University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln

Papers in the Earth and Atmospheric Sciences Earth and Atmospheric Sciences, Department of

1983 Miocene Burrows of Extinct Bear Dogs: Indication of Early Denning Behavior of Large Mammalian Carnivores Robert M. Hunt Jr. University of Nebraska-Lincoln, [email protected]

Xue Xiang-Xu Northwestern University

Joshua Kaufman Nebraska State Museum

Follow this and additional works at: https://digitalcommons.unl.edu/geosciencefacpub Part of the Earth Sciences Commons

Hunt, Robert M. Jr.; Xiang-Xu, Xue; and Kaufman, Joshua, "Miocene Burrows of Extinct Bear Dogs: Indication of Early Denning Behavior of Large Mammalian Carnivores" (1983). Papers in the Earth and Atmospheric Sciences. 541. https://digitalcommons.unl.edu/geosciencefacpub/541

This Article is brought to you for free and open access by the Earth and Atmospheric Sciences, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in the Earth and Atmospheric Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Fine structure in the occultation signa­ Miocene Burrows of Extinct Bear Dogs: Indication of Early tures of a given parallel ringlet should occur in the same order in p for all Denning Behavior of Large Mammalian Carnivores longitudes, if the orbits are all filled. The entwined model, however, would gener­ Abstract. Partial skeletons offour species of extinct carnivores have beenfound in ally show differences and under particu­ their dens excavated in the floodplain of an early Miocene ephemeral braided stream lar conditions, even a radial reversal. A at Agate Fossil Beds National Monument, Nebraska. Bear dogs (Carnivora: parallel model that is stabilized by self­ Amphicyonidae) were the principal occupants; their den dimensions and body size gravity must have a greater radial width are similar to those of living wolves and hyenas. Discovery of this predator at apoapsis than at periapsis and a char­ community extends the record of denning behavior of large mammalian carnivores acteristic longitudinal reversal in the tilt to the early Miocene, 20 million years ago. of the local plane of the ringlet relative to its average orbital plane. Neither charac­ Relatively complete fossil skeletons of two other individuals, which are not rep­ teristic is known to be required for the mammals preserved directly in their an­ resented by teeth, are adults. Although entwined model, although both are struc­ cient environment provide insight into old individuals possibly died in the dens tural possibilities (Fig. 2). Finally, the mammalian paleoecology. We report the through normal attrition, the deaths of nodal precessions for the two models discovery of a 20-million-year-old den the juvenile and young adults in the would be markedly different if they were complex (1) with partial skeletons offour burrows must have been premature and stabilized in the ways suggested above. species of extinct Miocene Carnivora. probably sudden. The partial disarticula­ VON R. ESHLEMAN The remains, found in burrow fills over tion of all skeletons in the burrows and Space, Telecommunications, and 30 m2 in the floodplain of an early Mio­ bite marks on some bones show that Radioscience Laboratory, cene ephemeral stream, are an unusual there was sufficient time for decomposi­ Stanford University, occurrence in the fossil record (2). tion and scavenging of carcasses to take Stanford, California 94305 The discovery extends the age of den­ place before sediment burial. ning behavior of large terrestrial Carni­ In addition to bear dogs, the dens References and Notes vora to the early Miocene. It also indi­ contained remains of small canid and I. J. L. Elliot, E. Dunham, D. Mink, Nature cates that amphicyonid carnivores (the mustelid carnivores. Because simulta­ (London) 267,328 (1977); R. L. Millis and L. H. Wasserman, Astron. J. 83. 993 (1978); J. L. dominant mid-Cenozoic land Carnivora) neous occupation of a den by more than Elliot, E. Dunham, L. H. Wasserman, R. L. used dens and that denning was within one species is uncommon among living Millis • .I. Churms, ibid., p. 980; P. D. Nicholson, S. E. Persson, K. Matthews, P. Goldreich, G. the capability of many if not all amp hi­ Carnivora, the presence of more than Neugebauer, ibid., p. 1240. cyonids, since species from two widely 2. B. A. Smith et al., Science 215,504 (1982); A. L. one kind offossil carnivore in these dens Lane et al., ibid., p. 537; B. R. Sandel et al., divergent lineages were found in sepa­ suggests they were used by a succession ibid., p. 548; G. L. Tyler, E. A. Marouf, R. A. Simpson, H. S. Zebker, V. R. Eshleman; Icarus rate dens (3). Furthermore, the skeletons of species, that the smaller carnivores 54, 160 (1983). in the den complex suggest that the dens were occasional prey of the larger bear 3. H. Jeffreys, Mon. Not. R. Astron. Soc. 107,263 (1947); A. Brahic, Aslran. Astraphys. 