BiologicalJournal of the Linnean Society, 11: 153-168. With 9 figures
March 1979
The ilio-sacral articulation in frogs :
form and function
U
SHARON B. EMERSON
University ofIllinois at Chicago Circle,
Chicago, Illinois 60680, U.S.A.
Acceptedforpublication June 1978
The amphibian order Anura (frogs) is a major group whose origin appears related to the
transformation of its locomotor system for saltation. However, the ilio-sacral articulation, a
uniquely specialized part of the frog locomotor morphology, remains largely unstudied.
Preliminary work reveals significant differences in the morphology of the ilio-sacral articulation
among extant frogs and suggests that differences in types of articulation are correlated with different
directional movements at the joint, with specificlocomotor modes, and with phylogenetic groupings.
KEY WORDS: -frog- pelvis-ilio-sacral articulation- locomotion- Anura,
CONTENTS
Introduction
. . . . . . . . . . . . . . . . .
Methods and materials
. . . . . . . . . . . . .
Morphology of the ilio-sacral articulation
. . . . . . .
Phylogeneticsignificance of the articulation types
. . . . .
Predictions of movement from morphology
. . . . . . .
Movement variation among frogs with the same articular morphology
Summary . . . . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . .
References
. . . . . . . . . . . . . . . . .
Appendix . . . . . . . . . . . . . . . . . .
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INTRODUCTION
Morphological specializations of the vertebral column and pelvis are among
the key ordinal adaptations of frogs (order Anura). One of the most unusual of
these specializations is the radical transformation of the sacral region. For
example, frogs are the only extant vertebrates in which the ilia articulate ventral
to the sacrum. Despite the importance of sacral and pelvic morphology to understanding frog locomotion and the evolutionary origins of the group, the
anatomy has not been extensively studied. Differences in the shape of pelvic
bones have been used as characters in systematic studies (e.g. Lynch, 1971;
Heyer, 19751, but the nature of the ilio-sacral articulation is unknown for most
frogs. Only brief descriptions for individual species appear in the early literature
0024-4066/79/020 153-16/$02.00/0
153
0 1979 The Linnean SocietyofLondon
I54
S.B. EMERSON
(Gaupp, 1896; Beddard, 1895, 1907; Devanesen, 1922) and in some recent
papers by Indian researchers (Charan, 197 1, 1973). There have been three
functional studies of the frog pelvic region (Green, 1981 ; Palmer, 1960; Whiting,
1961).Green’s (1931) work is primarily concerned with the role of the urostyle in
anuran locomotion. Palmer (1960)and Whiting (1961)demonstrate mobility at
the ilio-sacralarticulation in three species of frogs.
In this paper, I will examine one critical aspect of frog pelvic morphology: the
ilio-sacral articulation. Preliminary work, outlined below, reveals significant
differences in the morphology of the ilio-sacral articulation among extant frogs,
and these differences appear to be correlated with phylogenetic groupings as well
as with locomotor mode and ecology. Furthermore, key characters of the
articulation may be identifiable in fossil material. For these reasons, the frog
pelvis represents an appropriate system for studying the intersection of
functional morphology, phylogenetic interpretation, and behavioral ecology.
METHODSAND MATERIALS
Many of the species included in this study are rare in collections and only a few
preserved and/or osteological specimens were available for examination.
Therefore, a preliminary study was undertaken among adults of common species
to measure variability in pertinent morphology. Results of this work indicate that
among the species examined articulation morphology is not sexually dimorphic
nor size-related. Origin and insertion of musculature and ligaments are
consistent within adults of a species. Measurements of sacral diapophyseal
expansion show a coefficient ofvariation ( V )between 5 and 10.
Representatives of 54 species of frogs were dissected to examine the ilio-sacral
articulation and the origin and insertion of related musculature (Appendix).
Characteristic locomotion for each species was determined from literature reports
and, personal observations. Five modes are recognized : swimming, jumping,
hopping, walking and burrowing. Walking and burrowing are self-explanatory.
Fast walking is used to denote those species which are described in the literature as
runners, as it is uncertain, at this time, whether they conform to Hildebrand’s
( 1974) definition of running (each foot on the ground less than 50%of time of total
stride). The ability to swim is almost ubiquitous among frogs and it is listed as a
specific locomotor mode only in those species that are totally aquatic (see
Appendix). Delimiting the difference between jumping and hopping is difficult.
