Paleobiology, 25(3), 1999, pp. 295–304
Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology John R. Horner, Armand de Ricqle`s, and Kevin Padian
Abstract.—Twelve different bones from the skeleton of the holotype specimen of the hadrosaurian dinosaur Hypacrosaurus stebingeri were thin-sectioned to evaluate the significance of lines of arrested growth (LAGs) in age assessments. The presence of an external fundamental system (EFS) at the external surface of the cortex and mature epiphyses indicate that the Hypacrosaurus specimen had reached adulthood and growth had slowed considerably from earlier stages. The number of LAGs varied from none in the pedal phalanx to as many as eight in the tibia and femur. Most elements had experienced considerable Haversian reconstruction that had most likely obliterated many LAGs. The tibia was found to have experienced the least amount of reconstruction, but was still not optimal for skeletochronology because the LAGs were difficult to count near the periosteal surface. Additionally, the numbers of LAGs within the EFS vary considerably around the circumference of a single element and among elements. Counting LAGs from a single bone to assess skeletochronology appears to be unreliable, particularly when a fundamental system exists. Because LAGs are plesiomorphic for tetrapods, and because they are present in over a dozen orders of mammals, they have no particular physiological meaning that can be generalized to particular amniote groups without independent physiological evidence. Descriptions of dinosaur physiology as ‘‘intermediate’’ between the physiology of living reptiles and that of living birds and mammals may or may not be valid, but cannot be based reliably on the presence of LAGs. John R. Horner. Museum of the Rockies, Montana State University, Bozeman, Montana 59717-0040. E-mail: jhorner@montana.edu Armand de Ricqle`s. E´quipe Formations Squelettiques, URA CNRS 11 37, Universite´ Paris VII, 75251 Paris cedex 05, France and Colle`ge de France, Paris, France Kevin Padian. Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720-3140 Accepted:
13 April 1999
Introduction Bone histology is increasingly used to gain insights into the biology of Mesozoic vertebrates (recent reviews in Reid 1997a,b,c). Issues such as individual age, skeletal maturity, growth rates, seasonality of bone deposition, and broad ecological considerations can be illuminated by paleohistological study, especially in connection with experimental studies of living animals (e.g., Ricqle`s et al. 1991, 1998; Castanet et al. 1993; Curry 1998, in press; Horner et al. in press). This line of inquiry assumes the actualistic hypothesis that types of tissues and rates of deposition were generally similar and therefore comparable in extant and extinct organisms. Issues of physiology and behavior are obviously more complex and must be more indirectly approached (Ricqle`s 1992; Chinsamy 1994; Chinsamy and Dodson 1995; Chinsamy et al. 1995; Padian 1997a,b; Reid 1997c). Recent discussions of dinosaurian physiolq 1999 The Paleontological Society. All rights reserved.
ogy and behavior have examined the biological meaning of various kinds of growth lines, including lines of arrested growth, growth inflections, and other chronological variations in tissue deposition (recent reviews in Reid 1997a,b,c; Padian 1997a,b). The potential interest of the use of lines of arrested growth in both biology and paleontology was first demonstrated by the pioneering work of Peabody (1961), who used it to suggest applications to issues of growth and even thermophysiology. From his seminal work, a variety of basic and applied uses of these structures for skeletochronology, summarized by Castanet et al. (1993), has developed in fields as diverse as developmental biology and conservation biology. Because most studies of dinosaur bone histology, including the classic work of Enlow and Brown (1956, 1957, 1958), have been based on isolated sections of bone, it has been difficult to gain a comprehensive view of ske0094-8373/99/2503-0002/$1.00
