Erickson & Tumanova, 2000 by Felipe Elias

Zoological Journal of the Linnean Society (2000), 130: 551–566. With 5 figures doi:10.1006/zjls.2000.0243, available online at http://www.idealibrary.com on

Growth curve of Psittacosaurus mongoliensis Osborn (Ceratopsia: Psittacosauridae) inferred from long bone histology GREGORY M. ERICKSON1∗ AND TATYANA A. TUMANOVA2 1

Department of Integrative Biology and Museums of Paleontology and Vertebrate Zoology, University of California, Berkeley, CA 94720, U.S.A. 2 Paleontological Institute, Russian Academy of Sciences, Moscow, Russia 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 Psittacosaurus monogoliensis Osborn were examined from a growth series spanning juvenile 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. mongoliensis: (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.  2000 The Linnean Society of London

ADDITIONAL KEY WORDS:—Dinosauria – histology – skeletochronology – growth rings – growth rates – longevity – heterochrony – development – Developmental Mass Extrapolation. CONTENTS

Introduction . . . . . . . . . . Material and methods . . . . . . Histologic sample and techniques . Developmental Mass Extrapolation . Longevity and growth rate calculation Results . . . . . . . . . . . Discussion . . . . . . . . . . Acknowledgements . . . . . . . References . . . . . . . . . .

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552 553 553 554 555 557 561 564 564

∗ Corresponding author. Present address: Dept Biological Science, Conradi Bldg., Dewey Street and Palmetto Drive, Florida State University, Tallahassee FL 32306, U.S.A. Email: gerickson@bio.fsu.edu 0024–4083/00/120551+16 $35.00/0

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 2000 The Linnean Society of London

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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 lguanodon anglicus Holl, Hyaelosaurus armatus Mantell, Megalosaurus bucklandii Rutgen, Pelorosaurus 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 (Ricqle`s, 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 (Buffreńil, Farlow & Ricqle`s, 1986), phylogenetic affiliations (Berreto et al., 1993) and aspects of metabolism (Ricqle`s, 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; Ricqle`s 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 & Hill, 1987). The timing, sequence, and types of such changes often differ between elements within individuals (Ricqle`s, 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 find that morphological changes through ontogeny have effaced growth lines used to directly age specimens (Horner, Padian & Ricqle`s, 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 Ricqle`s 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 Troodon formosus Leidy 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 excelsus Marsh (Curry, 1998) and the hadrosaurid Maiasaura peeblesorum Horner et Makela (Ricqle`s, 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, Psittacosaurus mongoliensis Osborn from the Late Cretaceous

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T 1. Specimens of Psittacosaurus 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 PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN PIN

1369/1–11/1948 698/1977 698/15/1977 1369/1–11/1948 698/5–3/1946 698/4–22/1946 698/7–4/1946 698/1977 698/15/1977 698/2–2/1977–15 698/1977 698/1977 698/4–22/1946 698/1946 698/1977 698/2–2/1977–15 698/5–9/2/1946

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

aptian/albian 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. mongoliensis 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,

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turtles, lizards, and triconodont mammals (Kalandadze & Kurzanov, 1974; Novodvorskaya, 1974; Shuvalov, 1974; Barsbold & Perle, 1983). Humeri, femora, and tibiae from P. mongolienesis were 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 m thickness using a rotary lap grinder and descending grades of silica-carbide sandpaper (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× 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 P. mongoliensis 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

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T 2. Developmental mass extrapolation

Growth Stage

A B C D E F G

Est. age (yrs)

Femur length (cm)

Cube of femur length (cm3)

3 4 5 6 7 8 9

7.6 9.8 11.2 14.8 16.0 20.0 21.0

439 941 1405 3242 4096 8000 9261

% of Adult femur cubic length 4.7 10.2 15.2 35.0 44.2 86.4 100.0

Est. body mass (kg)

Α Mass from previous stage (kg/yr)

Α Mass per day from previous stage (g/dy)

Α Mass per day from regression equation for Fig. 4 (g/dy)

0.94 2.03 3.02 6.96 8.79 17.16 19.87

— 1.09 0.99 3.94 1.83 8.37 2.71

— 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 P. 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, 1984]) 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 (l3) for each specimen (femoral length scales isometrically to the >0.33 power during ontogeny in the extant archosaurs-crocodilians [Dodson, 1975] and birds [Carrier & Leon, 1990]) 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 P. mongoliensis growth stages (stages A–G, Table 2). Longevity and growth rate calculation Growth lines in the P. 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., 1990] 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-Vieillot et al., 1990; Castanet et al., 1993; Castanet, 1994].) 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

