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Sexual Dimorphism and Life History of Keichousaurus hui (Reptilia:

Sauropterygia)

Article  in  Journal of Vertebrate Paleontology · June 2009

DOI: 10.1671/039.029.0230

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Journal of Vertebrate Paleontology 29(2):401–408, June 2009
# 2009 by the Society of Vertebrate Paleontology

ARTICLE

SEXUAL DIMORPHISM AND LIFE HISTORY OF KEICHOUSAURUS HUI

(REPTILIA: SAUROPTERYGIA)

YEN-NIEN CHENG,1 ROBERT HOLMES,*,2,{ XIAO-CHUN WU,2 and NOEL ALFONSO2

1
National Museum of Natural Sciences, 1 Kuan Chien Road, Taichung 404, Taiwan, China;
National Cheng Kung University, No. 1 University Road, Tainan 701, Taiwan, RO China;
2
Canadian Museum of Nature, P.O. Box 3443, STN “D”, Ottawa, Ontario, K1P 6P4, Canada, holmes1@ualberta.ca

ABSTRACT—A large collection of recently prepared, complete specimens of Keichousaurus hui provides a wealth of
new anatomical data for this taxon. Sexual dimorphism can be unambiguously quantified by proportions of the humerus
as well as ratios of humerus length to standard length and femoral length. Multivariate (principal components and
discriminant) analysis identified ratios most useful in distinguishing the sexes. Sexual maturity was reached in males
at approximately 126 mm snout-vent length (SVL), and in females by 122 mm SVL. Mean SVL for mature males is
approximately 161 SVL, and for mature females, at most 149 mm SVL. Although the last dimension predicts a mean
hatchling SVL of approximately 50 mm based on data from extant squamates, the relationship between mean SVL of
mature females and mean SVL of hatchling/neonate in squamates is quite variable. As a result, a mean value of 40.4 mm
SVL for several tiny isolated individuals of Keichousaurus is well within the 95 percent confidence ellipse calculated from
data from extant squamates. Therefore, there is not reason to postulate that the common occurrence of tiny individuals of
between 33.5 mm and 48.2 mm SVL is the result of spontaneous abortions.

INTRODUCTION range in size from 2.6 mm standard length (defined as the com-
bined length of the four most posterior trunk vertebrae—see
The sauropterygian Keichousaurus hui was first described by
Sander, 1989) to 19.2 mm standard length. Based on humerus
Young (1958) using data from partly prepared specimens from the
morphology, it was estimated that the onset of sexual maturity in
Middle Triassic deposits of Guizhou Province, China. Additional
sex ‘y’ (males) occurred at some point between a standard length
specimens subsequently collected from the same area have since
of 11 mm and 13 mm, or a snout-vent length (SVL) of between
provided the basis for a more comprehensive description (Lin and
124.9 mm and 154.7 mm (Lin and Rieppel, 1998:table 1).
Rieppel, 1998), but some points remained unresolved, including
A case for viviparous habits has been made for Keichousaurus
some aspects of sexual dimorphism and the significance of the nu-
(Cheng et al., 2004). Two gravid (pregnant) individuals are
merous juvenile individuals found at the locality and nearby areas.
known. In neither case does the arrangement of the young indi-
Over the past several years, the National Museum of Natural
viduals in the abdominal cavity suggest that they represent a last
Science (NMNS), Taiwan RO China, has assembled a large col-
meal. Rather, their skeletons are at least semi-articulated, show
lection of Keichousaurus specimens. So far, more than seventy
no signs of digestion, and are located posterior to the expected
specimens have been carefully prepared and examined. The data
location of the stomach. They are arranged bilaterally, in one
derived from them contributes to the resolution of these out-
case (NMNS–cyn 2002–1), two on the left, and two on the right,
standing questions.
in the other specimen (NMNS–VL–191), three on the left, and at
As in the pachypleurosaurs Serpianosaurus (Rieppel, 1989)
least two on the right, indicating the presence of paired oviducts
and Neusticosaurus (Sander, 1989), Keichousaurus clearly exhi-
(Cheng et al., 2004). None is coiled in a manner expected if it had
bits sexual dimorphism (Lin and Rieppel, 1998). In all taxa, one
been contained within an egg (e.g., Sander, 1989; Ji et al., 2006).
of the morphs, initially designated sex ‘y’, can be distinguished
In both females, at least one of the young is positioned at or near
from the alternate morph (sex ‘x’) by the possession of a rela-
the vent, suggesting that birth was imminent. Although pressure
tively larger and more robust humerus. The recent discovery of
from gases formed during decomposition may have forced the
embryos in the body cavity of two individuals of sex ‘x’ (Cheng
embryo toward the birth canal, the relatively advanced state of
et al., 2004) has permitted the identification of the two sexes in
ossification of all of the young, at least in the larger of the two
Keichousaurus. All three taxa are represented by large numbers
females, indicates that they were close to full term.
of specimens ranging in size from tiny individuals (in the case of
Neusticosaurus, possibly embryonic) to large, mature adults. All
sub-adult specimens resemble females (sex ‘x’) closely in propor- MATERIALS AND METHODS
tions (Lin and Rieppel, 1998), and therefore cannot be sexed Seventy essentially complete skeletons were examined under
with any confidence. In the small collection of Keichousaurus dissecting microscope and 17 separate measurements (Fig. 1 and
(13 specimens) available to Lin and Rieppel (1998), individuals Table 1) were taken from each specimen using the criteria of
Sander (1989:568-569 and fig. 2) by one of the authors (Y-n. C.)
using an ocular mounted micrometer. Lengths of vertebrae of
neonates and embryos (Table 2) were obtained in the same man-
*
Corresponding author. ner. A principal components analysis (PCA) was done on a corre-
{
Current address: Department of Biological Sciences, Z 1012 lation matrix of log-transformed, standardized size-free variates.
Biological Sciences Building, University of Alberta, Edmonton, Alberta This approach allows for a priori discovery of multiple groups
T6G 2E9, Canada. (Humphries et al., 1981). Size effects in the data were minimized

