Decadal-scale phenology and seasonal climate drivers of migratory baleen whales in a rapidly warming marine ecosystem.

Species' response to rapid climate change can be measured through shifts in timing of recurring biological events, known as phenology. The Gulf of Maine is one of the most rapidly warming regions of the ocean, and thus an ideal system to study phenological and biological responses to climate change. A better understanding of climate-induced changes in phenology is needed to effectively and adaptively manage human-wildlife conflicts. Using data from a 20+ year marine mammal observation program, we tested the hypothesis that the phenology of large whale habitat use in Cape Cod Bay has changed and is related to regional-scale shifts in the thermal onset of spring. We used a multi-season occupancy model to measure phenological shifts and evaluate trends in the date of peak habitat use for North Atlantic right (Eubalaena glacialis), humpback (Megaptera novaeangliae), and fin (Balaenoptera physalus) whales. The date of peak habitat use shifted by +18.1 days (0.90 days/year) for right whales and +19.1 days (0.96 days/year) for humpback whales. We then evaluated interannual variability in peak habitat use relative to thermal spring transition dates (STD), and hypothesized that right whales, as planktivorous specialist feeders, would exhibit a stronger response to thermal phenology than fin and humpback whales, which are more generalist piscivorous feeders. There was a significant negative effect of western region STD on right whale habitat use, and a significant positive effect of eastern region STD on fin whale habitat use indicating differential responses to spatial seasonal conditions. Protections for threatened and endangered whales have been designed to align with expected phenology of habitat use. Our results show that whales are becoming mismatched with static seasonal management measures through shifts in their timing of habitat use, and they suggest that effective management strategies may need to alter protections as species adapt to climate change.

Are we ready to track climate-driven shifts in marine species across international boundaries? - A global survey of scientific bottom trawl data.

Marine biota are redistributing at a rapid pace in response to climate change and shifting seascapes. While changes in fish populations and community structure threaten the sustainability of fisheries, our capacity to adapt by tracking and projecting marine species remains a challenge due to data discontinuities in biological observations, lack of data availability, and mismatch between data and real species distributions. To assess the extent of this challenge, we review the global status and accessibility of ongoing scientific bottom trawl surveys. In total, we gathered metadata for 283,925 samples from 95 surveys conducted regularly from 2001 to 2019. We identified that 59% of the metadata collected are not publicly available, highlighting that the availability of data is the most important challenge to assess species redistributions under global climate change. Given that the primary purpose of surveys is to provide independent data to inform stock assessment of commercially important populations, we further highlight that single surveys do not cover the full range of the main commercial demersal fish species. An average of 18 surveys is needed to cover at least 50% of species ranges, demonstrating the importance of combining multiple surveys to evaluate species range shifts. We assess the potential for combining surveys to track transboundary species redistributions and show that differences in sampling schemes and inconsistency in sampling can be overcome with spatio-temporal modeling to follow species density redistributions. In light of our global assessment, we establish a framework for improving the management and conservation of transboundary and migrating marine demersal species. We provide directions to improve data availability and encourage countries to share survey data, to assess species vulnerabilities, and to support management adaptation in a time of climate-driven ocean changes.

Reconciling fisheries catch and ocean productivity.

Photosynthesis fuels marine food webs, yet differences in fish catch across globally distributed marine ecosystems far exceed differences in net primary production (NPP). We consider the hypothesis that ecosystem-level variations in pelagic and benthic energy flows from phytoplankton to fish, trophic transfer efficiencies, and fishing effort can quantitatively reconcile this contrast in an energetically consistent manner. To test this hypothesis, we enlist global fish catch data that include previously neglected contributions from small-scale fisheries, a synthesis of global fishing effort, and plankton food web energy flux estimates from a prototype high-resolution global earth system model (ESM). After removing a small number of lightly fished ecosystems, stark interregional differences in fish catch per unit area can be explained (r = 0.79) with an energy-based model that (i) considers dynamic interregional differences in benthic and pelagic energy pathways connecting phytoplankton and fish, (ii) depresses trophic transfer efficiencies in the tropics and, less critically, (iii) associates elevated trophic transfer efficiencies with benthic-predominant systems. Model catch estimates are generally within a factor of 2 of values spanning two orders of magnitude. Climate change projections show that the same macroecological patterns explaining dramatic regional catch differences in the contemporary ocean amplify catch trends, producing changes that may exceed 50% in some regions by the end of the 21st century under high-emissions scenarios. Models failing to resolve these trophodynamic patterns may significantly underestimate regional fisheries catch trends and hinder adaptation to climate change.

