Summary Temperature strongly regulates the distribution and fitness of ectotherms, and many studies have measured the temperature dependence of physiological performance in controlled laboratory settings. In contrast, little is known about how temperature influences ectotherm performance in the wild, so the ecological significance of physiological performance as measured in the laboratory is unclear. Our aim was to measure the temperature dependence of performance in the wild for several species of fishes and to explore how temperatures that maximize performance in the wild (ToptE) are related to species biogeographies. We gathered body activity and growth data from the wild for nine tropical and temperate fish species, and by fitting thermal performance curves to these data, compared ToptE to species‐specific warm range boundary temperatures (the average temperature of the warmest month at equatorward range limits). To explore the degree to which trends in the wild reflect trends in physiological performance measured in the laboratory, we also compiled published data on the temperature dependence of aerobic metabolic scope in fishes and compared these to our wild fish data. We found ToptE in the wild was strongly correlated with warm range boundary temperatures, and that the difference between these two temperatures (the ‘environmental heating tolerance’) was smaller for more‐tropical species. Comparison with laboratory data revealed that ToptE approaches warm boundary temperatures in the wild at the same rate that the optimal temperature for aerobic scope (ToptAS) approaches upper critical temperatures (upper Tcrit) for aerobic scope in the laboratory, meaning that environmental heating tolerances in wild fishes closely mirror physiological heating tolerance (i.e. upper Tcrit − ToptAS) in captive fishes. Our comparison of field‐ and laboratory‐derived data highlights the ecological significance of aerobic metabolic scope in fishes and suggests wild fish species tend to perform best near the highest temperatures encountered in their range while maintaining a safety margin from the deleterious effects of upper critical temperatures.
Acoustic telemetry has emerged as a leading approach to infer diel, tidal and lunar rhythmicity in the movements of aquatic organisms in a range of taxa. Typically, studies examine the relative frequency of detections from individuals tagged with acoustic transmitters, and then infer patterns in the species' behaviour, but studies to date have not controlled for factors that may influence tag detection patterns in the absence of animal behaviour. We compared patterns in acoustic detections from tagged cuttlefish Sepia apama and several fixed-location control tags, and used these data to highlight the danger of misinterpreting patterns in the absence of adequate controls. Cuttlefish and control tags displayed similar detection patterns, and correcting cuttlefish-detection data for the influence of environmental factors resulted in the opposite pattern of cuttlefish activity displayed prior to correction. This study highlights the danger of using acoustic data to infer animal behaviour in the absence of adequate controls.KEY WORDS: Acoustic telemetry · Rhythmicity · Behaviour · Diel · Activity · Temporal Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 419: [295][296][297][298][299][300][301] 2010 strongly influence detection frequency (e.g. wind speed, biological noise, current speeds; Heupel et al. 2006) typically occur with diel, tidal or lunar frequency, so it is likely that one may detect rhythmic patterns in detection frequency in the complete absence of tagged-animal behaviour. Consequently, using these types of analyses to create inferences about animal behaviour is justified only if the influence of alternative factors is discounted through the employment of controls. With the increasing frequency and scale of acoustic arrays deployed worldwide, the need to accurately interpret acoustic data has never been greater. Of the myriad of acoustic telemetry studies that use the relative frequency of detections to make inferences about animal behaviour, we could find no published studies that report the use of fixedlocation control tags to separate the patterns in detection frequency due to animal behaviour from those due to other (i.e. environmental) factors. Jackson et al. (2005) deployed a fixed-location reference tag to compare detection efficiency between different tagattachment methods (also with S. apama), but that study did not examine patterns in detection frequency through time.Here we examined the relationship between acoustic detections from tagged giant Australian cuttlefish Sepia apama and fixed-position control tags to show that patterns in detection frequency from animal tags are strongly influenced by factors other than animal behaviour. MATERIALS AND METHODSStudy site, species and tagging. Sepia apama (n = 7) were collected via SCUBA from breeding grounds at Point Lowly, South Australia (33°00' S, 137°44' E) during July of 2009 and tagged with Vemco acoustic transmitters (V9AP-2L, 69 kHz, 3.3 g in water, 46 mm length, mean delay 120 s...