401
402 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009
FIGURE 1. Keichousaurus hui, measurements recorded in Table 1. 1, skull, total length; 2, length of neck; 3, length of trunk; 4, length of tail;
5, snout-vent length; 6, standard length; 7, length of humerus; 8, length of femur; 9, length of radius; 10, length of ulna; 11, length of tibia; 12, length of
fibula; 13, total length; 14, maximum distal width of humerus; 15, minimum width of humeral shaft; 16, maximum distal width of femur; 17, minimum
width of femoral shaft.
using residuals from the pooled groups regression of logged (base
10) mensural character and logged total length. As these residuals
are orthogonal to the regression line, they reflect the shape of the
body part independent of size. Discriminant function analysis
(DFA) was used to classify individuals to a given sex and to
identify characters that contributed most to group differentiation.
Ratios of measurements against total length were calculated and
plotted against each other for diagnostic purposes.
Specimens Examined—NMNS-chw-01, NMNS-chw-02, NMNS-
chw-03, NMNS-chw-04, NMNS-cyn 2002-01, NMNS-cyn 2002-02,
NMNS-cyn 2002-03, NMNS-cyn 2002-04, NMNS-cyn 2002-05,
NMNS-cyn 2002-06, NMNS-cyn 2002-07, NMNS-cyn 2002-08,
NMNS-cyn 2002-10, NMNS-cyn 2002-11, NMNS-cyn 2002-12,
NMNS-cyn 2002-13, NMNS-cyn 2002-14, NMNS-cyn 2003-15,
NMNS-cyn 2003-16, NMNS-cyn 2003-17, NMNS-cyn 2003-18,
NMNS-cyn 2003-19, NMNS-cyn 2003-20, NMNS-cyn 2003-21,
NMNS-cyn 2003-22, NMNS-cyn 2003-23, NMNS-cyn 2003-24,
NMNS-cyn 2003-25, NMNS-cyn 2003-26, NMNS-cyn 2003-27,
NMNS-cyn 2005-01, NMNS-cyn 2005-02, NMNS-cyn 2005-03,
NMNS-cyn 2005-04, NMNS-cyn 2005-05, NMNS-cyn 2005-06,
NMNS-cyn 2005-07, NMNS-cyn 2005-08, NMNS-cyn 2005-09,
NMNS-cyn 2005-10, NMNS-cyn 2005-11, NMNS-cyn 2005-12,
NMNS-cyn 2005-13, NMNS-cyn 2005-14, NMNS-cyn 2005-15,
NMNS-cyn 2005-16, NMNS-cyn 005-17, NMNS-cyn 2005-18,
NMNS-cyn 2005-19, NMNS-cyn 005-20, NMNS-cyn 2005-21,
NMNS-cyn 2005-22, NMNS-cyn 2005-23, NMNS-cyn 2005-24,
NMNS-cyn 2005-25, NMNS-cyn 2005-26, NMNS-cyn 2005-27,
NMNS-cyn 2005-28, NMNS-cyn 2005-29, NMNS-cyn 2005-30,
NMNS-cyn 2005-31, NMNS-cyn 2005-32, NMNS-kiko 2004-01,
NMNS-kiko 2004-03, NMNS-kiko 2005-X, NMNS-kiko 2005-XX,
NMNS-kiko 2005-Y, NMNS-kiko 2005-YY, NMNS000933-
F0034394, NMNS-VL191.
RESULTS
Sexual Dimorphism
Examination of the large collection of Keichousaurus avail-
able to us indicates that the larger, more robust humerus of the
male is quantified most conspicuously by three ratios: (1) maxi-
mum distal width of the humerus (14)/minimum width of the
humeral shaft (15); (2) maximum length of humerus (7)/standard
length (6); and (3) maximum length of humerus (7)/maximum
length of femur (8). Each of these ratios shows a bimodal distri-
bution (Fig. 2). By analogy with similar qualitative analyses of
sexual dimorphism of other pachypleurosaur taxa performed by
Rieppel (1989) and Sander (1989), and using the sexual identifi-
cation criteria of Cheng et al. (2004), of the 70 essentially com-
plete individuals available to us, ratios (1) and (2) identify 22
males, and ratio (3), 24 males. The remaining individuals are, by
inference, females and/or immature. Sixteen individuals
(Table 3) are common to all three lists, and five appear on two
of the three lists. Of the10 specimens that appear on only one of
the three lists, five are small (with a snout-vent length, hereafter
abbreviated “SVL”, of between 40 and 118 mm), suggesting that
incomplete ossification may have compromised accurate mea-
surement, or that these specimens were simply too immature
for sexual characteristics to be clearly and consistently devel-
oped. Such a high degree of congruence supports the reliability
of these three criteria. The smallest individual (NMNS-cyn
2003–14) that appears on all three lists has a SVL of 126 mm.
This is near the lower end of the hypothesized size range for
advent of maturity in males (Lin and Rieppel, 1998) and very
close to the size (122 mm SVL) of the smaller embryo-bearing
female (Cheng et al., 2004), and is here accepted tentatively as
representing the minimum size of a mature male.
To more fully quantify both the evidence for the existence of
two groups within our collection and assignment of sex to each
specimen, a principal components analysis (PCA – Table 4) and
a discriminant function analysis (DFA – Table 5) of the data in
Table 1 were performed. However, four specimens (NMNS-chw-
04, NMNS-cyn 2002-10, NMNS-cyn 2003-20, and NMNS-kiko
2004-03) lack data, and one specimen (NMNS-cyn 2003-22),
plots consistently as a conspicuous outlier for most variables so
were not included in this analysis.
Principal Component 1 (PC1) is a contrast between positive
loadings for six fore- and hind-limb measurements (the lengths of
the ulna [10], fibula [12], maximum distal width of the femur [16],
 CHENG ET AL.—DIMORPHISM AND LIFE HISTORY OF KEICHOUSAURUS 403

