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3-30-2016
Distribution and Paleobiology of Hibernation in Fossil
Distribution and Paleobiology of Hibernation in Fossil
Ground-Dwelling Squirrels from the Great Plains, USA
Dwelling Squirrels from the Great Plains, USA
Randy Sanchez
Andrews University, [email protected]
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Sanchez, Randy, "Distribution and Paleobiology of Hibernation in Fossil Ground-Dwelling Squirrels from the Great Plains, USA" (2016). Honors Theses. 142.
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Abstract
Hibernation is a widespread phenomenon present across mammalian taxa, including in many
ground-dwelling squirrels (family Sciuridae). Prior work has shown that a hibernation mark can be
identified in the ever-growing incisors of these ground squirrels through surface inspection. In this
study, we inspected fossil incisors, originating from the Great Plains, from the C.W. Hibbard
collec-tion at the University of Michigan for features associated with hibernacollec-tion marks in modern species.
We noted hibernation mark-like features in several fossil ground squirrel incisors from the genera
Otospermophilus, “Spermophilus”, and Urocitellus, ranging stratigraphically from the early Pliocene to the late Pleistocene and providing the oldest known record of hibernation for ground squirrels.
Sanchez |3 Introduction
Hibernation is a phenomenon consisting of a decrease in metabolic activity along with a
drop in body temperature and heart rate, characterized by a prolonged state of dormancy (Williams
et al. 2014). Although hibernation is present across a wide range of mammalian taxa, it has been
most extensively studied in the rodent family Sciuridae, which includes the ground squirrels and
their relatives. Most genera of ground squirrels are capable of hibernation, but the ones relevant to
our study include Otospermophilus (Oaks et al. 1987) and Urocitellus (Michener 1984). The geographic
range of Otospermophilus has varied since the Pliocene, but today encompasses much of Mexico
northward through much of the western United States (Oaks et al. 1987). Urocitellus can usually be
found in central and western North America and also northeastern and central Asia (Helgen et al.
2009).
Studies with ground squirrels have shown that hibernation affects the growth of their
ever-growing incisors. Incisors are made up of enamel and dentin deposits, and in rodents these deposits
are laid down on a daily basis throughout the animal’s lifetime. The position on the incisor where
the enamel meets with the dentin is known as the enamel-dentin junction (EDJ). This junction is
characterized by a pair of reflective lines that run parallel to the EDJ in ground squirrels (Goodwin
et al. 2005). Due to severe metabolic reductions during hibernation, the deposition of enamel and
dentin is interrupted, creating physical abnormalities on the surface of the incisor that are visible
un-der a stereo light microscope. These abnormalities attributed to hibernation (a hibernation mark)
usually include a diagonal disruption to the pair of reflective bands on the medial surface of the
inci-sor adjacent to the EDJ, irregularities in the medial enamel, depression in the dentin, and/or often
fine and indistinct dentin increments (Goodwin et al 2005). The hibernation mark was first
identi-fied in marmots, genus Marmota (Rinaldi 1999) and subsequently confirmed in Urocitellus (Goodwin
(Klevezal and Lobkov 2008). This indicates the broad distribution of the hibernation mark across
taxa of hibernating ground squirrels. Prior study of fossil ground squirrels has recorded hibernation
as far back as the Pleistocene in Porcupine Cave, Colorado (Goodwin et al. 2005).
Data from stable isotope studies from the Great Plains characterized the Pliocene time
peri-od as being different in climate when compared to the mperi-odern-day environment. During the
Plio-cene-Pleistocene time period, there was a shift in climate and in plant ecology of the region, with
isotope data showing a step-wise shift from warmer climate and C3-dominated habitat in the
Plio-cene to that of cooler climate and C4-dominated grasslands in the early PleistoPlio-cene (Fox et al. 2012a;
2012b). This shift in vegetation/climate is not well understood, but provides a broad framework for
interpreting the paleobiology of fossil ground squirrels from the sequence.
Our study investigated fossil ground-squirrel incisors from the Claude W. Hibbard
Pliocene-Pleistocene Mammalian collection from the University of Michigan Museum of Paleontology. This
collection was chosen because it provided a rich source of fossils that was readily available to our
study. Hibbard’s collection focused on the central United States, the Great Plains, and covered the
Pleistocene-Pliocene time period, which ranges from 11,700 thousand to 5.3 million years ago based
on the standard radiometric chronometry. Most of the fossils collected by Hibbard were
concentrat-ed in the Meade Basin of southwestern Kansas, but other fossils from Oklahoma, Nebraska, and
Idaho were also included. The incisors were inspected for hibernation marks in order to elucidate
the history of hibernation among ground squirrels of the region, set in context of changes in
pale-oenvironments.
