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Journal of Arid Environments Journal of Arid Environments 56 (2004) 303–327 www.elsevier.com/locate/jnlabr/yjare

Dung-insect communitycomposition in arid zones of south-eastern Spain

Francisco Sanchez! Pin˜ ero*, Jose M. Avila Departamento de Biolog!ıa y Ecolog!ıa, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain

Received 14 February2002; received in revised form 23 September 2002; accepted 2 April 2003

Abstract

Dung- communitycomposition was studied at three sites for 1 year,and for a further 8 months at one site, in an arid region of Spain. The insect communitywas dominated byants, dung flies and . Ants were abundant and flies relativelyscarce at all three sites, whereas diversityand abundance differed among sites and between years.Community composition varied along the year in species richness, abundance and biomass. Although dung-insect communities of arid Spain share some traits with dung-insect assemblages in other deserts, diversityand trophic structure of these communities are highlyvariable, a common but underappreciated feature of communities in arid regions. r 2003 Elsevier Ltd. All rights reserved.

Keywords: Desert; Dung-insect community; Inter-annual variability; Seasonality; Spain; Spatial variability

1. Introduction

Insects associated with dung form a highlydiverse communityincluding specialized coprophagous and predatoryspecies of beetles and flies, as well as an arrayof generalist consumers, which colonize feces during the different stages of decomposition (Koskela and Hanski, 1977; Hanski, 1987, pp. 837–884, 1990, pp. 127–145, 1991, pp. 5–21). The activityof these , speciallyscarab beetles, is crucial to dung decomposition (Anderson and Coe, 1974; Holter, 1977, 1982; Gitting et al., 1994) and therebysignificantlyenhances primaryproductivity( Bornemissza

*Corresponding author. Tel.: +34-958-242-309; fax: +34-958-243-238. E-mail address: [email protected] (F. Sanchez! Pin˜ ero).

0140-1963/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0140-1963(03)00057-0 ARTICLE IN PRESS

304 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 and Williams, 1970; Fincher et al., 1981; Rougon and Rougon, 1983; Ricou and Loiseau, 1984). Plant productivityis increased byintegration of nutrients into the soil (Guillard, 1967; Edwards and Aschenborn, 1987) and byseed burial, which provides adequate microclimates for germination and reduces the risk of seed predation (Estrada and Coates-Estrada, 1991). In addition, the beetles’ burrowing activities aerate and soften the soil (Brusaard, 1987; Herrick and Lal, 1996). Thus, dung insects are keyorganisms in systems with grazing mammalian herbivores, particularlyin nutrient poor systems such as deserts. Manyarid regions are used as rangelands for livestock. In shrubsteppes of the Mediterranean Basin livestock (principallysheep and goats) consume about 1500 kg/ ha/year (dry weight) of vegetal matter, producing ca. 600 kg/ha/year of dung (Le Houreou,! 1981, pp. 479–521). Although dung-associated fauna are potentiallyan important part of these ecosystems, dung insects have been scarcely studied in arid zones. Some studies have described dung-beetle assemblages (Nealis, 1977; Rougon and Rougon, 1980, 1981, 1982a–c, 1983; Dajoz, 1994) and the role of termites during late stages of dung decomposition (Havertyand Nutting, 1975 ; Johnson and Whitford, 1975; Kingston, 1977; Whitford et al., 1982; Rougon and Rougon, 1991; Whitford, 1991). However, the composition and structure of entire dung-insect communities have been investigated onlyin the Chihuahuan desert ( Schoenly, 1983) and the Sahelian region (Rougon and Rougon, 1991). These studies show the diversityof insects that exploit dung but few general patterns emerge: whereas the most abundant insects exploiting dung in the Chihuahuan Desert are ants (although scarabaeids and tenebrionids were still the most important dung consumers), beetles (principallystaphylinid and scarabaeoid beetles) are the dominant species in dung communities in Sahel. Schoenly(1983) and Rougon and Rougon (1991) described dung-insect communities at single sites and over a period of a few months to 1 year. Neither studyaddressed among site, inter-annual or seasonal variabilityin community composition and structure, which are crucial to the understanding of desert communities (Polis, 1991, pp. 1–26; Sanchez-Pin! ˜ ero, 1997). The present study analysed the structure of dung-insect communities in three sites and 2 years (at one site) in an arid region of south-eastern Spain. The goals of this studywere to: (1) describe the taxonomic and trophic composition of the community; and (2) analyse the spatial, inter-annual and seasonal variabilityin communitystructure (taxonomic and trophic composition, abundance and biomass).

2. Study area

The studywas conducted at Barranco del Espartal (750 m elevation, hereafter Baza), Rambla del Grao (900 m, hereafter Grao) and Llanos de Guadix (1100 m, hereafter Llanos), located 10–40 km apart in the Guadix–Baza Basin (Granada Province, SE Spain). The three sites had similar grazing pressures (ca. 1.4–1.6 sheep/ ha). Sites included the characteristic landscapes of these arid zones: ramblas (occasional watercourses) with a substrate composed of silt and gypsum sediments ARTICLE IN PRESS

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(Baza) or sandyclaysoils (Grao); and the plateau, with a substrate composed of limestone plates and claysoil (Llanos). The climate is Mediterranean continental and highlyseasonal, with strong dailyand seasonal temperature fluctuations. Tempera- tures are usuallybetween zero and 14C in winter (October–April), and reach 60C at ground level in summer (Epypsa, 1985). Temperature records from the two main towns in the area (Guadix and Baza, 6–10 km to the studysites) showed that similar seasonal trends occur across the studyarea (maximum temperature: r ¼ 0:981; p ¼ 0:0001; minimum temperature: r ¼ 0:988; p ¼ 0:0001; n ¼ 36; Pearson’s correlation; Fig. 1). Precipitation is irregular and occurs mainlyduring the cold months. During the studyperiod, annual rainfall was lower in 1991 (227.3 mm) than in 1992 (304.9 mm), showing a similar seasonal distribution pattern across the studyarea

100 (A) 90 1990 1991 1992 80 Precipitation 70 T Max T min 60 50 40 30 20 10 0 -10 J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D 100 (B) 90 80 Precipitation/Temperature 70 60 50 40 30 20 10 0 -10 J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D Month

