C. Hendrickx & al. 2022: Non-feather integuments in non-avialan Theropoda.

59 MB·English

Biol.Rev.(2022),pp.000–000. 1
doi:10.1111/brv.12829
Morphology and distribution of scales, dermal
fi
ossi cations, and other non-feather
integumentary structures in non-avialan
theropod dinosaurs
† †
Christophe Hendrickx1 * , Phil R. Bell2 *, Michael Pittman3,4 ,
Andrew R. C. Milner5 , Elena Cuesta6, Jingmai O’Connor7 , Mark Loewen8,9,
Philip J. Currie10, Oct(cid:2)avio Mateus11,12 , Thomas G. Kaye13 and Rafael Delcourt14
1UnidadEjecutoraLillo,CONICET-Fundaci(cid:2)onMiguelLillo,251MiguelLillo,SanMigueldeTucum(cid:2)an,Tucum(cid:2)an,4000,Argentina
2SchoolofEnvironmentalandRuralScience,UniversityofNewEngland,Armidale,NSW2351,Australia
3VertebratePalaeontologyLaboratory,DepartmentofEarthSciences,TheUniversityofHongKong,Pokfulam,HongKong,SAR,China
4DepartmentofEarthSciences,UniversityCollegeLondon,WC1E6BT,UnitedKingdom
5St.GeorgeDinosaurDiscoverySiteatJohnsonFarm,2180EastRiversideDrive,St.George,UT,U.S.A.
6BayerischeStaatssammlungfürPaläontologieundGeologie,Richard-Wagner-Str.10,Munich,80333,Germany
7FieldMuseumofNaturalHistory,1400SLakeShoreDrive,Chicago,IL60605,U.S.A.
8DepartmentofGeologyandGeophysics,UniversityofUtah,FrederickAlbertSuttonBuilding,115South1460East,SaltLakeCity,UT,84112,
U.S.A.
9NaturalHistoryMuseumofUtah,301WakaraWay,SaltLakeCity,UT84108,U.S.A.
10DepartmentofBiologicalSciences,UniversityofAlberta,Edmonton,AB,Canada
11GeoBioTec,FaculdadedeCiênciaseTecnologia,UniversidadeNovadeLisboa,Caparica,Portugal
12MuseudaLourinha~,95RuaJoa~oLuisdeMoura,Lourinha~,2530-158,Portugal
13FoundationforScientificAdvancement,7023AlhambraDr.,SierraVista,AZ85650,U.S.A.
14UniversidadeEstadualdeCampinas(UNICAMP),InstitutodeGeociências,CidadeUniversit(cid:2)aria,RuaCarlosGomes,250,Campinas,SP,
13083-855,Brazil
ABSTRACT
Modernbirdsaretypifiedbythepresenceoffeathers,complexevolutionaryinnovationsthatwerealreadywidespreadin
the group of theropod dinosaurs (Maniraptoriformes) that include crown Aves. Squamous or scaly reptilian-like skin is,
however,consideredtheplesiomorphicconditionfortheropodsanddinosaursmorebroadly.Here,wereviewthemorphol-
ogy and distribution of non-feathered integumentary structures in non-avialan theropods, covering squamous skin and
nakedskinaswellasdermalossifications.Theintegumentaryrecordofnon-averostrantheropodsislimitedtotracks,which
ubiquitouslyshowacoveringoftinyreticulatescalesontheplantarsurfaceofthepes.Thisisconsistentalsowithyounger
averostranbodyfossils,whichconfirmanarthralarrangementofthedigitalpads.Amongaverostrans,squamousskiniscon-
firmedinCeratosauria(Carnotaurus),Allosauroidea(Allosaurus,Concavenator,Lourinhanosaurus),Compsognathidae(Juravenator),
and Tyrannosauroidea (Santanaraptor, Albertosaurus, Daspletosaurus, Gorgosaurus, Tarbosaurus, Tyrannosaurus), whereas dermal
ossifications consisting of sagittateand mosaic osteoderms are restricted toCeratosaurus. Naked,non-scale bearingskin is
foundinthecontentioustetanuranSciurumimus,ornithomimosaurians(Ornithomimus)andpossiblytyrannosauroids(Santanar-
aptor),andalsoonthepatagiaofscansoriopterygids(Ambopteryx,Yi).Scalesaresurprisinglyconservativeamongnon-avialan
* Authors for correspondence (Tel.: [phone]; E-mail: [email protected]); (Tel.: [phone];
E-mail:[email protected])
†
Authorscontributedequallytothiswork.
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
2 Christophe Hendrickx et al.
theropods compared to some dinosaurian groups (e.g. hadrosaurids); however, the limited preservation of tegument on
mostspecimenshindersfurtherinterrogation.Scalepatternsvaryamongand/orwithinbodyregionsinCarnotaurus,Conca-
venatorandJuravenator,andincludepolarised,snake-likeventralscalesonthetailofthelattertwogenera.Unusualbutmore
uniformlydistributedpatterningalsooccursinTyrannosaurus,whereasfeaturescalesarepresentonlyinAlbertosaurusandCar-
notaurus.Fewtheropodscurrentlyshowcompellingevidencefortheco-occurrenceofscalesandfeathers(e.g.Juravenator,
Sinornithosaurus),althoughreticulatescaleswereprobablyretainedonthemaniandpedesofmanytheropodswithaheavy
plumage. Feathers and filamentous structures appeartohave replaced widespreadscaly integuments in maniraptorans.
Theropodskin,andthatofdinosaursmorebroadly,remainsavirtuallyuntappedareaofstudyandtheappropriationof
commonlyusedtechniquesinotherpalaeontologicalfieldstothestudyofskinholdsgreatpromiseforfutureinsightsinto
thebiology,taphonomyandrelationshipsoftheseextinctanimals.
