OIKOS 93: 22–31. Copenhagen 2001

The interaction between bird predation and plant cover indetermining habitat occupancy of darkling beetles

Elli Groner and Yoram Ayal

Groner, E. and Ayal, Y. 2001. The interaction between bird predation and planetcover in determining habitat occupancy of darkling beetles. – Oikos 93: 22–31.

Tenebrionid beetles in the Negev Desert exhibit size-related habitat segregation, withlarger species found in denser cover. Size-dependent predation by birds has beensuggested as the mechanism behind this habitat segregation. Two predictions of thishypothesis were tested: (1) plant cover reduces the predation efficiency of birds uponlarge tenebrionids, and (2) birds prefer larger species. Both predictions were sup-ported: plant cover reduced predation rate by the most common spring and summerpredatory birds: white storks (Ciconia ciconia) and stone curlews (Burhinus oedicne-mus), in cage experiments. Results from preference experiments suggest that tenebri-onid species can be divided according to their profitability as prey. Large species arethe most profitable, medium-sized species are less profitable but still acceptable andsmall species are unprofitable and therefore ignored.Field observations demonstrated that the well-vegetated wadi habitats are dominatedby large and small species whereas acceptable, medium-sized species are under-repre-sented in this habitat. The results of the cage experiments indicate possible apparentcompetition between the large profitable and the medium acceptable tenebrionidspecies in the wadis. Aggregative response of predators in the profitable habitat issuggested as the mechanism leading to truncated distribution of prey species. Largeprofitable species are refuge-dependent, medium-sized acceptable species use enemyfree space and small species are predator independent.

E. Groner, Mitrani Dept for Desert Ecology, Blaustein Inst. for Desert Research, BenGurion Uni�. of the Nege�, Midreshet Sede Boqer 84990, Israel and Dept of E�olution,Systematics and Ecology, Berman-Shturman Building, Hebrew Uni�. of Jerusalem,Gi�at Ram, Jerusalem 91904, Israel (present address: School of Biology, Uni�. ofLeeds, UK LS2 9JT [bgyeg@leeds.ac.uk]). – Y. Ayal, Mitrani Dept for DesertEcology, Blaustein Inst. for Desert Research, Ben Gurion Uni�. of the Nege�, MidreshetSede Boqer 84990, Israel.

Primary productivity has traditionally been viewed asaffecting the community structure of higher trophiclevels by regulating energy input (Hairston et al. 1960,Coe et al. 1976, Leibold and Wilbur 1992, Abrams 1993).This is especially true in habitats where productivity islow (Munger and Brown 1981, Oksanen et al. 1981).However, the low primary productivity of the desertenvironment exerts a structural as well as an energeticinfluence on desert habitats. Primary productivity canshape herbivore communities by providing them withrefuge against predators (Bennett and Streams 1986,Black and Hairston 1988, Diehl 1992). Habitats with

dense vegetation will house species that are vulnerable topredation and can find refuge there, while open habitatswill house invulnerable species. Thus species will segre-gate according to their vulnerability to predation (Mit-telbach 1984). Community assemblages in suchpredator-mediated habitats are a function of vegetationlevel and predation pressure (Rozas and Odum 1988).This effect of predation on habitat segregation, andespecially on the usage of vegetated habitats, has beendiscussed mostly with regard to aquatic systems (e.g.Werner et al. 1983) and terrestrial vertebrates (e.g. Lima1990, Rosenzweig and Abramsky 1997).

Accepted 6 November 2000

Copyright © OIKOS 2001ISSN 0030-1299Printed in Ireland – all rights reserved

OIKOS 93:1 (2001)22

Plant cover is sparse in most deserts, consistingmostly of annuals, shrubs and low bushes. As a result,desert animals are likely to be exposed when active, andmay be easily located by visual predators. To compen-sate for the lack of protection by plant cover, manydesert animals exhibit protective morphological andbehavioural traits including crypsis, relatively large ear-bullae and avoidance of activity on moonlit nights(Harrison and Bates 1967, Webster and Webster 1980,Kotler 1984, Bouskila 1995, Abramsky et al. 1996,Skutelsky 1996). Several studies have demonstrated aneffect of visual predators, especially birds, on arthropoddensities in open grassland habitats (Joern 1986,Belovsky et al. 1990, Bock et al. 1992, Fowler et al.1991). Ayal (1988) suggested that such an effect will beeven stronger in sparsely vegetated desert habitats. Inthis study we explore the role of predation on habitatsegregation by examining the effect of predatory birdson the distribution of darkling beetles along a gradientof plant cover in the Negev Desert, Israel; and theeffect of vegetation on vulnerability to predation incage experiments.

