South African Journal of Botany 100 (2015) 58–62

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South African Journal of Botany

journal homepage: www.elsevier.com/locate/sajb

Hopliine beetle pollination in annual Wahlenbergia species

(Campanulaceae) from western South Africa, and the new
species W. melanops
J.C. Manning a,c,⁎, P. Goldblatt b,c, J.F. Colville d,e, C.N. Cupido a,f
a
Compton Herbarium, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, South Africa
b
B.A. Krukoff Curator of African Botany, Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
c
Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa
d
Kirstenbosch Research Centre, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, South Africa
e
Statistics in Ecology, Environment and Conservation, Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, South Africa.
f
Department of Biodiversity and Conservation Biology 7535, University of the Western Cape, Private Bag X17, Bellville, South Africa

a r t i c l e i n f o a b s t r a c t

Article history: Field exploration in western South Africa over the past 10 years has revealed the existence of an unnamed annual
Received 20 January 2015 species of Wahlenbergia Schrad. ex Roth that we describe here as W. melanops Goldblatt and J. C. Manning for the
Received in revised form 13 April 2015 dark grey center of the flower. Plants have alternate leaves scattered along the stem and are otherwise distinguished
Accepted 27 April 2015
in part by narrow calyx lobes and the presence of stylar glands at the base of the stigma lobes. Flowers of
Available online 7 June 2015
W. androsacea, W. capensis, and W. melanops conform to a specialized hopliine pollination system and we present
Edited by GV Goodman-Cron observations documenting hopliine pollination for these three species. This now confirms a third pollination system
in western South African Wahlenbergia species that includes one other specialized pollination system utilizing
Keywords: masarine (pollen) wasps and another possibly more generalist system using melittid bees. W. annuliformis Brehmer
New species is treated as a synonym of W. androsacea A. DC.
Nomenclature © 2015 SAAB. Published by Elsevier B.V. All rights reserved.
Pollination biology
Taxonomy

1. Introduction
The genus Wahlenbergia Schrad. ex Roth (Campanulaceae), with
some 260 species listed (Lammers, 2007), is by far the largest genus in
the family in the southern Hemisphere. Essentially pan-austral in distri-
bution, it includes minor incursions into the Mediterranean region,
Macaronesia, Arabia, and SE Asia.
Over 180 species are currently recorded from southern Africa
(Germishuizen and Meyer, 2003), with some 65 species in the Cape Flo-
ristic Region (Manning and Goldblatt, 2012). Recent phylogenetic anal-
yses of DNA sequence data confirm that the genus is not monophyletic
as currently circumscribed (Cupido et al., 2013; Prebble et al., 2011) but
an alternative classification has yet to be proposed.
Wahlenbergia is distinguished from related genera by a more or less
inferior ovary and mostly turbinate to subglobose capsules that dehisce
regularly through three to five terminal valves (Manning and Goldblatt,
2012). The African species were last comprehensively revised by von
Brehmer (1915), with more recent regional or partial revisions by
Adamson (1955) and Thulin (1975). One new species from Western
⁎ Corresponding author.
E-mail address: J.Manning@sanbi.org.za (J.C. Manning).
Cape has since been described by Cupido (2011). Although the taxono-
my of the genus in southern Africa is much in need of revision, a prelim-
inary list of species recognized from the Cape Floristic Region was
provided by Manning and Goldblatt (2012). This list includes just a
half-dozen annual species with three to five locules and stigma lobes.
Campanulaceae are characterized by a secondary pollination presen-
tation system involving transfer of pollen from the anthers to the present-
er region of the immature style, where it is held in place by special hairs.
This takes place in bud before the perianth expands. At expansion of the
perianth, the flower is said to be in the male phase and the stigma lobes
are not displayed and are not receptive. When most pollen is removed
from the presenter region, the flower enters the female phase and the
stigma lobes open and become receptive. The nectar at the base of the co-
rolla is covered by the accrescent bases of the stamens, which form a
dome-like structure, and nectar can only be accessed by insects strong
enough to force the filament bases apart.
Campanulaceae appear to be predominantly adapted to pollination
by bees, with many species evidently specialized for pollination by sol-
itary bees (Gess, 1996, 1999; Welsford and Johnson, 2012). This is likely
to be true in Wahlenbergia, in which most species have unmarked, pale
to deep blue flowers, sometimes with small dark markings around the
edge of the floral cup. In only two species, W. capensis and the new

http://dx.doi.org/10.1016/j.sajb.2015.04.014
0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved.
