J Conserv (2006) 10:323–333 DOI 10.1007/s10841-006-9006-0

ORIGINAL PAPER

The importance of monkey (: Hopliini) pollination for Aizoaceae and in grazed and ungrazed areas at Paulshoek, , South Africa

Carolin Mayer Æ Geoffrey Soka Æ Mike Picker

Received: 7 October 2005 / Accepted: 21 March 2006 / Published online: 17 October 2006 Springer Science+Business Media, Inc. 2006

Abstract The relative importance of monkey bee- Keywords Hopliini Æ Beetle pollination Æ load Æ tles (Hopliini, Scarabeidae) as pollinators of Aster- Livestock grazing Æ Colour preferences aceae and Aizoaceae in the Succulent Karoo as well as the influence of livestock grazing on their abun- dance and diversity was investigated. Hopliine bee- Introduction tles proved to be the, or among the, most abundant flower visitors of 12 investigated species. In the semi-arid Succulent Karoo and biomes However, during single flower observations at three of the Western and Northern Cape Provinces of South Aizoaceae species, bees (Apoidea), bee flies Africa, monkey (Scarabaeidae, Hopliini) are (Bombyliidae) and pollen wasps (Masaridae) were one of the most important pollinator guilds (White- the most frequent flower visitors. However, monkey head et al. 1987; Picker and Midgley 1996; Goldblatt beetles carried the highest Asteraceae and Aizoa- et al. 1998; Colville et al. 2002) pollinating a diverse ceae pollen loads, and are therefore considered to number of unrelated annuals and perennials. These play a vital role in the pollination of these two biomes contain the majority of the world’s monkey families. Abundance, species richness and diversity beetle species, having more than 700 described species of Hopliini did not appear to be heavily affected by (2/3 of the world fauna—(Steiner 1998; Vernon 1999; livestock grazing. Annual variation in the composi- Colville et al. 2002). In these biomes, the Hopliini are tion of monkey beetle populations was more dra- typically associated with the very speciose Aizoaceae matic. Still, some species showed higher abundances and Asteraceae, but relatively little is known about this on heavily grazed rangeland while others only oc- relationship (Picker and Midgley 1996). In addition to curred under low grazing pressure. It is presumed feeding on flowers, the beetles use the flowers as that changes in the composition of the vegetation, mating rendezvous sites which reinforces their role as especially the observed decrease of perennial pollinators (Goldblatt et al. 1998; Steiner 1998; John- in favour of annuals and geophytes (Todd and son and Midgley 2001). Unlike beetle pollinators in the Hoffman 1999) could in turn affect the composition tropics that generally rely on odour to locate flowers of monkey beetle assemblages. (Armstrong and Irvine 1990), hopliine beetles use vi- sual cues exclusively (Picker and Midgley 1996), and are attracted to bright colours even in the absence of food or odour (Steiner et al. 1994). The beetles are C. Mayer (&) Biocentre Klein Flottbek Botanical Garden, University of covered with hairs and scales, which are very effective Hamburg, Ohnhorststrasse 18, Hamburg 22609, Germany in trapping pollen grains (Goldblatt et al. 1998). e-mail: [email protected] However, in contrast to the fairly good host record data, little information is available on the pollen load G. Soka Æ M. Picker Department of Zoology, University of Cape Town, Cape capacity of monkey beetles and their relative impor- Town, South Africa tance as pollinators. The few studies that have

