Journal of Mammalogy, 87(3):563–570, 2006

ANATOMICAL CORRELATES TO SCRATCH DIGGING IN THE FORELIMB OF EUROPEAN GROUND ( CITELLUS)

ANNA LAGARIA AND DIONISIOS YOULATOS* Aristotle University of Thessaloniki, School of Biology, Department of Zoology, GR-54124 Thessaloniki,

In northern Greece, European ground squirrels or sousliks (Spermophilus citellus) construct complex burrow systems by scratch-digging behavior. The present study investigated the presence of anatomical characters related to digging in the forelimb of S. citellus. The forelimb of 3 preserved specimens was dissected and several qual- itative and quantitative variables on selected muscles were collected. In addition, selected osteological variables and indices were calculated in a sample of 207 sciurid postcrania representing 14 burrowing and nonburrowing genera. Both analyses showed that the forelimb of S. citellus was characterized by enlarged and powerful shoul- der retractors, well-developed arm retractors with distal insertions upon a relatively robust humerus, enlarged elbow extensors associated with a long olecranon, and dominant pronators and carpal and digital flexors. Similar morphology is also encountered in other semifossorial , indicating significant adaptations to scratch- digging behavior. However, the characters examined designate a more compromised morphology, associated with the generalized postcranium of sciurids. On the other hand, S. citellus exhibits a more specialized forelimb morphology, compared to that of other marmotines, for a semifossorial way of life, in association with the sub- generic derived morphology, lack of social interactions, and exploitation of a habitat with harder soils.

Key words: forelimb, muscles, osteology, scratch digging, Spermophilus citellus

Many mammals are active aboveground and yet are likewise extended forearm at the elbow joint, and a flexed or sta- highly adapted to dig. All are described as semifossorial in bilized wrist and forefoot (Gasc et al. 1985; Stalheim- terms of digging ability and are able to construct simple or Smith 1984). complex systems of burrows (Hildebrand 1995; Reichman and In terms of osteomuscular anatomy, the shoulder joint of Smith 1990). In semifossorial mammals, burrow construction is scratch diggers is characterized by well-developed and power- accomplished mainly by the claws of the forelimbs in an action ful humeral retractors, such as the teres major and latissimus described as scratch digging and involves 2 phases (Gasc et al. dorsi, with extensive origins and relatively distal insertions on 1985; Hildebrand 1995): the digging phase, when the a particularly robust humerus (Bou et al. 1990; Bryant 1945; moves the forelimbs alternatively and very rapidly, while the Fernandez et al. 2000; Gambaryan and Gasc 1993; Hildebrand body is supported by the hind limbs; and the clearing phase, 1995; Lessa and Stein 1992; Price 1993; Vassallo 1998). At the when support is brought to the forelimbs, and the accumulated elbow joint, the extensors triceps brachii are particularly de- soil particles are kicked by a simultaneous backward extension veloped and associated with a relatively long olecranon process of the hind limbs. The physical and mechanical properties of (Bryant 1945; Fernandez et al. 2000; Hildebrand 1995; Lessa the substrate that interact with forelimbs during the phase of and Stein 1992; Vassallo 1998). More distally, the forearm the loosening of the soil require that scratch diggers must be is characterized by very strong pronators and carpal and capable of applying great out-force (i.e., force derived) against digital flexors, such as the flexor digitorum profundus, that the substrate (Hildebrand 1995). This appears to be accom- originate from a notably prominent humeral medial epicondyle plished by the combination of a strongly retracted (flexed) (Fernandez et al. 2000; Gambaryan and Gasc 1993; Lessa and humerus at the shoulder joint, an actively pronated and Stein 1992; Vassallo 1998). These morphological adaptations appear to enhance out-force of the forelimb during burrow construction and maintenance. * Correspondent: [email protected] Simple or elaborate systems of burrows are common in semifossorial ground squirrels. Ground squirrels are diurnal Ó 2006 American Society of Mammalogists that live in and exploit open areas, and dig burrows by www.mammalogy.org scratch digging. Burrow construction may not be a frequent 563 564 JOURNAL OF MAMMALOGY Vol. 87, No. 3

