Pollination Biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in southern Africa; floral divergence and adaptation for long-tongued fly-pollination
Abstract | Materials and Methods | Results | Discussion | Literature
Most species of subgenus Lapeirousia
have a simple or branched flowering stem, and each axis terminates
in a spike of several to many flowers. In L. oreogena,
L. montana, L. plicata, and L. odoratissima
the inflorescence is a congested tuft of flowers borne at ground
level. The number of flowers per plant varies considerably from
year to year. Vigorous plants have as many as five spikes each
and up to 20 flowers per tuft or spike.
Floral Phenology and Life Span
Flowering in southern African species of subgenus Lapeirousia in the study area ranges from late May until early November Figure 1. Populations of each species
bloom for two to four weeks. Exact timing of flowering within
a species varies seasonally, and to some extent locally, depending
on elevation and aspect. The higher the elevation the later a
population comes into bloom. Despite considerable overlap in flowering times Figure 1, species may be characterized generally as early (June to mid August), mid (late August and September), or late season (October and November) bloomers.
The pattern of flower buds opening on an inflorescence is acropetal. In all species the perianth of a mature bud expands in the early to midmorning. The rate at which buds open and the longevity of the expanded perianth are dependent on ambient temperatures. The perianth of an open flower lives a maximum of five days if daily temperatures remain below 20°C and soils remain wet. At sunset the tepals of most species contract, partly or sometimes completely enclosing the exserted anthers and stigmas. In L. exilis, tropical African L. odoratissima, and L. pyramidalis (both subspecies) the tepals remain open all night.
The anthers of all species dehisce longitudinally
within two to four hours after the tepals unfold. Pollen remains
in the open thecae until contacted by insects or washed out by
rain. The three stylar lobes do not normally expand to expose
the receptive stigmas until the day after the anthers have dehisced.
This suggests that all the species studied are weakly protandrous.
Floral Morphology Figure 2
In most species of subgenus Lapeirousia
the perianth tube is cylindric. In L. divaricata and L.
spinosa, however, the tube is funnel-shaped Figure 2H. In
sixteen species the perianth tube always exceeds 17 mm in length,
with a maximum of 76 mm in L. anceps (Table 5). In L.
divaricata, L. spinosa and L. tenuis the tube
is less than 16 mm long. In L. exilis, L. montana,
and L. plicata, however, the external length of the tube
is misleading: the lower half of the tube is occluded by the style
and intrusive ridges, decurrent on the filaments Figure 2K,
so that the nectar is forced into the upper part of the tube.
Functional tube length, in terms of accessibility of nectar to
insects, is less than half what it appears to be (Table 5). Tube
length is unusually variable in L. anceps, and may be as
little as 20-30 mm in populations in the south of its range, and
45-76 mm in the west and north.
Seventeen species have a zygomorphic flower and unilateral, arcuate stamens and style (Table 5, Figure 2A, E, H). In contrast L. oreogena, L. montana, L. plicata, and L. odoratissima have actinomorphic flowers Figure 2J, K in which the stamens and style are symmetricallybdisposed.
Tepals of the fully open flower either
spread horizontally and are thus patent, or the dorsal (adaxial)
tepal is erect (Lapeirousia silenoides, L. pyramidalis,
L. verecunda), or inclined over the stamens (L. divaricata,
L. spinosa). In species with zygomorphic flowers the dorsal
tepal is broader and sometimes longer than the five other tepals.
Lapeirousia fabricii and L. barklyi are the only
species in which the tepals are broadly cupped below and patent
above, and thus include the filaments. In several species with
zygomorphic flowers (e.g., L. divaricata, L. fabricii
- Figure 2H), each of the three lower tepals bears a raised ridge
or narrow tooth. These appendages are absent in species with actinomorphic
In all species the stamens are equal
in size and the filaments are erect, or sometimes slightly inclined.
