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The Hesperornithiformes: A Review of the Diversity, Distribution, and Ecology of the Earliest Diving Birds

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The Hesperornithiformes (sometimes referred to as Hesperornithes) are the first known birds to have adapted to a fully aquatic lifestyle, appearing in the fossil record as flightless, foot-propelled divers in the early Late Cretaceous. Their known fossil record—broadly distributed across the Northern Hemisphere—shows a relatively rapid diversification into a wide range of body sizes and degrees of adaptation to the water, from the small Enaliornis and Pasquiaornis with lesser degrees of diving specialization to the large Hesperornis with extreme morphological specializations. Paleontologists have been studying these birds for over 150 years, dating back to the “Bone Wars” between Marsh and Cope, and as such have a long history of naming, and renaming, taxa. More recent work has focused to varying degrees on the evolutionary relationships, functional morphology, and histology of the group, but there are many opportunities remaining for better understanding these birds. Broad-scale taxonomic evaluations of the more than 20 known species, additional histological work, and the incorporation of digital visualization tools such as computed tomography scans can all add significantly to our understanding of these birds.
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Citation: Bell, A.; Chiappe, L.M. The
Hesperornithiformes: A Review of
the Diversity, Distribution, and
Ecology of the Earliest Diving Birds.
Diversity 2022,14, 267. https://
doi.org/10.3390/d14040267
Academic Editors: Eric Buffetaut
and Delphine Angst
Received: 23 February 2022
Accepted: 25 March 2022
Published: 1 April 2022
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diversity
Review
The Hesperornithiformes: A Review of the Diversity,
Distribution, and Ecology of the Earliest Diving Birds
Alyssa Bell * and Luis M. Chiappe
Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition Boulevard,
Los Angeles, CA 90007, USA; lchiappe@nhm.org
*Correspondence: abell@nhm.org
Abstract:
The Hesperornithiformes (sometimes referred to as Hesperornithes) are the first known birds to
have adapted to a fully aquatic lifestyle, appearing in the fossil record as flightless,
foot-propelled
divers
in the early Late Cretaceous. Their known fossil record—broadly distributed across the Northern
Hemisphere—shows a relatively rapid diversification into a wide range of body sizes and degrees
of adaptation to the water, from the small Enaliornis and Pasquiaornis with lesser degrees of diving
specialization to the large Hesperornis with extreme morphological specializations. Paleontologists
have been studying these birds for over 150 years, dating back to the “Bone Wars” between Marsh
and Cope, and as such have a long history of naming, and renaming, taxa. More recent work has
focused to varying degrees on the evolutionary relationships, functional morphology, and histology
of the group, but there are many opportunities remaining for better understanding these birds.
Broad-scale taxonomic evaluations of the more than 20 known species, additional histological work,
and the incorporation of digital visualization tools such as computed tomography scans can all add
significantly to our understanding of these birds.
Keywords: Hesperornithiformes; Aves; Mesozoic birds; evolution; paleoecology; diving birds
1. Introduction
In the winter of 1870, Othniel Charles Marsh discovered the distal-most end of a
tibiotarsus of a large bird in Cretaceous (Coniacian-early Campanian) marine sediments
near the Smoky Hill River in western Kansas (specimen 1205 at the Yale Peabody Museum
[YPM]) [
1
]. This unremarkable specimen was the first look at a remarkable group of
extinct animals, the first dinosaurs to adapt to a fully aquatic lifestyle and the earliest
group of birds to swim away from the ability to fly. On second and third expeditions to
western Kansas, in June of 1871 and the fall of 1872, Marsh discovered a more complete
specimen (YPM 1200) of the same species as well as fossils of other ancient birds, one of
which was nearly complete (YPM 1207) [
1
]. In 1872, as the infamous “Bone Wars”—an
ignominious chapter in American paleontology—were just beginning, Marsh published
his first work on these specimens [
2
]. Marsh designated the material as Hesperornis regalis,
a large swimming bird that he interpreted as being most closely related to modern loons,
albeit with significant differences from “all other known birds, recent and extinct” [
3
] (p.
361), and later assigned it to the Natatores [
4
], a paraphyletic group used at the time to unite
modern swimming birds that has since been abandoned. Over subsequent years, Marsh sent
numerous expeditions back to the Smoky Hill River in Kansas, resulting in the collection
of hundreds of specimens of birds belonging to a group termed the Odontornithes, which
Marsh erected for Ichthyornis and Apatornis [
5
]. Later, Marsh added the coeval Hesperornis
to the Odontornithes on the basis of the presence of teeth in the jaws [
6
]. Marsh would go
on to describe a second species of Hesperornis, H. gracilus, and three other related genera,
Baptornis advenus,Coniornis altus, and Lestornis crassipes [
7
], although the latter two are now
assigned to Hesperornis.
Diversity 2022,14, 267. https://doi.org/10.3390/d14040267 https://www.mdpi.com/journal/diversity
Diversity 2022,14, 267 2 of 28
At the same time that Marsh was working on the North American toothed birds, Harry
Seeley [
8
] was describing a group of small fossil birds from the Upper Cretaceous (Cenoma-
nian) Cambridge Greensand in England from material discovered by Lucas Barrett in 1858
and briefly discussed by Lyell a year later [
9
]. Unlike Marsh’s larger birds that included
well-preserved, articulated specimens, the two species identified by Seeley—Enaliornis
barretti and E. sedgewicki—were entirely disarticulated and heavily eroded, as part of a
reworked deposit [
8
]. However, like the fossils Marsh was discovering, these British fossils
were also abundant, with dozens of isolated bones available for study in the Woodwardian
Museum (now the Woodwardian Collection of the Sedgewick Museum) in Cambridge [
8
].
Seeley did not recover any specimens with teeth. Furthermore, he deemed Marsh’s reliance
on teeth for designation of the Odontornithes to be unsupported, in light of the variability
of teeth across modern mammals and reptiles [
8
], a view that was upheld by Furbringer [
9
]
in 1888 when he established the order Hesperornithiformes (now phylogenetically defined
as all taxa more closely related to Hesperornis regalis than to Neornithes or modern birds),
removing Hesperornis and Baptornis from Odontornithes. Seeley noted numerous similari-
ties between Enaliornis and modern loons, and so referred Enaliornis to the Natatores [
8
], as
Marsh had originally done with Hesperornis. The placement of Enaliornis within the Hes-
perornithiformes was first proposed by Lydekker [
10
] a few years after the erection of this
clade, which was later supported by Wetmore [
11
], Storer [
12
], Martin and Tate [
13
], and
others. Our modern understanding of hesperornithiform phylogenetics places them within
the Ornithurae and very close to the divergence of modern birds, Neornithes (
Figure 1
).
Thus, by the end of the 19th century the Hesperornithiformes were the most diverse lineage
of Cretaceous birds known, with a wide geographic and stratigraphic distribution and
ranging in size from a bird the size of a grebe to birds as much as 1.5 m long.
From these early studies, our modern understanding of the Hesperornithiformes has
expanded to over 20 species from across Laurasia, identified from marine, transitional, and
continental deposits (Figure 2). Interestingly, the fossil collections amassed at the Peabody
Museum in Yale University by Marsh and at the Sedgewick Museum in Cambridge University
remain the most abundant in terms of number of specimens, rivaled only by the Carrot River
material of Pasquiaornis collected in the latter part of the twentieth century [1416].
Studies over the past 150+ years have explored the evolutionary relationships and
trajectories, biomechanics, ecology, life history, and biogeography of these incredible birds,
as well as continually identifying new families, genera, and species. This review will
provide an overview of this body of research, summarizing both where we are today in
our understanding of the evolution and biology of these birds and how we got there, and
highlight areas for potential future research.
2. General Anatomy
From the first studies of specimens by both Marsh and Seeley, the highly modified
bauplan of these birds was recognized as a significant chapter in avian adaptation. This
consists of a streamlined body with an elongated skull and neck, heavily reduced forelimb,
and dramatically robust hindlimb (Figure 3). In superficial form, it is easy to see how
early researchers, and some not-so-early researchers, identified the similarities to modern
foot-propelled diving birds such as loons and concluded that these birds were part of
the modern diving lineage (e.g., [
3
,
8
,
17
19
]). However, this view fails to account for the
strong convergence found among modern diving bird lineages, as we now recognize foot-
propelled diving to have evolved independently at least four times among modern birds
(i.e., loons, grebes, diving ducks, and cormorants), and that even such morphologically
similar birds as loons and grebes are not closely related at all [
20
,
21
]. In fact, the results of
a comprehensive morphometric analysis of hesperornithiforms and modern diving birds
showed that the former rarely share morphospace with loons and grebes, and that instead,
they overlap more in morphospace with cormorants and diving ducks [22].
Diversity 2022,14, 267 3 of 28
Diversity 2022, 14, x FOR PEER REVIEW 3 of 28
Figure 1. Phylogenetic tree of birds, after Bell and Chiappe [17] and Tanaka et al. [18]. Arrows show
the alternative placement of Enaliornis and Pasquiaornis recovered by Tanaka et al. [18].
Figure 1.
Phylogenetic tree of birds, after Bell and Chiappe [
23
] and Tanaka et al. [
24
]. Arrows show
the alternative placement of Enaliornis and Pasquiaornis recovered by Tanaka et al. [24].
The skull of hesperornithiforms is elongate, with a long rostrum similar to that seen
in modern foot-propelled diving birds. This elongation is due primarily to the length of
the premaxilla, as in modern birds, which makes up nearly half the length of the rostrum
in Hesperornis [
25
]. This is unlike more stemward, longirostrine Mesozoic birds (e.g.,
Longipteryx,Rapaxavis,Dingavis), where elongation of the rostrum is due in part to an
extended maxilla [
26
]. Within hesperornithiforms, there appears to be variation in the
degree of elongation of the skull. Enaliornis, the most basal hesperornithiform currently
known [
23
], has a proportionally shorter skull than that of hesperornithids (Parahesperornis
and Hesperornis). This is seen in three different regions of the skull: the parietals and
temporal fenestrae, the frontals, and the portion of the rostrum rostral to the nares [
25
].
Furthermore, these regions of the skull are proportionally shorter in Parahesperornis than in
Hesperornis, implying potential ecological specializations (i.e., niche partioning) among
these likely coeval and sympatric birds [25].
The dentary and maxillae of hesperornithiforms bear small recurved teeth set in a
groove (Figure 4). While today we recognize a wide diversity of tooth retention patterns
across Mesozoic birds [
26
,
27
], when first discovered by Marsh, this feature was strik-
ing. The retention of teeth in birds is a conserved character with similar molecular and
developmental mechanisms inherited from their nonavian reptilian ancestors [28].
