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J. Zool., Lond.

(2001) 253, 457±471 # 2001 The Zoological Society of London Printed in the United Kingdom

Patagial morphology of Draco volans (Reptilia: Agamidae) and


the origin of glissant locomotion in ¯ying dragons

Anthony P. Russell and Luke D. Dijkstra


Vertebrate Morphology Research Group, Department of Biological Sciences, University of Calgary, 2500 University Drive N.W., Calgary,
Alberta, T2N 1N4 Canada
(Accepted 20 March 2000)

Abstract
The integrative patagial morphology of Draco volans was examined to elucidate the possible evolutionary
pathway of origin of active patagia in the ¯ying dragons and in extinct taxa that are thought to have
possessed similarly constructed ¯ight membranes. The area of the patagia and accessory aerodynamic
surfaces is compared between Draco volans and Ptychozoon kuhli, a gekkonid with passive patagia.
Comparisons of patagial area are also made between selected species of Draco. Scale architecture of the
patagium of Draco is described and is related to pertinent aspects of the structure and properties of the
integument. The relationships of these characteristics to the morphology of the ribs and their related
musculature are emphasized. The overall assessment of these features in relation to patagial form is
employed to develop an evolutionary scenario for the origin of active patagia.

Key words: Draco, gliding, integument, morphology, evolution

INTRODUCTION are an integral part of the patagium as an integrated


structure.
The agamid lizard genus Draco (consisting of the Our reasons for doing so are two-fold. First, we were
so-called `¯ying dragons') exhibits an array of morpho- led to this study by our investigations of the functional
logical traits associated with gliding (Klingel, 1965; morphology of the patagia of the gekkonid genus
Colbert, 1967; Inger, 1983; Mori & Hikida, 1992, 1993; Ptychozoon (Russell, 1979; A. P. Russell & L. D.
Shine et al., 1998). The musculoskeletal anatomy of the Dijkstra, pers. obs.), in which air pressure is responsible
patagium was documented by Colbert (1967), demon- for unfurling the patagia after the lizard has jumped and
strating that the ¯ight membrane is extended by the is in `free fall' (Tweedie, 1950; Heyer & Pongsapipatana,
action of specialized iliocostalis and intercostal muscles, 1970; Medway, 1975; Brown, Ferner & Diesmos, 1997).
and associated ligaments, acting upon greatly elongated The patagia of Ptychozoon are thus `passive', in that the
ribs in the immediately post-sternal region of the trunk. musculoskeletal system is not involved in their support
Observation and documentation of ¯ight in members of or control. This contrasts with the `active' system seen
the genus Draco (Klingel, 1965; Inger, 1983; Musters, in Draco. Second, considerable attention has been given
1983; Mori & Hikida, 1993), and attributes of patagial recently to the putative ¯ight capabilities and ¯ight
scaling in relation to ¯ight capabilities and the apparatus of small fossil diapsid lizard-like taxa ± the
in¯uences of sexual dimorphism (Mori & Hikida, 1992; Late Triassic kuehneosaurs of Britain and North
Shine et al., 1998) have continued to be of focal America and the Late Permian coelurosauravids of
interest. Since the work of Colbert (1967), however, less Europe and Madagascar (Robinson, 1962; Colbert,
attention has been given to the morphology of the 1966, 1970; Carroll, 1975; Evans, 1982; Evans &
patagium itself. While the patagium is largely an integu- Haubold, 1987; Sues, Frey & Monk, 1997). Sues et al.
mentary structure, the nature of the skin that makes up (1997) re-evaluated the ¯ight apparatus of the late
most of the ¯ight membrane, and its relation to under- Permian lizard-like diapsid Coelurosauravus and pro-
lying tissues and structures remains undocumented. A posed a support structure for the patagium that was
full appreciation of the functional attributes of the Draco-like in possessing stiffened supporting rods, but
patagium cannot be attained until all of its major different in that these rods were advocated to be integu-
structural components have been considered in relation mentary derivatives (not ribs) articulating at a single
to each other. In this contribution we document hub in the axillary region. Such a proposed system,
features of the integument and connective tissues that while having attributes of both the Ptychozoon and
458 A. P. Russell and L. D. Dijkstra

