Feeding requirements of white sharks may be higher than originally thought

Quantifying the energy requirements of animals in nature is critical for understanding physiological, behavioural, and ecosystem ecology; however, for difficult-to-study species such as large sharks, prey intake rates are largely unknown. Here, we use metabolic rates derived from swimming speed estimates to suggest that feeding requirements of the world's largest predatory fish, the white shark (Carcharodon carcharias), are several times higher than previously proposed. Further, our estimates of feeding frequency identify a clear benefit in seasonal selection of pinniped colonies - a white shark foraging strategy seen across much of their range.

U nderstanding the energetic requirements of organisms in their natural environment is fundamental to ecosystem ecology, as the energetic benefits and costs associated with their activities will heavily influence life-history strategies and trophic relationships. Inherent difficulties in studying marine predatory behaviour in the wild have hindered our understanding of the energetic requirements and associated trophic relationships of apex predators. In the case of pelagic predatory sharks, approaches that provide energetic data are urgently needed, as many of these species are highly vulnerable to overexploitation 1 .
White sharks Carcharodon carcharias (Lamnidae) are apex marine predators with a circumglobal distribution. Their longevity, late maturity and low fecundity renders them highly susceptible to overexploitation 2 . The population status of white sharks is poorly known over the species' range due to a lack of robust abundance indicators, given it is protected throughout much of its range and only caught as a fisheries bycatch species or as part of shark control programs 2 . Additionally, despite their protected status, white sharks are still regularly incidentally caught in various fishing gear throughout their range 3,4 . Even at very low levels of anthropogenic mortality, modelled white shark populations have greatly increased doubling times 5 , and declines in relative catch rates have been reported in parts of their range, e.g. Refs. 3,6. There is however, conjecture surrounding the magnitude of some of these declines 7-9 and some evidence for slight increases in relative catch rates in the last 10-20 years in parts of their range, e.g. Refs 3,4. Shifting from a predominantly piscivorous diet to one dominated by marine mammals at approximately 3.4 m in total length 10 , large white sharks are regular visitors to seal breeding colonies. For example, the Neptune Islands (South Australia) supports the largest seal colony in Australia, and white sharks are most abundant in the area during winter-spring when weaned New Zealand (NZ) fur seals Arctocephalus forsteri are present 11 .
Energy requirements of large sharks are poorly documented. The only published study of white shark energetics in the wild estimated the field metabolic rate (MR) of a single individual from telemetered muscle temperature data as the individual moved from cold to warm water 12 . The authors used their MR estimates to suggest a 943 kg white shark could survive on 30 kg of marine mammal blubber for approximately 1.5 months; a widely cited figure that has perpetuated the assumption that large sharks only need to feed every few weeks to maintain net energy gain.
Here, we combine estimates of swimming speeds [ Fig. 1] and measurements of standard (resting for an obligate ram-ventilator) MR (SMR) in young-of-the-year (YOY) white sharks 13 , with swim-tunnel respirometry data from closely-related shortfin mako sharks Isurus oxyrinchus (Lamnidae) 14 to estimate field routine metabolic rates (RMR), total daily energy expenditure (TDE), and feeding requirements of white sharks at a NZ fur seal colony at the Neptune Islands, South Australia.

Results
Throughout the entire monitoring period, 9,969 swim speed estimates were obtained across all individuals. The distribution of swimming speeds was strongly positively-skewed, so we calculated median swimming speeds as well as mean estimates. The grand mean swimming speed (n 5 12) was estimated as 2.91 6 0. 16

