Distributions of flower associations of pollen wasps (Vespidae: Masarinae) in southern Africa

ARTICLE IN PRESS Journal of Arid Environments Journal of Arid Environments 57 (2004) 17–44 www.elsevier.com/locate/jnlabr/yjare

Distributions of flower associations of pollen wasps (Vespidae: Masarinae) in southern Africa Sarah K. Gess*, Friedrich W. Gess Makana Biodiversity Centre, Albany Museum, Somerset Street, Grahamstown, Eastern Cape 6139, South Africa Received 4 July 2002; accepted 6 May 2003

Abstract Recent (1996–2002) sampling by the authors of flower visitors in particular in the Richtersveld and Namibia has added considerably to the knowledge of the flower associations of pollen wasps (Vespidae: Masarinae) in southern Africa which prior to that date was largely based on sampling to the south and east of the Richtersveld and Namibia. Their earlier findings that pollen wasps in southern Africa show major preferences (based on number of species visiting a plant taxon) for Aizoaceae and Asteraceae remains unchanged, although in the northwest summer rainfall region the preference is for Aizoaceae: non-Mesembryanthema rather than Mesembryanthema. The preference shown by some for Aptosimeae (Scrophulariaceae) stands throughout the area and that for Hermannia (Malvaceae) is established for the north and southwest. Preferences for Campanulaceae (principally Wahlenbergia) and Cape Crotalarieae (Fabaceae: Papilionoideae) are shown to be restricted to the southwest. Preference for Zygophyllum (Zygophyllaceae) is established for the Richtersveld and Namibia only. Limited preferences for Molluginaceae, Geraniaceae and Boraginaceae, and a single close mutualistic association between two narrow endemics, a pollen wasp and Tylecodon hallii . . (Tolken) Tolken (Crassulaceae), are demonstrated. A greater degree of casual visiting to a wider range of plant families was recorded for the Richtersveld and Namibia than for the southwest and southeast, however, a high degree of oligophagy to narrow polyphagy is maintained throughout. r 2003 Elsevier Ltd. All rights reserved. Keywords: Aizoaceae; Asteraceae; Boraginaceae; Zygophyllaceae; Aptosimeae; Hermannia; Tylecodon; Wahlenbergia; Masarinae; Southern Africa

*Tel.: +27-46-622-2312; fax: +27-46-622-2398. E-mail address: [email protected] (S.K. Gess). 0140-1963/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0140-1963(03)00093-4

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1. Introduction Pollen wasps, like all non-parasitic bees, visit flowers to collect pollen and nectar for provisioning their nests and both male and female in addition imbibe nectar, and possibly pollen, for their own nourishment. The majority of pollen wasps have long ‘‘tongues’’ giving them the potential, like long-tongued bees to obtain nectar from a wider range of flower forms than do short-tongued wasps and bees. The ‘‘pollen wasp pollination syndrome’’, though less broad, falls within the syndrome designated melittophily (the bee and fly pollination syndrome). This does not mean, however, that the flowers visited by pollen wasps are necessarily equally efficiently serviced by bees and/or bee flies. Indeed case studies have made it clear that whereas pollen wasps visiting some flower groups are members of a guild of flower visitors, all of which are potential pollinators, the pollen wasps visiting others are probably their most important pollinators (Gess, 1996). All pollen wasps in southern Africa are endemic to this region, some are broadly endemic and others narrowly endemic (Gess, 1996). The first substantial account of the flower associations of the Masarinae of southern Africa was given in 1989 (Gess and Gess, 1989). At that time flower visiting records for that area were available for 69 species belonging to seven genera (Ceramius, 14 spp.; Jugurtia, 4 spp.; Masarina, 3 spp. ; Celonites, 8 spp.; Quartinia and Quartinioides, 40 spp.). The subject was revisited in 1992 (Gess, 1992a, b), when the distributions and flower associations of pollen wasps of the world were reviewed. In 1996 an updated review was given together with an examination of pollen wasps as pollinators in southern Africa. At that time flower visiting records were available for an additional 26 species, that is in total 95 species, (Ceramius, 18 spp.; Jugurtia, 8 spp.; Masarina, 4 spp. ; Celonites, 10 spp.; Quartinia, Quartinioides and Quartiniella, 55 spp.) (Gess, 1996, pp. 36–54, 136–186, and appendices 1 and 2, 205–304) . At that time little sampling of flowers for aculeate wasp and bee visitors had been conducted in the Richtersveld and Namibia, the records for masarines in Namibia being solely Quartinia spp. (Turner, 1939, from Aus and Wharton, 1980, from Gobabeb). Since 1996 the present authors have extended their sampling of aculeate wasp and bee flower visitors in the semi-arid to arid areas of southern Africa northwards to include northern Richtersveld (Gess et al., 1997) and Namibia, bringing the number of masarine species for which flower visiting records are available to 130. Included are records for the recently described genus, Priscomasaris Gess (Gess, 1998, 2001), the most primitive known extant member of the Masarini, known only from Namibia. The present paper re-examines pollen wasp flower associations in southern Africa in particular with reference to the distributions of these associations.

