Abstract

A worldwide revision of the Cretaceous record of Neornithes (crown birds) revealed that unambiguous neornithine taxa are extremely scarce, with only a few showing diagnostic features to be confidently assigned to that group. Here we report two new neornithine specimens from Vega Island (López de Bertodano Formation). The first is a synsacrum (MN 7832-V) that shows a complex pattern of transversal diverticula intercepting the canalis synsacri, as in extant neornithines. Micro-CT scanning revealed a camerate pattern of trabeculae typical of neornithines. It further shows the oldest occurrence of lumbosacral canals in Neornithes, which are related to a balance sensing system acting in the control of walking and perching. The second specimen (MN 7833-V) is a distal portion of a tarsometatarsus sharing with Vegavis iaai a straight apical border of the crista plantaris lateralis. Osteohistologically the tarsometatarsus shows a thick and highly vascularized cortex that lacks any growth marks, resembling Polarornis gregorii. The cortex is osteosclerotic as in other extinct and extant diving neornithines. These new specimens increase the occurrences of the Cretaceous avian material recovered from the Upper Cretaceous strata of the James Ross Sub-Basin, suggesting that a Vegaviidae-dominated avian assemblage was present in the Antarctic Peninsula during the upper Maastrichtian.

Key words
Mesozoic birds; Neornithes; Vegavis; Antarctica; James Ross

INTRODUCTION

Research in Antarctica has been increasing worldwide with constant investment and collaboration among researchers from different countries (e.g., Sampaio 2022SAMPAIO DP. 2022. Diplomatic culture and institutional design: Analyzing sixty years of Antarctic Treaty governance. 2022. An Acad Bras Cienc 94: e20210539.), resulting in projects with increasing complexity (e.g., Simões et al. 2022SIMÕES JC, CARTES ML & SAYÃO JM. 2022. Forty years of Brazilian Antarctic research: A tribute to Professor Antonio Carlos Rocha-Campos. An Acad Bras Cienc 94: e20220493.). Despite the several challenges to developing studies in this region, there has been a steady increase of scientific activity in the area (e.g., Kellner 2022KELLNER AWA. 2022. Research in Antarctica - challenging but necessary. An Acad Bras Cienc 94: e202294S1., Santos et al. 2022SANTOS A ET AL. 2022. Paleoenvironment of the Cerro Negro Formation (Aptian, Early Cretaceous) of Snow Island, Antarctic Peninsula. An Acad Bras Cienc 94: e20201944.), which includes the search for fossil vertebrates (e.g., Reguero et al. 2022REGUERO MA ET AL. 2022. Late Campanian-Early Maastrichtian Vertebrates from the James Ross Basin, West Antarctica: Updated Synthesis, Biostratigraphy, and Paleobiogeography. An Acad Bras Cienc 94: e20211142.), including extinct birds.

Among the most interesting deposits for paleontology in Antarctica are the layers of Upper Cretaceous-Paleogene sequence that filled the James Ross Sub-Basin, in the northeastern margin of the Antarctic Peninsula. These beds are considered the most significant sedimentary sequence from high latitudes for this time interval and have yielded a diverse fossil assemblage from terrestrial and marine environments such as araucariacean (Césari et al. 2001CÉSARI SN, MARENSSI SA & SANTILLANA SN. 2001. Conifers from the Upper Cretaceous of Cape Lamb, Vega Island, Antarctica. Cretac Res 22: 309-319.), angiosperms (Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), scleractinian corals (Videira-Santos et al. 2020VIDEIRA-SANTOS R, SCHEFFLER SM, PONCIANO LCMO, WEINSCHÜTZ LC, FIGUEIREDO RG, RODRIGUES T, SAYÃO JM, RIFF DS & KELLNER AWAK. 2020. First description of scleractinian corals from the Santa Marta and Snow Hill Island (Gamma Member) formations, Upper Cretaceous, James Ross Island, Antarctica. Ad Polar Sci 31: 205-214.), serpulid worms and molluscans (e.g., Olivero et al. 1986OLIVERO EB, SCASSO RA & RINALDI CA. 1986. Revision of the Marambio Group, James Ross Island, Antarctica. Contrib Cient Inst Antart Argent 331: 1-28., Crame & Luther 1997CRAME JA & LUTHER A. 1997. The last inoceramid bivalves in Antarctica. Cretac Res 18: 179-195., Olivero 2012aOLIVERO EB. 2012a. New Campanian kossmaticeratid ammonites from the James Ross Basin, Antarctica, and their possible relationships with Jimboiceras? antarcticum Riccardi. Rev Paléobiol 11: 133-149., Raffi et al. 2019RAFFI ME, OLIVERO EB & MILANESE FN. 2019. The gaudryceratid ammonoids from the Upper Cretaceous of the James Ross Basin, Antarctica. Acta Palaeontol Pol 64: 3.), crustaceans (Pinheiro et al. 2020PINHEIRO AP, SARAIVA AAF, SANTANA W, SAYÃO JM, FIGUEIREDO RG, RODRIGUES T, WEINSCHÜTZ LC, PONCIANO LCMO & KELLNER AWAK. 2020. New Antarctic clawed lobster species (Crustacea: Decapoda: Nephropidae) from the Upper Cretaceous of James Ross Island. Polar Res 39: 3727.), chondrichthyans (e.g., Otero et al. 2014OTERO RA, SOTO-ACUÑA S, VARGAS AO, RUBILAR-ROGERS D, YURY-YÁÑEZ RE & GUTSTEIN CS. 2014. Additions to the diversity of elasmosaurid plesiosaurs from the Upper Cretaceous of Antarctica. Gond Res 26: 772-784.), osteichthyans (e.g., Richter & Ward 1990RICHTER M & WARD DJ. 1990. Fish remains from the Santa Marta Formation (Late Cretaceous) of James Ross Island, Antarctica. Antarctic Sci 2: 67-76.), plesiosaurs (e.g., Chatterjee & Small 1989CHATTERJEE S & SMALL BJ. 1989. New plesiosaurs from the Upper Cretaceous of Antarctica. Geol Soc London Spec Pub 47: 197-215., Kellner et al. 2011KELLNER AWA ET AL. 2011. The oldest plesiosaur (Reptilia, Sauropterygia) from Antarctica. Polar Res 30: 1-6., O’Gorman 2012O’GORMAN JP. 2012. The oldest elasmosaurs (Sauropterygia, Plesiosauria) from Antarctica, Santa Marta Formation (upper Coniacian? Santonian–upper Campanian) and Snow Hill Island Formation (upper Campanian–lower Maastrichtian), James Ross Island. Polar Res 31: 11090., O’Gorman et al. 2019O’GORMAN JP, SANTILLANA S, OTERO R & REGUERO M. 2019. A giant elasmosaurid (Sauropterygia, Plesiosauria) from Antarctica: new information on elasmosaurid body size diversity and aristonectine evolutionary scenarios. Cretac Res 102: 37-58., Brum et al. 2022BRUM AS, SIMÕES TR, SOUZA GA, PINHEIRO AEP, FIGUEIREDO RG, CALDWELL MW, SAYÃO JM & KELLNER AWAK. 2022. Ontogeny and evolution of the elasmosaurid neck highlight greater diversity of Antarctic plesiosaurians. Palaeontology 65: e12593.), mosasaurs (Martin et al. 2002MARTIN JE, BELL GL, CASE JA, CHANEY DS, FERNÁNDEZ MS, GASPARINI Z & WOODBURNE MO. 2002. Late Cretaceous mosasaurs (Reptilia) from the Antarctic Peninsula. Royal Society of New Zealand Bulletin 35: 293-299., Novas et al. 2002aNOVAS FE, CAMBIASO A, LÍRIO JM & NUÑES HJ. 2002b. Paleobiogeografía de los dinosaurios polares de Gondwana. Ameghiniana 39: 15R., Martin 2006MARTIN JE. 2006. Biostratigraphy of the Mosasauridae (Reptilia) from the Cretaceous of Antarctica. In: PIRRIE JE & CRAME JA (Eds). Cretaceous-Tertiary high-latitude palaeoenvironments, James Ross basin, Antarctica. Geol Soc Spec Publ 258: 101-108.), pterosaurs (Kellner et al. 2019KELLNER AWA, RODRIGUES T, COSTA FR, WEINSCHÜTZ LC, FIGUEIREDO RG, SOUZA GA, BRUM AS, ELEUTÉRIO LHS, MUELLER CW & SAYÃO JM. 2019. Pterodactyloid pterosaur bones from Cretaceous deposits of the Antarctic Peninsula. An Acad Bras Cienc 91: e20191300.), and avian and non-avian dinosaurs (Chatterjee 1989CHATTERJEE S. 1989. The oldest Antarctic bird. Journal of Vertebrate Paleontology 8: 11A., Noriega & Tambussi 1995NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61., Case & Tambussi 1999CASE JA & TAMBUSSI CP. 1999. Maastrichtian record of neornithine birds in Antarctica: comments on a Late Cretaceous radiation of modern birds. In: ABSTRACTS OF PAPERS, Journal of Vertebrate Paleontology, p. 37A., Case et al. 2000CASE JA, MARTIN JE, CHANEY DS, REGUERO M, MARENSSI SA, ANTILLANA SM & WOODBURNE MO. 2000. The first duck-billed dinosaur (family Hadrosauridae) from Antarctica. J Vertebr Paleontol 20: 612-614., 2006CASE JA, MARTIN JE & REGUERO M. 2007. A dromaeosaur from the Maastrichtian of James Ross Island and the Late Cretaceous Antarctic dinosaur fauna. US Geological Survey Short Research Paper 083: 1-4., 2007, Case 2001CASE JA. 2001. Latest Cretaceous record of modern birds from Antarctica: center of origin or fortuitous occurrence? In: NORTH AMERICAN PALEONTOLOGICAL CONVENTION 2001, Berkeley: https://ucmp.berkeley.edu/napc/abs5.html#CaseJ.
https://ucmp.berkeley.edu/napc/abs5.html... , Cordes 2001CORDES AH. 2001. A Basal charadriiform bird from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. (Master’s thesis) South Dakota School of Mines and Technology, Rapid City, 142 p., 2002CORDES AH. 2002. A new charadriiform avian specimen from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. J Vertebr Paleontol 22: 46A., Novas et al. 2002bNOVAS FE, FERNÁNDEZ MS, DE GASPARINI ZB, LÍRIO JM, NUÑEZ HJ & PUERTA P. 2002a. Lakumasaurus antarcticus, n. gen. et sp., a new mosasaur (Reptilia, Squamata) from the Upper Cretaceous of Antarctica. Ameghiniana 39: 245-249., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., Chatterjee et al. 2006CHATTERJEE S, MARTIONI D, NOVAS FE, MUSSEL F & TEMPLIN R. 2006. A new fossil loon from the Late Cretaceous of Antarctica and early radiation of foot-propelled diving birds. J Vertebr Paleontol 26: 49A-49A., Tambussi & Acosta Hospitaleche 2007TAMBUSSI C & ACOSTA HOSPITALECHE C. 2007. Aves antàrticas (Neornithes) durante el lapso cretácico-eoceno. Rev Asoc Geol Argent 62: 604-617., Reguero et al. 2013REGUERO MA, TAMBUSSI CP, CORIA RA & MARENSSI SA. 2013. Late Cretaceous dinosaurs from the James Ross Basin, west Antarctica. Geol Soc London Spe Pub 381: 99-116., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72., Brum et al. 2023BRUM AS, ELEUTÉRIO LHS, SIMÕES TR, WHITNEY MR, SOUZA GA, SAYÃO JM & KELLNER AWAK. 2023. Ankylosaurian body armor function and evolution with insights from osteohistology and morphometrics of new specimens from the Late Cretaceous of Antarctica. Paleobiology: 1-22.). All these discoveries have contributed to a better understanding of the Weddellian Biogeographic Province biota (sensu Zinsmeister 1979ZINSMEISTER WJ. 1979. Biogeographic significance of the Late Mesozoic and early Tertiary molluscan faunas of Seymour Island (Antarctic Peninsula) to the final break-up of Gondwanaland. In: GRAY J & BOUCOT AJ (Eds). Historical biogeography, plate tectonics and the changing environment. Corvallis: Oregon State University Press, p. 349-355.) that occurred in the Patagonia-Antarctica-New Zealand-Australia corridor during the Late Cretaceous-Eocene. Among the Mesozoic taxa found in James Ross Sub-Basin, birds comprise some of the most interesting records (Chatterjee 2002CHATTERJEE S. 2002. The morphology and systematics of Polarornis, a Cretaceous loon (Aves: Gaviidae) from Antarctica. In: ZHOU Z & ZHANG F (Eds), Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution, Beijing: Science Press, China, p. 125-155., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., Tambussi & Acosta Hospitaleche 2007TAMBUSSI C & ACOSTA HOSPITALECHE C. 2007. Aves antàrticas (Neornithes) durante el lapso cretácico-eoceno. Rev Asoc Geol Argent 62: 604-617., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.). Two nominal species have been recognized: Vegavis iaai Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308. and Polarornis gregorii Chatterjee 2002CHATTERJEE S. 2002. The morphology and systematics of Polarornis, a Cretaceous loon (Aves: Gaviidae) from Antarctica. In: ZHOU Z & ZHANG F (Eds), Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution, Beijing: Science Press, China, p. 125-155.. Besides them, an array of fragmentary remains of uncertain affinities have been reported (e.g., Ornithurae indet., Aves indet., Neornithes indet., Charadriiformes indet. Case & Tambussi 1999CASE JA & TAMBUSSI CP. 1999. Maastrichtian record of neornithine birds in Antarctica: comments on a Late Cretaceous radiation of modern birds. In: ABSTRACTS OF PAPERS, Journal of Vertebrate Paleontology, p. 37A., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72., Case 2001CASE JA. 2001. Latest Cretaceous record of modern birds from Antarctica: center of origin or fortuitous occurrence? In: NORTH AMERICAN PALEONTOLOGICAL CONVENTION 2001, Berkeley: https://ucmp.berkeley.edu/napc/abs5.html#CaseJ.
https://ucmp.berkeley.edu/napc/abs5.html... , Cordes 2001CORDES AH. 2001. A Basal charadriiform bird from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. (Master’s thesis) South Dakota School of Mines and Technology, Rapid City, 142 p., 2002). Vegavis and the putative neornithine Polarornis help in depicting the radiation of crown neornithines through the Maastrichtian, near the K-Pg extinction (e.g., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308.). Along with Asteriornis maastrichtensis Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401., from the upper Maastrichtian of Belgium, these are the only pre-Cenozoic fossils unambiguously assigned to crown birds (Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401.).

