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Due to unanticipated outcomes of climate change impacts on marine ecosystems, new challenges in management and conservation are arising1. One consequence of increasing anthropogenic climate warming is an increasing frequency, duration, and spatial extent of Marine heatwaves2 (MHWs). The variety of MHW impacts on marine life and fisheries has generated new challenges in ecosystem management and conservation of protected species3,4,5,6,7. Specifically, MHWs may lead to social and economic pressures, such as shifts in fisheries resources and/or by-catch of protected species3,8,9,10,11. In particular, whale entanglements in fishing gear have been increasing globally12,13,14, often at a rate greater than that of population recoveries from past exploitation, so there is a clear and immediate need to better understand how climate extremes are impacting habitat used by whales and fisheries15,16,17,18. Moreover, there is a growing need to improve the use and utility of ecosystem scientific advice relevant to marine resource management when confronted by novel ecosystem and fishery system states such as those that emerged in recent MHW events19,20,21,22.
Assessment of relative abundance and spatial intensity of forage species provides information for monitoring regional variability of prey resources used by whales at spatial scales relevant to whale movement and foraging patterns (Fig. 3 and Supplementary Fig. 4). Our evaluation of the regional distribution and spatial intensity of krill (measured by acoustics) and mid-water trawl catches of anchovy indicates changes in the availability of prey used by humpback whales preceding and during the MWH (Fig. 3). During 2013, when the HCI indicated expansion of cool water and record upwelling5,38 (Fig. 1), relative abundance of total anchovy was low, displaying low spatial intensity throughout the coast. In contrast, krill abundance was high, patches were plentiful, and spatial intensity was high, suggesting high clustering throughout the coast. During 2014, when the HCI indicated moderate compression of cool upwelled water, anchovy catches were significantly clustered in the southern portion of the coast, and krill abundance and spatial intensity declined (Figs. 1 and 3). At the peak of the MHW, under strong habitat compression (Fig. 1), 2015 catches of total anchovy were highly clustered coastwide, while krill spatial intensity decreased coastwide (Fig. 3). In 2015 and 2016, when upwelling habitat was highly compressed shoreward, krill abundance was lower, but spatial intensity increased in 2015 and declined abruptly in 2016, indicating there were fewer krill hotspots available for whales. Furthermore, mean abundance of total anchovy increased coastwide in 2015 and was relatively restricted in 2016 with extreme clustering within Monterey Bay and to the south off Point Conception (Fig. 3 and Supplementary Fig. 4). These indices provide reference points for evaluating potential thresholds in forage species availability utilized by whales.
The number of confirmed whale entanglements, most notably humpback whales, spiked throughout the MHW (Figs. 2a and 4). The confirmed whale-entanglement time series reflects a summary of reports for the entire US West Coast, but most entanglements were reported off California. A majority of the entanglements that were identified to some specific origin were linked to Dungeness crab fishing gear, especially within the central coast region of Monterey Bay where there is a substantial human population and a large whale-watching industry that could increase the relative probability of sighting entangled whales relative to less densely populated coastal areas16,17. When fishing gear is identified, the majority of confirmed humpback whale entanglements are due to pot gear and 70% is attributed to commercial Dungeness crab fishing gear17. Importantly, the reported entanglement location does not imply where the entanglement occurred, as whales have been documented to swim hundreds of miles trailing fishing gear for weeks, months, or even years54.
Prey-switching by humpback whales is a complex behavior that is in part related to forage species abundance and patch distribution43. Specifically, stable isotope analysis of humpback whales over an extended time period supports prey-switching between krill and anchovies, in a pattern consistent with the shifts in abundance observed in the survey data37,43. Prey-switching behavior could also depend on the abundance of whales within a feeding ground, because whales may compete for the most profitable foraging areas and higher whale densities could result in some whales having to take up other foraging areas (e.g., nearshore). Whales require sufficient prey concentrations to meet their energetic demands and arrangement of prey aggregations is a critical aspect of their foraging and movement ecology. Therefore, spatial intensity of forage aggregations is relevant for understanding whale feeding behavior (e.g., movement, feeding attempts) and their relative abundance to resolve whether a feeding location is more or less profitable. When whales feed on krill patches, it is presumed that feeding is energetically conservative because krill patches are typically densely concentrated over several kilometers, concentrated at particular depths (e.g., pycnocline), and compared with anchovy, krill are less likely to evade capture by whales. When feeding on anchovy, whale foraging and feeding behavior is considerably more active and acrobatic (e.g., breaching behavior to shoal fish), because they pursue faster moving fish schools56. It is thought, but not firmly established, that entanglement risk can be attributed to increased feeding-related movements by whales within areas of dense anchovy and high concentration of crab gear (i.e., density and number of vertical lines). To complicate things, anchovy are known vectors for concentrating and transferring domoic acid toxin to their predators. Therefore, domoic acid poisoning may have influenced behavior and health of whales feeding on anchovy26,28.