123 324 J Insect Conserv (2006) 10:323–333 examined pollination ecology of Aizoaceae and (heavily and continuously grazed), the second on Asteraceae in the Succulent Karoo suggest that the commercial rangeland. Since 1950, when the privately system is generalised (Struck 1992, 1994; Ihlenfeldt owned land was fenced (Rohde et al. 2003), it has only 1994) as one would expect, given the convergent floral been lightly grazed and the vegetation has recovered structure of many of the constituent flowers (especially well. The continuously high stocking rate on the com- the Asteraceae and Aizoaceae). Struck (1994) found munal rangeland had a clear impact on the vegetation, that Hymenoptera were the most frequent visitors on with a marked fence-line contrast evident. Aizoaceae and Asteraceae, followed by Diptera (bee The vegetation, typical of that of the Succulent flies) and Coleoptera (monkey beetles). Karoo, is dominated by dwarf shrub succulents, bulbs Within the greater context of global biodiversity, and annuals, with perennial grasses being rare (Struck habitat loss and fragmentation are the biggest prob- 1992). The study area receives 150–250 mm of rain lems for pollinators (Webb 1989; Donaldson et al. annually, most of which falls in winter (June– 2002; Nash et al. 2004). In the Succulent Karoo, over- August). The coefficient of variation in mean annual stocking of rangelands with resultant overgrazing of rainfall is 33% (Todd and Hoffman 1999). Studies habitats is often stated as the major negative impact on were carried out in the springs (August–October) of biodiversity and associated ecological processes, such 2002–2004. as pollination, seed dispersal, seed germination and nutrient dispersion (Davis and Heywood 1994; Dean Flower visitation by pollinators et al. 1995; Todd and Hoffman 1999). The perennial vegetation component decreases in favour of annuals In 2004, the pollination of 12 species, each of the most and geophytes (Allsopp 1999; Todd and Hoffman common and flowering Asteraceae and Aizoaceae 1999), and the reduced flower display of certain plant species was examined closely to determine the relative species could make degraded land less attractive to importance of monkey beetle pollinators for these two insect pollinators (Gess and Gess 1993; Mayer 2004). families. The species chosen for study were: Astera- Changes in plant species composition would also ceae—Chrysocoma ciliata L. (n = 6), incana reduce larval host plant availability (Kearns et al. (Thunb.) Kuntze (n =7), Senecio niveus (Thunb.) 1998). The reduced numbers of pollinators would Willd. (n = 9), Hirpicium alienatum (Thunb.) Druce result in lowered seed set, which in turn would also (n = 5), Tripteris sinuata DC. (n = 12) and Osteosper- affect recruitment and seed-eating , and thus mum spinescens Thunb. (n = 7), and Aizoaceae—Che- upset entire food chains (Kearns et al. 1998). Mayer iridopsis namaquensis N.E.Br. (n = 20), Cheiridopsis (2004) found significantly reduced numbers of flowers denticulata (Haw.) N.E.Br (n = 18), Ruschia goodiae and fruit set per individual plant for some Aizoaceae L. Bolus (n = 18), Conicosia elongata (Haw.) species on heavily grazed sites in the Paulshoek area of N.E.Br. (n = 9), Leipoldtia schultzei (Schltr. & Diels) central Namaqualand (the north-western part of the Friedrich (n = 16) and Lampranthus godmaniae L. Succulent Karoo). On the other hand hymenopteran Bolus (n = 6). diversity (especially that of bees and pollen wasps) was For each plant species, all flower visitors were col- not different across a gradient of grazing intensity lected directly from individual (tagged) plants at (Mayer 2005). hourly interval over a 4 day period. were pre- This study examines the relative importance of served in 70% ethanol in individual Eppendorf vials to monkey beetles as pollinators of Asteraceae and prevent cross contamination of pollen grains. Aizoaceae in the Succulent Karoo. Secondly, it inves- In 2003 and 2004, 10 min flower observations at tigated whether intensive livestock grazing had a neg- single flowers of different Aizoaceae species (Cheirid- ative impact on monkey beetle species richness, opsis denticulata, Ruschia goodiae and Ruschia viridi- diversity, and abundance. folia) were conducted on both study sites, recording number and (where possible) species of visiting insects.

Materials and methods Pollen analysis

Study site A pollen reference library (Moore and Webb 1978) was created for the 12 selected plant species. Pollen The present study was carried out at two sites in the from flowers and insects was processed and mounted vicinity of Paulshoek, Northern Cape Province (Todd on microscope slides essentially following the proce- and Hoffman 1999), one being situated on communal dure described by MacGillivray (1987), using Kaiser’s

123 J Insect Conserv (2006) 10:323–333 325 glycerine jelly to trap pollen grains (Hall and Hawes Beetles were also the most abundant flower visitors 1991). of Asteraceae (Table 1). In particular, Senecio niveus Also in 2004, colour preferences exhibited by monkey and Osteospermum spinescens were visited almost beetles were investigated with eight sets of transparent exclusively by a single species of Hopliini (comprising plastic water traps (tubs 8 ·6 · 7 cm), each set con- 95% of all visitors for both plant species, Table 1). tained one of each tub painted blue, yellow, orange, red, Bombyliidae, and, to a lesser extend Meloidae, pink and white. Four sets of six tubs (tubs spaced 25– Halictidae and Melyridae also visited the species of 30 cm apart) were placed at 50 m intervals on both the Asteraceae. Again, there was one exception with heavily and the lightly grazed site, approximately 1 km Hirpicium alienatum being mainly visited by Phalacri- away from the fence. To examine pollinator abundance dae (50%) and no monkey beetles. and diversity at the heavily and lightly grazed sites, three sets of colour traps filled with water were set out on each Pollen loads of Aizoaceae and Asteraceae side of the fence-line, at different distances (100, 400 and 1000 m) from the fence in the springs of 2002–2004. All the flower visitors carried appreciable pollen loads Each set comprised five pans (2 · 20 cm) of each colour except for Nitidulidae sp. 1 (Table 2). Some species (white and yellow, with additional blue and pink pans for carried more pollen than others. trials in 2002 and 2003, respectively), placed about 10 m For Aizoaceae, Apidae (i.e. Apis mellifera) carried apart along a transect line. In 2002, six sets of colour the highest amount of pollen followed by monkey traps were set out, in distances only up to 400 m from the beetles (Lepithrix sp. 1, Heterochelus detritus, Anis- fence line. When comparing numbers of individuals and ochelus inornatus and Kubousa sp.), Ceroctis karoo- species between the years, this double sampling effort ensis (Meloidae), as well as species of Bombyliidae, was adjusted by dividing the numbers that were caught Lycaenidae and different bees (Megachilidae, Antho- each day by two. Traps were set out every 2nd–4th day phoridae and Colletidae). When average pollen loads from August to October, resulting in 14 trapping days carried by the different families are considered, mon- for each of the 3 years. key beetles (Scarabaeidae, Hopliini) carried the high- est Asteraceae pollen loads (Table 2) followed by different bee species (Anthophoridae, Apidae and Results Halictidae) and bee flies (Bombyliidae) (Fig. 2).

