15 reproduction in the fast lane: Implications for size, success, and


Abstract sume that were broadly similar to large mam- Large dinosaurs were apparently r-strategy layers mals in population dynamics, genetic information with reproductive outputs much higher than those of K-strategy processing, and vulnerability to disruptive events. For large . Dinosaur populations may have consisted example, Jablonski (1991) lists large size as a possible mostly of posthatchlingjuveniles that were not dependent upon factor in the extinction of the dinosaurs, but also ac- their parents for survival. That dinosaurs grew as rapidly as knowledges that juveniles and small adult forms also mammals suggests similarly elevated metabolic rates. Dinosaur population recovery and dispersal potentials were probably vanished. The apparent fecundity of dinosaurs suggests much higher than those observed in mammals. Low pop- that in some ways their reproductive strategies were ulation levels of adult dinosaurs enabled individual adults to more like those of small mammals rather than large consume relatively large portions of the available resource mammals. The production of many nidifugous juveniles base, thereby becoming larger than mammals. The r-strategy- may help explain how and why dinosaurs often grew to based survival potential of the dinosaurs helps explain their gigantic dimensions and why they were such a stable long period of success, and exacerbates the problem of ex- and successful group for such a long time, and also plaining their final extinction. Some of the problems inherent makes it more difficult to explain their ultimate extinc- in modeling the population dynamics of r-strategy dinosaurs tion. are examined. Much of the data, discussion, and conclusions presented must be considered tentative, and are offered Introduction in the hope of encouraging further consideration on di- Most investigations of the evolutionary forces nosaur size and reproduction. The prefix "rnega-" re- behind the gigantism of some dinosaurs have focused fers to with a body mass of one or more tons. upon the great size of the adults (Figs. 15.1 and 15.2; Dinosaurs are not considered to be in the typ- see also Weishampel & Homer, Chapter 14). Little at- ical sense, and are treated as a separate group to tention has been paid to the fact that even the most better examine reproductive differences. I also assume colossal dinosaurs began as nidifugous hatchlings that dinosaurs reproduced on an annual basis, although no bigger than the . Can hatchling dinosaurs multi-annual and semi-annual breeding cannot be dis- provide clues toward understanding why they so often counted. Because dinosaurs probably grew at rates grew so large? similar to those of birds and mammals (see below), it Large terrestrial mammals are K-strategists that is assumed that their life and reproductive spans were emphasize low juvenile mortality, starvation resistance, also broadly similar to those of birds and mammals of and high dispersal to maintain population levels. As similar mass. shown below, dinosaurs, on the other , were fast breeding r-strategists. The dramatic difference between Reproduction, growth, and recovery these two reproductive strategies was briefly mentioned potential of dinosaurs by Kurten (1953), but was only recently examined in Reproductive method and potential detail by Carrano and Janis (1990), Janis and Carrano Recently, Bakker (1986) has suggested that sau- (1992), and Farlow (1993). ropods gave birth to live young. This hypothesis runs -Many studies