2. Study area The study area is constituted of the Karoo Biome of Rutherford (1997) together with the Fynbos fringe in the southwest and the Desert and Savanna fringes in the north (Fig. 1). This area coincides with the distribution of Masarinae in southern Africa (Gess, 1992a, b, 1996, pp. 12–35).The vegetation of the area is characterized

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Fig. 1. Southern Africa. Distributions of Fynbos (F), the Succulent Karoo (SK), the Nama Karoo (NK), the Desert (Namib) (N) and the Savanna (S) biomes, after Rutherford (1997).

by low to dwarf scrub with taller shrubs and/or trees in the main restricted to drainage channels and hill slopes. The scrub vegetation varies according to regional rainfall from sparse over most of the area, which receives 100–500 mm precipitation per annum to extremely sparse in the desertic area, the Namib desert which receives less than 100 mm precipitation per annum. Succulence is particularly associated with the winter rainfall region, resulting in this part of the Karoo being termed the Succulent Karoo. The summer rainfall region of the Karoo, with a lower level of succulence and a higher grassy element is known as the Nama Karoo. Detailed reviews of the climate, topography, geology and vegetation of the study area are presented by various authors in Cowling et al. (1997) and Dean and Milton (1999).

3. Flower sampling sites and times The distribution of the authors’ sampling sites within the study area is given in Fig. 2 and the distribution of sites from which masarines were present in the samples is given in Fig. 3.

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Fig. 2. Distribution of flower visitor sampling sites.

Sampling to the east and south has been spread over the past thirty years but principally from 1972 to 1985, that in the west south of the Richtersveld principally from 1985 to 1996, in the Richtersveld principally from 1996 to 1998 and in Namibia principally from 1997 to 2002. Apart from the area in which the authors are resident it has not been possible to sample throughout the year. Seasonal timing of sampling by the authors has been based on experience and for different areas on their gross rainfall and temperature patterns. Thus: in the southeast and south where the peaks of rainfall are in September and March and the summer is rarely excessively hot and dry sampling has been principally from late October through to March; in the southwest north to Luderitz . and Aus, that is in the winter rainfall region, from August, when temperatures start to rise, through to December, when most flowering is over and the land as a general rule becomes parched; and north of the Orange River in the south eastern karroiid areas and in the west to the north of the winter rainfall area sampling by the authors has been in March through to early May, when rains are expected and excessive heat is past. For the present analysis the area sampled, the Karoo–Namib and associated fynbos and arid savanna fringes has been divided into zones (Fig. 4): South (the area sampled

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Fig. 3. Distribution of sites at which pollen wasps were represented in flower visitor samples.

to the south of the Gariep River, formerly Orange River, excluding the Richtersveld), Transition (the Richtersveld south of the Gariep River and the winter rainfall region of southwestern Namibia as far north as Luderitz . and Aus) and North (the area to the north of the Gariep River excluding the area included in transition). The South is divided into two sub-zones, Southwest (the winter rainfall region) and Southeast (summer and spring/autumn rainfall regions), and the North into Northwest (west of a line through Mariental and Keetmanshoop) and Northeast (to the east of that line). The distribution and magnitude of rainfall events and therefore of flower patches in the semi-arid and arid areas of southern Africa is unpredictable. Thus although general sampling areas and sampling times have been purposefully selected, the choice of sampling sites has of necessity been opportunistic.

4. Sampling method Solitary aculeate wasps and bees visiting flowers were collected using a hand net. All plants in flower at the study sites were observed for visitors and, when possible,

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Fig. 4. Sampling zones.

were sampled over periods throughout the day. In effect wasps and bees in an area were all being offered the choice of visiting all those plants which were in flower. Each site sampled therefore represented a ‘‘choice chamber’’ in which all the wasps and bees were offered the same choice of plants in flower.

5. Classification of flowering plants The classification of flowering plants used for the 1992 analysis followed that of Cronquist (1988). The presently used classification follows that of ‘‘The Angiosperm Phylogeny Group’’ (APG, 1998).

6. Database The database is constituted of c 16 000 flower visiting records for 42 plant families. Of the c 850 species of aculeate wasps and bees included 130 species are pollen wasps

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(Gess and Gess, unpublished catalogue). That used for the 1992 analysis (Gess, 1992b) was constituted of 7000 records for 32 (35) plant families and 616 species of aculeate wasps and bees. In the sampling area overall all the described genera of southern African Masarinae are included (Ceramius Latreille, Celonites Latreille, Jugurtia Saussure, Masarina Richards, Priscomasaris Gess, and Quartinia Ed. Andre! , sensu lato, that is including Quartinioides Richards and Quartiniella Schulthess). Represented in the Southwest, Southeast and Transition are all genera except Priscomasaris; in the Northwest all genera except Masarina; and in the Northeast all genera except Ceramius, Masarina and Priscomasaris. Cowling and Hilton-Taylor (1999, Table 4.1) list the 10 largest plant families from each of five domains (Namaqualand–Namib semi-arid and Namaqualand–Namib arid, Southern Karoo, Eastern Karoo and Damaraland–Kaokoveld) of the Karoo– Namib Region, 14 families in all, Asteraceae, Aizoaceae, Acanthaceae, Asclepiadaceae, Chenopodiaceae, Capparaceae, Crassulaceae, Euphorbiaceae, Fabaceae, Geraniaceae, Scrophulariaceae, Sterculiaceae, Iridaceae, Liliaceae and Poaceae. The 42 families recorded in the database as visited by solitary aculeate wasps and bees include all the listed families excluding Poaceae and Chenopodiaceae.