Change in body size in a rapidly warming marine ecosystem: Consequences of tropicalization.

Climate change is profoundly affecting the physical environment and biota of the Northeast U.S. Continental Shelf ecosystem. To understand adaptations to climate change, in particular warming temperatures, we used bottom trawl survey data to describe the size of individual fish and macroinvertebrates. Using species distribution models to estimate abundance and biomass, we determined body size in weight for all modeled species. We demonstrate a tendency for increased abundance and biomass and a concomitant decline in body size over time. An analysis of length frequency data supports this assertion. There was no trend in the combined anthropogenic removals from the ecosystem, i.e. catches, suggesting a limited role of fisheries in influencing these changes. The changes in the fish and macroinvertebrate communities are consistent with the hypothesis of a tropicalization of this ecosystem, where the ecosystem experiences a change in diversity, abundance, biomass, and the size of individuals consistent with lower latitudes. The changes in how productivity is expressed in the ecosystem factors into how human populations relate to it; in a practical sense, change in body size will likely influence the strategies and efficiencies of harvest procedures and the industries built to support them.

Surface and subsurface oceanographic features drive forage fish distributions and aggregations: Implications for prey availability to top predators in the US Northeast Shelf ecosystem.

Forage fishes are a critical food web link in marine ecosystems, aggregating in a hierarchical patch structure over multiple spatial and temporal scales. Surface-level forage fish aggregations (FFAs) represent a concentrated source of prey available to surface- and shallow-foraging marine predators. Existing survey and analysis methods are often imperfect for studying forage fishes at scales appropriate to foraging predators, making it difficult to quantify predator-prey interactions. In many cases, general distributions of forage fish species are known; however, these may not represent surface-level prey availability to predators. Likewise, we lack an understanding of the oceanographic drivers of spatial patterns of prey aggregation and availability or forage fish community patterns. Specifically, we applied Bayesian joint species distribution models to bottom trawl survey data to assess species- and community-level forage fish distribution patterns across the US Northeast Continental Shelf (NES) ecosystem. Aerial digital surveys gathered data on surface FFAs at two project sites within the NES, which we used in a spatially explicit hierarchical Bayesian model to estimate the abundance and size of surface FFAs. We used these models to examine the oceanographic drivers of forage fish distributions and aggregations. Our results suggest that, in the NES, regions of high community species richness are spatially consistent with regions of high surface FFA abundance. Bathymetric depth drove both patterns, while subsurface features, such as mixed layer depth, primarily influenced aggregation behavior and surface features, such as sea surface temperature, sub-mesoscale eddies, and fronts influenced forage fish diversity. In combination, these models help quantify the availability of forage fishes to marine predators and represent a novel application of spatial models to aerial digital survey data.

Contrasting patterns in the occurrence and biomass centers of gravity among fish and macroinvertebrates in a continental shelf ecosystem.