In zygomorphicflowered species the anthers are parallel
and face the center of the flower and the lower tepals and nectar
guides, but in species with actinomorphic flowers the anthers
are symmetrically disposed and face outward Figure 2J, K. The
style branches of all species of subgenus Lapeirousia included
in the study are divided for half their length. Although this
is a generic characteristic, the style branches may be undivided
in some species or populations of the genus (Goldblatt, 1972,
1990). The resulting six stylar arms, which spread outward and
recurve, bear receptive stigmatic hairs that appear to be dry
when observed under a 10x hand lens. The style arms are normally
held between 1 and 3 mm above the anther apices, but in L.
arenicola, L. jacquinii, L. simulans, and L.
violacea the style arms become tangled in the anthers as the
style lobes expand.
Compatibility and Fruit Set
We were unable to make a thorough study
of compatibility in subgenus Lapeirousia, but present the
following observations. In L. arenicola, L. jacquinii,
L. simulans, and L. violacea, stems cut at bud stage,
maintained in water, and excluded from insects for two weeks
routinely set full capsules containing the normal number of seeds
for that species. Furthermore, L. jacquinii and L. oreogena
have been noted to set seed in greenhouses where insect activity
Lapeirousia barklyi, L. dolomitica
subsp. dolomitica, L. pyramidalis, L. silenoides,
and L. spinosa, did not set fruit when inflorescences were
maintained in water as in the species above. In these taxa dehisced
anthers and stigmatic surfaces are in contact in both field populations
and laboratory specimens. Lapeirousia silenoides and L.
pyramidalis subsp. regalis, in which the anthers and
stigmas are not in contact, do not set fruit even when self-pollinated
by hand either maintained in water or grown in pots. In field
populations of L. dolomitica, L. pyramidalis, and
L. silenoides individual plants were often observed to
produce none, or only one or two mature capsules per spike after
Floral Presentation, Attractants and Rewards
Field observations of species of subgenus
Lapeirousia indicate that they can be divided into three
morphological types based on floral chracteristics (Tables 3,
4, 5), and that each of the floral types is associated with a
different suite of pollinators. The three flower types are defined
primarily by floral pigmentation and patterning in combination
with perianth tube length. However, regardless of flower type,
in zygomorphic flowers visible nectar guides are always confined
to the three lower tepals Figure 2. In all species nectar is
secreted at the base of the floral tube in volumes ranging from
20 to 76 ml (only 10-12 ml in L. divaricata and L. spinosa)
(Table 4). In L. exilis, L. montana and L. plicata
occlusion of the basal part of the tube results in the nectar
being forced into the upper half.
1. The L. silenoides-type Figure
2A: tepal pigmentation dark blue to purple or dark red, darker
than the nectar guides; visible nectar guides yellow to white
streaks or blotches near the tepal bases and sometimes a zone
of intense pigmentation in the center of each lower tepal; callus
ridges absent; no scent discernable to the human nose except in
L. dolomitica subsp. dolomitica, which has a faint
sweet odor; floral tubes 33-70 mm long; flowers actinomorphic
or zygomorphic; nectar sucrose rich to sucrose dominant.
2. The L. fabricii-type Figure
2E: tepal pigmentation white to cream or pale pink (but usually
pink to red on the reverse), lighter than the nectar guides; visible
nectar guides dark red to maroon oblong to acute patterns at the
tepal bases; callus ridges usually present; no scent discernable
to the human nose; floral tubes normally 30-76 mm long; flowers
zygomorphic; nectar sucrose dominant or, in L. macrospatha,
3. The L. divaricata-type Figure
2H: tepal pigmentation white to cream or pale blue, lilac, or
pink; visible nectar guides usually narrow to streaky, light purple
sometimes grading to a yellow to cream-colored ridge at the base
of the tepals or merely a white zone in the center of the flower
(L. montana); scents present and variable, ranging from
a cloyingly sweet heavy fragrance (L. exilis, L. pyramidalis
subsp. pyramidalis) to a lightly sweet to mildly spicy
scent reminiscent of Dianthus or Narcissus; callus
ridges well-developed in L. divaricata, L. spinosa,
rare and inconspicuous in L. pyramidalis subsp. pyramidalis;
floral tubes never exceeding 55 mm, in 3 of the 5 species tubes
less than 30 mm (functional tube length always less than 35 mm);
flowers actinomorphic or zygomorphic; nectar usually sucrose dominant,
or sucrose rich (L. montana), or hexose rich (L. barklyi).
