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KEY WORDS: Predator ecology · Climate variation · El Niño · Shark · Seal · Temperature
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movements may be limited to water temperatures modeling has revealed that El Niño-Southern Oscilla-
within a fundamental thermal range defined by tion (ENSO) can influence interannual variability of
physiological tolerance (Kearney & Porter 2009, Agulhas leakage SST with a 2 yr time lag, which sub-
Allen-Ankins & Stoffels 2017) and, among elasmo- sequently affects regional climate variability (Putrasa-
branchs, individuals may behaviorally thermoregu- han et al. 2016), including ENSO effects on water
late by moving among different water temperatures temperatures in False Bay (Dufois & Rouault 2012).
to optimize hunting, digestion, and gestation (Hight Here, we compared changes in white shark predation
& Lowe 2007, Di Santo & Bennett 2011, Ketchum et patterns, in terms of successful and unsuccessful pre-
al. 2014, Papastamatiou et al. 2015). Experimental dation attempts on seals, in relation to environmental
exposure of sharks and other aquatic predators to and temporal variability and ENSO events, over a
warmer water temperatures in the laboratory have 15 yr period. In our analysis, explanatory environ-
shown increased hunting effort and feeding rate mental and temporal variables tested against shark
(Dowd et al. 2006, Miller et al. 2014, Pistevos et al. predation rates included water temperature and visi-
2015); however, comparative studies in the wild bility at the site, and the variables day of year (DOY),
involving large mobile fish are lacking due to logisti- month, and year to account for change over time
cal and technological challenges. Moreover, most
experiments have been over relatively short dura-
tions (weeks to months) and have not been able to MATERIALS AND METHODS
provide insight into how long-term (years to decades)
climate variability may directly impact ecological Predation events
processes, such as predation intensity. Thus, it re-
mains unknown how long-term climate cycles and Seal Island (35° 8’ 6” S, 18° 35’ 00” E) in False Bay,
temperature variability may impact the biology and South Africa, is inhabited by approx. 60 000 Cape fur
ecology of aquatic top predators. seals (Fig. 1). White sharks Carcharodon carcharias
As with other members of the lamnidae family, aggregate here during the winter to actively hunt
white sharks Carcharodon carcharias are partially Cape fur seals Arctocephalus pusillus pusillus when
endothermic elasmobranch fish, with stomach tem- they leave and return from Seal Island (Martin et al.
peratures measured up to 14.3°C higher than that of 2005, 2009). The seals forage in False Bay or up to
the surrounding water (Goldman 1997). Given that 30 km (or greater) offshore, returning to Seal Island
white sharks can modulate their body temperature to at irregular intervals (Martin et al. 2005, Fallows et
some extent, within a narrow range (e.g. 23.4−26.7°C, al. 2012). Seals travel to and from the island via por-
Goldman 1997), recurrent predation patterns are poising at the surface (Fallows et al. 2012). Thus,
likely due to behavioral optimization of predation for white shark attacks on seals occur at the water sur-
energy intake rather than for a need to maintain opti- face, where they can be documented (Hammerschlag
mal body temperature (as opposed to teleost fishes et al. 2006, Martin & Hammerschlag 2012). Attacks
(Pink et al. 2016)). False Bay, South Africa, is the are concentrated on the southern side of the island,
location of a long-term monitoring program on the close to shore (within 2 km). Thus, by positioning at
predation rates of white sharks on Cape fur seals the south end of Seal Island where most predatory
Arctocephalus pusillus pusillus (Martin et al. 2005, activity occurs, a single vessel can survey at least
2009, Hammerschlag et al. 2006, 2012, 2017, Fallows 270° uninterrupted to a distance of at least 3.5 km
et al. 2012, 2013, 2016, Martin & Hammerschlag 2012) (Hammerschlag et al. 2006, Martin et al. 2009). Ob-
as well as a site of ongoing climate and temperature servations were made at Seal Island each month, by
monitoring (Dufois & Rouault 2012). Accordingly, the 1 boat, between 1999 and 2013. At least part of the
system provides an opportunity to investigate for pos- research team averaged some 200 d per year on the
sible relationships between climate-driven tempera- water, although the majority of observation occurred
ture variability and predation rates by a marine apex during austral winter months (May−September),
predator. when most predatory activity occurs (Hammerschlag
The climate of the study region is influenced by sea- et al. 2006). The research vessel arrived and began
surface temperature (SST) leakage from the Agulhas observations at Seal Island at about 07:00 h (~1.5 h
current (known as Agulhas leakage), which transports before sunrise), sea conditions permitting. Although
warm and saline waters from the Indian Ocean (Gor- multiple people were on the observation boat each
don & Haxby 1990, de Ruijter et al. 1999, van Sebille day, the data in this study was restricted to that gath-
et al. 2009, Beal et al. 2011). However, recent climate ered by a trained observer (C. Fallows) onboard.