The distribution of a group of fish and macroinvertebrates (n = 52) resident in the US Northeast Shelf large marine ecosystem were characterized with species distribution models (SDM), which in turn were used to estimate occurrence and biomass center of gravity (COG). The SDMs were fit using random forest machine learning and were informed with a range of physical and biological variables. The estimated probability of occurrence and biomass from the models provided the weightings to determine depth, distance to the coast, and along-shelf distance COG. The COGs of occupancy and biomass habitat tended to be separated by distances averaging 50 km, which approximates half of the minor axis of the subject ecosystem. During the study period (1978-2018), the biomass COG has tended to shift to further offshore positions whereas occupancy habitat has stayed at a regular spacing from the coastline. Both habitat types have shifted their along-shelf distances, indicating a general movement to higher latitude or to the Northeast for this ecosystem. However, biomass tended to occur at lower latitudes in the spring and higher latitude in the fall in a response to seasonal conditions. Distribution of habitat in relation to depth reveals a divergence in response with occupancy habitat shallowing over time and biomass habitat distributing in progressively deeper water. These results suggest that climate forced change in distribution will differentially affect occurrence and biomass of marine taxa, which will likely affect the organization of ecosystems and the manner in which human populations utilize marine resources.

A systematic review of spatial habitat associations and modeling of marine fish distribution: A guide to predictors, methods, and knowledge gaps.

As species distribution models, and similar techniques, have emerged in marine ecology, a vast array of predictor variables have been created and diverse methodologies have been applied. Marine fish are vital food resources worldwide, yet identifying the most suitable methodology and predictors to characterize spatial habitat associations, and the subsequent distributions, often remains ambiguous. Our objectives were to identify knowledge gaps in fish guilds, identify research themes, and to determine how data sources, statistics, and predictor variables differ among fish guilds. Data were obtained from an international literature search of peer-reviewed articles (2007-2018; n = 225) and research themes were determined based on abstracts. We tested for differences in data sources and modeling techniques using multinomial regressions and used a linear discriminant analysis to distinguish differences in predictors among fish guilds. Our results show predictive studies increased over time, but studies of forage fish, sharks, coral reef fish, and other fish guilds remain sparse. Research themes emphasized habitat suitability and distribution shifts, but also addressed abundance, occurrence, stock assessment, and biomass. Methodologies differed by fish guilds based on data limitations and research theme. The most frequent predictors overall were depth and temperature, but most fish guilds were distinguished by their own set of predictors that focused on their specific life history and ecology. A one-size-fits-all approach is not suitable for predicting marine fish distributions. However, given the paucity of studies for some fish guilds, researchers would benefit from utilizing predictors and methods derived from more commonly studied fish when similar habitat requirements are expected. Overall, the findings provide a guide for determining predictor variables to test and identifies novel opportunities to apply non-spatial knowledge and mechanisms to models.

Changes in higher trophic level productivity, diversity and niche space in a rapidly warming continental shelf ecosystem.

There is long-standing ecological and socioeconomic interest in what controls the diversity and productivity of ecosystems. That focus has intensified with shifting environmental conditions associated with accelerating climate change. The U.S. Northeast Shelf (NES) is a well-studied continental shelf marine ecosystem that is among the more rapidly warming marine systems worldwide. Furthermore, many constituent species have experienced significant distributional shifts. However, the system response of the NES to climate change goes beyond simple shifts in species distribution. The fish and macroinvertebrate communities of the NES have increased in species diversity and overall productivity in recent decades, despite no significant decline in fishing pressure. Species distribution models constructed using random forest classification and regression trees were fit for the dominant species in the system. Over time, the areal distribution of occupancy habitat has increased for approximately 80% of the modeled taxa, suggesting most species have significantly increased their range and niche space. These niche spaces were analyzed to determine the area of niche overlap between species pairs. For the vast majority of species pairs, interaction has increased over time suggesting greater niche overlap and the increased probability for more intense species interactions, such as between competitors or predators and prey. Furthermore, the species taxonomic composition and size structure indicate a potential tropicalization of the fish community. The system and community changes are consistent with the view that the NES may be transitioning from a cold temperate or boreal ecoregion to one more consistent with the composition of a warm temperate or Carolinian system.

Accelerated warming and emergent trends in fisheries biomass yields of the world's large marine ecosystems.

