Biological Journal of the Linnean Socieg (1993), 50: 339-360. With 5 figures
A functional-morphometric analysis of
forelimbs in bipgdal and quadripedal
heteromyid rodents
MARY V. PRICE
Department of Biology, University of Calzfrnia, Riverside, California 92521, U.S.A.
Received 17 August 1992, accepted for publication 5 January 1993
The rodent family Heteromyidae contains bipedal hoppers and quadrupedal runners. The
possibility that bipedalism is associated with forelimb specialization for nonlocomotory functions,
such as burrowing and seed-gathering, motivated a static functional-morphometric and interspecific
allometric analysis of 18 metric characters of the forelimb skeleton. A principal-components analysis,
across 28 species in six genera, showed that lengths of proximal (scapula, humerus) and distal (ulna,
radius, metacarpal) elements were negatively allometric, and widths were positively allometric.
Quadrupedal and bipedal species groups showed qualitatively similar allometric patterns, except
that scapula width anterior to the spine was positively allometric in quadrupeds and negatively
allometric in bipeds; scapula width posterior to the spine was positively allometric in bipeds and
isometric in quadrupeds; and olecranon length was isometric in bipeds and positively allometric in
quadrupeds. Most morphometric characters varied significantly among species within genera, even
when effects of size variation were reduced by reconstructing all species to a common general size (as
indicated by their score on the first principal component). These shape differences caused species to
vary in the mechanical advantage of the forelimb, of possible importance for digging and seedharvesting performance. Relative to quadrupeds, bipedal species tended to have greater mechanical
advantage for proximal forelimb elements and smaller mechanical advantage for distal forelimb
elements, but only the distal pattern remained in reconstructed forms, and no functional character
was significantly different when tested over variation among genera nested within locomotion type.
Cluster analysis confirmed that forelimb characters related to digging or seed-harvest are not
coincident with mode of locomotion. Forelimb characters were, however, associated with digging or
seed-harvest performance. Mechanical advantage of the proximal forelimb was positively related to
an index of the compaction of soils with which 26 desert-dwelling species are associated, and also to
relative use of heavy vs. light soils by nine species in the laboratory. Across 10 species, deviations in
seed-harvest rate from expected allometric values were negatively correlated with mechanical
advantage of the distal forelimb.
ADDITIONAL KEY WORDS:-interspecific allometry - body form reconstruction - Chactodipus digging ability - Dipodomys - Hetnomys - Liomys - Microdipodops - Perognathus - seed-harvest rate - soil
associations - performance - morphology.
CONTENTS
Introduction . . . . . . . . . . . . . . . . . .
Methods . . . . . . . . . . . . . . . . . . .
The Heteromyidae . . . . . . . . . . . . . . .
Morphological measurements . . . . . . . . . . . . .
Analytical methods . . . . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . . . .
Allometric patterns . . . . . . . . . . . . . . .
Shape variation . . . . . . . . . . . . . . . .
Functional variation . . . . . . . . . . . . . . .
Relationship of functional variables to distribution, performance, and behaviour
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0 1993 The Linnean Society of London
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Discussion
Acknowledgements
References
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INTRODUCTION
The morphology of the Heteromyidae, a new-world family of rodents, is
interesting for various reasons. All of its members exhibit a number of unusual
features such as external fur-lined cheek pouches (Morton et al., 1980; Nikolai &
Bramble, 1983; Brylski & Hall, 1988; Ryan, 1989a), and some also exhibit
inflated auditory bullae (Webster & Webster, 1975, 1980) and skeletal
modifications for bipedal locomotion (Hatt, 1932; Howell, 1932; Pinkham, 1971;
Biewener et al., 1981, 1988; Berman, 1985; Biewener & Blickhan, 1988).
Furthermore, because species that represent extremes of size and shape within
the family occur sympatrically in North American deserts, and hence experience
similar environments, the Heteromyidae provides an unusual opportunity to
investigate the ecological consequences of an evolutionary radiation (e.g. Nikolai
& Bramble, 1983). Finally, the fact that heteromyid species of similar size and
shape rarely coexist (Bowers & Brown, 1982) suggests that morphological
similarity affects the probability of competitive displacement (e.g. Brown, 1973;
Price & Brown, 1983; Kotler & Brown, 1988). Much now is known about both
the form and the ecology of desert-dwelling heteromyids. Nevertheless, how
form, performance, and ecology are linked is still poorly understood, and the
ecological forces that may have moulded morphological patterns within this
family remain the subject of active debate (see Reichman & Brown, 1983;
Genoways & Brown, 1993).
Because bipedal locomotion is so rare in mammals, studies of heteromyid
morphology have concentrated on features that are directly involved in hopping,
such as the vertebral column, pelvic girdle, hindlimb, and tail. In contrast, the
forelimbs and pectoral girdle have received little attention, despite their role in
the ecologically significant activities of burrow construction and seed harvest,
and despite the possibility that bipedalism may be associated with forelimb
specialization for nonlocomotory functions (Bartholomew & Cary, 1954; Nikolai
& Bramble, 1983) because it removes constraints related to support and
propulsion.
In general, the potential for conflicting demands on forelimb design can be
seen by contrasts in the structure of extreme forms, such as cursorial vs.
burrowing mammals. Cursorial forms such as horses (Equus) have forelimbs that
generate rapid and energetically inexpensive movement of the foot relative to the
body, in addition to absorbing shock (Maynard Smith & Savage, 1956;
Hildebrand, 1985a). They achieve this with long, narrow scapulae that are held
at a steep angle to the horizontal, and proximal attachment of the teres major
muscle on the humerus, which has the effect of increasing the angle through
which the humerus rotates when the teres major contracts. Areas on either side
of the scapular spine are approximately equal in size, to accommodate muscles
that support the trunk and contribute to stride length by rotating the scapula.
The ulna and radius are relatively long and olecranon process short, increasing
the arc through which the foot swings as the limb is rotated. The foot is much
reduced in mass, which minimizes energetic costs of accelerating the limb
HETEROMYID RODENT FORELIMBS
34 1
forward and backward with each stride. Dislocation of the elbow and wrist
under forelimb loading is prevented by joint structures that limit rotation
around the long axis of the limb (Hildebrand, 1985a). While quadrupedal
heteromyids are hardly cursorial, their forelimbs do play a role during rapid
locomotion, which is not the case with bipeds (Bartholomew & Caswell, 1951;
Bartholomew & Cary, 1954; Nikolai & Bramble, 1983).
Scratch-diggers like armadillos (Dugpus), on the other hand, have forelimbs
that generate large forces at the expense of stride length and speed of limb
movement (Maynard Smith & Savage, 1956; Hildebrand, 1985b). Their short
scapulae, held at a shallow angle, have a long process on the ventral-posterior
border where the teres major muscle originates. This, along with a distal teres
major attachment on a short humerus, increases the mechanical advantage of
proximal forelimb elements, but restricts the angle through which the humerus
rotates. Distal forelimb elements tend to be relatively short and massive, with
long olecranon process to increase the mechanical advantage of the triceps
muscle that extends the ulna. The manus, or forefoot, often has strong curved
claws and mechanisms for keeping the digits flexed (Hildebrand, 1985b).
