Yehudah L. Werner 1

1997 Asiatic Herpetological Research Vol. 7. pp. 153-165

Varied and Fluctuating Foraging Modes in Nocturnal Lizards of the Family Gekkonidae

1 - 2 3 4 Yehudah L. Werner Shigeru Hidetoshi Okada , Ota , Gad Perry and Shoji TOKUNAGA5

Department ofEvolution, Systematics and Ecology, The Alexander Silberman Institute of Life Sciences, The Hebrew University ofJerusalem. 91904 Jerusalem, Israel; Kagoshima Environmental Research & Services, 2-7

Masago-cho, Kagoshima-shi, Kagoshima 890, Japan; Tropical Biosphere Research Center and Department of

Biology. University of the Ryukyus, Nishihara, Okinawa 903-01 .Japan; Department ofZoology, University of

Texas, Austin, TX 78712-1064. USA; Department ofPublic Health. School of Medicine, Kyushu University, 3-1- 1 Maidashi, Higashi-ku, Fukuoka SI 2. Japan

Abstract. -Heliothermic lizards have been used as model organisms in studies of foraging mode, although their behavior is generally complicated by thermoregulation. Tropical nocturnal gekkonid lizards could be better models than temperate diurnal lizards. In several recent reviews, gekkonids have been considered to be sit-and- wait (ambush) predators. Observation of Gekko hokouensis, G. japonicus and Teratoscincus roborowskii in the field on warm nights revealed that by the measure of moves-per-minute they are sit-and-wait (SW) predators but by the measure of percent-time-moving G. hokouensis is widely-foraging (WF), as is Coleonyx variegatus, according to the literature. The behavior of individuals of all three species combines to varying extent both SW and WF modes. This observation accords with recent reports of foraging behavior in G. gecko and Stenodactvlus doriae. Reexamination of the original literature sources quoted in recent reviews showed that these sources had already qualitatively described many geckos as either WF or mixed strategists. The fluctuating foraging mode of geckos presumably enables these noctural visual predators to locate stationary prey and. without wasting locomotor energy, to locate mobile prey. The option to employ both SW and WF modes may depend on the absence of competition. Although geckos as a group had been believed to be SW predators, their relative clutch mass (RCM) had often been believed to be as small as in WF lizards. More recently, several geckos were shown to have larger RCMs. Hence geckos, rather than having a paradoxically low RCM. are in fact intermediate between SW and WF lizard groups in both RCM and foraging mode.

Key words: Reptilia, Lacertilia, Gekkonidae, Gekko hokouensis, Gekko japonicus, Teratoscincus roborowskii, China, Japan, foraging mode, nocturnality. relative clutch mass.

Introduction assumptions that there is little intraspecific or intra individual variation in foraging behavior. Ever since they were first coined by Pianka (1966). Lizards have been used often as models for study- the terms "sit-and-wait" (SW) and "widely foraging" ing the foraging behavior of animals in the field. The (WF) have been used extensively to describe foraging two commonest coins for and behavior. Often they have been considered alternative quantification comparison have been the time PTM) and states of a dichotomy (Pianka. 1986; McLaughlin. "percent moving"! "movements minute" (MPM, see below) 1989; Etheridge and Wit. 1993; and references in per (Huey and Pianka, 1981; et al., Pietruszka, 1986). while some authors have viewed Perry 1990). them as extremes of a continuum (Pianka. 1974:203; Going by such yardsticks, the foraging mode, Pietruszka, 1986; Perry et al., 1990). Although Vitt either SW or WF. is usually considered typical of a and Congdon (1978) and Vitt (1990) recognized the whole lizard family. Thus, Agamidae, Anguidae and possibility of a continuum of foraging modes, their lguanidae (s.L), unless herbivorous, are SW foragers, papers highlight differences between SW and WF liz- whereas almost all Lacertidae, Scincidae, Teiidae and ards. Implicit in the use of these terms (or the equiva- Varanidae are WF (Huey and Pianka. 1981; Dunham lent "ambush" and "active" foragers) are the et al.. 1988; Green and King, 1993; Cooper. 1994a, b). Vol. 7, p. 154 Asiatic Herpetological Research 1997

The studies underlying this classification obvi- ments per minute", the average number of times, ously presuppose that the observations quantified had during one minute, that a lizard changed its locomo- been free of socially-motivated (Regal, 1983:1 16) and tory state from "stationary" to "moving"; PTM, "per- of thennoregulation-related (Anderson, 1993) behav- cent time moving" percentage of the total time, that ior. Whereas it is relatively easy to account for the the animal spent locomoting; percra. percents of ra; former (Kingsbury, 1989), it is often difficult to com- ra. rostrum-anus ("snout- vent") length (Werner, pletely exclude the latter when observing diurnal 1971); RCM. relative clutch mass, ratio of total clutch poikilotherms such as lizards. Nocturnal lizards such mass to total maternal mass, including the clutch (Vitt as geckos can thus provide superior models of forag- and Price, 1982); SD, standard deviation; SW, "sit- ing mode if observed in a climate with stable night and-wait" predator; WF, "widely ranging forager". temperatures approximating those preferred by the lizards. Data Collection