of dinosaur extinction tacitly as- contrary to the evidence of sauropod , , Figure 15.1. Size comparisons of giant continental dinosaurs, mammals, and reptiles drawn to the same scale, Extinct taxa based on largest known specimens, and masses from volumetric models. Extant and recent taxa based on large adult males. A. 60- to 80-(on titanosaur (Bonaparte, 1989). B. 55-(on . C. 45-ton (= ). D. 13-ton . E. 6-too . F. 7-too . G. 16-(on Indricotherium. H. 2-(00 . I. 5-100 Megacerops. J. 10-too Mammuthus, K. 6-(00 Loxodonta, L. 0.3-100 Panthera. M. I-ron Scu/osaurus. N. I-ron Megalania. Human figure 1.62 m tall. Scale bar = 4 m. '- Figure 15.2. Brachiosaurus brancai as a representative of large dinosaurs. Size distribution based on associated parallel sauropod trackways, and includes a few large adults, some subadults, and juveniles. Size of juveniles is believed to be the minimum size able to keep up with the . Dinosaur reproduction in the fast lane 247 and hatchlings (Fig. 15.3; Erben, Hoefs, & Wedepohl, one or two dozen eggs or nestlings. These numbers sug- 1979; Mohabey, 1987; Cousin et al., 1989; Hirsch, gests that each female laid a dozen eggs, and that two 1989; Paul, 1991; Moratalla and Powell, Chapter 3; dozen eggs represent the output of two females (Homer, however Jain, 1989,disputes Mohabey's report of a sau- 1987). ropod hatchling). Allknown dinosaur eggs had hard cal- cified shells, and it is possible that this barred Small theropod a shift to live birth (Packard, 1977). If this is true, then Egg clutches have been questionably assigned to dinosaurs must have been oviparous. , a small 50-kg theropod (Homer, 1987; Hirsch Prosauropods, small to large theropods, small or- & Quinn, 1990). The clutches contain two to three pairs nnhopods, some hadrosaurs (such as ), and of eggs a linear row. Four eggs is considered to repre- small ceratopsians had egg volumes of 0.1 to 0.5 L sent the minimal reproductive potential. It is possible (Case, 1978b; Homer & Makela, 1979; Homer, 1987; that multiple clutches were deposited. Homer & Gorman, 1988; Homer & Weishampel, 1988; Winkler & Murry, 1989). Eggs of the hadrosaur Hypa- crosaurus were more volurnous at 4 liters (Homer and I follow Thulborn (1991) in assigning clutches of Currie, Chapter 21), while those assigned variously to about 18 eggs to this -80-kg ceratopsian. iguanodonts and to sauropods were 2 to 3 liters in vol- ume (Case, 1978b; Cousin et al., 1989; Dodson, 1990). Hadrosaur Reproductive rates for five types of Late Creta- Nests of Maiasaura and are ceous dinosaurs can be determined. These are hypsilo- known for these 2,000 to 2,500-kg hadrosaurs. There phodontid iOrodromeus and an unnamed from are between eighteen and twenty-four eggs in a clutch Proctor Lake, Texas), small theropod (?Troodon), cer- (Homer & Makela, 1979; Homer, 1982, 1984, 1987; atopsian (Protoceratops), hadrosaur (Maiasaura and Homer·& Gorman, 1988; Homer & Weishampel, 1988; Hypacrosaurusi, and sauropod (). Coombs, 1989, 1990; Hirsch & Quinn, 1990; Horner and Currie, Chapter 21). The modest volume of these Hypsilophodontid eggs (5 to 100 liters) relative to the size of the adults Nests are known for the small -40-kg Orodro- suggests that one female laid all the eggs in a . meus and Proctor Lake hypsilophodontid (Homer, 1982, 1984, 1987; Homer & Gorman 1988; Homer & Weis- Sauropod hampel 1988; Coombs, 1989, 1990; Winkler & Murry, Large arcs of eggs have been identified as Hyp- 1989; Hirsch & Quinn, 1990). The nests contain either selosaurus (Case, 1978b; Hirsch, 1989; Cousin et al.,

