Reproductive potential of red king crab (Paralithodes camtschaticus) across warm and cold stanzas in Bristol Bay in southwestern Alaska: Supplementary Figure

The Bristol Bay, Alaska, fishery for red king crab Paralithodes camtschaticus is a male-only fishery. A safeguard against male overfishing is the requirement that at least 8.4 million successfully mated, newly fertilized females be present on the grounds each year; otherwise no harvest is permitted. Estimation of the number of mated females in the population is complicated by the timing of the Bering Sea trawl survey, which in most years moves through Bristol Bay before red king crab spawning is complete. From 1977 through 2000, an average of 22% (range, 0–87%) of the broodstock remained unmated at the time of the May–June survey. Eighty-nine percent of the observed annual variation in the proportion of unmated crabs was explained by water temperature and the date of the survey. Thus, the degree of mating success shown by each year's survey, although influenced by male availability, is predominantly an artifact of temperature and survey timing. Also, red king crabs tend to spawn in untrawlable nearshore waters, increasing the difficulty of obtaining unbiased estimates of abundance from sampling an open population. Because the proportion of mature females that emigrate each year to the nearshore spawning grounds is greater than that of males, the sex ratio within the sampled region of a survey conducted during spawning is biased toward males. This bias masks one of the more obvious signs of male overharvest—a male-depauperate sex ratio. Finally, a survey conducted during spawning cannot provide an accurate mapping of the spatial distribution of the postspawning broodstock returning from inshore spawning grounds to incubate their newly fertilized eggs during the next 10–12 months. A time–temperature model indicated that delaying the Bristol Bay red king crab survey until the end of June would ameliorate the problems caused by sampling an open population engaged in spawning.

The 1976 U.S. Magnuson‐Stevens Fishery Conservation and Management Act effectively eliminated the no‐trawl zone known as the Bristol Bay Pot Sanctuary, located in the southeastern Bering Sea, Alaska. Implemented by the Japanese in 1959, the boundaries of the Pot Sanctuary closely matched the well‐defined distribution of the red king crab (Paralithodes camtschaticus) population's mature‐female brood stock, thus affording a measure of protection to the reproductive potential of the stock. In 1980, the point at which the commercial harvest of Bristol Bay legal‐male red king crab reached an all‐time high after a decade‐long increase, domestic bottom trawling in the brood‐stock sanctuary began in earnest with the advent of a U.S.–Soviet, joint‐venture, yellowfin sole fishery. In the first year of trawling in the Pot Sanctuary, the Bering Sea/Aleutian Islands (BSAI) red king crab bycatch increased by 371% over the 1977–1979 average; in 1981 the BSAI bycatch increased another 235% over that in 1980, most of which were mature females. As the number of unmonitored domestic trawls in the brood‐stock area increased rapidly after 1979 and anecdotal reports of “red bags” (trawl cod‐ends plugged with red king crab) began to circulate, the proportion of males in the mature population (0.25 in 1981 and 0.16 in 1982) jumped to 0.54 in 1985 and 0.65 in 1986. It is unlikely that normal demographics caused this sudden reversal in sex ratio. Our hypothesis is that sequential, sex‐specific sources of fishing mortality were at work. Initially there were ten years (1970–1980) of increasing, male‐only exploitation in the directed pot fishery, followed by a drastic reduction in the male harvest after 1980 (to zero in 1983). Then, beginning around 1980, there was an increase in bottom trawling among the highly aggregated, sexually mature female brood stock concentrated near the western end of the Alaska Peninsula, an area documented by previous investigators to be the most productive spawning, incubation, and hatching ground for Bristol Bay red king crab. There has been considerable discussion about possible natural causes (e.g., meteorological regime shifts, increased groundfish predation, epizootic diseases) of the abrupt collapse of the Bristol Bay red king crab population in the early 1980s. The purpose of our study was to conduct a rigorous examination of existing data in order to evaluate the relative likelihood that the collapse was caused by human fishing instead of natural mortality. Our discussion focuses on the association between record harvests of male crab in the directed fishery, the onset of large‐scale commercial trawling within the population's primary reproductive refuge, and the population's collapse.

