(oological Journal of&
Linnean So&& (ZOOO), 130: 551-566. With 5 figures
doi: 10.1006/zjls.2000.0243, available online at http://www.idealibrary.com on
€3
I D E )r-L
*
Growth curve of Psittacosaurus mongoliensis
Osborn (Ceratopsia:Psittacosauridae) inferred
firom long bone histology
GREGORY M. ERICKSON'* AND TATYANA A. TUMANOVA2
Department o f Integrative Biology and Museums of Paleontology and Vertebrate <oology,
University o f Cal$omia, Berkdg, CA 94720, USA.
2Paleontological Institute, Russian Academy o f Schces, Moscow, Russia
I
Received December 1998; accepted for publication January 2000
The skeleton undergoes substantial histological modification during ontogeny in association
with longitudinal growth, shape changes, reproductive activity, and fatigue repair. This
variation can hinder attempts to reconstruct life history attributes for individuals, particularly
when only fossil materials are availble for study. Histological examinations of multiple
elements throughout development provide a means to control for such variability and
facilitate accurate life history assessments. In the present study, the microstructure of various
major long bones of the ceratopsian Psittacosaum monogolimis Osborn were examined from
a growth series spanningjuvenile through adult developmental stages. The first reconstruction
of a growth curve (mass vs. age) for a dinosaur was made for this taxon using a new method
called Developmental Mass Extrapolation. The results suggest P mongolitmix (1) had an Sshaped growth curve characteristics of most extant vertebrates, and (2) had maximal growth
rates that exceeded extant reptiles and marsupials, but were slower than most avian and
eutherian taxa.
0 2000 The Linnean Society of London
ADDITIONAL KEY WORDS:-Dinosauria - histology - skeletochronology - growth
rings - growth rates - longevity - heterochrony - development - Developmental Mass
Extrapolation.
CONTENTS
Introduction . . . . . . . . . . . . .
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Material and methods
Histologic sample and techniques . . .
Developmental Mass Extrapolation . . .
Longevity and growth rate calculation . .
Results . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . .
References . . . . . . . . . . . . .
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* Corresponding author. Present address: Dept Biological Science, Conradi Bldg., Dewey Street and
Palmetto Drive, Florida State University, Tallahassee FL 32306, U.S.A. Email: [email protected]
002+4083/00/120551+ 16 $35.00/0
55 I
0 2000 The Linnean Society of London
552
G. M. ERICKSON AND T. A. TUMANOVA
INTRODUCTION
Histological examinations have been conducted on the skeletal remains of dinosaurs
since their formal scientific recognition over 150 years ago (Owen, 1842). For
instance, morphological studies on the first known dinosaurs &nodon anglicus Holl,
Hyaelosaurus armatus Mantell, Megalosaurus bucklandii Rutgen, Pelomsaurus conybearei
Melville, and Cetiosaurus medius Owen all included descriptions of the osseus microstructure (Owen, 1840-45; 1859; Queckett, 1855; Mantell, 1850a, b). Recently it
has been demonstrated that histological data have utility for understanding multiple
aspects of dinosaur palaeobiology and evolution. For instance, by comparing bone
and tooth microstructure with that of extant vertebrates researchers have inferred
dinosaur longevity m c q l b , 1983; Chinsamy, 1990; Varicchio, 1993; Erickson,
1997), age at maturity (Chinsamy, 1993; Varricchio, 1993), tooth development and
replacement rates (Erickson, 1996), skeletal mechanical properties (Currey, 1987;
Erickson et al., 1996), locomotory capacities (Horner & Weishampel, 1988), anatomical functions (Buffkknil,Farlow & Ricqlts, 1986),phylogenetic affiliations (Berreto
et al., 1993) and aspects of metabolism (Ricqlb, 1974, 1980; Reid, 1997).