Here we present a review of the Mesozoic neornithines (equivalent to the bird crown group) with emphasis on the Antarctic fossils from the James Ross Sub-Basin and their role in a broader neornithine evolutionary context. We further report new bird specimens from the López de Bertodano Formation, comprising a partial synsacrum and a fragmentary tarsometatarsus collected from 40 m above the levels where Vegavis remains were recovered.

Institutional abbreviations

GPMK – Geologisch-Paläontologisches Institut und Museum, Germany, MACN-PV – Museo Argentino de Ciencias Naturales, Argentina, MLP – División Paleontología Vertebrados of the Museo de La Plata, Argentina, MN-A – Museu Nacional, Aves collection, Universidade Federal do Rio de Janeiro, Brazil, MN-V – Museu Nacional, Paleovertebrate Collection, Universidade Federal do Rio de Janeiro, Brazil, MPM – Paleontological Collection, Museo Regional Provincial “Padre Molina”, Argentina, NHMM – Natuurhistorisch Museum Maastricht, Netherlands, PIN – The Borissiak Paleontological Institute of the Russian Academy of Sciences, Russia, SDSM – South Dakota School of Mines and Technology, USA, TMM – Texas Memorial Museum, USA, TTU – Museum of Texas Tech University, Paleontology collection, USA, YPM – Yale Peabody Museum of Natural History, USA.

MESOZOIC NEORNITHINES

Despite the significant improvement in the understanding of Mesozoic birds during the last decades, the fossil record of the crown group of birds (i.e, Neornithes) from this era is limited worldwide. Based on the fossil record and molecular data, the split between stem and crown birds is postulated to have occurred in the Late Cretaceous around 90-100 Mya (e.g., Hedges et al. 1996HEDGES SB, PARKER PH, SIBLEY CG & KUMAR S. 1996. Continental breakup and the ordinal diversification of birds and mammals. Nature 381: 226-229., Cracraft 2001CRACRAFT J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous −Tertiary mass extinction event. Proc R Soc Lond 268: 459-469., Agnolín et al. 2006AGNOLÍN FL, NOVAS FE & LIO G. 2006. Neornithine bird coracoid from the Upper Cretaceous of Patagonia. Ameghiniana 43: 245-248., Ericson et al. 2006ERICSON PGP, ANDERSON CL, BRITTON T, ELZANOWSKI A, JOHANSSON US, KÄLLERSJÖ M, OHLSON JI, PARSONS TJ, ZUCCON D & MAYR G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2: 543-547., Worthy et al. 2017WORTHY TH, DEGRANGE FJ, HANDLEY WD & LEE MSY. 2017. The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres). R Soc Op Sci 4: 170975.) or earlier in the Early Cretaceous (Cooper & Penny 1997COOPER A & PENNY D. 1997. Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence. Science 275: 1109-1113., Paton et al. 2002PATON T, HADDRATH O & BAKER AJ. 2002. Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds. Proc. R Soc Lond B 269: 839-846., Brown et al. 2008BROWN JW, REST JS, GARCÍA-MORENO J, SORENSON MD & MINDELL DP. 2008. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biol 6: 6.). Nevertheless, with few exceptions (e.g., Asteriornis, Vegavis), unambiguous stem-representatives of the three main neornithine clades Panpalaeognathae (ratites and tinamous), Pangalloanserae (landfowl and waterfowl), and Neoaves (all the remaining crown birds) from this time are mostly represented by highly fragmentary and poorly preserved specimens, sparking controversy about their classification (Fig. 1) (Agnolín & Novas 2012AGNOLÍN FL & NOVAS FE. 2012. A carpometacarpus from the Upper Cretaceous of Patagonia sheds light on the Ornithurine bird radiation. Paläontol Z 86: 85-89.). The underrepresentation of neornithines during the Cretaceous may result from their lower abundance in the Mesozoic ecosystems relative to other contemporaneous avian lineages, such as Hesperornithiformes, Enantiornithiformes, and Ichthyornithiformes (Chiappe 1996CHIAPPE LM. 1996. Late Cretaceous birds of southern South America: anatomy and systematics of Enantiornithes and Patagopteryx deferrariisi. Münchner geowissenschaftliche abhandlungen 30: 203-244., Clarke & Chiappe 2001CLARKE JA & CHIAPPE LM. 2001. A New Carinate Bird from the Late Cretaceous of Patagonia (Argentina). Am Mus Nov. 2001: 1-24., Alvarenga & Nava 2005ALVARENGA H & NAVA WR. 2005. Aves Enantiornithes do Cretáceo Superior da Formação Adamantina do Estado de São Paulo, Brasil. In: KELLNER AWA, HENRIQUES DDR & RODRIGUES T (Eds) BOLETIN DE RESUMOS II CONGRESO LATINOAMERICANO DE PALEONTOLOGIA DE VERTEBRADOS, Rio de Janeiro. Rio de Janeiro: Museu Nacional, p. 20., Fountaine et al. 2005FOUNTAINE TM, BENTON MJ, DYKE GJ & NUDDS RL. 2005. The quality of the fossil record of Mesozoic birds. Proc of the Royal Soc B: Biological Sciences 272: 289-294., O’Connor & Forster 2010O’CONNOR PK & FORSTER CA. 2010. A Late Cretaceous (Maastrichtian) avifauna from the Maevarano Formation, Madagascar. J Vertebr Paleontol 30: 1178-1201.) rather than any taphonomic bias, as it was argued (e.g., Cooper & Penny 1997COOPER A & PENNY D. 1997. Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence. Science 275: 1109-1113., Bleiweiss 1998BLEIWEISS R. 1998. Fossil gap analysis supports early Tertiary origin of trophically diverse avian orders. Geology 26: 323-326., Pacheco et al. 2011PACHECO MA, BATTISTUZZI FU, LENTINO M, AGUILAR RF, KUMAR S & ESCALANTE AA. 2011. Evolution of Modern Birds Revealed by Mitogenomics: Timing the Radiation and Origin of Major Orders. Mol Biol Evol 28: 1927-1942.). As a result, the origin and early evolution of the crown birds are still poorly understood. Notwithstanding, relevant Cretaceous records of neornithines are found in both northern and southern higher paleolatitudes.

Figure 1
A generalized timecalibrated phylogeny of Mesozoic birds. The time of divergences of the non-neornithine nodes follows Wang & Lloyd (2016)WANG M & LLOYD GT. 2016. Rates of morphological evolution are heterogeneous in Early Cretaceous birds. Proc Royal Soc B Biol Scie 283: 20160214.. The split of neornithines in the Early Cretaceous follows Hedges et al. (1996)HEDGES SB, PARKER PH, SIBLEY CG & KUMAR S. 1996. Continental breakup and the ordinal diversification of birds and mammals. Nature 381: 226-229. and Ericson et al. (2006)ERICSON PGP, ANDERSON CL, BRITTON T, ELZANOWSKI A, JOHANSSON US, KÄLLERSJÖ M, OHLSON JI, PARSONS TJ, ZUCCON D & MAYR G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2: 543-547.. The positioning of the neornithines is according to Clarke (2004)CLARKE JA. 2004. Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bull Am Mus Nat His 286: 1-179. for Apatornis celer and Iaceornis marshi, McLachlan et al. (2017)MCLACHLAN SMS, KAISER GW & LONGRICH NR. 2017. Maaqwi cascadensis: A large, marine diving bird (Avialae: Ornithurae) from the Upper Cretaceous of British Columbia, Canada. PLoS ONE 12: e0189473. and Field et al. (2020)FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401. for Vegaviidae, De Pietri et al. (2016)DE PIETRI VL, SCOFIELD RP, ZELENKOV N, BOLES WE & WORTHY TH. 2016. The unexpected survival of an ancient lineage of anseriform birds into the Neogene of Australia: the youngest record of Presbyornithidae. R Soc Open Sci 3: 150635. for Teviornis gobiensis. Neogaeornis wetzelli, Limenavis patagonica, Kookne yeutensis, Antarcticavis capelambensis, and Australornis lovei were not submitted to any cladistic analyses. The black horizontal thick lines represent approximated temporal ranges of each taxon. Dotted lines indicate alternative positions of Vegaviidae.

The global paleogeographic maps of Figure 2 show the localities with records of Cretaceous Neornithes. The information concerning the known Mesozoic neornithines taxa and putative neornithines is summarized in Table I.

Figure 2
Global paleogeographic maps showing the localities with records of Cretaceous Neornithes. (a) Early Campanian, (b) Late Campanian-Maastrichtian. 1 - Northumberland Formation, British Columbia, Canada (Maaqwi), 2 - Niobrara Formation, Kansas, US (Apatornis and Iaceornis) but see the text to alternative position for these taxa outside Neornithes, 3 - Allen Formation, Rio Negro, Argentina (Limenavis and Lamarqueavis), 4 - Maastricht Formation, Belgium (Asteriornis), 5 - Nemegt Formation, Mongolia (Teviornis, af. Phalacrocoracidae, af. Charadriiformes), 6 - Quiriquina Formation, Chile (Neogaeornis), 7 - Chorrillo Formation, Santa Cruz, Argentina (Kookne, stratigraphic unit ranges from late Campanian to Maastrichtian), 8 - Cape Lamb Member of the Snow Hill Island Formation, Vega Island, Antarctica (Vegavis, Neornithes indet., and Charadriiformes indet.) and López de Bertodano Formation, Seymour Island, Antarctica (Polarornis). Yellow dots mean the Northern Hemisphere neornithines and red dots indicate the Southern Hemisphere neornithines. Plate tectonic maps of Early Campanian (~80 Mya) and Maastrichtian (~70 Mya) by C. R. Scotese (2001)SCOTESE CR. 2001. Atlas of Earth History. Vol 1, Paleogeography, PALEOMAP Project, Arlington, Texas: 52., PALEOMAP Project (www.scotese.com).

Northern Hemisphere neornithines - In the Northern Hemisphere, some well-preserved specimens help us to elucidate the gross anatomy of the first neornithines. The most impressive Mesozoic neornithine, in terms of preservation, is Asteriornis maastrichthensis Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401. from the upper Maastrichtian (66.8–66.7 Mya) of Belgium. It comprises a nearly complete 3D-preserved skull and postcranial materials (NHMM 2013 008). The combination of galliform (landfowl) and anseriform (waterfowl) features of Asteriornis support its affinities within Pangalloanserae (Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401.).

All other neornithine reports from the Northern Hemisphere are highly fragmentary and thus of controversial identification, they could be regarded either as ornithurines close related to the crown birds or as true neornithines (Hope 1999HOPE S. 1999. A new species of Graculavus from the Cretaceous of Wyoming (Aves: Neornithes). In: Olson (Ed). Avian Paleontology at the Close of the 20th Century: Proceedings of the 4th International Meeting of the Society of Avian Paleontology and Evolution, Washington, DC, June 1996. Smithsonian Contributions to Paleobiology 89: 261-266., 2002, Bono et al. 2016BONO RK, CLARKE J, TARDUNO JA & BRINKMAN D. 2016. A large ornithurine bird (Tingmiatornis arctica) from the Turonian High Arctic: climatic and evolutionary implications. Sci Rep 6: 1-8., Mayr 2017MAYR G. 2017. The Interrelationships and Origin of Crown Group Birds (Neornithes). In: MAYR G (Ed), Avian evolution: the fossil record of birds and its paleobiological significance, Chichester: J Wiley & Sons, Ltd, West Sussex, UK, p. 84-93., Mayr et al. 2018MAYR G, DE PIERTI VL, SCOFIELD RP & WORTHY TH. 2018. On the taxonomic composition and phylogenetic affinities of the recently proposed clade Vegaviidae Agnolín et al., 2017 ‒ neornithine birds from the Upper Cretaceous of the Southern Hemisphere. Cretac Res 86: 178-185.). Among them, Teviornis gobiensis Kurochkin, Dyke & Karhu 2002 possesses a set of features only present in neornithines. The specimen PIN 44991-1 was recovered from the Maastrichtian of Mongolia (Nemegt Formation) and it is represented by a crushed distal humerus, scapholunare, pisiform, carpometacarpus and phalanges (Kurochkin et al. 2002KUROCHKIN EN, DYKE GJ & KARHU AA. 2002. A new presbyornithid bird (Aves, Anseriformes) from the Late Cretaceous of southern Mongolia. Am Mus Nov: 1-11.). Teviornis was originally assigned as the sister taxon of Anseriformes Presbyornithidae. Although its systematic position has been questioned (e.g., Clarke & Norell 2004CLARKE JA & NORELL MA. 2004. New avialan remains and a review of the known avifauna from the Late Cretaceous Nemegt Formation of Mongolia. Am Mus Nov 3447: 12.), a recent reevaluation of Teviornis characters revealed a combination of features only found in presbyornithids (De Pietri et al. 2016DE PIETRI VL, SCOFIELD RP, ZELENKOV N, BOLES WE & WORTHY TH. 2016. The unexpected survival of an ancient lineage of anseriform birds into the Neogene of Australia: the youngest record of Presbyornithidae. R Soc Open Sci 3: 150635.).

Other incomplete material that was initially referred to Ornithurae and later relocated to crown birds comprises a right coracoid RBCM.EH2008.011.01120.001, collected in the upper Campanian Northumberland Formation, in British Columbia, Canada (Dyke et al. 2011DYKE G, XIA W & KAISER G. 2011. Large fossil birds from a Late Cretaceous marine turbidite sequence on Hornby Island (British Columbia). Can J Earth Sci 48: 1489-1496.). It was preserved in a concretionary mudstone nodule that, after further preparation, revealed novel details of its anatomy. A humerus, radius, and ulna were discovered in the same nodule, adjacent to the coracoid, leading to the erection of a new species named Maaqwi cascadensis (McLachlan et al. 2017MCLACHLAN SMS, KAISER GW & LONGRICH NR. 2017. Maaqwi cascadensis: A large, marine diving bird (Avialae: Ornithurae) from the Upper Cretaceous of British Columbia, Canada. PLoS ONE 12: e0189473.). The robustness of the bone cortices of Maaqwi suggested that it was adapted to diving, like modern loons and grebes (McLachlan et al. 2017MCLACHLAN SMS, KAISER GW & LONGRICH NR. 2017. Maaqwi cascadensis: A large, marine diving bird (Avialae: Ornithurae) from the Upper Cretaceous of British Columbia, Canada. PLoS ONE 12: e0189473.). Despite the fragmentary nature of Maaqwi, it was possible to perform a cladistic analysis which recovered the specimen within Vegaviidae, a recently proposed clade composed of diving foot-propelled birds endemic of Gondwana (Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.). All remaining vegaviids come from Gondwana, implying that Maaqwi is the only Laurasian representative of the group. Vegaviidae has been recovered crownward of Ichthyornithes and Hesperornithes, and in different positions across Aves (e.g., McLachlan et al. 2017MCLACHLAN SMS, KAISER GW & LONGRICH NR. 2017. Maaqwi cascadensis: A large, marine diving bird (Avialae: Ornithurae) from the Upper Cretaceous of British Columbia, Canada. PLoS ONE 12: e0189473., Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401.), as discussed later.