Evaluating the impact of ocean acidification on fishery yields and profits: The example of red king crab in Bristol Bay

Reproductive potential of red king crab (Paralithodes camtschaticus) across warm and cold stanzas in Bristol Bay in southwestern Alaska: Supplementary Table

Reproductive potential of red king crab (Paralithodes camtschaticus) across warm and cold stanzas in Bristol Bay in southwestern Alaska

Stock assessment of Alaskan red king crab, Paralithodes camtschaticus (Tilesius, 1815), can be improved by incorporating reproductive output, which requires an understanding of maternal size effects on embryo and larval quality. In June 2009 and 2010, we collected clutches of recently extruded red king crab embryos in Bristol Bay, Alaska, to assess embryo quality based on dry weight, carbon and nitrogen content. To assess larval quality, we collected ovigerous females from Bristol Bay in 2007 and reared them in the laboratory until larval hatching in 2008. Larval quality based on dry weight, carbon and nitrogen content, and times to 50% mortality under starvation conditions were assessed. All samples were collected in years that were colder than the 15-year average in the eastern Bering Sea. Among the measures of embryo quality, only nitrogen content was significantly different, increasing with maternal size. Carbon and nitrogen content were significantly higher for embryos in 2009 than in 2010, suggesting inter-annual differences in maternal investment. No effect of maternal size with larval quality was found. Our results indicate that maternal size does not have a biologically significant effect on embryo and larval quality in colder-than-average years, and therefore maternal size effects on embryo and larval quality does not need to be explicitly incorporated into reproductive output estimates in stock assessments under these conditions. We are, however, cautious to extrapolate our results to years with different environmental conditions. Further study is needed to fully resolve the possible interaction of environment with maternal size effects on embryo and larval quality for red king crab.

Red king crab, Paralithodes camtschaticus Tilesius, 1815, an economically and culturally important species in the state of Alaska, experienced drastic reductions in abundance over large portions of their Alaskan range by 1980. Abundance of crabs in some of the most important historical fishing areas have failed to rebound, some even in the absence of fishing, highlighting the need for additional research to infer genetic structure and reproductive biology of the species that can then be used to inform management efforts. Red king crab samples were collected from eleven locations throughout Alaska ( n = 845 ), of these, six locations were sampled at least one generation apart. Results of this study suggest moderate rates of gene flow within the Gulf of Alaska/Western Alaska region. Levels of genetic differentiation among populations within Southeast Alaska were higher than seen elsewhere, and there was strong evidence of multiple distinct populations. Red king crab in Bristol Bay and in two areas in Southeast Alaska show signs of recent population bottlenecks and shifts in allele frequencies not observed in previous studies that used less polymorphic genetic markers. In addition to population genetic structure analyses, 24 female red king crab and their broods were collected for purposes of inferring mating system. There was no evidence of multiple paternity in any brood. The results of this study support continued management of distinct geographic groups within the Gulf of Alaska/Western Alaska region and suggest that finer-scale management may be beneficial in Southeast Alaska.

Intra-guild predation among early benthic phase red and blue king crabs: Evidence for a habitat-mediated competitive advantage

Parasitism of the blue king crab, Paralithodes platypus, by the rhizocephalan, Briarosaccus callosus

Effects of diet, stocking density, and substrate on survival and growth of hatchery-cultured red king crab ( Paralithodes camtschaticus) juveniles in Alaska, USA

Distribution and abundance of ovigerous female red king crabs (Paralithodes camtschaticus) in the southeast Bering Sea from 1975 to 2001 were investigated using data collected during National Marine Fisheries Service annual trawl surveys. Peak abundance of ∼140 million crabs was observed in 1978, and declined rapidly to a low of just over 6 million in 1986. Abundance fluctuated from ∼6 to 22 million from the late 1980s through 2001, with a single strong recruitment event that resulted in ∼35 million ovigerous females observed in 1998. Changes in abundance were accompanied by changes in distribution. During the late 1970s the population was typified by high abundance to the southwest, along the northern shore of Unimak Island and the Alaska Peninsula. By the mid‐1980s the population's average center of abundance shifted substantially to the northeast and was found in central Bristol Bay. The distribution remained similar throughout the 1990s. Changes in distribution during the late 1970s and early 1980s coincided with changes in early summer near‐bottom temperature. The 1970s were typified by a pool of very cold water (<1°C) within central Bristol Bay. This retreated in ∼1978, and was not observed in consecutive summers during the remainder of the time series. The northeastward shift in the population, measured as the distance between Unimak Pass and the average center of abundance, showed a negative correlation with the geographic extent the cold‐pool. Abundance calculated for smaller spatial strata indicate that changes in distribution were not simply the result of relative abundance phenomena or solely generated by mortality in southwestern Bristol Bay, but also reflected regional increases in absolute abundance. Total broodstock abundance declined after 1978, but abundance in the western and northern areas of the region increased until at least 1982. The fact that distribution patterns change over time may have implications for population dynamics and fishery management. Changes in spatial population structure may affect recruitment patterns via changes in larval dynamics, and management might benefit if the causes of geographic displacement can be identified and predicted.