TABLE 1.—Functional muscle groups of the forelimb of Spermo- MATERIALS AND METHODS philus citellus. The left forelimbs of 3 European ground squirrels preserved in 10% Muscle group and muscles formaldehyde solution were dissected. The sample was composed of 1 eviscerated adult female (body weight of preserved specimen was Extrinsic scapular muscles 278.3 g) and 2 eviscerated subadult males (body weights of preserved Trapezius, atlantoscapularis ventralis, serratus ventralis, occipitoscapularis, specimens were 162.6 g and 162.0 g) from northern Greece and latissimus dorsi, rhomboideus, pectoralis major, pectoralis minor, belonged to the collections of the Department of Zoology of the pectoralis abdominalis Aristotle University of Thessaloniki (Appendix I). In northern Greece, Intrinsic scapular muscles both adult females and subadults spend 0.2–1.4% of total diurnal time Infraspinatus, supraspinatus, subscapularis, teres major, teres minor, in burrowing activities, showing no significant differences between deltoideus, coracobrachialis, subclavius them (Boutsis 2002). Elbow flexors For each muscle, the position of both the origin and insertion were Biceps brachii, brachioradialis, brachialis, clavobrachialis measured to the nearest 0.01 mm relative to the proximal end of the Elbow extensors bone. Subsequently, muscles were trimmed from fat and tendons and Triceps brachii, dorsoepitrochlearis their length was measured to the nearest 0.01 mm. All measurements Forearm pronators were taken with the aid of digital calipers (Mitutoyo, Kanagawa, Pronator teres, pronator quadratus Japan). In this way, the relative positions of both origin and insertion of each muscle were expressed as percentages from the proximal end Forearm supinators of the respective bone. For comparisons with previous studies, we Supinator used muscle nomenclature as reported by Thorington et al. (1997). Carpal and digital flexors All detached muscles were oven-dried for 24 h until complete Flexor carpi ulnaris, palmaris longus, flexor carpi radialis, flexor dehydration and were subsequently weighed to the nearest 0.0001 g digitorum sublimis, flexor digitorum profundus with the aid of an analog precision balance (August Sauter GmbH, Carpal and digital extensors Ebingen, Germany). Muscles were classified into joint functional Extensor carpi radialis longus, extensor carpi radialis brevis, extensor groups according to their point of origin, plane of action, or both digitorum communis, extensor indicis, extensor digiti quinti proprius, (Table 1). In this way, weights of selected muscles or muscle groups extensor carpi ulnaris were expressed as percentages of the functional groups they allegedly belonged to. Furthermore, to assess strength of muscles, we calculated the physiological cross-sectional area (PCSA), which indirectly behavior among ground squirrels but appears to be critical to estimates the peak isometric force (e.g., Brown et al. 2003). PCSA (in cm2) was determined from muscle weight (M), muscle density the survival of the species, because burrows are used for pred- (q ¼ 1.06 g/cm3), and muscle fiber length (L), whereby PCSA ¼ M/ ator avoidance, protection from extreme environmental con- (q L). For simplicity, measured muscle length replaced fiber length. ditions, food hoarding, parturition, lactation for the young, and In addition to muscular parameters, we measured 7 selected linear (Elliott and Flinders 1991; Jenkins and Eshelman variables of the humerus, ulna, and metacarpal III to the nearest 0.01 1984; Michener and Koeppl 1985; Yensen and Sherman 1997). mm with the aid of digital calipers (Fig. 1). The linear variables Thus, given that scratch digging is an integral part of their measured were humeral length (HL): length from head to capitulum; biology that may increase fitness, it is very likely that ground humeral width (HW): mediolateral width at midpoint of shaft; deltoid squirrels exhibit associated morphological correlates. process position (DPP): length from humeral head to midpoint of The present study aims to examine whether scratch-digging deltoid process; epicondyle width (HEW): mediolateral width at the activity in ground squirrels can be correlated with associated level of the epicondyles; ulnar length (UL): length from olecranon to morphofunctional adaptations. For this purpose, we used styloid process; olecranon length (OL): length from top of olecranon to midpoint of sigmoid cavity; and metacarpal III length (ML): length European ground squirrels or sousliks (Spermophilus citellus) from proximal to distal point. These measurements have been repeat- as study subjects. The species inhabits open natural plains and edly used in studies of fossorial adaptations among mammals and were cultivated lands, ranging from central Europe to northern used to calculate 5 functional indices: epicondyle index ¼ HEW/HL: Greece (Krystufek 1999). S. citellus is asocial and constructs an indicator of the relative width of the distal humerus available for the and maintains simple and elaborate burrows by scratch digging origin of the flexor, pronator, and supinator muscles of the forearm (Krystufek 1999). Each burrow system is occupied by a single related to fossorial activities; humeral robusticity index ¼ HW/HL: an animal and possesses 1–5 entrances with tunnels that vary in indicator of the ability of the humeral shaft to resist bending and length from 0.7 to 4.5 m, reaching a maximal depth of 2 m (Hut searing stresses; shoulder moment index ¼ DPP/HL: an indicator of 2001). Although burrowing activity represents only 0.2–2.0% the mechanical advantage of the deltoid and major pectoral muscles of total diurnal activity (Boutsis 2002; Hut 2001), burrows are acting across the shoulder joint; index of fossorial ability ¼ OL/(UL extensively used for hibernation, escape, and resting during the OL): a measure of the mechanical advantage of the triceps and dorsoepitrochlearis muscles during elbow extension; and triceps meta- active season (Boutsis 2002; Hut 2001), and appear to repre- carpal out-force index ¼ OL/(UL þ ML OL): estimates the down- sent a considerable investment in offspring (Huber et al. 2002). ward force generated at the distal end of the metacarpal per unit of In this context, this report aims to assess the degree of special- triceps in-force (i.e., applied force of the muscle), assuming negligible izations for digging in the forelimb of S. citellus by studying length of wrist elements (Price 1993). selected muscular and osteological characters that have been The sample of skeletal specimens was composed of 207 skeletons repeatedly associated with similar activities in other mammals. representing 14 extant sciurid genera (39 species) from the collections June 2006 LAGARIA AND YOULATOS—SOUSLIK FORELIMB ADAPTATIONS TO DIGGING 565

TABLE 2.—Physiological cross-sectional area for selected muscles of Spermophilus citellus. Only the muscles of the different functional groups associated with scratch digging and bearing relatively high physiological cross-sectional area values are presented.

