Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
Feeding biomechanics in Acanthostega
and across the fish –tetrapod transition
James M. Neenan1, Marcello Ruta2, Jennifer A. Clack3 and Emily J. Rayfield4
1
rspb.royalsocietypublishing.org
Research
Cite this article: Neenan JM, Ruta M, Clack
JA, Rayfield EJ. 2014 Feeding biomechanics in
Acanthostega and across the fish – tetrapod
transition. Proc. R. Soc. B 281: 20132689.
http://dx.doi.org/10.1098/rspb.2013.2689
Received: 15 October 2013
Accepted: 28 January 2014
Subject Areas:
palaeontology, biomechanics, evolution
Keywords:
Acanthostega, feeding, finite-element analysis,
geometric morphometrics, phylogeny,
fin – limb transition
Author for correspondence:
Emily J. Rayfield
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.2689 or
via http://rspb.royalsocietypublishing.org.
Palaeontological Institute and Museum, University of Zurich, 8006 Zurich, Switzerland
School of Life Sciences, University of Lincoln, Lincoln LN2 2LG, UK
3
University Museum of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
4
School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK
2
Acanthostega is one of the earliest and most primitive limbed vertebrates. Its
numerous fish-like features indicate a primarily aquatic lifestyle, yet cranial
suture morphology suggests that its skull is more similar to those of terrestrial taxa. Here, we apply geometric morphometrics and two-dimensional
finite-element analysis to the lower jaws of Acanthostega and 22 other tetrapodomorph taxa in order to quantify morphological and functional changes
across the fish –tetrapod transition. The jaw of Acanthostega is similar to that
of certain tetrapodomorph fish and transitional Devonian taxa both morphologically (as indicated by its proximity to those taxa in morphospace) and
functionally (as indicated by the distribution of stress values and relative
magnitude of bite force). Our results suggest a slow tempo of morphological
and biomechanical changes in the transition from Devonian tetrapod jaws
to aquatic/semi-aquatic Carboniferous tetrapod jaws. We conclude that
Acanthostega retained a primitively aquatic lifestyle and did not possess
cranial adaptations for terrestrial feeding.
1. Introduction
Biomechanical aspects of the origin of limbed vertebrates (tetrapods) add significantly to our knowledge of key structural, functional and ecological changes
underpinning a major animal radiation [1,2]. In particular, the analysis of feeding mechanisms at the fish–tetrapod transition permits in-depth exploration of
adaptive shifts during the assembly of the first terrestrial food webs and the colonization of new terrestrial habitats. In this paper, we analyse the lower jaw
biomechanics of Acanthostega gunnari from the Devonian of Greenland [3], one
of the most informative early limbed vertebrates, and a range of tetrapodomorph
taxa spanning the fish–tetrapod transition.
Acanthostega plays a central role in debates about terrestrialization [4].
Morphological and palaeoecological data suggest that this tetrapod had a primarily (if not exclusively) aquatic lifestyle. Its branchial skeleton, lateral line
system, elbow and wrist joint constructions (indicative of a paddling rather
than a weight-bearing function), weakly developed vertebral zygapophyses
and extensive tail fin are all consistent with this interpretation [5,6]. In addition,
its broad snout suggests that this tetrapod relied on suction as a feeding mechanism [7–10]. Finally, lithological and sedimentological data indicate that
Acanthostega inhabited an ephemeral, shallow and weakly channelized fluvial
system subjected to periodic intense flooding [11 –15].
In contrast, certain structural traits of Acanthostega appear to be in conflict
with its interpretation as an aquatic animal. In particular, a recent study has
shown that its complex and interdigitated cranial sutures [16] closely resemble
those of terrestrial taxa and are not consistent with an aquatic feeding mode
[17]. The cross-sectional shape of cranial sutures is a useful tool for identifying
different types of stress and strain in the vertebrate skull. For example, miniature pigs [18,19], goats [20] and fish [21] display complex interdigitating
cranial sutures to withstand tension, simple abutting sutures to counteract
tension and overlapping sutures to work simultaneously against tension and
compression. Comparisons of the cranial sutures of Acanthostega to those of
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
(a) Phylogeny
The tree in figure 1a (for alternative schemes of early tetrapod
interrelationships, see [28]) was time-calibrated with methods
available at: http://www.graemetlloyd.com/methdpf.html. Tree
branch lengths were scaled based on first appearance data for all
taxa. Branches with identical first appearances are allowed to
share a proportion of the time elapsed between their first appearance and that of an earlier branch. As a result, no branches have
zero-length duration [29,30]. Branch scaling allowed us to measure
‘phylogenetic distances’ between all pairs of taxa in millions of
years. These distances were used in correlations with biomechanical and morphological distances (see below). This approach
allowed us to assess the degree of intertaxon separation (both functional and morphological) based on time elapsed since the time of
divergence of any pair of taxa.
(b) Jaw reconstructions
The use of published jaw reconstructions (figure 1b; electronic
supplementary material, table S1) maximizes the amount of
information rarely observed in individual specimens owing to
incompleteness or deformation [30]. Taxon selection was determined in part by the reliability of the jaw reconstructions, assessed
through either first-hand observations of material or comparisons
with accompanying photographs in relevant publications. Different
jaw reconstructions are available for Ichthyostega, Crassigyrinus,
Megalocephalus and Gephyrostegus, so these reconstructions were all
included in our analyses to assess their impact on our results.