Habitat, predation, growth, and coexistence: Could interactions between juvenile red and blue king crabs limit blue king crab productivity?

Simple SummaryNew biodiversity records are important for expanding our knowledge about the symbiotic associations of the commercially important red king crab. This species was introduced into the Barents Sea, and now its population supports a viable fishery in the area. There are only a few reports regarding epibiotic relationships between echinoderms and marine crabs in general and the red king crab in particular. In our paper, we provide new data on the occurrence of the common starfish, Atlantic sea cucumber, green sea urchin, and brittle star on the invasive red king crab in the Barents Sea. The associations between echinoderms and red king crabs could have important ecological implications and provides an interesting example of how a prey species can avoid death by infesting its predator.During diving surveys for a Russian research project that monitored introduced species, red king crabs (Paralithodes camtschaticus) were collected at a coastal site of the Barents Sea to study the structure and dynamics of this species. Sampling of the organisms colonizing the crabs was part of this research project. For the first time, the presence of relatively large specimens of the common starfish Asterias rubens as epibionts of P. camtschaticus was observed in July 2010, 2018, and 2019. In 2010 and 2019, we also found three other echinoderm species (the Atlantic sea cucumber Cucumaria frondosa, the green sea urchin Strongylocentrotus droebachiensis, and the brittle star Ophiura sarsii). These findings add to the current list of associated species on king crabs not only in the Barents Sea but also in native areas of this host. Red king crabs have been documented as predators for these echinoderm species, and our records show additional possible interactions between king crabs and echinoderms in this region. More likely, the epibiotic lifestyle allows these echinoderms to avoid predation from red king crabs. There are no potential disadvantages derived by red king crabs through their relationships with the echinoderm epibionts due to low occurrences of these associations. We suggest no negative effects for the local red king crab population and populations of other commercial species in the Barents Sea.

Recruitment variability is poorly understood for Bering Sea crab stocks. The nearshore area in southwest Bristol Bay (Alaska, USA) is hypothesized as having historically (i.e., prior to ~ 1980) been the most important spawning ground for Bristol Bay red king crab (Paralithodes camtschaticus) because post‐larvae are thought to have been most likely to reach optimal settlement habitat along the Alaska Peninsula when hatched from this area as part of an endless‐belt reproductive strategy. We coupled a biophysical and oceanographic circulation model to test this hypothesis, investigate larval connectivity of more recent female spatial distributions, and evaluate the importance of climate variability on larval advection trajectories. Predicted settlement success varied through changes in larval pelagic duration and oceanographic circulation patterns: Shorter advective distance was associated with warmer conditions, causing higher rates of local retention relative to cold conditions. Contrary to earlier models, most larvae hatched in southwest Bristol Bay were advected offshore away from good habitat, whereas larvae hatched in central and nearshore Bristol Bay were retained in or advected to good habitat along the Alaska Peninsula. Our results suggest contemporary spatial distributions can supply settlement‐competent larvae to nurseries along the Alaska Peninsula and that under certain conditions, larvae may reach the Pribilof Islands when hatched from southwest Bristol Bay. Our study informs the role of environmental variability on larval transport and provides context within which to structure future investigations of recruitment mechanisms.

Punt, A. E., Siddeek, M. S. M., Garber-Yonts, B., Dalton, M., Rugolo, L., Stram, D., Turnock, B. J., and Zheng, J. 2012. Evaluating the impact of buffers to account for scientific uncertainty when setting TACs: application to red king crab in Bristol Bay, Alaska. – ICES Journal of Marine Science, 69: 624–634. Increasingly, scientific uncertainty is being accounted for in fisheries management by implementing an uncertainty buffer, i.e. a difference between the limit catch level given perfect information and the set catch. An approach based on simulation is outlined, which can be used to evaluate the impact of different buffers on short- and long-term catches, discounted revenue, the probability of overfishing (i.e. the catch exceeding the true, but unknown, limit catch), and the stock becoming overfished (i.e. for crab, mature male biomass, MMB, dropping below one-half of the MMB corresponding to maximum sustainable yield). This approach can be applied when only a fraction of the uncertainty related to estimating the limit catch level is quantified through stock assessments. The approach is applied for illustrative purposes to the fishery for red king crab, Paralithodes camtschaticus, in Bristol Bay, AK.