Diversity decoupled from ecosystem function and resilience during mass extinction recovery.

The Chicxulub bolide impact 66 million years ago drove the near-instantaneous collapse of ocean ecosystems. The devastating loss of diversity at the base of ocean food webs probably triggered cascading extinctions across all trophic levels1-3 and caused severe disruption of the biogeochemical functions of the ocean, and especially disrupted the cycling of carbon between the surface and deep sea4,5. The absence of sufficiently detailed biotic data that span the post-extinction interval has limited our understanding of how ecosystem resilience and biochemical function was restored; estimates6-8 of ecosystem 'recovery' vary from less than 100 years to 10 million years. Here, using a 13-million-year-long nannoplankton time series, we show that post-extinction communities exhibited 1.8 million years of exceptional volatility before a more stable equilibrium-state community emerged that displayed hallmarks of resilience. The transition to this new equilibrium-state community with a broader spectrum of cell sizes coincides with indicators of carbon-cycle restoration and a fully functioning biological pump9. These findings suggest a fundamental link between ecosystem recovery and biogeochemical cycling over timescales that are longer than those suggested by proxies of export production7,8, but far shorter than the return of taxonomic richness6. The fact that species richness remained low as both community stability and biological pump efficiency re-emerged suggests that ecological functions rather than the number of species are more important to community resilience and biochemical functions.

Warm plankton soup and red herrings: calcareous nannoplankton cellular communities and the Palaeocene-Eocene Thermal Maximum.

Past global warming events such as the Palaeocene-Eocene Thermal Maximum (PETM-56 Ma) are attributed to the release of vast amounts of carbon into the ocean, atmosphere and biosphere with recovery ascribed to a combination of silicate weathering and organic carbon burial. The phytoplanktonic nannoplankton are major contributors of organic and inorganic carbon but their role in this recovery process remains poorly understood and complicated by their contribution to marine calcification. Biocalcification is implicated not only in long-term carbon burial but also both short-term positive and negative climatic feedbacks associated with seawater buffering and responses to ocean acidification. Here, we use exceptional records of preserved fossil coccospheres to reconstruct cell size distribution, biomass production (particulate organic carbon, POC) and (particulate) inorganic carbon (PIC) yields of three contrasting nannoplankton communities (Bass River-outer shelf, Maud Rise-uppermost bathyal, Shatsky Rise-open ocean) through the PETM onset and recovery. Each of the sites shows contrasting community responses across the PETM as a function of their taxic composition and total community biomass. Our results indicate that nannoplankton PIC:POC had no role in short-term climate feedback and, as such, their importance as a source of CO2 to the environment is a red herring. It is nevertheless likely that shifts to greater numbers of smaller cells at the shelf site in particular led to greater carbon transfer efficiency, and that nannoplankton productivity and export across the shelves had a significant modulating effect on carbon sequestration during the PETM recovery.This article is part of a discussion meeting issue 'Hyperthermals: rapid and extreme global warming in our geological past'.

Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness.

The end-Cretaceous bolide impact triggered the devastation of marine ecosystems. However, the specific kill mechanism(s) are still debated, and how primary production subsequently recovered remains elusive. We used marine plankton microfossils and eco-evolutionary modeling to determine strategies for survival and recovery, finding that widespread phagotrophy (prey ingestion) was fundamental to plankton surviving the impact and also for the subsequent reestablishment of primary production. Ecological selectivity points to extreme post-impact light inhibition as the principal kill mechanism, with the marine food chain temporarily reset to a bacteria-dominated state. Subsequently, in a sunlit ocean inhabited by only rare survivor grazers but abundant small prey, it was mixotrophic nutrition (autotrophy and heterotrophy) and increasing cell sizes that enabled the eventual reestablishment of marine food webs some 2 million years later.

Coccolithophore calcification response to past ocean acidification and climate change.

Anthropogenic carbon dioxide emissions are forcing rapid ocean chemistry changes and causing ocean acidification (OA), which is of particular significance for calcifying organisms, including planktonic coccolithophores. Detailed analysis of coccolithophore skeletons enables comparison of calcite production in modern and fossil cells in order to investigate biomineralization response of ancient coccolithophores to climate change. Here we show that the two dominant coccolithophore taxa across the Paleocene-Eocene Thermal Maximum (PETM) OA global warming event (~56 million years ago) exhibited morphological response to environmental change and both showed reduced calcification rates. However, only Coccolithus pelagicus exhibits a transient thinning of coccoliths, immediately before the PETM, that may have been OA-induced. Changing coccolith thickness may affect calcite production more significantly in the dominant modern species Emiliania huxleyi, but, overall, these PETM records indicate that the environmental factors that govern taxonomic composition and growth rate will most strongly influence coccolithophore calcification response to anthropogenic change.

The geological record of ocean acidification.

Ocean acidification may have severe consequences for marine ecosystems; however, assessing its future impact is difficult because laboratory experiments and field observations are limited by their reduced ecologic complexity and sample period, respectively. In contrast, the geological record contains long-term evidence for a variety of global environmental perturbations, including ocean acidification plus their associated biotic responses. We review events exhibiting evidence for elevated atmospheric CO(2), global warming, and ocean acidification over the past ~300 million years of Earth's history, some with contemporaneous extinction or evolutionary turnover among marine calcifiers. Although similarities exist, no past event perfectly parallels future projections in terms of disrupting the balance of ocean carbonate chemistry-a consequence of the unprecedented rapidity of CO(2) release currently taking place.

Comment on "Calcareous nannoplankton response to surface-water acidification around Oceanic Anoxic Event 1a".

Erba et al. (Reports, 23 July 2010, p. 428) attributed calcareous nannofossil morphology and assemblage changes across Cretaceous Oceanic Anoxic Event 1a to the effects of surface ocean acidification. We argue that the quality of carbonate preservation in these sequences, the unsupported assumptions of the biotic response to acidity, and the absence of independent proxy estimates for ocean pH or atmospheric pCO(2) render this conclusion questionable.

Phytoplankton calcification in a high-CO2 world.

Ocean acidification in response to rising atmospheric CO2 partial pressures is widely expected to reduce calcification by marine organisms. From the mid-Mesozoic, coccolithophores have been major calcium carbonate producers in the world's oceans, today accounting for about a third of the total marine CaCO3 production. Here, we present laboratory evidence that calcification and net primary production in the coccolithophore species Emiliania huxleyi are significantly increased by high CO2 partial pressures. Field evidence from the deep ocean is consistent with these laboratory conclusions, indicating that over the past 220 years there has been a 40% increase in average coccolith mass. Our findings show that coccolithophores are already responding and will probably continue to respond to rising atmospheric CO2 partial pressures, which has important implications for biogeochemical modeling of future oceans and climate.

Nannoplankton extinction and origination across the Paleocene-Eocene Thermal Maximum.

The Paleocene-Eocene Thermal Maximum (PETM, approximately 55 million years ago) was an interval of global warming and ocean acidification attributed to rapid release and oxidation of buried carbon. We show that the onset of the PETM coincided with a prominent increase in the origination and extinction of calcareous phytoplankton. Yet major perturbation of the surface-water saturation state across the PETM was not detrimental to the survival of most calcareous nannoplankton taxa and did not impart a calcification or ecological bias to the pattern of evolutionary turnover. Instead, the rate of environmental change appears to have driven turnover, preferentially affecting rare taxa living close to their viable limits.