sign in sign up
<<
Home , Caviomorpha, Gopher, Spalax

Mastozoología Neotropical; 3(2):161-170 ISSN 0327-9383 SAREM, 1996 THE BURROWING BEHAVIOR OF Ctenomys eremophilus (RODENTIA, CTENOMYIDAE) IN RELATION WITH SUB STRATE HARDNES S

Stella M. Giannoni, Carlos E. Borghi and Virgilio G. Roig

Unidad de Zoología y Ecología (IADIZA-CRICYT), Casilla de Correo 507, 5500 Mendoza, Argentina. Tel/Fax: (54) 061- 287995; Fax: (54)061-287370, e-mail: [email protected]

ABSTRACT: The burrowing behavior of Ctenomys eremophilus in substrates of different hardness was studied in a glass terrarium. We found that both the type and frequency of use of burrowing tools are closely associated with the degree of hardness of the substrate. The study of the burrowing sequence showed that Ctenomys eremophilus uses both forelegs and incisors when burrowing in a hard substrate, but only forelegs in a soft substrate. Hence, this is a "mixed" digger according to Dubost's classification, and a "scratch- and chisel- tooth digger" according to Hildebrand's.

RESUMEN: Comportamiento excavador de Ctenomys eremophilus (Rodentia, Ctenomyidae) en relación a la dureza del substrato. Se estudió el comportamiento ex- cavador en un terrario vertical y en diferentes durezas de substrato. Encontramos que, tanto el tipo de herramienta como la frecuencia de uso, estaba estrechamente relacionada con el grado de dureza del substrato ofrecido. El estudio de la secuencia de excavación mostró que Ctenomys eremophilus en un substrato duro usa los miembros anteriores y los incisivos, pero solamente los miembros anteriores en uno blando. Así, esta especie es un excavador "mixto" de acuerdo a la clasificación de Dubost, y un excavador "rasguñador" y excavador "con dientes" de acuerdo a la clasificación de Hildebrand.

Key words: Burrowing behavior, substrate hardness, Ctenomys eremophilus, subterranean

Palabras claves: Comportamiento excavador, dureza del substrato, Ctenomys eremPphilus, mamíferos subterráneos.

INTRODUCTION claws in the forelegs, and the skull has suf- Burrowing mammals show a continuous gra- fered no modifications. The other group is dient of adaptation to underground life, as well represented by Marmota, Rattus manipulus, as appropriate adaptations for digging (Dubost, Nesokia and Microtus (Terricola) sikimensis 1968; Nevo, 1979). among others. They dig with both incisors and Several classifications of burrowing forelegs, and the skull is more specialized than have been proposed with regard to their mor- the forelegs. Agrawal (1967) holds that scratch- phological and behavioral adaptations. Agrawal digging species would be restricted to sandy (1967), based on the morphological features, and soft soils; whereas tooth-digging species classified burrowing in two groups. would be able to colonize either hard or soft soils. One group is represented by the genera Tatera, Meriones and Gerbillus, that inhabit arid areas According to Dubost (1968) three types of mainly, and dig their in sandy soils morphological adaptations can be distin- with their forelegs. They have developed strong guished: 1.- animals that dig only or mainly