Both the absolute jump distance and the relative jump distance (absolute distance/body length) of a frog are size-dependent(Emerson, in press). Larger frogs,
generally, jump longer absolute distances, but smaller Frogs, generally, have
longer relative jump distances. In addition, some frogs show considerable
variation in distance among jumps. For this paper, frogs which have been
observed or reported to jump shorter distances than one would expect for their
body size (less than 8-9 times body length for frogs under 100 mm) are listed as
hoppers, and all others are consideredjumpers (seeAppendix).
The dried skeletons of 140 additional species were examined to supplement
data obtained from dissected specimens. Measurements were taken to
characterize sacral morphology. The orientation of the sacral diapophyses in the
horizontal plane was measured as the angle between the midline of the vertebral
column and the central axis of the right sacral diapophysis. Degree of expansion
ILIO-SACRAL ARTICULATION IN FROGS
155
of the sacral diapophysis was measured between the anterior and posterior edges
of the right sacral diapophysis.
The ilio-sacral articulations of three species, Bufo americanus, Rana pipiens, and
Kaloula pulchra were paraffin embedded and sectioned to provide morphological
detail. These three species were chosen because they represent the major patterns
of ilio-sacral articulation. Serial sections were cut at 15-20 pm and triple stained
with Harris hematoxylin, Van Giesen’sand orcinol fuchsin.
Movement at the articulation during locomotion was recorded by
cineradiography and sequential still X-rays in Bufo boreas, Rhinophrynus dorsalis,
Rana pipiens, Phrynohyar venulosa, and Pachymedusa dacnicolor. Non-simultaneous
films in dorso-ventral and lateral projections were taken at 100 and 190 frames
per second. Films were studied with a Vanguard Motion Analyser.
MORPHOLOGY OFTHE ILIO-SACRAL ARTICULATION
The dissections revealed two heretofore undescribed patterns of articulation
between the pelvic girdle and the sacrum in frogs. Corresponding to these two
types of articulation are two patterns of ilio-lumbaris muscle attachment. Whiting
( 1961) recognized different patterns of muscle attachment in the three species he
studied, but he did not examine the detailed morphology of the articulation.
Articulation &be Z (Fig. IA). The sacral diapophysis is broadly expanded. The
diapophysis may be completely bony or composed, in part, of cartilage which
extends laterally from the bony part of the sacral diapophysis. The distal border of
the diapophysis is antero-posteriorly elongate. There is no ligamentous
attachment between the ilium and the sacrum. There is, however, a superficial
ligament which arises on the lateral aspect of one ilium and runs across the back to
insert on the lateral aspect of the other ilium, forming a cuff. This ligament is
superficial to all dorsal musculature. Sesamoids are variably developed in the
ligament where it extends over the distal border of the diapophysis, but no welldefined joint capsule is present around the ilio-sacral articulation. The iliolumbaris muscle originates on the lateral aspect of the ilium, one-third to one-half
the distance from the anterior tip. I t inserts on the transverse processes of presacral vertebrae 4-6. This type of articulation is found among members of the
Pipidae, Pelobatidae, Rhinodermatidae, some Discoglossidae, some Hylidae, and
some Microhylidae.
Articulation Qpe ZZ (Fig. IB). The bony part of the sacral diapophysis may or may
not be expanded, with variable cartilaginous extension. The connection between
the ilium and the sacrum is by an internal ligament which arises on the anterolateral aspect of the ilium, and inserts on the sacrum ventral to the dorsal back
musculature. A well-developed joint capsule is present around the ilio-sacral
articulation. The ilio-lumbaris muscle originates on the antero-lateral tip of the
ilium. This type of articulation is found among members of the Ranidae,
Lep todactylidae, Rhacophoridae, Bufonidae, Ascaphidae, Rhinophrynidae, some
Discoglossidae, some Hylidae, and some Microhylidae.
Within the second type of articulation, with an internal ligament, there are two
major subgroups.
Articulation type IZA (Fig. 2A). The sacral diapophysis extends laterally and is
distally expanded. The distal borders of the diapophyses form arc segments of a
circle. The internal ligament is broad and inserts on the dorsal surface of the
156
S.
