Accepted Article This article copyright.protected is by rights All reserved. 10.1111/jeb.13256 asdoi: cite thisdifferences Please article Record. of theVersion version between this and to lead may which process, proofreading and pagination typesetting, copyediting, the through been not has but review peer full undergone and for publication accepted been has article This Papers :Research type Article DR DENISCHARLES DEEMING: (Orcid ID 0000-0002-9587-6149) Keywords . late comparatively in evolved incubation contact Wedamage. that causing of suggest running the risk could not have evidence without yet approach saton their theearly that provides best birds heavier Our were eggs 110% their than support. indirect could earlyornithuromorphs some but birds, toextant comparable mass were and load mass For body the eggs. non-ornithothorac for that show we species, fossil 21 on Based remains. skeletal based on birds adult the of bodymasses predicted tothe compared were values These cracking. before endure could an egg mass the load hence and mass eggpredict elongati Known symphysis. the pubic by canal defined the pelvic of width the taxafrom avian Mesozoic of arange for breadth egg maximal Weestimated yetbeeninvestigated. has not adult a of breeding weight have the borne actually could birds Mesozoic whether the eggs but small, of are Mesozoicrelatively birds of living eggs Compared species to birds. extant of feature defining is a which contact incubation, of the of understanding our hampers which aspecies, to assigned canunambiguously eggs be avian Mesozoic No elusive. remains evidence direct but birds early of reproduction in interest an driven have fossils new Numerous Abstract 1 suggests that early Mesozoic birds were too heavy to contact incubate their contact their heavyto too incubate early Mesozoic were birds morphologythat suggests Pelvis School of Life Sciences, University of Lincoln, Joseph Banks Laboratories, Lincoln, LN6Lincoln, 7DL, UK; Laboratories, Banks Lincoln, Joseph of of LifeSchool University Sciences, 2 Ornithological Section, Senckenberg Research Institute and Natural History Museum Frankfurt, Museum Frankfurt, History andNatural Institute Senckenberg Research Section, Ornithological

: egg size, contact incubation, Mesozoic , pelvic canal width, shape shape pubis pelvic canalwidth, Mesozoic bird, incubation, contact size, : egg Senckenberganlage 25, 60325 Frankfurt am Main, Germany Germany amMain, Frankfurt 60325 25, Senckenberganlage Corresponding author mailid:[email protected] D. C. Deeming C. D. eggs ine birds body mass was 130% of the load mass of massof theload of was 130% mass body birds ine

1 & G. Mayr &G.

on ratios of Mesozoic bird eggs allowed us to us eggsallowed to on of Mesozoic ratios bird 2

Accepted Article This article is protectedThisarticle is byAll rightsreserved. copyright. range taxa. of a broader across comparisons adult inhibitsmeaningful of birds remains skeletal of eggs identifiable with association Unfortunately, the unambiguous 2016). Jackson, & (Varricchio small relatively is size egg andgenerally 2015) Barta, & Varricchio 2006; (Deeming, bird from the presumed derived the species extinct using from extant massof body a relationship predicted can be size egg evidence, direct fossil Aside from 2014). Ruta, (Deeming & birds modern al 2010). al., et Huynen 2009; Deeming, & eggs (Birchard the incubated males probably which the smaller in dimorphism sexual reverse in mass resulted load and mass body female avery high between disparity birds palaeognathous flightless and large extinct some in but mass, parents’ thanthe muchgreater are before breaking can tolerate eggshells thatbird masses load the Generally, allow enough Juang 1979; 2017). etal., etal., the to thin tohatch(Ar young the remaining whilst mass incubation bird the of during Eggshells2002b). haveadult towithstand by the (Deeming, adults incubation contact for need the particular, in and, environment the nesting to attuned is Egg offspring. the by required care parental of degree the turn on impacts in isin as pivotal it performance egg reproductive of size isa birds, element key Inextant which 2007), (Deeming, hatching at maturity developmental to related is and size clutch determining . of group important this in reproduction of understanding our restricting is therefore Mesozoicbirds in reproduction of record fossil Theincomplete eggs. associated with remains skeletal articulated of are there &Barta, 2015), noexamples (Varricchio hind fragmentary with association close in found been has Mongolia of Cretaceous theUpper from aneggclutch Although existbirds. for donot fossils 2017) and equivalent &Mullin, Bois 2004; &Unwin, Deeming 2015; 2002a, (Deeming, accepted universally isnot 2016) & Varricchio Jackson, 2011; Varricchio, 1999; al., et (Clark incubation contact exhibiting are eggs of clutches on sitting theropods non-avian that The hypothesis 2017). Wanget al., 2011; al., Lüet 1999; al., et (Clark apterosaur and theropods somenon-avian for seen as remains, skeletal and eggs between association close than rather structure of tobirds eggshell on the basis Eggs attributed are2014). invariably & eggs Ruta, (Deeming bird Cenozoic fossil and than extant elongated more are and 2016) &Meng, Chiappe 2016; Jackson, & Varricchio 2010; extant (Dyke species &Kaiser, compared with berelatively small to considered are eggs bird Mesozoic species, of any adults to known unattributed Although 2015). (Deeming, rare extremely remain embryos that contain those but 2016), al., et Lawver 2016; & Jackson, (Varricchio reported been have birds Mesozoic eggsof Various 2016). &Jackson, Varricchio 2015; 2002a, (Deeming, beingcontentious incubation especially of withthe origin contact understood, poorly remains birds early and theropods non-avian of behaviour reproductive of evolution The Introduction ., 2016) and their elongated symmetrical shape sets them aside from the asymmetrical eggs laid by by laid eggs the asymmetrical from them aside sets shape symmetrical elongated their and 2016) ., Lawver 2016; & Jackson, directly (Varricchio eggs canbemeasured bird fossil The size of

