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333 Turk J Zool 2011; 35(3) 333-341 © TÜBİTAK doi:10.3906/zoo-0904-19 Ecology and biology of scorpions in Palmyra, Syria Adwan Hussien SHEHAB 1 , Zuhair Sami AMR 2, *, Jeremy Arthur LINDSELL 3 1 General Commission for Scientific Agricultural Research (GCSAR), Douma, P. O. Box 113, Damascus - SYRIA 2 Department of Biology, Jordan University of Science & Technology. P. O. Box 3030, Irbid - JORDAN 3 e Royal Society for the Protection of Birds, e Lodge, Sandy, Beds, SG19 2DL - UK Received: 21.04.2009 Abstract: Near Palmyra, in the Syrian Desert, 5 species of scorpions belonging to 2 families (Buthidae and Scorpionidae) were observed; Buthacus tadmorensis, Androctonus crassicauda, Leiurus quinquestriatus, Orthochirus scrobiculosus, and Scorpio maurus palmatus. B. tadmorensis accounted for 80.6% of the total number of recovered or observed scorpions, while O. scrobiculosus was the least common (1.4%). Pitfall traps proved to be more efficient at sampling (304 individuals) than checking under stones (57 individuals). Pitfall trapping results showed that scorpion abundance differed significantly between the 3 survey areas, while their abundance showed no significant difference among the 3 areas when employing the under-stone method. Notes on predation of scorpions (interspecific and intraspecific) and predators of scorpions are also included. Seasonal abundance and emergence of scorpions is described briefly. Biometric data on collected scorpion species indicating their weight are given. Population structure of B. tadmorensis during the study period is analyzed. Key words: Scorpion, Buthacus tadmorensis, pitfall trapping, predation, population structure, Syria Research Article * E-mail: [email protected] Introduction Limited knowledge is available concerning the scorpions of Syria. Only 2 recent papers addressed the systematics of the scorpions of Syria (Kabakibi et al., 1999; Stathi and Lourenço, 2003). Kovařík and Whitman (2004) listed 5 species of scorpions from Talilah National Park, within the vicinity of Palmyra, Syria. On the other hand, there is a complete lack of species richness and abundance data for scorpions inhabiting the Syrian Desert. In the Middle East, Warburg et al. (1980) studied the scorpion distribution and diversity in arid regions of northern Palestine. Warburg (2000) studied several aspects of scorpion cohabitation. e burrowing behavior of Scorpio maurus palmatus was investigated by Rutin (1996). Fragmentary reports dealt with predation of other animals on scorpions in the Middle East (Tigar and Osborne, 2000; Zlotkin et al., 2003) including reptiles and birds. No previous study addressed the diversity and ecology of scorpions in Syria. e systematics of the genus Buthacus was revised by Kovařík (2005). He placed in synonymy with B. macrocentrus at least 3 other species, Buthacus tadmorensis Simon, Buthus pietschmanni Penther, and Buthacus yotvatensis Levy et al. However, Lourenço

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  • A. H. SHEHAB, Z. S. AMR, J. A. LINDSELL

    333

    Turk J Zool2011; 35(3) 333-341 © TÜBİTAKdoi:10.3906/zoo-0904-19

    Ecology and biology of scorpions in Palmyra, Syria

    Adwan Hussien SHEHAB1, Zuhair Sami AMR2,*, Jeremy Arthur LINDSELL31General Commission for Scientifi c Agricultural Research (GCSAR), Douma, P. O. Box 113, Damascus - SYRIA

    2Department of Biology, Jordan University of Science & Technology. P. O. Box 3030, Irbid - JORDAN3Th e Royal Society for the Protection of Birds, Th e Lodge, Sandy, Beds, SG19 2DL - UK

    Received: 21.04.2009

    Abstract: Near Palmyra, in the Syrian Desert, 5 species of scorpions belonging to 2 families (Buthidae and Scorpionidae) were observed; Buthacus tadmorensis, Androctonus crassicauda, Leiurus quinquestriatus, Orthochirus scrobiculosus, and Scorpio maurus palmatus. B. tadmorensis accounted for 80.6% of the total number of recovered or observed scorpions, while O. scrobiculosus was the least common (1.4%). Pitfall traps proved to be more effi cient at sampling (304 individuals) than checking under stones (57 individuals). Pitfall trapping results showed that scorpion abundance diff ered signifi cantly between the 3 survey areas, while their abundance showed no signifi cant diff erence among the 3 areas when employing the under-stone method. Notes on predation of scorpions (interspecifi c and intraspecifi c) and predators of scorpions are also included. Seasonal abundance and emergence of scorpions is described briefl y. Biometric data on collected scorpion species indicating their weight are given. Population structure of B. tadmorensis during the study period is analyzed.