Draco pattern, is indeed a hybrid between the two. We measurement endeavours to obtain a representation of
reasoned, therefore, that a fuller understanding of the actual area measured, rather than an approximation (as
anatomy and mechanics of operation of both passive obtained by Shine et al., 1998).
and active patagia, as exempli®ed by extant squamates, All mensural data were log10 transformed for scaling
may allow a more informed assessment of the putative analysis. The least-squares regression model is inap-
¯ight apparatus and function of the ®rst vertebrates to propriate for modelling scaling relationships (Gould,
have taken up aerial locomotion. 1966; Ricker, 1984; Jones, 1988; La Barbara, 1989), and
Russell (1979) proposed a hypothesis of the origin of so reduced major axis (RMA) regression statistics were
parachuting in gekkonids (using a passive patagial estimated for the relationships of each of body area
system). In this paper, the patagial structure in Draco (BA), patagium area (PA), accessory area (AA), and
(an active system) is examined and a hypothesis of how total body area (TBA) against SVL and weight, for both
glissant locomotion in this lineage may have arisen is D. volans and P. kuhli. Slope and intercept of each line
erected. These two models may assist in the interpreta- for each species was estimated as in Miller & Khan
tion of the structure and behaviour of fossil taxa for (1962) and Ricker (1984). Differences in slope between
which aerial locomotion has been advocated. pairs of lines were tested by Clarke's (1980) approxima-
The scaling relationships of patagial and other tion of the t-statistic. Pairwise differences in intercept
pertinent body areas to both snout±vent length (SVL) were tested by a Z-statistic as estimated by Miller &
and weight in Draco and Ptychozoon were examined to Khan (1962) and Jones (1988). For each set of 4 pair-
provide an initial assessment of the relative sizes of the wise comparisons (components and total area scaled
patagia in these two taxa. We then examined patterns of against SVL, and against weight) a stepwise Bonferroni
scale architecture and sensilla distribution across the adjustment (Rice, 1989) was used to determine acceptance
patagium in Draco, considered the internal anatomy of levels.
the patagium in relation to the erection and folding To examine patterns of area within the genus Draco,
mechanisms, and the shape of the patagium when erect. identical data to those described above were taken
Using this comprehensive overview, a scenario of how from the following species (number of specimens in
the active patagial system of squamates, as exempli®ed parentheses): D. haematopogon (10), D. maculatus (22),
by Draco, may have arisen and what constraints are D. maxima (10), D. melanopogon (15), D. quinquefas-
imposed upon it by virtue of its anatomical design and ciatus (16), and D. spilopterus (13). RMA regression
mode of functioning are presented. statistics for these taxa were compared with those
generated for D. volans. The sample sizes of all taxa
measured for area re¯ect the availability of museum
MATERIALS AND METHODS specimens in which the patagia could be extended and
accurately measured without irreparably damaging
For the primary comparison of appropriate areas them.
between Draco and Ptychozoon, SVL and weight (as Scalation patterns were observed for the entire sample
estimated by immersion in 70% ethanol and measuring of Draco mentioned above, plus additional museum
the ¯uid volumetrically displaced) were recorded for a specimens. For D. volans, the basic pattern of scale
series of Draco volans (n = 26) and Ptychozoon kuhli distribution was recorded by excising an intact patagium
(n = 15) selected from material borrowed from museum and associated region of the body wall, carefully dis-
collections: American Museum of Natural History, New secting apart the dorsal and ventral surfaces, mounting
York (AMNH); California Academy of Sciences, San each between glass microscope slides and examining
Francisco (CAS); Field Museum of Natural History, them under 70% ethanol. This treatment enabled the
Chicago (FMNH). For each of these specimens the upper and lower patagial surfaces to be rendered as
following were measured: body area (ventral surface of planes.
the head and torso, see icon in Figs 1a & 2a), patagium The relationship between dorsal and ventral scales
area (ventral surface of the extended patagia, see icon in and rib positions was determined by a combination of
Figs 1b & 2b), and accessory area (ventral surface of the manipulation of the patagia of preserved specimens,
gular ¯aps, tail crenelations, interdigital webbing, and observation of histological longitudinal sections stained
integumentary ¯aps along the limbs, see icon in Figs 1c with Milligan's trichrome (Humason, 1979), and
& 2c; Draco lacks interdigital webbing and accessory pinning specimens with their dorsal and ventral surfaces
surfaces on the limbs and tail). Total body area was uppermost onto a wax plate, with the patagium ex-
recorded as the sum of body area + patagial area + tended, and mapping scale patterns onto camera lucida-
accessory area (see icon in Figs 1d & 2d). Areas were based drawings with the rib positions marked. The
obtained by pinning each specimen to a sheet of trans- morphology of dorsal and ventral scales of the pata-
parent plastic, with patagia extended, and tracing gium, and the distribution of cutaneous sensilla, were
around the pertinent outlines with a permanent- documented using scanning electron microscopy (SEM).
marking pen. These tracings were then digitized using a Appropriate samples of integument were excised, dehy-
Wacom Digitizer 2 (model UD-1212R) digitizing drated through a series of increasing-strength ethanol
tablet and the data imported into an IBM-based PC baths, critical-point dried, sputter-coated with gold to a
using Sigma Scan1 (Jandel Scienti®c). This method of thickness of 20 nm in a Nanotech Semprep 2 sputter-
Patagial morphology of Draco volans 459

2.0 (a) 3.0 (b)

2.5

Log patagium area (cm 2)


1.5 2.0
Log body area (cm 2)

1.5
1.0
1.0

0.5
0.5

0.0

0.0 –0.5
1.0 1.5 2.0 2.5 1.0 1.5 2.0 2.5

2.0 (c) 3 (d)

1.5

Log total body area (cm 2)


Log accessory area (cm 2)

1.0
2

0.5

0.0
1
–0.5

–1.0

–1.5 0
1.0 1.5 2.0 2.5 1.0 1.5 2.0 2.5
Log SVL (mm)

Fig. 1. Log transformed reduced major axis regression plots of surface area components of Draco volans (~) and Ptychozoon
kuhli (&) measured against snout±vent length: (a) body area; (b) patagium area; (c) accessory area; (d) total body area. For
summary of comparative statistics see Tables 1 & 2.

coater, and viewed on a Hitachi S-450 SEM. Photo- sheet ®lm in a Hewlett-Packard Faxitron Series 43805N
graphs were taken using Polaroid Type 55 Positive/ X-ray system. Radiographic results were also of suf®-
Negative (P/N) ®lm. The extent of camber and overall cient resolution to reveal some degree of detail of
form of the patagia were assessed by extending the scalation of the periphery of the patagium. For clearing
patagia of living and preserved specimens and noting and staining, specimens were counter-stained with
the form of the patagial web in 3 dimensions. Alizarin Red S and Alcian Blue (Wassersug, 1976;
Internal anatomy of the patagium was examined in Dingerkus & Uhler, 1977) to reveal the presence and
various ways. Dissections were conducted to verify the distribution of bone and cartilage.
®ndings of Colbert (1967), and to make new observa-
tions. Both dissected patagia and those divided into
dorsal and ventral layers (see above) were bulk-stained RESULTS
for the presence of elastin and collagen using orcein
(Humason, 1979) and Verhoeff 's elastin stain with a Scaling of the ¯ight membranes
picro-ponceau counter stain for collagen (Humason,
1979). The orcein was used to corroborate the ®ndings Plotting body area against SVL for both D. volans and
for elastin from the Verhoeff 's test. The skeletal P. kuhli (Fig. 1a) reveals a very similar pattern, despite
structure of the patagium was investigated using radio- striking differences in overall body shape (Table 1). This
graphy, and clearing and staining. For radiography, indicates that comparisons of patagial area and acces-
specimens were pinned to a wax plate ventral side sory area can be conducted for these two taxa over a
uppermost with the patagium extended and placed into range of SVLs without body shape and area playing a
direct contact with Polaroid Type 55 P/N 465 inch confounding role. The plot of body area against weight
460 A. P. Russell and L. D. Dijkstra

2.0 (a) 2.0 (b)

1.5

Log patagium area (cm 2)


