J Ethol (2001) 19:105–113 © Japan Ethological Society and Springer-Verlag Tokyo 2001

ARTICLE

Andrei V. Tchabovsky · Boris R. Krasnov Irina S. Khokhlova · Georgy I. Shenbrot The effect of vegetation cover on vigilance and foraging tactics in the fat sand rat obesus

Received: January 15, 2001 / Accepted: April 17, 2001

Abstract The combination of the visual obstruction and Introduction protection properties of vegetation is considered to be one of the most important factors determining the trade-off between vigilance and foraging in a prey species. In the Vigilance is one of the main antipredator behaviors of prey Negev desert, diurnal fat sand rats construct their burrows species (Edmunds 1974). Vigilance has often been con- in the ephemeral river beds (“wadis”), under dense and tall sidered as an alternative to foraging and was assumed to shrubs of , or on the open first fluvial depend on perceived predation risk (Lima 1987a; Houston terrace, covered with scattered low shrubs of Anabasis et al. 1993). The vigilance/foraging trade-off has been articulata. We tested the hypothesis that properties of the reported to be affected by a variety of factors, including vegetation would affect the time budget of female sand rats. individual characteristics (age and sex: Reboreda and Sand rats spent more time aboveground, rested more, were Fernandez 1997; reproductive status: MacWhirter 1991; less vigilant, and moved more slowly under the dense cover body condition: Bachman 1993), social factors (Elgar 1989; in the wadi than at the open terrace. No differences in the Yaber and Herrera 1994), and environmental factors (veg- total foraging time were revealed, but foraging tactics etation cover: Sharpe and Van 1998; proximity to cover: varied between habitats: individuals in the wadi mainly fed Diaz and Asensio 1991; foraging substrate: Lima 1992). aboveground, whereas those at the terrace mainly hoarded. Open habitats allow long-distance monitoring of sur- Our results indicate that sand rats perceive the dense veg- roundings and are often, albeit not always, associated with etation cover as good protection despite its visual obstruc- decreased vigilance (Quenette 1990). Ambivalent proper- tive nature, and that vigilance in Psammomys obesus is ties of cover, namely obstructive versus protective (Sharpe performed at the cost of resting rather than at the cost of and Van 1998), are reflected by controversial results of foraging. empiric studies. Vigilance can increase (Diaz and Asensio 1991; Colagross and Cockburn 1993) or decrease (Metcalfe Key words Vigilance · Psammomys obesus · Vegetation 1984; Lima 1987b) with distance to cover. For example, cover · Antipredator behavior · Obstruction/protection vigilance rate decreased with distance to cover in the trade-off white-crowned sparrow Zonotrichia leucophrys (Slotow and Rothstein 1995). Contrastingly, vigilance of the buffy- headed marmoset Callithrix flaviceps was higher under less extensive leaf cover (Ferrari and Ferrari 1990), whereas the Townsend’s ground squirrel Spermophilus townsendii ap- peared to scan more often in vegetation of medium height and less often in low or tall vegetation (Sharpe and Van A.V. Tchabovsky Severtsov Institute of Ecology and Evolution RAS, Moscow, Russia 1998). In the teal Anas crecca, vigilance first decreased with distance to cover, but then began to increase as distance to B. Krasnov (*) · G.I. Shenbrot Ramon Science Center, Jacob Blaustein Institute for Desert cover increased further (Pöysä 1994). In the yellow baboon Research, Ben-Gurion University of the Negev, P.O. Box 194, Mizpe Papio cynocephalus, openness of the habitat proved not to Ramon 80600, Israel affect vigilance (Alberts 1994). ϩ ϩ Tel. 972-8-6586337; Fax 972-8-6586369 The balance between the protective and obstructive e-mail: [email protected] components of vegetation cover mirrors the trade-off be- I.S. Khokhlova tween the probability of being surprised and being detected Wyler Department of Desert Agriculture, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Sede by a predator (Pöysä 1994) and thus