Flower visitation rates and pollinator specificity Variation in pollen loads carried by monkey beetle species In total, 256 insects belonging to 40 species were col- lected from flowers in 2004 (Appendix 1). The most There was no significant difference (Kruskal–Wallis- speciose taxa were Scarabaeidae (Hopliini) (8 species) Test: H (7, N = 18) = 2.649, P = 0.916) in the mean and Bombyliidae (7 species), followed by Halictidae (4 pollen load carried by the 8 species of monkey beetles species) and Meloidae (3 species). sampled, although Platychelus sp., Heterochelus detri- For five of the six investigated Aizoaceae species, tus and Pachycnema flavolineata carried the highest monkey beetles were numerically the most frequent or Asteraceae pollen loads. Concerning Aizoaceae spe- at least among the three most frequent visitor groups cies, Lepithrix sp. 1, Heterochelus detritus and Anis- (Table 1). The only exception, Lampranthus godma- ochelus inornatus were the major carriers of pollen. niae, was mainly visited by Colydiidae (57%), with no Hopliini recorded. Other important visitors of Aizoa- ceae were blister beetles (Meloidae, especially for Colour preferences of monkey beetles Cheiridopsis denticulata), bombyliid flies or halictid bees. Other beetles (Melyridae and Histeridae) In total, 74 monkey beetles belonging to nine species occurred frequently on Ruschia goodiae. were caught in six different colour pan traps. Monkey On the other hand, during 10 min observations at beetles showed significant colour preferences (v2-test: single flowers of three different Aizoaceae species r2 = 31.50, df = 5, P < 0.001) for traps that reflected (Cheiridopsis denticulata, observed in 2003, Ruschia either short versus long wavelengths. Peritrichia pis- goodiae and Ruschia viridifolia, both observed in trinaria was the commonest monkey beetle, being 2004), bees (for C. denticulata), bombyliid flies and attracted largely to short wavelength emitting traps pollen wasps (Masaridae) were more frequent visitors (white, pink, and blue) and in smaller numbers to than hopliine beetles (Fig. 1). yellow traps (Fig. 3). In contrast, Heterochelus detritus

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Table 1 Numbers of flower visitors for selected Asteraceae and Aizoaceae plant species at Paulshoek Pollinator Cheiridopsis Cheiridopsis Conicosia Lampranthus Leipoldtia Ruschia Chrysocoma Pentzia Senecio Hirpicium Tripteris Osteospermum family namaquensis denticulata elongata namaquensis schultzei goodiae ciliata incana niveus alienatum sinuata spinescens

