Parasites of the Extinct Shasta Ground Sloth ...

University of Nebraska - Lincoln

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10-1-1992

Parasites of the Extinct Shasta Ground Sloth,
Nothrotheriops shastensis, in Rampart Cave, Arizona

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 Ground Sloth, Nothrotheriops
shastensis, in Rampart Cave, Arizona" (1992). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. Paper 181.
http://digitalcommons.unl.edu/parasitologyfacpubs/181

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J. Parasitol., 78(5), 1992, p. 811-816
? American Society of Parasitologists 1992

PARASITESOF THEEXTINCTSHASTAGROUNDSLOTH,
NOTHROTHERIOPSSHASTENSIS,IN RAMPARTCAVE, ARIZONA

Gerald D. Schmidt*,Donald W. Duszynski, and Paul S. Martint
Departmenotf BiologyT, heUniversitoyf NewMexico,AlbuquerqueN, ew Mexico87131

ABSTRACT:Of 7 dissecteddungballsof the extinctShastagroundsloth(Edentata)fromRampartCave,Arizona,
4 (57%)werefoundto containnematodejuveniles,helmintheggs,and/orcoccidianoocysts.One dungballwas
radiocarbondatedat 10,500 + 180yr,aboutthe time of groundslothextinction.It is supposedthattheparasites
also are extinct.Agamofilariaoxyuran. sp. is proposedfor first-stagejuveniles of an oxyurid.Thesejuveniles
measured13-20 x 126-198 (16.8 x 159)AimS. trongyloidesshastensisn. sp. is reportedas first-stagejuveniles,
some of whichclearlyaremolting.Thesejuvenilewormswere23-27 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 resembleda helminth egg had a thick wall and was 11-14 x 13-18 (13.5 x 15.5) ,m. A new
collectivegenus,Archeococcidiai,s proposedto include2 new fossil oocysts.Archeococcidiantiquusn. 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.Unsporulatedoocysts of Archeococcidianothrotheriopsane. sp. were spheroidal,31-35
(33.8) umwide, and had a smooth outersurface.

Parasites of prehistoric extinct mammals rare- at the top of a talusslope, morethan200 m above the
ly are reported. Home (1985) and Wilke and Hall levelof the ColoradoRiver.Passagewayesxtendroughly
100m into limestone(upperCambrianPeriod).About
(1975) provided annotated bibliographies on the 220 m2of dung,reachinga maximumdepthof 1.5 m,
analyses of ancient feces, mainly of human ori- coversthe floorof partof the cave. Two-thirdsof this
gin, and Fry and Moore (1969) found Enterobius was destroyedby a smolderingfirebetweenJuly 1976
sp. in dry human coprolites up to 10,000 yr in and March1977. Exactprovenienceof the dungballs
radiocarbon age. The fossil dung of some mam- in this study is unknown;they were obtained from
mals, especially pack rats (Neotoma), is found in heapsof dungin backdirtleft by the 1940 excavation
abundance in certain dry caves of the North of RemingtonKellogg(Martin,unpubl.).
American desert southwest, where ancient feces
may endure for tens of thousands of years (Be- Portionsof eachdungballwerebrokenup and rew-
tancourt et al., 1990). Occasionally, dung of cer- etted for 48 hr in a 0.5% solution of trisodium phos-
tain extinct mammals is also preserved, includ- phate, then filtered through coarse cheesecloth, and
ing entire and fragmentary boluses of the Shasta later through 40- and 60-mesh brass screens. Aliquots
ground sloth, Nothrotheriops shastensis. One of of the resulting filtrate then were examined either di-
several giant (extinct) edentates of the Western rectly as wet mounts or they were concentrated by
Hemisphere during the late Pleistocene Epoch, flotation with a concentrated sucrose solution (specific
its last remains can be traced to about 11,000 yr gravity 1.15). Parasitesand parasitestageswere mea-
ago (Martin et al., 1985) when Shasta ground sured with an ocular micrometerand photographed
sloths disappeared along with mammoths, sa- with Panatomic-X 35-mm film within a Zeiss Uni-
bertooths, and other megafauna (Martin, 1987).
Examination of these dried boluses can offer in- versalPhotomicroscopeequippedwithbothbrightfield
(Neofluar) and Nomarski-interference100x objec-
sight about the parasites that these mammals tives. All measurementsarein micrometers(,im)with
maintained. the means given in parenthesesfollowingthe ranges.
Phototypes(BandoniandDuszynski,1988)of the coc-
cidian oocysts and both phototypesand syntypesof
the worms have been depositedin the U.S. National
Museum Parasite Collection (USNMPC), Beltsville,

Maryland.