Darkling beetles (Coleoptera: Tenebrionidae) arecommon in deserts all over the world. About 20 speciesare commonly found in the compact soils of the NegevHighlands in the south of Israel (Ayal and Merkl 1994,Krasnov and Ayal 1995). These species exhibit size-de-pendent habitat segregation in relation to plant cover(Ayal and Merkl 1994): large species are common in thedensely vegetated wadis (valleys collecting run-off wa-ter), while smaller species are common on slopes andloessal plains with low plant cover. Food is probablynot the source of this segregation: tenebrionids, beingomnivorous-detritovorous (Thomas 1979, Sheldon andRogers 1984), tend to find their food in all micro-habi-tats (Seely and Louw 1980). Also, due to the availabil-ity of dry detritus all year round and everywhere,tenebrionids do not appear to be limited by competition(Wise 1981). Ayal and Merkl (1994) suggested thatpredation by birds drives this size-dependent distribu-tion. They showed that white storks (Ciconia ciconia)feed mainly on tenebrionids when they pass through theNegev, and that beetle densities drop after the time ofthe storks’ arrival from Africa. However, if competitionis not shaping the distribution of small beetles then theyshould either show the same distribution as large spe-cies or, if they are invulnerable to predation, theyshould be found in all habitats regardless of vegetationlevels. The distribution of small species with regard toplant cover needed a closer examination.

In this study the relationship between beetle size,vegetation level and predation were examined usingcage experiments. Specifically the following hypotheseswere tested: (a) the presence of bushes reduces thepredation risk of darkling beetles, and (b) birds preferlarge prey and therefore vulnerability to bird predationcorrelates positively with prey size. The effect of vegeta-

tion on the distribution of species was tested by moni-toring beetle activity in the field and corresponding thebeetle distribution with their vulnerability to predationaccording to size.

Methods

The study system

HabitatThe Negev Highlands are composed of rocky limestoneridges of low hills, 50–250 m high, with an absoluteelevation of 350–1000 m above sea level. Mean annualprecipitation is 90–130 mm (range of 30–200 mm),falling only between October and April. During majorrain events, run-off water flows from the rocky slopesto the wadis and penetrates into the deep loessal soil ofthe wadis. As a result of this redistribution of water,plant cover differs markedly between the different ar-eas. Winter annuals and perennial shrubs, 1–2 m high,are quite common in the wadis, and surface visibility istherefore limited. Conversely, on the rocky slopes,perennial and annual plant cover is sparse and occursonly where soil pockets between the rocks receive run-off water from exposed rocky outcrops above them.Stones of various size provide hiding sites on the slopes.Shrub height in this habitat does not exceed 0.5 m,hence visibility across the surface on the slopes is 25 to100 m all year round in most years. A more detaileddescription of plant species and cover in these habitatsis given by Ayal and Merkl (1994).

Tenebrionid beetlesNegev tenebrionid species are divided into two groups:diurnal spring species (nine species) and nocturnal sum-mer species (eleven species) (Ayal and Merkl 1994).Spring species are active from mid-February to the endof May with peak activity towards the end of March.Summer species are active from mid-April to the end ofSeptember with peak activity during May–June. Thetotal density of spring species is about twice that of thesummer species. Body mass of spring species rangesfrom 0.03–0.8 g and of summer species 0.015–1.9 g(Table 1).

