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Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

10-1992

Parasites of the Extinct Shasta Ground , shastensis, in Rampart Cave,

Gerald D. Schmidt university of Northern Colorado

Donald W. Duszynski University of New Mexico, [email protected]

Paul S. Martin University of Arizona

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Schmidt, Gerald D.; Duszynski, Donald W.; and Martin, Paul S., "Parasites of the Extinct Shasta , Nothrotheriops shastensis, in Rampart Cave, Arizona" (1992). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 181. https://digitalcommons.unl.edu/parasitologyfacpubs/181

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 78(5), 1992, p. 811-816 ? American Society of Parasitologists 1992

PARASITESOF THE EXTINCTSHASTA GROUNDSLOTH, NOTHROTHERIOPSSHASTENSIS, IN RAMPARTCAVE, ARIZONA

Gerald D. Schmidt*, Donald W. Duszynski, and Paul S. Martint Departmentof Biology,The Universityof New Mexico,Albuquerque, New Mexico87131

ABSTRACT:Of 7 dissecteddung balls of the extinct Shastaground sloth (Edentata)from RampartCave, Arizona, 4 (57%)were found to contain nematodejuveniles, helminth eggs, and/or coccidian oocysts. One dung ball was radiocarbondated at 10,500 + 180 yr, about the time of groundsloth .It is supposedthat the parasites also are extinct. Agamofilariaoxyura n. sp. is proposed for first-stagejuveniles of an oxyurid. These juveniles measured 13-20 x 126-198 (16.8 x 159) Aim.Strongyloides shastensis n. sp. is reportedas first-stagejuveniles, some of which clearlyare molting.These juvenile worms were 23-27 x 270-345 (24.4 x 305.3) ,em.Operculated schistosomelikeeggs, each with an abopercularpoint, were 33-50 x 63-90 (43.0 x 81.9) ,um.A second type of object that resembled a helminth egg had a thick wall and was 11-14 x 13-18 (13.5 x 15.5) ,m. A new collective genus,Archeococcidia, is proposedto include 2 new fossil oocysts. Archeococcidiaantiquus n. sp. was the most abundantform found. Its unsporulatedoocysts were 19-21 x 21-23 (19.6 x 22.1) Am, and its outer wall bore punctations.Unsporulated oocysts of Archeococcidianothrotheriopsae n. sp. were spheroidal,31-35 (33.8) um wide, and had a smooth outer surface.

Parasites of prehistoric extinct rare- at the top of a talus slope, more than 200 m above the ly are reported. Home (1985) and Wilke and Hall level of the ColoradoRiver. Passageways extend roughly 100 m into limestone About (1975) provided annotated bibliographies on the (upper Period). 220 m2 of dung, reachinga maximum depth of 1.5 m, analyses of ancient feces, mainly of human ori- covers the floor of part of the cave. Two-thirdsof this gin, and Fry and Moore (1969) found Enterobius was destroyedby a smolderingfire betweenJuly 1976 sp. in dry human up to 10,000 yr in and March 1977. Exact provenienceof the dung balls in this is were radiocarbon age. The fossil dung of some mam- study unknown; they obtained from of in back dirt left the 1940 excavation rats is found in heaps dung by mals, especially pack (Neotoma), of Remington Kellogg(Martin, unpubl.). abundance in certain dry caves of the North Portionsof each dung ball were brokenup and rew- American desert southwest, where ancient feces etted for 48 hr in a 0.5% solution of trisodium phos- may endure for tens of thousands of (Be- phate, then filtered through coarse cheesecloth, and later 40- and 60-mesh brass screens. tancourt et al., 1990). Occasionally, dung of cer- through Aliquots of the resulting filtrate then were examined either di- tain extinct mammals is also includ- preserved, rectly as wet mounts or they were concentrated by ing entire and fragmentary boluses of the Shasta flotation with a concentrated sucrose solution (specific ground sloth, Nothrotheriops shastensis. One of gravity 1.15). Parasitesand parasitestages were mea- sured with an ocular micrometer and several giant (extinct) edentates of the Western photographed with Panatomic-X 35-mm film within a Zeiss Uni- the late Hemisphere during Epoch, versalPhotomicroscope equipped with both brightfield its last remains can be traced to about 11,000 yr (Neofluar) and Nomarski-interference100 x objec- ago (Martin et al., 1985) when Shasta ground tives. All measurementsare in micrometers(,im) with disappeared along with mammoths, sa- the means given in parenthesesfollowing the ranges. Phototypes(Bandoni and Duszynski, 1988) of the coc- bertooths, and other (Martin, 1987). cidian oocysts and both phototypes and syntypes of Examination of these dried boluses can offer in- the worms have been deposited in the U.S. National sight about the parasites that these mammals Museum Parasite Collection (USNMPC), Beltsville, maintained. Maryland.

