Paleogene equatorial penguins challenge the
proposed relationship between biogeography,
diversity, and Cenozoic climate change
Julia A. Clarkea,b,c,d, Daniel T. Ksepkac, Marcelo Stucchie, Mario Urbinaf, Norberto Gianninig,h, Sara Bertellii,g,
Yanina Narváezj, and Clint A. Boyda
aDepartment of Marine, Earth, and Atmospheric Sciences, North Carolina State University, Campus Box 8208, Raleigh, NC 27695; bDepartment
of Paleontology, North Carolina Museum of Natural Sciences, 11 West Jones Street, Raleigh, NC 27601-1029; Divisions of cPaleontology and
gVertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024; eAsociación para la
Investigación y Conservación de la Biodiversidad, Los Agrólogos 220, Lima 12, Perú; fDepartment of Vertebrate Paleontology, Museo
de Historia Natural, Universidad Nacional Mayor de San Marcos, Avenida Arenales 1256, Lima 14, Perú; hProgram de Investigaciones
de Biodiversidad Argentina (Consejo Nacional de Investigaciones Cientı́ficas y Técnicas), Facultad de Ciencias Naturales, Instituto
Miguel Lillo de la Universidad Nacional de Tucumán, Miguel Lillo 205, CP 4000, Tucumán, Argentina; iThe Dinosaur Institute,
Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007; and jDepartment
of Geology, Centro de Investigación Cientı́fica y de Educación Superior de Ensenada, Kilometer 107
Carretera Tijuana–Ensenada, 22860 Ensenada, Baja California, México
Aves 兩 evolution 兩 Peru 兩 fossil 兩 Bergmann’s rule
C
limate has been hypothesized to play a key role in evolutionary patterns of both living (1–5) and extinct penguins
(4 –9). Whereas the earliest penguins appear ⬎60 Ma (10),
extant lineages were recently proposed to originate in association with abrupt latest Eocene–Oligocene global cooling
(⬇34 Ma; see refs. 11 and 12) and to undergo a major radiation
and range expansion to low latitudes only during later Neogene
cooling (4). Extant penguin species are broadly considered to
be cool-adapted, and even equatorial species are sensitive to
sea surface temperature increases associated with El Niño
Southern Oscillation events (13).
The new fossils are the first to indicate significant lowlatitude penguin diversity over a period characterized by one
of the most important climatic shifts in earth history: the
transition from peak temperatures in the pre-Oligocene greenhouse earth to the development of icehouse earth conditions
(11, 12). The fossils reveal key data on the poorly known
pre-Miocene history of penguins in South America (6, 9, 14).
The fauna, from new Eocene localities in Peru, includes the
two new species as well as additional material indicating the
www.pnas.org兾cgi兾doi兾10.1073兾pnas.0611099104
presence of at least five penguin taxa (ref. 15 and undescribed
specimens). The only other pre-Oligocene penguin fossil from
South America is a partial hindlimb from the high-latitude
southernmost tip of the continent, equivalent in age to the
middle Eocene Peruvian specimens (14). Together, these two
records constitute the earliest for penguins on the continent.
Systematic Paleontology
Aves Linnaeus, 1758 (sensu Gauthier, 1986).
Neognathae Pycraft, 1900.
Sphenisciformes Sharpe, 1891 (sensu Clarke et al., 2003).
Perudyptes devriesi. New genus, new species.
Holotype specimen. Museum of San Marcos University, Peru
(MUSM) 889, comprising a skull, mandible, cervical vertebrae
and ribs, humeri, left carpometacarpus, synsacrum, femora,
right tibiotarsus, and left tarsometatarsus (Fig. 1).
Etymology. ‘‘Peru’’ references the fossil provenance, and ‘‘dyptes’’ is
Greek for diver. The species name ‘‘devriesi’’ honors Tom DeVries,
whose dedicated work and longstanding collaboration in the Pisco
Basin of Peru made possible the discovery of the new localities
and species.
Locality and age. MUSM 889 is from a coarse-grained, thick-bedded,
siliciclastic sandstone exposed at Quebrada Perdida (14°34⬘S,
75°52⬘W), Department of Ica, Peru, identified to the basal portion
of the middle to late Eocene Paracas Formation (16). The presence
of the gastropod Turritella lagunillasensis in correlative sandstone
beds confirms the assignment of the holotype locality to the basal
Paracas Formation (16, 17), as does the discovery of late middle
Eocene radiolarians (Cryptocarpium ornatum, Lithocyclia aristotelis,
and Lithocyclia ocellus) in tuffaceous fine-grained sandstones much
higher in the section (⬇42 Ma).k
Author contributions: J.A.C. and D.T.K. designed research; J.A.C., D.T.K., M.S., M.U., N.G.,
S.B., Y.N., and C.A.B. performed research; J.A.C., D.T.K., M.S., N.G., S.B., Y.N., and C.A.B.
analyzed data; and J.A.C., D.T.K., M.S., N.G., S.B., and C.A.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. R.E.F. is a guest editor invited by the Editorial Board.
Abbreviation: MUSM, Museum of San Marcos University, Peru.
dTo
whom correspondence should be addressed. E-mail: julia㛭clarke@ncsu.edu.
kDeVries, T. J., Narváez, Y., Sanfilippo, A., Malumian, N., Tapia, P., XIII Congreso Peruano de
Geologı́a, Oct. 17–20, 2006, Lima, Perú (ext. abstr.).
This article contains supporting information online at www.pnas.org/cgi/content/full/
0611099104/DC1.
© 2007 by The National Academy of Sciences of the USA
PNAS 兩 July 10, 2007 兩 vol. 104 兩 no. 28 兩 11545–11550
GEOLOGY
New penguin fossils from the Eocene of Peru force a reevaluation of
previous hypotheses regarding the causal role of climate change in
penguin evolution. Repeatedly it has been proposed that penguins
originated in high southern latitudes and arrived at equatorial regions
relatively recently (e.g., 4 – 8 million years ago), well after the onset of
latest Eocene/Oligocene global cooling and increases in polar ice
volume. By contrast, new discoveries from the middle and late Eocene
of Peru reveal that penguins invaded low latitudes >30 million years
earlier than prior data suggested, during one of the warmest intervals
of the Cenozoic. A diverse fauna includes two new species, here
reported from two of the best exemplars of Paleogene penguins yet
recovered. The most comprehensive phylogenetic analysis of Sphenisciformes to date, combining morphological and molecular data,
places the new species outside the extant penguin radiation (crown
clade: Spheniscidae) and supports two separate dispersals to equatorial (paleolatitude ⬇14°S) regions during greenhouse earth conditions. One new species, Perudyptes devriesi, is among the deepest
divergences within Sphenisciformes. The second, Icadyptes salasi, is
the most complete giant (>1.5 m standing height) penguin yet
described. Both species provide critical information on early penguin
cranial osteology, trends in penguin body size, and the evolution of
the penguin flipper.
ENVIRONMENTAL
SCIENCES
Edited by R. Ewan Fordyce, University of Otago, Dunedin, New Zealand, and accepted by the Editorial Board May 21, 2007 (received for review
December 14, 2006)
Fig. 1. Holotype of P. devriesi (MUSM 889). (a) Skull in dorsal view. (b) Skull in left lateral view. (c) Left dentary in medial view. (d) Skull in ventral view. (e) Right
humerus in anterior and posterior views. ( f) Right humerus in proximal view. (g) Right humerus in distal view. (h) Left carpometacarpus in distal view. (i) Left
carpometacarpus in ventral and dorsal views. (j) Synsacrum, ilia, and left femur in dorsal view. (k) Right femur in posterior and anterior views. (l) Left
tarsometatarsus in plantar and dorsal views. All to same scale except j (scale for j is at lower left); f, g, and h are enlarged in the line drawings to show detail.
Anatomical abbreviations: ac, acetabulum; art, articular surface for antitrochanter; at, antitrochanter; cb, coracobrachialis insertion; d, depression on lingual
surface of dentary; f, femur; fmn, articular facet for first digit of metacarpal III; fmj, articular facet for first digit of metacarpal II; ld, scar for latissimus dorsi; mtr,
middle trochlear ridge; nc, nuchal crest; po, postorbital process; pp, pisiform process; ps, expansion of parasphenoid; ptr, posterior trochlear ridge; sc, scar for
supracoracoideus; sf, fossa for salt gland; sp, supracondylar tubercle.
Diagnosis. P. devriesi is diagnosed by the following four autapo-
morphies relative to all other Sphenisciformes: (i) postorbital
process directed anteroventrally; (ii) marked anterior expansion
of the parasphenoid rostrum; (iii) posterior ridge forming the
humeral scapulotriceps groove projects distal to the middle ridge
and is conformed as a large, broadly curved surface; and (iv)
femur with a convex articular surface for the antitrochanter.
Additional differential diagnosis is given in supporting information (SI) Appendix.
Description. Deep temporal fossae excavate the skull roof, and the
frontal is beveled for a supraorbital salt gland. A pronounced
sagittal crest meets the nuchal crest at a 90° angle. The postorbital process is directed anteroventrally, unlike the ventral
orientation in other penguins. The nasal–premaxilla suture is
obliterated. The left mandible indicates a straight, elongate beak
with a short symphysis. A lingually directed flange from the
dorsal margin expands to create a flat surface, a feature previously unknown in penguins. An elongate depression on the
lingual surface of the dentary is similar to a feature present in
Gaviidae (loons) and to an Eocene sphenisciform mandible (18);
extant penguins lack this morphology.