Recibido 1° noviembre 1995. Aceptado 29 julio 1996. 162 S.M. Giannoni, C.E. Borghi and V.G. Roig with forelegs (Marsupialia as Notoryctes, In- backwards with their hindlegs, e.g. Heteroceph- sectivora as Chrysochloridae and Talpidae; and alus glaber and Heliophobius argentinoci- Rodentia as some Cricetidae and Bathyer- nereus (Jarvis and Sale, 1971), Ctenomys ful- gidae); 2.- those that mainly use incisors (some vus (Hickman, 1985), Microtus (Terricola) rodents of the Old World, e.g. Arvicolidae, pyrenaicus and M. (T.) lusitanicus (Giannoni ) and 3.- those that use both, in a et al., 1993); and 2.- "forward-pushing": they complementary or combined action (some ro- transport the earth outwards by pushing it with dents of the New World, like Geomyidae and the head and the forelegs, e.g. Microtus (Pit- Ctenomyidae). On the other hand, Gasc et al. ymys) pinetorum (Hamilton, 1938), (1985) include not only the burrowing tools ehrenbergi (Nevo, 1961), Arvicola terrestris but also the different burrowing modes in their (Airoldi et al., 1976; Laville, 1989), and M. classification. They report two general groups: (T.) duodecimcostatus (Giannoni et al., 1992). 1.- animals that use forelegs: Pitymys system Considering these methods, Nevo (1979) sug- (current subgenus Terricola) and Eremitalpa gests that the way of transporting earth would system, and 2.- those that use incisors: Arvico- reflect phylogenetic relationships between the la terrestris system and Spalax system. How- groups of subterranean mammals. In contrast, ever, Giannoni et al. (1992) found that the Hickman (1985) considers that the different Pitymys system proposed by Gasc et al. (1985) ways represent several adaptive strategies in- does not exist, and suggest that it was proba- dependent of phylogeny. Giannoni et al. (1993) bly based on an inappropriate methodology. found that the subgenus Terricola supported Giannoni et al. (1992, 1993) include the stud- Hickman's hypothesis. ied species, from the subgenus Terricola, in Ctenomyids are endemic fossorial rodents the Arvicola terrestris system. widely distributed in (Pearson, Finally, Hildebrand (1985) found different 1959; Reig et al., 1990). These species make burrowing modes in small mammals: 1.- their presence obvious by ejecting mounds of "Scratch-diggers", that include fossorial mar- fresh earth. This is a "mixed" digger supials (Notoryctes), burrowing insectivores according to Dubost's classification, and a (except moles), armadillos, pangolin, ground "scratch-and chisel-tooth digger" according , pocket , coruro, tuco-tucos, Hildebrand' s classification, i.e. it would use the Bathyergus and cricetid Myospal- not only forelegs but incisors as well. Several ax; 2.- "Chisel-tooth diggers", i.e. those that authors have studied or inferred the burrowing use primarily the teeth (, Crato- manner of ctenomyids. Thus, Pearson (1959) , Cryptomys, Spalax, Eremitalpa, and found that both Ctenomys peruanus and C. Cannomys). 3.- "Head-lift diggers", that include opimus use mainly their forelegs in the field. those species that dig with the head to a lim- Altuna et al. (1993) found that C. pearsoni in ited degree, e.g. marsupial , golden moles, a sandy substrate uses principally the forelegs; mole- Spalax, and cricetid Myospalax; 4. and Camín et al. (1995) found similar results "Humeral-rotation diggers", moles and shrew for C. mendocinus. Moreover, Ubilla and moles that dig by rotating the humeros around Altuna (1990) inferred, through the morpho- its long axis. Some of them have more than logical adaptations of forelegs, the burrowing one burrowing mode, using both incisors and mode for C. rionegrensis, C. pearsoni and C. claws (pocket gophers, tuco-tucos, Bathyergus), torquatus. or both incisors and head (the mole-rat Spal- On these grounds, the aim of this work is to ax), or incisors, claws, and head (the cricetid describe the burrowing behavior of Ctenomys Myospalax). eremophilus in substrates of different hardness. Concerning the way in which the animal We find that studying this behavior is interest- transports soil outside the , Giannoni et ing because, being subterranean animals, dig- al. (1993) propose the existence of two meth- ging is one of the most relevant habits of these ods: 1.- "backward-pushing": the animals trans- species; and the different digging modes de- port the earth to the surface by pushing it termine the soil type to which they are re- stricted according to Agrawal (1967). BURROWING BEHAVIOR OF Ctenomys 163