Keywords: integument,scales,skin,Theropoda,dinosaur,footprints,tracefossils,feathers
CONTENTS
I. Introduction .........................................................................2
II. Historicaloverviewoftheropodintegumentarydiscoveries(includingfeathers) ......................4
III. Materialandmethods ..................................................................6
(1) Terminology .................................................................... 7
(a) Scaletypes ................................................................... 7
(b) Scaleshapeandornamentation ................................................... 8
(c) Interstitialtissue .............................................................. 10
(d) Dermalossificationsandosteodermmorphotypes .................................... 10
IV. Results .............................................................................10
(1) Stem-averostranTheropoda ....................................................... 10
(2) Indeterminateaverostrans ......................................................... 12
(3) Ceratosauria ................................................................... 13
(4) Carnosauria .................................................................... 13
(5) Tyrannosauroidea ............................................................... 17
(6) Compsognathidae ............................................................... 19
(7) Ornithomimosauria .............................................................. 21
(8) Pennaraptora ................................................................... 22
V. Discussion ..........................................................................25
(1) Morphologyanddistributionofepidermalstructuresinnon-avialantheropods ................ 25
(a) Body ...................................................................... 25
(b) Manusandpes ............................................................... 31
(c) Scalesandplumageco-occurrence ................................................ 31
(d) Excrescences ................................................................ 32
(2) Morphologicalcomparisonofthescalyskinoftheropodswithotherdinosaurs ................. 32
(3) Evolutionofintegumentarystructuresinnon-avialantheropods ............................ 34
(4) Futuredirections ................................................................ 34
VI. Conclusions .........................................................................36
VII. Acknowledgements ...................................................................36
VIII. References ..........................................................................37
IX. Supportinginformation ................................................................45
I. INTRODUCTION boundary mass extinction event 66 million years ago
(e.g.Gauthier&Gall,2002;Naish,2012;Brusatte,O’Con-
Theropods, including birds, form the most taxonomically nor & Jarvis, 2015). They are globally cosmopolitan and
and morphologically diverse clade of dinosaurs comprise>10000livingspecies,allcharacterisedbythepres-
(Rauhut, 2003; Brusatte et al., 2012; Holtz, 2012; Foth & enceofoneofthemostcomplexintegumentaryappendages
Rauhut,2013).Membersofthiscladewerebipedalanimals found in any vertebrate: the feather (Prum & Brush, 2002;
andmost,ifnotall,carnivorousdinosaursareincludedinthis Chiappe & Dyke, 2006). Although the first birds (i.e. the
group (Hendrickx, Hartman & Mateus, 2015). Birds are earliest-branching members of the clade Avialae) and their
nestedwithinthetheropodradiation,makingthemtheonly closesttheropodrelativesalreadyhadsomeformofplumage
dinosaurs to survive the Cretaceous–Paleogene (K–Pg) (e.g. Norell & Xu, 2005; Zhang, Zhou & Dyke, 2006; Xu
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
Non-feather integuments in non-avialan theropods 3
et al., 2014; Brusatte & Clark, 2015; Lefèvre et al., 2020; membranous patagium (Xu et al., 2015; Wang et al., 2019),
Xu, 2020), many early-diverging clades of theropods were illustrate the extent to which epidermal structures played a
still covered with scales, which is considered the ancestral roleinformingdisparatemorphologiesandecologiesamong
condition in dinosaurs [Barrett, Evans & Campione, 2015; theropods.Despitethisepidermaldiversity,therelevantstruc-
Campione,Barrett&Evans,2020;butseeYangetal.(2019) tures of many theropod taxa remain poorly described and
for another opinion]. Scales and feathers, like internal oftenlackdetailedillustrations.Consequently,thisreviewaims
organs, are soft tissues that are typically rarely preserved in toaddressthisissueby:(i)providingahistoricaloverviewofthe
thefossilrecord(Xu&Guo,2009;Schweitzer,2011).Never- historyoftheropodintegumentarydiscoveries;(ii)comprehen-
theless,aparticularlyhighnumberofnon-avialantheropod sively describing and illustrating the non-feather epidermal
speciesretainexceptionallypreservedintegument,revealing structures(i.e.squamousskin,nakedskin,dermalossifications)
of non-avialan theropods, including those known from foot-
a wide morphological diversity of epidermal structures
prints;(iii)exploringthedistributionandmorphologyofsqua-
among this group and illuminating remarkable detail on
mous integument in non-avialan theropods and other
the evolution of feathers (e.g. Prum & Brush, 2002;
dinosaurs,and;(iv)providingamuch-neededroadmapoutlin-
Norell&Xu,2005;Xu&Guo,2009;Xuetal.,2014;Lefèvre
ing promising future directions for the study of theropod
etal.,2020;Xu,2020).Themajorityofnon-avialantheropod
integument.
specimensthatincludeintegumentaryremainsarefromthe
Institutionalabbreviations:AC,BeneskiMuseumof
Lagerstätte fossil sites of the Jehol Group of northeastern
Natural History (formerly Pratt Museum of Amherst Col-
China,andallappeartobecoveredwithfilamentousstruc-
lege), Amherst, Massachusetts, USA; AMNH, American
tures, ‘protofeathers’ or true feathers (e.g. Zhang
MuseumofNaturalHistory,NewYorkCity,USA;BMMS,
et al., 2006; Xu et al., 2014; Benton et al., 2019; Lefèvre
Bürgermeister Müller Museum, Solnhofen, Germany;
et al., 2020; Xu, 2020). Yet, scales were foundin many non-
BSPG, Bayerische Staatssammlung für Paläontologie und
avialan theropods throughout the Mesozoic (Barrett
HistorischeGeologie,München,Germany;BYU-VP,Brig-
etal.,2015;Campioneetal.,2020),fromtheearliest-diverging hamYoungUniversityMuseumofVertebratePaleontology,
formsoftheLateTriassic(Gatesy,2001)tothelatest-diverging Provo,Utah,USA;CAGS,ChineseAcademyofGeological
ceratosaursandtyrannosauroidsattheend of the Cretaceous Sciences, Beijing, China; CMN, Canadian Museum of
(Belletal.,2017;Hendrickx&Bell,2021b). Nature, Ottawa, Ontario, Canada; DIP, Dexu Institute of
Because of their now-iconic connection with crown Aves, Paleontology,Chaozhou,China;HMNS,HoustonMuseum
theintegumentsoffeatheredtheropodshavereceivedparticu- ofNaturalScience,Houston,Texas,USA;IRSNB,Institut
larly wide coverage overthe past 20years and are relatively Royal des Sciences Naturelles de Belgique, Brussels,
