Estimating reproductive costs in marine mammal bioenergetic models : a review of current knowledge and data availability

This review was funded by the Office of Naval Research (N000142012392), with support from the Marine Mammal Commission (MMC 19-173).Reproductive costs represent a significant proportion of a mammalian female's energy budget. Estimates of reproductive costs are needed for understanding how alterations to energy budgets, such as those from environmental variation or human activities, impact maternal body condition, vital rates and population dynamics. Such questions are increasingly important for marine mammals, as many populations are faced with rapidly changing and increasingly disturbed environments. Here we review the different energetic costs that marine mammals incur during gestation and lactation and how those costs are typically estimated in bioenergetic models. We compiled data availability on key model parameters for each species across all six marine mammal taxonomic groups (mysticetes, odontocetes, pinnipeds, sirenians, mustelids and ursids). Pinnipeds were the best-represented group regarding data availability, including estimates of milk intake, milk composition, lactation duration, birth mass, body composition at birth and growth. There were still considerable data gaps, particularly for polar species, and good data were only available across all parameters in 45\poor, with some species having little or no data for any parameters, particularly beaked whales. Even for species with moderate data coverage, many parameter estimates were tentative or based on indirect approaches, necessitating reevaluation of these estimates. We discuss mechanisms and factors that affect maternal energy investment or prey requirements during reproduction, such as prey supplementation by offspring, metabolic compensation, environmental conditions and maternal characteristics. Filling the existing data gaps highlighted in this review, particularly for parameters that are influential on bioenergetic model outputs, will help refine reproductive costs estimated from bioenergetic models and better address how and when energy imbalances are likely to affect marine mammal populations.Publisher PDFPeer reviewe

Vulnerability to fluctuations in prey and predation landscape in a central place foraging marine predator

IntroductionHuman-induced environmental change is driving a global redistribution of biodiversity, resulting in shifting prey and predation landscapes. These shifting landscapes can lead to changes in behavior, health, and vital rates, with potential implications for population dynamics.MethodsIn the present study, a state-dependent life-history theory model was developed to investigate the individual- and population-level responses of Australian fur seals (Arctocephalus pusillus doriferus) to changes in prey availability and at-sea mortality risk.ResultsRates of pregnancy, pup nursing, and abortion were unaffected by prey availability in the simulated population. Likewise, on-land and at-sea durations were largely unaffected by prey availability, with more pronounced affects for nonreproductive and pregnant females than for lactating females. There was a strong influence of prey availability on the proportion of females that were concurrently pregnant and lactating, largely due to an increase in pup abandonments under low prey availability scenarios. This effect on pup abandonments also had flow on effects for pup recruitment. Increasing at-sea mortality risk resulted in greater offspring losses due to maternal death. The combined impact of prey availability and at-sea mortality risk on the number of simulated female offspring reaching sexual maturity was substantial.DiscussionConsequently, our results suggest high vulnerability of the Australian fur seal population to shifting prey and predation landscapes. These results indicate a need for continued monitoring of Australian fur seal pup production and population dynamics in the face of rapid environmental change

Growth in marine mammals : a review of growth patterns, composition and energy investment

Funded under award from Office of Naval Research: N000142012392. DPC and SA were funded under the E&P Sound and Marine Life Joint Industry Programme of the International Association of Oil and Gas Producers (IOGP; grant 00-07-23). CRM is supported by the Australian Integrated Marine Observing System (IMOS), IMOS s enabled by the National Collaborative Research Infrastructure Strategy.Growth of structural mass and energy reserves influences individual survival, reproductive success, population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1–74.3%) and blubber (0.4–97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities and to improve our understanding of how marine mammals grow and the associated energetic costs.Publisher PDFPeer reviewe

Key questions in marine mammal bioenergetics

This work was funded by the Marine Mammal Commission (MMC19-173). The Office of Naval Research funded the bioenergetic workshop (N000142012392) that provided support for this work.Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as ‘key’ questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.Publisher PDFPeer reviewe

Convergence of marine megafauna movement patterns in coastal and open oceans

Author Posting. © The Author(s), 2017. This is the author's version of the work. It is posted here for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 115 (2018): 3072-3077, doi:10.1073/pnas.1716137115.The extent of increasing anthropogenic impacts on large marine vertebrates partly depends on the animals’ movement patterns. Effective conservation requires identification of the key drivers of movement including intrinsic properties and extrinsic constraints associated with the dynamic nature of the environments the animals inhabit. However, the relative importance of intrinsic versus extrinsic factors remains elusive. We analyse a global dataset of 2.8 million locations from > 2,600 tracked individuals across 50 marine vertebrates evolutionarily separated by millions of years and using different locomotion modes (fly, swim, walk/paddle). Strikingly, movement patterns show a remarkable convergence, being strongly conserved across species and independent of body length and mass, despite these traits ranging over 10 orders of magnitude among the species studied. This represents a fundamental difference between marine and terrestrial vertebrates not previously identified, likely linked to the reduced costs of locomotion in water. Movement patterns were primarily explained by the interaction between species-specific traits and the habitat(s) they move through, resulting in complex movement patterns when moving close to coasts compared to more predictable patterns when moving in open oceans. This distinct difference may be associated with greater complexity within coastal micro-habitats, highlighting a critical role of preferred habitat in shaping marine vertebrate global movements. Efforts to develop understanding of the characteristics of vertebrate movement should consider the habitat(s) through which they move to identify how movement patterns will alter with forecasted severe ocean changes, such as reduced Arctic sea ice cover, sea level rise and declining oxygen content.Workshops funding granted by the UWA Oceans Institute, AIMS, and KAUST. AMMS was supported by an ARC Grant DE170100841 and an IOMRC (UWA, AIMS, CSIRO) fellowship; JPR by MEDC (FPU program, Spain); DWS by UK NERC and Save Our Seas Foundation; NQ by FCT (Portugal); MMCM by a CAPES fellowship (Ministry of Education)

