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Historical Development of Ornithophily in the Western North American Flora

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Historical Development of Ornithophily in the Western North American Flora Proc. Nati. Acad. Sci. USA Vol. 91, pp. 10407-10411, October 1994 Evolution Historical development of ornithophily in the western North American flora (hummingbird po an system/evolution of mut /Arcto-Terlary floistic eemets/Madro-Tertlary flowisc eements) VERNE GRANT Department of Botany, University of Texas, Austin, TX 78713 Contributed by Verne Grant, July 18, 1994 ABSTRACT The 129 ornithophilous plant species in west- MATERIALS AND METHODS ern North America have floristic afites with one or the other of four geofloras: the Arcto-Tertiary flora (101 species), Western North America is defined for this study as the area Madro-Tertary flora (19 species), Madrean-Tethyan flora (8 from the Rocky Mountains to the Pacific coast, and from the species), and Neotropical flora (1 species). The last three floras Mexicanborderto southwestern Canadaand southern Alaska. have been in continuous contact with hmngblrds ince some The ornithophilous plant species in this area are listed in time early in the Tertiary, and ornithophily is old in this subset Table 1. The list includes 129 species in 39 genera and 18 of western ornithophilous plants. The Arcto-Tertiary flora had families. Hummingbird pollination records are available for no contact with hummingbirds in Eurasia or in its early history 43 of the species; the other species have inflorescence and in North America. Ornithophily is a new condition in Arcto- floral characters similar to those in the 43 documented Tertiary plant groups, dating from the firstdgncant contact species (1, 2). Some ornithophilous species may exist in of these plants with hummingbirds in the Eocene. Buidu of nature but be undetected and omitted from the list; ifso, their the hummingbird polination system in the Arcto-Tertary flora number would be small, and the listed species provide a good is expected to be gradual and stepwise for several reasons. sample for the purpose of this study. Ornithophilous plant groups with Arcto-Tertary aits in Taxonomic disagreement exists concerning the rank of the modern western flora form a graded series with respect to four small genera in Table 1. Some taxonomists treat Dipla- taxonomic rank, taxonomic size, and ecological divert. The cus, Keckiella, and Zauschneria as subgenera ofother larger series consists ofone large genus (Castllja), three small genera genera (Mimulus, Penstemon, and Epilobium, respectively), (Zauschneria, etc.), species groups in several genera (Penste- while other students, myself included, see them as good mon, Aquieia, etc.), single ornithophilous species in otherwise minor genera. Diplacus, Keckiella, andZauschneria all differ nonornithophilous genera (seven genera-e.g., Pediculris, significantly from their related genera in floral and vegetative Monardela), and ornithophilous races in otherwise nonorni- characters and, in one case, in basic chromosome number; thophilous species (known in two species). It I suggested tat they represent distinct branch lines; and they have all moved the in size reflect sages into a new adaptive zone, hummingbird pollination. The gradations ofthe groups approximately fourth small genus, Galvezia, is construed broadly here to in their development, with the largest ornithophilous genus include the related Gambelia. being oldest, with single ornlthophilous species being reativey A genus problem exists also in Castilleja. Castilleja is close recent, and with ornithophilous races being most recent. The to Orthocarpus and the character differences separating the observed distribution of numbers of ornithophilous species two groups break down in some species. Pennell (7) recog- among genera is in agreement with the expectation ofa gradual nized the problem but maintained the two taxa as separate and stepwise development of ornithophily. genera. Chuang and Heckard (8) have recently reorganized Orthocarpus and transferred a block of Orthocarpus species Hummingbirds and hummingbird flowers form a flourishing to Castilleja. I follow the genus concept of Pennell for mutualistic association in western North America. This as- Castilleja; consequently, this taxon as discussed in this paper sociation is composed of about 129 plant species, with is equivalent to Castilleja subgenus Castilleja ofChuang and flowers adapted for foraging and pollination by humming- Heckard (8). birds, and 11 species ofhummingbirds (1-3). The mutualistic The option of basing a history of ornithophily directly on dependence ofthe birds and plants is not absolute. Individual fossil evidence is not available because of the lack of an birds can and do sustain themselves for a time on bee flowers, adequate fossil record of both hummingbirds and