Skubel et al.: Long-term climate and shark predation trends 131
level pressure, zonal and meridional components of both constituent terms are in the model, after which
surface wind, sea surface temperature, surface air point the single terms may be removed. For the
temperature, and cloudiness fraction of the sky) annual GLM, explanatory variables tested were
(Wolter & Timlin 1993, 1998). ENSO classification annual means of Tw , Vis, and wind, the standard
was based on historically ranked MEI values (1 deviation of annual Tw to look for effects of variabil-
through 67), with the upper quartile (54−67) indica- ity, and whether an El Niño or La Niña event had
ting an El Niño and lower quartile (1−14) indicating a occurred that year from May−September (indicated
La Niña. by a binary 0 for no, and 1 for yes). Putrasahan et al.
(2016) indicated a 2 yr lag in thermal impacts found
for the region; however, comparison of 2 yr-lagged
Data analysis Tw from our dataset with MEI did not show a signifi-
cant trend, so a second iteration of the annual GLM
For each day, kills (K) and unsuccessful attempted run with 2 yr-lagged El Niño or La Niña event occur-
predations (AP) by white sharks upon seals were rence was not included in the results. Wind was not
averaged over the sample period of 07:00−09:30 h to included in the daily model as there was insufficient
calculate an hourly rate of kills and total predations. data coverage, reducing the number of observations
This yielded a single value of kill rate (K h−1) and total in the model to 185 of 1085 observation days. Vari-
predation rate (K+AP h−1) for each day of observation ables were judged as significant in the model if they
within the standardized sampling period. The broader were significant at p < 0.05 (t-statistic versus the con-
(K+AP) h−1 metric showed hunting effort, while the K stant model). All analyses were performed in Matlab
h−1metric indicated presumed seal consumption by (Mathworks). Although SST was initially considered
the animal, and putatively, some extent of metabolic in the monthly GLMs, models produced for both K
demand fulfilment. Given that each of K h−1and h−1and (K+AP) h−1 were over-parameterized and had
(K+AP) h−1 were assigned on a daily basis, it was not lower performance than those fitted without SST, so
feasible to directly compare the 2 metrics as a direct SST was excluded from the final GLMs.
measure of relative predation success. Rather, each
was considered independently as a measure of gen-
eral predation patterns. Daily, monthly, and annual RESULTS
scale generalized linear models (GLMs) were used to
explore relationships of kill rates and total predation Over the study period from 1999−2013, SST and Tw
rates with environmental variability. For the daily measured during the observational period showed
GLM, explanatory variables tested were water tem- overall similar seasonal and interannual variability
perature (Tw, °C) and water visibility (Vis, m) meas- (Fig. 2a). When the Furono record of Tw (monthly
ured at the site, and the variables day of year (DOY), mean) from the study site and remotely-sensed SST
mo, and yr to account for change over time. For the for the region were compared, the 2 data sets demon-
monthly GLM, explanatory variables tested were strated consistent monthly variations in temperature
monthly means of Tw, Vis, and wind speed (wind, trends. However, a 2-way t-test comparing the
knots), and an indication of ENSO status via the MEI. monthly means of the 2 data sets revealed statistical
GLMs were constructed in Matlab using a stepwise difference (p = 9.04 × 10−5), reflecting differences in
procedure with interactions, using the default method the spatial and temporal coverage of the 2 data sets.