Predatory birdsWhite storks (Ciconia ciconia), and various buzzards(Buteo spp.) and kestrels (Falco spp.) commonly feedon tenebrionids during the spring migration periodfrom mid-March to the end of May (Ayal 1990).Brown-necked raven (Cor�us ruficollis), nocturnal stonecurlew (Burhinus oedicnemus) and little owl (Athenenoctua) are common predators of small arthropods allyear around. The small insectivorous birds in the studyarea do not feed on tenebrionids, perhaps because oftheir hard chitinous exoskeleton (Shkedy and Safriel

OIKOS 93:1 (2001) 23

1992, Rodl 1999). In this study we focus on the whitestork, as it is the most common of the large migratorybirds that pass through the study area in the spring(Leshem 1980) and their regurgitated pellets are com-posed mostly of tenebrionids (87.5%, Ayal and Merkl1994).

The stone curlew is the most common large summerresident bird species in the study area and feeds pre-dominantly on large tenebrionids as well as other largesurface dwelling arthropods (Cramp and Simmons1982, Amat 1986, Green and Tyler 1989). Local stonecurlew faeces consisted mostly of tenebrionid chitin (E.Groner unpubl.).

Animal maintenance

BeetlesBeetles were collected either from pitfall traps or manu-ally in four wadis at Halukim Ridge within 10 km ofthe Blaustein Institute for Desert Research at SedeBoqer in the Negev Highlands (30°51�N, 34°50�E, eleva-tion 450 m). Beetles were sorted according to speciesand kept in plastic trays (10×20×30 cm) in a con-trolled temperature room at 24�2°C with a L:D 14:10light regime until used in experiments. The bottom ofeach tray had 3 cm of soil on which pieces of cardboardwere scattered to provide cover (see Abushama andAl-Salameen 1991). Oatmeal, pieces of carrots andpotatoes, and water were supplied ad libitum and thesoil was dampened once every two weeks. Beetles wereindividually marked on their ventral side using nailvarnish and white correction liquid. In preliminaryexperiments this did not affect either their behaviour ortheir susceptibility to predation.

CagesPredation experiments were carried out in the groundsof the Blaustein Institute for Desert Research in four

wire-netting cages, each 9×9 m and 2 m high. The topsof the cages were covered with clear polythene nettingthat reduced the amount of light in the cages by 10%.At soil level, the cage was fenced with 25-cm-high stripsof black plastic that extended 10 cm into the soil and 15cm above ground, to prevent the beetles from leavingthe cage. The bottom of each cage was smoothed andcleared of vegetation and debris.

Two types of experimental cages were used: barecages with a clear ground surface and shrub coveredcages in which 24 artificial ‘‘shrubs’’ were evenly dis-tributed to imitate higher productivity conditions. Ar-tificial structures were used as shrubs to ensureuniformity. Artificial shrubs consisted of dried branchestied together into bundles 30 cm in diameter and 100cm long. Each artificial shrub was made of four suchbundles: one tied to a metal rod embedded in theground, and three that were laid on the ground aroundits base. This formed a triangle 1 m2 in area. The‘‘shrubs’’ covered a total area of 24 m2 or 30% of thecage floor. Shrubs were moved between cages duringthe experiments so that each cage was changed frombare to shrub-covered and vice versa.

BirdsAll the birds used in the experiments should have hadthe opportunity to encounter tenebrionids in the wildbefore they were caught. Six lopped or hung-wingstorks were borrowed from local zoos. All were born inthe wild but had been kept in captivity for 2–4 yr. Thestorks were housed at night in 4×5×2.5 m highholding cages under a shading roof located next to theexperimental cages. Each stork was fed well with sixone-day-old chicks daily.

Wild stone curlews were captured from airports aspart of ongoing air traffic security control programmes.A total of six stone curlews were used and were housedin pairs during the day in the holding cages (see above)and at night either in the holding cages or in theexperimental cages. Each stone curlew was fed wellwith two one-day-old chicks, cut into pieces, or driedcat food every morning.

Experimental design

The effect of �egetation on predation efficiencyPreliminary experiments revealed that inactive beetlesunder bushes are safe from predation. Therefore, ourexperiments were limited to times of peak beetle activ-ity. Marked beetles were introduced into the cages andallowed to habituate for one hour before a bird wasintroduced to the cage.