et et Accepted Article species of Early Cretaceous Enantiornithes (e.g., (e.g., Enantiornithes Cretaceous Early of species This article is protectedThisarticle is byAll rightsreserved. copyright. species of EarlyCretaceous ornithuromorphs(e.g., (e.g., Ornithothoraces outside birds Cretaceous 2017). 2016, belong birds (Mayr, modern to which charact bones, pubic separated widely with symphysis, pubic open A consistently and ornithuromorphs. basal in enantiornithines remainmost in connected pubes of the thetips Ornithothoraces, Within 2016). &Meng,Chiappe 2010; & Dyke Kaiser, 2007; (Kaiser, pass to have would egg an which through thespace delimits effectively synsacrum the and symphysis the by formed theopening birds, these In symphysis. pubic closed a by characterised are Ornithuromorpha, and Enantiornithes taxa sister the including clade the Ornithothoraces, outside birds basal Phylogenetically Mayr, 2016). 2010; Kaiser, eggs of & (Dyke maximumbreadth the predict substant underwent morphology pelvic However, to used be also could birds Mesozoic of dimensions pelvic that suggested hasbeen and it evolution taxonomic differences in pubis shape for Mesozoic birds. birds. Mesozoic shapefor pubis in differences taxonomic examine wealso Finally, birds. extant values for equivalent and with specimens fossil same individual the mass body thepredicted of with value this compare We breaking. then without eggs bear could the mass and maximum load the egg mass species calculate modern we for this value inrelationships Using the bird. by the egg laid of breadth the define to Early Cretaceous and the Late Jurassic from species bird of arange of canal pelvic the of width maximum the of measurements use We remains. skeletal their from birds Mesozoic of dimensions egg predicting of approach novel the pursue we Here behaviour. incubation their explore to species extinct for mass egg predicted can use we Hence, extant birds. in behaviour incubation mass and body contact allows between mass egg relationship the Additionally, eggmass. with correlates turn in which symphysis, fused pubic with birds extinct Deeming & Mayr [2018] for detailed methodology) (Zelditch (Zelditch for methodology) detailed Deeming &Mayr [2018] pubis shape(see of determination 2006) for in TPSDig2 geometric to allow morphometric (Rohlf, pubis imposedon the digitally Semilandmarks were (https://imagej.nih.gov/ij/). image ImageJ using the from measured was canal pelvic the of width maximum The image. published the from derived and or lengths this measurement for value of and thepubis, length the could be hadapublished also either aspect, and ventral or adorsal from pubes seen of pair articulated Late Jurassic the taxon includes Our sampling (2018). Deeming &Mayr in as published listed from reports species birds Mesozoic of 21 different Data for collected were Materials and methods isphysically breadth egg isthat hypothesis Our Species were selected on the basis of published images of a specimen that showed an showed that aspecimen of images published of basis the on selected were Species