(b)
Rhizodus
Megalichthys
2
VM stress
(MPa)
0
Eusthenopteron
Panderichthys
Tiktaalik
1.25
2.50
Elginerpeton
Densignathus
3.75
Ventastega
Metaxygnathus
5.00
Acanthostega
Ymeria
Ichthyostega
Whatcheeria
Crassigyrinus
Greererpeton
Megalocephalus
Gephyrostegus
Eoherpeton
Proterogyrinus
Silvanerpeton
Balanerpeton
Dendrerpeton
Phonerpeton
Figure 1. (a) Simplified cladogram for the 23 taxa used in this study; groups
are colour-coded as follows: blue, tetrapodomorph fish; red, Devonian stem
tetrapods; orange, aquatic/semi-aquatic Carboniferous stem tetrapods; green,
anthracosaurs; purple, temnospondyls. (b) VM stress distribution in 28 jaw
models with a muscle vector of 608, drawn to the same length and with
stress values colour-coded as in inset scale.
(c) Two-dimensional finite-element analysis
We could not apply three-dimensional FEA owing to a lack of
computed tomography (CT) data and the laterally crushed or fragmentary nature of most specimens. Two-dimensional models
allow us to sample a broader range of taxa but treat the mandible
as a thin plate and thus assume that stresses and strains act only in
the sagittal plane. Therefore, a limitation of the methodology used
in our study is that some details of constructional differences
among different jaws could not be taken into account. These differences include, among other features, sutural patterns of dermal
bones, proportions and degree of ossification of the Meckelian
element and size of coronoid fangs [31–33]. We acknowledge
that such constructional differences may have had a substantial
effect on the overall jaw biomechanics. However, two-dimensional
FEA permits a comparative analysis of the performance of jaw
shape without having to estimate precise values of material properties, muscle forces, muscle fibre distributions or yield/failure
stresses, all of which have been shown by recent validation studies
to be difficult to estimate even in extant taxa [34]. Furthermore,
we assume that the taxa in our study were capable of performing
simple orthal jaw movements, although the jaw musculature itself
may have undergone some degree or reorganization at the fish–
tetrapod transition (this is borne out by the observation that
the adductor fossa changes in shape and proportions at the
fish–tetrapod transition [23]). Orthal movements imply that
dorsoventral bending is chiefly responsible for the primary stress
and strain occurring during jaw closure and prey capture. Using
Proc. R. Soc. B 281: 20132689
2. Material and methods
(a)
rspb.royalsocietypublishing.org
the extant actinopterygian Polypterus, the Devonian tristichopterid sarcopterygian Eusthenopteron and presumably terrestrial
Permian temnospondyl Phonerpeton have led some researchers
to conclude that Acanthostega may have favoured direct biting in
a sub-aerial environment as a means of prey capture [17]. In this
context, it is therefore logical to ask whether other morphological traits of this tetrapod support this conclusion. Here,
we examine the argument in support of a terrestrial feeding
mode in Acanthostega by analysing its lower jaw from both
morphological and functional standpoints. Furthermore, we
compare the biomechanical performance of its jaw with those
of various other early tetrapods and near-tetrapod taxa that
span the fish–tetrapod transition.
We focus on the lower jaws because they are both easily
constrained from a functional perspective (that is, they are
predominantly feeding structures) and preserved very well in
numerous taxa. For these reasons, they are amenable to combined biomechanical and morphometric analyses. We apply
two-dimensional finite-element analysis (FEA) and geometric
morphometrics to the lower jaws of 23 taxa. These include:
(i) a sample of rhizodontid, megalichthyid and tristichopterid
tetrapodomorphs, representing the fish-like portion of the
tetrapod stem; (ii) the best-known Devonian digit-bearing
tetrapods, including Acanthostega; (iii) a number of Carboniferous aquatic/semi-aquatic stem tetrapods and (iv) some
anthracosaurs and temnospondyls, as putative members of the
amniote and amphibian stem groups, respectively (figure 1a;
electronic supplementary material, table S1). Stem- and crowngroup attributions differ in recent analyses of early tetrapod
interrelationships. Here, we follow broadly the scheme of
relationships in [22], with amendments and additions from
[23–26]. Jaw orientation and descriptive terminology conform
to [23,27].
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
(d) Geometric morphometrics
We applied landmark-based geometric morphometric methods to
explore shape variation in our taxon sample. Twelve landmarks on
the lateral surface of each jaw were digitized in 21 taxa using IMAGEJ
[42] (electronic supplementary material, table S3; inset, figure 3).
Two taxa were excluded from the morphometric analyses,
namely Tiktaalik, in which certain landmark positions could not
be discerned, and Dendrerpeton, in which the splenial and postsplenial have little or no exposure on the lateral aspect of the jaw.
Landmarks conform to Bookstein’s [43] types 1 and 3 (electronic
supplementary material, table S3; type 1: landmarks identifying
homologous points, for example triple joints among bones; type
3: landmarks placed at ‘extremes’ of a structure, for example
most anterior end of a given distance). Morphometric analyses
were performed in PAST [44].
(e) Comparisons among distance matrices
We further carried out traditional and modified Mantel tests [44,45]
to establish the degree of correlation among intertaxon distance
matrices generated from the functional analyses, morphometric
analyses and consensus phylogeny (see the electronic supplementary material, methods). Note that the morphological distances are
the Procrustes distances derived from the morphometric analysis,
whereas the phylogenetic distances are the temporal distances
that separate any two taxa along the time-calibrated branch lengths
of the preferred phylogeny. The traditional Mantel tests simply
considered pairwise correlations between any two of the three distance matrices. The modified Mantel test was conducted on
morphological and functional distances while taking phylogeny
into account, using codes supplied in [45].
