Reconstructing marine plankton food web interactions using DNA metabarcoding

Knowledge of zooplankton in situ diet is critical for accurate assessment of marine ecosystem function and structure, but due to methodological constraints, there is still a limited understanding of ecological networks in marine ecosystems. Here, we used DNA‐metabarcoding to study trophic interactions, with the aim to unveil the natural diet of zooplankton species under temporal variation of food resources. Several target consumers, including copepods and cladocerans, were investigated by sequencing 16S rRNA and 18S rRNA genes to identify prokaryote and eukaryote potential prey present in their guts. During the spring phytoplankton bloom, we found a dominance of diatom and dinoflagellate trophic links to copepods. During the summer period, zooplankton including cladocerans showed a more diverse diet dominated by cyanobacteria and heterotrophic prey. Our study suggests that copepods present trophic plasticity, changing their natural diet over seasons, and adapting their feeding strategies to the available prey spectrum, with some species being more selective. We did not find a large overlap of prey consumed by copepods and cladocerans, based on prey diversity found in their guts, suggesting that they occupy different roles in the trophic web. This study represents the first molecular approach to investigate several zooplankton–prey associations under seasonal variation, and highlights how, unlike other techniques, the diversity coverage is high when using DNA, allowing the possibility to detect a wide range of trophic interactions in plankton communities.     

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014–2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.     

Climate and productivity shape fish and invertebrate community structure in subarctic lakes

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Climate change disrupts core habitats of marine species

Driven by climate change, marine biodiversity is undergoing a phase of rapid change that has proven to be even faster than changes observed in terrestrial ecosystems. Understanding how these changes in species composition will affect future marine life is crucial for conservation management, especially due to increasing demands for marine natural resources. Here, we analyse predictions of a multiparameter habitat suitability model covering the global projected ranges of >33,500 marine species from climate model projections under three CO₂ emission scenarios (RCP2.6, RCP4.5, RCP8.5) up to the year 2100. Our results show that the core habitat area will decline for many species, resulting in a net loss of 50% of the core habitat area for almost half of all marine species in 2100 under the high-emission scenario RCP8.5. As an additional consequence of the continuing distributional reorganization of marine life, gaps around the equator will appear for 8% (RCP2.6), 24% (RCP4.5), and 88% (RCP8.5) of marine species with cross-equatorial ranges. For many more species, continuous distributional ranges will be disrupted, thus reducing effective population size. In addition, high invasion rates in higher latitudes and polar regions will lead to substantial changes in the ecosystem and food web structure, particularly regarding the introduction of new predators. Overall, our study highlights that the degree of spatial and structural reorganization of marine life with ensued consequences for ecosystem functionality and conservation efforts will critically depend on the realized greenhouse gas emission pathway.     

Climate change alters stability and species potential interactions in a large marine ecosystem

We have little empirical evidence of how large‐scale overlaps between large numbers of marine species may have altered in response to human impacts. Here, we synthesized all available distribution data (>1 million records) since 1992 for 61 species of the East Australian marine ecosystem, a global hot spot of ocean warming and continuing fisheries exploitation. Using a novel approach, we constructed networks of the annual changes in geographical overlaps between species. Using indices of changes in species overlap, we quantified changes in the ecosystem stability, species robustness, species sensitivity and structural keystone species. We then compared the species overlap indices with environmental and fisheries data to identify potential factors leading to the changes in distributional overlaps between species. We found that the structure of the ecosystem has changed with a decrease in asymmetrical geographical overlaps between species. This suggests that the ecosystem has become less stable and potentially more susceptible to environmental perturbations. Most species have shown a decrease in overlaps with other species. The greatest decrease in species overlap robustness and sensitivity to the loss of other species has occurred in the pelagic community. Some demersal species have become more robust and less sensitive. Pelagic structural keystone species, predominately the tunas and billfish, have been replaced by demersal fish species. The changes in species overlap were strongly correlated with regional oceanographic changes, in particular increasing ocean warming and the southward transport of warmer and saltier water with the East Australian Current, but less correlated with fisheries catch. Our study illustrates how large‐scale multispecies distribution changes can help identify structural changes in marine ecosystems associated with climate change.     

