Climate change impacts on seabirds and marine mammals: The importance of study duration, thermal tolerance and generation time.

Understanding climate change impacts on top predators is fundamental to marine biodiversity conservation, due to their increasingly threatened populations and their importance in marine ecosystems. We conducted a systematic review of the effects of climate change (prolonged, directional change) and climate variability on seabirds and marine mammals. We extracted data from 484 studies (4808 published studies were reviewed), comprising 2215 observations on demography, phenology, distribution, diet, behaviour, body condition and physiology. The likelihood of concluding that climate change had an impact increased with study duration. However, the temporal thresholds for the effects of climate change to be discernibly varied from 10 to 29 years depending on the species, the biological response and the oceanic study region. Species with narrow thermal ranges and relatively long generation times were more often reported to be affected by climate change. This provides an important framework for future assessments, with guidance on response- and region-specific temporal dimensions that need to be considered when reporting effects of climate change. Finally, we found that tropical regions and non-breeding life stages were poorly covered in the literature, a concern that should be addressed to enable a better understanding of the vulnerability of marine predators to climate change.

Geographical limits to species-range shifts are suggested by climate velocity.

The reorganization of patterns of species diversity driven by anthropogenic climate change, and the consequences for humans, are not yet fully understood or appreciated. Nevertheless, changes in climate conditions are useful for predicting shifts in species distributions at global and local scales. Here we use the velocity of climate change to derive spatial trajectories for climatic niches from 1960 to 2009 (ref. 7) and from 2006 to 2100, and use the properties of these trajectories to infer changes in species distributions. Coastlines act as barriers and locally cooler areas act as attractors for trajectories, creating source and sink areas for local climatic conditions. Climate source areas indicate where locally novel conditions are not connected to areas where similar climates previously occurred, and are thereby inaccessible to climate migrants tracking isotherms: 16% of global surface area for 1960 to 2009, and 34% of ocean for the 'business as usual' climate scenario (representative concentration pathway (RCP) 8.5) representing continued use of fossil fuels without mitigation. Climate sink areas are where climate conditions locally disappear, potentially blocking the movement of climate migrants. Sink areas comprise 1.0% of ocean area and 3.6% of land and are prevalent on coasts and high ground. Using this approach to infer shifts in species distributions gives global and regional maps of the expected direction and rate of shifts of climate migrants, and suggests areas of potential loss of species richness.

Rising synchrony controls western North American ecosystems.

Along the western margin of North America, the winter expression of the North Pacific High (NPH) strongly influences interannual variability in coastal upwelling, storm track position, precipitation, and river discharge. Coherence among these factors induces covariance among physical and biological processes across adjacent marine and terrestrial ecosystems. Here, we show that over the past century the degree and spatial extent of this covariance (synchrony) has substantially increased, and is coincident with rising variance in the winter NPH. Furthermore, centuries-long blue oak (Quercus douglasii) growth chronologies sensitive to the winter NPH provide robust evidence that modern levels of synchrony are among the highest observed in the context of the last 250 years. These trends may ultimately be linked to changing impacts of the El Niño Southern Oscillation on midlatitude ecosystems of North America. Such a rise in synchrony may destabilize ecosystems, expose populations to higher risks of extinction, and is thus a concern given the broad biological relevance of winter climate to biological systems.

Persistence of trophic hotspots and relation to human impacts within an upwelling marine ecosystem.