A third specimen composed of a relatively complete skeleton (YPM 1734) from the early Campanian Niobrara Formation (USA) shows the presence of ribs, scapulae, coracoids, partial furcula, sternum, and a partial forelimb. It was long considered to belong to the ichthyornithine Apatornis celer based on weak diagnostic avian features (e.g., keeled sternum, Marsh 1880MARSH OC. 1880. Odontornithes: a monograph on the extinct toothed birds of North America. In: United States Geological Exploration of the 40th Parallel. Washington: U.S. Government Printing Office, Washington, USA, p. 201.). However, several features found in YPM 1734 were also present in Telmabates antiquus Howard 1955HOWARD H. 1955. A new wading bird from the Eocene of Patagonia. Am Mus Novit 1710: 1-25. from the Eocene Sarmiento Formation of Patagonia (originally considered as phoenicopteriform, but now presbyiornithid). The specimen YPM 1734 presents a combination of basal ornithurine and derived neoavian features (e.g., short, angular, and expanded sternal end of the coracoid, and expanded dorsal trochlea on the carpometacarpus, Howard 1955HOWARD H. 1955. A new wading bird from the Eocene of Patagonia. Am Mus Novit 1710: 1-25.). Later, a set of features present in YPM 1734, such as the short coracoid glenoid, laterally protruding distal end of the scapular glenoid, and an elongated acromion, was used to consolidate the specimen within anseriforms (Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.). Recently, the hypodigm YPM 1734 was separated from the isolated holotype synsacrum of Apatornis (YPM 1451) and erected as a new taxon, Laceornis marshi Clake 2004. In the phylogeny of Clarke (2004)CLARKE JA. 2004. Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bull Am Mus Nat His 286: 1-179., Apatornis was recovered as an Ornithurae outside Aves, whereas Laceornis was nested within a more advanced position than Ichthyornis, but outside crown birds, thus no longer considered as a presbyiornithid neornithine.

The Cimolopterygidae forms an entire clade of avian species predominantly found in the non-marine Cretaceous sediments of Wyoming, USA. Originally, the clade included Cimolopteryx rara (Marsh 1892MARSH OC. 1892. Notes on Mesozoic vertebrate fossils. Am J Sci 44: 170-176.), Ceramornis major (Brodkorb 1963aBRODKORB P. 1963a. Birds from the Upper Cretaceous of Wyoming. In: XIII INTERNATIONAL ORNITHOLOGICAL CONGRESS., Lawrence, Kansas. Proceedings …, Kansas: SIBLEY CG, HICKEY JJ & HICKEY MB, p. 55-70.), Cimolopteryx maxima (Brodkorb 1963aBRODKORB P. 1963a. Birds from the Upper Cretaceous of Wyoming. In: XIII INTERNATIONAL ORNITHOLOGICAL CONGRESS., Lawrence, Kansas. Proceedings …, Kansas: SIBLEY CG, HICKEY JJ & HICKEY MB, p. 55-70.), Cimolopteryx minima (Brodkorb 1963aBRODKORB P. 1963a. Birds from the Upper Cretaceous of Wyoming. In: XIII INTERNATIONAL ORNITHOLOGICAL CONGRESS., Lawrence, Kansas. Proceedings …, Kansas: SIBLEY CG, HICKEY JJ & HICKEY MB, p. 55-70.), an array of ornithurine remains from the Maastrichtian of Saskatchewan referred to Cimolopteryx sp. (e.g., SMNH P1927.936, Tokaryk & James 1989TOKARYK TT & JAMES PC. 1989. Cimolopteryx sp. (Aves, Charadriiformes) from the Frenchman Formation (Maastrichtian), Saskatchewan. Can J Earth Sci 26: 2729-2730.; UALVP 55089, Mohr et al. 2021MOHR SR, ACORN JH, FUNSTON GF & CURRIE PJ. 2021. An ornithurine bird coracoid from the Late Cretaceous of Alberta, Canada. Canadian J Earth Scie 58: 134-140.), and indeterminate ornithurine bone fragments (Longrich 2009LONGRICH N. 2009. An ornithurine-dominated avifauna from the Belly River Group (Campanian, Upper Cretaceous) of Alberta, Canada. Cretac Res 30: 161-177.). Recently, Lamarqueavis australis was formally assigned to Cimolopterygidae by Agnolín (2010)AGNOLÍN FL. 2010. An avian coracoid from the Upper Cretaceous of Patagonia, Argentina. Stud Geol Salmant 46: 99-119., representing the only cimolopterygid from the Southern Hemisphere. Mayr (2017)MAYR G. 2017. The Interrelationships and Origin of Crown Group Birds (Neornithes). In: MAYR G (Ed), Avian evolution: the fossil record of birds and its paleobiological significance, Chichester: J Wiley & Sons, Ltd, West Sussex, UK, p. 84-93. offers an alternative perspective, suggesting that Lamarqueavis more closely resembles some gruiform birds, such as trumpeters (Psophiidae) and the early Cenozoic Messelornithidae, although the fossil remains are too fragmentary for a conclusive classification. Agnolín (2010)AGNOLÍN FL. 2010. An avian coracoid from the Upper Cretaceous of Patagonia, Argentina. Stud Geol Salmant 46: 99-119. also proposed the taxonomic reassignment of two additional species, namely L. minima and L. petra, whereby they were transferred from Cimolopteryx to Lamarqueavis. Lamarqueavis minima is based on the holotype UCMP 53976, a right coracoid discovered in the Lance Formation of Wyoming (Brodkorb 1963aBRODKORB P. 1963a. Birds from the Upper Cretaceous of Wyoming. In: XIII INTERNATIONAL ORNITHOLOGICAL CONGRESS., Lawrence, Kansas. Proceedings …, Kansas: SIBLEY CG, HICKEY JJ & HICKEY MB, p. 55-70.). Likewise, the classification of L. petra relies upon the holotype (AMNH 21911), a left coracoid also recovered from the Lance Formation (Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.).

The phylogenetic relationship of Cimolopterygidae has been neglected by many authors (Agnolín 2010AGNOLÍN FL. 2010. An avian coracoid from the Upper Cretaceous of Patagonia, Argentina. Stud Geol Salmant 46: 99-119.). In the past, it was regarded as a non-neornithine ornithurine or as a stem neornithine bird. However, Longrich et al. (2011)LONGRICH NR, TOKARYK TT & FIELD DJ. 2011. Mass extinction of birds at the Cretaceous–Paleogene (K–Pg) boundary. Proc. Natl. Acad. Sci. U.S.A 108: 15253-15257. recovered the cimolopterygids in a polytomy nesting in Neornithes, alongside Crypturellus, Iaceornis, and Galloanserae. The grade Cimolopterygidae needs a more comprehensive evaluation since its representatives could be related with the origin of the crown neornithines.

Non-Antarctic Southern Hemisphere neornithines - Outside Antarctica, some neornithines came from the Cretaceous of the Southern Hemisphere. Although these fossils are mostly comprised by poorly preserved materials, they furnish important information about the paleobiogeography of the Mesozoic birds. Most records came from South America, mainly from Argentina and Chile (e.g., Olson 1992OLSON SL. 1992. Neogaeornis wetzeli Lambrecht, a Cretaceous loon from Chile (Aves, Gaviidae). J Vertebr Paleontol 12: 122-124., Agnolín & Novas 2012AGNOLÍN FL & NOVAS FE. 2012. A carpometacarpus from the Upper Cretaceous of Patagonia sheds light on the Ornithurine bird radiation. Paläontol Z 86: 85-89., Novas et al. 2019NOVAS FE ET AL. 2019. Paleontological discoveries in the Chorrillo Formation (upper Campanian-lower Maastrichtian, Upper Cretaceous), Santa Cruz Province, Patagonia, Argentina. Rev Mus Argent Cienc Nat 21: 217-293.). Neogaeornis wetzelli Lambrecht 1929LAMBRECHT K. 1929. Neogaeornis wetzeli n. g. n. sp., der erste Kreidevogel der suedlichen Hemisphaere. Palaeontol Z 11: 121-129., from the Maastrichtian Quiriquina Formation of Chile, is based on two unrelated tarsometatarsal elements, the holotype (GMPK 123, Olson 1992OLSON SL. 1992. Neogaeornis wetzeli Lambrecht, a Cretaceous loon from Chile (Aves, Gaviidae). J Vertebr Paleontol 12: 122-124., Mayr et al. 2018MAYR G, DE PIERTI VL, SCOFIELD RP & WORTHY TH. 2018. On the taxonomic composition and phylogenetic affinities of the recently proposed clade Vegaviidae Agnolín et al., 2017 ‒ neornithine birds from the Upper Cretaceous of the Southern Hemisphere. Cretac Res 86: 178-185.) and another currently lost specimen (Schneider 1940SCHNEIDER O. 1940. La fauna fosil de Gualpen. Rev Chil de Hist Nat. 44: 49-54., Acosta Hospitaleche et al. 2023ACOSTA HOSPITALECHE C, O’GORMAN JP & PANZERI KM. 2023. A new Cretaceous bird from the Maastrichtian La Colonia Formation (Patagonia, Argentina). Cretac Res 150: 105595.). Neogaeornis was originally placed within Podicipediformes, a polyphyletic group comprised of loons, grebes, and taxa today recognized as hesperornithines (Lambrecht 1929LAMBRECHT K. 1929. Neogaeornis wetzeli n. g. n. sp., der erste Kreidevogel der suedlichen Hemisphaere. Palaeontol Z 11: 121-129.). Later, it was assigned to the podicipediform clade Baptornithidae (Brodkorb 1963bBRODKORB P. 1963b. Catalogue of fossil birds. Part 1 (Archaeopterygiformes through Ardeiformes). Bulletin of the Florida State Museum, Biol Sci 7: 179-293., Martin & Tate 1976MARTIN LD & TATE J. 1976. The skeleton of Baptornis advenus (Aves: Hesperornithiformes). In: OLSON (Ed). Collected Papers in Avian Phylogeny Honoring the 90th Birthday of Alaxander Wetmore. Smithson Contrib Paleobiol 27: 35-66.), and to the Gaviidae (Olson 1992OLSON SL. 1992. Neogaeornis wetzeli Lambrecht, a Cretaceous loon from Chile (Aves, Gaviidae). J Vertebr Paleontol 12: 122-124.), until being placed in the Vegaviidae, alongside the Antarctic birds Vegavis and Polarornis, the Paleocene Australornis lovei Mayr & Scofield 2014 (Waipara Greensand, New Zealand) and numerous unnamed specimens (Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.). The position of Neogaeornis within Vegaviidae was based on the presence of a transversely compressed tarsometatarsal shaft and a posteriorly tilted trochlea of metatarsal II.

Kookne yeutensisNovas et al. 2019NOVAS FE ET AL. 2019. Paleontological discoveries in the Chorrillo Formation (upper Campanian-lower Maastrichtian, Upper Cretaceous), Santa Cruz Province, Patagonia, Argentina. Rev Mus Argent Cienc Nat 21: 217-293., from the Maastrichtian Chorrillo Formation of Argentina, is represented by an incomplete right coracoid lacking the sternal end, with damaged proximal end (MPM 21550). It was referred to Ornithurae for having an acrocoracoid process that curves medially to embrace a wide and deep triosseous foramen, and a broad furcular articulation (Novas et al. 2019NOVAS FE ET AL. 2019. Paleontological discoveries in the Chorrillo Formation (upper Campanian-lower Maastrichtian, Upper Cretaceous), Santa Cruz Province, Patagonia, Argentina. Rev Mus Argent Cienc Nat 21: 217-293.). The authors pointed out that Kookne resembles crown birds by having a humeral articular facet anteriorly displaced relative to the scapular articular facet, scapular and humeral facets well-separated from each other, and acrocoracoid that medially wraps the triosseous foramen, and thus the specimen was referred to Neornithes, tentatively as an anseriform (Novas et al. 2019NOVAS FE ET AL. 2019. Paleontological discoveries in the Chorrillo Formation (upper Campanian-lower Maastrichtian, Upper Cretaceous), Santa Cruz Province, Patagonia, Argentina. Rev Mus Argent Cienc Nat 21: 217-293.).

The Campanian-Maastrichtian Allen Formation of Argentina has yielded a fossil association comprising the basal carinatae Limenavis patagonica (Clarke & Chiappe 2001CLARKE JA & CHIAPPE LM. 2001. A New Carinate Bird from the Late Cretaceous of Patagonia (Argentina). Am Mus Nov. 2001: 1-24.) alongside neornithine remains. The neornithines found in this unit consist of a tibiotarsus (PVL4730) dubiously attributed to a charadriiform (Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.) and an isolated but well-preserved left carpometacarpus (MML 206) (Agnolín & Novas 2012AGNOLÍN FL & NOVAS FE. 2012. A carpometacarpus from the Upper Cretaceous of Patagonia sheds light on the Ornithurine bird radiation. Paläontol Z 86: 85-89.). Although MML 206 presents apomorphic features of Neornithes (e.g., ventral rim of the proximal trochlea not in contact with the extensor process, and a shallow infratrochlear fossa), the specimen preserves insufficient data to ascribe it to any particular neornithine lineage (Agnolín & Novas 2012AGNOLÍN FL & NOVAS FE. 2012. A carpometacarpus from the Upper Cretaceous of Patagonia sheds light on the Ornithurine bird radiation. Paläontol Z 86: 85-89.).

In addition, the avian fossil record of Patagonia has revealed itself as a Gondwanan stronghold for neornithines. Additional material includes a galliform-like coracoid (PVPH 237) from the Turonian-Coniacian Portezuelo Formation of Sierra del Portezuelo, Patagonia (Agnolín et al. 2006AGNOLÍN FL, NOVAS FE & LIO G. 2006. Neornithine bird coracoid from the Upper Cretaceous of Patagonia. Ameghiniana 43: 245-248.). It is important to note that, as presented above, the neornithine remains come from beds not older than Maastrichtian, or perhaps Santonian (Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.). All neornithine records of older age (Early Cretaceous) have been questioned (e.g., Padian & Chiappe 1998PADIAN K & CHIAPPE KM. 1998. The early evolution of birds. Biological Review 73: 1-42., Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.). Thus, despite the incomplete nature of the coracoid PVPH 237, it would constitute one of the oldest known Neornithes yet recorded (Agnolín et al. 2006AGNOLÍN FL, NOVAS FE & LIO G. 2006. Neornithine bird coracoid from the Upper Cretaceous of Patagonia. Ameghiniana 43: 245-248.), which would be consistent with divergence times estimated for modern bird groups based on molecular data (Cooper & Penny 1997, Paton et al. 2002PATON T, HADDRATH O & BAKER AJ. 2002. Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds. Proc. R Soc Lond B 269: 839-846., Brown et al. 2008BROWN JW, REST JS, GARCÍA-MORENO J, SORENSON MD & MINDELL DP. 2008. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biol 6: 6.).