7. Results and discussion 7.1. Diversity of choice Of the 42 plant families recorded as receiving visits from aculeate wasps and bees 22 received visits from pollen wasps (Table 1) as compared with 28 from other aculeate wasps (excluding the Polistinae) and 39 from bees (excluding honeybees). For the 1992 analysis (Gess, 1992b) a formula was devised to obtain a measure of the percentage diversity of choice at the specific level, D=(a b)/b  100, where a is the sum of the number of species recorded visiting each of the flower families and b is the number of species of flower visitors (published in Gess, 1996). This is an index by which to compare the degree of oligophagy or polyphagy exhibited by taxa of differing numbers of species. At that time the percentage diversity of choice for pollen wasps obtained was 43 compared with 95.6 for bees and 114 for the non-masarine wasps, indicating an overall higher degree of oligophagy (sensu Struck, 1994, i.e. use of a taxonomically limited range of host plants) and lower degree of polyphagy (sensu Struck, 1994, i.e. use of a taxonomically diverse range of host plants) in pollen wasps compared with bees and non-masarine wasps. The percentage diversity of choice at the specific level for individual bee families (excluding Andrenidae and Fideliidae, for which there were too few records) was: 38.1 for Colletidae, 121.2 for Halictidae, 44.4 for Melittidae, 73.6 for Megachilidae and 150.8 for Anthophoridae, indicating a similar percentage diversity of choice for Masarinae, Colletidae and Melittidae and a narrower diversity of choice for Masarinae compared with Halictidae, Megachilidae and Anthophoridae.

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Table 1 Flower taxa recorded as visited by Masarinae in southern Africa No. of spp. for which flower visits are recorded

Priscomasaris

Ceramius

Celonites

Jugurtia

Masarina

Quartinia

1

20

14

16

9

70

MONOCOTS Asparagales Asphodelaceae

1

Iridaceae CORE EUDICOTS Caryophyllales Aizoaceae Mesembryanthema Non-Mesembryanthema

1 (1)

Amaranthaceae Molluginaceae

8 (8) 1 (1)

1

1

4 2

4 (4) 1

38 (18) 11 (6)

1 2

1

Nyctaginaceae

1

1

Plumbaginaceae

1

2

Saxifragales Crassulaceae

1

ROSIDS Zygophyllaceae

1 (1)

1

1

1

2

Geraniales Geraniaceae

4 (1)

EUROSIDS I Fabales Fabaceae Caesalpinoideae Mimosoideae Papilionoideae Malpigiales Euphorbiaceae

1 (1)

3

1

9 (4)

1 (1)

1 (1)

1

2 (1) 1 4 (3)

4 (3)

2

1

EUROSIDS II Brasicales Brassicaceae

1

Malvales Malvaceae

4 (4)

2

2 (1)

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Table 2 (continued) No. of spp. for which flower visits are recorded

Priscomasaris

Ceramius

Celonites

Jugurtia

Masarina

Quartinia

1

20

14

16

9

70

Neuradaceae

1

EUASTERIDS I Boraginaceae

1 (1)

2 (2)

2 (1)

Vahliaceae Lamiales Acanthaceae Lamiaceae Scrophulariaceae Aptosimeae Others Asterales Asteraceae Campanulaceae Lobeliaceae

1

2 1

1 7 (6) 3

2 (1) 1

2 (1)

1

9 (1) 3

9 (7)

5 (2)

9 (5)

3

28 (13)

1

5 (3) 1

1

2 (1)

10 (4)

For each genus: number of species visiting plant taxon; number of species exhibiting a specialization for plant taxon (in parentheses).

As indicated above, the data on which this analysis was based were almost entirely derived from the South. In the present analysis based on data from the entire area percentage diversity of choice has therefore been calculated for each zone separately to get some indication as to whether the figure previously obtained for pollen wasps is upheld by further sampling within the original study area and in areas beyond. The results obtained are percentage diversity of choice for the South 47.3, for the Transition 122.2 and for the North 134.6. Thus additional collecting in the South has not appreciably changed the view that pollen wasps in this area are oligophagous to narrowly polyphagous, however, there appears to be markedly wider polyphagy in the Transition and the Northwest and Northeast. This suggests that in these two northern zones there is an increase in the number of species provisioning with more than one plant family and/or a higher incidence of casual flower visiting. Taking as an example the genus Ceramius for which flower associations for all 20 species are known, of the 18 species occurring in the South each species specializes in one plant family. Of these, three species have been recorded making very occasional casual visits to flowers of a single additional plant family, and another to two additional families. Ceramius damarinus, recorded only from the North, shows a clear preference for Sesuvium sesuvioides (Fenzl.)Verdc.(Aizoaceae), with which it has been shown to provision (Gess, 1999). However, at a site where the preferred

