The influence of the biological pump on ocean chemistry: implications for long‐term trends in marine redox chemistry,the global carbon cycle,and marine animal ecosystems

The net export of organic matter from the surface ocean and its respiration at depth create vertical gradients in nutrient and oxygen availability that play a primary role in structuring marine ecosystems. Changes in the properties of this ‘biological pump’ have been hypothesized to account for important shifts in marine ecosystem structure, including the Cambrian explosion. However, the influence of variation in the behavior of the biological pump on ocean biogeochemistry remains poorly quantified, preventing any detailed exploration of how changes in the biological pump over geological time may have shaped long‐term shifts in ocean chemistry, biogeochemical cycling, and ecosystem structure. Here, we use a 3‐dimensional Earth system model of intermediate complexity to quantitatively explore the effects of the biological pump on marine chemistry. We find that when respiration of sinking organic matter is efficient, due to slower sinking or higher respiration rates, anoxia tends to be more prevalent and to occur in shallower waters. Consequently, the Phanerozoic trend toward less bottom‐water anoxia in continental shelf settings can potentially be explained by a change in the spatial dynamics of nutrient cycling rather than by any change in the ocean phosphate inventory. The model results further suggest that the Phanerozoic decline in the prevalence ocean anoxia is, in part, a consequence of the evolution of larger phytoplankton, many of which produce mineralized tests. We hypothesize that the Phanerozoic trend toward greater animal abundance and metabolic demand was driven more by increased oxygen concentrations in shelf environments than by greater food (nutrient) availability. In fact, a lower‐than‐modern ocean phosphate inventory in our closed system model is unable to account for the Paleozoic prevalence of bottom‐water anoxia. Overall, these model simulations suggest that the changing spatial distribution of photosynthesis and respiration in the oceans has exerted a first‐order control on Earth system evolution across Phanerozoic time.     

Tracking the rise of eukaryotes to ecological dominance with zinc isotopes

The biogeochemical cycling of zinc (Zn) is intimately coupled with organic carbon in the ocean. Based on an extensive new sedimentary Zn isotope record across Earth's history, we provide evidence for a fundamental shift in the marine Zn cycle ~800 million years ago. We discuss a wide range of potential drivers for this transition and propose that, within available constraints, a restructuring of marine ecosystems is the most parsimonious explanation for this shift. Using a global isotope mass balance approach, we show that a change in the organic Zn/C ratio is required to account for observed Zn isotope trends through time. Given the higher affinity of eukaryotes for Zn relative to prokaryotes, we suggest that a shift toward a more eukaryote‐rich ecosystem could have provided a means of more efficiently sequestering organic‐derived Zn. Despite the much earlier appearance of eukaryotes in the microfossil record (~1700 to 1600 million years ago), our data suggest a delayed rise to ecological prominence during the Neoproterozoic, consistent with the currently accepted organic biomarker records.     

A sedimentary record of the evolution of the global marine phosphorus cycle

Phosphorus (P) is typically considered to be the ultimate limiting nutrient for Earth's biosphere on geologic timescales. As P is monoisotopic, its sedimentary enrichment can provide some insights into how the marine P cycle has changed through time. A previous compilation of shale P enrichments argued for a significant change in P cycling during the Ediacaran Period (635–541 Ma). Here, using an updated P compilation—with more than twice the number of samples—we bolster the case that there was a significant transition in P cycling moving from the Precambrian into the Phanerozoic. However, our analysis suggests this state change may have occurred earlier than previously suggested. Specifically in the updated database, there is evidence for a transition ~35 million years before the onset of the Sturtian Snowball Earth glaciation in the Visingsö Group, potentially divorcing the climatic upheavals of the Neoproterozoic from changes in the Earth's P cycle. We attribute the transition in Earth's sedimentary P record to the onset of a more modern-like Earth system state characterized by less reducing marine conditions, higher marine P concentrations, and a greater predominance of eukaryotic organisms encompassing both primary producers and consumers. This view is consistent with organic biomarker evidence for a significant eukaryotic contribution to the preserved sedimentary organic matter in this succession and other contemporaneous Tonian marine sedimentary rocks. However, we stress that, even with an expanded dataset, we are likely far from pinpointing exactly when this transition occurred or whether Earth's history is characterized by a single or multiple transitions in the P cycle.     