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letochronology in dinosaurs, or to form and test generalizations about their growth (Horner et al. in press), even though growth marks have been extensively studied in living vertebrates (e.g., Castanet et al. 1993). To address this problem, we have organized a series of studies that assess histologic variation throughout a variety of bones in the skeleton, and through a series of growth stages where possible. Our study of Maiasaura peeblesorum (Ricqle`s et al. 1998; Horner et al. in press) uses elements from six growth stages of a variety of individuals. Although our histological results were consistent for bones within respective growth stages, most of these bones were not associated with others in the same skeleton because most of the sample was taken from a bone bed. Therefore the relative sizes of bones, their stage of histological development, and potential indications of skeletal growth and age had no external control. In this paper we test the generalizations about skeletal growth and timing based on the Maiasaura specimens by studying a range of bones in a single individual: the holotype of the hadrosaurid Hypacrosaurus stebingeri. We assess variation in tissue type, progression of osteogenesis, and distribution of features that are generally held to be related to skeletochronology, such as lines of arrested growth (LAGs). General Histological Description Transverse thin-sections of cortical bone were taken from twelve different skeletal elements of the holotype specimen (MOR 549; see Table 1) of the Late Cretaceous hadrosaurid Hypacrosaurus stebingeri (Horner and Currie 1994). Femoral length of this individual is 102 cm. We sectioned long bones through midshaft, unless otherwise noted, and took a longitudinal thin-section through the metacarpal to assess growth stage and conditions at the growing surface of the long bones. The thinsections were processed according to standard techniques (e.g. Ricqle`s and Bolt 1983; Wilson 1994). The sampled bones reflected a generally similar sequence of development (Horner et al. in press), with bone-specific differences generally attributable to growth dynamics, size, and mechanical function in the skeleton, as discussed below.
TABLE 1. Selected bones of the holotype of Hypacrosaurus stebingeri (MOR 540), indicating minimum and maximum number of lines of arrested growth (LAGs) counted in the cortex under microscopic examination, plus minimum and maximum numbers of ‘‘incremental lines’’ (which may or may not record temporal cycles) counted in the external fundamental system (EFS). Element
Scapula Radius Metacarpal Femur Tibia Fibula Metatarsal Pedal phalanx Rib Caudal chevron Neural spine Ossified tendon
Min cortex
Max cortex
Min EFS
Max EFS
5 5 0 6 7 5 2 0 5 6 3 6
6 7 1 8 8 7 6 0 6 6 4 6
2–3 2 3–4 1 1 1 4 0 3 3 2 3
6–8 7–8 7–8 1 2 4–5 10 0 5 5 3 5
General Osteohistogenesis.—In a cross-section of a typical long-bone shaft of this apparently adult individual, the medullary cavity contains a secondary cancellous spongiosa, often well marked outwardly by an endosteal margin with extensive erosion cavities lined by secondary bony trabeculae (Fig. 1A). Primary periosteal bone of the reticular type, which predominates in some elements (e.g., tibia, Fig. 1B), still sometimes composes the deep cortex; in other elements, however (e.g., metacarpal, Fig. 1C), it has been nearly completely replaced by dense Haversian bone tissue (secondary osteons). Toward the middle cortex the primary fibro-lamellar bone is generally of the plexiform or laminar types, with or without numerous radial vascular canals, respectively. Similarly, the outer cortex may be subplexiform, with few radial canals, to laminar, with none. As with the internal cortex, dense Haversian tissue generally invades the outer cortex, but it is not as well developed as in the deep cortex, where most primary structures may be completely obliterated. In some regions, localized ‘‘spurts’’ of dense Haversian bone may completely invade the external cortex, while neighboring regions remain primary in structure (Fig. 1D). The outermost periosteal layers frequently constitute an external fundamental system (EFS; see Cormack 1987) of generally pseudolamellar tissue with coarsely parallel-fibered, longitudinally ori-
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ented collagenous fibers. In this almost avascular bone, only a few secondary osteons may be present (Fig. 1E). Variations in these histological features may be traced to the individual bone and its overall size. For example, the tibia is less highly reconstructed than the fibula; small bones such as metapodials and phalanges tend to be more reworked and sometimes more compact in structure than larger ones (Horner et al. in press). The internal spongiosa of both the chevron and metacarpal contain large erosion rooms but no marrow cavity. Secondary osteons reach the edge of the external cortex in the metacarpal, but this is far less pronounced in the femur and tibia. Lines of Arrested Growth.