Fig. 1. Monthlymean maximum ( TMax) and minimum (Tmin) temperature ( C) and total amount of precipitation (mm) at the two main towns of the studyarea (A=Baza, B=Guadix) during 1990–1992. ARTICLE IN PRESS

306 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327

(r ¼ 0:783; p ¼ 0:0001; n ¼ 36; Fig. 1). The potential evapo-transpiration exceeds annual rainfall bythree times ( Sierra et al., 1990). The studyarea corresponds to a middle arid system (Le Houreou,! 1989). The vegetation consists of savannas with holm– trees (4% cover), grasses (30% cover) and Artemisia shrubs (12% cover) at Llanos, and typical arid open shrubsteppes (46–54% bare soil, 12–17% shrub cover) dominated by Artemisia (Compositae) and Salsola (Chenopodiaceae) shrubs, Stipa (Gramineae) tussock grasses and Retama sphaerocarpa (L.) Boissier (Fabaceae) brushes at Baza and Grao.

3. Methods

We used dung-baited pitfall traps to studythe fauna associated with excrements (see Southwood, 1978; Lobo et al., 1988). Traps consisted of a plastic cylinder (10 cm diameter  20 cm high) buried in the ground and containing a collecting cup (6.5 cm diameter  9 cm high) with a preservative (a solution of 10 g/l cloral hydrate and soap). A funnel on top of the cylinder was connected to the collecting cup in the interior of the cylinder. A baited grill (2.5  2.5 cm mesh) rested on the funnel. Bait was fresh sheep dung (200 g) collected in a sheep stockyard at Barranco del Espartal. We carried out sampling from March 1991 to February1992 at the three sites. We were also interested in inter-annual variation in dung arthropod assemblages, so we carried out additional sampling in Baza from March 1992 to October 1992. We established five pitfall traps at each site. Pitfall traps were baited with fresh dung at 15-dayintervals. Contents of the pitfall traps were collected at 2 and 15 daysafter baiting. After 15 days, due to the dry conditions in the zone, dung was completely dried and was no longer attractive to insects, but five drydung-pats were left on the ground in each site to examine for termite activity. We have classified insects into five trophic groups: predators, opportunistic predators, coprophages, opportunistic coprophages and omnivores. Predators (histerid and staphylinid beetles; Appendix A) eat only live prey, whereas coprophages (dipteran larvae and scarabeid, aphodiid, hydrophylid beetles) eat (exclusivelyor principally)dung. Omnivores (Formicidae) feed both on live preyand dung. Opportunists appear in dung as predators or coprophages, but are not restricted to excrement (e.g., carabid, tenebrionid, and some staphylinid and aphodiid beetles; Appendix A). Classification of species into trophic groups was based on direct observations in the studyarea and literature (e.g., Koskela and Hanski, 1977; Schoenly, 1983; Cambefort, 1991, pp. 156–178). Biomass was estimated from bodylength (0.01 mm accuracy)using allometric equations calculated from specimens from the studyarea ( Hodar,! 1996).

3.1. Statistical analysis

To analyse species turnover between sites and years, beetles were identified to species level (Appendix A). Alpha species diversitywas calculated using Shannon H 0 ARTICLE IN PRESS

F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 307 index of evenness, and differences in diversityvalues were compared using a t-test (Magurran, 1988). Species turnover (Beta diversity) was calculated using the Sorensen index (presence/absence of species) and Morisita–Horn index (which considers species abundance) (Magurran, 1988). To test whether frequencydistribution of species richness, abundance and biomass differed among sites or between years, we used a chi-square or G-test (Sokal and Rohlf, 1995). To compare differences in abundance and biomass, a Welch or Snedecor analysis of variance test was utilized depending on whether variances were unequal or equal, respectively. Data were log-transformed prior to analysis (Zar, 1984). We used Spearman rank correlation to compare seasonal variations between sites and between years. In this approach, phenologies will be similar if we can reject (po0:05) the null hypothesis that correlations do not exist between the given sequences (Siegel and Castellan, 1988). Throughout the text, results are shown as means71 S.D.

4. Results

A total of 29,347 individuals belonging to 12 orders of were collected in the dung-baited traps at the three sites and over the 2 years of the study. The most abundant orders were Coleoptera (60% of individuals), Hymenoptera (Formicidae accounted for 34% of individuals) and Diptera (5.6% mainlylarvae). Other arthropods collected included Scorpionida, Solifugae, Araneae, Isopoda, Diplopoda, Orthoptera, Embioptera, Dictyoptera, and Dermaptera, but they contributed only for 1.1–1.7% of total abundance (Table 1). No termites were found in dung during this study. Analyses were carried out with the three dominant taxa: Coleoptera, Formicidae and Diptera. The beetle assemblage was verydiverse, including 135 species from nine families (Appendix A). The beetle families with the highest number of species were Staphylinidae (34 spp.), Aphodiidae (28 spp.) and Tenebrionidae (23 spp.), while Aphodiidae (32.3% of the beetles), Staphylinidae (32.0%) and (21.1%) were the most abundant families (Table 1). In contrast, onlyfive ant species ( Messor bouvieri Bondroit, Cataglyphis iberica Emery, Camponotus cruentatus (Latreille), Pheidole pallidula (Nylander), and Monomorium sp.) were collected. Frequencydistribution of species abundances ( Fig. 2) showed that most species (40.3%) were rare (i.e., mean abundance o1 individual/trap). This pattern was consistent for both beetle species using dung as a resource (i.e. coprophages and opportunistic coprophages) and predators (w2 ¼ 8:53; p ¼ 0:49; df: ¼ 9; Fig. 2). The frequencydistribution of abundances did not differ significantlyamong the three sites for either coprophages (w2 ¼ 12:08; p ¼ 0:84; df: ¼ 18) or predators (w2 ¼ 19:91; p ¼ 0:13; df: ¼ 14). The three sites showed similar low numbers of Diptera and high numbers of ants (Table 1), but the patterns of composition of the dung-insect communitydiffered ARTICLE IN PRESS