3. Results
(a) von Mises stress
Stress values are reported here based on the overall patterns
observed across the jaw and the mean values recorded from
the dorsoventrally orientated mid-tooth row transect during
a simulated bite. The VM stress values recorded in the
3
Proc. R. Soc. B 281: 20132689
Furthermore, the anteriormost end of the tooth row was constrained in the Y-axis (five nodes) to simulate a bite. We then
derived values for VM stress, which was measured at five evenly
spaced points along a dorsoventral transect situated at the
middle of the tooth row (electronic supplementary material,
figure S1; [39]). VM stress is a function of the three principal
stress directions along the X-, Y- and Z-axes and effectively predicts failure in a structure [40]. In addition, we recorded reaction
forces from five restrained nodes at the anteriormost end of the
tooth row in order to provide an estimate of ‘bite force’ for each
model, which we name a ‘relative’ bite force as our input muscle
forces are scaled to the surface area. As our models have muscle
loads scaled in proportion to the jaw surface area, relative bite
forces allow us to use reaction force as a proxy for jaw performance
(figure 2). For taxa with more than one model (i.e. Ichthyostega,
Crassigyrinus, Megalocephalus and Gephyrostegus), relative bite
forces were measured for each model individually to derive a
mean value. We then calculated relative bite force as a proportion
of Acanthostega bite force. Finally, we compared bite ‘efficiency’ by
calculating the ratio of relative bite force to the scaled muscle input
force. This provides a size-independent measure of how effectively
jaw shape converts applied muscle load to output bite force [41]. In
addition, to ensure our models contained enough elements to provide reliable results, a convergence test was performed on the jaw
of Acanthostega (electronic supplementary material, figure S2).
rspb.royalsocietypublishing.org
this approach, we assume that both mediolateral bending and
torsional loads exerted a negligible effect on the jaw.
It may be argued that the simplifications and assumptions of our
models may be unwarranted or biologically unrealistic. However,
our analysis of the distribution of forces along the sagittal plane
(as stated above) is a first pass towards a more detailed treatment
of jaw biomechanics that also accounts for details of constructional
differences (research in progress by Laura Porro, E.J.R. and J.A.C.).
Crucially, our protocols are not conceptually different from those
adopted in other studies [30], where certain traits of a morphofunctional complex (e.g. input and output moment arms of lower jaws
treated as ‘levers’ in [30]) are considered as specific variables in
isolation from constructional details of those complexes.
Digitized jaw outlines were used to build FE models and these
were constructed and analysed in COSMOSM v. 2.0 (Dessault Systemes, MA, USA). Jaws were scaled to their correct size using
published measurements. Adductor muscle loads were then
added and scaled. We assigned a hypothetical adductor muscle
force of 10 N to Acanthostega, herein referred to as the Acanthostega
unit force. We then scaled this load for each jaw according to its surface area, following the protocol suggested and employed in
recent comparative FE studies, where validation or data on
input parameters are either unknown or difficult to obtain, for
example in fossil taxa [35]. Applying a constant unit force per surface area has the advantage of removing the effect of size, so that
only the effect of shape on jaw performance is quantified. This
method makes the assumption that muscle cross-sectional area
(and hence isometric force output) scales to jaw surface area. It
is important to note that this technique does not provide a measure
of the ecological performance of specimens; however, it does provide a comparative analysis of shape mechanical performance.
Therefore, the resulting von Mises (VM) stress values should not
be interpreted as the actual stresses experienced by the jaws, but
instead represent comparative performance values. If we assume
that all specimens operate to a common safety factor (the ratio
between everyday load and load at failure), then tetrapods in
which the jaws experience low stress (as recorded in our analysis)
could, in theory, be capable of biting harder than predicted by
exerting a stronger adductor muscle force. Conversely, jaws that
experience high stress (as recorded in our analysis) could, in
theory, be capable of generating smaller input forces in life and
hence generate lower bite forces than predicted. We have chosen
this approach, rather than applying an incremental load until a
nominal safety factor is reached, because it allows us to determine
which taxa deviate from a simple relationship between surface
area and jaw muscle force. Furthermore, it is not clear whether
skulls and jaws of different taxa operate at similar safety factors.
Recent in vivo strain data from mammals, lizards and crocodilians
show marked variation in peak cranial strains between taxa,
suggesting that these animals operate at very different cranial
safety factors [36 – 38]. Additionally, it can be problematic to
record performance metrics from peak stresses in FE models,
as these stresses may be localized peaks at constraint points and
may not reflect accurately the mechanical behaviour of the structure. The alternative approach of estimating a realistic adductor
muscle force for each taxon is problematic, as a number of specimens do not possess adequately preserved cranial material to
assess muscle size and orientation. Muscle loads were applied at
an angle of 608 to a horizontal axis between the tip of jaw and
articular surface. This angle was selected following sensitivity
analyses that considered varying muscle vector orientations (see
the electronic supplementary material, methods and figure S1).
Material properties were then applied to the model. However,
as no material property data for fish or amphibian skulls are
available, we selected the Young’s modulus of the pelvic metapterygium of the actinopterygian fish Polypterus (17.6 GPa [7]) and
applied an average Poisson’s ratio of 0.35. The jaws were constrained at the condyle in three translational degrees of freedom.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
1. Rhizodus
2. Megalichthys
3. Eusthenopteron
4. Panderichthys
5. Tiktaalik
6. Elginerpeton
7. Densignathus
8. Ventastega
9. Metaxygnathus
10. Acanthostega
11. Ymeria
12. Ichthyostega
13. Whatcheeria
14. Crassigyrinus
15. Greererpeton
16. Megalocephalus
17. Gephyrostegus
18. Eoherpeton
19. Proterogyrinus
20. Silvanerpeton
21. Balanerpeton
22. Dendrerpeton
23. Phonerpeton
taxa
0.35
bite ‘efficiency’
0.30
0.25
0.20
0.15
0.10
0.05
1. Rhizodus
2. Megalichthys
3. Eusthenopteron
4. Panderichthys
5. Tiktaalik
6. Elginerpeton
7. Densignathus
8. Ventastega
9. Metaxygnathus
10. Acanthostega
11. Ymeria
12. Ichthyostega
13. Whatcheeria
14. Crassigyrinus
15. Greererpeton
16. Megalocephalus
17. Gephyrostegus
18. Eoherpeton
19. Proterogyrinus
20. Silvanerpeton
21. Balanerpeton
22. Dendrerpeton
23. Phonerpeton
0
taxa
mean VM stress (MPa)
(c) 1.8
1.6
1.4
1.2
1.0
0.8
7
0.6 23 10
12
11
0.4 22 91883
21 20
0.2
2
17
0
6
Megalichthys experienced the least stress, particularly in the
anterior half of the jaw (mean of the stress recorded in the
mid-tooth row transect ¼ 0.21 and 0.16 MPa, respectively).
