Benthic studies adjacent to Sakhalin Island, Russia 2015 III: benthic energy density spatial models in the nearshore gray whale feeding area.

Energy densities of six dominant benthic groups (Actinopterygii, Amphipoda, Bivalvia, Cumacea, Isopoda, and Polychaeta) and total prey energy were modeled for the nearshore western gray whale feeding area, Sakhalin Island, Russia, as part of a multi-disciplinary research program in the summer of 2015. Energy was modeled using generalized additive mixed models (GAMM) with accommodations for zero-inflation (logistic regression and hurdle models) and regression predictions combined with kriging to interpolate energy densities across the nearshore feeding area. Amphipoda energy density was the highest nearshore and in the south whereas Bivalvia energy density was the highest offshore and in the northern portion of the study area. Total energy was the highest in mid-range distances from shore and in the north. Amphipoda energy density was higher than minimum energy estimates defining gray whale feeding habitats (312-442 kJ/m2) in 13% of the nearshore feeding area whereas total prey energy density was higher than the minimum energy requirement in 49% of the habitat. Inverse distance-weighted interpolations of Amphipoda energy provided a broader scale representation of the data whereas kriging estimates were spatially limited but more representative of higher density in the southern portion of the study area. Both methods represented the general trend of higher Amphipoda energy density nearshore but with significant differences that highlight the value of using multiple methods to model patterns in highly complex environments.

Benthic studies adjacent to Sakhalin Island, Russia, 2015 II: energy content of the zoobenthos in western gray whale feeding grounds.

The waters adjacent to the northeastern coast of Sakhalin Island, Russia, are an important feeding ground for the endangered western gray whale. Data on the energy available to foraging whales from their prey resources is required for researchers interested in modeling the bioenergetics of whale foraging, but little energy content information is available for the benthic prey communities of gray whales in this region. In this study, we describe the energy density (ED), biomass, and total energy availability (ED × biomass) of benthic prey sampled from two gray whale foraging areas adjacent to Sakhalin Island: the nearshore and offshore feeding areas. ED varied almost seven-fold among benthic taxa, ranging from 1.11 to 7.62 kJ/g wet mass. Although there was considerable variation within most prey groups, amphipods had the highest mean ED of all of groups examined (5.58 ± 1.44 kJ/g wet mass). Small sample sizes precluded us from detecting any seasonal or spatial differences in mean ED within or among taxa; however, mean biomass in the offshore feeding area was, in some cases, an order of magnitude higher than mean estimates in the nearshore feeding area, resulting in higher mean total energy available to foraging gray whales offshore (958-3313 kJ/m2) compared to nearshore (223-495 kJ/m2). While the proportion of total energy accounted for by amphipods was variable, this prey group generally made up a higher proportion of the total energy available in the benthos of the offshore feeding area than in the benthos of the nearshore feeding area. Data presented here will be used to inform bioenergetics modeling of the vital rates of mature females in an effort to improve understanding of population growth limits for western gray whales.

Benthic studies adjacent to Sakhalin Island, Russia, 2015 I: benthic biomass and community structure in the nearshore gray whale feeding area.

Okhotsk or western gray whales feed in summer along the northeastern coast of Sakhalin Island, Russia, a region with oil and gas extraction facilities. Seismic surveys increased sound levels in the nearshore feeding area in 2015 for part of the summer, potentially displacing whales from preferred foraging habitat or reducing foraging efficiency. Since lost foraging opportunities might lead to vital rate effects on this endangered species, detailed benthic surveys were conducted to characterize benthic community biomass patterns and spatial and temporal differences. Benthic biomass demonstrated strong spatial-temporal interactions indicating that prey biomass differences among locations were dependent on sampling period. Of greatest interest, Amphipoda biomass declined from June to October in the northern and southern portions of the nearshore study area but increased in the middle and Actinopterygii biomass increased in the northern area in mid-summer. Water depth and sediment type were significant covariates with community structure, and water depth strongly covaried with bivalve biomass. Total average prey biomass was ~ 100 g/m2 within the nearshore feeding area with no evidence of reduced biomass among sampling periods or locations, although there were fewer amphipods in the south. Multi-prey investigations provide a stronger basis for inferences than single-prey studies of amphipods when gray whales feed on diverse prey. Benthic community-level variability was moderate to high as would be expected for a shallow-water nearshore area. Overall, spatial and temporal changes in dominant macrofauna biomass reflected small to medium-sized effects that were well within the natural boundaries expected for benthic communities.