308 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 0.28 0.013 N.S. 2.29 7.08** 16.90284.78 1.26 N.S. 0.00 N.S. 2.452.39 1.62 N.S. 7.40** 0.433.97 0.03 N.S. 4.01* 25.40 3.03 N.S. 0.11 — 13.19 2.02 N.S. 7 7 7 7 7 7 7 7 7 7 7 S.D.) Snedecor/Welch test 7 0.33 0.09 1.89 1.28 29.0533.13 11.61 102.64 2.500.81 1.30 1.15 0.5528.67 0.12 0.22 2.48 0 — 40.18 11.24 0.11 0.01 14.93 4.46 7 7 7 7 7 7 7 7 7 7 7 7 : 001 : 0 o p 9.89***4.11* 0.09 0.57 16.76***24.21***11.86***12.57*** 14.14 18.55 1.65 0.34 ; 01 a c b : c b a 0 o p 24.08 17.20 1.16 3.17 2.09 29.59 1.4340.98 1.85 N.S.1.87 0.40 N.S. 2.12 N.S. 0.15 9.88 0.05 40.08 2.83 M.S. 19.10 0.86 1.79 N.S. 0.01 7.94 2.60 N.S. 5.51 7 7 7 7 7 7 7 7 7 7 7 7 ; 9.05 5.15 0.35 0.78 0.70 05 : 14.34 0 o p b b a b a b 4.01 3.46 2.20 1.38 0.22 3.06 0.9181.52 0.32 0.22 8.77 0.34 131.22 10.09 0.13 0.13 11.16 2.39 7 7 7 7 7 7 7 7 7 7 7 7 S.D.) Snedecor/Welch test Abundance (Mean 1.94 1.60 1.01 0.58 0.04 0.95 7 a a a a a a 24.46 27.92 0.4623.79 0.23 15.24 0.18 0.03 33.95 30.56 2.17 0.68 0.09 0.02 12.43 2.79 0.27 1.89 7 7 7 7 7 7 7 7 7 7 7 7 Baza Grao Llanos 1991 1992 Scarabaeidae 9.31 AphodiidaeHydrophilidae 15.21 Staphylinidae 0.10 Anticidae 6.73 0.03 Formicidae 12.76 HisteridaeTenebrionidae 1.14 Ptinidae 0.23 0.01 Carabidae 0.06 Table 1 Abundance (mean number of individuals/trap) of2 taxa years collected (from in March dung-baited traps to at October Baza, 1991 GraoTAXA and and Llanos 1992) from at March 1991 Baza to February1992 and in the Abundance (Mean Coleoptera Hymenoptera N.S.=not significant; M.S.=marginallysignificant; Means on one row sharing the same superscript were not significantlydifferent. Diptera 3.71 Other Arthropods 0.57 ARTICLE IN PRESS

F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 309

Fig. 2. Abundance (log mean number of individuals/trap) distribution of opportunistic and dung- specialized coprophagous and predatorybeetle species at the Guadix–Baza Basin. among sites in most other traits. The abundance of Scarabaeidae, Aphodiidae, Histeridae, Tenebrionidae and Carabidae differed significantlyamong the three sites (Table 1). These differences lead to variation in frequencydistribution of the taxa among sites (w2 ¼ 90:29; po0:0001; df: ¼ 22). This difference was probablydue to the different frequencydistribution of abundance of the diverse taxa in Grao with respect to both Baza (w2 ¼ 56:36; po0:0001; df: ¼ 7) and Llanos (w2 ¼ 65:63; po0:0001; df: ¼ 11), principallybecause of verylow abundance and relative low frequencyof Aphodiidae and Scarabaeidae at Grao. This led to an increase in relative frequencyof Formicidae and Staphylinidaeat this site ( Table 1); no significant differences occurred between Baza and Llanos (w2 ¼ 13:71; p ¼ 0:19; df: ¼ 10). The beetle assemblages also varied among sites in species richness and species composition. First, species richness differed among sites (Welch’s F ¼ 12:05; ARTICLE IN PRESS

310 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 po0:0001; df: ¼ 2; 230:97), with Baza having a significantlyhigher number of species/trap (3.7973.60) than Llanos (3.3574.37) and Grao (2.3374.37). The differences in species richness and abundance led to differences in diversity among sites: Grao was less diverse (H0 ¼ 1:52) than Llanos (H0 ¼ 2:76; t ¼ 28:39; df: ¼ 6641; po0:001) and Baza (H0 ¼ 2:56; t ¼ 23:56; df: ¼ 3984; po0:001), whereas Llanos was more diverse than Baza (t ¼ 6:81; df: ¼ 8519; po0:001). Second, species turnover between sites (Baza vs. Grao=0.49; Baza vs. Llanos=0.52; Grao vs. Llanos=0.54; Sorensen indices) was veryhigh (about 50%). Only26 species (19.3% of the total number of species) occurred in the three sites, whereas 63 species (46.7%) were collected in onlyone out of the three studysites (Appendix A). Similaritybetween assemblages was even lower when species abundance was considered (Morisita–Horn index): Grao showed the lowest similarityvalues with both Llanos (0.38) and Baza (0.43). Although Baza and Llanos showed a higher similarity(0.58), species turnover was still relativelyhigh. Indeed, some dominant species (e.g., ion and lemur) were unique to particular sites, and species occurring in two or the three sites differed significantlyin abundance between these sites (e.g., Onthophagus merdarius, tersus, A. distinctus, A. baeticus and Saprinus georgicus).

