Merging trait-based ecology and regime shift theory to anticipate community responses to warming.

Anthropogenic warming is altering species abundance, distribution, physiology, and more. How changes observed at the species level alter emergent community properties is an active and urgent area of research. Trait-based ecology and regime shift theory provide complementary ways to understand climate change impacts on communities, but these two bodies of work are only rarely integrated. Lack of integration handicaps our ability to understand community responses to warming, at a time when such understanding is critical. Therefore, we advocate for merging trait-based ecology with regime shift theory. We propose a general set of principles to guide this merger and apply these principles to research on marine communities in the rapidly warming North Atlantic. In our example, combining trait distribution and regime shift analyses at the community level yields greater insight than either alone. Looking forward, we identify a clear need for expanding quantitative approaches to collecting and merging trait-based and resilience metrics in order to advance our understanding of climate-driven community change.

Challenges to natural and human communities from surprising ocean temperatures.

The community of species, human institutions, and human activities at a given location have been shaped by historical conditions (both mean and variability) at that location. Anthropogenic climate change is now adding strong trends on top of existing natural variability. These trends elevate the frequency of "surprises"-conditions that are unexpected based on recent history. Here, we show that the frequency of surprising ocean temperatures has increased even faster than expected based on recent temperature trends. Using a simple model of human adaptation, we show that these surprises will increasingly challenge natural modes of adaptation that rely on historical experience. We also show that warming rates are likely to shift natural communities toward generalist species, reducing their productivity and diversity. Our work demonstrates increasing benefits for individuals and institutions from betting that trends will continue, but this strategy represents a radical shift that will be difficult for many to make.

Climate vulnerability and resilience in the most valuable North American fishery.

Managing natural resources in an era of increasing climate impacts requires accounting for the synergistic effects of climate, ecosystem changes, and harvesting on resource productivity. Coincident with recent exceptional warming of the northwest Atlantic Ocean and removal of large predatory fish, the American lobster has become the most valuable fishery resource in North America. Using a model that links ocean temperature, predator density, and fishing to population productivity, we show that harvester-driven conservation efforts to protect large lobsters prepared the Gulf of Maine lobster fishery to capitalize on favorable ecosystem conditions, resulting in the record-breaking landings recently observed in the region. In contrast, in the warmer southern New England region, the absence of similar conservation efforts precipitated warming-induced recruitment failure that led to the collapse of the fishery. Population projections under expected warming suggest that the American lobster fishery is vulnerable to future temperature increases, but continued efforts to preserve the stock's reproductive potential can dampen the negative impacts of warming. This study demonstrates that, even though global climate change is severely impacting marine ecosystems, widely adopted, proactive conservation measures can increase the resilience of commercial fisheries to climate change.

The cresting wave: larval settlement and ocean temperatures predict change in the American lobster harvest.

Adding to the challenge of predicting fishery recruitment in a changing environment is downscaling predictions to capture locally divergent trends over a species' range. In recent decades, the American lobster (Homarus americanus) fishery has shifted poleward along the northwest Atlantic coast, one of the most rapidly warming regions of the world's oceans. Building on evidence that early post-settlement life stages predict future fishery recruitment, we describe enhancements to a forecasting model that predict landings using an annual larval settlement index from 62 fixed sites among 10 study areas from Rhode Island, USA to New Brunswick, Canada. The model is novel because it incorporates local bottom temperature and disease prevalence to scale spatial and temporal changes in growth and mortality. For nine of these areas, adding environmental predictors significantly improved model performance, capturing a landings surge in the eastern Gulf of Maine, and collapse in southern New England. On the strength of these analyses, we project landings within the next decade to decline to near historical levels in the Gulf of Maine and no recovery in the south. This approach is timely as downscaled ocean temperature projections enable decision makers to assess their options under future climate scenarios at finer spatial scales.

The biogeography of marine plankton traits.

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations.

