Bee-pollination inHibbertia fasciculata (Dilleniaceae)

P1. Syst. Evol. 152, 231-241 (1986) Plunt |V.stemutics nnd Eunlutinn © by Springer-Verlag 1986

Bee-Pol l inat ion in

H i b b e r t i a f a sc i cu la ta (Di l l en iaceae )

By

Peter Bernhardt

(Received September 4, 1985)

Key Words: Angiosperms, Dilleniaceae, Hibbertia fasciculata, Lasioglossum ( Halictidae ) , Leioproctus ( Colletidae ) , Myrtaceae. - Bees, beetles, floral symmetry, stamens, stigmas.

Abstraet: In direct contrast to most Hibbertia spp., the flowers of H. fasciculata R. Be. ex D. C. bear only a single whorl of stamens and these stamens are arranged separately (not in typical "bundles"). The short filaments are appressed to the three carpels so that the inflated, porose and introrsive anthers form a centralized cluster obscuring the three ovaries. The three slender styles emerge at right angles from between the filaments. These styles curve upward and the stigmas form the three points of a triangle; each stigma is approximately one millimeter outside the centralized cluster of anthers. The flowers are nectarless and bear a bright yellow corolla. A pungent and unpleasant fragrance appears to be concentrated within the pollenkitt. When native bees attempt to forage for the pollen, within the cluster of anthers, the ventrally deposited loads of pollen, on the bees' abdomens, contact the outer triangle of stigmas. The major pollinators of H. fasciculata are female bees in the polylectic genera, Lasioglossum (subgenus Chilalictus, Halictidae) and Leioproctus (Colletidae). These bees carry an average of more than two pollen taxa when they are caught foraging on H. fasciculata. 78 % of the 47 bees, captured on H.fasciculata carried the pollen from at least one sympatric taxon bearing nectariferous flowers (e.g., genera in the Myrtaceae, Compositae, and Epacridaceae). The pollination biology of 11. fasciculata is assessed in relation to the known radiation of bee-pollinated flowers in the genus Hibbertia, and within the Dilleniaceae s. 1.

An ongoing study of the role of insects as pollinators of Hibbertia spp. should remain an important topic for both floral ecologists and evolutionary botanists. Hibbertia spp. reach their greatest degree of diversity around the periphery of the Australian continent and they are often dominant components of sclerophyll heaths and woodlands (STE~BINS & HOOGLAND 1975). These vernal-flowering shrubs and small trees may form part of a dominant "yellow-flower guild" in asspeciation with coblooming plants such as Acacia spp., herbaceous Compositae, papilionoid legumes

16"

232 PETER BERNHARDT:

and some of the terrestrial Orchidaceae (ARMSTRONG 1979, BERNHARDT 1982, 1984 and A. DAFNI, personal communication). Hibbertia pollen appears to be a common food source for the larvae of some Australian bees and some beetles in the families Scarabaeidae, ChrysomeIidae, and Curculionoidae (KEIGHERY 1975, ARMSTRONa 1979). Hibbertia flowers appear to be nectarless (KEIGHERY 1975, STEBmNS & HOOCLAND 1975) SO the insects that pollinate Hibbertia must seek chemical energy (diluted sugars) from the wide range of sympatric angiosperms (BERNHARDT 1982, 1984).

Within the current framework of evolutionary theory, the family DilIeniaceae is considered relatively rich in ancestral characteristics (CRoNQUIST 1981, DICKISON 1969). STEBBINS (1974) considered Hibbertia equal in primitiveness to the woody Magnoliales and interpreted the floral and vegetative morphology of Hibbertia as the least specialized within the DilIeniaceae. However, adaptive radiation within Hibbertia seems to have favored extraordinary variation in floral symmetry. Although the pentamerous calyx and corolla remain salver-funnelform, in most Hibber- tia spp., the number and arrangement of stamens and carpels profoundly effects floral presentation. Unlike all other putatively "primitive genera" of dicots both actinomorphic and zygomorphic flowers are found in Hibbertia (see illustrations in STERBINS & HOOaLAND 1975). The transition between radial and bilateral symmetry appears both gradual and pro- gressive in the flowers of Hibbertia. The number of carpels, within a flower, tends to correlate positively with the number of staminal whorls and staminal bundles.In some species, bundles of staminodes testify to the derivation of zygomorphic flowers from actinomorphic ancestors with multi-whorled, multi-staminate androecia (KEIGHERY 1975, STEBBINS HOOGLAND 1975).