Human impacts (e.g., fishing, pollution, and shipping) on pelagic ecosystems are increasing, causing concerns about stresses on marine food webs. Maintaining predator-prey relationships through protection of pelagic hotspots is crucial for conservation and management of living marine resources. Biotic components of pelagic, plankton-based, ecosystems exhibit high variability in abundance in time and space (i.e., extreme patchiness), requiring investigation of persistence of abundance across trophic levels to resolve trophic hotspots. Using a 26-yr record of indicators for primary production, secondary (zooplankton and larval fish), and tertiary (seabirds) consumers, we show distributions of trophic hotspots in the southern California Current Ecosystem result from interactions between a strong upwelling center and a productive retention zone with enhanced nutrients, which concentrate prey and predators across multiple trophic levels. Trophic hotspots also overlap with human impacts, including fisheries extraction of coastal pelagic and groundfish species, as well as intense commercial shipping traffic. Spatial overlap of trophic hotspots with fisheries and shipping increases vulnerability of the ecosystem to localized depletion of forage fish, ship strikes on marine mammals, and pollution. This study represents a critical step toward resolving pelagic areas of high conservation interest for planktonic ecosystems and may serve as a model for other ocean regions where ecosystem-based management and marine spatial planning of pelagic ecosystems is warranted.

Spatio-temporal dynamics of ocean conditions and forage taxa reveal regional structuring of seabird­prey relationships.

Studies of predator­prey demographic responses and the physical drivers of such relationships are rare, yet essential for predicting future changes in the structure and dynamics of marine ecosystems. Here, we hypothesize that predator­prey relationships vary spatially in association with underlying physical ocean conditions, leading to observable changes in demographic rates, such as reproduction. To test this hypothesis, we quantified spatio-temporal variability in hydrographic conditions, krill, and forage fish to model predator (seabird) demographic responses over 18 years (1990­2007). We used principal component analysis and spatial correlation maps to assess coherence among ocean conditions, krill, and forage fish, and generalized additive models to quantify interannual variability in seabird breeding success relative to prey abundance. The first principal component of four hydrographic measurements yielded an index that partitioned "warm/weak upwelling" and "cool/strong upwelling" years. Partitioning of krill and forage fish time series among shelf and oceanic regions yielded spatially explicit indicators of prey availability. Krill abundance within the oceanic region was remarkably consistent between years, whereas krill over the shelf showed marked interannual fluctuations in relation to ocean conditions. Anchovy abundance varied on the shelf, and was greater in years of strong stratification, weak upwelling and warmer temperatures. Spatio-temporal variability of juvenile forage fish co-varied strongly with each other and with krill, but was weakly correlated with hydrographic conditions. Demographic responses between seabirds and prey availability revealed spatially variable associations indicative of the dynamic nature of "predator­habitat" relationships. Quantification of spatially explicit demographic responses, and their variability through time, demonstrate the possibility of delineating specific critical areas where the implementation of protective measures could maintain functions and productivity of central place foraging predators.

Climate Change Impacts on Eastern Boundary Upwelling Systems.

The world's eastern boundary upwelling systems (EBUSs) contribute disproportionately to global ocean productivity and provide critical ecosystem services to human society. The impact of climate change on EBUSs and the ecosystems they support is thus a subject of considerable interest. Here, we review hypotheses of climate-driven change in the physics, biogeochemistry, and ecology of EBUSs; describe observed changes over recent decades; and present projected changes over the twenty-first century. Similarities in historical and projected change among EBUSs include a trend toward upwelling intensification in poleward regions, mitigatedwarming in near-coastal regions where upwelling intensifies, and enhanced water-column stratification and a shoaling mixed layer. However, there remains significant uncertainty in how EBUSs will evolve with climate change, particularly in how the sometimes competing changes in upwelling intensity, source-water chemistry, and stratification will affect productivity and ecosystem structure. We summarize the commonalities and differences in historical and projected change in EBUSs and conclude with an assessment of key remaining uncertainties and questions. Future studies will need to address these questions to better understand, project, and adapt to climate-driven changes in EBUSs.

Climate change and marine life.

A Marine Climate Impacts Workshop was held from 29 April to 3 May 2012 at the US National Center of Ecological Analysis and Synthesis in Santa Barbara. This workshop was the culmination of a series of six meetings over the past three years, which had brought together 25 experts in climate change ecology, analysis of large datasets, palaeontology, marine ecology and physical oceanography. Aims of these workshops were to produce a global synthesis of climate impacts on marine biota, to identify sensitive habitats and taxa, to inform the current Intergovernmental Panel on Climate Change (IPCC) process, and to strengthen research into ecological impacts of climate change.