Environmental factors such as illumination can affect The Gekkonidae have traditionally been consid- the of nocturnal 1979: ered SW predators (Pianka. 1986:48; Dunham et al.. activity geckos (Frankenberg. and Bouskila et 1988:513), and this view appears somewhat supported Frankenberg Werner, 1979; al., 1992; Petren et al., 1993). We therefore detail the circum- by recent observations on Gekko gecko (Stanner et al.. stances of the observations. in press). However, Coleonyx variegatus employs an intermediate stragtegy (Kingsbury. 1989) and some Observations were made at night by one observer others have recently been counted as active foragers carrying an electric torch with a removable cover of

Thus it remains unclear whether (Cooper, 1994a,b). red cellophane paper (two layers). When the torch was the Gekkonidae are characterized by a given foraging held on the observer's forehead, Teratoscincus could as are other lizard families, if what that mode, and. so, be located on the ground by their reflecting reddish mode is. foraging eyeshine. With both Gekko species, which were observed on walls, this method was This issue is of particular interest because whereas mainly superflu- ous. at a distance for Tera- SW lizards usually have greater relative clutch masses Searching began (>20 m less for the Gekko with white (RCMs) than WF lizards (Vitt and Congdon, 1978). toscincus; species) light. The main observations from geckos tend to have RCMs similar to those of WF were made 3-10 m, on and situation, with red We Lizards (Vitt and Price, 1982: figs. 1 and 3). This depending species light. endeavoured to observe each individual for 30 min- putative paradox cannot be explained fully as an adap- the was and examined. tation of geckos to life in crevices (Vitt, 1981): small utes; finally gecko approached In all three some of the locomotion of the RCMs occur also in cursorial, arenicolous species of species, individuals was towards the hence geckos (Vitt and Price, 1982: Werner, 1989): in some observer, presum- the observer did not affect them of these this could be a phylogenetic constraint (Vitt. ably (following 1986: Stearns, 1992) but presumably at least in the Anderson. 1993). primitive group of Eublepharinae (Kluge. 1967: To enable prompt photography, the observer car- Werner. 1972) this would not be the case. Hence addi- ried a ready camera (Leica M3 with 135 mm lens) tional data on the foraging modes of geckos are with flash and mostly Agfachrome Professional 200 needed. ASA film. Air temperature was recorded with a Miller- Weber thermometer Therefore, we report here on the foraging behavior mercury ("Schultheis"

1 above also 1 of three nocturnal geckos in the eastern Asian sum- type) m ground (for Teratoscincus cm above and substrate was also mer, Gekko hokouensis, G.japonicus, and Teratoscin- ground, temperature taken). Illumination was recorded with a Lunasix-3 cus roborowskii . We pay particular attention to meter. intraspecific variation, which has been reported in the (Gossen) light foraging behavior of some other lizards (Pianka et al„ Observations and environmental data were 1979; Kingsbury. 1989: Perry. 1996). and to intra- recorded into a microcassette recorder (Panasonic individual variation, a topic which has not been RN-102). When the information was transcribed on addressed previously. paper, detailed time data were derived from a clock synchronized with recorded times. Because the speeds Materials and Methods of recording and playback varied with battery strength, care was taken to use equivalent batteries. Abbreviations and Definitions

CV, coefficient of variation (standard deviation as percent of mean); FM. foraging mode: MPM, "move- 1997 Asiatic Herpetological Research Vol. 7, p. 155

32.7). We followed this methodology for approx. half the data of Gekko hokouensis, which included appro- priate time statements.

In the remainder of G. hokouensis data, the obser-

vations had been grouped per half-minute periods, leaving precise durations unknown. These records were scanned automatically by the NOTITA computer program (N. Werner & H. Dreher, in MS) which con- structed a quantitative table, from which some sum- marising statistics were derived by the Microsoft Excel program.

We do not use velocity as a descriptor of FM Figure 1 . Study site for Gekko hokouensis at the and Pianka. 1981; et al., 1985; Chinen Castle ruins, near Chinen, Okinawa Island, (Huey Magnusson Anderson. 1993) because is Japan (4 August 1992). velocity generally affected by body size (Avery et al., 1987b).