A forelimb designed primarily for support and propulsion hence seems
unlikely to be effective for digging, and an additional tradeoff should exist
between design for rapid seed harvest and design for running or for digging. Seed
harvest requires pronation and supination of the distal forelimb (Nikolai &
Bramble, 1983), which reduces the stability of the elbow and wrist joints under
loading. Efficient seed harvest also requires rapid oscillation of the distal
forelimb, which should be incompatible with a large triceps outforce.
It is of interest, therefore, to investigate forelimb structure within the
Heteromyidae to see whether quadrupeds differ from bipeds in ways that, from a
static mechanical analysis, can be expected to affect digging and seed harvesting
performance. I n this paper I describe morphometric variation in skeletal
elements of the heteromyid forelimb and its mechanical consequences. I also
provide evidence that variation in the mechanical advantage of proximal and
distal elements in desert-dwelling species are correlated, respectively, with
digging ability and with seed-harvest rates.
METHODS
The Heterornyidae
The Heteromyidae contains six modern genera (Hafner & Hafner, 1983); two
that inhabit tropical or subtropical forests from Mexico to northern South
America (spiny pocket mice, Heteromys, Liomys, both in the subfamily
Heteromyinae), and four that inhabit the deserts and arid grasslands or
shrublands of the western United States and Mexico (kangaroo rats, Dipodomys,
and kangaroo mice, Microdipodops, in the subfamily Dipodomyinae; pocket mice,
Chaetod$us and Perognathus, in the subfamily Perognathinae) . Discussions of
phylogenetic relationships within the family can be found in Hafner & Hafner
( 1983), Ryan ( 1989b), and Brylski ( 1993).
Two genera-Dipodornys
and Microdipodops-hop
on the hindlimbs when
travelling rapidly, whereas the other four genera use an asymmetrical
quadrupedal bound. Although all heteromyids can climb, the desert forms
342
M.
V. PRICE
appear to do so only occasionally in nature (Lemen & Freeman, 1986;
Reichman & Price, 1993) and are relatively clumsy when they do climb.
Heteromys and Liomys appear to be somewhat more arboreal (Eisenberg, 1963;
Fleming & Brown, 1975). With the possible exception of Heteromys (Fleming &
Brown, 1975)) all heteromyids construct burrows. Descriptions of gaits used by
heteromyids can be found in Bartholomew & Cary (1954), Bartholomew &
Caswell (1951))Eisenberg (1963), Howell (1932), Pinkham (1971), and Nikolai
& Bramble (1983); the biology of this ecologically uniform group of nocturnal,
burrowing granivores is reviewed in several edited volumes (Prakash & Ghosh,
1975; Reichman & Brown, 1983; Genoways & Brown, 1993).
When digging, all heteromyids balance on the hindfeet. They extend both
forelimbs forward, with palms of the manus facing down, and then bring the
forefeet down and back, shearing and moving soil in the process. Animals
periodically either kick accumulated soil backward from under the body with
the hindfeet or turn around and push it with extended forefeet. Similar motions
of the forelimb are used during extraction of seeds from the soil, except that once
a seed has been grasped (usually with one manus), the ulna, radius and manus
TABLE
1. Definition of morphological characters. N u m b e r s correspond to characters illustrated in
Figure 1.
Scapula
I.
2.
3.
4.
5.
6.
7.
8.
Length. Distance from glenoid fossa to dorsal border, along axis of the scapular spine (‘Scaplen’)
Widfh. Distance from the posterior to anterior border along dorsal border, taken perpendicular to the
long axis of scapular spine (‘Scapwid’)
Spine height. Maximum height of the scapular spine (‘Spinht’)
Acromion fength. Distance. parallel to the long axis of the acromion, from position of the glenoid fossa to
the distal end of acromion (‘Acrlen’)
Anterior b07de7 to spzne. Maximum distance, perpendicular to the long axis of the scapular spine, from
anterior border of scapula to spine (‘Antspin’)
fosferior border fo spine. Distance, perpendicular to the long axis of the scapular spine, from posterior
border of the scapula just ventral to teres major process, to scapular spine (‘Postspin’)
Spine-teres major. Distance, perpendicular to the long axis of the scapular spine, from scapular spine to
the anterior edge of the teres major process (‘Spinter’)
Length of feres major process: # 7-#6 (‘Terlen’)
Humerus
9. Lengfh. Distance from head to capitulum (‘Humlen’)
10. Widfh. Width, perpendicular to the long axis of the humerus, at the epicondyles (‘Humwid’)
11. Delfoidprocess height. Maximum width, perpendicular to the long axis of the humerus, at the deltoid
process (‘Deltht’i
12. Deltoid process length. Basal length of the deltoid process, parallel to the long axis of the humerus
(‘Deltlen’)
13. Deltoid process position. Distance, parallel to the long axis of the humerus, from the head of the humrrus
to the position of the midpoint of the deltoid process (‘Deltpos’)
14.
15.
Ulna
Length. Distance from head of the olerranon to the styloid process (‘Wen’)
Olecranon length. Distance from the head of the olecranon to the midpoint of the semilunar notch
( ‘Oleclen’)
Radius
16. Length. Distance from head to styloid process (‘Radlen’)
17. Curuature. Distance from outer edge of radius to inner surface of ulna at the midpoint in curve w3herr
radius separates from ulna at proximal end (‘Radcurv’)
Third metacarpal
18. Length. Distance from the proximal to the distal end (‘Metalen’)
HETEROMYID RODENT FORELIMBS
343
are rotated so that the palm faces up and back, and the seed is then placed into a
cheek pouch whose opening is lateral to the jaw. Nikolai & Bramble (1983)
provide a qualitative description of forelimb movements during digging and seed
gathering; quantitative information about limb positions during these
movements is lacking.
Morphological Measurements
Eighteen metric characters of the forelimb were measured (Table 1, Fig. 1)
from disarticulated skeletal material of 633 adult specimens of 28 heteromyid
species representing all six genera (Table 2). Measurements were taken with
Helios needle dial calipers to the nearest 0.001 cm by a single observer to reduce
.. ..
1
4
.....
G
... ...
.......
3’
...
2
i: l
7
...........
........
......
!
...
13
I
.....P .
10
16
18
14
15
L
Figure 1. Morphological measurements included in analyses. Definitions and labels are given in
Table 1.
344
M. V. PRICE
variance due to measurement technique. When possible, the left forelimb was
measured. Specimens were housed at the Museum of Vertebrate Zoology,
University of California at Berkeley, or at the Los Angeles County Museum,
California, U.S.A.