Studies on extant osteichthyan vertebrates have shown that skeletal elements
undergo substantial histologic changes during ontogeny in association with bone
growth (Enlow, 1963; Ricqlb et al., 1997), Haversian remodelling (fatigue damage
repair; Burr et al., 1985), osseous drifting (element shape changes owing to regional
growth differences; Enlow, 1963) and oviparity (Wink,Elsey & Ha, 1987). The
timing, sequence, and types of such changes often differ between elements within
individuals (Ricqlh, Padian & Horner, 1997). This developmental variation can
hinder attempts to histologically assess life history attributes (e.g. longevity, growth
rates, age at maturity) for individuals using the skeleton. This is particularly true for
dinosaurs, since single individuals and/or elements are often the only specimens
available for analysis. In cases where limited material is examined, it is not uncommon
to fmd that morphological changes through ontogeny have effaced growth lines
used to directly age specimens (Horner, Padian & Ricqlb, 1997) or that relative
assessments of somatic and/or reproductive maturity cannot be made using histology
due to uncertainties about osseous development throughout the body.
To overcome such problems, an a priori understanding of intra- and interelemental
changes through ontogeny is often necessary. It is for these reasons that Ricqlks et
al. (1997) advocate studies characterizing the histology of multiple elements in
specimens spanning development. Hypothetically, researchers armed with such
background information are able to make more accurate life history assessments
about individuals, even when partial remains are the only materials available for
study.
The only multi-elemental ontogenetic study published to date on dinosaur osteohistology was that performed on the maniraptor TmodonformosusLeidy by Varricchio
(1993) who studied the histologic changes in the third metatarsal and tibia in a
partial growth series for this taxon. Nevertheless, results from several other studies
along these lines may soon reach fruition. Findings on the histology of the giant
sauropod Apatosaurus excehs Marsh (Curry, 1998) and the hadrosaurid Maiasaura
peeblesomm Horner et Makela (Ricqlks, Horner & Padian, 1998) have been recently
presented at professional meetings.
Here we expand the multi-elemental, ontogenetic database for dinosaurs to include
the basal ceratopsian, Psitkzcosaurus mongoliensis Osborn from the Late Cretaceous
PSITLACOSAURUS MONGOLIENSIS GROWTH
553
TABLE
1. Specimens of Psittmosaurus mongoliensis used for histological analysis
Element
Specimen
number
Humerus
Humerus
Humerus
Humerus
Humerus
Femur
Femur
Femur
Femur
Femur
Femur
Femur
Tibia
Tibia
Tibia
Tibia
Tibia
PIN 1369/1-11/1948
PIN 698/1977
PIN 698/15/1977
PIN 1369/1-11/1948
PIN 698/5-3/ 1946
PIN 698/4-22/1946
PIN 698/7-4/1946
PIN 698/1977
PIN 698/15/1977
PIN 698/2-2/1977-15
PIN 698/1977
PIN 698/1977
PIN 698/4-22/1946
PIN 698/ I946
PIN 698/1977
PIN 698/2-2/1977-15
PIN 698/5-9/2/1946
Estimated
length (cm)
Growth
Stage
9.0
11.6
12.8
14.5
18.0
7.6
9.8
11.2
14.8
16.0
20.0
21.0
6.4
7.1
9.5
13.0
15.9
B
C
D
E
F
A
B
C
D
E
F
G
A
B
C
E
F
aptiadalbian Khukhtekska Svita of the People’s Republic of Mongolia. Major long
bones (appendicular skeletal elements that have lengths greatly exceeding their
widths; Marieb & Mallatt, 1992) from individuals spanning juvenile through adult
developmental stages were examined. Our specific goals were to: (1) characterize
histologic variation during the ontogeny of P mongoliensis long bones, (2) assess
longevity for the specimens, (3) reconstruct a growth curve for the taxon, (4)compare
the maximal growth rates of this taxon with those for extant taxa (i.e. address the
question: was this dinosaur capable of somatic growth rates rivaling extant birds
and mammals?), and (5) provide comparative data for future analyses of dinosaur
paleobiology, bone microstructure, functional skeletal morphology, phylogeny, physiology and heterochronic evolution.