may be reflected by its Boqer Campus, Israel effect on antipredator vigilance (Lima 1987b; Lazarus and 106 Symonds 1992; Arenz and Leger 1999). Vegetation cover densely covered with Atriplex halimus shrubs ranging in size may either be beneficial to a prey species, if it prevents a between 2 and 8m in diameter and up to 2m in height. predator from detecting prey, or it may be harmful, if it There were also a few shrubs of Anabasis articulata, merely obstructs the prey’s view and provides little or no Artemesia sieberi, and Salsola spp. in this habitat. The first protection (Arenz and Leger 1999). fluvial terrace bordering the rocky second terrace was cov- The fat sand rat, Psammomys obesus Cretzschmar, 1828, ered with scattered shrubs of Anabasis articulata that were is a diurnal solitary strictly folivorous gerbil, inhabiting 0.5–1.0m in diameter and up to 0.6m in height. In addition, deserts of North Africa and the Middle East. feed there were also a few small shrubs of Atriplex halimus, both above and below the ground. They cut and take leaves Artemisia spp., and Salsola spp. Apparently because of the of the plants to their burrows to be eaten later (Daly and relatively dry winter of 1998–1999 (54mm total precipita- Daly 1975). Daly and Daly (1975) noted that P. obesus tion), the vegetation of both Atriplex halimus and Anabasis construct their burrows only under their food shrubs and articulata was not especially verdant. Ten of 50 randomly avoid open habitats. However, in the Negev desert P. selected A. halimus shrubs and 13 of 50 randomly selected obesus use burrows not only under the shrubs in the wadi A. articulata shrubs had fresh leaves and stems, whereas the bottom but also those on the first fluvial terrace. This habi- others were dry. tat is much less protected than wadi beds and is covered Within the study area diurnal P. obesus is subjected with scattered and low shrubs of chenopods. Large shrubs mainly to diurnal avian predators, whereas all mammalian of Atriplex halimus in the wadi bottom provide good pro- and reptilian predators in the Negev desert are mainly tection from raptors, but simultaneously obstruct lateral nocturnal. vision, thereby preventing early detection of terrestrial predators, especially those using a creeping predatory tac- Burrow description tic. Scattered small shrubs of Anabasis articulata on the terrace, on the one hand, allow long-distance monitoring, In total, 132 burrows of P. obesus were found at the study but also expose gerbils to birds of prey and provide poor site. A burrow was considered to be active (inhabited or physical protection. visited) either if a sand rat was observed or if fresh feces or We studied the behavior of P. obesus in the Negev High- food remnants were found near the opened and clean bur- lands to understand how they allocate their time for vigi- row entrances. Otherwise, the burrow was classified as non- lance and foraging in relation to the degree of vegetation active (vacant). Burrows were classified according to their cover. We predicted, based on the hypothesis about trade- location as “wadi burrows” and “terrace burrows”; 31 off between foraging and vigilance, that the ratio of pro- active burrows (15 “wadi burrows” and 16 “terrace tective versus obstructive characteristics of the foraging burrows”) were described in detail. A plot 10m ϫ 10m substrate would affect time budgets and especially vigilance with a burrow in its center was established for each burrow. and foraging of the fat sand rats; that is, individuals that live In each plot we measured (a) maximal length and width in the densely covered wadi bottom would allocate more of the burrow area based on the farthest entrances, (b) time to foraging and would be less vigilant than individuals number of entrances, (c) number of shrubs by species, and living on the more exposed fluvial terrace. To test this pre- (d) maximum length, width, and height for each shrub. diction, we recorded time that P. obesus living in two micro- habitats with different vegetation cover allocated to various types of activities. Animals