The three modes of floral presentation
are accompanied by three different pollinator guilds. However,
all floral foragers collected on Lapeirousia species had
two foraging characters in common. First, pollen load analysis
(Table 2) and observations of flight patterns indicate that all
insects observed on Lapeirousia Figure 2, 3 forage actively
on the flowers of some other co-blooming plants (Table 2). Second,
no matter how elongated the mouth parts of the pollinator are,
they are always somewhat shorter than the perianth tube (Table
5). In addition, an insect was rarely observed to probe anthers
with its proboscis or actively collect pollen on any Lapeirousia
1. The Lapeirousia silenoides
group. Nectar foraging in this flower type was dominated by long-tongued
flies of the genus Prosoeca (Nemestrinidae) Figures 3A-B,
4A. Prosoeca peringueyi was observed foraging on the flowers
of all species in this group (Tables 2, 5) excluding L. oreogena.
Lapeirousia oreogena was visited by Prosoeca sp.
nov. Figure 3B, and this fly species also visited L. jacquinii
at two sites on the Nieuwoudtville Plateau (where P. peringueyi
evidently does not occur). In both species of flies the insects
hover while orienting and inserting their proboscis into the tube.
When the proboscis has been fully inserted into a tube that is
long enough to permit this, the insect grasps the tepals with
its legs during the actual feeding process, but the wings remain
in motion. By flexing the tibiae of the hind legs forward the
fly can use all three pairs of legs for grasping, and this is
done in plants with both vertical and horizontal flower presentation.
In flowers with short tubes that are visited for nectar, the body
does not contact the stamens or stigmas so that pollination is
not effected, and the fly hovers without grasping the tepals.
Prosoeca species are active on
mild to warm days from midmorning to early afternoon, and
again in the late afternoon. These flies remain at each Lapeirousia
flower for 3-5 seconds, and pollen adheres to the frons and thorax
in L. oreogena and on the dorsum and upper frons in other
species. Often pollen depositions are so heavy they are visible
to the naked eye. In species with zygomorphic flowers, the fly
always orients itself in the same way, approaching the flower
from the front, thus facing the anthers as it forages. Density
of visitors varies considerably, ranging from four to five flies
present locally at the same time, or as few as one or two flies at sites over periods as long as an hour. At one site,
the top of Botterkloof Pass, where L. jacquinii and L.
violacea co-occur, individuals of P. peringueyi were
observed to visit both species indiscriminately. Prosoeca
species typically interrupted foraging on Lapeirousia species
to collect nectar on other species growing nearby, including Pelargonium
species (Geraniaceae), and taxa of Iridaceae including Babiana
species, Sparaxis variegata subsp. metelerkampiae
(L. Bolus) Goldblatt, Xenoscapa uliginosa Goldblatt &
Manning, Hesperantha latifolia (Klatt) de Vos, and Geissorhiza
kamiesmontana Goldblatt. Interestingly, the flowers of Pelargonium
sericifolium van der Walt do not secrete nectar although they
have long floral tubes and may mimic flowers of species that do
produce nectar Figure 2, suggesting pollination by deceit, a
phenomenon best known in Orchidaceae.
Pollen deposition tends to be on the
head and back part of the thorax (nototribic) in Lapeirousia
except L. oreogena, but on the underside (sternotribic)
in Pelargonium, a factor that reduces contamination of
pollen loads and competition for vector sites on the insects'
2. The L. fabricii group. Nectar
foraging in this group was limited to one species of fly in the
Nemestrinidae (Moegistorhynchus longirostris - Figure 4B
and one species of fly of the family Tabanidae (Philoliche
gulosa - Figure 4C). Both fly taxa are long-tongued and have
mouth parts as long as or longer than the Prosoeca species
discussed above. Moegistorhynchus longirostris was observed
actively foraging on L. fabricii only in the late afternoon,
4:006:00 PM, at one study site in northern Namaqualand.
The same fly species was recorded visiting L. anceps at
the study site near Ysterfontein during the late morning on a
cool and cloudy day.
Philoliche gulosa visited Lapeirousia
fabricii at three sites between 11 AM and 3 PM.
The foraging behavior of Moegistorhynchus
longirostris and P. gulosa on Lapeirousia species
was similar to the foraging behavior of Prosoeca species.
