Cracking a developmental constraint: Egg size and bird evolution

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© The Authors, 2010. .loumal compilation © Australian Museum, Sydney. 20 10Records of the Australian Museum (2010) Vol. 62: 207-216. ISSN ()067-1975dui: IO.3853/J.OO67-1975,62.2010.1547

Cracking a Developmental Co nstraint:

Egg Size and Bird Evolution

G A R E T H J . D Y K E , * ' A N D G A R Y W . K A I S E R -

' School of Biology and Environmental Science, University College Dublin Belfield Dublin 4. Ireland

[email protected]

- Royal British Columbia Museum. Victoria. B.C. Canada V8W 9W2

[email protected]

ABSTRACT It has been suggested that relative egg size in living birds is strongly correlated with thedevelopm ental mode of the young ; altricial (helpless) or preco cial (independ ent). Using a data set

of extant taxa we show that altricial birds lay relatively larger eggs than their precocial counterparts butthat this may be due to the small size of most altricial species, Smaller birds tend to lay relatively smalleggs compared to large species. Nonetheless, a predictive egg mass-body mass relationship extends intothe avian fossil record. Such a relationship is important to our un derstanding of avian evolution b ecauserelative egg size (and thus available developmen tal m ode) was constrained in many early b irds—ov iductdiameter was limited by the presetice of pubic fusion. Therefore we document the evolution of aviandevelopmental strategies using morphology-based phylogenies for Meso/oic and extant avians andcorroborate correlations between developmental strategies, egg weight and female body mass. Thesequential loss of precocial features in hatchlings chaiacterises the evolution of birds while altriciality isderived within Neoaves. A set of precocial strategies is seen in earlier lineages, including basal Neornithes(modern birds) and are implied in their Mesozoic cou nterparts—skeletal constraints oti egg size, presentin many Jurassic and Early Cretaceous birds {Aixhaeoptei-y.x Confuciusornis. Enantiornithes) were lostin later diverging lineages. Attributes of precociality were already present in a number of lineages ofnon-avian maniraptoran theropods. We propose that the evolution of unrestricted egg size may have

precipitated subsequent d evelopment of the diverse reproductive strategies seen in living birds.

DYKE, GARETH 1 . & GARY W. KAISER. 2010. Cracking a developmental constraint: egg size and bird evolution. InProceedings of the V II Intern ational M eeting of the Society of Avian Paleontology an d Evolution ed. W.E. Boles andT.H. W orthy. Records of the Australian M useum 62( 1 ): 207-216.

Birds are unique amongst living vertebrates in the sheerrange of developmental strategies and forms of parentalcare they employ (O'Co nnor, 1994). This variation, spreadacross a spectrum that ranges from completely helplesshatchlings ( altriciur ) to those that are independent, evenimmediately flighted ( precocial ), has always proveddifficult to classify and un derstand in a phy logenetic con texteven when dealing with modern birds (living Neornithes)(Nice, 1962; O'Connor. 1994; Starck & Ricklefs. 1998).

This is because avian dev elopmental strategies are not alwaysconsistent within families and are a mixture of beh aviouraland physiological phenomena (Starck & Ricklefs, 1998).Consequ ently there has been little evidence of any directionaltrend when characteristics of this altricial-precocial (A-P)specttiim (effectively degree of neonate dependence ) havebeen mapped o nto the various phylogen ies proposed for birds(Aves) during the 20th century (Cracraft, 1986; Starck &Ricklefs. 1998: Sibley &Ahlquist. 1990; Deeming, 2007a).



208 Records of the Australian Museum (2010) Vol, 62

modern

birds

ionfuciusornithines enantiornithines ornithurines

non-avian

theropods

Figure 1. Cartoon to show a simplifiedconsensus phylogeny of Mesozoic birds.

We also [lote that the actual characteristics that determine

altriciality and preco ciality are not absolute: even simplecharacteristics are subject to observational judgment and arenot exactly the same in one lineage of birds as they are inanother (Starck & Ricklefs. 1998).