Psammomys obesus were live-trapped using Havahart two- door cage traps (model 1025; Woodstream, Lititz, PA, Materials and methods USA) baited with fresh leaves of Atriplex halimus. Trap- ping was performed under the license 1998/3694 issued by Study area and study site Nature Protection and National Parks Authority of Israel on November 1, 1998. Traps were placed near the entrances The study was carried out on the northern rim of the of the active burrows and were checked continuously during Ramon erosion cirque, Negev Highlands, Israel (30°35Ј N, the day, so that each trapped individual stayed in a trap no 34°45Ј E). The main landscape of the study area is a com- more than 15min. Fat sand rats do not need free water, so plex of hills with a deep loess layer (Յ1m) and wide dry the bait satisfied their water requirements. Trapped animals riverbeds covered with shrubs of Anabasis articulata, were sexed, aged, weighed, and marked individually by fur- Atriplex halimus, Artemisia sieberi, Salsola schweinfurthii, cutting in a symmetrical recognizable pattern. Handling and Noaea mucronata. Data were collected during March time took approximately 7min per individual if it was cap- and April when mean daily temperature ranged between tured for first time. Marked female was handled for 2min to 14° and 29°C. The mean annual rainfall in the area is near check for signs of pregnancy or lactation, whereas a marked 100mm and occurs in winter. male was released immediately. Daily temperature during The study site (800m ϫ 100m) was established along the study period was such that the animals did not need any valley of Wadi Nizzana and included both the bottom of bedding in the traps. We determined the relative age based the wadi and the first fluvial terrace. The wadi bottom was on the size and reproductive status of each . Animals 107 with body mass less than 70g were classified as juveniles; from behind a natural shelter at a distance of 30–40m animals with body mass of 70–120g were considered sub- through 12 ϫ 45 binoculars. We controlled for the detection adults; and animals with body mass of 120–170g were con- of observer by a sand rat and started observations only if sidered subadults if they were sexually immature or adults if an individual showed no response to our occupation of they were in reproductive condition. Animals with body the observation post by interrupting its activity or by alert mass greater than 170g were regarded as adults. Body mass posture. was measured by a Pesola spring balance to Ϯ1g. Focal individuals were observed for 10-min periods and A total of 26 animals was trapped and individually their activity was recorded into a constantly running tape marked; 15 of 26 individuals were adult (10 females and recorder. Total observational time was 890min. Every indi- 5 males) whereas the others were juveniles and subadults vidual was observed on 3–9 different days during the total (7 females and 4 males). No unmarked adult individuals of 17 days of observations. The number of 10-min observa- were recorded within the entire study area during the last tional periods varied between 8 and 24 per animal. 10 days of the field observations whereas about 12 young P. obesus often feed in semiupright posture as do ground animals from known litters remained unmarked. Thus, squirrels (e.g., Spermophilus tridecemlineatus) or great ger- population of the 8-ha study site comprised about 40 sand bils (Rhombomys opimus) to extend their lateral field of rats, and local population density may be estimated as 5 vision to scan surroundings while handling food or chewing individuals per 1ha. Hence, abundance of P. obesus in (Wistrand 1974; Smirin and Orlov 1975; Arenz and Leger spring 1999 seemed to be relatively low (average multi- 2000). To avoid possible misjudgment of an individual’s annual spring abundance of this species in this habitat type state of alertness while foraging, we considered a foraging is estimated to be 14.5 individuals per 1ha; Shenbrot and animal to be vigilant only if it abruptly paused in its activity, Krasnov, unpublished data). including chewing and handling food, and looked either Postweaned pups were observed at the burrows of six around or intently in one direction. In this respect, our adult females. One litter emerged on March 6 and five more criteria refer to those of Yaber and Herera (1994), who litters on March 28 (two litters) and March 31 and on April considered “vigilant behavior” in capybaras Hydrochaeris 4 and 13. Age, sex, reproduction status, group size, and hydrochaeris as “. . . instances in which the animal was ap- social bonds can affect vigilance behavior (see Introduc- parently intently looking around and not simply when it tion). Consequently, to avoid possible confounding effects, raised its head to, for instance, chew a mouthful.” Sand rats we used only the observations of adult females before the spend much time aboveground being motionless (Daly and weanlings’ emergence from the burrow and with no other Daly 1975). To discriminate between alert (vigilant) and individuals active at the burrow. Observations of eight fe- nonalert (resting) stationary postures, we used the positions males met these requirements and were included in the of the animal’s head and eyes following the criteria pro- analyses. Females of P. obesus usually change from one posed by Rose and Fedigan (1995), Hare (1998), Arenz and burrow to another as food supply becomes exhausted (Daly Leger (1999, 2000), and Blumstein et al. (1999). An animal and Daly 1975). During our study period, one of eight in a stationary posture (lying down, sitting, or semiupright) females without pups was subsequently observed in two was considered vigilant if it either was intently staring in different burrows, yielding nine female-burrow units for the one direction with its head elevated above horizontal plane analysis. and its eyes opened or was looking around with frequent Males (five marked individuals) ranged widely and vis- side-to-side head movements. Finally, sand rats were as- ited numerous burrows. Consequently, it was much more sumed to be vigilant when they stood still in the fully erect difficult to locate them than females, and they provided upright extended posture on extended hind feet with considerably fewer observational data. Moreover, they their back straight and mostly perpendicular to the ground were observed often in a social context (e.g., when visiting a (Wistrand 1974). Otherwise, a motionless animal was con- female or encountering another male), and thus another sidered resting. In the latter case, its eyes were often closed confounding variable was introduced. For these reasons, or half opened. General categories of activity and types of data on males were excluded from the analysis. aboveground behaviors are presented in Table 1. Other behaviors (exploratory activity, digging and cleaning the Behavioral observations burrow, marking, collecting nest material, etc.) comprised only a small portion of the total time budget and were not In contrast to the data on crepuscular activity pattern in included in the analyses. sand rats observed in April in the Saharan Desert (Daly and Daly 1975), P. obesus in the study area were active above Data analysis ground throughout the daytime (0730–1730) with a short afternoon break that occurred in the hottest days only. We The total shrub cover of a burrow was estimated as the sum avoid observing sand rats at the very beginning or at the end of the crown areas of all shrubs within a 10-m2 plot around of their activity periods; all observations included in the each burrow. Shrub cover at the height of 0.5m was calcu- analysis were performed between 0800 and 1700. lated as the sum of crown areas of the shrubs taller than We chose a focal animal for observations whenever we 0.5m. Both measurements were used as estimates of the met an active individual on the random inspection routes protection/obstruction conditions of a burrow and were in- performed one to three times a day. We observed sand rats cluded in the analysis as independent variables. 108