54, 895 were used in protection and care of the dogs, or both. However, the presence of (1977); P. Goldreich, Annu. Rev. A.mon. As­ young and as shelter for adults; to our only a few herbivore bone fragments lrophys. 20, 249 (1982); P. Goldreich and S. Tremaine, Icarus 34, 277 (1978); ibid., p. 240; knowledge they provide the only evi­ within the burrows indicates that prey A.wophy". 1. 233, 857 (1979); ibid. 243, 1062 dence known in the Tertiary fossil record carcasses were infrequently taken into (1981); J. A. Burns, P. Hamill, J. N. Cuzzi, R. H. Durisen, Aslran. J. 84, 1783 (1979); J. L. for the occupation of a den by a succes­ the dens, thus the small carnivores were Elliot, R. G. French, J. A. Frogel, J. H. Elias, D. J. Mink, W. Liller, ibid. 86,444 (1981); P. D. sion of carnivore species. The Agate den probablY den occupants. Nicholson, K. Matthews, P. Goldreich, ibid., p. complex represents one of the oldest The dens (Fig. I) occur in an area 5 by 596; J. N. Cuzzi, R .. H. Durisen, J. A. Burns, P. Hamill, Icarus 38, 54 (1979). known burrow systems (4). 6 m in quarry 3 on Beardog Hill, Agate 4. F. C. Michel, Planet. Space Sci. 29,1137 (1981); The history of this ancient predator Fossil Beds National Monument, Ne­ ASlraphys. Lett. 22, 101 (1982). 5. V. R. Eshleman, J. V. Breakwell, G. L. Tyler, community can be reconstructed from braska. Carnivores burrowed into a E. A. Marouf, Icarus 54, 212 (1983). Tyler and Eshleman discussed aspects of the entwined the size and form of the burrows, the stream channel fill of tuffaceous white model at two public meetings at the time of the ages of the carnivores (established by the fine-grained sandstone (Upper Harrison Voyager 2 encounter of Saturn in August 1981. 6. R. G. French, J. L. Elliot, D. A. Allen, Nature degree of eruption and wear on teeth), beds, Arikaree Group). Only 150 to 300 (London) 289, 827 (1982). the condition of the skeletons, and the m north of the dens, this same sandstone 7. P. D. Nicholson, K. Matthews, P. Goldreich, Astron. J. 87, 433 (1982). nature of sediment fill. The form and contains the dense bone deposits of early 8. J. B. Pollack, Space Sci. Rev. 18,3 (1975); J. N. large size of the burrows, similar to Miocene rhinoceros, chalicothere, and Cuzzi and J. B. Pollack, Icarus 33,233 (1978); J. N. Cuzzi, J. B. Pollack, A. L. Summers, ibid. burrows of living large canids and hyaen­ entelodont, which were found at the na­ 44,683 (1980); E. E. Epstein, M. A. Janssen, J. N. Cuzzi, W. G. Fogarty, J. Mortman, ibid. 41, ids, suggest their construction or remod­ tional monument early in this century (5, 103 (1980). eling by the largest terrestrial carnivores 6). Thus the dens must postdate deposi­ 9. E. A. Marouf, G. L. Tyler, H. A. Zebker. R. A. Simpson, V. R. Eshleman, Icarus 54,189 (1983); of the early Miocene, the amphicyonids tion of the principal Agate bone bed. The E. A. Marouf, G. L. Tyler, V. R. Eshleman, or bear dogs. The bear dogs found in the time that elapsed between formation of ibid. 49, 161 (1982); H. A. Zebker, G. L. Tyler, E. A. Marouf, in preparation; H. A. Zebker, dens resemble wolves in size and certain the great bone bed and the dens was private communication. skeletal features, but are not closely re­ probably brief in the perspective of geo­ 10. Satellite perturbations, particularly those of nearby "shepherding" satellites (11), are poten­ lated. The bear dog Daphoenodon super­ logic time, since fragments of the same tially important for ringlet stability, but it has not been established whether the narrow ringlets bus is represented by at least six or carnivore species found in the dens have generally have such shepherds. seven individuals, and a rare temnocyon­ also been found in the bone bed (6, 7). II. P. Goldreich and S. Tremain, Nalure (London) 277,97 (1979); Astron. J. 84, 1638 (1979). ine bear dog by one skeleton. Ajuvenile, These carnivores have short temporal 12. This work was supported by NASA. I thank J. a mature adult, and at least three old ranges of at most a few million years. We V. Breakwell, E. A. Marouf, G. L. Tyler, P. D. Nicholson, and R. G. French for helpful discus­ individuals of Daphoenodon can be iden­ suspect that the dens were emplaced SIOns. tified from dental evidence. Skeletal fea­ only weeks to a few years after the Agate II January 1983; revised 28 March 1983 tures indicate that the remains of one or bone bed was deposited.