Species, Environments and Observations Data Processing and Presentation Gekko hokouensis 1928. Gekko hokouensis Geographical grid references of towns, for macro- Pope, males attain 59.8 mm ra (mean53.9) and females 65.4 ecological evaluation, are from the Times Atlas of the ra on World (1967). mm (mean 54.8) Okinawa Island (Ota. unpublished data). Observations suspected of reflecting social inter- actions or observer effect were excluded. The proxim- Study site. G. hokouensis was studied at the Chinen Castle ruins near 127° south- ity of an observer may suppress the activity of lizards Chinen (26° 07'N. 49'E), (Sugerman and Hacker, 1980) or stimulate excessive ern Okinawa Island. Japan (. 1). Most observations activity (Regal. 1983). were made on geckos on and in a small modem but uninhabited concrete-block building among large To enable comparison with previous data (Huey trees (fig. 1); few observations were made on geckos and Pianka. 1981: Perry et al, 1990). we use MPM on the trees. None of the other occur- and PTM to assess FM. These depend on the defini- gecko species ring on Okinawa (Ota. 1989) was encountered in the tion of discrete locomotor states, although the activity study site. of the animals may constitute a continuum of patterns 1983:1 all (Regal. 15). We coarsely classified postures Procedure and conditions. On five nights between and actions as "stationary" or "moving". "Stationary" 28 July and 4 August 1992, observations started included the time during which the gecko remained in between 1850 h (at which time the illumination was the same place, perhaps moving its head, jaws, down to 700 lux) and 2015 h (sunset was approx. at tongue, limbs or tail, or even shifting its posture by 1915 h), and lasted as long as geckos were active on as as it did not towards another 180°, long move loca- the building. Throughout the observations, the sky tion. "Moving" included crawling, walking, running, was mostly at least half overcast, hiding the moon and forwards. jumping jerking which was waxing, in its first quarter. Air temperature

A complication arose from frequent brief pauses varied only between 26.0 and 28.1° C. On the first during locomotion in Gekko hokouensis. We found a night, observations were made by a team of two; on precedent in Avery et al. (1987a, b), who analyzed the the later nights, the two observers functioned as sepa- locomotion of four lacertid species by videotape. rate teams. Observations were made from distances of "Standard" locomotion (neither fleeing nor chasing), 3-5 m, so that behaviour was seen in detail. Observa- presumably representing foraging behavior, com- tion time totalled 27.25 team-hours. prised 88-143 bursts of movement per minute, each of Observations. Of 63 geckos recorded, only 12 could 0.25-0.56 sec. The intervening pauses lasted 0.12- be followed for >30 min. These showed varied move- 0. 1 7 sec. and occupied 18-40% of the time. In the FM ment patterns. of female Podarcis sicula in nature, Avery (1991) Bouts which the were defined as 'movement' a bout of locomotion separated during geckos stationary, lasted from <1 min to > 15 min. While from others by pauses of >1 second. Thus defined, stationary, geckos often turned their head (to one side or another, or movement duration in P. sicula averaged 10.9 sec; back to the to twice minute). pause duration averaged 22.4 sec (MPM= 1.8; PTM= straight position, up per Vol. 7. p. 156 Asiatic Herpetological Research 1997

Table 1 . Measures of foraging mode in the geckos studied. Species means are based on samples described or quoted in the text.

Species Minutes observed Moves/minute % of time moving X SD X SD X SD

(Range) (Range) (Range)

Gekko hokouensis n=12 37.8 7.15 0.35 0.15 25.5 14.7

(30.5-53.5) (0.18-0.65) (5.1-51.5)

G . japonicus n=12 25.44 12.32 0.15 0.2 8.94 9.7

(4-43) (0.00-0.75) (0.0-50.0)

Teratoscincus roborowskii 11.97 8.81 0.44 0.8 8.83 14.8

(1.5-36.03) (0.00-2 82 1 (0.0-50.0)

Duration (seconds) of a single-

Stationary pause Move

Gekko hokouensis n=12 150.2 74.1 50.2 29.9

(5-1050) (1-375)

G. japonicus n=12 856.6 818.7 34.7 38.6

(2-2580) (1-150)

Teratoscincus roborowskii n=\ 385.0 296.3 13.2 23.0

(1-1800) (1-150)

turned the whole body to another direction (up to once minute. Following Avery et al. (1987a, b; see Materi- per four minutes), or waved or vibrated the tail (up to als and Methods) we classify each sequence of loco- its brief once in seven minutes). Licking the lips could occur motion by "micromoves". including pauses, at any time (usually up to once per minute). as one bout of moving, or "move". But "micromoves" could also occur singly or widely spaced, and then Gecko movements between stationary bouts took were reckoned three major forms: (a) Normal walking or running, separately. usually for a distance of 5-100 cm at a time. On the basis of these definitions of "moves", their

statistics are summarized in Table 1 . (b) Crawling: the geckos sometimes advanced, with or without pauses, by a slow "crawl", at a speed The sex of twelve females was verified by capture

of about 1 cm/min. We saw no evidence that this was or was evident due to obvious gravidity but the sex of consistently related to the gecko having detected a only four males was ascertained by capture. Males prey item. appeared to be a little more active than females but the difference was not statistically significant (MPM: (c) Interrupted locomotion: a sequence of forward males, X=0.46; females, X=0.32; t-test movements by 1-2 cm each ("micromoves"). at a rate p=0.06). of usually 2-12 (rarely up to 72) "micromoves" per 1997 Asiatic Herpetological Research Vol. 7, p. 157

