Plants pollinated by Hemipepsis wasps. (a) Female H. capensis visiting Asclepias macropus , Wahroonga Farm; (b) Male H. capensis visiting Pachycarpus campanulatus , Bushman's Nek. Note the pollinaria attached to tarsal claws (indicated by arrows); (c) Female H. capensis visiting Aspidoglossum glanduliferum , Wahroonga Farm; (d) Male H. errabunda visiting Periglossum angustifolium , Midmar Nature Reserve. Note the pollinaria attached to the mouthparts (indicated by arrow); (e) Hemipepsis sp. visiting Woodia mucronata , Hogsback; (f) Xysmalobium stockenstromense inflorescence. All scale bars = 10 mm. 

Contexts in source publication

Context 1

... pollination biology of southern African asclepiads (Apocynaceae subfamily Asclepiadoideae sensu Endress and Bruyns, 2000) is remarkably poorly studied compared with other regions, especially North America (see reviews by Wyatt and Broyles, 1994; Ollerton and Liede, 1997). The asclepiads have diversified tremendously in southern African grasslands, and South Africa is considered a centre of diversity and endemism for this group of plants (Victor et al., 2000). Approxi- mately 600 species are currently described for southern Africa with 87% of these endemic to the region (Cowling and Hilton- Taylor, 1997; Victor et al., 2000). Knowledge of pollinator requirements is essential for conservation planning, especially given the high rates of habitat transformation in many of South Africa's grasslands. Our current knowledge of the diversity of pollination systems in southern African asclepiads, apart from the succulent carrion-flower stapeliads and the genus Ceropegia (tribe Ceropegieae, see review by Meve and Liede, 1994; Ollerton et al., 2009), is somewhat limited. The earliest documented studies of asclepiad pollination in South Africa include descriptions of floral visitors to Gomphocarpus , Periglossum and Woodia mucronata (then known as Xysmalobium linguaeforme ) in the Eastern Cape and on Table Mountain (Weale, 1873; Scott-Elliot, 1891). More recent studies have revealed a diversity of often specialized pollination systems within southern African asclepiads. These include specialized pollination by birds (Pauw, 1998), chafer beetles (Ollerton et al., 2003; Shuttleworth and Johnson, 2008), pompilid wasps (Shuttleworth and Johnson, 2006, 2008, 2009a,b,c), vespid wasps (Coombs et al., 2009) and possibly bees (Ollerton et al., 2003). Generalist insect pollination has also been described for several species (Liede and Whitehead, 1991; Ollerton et al., 2003). Nonethe- less, pollination systems are known for a total of only 18 southern African asclepiad species excluding stapeliads and members of the genus Ceropegia . This study documents floral visitors (and likely pollinators) to a further 15 species of South African asclepiads in the genera Asclepias , Aspidoglossum , Miraglossum , Pachycarpus , Periglossum , Woodia and Xysmalobium . Rates of visitation to many of these species are typically low and visitor observations are consequently limited for some species. However, these have been included as they provide a valuable starting point for subsequent research. Furthermore, both Woodia species are listed as rare in the Red Data List of southern African plants (Hilton-Taylor, 1996) and knowledge of their pollinator requirements is essential for their conservation. This study examined the pollination ecology of 15 perennial species of grassland asclepiad (Apocynaceae subfamily Asclepiadoideae sensu Endress and Bruyns, 2000) in the genera Asclepias , Aspidoglossum , Miraglossum , Pachycarpus , Periglossum , Woodia and Xysmalobium (Table 1; Figs. 1 and 2). Plant identifications were carried out with the assistance of Ashley Nicholas (University of KwaZulu-Natal, Westville) and were based on Langley (1980), Kupicha (1984), Smith (1988), Goyder (1998) and Nicholas (1999). Two of these species, Woodia mucronata and W. verruculosa , are listed as rare in the Red Data List of southern African plants (Hilton-Taylor, 1996). Voucher specimens of the species studied are deposited in the NU Herbarium (University of KwaZulu-Natal, Pietermaritzburg). This study was conducted over the course