The humerus is flattened and pachyostotic. The dorsal tubercle is nearly level with the apex of the head. The shaft is narrow
and lacks notable distal expansion. The coracobrachialis impression is developed as a shallow oblong fossa, and the tricipital
fossa is deep, undivided, and apneumatic. The supracoracoideus
insertion scar is elongate and well separated from the small,
11546 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0611099104
circular latissimus dorsi insertion scar. A compact dorsal supracondylar tubercle is present, a feature absent in all other
penguins except the basal taxon Waimanu (10). The ulnar
condyle is damaged, but a wide shelf-like surface is preserved
adjacent to the posterior margin of the condyle. Metacarpal II
is anteriorly bowed, with a broad anterior margin unlike the
compressed sharp edge present in extant penguins. The pisiform
process is a low but distinct ridge. The articular facet for the
phalanx of metacarpal III is plesiomorphically subtriangular.
The sutures between the ilia and the sacrum are open. The femur
has a very weak trochanteric crest and is nearly straight for its
preserved length. A proximally placed fibular crest and narrow
supratendinal bridge are discernable on the tibiotarsus. The
tarsometatarsus is short, with a straight metatarsal IV and a
shallow dorsal sulcus between metatarsals II and III. The medial
proximal vascular foramen and the distal vascular foramen are
absent.
Icadyptes salasi. New genus, new species.
Holotype specimen. MUSM 897, comprising a skull, axis, and eight
additional cervical vertebrae, partial right and left coracoids,
cranial end of the left scapula, left humerus, radius, ulna,
proximal carpals, carpometacarpus, and phalanges (Fig. 2).
Etymology. ‘‘Ica’’ refers to the Department of Ica, ‘‘dyptes’’ is
Greek for diver. ‘‘Salasi,’’ honors Rodolfo Salas for his important
contributions to vertebrate paleontology in Peru.
Locality and age. MUSM 897 is from a tuffaceous, diatomaceous,
fine-grained sandstone that is part of the basal transgressive
Clarke et al.
ENVIRONMENTAL
SCIENCES
sequence of the Otuma Formation (16)l exposed in the lower
Ullujaya Valley of the Rio Ica, Department of Ica (14°37⬘S,
75°37⬘W). The fossil-bearing unit lies 70 m above an angular
unconformity marking the base of the depositional sequence.
Specimens of the gastropods Peruchilus culberti and Xenophora
carditigera establish a late-middle to late Eocene age for this
sequence, whereas microfossils from a contiguous and continuous section indicate a more exact age of ⬇36 Ma for the strata
containing MUSM 897.l Additionally, ash beds collected near
the base of the same depositional sequence 5 km southwest
across the Rı́o Ica yielded 40Ar/39Ar dates of 37.2 and 36.5 Ma,
whereas an ash bed higher in the section, correlated with
beds above the horizon bearing MUSM 897, yielded an age of
35.7 Ma.k
Diagnosis. I. salasi possesses four proposed autapomorphies relative to all other penguins: (i) a beak forming more than
two-thirds of the skull length, (ii) fusion of the premaxillae and
palatines, (iii) axis with an elongate hypophysis terminating in a
greatly mediolaterally expanded disk-like plate, and (iv) a deep
ovoid fossa on the lateral surface of the acrocoracoid process. I.
salasi is also differentiated from all other penguins by the
following combination of postcranial characters: humerus with
a straight, broad shaft (midshaft width/length ⫽ 0.22); metacarpal I with a flat carpal trochlea and distinct distal terminus; and
lDeVries, T. J., XII Congreso Peruano de Geologı́a, Oct. 26 –29, 2004, Lima, Perú (ext. abstr.).
Clarke et al.
metacarpals II and III subequal in distal extent. Additional
differential diagnosis is given in SI Appendix.
Description. The skull of I. salasi is the first complete specimen
reported for a basal penguin. Striking is the hyperelongate,
spear-like beak, unlike that of any previously known extinct or
extant penguins. Fusion of the palatal elements and premaxillae
creates a powerfully constructed upper jaw with a flat ventral
surface bounded by lateral ridges and inscribed with reticulate
vascular sucli. Similar vascular texturing is seen in Sulidae
(boobies and gannets) but is not present in other penguins,
suggesting a distinct rhamphotheca in I. salasi. The mandible has
an extensive symphysis with a corresponding flat dorsal surface.
The cranium is extremely narrow, with deep temporal fossae
meeting at a midline sagittal crest. A supraorbital shelf for the
salt gland is present. The external nares extend posterior to the
anterior margin of the antorbital fenestra. The jugal bar is
straight. The pterygoid is rod-like, lacking the fan-like anterior
expansion present in Spheniscidae. The otic process of the
quadrate is shorter than the optic process. The quadrate shaft
bears a tubercle for the adductor mandibulae externus attachment that abuts the squamosal capitulum. A retroarticular
process is present.
The axis is mediolaterally compressed and elongate compared
with extant penguins, and the remaining cervical vertebrae are
robust, particularly compared with the narrow skull. The coracoids preserve deep scapular cotylae, and the scapula shares the
expanded proximal end present in extant penguins. The humeral
supracoracoideus scar parallels the long axis of its shaft, and the
PNAS 兩 July 10, 2007 兩 vol. 104 兩 no. 28 兩 11547
GEOLOGY
Fig. 2. Holotype of I. salasi (MUSM 897). (a) Skull in lateral view. (b) Mandible in dorsal view. (c) Left quadrate in lateral view. (d) Left humerus in posterior
and anterior views. (e) Left ulna in ventral view. ( f) Left radius in ventral view. (g) Left carpometacarpus and phalanges in ventral view. (h) Left coracoid in ventral
view. All are to the same scale except c, which is enlarged to show detail. Anatomical abbreviations: ac, acrocoracoid process; af, anteorbital fenestra; am, tubercle
for m. adductor mandibulae externus; atr, anterior trochlear ridge; cb, coracobrachialis insertion; cf, ovoid coracoid fossa; fa, distal facet of first metacarpal; j,
jugal; lc, lateral cotyle of mandible; mc, medial cotyle of mandible; mtr, middle trochlear ridge; n, nares; ol, olecranon; ptr, posterior trochlear ridge; qc,
quadratojugal cotyle; qt, tubercle on optic process; sc, scar for supracoracoideus; sf, fossa for salt gland; ss, sesamoid of m. scapulotriceps tendon; tf, temporal
fossa; tr, tricipital fossa; ts, transverse sulcus.
Fig. 3. Recovered penguin phylogenetic relationships, including placement of new species P. devriesi and I. salasi (in red) and showing stratigraphic and
latitudinal distribution of species against ␦18O values as a proxy for changes in global temperature over the last 65 Ma (from ref. 12). The strict consensus
cladogram of the four most parsimonious trees (4,356 steps) is shown. Black bars indicate stratigraphic range. No neospecies has a fossil record extending beyond
11548 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0611099104
Clarke et al.
Body Size Evolution
The phylogenetic results are consistent with a single origin of
extremely large size in the penguin lineage (in contrast to ref. 27)
by the early Eocene and retained in Icadyptes. Giant size
persisted into the Oligocene (6, 19) across the Eocene–
Oligocene climate transition (Fig. 3). Intriguingly, over late
Tertiary global cooling, the average size of penguins has become
smaller (Fig. 3).
Icadyptes was far larger than any living penguin, whereas
Perudyptes was approximately the size of the extant king penguin.
Compared with the three largest previously described extinct
taxa, the I. salasi holotype humerus is ⬇5 mm shorter than the
largest exemplars of Pachydyptes ponderosus (19) and Anthropornis nordenskjoeldi (8, 28) and exceeds the largest of Palaeeudyptes klekowskii (28) by ⬇9 mm. Regressions based on
hindlimb measurements estimated the standing height and mass
of A. nordenskjoeldi (1.66–1.99 m and 81.7–97.8 kg, respectively)
and of P. klekowskii (1.47–1.75 m and 56.0–65.7 kg, respectively)
(29). Humeral dimensions indicate that the holotype individual
of I. salasi would be intermediate in size between these two taxa,
yielding a conservative minimum standing height of 1.5 m.
When the body size of low-latitude I. salasi is compared with
all higher latitude taxa with overlapping observed and inferred
stratigraphic ranges (Fig. 3), I. salasi is larger or approximately
the same size. Although body size distribution in birds has been
suggested to be largely consistent with the proposed biological
law ‘‘Bergmann’s rule,’’ relating cooler temperatures and higher
latitudes with large body size (e.g., refs. 30 and 31; although, see
ref. 32), the warm water foraminiferan Asterigerina has been
recovered in matrix associated with giant-form P. ponderosus, a
form approximately the same size as Icadyptes (19). Giant size in
the penguin lineage does not appear to be correlated with either
cooler temperatures or higher latitudes. A period of increased
late Eocene upwelling (11) and ocean productivity that would
have impacted the Peruvian coast (26) should be investigated as
the Pleistocene (6). Extinct taxa are indicated with a †. Branch color indicates the latitude of extant taxon breeding territories and the paleolatitude of fossil taxon
localities, with ancestral latitude ranges reconstructed along internal branches from downpass optimization: 0 –30°S latitude (yellow), 30 – 60° (green), and
60 –90° (blue). Silhouettes reflect body size; small silhouettes indicate taxa smaller than extant Aptenodytes patagonicus (king penguin), medium silhouettes
indicate taxa intermediate between A. patagonicus and Aptenodytes forsteri (emperor penguin), and large silhouettes indicate taxa larger than A. forsteri. The
plot of mean ␦18O values and estimated mean ocean water temperature scale (only valid for an ice-free ocean, preceding major Antarctic glaciation at ⬇35 Ma)
are from ref. 12 and give an indication of changing conditions across the Cenozoic.
Clarke et al.
