Flora of North America species comparison

Species 8 (7 in the flora).

Subgeneric rank for Longifoliae is based on molecular, anatomical, developmental, chemical, genetic, and morphological evidence. In a molecular study using ribosomal DNA, E. Leskinen and C. Alström-Rapaport (1999) found that Salix interior (as S. exigua) fell well outside all other Salix species included in their study and suggested that it may have diverged early. A study based on chloroplast-encoded rbcL gene (T. Azuma et al. 2000) did not strongly support the uniqueness of S. interior other than to group it with subg. Protitea rather than with subg. Vetrix and to suggest that its two-stamened condition was independently derived. A cladistic and genetic distance study based on isozyme data (D. K. X. Chong et al. 1995) showed that S. interior (as S. exigua) was about equally divergent from both subg. Protitea (as subg. Salix) and subg. Vetrix. An anatomical study by A. K. Skvortsov and M. D. Golysheva (1966) showed that the completely isolateral leaves of S. interior and S. microphylla, with a bilateral, chlorophyll-deficient, one-layer hypodermis, resemble leaves in subg. Chosenia (as S. chosenia) and Populus subg. Turanga. Also, the leaf epidermis of the former, which consists of unequal-sized cells, resembles that of some Populus and Salix sects. Humboldtianae and Triandrae. W. Büchler (1996) reported that proximal leaves of S. exigua and S. interior both have an opposite decussate phyllotaxis, indicating that they are out of place in subg. Salix and confirming their morphologically isolated position within Salicaceae. Cyanogenesis, not positively documented for any other Salix, was found to occur in living and herbarium material of S. interior from central United States (A. M. Brinker et al. 1987). Pollen-stigma incongruity data (A. Mosseler 1989) showed that S. interior is more compatible with members of subg. Vetrix than with those of subgenera Protitea and Salix. Mosseler (1990) also found that interspecific hybrids between S. interior (as S. exigua) and species of subg. Vetrix were more viable.

Distinctive morphological characteristics of Longifoliae include the presence of root shoots, known in Salicaceae only in some species of Populus and in Salix setchelliana (subg. Chamaetia), branched catkins, in which the proximal two floral bracts, or the leaves on flowering branchlets, subtend secondary catkins (G. W. Argus 1997; A. K. Skvortsov 1999), the frequent production of sylleptic shoots, and the occasional occurrence of tricarpellate ovaries in S. exigua. Secondary buds flanking the axillary buds, which appear in some S. exigua and S. thurberi, may have possible taxonomic significance.

Subgenus Longifoliae originated in the New World, probably in riparian habitats in the semiarid regions of Mexico or Central America (S. J. Brunsfeld et al. 1992). Its xeromorphic leaf morphology is highly adaptive in that region (A. K. Skvortsov 1999). Species in Central Asia with similar xeromorphic leaf morphology, such as Salix linearifolia Wolf of sect. Helix, are cases of convergence.

The species of subg. Longifoliae are taxonomically difficult; they seem to form a syngameon of poorly resolved semispecies (V. Grant 1981; S. J. Brunsfeld et al. 1991). These taxa are not only highly variable, but they produce clones through root shoots (rhizoblasts), hybridize and introgress freely, and often produce sylleptic vegetative and reproductive shoots. Sylleptic shoots, arising from buds without a dormant period, can differ morphologically from the primary shoots, which arise from the previous year’s buds. In Salix, leaves on sylleptic branchlets usually are more densely hairy and more prominently toothed than those of the proleptic primary branchlets. Catkins of subg. Longifoliae, described in the literature as borne on relatively long, flowering branchlets, often are sylleptic shoots terminated by a catkin, and the branchlet length given may include the primary branchlets on which these secondary branchlets are borne. Sometimes syllepsis occurs after defoliation by insects, but usually it occurs without the loss of primary leaves. The factors that stimulate syllepsis in subg. Longifoliae are unknown, but it is common in Populus, where it has been shown to increase light capture and carbon production (R. Ceulemans et al. 1990). Because syllepsis is common and may have an influence on leaf morphology, taxonomists must be careful not to confuse proleptic and sylleptic shoots.

