Unexpected Formation of 11(9→7)-abeo-Steroid Skeleton in Synthetic Studies toward Batrachotoxin.

Batrachotoxin (1) is a potent cardio- and neurotoxic steroid isolated from certain species of frogs, birds, and beetles. We previously disclosed two synthetic routes to 1. During our synthetic studies toward 1, we explored an alternative strategy for efficiently assembling its 6/6/6/5-membered steroidal skeleton (ABCD-ring). Here we report the application of intermolecular Weix and intramolecular pinacol coupling reactions. While Pd/Ni-promoted Weix coupling linked the AB-ring and D-ring fragments, SmI2-mediated pinacol coupling did not cyclize the C-ring. Instead, we discovered that SmI2 promoted a 1,4-addition of the α-alkoxy radical intermediate to produce the unusual 11(9→7)-abeo-steroid skeleton. Thus, this study demonstrates the convergent assembly of the skeleton of the natural product matsutakone in 11 steps from 2-allyl-3-hydroxycyclopent-2-en-1-one.

The vulnerability of sharks, skates, and rays to ocean deoxygenation: Physiological mechanisms, behavioral responses, and ecological impacts.

Levels of dissolved oxygen in open ocean and coastal waters are decreasing (ocean deoxygenation), with poorly understood effects on marine megafauna. All of the more than 1000 species of elasmobranchs (sharks, skates, and rays) are obligate water breathers, with a variety of life-history strategies and oxygen requirements. This review demonstrates that although many elasmobranchs typically avoid hypoxic water, they also appear capable of withstanding mild to moderate hypoxia with changes in activity, ventilatory responses, alterations to circulatory and hematological parameters, and morphological alterations to gill structures. However, such strategies may be insufficient to withstand severe, progressive, or prolonged hypoxia or anoxia where anaerobic metabolic pathways may be used for limited periods. As water temperatures increase with climate warming, ectothermic elasmobranchs will exhibit elevated metabolic rates and are likely to be less able to tolerate the effects of even mild hypoxia associated with deoxygenation. As a result, sustained hypoxic conditions in warmer coastal or surface-pelagic waters are likely to lead to shifts in elasmobranch distributions. Mass mortalities of elasmobranchs linked directly to deoxygenation have only rarely been observed but are likely underreported. One key concern is how reductions in habitat volume as a result of expanding hypoxia resulting from deoxygenation will influence interactions between elasmobranchs and industrial fisheries. Catch per unit of effort of threatened pelagic sharks by longline fisheries, for instance, has been shown to be higher above oxygen minimum zones compared to adjacent, normoxic regions, and attributed to vertical habitat compression of sharks overlapping with increased fishing effort. How a compound stressor such as marine heatwaves alters vulnerability to deoxygenation remains an open question. With over a third of elasmobranch species listed as endangered, a priority for conservation and management now lies in understanding and mitigating ocean deoxygenation effects in addition to population declines already occurring from overfishing.

Formal Total Synthesis of Batrachotoxin Enabled by Radical and Weix Coupling Reactions.

Batrachotoxin (1), originally isolated from a Columbian poison-dart frog, is a steroidal alkaloid. Its 6/6/6/5-membered carbocycle (ABCD-ring) contains two double bonds, one nitrogen, and five oxygen functionalities. We developed a radical-based convergent strategy and realized the total synthesis of 1 in 28 steps. The AB-ring and D-ring fragments were efficiently synthesized and linked by exploiting a powerful Et3B/O2-mediated radical coupling reaction. Vinyl triflate and vinyl bromide were then utilized for a Pd/Ni-promoted Weix coupling reaction to cyclize the C-ring. A hydroxy group of the C-ring was stereoselectively installed by a decarboxylative hydroxylation reaction to prepare an advanced intermediate of our previous total synthesis of 1.

Identification of serum and glucocorticoid-regulated kinase 1 as a regulator of signal transducer and activator of transcription 3 signaling.