Table 1. Description of distinguished categories of activity and types of behavior of Psammomys obesus Category of activity Type of behavior Description

Resting Lying down Self-explanatory; nonalert, eyes half opened or closed Sitting Quadrupedal position, nonalert, head horizontal, eyes half opened or closed Standing semiupright Bipedal position, back curved, nonalert, head horizontal, eyes half opened or closed Vigilant Lying down Self-explanatory; alert, head fixed or frequently moves side to side, eyes opened Sitting Quadrupedal position, alert, head elevated and either fixed or frequently moves side to side, eyes opened Standing semiupright Bipedal position, back curved, alert, head elevated and either fixed or frequently moves side to side, eyes opened Standing upright Bipedal position, hind feet extended, back erect, head elevated and either fixed or frequently moves side to side, eyes opened Moving Climbing Self-explanatory; move on shrub or rock Walking Self-explanatory Running Self-explanatory Foraging (feeding) Immediate consumption Cutting and consuming leaves at feeding site directly from the shrub Delayed consumption Consuming leaves stored beforehand at the burrow entrance Foraging (hoarding) Cutting Cutting leaves and packing them in the mouth Transporting Carrying leaves in the mouth Dropping Dropping leaves near the burrow entrance Storing Disappearing into the burrow with leaves in the mouth Packing Gathering and packing into the mouth leaves previously dropped on the ground

