The burrowing behavior

of Ctenomys mendocinus (Rodentia)

by S. CAMIN, L. MADOERY and V. ROIG

Unidad de Ecologia Animal y Zoologia,

Institute Argentina de Investigations de Zonas Aridas,
Casilla de Correo n° 507, 5500 Mendoza, Argentina

Summary. - This paper describes the burrowing behavior of C. mendocinus in captivity.

A terrarium was utilized, where each animal was subject to a 23-minute trial. The digging
sequence showed by the animals was characterized by " scratching-kicking-scratching" and
pushing the removed soil backwards. Incisors were used only occasionally. All animals kept their
eyes closed while digging. From the data contributed by comparative anatomy it was inferred
that Ctenomyidae dig with both their incisors and claws, but by experience, Ctenomys mendoci-
nus is a claw-digger which only occasionally uses its incisors. The frequent exits from the tunnel
and the time that each animal stayed outside the burrow, in addition to certain behaviors and
anatomical traits, suggest the adaptation of tuco-tucos to both underground and aboveground life.

Resume. - On decrit le comportement fouisseur de Ctenomys mendocinus vivant en capti-

vite. On a utilise un terrarium ou chaque animal a ete observe pendant 23 minutes. La sequence
de fouissement est caracterisee par une succession de grattage-rejet au moyen des pattes-grattage
et deplacement en arriere du sol remue. Les incisives ne sont utilisees qu'occasionnellement.
Tous les animaux maintenaient leurs yeux fermes au moment du fouissement.
A partir des donnees de l'anatomie comparee, on peut deduire que les Ctenomyidae fouis-
sent par une action complementaire et combinee des incisives et des pattes anterieures, mais nos
observations nous permettent de classer C. mendocinus comme fouisseur-gratteur n'utilisant
qu'occasionnellement ses incisives. Les frequentes sorties ainsi que les temps que chaque animal
est reste en dehors de la galerie, en plus de certains traits anatomiques et du comportement, sug-
gerent que les tuco-tucos sont adaptes aussi bien ä la vie souterraine qu'a la vie epig6e.

INTRODUCTION

The behavior most obviously associated with fossorial mammals is the act of dig-
ging. There exist some studies on the convergent patterns of digging in fossorial mam-
mals (Nevo 1979, Lessa 1990, Reichman and Smith 1990), but only a few analyze in
detail the burrowing behavior of the different species (Airoldi etal. 1976, Casinos
etal. 1983, Giannoni etal. 1992). The majority of studies involve species occurring in
the northern hemisphere and in Africa.

Mammalia, t. 59, n° 1,1995 :9 - 17.

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10 MAMMALIA

The family Ctenomyidae, of widespread distribution in South America, includes

56 fossorial species (Reig etal. 1990). In spite of this large number of species, burro-
wing behavior has only been described for C.opimus (Pearson 1959) and C.fulvus
(Hickman 1985).
C.mendocinus is widely distributed in Argentina (Cabrera 1961, Honacki etal.,
1982). In Mendoza this species is to be found in different mountain environments (700
to 3000m above sea level), and occurs in isolated groups of low density (Rosi etal.
1992).
The goal of our study was to describe the digging behavior of Ctenomys mendoci-
nus, and to discuss some other associated behaviors.

