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Journal of East African Natural History 97(1): 33–42 (2008)
POLLINATION OBSERVATIONS OF THE AFRICAN VIOLET IN
THE TAITA HILLS, KENYA
Dino J. Martins
Museum of Comparative Zoology, Harvard University
26 Oxford Street, Cambridge, MA 02138, USA
dinojmv@oeb.harvard.edu
ABSTRACT
The African violet, Saintpaulia teitensis (Gesneriaceae), is an Eastern Arc global
biodiversity hotspot endemic. Forest fragments on the Taita Hills in south-eastern
Kenya hold the only known wild populations of this plant. The pollination ecology of
S. teitensis was investigated through direct observation. S. teitensis flowers show
enantiostyly which may promote xenogamy. Pollinators of this endangered plant
species were found to be exclusively wild bee species of the genus Amegilla (Apoidea:
Aprocrita: Apidae). Four different species of Amegilla were recorded visiting
S. teitensis. Observations of bee floral visitors showed distinctive floral manipulation
(buzz pollination) for release of pollen by pollinating bees. Amegilla spp. visiting
S. teitensis were observed to feed from other forest-floor plant species (Acanthaceae
and Lamiaceae) and on crops in adjacent small-scale mixed agriculture farms. Future
conservation and management of this endangered plant needs to take into account the
needs and biology of its pollinators.
Keywords: Buzz pollination, enantiostyly, Saintpaulia, Eastern Arc, Gesneriaceae,
Amegilla
INTRODUCTION
The Taita African Violet, Saintpaulia teitensis B.L.Burtt, is endemic to the Taita Hills
(Burtt, 1958; 1964), which are part of the Eastern Arc biodiversity hotspot. East of the main
range is Mbololo Hill (1779 m) where the largest remnant patch of forest is located (Bennun
& Njoroge, 1999). The only known populations of this rare plant are found on Mbololo Hill
in the higher parts of the forest (Faden et al., 1988; Darbyshire 2006). This biodiversity
hotspot consists largely of highly fragmented and relict forest patches on hills and mountains
with smaller areas of forest along the coast of Kenya and Tanzania. The Taita Hills in Kenya
are considered the northernmost outlier of the Eastern Arc biodiversity hotspot. The term
‘Eastern Arc’ was introduced in 1986 by Lovett to describe this exceptionally species-rich
area spanning southern Kenya and eastern Tanzania (Lovett 1986). It has been suggested that
as much as a third of the flora of forest regions of Eastern Tanzania and Kenya is endemic to
the floristic regions that cover the Eastern Arc (Lovett 1990).
The hills are surrounded by flat plains covered in dry, arid bushland dominated by
Acacia spp. (Acacia tortilis (Forssk.) Hayne, A. siebierana DC., A. senegal (L.) Willd.,
34 D.J. Martins
A. nilotica (L.) Delile, A. zanzibarica (S.Moore) Taub.) and Commiphora spp. This
bushland with scattered trees (Melia and Ficus spp.) extends up onto the flanks of the
hills giving way to intensive small-scale agriculture. The farms are typically small and
grow a wide range of subsistence crops alongside fruit trees, climbers such as passion-
fruit (Passiflora edulis Sims) and tubers, primarily cassava (Manihot esculenta Crantz)
and yams. Maize (Zea mays L.) is the most conspicuous and dominant crop. The land is
intensively cultivated with almost no natural forest habitat left in the farming zone. Many
farms have strips of wildflowers along hedgerows and small orchards with fruit trees.
As a result of many decades of intensive farming, the forests of the Taita Hills survive
only as fragmented patches on the hilltops and in general on slopes and areas inaccessible for
cultivation. The forest patches on the Taitas range in size from a few hectares to over 200
hectares (Beentje & Ndiang’ui, 1988; Bennun & Njoroge, 1999).
The genus Saintpaulia H.Wendl. is of regional interest to conservation especially as a
potential flagship species for the Eastern Arc. Several efforts have been made to improve the
first comprehensive treatment of the genus by Burtt (1958; 1964), including through the use
of molecular systematics (Möller & Cronk, 1997a, b; Smith, 1997; Linqvist & Albert, 1999;
Harrison et al., 1999). The taxonomy of the genus remains controversial at the species level
but has been recently revised and incorporated into the published Flora of Tropical East
Africa (Darbyshire, 2006).
The restricted distribution in highly-threatened and isolated fragmented forest is typical of
the genus (Johansson, 1978; Clarke, 1998; Eastwood et al., 1998; Kohlemainen &
Mutikainen, 2006). Mbololo Hill holds the largest contiguous area of forest in the Taita Hills
and is also home to a number of other endemics, including several birds, butterflies and an
amphibian (Collins & Morris, 1985; Faden et al., 1988; Simiyu et al., 1996). The Taita
African Violet is a shade-loving plant that grows in sheltered spots on rocks, amongst tree-
roots and occasionally on the lower trunks of moss-covered trees.