Hopliini 5 (14.7%) 3 (12.5%) 2 (18.2%) 0 3 (15.8%) 10 (35.7%) 3 (21.4%) 5 (45.5%) 60 (93.8%) 0 12 (66.6%) 19 (95%) Meloidae 16 (47.1%) 14 (58.3%) 2 (18.2%) 0 3 (15.8%) 3 (10.7%) 2 (14.3%) 0 1 (1.6%) 0 0 1 (5%) Dermestidae 2 (5.9%) 0 1 (9.1%) 0 0 0 0 0 0 0 0 0 Buprestidae 0 1 (4.2%) 0 0 0 0 0 0 0 0 0 0 Bruchidae 0 0 0 0 0 1 (3.6%) 0 0 0 0 0 0 Melyridae 1 (2.9%) 0 0 0 4 (21.1%) 4 (14.3%) 0 1 (9.1%) 0 0 0 0 Nitidulidae 0 0 1 (9.1%) 1 (14.3%) 0 0 0 0 0 0 0 0 Histeridae 0 0 0 0 0 1 (3.6%) 0 1 (9.1%) 0 1 (16.7%) 0 0 Phalacridae 0 0 0 0 0 0 0 1 (9.1%) 0 3 (49.9%) 0 0 Colydiidae 0 0 0 4 (57.1%) 0 3 (10.7%) 0 0 0 0 0 0 Unidentified beetle sp.1 1 (2.9%) 0 0 0 0 2 (7.1%) 0 1 (9.1%) 0 0 3 (16.7%) 0 Apidae 0 1 (4.2%) 1 (9.1%) 0 0 0 1 (7.1%) 0 0 0 0 0 Megachilidae 0 0 0 0 2 (10.5%) 0 1 (7.1%) 0 0 0 0 0 Halictidae 1 (2.9%) 2 (8.3%) 0 0 2 (10.5%) 0 2 (14.3%) 0 0 0 0 0 Colletidae 0 1 (4.2%) 0 0 0 0 0 0 0 0 0 0 Anthophoridae 0 0 1 (9.1%) 0 1 (6%) 0 0 1 (9.1%) 0 0 0 0 Masaridae 0 0 1 (9.1%) 0 0 0 0 0 2 (3.1%) 0 0 0 Braconidae 0 0 0 0 0 0 0 0 1 (1.6%) 0 0 0 Bombyliidae 4 (11.8%) 1 (4.2%) 2 (18.2%) 1 (14.3%) 3 (15.8%) 3 (10.7%) 5 (35.7%) 1 (9.1%) 0 1 (16.7%) 3 (16.7%) 0 Calliphoridae 0 0 0 0 1 (5.3%) 1 (3.6%) 0 0 0 0 0 0 Syrphidae 1 (2.9%) 0 0 0 0 0 0 0 0 0 0 0 Lycaenidae 3 (8.8%) 1 (4.2%) 0 1 (14.3%) 0 0 0 0 0 1 (16.7%) 0 0 netCnev(06 10:323–333 (2006) Conserv Insect J The proportion of each insect family is expressed as a percentage of the total number of insect visitors for each plant species J Insect Conserv (2006) 10:323–333 327

C.denticulata R.goodiae R.viridifolia n = 90) compared to the lightly grazed site (2002: 60 n = 98, 2003: n = 13, 2004: n = 24), the abundance of 50 Heterochelus detritus was higher under low grazing 40 pressure in 2002 and 2003 (28 and 85 vs. 23 and 8 under 30 high grazing pressure) but lower in 2004 (5 vs. 13 under 20 high grazing pressure). % of visits 10 Other species occurred in similar numbers at both 0 sites, including Anisochelus inornatus, one of the most a abundant monkey beetles in 2003 and 2004 (1002 and Hopliini Apoidea Meloidae 37 individuals on the lightly and 1220 and 47 on the Masaridae other WaspsBombyliidaeother Diptera Lepidopter heavily grazed site), which had very low numbers in other Coleoptera 2002 (7 on the heavily grazed site and 4 on the lightly visitor taxa grazed site). Fig. 1 Proportion of flower visiting taxa during 10 min flower In total, the heavily grazed site had a slightly higher observations of C. denticulata (650 min in total), R. goodiae species richness than the lightly grazed site in 2003, (780 min in total) and R. viridifolia (400 min in total) while in the other 2 years, species numbers were comparable (Table 3). However, species diversity and was mainly caught in long wavelength emitting traps evenness were always higher on the lightly grazed site (yellow, orange, and red). Anisochelus inornatus was (Table 3). attracted to yellow and pink traps. Only very low The high number of beetles in 2003 was largely numbers of Campulipus limbatus, Stigmatoplia ornata, attributable to large numbers of Anisochelus inornatus. Lepithrix sp. 1, and Pachycnema calcarata were col- Its numbers dropped dramatically in 2004. The same lected. Pachycnema flavolineata was only caught in trend was observed for Heterochelus pulverosus, with yellow pans, while Platychelus sp. was attracted to higher numbers in 2003 compared to 2002 and 2004. various short wavelength-emitting traps, but also to Some species were only present in 1 year, e.g. Dentic- yellow traps (Fig. 3). nema morbillosa, Inanda sp., Platychelus sp., Sce- lopyhsa sp. (in 2003) or Kubousa sp. (only trapped in The impact of grazing on monkey beetle species 2004). richness and species diversity