—We counted the numbers of lines of arrested growth (LAGs) in twelve skeletal elements of Hypacrosaurus stebingeri. This individual is ostensibly an adult in which growth has slowed and almost ceased, as demonstrated by the presence of the EFS (Fig. 1E) in most bones (Cormack 1987). The structure of the epiphyses (Fig. 1F) observed in longitudinal sections is consistent with this inference (Ricqle`s 1979). Because the bone deposited during earlier stages of growth has been destroyed by its relocation within the present medullary cavity, or by secondary reconstruction in more external regions, a complete sequence of growth lines cannot be recovered from any single bone. Additionally, dense Haversian bone has replaced most tissue in the internal cortex of many bones and often extends into the most superficial cortex, obliterating the primary structures that were once present. As a result, it is difficult to count LAGs in many parts of the skeleton, and then only if tissues are carefully traced through the full circumference of the bone. We did not include apparent growth lines within the EFS for reasons discussed below, but we did count the line at the base of the EFS as the most external LAG. Our results are given in Table 1. They are separated into four categories because LAGs and other lines of inflection of growth are differentially visible depending on the scale at which they are viewed. Minima and maxima are reported for microscopic observations of different magnifications, all using transmitted
light. Typical LAGs were counted in the cortex, and structures in the EFS, which may or may not represent true LAGs, were considered separately because they were often difficult to trace and were locally variable. As the table shows, there was substantial variation in the number of LAGs in the cortices. Up to six LAGs could be counted in the scapula, at least five and as many as seven in the radius, only one in the metacarpal, six to eight in the femur, seven or eight in the tibia (Fig. 1G), six in the metatarsal (Fig. 1H), five to seven in the fibula, six in the rib, caudal chevron, and ossified tendon (Fig. 1I), and three to four in the neural spine. One to eight lines could be counted in the EFS of various parts of bones, but these were locally variable. Independent of the LAGs, the largest bones, such as the femur and tibia (which are also those least affected by Haversian reconstruction), show concentric ‘‘cycles’’ superimposed on the cortex that are visible even to the naked eye. These cycles appear to be linked to slight modulations in density, diameter, and width of vascular canals and laminae in the tissues forming the cortex (Ricqle`s 1983; Horner et al. in press). Earlier, preliminary observations of the same material (Horner et al. 1997; Padian 1997a; Ricqle`s et al. 1997) reported numbers of LAGs that differ somewhat from those presented here, and these discrepancies reflect the practical difficulties of counting LAGs objectively. LAGs in the EFS were not always excluded in some counts; in the standardized count presented here, the outermost LAG is the one at the base of the EFS, when present. To standardize these counts, we used a range of magnifications, included only lines that could be traced completely circumferentially, and compared and verified counts made independently by each of us individually. Discussion Growth Lines and Age Assessment.—LAGs have long been used in the skeletochronology of ‘‘lower’’ vertebrates because in these living forms growth lines are known to be deposited annually (review in Castanet et al. 1993), and they can be tracked with relative if not always complete confidence throughout the growth of
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FIGURE 1. Histology of Hypacrosaurus stebingeri (MOR 549). A, Transverse section of femur (96-10-F-1B) showing transition between the deep cortex and the medullary cavity with large erosion rooms. B, Transverse section of tibia (96-10-T-2) showing primary periosteal bone of the reticular type in the deep cortex. C, Transverse section of metacarpal (96-10-MC-3) showing dense Haversian Systems within the deep cortex. D, Transverse section of fibula (96-10-FIB-2) showing a local region of primary tissue that has been invaded by Haversian Systems. Note that the LAGs (arrows) have been disrupted at this juncture. E, Transverse section of scapula (96-10-SCAP-1) showing the external fundamental system (EFS) at the exterior surface of the cortex (bracketed arrows). F, Longitudinal section of metacarpal (96-10-MC-L2) showing extremely thin coat of calcified cartilage overlying endochondral trabecular