TABLE
2. Heteromyid species included in morphometric analyses, their gaits, systematic and
environmental relationships, and the compaction and texture of soils with which they are
associated, as determined by a review of the indicated sources. Soil Texture Rank: 1 = fine,
2 = sand, 3 = gravel, 4 = rocky. Soil Compaction Rank: 1 = loose, 2 = various or firm, 3 = hard
Speries
Soil
texture
rank
Soil
compaction
rank
Sources
Genus Dipodumys (subfamily Dipodomyinae; Bipedal; desert-dwelling):
D . agilis Gambel
2.5
2.0
36
D. californicus Merriam
2.0
2.0
3, 29
I .5
I .o
18, 28, 19, 5, 8, 27, 17, 30, 9, 26
D . deserti Stephens
D . hecrmanni Le Conte
3.0
2.5
13, 39, 11
D . ingem (Merriamj
1.5
2.5
39; Fine alluvial valley bottom,
presumably compacted
2.0
2.0
2, 18, 5, 8, 27, 17, 30, 9, 25, 37, 38
D . merriami Mearns
D . microps (Merriamj
1.5
2.0
5, 8, 30, 9
D.nitratoides Merriam
1.o
2.0
26, 10
D . ordii Woodhouse
2.0
1.5
2, 1, 6, 8
D.panamintinus (Merriam)
2.5
2.0
26, 27, 8, 30
D . peninsularis (Merriamj
1.5
2.0
Alluvial valley bottom; like
D . stephensi
D. spectabilis Merriam
1.5
2.5
2, 38, 41
1.5
2.0
35, 7
D . stephemi (Memamj
D . vmwtw (Merriamj
2.0
1.5
22
Genus Microdipodops (subfamily Dipodomyinae; bipedal; desert-dwelling):
M. nugacephalus Merriam
2.0
1.5
32, 16, 26
M . pallidus Merriam
1.5
1.o
33, 16, 26
Genus Heteromys (subfamily Heteromyinae; quadrupedal; forest-dwelling):
H. desmarestianus Gray
3.5
?
21, 14, 15
L . rrroratus (Gray)
Genus Liomys (subfamily Heteromyinae; quadrupedal; forest-dwelling):
3.5
?
12, 4, 14, 15
Genus Chaefodipus (subfamily Perognathinae; quadrupedal; desert-dwelling):
3.5
2.0
26, 38, 34
C. baileyi (iMerriam)
C. califurnicus (Merriam)
2.5
2.0
26
C. failax (Merriam)
2.5
2.0
26, 31
C. formosus Merriam
3.5
2.0
31
C. infermedim (Merriam)
3.5
I .5
42, 24
23, 26, 20, 42, 24
C. penicdlatus (Woodhouse)
I .5
I .5
Genus Perognathus (subfamily Perognathinae; quadrupedal; desert-dwelling:
1.5
2.0
38, 34
I .5
2.0
2, 38
P . longimmbris M e m a m
1.5
2.0
26, 20, 31
2.0
1.5
20, 40
P. parnus (Peak)
P . amplw Osgood
P. javus Baird
'Armstrong, 1979; 'Bailey, 1931; 3Bailey, 1936; 'Baker el al., 1967; 5Beatley, 1976; 6Best & Hoditschek, 1982;
7Bleich, 1977; 'Brown, 1973; 'Burt, 1934; "Culbertson, 1945; "Dale, 1939; "Dowler & Genoways, 1978;
I3Fitch, 1948; "Fleming, 1974; "Fleming & Brown, 1975; I6Ghiselin, 1970; "Grinnell, 1914; "Grinnell, 1937;
"GrinneU & Swarth, 1913; "Hall, 1946; ''Hall, 1954; "Hawbecker, 1940; 23Hoffmeister,1986; "Hoover et al.,
1977; 25Huey, 1942; "Ingles, 1965; 'Qohnson et al., 1948; '8Jorgenson & Hayward, 1965; "Kelt, 1988;
"Matson, 1976; 3'Miller & Stebbins, 1964; 320'Farrell & Blaustein 1974a; 330Farrell & Blaustein 1974b;
3'Price, 1978; 35Pricect al., 1991; 36Price & Longland, 1989; 37Reynolds,1958; 38Rosenzweig & Winakur, 1969;
"Tappe, 1941; W e r t s & Kirkland, 1988; "Vorhies & Taylor, 1922; ''Wallwork, 1982.
HETEROMYID RODENT FORELIMBS
345
.
..
’....... .
i:
!
.
9-13 \
‘::
L
i
t.
.........
‘...
.
!
!
I
....... ........... ....
.-...-......,,........“”’ .“._..._..
_(.. ..............
.....
..... . .....
........
..........
A..
......
14-15
D
C
Figure 2. Geometric assumptions used to calculate mechanical advantage of forelimb elements,
Details of calculations and definitions of symbols are given in the text and in Appendix 1.
Mechanical properties of the forelimb lever system were calculated from
morphometric measurements as indicated in Fig. 2 and Appendix 1. This static
mechanical analysis focused on four force components: (1) the effective inforce
per unit of actual force generated by the teres major muscle (the vector ‘A’ in
Fig. 2, termed ‘effective teres inforce’); (2) the backward force generated a t the
distal end of the humerus per unit of actual teres major inforce (the vector ‘B’ in
Fig. 2, termed ‘teres outforce’); (3) the downward force generated at the distal
end of the ulna per unit of force exerted at the olecranon process by contraction
of the triceps muscle (the vector ‘C’ in Fig. 2, termed ‘triceps ulna outforce’);
and (4)the downward force generated at the distal end of the metacarpal per
unit of triceps inforce, assuming negligible length of wrist elements (the vector
‘D’ in Fig. 2, termed ‘triceps metacarpal outforce’).
To calculate these force components (termed ‘functional variables’), I made
several simplifying assumptions. First, I focused on the teres major and triceps
muscles. These muscles are assisted by others, such as the latissimus dorsi (the
teres major tendon of insertion is joined by that of the latissimus dorsi; Ryan,
1989b) and dorsoepitrochliaris (Lehmann, 1963; Ryan, 1989b)’ respectively.
Unless the additional muscles substantially alter the net direction of force
vectors, however, they are unimportant for calculations of mechanical
advantage. Second, I assumed that the scapula is held at a 45” angle to
horizontal (i.e. in Fig. 2, 8 = 45”), and that the teres major insertion on the
humerus is medial to the deltoid process (Howell, 1932; Lehmann, 1963; Ryan,
198913). Third, I assumed that the humerus and ulna are oriented vertically and
horizontally, respectively, and that the triceps inforce is directed vertically.
346
M. V. PRICE
Formulae used in calculations are summarized in Appendix 1, with reference to
Fig. 2 and Table 1. Original data are deposited with the Librarian of The
Linnean Society of London, Burlington House, Piccadilly, London W 1V OLQ,
from whom copies may be obtained.
Analytical methods
After 16 outliers (observations that were > 3 standard deviations from species
means) were removed, log,,-transformed morphometric variables were normal
and homoscedastic, as were untransformed functional variables. Statistical
analyses therefore were based on log,,-transformed morphometric data and
untransformed functional data.