MATERIAL AND METHODS A first-order Markov model was used to Six individuals of Ctenomys eremophilus (2 analyze the burrowing sequence (Fagen and females and 4 males) were captured with plas- Young, 1978). Statistical methods used in- tic live traps placed in tunnel entrances, in the cluded the x2 test to find out whether behav- Ñacuñán Biosphere Reserve (Mendoza prov- ioral acts showed a random occurrence ince, Argentina). C. eremophilus (Contreras and (Markov model, Fagen and Young, 1978), and Roig, 1975) is a nomen nudum, nevertheless to compare between sexes the frequency of we use this name because it was assigned to specific digging acts. The Mann-Whitney U- this population (V. Roig. personal observation). test and Kolmogorov-Smirnov test were used The animals were kept in the laboratory (23 ± to compare the time spent in each behavioral 2° C and natural light), in plastic boxes 35 cm act between sexes, and the frequency of spe- long, 20 cm high and 25 cm wide. Within the cific digging acts in packed and unpacked sub- boxes there was enough loose soil, and cotton strates (Zar, 1984; Siegel, 1986). for nesting. Food in surplus (carrots, sweet potatoes) was supplied. RESULTS Fifteen observations were made for females and twenty-four for males. Each observation Description of behavioral acts lasted 5 minutes, that is a total 195-minute We distinguished 14 behavioral acts, eight of observation. A focal sampling was made and which are directly linked to the burrowing each sample consisted in continuously record- activity, namely: ing the sequence of acts for 5 minutes, consid- - Claw-grooming (Cg): the animal is sitting, ering their repetition and duration (Slater, leaning on its hindlegs, and cleaning its fore- 1978). All observations were audio-vocally leg-claws with the incisors. It is a short-lasting recorded and videotaped. movement. Observations were made in a vertical glass - Out (0u): the animal stops digging, turns terrarium of 5 x 80 x 50 cm containing well- round by a lateral tumble, and then goes to the packed moist earth (2.73 Kg/cm' of mean outside box. compressive strength measured with a pocket - Flattening (FI): within the box it gives a penetrometer, SD= 0.76, n= 28). The terrarium series of strokes to the earth it transported from was connected by a 10 cm long pipe to a trans- the terrarium, using both hindlegs simulta- parent plastic box of 10 x 31 x 16 cm with a neously. The animal' s body is supported by perforated lid (Fig. 1). Later, observations were the forelegs and the tail is straightened up- made in soft unpacked earth (0.18 Kg/cm' of wards. The body gradually moves from one mean compressive strength, SD= 0.005, n= 22, side to the other in a fan-like motion. i.e. about 16 times less than normal soil for- merly used) on two adult males and three adult - Advancing (Ad): the animal goes back to females. the terrarium heading forwards. - Advance pushing (Ap): the animal goes back to the terrarium while pushing the torn I cm A: Terrarium S: Plastic box earth backwards. It stops from time to time, leaning on its forelegs, to push the earth back- wards with two or three simultaneous strokes of its hindlegs. The tan is straightened upwards during the strokes, and flaccid while advanc- ing. - Digging (D): the animal tears the earth mainly with its forelegs (F) and pushes it be- low the abdomen, with forelegs working alter- Fig. 1. Vertical terrarium used for studying the burrow- nately. Additionally, it bites (Bi) the earth with ing behavior of Ctenomys eremophilus. its incisors to tear it out. When using the fore- 164 S.M. Giannoni, C.E. Borghi and V.G. Roig legs, the body is supported by both hindlegs wards and throwing earth with the hindlegs. and one foreleg. When biting, all four limbs This would be equivalent to going out kicking are resting on the substrate. From time to time, (Gk). when the amount of earth below the body is 2. Turning round quickly and scanning or high, the animal throws it backwards with the sniffing. During our 20-minute observation the hindlegs, in two or three kicks (Ki), and dur- animal carne up to the surface five times. ing this phase the body is supported by the 3. Turning round again and, in a fan-like forelegs. fashion, flattening the earth removed with the - Kicking in the box (Kb): the animal is in hindlegs (through a number of strokes). This the box near the tunnel entrance, and kicks would be equivalent to flattening (F1). The away (with 2 or 3 strokes) the earth previously animal was observed to perform this activity removed from the terrarium. five times (30 seconds each) during the 20- - Going out kicking (Gk): the animal stops minute observation. digging and goes outside the terrarium kicking 4. Entering the burrow hastily. The equiva- the earth accumulated along the tunnel. Lean- lent would be advancing (Ad) or advance push- ing on its forelegs it throws the earth back- ing (Ap). wards. The tail would play an active role, since 5. The animal goes out in a backward mo- it moves from one side to the other touching tion while throwing earth with its hindlegs, the tunnel walls. thus beginning a new sequence. The remaining behavioral acts exhibited by Ctenomys, indirectly linked to burrowing, are: Description of the burrowing sequence Grooming (Gr): the animal cleans ears and head The burrowing sequence was studied in a hard mainly with the forelegs. Shaking (Sh): the substrate, basing on the behavioral acts closely body makes very rapid movements from side related to burrowing (i.e. Cg, Ou, Fl, Ad, Ap, to side, probably to clean the earth off the body. D, Kb, and Gk), since the other behavioral Feeding (Fe), Resting (R), Sniffing (Sn) and acts (i.e. Gr, Sh, F, R, Sn, and Sc) were not Scanning (Sc) coincide with the general pat- considered on account of their very low fre- terns found for these behaviors. The same quency. The general sequence was established patterns were found in both sexes. independently for males and females because we found significant differences in the fre- Description of mound formation in the field quency of behavioral acts between both sexes On one occasion, while on the Ñacuñán Re- on the Markov model (x2 = 87.4; g.1.= 16; p= serve, we observed an individual of C. eremo- 0.001). A specific sequence for each sex was philus building a mound. It was 10 a.m., and established using the specific digging acts (Bi, the animal dug for 20 minutes. This observa- F, and Ki), and all behavioral acts that precede tion is a peculiar event, since only Pearson and follow them (x2 = 94.5; g.1.= 11; p= 0.001). (1959) reported something similar for C. opi- Significant differences between sexes were also mus. Mounds of C. eremophilus are earth ac- found in this sequence. The frequencies of the cumulations generated by digging, in the shape behavioral acts were later turned into prob- of a horseshoe, with the hole opposite the abilities (Fig. 2). convex sector of the formation (mean distance Dealing specifically with the sequence of the between the hole and the mound outer side digging act, in both sexes, foreleg scratching right opposite the hole: 70 cm, SD= 175.5, n= (F) is followed with high probability by throw- 9; mean distance between the extremes of the ing earth backwards (Ki; Males: 0.81, and horseshoe-like mound: 83 cm, SD= 78.5, n= Females: 0.71). Besides, scratching may be 9; and mean height of the mound: 12 cm, SD= followed by biting (Bi), with like probability 6.5, n= 9). Concerning mound formation, five in both sexes (Males: 0.16, and Females: 0.18). phases can be distinguished: Scratching again after kicking (Ki; Males: 0.51, 1. Going out of the burrow moving back- and Females: 0.54) is more likely than going out kicking (Gk) in both sexes. There is a close BURROWING BEHAVIOR OF Ctenomys 165