 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62
W. melanops, do the flowers have prominent dark markings that are
consistent with ‘beetle-flowers.’
Although barely known in southern Africa until the late twentieth century,
specialization for hopliine beetle (Scarabaeidae:Melolonthinae:Hopliini)
pollination has now been documented in well over 70 species in several
plant families, primarily in the Greater Cape Floristic Region (Goldblatt
and Manning, 2011), the center of diversity for the hopliines (Colville
et al., 2014). Typical floral adaptations to hopliine pollination include
shallow or open flowers with relatively large, dark markings (beetle
marks). Among Campanulaceae, only a few species of Wahlenbergia
were identified by Goldblatt and Manning (2011) in their review of
the system as potential members of this pollination guild, notably
W. capensis (L.) DC. plus a second, as yet unnamed species that we
describe here.
This distinctive annual species with three locular ovaries, which
we describe as Wahlenbergia melanops Goldblatt and J. C. Manning,
is a narrow endemic of the Atlantic coast east of Doringbaai. It is
one of just two species of Wahlenbergia with shallow flowers with
a dark central eye. This distinctive floral morphology is part of the
syndrome associated with a specialized pollination system utilizing
hopliine beetles.
At the type locality, the flowers of Wahlenbergia melanops were visit-
ed by two species of hopliine beetle, Peritrichia pseudopistrinaria Schein
and Lepithrix longitarsis Schein, individuals of which were present on nu-
merous open flowers. Hopliine pollination has been documented in only
a single species of Wahlenbergia, W. capensis (Goldblatt et al., 1998; see
also Picker and Midgley, 1996; Gess and Gess, 2010) although it is likely
in a few other species as well. Here we present observations on hopliine
pollination in W. capensis and W. annularis A. DC., the last also visited by
worker honey bees carrying Wahlenbergia-type pollen.
2. Materials and methods
The new species was described and illustrated from living plants col-
lected in the wild. No additional herbarium material was located at BOL,
NBG, or SAM. Several plants were collected and pressed for documenta-
tion, and duplicate specimens have been distributed to multiple
herbaria as listed below.
Pollinator observations were made on plants in the field at four dif-
ferent localities along the west coast of Western Cape, South Africa
(Table 1). Observer data for the four localities are: 1. Leipodtville: two
observers on warm days over the period 11:00 to 13:00 (Sep 2012)
and 10:30 to 12:00 (Sep 2013) scanned over 100 plants in flower for vis-
iting insects, and sampled beetles from ± 50 plants; 2. Doringbaai: two
observers on warm days over the period 10:30 to 12:30 (Oct 2008) and
11:30 to 13:30 (Sep 2013) scanned ± 60 plants in flower for visiting in-
sects, and sampled beetles from ± 20 plants; 3. Aurora: two observers
on a warm day over the period 12:00 to 14:00 scanned ± 20 plants in
flower, all with beetles; 4. Orange Kloof: three observers on a warm
day over the period 09:30 to 12:30 scanned ± 50 plants in flower for
visiting insects, and sampled beetles from ± 15 plants.
Table 1
Study sites, all in Western Cape, with pollinator and host plant information (less frequent hopliine visitors in parentheses). P. (Peritrichia), L. (Lepithrix), W. (Wahlenbergia). Plant vouchers
deposited at MO and NBG).
Study site Hopliine species
1. Leipoldtville (32°13.39S 18°28.713E); sandy ground; P. pseudopistrinaria (L. longitarsis, Pachynema crassipes)
Sep 2012, Sep 2013
2. Doringbaai, Farm Kliphoek (31°45.61S 18°20.91E); P. pseudopistrinaria, L. longitarsis
sandveld; Oct 2008, Sep 2013
3. 1.5 km N of Aurora (32°41.58S 18°28.93E); rocky P. pseudopistrinaria (L. lineata)
sandy slope; Sept. 2012; Sep 2013
4. Cape Peninsula, Orange Kloof (34° 00'24.83S 18°24'05.10E), P. bipilosa sp. nov.
267 m; fynbos; 16 Nov 2013
59
Beetles were hand-collected and killed by freezing or in 80% ethanol
before pinning. Voucher specimens are housed in the Kirstenbosch Re-
search Centre.
3. Results
3.1. Taxonomy
Wahlenbergia melanops Goldblatt and J. C. Manning, sp. nov. Type:
South Africa, Western Cape, 3118 (Vanrhynsdorp): sandveld east of
Doringbaai at Farm Kliphoek, 61 m, (–CD), 11 Oct. 2013, Goldblatt & Por-
ter 13997 (NBG, holo.; K, MO, PRE, iso.).