Muscle group and muscle n X (cm2) SD Extrinsic scapular muscles Latissimus dorsi 1 53.8 103 Occipitoscapularis 1 8.5 103 Intrinsic scapular muscles Teres major 1 27.3 103 Elbow flexors Clavobrachialis 3 9.2 103 1.6 103 Elbow extensors Triceps brachii caput longum 3 54.4 103 4.6 103 Triceps brachii caput laterale 3 21.0 103 2.8 103 Triceps brachii caput mediale 3 8.8 103 5.0 103 Forearm pronators Pronator teres 3 2.9 103 1.8 103 Carpal and digital flexors Flexor digitorum profundus 3 11.4 103 6.7 103

Callosciurus and Funambulus are sister taxa characterized by arboreal adaptations, whereas the Funisciurus, Heliosciurus, and Protoxerus belong to the arboreal–scansorial tribe Protoxerini, which is a sister taxon to the terrestrial Marmotini (Steppan et al. 2004). The arbo- real Ratufa is reported as a basal sciurid, whereas Sciurus and Tamiasciurus are nested within the paraphyletic tribe Sciurini (Steppan et al. 2004). For each index, we calculated means and 1 SD, and differences between functional groups were tested using the nonparametric Mann–Whitney test (Zar 1996).

RESULTS FIG.1.—Osteological measurements on the humerus and ulna of Myological findings.—This part presents the anatomy of Spermophilus (S. richardsonii; USMNH 552457, adult female): A–B) forelimb muscles of S. citellus that are functionally related to humeral length; C–D) humeral width; A–E) deltoid process position; scratch-digging behavior. Thus, only the muscles with signifi- F–G) epicondyle width; H–I) ulnar length; H–J) olecranon length. cant percentages of mass relative to certain functional groups, and with relatively high PCSA values are reported and discussed (Tables 2 and 3). Of all extrinsic scapular muscles of the United States Museum of Natural History (USMNH) in examined, the occipitoscapularis constituted the most powerful Washington, D.C. (Appendix I). The specimens studied were divided retractor of the scapula. The muscle originated from the upper into 2 functional groups. The 1st group, defined as burrowers, repre- sented mainly terrestrial sciurids that dig extensive burrow systems, three-fourths of the nuchal line to insert on the cranial one-half and was composed of the following species: Ammospermophilus of the vertebral border of the scapula superficially to the harrisii, A. leucurus, Cynomys gunnisoni, C. ludovicianus, Marmota insertion of the rhomboid. The muscle was relatively powerful caligata, M. caudata, M. himalayana, M. monax, Sciurotamias (Table 2) and represented 7.06% of the extrinsic scapular davidianus, Spermophilus columbianus, S. lateralis, S. major, S. muscle group (Table 3). Other extrinsic scapular muscles that richardsonii, S. spilosoma, S. tridecemlineatus, S. undulatus, S. could possibly contribute to scapular retraction, such as parts of variegatus, and Tamias striatus. Recent phylogenetic analyses support the rhomboideus or trapezius, were found to be underdevel- that all these species belong to the tribe Marmotini, which is charac- oped (Lagaria 2004). terized by terrestrial burrowing activities (Steppan et al. 2004). The The latissimus dorsi was the main extrinsic humeral 2nd group, defined as nonburrowers, was composed of arboreal and retractor. It took its origin from all thoracic vertebrae and scansorial species that seldom dig extensive burrow systems but may occasionally dig for food caches, including Callosciurus erythraeus, ventrally from ribs 4–7. The muscle ended in a flat tendon that C. finlaysonii, C. notatus, C. prevostii, Funambulus pennantii, was common with that of teres major and inserted on the distal Funisciurus isabella, F. lemniscatus, F. pyrropus, Heliosciurus 36.2% of the medial surface of the humerus. Latissimus was rufobrachium, Protoxerus stangeri, Ratufa affinis, R. bicolor, R. one of the most powerful muscles with 1 of the 2 highest PCSA indica, R. macroura, Sciurus aberti, S. aestuans, S. carolinensis, S. values (Table 2), and represented 20.8% of extrinsic scapular niger, S. variegatoides, S. vulgaris, and Tamiasciurus hudsonicus. muscles (Table 3). 566 JOURNAL OF MAMMALOGY Vol. 87, No. 3

