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Pollination and flower diversity in Scrophulariaceae.

II. Introduction

Some families of flowering plants have evolved an amazing variety of floral forms. This variation is the result of selection by pollinators at the population level, which leads to adjustments in floral form that improve pollen transfer efficiency and, therefore, fruit set. For example, in Viola cazorlensis (Violaceae), variability of size and shape of corolla lobes within one population leads to significant differences in the dissection of flower outlines; the day-flying hawkmoth pollinator can distinguish those shape differences and discriminate in favor of more dissected corollas, leading to measurable differences in fruit production (Herrera, 1993). Coevolution of flowers and pollinators has led to extreme flower shapes in some orchids in which flower tubes, and their pollinator's tongues, can reach 30 cm in length; only if the visiting hawkmoth's tongue is shorter will the insect press up to the pollinia and so effect pollination and fruit set, thus selecting for longer tubes (Nilsson, 1988). Corolla curvature in Centropogon (Lobeliaceae) was found to be relatively labile and reversed to comparative straightness where no pollinating sicklebill hummingbirds were available (Stein, 1992). A change in pollinators may occur if populations are dispersed beyond the range of their species' usual pollinators. In Dalechampia (Euphorbiaceae), Armbruster (1993) usually observed pollinator transitions in which flowers were visited by both old and new pollinators, but 14% of transitions may have been instantaneous; the pollination systems in Dalechampia were labile, resulting in repeated parallelisms and reversals. Convergences decrease the usefulness of flower features in classification (Ornduff, 1978), but mapping of pollination systems onto phylogenetic trees allows inferences about the ancestor of a group (Armbruster, 1993).

In most animal-pollinated flowers, the organs, especially the corolla, are specialized with colors and scents to function as a pollinator attractant. Further specializations let the flower serve also as a pollinator manipulator, excluding organisms that would take nectar without effecting pollination and positioning a legitimate pollinator in a way to ensure pollen transfer. Such additional specializations can occur in flowers with free perianth parts, as in the evolution of a hummingbird-pollinated species of Delphinium (Ranunculaceae) from bumblebee-pollinated ancestors with zygomorphic flowers (Guerrant, 1982). The increased potential for variation of flowers with fused parts was discussed by Robinson (1985). A zygomorphic corolla consisting of a tube as well as lobes adds great potential to a plant lineage's ability to exploit different and more reliable pollinators, thus requiring a lower investment of flowers and pollen. A good example of such a potential and its realization are the Scrophulariaceae, a cosmopolitan family of 190 genera and 4000 species. It was last reviewed by Wettstein (1891). To date, familial and tribal delimitations, and the relationships between tribes, have not been resolved (Burtt, 1965; Thieret, 1967). A recent survey of sequence variation of a chloroplast-encoded gene yielded results indicating that tribes Cheloneae and Gratioleae are not monophyletic and that the Scrophulariaceae may consist of three independently derived lineages within the order Scrophulariales (DePamphilis et al., 1994; Olmstead & Reeves, 1995).

The family Scrophulariaceae encompasses a great diversity of floral forms. Pennell (1935) concluded that "it is in the form and color of the corolla that the Scrophulariaceae show a range of variation probably exceeded among flowering plants only by the orchids. Yet this diversity of structure may be readily interpreted as transformations of a simple primitive pattern."

The most common scrophulariaceous flower (see Table I) has a five-lobed calyx, a campanulate, slightly gibbous corolla tube bearing five lobes (two forming the upper lip, three the lower), four stamens attached to the inside of the corolla tube, and a bicarpellate pistil. This flower type also occurs in related families such as Bignoniaceae and Gesneriaceae (Endress, 1994). Striking modifications of this basic pattern have occurred as the flowers coevolved with a variety of pollinators.