Saintpaulia pollination biology has been little studied in the field (Kolehmainen &
Mutikainen, 2006). Given the restricted range of S. teitensis in a fragmented habitat, the
maintenance of pollination services could potentially be one of the main areas of concern for
the persistence of the species. Plants in forest fragments that are impacted by human
activities are particularly vulnerable to pollination deficits (Buchmann et al., 1997). In order
to establish the necessity of pollination to the survival of this species, information on the
floral visitors and their behaviour is required.
The aim of this study was to document the floral visitors (hence potential pollinators) of
the African Violet, S. teitensis. The main questions asked were: What insects are visiting the
flowers of S. teitensis? What are the patterns of visitation? And, how many different kinds of
visitors come to the flowers and what does their behaviour at the flowers tell us about the
interactions of the pollinators with this plant species i.e. if only a few species of insect
pollinators are involved, does this suggest a specialised guild? An additional aim of the study
was to observe closely the behaviour of floral visitors to the flowers of S. teitensis in order to
confirm the hypothesis of buzz pollination being the means of displacing pollen from the
anthers in this species. Once the identity of the floral visitors to S. teitensis was established, a
further question of what other species of plants the same insects are visiting was also asked.
This would help link the pollination of the plant with the broader context of the floral
community and put this information into the context of state of the fragmented habitat and
adjacent small-scale agriculture.
Pollination of Saintpaulia teitensis 35
MATERIALS AND METHODS
Morphological observations of floral form and variation were made in order to better inform
observation during fieldwork. Herbarium specimens of Saintpaulia teitensis and other species
of Gesneriaceae were studied at the East African Herbarium and at the Harvard University
Herbarium in order to determine the structure of the flowers e.g. enclosed anthers. Close
observations were also made of a number of species of Saintpaulia, including S. teitensis,
maintained in cultivation at the National Museums of Kenya and in the collections of plant-
enthusiasts. A number of flowers were bagged, to exclude pollinators, so as to determine the
role played by flower-visitors in pollination.
Individual plants of S. teitensis were watched in the wild for visitors. All observations
were carried out on Mbololo from 15 July to 10 August 2001, 15 May to 10 August 2003
and 15 to 17 June 2004. Plants were visited on 10 days, and watched closely for visitors on
three days. Individual plants bearing flowers were searched out and carefully observed from
early morning ca.7.00 am to mid-afternoon. This time period was observed to correspond
with the main activity patterns of flower-visiting diurnal insects based on pilot day-long
observations in July–August 2001.
Plants were watched from a short distance in order not to disturb the pollinating bees.
Some observations were carried out through a pair of close-focusing binoculars (Nikon
Pentax 8 x 40). Dull-coloured clothing was worn and unnecessary movement avoided when
conducting the observations. Close observations were made of bee behaviour at flowers. The
duration of visits as well as the number of flowers visited were recorded and tabled in
spreadsheets. Analysis of S. teitensis flower-visitation patterns was carried out using
spreadsheets in Excel.
Small numbers of bees were also captured by netting them as they approached or departed
from S. teitensis flowers and at other flowers near by when the same species had been seen
visiting the S. teitensis flowers earlier. No netting of bees was done at the flowers being
studied so as not to negatively impact on visitation rates and/or startle and scare the bees
away. This approach was found to be effective in studies of pollinator communities in the
adjacent Tsavo ecosystem and of hawkmoths pollinating orchids (Martins, 2004; Martins &
Johnson, 2007).
These bees were checked for pollen loads using the fuschin gel method (Beattie, 1971).
These fuschin gel pollen extractions were later melted onto glass slides and observed through
a simple monocular light microscope to confirm that the pollen was coming from the
Saintpaulia flowers. Bees were identified by the author up to the genus level on the basis of a
key developed for the African Bee Course by Dr Connal Eardley. Species level
identifications were done by Dr. Connal Eardley on the basis of digital images and of
mounted specimens by the late hymenoptera taxonomist Roy Snelling. Specimens have been
sent to Dr Eardley at ARC-PPRI in South Africa and will also be deposited at the National
Museums of Kenya.
RESULTS
Floral biology of Saintpaulia teitensis
The flowers of S. teitensis are borne on short stalks. These extend above or outwards from
the rosette of leaves if the plant is growing on a vertical rock or trunk face. Typically 2–3
flowers are open and viable per flowering spike, with up to 10 open flowers on a plant.