Nemestrinid species fly with their mouth parts hanging downward,
and forage for nectar by extending the fairly flexible proboscis
either forward or downward depending on the characteristics of
a particular flower. Philoliche gulosa flies with its proboscis
extended forward, and its proboscis appears to be less flexible
(S. Johnson, pers. comm.). Moegistorhynchus longirostris
interrupted its foraging on Lapeirousia species to forage
on the flowers of Pelargonium species, and species of two
other Iridaceae, Geissorhiza exscapa (Thunb.) Goldblatt
and Babiana tubulosa (Burm. f.) Ker-Gawl. We assume that
B. brachystachys (Bak.) G. Lewis, Ixia paniculata
Delaroche, Tritonia crispa (L. f.) Ker-Gawl., Geissorhiza
confusa Goldblatt, and Gladiolus angustus L. (all Iridaceae)
also belong to this guild, because their flowers are similarly
constructed and colored. Moegistorhynchus was also observed
attempting to forage on the spurred but nectarless terrestrial
orchid, Disa draconis (L. f.) Sw. The foraging of the fly
on the orchid suggests another example of pollination by deceit,
as the orchid produces creamy white flowers with narrow purple
nectar guides, similar to floral presentation in L. anceps.
3. The L. divaricata group.
Species in this group were visited by various combinations of
Lepidoptera, bees, and bombyliid flies (Table 2). Lapeirousia
exilis and L. plicata appear to be pollinated by a
combination of bombyliid flies and Hymenoptera, including the
native Apis mellifera Apidae: Figure 3C and Tetraloniella
karooensis (Anthophoridae). These insects were observed to
contact anthers and stigmas while foraging, and pollen was brushed
onto their bodies passively. All of the insects collected on flowers
in this group have mouth parts shorter than Philoliche gulosa
and the three taxa of nemestrinid flies (Table 5). Bees were active
throughout most of the day, but were observed most frequently
during the cooler periods before 11 AM or after 4 PM. The noctuid
moth, Heliothis armigera Figure 3D, was observed in large
numbers foraging on L. divaricata at two sites between
3.30 and 6 PM. Bombyliid flies, bees, H. armigera, and
the butterfly, Cynthia cardui (Nymphalidae), did not usually
forage by hovering. In zygomorphic flowers these insects always
perched on the lower tepals before foraging for nectar.
The only insect observed to feed while
hovering was the sphinx moth, Hippotion celerio (L.), which
was seen, but not captured in a population of Lapeirousia pyramidalis
subsp. pyramidalis near de Wet (Worcester District). Pollen
load analyses (Table 2) indicate that H. armigera and Cynthia
cardui may be poor vectors of pollen compared to bees.
All bees collected on the Lapeirousia
divaricata group belonged to long-tongued families. With the
exception of two specimens of Hoplitis similis (Megachilidae)
and one specimen of Parafidelia (Fideliidae), bees collected
on the L. divaricata group belong in the families Anthophoridae
and Apidae. Two anthophorid bee individuals collected (Anthophora
diversipes and Amegilla grisella) were males, and the
remainder, female. Analyses of pollen washes of the hairs on the
hind legs and ventral abdominal region show two characteristics.
First, all female bees collected on the L. divaricata
group are polylectic and polytrophic. Field observations as well
as pollen-load analyses showed that these bees collected pollen
actively on nectarless flowers including Cyanella alba
L.f. (Tecophilaeaceae) and Hermannia sp. (Sterculiaceae).
Hoplitis similis, collected on L. spinosa, interrupted
its visits to this species to forage on similarly pigmented Moraea
tortilis Goldblatt, the flower of which is also a meranthium
of the gullet type "blossoms" (see discussion), similar to that of
Iris. The flowers of M. tortilis produce small quantities
of nectar. Pollen-load analyses showed that all bees foraged on
a much broader selection of taxa than were recorded for fly or
moth specimens. Although female bees do not collect pollen actively
on Lapeirousia flowers, the pollen deposited passively
on the bee's head and thorax is combed off by the bee and deposited
in the scopae. Bee activity in species of the L. divaricata
group differed during the season. Apis mellifera was collected
most frequently in July and early August while the first anthophorids
were not observed and netted until mid August.
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