Digging Mi.35 Forelegs M).93 Claw-grooming MI.81 Mi.91 MW.81 ~.95 MI.75 FC1.54 Mr.).51

Bites F4.16 Hindlegs .21 ivH3.29

Fd/59 MM).73 Going out kicking F.52 M).54 Kicking in the box

:1.60 ~58 Flattening F:).1.4/ béM).29 NvM.46 Advance pushing Advancing

Fig. 2. Burrowing sequence and probabilities of each burrowing act "of Ctenomys eremophilus in hard substrates. Spe- cific sequence, i.e. the set of acts specifically belonging to digging is shown within the box. General sequence with all behavioral acts related to digging, is shown too. See text for further explanation. F= females, M= males. relationship between scratching (F) and claw- specific digging acts comparing packed and grooming (Cg), since the animal cleans its unpacked soils (Mann-Whitney U-test, Bite: claws very frequently while digging (Fig. 2). Z= -9.6, p< 0.001; Forelegs: Z= -5.3, p< 0.001; On average, in both sexes each burrowing Hindlegs: Z=. -0.49, p< 0.619, Fig. 3). sequence consisted of several repetitions, a low- Concerning the general sequence of burrow- order unit was made of 17 scratches (F) and 5 ing, we find that the digging act (D) in both kicks (Ki), and every two of these units they sexes is followed with high probability by bit (Bi) the earth three times. We found no going out kicking (Gk; Males: 0.73, and Fe- significant differences between sexes in the males: 0.59). Next, both males and females frequency of repetition of specific digging acts: usually kick in the box (Kb) the earth removed, Bi, F, and Ki (c2 = 5.46; g.1.= 2; p= 0.065, and then they flatten it (F1). Afterwards, the Table 1). animals may simply advance (Ad) or advance In a soft substrate, behavioral acts were the pushing (Ap), and in both sexes the former act same, but there were significant differences is more likely than the latter (Ad; Males: 0.46, between the mean frequency of repetition of and Females: 0.59 versus Ap; Males: 0.29 and 166 S.M. Giannoni, C.E. Borghi and V.G. Roig

35

30 —

25 — uency 20 — freq

n 15 —

Mea 10 —

Bites Forelegs Hindlegs Behavioral acts

Fig. 3. Mean number of repetitions in each digging sequence of the acts Iinked to burrowing behavior of Ctenomys eremophilus. Observations on packed and unpacked substrates.