MATERIALAS NDMETHODS RESULTS
Weexamined7 slothdungballscollectedfromRam-
part Cave, Arizona,at the westernend of the Grand The dung balls are large, up to 12 cm and
Canyon.The cave is about 7 km from Pierce'sFerry 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 animal was totally herbivo-
accepted 17 October 1991. rous; according to Hansen (1978), the identifiable
* Department of Biological Sciences, University of plant tissues in the dung consist principally of
globemallow, Sphaeralcea; Mormon tea, Ephed-
NorthernColorado,Greeley, Colorado 80631 (de- ra; and cactus, Opuntia. These xeric plants re-
main important in the regional vegetation of the
ceased).
t Departmentof Geosciences,University of Arizona,
Tucson, Arizona 85721.

811

812 THEJOURNALOF PARASITOLOGYV,OL.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
only occur now at higher elevations (Phillips, Agamofilariaoxyura n. sp.
1984). Indeed, there is no indication that the (Figs.1-3)
climate and vegetation were much different then
now. One dung ball, containing unsporulated Description: Robust worms, usuallytightlycoiled,
coccidian oocysts and schistosomelike eggs, has resemblingfirst-stagepinworms(Fig. 1). Mouth sur-
been '4C-dated at 10,500 + 180 yr; the other 3 roundedby 3 bilobedlips (Fig.2);tail sharplypointed
infected samples were not dated. The weighted (Fig. 3). Posteriorend of esophagusexpandedinto a
average of the youngest 10 samples of dung de- bulb,characteristicof the order(Fig. 1, arrow).Length
posited in the cave was within a few years of (n = 7) 13-20 x 126-198 (16.8 x 159).
11,000 BP (before present) (Martin et al., 1985).
All specimens are presumed to be of this age or Taxonomic summary
Typehost: Shastagroundsloth, N. shastensis.
greater. Typelocality: RampartCave, ca. 7 km upstream
Parasites were found in 4 of the 7 (57%) sam-
from Pierce'sFerry,36?06'N, 113?56'W,GrandCan-
ples. There were juveniles of 2 nematode species, yon, Arizona.
2 morphotypes of coccidian oocysts, and eggs of
2 helminth species. Fungal spores and pollen were Material deposited: Phototype of representative
abundant and had to be differentiated from pos- structuresfrom 1 juvenile worm and 10 syntypes in
the USNMPCNo. 82076.
sible oocysts. The condition of the nematodes
precluded detailed observations and measure- Remarks
One dungball containedmany nematodejuveniles
ments.
(about10worms/dropof sediment)thatresemblefirst-
The International Code of Zoological Nomen- stagepinworms.Adultnematodeswerenot found,sug-
clature (Art. 42 (b)(i)) (Ride et al., 1985: 83) makes gestingthat this does not representa coprophagous,
provision for "... certain assemblages of taxo- free-livingform. This species was found in only 1 of
nomic convenience known as 'collective groups'." the 7 dungballs examined.
Included are species known only from fossil trac-
es (ichnotaxa) and those known only from im- Strongyloides shastensis n. sp.
mature specimens, adult forms of which cannot (Figs.4-8)
be determined. Any of those can be reallocated
to the correct genus if it is later discovered. Ex- Description:Slenderworms,only slightlycoiled(Fig.
amples given are Agamodistomum Stossich, 1892 4). Head small, lackingconspicuouslips. Esophagus
(Trematoda), Agamofilaria Stiles, 1907 (Nema- usuallydetachedfrommouthand difficultto interpret
toda), and Stelloglyphus Vyalov, 1964 (trace fos- (Fig.5);in somespecimensin whichnot detachedfrom
sil), among others. Presumably, the frequent use mouth,a pairof rodlikestructuresarepresent(Fig.6).
of "agamo" as a prefix to these collective group Esophagusthicker at junction with intestine, repre-
genera stems from its derivation: a- (Gr., not, sentinga pseudobulb.Tail (Fig. 7) long and pointed,
without) and gam- (Gr., marriage). In applying resemblinga first-stagejuvenileof StrongyloidesS. ome
names to the organisms we found, we sought to worms in processof molting (Fig. 8). Length(n = 7)
follow this basic concept. 23-27 x 270-349 (24.4 x 305.3).