Additionally, Agnolín & Martinelli (2009)AGNOLÍN FL & MARTINELLI AG. 2009. Fossil birds from the Late Cretaceous Los Alamitos Formation, Río Negro Province, Argentina. J South Am Earth Sci 27: 42-49. reported numerous highly fragmentary specimens from the Campanian-Maastrichtian Los Alamitos Formation, Patagonia. The specimens represent different Ornithuromorpha/Ornithurae clades, some of them tentatively assigned to Enantiornithes, Hesperornithes, and Neornithes, reinforcing the presence of a diverse paleoavifauna in the Weddellian Province (Agnolín & Martinelli 2009AGNOLÍN FL & MARTINELLI AG. 2009. Fossil birds from the Late Cretaceous Los Alamitos Formation, Río Negro Province, Argentina. J South Am Earth Sci 27: 42-49.). Recently, a fragment of distal ulna was collected from the upper Campanian–lower Maastrichtian La Colonia Formation, outcropping at the southeastern margin of the Somún Curá Plateau, Chubut Province, Argentina (Acosta Hospitaleche et al. 2023ACOSTA HOSPITALECHE C, O’GORMAN JP & PANZERI KM. 2023. A new Cretaceous bird from the Maastrichtian La Colonia Formation (Patagonia, Argentina). Cretac Res 150: 105595.)

Antarctic neornithines -The Cretaceous neornithines from this continent comprise three nominal species Polarornis gregorii Chatterjee, 2002, Vegavis iaai Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., and Antarcticavis capelambensis Cordes-Person et al., 2020. Additionally, there is an array of poorly diagnosable specimens that have been referred to Gaviiformes (Chatterjee et al. 2006CHATTERJEE S, MARTIONI D, NOVAS FE, MUSSEL F & TEMPLIN R. 2006. A new fossil loon from the Late Cretaceous of Antarctica and early radiation of foot-propelled diving birds. J Vertebr Paleontol 26: 49A-49A., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), Charadriiformes (Case & Tambussi 1999CASE JA & TAMBUSSI CP. 1999. Maastrichtian record of neornithine birds in Antarctica: comments on a Late Cretaceous radiation of modern birds. In: ABSTRACTS OF PAPERS, Journal of Vertebrate Paleontology, p. 37A., Case 2001CASE JA. 2001. Latest Cretaceous record of modern birds from Antarctica: center of origin or fortuitous occurrence? In: NORTH AMERICAN PALEONTOLOGICAL CONVENTION 2001, Berkeley: https://ucmp.berkeley.edu/napc/abs5.html#CaseJ.
https://ucmp.berkeley.edu/napc/abs5.html... , Cordes 2001CORDES AH. 2001. A Basal charadriiform bird from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. (Master’s thesis) South Dakota School of Mines and Technology, Rapid City, 142 p., 2002), and Cariamiformes (Case et al. 2006CASE JA, REGUERO MA, MARTIN JE & CORDES-PERSON A. 2006. A cursorial bird from the Maastrichtian of Antarctica. J Vertebr Paleontol 26: 48A-48A., Tambussi & Acosta Hospitaleche 2007TAMBUSSI C & ACOSTA HOSPITALECHE C. 2007. Aves antàrticas (Neornithes) durante el lapso cretácico-eoceno. Rev Asoc Geol Argent 62: 604-617., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.).

Polarornis gregorii (TTU P 9265) comprises a partial skull, posterior cervical vertebrae, sternal fragment and ribs, femora, proximal tibiotarsus and fibula. The specimen was found in the late Campanian-Maastrichtian Lopéz de Bertodano Formation, Seymour Island, Antarctica in 1983. TTU P 9265 was assumed to belong to a stem-loon (Gaviiformes, Chatterjee, 1989, 1997, 2002, Olson 1992OLSON SL. 1992. Neogaeornis wetzeli Lambrecht, a Cretaceous loon from Chile (Aves, Gaviidae). J Vertebr Paleontol 12: 122-124., Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.), hesperornithid (Feduccia 1999FEDUCCIA A. 1999. In: The Origin and Evolution of Birds. 2nd edition. New Haven: Yale University Press, Connecticut, USA, 466 p.), or as synonymous with the Chilean bird Neogaeornis (Olson 1992OLSON SL. 1992. Neogaeornis wetzeli Lambrecht, a Cretaceous loon from Chile (Aves, Gaviidae). J Vertebr Paleontol 12: 122-124.), until Acosta Hospitaleche & Gelfo (2015)ACOSTA HOSPITALECHE C & GELFO JN. 2015. New Antarctic findings of Upper Cretaceous and Lower Eocene loons (Aves: Gaviiformes). Ann Paleontol 101: 315-324. recovered it within Pangaviiformes. Later, a distal femur and two proximal tiobiotarsi (MLP 96-I-6-2) were referred to Polarornis (Reguero et al. 2013REGUERO MA, TAMBUSSI CP, CORIA RA & MARENSSI SA. 2013. Late Cretaceous dinosaurs from the James Ross Basin, west Antarctica. Geol Soc London Spe Pub 381: 99-116., Acosta Hospitaleche & Gelfo 2015ACOSTA HOSPITALECHE C & GELFO JN. 2015. New Antarctic findings of Upper Cretaceous and Lower Eocene loons (Aves: Gaviiformes). Ann Paleontol 101: 315-324., Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.).

Another relevant taxon is Antarcticavis capelambensis (SDSM 78147) from the Cape Lamb Member (Late Campanian-Early Maastrichtian) of the Snow Hill Island Formation cropping out in Vega Island (Cordes-Person et al. 2020CORDES-PERSON A, ACOSTA HOSPITALECHE C, CASE J & MARTIN J. 2020. An enigmatic bird from the lower Maastrichtian of Vega Island, Antarctica. Cretac Res 108: 104314.). The holotype consists of dorsal vertebrae, rib fragments, synsacrum, coracoids, partial sternum, sternal ribs, humeri, proximal radius and ulnae, carpometacarpi, ilium, femora, tibiotarsi, fibula, and tarsometatarsus. SDSM 78147 was originally referred to the crown birds Charadriiformes (Cordes 2001CORDES AH. 2001. A Basal charadriiform bird from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. (Master’s thesis) South Dakota School of Mines and Technology, Rapid City, 142 p., 2002), until Cordes-Person and colleagues (2020) offered a formal publication with Zoobank’s registration number, erecting the taxon Antarcticavis capelambensis. In this paper, the authors recovered Antarcticavis as a sister taxon of Vegavis+Galloanserae.

Vegavis iaai is the most complete Cretaceous neornithine found, followed by Asteriornis. The first Vegavis specimen, MLP 93-I-3-1, was preserved in a carbonatic concretion collected during the 1992/93’ Antarctic Field expedition, supported by the Instituto Antártico Argentino (IAA), in the Sandwich Bluff Member of the López de Bertodano Formation, Vega Island. It was initially assigned to the anseriform family Presbyornithidae (Noriega & Tambussi 1995NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61.). The first identification was based on right coracoid, complete right humerus, proximal end of left humerus, distal end of right radius, synsacrum, proximal and distal ends of both femora, left tibiotarsus, proximal end of right (left of Noriega & Tambussi 1995NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61.) tarsometatarsus, distal end of left (right of Noriega & Tambussi 1995NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61.) tarsometatarsus, ribs and undetermined fragments published in the 1995 paper by Noriega & Tambussi (1995)NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61.. Later, the matrix was mechanically removed to expose the five thoracic vertebrae, two cervical vertebrae, left scapula, right ulna, all pelvic bones, right and left fibulae and left? tarsometatarsal shaft (Fig. 3), which resulted in the formal description and naming of Vegavis iaai, including a phylogenetic analysis that recovered the holotype within the crown anseriform clade Anatoidea (Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308.).

Figure 3
Map of the Antarctic Peninsula showing location of Vega Island (a). Copernicus Sentinel-2 image of ice-free portion of Cape Lamb, in Vega Island showing the locality (red dot) where the specimens studied here were collected (b). Stratigraphic interpretation of the Sandwich Bluff Member of the López de Bertodano Formation modified from Roberts et al. (2014)ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72. showing the levels where previous Vegavis specimens were found (marked by the red star) (c). Stratigraphic chart of the Marambio Group, James Ross Basin (d). Simplified schematic drawings showing all specimens unambiguously assigned to Vegavis iaai and the new avian materials studied here (white silhouettes indicate the preserved bones). See text for more details. Credit of figure b: European Union, Copernicus Sentinel-2 imagery. Abbreviations: SBM, Sandwich Bluff lithostratigraphic units recognized by Roberts et al. (2014)ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72., JRIVG, James Ross Island Volcanic Group.

Conversely, the phylogenetic affinities of Vegavis remain somewhat obscure (Ksepka & Clarke 2015KSEPKA D & CLARKE J. 2015. Phylogenetically vetted and stratigraphically constrained fossil calibrations within Aves. Palaeontol Elec 18: 1-25., Ericson et al. 2006ERICSON PGP, ANDERSON CL, BRITTON T, ELZANOWSKI A, JOHANSSON US, KÄLLERSJÖ M, OHLSON JI, PARSONS TJ, ZUCCON D & MAYR G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2: 543-547., Prum et al. 2015PRUM RO, BERV JS, DORNBURG A, FIELD DJ, TOWNSEND JP, LEMMON EM & LEMMON AR. 2015. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526: 569-573.). Such uncertainty regarding the phylogenetic position of Vegavis remains (Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9., Worthy et al. 2017WORTHY TH, DEGRANGE FJ, HANDLEY WD & LEE MSY. 2017. The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres). R Soc Op Sci 4: 170975.) even after the description of a second concretion containing more materials attributed to this species (Clarke et al. 2016CLARKE JA, CHATTERJEE S, LI Z, RIEDE T, AGNOLÍN F, GOLLER F, ISASI MP, MARTINIONI DR, MUSSEL FJ & NOVAS FE. 2016. Fossil evidence of the avian vocal organ from the Mesozoic. Nature 538: 502-505.). This new specimen, MACN-PV 19.748 (previously MLP 93-I-3-2), was collected by the same 1992/93 expedition but was only studied in the 2000s. It comprises a pterygoid, caudal portion of mandible, syrinx, cervical and thoracic series and part of the caudal series, coracoids, scapula, furcula, humerus, ulna, radius, radiale, ulnare, carpometacarpus, manual phalanges II-1 and II-2 in articulation, femora, patella, tibiotarsus, fibula, pedal phalanges, ribs, and a possible ceratobranchial element from the hyoid (Fig. 3). MACN-PV 19.748 was also treated as a presbyornithid (Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388.) or as a small sympatric, gracile specimen of Polarornis (Chatterjee et al. 2006CHATTERJEE S, MARTIONI D, NOVAS FE, MUSSEL F & TEMPLIN R. 2006. A new fossil loon from the Late Cretaceous of Antarctica and early radiation of foot-propelled diving birds. J Vertebr Paleontol 26: 49A-49A.). Later, MACN-PV 19.748 was described using micro-CT scanning and assigned to Vegavis in the 2016 paper by Clarke and colleagues, being remarkable by preserving the oldest known syrinx in the fossil record (Clarke et al. 2016CLARKE JA, CHATTERJEE S, LI Z, RIEDE T, AGNOLÍN F, GOLLER F, ISASI MP, MARTINIONI DR, MUSSEL FJ & NOVAS FE. 2016. Fossil evidence of the avian vocal organ from the Mesozoic. Nature 538: 502-505.).

In 2017, Agnolín and colleagues proposed the taxonomic name Vegaviidae, grouping Vegavis, Polarornis, the controversial Neogaeornis wetzeli, the Paleocene Australornis lovei and several unnamed specimens. By employing a version of Worthy’s basal avian analysis (Worthy et al. 2017WORTHY TH, DEGRANGE FJ, HANDLEY WD & LEE MSY. 2017. The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres). R Soc Op Sci 4: 170975.), ‘vegaviids’ were retrieved as a clade sister to Anseriformes. However, this hypothesis has not been widely accepted by paleornithologists. Mayr et al. (2018)MAYR G, DE PIERTI VL, SCOFIELD RP & WORTHY TH. 2018. On the taxonomic composition and phylogenetic affinities of the recently proposed clade Vegaviidae Agnolín et al., 2017 ‒ neornithine birds from the Upper Cretaceous of the Southern Hemisphere. Cretac Res 86: 178-185. disputed the placement of Neogaeornis, Australornis and most of the Tertiary unnamed specimens in Vegaviidae based on qualitative data, correctly observing that many characters shared with anseriforms are ambiguously present or also found in various neoavians that were not incorporated in Worthy’s matrix.

West et al. (2019)WEST AR, TORRES CR, CASE JA, CLARKE JA, O’CONNOR PM & LAMANNA MC. 2019. An avian femur from the Late Cretaceous of Vega Island, Antarctic Peninsula: removing the record of cursorial landbirds from the Mesozoic of Antarctica. PeerJ 7: e7231. re-evaluate an isolated partial femur SDSM 78247 collected 12 m up section from the horizon that yielded Vegavis (Sandwich Bluff Member of the López de Bertodano Formation). The specimen was initially reported as a Cenozoic Phorusrhacidae (‘terror birds’) or a representative of the extant Cariamidae (seriemas) within Cariamiformes (Case et al. 2006CASE JA, REGUERO MA, MARTIN JE & CORDES-PERSON A. 2006. A cursorial bird from the Maastrichtian of Antarctica. J Vertebr Paleontol 26: 48A-48A.). However, the presence of a deep, round ligament scar on the proximocaudal surface and elongated scar on its distolateral margin suggest that this isolated femur was more similar to Vegavis than other birds (West et al. 2019WEST AR, TORRES CR, CASE JA, CLARKE JA, O’CONNOR PM & LAMANNA MC. 2019. An avian femur from the Late Cretaceous of Vega Island, Antarctic Peninsula: removing the record of cursorial landbirds from the Mesozoic of Antarctica. PeerJ 7: e7231.). However, among the features that separate SDSM 78247 from Vegavis, the most remarkable is its size, approaching nearly twice that of the Vegavis femora (West et al. 2019WEST AR, TORRES CR, CASE JA, CLARKE JA, O’CONNOR PM & LAMANNA MC. 2019. An avian femur from the Late Cretaceous of Vega Island, Antarctic Peninsula: removing the record of cursorial landbirds from the Mesozoic of Antarctica. PeerJ 7: e7231.). This feature led the authors to assign SDSM 78247 to a new, unnamed, larger-bodied species within the genus Vegavis (West et al. 2019WEST AR, TORRES CR, CASE JA, CLARKE JA, O’CONNOR PM & LAMANNA MC. 2019. An avian femur from the Late Cretaceous of Vega Island, Antarctic Peninsula: removing the record of cursorial landbirds from the Mesozoic of Antarctica. PeerJ 7: e7231.). Curiously, the paleohistological analysis performed by Marsà and colleagues (2017) on V. iaai MACN-PV 19.748 pointed out that the specimen was close to, or even had reached, the somatic maturity at the time of death, based on the maturity of limb bones (humerus and femur), characterized by slow growth rates. Thus, even if there was wide variation in size within this species, it would not be expected that an individual could double in size once reaching the barrier of the adult stage, arguing in favor of two distinct species within the genus Vegavis.