Rapid biogeographical plankton shifts in the North Atlantic Ocean

Large‐scale biogeographical changes in the biodiversity of a key zooplankton group (calanoid copepods) were detected in the north‐eastern part of the North Atlantic Ocean and its adjacent seas over the period 1960–1999. These findings provided key empirical evidence for climate change impacts on marine ecosystems at the regional to oceanic scale. Since 1999, global temperatures have continued to rise in the region. Here, we extend the analysis to the period 1958–2005 using all calanoid copepod species assemblages (nine species assemblages based on an analysis including a total of 108 calanoid species or taxa) and show that this phenomenon has been reinforced in all regions. Our study reveals that the biodiversity of calanoid copepods are responding quickly to sea surface temperature (SST) rise by moving geographically northward at a rapid rate up to about 23.16 km yr^?1. Our analysis suggests that nearly half of the increase in sea temperature in the northeast Atlantic and adjacent seas is related to global temperature rises (46.35% of the total variance of temperature) while changes in both natural modes of atmospheric and oceanic circulation explain 26.45% of the total variance of temperature. Although some SST isotherms have moved northwards by an average rate of up to 21.75 km yr^?1 (e.g. the North Sea), their movement cannot fully quantify all species assemblage shifts. Furthermore, the observed rates of biogeographical movements are far greater than those observed in the terrestrial realm. Here, we discuss the processes that may explain such a discrepancy and suggest that the differences are mainly explained by the fluid nature of the pelagic domain, the life cycle of the zooplankton and the lesser anthropogenic influence (e.g. exploitation, habitat fragmentation) on these organisms. We also hypothesize that despite changes in the path and intensity of the oceanic currents that may modify quickly and greatly pelagic zooplankton species, these organisms may reflect better the current impact of climate warming on ecosystems as terrestrial organisms are likely to significantly lag the current impact of climate change.     

Projecting marine species range shifts from only temperature can mask climate vulnerability

Climate change is causing range shifts in many marine species, with implications for biodiversity and fisheries. Previous research has mainly focused on how species' ranges will respond to changing ocean temperatures, without accounting for other environmental covariates that could affect future distribution patterns. Here, we integrate habitat suitability modeling approaches, a high‐resolution global climate model projection, and detailed fishery‐independent and ‐dependent faunal datasets from one of the most extensively monitored marine ecosystems—the U.S. Northeast Shelf. We project the responses of 125 species in this region to climate‐driven changes in multiple oceanographic factors (e.g., ocean temperature, salinity, sea surface height) and seabed characteristics (i.e., rugosity and depth). Comparing model outputs based on ocean temperature and seabed characteristics to those that also incorporated salinity and sea surface height (proxies for primary productivity and ocean circulation features), we explored how an emphasis on ocean temperature in projecting species' range shifts can impact assessments of species' climate vulnerability. We found that multifactor habitat suitability models performed better in explaining and predicting species historical distribution patterns than temperature‐based models. We also found that multifactor models provided more concerning assessments of species' future distribution patterns than temperature‐based models, projecting that species' ranges will largely shift northward and become more contracted and fragmented over time. Our results suggest that using ocean temperature as a primary determinant of range shifts can significantly alter projections, masking species' climate vulnerability, and potentially forestalling proactive management.     

Lifeform indicators reveal large‐scale shifts in plankton across the North‐West European shelf