Gekkojaponicus (Dumeril ef Bibron, 1836). Gekko Teratoscincus roborowskii Bedriaga, 1905 65 ra 60 and japonicus males reach mm (mode mm), Teratoscincus roborowskii was synonymized by females reach 70 mm ra (mode 61 mm) (Tokunaga with T. but is in the Pope ( 1935:458) scincus process L984:fig.l). of being validated by J. R. Macey et al. (see Autumn and Han. 1989). The is arenicolous and its Stuclv site. G. japonicus was studied on the Hakozaki species toes lack adhesive males up to 87 mm ra, campus of Kyushu University. Fukuoka (33° 39'N. pads; females to 80 mm ra (from 30 adults in the Califor- 130° 21'E). Kyushu Island. Japan, where the investi- up been conducted. The nia Academy of Sciences, courtesy J. Vindum). gations of Tokunaga ( 1984) had were on various and sheds, geckos buildings espe- Study site. T. roborowskii was studied near Turpan of walls or lit cially in portions passage ceilings by (42°55'N, 89°06'E), Xinjiang Uygur Autonomous incasndescent or fluorescent or street lamps by nearby Region, People's Republic of China (on the Turpan- G. is the in this lamps. japonicus only gecko species Jiaohe road, approx. 4.5 km W of the Turpan SixMin- site and Ueno. 1963; study (Nakamura Tokunaga, arets Mosque; 3 km E of Jiaohe Ancient City). 1984). and no other reptiles were encountered during Located on the margin of the Turpan Depression (- the observations. 150 m), this area has a total annual precipitation aver- Procedure and conditions. During three nights, 9- age of 16.6 mm (Turpan Weather Bureau data). The

1 started in 1 August 1992, observations by one observer daily maximum air temperature ranged up to 45°C between 1915 h, when the illumination was 44 lux. September 1987 (Autumn & Wang, 1988) but aver- and 2030 h (sunset, approx. 1910 h; end of twilight. aged only 40°C during the study period. 2040 h), but had to be ended for rea- approx. logistic The study site comprised long-abandoned fields of sons 2300 h. while were still active. by geckos blackish sand at the foot of hills with undisturbed veg- the observations the was overcast; Throughout sky etation described by Autumn & Wang (1988). The sometimes a drizzle rained. The mostly-hidden slight sand was soft in some places, hard packed in others, in its second intensi- moon was waxing quarter. Light and retained remnants of furrows, ditches and wells. ties where most were observed ranged from geckos Plant coverage comprised only two small shrub spe- 0.35 to 1000 lux. Some were in the lit areas geckos cies and by estimate varied between patches from 2% and others in shaded situations. At the times - nearby to 80%. Rainfall had exceeded the average during the daily observations were conducted, air tempera- the first half of the year ( 1.1.-9.VII.92), 21.8 mm had tures from 27.2°C down to 24.5°C. These ranged already acummulated (Turpan Weather Bureau data). three followed two rainy nights, when the nights very In addition to the trees lining the road, some small site had been on the margin of a typhoon. The geckos stands of small Tamarix sp. trees occurred in the area. were observed from distances of 5-8 m, so that fine Other than the Teratoscincus encountered at night, details were missed. Observation time totalled 7.5 h. the only reptiles seen on the site were the diurnal liz- Observations. Of 20 geckos recorded, only 7 could ards Phrynocephalus axillaris (Agamidae) and Ere- be followed for >25 min; the 12 observed for >4 min mias velox (Lacertidae). Some individuals of both behaved three remained variably: stationary through- species, especially of Eremias, were still active in the to whereas others alternated out (up 43 min) moving last daylight after sunset. According to Autumn & and pausing, usually moving less frequently than once Wang (1988) Psammophis lineolatus (Colubridae) every ten minutes, and spending up to 10% of their may also occur on the site. These authors pointed out time in but one of the time locomotion; spent 50% the simplicity-in-principle of flora and herpetofauna

1 to be intra- moving (Table ). There appeared some on the site and in Chinese deserts in general. individual variation; for example gecko no. 13 was Procedure and conditions. On four nights, 6-10 once stationary for 15 min. whereas its other 7 station- July 1992, observations (by one observer) started at ary bouts all lasted <4 min. 2125-2200 h (Beijing time: sunset. 2135 h), i.e., The individuals were not sexed because most were before the geckos emerged for their nocturnal activity on walls. high on the surface: but had to be ended for administrative

at 0001-0030 h. while the were still Comment. The geckos may have been less active reasons geckos active. moon was about full the than usual during these observations due to the rainy The 1/2 (waxing), sky weather and the cool season - in summer 1992 the mostly 4/8 cloudy; when gecko activity was high, the

illumination was of the order of of 1 lux. mean daily temperatures were 2-3°C below the 30- magnitude

little between sand surface, air 1 year average (Fukuoka Meteorological Observatory Temperature differed

1 the over- records). cm above ground and air m above ground; Asiatic Research 1997 Vol. 7. p. 158 Herpetological

Individuals were not sexed because this species autotomizes the skin when held, as described for Ter- atoscincus scincus by Bauer et al. (1993).