TABLE 1. Keichousaurus hui, selected measurements, in millimeters.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
NMNS-chw-01 10.5 11.5 9.5 16 33.5 2.5 2 3 1 0.9 1 1 49.5 0.9 0.8 0.6 0.5
NMNS-chw-02 12.2 18.2 15 26 48.2 4 3.8 4.8 2 2 1.8 1.6 74.2 1.2 0.8 1 0.6
NMNS-chw-03 11 16 11 15 40 3 2.8 3.5 1.2 1.2 1 1.2 55 1 0.5 0.9 0.5
NMNS-chw-04 11 15 11.2 16 39.2 3 2.5 3 1.3 1.5 1 1.1 55.2 ? ? ? ?
NMNS-cyn 2002-01 28 76.5 70 110 187 18.2 21 19 10 9 7.5 8 297 5 5 4 3
NMNS-cyn 2002-02 22.5 60 52 96 145 13 13 12.8 6.5 6.2 5 6 241 3 2.5 2.4 1.8
NMNS-cyn 2002-03 21 57 44.5 82 130.5 12.5 13 13 6.5 6 5 5.5 212.5 3 2.5 2 1.8
NMNS-cyn 2002-04 23 70 63 120 166 15.5 25.5 21 12.5 12 8 9 286 3 2 6 3
NMNS-cyn 2002-05 20 54 44 88 128 11 11.5 12 6 6 4.5 4.5 216 3 2.2 2.2 1.3
NMNS-cyn 2002-06 28 81 75 127 198 18.5 22 21 10 9.5 7 8 325 5.2 3.7 3 2.7
NMNS-cyn 2002-07 26 70 61 128 168 16 17 17 9 8 6 6.5 296 4.2 3.8 2.5 2
NMNS-cyn 2002-08 24 72 57.8 120 163.8 14.5 26 21 10 11 8 9 283.8 7 2.9 4 2
NMNS-cyn 2002-10 ? 45 53 120 110 13.8 19.2 17 10 9 6.5 7 230 4.5 2.5 2 1.8
NMNS-cyn 2002-11 25 70.5 57.6 85 163.5 15 22 18 11.5 10 7.5 8 248.5 5.8 2.2 2.8 1.8
NMNS-cyn 2002-12 24 74 65 120 180 17 28 23 14 13 8 10 300 8.5 4 4 3
NMNS-cyn 2002-13 14 22.8 17.2 30 57.5 4.8 4.2 5 2 2 1.8 2 87.5 1 0.9 1.5 1
NMNS-cyn 2002-14 21 57 40 80 126 11.5 17.5 15 9 8.5 4 5.2 206 4.8 2 2 1.7
NMNS-cyn 2003-15 28 82 60 126 182 16.5 25.5 21.5 11 13 9 10 308 7 3 3 2
NMNS-cyn 2003-16 22.5 62 45 90 138 12 13 13.5 6.5 6 4.8 5.8 228 3 2.6 2.2 1.8
NMNS-cyn 2003-17 38 87 95 196 238 21 30 25 14 15 9 10 434 8 4 4 2.8
NMNS-cyn 2003-18 22 60 50.8 99 142.8 12.8 20 17 10.8 9.6 6.5 7 241.8 5.5 3 2.5 2
NMNS-cyn 2003-19 18 40 37 58 102 8.5 9.5 10 5 5 3 4.2 160 2 1.8 1.5 1
NMNS-cyn 2003-20 ? ? 67 138 ? 18 27.5 24 14.5 13 9.5 10.5 ? 10 5 3.6 2.6
NMNS-cyn 2003-21 25 69 67 90 174 17 17 16.5 8 7.5 6 7 264 4 3 3 2
NMNS-cyn 2003-22 28 73 61 20 177 16 24.5 19 12 11 7.5 8.5 197 7 3 3 2
NMNS-cyn 2003-23 20 51 35 70 112 9 10.5 11 5 5 4 4.2 182 2.5 1.8 2 1.2
NMNS-cyn 2003-24 24.5 68 54 95 154 13.8 15 15 7 7 5.6 6.2 249 3 2.6 2.5 2
NMNS-cyn 2003-25 24.5 72 60 112 169 17 25 20 12 11.5 8 9 281 7 3 4 2.1
NMNS-cyn 2003-26 22 56 50 75 148 11 11.5 12 6 6 4.5 4.5 223 3 2 2 1.5
NMNS-cyn 2003-27 23 60 55 90 150 14 16 14.5 7 8 5 6.5 240 3 3 3.5 2
NMNS-cyn 2005-01 28.8 84 71 130 197 16.5 26 22 14 13 8 9 327 7.8 4 3.5 3
NMNS-cyn 2005-02 24 58 50 90 141 12 13 14 7.5 7 5 5.2 231 2.8 2 2.1 1.5
NMNS-cyn 2005-03 28 81 67 130 189 18 19.5 16.5 8 8.5 6 7 319 4.5 3.8 3 2.5
NMNS-cyn 2005-04 19 42.5 36 72 104.5 9.2 10 10.5 5 5.2 4 4.8 176.5 2.3 1.8 1.8 1.1