Annual from slender taproot, to 600 mm high. Stem branching from
base and above, sparsely scabrid-papillose. Leaves alternate, ±narrowly
elliptic, 30–90 × 3–9 mm, margins shallowly toothed to lightly dentate,
sparsely ciliate at base, upper leaves becoming scale-like. Inflorescence
lax, pedicels 30–70 mm long, smooth. Flowers blue-mauve with conspic-
uous grey cup edged with white. Hypanthium obconic, ± 2 mm long, 10-
nerved. Calyx lobes narrowly triangular, 3–4 mm long, ascending, tips
slightly recurved, enlarging to 5 mm in fruit. Corolla up to 24 mm long
(much shorter late in season), lobes united below for 2.5–3.0 mm in
shallow, basin-like cup, cup densely puberulous. Stamens 5, filaments ±
1.5 mm long at dehiscence, bases deltoid, ± 1 mm long, orange with
black flecks, ciliate on margins, filiform distally for 0.5 mm, bases enlarg-
ing after dehiscence and to 2 mm long at anthesis and then conspicuously
lobed at base with upper part of filament recurved and thickened; anthers
linear, 2 mm long, Ovary inferior, 3-locular; style ± slender throughout,
± 4 mm long, hirsute in upper half, with 3 transverse glands alternating
with stigma lobes; stigma lobes ± ovate, ± 1.7 × 1.2 mm, obtuse, spread-
ing horizontally, upper surface papillate. Capsules obconic, 7–9 mm long,
± 6 wide at apex, domed in center, glabrous. seeds ellipsoid, smooth,
0.6–0.8 mm long. Flowering time September to mid October (Fig.1).
Distribution and ecology: Wahlenbergia melanops has been collected
several times over the past 50 years but all collections are from essen-
tially the same locality, and it is evidently restricted to the crest of the
ridge inland of Doringbaai on the Atlantic coast of Western Cape and
south of Vredendal (Fig. 2), where it occurs on sandy flats and gentle
sandstone slopes. Population sizes vary from season to season and we
have seen hundreds of plants along the road verges and inside farm
fences in some seasons but in dry years we struggled to find more
than 25 plants.
The species has not been collected from any additional localities in
more than a century and is thus evidently a highly localized endemic.
Conservation notes: The species is known from a single ridge in a re-
gion that has been highly transformed by agriculture. Grazing by cattle
and sheep on farms along the ridge and agriculture have already nega-
tively affected the population and will likely continue to do so.
Diagnosis: Wahlenbergia melanops is an annual with alternate leaves
not clustered basally in a rosette and 5-merous flowers with a glabrous,
3-locular ovary and three broad stigma lobes, each bearing a gland at
the base. The blue-mauve flowers are shallowly bowl-shaped with a
Plant host with voucher data
W. androsacea (Goldblatt & Porter 13983).
W. melanops (Goldblatt & Porter 13997).
W. capensis (Goldblatt & Porter s.n., no voucher)
W. capensis (Colville s.n., no voucher)
60 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62
Fig. 1. Wahlenbergia melanops. A. Flowering stem; B. calyx; C. single detached stamen;
D. filament at time of anther dehiscence in bud; E. filament after flower has expanded;
F. style and stigma showing ring of three stylar glands at base of stigma lobes; H, capsule.
Scale bars: A, G. 10 mm; B, 2.5 mm; C. 2 mm; D, E, 1 mm; F, 4 mm; H. 2.5 mm.
Fig. 2. Distribution of Wahlenbergia melanops.
conspicuous grey cup, and the slender calyx lobes enlarge from 3 mm
long in the open flower to 5 mm in fruit. The mature capsules are gla-
brous, 7–9 mm long and ± twice as long as wide.
Wahlenbergia melanops is a distinctive species that might only be
confused with W. capensis and collections of the species (Hall 3182,
Van Breda 1270) were generally referred to that species. The two species
share an annual habit, cauline foliage, similar open, mauve-blue flowers
with a large grey eye but W. capensis is unique in the genus in its hispid,
5-locular ovary with five enlarged stigma lobes fertile only along the
margins. W. capensis was segregated by von Brehmer (1915) as the
monotypic sect. Capenses Brehmer but phylogenetic analyses by
Prebble et al. (2011) and Cupido et al. (2013) place it as sister to
W. cernua (Thunb.) A.DC. (sect. Cernuae Brehmer). Other annual species
with relatively large bowl-shaped flowers, such as W. androsacea A.DC.
and W. annularis A.DC., have the leaves clustered at the base of the
stems and flowers either unmarked or with a ring of small markings
around the edge of the cup.