Nevertheless, in spite of a lack of clear phylogeneticassoc iation, it has long been suggested that preco cialityis the primitive condition within Aves {Elzanowski. 98 ;Starck & Ricklefs. 1998: Zhou & Zhang. 2004). Well-developed feathers in a late-stage embryo of a Cretaceouse n a n t i o r n i t h i n e e v en s u g g e s t s u p e r - p r e c o c i a l i t y(immediate flight) at hatching in at least one p re-neomithinefossil bird (Zhou & Zhang. 2004), Taken in combinationwith inferred osteological growth rates for other fossil

birds (Chinsamy, 2002: de Ricqlès et ai 2003; Cambra-M oo et al. 2006). and the egg and nest morphologiesof some non-avian theropods, evidence clearly points

onfuciusotrtis

sanctus

ilium

rib

ischium

g str li

pubis athartes aura

Turkey Vulture)

Varricchio et al. 1997). Other fossil evidence suggeststhat this developmental mode is likely primitive acrossall archosaurs (Horner, 2000; Unwin, 2006). However, nocomparable trace of altriciality has yet been found in thefossil record — evide nce for the evolu tion of obligateparental care in birds, beyond brooding or incubation ofeggs (i.e. feeding of helpless hatchling s), must therefore beindirect. We have no way of assessing the contribution ofcontact incubation lo this complex evolutionary scenario.even less so in fossils where the data simply cannot exist.

Egg mass is correlated with body mass (R ahn c/íí/., 1975)and incubation time increa.ses with egg mass (Rahn & Ar,1974). In addition ornithologists have long suggested thatthere is a link between egg muss and developmental mode(Heinroth. 1922; Amado n, 1943; Tullberg el al.. 2002).Although Rahn & Ar (1974) were unable to detect such a

relationship, it is supported by other evidence (Nice, 1962;Starck & R icklefs. 1998; Deeming, 20 07ab). If signiHcant.a predictive relationship would be hugely important tointerpreting the avian fossil record because of anatomicalcons traints on egg size (Fig. I B) , exception al flightlessliving birds like the kiwi. Aptéryx notwithstanding. Herewe restrict our d iscussion to flighted birds w here egg size isalso constrained by aerodynamic considerations.

In this paper we reconstruct the evolution of the A-Pspectrum in l iving neornithine birds by mapping thedistribution of neonate dependence (Nice, 1962; O'Connor,1994: Starck & Ricklefs, 1998: Deeming, 2007a) onto arecenf morphology-based phylogeny (Livezey & Zusi, 2006,

2007) (Fig. 2). Trends were cross-checked against anotherrecent large-scale genomic study that reconstructed thephylogenetic history of birds (Hackett etal. 2008 ). We then



Semi precocialand

Semi althcial

Dyke Kaiser: Developmental constraint in bird evolution 209

Galloanserinae

other theropods

Tinamiformes

Apterygiformes

Dinornithiformes

Cauariiformes

Struthioniformes

Aepyornith if ormes

Anseriformes \

Galiiformes J

Gaviiformes

Podicipediformes

Sphenlsciformes

Proceliariiformes

Balaenicipitiformes

Peiecaniformes

Ardeiformes

Ciconiiformes

Gruiformes

Turniciformes

RalliformesCharadriiformes

Strigiformes

Fa i coniformes

Opisthocomiformes

Cuculiformes

Psittaciformes

Columbiformes

Caprimuigiformes

ApodifcrmesConiformes

Trogoniformes

Coraciiformes

Piciformes

Passeriformes

Figure 2. Phylogenetic hypothesis for relationships amongst modem birds (Neornithes) showing altricialand precocial modes of development (Livezey Zusi. 2006. 2007).

betvi'een egg mass and female body mass (Appendix) asproxies for avian parental investment (Deeming, 2()07ab).Finally, using femur length to approximate body mass(Hone et al 2008), we added data for specimens of theabundant and early diverging Cretaceous bird onfuciusornis(Appendix) to extend this predictive lelationship back intothe avian fossil reeord und to augment our understanding oftbe theropod origin of birds.

Materials and methods

Our analyses use egg mass and female body mass datafor species-level taxa culled from the primary literatureand from Dunning (1993: see also Appendix), correlatedwith the morp hology-bas ed phylogeny of Livezey Zusi(2006, 2007). Data coverage across the major neoavianclades is good, but for this analysis we only have a small(N=2) sample for paleognaths. For the well-representedfossil bird Confuciusornis egg volutne was calculated fromthe measured width of the pelvic eanal and extrapolatedproportions of modern bird eggs and egg mass from astandard shape/volume equation (Hoyt. 1979). We know(Kaiser. 2007) that the eggs of these Cretaceous birds weremore-or-less round, as are those of described enantiornithines(Zhou Zha ng, 2004 ). Avian femur lengths were extracted

RBCM ornithology collection while fossil body massestimates w ere calculated using a standard allometric method(Hone et ai 2008). onfuciitsornis specimen measurementsare from Kaiser (2007 ) and Hone et al ( 2008), cross-checkedwith Chiappe et al (1999). Because this paper discussesinitial qualitative comparisons, at a very broad phylogeneticscale, a comparative analysis is not presented. This representsan area for future work.