Females: 0.14). Finally, the animals generally grooming (Cg) in females, showed long dura- start digging (D) again and a new sequence tion, though little frequency. Among the acts begins (Fig. 1). directly associated with burrowing, digging (D) and going out kicking (Gk) showed high mean Duration of the burrowing sequence duration in both sexes. In contrast, the shortest Table 2 shows the mean duration of every act in both sexes was advancing (A). We only behavioral act in the hard substrate and the found significant differences between sexes in corresponding frequency for both sexes of C. the mean duration of digging (D), which was eremophilus. Some acts not specifically related significantly higher in females than it was in to the burrowing activity, such as sniffing (Sn) males. Table 2 also shows the percentages of in both sexes, and scanning (Sc) and claw the total time spent in every act of burrowing for both sexes. We found no significant differ- ences between sexes in the time used for any Table 1. Mean frequency, standard deviation (SD), and burrowing act (difference between proportions frequency of occurrence (n) of the specific acts t-test). Both sexes spent most of the time dig- of the burrowing activity in both sexes of ging (D) (males: 47.5%, and females: 53.1%), Ctenomys eremophilus in hard substrates. and going out kicking (Gk) (males: 16.5% and females: 13.1%). Specific acts of burrowing behavior Bite (B) Foielegs (F) Hindlegs (H) Position and function of the tail while Mean SD Mean SD Mean SD burrowing Female 2.7 1.6 20.0 11.8 5.0 3.2 When the animal kicks in the box (Kb) the n= 196 n= 267 n= 260 earth it removed from the terrarium, the tail Male 2.5 1.7 17.1 11.3 5.0 2.7 lies flabby behind it, just as when the animal n= 280 n= 489 n= 479 advances from the outside into the terrarium BURROWING BEHAVIOR OF Ctenomys 167

(A). When it flattens the earth (F1) the tail is substrate of little humidity, Ctenomys pearso- raised in an angle of about 45° with respect to ni only uses its forelegs; but in a well-packed its body. When the animal is loosening earth substrate, this species uses its incisors as well. with its forelegs (F) the tail seems to provide C. mendocinus uses mainly the forelegs for support, for it rests on the walls of the ter- digging, and only occasionally the incisors rarium on the same side from which the ani- (Camín et al., 1995). In contrast, C. eremophi- mal is removing earth. Thus, if it is removing lus in a well-packed substrate like the soil of earth from the right side of the terrarium, its the area where the specimens were captured tail is also leaning upon the right side. In con- (mean compressive strength from study area is trast, when it kicks (Ki) the earth backwards, 2.81 Kg/ cm2, SD= 2.05, n= 32), uses mainly the distal end of the tail rests on the substrate. the forelegs but often the incisors as well (Ta- While going out kicking (Gk), the animal Me 1 and Fig. 2). Instead, this species uses mover its tail alternately from one side to the only the forelegs for loosening soft unpacked other touching the walls of the terrarium. Fi- moist earth. (Fig. 3) nally, while scanning (Sc), grooming (Gr) or The use of incisors as a secondary burrow- claw-grooming (Cg) the animal's tail is be- ing tool by ctenomyids has been suggested by hind it acting as a tripod, because the body is several authors, based on the microstructure of supported by hindlegs and tail. the enamel of incisors, the morphology of the digging apparatus, and the burrowing behav- DISCUSSION ior (De Santis, 1986; Reig et al., 1990; Altuna The various species of ctenomyids use differ- et al., 1993; Lessa, 1993; Justo et al., 1995). ent combination of digging tools (Lessa, 1993). Also, Justo et al. (1995) have suggested that Further, Lessa (1993) shows the existence of incisors could be used in moving obstacles in diverse combinations of morphological traits the tunnels, as Altuna et al. (1993) mentioned reflecting functional modifications for digging. for C. pearsoni, and we observed in C. Altuna et al. (1993) found that, in a loose sandy eremophilus at the laboratory.

Table 2. Mean duration, % of the total time spent in every behavioral act, standard deviation in minutes (SD), and occurrence frequency (n) for both sexes of Ctenomys eremophilus in hard substrates. Mann-Whitney U-test and Kolmogorov- Smirnov test(*) were used to compare the time used in each behavioral act by each sex, **p < 0.001.