Confuciusornis Changzuiornis Cathayornis erizes the ornithuromorph subclade Ornithurae, subclade Ornithurae, ornithuromorph the erizes constrained by the width of the pelvic canal in the of pelviccanal in width the by constrained ial modifications inthe ial modifications course avian of

et al et , Jeholornis , Parapengornis , ., 2012). and and Yanornis Sapeornis and and Zhouornis ). ), as well as as aswell ), and Early andEarly ) and ) and Accepted Article Core Development Team, 2012) to predict body mass from Log from mass body predict to Team, 2012) Development Core R (R in used was (pglm) regression squares least controlled phylogenetically on Birdtree.org, option 863 used Field by sexes and re-analysed the This data. 315species process reduced dataset the to (fromasize sample of both for replicated a species data any for averaged elements sowe skeletal from mass predictions and female analysis Initial th individuals. showed for a species. To correct for this, mean values for femur and humerus lengths were calculated malefor mass body mean single a used but specimens multiple of elements skeletal of measures on was based Fieldby analysis presented original The be accurate. more will limbs the and hind of fore soutilise that girdles calculations elements pectoralthe and both to reflect pelvic musculature around going is body mass Moreover, reliable. not are they fossils the of crushing to due or available, are not values such birds Mesozoic most for mass body of measure accurate more a provides circumference Field bypresented data of analysis on based lengths This article is protectedThisarticle is byAll rightsreserved. copyright. published values for breadth and length from Schönwetter (1960-1985) used in the equation: equation: the in used (1960-1985) Schönwetter from and length breadth for values published based on predicted was eggsmass For extant 1990). Ferguson, Deeming 1.64; & = 10 crocodilians of ratio elongation eggs (mean bird Mesozoic existing of shape elongated the represent which better eggs & 1990), crocodilian Ferguson, for (Deeming where isthemeandetermined 0.597 constant mass combined from two studies (Ar studies two from combined eggs bird 1979). (Hoyt, for determined constant meanmass isthe where 0.548 1979; Deeming & Ferguson, 1990): Deeming 1979; 1990): & Ferguson, (Hoyt, from equation a modified using g) (in mass egg calculate used to were Thesevalues 2016). &Jackson, eggs Mesozoic (Varricchio bird for values published = derived from (SE 1.757 0.060) of ratio egg elongation amean on based calculated was then mm) (L, egg in of the Thelength 0.814. maximum egg breath (B, in mm) was calculated the by multiplying maximum pelviccanalby width study this in Therefore, 2018). (Deeming, aperture pelvic the maximum of 0.814 average is on breadth egg maximum the that showed chelonians speciesof 17 for collected data published However, (R² = 0.9256; the equation: basisof on the was calculated birds Mesozoic of (g) body mass Therefore, model. best the determine were Criteria used to Information Akaike together. lengths or femur humerus and humerus length, new relationship the outlying excluded the ( new for data relationship Body mass of the individual specimen was calculated on the basis of femur and humerus humerus and femur of basis the on calculated was specimen individual the of Body mass EM = 0.548·L·B²·10 A new relationship was generated for load mass of an eggshell using data for extant species species extant datafor using eggshell an mass of load for wasgenerated A newrelationship Maximum pelvic canal width was assumed to limit the maximum breadth of the egg. the egg. theassumed maximum tolimit was width breadthof Maximum canal pelvic Log = 1.130 Body mass EM = 0.597·1.757·B³·10 λ = 0.941). Body mass for extant birds were taken from Dunning (2007). (2007). Dunning from taken were birds extant for Body mass 0.941). = et al et ., 2013). A phylogenetic was generated using the “Hackett All species” species” All “Hackett the using generated was phylogenetic tree 2013).., A -3 (Eq-3) · et al et Log Humerus Length +1.356 +1.356 Length Log Humerus -3 (Eq-2) ., 1979; Juang 1979; Juang ., at sex was not a significant factor body factor affecting asignificant at sex was not et al et al et ., 2017) that took into account phylogeny. Our Our phylogeny. intoaccount took that 2017) ., . (2013). Although we appreciate that femur femur that weappreciate Although . (2013).