Discussion
Our estimate of total daily energy expenditure (TDE) suggests white sharks feed far more frequently than previously estimated 12 and does not support the proposal that white sharks could survive at energy balance on 30 kg of marine mammal blubber for 1.5 months (44.1 d). Indeed, the mass-specific MR estimated by Refs. 12 for a 943 kg white shark was more than 12-times lower than our estimate for smaller (428 6 61 kg, mean 6 s.e.m., n 5 12) sharks (60 versus 723 mg O 2 kg 21 h 21 ). Given that absolute MR scales with body size with an exponent of ,0.8 for most fish including sharks 15,16 , it is unsurprising that our mass-specific MR estimate is higher than that of a much larger animal. However, if the measurements of SMR in ,30 kg sharks 13  Our estimated daily ration of 1.5-1.8% wbw d 21 is highly comparable to the mean ration (estimated directly from the amount of food eaten) for captive YOY white sharks 17 (1.2% wbw d 21 ), after scaling for differences in body mass between the YOY and adult white sharks. Furthermore, our daily ration is comparable to that estimated for free-ranging mako sharks 18 (2.3-2.8% wbw d 21 ), after scaling for differences in body mass between the mako and white sharks.
The new estimate of white shark RMR has implications for assessing the likely feeding frequency of this species. Using our estimate of RMR, 30 kg of blubber (27.9 MJ kg 21 ) would provide a 943 kg (the weight of the shark examined by Ref. 12) white shark with sufficient energy for approximately 11.6 days, which is about four times less than that calculated by Ref. 12 [ Table 1]. The winter-spring water temperature at the Neptune Islands, where we recorded the swimming speeds of white sharks, is 15.35 6 0.86uC (mean 6 s.d.). This is very similar to that recorded by Refs. 12 (14.7-16.7uC) during their measurement of MR, and as such cannot in itself account for the high RMR estimated. However, our RMR estimate takes into account the high levels of activity needed for a white shark to 'patrol' a seal colony (e.g. 2.9 6 0.2 m s 21 , grand mean 6 s.e.m, n 5 12; 0.81 TL s 21 ), including burst speeds up to 10 m s 21 [,2.85 TL s 21 for a 3.5 m shark, Fig. 1(b)]. When a median value of swimming speed is used (2. 25  Given their high metabolic rates, white sharks may target seal colonies to predate on seasonally abundant and more vulnerable weaned pups 20 , rather than adult seals or patchily-distributed fish. Silver seabream is a common teleost prey of Australian white sharks 21 , and while the energy density of both prey items are similar (9.4 MJ kg 21 and 8.8 MJ Kg 21 for weaned seal pups and silver seabream, respectively), the smaller mean size of silver seabream would necessitate at least one (1.0) successful predation event per day to maintain energy balance, compared to less than one (0.3) if targeting weaned seal pups. However, to contribute any energy toward growth and reproduction, they would need to eat more than one silver seabream per day, but would be in positive energy balance if predating on seal pups every third day. Patchily-distributed reef-associated prey such as C. auratus have been described as 'less-visitable' for white sharks 22 given the prey's ability to disperse and shelter among complex habitat. Hence, there may be a distinct energetic advantage in targeting one prey item every few days in a predictable (revisitable) habitat such as a seal colony 14 , compared to pursuing and capturing more than one prey item every day in a less-visitable patch (i.e. silver seabream aggregation). During the summer-autumn periods when the weaned pups are not present, white sharks are less common at the Neptune Islands, and during these periods sharks have been tracked moving away from the Neptune Islands to areas where large finfish aggregations (including species such as silver seabream) occur 21 . This movement is accompanied by a shift in search pattern from that approximating Brownian motion at the seal colony (predicted behaviour when prey is abundant) to movement well approximated by a specialized random walk known as a Lévy flight, predicted when foraging for sparsely-distributed prey in more open shelf and pelagic environments 22 . This indicates that feeding on finfish aggregations may be more efficient than foraging for adult seals that are less vulnerable to predation than juveniles 20 .
Our study suggests that due to high metabolic rates, white sharks need to feed more regularly than has been previously assumed 12,23,24 . Given direct observations of feeding frequency are generally not possible for apex marine predators and that the majority of information available is inferred from behavioural information, fieldenergetic approaches such as that used in this study may help to answer key ecological questions for a broad suite of such taxa, the populations of which are currently under immense pressure from  (1) represents that determined for a shortfin mako shark, and U in Eq (1) is the value calculated from our swim speed estimates (TL s 21 ). Total daily energy expenditure (TDE, MJ) was calculated from field RMR using an oxycalorific coefficient of 13.55 kJ g 21 O 2 (Ref. 28). To determine the number of weaned NZ fur seal pups needed to be consumed at this TDE to maintain energy balance and the associated daily ration (% wbw d 21 ; calculated as per Ref. 18) we used an energy content value (9.4 MJ kg 21 ) based on that for closely-related Antarctic fur seal pups (Arctocephalus gazella) 29 , with a mean weaned NZ fur seal pup weight of 14.6 kg (Ref. 11) and an assimilation value of 73% (Ref. 30). This was also undertaken for a dominant teleost prey of white sharks throughout their Australian range 21