MATERIALSAND METHODS RESULTS We examined7 sloth dungballs collected from Ram- part Cave, Arizona, at the western end of the Grand The dung balls are large, up to 12 cm and Canyon. The cave is about 7 km from Pierce's Ferry occasionally more than 20 cm in diameter, lo- bate, with a reddish-brown varnish of dried mu- Received 30 July 1991; revised 17 October 1991; cus. Evidently the was totally herbivo- accepted 17 October 1991. to Hansen the identifiable * rous; according (1978), Department of Biological Sciences, University of plant tissues in the dung consist principally of Northern Colorado, Colorado 80631 (de- Greeley, Sphaeralcea; Mormon tea, Ephed- ceased). globemallow, t Departmentof Geosciences, University of Arizona, ra; and , Opuntia. These xeric plants re- Tucson, Arizona 85721. main important in the regional vegetation of the

811 812 THE JOURNALOF PARASITOLOGY,VOL. 78, NO. 5, OCTOBER1992 area especially at higher elevation. Vegetation in ascarid egg (Fig. 11), but the outer layer is smooth the immediate vicinity of the cave during the and its size is much smaller (n = 8), 10.8-14.4 sloth's occupancy included juniper (Juniperus), x 12.6-18.0(13.5 x 15.5). ash (Fraxinus), and other woodland species that n. only occur now at higher elevations (Phillips, Agamofilaria oxyura sp. (Figs.1-3) 1984). Indeed, there is no indication that the Description: Robust worms, coiled, climate and vegetation were much different then usually tightly resemblingfirst-stage pinworms (Fig. 1). Mouth sur- now. One dung ball, containing unsporulated roundedby 3 bilobed lips (Fig. 2); tail sharplypointed coccidian oocysts and schistosomelike eggs, has (Fig. 3). Posteriorend of esophagusexpanded into a been '4C-dated at 10,500 + 180 yr; the other 3 bulb, characteristicof the (Fig. 1, arrow).Length = 13-20 x 126-198 x infected samples were not dated. The weighted (n 7) (16.8 159). average of the youngest 10 samples of dung de- Taxonomic summary posited in the cave was within a few years of Typehost: Shastaground sloth, N. shastensis. 11,000 BP (before present) (Martin et al., 1985). Type locality: Rampart Cave, ca. 7 km upstream All specimens are presumed to be of this age or from Pierce's Ferry, 36?06'N, 113?56'W,Grand Can- yon, Arizona. greater. Material deposited: Phototype of representative found in 4 of the 7 sam- Parasites were (57%) structuresfrom 1 juvenile worm and 10 syntypes in ples. There were juveniles of 2 nematode species, the USNMPC No. 82076. 2 of coccidian and of morphotypes oocysts, eggs Remarks 2 helminth species. spores and pollen were Fungal One ball contained nematode abundant and had to be differentiated from dung many juveniles pos- (about 10 worms/dropof sediment)that resemblefirst- sible oocysts. The condition of the nematodes stagepinworms. Adult nematodes were not found, sug- precluded detailed observations and measure- gesting that this does not representa coprophagous, ments. free-livingform. This species was found in only 1 of the 7 balls examined. The International Code of Zoological Nomen- dung clature (Art. 42 (b)(i)) (Ride et al., 1985: 83) makes shastensis n. provision for "... certain assemblages of taxo- Strongyloides sp. (Figs.4-8) nomic convenience known as 'collective groups'." Slender coiled Included are known from fossil trac- Description: worms,only slightly (Fig. species only 4). Head small, lacking conspicuous lips. Esophagus es (ichnotaxa) and those known only from im- usuallydetached from mouth and difficultto interpret mature specimens, adult forms of which cannot (Fig. 5);in some specimensin which not detachedfrom be determined. Any of those can be reallocated mouth, a pair of rodlikestructures are present(Fig. 6). Esophagusthicker at with intestine, to the correct genus if it is later discovered. Ex- junction repre- senting a pseudobulb.Tail (Fig. 7) long and pointed, 1892 amples given are Agamodistomum Stossich, resemblinga first-stagejuvenile of Strongyloides.Some (Trematoda), Agamofilaria Stiles, 1907 (Nema- worms in process of molting (Fig. 8). Length (n = 7) toda), and Stelloglyphus Vyalov, 1964 (trace fos- 23-27 x 270-349 (24.4 x 305.3). use sil), among others. Presumably, the frequent Taxonomic summary of as a to these collective "agamo" prefix group Typehost: Shastaground sloth, N. shastensis. genera stems from its derivation: a- (Gr., not, Type locality: Rampart Cave, ca. 7 km upstream without) and gam- (Gr., marriage). In applying from Pierce'sFerry, 36?06'N, 113?56'W,Grand Can- names to the organisms we found, we sought to yon, Arizona. Material deposited: of follow this basic concept. Phototype representative structuresfrom 1juvenile wormand about 10 syntypes Numerous bodies, presumably helminth eggs in the USNMPC No. 82075. representing 2 species, were found in 3 dung balls. Remarks One kind (Fig. 9) is conspicuously pointed at 1 One ball contained numerous end and have a subterminal operculum at dung nematode ju- may veniles that bear similaritiesto Stron- the other. The outer surface of the is striking juvenile egg capsule gyloides.Adult nematodeswere not found, suggesting pitted (Fig. 10). Except for the operculum, these that these specimensdo not representa coprophagous, eggs look somewhat like schistosome eggs. These free-livingform. This species was found in 2 of the 7 eggs were found in 3 of the 7 dung balls and dung balls examined. measured (n = 8) 33-50 x 63-90 (43.0 x 81.9). Archeococcidia n. A second type of object that resembled a hel- gen. minth egg was found in only 1 of the dung balls. Reserved for structures that are oocystlike in Its thick wall gives some resemblance to a tox- general size, shape, and appearance; that come SCHMIDTET AL.-PARASITES OF EXTINCT SHASTA GROUND SLOTHS 813