The synthesis of information on changes in ocean and forage species described in this study provided the basis for establishing an ecosystem oceanographic perspective to support the California Dungeness Crab Whale Entanglement Working Group to form and further develop the Risk Assessment and Mitigation Program (RAMP) to reduce whale entanglements in fixed-gear fisheries off California. Infographic prepared by S. Kim.
The connection among marine climate change, persistence of elevated SST and thresholds underlying MHW identification are now well established globally and regionally2. The factors underlying MHW events may occur under different ocean-climate conditions, but they have similar impacts on marine ecosystems and the services they provide (e.g., decline in fishery yield, unusual mortality events, and by-catch). Our study applied a straightforward measure of the amount of cool water upwelling habitat and upwelling habitat compression and evaluated it for understanding changes in forage species distribution and whale entanglements. This measure of habitat area may benefit dynamic ocean management61,62, especially during MHW monitoring2. Along with other metrics of upwelling, primary production, and harmful algal bloom occurrence, the HCI should be considered for ecosystem monitoring in the CCLME and may be easily extended to other eastern boundary upwelling ecosystems. Although the HCI provides a relative measure of thermal habitat, other satellite-based metrics are rapidly evolving to quantify seascape heterogeneity and future research should evaluate their ecological significance21,63. Dynamic ocean management tools for protected species offer platforms for providing custom-tailored information for managing and minimizing adverse impacts on sensitive species62, and should be explored for mitigating whale-entanglement risk. The benefit of these management tools is their flexibility, and extending the HCI with additional satellite-based seascape metrics that are spatially-explicit for krill, anchovy, whale distributions, fishing activity, and whale-entanglement risk can and should be investigated.
Whale-entanglement reports are compiled and maintained by NOAA Fisheries. The NOAA West Coast Region reviews all incoming documentation from entanglement reports (e.g., photo, video, descriptions, follow-up sighting reports, and response from disentanglement teams) before confirming them. Recent confirmed whale-entanglement data were derived from: _species/marine_mammals/5.2.2018_wcr_2018_entanglement_report_508.pdf). Considerable effort is required to assess each entanglement and determine the gear type that is involved. It is also important to note that a reported whale-entanglement location may not reflect the location of where the entanglement occurred. Confirmed entanglements for humpback whales are summarized by month to examine changes over time.
Data on fishery landings are available from the Pacific Fisheries Information Network (PacFIN), retrieval dated 22 May 2018. Pacific States Marine Fisheries Commission, Portland, Oregon (
www.psmfc.org). It is noteworthy that confidentiality restrictions prevent access to raw data in some instances. Filtered data are available at: =501:1000.
The project was supported in part from the CA Ocean Protection Council (to JAS) and by the US Marine Biodiversity Observation Network (MBON), jointly funded by NOAA, NASA, and the National Oceanographic Partnership Program (NNX14AP62A). We thank the California Dungeness Crab Whale Entanglement Working Group, Ocean Protection Council, and the Nature Conservancy. We thank the NOAA-NMFS Southwest Fisheries Science Center and the dedicated researchers maintaining the Rockfish Recruitment and Ecosystem Assessment Survey. We thank the NOAA California Current Integrated Ecosystem Assessment team and Su Kim for preparation of Fig. 5. J.A.S. thanks Richard Ogg and John Mellor for their insight and guidance. We also thank the many dedicated people that are working diligently to disentangle whales.
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