larger, respectively, than in bone. Nanocrystallite sizes (WAXS peak widths) in shark centra were larger than typical of bone, and little microstrain was observed. Compared with bone, shark centra exhibited SAXS D -period peaks with larger D magnitudes, and D -period arcs with narrower azimuthal widths. The shark mineral phase, therefore, is closely related to that in bone but does possess real differences which probably affect mechanical property and which are worth further study.
... These ADLs must be retrieved to obtain data, but allow data to be recorded at higher frequencies, providing insight into fine-scale behaviour. Their application has become increasingly popular for use on animals occupying media that preclude direct observations, and now many ADLs are coupled with additional sensors for monitoring abiotic factors (e.g., temperature and depth, Watanabe et al. 2012;Wright et al. 2014;Lear et al. 2017;Carroll et al. 2014). ...
... Sharks regularly occupy high trophic positions (Cortés 1999;Estrada et al. 2003) and can influence the structure of marine ecosystems (Heithaus et al. 2008;Rasher et al. 2017;Barley et al. 2017). However, their typically high mobility and inaccessible habitat make their natural behaviour difficult or impossible to observe directly (Klimley et al. 1992;Nakamura et al. 2011;Watanabe et al. 2012;Payne et al. 2016). To date, accelerometer application with sharks has provided new information on activity patterns (Whitney et al. 2007;Gleiss et al. 2013;Leos-Barajas et al. 2017;Gleiss et al. 2017), mating behaviour (Whitney et al. 2010), metabolic demands (Gleiss et al. 2010;Barnett et al. 2016;Whitney et al. 2016b;Bouyoucos et al. 2017;Lear et al. 2017), post-release mortality (Whitney et al. 2016a) and biomechanics (Gleiss et al. 2011a;Payne et al. 2016;Papastamatiou et al. 2018). ...
Article
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Discerning behaviours of free-ranging animals allows for quantifcation of their activity budget, providing important insight into ecology. Over recent years, accelerometers have been used to unveil the cryptic lives of animals. The increased ability of accelerometers to store large quantities of high resolution data has prompted a need for automated behavioural classifcation. We assessed the performance of several machine learning (ML) classifers to discern fve behaviours performed by accelerometer-equipped juvenile lemon sharks (Negaprion brevirostris) at Bimini, Bahamas (25°44′N, 79°16′W). The sharks were observed to exhibit chafng, burst swimming, headshaking, resting and swimming in a semi-captive environment and these observations were used to ground-truth data for ML training and testing. ML methods included logistic regression, an artifcial neural network, two random forest models, a gradient boosting model and a voting ensemble (VE) model, which combined the predictions of all other (base) models to improve classifer performance. The macro-averaged F-measure, an indicator of classifer performance, showed that the VE model improved overall classifcation (F-measure 0.88) above the strongest base learner model, gradient boosting (0.86). To test whether the VE model provided biologically meaningful results when applied to accelerometer data obtained from wild sharks, we investigated headshaking behaviour, as a proxy for prey capture, in relation to the variables: time of day, tidal phase and season. All variables were signifcant in predicting prey capture, with predations most likely to occur during early evening and less frequently during the dry season and high tides. These fndings support previous hypotheses from sporadic visual observations.
... When a shark swims, its tail beats from left to right, compressing first one side then the other side of each centrum (Fig. 1b), and the magnitude increases from the juncture of the thorax and abdomen toward the tail. The structure and mineralization of the carcharhiniform and lamniform centra enables shark vertebrae to survive enormous compressive strains of 3-8% (Porter et al., 2014) for millions of cycles of loading (Watanabe et al., 2012), despite the absence of a repair mechanism like remodeling in bone. ...
Article
The centra of shark vertebrae consist of cartilage mineralized by a bioapatite similar to bone's carbonated hydroxyapatite, and, without a repair mechanism analogous to remodeling in bone, these structures still survive millions of cycles of high-strain loading. The main structures of the centrum are an hourglass-shaped double cone and the intermedialia which supports the cones. Little is known about the nanostructure of shark centra, specifically the relationship between bioapatite and cartilage fibers, and this study uses energy dispersive diffraction (EDD) with polychromatic synchrotron x-radiation to study the spatial organization of the mineral phase and its crystallographic texture. The unique energy-sensitive detector array at beamline 6-BM-B, the Advanced Photon Source, enables EDD to quantify the texture within each sampling volume with one exposure while constructing 3D maps via specimen translation across the sampling volume. This study maps a centrum from two shark orders, a carcharhiniform and a lamniform, with different intermedialia structures. In the blue shark (Prionace glauca, Carcharhiniformes), the bioapatite's c-axes are oriented laterally within the centrum's cone walls but axially within the wide wedges of the intermedialia; the former is interpreted to resist lateral deformation, the latter to support axial loads. In the shortfin mako (Isurus oxyrinchus, Lamniformes), there is some tendency for c-axis variation with position, but the situation is unclear because one dimension of the sampling volume is considerably larger than the thickness and spacing of the intermedialia's radially-oriented lamellae. Because elastic modulus in collagen plus bioapatite mineralized tissues varies significantly with both volume fraction of bioapatite and crystallographic texture, the present 3D EDD-derived maps should inform future 3D numerical models of shark centra under applied load.
... Swimming speeds of these sharks ranged between 0.16 m s − 1 to 0.84 m s − 1 , which are in consistency with swimming speeds of 0.1 m s − 1 to 1.4 m s − 1 visually estimated by scuba divers of undisturbed Greenland sharks (N = 10, Harvey-Clark et al., 2005). It also coincides with estimates obtained from Greenland sharks tagged with accelerometers (N = 6, mean = 0.37 m s − 1 , max = 0.74 m s − 1 , Watanabe et al., 2012). On several occasions, the acoustic tracks revealed Greenland sharks in pairwise swimming. ...
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The conservation status of the long-lived Greenland shark (Somniosus microcephalus) is unknown, and methods for non-invasively estimating local or regional abundances are wanted. Using a multifrequency split beam echosounder during long line fishery for Greenland sharks, we demonstrate how individual sharks can be identified and separated with high accuracy from the acoustic backscattering at three frequencies. From a slowly drifting vessel, hooked and free-swimming targets with similar target characteristics were identified on echograms along the bottom and in the water column over a depth of ∼400 m. A discriminate analysis using target frequency response, target strength and echo pulse stretching was used to identify shark targets from the only possible competitor, with respect to target strength, being large Atlantic cod (Gadus morhua). Isolation and tracking of single targets allowed us to calculate the swimming speeds ranging between 0.16 and 0.84 m s⁻¹ (mean±SD, 0.47±0.18 m s⁻¹) from 15 free-swimming sharks over distances from 11 and 50 m in time periods of 28 to 122 seconds per track. Our findings demonstrate the first acoustic detection of Greenland sharks, and thus a new non-invasive monitoring method applicable in otherwise difficult-to-access arctic and deep-sea waters.
... Sharks have cartilaginous skeletons, and each vertebra of their vertebral column contains a mineralized centrum that carries the loads generated during swimming. 1 The structure and mineralization of the centra enable shark vertebrae to survive enormous compressive strains of 3% to 8% 2 for millions of cycles of loading, 3 despite the absence of a repair mechanism analogous to remodeling in bone. Diffraction has shown that the centra's mineral is a bioapatite closely related to hydroxyapatite (hAp), 4,5 and is organized similarly to the bone. ...