To analyse shape differences among heteromyid groups, I followed procedures
of Bookstein et al. (1985) and Strauss & Bookstein (1982). I first performed
principal components analysis on the variance-covariance matrix of species
means of log-transformed morphometric data. The first principal component
(PCl ) describes major patterns of positive covariation of metric characters across
species and can be interpreted as a descriptor of a ‘general size’ latent variable;
each species’ score on this variable indicates its ‘general size’. When PC1
coefficients are scaled to a mean of 1.0, the scaled coefficients represent
allometric coefficients that describe how each metric character increases with
‘general size’; coefficients greater than 1 .O indicate positive allometry, coefficients
of 1.0 indicate isometry, and coefficients less than 1.0 indicate negative
allometry. For derivation and discussion of these methods, see Jolicoeur (1963)
and Bookstein et al. ( 1985).
First principal components were extracted for the entire set of 28 species (‘allheteromyid PCl’), as well as for various subsets of species, to compare
interspecific allometric patterns among subgroups, e.g. quadrupeds vs. bipeds.
Confidence intervals around allometric coefficients were determined by
removing each species sequentially from the analysis and recalculating allometric
coefficients to generate ‘pseudovalues’. T h e variance among pseudovalues
obtained by this jackknifing procedure was then used to calculate 95%
confidence intervals for allometric coefficients (Sokal & Rohlf, 1981 ).
Coefficients whose 95% confidence intervals do not include 1.O are significantly
allometric at the So/; level, and as a general rule, when confidence intervals for
two groups do not overlap the mean for the other group for a particular
character has significantly different allometric coefficients for that character.
The overall similarity between subgroups in allometry was determined by
calculating the cosine of the angle between their first principal components. This
is equal to the expected correlation in PC1 scores that would be obtained using
the first principal components for different subgroups (Cooley & Lohnes, 1971).
Because the allometric patterns of heteromyid subgroups were extremely
similar (see below), I could use the form-reconstruction method of Strauss and
Bookstein (1982; Bookstein el al., 1985) to analyse shape differences among
heteromyid groups with much of the between-group size variation removed. The
method exploits the fact that raw coefficients of the all-heteromyid PC1 reflect
partial regression coefficients of each log-morphological variable on general size,
This means that one can calculate, for each species, what value each character
would take on if the species were a different size (indicated by its score on the allheteromyid P C l ) . By thus ‘reconstructing’ species to a common size, it is possible
HETEROMYID RODENT FORELIMBS
347
to visualize how groups vary in shape, with much of the confounding effect of
between-group size differences removed. Shape variation among reconstructed
forms is produced both by size-independent shape differences between groups, as
well as by allometric differences between groups (which in the heteromyid case
are slight, judging from the high correlations among first principal components).
Variation among groups (species, genera, or locomotory types) in functional
or morphometric variables was assessed before and after reconstruction with
hierarchical univariate or Multivariate Analysis of Variance (ANOVA or
MANOVA), using either species means (for comparisons of genera or
locomotory types) or individuals’ data (for comparisons of species within
genera). Relative similarity of groups was also assessed with centroid-based
cluster analysis. Analyses were conducted using the SAS PRIN (for principal
components analyses), GLM (for ANOVA and MANOVA), and CLUSTER
procedures (SAS Institute, 1985).
Relationships between functional variables and ecology were assessed in
several ways. First, I reviewed the literature on soil distributions of heteromyid
species and derived a score for the coarseness and the compaction of soils with
which each species is associated (Table 2). These soil attributes influence the
energy cost of burrowing (Vleck, 1979). There was necessarily some ambiguity
in assigning these ranks, especially for species with broad edaphic associations or
those associated with rocky soil; I assumed that the latter soils were relatively
loose, since burrows would be constructed in the relatively uncompacted
interstitial soil between rocks. I than reanalysed results of laboratory foraging
experiments run with several of the species included in morphometric analyses.
In one set of experiments (Price & Longland, 1989)’ individuals were given a
choice of harvesting millet seeds from several artificial substrates. I used the
(arcsin-transformed) fraction of all harvested seeds that were taken from coarsevs. fine-soil patches, and from heavy- vs. light-soil patches, as indices of soil
texture and bulk density choice. I n the second set of experiments (Morgan &
Price, 1992), individuals were timed as they harvested millet seeds continuously
from sand in a metabolic chamber. The (log-transformed) number of seeds
harvested per minute was regressed against log of body mass, and each species’
average deviation from the foraging rate expected for a heteromyid of its mass
was calculated.
To determine whether there is a relationship between forelimb structure and
soil association, I used multivariate analysis of variance to assess whether species
associated with soils of different texture or compaction ranks differed in forelimb
functional variables (GLM procedure, SAS Institute, 1985). To assess the
relationship between forelimb structure and substrate choice behaviour or
foraging rate, substrate-choice and foraging-rate estimates were regressed
individually against forelimb functional variables using multiple regression
(REG procedure, SAS Institute, 1985).
RESULTS
Allometric patterns
Not unexpectedly, much of the variation among heteromyid species in
forelimb metric characters is related to variation in size. For all species taken
together, the first principal component accounted for 89% of between-species
M. V. PRICE
348
variation in forelimb characters (Table 3). This percentage varied between 80%
and 9604 for various species subsets; the group with the most residual variation
was the genus Dipodomys. Quadrupeds as a whole were smaller than bipeds,
judging from species' mean scores on the all-species first principal component
(biped mean PCI score = 0.24, quadruped mean PCl score = -0.32), but this
effect was not significant when locomotion types were tested over genus nested
within locomotion type (F[ 1,4] = 2.62, P = 0.18) because bipedal Microdipodops
TABLE
3. Allometric coefficients of log-transformed morphometric variables and percent of
variation explained by the first principal component, for various heteromyid species groups, and
PCI coefficients for principal-components analysis of all species. Values in parentheses are 95%
confidence intervals based on n jackknifed PC runs for various species groups. Asterisks indicate
allometric coefficients different from 1.0 at the 5O4, level. Allometric coefficients greater than 1.0
indicate positive allometry; those less than 1 .O indicate negative allometry; those = 1 .O indicate
negative allometry; those = 1.0 indicate isometry with 'general size'. See text for further details
Allometric coefficients ( +95:/,
confidence interval)C
-
Perognathus
All
Variable
_______
Scaplen
PC 1
coefficient
Heteromyids
n = 28
0.270
Spinht
0.294
Ac rlrn
0.181
Antspin
0.187
Po5tspin
0.302
Spintcr
0.292
rerlen
0.281
Hurnlen
0.196
*O 895
( + O 041)
*1 171
j k 0 077)
* I 274
( + O 118)
*0 784
ik0 182)
0811
i f 0 205)
* I 309
i + O 134)
* 1 264
if0 123)
I216
1 f0 223;
*O 851
I+ O
Hurnwid
0.262
Urltht
0.232
Deltlen
0.267
Del tpos
0.230
Oleclen
O.23 I
061
* I 133
, f O 1071
1 006
k 0 069)
I I57
( f 0 176,
0 995
j f0 1051
1001
I
Kadcur\
0.205
f00461
*O 886
+ o 100
o.ini
0 786
+ 0 2361
L llen
0.209
*O 906
I
Metalrn
'Ijt
Variation
All
Quadrupeds
n = 12
+
Dipodomys
n = 14
Chaetodipus
n = 10
*0.771
*0.873
(k0.122)
1.237
(f0.261)
0.905
f0.201)
1.070
k0.302)
*1.787
f0.479)
0.924
+0.302)
0.897
(f0.135)
0.861
(10.549)
0.969
( f 0.096)
1.046
( 10.272)
*0.832
(f0.050)
* 1.557
[ f0.404)
0.982
(k0.197)
~
0.207
Srapwd
Kadlen
All
Bipeds
n = 16
0.128
89
k0092
$0 554
i f 0 074)
89
*0.820
! k0.054)
*1.301
(fO.ll8)
1.206
if 0.259)
1.087
(k0.402)
*0.789
(f(O.192)
* 1.472
(k0.313)
* 1.406
(f0.245)
1.334
! k0.345;
*0.948
! f0.048)
0.930
i f0.087)
0.932
i+0.125)
1.209
if0.237)
*1.144
( k0. 134)
0.992
i +0.120!