· Log Femur Length – 1.690 Length Femur – Log (Eq-1) 1.690 Struthio camelus Struthio 10 -transformed data for femur length, ) egg,) which is two et al . (2013) (2013) . Accepted Article This article is protectedThisarticle is byAll rightsreserved. copyright. equation: the of basis the on calculated was birds and extant Mesozoic of (g) mass load Therefore, mass. calculated egg from mass load predict to 2012) Team, Development Core (R R in used was (pglm) regression least squares controlled a phylogenetically Birdtree.org, on species” option the All “Hackett (Packard regression Log-transformed natural have studyand socould our egg than this range biased the sizes greater magnitude in of of orders Mesozoic bird mass. The effects of taxonomic group and category of mass were both significant ( significant mass both were of category group and taxonomic effects of The mass. bird Mesozoic the predicted until breaking with endure mass anegg could (g)that calculated maximum load of body mass. eggs8.5% lay thataverage birds The extant respectively. Ornithuromorpha, and Mesozoic Enantiornithes non-ornithoracine birds, and for 1.71 1.01 as eggmasses Predicted 1). (Table canal dimensions the pelvic predicted that from than greater at seven times isapproximately which 2007), (Deeming, birds extant in mass eggs and precocial mass body female between therelationship describing smallerthe 28 than of from value the gestimateegg is equation significantly calculated mass for This wereeggs andthe (Table laid by 1). smallest birds were laid by Enantiornithes non-ornithoracine The largest g; 41.0 Table of an 1). outlier with g a 2.0 0.6–10.8 of ofrangewith g(SE 4.7 averaged birds Cretaceous and Early Late Jurassic of species 21 the for masses egg The predicted 2018). ( species asingle large for species except all to 26mmfor 10 between ischia andranged the closeto position (Table 1). had masses comparable body the Ornithuromorpha the Mesozoic to of size femur in similar were that species Extant 1). (Table Ornithuromorpha Early Cretaceous for predicted masses theof that half than less and birds non-ornithothoracine for predicted masses the of asixth only about were Enantiornithes for masses body Predicted 1). Ornithothoraces (Table of members Cretaceous Early than heavier were birds non-ornithothoracine basal lengths, humerus and femur Based on Results pubis. the length the of along semi-landmarks analysis component of principal generated by PC2 and on PC1 MANOVA and general tests Wallis Kruskal using investigated were types bird the between shape pelvis in Differences reported. cases all in and removed terms observed were interaction Non-significant factors. mass asfixed load and egg mass the body and group taxonomic of effects the compare to 17) (ver. Minitab using analysed were models linear whilstOrnithuromorpha) controlling for femur length as and a covariate. General, general mixed, and Enantiornithes (non-ornithothoracine, grouping taxonomic of theeffect test for covariance to

Statistical analysis involved Log analysis involved Statistical Log 0.835 Load mass = The maximum width of the pelvic canal delimited by the pubes was typically in an anterior ananterior in wastypically bythe pubes delimited canal of pelvic the The maximumwidth A general linear mixed model, with species as a random factor, the compare was used withspeciesA factor, mixed asato linear general model, random Sapeornis

chaoyangensis · Log Eggmass (R² 1.861 0.8441; + = ), which had a pelvic canal width of 42 mm (see Deeming & Mayr, 10 -transformation of the data before doing analysis of of analysis of databefore doing the -transformation et al et ., 2009). Using a phylogenetic tree generated from from generated tree aphylogenetic Using 2009). ., a percentage of predicted body mass were 0.80, body 0.80, predicted were mass of percentage a

λ = 0.734). (Eq-4) (Eq-4) 0.734). = F 2,20

Accepted Article Varricchio & Jackson, 2016). 2016). & Jackson, Varricchio from and 27mm,respectively, 22.3 (20, here reported the values allwithin of range liewell 2013) Mongolia 2004), (Balanoff &Zhang, (Zhou China eggs from enantiornithine of diameter the 41mm. Likewise, were below 2 (2016) only bywere and Jackson 14 below all 20 mm reported values but Varricchio of valuesthe the Of mm. be<15 to predicted egg breadths had species four but all but mm 8.6–33.9 was breadths egg our of The range record. the fossil eggs in avian larger of examples many are there that appreciate Lawver 2016; &Jackson, (Varricchio birds to attributed eggs fossil incubation. of pattern the for consequences havehad would this and small very relatively study were inthis the Mesozoic birds eggs of Hence, the (see 2018). the pubis Deeming &Mayr, the lengthof by pelvis delimited thesize ofthe within well theeggs fit lengths of calculated the canal. However, the pelvic for size minimum a preserved but size body affected birds early in changes Evolutionary 2016). & Jackson, (Varricchio egg birds Mesozoic estimates size for thanother smaller in such is and species extant datafor from predicted that 25%of around amass to eggs size of physical This article is protectedThisarticle is byAll rightsreserved. copyright. = 4.67, Discussion pubes ashorter delimit having canal. relativelyto wide pelvic by relatively exaggerated was further the pattern theEnantiornithescanal. this a In pelvic U-shaped of more so forming symphysis pubic the to anteriorly recurved more were the pubes Ornithuromorpha the In canal. pelvic V-shaped a and formed straight relatively thatwere pubes ornithothoracine had non- Quantitatively, 1). (Table the Enantiornithes in longer times 2.3 wasonly but Ornithuromorpha and birds non-ornithothoracine canal for pelvic than longer times three was approximately pubis the Theof length 0.178). DF = 2,P = 3.45, covariate = (H asignificant but PC1 was not 0.014) DF test: Wallis 2, P=H =8.28, = (Kruskal group taxonomic by affected PC2, was significantly which Wilk’s test: (Fig. 2; group affected taxonomic by PC1and PC2were significantly that showed MANOVA General respectively. inshape, variation the of and 15% ~75% explained (29) values and PC2 PC1 that (Fig. 1). laidthem that birds the of body times the three wasover support could eggs extant massthat the load contrast, By greater than the(Fig. loadmass the 1). mass ~79% predicted Ornithuromorpha was body forthe and values theEnantiornithes were these for heavier mass,but ~27% lower than load ~87% was body mass birds, non-ornithothoracine For the model. from wasremoved and significant The predicted breadth of Early Mesozoic bird eggs is smaller to that of many of the known known the manythat of of to smaller eggsis Early bird Mesozoic of breadth The predicted the constrained that canal apelvic delimited symphysis the pubic that suggest analyses Our