TABLE 3.—Percentages of mass of specific muscles in relation to (Table 2). Pronator quadratus took its origin from the distal mass of functional muscle groups they purportedly belong to and 73.5–89% of the radial surface of the ulna to insert on the distal percentages of mass of muscle groups in relation to total muscle mass 79.9% of the ulnar surface of the radius. of specific articulations. In general, carpal and digital flexors dominated forearm ex- Muscle group and muscle n XSD tensors in muscle mass (Table 3). The major digital flexor was the flexor digitorum profundus, which represented almost one- Extrinsic scapular muscles half of all flexor musculature (Table 3) and was 4.7 times Latissimus dorsi 3 20.84 2.63 heavier than the superficial digital flexor. The flexor digitorum Occipitoscapularis 3 7.06 0.49 profundus was composed of 4 heads. Two heads originated Intrinsic scapular muscles from the anterior surface of the medial epicondyle, 1 from the Spinodeltoideus 3 5.90 2.03 distal 19.5–47.7% of the radial surface of the ulna, and 1 from Teres major 3 15.93 3.61 the distal 35.4–61.5% of the ulnar side of the radius. The Elbow joint 4 heads converged to a common tendon and were distributed in Extensors 3 67.21 4.85 a variable way to the palmar side of the distal phalanx of digits Elbow flexors 2–5. The PCSA value of the flexor digitorum profundus de- Clavobrachialis 3 20.57 1.16 picted a quite powerful muscle (Table 2). Forearm rotators Osteological findings.—The functional indices of the fore- Pronators 3 82.25 10.39 limb distinguished well between burrowing and nonburrowing Carpal and digital flexors and extensors sciurids. The epicondyle index illustrated the relative de- Flexors 3 76.85 5.60 velopment of the humeral medial epicondyle, which is the area Carpal and digital flexors of origin of forearm pronators and carpal and digital flexors. Flexor digitorum profundus 3 48.90 1.64 Burrowing sciurids scored significantly higher values (Mann– Whitney, Z ¼5.60, P , 0.001) than those of nonburrowing species (Table 4). S. citellus from Greece scored the highest, with values that were closer to those of Cynomys (although this The main intrinsic humeral retractors were the spinodeltoi- may be related to the small sample size of S. citellus; Table 4). deus and teres major. The former represented 47.3% of the The humeral robusticity index indirectly estimated the deltoid mass and 5.9% of total intrinsic scapular muscle mass. It stresses applied on the shaft of the bone during humeral activity. originated from the distal 34.6–85.4% of the scapular spine and Burrowing sciurids possessed significantly more-robust humeri inserted via a short, flat tendon on the lateral side of the deltoid (Mann–Whitney, Z ¼4.71, P , 0.001) than those of non- process at the distal 42.8% of the humerus. Teres major took its burrowing species (Table 4). The scores of S. citellus were the origin from the proximal 44.1% of the caudal scapular border highest, approximating those of Marmota (Table 4). and inserted along with the tendon of latissimus on the distal The relative mechanical advantage of the deltoid was assessed 36.2% of the humerus. The teres major represented 15.9% of the by the shoulder moment index. The values of burrowing intrinsic scapular musculature (Table 3) and was among the squirrels were significantly higher (Mann–Whitney, Z ¼4.88, most powerful muscles with a high PCSA value (Table 2). P , 0.001), indicating a relatively distal deltoid process The clavobrachialis appeared to be among the most compared to that of nonburrowing squirrels (Table 4). Once important elbow flexors. It took its origin from the ventral again, S. citellus, Cynomys, and Marmota scored the highest surface of the distal 41.9–78.5% of the clavicle to insert via values (Table 4). a tendon on the distal 54% of the ulna. It represented 20.6% of The mechanical advantage of the triceps, reflected by the total elbow flexor muscle mass and scored a significant PCSA relative elongation of the olecranon process, was estimated by value (Tables 2 and 3). The 3 parts of the triceps brachii were the index of fossorial ability. Burrowing squirrels scored sig- the main elbow extensors and represented 67.2% of all elbow nificantly higher index values (Mann–Whitney, Z ¼10.65, musculature (Table 3). The long head took a tendinous origin P , 0.001); that is they possessed relatively long olecrana from the distal 63.3–87.3% of the caudal scapular border. The compared to that of nonburrowing genera (Table 4). Within other 2 heads originated from the humerus, the lateral head burrowing squirrels, S. citellus scored similar to Ammosper- from the distal 20.1–27.5% of the lateral surface and the medial mophilus, whereas Tamias and Sciurotamias scored the lowest one from the 22.6–67.2% of the posteromedial surface. All values (Table 4). heads joined in the distal two-thirds of the brachium and in- The force of the triceps muscles generated at the end of the serted via tendon on the proximal, medial, and lateral surface of metacarpals was estimated by the triceps metacarpal out-force the olecranon process. The long head was the most powerful index. Values of burrowing sciurids were significantly higher muscle in S. citellus, as shown by the PCSA (Table 2). (Mann–Whitney, Z ¼8.24, P , 0.001) than those of The forearm pronators were well developed, largely nonburrowing sciurids, indicating higher out-force (force dominating the rotatory musculature (Table 3). Pronator teres derived from a muscle) at the metacarpals per triceps muscle took a tendinous origin from the anterior surface of the medial unit in-force (applied force of a muscle; Table 4). In contrast, humeral epicondyle and inserted distally on the 68.9% of the S. citellus scored relatively low values between Sciurotamias ulnar surface of the radius. This muscle was relatively powerful and Ammospermophilus (Table 4). June 2006 LAGARIA AND YOULATOS—SOUSLIK FORELIMB ADAPTATIONS TO DIGGING 567

TABLE 4.—Selected osteological indices in Spermophilus citellus compared to other burrowing and nonburrowing sciurid genera.