Marsh’s [
3
] first description of the teeth of Hesperornis noted that they were not
set in true sockets (i.e., thecodont implantation), but were instead separated by slight
projections from the sides of the groove in which they were set in the jaws. While dentary
Diversity 2022,14, 267 4 of 28
fragments assigned to Pasquiaornis have been described as having similar tooth implantation
in a groove with incomplete sockets [
15
], published images of some specimens appear
to show much more extensive socket development than the slight projections found in
hesperornithids (Figure 4).
Diversity 2022, 14, x FOR PEER REVIEW 4 of 28
Figure 2. Distribution of hesperornithiform specimens across the Northern Hemisphere, mapped
on paleogeographic reconstructions of the Cretaceous (after [19]): (A) Maastrichtian; (B) Campa-
nian; (C) Coniacian to Santonian; (D) Cenomanian [19]. After Bell and Chiappe [20].
2. General Anatomy
From the first studies of specimens by both Marsh and Seeley, the highly modified
bauplan of these birds was recognized as a significant chapter in avian adaptation. This
consists of a streamlined body with an elongated skull and neck, heavily reduced fore-
limb, and dramatically robust hindlimb (Figure 3). In superficial form, it is easy to see how
early researchers, and some not-so-early researchers, identified the similarities to modern
foot-propelled diving birds such as loons and concluded that these birds were part of the
modern diving lineage (e.g., [3,8,2123]). However, this view fails to account for the strong
convergence found among modern diving bird lineages, as we now recognize foot-pro-
pelled diving to have evolved independently at least four times among modern birds (i.e.,
loons, grebes, diving ducks, and cormorants), and that even such morphologically similar
Figure 2.
Distribution of hesperornithiform specimens across the Northern Hemisphere, mapped on
paleogeographic reconstructions of the Cretaceous (after [
29
]): (
A
) Maastrichtian; (
B
) Campanian;
(C) Coniacian to Santonian; (D) Cenomanian [19]. After Bell and Chiappe [25].
More recent work exploring the nature of the teeth in Hesperornis via synchrotron
imaging found that they have fully thecodont-style root attachments but that secondary
loss of periodontal ligaments led to the implantation of the teeth in a groove [
30
]. While the
retention of teeth in the jaw is plesiomorphic in Hesperornis, the emplacement of the teeth
is an autapomorphy, uniquely evolved in hesperornithiforms and not seen in other toothed
birds such as Archaeopteryx [
31
], Ichthyornis [
32
], other toothed ornithuromorphs [
33
], or
toothed enantiornithines [
26
,
34
]. The enamel on Hesperornis teeth is thin and simple in
Diversity 2022,14, 267 5 of 28
structure, with fine fluted ornamentation [
35
] formed by thickened ridges of enamel [
30
].
The teeth have a relatively high extension rate (a measure of how fast the tooth growths in
height) in the dentine compared to that of nonavian dinosaurs, as calculated from dentine
increment lines preserved in the teeth [
30
]. Tooth replacement involved a resorption
pit in the root of the functional tooth, leading to lingual replacement with a calculated
mean frequency of 66 days [
30
]. The teeth of hesperornithiforms are unicuspid and highly
recurved, with a hooked shape in side view [
20
,
30
]. The teeth exhibit a gradient in curvature,
with the mesial teeth more recurved than the distal teeth [
1
], more than is seen in other
Mesozoic birds [36]. Teeth are absent in the premaxillae, as in Ichthyornis and some other
early ornithuromorphs (e.g., Gansus,Iteravis), while the dentary and maxilla are toothed.
Diversity 2022, 14, x FOR PEER REVIEW 5 of 28
birds as loons and grebes are not closely related at all [24,25]. In fact, the results of a com-
prehensive morphometric analysis of hesperornithiforms and modern diving birds
showed that the former rarely share morphospace with loons and grebes, and that instead,
they overlap more in morphospace with cormorants and diving ducks [26].
Figure 3. The basic bauplan of a hesperornithiform bird, based off Hesperornis regalis. While the de-
gree of reduction of the forelimb and hindlimb proportions vary across taxa, this overall morphol-
ogycharacterized by an elongated skull and neck, abbreviated forelimbs, and robust hindlimb
with a long pelvisis typical of all hesperornithiforms. Forelimb girdle shown in blue and hindlimb
girdle shown in green.
The skull of hesperornithiforms is elongate, with a long rostrum similar to that seen
in modern foot-propelled diving birds. This elongation is due primarily to the length of
the premaxilla, as in modern birds, which makes up nearly half the length of the rostrum
in Hesperornis [20]. This is unlike more stemward, longirostrine Mesozoic birds (e.g., Long-
ipteryx, Rapaxavis, Dingavis), where elongation of the rostrum is due in part to an extended
maxilla [27]. Within hesperornithiforms, there appears to be variation in the degree of
elongation of the skull. Enaliornis, the most basal hesperornithiform currently known [28],
has a proportionally shorter skull than that of hesperornithids (Parahesperornis and Hes-
perornis). This is seen in three different regions of the skull: the parietals and temporal
fenestrae, the frontals, and the portion of the rostrum rostral to the nares [19]. Further-
more, these regions of the skull are proportionally shorter in Parahesperornis than in Hes-
perornis, implying potential ecological specializations (i.e., niche partioning) among these
likely coeval and sympatric birds [19].
The dentary and maxillae of hesperornithiforms bear small recurved teeth set in a
groove (Figure 4). While today we recognize a wide diversity of tooth retention patterns
across Mesozoic birds [29,30], when first discovered by Marsh, this feature was striking.
The retention of teeth in birds is a conserved character with similar molecular and devel-
opmental mechanisms inherited from their nonavian reptilian ancestors [31]. Marsh’s [3]
first description of the teeth of Hesperornis noted that they were not set in true sockets (i.e.,
thecodont implantation), but were instead separated by slight projections from the sides
of the groove in which they were set in the jaws. While dentary fragments assigned to
Pasquiaornis have been described as having similar tooth implantation in a groove with
incomplete sockets [15], published images of some specimens appear to show much more
extensive socket development than the slight projections found in hesperornithids (Figure
4).
Figure 3.
The basic bauplan of a hesperornithiform bird, based off Hesperornis regalis. While the degree
of reduction of the forelimb and hindlimb proportions vary across taxa, this overall morphology—
characterized by an elongated skull and neck, abbreviated forelimbs, and robust hindlimb with a
long pelvis—is typical of all hesperornithiforms. Forelimb girdle shown in blue and hindlimb girdle
shown in green.
The hesperornithiform skull retains numerous additional ancestral characters that
are only well-preserved in two taxa (Hesperornis and Parahesperornis). Smaller hesperor-
nithiforms only preserve limited parts of the skull (i.e., Pasquiaornis,Enaliornis,Potamornis).
Marsh noted a number of similarities of the skull of Hesperornis to those of modern ratites,
including palatines and pterygoids that articulate with facets on the basipterygoid process
present on the body of the basisphenoid rostrum as well as an undivided quadrate head [
1
].
Elzanowski and Galton [
37
] identified additional ancestral features in the skulls of hesper-
ornithiforms, including open frontoparietal and intraparietal sutures, caudal origination of
the pseudotemporalis muscle, and the lack of carotid canals, among others.
A key feature contributing to the streamlined body of hesperornithiforms comes
from the elongation of the neck. The majority of hesperornithiform specimens do not
preserve a complete vertebral column, with the exception of one specimen of Parahesperornis
(KUVP 2287) that appears to preserve the entirety of the vertebral column, minus the atlas.
This specimen was largely collected in articulation, and the fit of articulation between
the separated vertebral sections indicates it is likely that only the atlas is missing [
25
].
Modern foot-propelled diving birds use their elongate necks to increase maneuverability
underwater. For example, cormorants have been documented to move their head and neck
independently of the body during pursuit diving, thus avoiding limitations imposed by the
limited turning radius of the entire body [
38
]. This contrasts with penguins, wing-propelled
diving birds that swim with their necks retracted, thus limiting their range of motion to the
turning radius of the entire body [39].
Diversity 2022,14, 267 6 of 28
Diversity 2022, 14, x FOR PEER REVIEW 6 of 28
Figure 4. Hesperornithiform teeth and dentaries: (A) dentaries of Hesperornis regalis, showing the
groove with implanted teeth in ventral view (1KUVP 71012) and a broken specimen in medial view
showing the internal projections separating individual teeth (2YPM 1206) as well as an isolated
tooth preserved with KUVP 71012 (3); (B) isolated teeth (1, 2) preserved in the roof of the articulated
premaxillae of Parahesperornis alexi KUVP 2287; (C) dentary fragment assigned to Pasquiaornis tankei
(RSM P2995.5) in lateral (1) and dorsal (2) views showing more extensive socketing (i.e., alveolar
configuration) and isolated teeth attributed to Pasquiaornis (3, 4) (images in c from [15]).
More recent work exploring the nature of the teeth in Hesperornis via synchrotron
imaging found that they have fully thecodont-style root attachments but that secondary
loss of periodontal ligaments led to the implantation of the teeth in a groove [32]. While
the retention of teeth in the jaw is plesiomorphic in Hesperornis, the emplacement of the
teeth is an autapomorphy, uniquely evolved in hesperornithiforms and not seen in other
toothed birds such as Archaeopteryx [33], Ichthyornis [34], other toothed ornithuromorphs
[35], or toothed enantiornithines [31,36]. The enamel on Hesperornis teeth is thin and sim-
ple in structure, with fine fluted ornamentation [37] formed by thickened ridges of enamel
Figure 4.
Hesperornithiform teeth and dentaries: (
A
) dentaries of Hesperornis regalis, showing the
groove with implanted teeth in ventral view (1–KUVP 71012) and a broken specimen in medial view
showing the internal projections separating individual teeth (2–YPM 1206) as well as an isolated
tooth preserved with KUVP 71012 (3); (
B
) isolated teeth (1, 2) preserved in the roof of the articulated
premaxillae of Parahesperornis alexi KUVP 2287; (C) dentary fragment assigned to Pasquiaornis tankei
(RSM P2995.5) in lateral (1) and dorsal (2) views showing more extensive socketing (i.e., alveolar
configuration) and isolated teeth attributed to Pasquiaornis (3, 4) (images in c from [15]).