    Key words: Scorpion, Buthacus tadmorensis, pitfall trapping, predation, population structure, Syria

    Research Article

    * E-mail: [email protected]

    IntroductionLimited knowledge is available concerning the

    scorpions of Syria. Only 2 recent papers addressed the systematics of the scorpions of Syria (Kabakibi et al., 1999; Stathi and Lourenço, 2003). Kovařík and Whitman (2004) listed 5 species of scorpions from Talilah National Park, within the vicinity of Palmyra, Syria. On the other hand, there is a complete lack of species richness and abundance data for scorpions inhabiting the Syrian Desert.

    In the Middle East, Warburg et al. (1980) studied the scorpion distribution and diversity in arid regions of northern Palestine. Warburg (2000)

    studied several aspects of scorpion cohabitation. Th e burrowing behavior of Scorpio maurus palmatus was investigated by Rutin (1996). Fragmentary reports dealt with predation of other animals on scorpions in the Middle East (Tigar and Osborne, 2000; Zlotkin et al., 2003) including reptiles and birds. No previous study addressed the diversity and ecology of scorpions in Syria.

    Th e systematics of the genus Buthacus was revised by Kovařík (2005). He placed in synonymy with B. macrocentrus at least 3 other species, Buthacus tadmorensis Simon, Buthus pietschmanni Penther, and Buthacus yotvatensis Levy et al. However, Lourenço

  • Ecology and biology of scorpions in Palmyra, Syria

    334

    (2006) argued on the validity of the new assignment of B. tadmorensis, and concluded that B. tadmorensis is a valid species, not related to B. macrocentrus as asserted by Kovařík (2005). Furthermore, analysis of the morphological characteristics of the species of Buthacus distributed in Sinai and the Middle East, including Syrian specimens, indicate only that Buthacus leptochelys nitzani Levy, Amitai & Shulov, 1973, could be a junior synonym of B. tadmorensis (Lourenço, 2006). For the purpose of uniformity in the literature, we will consider the name B. tadmorensis for the Palmyra scorpion.

    While undertaking ecological fi eldwork near Palmyra, Syria, we collected a large number of scorpions and made a number of fi eld observations. Th e aims of the present study were to investigate scorpion diversity and abundance, compare 2 sampling methods, comment on the population structure of Buthacus tadmorensis, and document some fi eld observations of these scorpions.

    Materials and methodsStudy sitesPalmyra is located in the heart of the Syrian

    Desert. Th e annual rain fall is about 127 mm (average for the last 50 years), with the maximum annual mean temperature reaching 25 °C and a minimum of 12 °C. January and February are the coldest months in Palmyra, where in previous years the average monthly minimum temperature reached -4.4 °C. June, July and August are the hottest months, and the monthly temperature can reach 42 °C in July. Near Palmyra, within the Northern Bald Ibis Reserve, 3 sites were selected as study areas (Figure 1). Th e following are descriptions for each site:

    1. Site 1: about 596 m asl. Located 18 km northeast of Palmyra. Th is is a fl at arid area, with small wadi beds formed by fl ash fl oods. Scattered stones are abundant over the hard soil. Sand sheets caused by wind action are formed in some parts of this area and dominant vegetation consists of Peganum harmala with less than 1% cover. Other plants include Achillea fragantissima, Poa sinaica, and Haloxylon articulata.

    2. Site 2: about 732 m asl. Located 18 km northwest of site 1. Th is is an arid area with hard soil and few rocks. It is a fl at area with wadi systems. Vegetation cover is about 10%, with Anabasis syriaca being the dominant species. Other less common plants include H. articulata and Poa sinaica.

    3. Site 3: altitude 924 m asl. Located 19 km west of site 2. A fl at arid area with loose soil and scarce stones. Vegetation cover is less than 1%

    Figure 1. Landscape of the 3 study sites.