well described in the literature. Scales, conversely, have Belgium; IVPP, Institute for Vertebrate Paleontology and
receivedasurprisinglyshallowtreatment,despitetheirwider Paleoanthropology, Beijing, China; JME, Jura Museum
taxonomic distribution among non-avialan theropods Eichstätt,Eichstätt,Germany;KNHM,KnuthenborgNatu-
(Barrettetal.,2015;Campioneetal.,2020).Scalyskinhasbeen ral History Museum Collection, Knuthenborg Safaripark,
reported in the abelisaurid Carnotaurus (Bonaparte, Novas & Bandholm,Denmark;LHC,LasHoyasCollection,Univer-
Coria,1990;Czerkas&Czerkas,1997),theallosauroidsAllo- sidadAut(cid:2)onomadeMadrid,Madrid,Spain;LPM,Liaoning
saurus (Pinegar et al., 2003) and Concavenator (Cuesta PaleontologicalMuseum,Liaoning,China;MACN,Museo
etal.,2015),varioustyrannosaurids(Tarbosaurus,Tyrannosaurus, Argentino de Ciencias Naturales ‘Bernardino Rivadavia,’
Gorgosaurus,Albertosaurus,Daspletosaurus;Belletal.,2017),comp- Buenos Aires, Argentina; MCCM, Museo de Ciencias de
sognathids (Compsognathus; Peyer, 2006), Juravenator Castilla-La Mancha [now MUPA, Museo de Paleontología
(e.g. Göhlich & Chiappe, 2006; Bell & Hendrickx, 2020, de Castilla-La Mancha], Cuenca, Spain; MCF-PVPH,
2021; Foth et al., 2020), and Sinornithosaurus (Ji et al., 2001), Museo Municipal ‘Carmen Fuñes,’ Plaza Huincul, Neu-
andtheanchiornithineAnchiornis(Wangetal.,2017b),whereas quén,Argentina; MGUH,Geological Museum at theUni-
dermal ossifications have only been identified in the epony- versity of Copenhagen, Copenhagen, Denmark; ML,
mous ceratosaurian Ceratosaurus (Gilmore, 1920). True skin Museu da Lourinh~a, Lourinh~a, Portugal; MN, Museu
impressionsarealsoreportedfromavarietyoftheropodtracks Nacional, Universidade Federal do Rio de Janeiro, Brazil;
and trackways (e.g. Hitchcock, 1841; Gatesy, 2001; Currie, MPC, Institute of Paleontology and Geology (also known
Badamgarav & Koppelhus, 2003; Milner, Lockley & as the “Mongolian Palaeontology Centre”), Mongolian
Johnson, 2006a; Milner, Lockley & Kirkland, 2006b; Kim Academy of Sciences (formerly IGM), Ulaanbaatar,
etal.,2019).Smoothorbareskinhasbeennotedintheconten- Mongolia; MWC, Museum of Western Colorado, Fruita,
tious tetanuran Sciurumimus (Rauhut et al., 2012) and the Colorado, USA; NGMC, National Geological Museum of
ornithomimosaurianPelecanimimus(Pérez-Morenoetal.,1994; China, Beijing, China; NHMUK PV, Natural History
Briggs et al., 1997), whereas the remarkably preserved skin Museum, London, UK; MNHN, Muséum national d’His-
(epidermis) and other soft tissues have been described in the toire naturelle, Paris, France; SGDS, St. George Dinosaur
tyrannosauroid Santanaraptor (Kellner, 1996; Kellner & de Discovery Site at Johnson Farm, St. George, Utah, USA;
Campos, 1998). Scansoriopterygids, bizarre early-diverging SMA, Sauriermuseum Aathal, Aathal, Switzerland; SMF,
pennaraptorans that evolved a unique airfoil formed from a SenckenbergNaturalHistoryMuseum,FrankfurtamMain,
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
4 Christophe Hendrickx et al.
Germany;STM,ShandongTianyuMuseumofNature,Pin- (VON MEYER, 1861; Griffiths, 1996; Carney et al., 2012;
gyi, Shandong, China; TMP, Royal Tyrrell Museum of Fig. 1B), although its true identity would not be recognised
Palaeontology,Drumheller,Alberta,Canada;UALVP,Uni- until the description of the so-called London specimen of
versityofAlbertaLaboratoryforVertebratePalaeontology, Archaeopteryx (NHMUK OR 37001) the following year
Edmonton,Alberta,Canada;UAM,UniversidadAut(cid:2)onoma (Owen, 1863). Recent analysis, however, indicates this iso-
de Madrid, Madrid, Spain; UCL, University College latedfeathermaynotpertaintoArchaeopteryxafterall,butto
London, London, England; UMNH VP, Natural History another yet-unknown feathered theropod (Kaye
Museum of Utah Vertebrate Paleontology Collection, Salt et al., 2019). On the other side of the Atlantic, between
Lake City, Utah, USA; USNM, United States National 1876 and 1884, M. P. Felch and his brother Charles
Museum Vertebrate Paleontology, National Museum of E. Felch found and collected an almost complete skeleton
Natural History, Washington, District of Columbia, of Ceratosaurus nasicornis in Garden Park, near Canyon City,
USA; WDC, Wyoming Dinosaur Center, Thermopolis, Colorado (Gilmore, 1920). Although initially reported in
Wyoming,USA. the literature by Marsh (1884), it was Gilmore (1920) that
wasthefirsttodescribetherowofdermalossificationsabove
theneuralspinesofCeratosaurus–thefirstforanytheropod.
Although squamous skin of a sauropod was reported in
II. HISTORICALOVERVIEWOFTHEROPOD 1852byGideonM.Mantell(Mantell,1852;Czerkas,1997;
INTEGUMENTARYDISCOVERIES(INCLUDING Upchurch, Mannion & Taylor, 2015; albeit incorrectly
FEATHERS) attributedtoagiantcrocodilian;Hooley,1917),itwouldbe
morethanacenturybeforescalybodyskininanon-avialan
The earliest published record of fossilised integument in a theropod was discovered. In 1984, during fieldwork of the
Mesozoictheropodgoesbacktotheearlynineteenthcentury 8th Paleontological Expedition to Patagonia, Argentinian
when German palaeontologist and politician Ernst Friedrich palaeontologist JoséBonaparteandhisteamuncovered the
FreiherrvonSchlotheim(1820)brieflymentionedthepresence skeleton of the abelisaurid Carnotaurus sastrei in Estancia
of feathered fossils from limestone beds near the towns of Pocho Sastre at Bajada Moreno in Chubut Province
Pappenheim and Solnhofen in Bavaria, Germany (Bonaparte, 1985; Bonaparte et al., 1990; Hendrickx &
(Ostrom,1976).Ostrom(1976,p.97)lamentedthat“thewhere- Bell,2021b).Thediscoverywasexceptionalfortworeasons:
aboutsofvonSchlotheim’sfeatheredfossilsareunknowntoday”,yetthe thespecimenwasalmostcompleteandlargepatchesofskin
factthattheLateJurassicSolnhofendepositshavesinceyielded were preserved on its right side, revealing the detailed skin
numerousspecimensoftheearly-divergingavialanArchaeopteryx morphology of a non-avialan theropod for the first time
stronglysupportsvonSchlotheim’spublishedrecordoffeath- (Bonaparteetal.,1990;Fig.1C).Theimportanceofthisdis-
eredtheropods.Toourknowledge,thefirstillustrateddiscov- coveryleadBonapartetolaunchasecondexpeditiontothe
ery of the integument of a non-avialan theropod dinosaur excavation site of Carnotaurus with paleoartists and skin
appeared in 1841 when the president of Amherst College in experts Stephen and Sylvia Czerkas in 1988 (Czerkas &
theUSA,ReverendEdwardHitchcock,reportedthepresence Czerkas, 1989). This expedition collected additional frag-
of“animpressionoftheskinoftheanimal’sfoot”(Hitchcock,1841, ments of fossil skin from different body parts, which ulti-
p. 486, plate 36, figure 19; Fig. 1A) on a track referred to mately helped Stephen Czerkas realise an accurate life-size
Ornithoidichnites giganteus (= Eubrontes giganteus) recovered a few model of Carnotaurus covered with scales (Czerkas &
yearsbeforefromafineredslateofWethersfield,Connecticut. Czerkas,1989,1997;Hendrickx&Bell,2021b).