Marginally higher stresses were observed in the anterior jaw
in the more derived tetrapodomorph, Eusthenopteron, which
exhibited very similar mean transect stress values to those of
most Devonian tetrapods. The highest values among fish
occurred in Tiktaalik and Panderichthys (transect means ¼ 0.69
and 1.18 MPa, respectively) and were similar in magnitude to
those of Carboniferous tetrapods.
Among Devonian tetrapods, Elginerpeton experienced by
far the highest stress value at every point in the jaw (transect
mean ¼ 1.71 MPa). All other Devonian tetrapods, including
Acanthostega, showed much lower values; stresses were more
uniformly distributed across the jaw and had less variable
transect means (0.38–0.66 MPa). Acanthostega has an estimated
average value of 0.58 MPa at the mid-tooth row transect, well
within the range of two of the Ichthyostega models [23], both
of which show similarly distributed and comparable values
(transect means ¼ 0.50 and 0.63 MPa).
The Carboniferous semi-aquatic/aquatic stem amniotes consistently showed the highest stresses of all tetrapods, and also
resembled each other in terms of mean stresses at the transect.
The more terrestrial anthracosaurs, particularly Gephyrostegus,
exhibited low stress (means ¼ 0.16 and 0.23 MPa for the two
jaw models). Proterogyrinus emerged as an outlier (mean ¼
1.01 MPa), showing a much higher value than any other anthracosaur and resembling closely Carboniferous stem tetrapods.
Terrestrial temnospondyls generally showed low stresses,
with average values being lower than those of the Devonian
tetrapods. Phonerpeton is an exception, as its mean value
(0.48 MPa) was similar to that of the Devonian tetrapods,
especially Ichthyostega.
14
(b) Relative bite force and efficiency
4
19
13
15
5
16
1
2
4
6
8
10
mean relative BF as a proportion of Acanthostega BF
Figure 2. Biomechanical performance of jaws, colour-coded as in figure 1.
(a) Mean relative bite force measurements for each taxon as a proportion
of Acanthostega bite force. (b) Bite ‘efficiency’ of each taxon; note the
high efficiency in temnospondyl taxa despite low relative bite force. For
taxa with more than one model and thus efficiency value, the mean was
used. (c) Mean relative bite force as a proportion of Acanthostega bite
force, plotted against mean VM stress; numbers correspond to taxa shown
in (a) and (b); note the linear relationship between stress and bite
force, except for the outlying positions of Megalocephalus and Rhizodus.
BF, bite force.
mid-tooth row transect followed a distinct trend (figure 1b; electronic supplementary material, table S2). Maximum values
occurred at the dorsal and ventral edges of the jaw (0% and
100% points, respectively); values decreased through the 25
and 75% quartile points up to the jaw mid-point (50%), where
the lowest value was recorded. At the base of tetrapodomorph
sarcopterygians, the rhizodont Rhizodus and the megalichthyid
Carboniferous stem tetrapods recorded by far the highest
relative bite forces of all (n ¼ 4; mean ¼ 7.69 N; s.d. ¼ 4.98;
Crassigyrinus ¼ 10.6 N; Megalocephalus ¼ 13.2 N; electronic
supplementary material, figure S3a and table S2). Relative
bites for Crassigyrinus and Megalocephalus were 6.24 and eight
times greater than relative bites in Acanthostega, respectively
(figure 2a). The next highest values occurred in sarcopterygians
(n ¼ 5; mean ¼ 4.45 N; s.d. ¼ 2.46): Rhizodus, Panderichthys
and Tiktaalik showed, respectively, the fourth, fifth and sixth
most powerful relative bite forces at 4.61, 3.72 and 2.64 times
greater than Acanthostega relative bites. Devonian tetrapods
were next in sequence (n ¼ 5; mean ¼ 2.85 N; s.d. ¼ 0.42).
A relative bite force of 9.67 N was estimated for Elginerpeton,
which had the third highest value overall. At 5.86 times
the relative bite of Acanthostega, it had a greater bite than
other Devonian tetrapods included here (all with values
lower than 2 N; e.g. 1.65 N in Acanthostega). Terrestrial taxa
recorded the lowest values of all, ranging from nearly equivalent to Acanthostega in Eoherpeton, to 12% of Acanothstega relative
bite force in Gephyrostegus (figure 2a; electronic supplementary material figure S3a and table S2) (anthracosaurs:
n ¼ 4; mean ¼ 1.31 N; s.d. ¼ 1.22; temnospondyls: n ¼ 3;
mean ¼ 0.58 N; s.d. ¼ 0.44).
