Physiological and nutritional constraints on zooplankton productivity due to eutrophication and climate change predicted using a resource-based modeling approach

Emerging evidence suggests that zooplankton production is affected by physiological and nutritional constraints due to climate change and eutrophication, which in turn could have broad implications for food-web dynamics and fisheries production. In this study, we developed a resource-based zooplankton production dynamics model that causally links freshwater cladoceran and copepod daily production-to-biomass (P/B) ratios with water temperature, phytoplankton biomass and community composition, and zooplankton feeding selectivity. This model was used to evaluate constraints on zooplankton growth under four hypothetical scenarios: involving natural plankton community seasonal succession; lake fertilization to enhance fisheries production; eutrophication; and climatic warming. Our novel modeling approach predicts zooplankton production is strongly dependent on seasonal variation in resource availability and quality, which results in more complex zooplankton dynamics than predicted by simpler temperature dependent models. For mesotrophic and hypereutrophic lakes, our study suggests that the ultimate control over zooplankton P/B ratios shifts from physiological control during colder periods to strong resource control during warmer periods. Our resource-based model provided important insights into the nature of biophysical control of zooplankton under a changing climate that has crucial implications for food web energy transfer and fisheries production.

Zooplankton Biomass Depletion Event Reveals the Importance of Small Pelagic Fish Top-Down Control in the Western Mediterranean Coastal Waters

The influence of hydrochemistry and trophic conditions on the coastal zooplankton community’s biomass and metabolic activities was investigated along the Spanish Mediterranean coastal waters, from Algeciras Bay to Barcelona, from autumn 2011 to autumn 2012. Two hydrographic regions were differentiated: NW Alboran (ALB) and W Mediterranean (MED). Zooplankton metabolism was assessed from measurements of the electron transport system (ETS) and aminoacyl-tRNA synthetases (AARS) activities, as proxies for potential respiration and somatic growth, respectively. Zooplankton showed three to fivefold higher biomass in ALB than in MED during autumn 2011 and spring 2012. However, in autumn 2012, a drastic decrease in biomass standing stock was observed in ALB, with no significant differences between the two regions. This biomass depletion event was not associated with environmental variables, food availability or zooplankton metabolic rates, but coincided with a twofold peak of Sardina pilchardus landings in ALB. A reduced standing stock coupled with high zooplankton growth rates suggests mortality by predation as the main cause for the low zooplankton biomass typically observed in MED, and in ALB during autumn 2012.

Zooplankton growth and survival differentially respond to interactive warming and acidification effects

The copepod Acartia tonsa is a key component of a wide range of marine ecosystems, linking energy transfer from phytoplankton to higher trophic levels, and has a central role in productivity and biogeochemistry. The interaction of end-of-century global warming and ocean acidification scenarios with testing moderate temperature effects on a seminatural copepod community is needed to understand future community functioning. Here, we deployed a mesocosm experimental set-up with a full factorial design using two temperatures (13°C and 19°C) crossed with a pCO2 gradient ranging from ambient (550 μatm) to 3000 μatm. We used the natural bacteria, phyto- and microzooplankton species composition and biomass of the Kiel Bight and tested the response of A. tonsa development, carbon growth, mortality, size and condition. The tested traits were differently affected by the interaction of temperature and acidification. Ocean acidification increased development, carbon growth, size and mortality under the warming scenario of 19°C. At 13°C mortality rates decreased, while carbon growth, size and condition increased with acidification. We conclude from our experimental approach that a single species shows a variety of responses depending on the focal functional trait. Trait-specific mesozooplankton responses need to be further investigated and compared between geographical regions, seasons and taxonomic groups.

Direct and indirect effects of near-future pCO2 levels on zooplankton dynamics

Ocean acidification has direct physiological effects on organisms, for example by dissolving the calcium carbonate structures of calcifying species. However, non-calcifiers may also be affected by changes in seawater chemistry. To disentangle the direct and indirect effects of ocean acidification on zooplankton growth, we undertook a study with two model organisms. Specifically, we investigated the individual effects of short-term exposure to high and low seawater pCO2, and different phytoplankton qualities as a result of different CO2 incubations on the growth of a heterotrophic dinoflagellate (Oxyrrhis marina) and a copepod species (Acartia tonsa). It was observed previously that higher CO2 concentrations can decrease phytoplankton food quality in terms of carbon:nutrient ratios. We therefore expected both seawater pCO2 (pH) and phytoplankton quality to result in decreased zooplankton growth. Although we expected lowest growth rates for all zooplankton under high seawater pCO2 and low algal quality, we found that direct pH effects on consumers seem to be of lesser importance than the associated decrease in algal quality. The decrease in the quality of primary producers under high pCO2 conditions negatively affected zooplankton growth, which may lead to lower availability of food for the next trophic level and thus potentially affect the recruitment of higher trophic levels.