North American Atlantic salmon (Salmo salar) populations experienced substantial declines in the early 1990s, and many populations have persisted at low abundances in recent years. Abundance and productivity declined in a coherent manner across major regions of North America, and this coherence points toward a potential shift in marine survivorship, rather than local, river-specific factors. The major declines in Atlantic salmon populations occurred against a backdrop of physical and biological shifts in Northwest Atlantic ecosystems. Analyses of changes in climate, physical, and lower trophic level biological factors provide substantial evidence that climate conditions directly and indirectly influence the abundance and productivity of North American Atlantic salmon populations. A major decline in salmon abundance after 1990 was preceded by a series of changes across multiple levels of the ecosystem, and a subsequent population change in 1997, primarily related to salmon productivity, followed an unusually low NAO event. Pairwise correlations further demonstrate that climate and physical conditions are associated with changes in plankton communities and prey availability, which are ultimately linked to Atlantic salmon populations. Results suggest that poor trophic conditions, likely due to climate-driven environmental factors, and warmer ocean temperatures throughout their marine habitat area are constraining the productivity and recovery of North American Atlantic salmon populations.

Whales in the carbon cycle: can recovery remove carbon dioxide?

The great whales (baleen and sperm whales), through their massive size and wide distribution, influence ecosystem and carbon dynamics. Whales directly store carbon in their biomass and contribute to carbon export through sinking carcasses. Whale excreta may stimulate phytoplankton growth and capture atmospheric CO2; such indirect pathways represent the greatest potential for whale-carbon sequestration but are poorly understood. We quantify the carbon values of whales while recognizing the numerous ecosystem, cultural, and moral motivations to protect them. We also propose a framework to quantify the economic value of whale carbon as populations change over time. Finally, we suggest research to address key unknowns (e.g., bioavailability of whale-derived nutrients to phytoplankton, species- and region-specific variability in whale carbon contributions).

First principles of copepod development help explain global marine diversity patterns.

A major goal of modern ecology is to understand macroecological patterns based on their mechanistic underpinnings. The metabolic theory of ecology predicts a monotonic increase of biodiversity with temperature based on the principles of metabolism. For marine copepods, observations have shown that while biodiversity does increase with temperature, the theory's prediction overestimates the slope of this relationship by a factor of two. By relaxing the theory's assumption that size is invariant with respect to temperature, and by incorporating a mechanistic description of copepod development into the theory, we provide an adjusted prediction that agrees with the observed relationship. The addition of development into the theory adds the potential to refine the prediction for a wider range of taxa, to account for discrepancies between prediction and observations, and to describe a wider variety of temperature-richness relationships.

The North Atlantic Ecosystem, from Plankton to Whales.

Compared with terrestrial ecosystems, marine ecosystems have a higher proportion of heterotrophic biomass. Building from this observation, we define the North Atlantic biome as the region where the large, lipid-rich copepod Calanus finmarchicus is the dominant mesozooplankton species. This species is superbly adapted to take advantage of the intense pulse of productivity associated with the North Atlantic spring bloom. Most of the characteristic North Atlantic species, including cod, herring, and right whales, rely on C. finmarchicus either directly or indirectly. The notion of a biome rests inherently on an assumption of stability, yet conditions in the North Atlantic are anything but stable. Humans have reduced the abundance of many fish and whales (though some recovery is underway). Humans are also introducing physical and chemical trends associated with global climate change. Thus, the future of the North Atlantic depends on the biome's newest species, Homo sapiens.

Comparing and synthesizing quantitative distribution models and qualitative vulnerability assessments to project marine species distributions under climate change.