NMNS-cyn 2005-05 20.5 57 45.5 78 129.5 11.2 10.8 11.5 6 5 4 5 207.5 2.9 2 1.6 1.5
NMNS-cyn 2005-06 25 80 68 100 184 16 20 20 9.5 9.8 7 8 284 5 3 3 2.5
NMNS-cyn 2005-07 21.8 56 50 75 136.8 11 13 12 5.8 5.5 4 5 211.8 2.8 3 2 1.5
NMNS-cyn 2005-08 25 70 56 118 162 15 23 20 12 12 7 9 282 6 2.5 3 2
NMNS-cyn 2005-09 24 73 67 105 176 12 19.5 17 10 10 8 8 281 4 3 3 2.6
NMNS-cyn 2005-10 27 72 64 80 176 16 27 22 13.5 13 9 9 256 7 3.2 3.6 2
NMNS-cyn 2005-11 25 77 65 108 179 15.8 18.5 15 8 8 6 7.2 287 4 3 2.5 2
NMNS-cyn 2005-12 26 73 60 118 172 16 21.5 18 10.5 10 7 8 290 6.5 4 3.5 2.2
NMNS-cyn 2005-13 19 46 38 60 109 8.8 9.5 9.5 4 4 3.5 4 169 1.5 1.5 1.8 1
NMNS-cyn 2005-14 25 58 51.5 90 141.5 12.2 12.5 12.5 6.5 6 5 5.5 231.5 3 2.2 1.8 1.5
NMNS-cyn 2005-15 25 68 61 99 164 14 19 17.5 9 8.5 5.6 7.5 263 3 3.5 2.5 2
NMNS-cyn 2005-16 24 56 52 90 142 13 13 14.5 7 6 5 5.1 232 3.6 2.1 1.9 1.8
NMNS-cyn 2005-17 20 56 43 80 127 10 11 11.2 5 5 4 5 207 2.4 2 1.3 1
NMNS-cyn 2005-18 24.5 71 62 112 169 16.5 18 17 9 9 6 7 281 5 4.2 2.5 3
NMNS-cyn 2005-19 21 47 46 83 124 11 10.5 11.2 5.2 4.5 4 4.2 207 2.8 1.6 1.8 1.2
NMNS-cyn 2005-20 19 41 35 76 102.5 9 9.5 10.1 5 4.8 4.8 4.5 178.5 2.1 1.6 1.2 1
NMNS-cyn 2005-21 25.5 75 63 95 173 15.5 17 18 8 8 7.5 8 268 4 3 2 2.1
NMNS-cyn 2005-22 25 66 52 100 158 14 15 14.5 7 7 4.7 6 258 3.2 2.4 2 1.5
NMNS-cyn 2005-23 21.5 56 45 85 128 11 15 13 7 7 4 5 213 3.8 2 2.1 1.6
NMNS-cyn 2005-24 26 76 60.5 105 175 15 16.8 16 8 7.5 6 6.5 280 3.2 3 3 2.1
NMNS-cyn 2005-25 20 47 37 63 112 10.5 12 12 5.5 5.5 4 5 175 2.9 2 2 1.8
NMNS-cyn 2005-26 23 63 47 87 140 11 11 12 6 6 5 5 227 2 2.3 2.2 1.8
NMNS-cyn 2005-27 21.5 49 38 68 118 10.5 11.2 12 6 5.5 4.5 5 186 3.3 1.5 2 1.2
NMNS-cyn 2005-28 25 70 59 115 166 16.5 22 19 11.5 10.5 6.5 7.5 281 7 3.5 3 2
NMNS-cyn 2005-29 17 24 18 30 63 4.8 5.8 5.8 3 3 2 3 93 1.9 1 1.2 1
NMNS-cyn 2005-30 23 52 42 90 127 11 16 14 8 8 5 6 217 5 2.5 2.9 1.5
NMNS-cyn 2005-31 23 50 41 65 120 10.5 11 12 5.8 5 4 4.8 185 2.8 2.5 2 1.5
NMNS-cyn 2005-32 20 56 52 88 136 12 13 13.5 6 6 5 5.5 224 2.8 2.8 2.5 1.5
NMNS-kiko 2004-01 12 18.2 14 18 47 3.2 3.2 1.8 1.5 4 1.3 1.8 65 1 0.9 1 0.8
NMNS-kiko 2004-03 10.5 13.5 10.8 15 37.3 3 2.9 3 1.8 1.6 1 1.3 52.3 1 0.9 ? ?
NMNS-kiko 2005-X 19 37.5 30 50 93 8 6.8 6.5 3.2 3.2 3 3.2 143 2 1.4 1 0.9
NMNS-kiko 2005-Y 16 32 26 41 79 6.5 6 6 3 2.8 2.2 3 120 1.5 1 1 0.9
NMNS-kiko 2005-XX 28 77 70 140 188 17 30 22 16 14 9 10 328 8 3.8 3.5 2.5
NMNS-kiko 2005-YY 15 31 26 42.5 75 6.5 6 7 3 3 2.5 3 117.5 1.4 1 1.1 1
NMNS000933- 15.6 28 30 40 78 7 6.2 6.8 3.1 3.1 2.3 3 118 2 1 1.8 1
F0034394
NMNS-VL-191 21 44 47 72 122 10.5 12 11 5.5 5 5 5 194 3 2 2 1.8