The three temnospondyls possessed the most efficient jaw
shape in terms of the ability to transfer jaw muscle input force
to bite force (figure 2b; see Material and methods). The anthracosaur Proterogyrinus and the stem tetrapod Crassigyrinus also
4
Proc. R. Soc. B 281: 20132689
(b)
9.0
8.0
7.0
6.0
5.0
4.0
3.0
2.0
1.0
0
rspb.royalsocietypublishing.org
mean relative BF as a proportion
of Acanthostega BF
(a)
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
0.2
5
Proterogyrinus
Silvanerpeton
0.1
Ichthyostega 80
0.2
0.3
Greererpeton
Gephyrostegus
Panderichthys
–0.1
Megalichthys
Rhizodus
Eusthenopteron
Phonerpeton
2
1
12
3
10
–0.2 PC1
4
8
11
6
5
7
9
Figure 3. Plot of principal components 1 and 2, which account for 68.08% of the total morphological variance; colour key is the same as in figure 1; Ichthyostega
80 is from [50] and Ichthyostega 96 is from [51]. Inset shows the jaw of Acanthostega, redrawn from [23], with the position of the 12 landmarks used in the
morphometric analysis (landmark descriptions can be found in the electronic supplementary material, table S3).
had moderately efficient jaws. Acanthostega clustered with
other Devonian tetrapods, Metaxygnathus and Densignathus,
and was mid-range in terms of its efficiency. The Devonian
tetrapods Ventastega, Ymeria and Ichthyostega, and the large
tetrapodomorph fish Rhizodus and Megalichthys, were the
least efficient.
Relative bite force values and mean VM stress values are
significantly correlated (Spearman’s r ¼ 0.68182, p ¼ 0.00034;
figure 2c; electronic supplementary material, S3b). However,
Megalocephalus and Rhizodus exhibited lower VM stress than
predicted from bite forces.
(c) Morphometric analysis
Principal components (PC) 1 and 2 accounted for 45.13% and
22.95% of the total morphological variance, respectively
(figure 3). Each group plotted in a distinct region of morphospace, with the exception of Elginerpeton, which fell within the
convex hull delimited by semi-aquatic/aquatic Carboniferous
tetrapods. Acanthostega plotted closer to some Devonian tetrapods, but some distance from Ichthyostega and Elginerpeton.
Devonian and Carboniferous tetrapods are not significantly
separate (non-parametric multivariate analysis of variance or
NPMANOVA [44]; F ¼ 4.282, p ¼ 0.08), even if Elginerpeton is
removed. Tetrapodomorphs were distributed chiefly along
PC2 owing to differences in jaw curvature between rhizodonts
and megalichthyids (with straight jaws and tooth rows), at positive PC2 values, and Panderichthys and Eusthenopteron (with
more curved jaws and tooth rows), at negative PC2 values.
The latter two taxa plotted closer to Ichthyostega. Sarcopterygian
fish and Devonian tetrapods were significantly separate
(NPMANOVA; F ¼ 4.282, p ¼ 0.007), probably owing to the
broad separation of rhizodonts and megalichthyids from
other tetrapodomorphs. The anthracosaurs were distributed
mostly along PC1 and were well separated from most other
groups except rhizodonts, megalichthyids and temnospondyls.
The two temnospondyl taxa, however, were not close to each
other in morphospace. Although they were almost aligned in
a direction parallel to PC2, they plot at nearly opposite ends
of PC1 and only show significant separation from the Devonian
taxa (NPMANOVA; F ¼ 4.282, p ¼ 0.04).
(d) Shape –function correlation
With traditional Mantel tests [44], the stress-based (functional)
distances were not significantly correlated with either morphological (Pearson’s r ¼ 0.01411; p ¼ 0.4136) or phylogenetic
distances (Pearson’s r ¼ 20.1048; p ¼ 0.7262). However, the
correlation between morphological and phylogenetic distances was significant (Pearson’s r ¼ 0.4066; p ¼ 0.0013).
With the modified Mantel test [45], we found that, once
again, the stress-based and morphological distances were not
significantly correlated (Pearson’s r ¼ 0.01411; p ¼ 0.3882).
4. Discussion
It is important to reiterate here that our analysis is comparative, and that relative bite forces and stress values are used for
this purpose, and do not reflect the absolute magnitude of
stress and force experienced or generated by the jaw.
(a) Bite performance
Mechanically, the semi-aquatic/aquatic Carboniferous stem
tetrapods (Crassigyrinus, Megalocephalus) exerted by far the
strongest relative bites, consistent with their powerful jaws
and massive teeth. Anthracosaurs and temnospondyls
showed, on average, the weakest relative bites and appear
Proc. R. Soc. B 281: 20132689
Metaxygnathus
Densignathus
Elginerpeton
Megalocephalus
–0.1
Ichthyostega 96
Eoherpeton
Crassigyrinus
PC2
–0.2
0.1
Balanerpeton
Ymeria
Ventastega
Acanthostega
rspb.royalsocietypublishing.org
Whatcheeria
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
Jaw curvature (changing mostly along PC2) and proportion
of tooth row length relative to total jaw length (changing
mostly along PC1) define the pattern of taxon distribution
in morphospace. Some Devonian tetrapods share similarities
(c) Form, function and phylogeny
As comparative jaw stress does not appear to be correlated
with morphology, jaw shape alone cannot be used to infer
its function. Convergent biomechanical performances can
be achieved with different morphologies. Notable examples
are Acanthostega and Phonerpeton. These taxa are both phylogenetically separate and morphologically distinct, yet their
jaw performances are similar. Functional distances from comparative jaw stress values do not correlate with phylogenetic
distances. We interpret this result as evidence of divergent
functions in closely related species (e.g. Elginerpeton and
other Devonian tetrapods; Crassigyrinus and Megalocephalus
and other Carboniferous, aquatic/semi-aquatic tetrapods),
though comprehensive analyses of biting performance evolution must await data collection from a larger taxon sample
than that used here. By contrast, morphological and phylogenetic distances correlate well, implying that, at least for
our sample, morphology is constrained to some degree by
taxon position in phylogeny.