Methods
The Claude W. Hibbard Collection was accessed at the University of Michigan Museum of
Sanchez |5 rodent incisors, which included those of squirrels. We initially attempted to pull out isolated squirrel
incisors from a large batch of rodent incisors, but found this to be unreliable. We then focused on
specimens whose incisor was in or associated with a known squirrel jaw. Based on a refined search
image, we were also able to identify a few additional isolated squirrel incisors for inspection.
All squirrel incisors were then analyzed under a light microscope for any physical
abnormali-ties on the surface of the incisor that resembled a hibernation mark. A modern squirrel incisor with
a known hibernation mark, and images of hibernation marks from prior work (Goodwin et al. 2005),
were used as a comparison when identifying hibernation mark-like features on these incisors. These
incisors originated from the Buis Ranch fauna in Oklahoma; Fox Canyon, Jones, and Rexroad 3
faunas in Kansas; the Sand Draw fauna in Nebraska; and the Hagerman fauna in Idaho.
The generic taxonomy proposed by Helgen and colleagues was applied when possible to
fos-sil species; this taxonomy raised previous subgenera to genera, resulting in the elimination of
Sper-mophilus from North America (Helgen et al. 2009). However, we refer to the genus “SperSper-mophilus” in quotation marks for “S.” meltoni due to the uncertainty of which genus it belongs to. This holotype
was collected by Hibbard in 1965 from the upper part of the Keim Formation in Brown County,
Nebraska and described by Skinner and Hibbard (Skinner et al. 1972).
For each specimen examined, the catalog number and locality were recorded along with a
brief description of the incisor and its characteristics. A photograph was taken under the microscope
if the specimen had a probable hibernation mark and when available, the dimensions of the incisors
were obtained. After these incisors were analyzed, those with a possible hibernation mark were
plot-ted geographically and stratigraphically to show physical locations and most importantly their
Results
Incisors examined – We inspected 19 incisors from 6 localities ranging from Oklahoma in the South, to the Nebraska and Idaho in the north and northwest (Table 1). Of these specimen, four of
them showed features similar to those caused by hibernation.
Descriptions of fossil incisors with a possible hibernation marks –The holotype for “Spermophilus” mel-toni (UMMP 52167) from the late Pliocene Sand Draw fauna, NE had an abrupt disruption in the pair of reflective bands that run parallel to the EDJ on the medial side (Figure 1A). The disruption
creates a diagonal feature in the upper reflective band. Fine dentin increments were also observed
just basal to the diagonal (Figure 1B). An incisor of Urocitellus richardsonii (UMMP 56482) from the
late Pleistocene Jones fauna, KS exhibited a slight depression in the dentin on its medial side, and
irregularities in enamel adjacent to the EDJ associated with and just basal to the depression (Figure
2). The incisor of Otospermophilus rexroadensis (UMMP 60813) from the mid-Pliocene Rexroad 3
lo-cality, KS exhibited a depression in the dentin on the medial side of the incisor with narrow
incre-ments that looked similar to features seen on incisors with hibernation marks. A short diagonal
dis-ruption in the pair of reflective lines of the EDJ was also evident just apical to the zone of
depres-sion (Figure 3). An incisor of Otospermophilus sp. (V56578) from the Pliocene Buis Ranch fauna, OK
displayed some abnormalities of the reflective bands of the EDJ but did not display other physical
features usually associated with hibernation (this incisor is not pictured). Fossils with a probable
hi-bernation mark ranged from northern Oklahoma to northern Nebraska and from the early Pliocene
to the late Pleistocene (Figure 5).
Discussion
While some of the incisors we examined showed a very probable hibernation marks – S.
Sanchez |7 not as convincing because it lacked other abnormalities normally found in a hibernation mark
(Goodwin et al. 2005). For the other incisors, there was a greater confidence level due to more than
one feature usually observed in modern day marks, including the diagonal disruption in the medial
surface of incisors’ enamel (Goodwin et al. 2005). Prior work has shown this feature in fossil
Urocitel-lus elegans from the mid-to late Pleistocene (Goodwin et al. 2005). Our study documented hiberna-tion in the middle Pliocene and thus provides the oldest record of hibernahiberna-tion in fossil ground
squir-rels.