Increasing direct human pressures on the marine environment, coupled with climate‐driven changes, is a concern to marine ecosystems globally. This requires the development and monitoring of ecosystem indicators for effective management and adaptation planning. Plankton lifeforms (broad functional groups) are sensitive indicators of marine environmental change and can provide a simplified view of plankton biodiversity, building an understanding of change in lower trophic levels. Here, we visualize regional‐scale multi‐decadal trends in six key plankton lifeforms as well as their correlative relationships with sea surface temperature (SST). For the first time, we collate trends across multiple disparate surveys, comparing the spatially and temporally extensive Continuous Plankton Recorder (CPR) survey (offshore) with multiple long‐term fixed station‐based time‐series (inshore) from around the UK coastline. These analyses of plankton lifeforms showed profound long‐term changes, which were coherent across large spatial scales. For example, ‘diatom’ and ‘meroplankton’ lifeforms showed strong alignment between surveys and coherent regional‐scale trends, with the 1998–2017 decadal average abundance of meroplankton being 2.3 times that of 1958–1967 for CPR samples in the North Sea. This major, shelf‐wide increase in meroplankton correlated with increasing SSTs, and contrasted with a general decrease in holoplankton (dominated by small copepods), indicating a changing balance of benthic and pelagic fauna. Likewise, inshore‐offshore gradients in dinoflagellate trends, with contemporary increases inshore contrasting with multi‐decadal decreases offshore (approx. 75% lower decadal mean abundance), urgently require the identification of causal mechanisms. Our lifeform approach allows the collation of many different data types and time‐series across the NW European shelf, providing a crucial evidence base for informing ecosystem‐based management, and the development of regional adaptation plans.     

High evolutionary potential of marine zooplankton

Open ocean zooplankton often have been viewed as slowly evolving species that have limited capacity to respond adaptively to changing ocean conditions. Hence, attention has focused on the ecological responses of zooplankton to current global change, including range shifts and changing phenology. Here, we argue that zooplankton also are well poised for evolutionary responses to global change. We present theoretical arguments that suggest plankton species may respond rapidly to selection on mildly beneficial mutations due to exceptionally large population size, and consider the circumstantial evidence that supports our inference that selection may be particularly important for these species. We also review all primary population genetic studies of open ocean zooplankton and show that genetic isolation can be achieved at the scale of gyre systems in open ocean habitats (100s to 1000s of km). Furthermore, population genetic structure often varies across planktonic taxa, and appears to be linked to the particular ecological requirements of the organism. In combination, these characteristics should facilitate adaptive evolution to distinct oceanographic habitats in the plankton. We conclude that marine zooplankton may be capable of rapid evolutionary as well as ecological responses to changing ocean conditions, and discuss the implications of this view. We further suggest two priority areas for future research to test our hypothesis of high evolutionary potential in open ocean zooplankton, which will require (1) assessing how pervasive selection is in driving population divergence and (2) rigorously quantifying the spatial and temporal scales of population differentiation in the open ocean.     

UV effects that come and go: a global comparison of marine benthic community level impacts

Ambient UV radiation has substantially increased during the last decades, but its impact on marine benthic communities is hardly known. The aim of this study was to globally compare and quantify how shallow hard‐bottom communities are affected by UV during early succession. Identical field experiments in 10 different coastal regions of both hemispheres produced a consistent but unexpected pattern: (i) UV radiation affected species diversity and community biomass in a very similar manner, (ii) diversity and biomass were reduced to a larger extent by UVA than UVB radiation, (iii) ambient UV levels did not affect the composition of the communities, and (iv) any UV effects disappeared during species succession after 2–3 months. Thus, current levels of UV radiation seem to have small, predictable, and transient effects on shallow marine hard‐bottom communities.     

Response of marine communities to local temperature changes

As global climate change and variability drive shifts in species’ distributions, ecological communities are being reorganized. One approach to understand community change in response to climate change has been to characterize communities by a collective thermal preference, or community temperature index (CTI), and then to compare changes in CTI with changes in temperature. However, important questions remain about whether and how responsive communities are to changes in their local thermal environments. We used CTI to analyze changes in 160 marine assemblages (fish and invertebrates) across the rapidly‐changing Northeast U.S. Continental Shelf Large Marine Ecosystem and calculated expected community change based on historical relationships between species presence and temperature from a separate training dataset. We then compared interannual and long‐term temperature changes with expected community responses and observed community responses over both temporal scales. For these marine communities, we found that community composition as well as composition changes through time could be explained by species associations with bottom temperature. Individual species had non‐linear responses to changes in temperature, and these nonlinearities scaled up to a nonlinear relationship between CTI and temperature. On average, CTI increased by 0.36°C (95% CI: 0.34–0.38°C) for every 1°C increase in bottom temperature, but the relationship between CTI and temperature also depended on community composition. In addition, communities responded more strongly to interannual variation than to long‐term trends in temperature. We recommend that future research into climate‐driven community change accounts for nonlinear responses and examines ecological responses across a range of temporal and geographical scales.     