Results and discussion

Extant birds living Neornithes)

In contrast to earlier studies of avian developmental evolutionthat require multiple origins of altriciality in birds (StarckRicklefs. 1998; Deeming, 2(X)7ab), simple qualitative mappingof neonate dependence onto the phylogenetic hyptuhesls ofLivezey Zusi (2(X)7) is approp riate because this topologyimplies a sequential loss of precocial features towards thecrown of Neoaves (Fig. 2). Earlier diverging lineages ofNeornithes (Paleognathae. Galloanserinae, Gaviiformes,and Podicipediformes) are characterized by a high degree ofprecociality (del Hoyo et ai I992-2(K)2; Starck Ricklefs,

1998). The young of the Pelecaniformes, a later divergingmem ber of the Natatores (Livezey Zusi, 2007), are thefirst to exhibit altriciality. The deg ree of altriciality is highly



210 Records of the Australian Museum (2010) Vol. 62

neonate stages, as in the Sphenisciformes (penguins) atidProcelhiriiformes (petrels). L ater stages are typically active andmobile (Dunn. 1975; Simpson. 1976: W arham, 1990: Gaston.2(X)4). Later diverging gro ups, such as those clustered in theTerrestrornithes also exhibit varying degrees of altriciàlity. Incontrast, it does appear to be the case that completely helplesshatchlings—bom naked, blind and immobile—characterizethe ku ge monophyletic cluster of small, forest-dwelling birdsat the crown of Neoaves. Dendromithes (Fig. 2). althoughmore data combined with a phyiogenetic cotnparative analysiswill be require to verify this correlation. The most significantincompatibility between our qualitative mapping of neonatedependence (qualitative data from Kaiser. 2007) onto themorphology-based phylogeny of Livezey & Zusi (2007) orthe phylogenomic result of Hackett et ÍÍ/ . (2008). relates tothe crownward movement of falconids. which places a groupwith sem i-altricial developmental strategies (sensu Starck& Ricklefs. 1998) as the closest relative to two other clades(Passeriformes and Psittaciformes) that have fully altricialyoung. This correlation is intuitive.

The evolutionary transition from precociality to altriciality.correlated with changes in relative egg-size, is not the onlyaspect of avian reproduction that can be accommodated byphylogeny (Livezey & Zusi. 2006. 2007): broad qualitativetrends in duration of incubation and enhanced nestling-care,increasingly sophisticated nest-building and decreases inclutch size are also apparent (Fig. 2). Some of these may berelated to an overall decrease in adult size associated with ashift from relatively simple, open environments to the complexthree-dimensional structure of tree canopies. As expectedfrom their less-developed hatchlings. the eggs of altricial birdsrequire shorter incubation periods (on average 20.8 days, n =18 non-passerine birds). All Passeriformes produce altricialyoung and some have extremely short incubation periods,

between 10 and 16 days (Skutch. 1945) although this mayreflect their small btxJy and eggs (Kaiser. 2007). Birds thatproduce precocial young incubate their eggs for somewhatlonger periods (23.2 days, n 5). Sem i-precocial and semi-altricial young appear to be incubated for even longer periods:24.4 days {n 23) and 32.3 days (n = 42) days re.spectively (delHoyo et ai. 1992 -2002). Interestingly. Grellet-Tinner et ai(2006) díKumented a clear egg-size increase within oviratoridnon-avian theropods that they suggested could have occurredto accomm odate additional nutrients within the egg

Small adult body size and intense parental care in altricialtaxa may combine to produce shorter periods of nestlingdependence (28.5 days) than in semi-precocial (40.3 days)

or semi-altricial birds (42.2 days) although this is likelyphyiogenetically constrained (Deeming etal.. 2006). At a verybroad level, early diverging precocial b irds, and later divergingsemi-precocious and semi-altricial taxa, use unsophisticatednests that simply keep their eggs from rolling away. These nests tend to be limited to scrapes, cushions of feathersand plant stems, or simple platforms of twigs placed out inthe open. At best, they are camouflaged or hidden by adjacentvegetation. A wide range of birds h ides its nesLs in tree cavities,underground burrows, or rock crevices. Some tree cavitiesboast a thick mattress of feathers but most are bare imd manyburrow nesters, especially seabirds. place their eggs on theground, with only a thin pad of vegetation for protection

(Warham. 1990: Gaston. 2004). Il is only among tbe mostcrownward and wholly altricial taxa that we find elaboratelyconstructed woven and moulded nests, an elaboration of the

et cd. (2006). Indeed, this trend, in particular, may proverelated again to b(xly size: m ore complex nests may representa response to the thermal issues related to small parental size.This represents another area for future work.