Therefore, the analysis of the pollination biology on an Hibbertia sp. should offer two benefits. First, it contributes to our knowledge of reproductive systems in the temperate-mediterranean flora of Australia and the exploitation of Australian insects as pollen vectors. Secondly, and expanding view of floral mechanisms, with the the genus Hibbertia, may make it possible to interpret the role of natural selection on extant flowers with ancestral characteristics.

Study Site

Approximately 50 plants of H. fasciculata were located at Frankston Victoria, on the Mornington Penninsula, about 35kin southwest of Melbourne. The population was distributed through the Langwarren Reserve and on the directly adjacent property of Mr. Peter Chance. The vegetation of the Reserve and the unfarmed property of Mr. Chance consisted of disturbed tall shrubland and remants of epacrid heath

Bee-Pollination in Hibbertia 233

(SPECWr & al. 1974). Hibbertiafasciculata grew in the heath remnants or in the meadows of naturalized European grasses that colonized the areas where the native vegetation had been cleared.

Materials and Methods

Living material was collected from the study site for dissection and selective staining. To determine the presence of osmophores floral parts and whole flowers were submerged in Neutral Red for intervals of five minutes, one hour and two hours.

To understand the role of floral display a weekly count was taken of open flowers per branch during the first three weeks of October 1984. Flowers were counted as open when the corolla had expanded exposing the androecium and gynoecium. Flowering branches were counted at random from a total of 12 individual shrubs.

Insects were collected weekly from September 24, 1984 to October 26, 1984. Insects were removed from flowers of H.fasciculata only when they were observed manipulating the floral organs or probing floral structures with their proboces. The insects were killed in jars containing fumes of ethyl acetate. To determine the contents of pollen loads present on the insects pollen was removed and stained with Calberla's fluid (OaDEY & al. 1974) according to pollen washing techniques as described by BERNHARDT (1984). AS insects were killed in the same jar con- tamination of different pollen species was possible as bodies touched. Therefore, a pollen species was not counted as present in an individual pollen load unless 25 individual grains could be counted (for plants with monad pollen). Twenty five individual polyads had to be counted for taxa with compound pollen (e.g., Acacia and Epacridaceae) before the plant taxon could be recorded as present on a particular insect. Insect washed of pollen were allowed to air dry then they were labeled, placed in individual glassine bags and identified.

Results

Flowering Period and Floral Presentation. Individual shrubs are found with open flowers from the last week in August until the first two weeks in November. The flowering peak occurs in October. The sessile, axillary flowers are held in suberect-erect, or infrequently horizontal, positions on the prostrate-ascending stems of each shrub. The flower buds on each stem open acropetally. An average of > 2 open flowers per branch may be seen in October ( n = 3 9 ; Mean=2 .69 ; Standard Deviat ion= 1.9; Range = 1 - 9 open flowers per branch).

The five petalled corolla (Fig. 1) is bright yellow while the anthers often have a darker "mustard" tone. A pungent floral fragrance is obvious as soon as the petals expand. The fragrance is a musty-fetid "stink" like a combination of commercial honey and fresh cow dung. This is reminiscent of the floral fragrance of Chrysanthemum leeucanthemum but the fecal element was much more pronounced in H. fasciculata. The results of the Neutral Red Test are identical for each staining interval. The only areas that stain with soaking are the pollenkitt, anther slits and the stigmas.


A S'[

Y

2

3 Figs. 1 - 3. H i b b e r t i a f a s c i c u l a t a ; - Fig. 1. Flower, × 6; - Fig. 2. Androecium and gynoecium; x 12.5; - Fig. 3. Stamen; × 25. A anther, AC anther cluster, F

filaments, O ovaries, P petals, S sepals, ST stigmas, SY styles

Anflroecium. The androecium consists of 11 - 12 stamens grouped in a single whorl around the gynoecium (Figs. 1 and 2). Each staminal filament is approximately as long as its anther (Figs. 2 and 3). Each anther is inflated, and papery. Dehiscence occurs just prior to the expansion of the corolla and the anthers are introsed (Fig. 2). Although each anther has two unfused longitudinal slits they are technically poricidal (sensu BUCHMANN 1983) as each slit expands most widely towards the anther tip (Fig. 3). Pollen falls out of these enlarged openings when shaken or prodded with a dissecting needle.

Gynoeeium. Each flower bears three carpels and each carpel is flanked by two or more staminal filaments. A slender style surmounts the ovary at a right angle so the styles always emerge from b e t w e e n the staminal filaments. The stiff style gradually recurves back towards the androecium until the stigma is approximately one millimeter from the tip of the nearest


a n t h e r (Fig. 2). There fore , the s t igmas fo rm the three po in t s o f a n equ i l a te ra l t r i ang le ou t s ide the c luster o f an the r s (Fig. 1).