*0.692
:f0.063j
*0.505
i k0.305)
*0.729
! k0.064)
*0.504
ifO.224j
91
0.975
( k0.0891
( f 0.107)
1.044
( + O 115)
1.02I
( f 0.089)
0.951
(f0.132)
* 1.706
I k 0.157)
0.976
, f0.115)
*0.764
i f0.058)
*0.505
j f0.223)
1.038
f 0.047)
1.030
(f0096)
*0.796
kO.027)
* 1.594
1.187
(f0.216)
1.072
(f0.427)
1.375
(k0.677)
1.000
I f0.167)
1.135
( + O . 195)
1.146
(k0.346)
1.141
f0.1451
"1.112
kO.070)
*1.147
k0.092)
*0.814
+0.077;
0.792
(k0.241)
'0.850
( f0.068)
0.885
(+0. 160)
96
+0.810)
0.941
kO.174)
1.012
+0.138)
0.857
f0.297)
1.095
& 0.728)
1.000
f0.245)
1.147
f0.144)
*0.734
+O. 137)
0.789
(f0.554)
*0.778
( f0.128)
*0.820
(k0.163)
80
1.028
( 1 0 . 121)
*0.7 1 7
(+0.101)
0.830
(kO.712)
*0.719
( f0.084)
0.768
(k0.274)
91
349
HETEROMYID RODENT FORELIMBS
are small (PC1 score = -0.63) and quadrupedal Heteromys and Liomys are
relatively large (PC1 score = 0.49, 0.17, respectively).
When PCl coefficients are scaled to a mean value of 1.0, they represent
allometric coefficients that describe the scaling of each character with respect to
‘general size’ (Bookstein et al., 1985). Scaled PC1 coefficients and their 95%
confidence intervals are indicated in Table 3. For all species taken together (‘All
heteromyids’), scapula length (scaplen), anterior scapula width (antspin), and
acromion length (acrlen) were the only negatively allometric scapula variables.
Humerus length (humlen) was negatively allometric, whereas humerus width at
the epicondyles (humwid) was positively allometric and other humerus variables
were isometric. Of the distal limb elements, all characters were negatively
allometric except olecranon length (oleclen) and radius length (radlen), which
were isometric.
Species subgroups had forelimb allometries that deviated somewhat from this
basic pattern (Fig. 3; Table 3). It should be emphasized, however, that there
was a very high correlation between subgroup PC1 scores (the cosine of the angle
between principal components was > 0.93 for all pairwise group comparisons,
and actual score correlations exceeded 0.98). For instance, anterior scapula
width (antspin) was negatively allometric in bipeds but positively allometric in
quadrupeds; and posterior scapula elements (postspin, spinter, terlen) were
QUADRUPEDS
Chetodipus baileyi
VENTRAL
VENTRAL
ANTERIOR
BIPEDS
Dipodomys panamintinus
///
/OF
LATERAL
ANTERIOR
//
LATERAL
Figure 3. Allornetry of forelimb characters in quadrupedal and bipedal heteromyids. Diagrams are
camera lucida drawings of a representative quadrupedal species on the left (Chactodipus baileyi) and
bipedal species on the right (D$odomys panamintinu). Numerical values indicate allornetric
coefficients (first principal component coefficients scaled to a mean value of 1) for the indicated
metric character.
350
M. V. PRICE
positively allometric in bipeds but negatively allometric or isometric in
quadrupeds. I n most other respects, the qualitative allometric patterns were
similar, even though quadrupeds and bipeds differed significantly in all forelimb
allometric coefficients except for deltoid position, based on two-sample t-tests
(Table 3 ) .
Differences between quadrupeds and bipeds in allometric patterns were
strongly influenced by Liomys and Heteromys, members of the Heteromyinae and
the largest quadrupeds. Allometric coefficients for quadrupeds changed when
these two genera were excluded, leaving only the desert quadrupeds
(Perognathinae; Table 3 ) . For some characters the desert quadruped allometry
converged on that for the bipeds [e.g. lengths of distal forelimb elements became
more negatively allometric, scapula length (scaplen) became more negatively
allometric, and scapula width (scapwid) more positively allometric], but for
others [e.g. scapula spine height (spinht), scapula width anterior or posterior to
the spine (antspin and postspin, respectively)] the desert quadruped allometry
was more different from that of bipeds than was the all-quadruped allometry.
Shape uariation
Even though general size accounted for most of the among-species
morphometric variation, additional shape variation was apparent when species
were ‘reconstructed’ to conform to a common ‘general size’ (Strauss &
Bookstein, 1982; Bookstein et al., 1985). Figure 4 shows mean forelimb
dimensions of the six genera, calculated from species means that had been scaled
to an all-heteromyid PC1 score of 0.0, approximately the midpoint of the size
range and corresponding to a heteromyid of approximately 35 g mass.
Reconstructed genera differed significantly in all morphometric variables except
for height of scapular spine and acromion length.
The heteromyines Heteromys and Liomys were distinct in having long scapula,
relatively large scapula area anterior to the spine, and long humerus and deltoid
process (Fig. 4). Microdipodops had the shortest humerus and longest ulna and
radius. The desert-dwelling genera (Chaetodipus, Perognathus, Microdipodops, and
Dipodomys) all had wide scapula posterior to the spine, and long teres major
process. Chaetodipus tended to be intermediate between the heteromyines and the
other genera.
There was little suggestion that bipeds as a group differ from quadrupeds, and
indeed locomotion types differed significantly (F,.4> 8.00, P < 0.05) only in
acromion length (acrlen), humerus length (humlen), and deltoid process position
(deltpos; Fig. 4). A cluster analysis performed based on 18 metric characters of
reconstructed genera (SAS proc CLUSTER, centroid method; Figure 5C)
confirmed the lack of segregation of bipeds and quadrupeds; Dipodomys clustered
with Perognathines, and Microdipodops was distinct from all other genera.
Alternative clustering algorithms (SAS proc CLUSTER, average and Ward
methods) gave this same qualitative result.