The colour pan samples were pooled to arrive at the Discussion observed species richness and diversity for the heavily and lightly grazed sites (Table 3). Relative importance of monkey beetles as Similar numbers of monkey beetles were trapped on pollinators both study sites in all 3 years of investigation (MWU- tests: 2002: Z = )0.74, P = 0.46, 2003: Z = )0.39, Most of the Aizoaceae and Asteraceae species exam- P = 0.70, 2004: Z = 1.01, P = 0.31, n = 14). In 2003 ined here were visited by a range of pollinators from though, up to 10 times more individuals were caught various orders, but nearly always dominated by mon- than in 2002 and 2004 (2002: n = 433, 2003: n = 2508, key beetles, bombyliid flies, meloid beetles and halictid 2004: n = 239; Kruskal–Wallis-Test: H (2, bees. N = 84) = 11.82, P < 0.003). For five of the six species of Asteraceae examined, Comparing numbers of species that were caught, monkey beetles were the most frequent flower visitors. there were no significant differences between the sites In addition, five species of monkey beetles accounted under different grazing regimes in 2002 and 2004 for the highest Asteraceae pollen loads, with antho- (MWU-test: 2002: Z = )0.18, P = 0.85, 2004: phorid, apid and halictid bees carrying smaller amounts Z = )0.41, P = 0.68, n = 14). In 2003 on the other of pollen. Although various authors have indicated the hand, on average more species were trapped on the importance of monkey beetles for Asteraceae pollina- lightly grazed site (Student’s t: t = )2.34, df = 26, tion in the Succulent Karoo and fynbos biomes of P = 0.027, n = 14). Southern Africa (Picker and Midgley 1996; Goldblatt Some species also had contrasting abundances on et al. 1998; Steiner 1998), none has attempted to the heavily and lightly grazed sites. For example, while evaluate their importance as pollinators using quanti- Peritrichia pistrinaria was more abundant on the tative pollen analysis. Monkey beetles and meloids heavily grazed site (2002: n = 131, 2003: n = 60, 2004: were the most frequent visitors to Aizoaceae, followed

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Table 2 Pollen loads carried by each flower visitor in the Paulshoek area Pollinator species Family No. of individuals Mean Asteraceae Mean Aizoaceae examined pollen load – SD pollen load – SD

Amegilla niveata Anthophoridae 1 4435 4160 Apis mellifera Apidae 4 4036 – 7003 12,744 – 11,114 Australoechus ammophilus Bombyliidae 4 1381 – 41 5420 – 15 Australoechus micans Bombyliidae 7 3504 – 4076 3139 – 3780 Australoechus sp. 1 Bombyliidae 2 5150 – 7285 6452 – 1917 Exoprosopa sp. Bombyliidae 5 1513 – 2649 4753 – 5430 Megapalpus sp. Bombyliidae 1 0 657 Systoechus plebelus Bombyliidae 5 1791 – 3102 3323 – 3544 sp. 1 Braconidae 1 2957 370 sp. 1 Bruchidae 2 59 – 23 85 – 72 Neojulodis picta Buprestidae 1 0 1558 Chrysomyia sp. Calliphoridae 2 0 1088 – 273 Scrapter sp. 1 Colletidae 1 0 3812 sp. 1 Colydiidae 1 0 68 sp. 2 Colydiidae 6 53 – 75 629 – 407 sp. 1 Dermestidae 3 0 909 – 788 Chaetalictus sp. Halictidae 4 3297 – 3693 3853 – 852 Halictus jacandus Halictidae 2 2330 – 3296 2528 – 1489 sp. 2 Halictidae 1 6785 2610 sp. 1 Histeridae 3 383 – 540 702 – 750 spp. Lycaenidae 6 1050 – 1321 4310 – 2141 sp. 1 Masaridae 1 1987 723 sp. 3 Masaridae 1 0 2307 Hoplitis sp. 2 Megachilidae 1 2125 607 sp. 1 Megachilidae 2 970 – 168 6802 – 998 Ceroctis karooensis Meloidae 2 1686 – 1153 7044 – 9084 Iselma sp. Meloidae 39 1693 – 2284 2835 – 1566 Mimesthes holgaticus Meloidae 1 501 2357 Malachiidae sp. 1 Melyridae 10 194 – 401 318 – 51 sp. 1 Nitidulidae 2 0 0 sp. 1 Phalacridae 4 270 – 132 92 – 68 Anisochelus inornatus Scarabaeidae 18 5126 – 8277 8158 – 4538 Stigmatoplia ornata Scarabaeidae 36 5499 – 6147 2406 – 3573 Heterochelus detritus Scarabaeidae 3 6923 – 9029 9294 – 8653 Kubousa sp. 1 Scarabaeidae 1 3322 6037 Lepithrix sp. 1 Scarabaeidae 2 2975 – 4207 9731 – 227 Pachycnema flavolineata Scarabaeidae 1 5870 2645 Platychelus sp. 1 Scarabaeidae 60 9885 – 2242 2168 – 477 Unidentified sp. 1 Scarabaeidae 1 2199 5984 Syrphidae sp. 1 Syrphidae 1 284 284 Coleoptera sp. 1 unidentified 7 349 – 401 180 – 176 by bombyliid flies. Concerning Aizoaceae pollen loads, pollinator association between monkey beetles and the monkey beetles were only exceeded by honey bees. convergent disc form of the Asteraceae and Aizoaceae Generally, the large pollen loads carried by monkey suggests that the extensive adaptive radiation of these beetle species, and their selection of a few hosts rank plant families in the Succulent Karoo (accounting for them amongst the most important pollinators of As- 18 and 20% of the approximately 4850 species of the teraceae and Aizoaceae. Pollen load is one of the most biome, (Cowling and Hilton-Taylor 1999) may be important components in the evaluation of the associated with the equally spectacular adaptive radi- importance of a pollinator (Dafni 1992), even if heavily ation of the monkey beetles (approximately 700 spe- loaded pollinators are not always the most efficient cies are described from the region, Colville et al. 2002). ones (Pe´rez-Mellado et al. 2000). The large population However, the potential of bees and other insects as sizes and huge numbers of monkey beetle species in effective pollinators should not be underrated as shown the Succulent Karoo (Vernon 1999) add further sup- by the results of flower observations, where bees, pol- port to a major pollinator role played by monkey len wasps and bee flies were more frequent visitors beetles in this region (see also Picker and Midgley than monkey beetles. Monkey beetles tend to remain 1996; Goldblatt et al. 1998; Steiner 1998). This close for longer periods on individual flowers (especially the