MATERIAL AND METHODS

Eight adults (five males: 157.29g, 194.11 g, 211.47g, 281.24g, 305.87g, three
females: 159.00g, 191.79g, 197.16g), were captured with live traps in Cacheuta at
1 330 m above sea level (Province of Mendoza, Argentina). Mean annual rainfall
ranges between 200-300 mm, and mean annual temperature is 10-15°C. Sandy soils
prevail (Rosi et al 1992).
All animals were kept in individual plastic containers (90 x 60 χ 30 cm) for 2 months
before the trials. The room in which the animals were housed was kept on a 12-hour
photoperiod and at temperatures ranging from 14°C to 20 °C. The daily food supply
consisted of plenty of alfalfa, carrots, grasses and a large supply of oat and sunflower
seeds.
The experiments were performed in a vertical terrarium of 115 x 115 x 10cm
(Hendricksen and Mac Gaugh 1975) filled with well-packed moist alluvial soil, 3 kg/cm of
compressive strength, measured with a Penetrometer Model FT 327. In order to measure
the burrows, a grid (squares of 5 x 5 cm) was drawn on the glass side of the terrarium. The
terrarium was connected laterally, by means of a transparent acrylic tube 10cm long, to a
plastic container (45 x 30 x 20 cm) from where the animals entered the terrarium and to
where they transported the excavated earth. The front side of this container, made of glass,
was covered with red cellophane paper in order to observe the animals without disturbing
them.
Each animal was observed for 23 min, during which all behaviors were recorded. This
time interval was chosen because in previous observations animals would show a period of
rest after that time. The behavioral patterns were recorded by direct observation and
through video taping.
At the end of each trial, both the angle of entrance and the length of the burrow were
recorded, as well as the amount of soil removed. Eight behavioral patterns were recorded.
Four of them were directly associated with the burrowing activity (D, K, T, E), thus being
selected to test our null hypothesis (see below). The same patterns were found in both
sexes. The sampling method used was a record of sequences with excluded repetitions (Sla-
ter 1978). The behavioral patterns recorded were the following (see Fig. 1).
1) SCRATCHING (S): the animal loosens the earth by scratching with alternate strokes
of its fore claws.
2) KICKING (K): backward throwing of the earth accumulated below the abdomen
with synchronous strokes of hind legs, while resting on the fore feet and tail.

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 BURROWING BEHAVIOR OF CTENOMYS MENDOCINUS 11

8cm

Fig. 1. - Behavioral patterns of Ctenomys mendocinus : (a) scratching ; (b) kicking; (c) transport;
(d) bipedal stance.

3) TRANSPORT (T): pushing of a load of loosened soil with the hind legs, along and
out of a tunnel in a stop-start fashion.
4) EXIT (E): the animal stays with its body completely outside the tunnel, moving
backwards as a last movement of transport, walking forward or wandering around from one
side to the other of the plastic container smelling the floor and walls.
5) BIPEDAL STANCE (I): the animal stands on its hind feet inside the plastic container,
with fore feet close to the chest, watching the surroundings and staying like this for a few
seconds.
6) BITING (B): the animal tears out the earth by means of bites.
7) GROOMING (G): includes the common patterns of washing the face, ears and eyes.
This also includes cleaning the fore claws with incisors, and quick shakings of the body to
remove earth.
8) RESTING (R).
Sequence analysis was carried out by a first order Markov model (Fagen and Young
1978). Our null hypothesis was that the digging sequence was at random, i.e., any pattern
of behavior could be followed by any other one with equal probability. A Chi-square
contingency test was used to verify whether the observed transition probabilities departed
significantly from those predicted by the null hypothesis.
Measurements of body mass, duration of behavioral patterns, soil removed, angle of
entrance and length of tunnel were made.
All variables were first tested for homogeneity of variance (variance ratio F test).
According to results we used t-tests to compare mean body mass, mean duration of digging

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12 MAMMALIA

patterns, mean angle of entrance, mean length of tunnel, and mean soil removed between
sexes.
SCRATCHING —
0.57

0.52 0.34
KICKING
0.15

-TRANSPORT

Fig. 2. -Sequence and probabilities of occurrence of each burrowing pattern of Ctenomys mcndo-
dnus.