Article
Purpose: Tomography using diffracted x-rays produces reconstructions mapping quantities such as crystal lattice parameter(s), crystallite size, and crystallographic texture, information quite different from that obtained with absorption or phase contrast. Diffraction tomography is used to map an entire blue shark centrum with its double cone structure (corpora calcerea) and intermedialia (four wedges). Approach: Energy dispersive diffraction (EDD) and polychromatic synchrotron x-radiation at 6-BM-B, the Advanced Photon Source, were used. Different, properly oriented Bragg planes diffract different x-ray energies; these intensities are measured by one of ten energy-sensitive detectors. A pencil beam defines the irradiated volume, and a collimator before each energy-sensitive detector selects which portion of the irradiated column is sampled at any one time. Translating the specimen along X , Y , and Z axes produces a 3D map. Results: We report 3D maps of the integrated intensity of several bioapatite reflections from the mineralized cartilage centrum of a blue shark. The c axis reflection's integrated intensities and those of a reflection with no c axis component reveal that the cone wall's bioapatite is oriented with its c axes lateral, i.e., perpendicular to the backbone's axis, and that the wedges' bioapatite is oriented with its c axes axial. Absorption microcomputed tomography (laboratory and synchrotron) and x-ray excited x-ray fluorescence maps provide higher resolution views. Conclusion: The bioapatite in the cone walls and wedges is oriented to resist lateral and axial deflections, respectively. Mineralized tissue samples can be mapped in 3D with EDD tomography and subsequently studied by destructive methods.
... The vertebrae experience tens of millions of cycles of swimmingrelated loading (Watanabe et al. 2012), and strain magnitudes can reach 3-8% (Porter et al. 2014), an enormous level for mineralized tissue. Although the mineralized cartilage of shark centra has some capacity for repair, e.g. ...
Article
Centra of shark vertebrae from three species of Lamniformes (Alopias vulpinus, Carcharodon carcharias and Isurus oxyrinchus) and three species of Carcharhiniformes (Carcharhinus plumbeus, Carcharhinus obscurus and Prionace glauca) were imaged with laboratory microcomputed Tomography (microCT) using volume element (voxel) sizes between 16-24 µm. Linear attenuation coefficients were the same in the corpus calcarea (hour-glass-shaped cone) and intermedialia of the lamniforms but were smaller in the intermedialia than in the corpus calcarea of the carcharhiniforms. All centra contained growth bands which were visible as small changes in linear attenuation coefficient. In all six cases, the cross-sections of the cones were close to circular, and the cone angles matched those reported in the literature. Cartilage canals were a prominent structure in the intermedialia of all species, 3D renderings of centra of C. obscurus and I. oxyrinchus diameters showed these canals ran radially outward from the cone walls, and canal diameters were consistent with the limited numerical values in the literature. Somewhat higher calcification levels around the periphery of cartilage canals and of outer surfaces of the intermedialia and corpus calcerea suggest microstructural variation exists at scale below that which can be resolved in the present data sets.
... There are over 1,000 extant species of elasmobranch that arose sometime during c. 400 million years of independent evolution, with the main living families having first appeared sometime between the Permian and Jurassic Periods (∼250-150 million years ago) (Young, 1981). Over that time elasmobranchs have evolved to occupy a very broad range of habitats within aquatic ecosystems worldwide: they are distributed in freshwater and estuarine systems and in the oceanic pelagic realm and the deep sea (to at least 4,500 m depth; Kyne & Simpfendorfer, 2010), and from polar Arctic seas (but not the Antarctic) in water temperatures of ∼2 o C (Watanabe et al., 2012) through to low latitude coral reefs circumglobally (∼30 o C). This broad distribution across aquatic habitats that exhibit large spatial and temporal variations in physico-chemical variables, including oxygen concentration, coupled with the relatively large body size and active predatory lifestyle of elasmobranchs indicates the physiology, behaviour and ecology of sharks, skates and rays are likely to be strongly influenced by oxygen depletion. ...
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All of the >1000 species of sharks, skates and rays are obligate water-breathers with comparatively high absolute oxygen demands being relatively large-bodied, active predators. With broad distributions across aquatic habitats exhibiting large variations in physico-chemical variables including oxygen concentration indicates elasmobranch physiology, behaviour and ecology to be strongly influenced by oxygen depletion. Many elasmobranchs show rapid behavioural responses to hypoxic water by increased activity associated with avoidance. Nonetheless, elasmobranchs also appear capable of withstanding mild hypoxia with circulatory and/or ventilatory responses, perhaps even for extended periods. However, such strategies may be insufficient to endure moderate, progressive or prolonged hypoxia or anoxia. As water temperatures rise with climate warming most elasmobranchs (as ectotherms) will exhibit elevated metabolic rates and will be increasingly less able to tolerate the effects of even mild hypoxia associated with ocean deoxygenation. Thus, sustained hypoxia in warmer coastal waters is likely to lead to shifts in elasmobranch distributions. Expansion of oxygen minimum zones (OMZs) of the open ocean in particular are predicted to have significant population-level implications for pelagic elasmobranchs as they become habitat compressed into surface layers by shoaling hypoxic water. Surface layers overlying OMZs appear to be space use hotspots of pelagic sharks that may be increasingly likely to undergo significant ‘habitat compression’ (reduced habitat volumes) with expanding OMZs, potentially increasing their susceptibility to surface fisheries, e.g. long-lining, leading to further risks of over-exploitation especially of threatened species such as shortfin mako (Isurus oxyrinchus). A priority for conservation is to mitigate ocean deoxygenation effects on elasmobranchs, such that future catch rates are controlled in the light of climate change rather than for exploitation to be exacerbated by ocean oxygen losses.
... Animals incur less hydrodynamic drag during gliding than active swimming; therefore, in theory, negatively buoyant animals can save locomotion cost by alternating passive gliding in descents and active swimming in ascents compared with continuous horizontal swimming (Weihs 1973). However, as for tiger sharks Galeocerdo cuvier (Nakamura et al. 2011) and Greenland sharks Somniosus microcephalus (Watanabe et al. 2012), the blue sharks tagged in this study glided only for a minor proportion (10 − 20%) of their descent durations, indicating that locomotion cost saving is not the main explanation for deep dives. In some pelagic fishes, deep dives may be associated with navigation because geomagnetic and bathymetric cues can be accessed at great depths (Klimley 1993). ...
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Large pelagic fishes often dive and surface repeatedly as if they were airbreathers, raising a question about the functions of these movements. Some species (e.g., bigeye tuna, ocean sunfish) apparently alternate foraging in deep cold waters and rewarming in shallow warm waters. However, it is unclear how prevalent this pattern is among species. Blue sharks are the widest-ranging pelagic shark with expanded vertical niches, providing a model for studying foraging-thermoregulation associations. We used electronic tags, including video cameras, to record the diving behaviour, muscle temperature, and foraging events of two blue sharks. During repeated deep dives (max. 422 m), muscle temperature changed more slowly than ambient water temperature. Sharks shifted between descents and ascents before muscle temperature reached ambient temperature, leading to a narrower range (8 °C) of muscle temperature than ambient temperature (20 °C). 2.5-h video footage showed a shark catching a squid, during which a burst swimming event was recorded. Similar swimming events, detected from the entire tag data (20 - 22 h), occurred over a wide depth range (5 - 293 m). We conclude that, instead of alternating foraging and rewarming, blue sharks at our study site forage and thermoregulate continuously in the water column. Furthermore, our comparative analyses showed that the heat exchange rates of blue sharks during the warming and cooling process were not exceptional among fishes for their body size. Thus, behavioural thermoregulation linked to foraging, rather than enhanced abilities to control heat exchange rates, is likely key to the expanded thermal niches of this ectothermic species. Supplementary information: The online version contains supplementary material available at 10.1007/s00227-021-03971-3.
... Using data collected in 2018, where video recording was continuous, TBF was estimated every minute (using 30 second of data), and every five minutes for the 2019 duty cycled data for the first 30 minutes following tagging. TBF was also estimated for each 30-second video sequence of surface feeding behaviour to compare swimming behaviour with previously reported swimming metrics from surface observations [67,68]. Temperature and depth data collected by the time-depth recorder were analysed in R (version 3.5.3) ...
