Floral Isolation Between Ornithophilous and Sphingophilous

Proc. Natd. Acad. Sci. USA Vol. 89, pp. 11828-11831, December 1992 Ecology Floral isolation between ornithophilous and sphingophilous species of Ipomopsis and Aquilegia (mechanical lsolation/hummlnbfrd pon /hawkmoth natl/ aptatln/Ipomopuis aggregata) VERNE GRANT Department of Botany, University of Texas, Austin, TX 78713 Contributed by Verne Grant, September 4, 1992 ABSTRACT The Ipomopsis aggregate group (Polemoni- These cases involve floral isolation between hummingbird- aceae) and Aqulegia formosa-Aquikgia caerulea group (Ra- pollinated species and hawkmoth-pollinated species. nunculaceae) in western North America contain species with ornithophilous flowers and related species with sphlngophllous flowers. The ornithophilous and sphingophilous species are MATERIALS sympatric over large areas and remain distinct in some sites The two species groups with which we are concerned are the where they grow dose together. Floral tin combina- Ipomopsis aggregata group (Polemoniaceae) and Aquilegia tion ofmechanical and ethological Isoation-plays a significant formosa-Aquilegia caerulea group (Ranunculaceae). Both role in the reproductive Isolation. The primary pollinators of groups occur in mountainous regions ofwestern North Amer- the ornithophilous taxa are the common western American ica. They have been extensively studied by various botanists, species of hummingbirds, and the primary plinators of the including myself, from the standpoint of systematics, ecol- sphingophilous taxa are western hawkmoths. The ornithophil- ogy, and pollination. ous and sphingophilous flowers are adapted to their re ve The plants are outcrossing diploid perennials with showy primary pollinators. A corollary of these sec ons is that flowers. Most of the taxa in each group have either ornitho- the differences between the two types of floral mechanisms philous or sphingophilous flowers. The I. aggregata group significantly reduce interspecific naon. The floral isola- has six ornithophilous and four sphingophilous taxa (3, 4); the tion is incomplete. However, Itacts not alone but in conjunction A. formosa-A. caerulea group has seven ornithophilous and with ecological and seasonal isolation, which are also incom- seven sphingophilous taxa (5, 6). plete. The combination of these three incomplete external Most of the ornithophilous taxa in the I. aggregata group Isolating mehanism Is sufficient to maintain the di and all of those in the A. formosa-A. caerulea group have of the ornithophilous and sphngphilous spece in some areas allopatric distribution areas. The sphingophilous taxa in each of sympatric coexistence. group are also allopatric. The allopatric taxa with a given pollination system are essentially geographical races belong- ing to the same species, and they are treated taxonomically Floral isolation is external reproductive isolation at the stage as such in Ipomopsis (3) but not in Aquilegia (7). On the other of pollination in angiosperms. It has two components: me- hand, the ornithophilous species and the sphingophilous chanical and ethological isolation. Mechanical isolation oc- species are broadly sympatric in both Ipomopsis and Aqui- curs when two (or more) plant species have different flower legia. The species with contrasting pollination systems re- structures that reduce or prevent interspecific cross- main reproductively isolated in some sympatric localities but pollination. The flowers of two species may be adapted for hybridize in other localities. the same pollinator but deposit pollen on different parts ofthe Internal sterility barriers are known to be weak in the I. pollinator's body. Or the contrasting species may have flow- aggregata group (8) and in the genus Aquilegia (9-11). ers adapted for different types of pollinating animals with Reproductive isolation between sympatric species is there- different body forms. We are concerned with the latter type fore determined mainly by external barriers. of mechanical isolation in this paper. We are concerned primarily with certain taxa in the two Ethological isolation frequently develops as a side effect of groups-namely, I. aggregata formosissima (ornithophil- mechanical isolation involving different classes of pollina- ous), Ipomopsis tenuituba (sphingophilous), A. formosa tors. The structural differences that promote mechanical truncata (ornithophilous), Aquilegia pubescens (sphingophil- isolation often make the floral reward of one species more or ous), and Aquilegia chrysantha (sphingophilous). Further- less inaccessible to the normal pollinator ofthe other species. more, we are concerned only with the nonintrogressive forms The pollinators recognize these structural differences and of these taxa. However, the evidence is applicable and the adjust their behavior so as