RESULTS

All the animals started to dig as soon as they were placed into the terrarium.
After eight recordings totalling 184 minutes of observation (total 2854 patterns, and a
repertoire of 4 patterns: D, K, T, E), the null hypothesis could be rejected OC = 956.91 ;
df = 9; P« 0.01). Table 1 shows both frequency per trial (23 minutes) and mean durations
in seconds of each behavioral pattern. The recorded sequences were transformed into pro-
babilities and are given in figure 2.
The burrowing sequence consisted of successive repetitive series of " scratching-kic-
king-scratching " (S-K-S), followed by transport (T) of the removed earth through the tun-
nel ; nevertheless, in some cases scratching was directly followed by transport (0.34), and
the earlier series was resumed through either scratching or kicking. The rapid alternate
strokes of the fore claws occurred at a speed of 5-6 strokes/sec/leg, and the hind feet stro-
ked with 1-2 stroke/sec. In a low proportion, scratching was replaced by biting (0.02). This
pattern (B) was only observed in four animals (three females, one male). Any of the three
above patterns (D-K-T) was always followed by exit from the tunnel (E). In most cases
(0.67) exits were followed by transport. Only one animal plugged the burrow opening. All
of them closed their eyes while scratching.
Backward departures proved to be much more frequent (90.69 %) than forward depar-
tures, in which case the animals turn round to the right or left in order to face the burrow
entrance. Forward departures were never used for soil transport.

TABLE 1. - Frequency (f) per trial (23 minutes) and mean durations (x) in seconds of each behavioral
pattern.

(0
Scratching 148.12 2.76
Kicking 112.99 0.77
Transport 75.99 5.68
Exit 19.50 14.93
Others 20.12 7.62

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 BURROWING BEHAVIOR OF CTENOMYS MENDOCINUS 13

Once outside the burrow, the animals scattered the accumulated soil, exploring the
container, smelling the floor and walls, scanning the surroundings while sitting on their
haunches in a squirrel-like fashion (I) (Fig. 1).
There were no differences between males and females in the mean duration of digging
patterns (t-test). Transport (T) and scratching (S) took most of the time (0.61) of the total
observation period (184 min) (Fig. 3).

0.35 τ

0.3 -

0.25 -

0.2 ·

0.15 ·

0.1 ··

0.05 - ·

Scratching Transport Exit Kicking Other«

Fig. 3. - Proportion of time spent by Ctenomys mendodnits in performing each behavioral pat-
tern during the observation period.

No differences between sexes were verified for body mass, angle of entrance, length
of tunnel and soil removed (t-test). There was no correlation between body mass-tunnel
length, body mass-soil removed, or body mass-angle of entrance.
The mean volume of extracted soil for the experiment was 5553.57cm3
(4959.74 grams), the standard error of the mean (SEM) and the coefficient of variation (V)
were ± 1546 and 78% respectively i.e., 23.39 times the average body weight (212 g)
(SEM = ± 19.06, V = 25%).
The mean distance covered was 85.93cm (SEM = ±9.49, V = 31%) (0.062 cm/sec).
The angles of entrance to the burrow varied between 0° and 45° (x = 15°66', SEM = ± 4.81,
V =86%).