ornitho- insects, and stored food reserves, and some ornithophilous philous plants. No fossil records of hummingbirds are listed plants can accomplish pollination and seed set with the aid of for North America in standard compendia (9, 10). Most bees or other insects or by selfing. Nevertheless, the mutual ornithophilous plants in western North America are herba- dependence is strong, as indicated by the fact that breeding ceous and would be poorly preserved. However, the history and nesting hummingbirds generally occur near populations ofwestern North American floras is well known and is based ofornithophilous plants, while plant taxa with ornithophilous on the fossil records of the dominant woody species. Fur- floral characters are absent in regions such as the Great Plains thermore, we know the floristic affinities of western North of Nebraska, Wyoming, and Montana, which are outside the American ornithophilous plants. One approach to the prob- distribution range of hummingbirds. lem used here is to infer the history ofwestern ornithophilous How does a mutualistic association such as that involving plants from the known history of their plant communities. western North American hummingbirds and ornithophilous A second approach is to use the taxonomic rank ofnatural plants develop? This question can be approached from several groups ofornithophilous plant groups as an indicator oftheir standpoints. The approach adopted here is a historical one. relative ages. Supplementary criteria are the relative taxo- nomic size and ecological diversity of the groups. These The publication costs ofthis article were defrayed in part by page charge criteria have to be used with discrimination and controls. A payment. This article must therefore be hereby marked "advertisement" relict species can be older than a larger indigenous species in accordance with 18 U.S.C. §1734 solely to indicate this fact. group. This source of error is avoided by restricting the rank 10407 Downloaded by guest on September 29, 2021 10408 Evolution: Grant Proc. Natl. Acad. Sci. USA 91 (1994) Table 1. Native ornithophilous species in the western North American flora Family, genus, and species Family, genus, and species Nyctaginaceae Scrophulariaceae Allionia coccinea Castilleja: affinis, angustifolia, applegatei, austromontana, brevilobata, Caryophyllaceae breweri, chromosa, covilleana, crista-galli, cruenta, culbertsonii, Silene: californica, laciniata elmeri, exilis, foliolosa, franciscana, fraterna, haydeni, hispida, Ranunculaceae hololeuca, inconstans, integra, lanata, latifolia, laxa, lemmonii, Aquilegia: desertorum, elegantula, eximia, leschkeana, linariaefolia, martinii, miniata, minor, nana, neglecta, flavescens, formosa, shockleyi, triternata organorum, parviflora, patriotica, payneae, peirsonii, plagiotoma, Delphinium: cardinale, nudicaule pruinosa, rhexifolia, roseana, rupicola, stenantha, suksdorfti, Saxifragaceae subinclusa, uliginosa, wightii, wooteni Ribes speciosum Diplacus: aurantiacus, longiflorus, parviflorus, puniceus Leguminosae: Papilionoideae Galvezia speciosa Astragalus coccineus Keckiella: cordifolia, corymbosa, ternata Erythrina flabelliformis Mimulus: cardinalis, eastwoodiae Cactaceae Pedicularis densiflora Echinocereus triglochidiatus Penstemon: barbatus, bridgesii, cardinalis, centranthjfolius, clevelandii, Fouquieriaceae crassulus, eatonii, labrosus, lanceolatus, newberryi, parryi, Fouquieria splendens pinifolius, rupicola, subulatus, utahensis Convolvulaceae Scrophularia coccinea Ipomoea coccinea (including I. hederifolia) Acanthaceae Polemoniaceae Anisacanthus thurberi Collomia rawsoniana Beloperone californica Gilia subnuda Jacobinia ovata Ipomopsis: aggregata, arizonica, Rubiaceae sancti-spiritus, tenuifolia Bouvardia glaberrima Polemonium: pauciflorum, brandegei Caprifoliaceae Boraginaceae Lonicera: arizonica, ciliosa Macromeria viridiflora Campanulaceae Labiatae Lobelia: cardinalis, laxiflora Monarda fistulosa Onagraceae Monardella macrantha Zauschneria: calfornica, cana, garrettii, septentrionalis Satureja mimuloides Liliaceae Salvia: henryi, lemmoni, spathacea Fritillaria recurva Stachys: chamissonis, ciliata, coccinea Lilium: maritimum, parvum Trichostema lanatum Brodiaea: ida-maia, venusta Data are based on refs. 1, 2, and 4-6. and size comparisons to nonrelictual ornithophilous groups Contacts between the Arcto-Tertiary and Madro-Tertiary belonging to the same historic flora. floras resulted in numerous exchanges of floristic elements. For reconstructing phylogenetic relationships, I use the Nevertheless, Arcto-Tertiary elements predominate today in traditional method in which one draws inferences from com- the central and northern parts ofwestern North America and parative morphology, biogeography, and ecology. I use this decline in abundance to the south, while Madro-Tertiary method in preference to the currently
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