Interestingly, this discovery pre-dated the name Dinosauria The1990swerepivotalinthediscoveryofvariousepider-
(Davis,2014),whichwascoinedbySirRichardOwenonlya malstructuresinnon-avialantheropods.Within6years,sev-
yearlater(Owen,1842).Hitchcock(1841)didnotascribethe eral major discoveries were announced that revolutionised
track to a particular animal but noted that the cross furrows our understanding of the morphological diversity of thero-
producingsmallpapillaeparticularlyresembledthoseofbirds. podintegumentandtheevolutionoffeathers.Pérez-Moreno
Given its morphology and stratigraphic distribution etal.(1994)andKellner(1996)reportedsofttissueandinteg-
(i.e. Portland Formation, Hettangian−Sinemurian; Lower umentary structures in the early-diverging ornithomimo-
Jurassic; Gierlowski-Kordesch & Rust, 1994), the track can saurian Pelecanimimus polyodon and the tyrannosauroid
confidently be referred to a theropod and possibly to a non- Santanaraptor placidus from the Early Cretaceous of Spain
averostran neotheropod. Edward Hitchcock later reported and Brazil, respectively. In 1997, skin morphology was
additionaltheropodtracks(allreferredtotheichnogenusBron- revealedintyrannosauridtheropods,withaspecimenofGor-
tozoum [= Eubrontes]) with skin (or ‘papillary’ sensu gosaurus libratus being described as having small rounded or
Hitchcock,1865)impressionsfromtheConnecticutValleyof hexagonalscalesonthetail(Carpenter,1997).Ayearbefore,
NewEngland(Hitchcock,1858,pp.63–64and178,plateX; Ji&Ji’s(1996)publicationOnthediscoveryoftheearliestfossilbird
Hitchcock,1865,p.24,plateXVI). inChina(Sinosauropteryxgen.nov.)andtheoriginofbirdswasthe
The next landmark discovery was that of an isolated turningpointinourunderstandingoftheoriginandevolu-
feather and initial holotype of Archaeopteryx lithographica from tionofbirdsandfeathers.InAugust1996,QiangandShu’an
the lithographic limestone of Solnhofen, Germany, in 1860 JiunearthedforthefirsttimeaMesozoictheropodcovered
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
Non-feather integuments in non-avialan theropods 5
Fig. 1. Historical discoveries of integument in Mesozoic theropod dinosaurs. (A) First illustration of scaly skin in a non-avialan
theropod, the reticulate scales preserved on a pedal track ascribed to Ornithoidichnites giganteus (= Eubrontes giganteus) by Reverend
Edward Hitchcock (1841, plate 36) from a fine red slate of Wethersfield, Connecticut. (B) First illustration of a feather-type
integument in a Mesozoic theropod, the holotype of Archaeopteryx lithographica described and illustrated by von Meyer (1861),
consisting of an isolated pennaceous feather from the lithographic limestone of Solnhofen, Germany, belonging to an
indeterminate feathered theropod. (C) First specimen with scaly integument to be described from the body of a non-avialan
theropod, the skin impression of the abelisaurid Carnotaurus sastrei (MACN-CH 894) from the anteroventral portion of the tail,
described and illustrated by Bonaparte et al. (1990, figure 37C, modified). (D) First non-avialan theropod to be discovered with
filamentous impression, the holotype of Sinosauropteryx prima from the Lower Cretaceous Yixian Formation (Jehol Group) of
LiaoningProvince,China,describedandillustratedbyJi&Ji(1996),whichmarksthebeginningofthediscoveriesofnon-avialan
theropodswithfeathers.
with filamentous integument. Christened Sinosauropteryx et al., 2012; Godefroit et al., 2013a,b; Foth, Tischlinger &
prima, the specimen (Fig. 1D) was uncovered in the village Rauhut,2014;Hanetal.,2014;Lü&Brusatte,2015;Lefèvre
ofShangyuanxiang, Beipiao,in western Liaoning Province, et al., 2020; Poust et al., 2020; Xu, 2020), whereas early-
and initially thought to be a primitive bird (Ji & Ji, 1996) diverging megalosauroids (Rauhut et al., 2012), early-
but classified as an earlier-diverging coelurosaurian divergingtyrannosauroids(Xuetal.,2004,2012)andcomp-
twoyearslater(Chen,Dong&Zhen,1998).Alargenumber sognathids (Ji et al., 2007; Chiappe & Göhlich, 2010; Foth
of specimens from Early Cretaceous deposits of Liaoning etal.,2020)borefilament-likeintegumentarystructures.
