Table Of ContentDromiciops gliroides Thomas, 1894, Last of the
Microbiotheria (Marsupialia), with a Review of the
Family Microbiotheriidae
Philip Hershkovitzf
Abstract
The tiny Chilean and bordering Argentinian endemic Dromiciops gliroides Thomas, lone
survivor of the South American Cohort Microbiotheriomorphia, is basal to all known marsu-
pials. Indications are that the ancestral microbiothere may have originated in South America
during the Late Mesozoic in a cool, humid, low-latitude biome dominated by a beech-bamboo
(Nothofagus-Chusquea) plant association, the bamboo being its primary nesting material. A
postulated worldwide climatic warming initiated a southward migration ofcool-loving elements
of the Southern Hemisphere. The philopatric microbiotheres evidently clung to their Nothofa-
gus-Chusquea niche and nesting material as the association shifted from subequatorial into
Patagonian and Antarctic latitudes. A climatic reversal during the Tertiary returned the Noth-
ofagus-Chusquea-vmcvobioihcvc association to Patagonian latitudes. An expanding arid scrub
savanna farther north, however, halted the Nothofagus community shift in that direction. At the
same time, habitat was being lost to the increasingly colder climate advancing from the south.
Extinction followed. The most northern progression of the association was in the west, where
rains intercepted by the rising Andes provided a favorable environment. The Nothofagus-
Chusquea-microbiothere association now survives in the cool, humid Valdivian region ofChile
and its narrow Argentine extension as a relictual enclave sharply delimited by the warmer arid
environment to the north and the colder, drier environment to the south.
The present ecogeographically restricted Cohort Microbiotheriomorphia is described and
compared with its sisterCohort Didelphimorphia, which, by virtue ofits adaptability, fecundity,
and diversity, had dispersed into all continents. The narrow climatically controlled distribution
and what little is known ofthe life history and anatomy ofthe single surviving microbiothere,
Dromiciops gliroides, are reviewed.
Introduction recognize the relationship between the living
Dromiciops and the extinct microbiotheriid mar-
The monito del monte, Dromiciops gliroides supial then known only from the Miocene.
Thomas (frontispiece; Plates 1, 2), a mouse opos- The Microbiotheriomorphia, with its single
sum with a simian vernacular name, is the lone known family Microbiotheriidae, was reviewed
survivor of the South American marsupial family by Marshall (1982), with attention given to cra-
Microbiotheriidae Ameghino, 1887. The monito nial, dental, and external characters. The clade
del monte and a dozen or so known extinct spe- was treated as a family of Didelphoidea, its dis-
cies of the same family compose the monophy- tinctive characters unperceived except for men-
letic Cohort Microbiotheriomorphia Ameghino. tion of small canine teeth. It has since been de-
Togetherwith Cohort DidelphimorphiaGill, 1872, termined (Hershkovitz, 1992a) that microbiothe-
it constitutes the Infraclass Marsupialia, also riids are monophyletic and must have arisen at
known as Metatheria. Reig (1955) was the first to some time before the divergence of didelphoids,
FIELDIANA: ZOOLOGY, N.S., NO. 93, MAY 28, 1999, PP. 1-60
Plate 1. Dromiciops gliroides, natural size: top, note incrassate prehensile tail displayed by adult; bottom, same
individual cupped in hand. Animal captured in Chile by Dr. Bruce Patterson and donated to the Chicago Zoological
Society, Brookfield, Illinois. Photograph by Mike Greer; original photograph courtesy of the Zoological Society
(reproduced from Hershkovitz, 1992a).
which are characterized by their distinctive stag- of south central Chile, from the latitude of Con-
gered lower third incisor (Hershkovitz, 1995). ception (ca. 37°00', 72°30') tothe southernborder
of Isla Chiloe (ca. 44°00', 72°00'), thence east-
Order Microbiotheria Ameghino, ward into adjacent parts of Argentina in western
1887, Cohort Microbiotheriomorphia Neuquen and southwestern Rio Negro. PAST:
Ameghino Successively: Upper El Molino-Santa Lucia For-
mation, Cochabamba, south central Bolivia (Early
Distribution (Figs. 1-4)—PRESENT: Cool, Paleocene; see Marshall et ah, 1995, for details);
humid, dominantly Nothofagus-Chusquea forests Itaboraian Formation in Rio de Janeiro, south-
Plate 2. A, Arboreal nest of Dromiciops gliroides constructed of moss and the leaves of bamboo (Chusquea
culeou). B, Nestling. C, Young taken from back ofmother. (Copied from photographs by Mann, 1958.)