nterpreting the avian fossil record

Of clear significance for interpreting the fossil record, ourdata dem onstrate that within the neoavian clade, fullyaltricial birds (sensu Nice, 1962: Starck & Ricklefs,1998; Deeming, 2007a) produce significantly larger eggs(cotnpared to female body mass) (Fig. 3A.B), than thoseof precocial and super precocial taxa. However suchresults likely reflect two distinct evolutionary trends. Thefirst reflects the preponderance of precocial neonates amongbasal clades and altricial neonates among crown clades.The second reflects trends in body size and a bias in thedistribution of body masses among living birds. Membersof basal clades tend to be larger than members of crownclades. Both with in clades and across class Aves, largerbirds have lower egg to body ratios. A sub-sample of birdsof comparab le w eights shows little difference in relative egg

size between grou ps with altricial and precocial s trategies. Itis more supporting of the conclusions of Faaborg ( 1988) orTulberg et ai (2002) that larger eggs are necessary for thepre-hatching development of precocial young.

Perhaps of greater evolutionary significance is thetendency of birds {within the subset of birds of comparableweight) that use either semi-altricial or semi-precocialstrategies to have relatively large eggs. Some of thesegroups [e.g.. Procellariiformes. Alcidae (Charadriifomies),Phaethontidae (Pelecaniformes)] combine relatively largeeggs with minimal clutch sizes {I or 2).

Combined with the concentration of altricial strategiesin smaller birds, our data suggest the possibility of a lower

limit on absolute egg size that may preclude precocialityin most birds. Final adult body size is also much closer tothe mass of the hatchling in small altricial birds than it is intheir precocial counterparts {Deeming & Birchard. 20{)7).suggesting that time-to-indepe ndence is also a limiting factoron avian relative egg mass.

Using femur length as a proxy for body mass thepredictive relationship between egg mass, body massand reproductive strategy (Fig. 3) can be extended intothe fossil record (Fig. 4). Although this proxy approachdoes not allow the subdivisions of the A-P spectrum to bedistinguished {Appendix), it can be used to extrapolate eggmass relative to body mass across Aves. Corroborated by its

pelvic anatomy (Fig. IB), the relative egg size of the basalEarly Cretaceous fossil bird Confuciusornis, for example.was small in comparison to that of most living birds (Fig.4) . Constrained by their anatomy, relatively small eggsmust characterize inost of the early diverging avian lineages(Fig. 1). In Confuciusornis s case, in combination with itsinferred growth rate (de Ricqlès et ai. 2003: Cambra-Mooet ai, 2(X)6) and phylogen etic position (Chiap pe et ai. 1999:Zhou & Zhang. 2004: Gao et ai. 2008) this bird was almostcertainly precocial {Fig. I ). Recent studies also determinedthe growth rate of Confuciusornis to have been slower thanthat of many extant birds {Cambra-Moo et cd. 2006): tbiswould also be reflected in extended time-to-independencefor its nestlings as is seen in modern precocial birds.Confuciusornis appears to have laid an egg comparable insize to that of the extant Buttonquail (genus Tuniix) even



Dyke & Kaiser: Developmental constraint in bird evolution 21

A 4 0

log body m ssFigure 3. Rela t ionsh ip between egg weight and female body weight in extant birds. (A) Grap h to discrim inate betwe en al tr ieial [n = 96 :l i l led circ les: r- = 0.906 , p < 0 . 0 0 1 : egg mass = -0 .65939 4-H 0 .788 9097 .bodym ass] , and precoc ia l [n = 113; open c i rc les ] ( inc lud ingsuper p recoc ia l | n = 29 ; g rey t r i ang les l : r -= 0 .801 . / ?< 0 .001 : egg mass =- 0 .16 461 5- ( -0 .645 I í í72 .bodymass) t axa . Both of these resu l t shave signil icantly higher r- values than those found for 100 bootstrap replicates that paired body and egg mass at random. (B) Bar chartshowing that the three broad developmental modes seen in Neornithes arc characterized by signif icantly different egg/female body massrelat ionships. Discrimination among al l three groups is borne out by averaged data (Kruskal-Wall is test , p < 0 .005) . Abbrev ia t ions : A,al tr ieial ; P. Precocial ; SP, super precocial .

However, the hatchlings of Confuciusomis appear to havetaken about Hve times as long to reach their adult size basedon an estimate for onfusiusornis of 20 weeks (Cambra-Mooet al.. 2006) cotnpared to three weeks from hatching lo fullitidependence in 7"/ÍÍ/Í/.V {Debus, 1996).