See Figure 1 for an explanation of the measurements.

404 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009

TABLE 2. Selected measurements of young and embryos.

Trunk Vertebra
Specimen Number Snout-vent (mm) length (mm)
NMNS-chw-01 33.5 0.7
NMNS-chw-02 48.2 1.0
NMNS-chw-03 40.0 0.7
NMNS-chw-04 39.2 0.75
NMNS-cyn 2002-01 (embryos) — 0.9–1.1
NMNS-cyn 2002-13 57.5 1.2
NMNS-cyn 2005-29 63 1.5
NMNS-kiko 2004-01 47.0 0.8
NMNS-kiko 2004-03 37.3 0.75
NMNS-kiko 2004-04 43 0.9
NMNS-kiko 2005-X 93.0 1.9
NMNS-kiko 2005-Y 79.0 1.5
NMNS-kiko 2005-YY 75.0 1.55
NMNS000933-F0034394 78.0 1.3
NMNS-VL-191 (embryos) — 0.5–0.7

maximum distal width of the humerus [14], minimum width of

femoral shaft [17], and minimum width of humeral shaft [15])
and one negative but relatively weak loading for length of humer-
us (7). PC2 is a contrast between one positive loading for length of
humerus (7) and high negative loadings for length of femur (8),
snout-vent length (5), and standard length (6). Five principal
components together explained 77.2 % of the variation in the
dataset. A bivariate plot (Fig. 3) of principal component 1 (PC1)
against principal component 2 (PC2) showed two separate groups.
Backward stepping DFA showed highly significant differences
(p Wilk’s l = 0.0000) with a very high classification accuracy
(91%, jackknifed rate 86%). Backward stepping DFA output
(Table 5) showed that the six variables contributing most highly
to differentiation between sexes are, in order of F-to-remove
statistics and hence their contribution of the prediction of group
membership, minimum width of femoral shaft (17), neck length
(2), minimum width of humeral shaft (15), lengths of radius (9),
skull (1) and tail (4). A bivariate plot of the maximum distal
width of femur (16) and maximum distal width of humerus (14)
ratios (each divided into total length [13]) showed a 94% correct
classification of the sexes (Fig. 4).
In seven cases (NMNS-chw-01, NMNS-chw-02, NMNS-cyn
2003-17, NMNS-cyn 2005-06, -23, -25, and NMNS-kiko 2004-01),
the sex assigned by the DFA (Table 6) flatly contradicts an un-
equivocal identification based on the three ratios used in the
initial qualitative analysis (Table 3). However, only one of these
individuals (NMMS cyn-2003-17) is large enough to be expected
to exhibit fully developed sexual dimorphism. Two others
(NMNS-cyn 2005-05 and -23) are, at most, subadults, and the
remainder are considerably smaller (Table 1) and presumably
immature, making the recognition of sexual dimorphism difficult.
In the 15 cases in which the qualitative identification of males
was equivocal (i.e., at least one of the three ratios did not sup-
port the determination – see Table 3), the DFA identified 10
(NMNS-chw-03, NMNS-cyn 2002-01, -04, NMNS-cyn 2003-25,
-27, NMNS-cyn 2005-09, -27, -28, -29, and NMNS-000933-
F0034394) as males. However, almost all are clearly juvenile;
the largest individual (NMNS-cyn 2002-04) has a snout-vent
length of only 120 mm, most of the others are considerably FIGURE 2. Distribution of three ratios in 70 specimens of Keichou-
smaller. Nevertheless, partial agreement between the qualitative saurus hui inferring sexual dimorphism. See “Discussion” for complete
sex identification and the DFA based on data from primarily explanation.
small individuals suggests that subtle expression of male charac-
teristics may have occurred before the onset of sexual maturity.
The remaining five individuals (NMNS-cyn 2003-27, NMNS-cyn
Reproduction and Growth Patterns in Keichousaurus
2005-03, -11, -15, and NMNS-kiko 2005-X), were identified as
females. All but one are subadult or juvenile, and in all cases, the Although the more than 70 Keichousaurus specimens at
qualitiative identification is weak (only one of the three ratios our disposal vary enormously in size (Table 1), they do not
indicating male). cluster unambiguously into size classes. However, the eight
 CHENG ET AL.—DIMORPHISM AND LIFE HISTORY OF KEICHOUSAURUS 405