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HERSHKOVITZ: LAST OF THE MICROBIOTHERIA
60c 55c
65e
"35°
35°
55c
—
40°
40°
60°
.fCaradonVaca
fCanodonHordIo
45°
PuertoDeseado
MICRDBIOTHERIIDAE+
50°
MonteLeon
LaCueva
OueqiiaQuanada
50° SantaCruz
MonteObservacion
KillikAikeNorte(Felton'sEstarcia
RfoGallegos
C5^
Fig. 1. Distributions of living Dromiciops gliroides in Chile and bordering Argentina (see Fig. 19, p. 29, for
locality records, and p. 9 for names and ages ofextinct Oligocene-Miocene microbiotheriids in southern Argentina).
FIELDIANA: ZOOLOGY
Fig. 2. Geoclimatic stages in the odyssey of the Nothofagus-Chusquea-m'icrob'wtheriid association in southern
South America and Antarctica. Stage 1: South central Bolivia (Early Paleocene). Stage 2: Sao Jose de Itaboraf, Rio
de Janeiro (Middle Paleocene). Stage 3: La Meseta Formation, Seymour Island. Antarctic Peninsula (Eocene). Stage
4: Reversion to southern Patagonia (Argentina) (Oligocene-Miocene), continuing into (Stage 5) central Chile (Ter-
tiary-Recent). Arrows point to direction of migration with changing climates.
eastern Brazil (Middle Paleocene);Colhuehuapian eutherian-like grade characters may have ap-
and Santacrucian formations from Lago Colhue- peared in latest Jurassic or earliest Cretaceous. Its
Huapi (46°30'S) to Rio Gallegos (51°36'S), Chu- origin may have been from the same metatherian
but and Santa Cruz provinces, Argentina (Oligo- stock that later gave rise to Cohort Didelphimor-
cene, Miocene); La Meseta Formation, Seymour phia, distinguished by the staggered i„ precaudal
Island, Antarctic Peninsula, Weddellian Province, cloaca, and other derived characters fully evolved
Antarctica (Eocene). by late Early Cretaceous (Hershkovitz, 1982,
1992a, 1995) but inferentially not before the ap-
pearance ofthe microbiotheriids, which lackthese
Biological Origin
derivedcharacters. The tree showing phylogenetic
Monophyletic Microbiotheriomorphia with its position and relationship of didelphoids (Hersh-
combination of prototherian-, metatherian-, and kovitz, 1992a, p. 210) is subject to modification
HERSHKOVITZ: LAST OF THE MICROBIOTHERIA
FIELDIANA: ZOOLOGY
within a Metatheria perceived as independently South America, New Zealand, and encompassed
differentiated from a therian stock. islands. The southern provincial border was de-
termined as the Transantarctic Mountain front; the
northern limit was said to coincide with the edge
of the continental shelf, including southern Ar-
Geographic Origin gentina and central Chile (map. Fig. 2, p. 5).
The oldest known didelphoids are North Amer-
ican Albian age (late Early Cretaceous: Adinodon
[Hershkovitz, 1995], Kokopellia [Cifelli, 1993],
and Holoclemensia [Slaughter, 1968a,b]; see also Weddellian Land Habitats
Turnbull, 1995). Both the phylogenetically older
microbiotheres and the geologically younger di-
delphoids are known as fossils from the Bolivian Forest-covered habitats within atemperate Ant-
El Molino Formation of earliest Paleocene (Mar- arctic zone such as the Meseta Formation of the
shall et al., 1985, 1995; Marshall & de Muizon, peninsular Seymour Island (Fig. 2) were known
1988). It has been argued that the earlier Albian to exist during Permian through Early Tertiary pe-
age of some didelphoids presupposes a North riods (Seward, 1914). Woodburne andZinsmeister
American origin of marsupials, microbiotheres (1984, p. 935) note that the "presence of large
not having been distinguished at the time from the logs (up to a meter in diameter), together with
derived didelphoids. Microbiotheres, however, are otherplant debris indicates that the Antarctic Pen-
unknown in North America. All locality records, insula was still heavily vegetated during the Eo-
whether of extant or known extinct microbio- cene [and that] preliminary analysis of the abun-
theres, are from well south ofthe equatorin South dant palynomorph floras of the La Meseta For-
America, including one from the Antarctic Pen- mation [of Seymour Island] indicates that condi-
insula (Carlini et al., 1991; Goin & Carlini, 1995). tions on the northern part of the Antarctic
It appears, therefore, that the continent of mar- Peninsula were similar to present-day humid-tem-
supial origin is properly based on the phyloge- perature climates in Tasmania, New Zealand, and
netically basal South American or Weddellian mi- southern South America." Similar conclusions
crobiotheres and not the (tentatively) geologically were reached by Doktor et al. (1996) from the
older but phylogenetically younger North Ameri- plant and fish assemblages from the Eocene La
can didelphimorphs. Meseta Formation.