To estimate the proportions of various behaviors in the vigilant behavior within a hoarding context, namely, within time budget, the observational data were treated using the a sequence that begins with cutting and ends with dropping “one-zero” method (Altmann 1974). To avoid strong bias in or storing leaves in the burrow. To estimate hoarding effi- the proportions of behaviors in the total time budget, short ciency, we calculated the proportion of time allocated to 5-s intervals were used for a “one-zero” procedure (Crokett hoarding per se from the total time allocated to a hoarding 1996). After that, the proportions of 5-s intervals when series. For short-term behaviors such as upright postures, particular behaviors occurred were calculated for each 10- we also estimated the performance frequency as the num- min sample. We included in the analysis observations of ber of acts per 10min aboveground. individuals that were active aboveground for at least 5min Neither environmental nor behavioral variables con- during a 10-min focal sample (60 5-s intervals). In total, formed to the assumptions of normality (Kolmogorov– ϭ Ͻ there were 69 such observational samples of eight females Smirnov, Dmax 0.16–0.44, P 0.01) and could not be (from 8 to 12 10-min observational periods per capita) at transformed to normal distribution. Thus, nonparametric nine burrows. statistical analyses were used. The characteristics of the We analyzed time budget in two ways. To characterize burrows were compared using the Kruskal–Wallis the general time budget of P. obesus, we included all 69 ANOVA. The burrow location (“in the wadi bottom” or observational samples in the data set. However, because “on the terrace”) was used as a grouping variable for non- sand rats spent much of their time aboveground motionless, parametric Kruskal–Wallis ANOVA to assess the effect of to characterize the time budget within a foraging context we the burrow location on the proportion of time allocated to selected only those observations when the proportion of different activities treated as dependent variables. The total foraging behavior was no less than 10% of the aboveground shrub cover and shrub cover at the height of 0.5m were activity. There were 23 such observational samples of eight tested for correlation with the proportions of the particular individuals, with two to four observational intervals per activities using the Spearman rank order correlation coeffi- capita. cient. In general, all statistical tests follow Zar (1984). Val- To characterize the general pattern of activity, we calcu- ues are presented as X¯ Ϯ SE. We avoided an inflated type lated the proportion of time spent aboveground of the total I error by performing sequential Bonferroni adjustments time of observations and then the proportions of major of alpha (Rice 1989). Significance is recorded only at this categories of activity of the total time of aboveground activ- adjusted level. ity. To characterize foraging, vigilance, and locomotory activities in a more detailed way, we calculated proportions of a particular behavior of the total time allocated to the Results particular category of activity (e.g., percent of immediate consumption from the total foraging time or percent of Use of burrow “stock” running from the total time spent moving). In addition to these activities, we distinguished “hoarding series.” A Sand rats were seen at least once at 46 of 132 burrows hoarding series includes a hoarding activity per se and a located at the study site. Fresh feces and food remnants 109

Table 2. Structure of P. obesus burrows in two different locations Characteristics The first terrace (n ϭ 16) Wadi bottom (n ϭ 15) Kruskal–Wallis HP

Number of entrances 15.69 Ϯ 1.79 9.87 Ϯ 1.93 5.84 0.01 Overall area (m2) 49.37 Ϯ 6.03 24.87 Ϯ 7.68 10.54 Ͻ0.001 Shrub cover (m2/100-m2 area) 3.61 Ϯ 0.93 25.53 Ϯ 4.46 19.25 Ͻ0.0001 Shrub cover at 0.5-m height 0.86 Ϯ 0.03 17.83 Ϯ 0.04 21.76 Ͻ0.0001 (m2/100-m2 area) Relative cover by Atriplex halimus (%) 13.68 Ϯ 8.51 84.89 Ϯ 4.73 14.30 0.0003 Relative cover by Anabasis articulata (%) 75.54 Ϯ 8.25 7.03 Ϯ 4.26 15.27 0.0001

were found at 3 more burrows, although no animals were observed there. Thus, in total, 49 burrows were used by sand rats to some extent, whereas 63% of available burrows were left vacant. Twenty-four active burrows were used by P. obesus during the minimal interval of 3 days and were classified as occupied. The number of occupied burrows in the wadi bottom was similar to that on the terrace (13 vs. 11, respectively).

Burrow structure

Burrows located on the terrace differed significantly in their structural characteristics from the burrows located in the wadi bottom (Table 2). “Terrace burrows” had more en- trances and occupied greater areas than “wadi burrows.” The total vegetation cover was composed almost entirely of two shrub species. Shrub cover of the terrace burrows was created mainly by Anabasis articulata, which provided sparse low cover, whereas wadi burrows were located under large shrubs of Atriplex halimus that provided dense tall cover. Additionally, sand rats fed on these most available plants. Indeed, leaves and stems of A. halimus and A. articulata comprised 88% and 12%, respectively, of food items observed to be consumed by P. obesus at the wadi burrows and 6% and 80%, respectively, of those at the terrace burrows (in total, 250 food items). All the foregoing observations suggest that the differences in structural char- acteristics of the burrows of different topography mirror the differences both in their protection/obstruction condition and in foraging substrate.