of ‘sse’ to determine model criterion. Here, the func- While Furono measured daily temperatures at Seal
tion ‘stepwiseglm’ begins with an initial model con- Island, the remotely sensed SST encompassed a
taining all terms, then uses forward and backward broader regional area. Further, Tw captured water
stepwise regression to construct the final model, temperature at the time of predation observation
comparing the explanatory power of these smaller or expeditions (morning) versus the more encompass-
larger models via the p-value of an F-test of change ing daytime SST which was capable of capturing
in sum of squared error (SSE) with addition or warmer temperatures over the course of the entire
removal of terms. Terms themselves are added or diel period. Although SST tended to be higher than
removed based on whether the term would have a Tw , temporal trends were generally similar among
zero coefficient once added to the model (or the term the 2 datasets, supporting the use of the daily water
is removed from the model if it has a zero coefficient temperature measurements from the predation ob-
when included, e.g. in the initial model or with suc- servation expeditions. El Niño conditions based on
cessive steps). Interaction terms are not added unless the MEI occurred in 2002, 2005, 2006, 2009, and
Skubel et al.: Long-term climate and shark predation trends 133
Fig. 2. Monthly trends in (a) daily water temperature (Tw) and sea surface temperature (SST) measured during predation ob-
servation expeditions, (b) multivariate ENSO index (MEI) and El Niño/La Niña status, (c) daily wind speed and visibility (Vis)
measured during predation observation expeditions, and (d) daily kills per hour (K h−1) and total predations (kills plus
attempted predations per hour, (K +AP) h−1) measured during predation observation periods. Standard deviation is indicated
by the shaded area around the main trendline in panels a, c and d
2012, while La Niña conditions occurred in 1999, from June through September (Fig. 2d). Years 2003,
2007, 2010, and 2011 (Fig. 2b). 2004, 2005, and 2007 exhibited the greatest magni-
From 1999 through 2013 from May through Sep- tude peaks in (K+AP) h−1 during this season (Figs. 2a
tember, a total of 1085 observation periods occurred & 3). Frequency distributions of Tw for all daily obser-
between 07:00 and 09:30 h, 941 of which featured vational periods, and those days with either K h−1 or
successful and/or unsuccessful predations of white (K+AP) h−1 greater than zero, show that most preda-
sharks Carcharodon carcharias upon Cape fur seals tion effort, successful and otherwise peaked at
Arctocephalus pusillus pusillus and 801 of which 14−14.5°C (10.8% of all observations), although this
featured successful attacks. A comparison of daily, may have been an artefact of the distribution of
monthly, and annual (K+AP) h−1 and K h−1 showed observation effort (Fig. 3).
consistently strong and significant Pearson correla- GLMs constructed for daily K h−1 and (K+AP) h−1
tion coefficients (r = 0.875, 0.934, 0.957 and p = 0, had significant yet weak fits (adjusted r2 for the
1.19 × 10−31, 2.32 × 10−8 for daily, monthly, and annual model and p-value for the F-statistic = 0.173 and 6.97
scales respectively), while a t-test showed the 2 met- × 10−20 and 0.222 and 1.14 × 10−26 for K h−1 and (K+AP)
rics to be significantly different (p = 7.73 × 10−43, 2.91 h−1, respectively). Model fit for monthly GLMs of K
× 10−7, 7.73 × 10−43 for daily, monthly, and annual h−1 and (K+AP) h−1 had similarly weak fits, with lower
scales respectively). Predation intensity peaked in the significance (adjusted r2 for the model and p-value
austral winter, with the greatest K h−1 and (K+AP) h−1 for the F-statistic = 0.245 and 0.00221 and 0.139 and
134 Mar Ecol Prog Ser 587: 129–139, 2018
DISCUSSION
Table 1. For daily, monthly, and annual generalized linear models of kills + attempted predations per hour, (K+AP) h−1, and
kills per hour, K h−1: coefficient estimates, SE, t-statistic, and p-value of each variable included in the final model, adjusted r2,
number of observations (obs.), F-statistic versus the initial model, and p-value of the F-statistic. Abbreviated variables are
water temperature (Tw), visibility (Vis), day of year (DOY), El Niño (EN), and La Niña (LN).