B. EMERSON
Figure 1. Dorsal view of the morphology of the two major patterns of articulation. Insets show cross
sections across the sacral diapophysis. Arrows in insets point to the relation of the ligament to the
superficial back musculature. Cartilaginous portions of the sacral diapophyses are stippled. Bone
and sesamoids are black. Ligaments are shown in white. Abbreviations: ex, Extensor dorsicomrnunis muscle: sd, sacral diapophysis; ci, coccygeo-iliacusmuscle; a,coccygeo-sacralismuscle;
i, ilio-lumbaris muscle; lig., ligament; s, sesamoid. Scale bars represent 1 mm.
diapophysis near the midline of the sacrum. A cartilaginous tip is present on the
distal end of the sacral diapophysis and forms a ventrally turned lip. The ilium is
positioned ventral to the lip in a groove. A well-developed sesamoid occurs
between the ventral surface of the ligament and the dorsal surface of the
cartilaginous part of the diapophysis. The ilio-lumbaris muscle inserts on the
transverse processes of pre-sacral vertebrae 4 to 7. This pattern is found in some
members of the Ranidae, Hylidae, Leptodactylidae, Microhylidae, and Discoglossidae,and in all species examined of the Bufonidae and Rhinophrynidae.
Articulation type ZZB (Fig. 2B). The sacral diapophysis is posterolaterally
oriented and not expanded. The internal ligament is narrow and inserts on the
dorsal surface of the diapophysis near its distal tip. There is a small cartilaginous
tip on the diapophysis, but no groove is formed. A well-developed sesamoid is
present in the internal ligament at the distal tip of the diapophysis. The iliolumbaris muscle inserts on the transverse processes of all presacral vertebrae.
This pattern is found in most members of the Ranidae, in A~cuphw,and in some
Leptodactylidae.
ILIO-SACRALARTICULATION IN FROGS
Y
..:..
..:..
.:>..:. .
9
sn
B
D
E
S
.....
......
,.....
.....
...,:i
:;.
157
s
IL
C
F
IL
Figure 2. Diagrammatic representations of the two variants of articulation type 11. A, Articulation
type IIA: dorsal view of the pelvic girdle and sacrum; B, postero-lateral view ot the articulation; C,
cross section of articulation. D. Articulation type IIB: dorsal view of the pelvic girdle and sacrum; E,
postero-lateral view of the articulation; F, cross section of articulation. Lines indicate points at
which cross sections were taken. Abbreviations as in Figure 1 .
The cartilaginous extensions of the diapophyses, the position and shape of the
sesamoids, and the origin and insertion of the articular ligaments are critical to
identification and functional interpretation of the patterns of sacral articulation
in frogs. Previous workers have assumed that little variation exists at the
articulation because differences in joint morphology are not obvious from dried
skeletal material (used in most previous studies). The cartilaginous extensions of
the diapophyses and the sesamoids are always distorted and often lost in this type
of preparation.
Measurements of degree of expansion of the bony part of the sacral
diapophysis from dried skeletons do vary among species (see Fig. 31, but are not
sufficient to characterize sacral morphology. This is because it is the cartilaginous
extensions which often show the greatest amount of expansion. Furthermore,
expanded sacral diapophyses are found associated with two fundamentally
different types of articulation, Type I and Type I1 (Fig. 31, and appear to be
involved with different patterns of movement at the articulation.
PHYLOGENETIC SIGNIFICANCE OFTHE ARTICULATIONTYPES
Figure 4 shows the distribution of the two major types of articulation
superimposed on a recently proposed dendrogram of anuran phylogeny (Kluge
& Farris, 1969). Regardless of which phylogenetic schema is used (see Lynch,
1973 for an alternative), and which type of articulation is considered primitive,
158
S. B. EMERSON
. .
120-
110
"
*.
loo
+
'
.
so-
*
c
.
c
*
c
cc
1
.
*
+
10
'r
I
10
30
50
70
so
110
degree of expansion
Figure 3. The degree of bony sacral expansion for 46 genera of frogs plotted against the orientation
of the diapophyses. Stars represent frogs with articulation type I, circles articulation type 11.
Ascophidae
(I)
0
Discoglossidae (4)0 A
P i p i d a e (2) A
Rhinophrynidae ( 1 ) 0
Pelobatidae (4) A
Bufonidae (2) 0
Atelopodidae (2) 0
L e p t o d o c t y l i d o e ( 1 7 )0
H y l i d a e 19) 0 A
R a n i d a e (13) 0
R h a c o p h o r i d a e (4) 0
M i c r o h y l i d a e (16) 0 A
Figure 4. Distribution of the two major articulation types superimposed upon a dendrogram
showing the relations of the major anuran families (after Kluge & Fmis, 1969). Triangles represent
articulation type I, circles articulation type 11. Numbers in parentheses indicate number of genera
examined in each family.
