What happened to gray whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean

Abstract

Background: Gray whales (Eschrichtius robustus) undertake long migrations, from Baja California to Alaska, to feed on seasonally productive benthos of the Bering and Chukchi seas. The invertebrates that form their primary prey are restricted to shallow water environments, but global sea-level changes during the Pleistocene eliminated or reduced this critical habitat multiple times. Because the fossil record of gray whales is coincident with the onset of Northern Hemisphere glaciation, gray whales survived these massive changes to their feeding habitat, but it is unclear how.

Methodology/principal findings: We reconstructed gray whale carrying capacity fluctuations during the past 120,000 years by quantifying gray whale feeding habitat availability using bathymetric data for the North Pacific Ocean, constrained by their maximum diving depth. We calculated carrying capacity based on modern estimates of metabolic demand, prey availability, and feeding duration; we also constrained our estimates to reflect current population size and account for glaciated and non-glaciated areas in the North Pacific. Our results show that key feeding areas eliminated by sea-level lowstands were not replaced by commensurate areas. Our reconstructions show that such reductions affected carrying capacity, and harmonic means of these fluctuations do not differ dramatically from genetic estimates of carrying capacity.

Conclusions/significance: Assuming current carrying capacity estimates, Pleistocene glacial maxima may have created multiple, weak genetic bottlenecks, although the current temporal resolution of genetic datasets does not test for such signals. Our results do not, however, falsify molecular estimates of pre-whaling population size because those abundances would have been sufficient to survive the loss of major benthic feeding areas (i.e., the majority of the Bering Shelf) during glacial maxima. We propose that gray whales survived the disappearance of their primary feeding ground by employing generalist filter-feeding modes, similar to the resident gray whales found between northern Washington State and Vancouver Island.

Figure 1. Pliocene through Holocene eustatic sea-level changes, at two different scales.

Sea-level change juxtaposed with A) the oldest known fossil belonging to the genus Eschrichtius, from the Pliocene of Japan (dashed line) ; and B) the relative temporal ranges from other historical gray whale data, with the oldest example belonging to the species occurrence (solid line), from the Palos Verdes Peninsula of California , . Age for census estimates reflects an upper bound for reports from the written historical record , , , .

Figure 2. Benthos availability, sea-level change and coastal configuration of continental margins in the North Pacific Ocean, at select intervals, during the last 120 ka.

A) Geographic plates at the top of the figure depict reconstructed coastal configurations and 20 m depth contours for (a) present day, (b) 15 ka, (c) 45 ka, (d) 70 ka, (e) 100 ka, and (f), 120 ka. See Table 1 for regional boundaries and summary data; depth data from ETOPO1 . B) Left axis on the plot shows bar graphs with available benthos at 20 m increments at select time intervals (a–f). Right axis shows mean sea-level changes in past 130 ka, using data from Miller et al. . Dashed lines indicate (left, in orange) current sea-level and (right, in blue) current benthos availability.

Figure 3. Estimated carrying capacity for North Pacific gray whales determined by benthos availability (<75 m) during the last 120 ka.

Dashed gray lines indicate current gray whale population size and red lines show harmonic means for carrying capacity estimates. A) Total and regional North Pacific unconstrained carrying capacities. Gray box indicates range of population size suggested by analysis of genetic diversity . B) Total and regional North Pacific carrying capacities constrained to 22 k gray whales; see Table 2; C) Unconstrained, estimated carrying capacities of non-glaciated regions in the western and eastern Pacific; D) Estimated carry capacities of non-glaciated regions in the western and eastern Pacific constrained to 22 k gray whales; see Table 2.

Figure 4. Gray whales amidst ice in the eastern North Pacific Ocean.

Taken as anecdotal evidence, this illustration, reproduced from , provides insight into gray whale behavioral plasticity, especially in the presence of sea and pack ice. Several observations (e.g., [59]) suggest that gray whales possess a latent ability to tolerate ice, which would be a beneficial trait during episodes of glacial maxima.

Figure 5. Non-migratory gray whale feeding.

Photograph of a gray whale feeding on herring near Cape Scott, Vancouver Island, British Columbia, 17 April 2000. Photograph and observations by the late Donovan Girard, courtesy of K. Lihou and R. Graham.