Summer (night-time) experiments were carried out usingstone curlews and two large common summer activetenebrionid species: Trachyderma philistina and Pimelia

Table 1. Activity season and body masses of tenebrionidspecies used in the experiments.

Body mass (g)Species(mean�S.D.)

Spring active0.728�0.107Adesmia dilatata Klug0.702�0.097Adesmia abbre�iata Klug

Pimelia boehmi Reitter 0.572�0.095Adesmia metallica syriaca Baudi 0.198�0.042

Summer activePimelia grandis Klug 1.889�0.319Trachyderma philistina Reiche & 1.020�0.152

SaulcyZophosis complanata Solier 0.074�0.022Gonocephalum perplexum Lucas 0.037�0.008Opatroides punctulatus Klug 0.032�0.004Zophosis punctata Brulle 0.016�0.002Adelostoma grande Haag & Rutenberg 0.015�0.003

24 OIKOS 93:1 (2001)

grandis. Ten beetles of one of these two species wereintroduced into the cage at dusk and one bird wasintroduced one hour later. Experiments in both bareand shrub cages were carried out simultaneously. Stonecurlews were removed from the cages just before dawn,and the cages were inspected for surviving beetles thenand again before a new batch of beetles were intro-duced for the following night’s experiment. The numberof surviving beetles per night was recorded as a mea-sure of cover protection. Between five and ten replica-tions were performed for each of six birds.

Spring (daytime) experiments were carried out withwhite storks and Adesmia dilatata, the largest of thecommon spring beetles. Twenty Adesmia were put inthe cage on sunny days, when conditions were suitablefor beetle activity. After 10 min, when the beetles wereacclimatised to the cage, a stork was allowed into thecage. The time since the introduction of the stork untilthe first capture was considered the stork’s acclimatisa-tion time. The stork was then allowed to forage foranother 10 min and the time of each beetle capture wasrecorded. At the end of each experiment the remainingbeetles were collected and counted to ensure therecorded number of captures. Between three and eightexperiments were performed with each of six birds.

Vulnerability to predationStorks were used to investigate whether beetle speciesdiffered in their characteristics as prey as defined below.

Acceptability – Beetles might not be eaten because theyare not accepted by the storks. To test this we exploredwhether the birds will eat a species when it is offeredalone in a tray. In each experiment two individualbeetles of one of eight species, covering a wide range ofbody mass (Table 1), were offered in a white 20×30cm tray to a stork; A. grande (the smallest species of thearea), Z. punctata, O. punctulatus, G. perplexum, Z.complanata, A. metallica, P. boehmi and A. dilatata (thelargest diurnal species of the area). The number of eachspecies consumed during a 5-min period was recorded.Three runs were performed for each of six storks andeight tenebrionid species.

Accessibility – Beetles might not be eaten, althoughthey are acceptable, because they are not accessible tothe storks, even when there are no shrubs. To test thiswe explored whether the birds will locate, catch and eata species when it is offered alone in a bare cage. In eachexperiment 20 individuals of one of the above eightspecies were offered in a bare cage to a stork. Thenumber of beetles consumed during a 10-min periodwas recorded. Three runs were performed for each ofsix storks and eight tenebrionid species.

Preference – Beetles might not be eaten, although theyare acceptable and accessible, because the storks ignorethem when other beetles are available. To test this weexplored whether the storks had any preferences byoffering individuals of two species simultaneously eitherin a tray, where no effort was required to catch thebeetles, or in a bare cage, where some effort wasrequired to catch them. To detect preferences, the Ches-son-Manly model was used to calculate G-statisticstesting if one species was preferred to the other (Manly1974, 1985).

Preference 1 (tray): Each species was tested against thespecies ranked next in size. Experiments were per-formed on adjacent species pairs from the list: A.grande, O. punctulatus, A. metallica, A. dilatata, T.philistina. In each experiment storks were offered fourbeetles on a tray: two of a large species and two of thenext smaller species. The experiment was terminatedafter the stork ate two of the four offered beetles. Eachexperiment was repeated three times for each stork.