MATERIAL AND METHODS
Histologic sample and techniques
Specimens of P monogoliensis from the collections of the Paleontological Institute
(PIN), Moscow, Russia were selected for histological analysis (Table 1). These fossils
were collected during the joint Soviet-Mongolian expeditions of 1946, 1948, and
1977 to the Khukhtekska Svita of the People’s Republic of Mongolia (Kalandadze
& Kurzanov, 1974; Novodvorskaya, 1974; Barsbold & Perle, 1983) and included
an ontogenetic series ranging from juvenile to adult growth stages (Weishampel &
Horner, 1994). During these expeditions, associations of both partially and fully
articulated specimens of P mongo1hi-s were found from various horizons at a locality
known as Khamrin-Us. Taphonomic interpretations suggest these animals were
buried by the deltaic sands of a tropical flood plain (Shuvalov, 1974). Other
inhabitants from this environment included tyrannosaurs, stegosaurs, ankylosaurs,
554
G. M.ERICKSON AND T. A. TUMANOVA
turtles, lizards, and triconodont mammals (Kalandadze & Kurzanov, 1974;
Novodvorskaya, 1974; Shuvalov, 1974; Barsbold & Perle, 1983).
Humeri, femora, and tibiae from I! mongolinesiswere assigned by size to one of seven
classes (designated A-G from smallest to largest, Table 1) and single representative
specimens chosen for microstructural examination. The bones were missing either
the proximal or distal ends, thereby minimizing processing damage to elements in
the collection, but each had a portion of the diaphysis intact. Whole element lengths
were determined from the intact contra-lateral elements or from comparably sized
elements from associated individuals.
Prior to histologic processing, mid-diaphyseal minimal circumference measurements were made on the largest femur (stage G, Table 1) for later use in body
mass and growth rate estimations (see below).
Diaphyseal transverse thin-sections were made from each long bone. Onemillimeter transverse cortical cuts were made into the bones using a slow-speed saw
fitted with a diamond-tipped wafering blade. When possible the plane of sectioning
for each element was made at mid-shaft. Nevertheless in some cases the sites of
fracture necessitated taking the sections from the proximal or distal diaphysis. For
femora, mid-shaft lay immediately distal to the third trochanter at mid-shaft. For
tibiae it lay roughly two-fifths of the distance from the distal end of the bones.
Humeri were cut just below the deltoid crest at the distal-third of each element.
For the majority of the specimens the entire excised bone wafers were glued onto
petrographic microscope slides using epoxy and manually ground to 50-100 pm
thickness using a rotary lap grinder and descending grades of silica-carbidesandpaper
(150-600 grit). For the two largest femora (stages F & G, Table 1) however, only
representative sections were taken prior to mounting and sanding owing to postmortem longitudinal fracturing. All sectioned materials were then rotary polished
on a felt pad using wetted aluminum-oxide powder. The slides were then placed in
a water-filled ultrasonic cleaner to remove microscopic grit. The finished thinsections were viewed at 20 to 400 x magnifications with a polarizing petrographic
microscope.
The criteria and terminology adopted by Francillon-Vieillot et al. (1990) were
used to qualitatively describe the osseous microstructure of each specimen. The
intracortical histologic structure of older individuals was used to infer patterns in
more juvenile growth stages: (1) when representative specimens were not available
for a particular growth stage, and (2) when it was found that the histologic structure
of specimens had been destroyed by fungal activity.
It should be noted that the use of single specimens in this study to represent
individual growth stages left open the possibility for variance from typical growth
for this taxon owing to individual and/or sexual variation. Thus we view the results
and growth rate inferences made in this study as approximations of the general
patterns to be expected should a larger survey be conducted on I! mongolienris from
the Khukhtekska Svita.
Developmental Mass Extrapolation
An estimate of adult body mass was made using the minimal femoral diaphyseal
circumference measurement from the largest individual (Stage G, Table 1) and the
PSL'TACOSA URUS MONGOLIENSIS GROWTH
555
TABLE
2. Developmental mass extrapolation
Growth
Stage
A
B
C
D
Femur
length
(F) (cm)
Est.
age
3
4
5
6
E
7
F
G
8
9
7.6
9.8
11.2
14.8
16.0
20.0
21.0
A Mass
Cube
of
femur
length
(cm')
Yo of
Adult
femur
cubic
length
body
mass
from
previous
stage
0%)
(kg/yr)
439
94 1
1405
3242
4096
8000
926 1
4.7
10.2
15.2
35.0
44.2
86.4
100.0
0.94
2.03
3.02
6.96
8.79
17.16
19.87
1.09
0.99
3.94
1.83
8.37
2.7 1
Est.
AMass
per day
from
previous
stage
(g/dy)
AMass
per day
from
regression
equation
for Fig. 4
WdY)
-
-
2.9
2.6
10.5
4.9
22.4
7.2
2.6
5.0
8.3
11.5
12.5
10.5
interspecific allometric equation established by Anderson, Hall-Martin & Russell
(1985).