1.5
Log body area (cm 2)

1.0
1.0
0.5

0.5
0.0

0.0 –0.5
70.5
–0.6 0.0
0.0 0.5
0.5 1.0 1.5 2.0 70.5
–0.5 0.5
0.5 1.5
1.0 2.0

2.0 (c) 2.0 (d)

1.5
1.5

Log total body area (cm 2)


Log accessory area (cm 2)

1.0

1.0
0.5

0.0
0.5

–0.5
0.0
–1.0

–1.5 l l l l l
–0.5
–0.5
70.5 0.0
0.0 0.5
0.5 1.0
1.0 1.5
1.5 2.0
2.0 –0.5
70.5 0.0 0.5 1.0 1.5 2.0
Log weight
Log (gm)
weight (gm)

Fig. 2. Log transformed reduced major axis regression plots of surface area components of Draco volans (~) and Ptychozoon
kuhli (&) measured against weight: (a) body area; (b) patagium area; (c) accessory area; (d) total body area. For summary of
comparative statistics see Tables 1 & 2.

(Fig. 2a) indicates that D. volans has a greater body area & 2d), the lines for the two taxa are much more
per unit volume of mass, especially as individuals congruent. Although there are signi®cant differences
become heavier, but this difference is not signi®cant between D. volans and P. kuhli in both slope and
(Table 2). intercept (Table 2) in the relationship between total
Comparison of patagial area to SVL and mass indi- body area and SVL, largely owing to the difference in
cate that the patagia of D. volans are considerably larger accessory area between the two (Figs 1c & 2c), these
than those of P. kuhli of equivalent mass (Figs 1b & 2b), differences do not seem to comprise major discrepancies
but that there is no signi®cant difference in the slope or in total body area presented for the common SVL range
intercept of SVL plotted against patagial area. The (Fig. 1d). These combined results indicate that although
equivalent plot against weight reveals a signi®cant P. kuhli has a markedly smaller patagial contribution to
difference in intercept (Table 2). When accessory area is total body area, this is largely compensated for by the
considered (Figs 1c & 2c), the slope and intercept of the accessory membranes that provide this taxon with
relationship to SVL is signi®cantly different (Table 2), almost identical total body area vs. SVL and mass when
and the intercept of the plot against weight is also compared to D. volans. Conversely, D. volans achieves
signi®cantly different (Table 2). The positions of the its available aerodynamic body area much more
regression lines for D. volans and P. kuhli are reversed completely by way of the patagia alone.
when compared to the plots for patagial area. These Secondary comparisons reveal that for all species of
results indicate that the accessory structures contribute Draco examined for body area, patagial area and
more signi®cantly to total available aerodynamic area in accessory area scaling relationships across the entire
P. kuhli than they do in D. volans. SVL range, there are some signi®cant differences in
When body area, patagial area and accessory area are slope and/or intercept of patagial area and total body
summed to yield an estimate of total body area (Figs 1d area measured against SVL and weight (Fig. 3, Tables 3
Patagial morphology of Draco volans 461

Table 1. GMR statistics (slope, s d of slope and intercept) of extended and relaxed, but intervening scales, lying in
all lines used in comparisons of Draco volans and Ptychozoon ®elds of more extensible skin, undergo changes in the
kuhli (see Figs 1 & 2) orientation of their long axes and their relationships to
Slope sd Intercept each other as these movements occur.
The dorsal aspect of the patagium is not sharply
Draco volans demarcated from the dorsum of the body in terms of the
Body area±SVL 2.054 0.139 72.883 super®cial appearance of the scales. Those of the
Patagium area±SVL 2.571 0.197 73.615 dorsum are small and granular, and most of the dorsal
Accessory area±SVL 2.514 0.298 75.074
Total body area±SVL 2.324 0.157 72.946 surface of the patagium is clad in small scales, although
Body area±weight 0.831 0.122 0.289 closer inspection reveals both subtle differences from
Patagium area±weight 1.403 0.159 0.360 the dorsal scales, and zonal variation.
Accessory area±weight 1.007 0.154 71.185 The marginal scales of the patagium are substantive
Total body area±weight 0.943 0.139 0.640 and tightly imbricating, providing a ®rm edge to this
Ptychozoon kuhli structure (Figs 4 & 5a). Anteriorly the marginal scales
Body area±SVL 1.888 0.050 72.588 are quite robust, forming a band of lozenges with
Patagium area±SVL 2.285 0.094 73.607 medio-laterally oriented long axes that form the stout
Accessory area±SVL 1.908 0.098 72.468 leading edge of the patagium. These scales envelop the
Total body area±SVL 1.953 0.135 72.234
®rst patagial rib (Figs 4 & 7) and the stout muscle that
Body area±weight 0.567 0.107 0.391
Patagium area±weight 0.972 0.048 70.033 protracts it (see below). Dorsally, about six rows of such
Accessory area±weight 0.809 0.044 0.338 scales overlie the ®rst patagial rib (Fig. 4) and spill over
Total body area±weight 0.829 0.033 0.630 the front edge of the patagium onto its anteroventral
surface.
The leading edge of the patagium gradually curves,
& 4). However, all D. volans occupy a central position following the contour of the ®rst patagial rib (Fig. 7),
among the plots (Fig. 3). These results are very pre- and ultimately becomes the lateral margin of the un-
liminary, but they are suggestive of subtle differences furled patagium. Here the marginal scales continue to
between species of Draco in the overall design of the imbricate, but are smaller than those of the leading
patagial apparatus and its relationship to habits and edge. Their long axes are oriented antero-posteriorly, or
habitat. The results presented herein (Fig. 3, Tables 3 & further posteriorly, somewhat more obliquely laterally.
4) indicate that D. volans is a reasonable exemplar of the Along the lateral margin of the patagium these
aerodynamic apparatus of the genus and that, in terms bordering, imbricated scales transgress onto the lateral
of the generalities of design of the patagium, it can be border of the ventral surface, forming a stout rim to the
used as an appropriate representative example for patagial edge.
assessment against the passive apparatus of Ptychozoon. From about half of the length of the patagium from
its anterior border to its posterior terminus, its lateral
margin is no longer continuously underlain by the distal
Scale architecture of the patagium of D. volans ends of the ribs, and instead the marginal scales overlie
both de®nitive skeletal tissues and connective tissue
All of the following descriptions of scale distribution bridges that link the latter together along the patagial
and orientation are concordant with the patagium in its margin (Fig. 7) (see below).
extended position (Figs 4 & 6). In the relaxed state, as The lateral margin of the patagium curves back
displayed when skin samples are excised and prepared towards the body wall proper at the trailing edge of the
for SEM examination (Fig. 5) the scales compact to- patagium (Figs 4 & 7). Here the marginal scales are
gether. Robust bands of scales (see below) maintain a smaller still (Figs 4 & 5b), imbricated (but less tightly so
®xed relationship with the ribs as the patagium is than on the leading edge and lateral margins), and those