A third key feature contributing to the overall bauplan of the hesperornithiforms comes
from the pelvic girdle. The pelvis is highly elongated, with an expanded preacetabular
ilium that varies in degree across hesperornithiforms but is found in all taxa (Figure 5). The
pelvis is fused only around the acetabulum, a plesiomorphic feature also found in most
other stem birds (e.g., Archaeopteryx, Sapeornis,Confuciusornis, basal ornithuromorphs,
Diversity 2022,14, 267 7 of 28
and some enantiornithines). Many enantiornithines have secondarily developed a contact
between the ischium and the postacetabular wing of the ilium [40].
Diversity 2022, 14, x FOR PEER REVIEW 8 of 28
Figure 5. Comparison of hesperornithiform pelves of: (A) Hesperornis YPM 1476; (B) Parahesperornis
KUVP 2287; (C) Fumicollis UNSM 20030; and (D) Baptornis AMNH 5101 in left lateral view. Elements
are scaled to be of a similar acetabular diameter and aligned at the acetabulum. Inset shows silhou-
ettes of the same elements to scale. After Bell and Chiappe [20].
Figure 5.
Comparison of hesperornithiform pelves of: (
A
) Hesperornis YPM 1476; (
B
)Parahesperornis
KUVP 2287; (
C
)Fumicollis UNSM 20030; and (
D
)Baptornis AMNH 5101 in left lateral view. Elements
are scaled to be of a similar acetabular diameter and aligned at the acetabulum. Inset shows silhouettes
of the same elements to scale. After Bell and Chiappe [25].
The proportion and, perhaps most importantly, the orientation of the hindlimbs
constitute a significant suite of adaptations that underlie interpretations of these birds as
foot-propelled divers. In proportion, the femur and tarsometatarsus are reduced in length,
and the tibiotarsus is highly elongated, as in modern diving birds (Figure 6). The degree of
the shortening of the femur and extension of the tibiotarsus appears to vary dramatically
across hesperornithiforms, with more basal taxa such as Baptornis and Fumicollis having a
proportionally longer femur and shorter tibiotarsus than in the more derived Hesperornis
and Parahesperornis [22].
Of particular interest to the mechanics of swimming in these birds is the orientation of
the hindlimb. The earliest observations of these birds included reference to the extreme
rotation of the femur, orienting the hindlimb behind the body. Marsh noted that the
hindlimb orientation was such that the birds must have had difficulty standing and walking
on land [
3
]. The orientation of the hindlimb directly behind the body is important for
two reasons. It places the point of propulsion directly in line with the body being propelled,
Diversity 2022,14, 267 8 of 28
and it reduces the overall surface area of the body in the direction of motion, where
resistance from the water is greatest.
Diversity 2022, 14, x FOR PEER REVIEW 9 of 28
Figure 6. Ternary diagram showing proportions of the tarsometatarsus, tibiotarsus, and femur of
hesperornithiform birds and modern foot-propelled diving birds (inset), and other modern birds.
After Bell et al. [42].
A final key feature of the hesperornithiform bauplan is the extreme reduction of the
forelimb to the point of flightlessness. This is discussed in evolutionary terms in more
detail below, but the reduction of the forelimb is seen to varying degrees across the taxa
for which forelimb elements are known, with Pasquiaornis displaying the least reduction
(but see the discussion in Section 4 regarding this problematic taxon) and Hesperornis and
Parahesperornis displaying the most (Figure 7). While the articular ends of the humerus of
Pasquiaornis retain easily identifiable morphological landmarks, such as a deltopectoral
crest at the proximal end and distinct dorsal and ventral condyles at the distal end, in
Hesperornis virtually all such detail is lost, with no discernable deltopectoral crest and only
a faint subdivision of the distal end where the condyles would be. Martin and Tate [13]
questioned whether the more distal forelimb elements (ulna, radius, carpometatacarpus,
and manual digits) developed at all, and proposed that perhaps they had been completely
lost in some taxa. The complete loss of flight in hesperornithiforms underscores the suc-
cess of these birds as foot-propelled divers, the first birds we currently know of to follow
this evolutionary path. Among modern foot-propelled divers, flightlessness has evolved
occasionally, with one species of flightless cormorant and two of grebes. The loss of flight
may indicate that these birds were so well adapted to their foot-propelled lifestyle that
they no longer needed flight to be successful for hunting, avoiding predation, and other
activities for which birds typically use flight.
Figure 6.
Ternary diagram showing proportions of the tarsometatarsus, tibiotarsus, and femur of
hesperornithiform birds and modern foot-propelled diving birds (inset), and other modern birds.
After Bell et al. [22].
A final key feature of the hesperornithiform bauplan is the extreme reduction of the
forelimb to the point of flightlessness. This is discussed in evolutionary terms in more
detail below, but the reduction of the forelimb is seen to varying degrees across the taxa
for which forelimb elements are known, with Pasquiaornis displaying the least reduction
(but see the discussion in Section 4regarding this problematic taxon) and Hesperornis and
Parahesperornis displaying the most (Figure 7). While the articular ends of the humerus of
Pasquiaornis retain easily identifiable morphological landmarks, such as a deltopectoral
crest at the proximal end and distinct dorsal and ventral condyles at the distal end, in
Hesperornis virtually all such detail is lost, with no discernable deltopectoral crest and only
a faint subdivision of the distal end where the condyles would be. Martin and Tate [
13
]
questioned whether the more distal forelimb elements (ulna, radius, carpometatacarpus,
and manual digits) developed at all, and proposed that perhaps they had been completely
lost in some taxa. The complete loss of flight in hesperornithiforms underscores the success
of these birds as foot-propelled divers, the first birds we currently know of to follow
this evolutionary path. Among modern foot-propelled divers, flightlessness has evolved
occasionally, with one species of flightless cormorant and two of grebes. The loss of flight
may indicate that these birds were so well adapted to their foot-propelled lifestyle that
Diversity 2022,14, 267 9 of 28
they no longer needed flight to be successful for hunting, avoiding predation, and other
activities for which birds typically use flight.
Figure 7.
Comparison of the humeri of hesperornithiform taxa: (
A
) Hesperornis FHSM VP-2293;
(
B
)Parahesperornis KUVP 2287; (
C
)Baptornis KUVP 2290; and (
D
)Pasquiaornis RSM P2995.1 (from [
15
]);
as well as the modern cormorants: (
E
)Phalacrocorax penicillatus (flighted); and (
F
)Nannopterum harrisi
(flightless) in (1) dorsal; and (2) cranial views. Elements are scaled to be of a similar width across the
distal condyles and aligned at the distal ends. Inset shows silhouettes of the same elements to scale.
After Bell and Chiappe [25].
3. Taxonomy
The past 150 years of research have resulted in numerous hesperornithiform taxa
being named, some of which have been revised or rejected and many of which have never
been revisited in light of more recent discoveries. This is undoubtedly one of the main
areas for future work on the Hesperornithiformes, as while many taxonomic units are still
recognized as valid, they have not undergone robust analysis and lack strong support.
The current taxonomic structure of the Hesperornithiformes recognizes four families:
the Enaliornithidae and the Brodavidae, which are both monogeneric; the Baptornithidae,
Diversity 2022,14, 267 10 of 28
with two genera; and the Hesperornithidae, with five genera (Table 1). Additionally,
Pasquiaornis,Potamornis, and Fumicollis are currently unassigned to a family, as discussed
in detail below. This overall structure largely predates the use of phylogenetic analyses in
developing taxonomic hypotheses, as typified by the initial assignment and later removal of
Pasquiaornis to the Baptornithidae. These families and intermediate genera are introduced
in this section.
Table 1.
Current taxonomic framework of the Hesperornithiformes, with taxa that have been previ-
ously invalidated shown in red.
Class Family Genus Species
Hesperornithiformes
Enaliornithidae Enaliornis
barretti
sedgewicki
seeleyi
Baptornithidae
Baptornis advenus
varneri
Judinornis nogontsavensis
Parascaniornis stensoei
Brodavidae Brodavis
americanus
baileyi
mongoliensis
varneriv
Hesperornithidae
Asiahesperornis bazhanoviv
Canadaga arctica
Coniornis altus
Hargeria gracilis
Hesperornis
altus
bairdi
chowi
crassipes
gracilis
macdonaldi
mengeli
montana
regalis
rossicus
Lestornis crassipes
Parahesperornis alexi
NA Pasquiaornis hardei
tankei
NA Chupkaornis keraorum
NA Fumicollis hoffmani
NA Potamornis skutchi
Diversity 2022,14, 267 11 of 28
3.1. Enaliornithidae
The Enaliornithidae from the Cambridge Greensand of England are the oldest hesper-
ornithiform family currently known. The Cambridge Greensand is usually interpreted as
dating from the early Cenomanian, with reworked late Albian material from the underlying
Gault Formation [
41
], indicating Enaliornis is the oldest group of hesperornithiforms. As
described above, they were first reported in 1859 by Lyell [
42
] and then more fully described
by Seeley [8].
Originally, two species were identified on the basis of size but without quantification
of those differences [
8
]. As the remains are highly fragmentary and consist entirely of
disarticulated and unassociated remains, determining the exact taxonomic diversity of
this group has proven difficult (e.g., [
8
,
13
,
43
,
44
]). Brodkorb [
45
] identified a lectotype
and numerous paralectotypes for each species. Later, extensive evaluation of all known
material by Galton and Martin [
44
] proposed diagnostic features for the genus as well as
for each species. The features identified in combination as diagnostic of the genus included
a transversely constricted centrum in the preacetabular synsacrum, the presence of an
antitrochanter on the ilium, absence of a distinct neck on the femur, tarsometatarsus with a
cranioproximal process originating proximally from metatarsal III, a caudomedial ridge
leading to trochlea II distally, and the cranial edge of trochlea IV caudal to the cranial edge
of trochlea III. They also identified a third species, E. seeleyi, as being intermediate in size
between the larger E. barretti and the smaller E. sedgewicki, but it remains unclear how
unassociated elements were combined into a single species [44].
3.2. Baptornithidae
The Baptornithidae was erected to place Baptornis advenus within the Hesperornithi-
formes as a unique monogeneric family [
13
]. Since the establishment of the family, several
new genera and species have been added to the group. A small baptornithid, Judinornis
nogontsavensis, was described from a single thoracic vertebra discovered in Maastrichtian-
aged fluvial deposits of Mongolia [
46
]. The genus Pasquiaornis, consisting of two species
from Cenomanian-aged marine strata in Canada, was also added to the Baptornithidae [
47
].
However, more recent phylogenetic analysis has determined this placement to be unsup-
ported (as discussed in Section 4below).