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plant was in short supply, it was found to be visiting plants from five additional families. 7.2. Distributions of flower associations of pollen wasps Pollen wasp flower associations by zone (Fig. 4) are shown in Table 2, the taxa arranged following APG (1998). The associations of pollen wasps with the taxa from which they have been recorded with particular reference to the distributions of these associations are considered below. Plant taxa for which apparently only casual visits or possible preferences, rather than proven preferences, are included. These are considered to be of significance as possible indicators of as yet undiscovered preferences and/or as links to preferences shown by pollen wasps in other zoogeographic regions. Distributions of sites of recorded collections of pollen wasps from flower taxa for which some species, at least, show a strong preference are shown in Figs. 5–14. 7.3. Monocots 7.3.1. Asparagales 7.3.1.1. Asphodelaceae. Over a period of two weeks Quartinia antigone (Richards) was found to be visiting Aloe striata Haw. near Prince Albert at the Southwest/ Southeast divide. These are the only flower visiting records for this pollen wasp and the only records of a pollen wasp visiting Aloe or any other Asphodelaceae. 7.3.1.2. Iridaceae. The only irid genus from which pollen wasps have been recorded is Ferraria. Ferraria is generally considered to be attractive only to flies (Scott-Elliot, 1891; Vogel, 1954; Manning and Goldblatt, 2001) or flies and small beetles (De Vos, 1979), however the present authors have observed these plants for flower visitors at several sites in Namaqualand in the Southwest and Transition and have only twice observed visitors. In both instances these were masarines, Celonites capensis Brauns in the Kamiesberg and Jugurtia koeroegabensis Gess in the Richtersveld, however, neither shows a specialization for Ferraria. Both are relatively polyphagous. 7.4. Core eudicots 7.4.1. Caryophyllales 7.4.1.1. Aizoaceae and Molluginaceae. The Aizoaceae, following Bittrich and Hartmann (1988), are divided into two groups, the Mesembryanthema, which includes all those species with petaloid staminodes (Rushioideae and Mesembryanthemoideae), and the non-Mesembryanthema. The Aizoaceae are listed as one of the 10 largest families in the Karoo–Namib Region (Cowling and Hilton-Taylor, 1999). The distribution of the Mesembryanthema is centered in southwestern Africa (Hartmann, 1991). The non-Mesembryanthema are cosmopolitan in distribution. Visits to Aizoaceae by pollen wasps have been recorded from all the zones except the Northeast. Distributions of species visiting Mesembryanthema (Fig. 5)

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Table 2 Flower taxa recorded as visited by Masarinae in southern Africa No. of spp. of masarines for which flower visits recorded

Northwest

Northeast

Transition

Southwest

Southeast

26

8

27

82

21

1 w/e Aloe

1 w/e Aloe

MONOCOTS Asparagales Asphodelaceae Iridaceae CORE EUDICOTS Caryophyllales Aizoaceae Mesembryanthema Non-Mesemb

4 (4) 15% 11 (7) 42%

Amaranthaceae

2

Molluginaceae

4 (3) 15%

Nyctaginaceae

2

1 Ferraria

1 Ferraria

10 (3) 37% 3 (2) 11%

35 (21) 43% 4 (?1) 2%

2

Plumbaginaceae

3 Tylecodon hallii 1 (1)

Saxifragales Crassulaceae

ROSIDS Zygophyllaceae

11 (5) 42%

Geraniales Geraniaceae EUROSIDS I Fabales Fabaceae Caesalpinoideae Mimosoideae Papilionoideae

Crassula dichotoma 1

6 (1) 22%

5 (2) 6%

2 1 w/e

1 w/e

3 (1) 12% Acacia 1 Indigofera 1

Malpighiales Euphorbiaceae

9 (4) 43%

1

Crotalarieae Cape 9 (6) 11%

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Table 2 (continued) No. of spp. of masarines for which flower visits recorded EUROSIDS II Brassicales Brassicaceae Malvales Malvaceae

Neuradaceae EUASTERIDS I Boraginaceae

Northwest

Northeast

Transition

Southwest

Southeast

26

8

27

82

21

Cleome 1

Hermannia 4 (4) 15%

Cleome 3

Hermannia 1 (1) 1 Codon 3 (2) 11%

Heliotropium 3 (2) 12%

Vahliaceae

Hermannia 2 (1)

1

Lamiales Acanthaceae

1

Lamiaceae

2

Scrophulariaceae Aptosimeae Other

4 (3) 15% 1

1 (1)

12 (7) 44%

6 (5) 7% 6

4 (4) 19% 1

Asterales Asteraceae

8 (4) 31%

1 (1)

12 (4) 44%

34 (20) 42%

12 (4) 57%

3

18 (9) 22%

Campanulaceae Lobeliaceae

1

For each zone and plant taxon: number of masarine species visiting taxon, number of masarine species exhibiting a specialization for taxon (in parentheses), percentage of masarine species, for which flower visits recorded, visiting taxon. (w/e indicates that the record is from the interface between west and east.)

and non-Mesembryanthema (Fig. 6) show marked differences. By far the largest number of species associated with Mesembryanthema were recorded from the South, the majority being from the Southwest, however, the percentage of species recorded from flowers was equally high in the Southeast and Southwest and closely followed by the Transition. In the North visits by pollen wasps to Mesembryanthema have been recorded only along the coast and short distances inland in drainage channels reflecting the distribution of these plants. Pollen wasps visit mesems of a range of forms and are considered to be efficient potential pollinators of those species which they visit (Gess, 1996, pp. 140–145).

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Fig. 5. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Aizoaceae: Mesembryanthema.

