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    Evolutionary Dynamics of Eocene Antarctic Fishes

    (FWF-Project P26465-B25)


    Primary Investigator: Univ.-Prof. Dr. Jürgen Kriwet

    Background

    The Palaeogene was one of the most important time intervals in global climatic developments characterized, inter alia, by a late Eocene transition from the greenhouse world to icehouse conditions (ca. 49-34 Ma). The final cooling phase across the Eocene-Oligocene (E-O) boundary (ca. 33.7 Ma) resulted in the thermal isolation of Antarctica and the establishment of large Antarctic ice sheets. These climatic changes, which persisted into the earliest Oligocene resulted in major biotic turnovers in marine and terrestrial floras and faunas. Today´s Southern Ocean, which is delimited by the circum-Antarctic current (Antarctic Convergence) and the Antarctic continent, which is located within it are amongst the most remote and coldest places in the world and are both a key element in any model of Earth processes and climatic changes as well as a site of unique evolutionary traits related to the abiotic characters. The extant fish fauna within the Antarctic Convergence is striking in its low taxonomic diversity and high number of endemic taxa. The chondrichthyan fauna is extremely impoverished compared to the modern teleost fauna and this situation was similar in the Eocene.
    The project aims at documenting and analysing the biotic effects of both short-term and long-term climate and palaeogeographic changes in Antarctica focusing on the taxonomic composition and diversity dynamics of Eocene Antarctic holocephalan and elasmobranchian fishes, which will serve as model organisms for evolutionary patterns in high-latitudes. Analysing originations, extinctions, diversity and diversification patterns and the palaeoecology of chondrichthyans in combination with extrinsic factors, which might influence evolutionary processes (e.g., climatic changes, palaeogeographic constellations) throughout the Eocene until the thermal and geographic isolation of Antarctica will not only provide deeper insights into adaptive and evolutionary patterns of high-latitude cartilaginous fishes but also into the development and probably the origin of the conspicuous modern-day Antarctic fish fauna with no resident holocephalans and sharks. Previous hypotheses stating, for instance, that there is a continuous diversity increase until the middle Eocene and that the absence of chondrichthyans in the uppermost Eocene of Antarctica is the result of the onset of the thermal isolation of the Antarctic continent will be tested with rigorous methodological approaches. The figure displays several elasmobranch remains from the Eocene of Seymour Island: Tooth of Carcharocles sokolovi in lingual (A) and labial (B) views; fin spine of Squalus sp. (C); a rostral spine of Pristiophorus laevis in dorsal view (D); tooth of a sandtiger shark in labial view (E).

    Locality and Material

    The material that forms the basis of this project was assembled by an Argentine-Swedish field party as a joint project of the Instituto Antártico Argentino (IAA) and the Swedish Polar Secretary (SPFS) and is housed in the palaeozoological collections of the Swedish Museum of Natural History (NRM). This abundant new material of cartilaginous fishes from all stratigraphic levels of the La Meseta Fm. of Seymour Island (Antarctic Peninsula) was collected during three Antarctic summer campaigns (SWEDARP 2011 – 2013). Further field campaigns are planned for 2014 and 2015. The material was obtained by surface collecting and screen-washing of bulk samples. Currently, the NRM collection comprises > 3.500 specimens (isolated dental plates, teeth, placoid scales, fin spines, etc.). The significance of this new material is: (1) it represents the largest collection of cartilaginous fish remains from the Eocene of Antarctica up to now, (2) it includes abundant new material of hitherto incompletely known but also new taxa, (3) it contains the first chondrichthyan records from the upper most parts of the Antarctic Eocene and (4) it contains a highly diverse microvertebrate fauna including ample micro-teeth and placoid scales from different Eocene levels of Antarctica. This is the most complete collection of chondrichthyans from the Eocene of Antarctica in terms of number of specimens, taxonomic covering and stratigraphic distribution.

    Goals

    The ultimate goal is to present a comprehensive study of cartilaginous fish assemblages from the Eocene of Antarctica including revisions of previously published records. Integrated goals of this project are to (1) establish the taxonomic / systematic composition and stratigraphic distribution of cartilaginous fishes for each Eocene stratigraphic unit (here TELMs) of Antarctica, (2) establish the quality of their fossil record, (3) analyse the faunal relationships (Beta Diversity) of Eocene Antarctic chondrichthyan compositions, (4) study the underlying evolutionary dynamics such as origination, diversification, diversity fluctuation and extinction patterns of fishes in high latitudes during the Eocene and (5) reconstruct ecological patterns of Eocene Antarctic chondrichthyans.