PNAS 兩 July 10, 2007 兩 vol. 104 兩 no. 28 兩 11549
ENVIRONMENTAL
SCIENCES
Penguin Evolution and Cenozoic Climate Change
Phylogenetic results from analysis of the largest data set yet
compiled for penguins, following the combined analysis methods
of ref. 20, identify P. devriesi as a deep divergence within
penguins and I. salasi as part of a paraphyletic assemblage of
giant Eocene–Oligocene taxa closer to Spheniscidae, the penguin crown clade (Fig. 3). Relationships among extant genera are
those recovered from less inclusive molecular data sets in
maximum-likelihood and Bayesian analyses (4).
The Peruvian species inform estimates of Pacific biotic connections during greenhouse-to-icehouse earth transition. Two
equatorial ingressions by Paleogene penguins are supported
(Fig. 3). On the basis of ancestral area reconstructions (see SI
Appendix), one dispersal from Antarctic regions is inferred by
the middle Eocene and a second from New Zealand by the late
Eocene. Whether this biogeographical pattern reflects proposed, but controversial, late Eocene (⬇41 Ma; ref. 21) beginnings for reorganization of southern ocean circulation patterns
and isolation of Antarctica (21) deserves further investigation.
We find no fossil evidence for the extant penguin radiation,
Spheniscidae, earlier than a species of Spheniscus ⬇8 million
years in age (22); all pre-late Miocene taxa are placed outside
this radiation (Fig. 3). By contrast, molecular sequence divergence estimates identify the origin of this radiation at 40 Ma (4).
Although there is an extensive sphenisciform fossil record from
multiple continents between 40 and 8 Ma, no fossil from this
interval has been placed as part of Spheniscidae (refs. 6 and 23
and Fig. 3). Calculations from modified scripts for MSM*range
(ref. 24 and see Materials and Methods) indicate that accommodation of the molecular divergence estimates would require an
additional 164.1–334.2 million years of missing fossil record (a
172–205% increase) compared with the inferred missing record
(‘‘ghost lineages’’) given only cladogram topology and fossil ages.
The fossil record of penguins is approximately three times as
incomplete when divergence dates are required to be true and
would be strikingly biased toward recovery of only stem taxa.
Extant penguin diversification may be related to later Neogene global cooling phases (4, 12), but there is no fossil evidence
to support a crown radiation in the Paleogene concomitant with
the initiation of the circum-Antarctic current, initial onset of
Cenozoic global cooling, or at the proposed extinction of giant
penguins (in contrast to ref. 4). An Oligocene fossil cited as
representing the extant genus Eudyptula in support of a Paleogene crown radiation (4) is not assignable to that genus (6).
Although stratigraphic data can only falsify a divergence date
when a fossil discovery is older than estimated, the large amount
of implied missing fossil record suggests that proposed crown
penguin divergence times may be too old. Future analyses using
calibration points within the crown clade (e.g., refs. 22 and 25)
could improve the fit of these estimates.
Based on inferred patterns linking latitudinal expansion,
increases in extant species diversity, and phases of Cenozoic
global cooling, it was predicted (4) that global warming could
trigger an opposite pattern in the penguin lineage, with equatorial species retreating to higher latitudes and high-latitude
species facing extinction. This prediction is supported by data on
some extant species (1, 3). The new Peruvian species indicate
that early in penguin evolution there was a more complex
relationship between global temperature and diversity than
previously recognized. Additional factors such as upwelling (26)
and ocean circulation patterns (6, 20, 23) were also critical in the
evolution of the penguin lineage. Because the Peruvian species
are members of the stem sphenisciform lineage and current
global warming would be on a distinct, significantly shorter time
scale, the data from these basal forms should not be used to
refute predictions of changes in extant penguin distribution with
continued warming. Given the different interactions between
climate and distribution seen in basal penguins and in extant
species, the physiological and ecological factors that could drive
the response of extant penguins to climate change (1, 3, 13) may
well be restricted to the crown clade.
GEOLOGY
latissimus dorsi insertion is displaced distally to near midshaft.
The tricipital fossa is undivided. Two distal trochlea are present
for the humerotriceps and scapulotriceps sesamoids. The ulnar
olecranon process is tab-like and proximally located, as in
Waimanu (10) and Palaeeudyptes (19). The radius bears a
roughened anteroproximal brachialis insertion surface but lacks
a proximally directed process on the anterior border. Metacarpals II and III are equal in distal extent as in some other
Paleogene species, whereas in extant and most extinct species
metacarpal III extends farther. A free alular digit is absent.
Phalanx II-1 is longer than phalanx III-1, unlike in extant
penguins in which these two digits are subequal in length.
a potentially important factor driving low-latitude penguin species diversity and body size.
Implications for the Evolution of Penguin Morphology
The Peruvian fossils provide insight into early penguin cranial
anatomy and the evolution of the penguin flipper apparatus. An
elongate, powerfully constructed beak unknown in extant penguins
is present in both Perudyptes and Waimanu (10) and, in an extreme
form, in Icadyptes. This morphology can now optimized as ancestral
for penguins. Undescribed long-billed Oligocene fossils have also
been reported (6, 10), revealing that this morphology was retained
for a significant portion of early penguin evolution and through the
greenhouse-to-icehouse transition (12).
Perudyptes displays a unique combination of traits that fills an
important gap between the wing morphology of the basal-most
penguin, Waimanu, and living penguins. The extant penguin
wing is highly modified into a stiffened, paddle-like structure
equipped with a greatly reduced set of intrinsic wing muscles (33)
and exhibiting the lowest degree of intrinsic joint mobility of any
extant avian group (34). The presence of a conspicuous dorsal
supracondylar tubercle and distinct pisiform process in Perudyptes are consistent with retention of functioning major intrinsic wing muscles whose attachment surface (extensor carpi
radialis) and pulley-like guide (flexor digitorum profundus)
these processes represent. In penguins closer to and including the
crown clade, the dorsal supracondylar tubercle is absent, with
indication of muscle origin reduced to a weak, flat scar. The
pisiform process is reduced to a barely perceptible ridge. Like
other basal penguins, Perudyptes retains a prominent ulnar
condyle that potentially permitted greater flexion at the humerus/ulna joint, although the large shelf adjacent to the condyle
would restrict flexion during the flight downstroke (23). New
data from the Peruvian fossils invite further biomechanical
research to discern implications for locomotor differences and
feeding ecology in basal penguins.
Conclusions
With the discovery of the new Peruvian species, penguins show
a much more complex relationship with climate factors early in
their evolution. Inference of ancestral vs. extant ecologies within
a lineage, and attention to when in that lineage derived characteristics arose, are key to qualifying interpretations relating past
biotic events causally to climate shifts, as well as to informing
predictions for future responses to change. Although molecular
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11550 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0611099104
divergence dating approaches offer great insight into the timing
and potential causal factors in lineage diversification, case
studies evaluating groups with a comparably rich record offer the
only available test to these scenarios. In the case of the penguin
lineage, a much more complex paleobiogeographical pattern and
grossly different timing of key origin and radiation events are
indicated, at odds with current divergence dating estimates.
Materials and Methods
Phylogenetic Analysis and Ancestral Area/Latitude Reconstruction.
The data set comprised 194 morphological characters sampled
for 43 fossil and living penguin taxa and ⬇6.5 kbp from five genes
(RAG-1, 12S, 16S, COI, and cyt-b) for all extant penguins. Direct
optimization methods and search strategy follow ref. 20, with 200
tree bisection and reconnection replicates conducted in POY
(version 3.0.11; American Museum of Natural History). See SI
Data Set and SI Appendix for matrix, GenBank accession numbers, Bremer support values, area and latitude categories, and
references for fossil ages.
Missing Fossil Range Calculation. MSM*range (24), a method used
to compare the temporal order of successive branching events
with the age of appearance of terminal taxa in the stratigraphic
record, was adapted to analyze the effects of requiring the
divergence times estimated from calibrated molecular sequence
data (4). Ancestral nodes, and associated inferred divergence
dates, were incorporated into the analyzed Newick tree. The
range of missing record reflects the iterative first appearance
datum sampling procedure used by MSM*range and different
resolutions of polytomies in our consensus tree.
We thank T. DeVries for stratigraphic data and for many contributions
to Peruvian geology and paleontology; R. Salas, N. Valencia, D. Omura,
W. Aguirre, and E. Dı́az, for fieldwork assistance and fossil preparation;
L. Brand and C. Aguirre for contributions to fieldwork; K. Lamm for
illustrations; T. Ando and R.E.F. for information on Waimanu; P.
Goloboff for supercluster access; and the editor and two anonymous
reviewers for comments that improved our manuscript. We are grateful
for support provided by the National Science Foundation Office of
International Science and Engineering, National Geographic Society
Expeditions Council, North Carolina State University, and North Carolina Museum of Natural Sciences (J.A.C.); The Frank M. Chapman
Memorial Fund, The Doris O. and Samuel P. Welles Research Fund, and
American Museum of Natural History Division of Paleontology
(D.T.K.); and the National Science Foundation Assembling the Tree of
Life Project: Archosaur Phylogeny.
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SI Appendix
Additional Differential Diagnosis for Perudyptes devriesi and Icadyptes salasi. Multiple
features of the skulls of P. devriesi and I. salasi are unknown in any other penguins and are
currently supported as apomorphies of these species (i.e., those given in the main text).
However, cranial material is rare for fossil penguin taxa, and additional differential diagnosis
is desirable. The tarsometatarsus and humerus are traditionally considered among the most
diagnostic bones in the penguin skeleton, and either one or both of these elements is included
in the hypodigm of all named species, with the exception of the fossil crown species
Pygoscelis calderensis. These two elements are thus given particular attention below.