Increasing importance of small phytoplankton in a warmer ocean

The macroecological relationships among marine phytoplankton total cell density, community size structure and temperature have lacked a theoretical explanation. The tiniest members of this planktonic group comprise cyanobacteria and eukaryotic algae smaller than 2 μm in diameter, collectively known as picophytoplankton. We combine here two ecological rules, the temperature–size relationship with the allometric size‐scaling of population abundance to explain a remarkably consistent pattern of increasing picophytoplankton biomass with temperature over the ?0.6 to 22 °C range in a merged dataset obtained in the eastern and western temperate North Atlantic Ocean across a diverse range of environmental conditions. Our results show that temperature alone was able to explain 73% of the variance in the relative contribution of small cells to total phytoplankton biomass regardless of differences in trophic status or inorganic nutrient loading. Our analysis predicts a gradual shift toward smaller primary producers in a warmer ocean. Because the fate of photosynthesized organic carbon largely depends on phytoplankton size, we anticipate future alterations in the functioning of oceanic ecosystems.     

Metal limitation of cyanobacterial N2 fixation and implications for the Precambrian nitrogen cycle

Nitrogen fixation is a critical part of the global nitrogen cycle, replacing biologically available reduced nitrogen lost by denitrification. The redox‐sensitive trace metals Fe and Mo are key components of the primary nitrogenase enzyme used by cyanobacteria (and other prokaryotes) to fix atmospheric N₂ into bioessential compounds. Progressive oxygenation of the Earth's atmosphere has forced changes in the redox state of the oceans through geologic time, from anoxic Fe‐enriched waters in the Archean to partially sulfidic deep waters by the mid‐Proterozoic. This development of ocean redox chemistry during the Precambrian led to fluctuations in Fe and Mo availability that could have significantly impacted the ability of prokaryotes to fix nitrogen. It has been suggested that metal limitation of nitrogen fixation and nitrate assimilation, along with increased rates of denitrification, could have resulted in globally reduced rates of primary production and nitrogen‐starved oceans through much of the Proterozoic. To test the first part of this hypothesis, we grew N₂‐fixing cyanobacteria in cultures with metal concentrations reflecting an anoxic Archean ocean (high Fe, low Mo), a sulfidic Proterozoic ocean (low Fe, moderate Mo), and an oxic Phanerozoic ocean (low Fe, high Mo). We measured low rates of cellular N₂ fixation under [Fe] and [Mo] estimated for the Archean ocean. With decreased [Fe] and higher [Mo] representing sulfidic Proterozoic conditions, N₂ fixation, growth, and biomass C:N were similar to those observed with metal concentrations of the fully oxygenated oceans that likely developed in the Phanerozoic. Our results raise the possibility that an initial rise in atmospheric oxygen could actually have enhanced nitrogen fixation rates to near modern marine levels, providing that phosphate was available and rising O₂ levels did not markedly inhibit nitrogenase activity.     

Marine biodiversification in response to evolving phytoplankton stoichiometry

Diversification of the marine biosphere is intimately linked to the evolution of the biogeochemical cycles of carbon, nutrients, and primary productivity. A meta-analysis of the ratio of carbon-to-phosphorus buried in sedimentary rocks during the past 3 billion years indicates that both food quantity and, critically, food quality increased through time as a result of the evolving stoichiometry (nutrient content) of eukaryotic phytoplankton. Evolving food quantity and quality was primarily a function of broad tectonic cycles that influenced not just carbon burial, but also nutrient availability and primary productivity. Increasing nutrient availability during the middle-to-Late Proterozoic culminated in the production of food (phytoplankton biomass and fresh dead organic matter) with C:P Redfield ratios sufficient to finally promote geologically-rapid biodiversification during the Proterozoic–Phanerozoic transition. This resulted in further, massive nutrient sequestration into biomass that triggered positive feedback via nutrient recycling (bioturbation, mesozooplankton grazing) on phytoplankton productivity. Increasing rates and depths of bioturbation through the Phanerozoic suggest that nutrient recycling continued to increase. Increasing bioturbation and nutrient cycling appear to have been necessary to sustain the primary productivity and “energetics” (biomass, metabolic rates, and physical activity such as predation) of the marine biosphere because of the geologically-slow input of macronutrients like phosphorus from land and the continued sequestration of nutrients into marine and terrestrial biomass.     