General time budget

Fig. 1A,B. Percentage of time (mean Ϯ SE) allocated by Psammomys Psammomys obesus spent significantly more time above obesus to various types of activity in the wadi bottom (black columns) ground at the wadi burrows than at the terrace burrows and on the first terrace (white columns). A General budget. B Foraging (92% Ϯ 2%, n ϭ 15 vs. 83% Ϯ 2%, N ϭ 54, respectively; context ϭ ϭ Kruskal–Wallis H69 3.9675, P 0.04). For most of this time they were motionless at burrows of both types, resting ϭ or vigilant (Fig. 1A). However, the sand rats moved more events per 10min of activity; Kruskal–Wallis H69 4.9534, ϭ ϭ ϭ (H69 4.4136, P 0.05) and spent much less total time P 0.05) than individuals at the terrace burrows. In addi- ϭ ϭ vigilant (Kruskal–Wallis H69 18.1173, P 0.006) at the tion, P. obesus at the wadi burrows ran much less frequently wadi burrows than at the terrace burrows. Also, individuals than those at the terrace burrows did. Running comprised at the wadi burrows spent significantly less time in upright only 9% Ϯ 6% of the total time allocated to locomotion at Ϯ Ϯ ϭ postures (0.3% 0.1% vs. 9% 2%; Kruskal–Wallis H69 the wadi burrows whereas at the terrace burrows this pro- ϭ Ϯ ϭ ϭ 5.4763, P 0.04) and stood upright and alerted less fre- portion was 37% 7% (Kruskal–Wallis H35 7.4775, P quently (0.22 Ϯ 0.12 posture events vs. 1.89 Ϯ 0.45 posture 0.03). No significant difference in foraging time of P. obesus 110

Table 3. Correlation (Spearman’s R) between the vegetation cover and characteristics of the time budget in P. obesus Time budget characteristics General budget Foraging context

Vegetation cover Total vegetation cover Total vegetation cover at 0.5-m height

Active aboveground 0.24* (69) 0.67* (23) 0.67* (23) Resting 0.41* (69) 0.29ns (23) 0.15ns (23) Vigilant Ϫ0.65* (69) Ϫ0.74* (23) Ϫ0.71* (23) Standing upright Ϫ0.42* (69) Ϫ0.78* (23) Ϫ0.77* (23) Frequency of standing upright Ϫ0.40* (69) Ϫ0.75* (23) Ϫ0.82* (23) Foraging 0.04ns (69) 0.21ns (23) 0.20ns (23) Feeding 0.09ns (69) 0.49* (23) 0.56* (23) Consuming immediately 0.30* (69) 0.54* (23) 0.52* (23) Consuming immediately/foraginga ratio 0.48* (35) 0.55* (23) 0.54* (23) Hoarding 0.07ns (69) Ϫ0.25ns (23) Ϫ0.35ns (23) Storing into the burrow 0.13ns (69) Ϫ0.26ns (23) Ϫ0.38ns (23) Hoarding series 0.06ns (69) Ϫ0.31ns (23) Ϫ0.44* (23) Hoarding efficiency 0.51* (24) 0.67* (23) 0.77* (23) Moving 0.14ns (69) Ϫ0.06ns (23) Ϫ0.05ns (23) Running Ϫ0.18ns (69) Ϫ0.51* (23) Ϫ0.59* (23) Running/moving ratiob Ϫ0.38* (35) Ϫ0.60* (23) Ϫ0.72* (23) Number of observational samples is given in parentheses *P Ͻ 0.05; ns, nonsignificant a Time allocated to immediate consumption from the total foraging time b Time occupied by running from the total time moving