Origin of avian neonate adaptations

and survivorship

Even it the absence of direct fossil evid ence, small relative

egg size in basal birds (including Confuciusomis is expected:the eggs of comparably-sized dinosaurs close to the theropod-bird transition v^erealso small (Buffetaut etal.. 2005). Indeed,phylogenetic studies predict that in addition to the acquisitionand refinement of feathers, retenlion of a basal small bodysize was paramount at the "theropod-bird evolutionarytransition" {Turner et al., 2007) (Fig. 1). Of course theevolution of feathers would also allow for better heatretention at relatively smaller body sizes while the neonatesof many non-avian theropod dinosaurs are known to havebeen extremely "b irdlike"— evidence for precociality in babytheropod dinosaurs comes from osteology and even posture(Xu & Norell, 2004). In addition, just like modern birds,

maniraptoran theropods are known to have laid eggs froma single functional oviduct (V anicchio et ai, 1997, Grellet-Tinner Makov icky, 2(X)6; Gre llet-Tinner et al. 2006) and in

2000). As far as is known simple nesting structures alsocharacterize both non-avian therop ods and basal birds (Grellet-Tinner et al., 2006); there are no known Mesozoic examplesof elaborately constructed nest structures comparable to thewoven nests of mtKlern Passertormes (Fig. 3).

MitToring our " egg size-neonate depende nce" hypothesisat the reproductive level, the production of diminutive eggsby early birds is anatomically consistent with the pubicfusion (sytnphysis) seen in early diverging Jurassic andCretaceous taxa ( i e Aivhaeopteryx, C onfttciusornis, known

enantiornithines) and recorded as characters in phylogenetichypothe.ses (e.g.. Gao et ai. 2008): the presence of thisrigid pubic structute would have limited the maximumdiameter of the egg passing through the t)viduct. Somenoti-avian dinosaurs appear to have attempted to overcomethe effects of this constraint by producing elongated eggsthat could contain more nutrient than a spherical egg ofthe same diameter (Grellet-Tinner et al., 2006). Modernavian embryos develop their lightv^eight skeletons fromcalcium extracted from the eggshell. The increased surfaceto volume ratio of elongated dinosaur eggs might have mademore calcium available to an embryo developing a longbony tail and the relatively heavy skeleton of a terrestrial

animal. Because there is a relationship between egg size andneonate dependence, loss of this structural constraint in theMid- to Late Cretaceous enabled the production of larger



2 12 R ec or ds of th e A us tra lia n M us eu m (2 01 0) V ol. 6 2

3,0-

co

^ 2.0^

¡15^

•2 1.0^

-0.5 0.0 0.5 1 0 1 5 2.0 2.5 3.0 3.5 4.0

log egg mass

Figure 4. Relationship between femur length (appro ximates body mass) and egg mass in extant and fossil birds (n = 117; r- = 0.758, p

< 0.001). These data show that both Confuciu.wrnis (carloon. open circ-le) and the similarly-sized Buttonqua il {Titrnix (grey U"iangle) layrelatively small eggs compared to their body size (Appendix).

subsequent proliferation of avian reproductive strategies.Reduction of constraints on egg size and thus neonatedependence in ornithurine and basal neornithine birdsalso provides a possible explanation for the "selectivesurvivorship" of modern birds in the aftermath of the end-Cretaceous extinction event.

ACK N O WL E D G ME N TS . W e thank Michael McN all for collectionsaccess at the RBCM (Victoria BC. Canada) and for kindly sharinghis unpublished measurem ents. G erald G rellet-Tinner, AlistairMcG owan, Julia S igwart. W ill S tein and an anonymous reviewers

provided very helpful comments on earlier drafts of t is

manuscript.W e thank W alter Boles and Trevor W orthy for their editorial efforts.

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Appendix

Data used in the paper. Confuciusornis egg measurement from Kaiser (2007; Kenya Museum number B 072). Femur lengths{N=15) from Hone et al. (2008), with mean length value verified by Chiappe et al. (1999 ). Abbreviations for developmentcategories are (/, altricial:/?, precocial; sa, semi-altricial; sp . .semi-precocial. The Ía.st column shows mean femur length andsample size.

species

Accipiter badiusAccipiter brevipesAccipiter cooperiiAccipiter gentilisAccipiter striatusAlcedo atthisAlectoris barbaraAtecttn'is ch ukarAlectoris graecaAlectoris rufaAlectura lathamiAnas acutaAnas americana

Anas clypeataAnas discorsAnas platyrhynchos

developmencategory

aaaaaapPPPspPP pP

t eggmass (g)

21.321.743.059.018.54,3

21.922.021,821.6

192.041.652,9

37.828,152,2

femalemass (g)