Geometric morphometric and principal component analysis component morphometric and principal &Geometric (Deeming 2014) revealed Ruta, P = 0.023; 0.023; =

λ = 0.552, F 1,20 F = 12.61, =12.61, 4,34 = 2.9, et al ., 2008) and Argentina (Schweitzer (Schweitzer Argentina and 2008) ., P P < 0.001, respectively; R² = 89.0%) but the interaction was not was not the interaction but 89.0%) R² = respectively; 0.001, < = 0.035). This effect was primarily associated with variation in variation with associated primarily was This effect =0.035).

et al et et al et ., 2002; Fernández Fernández 2002; ., ., 2016), although we although we 2016), ., et al ., Accepted Article tortoise tortoise smaller birds (Ar eggs the problematical. makes assigning This article is protectedThisarticle is byAll rightsreserved. copyright. aperture (Prieto-Marquez thepelvic of width mm the65 average of 65% which is 1990), Ferguson, & mmonly 42 (Deeming which is aratio Inof 0.833. female American ( observations), 12.5cm of personal aperture is15cm andthebreadth pelvic maximum (Deeming, ( Ostrich the symphysis, pubic aclosed with species bird extant the only Moreover, (Deeming, 2018). width and pelvic maximal breadth between egg relationship of the is a very and there good pelvicmaximal eggs 81.4% averages of width Breadth only turtle canal. pelvic the through alsopasses tract the gastro-intestinal and tissue soft bylayers of surrounded bonesare than egg issmaller the maximalthe because opening breadth that indicates pelvic is justified. birds to birds eggsthe fossil of extant data of mass applying load of approach our that consider We, therefore, 2017). communication, &Webb, personal (FigureManolis S5; shape structure andmore elongated eggshell the different avian thesame mass, of tothat of despite eggs equivalent is this eggshowthat to break acrocodilian data the loadmass for limited of theHowever, our on impact and this interpretation data. 2016) could Jackson, & Varricchio 2014; Ruta, &Deeming (see birds extant those of than structure eggshell and shape havea different birds early Mesozoic of eggs We that acknowledge adult. incubating than the al et both of the remains contain strata same the secondly, and, theeggs,with found havebeen element skeletal no firstly, because, unfounded if aconclusion such However, size. body adult the of 7.5% eggs were the enantiornithine (Fernández Argentina in found eggs Avian 2015). al. et (Varricchio remains avian contain to shown been has neoceratopsian (Fernandez alizard of remains contain Lawver 2016; Jackson, & (Varricchio study this instance, presumed “theropod” eggs from Thailand (Buffetaut (Buffetaut Thailand from eggs “theropod” presumed instance, of eggs can the taxonomic For in of origin be isolation assessment found difficult. remains. Moreover, direct in not and China outside locations Cretaceous Late Early and of arange in found mainly were which eggs, these of origin and geographical ., 2017; Juang Juang 2017; ., Neuquenornis Homopus signatus Homopus Load mass of eggs of extant species is very high compared to body mass, especially in in especially mass, body to compared high very is species extant of eggs of mass Load Predicting egg size from pelvic dimensions is not unrealistic but data from extant species species data from extant but unrealistic isnot pelvic dimensions from egg size Predicting in included could belaidby than theare birds broader toMesozoic eggsSome attributed birds et al and the much larger ornithurine ornithurine themuch larger and et al et Neuquenornis volans Neuquenornis ., 2017; Juang Juang 2017; ., ., 2017), it is unclear why bird eggs need to withstand masses much greater greater much masses withstand to need eggs bird why isunclear it 2017), ., et al et that lays that thanits eggs are (Hofmeyr that pelvic aperture larger ., 2007). There is, however, one report of pelvic kinesis in the smallest smallest the in pelvic kinesis of one report however, is, There 2007). ., et al ., 2013) have been linked by Varricchio and Jackson (2016) with (2016) and Jackson Varricchio by linked have been 2013) ., et al ., 2017). Whilst load mass correlates with shell thickness (Ar (Ar thickness shell with correlates mass load Whilst ., 2017). (Clark & Norell, 2001) and it has been suggested that the suggested that and has been 2001) it &Norell, (Clark et al ., 2015). Similarly, an egg originally attributed to a to attributed originally egg an Similarly, 2015). ., et al et ., 2016). This may reflect the differing temporal temporal the differing may This reflect 2016). ., association with comparable articulated skeletal skeletal articulated comparable with association Patagopteryx mississippiensis Alligator