Baptornis is monotypic and known from several specimens, both partially complete
and isolated elements, in North America, an isolated vertebra from Europe, and an isolated
tibiotarsus fragment from Mongolia, while Judinornis remains known from the isolated ver-
tebrae from Mongolia described above. These specimens all date from the Late Cretaceous,
the youngest of which is from the Lincoln Limestone Member of the Greenhorn Formation
of Kansas (upper middle Cenomanian) [
48
] and the latest of which is from the Campanian
to Maastrichtian-aged Tsagan-Khusu locality in Mongolia [49].
These studies, along with research into baptornithid specimens from Canada [
16
] and
Kansas [
48
], have added to the diagnostic features of the family. A suite of features has
been used as diagnostic of the Baptornithidae, including a slender coracoid (as compared
to hesperornithids [
13
]), elongate preacetabular illium [
13
], pyramidal patella [
13
], and
dorsally inclined cotyla of the tarsometatarsus [48].
3.3. Brodavidae
The Brodavidae was erected to unite four fragmentary specimens into a single fam-
ily [
50
]. The Brodavidae is the second most taxonomically diverse family of hesperornithi-
forms following the hesperornithids, with four species that range widely in size (Figure 8).
Three of the four species are known from isolated tarsometatarsi. However, the holotype
and sole specimen of B. varneri is partially complete, preserving a portion of the vertebral
column, ribs, pelvis, and most of the hindlimb. This specimen was originally assigned to
Baptornis [
51
] but later moved to the Brodavidae [
50
], an assignment that has since been
supported by phylogenetic analysis [23,24].
Diversity 2022,14, 267 12 of 28
The brodavids are known primarily from the Maastrichtian (the fluvial Nemegt For-
mation of Mongolia, the Frenchman Formation of Canada, and the coastal plain Hell Creek
Formation of the USA), with the oldest specimen dating to the Campanian (the marine
Pierre Shale, USA) [50].
The Brodavidae was defined using features of the tarsometatarsus, known for all taxa,
and the rest of the postcranial skeleton, known only from B. varneri [
50
]. Two diagnostic
features were identified as separating brodavids from other hesperornithiforms [
50
]: the
shortness compared to breadth of the tarsometatarsus (this value was not quantified) and
the proximal displacement of the facet for metatarsal I (described as almost in the middle
of the tarsometatarsus).
Diversity 2022, 14, x FOR PEER REVIEW 13 of 28
Figure 8. Comparison of body size among the brodavids: (A) Brodavis varneri SDSM 68430; (B) Broda-
vis americanus cast of RSM P2315.6; and (C) Brodavis baileyi UNSM 50665.
3.4. The Hesperornithidae
The family Hesperornithidae was proposed by Marsh [2] as Hesperornidae, later
used as Hesperornithidae [7], and at the time was monogeneric and monospecific. Much
later, Clarke [54] provided the first cladistic definition for the group as a stem-based name
encompassing all taxa more closely related to Hesperornis regalis than to Baptornis advenus
[34]. Bell and Chiappe [20] later revised this definition to a node-based clade encompass-
ing all taxa descended from the common ancestor of Hesperornis regalis and Parahesperornis
alexi. The Hesperornithidae are the most taxonomically diverse group of hesperornithi-
forms. In addition to Hesperornis and Parahesperornis, Asiahesperornis [53], Canadaga [55],
and eight additional species of Hesperornis [7,5659] have been added to the family.
The Hesperornithidae are known from North America, Europe, and Asia, ranging in
age from the Coniacian/Santonian (Vermillion River Formation, Canada) to the Maas-
trichtian (Hell Creek Formation, USA and Zhuravlovskaya Svita, Russia). This range may
in fact be much older, as a specimen has been reported from the marginal marine Mesa
Verde Group, USA [58], but the stratigraphic position is poorly constrained. It is interest-
ing to note that the highest hesperornithid diversity in terms of body size and species
richness is known from the oldest deposits (such as the marine Niobrara Formation), im-
plying much information on the evolution and diversification of this group remains un-
known.
Unfortunately, Marsh did not diagnose the family separately from the genus Hesper-
ornis, and subsequent work has focused on individual species or genera and not diagnos-
tic features of the entire family. Phylogenetic work by Bell and Chiappe [17] identified 28
unambiguous synapomorphies uniting the monophyletic clade Hesperornithidae, which
could be evaluated for expanding the current diagnosis. Typical hesperornithid features
include the combination of a dramatically reduced forelimb; robust, blocky coracoid; ro-
bust femur with expanded trochanter; expanded proximal tibiotarsus with robust cnemial
crests; and enlarged fourth trochlea of the tarsometatarsus and pedal phalanx IV. While
often considered the largest of the Hesperornithiformes, it is important to remember that
species of hesperornithids range widely in size, with H. macdonaldi, H. lumgairi, H. mengeli,
and Parahesperornis much smaller than the larger species such as H. regalis and H. rossicus
(Figure 9).
Figure 8.
Comparison of body size among the brodavids: (
A
)Brodavis varneri SDSM 68430; (
B
)Bro-
davis americanus cast of RSM P2315.6; and (C)Brodavis baileyi UNSM 50665.
3.4. The Hesperornithidae
The family Hesperornithidae was proposed by Marsh [
2
] as Hesperornidae, later
used as Hesperornithidae [
7
], and at the time was monogeneric and monospecific. Much
later, Clarke [
32
] provided the first cladistic definition for the group as a stem-based name
encompassing all taxa more closely related to Hesperornis regalis than to Baptornis advenus.
Bell and Chiappe [
22
] later revised this definition to a node-based clade encompassing all
taxa descended from the common ancestor of Hesperornis regalis and Parahesperornis alexi.
The Hesperornithidae are the most taxonomically diverse group of hesperornithiforms. In
addition to Hesperornis and Parahesperornis,Asiahesperornis [
52
], Canadaga [
53
], and eight
additional species of Hesperornis [7,5456] have been added to the family.
The Hesperornithidae are known from North America, Europe, and Asia, ranging
in age from the Coniacian/Santonian (Vermillion River Formation, Canada) to the Maas-
trichtian (Hell Creek Formation, USA and Zhuravlovskaya Svita, Russia). This range may
in fact be much older, as a specimen has been reported from the marginal marine Mesa
Verde Group, USA [
57
], but the stratigraphic position is poorly constrained. It is interesting
to note that the highest hesperornithid diversity in terms of body size and species richness
is known from the oldest deposits (such as the marine Niobrara Formation), implying
much information on the evolution and diversification of this group remains unknown.
Unfortunately, Marsh did not diagnose the family separately from the genus Hesper-
ornis, and subsequent work has focused on individual species or genera and not diagnostic
features of the entire family. Phylogenetic work by Bell and Chiappe [
22
] identified 28 un-
Diversity 2022,14, 267 13 of 28
ambiguous synapomorphies uniting the monophyletic clade Hesperornithidae, which
could be evaluated for expanding the current diagnosis. Typical hesperornithid features
include the combination of a dramatically reduced forelimb; robust, blocky coracoid; ro-
bust femur with expanded trochanter; expanded proximal tibiotarsus with robust cnemial
crests; and enlarged fourth trochlea of the tarsometatarsus and pedal phalanx IV. While
often considered the largest of the Hesperornithiformes, it is important to remember that
species of hesperornithids range widely in size, with H. macdonaldi,H. lumgairi,H. mengeli, and
Parahesperornis much smaller than the larger species such as H. regalis and H. rossicus (Figure 9).
Diversity 2022, 14, x FOR PEER REVIEW 14 of 28
Figure 9. Comparison of body size among Hesperornithidae taxa: (A) H. regalis YPM 1200; (B) H.
chowi YPM PU 17208; (C) H. rossicus SGU 3442 Ve01; (D) H. gracilis, YPM 1473; (E) H. lumgairi CFDC
B78.02.07; (F) H. bairdi YPM PU 17208a; (G) Asiahesperornis bazhanovi IZASK 5/287/86a; (H) H. mengeli
CFDC 78.01.08; (I) Parahesperornis alexi KUVP 2287; (J) H. altus YPM 515; (K) H. macdonaldi LACM
9727. Silhouettes are approximately scaled to averages of measurements of the corresponding ele-
ments preserved in specimens of H. regalis.
3.5. Taxa Outside of Recognized Families
3.5.1. Pasquiaornis
Pasquiaornis was erected to unite two species of small hesperornithiforms from the
marine Belle Fourche Formation (Cenomanian) of Canada [46]. Pasquiaornis was originally
assigned to the Baptornithidae [46]. However, subsequent phylogenetic analysis failed to
return Pasquiaornis + Baptornis as a monophyletic clade, and it was suggested that Pasqui-
aornis should not be considered part of the Baptornithidae [50,56]. Additional analysis has
since supported this phylogenetic topography [17]. These taxa are only known in the lit-
erature from unassociated and disarticulated elements found in a bone-bed deposit in the
Belle Fouche Formation [13].
Figure 9.
Comparison of body size among Hesperornithidae taxa: (
A
)H. regalis YPM 1200; (
B
)H.
chowi YPM PU 17208; (
C
)H. rossicus SGU 3442 Ve01; (
D
)H. gracilis, YPM 1473; (
E
)H. lumgairi
CFDC B78.02.07; (
F
)H. bairdi YPM PU 17208a; (
G
)Asiahesperornis bazhanovi IZASK 5/287/86a; (
H
)H.
mengeli CFDC 78.01.08; (
I
)Parahesperornis alexi KUVP 2287; (
J
)H. altus YPM 515; (
K
)H. macdonaldi
LACM 9727. Silhouettes are approximately scaled to averages of measurements of the corresponding
elements preserved in specimens of H. regalis.
Diversity 2022,14, 267 14 of 28
3.5. Taxa Outside of Recognized Families
3.5.1. Pasquiaornis
Pasquiaornis was erected to unite two species of small hesperornithiforms from the
marine Belle Fourche Formation (Cenomanian) of Canada [
47
]. Pasquiaornis was originally
assigned to the Baptornithidae [
47
]. However, subsequent phylogenetic analysis failed
to return Pasquiaornis +Baptornis as a monophyletic clade, and it was suggested that
Pasquiaornis should not be considered part of the Baptornithidae [22]. Additional analysis
has since supported this phylogenetic topography [
24
]. These taxa are only known in the
literature from unassociated and disarticulated elements found in a bone-bed deposit in
the Belle Fouche Formation [13].
Tokaryk et al. [
47
] proposed that a combination of size and select morphological
differences could be used to separate the disarticulated elements and assigned Pasquiaornis
specimens into two species, P. hardei and P. tankei. While P. tankei was described as the
larger of the two taxa, specific size differentials used to separate these species have never
been quantified. Furthermore, as there are no associated elements known within the
genus, it is unclear how different elements are assigned together in one of the two species.