First observations of ovary regeneration in an amphipod, Ampelisca eschrichtii Krøyer, 1842.

Background: Females of the gammaridean amphipod Ampelisca eschrichtii with signs of regenerating, previously atrophied ovaries were recovered from the northeastern shelf of Sakhalin Island (Okhotsk Sea, Russia). Ovarian regeneration was previously unknown for any amphipod species. A. eschrichtii have a predominantly 2-year life cycle (from embryo to adult death) and reproduce once between late winter or early spring at the age of 2 years. Occasionally, females survive to a third year. An adaptive value of extended survival among these females is likely to require that they are also reproductive. Methods: Histological sections from a second-year female with ovarian atrophy, a female with normal ovaries, a third-year female with ovarian regeneration, as well as testes of an immature and a sexually mature male were compared to determine the sources of cells of the germinal and somatic lines necessary for ovarian regeneration. Results: Ovarian regeneration in the third-year female began with the formation of a new germinal zone from germ cells preserved in the atrophied ovaries and eosinophilic cells of the previously starving second-year female. Eosinophilic cells form the mesodermal component of the germinal zone. A mass of these cells appeared in the second-year female that had atrophied ovaries and in large numbers on the intestine wall of the third-year female with regenerating ovaries. These eosinophilic cells appear to migrate into the regenerating ovaries. Conclusions: All germ cells of the second-year female are not lost during ovarian atrophy and can be involved in subsequent ovarian regeneration. Eosinophilic cells involved in ovarian regeneration are of mesodermal origin. The eosinophilic cell morphologies are similar to those of quiescence cells (cells in a reversible state that do not divide but retain the ability to re-enter cell division and participate in regeneration). These histological data thus indicate that eosinophilic and germ cells of third-year females can participate in the regeneration of the ovaries to reproduce a second brood. The precursors of these third-year females (a small number the second-year females with an asynchronous [summer] breeding period and ovaries that have atrophied due to seasonal starvation) appear to possess sources of somatic and germ cells that are sufficient for ovarian regeneration and that may be adaptations to starvation stress.

Trophic basis of dominant amphipods in the gray whale feeding grounds near northeastern Sakhalin Island (the Sea of Okhotsk) inferred from fatty acid and stable isotope analyses.

The shelf waters off northeastern Sakhalin Island are the main feeding ground for the endangered western subpopulation of the gray whale Eschrichtius robustus. Amphipods, which dominate the benthic communities, are key dietary sources for the gray whales foraging in this area. To elucidate the trophic base supporting the large local amphipod biomass, fatty acid (FA) compositions and the stable isotope ratios δ13C and δ15N of the five most abundant amphipod species in the area were studied. The FA compositions were unusually similar (85% similarity) across the amphipod species although these species were represented by suspension-feeders, deposit-feeders and carnivores. The FAs of diatom origin predominated in the FA profiles of all amphipods and decreased in accordance with the increase in trophic position as determined by δ15N values and the FA trophic markers of carnivorous feeding. These results suggested that diatoms are the single, main trophic basis that underpins the food web of the feeding grounds on the northeastern Sakhalin shelf. Further studies on factors influencing the local production of large diatoms on the Sakhalin shelf can be important for the prognosis of future changes of foraging resources of the gray whales.

Prey biomass dynamics in gray whale feeding areas adjacent to northeastern Sakhalin (the Sea of Okhotsk), Russia, 2001-2015.