The species appears to have been first collected by Carl Zeyher, some-
time in the first half of the nineteenth century [Zeyher s.n. (SAM)]. This
collection was misidentified as W. arenaria A. DC., now treated as a syno-
nym of W. androsacea A. DC., and was evidently overlooked by von
Brehmer (1915) in his revision of the genus.
The immediate relationships of W. melanops are difficult to assess and
it does not key to section satisfactorily in Brehmer's monograph of the
African species (von Brehmer, 1915). We initially keyed W. melanops to
sect. Dichotomae Brehmer on the basis of its oblanceolate, alternate
leaves, pedunculate flowers, and 5-locular ovary with well-developed
stylar glands but it does not have the slender, elongate stigma lobes of
the other species in the section. Alternatively, W. melanops keys to the
monotypic sect. Annuliformes Brehmer, defined by three transverse
glands forming an almost a complete ring at the base of the stigma and
short stigma lobes. The only species in the section, W. annuliformis
 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62
Brehmer, has white to pale blue petals with a white throat, and is said to
have sparsely hairy capsules.
3.1.1. Additional specimens
South Africa, Western Cape, 3118 (Vanrhynsdorp): road from Lam-
berts Bay to Vredendal, red sand dunes, (–CD), 2 Sept. 1961, Van Breda
1270 (PRE); Farm Kliphoek, 12 km inland from Doringbaai, (–CD), 29
Aug. 1970, Hall 3798 (NBG, PRE); 6 Sept. 1970, Hall 3812 (PRE); 11
Sept. 2008, Goldblatt & Porter 13107 (MO, NBG, PRE); 13 Sept. 2008.
Cupido 371 (NBG); east of Vredendal, Fonteintjie, 15 km SE of
Doringbaai, (–CD), 25 Aug. 2006, Helme 4292 (NBG).
Without precise locality: In region trans Olifantsrivier, Zeyher
SAM40417 (SAM).
3.2. Nomenclature of Wahlenbergia annuliformis
We have located and examined one of the two syntypes cited for
W. annuliformis (von Brehmer, 1915), viz. Bachmann 1729 (Z). This col-
lection closely matches W. androsacea (sect. Rosulatae Brehmer) in the
subrosulate, narrowly oblanceolate leaves, sparsely branched stems,
bowl-shaped corolla of comparable size, and three broad stigma lobes
with prominent stylar glands at the base. The essential difference be-
tween sects. Annuliformes and Rosulatae thus resides in whether the
glands form an annular collar around the style (sect. Annuliformes) or
remain as three discrete glands (sect. Rosulatae) (sect. Rosulatae). We
have examined numerous specimens of both W. annularis and
W. androsacea and find all grades from a ring of three discrete stigma
glands to a more or less continuous annulus (see also Manning and
Goldblatt, 2012). We therefore place W. annuliformis in synonymy
under W. androsacea.
Wahlenbergia androsacea A. DC., Monogr. Camp.: 150, t. 19, f. I.
Wahlenbergia annuliformis Brehmer in Bot. Jahrb. 53: 118 (1915),
syn. nov. Type: South Africa, [Western Cape], ‘umgegend von Hopefield’,
Oct. 1885, Bachmann 1729 (Z, lecto.!, designated here). [Paratype: South
Africa, [Western Cape], ‘Troe Troe’, Oct. 1883, Bachmann 343 (not
located)]
3.3. Hopliine pollination in Wahlenbergia
The observations on hopliine pollination in the shrubby
Prismatocarpus pedunculatus (P.J.Bergius) A. DC. and the annual
Wahlenbergia capensis by Goldblatt et al. (1998) evidently constitute
the first report of this pollination strategy in the family but since then
we have regularly noted hopliines on W. capensis (see also Gess and
Gess, 2010). More recently, hopliine pollination was also reported
for Roella ciliata L. by Cupido and Nelson (2012).