Functional variation
Both allometric and size-independent shape variation contributed to
significant variation among species in mechanical advantage of forelimb
HETEROMYID RODENT FORELIMBS
r
35 1
1
Figure 4. Diagrammatic illustration of forelimb dimensions of six heteromyid genera. Generic values
are averaged over species reconstructed to a common general size (PC1 score = 0). From left to
right, forelimb elements are scapula, humerus, ulna, and metacarpal. Height of scapular spine and
acromion process length are indicated by vertical and horizontal bars, respectively, at extreme left of
the scapula. D = Dipodomys, M = Microdipodops, P = Peropathus, C = Chaetodipus, L = Liomys, H =
Heteromys.
elements (Table 4). The tendency for out-levers to show more negative
allometry than in-levers contributed to positive correlations over all 28 species
between functional variables and all-heteromyid PCl score (r = 0.58, 0.68, 0.76,
0.28, and 0.48 for effective teres inforce, humerus outforce, teres outforce, triceps
ulna outforce, and triceps metacarpal outforce, respectively). MANOVA
indicated highly significant differences among species within locomotion types.
Within bipeds, there was significant variation among species in all forelimb
functional variables (Wilks’ lambda = 0.048, F[90,1311.29] = 10.47, P <
0.0001; for each variable, F[15,237] > 15.28, P < 0.001). Within quadrupeds
there also was significant overall among-species variation (Wilks’ lambda =
0.103, F[66,743.87] = 5.97, P = O.OOOl), and species differed in all functional
variables (F[11,143] > 2.90, P < 0.01)) except teres outforce (F = 1.61, P =
0.10).
Although there was a tendency for bipeds to have greater mechanical
advantage for all proximal elements (effective teres inforce, humerus outforce,
and teres outforce), and for quadrupeds to have greater mechanical advantage
in distal elements (triceps ulna and metacarpal outforces), these differences were
M. V. PRICE
352
0
0.2
I
I
0.4
I
0.6
0.8
1.0
1.2
1.4
I
1
I
I
1
Heteromys
-
A
Liomys
Dipodomys
Perognat hus
B
Liomys
Chaetodipus
Dipodomys
Perognathus
Heteromys
Microdipodops
C
1
Figure 5 . Results of cluster analyses (centroid method) performed on genus means. A, Clusters based
on five functional variables. B, Clusters based on five functional variables calculated from forms
reconstructed to a common general size. C, Clusters based on 18 metric variables of forms
reconstructed to a common general size.
not statistically significant when tested over genera nested within locomotion
types (Table 4), and cluster analyses (using centroid, average, and Ward
methods) based on genus means of all five functional variables grouped
Microdipodops with Perognathines, while Dipodomys was most distinct (Fig. 5A).
The picture did not change when functional variables were calculated from
forms reconstructed to the same general size. Reconstructed genera differed
significantly overall in functional variables (Wilks’ lambda = 0.022,
F[ 15,36291 = 7.28, P = 0.0001); univariate ANOVAs indicated significant
differences among genera for all functional variables except humerus outforce.
Reconstructed bipeds, however, did not differ as a group from reconstructed
quadrupeds for any functional variable, although triceps outforces approached
significance ( P = 0.10). Cluster analyses (using centroid, average, and Ward
353
HETEROMYID RODENT FORELIMBS
TABLE
4. Species means for functional variables, based on all specimens with complete data, and
means of species means for bipedal and quadrupedal species. For definitions of functional
variables, refer to text, Appendix 1 and Fig. 2. Species within a locomotion category that have the
same superscripted letter were not significantly different at the 5% levels by Duncan's multiple
range test performed separately for bipeds and quadrupeds; = number of individuals;
s = standard deviation; nd = no data
n
Body
mass
D . agilis
D . califomicus
D . deserti
D. heermanni
D . ingens
D. merriami
D. microps
D . nitratoides
D . ordii
D. panamintinus
D . peninsularis
D. spectabilis
D . stephensi
D. uenustus
M . megacephalus
M . pallidus
14
33
18
23
2
30
13
I1
37
19
3
5
9
3
17
16
58
nd
98
62
128
40
58
35
48
61
nd
131
nd
43
14
14
C. baileyi
C. califonticus
C. fallax
C. fairnosus
C intermedius
C penicillatus
H. desmarestianus
L. irroratus
P. amplus
P. flauus
P . longimembris
P. pawus
19
12
7
18
21
18
7
18
5
20
21
19
18
14
14
72
38
12
7
8
Species
Bipedal species
2
17
11
20
X
S
Quadrupedal
species
X
S
Effective
teres
inforce
Triceps
outforce
at
metacarpal
Teres
outforce
Triceps
outforce
at ulna
0.31Vb
0.314""
0.2788
0.306hd
0.326"
0.295'de'8
0.285'K
0.300*"
0.28gde&
0.308"d
0.284'R
0.306*
0.305"dc
0.286'"
0.254h
0.237h
0. 15Zd'
0.16gab
0.153dc
0.155*'
0.180"
0.134'
0.148d"
0.147"
0.15 Id'
0.153d'
0.1620.167a"
0.174"b
0.174ab
0.137'
0. 142d
0.127'
0. 1Wb
0.128'
0.129'
0.150"
0.113'
0. 125'd
0.1 24'd
0.126&
0.128'
0.136&
0.1 3Yb
(B) Quadrupedal spec:ies
0.790ab
0.335ab'
0.264ab
0.25gab
0.804"b
0.322"
0.803"b
0.331bC
0.265ab
0.261ab
0.809ab
0.323&
0.80Yb
0.340ab
0.272"
0.815"
0.332"b'
0.271ab
0.753'
0.355"
0.267"b
0.785b
0.341ab
0.26Pb
0.274"
0.79Vb
0.34Pb
0.805"b
0.315'
0.253b
0.260ab
0.816"
0.319"
0.805"b
0.34Iab
0.275"
0.175"d
0.179"
0.16Pd'
0.1 62dcr
0.169"''
0.174w
0.186b
0.207"
0. 16ZdC'
0.1468
0.150'8
0.158&8
0. 139"
O.14lk
0.133Cd'
0.128"
0.133'd'
0. 138kd
0.146b
0.165"
0.12gd"
0.1188
0.120'8
0.127"
0.839
0.023
0.348
0.023
0.292
0.023
0.152
0.014
0.127
0.01 1
0.801
0.017
0.333
0.012
0.266
0.007
0.172
0.016
0.137
0.013
Humerus
outforce
(A) Bipedal species
0.830d
0.380ab
0.85Ikd
0.36gab'
0.870ab
0.320"
0.838cd
0.365"
0.837d
0.390"
0.841"'
0.35lcd
O.84Td
0.338d'
0.842&
0.357M
O.83Od
0.34gCd
0.861""
0.358M
O.84lcd
0.338dc
0.878"
0.34gCd
0.867"b
0.351"'
0.83Id
0.345*
0.799'
0.318"
0.794'
0.299'
0.144"b
0.143"b
0.1 11'
0.115d'
methods) confirmed once again the mixing of bipedal and quadrupedal genera
(Fig. 5B).