ILIO-SACRALARTICULATION IN FROGS
159
B
C
Figure 5. Diagrammatic dorsal views of the sacrum in the three types of articulation. Black circles
show position of Ligament scars. A. Type I, no ligament scars. B. Type IIA, ligament scars near
midline of sacrum. C. Type IIB, ligament scars on distal edges of diapophyses.
each system must have evolved independently several times. Distribution of
articulation types may, however, provide some insight into the relationships
among extant frogs as the patterns of articulation do not appear to be randomly
distributed among frog species. Except for the Hylidae, Microhylidae, and
Discoglossidae, the articulation patterns are family specific.
Significantly, the major articulation es can be identified from bone alone by
the presence or absence and position o ligament scars on the dorsal surface of
the sacrum (Fig. 5 ) . The bony part of the sacrum of articulation I has no ligament
scars, the sacrum of type IIA articulation has ligament scars near the midline of the
diapophyses, and type IIB has ligament scars on the distal tips of the diapophyses.
Again, shape of the diapophyses (ie. expanded or not) is not sufficient, by itself,
for identification of articulation types as the bony part of the sacrum of a type I
articulation may appear similar to the bony part of the sacrum of either of the type
I1 articulations. Only the presence or absence and position of the ligament scars
can differentiate the articulation types, if the cartilaginous extensions have been
lost. Depending on preservation, then, the fossil record could provide a clue to the
evolution of articulation types. Secondly, identification of an articulation type for
a fossil frog may provide information regarding its locomotor behavior (seeNevo,
?
S. B. EMERSON
160
1968, for example) as certain articular morphologies appear correlated with
specificlocomotor repertoires ( s e e discussion below).
Unfortunately, the fossil record of frogs, generally, is poor. The earliest
unmistakable frog fossils date from the late Jurassic (Estes & Reig, 19731, and
include only three genera. I have examined specimens of one of these genera
(Eodiscoglossus), but only the ventral surface of the sacrum has been preserved
(Vergnaud-Grazzini & Wenz, 1975). Vieraella and Notobatrachus, the other two
genera, need to be re-examined carefully (although there is no mention of
ligament scars in the original descriptions) as the published photographs and
reconstructions of the specimens are inadequate to allow determination of
possible sacral ligament scars.
PREDICTIONS OF MOVEMENT FROM MORPHOLOGY
The variation in morphology of frog sacro-iliac joints can be generalized into
three basic patterns, as illustrated in Figure 6. Initial hypotheses of what types of
movement are facilitated by each of these morphologies were formulated by
constructing and manipulating Styrofoam models that approximate these three
patterns. In articulation type I, antero-posterior movement in a horizontal plane
is maximized. In articulation type IIA, the greatest degree of movement is lateral
rotation of the pelvic girdle on the sacrum in a horizontal plane. In articulation
type IIB, the greatest degree of movement is dorso-ventral rotation of the pelvic
girdle in the vertical plane.
Type 1
Type IIA
Type I I B
Figure 6 . Diagrammatic representations of the three major articulation types in dorsal view. Stippled
areas represent ligaments. Ilio-lumbaris muscle shown by lines with arrows. Type I : predominant
movement, antero-posterior. Type IIA: predominant movement, lateral rotation. Type IIB:
predominant movement, vertical rotation.
Tests ofpredictions. Cine X-ray films and sequential still X-rays of animals with
the three articulation types confirm the predictions generated from the
morphological models (Table 1). These results are consistent with data from
Whiting’s (1961)study where movement at the articulation was effected by direct
stimulation of the ilio-lumbaris muscle. Furthermore, cineradiographic analysis
reveals ( 1) that different movements at the articulation are correlated with
different modes of locomotion, and (2) that species with the same articulation
morphology may show significant differences in degree of movement (Table 1).
ILIO-SACRALARTICULATION I N FROGS
161
Table 1. Movements at the sacrum during locomotion as determined by
cineradiography. (N, number of sequences, measurements are given in degrees).