Preference 2 (cage): Each of the species was testedagainst the common large species, A. dilatata. Speciesused in this experiment were the same as in the accessi-bility experiment and in addition A. abbre�iata wasused to compare A. dilatata against a species of its ownsize. In order to test preferences of the storks whileforaging, experiments were conducted in large barecages (81 m2). Each run was performed with 20 beetlesin a cage, ten A. dilatata and ten of the test species. Theexperiment was terminated after the stork had con-sumed ten out of the 20 beetles. The proportion of aspecies eaten was used as a measure of preference.Three experiments were performed for each of sixstorks and eight beetle pairings.

In both the preference experiments the number ofcaptures was recorded from the hide using binoculars.However, the identity of the captured species couldonly be revealed by counting the number of survivingbeetles of each species at the end of each trial.

Statistical analysis

To avoid pseudoreplication, analyses were carried outon the mean values for each individual bird. This gavea sample size of six for each analysis, and non-paramet-ric tests were used (Sokal and Rohlf 1995).

Field observations

Tenebrionid activity was quantified in 2–3 study plotsfor both slopes (open habitats) and wadis (shrub habi-tats) in the Negev highlands using pitfall traps over oneyear. Traps were made of plastic cups ten cm in depth

OIKOS 93:1 (2001) 25

Fig. 1. Proportion of T. philistina (T.p.) and P. grandis (P.g.)eaten overnight by stone curlews out of 20 individuals offeredin bare and shrub-covered cages. Means�S.D. are presented(Wilcoxon’s signed-rank test, n=6, T+ =21, P=0.0312, forboth species).

The effect of vegetation on predation efficiency

Stone curlews on summer nocturnal tenebrionidsPredation rates of stone curlew on both P. grandis andT. philistina were significantly higher in the bare than inthe shrub cages (Fig. 1). Almost all of the ten individu-als present in the cage were consumed in the bare cages,whereas less than half were consumed in the shrubcages. The consumption rates for individual stonecurlews were 1.7 to 3 times higher in open cages than inshrub cages.

White storks on spring diurnal-acti�e tenebrionidsConsumption rates of A. dilatata by storks were signifi-cantly higher in bare than in shrub cages (Fig. 2).Predation levelled off once about eight of the 20 beetleshad been consumed. In bare cages storks then stoppedforaging and spent the rest of the time grooming andperching, while in shrub cages storks continued toforage for the whole 10 min of the experiment. Duringthis period they succeeded in capturing only three tofour beetles. The beetles took cover in a shrub at theapproach of the stork, unless they were captured on theway. Only very rarely did the storks manage to extri-cate beetles from a shrub.

Vulnerability to predation

Beetle acceptabilityWhen offered on a tray, all beetle species were con-sumed immediately by storks, regardless of size. Nobeetle was ever left uneaten.

Beetle accessibilityWhen species were offered singly in a bare cage, eightof the 20 individual beetles of the four largest specieswere consumed in 10 min (Fig. 3). Of the four smallerspecies almost none (G. perplexum and O. punctulatus),

and 500 cm3 in volume, buried level with the soilsurface. In each site, traps were arranged in grids of fiverows of ten cups. Traps were checked once a week inOctober–May, and in the early morning for five con-secutive days each month in June–September. Thenumber of individuals of each species was recorded andbeetles were then released. Pitfall traps have manylimitations for quantifying absolute species densities.However, they do provide an index combining relativeabundance and activity levels allowing a comparison ofthe rate at which one encounters different species in thefield. More information on the methodology and habi-tats can be found in Ayal and Merkl (1994). Theactivity index was defined as the average number ofindividuals trapped per trap per day and we will referto it as beetle abundance.

For each species the indices were averaged for shrubhabitats (wadis) and open habitats (north and southslopes) then summed to provide an overall activityindex. The average activity index in shrub habitats wasdivided by the overall activity index to give a distribu-tion index, similar to that of Schwinning and Rosen-zweig (1990). A value of 1 indicates activity only inshrub habitats and a value of 0 indicates activity only inopen habitats. Species values were then averaged ac-cording to size. The total abundance of beetles in eachof the two habitat types was calculated by summing upthe abundances of all species present in them. Thesetotals represent a profitability index of the respectivehabitats to the birds.

Results

In all trials of the experiments in which captures wererecorded there was a perfect match between the numberof recorded captures and the number of survivingbeetles at the end of each trial proving the reliability ofour records.