et al et Struthio camelus ., 2005) wereeventually shown to (Fernández (Fernández ), has an average egg egg average has an ), et al et ) ) the average egg is ., 2013), which which 2013), ., et al et ., 2005) 2005) ., Accepted Article This article is protectedThisarticle is byAll rightsreserved. copyright. not universally (Birchard accepted (Varricchio eggs their incubate and contact on tosit able were avian theropods and re eggmass for implications its and theropods Mullin, 2017). Clearly, thereis aneed further for into theinvestigation size ofthepelvic canals of & Bois 2002a; (Deeming, very unlikely was intheropods thesupport contact view incubation that serve to Such values predicted. the of 20-50% eggs only were for masses load and calculated (0.5-1%) mass body relative to small egg very was mass that suggest 2013) (Werner & Griebeler, theropods of species four for egg and of mass body mass – bodyestimates of 0.02% mass. only Data for an 2014) & Ruta, (Deeming sometheropods in found 2.1 of ratio anelongation – with theropods by be laid could that egg sizes for implications profound has This of aperature pelvic the that show that drawings provides (2001) Hutchinson study, our of the scope beyond is canaltheropods in the pelvic of the of dimensions comprehensive review Whilst a shaped pelvic canal to relatively short bones delimiting a U-shaped pelvic canal. aV- bonesforming long relatively straight, from changed thepubes have of shapes means thatthe Enantiornithes, which for the reduction a significant exhibited The hasonly the pubes length of birds). ca pelvic aminimum of maintenance accommodate the to shape thepubishave thisboneseemsto changed of the length in but reflecteda reduction in was birds) to non-ornithothoracine (compared size body in reduction the overall Enantiornithes by example, inEarly means, physically the limitation for pelvicThis Cretaceous delimited that canal. was that birds Mesozoic for width egg maximum a was there that suggests conserved was width canal pelvic size, body whilst with scales length thatpubic study our fact the in thespecies Hence, for these to eggs species. a attributed being there fossil despite lack of theirinto reproduction insight size futher. and egg egg which reduces breadth overestimates, most likely therefore,likely to limit thewidth of thepelvic is, of pelvis the reconstruction Three-dimensional synsacrum. the below thespace have delimited would ischiumpubis , ofthe and articulation life the and in canal pelvic of the that similar to very isusually thesynsacrum of width the However, unrealistic. pubes may be thearticulated of cr considerable exhibit all articulated are unclear. also themovement of is pelvic bones much for allow would musculature pelvic Whether limb the breadth. egg would and this limit girdle inthe pelvic place takes eggformation egg. However, a larger of laying allowing pelvic kinesis exhibited study in this described birds Mesozoic the small that possible is It may unusual. this be but A bypelvic canal delimited a symphysis non-avian pubic is aof general. in feature theropods provides birds Mesozoic egg size in calculate canal to pelvic the of dimensions Using the many whilst usedinthisstudy but the is remarkable of birds preservation of The degree measured ~ 7cm in breadth for an animal estimated to weigh 1500 kg (Bates 1500 weigh estimated to ananimal for breadth 7cmin ~ measured et al ., 2013), is not supported by the present study. the isnot by study. ., present 2013), supported canal further. This means that our measurements are are measurements our that means This further. canal production in these animals. The concept that non- that concept The animals. these in production ushing. This could suggest that our measurements measurements our suggest that could This ushing. nal width (> mmnal width 10 inthese Mesozoic Chinese Allosaurus