Our next goal was to estimate body mass at each of the various €? mongoliensis
growth stages. However, since interspecific growth equations such as that employed
by Anderson et al. (1985) cannot be used to predict ontogenetic growth patterns
(each taxon is predicted to cross the regression line at adulthood but not necessarily
track it throughout development [see Calder, 19841) we developed a new method
using allometric principles that we refer to as Developmental Mass Extrapolation
(hereafter DME). Hypothetically, if one knows how a linear measurement from an
anatomical structure scales with body mass throughout ontogeny, and the body
mass(es)of one or more individuals are known, then comparable linear measurements
taken from conspecifics can be used to extrapolate individual body masses. In the
present study we used the DME principle as follows: first we took the cube of
femoral length (13) for each specimen (femoral length scales isometrically to the
0.33 power during ontogeny in the extant archosaurs-crocodilians [podson, 19751
and birds [Carrier & Leon, 19901) and assessed each value as a percentage of the
adult value (i.e. the value for the largest femur). The percentages were then converted
to fractional values. Finally, we multiplied the fractional values by the adult mass
estimate (see above) to obtain body mass estimates at each of the R mongoliasis
growth stages (stages A-G, Table 2).
-
IAngevip and p w t h rate calculation
Growth lines in the t? mongoliensis bones were interpreted as having been annually
deposited based on morphological (Francillon-Vieillot et al., 1990; Castanet et al.,
1993)and phylogenetic considerations (Growth lines in the form of annuli and lines
of arrested growth [sensuFrancillon-Vieillot et al., 19901 are annually deposited in
extant members of the outgroup clades to the dinosauria-Actinopterygia, Amphibia,
Lepidosauria, and Crocodylia [Adams, 1942; Netsch & Witt, 1962; Castanet &
Smirina, 1990; Francillon-Vieillotet al., 1990; Castanet et al., 1993; Castanet, 19941.)
Longevity estimates were made for each specimen by counting the growth line
annuli in the thin-sectioned bones. Missing growth lines due to medullar cavity
556
G . M.ERICKSON AND T. A. TUMANOVA
PSITLACOSAURUS MONGOLIEABIS GROWTH
557
expansion were backcalculated using the methods of Castanet & Cheylan (1979)
and Chinsamy (1990, 1993).
To assess growth rates for El rnongoliasis, the DME and age data for the taxon
were coupled. Growth rate estimates between consecutive years during ontogeny
were obtained by subtracting body mass values (regression values, Table 2) for
consecutive annual growth stages from one another progressing from the largest
(Stage G) to the smallest (Stage A). To allow comparison with the maximal growth
rates for extant taxa, the rates were then converted to daily values by dividing each
by 374 days, the length of an aptiadalbian year (Wells, 1963). The conversion to
daily rates facilitated direct comparison with the data for extant vertebrate taxa
such as small avian and mammalian animals that often attain all or the majority of
their mass in a matter of weeks and whose growth rates are typically presented in
sub-annual increments (Case, 1978). It should be noted that these comparisons are
only possible between animals of comparable adult mass due topcaling considerations.
For instance scaling laws dictate that if two species have different body masses at
comparable stages in development, one being twice the size of the other, and both
undergo a comparable ontogenetic transition whereby they mitotically double in
size-the taxon that is initially larger will show a growth rate eight times greater
than the smaller animal. However, these differences would be largely attributable
to initial size variance rather than differences in tissue formation rates. It is for these
reasons that in order to help isolate histological tissue level signal from scaling
influences, only the growth of comparable sized animals can by contrasted (see
Case, 1978; Calder, 1984).
RESULTS
The microscopic preservation of the majority of the El mongolienis specimens from
the Khukhtekska Svita was outstanding relative to fossilized bones from other
formations examined by us previously. During diagenesis the bony matrices had
been replaced by an opaque, siliceous mineral, whereas the vascular canals were
infilled with a dark, ferric mineral. This unusual contrast made it possible to threedimensionally view the vascular lattice in much of the thin-sectioned material (Figs
1, 2) and qualitatively ascribe each specimen to histologic type with certainty. For
a few specimens (three femora and two humeri) post-mortem fungal activity had
effaced some of the extracellular bone matrix. Nevertheless, it was possible to
determine the predominant microstructural bone type in each case using the
unaffected portions of the thin-sections and by backcalculating using older specimens
(see methods above).