Numerous bodies, presumably helminth eggs Taxonomic summary
representing 2 species, were found in 3 dung balls. Typehost: Shastagroundsloth, N. shastensis.
One kind (Fig. 9) is conspicuously pointed at 1 Typelocality: RampartCave, ca. 7 km upstream
end and may have a subterminal operculum at
the other. The outer surface of the egg capsule is from Pierce'sFerry,36?06'N, 113?56'W,GrandCan-
pitted (Fig. 10). Except for the operculum, these yon, Arizona.
eggs look somewhat like schistosome eggs. These
eggs were found in 3 of the 7 dung balls and Material deposited: Phototype of representative
measured (n = 8) 33-50 x 63-90 (43.0 x 81.9). structuresfrom 1juvenilewormandabout 10syntypes
in the USNMPCNo. 82075.
A second type of object that resembled a hel-
minth egg was found in only 1 of the dung balls. Remarks
Its thick wall gives some resemblance to a tox- One dung ball contained numerous nematodeju-

veniles thatbearstrikingsimilaritiesto juvenile Stron-
gyloides.Adult nematodeswerenot found, suggesting
thatthesespecimensdo not representa coprophagous,
free-livingform. This specieswas found in 2 of the 7
dung balls examined.

Archeococcidia n. gen.
Reserved for structures that are oocystlike in
general size, shape, and appearance; that come

SCHMIDETTAL.-PARASITEOSFEXTINCSTHASTAGROUNDSLOTHS 813

FIGURES1-8. Photomicrographsof juvenile nematodesextractedfrom the desiccatedfeces of the extinct
Shastagroundsloth,Nothrotheriopshastensis,fromRampartCave,GrandCanyon,Arizona.Figures1-3, bars
= 15 um; Figures4-8, bars = 30 Aim.1. Lateralview of entirejuvenile of Agamofilariaoxyuran. sp.; note
esophagealbulb (arrow).2. Enlargedhead of A. oxyurashowing3 bilobedlips of mouth.3. Pointedtail of same
species. 4. Lateralview of entirejuvenile of Strongyloidesshastensisn. sp.; note pointed tail and esophagus
pulledawayfrommouth.5. Enlargemenot f anteriorendof S. shastensisjuvenile;notehowesophagusis detached
frommouth.6. Anteriorends of some S. shastensisjuveniles show 2 rodlikestructures(arrows)seen only when
the esophagushas not separatedfrom the mouth. 7. Enlargedlateralview of tail showinglocation of anus. 8.
Same species showingmoltingto second stage.

from dried, petrified, or mummified feces or bod- Taxonomic summary
ies of extinct animals; and that, because of their Typehost: Shastagroundsloth, N. shastensis.
antiquity, are unsporulated and, therefore, not Typelocality: RampartCave, ca. 7 km upstream
able to be placed into an appropriate genus.
from Pierce'sFerry,36?06'N, 113?56'W,GrandCan-
Archeococcidia antiquus n. sp. yon, Arizona.
(Figs.12, 13)
Materialdeposited: Phototypeof unsporulatedoo-
Description: Unsporulatedcoccidianoocysts ellip- cyst in the USNMPCNo. 82073.
soidalwith pittedouterwall (Fig. 13)(n = 8) 19-21 x
21-23 (19.6 x 22.1). Inner mass disrupted,no indi- Remarks
cationof sporocystformationcould be seen, andthus, An abundanceofunsporulatedcoccidianoocysts(Fig.
it is impossibleto placeit in any knowngenus.
12) was found in 1 dungball. It is likely an eimerian
as all known coccidians describedfrom edentatesto



SCHMIDETTAL.-PARASITEOSFEXTINCSTHASTAGROUNDSLOTHS 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
from Pierce's Ferry, 36?06'N, 113?56'W, Grand Can- LITERATURECITED
yon, Arizona.
Material deposited: Phototype of unsporulated oo- BANDONIS, . M., ANDD. W. DUSZYNSKI.1988. A plea
cyst in the USNMPC No. 82074. for improved presentation of type material for coc-
cidia. Journal of Parasitology 74: 519-523.
Remarks
BETANCOURTJ., L., T. R. VANDEVENDERA, ND P. S.
A second kind of oocyst, not as common as A. an- MARTIN. 1990. Packrat middens: The last 40,000
tiquus, was found in another dung ball. Oocysts of this years of biotic change. University of Arizona Press,
form were found only in 1 of the 7 dung balls examined. Tucson, 468 p.