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many bones. In living amphibians and nonavian reptiles, LAGs generally consist of a marked line where growth has ceased (sometimes providing evidence of subperiosteal erosion) plus a band of avascular tissue (the annulus) that sets the LAG apart from the surrounding bony matrix. However, in pterosaurs (Ricqle`s et al. in press) and various dinosaurs (Ricqle`s 1975, 1976, 1979, 1980, 1983; Reid 1981, 1990, 1993, 1996, 1997a; Chinsamy 1990, 1993; Varricchio 1993; Chinsamy et al. 1995; Padian 1997a), LAGs often or usually consist solely of a marked interruption in growth of the typically fibrolamellar matrix, which resumes normal growth immediately thereafter. Sometimes, however, pronounced avascular lamellar tissue can be formed, as Reid (1981, 1997a) has shown for some sauropods and Allosaurus. These LAGs and ‘‘growth rings’’ may well represent annual suspensions of growth, although to date only indirect tests of this hypothesis have been possible, and some apparent LAGs may form for other reasons related to illness, starvation, or temporary stress (Castanet et al. 1993; Reid 1997a; Horner et al. in press). A LAG may not form at all if the local rate of radial bone growth is either too fast or too slow to record it (Ricqle`s 1983; Reid 1997a,b,c). (For example, the femur of a threeyear-old alligator in the collections of the Museum of the Rockies has no growth lines at all, unlike those of feral alligators; it was raised in constant high temperature and with superabundant, high-quality food constantly available). In some cases a discrete LAG is not visible, but an inflection in growth may be seen because of a change either in growth pattern, such as the transition from mostly longitudinal to mostly circumferentially oriented vascular canals or only local changes in the width of laminae, or in the diameter of vascular canals. Such changes, which are modulations of the overall growth as noted above, appear to coincide with LAGs, when they are present. But they may also be distinguished at very
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low magnification when there is no obvious LAG at higher magnification. Discrepancies that we discovered in the number of LAGs that could be counted reliably in various bones of the Hypacrosaurus skeleton led us to reconsider the use and reliability of this method for inferring the age of individual dinosaurs. Ignoring for the present the potential meaning of the lines in the EFS, it would be reasonable to infer from our cortical data (Table 1) that the individual was at least eight years old, because eight is the maximum number of LAGs in a single bone (femur and tibia). However, because of local variations in bone tissue, any other bone or even a different section of the same bone could easily yield a different estimate. Our results suggest, first, that there may not be a single optimal bone to use for dinosaurian skeletochronology, and second, that in such animals, in which early records of growth are reworked and destroyed later in life, an ontogenetic sequence of bones should be used if possible. We have done this for populations of the hadrosaurid Maiasaura peeblesorum using a variety of bones from early nestling through adult stages (Ricqle`s et al. 1998; Horner et al. in press), and Curry (1998, in press) has done so for the sauropod Apatosaurus. Chinsamy (1993) was able to incorporate some ontogenetic control into her studies of femora of the basal sauropodomorph Massospondylus, the basal theropod Syntarsus (Chinsamy 1990), and the ornithopod Dryosaurus (Chinsamy 1995). Rimblot-Baly et al. (1995) used a similar approach to study the humeral growth of a sauropod. In our studies of both Maiasaura and Hypacrosaurus, we have noted extensive variation from bone to bone in the number of LAGs. The femur and tibia show less Haversian reconstruction than other bones and therefore may record LAGs more reliably than other bones. However, we stress the need to use complete growth sequences of multiple elements, working from younger to
← tissue (arrow shows zone of calcified cartilage). G, Transverse section of a portion of the cortex of the tibia (96-10T-2) showing three LAGs. H, Transverse section of rib (96-10-RIB-1) showing five LAGs. I, Transverse section of ossified tendon (96-10-OT-1) showing five LAGs. Scale bar, 4.5 mm for A and G; 1 mm for B, C, D, F, H, and I; 0.4 mm for E.