DISCUSSION

The mode of digging by scratching is shared by large mammals (e.g. armadillos

and pangolins) and small mammals (e.g. Bathyergus sp., Myospalax sp., pocket

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14 MAMMALIA

gophers, coruros, and tuco-tucos). All of them apply a rapid succession of scratching
creating a momentum that contributes to soil breaking, while gripping the floor with
toes and claws of their hind feet, using the tail as a prop (Hildebrand 1985). In our
experiments the speed of the fore claws (5-6 strokes/sec/leg) as well as the position of
the hind feet and the tail while digging (Fig. 1) coincide with the above statement.
Thus, although it has been inferred from the data from comparative anatomy (Dubost
1968) that Ctenomyidae dig with teeth and fore claws, our data allowed us to classify
Ctenomys mendocinus from Cacheuta as a claw-digger that uses its incisors only occa-
sionally. Nevertheless, owing to the widespread distribution of this species and to the
wide range of soils it inhabits, other populations of C. mendocinus occurring in harder
soils (e.g. clay soils) are likely to use their incisors much more frequently.
As reported by Hickman (1985) for C.fulvus, the movement of the tail from one
side to the other during the backward removal of earth also facilitates the action of the
hind feet in C. mendocinus.
The average amount of soil removed by tuco-tucos (215 g/min) was quite below
the one reported by Ognev (1947) for Spalax giganteus (750 g/min) in the field. The
removed soil-body weight ratio (23.39) was similar to that shown by Spalax leucodon
(15-20) (Gambarian 1953) and higher (1.01) than that of Pity my s duodecimcostatus in
one minute's time (0.4) (Giannoni et al. 1991). Mean digging speed (0.062 cm/sec) was
lower than that of Scalopus (0.11 cm/sec) (Arlton 1936).
Tuco-tucos transported the removed soil out of the burrow like bathyergids (back-
wards) although they did not thrust their nose and upper incisors into the top of the
burrow for purchase like Heliophobius, nor did they work in a " digging chain " like the
colonial Heterocephalus (Jarvis and Sale 1971). The sideways turn the animals take for
a forward departure is similar to that of Tachyoryctes (Jarvis and Sale 1971) but differs
from Reichman's and Smith's description for entirely subterranean species (1990).
All other fossorial mammals use the forward body orientation for earth transport.
Most of them show either a pronounced ocular reduction or eyes completely covered
by skin. On the other hand, although reduced eyes and tail are typical of fossorial
mammals (Agrawal 1967), it is also likely that blindness does not represent an adaptive
advantage for the animal (Pearson 1959), therefore the presence of functional eyes
could increase survival chances. Ctenomyid's eyes are moderately developed and set
well towards the top of the head; the main lines of vision are upwards and sideways,
suggesting a need for alertness to aerial predators (Weir 1974). Lessa (1990) has sug-
gested that the variation in eye size could be related to the frequency of surface and
underground foraging, and that scratch-digging and humeral rotation are less conflic-
tive with vision than other digging modes, and do not require an extreme eye reduc-
tion. In the digging process, there exist two critical instants for eye safety : the first one
when the earth is broken, and the second one when the earth is transposed. Tuco-tucos
solve the first problem by closing the eyelids while digging. Hickman (1985) holds that
the way they push the removed earth backwards could resolve the second.
Several authors have reported the presence on the surface of specimens belonging
to other species of Ctenomys in the daytime (Pearson 1959, Altuna 1983, Pearson and
Christie 1985, Roig etal. 1988). Pearson (1959) pointed out differences in the time of
day selected by C. opimus and C. peruanus for coming up to the surface. Although in
the field we did not observe any C. mendocinus on the surface during the day, field
works (Torres Mura etal. 1989, Madoery 1993) and laboratory trials (Camin and
Madoery 1994) show that C. mendocinus feeds on plant stems. The frequent exits of
the animals during trials, and the time they stayed outside the burrow (table 1) together
with our field observations of cut-off stems of bushes, grasses and cacti around the bur-

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 BURROWING BEHAVIOR OF CTENOMYS MENDOCINUS 15

row entrances of C. mendocinus suggested that in certain occasions (i.e. foraging) sight
may be of great importance for the survival of this species.
The bipedal stance of Ctenomys mendocinus (Fig. 1) is also shown by C. opimus
(Pearson 1959) and C.fulvus (Hickman 1985) as well as by other rodents that perform
both burrowing and surface activities : the Black-tailed prairie dog Cynomys ludovicia-
nus (King 1955), the Uinta ground squirrel, Citellus armatus (Balph and Stoken 1963),
the Desert cavy, Microcavia australis (Rood 1970) and the Degu, Octodon degus
(Yanez and Jacksic 1978).
M. australis keeps the area around the bushes clear of vegetation, which probably
helps to visually detect their predators (Rood 1970). The habit of Ctenomys of lowering
the height of the mounds close to tunnel entrances could possibly serve the same pur-
pose.
Tuco-tucos show a great number of adaptations reported as typical of subterranean
life (Dubost 1968, Nevo 1979). Nevertheless, they also show features related to life on
the surface (size and location of the eyes, mode of foraging and bipedal stance). This
would suggest that tuco-tucos are adapted to underground life as well as to above-
ground life, probably because of their dependance on the world outside their burrow
for food.