4.1. Trophic structure

Most of the beetle species were coprophages (67), with more than twice the species richness than opportunistic coprophagous (32) or predatorybeetles (24) (see Appendix A). In contrast, opportunistic predaceous beetles (12 species) were represented bythe lowest number of species. Frequencydistribution of the number of species in each trophic guild did not differ significantly between sites (Baza vs. Grao: G ¼ 3:10; p ¼ 0:38; Baza vs. Llanos: G ¼ 6:70; p ¼ 0:10; Grao vs. Llanos: G ¼ 2:47; p ¼ 0:50; df: ¼ 3 in all cases; G-test). In general, the assemblage was dominated bycoprophages (43.3% of total abundance), omnivores (33.5%) and predators (21.2%), whereas opportunistic detritivores and opportunistic predators were scarce. However, the three sites differed in the abundance of coprophages, opportunistic predators and (at a marginallysignificant level) omnivores ( Table 2). These variations of abundance among different functional groups between sites led to assemblages with different trophic structures (Baza vs. Grao: G ¼ 2492:16; po0:001; Baza vs. Llanos: G ¼ 2845:13; po0:001; Llanos vs. Grao: G ¼ 207:24; po0:001; df: ¼ 4 for all cases; G-test). In terms of biomass, coprophages dominated all three assemblages, comprising 37.4–86.4% of the total biomass, although coprophages and opportunistic detritivores had similar biomass at Grao (Table 2). Frequencydistribution of biomass in the different trophic guilds differed among sites (Baza vs. Grao: G ¼ 1431:98; Baza vs. Llanos: G ¼ 550:18; Grao vs. Llanos: G ¼ 786:36; po0:0001; df: ¼ ARTICLE IN PRESS

F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 311 lanos M.S 11.88 3.94* 27.05 3.12 N.S. 282.682.37 0.11 N.S. 5.05 1.810.28 N.S. 5.65* 25.40 0.01 N.S. 3.03 N.S. 1468.58 0.99293.19 N.S. 3.77 52.77 1.21 N.S. 7 7 7 7 7 7 7 7 7 7 48.91 7.53 43.39 11.97 53.951.45 119.35 25.650.33 1.28 40.18 3.39 0.09 11.24 1025.29 954.43 133.92 138.58 7.53 11.71 S.D. Snedecor/Welch test 7 7 7 7 7 7 7 7 7 7 7 : 001 : 0 o p 3.69* 20.63 51.68***10.82*** 40.69 34.63*** 0.09 13.07*** 563.12 1.67 ; c c b a,c 01 : b 0 o 133.19 1.36 N.S. 19.32 3.18 34.23 68.87 67.41 531.24 3.2442.42 0.67 N.S. 0.4240.08 N.S. 2.83 M.S.147.15 0.79 10.21 1.53 N.S. 19.10 47.66 p 7 7 7 7 7 7 7 7 7 7 ; 0.80 8.61 05 31.70 17.23 : 226.64 0 o p b a,b b a a 20.05 0.22 2.30 151.37 36.62 144.63 121.83 1.5179.57131.42 1.11 11.12 10.09 121.99 41.99 7 7 7 7 7 7 7 7 7 7 7.60 0.03 0.25 64.31 28.33 a a a a a 46.64 40.796.19 28.99 1.2321.400.27 0.70 15.71 33.95 30.56 868.39 110.75 49.95 36.67 S.D. Snedecor/Welch test Mean 7 7 7 7 7 7 7 7 7 7 7 Baza Grao Llanos 1991 1992 Abundance Coprophages 29.82 Opp. predators 1.11 Table 2 Abundance (mean number of individuals/trap) and biomass (mg/trap) of the different trophic groups collected in dung-baited traps at Baza, Grao and L Predators 13.29 from March 1991 to February1992, and inTrophic the guild 2 (from years March to October 1991 and 1992) at Mean Baza N.S.=not significant; M.S.=marginallysignificant; Opp. coprophagesPredators 0.54 Opp. predatorsOmnivores 0.06 Biomass 6.99 Coprophages 12.76 Opp. coprophages 31.37 380.16 Omnivores 13.78 Means on one row sharing the same superscript were not significantlydifferent. ARTICLE IN PRESS

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4 for all cases; G-test). As in the case of abundance, biomass of coprophages differed among the three sites, opportunistic predators had significantlyhigher biomass at Llanos, and omnivores had a higher biomass at Baza than at Llanos (Tukey–Kramer test).

4.2. Inter-annual variability

Number of species was higher in 1991 (72 species, 4.973.95 species/sample) than 1992 (61 species, 2.5072.74 species/sample) (F ¼ 28:14; po0:0001; df: ¼ 1; 155; ANOVA) (Appendix A). This decrease in species richness and the nearly10-fold increase in the abundance of Aphodius baeticus in 1992 produced a noticeable decrease of diversityin 1992 ( H0 ¼ 1:00) with respect to 1991 (H0 ¼ 2:49; t ¼ 55:95; df: ¼ 8709; po0:001). Similarityin species composition between yearswas relativelyhigh (Sorensen index=0.82). However, a high species turnover occurred between years when the abundance of species is considered (Morisita–Horn index=0.54); even though, only six species showed significant differences in abundance between both years (Appendix A). There were also between year differences in assemblage structure (w2 ¼ 50:87; po0:0001; df: ¼ 8; chi-square test): tenebrionids and other arthropods increased, and staphylinids decreased significantly in 1992 compared to 1991 (Table 1). Trophic structure differed according to abundance (w2 ¼ 24:06; po0:0001; df: ¼ 3; chi-square test) but not biomass (w2 ¼ 4:32; p ¼ 0:36; df: ¼ 4; chi-square test). Onlypredator abundance differed significantlybetween years( Table 2); nevertheless, the significant differences in abundance of A. baeticus suggest that coprophages were actuallymore abundant in 1992 than 1991. In terms of biomass, there was an increase in abundance of coprophages (Aphodiidae) and opportunistic coprophages (Tenebrionidae) and a decrease in predators (staphylinid and histerid beetles). This indicates that differences in the biomass between years (Table 2) were due to the dominance of coprophages and the low biomass of predators and opportunistic predators.