Fig. 2. Accumulated number of A. dilatata eaten by a singlestork during 10 min of foraging in a bare and shrub-coveredcages. Means�S.D. are presented (Wilcoxon’s signed-ranktest, applied for 100 s, n=6, T+ =21, P=0.0312).

26 OIKOS 93:1 (2001)

Fig. 3. The number of individuals eaten by a stork whenoffered 20 individuals of a single species in a bare cage(means�S.D.) in relation to body size (mass on log scale).Species used are the same as in Fig. 5 except for A. abbre�iata(A. dilatata was used instead).

Fig. 5. The proportion of each species eaten when presented ina bare cage together with A. dilatata according to their size(log scale). Figures are means�S.D. Chesson-Manly teststatistics, n=6: Adesmia abbre�iata G=0.36, P�0.1; P.boehmi G=0.43, P�0.1; A. metallica G=0.45, P�0.1; Z.complanata G=32.32, P�0.001; G. perplexum (no beetleswere eaten); O. punctulatus (no beetles were eaten); A. grande(no beetles were eaten) and Z. punctatus (no beetles wereeaten).

or none at all (A. grande and Z. punctata) were con-sumed. The storks tried to catch the small beetles, butthe beetles were too evasive and the storks gave up aftera few minutes. Beetle preference

Preference 1 – When offered two species close in sizeon a tray the storks displayed a significant preferencefor the larger species in every case (Fig. 4). Preference 2– However, when individuals of each of eight specieswere offered in a bare cage together with A. dilatata,there was a clear dichotomy in behaviour: no prefer-ence was shown between the three largest species andA. dilatata, whereas the four smallest species werealmost totally ignored when A. dilatata was present asan alternative prey species (Fig. 5). As the experimentswere only terminated when half of the available beetleswere consumed they could last a long time and up to 30min.

Field observations

Species that are 0.04 g or smaller were too evasive andtherefore inaccessible to storks (Fig. 3) and were con-sidered small for the purposes of the field analysis.Species that are 0.2 g or larger were consumed equallyto the largest diurnal species (A. dilatata) and wereconsidered large (Fig. 5). Species that are between 0.04g and 0.2 g were considered medium-sized species.

Size had a significant effect on habitat usage(ANOVA, F2,23=7.86, P=0.003). Large species usedmostly vegetated habitats (wadis), medium-sized speciesused mostly open habitats (slopes) and small speciesused both open and vegetated habitats (Fig. 6a). Therewas a significant difference in habitat usage betweenmedium-sized species and both large (F1,16=13.98, P=0.002) and small species (F1,11=7.40, P=0.020). There

Fig. 4. The proportion of each tenebrionid species eaten, whentwo species were presented simultaneously in a tray and thebird was allowed to consume two out of the four offeredindividuals (Chesson-Manly test, n=6, G�4 and P�0.001for all the pairs).

OIKOS 93:1 (2001) 27

was no significant difference between large and smallspecies (F1,19=3.24, P=0.088).

Overall, many more beetles were caught in the wadisthan in the open habitats (Fig. 6b). Medium-sizedbeetles contributed less than the large beetles to thetotal densities in both habitats.

Discussion

The results lend experimental support to Ayal andMerkl’s (1994) hypothesis that predation by birds maybe the mechanism behind the size-dependent habitatsegregation observed among the tenebrionid species ofthe Negev Highlands. The size of beetles active in eachof the habitats is determined by an interaction betweentwo factors: (1) the level of protection provided byhabitat structure for tenebrionid species and (2) size-de-pendent vulnerability to predation arising from preda-tor preferences. The cage experiments demonstratedthat plant cover substantially decreases the predationrate of both model bird species upon large tenebrionids.During the migration season, storks typically consume

70–100 tenebrionids before their gizzard is full and thechitinous beetle integuments are regurgitated as a singlepellet (Ayal and Merkl 1994; pers. obs.). Taking intoaccount that flocks of 10–500 storks are commonlyobserved foraging within the study area during thespring (Ayal pers. obs.) bird predation may have anenormous effect on the local spring-active tenebrionidpopulations (Ayal and Merkl 1994).