We also provide the first record of hibernation in a pre-modern environment of the Great
Plains. Currently, the ecosystem dominating the Great Plains is a moderate temperate grassland with
a C-4 dominated plant ecosystem (Fox and Koch 2003). Although the paleoclimate of the Great
Plains during the Pliocene is not well characterized, some studies have suggested that there was a
warmer, more arid ecosystem in the central United States in contrast to today’s environment (Martin
et al. 2008). Whatever the environment, we can assume it supported squirrels that employed
hiber-nation during their life history even if warmer than the modern day environment. Of particular
in-terest, the extinct species “Spermophilus” meltoni was a hibernator.
The Pleistocene brought about changes in the ecosystem and the climate that was present
during the Pliocene. Climate cooled and a transition in the vegetation from a C3-dominated
envi-ronment to a C4-dominated envienvi-ronment occurred (Fox et al. 2012a; 2012b). Therefore, it is no
sur-prise that the incisor of Urocitellus richardsonii from the Pleistocene had a hibernation mark given the
cooling climate of the later Pleistocene and the fact that the species is an obligate hibernator at
pre-sent.
Our study could be pushed further by expanding coverage geographically. The stratigraphic
time period can also be expanded earlier than the Pliocene to the Miocene or even earlier. Data from
together information and make a well-formed hypothesis about the climate during the Pliocene and
what occurred during the Pliocene-Pleistocene ecological shift.
Literature Cited
Fox DL, Koch PL: 2003. Tertiary history of c4 biomass in the great plains, USA. Geology. 31(9):809-812.
Fox DL, Honey JG, Martin RA, Pelaez-Campomanes P. 2012. Pedogenic carbonate stable isotope record of environmental change during the neogene in the souther great plains, southwest kansas, USA: Carbon isotopes and the evolution of c4-dominated grasslands. Geological Society of America Bulletin. 124(3-4):444-462.
Fox DL, Honey JG, Martin RA, Pelaez-Campomanes P. 2012b. Pedogenic carbonate stable isotope record of environmental change during the neogene in the southern great plains, southwest kansas, USA: Oxygen isotopes and paleoclimate during the evolution of c4-dominated grasslands. Geological Society of America Bulletin. 124(3-4):431-443.
Goodwin HT, Ryckman EM. 2006. Lower incisors of prairie dogs (cynomys) as biorecorders of hibernation and season of death. Journal of Mammalogy. 87(5):1002-1012.
Goodwin HT, Michener GR, Gonzalez D, Rinaldi CE. 2005. Hibernation is recorded in lower incisors of recent and fossil ground squirrels (spermophilus). Journal of Mammalogy. 86(2):323-332.
Helgen KM, Cole FR, Helgen LE, Wilson DE. 2009. Generic revision in the holarctic ground squirrel genus spermophilus. Journal of Mammalogy. 90(2):270-305.
Kisser B, Goodwin HT. 2012. Hibernation and overwinter body temperatures in free-ranging thirteen-lined ground squirrels, ictidomys tridecemlineatus. The American Midland Naturalist. 167(2):396-409.
Kisser BC. 2009. The relationship between dental growth increments and body temperatures from late summer through early spring in free-ranging thirtheen-lined ground squirrels
spermophilus tridecemlineatus. Andrews University.
Klevezal, G.A. and Lobkov, V.A. 2008. Daily Increments and the Hybernation Zone on the incisor Surface of Ground Squirrels of the Genus Spermophilus. ZOOLOGICHESKIĬ
ZHURNAL. 87(12):1495–1503.
Martin RA, PelÁEz-Campomanes P, Honey JG, David L. Fox, Zakrzewski RJ, Albright LB, Lindsay EH, Opdyke ND, Goodwin HT. 2008. Rodent community change at the
pliocene-pleistocene transition in southwestern kansas and identification of the microtus immigration event on the central great plains. Palaeogeography, Palaeoclimatology, Palaeoecology. 267(3-4):196-207.