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Fig. 2 The average amount 45000 of pollen grains carried by 40000 each pollinator family Average number of pollen grains for Asteraceae 35000 Average number of pollen grains for Aizoaceae 30000 25000 20000 15000 10000 5000 Average number of pollen grains 0

Apidae Butterfly Meloidae Melyridae Colletidae HalictidaeBruchidae Masaridae HisteridaeColydiidae Syrphidae Buprestidae Braconidae Bombyliidae Megachilidae Dermestidae Calliphoridae Scarabaeidae Anthophoridae Phalacridiidae

unidentified beetle sp1 Pollinator family

Fig. 3 Total number of 20 Blue Orange Pink Red White Yellow monkey beetles trapped in different colour pans in the 18 Paulshoek area 16 14 12 10 8 6 4 number of individuals 2 0

Lepithrix sp1 Platychelus sp1 Stigmatoplia ornota Campulipus limbatus Heterochelus detritus Peritrichia pistrinaria Anisochelus inornatus Pachycnema calcarata Pachycnema flavolineata Monkey beetle species

Table 3 Differences between lightly and heavily grazed sites in terms of species diversity and richness in Paulshoek (trap yields from three colour traps) Site (year) No. of No. of Margalef’s index Pielou’s evenness Brillouin’s index Shannon–Wiener’s species individuals of species richness index (J’) of species diversity index of species diversity (S) (N) (d) (HB) (H’)

Lightly grazed (2002) 10 218 1.724 0.608 1.321 1.399 Heavily grazed (2002) 10 215 1.688 0.563 1.223 1.295 Lightly grazed (2003) 13 1197 1.693 0.275 0.688 0.706 Heavily grazed (2003) 10 1311 1.253 0.147 0.327 0.338 Lightly grazed (2004) 7 90 1.333 0.691 1.232 1.344 Heavily grazed (2004) 8 149 1.399 0.546 1.062 1.136 embedding guild—Picker and Midgley 1996). The two periods, they are more probable to be recorded during methods applied tend to favour different kinds of snap-shot examinations of plants. During flower pollinators. Since beetles remain on flowers for lengthy observations on the other hand, one is more likely to