Article
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While biologging tags have answered a wealth of ecological questions, the drivers and consequences of movement and activity often remain difficult to ascertain, particularly marine vertebrates which are difficult to observe directly. Basking sharks, the second largest shark species in the world, aggregate in the summer in key foraging sites but despite advances in biologging technologies, little is known about their breeding ecology and sub-surface behaviour. Advances in camera technologies holds potential for filling in these knowledge gaps by providing environmental context and validating behaviours recorded with conventional telemetry. Six basking sharks were tagged at their feeding site in the Sea of Hebrides, Scotland, with towed cameras combined with time-depth recorders and satellite telemetry. Cameras recorded a cumulative 123 hours of video data over an average 64-hour deployment and confirmed the position of the sharks within the water column. Feeding events only occurred within a metre depth and made up ¾ of the time spent swimming near the surface. Sharks maintained similar tail beat frequencies regardless of whether feeding, swimming near the surface or the seabed, where they spent surprisingly up to 88% of daylight hours. This study reported the first complete breaching event and the first sub-surface putative courtship display, with nose-to-tail chasing, parallel swimming as well as the first observation of grouping behaviour near the seabed. Social groups of sharks are thought to be very short term and sporadic, and may play a role in finding breeding partners, particularly in solitary sharks which may use aggregations as an opportunity to breed. In situ observation of basking sharks at their seasonal aggregation site through animal borne cameras revealed unprecedented insight into the social and environmental context of basking shark behaviour which were previously limited to surface observations.
... In contrast, while white muscle relies on aerobic metabolism in rest and recovery, anaerobic metabolism supports high intensity activity. It has few blood capillaries and contains a low level of mitochondria (Watanabe et al., 2012;Ryan et al., 2015). An intermediate type of fibre called pink fibre, is located between the red and the white muscles (Kryvi and Totland, 1977;Bone et al., 1986;Kiessling et al., 2006). ...
Article
In the last decade, there has been an increase in the study of the ecology of deep-sea organisms. One way to understand an organism's ecology is the study of its metabolism. According to literature, deep-sea sharks possess a lower anaerobic enzyme activity than their shallow-water counterparts, but no difference has been observed regarding their aerobic enzyme activities. These studies have suggested deep-sea sharks should be slow and listless swimmers. However, other studies based on video observations have revealed differences in cruise swimming speed between different species. The present study examined muscles of squaliform sharks, including both luminous and non-luminous species. We combined measurements of the relative amounts of red and white muscle with assays of enzymes that are used as markers for aerobic (citrate synthase, malate dehydrogenase) and anaerobic (lactate dehydrogenase) metabolism, searching for a relationship with cruising speeds. Non-luminous deep-sea species displayed lower aerobic enzymes activities but similar anaerobic enzymes activities than the benthic shallow-water counterpart (Squalus acanthias). Conversely, luminous Etmopteridae species were found to have similar aerobic enzymes activities to S. acanthias but displayed lower anaerobic enzymes activities. Analyses revealed that red muscle proportion and aerobic enzyme activities were positively related to the cruise swimming speed. In contrast, Dalatias licha, which swims at the slowest cruise swimming speed ever recorded, presented a very low aerobic metabolic phenotype (lower aerobic marker enzymes and less red muscle). Finally, the values obtained for white muscle proportion and anaerobic metabolic phenotype suggested a high burst capacity for D. licha and non-luminous sharks.
... In addition to these three-dimensional motion sensors, swimming speed sensors have been integrated into many biologging packages. Modern versions of these sensors are comprised of two parts: (1) a freely rotating propeller (Muramoto et al., 2004, Nakamura et al., 2011Watanabe et al., 2012) or exible paddle (Shepard et al., 2008b), and usually (2) an optical or magnetic sensor that detects the movement of the propeller or paddle. Swimming speed sensors need to be oriented along the same axis as the swimming direction of the animal and have a clear path for water to ow through and move the propeller. ...
... As the world's longest-lived vertebrate (Nielsen et al. 2016), the Greenland shark (Somniosus microcephalus) represents one such species. Greenland sharks exhibit the slowest observed mean swim speed (0.34 m·s À1 ) and tailbeat frequency (0.15 Hz) relative to their size of any fish (Watanabe et al. 2012), yet they are highly mobile (Campana et al. 2015;Fisk et al. 2012) and broadly distributed throughout Baffin Bay (eastern Canadian Arctic). As one of only a handful of shark species inhabiting the periodically ice-covered regions of the North Atlantic (McMeans et al. 2013), they face extreme temperatures and dramatic seasonal fluctuations in light levels and productivity (Gradinger 1995). ...
Article
As Arctic ecosystems become increasingly vulnerable to climate- and human-induced stressors, effective marine management will rely on the characterization of fish movements. Over a six-year study period, the movements of 65 Greenland sharks (Somniosus microcephalus) (41 males, 24 females [mean LT = 2.48 ± 0.50 m]) were monitored using static acoustic telemetry. Shark presence in a typical deep-water fjord was restricted to the summer open-water period. Residency duration varied based on age-class (juvenile [n=17] vs. subadult [n=48]), however, activity space size and extent were comparable. A quarter of tagged sharks (n=16) returned to the system in subsequent years after tagging, with individuals re-detected for a maximum of 4 y. Movements between coastal and offshore waters occurred primarily via a deep-water channel with sharks detected along the channel banks. These multi-year data depict how a potentially vulnerable Arctic predator utilizes a deep-water fjord in the context of the regional development of community inshore and offshore commercial fisheries.
... As our speed measurements were strongly unimodal and right-skewed, the modal speed was used in the models to represent the cruising speed of the animal, as opposed to burst events. Cruising speed was chosen specifically for analysis as it is aerobically powered, can be sustained for prolonged periods of time (Gioanni, 1988;Ryan et al., 2015;Ware, 1978;Watanabe et al., 2012) and is the most common speed at which the animals travel as we have defined it (i.e. modal swimming speed). ...
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Regional endothermy has evolved several times in marine fishes, and two competing hypotheses are generally proposed to explain the evolutionary drivers behind this trait: thermal niche expansion and elevated cruising speeds. Evidence to support either hypothesis is equivocal, and the ecological advantages conferred by endothermy in fishes remain debated. By compiling published biologging data and collecting precise speed measurements from free-swimming fishes in the wild, we directly test whether endothermic fishes encounter broader temperature ranges, swim faster or both. Our analyses avoid several complications associated with earlier tests of these hypotheses, as we use precise measurements of the thermal experience and speed of individual fish. Phylogenetically-informed analyses of 89 studies reporting temperature ranges encountered by tagged fishes reveal that endotherms do not encounter broader temperature ranges than their ectothermic counterparts. In contrast, speed measurements from 45 individuals (16 species, of which four were regional endotherms) show that endothermic fishes cruise ~1.6 times faster than ectotherms, after accounting for the influence of body temperature and body mass on speed. Our study shows that regionally endothermic fishes—those with the ability to conserve metabolically derived heat through vascular countercurrent heat exchangers and elevate the temperature of internal tissues—swim at elevated cruising speeds, although not as fast as previously thought. Contrary to previous studies of endothermy's role in thermal niche expansion, our results suggest the significance of endothermy in fishes lies in the advantages it confers to swimming performance rather than facilitating the occupation of broader thermal niches. Given speed's major influence on metabolic rate, our updated speed estimates imply endotherms have lower routine energy requirements than current estimates. Our findings shed light on the evolutionary drivers of regional endothermy in fishes and question the view that the trait confers resilience to climate change through broader thermal tolerance than that of ectotherms.
... The importance of such differentiation becomes evident when for example comparing the results of this study with cases from Sable Island, Canada. On Sable island, the death of over 4000 seals has been attributed to Greenland sharks (Somniosus microcephalus) 24 , despite the fact that this species has been shown to be a very slow swimming fish presumably only capable of catching sleeping or deceased seals 25 , as well as that the lesions of the shown cases bear a striking similarity to the ones described here and in prior publications [15][16][17][18] . ...