Information on the effects of global climate change on trends in global fisheries biomass yields has been limited in spatial and temporal scale. Results are presented of a global study of the impact of sea surface temperature (SST) changes over the last 25 years on the fisheries yields of 63 large marine ecosystems (LMEs) that annually produce 80% of the world's marine fisheries catches. Warming trends were observed in 61 LMEs around the globe. In 18 of the LMEs, rates of SST warming were two to four times faster during the past 25 years than the globally averaged rates of SST warming reported by the Intergovernmental Panel on Climate Change in 2007. Effects of warming on fisheries biomass yields were greatest in the fast-warming northern Northeast Atlantic LMEs, where increasing trends in fisheries biomass yields were related to zooplankton biomass increases. In contrast, fisheries biomass yields of LMEs in the fast-warming, more southerly reaches of the Northeast Atlantic were declining in response to decreases in zooplankton abundance. The LMEs around the margins of the Indian Ocean, where SSTs were among the world's slowest warming, revealed a consistent pattern of fisheries biomass increases during the past 25 years, driven principally by human need for food security from fisheries resources. As a precautionary approach toward more sustainable fisheries utilization, management measures to limit the total allowable catch through a cap-and-sustain approach are suggested for the developing nations recently fishing heavily on resources of the Agulhas Current, Somali Current, Arabian Sea, and Bay of Bengal LMEs.

It's about time: A synthesis of changing phenology in the Gulf of Maine ecosystem.

The timing of recurring biological and seasonal environmental events is changing on a global scale relative to temperature and other climate drivers. This study considers the Gulf of Maine ecosystem, a region of high social and ecological importance in the Northwest Atlantic Ocean and synthesizes current knowledge of (a) key seasonal processes, patterns, and events; (b) direct evidence for shifts in timing; (c) implications of phenological responses for linked ecological-human systems; and (d) potential phenology-focused adaptation strategies and actions. Twenty studies demonstrated shifts in timing of regional marine organisms and seasonal environmental events. The most common response was earlier timing, observed in spring onset, spring and winter hydrology, zooplankton abundance, occurrence of several larval fishes, and diadromous fish migrations. Later timing was documented for fall onset, reproduction and fledging in Atlantic puffins, spring and fall phytoplankton blooms, and occurrence of additional larval fishes. Changes in event duration generally increased and were detected in zooplankton peak abundance, early life history periods of macro-invertebrates, and lobster fishery landings. Reduced duration was observed in winter-spring ice-affected stream flows. Two studies projected phenological changes, both finding diapause duration would decrease in zooplankton under future climate scenarios. Phenological responses were species-specific and varied depending on the environmental driver, spatial, and temporal scales evaluated. Overall, a wide range of baseline phenology and relevant modeling studies exist, yet surprisingly few document long-term shifts. Results reveal a need for increased emphasis on phenological shifts in the Gulf of Maine and identify opportunities for future research and consideration of phenological changes in adaptation efforts.

Lake Ontario salmon (Salmo salar) were not migratory: A long-standing historical debate solved through stable isotope analysis.

Lake Ontario once supported a large complex of Atlantic Salmon (Salmo salar) populations that became extinct prior to scientific study. Since the 1860s, research efforts to conserve and reintroduce a sustainable population of Atlantic Salmon have focused on determining whether Lake Ontario's original salmon populations had migrated to the Atlantic Ocean as part of their lifecycle (anadromy), stayed in the lake year-round (potamodromy), or both. We used stable carbon, nitrogen, and sulfur isotope analyses of archaeological bones and historical museum-archived salmon scales to show that the original salmon populations from Lake Ontario completed their entire lifecycle without migrating to the Atlantic Ocean. With a time depth of more than 500 years, our findings provide a unique baseline with significant potential for informing modern restocking and conservation efforts.

Quantifying patterns of change in marine ecosystem response to multiple pressures.