Signal transducer and activator of transcription 3 (STAT3) plays key roles in cancer cell proliferation, invasion, and immunosuppression. In many human cancer cells, STAT3 is hyperactivated, which leads to tumor progression and drug resistance, and therefore STAT3 and its modulators are considered effective drug targets. However, the complex regulatory mechanisms of STAT3 have made it difficult to develop potent anticancer drugs that suppress its activity. Here, we report serum and glucocorticoid-regulated kinase 1 (SGK1) as a novel regulator of STAT3 signaling and an effective target for combination therapy with Janus kinase (JAK) inhibitors. We screened small molecules using a gain-of-function mutant of STAT3 resistant to JAK inhibition and found that an SGK1 inhibitor suppressed the constitutive activation of STAT3. Importantly, our results revealed that SGK1 also mediated the activation of wild-type STAT3. Further examination suggested that the tuberous sclerosis complex 2 and mammalian target of rapamycin signaling pathway were involved in STAT3 activation by SGK1. Finally, we demonstrated that SGK1 inhibition enhanced the inhibitory effect of a JAK inhibitor on STAT3 phosphorylation and cancer cell proliferation. Our findings provide new insights into the molecular mechanisms of STAT3 activation and suggest SGK1 as a potential target for STAT3-targeted combination cancer therapy.

Decreased thymic output predicts progression of chronic kidney disease.

BACKGROUND: Chronic kidney disease (CKD) is age-related disease, and decreased renal function is associated with the premature aging of T cells and increased incidence of other age-related diseases. However, the relationship between T cell senescence and CKD progression remains unclear. Here, we investigated the relationship between T cell senescence, as indicated by decreased thymic output and increased proportion of highly differentiated CD28- T cells, and CKD progression. RESULTS: A total of 175 patients with non-dialysis-dependent CKD were enrolled in this study. Thymic output was assessed based on the CD45RA+CD31+CD4+ cell (recent thymic emigrant [RTE]) counts (RTEs) (/mm3) and the proportion of RTE among CD4+ T cells (RTE%). Highly differentiated T cells were assessed based on the proportion of CD28- cells among CD4+ T cells (CD28-/CD4+) and CD28- cells among CD8+ T cells (CD28-/CD8+). The primary outcome was estimated glomerular filtration rate (eGFR) decline of ≥40% or initiation of renal replacement therapy. The association between T cell senescence and renal outcomes was examined using Cox proportional hazards models and restricted cubic splines. The median age was 73 years, 33% were women, and the median eGFR was 26 mL/min/1.73 m2. The median RTEs, RTE%, CD28-/CD4+, and CD28-/CD8+ were 97.5/mm3, 16.2, 5.3, and 49.7%, respectively. After a median follow-up of 1.78 years, renal outcomes were observed in 71 patients. After adjusting for age, sex, eGFR, proteinuria, diabetes, and cytomegalovirus seropositivity, decreased RTEs, which corresponded to decreased thymic output, significantly and monotonically increased the risk of poor renal outcome (p = 0.04), and decreased RTE% and increased highly differentiated CD28-/CD4+ T cells also tended to monotonically increase the risk (p = 0.074 and p = 0.056, respectively), but not CD28-/CD8+ T cells. CONCLUSIONS: Decreased thymic output in CKD patients, as well as increased highly differentiated CD4+ T cells, predicted renal outcomes. Thus, the identification of patients prone to CKD progression using T cell senescence, particularly decreased RTE as a biomarker, may help to prevent progression to end-stage kidney disease.

Ultrahigh foraging rates of Baikal seals make tiny endemic amphipods profitable in Lake Baikal.

Understanding what, how, and how often apex predators hunt is important due to their disproportionately large effects on ecosystems. In Lake Baikal with rich endemic fauna, Baikal seals appear to eat, in addition to fishes, a tiny (<0.1 g) endemic amphipod Macrohectopus branickii (the world's only freshwater planktonic species). Yet, its importance as prey to seals is unclear. Globally, amphipods are rarely targeted by single-prey feeding (i.e., nonfilter-feeding) mammals, presumably due to their small size. If M. branickii is energetically important prey, Baikal seals would exhibit exceptionally high foraging rates, potentially with behavioral and morphological specializations. Here, we used animal-borne accelerometers and video cameras to record Baikal seal foraging behavior. Unlike the prevailing view that they predominantly eat fishes, they also hunted M. branickii at the highest rates (mean, 57 individuals per dive) ever recorded for single-prey feeding aquatic mammals, leading to thousands of catches per day. These rates were achieved by gradual changes in dive depth following the diel vertical migration of M. branickii swarms. Examining museum specimens revealed that Baikal seals have the most specialized comb-like postcanine teeth in the subfamily Phocinae, allowing them to expel water while retaining prey during high-speed foraging. Our findings show unique mammal-amphipod interactions in an ancient lake, demonstrating that organisms even smaller than krill can be important prey for single-prey feeding aquatic mammals if the environment and predators' adaptations allow high foraging rates. Further, our finding that Baikal seals directly eat macroplankton may explain why they are so abundant in this ultraoligotrophic lake.