of five flowering seasons (between 2004 and 2009; see Table 1) at 12 sites in South Africa (Table 2). Floral visitors were recorded for all species and, where possible, representative specimens were collected for subsequent identification (Table 1). Pollen loads were determined for all collected individuals using a dissecting microscope. In some instances individual insects were inspected for pollinaria in the field and released. Representative insect specimens are deposited in the Natal Museum (Pietermaritzburg). The behaviour of pollinators and mechanism of pollinarium attach- ment was noted for species where sufficient visits were observed. Pompilid wasps were identified using keys given in Arnold (1932), Day (1979) and Goulet and Huber (1993). Chafer beetles were identified using Holm and Marais (1992). Visits by the beetle Atrichelaphinis tigrina to Pachycarpus concolor were inferred from the presence of the highly dis- tinctive Pa. concolor pollinaria on individual beetles that were collected on the sympatrically occurring asclepiad Xysmalobium undulatum as part of a separate study (see Shuttleworth and Johnson, 2008). Visitors identified as Hemipepsis spp. (Table 1) are all individuals of one of the following species: H. capensis , H. errabunda or H. hilaris . These wasps are familiar to the authors from previous fieldwork but can usually only be identified to species where the individuals were collected or photographed. Total nectar production over a 24 h period was measured for five of the study species (Table 3). Flowers were bagged for 24 h prior to nectar sampling except for Pachycarpus campanulatus where plants were collected and kept in vases in the laboratory overnight (nectar present at the beginning of the 24 h period was removed with capillary tubes). The volume and the concentration (percentage sucrose equivalent by weight) of nectar were measured with 20 μl capillary tubes and a Bellingham and Stanley (0 – 50%) hand-held refractometer. Means were calculated per flower for each plant and these values used to calculate a grand mean for the species (see Table 3 for sample sizes). Floral visitors suggest four distinct pollination systems in the species studied (Table 1): (1) pollination by Hemipepsis wasps (Hymenoptera: Pompilidae) in Asclepias macropus , Aspidoglossum glanduliferum , Miraglossum pulchellum , Pachycarpus campanulatus , Periglossum angustifolium , Woodia verruculosa , W. mucronata and Xysmalobium stockenstromense (Fig. 1); (2) pollination by chafer beetles (Scarabaeidae: Cetoniinae) in Pa. concolor , Pa. scaber and Pachycarpus sp. nov. (Fig. 2); (3) pollination by honeybees ( Apis mellifera , Hymenoptera: Apidae) in Asc. dregeana and Asc. gibba (Fig. 2); and, (4) pollination by flies in X. parviflorum (Fig. 2). The pollination system of Asc. crispa is unclear, but this species appears to be a generalist insect-pollinated species. Pollinaria were found on representative visitors to 11 of the 15 (73%) plant species studied (see Table 1 for summary and placement of pollinaria on insects). For eight of these plant species, pollinaria were carried by visitors belonging to a single functional group. Hemipepsis wasps approach flowers with a zigzag flight path typical of insects tracking an odour plume (Raguso, 2006). In Pa. campanulatus , the flowers face down and wasps land on the outside of the corolla and crawl inside the large flowers. Once inside, the shape of the corona lobes forces the wasps to hang from the central column in order to access nectar (Fig. 1b) and in so doing, pollinaria are attached to their claws. In Asc. macropus , nectar gathers in the upward facing cup formed by the corona lobes. The small size of the flowers means that wasps accessing nectar from a particular flower cling to adjacent flowers and get pollinaria from these flowers attached to their claws (Fig. 1a). In Asp. glanduliferum , wasps land on the small flowers and hang below them whilst lapping the nectar (Fig. 1c). Pollinia are presumably attached to their mouthparts, although this was not actually observed. Weale (1873) provides detailed descriptions of wasp behaviour on W. mucronata (Fig. ...