  • A. H. SHEHAB, Z. S. AMR, J. A. LINDSELL

    335

    and consists of Anabasis syriaca, H. articulata and Poa sinaica.

    Within the study area, we identifi ed numerous species of arthropods that were collected in pitfall traps or were observed under stones. Hymenoptera (ants) and coleopterans were the most frequently encountered insects and represented several families (Tenebrionidae: Trachiderma hispida, Erodius sp., Mesostena sp., Akis sp., Adesmia sp., Pimelia sp., Zophosis sp.; Carabidae: Calosoma chlorosticum; Buprestidae: Julodis distincta; and Scarabaeidae: Scarabaeus sacer). Solphugidae, Empusidae (Berpharopsis sp.), and Acrididae were less abundant.

    Scorpion collectingPitfall transects: In each study site, 6 transects were selected. For

    each transect, 5 plastic containers (13 × 9 cm) were leveled in the ground, 50 m apart, and were without bait. Scorpions were inspected, measured, identifi ed, and then released every 2-7 days beginning from April 2008 to the end of July 2008. Other arthropods that were trapped in the plastic containers were also identifi ed where possible, counted, and then released.

    Under-stone collecting:At each site, 20 stones (15-30 cm in diameter)

    were lift ed to check for the presence of scorpions. Th is method was employed every 15 days beginning from April until the end of July.

    Data analysisTh e association of scorpion abundance with

    locality and methods of survey were analyzed using Genstat 7th edition soft ware for general analysis of variance.

    Predation activityDuring the fi eld work, various activities of

    collected scorpions were recorded, including scorpion-scorpion predation and predation of other animals on scorpions. Th e predation of these animals was documented with digital images.

    BiometryTotal body length (from the anterior edge of

    the prosoma to the end of the telson) for collected scorpions was measured by means of a digital calliper (measuring range: 0-150 mm), and scorpions were weighed using a digital balance (0.01 g increments).

    ResultsScorpion diversityA total of 361 scorpions representing 5 species

    (Figure 2) belonging to 2 families (Buthidae and Scorpionidae) were collected from the study area: Buthacus tadmorensis (Simon, 1892), Androctonus crassicauda (Olivier, 1807), Leiurus quinquestriatus Hemprich & Ehrenberg, 1829, Orthochirus scrobiculosus (Grube, 1873), and Scorpio maurus palmatus (Hemprich & Ehrenberg, 1829).

    Table 1 shows the number of recovered species from the 3 study sites using the pitfall traps and under-stone collecting method. By far, B. tadmorensis was the most commonly collected species for both methods, accounting for 63.6%-86.6% of the total number of collected scorpions from all 3 sites. Orthochirus scrobiculosus was the least common species (2.7%-3.9% of the total number of collected scorpions) and was recovered from 2 areas. In site 2, B. tadmorensis was found in pitfall traps along with A. crassicauda, O. scrobiculosus, and L. quinquestriatus.

    Comparison between pitfall and under-stone sampling methods

    Pitfall trapping proved to be more effi cient than the under-stone method; while the fi rst method yielded 304 scorpions, the second yielded only 57 scorpions.

    Both pitfall traps and searching under stones recorded 5 scorpion species during the entire period of the study. Orthochirus scrobiculosus and S. m. palmatus were recovered from under stones during April only.

    Pitfall trapping methodPitfall results showed that scorpion abundance

    diff ered signifi cantly between the 3 areas; Site 1 (M = 1.4 scorpions), Site 2 (M = 2.8 scorpions), and Site 3 (M = 3.4 scorpions), with the lowest in Site 1 and highest in Site 3 (F = 3.83, P = 0.028). Th e diff erence was signifi cant only between Site 3 and Site 1, while no signifi cant diff erences were observed in scorpion abundance between Site 2 and Site 3 or Site 2 and Site 1 (LSD = 1.487).

    A signifi cant diff erence was found between the 5 scorpion species trapped in pitfalls (F = 41.78, P < 0.001), where B. tadmorensis was the most abundant

  • Ecology and biology of scorpions in Palmyra, Syria

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    (M = 10.33 scorpions), while no signifi cant diff erence was found between the other 4 species themselves (LSD = 1.919), A. crassicauda (M = 0.63 scorpions), L. quinquestriatus (M = 1.21 scorpions), O. scrobiculosus (M = 0.13 scorpions), and S. m. palmatus (M = 0.38 scorpions).

