Resilience of marine invertebrate communities during the early Cenozoic hyperthermals

Resilience of marine invertebrate communities during the early Cenozoic hyperthermals


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The hyperthermal events of the Cenozoic, including the Paleocene-Eocene Thermal Maximum, provide an opportunity to investigate the potential effects of climate warming on marine ecosystems.


Here, we examine the shallow benthic marine communities preserved in the late Cretaceous to Eocene strata on the Gulf Coastal Plain (United States). In stark contrast to the ecological


shifts following the end-Cretaceous mass extinction, our data show that the early Cenozoic hyperthermals did not have a long-term impact on the generic diversity nor composition of the Gulf


Coastal Plain molluscan communities. We propose that these communities were resilient to climate change because molluscs are better adapted to high temperatures than other taxa, as


demonstrated by their physiology and evolutionary history. In terms of resilience, these communities differ from other shallow-water carbonate ecosystems, such as reef communities, which


record significant changes during the early Cenozoic hyperthermals. These data highlight the strikingly different responses of community types, i.e., the almost imperceptible response of


molluscs versus the marked turnover of foraminifera and reef faunas. The impact on molluscan communities may have been low because detrimental conditions did not devastate the entire Gulf


Coastal Plain, allowing molluscs to rapidly recolonise vacated areas once harsh environmental conditions ameliorated.


Human activities are drastically changing conditions in coastal marine ecosystems by polluting, destroying habitats, overexploiting resources, enabling invasive species, and driving climate


warming. Increased greenhouse gas emissions associated with these activities harm marine communities by expanding hypoxic dead zones, increasing ocean acidity, and causing thermal stress1,2.


In order to understand how communities will respond to climate-related stressors, we look to potential deep-time analogues and the community shifts recorded by fossils. The Eocene witnessed


two separate long-term warming trends of ~6 °C culminating in the late Ypresian and Bartonian, known as the Early Eocene Climatic Optimum (EECO) and the Middle Eocene Climatic Optimum


(MECO), respectively (Fig. S1). Superimposed on these long-term trends are many short-lived intervals of increased carbon injection into the atmosphere and increased sea surface


temperatures, known as hyperthermals, and of these the Paleocene-Eocene Thermal Maximum (PETM) and the Eocene Thermal Maximum 2 have the highest magnitude and pace3 (Fig. S1). It has been


argued that these hyperthermal events represent the best analogues for projected climatic change, as they were caused by rapid increases in pCO2 and involved various environmental


consequences, such as ocean acidification and intensification of the hydrological cycle2,4. In addition, the peak of the MECO saw rapid warming5 and could be considered another hyperthermal.


Similar hyperthermal events of smaller magnitude have also been recorded from the Paleocene, e.g., the latest Danian Event6.


The PETM was the most rapid warming event of the early Cenozoic and had the largest ecological impact on marine ecosystems of any hyperthermal during that time7. In shallow-water carbonates


there was a substantial decline in reef volume8 that manifested as a shift from coral-algae reefs to large foraminiferal carbonate ramps9; in the deep-sea, there was a major extinction of


deep-sea benthic foraminifera10, dwarfing of both benthic foraminifera and ostracods11; a rapid diversification of pteropods12, and poleward shifts in the distribution of planktic


foraminifera, dinoflagellates, and radiolarians13. Supposed causes of PETM ecological changes include ocean deoxygenation, rising temperatures, shoaling of the calcium carbonate compensation


depth, and variations in food supply7,13. Nevertheless, the response of non-reefal shallow marine ecosystems to the PETM remains unclear, and there are few studies that quantitatively


investigate changes in the composition of macrobenthic assemblages. Along the United States (US) Atlantic Coastal Plain (South Carolina to New Jersey), the PETM interval contains few or no


adult molluscs, potentially due to low oxygen conditions and/or ocean acidification14,15. Conversely, the US Gulf Coastal Plain (Texas to Georgia) shows no evidence that the PETM resulted in


a diversity decline or body size decline in molluscan communities16,17. Furthermore, Ivany et al.16 do not report a faunal turnover at the family-level, but their data do suggest changes in


the dominant genera and species.


To improve our understanding of the impact of the early Cenozoic hyperthermals on shallow marine benthic communities, we quantitatively investigated changes in their diversity and


composition along the Gulf Coastal Plain. This study tests the hypothesis that early Cenozoic hyperthermal events were associated with significant, long-term changes in community diversity


and composition. We compiled a dataset of species abundance and richness from the Late Cretaceous through Eocene (Maastrichtian-Priabonian) interval and quantitatively assessed the molluscan


communities for changes in (i) taxon richness, (ii) taxonomic composition, and (iii) functional composition. Although the faunal record does not allow for the assessment of the short-term


(up to millennial-scale) responses of molluscs to the early Cenozoic hyperthermals, our comprehensive analysis shows that the early Cenozoic hyperthermals did not significantly impact the


evolutionary history of benthic molluscan communities.


Analyses of the raw and Shareholder Quorum Sampling (SQS) data yield similar trends in the species, generic, and functional richness of benthic assemblages respectively (Fig. 1). Our


analyses provide evidence for two substantial changes in generic richness: a significant (Kruskall-Wallis test (KW): p