III. Variation in Flower Organs of Scrophulariaceae

All organ types show considerable variation across the family (Bentham, 1876; Wettstein, 1891; Endress, 1994). The calyx lobes can be free or only minute tips on a campanulate cup; they can be equal or very asymmetric [for example, in the tribe Antirrhineae (Sutton, 1988), where there can be strong size differences between adaxial and abaxial lobes, or between the median adaxial lobe and the rest]. The stamens can be inserted very low on the corolla tube or high near the sinuses of the corolla lobes; their filaments can be short or very long and may have broad or pubescent bases; in the lower stamens of Craterostigma (tribe Gratioleae; see also Table I), each filament base forms a yellow bulge that mimics an anther, whereas in a species of Torenia (Gratioleae/Torenieae) each develops a pinlike branch (Magin et al., 1989). The anther thecae can be separated by a broad connective or confluent, symmetric or asymmetric, and be parallel or divergent to various degrees at maturity. Usually the thecae dehisce longitudinally; the exception is Seymeria cassioides (Agalineae), in which the anthers open by apical pores (Gwynn et al., 1978). The adaxial and abaxial stamen pairs show various degrees of asymmetry; either pair can be missing entirely or develop only as staminodes, or there may be a fifth stamen or staminode present in the adaxial median position. The ovary can be round or compressed, can taper to a point or be notched, and can bear many small or very few large seeds on its two placentae. The short or very long style terminates in a two-lobed or entire, capitate, decurrent, or punctate stigma.

The most striking variation of all flower organs is exhibited by the corolla. There are Scrophulariaceae with yellow, white, orange, red, pink, or blue flowers, with or without nectar guides in the form of spots, stripes, or hairs. The corolla tube may be long or very short, narrow or wide, nearly radially symmetric or very gibbous; the entrance of the flower may be closed by an upward bulge (a palate: e.g., Antirrhinum, Antirrhineae) or a downward bulge (a balloon: e.g., Calceolaria, Calceolarieae), or the corolla tube may be widely flaring. Style and anthers may be enclosed in a keel formed by the lower middle petal or by a keel formed by the enlarged base of the upper petals. The pollinator reward can be hidden in one median (Linaria, Antirrhineae) or two lateral (Diascia, Hemimerideae) spurs. The corolla lobes can be symmetric or not, especially those of the upper lip can be reduced and minute, or partially or completely fused together. Yet all these flower shapes are probably derivatives of open, bell-shaped, bee-pollinated corollas, since these occur throughout the Scrophulariales (Pennell, 1935; Bentham, 1876).

Each flower has evolved to fit to its pollinators (Straw, 1956a); stabilizing selection maintains that effective shape, since pollinators discriminate against rare corolla shape variants within species (Levin, 1972). However, new species or hybrids, or species ending up in a new habitat, are usually "adopted" by some pollinator - this has been observed, for example, in Penstemon (Cheloneae) (Straw, 1955, 1956b) and in tropical Bignoniaceae (Gentry, 1990). Once a switch has occurred, flower and pollinator can coevolve, and the plant species can develop features resulting in reproductive isolation (Grant, 1994). Scrophulariaceae are pollinated by bees, wasps, flies, moths, butterflies, and hummingbirds, and their flowers are shaped and colored accordingly.

IV. Pollination in Scrophulariaceae

A. POLLINATOR ATTRACTANTS

Flowers attract birds and insects by using bright colors and attract moths by using odors. Bird-pollinated flowers are often red, since bird eyes probably perceive like human ones. The importance of flower coloration has been shown in two species of Mimulus (Gratioleae) with red flowers attractive to hummingbirds. Both species were discovered to have mutants with yellow flowers, which were preferred by bumble bees and avoided by hummingbirds, thus leading to partial reproductive isolation between the normal populations and the variants (Vickery, 1992).

Insects are able to see ultraviolet radiation. Pink and blue look green to them, although brighter than the background green of vegetation; yellow appears red to insects, and UV-reflecting surfaces are seen as blue (Richards, 1986). This type of vision seems to optimize discrimination of flower hues in bees (Chittka et al., 1993). The yellow flowers of Verbascum thapsus (Verbasceae) are UV reflective on the periphery of the petals; [TABULAR DATA FOR TABLE I OMITTED] Linaria vulgaris (Antirrhineae) and Veronica serpyllifolia (Veroniceae) do not show such patterns (Milligan & Kevan, 1973). In Collinsia (Cheloneae/Collinsieae), the upper lip absorbs UV radiation, whereas the lower lateral lobes reflect it, and the folded median lobe shows a mixed pattern (Rust & Clement, 1977).

Not much information is available on floral scents in Scrophulariaceae, possibly because they are usually not very noticeable. Sutton (1988) commented on the weak scents of most Antirrhineae flowers; floral odors may be more noticeable in species pollinated by moths. He also observed that species of Linaria in that tribe have scents similar to violets and strawberries.