FIGURES1-8. Photomicrographsof juvenile nematodes extractedfrom the desiccated feces of the extinct Shastaground sloth, Nothrotheriopsshastensis, from RampartCave, GrandCanyon, Arizona. Figures 1-3, bars = 15 um; Figures 4-8, bars = 30 Aim.1. Lateral view of entire juvenile of Agamofilariaoxyura n. sp.; note esophagealbulb (arrow).2. Enlargedhead of A. oxyura showing 3 bilobed lips of mouth. 3. Pointed tail of same species. 4. Lateralview of entire juvenile of Strongyloidesshastensis n. sp.; note pointed tail and esophagus pulledaway from mouth. 5. Enlargementof anteriorend of S. shastensisjuvenile; note how esophagusis detached from mouth. 6. Anteriorends of some S. shastensisjuveniles show 2 rodlikestructures (arrows) seen only when the esophagushas not separatedfrom the mouth. 7. Enlargedlateral view of tail showing location of anus. 8. Same species showing molting to second stage. from dried, petrified, or mummified feces or bod- Taxonomic summary ies of extinct ; and that, because of their Type host: Shasta groundsloth, N. shastensis. antiquity, are unsporulated and, therefore, not Type locality: Rampart Cave, ca. 7 km upstream from Pierce's Grand able to be placed into an appropriate genus. Ferry, 36?06'N, 113?56'W, Can- yon, Arizona. Archeococcidia antiquus n. sp. Material deposited: Phototype of unsporulatedoo- in the USNMPC No. 82073. (Figs. 12, 13) cyst coccidian Description: Unsporulated oocysts ellip- Remarks soidal with pitted outer wall (Fig. 13) (n = 8) 19-21 x 21-23 (19.6 x 22.1). Inner mass disrupted,no indi- An abundanceofunsporulated coccidian oocysts (Fig. cation of sporocystformation could be seen, and thus, 12) was found in 1 dung ball. It is likely an eimerian it is impossible to place it in any known genus. as all known coccidians described from edentates to