TABLE 3. Specimens identified as male based on three ratios. TABLE 5. Six variables selected in backward estimation discriminant
function analysis of 17 measurements taken from 65 individuals.
Sexing Criteria
Variable F-to-remove Tolerance
MAXDWH/ HUMERUS/ HUMERUS/ SKULL (1) 0.73 0.910362
Specimen Numbers MINWHS STANDARDL FEMUR NECK (2) 18.90 0.878165
NMNS-chw-03 X TAIL (4) 0.42 0.927567
NMNS-cyn 2002-01 X RADIUS (9) 3.68 0.858267
NMNS-cyn 2002-04 X X MINWHS (15) 7.14 0.979010
NMNS-cyn 2002-08 X X X MINWFS (17) 58.59 0.796745
NMNS-cyn 2002-10 X X X
NMNS-cyn 2002-11 X X X See Table 1 and Figure 1 for details.
NMNS-cyn 2002-12 X X X See Table 4 for explanation of variables.
NMNS-cyn 2003-14 X X X Four specimens listed in TABLE 1 (NMNS-cwh-04, NMNS-cyn 2002-10,
NMNS-cyn 2003-15 X X X NMNS-cyn 2003-20, and NMNS-kiko 2004-03) lack data, and one speci-
NMNS-cyn 2003-17 X X X men (NMNS-cyn 2003-22) plots as a conspicuous outlier for most vari-
NMNS-cyn 2003-18 X X X ables, so were not included in this analysis. Abbreviations: MINWFS,
NMNS-cyn 2003-20 X X X minimum width of femoral shaft; MINWHS, minimum width of humeral
NMNS-cyn 2003-22 X X X shaft.
NMNS-cyn 2003-25 X X
NMNS-cyn 2003-27 X the smallest specimen are each 0.7 mm long, and of the largest,
NMNS-cyn 2005-01 X X X
NMNS-kiko 2005-X X
1.0 mm long. The SVL of the next larger individual (NMNS-cyn
NMNS-kiko 2005-XX X X X 2002-13—see Table 2) exceeds that of the largest of the eight
NMNS-cyn 2005-03 X putative neonates by almost 10 mm and is almost twice that of
NMNS-cyn 2005-08 X X X the smallest, suggesting that it is almost certainly not a neonate,
NMNS-cyn 2005-09 X X and should not be included when estimating mean neonate size.
NMNS-cyn 2005-10 X X X In addition to the eight isolated neonates, the collection
NMNS-cyn 2005-11 X
NMNS-cyn 2005-12 X X includes a tight cluster of at least seven tiny individuals (NMNS-
NMNS-cyn 2005-15 X chw-04). Extensive overlap of the skeletons (Fig. 6) makes accu-
NMNS-cyn 2005-23 X X X rate measurements difficult, but all individuals are approximately
NMNS-cyn 2005-27 X the same size, with a mean snout-vent length (SVL) of about
NMNS-cyn 2005-28 X X 39 mm, and trunk vertebral length of .75 mm (Table 2). A sepa-
NMNS-cyn 2005-29 X rate tiny, isolated individual (NMNS-kiko 2004-03) with verteb-
NMNS-cyn 2005-30 X X X
NMNS00933-F0034394 X rae of the same length and a SVL of 37.3 mm (Table 2) supports
the estimate of mean SVL for NMNS-chw-04.
Abbreviations: FEMUR, femur length; HUMERUS, humerus length; It is more difficult to estimate the sizes of the embryos
MINWHS, minimum width of humeral shaft; MAXDWH, maximum contained in the gravid females (Cheng et al., 2004:figs. 2, 3),
distal width of humerus; STANDARDL, standard length. since their skeletons overlap and many bones are difficult to
assign to a particular individual. However, at least a few articu-
smallest isolated tiny individuals, ranging in age from 33.5 mm
(NMNS- chw-01, Fig. 5A) to 48.2 mm (NMNS-chw-02, Fig. 5B)
snout-vent length (SVL), with an average of 40.4 mm SVL (see
Table 2) probably represent neonates. The trunk vertebrae of

TABLE 4. Loadings of eigenvectors on five components produced by

principal components analysis of 16 measurements taken from 65
individuals.

1 2 3 4 5
ULNA (10) 0.929 0.221 0.099 0.026 0.019
FIBULA (12) 0.874 0.300 0.113 0.071 0.019
MAXDWF (16) 0.854 0.072 0.158 0.014 0.167
MAXDWH (14) 0.789 0.172 0.063 0.152 0.439
MINWFS (17) 0.740 0.277 0.129 0.286 0.220
MINWHS (15) 0.725 0.157 0.205 0.510 0.021
NECK (2) 0.679 0.710 0.214 0.367 0.110
TIBIA (11) 0.615 0.247 0.295 0.142 0.503
TRUNK (3) 0.566 0.192 0.541 0.252 0.148
FEMUR (8) 0.322 0.917 0.114 0.093 0.034
HUMERUS (7) 0.363 0.889 0.083 0.137 0.074
SVL (5) 0.124 0.711 0.006 0.413 0.075
STANDARDL (6) 0.233 0.559 0.409 0.170 0.291
SKULL (1) 0.267 0.177 0.722 0.280 0.029
RADIUS (9) 0.146 0.267 0.270 0.725 0.326
TAIL (4) 0.392 0.387 0.029 0.244 0.591

See Table 1 and Figure 1 for details.

Four specimens listed in Table 1 (NMNS-cwh-04, NMNS-cyn 2002-10,
NMNS-cyn 2003-20, and NMNS-kiko 2004-03) lack data, and one speci-
men (NMNS-cyn 2003-22) plots as a conspicuous outlier for most vari-
ables, so were not included in this analysis. All measurements represent FIGURE 3. A bivariate plot of principle component 1 (Factor 1)
maximum lengths except MAXDWF, maximum distal width of femur; against principle component 2 (Factor 2; see Table 3) showing clear
MAXDWH, maximum distal width of humerus; MINWFS, minimum separation between males (open stars) and females (filled circles). Nine-
width of femoral shaft; MINWHS, minimum width of humeral shaft. ty percent confidence ellipses are indicated.
406 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009

TABLE 6. Sex assigned to individuals using complete estimation DFA.