B. MANIPULATION OF POLLINATOR BEHAVIOR

Pollinator behavior must be manipulated by the flower to optimize pollen transfer. In radially symmetric flowers, it does not matter from which direction the pollinator enters, but bilaterally symmetric flowers such as those of the Scrophulariaceae induce more specific behavior to ensure that stigma and anthers are touched effectively. Nectar guides, such as the contrasting spots or stripes on the abaxial corolla tube of many Scrophulariaceae, are orientation cues to which bees and wasps respond. On unspotted mutant flowers the insects will land, but they do not then act with normal purposefulness (Waser, 1983). In Scrophulariaceae, flowers that have switched to bird pollinators, or those that have evolved closed corollas, do not bear these spots.

A number of strategies have evolved to encourage cross-fertilization. The flowers can mature stigma and anthers at different times (dichogamy). The majority of Scrophulariaceae studied to date is protogynous [Scrophularia nodosa (Cheloneae/Verbasceae), Bartsia alpina, Pedicularis oederi, P. sceptrum-carolinum (Rhinantheae) (Faegri & van der Pijl, 1979); Veronica beccabunga (Veroniceae) (Grime et al., 1988)] rather than protandrous (Digitalis purpurea, Digitaleae) (Darwin, 1877; Best & Bierzychudek, 1982). Anthers and stigma can be positioned at a distance (herkogamy), in such a way that an incoming visitor touches the stigma first, hopefully depositing suitable pollen, and then gets showered by the anthers. In Mimulus (Gratioleae), the bilobed stigma is sensitive and closes if touched. If no pollen was deposited, it reopens (Darwin, 1877). Gender dimorphism in New Zealand Hebe (Veroniceae), with bisexual and male-sterile flowers, may have evolved to enforce outcrossing in mountain areas where only less efficient pollinators such as flies and beetles were available rather than bees, as in the lowlands (Delph, 1990).

C. POLLINATOR REWARDS

The pollinator reward in the Scrophulariaceae consists usually of nectar, produced by a ringlike, asymmetric nectary at the base of the ovary or, in Penstemon (Cheloneae), on the external bases of the stamens, opposite the ovary (Straw, 1956b). In Digitalis (Digitaleae), nectar production was ample and lasted from the second day of anthesis to the sixth before tapering off; flowers near the inflorescence tips produced less nectar (Daumann, 1970). Intraspecific differences in nectar production were also observed by Delph and Lively (1992) in a gynodioecious species of Hebe (Veroniceae), in which the "male" (hermaphrodite) flowers produced four times as much nectar as the "female" (male-sterile) ones.

Elisens and Freeman (1988) studied the nectar sugar composition in New World Antirrhineae, which are pollinated by both long-tongued and short-tongued bees and by hummingbirds. Nectars were sucrose-dominant in all genera (except for a hexose-dominant nectar in a species of Mohavea) but still varied according to pollinator type; hummingbirds prefer a high sucrose content (this has also been observed in other, unrelated bird flowers), as do long-tongued bees, whereas short-tongued bees visit low-sucrose flowers (Elisens & Freeman, 1988). In Scrophulariaceae, nectars seem to have changed from sucrose-dominant to hexose-dominant in several instances; apparently sugar ratios do not vary in different environments, and hybrids resemble one parent or have intermediate values (Elisens & Freeman, 1988). Macior (1988) observed intraspecific differences in nectar sugar type between disjunct North American and Japanese populations of Pedicularis.

Bees also collect pollen, for example, in Pedicularis and other Rhinantheae (Kwack, 1977; Macior, 1983). Some Scrophulariaceae do not produce nectar, and here pollen is the only reward. In Verbascum (Verbasceae), the upper stamen pair serves as feeding stamens (Richards, 1986). In some genera from Africa and South America belonging to three different tribes, the pollinator reward consists of oil: Diascia, Angelonia, Hemimeris, Alonsoa (Hemimerideae), Calceolaria (Calceolarieae), Basistemon, Bowkeria, Anastrabe (Cheloneae), Colpias (Antirrhineae) (Buchmann, 1987), and Monttea (Gratioleae) (Simpson et al., 1990). Complex mixtures of lipids are secreted by glandular trichomes (elaiophores) in the bottom part of the gibbous corolla tube [e.g., Ixianthes (Cheloneae) (Steiner, 1993)], in pouchlike depressions on the inside of the lower corolla lip [e.g., in Monttea (Simpson et al., 1990) and in Angelonia (Vogel & Machado, 1991)], or in twin spurs which coevolved with very long forelegs in the pollinating bee [in Diascia (see below) (Vogel, 1984; Steiner, 1990)].

