WATER VAPOR CONDUCTANCE IN FOSSIL EARLY BIRD EGGS AND NON-AVIAN THEROPODS: IMPLICATIONS FOR THE EVOLUTION OF MODERN BIRDS EXPOSED NEST STRUCTURE

Rodrigo Brincalepe Salvador 1#^%:C0:RQ`8`QR`1$Q8G$I:1C8HQI_5# Lucas Ernesto Fiorelli #^C`1Q`VCC1H`1C:`RHQJ1HV 8HQI8:`_ 1:%%V%#RV#QQCQ$1:#R:#J10V`%1R:RV#RV#>>Q#@:%CQ#^:>@_6# BVJ `Q#CV$1QJ:C#RV#DJ0V% 1$:H1QJV%#B1VJ 3`1H:%#7#G`:J%`V`VJH1:#GVHJQCS$1H:#^BCDIJCRBKLDBMG_5#JJ1CC:HQ5#I:#C1Q=:5#J`$VJ 1J: ABSTRACT em Avialae. Mais estudos que lidem com outras aves fósseis e Maniraptoriformes são necessários The functional properties of eggshells e GH 2O pode ser uma valiosa ferramenta para tal )/*& 5 1#."5 *, (.&5 ( -.#(!5  "0#),-5 !, .&35 (ainda que subutilizada até o momento). #( &/ ( 5 ." 5 -/ --5 ) 5 ',3)! ( -#-5 (5 Palavras-chave: Avialae, Enantiornithes, "."#(!85
-5-/"65)( 5) 5." 5'#(5*"3-#)&)!#&5 Neuquenornis volans *,)* ,.# -5 ) 5 ." 5 !!-" &&65 ." 5 1. ,5 0*),5 conductance (GH 2O), of the Patagonian ((.#),(#."#( 5 #,5  /+/ (),(#-5 0)&(-5 1-5 INTRODUCTION  . ,'#( 5 (5 )'*, 5 1#."5 )." ,5 #,5 (5 Eggshell structure and its functional O/ ." ,)*)5 !!5 '. ,#&85 " 5 &)15 j8gi5 '! 2 properties are paramount for the incubating and 3R),,5 25) 5850)&(-5 !!-5*)#(.-5.)55,35 "."#(!5 -/ --5 ) 5 , *.#& 5 (5 #,5 ',3)-5 2*)- 5( -.5(51#."55,))#(!5*, (.5 ),5."#-5 species, similar to modern birds (the same holds B),65 gonhC85 ( 5 ) 5 ." 5 '#(5 *"3-#)&)!#&5 *,)* ,.# -5) 5(5 !!5#-5." 5 !!-" &&5* ,' #&#.365 .,/ 5.)5)3*. ,#25'#(/.C651"#& 5.,)))(.#-5(5 ),5 )(/.( 65 .)5 !- -65 )."5 , -*#,.),35 !- -5 0#,*.),5 -")1-5 - '#7/,# 5 ( -.-85 " , ), 5 (5 1. ,5 0*),85 -5 # /-#)(5 .",)/!"5 ." 5 #.5 #-5 &#% &35 .".5 ." 5 2*)- 5 ( -.5 #,-.5 ** , 5 !!-" &&5 *), -5 (5  5 +/(.# # 5 -5 ." 5 1. ,5 #(5
0#& 85 ), 5 -./# -5 1#."5 )." ,5 ,&35 #,-5 vapor conductance (GH O). GH and non-avian Maniraptoriformes are required 2 25#-5)'')(&35 and GH O can be a valuable tool for nesting ).#( 5 2* ,#' (.&&35 ),5 ') ,(5 #,5 (5 2 reptile eggs (Ar et al ., 1974), but in fossil material it *& ) "0#),5B& #.5)0 ,&))% 5/(.#&5()1C8 Keywords: Avialae, Enantiornithes, (5 5 . ,'#( 535-#'*& 5 +/.#)(-65 )'#(!5 5 0&/& 5 *,)235 ),5 -- --#(!5 ." 5 ')#-./, 5 Neuquenornis volans content in archosaurian nesting environments (5 *, (.&5 ( -.#(!5 -.,. !# -5 B 3')/,65 gomo:5 RESUMO  '#(!65hfflC85 (35#()-/,5 !!-5"0 5&, 35 been studied in respect to their GH O (Deeming, As propriedades funcionais das cascas 2 2006; Grellet-Tinner et al dos ovos juntamente com os comportamentos 865-/'#.. C65/.51),%-5 de nidificação dos pais influenciam o sucesso  &#(!51#."5 ,&35#,-5, 5 ,5& --5)'')(85 , 5 O of Neuquenornis volans da embriogênese e incubação. Assim, uma 1 5 . ,'#( 5." 5 2 das principais propriedades fisiológicas dos !!-65(5 ((.#),(#."#( 5#,651")- 5 #&#.#)(5#-5 more precise than most eggshell material since it O), )0)-65 5 )(/.â(#5  5 0*),5 ]á!/5 B 2 1-5# (.# # 535 ',3)(#5, '#(-5B"1 #.4 ,5 do enantiornitídeo Neuquenornis volans foi et al determinada e comparada com dados de outras 865hffhC85)&&)1#(!5#.651 5*, - (.55)'*,#-)(5 1#."5." 5 250&/ -5) 5)." ,5 )--#&5 ,&35#,5 aves e terópodes. O valor baixo de 4,13 mgH 2O/ O dos ovos de N. volans indica (5 ." ,)*)5 !!-65 1#."5 0&/& 5 .5 .)5 ) ,5 3R),,5)5 2 some implications for the evolution of modern um ninho exposto e com um pai incubando os birds nest structure. ovos para essa espécie, similar às aves modernas B)5 ' -')5 ï5 0á&#)5 *,5 )3*. ,#25 '#(/.C65 enquanto troodontídeos e Oviraptor apresentam MATERIALS & METHODS ninhos semi-enterrados. Portanto, é plausível que  /+/ (),(#-50)&(-5 !!-51 , 5 )/(5#(5 o ninho exposto tenha surgido pela primeira vez the Upper Cretaceous Bajo de la Carpa Formation