In my discussion ofmarsupial ankle bones and Dettman (1989, p. 89), in her paper "Antarc-
phylogeny (Hershkovitz, 1992a, p. 206), the hab- tica: Cretaceous cradle of austral temperate rain-
itat of the Microbiotheriomorphia was inadver-
forests?" observed that "fossil evidence from
tbeenetnlySoguivtehnAmaserNiocratnh. American. It should have Antarctica and closely associated regions in the
Cretaceous southern Gondwana assembly con-
firms that Antarctica was a Cretaceous originator
and dispersal region ofcertain elements oftoday's
Weddellian Biotic Province of southern hemispheric humid and prehumid for-
Antarctica ests. Antarctica origins are indicated for the fern
Lophosoria, podocarp gymnosperms, and several
The Weddellian Paleogene-Cretaceous Biotic lineages ofthe Proteaciae; migration to theirpres-
Province was distinguished by Zinsmeister (1976) entregions ofdistribution wasprobably step-wise.
on the basis of similarities between the late Cre- Antarctica also served as a Cretaceous dispersal
taceous and Early Paleocene shallow-water mol- corridor for other angiosperms represented today
luscan faunas of Antarctica, Australia, southern in mid to low latitude austral regions."
Fig. 3. Top.bamboo(Chusquea sp.) in secondgrowth forestofLaPetardStatePark. Iporanga,SaoPaulo. Bottom.
Chusquea in lowerstoryclearingofLaPetard State Park. Sao Paulo. Microbiothcriidsare not knowntohaveoccurred
in Sao Paulo (see map. Fig. 1, p. 4). Photographs by Barbara Brown, December 1989.
HERSHKOVITZ: LAST OF THE MICROBIOTHERIA
2mm
Chusquea culeou
Fig. 4. Leaves ofthe bamboo Chusquea culeou, used by Dromiciops for weaving its waterproofnest.
Weddellian Land Mammals burne and Zinsmeister (1984, p. 933), "the Sey-
mour Island polydolopids represent a sample ofa
The first land mammal known from Antarctica, mammal population that likely had been endemic
described by Woodburne and Zinsmeister (1984), to the region for about 10 Ma, and had actually
is the polydolopoid marsupialAntarctodolopsdai- dispersed from South America at about 50 Ma,
lyi from the Late Eocene of Seymour Island, when the group was most abundant and diverse
northern Antarctic Peninsula. The degree of bio- there. . . . We also conclude from the number of
logical differentiation from its nearest South specimens represented, and geological evidence
American relative suggested "a late Cretaceous . . . that the entry of polydolopids into Antarctica
presence of marsupials in Greater Antarctica and reflects waifdispersal via an archipelago between
their isolation in Australia by whatever means by southern South America and the Antarctic Pen-
the close ofthat period." In the opinion ofWood- insula rather than a continuous land connection."
FIELDIANA: ZOOLOGY
The overall evidence suggests, continue Wood- crept in. Compare, for example, lower canines of
burne and Zinsmeister (1984, p. 942), that "mar- numbers 2 and 6 in Marshall (1982, p. 47). Iden-
supials must have been present on Antarctica tification ofnumber 2 may be equivocal. Itcarries
sometime from the Late Cretaceous tothe Eocene. the same name and registry number, PU 15038,
The Oligocene and young—er marsupials on Aus- ofthe figured auditory region ofMicrobiotherium
tralia . . . require an earlier probably amuchear- tehuelchum (Marshall, 1982, p. 30), which is a
lier (because o—f their diversity in the Oligocene true microbiothere. Neither it nor the aforemen-
and Miocene) ancestor there or in a closely tioned figured canine belong to the same taxon or
neighboring place. That place was Antarctica to the neotype ofM. tehuelchum Ameghino, 1887
from at least 80 Ma and, diminishingly, to about (MLP36). The identification of Mirandatherium,
38 Ma ago." although not queried, requires reexamination. The
The recovery of a ground sloth "Megatherioi- Pediomyinae, generally classified as microbio-
dea" reportedby Carlini et al. (1991, p. 15) added therioid (cf. Marshall et al., 1990), are not so re-
another order ofSouth American mammals to the garded here. The named forms follow.