Provinceweredescribedinthetwofollowingyears,exposing Theproliferationoffeatherednon-avialantheropodsfrom
forthefirsttimethepresenceofplumaceousfeathersinearly- China and the extremely rapid rate of discovery in this and
divergingoviraptorosaurians(Ji&Ji,1997;Jietal.,1998)and other countries (e.g. Canada, Myanmar) has overshadowed
filamentous integuments in compsognathids (Chen squamous-skinned theropods found in more recent years.
et al., 1998), therizinosaurians (Xu, Tang & Wang, 1999a) Despite this, there have been several exceptions, including
and dromaeosaurids (Xu, Wang & Wu, 1999b). Additional the bull-like abelisaurid Carnotaurus sastrei with small non-
discoveriesinthe21stcenturyrevealedthatallcladesofPen- overlapping scales surrounding larger conical studs
naraptora, and possibly all maniraptoriforms, were likely (Hendrickx & Bell, 2021b), the diminutive Juravenator starki
covered with symmetrical or asymmetrical feathers with filamentous structures and three types of scales
(e.g. Xu, Zhou & Wang, 2000; Xu, Zheng & You, 2010; (Chiappe & Göhlich, 2010; Bell & Hendrickx, 2020, 2021;
Xu et al., 2011, 2017; Xu & Zhang, 2005; Zelenitsky Foth et al., 2020), the bizarre hump-backed
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
6 Christophe Hendrickx et al.
carcharodontosauridConcavenatorcorcovatuswithfeetrevealing otherdinosaursandlivingamniotesbasedonpersonalexami-
abird-likepodotheca(Cuestaetal.,2015),andtyrannosaurids nationandhigh-qualityphotographsoftheskinofornithischian
such as Tyrannosaurus, whose bodies were evidently covered andsauropodomorphdinosaurs,livingbirds,crocodiles,squa-
with tiny polygonal scales and likely no feather structures matesandturtles.
(Bell et al., 2017). One of the most unusual integumentary To review the distribution and evolution of epidermal
structuresdiscoveredinrecentyearspertaintotheenigmatic structuresanddermalossificationsindinosaurs,wemapped
scansoriopterygids,onceagainfromChina.Atleasttwogen- 71tegument-based characters coded for 67 archosauriform
era,YiandAmbopteryx,appeartoshowbare-skinmembranes taxa, among which 40 taxa were examined first hand
stretchedbetweenhypertrophiedmanualdigitsandarod-like (AppendixS2;Hendrickxetal.,2021b).Althoughcharacters
styliform element (Xu et al., 2015; Wang et al., 2019), repre- onepidermalstructures(i.e.smoothskin,scales,osteoderms
senting an entirely novel theropod flight architecture and and feathers) are incorporated in some data matrices, the
demonstrating the role of integument in forming unprece- majority of the integument-based characters we propose
dentedstructures(Dececchietal.,2020). are new (Appendix S2.2). Following the best practices of
recent studies dealing with integument-based characters
(e.g.Holtz,Molnar&Currie,2004;Brusatteetal.,2009;Bar-
rettetal.,2015;Yangetal.,2019;Campioneetal.,2020),we
III. MATERIALANDMETHODS scored all integumentary structures (monofilaments, feature
scales,scutatescales,etc.)thatwerenotobservedinthepre-
Toperformourreview,westudiedthe non-featheredepider- served patch (or patches) of integument as being absent
mal structures and dermal ossifications in 25 non-avialan (Appendix S2.1). Many dinosaur taxa preserve skin and/or
theropod taxa bracketed phylogenetically between the early- feathersinasmallportionoftheirbody(e.g.Allosaurus,Jura-
diverging Theropoda Tawa alae (Nesbitt et al., 2009) and venator,Lourinhanosaurus,Tarbosaurus)sotheresultsofthedistri-
the early-diverging avialan Archaeopteryx lithographica bution of integument-based characters should be seen as
(Elzanowski, 2001; Christiansen & Bonde, 2004; Mayr, tentative since the discovery of additional specimens with
Pohl & Peters, 2005; Foth et al., 2014; see online Supporting moreextensivebodytegumentsornewtaxawithintegumen-
information,AppendixS1).Onlypostcranialosteodermswere tarystructurescouldsignificantlychangetheseresults.
consideredinthisstudy.WiththepossibleexceptionofTyranno- Taxa were bracketed phylogenetically between early-
saurus (the epipostorbital; see Carr, 2020), the cranial dermal diverging archosauriforms [Campione et al. (2020) and
ossifications reported in some theropods such as abelisaurids references therein; Appendix S1 and S2.3] and the early-
(Carrano & Sampson, 2008) are more cornified tissues, diverging avialan Archaeopteryx lithographica (e.g. Foth
armour-likedermisandothertypesofdermalornamentations etal.,2014).BasallybranchingarchosauriformssuchasPro-
thantrueosteoderms(Carretal.,2017;Delcourt,2018).Speci- terosuchus (Thornley, 1970) and Longisquama (Reisz &
mensbelongingto22taxadepositedinscientificcollectionsof Sues, 2000) were chosen as the outgroup over pterosaurs
France, Germany, Portugal, Spain, Argentina, Brazil, USA, becausethelatteralreadyshowparticularlyderivedintegu-
Canada,andChinawereexaminedfirst-handandanatomical mentssuchasanon-scalyskinforminganairfoilandcom-
observations were assisted with the use of a digital camera plex filamentous structures (Bakhurina & Unwin, 1995;
and/oradigitalmicroscopeAM411TDino-LitePro.Theorig- Frey et al., 2003; Kellner et al., 2010; Barrett et al., 2015;
inalintegumentwasobservedinthemajorityoftheropodtaxa, Yangetal.,2019)whereasbasalmostarchosauriformsshow
but high-resolution casts of skin were also used for specimens theplesiomorphicconditionofhavingbodyscales(Reisz&
belongingtofournon-maniraptoriformavetheropods(Allosau- Sues,2000;Campioneetal.,2020).Sauropodomorphsand
rus, Albertosaurus, Tarbosaurus and Tyrannosaurus). Descriptions ornithischianswerealsoexcludedastheoutgroupsbecause
and illustrations in the literature were relied upon for three theirphylogeneticdistributionamongdinosaursisunsettled
additional taxa (Sciurumimus, Ornithomimus, and Epidendrosaurus), (see Baron, Norman & Barrett, 2017; Langer et al., 2017;
including high-resolution photographs provided by two col- Mülleretal.,2018;Baron,2021)andtheirmost-basalmem-
leagues for one of them (Sciurumimus). Three-dimensional bers preserving integument [monofilaments in the hetero-
(3D) models of skin were generated for Carnotaurus (MACN- dontosaurid Tianyulong, polygonal basement scales in the
CH894)usingphotogrammetricdataandthesoftwareAgisoft sauropod Mamenchisaurus (Xu & Guo, 2009; Zheng
Photoscan 1.3.4, as well as for Allosaurus (UMNH VP C481) etal.,2009)]haveverydifferentepidermalstructures.