Table 2. Test statistics for differences in slope (T12) and intercept (Z) between GMR lines for Draco volans and Ptychozoon kuhli
used in this study (see Figs 1 & 2)

Slope Intercept

T12 d.f. P Z P

Body area±SVL 71.151 21.25 NS 1.343 NS


Patagium area±SVL 71.348 21.99 NS 0.025 NS
Accessory area±SVL 72.114 22.55 < 0.023 5.589 < 0.001
Total body area±SVL 72.428 21.51 < 0.012 2.302 < 0.011
Body area±weight 71.929 20.685 NS 0.423 NS
Patagium area±weight 70.442 23.505 NS 72.445 < 0.007
Accessory area±weight 71.347 23.623 NS 6.388 < 0.001
Total body area±weight 70.838 23.101 NS 70.046 NS
462 A. P. Russell and L. D. Dijkstra

2.0 (a) 2.0 (b)


q mx
q mx
1.5 1.5
s s

1.0 ma 1.0
h

ma
h
0.5 0.5 v me
2 2)
(cm
(cm )

Log total body area (cm2)


me
area
bpatagiumarea

0.0 0.0
1.2 1.4 1.6 1.8 2.0 2.2 1.2 1.4 1.6 1.8 2.0 2.2
Log patagium

Log SVL (mm) Log SVL (mm)

2.0 (c) 2.0 (d)


Log total

mx
q
q mx
1.5 1.5 s
ma

ma h
1.0 1.0
s
v
h
v me
0.5 0.5

me

0.0 0.0
–0.5 0.0 0.5 1.0 1.5 –0.5 0.0 0.5 1.0 1.5
Log weight (g) Log weight (g)
Fig. 3. Log transformed reduced major axis regression plots of surface area components of selected species of Draco in
comparison with Draco volans. Only regression lines are shown: (a) patagium area vs snout-vent length (SVL); (b) total body
area vs. SVL; (c) patagium area vs. weight; (d) total body area vs weight. For summary of comparative statistics see Tables 3 &
4. Regression lines for Draco volans are bold. Abbreviations for Draco species: h, haematopogon; ma, maculatus; me,
melanopogon; mx, maximus; q, quinquefasciatus; s, spilopterus; v, volans.

at the extreme trailing edge form erect triangles (Figs 5b ®elds of elongate, rhomboid scales that partially juxta-
& 7) that are vane-like. These latter scales support the pose but do not imbricate (Figs 4 & 5c). The long axes
trailing edge of the patagium and, in the region medial of these scales parallel the mean trend of the chains of
to the distal end of the last patagial rib (Fig. 7), are granules that immediately border them. As with the
neither underlain by skeletal tissue proper nor a granular scales, the rhomboidal scales reside within
connective tissue band (see below). ®elds of ¯exible scaleless integument.
The dorsal surface of the patagium proper, rather At the distal ends of the chains of granular scales
than the margin, is characterized by two alternating there is a change in morphology towards a more elon-
scale patterns. Chains of rounded scales radiate postero- gate shape overall and an increasing degree of
laterally across the patagial surface (Figs 4 & 5c) from a imbrication (Fig. 4). In such a way the chain-like rows
focal point in the axillary region. These granules overlie merge with the marginal scales.
the ®rst two patagial ribs, but posterior to this the paths The ventral aspect of the patagium is similarly, but
of the ribs and the chains of scales deviate from one less regularly, organized in comparison with the dorsal
another (Fig. 4) and the granules radiate across the surface. As mentioned above, the dorsal marginal scales
dorsal patagial surface. These scales furnish the dorsal encroach onto the ventral surface and form a raised rim
aspect of the patagium with the familiar ribbed pattern around the edge of the patagium. The distal ends of the
so evident on illustrations of Draco with the patagia ribs (both bony and cartilaginous regions) underlie this
extended (e.g. Zhao & Adler, 1993: frontispiece; Pough rim (Fig. 7) and bands of collagenous connective tissue
et al., 1998: Fig. 8.23). The granules in these rows that connect successive ribs at their lateral-most extre-
juxtapose one another or lie in slight isolation (Figs 4 & mities (see below). The marginal patagial scales on the
5c) and reside in ®elds of ¯exible, scaleless integument. ventral surface are rectangular or square in the lateral
In the spaces between these chains of granules are and posterior regions of the patagium (Fig. 6), and
Patagial morphology of Draco volans 463

Table 3. GMR statistics (slope, SD of slope and intercept) of


ams
all lines used in comparisons of Draco volans with other
selected Draco species (see Fig. 3)

(n) Slope sd Intercept

Draco haematopogon (10)