Timing and abundance as key mechanisms affecting trophic interactions in variable environments

Climatic changes are disrupting otherwise tight trophic interactions between predator and prey. Most of the earlier studies have primarily focused on the temporal dimension of the relationship in the framework of the match–mismatch hypothesis. This hypothesis predicts that predator's recruitment will be high if the peak of the prey availability temporally matches the most energy‐demanding period of the predators breeding phenology. However, the match–mismatch hypothesis ignores the level of food abundance while this can compensate small mismatches. Using a novel time‐series model explicitly quantifying both the timing and the abundance component for trophic relationships, we here show that timing and abundance of food affect recruitment differently in a marine (cod/zooplankton), a marine–terrestrial (puffin/herring) and a terrestrial (sheep/vegetation) ecosystem. The quantification of the combined effect of abundance and timing of prey on predator dynamics enables us to come closer to the mechanisms by which environment variability may affect ecological systems.     

Territorial ants depress plant growth through cascading non‐trophic effects in an alpine meadow

Understanding non‐trophic interactions is critical to mechanistically linking community structure and ecosystem functioning. Despite the widespread occurrence of territoriality across animal taxa and ecosystems, the cascading ecological consequences of non‐trophic interactions between territorial animals and intruders have been poorly studied. We experimentally investigated the non‐trophic interaction between territorial ants and members of a dung decomposer community (i.e. predatory arthropods, maggots and coprophagous beetles) in an alpine meadow. We further examined how this non‐trophic interaction cascaded to influence ecosystem properties including dung removal rate, soil nutrient status and aboveground plant biomass surrounding dung pats. Results indicated that territorial interference of ants on key decomposers cascaded to affect plant growth. Specifically, ants significantly decreased the abundance of coprophagous beetles at the time of their peak‐abundance and hence decreased dung removal rates and soil nitrogen concentrations, ultimately decreasing aboveground plant biomass. The strength of this non‐trophic cascading effect was comparable to those reported in studies addressing trophic cascades triggered by predator–prey interactions. Our findings suggest that the non‐trophic interactions and associated cascading effects stemming from territorial behavior should be incorporated into ecological network modeling and research addressing biodiversity–ecosystem functioning relationships.     

Nutrient reduction and climate change cause a potential shift from pelagic to benthic pathways in a eutrophic marine ecosystem

The degree to which marine ecosystems may support the pelagic or benthic food chain has been shown to vary across natural and anthropogenic gradients for e.g., in temperature and nutrient availability. Moreover, such external forcing may not only affect the flux of organic matter but could trigger large and abrupt changes, i.e., trophic cascades and ecological regime shifts, which once having occurred may prove potentially irreversible. In this study, we investigate the state and regulatory pathways of the Kattegat; a eutrophied and heavily exploited marine ecosystem, specifically testing for the occurrence of regime shifts and the relative importance of multiple drivers, e.g., climate change, eutrophication and commercial fishing on ecosystem dynamics and trophic pathways. Using multivariate statistics and nonlinear regression on a comprehensive data set, covering abiotic factors and biotic variables across all trophic levels, we here propose a potential regime shift from pelagic to benthic regulatory pathways; a possible first sign of recovery from eutrophication likely triggered by drastic nutrient reductions (involving both nitrogen and phosphorus), in combination with climate‐driven changes in local environmental conditions (e.g., temperature and oxygen concentrations).     