V. Coevolution of Flower and Pollinator

A. THE BASIC BELL-SHAPED FLOWER

Open, campanulate, bee-pollinated flowers occur in the various tribes of the Scrophulariaceae (Table I). In the corolla tubes of these flowers the stigma and anthers are positioned at the adaxial side, due to asymmetric filaments and styles. Hence, if the bee enters with the feet on the abaxial side, pollination is nototribic - the stigma touches the bee at the notum on the back [ILLUSTRATION FOR FIGURE 1 OMITTED]; if the bee enters upside down, pollination is sternotribic - the stigma touches at the sternum in the front [ILLUSTRATION FOR FIGURE 2 OMITTED]. Trichomes along one side of the corolla tube give the insects a foothold and induce them to enter the flower in the appropriate way. If these hairs are on the lower side, an appropriately sized bee is dusted with pollen on its back, as, for example, in Digitalis (Digitaleae) (Darwin, 1877) and the large-flowered prairie species Penstemon grandiflorus and P. cobaea (Cheloneae) (Pennell, 1935), which are pollinated by correspondingly large bumblebees. If the hairs are on the upper side, the bee turns over and pollen is dusted on its front, as, for example, in Aureolaria, Agalinis (Agalineae), and Gratiola neglecta (Gratioleae) (Pennell, 1935). Campanulate flowers are also visited by wasps, for their rewards of nectar and/or pollen. The odd zygomorphic, greenish-brown corollas of Scrophularia (Cheloneae/Verbasceae) are basically campanulate, but their size is reduced compared to other genera in the family. The small flowers have a ringlike nectary and are protogynous: The stigma becomes receptive first, while the filaments remain bent; after pollination, the stigma bends and the stamens straighten and release pollen. They are visited by wasps, small bees (Faegri & van der Pijl, 1979), and syrphid flies (Ortega-Olivencia & Devese-Alcaraz, 1993). Since the size and shape of the flower is adapted to the wasp's head, wasps would seem to be the most efficient pollinators; the staminode may act in forcing the insect's head downward so that its chin brushes anthers or stigma (DeVos, 1983).

The potential of campanulate flowers for adaptation to different pollinators is exemplified by the genus Penstemon (Cheloneae), which, in addition to various bees (honey, carpenter, bumble, and solitary bees), is pollinated by hummingbirds, coleopterans, masarid wasps, bee flies, syrphid flies, moths and other lepidopterans, dipterans, and hymenopterans (Schmid, 1976). Apparently, despecialization can occur if pollinators are not available in a new habitat; the narrow-tubed flowers of a New Zealand species of Ourisia (Digitaleae) are pollinated by small halictid bees and syrphids, which may carry pollen on any part of their bodies, not strictly nototribically (Schlessman, 1986).

B. NARROW COROLLA TUBES

Butterfly-pollinated flowers are modified from the campanulate bee flower with a longer, narrower tube and large petal lobes serving as a landing platform [ILLUSTRATION FOR FIGURE 3 OMITTED]. The nectar at the base of the ovary can be reached only by an insect with a long proboscis, while pollen is deposited on its head. Examples of this flower type occur in both subfamilies of the Scrophulariaceae, for example, in Penstemon (Cheloneae) and Buchnera (Agalineae) (Pennell, 1935). The similar moth-pollinated flowers differ in having small petal lobes, since they need not provide a foothold for their hovering pollinators [ILLUSTRATION FOR FIGURE 4 OMITTED]. The two (unrelated) species Penstemon albidus and P tubaeflorus both show this flower shape. Their white corollas have sticky glandular hairs inside the tube (Pennell, 1935), possibly to exclude nectar thieves.