Comment. Thus these geckos are not simply "active foragers" as has been described for Teratoscincus przewalskii (Semenov and Borkin, 1992).

Discussion

Figure 2. Teratoscincus roborowskii. half-grown indi- The Foraging Mode of Gekkonid Species vidual, scouting from the entrance of its burrow (Tur- and to be the extremes of pan, 2235 h, 8 July 1992). For lizards. SW WF appear are a FM continuum: ( 1 ) Both SW and WF practiced

differently by different lizard species, which combine The all range during observations was 26.5-34.4°C. different MPM and PTM values; (2) Some lizard spe- absent to for short wind varied from fairly strong cies vary their FM during the day or during the year times, commonly blew from the north, and sometimes (Pietruszka. 1986); (3) the intermediate FM, repeat- warm. In the darkness, at distances of for was noticeably edly shifting the position for stationary scanning 10 behavior was assessed mostly approx. m, gecko prey, called "cruising" by Regal (1983:113-114). or, their returned Observation time et al. from eyeshine. more aptly, "saltatory" by O'Brien (1989), totalled lOh 20' but as the torch became effective only occurs also in lizards (Moremond. 1979). Neverthe- observation time at approx. 2210 h, the effective less, SW and WF are definite foraging techniques: 8h 20'. approximated only Sceloporus merriami and Urosaurus ornatus switched from distinct WF to distinct SW Observations. On each night, the earliest gecko was (Iguanidae) 19S3). Indeed, a search of 10-60 when food was scarce (Dunham. gen- spotted 40-65 min after sunset, after SW is the optimal strategy for motile prey, and min. Thereafter, the finding of each successive indi- erally WF the optimal strategy for stationary prey (Gerritsen vidual usually required 0.5-5 min. and Strickler. 1977). One individual, caught at 231 Oh on 9.VII.92 with In lacertid lizards the two FM measures. MPM sand temperature 30.5°C and air temperature (1 cm) and PTM, yield the same verdict as to whether 31.3°C, had a rectal temperature of 30.2°C. usually < 1-2 and a species is SW or WF, i.e.. MPM values of Time budgets were calculated for the 1 1 animals PTM values of <15 indicate SW; MPM of > 1.5-2 and observed (despite the vegetation) for > 90 sec and not PTM of >30 indicate WF (Huey and Pianka. 1981; suspected of having been affected by the observer Perry et al.. 1990). By either index the species aver- (Table 1 ). Of 28 individuals discovered at a distance, ages of Gekko japonicus and of Teratoscincus three were when This value of only moving spotted. are roborowski (Table 1 ) indicate that these geckos 10.7% of the animals moving when discovered is SW foragers. The observations of Stanner et al. (in close to the 8.8 PTM calculated for the (Table species with the press) of Gekko gecko also are compatible 1). suggestion of this species being a SW predator (0.04 behavior was variable Individual foraging highly MPM. 4.37 PTM). However, the third species studied to be dominant: but two extreme patterns appeared here, Gekko hokouensis, is SW only in its MPM several animals remained an stationary throughout mean, and is WF, or nearly so. in its PTM. The situa- observation of 10-15 min; others alternat- period kept tion in Coleonyx variegatus is very similar, with 0.57 and at intervals of 1-7 ing between standing walking MPM but 34 PTM (Kingsbury, 1989). sec (rarely <1 or >60 sec). Thus by the index of MPM. all five gecko species Two individuals individual (a half-grown spotted for which at least some quantitative data exist, are SW

on 8. VII at 223 1 h and a subadult on 9. VII at spotted predators. But the index of PTM is probably ecologi- out of 2327 h) were with their fore-parts it reflects sitting only cally more significant, because partly the of their burrows One retained openings (fig. 2). energy investment in foraging, and by this index three this for 36 min. then ran out and (the the position away species are SW, whereas two are WF. Moreover, other was disturbed the observer after 14 min, and by diet of Ptyodactylus guttatus indicates that this spe- retreated down its hole). When out from the looking cies forages more widely than previously believed burrow, these have been SW scouting like Borkin geckos may (Perry and Brandeis. 1992). and Semenov and 1981 Ptenopus (Huey and Pianka, ). (1992) have stated that Teratoscincus przewalskii is a 1997 Vol. 7. p. 160 Asiatic Herpetological Research 1997