4.3. Seasonal variability

The assemblages varied markedlyin number of species, abundance and biomass along the year, showing a sharp peak for the three descriptors during April (Fig. 3). Number of species was highest in spring, then declined at the beginn- ing of the summer, and remained low throughout the fall and winter (Fig. 3A). This pattern was similar in the three sites (rs > 0:72; po0:001; n ¼ 24 in all cases) and in the 2 years at Baza (1991 vs. 1992: rs ¼ 0:56; po0:01; n ¼ 16) (Fig. 3A). Seasonal variations of total abundance (Fig. 3B) were similar across the three sites (rs > 0:55; po0:01; n ¼ 24 in all cases). In general, maximum abundance occurred in spring and summer, with a considerable decrease after the summer, although smaller peaks also occurred in September and February(speciallymarked ARTICLE IN PRESS

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16

14

12

10 8

6

4

2 No. beetle species/trap 0 (A) Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb

450 400 350 300 250 200 150

No. insects/trap 100 50 0 (B) Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb

20000

17500

15000

12500 10000

7500

5000 Biomass (mg/trap) 2500

0 Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb (C) Month Fig. 3. Fortnightlyvariation patterns of: (A) species richness (mean number of species/trap); (B) abundance (mean number of individuals/trap); and (C) biomass (mg/trap) throughout March 1991– February1992. Mean values for the three sites during 1991/1992 are represented. at Baza and Llanos, respectively). Most taxa showed a pattern of maximum spring abundance (rs > 0:38; po0:02; n ¼ 40 in all cases), and onlyFormicidae (which caused the peaks of abundance observed in Julyand August) and Aphodiidae (with ARTICLE IN PRESS

314 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 peaks in spring, autumn and winter) showed different seasonal patterns of abundance. Biomass variations along the year showed a similar pattern at the three sites (rs > 0:60; po0:005; n ¼ 24 in all cases), with a marked peak during April and a considerable decrease during and after the summer (Fig. 3C). Communitycomposition varied markedlyin the frequencydistribution of abundance of different taxa (Fig. 4) and biomass of trophic groups (Fig. 5) among seasons in the three sites (w2 > 18:7; po0:001; df: ¼ 15 in all cases). In terms of abundance, during the spring Baza showed a higher proportion of ants, while Grao showed a lower proportion of scarabs and higher proportion of Staphylinids, and Llanos had a higher proportion of Histers. Summer showed a similar trend of ant dominance at the three sites. Autumn and winter differed between Grao (with a relativelyhigh proportion of staphylinids and ants) and the other two sites (dominated byaphodiid beetles). Differences among sites in the proportion of the biomass corresponding to each trophic group in different seasons were also very marked (Fig. 5). Seasonal variations of abundance differed between 1991 and 1992 (rs ¼ 0:43; p ¼ 0:09; n ¼ 16) because of the existence of a longer and lower spring biomass peak and the occurrence of a larger peak in the biomass of coprophages during the autumn (due to A. baeticus activity). Nevertheless, a similar trend of spring and autumn peaks of biomass occurred in both years (1991 vs. 1992: rs ¼ 0:51; po0:05; n ¼ 16).

5. Discussion

5.1. Spatial and temporal patterns in the Guadix–Baza Basin

The dung-insect communities at the arid Guadix–Baza Basin consisted of a diverse assemblage of coprophagous and predatorybeetles, a relativelyhigh abundance of ants and a low abundance of diptera. A striking characteristic of these communities is their variabilityin diversity,abundance of different taxa and trophic structure among the three study sites, between years and seasonally. Species composition and diversityof beetles (both species richness and evenness) varied, with a high (ca. 50%) species turnover between sites. This high species turnover resulted from the extreme site-specificityof most beetle species (47% of the beetle species occurred exclusivelyat one site, in contrast to only19% of the beetle species common to the three sites), as well as differences in relative abundance of common species among sites. Differences in communitycomposition and abundance of dung insects among sites maybe related to variations in abiotic and biotic factors such as soil characteristics (Fincher, 1973; Hanski and Cambefort, 1991a, pp. 331–349; Sowig, 1995), vegetation (Doube, 1987, pp. 253–280; Lumaret and Kirk, 1987) and predation (Kingston, 1977; see in addition Doube, 1991, pp. 133–155). Spatial heterogeneityat several scales of the above factors is a common trait in deserts ARTICLE IN PRESS

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Fig. 4. Seasonal variations in the percentage of abundance represented bythe dominant taxa at the three studysites from March 1991 to February1992. ARTICLE IN PRESS

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Fig. 5. Seasonal variations in the percentage of biomass corresponding to the different trophic groups at the three studysites from March 1991 to February1992. ARTICLE IN PRESS

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(Polis, 1991), and therefore differences in diversity, abundance of different taxa, and trophic structure (both in terms of abundance and biomass) among sites also occur, especiallyfor communities exploiting ephemeral and patchyresources such as dung and carrion (Sanchez-Pin! ˜ ero, 1997). The strong seasonalityin the region produced similar seasonal trends in terms of species richness, total abundance and total biomass among sites, although the composition of the assemblages in each season (as the proportion of abundance of diverse taxa and the biomass of different trophic groups) varied markedlyamong sites. Variations in abundance and biomass, specially, show the sharp pulsed activity of insects in the area, most activitybeing restricted to veryshort periods in spring, summer and (at Baza and Llanos) earlyfall and winter. Seasonal variations in communitycomposition are related to changes in temperature and humiditythat affect activityand development (Landin, 1961; Hanski and Cambefort, 1991a). Differences in seasonal variations of abundance between years at Baza may reflect the effect of weather conditions, and the nine-fold increase in abundance of A. baeticus in 1992 was probablyrelated to the summer rainfall at Baza that year. However, seasonal variations of dung- insect populations also probablyreflect seasonal variabilityin availabilityand qualityof food resources ( Hughes and Walker, 1970, pp. 255–269; Kingston, 1977; Tyndale-Biscoe et al., 1981; Macqueen et al., 1986; Ridsdill-Smith, 1986). Plant growth (i.e., available grazing) occurs mainlyduring the spring at the study area, and dung qualityis highest during this period of the year( Gomez-Guti! errez! et al., 1979). In contrast, elevational migrations of livestock and wild ruminants make dung a scarce resource during the summer in the area. All of these factors are probablyresponsible for the general decrease in dung-beetle activity during the dryseason in tropical, sub-tropical and Mediterranean systems (Kingston, 1977; Hanski and Cambefort, 1991a and references therein). Thus, the seasonal patterns observed on all three sites (Fig. 3) mayreflect a similar combination of regional weather and variabilityin resource availabilitythroughout the Guadix–Baza Basin. In addition, species abundance and communitycomposition varied between years at the Baza site. Species richness was 15% lower in 1992 than in 1991, and differences in relative abundances reduced the similarityof beetle assemblages between yearsto 54%. This reduction of similarityis a consequence of the fluctuations in abundance of different taxa (e.g., Staphylinidae, A. baeticus). Variations in abundance in excess of one order of magnitude between years have been reported in dung-beetle assemblages (e.g., Tyndale-Biscoe et al., 1981; Doube, 1987). Indeed, extreme inter- annual fluctuations in abundance are a general trait of desert biotas (e.g., Rickard, 1970; Thomas, 1979; Seelyand Louw, 1980 ; Sheldon and Rogers, 1984; Sanchez-! Pin˜ ero, 1994).