Article
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In order to conduct an objective evaluation of potential ecological effects of grey seal predation on marine mammals, it is essential to establish a broad knowledge base helping in the thorough identification of such cases during post-mortem examination. The aim of this work is to report and discuss outcomes resulting from a retrospective evaluation of harbour ( Phoca vitulina ) and grey seal ( Halichoerus grypus ) stranding and necropsy data (n = 3274). In addition, the results are compared to a recent case of definite grey seal predation from Germany as well as reports from other countries. Carcasses potentially subjected to grey seal predation show severe lacerations with a circular pattern leaving a smooth, linear and cut-like wound margin. Large parts of skin and underlying tissue are detached from the body and loss of blubber is common. Occurrence frequencies of encountered lesions are presented and a list of parameters to be used for the assessment of similar cases as well as a complementary decision tree are suggested. With the proposed parameters, categories and tools, a baseline can be built in order to facilitate the standardised recognition of predation cases during post-mortem examinations of seals between groups working with populations across several geographic ranges.
... Mean tailbeat frequency (Hz) of blacktip sharks swimming in the wild was 0.82 Hz, also within the range of values obtained from tagged animals swimming (0. 15-1.16 Hz) in the wild [56][57][58]. Lastly, mean peak-peak amplitude was 0.24 bl, which approaches the calculated optimal amplitude of 20% of bl [46]. ...
Article
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Recent work showed that two species of hammerhead sharks operated as a double oscillating system, where frequency and amplitude differed in the anterior and posterior parts of the body. We hypothesized that a double oscillating system would be present in a large, volitionally swimming, conventionally shaped carcharhinid shark. Swimming kinematics analyses provide quantification to mechanistically examine swimming within and among species. Here, we quantify blacktip shark (Carcharhinus limbatus) volitional swimming kinematics under natural conditions to assess variation between anterior and posterior body regions and demonstrate the presence of a double oscillating system. We captured footage of 80 individual blacktips swimming in the wild using a DJI Phantom 4 Pro aerial drone. The widespread accessibility of aerial drone technology has allowed for greater observation of wild marine megafauna. We used Loggerpro motion tracking software to track five anatomical landmarks frame by frame to calculate tailbeat frequency, tailbeat amplitude, speed, and anterior/posterior variables: amplitude and frequency of the head and tail, and the body curvature measured as anterior and posterior flexion. We found significant increases in tailbeat frequency and amplitude with increasing swimming speed. Tailbeat frequency decreased and tailbeat amplitude increased as posterior flexion amplitude increased. We found significant differences between anterior and posterior amplitudes and frequencies, suggesting a double oscillating modality of wave propagation. These data support previous work that hypothesized the importance of a double oscillating system for increased sensory perception. These methods demonstrate the utility of quantifying swimming kinematics of wild animals through direct observation, with the potential to apply a biomechanical perspective to movement ecology paradigms.
... Similarly, Grant, Sullivan & Hedges (2018) found that all entangled sharks captured on longlines in overnight sets of 14-16 h survived the disentanglement process. The Greenland shark's lack of resistance during haul back and lethargic behaviour observed while at the surface of the ocean in the current and previous studies (Bigelow & Schroeder, 1948;Idrobo & Berkes, 2012;Watanabe et al., 2012;Grant, Sullivan & Hedges, 2018) facilitates disentanglement, prevents injuries to sharks and fishers, and may lead to a high probability of post-release survival when sharks are released with no or minimal trailing fishing gear. ...
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The Greenland shark ( Somniosus microcephalus ) is the main bycatch species in established and exploratory inshore longline fisheries for Greenland halibut ( Reinhardtius hippoglossoides ) on the east coast of Baffin Island, Canada. Bycatch and entanglement in longline gear has at times been substantial and post-release survival is questionable when Greenland sharks are released with trailing fishing gear. This study investigated the effect of the type of fishing line used in the gangion and gangion breaking strength on catch rates of Greenland shark and Greenland halibut in bottom set longlines. Circle (size 14/0, 0° offset) hooks were used throughout the study. Behavior of captured sharks, mode of capture (i.e., jaw hook and/or entanglement), level of entanglement in longline gear, time required to disentangle sharks and biological information (sex, body length and health status) were recorded. Catch rates of Greenland shark were independent of monofilament nylon gangion breaking strength and monofilament gangions captured significantly fewer Greenland sharks than the traditional braided multifilament nylon gangion. Catch rates and body size of Greenland halibut did not differ significantly between gangion treatments. Although most (84%) of the Greenland sharks were hooked by the jaw, a high percentage (76%) were entangled in the mainline. The mean length of mainline entangled around the body and/or caudal peduncle and caudal fin was 28.7 m. Greenland sharks exhibited cannibalistic behavior with 15% of captured sharks cannibalized. All remaining sharks were alive and survived the disentanglement process which can be attributed to their lethargic behavior and lack of resistance when hauled to the surface. Thus, as a conservation measure fishers should be encouraged to remove trailing fishing gear prior to release. Our results are used to demonstrate benefits to the fishing industry with regard to an overall reduction in the period of time to disentangle sharks and damage to fishing gear by switching from braided multifilament to monofilament gangions in Greenland halibut longline fisheries.
... The increase in gape size and increased bulging of the pharyngeal cavity 561 observed in this study would increase inertial suction forces during a feeding event and are likely 562 to increase feeding success. Stealthy cryptic approaches and powerful suction would also explain 563 how such a slow swimming shark (Watanabe et al., 2012) is able to consume Greenland halibut 564 and small seals, especially when these animals are consumed whole and with no external damage. 565 For example, stomach content analysis of a large (>4 m) Greenland shark captured on longlines 566 set through the ice in Scott Fjord, Nunavut revealed the presence of a fully intact (i.e., no external 567 wounds) and recently consumed 60 cm Greenland halibut and a fully intact 50-60 cm ringed seal 568 (Pusa hispida) (R. Sullivan, pers. ...
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The Greenland Shark ( Somniosus microcephalus ) is the most common bycatch in the Greenland halibut ( Reinhardtius hippoglossoides ) bottom longline fishery in Cumberland Sound, Canada. Historically, this inshore fishery has been prosecuted through the ice during winter but winter storms and unpredictable landfast ice conditions since the mid-1990s have led to interest in developing a summer fishery during the ice-free season. However, bycatch of Greenland shark was found to increase substantially with 570 sharks captured during an experimental Greenland halibut summer fishery (i.e., mean of 6.3 sharks per 1,000 hooks set) and mortality was reported to be about 50% due to in part to fishers killing sharks that were severely entangled in longline gear. This study investigated whether the SMART (Selective Magnetic and Repellent-Treated) hook technology is a practical deterrent to Greenland shark predation and subsequent bycatch on bottom longlines. Greenland shark feeding behavior, feeding kinematics, and variables affecting entanglement/disentanglement and release are also described. The SMART hook failed to deter Greenland shark predation i.e., all sharks were captured on SMART hooks, some with more than one SMART hook in their jaw. Moreover, recently captured Greenland sharks did not exhibit a behavioral response to SMART hooks. In situ observations of Greenland shark feeding show that this species uses a powerful inertial suction mode of feeding and was able to draw bait into the mouth from a distance of 25-35 cm. This method of feeding is suggested to negate the potential deterrent effects of electropositive metal and magnetic alloy substitutions to the SMART hook technology. The number of hooks entangled by a Greenland shark and time to disentangle and live-release a shark was found to increase with body length.
... In Review). Greenland sharks swim with approximately half the tail-beat frequency (0.15 Hz, [37], but in water of 2.3 °C, compared to 11 °C in the present study. Behavioural modification due to contact events, or heightened alertness due to the presence of the AUV, are Depth and temperature profiles from three sharks. ...