Species distribution shifts are a widely reported biological consequence of climate-driven warming across marine ecosystems, creating ecological and social challenges. To meet these challenges and inform management decisions, we need accurate projections of species distributions. Quantitative species distribution models (SDMs) are routinely used to make these projections, while qualitative climate change vulnerability assessments are becoming more common. We constructed SDMs, compared SDM projections to expectations from a qualitative expert climate change vulnerability assessment, and developed a novel approach for combining the two methods to project the distribution and relative biomass of 49 marine species in the Northeast Shelf Large Marine Ecosystem under a "business as usual" climate change scenario. A forecasting experiment using SDMs highlighted their ability to capture relative biomass patterns fairly well (mean Pearson's correlation coefficient between predicted and observed biomass = 0.24, range = 0-0.6) and pointed to areas needing improvement, including reducing prediction error and better capturing fine-scale spatial variability. SDM projections suggest the region will undergo considerable biological changes, especially in the Gulf of Maine, where commercially-important groundfish and traditional forage species are expected to decline as coastal fish species and warmer-water forage species historically found in the southern New England/Mid-Atlantic Bight area increase. The SDM projections only occasionally aligned with vulnerability assessment expectations, with agreement more common for species with adult mobility and population growth rates that showed low sensitivity to climate change. Although our blended approach tried to build from the strengths of each method, it had no noticeable improvement in predictive ability over SDMs. This work rigorously evaluates the predictive ability of SDMs, quantifies expected species distribution shifts under future climate conditions, and tests a new approach for integrating SDMs and vulnerability assessments to help address the complex challenges arising from climate-driven species distribution shifts.

Climate change effects on biodiversity, ecosystems, ecosystem services, and natural resource management in the United States.

Climate change is a pervasive and growing global threat to biodiversity and ecosystems. Here, we present the most up-to-date assessment of climate change impacts on biodiversity, ecosystems, and ecosystem services in the U.S. and implications for natural resource management. We draw from the 4th National Climate Assessment to summarize observed and projected changes to ecosystems and biodiversity, explore linkages to important ecosystem services, and discuss associated challenges and opportunities for natural resource management. We find that species are responding to climate change through changes in morphology and behavior, phenology, and geographic range shifts, and these changes are mediated by plastic and evolutionary responses. Responses by species and populations, combined with direct effects of climate change on ecosystems (including more extreme events), are resulting in widespread changes in productivity, species interactions, vulnerability to biological invasions, and other emergent properties. Collectively, these impacts alter the benefits and services that natural ecosystems can provide to society. Although not all impacts are negative, even positive changes can require costly societal adjustments. Natural resource managers need proactive, flexible adaptation strategies that consider historical and future outlooks to minimize costs over the long term. Many organizations are beginning to explore these approaches, but implementation is not yet prevalent or systematic across the nation.

Arctic climatechange and its impacts on the ecology of the North Atlantic.

Arctic climate change from the Paleocene epoch to the present is reconstructed with the objective of assessing its recent and future impacts on the ecology of the North Atlantic. A recurring theme in Earth's paleoclimate record is the importance of the Arctic atmosphere, ocean, and cryosphere in regulating global climate on a variety of spatial and temporal scales. A second recurring theme in this record is the importance of freshwater export from the Arctic in regulating global- to basin-scale ocean circulation patterns and climate. Since the 1970s, historically unprecedented changes have been observed in the Arctic as climate warming has increased precipitation, river discharge, and glacial as well as sea-ice melting. In addition, modal shifts in the atmosphere have altered Arctic Ocean circulation patterns and the export of freshwater into the North Atlantic. The combination of these processes has resulted in variable patterns of freshwater export from the Arctic Ocean and the emergence of salinity anomalies that have periodically freshened waters in the North Atlantic. Since the early 1990s, changes in Arctic Ocean circulation patterns and freshwater export have been associated with two types of ecological responses in the North Atlantic. The first of these responses has been an ongoing series of biogeographic range expansions by boreal plankton, including renewal of the trans-Arctic exchanges of Pacific species with the Atlantic. The second response was a dramatic regime shift in the shelf ecosystems of the Northwest Atlantic that occurred during the early 1990s. This regime shift resulted from freshening and stratification of the shelf waters, which in turn could be linked to changes in the abundances and seasonal cycles of phytoplankton, zooplankton, and higher trophic-level consumer populations. It is predicted that the recently observed ecological responses to Arctic climate change in the North Atlantic will continue into the near future if current trends in sea ice, freshwater export, and surface ocean salinity continue. It is more difficult to predict ecological responses to abrupt climate change in the more distant future as tipping points in the Earth's climate system are exceeded.

The relation between productivity and species diversity in temperate-Arctic marine ecosystems.