Drivers of trophic amplification of ocean productivity trends in a changing climate

Pronounced projected 21st century trends in regional oceanic net primary production (NPP) raise the prospect of significant redistributions of marine resources. Recent results further suggest that NPP changes may be amplified at higher trophic levels. Here, we elucidate the role of planktonic food web dynamics in driving projected changes in mesozooplankton production (MESOZP) found to be, on average, twice as large as projected changes in NPP by the latter half of the 21st century under a high emissions scenario in the Geophysical Fluid Dynamics Laboratory's ESM2M–COBALT (Carbon, Ocean Biogeochemistry and Lower Trophics) earth system model. Globally, MESOZP was projected to decline by 7.9% but regional MESOZP changes sometimes exceeded 50%. Changes in three planktonic food web properties – zooplankton growth efficiency (ZGE), the trophic level of mesozooplankton (MESOTL), and the fraction of NPP consumed by zooplankton (zooplankton–phytoplankton coupling, ZPC), explain the projected amplification. Zooplankton growth efficiencies (ZGE) changed with NPP, amplifying both NPP increases and decreases. Negative amplification (i.e., exacerbation) of projected subtropical NPP declines via this mechanism was particularly strong since consumers in the subtropics have limited surplus energy above basal metabolic costs. Increased mesozooplankton trophic level (MESOTL) resulted from projected declines in large phytoplankton production. This further amplified negative subtropical NPP declines but was secondary to ZGE and, at higher latitudes, was often offset by increased ZPC. Marked ZPC increases were projected for high-latitude regions experiencing shoaling of deep winter mixing or decreased winter sea ice – both tending to increase winter zooplankton biomass and enhance grazer control of spring blooms. Increased ZPC amplified projected NPP increases in the Arctic and damped projected NPP declines in the northwestern Atlantic and Southern Ocean. Improved understanding of the physical and biological interactions governing ZGE, MESOTL and ZPC is needed to further refine estimates of climate-driven productivity changes across trophic levels.

Drivers of trophic amplification of ocean productivity trends in a changing climate

Pronounced projected 21st century trends in regional oceanic net primary production (NPP) raise the prospect of significant redistributions of marine resources. Recent results further suggest that NPP changes may be amplified at higher trophic levels. Here, we elucidate the role of planktonic food web dynamics in driving projected changes in mesozooplankton production (MESOZP) found to be, on average, twice as large as projected changes in NPP by the latter half of the 21st century under a high emissions scenario. Globally, MESOZP was projected to decline by 7.9% but regional MESOZP changes sometimes exceeded 50%. Changes in three planktonic food web properties – zooplankton growth efficiency (ZGE), the trophic level of mesozooplankton (MESOTL), and the fraction of NPP consumed by zooplankton (zooplankton-phytoplankton coupling, ZPC), were demonstrated to be responsible for the projected amplification. Zooplankton growth efficiencies (ZGE) changed with NPP, amplifying both NPP increases and decreases. Negative amplification (i.e., exacerbation) of projected subtropical NPP declines via this mechanism was particularly strong since consumers in the subtropics already have limited surplus energy above basal metabolic costs. Increased mesozooplankton trophic level (MESOTL) resulted from projected declines in large phytoplankton production, the primary target of herbivorous mesozooplankton. This further amplified negative subtropical NPP declines but was secondary to ZGE and, at higher latitudes, was often offset by increased ZPC. Marked ZPC increases were projected for high latitude regions experiencing shoaling of deep winter mixing or decreased winter sea ice – both tending to increase winter zooplankton biomass and enhance grazer control of spring blooms. Increased ZPC amplified projected NPP increases associated with declining sea ice in the Artic and damped projected NPP declines associated with decreased mixing in the Northwest Atlantic and Southern Ocean. Improved understanding of the complex interactions governing these food web properties is essential to further refine estimates of climate-driven productivity changes across trophic levels.