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Background Biologging studies have revealed a wealth of information about the spatio-temporal movements of a wide range of vertebrates large enough to carry electronic tracking tags. Advances in autonomous underwater vehicles (AUVs or UAVs) and unmanned aerial vehicles (commonly known as drones), which can carry far larger payloads of sensor technologies, have revealed insights into the environment through which animals travel. Some AUVs have been used to film target animals, but are generally limited to periods as long as a drone operator can actively follow an animal. In the present study, we use an AUV, the REMUS-100 SharkCam, paired with a custom transponder tag attached to the shark, to autonomously follow three basking sharks for a cumulative total of 10.9 h to collect video and environmental data on their sub-surface behaviour. The basking shark is the second largest fish in the world and is endangered globally, but despite being subject to various biologging studies, little is known of this species breeding ecology and their mating grounds remain unknown. Results We detail the first successful autonomous tracking of basking sharks, comprising three missions that filmed basking sharks in mid-water and close to benthic habitats. Sharks spent very little time feeding, and travelled relatively close to sandy, rocky and algae-covered benthos. One basking shark was observed defecating. Conspecifics were not observed in the three missions, nor were courtship or breeding behaviours. AUV offset distances for videography were determined iteratively through tracking. These offsets varied depending on the trade-off of between water clarity and proximity of the AUV for obtaining useful video data and directly influencing shark behaviour. Conclusions The present study is the first successful use of an AUV to gain insight into the sub-surface behaviour of basking sharks.
... We systematically adjusted the cycle frequency and the stimulus parameters to produce maximal net-work. Strain cycle frequency was varied over a range of 0.25 to 1 Hz, a range that encompasses tailbeat frequencies observed in large, free-swimming pelagic fishes as well as optimum cycle frequencies used in previous studies (Altringham and Block 1997;Donley et al. 2005Donley et al. , 2007Shadwick and Syme 2008;Aalbers et al. 2010;Bernal et al. 2010;Donley et al. 2012;Watanabe et al. 2012). Although our goal was not to assess the stimulus parameters that resulted in maximal work, we determined that the optimized stimulation phase consistently occurred during the late, lengthening period of the strain cycle (around 25%; Online Resource 1). ...
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Bigeye thresher sharks (Alopias superciliosus) and swordfish (Xiphias gladius) are large, pelagic fishes, which make long-duration, diurnal foraging dives from warm, surface waters (18–24 °C) to cold waters beneath the thermocline (5–10 °C). In bigeye thresher sharks, the subcutaneous position of the red, aerobic swimming muscles (RM) suggests that RM temperature mirrors ambient during dives (i.e., ectothermy). In swordfish, the RM is closer to the vertebrae and its associated with vascular counter-current heat exchangers that maintain RM temperature above ambient (i.e., RM endothermy). Here, we sought to determine how exposure to a wide range of ambient temperatures (8, 16, 24 °C) impacted peak power output and optimum cycle (i.e., tailbeat) frequency (0.25, 0.5, 1 Hz) in RM isolated from both species. Bigeye thresher shark RM did not produce substantial power at high cycle frequencies, even at high temperatures; but it did produce relatively high power at slow cycle frequencies regardless of temperature. Swordfish RM produced more power when operating at a combination of fast cycle frequencies and higher temperatures. This suggests that swordfish RM benefits considerably more from warming than bigeye thresher shark RM, while the RM of both species was able to produce power at cold temperatures and slow cycle frequencies. Despite different thermal strategies (i.e., ectothermy vs. RM endothermy), the ability of the RM to power sustained swimming during foraging-related search behaviors may contribute to the unique ability of these fishes to successfully exploit food resources in deep, cold water.
... 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 ...
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Background 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. Results 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. Conclusion 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.
... Hz) and swimming speeds (mean 0.3-0.4 m s -1 [11]) suggest they have low metabolic rates relative to more active, shallower-dwelling species [70,71]. Low metabolic rates could allow sixgill sharks to maintain aerobic metabolism under low oxygen conditions [17,18]. ...
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Diel vertical migration is a widespread behavioral phenomenon where organisms migrate through the water column and may modify behavior relative to changing environmental conditions based on physiological tolerances. Here, we combined a novel suite of biologging technologies to examine the thermal physiology (intramuscular temperature), fine-scale swimming behavior and activity (overall dynamic body acceleration as a proxy for energy expenditure) of bluntnose sixgill sharks (Hexanchus griseus) in response to environmental changes (depth, water temperature, dissolved oxygen) experienced during diel vertical migrations. In the subtropical waters off Hawai‘i, sixgill sharks undertook pronounced diel vertical migrations and spent considerable amounts of time in cold (5–7°C), low oxygen conditions (10–25% saturation) during their deeper daytime distribution. Further, sixgill sharks spent the majority of their deeper daytime distribution with intramuscular temperatures warmer than ambient water temperatures, thereby providing them with a significant thermal advantage over non-vertically migrating and smaller-sized prey. Sixgill sharks exhibited relatively high rates of activity during both shallow (night) and deep (day) phases and contrary to our predictions, did not reduce activity levels during their deeper daytime distribution while experiencing low temperature and dissolved oxygen levels. This demonstrates an ability to tolerate the low oxygen conditions occurring within the local oxygen minimum zone. The novel combination of biologging technologies used here enabled innovative in situ deep-sea natural experiments and provided significant insight into the behavioral and physiological ecology of an ecologically important deepwater species.
... Swim speed has occasionally been used as a proxy for activity energy cost in bioenergetics models (e.g., [76]) and has provided useful qualitative insights into elasmobranch energetics (e.g., [77]). Swim speed is an essential parameter of kinematic modelling (KM), a promising approach that uses hydrodynamics to estimate transport cost. ...
Article
Shark and ray megafauna have crucial roles as top predators in many marine ecosystems, but are currently among the most threatened vertebrates and, based on historical extinctions, may be highly susceptible to future environmental perturbations. However, our understanding of their energetics lags behind that of other taxa. Such knowledge is required to answer important ecological questions and predict their responses to ocean warming, which may be limited by expanding ocean deoxygenation and declining prey availability. To develop bioenergetics models for shark and ray megafauna, incremental improvements in respirometry systems are useful but unlikely to accommodate the largest species. Advances in biologging tools and modelling could help answer the most pressing ecological questions about these iconic species.
... Despite the great promise of new biologging technologies, its uptake in the study of teleost fishes has been lagging behind the work on air-breathing marine vertebrates and elasmobranch fishes [24,25,31,32]. Indeed, due to their large size and prominent dorsal fins, much of the work on motion-sensitive biologging tags has come from elasmobranch fishes due to the relative ease of attaching data-loggers [33][34][35][36][37], whereas the morphology of pelagic teleost fish provides extraordinary challenges for firm attachment of loggers. Early work with multi-sensor acoustic tags has demonstrated some success in large teleost fishes, such as blue marlin (Makaira nigricans). ...
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Tunas possess a range of physiological and mechanical adaptations geared towards high-performance swimming that are of considerable interest to physiologists, ecologists and engineers. Advances in biologging have provided significant improvements in understanding tuna migrations and vertical movement patterns, yet our understanding of the locomotion and swimming mechanics of these fish under natural conditions is limited. We equipped Atlantic bluefin tuna (Thunnus thynnus) with motion-sensitive tags and video cameras to quantify the gaits and kinematics used by wild fish. Our data reveal significant variety in the locomotory kinematics of Atlantic bluefin tuna, ranging from continuous locomotion to two types of intermittent locomotion. The tuna sustained swimming speeds in excess of 1.5 m s-1 (0.6 body lengths s-1), while beating their tail at a frequency of approximately 1 Hz. While diving, some descents were entirely composed of passive glides, with slower descent rates featuring more gliding, while ascents were primarily composed of active swimming. The observed swimming behaviour of Atlantic bluefin tuna is consistent with theoretical models predicting such intermittent locomotion to result in mechanical and physiological advantages. Our results confirm that Atlantic bluefin tuna possess behavioural specializations to increase their locomotory performance, which together with their unique physiology improve their capacity to use pelagic and mesopelagic habitats.
... The natural swimming speeds of the three shark species are not well known. For the Greenland shark, a cruising speed of 0.34 m/s has been suggested [34]. We aimed to perform the experiments at a flow speed that would mimic this estimated cruising speed of a Greenland shark, but were limited by the performance of the pumping system and the requirement for the microfluidic chambers to stay tightly sealed. ...