From bottom-up to top-down control of invertebrate herbivores in a retrogressive chronosequence

In the long-term absence of disturbance, ecosystems often enter a decline or retrogressive phase which leads to reductions in primary productivity, plant biomass, nutrient cycling and foliar quality. However, the consequences of ecosystem retrogression for higher trophic levels such as herbivores and predators, are less clear. Using a post-fire forested island-chronosequence across which retrogression occurs, we provide evidence that nutrient availability strongly controls invertebrate herbivore biomass when predators are few, but that there is a switch from bottom-up to top-down control when predators are common. This trophic flip in herbivore control probably arises because invertebrate predators respond to alternative energy channels from the adjacent aquatic matrix, which were independent of terrestrial plant biomass. Our results suggest that effects of nutrient limitation resulting from ecosystem retrogression on trophic cascades are modified by nutrient-independent variation in predator abundance, and this calls for a more holistic approach to trophic ecology to better understand herbivore effects on plant communities.     

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.     

Evaluating trophic cascades as drivers of regime shifts in different ocean ecosystems

In ecosystems that are strongly structured by predation, reducing top predator abundance can alter several lower trophic levels—a process known as a trophic cascade. A persistent trophic cascade also fits the definition of a regime shift. Such ‘trophic cascade regime shifts'' have been reported in a few pelagic marine systems—notably the Black Sea, Baltic Sea and eastern Scotian Shelf—raising the question of how common this phenomenon is in the marine environment. We provide a general methodology for distinguishing top-down and bottom-up effects and apply this methodology to time series from these three ecosystems. We found evidence for top-down forcing in the Black Sea due primarily to gelatinous zooplankton. Changes in the Baltic Sea are primarily bottom-up, strongly structured by salinity, but top-down forcing related to changes in cod abundance also shapes the ecosystem. Changes in the eastern Scotian Shelf that were originally attributed to declines in groundfish are better explained by changes in stratification. Our review suggests that trophic cascade regime shifts are rare in open ocean ecosystems and that their likelihood increases as the residence time of water in the system increases. Our work challenges the assumption that negative correlation between consecutive trophic levels implies top-down forcing.     

Biodiversity and ecosystem functioning in food webs: the vertical diversity hypothesis

One challenge in merging community and ecosystem ecology is to integrate the complexity of natural multitrophic communities into concepts of ecosystem functioning. Here, we combine food‐web and allometry theories to demonstrate that primary production, as measured by the total nutrient uptake of the multitrophic community, is determined by vertical diversity (i.e. food web's maximum trophic level) and structure (i.e. distributions of species and their abundances and metabolic rates across trophic levels). In natural ecosystems, the community size distribution determines all these vertical patterns and thus the total nutrient uptake. Our model suggests a vertical diversity hypothesis (VDH) for ecosystem functioning in complex food webs. It predicts that, under a given nutrient supply, the total nutrient uptake increases exponentially with the maximum trophic level in the food web and it increases with its maximum body size according to a power law. The VDH highlights the effect of top–down regulation on plant nutrient uptake, which complements traditional paradigms that emphasised the bottom–up effect of nutrient supply on vertical diversity. We conclude that the VDH contributes to a synthetic framework for understanding the relationship between vertical diversity and ecosystem functioning in food webs and predicting the impacts of global changes on multitrophic ecosystems.     

High trophic level feedbacks on global ocean carbon uptake and marine ecosystem dynamics under climate change

Despite recurrent emphasis on their ecological and economic roles, the importance of high trophic levels (HTLs) on ocean carbon dynamics, through passive (fecal pellet production, carcasses) and active (vertical migration) processes, is still largely unexplored, notably under climate change scenarios. In addition, HTLs impact the ecosystem dynamics through top-down effects on lower trophic levels, which might change under anthropogenic influence. Here we compare two simulations of a global biogeochemical–ecosystem model with and without feedbacks from large marine animals. We show that these large marine animals affect the evolution of low trophic level biomasses, hence net primary production and most certainly ecosystem equilibrium, but seem to have little influence on the 21st-century anthropogenic carbon uptake under the RCP8.5 scenario. These results provide new insights regarding the expectations for trophic amplification of climate change through the marine trophic chain and regarding the necessity to explicitly represent marine animals in Earth System Models.     