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.     

Linking macroecology and community ecology: refining predictions of species distributions using biotic interaction networks

Macroecological models for predicting species distributions usually only include abiotic environmental conditions as explanatory variables, despite knowledge from community ecology that all species are linked to other species through biotic interactions. This disconnect is largely due to the different spatial scales considered by the two sub‐disciplines: macroecologists study patterns at large extents and coarse resolutions, while community ecologists focus on small extents and fine resolutions. A general framework for including biotic interactions in macroecological models would help bridge this divide, as it would allow for rigorous testing of the role that biotic interactions play in determining species ranges. Here, we present an approach that combines species distribution models with Bayesian networks, which enables the direct and indirect effects of biotic interactions to be modelled as propagating conditional dependencies among species’ presences. We show that including biotic interactions in distribution models for species from a California grassland community results in better range predictions across the western USA. This new approach will be important for improving estimates of species distributions and their dynamics under environmental change.     

Natural acidification changes the timing and rate of succession,alters community structure,and increases homogeneity in marine biofouling communities

Ocean acidification may have far‐reaching consequences for marine community and ecosystem dynamics, but its full impacts remain poorly understood due to the difficulty of manipulating pCO₂ at the ecosystem level to mimic realistic fluctuations that occur on a number of different timescales. It is especially unclear how quickly communities at various stages of development respond to intermediate‐scale pCO₂ change and, if high pCO₂ is relieved mid‐succession, whether past acidification effects persist, are reversed by alleviation of pCO₂ stress, or are worsened by departures from prior high pCO₂ conditions to which organisms had acclimatized. Here, we used reciprocal transplant experiments along a shallow water volcanic pCO₂ gradient to assess the importance of the timing and duration of high pCO₂ exposure (i.e., discrete events at different stages of successional development vs. continuous exposure) on patterns of colonization and succession in a benthic fouling community. We show that succession at the acidified site was initially delayed (less community change by 8 weeks) but then caught up over the next 4 weeks. These changes in succession led to homogenization of communities maintained in or transplanted to acidified conditions, and altered community structure in ways that reflected both short‐ and longer‐term acidification history. These community shifts are likely a result of interspecific variability in response to increased pCO₂ and changes in species interactions. High pCO₂ altered biofilm development, allowing serpulids to do best at the acidified site by the end of the experiment, although early (pretransplant) negative effects of pCO₂ on recruitment of these worms were still detectable. The ascidians Diplosoma sp. and Botryllus sp. settled later and were more tolerant to acidification. Overall, transient and persistent acidification‐driven changes in the biofouling community, via both past and more recent exposure, could have important implications for ecosystem function and food web dynamics.     

Long-term changes in metapopulation genetic structure: a quarter-century retrospective study on low-Arctic rock pool Daphnia

Population genetic surveys approximately 25 years apart examined the distribution and abundance of asexual clones of the freshwater zooplankter Daphnia pulex complex in rock pools near Churchill, Manitoba, Canada. In 1984–1985, melanic members of this species complex were present in 131 rock pools at this site, but were only detected in 90 of these pools in 2007–2008. Allozymic surveys conducted during these two time periods revealed that 59 per cent of these populations showed unchanged clonal composition. Total clonal replacement occurred in 8 per cent of the populations, while the others (33%) included a mixture of ‘resident’ clones and new ‘colonists’. We discuss these changes in light of shifts in biotic and abiotic factors. We also discuss the use of rock pool habitats as ‘sentinel’ systems for examining long-term environmental changes in the ecological genetics of aquatic organisms in the Arctic.     