    Under-stone methodScorpion abundance employing the under-stone

    method showed no signifi cant diff erence between the 3 areas: Site 1 (M = 0.25 scorpions), Site 2 (M = 0.50 scorpions), and Site 3 (M = 0.67 scorpions) (F = 2.74, P = 0.073).

    A signifi cant diff erence was found among the 5 scorpion species recovered from under stones (F = 19.82, P < 0.001), where B. tadmorensis was the most abundant scorpion species (M = 1.79 scorpions), while no signifi cant diff erence was found among the other 4 species (LSD = 0.471), A. crassicauda (M = 0.12 scorpions), L. quinquestriatus (M = 0.29 scorpions), O. scrobiculosus (M = 0.08 scorpions), and S. m. palmatus (M = 0.08 scorpions).

    Seasonal abundance of scorpions Table 2 shows the number of collected scorpions

    over the study period. Numbers of scorpions collected

    A B

    C D

    E

    Figure 2. Scorpions collected from the study area. A) Scorpio maurus palmatus, B) Androctonus crassicauda, C) Orthochirus scrobiculosus, D) Leiurus quinquestriatus, and E) Buthacus tadmorensis.

  • A. H. SHEHAB, Z. S. AMR, J. A. LINDSELL

    337

    in pitfalls increased signifi cantly over the season (F = 5.02, P < 0.001), with the highest levels in July (LSD = 2.428); the number of scorpions observed under stones decreased signifi cantly over the season (F = 2.28, P = 0.041), with the highest levels in the second half of April (LSD = 0.596). For instance, both B. tadmorensis and L. quinquestriatus increased about six-fold.

    Buthacus tadmorensis was the most common species throughout the study period (Table 2), reaching the highest level in July, with A. crassicauda ranked second. Numbers of O. scrobiculosus remained constant over the study period.

    Predation by scorpions of other arthropodsWe observed several occasions where scorpions

    predated on other arthropods as well as other scorpions; B. tadmorensis was observed feeding on a mantid of the genus Eremiaphila sp. during day time in a pitfall trap, while B. tadmorensis was observed feeding on a 1-cm spider.

    Interspecifi c predation among scorpions was observed; an adult L. quinquestriatus fed on all body parts except the metasoma of B. tadmorensis. Intraspecifi c predation was also observed, with an adult B. tadmorensis attacking a 3-cm young individual from its chelicerae. In captivity, a gravid

    Table 1. Recovered scorpions employing under-stone method and pitfall transects in the study sites.

    Scorpion speciesUnder stones Pitfalls transect

    TotalSite 1 Site 2 Site 3 Site 1 Site 2 Site 3

    N % N % N % N % N % N % N %

    A. crassicauda 1 9.1 2 10 0 0 3 5.4 8 7.1 4 2.9 18 5

    B. tadmorensis 7 63.6 14 70 22 84.6 40 71.4 97 86.6 111 81.6 291 80.6

    L. quinquestriatus 3 27.3 1 5 3 11.5 6 10.7 2 1.8 21 15.4 36 10

    O. scrobiculosus 0 0 1 5 1 3.9 0 0 3 2.7 0 0 5 1.4

    S. m. palmatus 0 0 2 10 0 0 7 12.5 2 1.8 0 0 11 3

    Total 11 100 20 100 26 100 56 100 112 100 136 100 361 100

    Table 2. Th e number of recovered scorpions using opportunistic collecting and pitfall traps during the study period from the 3 sites.

    Scorpion speciesMethod of collecting

    MonthTotal

    April May June July

    A. crassicaudaUnder stone 1 0 2 0 3Pitfall traps 2 6 1 6 15

    B. tadmorensisUnder stone 12 10 12 9 43Pitfall traps 19 41 91 97 248

    L. quinquestriatusUnder stone 1 0 4 2 7Pitfall traps 1 0 6 22 29

    O. scrobiculosusUnder stone 2 0 0 0 2Pitfall traps 0 1 1 1 3

    S. m. palmatusUnder stone 2 0 0 0 2Pitfall traps 0 3 3 3 9

    Total 40 61 120 140 361

  • Ecology and biology of scorpions in Palmyra, Syria

    338

    female of B. tadmorensis gave birth to 21 individuals, all of which later died; the mother ate all of them within a day.