ϭ ϭ between burrows of different topography was revealed Wallis H23 2.9043, P 0.05). In addition, individuals at ϭ ϭ (H69 2.1984, P 0.5). the terrace burrows consumed leaves immediately at the The results of the analysis of correlations between shrub feeding site at a much lower rate than did those at the wadi cover and behavioral patterns support the aforementioned burrows (11.3% Ϯ 5.8% vs. 53.3% Ϯ 14.9% of the total ϭ data (Table 3). Sand rats spent significantly more time foraging time, respectively; Kruskal–Wallis H23 5.2309, aboveground, rested more, and spent less time vigilant as P ϭ 0.04). shrub cover increased. Total foraging time, feeding, hoard- Duration of vigilance of P. obesus at the wadi burrows ing, and locomotory activity proved not to be significantly was extremely low (1.1% Ϯ 0.5% of aboveground activity), correlated with shrub cover. However, P. obesus consumed whereas individuals at the terrace burrows were vigilant food immediately more often and spent less time vigilant 24.4% Ϯ 4.45% of their aboveground time budgets (Fig. 1B; ϭ ϭ during hoarding series, so that “hoarding efficiency” in- Kruskal–Wallis H23 11.2217, P 0.004). Running occu- creased with shrub cover. The portion of time allocated pied as much as 6.1% Ϯ 1.2% of the aboveground activity of to running from total locomotion decreased under dense sand rats on the terrace and only 0.1% Ϯ 0.1% in the wadi ϭ ϭ cover. bottom (Kruskal–Wallis H23 7.7768, P 0.02), so that running comprised 47.7% Ϯ 8.3% of total locomotion on the terrace and only 0.5% Ϯ 0.5% in the wadi bottom ϭ ϭ Foraging context (Kruskal–Wallis H22 8.7480, P 0.02). Correlation analysis supported these results (see Table Unlike the overall budget, neither resting nor locomotory 3). Resting, moving, and total foraging time were not corre- activity of sand rats during foraging differed in relation to lated with shrub cover, whereas animals spent significantly ϭ ϭ burrow location (Kruskal–Wallis H23 1.0045, P 0.8 and more time feeding aboveground and less time hoarding ϭ ϭ Kruskal–Wallis H23 0.0045, P 0.9, respectively, Fig. 1B). (albeit nonsignificantly) as shrub cover increased. They also Similarly, the analysis of time budgets within a foraging demonstrated a strongly significant tendency to delay food context revealed no differences in the total foraging time at consumption (as indicated by the decrease of immediate different burrows (44% Ϯ 9% in the wadi bottom and 34% consumption) when the cover was sparse. P. obesus spent Ϯ ϭ ϭ 4% on the terrace; Kruskal–Wallis H23 0.6429, P 0.8). much less total time being vigilant, stood upright distinctly Nevertheless, there were differences in foraging tactics; in- less frequently, and hoarded more efficiently as shrub cover dividuals at the wadi burrows mainly fed aboveground, increased. Despite the fact that total time spent moving did whereas those at the terrace burrows mainly hoarded (Fig. not vary with shrub cover, sand rats ran significantly more 1B). Feeding time differed significantly at burrows of differ- often at the terrace burrows than at the wadi burrows. ent locations, although the difference in hoarding time was Shrub cover at 0.5-m height appeared to be correlated with ϭ ϭ not significant (Kruskal–Wallis H23 6.9097, P 0.03 and activity patterns of P. obesus in a similar way. Sand rats ϭ ϭ Kruskal–Wallis H23 1.8770, P 0.6, respectively). Ani- spent more time aboveground, were less vigilant, ran less, mals on the terrace stored food in their burrows twice as and allocated more time to feeding whereas total foraging frequently that those at wadi burrows (4.4 Ϯ 0.9 vs. 2.0 Ϯ 0.4 time remained unchanged as the cover of tall shrubs in- storing events per 10min of activity, respectively; Kruskal– creased. Moreover, hoarding rate, which tended to vary 111 inversely with total shrub cover (albeit nonsignificantly), predators. For example, the only predated sand rat at our tended also to be negatively correlated with cover when it study site was killed by a caracal (Felis caracal) despite the was measured at the height of 0.5m (see Table 3). lower perceived vulnerability under large Atriplex halimus shrubs, which, in this case, turned out to be an obstruction rather than a protection. However, caracals are mainly noc- turnally active, so this case was likely an unusual event. Discussion The lack of a pronounced effect of protective conditions on total foraging time is an intriguing result. In our study, Our predictions that individuals inhabiting the wadi bottom vigilance did not incur costs of reduced foraging time in P. would allocate more time to foraging and would be less obesus. This result contrasts with numerous studies that vigilant than individuals living on the terrace appear to be have demonstrated the negative effect of the perceived pre- partly supported. P. obesus showed quite different activity dation risk on foraging behavior due to the trade-off be- patterns in terms of time budget allocation in these two tween foraging and predator avoidance (Kotler 1984, 1992; microhabitats. They spent more time aboveground, were Vasquez 1994, 1997). This discrepancy may result because less vigilant, and ran less at the burrows in the wadi bottom the effect of predation risk on foraging time has often been than at the burrows on the first terrace. Contrary to our analyzed within foraging series