Monitoring and modelling marine zooplankton in a changing climate.

Zooplankton are major consumers of phytoplankton primary production in marine ecosystems. As such, they represent a critical link for energy and matter transfer between phytoplankton and bacterioplankton to higher trophic levels and play an important role in global biogeochemical cycles. In this Review, we discuss key responses of zooplankton to ocean warming, including shifts in phenology, range, and body size, and assess the implications to the biological carbon pump and interactions with higher trophic levels. Our synthesis highlights key knowledge gaps and geographic gaps in monitoring coverage that need to be urgently addressed. We also discuss an integrated sampling approach that combines traditional and novel techniques to improve zooplankton observation for the benefit of monitoring zooplankton populations and modelling future scenarios under global changes.

Historical biomonitoring of pollution trends in the North Pacific using archived samples from the Continuous Plankton Recorder Survey.

First started in 1931, the Continuous Plankton Recorder (CPR) Survey is the longest-running and most geographically extensive marine plankton sampling program in the world. This pilot study investigates the feasibility of biomonitoring the spatiotemporal trends of marine pollution using archived CPR samples from the North Pacific. We selected specimens collected from three different locations (British Columbia Shelf, Northern Gulf of Alaska, and Aleutian Shelf) in the North Pacific between 2002 and 2020. Comprehensive profiling of the plankton chemical exposome was conducted using liquid and gas chromatography coupled with tandem mass spectrometry (LC-MS/MS and GC-MS/MS). Our results show that phthalates, plasticizers, persistent organic pollutants (POPs), pesticides, pharmaceuticals, and personal care products were present in the plankton exposome, and that many of these pollutants have decreased in amount over the last two decades, which was most pronounced for tri-n-butyl phosphate. In addition, the plankton exposome differed significantly by regional human activities, with the most polluted samples coming from the nearshore area. Exposome-wide association analysis revealed that bioaccumulation of environmental pollutants was highly correlated with the biomass of different plankton taxa. Overall, this study demonstrates that exposomic analysis of archived samples from the CPR Survey is effective for long-term biomonitoring of the spatial and temporal trends of environmental pollutants in the marine environment.

Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Heatwave-induced synchrony within forage fish portfolio disrupts energy flow to top pelagic predators.

During the Pacific marine heatwave of 2014-2016, abundance and quality of several key forage fish species in the Gulf of Alaska were simultaneously reduced throughout the system. Capelin (Mallotus catervarius), sand lance (Ammodytes personatus), and herring (Clupea pallasii) populations were at historically low levels, and within this community abrupt declines in portfolio effects identify trophic instability at the onset of the heatwave. Although compensatory changes in age structure, size, growth or energy content of forage fish were observed to varying degrees among all these forage fish, none were able to fully mitigate adverse impacts of the heatwave, which likely included both top-down and bottom-up forcing. Notably, changes to the demographic structure of forage fish suggested size-selective removals typical of top-down regulation. At the same time, changes in zooplankton communities may have driven bottom-up regulation as copepod community structure shifted toward smaller, warm water species, and euphausiid biomass was reduced owing to the loss of cold-water species. Mediated by these impacts on the forage fish community, an unprecedented disruption of the normal pelagic food web was signaled by higher trophic level disruptions during 2015-2016, when seabirds, marine mammals, and groundfish experienced shifts in distribution, mass mortalities, and reproductive failures. Unlike decadal-scale variability underlying ecosystem regime shifts, the heatwave appeared to temporarily overwhelm the ability of the forage fish community to buffer against changes imposed by warm water anomalies, thereby eliminating any ecological advantages that may have accrued from having a suite of coexisting forage species with differing life-history compensations.

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.

Zooplankton monitoring to contribute towards addressing global biodiversity conservation challenges.