Po l l ina t ion . O n w a r m , s u n n y , c loudless m o r n i n g s insect ac t iv i ty m a y bee seen o n f lowers o f H . fa sc i cu la ta f rom 9 a .m. to 1 p .m. N a t i v e bees are the m o s t c o m m o n f lora l foragers a l t h o u g h one fly in the fami ly Heleomyzidae, Tapeigaster sp., was col lected o n O c t o b e r 8, 1984. The fly

Table 1. Gross pollen loads of insects captured on Hibbertiafasciculata

Insect Taxon Carried pollen of H. fasciculata + H. fascieulata pollen of other

only species

Carried no pollen

Diptera Tapeigaster sp.

Hymenoptera Apis mellifera Lasioglossum ( A ustrevylaeus ) Lasioglossum ( Chilalictus) Leioproctus ( Leioproctus )

- 1 -

- - 1 - -

4 27 1 1 1 2 -

Table 2. Analysis of those pollen loads containing the pollen grains of H. fasciculata plus the pollen of other species. + = Extra-floral nectar present; + + -- floral nectar present; - = floral nectar absent. Ac = Acacia longifolia and/or A. melanoxylon (16 grain polyad; Leguminoseaes. 1.); Co = mixed genera of Compositae, Ei = Epacris impressa (Epacridaceae); H f = Hibbertia fasciculata (Dilleniaceae); Le = Leucopogon spp. (Epacridaceae); LM = Unidentified lilioid Monocot; MY --- Melaleuca squarrosa and/or Leptospermum obovatum (Myrtaceae); PA = Unidentified papilionoid legume (Leguminosae sensu lato);

Rp = Ricinocarpos pinifolius (Euphorbiaceae); U D = Unidentified Dicot

Insect Taxon

Plant Taxon

Ac + Co ++ Ei ++ Hf - Le ++ LM MY + + P A ++ R P - UD

Diptera Tapeigaster sp. 1 - - 1 . . . . . .

Hymenoptera Apis mellifera 1 1 - 1 - 1 1 - - - Lasioglossum (Austrewleus) - - - 1 - - 1 - - - Lasioglossum (Chilalictus) 8 6 2 27 3 2 14 - 7 1 Leioproctus (Leioproctus) 2 2 - 12 1 4 8 1 1 1

Totals 12 9 2 42 4 7 24 1 8 2


I!

o4 Fig. 4. Branched scopal hair of female Lasioglossum (Chilalictus) showing mixed pollen load. x 140. A polyads of Acacia spp., C monads of Compositae, H monads

of Hibbertia fasciculata

did carry the pollen of H. fasciculata (Tables 1 and 2) but appeared to be probing the surface of anthers for loose, "spilled" grains and not actively removing pollen from the poricidal anthers. The fly's body did not contact the stigmas.

Only female bees were collected on the flowers of H. fasciculata. The most commonly collected bee taxa were Lasioglossum (subgenus Chilalic~ tus; Halictidae) spp. and Leioproctus (subgenus Leioproctus; Colletidae) spp. The large-bodied, but fast-flying Lasioglossum (subgenus Austrevyleus) sp. was observed much more often than it could be captured. All of these bees deposit the pollen they collect on the scopal hairs of the hindlegs (Fig. 4) and the ventral hairs at the base of the abdomen (BERNHARDT 1984, BERNHARDT & al. 1984). Forty seven, out of 48 bees captured on H. fasciculata carried pollen of H.fasciculata (Table 1). These bees smell like the flowers of H.fasciculata even though they may be kept in a jar with ethyl acetate fumes for 2 - 3 hours.

A bee lands directly on the cluster of anthers and attempts to remove pollen by a combination of thoracic vibration and scraping the poricidal openings with her forelegs. The bee's abdomen usually hangs over the anther cluster and is parallel to the stigmas. As the bee grasps and vibrates the anther cluster its abdomen swings back and forth. The loads of pollen, deposited ventrally at the base of the bee's abdomen, are rubbed into the receptive stigmatic cup while the bee swings.


The bees that pollinate H.fasciculata are polylectic foragers. The vast majority of bees collected carried the pollen of at least one other coblooming taxon (Table 1 and Fig. 4) and 78% of the bees collected carried the pollen of one, or more, plants bearing nectariferous flowers (Table 2). Lasioglossum and Leioproctus spp. have been recorded foraging on the extra-floral nectaries of some Acacia spp. (BERNHARDT & WALKER 1984) SO that the glands on the phyllodes of A. longifolia and A. melanoxylon may also act as nectar (Table 2).