The predominant extracellular matrix in all of the long bone specimens was
woven-fibred (randomly oriented bone fibres and rounded osteocyte lacunae, [smu
Pritchard, 19561; Fig. 2A-D) and vascularized. The matrices of the bones were
interrupted by annuli consisting of parallel-fibred bone (moderately packed bone
fibres with flattened osteocyte lacunae that collectivelyrun in parallel; s m u FrancillonVieillot et al., 1990) and/or a lamellar-bone matrix (mats of tightly packed bone
fibres with flattened osteocyte lacunae stacked in thin layers known as lamellae, s m u
Frost, 1960; Figs 1, 2A & B). The vascular canals of all specimens had been infilled
by centripetally deposited lamellar bone, thus forming a fibrolamellar complex (smu
Ricqlks, 1975).
.
558
G. M. ERICKSON AND T. A. TUMANOVA
Figure 2. Common histologic types in long bone diaphyses of PsittaCosaunu rnongo1imi.s during ontogeny.
Sections are viewed in the transverse plane. A, tibia from growth stage A (- 3 years of age) showing
an extracellular matrix (grey) composed of fibro-lamellar bone with longitudinally oriented vascular
canals (black, unbranched) and simple reticular vascular canals (black, branched). The arrow denotes
an annulus, a type of growth line composed of parallel-fibred bone. The width of the plate is 1.O mm.
B, tibia from growth stage E (-7 years of age) with an extracellular matrix (grey) composed of
fibrolamellar bone and showing reticular vascularization (black branched structures). Arrow denotes
an annulus composed of parallel-fibred bone. The width of the plate is 2.25 mm, C, tibia from growth
stage F ( N8 yeares of age) showing a fibrolamellar extracellular matrix (opaque). Simple reticular
vascularization (black branched structures) appear in the lower half of the plate, whereas radially
oriented vascular canals predominate nearer the periosteal surface (black structures aligned vertically
in the upper two-thirds of the plate). This intra-elemental change in vascularization reflects osseous
drifting (changes in long bone shape in the transverse plane of a long bone) that occurred during
PSIT7ACOsilURUS MONGOLIEWS GROWTH
559
Medullar cavity expansion had effaced the earliest formed bone in each element
no later than stage D (age 6, see below) and no one specimen had bone representing
greater than five growth stages remaining (Fig. 1). Endosteal deposition of lamellar
or parallel-fibred bone was observed locally in some of the thin-sections from various
ontogenetic stages, and in all instances in which osseous drift had occurred.
Longevity estimates for the specimens from growth stages A-G ranged from 3 to
9 years, respectively (Table 2). Equivalent estimates of age were obtained for the
various elements from each developmental stage.
Substantial ontogenetic differences in vascular canal branching patterns occurred
in Z? mongoliensis long bones during ontogeny. These changes are outlined below
with respect to age and are depicted graphically in Figure 3.
The tibial diaphyses of neonate I? monogoliensix primarily showed longitudinal
vascularization, although some simple reticular vascular canals were occasionally
present (Fig. 2A). The proportion of the two patterns reversed through ages 2 and
3, and by 4 years of age only reticular vascular canals were formed (Fig. 2B). At 5
years of age, a thin layer of longitudinally vascularized bone formed half of
circumference of the tibial cortices, whereas thicker zones of reticular vascularized
bone formed over the rest of the diaphysis. This dichotomy presumably reflects
osseous drifting whereby the more highly vascularized reticular bone formed more
rapidly than the former (Amprino, 1947; Ricqles et al., 1983, Castanet et al., 1996 ).
Reticular vascularized matrices were formed between 6 and 7 years of age. During
the 8th year of growth it was found that three variably vascularized tissues were
formed reflecting another bout of osseous drifting. A thick layer of highly porous
radially vascularized bone was deposited over one quarter of the diaphyses (Fig.
2C), a layer with intermediate cortical thickness composed of moderately vascularized
reticular bone formed on half of the periosteal surface, and a thin layer of lightly
vascularized longitudinally oriented matrix formed about the remainder of the shaft.