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older bones in order to avoid as far as possible the need for retrocalculations (see Chinsamy 1993). ‘‘Lines of Arrested Growth’’ in the EFS.—The number of LAGs in the cortex is not consistent among individual bones of the skeleton. We decided to ask whether ‘‘LAGs’’ in the EFS of bones in which growth had already nearly ceased could reflect further deposition of cortical LAGs in bones that had not yet finished growing. If so, addition of cortical LAGs to ‘‘LAGs’’ in the EFS might produce more consistent totals among bones, and hence give a better resolved estimate of skeletal age. The number of lines in the thin sheet of periosteal bone that forms the EFS can also vary considerably (Table 1), even within the periphery of a single section. Objective counting of these lines is difficult because the overall thickness of the EFS may be less than 0.5 mm, and the tissue that forms the EFS naturally induces discontinuities and superpositions (pseudolamellae) that are difficult to distinguish from actual LAGs. We regarded the line at the base of the EFS as the last true LAG. This boundary is also sometimes difficult to assess objectively, because the most external sheets of the ‘‘regular’’ primary cortex tend to comprise less vascularized, more lamellar tissues, like those of the EFS, as growth rates slow. What is the significance of growth lines in the EFS? Experimental data from newts (Triturus) (Francillon-Vieillot et al. 1990) show that at least in this taxon the numerous very thin lines that mark the most external cortex of even tiny long bones (e.g., phalanges) still faithfully record yearly cycles. But these workers also found variation within single bones: numerous thin lines on one side of a bone could coalesce into a single thick one on the opposite side. We have no reason to accept or reject a priori the hypothesis that this is also true for dinosaurs. If such lines within the EFS were indeed annual in dinosaurs, the highest reliably recorded number in each bone should ostensibly be added to the number of years represented by LAGs in the regular cortex. If this is done, however, it is obvious from Table 1 that the signal given by the total number of growth lines distributed among different elements will be more variable than ever. How-
ever, the high variability and inconsistency of the number of growth lines in the EFS among the bones of a single individual suggest caution about interpreting them as annual markers. Like lines of cortical drift and other annuli, they probably reflect mechanical, maturational, or other inflections of growth with perhaps no cyclical regularity. This pattern may vary among taxa and requires further testing. An indirect argument suggests that the highest numbers of growth lines recorded in the EFS may not reflect annual cycles. Several of the largest long bones still have a deep cortex formed of primary tissue. Those that are most extensively remodeled into Haversian tissue often show only a first generation of superimposed secondary osteons. Together, these observations suggest a moderate age for this specimen, with the number of years probably commensurate with the lowest number of lines observed in the EFS plus the maximum seen in the regular cortex. The question remains whether LAGs have any established significance for interpreting the metabolism of extinct dinosaurs. Their occurrence has been used to support a ‘‘dinosaurian’’ physiology different from those of both extant endotherms and ectotherms (Ricqle`s 1983, 1992; Farlow 1990; Rimblot-Baly et al. 1995; Reid 1997a,b,c,). According to Farlow’s hypothesis of dinosaurian metabolism, the bone histology shows that dinosaurs grew faster and at higher sustained rates than living ectotherms, which cannot maintain such growth rates; but as great size is reached, there is less practical difference between endothermy and ectothermy. Farlow predicted that continuously rapid metabolic rates in dinosaurs would be best developed (especially in small-bodied forms) in animals inhabiting high-latitude or thermally seasonal environments. Recent findings concerning the bone histology of ‘‘polar’’ dinosaurs (Chinsamy et al. 1998) and other data appear to be in accordance with Farlow’s (1990) general hypothesis. We concur with such balanced views and wish to go a step further to emphasize an often overlooked fact: the potential to produce LAGs is plesiomorphic for tetrapods. Their
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FIGURE 2. A–C. Histology of the femoral cortex of the elk, Cervus canadensis (MOR-OST-800), showing LAGs at various magnifications (the specimen was stained according to Diane’s Microwave T-blue method, described by Eurell and Sterchi, 1994). Scale bar, 2 mm for A, 0.6 mm for B, and 0.5 mm for C.