Specimen Number Sex Specimen Number Sex

NMNS-chw-01 M NMNS-cyn 2005-08 M
NMNS-chw-02 M NMNS-cyn 2005-09 M
NMNS-chw-03 M NMNS-cyn 2005-10 M
NMNS-cyn 2002-01 M NMNS-cyn 2005-11 F
NMNS-cyn 2002-02 F NMNS-cyn 2005-12 M
NMNS-cyn 2002-03 F NMNS-cyn 2005-13 F
NMNS-cyn 2002-04 M NMNS-cyn 2005-14 F
NMNS-cyn 2002-05 F NMNS-cyn 2005-15 F
NMNS-cyn 2002-06 F NMNS-cyn 2005-16 F
NMNS-cyn 2002-07 F NMNS-cyn 2005-17 F
NMNS-cyn 2002-08 M NMNS-cyn 2005-18 F
NMNS-cyn 2002-11 M NMNS-cyn 2005-19 F
NMNS-cyn 2002-12 M NMNS-cyn 2005-20 F
NMNS-cyn 2002-13 F NMNS-cyn 2005-21 F
NMNS-cyn 2002-14 M NMNS-cyn 2005-22 F
NMNS-cyn 2003-15 M NMNS-cyn 2005-23 F
NMNS-cyn 2003-16 F NMNS-cyn 2005-24 F
NMNS-cyn 2003-17 F NMNS-cyn 2005-25 M
NMNS-cyn 2003-18 M NMNS-cyn 2005-26 F
NMNS-cyn 2003-19 F NMNS-cyn 2005-27 M
MNS-cyn 2003-21 F NMNS-cyn 2005-28 M
NMNS-cyn 2003-23 F NMNS-cyn 2005-29 M
NMNS-cyn 2003-24 F NMNS-cyn 2005-30 M
NMNS-cyn 2003-25 M NMNS-cyn 2005-31 F
NMNS-cyn 2003-26 F NMNS-cyn 2005-32 F
NMNS-cyn 2003-27 F NMNS-kiko 2004-01 M
FIGURE 4. A bivariate plot of maximum distal width of the femur NMNS-cyn 2005-01 M NMNS-kiko 2005-X F
(MAXDWF) and maximum distal width of the humerus (MAXDWH), NMNS-cyn 2005-02 F NMNS-kiko 2005-Y F
each divided in to total length, showing a 94% correct classification of NMNS-cyn 2005-03 F NMNS-kiko 2005-XX M
the sexes (males represented by open stars, females by filled circles). NMNS-cyn 2005-04 F NMNS-kiko 2005-YY F
Ninety percent confidence elipses are indicated. NMNS-cyn 2005-05 M NMNS-000933-F0034394 M
NMNS-cyn 2005-06 M NMNS-VL-191 F
NMNS-cyn 2005-07 F

Four specimens listed in TABLE 1 (NMNS-chw-04, NMNS-cyn 2002-10,

lated series of trunk vertebrae can be measured. These vertebrae NMNS-cyn 2003-20, and NMNS-kiko 2004-03) lack data, and one speci-
of the embryos in the smaller gravid female (NMNS-VL-191) men (NMNS-cyn 2003-22) plots as a conspicuous outlier for most vari-
average between 0.5 and 0.7 mm in length, and those in the ables, so were not included in this analysis.
larger gravid female, between 0.9 and 1.1 mm.