5.2. Comparison with other dung-insect assemblages

Variation in composition, abundance and trophic structure of the communities among sites and between years evidence the important effects of spatial ARTICLE IN PRESS

318 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 heterogeneityand temporal unpredictabilityof arid systemson community composition. However, despite this variability, the dung-insect communities of the Guadix–Baza Basin show similarities with dung-insect communities from other arid regions. The insect fauna of sheep dung in the Guadix–Baza Basin is diverse, and includes a high proportion of rare specialized and opportunistic coprophages and predators. Dung-insect communities of the Guadix–Baza Basin differ in this feature from those of other regions where most rare species are predators (Hanski, 1983, 1987). Interestingly, the number of opportunistic and rare predators in the dung communities differ from that in carrion, where predators included mostlyspecialized species of histerid beetles (Sanchez-Pin! ˜ ero, 1997). However, both dung and carrion communities in the Guadix–Baza Basin have a high proportion of rare detritivore species, which differentiates them from assemblages found in these resources in temperate and tropical systems (Hanski, 1983, 1987, 1990). This high number of rare species of coprophages and predators is increased bythe occurrence of opportunistic predator and detritivore beetle species, most of which appeared in low numbers in dung, thus increasing considerablythe number of rare species in the assemblage. Opportunists, however, were not always scarce, and ants were present in large numbers at the three sites. Opportunistic species were a significant component of the communities, representing 25–29% of the beetle species, 22–57% of the total abundance, and 10–46% of the biomass. Although there were differences in abundance of opportunists between sites and between years, ants and tenebrionids were important components of the dung community. Both taxa represented a substantial proportion of the abundance (especiallyants) and biomass (tenebrionids), and became more important during the summer, especiallyat Grao. The high abundance of ants and the large proportion of biomass represented bytene- brionids is also a feature of dung communities in the Chihuahuan Desert (Schoenly, 1983), which maysimplyreflect the dominance of both taxa in deserts (e.g., Cloudsley-Thompson and Chadwick, 1964; Crawford, 1981, 1991, pp. 89–112; Mackay, 1991, pp. 113–150; Sanchez-Pin! ˜ ero, 1994) and their omnivorous habits (Fiori, 1969; Rogers et al., 1988; Mackay, 1991; Heatwole, 1996). However, the Guadix–Baza Basin fauna lacked termites as dung decom- posers, even though this group plays a major role in dung decomposition in other desert systems (Ferrar and Watson, 1970; Havertyand Nutting, 1975 ; Johnson and Whitford, 1975; Kingston, 1977; Whitford et al., 1982; Whitford, 1991). Termites are onlyfound occasionallyin the roots of dead shrubs in the Guadix–Baza Basin (F. Sanchez-Pin! ˜ ero, pers. obs.). In addition to the relative importance of opportunists, specialized coprophages represented the highest proportion of the biomass (37.4–86.5%) of the dung-insect communities at the Guadix–Baza Basin. The abundance of specialized flies and beetles, also, show some common patterns of desert dung-insect communities. Dung specialists, including both coprophages and predators, characterize the dung-insect communities worldwide, although the relative abundance of the different taxa changes regionally( Hanski, 1991; Hanski and Cambefort, 1991b, pp. 350–365): ARTICLE IN PRESS

F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 319

Dung-insect communities in temperate systems are dominated by predatory beetles, and have fewer dung beetles and dung flies. In contrast, in African savannas scarabs outnumber predatorybeetles, and dipteran larvae occur in relativelylow abundance. The small proportion of abundance represented bydipterans in the three studysites of the Guadix–Baza Basin (4.6–7.4%) indicates that dung-insect communities of this region are more similar to those of arid African savannas and other arid regions (Schoenly, 1983; Rougon and Rougon, 1991). These authors suggest that high temperature and, hence, rapid desiccation of dung, mayprevent dipteran larvae from being abundant in desert environments. In the Guadix–Baza Basin, for example, sheep dung loses >45% of its water-content in o24 h during the spring (Gonzalez-Meg! !ıas and Sanchez-Pin! ˜ ero, 2003). Dung desiccation imposes a strong constraint on larval development of flies but predatorybeetles and scarab competitors mayalso contribute to low populations of dung-dipteran larvae in the Guadix–Baza Basin, as in other dung communities elsewhere (e.g., Summerlin et al., 1982, 1984; Hanski and Cambefort, 1991b; Hanski, 1991and references therein; Ridsdill-Smith, 1993). Specialist coprophagous and predatorybeetles are found in dung communities all over the world (notably scarabs, hydrophilids, staphylinids and histerids). In the Guadix–Baza Basin, scarabs (Scarabaeidae and Aphodiidae) are the dominant coprophages, whereas hydophilids are scarce (0.2–0.5% of total abundance). Hydrophilids tend to be rare in other arid regions (Schoenly, 1983; Cambefort, 1991; Rougon and Rougon, 1991; Dajoz, 1994), compared to temperate and mesic Mediterranean systems, where hydrophilids represent 13–25% of all insects in dung (Finne! and Desiere," 1971; Hanski and Koskela, 1977; Lobo, 1992). Staphylinids are the dominant predatory beetles in the Guadix–Baza Basin, in contrast to their general scarcityin deserts ( Crawford, 1981; Wallwork, 1982; Schoenly, 1983; Schoenlyand Reid, 1983 ; Dajoz, 1994; Sanchez-Pin! ˜ ero, 1997), although theyoccur locallyin large numbers ( Crawford, 1988), and are the dominant dung insects (39% of the abundance) in the Sahelian region. The relative abundance of coprophagous and predatorybeetles varied among sites and between years at the Guadix–Baza Basin. The abundance of copro- phagous beetles differed among sites, principallybecause of the low numbers of scarabs at Grao. In addition, scarabs were more abundant in 1992 because of the increase of a single species, A. baeticus. Predators did not differ among sites (in spite of the higher abundance of Histeridae at Llanos), although differences were significant between years (staphylinid abundance decreased 4 times in 1992 compared to 1991). These variations resulted in a much lower proportion of the abundance of coprophagous insects at Grao. Similarly, at Baza the decrease of staphylinid abundance and the increase of A. baeticus in 1992, enlarged the dominance of coprophages during 1992 (although the general pattern of dominance of coprophages and low opportunistic predator abundance was common for the 2 years). In summary, some general patterns can be established for the dung-insect communities in the Guadix–Baza Basin: (a) there are numerous rare coprophagous ARTICLE IN PRESS