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... to Pachycarpus concolor and Pachycarpus sp. nov. were too limited to enable visitor behaviour to be described. In Pa. concolor , the widely spaced anther wings (forming the guide rails; Fig. 1f) combined with the placement of pollinaria on the tibiae and tarsi of visiting beetles suggests that the entire leg of the insect is trapped whilst accessing nectar. In Pa. scaber , the corona lobes curve back over the central column (Fig. 2b) and nectar gathers between ridges at the base of the corona lobe. Visiting beetles are thus forced to access the nectar from between the corona lobes (Fig. 2b). In doing so the palps are trapped between the guide rails and pick up the pollinaria. In Asc. dregeana , flowers are suspended in an umbelliform inflorescence which faces down. Honeybees fly into the flowers from below and hang from the central column whilst probing for nectar. During this process, pollinaria are attached to the claws as these get trapped between the guide rails (Fig. 2a). Observations of visits to Asc. gibba were insufficient to describe pollinator behaviour. In X. parviflorum , the flowers are small and nectar appears to gather in the bottom of the cup formed by the corolla lobes (Fig. 2e). Flies visiting the flowers probe the base of the corolla, during which pollinaria are attached to their mouthparts and proboscides (Fig. 2e). Pachycarpus concolor and Pa. scaber (both chafer- pollinated) produced large amounts (3.7 and 6.6 μl respectively) of nectar with a concentration of 37% and 28% respectively (Table 3). Pa. campanulatus ( Hemipepsis wasp pollinated) produced less nectar with a lower concentration (Table 3). The two honeybee-pollinated species ( Asc. dregeana and Asc. gibba ) produced smaller amounts of nectar, but the concentration of Asc. dregeana nectar (54%) was considerably higher than that of Asc. gibba (36%; Table 3). The results of this study suggest that most of the asclepiad species studied have pollination systems which are highly specialized at the level of functional group. These groups are Hemipepsis pompilid wasps (for eight species of asclepiads), chafer beetles (for three species), honeybees (for two species) and flies (for one species) (Table 1). However, confirmation of the pollinator spectrum for some of the study species requires a larger sample of flower visitors and these results should thus be considered to be preliminary. Pollination by Hemipepsis pompilid wasps is now known for several South African asclepiads and these insects appear to be especially important as asclepiad pollinators within the region (Ollerton et al, 2003; Shuttleworth and Johnson, 2006, 2008, 2009a,b,c). Visitor observations and pollen load data are reasonably comprehensive for Asclepias macropus (Fig. 1a), Pachycarpus campanulatus (Fig. 1b) and Periglossum angustifolium (Fig. 1d), and these three species are clearly pollinated exclusively by these wasps (Table 1). Pollination by Hemipepsis wasps has not previously been described in the genus Asclepias but specialized pollination by these wasps is known in four other Pachycarpus species ( Pa. appendiculatus , Pa. asperifolius , Pa. grandiflorus and Pa. natalensis ; see Ollerton et al, 2003; Shuttleworth and Johnson, 2006, 2009a,c). The role of Hemipepsis wasps as the pollinators of Pe. angustifolium is consistent with early observations by Weale (1873) of visits by “ a large black and yellow wasp ... Pallosoma , one of the Pepsidae ” to Periglossum in the Eastern Cape. The genus Pal- losoma Lepeletier 1845 referred to by Weale (1873) is a synonym for Hemipepsis Dahlbom 1844 (Arnold, 1932). In addition, Pe. angustifolium pollinia have been found inserted between the guide rails of another exclusively Hemipepsis wasp pollinated species ( Xysmalobium orbiculare ) at a site near Midmar Nature Reserve (Shuttleworth and Johnson, 2009b; A. Shuttleworth, unpubl. data). Observations of visitors to flowers of Aspidoglossum glanduliferum , Miraglossum pulchellum , Woodia verruculosa , W. mucronata and Xysmalobium stockenstromense were more limited (Table 1). However, Hemipepsis wasps were the only insects observed to visit these plants (except for a single chafer beetle on W. mucronata ) and the floral characteristics of these species (see Fig. 1) appear to be consistent with a guild of cryptic flowers that are pollinated by Hemipepsis wasps (Ollerton et al., 2003; Johnson, 2005; Johnson et al., 2007; Shuttleworth and Johnson, 2006, 2008, 2009a,b,c,d). Pollination by Hemipepsis wasps is known for two other Miraglossum species ( M. verticillare and M. pilosum ) and