Winter oceanographic conditions predict summer bull kelp canopy cover in northern California.

Bull kelp, Nereocystis luetkeana, is an iconic kelp forest species of the Northeast Pacific that provides a wide range of ecosystem services to coastal marine species and society. In northern California, U.S.A., Nereocystis abundance declined sharply in 2014 and has yet to recover. While abiotic and biotic stressors were present prior to 2014, the population collapse highlights the need for a better understanding of how environmental conditions impact Nereocystis. In this study, we used a newly-developed, satellite-based dataset of bull kelp abundance, proxied by canopy cover over 20 years, to test the hypothesis that winter oceanographic conditions determine summer Nereocystis canopy cover. For the years before the collapse (1991 through 2013), wintertime ocean conditions, synthesized in a Multivariate Ocean Climate Indicator (MOCI), were indeed a good predictor of summer Nereocystis canopy cover (R2 = 0.40 to 0.87). We attribute this relationship to the effects of upwelling and/or temperature on nutrient availability. South of Point Arena, California, winter ocean conditions had slightly lower explanatory power than north of Point Arena, also reflective of spring upwelling-driven nutrient entrainment. Results suggest that the Nereocystis gametophytes and/or early sporophytes are sensitive to winter oceanographic conditions. Furthermore, environmental conditions in winter 2014 could have been used to predict the Nereocystis collapse in summer 2014, and for kelp north of Point Arena, a further decline in 2015. Importantly, environmental models do not predict changes in kelp after 2015, suggesting biotic factors suppressed kelp recovery, most likely extreme sea urchin herbivory. Conditions during winter, a season that is often overlooked in studies of biophysical interactions, are useful for predicting summer Nereocystis kelp forest canopy cover, and will be useful in supporting kelp restoration actions in California and perhaps elsewhere in the world.

Global decline in ocean memory over the 21st century.

Ocean memory, the persistence of ocean conditions, is a major source of predictability in the climate system beyond weather time scales. We show that ocean memory, as measured by the year-to-year persistence of sea surface temperature anomalies, is projected to steadily decline in the coming decades over much of the globe. This global decline in ocean memory is predominantly driven by shoaling of the upper-ocean mixed layer depth in response to global surface warming, while thermodynamic and dynamic feedbacks can contribute substantially regionally. As the mixed layer depth shoals, stochastic forcing becomes more effective in driving sea surface temperature anomalies, increasing high-frequency noise at the expense of persistent signals. Reduced ocean memory results in shorter lead times of skillful persistence-based predictions of sea surface thermal conditions, which may present previously unknown challenges for predicting climate extremes and managing marine biological resources under climate change.

Interannual temperature variability is a principal driver of low-frequency fluctuations in marine fish populations.

Marine fish populations commonly exhibit low-frequency fluctuations in biomass that can cause catch volatility and thus endanger the food and economic security of dependent coastal societies. Such variability has been linked to fishing intensity, demographic processes and environmental variability, but our understanding of the underlying drivers remains poor for most fish stocks. Our study departs from previous findings showing that sea surface temperature (SST) is a significant driver of fish somatic growth variability and that life-history characteristics mediate population-level responses to environmental variability. We use autoregressive models to simulate how fish populations integrate SST variability over multiple years depending on fish life span and trophic position. We find that simulated SST-driven population dynamics can explain a significant portion of observed low-frequency variability in independent observations of fisheries landings around the globe. Predictive skill, however, decreases with increasing fishing pressure, likely due to demographic truncation. Using our modelling approach, we also show that increases in the mean and variance of SST could amplify biomass volatility and lessen its predictability in the future. Overall, biological integration of high-frequency SST variability represents a null hypothesis with which to explore the drivers of low-frequency population change across upper-trophic marine species.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.