Patagium area±SVL 2.664 0.674 73.974
Total body area±SVL 2.168 0.385 72.792
Patagium area±weight 0.655 0.179 0.575
Total body area±weight 0.533 0.122 0.910
Draco maculatus (21) cgs
Patagium area±SVL 1.466 0.188 71.810
Total body area±SVL 1.323 0.156 71.246
Patagium area±weight 0.611 0.078 0.478 lms
ims
Total body area±weight 0.550 0.060 0.821
Draco maximus (10)
Patagium area±SVL 1.896 0.260 72.523
Total body area±SVL 1.909 0.251 72.258 rs
Patagium area±weight 1.366 0.382 70.066
Total body area±weight 1.376 0.384 0.214
Draco melanopogon (15)
Patagium area±SVL 2.829 0.471 74.146
Total body area±SVL 2.563 0.441 73.436
Patagium area±weight 1.310 0.136 0.312
tsgc
Total body area±weight 1.188 0.120 0.602 2
Draco quinquefasciatus (16)
Patagium area±SVL 2.497 0.217 73.428
Total body area±SVL 2.344 0.162 72.969 1
Patagium area±weight 0.949 0.121 0.612
Total body area±weight 0.891 0.101 0.823
Draco spilopterus (12)
Patagium area±SVL 2.064 0.272 72.752 pms
Total body area±SVL 1.879 0.155 72.199
Patagium area±weight 0.680 0.121 0.608 Fig. 4. Dorsal aspect of the patagium of Draco volans indi-
Total body area±weight 0.619 0.087 0.860 cating scale pattern distribution. Dashed lines, position of the
Draco volans (30) patagial ribs. Abbreviations: ams, anterior marginal scales;
Patagium area±SVL 2.465 0.151 73.432
Total body area±SVL 2.273 0.116 72.859 cgs, chains of granular scales; lms, lateral marginal scales;
Patagium area±weight 1.189 0.165 0.223 pms, posterior marginal scales; rs, rhomboidal scales; tsgc,
Total body area±weight 1.097 0.146 0.510 terminal scales of granular chains. Scale bars: for scale en-
largements = 1 mm; for entire patagium (superimposed upon
patagium) = 2 mm.
many bear a posterior pit that houses a mechano-
receptor.
The ventral surface of the patagium proper, like the imbricating keeled scales of the former to the small
dorsal surface, is clad in a mixture of chains of granular juxtaposed granules (Fig. 6), that in turn give way to the
scales and intervening patches of rhomboid scales more elongated, rhomboid scales of the major portion
(Fig. 6). Unlike the dorsal surface of the patagium, of the ventral patagial surface. The ventral patagial
however, the chain-like aggregations of granules are scales are generally more diaphanous and less robust
restricted to the anterior extremity and lateral one-third than those of the dorsal surface.
of the patagium (Fig. 6), where they in®ltrate from the The mechanoreceptors of the patagium of D. volans
lateral margin and fade towards the centre of the bear an unbranched spike (Fig. 5e), the papilla being
patagial web. The granular scales of the ventral surface c. 40 mm in diameter, and the spike c. 30 mm long. Only
are generally more closely juxtaposed than those of the the rows of robust, chain-like scales and the scales of the
dorsal surface (Fig. 5d), are heavily microsculptured, and perimeter bear mechanoreceptors, and most are located
may bear mechanoreceptors that are recessed in pits. on the ventral and ventrolateral surfaces. When the
The rhomboidal scales that lie between these rays of patagium is folded, the scales bearing the sensilla rest at
granules laterally (Figs 5d & 6), also occupy most of the the apices of the accordion-like integumentary folds or
ventral patagial surface. Their long axes are oriented in remain in the same orientation on the uncollapsed
parallel with the mean trend of the rays in the lateral margin. The scale microarchitecture of the ventral
part of the patagium (Fig. 6), and continue this general surface is honeycombed, a pattern typical of agamids
orientation when traced further medially. (Peterson, 1984).
The transition from the ventral body wall proper to
the patagium is marked by a transition from the
464 A. P. Russell and L. D. Dijkstra

Table 4. Pairwise test statistics for differences in slope (T12) and intercept (Z) between GMR lines of selected Draco species
against D. volans. Signi®cance levels for pairwise comparisons determined by stepwise Bonferroni adjustment of a = 0.05; *
signi®cant difference (see Fig. 3)

Slope Intercept

T12 d.f. P Z P

Draco haematopogon
Patagium area±SVL 0.298 11.040 0.614 70.426 0.665
Total body area±SVL 70.255 10.287 0.402 0.091 0.464
Patagium area±weight 71.935 12.956 0.038 2.300 0.011*
Total body area±weight 72.715 13.000 0.009* 3.259 < 0.001*
Draco maculatus
Patagium area±SVL 73.655 22.503 0.001 3.715 < 0.001*
Total body area±SVL 74.198 21.618 < 0.001* 4.590 < 0.001*
Patagium area±weight 73.517 27.887 0.001* 2.048 0.020
Total body area±weight 73.944 27.919 < 0.001* 2.873 0.002
Draco maximus
Patagium area±SVL 71.747 11.135 0.054 1.556 0.060
Total body area±SVL 71.241 10.608 0.121 1.115 0.132
Patagium area±weight 0.443 12.971 0.668 70.759 0.776
Total body area±weight 0.732 12.834 0.761 70.781 0.783
Draco melanopogon
Patagium area±SVL 0.777 15.468 0.775 70.806 0.790
Total body area±SVL 0.671 14.950 0.744 70.708 0.760
Patagium area±weight 0.559 24.927 0.709 0.675 0.250
Total body area±weight 0.477 24.705 0.681 0.792 0.214
Draco quinquefasciatus
Patagium area±SVL 0.120 19.477 0.547 0.008 0.497
Total body area±SVL 0.360 19.836 0.639 70.296 0.616
Patagium area±weight 71.192 23.691 0.123 2.699 0.003*
Total body area±weight 71.186 24.453 0.123 2.315 0.006
Draco spilopterus
Patagium area±SVL 71.227 14.067 0.120 1.188 0.117
Total body area±SVL 71.968 15.497 0.034 1.860 0.031
Patagium area±weight 72.450 17.745 0.012 2.726 0.003*
Total body area±weight 72.952 18.571 0.004* 2.976 0.001