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Shark skin has for many years inspired engineers to produce biomimetic structures reducing surface drag or acting as an anti-fouling layer. Both effects are presumed to be consequences of the structure of shark skin that is composed of arrays of so-called dermal denticles. However, the understanding of the full functional role of the dermal denticles is still a topic of research. We report optical microscopy and scanning electron microscopy of dermal denticles from three slowly swimming shark species for which the functional role of the dermal denticles is suggested as one of defense (possibly understood as anti-fouling) and/or abrasion strength. The three species are Greenland shark (Somnosius microcephalus), small-spotted catshark (Scyliorhinus canicula) and spiny dogfish (Squalus acanthias). Samples were taken at over 30 different positions on the bodies of the sharks. In addition, we demonstrate that the flow pattern near natural shark skin can be measured by micro-PIV (particle image velocimetry). The microfluidic experiments are complemented by numerical flow simulations. Both visualize unsteady flow, small eddies, and recirculation bubbles behind the natural dermal denticles.
... For applications where animal speed is used to test ecological and physiological hypotheses, many biologging tags have introduced external sensors to measure passing flow. Many have calibrated measured speed with the rotation rate of external impellers (Blackwell, Haverl, Le Boeuf, & Costa, 1999;Burgess, Tyack, Le Boeuf, & Costa, 1998;Watanabe, Lydersen, Fisk, & Kovacs, 2012) and micro-turbines (Gabaldon et al., 2019), as well as the amplitude of vibrations as measured by the tag's accelerometers (Cade, Barr, Calambokidis, Friedlaender, & Goldbogen, 2018). Absolute speed estimates are sensitive to stalling at high and low speeds, tag shape and placement on the body, orientation with respect to the flow and calibration technique, as well as to the estimation errors in the analytical techniques (e.g. ...
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North Atlantic right whales spend their summer months foraging primarily in American and Canadian Atlantic waters on high‐energy‐density prey. Here they rapidly accumulate and store energy obtained within a few months to support future migrations and reproduction while fasting. High drag from their ram‐filter foraging strategy places a limit on what prey densities will be energetically efficient to target. Our understanding of the volume of prey‐laden water filtered by right whales during a dive or foraging bout, and what information they use to decide to forage or not, has been limited by the difficulties of measuring when they feed at depth, how fast they swim during continuous ram filtration, and how often they might swallow accumulated prey. We used 10 DTAG deployments from right whales in the Bay of Fundy, Canada, to quantify swimming speeds and estimate the volume of prey‐laden water filtered per dive. We used the tag's inertial sensors to evaluate the timing of frequent biomechanical changes that indicate the truncation of continuous filtration, and whether the number or timing of these fluking bouts relate to longer feeding dives or other foraging decisions. During foraging dives, right whales descended at 1.4 (±0.2) m/s and slowed to swim at 1.1 (±0.3) m/s while filtering. We found consistent pauses in the fluking behaviour of foraging right whales, every 56 (±22 SD) seconds. Whales filtered on average 78 (±30) m3 of water per fluking bout, and on average filtered 673 (±201) m3 per dive. Right whales filter large volumes of water at low speeds with a high duty cycle, but require sufficiently high prey energy densities to compensate for a high‐drag foraging strategy. Closely related bowhead whales have a larger gape but swim more slowly, filtering greater volumes with lower drag. Our findings highlight that these endangered balaenids acquire their energy in a relatively short period of intense foraging; even moderate changes in their feeding behaviour or their prey energy density are likely to negatively impact their yearly energy budgets and therefore reduce fitness substantially. This article is protected by copyright. All rights reserved.
... For decades, scientists have noted the discrepancy between the lethargic appearance of the Greenland shark and the potentially faster moving prey species found in their stomachs (Jensen, 1914;Bigelow and Schroeder, 1948;Hansen, 1963;Watanabe et al., 2012) which has raised the question as to whether Greenland sharks are capable of active hunting or mainly feed as scavengers (Leclerc et al., 2012;Nielsen et al., 2014;Edwards et al., in press). Greenland shark scavenging events have been documented (Leclerc et al., 2011) but observations made in our study provide supporting evidence that Greenland sharks also are capable of active predation on fast swimming seals and large epibenthic fishes such as Atlantic cod and Greenland halibut. ...
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Current knowledge on the feeding ecology of the Greenland shark (Somniosus microcephalus), a potential top predator in arctic marine ecosystems, is based on small sample sizes as well as narrow size ranges of sharks. Therefore, potential size-related feeding patterns remain poorly documented. Using stomach content data (N=88) and stable isotope values of white muscle tissue (N=40), this study evaluates the diet in sharks ranging in size from 81 cm to 474 cm (total length). The importance of prey categories (‘Fish’, ‘Mammal’, ‘Squid’, ‘Crustacean’ and ‘Other’) was evaluated based on the reconstructed prey biomass of the stomach contents. Stable isotopes values of δ13C and δ15N ranged between -14.4‰ to -19.9‰ and 11.8‰ to 17.2‰, respectively. The importance of each prey category was estimated by the Index of Relative Importance (IRI). Our findings suggest that the smallest Greenland sharks (<200 cm) feed on lower trophic level prey, predominantly squids. Larger sharks (>200 cm) mainly feed on higher trophic level prey such as seals, epibenthic and benthic fishes including gadoids (Gadidae), skates (Rajidae), righteye flounders (Pleuronectidae), lumpfish (Cyclopteridae), wolffish (Anarhichadidae), and redfish (Sebastidae). Redfish were, however, only found to be important in the largest sharks sampled (>400 cm). In addition to demonstrating ontogenetic shits in their feeding preferences, this study supports that Greenland sharks are capable of active predation on fast swimming seals and large fishes.
... Nevertheless, a large difference in FMR between deep dives and surface swimming, as well as the commonness of deep diving behaviour in both coastal and offshore habitats reported for this species from longer-term satellite telemetry data (Domeier and Nasby-Lucas, 2008;Sims et al., 2012;Weng et al., 2007), suggests that gliding behaviour has substantial effects on the overall swimming costs of white sharks. Among large-bodied sharks, prolonged gliding during descents has also been reported for whale sharks (Gleiss et al., 2011b), but not for tiger or Greenland sharks (Nakamura et al., 2011;Watanabe et al., 2012), despite their negative buoyancy. As apparently rare cases, prolonged gliding during ascents with positive buoyancy was reported for bluntnose sixgill and prickly sharks (Nakamura et al., 2015). ...
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Some fishes and sea turtles are distinct from ectotherms by having elevated core body temperatures and metabolic rates. Quantifying the energetics and activity of the regionally endothermic species will help us understand how a fundamental biophysical process (i.e. temperature-dependent metabolism) shapes animal ecology; however, such information is limited owing to difficulties in studying these large, highly active animals. White sharks, Carcharodon carcharias, are the largest fish with regional endothermy, and potentially among the most energy-demanding fishes. Here, we deployed multi-sensor loggers on eight white sharks aggregating near colonies of long-nosed fur seals, Arctocephalus forsteri, off the Neptune Islands, Australia. Simultaneous measurements of depth, swim speed (a proxy for swimming metabolic rate) and body acceleration (indicating when sharks exhibited energy-efficient gliding behaviour) revealed their fine-scale swimming behaviour and allowed us to estimate their energy expenditure. Sharks repeatedly dived (mean swimming depth, 29 m) and swam at the surface between deep dives (maximum depth, 108 m). Modal swim speeds (0.80-1.35 m s-1) were slower than the estimated speeds that minimize cost of transport (1.3-1.9 m s-1), a pattern analogous to a 'sit-and-wait' strategy for a perpetually swimming species. All but one shark employed unpowered gliding during descents, rendering deep (>50 m) dives 29% less costly than surface swimming, which may incur additional wave drag. We suggest that these behavioural strategies may help sharks to maximize net energy gains by reducing swimming cost while increasing encounter rates with fast-swimming seals.