(d) Feeding in Acanthostega
With the exception of Elginerpeton, Acanthostega plots out in
proximity to other Devonian taxa, which it also resembles
mechanically (figures 1b, 2 and 3). In terms of average VM
stress, its lower jaw shape resembles that of Ichthyostega,
has similar relative bite force to Ventastega and Densignathus
and similar relative bite efficiency to Densignathus and
Metaxygnathus. Devonian tetrapods share similarities in overall
jaw shape with Panderichthys and Eusthenopteron as well as
Carboniferous aquatic/semi-aquatic forms, providing limited
evidence for notable morphological change in jaw morphology
across the fish–tetrapod transition. There are some functional
differences, however; for example, Carboniferous forms, such
as Crassigyrinus and Megalocephalus, generate greater relative
bite forces than Devonian taxa, but at the expense of increased jaw stress. As Devonian tetrapods (with the exception of
Elginerpeton) tend to have low relative bite forces and concomitant lower jaw stress, this places their functional capabilities
midway between those of aquatic Carboniferous forms and
those of anthracosaurs and temnospondyls. Devonian tetrapod
jaws are therefore not functioning in exactly the same manner
as aquatic Carboniferous tetrapod jaws, but certainly do not
conform functionally to terrestrial tetrapod jaws either. Given
6
Proc. R. Soc. B 281: 20132689
(b) Jaw shape
in lower jaw morphology with Carboniferous aquatic/semiaquatic tetrapods and with Eusthenopteron and Panderichthys
and are morpohologically distinct from anthracosaurs, temnospondyls, rhizodonts and megalichthyids. Shape changes along
PC2 are particularly noteworthy (figure 3), as tooth row curvature affects mechanical performance. The development of a
straight tooth row and the presence of a coronoid process
(e.g. Proterogyrinus, Eoherpeton, Gephyrostegus) imply that all
marginal dentary teeth are brought into contact with prey simultaneously in a vice-like manner. A similar jaw action may
have characterized the stem tetrapod Greererpeton, and the rhizodonts and megalichthyids. Conversely, a curved jaw with an
upturned tip brings the tip in contact with the prey first. This
could be interpreted as an adaptation for snapping feeding,
and a likely adaptation for dealing with fast prey. Posterior
inclination of the anteriormost teeth and fangs in these taxa
support the interpretation of a jaw adapted for fast closure
and prey seizure.
rspb.royalsocietypublishing.org
to have been capable of quick, snapping jaw movements
(figure 2a; electronic supplementary material, figure S3a).
Generally, relative bite force increases linearly with VM
stress, except in Megalocephalus, Rhizodus and Megalichthys,
all of which are outliers (figure 2c; electronic supplementary
material, figure S3b) and show relatively low stress for a given
relative bite force. Using these results, we can consider which
taxa are operating at notably high or low safety factors in our
comparative analysis. It might be predicted that in life such
taxa could have modified their feeding performance, by
either decreasing or increasing muscle force input, respectively, in order to equilibrate the stresses within their jaws.
Following this rationale, taxa can be divided into three
categories, as described below.
(i) Low-stress, high relative bite force. Two outlier taxa exhibited this pattern, the semi-aquatic Megalocephalus and the
fully aquatic Rhizodus. If all taxa are assumed to operate to
a similar safety factor, these taxa, in life, may have been
able to generate higher adductor input forces than modelled
here, thereby generating an increased bite force yet still operate within a margin of safety. Although not closely related,
both taxa possess cranial features suited for crushing and/
or stabbing relatively large prey [23,46,47].
(ii) High-stress, high relative bite force. The most basal tetrapod,
Elginerpeton, also exhibits the most divergent jaw morphology
of the group, possibly indicating a different feeding mode
[23,31,32]. This conclusion is supported by the mechanical performance of the jaw, which boasts a very high relative bite force
and by far the highest comparative stress levels recorded, probably owing to its narrow and elongate morphology. Again,
assuming similar safety factors, this taxon in life may have generated a reduced adductor muscle force, thereby lowering the
elevated stresses in the jaw. This slender jaw shows thickened
and tightly sutured dermal bones and a reduced Meckelian
space [23,31,32]. The overall construction is consistent with
quick, forceful movements through the water column, possibly
when the animal chased small, fast prey. Similar functional
considerations apply to the seemingly secondarily aquatic
Carboniferous tetrapod, Crassigyrinus [48,49]. Morphological evidence indicates that this animal was an extremely
agile aquatic predator. Its size, morphology, high bite force
and high efficiency are consistent with hunting large prey and
seizing it with a powerful bite.
(iii) Low-stress, low bite force. Some predominantly terrestrial
taxa show exceptionally low comparative jaw performance.
Examples include Gephyrostegus and Balanerpeton. Our results
indicate intrinsically different mechanical demands on skull
function, presumably owing to their postulated terrestrial lifestyle. Increasing adductor muscle force could have generated
an increased bite force within these taxa and maintained
skull stress within acceptable levels of safety. The majority of
Devonian taxa (including Acanthostega) and the fish Eusthenopteron plot fairly close to these terrestrial forms, but with slightly
higher average stresses and relative bite forces, intermediate
between those of terrestrial forms and those of sarcopterygian
fish and Carboniferous aquatic tetrapods.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
Acknowledgements. We thank P. Anderson, M. Bell, J. Bright, T. Fletcher and
M. Sakamoto for valuable discussions and input. We are also grateful to
two anonymous reviewers and to our Associate Editor, Prof. Peter Aerts,
whose comments greatly improved the manuscript. This study was
completed as part of J.M.N.’s MSc project at the University of Bristol.
References
1.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
of faunal composition and distribution. Geodiversitas
29, 119– 141.
Astin TR, Marshall JEA, Blom H, Berry CM. 2010
The sedimentary environments of the Late
Devonian East Greenland tetrapods. Geol. Soc.