Total Synthesis of (-)-Batrachotoxin Enabled by a Pd/Ag-Promoted Suzuki-Miyaura Coupling Reaction.

Batrachotoxin is an extremely potent cardio- and neurotoxic steroidal alkaloid found in certain species of frogs, birds, and beetles. The steroidal 6/6/6/5-membered carbocycle (ABCD-ring) is U-shaped and functionalized with two double bonds, a six-membered C3-hemiacetal across the AB-ring, a seven-membered oxazepane on the CD-ring, and a dimethylpyrrolecarboxy group at the D-ring carbon chain. These structural features present an unusual and formidable synthetic challenge. Herein we report a total synthesis of batrachotoxin based on a newly devised convergent strategy through a 22-step sequence. Enantiopure AB-ring and D-ring fragments were prepared and subjected to a crucial C(sp2 )-C(sp2 ) coupling reaction. Although both C(sp2 ) centers were sterically encumbered by proximal tetrasubstituted carbon atoms, Ag2 O strongly promoted the Pd(PPh3 )4 -catalyzed Suzuki-Miyaura coupling reaction at room temperature, thereby connecting the two fragments without damaging their preexisting functionalities. Subsequent treatment with t-BuOK induced Dieckmann condensation to cyclize the C-ring. The judiciously optimized functionalizations realized oxazepane formation, carbon chain extension, and pyrrole carboxylic acid condensation to deliver batrachotoxin.

Life in the slow lane: field metabolic rate and prey consumption rate of the Greenland shark (Somniosus microcephalus) modelled using archival biologgers.

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 that 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 modelled 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 (±s.d.) FMR of 21.67±2.30 mg O2 h-1 kg-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 mg O2 h-1 kg-0.84 (n=6; PSATs) over an entire year. When considering prey consumption rate, an average shark in these systems (224 kg) requires a maintenance ration of 61-193 g of fish or marine mammal prey daily. As Greenland sharks are a lethargic polar species, these low FMR estimates, and corresponding prey consumption estimates, suggest they 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, which is essential given growing pressures from climate change and expanding commercial fisheries in the Arctic.

Too big to study? The biologging approach to understanding the behavioural energetics of ocean giants.

Wild animals are under selective pressure to optimise energy budgets; therefore, quantifying energy expenditure, intake and allocation to specific activities is important if we are to understand how animals survive in their environment. One approach toward estimating energy budgets has involved measuring oxygen consumption rates under controlled conditions and constructing allometric relationships across species. However, studying 'giant' marine vertebrates (e.g. pelagic sharks, whales) in this way is logistically difficult or impossible. An alternative approach involves the use of increasingly sophisticated electronic tags that have allowed recordings of behaviour, internal states and the surrounding environment of marine animals. This Review outlines how we could study the energy expenditure and intake of free-living ocean giants using this 'biologging' technology. There are kinematic, physiological and theoretical approaches for estimating energy expenditure, each of which has merits and limitations. Importantly, tag-derived energy proxies can hardly be validated against oxygen consumption rates for giant species. The proxies are thus qualitative, rather than quantitative, estimates of energy expenditure, and have more limited utilities. Despite this limitation, these proxies allow us to study the energetics of ocean giants in their behavioural context, providing insight into how these animals optimise their energy budgets under natural conditions. We also outline how information on energy intake and foraging behaviour can be gained from tag data. These methods are becoming increasingly important owing to the natural and anthropogenic environmental changes faced by ocean giants that can alter their energy budgets, fitness and, ultimately, population sizes.

A framework to estimate the likelihood of species interactions and behavioural responses using animal-borne acoustic telemetry transceivers and accelerometers.