presence in non-avian dinosaurs, even in a form not found in other extant reptiles, tends to create an association with extant non-avian (i.e., ‘‘typical’’) reptile physiology that is not warranted by other aspects of bone histology and apparent growth regimes. To the contrary, in view of the relationship of birds to Mesozoic dinosaurs, it appears more appropriate and profitable to emphasize what are clearly derived or even specialized characteristics of non-avian dinosaur bone structures that may ally them physiologically in many respects to living tachymetabolic endotherms, even if these dinosaurs did not have metabolisms exactly like those of extant birds or mammals. To emphasize this point we refer the reader to Fig. 2A–C, which shows a section from the mid-diaphysis of a femur of the extant elk, Cervus canadensis, from Montana. This bone clearly has three LAGs like those seen in the midcortex of the femur and tibia of Hypacrosaurus. Other mammals also have LAGs (see also Klezeval’ and Kleinenberg 1967; de Buffre´nil 1982; Chinsamy et al. 1998) and yet unquestionably remain endothermic homeotherms. If some living endothermic mammals
have LAGs like those of dinosaurs, and if some dinosaurs lack LAGs as most mammals do, of what use are LAGs for supporting inferences of an ‘‘intermediate’’ metabolic status? Reid (1997c) has made a reasoned and wellintegrated case that in many physiological and metabolic effects, dinosaurs were not at all like extant reptiles; nor do any features of their osteological remains suggest ectothermic metabolism. We agree with nearly all of Reid’s observations and inferences, which are also consistent with those of Farlow (1990). However, we still find confusing the phraseology that dinosaurs were ‘‘intermediate’’ in their physiology between typical reptiles on the one hand and birds and mammals on the other, possibly because of the connotations of the word ‘‘intermediate’’ and the expression ‘‘failed endotherms,’’ which Reid (1997c: p. 471) explains ‘‘started on the road to endothermy but never attained it through opting for bulk as their main means of stabilizing temperature.’’ Basal dinosaurs, however, were not especially large. We agree that Mesozoic dinosaurs were not exactly like living birds and mammals, physiologically (and, perhaps, neither were many Mesozoic birds and mam-
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mals). But it is important to specify which birds and mammals and what physiological respects are being compared. In today’s birds and mammals there are substantial ranges of basal metabolic rates, activity levels, and homoiothermy: the echidna, for example, does not maintain a body temperature nearly as constant as that of the cat (Ostrom 1980, fig. 1), and no one would regard many aspects of the metabolic strategies of bats, cheetahs, and whales as comparable, for many obvious reasons. Non-avian dinosaurs, as Farlow (1990) and Reid (1997c) concur, had a range of adult sizes and growth strategies, and they all seem to have grown much faster than typical reptiles, no doubt in part as a result of a double-pump cardiac system and advanced respiratory structures. We see no reason to conclude that these dinosaurs were not as diverse physiologically as mammals and birds are. But can their bone growth provide any conclusive insights on this question? Reid (1997c: p. 468–471) first rejects the view that dinosaurs could not have been endothermic, because they clearly grew so quickly, and he correctly concludes on the other hand that this is not in itself an argument for endothermy. We agree that it is important to distinguish between basal and activity metabolic levels, and that it is unlikely that the former (which is the key factor here) will be measurable in extinct animals. But absence of evidence is not evidence of absence. Reid proposes two indirect indications of the ability to maintain high steady temperatures at small sizes. First is the presence of external, actively regulated insulation. Archaeopteryx aside, the increasingly wider phylogenetic distribution of epidermal feathers and ‘‘proto-feathers’’ in theropods (Padian 1998) may be an indication of this sort of homeothermic capacity (conversely, elephants and humans have little or no fur, even when young). Second is the distribution of bone tissue types in individuals from different climatic regimes. Since Reid’s paper appeared, Chinsamy et al. (1998) have shown that hypsilophodontids from Cretaceous polar regions lack growth rings, just like hypsilophodontids from temperate regions (Chinsamy 1995); yet other dinosaurs in both