ACKNOWLEDGEMENTS

We wish to thank Luis Marone, Stella Giannoni, Carlos Borghi, Marisa Rosi and Manuel
Homo for their critical review of this paper and their valuable comments and suggestions. We
also thank Nelly Horak for translating the manuscript and Margarita Gonzalez Loyarte for wri-
ting the French version of the Abstract.
This work is in partial fulfilment of the requirements for a doctoral degree for Sergio Camin.

BIBLIOGRAPHY

AGRAWAL, V.C., 1967. - Skull adaptation in fossorial rodents. Mammalia, 21 : 300-312.

AIROLDI, J.P., R. ALTROCCHI et A. MEYLAN, 1976. - Le comportement fouisseur du Campagnol
terrestre. Arvicola terrestris scherman Shaw (Mammalia, Rodentia). Rev. Suisse ZooL,
83 : 282-286.
ALTUNA, C., 1983. - Sobre la estructura de las construcciones de Ctenomys pearsoni Lessa y
Langguth (Rodentia, Octodontidae). Revista de Communicaciones de las Jornadas de
Ciencias Naturales de Montevideo (Uruguay), 3 : 70-72.
ARLTON, A.V., 1936. - An ecological study of the mole. J. Mammal., 17 : 349-371.
BALPH, D.F. and A.W. STOKEN, 1963. - On the ethology of a population of Uinta ground squir-
rels. Amer. Midi. Natur., 69 : 106-126.
CABRERA, A., 1961. - Catälogo de los mamiferos de America del Sur. Rev. Mus. Cs. Nat. "Ber-
nardino Rivadavia ", Cs ZooL, 4 (2): 309-732.
CAMI'N, S.R. and L.A. MADOERY, 1994. - Feeding behavior of the tuco-tuco (Ctenomys mendoci-
nus) its modifications according to food availability and the changes in the harvest pat-
tern and consumption. Rev. Chil. Hist. Nat. (in press).
CASINOS, A., J.P. GASC., S. RENOUS et J. Bou, 1983. - Les modalites de fouissage de Pitymys
duodecimcostatus (Mammalia : Arvicolidae). Mammalia, 47 : 27-36.

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Download Date | 5/25/15 11:47 AM
16 MAMMALIA