19625 456 697 317427

37 645353 0453

2210755672

65 342 2

1301

log female log eggmass

2.29232,40482,75282,98802,24051,4314 (2.57522,65562.72432.65563.34442.87792.8274

2,81492,62533.1143

mass

,329 t,3357,6335,7709,2672

),6340,3407.3424,3376,3341

Î.2833,6191.7237

.5775

.4487

.7177

egg / femalemass

10.98.57.66.1

10.615.95.84.94.14.88.75.57.9

5.86,74,0

mm (n)mean femur

64 .9 (15)82,8(11)48.4 (24)15.3 (3)

61 .0 (1 )56.8(1)55 .4 (1 )89 .5 (1 )46.6 (2)43 .0 (8)41 .4 (5)32,9 (3)48,1 (7)



214 Records of the Australian Museum 2010) Vol. 62

species

Anas streperaAnhinga anhingaAnser atbifronsAphetocoma catifomicaAptietocoma coerulescensAphelocoma insularis

Aphelocoma uttraniarinaAptéryx au stralisAptéryx oweniiApus affinisApus apusApus cafferApus melbaApus palUdusAramus guaranáArdea albaArdea cinéreaArdea herodiasArdea purpureaArdeotis arabsArdeotis koriBalaeniceps rex

Bombycilla cedrorumBombycilld garrulusBotaurus tentiginosusBotaurus stettarisBurhinus oedicnemusCacatúa sanguinedCacatúa tetutirostrisCatyptortiynchus iianksiiCalyptortiynchus latirostrisCaprimulgus aegyptiusCaprimutgus carotinensisCaprimutgus europaeusCaprimutgus ridgwayiCaprimutgus rußcottisCaprimutgus vociferusCasuarius casuarius

Cathartes auraCentropus senegatensisChlamydotis utidulataChlidcmias hybridaChlidoniiis leucopteraChlidonias nigerChlomstilbtm mettisugusCiconia ciconiaCiconia nigraCoccyzus americanusCoecyzus eiythropalmusCoceyzus minorCotumba liviaCoradas benghatensisCoradas garrutusCuculus canorus

Cucutus saturatusCursorius cursorCypsetoides niger

development egti

categorj

Psa

Paaa

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saPpsa

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Dendragapus obscurus montana pDiomedea chtororhynchosDiomedea epomophoraDiomedea exutansDiomedea imnuitabdisDiomedea melanophrisDiomedea nigripesDromaeus novaehottandiaeEolophus roseicapittusFalco me xicanusFalco peregrinusFalco rusticolisFalco sparverius

Erancolinus africanusErancolinus iticatcaratusFrancolinus francolinusFregata nmgnißcens

spspspspspsppaaaaa

PPPa

mass (gj

43.136 3

128 5

6.25.8

7.1

8.2430.0275.5

2 4

3 6

2 8

6

3 9

57 4

39 4

6 3

5 7

5 8

1 7 5

151 1

159 5

3.23.8

35.142.042.823.120.333.232.88.4

17.38,7

4.39.27.0

584.0

82.111.752.416.311.011.00.4

105.983.9

9 46.3

9.014.614.615.4

3 5

2.113.75.3

28.8202,9452.5445.0279.0258.0298.0550.0

13.037 6

46 4

62

13 8

19 5

23.324.388.2

l cinale

mass (g)