DISCUSSION
Sexual Dimorphism
Although a minimum adult size for males can be estimated
objectively using sexually dimorphic features, establishing the min-
imum adult size for females is problematic because mature females
cannot be reliably distinguished from immature individuals of ei-
ther sex on morphological grounds. The presence of embryos in
NMNS-VL-191 effectively sets the maximum size at which sexual
maturity occurred in females, but the onset of maturity may have
occurred (and given the sample size of only two pregnant females,
likely did occur) earlier. However, if minimum adult sizes of 126
mm SVL for males and 122 mm SVL for females are accepted, the
mean SVL for sexually mature individuals, based on all available
complete specimens (Table 1), is approximately 149 mm for
females, and approximately 161 mm for males. Although there is
no evidence that the sexes differed in size in Neusticosaurus (Sand-
er, 1989:636), in Serpianosaurus, the mean SVL for females (sex
‘x’) is 82 percent of that of the males (sex ‘y’) (Rieppel, 1989:39).
Our sample indicates that female Keichousaurus are also, on aver-
age, smaller than males, but how much smaller cannot be deter-
mined. All that can be said is that the mean value for females is at
least 93% of that of males, which is not as marked as in Serpiano-
saurus, but the disparity in size between the sexes could well have
been, and probably was, greater.
Reproduction and Growth Patterns in Keichousaurus
The presence of an unusually large number of tiny individuals
in deposits of the Middle Triassic of Guizhou Province suggests
that this locality may have been a birthing center where gravid
females congregated. Perhaps the most convincing evidence for
this hypothesis is a tight cluster of at least seven individuals
(Fig. 6). The very close association of these individuals suggests
that they died immediately after birth and never had an oppor-
tunity to disperse. The fact that they are all about the same size,
and that the mean SVL of the seven individuals is very close to
the mean SVL calculated for eight other tiny, isolated indivi-
duals supports this.
Curiously, the dorsal vertebrae of the several smallest isolated
individuals (Fig. 5) measure between 0.7 and 1.0 mm (Table 2),
indicating that they are, on average, smaller than the embryos in
the body cavity of the larger of the two gravid females (NMNS-
cyn 2002-01). The significance of this is uncertain. There is some
evidence to show that in at least some species of garter snake,
there is a positive correlation between the SVL of the mother
and that of the neonates, with smaller females producing smaller
neonates, and a negative correlation with clutch size, with neo-
nates of large clutches being smaller than neonates of smaller
clutches for a given size of the mother (Gregory and Larsen,
1996). It is unknown how generalized this relationship is in squa-
mates, but if applicable to Keichousaurus, then the large size
of the embryos in NMNS-cyn 2002-01 could simply be a product
of the lower number of embryos (relative to the other gra-
vid female) and the large size (SVL of 187 mm as compared
to 122 mm) of the mother. This, and the size range represented
by the several tiny, isolated individuals preserved in the
Middle Triassic deposits of Guizhou Province, suggests that the
embryos in NMNS-cyn 2002–01 are approaching the maximum
neonate size.
 CHENG ET AL.—DIMORPHISM AND LIFE HISTORY OF KEICHOUSAURUS
FIGURE 5. Keichousaurus hui. Tiny, probably neonate individuals. A, NMNS-chw-01; B, NMNS-chw-02; C, NMNS-chw-03. Scale in mm.
Another possibility is that these tiny isolated individuals are
still embryos, as suggested by Lin and Rieppel (1998), possibly
miscarriages that were ejected from the mother’s body at some
point prior to full term. Incomplete ossification in the caudal
region of these smallest individuals potentially supports such
a hypothesis. In contrast with larger sub-adult and adult speci-
mens of Keichousaurus, which have at least 37 caudal vertebrae,
one small specimen (34.2 mm SVL) with a closely articulated
tail comprises 24 well-ossified segments and 10 poorly ossified
FIGURE 6. Keichousaurus hui NMNS-chw-04. Cluster of at least sev-
en tiny individuals.
407
terminal segments (Lin and Rieppel, 1998:fig. 15), and another
(NMNS-chw-03, Fig. 5C) with a SVL of 37 mm possesses only 29
caudal vertebrae. A similar phenomenon is seen in Neustico-
saurus peyeri, in which one small individual (32 mm SVL) pre-
serves only 26 caudal vertebrae in contrast with between 40 and
48 mm recorded in adult specimens (Sander, 1989). Unfortu-
nately, a comprehensive study of the rate and timing of ossifica-
tion of caudal vertebrae in embryonic and neonate reptiles is
lacking. In those extant taxa for which we have data, ossification
of the vertebral column follows an anteroposterior gradient.
Although the caudal skeleton is completely ossified in hatchlings
of Alligator mississippiensis (Rieppel, 1993), advanced ossifica-
tion in hatchling squamates is often restricted to the base of the
tail, with the more posterior portions only incompletely ossified
at best (e.g., Rieppel, 1992a, 1992b, 1994). Thus, the significance
of an incompletely ossified tail in the smallest individuals of
Keichousaurus is equivocal at best.
Studies on extant squamates, of all living amniotes probably
most closely related to sauropterygians (Rieppel, 2000) show
that, for any species, a clear relationship exists between the mean
SVL of the adult female and that of the hatchling (Andrews,
1982). This relationship has been used to predict hatchling size
in extinct reptiles (Currie and Carroll, 1984) and in a few cases, to
support the hypothesis that certain tiny sauropterygian skeletons
were pre-hatchling or prenatal (Lin and Rieppel, 1998; Renesto
et al., 2003; Sander, 1988). If the mean SVL of a reproducing
female Keichousaurus (149 mm, but given the difficulties in esti-
mating minimum adult size of females [see above], this is almost
certainly an overestimate) is plotted on figure 4 of Andrews
(1982), a mean hatchling SVL of approximately 50 mm is pre-
dicted, considerably more than the 40.4 mm calculated from
the specimens available. However, for any given adult size,
hatchling/adult SVL ratios are quite variable in squamates, as
408 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009
FIGURE 7. Log-Log plot of mean snout-vent length of hatchling
against mean snout-vent length of mature females. Squares represent
snakes, circles, lizards. The star represents Keichousaurus. Ninety-five
percent confidence ellipses are indicated. Data from Andrews (1982),
plotted using SYSTAT.
demonstrated when the data (Andrews, 1982:appendix II) are re-
plotted (Fig. 7) using SYSTAT (SYSTAT, 2005). If the average
Keichousaurus neonate SVL is plotted, it falls below the regres-
sion line, but nevertheless well within the 95% confidence ellipse
established for lizards. Therefore, there is no reason to suggest
that the smallest individuals of Keichousaurus are prenatal.
In summary, the minimum snout-vent length (SVL) of mature
male Keichousaurus is approximately 126 mm, and that of the
mature female, at least 122 mm. The mean SVL of mature male
and female Keichousaurus specimens are approximately 161 mm
and at most 149 mm respectively. The size range of the smallest
individuals, as well as the size of the embryos in the two gravid
females, indicate that neonates of Keichousaurus range from
about 33.5 to 48.2 mm SVL at birth, establishing the mean SVL
of hatchlings/neonates at about 40.4 mm. There is no compelling
evidence to suggest that the several tiny isolated individuals are
aborted embryos. Rather, their size, relative to the mean adult
female size, as well as extent of ossification, falls within the
ranges exhibited by hatchlings/neonates of extant squamates.
ACKNOWLEDGMENTS
We thank Shan Shi-yin of the NMNS for her assistance at all
times when accessing the specimens under her care, Cheng Hao-
wen for access to his collections, and Paleowonder Fossil and
Mineral Museum in Taipei for the skillful preparation of the
specimens and generous assistance during the course of this
project. R.Holmes and X.-c. Wu are grateful to the NMNS for
their hospitality during their visit. This work was supported
by research grants from the NMNS and the National Science
Council of RO China (NSC 95-2116-M-178-001) to Y.-n. Cheng,
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and RAC Grants from the Canadian Museum of Nature to
R. Holmes and X.-c. Wu.
We would also like to thank P. Gregory of the University of
Victoria for helpful information on reproduction in snakes,
A. Resenter of the Field Museum of Natural History (Chicago)
for allowing us to examine cleared and stained material under
his care, A. Murray for help with graphics, M. Calwell and
P. M. Sander for their sympathetic and helpful reviews, and
R. Motani and F. O’Keefe for their editorial assistance and sug-
gestions regarding the statistical analysis.
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