After the sedimentary matrix of the holotype MLP 93-I-3-1 was removed, it was submitted to CT-scanning which resulted in the redescription with new observations of the anatomy of Vegavis (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). Although it enables the scoring of new characters into the cladistic matrix of Field and colleagues (2020), no improvement in the phylogenetic relationship of Vegavis was acquired (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). Álvarez-Herrera et al. (2023)ÁLVAREZ-HERRERA GP, ROZADILLA S, AGNOLÍN FL & NOVAS FE. 2023. Jaw anatomy of Vegavis iaai (Clarke et al., 2005) from the Late Cretaceous Antarctica, and its phylogenetic implications. Geobios (2023). have recently provided a description of the lower jaw of the specimen MACN-PV 19.748. Their analysis revealed that the anatomical characteristics of the articular region align more closely with those of neoavians, which contrasts with the anseriform signature of its postcranial skeleton.

Vegavis is recovered either together with Galliformes and Anseriformes within Pangalloanserae (Worthy et al. 2017WORTHY TH, DEGRANGE FJ, HANDLEY WD & LEE MSY. 2017. The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres). R Soc Op Sci 4: 170975., Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.), in its own family Vegaviidae also including Polarornis, Australornis lovei Mayr & Scofield 2014, and Neogaeornis wetzeli Lambrecht 1929LAMBRECHT K. 1929. Neogaeornis wetzeli n. g. n. sp., der erste Kreidevogel der suedlichen Hemisphaere. Palaeontol Z 11: 121-129. as the sister group to crown Anseriformes (Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.), or as a sister clade of Pangalloanserae+Panneoaves within Panneognathae (Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401.). The difficulty of allocating Vegavis within Pangalloanserae is expected because this species represents one of the earliest radiations of neornithine birds, exhibiting a combination of plesiomorphic neornithine features and derived ones, typical of neoavians (Álvarez-Herrera et al. 2023ÁLVAREZ-HERRERA GP, ROZADILLA S, AGNOLÍN FL & NOVAS FE. 2023. Jaw anatomy of Vegavis iaai (Clarke et al., 2005) from the Late Cretaceous Antarctica, and its phylogenetic implications. Geobios (2023).). Although there is still some debate about which taxa are assigned to Vegaviidae (Mayr et al. 2018MAYR G, DE PIERTI VL, SCOFIELD RP & WORTHY TH. 2018. On the taxonomic composition and phylogenetic affinities of the recently proposed clade Vegaviidae Agnolín et al., 2017 ‒ neornithine birds from the Upper Cretaceous of the Southern Hemisphere. Cretac Res 86: 178-185., Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.), the close relationship between Vegavis and Polarornis as members of the monophyletic clade Vegaviidae remains well supported (Mayr et al. 2018MAYR G, DE PIERTI VL, SCOFIELD RP & WORTHY TH. 2018. On the taxonomic composition and phylogenetic affinities of the recently proposed clade Vegaviidae Agnolín et al., 2017 ‒ neornithine birds from the Upper Cretaceous of the Southern Hemisphere. Cretac Res 86: 178-185.). In this work, we follow the proposal of Agnolín et al. (2017)AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9., considering Vegaviidae as a valid clade.

Dozens of isolated bird fossils have been reported from the Cape Lamb Member of the Snow Hill Island Fm. and the Sandwich Bluff Member of the Lopéz de Bertodano Fm. on Vega Island, mostly comprised of fragments. From Cape Lamb Member, we point out an incomplete tarsometatarsus (MLP 98-I-10-25) (Case & Tambussi 1999CASE JA & TAMBUSSI CP. 1999. Maastrichtian record of neornithine birds in Antarctica: comments on a Late Cretaceous radiation of modern birds. In: ABSTRACTS OF PAPERS, Journal of Vertebrate Paleontology, p. 37A., Reguero et al. 2013REGUERO MA, TAMBUSSI CP, CORIA RA & MARENSSI SA. 2013. Late Cretaceous dinosaurs from the James Ross Basin, west Antarctica. Geol Soc London Spe Pub 381: 99-116.) and incomplete trunk vertebrae (AMNH 30920) (Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), all of them have been tentatively referred to Charadriiformes. From Sandwich Member, we can cite an incomplete coracoid (AMNH 30898) provisionally referred to Aves (Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), a thoracic vertebra (AMNH FARB 30920) of an unidentified ornithurine bird (Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), a distal tarsometatarsus (AMNH FARB 30913) referred to cf. Vegavis (Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), and an avian femur and tibia from the same level as V. iaai (Coria et al. 2015CORIA RA, O’GORMAN JP, CARDENAS M, GOUIRIC-CAVALLI S, MORS T, CHORNOGUBSKY L & LOPEZ G. 2015. Late Cretaceous vertebrates from Isla Vega, Antarctica: Reports from the 2015 fieldwork. In: XXIX JORNADAS ARGENTINAS DE PALEONTOLOGÍA DE VERTEBRADOS, resumenes. Ameghiniana 52: 27-28.). Nonetheless, in most cases, the taxonomic identification of these specimens cannot be verified due to the incomplete nature of the available materials and the lack of comprehensive descriptions.

Geological and geographical setting

The material studied here was collected in Vega Island during the 2018/19’ austral summer by the PALEOANTAR project that is coordinated by the Museu Nacional/UFRJ, Brazil. Vega is a small island located northeast of James Ross Island, in the Weddell Sea, eastern flank of the Antarctic Peninsula (Fig. 3). Cape Lamb is the southern sector of the island, where sedimentary sequences that filled the James Ross Sub-Basin crop out (Del Valle et al. 1992DEL VALLE RA, ELLIOT DH & MACDONALD DIM. 1992. Sedimentary basins on the east flank of the Antarctic Peninsula: proposed nomenclature. Antarct Sci 4: 477-478.). Among the three main lithostratigraphic units of the basin, only the Santonian-Danian Marambio Group is represented in the Cape Lamb area (e.g., Crame et al. 1991CRAME JA, PIRRIE D, RIDING JB & THOMSON MRA. 1991. Campanian–Maastrichtian (Cretaceous) stratigraphy of the James Ross Island area, Antarctica. J Geol Soc 148: 1125-1140.). Marambio Group is subdivided into Santa Marta (Santonian to Middle Campanian), Snow Hill Island (Upper Campanian to Lower Maastrichtian), and López de Bertodano (Lower Maastrichtian to Lower Danian) formations (Crame et al. 2004CRAME JA, FRANCIS JE, CANTRILL DJ & PIRRIE D. 2004. Maastrichtian stratigraphy of Antarctica. Cretac Res 25: 411-423., Olivero 2012bOLIVERO EB. 2012b. Sedimentary cycles, ammonite diversity and palaeoenvironmental changes in the Upper Cretaceous Marambio Group, Antarctica. Cretac Res 34: 348-366., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.).

Previous bird remains from Vega Island were found in the upper Cape Lamb Member (upper Campanian-lower Maastrichtian), which corresponds to the top levels of Snow Hill Island Fm., and in the Sandwich Bluff Member (upper Maastrichtian), which corresponds to beds of the López de Bertodano Fm. cropping out in Vega (Case & Tambussi 1999CASE JA & TAMBUSSI CP. 1999. Maastrichtian record of neornithine birds in Antarctica: comments on a Late Cretaceous radiation of modern birds. In: ABSTRACTS OF PAPERS, Journal of Vertebrate Paleontology, p. 37A., Chatterjee et al. 2006CHATTERJEE S, MARTIONI D, NOVAS FE, MUSSEL F & TEMPLIN R. 2006. A new fossil loon from the Late Cretaceous of Antarctica and early radiation of foot-propelled diving birds. J Vertebr Paleontol 26: 49A-49A., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., Case et al. 2006CASE JA, REGUERO MA, MARTIN JE & CORDES-PERSON A. 2006. A cursorial bird from the Maastrichtian of Antarctica. J Vertebr Paleontol 26: 48A-48A.). Both units are regarded as progradational deltaic wedges to near-shore marine deposits (Crame et al. 1991CRAME JA, PIRRIE D, RIDING JB & THOMSON MRA. 1991. Campanian–Maastrichtian (Cretaceous) stratigraphy of the James Ross Island area, Antarctica. J Geol Soc 148: 1125-1140., 2004, Olivero 2012aOLIVERO EB. 2012a. New Campanian kossmaticeratid ammonites from the James Ross Basin, Antarctica, and their possible relationships with Jimboiceras? antarcticum Riccardi. Rev Paléobiol 11: 133-149., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.).

Roberts and colleagues (2014) subsequently subdivided the Sandwich Bluff Member into fifteen discrete lithostratigraphic units, termed Units SBM1 to SBM15. Some of these lithostratigraphic units represent concretionary horizons bearing spherical-subspherical and fossil nucleated concretions. The vegaviid specimens MACN-PV 19.748 and MLP 93-I-3-1 were collected from the SBM1. Unlike the other specimens of Vegavis reported in the literature, the specimens here studied were not found inside carbonatic concretions, but on a distinct bench of poorly indurated siltstone. We tentatively assigned the specimens to the horizon SBM8, however, it cannot be ruled out that the specimens may have rolled down from upper strata (particularly horizons SBM11 and SBM 12) (Fig. 3).

MATERIALS AND METHODS

Material and anatomical nomenclature

The material is housed in the Paleovertebrate collection of the Museu Nacional of Universidade Federal do Rio de Janeiro (UFRJ), Brazil. The specimens consist of three fused synsacral vertebrae lacking the respective centra (MN 7832-V) and a fragment of long bone (MN 7833-V), identified as a distal portion of a tarsometatarsus.

Measurements were taken with a digital caliper Vernier 0-150 mm. Photographs were taken using the digital camera Nikon D7200. The anatomical plates were constructed with Adobe Photoshop® CS6. We adopted the anatomical terms and views of Baumel et al. (1993)BAUMEL JJ, KING AS, BREAZILE JE, EVANS HE & VANDEN BERGE JC 1993. Handbook of avian anatomy: nomina anatomica avium., Cambridge. Publications of the Nuttall Ornithological Club, n. 23. Cambridge: Publications …, 779 p. for osteological description. Comparative material includes photographs and 3D models of Vegavis and Polarornis from the literature (Chatterjee 2002CHATTERJEE S. 2002. The morphology and systematics of Polarornis, a Cretaceous loon (Aves: Gaviidae) from Antarctica. In: ZHOU Z & ZHANG F (Eds), Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution, Beijing: Science Press, China, p. 125-155., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., 2016, Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). Extant dry skeletons examined first-hand and used for comparisons were Spheniscus magellanicus, Rhea americana, Anhinga anhinga, and Vanellus chilensis from the Aves Collection (MNA) of Museu Nacional/UFRJ.

Micro-CT scanning and tridimensional reconstructions

The synsacrum (MN 7832-V) was scanned at the Laboratório de Sedimentologia e Petrologia of the Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Porto Alegre (Brazil), using 110 kV and 72 µA. The scan resulted in 2,012 tomographic slices, with a voxel size of 21.87 µm. Digital preparation and volume rendering was performed using 3D Slicer image computing software version 4.10 freely available in slicer.org.

Microstructural analysis

The protocol of thin section preparation and paleohistological analysis was modified from Lamm (2007)LAMM ET. 2007. Paleohistology widens the field of view in paleontology. Microsc Microanal 13: 50-51.. The long bone (MN 7833-V) was embedded in epoxy resin Rp031 to produce resin blocks that protected it against saw trepidation. Although midshafts offer better information about the growth record and lead to underestimated skeletochronology (Stein & Sander 2009STEIN K & SANDER PM. 2009. Histological core drilling: a less destructive method for studying bone histology. In: BROWN MA, KANE JF & PARKER WG (Eds). Methods in fossil preparation: proceedings of the first annual Fossil Preparation and Collections Symposium. Petrified Forest: Petrified Forest National Park, p. 69-80.), MN 7833-V preserved no midshaft. Therefore, the section was done by a precision router (Dremel®, Racine, WI, USA), as close as possible to the middle part. The resin block containing the bone was fixed on a histological slide using epoxy resin Rp031. After the hardening, the block was polished to millimeter thickness using a lap wheel Politriz Aropol® VV200-PU and sandpapers Norton Saint-Gobain® T277 with P100, P600, and P1200 lines/inch sequentially. Finally, the other side was thinned and polished using the same sandpaper series. The histological slide was analyzed using a ZEISS Axioscope 5 Phase Contrast Microscope under conventional white-light reflection and transmitted circularly polarized light with 4×, 20×, or 40× objectives. Images were acquired with an Axiocam 202 mono video camera using the interface program ZEN® software. The histological terms used in the description follow Buffrénil et al. (2021)BUFFRÉNIL VD, DE RICQLÈS AJ, ZYLBERBERG L & PADIAN K. 2021. Vertebrate skeletal histology and paleohistology, 1st ed., Boca Raton: CRC Press, 826 p.. Microstructural measurements were made in ImageJ Software (Schneider et al. 2012SCHNEIDER CA, RASBAND WS & ELICEIRI KW. 2012. “NIH Image to ImageJ: 25 years of image analysis”. Nat Methods 9: 671-675.).