SCHMIDTET AL.-PARASITES OF EXTINCT SHASTA GROUND SLOTHS 815

Taxonomic summary were oocysts and that we should publish this Type host: Shasta ground sloth, N. shastensis. information. Type locality: Rampart Cave, ca. 7 km upstream LITERATURECITED from Pierce's Ferry, 36?06'N, 113?56'W, Grand Can- yon, Arizona. BANDONI,S. M., ANDD. W. DUSZYNSKI.1988. A plea Material deposited: Phototype of unsporulated oo- for improved presentation of type material for coc- cyst in the USNMPC No. 82074. cidia. Journal of Parasitology 74: 519-523. J. T. R. VAN AND P. S. Remarks BETANCOURT, L., DEVENDER, MARTIN. 1990. Packrat middens: The last 40,000 A second kind of oocyst, not as common as A. an- years of biotic change. University of Arizona Press, tiquus, was found in another dung ball. Oocysts of this Tucson, 468 p. form were found only in 1 of the 7 dung balls examined. FERREIRA,L. F., A. ARAUJO,U. CONFALONIERI,M. In summary, 4 of 7 (57%) dung balls from the extinct CHAME,AND D. C. GOMES. 1991. Trichuris eggs Shasta ground sloth from Rampart Cave, Arizona, had in animal coprolites dated from 30,000 years ago. parasite stages in them. One dung ball had only a few Journal of Parasitology 77: 491-493. juveniles of S. shastensis. Another had oocysts of A. FRY, G. F., ANDJ. G. MOORE. 1969. Enterobius ver- antiquus (Figs. 12, 13) and schistosomelike eggs (Figs. micularis: 10,000--old human infection. Sci- 9, 10). A third ball had many juveniles of S. shastensis ence 166: 1620. (Figs. 4-8) and both schistosomelike and small, thick- GoocH, P. S. 1973. Helminths in archaeological and walled eggs (Fig. 11). The fourth infected dung ball had pre-historic deposits. Commonwealth Institute of oocysts of A. nothrotheriopsae (Fig. 14), schistosome- Helminthology, Annotated Bibliography No. 9, St like eggs, and juveniles of A. oxyura (Figs. 1-3). Albans, Herts, England, 8 p. HANSEN,R. M. 1978. Shasta ground sloth food hab- DISCUSSION its, Rampart Cave, Arizona. Paleobiology 4: 302- 319. is an Paleoparasitology attracting increasing HANTZSCHELL,W., F. EL-BAZ,AND G. C. AMSTUTZ. number of investigations (Kliks, 1983, 1990; 1968. Coprolites: An annotated bibliography. Reinhard et al., 1987; Ferreira et al., 1991). For Memoirs of the Geological Society of America 108: 1-132. annotated bibliographies, see reports by Hantz- HORNE,P. D. 1985. A review of the evidence of schell et al. Gooch Wilke and Hall (1968), (1973), human endoparasitism in the pre-Columbian New (1975), and Hore (1985). Nearly all previous World through the study of coprolites. Journal of reports have been on human, or presumably hu- Archaeological Science 12: 299-310. man, materials. KLIKS,M. M. 1983. Paleoparasitology: On the origins and impact of human-helminth relationships. Hu- Two reports are known to us concerning par- man Ecology and Infectious Diseases 11: 291-313. asites of sloths from the Pleistocene Epoch. Rin- 1990. Helminths as heirlooms and souvenirs: guelet (1957) described "probable remains of A