    Team

    • Univ.-Prof. Dr. Jürgen Kriwet (PI) Read more
    • Dr. Andrea Engelbrecht (Predoctoral Researcher)

    Collaborations:


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    Results

    So far, the following chondrichthyan groups have been revised and/or described: Pristiophoriformes (saw sharks), Hexanchiformes (cow sharks), Squaliformes (dogfish sharks), Squatiniformes (angel sharks), Orectolobiformes (carpet sharks), and Batomorphii (skates and rays). Additionally, an analysis of the youngest and last chondrichthyan assemblage before the onset of Antarctic glaciation and a study of a single lamniform shark have been published. In total, more than 4,500 chondrichthyan remains from various institutional collections combined with newly collected material was analysed and resulted in the recognition of a highly diverse chondrichthyan fauna comprising three holocephalans, a single synechodontiform, 11 squalomorphs, 21 (probably 22) galeomorphs and five (probably six) batomorphs.

    Holocephali: Callorhinchus stahli, Chimaera seymourensis, Ischyodus dolloi
    Synechodontiformes: Paraorthacodus sp.
    Hexanchiformes: Heptranchias howelli, Hexanchus sp.
    Pristiophoriformes: Pristiophorus laevis
    Squatiniformes: Squatina sp.
    Squaliformes: Squalus sp., Squalus weltoni, Squalus woodburnei, Centrophorus sp. 1, Centrophorus sp. 2, Deania sp., Eodalatias austrinalis
    Orectolobiformes: Notoramphoscyllium woodwardi, Coelometlaouia pannucea, Orectolobiformes gen. et sp. indet. A, Orectolobiformes gen. et sp. indet. B
    Lamniformes: Anomotodon multidenticulata(?), Cetorhinus sp., Macrorhizodus praecursor, Brachycarcharias lerichei, Palaeohypotodus rutoti, Striatolamia macrota, Odontaspis winkleri, Carcharias sp. 1, Carcharias sp. 2, Carcharocles auriculatus, Carcharocles sokolovi
    Carcharhiniformes: Mustelus sp., Galeoorectopsis cristatus, Kallodentis rhytistemma, Galeorhinus sp., Abdounia richteri, Abdounia mesetae, Carcharhinus sp.
    Rajiformes: Raja manitaria, Raja amphitrita, Marambioraja leiostemma, Mesetaraja maleficapelli
    Myliobatiformes: Myliobatiformes gen. indet. (Myliobatis vel Rhinoptera)

    The stratigraphic distribution of the chondrichthyan taxa throughout the Eocene of Antarctica is depicted in Table 1 below.



    Simultaneously, additional Eocene chondrichthyan assemblages from the Southern Hemisphere (e.g., Chile) and Northern Hemisphere (e.g., Abbey Wood, UK; Monte Bolca, Italy; North Sea Basin, Germany; Morocco) were studied for comparison. This resulted in the identification and revision of various taxa from these localities that already have been or that will be published in the future. The comparative study of the Eocene Monte Bolca and Monte Pesciara chondrichthyan faunas from Italy also resulted in a separate project, because of the large number of taxa, which currently is supported by the FWF (M 2368 Meitner-Program). During the second major part of the project, which started in parallel to the first part (last 9 month of the project), we assessed differences in diversity and diversification patterns (e.g. turnover, diversification, origination and extinction rates, etc.) over a time period of 23 million years (early Eocene to Eocene-Oligocene Transition) in the Southern Ocean (Antarctica) for identifying abiotic drivers underlying possible changes. The analyses were conducted in R and with the Past software package. It is evident that global climate changed significantly throughout the Eocene and seemingly affected chondrichthyan diversity patterns in the Antarctic Ocean during the Eocene severely (Fig. 1: Diversity, origination, and extinction rates of Eocene chondrichthyans from Antarctica within the 95%CI and times of major climatic changes).