Ectotherms generally shrink under experimental warming, but whether this pattern extends to wild populations is uncertain. We analysed ten million visual survey records, spanning the Australian continent, multiple decades and comprising all common coastal reef fish (335 species). We found that temperature indeed drives spatial and temporal changes in fish body size, but not consistently in the negative fashion expected. Around 55% of species were smaller in warmer waters (especially among small-bodied species) while 45% were bigger. The direction of a species' response to temperature through space was generally consistent with its response to temperature increase at any given location, suggesting that spatial trends could help forecast fish responses to warming. However, temporal changes were ~10x faster than spatial trends (~4% versus ~40% body size change per 1°C change through space and time respectively). The rapid and variable responses of
Ectotherms from higher latitudes can generally perform over broader temperature ranges than tropical ectotherms. This pattern is thought to reflect trends in temperature variability: tropical ectotherms evolve to be 'thermal specialists' because their environment is thermally stable. However, the tropics are also hotter, and most physiological rates increase exponentially with temperature. Using a dataset spanning diverse ectotherms, we show that the temperature ranges ectotherms tolerate (the difference between lower and upper critical temperatures, and between optimum and upper critical temperatures) generally represents the same range of equivalent biological rates (e.g. metabolism) for cool- and warm-adapted species, and independent of latitude or elevation. This suggests that geographical trends in temperature variability may not be the ultimate mechanism underlying latitudinal and elevational trends in thermal tolerance. Rather, we propose that tropical ectotherms can perform over a narrower range of temperatures than species from higher latitudes because the tropics are hotter.
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.
Summary1. Estimating the metabolic rate of animals in nature is central to understanding the physiological, behavioural and evolutionary ecology of animals. Doubly labelled water and heart-rate methods are the most commonly used approaches, but both have limitations that preclude their application to some systems. 2. Accelerometry has emerged as a powerful tool for estimating energy expenditure in a range of animals, but is yet to be used to estimate field metabolic rate in aquatic taxa. We combined two-dimensional accelerometry and swim-tunnel respirometry to estimate patterns of energy expenditure in giant Australian cuttlefish Sepia apama during breeding. 3. Both oxygen consumption rate ( _ Vo 2 ) and swimming speed showed strong positive associations with body acceleration, with coefficients of determination comparable to those using similar accelerometers on terrestrial vertebrates. Despite increased activity during the day, field metabolic rate rarely approached _ Vo 2 , and night-time _ Vo 2 was similar to that at rest. 4. These results are consistent with the life-history strategy of this species, which has a poor capacity to exercise anaerobically, and a mating strategy that is visually based. With the logistical difficulties associated with observation in aquatic environments, accelerometry is likely to prove a valuable tool for estimating energy expenditure in aquatic animals.
The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.
Summary1. Body size is a key determinant of metabolic rate, but logistical constraints have led to a paucity of energetics measurements from large water-breathing animals. As a result, estimating energy requirements of large fish generally relies on extrapolation of metabolic rate from individuals of lower body mass using allometric relationships that are notoriously variable. Swim-tunnel respirometry is the 'gold standard' for measuring active metabolic rates in water-breathing animals, yet previous data are entirely derived from body masses <10 kg -at least one order of magnitude lower than the body masses of many top-order marine predators. 2. Here, we describe the design and testing of a new method for measuring metabolic rates of large waterbreathing animals: a c. 26 000 L seagoing 'mega-flume' swim-tunnel respirometer. We measured the swimming metabolic rate of a 2Á1-m, 36-kg zebra shark Stegostoma fasciatum within this new mega-flume and compared the results to data we collected from other S. fasciatum (3Á8-47Á7 kg body mass) swimming in static respirometers and previously published measurements of active metabolic rate measurements from other shark species. 3. The mega-flume performed well during initial tests, with intra-and interspecific comparisons suggesting accurate metabolic rate measurements can be obtained with this new tool. Inclusion of our data showed that the scaling exponent of active metabolic rate with mass for sharks ranging from 0Á13 to 47Á7 kg was 0Á79; a similar value to previous estimates for resting metabolic rates in smaller fishes. 4. We describe the operation and usefulness of this new method in the context of our current uncertainties surrounding energy requirements of large water-breathing animals. We also highlight the sensitivity of mass-extrapolated energetic estimates in large aquatic animals and discuss the consequences for predicting ecosystem impacts such as trophic cascades.
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