80813381809

8675

111

11329551200

25

38

22

18

42

111

81 2

15472110

83 0450059005130

335448 286 745 955 045 572 067 5

7710867486957

29000

20331561450

875463

333503000

635669

340171142113

77138

351271243480406950275032063069

4308031 18 1

12 1

1748

12

36 238142 4

1344

log female

mass

2.9074

3.1263

3.2574

1.93371.8749

2.0461

2.05193.4706

3.0792

1.39791.5752

1.34441.25291.6222

3.0453

2.90963.1893

3.3243

2.9191

3.6532

3.77093.7101

1.51981.7340

2.6830

2.93802.6618

2.7404

2.65802.8573

2.8293

1.88822.0330

1.8261

1.68121.83571.75204.4624

3.30812.1931

3.16141.9370

1.7324

1.79870.4150

3.52503.4771

L79661.7443

1.83882.5315

2.2330

2.15232.0531

1.88652.1399

1.5490

3.1041

3.38633.9053

3.84203.43933.5060

3.4870

4.63432.4928

2.90363.0795

3.24252.0792

2.55812.58092.6274

3.1282

log egg

mass

.6345

.55992.10890.7924

0.7642

0.8507

0.91492.6335

2.4401

0.38250.5539

0.44360.7955

0.5904

1.7589.5956.7800.7053

1.7055

2.0314

2.17932.2028

0.50510.5798

.5452

.62321.6310.3644.3064.5209.5163

0.9267

.23760.9397

0.6311

0.9651

0.84812.7664

1.91431.0700

1.71921.2122

.0414

.0414-0.39792.0248

.92360.973]0.7993

0.9518.1644.1643

1.18720.5434

0.3313.13790.7243

.45942.30732.6556

2.64842.4456

2.4116

2.4742

2.7404.1153.5752.6665.7923.1399

.2897.3682

.3861

.9453

egg / female

mass

5.3

2.77.17.27.7

6.4

7.314.623.09.79.5

12.634.99.3

5.24.93.92.46.12.42.63.1

9.77.0

7.34.89.34.24.54.64.9

10.916.013.08.9

13.512.52.0

4.07.5

3.68.1

20.417.515.43.22.8

¡5 011.413.04.38.5

10.83.1

2.810.015.02.38.35.6

6.410.18.0

9.7

1.34.24.73.9

3.511.5

5.46.15.7

6.6

mm (n)

mean lemur

44.1 (4)

53.8 (6)

70 .9 1 )

90.3 (5)76.3 (2)15.4 1)17.5 3)

76.5 (2)

102.8 3)99.4 16)87.3 (3)

145.0 1)127.0 1)

19.1 (2)22.3 1)

94.6 (4)

23.4 2)21.5 1)

21.0 2)232.0 1 )

71.7 12)

65.5 (2)

94.0 1)85.0 (3)

27 9 (2)

26.4 1)

39.0 (4)

26.8 1)28.9 (2)

68.2 1)

103.0 4)72.7 19)84.0 1 )77.6 18)

227.9 11)

73.3 (9)73 .0 10)88.1 (9)36 .6 15)



Dyk e Kaiser: Develo pmen tal constraint in bird evolution 215

dcvclnp nient egg female log female

category mass (g) mass (g) masslog egg egg / female mm (n)

mass mass ^/< meiin lemur

Gavia ackimsiiGavia immerGavia pacifica arcticalGavia stellataGeococcyx califomianusGlareola nonlmanni

Gtareola pratincolaGlaucis hirsutaGrus americanaGrus canadenis canadensisGrus canadenis tábidaGrus grusGrus ¡eucogeranusGyps ful vusHaematopus bachmaniHaemalopus ostralegusHaematopus pallicitusHalcyon smynwnsisHeteroscelus incanusHinuintopiís hinmntopusHimantopus mcxiccmusJücana spino saJynx torquilluLeipoa oceltcitaLophortyx californicusLophotis ruficristaMeleagris gaUopcivoMenura novaehollandiaeMerops cipiasterMerops orientalisMerops superciliosusNumida meleagrisOceanites ocecinitesOpisihocomus hoazjnOrtalis vetulaOtis tardaOtis tetrcixOtus bruceiOtus flammeohisOtus scopsPachyptila desolataPachyptila vitrataPanilion haUaetusParus caerParus caeruleusParus cristatusParus cycinusParus lugubrisParus majorParus montanusPa tser domesticusPasser hispanolensisPasser moahiticusPasser mcmtcmusPasser simplex

Pedionomus torquatusPelecanoides urinatrixPelecanus eiythrorhynchusFelecanus occidemalisFelecanus rufescensPhaeíhon leturusPhaetlion aethereusFhciethon rubricauciaFhalacrocora.\ aristotelisPhalacrocorax atricepsPhalacrocoriLX auritusPhcúacrocoríLX carboPhalacrocorax olivaceusFhalacrocorax pelagicusFhalacrocorax penicillatusFhalacrocorax pygmaeus

Fhalacrocorax uriteFhalaropus fulicariusFlwlaropus lobatus (Alaska)

pp

ppa

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2 0 2 . 3

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3 . 2 0 3 6

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3 . 1 8 7 5

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2 16 R ec or ds of th e A us tra lia n Mu se nm 2 01 0) V ol. 6 2

species

Phataropus tricolorPluiromaihus mocinnoPhoenicopterus ruherPicoides athotarvatusPicoides árcticaPicoides arizonae

Picoides horealisPicoides dorsalisPicoides nuttatliiPicoides pubescensPicoides scalarisPicoides vltlosusPlegades falcinellusPluvialis apricariaPluvialis dominicaPluvialis squatarolaPodceps nigricollisPodiceps auritusPodiceps grisegenaPodiceps podicepsPsophia crepitansPsophia leucoptera