Energy variables, such as evapotranspiration, temperature, and productivity explain significant variation in the diversity of many groups of terrestrial plants and animals at local to global scales. Although the ocean represents the largest continuous habitat on earth with a vast spectrum of primary productivity and species richness, little is known about how productivity influences species diversity in marine systems. To search for general relationships between productivity and species richness in the ocean, we analyzed data from three different benthic marine ecosystems (epifaunal communities on subtidal rock walls, on navigation buoys in the Gulf of St. Lawrence, and Canadian Arctic macrobenthos) across local to continental spatial scales (<20 to >1000 km) using a standardized proxy for productivity, satellite-derived chlorophyll a. Theoretically, the form of the function between productivity and species richness is either monotonically increasing or decreasing, or curvilinear (hump- or U-shaped). We found three negative linear and three hump-shaped relationships between chlorophyll a and species richness out of 10 independent comparisons. Scale dependence was suggested by more prevalent diversity-productivity relationships at smaller (local, landscape) than larger (regional, continental) spatial scales. Differences in the form of the functions were more closely allied with community type than with scale, as negative linear functions were restricted to sessile epifauna while hump-shaped functions occurred in Arctic macrobenthos (mixed epifauna, infauna). In two of the data sets, (St. Lawrence epifauna and Arctic macrobenthos) significant effects of chlorophyll a co-varied with the effects of salinity, suggesting that environmental stress as well as productivity influences diversity in these marine systems. The co-varying effect of salinity may commonly arise in broad-scale studies of productivity and diversity in marine ecosystems when attempting to sample the largest range of productivity, often encompassing a coastal-oceanic gradient.

Response to Comments on "Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery".

Palmer et al and Swain et al suggest that our "extra mortality" time series is spurious. In response, we show that including temperature-dependent mortality improves abundance estimates and that warming waters reduce growth rates in Gulf of Maine cod. Far from being spurious, temperature effects on this stock are clear, and continuing to ignore them puts the stock in jeopardy.

Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery.

Several studies have documented fish populations changing in response to long-term warming. Over the past decade, sea surface temperatures in the Gulf of Maine increased faster than 99% of the global ocean. The warming, which was related to a northward shift in the Gulf Stream and to changes in the Atlantic Multidecadal Oscillation and Pacific Decadal Oscillation, led to reduced recruitment and increased mortality in the region's Atlantic cod (Gadus morhua) stock. Failure to recognize the impact of warming on cod contributed to overfishing. Recovery of this fishery depends on sound management, but the size of the stock depends on future temperature conditions. The experience in the Gulf of Maine highlights the need to incorporate environmental factors into resource management.

The impact of whaling on the ocean carbon cycle: why bigger was better.

BACKGROUND: Humans have reduced the abundance of many large marine vertebrates, including whales, large fish, and sharks, to only a small percentage of their pre-exploitation levels. Industrial fishing and whaling also tended to preferentially harvest the largest species and largest individuals within a population. We consider the consequences of removing these animals on the ocean's ability to store carbon. METHODOLOGY/PRINCIPAL FINDINGS: Because body size is critical to our arguments, our analysis focuses on populations of baleen whales. Using reconstructions of pre-whaling and modern abundances, we consider the impact of whaling on the amount of carbon stored in living whales and on the amount of carbon exported to the deep sea by sinking whale carcasses. Populations of large baleen whales now store 9.1×10(6) tons less carbon than before whaling. Some of the lost storage has been offset by increases in smaller competitors; however, due to the relative metabolic efficiency of larger organisms, a shift toward smaller animals could decrease the total community biomass by 30% or more. Because of their large size and few predators, whales and other large marine vertebrates can efficiently export carbon from the surface waters to the deep sea. We estimate that rebuilding whale populations would remove 1.6×10(5) tons of carbon each year through sinking whale carcasses. CONCLUSIONS/SIGNIFICANCE: Even though fish and whales are only a small portion of the ocean's overall biomass, fishing and whaling have altered the ocean's ability to store and sequester carbon. Although these changes are small relative to the total ocean carbon sink, rebuilding populations of fish and whales would be comparable to other carbon management schemes, including ocean iron fertilization.