Hummingbirds are also hoverers that pollinate tubular flowers [ILLUSTRATION FOR FIGURE 5 OMITTED]; they are more attracted to red flowers or at least orange or yellow ones. In Agalinis (Agalineae), the flowers of bee-pollinated North and South American species are bell-shaped, pink with guide spots and lines, and stigma and anthers positioned at the rim of the corolla tube (Pennell, 1935); the flowers of presumably hummingbird-pollinated South American species are tubular, red, with exserted stigma and stamens (J. M. Canne-Hilliker, pers. comm.). Some Penstemon (Cheloneae) species are pollinated by both bees and hummingbirds; they may be in transition between two pollinators (Lyon & Chadek, 1971). Bee-pollinated Castilleja (Rhinantheae) species also receive moderate hummingbird visitation (Waser, 1983). Hummingbird flowers have nectar sugar types and concentrations different from bee-pollinated ones; it would be interesting to compare this in Castilleja species to see if the reward is of intermediate type.

Pseudolysimachion longifolium (Veroniceae), which has dense racemes of more or less rotate (i.e., short-tubed and large-lobed) flowers, is pollinated by syrphid flies (Noll, 1883) or small bees (Pennell, 1935) [ILLUSTRATION FOR FIGURE 6 OMITTED] that possibly touch the stigma and anthers while trying to land on the dense racemes. The superficially similar flowers of Seymeria (Agalineae) could also be syrphid fly pollinated (Pennell, 1935).

C. EXCLUSION OF INEFFECTIVE VISITORS

In bell-shaped flowers, there is the possibility of small visitors reaching the nectar while not coming in contact with pollen and stigma. Several different modifications have evolved to exclude such visitors. Possibly the Penstemon (Cheloneae) "beardtongue" (staminode in the fifth, median position) has such a function, its hairs helping to exclude small insects while serving as a foothold for larger ones (Straw, 1956b). Another exclusion technique is to arch the bottom of the corolla tube upward to close the entrance [ILLUSTRATION FOR FIGURE 7 OMITTED]; this allows only strong insects to enter, and they are forced to scrape along stigma and stamens [ILLUSTRATION FOR FIGURE 8 OMITTED]. In the unrelated genera Chaenorrhinum (Antirrhineae), Chelone (Cheloneae), Mimulus (Gratioleae), and also Penstemon hirsutus, the tube is partially closed with such a bulge (Pennell, 1935). In Linaria and Antirrhinum (Antirrhineae) the tube is completely blocked by this arched "palate" which is reinforced with grooves and folds to form an elastic "joint" which snaps closed (Muller, 1929). This palate is distinctively colored as a signal to the pollinators. Strong, heavy long-tongued bees have learned how to reach the nectar. But hawkmoths have also learned to probe the orange spot of Linaria for access to the reward. They will do so even if the spot is experimentally offered in the wrong position. Other bees who are too light to force the entrance or too short-tongued to reach into the spur steal nectar by biting a hole in the spur (Waser, 1983). Having attained one form of specialization does not make it impossible to switch pollinators, however. Within the genus Antirrhinum, one species, A. coulterianum, has probably become moth-pollinated, its white flowers having a large palate grooved for access to the copious nectar and exserted anthers to touch the hovering pollinator (Thompson, 1988). Species of section Macrocentrum of Linaria (Antirrhineae) are likely to be pollinated by moths. They are scented at certain times of the day, and their poorly developed palate does not form a barrier to a long moth proboscis able to reach through the narrow tube into the exceptionally long spur (Sutton, 1988).

D. WIDE COROLLA TUBES

The large, open flowers of Verbascum (Verbasceae) are visited by various insects, and bees come to collect pollen. The upper three stamens are shaped differently from the lower two and have more and longer hairs (Richards, 1986). Pollination is probably sternotribic from the lower stamens while the bee handles the upper, hairy feeding stamens [ILLUSTRATION FOR FIGURE 9 OMITTED].

On the flowers of Veronica (Veroniceae), which are also saucer-shaped and usually very small, insects are rarely seen. In several species the flowers are probably selling (Grime et al., 1988) or visited by flies (Pennell, 1935). In the bee-pollinated species of Veronica and the very similar Parahebe (Veroniceae), the bee grasps the attenuate filament bases and receives pollen on its abdomen (Garnock-Jones, 1976) [ILLUSTRATION FOR FIGURE 10 OMITTED].