egg isestimated to gbe ~430 et al et ., 2008), whichis ., 2008), et al ., 2009). 2009). ., Accepted Article This article is protectedThisarticle is byAll rightsreserved. copyright. t-test paired 8±200. = 49.6; thickness eggshell predicted ±100.7; 223.3 thickness: eggshell (actual significant not was difference but this predicted than greater actual thicknesses actual that thesethicknessand for eggs ~10% predicted fossil eggshell showed is mean of Comparison (±SD) & 2009). Deeming, bird species extant (Birchard for the relationship from thickness eggshell predict hence and egg mass calculate can beused to eggs these dimensions of (Lawver birds enantiornithine to attributed eggs are there but here studied to the species attributed eggs no of Weknow body mass. the withstand able to so better 2002d). (Deeming, in which contact the incubation, eggs need also tobe for development regularly normal turned Fernández 2006; (Deeming, sediment in deposited partially at least were thatthese show birds enantiornithine of eggs for data limited the addition, In envisage.to difficult scenario make this does the eggs of smallness relative the and contact bodily intimate Such aneedto 2002). Klandorf, (Lea & transfer of skin body the ventral heat developand thetopof often patch to the abrood eggsand facilitate between the incubation contact on rely birds extant However, weight. their of all applying without of true contact evolution incubation. the bodyand allow support mass can to laywhich larger eggs, birds allowing eggsizeremoved on restriction the was the Ornithurae in be isopened up very symphysis Only when the egg still but the high. pubic scope for would breakage smaller is Enantiornithes the sizein bird and load eggshell between Thedifference Ornithuromorpha. Early Cretaceous and non-ornithothoracines in precluded most likely was Deeming, 2002c), (see birds byextant asexhibited contactincubation, havemeant that eggs would the load massof the and bodymass inthe Differences . of eggs small relatively the to comparable are so and 2009; Huynen &Deeming, (Birchard (Dinornithiformes) e.g., somein species, dimorphism reversed sexual to leading incubation contact for safety margin alow was there eggshells that meant thin combined with mass, shellegg size, ratites inextinct thickness su and body of Analyses causing damage. without birds toextant breeding a eggs similar their manner in on sit to hard find it would species these that suggests here as indicated Mesozoic birds the eggs of chances of fossilisation or discovery. This study does predict that any avian eggs found from the from eggs found any avian that predict does study This or discovery. fossilisation of chances larger here. sizesmall thanthe This of the apparently size eggs the mayreflect predicted disparity be to tend and they rare areembryos contain eggs that Avian skeletons. articulated of preservation of future fossil specimens may allow us to but eggs extant tocomparable loadsmasses be withstand to able would eggshells enantiornithine Another possibility is that the shells of the eggs laid by these Mesozoic birds were thicker and and thicker were birds Mesozoic these by laid eggs the of shells the that is possibility Another this achieve eggs ableto sit ontheir to were birds first thein the Mesozoic that possible It is the by endured besafely could that mass load andpresumed mass body between The disparity This study primarily focusses on Mesozoic birds from China, which exhibit remarkable levels levels remarkable whichexhibit China, from birds onMesozoic focusses This primarily study et al et al et ., 2013; Varricchio & Jackson, 2016), which contrasts with a contrasts with avian &which 2013; 2016), Varricchio ., Jackson, modern-type ., 2010). Egg sizes are relatively small (< 1.5%) 1.5%) in (< small all ofthe here species Mesozoic 2010). relatively Egg., sizes are test whether is this generally true. ggests that the relatively small size of the eggs size of eggs the small the relatively that ggests t 5 =-0.69,