Lond. Spec. Publ. 339, 93 – 109. (doi:10.1144/
SP339.9)
Clack JA. 2002 The dermal skull roof of
Acanthostega gunnari, an early tetrapod from the
Late Devonian. Trans. R. Soc. Edin. Earth Sci. 93,
17 –33. (doi:10.1017/S0263593302000020)
Markey MJ, Marshall CR. 2007 Terrestrial-style
feeding in a very early aquatic tetrapod is
supported by evidence from experimental
analysis of suture morphology. Proc. Natl Acad. Sci.
USA 104, 7134–7138. (doi:10.1073/pnas.
0701706104)
Rafferty KL, Herring SW. 1999 Craniofacial sutures:
morphology, growth, and in vivo masticatory strains.
J. Morphol. 242, 167– 179. (doi:10.1002/(SICI)10974687(199911)242:2,167::AID-JMOR8.3.0.CO;2-1)
Herring SW, Ochareon P. 2005 Bone: special
problems of the craniofacial region. Orthod.
Craniofac. Res. 8, 174–182. (doi:10.1111/j.16016343.2005.00328.x)
Jaslow CR. 1990 Mechanical properties of cranial
sutures. J. Biomech. 23, 313–321. (doi:10.1016/
0021-9290(90)90059-C)
Markey MJ, Main RP, Marshall CR. 2006 In vivo
cranial suture function and suture morphology
in the extant fish Polypterus: implications for
inferring skull function in living and fossil fish.
J. Exp. Biol. 209, 2085 –2102. (doi:10.1242/
jeb.02266)
Ruta M, Coates MI. 2007 Dates, nodes and character
conflict: addressing the lissamphibian origin
problem. J. Syst. Palaeontol. 5, 69 –122. (doi:10.
1017/S1477201906002008)
Ahlberg PE, Clack JA. 1998 Lower jaws, lower
tetrapods: a review based on the Devonian genus
Acanthostega. Trans. R. Soc. Edin. Earth Sci. 89,
11 –46. (doi:10.1017/S0263593300002340)
Ruta M, Jeffery JE, Coates MI. 2003 A supertree of
early tetrapods. Proc. R. Soc. Lond. B 270,
2507 –2516. (doi:10.1098/rspb.2003.2524)
Ahlberg PE, Clack JA, Lukševics E, Blom H, Zupinš I.
2008 Ventastega curonica and the origin of tetrapod
morphology. Nature 453, 1199– 1204. (doi:10.
1038/nature06991)
Clack JA, Ahlberg PE, Blom H, Finney SM. 2012 A
new genus of Devonian tetrapod from North-East
Greenland, with new information on the lower jaw
of Ichthyostega. Palaeontology 55, 73 –86. (doi:10.
1111/j.1475-4983.2011.01117.x)
27. Jeffery JE. 2003 Mandibles of rhizodontids:
anatomy, function and evolution within the
tetrapod stem-group. Trans. R. Soc. Edin. Earth Sci.
93, 255 –276.
28. Anderson JS. 2008 Focal review: the origin(s) of
modern amphibians. Evol. Biol. 35, 231 –247.
(doi:10.1007/s11692-008-9044-5)
29. Brusatte SL, Benton MJ, Ruta M, Lloyd GT. 2008
Superiority, competition, and opportunism in the
evolutionary radiation of dinosaurs. Science 321,
1485– 1488. (doi:10.1126/science.1161833)
30. Anderson PSL, Friedman M, Ruta M. 2013 Late to
the table: diversification of tetrapod mandibular
biomechanics lagged behind the evolution of
terrestriality. Integr. Comp. Biol. 53, 197–208.
(doi:10.1093/icb/ict006)
31. Ahlberg PE. 1991 Tetrapods or near-tetrapod fossils
from the Upper Devonian of Scotland. Nature 354,
298–301. (doi:10.1038/354298a0)
32. Ahlberg PE. 1991 Elginerpeton pancheni and the
earliest tetrapod clade. Nature 373, 420 –425.
(doi:10.1038/373420a0)
33. Ahlberg PE, Lukševics E, Lebedev O. 1994 The first
tetrapod finds from the Devonian (Upper
Famennian) of Latvia. Phil. Trans. R. Soc. Lond. B
343, 303–328. (doi:10.1098/rstb.1994.0027)
34. Bright JA, Rayfield EJ. 2011 Sensitivity and ex vivo
validation of finite element models of the domestic
pig cranium. J. Anat. 219, 456–471. (doi:10.1111/j.
1469-7580.2011.01408.x)
35. Dumont ER, Grosse IR, Slater GJ. 2009 Requirements
for comparing the performance of finite element
models of biological structures. J. Theor. Biol. 256,
96– 103. (doi:10.1016/j.jtbi.2008.08.017)
36. Ross CF, Metzger KA. 2004 Bone strain gradients
and optimization in vertebrate skulls. Ann. Anat.
186, 387–396. (doi:10.1016/S0940-9602(04)
80070-0)
37. Porro LB, Metzger KA, Iriarte-Diaz J, Ross CF.
2013 In vivo bone strain and finite element
modeling of the mandible of Alligator
mississippiensis. J. Anat. 223, 195– 227.
(doi:10.1111/joa.12080)
38. Porro LB, Ross CF, Iriarte-Diaz J, O’Reilly J, Evans SE,
Fagan MJ. In press. In vivo cranial bone strain and
bite force in the agamid lizard Uromastix geyri.
J. Exp. Biol.
39. Fletcher TM, Janis CM, Rayfield EJ. 2010 Finite
element analysis of ungulate jaws: can mode of
digestive physiology be determined? Palaeontol.
Electron. 13, 21A. See http://palaeo-electronica.org/
2010_3/234/index.html.