One Leioproctus sp. carried the pollen of six taxa in her scopae; H. fasciculata, Acacia sp., Compositae, Epacris impressa and Ricinocarpos pinifolius. Most bees carry an average of less than half the number of pollen taxa when they forage on H. fasciculata (n = 48; Mean = 2.63; Standard Deviation = 1.3; Range = 0 - 6 pollen taxa on a bee).

Discussion

The Adaptive Significance of the Stigma/Anther Alignments. In H. fasciculata, the stigmas and anthers have literally traded places. Three stigmas are positioned outside the radius of the rotate androecium to form a triangle. The adaptive significance of this realignment is comparable to systems described in flowers that bear only a solitary pistil but present a zygomorphic androecium and/or perianth. This condition is extremely common in the buzz-pollinated flowers of the genera Cassia, Cyanella, Pedicularis, and Solanum (see review by BUCHMANN 1983 and discussion by BERNr~ARDT 1984). As the bee vibrates the clustered, porose anthers the stigma contacts an isolated region of the bee's body that retains pollen but is spatially isolated from the clustered anthers. In H. fasciculata the position of the stigma exploits the region of the bee's body where pollen deposition is heaviest.

Unlike the eusocial Apidae the majority of solitary bees lack a true corbiculae. Some bees, like Lasioglossum and Leioproctus spp. tem- porarily store pollen on ventral hairs on the abdomen (see micrograph in BERNHARDT 1984). This pollen may be packed down on the hairs but it has not been cemented with saliva and nectar as in the eusocial bees (M~crtENER 1974). The coherent quality of Hibbertia pollen appears to be due to the natural deposition of pollenkitt (BERNHARDT 1984).

Introsed anthers are usually interpreted as a mechanism for encourag- ing self-pollination by mechanical autogamy (ORNDUFF 1969). In H. fasciculata they may prevent mechanical autogamy as the dehiscent side of the anther is opposite the triangle of stigmas. The adaptive alignment of anthers and stigmas is probably characteristic of other Hibbertia spp. with small flowers and rotate androecia (BEe, NIqARDT, personal observation). Nectarless lilioid monocots in Australia like Calectesia, and some genera


within the Iridiaceae s. s. may also bear a similar floral presentation with their deeply divided, tripartite stigmas (BERNHARDT, personal observation).

Bee-Pollination in H. fasciculata vs. H. stricta. An uncomfortable question must be asked in light of the results presented in this study. If the actinomorphic flowers of H. fasciculata and the zygomorphic flowers of H. stricta are both pollinated by female Lasioglossum spp. (BERNHARDT 1984) what is the selective advantage of two radically different modes of floral presentation? In fact, what is the neodarwinian explanation for adaptive radiation of floral symmetry within the genus Hibbertia?

Interspecific isolation is not a sufficient explanation. It is true that the two stigmas in a flower of H. stricta are aimed at the bee's head and thorax while the three stigmas of It. fasciculata are aimed at the bee's abdomen. However, when the foraging bee combs itself, between flowers, all the loose pollen on the head and thorax will be swept into the deposits of the legs and abdomen. The stigmas of H.fasciculata can still receive pollen of H. stricta under such circumstances. To remove pollen from the cluster of anthers of H. fasciculata bees must apply the same thoracic vibration as applied to the flowers of H. stricta (BERNHARDT 1984). Pollen of H. fasciculata may still be deposited on the stigmas of H. stricta if the bee has not combed all H. fasciculata from her thorax.

I would argue that the symmetry of the sexual organs of Hibbertia flowers, combined with the actual size of all the floral organs, determines the diversity of bees that may forage on the flowers of Hibbertia and which bees may pollinate them. Lasioglossum spp. are the only bees that pollinate H. stricta in the Brisbane ranges but they weren't the only bees collecting pollen from sympatric angiosperms at that site (BERNHARDT & WALKER 1984). Exoneura spp. commonly collected pollen from the anthers but their bodies were too small to contact both the poricidal opening of the anther and the adjacent stigmas. Exoneura remained a pollen thief on H. stricta.

The rotate symmetry of the androecium, coupled with the realignment of the stigmas in H. fasciculata, expands the number of potential pollinators to bee taxa smaller than Lasioglossum spp. Leioproctus spp. also collect the pollen of H. fasciculata and they are a major pollen vector of this species not merely thieves. The erect-suberect flowers of H. fasciculata provide open access to bees that do not cling to a nodding cluster of anthers while foraging. Even the naturalized, A. mellifera, is capable of collecting pollen of H. fasciculata although the saliva-glued pollen in the corbiculae are probably not deposited on the stigmas.

