Elizabeth C Sibert

New Age of Fishes initiated by the Cretaceous−Paleogene mass extinction

Significance Ray-finned fishes are the most diverse and ecologically dominant group of vertebrates on the planet. Previous molecular phylogenies and paleontological studies have shown that modern ray-finned fishes (crown teleosts) radiated sometime in the Late Cretaceous or early Paleogene. Our data suggest that crown teleosts came into their current dominant ecological role in pelagic ecosystems immediately following the Cretaceous−Paleogene mass extinction 66 million years ago by filling newly vacated ecological niches and marking the beginning of an “age of ray-finned fishes.” Our study is, to our knowledge, the first geographically comprehensive, high-resolution study of marine vertebrate communities across the 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.”

Eighty-five million years of Pacific Ocean gyre ecosystem structure: long-term stability marked by punctuated change

While the history of taxonomic diversification in open ocean lineages of ray-finned fish and elasmobranchs is increasingly known, the evolution of their roles within the open ocean ecosystem remains poorly understood. To assess the relative importance of these groups through time, we measured the accumulation rate of microfossil fish teeth and elasmobranch dermal denticles (ichthyoliths) in deep-sea sediment cores from the North and South Pacific gyres over the past 85 million years (Myr). We find three distinct and stable open ocean ecosystem structures, each defined by the relative and absolute abundance of elasmobranch and ray-finned fish remains. The Cretaceous Ocean (pre-66 Ma) was characterized by abundant elasmobranch denticles, but low abundances of fish teeth. The Palaeogene Ocean (66–20 Ma), initiated by the Cretaceous/Palaeogene mass extinction, had nearly four times the abundance of fish teeth compared with elasmobranch denticles. This Palaeogene Ocean structure remained stable during the Eocene greenhouse (50 Ma) and the Eocene–Oligocene glaciation (34 Ma), despite large changes in the overall accumulation of both groups during those intervals, suggesting that climate change is not a primary driver of ecosystem structure. Dermal denticles virtually disappeared from open ocean ichthyolith assemblages approximately 20 Ma, while fish tooth accumulation increased dramatically in variability, marking the beginning of the Modern Ocean. Together, these results suggest that open ocean fish community structure is stable on long timescales, independent of total production and climate change. The timing of the abrupt transitions between these states suggests that the transitions may be due to interactions with other, non-preserved pelagic consumer groups.

Methods for isolation and quantification of microfossil fish teeth and elasmobranch dermal denticles (ichthyoliths) from marine sediments

Ichthyoliths—microfossil fish teeth and shark dermal scales (denticles)—are found in nearly all marine sediments. Their small size and relative rarity compared to other microfossil groups means that they have been largely ignored by the paleontology and paleoceanography communities, except as carriers of certain isotopic systems. Yet, when properly concentrated, ichthyoliths are sufficiently abundant to reveal patterns of fish abundance and diversity at unprecedented temporal and spatial resolution, in contrast to the typical millions of years-long gaps in the vertebrate body fossil record. In addition, ichthyoliths are highly resistant to dissolution, making it possible to reconstruct whole fish communities over highly precise and virtually continuous timescales. Here we present methods to isolate and utilize ichthyoliths preserved in the sedimentary record to track fish community structure and ecosystem productivity through geological and historical time periods. These include techniques for isolation and concentration of these microfossils from a wide range of sediments, including deep-sea and coral reef carbonates, clays, shales, and silicate-rich sediments. We also present a novel protocol for ichthyolith staining using Alizarin Red S to easily visualize and distinguish small teeth from debris in the sample. Finally, we discuss several metrics for quantification of ichthyolith community structure and abundance, and their applications to reconstruction of ancient marine food webs and environments. Elizabeth C. Sibert. Society of Fellows, Harvard University, 78 Mount Auburn Street, Cambridge, Massachusetts 02138, USA; Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive MC 0208, La Jolla, California 92093, USA. esibert@fas.harvard.edu Katie L. Cramer. Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive MC 0208, La Jolla, California 92093, USA. kcramer@ucsd.edu Philip A. Hastings. Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive MC 0208, La Jolla, California 92093, USA. phastings@ucsd.edu Richard D. Norris. Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive MC 0244, La Jolla, California 92093, USA. rnorris@ucsd.edu

AutoMorph: Accelerating morphometrics with automated 2D and 3D image processing and shape extraction

Large-scale, comparative studies of morphological variation are rare due to the time-intensive nature of shape quantification. This data gap is important to address, as intraspecific and interspecific morphological variation underpins and reflects ecological and evolutionary processes. Here, we detail a novel software package, AutoMorph, for high-throughput object and shape extraction. AutoMorph can batch image many types of organisms (e.g. foraminifera, molluscs and fish teeth), allowing for rapid generation of assemblage-scale morphological data. We used AutoMorph to image and generate 2D and 3D morphological data for >100,000 marine microfossils in about a year. Our collaborators have used AutoMorph to process >12,000 patellogastropod shells and >50,000 fish teeth. AutoMorph allows users to rapidly produce large amounts of morphological data, facilitating community-scale evolutionary and ecological studies. To hasten the adoption of automated approaches, we have made AutoMorph freely available and open source. AutoMorph runs on all UNIX-like systems; future versions will run across all platforms.

Two pulses of morphological diversification in Pacific pelagic fishes following the Cretaceous–Palaeogene mass extinction

Molecular phylogenies suggest some major radiations of open-ocean fish clades occurred roughly coincident with the Cretaceous–Palaeogene (K/Pg) boundary, however the timing and nature of this diversification is poorly constrained. Here, we investigate evolutionary patterns in ray-finned fishes across the K/Pg mass extinction 66 million years ago (Ma), using microfossils (isolated teeth) preserved in a South Pacific sediment core spanning 72–43 Ma. Our record does not show significant turnover of fish tooth morphotypes at the K/Pg boundary: only two of 48 Cretaceous tooth morphotypes disappear at the event in the South Pacific, a rate no different from background extinction. Capture–mark–recapture analysis finds two pulses of origination in fish tooth morphotypes following the mass extinction. The first pulse, at approximately 64 Ma, included short-lived teeth, as well as forms that contribute to an expansion into novel morphospace. A second pulse, centred at approximately 58 Ma, produced morphotype novelty in a different region of morphospace from the first pulse, and contributed significantly to Eocene tooth morphospace occupation. There was no significant increase in origination rates or expansion into novel morphospace during the early or middle Eocene, despite a near 10-fold increase in tooth abundance during that interval. Our results suggest that while the K/Pg event had a minor impact on fish diversity in terms of extinction, the removal of the few dominant Cretaceous morphotypes triggered a sequence of origination events allowing fishes to rapidly diversify morphologically, setting the stage for exceptional levels of ray-finned fish diversity in the Cenozoic.