Pasquiaornis was diagnosed as having a less-expanded trochanter and proximal end of the
femur than is seen in Baptornis, as well as having the anterior intercotylar eminence on the
tarsometatarsus overhanging the shaft and trochlea II of the tarsometatarsus positioned
posterior to and near the base of trochlea III [47].
3.5.2. Chupkaornis
Chupkaornis is a small hesperornithiform discovered in the Coniacian to Santonian-
aged Kashima Formation in Hokkaido, Japan [
24
]. The holotype and sole specimen was
published as a partial skeleton preserving six vertebrae, distal femora, and a fragment
of fibula [
24
]. However, examination of the photographs published indicates what is
described as the distal left femur is actually a distal tibiotarsus. Phylogenetic analysis
returned Chupkaornis as basal to Brodavis within the Hesperornithiformes and derived from
Enaliornis and Pasquiaornis.
Diagnostic features proposed as separating Chupkaornis from other hesperornithiforms
include the combination of vertebrae that are fully heterocoelous (but see discussion in
Section 4below) with emarginated lateral excavations on the centra and sharp ventral
margins; slender ventral process and laterally expanded fibular condyle of the femur with
a finger-like projection on the tibiofibular crest [24].
3.5.3. Fumicollis
The holotype of Fumicollis was originally identified as Baptornis [
13
] but later recog-
nized as possessing some characters typical of hesperornithids and some typical of Baptornis
during the course of research for a phylogenetic study of the hesperornithiforms [
23
]. This
specimen was therefore used to erect a new species—Fumicollis hoffmani—phylogenetically
intermediate between the Baptornithidae and the Hesperornithidae [
58
]. This placement
has since been supported by additional analysis [
24
]. Two additional specimens, both
isolated femora, have also been proposed as belonging to Fumicollis. Both of these are
known from museum collection studies but are currently unpublished (specimen numbers
not available). The holotype and only published specimen preserves a partial vertebral
column and nearly complete hindlimb, making it one of the more complete hesperornithi-
form specimens. Fumicollis is known from the marine Smoky Hill Member of the Niobrara
Formation (upper Coniacian to lower Campanian [59]) of Kansas (USA) [58].
A combination of features from the vertebrae, pelvis, femur, tibiotarsus, and tar-
sometatarsus were used to diagnose the genus [
58
]. These include an elongate preacetabu-
lar pelvis, expanded lateral condyle on the femur (defined as midshaft width 75% of lateral
condyle width), medial cnemial crest extended to midshaft of the femur, pyramidal patella,
a distinct dorsal ridge of the tarsometatarsus formed by the entire length of metatarsal IV,
and others. The presence of both baptornithid and hesperornithid characters can be seen
Diversity 2022,14, 267 15 of 28
in these traits. For example, the degree of expansion of the lateral condyle is also found
in Baptornis, while the dorsal surface of metatarsal IV forming a prominent ridge along its
entire length is typical of hesperornithids.
3.5.4. Potamornis
Potamornis skutchi was erected for an isolated quadrate discovered from the flu-
viodeltaic Lance Formation (late Maastrichtian) in Wyoming (USA) [
60
]. The element was
assigned to the Hesperornithiformes on the basis of an undivided head and an elongate
pterygoid condyle, features typical of hesperornithiform quadrates. A unique combina-
tion of characters was identified as diagnostic of Potamornis skutchi, including: a strongly
asymmetrical quadrate head, rostrally open pit near the medial apex of the head, shallow
caudomedial depression, small orbital process, a quadratojugal buttress on the lateral pro-
cess, and medial and lateral mandibular condyles meeting at an angle of 115 degrees [
60
].
An isolated tarsometatarsus from the same formation was also tentatively assigned to
the genus on the basis of size [
60
]. However, the specimen was not figured or formally
described, and no additional work has been done.
3.6. Taxonomic Challenges
Our understanding of hesperornithiform taxonomy is plagued by a host of problems
common to paleontology, such as the renaming of previously described taxa [
59
,
61
]; taxa
described from highly fragmentary material [
24
,
50
,
55
,
56
,
62
]; elements misidentified [
24
];
and subjective, unspecific, or incorrect characters used for diagnosis [
47
,
63
]; reliance upon
which may result in further confusing the assignment of fragmentary taxa [
50
,
64
]. The
majority of hesperornithiform species have been described from fragmentary material
(Figure 10). Of the 25 described species, only six include specimens preserving more than
three elements, one is known from two elements, and 18 species were described and remain
known from a single bone. Whether or not all of these species are valid taxa has rarely
been rigorously examined. For example, debate over the synonymy of Coniornis altus [
65
],
Hesperornis altus [
62
], and Hesperornis montana [
62
] has appeared in the literature, with both
Coniornis and H. montana being invalidated without H. altus ever being resolved in the form
of a concise diagnostic description and justification of the “valid” taxon.
Perhaps due to difficulties arising from the fragmentary nature of the fossil record,
a number of taxa have been poorly or inaccurately described. An example of one such
recurring error and source of much confusion is the presence or absence of the proximal
foramina on the cranial surface of the tarsometatarsi of hesperornithiforms. In his mono-
graph on hesperornithiforms, Marsh did not mention the presence of these foramina in
Hesperornis or Baptornis [
1
]. More recent descriptive work has specifically pointed out the
lack of these foramina in numerous species of hesperornithiforms [
13
,
44
,
63
]. This has led to
the presence of these foramina to be used, in part, as justification for the Cretaceous of Chile
from the Hesperornithiformes [
64
]. Furthermore, the relative degree of development of the
foramina has been used as a diagnostic feature of two species of Brodavis [
50
]. However,
closer examination of specimens of H. regalis,H. gracilis, H. crassipes,P. alexi, B. advenus, and
other unidentified hesperornithiforms shows that in all cases proximal foramina are present
on the cranial surface of the tarsometatarsi [
32
,
48
]. Incomplete preparation of the bones
may be to blame for the foramina being overlooked by previous authors. Additionally, the
appearance of these foramina appears to be closely tied to preservation quality.
As discussed by Bell [
65
], another problem that is commonly seen in hesperornithiform
taxonomy is the reliance on qualitative language to describe quantitative traits. For example,
the tarsometatarsus of numerous species has been described as being “slender”. This
is essentially a qualitative way of describing the length to width ratio of the element.
Using this sort of language in the diagnosis of numerous species instead of presenting
morphometric data to precisely define important aspects of morphology creates uncertainty
and confusion when making comparisons across dozens of species.
Diversity 2022,14, 267 16 of 28
Diversity 2022, 14, x FOR PEER REVIEW 16 of 28
combination of characters was identified as diagnostic of Potamornis skutchi, including: a
strongly asymmetrical quadrate head, rostrally open pit near the medial apex of the head,
shallow caudomedial depression, small orbital process, a quadratojugal buttress on the
lateral process, and medial and lateral mandibular condyles meeting at an angle of 115
degrees [62]. An isolated tarsometatarsus from the same formation was also tentatively
assigned to the genus on the basis of size [62]. However, the specimen was not figured or
formally described, and no additional work has been done.
3.6. Taxonomic Challenges
Our understanding of hesperornithiform taxonomy is plagued by a host of problems
common to paleontology, such as the renaming of previously described taxa [62,63]; taxa
described from highly fragmentary material [18,52,57,64]; elements misidentified [18]; and
subjective, unspecific, or incorrect characters used for diagnosis [49,65]; reliance upon
which may result in further confusing the assignment of fragmentary taxa [28,66]. The
majority of hesperornithiform species have been described from fragmentary material
(Figure 10). Of the 25 described species, only six include specimens preserving more than
three elements, one is known from two elements, and 18 species were described and re-
main known from a single bone. Whether or not all of these species are valid taxa has
rarely been rigorously examined. For example, debate over the synonymy of Coniornis
altus [67], Hesperornis altus [64], and Hesperornis montana [64] has appeared in the literature,
with both Coniornis and H. montana being invalidated without H. altus ever being resolved
in the form of a concise diagnostic description and justification of the valid taxon.
Figure 10. Specimen completeness of hesperornithiform taxa. Insets show percentages of specimens
that preserve: (A) elements belonging to different regions of the body; and (B) main elements of the
hindlimb. After Bell and Chiappe [20].
Figure 10.
Specimen completeness of hesperornithiform taxa. Insets show percentages of specimens
that preserve: (
A
) elements belonging to different regions of the body; and (
B
) main elements of the
hindlimb. After Bell and Chiappe [20].
The examples of fraught taxonomy of hesperornithiforms described here illustrate
opportunities for future research, as significant synthesis and revision may be achieved
from broad-scale studies of currently known material, enhanced and improved with the
addition of more recently discovered material that has not been previously published as
well as future discoveries [65].
4. Phylogeny of the Hesperornithiformes
Early approaches to hesperornithiform phylogenetics relied on a limited number of
taxa (usually under five) and characters (usually under ten) identified as synapomorphies
a priori and then used as justification for a particular tree topology. One example of this
approach is Cracraft’s [
19
] tree of diving birds that showed hesperornithiforms within mod-
ern birds, basal to a clade containing loons and grebes and derived from penguins, pelicans,
and other seabirds (Procellariiformes). Another example is Martin’s [
63
] work in which
he developed two trees showing: (1) Hesperornis and Parahesperornis as a monophyletic
clade progressively more derived than the Baptornithidae and the Enaliornithidae; and
(2) hesperornithiforms as basal to a monophyletic clade of ichthyornithiforms and modern
birds but more derived than “Sauriurae”. A more modern approach to a phylogenetic
Diversity 2022,14, 267 17 of 28
analysis was taken by Elzanowski and Galton [
37
], who developed a matrix of 17 characters
for seven taxonomic units, but did not conduct an analysis of this matrix and did not offer
any phylogenetic hypotheses from these data.
The explosion of Mesozoic bird fossils in the 1990s from China, South America, and
Europe initiated a new wave of research into early bird evolution, including the widespread
application of modern phylogenetic methods. In these analyses, hesperornithiforms, usu-
ally represented by Hesperornis, consistently placed as fairly derived within Ornithuro-
morpha, usually as the sister taxon to a clade containing Ichthyornis and modern birds
(e.g., [
32
,
66
68
]). More recent work involving multiple hesperornithiform taxa has returned
the Hesperornithiformes as the sister taxon to Neornithes, or crown clade birds [
22
,
69
71
],
while other studies retain the placement of the hesperornithiforms as sister to Ichthyornis +
Neornithes [24,72,73].