Pteroctes alchataPterocles coronatusPterocles exustusPterocles U chtensteiniPíemeles orientalisPterocles .\enegallusPujßnus assimitisPujfinus gravisPufßnus ilherminieriPuffinus tuivitatusPujßmis puffinusPujßnus tenuirostrisRliea americanaRhyncliotus rufescensRhynochetos juhatusRis.sa hreviro.stris

Rissa tridact\ laRostratiita henghalensisRynchops nigerScopus umhrettaSpheniscus demersusSpheniscus humholdtiSpheniscus magellanicusStercorarius longicaudusStercorarius parasiticusStercorarius pomarhiusStercorarius skuaStrix alucoStrix nebulosaStrix occidentalisStrix uralensisStrix varia

Struthio cimielusSula abhottiSuia bassanaSula capensisSula dactylatraSula ¡eucogasterSula nehouxiiSula serratorSula sulaSula variegataTrogon etegansTurnix sylvaticaTyto albaUpupa epopsUria aalgeUria lomvia

Zenaida asiáticaZenaida macroura

development eggcategorj

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spPP

sp

sp

spspspa

sp

spsp

spsp

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PsasasasasasasaasaaPaas

sp

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mass g)

9.017.0

142.74.44.83. 9

4.25.12.92.12.9A.A

38.535 4

27.035.222,821.038.321.611.683 2

21.915.912.415.721.117.632.0

102.035.063.058.082.0

609.338.067.549.4

55.412.026.931.0

103.0109.0120.044.351.668.091.738.552.649.037.345.5

1480.0112.0105.0105.078.054.061.094.058.076.0

8.23 4

26.64 5

109.01 6

1.16 5

lemalemass g)

6820 6

2530597144

486738293076

60 521 4154

21 431 9392

1052358

12501256

22 530 019224838 325 522287 016332445 053 0

230009 2 8

9 0 0

367

388121

25442 3

296042004900

30749 98296 0 4

5 24

12676 63863

873

63000150030902670190213821840235010301410

74405761

100193 2

153116

log female 1mass

1.83312.31393.40311.7723 1.8500 1.6444

1.6767 1.8228 1.5832 1.4564 1.4814 1.8791 2.78182.33042.18752.33042.50312.59273.02222.55393.09693.0990

2.35222.47712.28222.39452.58322.40652.34642.93952.21222.51052.65322.72434.36172.96732.95422.5647

2.58832.08282.40482.62583.4713 :3.62323.6902 :2.48742.69812.91862.78102.71933.10282.82152.93602.9408

4.7993 :3.1761 :3.4900 :3.4265 :3.27913.14053.26483.37113.01283.1492

mass

3.9542.2304

M 544 .6435 .6812 .5868

.6182 .7O76 .4683}.3222 .4624}.6435.5858.5489.4314.5465.3579.3222.5826.3336.8612.9201

.3399

.2026

.0919

.1947

.3245

.2460

.5051Î.0086.5441.7993.7634.9138

Î.7848.5798.8293.6937

.7435

.0777

.4298

.4914Î.0I28Î.0374..0792.6467.7130.8325.9626.5853.7211.6899.5717.6580

Î.17O3..0492Î.0212..0212.8921.7324.7853.9731.7634.8808

1.8681 0.91641.5966 0.53611.7551 .42491.7882 0.65323.0004 :2.9694 :

2.1847

..0374

..0253

.88652.0626 0.8129

egg / femalem a s s •

13.28.35.67.46.88.8

8.77.77.77.39.65.86.4

16.517.516.47.25.43.66.05.86.6

9.75.36.56.35.56.9

14.411.721.519.412.915.52.64.17.5

13.5

14.39 .9

10.67.33.52.62.4

14.410.38.2

15.27.34.27.44 .35.2

2.37.53.43.94. 13.93.34.05.65.4

11.28.7

46.77.3

10.911.4

5.05.6

mm n)mean femur

21.9 1)

86.6 8)32.5 2)24.4 11)

22.6 11)

16.7 9)

24.3 10)

35.7 2)33.0 I )37.4 3)31.2 4)32.7 6)46.9 18)

15.7 1)

47 .2 1 )

23.7 1)

31.0 1)3 6 . 9 4 )

180.4 11)

71.1 4)

37.3 9)

34.8 2)4 6 . 8 1 )

74.0 2)79.0 3)76.3 2)36.2 5)38.4 10)45.8 1 )

60.8 4)88.9 11)67.9 10)

74.6 15}

289.2 15)

6 1 . 2 2 )

47.0 2)54.9 1)

58.1 26)22.4 1)48.6 6)47.5 5)

27.3 4)



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Cracking a developmental constraint: Egg size and bird evolution