40. Dumont ER, Piccirillo J, Grosse IR. 2005 Finiteelement analysis of biting behavior and bone stress
Proc. R. Soc. B 281: 20132689
2.
Anderson PSL, Friedman M, Brazeau MD, Rayfield EJ.
2011 Initial radiation of jaws demonstrated stability
despite faunal and environmental change. Nature
476, 206–209. (doi:10.1038/nature10207)
Pierce SE, Clack JA, Hutchinson JR. 2012 Threedimensional limb joint mobility in the early
tetrapod Ichthyostega. Nature 486, 523–526.
Jarvik E. 1952 On the fish-like tail in the
ichthyostegid stegocephalians. Medd. Groenland
114, 1–90.
Clack JA. 2012 Gaining ground: the origin and
evolution of tetrapods, 2nd edn. Bloomington, IN:
Indiana University Press.
Coates MI, Clack JA. 1990 Polydactyly in the earliest
known tetrapod limbs. Nature 347, 66 –69. (doi:10.
1038/347066a0)
Coates MI. 1996 The Devonian tetrapod
Acanthostega gunnari Jarvik, postcranial anatomy,
basal tetrapod relationships and patterns of skeletal
evolution. Trans. R. Soc. Edin. Earth Sci. 87,
363–421. (doi:10.1017/S0263593300006787)
Lauder GV, Gillis GB. 1997 Origin of the amniote
feeding mechanism: experimental analysis of
outgroup clades. In Amniote origins: completing the
transition to land (eds SS Sumida, KLM Martin),
pp. 169 –206. San Diego, CA: Academic Press.
Kardong KV. 2002 Vertebrates: comparative
anatomy, function, evolution, 3rd edn. Columbus,
OH: WCB McGraw-Hill Co.
Lauder GV, Shaffer HB. 1986 Functional design of
the feeding mechanism in lower vertebrates:
unidirectional and bidirectional flow systems in the
tiger salamander. Zool. J. Linn. Soc. 88, 277–290.
(doi:10.1111/j.1096-3642.1986.tb01191.x)
Reilly SM, Lauder GV. 1988 Ontogeny of aquatic
feeding performance in the eastern newt,
Notophthalmus viridescens (Salamandridae). Copeia
1, 87 –91. (doi:10.2307/1445926)
Bendix-Almgreen SE, Clack JA, Olsen H. 1990 Upper
Devonian tetrapod palaeoecology in the light of
new discoveries in East Greenland. Terra Nova 2,
131–137. (doi:10.1111/j.1365-3121.1990.
tb00053.x)
Clack JA, Neininger SL. 2000 Fossils from the Celsius
Bjerg Group, Upper Devonian sequence, East
Greenland: significance and sedimentological
distribution. Geol. Soc. Lond. Spec. Publ. 180,
557–566. (doi:10.1144/GSL.SP.2000.180.01.29)
Blom H, Clack JA, Ahlberg PE. 2005 Localities,
distribution and stratigraphical context of the Late
Devonian tetrapods of East Greenland. Medd. Grønl.
Geo. 43, 1–50.
Blom H, Clack JA, Ahlberg PE, Friedman M. 2007
Devonian vertebrates from East Greenland: a review
7
rspb.royalsocietypublishing.org
the anatomical evidence supporting a predominantly (if
not exclusively) aquatic mode of life in Acanthostega and
other Devonian tetrapods, we conclude that these tetrapods
fed primarily in an aquatic rather than terrestrial environment.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 17, 2017
48. Panchen AL. 1985 On the amphibian Crassigyrinus
scoticus Watson from the Carboniferous of Scotland.
Phil. Trans. R. Soc. Lond. B 309, 505–568. (doi:10.
1098/rstb.1985.0095)
49. Clack JA. 1998 The Scottish Carboniferous
tetrapod Crassigyrinus scoticus (Lydekker): cranial
anatomy and relationships. Trans. R. Soc. Edin.
Earth Sci. 88, 127 –142. (doi:10.1017/S026359
3300006908)
50. Jarvik E. 1980 Basic structure and evolution
of vertebrates, vol. 1. London, UK: Academic Press.
51. Jarvik E. 1996 The Devonian tetrapod Ichthyostega.
Fossils Strata 40, 1–206.
8
Proc. R. Soc. B 281: 20132689
44. Hammer Ø, Harper D. 2006 Paleontological data
analysis. Oxford, UK: Blackwell Publishing.
45. Harmon LJ, Glor RE. 2010 Poor statistical
performance of the Mantel test in phylogenetic
comparative analyses. Evolution 64, 2173–2178.
46. Beaumont EH. 1977 Cranial morphology of the
Loxommatidae (Amphibia: Labyrinthodontia). Phil.
Trans. R. Soc. Lond. B 280, 29–101. (doi:10.1098/rstb.
1977.0099)
47. Ahlberg PE, Friedman F, Blom H. 2005 New light on
the earliest known tetrapod jaw. J. Vertebr.
Paleontol. 25, 720–724. (doi:10.1671/02724634(2005)025[0720:NLOTEK]2.0.CO;2)
rspb.royalsocietypublishing.org
in the facial skeletons of bats. Anat. Rec. 283A,
319–330. (doi:10.1002/ar.a.20165)
41. Dumont ER, Davis JL, Grosse IR, Burrows AM.
2010 Finite element analysis of performance
in the skulls of marmosets and tamarins. J. Anat.
218, 151 – 162. (doi:10.1111/j.1469-7580.2010.
01247.x)
42. Abramoff MD, Magalhaes PJ, Ram SJ. 2004
Image processing with ImageJ. Biophotonics Int. 11,
36–42.
43. Bookstein FL. 1991 Morphometric tools for landmark
data: geometry and biology. Cambridge, UK:
Cambridge University Press.