to ignore the "wrong" species conclusions can be extended to some other parts of the two during foraging. Ethological isolation then accompanies and species groups. reinforces the mechanical isolation. Because mechanical and ethological isolation are often combined in actual cases, and because the two components RESULTS cannot always be readily distinguished, it is convenient to Ecological Ioaction. The sphingophilous taxa ofAquilegia refer to them collectively as floral isolation. Examples of and of Ipomopsis (with one exception) occur in a higher floral isolation have been reported in a number of plant elevational zone than do the ornithophilous taxa. The two groups (1, 2), but additional examples are needed. Two classes of taxa live in different but contiguous plant commu- cases-one not previously explored (in Ipomopsis) and the nities. Thus in the Sierra Nevada, ornithophilous A.formosa other revisited (Aquilegia)-are described in this paper. truncata grows along streams, and sphingophilous A. pubescens grows in dry rocky places above the wooded streams. The publication costs of this article were defrayed in part by page charge The two species occur within normal pollen dispersal range payment. This article must therefore be hereby marked "advertisement" of one another without hybridizing in a number of known in accordance with 18 U.S.C. §1734 solely to indicate this fact. sites (ref. 12; unpublished data). Ornithophilous I. aggregata 11828 Downloaded by guest on September 24, 2021 Ecology: Grant Proc. Nadl. Acad. Sci. USA 89 (1992) 11829 and sphingophilous I. tenuituba have a parallel relationship in the Kaibab Plateau, Arizona, where the former occurs in montane forest and the latter in the neighboring subalpine zone (3, 8). Ornithophilous I. aggregata collina and sphingophilous I. aggregata candida occur in neighboring wood- land and grassland habitats without hybridizing in various sites in Colorado (13). In these and other cases ecological isolation plays a leading role in the isolation of the ornithophilous and sphingophilous species (8, 12-16). Since the sphingophilous taxa usually occur at higher elevations than their ornithophilous relatives, the former come into flower later. The flowering seasons of the two A B classes of taxa have different peaks but overlapping ranges. Some seasonal isolation thus exists, but it is incomplete (8, 12, 14). Contrasting Pollination Systems. The primary pollinators of 1cm the ornithophilous taxa of the I. aggregata and A. for- FIG. 1. Flowers of the l. aggregata group. (A) I. aggregata mosa-A. caerulea groups are the hummingbird species with formosissima, ornithophilous. (B) L. tenuituba latiloba, sphingophil- wide breeding ranges in western North America. Selasphorus ous. Circles indicate positions of included anthers; arrow indicates rufus, Stellula calliope, and unidentified hummingbirds have highest anther. been recorded on I. aggregataformosissima at four sites in the Sierra Nevada, California, and Selasphorus rufus and In the sphingophilous taxa, by contrast, the floral tube is Selasphorus platycercus at three sites in northern Arizona very long and slender. The floral tube in I. tenuituba is 30-46 (refs. 17 and 18; unpublished data). Selasphorus rufus and mm long (Fig. 1B); that in nonintrogressive A. pubescens is Selasphorus platycercus are also common visitors and pol- 28-39 mm long (Fig. 2B); and that in A. chrysantha is 39-69 linators of the related I. aggregata aggregata and I. aggre- mm long (Fig. 2C) (25). These floral tubes are well fitted for gata collina in Colorado (17, 19-21). Selasphorus rufus, the long slender probosces ofwestern American hawkmoths. Stellula calliope, Calypte anna, and unidentified humming- The mean length ofthe proboscis in H. lineata is 38 mm; that birds have been recorded on A. formosa truncata at seven of Eumorpha achemon is 43-50 mm; and the mean length sites in central and northern California (12, 14, 15, 22). In ranges from 44 to 69 mm in different species of Sphinx (26). Colorado the related Aquilegia elegantula is pollinated by Probosces are even longer in Manduca (26). Selasphorus platycercus (16, 20). It is fair to conclude that the ornithophilous flowers of The ornithophilous taxa of Ipomopsis and Aquilegia ex- Ipomopsis and Aquilegia and widespread western humming- hibit a suite of floral and inflorescence characters that cor- birds form a coadapted system (5, 25). Similarly, the sphin- respond to the foraging habits of their hummingbird visitors. gophilous flowers of these plant groups and western hawk- Such characters include flower color, orientation of flowers moths form another coadapted system (6, 17). in the inflorescence, daytime nectar production, length and Effects of Differences Between the Ornithophilous

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