The humerus of P. devriesi differs from all described penguin humeri by the
apomorphies described in the main text. P. devriesi can be additionally differentiated from
Mesetaornis polaris, Marambiornis exilis, Delphinornis larseni, Delphinornis gracilis,
Delphinornis arctowski, Duntroonornis parvus, and Korora oliveri (the humerus is unknown
for these taxa) by the absence of the medial proximal vascular foramen of the tarsometatarsus
as well as by much larger size. The absence of the medial proximal vascular foramen also
differentiates P. devriesi from all extant species, Waimanu manneringi, Waimanu tuatahi,
Anthropornis nordenskjoeldi, Anthropornis grandis, Paraptenodytes antarcticus,
Archaeospheniscus lopdelli, and Archaeospheniscus wimani. A penguin from Tierra del
Fuego (CADIC P-21) approximately the same age as P. devriesi (6) remains unnamed,
nevertheless it should be noted that P. devriesi differs from this fossil by features of the femur
listed in the main text. For example, by contrast to the femoral morphologies described and
figured for P. devriesi, CADIC P-21 possesses a conspicuously concave antitrochanteric
articular surface and exhibits greater projection of the trochanteric crest.
Given the phylogenetic placement and large size of I. salasi, comparisons with
Pachydyptes, Anthropornis, and specimens traditionally assigned to the genus Palaeeudyptes
are most relevant. I. salasi differs from Pachydyptes ponderossus in possessing a significantly
more slender humerus (midshaft length/width = 0.22 for I. salasi, 0.26 for P. ponderossus).
Metacarpal I of I. salasi ends in a distinct flat surface, whereas metacarpal I of P. ponderossus
appears to slope gradually to the level of metacarpal II, without a distinct flat distal end. I.
salasi differs from all specimens traditionally assigned to the genus Palaeeudyptes
(Palaeeudyptes klekowskii, Palaeeudyptes gunnari and New Zealand specimens traditionally
assigned to Palaeeudyptes antarcticus) in two features of the humerus. The coracobrachialis
caudalis scar (located on the proximal lip of the tricipital fossa) is significantly less distally
directed in I. salasi, and the shaft of the humerus is much wider in I. salasi than in all of these
specimens. Additionally, I. salasi differs from the New Zealand specimens OM C.47:23 and
C.47:25 (referred to Palaeeudyptes) in possessing an ulna with a more proximally placed
olecranon process and a carpometacarpus with metacarpal I ending in a distinct facet. The
humerus of I. salasi differs from humeri assigned to A. nordenskjoeldi and A. grandis by
possessing a nearly straight, as opposed to strongly sigmoid, shaft. Further, Icadyptes and
these species are distantly related in the results of the phylogenetic analysis.
Notes on the Phylogenetic Data Set and Ancestral Area Catagories. The data set includes
17 extant penguin species (plus one distinct subspecies) and 26 fossil taxa, evaluated for 194
morphological characters. The data set also includes ≈6.5kbp from one nuclear and four
mitochondrial genes (RAG-1, 12S, 16S, COI, and cyt-b) for all extant penguins. This study
adds eight ingroup and two outgroup operational taxonomic units and 15 morphological
characters to previously published penguin data sets (1–3). Codings for 53 of the 58
operational taxonomic units were taken from direct observation of specimens, and codings for
M. polaris, M. exilis, Eretiscus tonnii, W. manneringi, and W. tuatahi were obtained from the
literature. Three specimens previously assigned to P. antarcticus (4) or Palaeeudyptes sp. (5)
were treated as separate terminals because they preserve combinations of characters that
suggest they are not monophyletic. Procellariiformes (12 species) and Gaviiformes (2 species)
were used as outgroups, because these higher taxa have been consistently identified as the
closest relatives of Sphenisciformes in analyses of both morphological and molecular data
(reviewed in refs. 1, 2, and 6; although, see ref. 7).
Sequence treatment follows (1), with molecular and morphological transformations
weighted equally. Search refinements were conducted on the results (tree fusing; ref. 8), and
Bremer support values were calculated (see SI Fig. 4 below). The phylogenetic signal in the
molecular data is robust to the choice of alignment and optimization criteria.
To reconstruct ancestral biogeographic distributions, the Southern Hemisphere was
divided into nine discrete areas representing the breeding ranges of extant penguins (obtained
from ref. 9), and each of these areas was assigned a character state for a single geographic
character. These areas are (i) the Galapagos Islands, (ii) South African coast, (iii) Tristan da
Cunha and Gough, (iv) Bouvet Island, (v) Kerguelen and other Indian Ocean islands, (vi)
Australia/New Zealand, (vii) Antarctic Peninsula, (viii) Scotia Arc, and (ix) shores of the
Antarctic Continent (for area definition criteria, see ref. 1). Each extant taxon was assigned as
many states as required to represent its breeding territory. Extinct taxa were scored based on
known fossil range (see SI Table 1, below), with the assumption that the localities of a fossil
taxon represented, or at least included, in its breeding territory. This geographic character was
mapped onto the strict consensus cladogram from the phylogenetic analysis by using a single
downpass optimization, consistent with a dispersal–vicariance interpretation of historical
biogeographic reconstruction (10). In this way, ancestral distributions can be reconstructed.
The same methodology was applied to reconstruct the latitudinal distributions presented in
Fig. 3. In this case, a geographical character was created with three states: Antarctic
(encompassing 60–90°S latitude), Subantarctic (30–60°), or Subtropical/Tropical (0–30°).
Extinct taxa were scored based on known fossil range, corrected for differences in
paleolatitude.
GenBank Accession Numbers and Authorship of Sequences Used
12S rDNA:
(11): DQ137187, DQ137190-1, DQ137193-4, DQ137196-202, DQ137205.
(12): U88007, U88024.
García-Moreno et al. (unpublished): AY139621, AY139623, AY139630.
(13):X82517-8, X82522-3, X82533.
(14): AY158677; NC_004538.
(15): AF173573, AF173577-8.
16S rDNA:
(11): DQ137147-62, DQ13714765-6.
(14): AY158677, AY293618.
cytochrome b:
(11): DQ137207-10, DQ137215-20, DQ13723-5, NC_004538;
(16): U48943, U48955.
(17): AF076051-2, AF076046, AF076060, AF076062, AF076064, AF076068, AF076076,
AF076089-90, U74335, U74350, U74353.
(18): AF158250.
COI:
(11): DQ137167-72, DQ137174-86
(14): NC_007172.
(19): AY666477, AY666284.
RAG-1:
(10): DQ137230-3, DQ137235-47.
Fig. 4. Primary phylogenetic analysis results. A strict consensus cladogram (four trees; tree
length = 4,356 steps) with Bremer support values and ancestral area reconstructions from the
biogeographical analysis. Area abbreviations: AC, shores of the Antarctic continent; AF,
South African coast; AP, Antarctic Peninsula; B, Bouvet Island; G, Galapagos Islands; I,
Kerguelen and other Indian Ocean islands; NZ, Australia/New Zealand; S, Scotia Arc; and
TG, Tristan da Cunha and Gough.
Table 1. Locality and Age Data Used to Construct Fig. 3
Taxon
Locality
Age
Citations
Anthropornis grandis
Seymour Island, Antarctica
mid-latest Eocene
20
Latest Eocene
20
4, 21, 22
Telm 4-7 of La Meseta Fm.
Anthropornis
Seymour Island, Antarctica
nordenskjoeldi
Telm 7 of La Meseta Fm.
Archaeospheniscus
Duntroon, New Zealand
Late Oligocene
lopdelii
Kokoamu Greensand
(Duntroonian stage)
Archaeospheniscus
Duntroon, New Zealand
Late Oligocene
lowei
Kokoamu Greensand
(Duntroonian stage)
Delphinornis larseni
Seymour Island, Antarctica
mid-latest Eocene
4, 21, 22
20
Telm3-7 of La Meseta Fm.
Eretiscus tonnii
Chubut Valley, Argentina
early Miocene
24
Gaiman Fm. (formerly
referred to as ‘Patagonia Fm.’)
Marplesornis
Motunau, North Canterbury,
most likely Pliocene
novaezealandiae
New Zealand
(Waitotaran stage)
Marambiornis exilis
Seymour Island, Antarctica
latest Eocene
25, 26
20
Telm 7 of La Meseta Fm.
Marambiornis exilis
Seymour Island, Antarctica
latest Eocene
20
Telm 7 of La Meseta Fm.
Pachydyptes
Fortification Hill, Oamau,
ponderosus
New Zealand
latest Eocene
21, 22
mid-latest Eocene
20
latest Eocene
20
late Eocene
21, 22
21, 22
Ototara Limestone
Palaeeudytpes
Seymour Island, Antarctica
gunnari
Telm3-7 of La Meseta Fm.
Palaeeudyptes
Seymour Island, Antarctica
klekowskii
Telm 7 of La Meseta Fm.
Palaeeudyptes sp.
Burnside, Dunedin
C48:73-81
New Zealand
Burnside Mudstone
Palaeeudyptes sp.
Duntroon, New Zealand
late Oligocene
C47:23
Kokoamu Greensand
(Duntroonian stage)
Palaeeudyptes sp.
Duntroon, New Zealand
late Oligocene
C47:25
Kokoamu Greensand
(Duntroonian stage)
Palaeospheniscus
Chubut and Santa Cruz,
early-middle
patagonicus
Argentina, Gaiman Fm.
Miocene
21, 22
26, 27
(formerly referred to as
‘Patagonia Fm.’)
Peru, Chilcatay Fm.