Among-group differences in allometric coefficients (Table 3) suggested that
functional variables show different size-dependence in bipeds and quadrupeds.
In bipeds scapula length (scaplen) varied as general size raised to the 0.82
power, whereas distance from spine to origin of the teres major (spinter) varied
as size to the 1.47 power. The differences in allometry of these characters caused
effective teres inforce to increase with body size. In quadrupeds effective teres
M. V. PRICE
354
inforce actually decreased with body size, because scapula length was isometric
with general size (coefficient = 0.98), whereas distance from the spine to the
teres major origin (spinter) was negatively allometric (coefficient = 0.76).
Because humerus length (humlen) and deltoid process position (deltpos) scaled
similarly in bipeds and quadrupeds, the difference between these two groups in
teres inforce scaling caused teres outforce to increase with size in bipeds more
quickly than in quadrupeds. I n quadrupeds mechanical advantage of distal
forelimb elements increased more quickly with size than for bipeds, because
there was a larger difference in allometric coefficients of olecranon process length
joleclen) relative to ulna or metacarpal length (ullen, metalen).
Relationship of functional variables to distribution, performance, and behaviour
Heteromyid species exhibit a wide range of soil associations (Table 2), from
loose wind-blown sand (e.g. Dipodomys deserti) to rocky slopes (e.g. Chaetodipus
intermedius). I used MANOVA to determine whether species that were grouped
according to their soil texture or soil compaction ranks differed in two functional
variables, teres outforce and triceps metacarpal outforce. Species with different
soil texture associations did not differ in functional variables (Wilks’ lambda =
0.695, F,,,, = 1.395, P = 0.24). However, species grouped according to soil
compaction did differ marginally (Wilks’ lambda = 0.665, F,,,, = 2.485, P =
0.06). This overall difference was due to a significantly greater teres outforce
= 6.96, P = 0.01);
among bipedal species associated with compacted soils (F2,13
although compacted soil was also associated with greater triceps metacarpal
outforce in bipeds, this effect was not statistically significant by univariate
ANOVA (F2,13= 1.49, P = 0.26). There were no patterns for quadrupeds
analysed separately.
I n the laboratory, nine desert heteromyid species (five bipedal, four
quadrupedal) varied in the fraction of harvested seeds taken from heavy vs. light
TABLE
5. Results of multiple regression analysis of the relationships between
substrate choice in the laboratory and the species mean for two forelimb
functional variables, teres major outforce (‘teres out’) and triceps outforce at
the metacarpal (‘triceps out’). Beta = multiple regression coefficient; n =
number of species; P = probability of type I error; %heavy = percentage of all
seeds harvested that were taken from heavy-substrate patches; :<coarse =
percentage of all seeds harvested that were taken from coarse-substrate patches
~
Dependent
variable
All species
Bipedaf species
lJo
heavp
OO
coarse
(It)
heat)
”,, cnarse
Quadrupedal species
O0
heavy
ug
coarse
Functinnal
variable
teres out
tri~epbout
teres out
triceps out
teres out
triceps out
teres nut
triceps out
teres nut
triceps out
teres out
triceps nut
Beta
R
9
9
9
9
5
5
5
5
4
4
4
4
3.9
5.2
-2.2
5.2
4.3
4.2
-2.7
5.3
1.3
8.8
20.6
26.9
t
4.8
3.1
-1.6
1.9
2.0
1.0
-1.1
1.2
0.5
3.2
5.7
7.2
P
0.003
0.02
0.17
0.11
0.19
0.41
0.38
0.35
0.71
0.19
0.11
0.09
HETEROMYID RODENT FORELIMBS
355
or fine vs. coarse substrates (Price & Longland, 1989). Relative use of coarse
substrate was uncorrelated with either teres or triceps outforces (Table 5), but
use of heavy substrate increased with teres and triceps outforces. There were no
significant relationships within quadrupedal or bipedal species treated
separately.
Deviations from expected seed-harvest rate for 10 heteromyid species (five
quadrupedal, five bipedal; see Morgan & Price, 1992) were positively but
insignificantly correlated with teres outforce (r = 0.18, P > 0.05), and were
significantly negatively correlated with triceps metacarpal outforce (r = -0.48,
P = 0.04, one-tailed).
DISCUSSION
Increasing availability of powerful computers has stimulated development of a
diverse array of multivariate methods for describing and analysing
morphometric variation within and among taxa (cf. Bookstein et al., 1985; Rohlf
& Bookstein, 1990). These methods are generally useful for a wide variety of
problems in evolutionary biology, including the study of linkages between form
and performance of ecologically relevant tasks (cf. Ehlinger, 1991) .
Application of these methods to the heteromyid forelimb has revealed
considerable variation in proportions of forelimb elements, both among species
within genera, and among genera. Like the variation in heteromyid forelimb
musculature described by Ryan (1989b), however, this skeletal variation is
primarily quantitative rather than qualitative, reflecting diversity in relative
sizes of muscle groups or in positions of muscle insertion or origin, rather than
variation in the presence or absence of characters. This constrains the value of
such data for answering questions of phylogenetic relationships in the
Heteromyidae, a perennial source of controversy (see Hafner & Hafner, 1983;
Ryan, 1989b; Brylski, 1992), but does not affect their value for addressing
questions of functional significance.
Most of the variation in forelimb shape reflected family-wide shortening of all
forelimb elements with increasing size, and broadening of the scapula.
Additional variation was produced by slight allometric differences between
quadrupedal and bipedal species, as well as by size-independent shape variation
among species within and between locomotion groups.
Major effects of size can be removed by reconstructing species to a common
general size. Analysis of such ‘reconstructed’ forms indicated that some shape
variation was organized along recognized subfamily lines. For example, the
Heteromyines Heteromys and Liomys differed from desert-dwelling heteromyids in
having a long scapula with proportionally greater area anterior to the spine,
short teres major process, longer humerus, and relatively long olecranon process
(Figs 4, 5C). Most other patterns of shape variation were not concordant with
recognized phylogenetic groupings; one Dipodomyine genus (Dipodomys), for
example, clustered with Perognathines, whereas the other (Microdipodops) did not
(Fig. 5C).
This lack of phylogenetic consistency could reflect adaptation to diverse
environments. Heteromyines differ from other heteromyids in that they inhabit
subtropical or tropical forests, rather than deserts or arid grasslands. Their
unusually shaped forelimbs could therefore indicate a more arboreal, less
356
M. V. PRICE
fossorial habit, especially in Heteromys. Fleming & Brown (1975) provide
evidence that Heteromys desmarestianus burrows less than Liomys salvini (Thomas); a
comparison with desert heteromyids remains to be done. The similarity in
forelimb shape between Dipodomys and Perognalhus (Fig. 5C) could also indicate
environmental similarity. Both genera are associated with flat topography and
fine soils, unlike Chaetodipus species, which often occupy steep or rocky terrain.