By comparison non-Mesembryanthema (Fig. 6) and Molluginaceae (Fig. 7) (formerly included in Aizoaceae) are relatively widely and abundantly visited in the Northwest, the percentage (42%) of species represented in this zone visiting them being equivalent to that (43%) of species visiting Mesembryanthema in the South where visits to non-Mesembryanthema and Molluginaceae are rare. The numbers and percentages of species specializing in Mesembryanthema or nonMesembryanthema though lower than the numbers and percentages visiting them reflect the same distribution pattern. 7.4.1.2. Amaranthaceae. Amaranthaceae form a notable component of the vegetation of northern Namaqualand and Namibia. Preliminary palyonological evidence suggests that they were a previously predominant element before Aizoaceae: Mesembryanthema took over in the early Holocene (Scott et al., 1997). Several species are very attractive to a wide range of wasps and bees but only two species of pollen wasps have been recorded making occasional casual visits.

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Fig. 6. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Aizoaceae: non-Mesembryanthema.

7.4.1.3. Nyctaginaceae. Boerhavia deserticola Codd, flowering near Palm on the desert fringe in northwestern Namibia, attracted visits from wasps and bees. Included were two pollen wasps, Celonites gariepensis Gess, otherwise specializing in Aptosimeae, and a Quartinia, recorded in all from eight families. 7.4.1.4. Plumbaginaceae. Plumbaginaceae are represented in southern Africa by three genera, Plumbago with slender tubular flowers, Dyerophyllum with more funnel-shaped flowers and Limonium with petals separate or only fused for a short distance. The flowers of Limonium only are visited by wasps and bees, those of the other two genera by butterflies. Generally Limonium does not appear to be visited by pollen wasps, however, Celonites promontorii Brauns, specializing in Asteraceae, and two species of Quartinia, specializing in mesems, were recorded from Limonium east-north-east of Ceres in the Southwest and a further species of Quartinia was found to be foraging on Limonium together with mesems on the south coast near Mossel Bay.

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Fig. 7. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Molluginaceae.

7.4.2. Saxifragales 7.4.2.1. Crassulaceae. The Crassulaceae are listed as one of the largest families in the Karoo–Namib (Cowling and Hilton-Taylor, 1999), however, they are generally not visited by pollen wasps. One notable exception has been discovered indicating that there may be others. In the Richtersveld the narrowly endemic Tylecodon . . hallii (Tolken) Tolken appears to be visited solely by Masarina tylecodoni Gess which has been shown to be morphologically and behaviourally suited to pollinating it (Gess et al., 1997). Bird and fly pollination have been observed for other species of Tylecodon morphologically very different from T. hallii (Gess et al., 1998; Gess, 2001). The only other member of the Crassulaceae recorded as receiving visits from a pollen wasp is Crassula dichotoma L., an annual herb found growing commonly together with Wahlenbergia in sandy areas in the Southwest and like them bearing erect campanulate flowers. At Clanwilliam it was observed to be receiving nectar collection visits from Celonites wahlenbergiae Gess which is closely associated with Wahlenbergia although it does visit other flowers for nectar (Gess and Gess, 1992).

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Fig. 8. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Zygophyllum L. (Zygophyllaceae).

7.5. Rosids 7.5.1. Zygophyllaceae Zygophyllaceae are most abundant in the tropics and sub-tropics, mainly in hot, arid, alkaline regions. In southern Africa the greatest species diversity and the greatest abundance of individuals is encountered in the west. Though not amongst the 10 largest families in the Karoo–Namib they are amongst those which characterize the vegetation (Cowling et al., 1997). Zygophyllaceae occur in all the sampling zones where they are visited variously by several families of bees, however, it is only in the Transition and in the Northwest that visits are received from pollen wasps (Fig. 8). In these two zones they are expected visitors to Zygophyllum. In the Transition visits from six species, of the genera Ceramius, Jugurtia, Masarina and Quartinia, have been recorded (Gess et al., 1997) and in the Northwest from 11 species, Priscomasaris namibiensis Gess and 10 Quartinia spp. (12% of species overall). However, the only pollen wasp visitors, which are possibly specialists, are four species of Quartinia in the Northwest where it

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Fig. 9. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Fabaceae; Cape Crotalarieae (Papilionoideae) in the southwest; Adenolobus Torre & Hillc. (Caesalpinoideae) in the northwest.

has been shown that one, at least, may be of some importance as a pollinator of Zygophyllum simplex L. (Wharton, 1980). 7.5.2. Geraniales 7.5.2.1. Geraniaceae. Geraniaceae are listed amongst the 10 largest families in Namaqualand–Namib (Cowling and Hilton-Taylor, 1999). They are not widely visited by pollen wasps, however, one species each of Jugurtia and Masarina, and four of Celonites have been recorded from Pelargonium. The Jugurtia and Masarina species were abundant visitors to P. klinghardtense Knuth in the Richtersveld. They may be found to be specialist visitors and do have the potential in structure and behaviour to be pollinators of this plant. The four species of Celonites, one in the Southeast/Southwest, two in the Southwest, which specialize in Wahlenbergia and Microcodon, and one in the Transition, a widespread species specializing in Asteraceae, are probably only occasional visitors. The available information on visitors to the flowers of 28 Pelargonium taxa was assembled and analyzed by Struck (1997). He suggested that 60% fall within the bee

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Fig. 10. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Hermannia L. (Malvaceae: Sterculioideae).