In summary, 4 of 7 (57%) dung balls from the extinct FERREIRAL, . F., A. ARAUJO,U. CONFALONIERMI,.
Shasta ground sloth from Rampart Cave, Arizona, had CHAMEA, NDD. C. GOMES. 1991. Trichuris eggs
parasite stages in them. One dung ball had only a few in animal coprolites dated from 30,000 years ago.
juveniles of S. shastensis. Another had oocysts of A. Journal of Parasitology 77: 491-493.
antiquus (Figs. 12, 13) and schistosomelike eggs (Figs.
9, 10). A third ball had many juveniles of S. shastensis FRY,G. F., ANDJ. G. MOORE. 1969. Enterobius ver-
(Figs. 4-8) and both schistosomelike and small, thick- micularis: 10,000-year-old human infection. Sci-
walled eggs (Fig. 11). The fourth infected dung ball had ence 166: 1620.
oocysts of A. nothrotheriopsae (Fig. 14), schistosome-
like eggs, and juveniles of A. oxyura (Figs. 1-3). GoocH, P. S. 1973. Helminths in archaeological and
pre-historic deposits. Commonwealth Institute of
DISCUSSION Helminthology, Annotated Bibliography No. 9, St
Albans, Herts, England, 8 p.
Paleoparasitology is attracting an increasing
number of investigations (Kliks, 1983, 1990; HANSENR, . M. 1978. Shasta ground sloth food hab-
Reinhard et al., 1987; Ferreira et al., 1991). For its, Rampart Cave, Arizona. Paleobiology 4: 302-
annotated bibliographies, see reports by Hantz- 319.
schell et al. (1968), Gooch (1973), Wilke and Hall
(1975), and Hore (1985). Nearly all previous HANTZSCHELWL,., F. EL-BAZ,AND G. C. AMSTUTZ.
reports have been on human, or presumably hu- 1968. Coprolites: An annotated bibliography.
man, materials. Memoirs of the Geological Society of America 108:
1-132.
Two reports are known to us concerning par-
asites of sloths from the Pleistocene Epoch. Rin- HORNE,P. D. 1985. A review of the evidence of
guelet (1957) described "probable remains of human endoparasitism in the pre-Columbian New
nematode eggs" from dung of the giant sloth, World through the study of coprolites. Journal of
Mylodon listai, in Tierra del Fuego, Chile. The Archaeological Science 12: 299-310.
eggs were elliptical, 31.5-49.5 x 18.7-29.2 in
size. KLIKSM, . M. 1983. Paleoparasitology: On the origins
and impact of human-helminth relationships. Hu-
Laudermilk and Munz (1938) studied dung man Ecology and Infectious Diseases 11: 291-313.
balls of "Nothrotherium" (=N. shastensis) also 1990. Helminths as heirlooms and souvenirs:
from Rampart Cave. Although their paper was
concerned with the plants making up the dung A review of New World paleoparasitology. Para-
balls, they reported, "... perfectly preserved sitology Today 6: 93-100.
nematode worms as well as their eggs were abun- LAUDERMILKJ., D., ANDP. A. MUNZ. 1938. Plants
dant." Remains of their material are not known in the dung of Nothrotherium from Rampart and
Muav Caves, Arizona. Carnegie Institution of
to exist. This is the only previous report of par- Washington, Publication No. 487: 271-281.
asites of N. shastensis. Further studies probably LEVINEN, . D. 1988. The protozoan phylum Apicom-
would uncover other parasite remains, and a de- plexa, Vol. I. CRC Press, Inc., Boca Raton, Flor-
tailed chronological sequence might be of inter- ida, 203 p.
est to those seeking causes of extinction. MARTIN,P. S. 1987. Late Quaternary extinctions:
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ACKNOWLEDGMENT of the fourth international symposium on accel-
eration mass spectrometry, H. Gove, A. E. Lith-
Thanks are due Norman D. Levine, Professor erland, and D. L. Moore (eds.). Nuclear instru-
Emeritus, The University of Illinois, who looked ments and methods in physics research B29. North
at photomicrographs of our unsporulated oocysts Holland Publishing Company, Amsterdam, p. 179-
and gave his opinion that he too thought they 186.

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