Coefficient SE t p
speculative to presume that our measurements cap- sence of Tw from these annual models suggests that,
tured this ENSO-modulated variability in wind speed, at a local scale, ENSO-influenced water temperatures
particularly given that meteorological teleconnections had minimal effects on white shark predation. How-
differ between ENSO events (Gershunov & Barnett ever, it is possible that ENSO-mediated changes in
1998). Although the annual GLMs indicated that El water temperature are impacting predation-related
Niño and La Niña occurrence had explanatory power factors external to the study area surrounding Seal Is-
for inter-annual variability in predation rates, the ab- land; for instance, large-scale changes in biological
136 Mar Ecol Prog Ser 587: 129–139, 2018
productivity under El Niño conditions (Barber & lated, its direct impact on metabolic demand could
Chavez 1983). not be ascertained. Complicating estimates of change
Greater visibility appeared to have a negative in metabolic rate with respect to temperature in the
effect on both kill and total predation rates across white shark, (1) the large body size of this species
temporal scales; Robbins (2007) found that increased allows for thermal inertia with movement through
visibility was inversely related to white shark pres- heterogeneous water temperatures, and (2) heat
ence at Neptune Island (Australia). In the present shedding is facilitated through manipulation of the
study, low visibility may lead to greater abundance, hepatic sinus which bypasses the suprahepatic rete
and thus greater chance of observing an attack, or (Carey et al. 1981). As white sharks are among the
the lower visibility may provide a higher chance of largest elasmobranchs (Compagno 1984, Schmidt-
success for the attacking shark as an individual may Nielsen 1984) and have a lower surface area to vol-
be less visually apparent to the targeted seal (Martin ume ratio for gaining or losing heat, they may be less
& Hammerschlag 2012). Given the high energetic re- sensitive to temperature variability than smaller spe-
quirements of a predation attempt, white sharks are cies given greater capacity for thermal inertia. Simi-
observed to launch attacks on seals only when envi- larly, metabolic Q10 has been found to be higher with
ronmental conditions are optimal for success, increas- lower body mass, suggesting higher sensitivity to
ing efficiency of energy expenditure (Hammerschlag temperature with smaller-bodied species and the
et al. 2006). These conditions include targeting seals inverse for larger species (Du Preez et al. 1988);
during a specific range of low-light levels as well as given that the white shark’s ability to regulate body
staging attacks from identifiable deep-water loca- temperature, the Q10 value may have less signifi-
tions around the Island that provide sharks with a cance for metabolic rate in response to ambient tem-
visual and tactical advantage over seals (Hammer- perature change. In our study, daily and monthly
schlag et al. 2006, Martin et al. 2009). GLMs suggested that increasing Tw corresponded
Considering the 2 metrics of predation patterns, with increasing (K+AP) h−1 and K h−1, but the influ-
both (K+AP) h−1 and K h−1 showed similar temporal ence of water temperature was not supported on an
trends (Fig. 2d) and frequency distribution with re- inter-annual scale. Taken together with the heat reg-
spect to water temperature (Fig. 3), as well as similar ulation capacity of white sharks, it is not directly evi-
final GLMs. However, kill rates tended to have dent that the predation patterns observed here were
higher model fit (adjusted r2), which may have been a result of rising metabolic demand with temperature.
due to this metric showing slightly greater corre- Both a strength and limitation of this study is that
spondence to variability in the explanatory variables our results are based on comparing long-term obser-
considered, while total predation rates may be more vational data sets and not controlled laboratory ex-
reflective of shark presence as a whole. However, periments. Although it appears that predation trends
without direct evidence of physiological response to across daily, monthly, and annual timescales are re-
changes in environmental condition (e.g. telemetry lated to environmental and seasonal (temporal) vari-
of internal temperature as per Goldman (1997) or ability, there are several other factors that could have
swimming speed as per Semmens et al. (2013)) it is contributed, at least partly, to the documented changes
not possible to draw inferences from our measure- in predation rates and likely contributed to the vari-
ments of kill rates to conclusions regarding metabo- ability unexplained by the GLM. These factors could
lism or feeding. include, for example, variability in seal, shark and
Change in ambient Tw can influence metabolic de- teleost abundance. Although seal population size has
mand (e.g. metabolic Q10), with an estimated Q10 of been shown to be relatively consistent over the study
between 2 and 3 presumed for the white shark as per period (Kirkman et al. 2007), there may be unac-
Carlson et al. (2004). Change in metabolic rate with counted marginal changes impacting predation.