Oceanographers have an increasing responsibility to ensure that the outcomes of scientific research are conveyed to the policy-making sphere to achieve conservation and sustainable use of marine biodiversity. Zooplankton monitoring projects have helped to increase our understanding of the processes by which marine ecosystems respond to climate change and other environmental variations, ranging from regional to global scales, and its scientific value is recognized in the contexts of fisheries, biodiversity and global change studies. Nevertheless, zooplankton data have rarely been used at policy level for conservation and management of marine ecosystems services. One way that this can be pragmatically and effectively achieved is via the development of zooplankton indicators, which could for instance contribute to filling in gaps in the suite of global indicators to track progress against the Aichi Biodiversity Targets of the United Nations Strategic Plan for Biodiversity 2010-2020. This article begins by highlighting how under-represented the marine realm is within the current suite of global Aichi Target indicators. We then examine the potential to develop global indicators for relevant Aichi Targets, using existing zooplankton monitoring data, to address global biodiversity conservation challenges.

Essential ocean variables for global sustained observations of biodiversity and ecosystem changes.

Sustained observations of marine biodiversity and ecosystems focused on specific conservation and management problems are needed around the world to effectively mitigate or manage changes resulting from anthropogenic pressures. These observations, while complex and expensive, are required by the international scientific, governance and policy communities to provide baselines against which the effects of human pressures and climate change may be measured and reported, and resources allocated to implement solutions. To identify biological and ecological essential ocean variables (EOVs) for implementation within a global ocean observing system that is relevant for science, informs society, and technologically feasible, we used a driver-pressure-state-impact-response (DPSIR) model. We (1) examined relevant international agreements to identify societal drivers and pressures on marine resources and ecosystems, (2) evaluated the temporal and spatial scales of variables measured by 100+ observing programs, and (3) analysed the impact and scalability of these variables and how they contribute to address societal and scientific issues. EOVs were related to the status of ecosystem components (phytoplankton and zooplankton biomass and diversity, and abundance and distribution of fish, marine turtles, birds and mammals), and to the extent and health of ecosystems (cover and composition of hard coral, seagrass, mangrove and macroalgal canopy). Benthic invertebrate abundance and distribution and microbe diversity and biomass were identified as emerging EOVs to be developed based on emerging requirements and new technologies. The temporal scale at which any shifts in biological systems will be detected will vary across the EOVs, the properties being monitored and the length of the existing time-series. Global implementation to deliver useful products will require collaboration of the scientific and policy sectors and a significant commitment to improve human and infrastructure capacity across the globe, including the development of new, more automated observing technologies, and encouraging the application of international standards and best practices.

Temperature and zooplankton size structure: climate control and basin-scale comparison in the North Pacific.

The global distribution of zooplankton community structure is known to follow latitudinal temperature gradients: larger species in cooler, higher latitudinal regions. However, interspecific relationships between temperature and size in zooplankton communities have not been fully examined in terms of temporal variation. To re-examine the relationship on a temporal scale and the effects of climate control thereon, we investigated the variation in copepod size structure in the eastern and western subarctic North Pacific in 2000-2011. This report presents the first basin-scale comparison of zooplankton community changes in the North Pacific based on a fully standardized data set obtained from the Continuous Plankton Recorder (CPR) survey. We found an increase in copepod community size (CCS) after 2006-2007 in the both regions because of the increased dominance of large cold-water species. Sea surface temperature varied in an east-west dipole manner, showing the typical Pacific Decadal Oscillation pattern: cooling in the east and warming in the west after 2006-2007. The observed positive correlation between CCS and sea surface temperature in the western North Pacific was inconsistent with the conventional interspecific temperature-size relationship. We explained this discrepancy by the geographical shift of the upper boundary of the thermal niche, the 9°C isotherm, of large cold-water species. In the eastern North Pacific, the boundary stretched northeast, to cover a large part of the sampling area after 2006-2007. In contrast, in the western North Pacific, the isotherm location hardly changed and the sampling area remained within its thermal niche throughout the study period, despite the warming that occurred. Our study suggests that while a climate-induced basin-scale cool-warm cycle can alter copepod community size and might subsequently impact the functions of the marine ecosystem in the North Pacific, the interspecific temperature-size relationship is not invariant and that understanding region-specific processes linking climate and ecosystem is indispensable.