DUBOST, G., 1968. - Les mammiferes souterrains. Rev. EcoL Biol. Sol., 5 : 99-133.
FAGEN, R.M. and D.Y. YOUNG, 1978. - Temporal patterns of behaviors : durations, intervals,
latencies and sequences. Pp. 79-114 in: Quantitative Ethology. Ed. P.W. Colgan John
Wiley and Sons, New York.
GAMBARIAN, P.P., 1953.- Adaptive specializations of the forelimbs of blind mole rats (Spalax
leucodon nehringi Saturnin). Zool. Inst. Akad. Nauk. Armianskoi SSSR, 8 : 67-125 (In
Russian).
GIANNONI, S.M., C.E. BORGHI and J.P. MARTINEZ RICA, 1991. - Capacidad potencial de movi-
miento del suelo por parte de Pitymys duodecimcostatus en cautividad. Lucas Mallada, 3 :
73-81.
GIANNONI, S.M., C.E. BORGHI y J.P. MARTINEZ RICA, 1992. - New data on the burrowing beha-
vior of Microtus (Pitymys) duodecimcostatus. Z. Säugetierk., 57 : 23-28.
HENDRICKSEN, R.L. and M.H. MAC CAUGH, 1975.- A display unit for a live pocket-gopher.
Museum Sc. Program., Texas Tech. University, 1 : 1-10.
HICKMAN, G.G., 1985.- Surface mound formation by the Tuco tuco Ctenomys fulvus (Rodentia,
Ctenomyidae), with comments on earth pushing in other fossorial mammals. J. Zool.
London, 205 A : 385-390.
HILDEBRAND, M., 1985. - Digging of Quadrupeds. Pp. 89-110 in : Functional Vertebrate Mor-
phology. Eds. Hildebrand, Bramble D., Liem K., Wahe D., Harvard University Press,
Cambridge, Massachussetts.
HONACKI, HJ., K.E. KiNMAN and J.W. KOEPPL, 1982. - Mammal species of the world. The
Assoc. Syst. Coll., Lawrence.
JARVIS, J.U. and J.B. SALE, 1971. - Burrowing and burrow patterns of East African mole-rats
achyorydes, Heliophobius and Heterocephalus. J. Zool. London, 163 : 451-479.
KING, J.A., 1955. - Social behavior, social organization and population dynamics in a black-tai-
led prairie dog town in the Black Hills of South Dakota. Contrib. Lab. Vert, biol., Univ.
Mich., 67 : 1-23.
LESSA, E.P., 1990. - Morphological evolution of subterranean mammals : integrating structural,
functional and ecological perspectives. Pp. 211-230 in : Evolution of subterranean mam-
mals at the organismal and molecular levels. Eds. Eviatar Nevo and Osvaldo A. Reig,
Wiley-Liss, New York.
MADOERY, L., 1993. - Composicion botanica de la dieta del tuco-tuco (Ctenomys mendocinus) en
el piedemonte cordillerano. Ecologia Austral, 3 : 49-55.
NEVO, E., 1979. — Adaptative convergence and divergence of subterranean mammals. Ann. Rev.
Ecol. Syst., 10 : 269-308.
OGNEV, S.I., 1947. - Mammals of the U.S.S.R. and adjacent countries. Publications for the
National Science Foundation by the Israel Project for Scientific Translation.
PEARSON, O.P., 1959. - Biology of the subterranean rodents, Ctenomys in Peru. Memorias del
Museo de Historia Natural "Javier P rado ", 9 : 1-55.
PEARSON, O.P. y M.I.CHRISTIE, 1985.- Los tuco-tucos (Genero Ctenomys) de los Parques
Nacionales Lanin y Nahuel Huapi, Argentina. Historia Natural, 5 : 337-343.
REICHMAN, O.J. and S.C. SMITH, 1990. - Burrows and burrowing behavior by mammals. Volume 2,
chapter 5, pp. 197-244, in : Current Mammalogy. Ed. Hugh H. Genoways, University of
Nebraska State Museum, Lincoln.
REIG, O.A., C. BUSCH, M. ORTELLS and J. CONTRERAS, 1990. - An overview of evolution, syste-
matics, population biology, cytogenetics, molecular biology and speciation in Ctenomys.
Pp. 71-96 in : Evolution of subterranean mammals at the organismal and molecular
levels. Eds. Eviatar Nevo and Osvaldo Reig, Wiley-Liss, New York.
ROIG, V.G., M. GONZALEZ LOYARTE and M.I. Rosi, 1988. - Ecological analysis of a mound for-
mation of the mima type in Rio Quinto (Province of Cordoba, Argentina). Studies on
Neotropical Fauna and Environment, 23 : 103-115.

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 BURROWING BEHAVIOR OF CTENOMYS MENDOCINUS 17

RIOOD, J.P., 1970. - Ecology and Social behavior of the desert cavy (Microcavia australis). Am.
Midi. Nat., 83 : 415-454.
Rtosi, M.I., J.A. SCOLARO y F. VIDELA, 1992. - Distribution y relaciones sistemäticas entre pobla-
ciones del genero Ctenomys (Rodentia, Ctenomyidae) de la provincia de Mendoza
(Argentina). Misc. ZooL, 16 : 207-222.
SILATER, J.B., 1978. - Data collection. Pp. 7-25 in : Quantitative Ethology. Ed. P.W. Colgan, John
Wiley and Sons. New York.
T<ORRES-MURA, J.C., M.L. LEMUS and L.C. CONTRERAS, 1989. - Herbivorous specialization of the
South American desert rodent Tympanoctomys barrerae. J. Mammal., 70 : 646-648.
WEIR, B.J., 1974. - The tuco-tuco and plains viscacha. Symp. zool. Soc. London, 34 : 113-130.
Y'ANEZ, and JACKSIC, 1978. - Historia Natural de Octodon degus Molina (Rodentia, Octodonti-
dae). Publication ocasional, Museo Nacional de Historia Natural, Stgo. de Chile, 27.

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