The ability to understand and ultimately predict ecosystem response to multiple pressures is paramount to successfully implement ecosystem-based management. Thresholds shifts and nonlinear patterns in ecosystem responses can be used to determine reference points that identify levels of a pressure that may drastically alter ecosystem status, which can inform management action. However, quantifying ecosystem reference points has proven elusive due in large part to the multi-dimensional nature of both ecosystem pressures and ecosystem responses. We used ecological indicators, synthetic measures of ecosystem status and functioning, to enumerate important ecosystem attributes and to reduce the complexity of the Northeast Shelf Large Marine Ecosystem (NES LME). Random forests were used to quantify the importance of four environmental and four anthropogenic pressure variables to the value of ecological indicators, and to quantify shifts in aggregate ecological indicator response along pressure gradients. Anthropogenic pressure variables were critical defining features and were able to predict an average of 8-13% (up to 25-66% for individual ecological indicators) of the variation in ecological indicator values, whereas environmental pressures were able to predict an average of 1-5 % (up to 9-26% for individual ecological indicators) of ecological indicator variation. Each pressure variable predicted a different suite of ecological indicator's variation and the shapes of ecological indicator responses along pressure gradients were generally nonlinear. Threshold shifts in ecosystem response to exploitation, the most important pressure variable, occurred when commercial landings were 20 and 60% of total surveyed biomass. Although present, threshold shifts in ecosystem response to environmental pressures were much less important, which suggests that anthropogenic pressures have significantly altered the ecosystem structure and functioning of the NES LME. Gradient response curves provide ecologically informed transformations of pressure variables to explain patterns of ecosystem structure and functioning. By concurrently identifying thresholds for a suite of ecological indicator responses to multiple pressures, we demonstrate that ecosystem reference points can be evaluated and used to support ecosystem-based management.

Pathways between primary production and fisheries yields of large marine ecosystems.

The shift in marine resource management from a compartmentalized approach of dealing with resources on a species basis to an approach based on management of spatially defined ecosystems requires an accurate accounting of energy flow. The flow of energy from primary production through the food web will ultimately limit upper trophic-level fishery yields. In this work, we examine the relationship between yield and several metrics including net primary production, chlorophyll concentration, particle-export ratio, and the ratio of secondary to primary production. We also evaluate the relationship between yield and two additional rate measures that describe the export of energy from the pelagic food web, particle export flux and mesozooplankton productivity. We found primary production is a poor predictor of global fishery yields for a sample of 52 large marine ecosystems. However, chlorophyll concentration, particle-export ratio, and the ratio of secondary to primary production were positively associated with yields. The latter two measures provide greater mechanistic insight into factors controlling fishery production than chlorophyll concentration alone. Particle export flux and mesozooplankton productivity were also significantly related to yield on a global basis. Collectively, our analyses suggest that factors related to the export of energy from pelagic food webs are critical to defining patterns of fishery yields. Such trophic patterns are associated with temperature and latitude and hence greater yields are associated with colder, high latitude ecosystems.

Sieving functional morphology of the gill raker feeding apparatus of atlantic menhaden.

Menhaden occupy an important position in estuarine food webs, thus the rate processes associated with their feeding are critical to the ecosystem management of fishery and ecological resources. Atlantic menhaden feed on a wide range of plankton, the size and food quality of which change ontogenetically. We analyzed the functional morphology of the menhaden feeding apparatus in a size series of menhaden representative of juveniles and the adult migratory stock. The physical dimensions of gill arches and rakers increased isometrically with fish length; however, branchiospinule spacing, the dimension that forms the sieve apertures of the branchial basket, scaled allometrically with fish length. Juvenile menhaden from North Carolina have branchiospinule spacings that averaged 12 microm, with three arch subsections of average spacing < 10 microm. Spacings did not increase with juvenile growth until the first allometric inflection point at approximately 100 mm fork length (FL). Spacing data for juveniles from other locations suggests spacing increases with latitude. Spacings increase with fish length in adults until a second inflection at 200 mm FL, after which spacing averages 37 microm. These data suggest menhaden juveniles filter smaller plankton with higher filtration efficiency than previously considered and that regional recruitment may affect adult distribution through foraging preferences.