Because MN 7833-V exhibits moderate cortical thickness, we calculated the Relative Bone Thickness (RBT, Wall, 1983WALL W. 1983. The correlation between limb-bone density and aquatic habits in recent mammals. J Paleontol 57: 197-207.) and compared it to other fossil and extant birds (e.g., Smith & Clarke 2014SMITH NA & CLARKE JA. 2014. Osteological Histology of the Pan-Alcidae (Aves, Charadriiformes): correlates of wing-propelled diving and flightlessness. Anat Rec 297: 188-199.). RBT was calculated by dividing the mean thickness of cortex by mean diameter of the total cross-section and then multiplying by 100 (Bühler 1986BÜHLER P. 1986. Das Vogelskellet – hochentwickelter knochen-leichtbau. Arcus 5: 221-228., Chinsamy 1993CHINSAMY A. 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geol 18: 319-329.). Five sets of measurements were taken in the cross-sectional area approaching 40° from each other to obtain the mean thickness of the cortex. However, the incompleteness of the shaft prevented us from calculating the RBT at the midshaft level, which would be ideal. The histological slide was deposited in the Paleovertebrate collection of Museu Nacional/UFRJ.

RESULTS

Systematic Paleontology

Aves Linnaeus 1758

Ornithurae Haeckel 1866

Panneognathae Gauthier & de Queiroz 2001

Vegaviidae Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.

Vegavis iaai Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308.

cf. V. iaai

Material – MN 7832-V, three fused synsacral vertebrae lacking the corpus vertebrae.

Locality and horizon – Sandwich Bluff, Sandwich Bluff Member, SBM8, 9, 10, 11 or 12 of Roberts et al. (2014)ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72., approximately 40 m above the level where Vegavis specimens were recovered, López de Bertodano Formation outcropping in Cape Lamb, Vega Island, Antarctic Peninsula. Upper Maastrichtian (~ 66-68 Mya).

Description and comparisons – The specimen MN 7832-V consists of three fused synsacral neural arches 3.7 mm in length (Fig. 4). It lacks the corpus vertebrae and the most of the processus transversi. Despite its incompleteness, there are no signals of taphonomic deformation. The inner surface of the neural spines has a nacreous aspect, ranging from dusky- to dark-red colors (Fig. 4d). The proccessus spinosum and ossified tendons are ankylosed into a crista spinosa sinsacri, which is low but exceeds dorsally the processus transversi in lateral view. In Vegavis, the crista spinosa exceeds dorsally the processus transversi in synsacral vertebrae 4^th to 8^th, similarly to MN 7832-V. The dorsal surface of the crista is straight. The crista decreases in both height and thickness caudally. Two longitudinal sulci extend side by side to the crista. MN 7832-V preserves three proximalmost portions of the processus transversi. Each processus is dorsoventrally tall and mediolaterally short, being laterally rather than caudolaterally or laterocaudally projected. A laterally projected processus also occurs in the preacetabular vertebrae synsacrales in Vegavis (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). In MN 7832-V, the processus transversi lack the end that articulates with the os coxae. The processus transversi are separated by deep concave intervertebral spaces in lateral view. In the floor of these spaces, ventral to each processus transversus lies a series of small foramina intervertebralia (Fig. 4g and h). Each intervertebral space bears a small foramen. Similar foramina occur in vertebrae synsacrales 5^th to 7^th (apparently also in 4^th and 9^th) of the Vegavis holotype (MLP 93-I-3-1) (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). The smaller size and low density of foramina resemble extant diving birds such as the examined sphenicid Spheniscus magellanicus (MNA 32383, MNA 2858), the suliform Anhinga anhinga (MNA 22863, MNA 26347), rather than cursorial terrestrial Neornithes such as the ratite Rhea americana (MNA 7679) and the charadriid Vanellus chilensis (MNA7004), reinforcing the interpretation of adaptations for a foot-propelled diving ecology for MN 7832-V and Vegavis.

Figure 4
Synsacrum MN 7832-V (a-i), photographs of the specimen in (a) right lateral, (b) left lateral, (c) dorsal, and (d) ventral view. Micro CT-scan of MN 7832-V in (e) dorsal, (f) anterior, (g) left lateral, (h) posterior, and (i) ventral views. Scale bar for (a-d) = 10mm, (e-i) 5mm. Arrows indicate anterior side. Abbreviations: cs, canalis synsacri, css, crista spinosa synsacri, f, foramina intervertebralia, lsi, lumbosacral intumescence, lstc, lumbosacral transverse canals, pt, processus transversus.

Externally, the contacts between vertebrae are indiscernible. However, the absence of corpus vertebrae exposes, in ventral view, the roof of the canalis synsacri, enabling us to examine the inner structure of the neural arches (Fig. 4d and i). Internally, a sulcus extends longitudinally over the roof of the canalis synsacri, likely accommodating the spinal cord canal. The divisions of the vertebrae are represented by small recesses, identified as lumbosacral transverse canals, that intercept transversally the canal synsacri (Fig. 4i). The functional hypothesis about such canals is that they are part of a secondary balance sensing system, working similarly to the semicircular channels of the inner ear, involved in the control of walking and perching (Stanchak et al. 2020STANCHAK KE, FRENCH C, PERKEL DJ & BRUNTON BW. 2020. The balance hypothesis for the Avian lumbosacral organ and an exploration of its morphological variation. Integr Org Biol 2: obaa024., Jadwiszczak et al. 2022JADWISZCZAK P, SVENSSON-MARCIAL A & MÖRS T. 2022. An integrative insight into the synsacral canal of fossil and extant Antarctic penguins. Integr Zool 18: 237-253.). These canals are found in most neornithine groups (Jalgersma 1951JALGERSMA HC. 1951. On the sinus lumbosacralis, spina bifida occulta, and status dysraphicus in birds. Zool Meded 10: 95-105.) and, up to now, the oldest record of lumbosacral canals in a synsacrum was reported in a Maastrichthian Ornithurae FMNH PA 741 from Madagascar (O’Connor & Forster 2010O’CONNOR PK & FORSTER CA. 2010. A Late Cretaceous (Maastrichtian) avifauna from the Maevarano Formation, Madagascar. J Vertebr Paleontol 30: 1178-1201.). Thus, in the fossil Neornithes context, the specimen MV 7832-V exhibits the oldest record of the lumbosacral canals, since before they were only reported in early Sphenisciformes penguins from the Eocene of Seymour Island, Antarctic Peninsula (Jadwiszczak et al. 2022JADWISZCZAK P, SVENSSON-MARCIAL A & MÖRS T. 2022. An integrative insight into the synsacral canal of fossil and extant Antarctic penguins. Integr Zool 18: 237-253.). The canalis synsacri expands cranially, which likely corresponds to the lumbosacral intumescence (= bulla intumescentia lumbosacralis) (Fig. 4d and i) that contains the glycogen body (cranium inferior of Barkow 1856BARKOW HCL. 1856. Syndesmologie der Vógel. Breslau: Königlichen Universität, 41 p.). In living birds, this glycogen body is placed medially between two lateral rami of the spinal cord that bifurcate at the level of lumbosacral vertebrae. This feature is present in all crown birds, neornithines, ichthyornithids, and hesperornithids (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). In Vegavis, the lumbosacral intumescence reaches its maximum width around the 6^th and 7^th vertebrae (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.).

Comparison among ornithurines is restricted by the small number of specimens in which the synsacrum is preserved. The crista synsacri of MN 7832-V differs from the ornithurine UA 9601 by having a mediolaterally broader crest, whereas in UA 9601, the crest is sharp. Instead, the dorsal surface of the crista synsacri of MN 7832-V is flattened similar to Apatornis (YPM 1451). The ornithurine UA 9601 lacks the sulci bounding laterally the crista synsacri seen in MN 7832-V and in the anteriormost synsacral vertebrae of Apatornis. In UA 9601, the lumbosacral intumescence occurs around the 4^th and 5^th vertebrae, whereas in Vegavis and Apatornis it occurs in the 6^th and 7^th, which we assume to be similar to MN 7832-V. A single large foramen intervertebralis facing laterally lies on the lateral surface of the 4^th vertebra in UA 9601 and Apatornis, whereas in Vegavis and MN 7832-V, the foramina occur on the processus transversi of the 5^th, 6^th, and 7^th vertebrae. The morphology of MN 7832-V is consistent with its referral to Vegavis. Based on the morphological comparisons performed here, MN 7832-V is assigned to Vegavis, most likely representing the 5^th to 7^th vertebra synsacrales. Furthermore, both Vegavis and MN 7832-V possess a pattern of synsacral pneumaticity similar to that of diving birds, reinforcing the hypothesis of a diving ecology for this species.

Ornithurae Haeckel 1866

Panneognathae Gauthier & de Queiroz 2001

Vegaviidae Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9.

Polarornis gregorii Chatterjee 1989CHATTERJEE S. 1989. The oldest Antarctic bird. Journal of Vertebrate Paleontology 8: 11A.

cf. Polaronis gregorii

Material – MN 7833-V, isolated fragment of a tarsometatarsus? (Fig. 5a).

Figure 5
Microstructural pattern of MN 7833-V (a-h), proximal fragment of tarsometatarsus MN 7833-V in lateral view (a), whole cross section of MN 7833-V (b). Two cortical regions showing the large amount of intertrabecular spaces (c) and thick endosteal lamella (d) in different portions of the perimedullary cortex. High-magnification of the cortex showing the clusters of osteocyte lacunae, which characterize the woven-fibered bone matrix (e). Nutrient foramen in subperiosteal cortex (f). High magnification of subperiosteal cortex showing the longitudinal primary osteons (g). High magnification of trabeculae bounded by cement lines in perimedullary cortex (h). Red line in a corresponds to the level where the section was made. The outer cortex face upward in b-g. Scale bar in a is equal to 15 mm. Abbreviations: cl, cement line, el, endosteal lamellae, mc, medullary cavity, nf, nutrient foramen, nvc, neurovascular canals, po, primary osteons, oc, osteocyte clusters, rc, resorption cavities, so, secondary osteon, t, trabeculae, ts, intertrabecular spaces.

Locality and horizon – Sandwich Bluff, Sandwich Bluff Member, SBM8, 9, 10, 11 or 12 of (sensu Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.), approximately 40 m above the level where Vegavis specimens were recovered, López de Bertodano Formation outcropping in Cape Lamb, Vega Island, Antarctic Peninsula. Upper Maastrichtian (~66-68 Mya).

Description and comparisons

MN 7833-V consists of a small fragment (3.5 mm) of a rod-like bone with a diameter of 8.8 mm, lacking its proximal and distal ends. The specimen was found with no association with the synsacrum MN 7832-V. The incompleteness of the bone precludes its precise identification (Fig. 5a), but some features are informative. The partial diaphysis has a longitudinal and sharp crest extending along the shaft, but its presumably distal portion is broken. The apical margin of the crest is straight and roughly parallel to the shaft surface. As it extends along the shaft, the crest deflects and gradually merges onto the shaft surface. One of the surfaces of the crest is convex and continuous with the shaft, whereas the opposite surface is concave, which gives to the shaft a half salinon-shape to the transverse section in distal view. Above the crest level, the shaft exhibits a roughly circular cross-section. The combination of straight shaft, roughly circular shape in transversal section, and the presence of a sharp and bowed crest suggests that the specimen represents a hind limb long bone. The preserved shaft is elongated and robust, possessing a thick cortex, similar in proportions to the avian tibiotarsus or tarsometatarsus. In comparison with partially chronocorrelated birds, the crest of MN 7833-V superficially resembles the crista fibularis or tuberositas retinaculi extensoris of the tibiotarsus of Vegavis (Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.). These crests are sharp and have rounded apical edges as in MN 7833-V. However, they are lower in Vegavis, protruding briefly from the shaft to immediately merge into the bone surface. In addition, the apical margins of these crests are not parallel to the shaft as in MN 7833-V. Instead, the crest of MN 7833-V is more similar to the crista plantaris lateralis (crista dorsalis lateralis of Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.) of the tarsometatarsus of Vegavis. In both MN 7833-V and Vegavis tarsometatarsus, the crests similarly protrude acquiring a more dorsal inclination. Their apical edges are parallel to the straight shaft. The shafts possess a deeply concave sulcus extensorum on one side, whereas they have a convex shaft in the opposite side. The half ‘salinon-shaped’ cross-section is present in both MN 7833-V and Vegavis. However, unlike Vegavis, MN 7833-V lacks foramina vasculare proximale laterale et proximale on the floor of sulcus extensori. MN 7833-V may represent a fragment from a more distal part of the shaft of the tarsometatarsus than the one preserved in Vegavis, in which the distalmost portion of crista plantaris is missing, preventing us from determining whether the inflection of the crest is similar to MN 7833-V or not.

The anatomy of the crest of MN 7833-V also resembles the crista deltopectoralis of the vegaviids Vegavis, Maaqwi (McLachlan et al. 2017MCLACHLAN SMS, KAISER GW & LONGRICH NR. 2017. Maaqwi cascadensis: A large, marine diving bird (Avialae: Ornithurae) from the Upper Cretaceous of British Columbia, Canada. PLoS ONE 12: e0189473., Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.), and many extant neornithines such as Gavia adamsii and Haliaeetus leucocephalus (Serrano et al. 2020SERRANO FJ, COSTA-PÉREZ M, NAVALÓN G & MARTÍN-SERRA A. 2020. Morphological disparity of the humerus in modern birds. Diversity 12: 173., Watanabe et al. 2021WATANABE J, FIELD D & MATSUOKA H. 2021. Wing musculature reconstruction in extinct flightless auks (Pinguinus and Mancalla) reveals incomplete convergence with penguins (Spheniscidae) due to differing ancestral states. Integr Org Biol 3: obaa040.), with a straight apical margin almost parallel to the shaft. The deflection of the crest within the shaft in lateral view of MN 7833-V approaches angles similar to those of the cited vegaviids. However, MN 7833-V differs from the humerus by having a sinuous apical outline instead straight. Given its morphology, we tentatively identify MN 7833-V as an undetermined vegaviid tarsometatarsus.

Microstructural pattern

The thin section of MN 7833-V revealed a roughly circular cross-section (Fig. 5b). It shows a relatively thick and azonal compact cortex that represents 89.6% of the cross-sectional area (RBT ranging from 32.7% to 37.14%, mean = 34.55±1.957). A wide, roughly circular, and well delimited medullary cavity is present. The cavity is delimited by thick endosteal lamellae (avascular inner circumferential layer of some authors - e.g., Chinsamy-Turan 2005CHINSAMY-TURAN A (Ed). 2005. The microstructure of dinosaur bone. Deciphering Biology with Fine-Scale Techniques, Baltimore and London: Johns Hopkins University Press, p. 216., Màrsa et al. 2017), which indicates that the specimen was a skeletally mature adult at the time of death (Fig. 5b and d).