Internal anatomy of the patagium of D. volans These features of the erection mechanism and the
associated ribs are summarized in Fig. 8.
Specimens of D. volans were dissected to corroborate Colbert (1967) was much less de®nitive about rib
the basic details of the musculoskeletal anatomy of the anatomy, and diagrammed only the osseous portions of
patagium (Colbert, 1967: ®gs 2 & 3). Details of the these elements, treating them all as being essentially
iliocostalis and intercostal muscles and their relation- uniform in spacing and form (Colbert, 1967: ®g. 2).
ships to the patagial ribs accorded well with Colbert's Closer inspection (Fig. 7) reveals that the ®rst patagial
(1967) ®ndings. The former is a thin sheet of dorsal rib is the most robust in terms of mid-shaft diameter.
musculature that extends downward onto the ¯ank, This rib (Fig. 7) curves smoothly at its distal end and
from its serial origin deep to the longissimus dorsi, to overlaps the osseous portion of the second patagial rib
attach laterally to the ribs (Romer & Parsons, 1977: for a considerable distance (Fig. 9). In the region of
®g. 201). The anterior-most part of this muscle in Draco close approximation of the ®rst and second patagial
is enlarged, extends anteriorly deep to the trapezius, ribs, the ossi®ed portion of the ®rst gives way to a distal
longissimus dorsi and scapula and is drawn out along costal cartilage (Fig. 7) that broadens slightly and runs
the anterior border of the ®rst rib (Colbert, 1967). The towards the second rib, where it tapers towards its
ligaments running obliquely between successive pairs of terminus. At their point of juxtaposition, a collagenous
ribs (Colbert, 1967: ®gs 2 & 3) were also identi®ed, and band runs from the distal tip of the costal cartilage of
were also demonstrated by using the bulk staining the ®rst patagial rib to attach to the lateral aspect of the
technique for collagen mentioned above. Protraction of osseous portion of the second patagial rib (Fig. 7).
the patagium is achieved by powerful contraction of the The shaft of the second patagial rib does not deviate
large iliocostalis muscle pulling on the ®rst patagial rib, greatly from that of the ®rst, and the enclosed space
with branches of the intercostal system and the ligamen- between the two is quite small (Fig. 8). The posterior
tous bands running between adjacent ribs assisting in curvature of the distal end of the second patagial rib is
the protraction of the more posterior patagial ribs. much more dramatic than that of the ®rst (Fig. 7), and
Patagial morphology of Draco volans 465

Fig. 5. Scanning electron micrographs of patagial scales of Draco volans: (a) anterior marginal scales; (b) posterior marginal
scales; (c) a portion of the dorsal patagial integument showing parts of two chains of granular scales with an intervening region
of rhomboidal scales; (d) a portion of ventral patagial integument showing rhomboidal and granular scales; (e) an enlargement
of a series of ventral granular scales depicting the honeycombed surface sculpturing and sensilla recessed in pits on the free
margins of the scales. Abbreviations as in Fig. 4. Sensilla are indicated with arrowheads. Scale bars: a±d = 500 mm: e = 50 mm.

its osseous distal portion supports a large portion of the cartilage of the third rib broadens and is connected to
lateral aspect of the patagium. As with the ®rst patagial the osseous portion of the fourth patagial rib by a quite
rib, the second terminates in a slightly ¯ared costal extensive collagenous band (Fig. 7).
cartilage, which, in turn, is connected to the osseous The fourth patagial rib (Fig. 7) is oriented postero-
part of the third rib by way of a prominent band of laterally and, unlike the preceding three ribs (but similar
collagenous tissue. to the following two), the shaft is bowed posteriorly.
The third patagial rib (Fig. 7) bows quite considerably Towards its distal end it forms two bends that turn the
posteriorly in its medial portion and then courses rib backwards and then align it with the periphery of the
posterolaterally across the patagium. Close to the patagium (Fig. 7). Connection to the osseous portion of
lateral extremity of the patagium, the third patagial rib the ®fth rib is by a costal cartilage and a collagenous
begins to curve posteriorly quite gently and then, at the band. The gap between ribs three and four is quite
periphery, makes an abrupt posterior turn. The space substantial.
between the second and third ribs is much larger than The ®fth patagial rib angles steeply posteriorly
that between the ®rst and second. The distal costal (Fig. 7) and turns sharply backwards at its distal tip,
466 A. P. Russell and L. D. Dijkstra

ams

Ims

mp

rs

cgs

bws
mp pms
1
Fig. 6. Diagrammatic representation of the ventral aspect of
the patagium of Draco volans indicating scale pattern distribu-
tion. Dashed lines, position of the patagial ribs. Lateral
marginal scales (lms) form a distinct rim around the edge of
the patagium. Abbreviations as in Fig. 4 except: bws, body Fig. 7. Radiograph of the right patagium of Draco volans
wall scales; mp, mechanoreceptor pits. Scale bars: for enlarged (CAS 28033) in ventral view, pinned in the extended position.
scale outlines = 1 mm (all except the body wall scales are The dashed lines X±X, Y±Y and Z±Z represent the planes of
associated with the scale bar on the right); for entire patagium sectioning and the extent of the patagium sectioned in Fig. 9a,
(superimposed upon patagium) = 2 mm. b and c, respectively. Abbreviations: cb, spans of collagenous
bands connecting costal cartilage to the following osseous rib;
cc, costal cartilages; mil, m. iliocostalis; pams, position of
although the angles for this turn are not nearly as sharp
as those of the fourth. Connection to the distal, osseous anterior marginal scales; plms, position of lateral marginal
portion of the sixth rib is again by a costal cartilage and scales; ppms, position of posterior marginal scales; r1-r6,
a collagenous band. The distal space between ribs four patagial ribs 1±6. Scale bar = 2 mm.
and ®ve is very broad.
The sixth patagial rib is bowed sharply posteriorly at binding adjacent ribs together creates the robust and
mid-shaft (Fig. 7) and gently curved distally. It bears at substantive free lateral margin of the patagium. The
its distal end a quite elongate costal cartilage, but this is stout ®rst patagial rib provides the skeletal support for
not continued by a collagenous band. The space the leading edge of the patagium. The perimeter of the
between the ®fth and sixth ribs is quite narrow, and the patagium remains essentially smooth at all stages from
area of patagium posterior to the sixth rib is quite broad fully retracted to fully extended (save for that part
(Fig. 7). posterior to the last patagial rib), this being made
When the distal ends of the patagial ribs are dissected possible by the continuous, stiffened free edge.
free of the patagium and the collagenous connecting Bulk staining of the dissected patagium with stains
strands of tissue are broken, the ribs spring forward and speci®c for elastin (see above) reveal three major elastin
the costal cartilages recoil and curl upon themselves. tracts within the integument (Fig. 8). These are curved
This indicates that the margin of the patagium is under and follow the arc of the perimeter of the patagium. A
a signi®cant amount of pre-tension, mediated by the narrow band is situated along the perimeter of the
collagenous bands, and the relationships of the distal patagium (Fig. 8), a broad band is located about two-
ends of the ribs are maintained by these connections. thirds along the length of the osseous ribs from their
The combination of recurved distal ends of the patagial origin, and a third is placed at about one-third of the
ribs, the costal cartilages, and the collagenous strips length along the anterior two ribs, close to the axilla.
Patagial morphology of Draco volans 467

el
mil r1
mint
r2
r3

lig
r4

cc cb
r5

r6

Fig. 8. Musculoskeletal and elastin components of the pata-


gium of Draco volans (partly after Colbert, 1967). Abbrevia-
tions as in Fig. 7 except: el, bands of elastin; lig, ligaments
binding adjacent ribs; mint, m. intercostales.