The experiments also demonstrated a clear preferencefor large over small tenebrionid species by the storks.Although species of all sizes were consumed by thestorks, the birds preferred the larger species of a pairwhen offered them simultaneously in trays (Fig. 4).However, when a single species was offered to thestorks in a large bare cage the birds pursued and ateonly large and medium-sized species (i.e. A. dilatata, P.boehmi, A. metallica and Z. complanata) but not smallones (i.e. G. perplexum, O. punctulatus, A. grande andZ. punctata) (Fig. 3). Moreover, when these specieswere offered to the storks in a large bare cage pairedwith A. dilatata, Z. complanata was also ignored as wellas the other four smaller species. Fig. 5 shows a zero-one rule behaviour (Krebs et al. 1977), whereby abovea certain size threshold all species are accepted equallyand below it they are rejected.

Thus, tenebrionid species can be said to be dis-tributed according to their profitability to large birds.Large beetles are most profitable and are, therefore,preferred by storks. Their distribution is refuge depen-dent and is restricted mostly to shrub habitats (wadis).Small species are unprofitable and seem to be un-touched by the storks, being too small to catch. Ac-cordingly, their distribution is refuge-independent.Medium-sized beetles are, on one hand, less profitablethan large ones, but on the other hand, acceptable.These beetles are found mostly in open habitats. Thisdivision into three categories, rather than two that Ayaland Merkl 1994 suggested, might explain why theyclaimed small species are found mainly in the openhabitats, despite small species being refuge independent.In fact, small species are equally distributed among thehabitats. It is the segregation between medium-sizedspecies and large ones that makes the habitat differ.

Since most of a stork’s diet in the Negev is composedof tenebrionids (Ayal and Merkl 1994), the profitabilityof a habitat, for the storks, is determined by thebiomass of a beetle times the rate of capture. Althoughthe rate of capture is 3.5 times higher in open habitats,the size and density of large beetles in wadis more thancompensate for that. The abundance of large beetles is2.5 times higher than that of medium-sized in the openhabitats and over 30 times in the shrub habitats (Fig.6b). More so, the size of the most common species inthe wadi, the large A. dilatata, is ten times larger thanthe most common medium species in the open slopes,Z. complanata, making the wadis much more profitablefor the birds than open habitats. As consumers are

Fig. 6. (a) Habitat usage index of each of a size group oftenebrionids in the field. Relative abundance is the proportionof each size caught in the wadis out of the total caught of thatsize (wadis+open). Small species are �0.04 g, Medium-sizedspecies are between 0.04 g and 0.2 g and large species are�0.2 g. Mean�S.D. are given. (b) Abundance (as measuredby activity index) of the three beetle size categories in openand shrub habitats. Number of species in each size category:small=8, medium=5, large=13.

28 OIKOS 93:1 (2001)

Table 2. Size effect on vulnerability to predation and habitat usage.

Beetle size

Small LargeMedium

Predation vulnerability Unprofitable Acceptable (less profitable) Most profitable

Habitat usage Refuge dependentPredation independent Enemy free space

expected to aggregate in profitable habitats (Hasselland May 1974, Curio 1976, Hassell 1982, Schwinningand Rosenzweig 1990), it is not surprising to learn thatstorks tend to forage in the wadis rather than the openhabitats (pers. obs.).

Note that we measured the beetles’ relative vulnera-bility by exposing them to storks in bare cages, whichsimulate the open habitat in which large species aremore vulnerable than medium ones. However, relativevulnerability may change if measured in shrub-coveredcages under conditions simulating the wadi. That is,large species may be better than medium ones at utilis-ing refuges and hence become less vulnerable to preda-tion in the wadi than medium species. This could be thecase if size is not the only factor that matters. Beingcryptic, fast or poisonous may lower the vulnerabilityof a species. If this is the case it will strengthen ourargument about the relative vulnerability of medium-sized species in the wadi and will lend stronger supportto the above explanation of size-dependent habitatsegregation observed in the field.