Figure 15.3. Small size of dinosaur hatchlings (3 kg titanosaur sauropod hatchling shown here) made possible large clutch sizes and high reproductive rates that rendered even the largest dinosaurs r-strategists with exceptional population recovery and dispersal potential. I,

Gregory S. Paul 248

1989, Chapter 5; Dodson 1990; Vianey et al., Chapter hatchlings may have been display characters designed 11). This sauropod is poorly known, but the adult mass to invoke parental care. Certainly hadrosaur hatChlings is believed to be about 5000 kg. The arcs contain up to appeared to have been nest bound and dependent upon fourteen eggs, and this is taken as the minimum poten- their parents for 1 or 2 months (Horner & Makela, 1979; tial reproductive output of the sauropod. Case (l978b) Horner, 1982, 1984; Horner & Gorman, 1988; Homer suggested a maximum of 100 eggs per individual, a & Weishampel, 1988; Coombs, 1989; Lambert, 1991). number that is reasonable for an of this size. Trackway and -bed evidence indicate that In Figure 15.4 the estimated breeding rates for young dinosaurs did notjoin with adults until they the dinosaurs just discussed is compared to the known were sufficiently large enough to keep up. The minimal rates of extant female . In extant taxa with an sizes of juveniles in mixed size herds are the follow- adult mass of I g to \0 kg, the annual number of young ing: sauropods, over one third adult size (Fig. 15.2, produced is broadly similar in both egg layers and live , 1985; Farlow, Pittman, & Hawthorne, \989); bearers. Above 10 kg the number of young of the two hadrosaurs, nearly one half adult size (Homer & Gor- types diverge significantly, with many oviparous taxa man, 1988); ceratopsids, one fifth adult size (Currie & being much more prolific than mammals. This diver- Dodson 1984); , one quarter 'adult size gence is mainly due to a decline in fecundity in mam- (Thulborn & Wade, 1984). Before joining the herds, the mals with a mass of over 5 tons. young may have formed into pods that were either in- Dinosaur reproduction is essentially an extension dependent or under the care of one or more adults (Hor- of the reptilian-avian pattern, with many eggs produced ner & Makela, 1979; Homer & Gorman, 1988; Forster, as part of an r-strategy mode of reproduction. Small di- 1990; Lockley, 1991). Pod behavior in some theropods nosaurs had reproductive potentials overlapping those of may be seen in juvenile trackways that are not in as- both viviparous and oviparous animals. The annual re- sociation with the tracks of larger adults, suggesting that productive output of herbivorous dinosaurs equals or ex- the youngsters were independent (Bird, 1985; Lockley ceeds that of , lagomorphs, and other small 1991). mammals, and was much higher than that of large her- As these young became less dependent upon the bivorous mammals. parents, they were able to meet their own food, ther- Reproductive potential over a lifetime can also be moregulatory, and defensive requirements which may compared. For example, female between age have differed significantly from those of the adults. In ten to fifty produce about a dozen young (Owen-Smith, these respects dinosaurs were like typical reptiles in that 1988). During the same 40- interval, a sauropod by pursuing a distinctly different niche, the juveniles could. have produced 5004,000 eggs. Reproductive avoid competing with and being a burden upon their rates for dinosaurs and mammals also scale differently. parents. Large mammals breed less rapidly than small mammals (Western, 1979; Eisenberg, 1981; Owen-Smith, 1988). Rates of growth In dinosaurs, however, reproductive rates remain con- Juvenile dinosaurs grew rapidly at rates compa- stant or increase with size. This conclusion is similar to rable to those of birds and mammals (Ricqles, 1980; that of Janis and Carrano (1993) that the reproductive Currie, 1981; Bakker, 1980, 1986; Currie & Dodson, output of large mammals diverges from that of large 1984; Paul, 1988b; Reid, 1990; Dunham et aI., 1989; dinosaurs. Russell, 1989; Farlow, 1990; Lambert, 1991; Leahy & Dinosaurs could breed every year or two, replac- Paul, 1991; Chinsamy, 1992; Varricchio, 1992). Rates ing clutches that were destroyed. Female mammals with of growth are plotted in Figure 15.5. The very rapid a mass over 10-100 kg are constrained by the long ges- growth of hadrosaur nestlings matches the highest rates tation period or time spent by the progeny in a pouch in altricial bird nestlings. These rates, as well as those or nursing. Weaning takes 3-12 months in most ungu- of extant birds, show that lactation is not a prerequisite lates, 2-3 in megaungulates, and 3-\8 months in for high rates of growth (contra Pond, 1983). Instead, large marsupials (Langman, 1982; Owen-Smith, 1988; high minimal and maximal metabolic rates are required Nowak, 1991). Therefore, most cannot reproduce faster (Case, I978a; "Leahy & Paul, 1991). The gap between than once every year; megamammals are limited to re- the growth rates of terrestrial reptiles and mammals in- producting every 2 or more years. . creases with increasing size! This fact contradicts the possibility that the growth rates of gigantic ectothenTIS Parental care and feeding of juveniles converge with those giant endothenns. The amount of parental care given by dinosaurs appears to have varied widely, from wholly dependent Aduitljuvenile population ratios and total (precocial) nestlings to fully independent (altricial) populations hatchlings (see Paul, Chapter 18). Richmond (1965) suggested that the scarcity of Bomer (1988; Homer & Gorman, 1988) has sug- juvenile dinosaur reflected a reptilian pattern of gested that the short, "cute" snouts of altricial dinosaur high juvenile mortality and slow growth. In point of Dinosaur reproduction in the fast lane 249

