To pup or not to pup? Using physiology and dive behavior to answer the Weddell Seal's overwinter question

Thesis (Ph.D.) University of Alaska Fairbanks, 2015Female Weddell seals (Leptonychotes weddellii) haul-out on the fast-ice surrounding the Antarctic continent in October and November each year to give birth to and nurse their pups. Breeding follows directly after weaning (December) and the annual molt begins in January-February. Animals reduce foraging efforts during the lactation and molting periods, but very little is known regarding the influence of this reduced activity on physiological condition. After a period of embryonic diapause, the annual molt coincides with embryo attachment and the start of active gestation. Consequently, female physiological condition at this time may influence reproductive success the following year. Overall female health and the ability to forage successfully throughout the gestation period (austral winter) may impact the likelihood that a pregnancy is brought to term. Therefore, this study tested whether overwinter changes in Weddell seal physiology and foraging efforts are reflected in reproductive outcomes the following year (i.e., to answer the over winter question of "to pup or not to pup?"). From 2010-2012, 100 (January-February: n = 53; October-November: n = 47) adult female Weddell seals were captured in Erebus Bay, Antarctica to assess overwinter changes in physiological condition and/or dive behavior that may be associated with reproductive success. Morphometric measurements and isotopic dilution procedures revealed that female Weddell seals gain ~10-15% of their body mass across the winter period, primarily in the form of blubber and lipid mass. The proportion of mass and lipid gain was similar regardless of whether females returned the following year and successfully gave birth, or did not produce a pup. Further, the amount of mass and energy acquired across gestation in the Weddell seal was markedly less than previously reported for other phocid species. Despite changes in activity patterns and body composition, Weddell seals maintained blood hemoglobin and muscle myoglobin concentrations across the winter. Therefore, Weddell seal total body oxygen stores and calculated aerobic dive limit (cADL) were conserved. This ensures that females have the physiological capabilities to effectively forage directly following the annual molt when they are at their leanest and must regain body mass and lipid stores. Although aerobic capacities did not change, dive effort varied considerably throughout the austral winter. Proxies of dive effort (duration, depth, %dives > cADL) were highest just after the molt (January-February) and just prior to the subsequent pupping season (August-September). Additionally, the proportion of each day spent diving increased mid-winter. Females that were observed the following year with a pup significantly increased all indices of foraging effort during the austral winter as compared to females that returned without a pup. This study is the first to identify and measure differences in dive efforts due to reproductive status, and indicates that successful reproduction is associated with greater foraging effort

Temporal changes in Weddell seal dive behavior over winter: are females increasing foraging effort to support gestation?

© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Ecology and Evolution, 8(23), (2018): 11857-11874. doi: 10.1002/ece3.4643.In capital‐breeding marine mammals, prey acquisition during the foraging trip coinciding with gestation must provide energy to meet the immediate needs of the growing fetus and also a store to meet the subsequent demands of lactation. Weddell seals (Leptonychotes weddellii) that give birth following the gestational (winter) foraging period gain similar proportions of mass and lipid as compared to females that fail to give birth. Therefore, any changes in foraging behavior can be attributed to gestational costs. To investigate differences in foraging effort associated with successful reproduction, twenty‐three satellite tags were deployed on post‐molt female Weddell seals in the Ross Sea. Of the 20 females that returned to the area the following year, 12 females gave birth and eight did not. Females that gave birth the following year began the winter foraging period with significantly longer and deeper dives, as compared to non‐reproductive seals. Mid‐ to late winter, reproductive females spent a significantly greater proportion of the day diving, and either depressed their diving metabolic rates (DMR), or exceeded their calculated aerobic dive limit (cADL) more frequently than females that returned without a pup. Moreover, non‐reproductive females organized their dives into 2–3 short bouts per day on average (BOUTshort; 7.06 ± 1.29 hr; mean ± 95% CI), whereas reproductive females made 1–2 BOUTshort per day (10.9 ± 2.84 hr), comprising one long daily foraging bout without rest. The magnitude of the increase in dive activity budgets and depression in calculated DMR closely matched the estimated energetic requirements of supporting a fetus. This study is one of the first to identify increases in foraging effort that are associated with successful reproduction in a top predator and indicates that reproductive females must operate closer to their physiological limits to support gestational costs.We are grateful for the help of field team members: Drs. Luis Hückstädt, Linnea Pearson, and Patrick Robinson for sample collection. Group B‐009‐M led by Drs. Robert Garrott, Jay Rotella, and Thierry Chambert provided information regarding animal reproductive status and provided great assistance in locating study animals. Logistical support was provided by the National Science Foundation (NSF) U.S. Antarctic Program, Raytheon Polar Services, and Lockheed Martin ASC; we thank all the support staff in Christchurch, NZ and McMurdo Station. This research was conducted with support from NSF ANT‐0838892 to D.P.C. and ANT‐0838937 to J.M.B. For J.M.B., this material is based upon work while serving at the National Science Foundation, and M.R.S was supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE‐1242789. Any opinion, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. Animal handling protocols were approved by the University of Alaska Anchorage and University of California Santa Cruz's Institutional Animal Care and Use Committees. Research and sample import to the United States were authorized under the Marine Mammal permit No. 87‐1851‐04 issued by the Office of Protected Resources, National Marine Fisheries Service. Research activities were also approved through Antarctic Conservation Act permits while at McMurdo Station