pollination syndrome within which the pollen wasps can be included (Gess, 1996, pp. 183–186). The only other records of a pollen wasp visiting Geraniaceae are for a species of Quartinia in the Transition visiting Sarcocaulon in addition to Aizoaceae, Asteraceae, Brassicaceae and Scrophulariaceae (Gess and Gess, 1999). 7.6. Eurosids 7.6.1. Fabales 7.6.1.1. Fabaceae. The Fabaceae are listed as one of the 10 largest plant families occurring throughout the Karoo–Namib Region (Cowling and Hilton-Taylor, 1999). They are widely visited by bees and wasps, however, pollen wasp visits to Fabaceae have been recorded only in the Southwest and Northwest apart from one casual visit by a male Jugurtia to Acacia (Mimosoideae) in the Southeast (Fig. 9). In the Southwest all visits were to Aspalathus, Lebeckia or Wiborgia (Papilionoideae: Cape Crotalarieae). In this zone pollen wasps are expected visitors to these

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Fig. 11. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Boraginaceae (including Hydrophyllaceae) (group of sites in north Heliotropium tubulosum E. Mey. ex Benth.; group of sites in transition Codon royenii L.).

plants. Three species of Ceramius and three of Masarina are specialist visitors. Together with a complex of bees, they are potential pollinators of these plants (Gess and Gess, 1989, 1994a; Gess, 1996, pp. 151–160). In the Northwest apart from casual visits to Indigofera (Papilionoideae) by one species of Quartinia the recorded visits were to Adenolobium (Caesalpinoideae). Three species of Quartinia were recorded but only one of these was present in sufficient numbers at several sites to indicate a possible specialization. Adenolobium is more generally visited by bees of several families and it is bees rather than pollen wasps which are the potential pollinators. 7.6.2. Malpigiales 7.6.2.1. Euphorbiaceae. The Euphorbiaceae are listed amongst the largest families in the southern Karoo, Namaqualand–Namib and Damaraland–Kaokoveld (Cowling and Hilton-Taylor, 1999). Their flowers are not visited by pollen wasps, however, nectar collection by Priscomasaris namibiensis from the extrafloral nectaries of a

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Fig. 12. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Aptosimeae (Scrophulariaceae).

herb, Chamaesyce glanduligera (Pax) Koutnik, was observed near Bullsport . where this wasp was otherwise abundantly visiting Limeum and Gisekia (Molluginaceae), its more usual forage plants, for pollen and nectar. 7.6.3. Brassicales 7.6.3.1. Brassicaceae. Cleome (formerly in Capparaceae), a widespread genus in southern Africa, forms a common and showy component of flower communities in the Transition and North, where it is well attended by bees of several families. Visits by pollen wasps, one species of Jugurtia and three of Quartinia, were recorded but these were uncommon and were probably casual. 7.6.4. Malvales 7.6.4.1. Malvaceae: Sterculioideae. Of the Malvaceae Hermannia (Sterculioideae) only has been recorded as receiving visits from Masarinae. However, pollen wasp visits to this genus are sufficiently frequent and widespread in the Southwest and Northeast (Fig. 10) that they can be expected in these zones. So far recorded are four

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Fig. 13. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Asteraceae. Included in addition are two sites in the northeast of south, where pollen wasps were collected on Asteraceae by C.F. Jacot Guillarmod.

Jugurtia in the North and two Masarina in the Southwest. Three Jugurtia and Masarina strucki Gess are considered to be specialists and furthermore are considered, together with a complex of bees of several families, to be pollinators of these plants. Jugurtia alfkeni (du Buysson) and an undescribed Jugurtia were encountered abundantly on two species of Hermannia, most notably H. modesta (Ehrenb.) Mast., in the North from Karasburg in the southeast, northeast to Aranos, west to south of . and northwards to north of Sesfontein in the Kaokoveld. Visits to other Maltahohe plants are infrequent and probably casual. The third species of Jugurtia was found from Karibib in thornveld savanna northwest to north of Sesfontein in the Kaokoveld. The most widespread Jugurtia, J. confusa Richards, nesting in the Grahamstown district in the Southeast, obtained provision from mesems (Gess and Gess, 1980) but in Namibia, east of the Gamsberg Pass was foraging abundantly on Hermannia comosa (Burch. ex DC.), although a range of other plants was in flower.

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Fig. 14. Distribution of sampling sites at which pollen wasps were represented in flower visitor samples from Wahlenbergia Schrad. ex Roth. (including Lightfootia L’H!erit.) and Microcodon A. DC. (Campanulaceae).

The association between Masarina strucki Gess and Hermannia to which it is apparently restricted has been examined (Gess et al., 1997). M. strucki has been encountered on Hermannia in Namaqualand from Springbok south to the Olifants River Valley and from east of the escarpment northeast of Nieuwoudtville and from the western Little Karoo at Ladismith. Other records of flower visiting for M. strucki made available by M. Struck and V. Whitehead are similarly for Hermannia and are from Goegap Nature Reserve, Springbok and from Ladismith respectively. The other Masarina, M. mixta Richards, is an occasional, casual visitor; most commonly associated with but not restricted to Wahlenbergia. 7.6.4.2. Neuradaceae. Grielum and Neuradopsis were most generally visited by bees of several families, however, a masarine, Quartinia propinqua Schulthess was recorded visiting Grielum grandiflorum south of Rosh Pinah in the Transition. This is considered unusual for Q. propinqua, which is found visiting Asteraceae from the Southeast through the Southwest to the Northwest.