Much of the variation in forelimb skeletal proportions can be expected to
affect forelimb mechanical characteristics, and therefore is likely to be of
functional significance, rather than a simple by-product of nonadaptive
transformations within the Heteromyidae. Several lines of evidence support this
expectation. The inverse relationship between triceps outforce and deviations
from expected seed-harvest rate supports the prediction that low distal lever-arm
ratios increase the speed of distal forelimb extension/flexion. Nikolai & Bramble
(1983: 54) provide additional evidence of this relationship; for three species (two
bipedal, one quadrupedal), stroke frequencies during soil ‘patting’ motions
increased with decreasing triceps outforce. In addition, the association of teres
major outforce with soil compaction in habitats occupied by desert-dwelling
heteromyids [a result concordant with the earlier analysis of Heinz (1983) for a
smaller set of species], and the correlation between teres major outforce and use
of heavy substrates in the laboratory, support the idea that teres major outforce
indeed has a bearing on digging ability because compacted soils are more
difficult to dig through than loose soils (Vleck, 1979).
Nevertheless, distinguishing alternative explanations for the functional
significance of variation in forelimb mechanical properties will require a
thorough dynamic analysis of forelimb motions during digging and seed harvest,
as well as extensive comparative studies of digging and seed-gathering
performance.
The analysis presented here provides little statistical support for
Bartholomew’s hypothesis (Bartholomew & Cary, 1954) that bipedalism is
associated with specialization of the forelimb for nonlocomotory functions. This
conclusion should be viewed with caution, however, until comparisons of bipeds
and quadrupeds from other rodent families can be carried out: the small size of
the Heteromyidae (only two bipedal genera and four quadrupedal genera)
restricts the power of statistical comparisons of locomotion types. It is
worthwhile, therefore, to discuss some of the qualitative patterns of difference
between heteromyid bipeds and quadrupeds, with the hope that forthcoming
comparative information from other groups will permit a more rigorous
assessment of the association of forelimb functional characteristics with gait.
Bipeds differ from quadrupeds in having relatively smaller anterior scapula
area, shorter acromion, shorter humerus, more proximally placed deltoid
process, longer ulna, and wider humerus at the epiconmdyles (Fig. 4). Some of
these shape differences conform to the simple expectation that the quadruped
forelimb serves a support and propulsion function, in addition to being used in
digging and foraging. The greater anterior area of the quadruped scapula
suggests that muscles used in stabilization and rotation of the pectoral girdle are
relatively more developed than in bipedal species (see also Lehmann, 1963;
Ryan, 1989b; Brylski, 1993). The longer quadruped humerus would permit
greater stride length for a given limb excursion angle. The narrower humerus at
the epicondyles may indicate less rotational capability in the distal forelimb, and
hence greater joint stability under loading.
HETEROMYID RODENT FORELIMBS
357
Desert quadrupeds have several features that should increase digging ability at
the expense of rapid locomotion. The scapula, for example, is short and has a
long teres major process, which increases effective teres inforce but restricts limb
excursion angle. The ulna has a lever-arm ratio more favourable for generating
force than moving the foot rapidly relative to the body. Desert quadrupeds often
are associated with more rocky, steep, three-dimensional habits than bipeds
(Reichman & Price, 1993) and may need a relatively powerful distal forelimb for
climbing. Also, they may be able to use flexionlextension of the back as a means
of increasing stride length without compromising forelimb power (Hildebrand,
1985a). It is interesting to note that quadrupedal species associated with more
open, level habitats where climbing would be relatively unimportant (Perognathus
spp.) are convergent on bipeds in having smaller triceps outforces than the other
quadrupeds (Table 5).
Small triceps outforces in bipeds and in Perognathus indicate that the
heteromyid forelimb is not designed in all respects for generating power during
scratch-digging. I t is possible that heteromyids are ‘hook-and-pull’ diggers,
rather than scratch-diggers (Hildebrand, 1985b), or that the design of the distal
forelimb is influenced by its function in seed harvest.
Most discussion of the adaptive significance of bipedalism in desert rodents has
focused on its direct consequences for locomotion: speed, leaping distance,
manoeuverability, or energetic efficiency (Thompson et al., 1980; Biewener et al.,
1981, 1988; Garland, 1983; Emerson, 1985; Thompson, 1985; Biewener &
Blickhan, 1988; Longland & Price, 1992). If the trends described here apply
consistently to other groups, then a reasonable conclusion is that an indirect, but
evolutionarily important, consequence of gait is that it modifies the pattern of
selection on suites of other characters, such as those of the forelimb, as
Bartholomew & Gary (1954) and Nikolai & Bramble ( 1983) have suggested.
For example, a change in the forelimb (e.g. a lengthening of the ulna with no
change in the olecranon) that increases the speed of seed harvest from the soil
may have little associated detrimental effect in a form that climbs only rarely
(such as primitive bipeds or quadrupeds of flat terrain), but would otherwise be
disadvantageous. Selection may therefore increase ulna length in bipeds and
Perognathus species, but not in other forms. This in turn could promote
divergence in foraging behaviour, for example, by changing the relative
profitability of sparse and dense seed patches, and further alter subsequent
selection on locomotory traits that affect costs of searching for seed clumps
(Reichman, 1981; Price, 1983).
The possibility that bipedalism is intimately related to selection for forelimbdependent function comes to mind only if we consider the organism as a whole
functioning unit in an ecological context, rather than focusing on a single aspect
of behaviour or morphology. This underscores the importance of integrating
perspectives from fields as disparate as morphology, behaviour, and ecology, if
we are to develop a thorough understanding of the diversity of form in the
organic world.
ACKNOWLEDGEMENTS
I am indebted to Kevin Heinz, who identified heteromyid forelimb
morphology as an interesting problem, made the morphological measurements,
and completed a preliminary analysis of variation within the genus Dipodomys
358
M. V. PRICE
and its correlation with soil associations. Bill Longland and Patty Endo
computerized the data and assisted with data analysis. I thank the Duke
morphometrics study group, Kathleen Smith, Rich Strauss, Dennis Bramble,
and especially Sharon Emerson for educating me in current morphometric
analytical methods and helping to interpret the resulting patterns. As always,
Nick Waser has contributed greatly to all phases of this study. Comments by
James Ryan, Enrique Lessa, and Norman MacLeod greatly improved the
manuscript. This work has been supported by intramural grants from the
University of California, Riverside, Academic Senate, and by National Science
Foundation grant BSR 84-07602.
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APPENDIX 1
Calculations used to generate 'functional variables' that reflect the mechanical advantage of various
forelimb elements. Please refer to Figure 2 for geometric definitions and Table 1 for definition of
morphometric variables.
Assume theta = 45"
alpha = 45-arctan (spinter/scaplen)
sin (alpha) = x/y
-+ x = sin (alpha) [(scaplen)'+ (spinter)']'"
cos (alpha) = z/y
-+ z = cos (alpha) [(scaplen)'+ (spinter)*]"'
tan (beta) = (x+deltpos)/z
- + b e t a= arctan [(x+deltpos)/z]
A = cos (beta)
B = A (dcltpos/humlen)
humerus outforce = deltpos/humlen
C = oleclen/(ullen- oleclen)
D = oleclen (ullen + metalen-oleclen)