two other Xysmalobium species ( X. orbiculare and X. undulatum ; Ollerton et al, 2003; Shuttleworth and Johnson, 2008, 2009b). Hemipepsis wasps have also been observed visiting M. anomalum (S.D. Johnson, unpubl. data). Weale (1873) provides detailed descriptions of the behaviour of “ Pallosoma ” (now Hemipepsis ) wasps on “ ? Xyomalobium [sic.] linguaeforme ? ” in the Eastern Cape. “ Xyomalobium linguaeforme ” presumably refers to Xysmalobium linguaeforme Harv ex. Weale which has subsequently been classified as Woodia mucronata (Victor et al., 2000, 2003). The results of our study, supplemented with Weale's (1873) observations, suggest that Woodia mucronata is indeed a Hemipepsis wasp specialist and it seems likely that W. verruculosa is similarly reliant on Hemipepsis wasps. Specialized pollination by chafer beetles (Scarabaeidae: Cetoniinae) has been described in three South African asclepiads ( Asclepias woodii , Sisyranthus trichostomus and Xysmalobium involucratum ; Ollerton et al., 2003). We suggest that specialized chafer pollination systems also occur in the genus Pachycarpus . Our observations for Pa. scaber are relatively comprehensive and this species appears to be pollinated almost exclusively by the chafer Cyrtothyrea marginalis (Fig. 2b) although a single monkey beetle (Scarabaeidae: Rutelinae) was also found to be carrying pollinia (Table 1). Visitor observations to Pa. concolor and Pachycarpus sp. nov. (Fig. 2d, f) were more limited, but suggest that these species are pollinated primarily by the chafer beetle Atrichelaphinis tigrina . Apart from chafer beetles, Pachycarpus sp. nov. was also visited by a large number of flies (Table 1). However, we believe the delicate nature of the flies' legs makes them unlikely to systematically remove and insert pollinaria on the large and relatively robust flowers (Fig. 2d), although we cannot rule out the possibility that flies may contribute to the pollination of this species. Pachycarpus sp. nov. is currently known from only a single site near the village of Highflats in KwaZulu-Natal (M. Glenn, J. Lamb, A. Nicholas and A. Shuttleworth, unpubl. data) and its pollinator requirements should be assessed for its conservation. In the case of Pa. concolor , only a single visit by A. tigrina was observed. However, a large number of these beetles were collected on the sympatric X. undulatum and found to be carrying Pa. concolor pollinaria (Table 1). Furthermore, the pollinaria on these beetles were frequently reduced to just the corpusculum suggesting successful insertion of individual pollinia in Pa. concolor flowers. Pachycarpus concolor pollinia are considerably larger than the stigmatic grooves on X. undulatum flowers and were thus unlikely to have been inserted into the grooves of these flowers. Furthermore, Pa. concolor pollinia were never discovered inserted in X. undulatum flowers from Midmar Nature Reserve when these were being inspected for removal and insertion rates of pollinia in a separate study (see Shuttleworth and Johnson, 2008). The flowers of X. undulatum are very attractive to A. tigrina beetles (Shuttleworth and Johnson, 2008) and the presence of a large X. undulatum population alongside the population of Pa. concolor at Midmar Nature Reserve may partly explain the low visitation rates of A. tigrina to Pa. concolor at this site (Table 1). Pollination by bees (honeybees and halictids) has been suggested for Aspidonepsis diploglossa and Asc. cucullata (Ollerton et al., 2003). Our observations suggest that Asc. dregeana (Fig. 2a) and Asc. gibba (Fig. 2b) are pollinated primarily by honeybees (Table 1). Honeybees were the most abundant of the visitors to both species and appeared to be the most important pollen vectors (Table 1). However, a single chafer beetle ( A. tigrina ) was collected carrying Asc. gibba pollinia and these beetles may also contribute to the pollination of this species. Myophily in asclepiads has typically been associated with the succulent stapeliads and members of the genus Ceropegia (Asclepiadoideae: Ceropegieae sensu ; Endress and Bruyns, 2000; see review by Meve and Liede, 1994; Ollerton et al., 2009). Our observations suggest that X. parviflorum is pollinated exclusively by flies (Fig. 2e). This is consistent with the results of pollinator observations reported for this species by Johnson et al. (in press). This therefore represents the first record of myophily outside of the stapeliads and the genus Ceropegia in a southern African asclepiad. Xysmalobium parviflorum has a very powerful faecal odour (resulting from the production of high levels of p -Cresol by the flowers; A. ...