E. KEEL FLOWERS

Collinsia (Collinsieae/Cheloneae) flowers are an interesting variation on the bell-shaped flower. They mimic leguminous flowers with a standard of the two upper petals, wings of the two lateral ones, and the lower middle petal is folded to form the keel. As in the Leguminosae, the keel contains the style and stamens. Collinsia is pollinated by bumblebees, honey bees, and other bees. It is also visited (without effect) by moths, butterflies, and flies. If a bee lands on the keel to collect nectar and pollen, its weight causes a lowering of the petals while stigma and stamens stay in place and so emerge from the keel for sternotribic pollination (Rust & Clement, 1977) [ILLUSTRATION FOR FIGURE 11 OMITTED].

The flowers of the Rhinantheae, such as Pedicularis, Melampyrum, Rhinanthus, Castilleja, and Lamourouxia [the latter may be a member of the Agalineae, according to its seed morphology in Barringer's (1984) study], also show strong bilateral symmetry. Here the lower three petal lobes form a landing platform of varying size. The upper two petal lobes are very small, but the corolla subtending them is enlarged to form a keel or galea. As in Collinsia (Collinsieae/Cheloneae), where the keel was on the lower side, the galea encloses the style and stamens. These flowers are, again, pollinated mostly by bees but also visited by hummingbirds, butterflies, and syrphid flies (Kwack, 1977). Pollination can be nototribic or sternotribic. Nectar-collecting long-tongued bees approach the flower upright and stick their head inside. They are then touched by the stigma. By entering further, the bee separates the sides of the keel, the pollen chamber opens, and pollen sifts down onto its back [ILLUSTRATION FOR FIGURE 12 OMITTED]. The bee cannot remove all of it and so transfers some to the next flower.

Short-tongued bees bite a hole into the corolla tube close to the nectary, but, since they also collect pollen, they still have a role in pollination. Some flowers offer only pollen, and these are also pollinated sternotribically. For this, the bee turns over, grasps the edge of the keel with its mandibles, and pulls open the keel, Then it buzzes its wings [ILLUSTRATION FOR FIGURE 13 OMITTED]. The vibration loosens the pollen, which sifts down onto the bee's body and is then groomed into the bee's corbiculae. Pollination occurs when the bee's front curves around the next flower and touches the stigma with residual pollen (Kwack, 1977). The long corolla tubes of certain species of Pedicularis (Rhinantheae) may have evolved to ensure that the rostrum extends beyond the plant's foliage and so is accessible for buzz pollination (Macior & Sood, 1991). Some species of Pedicularis have specialized so that the flowers look elephantlike, with the petal lobes similar to ears and the keel drawn out into a long trunk that turns two and a half times. This trunk, with its enclosed stigma, touches the bee as it forages (Wendelbo, 1965).

One exception among the bee-pollinated flowers of the Rhinanthaceae is a species of Orthocarpus that grows as colonies with interwoven branches. Its flowers are small, the corolla reaching only to the tips of the calyx lobes. The nectaries are on the inside of the corolla tube near the lower corolla lobes. These flowers are pollinated by ants (Kinkaid, 1963).

F. UNUSUAL COROLLA TUBE MODIFICATIONS

More specialized relationships have evolved between some Scrophulariaceae and oil-collecting bees feeding their young with a mixture of oil and pollen. In Calceolaria (Calceolarieae), the decorative flower balloon is formed by the inflated lower corolla tube. In one species, the ridges of the upper and lower sides of the corolla fit together so that the flower is tightly closed. The stigma is surrounded by a groove formed by the upper lip. The stamens have one sterile and one fertile anther side and are attached so as to give a lever effect. A patch of trichomes at the enclosed edge of the lower lip produces the oil (Ritterbusch, 1976). Sternotribic pollination has been observed in these flowers [Sersic, 1991 (abstract seen)]. Probably as the bee enters, first the stigma is touched with pollen from other flowers; then, as the bee forces its way further inside, it trips the anther lever and is showered with new pollen [ILLUSTRATION FOR FIGURE 14 OMITTED].