320 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 species; (b) coprophagous beetles dominate the system in terms of biomass, but the relative importance of biomass and abundance varied widelyamong sites and years; (c) diptera are relatively scarce; and (d) ants and opportunistic coprophages are relativelyimportant but termites are effectivelyabsent as dung decomposers. Despite the general patterns indicated above, one of the most noteworthy traits of dung-insect communities is their inherent variability, at local and regional scales. Communities in the studyarea differed in species composition, abundance and biomass, both taxonomicallyand among trophic groups. Temporal variabilityis shown bythe striking seasonalityand the inter-annual differences among the communities. This high variability, caused by the extreme conditions of desert habitats, affects communitytraits, from species composition to trophic structure (Polis, 1991). Variation in ecological as well as historical factors contribute to regional divergence in community composition and processes (e.g., Mares and Rosenzweig, 1978; Orians and Paine, 1983, pp. 431–458; Kerleyand Whitford, 1994 ; Valone et al., 1994). However, this variabilitymust be taken into account when establishing sampling procedures to detect communitypatterns, and when performing regional comparisons among communities, since a single location (or season) maymisrepresent a regional pattern, and differences in communitystructure among regional assemblages mayreflect local conditions rather than regional differences.

Acknowledgements

We are particularlygrateful to J.A. H odar,! J.M. Gomez! and J. Aguirre for their help with the field work and comments on earlydrafts of the manuscript. J.L. Ruiz also provided enthusiastic assistance in the field and with the identific- ation of scarab beetles. April Boulton, Paul Stapp and Barbara Tigar provided useful comments. Voucher specimens were kindlyidentified byseveral specialists: E. Romero-Alcaraz (Hydrophilidae), R. Outerelo (Staphylinidae), T. Yelamos! and J. de Ferrer (Histeridae), J. Mateu (Carabidae), S. Vin˜ olas (Tenebrionidae) and J.A. Tinaut (Formicidae). This work was funded bya FPI grant (PN89-52300837) from the Spanish Ministerio de Educacion! yCiencia to FSP.

Appendix A

List of beetle species, trophic group and total number of specimens collected at the three studysites and the two different years(1991 and 1992) sampled at Baza. Letters behind the numbers show sites/years with statistically significant (po0:05) mean number of beetles/trap. See Table 3. ARTICLE IN PRESS

F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327 321

Table 3

Species Trophic Sites Years

Guild Baza Grao Llanos 1991 1992

SCARABAEIDAE Scarabaeus sacer L. C 3 4 3 11 Scarabaeus typhon Fischer C — — 1 — — Scarabaeus puncticollis Latr. C 7 — — 7 9 Gymnopleurus flagellatus (F.) C — — 8 — — Onitis ion (Ol.) C 265 — — 265 217 bubalus (Ol.) C 1 — 3 1 1 Euoniticellus fulvus (Goeze) C 3 1 — 3 2 Euoniticellus pallipes (F.) C 9 1 — 9 5 Euonthophagus amyntas (Ol.) C — 2 6 — — Euonthophagus gibbosus (Scriba) C — — 3 — — Onthophagus merdarius Chevr. C 591a 98b 477a 591 469 Onthophagus vacca (L.) C 70 41 72 70 79 Onthophagus lemur (F.) C — — 277 — — Onthophagus similis (Scribra) C — — 2 — — Onthophagus taurus (Schreber) C 3 — — 3 10 Onthophagus emarginatus Muls. C — — 7 — — Onthophagus furcatus (F.) C 86a 83a 249b 86 55 Onthophagus ruficapillus Brulle C 49a 2b 6b 49 72

APHODIIDAE Aphodius elevatus (Ol.) C — — 174 — — Aphodius nanus Fairm. C — — 2 — — Aphodius luridus (F.) C 16 24 68 16 14 Aphodius contaminatus (Herbst) C — — 1 — — Aphodius lineolatus Illiger C — 1 — — — Aphodius distinctus (Muller) C 331a 92b 1108c 68 70 Aphodius melanostictus Schmidt C — 19 58 — — Aphodius tingens Reitt. C 59a 1b 1b 23 28 Aphodius sphacelatus Panz. C — — 1 — — Aphodius baeticus Muls. C 869a —65b 869a 7807b Aphodius annamariae Baraud C — 6 5 — — Aphodius scrofa (F.) C 1 — — 1 1 Aphodius striatulus Waltl C 2 — — 2 9 Aphodius leucopterus Klug C 24 5 — 24a 91b Aphodius tersus Erich. C 217a 12b 102 217 101 Aphodius foetidus (F.) C 2 3 2 2 4 Aphodius fimetarius (L.) C — 1 3 — — Aphodius ictericus Balthasar C 193a 4b 2b 143a 25b Aphodius longispina Kust.. C 52a 5b 42a 52 42 Aphodius varians Duftsch. C — 1 — — — Aphodius granarius (L.) C 7 — — 5 7 Aphodius hyxos Petrovitz C — 13 38 — — Aphodius diecki Har. C 5 — — 5 — Aphodius bonnairei Reit. C 2 — 1 1 — Aphodius satellitius (Herbst) C — 1 — — — Aphodius merdarius (F.) C — 1 1 — — (Creutz.) O 12 7 6 12a 3b Rhyssemus algiricus Luc. O 1 — — 1 — ARTICLE IN PRESS

