Effects of disease on foraging behaviour and success in an individual free-ranging northern elephant seal.

Evaluating consequences of stressors on vital rates in marine mammals is of considerable interest to scientific and regulatory bodies. Many of these species face numerous anthropogenic and environmental disturbances. Despite its importance as a critical form of mortality, little is known about disease progression in air-breathing marine megafauna at sea. We examined the movement, diving, foraging behaviour and physiological state of an adult female northern elephant seal (Mirounga angustirostris) who suffered from an infection while at sea. Comparing her to healthy individuals, we identified abnormal behavioural patterns from high-resolution biologging instruments that are likely indicators of diseased and deteriorating condition. We observed continuous extended (3-30 minutes) surface intervals coinciding with almost no foraging attempts (jaw motion) during 2 weeks of acute illness early in her post-breeding foraging trip. Elephant seals typically spend ~ 2 minutes at the surface. There were less frequent but highly extended (30-200 minutes) surface periods across the remainder of the trip. Dive duration declined throughout the trip rather than increasing. This seal returned in the poorest body condition recorded for an adult female elephant seal (18.3% adipose tissue; post-breeding trip average is 30.4%). She was immunocompromised at the end of her foraging trip and has not been seen since that moulting season. The timing and severity of the illness, which began during the end of the energy-intensive lactation fast, forced this animal over a tipping point from which she could not recover. Additional physiological constraints to foraging, including thermoregulation and oxygen consumption, likely exacerbated her already poor condition. These findings improve our understanding of illness in free-ranging air-breathing marine megafauna, demonstrate the vulnerability of individuals at critical points in their life history, highlight the importance of considering individual health when interpreting biologging data and could help differentiate between malnutrition and other causes of at-sea mortality from transmitted data.

Brain activity of diving seals reveals short sleep cycles at depth.

Sleep is a crucial part of the daily activity patterns of mammals. However, in marine species that spend months or entire lifetimes at sea, the location, timing, and duration of sleep may be constrained. To understand how marine mammals satisfy their daily sleep requirements while at sea, we monitored electroencephalographic activity in wild northern elephant seals (Mirounga angustirostris) diving in Monterey Bay, California. Brain-wave patterns showed that seals took short (less than 20 minutes) naps while diving (maximum depth 377 meters; 104 sleeping dives). Linking these patterns to accelerometry and the time-depth profiles of 334 free-ranging seals (514,406 sleeping dives) revealed a North Pacific sleepscape in which seals averaged only 2 hours of sleep per day for 7 months, rivaling the record for the least sleep among all mammals, which is currently held by the African elephant (about 2 hours per day).

Whiskers as hydrodynamic prey sensors in foraging seals.

The darkness of the deep ocean limits the vision of diving predators, except when prey emit bioluminescence. It is hypothesized that deep-diving seals rely on highly developed whiskers to locate their prey. However, if and how seals use their whiskers while foraging in natural conditions remains unknown. We used animal-borne tags to show that free-ranging elephant seals use their whiskers for hydrodynamic prey sensing. Small, cheek-mounted video loggers documented seals actively protracting their whiskers in front of their mouths with rhythmic whisker movement, like terrestrial mammals exploring their environment. Seals focused their sensing effort at deep foraging depths, performing prolonged whisker protraction to detect, pursue, and capture prey. Feeding-event recorders with light sensors demonstrated that bioluminescence contributed to only about 20% of overall foraging success, confirming that whiskers play the primary role in sensing prey. Accordingly, visual prey detection complemented and enhanced prey capture. The whiskers' role highlights an evolutionary alternative to echolocation for adapting to the extreme dark of the deep ocean environment, revealing how sensory abilities shape foraging niche segregation in deep-diving mammals. Mammals typically have mobile facial whiskers, and our study reveals the significant function of whiskers in the natural foraging behavior of a marine predator. We demonstrate the importance of field-based sensory studies incorporating multimodality to better understand how multiple sensory systems are complementary in shaping the foraging success of predators.

Cyanide sensitivity in direct electron transfer-type bioelectrocatalysis by membrane-bound alcohol dehydrogenase from Gluconobacter oxydans.

An overexpression system of membrane-bound alcohol dehydrogenase (ADH) from Gluconobacter oxydans was constructed to examine its bioelectrocatalytic characteristics. The effects of cyanide (CN-) addition on the kinetics of direct electron transfer (DET)-type bioelectrocatalysis by ADH were analyzed. CN- enhanced the bioelectrocatalytic activity, while the catalytic activity in the solution remained unchanged, even in the presence of CN-. Electrochemical methods and electron spin resonance spectroscopy showed the detailed electron transfer pathway in the DET-type bioelectrocatalysis by ADH. Briefly, ADH is suggested to communicate with an electrode via a CN--insensitive and H+-sensitive heme c in DET. These characteristics of ADH with respect to CN- suggest the involvement of ADH in CN--insensitive respiration in G. oxydans.

Forced into an ecological corner: Round-the-clock deep foraging on small prey by elephant seals.