    The detailed stratigraphic and palaeoecological data indicate that chondrichthyan diversity increased from the Early Eocene to the middle Eocene in relation to the Early Eocene Climate Optimum (EECO), the Middle Eocene Climate Optimum (MECO), however, had almost no impact on diversity increase. All chondrichthyans subsequently disappeared from the Antarctic Ocean at the Eocene-Oligocene transition (EOT), when glaciation of Antarctica started and sea-surface temperatures significantly dropped. The standing diversity increased from the late Ypresian towards the Lutetian correlating with an increase in sea-surface temperatures. This high diversity equals that of contemporaneous lower latitude faunas, like those in Morocco and the UK. Pulsed extinction events are related to the disappearance of cold-water adapted taxa. In the Bartonian, a gradual decrease in species diversity occurred and the final disappearance of chondrichthyans at the end of Priabonian is to the establishment of Antarctic ice-sheets. The applied diversity indices indicate highest diversities in TELMs 5 (Ypresian) and 6 (Lutetian, Bartonian) and an unequal distribution of individuals across genera indicates that saw- and angel sharks were the dominant sharks, whereas odontaspidid sharks were dominating the chondrichthyan faunas in the lower and the upper-most part of the Eocene (Fig. 2: Quantitative distribution and standing diversity of elasmobranchs in the Eocene of Antarctica displaying the most dominant species in each TELM).

    Employed rarefaction analyses demonstrated that the sampling effort is rather uneven. Accordingly, a high quality for the fossil record of chondrichthyans is indicated for the upper TELMs, but it is less good in the lowest parts. Turnover rates were highest in the Early Eocene, whereas the diversification rate was lowest in the Early Eocene and highest in the middle Eocene. The highest origination rates (Early Eocene) and the highest extinction rates (Middle Eocene) correspond well with the EECO and late Eocene cooling, where an increase in temperature favoured origination of taxa in the Southern Ocean during the Eocene, whereas the decrease in water temperatures towards the end of the Eocene lead to local (Antarctic) and regional (Southern Hemisphere) extinction events. These results strongly support that the diversity of Eocene Antarctic chondrichthyans was linked mostly to climate changes. Habitat changes (e.g., reduced continental shelves) and sea-level fluctuations also influenced the diversity and diversification patterns of chondrichthyans in high-latitudes during the Eocene, but these factors also are dependant on climatic conditions. Palaeogeographic changes (e.g., opening of the Tasman Gateway) that resulted in changes in Antarctic Ocean circulations also might have been affected chondrichthyan diversity patterns but correlations still are ambiguous. According to our findings, global climate is the main diversity driver in marine elasmobranch faunas. Sea level also influences their diversity dynamics, but sea levels are dependant of global climates. It also is evident that highest diversity and diversification rates in the Southern Hemisphere occurred in the Eocene during times of significantly elevated global temperatures (ca. 56-40 Ma; PETM, EECO, MECC), which resulted in extensive greenhouse conditions. Increase of global temperatures, however, also triggered subordinate local extinctions, which mainly affected cold-water adapted taxa. We also analysed post-Jurassic (last 120 MA) chondrichthyan diversity and diversification patterns of the Southern Hemisphere (regional scales). Results from this analysis also support the close links between diversity changes and global climates (Fig. 3: Range-through diversity of post-Jurassic elasmobranch fishes of the Southern Hemisphere (1 million year bins). Black curve: with singletons; red curve without singletons; green curve: sea-surface temperatures for the Cretaceous. Blue arrow: opening of trans-equatorial seaway; red arrow: South Pacific route between N. Zealand and Australia (possible invasion event). OAW: Oceanic Anoxic Event. Green bars: positive climatic excursions; blue bar: Eocene-Oligocene cooling event. Red dots: Maximum diversity peaks of elasmobranchs during the Eocene and Miocene.).

    The main conclusions from this part of the study indicate that increasing sea-surface temperatures result in high turnover rates due to local extinctions and invasion of taxa from other areas during transient climate states (on century - millennium scales), while high turnover rates during mean climate states (on million year scales) are related to elevated origination rates that exceed extinction rates, and a positive correlation between increased sea surface temperatures and increased origination/diversity rates in the since Late Cretaceous in the Southern Hemisphere. The establishment of trans-equatorial and South Pacific seaways, conversely, are only of minor importance; some invasions into the Southern Hemisphere from the North are recognized in the Campanian (supported by similarity measures). Interestingly, no negative or positive correlations between chondrichthyan diversity patterns and Oceanic Anoxic Events in the Cretaceous exist.

    This project, although not yet finished (several studies about lamniform and chimeroid fishes still commence and some manuscripts still need to be completed for submission), significantly augmented our knowledge about chondrichthyan associations in high-latitudes during one of the most crucial time periods in Earth history, the Eocene and also significantly increased our understanding of the influence of abiotic factors on their diversity patterns and what drives originations and extinctions. Innovative aspects of this project are the multidisciplinary and integrated approaches and analytical procedures, combining up-to-date fossil record and sophisticated statistic methodologies and approaches (e.g., R, shareholder quorum subsampling). In this, the project represents not only pure research but also has an applied perspective, since the evidence obtained from this study might help to make future predictions about chondrichthyan diversity patterns in relation to climate changes and consequently might assist in informing policy-makers.