usingaCreaformGo!SCAN20surfacescannerat0.2mmres- The distribution of integument-based characters was
olution.The3Dmodelswereexported,oriented,andscaledin visualised on six topological trees representative of alterna-
Meshlabversion1.3.4BETA(Cignonietal.,2008)anddepos- tive phylogenetic hypotheses for non-avian theropod evolu-
ited in MorphoMuseuM (https://morphomuseum.com/) tion (Appendix S2.1; see Hendrickx et al., 2021b). These
where they are freely downloadable (Hendrickx et al., 2021a; informal supertrees were built using Mesquite 3.2
Hendrickx&Bell,2021a).Laser-stimulatedfluorescence(LSF) (Maddison&Maddison,2017)followingtheresultsobtained
imagingwasusedtodescribepreservedintegumentusingstan- byGodefroitetal.(2014)andBoyd(2015)forornithischians,
dardprotocols(Kayeetal.,2015;Wangetal.,2017b).Morphol- Müller et al. (2018) for non-tetanuran saurischians, Rauhut
ogyofthenon-avialantheropodskinwascomparedtothatof et al. (2012) for non-coelurosaur tetanurans, Delcourt &
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
Non-feather integuments in non-avialan theropods 7
Grillo (2018) for tyrannosauroids, and Pei et al. (2020) for (Ji et al., 2012) and the microraptorine IVPP V13476 (Xu &
maniraptoriforms (see Pittman et al., 2020). Variations in Li,2016)wereexcludedastheirphylogeneticaffinitiesareinsuf-
thetopologyresultfromthedifferingplacementof:(i)Jurave- ficientlyresolved.TheExcel,MesquiteandTNTfilesusedto
nator as a non-avetheropod tetanuran (Tree1; Rauhut mapintegument-basedapomorphiesandreconstructancestral
etal.,2012;Fothetal.,2020)oracompsognathidcoelurosaur states on different topological trees are deposited and freely
(Tree2; Pei et al., 2020); (ii) sauropodomorphs within the availableonDryad(Hendrickxetal.,2021b).Themainresults
clade of Saurischia (Tree1; e.g. Langer et al., 2017; Müller of the ancestral state reconstruction analysis are also sum-
et al., 2018) or as a sister-clade of Ornithoscelida (Tree3; marisedinAppendixS2.5.
i.e. Theropoda + Ornithischia; Baron et al., 2017); (iii) Finally,wefollowedthephylogeneticdefinitionscompiled
anchiornithines as early-branching avialans (Tree1; Pei byHendrickxetal.(2015)fornon-avialantheropods,withthe
et al., 2020) or troodontids (Tree4; Brusatte et al., 2014); updatesprovidedbyHendrickx&Carrano(2016)andPitt-
and (iv) troodontids among Deinonychosauria (Tree1; manetal.(2020)fornon-coelurosaurneotheropodsandpen-
Turner, Makovicky & Norell, 2012; Pei et al., 2020), as the naraptorans,respectively.
sistercladeofDromaeosauridae+Averaptora(Tree5;Motta
et al., 2020), or as the sister clade of Avialae (Tree6;
(1) Terminology
Avialae = Anchiornithinae + Archaeopteryx; Cau et al., 2017;
Foth & Rauhut, 2017).Our preferred topology (Tree1) fol- The anatomical nomenclature used to describe and annotate
lows a phylogenetic tree in which Sauropodomorpha and epidermalscales(Figs2and3)mostlyfollowstheterminology
TheropodaformthecladeSaurischia,JuravenatorandSciuru- providedbyLucas&Stettenheim(1972)andBell(2012),except
mimus are classified as early-branching non-avetheropod wherenoted.‘Feather’isusedhereintodescribeastructurein
Tetanurae (N.B., the integument of Juravenator is, however, whichthereisclearevidenceofbarbsand/orbarbulesandan
described in the section on Compsognathidae), anchior- inferredoriginfromafollicle(Campioneetal.,2020).Following
nithines are placed as the earliest birds, and Deinonycho- Campione et al. (2020), we use the general term ‘filament’ to
sauria is resolved. Althoughincludedin thedatamatrix for refertoallothernon-squamous,non-featherepidermalstruc-
comparative purposes, a large unnamed tyrannosauroid tures,recognisingthefactthatthesemayormaynothavediffer-
STM1-5(Xuetal.,2010)andthecontentiousmaniraptoran ing developmental origins from one another. Plumage herein
Yixianosaurus longimanus (Xu & Wang, 2003) were excluded describes the widespread covering of the body with feathers
in the analyses because their phylogenetic placement and/orfilaments.Termsrelatingtosquamousintegumentare
among coelurosaurians is unsettled (Dececchi, Larsson & organisedbycategoriesanddefinedasfollows:
Hone,2012;Xu,Sullivan&Wang,2013;Lambertz,2017).
Conversely,becauseofitsimportanceinourunderstanding
(a) Scaletypes
offeatherevolution(Xingetal.,2016;Lambertz,2017)and
whileitspositionamongcoelurosaursisunsettled,thespeci- Basement scales (bas) – small to large (typically 1–
menDIP-V-15103wasincludedintheanalysisandclassified 10mm, but up to 30mm) scales forming a major part of
asabasallybranchingnon-neocoelurosaurcoelurosaurina theintegumentarysurface(Bell,2012;Figs2B,D–I,3A).
singletree(Tree0)usingourpreferredtreetopology.Charac- Feature scales (fes) – large (>7mm) and regularly or
ter distributions for integument-based features were visua- sporadically arranged scales interspersed among and often
lised on each tree using WinClada 1.00.08 (Nixon, 2002) having a different morphology from that of the basement
based on the Nexus file created with Mesquite 3.6.1. Only scales(Bell,2012;Figs2B,D,3A).
unambiguous changes, which include non-homoplasious Midline feature-scale (mfs) – feature scales present
(apomorphies) and homoplastic changes (representedin the alongthedorsalmidlineabovetheneuralspines(Bell,2012).
figures by black and white circles, respectively), were visua- Podotheca (pod) – layer of scales covering the pes, from
lised.Alistofintegument-basedapomorphiesforeachclade thetibiotarsustotheendofthetoes,andvariouslycomposed
and taxon was created using TNT 1.5 (Goloboff & ofscutate,scutellate,andreticulatescales(Cuestaetal.,2015;
Catalano,2016)andisprovidedinAppendixS2.4. Fig.2C).