temperature increase has not been directly measured White shark population declines have been specu-
for this species, although studies have measured lated for the region based on mark-recapture and
body temperature as an indicator (Carey et al. 1982, genetic analysis (Andreotti et al. 2016), although
McCosker 1987, Goldman 1997) or body mass and interpreted with some level of skepticism (Irion et al.
swimming speed (Semmens et al. 2013) as field- 2017). Further, white shark sightings have declined
based approaches to estimating metabolic rate. at Seal Island in False Bay over a 9 yr monitoring
White shark oxygen consumption has previously period (Hewitt et al. 2018). If predation rates were
been measured in transit to an aquarium (Ezcurra et reflective of white shark population trends alone,
al. 2012); however as temperature was not manipu- such as those suggested in the aforementioned stud-
Skubel et al.: Long-term climate and shark predation trends 137
ies, it would likely manifest as prolonged long-term and escape speeds (Grigaltchik et al. 2012, Creel et
declines in predation rates, rather than the alternat- al. 2016), contributing to asynchronous trophic rela-
ing increases and decreases observed here. Changes tionships. These questions highlight areas for directed
in teleost prey cannot be ruled out, however were not future experimentation when considering climate-
monitored in this investigation. Future studies includ- driven effects on predator–prey dynamics.
ing measurement of prey abundance may be reveal- In summary, our analysis of white shark predation
ing of ecosystem-level interactions among predators rates on seals paired with environmental monitoring
and other constituents of the regions they occupy. over 15 years suggests that water temperatures on an
One of the major challenges in projecting the climate intra-annual scale might contribute to predation pat-
response of a predatory species is unknowns sur- terns in white sharks either directly or indirectly, but
rounding respective spatial shifts in predator−prey do not implicate water temperature as a primary
distribution (Winder & Schindler 2004); namely, will driver of predation rates in this scenario, or on an
there be changes in overlap (Hunsicker et al. 2013), interannual scale. In contrast, inter-annual variability
or will predators remain synchronized with their prey in predation rate appeared linked to other environ-
species (Sergeant et al. 2014). Given the role of wind mental factors (wind, water visibility, and the occur-
and visibility in the GLMs, we recommend further rence of El Niño and La Niña events) which may
study exploring how local meteorology may impact drive both prey abundance and predation efficacy.
spatiotemporal patterns of predator and prey abun- Quantifying ecosystem-scale change in the wild to a
dance, and predation behavior. Further, the strong reliable and useful extent is not a feasible goal in
signal of temporal variability in intra-annual preda- many natural systems due to known and unknown
tion patterns may be tied to broader seasonal shifts in complexities, and the limits of scientific measure-
diet of white sharks, which may be explored via ment in capturing these complexities. However, pro-
methods such as stable isotope analysis and oppor- longed monitoring of species with known predator−
tunistic stomach content analysis. prey relationships, such as the white shark and Cape
Laboratory experiments with Port Jackson sharks fur seal Arctocephalus pusillus pusillus in False Bay,
Heterodontus portusjacksoni exposed to water tem- may provide an opportunity for ongoing investiga-
perature increases to projected 2100 levels increased tions of how climate variability might impact the eco-
their feeding but not growth (compared to a control logy of an ecosystem and for generating hypotheses
treatment), as feeding simply supplemented the rise to be tested in controlled experimental studies.
in metabolic demand associated with higher temper-
atures (Pistevos et al. 2015). However, oceanographic Acknowledgements. We thank all the assistants, partici-
consequences of climate change are not limited to a pants, and filmmakers throughout the years that supported
temperature increase. Indeed, with increasing CO2 this work, including the guests and crew of Apex Shark
emissions comes increased ocean acidification (IPCC Expeditions that made data collection possible. This work
was conducted under permits from the South African
2013), which has been shown to negatively impact Department of Environmental Affairs and with permission
olfactory ability and hunting behavior of some sharks from the University of Miami Institutional Animal Welfare
in controlled settings (Dixson et al. 2015, Pistevos et and Care Committee.
al. 2015). If the hunting ability of white sharks is im-
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Editorial responsibility: Alistair Hobday, Submitted: January 18, 2017; Accepted: November 20, 2017
Hobart, Tasmania, Australia Proofs received from author(s): January 22, 2018