    The project was also high-lighted 2014 in the media portal of the University of Vienna (https://medienportal.univie.ac.at/uniview/forschung/detailansicht/artikel/hai-society-in-der-eozaenen-antarktis/) and in "Der Standard" (https://derstandard.at/2000001941102/DieUrhaie-die-aus-der-Antarktis-kamen). We intend to make additional media releases when the manuscript concerning the influence of climate change on past chondrichthyan diversity patterns is submitted. Additionally, the project was presented during the "Lange Nacht der Forschung" (April 4, 2014).

    Scholarly Papers

    2019
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2019. Skates and Rays (Elasmobranchii, Batomorphii) from the Eocene La Meseta Formation, Seymour Island, Antarctica. Historical Biology, 31: 1028-1044. Link to article
    • Marramà, G., Engelbrecht, A., Carnevale, G. & Kriwet, J. 2019. Eocene sand tiger sharks (Lamniformes, Odontaspididae) from the Bolca Konservat-Lagerstätte, Italy: Palaeobiology, palaeobiogeography and evolutionary significance. Historical Biology, 31: 101-115. Link to article
    2018
    • Marramà, G., Claeson, K.M,, Carnevale, G. & Kriwet, J. 2018. Revision of Eocene electric rays (Torpediniformes, Batomorphii) from the Bolca Konservat-Lagerstätte, Italy, reveals the first fossil embryo in situ in batoids and provides new insights into the origin of trophic novelties in coral reef fishes. Journal of Systematic Palaeontology, 16: 1189-1219. Link to article
    • Marramà, G., Carnevale, G., Engelbrecht, A., Claeson, K.M., Zorzin, R., Fornasiero, M. & Kriwet, J. 2018. A synoptic review of the Eocene (Ypresian) cartilaginous fishes (Chondrichthyes: Holocephali, Elasmobranchii) of the Bolca Konservat-Lagerstätte, Italy. PalZ, 92: 283-313. Link to article
    • Marramà, G., Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2018. The southernmost occurrence of Brachycarcharias (Lamniformes, Odontaspididae) from the Eocene of Antarctica provides new information about the paleobiogeography and paleobiology of paleogene sand tiger sharks. Rivista Italiana di Paleontologia e Stratigrafia (Research In Paleontology and Stratigraphy) 124: 283-298. Link to article
    2017
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2017. New carcharhiniform sharks (Chondrichthyes, Elasmobranchii) from the early to middle Eocene, of Seymour Island, Antarctic Peninsula. Journal of Vertebrate Paleontology, 37: e1371724 (25 pages). Link to article
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2017. A new sawshark, Pristiophorus laevis, from the Eocene of Antarctica with comments on Pristiophorus lanceolatus. Historical Biology 29: 841-853 Link to article
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2017. Eocene squalomorph sharks (Chondrichthyes, Elasmobranchii) from Antarctica. The Journal of South American Earth Sciences.Historical Biology 78: 175-189. Link to article
    • Schwarzhans, W., Mörs, T., Engelbrecht, A., Reguero, M. & Kriwet, J. 2017. Before the freeze: Otoliths from the Eocene of Seymour Island, Antarctica, reveal dominance of gadiform fishes (Teleostei). Journal of Systematic Palaeontology 15(2): 147-170. Link to article
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2017. Revision of Eocene Antarctic carpet sharks (Elasmobranchii, Orectolobiformes) from Seymour Island, Antarctic Peninsula. Journal of Systematic Palaeontology 15: 969-990.Link to article
    2016
    • Kriwet, J., Engelbrecht, A., Mörs, T., Reguero, M. & Pfaff, C. 2016. Ultimate Eocene (Priabonian) chondrichthyans (Holocephali, Elasmobranchii) of Antarctica. Journal of Vertebrate Paleontology 36: e1160911 (19 pages).

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    Conference Abstracts

    2019
    • Kim, S., Zeichner, S.S., Colman, A.S., Sher, H. & Kriwet, J. 2019. Navigating the Drake Passage during the Eocene greenhouse to icehouse climate transition: a paleoecological and geochemical perspective based on sand tiger shark Striatolamia macrota teeth. AGU100 Fall Meeting, San Francisco, U.S.A., Abstracts.