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7.7. Euasterids 7.7.1. Boraginaceae (including Hydrophyllaceae) Boraginaceae occur in all zones. Some species, for example the widespread and showy Anchusa capensis Thunb. attract large numbers and a wide range of bee and wasp families. However, records of visits by pollen wasps to Boraginaceae are very restricted (Fig. 11) and the number of species visited limited. Two species are an important resource for their pollen wasp visitors. In the Transition Codon royenii L. (formerly Hydrophyllaceae) appears to be the principal forage plant of Jugurtia codoni Gess (Gess et al., 1997) and of a species of Quartinia and a secondary forage plant of another Quartinia. Due to their small size in relation to the flower structure none is considered to be a pollinator. The pollinators of this plant in the Transition, Southwest and Northwest are considered to be Xylocopa species (Apidae: Xylocopinae) (Gess et al., 1997). The discovery of pollen wasp associations with Hydrophyllaceae in southern Africa is of note when considered in relation to the strong association between Pseudomasaris Ashmead and Hydrophyllaceae in western North America (summarized in Gess, 1996). In the Northwest Heliotropium tubulosum E. Mey. ex DC., an abundant plant in the drainage channels of the Central Namib, is abundantly visited by two pollen wasps, undescribed species of Jugurtia and Celonites, both of which have been recorded solely from these plants, of which it seems likely that they are pollinators. Indeed, the fore-legs of the Jugurtia show similar modifications (Gess, in prep.) to those of Trimeria Saussure associated with Heliotropium in South America (Neff and Simpson, 1985). The only other recorded visits to Boraginaceae were a single visit in the Transition by Quartinia to Trichodesma africanum (L.) Lehm., which is regularly visited by bees of several families, and a single visit by a male Celonites capensis Brauns to Ehretia rigida (Thunb.) Druce in the Grahamstown area in the Southeast. 7.7.2. Vahliaceae The single genus Vahlia is represented in the database by one species, V. capensis (L. f.) Thunb. This species has been sampled at sites from Augrabies north to the Kuiseb. Visits by bees of several families were recorded but only a single visit by a pollen wasp, Quartinia propinqua, widely associated with Asteraceae. 7.7.3. Lamiales 7.7.3.1. Acanthaceae. For the Karoo–Namib Acanthaceae are listed as one of the 10 largest plant families in the Damaraland–Kaokoveld only (Cowling and Hilton-Taylor, 1999). They are nonetheless widespread throughout the Nama Karoo. They are commonly visited by bees of several families, however, only one pollen wasp, Ceramius lichtensteinii (Klug) which specializes in mesems throughout its range, has been recorded from a species of Acanthaceae, Blepharis capensis (L. f.) Pers. at two widely separated sites in the Southeast, Grahamstown and Waterford.

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7.7.3.2. Lamiaceae. Lamiaceae are amongst the plants favoured by pollen wasps in the Palaearctic (Mauss, 1996). They occur throughout southern Africa but are most species diverse in the east. Ten species were sampled. All were visited by bees of various families but only casual visits from two pollen wasps were recorded, both in the Northeast, where incidence of casual visiting is highest. 7.7.3.3. Scrophulariaceae. The Scrophulariaceae are listed as one of the 10 largest plant families throughout the Karoo–Namib Region (Cowling and Hilton-Taylor, 1999). There is marked and widespread association between Masarinae and Aptosimeae, Aptosimum, Peliostomum and Anticharis (Fig. 12). Specialist Celonites species are considered to be the most important pollinators of these plants (Gess and Gess, 1989; Gess, 1996; Gess et al., 1997). The Quartinia visitors, with one possible exception, are not specialist visitors and are generally, except where flowers are undersized, too small to be pollinators (Gess, 1996). The highest number of masarine genera and species visiting Aptosimeae has been recorded from the transition where, in addition to species of Celonites and Quartinia, two species each of Jugurtia and Masarina are amongst the visitors, and one species each of these is considered to be a specialist and potential pollinator. Indeed in the Transition the percentage of species visiting Aptosimeae is exceptionally high, on a par with Aizoaceae and Asteraceae, including not only an exceptional number of specialist pollen wasp visitors but also an almost equal number of casual visitors with other specializations. Recorded visits by Masarinae to Selago and Phyllopodium are secondary or casual and never represent specializations. 7.7.4. Asterales 7.7.4.1. Asteraceae. The Asteraceae are listed as the largest or second largest family throughout the Karoo–Namib (Cowling and Hilton-Taylor, 1999). Generally Asteraceae are visited by a wide range of insect orders, notably Hymenoptera, Diptera, Lepidoptera, and Coleoptera. All six tribes of Asteraceae characteristic of the semi-arid areas of southern Africa are visited by a wide range of families of wasps and bees. They are widely visited by Masarinae in all zones (Fig. 13), the numbers and percentages of masarine species being similar to those for Mesembryanthema in the South and Transition but being higher in the North (31% as against 15%) where Asteraceae are widespread unlike Mesembryanthema. None specialize at the generic or specific level. The numbers and percentages of species specializing in Asteraceae though lower than the numbers and percentages visiting them reflect the same distribution pattern. Where pollen wasps specializing in Asteraceae are common, they, particularly the specialists, are probably amongst the important pollinators of the species they visit, indeed in some areas they are probably the most important pollinators (Gess, 1996, pp. 145–150). 7.7.4.2. Campanulaceae. In the Campanulaceae, the genera Wahlenbergia Schrad. ex Roth. (including Lightfootia L’He! rit.), most species diverse in the Southwest, and Microcodon A. DC., endemic to the Southwest, are visited abundantly by Masarinae