known Late Eocene fauna of the La Meseta For-
mation. Other remains in the same Seymour Is- Microbiotherium acicula Ame—ghino, 1891
land Formation and underlying Cross Valley (Marshall, 1982, p. 12) Santacrucian
members of the Sobral Formation (Paleocene) re- (Monte Observacion), Santa Cruz Prov-
ported by Carlini et al. (1991) are a "probable ince, Argentina (Miocene).
microbiotheriid, polydolops, birds and plants." Microbiotherium patagonicum Ameghino,
Isolated teeth ofthe unique South American deer- 1887 (Marshall, 1982, p. 14)—Santacru-
like "ungulates" representing the families Theri- cian, Santa Cruz Province, Argentina
dodontidae and Trigonostyliodae, recovered by (Miocene).
Bond et al. (1990, p. 3) from the Seymour Island Microbiotherium divisum A—meghino, 1902
Formation, are the first eutherians known for the (Marshall, 1982, p. 22) Colhuehuapian
region. beds, at the Barranca south of Lago Col-
Discovery by Pascual et al. (1992a,b) of a hue-Huapi, Chubut, Argentina (Miocene).
platypus (Monotremata) tooth in sediments ofthe Microbiotherium tehuelchum Ameghino, 1887
Banco Negro Inferior (45°30'S, 67°1l'W),Chubut (Marshall, 1982, p. 26)—Santa Cruz For-
Province, southern Patagonia or within the Pata- mation (Corriquem-Kaik; Quequa-Quema-
gonian Terrane, a subset of the Weddellian Prov- da; La Cueva; Monte Observacion; Killik
ince, added another biogeographic dimension to Aike) Santa Cruz, Argentina (Miocene).
the region. Microbiotherium praecursor Ameghino, 1898
(Marshall, 1982, p. 19)—"Cretaceo infe-
rior." Age and locality unknown.
Microbiotherium gallegosense Sinclair, 1906
Recorded Microbiotheres (Marshall, 1982, p. 35)—Santa Cruz For-
mation, N bank Rio Gallegos, Santa Cruz,
The 13 recorded extinct species, including 2 Argentina (Miocene).
undescribed (types, tentatively and dubiously as- IPachybiotherium acclinum —Ameghino, 1902
signed individuals), and 1 living species, distrib- (Marshall, 1982, p. 61) Colhuehuapian
uted among the 7 genera, are listed below (and in beds, probably—Barranca, Chubut, Argen-
Fig. 2). References to original descriptions, tax- tina (Miocene) microbiotheriid identity
onomies, synonymies, geographic data, and fig- questioned by Marshall (1982, p. 63).
ures of teeth and bone fragments of the first 8 ?Eomicrobiotherium gaudr—yi Simpson, 1964
species are from Marshall (1982). The determi- (Marshall, 1982, p. 58) Barranca, S Lago
nations of the fossils as microbiotheres are ac- Colhu—e Huapf, Chubut, Argentina (Mio-
cepted as tentative from Marshall (1982, 1987), cene) The genus reviewed by Marshall
Marshall and de Muizon (1988), and Marshall et (1982, p. 57) includes a second, unrevised
al. (1990). Description ofPucadelphys andinus is species, E. gutierrezidel Corro, but the mi-
from Marshall and de Muizon (1988). Discussion crobiotheriid affinities of the genus are
of the genus as a microbiothere is based on data problematic (Marshall, 1982, p. 59).