Recently Arnold ( 1993) listed the forgaing modes tage point in the dark, and during 280 min of observa- of seven gecko taxa: he considered four species of tion moved only 8 times, within only 40 cm (0.03 Pristurus and Quedenfeldtia trachyblepharus passive MPM. 2.5 PTM). In the second night it stationed itself feeders, P. celerrimus a cruising forager, and at an illuminated window and was more active: during active Gonatodes foragers, although he provided no 640 min it moved 29 times (10 of these, eating); by quantitative data by either of the two indices men- these movements, which totalled 40 min. it loeomoted tioned above. Hence by the criteria developed for nearly 50 meters (0.05 MPM. 6.25 PTM). (3) Prelimi- other lizards (especially Lacertidae), of the seventeen nary observations of Hemidactylus turcicus (Perry, gekkonoid species whose FMs have been quantified unpublished) also show great variability in FM. or described, only eight are strict SW predators: nine No similar variability has been reported by Kings- tend in varying degree to WF strategies. This agrees in bury (1989) from Coleonyx variegatus, so currently

with the recent of ( 1994a. b) principle survey Cooper the combination of SW and WF behaviors is known who counted 52 as SW and 8 as WF or species having only from gekkonine geckos. mixed strategies. This heterogeneity resembles that reported in Lac- erta laevis in which The Structure and Sources of the Variable FM (Lacertidae). during observation of Geckos periods of five minutes, most individuals were either completely stationary or rather active (Perry et al., Previous studies of lizard FM have found intraspecific 1990). variation, which varied in extent even among the spe- Unless random, such heterogeneity could result cies within a family in one region. Among Lacertidae from three factors, which are not exclusive. in the Kalahari, the CV of MPM ranged from 10.0% mutually (1) FM change with age: in two of Ich- in Ichnotropis squamulosa to 105.8% in Eremias line- may species notropis (Lacertidae). as well as in Yaranus komo- oocellata and that of PTM ranged from 10.4% in the are WF whereas the adults Nucras tessellata to 81.1% in Eremias lineoocellata doensis, juveniles partly adopt SW behavior (Broadley, 1979; Auffen- (Table 2; Huey and Pianka. 1981 ). In the gecko Cole- berg, 1981). But all the data discussed above were onyx variegatus, males in an enclosure moved a derived from adults and subadults. greater distance per hour ( 1 7.6 m/hr) than did females (9.4 m/hr), although MPM were equal (0.57) (Kings- (2) There are precedents for a sexual difference in bury, 1989). In Anolis polylepis, Perry (1996) found the FM of lizards of other families, usually with males significant differences in foraging behavior between more active than females, by one measure or another males, females and juveniles. But we are unaware of (Pietruszka. 1986; Anderson. 1993; Perry, 1996). In any attention given to intraindividual variation in FM. Coleonyx variegatus, Kingsbury (1989) found that, although males and females moved equally fre- The three species reported here share great behav- quently, males moved longer distances each time. ioral variability, as shown also (in two of them) by the This confirmed the earlier observation by Cooper et high CVs of MPM and of PTM (Table 2). In each spe- al.( 1985). that males were more active (exposed) than cies, some individuals appeared to be very stationary, females. sometimes throughout the whole observation time

1 reverse sexual difference occurs in (Table ). Other individuals were so active that they A Phrynoceph- could not be observed throughout the intended period. alus mystaceus (Agamidae): males scout SW while Single consecutive movement (or bouts of rapid alter- perched in presumably territory-guarding situations, nations of standing and moving) lasted several min- whereas females are WF (Polynova and Lobachev,

at 1 and utes the most (Table ) but the maximum PTM quoted by Ananjeva Tsellarius, 1986). Perry observed in individuals approximated 50% in two of ( 1996) found a similarly reversed sexual difference in the species (Table 1 ). Anolis polylepis.

Similar variability occurs in three other geckos for Of the geckos reported here. Gekko hokouensis males have been a little active than females. which some data are available. ( 1 ) The arenicolous may more