An ancestral state reconstruction analysis was additionally
performed in Mesquite 3.6.1 using the parsimony criterion Reticulate scales (res) – small circular-to-
withtheintegument-baseddatamatrixandthetreetopologies
polygonalscalesontheventral(plantar)surfaceofthe
Tree1toTree6(seeHendrickxetal.,2021b).TheParsimony-
toesandthelateralandposteriorsurfacesofthemeta-
Unorderedmodelwasusedasitisthesoftware’sstandardpar-
tarsus(Lucas&Stettenheim,1972;Figs2C,L,M,3G,
simony mapping for categorical data (Appendix S2.1). This
H).Reticulatescalesareheredividedintoprimaryand
calculates the most parsimonious ancestral states at the nodes
secondaryreticulatescales.
of the tree assuming one step per state change (unordered or
Fitch parsimony). In this analysis, the ichnotaxa Grallator and
Eubrontes (e.g. Gatesy, 2001; Demathieu et al., 2002; Milner Primaryreticulate scales(prs) –large reticulate
et al., 2006a) as well as the non-avialan coelurosaur DIP-V- scales adjacent to the scutate and scutellate scales
15103 (Xing et al., 2016), the oviraptorosaur Ningyuansaurus (Figs2L,3H).
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
8 Christophe Hendrickx et al.
Fig.2. Scaletypesandintegumentary-basedterminologyusedinthisstudy.(A)Exemplifiednon-maniraptoriformtheropodshowing
thepositionofeachscalemorphotypeillustratedinBtoM(courtesyofJohnSibbick,usedwithpermission).(B)Scalyintegumentofa
non-maniraptoriformtheropodfromthethoracicregionandshowingthebasementandfeaturescalesseparatedbytheinterstitial
tissues. (C) Podotheca from the pes of a theropod dinosaur and made of scutate, scutellate and reticulate scales (artwork inspired
from a drawing by Arturo García). (D) Feature and irregular basement scales. (E) Pebbly basement scales. (F) Oblong basement
scales. (G) Polygonal basement scales. (H) Ornamented basement scales. (I) Sagittate basement scales. (J) Scutate ventral scales.
(K) Scutate scales. (L) Scutellate scales. (M) Reticulate scales. bas, basement scales; cor, corrugations; emr, epidermal midrib; fes,
feature scale; ist, interstitial tissue; pev, primary epidermal vein; prs, primary reticulate scale; res, reticulate scales; sev, secondary
epidermalvein;sls,scutellatescales;sts,scutatescales.
Secondary reticulate scales (srs) – small to Scutateventralscales(svs)–large,rectangularor
minutereticulatescalesadjacenttothelargerprimary stadium-shaped scale covering the ventral surface of
reticulatescales(Figs2M,3H). the body (Figs 2J, 3C); resembling the ventral scales
(knownasthegastrosteges)ofmanysnakes.
Scutate scales (sts) – large, rectangular or
polygonal and regularly arranged scales on the Tuberculate scales (ts) – general term for any non-
anterior and caudal surfaces of the tarsometatar- imbricating, non-polarised scale (Figs 2B, D, E, G, L,
sus, the dorsal surface of the toes, and the ventral M, 3A–D, G, H). Tubercles can assume many of the
surface of the neck, belly and tail (Lucas & forms mentioned here (e.g. pebbly, polygonal, reticulate,
Stettenheim, 1972; Chuong et al., 2000; Figs 2C, scutellate) and may form either basement and/or feature
K, 3C, G). Also referred to as ‘scutes’ by Lucas & scales.
Stettenheim (1972).
(b) Scaleshapeandornamentation
Scutellate scales (sls) – rectangular or polygonal
andregularlyarrangedscalessmallerthanthescutate Irregular (irs) – basement and/or feature scales with no
scalesandfoundadjacenttothescutatescalesandon obviousgeometricalsidesandwhosesurfacecanbesmooth
the caudal surface of the metatarsus (Lucas & orcorrugated(Bell,2012;Figs2D,3A).
Stettenheim, 1972; Figs 2C, L, 3H). Also referred as Oblong (obs) – elongated basement scales with rounded
‘scutella’byLucas&Stettenheim(1972). extremities, such as those forming striate-like rows in some
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
Non-feather integuments in non-avialan theropods 9
Fig.3. Terminologyusedtodescribethescalyintegumentinnon-avialantheropods.(A)Mouldoftheskinfromtheanteriorportion
of the tail of the abelisaurid Carnotaurus sastrei (MACN-CH 894). (B) Natural mould of the skin from the neck region of the
tyrannosaurid Tyrannosaurus rex (HMNS 2006.1743.01). (C) Skin impression ventral to the 10th caudal vertebra of the putative
compsognathidJuravenatorstarki(JMESch200;takenbyC.IfrimandA.Hecker,courtesyofC.Ifrim).(D)Castofthescalyskinof
thetyrannosauridAlbertosaurus sarcophagus(TMP1994.186.0001).(E)ScalescratchlinesonthelateralborderoftheEubrontestrack
SGDS451.(F)DermalossificationoftheceratosauridCeratosaurusnasicornis(UMNHVP5278[UUVP80])indorsalview.(G,H)
SkinimpressionsfromthepesofthecarcharodontosauridConcavenatorcorcovatus(MCCM-LH-6666)associatedwithmetatarsalsIV
and V (G), and over the metatarsals and tarsals (H). bas, basement scales; cod, concentric dome; emr, epidermal midrib; fes,
feature scale; irs, irregular scales; ist, interstitial tissue; ors, ornamented scales; ost, osteoderm; pev, primary epidermal vein; pos,
polygonal scale; pol, polarised scales; prs, primary reticulate scale; res, reticulate scales; sev, secondary epidermal vein; sls,
scutellate scales; srs, secondary reticulate scales; ssl, scale scratch lines; sts, scutate scales; svs, scutate ventral scale. Scale
bars=5cm(F),2cm(A),1cm(E,G,H),5mm(B,D),and1mm(C).
part of the skin of titanosaur embryos (Coria & Sagittate (sas) – arrowhead-shaped basement scales,
Chiappe,2007;Fig.2F). typically showing imbrication (Bell & Hendrickx, 2021;
Ornamented (ors) – basement scales showing a ring-like Fig.2I).
circular structure adjacent to several longitudinal ridges Corrugation (cor) – radial striae on a scale surface
(Bell&Hendrickx,2020;Figs2H,3C). (Bell,2012;Fig.2D).
Pebbly (pes) – small basement scale forming a pattern of Papillae (pap) – minute ((cid:1)1mm diameter) dome-like
closelypacked,roundednodes(Bell,2012;Figs2E,3D).Pebbly protrusions on the scale surface variously described as
scalesontheplantarsurfaceofthepesarereferredtoasreticu- bumps, papilliform texture, or tubercles (e.g. Foster &
latescalesinaccordancewithavianterminology(seeabove). Hunt-Foster, 2011); commonly associated with sauropod
Polarised (pol) – scale with a distinctly elongated axis scales.