et al et p = 0.523). This suggests that that suggests This 0.523). = ., 2016). Where available Where available 2016). ., Accepted Article Clark, J.A. & Norell, M.A. 2001. The morphology and phylogenetic position of of position phylogenetic and Themorphology 2001. M.A. &Norell, J.A. Clark, Chiappe, L.M. & Meng, Q. 2016. L.M. 2016. Chiappe, &Meng, Q. Buffetaut, E., Grellet-Tinner, G., Suteethorn, V., C V., Suteethorn, G., E.,Grellet-Tinner, Buffetaut, was Late Cretaceous: the during and predation ecology nest Dinosaur 2017. S.J. &Mullin, J. Bois, behaviour in incubation of parental Evolution M. D.C. & Ruta, 2013. Deeming, G.F., Birchard, for implications thickness: eggshell avianof Scaling D.C. 2009. G.F. &Deeming, Birchard, This article is protectedThisarticle is byAll rightsreserved. copyright. 2009. W.I.Manning, &P.L. Sellers, D., Hodgetts, B.H., Breithaupt, P.L., Falkingham, K.T., Bates, a of Digital preparation & 2008. M.R. G. Lewin, M.A., Grellet-Tinner, A.M., Norell, Balanoff, 1979. The C.V. egg: andstrength. mass avian & H., Paganelli, A, Rahn, Ar, References draft of this manuscript. a previous made of reviewers by comments constructive the the We appreciate of version manuscript. aprevious on comments critical provided Soulsbury Carl and Humphries here.Eady, Stuart Paul described analysis and concepts the about discussions constructive for Unwin and Dave EadyPaul Acknowledgements. symphysis. the pubic of opening an with associated egg width in an increase was there after only evolved probably birds, in extant asobserved incubation, contact that suggests strongly accommodate eggshells could their than heavier much were Mesozoic birds That increase. only can size eggand mass bird between differences that suggests which canal, themaximum pelvic based on mass egg canover-estimate only values above, Asnoted our birds. small. be very to likely are China of Mesozoic from the Late Cretaceous of Mongolia. Mongolia. of LateCretaceous the from University Hopkins John 477–482 477–482 the Lower Cretaceous of Thailand and the dinosaur-bird transition. transition. and thedinosaur-bird Thailand Lower of Cretaceous the from embryo eggs and theropod 2005.Minute J. LeLoeuff, & J. Tabouelle, P.J., Griffiths, S., 10.1080/08912963.2016.1277423. behavior? nesting and extinction Cretaceous upper between arelationship there clutch mass from birds. be in inferred cannot body maximum birds. in mass predictions for for predictions mass on unknowns osteological and soft tissue effect of the Quantifying Al’? as‘Big big How of ornithischian eggshells. eggshells. ornithischian of anatomy microstructural on comments anegg, with within preserved neoceratopsian probable in Mesozoic reproduction imposed upon the limitations demonstrated indirectly study Our has

The authors confirm that they have no conflicts of interest. DCD is grateful to to grateful is DCD interest. of conflicts no have they that confirm authors The Allosaurus Press, Baltimore. (Dinosauria:). (Dinosauria:Theropoda). Naturwissenschaften Naturwissenschaften Birds of Stone. Chinese Avian Fossils from the Age of Dinosaurs Age of the from Fossils Chinese Avian Stone. Birds of J. Zool. J.

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Accepted Article This article is protectedThisarticle is byAll rightsreserved. copyright. Mesozoic birds in the dataset. of groups taxonomic three the for shape pubis of analysis morphometric geometric semi-landmark a derived from and PC2) components (PC1 two principal first (±the Fig. for 2. SE) values Mean

body mass eggmass and for birds groups three and extantof Mesozoic birds. width*0.814 width*0.814 from pelviccanal massEgg (g) predicted from birdmass massEgg (g) predicted and humeruslengths femur from predicted Bird mass (g) canal width Pelvic / length Pubes (mm) width Pelvic canal, (mm) length Pubis (mm) Femur length (mm)Humerus length 1. Table

*Actual mean mass derived from Dunning (2007); from mean Dunning mass derived *Actual derived from Schönwetter derived from Schönwetter (1960-1985) Summary statistics (mean ± SD) for femur and ± femur and for SD) (mean statistics Summary ornithothoracine 753.5 ± 753.5 210.9 76.1 ±10.6 76.1

45.1 ±45.1 8.8 ±19.8 3.8 ±52.1 6.9 ±56.5 5.7 8.6 ± 8.6 5.6 ± 2.8 0.2 (N = 6) =6) (N Non- birds Enantiornithes Enantiornithes 124.7 ±124.7 33.5 13.2 ±13.2 1.1 ±28.5 3.0 ±28.2 2.9 ±36.5 4.9 13.0 ±13.0 2.5 2.2 ± 2.2 0.1 1.5 ± 1.5 0.4 (N = 7) =7) (N pelvic dimensions and various predictions for various predictions dimensions and pelvic #

Calculated from actual egg dimensions dimensions egg from actual Calculated Ornithuromorpha Ornithuromorpha 386.6 ±386.6 89.4 17.3 ±2.0 17.3 4.8 ± 48.0 5.1 ± 42.2 6.5 ± 60.0 28.5 ±5.1 28.5 Mesozoic 2.9 ±0.3 3.5 ±1.2 (N = 8) 381.0 Extant birds 27.8 41.6 ±41.6 2.4 ±43.2 2.5 ±59.3 3.2 (N =20) (N * # - - - ± 3.8 ± ±44.1

Accepted Article