Changing climate patterns strongly influence marine ecosystems across the Pacific Arctic region creating significant ecosystem transitions and change. Macrobenthic species are essential prey for numerous marine mammals and seabirds but the influence of climatic drivers that control macrobenthic community population dynamics are poorly known in critical prey habitats. We investigated associations of environmental, temporal, and climatic covariates with the biomass concentrations of six prey groups (Actinopterygii, Amphipoda, Bivalvia, Cumacea, Isopoda, and Polychaeta) in essential habitats for Korean-Okhotsk (western) gray whales adjacent to northeastern Sakhalin Island in the Sea of Okhotsk. Prey community biomass concentrations were correlated with water depth, year, and climate indices reflecting oceanographic and climatic patterns associated with macro-scale climatological effects. The correlation of prey biomass with water depth and year accounted for ∼90% of total variation in canonical correlation analyses (CCor). Climate indices accounted for ∼10% of total variation in CCor. Water circulation in winter may be particularly important for maintaining populations through the advection of particulate organic carbon entrained in winter currents. Overall, temporal trends in the biomass concentrations of gray whale prey resources appear to reflect climatic and oceanographic factors that are driving ecosystem changes across the Sea of Okhotsk and the Pacific Arctic region.

Ampelisca eschrichtii Krøyer, 1842 (Ampeliscidae) of the Sakhalin Shelf in the Okhotsk Sea starve in summer and feast in winter.

BACKGROUND: Ampelisca eschrichtii Krøyer, 1842 of the Sakhalin Shelf of the Okhotsk Sea, Far Eastern Russia, comprise the highest known biomass concentration of any amphipod population in the world and are a critically important prey source for western gray whales. Growth and reproduction in this population has not been apparent in summer. However, they are not accessible for sampling in winter to test a previous default conclusion that they grow and reproduce in winter. METHODS: We tested the default winter growth and reproduction hypothesis by detailed comparisons of the brood and gonad development among 40 females and 14 males and brood sizes among females observed since 2002. Our test included six predictions of reproductive synchrony that would be apparent from gonad and brood morphology if active reproduction occurs in summer. RESULTS: We found high prevalences of undersized and damaged oocytes, undersized broods, a lack of females brooding fully formed juveniles, atrophied ovaries, and males with mature sperm but lacking fully developed secondary sex morphologies required for pelagic mating. All of these conditions are consistent with trophic stress and starvation. DISCUSSION: These A. eschrichtii populations therefore appear to starve in summer and to grow and reproduce in winter. The Offshore A. eschrichtii populations occur in summer below water strata bearing high phytoplankton biomasses. These populations are more likely to feed successfully in winter when storms mix phytoplankton to their depths.

Life History and Production of the Western Gray Whale's Prey, Ampelisca eschrichtii Krøyer, 1842 (Amphipoda, Ampeliscidae).

Ampelisca eschrichtii are among the most important prey of the Western North Pacific gray whales, Eschrichtius robustus. The largest and densest known populations of this amphipod occur in the gray whale's Offshore feeding area on the Northeastern Sakhalin Island Shelf. The remote location, ice cover and stormy weather at the Offshore area have prevented winter sampling. The incomplete annual sampling has confounded efforts to resolve life history and production of A. eschrichtii. Expanded comparisons of population size structure and individual reproductive development between late spring and early fall over six sampling years between 2002 and 2013 however, reveal that A. eschrichtii are gonochoristic, iteroparous, mature at body lengths greater than 15 mm and have a two-year life span. The low frequencies of brooding females, the lack of early stage juveniles, the lack of individual or population growth or biomass increases over late spring and summer, all indicate that growth and reproduction occur primarily in winter, when sampling does not occur. Distinct juvenile and adult size cohorts additionally indicate growth and juvenile production occurs in winter through spring under ice cover. Winter growth thus requires that winter detritus or primary production are critical food sources for these ampeliscid populations and yet, the Offshore area and the Eastern Sakhalin Shelf ampeliscid communities may be the most abundant and productive amphipod population in the world. These A. eschrichtii populations are unlikely to be limited by western gray whale predation. Whether benthic community structure can limit access and foraging success of western gray whales is unclear.