Spatio-temporal persistence of zooplankton communities in the Gulf of Alaska.

Spatial structuring of mid-trophic level forage communities in the Gulf of Alaska (GoA) is poorly understood, even though it has clear implications for the health of fisheries and marine wildlife populations. Here, we test the hypothesis that summertime (May-August) mesozooplankton communities are spatially-persistent across years of varying ocean conditions, including during the marine heatwave of 2014-2016. We use spatial ordinations and hierarchical clustering of Continuous Plankton Recorder (CPR) sampling over 17 years (2000-2016) to (1) characterize typical zooplankton communities in different regions of the GoA, and (2) investigate spatial structuring relative to variation in ocean temperatures and circulation. Five regional communities were identified, each representing distinct variation in the abundance of 18 primary zooplankton taxa: a distinct cluster of coastal taxa on the continental shelf north of Vancouver Island; a second cluster in the western GoA associated with strong currents and cold water east of Unimak Pass; a shelf break cluster rich in euphausiids found at both the eastern and western margins of the GoA; a broad offshore cluster of abundant pelagic zooplankton in the southern GoA gyre associated with stable temperature and current conditions; and a final offshore cluster exhibiting low zooplankton abundance concentrated along the northeastern arm of the subarctic gyre where ocean conditions are dominated by eddy activity. When comparing years of anomalous warm and cold sea surface temperatures, we observed change in the spatial structure in coastal communities, but little change (i.e., spatial persistence) in the northwestern GoA basin. Whereas previous studies have shown within-region variability in zooplankton communities in response to ocean climate, we highlight both consistency and change in regional communities, with interannual variability in shelf communities and persistence in community structure offshore. These results suggest greater variability in coastal food webs than in the central portion of the GoA, which may be important to energy exchange from lower to upper trophic levels in the mesoscale biomes of this ecosystem.

Habitat compression and ecosystem shifts as potential links between marine heatwave and record whale entanglements.

Climate change and increased variability and intensity of climate events, in combination with recovering protected species populations and highly capitalized fisheries, are posing new challenges for fisheries management. We examine socio-ecological features of the unprecedented 2014-2016 northeast Pacific marine heatwave to understand the potential causes for record numbers of whale entanglements in the central California Current crab fishery. We observed habitat compression of coastal upwelling, changes in availability of forage species (krill and anchovy), and shoreward distribution shift of foraging whales. We propose that these ecosystem changes, combined with recovering whale populations, contributed to the exacerbation of entanglements throughout the marine heatwave. In 2016, domoic acid contamination prompted an unprecedented delay in the opening of California's Dungeness crab fishery that inadvertently intensified the spatial overlap between whales and crab fishery gear. We present a retroactive assessment of entanglements to demonstrate that cooperation of fishers, resource managers, and scientists could mitigate future entanglement risk by developing climate-ready fisheries approaches, while supporting thriving fishing communities.

Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016.

About 62,000 dead or dying common murres (Uria aalge), the trophically dominant fish-eating seabird of the North Pacific, washed ashore between summer 2015 and spring 2016 on beaches from California to Alaska. Most birds were severely emaciated and, so far, no evidence for anything other than starvation was found to explain this mass mortality. Three-quarters of murres were found in the Gulf of Alaska and the remainder along the West Coast. Studies show that only a fraction of birds that die at sea typically wash ashore, and we estimate that total mortality approached 1 million birds. About two-thirds of murres killed were adults, a substantial blow to breeding populations. Additionally, 22 complete reproductive failures were observed at multiple colonies region-wide during (2015) and after (2016-2017) the mass mortality event. Die-offs and breeding failures occur sporadically in murres, but the magnitude, duration and spatial extent of this die-off, associated with multi-colony and multi-year reproductive failures, is unprecedented and astonishing. These events co-occurred with the most powerful marine heatwave on record that persisted through 2014-2016 and created an enormous volume of ocean water (the "Blob") from California to Alaska with temperatures that exceeded average by 2-3 standard deviations. Other studies indicate that this prolonged heatwave reduced phytoplankton biomass and restructured zooplankton communities in favor of lower-calorie species, while it simultaneously increased metabolically driven food demands of ectothermic forage fish. In response, forage fish quality and quantity diminished. Similarly, large ectothermic groundfish were thought to have increased their demand for forage fish, resulting in greater top-predator demands for diminished forage fish resources. We hypothesize that these bottom-up and top-down forces created an "ectothermic vise" on forage species leading to their system-wide scarcity and resulting in mass mortality of murres and many other fish, bird and mammal species in the region during 2014-2017.