Paraptenodytes
Chubut Valley, Argentina
antarcticus
lower and middle
Patagonia Fm.
early Miocene
26
Platydyptes amiesi
Platydyptes marplesi
Hakataramea Valley,
late Oligocene
South Canterbury,
(Duntroonian or
New Zealand
Waitakian stage)
Duntroon, New Zealand
late Oligocene
(recorded Oamaru, but
(Duntroonian stage)
21, 22
21, 22
believed to be Wharekuri)
Oamaru, New Zealand
late Oligocene
21, 22
Spheniscus
Pisco Basin, Peru
late Miocene to
28
megaramphus
Pisco Fm.
early Pliocene
Spheniscus urbinai
Pisco Basin, Peru
late Miocene to
Pisco Fm.
early Pliocene
Waimanu
Waipara River,
early Paleocene
14
manneringi
New Zealand
late Paleocene
14
Platydyptes
novaezealandiae
29
Basal Waipara Greensand
Waimanu tuatahi
Waipara River,
New Zealand
middle to upper
Waipara Greensand
Table 2. Measurements (mm) of P. devriesi (MUSM 889) and I. salasi (MUSM 897)
P. devriesi
I. salasi
Total length
-
~318
Beak
-
~230
Diameter of scapular cotyle
-
15.3
Maximum length
-
~167
Length head to ulnar condyle
113.8
164.0
Greatest proximal width
31.5
61.7
Length of coracobrachialis fossa
~30
~42
Width at midshaft
18.5
36.1
Breadth at midshaft
9.6
16.9
Ulna
Total length
-
114.5
Radius
Total length
-
116.1
Carpometacarpus
Total length
-
97.6
Phalanx II-1
Total length
-
59.5
Phalanx II-2
Total length
-
39.5
Phalanx III-1
Total length
-
40.6
Cranium
Coracoid
Humerus
Character Descriptions for Morphological Characters Used in the Phylogenetic
Analysis. Nineteen characters, marked with an asterisk, are new to this study or have been
significantly revised. See refs. 1–3 for detailed description, discussion of sources, and
illustrations of previously used characters.
INTEGUMENT
1. Tip of mandibular rhamphotheca, profile in lateral view: pointed (0); slightly truncated (1);
strongly truncated, squared off (2); truncated but with a rounded margin (e.g., as seen in
Procellariiformes) (3).
2. Longitudinal grooves on the base of the culmen: absent (0); present (1).
3. Longitudinal grooves on the base of latericorn and ramicorn: absent (0); present (1).
4. Feathering of maxilla (rostrum maxillare), extent: completely unfeathered (0); slightly
feathered, less than half the length of maxilla (1); feathering that reaches half the length of
maxilla (2); feathering surpassing half the length of maxilla (3). Ordered
5. Ramicorn, inner groove at tip: absent (0); present and single (1); present and double (2).
Ordered.
6. Orange or pink plate on ramicorn: absent (0); present (1).
7. Plates of ramphotheca, inflated aspect: absent (0); present (1).
8. Gape (rima oris), aspect: not fleshy (0); margin narrowly fleshy (1); margin markedly
fleshy (2). Ordered.
9. Ramicorn color pattern: black (0); reddish (1); pink (2); yellowish (3); orange (4); green
(5); blue (6).
10. Latericorn and ramicorn, light distal mark: absent (0); present (1).
11. Latericorn color: black (0); red (1); orange (2); yellow (3); green (4); blue (5).
12. Culminicorn color: black (0); red (1); orange (2).
13. Maxillary and mandibulary unguis, color: black (0); red (1); yellow (2); green (3); bluish
gray (4).
14. Bill of downy chick, color: dark (0); reddish (1); pale, variably horn to yellowish (2);
bluish (3).
15. Bill of immature, color: dark (0); bicolored reddish and black (1); red (2); yellowish (3);
grayish (4).
16. Nostril tubes: absent in adult (0); present in adult (1).
17. Nostril tubes: absent in hatchling (0); present in hatchling (1).
18. External nares: present (0); absent (1).
IRIS
19. Iris color: dark (0); reddish-brown (1); claret red (2); yellow (3); white (4); silvery gray
(5).
FEATHERS
20. Scale-like feathers: absent (0); present (1).
21. Rhachis of contour feathers: cylindrical (0); flat and broad (1).
22. Rectrices: form a fan functional for steering (0); do not form a functional fan (1).
23. Remiges: differentiated from contour feathers and specialized for flight propulsion (0);
indistinct from contour feathers (1).
24. Apteria: present (0); absent (1).
25. Molt of contour feathers: gradual (0); simultaneous (1).
ADULT PLUMAGE
26. Yellow pigmentation in crown feathers (pileum): absent (0); present (1).
27. Head plumes (crista pennae): absent (0); present (1).
28. Head plumes (crista pennae), aspect: compact (0); sparse (1).
29. Head plumes (crista pennae), aspect: heading upward (0); heading backward, not
drooping (1); heading backward, drooping (2).
30. Head plumes (crista pennae), position of origin: at base of bill close to gape (0); on the
recess between latericorn and culminicorn (1); on forehead (2). Ordered.
31. Head plumes (crista pennae), color: yellowish (0); orange (1).
32. Nape (occiput), crest development: absent (0); slight (1); distinct (2). Ordered.
33. Periocular area (regio orbitalis), color: black (0); white (1); yellow (2); bluish gray (3).
34. Fleshy eyering (regio orbitalis): absent (0); present (1).
35. White eyering (regio orbitalis): absent (0); present (1).
36. White eyebrow (regio orbitalis, supercilium): absent (0); narrow, from postocular area
(1); narrow, from preocular area (2); wide, from preocular area (3). Ordered.
37. Loreal area (lorum), aspect: feathered (0); with spot of bare skin in the recess between
latericorn and culminicorn (1); with spot of bare skin contacting eye (2); bare skin
extending to the base of bill (3). Ordered.
38. Auricular patch (regio auricularis): absent (0); present (1).
39. Throat pattern (jugulum): black (0); white (1); yellowish (2); irregularly streaked (3); with
chinstrap (4).
40. Collar: absent (0); at most slight notch present (1); present, diffusely demarcated (2);
black, strongly demarked (3). Ordered.
41. Breast (pectus), golden in color: absent (0); present (1).
42. Dorsum color: black (0); dark bluish gray (1); light bluish gray (2).
43. Black marginal edge of dorsum between lateral collar and axillary patch (axilla),
contrasting with dorsum: absent (0); present (1).
44. Black dots irregularly distributed over white belly (venter): absent (0); present (1).
45. Flanks (ilia), dark lateral band reaching the breast (pectus): absent (0); present (1).
46. Distinct dark axillary patch of triangular shape (axila): absent (0); present (1).
47. Flanks (ilia), extent of dorsal dark cover into the leg: incomplete, not reaching tarsus (0);
complete, reaching tarsus (1).
48. Rump (pyga): indistinct from dorsum (0); distinctly whitish (1).
49. Tail length (cauda): short, the quills barely emerge from the rump (0); the quills are
distinctly developed (1).
50. Outer rectrices, color: same as inner rectrices (0); lighter than inner rectrices (1).
51. White line connecting leading edge of flipper with white belly (venter): absent (0); present
(1).
52. Flipper (ala [membrum thoracicum]), upperside, light notch at base: absent (0); present
(1).
53. Leading edge of flipper (ala [membrum thoracicum]), pattern of upperside: black (0);
white (1).
54. Leading edge of flipper (ala [membrum thoracicum]), pattern of underside: white (0);
incompletely dark (1); completely dark and wide (2). Ordered.
55. Flipper (ala [membrum thoracicum]), underside, dark elbow patch: absent (0); present (1).
56. Flipper (ala [membrum thoracicum]), underside, tip pattern: immaculate (0); patchy, in
variable extent (1); small circular dot present (2).
IMMATURE PLUMAGE
57. White eyebrow (supercilium): absent (0); or present (1).
58. Throat pattern (jugulum): black (0); or mottled (1); or white (2); or brown (3).
59. Flanks (ilia), dark lateral band: absent (0); or present (1).
60. Chicks hatch almost naked: no (0); yes (1).
61. Dominant color pattern of first down: pale gray (0); distinctly brown (1); bicolored, dark
above and whitish bellow (2); uniformly blackish gray (3).
62. Dominant color pattern of second down: pale grey (0); distinctly brown (1); bicolored,
dark above and whitish bellow (2); uniformly blackish gray (3).
63. Chick, second down, collar: absent (0); present (1).
TARSUS
64. Feet (pedes), dorsal color: dark (0); pinkish (1); orange (2); white-flesh (3); blue (4).
65. Feet (pedes), dark soles: absent (0); present (1).
66. Feet (pedes), unguis digiti: flat (0); compressed (1).
BREEDING
67. Clutch size: two eggs (0); one egg (1).
68. Incubatory sac: absent (0); present (1).
69. Nest: no nest, incubation over the feet (0); nest placed underground, either burrowed on
sand or inside natural hollow or crack (1); open nest, a shallow depression on bare ground
or in midst of vegetation (2).
70. Size of first egg relative to the second egg: similar (0); dissimilar, first smaller (1);
dissimilar, second smaller (2).
71. Crèche: absent (0); small, 3-6 birds (1); conformed by dozens to hundreds of immatures
(2).
72. Eggs, shape: oval (0); conical (1); spherical (2).
73. Ecstatic display: absence (0); presence (1).
OSTEOLOGY
74. Premaxilla, tip (os premaxillare, rostrum maxillare): pointed (0); hooked (1); strongly
hooked (2). Ordered.
*75. Internarial bar (pila supranasalis) shape in cross section: suboval (0); inverted U-shape
(1).
76. Basioccipital, subcondylar fossa (os basioccipitale, fossa subcondylaris): absent or
shallow (0); deep (1).
77. Supraoccipital, paired grooves for the exit of v. occipitalis externae (os supraoccipitale,
sulcus vena occipitalis externae): poorly developed (0); deeply excavated (1).
78. Frontal, shelf of bone bounding salt-gland fossa (os frontale, fossa glandulae nasalis)
laterally: absent (0); present (1).