... The increase in gape size and increased bulging of the pharyngeal cavity 561 observed in this study would increase inertial suction forces during a feeding event and are likely 562 to increase feeding success. Stealthy cryptic approaches and powerful suction would also explain 563 how such a slow swimming shark (Watanabe et al., 2012) is able to consume Greenland halibut 564 and small seals, especially when these animals are consumed whole and with no external damage. 565 For example, stomach content analysis of a large (>4 m) Greenland shark captured on longlines 566 set through the ice in Scott Fjord, Nunavut revealed the presence of a fully intact (i.e., no external 567 wounds) and recently consumed 60 cm Greenland halibut and a fully intact 50-60 cm ringed seal 568 (Pusa hispida) (R. Sullivan, pers. ...
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The Greenland Shark ( Somniosus microcephalus ) is the most common bycatch in the Greenland halibut ( Reinhardtius hippoglossoides ) bottom longline fishery in Cumberland Sound, Canada. Historically, this inshore fishery has been prosecuted through the ice during winter but winter storms and unpredictable landfast ice conditions since the mid-1990s have led to interest in developing a summer fishery during the ice-free season. However, bycatch of Greenland shark was found to increase substantially with 570 sharks captured during an experimental Greenland halibut summer fishery (i.e., mean of 6.3 sharks per 1,000 hooks set) and mortality was reported to be about 50% due to in part to fishers killing sharks that were severely entangled in longline gear. This study investigated whether the SMART (Selective Magnetic and Repellent-Treated) hook technology is a practical deterrent to Greenland shark predation and subsequent bycatch on bottom longlines. Greenland shark feeding behavior, feeding kinematics, and variables affecting entanglement/disentanglement and release are also described. The SMART hook failed to deter Greenland shark predation i.e., all sharks were captured on SMART hooks, some with more than one SMART hook in their jaw. Moreover, recently captured Greenland sharks did not exhibit a behavioral response to SMART hooks. In situ observations of Greenland shark feeding show that this species uses a powerful inertial suction mode of feeding and was able to draw bait into the mouth from a distance of 25-35 cm. This method of feeding is suggested to negate the potential deterrent effects of electropositive metal and magnetic alloy substitutions to the SMART hook technology. The number of hooks entangled by a Greenland shark and time to disentangle and live-release a shark was found to increase with body length.
... The location of individual sharks when consecutive mrPATs popped off indicated that shark movements occurred at a similar time, suggesting an overall synchronization of movements or a potential seasonal migration route. The reported slow swimming speed of this species (0.34 ms −1 ; Watanabe et al., 2012) coupled with the short time taken for all sharks to travel to northwest Greenland (~16 days) would also indicate the animals were making a directed migration. Previous pop up archival tagging of Greenland sharks off Svalbard showed large-scale movements, but the direction of migration was random with animals headed in all directions when departing coastal waters . ...
... The burst locomotor performance of large aquatic animals is increasingly being measured in situ using accelerometers (Marras et al., 2015;Watanabe et al., 2012). Generally, small animals are more agile and quicker in their movements; therefore, small and high-frequency accelerometers are required to measure their burst movements. ...
Article
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Although animal-borne accelerometers are effective tools for quantifying the kinematics of animal behaviors, quantifying burst movements of small and agile aquatic animals remains challenging. To capture the details of burst movements, accelerometers need to sample at a very high frequency, which will inevitably shorten the recording duration or increase the device size. To overcome this problem, we developed a high-frequency acceleration data-logger that can be triggered by a manually-defined acceleration threshold, thus allowing the selective measurement of burst movements. We conducted experiments under laboratory and field conditions to examine the performance of the logger. The laboratory experiment using red seabream (Pagrus major) showed that the new logger could measure the kinematics of their escape behaviors. The field experiment using free-swimming yellowtail kingfish (Seriola lalandi) showed that the loggers trigger correctly. We suggest that this new logger can be applied to measure the burst
Article
In aquaculture, fish behaviour monitoring and analysis can provide the information required to guide daily feeding, schedule making and disease diagnosis. Technology such as machine vision, bio‐loggers and acoustic systems is essential to analyse fish behaviour. This paper focuses on tools and algorithms for fish behaviour quantification analysis. The goal is to present their basic concepts and principles, including the quantification analysis procedure and its potential application scenarios. This review shows that the most common behaviour quantification indexes can be categorised into three classes: swimming indexes, physical indexes and context indexes. Typically, swimming indexes are of the most interest to researchers. However, achieving comprehensiveness of the information and quantisation precision remain challenging in fish behaviour analysis. In brief, this paper aims to help researchers and practitioners better understand the current state‐of‐the‐art behavioural quantification analysis, which provides strong support for the implementation of intelligent breeding.
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Metabolic rate is intricately linked to the ecology of organisms and can provide a framework to study the behaviour, life history, population dynamics, and trophic impact of a species. Acquiring measures of metabolic rate, however, has proven difficult for large water-breathing animals such as sharks, greatly limiting our understanding of the energetic lives of these highly threatened and ecologically important fish. Here, we provide the first estimates of resting and active routine metabolic rate for the longest lived vertebrate, the Greenland shark (Somniosus microcephalus). Estimates were acquired through field respirometry conducted on relatively large-bodied sharks (33–126 kg), including the largest individual shark studied via respirometry. We show that despite recording very low whole-animal resting metabolic rates for this species, estimates are within the confidence intervals predicted by derived interspecies allometric and temperature scaling relationships, suggesting this species may not be unique among sharks in this respect. Additionally, our results do not support the theory of metabolic cold adaptation which assumes that polar species maintain elevated metabolic rates to cope with the challenges of life at extreme cold temperatures.
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Capabilities of remotely operated vehicles (ROVs) have increased substantially in the last decade, and mini-ROV designs are now able to conduct visual research frequently conducted by snorkellers or divers in shallow marine environments. There are logistical, financial and experimental benefits of using mini-ROVs over snorkellers or divers, yet the adoption of mini-ROVs for common shallow underwater research tasks has not been widespread. To assess the capabilities of mini-ROVs to sample fish communities we compared the results produced by a mini-ROV to that of snorkellers for performing two of the most common marine video-based research activities (1) underwater visual fish census and (2) observing and tracking fish behaviour. Results of both activities suggested that the fish community observed by the mini-ROV was not distinguishable to that observed by the snorkellers, however, the mini-ROV detected significantly more fish (39% higher abundance) and greater diversity (24% higher). When tracking butterflyfish behaviour, video obtained from the mini-mini-ROV was as efficient as a snorkeller at finding and tracking individuals. Video from the mini-ROV produced comparable responses to that from snorkellers with hand-held GoPros, although over the course of tracks the response between the two methods differed, with a decrease in refuge time for snorkeller video and an increase in tailbeat rate for the mini-ROV video. Our study shows that video obtained from mini-ROVs can be used for research in shallow marine environments when direct manipulations are not required. We predict the research capabilities of mini-ROVs to increase substantially in the coming years, which should cement the use of this tool for research across all marine environments.
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Summary Acoustic telemetry was used to monitor the swimming speed, depth and water temperature of three blue marlin (60 kg, 70 kg, 125 kg) and 165 h of continuous swimming speed data containing both sustained and burst swimming events were collected. Measurements of swimming speed show that, while blue marlin are capable of high speeds, they spend most of their time swimming slowly. The fastest sustained swimming speeds (80-120cms"') occurred during a 4-6h recovery period immediately after tagging when marlin consistently swim at depths greater than 50m. Short bursts of speeds up to 225cms"1 were usually associated with changes in depth. Slower swimming (15-25cms"1) occurred when fish were within 10 m of the surface. These velocities are similar to direct measurements of swimming speeds of free-swimming sharks, seals and sea lions, indicating that many large aquatic vertebrates swim slowly to minimize energetic costs of transport.