Range-wide reproductive consequences of ocean climate variability for the seabird Cassin's Auklet.

We examine how ocean climate variability influences the reproductive phenology and demography of the seabird Cassin's Auklet (Ptychoramphus aleuticus) across approximately 2500 km of its breeding range in the oceanographically dynamic California Current System along the west coast of North America. Specifically, we determine the extent to which ocean climate conditions and Cassin's Auklet timing of breeding and breeding success covary across populations in British Columbia, central California, and northern Mexico over six years (2000-2005) and test whether auklet timing of breeding and breeding success are similarly related to local and large-scale ocean climate indices across populations. Local ocean foraging environments ranged from seasonally variable, high-productivity environments in the north to aseasonal, low-productivity environments to the south, but covaried similarly due to the synchronizing effects of large-scale climate processes. Auklet timing of breeding in the southern population did not covary with populations to the north and was not significantly related to local oceanographic conditions, in contrast to northern populations, where timing of breeding appears to be influenced by oceanographic cues that signal peaks in prey availability. Annual breeding success covaried similarly across populations and was consistently related to local ocean climate conditions across this system. Overall, local ocean climate indices, particularly sea surface height, better explained timing of breeding and breeding success than a large-scale climate index by better representing heterogeneity in physical processes important to auklets and their prey. The significant, consistent relationships we detected between Cassin's Auklet breeding success and ocean climate conditions across widely spaced populations indicate that Cassin's Auklets are susceptible to climate change across the California Current System, especially by the strengthening of climate processes that synchronize oceanographic conditions. Auklet populations in the northern and central regions of this ecosystem may be more sensitive to changes in the timing and variability of ocean climate conditions since they appear to time breeding to take advantage of seasonal productivity peaks.

Timing is everything: flexible phenology and shifting selection in a colonial seabird.

1. In order to reproduce successfully in a temporally varying environment, iteroparous animals must exhibit considerable behavioural flexibility across their lifetimes. By adjusting timing of breeding each year, parents can ensure optimal overlap between the energy intensive period of offspring production and the seasonal peak in favourable environmental conditions, thereby increasing their chances of successfully rearing young. 2. Few studies investigate variation among individuals in how they respond to fluctuating conditions, or how selection acts on these individual differences, but this information is essential for understanding how populations will cope with rapid environmental change. 3. We explored inter-annual trends in breeding time and individual responses to environmental variability in common guillemots Uria aalge, an important marine top predator in the highly variable California Current System. Complex, nonlinear relationships between phenology and oceanic and climate variables were found at the population level. Using a novel application of a statistical technique called random regression, we showed that individual females responded in a nonlinear fashion to environmental variability, and that reaction norm shape differed among females. 4. The pattern and strength of selection varied substantially over a 34-year period, but in general, earlier laying was favoured. Females deviating significantly from the population mean laying date each year also suffered reduced breeding success, with the strength of nonlinear selection varying in relation to environmental conditions. 5. We discuss our results in the wider context of an emerging literature on the evolutionary ecology of individual-level plasticity in the wild. Better understanding of how species-specific factors and local habitat features affect the timing and success of breeding will improve our ability to predict how populations will respond to climate change.