Male Female Mean Mean duration % SD n duration % SD (min) (min) Claw-grooming 0.04 2.8 (101) 101 0.04 5.0 (99) 99 ns Out 0.08 1.1 (18) 18 0.17 1.8 (8) 8 ns* Flattening 0.03 4.4 (168) 168 0.03 2.8 (69) 69 ns Advancing 0.02 4.1 (228) 228 0.02 3.5 (115) 115 ns Advance pushing 0.04 5.1 (178) 178 0.04 3.8 (72) 72 ns Digging 0.13 47.5 (495) 495 0.15 53.1 (275) 275 ** Kicking in the box 0.04 7.0 (260) 260 0.04 5.4 (107) 107 ns Going out kicking 0.05 16.5 (404) 404 0.06 13.1 (182) 182 ns Grooming 0.05 0.4 (10) 10 0.17 1.1 (5) 5 ns* Feeding 0.08 0.3 (4) 4 0.08 1.0 (9) 9 ns* Resting 0.04 0.8 (28) 28 0.03 0.7 (17) 17 ns* Sniffing 0.12 7.1 (79) 79 0.14 4.2 (23) 23 ns* Scanning 0.07 2.6 (49) 49 0.11 4.0 (28) 28 ns* Shaking 0.04 0.3 (11) 11 0.02 0.5 (16) 16 ns* 168 S.M. Giannoni, C.E. Borghi and V.G. Roig

Several authors have suggested that the tools eremophilus, but we did not find "accumula- subterranean mammals use for digging are tion" (joint movements of the forelegs in equal closely related to the hardness of the soil they direction, with which the animal pushes the inhabit (Agrawal, 1967; Lessa and Thaeler, removed material under its abdomen) in C. 1989; Lessa 1990; Giannoni et al., 1992). eremophilus, since this species accumulates the Additionally, it has been found that morpho- earth below the abdomen with alternate move- logical convergence present in the digging ments of its forelegs, and not simultaneously apparatus (Mathias, 1990), and in the digging as C. pearsoni. behavior (Giannoni et al., 1993) are more As for the different ways of transporting the closely associated with environment than with earth outside, most species of fossorial mam- phylogeny. On account of the close relation- mals use the head and the forelegs, the only ship between soil hardness, morphology of the exception being the families Ctenomyidae; digging apparatus, structure of the enamel of Bathyergidae (Hickman, 1985), and some incisors (Justo et al., 1995), and burrowing Arvicolidae (Microtus (Terricola) pyrenaicus behavior, it is necessary to take into consider- and M. (T.) lusitanicus, Giannoni et al., 1992, ation the nature and hardness of the substrate 1993). The way in which C. eremophilus ex- at the time of studying such behavior, and of pels the earth outside the terrarium coincides extrapolating results to field conditions. For with that found in other ctenomyid species, example, Casinos et al. (1989) and Giannoni such as C. peruanus and C. opimus (Pearson, et al. (1992) found unlike results in the bur- 1959), C. fulvus (Hickman, 1985), and C. rowing behavior of Microtus (Terricola) mendocinus (Camín et al., 1995). According duodecimcostatus, probably because the former to Hickman (1985) Ctenomys is unique, with authors used a very soft substrate in their study. greatly enlarged snowshoe-like hindlegs which In general, comparing the burrowing behav- push soil backwards. This author considers that ior of subterranean species is very difficult, this way of removing earth would be a disad- due to the variability this behavior may show vantage in preventing the attack of predators. in different substrates, to the various tools used, However, this disadvantage could be counter- and to the variations in the frequency of use of acted by the good-enough vision of ctenomyids the different tools (Giannoni et al., 1992). (Pearson et al., 1968; Hickman, 1985), and the Consequently, we believe that these studies high frequency of scanning observed in C. need further information about hardness and peruanus and C. opimus (Pearson, 1959), and texture of the soil from the study area, neces- in C. eremophilus on the field and in the labo- sary to understand the adaptive value of bur- ratory (Table 2). Since on the field the se- rowing behavior. Hence, the diverse results quence always begins with scanning and sniff- found for different ctenomyids probably re- ing, this enables the animal to look out for flect several adaptive digging modes in re- predators. sponse to the different soils they inhabit. This Hickman (1985) reports that the tau can have assumption would be strengthened by the fact several uses in burrowing: it can be used to that C. pearsoni is a "scratcher" in a loose arrange and smooth the earth removed, and to substrate, similar to that of its habitat, although give strength to the body while digging, leav- it makes additional use of its incisors in a well- ing hindlegs free to kick backwards; and Sharpe packed substrate (Altuna et al., 1993). (1943) suggests that the tail is used to increase With respect to behavioral patterns, as a sensitivity in those species that remove the whole they are similar in all species of earth backwards. We found that, in Ctenomys ctenomyids studied, although there are some eremophilus, the tail could have at least three differences. Thus, the first part, "crumbling", functions: to provide the animal with support, of the so called "Phase 1: crumbling and accu- strength, and orientation inside the tunnels mulation (Fase 1: disgregación y acumulación)" while moving backwards. Thus, when scan- described for C. pearsoni by Altuna et al. ning, sniffing, grooming (claws or body), or (1993) coincides with our findings for C. pushing earth with the hindlegs, the animal BURROWING BEHAVIOR OF Ctenomys 169