Relationships of component parts of the patagium


are also evident in histological section (Fig. 9). In
oblique longitudinal section (orientation, see Fig. 7;
sections, see Fig. 9) the relationships of the ®rst three
ribs to the integument and associated structures are
illustrated. The dorsal and ventral aspects of the integu-
ment clearly reveal the differences in scale shape
between the chains of granular scales and the rhom-
boidal scales (Fig. 9). The dermal layers of the scales of
the dorsum of the patagium (both granular and rhom-
boidal) are thicker than those of the ventral surface
(Fig. 9), con®rming the observation from external
appearance that the dorsal scales are more robust. The
chains of granular scales lie above and below the ribs
and at the apices of the concertina-like folds of the Fig. 9. Histological cross sections of the anterolateral region
patagium, and the rhomboidal scales lie within the folds of the patagium of Draco volans. The planes of sectioning of
and in the areas between the ribs (Fig. 9). panels a, b and c are depicted by the dashed lines X±X, Y±Y
At the leading edge of the patagium the enlarged and Z±Z on Fig. 7, respectively. Dorsal, top; anterior, left.
anterior marginal scales are evident (Fig. 9a), forming a Abbreviations as in Figs 4, 7 & 8, except: mint 2,3, m.
robust leading edge to the aerofoil in advance of the ®rst interostalis 2,3; r1cc, costal cartilage of ®rst rib. Scale
two ribs and their associated musculature. The sections bar = 500 mm.
illustrated (Fig. 9) become increasingly oblique with
respect to the patagial outline (Fig. 7, lines X±X; Y±Y
and Z±Z), and diminution in the size of the fringing evident in the ®rst rib (Fig. 9a, b) as the plane of
scales is evident (Fig. 9a±c) as they trend from anterior sectioning changes (see Fig. 7). The proximal-most part
to lateral marginal scales. of the costal cartilage of the ®rst rib (Fig. 9b) is
Within the con®nes of the patagium, portions of the considerably greater in diameter than the distal-most
®rst three patagial ribs are evident in cross-section part of the osseous portion (Fig. 9a), but tapers con-
(Fig. 9). The ®rst section illustrated (Fig. 9a) is cut at a siderably in its distal-most region (Fig. 9c), at which
point at which the osseous part of the ®rst rib has point it comes to lie ventral to the second rib in the area
tapered markedly at its distal extremity. The cross of overlap of these two skeletal elements (Fig. 7). The
sections of the second and third ribs are much greater in connective tissue membranes binding the distal portions
girth at this point, and the plane of sectioning is such of the ®rst and second ribs together are especially
that the intercostal muscle (Fig. 9a±c) associated with evident in the costal cartilage region (Fig. 9b, c), indi-
the second and third ribs is still very evident, whereas the cating the physical union of the ribs at the periphery of
point of sectioning of the ®rst rib lies distal to the distal- the patagium. This is ultimately continued by stout
most point of attachment of the iliocostalis muscle. connective tissue bands, but these are more evident
A transition from osseous rib to costal cartilage is between the distal ends of the second and third, third
468 A. P. Russell and L. D. Dijkstra