    Predators of scorpionsDuring our study we observed several animals,

    including beetles, ants, lizards, and birds, feeding on scorpions. On one occasion, a lizard of the species Acanthodactylus boskianus viciously attacked a 5-cm B. tadmorensis (Figure 3A). Northern Bald Ibis, Geronticus eremita, was photographed by Lubomir Peske during June 2007 at Site 3, while feeding on B. tadmorensis (Figure 3B). Droppings of the Bald Ibis collected under the Ibis nesting sites yielded a few remains of B. tadmorensis. Within the pitfall traps, remains of B. tadmorensis were found in association with the presence of ants, Trachyderma hispida, Erodius sp., and Pimelia sp. Pellets collected near a nest of a Little Owl, Athene noctua, revealed many remains of B. tadmorensis, S. m. palmatus, and A. crassicauda.

    Biometric data on scorpionsA total of 14 B. tadmorensis representing diff erent

    sizes were weighed. Scorpions measuring 4, 5, and 6 cm in length had an average weight of 0.39 g (n = 6, 0.29-0.57 g, SD ± 0.124), 0.466 g (n = 5, 0.33-0.62 g, SD ± 0.113), and 0.95g (n = 3, 0.6-1.26 g, SD ± 0.332) respectively. A single O. scrobiculosus measuring 2 cm in length weighed 0.08 g, and 2 A.

    crassicauda measuring 8 cm each had an average weight of 3.33g (n = 2, 2.68-3.98 g). We also collected 4 L. quinquestriatus measuring 2 cm (n = 1) and 6 cm (n = 3, 1-1.98 g, SD ± 0.494), with an average weight of 0.33 g and 1.53 g, respectively, and 4 S. m. palmatus with body length ranging from 3-7 cm, weighing 0.36 g (3 cm, n = 1), 2.05 g (6 cm, n = 2, 1.47-2.6 g, SD ± 0.841), and 2.22 g (7 cm, n = 1).

    Population structure of B. tadmorensisButhacus tadmorensis was the most common

    species, allowing us to study variation in size in order to determine population structure. Scorpions measuring 2 cm constituted the highest percentage of the population (34.1%), and larger scorpions reaching about 6 cm constituted 4.9% of the population (Figure 4). Th e observed diff erences among collected specimens were probably due to diff erent instars or sex of the arthropod. One of the 6-cm long specimens was a gravid specimen of B. tadmorensis, which gave birth to 21 young during 24 July 2008.

    Size groups of collected B. tadmorensis were similar among the 3 study sites (Figures 4 and 5). Small scorpions measuring 2 cm in length were the most common in all study areas. Th e number of small scorpions increased dramatically over the study period. Large scorpions measuring 5 cm increased to a maximum in July and the largest size recorded in this study was 6 cm in length, although their numbers were very low throughout the study.

    AB

    Figure 3. Predators of scorpions. A) Lizard, Acanthodactylus boskianus feeding on B. tadmorensis. B) Th e Northern Bald Ibis, Geronticus eremita feeding on B. tadmorensis.

  • A. H. SHEHAB, Z. S. AMR, J. A. LINDSELL

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    DiscussionDiff erent methods have been evaluated for

    sampling various terrestrial arthropods, including pitfall traps, active searching of quadrats, wet cloths, and drive transects (Tigar and Osborne, 1997; Druce et al., 2004). In general, scorpions were most eff ectively sampled using pitfall traps. Our results are in agreement with Druce et al. (2004), for whom pitfall trapping resulted in a higher number of recovered samples than searching under stones. Even if active searching at night using ultraviolet light is considered the most eff ective sampling method (Sissom et al., 1990; Warburg, 1997), this method is time and eff ort consuming and requires several fi eld biologists, so we did not test it.

    Th e majority of the scorpion species recovered during this study were collected using pitfall traps, while O. scrobiculosus and S. m. palmatus were recovered during April by searching under stones. Th is is perhaps due to the mild temperature during April, compared with the hot summer months when both species retreat to their deep burrows (Amr and Al-Oran, 1994). Rutin (1996) found that S. m. palmatus was active during April, excavating soil for burrow preparation.