(e.g.medial–lateralaxis),asintheoblongandscutatescales Scale scratch lines (ssl) – parallel striations associated
(Bell,2012;Figs2C,F,J,K,3C,G). with vertebrate tracks and traces (Fig. 3E). They are pro-
Polygonal (pos) – basement and/or feature-scale with ducedbyscales(usuallyfromthepesintheropods)scratch-
three or more geometrical sides but typically ranging from ingthesubstrateandareoftengoodindicatorsofdigitand
fourtosixsides(Bell,2012;Figs2G,H,L,M,3B,C,G,H). foot movement. Estimations of scale diameters can be
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.
10 Christophe Hendrickx et al.
measured from these scratch lines (Milner et al., 2006b; (Hitchcock, 1858, 1865; Gierlin(cid:2)ski, 1994, 1997; Lockley,
Milner&Lockley,2016). Matsukawa & Jianjun, 2003; Kundr(cid:2)at, 2004). Impres-
sions of filamentous appearance are preserved on the
ischiadic imprint and the marginal line of the pre-pubic
(c) Interstitialtissue
imprint in the abdominal region of a theropod dinosaur in
Epidermalmidrib(emr)–mainand/orwidestbandof a resting posture (Kundr(cid:2)at, 2004). These filamentous
interstitialtissuebetweenfieldsofepidermalscalesandfrom imprints have been suggested to be feather impressions from
whichthesecondaryveinsarise(Figs2B,3B).Theepidermal semiplume-like structures (Gierlin(cid:2)ski, 1997) or branched
midribandveinssubdividepatchesofscalesontheskinand feathers (Kundr(cid:2)at, 2004). If true, the specimen AC 1/7
follow venation patterns similar to those on a leaf (Bell would be the earliest-diverging theropod with evidence of
etal.,2017). feathers. Lockley et al. (2003) and Martin & Rainforth (2004)
Interstitial tissue (ist) – integument of the hinge area have, nevertheless, interpreted these fine parallel striations as
between the scales and affording flexibility to the skin the result of the motion of the scaly skin against the substrate
(Bell,2012;Figs2B,3A,B,H).Alsoreferredtoasthe‘hinge (i.e. scale scratch lines) and pressure-release structures caused
area’. by the movement of the theropod when shifting its weight
Primary epidermal vein (pev) – accessory groove of and standing up, respectively. Small trapezoid tuberculate
interstitialtissuelaterallyarisingfromtheepidermalmidrib. scales are nonetheless present on the right posterior metatar-
Primaryepidermalveinstendtobesubparalleltoeachother sals of AC 1/7, representing a rare example of scaly skin in
and obliquely oriented from the epidermal midrib a body part other than the sole of the foot in a non-
(Figs2B,3B). averostran theropod. This is further supported by the pres-
Secondary epidermal vein (sev) – accessory groove of ence of scale scratch lines from the tail region of a probable
interstitialtissuearisinglaterallyfromtheprimaryepidermal theropodin one Characichnosswim track from the LowerHet-
vein(Figs2B,3B). tangian Moenave Formation of Utah (Milner et al., 2006b;
Appendix S3.1).
(d) Dermalossificationsandosteodermmorphotypes GrallatortracksfromtheUpperTriassic–LowerJurassicof
Greenland, Utah, and France preserve reticulate scale
Osteoderms (ost) – dermally derived bone-rich organs,
impressions and/or parallel scale scratch lines but vary in
which vary widely in form and location across the body
the arrangement of the scales (Gatesy, 2001; Demathieu
(Fig. 3F). Osteoderm morphotypes are either sagittate or
etal.,2002;Fig.4;AppendixS3.1).Thelargestcollectionof
mosaicintheropods. these come from 19 tracks from the Norian–Rhaetian of
Sagittate(sag)–ellipticalosteodermindorsalview,which Greenland (15–23 cm in length) in which scales are collec-
is flared ventrally and has a prominent anteroposteriorly
tivelyfoundonalldigitalpads.Despitethevariationinfoot-
elongated dorsal keel conferring a distinct Eiffel-tower out-
print length, scales are homogenous, consisting of polygons
lineinanteriorandposteriorviews(Fig.3F). (1–2mm diameter, with interstitial spacing up to 0.5mm)
Mosaic (mos) – osteoderm with indistinct and variable
arranged into roughly hexagonal clusters (Gatesy, 2001;
morphologies(D’Emic,Wilson&Chatterjee,2009).
Fig. 4A) or parallel, longitudinal rows (SGDS 642 Fig. 4B,
C). Other Grallator tracks from the Early Jurassic of France
(Fig. 4E–H) show a different pattern in which the smallest
IV. RESULTS scales are found on thecentral part of each digital pad and
increase in size centrifugally (Fig. 4F, G). This pattern is
Below,weprovidebriefdescriptionsofthesquamousintegu- reversed on the metapodium where scales decrease in size
ment preserved in currently known non-avialan theropods. centrifugally (Demathieu et al., 2002, Plate 5, figures 6 and
A comprehensive description of each of these is given in 8; Fig. 4H). Short ridges likely representing folds of skin on
AppendixS3. theundersideofthefootarealsofoundinatleastoneGralla-
tortrack(SGDS1211)fromthelowerHettangianSt.George
DinosaurDiscoverySiteofUtah(AppendixS3.1).
(1) Stem-averostranTheropoda
EubrontestracksfromNorthAmericaareconsideredtohave
Information on integumentary structure in non- been produced by a relatively large theropod similar to the
averostran theropod saurischians is particularly scarce stem-averostran Dilophosaurus (Marsh & Rowe, 2020; Marsh
and rests only upon skin impressions from pedal tracks et al., 2021). Numerous Eubrontes tracks (23–37 cm long) from
uncovered in Greenland, France, and the USA. To theEarlyJurassicMoenaveFormationincludeskinimpressions
our knowledge, epidermal structure with a well-defined (Milner et al., 2006b; Fig. 5). Despite the range of foot sizes,
pattern is unknown for the rest of the body in Coelo- scalesarerelativelyuniformandconsistofcircularorill-defined
physoidea and other stem-averostran Theropoda. Integ- polygons(0.6–1.75mmdiameter)andarrangedintolongitudi-
ument impressions have been described in the famous nal,transverse,orobliquerowsonproximaldigitIV,digitsIII
trace of a crouching theropod AC 1/7 from the Lower and IV, and proximal digit II, respectively as seen in
Jurassic Portland Formation of Massachusetts, USA Fig.5B,C,EandF(AppendixS3.1).
BiologicalReviews(2022)000–000©2022CambridgePhilosophicalSociety.