79. Squamosal, temporal fossa (os squamosum, fossa temporalis), size: fossae separated by
considerable wide surface (at least the width of the cerebellar prominence) (0); more
extensive, fossae meeting or nearly meeting at midline of the skull (1).
80. Squamosal, temporal fossa (os squamosum, fossa temporalis), depth of caudal region: flat
(0); shallow (1); greatly deepened (2). Ordered.
81. Squamosal (os squamosum), development of the opening/s that transmits the a.
ophthalmica externa in the caudoventral area of the fossa temporalis (near the crista
nuchalis): small or vestigial (0); well-developed (1).
82. Orbit (orbita), fonticuli orbitocraneales: small or vestigial (0); broad and conspicuous
openings (1).
83. Ectethmoid (os ectethmoidale): absent (0); weakly developed, widely separate from the
lacrimal (1); well developed, contacting or fused to the lacrimal (2).
84. Lacrimal (os lacrimale): unperforated (0); perforated (1).
85. Lacrimal (os lacrimale): reduced, concealed in dorsal view (0); small portion exposed in
dorsal view (1); well-exposed in dorsal view (2). Ordered.
86. Lacrimal (os lacrimale), dorsal border: closely applied to the frontal (0); separated by a
wide split from the frontal (1).
87. Nasal cavity, external naris (cavum nasi, apertura nasi ossea), caudal margin: extended
caudal to the rostral margin of the hiatus orbitonasalis (0); not extended caudal to the
rostral margin of the hiatus orbitonasalis (1).
88. Nasal cavity, pila supranasalis: slender, slightly constricted laterally (0); wide throughout
its length (1).
89. Basitemporal plate (lamina parasphenoidalis), dorsoventral position with respect to the
occipital condyle: ventral to the level of the condyle (0); at the level of the condyle (1);
dorsal to the level of the condyle, surface depressed (2). Ordered.
90. Basipterygoid process (proccessus basipterygoideus): absent (0); vestigial or poorly
developed (1); well developed (2). Ordered.
91. Eustachian tubes (tuba auditiva): open or very little bony covering near the caudal end of
the tube (0); mostly enclosed by bone (1).
92. Pterygoid (os pterygoideum), shape: elongated (0); slight lateral expansion of rostral end
(1) rostal end broad, pterygoid sub-triangular (2). Ordered
93. Palatine (os palatinum), lamella choanalis: curved and smooth plate, sligthly
differentiated from main palatine blade (0); ridged, distinct from main blade by a low keel
(1); extended vertically ventrally forming the crista ventralis (2). Ordered.
94. Vomer (vomer): laterally compressed, vertical laminae and free from palatines (0);
horizontally flattened laminae and ankylosed with palatines (1), absent (2).
95. Facial foramen (ossa otica, fossa acustica interna, foramen n. facialis): absent (0); present
(1).
96. Jugal arch (arcus jugalis), bar shape in lateral view: straight (0); slightly curved (1);
ventrally bowed (2); strongly curved, sigmoid shape (3). Ordered.
97. Jugal arch (arcus jugalis), dorsal process: absent (0); present (1). This pointed process is
located on the caudal end of the jugal, adjacent to the condyle for articulation with the
quadrate.
98. Premaxilla, frontal process (os premaxillare, proc. frontalis), naso-premaxillary suture:
visible (0); obliterated (1).
99. Quadrate, otic process (os quadratum, proc. oticus), rostral border, tuberculum origi m.
adductor mandibulae externus, pars profunda: absent (0); present, as a ridge (1);
presence, as a tubercle (2).
100. Tomial edge (crista tomialis): plane of tomial edge approximately at the level of the
basitemporal plate (lamina parasphenoidalis) (0); dorsal to the level of the basitemporal
plate (1).
*101. Mandible, symphysis (rostrum mandibulae, pars symphysialis): extensive bony
connection (0); short terminal bony connection (1).
102. Mandible, coronoid process (mandibula, processus coronoideus), position on the dorsal
margin of the mandible with respect to the caudal fenestra (fenestra mandibulae
caudalis): markedly rostral (0); on the rostral end of the fenestra (1); caudal to fenestra
(2). Ordered.
103. Mandible, rostral fenestra (mandibula, fenestra mandibulae rostralis): imperforate or
small opening (0); large opening (1).
104. Mandible, caudal fenestra (mandibula, fenestra mandibulae caudalis): open, can be seen
through from the medial or lateral aspects (0); nearly or completely concealed by the os
spleniale medially, i.e., fenestra not visible in the medial aspect (1).
105. Mandible, mandibular ramus (mandibula, ramus mandibulae): depth subequal over
entire ramus (0); pronounced deepening at midpoint (1).
106. Mandible, dentary, length of dorsal edge (ossa mandibulae, os dentale, margo dorsalis)
relative to mandibular ramus length in lateral view: markedly more than half the length
of ramus (0); approximately half the length of ramus (1).
107. Mandible, articular, medial process (os articulare, proc. medialis mandibulae): not
hooked (0); hooked (1).
108. Mandible, angular, retroarticular process (mandibula, os angulare, proc.
retroarticularis), aspect in dorsal view in relation to the articular area with the quadrate
(area between the lateral condyle [condylus lateralis] and medial condyle [condylus
medialis]): broad, approximately equal to the articular area (0); moderately long,
narrower than the articular area (1); very long, longer and narrower than the articular
area (2). Ordered.
109. Mandible, angular (mandibula, os angulare), aspect in dorsal view: sharply truncated
caudally (0); caudally projected, forming the retroarticular process (proc.
retroarticularis) (1).
110. Mandible, medial emargination between retroarticular process (os angulare, proc.
retroarticularis), and medial process (os articulare, proc. medialis mandibulae): absent
(0); weak concavity (1); strong concavity (2). This character is easiest to evaluate in
ventral view. This character is non-comparable in taxa lacking a retroarticular process.
Ordered.
111. Atlas (atlas), proc. ventralis: absent or sligthly developed (0); well developed, high and
prominent ridge on the dorsal surface of the arcus atlantis (1).
112. Transition to free cervicothoracic ribs (costae incompletae) arrives at: 13th cervical
vertebrae (vertebrae cervicodorsales): (0); 14th cervical vertebrae (1); 15th cervical
vertebrae (2). Ordered.
113. Cervical vertebrae (vertebrae cervicales), elongated dorsal process (processus spinosus)
on the sixth cervical vertebra: absent (0); present (1).
114. Cervical vertebrae (vertebrae cervicales), transverse processes (processus transversus) in
last five cervical vertebrae: not elongated laterally (0); greatly elongated laterally (1).
115. Cervical vertebrae (vertebrae cervicales), transverse processes (processus transversus)
of vertebrae 12-13: laterally oriented (0); deflected dorsally (1).
116. Thoracic vertebrae (vertebrae thoracicae), posteriormost vertebrae: heterocoelous (0);
weakly opisthocoelous; (1); strongly opisthocoelous (2). Ordered.
*117. Synsacrum (synsacrum), number of incorporated vertebrae: eleven (0); twelve (1);
thirteen (2); fourteen (3).
118. Caudal vertebrae (vertebrae caudales): seven (0), eight (1), nine (2). Ordered.
119. Ribs, uncinate processes (costae, proc. uncinatus): elongate, narrow (0), wide, spatulate
(1), wide, bifurcated (2).
120. Sternum, external spine (sternum, spina externa rostri): absent (0); present (1).
121. Sternum, furcular facet (sternum, facies articularis furculae) projects as a distinctive
process: absent (0); present (1).
*122. Sternum, coracoid facets (sternum, sulcus articularis coracoideus): meet or overlap one
another at midline (0); separated by wide non-articulatory surface (1).
*123. Sternum, labrum internum: continues as sharp ridge onto the base of the external spine
(spina externa) (0); fades away without continuing onto the base (1).
124. Clavicle, furcular process (clavicula, apophysis furculae): absent or low blade-like
process (0); knob-like process (1); long process (2).
125. Scapula, blade, caudal half (scapula, corpus scapulae, extremitas caudalis): blade-like
(0); expanded and paddle-shaped (1).
126. Coracoid, medial margin, (coracoideum, margo medialis) coracoidal fenestra: complete
(0); incomplete (1); absent (2).
127. Coracoid, foramen nervi supracoracoidei: absent (0), present (1).
128. Coracoid, sternal end (coracoideum, extremitas sternalis coracoidei): greatly expanded
(0); moderate expansion (1).
129. Coracoid, sternal end (coracoideum, extremitas sternalis coracoidei): convex (0)
concave (1), flat (2).
130. Forelimbs (ossa alae), flattened: absent (0); present (1).
131. Humerus, head (caput humeri): very developed and reniform, continuous with
tubercucum dorsale: absent (0); present (1).
132. Humerus, head (caput humeri) in posterior view: apex of humeral head located near
midline (0); humeral head slopes so that apex of humeral head located ventrally (1).
133. Humerus, incisura captius: essentially confluent with sulcus transversus (0); clearly
separated from sulcus transversus (1).
134. Humerus, pit for ligament insertion on proximal surface adjacent to head (see Fig. 8 in
reference 2): absent or very shallow (0); deep (1).
*135. Humerus, orientation of intumenscenita humeri and tuberculum ventrale:
intumenscentia projects ventrally from shaft, tuberculum oriented posteriorly (0);
intumenscentia projects ventrally from shaft, tuberculum oriented ventrally (1);
intumenscentia projected more anteroventrally (so as to be partially obscured in posterior
view), tuberculum oriented anteroventrally (2).
136. Humerus, tricipital fossa (humerus, fossa tricipitalis), aspect: small with penetrating
pneumatic foramina (0); moderate fossa without pneumatic foramen (1); deep fossa
without pneumatic foramen.