Index Epicondyle Humeral robusticity Shoulder moment Fossorial ability Triceps metacarpal out-force Group n (X 6 SD)(X 6 SD)(X 6 SD)(X 6 SD)(X 6 SD) Spermophilus citellus 3 0.323 6 0.007 0.118 6 0.003 0.469 6 0.039 0.205 6 0.045 0.142 6 0.024 Other burrowers Ammospermophilus 10 0.242 6 0.010 0.082 6 0.005 0.407 6 0.018 0.196 6 0.018 0.152 6 0.023 Spermophilus 53 0.265 6 0.015 0.087 6 0.008 0.436 6 0.021 0.224 6 0.019 0.177 6 0.023 Cynomys 15 0.291 6 0.011 0.093 6 0.004 0.464 6 0.014 0.250 6 0.013 0.196 6 0.024 Marmota 13 0.286 6 0.010 0.100 6 0.007 0.478 6 0.019 0.251 6 0.011 0.208 6 0.026 Tamias 12 0.253 6 0.009 0.079 6 0.005 0.404 6 0.025 0.169 6 0.013 0.157 6 0.024 Sciurotamias 9 0.247 6 0.008 0.078 6 0.004 0.401 6 0.009 0.172 6 0.032 0.133 6 0.026 All other burrowers 112 0.266 6 0.010 0.087 6 0.009 0.435 6 0.031 0.217 6 0.033 0.175 6 0.031 Nonburrowers Callosciurus 12 0.252 6 0.014 0.081 6 0.006 0.400 6 0.023 0.170 6 0.009 0.137 6 0.017 Protoxerus 4 0.239 6 0.003 0.083 6 0.002 0.432 6 0.018 0.168 6 0.001 0.127 6 0.002 Heliosciurus 3 0.224 6 0.004 0.083 6 0.004 0.400 6 0.003 0.163 6 0.005 0.139 6 0.026 Funisciurus 7 0.225 6 0.007 0.079 6 0.005 0.382 6 0.033 0.144 6 0.011 0.118 6 0.015 Ratufa 8 0.241 6 0.015 0.082 6 0.005 0.399 6 0.026 0.162 6 0.005 0.139 6 0.018 Funambulus 3 0.234 6 0.006 0.077 6 0.010 0.411 6 0.015 0.159 0.159 Tamiasciurus 12 0.254 6 0.008 0.078 6 0.004 0.413 6 0.019 0.163 6 0.010 0.153 6 0.022 Sciurus 44 0.256 6 0.013 0.083 6 0.006 0.423 6 0.021 0.162 6 0.012 0.140 6 0.022 All nonburrowers 92 0.249 6 0.015 0.081 6 0.006 0.413 6 0.025 0.162 6 0.012 0.139 6 0.021