Interactions between animals structure food webs and regulate ecosystem function and productivity. Quantifying subsurface 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 subsurface interactions occur and test for a movement-related behavioural 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 tag to quantitatively assess fine-scale behaviour during detection events, that is 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 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 behavioural 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.

Swimming strategies and energetics of endothermic white sharks during foraging.

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.

Distribution, body size and biology of the megamouth shark Megachasma pelagios.

We compiled historical reports of megamouth sharks Megachasma pelagios (mostly fishery by-catch and strandings) from 1976 to 2018 (n = 117) and found that they are distributed globally (highest latitude, 36°) with three hotspots: Japan, Taiwan and the Philippines. Despite possible biases due to variability in fishing effort, more individuals were reported at higher latitudes in the summer, suggesting seasonal, latitudinal migrations. Sex ratios were female-biased in Japan, but more even in Taiwan and the Philippines, suggesting some sexual segregation. Females (total length, LT = 3.41-7.10 m) were larger than males (LT = 1.77-5.39 m) and matured at a larger LT (5.17 m) than males (4.26 m). Also, we reviewed the systematics, feeding ecology and swimming behaviour of Megachasma pelagios based on the literature. Our review shows that, compared with their morphology, anatomy and genetics, behavioural ecology of this species remains largely unknown and electronic tagging studies are warranted.

A miniaturized threshold-triggered acceleration data-logger for recording burst movements of aquatic animals.

Although animal-borne accelerometers are effective tools for quantifying the kinematics of animal behaviors, quantifying the 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 movements of various small and agile animals.

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes.

Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources.

Global Monitoring of Persistent Organic Pollutants (POPs) Using Seabird Preen Gland Oil.

Situated at high positions on marine food webs, seabirds accumulate high concentrations of persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane and its metabolites (DDTs), and hexachlorocyclohexanes (HCHs). Our previous studies proposed the usefulness of seabirds preen gland oil as a nondestructive biomonitoring tool. The present study applied this approach to 154 adult birds of 24 species collected from 11 locations during 2005-2016 to demonstrate the utility of preen gland oil as a tool for global monitoring POPs, i.e., PCBs, DDTs, and HCHs. Concentrations of the POPs were higher in the Northern Hemisphere than in the Southern Hemisphere. In particular, ∑20PCBs and∑DDTs were highly concentrated in European shags (Phalacrocorax aristotelis) and Japanese cormorants (Phalacrocorax capillatus), explainable by a diet of benthic fishes. Higher concentrations of γ-HCH were detected in species from the polar regions, possibly reflecting the recent exposure and global distillation of ∑HCHs. We examined the relationship between age and POP concentrations in preen gland oil from 20 male European shags, aged 3-16 years old. Concentrations and compositions of POPs were not related to age. We also examined sex differences in the POP concentrations from 24 streaked shearwaters (Calonectris leucomelas) and did not detect a sex bias. These results underline the importance of the geographic concentration patterns and the dietary behavior as determinants species-specific POPs concentrations in preen gland oil.

Flight mode affects allometry of migration range in birds.

Billions of birds migrate to exploit seasonally available resources. The ranges of migration vary greatly among species, but the underlying mechanisms are poorly understood. I hypothesise that flight mode (flapping or soaring) and body mass affect migration range through their influence on flight energetics. Here, I compiled the tracks of migratory birds (196 species, weighing 12-10 350 g) recorded by electronic tags in the last few decades. In flapping birds, migration ranges decreased with body mass, as predicted from rapidly increasing flight cost with increasing body mass. The species with higher aspect ratio and lower wing loading had larger migration ranges. In soaring birds, migration ranges were mass-independent and larger than those of flapping birds, reflecting their low flight costs irrespective of body mass. This study demonstrates that many animal-tracking studies are now available to explore the general patterns and the underlying mechanisms of animal migration.

Linking animal-borne video to accelerometers reveals prey capture variability.