Two things are important to note in comparing the different placement of hesperor-
nithiforms among derived ornithuromorphs. First, the choice of taxa seems to play a role
in the placement of hesperornithiforms, with studies that include numerous hesperornithi-
forms more likely to resolve them as closer to Neornithes (e.g., [
24
,
71
]) than studies that
include only one or two of the typically more derived hesperornithiforms (i.e., Hesperornis)
(e.g., [
32
,
72
,
73
] but see [
24
]). Second, many matrices have not updated specimen codings in
response to the ever-evolving taxonomic changes and in light of new evidence identifying
mistakes in previous descriptions of taxa. For example, some studies maintain specimens
coded as Baptornis that have since been removed from that genus (e.g., [
73
]) or use charac-
ters that have been identified as erroneous such as features of the quadrate of Baptornis,
which was incorrectly described by Martin and Tate [
13
] and is, in fact, unknown for that
taxon (as described in Bell [65] and Bell and Chiappe [25] (e.g., [24,73]).
There are few studies that have examined phylogenetic relationships among the hes-
perornithiforms, but these studies generally agree in overall topography (Figure 11). The
most derived clade consists of a monophyletic Hesperornis, with Parahesperornis as sister
taxa, followed by the progressively more basal Fumicollis,Brodavis, and Baptornis [
22
,
24
].
There is disagreement at the base of the tree, with Bell and Chiappe [
22
] resolving Pasquiaor-
nis as more basal than Enaliornis and Tanaka et al. [
24
] resolving the reverse relationship
and a similar switch between Baptornis and Brodavis (Figure 12). This disagreement likely
results from the incredibly fragmentary nature of the material for both these taxa and stems
from coding discrepancies of features easily obscured by weathering. The details of this are
reviewed in Bell and Chiappe [
25
] but are rooted in the very poor preservation of Enaliornis
as part of a reworked deposit that has resulted in the smoothing of the bones, thus making
the observation of many details difficult, if not impossible.
5. Evolutionary Trends
As the oldest known lineage of diving birds, hesperornithiforms allow us to study a
remarkable evolutionary transition—a group of birds that gave up the ability to fly in favor
of foot-propelled diving. This transition is evident in a unique suite of skeletal adaptations
as well as in the size of these birds and the range of environments they occupied.
Perhaps one of the most interesting aspects of the evolutionary trends described below
is the absence of a fossil record of early stages of these trends. It remains unclear who the
predecessors of the Hesperornithformes were. Despite an abundance of Early Cretaceous
lagerstätten preserving both freshwater and estuarine environments in China and Spain,
there are no clear foot-propelled diving adaptations in the diverse avifauna. The oldest
hesperornithiforms, the species of Enaliornis, appear in the earliest Late Cretaceous already
equipped with numerous adaptations that support interpretations of a foot-propelled
diving lifestyle, including an expanded lateral condyle on the femur and angled articular
surface with greatly expanded cnemial expansion on the tibiotarsus, and stacked or shingled
metatarsals in the tarsometatarsus. By the middle of the Late Cretaceous (late Coniacian
to early Campanian) some of the most abundant deposits of hesperornithiform birds are
known from the Smoky Hill Chalk (Kansas, USA) of the Western Interior Seaway, with many
Diversity 2022,14, 267 18 of 28
roughly coeval taxa ranging from the small Baptornis to the large, highly derived Hesperornis
regalis. Furthermore, all of the hesperornithiforms from the early Late Cretaceous (pre-
Campanian) are known from entirely marine deposits, while fewer hesperornithiforms
are known from the Maastrichtian, these are primarily known from marginal marine to
terrestrial deposits (with a small number of exceptions in the Campanian) (Table 2). It is
tempting to interpret this as demonstrating an evolutionary diversification from entirely
marine taxa to taxa constituting different species adapted to the marine realm, shallow
waters of estuaries, and even freshwater. It should be noted that there may be an element
of taphonomic bias at play, as the depositional environment of an animal is not necessarily
that in which it lived, and the fact that climate and tectonic-driven transgressions of the
late Early to early Late Cretaceous led to a disproportionate abundance of marine deposits
for this time period [74].
Diversity 2022, 14, x FOR PEER REVIEW 18 of 28
Two things are important to note in comparing the different placement of hesper-
ornithiforms among derived ornithuromorphs. First, the choice of taxa seems to play a
role in the placement of hesperornithiforms, with studies that include numerous hesper-
ornithiforms more likely to resolve them as closer to Neornithes (e.g., [17,75]) than studies
that include only one or two of the typically more derived hesperornithiforms (i.e., Hes-
perornis) (e.g., [34,73,76] but see [18]). Second, many matrices have not updated specimen
codings in response to the ever-evolving taxonomic changes and in light of new evidence
identifying mistakes in previous descriptions of taxa. For example, some studies maintain
specimens coded as Baptornis that have since been removed from that genus (e.g., [73]) or
use characters that have been identified as erroneous such as features of the quadrate of
Baptornis, which was incorrectly described by Martin and Tate [13] and is, in fact, un-
known for that taxon (as described in Bell [77] and Bell and Chiappe [20] (e.g., [18,73]).
There are few studies that have examined phylogenetic relationships among the hes-
perornithiforms, but these studies generally agree in overall topography (Figure 11). The
most derived clade consists of a monophyletic Hesperornis, with Parahesperornis as sister
taxa, followed by the progressively more basal Fumicollis, Brodavis, and Baptornis [17,18].
There is disagreement at the base of the tree, with Bell and Chiappe [17] resolving Pasqui-
aornis as more basal than Enaliornis and Tanaka et al. [18] resolving the reverse relation-
ship and a similar switch between Baptornis and Brodavis [50,54] (Figure 12). This disa-
greement likely results from the incredibly fragmentary nature of the material for both
these taxa and stems from coding discrepancies of features easily obscured by weathering.
The details of this are reviewed in Bell and Chiappe [20] but are rooted in the very poor
preservation of Enaliornis as part of a reworked deposit that has resulted in the smoothing
of the bones, thus making the observation of many details difficult, if not impossible.
Figure 11.
Phylogenetic tree of hesperornithiform birds, after Bell and Chiappe [
22
], with the addition
of Chupkaornis from Tanaka et al. [
24
]. Arrows indicate alternative positions for Enaliornis and
Pasquiaornis and Baptornis and Brodavis in Tanaka et al. [
24
]. Diagrams indicate anatomical adaptations
proposed to correlate with foot-propelled diving: (
A
) angled articular surface and cnemial expansion
on the tibiotarsus; (
B
) reduced humerus; (
C
) expanded femoral trochanter; (
D
) fourth trochlea of
the tarsometatarsus forms a sharp ridge; (
E
) enlarged, triangular patella; (
F
) expanded intercotylar
eminence on the tarsometatarsus.
Diversity 2022,14, 267 19 of 28
Diversity 2022, 14, x FOR PEER REVIEW 19 of 28
Figure 11. Phylogenetic tree of hesperornithiform birds, after Bell and Chiappe [17], with the addi-
tion of Chupkaornis from Tanaka et al. [18]. Arrows indicate alternative positions for Enaliornis and
Pasquiaornis and Baptornis and Brodavis in Tanaka et al. [18]. Diagrams indicate anatomical adapta-
tions proposed to correlate with foot-propelled diving: (A) angled articular surface and cnemial
expansion on the tibiotarsus; (B) reduced humerus; (C) expanded femoral trochanter; (D) fourth
trochlea of the tarsometatarsus forms a sharp ridge; (E) enlarged, triangular patella; (F) expanded
intercotylar eminence on the tarsometatarsus. After Bell and Chiappe [17].
Figure 12. Distribution of hesperornithiform specimens in geologic units and: (A) depositional en-
vironments; and (B) time periods within the Late Cretaceous. All formations from which fewer than
five specimens are known are included in “other” for each depositional environment and time pe-
riod. After Bell et al. [42].
5. Evolutionary Trends
As the oldest known lineage of diving birds, hesperornithiforms allow us to study a
remarkable evolutionary transitiona group of birds that gave up the ability to fly in
favor of foot-propelled diving. This transition is evident in a unique suite of skeletal ad-
aptations as well as in the size of these birds and the range of environments they occupied.
Perhaps one of the most interesting aspects of the evolutionary trends described be-
low is the absence of a fossil record of early stages of these trends. It remains unclear who
the predecessors of the Hesperornithformes were. Despite an abundance of Early Creta-
ceous lagerstätten preserving both freshwater and estuarine environments in China and
Spain, there are no clear foot-propelled diving adaptations in the diverse avifauna. The
oldest hesperornithiforms, the species of Enaliornis, appear in the earliest Late Cretaceous
already equipped with numerous adaptations that support interpretations of a foot-pro-
pelled diving lifestyle, including an expanded lateral condyle on the femur and angled
articular surface with greatly expanded cnemial expansion on the tibiotarsus, and stacked
or shingled metatarsals in the tarsometatarsus. By the middle of the Late Cretaceous (late
Coniacian to early Campanian) some of the most abundant deposits of hesperornithiform
birds are known from the Smoky Hill Chalk (Kansas, USA) of the Western Interior Sea-
way, with many roughly coeval taxa ranging from the small Baptornis to the large, highly
derived Hesperornis regalis. Furthermore, all of the hesperornithiforms from the early Late
Cretaceous (pre-Campanian) are known from entirely marine deposits, while fewer hes-
perornithiforms are known from the Maastrichtian, these are primarily known from mar-
ginal marine to terrestrial deposits (with a small number of exceptions in the Campanian)
(Table 2). It is tempting to interpret this as demonstrating an evolutionary diversification
Figure 12.
Distribution of hesperornithiform specimens in geologic units and: (
A
) depositional
environments; and (
B
) time periods within the Late Cretaceous. All formations from which fewer
than five specimens are known are included in “other” for each depositional environment and time
period. After Bell et al. [22].
Table 2.
Geologic units, divided by depositional environment, with published hesperornithiform
taxa. After Bell et al. [22].
Continental
Mesa Verde Formation (Teapot Sandstone) [57]
Hesperornis regalis
Campanian
Hesperornis sp.
Nemegt Formation [75]
Brodavis
mongoliensis
Maastrichtian
Judinornis
nogontsavensis
Hesperornithidae
indet.
Lance Formation [76]Potamornis skutchi Late Maastrichtian
Frenchman Formation [77]Brodavis americanus Late Maastrichtian
Transitional
Foremost Formation [78] Hesperornis sp. Campanian
Judith River Formation [79]
Baptornis sp.