climates had growth rings in their bones. This appears to imply that the rhythms of bone growth were primarily endogenous and not primarily dependent on environmental variables. So the case for ‘‘intermediacy’’ based on both integument and bone histology may be challenged. In the end, we must regard ‘‘dinosaurs as dinosaurs,’’ as Dodson (1974) said; but this tautology is meaningful only if it is characterized qualitatively. Bone histology indeed suggests that dinosaurs grew much more like mammals and birds than like other living reptiles (Reid 1997c). In some other respects Reid regards them as more like living reptiles than birds and mammals are, but we maintain that these are simply plesiomorphic features of tetrapod bone growth that reflect little of metabolism. We will not have a fair comparison, however, until the evolution of bone histologic patterns in nonmammalian synapsids is better understood. We cannot say that dinosaurs were either ‘‘failed endotherms’’ (Reid 1997c) or ‘‘damn good reptiles’’ (Farlow 1990); they may have been metabolically very much like many birds and mammals, and their bones show histologic patterns and rates of growth that are more consistent with birds and mammals than with any other animals. Conclusions The general distribution of LAGs and other growth cycles in dinosaur bone has long been understood (Reid 1981; Ricqle`s 1983; etc.). But it now seems more complex than previously assumed to assess their general significance and practical utility with respect to skeletochronology and other biological aspects. The differences that can be readily perceived in the number of LAGs among various bones of a single skeleton can be easily explained by bone-specific ontogenetic peculiarities of individual skeletal elements (Castanet et al. 1977). Simply counting growth lines in a single bone now appears to be potentially unreliable, irrespective of other causes of error (Horner et al. in press). Sectioning complete skeletons, especially in a growth series, remains an exceptional opportunity. When this is not possible, the femur and tibia appear to give the most consistent skeletochronological
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results, at least among hadrosaurs, following the reasoning detailed in this paper and in our work on Maiasaura (Horner et al. in press). However, we stress that this statement should not be used prescriptively in the absence of better empirical studies. The presence of LAGs within some mammalian bone tissues and their absence in some crocodilians demonstrate conclusively that these features are independent of the physiological constraints of endothermy and may actually reflect various growth modulations within a homeothermic regime. No features of bone histology preclude Mesozoic dinosaurs from having been endothermic, and no independent evidence suggests or specifies the conditions of ‘‘intermediate’’ physiology that have frequently been suggested. Acknowledgments We are extremely grateful to E. Lamm for the histological preparations and to C. Ancell and P. Leiggi for the physical preparations. Helpful suggestions and critical reviews by R. Reid and A. Chinsamy are also much appreciated. Funding for this project was derived from an National Science Foundation grant (EAR-9219035) to J. R. H. and a grant from The Charlotte and Walter Kohler Charitable Trust. We also acknowledge the University of California Museum of Paleontology (Contribution No. 1686) and the Committee on Research of the University of California, Berkeley. Literature Cited Castenet, J., F. J. Meunier, and A. de Ricqle`s. 1977. L’enregistrement de la croissance cyclique par le tissu osseux chez les Verte´ bre´s poikilothermes: donne´es comparatives et essai de synthe`se. Bulletin Biologique de la France et Belgique 111:183–202. Castanet, J., H. Francillon-Vieillot, F. J. Meunier, and A. de Ricqle`s. 1993. Bone and individual aging. Pp. 245–283 in B. K. Hall, ed. Bone, Vol. 7. Bone growth. CRC Press, London. Chinsamy, A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Paleontologia africana 27:77–82. . 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geology 18:319–329. . 1994. Dinosaur bone histology: implications and inferences. In G. D. Rosenberg and D. L. Wolberg, eds. DinoFest. Paleontological Society Special Publication 7:213–227. . 1995. Ontogenetic changes in the bone histology of the Late Jurassic ornithopod Dryosaurus lettowvorbecki. Journal of Vertebrate Paleontology 15:96–104.
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