would use its tail to stand upright, since it CAMÍN, S.R.; L.A. MADOERY and V. ROIG. 1995. The would be part of a tripod as suggested by burrowing behavior of Ctenomys mendocinus Hickman (1985). When crumbling the earth (Rodentia). Mammalia, 59:9-17. CASINOS, A.; J.P. GASC; S. RENOUS and J. BOU. with the forelegs the tail can be used as a prop, 1983. Les modalités de fouissage de Pitymys duodec- and to give the animal additional strength. imcostatus (Mammalia, Arvicolidae). Mammalia, Finally, the movement of the tail from one 47:28-36. side to the other, touching the terrarium walls, CONTRERAS, J.R. and V.G, ROIG. 1975. Ctenomys er- emophilus, una nueva especie de tuco-tuco de la región during the backward removal of earth, would de Ñacuñán, provincia de Mendoza (Rodentia, Oct- facilitate orientation inside the tunnel. This odontidae). Resúmenes de las 10 Jornadas Argentinas function has been mentioned for Geomys, and de Zoología, Corrientes, P. 17. Hickman (1985) suggests that the tail may be DE SANTIS, L.J.M. 1986. Estudio comparado del aparato masticatorio de los Ctenomyinae (Rodentia, Octodon- used in orienting and bracing the body when tidae) fósiles y vivientes. Tesis Doctoral de la Univ. digging. Nac. de La Plata, 64 pp, 100 1•m. It has then been proven that, while digging, DUBOST, G. 1968. Les mammiferes souterrains. Revue D'Ecologie et de Biologie du sol, 5: 99-133. Ctenomys eremophilus uses the forelegs in soft FAGEN, R.M. and D. Y. YOUNG. 1978. Temporal pat- substrates, and both forelegs and incisors in tems of behaviors: durations, intervals, latencies, and well-packed substrates, as the soil in the field. secuences. Pp. 79-114. In: Quantitative Ethology These results agree with those of Lessa (1990) (Colgan, P. W., ed). John Wiley y Sons, New York, 364 pp. and Justo et al. (1995) based on the morphol- GASC, J.P.; S. RENOUS; A. CASINOS; E. LAVILLE ogy of the digging apparatus and on incisor and J. BOU. 1985. Comparison of diverse digging microstructure, respectively. Furthermore, the patterns in some small mammals. Pp. 35-38. In: type and frequency of use of the burrowing Fortschritte der Zoologie, 30, Gustav Fischer Verlang, Stuttgart. tools would depend on the degree of hardness GIANNONI, S.M.; C.E. BORGHI and J.P. MARTÍNEZ of the soil. Finally, the burrowing behavior RICA. 1992. New data about the burrowing behaviour that we found in C. eremophilus is in agree- of Microtus (Pitymys) duodecimcostatus. Zeitschrift ment with Dubost (1968), who regards this für Sáugetierkunde, 57:23-28. GIANNONI, S.M.; C.E. BORGHI and J.P. MARTÍNEZ species as a "mixed" digger, and also with RICA. 1993. Comparing burrowing behaviour of the Hildebrand (1985), who considers it as a Iberian mole (Microtus (Terrícola) lusitanicus; "scratch- and chisel-tooth digger". M. (T.) pyrenaicus and M. (T.) duodecimcostatus). Mammalia, 57:487-490. HAMILTON, W.J. Jr. 1938. Life history notes on the northern pine mouse. Journal of Mammalogy, 19:163-' A CKNOWLEDGMENTS 170. HICKMAN, G. 1985. Surface-mound formation by the Stella M. Giannoni's and C. E. Borghi's research was Tuco-tuco, Ctenomys fulvus (Rodentia:Ctenomyidae), supported by a Fellowship from the CONICET. The au- with comments on earth-pushing in the other fosso- thors wish to express their gratitude to the members of rial mammals. Journal of Zoology, London, 205: 385- GIB (Grupo de Investigaciones de la Biodiversidad, 390. IADIZA, Argentina) for their interest and encouragement. HILDEBRAND, M. 1985. Digging of Quadrupeds. Pp. They also thank reviewers for their insightful comments. 89-109. In: Functional Vertebrate Morphology (M. N. Horak assisted with the English versioq. Hildebrand, D. Bramble, K. Liem, and D. Wake, eds). Harvard University Press, Cambridge, 430 pp. JARVIS, J.U.M. and J.B. SALE. 1971. Burrowing and burrow patterns of East African mole LITERATURE CITED , Heliophobius and Heterocephalus. Jour- nal of Zoology, London, 164:451-479. AGRAWAL, V.C. 1967. Skull adaptations in fossorial rodents. Mammalia, 21:300-312. JUSTO, E.R.; L. BOZZOLO and L.J.M. DE SANTIS. AIROLDI, J.-P.; R. ALTROCCHI and A. MEYLAN. 1995. Microstructure of the enamel of the incisors of 1976. Le comportement fouisseur du campagnol ter- some ctemyid and octodontid rodents (Rodentia, ). Mastozoología Neotropical, 2:43-51. restre, Arvicola terrestris scherman Shaw (Mamma- LAVILLE, E. 1989. Etude cinematique du fouissage chez lia, Rodentia). Revue Suisse de Zoologie, 83:282-286. Arvicola terrestris scherman ALTUNA, C.; G. IZQUIERDO and B. TASSINO. 1993. (Rodentia, Arvicolidae). Mammalia, 53:177-189. Análisis del comportamiento de excavación en dos LESSA, E.P. 1990. Morphological evolution of subterra- poblaciones del complejo Ctenomys pearsoni (Rodentia ). Bol. Soc. Zool. Uruguay, nean mammals: integrating structural, functional and 2° época, 8:275-282. ecological perspectives. Pp. 211-230. In: Evolution 170 S.M. Giannoni, C.E. Borghi and V.G. Roig