Campanian
Hesperornis altus
Dinosaur Provincial Park Formation [80]Baptornis sp. Late Campanian
Hell Creek Formation [81]Brodavis baileyi
Maastrichtian
Hesperornis sp.
Marine
Cambridge Greensand Member (West Melbury Chalk
Formation) [44]
Enaliornis barretti
Early Cenomanian
Enaliornis seeleyi
Enaliornis sedgewicki
Belle Fouche Formation (formerly Ashville Formation)
[14]
Pasquiaornis hardiei
Late Cenomanian
Pasquiaornis tankei
Diversity 2022,14, 267 20 of 28
Table 2. Cont.
Greenhorn Formation [48]Baptornis sp. Cenomanian
Kashima Formation [24]Chupkaornis
keraorum Coniacian to Santonian
Vermillion River Formation [82]
Hesperornis regalis
Coniacian to Santonian
Hesperornis sp.
Ignek Formation [83] Hesperornis sp. Late Coniacian to Campanian
Smoky Hill Chalk, Niobrara Formation [84]
Baptornis advenus
Late Coniacian to early Campanian
Hesperornis crassipes
Hesperornis gracilis
Hesperornis regalis
Hesperornis sp.
Fumicollis hoffmani
Parahesperornis alexi
Parahesperornis sp.
Smoking Hills Formation [85]Hesperornis regalis Middle Santonian to early late
Campanian
Eginsaiskaya [49]
Baptornis advenus
Latest Santonian to Early Campanian
Asiahesperornis
bazhanovi
Rybushka Formation [86]
Hesperornis rossicus
Early Campanian
Hesperornis sp.
Kristianstad Basin (unreported formation) [61]
Baptornis sp.
Latest early Campanian
Hesperornis rossicus
Hesperornis sp.
Kanguk Formation [87]
Canadaga arctica
Early to middle Campanian
Hesperornis sp.
Clagget Shale [57] Hesperornis sp. Campanian
Pierre Shale [88]
Baptornis advenus
Campanian
Brodavis varneri
Hesperornis bairdi
Hesperornis chowi
Hesperornis lumgairi
Hesperornis
macdonaldi
Hesperornis mengeli
Hesperornis regalis
Hesperornis rossicus
Hesperornis sp.
Chico Formation [89] Hesperornis sp. Campanian
Ozan Formation [90] Hesperornis sp. Campanian
Kita-ama Formation [91]Hesperornithiformes
undet. Early Maastrichtian
Zhuravlovskaya Svita [92]Asiahesperornis
bazhanovi Maastrichtian
Diversity 2022,14, 267 21 of 28
5.1. Flightlessness
The most dramatic and obvious evolutionary trend in the Hesperornithiformes is the
complete adaptation to a foot-propelled diving lifestyle. For the majority of hesperornithi-
forms that preserve forelimb elements, there is agreement that these birds were entirely
flightless [
1
,
8
,
13
,
25
,
63
,
65
,
93
]. The only hesperornithiform for which a degree of flight ca-
pacity has been proposed as plausible is Enaliornis, on the basis of the small body size and
extensive pneumatization of the braincase [
37
]. Indeed, the degree of pneumatization in
the braincase of Enaliornis is much greater than in either Parahesperornis or Hesperornis [
25
].
However, additional data from the forelimb, which is entirely unknown in Enaliornis, is
required to better evaluate these claims. As described below, some form of limited flight
capabilities have also been tentatively suggested for Pasquiaornis [
15
], but again the dearth
of fossil evidence for this taxon makes those claims speculative.
The forelimb and shoulder girdle are indicative of the evolutionary pathway leading
to loss of flight in hesperornithiforms, with Pasquiaornis less derived than Baptornis and
hesperornithids. The coracoids of hesperornithiforms are less developed as compared
to flying birds, with reduced acrocoracoid processes and the absence of a procoracoid
process. This trend culminates in hesperornithids, which also have an increasingly short
coracoidal neck compared to Baptornis and even more than in Pasquiaornis. A similar trend
is seen in the scapula and clavicle, with the articular surfaces only faintly developed in
hesperornithiforms. Another factor associated with flightlessness is the complete absence
of a ventral keel on the sternum. Hesperornis and Parahesperornis both preserve nearly
complete sterna which show the complete absence of a keel.
The humerus is known for several hesperornithiform taxa and consists of an incredibly
gracile bone with little to no development of articular surfaces and the deltopectoral and
bicipital crests, in both large birds such as Hesperornis and small birds such as Baptornis
(Figure 7). Pasquiaornis is the only hesperornithiform that preserves forelimb material for
which rudimentary flight abilities have been suggested as tentatively possible [
15
], based
largely on the less reduced state of flight-related features such as the development of the
distal condyles and deltopectoral and bicipital crests on the humerus [
15
,
47
]. The ulna and
radius are only known in Baptornis and Pasquiaornis, where both are reduced with faintly
developed articular ends compared to flying birds [
13
,
15
,
93
]. The carpometacarpus is only
known in Pasquiaornis, which is also consistent with flightlessness in the thickened compact
bone and the distal placement of the extensor process [
15
]. As indicated above, only the
discovery of more complete material in this basal-most hesperornithiform can provide a
reliable interpretation of its potential aerial capabilities.
5.2. Foot-Propelled Diving
In concert with the reduction of the forelimb described above, a number of hesperor-
nithiform skeletal features point to a highly derived foot-propelled diving lifestyle. These
features have been assessed morphometrically [
22
,
94
] and discussed in detail by Bell and
Chiappe [
25
]. In particular, the articulation of the leg in hesperornithiforms has the femur
splayed laterally from the pelvis and possibly contained entirely within the body, with
the lower limb extending linearly from the knee joint parallel with the mainline of the
body. This orients the feet, the source of propulsion, directly behind the body. Adaptations
associated with this in Hesperornis include a robust femoral trochanter that extends evenly
to the femoral head, an exaggerated lateral femoral condyle roughly even with the medial
condyle, a sharply angled proximal articular surface on the tibiotarsus, twisted shafts on
the tibiotarsus and tarsometatarsus, and a dramatically enlarged third toe with expanded
lateral condyle for rotation of the toe. These features are variably present, but often to a
lesser degree, in more basally diverging hesperornithiform taxa.
In addition to the dramatic restructuring of the hindlimb for foot-propelled diving,
hesperornithiforms have a suite of more subtle features that also indicate a diving lifestyle.
The number, shape, and arrangement of teeth in the jaws of Hesperornis have trophic
implications, with the increased number of teeth in the dentary having been related to a
Diversity 2022,14, 267 22 of 28
piscivorous diet [
28
], an interpretation well aligned with the environment these birds lived
in and morphological interpretations discussed above. The distinct hooked cranial terminus
of the premaxilla, which may have been emphasized by the shape of the keratinous beak,
may have also been useful for the retention or capture of larger fish. The wide variation in
tooth loss, reduction, and shape seen across Mesozoic birds highlights the trophic diversity
present among these early birds [
26
] (in some cases supported by gut contents). However,
specific correlations between a particular dental trait, such as the dramatic mesio-distal
recurvature gradient in hesperornithiforms, and specific dietary specializations, have not
been identified to date [30].
Several features of the skull of hesperornithiforms have been used to support inter-
pretations of a diving lifestyle. Elzanowski and Galton identified the large size of the
auricular fossae, the reduced dorsal pneumatic recess, and the flattened cerebellar fossa as
traits shared with modern diving birds [
37
]. The latter two of these features was noted as
possibly associated with the expansion of the dural sinuses [
37
], a convergent feature found
in a wide range of diving birds and mammals [
95
97
]. Histological work has identified
a thick compact bone wall and comparatively small medullary cavity in the femur of
Hesperornis, a feature also found in penguins and interpreted as decreasing buoyancy as a
diving adaptation [98].
5.3. Gigantism
One of the first things noted about Hesperornis was its very large body size [
2
,
3
],
which could approach 1.5 m in length. The discovery of the much smaller Baptornis soon
after, showed the dramatic size range present in hesperornithiforms [
99
]. Most interestingly,
this range of sizes does not appear to be correlated to any particular evolutionary trend
and is unrelated to the degree of diving specialization [
22
,
25
]. While large-bodied taxa are
missing among the most basally diverging hesperornithiforms, Enaliornis and Pasquiaornis,
there are more derived taxa that are also small. Within the brodavids, for example, the
midshaft of the tarsometatarsus of the smallest species, B. mongoliensis, is less than half the
diameter of that of the largest species, B. varneri (Figure 9). Similarly, there are several small
species of Hesperornis, and while it is not possible to make direct comparisons between
them due to lack of overlap in preserved elements, they can be compared to larger species
such as H. regalis and H. rossicus (Figure 9). The tarsometatarsus of H. mengeli is half the
size of H. rossicus, while the femur of H. macdonaldi is less than half the length of that of
H. regalis. All of these species of Hesperornis show similar development of the features
described above associated with diving specializations, thus decoupling the evolution
of foot-propelled diving from changes in body size [
22
,
25
] which we see varying within
lineages of hesperornithiforms, indicating the independent evolution of gigantism [
22
].
This occurred at least twice, once in the brodavids and at least once in several species of
Hesperornis, with miniaturization possible in some of the smallest species of Hesperornis
as well.
The topic of body size goes hand-in-hand with that of growth rates and ontogenetic
patterns. Very little histological work has been done on hesperornithiforms, so the manner
or timing in which gigantism (or lack thereof) was achieved in these birds is largely
unknown. The first histological study of hesperornithiforms was conducted to address the
discrepancies at the time regarding the treatment of hesperornithiforms as either ratites or
neognaths within neornithines (modern birds) and found that the bone microsctructure
of the hindlimb of Hesperornis was like that of neognaths [
100
]. This study did not
address growth rates. The next histological study of hesperornithiforms characterized
the microstructure of the bone from a femur of Hesperornis, identifying the individual
as a subadult from the lack of peripheral lamellar bone [
98
]. Significantly, this study did
not identify lines of arrested growth in Hesperornis, indicating there was no evidence
for cyclical growth as seen in more basal Mesozoic birds (e.g., Archaeopteryx, Sapeornis,
Confuciusornis, enantionithines, and many stem ornithuromorphs). Thus, continuous
growth and the resulting absence of lines of arrested growth is a derived feature that
Diversity 2022,14, 267 23 of 28
Hesperornis shares with modern birds [
98
]. This has important implications for physiology
and life history, as it may indicate a fully endothermic physiology consistent with the
interpretation of hesperornithids as venturing far offshore into deep marine waters [
98
]
and growth patterns comparable to those of modern birds (i.e., reaching full-grown size
within the first year). The capability for rapid, sustained growth would also contribute to
the gigantic body size attained in multiple lineages of these birds.