Small mesopelagic fishes dominate the world's total fish biomass, yet their ecological importance as prey for large marine animals is poorly understood. To reveal the little-known ecosystem dynamics, we identified prey, measured feeding events, and quantified the daily energy balance of 48 deep-diving elephant seals throughout their oceanic migrations by leveraging innovative technologies: animal-borne smart accelerometers and video cameras. Seals only attained positive energy balance after feeding 1000 to 2000 times per day on small fishes, which required continuous deep diving (80 to 100% of each day). Interspecies allometry suggests that female elephant seals have exceptional diving abilities relative to their body size, enabling them to exploit a unique foraging niche on small but abundant mesopelagic fish. This unique foraging niche requires extreme round-the-clock deep diving, limiting the behavioral plasticity of elephant seals to a changing mesopelagic ecosystem.

Seasonal resource pulses and the foraging depth of a Southern Ocean top predator.

Seasonal resource pulses can have enormous impacts on species interactions. In marine ecosystems, air-breathing predators often drive their prey to deeper waters. However, it is unclear how ephemeral resource pulses such as near-surface phytoplankton blooms alter the vertical trade-off between predation avoidance and resource availability in consumers, and how these changes cascade to the diving behaviour of top predators. We integrated data on Weddell seal diving behaviour, diet stable isotopes, feeding success and mass gain to examine shifts in vertical foraging throughout ice break-out and the resulting phytoplankton bloom each year. We also tested hypotheses about the likely location of phytoplankton bloom origination (advected or produced in situ where seals foraged) based on sea ice break-out phenology and advection rates from several locations within 150 km of the seal colony. In early summer, seals foraged at deeper depths resulting in lower feeding rates and mass gain. As sea ice extent decreased throughout the summer, seals foraged at shallower depths and benefited from more efficient energy intake. Changes in diving depth were not due to seasonal shifts in seal diets or horizontal space use and instead may reflect a change in the vertical distribution of prey. Correspondence between the timing of seal shallowing and the resource pulse was variable from year to year and could not be readily explained by our existing understanding of the ocean and ice dynamics. Phytoplankton advection occurred faster than ice break-out, and seal dive shallowing occurred substantially earlier than local break-out. While there remains much to be learned about the marine ecosystem, it appears that an increase in prey abundance and accessibility via shallower distributions during the resource pulse could synchronize life-history phenology across trophic levels in this high-latitude ecosystem.

Lightscapes of fear: How mesopredators balance starvation and predation in the open ocean.

Like landscapes of fear, animals are hypothesized to strategically use lightscapes based on intrinsic motivations. However, longitudinal evidence of state-dependent risk aversion has been difficult to obtain in wild animals. Using high-resolution biologgers, we continuously measured body condition, time partitioning, three-dimensional movement, and risk exposure of 71 elephant seals throughout their 7-month foraging migrations (N = 16,000 seal days). As body condition improved from 21 to 32% fat and daylength declined from 16 to 10 hours, seals rested progressively earlier with respect to sunrise, sacrificing valuable nocturnal foraging hours to rest in the safety of darkness. Seals in superior body condition prioritized safety over energy conservation by resting >100 meters deeper where it was 300× darker. Together, these results provide empirical evidence that marine mammals actively use the three-dimensional lightscape to optimize risk-reward trade-offs based on ecological and physiological factors.

Development Perspective of Bioelectrocatalysis-Based Biosensors.

Bioelectrocatalysis provides the intrinsic catalytic functions of redox enzymes to nonspecific electrode reactions and is the most important and basic concept for electrochemical biosensors. This review starts by describing fundamental characteristics of bioelectrocatalytic reactions in mediated and direct electron transfer types from a theoretical viewpoint and summarizes amperometric biosensors based on multi-enzymatic cascades and for multianalyte detection. The review also introduces prospective aspects of two new concepts of biosensors: mass-transfer-controlled (pseudo)steady-state amperometry at microelectrodes with enhanced enzymatic activity without calibration curves and potentiometric coulometry at enzyme/mediator-immobilized biosensors for absolute determination.

Acceleration-triggered animal-borne videos show a dominance of fish in the diet of female northern elephant seals.

Knowledge of the diet of marine mammals is fundamental to understanding their role in marine ecosystems and response to environmental change. Recently, animal-borne video cameras have revealed the diet of marine mammals that make short foraging trips. However, novel approaches that allocate video time to target prey capture events is required to obtain diet information for species that make long foraging trips over great distances. We combined satellite telemetry and depth recorders with newly developed date-/time-, depth- and acceleration-triggered animal-borne video cameras to examine the diet of female northern elephant seals during their foraging migrations across the eastern North Pacific. We obtained 48.2 h of underwater video, from cameras mounted on the head (n=12) and jaw (n=3) of seals. Fish dominated the diet (78% of 697 prey items recorded) across all foraging locations (range: 37-55°N, 122-152°W), diving depths (range: 238-1167 m) and water temperatures (range: 3.2-7.4°C), while squid comprised only 7% of the diet. Identified prey included fish such as myctophids, Merluccius sp. and Icosteus aenigmaticus, and squid such as Histioteuthis sp., Octopoteuthis sp. and Taningia danae Our results corroborate fatty acid analysis, which also found that fish are more important in the diet, and are in contrast to stomach content analyses that found cephalopods to be the most important component of the diet. Our work shows that in situ video observation is a useful method for studying the at-sea diet of long-ranging marine predators.