fact, juvenile dinosaurs are abundantly represented in of modem megaherbivores, and 45-55 percent of grow- the fossil record (Dodson, 1975 Carpenter, 1982). Up to ing populations. (Owen-Smith, 1988). Among carni- 80 percent of the dinosaur skeletal remains in the Two vores, adults form 40-85% of the populations (Kruuk, Medicine Formation are of juveniles less than half adult 1972; Schaller 1972). size (Homer & Makela, 1979). The high percentage of young individuals in the Two Medicine Formation is not Population expansion, dispersal and recovery abnorrnal, based on the many eggs laid by female di- potential nosaurs. In fact, adult/juvenile population ratios should In stable populations of r- and K-strategy ani- be skewed towards younger age classes. Support for mals, reproductive rates tend to be balanced by juvenile such a prediction is available from the abundant track- mortality (Colinaux, 1978). The differences between the way data of Texas and Korea (Lockley, 1991, Chapter two reproductive strategies become more apparent when 23). the populations are less stable due to decreased .corn- The adult/juvenile ratios of dinosaurs stand in petition (e.g., availability of a new ) or a popu- marked contrast with those of K-strategy mammals. Ma- lation decrease of predators. K -strategists produce few ture adults make up 60-70 percent of stable populations offspring; therefore, maximum rates of population

Figure 15.4. A. Annual reproductive potential as a function of body mass in living and recent vertebrates and dinosaurs. B. Same data reorganized to compare oviparous and oviviviparous taxa with viviparous taxa and dinosaurs. Reproductive potential is measured in terms of total egg or newborn production (marsupials newborn based on available number of teats). Ranges of reproductive potential are plotted except for unusually extreme values in mammals, and domestic and captive animals. Most living groups enclosed in least area polygons, except nonpredaceous 3- to 4O-kg marsupials which all fall upon the single line indicated. Symbols and abbreviations: small open circles, continental (rhea, emu, cassowary, and ostrich); circles with dots, island ratites ( and ); small solid circles, ; large solid circles, sauropod (Hypselosaurus); large heavy circles with dots, hadrosaurs (Maiasaura and Hypacrosaurus); large half solid circles, Protoceratops; large light circle with heavy dot, hypsiiophodonts and the theropod Troodon. ae, African elephants; br, black rhinoceros; ce, cetaceans; cv, ; s. giraffes; H, humans; h, hippopotamus; hm, herbivorous marsupials; ie, Asian elephants; in, insectivores; ir, Indian rhinoceros; la, lagarnorphs; mo, monotremes: pm, predaceous marsupials; reptiles. sphenodonts, , . . and crocodilians; ro, rodents; st, marine turtles; SU, suids; ug, ; wr, white rhinoceros. Data from Austin and Singer (1971), Grzimek (1972), Porter (1972), Ellis (1980), Nowak (1991), Campell and Lack (1985), Perrins and Middleton (1985). Seymour (1991), data for moas from Anderson (1989). reptiles --...., 100 -st ro,

; UJ ><-, (9 A z a: O·rOO:::I~__ O::.~O_=:.=...01=.1 ====I.O~==='O===='O:;:O:::::::::l:.:'O;O:.:O~=~'O::O::;:O::::O~-..:I:::O:::OO::;.O:::Ol O--IOO~ ~ LL ------...... -dinosaurs o -...... -...... 10 ( <, marsupials & -_ -...... -...... placentals ---- -...... ~ I.Or------_,.....:.::-::::::-::::.:::= ./ <, rePtiles,bird~& monot;;'es --______-':) B ------BODY MASS kg Gregory S. Paul 250 growth remain low even when juvenile mortality is re- are hypothetically possible. In reality, high egg and ju- duced. In contrast, the population of r-strategists can venile mortality prevented this from happening. grow much more rapidly when many juveniles survive. The hypothetically high replacement rates of di- High rates of growth to sexual maturity increases the nosaurs suggests that juvenile (post-nestling) dinosaurs intrinsic rate of natural increase (McNab, 1980) could replenish decimated population levels to their for- Megamammals (giraffes, , hippopot- mer levels relatively fast, even if all the adults had been omuses, and elephants), which are K-strategists, are.lim- killed off! In this, megadinosaurs may have been better ited to annual population expansions of only 6-12% by suited than megarnarnmals to rebounding after dcvas. their maximum reproductive rates and minimal juvenile tation of their populations. mortality rates (Owen-Smith, 1988). For this reason, at the beginning their population growth curves are rather shallow (Colinaux, 1978). Megadinosaurs, on the other ReprOduction: key to the large size and hand, had steeper population growth curves because success of dinosaurs they produced many more young. How high the annual Evolving into a large size is a common feature population growth of large dinosaurs might have been among vertebrates (Stanley, 1973). The great size of di- is unknown. Considering how many more potential, nosaurs was remarkable not only because many of them fast-growing young a megadinosaur could produce an- grew' to body sizes unmatched by terrestrial mammals nually than a megamammal, dinosaurian population (Figs. 15.1 and 15.6), but also because they were a very growth rates approaching or exceeding 100% per year successful group for -150 Myr. About three-fifths of the dinosaur species were in the mega-size range (Hot-