Our observations on hopliine pollination in annual Wahlenbergia
species confirm the association of this pollination system with dark flo-
ral markings documented by Van Kleunen et al. (2007). The unique,
large grey stigma lobes in Wahlenbergia capensis appear to mimic the
color and texture of visiting hopliine species, suggesting co-adaptation
between plant and pollinators in this species. Beetle species recorded
visiting W. capensis include Peritrichia pseudursa Schein (Gess and
Gess, 2010), to which we now add observations of visits by P. bipilosa
sp. nov. (Dombrow, in prep.) and Dicranocnemus sulcicollis Wiedem.,
from the Cape Peninsula (Fig. 3A, see also Fig. 3B), and by Lepithrix
lineata Fabricius and P. pseudopistrinaria (Fig. 3D) near Aurora
(Table 1). These beetles were observed carrying a dense covering of
the grey-blue pollen of W. capensis, which adheres to the hairs on the
beetle’s prothorax and elytra during feeding and mating. Species of
Peritrichia and Lepithrix are typically attracted to blue and white flowers,
where they have been observed to feed on pollen and nectar (Picker and
Midgely, 1996). Examination of gut contents and mouthpart morpholo-
gy has confirmed the feeding preferences of these species for pollen and
nectar (Hansal, 2014; Johnson and Nicolson, 2001).
61
Fig. 3. Hopliine pollination in Wahlenbergia. A. Pollination of W. capensis by male
Peritrichia bipilosa sp. nov. (Dombrow, in prep.) (body length = 7.24 mm) at Orange
Kloof (Photo: Annalie Melin). B. Pollination of W. capensis by two male Dicranocnemus
sulcicollis (body length = 5.10 mm) at Rondevlei on the Cape Peninsula (Photo: Sarah-
Leigh Hutchinson). C. Pollination of W. annularis by male Peritrichia pseudopistrinaria
(body length = 7.59 mm), near Leipoldtville, on the west coast (Photo: Lendon Porter).
D. Pollination of W. capensis by female Lepithrix lineata Fabricius (brown beetle, left:
body length = 9.38 mm) and female P. pseudopistrinaria (grey beetle, right; body
length = 7.42 mm) near Aurora, on the west coast (Photo: Lendon Porter).
We have also observed and captured hopliines on Wahlenbergia
annularis at Leipoldtville (Goldblatt and Porter 13983) (Fig. 3C), notably
Peritrichia pseudopistrinaria but also individuals of Lepithrix longitarsis
and Pachynema crassipes Fabricius. The beetles behaved as described by
Goldblatt et al. (1998), using the flowers as a platform to assemble, en-
gage in agonistic behavior and copulation, and not infrequently flying
from flowers of one plant to another. Their behavior, matched in hopliines
visiting W. melanops flowers, results in their becoming visibly covered in
pollen which they passively transport to other flowers. The flowers of
W. annularis are moderately sized, 15–20 mm in diameter, and pale
blue with dark longitudinal marks or streaks around the edge of the
bowl. We also recorded visits to flowers of W. annularis (but never to
those of W. melanops) by worker honey bees which collected pollen but
also acquired dorsal deposits of Wahlenbergia pollen. Gess (1996) noted
honey bees as opportunistic visitors of several Wahlenbergia species and
considered them as unreliable pollinators. This was not supported by ob-
servations on two Wahlenbergia species in the KwaZulu-Natal Drakens-
berg, in which solitary halictid bees and social honey bees were
frequent and effective pollinators (Welsford and Johnson, 2012).
We observed that the beetles landed on the flower and then imme-
diately crawled to the base of the style with their heads downward,
sometimes proceeding to move around the base of the style. This sug-
gests to us that the beetles were feeding on the nectar held at the base
of the style but we are unable to confirm this. We saw no evidence of de-
structive feeding by the beetles, nor were they observed to feed on the
pollen during the male phase of the flowers.
Two pollination systems were documented among southwestern
Cape Wahlenbergia species by Gess (1996). Species with deeply cam-
panulate flowers, including W. paniculata A.DC., were pollinated by
masarine wasps (Vespidae: Celonites) (Gess, 1996), and those with shal-
lowly campanulate flowers, e.g., W. annularis and W. namaquana Sond.,
were visited by as many as 19 species of bees and wasps but pollinated
primarily by melittid bees (Melittidae: Capicola). We conclude that the
pollination strategy of W. capensis and W. melanops represents a third
62 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62
pollination type that conforms to the specialized hopliine system in
southern Africa, i.e., shallowly campanulate flowers with dark central
markings darker band of color. W. annularis appears to belong to the
class of more generalist flowers but in this species transfer by hopliine
beetles is also important.
Acknowledgements
We thank Lendon Porter for his assistance and companionship in the
field, and Anthony Magee and Michelle Smith for help in preparing the il-
lustrations. Peter Linder (Z) kindly provided a scan of the type of
W. annuliformis. Cape Nature provided a beetle-collecting permit (Permit
No.: AAA007-0081-0056). J.F.C. is supported by a National Research Foun-
dation RCA-Fellowship (grant no. 91442).
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