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throughout the Zone (Fig. 14) where the number and percentage of species visiting them, though far less than visiting Mesembryanthema and Asteraceae, is next highest, as too are the numbers and percentages of species specializing in them. In addition some few casual visits to Wahlenbergia but no records of specializations by pollen wasps have been recorded from the Transition. Although Wahlenbergia has been sampled in the North and Southeast no pollen wasps have been recorded visiting them in these areas. Masarinae have been shown to collect both nectar and pollen from narrow tubed Wahlenbergia and of Microcodon and to be their most important potential pollinators in the Southwest and possibly in some instances in the Transition. However, in these zones stellate flowered species are serviced by melittid bees (Gess, 1996, pp. 160–175) although pollen wasps do collect pollen from them. In the North and Southeast where pollen wasps have not been recorded from Wahlenbergia several bee taxa are involved. 7.7.4.3. Lobeliaceae. Few flower visiting records have been obtained for Lobeliaceae with the exception of Monopsis debilis (L. f.) Presl. Monopsis debilis is common in damp places in the Southwest at localities where Wahlenbergia, abundantly visited by pollen wasps, are also present. It is always visited solely by a melittid bee, Haplomelitta ogilviei (Cockerell), which is considered to be its pollinator (Gess and Gess, 1994b), never even casually by pollen wasps. Visits to Lobelia by small carpenter bees, Ceratinini (Apidae: Xylocopinae), have been recorded in both the Southwest and Southeast. At only one site near Nieuwoudtville in the Southwest was a pollen wasp found to be a visitor. At this site regular visits by Celonites, also a visitor to Wahlenbergia, and Ceratina to Lobelia linearis Thunb. were recorded.

8. Summary Taking the pollen wasps of southern Africa as a group, visits to 22 families of flowering plants have been recorded but of these only 11 families include taxa which can be considered to represent preferences: Aizoaceae: Mesembryanthema and Asteraceae are the most favoured families, each receiving visits from 42% of the species of pollen wasps for which flower visiting records are available. Of the other taxa visited, Aptosimeae (Scrophulariaceae) and Wahlenbergia (including Lightfootia) together with Microcodon each receive visits from 15% of the species, Aizoaceae: non-Mesembryanthema and Zygophyllum (Zygophyllaceae) each 12%, Cape Crotalarieae (Fabaceae: Papilionoideae) 8%, Hermannia (Malvaceae: Sterculioideae) and Geraniaceae each 5%, Molluginaceae and Boraginaceae each 4%, Crassulaceae less than 2%. Specializations of pollen wasps in southern Africa show similarities and differences between zones: Aizoaceae are visited throughout except possibly in the northeast.

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Within the Aizoaceae associations with Mesembryanthema are most numerous and widespread in the Southwest corresponding with the distribution and nodes of species diversity of this group. Correspondingly associations with non-Mesembryanthema and Molluginaceae are most numerous and widespread in the Transition and Northwest. Asteraceae are visited throughout. The percentage of associations per zone is highest in the Southeast, comparable in the Southwest and Transition and lowest in the North. By far the greatest actual number of species visiting Asteraceae was recorded from the Southwest where species diversity is greatest. Aptosimeae (Scrophulariaceae) are visited throughout. The percentage of associations per zone is highest in the Transition. Hermannia (Malvaceae: Sterculioideae) are visited throughout the Southwest and the North. The percentage associations per zone is highest in the Northwest. Wahlenbergia (Campanulaceae) are visited solely in the Southwest although Wahlenbergia is more widely distributed. Cape Crotalarieae (Fabaceae: Papilionoideae: Crotalarieae) are visited solely in the Southwest although they are more widely distributed. Zygophyllaceae are visited only in the Transition and North. The percentage of associations is higher in the Northwest. Of the Boraginaceae, Codon royenii is visited in the Transition and southern Northwest and Heliotropium tubulosum in the Central Namib. Of the Crassulaceae, the only close association is in the Transition. Specializations of flower choice by pollen wasp species throughout their distributions are generally constant.

9. Conclusion Throughout the semi-arid areas of southern Africa pollen wasps are present as users of floral resources and as potential pollinators. Their evolution paralleled that of the bees. Functionally they are ‘‘bees’’. Any ecological study , particularly any pollination ecology study, in the semi-arid areas, which includes bees but does not include pollen wasps is incomplete.

Acknowledgements Thanks are expressed to the following for much appreciated assistance: Estelle Brink, Schonland Herbarium, Albany Museum, Grahamstown, and Coleen Mannheimer and Sabine Austaller of the National Botanical Research Institute, National Herbarium of Namibia, Windhoek for identification of plant specimens; the Cape Department of Nature Conservation, the South African National Parks Board and the Ministry of Environment and Tourism, Namibia for collecting permits; NAMDEB for permission to collect in Diamond Area no. 1, Namibia; Sarah Radloff, Department of Statistics, Rhodes University for confirming the

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validity of the formula used for calculating percentage diversity of choice at the specific level for use as an index for comparison between taxa represented by differing numbers of species; and the South African Foundation for Research Development and the South African National Research Foundation for running expenses grants for fieldwork.

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