Figure 15.5. Growth in grams per day as a function of adult body mass in living vertebrates and dinosaurs. Only terrestrial and freshwater, noncaptive reptiles are plotted. Placental data excludes primates and edentates. Symbols and abbreviations: small solid circle, rnegapode; small open circle, ; large solid circle, subadult sauropod; large solid left half circle, ceratopsian (Monocionius); large circle with black dot, hadrosaur overall growth (Maiasauray; large circle with white dot, hadrosaur nestling growth (Maiasaura); large open circle, prosauropod (Massospondylusy; large solid lower half circle, theropod (Syntarsusy; large solid upper half circle, theropod (Troodon); e, African elephantcow and bull; g, ; h, hippopotamus; r, white rhinoceros. Data from Ricklefs (1968,1973), Case (1978a), Laws (1968), Dagg and Foster (1976), Webb et al. (1978), Chabreck and Joanen (1979); Hillman-Smithet al. (1986), Hurxthal (personal communication), Reid (1981, 1990), Currie (1981), Currie and Dodson (1984), Homer and Gorman (1988), Russell (1989), Chinsamy (1992), Varricchio (1992}, and Paul (unpublished notes).



>-100 ro ~ Cl I 10 I- ~ CC (!J 1.0



0.01 1.0 10 100 1000 10000 100000 BODY MASS kg Dinosaur reproduction in the fast lane 251

ton, 1980). Among ectothenns, the inability to grow r-strategy reproduction allowed them to achieve larger rapidly to maturity may be one reason why they are biomass/area ratios and body sizes than they otherwise limited to adult sizes of about I ton. As Dunham et aJ. could. Nevertheless, the megapredators cannot become (1989) have noted, giant animals must grow rapidly to as large as the megaherbivores because of the latter's reach sexual maturity in a reasonably short time (about broader energy base (various plants). This restricts the tWOdecades). Slow growth, slow generational turnover predators to sizes not exceeding elephantine masses rates, and limited locomotion dispersal may inhibit even (Farlow, 1993). fast-breeding reptiles from exceeding 100 kg, and any The reproductive strategy of the dinosaurs also reptiles from breaking the I-ron barrier. has implications for predator/prey ratios. Much of the Dinosaurs were able to evolve large sizes because mortality due to by megapredators of their high and r-strategy reproductive probably occurred among one-third to half-grown ju- system. Only a few adults are needed to produce the veniles. With a large portion of the herbivore biomass many juveniles needed to keep the population viable. made up of juveniles, predators can cull a larger portion With fewer adults in the population, each can claim an of the herbivore biomass. If true, it is possible (but not unusually large share of the resource base. This would proven) that predator/prey ratios might be higher (- 1.5- allow the of larger adult body sizes than could 3.0 percent) than are observed in modem communities be reached by high metabolic, K-strategy living of large endothenns (-0.2-1.5 percent, Farlow, 1990). on the same resource base. Any serious depletion of the An "arms race" may have occurred between prey adult population is not critical to the survivability of the and predator dinosaurs. Adult are under se- species as long as enough of the juveniles survive and lective pressure to improve their defensive performance mature to reproduction. to enhance the ability of each adult to protect their own The predatory dinosaurs benefited from the in- high reproductive value. This might entail developing creased size of their prey because their resource base better defensive weaponry or armor, to increasing size, was expanded. This expansion in combination with their or a combination of both. Predators would also increase