322 F. Sanchez! Pin˜ero, J.M. Avila / Journal of Arid Environments 56 (2004) 303–327

Table 3 (continued)

Species Trophic Sites Years

Guild Baza Grao Llanos 1991 1992

HISTERIDAE Saprinus politus (Brahm) P 22 17 38 20 6 Saprinus melas Kust.. P 1 — — 1 — Saprinus georgicus Marseul P 57a 73a 5b 57 41 Saprinus calatravensis Fuente P 1 — — 1 — Hister grandicollis Ill. OP — — 1 — — Margarinotus ignobilis (Marseul) P — — 1 — — Margarinotus binotatus (Erich.) P 26 — 514 26 38 Atholus bimaculatus (L.) P 4a 17b 1a 48 Atholus duodecimstriatus (Schrank) P 24 14 42 24 8 Hypocacculus metallescens (Erich.) P 1 — — 1 1 Hypocacculus praecox (Erich.) P 1 — — 1 2 Onthophilus globulosus (Ol.) P — — 6 — —

HYDROPHILIDAE Sphaeridium scarabaeoides L. C 8 13 10 8 9 Sphaeridium marginatum F. C — 9 7 — — Sphaeridium bipustulatum F. C — 1 1 — — Cercyon quisquilius L. C 3 3 10 3 1 Cercyon haemorrhoidalis F. C — 1 8 — — Cercyon sp.— C1121—

STAPHYLINIDAE Anotylus inustus (Grav.) O 17 — 26 16 6 Anotylus sculpturatus (Grav.) C — — 1 — — Medon apicalis (Kr.) C — 1 — — — Phacophallus parumpunctatus (Gyll.) P — — 1 — — Leptacinus othioides (Baudi) P 2 2 — 2 1 Leptacinus faunus Coiff. P 1 — — 1 — Gyrohypnus fracticornis (Mull.). P 11 — 31 11 3 Gabrius nigritulus (Grav.) P 1 — — 1 — Philontus ochropus P 685 1758 662 685a 162b Philontus fenestratus (Fauv.) P — 1 — — — Philontus intermedius (Boisd. Lac.) P — 4 8 — — Philontus laeviusculus (Grav.) P — — 5 — — Philontus varians (Payk.) P 1 — — 1 1 ophthalmicus (Scop.) OP — — 1 — — Quedius semiobscurus (Marsh.) P — — 4 — — Tachynus flavolimbatus Pand. P — — 5 — — Tachyporus nitidulus (Fauv.) P — — 1 — — Leucoparyphus silphoides (L.) OP — — 4 — — Aleochara bipustulata (L.) C 32 26 22 32 8 Aleochara brundini Bernh. C — 1 1 — — Aleochara moesta Grav. C 22 25 24 22 7 Aleochara tristis Grav. C 1 4 11 1 — Aleochara crassa Baudi C — — 1 — — Aleochara maculata Brisout C 10 — 1 10 4 Aleochara laeviegata Gyll. C — — 2 — — Aleochara spissicornis Erich. C 2 1 — 2 1 Tinotus morion (Grav.) C — 2 — — — Atheta sordida (Marsh.) C 7 4 2 7 2 ARTICLE IN PRESS

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Table 3 (continued)

Species Trophic Sites Years

Guild Baza Grao Llanos 1991 1992

Atheta amicula (Steph.) O 1 — 1 1 — Atheta steineri Scheerp. C 5 — 210 5 1 Atheta nigra Kr. C — — 13 — — Dimetrota atramentaria (Gyll.) C 8 — 17 8 2 Acronota aterrima (Grav.) C — — 2 — — Oxypoda annularis (Mannh.) O — — 1 — —

TENEBRIONIDAE Pimelia integra Sol. O 14 20 — 14a 59b Pimelia monticola Rosenh. O 1 — 3 1 5 Pimelia brevicollis Sol. O — 7 — — — Tentyria incerta Sol. O 1 — 30 1a 8b Tentyriria platyceps Stev. O — 23 — — — Sepidium bidentatum Sol. O — — — — 19 Erodius parvus Sol. O — 11 — — — Morica hybrida Charp. O 1 — — 1 11 Akis discoidea Quens. O 2 — 3 2 — Asida cincta Rosenh. O — — — — 1 Elongasida rectipennis (Esc.) O 1 — — 1 2 clementei P-A. O — — — — 1 Dichillus subcostatus Sol. O — 1 — — — Blaps waltli Seidl. O 1 — — 1 — Blaps lusitanica Herbst O — 1 2 — — Scaurus punctatus F. O 1 1 3 1 2 Scaurus rugulosus Sol. O 4 1 — 4 1 Gonocephalum pusillum F. O — — — — 1 Phylan gibbulus (Motsch.) O — — — — 1 Anemia sardoa Gene O 1 — — 1 — Anemia submetallica Raffr. O 1 — — 1 — Crypticus gibbulus Quens. O — 6 — — — Pseudoseriscius adspersus Kust.. O 1 — — 1 —

CARABIDAE Carabus lusitanicus F. OP — — — — 3 Orthomus barbarus expansus Mateu OP 4 — 59 4 3 Calathus ambiguus Payk. OP — — 18 — — Parophonus hirsutulus Dej. OP — 1 — — — Prystonichus baeticus Rambur OP — — 1 — — Ditomus capito (Serv.) O 1 — — 1 — Acinopus picipes (Ol.) O — — 2 — 1 Cymindis lineola Dufts. OP — 2 3 — — Lampryas cyanocephalus (L.) OP — 1 — — — Syntomus fuscomaculatus Mostch. OP 2 — 5 2 — Microlestes luctuosus Holdh. OP — — 1 — — Amara metallescens Zimm. O — — 2 — —

PTINIDAE Ptinus fur L. O 1 2 16 1 1

ANTHICIDAE Anthicus sp. O 4 4 40 4 — ARTICLE IN PRESS

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