123 330 J Insect Conserv (2006) 10:323–333 observe more actively flying insects, especially bees, literature, probably because of the great effort re- which stay on a plant only for a few seconds. quired to study the wide variety of insects and plants Although smaller beetles (e.g. Nitidulidae) were involved. abundant in the flowers, they only carried small Insect responses to grazing disturbance differ wide- amounts of pollen, probably because they are less ly, some benefiting and increasing in abundance while hairy. Proctor et al. (1996) have reported that although others are displaced (Milton and Dean 1992). small beetles may be abundant in flowers, they transfer However, the different plant species composition on little pollen. both sides of the grazing line at the experimental site (Todd and Hoffman 1999) attracted different species of monkey beetles, since different genera and species Colour preferences of monkey beetles have distinct flower preferences (Picker and Midgley 1996). The overall number of beetles was consistently Monkey beetle pollination differs from the general higher on the heavily grazed site (although not statis- beetle pollination syndromes (Proctor et al. 1996; tically significant), a finding similar to that of Colville Gemmill et al. 2004) in that visual attraction seems et al. (2002) for disturbed sites in the Succulent Karoo, more important than odour (Picker and Midgley 1996). and of (Seymour and Dean 1999) for general inverte- There was fairly poor overlap between the flower col- brates on the heavily grazed site in Paulshoek. This ours selected, and the colour of the pan traps to which suggests the presence of suitable resources for monkey the various species of beetles were attracted. This beetles in grazed areas, possibly abundances of the finding is in contrast to the correlation observed by annual Asteraceae that flourish under disturbed con- Picker and Midgley (1996) who were able to distin- ditions. Also, the pan traps on the two sites were sit- guish a short from a long wavelength guild of pollina- uated up to 2 km apart, well within the flight tor. Johnson and Midgley (2001) also found a capabilities of foraging monkey beetles, which travel correlation between the attraction of monkey beetles such distances within 60 min in times of flower short- to model flowers and the colours of host-plant flowers. age (pers. obs.). The similarity in numbers, species Since between season variation in rainfall results in richness and diversity of the monkey beetle commu- different plant composition from year to year, the nities on either side of the fence suggest that over- beetles may not have been able to make optimal grazing does not impact severely on these insects, and selection of flower hosts, (2003 and 2004 were below that a viable pollinator community can still exist under average rainfall years in the Succulent Karoo), while heavy grazing pressure. Given the generalised flower the traps still offered the full spectrum of colour for visitation behaviour of monkey beetles, overgrazing is inherent preferences. unlikely to impact negatively on the pollination of Cowling and Hilton-Taylor (1999) suggested that Asteraceae and Aizoaceae. the large floral displays characteristic of the Succulent The observed differences in monkey beetle popu- Karoo reflect interspecific competition for pollinators. lations between the study years are most likely the A large proportion of the Asteraceae flowers in the result of variations in winter rainfall. Heavy rains in Succulent Karoo are yellow, possibly indicating their August 2003 (66 mm compared to 16.5 mm in 2002 and generalist mode of pollination (yellow flowers are 3 mm in 2004, data provided by T. M. Hoffman) might often highly reflective and considered to be a generalist have led to the high emergence rates of monkey bee- colour in pollination biology (Kevan 1978; Kirk 1984; tles in 2003. On the other hand, early rains from Jan- Leong and Thorp 1999). Monkey beetles were also uary to July were totally lacking (only 18 mm in 2003 highly attracted to yellow pans. In contrast, orange and compared to 101 and 94.5 mm in 2002 and 2004), red pans attracted fewer beetles. However, monkey leading to very few flowers at time of study. It is as- beetles are among few beetles known to visit red sumed that due to low flower numbers, the attractive- flowers (Picker and Midgley 1996). ness of colour traps to monkey beetles was much higher at that time, while in other years the traps Impact of overgrazing on the pollinator community competed with surrounding flowers for the attraction of insects. The same phenomenon has been recorded Insects are generally considered to be good indicators for bees (Mayer 2005). Additionally, because of food of landscape change as they are abundant, species rich shortages, i.e. low flower numbers, the beetles may and widespread, and are important in the functioning have experienced reproductive failure in 2003. A fur- of ecosystems (Samways 1994). However, community- ther factor influencing inter-annual beetle numbers level studies of pollination are relatively rare in the would be rainfall in the preceding year. This would

123 J Insect Conserv (2006) 10:323–333 331 explain the high numbers in 2003 and low numbers of (Lepithrix and Heterochelus) are soil-inhabiting detri- beetles in 2004. tivores, and as such might not be affected by changes in the plant community, as long as the organic content of Conclusions for conservation management the soil remains unchanged (J. Colville, pers. comm.). The major impact on the larvae would be by trampling Evidently, monkey beetles are one of the most and soil compaction which accompany overstocking. important pollinators of Asteraceae and Aizoaceae in To preserve biodiversity, conservation should be di- the Paulshoek area, and probably for much of the rected towards tracts of undisturbed veld between Succulent Karoo. The major impact of overgrazing is grazed habitats which could provide a source of poll- not on the pollinators, but on the plants themselves, inators that could then move into disturbed areas, with the entire plant community changing under con- including those some distance from the preserved ditions of intense grazing. This change in the compo- tracts. Longer term studies would be necessary to dis- sition of plant species, especially the shift from tinguish inter-annual, natural fluctuations in species perennial plants to annuals and geophytes could in turn composition of monkey beetles from changes in com- affect the composition of monkey beetle assemblages. munity composition that might be driven by the effects Since annuals are not a reliable food source in drought of overgrazing. years, the likely reproductive failure of monkey beetles as observed in 2004 could increase with the risk of Acknowledgements This study is embedded in BIOTA Africa climate change and aridification (Rutherford et al. (http://www.biota-africa.org) which is sponsored by the German Federal Ministry of Education and Research (Bmbf 01LC0024). 1999). It was shown that some Hopliini, probably the Carolin Mayer would like to thank Professors N. Ju¨ rgens (Uni- more widespread and ‘weedy’ species, increased versity of Hamburg) and M.T. Hoffman (University of Cape enormously in abundance on degraded sites, while Town) for supervision. Northern Cape Nature Conservation rarer species were more vulnerable to the impacts of Services provided research permits. Special thanks go to Jona- than Colville (University of Cape Town) for helping with the grazing and disappeared. This was probably a response identification of monkey beetles. A University of Cape Town to changing plant species composition. Research Grant awarded to M. Picker provided travel costs. G. The role of the soil for the larval development of Soka acknowledges the financial support kindly provided by the monkey beetles should be considered as well. The few Tropical Biology Association (TBA), as well as supervision by M. Picker and C. Mayer. monkey beetle larvae that have been found thus far