BODY MASS tonnes Figure 15.6. Mass ranges over I en ton in continental groups. o ~ Maximum values represent typical large adults for extant groups and sauropods for extinct groups of the largest ornithopods known specimens (either . _ segoosaurs or ). Data in pan from Paul (J988a, 1992). _ ceratopsids _ ankylosaurs

• stegosaurs _ theropods

'- --.JI indricotheres o horned rhinos CJ brontotheres [ I proboscideans o uintatheres o arsinoitheres o pyrotheres o n~toun9Ulates Oedentates o marsupials I carnivores

pareiasaurs tortoises monitors Gregory S. Paul 252 their size to better overcome the prey's defenses. The of the dinosaurs. However, large K-strategy mammals resulting feedback system could result in very large have endured well with the competition from small r- body sizes. strategy mammals. In fact, fast reproduction should have Another possible cause for large adult dinosaur given dinosaurian megaherbivores an even better ability sizes was the sheer numbers of juveniles. Small adult to meet the Challenge posed by the tiny herbivores. dinosaurs could have found themselves facing compet- Another hypothesis attributes the extinction of the itive or exclusionary pressures from large populations dinosaurs at the end of the to the formation of juveniles their own size. Many small dinosaur niches of extensive volcanic traps (Duncan & Pyle, 1988; Of- may, therefore, have been filled by juveniles of larger ficer et aI., 1987; McLean, 1988; Kerr, 1991b; Chatter- species. jee, 1992). The intense volcanism produced extremely Janis and Carrano (1992) conclude that high rates adverse climatic effects and pollution that caused peri- of reproduction, population growth, and population re- odic collapses of the global flora communities. How- covery were important reasons that so many dinosaurs ever, small dinosaur species and the juveniles of larger became so large. In addition, juvenile independence, ge- dinosaur species might have survived to recover along netic flexibility, high rates, and the positive with the fiora> Again, the geneticflexibility of the di- attributes that derive from fast growth and high metab- nosaurs improved the chances of their survivaJ. olism also contributed to their great size and success. Finally, evidence has been growing for the impact of an coincident with the global termination of the dinosaurs globally (Melosh et aI., 1990; Kerr 1991a, Dinosaur reproduction and extinction Izett, Dalrymple, & Snee, 1991; Pope, Ocampo, & During the several events occurred that Duller 1991; Sigurdsson et aI., 1991; Smit 1991; Hil- were potentially lethal to the dinosaurs. Periods of low debrand et al. 1991; Chatterjee 1992). However, the ef- sea level and low topography may have suppressed spe- fects of the impact on the dinosaurs needs to be ciation rates among the dinosaurs and heightened ex- examined in light of the reproductive system of dino- tinction rates via competitive interchange between saurs. faunas and increased disease vectors (Bakker, 1977, Inthe worst case scenario, the impact resulted in 1986). Dinosaurs survived some of these events because a total collapse of the terrestrial , resulting in of the potentially high speciation rate of their r-straregy the death of the dinosaurs (see discussions by Crutzen, reproduction. High rates of genetic processing should 1987; Waldrop, 1988; Paul, 1989; Melosh et al., 1990; have increased the ability of dinosaurs to evolve dis- Kerr, 1991a; Sigurdsson et al., 1991; Smit, 1991; Wolfe, ease-resistent strains. Wildebeest, cape buffalo, and cat- 1991; Hildebrand et al., 1991). Burrowing and fresh- tle had little trouble recovering after the devastating water vertebrates were the least affected, as were many rinderpest epidemic of the 1890s (Sinclair, 1979). The birds (Olson, 1985). faster-breeding dinosaurs should have been even better The survival of the birds after the Cretaceous is able to recover from similar events.. important because they may hold a 'clue to the ways The high rate of genetic processing by the dino- dinosaurs might have been able to resist extinction. saurs should also have enhanced the species' ability to Most birds lay fewer eggs than dinosaurs and are ap- adapt to changing climates and floras. The high repro- parently more sensitive to environmental change than duction and dispersal potential of those din':'saurs that were dinosaurs. It is therefore difficult to understand could' not adapt enabled them 'to shift their populations how birds could have survived the impact but not the to more favorable climes and during the many dinosaurs. If just a few dinosaurs survived the catastro- climatic shifts of the Mesozoic. phe, their rapid reproduction and genetic flexibility It is doubtful that changing climate affected the should have allowed them to reestablish themselves and ability of dinosaur eggs to hatch or skewed the sex ratios adapt to a dramatically altered world. These surviving of the in a dysfunctional manner. Today, birds dinosaurs would have formed the basis of a new dino- and reptiles living in a wide variety of temperature re- saur radiation. That this did not happen is an unsolved gimes are able to maintain the nest temperatures for puzzle. proper egg viability and embryonic sex selection. There The history of the dinosaurs is marked by re- is no reason to suppose that dinosaurs could not also markable success and stability during the Mesozoic. Far have kept the nest temperatures within tolerable limits, from being inherently vulnerable, the dinosaurs survived contrary to the arguments of Erben et aJ. (1979) and in spite of repeated changes in sea level and climate, Paladino et aJ. (1989). After all, dinosaurs successfully enormous volcanic eruptions, and great impacts. Indeed, nested in a variety of different and changing thermal the dinosaurs' fecundity makes it hard to see how such conditions for over 150 Myr. resilent animals could ever have been killed off. The Competition by early ungulates and other small extinction of the dinosaurs was probably not part of the herbivorous mammals has been suggested by Van Valeri normal course of evolutionary fluctuations, nor was it an:I.,S!oan (1977) as a possible cause for the extinction just another result of random extraterrestrial disruptions. Dinosaur reproduction in the fast lane 253