364 SCIENCE, VOL. 221 Den dimensions approximate those of sively by sediment influx through the ing, with breakdown and incorporation wolves, coyotes, and hyenas today (8). burrow mouth. In burrow B, 10- to 20- of part of the burrow wall. Although we Den 1 (Fig. l) contained two nearly cm-thick layers of homogeneous fine are not able to Oligocene canid Hesperocyon, as ed at 6 months; epiphyses fuse about I year from well as bones of many smaller mammals, proba­ birth. to a few years. bly prey of the canid, in an early Oligocene 10. The adult and juvenile Daphoenodon were Four species of carnivores, represent­ burrow in Wyoming. He believes that the bur­ found in 1905 by O. Peterson [(7); Ann. Carne­ row was occupied by, but probably not excavat­ gie Mus. 4, 51 (1907)]. who discovered and ed by about 11 individuals, have been ed by, Hesperocyon. named quarry 3 and reported from it three or 3. See M. Voorhies, in The Study of Trace Fossils, four other individuals of Daphoenodon, a small found in the three dens: the bear dog R. Frey, Ed., (Springer-Verlag, New York, canid, and mustelid. Despite the number of Daphoenodon superb us , the unnamed 1975), p. 336. carnivores and the absence of herbivores, Peter­ 4. Older vertebrate burrows that contained resi­ son did not identify the site as a den complex. temnocyonine bear dog, a small canid dent fossil mammals are those of extinct fossori­ To determine why only carnivores were found, Phlaocyon annectens, and the mustelid al rodents [0. Peterson, Mem. Carnegie Mus. 2, we relocated Peterson's original site. By screen­ 139 (1905)], early Miocene, Harrison Formation, ing topsoil at the most probable locality at Paroligobunis simplicidens. Two species Sioux County, Nebraska. These' burrows pre­ Beardog Hill in September 1981, we found a of bear dogs were found by us in place in served not only rodents but also two carnivores proximal Daphoenodon tibia that fit a bone (2). Somewhat older Oligocene burrows (3) from fragment collected by Peterson in 1905. In Fig. the burrows: the aged Daphoenodon in the Brule Formation, Nebraska, did not contain 1, quarry 3 could have been limited to meter mammal bones. squares B-D 5-6, an area of 6 m', where the den 3 and the adult temnocyonine in den 5. O. Peterson, Ann. Carnegie Mus. 3. 487 (1906); bone fragment was found. 2. Because of the proximity of these dens Mem. Carnegie Mus. 4, 41 (1909); ibid. 7, 399 II. R. Vicars and 1. Breyer, 1. Sed. Petrol. 51, 909 (1920); W. Holland and O. Peterson, ibid. 3, 189 (1981). to an early Miocene braided stream (11), (1914). 12. We thank A. 1. Banta, 1. Rapier, R. Todd, and flooding of the burrows is the most likely 6. R. Hunt, Am. Mus. Novit. 2506 (1972). W. Taylor, National Park Service, for support 7. O. Peterson, Mem. Carnegie Mus. 4, 206 (1910). and access to Agate sites; B. Van Valkenburgh cause of death of younger animals. 8. D. Mech, The Wolf(Univ. of Minnesota Press, for information on dens; A. Boucot, 1. Fager­ Minneapolis, 1970), p. 120; I. Grinnell et al., strom, P. Freeman, B. Ratcliffe, M. Dawson, R. In summary, this unusual site appears Fur-Bearing Mammals of California (Univ. of Tedford for manuscript review. Fieldwork fund­ to represent a den complex of early California Press, Berkeley, 1937), vol. 2, pp. ed by NSF grant INT-8117703 to R.M.H. and 509-511; H. Kruuk, The Spotted Hyaena (Univ. X.X. and by National Geographic Society funds Miocene amphicyonid, canid, and mus­ of Chicago Press, Chicago, 1972), pp. 242-247. to R.M.H. telid carnivores that was developed dur­ 9. On basis of development of living wolves (8), the ing an unknown time interval in the juvenile den I Daphoenodon is 6 months to I , 7 October 1982; revised 20 December 1982 channel floodplain of a wide, shallow, ephemeral stream which was subject to intense periodic floods, probably season­ al in nature. Daphoenodon was the prin­ Intracellular pH Regulates Transitions Between Dormancy and cipal occupant of the dens, but other Development of Brine Shrimp (Artemia salina) Embryos bear dogs, canids, and mustelids used them for shelter, and Daphoenodon fe­ Abstract. The intracellular pH (pH;) of encysted gastrula-stage