Stenodactylus doriae in the Arava Valley, Israel: dur- As explained above. G. japonicus and Teratoscincus ing 30 min observation periods, some individuals rohorowskii individuals were not sexed. In Lacerta remain stationary throughout, whereas others move laevis it is likewise unknown whether the different about actively (Werner, pers. obs.; Bogin, 1993). (2) behavior patterns were related to sex (Perry et al.. The adult Gekko gecko individual briefly observed by 1990). Stanner et al. near also behaved (in press) Bangkok (3) Species averages of MPM and PTM always In the first it itself on a van- variably: night perched mask intraspecific variation. With the usual short 1997 Asiatic Herpetological Research Vol. 7. p. 161

observation bouts per individual, it remains unknown prey while reducing the costs associated with locomo- whether the variation is inter- or intra-individual. The tion (e.g.. energy expenditure and detection by preda- longer observation bouts applied here, revealed indi- tors). This would parallel the behavior of other viduals that switched from stationary to active behav- animals which vary their foraging tactics at times of ior or vice versa. Because of the variations in the style food shortage or increased food requirements (Curio, and speed of the active behaviour, it seems that the 1976:20.27). were then and not to new animals foraging shifting The employment of both SW and WF modes by i.e.. this was not SW stations; saltatory foraging these geckos may be related to lack of competition: (O'Brien et 1989). But the brief al., conceivably The segregation of diurnal lizards in a community into WF in G. hokouensis, and also in the pauses during SW and WF species presumably aids in resource par- Lacerta et al.. 1987a. b; 1991). spp. (Avery Avery. titioning (Pianka et al., 1979:87-88; Huey and Pianka, indeed serve for as "snapshot scanning" suggested by 1981:995). This dimension of resource partitioning

O'brien et al. ( so that in these the WF 1989), species comes in addition to the many reviewed by Schoener are actually saltatory foraging. As the data periods ( 1974). The species reported here, Gekko hokouensis, now stand, the three here, as well as species reported G. japonicus and Teratoscincus roborowskii, were G. and S. doriae, seem to gecko methodically practice each the sole nocturnal lizard species observed in the a SW and WF bouts. fluctuating FM alternating area. Where G. gecko was observed (Stanner et al., in press) it was associated only with Hemidactylus Function of the Fluctuating FM in Geckos frenatus, two orders of magnitude smaller (>l()0g and and Pianka summarized theoretical Huey (1981) pre- <10g, respectively). Where Stenodactylus doriae was observations to the effect that an increase dictions and observed (Bogin. 1933) the area carrying its dense in should result in an increase in for- food availability population (Bouskila. 1987) contains very few indi- in as well as More- aging velocity, SW WF species. viduals of other cursorial geckos. It would be instruc- that over, Dunham (1983) found Sceloporus merriami tive to observe FM where a number of gecko species and Urosaurus ornatus switched from a WF to a SW forage together. The comparison should be made foraging tactic during periods of low resource abun- within the Gekkonidae so as to minimize the confu- dance. sion of ecological and phylogenetic factors (Dunham and and Bennett. If this principle were applicable to the fluctuating Miles, 1985; Huey 1986). FM of geckos, a reversed "giving-up time" principle FM and Relative Clutch Mass (Green, 1987) would be indicated: a gecko forages actively, till the lack of prey causes it to switch to the It has been stated that geckos, believed to be SW energetically cheaper SW strategy. When its patience predators, have small RCM, compared to SW lizards is rewarded with prey, it "can afford to try its luck" of other families (Vitt and Price. 1982; Vitt. 1986). and resumes the WF strategy. However, on the one hand. Werner ( 1989) has already out that the RCM of geckos is actually some- We suggest that some geckos fluctuate between pointed what larger than generally believed, being intermedi- the two FMs irrespective of momentary success. Gec- ate between those typical of WF and SW lizards. On kos are visual hunters despite the poor light in which the other hand, we have shown here that the FM of most operate. They seem to cope with this handicap is not as SW as stated but 1 if if geckos strictly generally by ( ) having larger eyes nocturnal and also (2) contains WF to varying extent. Hence foraging cursorially. without scouting from vantage components rather than having a paradoxically low RCM. points (Werner, 1969): (3) by foraging in erect, geckos, are in fact intermediate between SW and WF lizard stretch-limbed, posture (if cursorial), the better to in both their FM and RCM. view their surroundings (Werner and Broza. 1969); groups

1 that and (4) by being more active, WF. in the better-illumi- Werner and Frankenberg ( 989 ) have shown nated times of night (at least in some species) (Fran- among lizard species, the correlation of the RCM to kenberg and Werner. 1979: Bouskila et al.. 1992). The the relative body size of the female (female ra as per- last phenomenon seems to parallel the observation of cent of male ra). depends on the FM of the species: m Dunham (1983) quoted above: when food is more SW predators (Agamidae. Chamaeleonidae. apparent, foraging becomes more active. Iguanidae), the larger the female is compared to the male, the the RCM. But in WF species (Lac- We hypothesize that (5) by alternatingly employ- greater ertidae. Scincidae), the larger the female (relative to ing SW and WF strategies, some geckos, foraging the male), the smaller the RCM. the when the range of vision is short, increase their proba- Interestingly, tends to be as bilitv of encountering stationary as well as mobile relationship among gekkonidae among Asiatic Research 1997 Vol. 7, p. 162 Herpetological