Understanding foraging is important in ecology, as it determines the energy gains and, ultimately, the fitness of animals. However, monitoring prey captures of individual animals is difficult. Direct observations using animal-borne videos have short recording periods, and indirect signals (e.g., stomach temperature) are never validated in the field. We took an integrated approach to monitor prey captures by a predator by deploying a video camera (lasting for 85 min) and two accelerometers (on the head and back, lasting for 50 h) on free-swimming Adélie penguins. The movies showed that penguins moved the heads rapidly to capture krill in midwater and fish (Pagothenia borchgrevinki) underneath the sea ice. Captures were remarkably fast (two krill per second in swarms) and efficient (244 krill or 33 P. borchgrevinki in 78-89 min). Prey captures were detected by the signal of head acceleration relative to body acceleration with high sensitivity and specificity (0.83-0.90), as shown by receiver-operating characteristic analysis. Extension of signal analysis to the entire behavioral records showed that krill captures were spatially and temporally more variable than P. borchgrevinki captures. Notably, the frequency distribution of krill capture rate closely followed a power-law model, indicating that the foraging success of penguins depends on a small number of very successful dives. The three steps illustrated here (i.e., video observations, linking video to behavioral signals, and extension of signal analysis) are unique approaches to understanding the spatial and temporal variability of ecologically important events such as foraging.

Drift dives and prolonged surfacing periods in Baikal seals: resting strategies in open waters?

Many pinnipeds frequently rest on land or ice, but some species remain in open waters for weeks or months, raising the question of how they rest. A unique type of dive, called drift dives, has been reported for several pinnipeds with suggested functions of rest, food processing and predator avoidance. Prolonged surfacing periods have also been observed in captive seals and are thought to aid food processing. However, information from other species in a different environment would be required to better understand the nature and function of this behavior. In this study, we attached multi-sensor tags to Baikal seals Pusa sibirica, a rare, freshwater species that has no aquatic predators and few resting grounds during the ice-free season. The seals exhibited repeated drift dives (mean depth, 116 m; duration, 10.1 min) in the daytime and prolonged periods at the surface (mean duration, 1.3 h) mainly around dawn. Drift dives and prolonged surfacing periods were temporally associated and observed between a series of foraging dives, suggesting a similar function, i.e. a combination of resting and food processing. The maximum durations of both drift and foraging dives were 15.4 min, close to the aerobic dive limit of this species; therefore, metabolic rates might not be significantly depressed during drift dives, further supporting the function of food processing rather than purely resting. Our results also show that drift diving can occur in a predator-free environment, and thus predator avoidance is not a general explanation of drift dives in pinnipeds.

Optical coherence tomography imaging for analysis of follicular development in ovarian tissue.

We describe the application of optical coherence tomography (OCT) for noninvasive analysis of follicular development in mouse ovaries. Ovaries contain many follicles and oocytes. Quantification of follicles at various developmental stages is an indication of the ability of an ovary to provide oocytes capable of fertilization. Three-dimensional structural OCT images identified each developmental stage, from a primary follicle (50 µm in diameter) to an antral follicle (350 µm in diameter), in the ovary of a 25.5-day-old mouse. We discovered time-varying OCT signals at the oocytes that differentiated them from surrounding tissues. These signals were clearly enhanced by interframe intensity-based Doppler OCT techniques. The OCT technology was effective in analyzing the development of follicles and oocytes in ovaries.

Testing optimal foraging theory in a penguin-krill system.

Food is heterogeneously distributed in nature, and understanding how animals search for and exploit food patches is a fundamental challenge in ecology. The classic marginal value theorem (MVT) formulates optimal patch residence time in response to patch quality. The MVT was generally proved in controlled animal experiments; however, owing to the technical difficulties in recording foraging behaviour in the wild, it has been inadequately examined in natural predator-prey systems, especially those in the three-dimensional marine environment. Using animal-borne accelerometers and video cameras, we collected a rare dataset in which the behaviour of a marine predator (penguin) was recorded simultaneously with the capture timings of mobile, patchily distributed prey (krill). We provide qualitative support for the MVT by showing that (i) krill capture rate diminished with time in each dive, as assumed in the MVT, and (ii) dive duration (or patch residence time, controlled for dive depth) increased with short-term, dive-scale krill capture rate, but decreased with long-term, bout-scale krill capture rate, as predicted from the MVT. Our results demonstrate that a single environmental factor (i.e. patch quality) can have opposite effects on animal behaviour depending on the time scale, emphasizing the importance of multi-scale approaches in understanding complex foraging strategies.