DISCUSSION S. citellus. This morphology also characterizes other burrowing mammals (Gambaryan and Gasc 1993; Gasc et al. 1986; Scratch digging constitutes an essential part of the biology of Hildebrand 1995; Lessa and Stein 1992; Vassallo 1998). The semifossorial mammals, because it permits the construction of anatomical position of these muscles implies substantial arm extensive burrow systems that appear to enhance fitness. This is retraction, necessary during the digging phase of scratch further reflected in a series of forelimb osteomuscular features digging (Gasc et al. 1985; Stalheim-Smith 1984). However, the that are commonly shared by many phylogenetically distant lack of a prominent teres major process on the scapula of taxa (Hildebrand 1995). The present study showed that some burrowing sciurids (Bryant 1945) suggests that the teres major of these morphofunctional correlates are also shared by the may not provide the same mechanical advantage to arm retrac- European ground . More particularly, the forelimb of S. tion as in other fossorial mammals (Hildebrand 1995; Lessa citellus was characterized by well-developed scapular retractors and Stein 1992; Vassallo 1998). This may also be implied by (occipitoscapularis), arm retractors (spinodeltoideus, latissimus the lower out-forces of both teres major and latissimus dorsi in dorsi, and teres major) with distal insertions upon a robust burrowing sciurids compared to arboreal forms (Stalheim- humerus, elbow extensors (triceps brachii) and flexors Smith 1984). However, their longer mean contraction time and (clavobrachialis), forearm pronators with distal insertions, and greater resistance to fatigue (Stalheim-Smith 1984) may indi- carpal and digital flexors (flexor digitorum profundus) with cate more controlled actions, in cooperation with another extensive origins from a prominent medial humeral epicondyle. intrinsic scapular unit, the pars spinalis of the deltoideus. Similar features appear to improve the mechanical advantage In effect, spinodeltoideus was well developed and inserted of the osteomuscular system during the digging phase in order to loosen the soil (Gasc et al. 1985; Hildebrand 1995). distally on the humerus in S. citellus. A similar morphology The occipitoscapularis of S. citellus was an enlarged and also is found in semifossorial claw-digging caviomoprh rodents powerful muscle. A similar condition is encountered in scratch- (Elissamburu and Vizcaino 2004). The anatomical position of digging geomyine rodents, when compared to nonfossorial the muscle appears to promote powerful arm retraction, and forms (Lessa and Stein 1992). The anatomical position of the this was also implied by the relative high values of the shoulder muscle suggests powerful cranial pulling of the proximal part moment index. Similar values characterize all burrowing of the scapula (near the vertebral border), contributing to scap- squirrels, as well as other burrowing rodents and armadillos, ular retraction (see also Thorington et al. 1997). This move- indicating its significant mechanical advantage on arm re- ment would displace caudally the shoulder joint (distal part of traction necessary during the digging phase of scratch digging the scapula) and contribute to overall arm retraction, which is (Elissamburu and Vizcaino 2004; Fernandez et al. 2000; necessary during the digging phase of loosening the soil (Gasc Laville et al. 1989). et al. 1985; Stalheim-Smith 1984). The action of arm retractors implies the presence of high Latissimus dorsi and teres major were both well developed loads on the humeral shaft, coupled with those imposed by the and powerful and possessed a common distal insertion in resistance of the substrate. The humeral shaft of S. citellus was 568 JOURNAL OF MAMMALOGY Vol. 87, No. 3 particularly robust, a condition that characterized all burrowing importance in other digging rodents and are further character- sciurids, other semifossorial rodents, and most burrowing ized by extensive origins upon the medial humeral epicondyle mammals (Bou et al. 1990; Bryant 1945; Elissamburu and (Elissamburu and Vizcaino 2004; Fernandez et al. 2000; Vizcaino 2004; Fernandez et al. 2000; Gambaryan and Gasc Gambaryan and Gasc 1993; Hildebrand 1995; Lessa and Stein 1993; Hildebrand 1995; Laville et al. 1989). This robust mor- 1992; Vassallo 1998; Vizcaino and Milne 2002). The signifi- phology enables the shaft to withstand high and frequent cant, high values of the epicondyle index suggested prominent stresses, similar to those imposed during digging, without medial epicondyles in S. citellus and all burrowing sciurids (see breakage (Hildebrand 1995). also Bryant 1945). However, this appeared to be the result of At the elbow joint, S. citellus possessed well-developed and the combination of relatively short humeri and large epicon- very powerful triceps brachii muscles, as is the case of other dyles in all burrowing forms compared to longer shafts and burrowing mammals (Bryant 1945; Fernandez et al. 2000; shorter epicondyles in scansorial and arboreal forms (Lagaria Gambaryan and Gasc 1993; Gasc et al. 1985; Hildebrand 1995; 2004). In all cases, this morphology provides a good leverage Lessa and Stein 1992; Vassallo 1998). Well-developed elbow for these muscles and thus a mechanical