Context 3

... visitors suggest four distinct pollination systems in the species studied (Table 1): (1) pollination by Hemipepsis wasps (Hymenoptera: Pompilidae) in Asclepias macropus, Aspido- glossum glanduliferum, Miraglossum pulchellum, Pachycar- pus campanulatus, Periglossum angustifolium, Woodia verruculosa, W. mucronata and Xysmalobium stockenstro- mense (Fig. 1); (2) pollination by chafer beetles (Scarabaeidae: Cetoniinae) in Pa. concolor, Pa. scaber and Pachycarpus sp. nov. (Fig. 2); (3) pollination by honeybees (Apis mellifera, Hymenoptera: Apidae) in Asc. dregeana and Asc. gibba (Fig. 2); and, (4) pollination by flies in X. parviflorum (Fig. 2). The pollination system of Asc. crispa is ...

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... approach flowers with a zigzag flight path typical of insects tracking an odour plume (Raguso, 2006). In Pa. campanulatus, the flowers face down and wasps land on the outside of the corolla and crawl inside the large flowers. Once inside, the shape of the corona lobes forces the wasps to hang from the central column in order to access nectar (Fig. 1b) and in so doing, pollinaria are attached to their claws. In Asc. macropus, nectar gathers in the upward facing cup formed by the corona lobes. The small size of the flowers means that wasps accessing nectar from a particular flower cling to adjacent flowers and get pollinaria from these flowers attached to their claws (Fig. 1a). In ...

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... to access nectar (Fig. 1b) and in so doing, pollinaria are attached to their claws. In Asc. macropus, nectar gathers in the upward facing cup formed by the corona lobes. The small size of the flowers means that wasps accessing nectar from a particular flower cling to adjacent flowers and get pollinaria from these flowers attached to their claws (Fig. 1a). In Asp. glanduliferum, wasps land on the small flowers and hang below them whilst lapping the nectar (Fig. 1c). Pollinia are presumably attached to their mouthparts, although this was not actually observed. Weale (1873) provides detailed descriptions of wasp behaviour on W. mucronata (Fig. 1e). Visits to Pachycarpus concolor and ...

Context 6

... in the upward facing cup formed by the corona lobes. The small size of the flowers means that wasps accessing nectar from a particular flower cling to adjacent flowers and get pollinaria from these flowers attached to their claws (Fig. 1a). In Asp. glanduliferum, wasps land on the small flowers and hang below them whilst lapping the nectar (Fig. 1c). Pollinia are presumably attached to their mouthparts, although this was not actually observed. Weale (1873) provides detailed descriptions of wasp behaviour on W. mucronata (Fig. 1e). Visits to Pachycarpus concolor and Pachycarpus sp. nov. were too limited to enable visitor behaviour to be described. In Pa. concolor, the widely spaced ...