Flowers of the genus Diascia (Hemimerideae) in South Africa and the bee pollinating them are a remarkable example of coevolution. The bee has very long front legs with specialized hairs to blot up oil. The flowers of Diascia have no nectar and produce little pollen, but instead secrete fatty oils in two spurs at the base of the lower corolla. This forces the bee to assume a position designed to effect the transfer of pollen on its chest. The blossoms are usually pink and UV reflecting. At the base of the upper corolla there are two "windows," i.e., translucent, UV-absorbing, yellow-dotted depressions that serve as orientation cues. The bee puts its head toward the windows, and then it is able to stick its front legs into the spurs to gather oil. This also brings the bee's front in contact with the short style and stamens [ILLUSTRATION FOR FIGURE 15 OMITTED]. As the bees evolved longer and longer legs, the spurs had to become longer, too, to ensure that the bee still had to press against the stigma and stamens. Some other Diascia species and also Hemimeris are oil producers as well, but not in spurs, and there the pollinators need no specially elongated legs - one such bee species blots up the oil with its specialized abdomen (Vogel, 1984; Steiner, 1990; Steiner & Whitehead, 1990).

G. SELF-POLLINATION

If no pollinator arrives, some Scrophulariaceae flowers can also self-pollinate. Usually the stigma is positioned only a few millimeters in front of the longer stamen pair. After a certain time, the filaments or the corolla to which they are attached elongate and pollen reaches the stigma. In Mimulus (Gratioleae), for example, selfing can occur when the lower stigma lobe curls back towards the anthers. In some populations the abscising corolla, with the attached stamens, slid over the stigma (Dole, 1992). However, corolla dragging may not contribute to selfing, at least in some populations of this plant (Dudash & Ritland, 1991). Elisens (1985) found that seed set from self-pollinations in species of subtribe Maurandyinae (Antirrhineae) varied at the intra-individual and interspecific levels; he characterized this subtribe as facultatively autogamous/xenogamous, with mostly showy flowers having a prevalence of dichogamy and herkogamy. Digitalis (Digitaleae) sets some seed if insects are excluded and the plant is shaken (Darwin, 1877). Similarly, the long-tubed, scarlet, nectar-rich flowers of a South American species of Ourisia (Digitaleae) selfed spontaneously in areas where no pollinators (presumably hummingbirds) were observable, probably due to the harsh climate (Arroyo & Penaloza, 1990). Low pollinator availability due to climate is also the likely factor in the prevalence of autogamy in species (in one case, populations of a species) of Parahebe (Veroniceae) in New Zealand. Here, the entomophilous lowland species have large colorful flowers with nectar guides, spreading corolla lobes, short tubes filled with trichomes, and divergent stamen filaments. The subalpine, alpine, and nival species are autogamous, with usually white, tubular or funnelform corollas that are glabrous and shorter-lobed and have short erect filaments, causing close proximity of anthers and stigma (Garnock-Jones, 1976).

Some Scrophulariaceae even produce cleistogamous flowers which are specialized for selfing and never open. Often, cleistogamous flowers are produced early in the growing season or are induced by water, drought, shade, or light. They have been found on some Antirrhinum, Linaria (Antirrhineae), and Vandellia (Gratioleae?) species. Heteranthia dubia (Aptosimeae?) produces closed flowers underwater, but if they reach the surface, they open (Uphof, 1938).

VI. Conclusions

The Scrophulariaceae are pollinated in very diverse ways - by bees collecting nectar, pollen, or oil in various manners; by butterflies, moths, flies, wasps; and by hummingbirds. Flower shapes in the family range from slightly zygomorphic bell-shaped to narrow long-tubed (with and without large spreading lobes), short-tubed, wide-tubed, to closed by palates, keeled on the upper or lower side of the flower, or outcurved into a balloon, and the pollinator reward may be hidden in one or two spurs [ILLUSTRATION FOR FIGURES 1-15 OMITTED]. This enormous variation is probably derived from bee pollination of simple bell-shaped flowers, since that is the most widespread mode of pollination in the tribes of this family (Table I). Bell-shaped flowers occur in Verbasceae, Cheloneae, Calceolarieae, Gratioleae, Digitaleae, Agalineae - i.e., in tribes of both subfamilies. This flower type changed (possibly several times during the phylogeny of each tribe and genus), optimizing its efficiency when encountering other widespread pollinators. Tubular flowers for butterfly, moth, and hummingbird pollination have evolved convergently in Cheloneae, Manuleae, Selagineae, Digitaleae, and Agalineae; and short tubular flowers for short-tongued bee and fly pollination in Veroniceae and Agalineae. The opposite flower type, wide corollas, also for bee pollination, occurs in Verbasceae and Gratioleae as well as Veroniceae. Palates close the corolla tubes of species in Antirrhineae, Gratioleae, and Cheloneae to be accessible only to strong, heavy bees. Corolla keels enclosing the anthers and stigma at the upper side of the flowers may be a parallelism in Rhinantheae and Agalineae that evolved together with pollen-gathering behavior of bees. Thus, these floral features cannot be used to characterize these tribes. On the other hand, some specialized features are (still) unique since they coevolved with equally specialized pollinators: the balloonlike corolla of Calceolaria (Calceolarieae) and the two spurs of Diascia (Hemimerideae) are visited by different bees collecting oil with specialized absorbent pads. The keel formed by the lower petal of Collinsia (Gratioleae/Collinsieae) requires bees of a certain minimum weight and behavior to operate it.