embryos of the males probably used the dens to care for brine shrip, Artemia, as previously shown by in vivo phosphorus-31 nuclear magnetic their young. Before the den complex was resonance spectroscopy, increases by more than 1 unit during arousal from buried by stream sediments, floodwaters cryptobiotic dormancy and decreases by the same amount during reinduction of may have drowned juvenile and young dormancy. These changes in pHi are now shown to be a fundamental regulator of the adult bear dogs (including a mother-cub transitions between dormancy and metabolism: acidification of activated embryo pair) in their dens. The carcasses decom­ pHi by more than 1 unit with carbon dioxide induced a state comparable to natural posed in the burrows and were disturbed dormancy, while alkalinization of dormant embryo pHi with the weak base ammonia by scavengers and additional floods. As terminated natural dormancy. This demonstration of pHi-mediated regulation of shifting episodic streamflow resulted in cryptobiotic dormancy extends the known scope for pHi as a regulator of develop­ channel migration over the dens, ash­ ment to include multicellular stages of the metazoan life cycle. rich sediment gradually filled the bur­ rows, thereby preserving a remarkable Cellular dormancy, a spectrum of hy­ versibility, enabling study of both initia­ association of young, mature, and aged pometabolic states involving inhibition tion and termination of dormancy, offers extinct Carnivora. of both catabolic and anabolic processes, opportunities to further test the role of ROBERT M. HUNT, JR. is common to some stage of the life pHj in metabolic regulation. Department of Geology, University of cycles of most organisms. Arousal from The Artemia cyst displays two distin­ Nebraska, Lincoln 68588 the comparatively modest dormancy of guishable but related forms of dormancy XUE XIANG-XU the sea urchin egg is regulated in part by (8). Newly released from the ovisac, the Department of Geology,Northwestern a moderate (~ 0.4 unit) alkalinization of cyst remains developmentally arrested University, Xian, Shaanxi, China intracellular pH (pHj) (1, 2). Even larger for extended periods. Under natural con­ JOSHUA KAUFMAN increases in pHj (~ 1 unit) accompany ditions, such aerobic dormant cysts, Nebraska State Museum, the transitions between dormancy and which are so called because the embryos Lincoln 68588 metabolism of bacterial (3) and perhaps remain dormant even in the presence of also yeast spore (4, 5) germination, but oxygen, are activated to resume metabo­ References and Notes the physiological significance of these lism and development by desiccation and I. The age of the den complex is determined from two volcanic tuffs, Sioux County, Nebraska: (i) larger pHj changes is not yet clear (6). subsequent aerobic rehydration. When Agate Ash, about 10 m stratigraphically below The largest pHj changes observed under rehydrated in the absence of oxygen, the dens and main Agate bone bed, 21.3 million years, KA sample 481 [1. Evernden et al., Am. biologically meaningful conditions (> 1 however, they remain dormant, or reen­ 1. Sci. 262, 145 (1964)]; (ii) Eagle Crag Ash [location: WY2, NWY4, SWY4, SEY4, section 27, unit) accompany transitions between ter dormancy if oxygen is withdrawn T.32N, R. 56W], either stratigraphically above profound dormancy (cryptobiosis) and after aerobic rehydration; we term these or about the same level as the dens, dated at 19.2 ± 0.5 million years (1 standard deviation), development in encysted gastrula-stage "anaerobic dormant" cysts because fission track (zircon) by R.M.H. embryos (cysts) of the brine shrimp, they normally remain dormant only un­ 2. E. Riggs [Fieldiana Geol. 8,59 (1942); ibid. 9, 69 (1945)] reported finding partial skeletons of two Artemia salina (7). While the extreme der anoxic conditions. Aerobic dorman­ small carnivores, each found separately in the degree of dormancy of Artemia cysts is cy, anaerobic dormancy, and aerobic burrows of fossorial rodents, early Miocene, Harrison Formation, Sioux County, Nebraska, unusual among metazoans, its true re- development thus represent three alter-

366 SCIENCE, VOL. 221