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Time-depth-speed recorders and stomach-temperature sensors were deployed on 11 harbor seals (Phoca vitulina) in the St. Lawrence estuary to examine their diving and foraging behavior. Fifty-four percent of dives were to depths of <4 m. Dives that were 4 m deep were classified into five distinct types, using a combination of principal components analysis and hierarchical and nonhierarchical clustering analyses. Feeding, indicated by a sharp decline in stomach temperature, occurred during dives of all five types, four of which were U-shaped, while one was V-shaped. Seals swam at speeds near the minimum cost of transport (MCT) during descents and ascents. V-shaped dives had mean depths of 5.8 m, lasted an average of 40 s, and often preceded or followed periods of shallow-water (<4 m) activity. Seals invariably dove to the bottom when performing U-shaped dives. These dives were to an average depth of 20 m during daylight and occurred in shallower waters (~8 m) at twilight and during the night. Once on the bottom, seals (i) swam at MCT speeds with occasional bursts of speed, (ii) swam at speeds near MCT but not exceeding it, or (iii) remained stationary or swam slowly at about 0.15 m/s, occasionally swimming faster. It is unlikely that all dives to depths 4 m are dedicated to foraging. However, the temporal segregation of dive types suggests that all types are used during foraging, although they may represent different strategies.
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This study documents activity patterns and diving behaviour of four bearded seal (Erignathus barbatus) mothers during the lactation period. The females spent 8 ± 3% (mean ± SD) of their time hauled out on the ice and 92 ± 3% in the water. Approximately half of their time was spent diving. During the study 15 077 dives were recorded. The duration of dives was 2.0 ± 2.3 min and diving depth was 17.2 ± 22.5 m (maximum 18.7 min and 288 m, respectively). Haulout periods occurred 3 ± 2 times per day (duration = 44.0 ± 98.1 min). The overall distance swum per day was 48.1 ± 23.2 km. Three dive types were differentiated using a combination of hierarchical and k-means clustering, one V-shaped grouping and two U-shaped groupings. The most common dive type was U1; these dives were the deepest and longest type (depth = 28 ± 32 m, duration = 185 ± 146 s), and bottom time occupied a significant fraction of the total dive time (120 ± 120 s). These dives are likely foraging dives. Lactation is energetically demanding for bearded seals, and females do forage while they have dependent pups.
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We used electromyogram (EMG) radiotelemetry to assess swimming activity (e.g., swim speeds), behaviour, and migration speeds (e.g., ground speeds) of individual adult sockeye salmon (Oncorhynchus nerka) migrating through several reaches of the Fraser and Nechako rivers in British Columbia. Using a laboratory swim flume and volitionally swimming adult fish carrying EMG transmitters, we developed relationships between EMG pulse intervals and swim speeds. A bioenergetics model was used to estimate reach-specific energy use per metre for each individual based on the average swim speed, migration time, body size, and river temperature. Migration was most energetically efficient (i.e., migration costs per unit distance traveled were relatively low) for females compared with males, large males compared with small males, and 1995 males compared with 1993 males. In all three cases, differences in swim speed patterns were primarily responsible for differences in energy use. For both sexes and in both years, migrations through reaches that contained a constriction (caused by an island, gravel bar, or large rock outcropping) were energetically inefficient compared with that through reaches with no constrictions. The high energetic costs at constrictions seem to result from long travel times probably caused by turbulent flow patterns that may generate confusing migrational cues. Résumé : Nous avons utilisØ la radiotØlØmØtrie avec Ølectromyogramme (EMG) pour Øvaluer líactivitØ natatoire (p. ex., vitesses de nage), le comportement et les vitesses de migration (p. ex., vitesses sol) de saumons rouges (Oncorhynchus nerka)
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Unusually deep water due to dam construc-tion has the potential to negatively effect endangered sturgeons, which lack a physiological mechanism to inflate their swimbladder and may be unable to remain buoyant under high pressure at depth. In a previous study, some juvenile sturgeons released in a deep (>100 m) reservoir lost buoyancy and stayed nearly motionless on the bottom. However, it is not clear whether this behavior represents a negative effect of the dam, because natural sturgeon swimming behavior is unknown. In this study, we attached multi-sensor data loggers to nine wild adult Chinese sturgeons Acipenser sinensis in an unimpounded reach of the Yangtze River, China. The depth utilization, tail beating activity, swim speed, and body inclination of these fish were monitored for 1–3 days. Fish swam up and down successively in the water column (mean depth, 9.9 m) with a cycle of 100–1,000 s during 64 % of the time on average, and stayed at depth, presumably on the riverbed, during rest periods. Tail beats were continuous (mean frequency, 0.77 Hz) throughout the records, indicating that their buoyancy was maintained. These results contrast with the previous study, suggesting that the behavior ob-served in the reservoir is unusual and that deep water poses a risk of losing buoyancy for sturgeons. Further-more, all fish intensively swam (maximum speed, 3.0 ms −1) to the river surface at a mean frequency of 0.35 times per hour—a behavior that could explain why ship strikes are a serious cause of mortality in sturgeons.
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We observed patterns in echograms of data collected with a dual-frequency identification sonar (DIDSON) that were related to the tail beats of fish. These patterns reflect the size, shape, and swimming motion of the fish and also depend on the fish’s angle relative to the axis of the beam. When the tail is large enough to reflect sound of sufficient intensity and the body is angled such that the tail beat produces periodic changes in the range extent covered by the fish image, then the tail beat becomes clearly visible on echograms that plot the intensity maximum of all beams. The analysis of DIDSON echograms of a mix of upstreammigrating Chinook salmon Oncorhynchus tshawytscha and sockeye salmon O. nerka resulted in the separation of two groups: (1) fish of sockeye salmon size that swam with a tail-beat frequency (TBF) between 2.0 and 3.5 beats/s and (2) fish of Chinook salmon size with a TBF between 1.0 and 2.0 beats/s. There was no correlation between TBF and fish size within each group, which suggests that the observed difference in TBF between the two groups was species-specific rather than an indirect effect of the groups’ difference in size. The technique of extracting TBF from DIDSON echograms may also be useful for bioenergetics studies. Compared with electromyogram telemetry, it offers the advantages of being nonintrusive and faster to set up and analyze and therefore is suitable for analyzing larger sample sizes. The disadvantages are that the technique’s potential is limited to relatively large fish, it can cover only relatively small areas, it cannot be used to follow individual fish over long distances, and some environments are too noisy to produce DIDSON images of sufficient quality.
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Although several studies have determined swimming speeds for Atlantic cod (Gadus morhua L.) using acoustic telemetry, none have reported high-resolution tracking (high sampling frequency) for individual fish in order to obtain more accurate estimates of swimming speeds and to quantify within- and between-individual variation. In this study, in situ swimming speed of acoustically tagged Atlantic cod were recorded with high resolution (position fixing every 17 s) throughout the diel cycle during summer in a fjord in northern Norway using a stationary positioning system. The frequency distributions of swimming speeds are presented for individual cod (~30-60 cm). The high-resolution tracking technique revealed higher swimming speeds than previously reported for cod. Swimming speeds below 1.0 body lengths (bl) s-1 were most common (>70%), with only 4-7% of the recordings above the sustained swimming speed for this species. The observation that cod employed a blend of swimming speeds could reflect that searching for and capturing different prey types require a mix of swimming speeds.
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Several methods to indirectly estimate metabolism of aquatic animals have been reported, including heart rate, electromyograms, video recording, and averaging velocity of an animal moving between two or more points. The present study carried out in the lagoon at Bimini Islands, Bahamas, used acoustic, speed-sensing transmitters to indirectly estimate energy consumption of 1.5–2 m subadult lemon sharks (Negaprion brevirostris). Speed records from three sharks tracked a total of 170 h, yielded average swimming speeds of 0.44–0.71 m s-1. These speeds were converted into energy consumption to obtain metabolism. By combining the estimates of metabolism with calculated values on assimilation and production, we are able to present a balanced bioenergetics model for the subadult lemon shark: 100C = 7P + 66M + 26E, where C = consumption, P = production, M = metabolism, and E = excretion. When comparing juvenile lemon sharks to subadults, an ontogenetic shift is seen: 0 to 2 yr olds allocate 22% of consumed energy to production and 50% to metabolism while 6 to 9 yr olds show values of 7% and 66%, respectively. We believe this to be the first field-based, balanced equation presented for any large elasmobranch.
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