from Marshall et al. (1995). Pucadelph—ys andinus Marshall and de Muizon,
Some discrepancies in earlier reports may have 1988 Tiupampa local fauna. El Molino-
HERSHKOVITZ: LAST OF THE MICROBIOTHERIA
Santa Lucia Formation, Cochabamba, Bo- Biogeography: The Nothofagus-
livia (Early Paleocene). CTiMSrfjrwtfa-Microbiothere Association
Khasia co—rdillerensis Marshall and de Muizon,
1988 Tiupampa local fauna, El Molino Knowledge of living microbiotheres and nest-
Formation, Cochabamba, Bolivia (Early ing preferences indicates that the habitatofDrom-
Paleocene). — iciops is restricted to the Nothofagus-Chusquea
Mirandatherium alipioi Paula-Couto, 1962 association ofcentral Chile and bordering Argen-
Sao Jose de Itaborai, Rio deJaneiro, Brazil tina. Fossil evidence suggests that habitat prefer-
(Middle Paleocene); Marshall (1987, pp. ence of Dromiciops may have changed little in
114, 137, 148). time. The fossils also record the latitudinal trans-
Microbiotherium sp., Antarctica, La Meseta lations experienced by microbiotheres concomi-
Formation, Seymour Island, Antarctic Pen- tant with the climatic shiftings oftheir nearly ob-
insula, Late Eocene. Carlini et al. (1991); ligate Nothofagus-Chusquea-dominated habitat
Goin and Carlini (1995). — (Figs. 2-4).
Dromiciops gliroides Thomas, 1894 Isla de The oldest known microbiofherians are from
Chiloe; Los Lagos, Central Chile (Recent). the El Molino Formation in Tiupampa, Cocha-
&
bamba, Bolivia (Marshall de Muizon, 1988, p.
23; Marshall et al., 1995), now regarded as Early
Among 169 newly recovered dental specimens Paleocene. The next chronological record of mi-
of Colhuehuapian-Santacrucian age, Bown and crobiotherian occurrence is the mid-Paleocene It-
Fleagle (1994) distinguished the teeth of three aborafan of Rio de Janeiro, southeastern Brazil.
species of the genus Microbiotherium from Oli- This suggests a climatic change that shifted the
gocene and Miocene Patagonian rocks. The ma- Bolivian Nothofagus-Chusquea biome with its
terial included a new species of Colhuehuapian microbiotheres to the more southern or possibly
Microbiotherium, closestin sizetoM.praecursor, then cooler latitudes of coastal Rio de Janeiro.
a new Santacrucian Microbiotherium from the Continuation ofthe warming trend southward led
Pinturas Formation, intermediate in size between the Nothofagus-Chusquea-microbiothere associ-
M. acicula and M. praecursor, and the common ation into Antarctica during the Eocene (Carlini
Pinturas and Santacrucian M. tehuelchum. et al., 1991; Goin & Carlini, 1995) and led to the
Four partial skeletons and an extra skull ofPu- extinction of the Itaboraian species of the lower
cadelphys andinus Marshall and de Muizon latitudes.
(1988) recovered from the Santa Lucia Formation A climatic reversal brought freezing tempera-
of Tiupampa, about 95 km SE of Cochabamba tures into Antarctica, ending the southward ad-
(65°35'W, 18°02'S), Cochabamba Department, vance of the Nothofagus-Chusquea-microbio-
south central Bolivia, were studied by Marshall et there association and shunting it back into the
al. (1995). The geochronological positionhadpre- warmer Patagonia of the then Oligocene-Mio-
viously been, and continues to be, referred to as cene. The northward trend, however, was re-
the El Molino Formation. strained by the more rapidly advancing arid scrub
Skeletal measurements provided by Marshall et savanna arriving from the north, and habitat loss
al. (1995, p. 156) reveal Pucadelphys andinus to to the falling temperatures moving in from the
be relatively small, comparable in size to living south. Rains intercepted by the western versant of
caenolestids, marmosids, and the microbiothere the rising Andes provided scope for continuation
Dromiciops gliroides. Cranially, Pucadelphys, of the northward trend of the Nothofagus-Chus-
with its more or less evenly proportioned skull, gwea-microbiothere association into the Valdivian
resembles Dromiciops as contrasted with the long region of Chile and bordering parts of western
rostrate caenolestid and narrowly triangulate mar- Argentina during the Neogene. Continued favor-
mosid skulls. Notwithstanding, caenolestids, like able conditions at leastlocally intotheQuaternary
Pucadelphys, but unlike the others, are terrestrial, allowed the association to persist as a relict ofthe
non-prehensile-tailed, and locomotorily similar. once cool, humid Tertiary Antarctic climate (Fig.
Nevertheless, phylogenetic, morphological, and 2). The Tertiary microbiotheres east ofthe Andes
behavioral comparisons and alignments of Puca- in southern Argentina disappeared as their special
delphys made by Marshall et al. (1995) were with habitat gave way before the advancing aridity of
the least likely, most derived, and unrelated, stag- the north and the cold climate of the south.
gered-toothed didelphoid Didelphis. The Chilean-Argentine habitat of surviving
10 FIELDIANA: ZOOLOGY