and fourth, and so on, pairs of patagial ribs (Fig. 7), aerial capabilities of Draco (e.g. Hairston, 1957; Herre,
where there is no region of overlap of the distal ends of 1958; Klingel, 1965) attest to its manoeuvrability,
the ribs (Fig. 7). agility, ¯ight-path accuracy and ability to stay aloft for
Also evident within the patagium are bands of extended periods. The geckos are probably less pro®-
connective tissue that are elastin-rich (Fig. 9a±c), cient, but are none the less very effective in aerial
associated with the folding mechanism (Fig. 8). In the locomotion (Honda & Hikida, 1997).
regions of the patagium between successive ribs, little in Examination of total additional surface area available
the way of organized tissue intervenes between the for enhancing aerial locomotion reveals that Draco and
upper and lower layers of integument (Fig. 9). Some Ptychozoon are not signi®cantly different (Figs 1 & 2,
blood vessels and some strands of dense connective Table 2). The proportional area that is contributed by
tissue are evident, but in the planes of sectioning the patagium proper, however, is much larger in Draco
illustrated here the patagial structure is seen to be little (Figs 1 & 2, Table 2), than in Ptychozoon, with the latter
more than an integumentary fold with supporting ribs compensating by the addition of extensive accessory
and their associated musculature. ¯aps and folds. Thus, while overall area is not markedly
different, its distribution and the ways in which it is
deployed are. The active patagium of Draco uses a
Patagial form unique combination of integumentary, muscular and
connective tissue modi®cations that allow it to be
When folded, the ribs in the patagium approximate each erected, controlled in ¯ight, and furled against the body
other to some extent, but the basal portions change once the ¯ight (or intraspeci®c signalling bout ± see
their relative relationships very little. When pulled into below) is over.
the protracted erect position, the margin of the pata- Russell (1979; Fig. 6) developed a scenario by which
gium is displaced laterally as the ribs rotate but the aerial locomotion may have come about in geckos such
margin remains curved. The distal ends of the osseous as Cosymbotus and Ptychozoon. This was predicated
ribs and their costal cartilage continuations undergo upon pre-existing habitat±behaviour and structure±
posterior bending. The collagen bands connecting the function couplets that resulted in a lateral body fold
rib ends are pulled taut and the elastin bands within the that was used for fat storage being combined with a
patagium are placed under tension and are stretched. At behavioural trait of jumping to avoid predators. It was
the leading edge of the patagium a substantial fold in hypothesized that these two components fell under the
the post-axillary region becomes stretched (this fold in¯uence of a new selective regime when the enlarged
contains the enlarged iliocostalis muscle) and forms the fold was suf®ciently enhanced to result in the retarda-
broad leading edge of the patagium close to the body. A tion of the rate of descent during the predation-avoiding
pocket is thus created on the ventral surface of the jumps. A. P. Russell & L. D. Dijkstra (pers. comm.)
patagium just posterior to this fold, and both a medio- have noted the morphological attributes of such passive
lateral and an antero-posterior camber of the patagium patagia that make them (and their accessory structures)
are set up as a result of these unfurling activities. The effective in parachuting and gliding.
anterior leading edge tapers from medial to lateral and Comparing the gekkonid system to that found in
thins to the `normal' thickness of the patagial margin by Draco reveals some noteworthy differences. The pata-
the point at which the patagial margin begins to turn gium of Draco is the active type, being supported by
posteriorly. The marginal scales of the patagium and outgrowths of the somatic skeleton that are under
their underlying rib ends and the collagenous bands muscular control. This type of patagium is able to be
form a prominent rim to the patagium. erected and folded at will, and its con®guration can be
As the patagium is extended and achieves its cam- adjusted in ¯ight, giving a much more controllable
bered form, the regions of rhomboidal scales (Figs 5c, d combination of aerodynamic surfaces. This indicates
& 9) become extended, and their folds become dimin- that such a patagium is unfolded, rather than being
ished. The pleats between the rows of granular scales erected as in Ptychozoon and Cosymbotus. For this
open up on both dorsal and ventral surfaces and result con®guration to function, there are modi®cations of the
in a relatively smooth patagial surface. musculature and skeleton that provide the lever me-
chanics necessary for active unfolding of the ¯ight
membranes. The relationship of the integument to the
DISCUSSION underlying musculoskeletal modi®cations provides con-
touring and shaping to the patagium. Using highly
Among modern lizards, the gekkonid genera Ptycho- variable scale morphology, the patagium can be com-
zoon and Cosymbotus and the agamid genus Draco pactly and controllably folded, and effectively stretched
possess morphological adaptations that enable them to to provide a continuous and cambered aerodynamic
parachute and glide with a considerable degree of surface. Bands of elastin, together with the inherent
pro®ciency. These taxa inhabit the primary tropical rain elasticity of the integument overall and the elastic
forests of the Old World and make effective use of the properties of the distal ends of the ribs, provide a
spacing patterns between the trees of these forests in mechanism for largely passive and accurate folding of
executing their ¯ight paths. Detailed accounts of the the ¯ight membranes. Scale architecture and underlying
Patagial morphology of Draco volans 469

Representative
genus Structure Function Habitat Behaviour

Uromastyx Depressed Thermo- Terrestrial Body


body regulation, inflation,
predator posturing
deterrence

Leiolepis Lateral Thermo- Terrestrial Body


expansion, regulation, inflation,
elongate ribs predator posturing
deterrence and erection
and of ribs
intraspecific
communication

Draco Further Intra- Arboreal Erection of


elongation of specific ribs,
ribs, patagium communication leaping,
and gliding foraging

Fig. 10. Integration of factors postulated to be important in the evolution of the patagia in Draco, using three genera (discussed
in the text) to exemplify the hypothetical stages. Horizontal arrows, feedback systems in the selection process. When the rib-
supported body folds become operative in retarding descent and controlling the ¯ight path (Draco stage) the `structure±function'
and `habitat±behaviour' sets interrelate in a new way, enhancing the new adaptive role of the new functional unit.

collagenous networks provide governance to the system (1997) drew a comparison between the late Permian
and create regional differences that are appropriate for Coelurosauravus and the gekkonid Ptychozoon when
enhancing effective air ¯ow and pressure differentials discussing parachuting/gliding capabilities, even though
that result in the generation of lift and the ability to Coelurosauravus possessed skeletal supports in its
steer with some precision. Subtle differences in the putative patagium and thus might be likened more
morphology of individual patagial ribs contribute to the effectively to taxa possessing active patagia. It is prob-
effectiveness of the geometry of the entire patagium. In able that those forms with patagia supported by
both Draco and Ptychozoon, the upper integument of elongated ribs (or other skeletal devices that require
the patagium is considerably thicker than the lower, erecting and unfolding) did not develop them via the
chie¯y owing to a differential thickness of the dermis. pathway leading to the elaboration of passive patagia as
This arrangement assists in maintaining the form of the outlined by Russell (1979). Instead, a consideration of
patagial skin and resisting ballooning between the ribs the form and function of the patagium of Draco leads to
in Draco and eversion of the patagium in Ptychozoon. the development of an alternate scenario, the details of
In this paper we have indicated how the various which are outlined in Fig. 10.
components of the patagium of Draco interact to In this theoretical model we propose that the pata-
produce aerodynamic surfaces that offer a considerable gium of Draco, as an aerodynamic structure, was
degree of control. As such they differ markedly in exapted (Gould & Vrba, 1982) from prior modi®cations
structural detail from the passive patagia of gekkonids. associated with thermoregulation, intraspeci®c commu-
While both types of patagia have resulted in these nication and predator escape. The scenario employs
groups of lizards using the aerial medium with consider- three representative genera, Uromastyx, Leiolepis and
able effectiveness, differences in the detail of design Draco, not in a phylogenetic sense, but in the context of
suggest different pathways of origin (behaviourally as a morphotypic series (Russell, 1976). The initial
well as phylogenetically). structure±function couplet in this instance associates a
This is of some signi®cance not only to the under- depressed body form with enhanced thermoregulatory
standing of the basic biology of the two taxonomic abilities and potential predator avoidance, working
groups from which these exemplars come, but also in through a habitat±behaviour couplet of a terrestrial
the consideration of the occupancy of the parachuting/ existence associated with body in¯ation and posturing.
gliding niche by lizard-like taxa of the past. Sues et al. Such a situation is evident in Uromastyx, and the
470 A. P. Russell and L. D. Dijkstra

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