The articulation type of each animal is given in parentheses after the species
name
N
x
8
f6
f4.1
1
65.9
49.3
28.8
20.0
-
-
5
5
6
8.8
3.6
14.2
f 1.6
7-11
+1.1
2-5
12-16
S
Range
1. Jumping: vertical rotation of the pelvic girdle
a.
b.
c.
d.
Rana pipiens (IIB)
EuJo boreas (IIA)
Phrynohyas uenulosa (HA)
Pachymedlwa dmicolor ( I )
1
4
+5.8
55-15
44-55
24-33
11. Walking: lateral rotation of the pelvic girdle
a. BuJo boreas (IIA)
b. Phtynohyas uenulosa (IIA)'
c. Rhinophrynus dorsalis (IIA)
111. Walking: antero-posterior movement of the pelvic girdle
a. Phrynohyas venulosa (IIA)"
b. Pachyrnedusa dmicolor (I)
f 1.5
10%of total body length
20%of total body length
* Measurements taken from vertical walking sequences.
Verticol
r ototion
Lateral
rot otion
Antero posterior
movement
Table 1 (Figure).Three types of movement for which data are presented in Table 1. The black circle
represents the position of the sacrum. Arrows indicate direction of movement.
The situation is complicated because there is not a one on one mapping of
behavior on morphology. Variants of both major articulation types appear to
represent adaptations for the same locomotor modes. And, some articulation
morphologies appear correlated with a diversity of locomotor modes, while
others are behavior specific. To facilitate presentation, I will first discuss the
simplest situation where movement is restricted to one direction and correlated
with a single locomotor mode, and then proceed to the more complicated cases
where multi-directional movement takes place, and a suite of locomotor
behaviors is involved.
Articulation tjpe ZZB. Only this articular type is correlated with a specific
movement: dorso-ventral rotation of the pelvis in the vertical plane.
Cineradiographic films show that this movement takes place during jump takeoff and landing in Rana pipiens. The restriction of movement to a vertical plane
with this morphology and the involvement of such movement in jumping
suggests that articulation type IIB should be distributed among frogs which use
162
S. 8 . EMERSON
jumping as their dominant terrestrial locomotor mode. Literature survey and
personal observations on live frogs confirm this prediction. With the exception
of the dendrobatids, which are short distance jumpers, all frogs with articulation
type IIB are strong jumping species (seeAppendix).
Vertical rotation at the ilio-sacral articulation during jumping was initially
demonstrated by Whiting (1961) in R a m temporaria. He suggested that vertical
rotation may be particularly important in jump landing for absorbing inertial
energy. A recent review paper on jumping by Bennet-Clark (1977) suggests
another possible function as well. Bennet-Clark demonstrated that in small
animals (under one metre) where more power is used in jump take-off than can
be directly supplied by muscles, extra power may come from energy stored in
stretched tendons or ligaments. The morphology and position of the internal
ligaments in articulation type IIB suggest that they could function as energy stores
when the frog is in the pre-jump position and the pelvic girdle is rotated ventrally.
The articular ligaments are stretched when the pelvic girdle is rotated ventrally,
and during jump take-off, as the angle bemeen the vertebral column and pelvic
girdle is decreased (thebody straightens out as it leaves the ground), stored energy
of the ligaments could be released. Measurements from live animals compared to
freshly killed frogs suggest that this may be the situation. The mean angle of pelvic
rotation for live Runapipiens in the pre-jump position (fromcine X-rays and stills)
is 65.9O. In six freshly killed Ranapipiens the greatest degree of pelvic rotation was
only 4 5 O . (Thismeasurement was taken by suspending the frog at the sacrum, with
the legs in the pre-jump position, and measuring the angle of the ilia. Forty-five
degrees is probably a generous estimate, since the weight of the hindlimbs
probably caused some passive stretchingof the ligaments).