Michener GR. 1984. Age, sex, and species differences in the annual cycles of ground-dwelling sciurids: Implications for sociality. In: Murie JO, Michener GR, editors. The biology of ground-dwelling squirrels. University of Nebraska Press. p. 81-107.
Oaks EC, Young PJ, Gordon L. Kirkland J, Schmidt DF. 1987. Spermophilus variegatus. The American Society of Mammalogists. (272):1-8.
Rinaldi C. 1999. A record of hibernation in the incisor teeth of Recent and fossil marmots (Marmota flaviventris). Proceedings of the 11th International Symposium on Dental Morphology. 112-119.
Sanchez |9 Skinner MF, Hibbard CW, Gutentag ED, Smith GR, Lundberg JG, Holman JA, Feduccia JA, Rich
PV. 1972. Early pleistocene pre-glacial and glacial rocks and faunas of north-central nebraska. Bulletin of the American Museum of Natural History. 148(1):1-148.
Williams CT, Barnes BM, Kenagy GJ, Buck CL. 2014. Phenology of hibernation and reproduction in ground squirrels: Integration of environmental cues with endogenous programming. Journal of Zoology. 292(2):112-124.
Figures and Tables R em ar ks U M M P V 56 57 8 w ith p os si-ble H M . No in cis or s a h ad v is ib le sig ns o f a H M . U M M P 6 08 13 w as w ig gle fr ee f ro m ja w , h ad a c le ar HM. No in cis or s h ad v is ib le s ig ns of a H M . U M M P 5 21 67 w ith H M . U M M P 5 64 82 w ith H M . n 4 2 1 6 2 4 Ge nu s O tos pe rmop hil us Ictid omy s O tos pe rmop hil us N/A Sper mop hil us U rocite llu s L oc al it y B uis Ra nc h, O K Fo x C an yo n, K S Re xr oa d 3 , K S H ag er ma n, ID Sa nd Dr aw , NE Jo ne s, K S Ag e E ar ly P lio ce ne E ar ly P lio ce ne M id P lio ce ne L at e P lio ce ne L at e P lio ce ne L at e P le is to ce ne T ab le 1 D at a of in ci so rs a na ly ze d. Th e ta bl e be lo w p ro vi de s a su m m ar y of in fo rm at io n ab ou t t he in ci so rs th at w er e an al yz ed, li st ed fr ea rli es t i n th e re co rd to la te st . T he ta bl e di sp la ys th e ag e an d lo ca lit y of th e fa un a an al yz ed, th e ge nu s of th e gr ou nd sq ui rr el s w ho se in ci so w er e an al yz ed in th at f au na , t he n um be r of in ci so rs a na ly ze d (n ), an d so m e re m ar ks (i f n ec es sa ry ) a bo ut w ha t w as f ou nd f or e ach lo ca tio
Sanchez |11
A)
B)
Figure 1"Spermophilus" meltoni holotype (UMMP 52167) from Sand Draw, NE. (A) Lower right incisor of "Spermophilus" meltoni holotype, inmedial view. Apical to the right. Two slightly dif-ferent orientations display (A) diagonal disruption of enamel adjacent to the EDJ (in box), and (B) fine increments towards the base of the incisor (surrounded by the dashed rectangle). Scale incre-ments = mm.
Figure 2 Right lower incisor of Urocitellus richardsonii from Jones fauna, Kansas (UMMP 56482), in medial view, displaying the zone of depressed dentin (dashed polygon) and irregular enamel (arrow). Apical to the right. Scale increments = mm.
Sanchez |13
Figure 3 Lower right incisor of Otospermophilus rexroadensis from Rexroad 3 fauna, Kansas (UMMP 60813), in medial view. The dashed polygon outlines a depression in the den-tin on the medial side of the incisor. Above the depression (seen in the panel on the top), there is an overlap of a new enamel sleeve over a pre-existing sleeve. Scale increments = mm.
Figure 4 Stratigraphic distribution of incisors with possible hibernation marks. The incisor specimen that had probable signs of hibernation were plotted stratigraphically below. The orange dot represents U. richardsonii, the purple dot represents the “S.” meltoni holotype, the red dot repre-sents O. rexroadensis, and the blue dot reprerepre-sents Otospermophilus sp.
Period Epoch Qu at er na ry Holocene Pleistocene Te rt ia ry Pliocene Miocene U. richardsonii “S”. meltoni O. rexroadensis Otospermophilus sp.