lian and later Dr. Jim Univer- WF species (Werner, 1996). Moreover, Vitt (1990) has Museum, by Saunders, pointed out that among sympatric caatinga lizards, sity of Pennsylvania, Philadelphia. geckos differ from typical SW species in possessing continual rather than seasonal reproduction. The last Literature Cited two observations seem to further support the notion Ananjeva, N. B. and A. Y. Tsellarius. 1986. On the that geckos should not be considered strict SW preda- factors determining desert lizards' diet. Pp. 445-448. tors. In E. Rocek (ed.). Studies in Herpetology (Proc. Charles Conclusions Europ. Herp. Meeting, Prague). University, Prague. statistical measure of used for lac- By the MPM (as Anderson, R. A. 1993. An analysis of foraging in the the Gekko ertids). geckos Coleonyx variegatus, gecko, lizard, Cnemidophorus tigris. Pp. 83-116. In J. W. G. and Teratoscincus G. hokouensis, japonicus Wright and L. J. Vitt (eds.). Biology of Whiptail Liz- roborowskii are SW predators. ards (Genus Cnemidophorus). Oklahoma Museum of Gekko gecko, G. japonicus and Teratoscincus Natural History, Norman, Oklahoma. roborowskii are SW predators also by the statistical Arnold, E. N. 1993. Historical changes in the ecology but this measure of PTM (as used for lacertids); by and behaviour of semaphore geckos (Pristurus, hokouensis are measure Coleonyx variegatus and G. Gekkonidae) and their relatives. Journal of Zoology, WF. Most other gekkonine species, whose foraging London 229:353-384. has been verbally described in literature, also appear Auffenberg, W. 1981. The Behavioral Ecology of the to have at least partial WF tendencies. Komodo Monitor. University of Florida, Gainesville. The foraging behavior of Gekko gecko, G. hok- Autumn. K. and B. Han. 1989. Mimicry of scorpions ouensis, G. japonicus, Stenodactylus doriae and Tera- by juvenile lizards. Teratoscincus roborowskii toscincus roborowskii is sometimes SW and (Gekkonidae). Chinese Herpetological Research [con- sometimes WF; at least in G. hokouensis, G. japoni- tinued as Asiatic Herpetological Research] 2:60-64. cus and T. roborowskii individuals appear to fluctuate Autumn. K. and Y Z. Wang. 1988. Preliminary obser- between these two predation tactics. vations on the ecology of Phrynocephalus axillaris The variable, often fluctuating. FM of these and Eremias velox in the Turpan Depression, Xinjiang gekkonines probably serves to increase the variety of Uygur Autonomous Region, China. Chinese Herpeto- accessible prey for these nocturnal visual hunters. logical Research (continued as Asiatic Herpetological both and tactics The employment of SW WF by Research] 2:6-13. these gekkonines may depend on the absence of other, Avery. R. A. 1991. Temporal dynamics of a vigilance competing nocturnal lizards. posture in the ruin lizard Podarcis sicula. Amphibia- Geckos are intermediate between SW and WF liz- Reptilia 12:352-356. ards, in both foraging mode and relative clutch mass. Avery. R. A.. C. F Mueller. J. A. Smith and D. J. Bond. 1987a. The movement patterns of lacertid liz- Jour- Acknowledgments ards: speed, gait and pauses in Lacerta vivipara.

nal of London 2 1 1 :47-63. We are indebted to Yael Bogin (Israel Herpetological Zoology, for to from her Information Center) permission quote Avery. R. A.. C. F Mueller. S. M. Jones, J. A. Smith data, to Dr. Amos Bouskila (Simon Fraser University) and D. J. Bond. 1987b. Speeds and movement pat- and Dr. Kellar Autumn (University of California. Ber- terns of European lacertid lizards: a comparative for their advice and keley) decissive help through study. Journal of Herpetology 21:324-329. information, and to Nurit Werner for data processing Bauer. A. M.. A. P. Russell and R. E. Shadwick. 1993. with the NOTITA J. Vindum maxi- program. provided Skin mechanics and morphology of the gecko Tera- mum ra of Teratoscincus roborowskii specimens in toscincus scincus. Amphibia-Reptilia 14:321-331. the California Academy of Sciences. YLW acknowl- Bogin, Y 1993. Personal communication to edges logistic information received from Batur Han Y.L.Werner, dated 9.IX.93. (Academia Sinica, Urumqi); the unusual helpfulness of the of Mr. Bey (Chinese International Travel Service, Tur- Bouskila. A. 1987. Preliminary observations of doriae. Hardun. Journal of pan). his guide during one of the nights at Turpan; and ecology Stenodactylus the Israel Information Center 4:29-40. the friendly logistic base provided for the preparation Herpetological Hebrew; abstract E9-10). of the manuscript by Dr. Ken Aplin, Western Austra- (In English pp. 1997 Asiatic Herpetological Research Vol. 7. p. 163

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