Bee pollination of bell-shaped flowers could also be the basic pollination pattern in the families related to the Scrophulariaceae. Other families of the order Bignoniales/Lamiales show similar variation on the basic campanulate, slightly asymmetric flower form (Endress, 1994). Their flowers have evolved various features to attract insects and birds, cue them into the correct positions, and reward them, usually with nectar. The Gesneriaceae exhibit broad ranges in floral morphology, frequently with morphological and pollinator switches within genera; they are often pollinated by hummingbirds but also by bees, bats, butterflies, moths, flies, and perfume-collecting male bees (Endress, 1994). The large showy flowers of the Bignoniaceae are visited by large bees, birds, bats, and hawkmoths (Gentry, 1990; Endress, 1994). The Acanthaceae often exhibit corollas with lower corolla lips larger than the upper ones; they are usually pollinated by bees but also, in some cases, by hummingbirds, flies, and moths (Endress, 1994). Some Acanthaceae pollinated by hummingbirds with strongly curved beaks exhibit strongly curved long-tubed flowers which probably evolved from straight-tubed hummingbird flowers (McDade, 1992). Convergences in flower morphology occur frequently between the families of the Scrophulariales. For example, a "beardtongue" staminode like the one in Penstemon (Cheloneae, Scrophulariaceae) also occurs in Jacaranda (Bignoniaceae); petal aestivation, or folding in the buds, shows both ascending and descending patterns within Scrophulariaceae, Lentibulariaceae, and Bignoniaceae, ascending and quincuncial patterns within Acanthaceae, and descending and quincuncial patterns in Orobanchaceae [whereas their presumed closest relatives, Rhinantheae (Scrophulariaceae) have ascending petal folding]; personate corollas similar to those of Antirrhineae (Scrophulariaceae) are exhibited by some Acanthaceae, Gesneriaceae, Bignoniaceae, and Lentibulariaceae; other parallelisms occur in ovary structure, ovule number, sensitive stigma lobes, and postgenital fusion of the anthers (Endress, 1994).

The Lamiaceae have sucrose-dominant nectar, like the Scrophulariaceae (Elisens & Freeman, 1988); hummingbird flowers in Acanthaceae, Lamiaceae, and Scrophulariaceae show similar nectar sugar ratios (Freeman et al., 1984). The only exception are the wind-pollinated Plantaginaceae, in which the flowers have a very reduced perianth and long-exserted stamens and styles, and the water plants Hippuridaceae and Callitrichaceae, also with reduced flowers.

The flower convergences caused by coevolution with pollinators operating at the population level decrease the usefulness of mature floral characters for estimating the phylogeny and for devising a corresponding classification above the generic level. However, the Scrophulariaceae and their relatives illustrate the variability and evolutionary potential of tubular-flowered plants.

VII. Acknowledgments

The author thanks Nancy G. Dengler, Tammy L. Sage, and Elizabeth A. Kellogg for critical readings of the manuscript, and gratefully acknowledges financial support through an Ontario Graduate Scholarship during part of this project, and partly through NSERCC Operating Grants A3430 and A5720 to Nancy G. Dengler and Timothy A. Dickinson, respectively. This work was part of a project conducted in partial fulfilment of the requirements for a Ph.D. at the University of Toronto.

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Title Annotation:Interpreting Botanical Progress
Author:Kampny, Christine M.
Publication:The Botanical Review
Date:Oct 1, 1995
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