advantage (Hildebrand extensors were coupled with an enlarged olecranon process 1995). These muscles operate wrist and digit flexion that are as also indicated by the index of fossorial ability. The index essential during the digging phase, as maximal forelimb out- separated well between burrowing and nonburrowing members force is applied upon the substrate (Gambaryan and Gasc 1993; of the family Sciuridae, but appears to have limited value across Hildebrand 1995; Stalheim-Smith 1984). Among these mus- different mammalian clades as imposed by phylogenetic cles, the flexor digitorum profundus, which sends tendons di- constraints. However, when single clades are concerned, bur- rectly to the ungual phalanges, was exceptionally developed rowing taxa almost always exhibit longer olecrana compared to in S. citellus, a condition also encountered in many burrowing nonburrowing forms (Elissamburu and Vizcaino 2004; Fernan- rodents (Bryant 1945; Gambaryan and Gasc 1993; Lessa and dez et al. 2000; Price 1993; Vizcaino et al. 1999; Vizcaino and Stein 1992). Milne 2002). In effect, a long olecranon process increases the The present study of the forelimb of S. citellus showed that in-lever, and thus improves the action of the enlarged triceps, the species exhibits some morphofunctional adaptations that resulting in greater out-force at the level of the metacarpals are related to shoulder and arm retraction, elbow extension, (Hildebrand 1995; Price 1993). This is necessary for dissoci- forearm pronation, and carpal and digital flexion. These move- ating soil particles during the digging phase. However, the ments facilitate the digging phase of scratch digging during triceps–metacarpal index, although distinguishing between burrow construction and maintenance (Gasc et al. 1985; burrowing and nonburrowing sciurids, did not produce con- Hildebrand 1995). Burrows are essential for S. citellus,asin vincing results. Values were low for S. citellus and were near the other ground squirrels and semifossorial mammals, because scores of arboreal sciurids. Stalheim-Smith (1984) found that burrows provide enhanced independence from the variability the triceps of arboreal squirrels produced larger out-forces than of external conditions and risk of predation. These advantages those of semifossorial sciurids and associated this finding with enable S. citellus to use burrows for food caching, predator rapid grasps during vertical trunk claw climbing that enables avoidance, birth and nourishing of the young, and hibernation, escape from predators. This implies that S. citellus and many and may therefore contribute to increased fitness (Nevo 1979; semifossorial sciurids may not exhibit the highly specialized Reichman and Smith 1990). morphological complex that characterizes other scratch-digging However, the high energetic cost of burrowing (Nevo 1979; rodents, because they also engage in other frequent and critical Reichman and Smith 1990) would select for increased effi- behaviors, such as alert and feeding postures (Boutsis 2002). ciency of the involved morphological tools. This appears to be The digging phase requires the arrangement of the forearm in true for most subterranean mammals (Hildebrand 1995), but a pronated position, because palm and claws are placed facing may not be valid for ground squirrels (see Stalheim-Smith toward the substrate. This is accomplished by forearm flexors 1984). Ground squirrels are derived from an ancestral stock of that simultaneously pronate the forearm, as well as enlarged arboreal forms and possess a relatively generalized postcra- and powerful forearm pronators. In S. citellus and other bur- nium that retains arboreal adaptations (Emry and Thorington rowing Marmotini, the former role appears to be played by the 1982; Stalheim-Smith 1984; Steppan et al. 2004). The semi- clavobrachialis (Bryant 1945; Thorington et al. 1997). This fossorial sciurids examined in this study consistently presented distinct muscle was relatively powerful and well represented osteological correlates to scratch digging that differentiated among the flexor musculature of the elbow in S. citellus, but them well from nonburrowing sciurids. However, they all comparable data are not available in the literature. Similarly, belonged to a single tribe (Marmotini). The tribe is character- the distal insertion of the enlarged forearm pronators further ized by few apomorphic postcranial features, such as the form contributed to an actively pronated forearm. Similar anato- of the coracoid, acromion, and teres major process, and the mical organization characterizes other burrowing mammals, presence of a clavobrachialis, which are very likely related to aiding in the effective arrangement of the forearm at a pro- digging activities and may represent characters inherited from nated position (Fernandez et al. 2000; Gasc et al. 1986; a common ancestor (Bryant 1945; Thorington et al. 1997). Vassallo 1998). Unfortunately, postcranial material of the other semifossorial Distally, S. citellus was characterized by relatively well- tribe (Xerini) was unavailable to test for convergent morphol- developed and powerful flexors. These muscles also gain in ogies related to this derived way of life. June 2006 LAGARIA AND YOULATOS—SOUSLIK FORELIMB ADAPTATIONS TO DIGGING 569