consisting of foraging per se expectations, total foraging time was similar in both micro- interrupted by scanning (Pöysä 1994; Burger and Gochfeld habitats, although different foraging tactics may have com- 1992). In such cases, vigilance and foraging were considered pensated. Animals showed a strong tendency to delay food to be mutually exclusive activities that occupied the major consumption on the terrace whereas they did not do so in part of the time budget of animals. However, animals the wadi bottom. should not be regarded as “foraging machines.” Obviously, Apparently, natural vegetation and, sometimes, foraging if analyzed within foraging series only, the increase in vigi- substrate itself combine both protective and obstructive lance would automatically result in decreased foraging time. properties (Lima 1987b, 1992), which is exactly the case for However, such “refined” analysis of short-term series ex- P. obesus. The only way to infer the property of the cover in cised from the general context ignores the overall time bud- the field is to assess its effects on vigilance as an indicator of get, which may provide sufficient spare time to compensate perceived vulnerability. The relatively low level of vigilance time expenditures on vigilance without incurring a cost of of P. obesus at the burrows in the wadi bottom indicates foraging. This spare time would allow an individual to main- that they perceive the dense vegetation cover in this micro- tain total foraging time regardless of the perceived preda- habitat as good protection despite its obvious obstructive tion risk. nature. In addition, sand rats hoard more at the exposed Our analysis of general time budget indicates that vigi- terrace burrows. A similar phenomenon has been reported lance behavior in P. obesus is performed at the cost of for Gerbillurus tytonis, which carried food items to a safe resting rather than at the cost of foraging. Similar results place for consumption as the distance to cover and per- were reported for the yellow-bellied marmot Marmota ceived predation risk increased (Hughes and Ward 1993). flaviventris, which allocated much time to resting, and nei- Decreased vigilance of P. obesus under dense cover can ther foraging time nor vigilance seemed to constrain energy also be explained by the low utility of scanning when the intake (Armitage et al. 1996). Analogously, variation in view is obstructed. Similar behavior has been reported for vigilance in the wedge-capped capuchin Cebus olivaceus different species. For example, the warthog Phacocheroerus also appeared not to depend on time needed for foraging or aithiopicus and the wildebeest Connochaetes taurinus the risk of predation but rather was related to intrinsic scanned more in habitats with fewer visual obstructions individual characteristics (Fragaszy 1990). Another expla- than in habitats with more visual obstructions (Scheel nation can be that animals are vigilant while handling food 1993). Ground squirrels (S. townsendii) spent more time in without incurring the costs of reduced food intake, as was upright postures in low vegetation (Sharpe and Van 1998). shown for ungulates (Illius and Fitzgibbon 1994); this may In our study, P. obesus also stood upright more frequently also be the case for feeding P. obesus. Nevertheless, the at the exposed terrace burrows. extent to which foraging and vigilance really do represent Obstructions may affect vigilance in various ways de- alternatives still remains unclear in many respects. pending on predator type (Lima 1987a). For example, the Finally, sand rats may scan less when the view is ob- buffy-headed marmoset Callitrix flaviceps, which is most structed by dense vegetation cover merely because they vulnerable to aerial raptors, tends to be more vigilant when cannot see predators or other potential danger, unlike the the leaf cover is less extensive (Ferrari and Ferrari 1990). As individuals in open habitats, which respond even to small are other diurnal desert , P. obesus is mainly subject passerines. In other words, individuals in open habitats have to predation by raptors. Consequently, large shrubs can to pay an opportunity cost for monitoring their surround- serve as good protection and may prevent an individual ings via an increased cost of being vigilant, because the from being detected and preyed on from above. Thus, the wide field of view exaggerates perceptional scope, and, obstruction, which simultaneously provides protection, consequently, may increase perceived predation risk. does not result in increased vulnerability. However, this is Contrastingly, an obstructed view reduces perceived preda- not true for terrestrial predators because a large shrub sim- tion risk through reduced perception opportunities. This ply obstructs a ’s view, preventing it from detecting explanation can be rephrased in a famous Russian proverb 112 of the Soviet period: “The less you know, the better you Burger J, Gochfeld M (1992) Effect of group size on vigilance while sleep.” drinking in the coati, Nasua narica, in Costa Rica. Anim Behav 44:1053–1057 High vigilance rate, delayed consumption, and obvious Colagross AML, Cockburn A (1993) Vigilance and grouping in the energetic expenditures of quick running in combination eastern gray kangaroo, Macropus giganteus. 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