    2017
    • Kriwet, J., Mörs, T., Kiessling, W. & Engelbrecht, A. 2017: Drivers of post-Jurassic diversity dynamics of southern hemisphere elasmobranchs (Vertebrata, Chondrichthyes). Libro de Resúmenes, Reunión de Paleontología de Vertebrados de Chile: 11.
    • Kriwet, J., Mörs, T., Reguero, M.A., Kiessling, W. & Engelbrecht, A. 2017. Lessons from the past: Diversity dynamics are linked to climate change in elasmobranchs (Vertebrata, Chondrichthyes) in deep-time. The 21st European Elasmobranch Association Annual Scientific Concerence, Amsterdam, Abstracts: 60.
    • Kriwet, J., Mörs, T., Reguero, M.A., Kiessling, W. & Engelbrecht, A. 2017. Diversity dynamics are linked to climate change in cartilaginous fishes (Chondrichthyes, Holocephali Elasmobranchii) from the Eocene of Antarctica. Journal of Vertebrate Palaeontology, Program and Abstracts: 145.
    2016
    • Engelbrecht, A., Mörs, T., Reguero, M. & Kriwet, J. 2016. Small sharks - big surprise: New information on diversity patterns of Eocene Antarctic chondrichthyes. In: Niebuhr, B., Wilmsen, M., Kunzmann, L. & Stefen, C. (eds.): Fossils: Key to evolution, stratigraphy and palaeoenvironments: 49; Saxoprint GmbH, Dresden.
    2015
    • Engelbrecht, A., Kriwet, J., Mörs, T. & Reguero, M. 2015. Revision of Eocene Antarctic carpet sharks and ground sharks (Chondrichthyes, Orectolobiformes, Carchariniformes). Journal of Vertebrate Paleontology, Program and Abstracts: 125.
    • Engelbrecht, A., Mörs, T., Reguerro, M. & Kriwet, J. 2015. New information on Eocene Antarctic Chondrichthyan diversity. NOBIS, Program and Abstracts: 20.
    • Kaineder, G., Pfaff, C. & Kriwet, J. 2015. Reduced ossification in the dentary bone of notothenioid ice-fishes (Teleostei: Perciformes). NOBIS, Program and Abstracts: 29.
    2014
    • Engelbrecht, A., Kriwet, J., Mörs, T. & Reguero, M. 2014. Diversity of Eocene Antarctic sand tiger sharks (Chondrichthyes, Odontaspididae): Climatic controls or implications for nursery areas? Journal of Vertebrate Palaeontology, Program and Abstracts: 125.
    • Engelbrecht, A., Kriwet, J., Mörs, T., Pfaff, C. & Reguero, M. 2014. New information on diversity patterns of Eocene Antarctic sharks, skates and rays (Chondrichthyes, Elasmobranchii). XXXIII SCAR Open Science Conference and COMNAP Symposium Success through International Cooperation: 407.
    • Engelbrecht, A., Kriwet, J., Mörs, T., Schwarz, C. & Reguero, M. 2014. Origin of Antarctic ice-fishes (Teleostei, Notothenioidei): Current controversies and facts. XXXIII SCAR Open Science Conference and COMNAP Symposium Success through International Cooperation: 716.
    • Kriwet, J., Engelbrecht, A., Reguero, M. & Mörs, T. 2014. Eocene Antarctic fish diversity patterns revisited. XII Annual Meeting of the European Association of Vertebrate Paleontologists: 192.
    • Mörs, T., Engelbrecht, A., Kriwet, J., Schwarz, C. & Reguero, M. 2014. Origin of modern Antarctic ice-fishes (Teleostei, Notothenioidei) and the identity of Eocene fish remains from Seymour Island, Antarctica. 4th International Palaeontological Congress - The history of life: A view from the Southern Hemisphere: 2019.
    2013
    • Engelbrecht, A., Kriwet, J., Mörs, T., Reguero, M. & Schwarz, C. 2013. New information on the cranial anatomy of ice-fishes (Teleostei, Notothenioidei) from Antarctica based on micro-CT analyse. 10. Tagung der Gesellschaft für Ichthyologie (GfI): 15.
    • Engelbrecht, A., Kriwet, J., Mörs, T., Schwarz, C., Reguero, M. & Tambussi, C. 2013. A revision of Eocene Antarctic fishes (Vertebrata: Neopterygii: Teleostei). In Reitner, J., Qun, Y., Yongdong, W. & Reich, M. (eds): Palaeobiology and Geobiology of Fossil Lagerstätten through Earth History: 42.

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