Estimating reproductive costs in marine mammal bioenergetic models:a review of current knowledge and data availability

Reproductive costs represent a significant proportion of a mammalian female's energy budget. Estimates of reproductive costs are needed for understanding how alterations to energy budgets, such as those from environmental variation or human activities, impact maternal body condition, vital rates and population dynamics. Such questions are increasingly important for marine mammals, as many populations are faced with rapidly changing and increasingly disturbed environments. Here we review the different energetic costs that marine mammals incur during gestation and lactation and how those costs are typically estimated in bioenergetic models. We compiled data availability on key model parameters for each species across all six marine mammal taxonomic groups (mysticetes, odontocetes, pinnipeds, sirenians, mustelids and ursids). Pinnipeds were the best-represented group regarding data availability, including estimates of milk intake, milk composition, lactation duration, birth mass, body composition at birth and growth. There were still considerable data gaps, particularly for polar species, and good data were only available across all parameters in 45% of pinniped species. Cetaceans and sirenians were comparatively data-poor, with some species having little or no data for any parameters, particularly beaked whales. Even for species with moderate data coverage, many parameter estimates were tentative or based on indirect approaches, necessitating reevaluation of these estimates. We discuss mechanisms and factors that affect maternal energy investment or prey requirements during reproduction, such as prey supplementation by offspring, metabolic compensation, environmental conditions and maternal characteristics. Filling the existing data gaps highlighted in this review, particularly for parameters that are influential on bioenergetic model outputs, will help refine reproductive costs estimated from bioenergetic models and better address how and when energy imbalances are likely to affect marine mammal populations

Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species

RationaleMixing models are a common method for quantifying the contribution of prey sources to the diet of an individual using stable isotope analysis; however, these models rely upon a known trophic discrimination factor (hereafter, TDF) that results from fractionation between prey and animal tissues. Quantifying TDFs in captive animals is ideal, because diet is controlled and the proportional contributions and isotopic values of all prey items are known.MethodsTo calculate TDFs for the Hawaiian monk seal, northern elephant seal, bearded seal, ringed seal, spotted seal, harbor seal, and California sea lion, we obtained whiskers, serum, plasma, red blood cells, and prey items from nine captive individuals. We obtained δ(13) C and δ(15) N values using continuous-flow isotope-ratio mass spectrometry. The average δ(13) C and δ(15) N values from bulk and lipid-corrected prey from the diet were subtracted from the δ(13) C and δ(15) N values of each blood and whisker sample to calculate tissue-specific TDFs for each individual (∆(13) C or ∆(15) N).ResultsThe ∆(13) C values ranged from +1.7 to +3.2‰ (bulk prey) and from +0.8 to +1.9‰ (lipid-corrected prey) for the various blood components, and from +3.9 to +4.6‰ (bulk prey) or +2.6 to +3.9‰ (lipid-corrected prey) for whiskers. The ∆(15) N values ranged from +2.2 to +4.3‰ for blood components and from +2.6 to +4.0‰ for whiskers. The TDFs tended to group by tissue, with whiskers having greater ∆(13) C values than blood components. In contrast, the ∆(15) N values were greater in serum and plasma than in red blood cells and whiskers.ConclusionsBy providing the first TDF values for five seal species (family Phocidae) and one otariid species (family Otariidae), our study facilitates more accurate mixing models for these species. These values are particularly important for critically endangered Hawaiian monk seals and the three Arctic seal species (bearded, ringed, and spotted) that are faced with a rapidly changing environment

Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species.

RationaleMixing models are a common method for quantifying the contribution of prey sources to the diet of an individual using stable isotope analysis; however, these models rely upon a known trophic discrimination factor (hereafter, TDF) that results from fractionation between prey and animal tissues. Quantifying TDFs in captive animals is ideal, because diet is controlled and the proportional contributions and isotopic values of all prey items are known.MethodsTo calculate TDFs for the Hawaiian monk seal, northern elephant seal, bearded seal, ringed seal, spotted seal, harbor seal, and California sea lion, we obtained whiskers, serum, plasma, red blood cells, and prey items from nine captive individuals. We obtained δ(13) C and δ(15) N values using continuous-flow isotope-ratio mass spectrometry. The average δ(13) C and δ(15) N values from bulk and lipid-corrected prey from the diet were subtracted from the δ(13) C and δ(15) N values of each blood and whisker sample to calculate tissue-specific TDFs for each individual (∆(13) C or ∆(15) N).ResultsThe ∆(13) C values ranged from +1.7 to +3.2‰ (bulk prey) and from +0.8 to +1.9‰ (lipid-corrected prey) for the various blood components, and from +3.9 to +4.6‰ (bulk prey) or +2.6 to +3.9‰ (lipid-corrected prey) for whiskers. The ∆(15) N values ranged from +2.2 to +4.3‰ for blood components and from +2.6 to +4.0‰ for whiskers. The TDFs tended to group by tissue, with whiskers having greater ∆(13) C values than blood components. In contrast, the ∆(15) N values were greater in serum and plasma than in red blood cells and whiskers.ConclusionsBy providing the first TDF values for five seal species (family Phocidae) and one otariid species (family Otariidae), our study facilitates more accurate mixing models for these species. These values are particularly important for critically endangered Hawaiian monk seals and the three Arctic seal species (bearded, ringed, and spotted) that are faced with a rapidly changing environment