Articulation type ZZA. Whiting (1961)and Palmer (1960)studied movement at the
articulation of Rana temporaria and Discoglossus pictus during jumping and of
Xenopus laevis during swimming. They did not examine other types of frog
locomotion. Cineradiographs reveal that among the articulation type IIA frogs
filmed (&yo boreas, Rhinophrynw dorsalis, Phrynohyas venulosa) lateral rotation of the
pelvis is an integral movement in walking. Figure 7 illustrates this movement
during walking in Rhinophrynus dorsalis. Given the morphology of the articulation
in these frogs (see Fig. 6), it appears likely that lateral rotation is accomplished by
asymmetrical contraction of the ilio-lumbaris muscle. Alternate contractions
would result in one ilium being pulled forward in the track formed by the
ventrally turned lip of the sacral dia ophysis, with the internal ligament on the
same side sliding over the dorsal sur ace of the sacral diapophysis in an anterior
direction. Concommitant with this, the internal ligament and ilium o n the contralateral side would move posteriorly. The distal border of the sacral
diapophysis then prescribes an arc through which the ilium and internal
ligament move during lateral rotation.
The lateral rotation of the pelvis in Rhinophrynus dorsalis results in the femur of
the protracting hindlimb having a more anterior position than would be possible
if the pelvis were fixed. Concommitant with the lateral movement of the ilium is
marked lateral flexion of the vertebral column. Lateral flexion of the vertebral
column increases the reach of the protracting forelimb and indirectly supports
the hypothesis that lateral rotation of the ilium is due to asymmetrical
contraction of the ilio-lumbaris muscle. Lateral rotation of the pelvis during
walking would thus increase stride length, and if stride rate is maintained
P
ILIO-SACRALARTICULATION IN FROGS
+
I63
I
Figure 7 . Tracing cineradiograph of Rhinophrynus dorsalis walking. Vertebral column is in white; the
rest of the skeleton is black. Dotted line shows the midline of the body.
constant, result in increased speed. Higher speeds among quadrupeds may result
from increased stride frequency and/or increased stride length.
If articulation type IIA is a specialization for increasing speed of walking, then
one would predict that frogs having this type of morphology would use walking
as their main form of locomotion, and that the degree of expansion of the sacral
diapophyses should increase from frogs which are primarily jumpers to those
that are slow and fast walking species. Behavioral notes from the literature as
well as personal observations (see Appendix) do indicate that all articulation type
IIA frogs examined, with the exception of Discoglossus pictus, use some combination of walking, burrowing and/or hopping (short distance jumping) locomotion. This is in contrast to frogs with articulation type IIB, which are primarily
long distancejumpers.
If degree of vertical rotation during saltation is related to jumping ability (see
discussion above), then one might expect type IIA frogs to jump relatively
shorter distances k e . : hop) than type IIB frogs, all other things being equal. This
is based on the fact that the degree of vertical rotation during jump take-off is
less in the type IIA frogs filmed than those with type IIB and this correlates with
their poorer jumping distances.
The functional role of the type IIA articulation morphology in burrowing is
problematical. The preliminary data collected do not include cineradiographic
films of burrowing locomotion, and other work (Emerson, 1976) indicates that
many morphological specializations are the same for walking and burrowing. It
is possible that lateral rotation is a specialization for burrowing as well as for
164
S. B. EMERSON
Figure 8 . Degree of sacral expansion in genera of frogs of three families plotted against locomotor
mode and ecology. Vertical lines represent the range, numbers show the mean. Ranidae: 1, Rana; 2,
Kassina; Leptodactylidae:3, Leptodactylus; 4, Pseudophyne; Bufonidae: 5, Bufo; 6 , E g o calamita.
walking. Until more work is completed, one can only say that frogs with
articulation type IIA do tend to use a suite of locomotor behaviors (walking,
burrowing, and hopping) not characteristic of frogs with articulation type IIB.
The second prediction of increased expansion of the sacral diapophyses in
articulation type I1 species that are primarily slow and fast walkers (e.g. Kmsina
senegalensis (Ranidae), Pseudophryne occidentalis (Leptodactylidae); Bufo calamita
(Bufonidae))is borne out by comparing these species with species of different
locomotor modes but belonging to the same family. In the Ranidae and
Leptodactylidae there is not only an increase in sacral expansion when walking,
burrowing, hopping species are compared to jumping species, but a shift in the
point of internal ligament attachment as well. Jumping species have a narrow
internal ligament that inserts on the distal edge of the sacral diapophysis (type
IIB), while walking, hopping, burrowing species have a broad internal ligament
that inserts on the proximal part of the sacral diapophysis (type IIA). In the
Bufonidae, the third family examined, all species have a type IIA articulation,
but there is a greater degree of sacral expansion in the fast walking Bufo calamita
than in the slow walking species of Bufo (Fig. 8).