More recently, hindlimb bones from Hesperornis specimens discovered along a latitu-
dinal gradient from Kansas to the Arctic were examined to investigate the effects of climate
and possible migration on bone microstructure [
101
]. This study found continuous bone
deposition and did not identify cyclic growth marks [
101
], supporting the previous results
of Chinsamy et al. [
98
] and indicating that migratory patterns to different climates is either
not recorded in bone microstructure or that these birds achieved skeletal maturity before
migrating [
101
]. The lack of histological work may be in part complicated by taphonomic
processes in some of the more prolific hesperornithiform sedimentary units. For exam-
ple, several members of the Pierre Shale are characterized by calcite crystallization in the
preserved bones, destroying histological information.
6. Paleoecology
The obvious and dramatic diving adaptations in hesperornithiforms described above,
combined with their wide distribution across the Northern Hemisphere (Figure 2), have
led to a large body of work involving the paleoecology of these birds, including the aquatic
environments they occupied [
22
,
94
,
101
], modern ecological analogues [
22
,
94
], and niche
partioning [22,24].
The diversity of hesperornithiform taxa in terms of size, morphological features that
are interpreted as diving specializations, and the range of environments in which they
are preserved all point to habitat or trophic specializations among hesperornithiforms.
Interpretations of habitat preference for hesperornithiforms are limited to the depositional
environment in which their fossils were discovered. While these interpretations may not
precisely align with the environment in which these birds actually lived, some general
conclusions can be drawn. Hesperornithiforms are predominantly known from marine
environments, with some specimens known from continental and transitional environments
(Figure 12 and Table 2). As mentioned above, only in the latter half of the Late Cretaceous
(Campanian-Maastrichtian) do fossils occur in nonmarine sediments, thus suggesting a
possible colonization of these environments later in their evolutionary history. Body size
does not appear to correlate well with depositional environment, with large and small
taxa reported from continental, transitional, and marine environments. There may be an
underlying trend of large-bodied birds restricted to marine environments that is obscured
by taphonomic processes, particularly in regards to preservation in the reworked marine
Cambridge Greensand and Belle Fouche Formation.
Of particular interest is the overlap of multiple taxa in single geologic units such as
that seen in the Niobrara Formation and the Pierre Shale of the United States. Both of these
units are widely deposited deep-water marine sediments of the Western Interior Seaway,
with the older Niobrara Formation grading into the Pierre Shale in some places [
102
]. While
the number of taxa reported may be inflated (see Section 3above), the range of body sizes
preserved in both is striking, with the small Baptornis and Fumicollis, the large H. regalis,
and taxa such as Parahesperornis of intermediate size, known from the Niobrara Formation,
and some of the smallest Hesperornis species, H. lumgairi and H. macdonaldi, found with
large species such as H. chowi and H. regalis in the Pierre Shale. This juxtaposition should
not necessarily be interpreted as direct evidence of niche partioning, as it may result in full
or part from taphonomic processes or time averaging. However, it does raise the possibility
of ecological specializations to reduce interspecific competition. Ecologic niche segregation
is common among modern diving birds in which sympatric species differentiate in either
diet (prey type) or foraging range [103].
Diversity 2022,14, 267 24 of 28
7. Summary and Future Directions
Hesperornithiforms became the first birds (and dinosaurs) to adapt to a fully aquatic
lifestyle. A number of morphological features highlight this evolutionary pathway, re-
sulting in a highly streamlined body optimized for diving through the water, propelled
by powerful hindlimbs. Adaptations include an elongate neck that allowed for increased
maneuverability of a skull with sharp teeth and an expanded rostrum, ideal of capturing
fish and other mobile prey. The pelvis was also elongate, allowing for the attachment of
larger muscles for powering the feet. The femur was reduced to varying degrees in the
different species of hesperornithiform, but the shortened length and horizontal articulation
with the pelvis allowed for the orientation of the feet in line with and directly behind
the body, optimizing power production by reducing drag. As evidence of the degree to
which these birds optimized foot-propelled diving, the forelimbs of all hesperornithiforms
were reduced to the point of flightlessness, with the hesperornithids showing the most
extreme reduction.
This suite of morphological adaptations are present in varying degrees among the dif-
ferent specimens assigned to the group, suggesting a progression of diving specializations
and even the evolution of niche partitioning among these birds. This is supported by the
many geologic units where multiple species showing ranges in size and interpreted diving
capabilities have been discovered.
The broad morphological diversity present among hesperornithiform specimens has
been interpreted as representing an increasing number of taxa over the years. These tax-
onomic interpretations are complicated by the highly fragmentary nature of the fossil
record of these birds. While the addition of more specimens, particularly of the most basal
taxa, through future fieldwork is something to look forward to, there remains much to
be done with the existing global collection of specimens. Much of the taxonomic work
published to date has been limited to the geographic area of the authors (i.e.,
[13,47,56]
)
or relied on photographs and loans of select specimens (i.e., [
15
,
24
,
50
]). Very few studies
have incorporated direct observations of unpublished material from multiple continents,
but even these studies were not able to access much of the Asian and Canadian material
(i.e., [
22
,
25
,
65
]). Digitization and publication of a more complete record of current mu-
seum collections as measurements, photographs, written morphological descriptions, and
three-dimensional datasets such as those from computed tomography or laser scans, would
enable broad-scale studies not limited by geography (or travel funds). Such studies could
test taxonomic hypotheses that have remained largely untested over the past 150 years of
taxonomic work. The creation of digital specimens might also enable digital reconstruc-
tions of the skulls, which are disarticulated and often deformed to some degree. Such
reconstructions might provide insight into the shape of the hesperornithiform brain and
allow comparisons to Mesozoic and modern birds as well as inferences about the sensory
capabilities of these birds.
While much of the modern work on these birds has focused on taxonomy (e.g.,
[15,24,50,58]
)
or ecology [
22
,
94
,
101
], very little has been done regarding the ontogeny of these birds [
98
].
Additionally, histological studies might better inform taxonomic studies involving speci-
mens that range widely in size but have less variability in morphology, such as the species
of Hesperornis. There are a surprisingly large number of isolated hesperornithiform bones,
primarily from the hindlimb, in museum collections across North America, and addi-
tional histological work to characterize growth patterns and rates as well as life history
as a whole seem to be a potentially fruitful line of inquiry, despite complications from
poor preservation.
In conclusion, taxonomic, phylogenetic, and paleoecologic studies on the Hesperor-
nithiformes for the past 150 years have led us to an understanding of these birds as a
fascinating chapter in adaptive evolution. Hesperornithiforms are the first group of marine
diving birds to evolve, and while the origins of this group remain elusive, a large body of
work documents their spread across Laurasia and their expansion from marine to estuarine
Diversity 2022,14, 267 25 of 28
and even to freshwater environments by the Maastrichtian. While we have a large body of
previous research on these birds, there is much to be done in the future.
Author Contributions:
Conceptualization, literature review, and initial draft of the manuscript and
figures were drafted by A.B. Conceptualization, contribution to the manuscript, and review was
provided by L.M.C. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded in part by a generous donation from the Augustyn Family.
Acknowledgments:
The authors would like to thank Stephanie Abramowicz for assistance with
figures as well as the collections management staff at all of the museums for their assistance with
accessing specimens.
Conflicts of Interest: The authors declare no conflict of interest.
Abbreviations
AMNH, American Museum of Natural History, New York, NY, USA; IZASK, Institute of
Zoology, Ministry of Science, Almaty, Kazakhstan; KUVP, University of Kansas Museum of Nat-
ural History, Lawrence, KS, USA; LACM, Natural History Museum of Los Angeles County, Los
Angeles, CA, USA
; MCM, Mikasa City Museum, Mikasa, Japan; RSM, Royal Saskatchewan Museum,
Regina, SK, Canada; SDSM, Museum of Geology, South Dakota School of Mines and Technology,
Rapid City, SD, USA; UNSM, University of Nebraska State Museum, Lincoln, NE, USA; YPM, Yale
Peabody Museum, New Haven, CT, USA; YPM PU, Princeton University (collections now housed in the
Yale Peabody Museum).
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... B 289: 20221398 occiputs, particularly when compared with the primarily terrestrial/arboreal landbird clade Inopinaves (figure 8) [46,47]. Both Enaliornis (a foot-propelled diver, [48,49]) and Cerebavis have been hypothesized to have exhibited water-linked ecologies, along with much of the avian stem lineage crownward of Enantiornithes [24], which could therefore underlie their lower degree of ventralization with respect to MPM-334-1. ...
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Asian hesperornithiforms are extremely rare in contrast to the much more abundant record from North America. In Asia, these fossil birds are only known from fragmentary materials from Mongolia. Here we describe the skeletal remains of a new hesperornithiform Chupkaornis keraorum gen. et sp. nov. from the Upper Cretaceous Kashima Formation (Coniacian to Santonian) of the Yezo Group in Mikasa City, Hokkaido, Japan. This is the best-preserved hesperornithiform material from Asia and it is the first report of hesperornithiforms from the eastern margin of the Eurasian continent. Chupkaornis has a unique combination of characters: finger-like projected tibiofibular crest of femur, deep, emarginated lateral excavation with a sharply defined edge of the ventral margin of the thoracic vertebrae, and the heterocoelous articular surface of the thoracic vertebrae. Our new phylogenetic analysis revises the phylogenetic relationships of Hesperornithiformes. In contrast to previous studies, Enaliornis is assigned as the most basal taxon and Baptornis is positioned as more derived than Brodavis. Chupkaornis is a sister taxon to the clade of Brodavis and higher taxa. Parahesperornis and Hesperornis are positioned within Hesperornithidae, the derived Hesperornithiformes. Many of the skeletal character changes are concentrated at the base of Hesperornithidae (Parahesperornis and more derived taxa), and involve the modification of the pelvic girdle and hind limb morphology (e.g. dorsal directed antitrochanter of pelvis, short and sprawled femur, including probable lobe-toed feet suggested by the specialized distal articular surface of first digit of fourth toe, and predominantly robust digit IV phalanges). These skeletal modifications are likely adaptations for foot-propelled diving behaviour. http://zoobank.org/urn:lsid:zoobank.org:pub:FB783237-E565-4B74-9386-EADF8E12DFD4 © The Trustees of the Natural History Museum, London 2017. All rights reserved.