of subterranean mammals at the organismal and mo- REIG, O.; C. BUSCH; M. ORTELLS and J. CONTRE- lecular levels (E. Nevo and O.A. Reig eds). Alan R. RAS. 1990. An overview of evolution, systematics, Liss: New York, 422 pp. population biology, cytogenetics, molecular biology LESSA, E.P. 1993. Patrones de evolución morfológica en and speciation in Ctenomys. Pp. 71-96. In: Evolution roedores subterráneos americanos. Boletín de la of Subterranean Mammals at the Organismal and Sociedad de Zoología del Uruguay, 2° época, 8:37- Molecular Levels (E. Nevo and. O. Reig eds). Alan 46. R. Liss, Inc., New York. 422 pp. LESSA, E.P., and C.S. THAELER Jr. 1989. A reassess- SHARPE, W. M. 1943. A pocket (Geomys ment of morphological specializations for digging in lutescens) travels backward. Journal of Mammalogy, pocket gophers. Joumal of Mammalogy, 70:689-700. 24:99. MATHIAS, M.L. 1990. Morphology of the incisors and SIEGEL, S. 1986. Estadística no paramétrica. Quinta the burrowing activity of Mediterranean and Lusitanian edición. Editorial Trillas, México, 344 pp. pine voles (Mammalia, Rodentia). Mammalia, 54:302- SLATER, P.J.B. 1978. Data Collection. Pp. 7-24. In: Quan- 306. titative Ethology (P. W. Colgan ed). John Wiley & NEVO, E. 1961. Observation on israieli populations of Sons, New York, 364 pp. the mole rats Spalax ehrembergi, Nehring 1898. UBILLA, M. and C.A. ALTUNA. 1990. Analyse de la Mammalia, 25:127-144. morphologie de la main chez des espéces de Ctenomys NEVO, E. 1979. Adaptive convergence and divergence of de I'Uruguay (Rodentia: Octodontidae). Adaptations subterranean mammals. Annual Review of Ecology au fouissage et implications évolutives. Mammalia, and Systematics, 10:269-308. 54:107-117. PEARSON, O.P. 1959. Biology of the subterranean ro- ZAR, J.H. 1984. Biostatistical Analysis. Prentice-Hall In- dents, Ctenomys, in Perú. Memorias del Museo de ternational Editions, New Jersey, 718 pp. Historia Natural "Javier Prado", 9:1-56. PEARSON, O.; N. BINSZTEIN; L. BOIRY; C. BUSCH; M. DI PACE; G. GALLOPIN; P. PENCHASZADEH and M. PIANTANIDA. 1968. Estructura social, distribución espacial y composición por edades de una población de tuco-tucos (Ctenomys talarum). In- vestigaciones Zoológicas Chilenas, 13:47-79.