The femora of Z? mongoliensis at partition had diaphyses that were longitudinally
vascularized. At 2 years of age the cortices showed simple reticular and radially
oriented reticular vascular canals. From ages 3 through 6, only highly branched
reticular vascular canals formed in the growth zones. From ages 7 through 8,
reticular vascularized bone continued to form, but local deposition of radially
vascularized bone also occurred. By 9 years of age, radially oriented vascular canals
were forming over half of the circumference of the element when the final growth
zone was made. Like the changes that occurred in the tibiae, these histologic changes
may reflect osseous drifting at the site of sectioning.
The diaphyses of neonate-through-age four humeri had longitudinally oriented
vascular canals or radially oriented simple reticular vascular canals (short vessels
with a few [typically one to five] reticulating branches emanating from a longer
radially oriented stem canal; new definition). The latter pattern predominated at 5
ontogeny. The width of the plate is 10.4 mm. D, tibia from growth stage C (- 5 years of age) showing
an annulus of parallel-fibred and lamellar bone (moderately vascularized bone in upper third of the
plate with laminations [lamellael running horizontally) that was forming on the outermost periosteal
surface of the element at the time of death. Reticular vascularized fibro-lamellar bone (black branching
structures within a grey surrounding matrix) is seen in the lower half of the plate. The width of the
plate is 1.25 mm.
560
G. M. ERICKSON AND T. A. TUMANOVA
Figure 3. Diagram depicting changes in diaphysealvascularization patterns during ontogeny for various
major long bones in PSittacosau7u.s rnongo1k.k from the Khukhtekska Svita. The icons within each
rectangle represent vascular canal branching patterns prevalent in each respective thin-section that
were deposited during the last ‘annual’bout of bone deposition. The proportions of each vascularization
type are reflective of their prevalence relative to the total circumference of the thin-sectioned bones.
Growth stages in letters were assigned prior to the determination of the ages for each specimen using
skeletochronology (growth line counts, smu Castanet, 1994).The vascularizationpatterns for specimens
shown with gray backgrounds were inferred from older specimens by characterizing the histology from
growth zones deposited earlier in ontogeny (i.e. nearer the present medullar cavity). The vascularization
patterns differed substantially between elements at comparable growth stages and during development.
years of age. From ages 6 through 8, highly branched reticular vascular canals were
most commonly formed.
Several large intracortical osteoclastic resorption cavities without lamellar infilling
were found in the tibia from an individual estimated to be 8 years of age. Comparable
structures were not observed in other elements from the growth series.
Mass estimates through ontogeny ranged from 0.94 kg for the smallest individuals
(Stage A, age 3) to 19.87 kg for the largest individuals (Stage G, age 9; Table 2).
PSl71ACOSAURU.S MO.NGOLIIXS1.S GROWTH
56 1
25
,,I--
20
-
Mass =
25.2
,
,,
( l+e-0.74 (Age-7.33)
h
M
6
15m
i
h
g
10-
0
5
10
15
Age (years)
Figure 4. Life history curve for Psithcosaurus mongoliensis from the Khukhtekska Svita. As in most extant
animals the growth curve appears to have an S-shape that is best described using a logistic (or
sigmoidal) equation. The absence of a complete plateauing to the growth asymptote by the largest
specimens used in this analysis may be attributable to these animals not being of maximal adult size.
Based on the regression equation for the mass estimates versus age (Fig. 4), daily
growth rate estimates between ages three and nine ranged from 2.6 g/day to 12.5 g/
day for I! mongolimsis (Table 2).
DISCUSSION
Although it was demonstrated decades ago that dinosaur bones undergo substantial
histologic changes during ontogeny (Nopsca & Heidsiek, 1933), the practical use of
microstructural type to assess age in dinosaurs has not been realized. The reasons
for this stem from uncertainties regarding the timing, sequence and types of histologic
tissues deposited between elements during ontogeny (Ricqlb et al., 1997). The
present study represents the most extensive multi-element documentation of ontogenetic changes in these parameters for a dinosaur. This study opens the door to
attaining life history information from incomplete specimens of I! mongolimsis found
in the future and provides a template for gaining a much greater understanding of
the biology and evolutionary life history of this taxon.