The cortex is intensely vascularized (Fig. 5). It is filled by globular, and haphazard-oriented osteocyte lacunae, which occur in clusters approaching a high degree of overlapping (Fig. 5e). The primary osteons are arranged in a mixed reticular and longitudinal neurovascular pattern. Primary longitudinal osteons are particularly abundant toward the subperiosteal region (Fig. 5g). The primary osteons are surrounded by flattened osteocyte lacunae, which are concentrically arranged around the inner canals. The longitudinal primary osteons show birefringence under circularly cross-polarized light (Fig. 5b and f). In the subperiosteal cortex lies a large, longitudinal nutrient foramen (Fig. 5e). This foramen houses the arterial supply for the primary diaphyseal growth center during development and it is regarded as indicative of mid-diaphysis in adults (Payton 1934PAYTON CG. 1934. The position of the nutrient foramen and direction of the nutrient canal in the long bones of the madder-fed pig. J Anatol 68: 500.).

Under circularly cross-polarized light most of the cortex exhibits isotropism (i.e., exhibiting transmitted light regardless of the plane of observation, Shapiro & Wu 2019SHAPIRO F & WU JY. 2019. Woven bone overview: Structural classification based on its integral role in developmental, repair and pathological bone formation throughout vertebrate groups. Eur Cell Mater 38: 137-167.), which occurs when large amounts of matrix are quickly deposited (Buffrénil et al. 2021BUFFRÉNIL VD, DE RICQLÈS AJ, ZYLBERBERG L & PADIAN K. 2021. Vertebrate skeletal histology and paleohistology, 1st ed., Boca Raton: CRC Press, 826 p.). The combination of isotropic bone matrix, globular haphazard-oriented and clustered osteocyte lacunae characterize the woven-fibered matrix (de Ricqlès 1976DE RICQLÈS AJ. 1976. On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. In: BELLAIRS A & COX CB (Eds), Morphology and Biology of Reptiles. Ed: Linnean Society Symposium Series, Cambridge: Academic Press 3, Cambrige, USA, p. 123-151.). The woven-fibered bone matrix extensively occupied by longitudinal primary osteons indicates that the bone is of fibrolamellar type (=woven-parallel of Buffrénil et al. 2021BUFFRÉNIL VD, DE RICQLÈS AJ, ZYLBERBERG L & PADIAN K. 2021. Vertebrate skeletal histology and paleohistology, 1st ed., Boca Raton: CRC Press, 826 p.). This bone is typical of endothermic tetrapods and is commonly indicative of high, sustained metabolic activity (e.g., de Ricqlès et al. 2008DE RICQLÈS A, PADIAN K, KNOLL F & HORNER JR. 2008. On the origin of high growth rates in archosaurs and their ancient relatives: complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. Annales de Paléontologie 94: 57-76.).

The cortex is devoid of any cyclical growth marks (LAG or annuli), suggesting that the specimen exhibited a high and continuous growth rate (Shapiro & Wu 2019SHAPIRO F & WU JY. 2019. Woven bone overview: Structural classification based on its integral role in developmental, repair and pathological bone formation throughout vertebrate groups. Eur Cell Mater 38: 137-167., Buffrénil et al. 2021BUFFRÉNIL VD, DE RICQLÈS AJ, ZYLBERBERG L & PADIAN K. 2021. Vertebrate skeletal histology and paleohistology, 1st ed., Boca Raton: CRC Press, 826 p.), likely reaching adulthood without any periodic interruption.

The perimedullary cortex of MN 7833-V has enlarged eroded resorption cavities (Fig. Fig 5c and h). The cavities grade to bone trabeculae endosteally. Trabeculae are formed by primary lamellated bone. They are asymmetrically distributed over the cross-section, completely obliterating the endosteal lamella in one of the sides of the section. The resorption cavities decrease in size toward the outer cortex, but they do not extend outside the deep cortex (Fig. 5b, d, f and h). Outwardly, these cavities are replaced by secondary osteons with wide Harversian canals (Fig. 5f and h). The Harvesian canals decrease in diameter outwards (Fig. 5f).

The overall microstructure of MN 7833-V is roughly similar to the pattern seen in the femur of Polaronis (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235.), and has some resemblance with the humerus, radius, and femur of Vegavis (Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., Màrsa et al. 2017).

The cortex of MN 7833-V is highly populated by resorption cavities like the pattern seen in the Polarornis TTU 9265. In both MN 7833-V and Polarornis, these cavities occur in the margins of the medullary cavities. Although Vegavis’ femur has numerous porosities, they differ in diameter from those of Polaronis. The perimedullary cortices of MN 7833-V and Polarornis contain numerous Volkman’s canals passing through the endosteal lamellae, whereas the Vegavis specimens do not exhibit such structures in the endosteal lamellae. In Vegavis, the predominant neurovascular pattern is longitudinal, unlike MN 7833-V and Polarornis, which have predominantly reticular neurovascular pattern. Furthermore, the specimen MN 7833-V shares with Polarornis proportionally thick endosteal lamellae.

MN 7833-V and Vegavis femora share perimedullary cortices intensely populated by resorption cavities. However, MN 7833-V differs from all sampled Vegavis bones by the presence of a large nutrient foramen in the subperiosteal cortex and proportionally thicker endosteal lamellae. It is difficult to confirm whether these features (especially the thicker endosteal lamellae) may result from intra-elemental histovariability or not.

Although the Cretaceous vegaviid Maaqwi has not been histologically analyzed, its broken proximal humerus shows a large nutrient foramen close to the subperiosteal cortex, as in MN 7833-V. Maaqwi also possesses a thick cortex (we calculated RBT = 31.54) that is more similar to MN 7833-V (34.55) than Vegavis (20 for humerus and 21.6 for femur, Marsà et al. 2017MARSÀ JAG, AGNOLÍN FL & NOVAS F. 2017. Bone microstructure of Vegavis iaai (Aves, Anseriformes) from the Upper Cretaceous of Vega Island, Antarctic Peninsula. His Biol 31: 163-167.).

The microstructural features of MN 7833-V also resemble Ichthyornis (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235.), but it can be easily distinguished from the latter by possessing a considerably thicker cortex. Unlike Polarornis and Vegavis, the relatively thin bone wall of Ichthyornis is more consistent with other non-diving volant birds (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235.).

The vascular pattern, bone type, and absence of LAGs in MN 7833-V are consistent with its placement within Neornithes, but also Ornithurae as a whole. However, these attributes alone are not enough to provide a less inclusive taxonomic assignment of the specimen with confidence. Among the birds herein examined, Vegavis, Polarornis, and Maaqwi shared similar microstructural patterns resulting from adaptation to their diving-ecologies.

Hollow long bones with a cortical thickness comparable to or even thinner than MN 7833-V only occur in theropod dinosaurs, including birds (Erickson 2014ERICKSON GM. 2014. On Dinosaur Growth. Annu Rev Earth Planet Sci 42: 675-697.). In fact, non-avian theropod bones occasionally occur in horizons SBM7, 12, and 15 (Case et al. 2003CASE JA, MARTIN JE, CHANEY DS & REGUERO M. 2003. Late Cretaceous dinosaurs from the Antarctic Peninsula: remnant or immigrant fauna? J Vertebr Paleontol 23: 39A., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72., Lamanna et al. 2019LAMANNA MC, CASE JA, ROBERTS EM, ARBOUR VM, ELY RC, SALISBURY SW, CLARKE JA, MALINZAK DE, WEST AR & O’CONNOR PM. 2019. Late Cretaceous non-avian dinosaurs from the James Ross Basin, Antarctica: description of new material, updated synthesis, biostratigraphy, and paleobiogeography. Adv Polar Sci 30: 228-250.). However, because ornithurine (those including Neornithes) exhibit extremely high growth rates, they rarely deposit cyclical growth marks during growth, differing from other non-ornithurine theropods that show LAGs (Padian et al. 2001PADIAN K, DE RICQLÈS AJ & HORNER JR. 2001. Dinosaurian growth rates and bird origins. Nature 412: 405-408., Chinsamy 2002CHINSAMY A. 2002. Bone microstructure of early birds. In: CHIAPPE LM & WITMER LM (Eds), Mesozoic birds: above the heads of dinosaurs. Berkeley: University of California Press, EUA, p. 421-431.). Therefore, LAGs have been observed in only few neornithines, including the king penguin (Castanet 2006CASTANET J. 2006. Time recording in bone microstructures of endothermic animals, functional relationships. CR Palevol 5: 629-636.), kiwi (Bourdon et al. 2009BOURDON E, CASTANET J, DE RICQLÈS A, SCOFIELD P, TENNYSON A, LAMROUS H & CUBO J. 2009. Bone growth marks reveal protracted growth in New Zealand kiwi (Aves, Apterygidae). Biol Lett 5: 639-642.), orange-winged Amazon parrot (Amprino & Godina 1947AMPRINO R & GODINA G. 1947. La Struttura delle ossa nei vertebrati. Ricerche comparative negli anfibi e negli amnioti [with plates]. Comment 11: 329-464.), extinct Moa (Turvey et al. 2005TURVEY ST, GREEN OR & HOLDAWAY RN. 2005. Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435: 940-943.), and Gastornis (Padian et al. 2001PADIAN K, DE RICQLÈS AJ & HORNER JR. 2001. Dinosaurian growth rates and bird origins. Nature 412: 405-408.). The absence of LAGs in MN 7833-V is thus consistent with ornithurine birds and excluded it from non-ornithurine theropods.

However, the cortex of MN 7833-V is thicker than in most typical volant ornithurines. Thick cortices are present in Hesperornis, Polarornis, anatids, penguins, and diving charadriiforms, and are associated with their diving ecology (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235., Smith & Clarke 2014SMITH NA & CLARKE JA. 2014. Osteological Histology of the Pan-Alcidae (Aves, Charadriiformes): correlates of wing-propelled diving and flightlessness. Anat Rec 297: 188-199.). The cortical thickness varies considerably even among diving birds. This feature can be expressed through comparisons of RBT among extant and extinct taxa. The RBT of tarsometatarsus MN 7833-V (=34.5) is considerably higher than in Vegavis (20 – 21.6) (Marsà et al. 2017MARSÀ JAG, AGNOLÍN FL & NOVAS F. 2017. Bone microstructure of Vegavis iaai (Aves, Anseriformes) from the Upper Cretaceous of Vega Island, Antarctic Peninsula. His Biol 31: 163-167.), some anseriforms (~17.6) (Mendoza & Tambussi 2015MENDOZA RS & TAMBUSSI CP. 2015. Osteosclerosis in the extinct Cayaoa bruneti (Aves, Anseriformes): insights on behavior and lightlessness. Ameghiniana 52: 305-313.), but lower than in Polarornis (37) (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235.) and the larger femur of the unnamed species of Vegavis SDSM 78247 (37) (West et al. 2019WEST AR, TORRES CR, CASE JA, CLARKE JA, O’CONNOR PM & LAMANNA MC. 2019. An avian femur from the Late Cretaceous of Vega Island, Antarctic Peninsula: removing the record of cursorial landbirds from the Mesozoic of Antarctica. PeerJ 7: e7231.). Instead, the RBT of MN 7833-V approximates to diving charadriiformes (~30) (Smith & Clarke 2014SMITH NA & CLARKE JA. 2014. Osteological Histology of the Pan-Alcidae (Aves, Charadriiformes): correlates of wing-propelled diving and flightlessness. Anat Rec 297: 188-199.), the Andean ruddy duck Oxyura ferruginea (31.42) (Mendoza & Tambussi 2015MENDOZA RS & TAMBUSSI CP. 2015. Osteosclerosis in the extinct Cayaoa bruneti (Aves, Anseriformes): insights on behavior and lightlessness. Ameghiniana 52: 305-313.), Maaqwi (31.54), gentoo penguin Pygoscelis papua (32.83) (Mendoza & Tambussi 2015MENDOZA RS & TAMBUSSI CP. 2015. Osteosclerosis in the extinct Cayaoa bruneti (Aves, Anseriformes): insights on behavior and lightlessness. Ameghiniana 52: 305-313.), and emperor penguin Aptenodytes forsteri (33) (Chinsamy et al. 1998CHINSAMY A, MARTIN LD & DOBSON P. 1998. Bone microstructure of the diving Hesperornis and the voltant Ichthyornis from the Niobrara Chalk of western Kansas. Cretac Res 19: 225-235.). Therefore, it is important to note that the RBT observed in MN 7833-V is intermediate between sphenicids and highly osteosclerotic anseriforms.

Although the microstructure of the tarsometatarsus MN 7833-V shows a pattern consistent with ornithurine birds and roughly similar to diving neornithines (especially vegaviids), the anatomy fails to show any feature that enables a less inclusive taxonomic identification of the specimen.

Regardless of both bias inherent to the histological sampling and plasticity of nutrient foramina, and consistent with the morphologic comparisons here provided, we tentatively consider MN 7833-V as an undetermined vegaviid tarsometatarsus, with striking microstructural similarities with Polarornis, and thus potentially regarded as belonging to this taxon.

DISCUSSION

The literature shows a dramatic improvement in the number of Mesozoic avian specimens since 1980, expanding our knowledge about the diversity, distribution, and early stages of the evolution of the crown birds. Most of the discoveries come from taxa found in South America, Asia, and Antarctica, adding materials known for a long time from Europe and North America, which also revealed recent findings.

Putative neornithines appear in the fossil record probably in the Coniacian of South America (Agnolín et al. 2006AGNOLÍN FL, NOVAS FE & LIO G. 2006. Neornithine bird coracoid from the Upper Cretaceous of Patagonia. Ameghiniana 43: 245-248.), which could reinforce the Gondwanan origin of the crown neornithines (Cracraft 2001CRACRAFT J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous −Tertiary mass extinction event. Proc R Soc Lond 268: 459-469.). The fossil record indicates that the group coexisted alongside Enantiornithes, Hesperornithes, Ichthyornithes and their kin in both Northern and Southern Hemispheres. While most non-neornithine avian lineages reached the apex of diversification and abundance before the Late Cretaceous (O’Connor & Forster 2010O’CONNOR PK & FORSTER CA. 2010. A Late Cretaceous (Maastrichtian) avifauna from the Maevarano Formation, Madagascar. J Vertebr Paleontol 30: 1178-1201.), the neornithines only represented modest components of the paleocommunities of this time. It is hard to determine whether the apparent paucity of Cretaceous neornithines results from taphonomic bias or paleoecology, but the current data support both hypotheses.