    Relative abundance of scorpions was studied among some North American species using pitfall traps (Bradley and Brody, 1984). It was found that

    Paruroctonus utahensis was the dominant species in fl at grassland habitat, along with other species in low numbers. Other species (Vejovis coahuilae and Vejovis russelli) were associated with rocky cliff habitat. In our study, Site 3 had the highest number of scorpions, and B. tadmorensis was the most dominant species. Th is is perhaps due to the dominant loose soil, while the other 2 sites (Site 1 and Site 2) have harder and drier soil textures.

    Höfer et al. (1996) studied the surface abundance of the scorpion Brotheas amazonicus, using pitfall traps. Th ey found that capture rates in the primary plateau forest and in the primary forest on white sand soil were higher than in disturbed areas. Th ey concluded that high structural diversity, ultimately refl ecting the availability of hiding places, is important for B. amazonicus. Our study sites were located within the arid Irano-Turanian biotope, with variations in soil hardness and vegetation cover. Structural habitat diversity in the study sites are low, and consist of burrows, scattered stones, and hiding places under bushes.

    It seems that emergence from burrows at night is related to decreasing levels of ambient temperature and insect abundance. Th is opinion by shared with Polis (1980). In the study areas, several species of terrestrial arthropods were also trapped in the pitfall traps, with the highest number of various arthropods recorded from Site 3.

    0

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    2 3 4 5 6Length in cm

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    No.

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    Figure 4. Comparison between body length of collected B. tadmorensis from the 3 study sites. Combined data from under-stone collecting and pitfall traps.

    Figure 5. Body length of collected B. tadmorensis from all the study sites using under-stone collecting and pitfall traps.

  • Ecology and biology of scorpions in Palmyra, Syria

    340

    Many species of vertebrates and invertebrates were reported to feed on scorpions. Polis et al. (1981) listed about 150 species that feed on scorpions. Among vertebrates, birds and lizards were the most signifi cant predators. Th ese studies indicated predation of scorpions by the desert monitors, Varanus sp. (Millot and Vachon, 1949; Cisse, 1972), the Common Kestrel, Falco tinnunculus, and the Woodchat Shrike Lanius senator, in Eurasia and Africa (Lourenco and Dekeyser, 1976). Th is study reports, for the fi rst time, predation by Acanthodactylus boskianus on B. tadmorensis. Ptyodactylus spp. was found to feed on scorpions both naturally and under laboratory conditions (Zlotkin et al., 2003). It seems that Acanthodactylus boskianus can tolerate the venom of B. tadmorensis, which is less potent for humans than L. quinquestriatus.

    Th e Little Owl and the Northern Bald Ibis also predated on this species. Owls were reported to feed on scorpions in the Middle East; pellets of the Desert Eagle Owl, Bubo ascalaphus were found to include remains of A. crassicauda, Compsobuthus werneri, and S. m. palmatus (Rifai et al., 2000). Shehab (2004) found that scorpions constituted 9.22% of prey items of the Eagle Owl in the Syrian Desert, while the Little Owl fed on other unidentifi ed scorpions (Obuch and Krištìn, 2004). Th e diet of other birds such as the Houbara Bustard (Chlamydotis macqueenii) included

    Buthacus yotvatensis nigroaculeatus and Vachoniolus spp. in Abu Dhabi (Tigar and Osborne, 2000). Vachon (1952) reported predation of scorpions by the Northern Bald Ibis, Geronticus eremta, in Southeastern Europe, Asia and Northern Africa.

    Scorpions will capture almost any prey that they can overcome. Th ey feed primarily on several groups of insects, arachnids, and other arthropods (Williams, 1987). Intraspecies predation was reported among many scorpion species in North America (Polis, 1979). We report here predation of L. quinquestriatus on B. tadmorensis and cannibalism among B. tadmorensis. Maternal cannibalism in B. tadmorensis was observed, although only in captivity.

    AcknowledgmentsWe would like to thank Professor Adel Safar,

    the Minister of Agriculture and Agrarian Reform, Engineer Ali Hamoud, the Director General of the General Commission of Al Badia Development and Management, and the General Commission for Scientifi c Agricultural Research for facilitating the fi eld work, and for their encouragement and continuous support. We also wish to express our gratitude to BirdLife International for supporting this study.

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