Submarine canyons represent an essential habitat network for krill hotspots in a Large Marine Ecosystem.

Submarine canyon systems are ubiquitous features of marine ecosystems, known to support high levels of biodiversity. Canyons may be important to benthic-pelagic ecosystem coupling, but their role in concentrating plankton and structuring pelagic communities is not well known. We hypothesize that at the scale of a large marine ecosystem, canyons provide a critical habitat network, which maintain energy flow and trophic interactions. We evaluate canyon characteristics relative to the distribution and abundance of krill, critically important prey in the California Current Ecosystem. Using a geological database, we conducted a census of canyon locations, evaluated their dimensions, and quantified functional relationships with krill hotspots (i.e., sites of persistently elevated abundance) derived from hydro-acoustic surveys. We found that 76% of krill hotspots occurred within and adjacent to canyons. Most krill hotspots were associated with large shelf-incising canyons. Krill hotspots and canyon dimensions displayed similar coherence as a function of latitude and indicate a potential regional habitat network. The latitudinal migration of many fish, seabirds and mammals may be enhanced by using this canyon-krill network to maintain foraging opportunities. Biogeographic assessments and predictions of krill and krill-predator distributions under climate change may be improved by accounting for canyons in habitat models.

Climate change and marine vertebrates.

Climate change impacts on vertebrates have consequences for marine ecosystem structures and services. We review marine fish, mammal, turtle, and seabird responses to climate change and discuss their potential for adaptation. Direct and indirect responses are demonstrated from every ocean. Because of variation in research foci, observed responses differ among taxonomic groups (redistributions for fish, phenology for seabirds). Mechanisms of change are (i) direct physiological responses and (ii) climate-mediated predator-prey interactions. Regional-scale variation in climate-demographic functions makes range-wide population dynamics challenging to predict. The nexus of metabolism relative to ecosystem productivity and food webs appears key to predicting future effects on marine vertebrates. Integration of climate, oceanographic, ecosystem, and population models that incorporate evolutionary processes is needed to prioritize the climate-related conservation needs for these species.

Climate change. Six centuries of variability and extremes in a coupled marine-terrestrial ecosystem.

Reported trends in the mean and variability of coastal upwelling in eastern boundary currents have raised concerns about the future of these highly productive and biodiverse marine ecosystems. However, the instrumental records on which these estimates are based are insufficiently long to determine whether such trends exceed preindustrial limits. In the California Current, a 576-year reconstruction of climate variables associated with winter upwelling indicates that variability increased over the latter 20th century to levels equaled only twice during the past 600 years. This modern trend in variance may be unique, because it appears to be driven by an unprecedented succession of extreme, downwelling-favorable, winter climate conditions that profoundly reduce productivity for marine predators of commercial and conservation interest.

Increasing variance in North Pacific climate relates to unprecedented ecosystem variability off California.

Changes in variance are infrequently examined in climate change ecology. We tested the hypothesis that recent high variability in demographic attributes of salmon and seabirds off California is related to increasing variability in remote, large-scale forcing in the North Pacific operating through changes in local food webs. Linear, indirect numerical responses between krill (primarily Thysanoessa spinifera) and juvenile rockfish abundance (catch per unit effort (CPUE)) explained >80% of the recent variability in the demography of these pelagic predators. We found no relationships between krill and regional upwelling, though a strong connection to the North Pacific Gyre Oscillation (NPGO) index was established. Variance in NPGO and related central Pacific warming index increased after 1985, whereas variance in the canonical ENSO and Pacific Decadal Oscillation did not change. Anthropogenic global warming or natural climate variability may explain recent intensification of the NPGO and its increasing ecological significance. Assessing non-stationarity in atmospheric-environmental interactions and placing greater emphasis on documenting changes in variance of bio-physical systems will enable insight into complex climate-marine ecosystem dynamics.