137. Humerus, tricipital fossa (humerus, fossa tricipitalis), subdivided into cavities: single
(0); bipartite (1).
*138. Humerus, deltoid crest, impression for attachment of pectoral muscle (humerus, crista
deltopectoralis, impressio m. pectoralis): superficial poorly-defined groove (0); shallow,
well-defined oblong fossa (1); deep, well-defined oblong fossa (2). Ordered
139. Humerous, imperssio insertii m. supracoracoideus : small, semicircular scar (0); greatly
elongated with long axis parallel to main axis of humeral shaft (1), greatly elongated
with long axis oblique to long axis of shaft (2).
140. Humerus, imperssio insertii m. supracoracoideus and m. latissimus dorsi: separated by a
wide gap (0); separated by small gap or confluent (1).
141. Humerus, proximal margin of tricipital fossa ( fossa tricipitalis): weak projection (0);
projects so as to be well-exposed in proximal view (1).
142. Humerus, shaft, dorsoventral width: shaft thins or maintains width distally (0); shaft
widens distally (1).
*143. Humerus, nutrient foramen (foramen nutricum): situated on ventral face of shaft (0)
situated on anterior face of shaft (1).
*144. Humerus, anterior face of shaft (humerus, facies cranialis) elongate depression near
ventral margin: absent (0); present (1). This depression is present only in certain fossil
taxa and is not to be confused with the vascular depression that runs distally from the
ventral to the dorsal margin of the shaft in all penguins.
145. Humerus, shaft, sigmoid curvature: absent or weak (0); strong (1).
146. Humerus, development of dorsal supracondylar process (humerus, proc. supracondylar
dorsalis): absent (0); compact tubercle (1); very long process (2).
*147. Humerus, demarcation of scapulatriceps groove (sulcus scapulotricipitalis): not
demarcated (0); passage a well-marked groove (1); development of trochlear process for
articulation with os sesamoideum m. scapulotricipitis (2). Ordered.
*148. Humerus, anterior trochlear ridge: does not project distal to the middle and posterior
trochlear processes (0), projects distal to the middle and posterior trochlear processes (1).
149. Humerus, posterior trochlear process: extends beyond the humeral shaft (0); does not
extend beyond the humeral shaft (1).
150. Humerus, angle between main axis of shaft and tangent of radial and ulnar condyles
(condylus dorsalis humeri et condylus ventralis humeri): less than 45 degrees (0); more
than 45 degrees (1); nearly 90 degrees (2).
151. Humerus, ulnar and radial condyles (humerus, condylus dorsalis humeri et condylus
ventralis humeri): ulnar condyle projected and rounded (0); ulnar condyle flattened (1).
*152. Humerus, shelf adjacent to ulnar condyle (condylus ventralis): large, ratio of condyle
width: shelf width >1.3 (0); moderate, ratio of condyle width:shelf width 1.3-2.0 (1);
greatly reduced, less than half condyle width (2).
153. Ulna, olecranon and posterior border (ulna, olecranon et margo caudalis): border forms
smooth curve with apex located one fourth of length to distal end (0) well-developed tablike projection arises proximally, very close to humeral articulation (1) acute projection,
distally displaced from humeral facet (2); rounded (3).
154. Ulna, distinct process extending toward sulcus humerotricipitalis of humerus: absent (0),
present (1).
*155. Carpometacarpus, processus pisiformis: well-projected round tubercle (0); reduced to a
low ridge (1).
156.Carpometacarpus, distal facet on metacarpal I (os metacarpale aluaris): absent (0);
present (1).
*157. Carpometacarpus, metacarpal II (os metacarpale majus), distinct anterior bowing:
absent (0); present (1).
*158. Carpometacarpus, extension of metacarpals II and III (os metacarpale majus et minus):
subequal (0); metacarpal III projects markedly distal of metacarpal II.
*159. Carpometacarpus, metacarpal III, distal articular surface (fascies articularis digitalis
major): wedge shaped or broadens anteriorly in distal view (0), slightly depressed ovoid
surface (1).
160. Phalanges of manus, phalange digit III (ossa digitorum manus, phalanx digiti minoris),
proximal process: absent (0); present (1).
*161. Phalanges of manus, relative length of phalanx digiti minoris and first phalanax digiti
minoris: phalanx digiti minoris much shorter (0); subequal (1)
162. Phalanges of manus (ossa digitorum manus, phalanges), length relative to
carpometacarpus: long (0); short (1)
163. Fusion of illia to synsacrum: unfused (0); partially fused (1); well-fused (2).
164. Pelvis, size of ilio-ischiatic fenestra (foramen ilioischiadicum) in relation to acetabulum
(foramen acetabuli): smaller (0); similar or larger (1).
165. Pelvis, ischio-pubic fenestra (fenestra ischiopubica): very wide and closed at its caudal
end (0); slit-like and open at its caudal end (1).
166. Ischium, most caudal extent in relation to postacetabular ilium (ala postacetabularis illi):
ischium shorter than ilium (0); ischium projects slightly beyond the ilium (1); ischium
produced far caudal to ilium (2).
167. Femur, patella (femur, patella), sulcus m. ambiens: shallow groove (0); deep groove (1);
perforated (2).
168. Tibiotarsus, patellar crest (tibiotarsus, crista patellaris): greatly enlarged (0); slightly
developed (1).
*169. Tibiotarsus, shaft, anteroposterior flattening: weak, midshaft anteroposterior depth
greater than 75% mediolateral width (0) ; strong, midshaft anteroposterior depth equal to
or less than 75% mediolateral width (1).
170. Tarsometatarsus (tarsometatarsus), elongation index (proximodistal length / mediolateral
width at proximal end): slender, EI>3 (0); shortened, 2.5<EI < 3 (1), greatly shortened EI
< 2.5 (2). Ordered.
171 Tarsometatarsus, medial margin (tarsometaasus, margo medialis), pronounced convexity:
absent (0), present (1).
172. Tarsometatarsus, intermediate hypotarsal crest (crista intermediae hypotarsi): nondistinct (0); distinct (1).
173. Tarsometatarsus, sulcus longitudialis dorsalis medialis: absent or barely perceptible (0);
shallow groove (1); deep groove (2). Ordered.
*174. Tarsometatarsus, os metatarsale IV: distal end projects laterally (0); straight (1), distal
end deflected medially (2). A new state is added here to accommodate the shape in
Archaeospheniscus lopdelli.
175. Tarsometatarsus, foramem vascularia proximalia medialis opening on fossa para
hypotarsalis medialis: absent (0); present (1).
176. Tarsometatarsus, proximal vascular foramina on plantar surface: medial foramen
(foramen vasculare proximale mediale) present, lateral foramen (foramen vasculare
proximale laterale) absent or vestigal (0); both foramina present (1); lateral foramen
present, medial foramen absent or vestigal (2).
177. Tarsometarsus, foramen vasculare distale: present, separated from incisura
intertrochlearis lateralis by osseus bridge (0); present, open distally (1); absent (2).
Ordered.
178. Tarsometatarsus, hypotarsus, tendinal canals (tarsometatarsus, hypotarsus, canales
hypotarsi): present (0); absent (1).
MYOLOGY
179. M. latissimus dorsi, pars cranialis, accesory slip: absent (0); present (1).
180. M. latissimus dorsi, pars cranialis and pars caudalis: separated (0); fused (1).
181. M. latissimus dorsi, pars metapagialis, development: wide (0); intermediate (1); narrow
(2). Ordered.
182. M. serratus profundus, cranial fascicle: absent (0); present (1);
183 M. deltoideus, pars propatagialis, subdivision in superficial and deep layers: undivided
(0); divided (1).
184. M. deltoideus, pars major: triangular or fan-shaped (0); strap-shaped (1).
185. M. deltoideus, pars major, caput caudale: short (0); intermediate (1); long (2). Ordered.
186. M. deltoideus, pars minor, origin on the clavicular articulation of the coracoid: absent
(0); present (1).
187. M. ulnometacarpalis ventralis: absent (0); present (1).
188. M. iliotrochantericus caudalis: narrow (0); wide (1).
189. M. iliofemoralis, origin: tendinous (0); mostly tendinous (1); mostly fleshy (2); totally
fleshy (3). Ordered.
190. M. flexor perforatus digitis IV, rami II-III: free (0); fused (1).
191. M. flexor perforatus digitis IV, rami I-IV: free (0); fused (1).
192. M. flexor perforatus digitis IV, insertion of middle rami: on phalanx 3 (0); on phalanx 4
(1).
193. M. latissimus dorsi, pars caudalis, additional origin from dorsal process of vertebrae
(spinous process of Schreiweis, 1982): absent (0); present (1).
DIGESTIVE TRACT
194. Mouth, oral mucosa (bucca, tunica mucosa oris), buccal papillae group on the medial
surface of the lower jaw (ramus mandibularis) at the level of the rictus: small number of
rudimentary papillae with no clear arrangement (0); two clear rows of short conical
papillae (1); large, elongated papillae with no clear arrangement (2).
References
1. Bertelli S, Giannini NP (2005) Cladistics 21:209–239.
2. Ksepka DT, Bertelli S, Giannini NP (2006) Cladistics 22:412–441.
3. Giannini P, Bertelli S (2004) Auk 121:422–434.
4. Marples BJ (1952) N Z Geol Surv Paleontol Bull 20:1–66.
5. Simpson GG (1946) Bull Am Mus Nat Hist 87:7–99.
6. Clarke JA, Olivero EB, Puerta P (2003) Am Mus Novit 3423:1–18.
7. Mayr G (2004) J Zool Syst Evol Res 43:61–71.
8. Goloboff PA (1999) Cladistics 15:415–428.
9. Williams TD (1995) The Penguins (Oxford University Press, Oxford).
10. Ronquist F (1997) Syst Biol 46:195–203.
11. Baker AJ, Pereira SL, Haddrath OP, Edge K-A (2006) Proc R Soc London Ser B 212:11–
17.