Articulation type 1. Palmer ( 1960) found antero-posterior movement at the
sacral articulation during swimming in a type I articular morphology frog,
Xenopus laevis. My data indicate that antero-posterior movement occurs in
Pachymedusa dmicolor, another type I frog, during walking. A survey of frogs with
165
ILIO-SACRAL ARTICULATION IN FROGS
A
B
Figure 9. The sacrum of a type I articulation compared to a type IIA articulation. Circles of curviture
were drawn by defining the radius as the distance from the midpoint of the sacrum to the lateral
edge of the right diapophysis. Stippled areas represent cartilage.
type I articular morphology shows a repertoire of locomotor behavior similar to
that found among frogs with type IIA articular morphology (walking, hopping,
burrowing). However, in articulation type I, the distal borders of the sacral
diapophyses, although expanded, do not define an arc of rotation such as occurs
in type IIA frogs (Fig. 9). The lateral border is relatively straight, with the
expansion largely in an antero-posterior direction. Asymmetrical contraction of
the ilio-lumbaris muscle could result in a small degree of lateral rotation, but
the cuff-like morphology of the superficial ligament would restrict it from
reaching the extent seen in articulation type IIA. The greater degree of expansion
in an antero-posterior direction in the sacral diapophyseal border of type I frogs
may instead be correlated with the greater antero-posterior movement in these
frogs (20% body length) as compared to a type IIA frog ( 10% body length). This
antero-posterior movement may be important for increasing the reach of the
animal during walking and climbing.
Although walking locomotion occurs in both type I and IIA frogs, films of
Pachymdusa dacnicolor (type I) compared to Bufo boreas (type IIA) show some
differences in pattern of locomotion. Both animals utilize the standard diagonal
pattern of limb movement, but the “fast” walking speed is slower in the type I
species than the “average” walking speed of the type IIA species. While the stride
frequency is 435 mseconds for the Bufo boreus (an average gait sequence from 15
runs), it is 1230 mseconds for Puchymedusa dacnicolor (the fastest gait sequence
from six runs).
MOVEMENT VARIATION AMONG FROGS WITH THE SAME ARTICULAR MORPHOLOGY
Table 1 shows significant differences in amount of movement in specific
directions among type IIA frogs which have the same articular morphology.
These data suggest that movement at the articulation is not controlled exclusively
by the pattern of ligamentous attachment between the ilium and the sacrum.
Manipulation of freshly killed animals supports this as well. When the
musculature is removed around the articulation in freshly killed animals, there is
no restriction to movement in the vertical direction, and there is a larger degree
of lateral rotation and antero-posterior movement than when the musculature is
166
S. B. EMERSON
intact or than observed in live frogs. On the basis of these preliminary data, I
would suggest that movement at the articulation is muscle-mediated, and that
the ligaments may function primarily as check ligaments during locomotion. This
is a testable hypothesis and a series of experiments on the role of the pelvic
musculature in effecting movement are currently underway.
SUMMARY
The morphology of the ilio-sacral articulation in frogs is correlated with
different patterns of mobility at the joint and different locomotor behaviors.
Overlain on these basic differences in articulation among frogs is variation in
other aspects of pelvic and vertebral morphology as well: muscle origin and
insertion, urostyle fused or free, length and angle of the ilia, length of transverse
processes of the pre-sacral vertebrae, and the articulation pattern of the presacral vertebrae. 0bviously, the role of these additional morphologies must be
established and integrated with the data on articular morphology before the
form-function complex is completely understood. This paper is the first step
towards that end, and work on other aspects of pelvic and vertebral morphology
is underway.
ACKNOWLEDGEMENTS
The data base for this study is the amphibian collection at the Field Museum of
Natural History, Chicago. I thank Hymen Mam for allowing me access to this
material and providing working space in a congenial atmosphere. I thank C.
Vergnaud-Grazzini and S.Wenz, Institut de Paleontologie, Paris for allowing me
to examine fossil specimens of Eodiscoglossw. Live Rhinophrynus were obtained in
Mexico under Mexican collecting permit #50-76/896 to the author.
X-ray equipment was provided by Harvard University, Museum of
Comparative Zoology and Brookfield Zoological Gardens. I appreciate the time
and technical assistance of P. Parker, E. Gordon, A. Crompton, and F. Jenkins.
H. Barghusen was especially helpful in reviewing a preliminary draft of this
manuscript. L. Radinsky assisted in the illustrations. I thank them both for their
time and interest.