 (Neuquén Group; middle-Upper Santonian), look out for them (since an egg can’t be left alone Neuquén, Argentina, and are described on in an open nest due to desiccation and predators). et al "1 #.4 ,5 . (2002). All the information and The troodontid Troodon formosus is .5 (  5 ),5 )/,5 -./35 &-)5 -. '5 ,)'5 ."#-5 %()1(5 .)5 /#&5 )* (5 ( -.5 (5 -/**)- 5 .)5 et al 1),%8 present brooding behavior (Varricchio ., (5 ), ,5 .)5 ).#(5 ." 5 1. ,5 0*),5 goomC65 1"#& 5 #(5 0#,*.),5 *"#&) ,.)*-5 )."5 conductance (GH 2C5 ),5 ." 5 !!-651 5 /- 5 ." 5 ."#-5 ",. ,#-.#-5 , 5 1 &&5 -.&#-" 5 B), &&5 et al +/.#)(5 / 5 ),5 2.(.5#,-535
,5;5"(5 865 gookC85 ,)))(.#-5 (5 0#,*.),5 -")15 BgomnC65 ),51"#"5)(&35.1)5))&)!#&5*,' . ,-5 5'#2./, 5) 5)* (5( -.51#."5*,.#&5/,# 5 !!-65 , 5, +/#, 65 !!5 (-#.35(5 !!5,#/-65." 5)." ,5 but both taphonomic evidences and GH2O parameters are calculated base on them (Figure 0&/ -5#'*&# -5.".5." 5( -.-51 , 5*,.#&&35)* (5 et al et g
C85 85 0)&(-5 !!-5 1 , 5 )(-# , 5 &&#*-)#-5 (Figure 1B; Norell ., 1995; Varricchio al B*,)&. 5-*" ,)#-C5 ),5-#'*&##.35(5-5-/"5." , 5 865 goomC85
&-)65 ." #,5 !!-" &&-5 , 5 \0 ,35 0#(7 et al , 5.1)5,##5.)5 5)(-# , 65 +/.),#&5B ) and &#% ]5-.,/./,&&35 B,,#"#)5 ., 1997). These polar ( !C85!!5 (-#.351-5--/' 5 ,)'5 2.(.5 /."),-5 "3*)." -#4 5 *,.#&&35 )* (5 ( -.-5 (5 et al bird eggs, according to Paganelli . (1974). ,))#(!5 -5 -3(*)'),*"# -5 ) 5 ) &/,)-/,#65 Aiming a proper comparison, information on 1"#& 5)'*& . &35)* (5( -.-51)/&5 5, -.,#. 5 GH to Aves, also stating that incubation in Troodon 250&/ -5 ,)'5." 5)." ,5-)/, -51-5 5 .)5."#-51),%5B#!/, 5gC8 (5 0#,*.),5 , 5 #(. ,' #. 5  .1 (5 ,))#& -5(5#,-65 ),5." 35/- 5)."5- #' (.-5 et al RESULTS & DISCUSSION (half-buried eggs) and brooding (Varricchio ., 1997). Their GH 265 %()1(5 )(&35 #(5 .,)))(.#5 #!/, 5g
5-")1-5&&5." 5.5).#( 5 ),5 !!-5/(.#&5()15B '#(!65hfflC65, 5'/"5&)- ,5 ." 5  /+/ (),(#-5 0)&(-5 !!-5 1"#& 5 #!/, 5 g5 .)5#,-5( 0 ,." & --5B#!/, 5gC85)1 0 ,65." , 5 O values of N. volans eggs together -")1-5." 5 2 #-5'/"5.5&%#(!5 ),5'(35!,)/*-5#(5 .1 (65 et al 1#."5." 5, -/&.-5) 5*, 0#)/-5/."),-5)(5 )--#&5#,5 ().5.% (5#(5)/(.535,,#"#)5 . (1997), be and non-avian theropod eggs and modern bird it taphonomic nest data or the eggs’ GH 2O. The O of !!-85),5850)&(-5 !!-651 5).#( 55 2 "(! 5) 5( -.5.3* -5 ,)'5/,,)1-5.)5- '#7/,# 5 4.14 mgH 2I3R),,6550&/ 5.".5 &&51 &&51#."#(5 could also have appeared in Maniraptoriformes, ." 5&)1 ,5&/-. ,5) 5') ,(5#,5 !!-85/"55&)15 Maniraptora or even before the Coelurosauria, in GH et al 250&/ 5, *, - (.-55( -.5 (0#,)(' (.5&)15#(5 Avetheropoda (sensu Padian ., 1999). And the "/'##.35)(. (.65(5."#-50 ,35,35( -.51-5')-.5 change from the semi-buried to an exposed nest  ,.#(&35(5 2*)- 5( -.51#."55,))#(!5*, (.65 )/&5"0 5"** ( 5#(5
0 -65/.5#.]-5&-)5&#% &35 -5." 5,/& 5#(5') ,(5#,-65)." ,1#- 5." 5 ',3)5 .".5#.5"** ( 5#(5
0#& 651"#"51)/&5#(&/ 5 1)/&5 "3,. 5(5# 5B '#(!65hfflC85" 5 ." 5 )--#&5 ,&35#,-5-/"5-5." 5((.#),(#." -8 same is valid for the other enantiornithine bird, )3*. ,#25'#(/.5B#!/, 5gC8 CONCLUSION " ,)*)-5'), 5#-.(.&35, &. 5.)5#,5 O values (Figure 1B), not as high O values obtained for the -")15"#!"5 2 " 5 &)15  2 as other non-avian dinosaurs but still greater ((.#),(#."#( 5#,-5" , 5(535."5BgoogC5 ."(5 (35 %()1(5 #,65 #(#.#(!5 ." - 5 (#'&-]5 (5  '#(!5 BhfflC5 -.,)(!&35 *)#(.-5 .)1,-5 an exposed nest for these animals (agreeing !!-5 (  5 5 0 ,35 "/'#5 ( -.5 (0#,)(' (.65 -/"5 -5 /,,)1-5 ),5 ')/(-5 B '#(!65 hffl:5 1#."5 *, &#'#(,35 .*")()'#5 )- ,0.#)(-5 35 et al Grellet-Tinner 865-/'#.. C85)1 0 ,65.")- 5 885 #), & (5 ." 5 ,#5 (5 ,35 )(.#( (.&5 paleoclimate reported for the region; see Fiorelli, ." ,)*)-5 '), 5 &)- &35 --)#. 5 .)5 #,-5 &#% 5 .,)))(.#-5-")15&)15 250&/ -5.".5 &&51 &&5 hfgfC65 1"#& 5 .,)))(.#-5 (5 0#,*.),5 -")1-5 semi-buried nests (Norell et al ., 1995; Varricchio 1#."#(5." 5,(! 5) 5 2.(.5#,-5B#!/, 5gC85"#-5 et al #(#. -5 ,# ,5 ( -.-5 .".5 1)/&5 &#% &35  5 )* (5 865goomC85)5#.5#-5&#% &35.".5." 5 2*)- 5( -.5 first appeared in Avialae after all and not in ( -.-51#."55,))#(!5*, (.5.)5"."5." 5 !!-5(5 et al
0 -5 B-5 *,)*)- 5 35 ,,#"#)5 ., 1997).

