New Age of Fishes initiated by the Cretaceous-Paleogene mass extinction.

Ray-finned fishes (Actinopterygii) comprise nearly half of all modern vertebrate diversity, and are an ecologically and numerically dominant megafauna in most aquatic environments. Crown teleost fishes diversified relatively recently, during the Late Cretaceous and early Paleogene, although the exact timing and cause of their radiation and rise to ecological dominance is poorly constrained. Here we use microfossil teeth and shark dermal scales (ichthyoliths) preserved in deep-sea sediments to study the changes in the pelagic fish community in the latest Cretaceous and early Paleogene. We find that the Cretaceous-Paleogene (K/Pg) extinction event marked a profound change in the structure of ichthyolith communities around the globe: Whereas shark denticles outnumber ray-finned fish teeth in Cretaceous deep-sea sediments around the world, there is a dramatic increase in the proportion of ray-finned fish teeth to shark denticles in the Paleocene. There is also an increase in size and numerical abundance of ray-finned fish teeth at the boundary. These changes are sustained through at least the first 24 million years of the Cenozoic. This new fish community structure began at the K/Pg mass extinction, suggesting the extinction event played an important role in initiating the modern "age of fishes."

Intermediate water circulation drives distribution of Pliocene Oxygen Minimum Zones.

Oxygen minimum zones (OMZs) play a critical role in global biogeochemical cycling and act as barriers to dispersal for marine organisms. OMZs are currently expanding and intensifying with climate change, however past distributions of OMZs are relatively unknown. Here we present evidence for widespread pelagic OMZs during the Pliocene (5.3-2.6 Ma), the most recent epoch with atmospheric CO2 analogous to modern (~400-450 ppm). The global distribution of OMZ-affiliated planktic foraminifer, Globorotaloides hexagonus, and Earth System and Species Distribution Models show that the Indian Ocean, Eastern Equatorial Pacific, eastern South Pacific, and eastern North Atlantic all supported OMZs in the Pliocene, as today. By contrast, low-oxygen waters were reduced in the North Pacific and expanded in the North Atlantic in the Pliocene. This spatially explicit perspective reveals that a warmer world can support both regionally expanded and contracted OMZs, with intermediate water circulation as a key driver.

An early Miocene extinction in pelagic sharks.

Shark populations have been decimated in recent decades because of overfishing and other anthropogenic stressors; however, the long-term impacts of such changes in marine predator abundance and diversity are poorly constrained. We present evidence for a previously unknown major extinction event in sharks that occurred in the early Miocene, ~19 million years ago. During this interval, sharks virtually disappeared from open-ocean sediments, declining in abundance by >90% and morphological diversity by >70%, an event from which they never recovered. This abrupt extinction occurred independently from any known global climate event and ~2 million to 5 million years before diversifications in the highly migratory, large-bodied predators that dominate pelagic ecosystems today, indicating that the early Miocene was a period of rapid, transformative change for open-ocean ecosystems.

Response to Comment on "An early Miocene extinction in pelagic sharks".

Naylor et al. argue that the existence of multiple denticle types within a single species precludes the use of this metric as a measure of the decline of multiple shark species. We show that species-level shark diversity would have to decrease by >90% to account for the observed >70% denticle extinction, implying that the early Miocene shark extinction was larger than previously recognized.

Response to Comment on "An early Miocene extinction in pelagic sharks".

Feichtinger et al. assert that the reduction in denticle abundance and diversity we found are incorrect, claiming that we failed to consider changes in sedimentation rate. However, we used standard methods that explicitly account for changes in sedimentation rate and density. We maintain that our initial dataset and conclusions are robust and provide evidence for a major early Miocene extinction in pelagic sharks.

Paleo-diatom composition from Santa Barbara Basin deep-sea sediments: a comparison of 18S-V9 and diat-rbcL metabarcoding vs shotgun metagenomics.

Sedimentary ancient DNA (sedaDNA) analyses are increasingly used to reconstruct marine ecosystems. The majority of marine sedaDNA studies use a metabarcoding approach (extraction and analysis of specific DNA fragments of a defined length), targeting short taxonomic marker genes. Promising examples are 18S-V9 rRNA (~121-130 base pairs, bp) and diat-rbcL (76 bp), targeting eukaryotes and diatoms, respectively. However, it remains unknown how 18S-V9 and diat-rbcL derived compositional profiles compare to metagenomic shotgun data, the preferred method for ancient DNA analyses as amplification biases are minimised. We extracted DNA from five Santa Barbara Basin sediment samples (up to ~11 000 years old) and applied both a metabarcoding (18S-V9 rRNA, diat-rbcL) and a metagenomic shotgun approach to (i) compare eukaryote, especially diatom, composition, and (ii) assess sequence length and database related biases. Eukaryote composition differed considerably between shotgun and metabarcoding data, which was related to differences in read lengths (~112 and ~161 bp, respectively), and overamplification of short reads in metabarcoding data. Diatom composition was influenced by reference bias that was exacerbated in metabarcoding data and characterised by increased representation of Chaetoceros, Thalassiosira and Pseudo-nitzschia. Our results are relevant to sedaDNA studies aiming to accurately characterise paleo-ecosystems from either metabarcoding or metagenomic data.

Enhanced fish production during a period of extreme global warmth.

Marine ecosystem models predict a decline in fish production with anthropogenic ocean warming, but how fish production equilibrates to warming on longer timescales is unclear. We report a positive nonlinear correlation between ocean temperature and pelagic fish production during the extreme global warmth of the Early Paleogene Period (62-46 million years ago [Ma]). Using data-constrained modeling, we find that temperature-driven increases in trophic transfer efficiency (the fraction of production passed up trophic levels) and primary production can account for the observed increase in fish production, while changes in predator-prey interactions cannot. These data provide new insight into upper-trophic-level processes constrained from the geological record, suggesting that long-term warming may support more productive food webs in subtropical pelagic ecosystems.

On impact and volcanism across the Cretaceous-Paleogene boundary.

The cause of the end-Cretaceous mass extinction is vigorously debated, owing to the occurrence of a very large bolide impact and flood basalt volcanism near the boundary. Disentangling their relative importance is complicated by uncertainty regarding kill mechanisms and the relative timing of volcanogenic outgassing, impact, and extinction. We used carbon cycle modeling and paleotemperature records to constrain the timing of volcanogenic outgassing. We found support for major outgassing beginning and ending distinctly before the impact, with only the impact coinciding with mass extinction and biologically amplified carbon cycle change. Our models show that these extinction-related carbon cycle changes would have allowed the ocean to absorb massive amounts of carbon dioxide, thus limiting the global warming otherwise expected from postextinction volcanism.