The histological changes in I! mongoliensis long bones suggest the growth of this
dinosaur differed from that typical of other dinosaurs at the tissue level. The most
notable difference was the deposition of progressively more highly vascularized bone
through ontogeny culminating with the local formation of radially vascularized tissue
in three of the largest individuals. This pattern is converse to that typically found
in dinosaurs (Ricqlks et al., 1983; Chinsamy, 1990, 1993, 1994, 1995; Varricchio,
1993) and the formation of the latter tissue type is a rarity in this clade. Since
growth rates in osseous tissues have been shown to positively correlate with vascular
canal density (Amprino, 1947; Ricqlb et al., 1983, Castanet et al., 1996), it would
562
G . M. ERICKSON AND T. A. TUMANOVA
appear that accelerated rather than slowed osteoblastic activity characterized osseous
formation in this animal during the ontogenetic stages surveyed. In extent vertebrates
highly vascularized, radial bone tissue forms locally within the skeleton and is
deposited at rates as great as 1 mm/day (Goodship, Lanyon & McFie, 1979; Lanyon
& Rubin, 1985). It forms the bulk of bony calli during fracture repair and manifests
itself when bones undergo substantial shape changes in association with loading
changes. Whether this tissue type in El mongoliensk is somehow pathologic (calli were
not observed), reflects a loading change perhaps associated with a shift from faculative
bipediality to quadrapedality, or results from muscle insertion migration is currently
indeterminable.
If a taxon’s growth rates are known throughout development, growth curves
(body mass vs. age) can be plotted and used to make interspecific life history
comparisons (McKinney & McNamara, 1991). The information from the present
examination fits these criteria and allows the first quantified reconstruction of such
a life history curve for a dinosaur (Fig. 4)and growth rate comparisons with extant
taxa (see below). It is apparent from Figure 4, that the overall pattern of growth in
El mongoliensis was S-shaped or idealized ( s m u Purves et al., 1992). (The stepped,
discontinuous annual growth in this taxon is smoothed-out when presented in this
manner). Such life history curves characterize the development of most extant
animals regardless of scale, phylogenetic affinities, and physiological status (Peters,
1983; Purves et al., 1992). Animals growing in this manner characteristically experience relatively slow increases in body mass early in ontogeny during a stage
known as the lag phase (smu Sussman, 1964). The lag phase is followed by a
sustained rapid growth period known as the logarithmic or exponential stage ( s m u
Sussman, 1964) in which most of the eventual adult body mass is gained. The third
and final growth stage is known as the stationary phase ( s m u Sussman, 1964) and
is typified by a plateauing of somatic growth late in ontogeny as growth gradually
comes to a near or complete standstill. The growth rates for I! mongolien& of up to
2.6 g/day between ages 3 and 4, increasing up to 12.5g/day between the ages of
7 and 8, and a slowing slightly to 10.5 g/day between ages 8 and 9 (Table 2; Fig.
4), likely conform to these respective stages with the latter specimens potentially
representing individuals at the beginning of the stationary phase.
Comparison of the maximum daily growth rate for El mongolienk (12.5 g/day) from
the growth curve (Table 2) with rates for extant terrestrial vertebrates of comparable
adult mass of during the exponential stages of growth (multi-author compilations
by Case, (1978) and Calder, (1984); Fig. 5) reveals that the dinosaur grew approximately four times faster than most extant reptiles (3.4 g/day for a 19.87 kg
animal), 25% faster than marsupials (10 g/day), and about 3-20 times slower than
typical eutherian (50 g/day) or avian taxa (41-261 g/day).