This research is supported, in part, by a Research Board Grant fiom the
University of Illinois and National Science Foundation Grant DEB 7 7-2 190 1.
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to other genera of Batrachia. Proceedings of the Zoological Society of London, 1907 : 324-352.
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APPENDIX
Species
Articulation
Locomotor mode
Ecology
I
I
swimming
swimming
aquatic
aquatic
IIB
jumping
semi-aquatic
I
hoppjng
jumping
semi-aquatic
semi-aquatic
I1A
walking, burrowing
hopping
fossorial
I
I
hopping, burrowing
hopping, burrowing
hopping, walking
fossorial
fossorial
terrestrial
IIA
I IA
IIA
IIA
I IA
IIA
hopping, burrowing
hopping, walking
hopping
hopping, burrowing
running, burrowing
hopping, walking
terrestrial
terrestrial
terrestrial
terrestrial
terrestrial
terrestrial
11A
fast walking
terrestrial
IIA
IIA
hopping
walking, burrowing
hopping
terrestrial
fossorial
IIA
walking, burrowing
terrestrial
IIB
jumping
terrestrial
IIB
jumping
terrestrial
I IB
?
semi-aquatic
we
Pipidae
Xenopus laeuir
Pipa pipa
Ascaphidae
Ascaphus truei
Discoglossidae
Bombina orientalis
Discoglossus pictus
Rhinophrynidae
Rhirwphrynus dorsalis
Pelobatidae
Pelobaterf i c u s
Scaphiopus couchii
Megophys monticola
Bufonidae
Bufo boreas
Bufo blombergii
Bufo marinus
Bufo amencanus
Bufo calamita
Atelopus zetehi
Pelanophryniscus
stelzneri
Leptodactylidae
Physalaemuspustulosus
Notoden bennetti
Pseudophryne
occidentalis
Leptodactylus
pentadacty lus
Eleutherodactylus
punctarioli
Telmatobius
maworatus
9
IIA
I
S. 8. EMERSON
168
APPENDIX-CO~L
Species
Rhinodermatidae
Rhinodena danutnii
Hylidae
Pseudacris
tnseriata
Hyla regdla
Hyla nnerea
Hyla gratiosa
Phrynohyas vtnulosa
Agalychnis callidryas
Pachymedusa dacntcolor
Litorta rubella
Smihsca phaeota
Dendrobatidae
Dendrobales
lrnctorlus
Ranidae
Rana catesbetana
Rana pipicnr
Rhacophorus
leucomystax
Rhacophorus colleti
C hiromanlts rufescens
Hyperoltus manoratus
Leptopelis aubryt
Leptopelis bocagzi
Hemisus marmoratus
Katstna senegalensis
Htldebrantta omata
Microhylidae
Kaloula pulrhra
Articulation
Locomotor mode
Ecology
I
jumping
terrestrial
IIA
IIA
I
I
IIA
Jumpfng
Jumping
Jumpfng
JumPW
jumping
jumping, walking
jumping, walking
terrestrial
terrestrial
semi-arboreal
arboreal
aboreal
arboreal
arboreal
we
I
I
I
I
3
?
jumping, walking
semi-arboreal
IIB
walking, hopping
terrestrial
IIB
IIB
jumping
jumping
aquatic
semi-aquatic
IIB
IIB
IIB
IIB
IIB
IIB
I IA
Jumpfng
Jumping
Jumping
Jump'ng
jumping
jumping, burrowing
walking, burrowing
hopping
fast walking
jumping, burrowing
arboreal
arboreal
arboreal
arboreal
arboreal
fossorial
fossorial
I IA
IIB
I
(,&hoglossus molossus
Hypopachus vanolosus
11A
11A
Mtcrohyla rubra
Phrynumerus annectens
IIA
I
Kalophrynus
pleurastigma
L ophixalus ripanus
Gastrophryne
tarolinensts
Myseriella subnigra
Dasypop~shirsrhi
I
I
I
I
I
terrestrial
terrestrial
walking, burrowing
hopping
walking, burrowing
walking, burrowing
hopping
jumping
fast walking
burrowing
terrestrial
hopptng
Jumping
terrestrial
arboreal
jumping
burrowng
burrowing
terrestrial
fossorial
fossorial
fossorial
terrestrial
terrestrial
terrestrial