36 D.J. Martins
S. teitensis bears bilaterally symmetrical flowers. Of a total of 20 bagged flowers, 19 did not
set fruit, and one developed a small fruit that withered and aborted before ripening. Of 17
out-crossed flowers in the related S. ionantha, 15 set fruit and developed to maturity.
The individual flower consists of an arrangement of five partly fused petals in a bilaterally
symmetrical display with the yellow anthers in the middle contrasting with the surrounding light
blue-purple petals (Martins, 2005). S. teitensis also shows an interesting floral feature known as
enantiostyly. Enantiostyly is a form of flower polymorphism where the style projects away
from the symmetric plane of the flower. In S. teitensis this feature is heteromorphic, with the
style projecting either to the left (left-styled) or right (right-styled) to the main axis of the
flower (figure 1), with both kinds of flowers on the same plant. Heteromorphic enantiostyly
was observed on all individual S. teitensis plants studied and is typically in a 1:1 ratio of left-
styled to right-styled flowers. (N= 20 plants observed in flower).
Figure 1. Enantiostyly: left- and right-styled flowers of Saintpaulia teitensis.
The pollen is contained within the bright yellow anthers, which are a fused structure. This
structure needs to be specially manipulated by a pollinator in order for the pollen to be
released. In contrast with the bright yellow anthers, the pollen grains of S. teitensis are white in
colour.
Pollination of Saintpaulia teitensis
Pollen grains of S. teitensis are spherical and adhere readily to the hairs of the Amegilla bees
that visit it. Observations of visitors to flowers were made on 10 days, with specific visitation
data collected over 8 hour periods for three days (figure 3). We only observed Amegilla bees
visiting S. teitensis flowers. The bees approach the flowers while flying 60–90 cm above the
forest floor. When an individual bee has noticed a particular patch of flowers its flight
changes from meandering to direct. The bee approaches to within ca. 20 cm of the flowers
and weaves back and forth in flight (figure 2). This hovering stance is maintained for a few
seconds. The bee makes several closer approaches and retreats while weaving from side to
side in the air. The bee then flies directly towards a particular flower.
The bee flies towards the flower perpendicular to the flower’s ‘face’. The bee lands on
the flower by seizing it with its legs and grappling with the petals and fused anther structure
(figure 2). During this contact with the flower the bee holds part of the flower in its
mandibles and vibrates its wing muscles. This transfers the high-frequency vibrations to the
flower and pollen is released from the fused anthers. This process takes place very rapidly
and lasts 1–3 seconds. During this time, as the bee holds on to the flower, short pulses
of a buzzing sound can be heard. This is the result of the vibrating flight muscles that cause the
Pollination of Saintpaulia teitensis 37
Figure 2. Behaviour of Amegilla and pollination of Saintpaulia teitensis flowers. Top: bee
approaches flower directly from a distance. Middle: bee weaves in front of flower for 2-5
seconds often switching position. Bottom left: bee ‘buzz’ pollinating flower. Bottom right: detail of
anthers shaking and releasing pollen grains.
38 D.J. Martins
pollen to be released. This is indicative of buzz pollination (Proctor et al., 1996). During its
time on the flower the bee makes circular movements on the flower, which helps more pollen
adhere to its body hairs.
The bee then lifts itself into the air and hovers again briefly while combing pollen into its
pollen baskets. This motion is very rapid and is followed by a return to weaving flight in
front of the flowers. The bee then either drops back onto another flower or flies away. The
numbers of flowers visited during a particular visit are variable, but the durations of the
visits are always under 1 minute (N=20 timed visits observed, mean=37.25 seconds,
st. dev.=13.714 seconds). Visitation rates are variable, bi-modal peaks around mid-morning
and early to mid-afternoon were observed in 2003 (figure 3).
Figure 3. Amegilla visitation rates to Saintpaulia teitensis.
Pollination of Saintpaulia teitensis 39
Four different species of Amegilla were recorded on S. teitensis: Amegilla calens
Lepeletier, A. acraensis Fabricius, A. caerulea Friese and A. sp. Of these four, A. calens
and A. caerulea were the most frequent visitors. Initially, only the duration and number of
visits were recorded. As it became apparent there was more than one species of bee
involved, all from the same genus, more detailed information on visitation was recorded. It
was challenging at first noting the species of bee involved due to the speed and short duration
of the visits. Observations made later in the study in 2003 and 2004, noted the identity of the
bee during recording of visitation. All four species of Amegilla were often observed on the
same day. More work on the visitation patterns and behaviour of the 4 different Amegilla
spp. remains to be done in order to determine whether all are equally effective pollinators or
engaging in resource-partitioning on S. teitensis.