12. Cooper A, Penny D (1997) Science 275:1109–1113.
13. Patterson AM, Wallis GP, Gray RD (1995) Evolution (Lawrence, Kans) 49:974–989.
14. Slack KE, Jones CM, Ando T, Harrison GL, Fordyce RE, Arnason U, Penny D (2006)
Mol Biol Evol 23:1144–1155.
15. Van Tuinen M, Sibley CG, Hedges SB (2000) Mol Biol Evol 17:451–457.
16. Nunn GB, Cooper J, Jouventin J, Robertson CJR, Robertson GG (1996) Auk 113:784–
801.
17. Nunn GB, Stanley SE (1998) Mol Biol Evol 15:1360–1371.
18. Stanley SE, Harrison RG (1999) Mol Biol Evol 16:1575–1585.
19. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) PLoS Biol 2:1657–1663.
20. Myrcha A, Jadwiszczak P, Tambussi CP, Noriega JI, Gazdzicki A, Tatur A, del Valle RA
(2002) Polish Polar Res 23:5–46.
21. Simpson GG (1971) Bull Am Mus Nat Hist 144:319–378.
22. Fordyce RE, Jones CM (1990) in Penguin Biology, eds Davis LS, Darby JT (Academic,
San Diego), pp 419–446.
23. Marples BJ (1960) Records Canterbury Mus 7:185–195.
24. Simpson GG (1981) Ameghiniana 18:266–272.
25. Simpson GG (1971) Records Canterbury Mus 9:159–182.
26. Simpson GG (1972) Am Mus Novit 2488:1–37.
27. Acosta Hospitaleche C, Stucchi M. (2005) Revista de la Sociedad Española de
Paleontología 20:1–15.
28. Stucchi M, Urbina M, Giraldo A (2003) Bol Instituto Francés de Estudios Andinos
32:361–375.
29. Stucchi M (2002) Bol Soc Geol Perú 94:19–26.
SI Data Set. Morphological Data Matrix
Numbered entries refer to the character states listed in SI Appendix . ?, missing data; -, nonapplicable. These two symbols are treated identically in analysis.
Taxon
Gavia immer
Gavia stellata
Diomedea exulans
Diomedea melanophrys
Phoebetria palpebrata
Macronectes giganteus
Daption capense
Procellaria aequinoctialis
Puffinus griseus
Pterodroma incerta
Oceanodroma leucorhoa
Oceanites oceanicus
Pachyptila desolata
Pelecanoides urinatrix
Aptenodytes forsteri
Aptenodytes patagonicus
Pygoscelis antarctica
Pygoscelis papua
Pygoscelis adeliae
Megadyptes antipodes
Eudyptes chrysocome moseleyi
Eudyptes chrysocome chrysocome
Eudyptes chrysolophus
Eudyptes schlegeli
Eudyptes pachyrhynchus
Eudyptes robustus
Eudyptes sclateri
Eudyptula minor
Spheniscus demersus
Spheniscus humboldti
Spheniscus magellanicus
Spheniscus mendiculus
Spheniscus urbinai
Spheniscus megaramphus
Marplesornis novaezealandiae
Palaeospheniscus patagonicus
Eeretiscus tonnii
Platydyptes novaezealandiae
Platdyptes marplesi
Platydyptes amiesi
Paraptenodytes antarcticus
Archaeospheniscus lowei
Archaeospheniscus lopdelli
Pachydyptes ponderosus
Icadyptes salasi
Palaeeudyptes sp. OM C.48:73-81
Palaeeudyptes sp. OM C.47:25
Palaeeudyptes sp. OM C.47:23
Palaeeudyptes klekowskii
Palaeeudyptes gunnari
Anthropornis nordenskjoeldi
Anthropornis grandis
Delphinornis larseni
Mesetaornis polaris
Marambiornis exilis
Perudyptes devriesi
Waimanu tuatahi
Waimanu manneringi
Character
1 2
?
?
0
0
?
?
3
0
3
0
3
0
3
0
3
0
3
0
3
0
3
0
3
0
3
0
3
0
0
0
0
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
0
1
1
2
1
2
1
2
1
2
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
3
0
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
4
?
1
?
0
0
1
1
0
0
0
0
0
0
0
2
1
2
2
3
1
1
1
1
1
1
1
1
1
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
5
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
2
2
2
2
2
2
2
2
2
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
6
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
7
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
8
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
2
2
0
2
2
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
9
?
0
?
4
0
3
0
5
0
0
0
0
6
0
0
0
0
1
1
2
1
1
1
1
1
1
1
0
0
0
0
3
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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10
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
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1
1
1
1
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?
?
?
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?
?
?
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11
?
0
?
2
0
3
0
4
0
0
0
0
5
0
0
0
0
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
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?
?
?
?
?
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?
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?
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12
?
0
?
2
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
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?
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13
?
0
?
1
0
2
0
3
0
0
0
0
4
0
0
0
0
0
0
1
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
?
?
?
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?
?
?
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?
14
?
0/1/2/3
?
0
0
2
0
?
0
0
0
0
3
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
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?
?
?
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?
?
?
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?
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15
?
0
?
0
0
3
0
0
0
0
0
0
4
0
0
0
0
1
1
0
2
2
2
2
2
2
2
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
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?
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?
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16
?
0
?
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
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1
0
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?
?
?
?
?
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?
?
?
?
?
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?
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?
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?
?
?
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?
?
?
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17
?
0
?
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
0
0
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0
0
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0
?
?
?
?
?
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?
?
?
?
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?
?
?
?
?
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?
?
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18
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
19
?
2
?
0
0
5
0
0
0
0
0
0
0
0
0
0
2
1
4
3
2
2
2
2
6
6
0
5
0
1
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
?
?
?
?
?
?
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20
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
21
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
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?
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?
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?
?
?
?
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?
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?
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22
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
23
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
24
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
?
?
?
?
?
25
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
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1
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1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
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?
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?
26
?
?
0
0
0
0
0
1
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
27
?
?
0
0
0
0
0
0
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
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?
?
?
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?
?
?
?
28
?
?
1
1
1
1
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
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29
?
?
2
2
2
2
1
1
0
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
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?
30
?
?
1
1
2
2
1
1
0
?
?
?
?
?
?
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?
?
?
?
?
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?
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31
?
?
0
0
1
1
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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32
?
?
0
0
0
0
1
0
2
2
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
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33
?
?
0
0
1
0
0
2
0
0
0
1
0
0
0
3
0
0
0
0
?
?
?
?
?
?
?
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?
?
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?
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34
?
?
0
0
0
0
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1
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0
0
0
0
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0
1
1
1
1
?
?
?
?
?
?
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?
?
?
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?
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35
?
?
0
0
0
1
1
0
0
0
0
0
0
0
0
0
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0
?
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36
?
?
0
0
0
0
0
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0
0
0
0
0
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0
3
2
2
1
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?
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?
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37
?
?
0
0
0
0
0
0
0
0
0
0
0
0
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0
2
3
1
3
?
?
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38
?
?
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
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39
?
?
0
0
4
0
0
2
0
0
0
1
0
0
0
1
0
3
0
3
?
?
?
?
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?
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?
?
?
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?
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?
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?
40
?
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
3
2
?
?
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41
?
?
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
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?
?
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?
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?
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?
?
42
?
?
1
1
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
?
?
?
?
?
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?
?
?
?
?
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?
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?
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?
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43
?
?
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
?
?
?
?
?
?
?
?
?
44
?
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
?
?
?
?
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?
?
?
?
?
?
?
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?
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?
?
?
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45
?
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
?
?
?
?
?
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?
?
?
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?
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?
?
?
?
?
?
?
?
?
46
?
?
0
0
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
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?
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?
?
?
?
?
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?
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?
?
?
?
?
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47
?
?
1
1
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
60 61
?
?
0
1
?
?
0
0
0
0
0
3
0
0
0
1
0
0
0
?
0
0
0
1
0 0/1
0
0
1
0
1
1
0
0
0
0
0
0
0
1
0
2
0
2
0
2
0
2
0
2
0
2
0
2
0
1
0
2
0
?
0
?
0
?
?
?
?
?
?
?
?
?
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?
?
?
?
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?
?
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?
?
?
?
?
?
?
?
?
?
?
?
?
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?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
62
?
1
?
0
0
3
0
1
0
?
0
1
0
0
0
1
0
2
1
1
2
2
2
2
2
2
2
2
2
2
2
2
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
63
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
64
?
0
?
3
3
0/1/2/3
0
0
1
1
0
0
4
4
0
0
1
2
1
1
1
1
1
1
1
1
1
3
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
65
?
0
?
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
66
?
0
?
0
0
0
1
1
1
1
1
1
1
1
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
67
?
0
?
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
68
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
69
?
2
?
2
2
2
2
1
1
1
1
1
1
1
0
0
2
2
2
2
2
2
2
2
2
2
2
1
1
1
1
1
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
70
?
0
?
0
2
2
0
1
1
1
1
1
1
1
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
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?
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?
?
?
?
?
?
?
?
?
?
71
?
0
?
0
0
0
0
0
0
0
0
0
0
0
2
2
2
2
2
0
2
2
2
2
2
2
2
1
1
?
2
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
72
?
0
?
0
0
0
0
0
0
0
0
0
0
0
1
1
2
2
2
0
0
0
0
0
0
0
0
0
0
0
0
0
?
?
?
?
?
?
?
?
?
?
?
?
?
?
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130
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131
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132
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133 134
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135
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136
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137
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138
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139
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140
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141
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142 143
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148 149
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182 183
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