Instead, it remains one of the most extraordinary and Austin, O. L., & Singer, A. 1971. Families of Birds. (New inexplicable events in history. York: Golden Press), Bakker, R. T. 1977. Tetrapod mass - a model of the regulation of speciation rates and immigration by Conclusion cycles of topographic diversity, In A, Hallam (ed.) The last quarter of a century has seen the emer- Patterns of Evolution, (New York: ), pp. 439- gence of a revisionist view that sees dinosaurs as much 68. more like birds and mammals than the typical , ]980. Dinosaur heresy - : why we Dinosaurs are now seen as having been highly active on need endothermic for a comprehensive the- a sustained basis, fast growing, and often possessing ory of bioenergetic evolution. In D. K. Thomas & E. highly developed social and parental skills. A few re- C. Olson (eds.), A Cold Look at the Warm·Blooded searchers have taken this concept to the extreme, sug- Dinosaurs. American Association for the Advancement of Selected Symposium 28: 351-462. gesting that the sauropods dropped live young like the 1986. . (New York: William Mor- giant ungulates. However, a combination of very high row and Company, Ltd.). breeding rates, high genetic turnover, nonlactation, and Bird, R. T, 1985, for Barnum Brown. (Fort Worth: fast growth shows that large dinosaurs were not K- Texas Christian University Press). strategist large mammals. But nor did they have the Bonaparte, J. F, 1989, Un gigamesco titanosauridae de la slow generational turnover rate and short travel range of Formacion Rio Limay (Provincia del Neuquen). Jor- ectothermic reptiles, nadas de Paleontologia de Yertebrados Instead, they enjoyed a remarkable, dualistic sys- 22: 27-9. rem combining features of both r- and K-strategist en- Campell, B" & Lack, E, 1985. A Dictionary of Birds. (Ver- dotherms. They had an r-strategy of reproduction, million: Buteo Books). Carpenter, K. 1982. Baby dinosaurs from the high population growth, rapid recovery rates, dispersal Lance Formation USA and a description of a new performance, and genetic processing usually found in species of theropod dinosaur. University of , much smaller mammals. But they also utilized the K- Contributions to 20: 123-4. strategy of survival, high dispersal performance, rapid Carrano, M., & Janis, C. 1990. Scaling of reproductive turn- growth, and generational turnover rates found in large over in archosaurs and mammals, why are large ter- endothermic mammals. restrial mammals so rare? Journal of Juvenile (post-nestling) dinosaur independence 10 (supplement to No.3): 17A. and the potential ability to survive the loss of all adults Case, T. J. 1978a. On the evolution and adaprative signifi- is a reptilian trait that is shared by a few birds and even cance of postnatal growth rates in the terrestrial verte- . insects. The juveniles may have congregated into large brates. 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