Appendix 1 A list of flower visitor species collected from flowers Insect species Family Host plant species

Amegilla niveata Anthophoridae Conicosia elongata Apis mellifera Apidae Cheiridopsis denticulata, Chrysocoma ciliata, Conicosia elongata and Pentzia incana Australoechus sp. 1 Bombyliidae Cheirodopsis namaquensis and Leipoldtia schultzei Systoechus plebelus Bombyliidae Cheirodopsis namaquensis, Chrysocoma ciliata, Conicosia elongata and Ruschia goodiae Megapalpus sp. Bombyliidae Cheirodopsis namaquensis and Leipoldtia schultzei Exoprosopa sp. Bombyliidae Cheirodopsis namaquensis, Leipoldtia schultzei, Pentzia incana and Chrysocoma ciliata Australoechus ammophilus Bombyliidae Cheiridopsis denticulata and Ruschia goodiae Australoechus micans Bombyliidae Chrysocoma ciliata, Conicosia elongata, Hirpicium alienatum, Tripteris sinuata and Lampranthus goodmaniae Australoechus hirtus Bombyliidae Pentzia incana sp. 1 Braconidae Senecio niveus sp. 1 Bruchidae Leipoldtia schultzei and Ruschia goodiae Neojulodis picta Buprestidae Cheiridopsis denticulata spp. Lycaenidae Cheirodopsis namaquensis, Hirpicium alienatum, Cheiridopsis denticulata and Lampranthus goodmaniae Scrapter sp. 1 Colletidae Cheiridopsis denticulata sp. 1 Colydiidae Lampranthus namaquensis and Ruschia goodiae sp. 2 Colydiidae Ruschia goodiae sp. 1 Dermestidae Cheirodopsis namaquensis and Conicosia elongata Halictus jucundus Halictidae Cheirodopsis namaquensis, Cheiridopsis denticulata and Leipoldtia schultzei Chaetalictus sp. 1 Halictidae Cheiridopsis denticulata, Chrysocoma ciliata and Leipoldtia schultzei sp.1 Halictidae Chrysocoma ciliata sp. 1 Histeridae Hirpicium alienatum, Pentzia incana and Ruschia goodiae

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Appendix 1 continued Insect species Family Host plant species sp. 1 Masaridae Conicosia elongata and Senecio niveus Hoplitis sp. 2 Megachilidae Chrysocoma ciliata sp.1 Megachilidae Leipoldtia schultzei Iselma sp. Meloidae Cheirodopsis namaquensis, Chrysocoma ciliata, Leipoldtia schultzei, Ruschia goodiae and Senecio niveus Ceroctis karooensis Meloidae Chrysocoma ciliata and Osteospermum spinescens Mimestaes holgaticus Meloidae Ruschia goodiae sp. 1 Melyridae Cheirodopsis namaquensis, Leipoldtia schultzei, Pentzia incana and Ruschia goodiae sp. 1 Nitidulidae Conicosia elongata and Lampranthus goodmaniae sp.1 Phalacridae Hirpicium alienatum and Pentzia incana Anisochelus inornatus Scarabaeidae Cheirodopsis namaquensis, Pentzia incana and Ruschia goodiae Lepithrix sp.1 Scarabaeidae Cheiridopsis denticulata and Conicosia elongata Heterochelus detritus Scarabaeidae Cheiridopsis denticulata Platychelus sp.1 Scarabaeidae Chrysocoma ciliata and Senecio niveus Stigmatoplia ornata Scarabaeidae Osteospermum spinescens, Pentzia incana, Ruschia goodiae, Tripteris sinuata and Senecio niveus Unidentified sp. 1 Scarabaeidae Leipoldtia schultzei Kubousa sp. 1 Scarabaeidae Tripteris sinuate Pachycnema flavolineata Scarabaeidae Tripteris sinuate sp. 1 Coleoptera Cheirodopsis namaquensis, Pentzia incana, Ruschia goodiae and Tripteris sinuata

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