Iron mobilization during lactation reduces oxygen stores in a diving mammal

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Shero, M. R., Kirkham, A. L., Costa, D. P., & Burns, J. M. Iron mobilization during lactation reduces oxygen stores in a diving mammal. Nature Communications, 13(1), (2022): 4322, https://doi.org/10.1038/s41467-022-31863-7.The profound impacts that maternal provisioning of finite energy resources has on offspring survival have been extensively studied across mammals. This study shows that in addition to calories, high hemoprotein concentrations in diving mammals necessitates exceptional female-to-pup iron transfer. Numerous indices of iron mobilization (ferritin, serum iron, total-iron-binding-capacity, transferrin saturation) were significantly elevated during lactation in adult female Weddell seals (Leptonychotes weddellii), but not in skip-breeders. Iron was mobilized from endogenous stores for incorporation into the Weddell seal’s milk at concentrations up to 100× higher than terrestrial mammals. Such high rates of iron offload to offspring drew from the female’s own heme stores and led to compromised physiologic dive capacities (hemoglobin, myoglobin, and total body oxygen stores) after weaning their pups, which was further reflected in shorter dive durations. We demonstrate that lactational iron transfer shapes physiologic dive thresholds, identifying a cost of reproduction to a marine mammal.This research was conducted with support from NSF ANT-0838892 to DPC; ANT-0838937 and ANT-1246463 to JMB (which also supported ALK and MRS); and The Investment in Science Fund at WHOI to MRS

Seasonal Habitat Preference and Foraging Behaviour of Post-Moult Weddell Seals in the Western Ross Sea

Weddell seals (Leptonychotes weddellii) are important predators in the Southern Ocean and are among the best-studied pinnipeds on Earth, yet much still needs to be learned about their year-round movements and foraging behaviour. Using biologgers, we tagged 62 post-moult Weddell seals in McMurdo Sound and vicinity between 2010 and 2012. Generalized additive mixed models were used to (i) explain and predict the probability of seal presence and foraging behaviour from eight environmental variables, and (ii) examine foraging behaviour in relation to dive metrics. Foraging probability was highest in winter and lowest in summer, and foraging occurred mostly in the water column or just above the bottom; across all seasons, seals preferentially exploited the shallow banks and deeper troughs of the Ross Sea, the latter providing a pathway for Circumpolar Deep Water to flow onto the shelf. In addition, the probability of Weddell seal occurrence and foraging increased with increasing bathymetric slope and where water depth was typically less than 600 m. Although the probability of occurrence was higher closer to the shelf break, foraging was higher in areas closer to shore and over banks. This study highlights the importance of overwinter foraging for recouping body mass lost during the previous summer

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

Adult Weddell seals (Leptonychotes weddellii) haul-out on the ice in October/November (austral spring) for the breeding season and reduce foraging activities for ~4 months until their molt in the austral fall (January/February). After these periods, animals are at their leanest and resume actively foraging for the austral winter. In mammals, decreased exercise and hypoxia exposure typically lead to decreased production of O2-carrying proteins and muscle wasting, while endurance training increases aerobic potential. To test whether similar effects were present in marine mammals, this study compared the physiology of 53 post-molt female Weddell seals in the austral fall to 47 pre-breeding females during the spring in McMurdo Sound, Antarctica. Once body mass and condition (lipid) were controlled for, there were no seasonal changes in total body oxygen (TBO2) stores. Within each season, hematocrit and hemoglobin values were negatively correlated with animal size, and larger animals had lower mass-specific TBO2 stores. But because larger seals had lower mass-specific metabolic rates, their calculated aerobic dive limit was similar to smaller seals. Indicators of muscular efficiency, myosin heavy chain composition, myoglobin concentrations, and aerobic enzyme activities (citrate synthase and β-hydroxyacyl CoA dehydrogenase) were likewise maintained across the year. The preservation of aerobic capacity is likely critical to foraging capabilities, so that following the molt Weddell seals can rapidly regain body mass at the start of winter foraging. In contrast, muscle lactate dehydrogenase activity, a marker of anaerobic metabolism, exhibited seasonal plasticity in this diving top predator and was lowest after the summer period of reduced activity

Non-invasive measurements of respiration and heart rate across wildlife species using Eulerian Video Magnification of infrared thermal imagery

Abstract Background An animal’s metabolic rate, or energetic expenditure, both impacts and is impacted by interactions with its environment. However, techniques for obtaining measurements of metabolic rate are invasive, logistically difficult, and costly. Red–green–blue (RGB) imaging tools have been used in humans and select domestic mammals to accurately measure heart and respiration rate, as proxies of metabolic rate. The purpose of this study was to investigate if infrared thermography (IRT) coupled with Eulerian video magnification (EVM) would extend the applicability of imaging tools towards measuring vital rates in exotic wildlife species with different physical attributes. Results We collected IRT and RGB video of 52 total species (39 mammalian, 7 avian, 6 reptilian) from 36 taxonomic families at zoological institutions and used EVM to amplify subtle changes in temperature associated with blood flow for respiration and heart rate measurements. IRT-derived respiration and heart rates were compared to ‘true’ measurements determined simultaneously by expansion of the ribcage/nostrils and stethoscope readings, respectively. Sufficient temporal signals were extracted for measures of respiration rate in 36 species (85% success in mammals; 50% success in birds; 100% success in reptiles) and heart rate in 24 species (67% success in mammals; 33% success in birds; 0% success in reptiles) using IRT-EVM. Infrared-derived measurements were obtained with high accuracy (respiration rate, mean absolute error: 1.9 breaths per minute, average percent error: 4.4%; heart rate, mean absolute error: 2.6 beats per minute, average percent error: 1.3%). Thick integument and animal movement most significantly hindered successful validation. Conclusion The combination of IRT with EVM analysis provides a non-invasive method to assess individual animal health in zoos, with great potential to monitor wildlife metabolic indices in situ