Evolution of iron and oxygen biogeochemical cycles during the Precambrian

Iron (Fe) is an essential element for life, and its geochemical cycle is intimately linked to the coupled history of life and Earth's environment. The accumulated geologic records indicate that ferruginous waters existed in the Precambrian oceans not only before the first major rise of atmospheric O₂ levels (Great Oxidation Event; GOE) during the Paleoproterozoic, but also during the rest of the Proterozoic. However, the interactive evolution of the biogeochemical cycles of O₂ and Fe during the Archean–Proterozoic remains ambiguous. Here, we develop a biogeochemical model to investigate the coupled biogeochemical evolution of Fe–O₂–P–C cycles across the GOE. Our model demonstrates that the marine Fe cycle was less sensitive to changes in the production rate of O₂ before the GOE (atmospheric pO₂ < 10⁻⁶ PAL; present atmospheric level). When the P supply rate to the ocean exceeds a certain threshold, the GOE occurs and atmospheric pO₂ rises to ~10⁻³–10⁻¹ PAL. After the GOE, the marine Fe(II) concentration is highly sensitive to atmospheric pO₂, suggesting that the marine redox landscape during the Proterozoic may have fluctuated between ferruginous conditions and anoxic non-ferruginous conditions with sulfidic water masses around continental margins. At a certain threshold value of atmospheric pO₂ of ~0.3% PAL, the primary oxidation pathway of Fe(II) shifts from the activity of Fe(II)-utilizing anoxygenic photoautotrophs in sunlit surface waters to abiotic process in the deep ocean. This is accompanied by a shift in the primary deposition site of Fe(III) hydroxides from the surface ocean to the deep sea, providing a plausible mechanistic explanation for the observed cessation of iron formations during the Proterozoic.     

A sluggish mid‐Proterozoic biosphere and its effect on Earth's redox balance

The possibility of low but nontrivial atmospheric oxygen (O₂) levels during the mid‐Proterozoic (between 1.8 and 0.8 billion years ago, Ga) has important ramifications for understanding Earth's O₂ cycle, the evolution of complex life and evolving climate stability. However, the regulatory mechanisms and redox fluxes required to stabilize these O₂ levels in the face of continued biological oxygen production remain uncertain. Here, we develop a biogeochemical model of the C‐N‐P‐O₂‐S cycles and use it to constrain global redox balance in the mid‐Proterozoic ocean–atmosphere system. By employing a Monte Carlo approach bounded by observations from the geologic record, we infer that the rate of net biospheric O₂ production was Tmol year^?1 (1σ), or ~25% of today's value, owing largely to phosphorus scarcity in the ocean interior. Pyrite burial in marine sediments would have represented a comparable or more significant O₂ source than organic carbon burial, implying a potentially important role for Earth's sulphur cycle in balancing the oxygen cycle and regulating atmospheric O₂ levels. Our statistical approach provides a uniquely comprehensive view of Earth system biogeochemistry and global O₂ cycling during mid‐Proterozoic time and implicates severe P biolimitation as the backdrop for Precambrian geochemical and biological evolution.     

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.     

Planktonic microbes: Tiny cells at the base of the ocean's food webs

Phytoplankton in the size range 5-100 μm was originally thought to be the primary source of food for most life in the sea. However, smaller planktonic microbes, down to 0.2 μm in size, have been the focus of intensive investigation by marine scientists during the past two decades. These microbes attain high abundance and biomass in all parts of the world ocean. They include non-photosynthesizing bacteria, at least two types of photosynthesizing prokaryotes, and eukaryotic phototrophs. The new information has resulted in a greatly revised concept of how pelagic ecosystems in both marine and freshwater environments function. The original idea of a basically linear food chain from diatoms to copepods to fish has given way to an extremely complex model of trophic interactions within a microbial food web, which supports metazoan food webs via biomass production of both heterotrophic and autotrophic cells.