Regime shifts in exploited marine food webs: detecting mechanisms underlying alternative stable states using size-structured community dynamics theory

Many marine ecosystems have undergone ‘regime shifts’, i.e. abrupt reorganizations across trophic levels. Establishing whether these constitute shifts between alternative stable states is of key importance for the prospects of ecosystem recovery and for management. We show how mechanisms underlying alternative stable states caused by predator–prey interactions can be revealed in field data, using analyses guided by theory on size-structured community dynamics. This is done by combining data on individual performance (such as growth and fecundity) with information on population size and prey availability. We use Atlantic cod (Gadus morhua) and their prey in the Baltic Sea as an example to discuss and distinguish two types of mechanisms, ‘cultivation-depensation’ and ‘overcompensation’, that can cause alternative stable states preventing the recovery of overexploited piscivorous fish populations. Importantly, the type of mechanism can be inferred already from changes in the predators'' body growth in different life stages. Our approach can thus be readily applied to monitored stocks of piscivorous fish species, for which this information often can be assembled. Using this tool can help resolve the causes of catastrophic collapses in marine predatory–prey systems and guide fisheries managers on how to successfully restore collapsed piscivorous fish stocks.     

Risks of ocean acidification in the California Current food web and fisheries: ecosystem model projections

The benefits and ecosystem services that humans derive from the oceans are threatened by numerous global change stressors, one of which is ocean acidification. Here, we describe the effects of ocean acidification on an upwelling system that already experiences inherently low pH conditions, the California Current. We used an end‐to‐end ecosystem model (Atlantis), forced by downscaled global climate models and informed by a meta‐analysis of the pH sensitivities of local taxa, to investigate the direct and indirect effects of future pH on biomass and fisheries revenues. Our model projects a 0.2‐unit drop in pH during the summer upwelling season from 2013 to 2063, which results in wide‐ranging magnitudes of effects across guilds and functional groups. The most dramatic direct effects of future pH may be expected on epibenthic invertebrates (crabs, shrimps, benthic grazers, benthic detritivores, bivalves), and strong indirect effects expected on some demersal fish, sharks, and epibenthic invertebrates (Dungeness crab) because they consume species known to be sensitive to changing pH. The model's pelagic community, including marine mammals and seabirds, was much less influenced by future pH. Some functional groups were less affected to changing pH in the model than might be expected from experimental studies in the empirical literature due to high population productivity (e.g., copepods, pteropods). Model results suggest strong effects of reduced pH on nearshore state‐managed invertebrate fisheries, but modest effects on the groundfish fishery because individual groundfish species exhibited diverse responses to changing pH. Our results provide a set of projections that generally support and build upon previous findings and set the stage for hypotheses to guide future modeling and experimental analysis on the effects of OA on marine ecosystems and fisheries.     

Climate change undermines the global functioning of marine food webs

Sea water temperature affects all biological and ecological processes that ultimately impact ecosystem functioning. In this study, we examine the influence of temperature on global biomass transfers from marine secondary production to fish stocks. By combining fisheries catches in all coastal ocean areas and life‐history traits of exploited marine species, we provide global estimates of two trophic transfer parameters which determine biomass flows in coastal marine food web: the trophic transfer efficiency (TTE) and the biomass residence time (BRT) in the food web. We find that biomass transfers in tropical ecosystems are less efficient and faster than in areas with cooler waters. In contrast, biomass transfers through the food web became faster and more efficient between 1950 and 2010. Using simulated changes in sea water temperature from three Earth system models, we project that the mean TTE in coastal waters would decrease from 7.7% to 7.2% between 2010 and 2100 under the ‘no effective mitigation’ representative concentration pathway (RCP8.5), while BRT between trophic levels 2 and 4 is projected to decrease from 2.7 to 2.3 years on average. Beyond the global trends, we show that the TTEs and BRTs may vary substantially among ecosystem types and that the polar ecosystems may be the most impacted ecosystems. The detected and projected changes in mean TTE and BRT will undermine food web functioning. Our study provides quantitative understanding of temperature effects on trophodynamic of marine ecosystems under climate change.