A taphonomic bias has often been argued to explain the relatively low abundance of neornithines in the Mesozoic, with many authors suggesting that the avian fossil record is poor (Cooper & Penny 1997COOPER A & PENNY D. 1997. Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence. Science 275: 1109-1113., Cooper & Fortey 1998COOPER A & FORTEY R. 1998. Evolutionary explosions and the phylogenetic fuse. Trends Ecol Evol 13: 151-156., Smith & Peterson 2002SMITH AB & PETERSON KJ. 2002. Dating the time of origin of major clades: molecular clocks and the fossil record. A Rev Earth Planet Sci 30: 65-88.) or that paleontologists have performed relatively little collecting effort, especially in the Southern Hemisphere (Cooper & Fortey 1998COOPER A & FORTEY R. 1998. Evolutionary explosions and the phylogenetic fuse. Trends Ecol Evol 13: 151-156., Cracraft 2001CRACRAFT J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous −Tertiary mass extinction event. Proc R Soc Lond 268: 459-469.). Other authors, however, suggested that neornithines were simply ecologically less abundant (Fontaine et al. 2005). However, the high number of specimens discovered in South America (Lambrecht 1929LAMBRECHT K. 1929. Neogaeornis wetzeli n. g. n. sp., der erste Kreidevogel der suedlichen Hemisphaere. Palaeontol Z 11: 121-129., Clarke & Chiappe 2001CLARKE JA & CHIAPPE LM. 2001. A New Carinate Bird from the Late Cretaceous of Patagonia (Argentina). Am Mus Nov. 2001: 1-24., Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388., Agnolín et al. 2006AGNOLÍN FL, NOVAS FE & LIO G. 2006. Neornithine bird coracoid from the Upper Cretaceous of Patagonia. Ameghiniana 43: 245-248., Agnolín & Martinelli 2009AGNOLÍN FL & MARTINELLI AG. 2009. Fossil birds from the Late Cretaceous Los Alamitos Formation, Río Negro Province, Argentina. J South Am Earth Sci 27: 42-49., Agnolín 2010AGNOLÍN FL. 2010. An avian coracoid from the Upper Cretaceous of Patagonia, Argentina. Stud Geol Salmant 46: 99-119., Novas et al. 2019NOVAS FE ET AL. 2019. Paleontological discoveries in the Chorrillo Formation (upper Campanian-lower Maastrichtian, Upper Cretaceous), Santa Cruz Province, Patagonia, Argentina. Rev Mus Argent Cienc Nat 21: 217-293., Acosta Hospitaleche et al. 2023ACOSTA HOSPITALECHE C, O’GORMAN JP & PANZERI KM. 2023. A new Cretaceous bird from the Maastrichtian La Colonia Formation (Patagonia, Argentina). Cretac Res 150: 105595.) and the well-preserved Vegavis specimens found in Antarctica (Noriega & Tambussi 1995NORIEGA JI & TAMBUSSI CP. 1995. A Late Cretaceous Presbyornithidae (Aves: Anseriformes) from Vega Island, Antarctic Peninsula: Paleobiogeographic implications. Ameghiniana 32: 57-61., Hope 2002HOPE S. 2002. The Mesozoic radiation of Neornithes. In: CHIAPPE & WITMER (Eds) Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, United States, p. 339-388., Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308., 2016, Chatterjee et al. 2006CHATTERJEE S, MARTIONI D, NOVAS FE, MUSSEL F & TEMPLIN R. 2006. A new fossil loon from the Late Cretaceous of Antarctica and early radiation of foot-propelled diving birds. J Vertebr Paleontol 26: 49A-49A., Agnolín et al. 2017AGNOLÍN FL, EGLI FB, CHATTERJEE S, MARSÀ JA & NOVAS FE. 2017. Vegaviidae, a new clade of southern diving birds that survived the K/T boundary. Sci Nat 104: 1-9., Marsà et al. 2017MARSÀ JAG, AGNOLÍN FL & NOVAS F. 2017. Bone microstructure of Vegavis iaai (Aves, Anseriformes) from the Upper Cretaceous of Vega Island, Antarctic Peninsula. His Biol 31: 163-167., Acosta Hospitaleche & Worthy 2021ACOSTA HOSPITALECHE C & WORTHY TH. 2021. New data on the Vegavis iaai holotype from the Maastrichtian of Antarctica. Cretac Res 124: 104818.) in the last decades have challenged these traditional assumptions. Furthermore, frequently neornithines and non-neornithine birds occur in the same strata, with rare exceptions (e.g., O’Connor & Foster 2010). They also possess similar habits and sizes, making it improbable that these birds had significantly different preservation potential (Fontaine et al. 2005). This argues against a taphonomic filter acting over the neornithine fossil record.

Although molecular data indicate that the origin of crown birds occurred in the mid-Cretaceous (Cooper & Penny 1997COOPER A & PENNY D. 1997. Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence. Science 275: 1109-1113., Paton et al. 2002PATON T, HADDRATH O & BAKER AJ. 2002. Complete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds. Proc. R Soc Lond B 269: 839-846., Brown et al. 2008BROWN JW, REST JS, GARCÍA-MORENO J, SORENSON MD & MINDELL DP. 2008. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biol 6: 6.), the fossil record shows that only in the Campanian they began to increase slightly in diversity, becoming more abundant in the Maastrichtian. Such a pattern would corroborate the model of evolution of bird lineages throughout vicariance events related to the break-up of Gondwana (Cracraft 2001CRACRAFT J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous −Tertiary mass extinction event. Proc R Soc Lond 268: 459-469.). The end-Cretaceous encompassed the extinction of all basal avian lineages (Enantiornithes, Hesperornithes, Ichtyornithes and kin) but not the neornithines. Several studies have attempted to list the features of the neornithines that enabled them to survive across the K-Pg boundary (Feduccia 1995FEDUCCIA A. 1995. Explosive Evolution in Tertiary Birds and Mammals. Science 267: 637-638., Cooper & Penny 1997COOPER A & PENNY D. 1997. Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence. Science 275: 1109-1113., Longrich 2009LONGRICH N. 2009. An ornithurine-dominated avifauna from the Belly River Group (Campanian, Upper Cretaceous) of Alberta, Canada. Cretac Res 30: 161-177., Bono et al. 2016BONO RK, CLARKE J, TARDUNO JA & BRINKMAN D. 2016. A large ornithurine bird (Tingmiatornis arctica) from the Turonian High Arctic: climatic and evolutionary implications. Sci Rep 6: 1-8., Mayr 2017MAYR G. 2017. The Interrelationships and Origin of Crown Group Birds (Neornithes). In: MAYR G (Ed), Avian evolution: the fossil record of birds and its paleobiological significance, Chichester: J Wiley & Sons, Ltd, West Sussex, UK, p. 84-93., Torres et al. 2021TORRES CR, NORELL MA & CLARKE JA. 2021. Bird neurocranial and body mass evolution across the end-Cretaceous mass extinction: The avian brain shape left other dinosaurs behind. Sci Advances 7: eabg7099.). Among the hypotheses, that of the different growth rates between neornithines and non-neornithine avians have gained strength in the last years (Longrich 2009LONGRICH N. 2009. An ornithurine-dominated avifauna from the Belly River Group (Campanian, Upper Cretaceous) of Alberta, Canada. Cretac Res 30: 161-177., Bono et al. 2016BONO RK, CLARKE J, TARDUNO JA & BRINKMAN D. 2016. A large ornithurine bird (Tingmiatornis arctica) from the Turonian High Arctic: climatic and evolutionary implications. Sci Rep 6: 1-8., Marsà et al. 2017MARSÀ JAG, AGNOLÍN FL & NOVAS F. 2017. Bone microstructure of Vegavis iaai (Aves, Anseriformes) from the Upper Cretaceous of Vega Island, Antarctic Peninsula. His Biol 31: 163-167.). Although all ornithothoraceans shared bone cortices composed of fast-growing fibrolamellar bone, neornithines differed by usually lacking LAGs, despite growth marks have been observed in the outer cortices of some species (Canoville et al. 2022CANOVILLE A, CHINSAMY A & ANGST D. 2022. New comparative data on the long bone microstructure of large extant and extinct flightless birds. Diversity 14: 298.). This suggests a relatively higher metabolism and continuously sustained growth rates, without annual interruption. However, because neornithines did not comprise predominant elements across the world or were even absent in some Mesozoic paleocommunities (O’Connor & Foster 2010), this higher growth rate seems not to have provided considerable advantage over the non-neornithine birds. Notwithstanding, a fast growth, allied with relatively small body size, may have been advantageous and selectively beneficial through the K-Pg extinction event (Field et al. 2020FIELD DJ, BENITO J, CHEN A, JAGT JWM & KSEPKA DT. 2020. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579: 397-401.)

Antarctica has the only Mesozoic sites where neornithines are predominant. In parallel, the identification of basal ornithurines from Vega and Seymour islands (Cordes 2001CORDES AH. 2001. A Basal charadriiform bird from the early Maastrichtian of Cape Lamb, Vega Island, Antarctic Peninsula. (Master’s thesis) South Dakota School of Mines and Technology, Rapid City, 142 p., Roberts et al. 2014ROBERTS EM, LAMANNA MC, CLARKE JA, MENG J, GORSCAK E, SERTICH JJW, O’CONNOR PM, CLAESON KM & MACPHEE RDE. 2014. Stratigraphy and vertebrate paleoecology of Upper Cretaceous–? lowest Paleogene strata on Vega Island, Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 402: 55-72.) may be a result of the lack of diagnostic neornithines characters in the aforementioned specimens, what places them on a more inclusive level. The paucity of the “non-neornithine birds” in Antarctica (notably enantiornithines) contrasts with the abundance of Mesozoic neornithines there. Despite the low sampling due to the extreme conditions imposed to fieldwork on the continent and the high weathering acting on the Antarctic fossils, Vega and Seymour Islands have provided abundant neornithine remains. They include one of the best-preserved neornithines of the Mesozoic (Clarke et al. 2005CLARKE JA, TAMBUSSI CP, NORIEGA JI, ERICKSON GM & KETCHAM RA. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433: 305-308.).

The predominance of neornithines in Antarctica suggests that the uninterrupted fast growth rates could be advantageous in these higher latitudes (Longrich 2009LONGRICH N. 2009. An ornithurine-dominated avifauna from the Belly River Group (Campanian, Upper Cretaceous) of Alberta, Canada. Cretac Res 30: 161-177., Bono et al. 2016BONO RK, CLARKE J, TARDUNO JA & BRINKMAN D. 2016. A large ornithurine bird (Tingmiatornis arctica) from the Turonian High Arctic: climatic and evolutionary implications. Sci Rep 6: 1-8., Marsà et al. 2017MARSÀ JAG, AGNOLÍN FL & NOVAS F. 2017. Bone microstructure of Vegavis iaai (Aves, Anseriformes) from the Upper Cretaceous of Vega Island, Antarctic Peninsula. His Biol 31: 163-167.), where extreme seasonal changes in luminosity, temperature, and food availability presumably occurred, such as in Antarctica during the end Cretaceous. The possible absence of non-neornithine birds in the Maastrichtian rocks of Vega and Seymour islands may support this statement, which is also corroborated by our findings.

The south polar region and the Southern Hemisphere as a whole were less affected by the Chicxulub impact than the equatorial zones (Cracraft 2001CRACRAFT J. 2001. Avian evolution, Gondwana biogeography and the Cretaceous −Tertiary mass extinction event. Proc R Soc Lond 268: 459-469.), which may have contributed to their survival through the K-Pg Mass Extinction Event (Case 2001CASE JA. 2001. Latest Cretaceous record of modern birds from Antarctica: center of origin or fortuitous occurrence? In: NORTH AMERICAN PALEONTOLOGICAL CONVENTION 2001, Berkeley: https://ucmp.berkeley.edu/napc/abs5.html#CaseJ.
https://ucmp.berkeley.edu/napc/abs5.html... , Chatterjee 2002CHATTERJEE S. 2002. The morphology and systematics of Polarornis, a Cretaceous loon (Aves: Gaviidae) from Antarctica. In: ZHOU Z & ZHANG F (Eds), Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution, Beijing: Science Press, China, p. 125-155.).

CONCLUSIONS

In the comprehensive global reevaluation of the Late Cretaceous record of Neornithes (crown birds) presented here, it has been ascertained that unequivocal neornithine taxa are notably rare with only a few confidently assigned to that group. In contrast to this scarcity, the sedimentary deposits of the James Ross Sub-Basin in the Antarctic Peninsula exhibit an abundance of neornithine fossilized remains. These findings assume a paramount significance in elucidating the early evolutionary trajectories of neornithines and their resilience during the K-Pg extinction event.

Two new specimens of vegaviids from the Maastrichtian of the Antarctic Peninsula are described in this contribution, a partial synsacrum assigned to Vegavis (MN 7832-V) and a tarsometatarsal fragment tentatively assigned to Polarornis (MN 7833-V). Vegavis is the most representative fossil bird found in the Maastrichtian López de Bertodano Formation. Four specimens are now recognized for this taxon, the holotype (MLP 93-I-3-1), referred materials remarkable by preserving the oldest syrinx known in the fossil record (MACN-PV 19.748), the larger isolated femur (SDSM 78247), and the partial synsacrum (MN 7832-V) here studied. Despite its incompleteness, this specimen records the oldest occurrence of the lumbosacral canals in fossil Neornithes, related to a balance sensing system acting in the control of walking and perching. The tarsometatarsus fragment MN 7833-V shares with Vegavis a roughly similar microstructure, but its incompleteness prevents us from confirming the assignment to this taxon. On the other hand, the general osteohistological pattern exhibited by MN 7833-V resembles more that of the vegaviid Polarornis gregorii. Furthermore, our findings agree with previous authors that higher latitudes had an avifauna dominated by ornithurines, and especially by neornithines in Antarctica, supporting the hypothesis that crown birds were better fitted to live in these environments than more ancient bird lineages presumably by having higher metabolic and growth rates.

ACKNOWLEDGMENTS

We thank Dr. Renata Stopiglia and Dr. Marcos Andre Raposo Ferreira (Setor de Ornitologia, Museu Nacional/UFRJ) for curatorial assistance, Dr. Maria Elizabeth Zucolotto for help in the preparation of the osteohistological slide and Dr. Luciana Carvalho (Departamento de Geologia e Paleontologia, Museu Nacional/UFRJ) for assistance with cataloging specimens. The Marinha do Brasil provided key logistical support for fieldwork during the OPERANTAR XXXVII (37th Brazilian Antarctic Operation). The Brazilian Antarctic Program to supports the PALEOANTAR Project. This study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq #313461/2018-0, #406779/2021-0, #442677/2018-9, and #406902/2022-4 to AWAK, #307938/2019-0 to MBS, #314222/2020-0 to JMS, #310734/2020-7 to AB), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES #88887314459/2019-00 to AWAK, #88887371713/2019-00 to GAS), and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ# E-26/201.095/2022 to AWAK, E-26/010.002178/2019, E-26/201.066/2021 to MBS, E-26/210.066/2023 to JMS).

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