In regard to these comparisons one should bear in mind that the growth rate
estimates for I! mongolimis are conservative to an unknown degree. The data
compiled by Case (1978) were taken while the animals were experiencing rapid
sustained growth over a portion of the year. Whereas, the growth rate calculations
for El mongoliensis are estimates for an entire year’s growth and thus include the slowgrowth period when annuli were deposited. (It is not currently possible to accurately
assess the duration of such slow-growth periods.) In addition, although the largest
specimens in this study rival the largest known for the species, it is possible that El
mongo1iensi.s reached somewhat larger sizes given the incomplete plateauing of the
PSITLACOSAURUS MONGOLIENSIS GROWTH
Altricial
ds ,Eutherians
Precocial
birds
Marsupials
1000
h
33
100
Ii
10.0
563
,Reptiles
a
a2
4J
E
0
k
&
1.00
.l
x
4
0.10
0.01
10
100
1000
10k
100k 1OOOk
Adult body mass (grams)
Figure 5. Growth rate for Psittucosaunrr mongolhsis compared with rates for members of extant vertebrate
clades of comparable adult size. The regression lines represent typical maximal daily growth rates
during the exponential phase of growth in each clade. These values and the layout for the plate are
adapted from the multi-author compilations by Case (1978) and Calder (1984).The maximal growth
rate estimate for l? mongolimsis (12.5g/day, denoted by P in white box) exceeds values typical for
comparable sized extant reptiles by 3.7 times and is 1.25 times faster than marsupialian taxa. The
rates are however 3.3-20.8 times slower than most eutherian or avian taxa. The dinosaur data
includes growth that occurred at decelerated levels when histological growth line annuli were
formed. Consequently, these data probably underestimate the actual maximal growth rates these taxa
experienced. In addition these data assume an adult mass of 19.87 kg for l? mongolimis that may be
an underestimate based on the asymptote in Figure 4.Mean growth rates within each grouping for a
19.87 kg animal are 3.4 g/day for reptiles, 10 g/day for marsupials, 50 g/day for eutherian mammals,
41 g/day for precocial birds, and 261 g/day for altricial birds (Case, 1987).
asymptotic stage plotted in Figure 4. This would also confer a slight increase in the
estimated growth rates for the taxon.
Although growth rates are considered a strong indicator of metabolic and
physiological status in vertebrates (Bertalanffy, 1957; Case, 1978; Calder, 1984),we
feel the link between histologically derived growth rates for P mongoliensis and these
attributes should be made with caution due to uncertainties regarding environmental
influences on dinosaurian growth. We can not currently assess whether Mesozoic
environmental conditions (temperature, diet, atmospheric consistency, etc.) may
have facilitated rapid growth rates in this taxon as have been similarly been induced
in captively raised reptiles. The data used by Case (1978) in generating the regression
lines seen in Figure 5 serve to convey this point. Although not conveyed graphically,
there was overlap in the growth rates between slow growing eutherians (e.g. primates)
and rapidly grown captive snakes and chelonians in the data used in making the
regression lines. Thus it appears that some reptiles (albeit with unusual bodily
proportions) can attain maximal growth rates within the lower bounds of mammalian
rates under certain environmental conditions.
564
G. M. ERICKSON AND T. A. TUMANOVA
This paper is but one of many demonstrating the utility of histological analyses
for interpreting paleobiologicaland/or evolutionary information regarding dinosaurs
that cannot be gained solely from traditional gross morphological studies. There are
nearly a dozen dinosaurs for which numerous specimens are available and individuals
spanning broad developmental ranges exist (Weishampel & Horner, 1994)for which
similar analyses could be done. We believe their study would greatly advance our
understanding of dinosaur life history and other aspects of palaeobiology and
evolution and we strongly encourage future investigations.We are currently applying
the DME principle to some of these taxa with the intention of comparing their
growth with that of II morgolienrG and comparing dinosaur growth as a whole with
extant vertebrate clades.
ACKNOWLEDGEMENTS
This research was made possible by the Exchange Program the Museum of
Paleontology of the University of California, Berkeley and the Paleontological
Institute of the Russian Academy of Sciences, Moscow. We thank then-Director J.
H. Lipps (UCMP) and Director A. Y. Rozanov (PIN) for their support and
arrangements, and Dr J. Cerny, Dean of the Graduate Division, U.C. Berkeley for
financial support for our participation in the Exchange Program. Histologic processing of specimens was made possible by Marvalee Wake at the University of
California, Berkeley through a grant presented to her by the National Science
Foundation, NSF-IBN95-27681. We also wish to acknowledge the assistance of S.
M. Kurzanov, M. A. Fedonkin, J. Tkach, B. Waggoner, A. Collins, B. Dundas, T.
Trukatis, M. Wake, M. Goodwin, D. Polly, and P. Holroyd, D. Carter, A. de
Ricqlb, K. Padian, J. Horner, Y. Norpchen, S. Yerby, G. BeaprC, Y. Katsura, D.
Varricchio, K. Chin, K. Middleton, S. Gatesy, and P. Sereno.
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