review of New World paleoparasitology. Para- nematode eggs" from dung of the giant sloth, sitology Today 6: 93-100. AND P. A. MUNZ. 1938. Plants listai, in Tierra del Fuego, Chile. The LAUDERMILK,J. D., in the dung of from Rampart and were elliptical, 31.5-49.5 x 18.7-29.2 in eggs Muav Caves, Arizona. Carnegie Institution of size. Washington, Publication No. 487: 271-281. Laudermilk and Munz (1938) studied dung LEVINE,N. D. 1988. The protozoan phylum Apicom- balls of "Nothrotherium" (=N. shastensis) also plexa, Vol. I. CRC Press, Inc., Boca Raton, Flor- ida, 203 p. from Rampart Cave. Although their paper was MARTIN,P. S. 1987. Late Quaternary : concerned with the the plants making up dung The promise of TAMS 14Cdating. In Proceedings balls, they reported, "... perfectly preserved of the fourth international symposium on accel- nematode worms as well as their eggs were abun- eration mass spectrometry, H. Gove, A. E. Lith- dant." Remains of their material are not known erland, and D. L. Moore (eds.). Nuclear instru- ments and methods in physics research B29. North to exist. This is the only previous report of par- Holland Publishing Company, Amsterdam, p. 179- asites of N. shastensis. Further studies probably 186. would uncover other parasite remains, and a de- , R. S. THOMPSON,AND A. LONG. 1985. Shasta tailed chronological sequence might be of inter- ground sloth extinction: A test of the blitzkrieg model. In Environments and extinctions: Man in est to those seeking causes of extinction. late glacial , J. I. Mend and D. Meltzer (eds.). Center for the of ACKNOWLEDGMENT Study Early Man, Orono, Maine, p. 5-14. Thanks are due Norman D. Levine, Professor PELLERDY,L. P. 1974. Coccidia and coccidiosis, 2nd ed. Verlag Paul Parey, Berlin, 959 p. Emeritus, The University of Illinois, who looked PHILLIPS,A. M. 1984. Shasta ground sloth extinction: at photomicrographs of our unsporulated oocysts Fossil packrat midden evidence from the western and gave his opinion that he too thought they . In Quaternary extinctions: A pre- 816 THEJOURNAL OF PARASITOLOGY,VOL. 78, NO. 5, OCTOBER1992

historic revolution, P. S. Martinand R. G. Klein RINGUELET,R. A. 1957. Restos de probables huevos (eds.). University of Arizona Press, Tucson, Ari- de nematodes en el estiercol del edentado extin- zona, p. 148-158. guidoMylodon listai (Ameghino).Ameghiniana 1: REINHARD, K. J., R. H. HEVLY,AND G. A. ANDERSON. 15-16. 1987. Helminth remainsfrom prehistoricIndian WILKE,P. J., ANDH. J. HALL. 1975. Analysis of an- coproliteson the ColoradoPlateau. Journal of Par- cient feces: A discussion and annotated bibliog- asitology73: 630-639. raphy. Contribution of the University of Califor- RIDE, W. D. L., C. W. SABROSKY, G. BERNARDI, AND nia Archeological Research Facility, No. 24, R. V. MELVILLE(eds.). 1985. International code Department of Anthropology, University of Cal- of zoological nomenclature,3rd. ed. H. Charles- ifornia, Berkeley, , 47 p. worth and Co., Ltd., Huddersfield, England, 338 p.