Direct electron transfer-type bioelectrocatalysis of FAD-dependent glucose dehydrogenase using porous gold electrodes and enzymatically implanted platinum nanoclusters.

The direct electron transfer (DET)-type bioelectrocatalysis of flavin adenine dinucleotide (FAD)-dependent glucose dehydrogenase (GDH) from Aspergillus terreus (AtGDH) was carried out using porous gold (Au) electrodes and enzymatically implanted platinum nanoclusters (PtNCs). The porous Au electrodes were prepared by anodization of planar Au electrodes in a phosphate buffer containing glucose as a reductant. Moreover, PtNCs were generated into AtGDH by an enzymatic reduction of hexachloroplatinate (IV) ion. The modification was confirmed by native polyacrylamide gel electrophoresis and sodium dodecyl sulfate polyacrylamide gel electrophoresis analyses. The AtGDH-adsorbed porous Au electrode showed a DET-type bioelectrocatalytic wave both in the presence and absence of PtNCs; however, the current density with PtNCs (~1 mA cm-2 at 0 V vs. Ag|AgCl|sat. KCl) was considerably higher than that without PtNCs. The kinetic and thermodynamic analysis of the steady-state catalytic wave indicated that inner PtNCs shortened the distance between the catalytic center of AtGDH (=FAD) and the conductive material, and improved the heterogeneous electron transfer kinetics between them.

Bioelectrocatalytic performance of d-fructose dehydrogenase.

This review summarizes the bioelectrocatalytic properties of d-fructose dehydrogenase (FDH), while taking into consideration its enzymatic characteristics. FDH is a membrane-bound flavohemo-protein with a molecular mass of 138 kDa, and it catalyzes the oxidation of d-fructose to 5-keto-d-fructose. The characteristic feature of FDH is its strong direct-electron-transfer (DET)-type bioelectrocatalytic activity. The pathway of the DET-type reaction is discussed. An overview of the application of FDH-based bioelectrocatalysis to biosensors and biofuel cells is also presented, and the benefits and problems associated with it are extensively discussed.

Oxygen minimum zone: An important oceanographic habitat for deep-diving northern elephant seals, Mirounga angustirostris.

Little is known about the foraging behavior of top predators in the deep mesopelagic ocean. Elephant seals dive to the deep biota-poor oxygen minimum zone (OMZ) (>800 m depth) despite high diving costs in terms of energy and time, but how they successfully forage in the OMZ remains largely unknown. Assessment of their feeding rate is the key to understanding their foraging behavior, but this has been challenging. Here, we assessed the feeding rate of 14 female northern elephant seals determined by jaw motion events (JME) and dive cycle time to examine how feeding rates varied with dive depth, particularly in the OMZ. We also obtained video footage from seal-mounted videos to understand their feeding in the OMZ. While the diel vertical migration pattern was apparent for most depths of the JME, some very deep dives, beyond the normal diel depth ranges, occurred episodically during daylight hours. The midmesopelagic zone was the main foraging zone for all seals. Larger seals tended to show smaller numbers of JME and lower feeding rates than smaller seals during migration, suggesting that larger seals tended to feed on larger prey to satisfy their metabolic needs. Larger seals also dived frequently to the deep OMZ, possibly because of a greater diving ability than smaller seals, suggesting their dependency on food in the deeper depth zones. Video observations showed that seals encountered the rarely reported ragfish (Icosteus aenigmaticus) in the depths of the OMZ, which failed to show an escape response from the seals, suggesting that low oxygen concentrations might reduce prey mobility. Less mobile prey in OMZ would enhance the efficiency of foraging in this zone, especially for large seals that can dive deeper and longer. We suggest that the OMZ plays an important role in structuring the mesopelagic ecosystem and for the survival and evolution of elephant seals.

The foraging benefits of being fat in a highly migratory marine mammal.

Foraging theory predicts that breath-hold divers adjust the time spent foraging at depth relative to the energetic cost of swimming, which varies with buoyancy (body density). However, the buoyancy of diving animals varies as a function of their body condition, and the effects of these changes on swimming costs and foraging behaviour have been poorly examined. A novel animal-borne accelerometer was developed that recorded the number of flipper strokes, which allowed us to monitor the number of strokes per metre swam (hereafter, referred to as strokes-per-metre) by female northern elephant seals over their months-long, oceanic foraging migrations. As negatively buoyant seals increased their fat stores and buoyancy, the strokes-per-metre increased slightly in the buoyancy-aided direction (descending), but decreased significantly in the buoyancy-hindered direction (ascending), with associated changes in swim speed and gliding duration. Overall, the round-trip strokes-per-metre decreased and reached a minimum value when seals achieved neutral buoyancy. Consistent with foraging theory, seals stayed longer at foraging depths when their round-trip strokes-per-metre was less. Therefore, neutrally buoyant divers gained an energetic advantage via reduced swimming costs, which resulted in an increase in time spent foraging at depth, suggesting a foraging benefit of being fat.