On the other hand, it appears that some marmotines (e.g., (Mammalia, Rodentia): cinefluorographical, anatomical, and bio- Cynomys) may not be highly specialized for scratch digging, as mechanical analyses of burrowing. Zoologische Jahrbucher Anat- revealed by several biomechanical features of the forelimb omie 123:363–401. (Stalheim-Smith 1984). This was related to the soft soils they GASC, J.-P., S. RENOUS,A.CASINOS,E.LAVILLE, AND J. BOU. 1985. exploit and their communal social systems (Stalheim-Smith Comparison of diverse digging patterns in some small mammals. Fortschritte der Zoologie 30:35–38. 1984). The present research showed that this also may be true for GASC, J.-P., S. RENOUS, AND E. LAVILLE. 1986. Myologie de la region S. citellus. However, the subgenus Citellus, to which European scapulo-hume´rale chez deux mammife`res souterraines, Spalax grounds squirrels belong, appears to be highly specialized in ehrenbergi (Rodentia) et Eremitalpa granti (Insectivora). Annales external morphology (Bryant 1945), most likely related to a de la Socie´te´ Royale Zoologique de Belgique 116:61–70. derived semifossorial way of life. In effect, S. citellus is asocial, HILDEBRAND, M. 1995. Analysis of vertebrate structure. John Wiley and unlike Cynomys each animal is responsible for its own and Sons, New York. extensive burrow system. This, in combination with the HUBER, S., E. MILLESI, AND J. P. DITTAMI. 2002. Paternal effort and its relatively harder soils the species exploits in southern Europe, relation to mating success in the European ground squirrel. Animal may be related to the more specialized burrowing morphological Behaviour 63:157–164. complex observed. However, further detailed analysis of the HUT, R. A. 2001. Natural entrainment of circadian systems: a study in osteomusuclar system and digging behavior of the same species the diurnal ground squirrel (Spermophilus citellus). Ph.D. disserta- in habitats with different soil characteristics, as well as different tion, Rijksuniversiteit Groningen, Groningen, Netherlands. JENKINS, S. H., AND B. D. ESHELMAN. 1984. Spermophilus beldingi. species is required to determine subtle relationships between Mammalian Species 221:1–8. morphological adaptations and ecological factors that character- KRYSTUFEK, B. 1999. Spermophilus citellus. Pp. 190–191 in Atlas ize these morphofunctional associations among ground squirrels. of European mammals (A. J. Mitchell-Jones, et al., eds.). Poyser Natural History, London, United Kingdom. ACKNOWLEDGMENTS LAGARIA, A. 2004. Morphological adaptations of the forelimb of We acknowledge financial support provided by the Aristotle sousliks, Spermophilus citellus (Rodentia, Mammalia) to scratch- University of Thessaloniki. We also want to express our warm thanks digging. B.S. thesis, University of Thessaloniki, Thessaloniki, to S. Kalpakis and Y. Boutsis, who provided the collections of the De- Greece (in Greek). partment of Zoology with preserved specimens of European ground LAVILLE, E., A. CASINOS, J.-P. GASC,S.RENOUS, AND J. BOU. 1989. squirrels. DY particularly thanks R. W. Thorington, Jr., for authorizing Les me´canismes du fouissage chez Arvicola terrestris et Spalax access at the collections at the USMNH and for all his help ehrenbergi:e´tude fonctionelle et e´volutive. Anatomische Anzeiger during DY’s stay in Washington, D.C. Many thanks also go to S. 169:131–144. Vizcaino, R. W. Thorington, Jr., and 1 anonymous reviewer for con- LESSA, E. P., AND B. R. STEIN. 1992. Morphological constraints in the structive remarks on previous drafts of the manuscript. digging apparatus of pocket gophers (Mammalia: Geomyidae). Biological Journal of the Linnean Society 47:439–453. MICHENER, G. R., AND J. W. KOEPPL. 1985. Spermophilus richardsonii. LITERATURE CITED Mammalian Species 243:1–8. BOU, J., J. CASTIELLA,J.OCANA, AND A. 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VIZCAINO, S. F., AND N. MILNE. 2002. Structure and function in Marmota caligata (3).—271698, 271701, 583155. armadillo limbs (Mammalia: Xenartha: Dasypodidae). Journal of Marmota caudata (2).—173381, 173386. Zoology (London) 257:117–127. Marmota himalayana (3).—198637, 198638, 255958. YENSEN, E., AND P. W. SHERMAN. 1997. Spermophilus brunneus. Marmota monax (5).—297840, 349711, 397378, 514747, 514748. Mammalian Species 560:1–5. Protoxerus stangeri (4).—237333, 539438, 539443, 543111. ZAR, J. H. 1996. Biostatistical analysis. Prentice Hall, London, United Ratufa affinis (2).—151757, 317202. Kingdom. Ratufa bicolor (2).—49703, 261070. Ratufa indica (2).—155401, 308415. Submitted 21 July 2005. Accepted 26 October 2005. Ratufa macroura (1).—269970. Sciurotamias davidianus (9).—258507, 258508, 258509, 258511, Associate Editor was Eric A. Rickart. 258512, 258513, 258514, 258516, 259735. Sciurus aberti (7).—448232, 448233, 448234, 448235, 548403, 548404, 548405. APPENDIX I Sciurus aestuans (2).—548445, 548446. Specimens examined.—Specimens used in this study are housed in Sciurus carolinensis (12).—248250, 347937, 347938, 347939, the Zoological Museum of the School of Biology, Aristotle University 347948, 396996, 397042, 397099, 397180, 397182, 397211, 541441. of Thessaloniki (ZMUTH), Thessaloniki, Greece, and the United Sciurus niger (12).—264948, 397092, 397093, 397094, 397118, States Museum of Natural History (USMNH), Washington, D.C. 397120, 397121, 397166, 548037, 548043, 548045, 548047. Material of S. citellus studied (n ¼ 3) included both preserved and Sciurus variegatoides (8).—449011, 449012, 449014, 449015, postcranial specimens that are yet uncatalogued in ZMUTH. The 449016, 449017, 449018, 449019. following comparative specimens were exclusively postcranial mate- Sciurus vulgaris (3).—581893, 582904, 582905. rial housed in USMNH. Spermophilus columbianus (7).—398222, 398328, 398292, 398301, Ammospermophilus harrisii (3).—248454, 270704, 526321. 398304, 398562, 564095. Ammospermophilus leucurus (7).—41396, 54161, 93712, 398261, Spermophilus lateralis (10).—271150, 398243, 398305, 398306, 510859, 531440, 564090. 398307, 398309, 398310, 398311, 501002, 564113. Callosciurus erythraeus (3).—253311, 254584, 255936. Spermophilus major (3).—273183, 273184, 273185. Callosciurus erythraeus bonhotei (4).—253309, 253310, 254808, Spermophilus richardsonii (10).—192877, 552453, 552454, 255368. 552455, 552456, 552457, 552458, 552460, 552461, 552467. Callosciurus finlaysonii (1).—267366. Spermophilus spilosoma (3).—98631, 192770, 497850. Callosciurus notatus (1).—548412. Spermophilus tridecemlineatus (9).—HW5001, HW5002, 47612, Callosciurus prevostii (3).—259034, 396642, 545016. 348373, 398257, 399295, 541440, 564105, 564106. Cynomys gunnisoni (5).—133695, 448236, 448238, 485422, 533015. Spermophilus undulatus (8).—135159, 246459, 247005, 251530, Cynomys ludovicianus (10).—21659, 21660, 23541, 35084, 35086, 251531, 251532, 251533, 397001. 34976, 261275, 266930, 491380, 564088. Spermophilus variegatus (3).—55248, 498437, 501001. Funambulus pennantii (3).—328002, 328003, 395769. Tamias striatus (12).—49823, 261015, 347165, 347967, 348380, Funisciurus isabella (3).—539406, 539407, 539408. 349625, 397128, 397132, 397136, 398269, 505613, 569012. Funisciurus lemniscatus (2).—539410, 539411. Tamiasciurus hudsonicus (12).—397012, 397071, 397090, 397097, Funisciurus pyrropus (2).—539421, 539422. 397145, 397148, 397150, 397153, 397154, 397155, 397163, Heliosciurus rufobrachium (3).—543109, 539427, 539431. 397175.