Figure 1. Psittacosaurus mongoliensis long bone thin sections. Each section spans nearly or entirely from the endosteal medullary (concave) surface of the diaphysis to the periosteal (convex) surface of each bone. The sections are viewed in the transverse plane with polarizing light microscopy. Note the excellent resolution of vascular canal branching patterns (black) and growth line annuli (arrows) A, figure of typical juvenile P. mongoliensis long bone (Tibia, stage A). The periosteal surface is on the left. The plate 1.75 mm in width. B, figure of typical intermediate growth stage histology of P. mongoliensis long bones. (Tibia, stage E). The plate spans 5 mm from the medullar cavity (lower right) to the periosteal surface (upper left). Note that expansion of the medullar cavity (lower right) has eroded previously deposited longitudinally vascularized bone and annuli as seen in A (above). Such activity necessitated the use of backcalculation to age the specimens. C, figure of highly vascularized bone seen late in P. mongoliensis ontogeny. The plate spans 5.3 mm from the medullar cavity (lowermost right) to the periosteal surface (uppermost left). Note radially vascularized bone that formed the final growth zone (upper left).

556 G. M. ERICKSON AND T. A. TUMANOVA

PSITTACOSAURUS MONGOLIENSIS GROWTH

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expansion were backcalculated using the methods of Castanet & Cheylan (1979) and Chinsamy (1990, 1993). To assess growth rates for P. mongoliensis, 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 aptian/albian 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 to scaling 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 P. mongoliensis 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, [sensu Pritchard, 1956]; 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 collectively run in parallel; sensu 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, sensu 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 (sensu Ricqle`s, 1975).

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Figure 2. Common histologic types in long bone diaphyses of Psittacosaurus mongoliensis 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 1.0 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 (>8 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

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Medullar cavity expansion had eďŹ&#x20AC;aced 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 Aâ&#x20AC;&#x201C;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 diďŹ&#x20AC;erences in vascular canal branching patterns occurred in P. 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 P. monogoliensis 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; Ricqle`s 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 P. 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 [lamellae] 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.

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Humeri

Femora

Tibiae

Age

Growth Stage

Legend

na Longitudinal vascularization

Radiating Reticular Radial Specimen reticular vascularization vascularization unavailable vascularization

Inferred from later stages

Figure 3. Diagram depicting changes in diaphyseal vascularization patterns during ontogeny for various major long bones in Psittacosaurus mongoliensis 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 â&#x20AC;&#x2DC;annualâ&#x20AC;&#x2122; 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, sensu Castanet, 1994). The vascularization patterns 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 diďŹ&#x20AC;ered 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).

PSITTACOSAURUS MONGOLIENSIS GROWTH

561

Body mass (kg)

25.2

Mass = (1+e

–0.74 (Age–7.33)

)

15 R2 = 0.983 10

Age (years)

Figure 4. Life history curve for Psittacosaurus 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 P. mongoliensis (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 (Ricqle`s 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 P. mongoliensis 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 P. 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 (Ricqle`s 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; Ricqle`s et al., 1983, Castanet et al., 1996), it would

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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 P. mongoliensis 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 P. mongoliensis was S-shaped or idealized (sensu 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 (sensu Sussman, 1964). The lag phase is followed by a sustained rapid growth period known as the logarithmic or exponential stage (sensu 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 (sensu 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 P. mongoliensis of up to 2.6 g/day between ages 3 and 4, increasing up to 12.5 g/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 P. mongolienis (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 P. mongoliensis 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 P. 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 P. mongoliensis reached somewhat larger sizes given the incomplete plateauing of the

PSITTACOSAURUS MONGOLIENSIS GROWTH

Altricial birds Eutherians Precocial birds Marsupials

1000 Maximal growth rate (grams/day)

563

100

Reptiles P

10.0

Fish 1.00

0.10

0.01

100

10 k 1000 100 k 1000 k Adult body mass (grams)

Figure 5. Growth rate for Psittacosaurus mongoliensis 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 P. mongoliensis (12.5 g/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 3.3â&#x20AC;&#x201C;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 P. mongoliensis 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 (BertalanďŹ&#x20AC;y, 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.

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This paper is but one of many demonstrating the utility of histological analyses for interpreting paleobiological and/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 P. mongoliensis 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 Ricqle`s, K. Padian, J. Horner, Y. Norpchen, S. Yerby, G. Beapre´ , Y. Katsura, D. Varricchio, K. Chin, K. Middleton, S. Gatesy, and P. Sereno.

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