Consequently, medium-sized species, sharing a habi-tat with large species, could suffer from apparent com-petition inflicted on them by the abundance of largetenebrionids attracting large predatory birds to thewadis. Conversely, the open habitats are less foraged bystorks and although they might seem more risky, theyare, in fact, safer for the medium-sized species. Indeed,in the data presented here, medium-sized species areunder-represented in the wadis relative to both largeand small tenebrionids, while they are relatively com-mon in open habitats.

Resource competition and abiotic factors may serveas alternative explanations to the habitat segregationbetween large and medium-sized tenebrionids observedin the field. However, resource competition seems to beunimportant in determining tenebrionid abundances(Wise 1981). It is also difficult to conceive how abioticfactors will act differentially on medium-sized species,i.e. what is unique to medium-sized beetles that makesthe wadi less hospitable to them than to either small orlarge ones. Hence, apparent competition seems to us tobe the best explanation for the observed distribution,considering the attractiveness to storks of large beetlesrelative to medium ones as demonstrated in the experi-ments. Yet the only way to differentiate between theabove three mechanisms is by carrying out fieldexperiments.

The paucity of species, in the refuge habitat, that areacceptable but not highly profitable may be a commonphenomenon in systems in which habitat segregation ispredator-mediated. When there is ‘‘apparent ammensal-ism’’ (one-sided ‘‘apparent competition’’) betweenprofitable and acceptable species, the acceptable speciescould be absent from the refuge habitat and over-repre-sented in the open habitat. This enables them to avoidthe predators who are attracted to the refuge habitat bythe profitable species. Table 2 shows how profitabilitycan determine the distribution of prey species. Theacceptable species can share a habitat with theprofitable species only if the refuge in the profitables’habitat is a ‘‘perfect’’ one for them. Otherwise, avoidingthose habitats is safer.

Ideal free distribution models of unequal competitorssuggest that density dependence may lead to speciessegregating between patches of different quality givinga ‘‘truncated distribution’’ (Sutherland and Parker1985, 1992, Tregenza 1995). In a similar way, a trun-cated distribution could be the result of apparent com-petition rather than competition. Since habitat selectioncan be a result of vulnerability to predation (Kotler etal. 1991), the distribution of the prey depends on theeffect of prey density upon predator distribution: themore predators aggregate the less prey should aggre-gate. If sharing the burden of predation reduces the percapita vulnerability to predation (Rosenzweig et al.1997) predation will affect prey distribution in theopposite way to competition (Grand and Dill 1999), i.e.it will be inversely density dependent. In such cases preyaggregate in order to reduce their predation risk. How-ever, if high densities of prey create an overcompensat-ing aggregative response by predators (Royama 1970,Sutherland 1983), then we should expect to see directdensity dependent habitat segregation (Chesson andMurdoch 1986). This is similar to the truncated pheno-type distribution predicted by some unequal competitorideal free distribution models (Tregenza 1995), onlyprey species avoid aggregation to minimise predationrisk, rather than competition. Prey distribution dependsmainly on the level of the aggregative response of thepredators (Hassell 1982). Efficient refugia, which reducepredation (to a limit), will concentrate prey, and thusmake the refugia more attractive to predators (Schwin-ning and Rosenzweig 1990), resulting in an aggregativeresponse. The cage experiments show that the wadis docontain effective refuges, decreasing predation by 71%

OIKOS 93:1 (2001) 29

(storks) and 54% (stone curlews). This should increasedensities of refuge-dependent species making the wadisvery attractive to predators, thus leading to a truncateddistribution between prey species, as field data suggest.

Acknowledgements – We are grateful to Karsten Wiblitz, EvanMeir, Tracey Holt, Mike Fyne, Mark Goldberg, Iris Moosly,Shi Dori and Tamar Tzitlin for help with the experiments andfieldwork. E.G. is grateful to Uriel Safriel for supervisiongiven during the work and to the Vatat foundation for finan-cial support during the study period. We thank kibbutz SedeBoker for permission to carry out field observations on theirland. Thanks to Zoe Grabinar, Stephen Hartley, Dan Horae,Jens Krause, Tom Tregenza and Dale Taneyhill for construc-tive comments. This is publication of the Mitrani Dept forDesert Ecology.

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