 )1 0 ,65'), 5-./# -5, 5-.#&&5, +/#, 65 &#(!5 PDIAN, K.; HUTCHINSON, J.R. & HOLTZ, 1#."5 )." ,5 ,&35 #,-5 -5 1 &&5 -5 1#."5 ()(7 8865 85 gooo85 "3&)! ( .#5  ŀ(#.#)(-5 avian Maniraptoriformes. GH and nomenclature of the major taxonomic 25 #-5 5 *,)235 ),5 -- --#(!5( -.5"/'##.35(5."/-5(5. &&5/-5# 5." 5 categories of the carnivorous Dinosauria ( -.51-5 2*)- 5),5().85 (5." 5- ( 5) 5#, .5 (Dinosaur eggs: gas thickness, and functional pore area.

FIORELLI, L.E. 2010. Predation bite-marks on 5* #,)-/,#5,))3&# ),'5 ,)'5." 5** ,5 Cretaceous of Neuquén Province, Argentina. Ameghiniana 47 (3): 387–400.

GRELLET-TINNER, G.; FIORELLI, L.E. ;5 

65 885 Ļ 5 1. ,5 0*),5 conductance of Cretaceous neosauropod eggs from Sanagasta, La Rioja, Argentina, 1#."5 *& )#)&)!#&5 #'*&#.#)(-5 ),5 neosauropod eggs and nesting environments. Palaios (submitted).

NORELL, M.A.; CLARK, J.M; CHIAPPE, L.M. & DASHZEVEG, D. 1995. A nesting dinosaur. Nature 378: 774–776.

 Figure 1. A. Summary of all parameters, units, equations, and results for the eggs of Neuquenornis volans 8 B. G QK values

(in mg Q LR:7\GQ``_#QG :1JVR#`Q`# N. volans #:CQJ$%1RV# .Q%V#Q`#]`V01Q%%#1Q`@%8