Note how the canalization of floral morphology in other buzz- pollinated flowers may correlate with a reduced spectrum of primary pollinators (see review by BUCHMANN 1983). The bees that do pollinate


these flowers tend to belong to genera with polylectic habits of floral foraging (MAcIOR 1974, BOWERS 1975, BERNHARDT & MONTALVO 1977, BUCHMANN & al. 1977). Australian Lasioglossurn spp. do not appear to be exceptions to this rather general rule (BERNHARDT 1982, 1984, BERNHARDT & WALKER 1985a).

Bees and Beetles in the Pollination of Hibbertia. In contrast to relictual angiosperms such as palms (UHL & MOORE 1977), Cyclanthaceae (MOORE 1983), Nymphaeaceae (SCHNEIDER 1979) and the woody magnolioids (CORNER 1952, TmEN 1974, 1980) Hibbertia spp. seem to show few of the classic traits associated with beetle-pollination (FAEOR~ & VAN DER P~JL 1971). Only the unpleasant odor of H.fasciculata is suggestive of a system pollinated by beetles. Floral odor, however, is not always a useful feature for classifying pollination syndromes. Field workers have often com- mented on the unpleasant acridity of the flowers of Curcubita spp. yet these flowers appear to be pollinated almost exclusively by bees (see review by FREE 1970). Some Magnolia spp. have rather sweet fragrances (TmEN & al. 1975) but beetles remain the dominant pollinators. As W~LLIAMS (1983) has noted, while the human nose is an adequate tool for the qualitative and quantitative identification of some fragrance compounds simply smelling a flower does not automatically permit an easy definition of a pollination syndrome. Furthermore, there is now some evidence to suggest that, while the floral architecture of some primitive angiosperms may have changed radically to restrict prospective foragers the composition of the floral fragrance has remained remarkably constant (TmEN & al. 1985).

Previous reports of beetle-pollination in Hibbertia (KEIGHERY 1975, ARMSTRON~ 1979) undoubtedly require more detailed investigations. Of course, it must be noted that the beetles that pollinate some Australian angiosperms belong to specialized subfamilies within the Scarabaeidae and Buprestidae. These beetles bear modified mouthparts and digestive tracts specifically for the consumption of pollen and nectar (see review by ARMSTRONG 1979). The attractants employed by primitive angiosperms in other parts of the world may not apply here. However, T. HAWKESWOOD (personal communication) has repeated the work of KHEIaHERY (1975) on H. hypericoides. HAWKESWOOD states that Diphucephala spp. eat the floral structures ofH. hypericoides and use the wide corolla as a mating site. The pollen transported by the beetles belongs to other plants flowering sympatrically with H. hypericoides! These beetles undoubtedly pollinate some Myrtaceae but they are floral predators of H. hypericoides.

Bright yellow petals, staminal filaments, inflated-poricidaal anthers and slender styles seem to be modifications for bee-pollination in many Hibbertia spp. Bee-pollination is found in other genera within the Dilleniaceae (VOGEL 1978) and the syndrome of nectarless/pollen rich flowers seems to hold. In the neotropics, large bees pollinate Curatella


a m e r i c a n a (FRANKIE & al. 1983) while S a u r a u i a veraguens i s depends o n medium size bees especially M e I i p o n a spp. (HABER & BAWA 1985). Information on paleotropical genera has not been actively pursued, unfortunately. W o r m i a spp. are probably bee-pollinated (CORNER 1952) and the pollen o f D i l I e n i a spp. are collected by native A p i s spp. (Now~cKE & MESELSON 1984). Comparat ive studies on pollination syndromes within the Di l l en iaceae may, in the long term, offer greater information regarding floral evolution in H i b b e r t i a than by searching for comparative syndromes within the M a g n o l i i d a e (sensu CRONQUTST 1981).

Fieldwork was conducted through the Plant Cell Biology Research Centre at the School of Botany, U. of Melbourne under the supervision of Professor R. B. KNox. Funding was provided by the Australian Research Grants Scheme and the Australian Department of Education (CPPER). I wish to express my gratitude to Dr. K. WALKER, of the National Museum of Victoria, for his continued cooperation in the identification of insects. Mr. PETER CHANCE generously allowed access to his property. Miss P. O'NEAL, Miss T. Houan, and Miss T. Hough assisted with transportation and insect collections.

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Address of the author: PETER BERNHARDT, Department of Biology, St. Louis University, St. Louis, MO 63103, U.S.A.

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Bee-pollination inHibbertia fasciculata (Dilleniaceae)