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... from these flowers attached to their claws (Fig. 1a). In Asp. glanduliferum, wasps land on the small flowers and hang below them whilst lapping the nectar (Fig. 1c). Pollinia are presumably attached to their mouthparts, although this was not actually observed. Weale (1873) provides detailed descriptions of wasp behaviour on W. mucronata (Fig. 1e). Visits to Pachycarpus concolor and Pachycarpus sp. nov. were too limited to enable visitor behaviour to be described. In Pa. concolor, the widely spaced anther wings (forming the guide rails; Fig. 1f) combined with the placement of pollinaria on the tibiae and tarsi of visiting beetles suggests that the entire leg of the insect is ...

Context 8

... to their mouthparts, although this was not actually observed. Weale (1873) provides detailed descriptions of wasp behaviour on W. mucronata (Fig. 1e). Visits to Pachycarpus concolor and Pachycarpus sp. nov. were too limited to enable visitor behaviour to be described. In Pa. concolor, the widely spaced anther wings (forming the guide rails; Fig. 1f) combined with the placement of pollinaria on the tibiae and tarsi of visiting beetles suggests that the entire leg of the insect is trapped whilst accessing nectar. In Pa. scaber, the corona lobes curve back over the central column (Fig. 2b) and nectar gathers between ridges at the base of the corona lobe. Visiting beetles are thus ...

Context 9

... Pollination by Hemipepsis pompilid wasps is now known for several South African asclepiads and these insects appear to be especially important as asclepiad pollinators within the region ( Ollerton et al, 2003;Shuttleworth and Johnson, 2006, 2008, 2009a. Visitor observations and pollen load data are reasonably comprehensive for Asclepias macropus (Fig. 1a), Pachycarpus campanulatus (Fig. 1b) and Periglossum angu- stifolium (Fig. 1d), and these three species are clearly pollinated exclusively by these wasps (Table 1). Pollination by Hemi- pepsis wasps has not previously been described in the genus Asclepias but specialized pollination by these wasps is known in four other Pachycarpus ...

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... wasps is now known for several South African asclepiads and these insects appear to be especially important as asclepiad pollinators within the region ( Ollerton et al, 2003;Shuttleworth and Johnson, 2006, 2008, 2009a. Visitor observations and pollen load data are reasonably comprehensive for Asclepias macropus (Fig. 1a), Pachycarpus campanulatus (Fig. 1b) and Periglossum angu- stifolium (Fig. 1d), and these three species are clearly pollinated exclusively by these wasps (Table 1). Pollination by Hemi- pepsis wasps has not previously been described in the genus Asclepias but specialized pollination by these wasps is known in four other Pachycarpus species (Pa. appendiculatus, Pa. ...

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... asclepiads and these insects appear to be especially important as asclepiad pollinators within the region ( Ollerton et al, 2003;Shuttleworth and Johnson, 2006, 2008, 2009a. Visitor observations and pollen load data are reasonably comprehensive for Asclepias macropus (Fig. 1a), Pachycarpus campanulatus (Fig. 1b) and Periglossum angu- stifolium (Fig. 1d), and these three species are clearly pollinated exclusively by these wasps (Table 1). Pollination by Hemi- pepsis wasps has not previously been described in the genus Asclepias but specialized pollination by these wasps is known in four other Pachycarpus species (Pa. appendiculatus, Pa. asperifolius, Pa. grandiflorus and Pa. ...

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... to flowers of Aspidoglossum glanduliferum, Miraglossum pulchellum, Woodia verruculosa, W. mucronata and Xysmalobium stockenstromense were more limited (Table 1). However, Hemipepsis wasps were the only insects observed to visit these plants (except for a single chafer beetle on W. mucronata) and the floral characteristics of these species (see Fig. 1) appear to be consistent with a guild of cryptic flowers that are pollinated by Hemipepsis wasps ( Ollerton et al., 2003;Johnson, 2005;Johnson et al., 2007;Shuttleworth and Johnson, 2006, 2008, 2009a). Pollina- tion by Hemipepsis wasps is known for two other Miraglossum species (M. verticillare and M. pilosum) and two other Xys- ...