The fuschin gel slides showed pollen grains from S. teitensis present on all the flower-
visiting Amegilla bees’ bodies and in their pollen baskets. Amegilla spp. were common
visitors to other forest floor flowers primarily Lamiaceae and were seen visiting
Streptocarpus spp., the genus within which Saintpaulia is embedded (Möller & Cronk,
1997b), in the Taita Hills forest, Mount Kasigau and in the Aberdares (pers. obs.). In the
Taita Hills the same four species of Amegilla bees were observed visiting flowers along the
forest edge adjacent to cultivated areas (bees were netted and released). They visited the
flowers of the following crops being cultivated in small-scale farms bordering the forest:
cowpea (Vigna unguiculata L.Walp.), eggplant (Solanum melongena L.), pigeon pea
(Cajanus cajan L.Millsp.) and tomato (Solanum lycopersicum L.).
DISCUSSION
The Taita African Violet appears to be pollinated in its natural habitat by a limited number of
bee species from a single genus. Pollination is required for fruit set, even if it is self-pollen
landing on the stigma of the same flower, it still needs to be mechanically displaced from the
anthers (Kolehmainen & Mutikainen, 2006). Amegilla bees are also visiting other Saintpaulia
spp. in Tanzania (J. Kolehmainen, pers comm.). The limited number of bee species
involved, and the manipulation of the flowers suggests a more specialised pollination system
(Roubik, 1989). The Amegilla bees, if confirmed as the sole pollinators of all other
Saintpaulia spp., suggests a pollination guild. The Taita African Violet can only be
adequately conserved if both its pollinators and habitat are protected. The pollinators
themselves, such as the Amegilla bees in the forest fragments and their edges, require a wide
range of flowering plants so as to access enough nectar and pollen resources throughout the
year and therefore sufficiently provision their nests and larvae (Roubik, 1989). The limited
numbers of bee species available to pollinate this Eastern Arc endemic indicates that the
conservation of specialised interactions is just as crucial as that of protecting individual
species and habitats.
The pollination mechanism, buzz-pollination, is in itself interesting and worth further
investigation to determine if this is a unique feature of the genus Saintpaulia within the Afro-
tropical Gesneriaceae, or if it occurs in other species of Gesneriaceae as well. Preliminary
observations of other plants in cultivation indicate that both heteromorphic enantiostyly and
buzz-pollination are common features of Saintpaulia spp. Enantiostyly has evolved in at least
ten different angiosperm families (Jesson & Barret, 2002). More detailed observations of the
behaviour of the floral visitors will indicate the role of enantionstyly in the pollination
ecology of S. teitensis and other Saintpaulia spp.
40 D.J. Martins
Dispersal of pollen between sub-populations of the plant and movement by bees across
forest fragments and adjacent cultivation is key to both survival of the plants and their
pollinators (Kolehmainen & Mutikainen, 2006). This study suggests that even small highly
fragmented and impacted forests can support pollination services for endangered plants as has
been found in some orchids (Murren, 2002; Martins & Johnson, 2007). However,
fragmentation can also lead to a potential collapse of pollination services even within
protected areas (Pauw, 2007).
The observation of Amegilla bees on crops and forest-edge/agricultural matrix areas need
to be investigated further. This feature represents an opportunity to link the pollination
ecology and conservation of a flagship endemic species with the sustainable farming practices
and rural livelihoods of small-scale farmers living adjacent to forest fragments. Given the
current focus on the conservation of the Eastern Arc forests and the wider issue of
sustainable development in the region, the specialised interactions between Amegilla bees and
the Taita African Violet could serve as an example of the necessity of conserving forest
fragments for this flagship endangered species.
ACKNOWLEDGMENTS
This study was conducted as a parallel project to an analysis of bee diversity and interactions
in the Tsavo ecosystem while based at the Taita Discovery Centre. Thanks are due to the
staff and management of Origins Safaris and Taita and Rukinga Ranches for logistical
support. Dr. Connal Eardley of ARC-PPRI, South Africa and the late Roy Snelling of the
Los Angeles County Natural History Museum helped provide the bee identifications.
Assistance, useful comments and various insights were provided by Edwin Selempo,
Dr. Paula Kahumbu, James Mwang’ombe, Peter Greste, Dr. Gerard Hertel, Dr. Henk
Beentje, Dr. Stella Simiyu, Anne Powys, Job Ballard, Dr. Ian Gordon, Dr. Barbara
Gemmill, Anne Robertson, Dr. Benny Bytebier, Gordon Boy, Dr. P. Siro Masinde and the
scientists and staff of the East African Herbarium, the National Museums of Kenya, and the
Taita Hills project team of the East African Wildlife Society. Useful comments on this
manuscript were provided by Dr. Benny Bytebier and Dr. Timo van der Niet and an
anonymous reviewer, I thank them for their time and efforts.
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