A study of genetic variation by S. J. Brunsfeld et al. (1991) revealed four major elements within subg. Longifoliae in North America: 1) Salix interior, 2) S. taxifolia, 3) the S. exigua group, and 4) S. melanopsis. Within the S. exigua group, they recognized four major geographic entities: S. hindsiana (treated here as S. exigua var. hindsiana), S. sessilifolia, and a northern and a southern race in the Intermountain West. The two races were not named but they include S. exigua and possibly S. thurberi. Brunsfeld et al. also noted that S. columbiana (as S. fluviatilis) may be of hybrid origin. All of these taxa are recognized here, although the ranks do not always correspond to those proposed. A second study by Brunsfeld et al. (1992) revealed incongruencies between molecular genetic and morphological data, as well as evidence of long-distance gene transfer.

Taxonomic problems in subg. Longifoliae, including the practical problem of specimen identification, cannot be solved by field study and herbarium specimens alone. This group requires an interdisciplinary approach including molecular genetics, cytology, and common garden studies where synthetic hybridization and morphological observations of the same plants can be made in all stages of development.

Excluded species:

Salix microphylla Schlechtendal & Chamisso occurs only in Mexico and Guatemala. (See 17. S. taxifolia for comments on its nomenclature.) It is characterized by: shrubs or trees, 0.8–6 m; stipules on late leaves foliaceous; largest medial blade amphistomatous, lorate, narrowly oblong, or narrowly oblanceolate, 5.6–24 × 1.2–3.8 mm, 2.1–13.3 times as long as wide, margins entire or serrulate; staminate abaxial nectary absent; stipes 0.2–1.2 mm; ovary pyriform, long-silky; ovules 21–43 per ovary; style 0.2–0.3 mm; stigmas persistent, slenderly cylindrical lobes, 0.6–0.75–0.92 mm; capsules 4–7 mm (Mexico, Central America [Guatemala]).

(Discussion copyrighted by Flora of North America; reprinted with permission.)

Genera 50+, species ca. 1000 (4 genera, 123 species in the flora).

Taxonomic placement of the Salicaceae and the genera included in it have varied greatly. Some botanists (H. G. A. Engler and K. Prantl 1887–1915) treated it as a primitive member of the Dicotyledoneae and grouped it with other families having simple, apetalous, unisexual flowers arranged in catkins, the “Amentiferae.” At about the same time, others (C. E. Bessey 1915) took a different view, regarding the simple flowers as the result of reduction, and placed the taxa in Caryophyllales. As early as 1905, H. Hallier could see that there were similarities between Salicaceae and Flacourtiaceae; at the time, he was vigorously challenged by E. Gilg (1915). A. D. J. Meeuse (1975) summarized evidence for a close relationship between these families, including wood anatomy, phytochemistry, host-parasite relationships (including rust fungi), and morphology. He concluded that the Salicaceae could be combined with the Flacourtiaceae, “perhaps as a tribe.” A. Cronquist (1988) and R. F. Thorne (1992b) placed the Salicaceae, in a narrow sense, in Violales near Flacourtiaceae.

Molecular studies support a close relationship between Salicaceae and Flacourtiaceae in Malpighiales and show that Flacourtiaceae, in a broad sense, is paraphyletic. Based on a study of plastid rbcL DNA sequences, Salix and Populus were nested within a subset of 52 genera of Flacourtiaceae (M. W. Chase et al. 2002). Chase et al. proposed moving some genera from broadly circumscribed Flacourtiaceae to Salicaceae. Other studies, based on different gene sequences, came to the same conclusion (O. I. Nandi et al. 1998; V. Savolainen et al. 2000; K. W. Hilu et al. 2003; Angiosperm Phylogeny Group 2003). The discovery of the extinct fossil genus Pseudosalix (L. D. Boucher et al. 2003), from the Eocene Green River Formation of Utah, provided further support for placing some members of Flacourtiaceae in Salicaceae. The well-preserved Pseudosalix fossils, in which reproductive structures are directly associated with the leaves, occur intermixed with Populus fossils. The leaves are slender and have salicoid teeth, inflorescences are cymose, flowers are unisexual, pedicellate, tetrasepalous, and 3- or 4-carpellate, and seeds are comose, i.e., having characteristics intermediate between Salicaceae and Flacourtiaceae.

The presence, in both families, of salicoid teeth is often cited in support of their close relationship (W. S. Judd 1997b; O. Nandi et al. 1998; M. W. Chase et al. 2002; H. P. Wilkinson 2007). Salicoid teeth were first recognized and defined as having the tip of the medial vein (seta) of the tooth retained as a dark, but not opaque, non-deciduous spherical callosity fused to the tooth apex and were reported to occur in Salicaceae and Idesia of the Flacourtiaceae (L. J. Hickey and J. A. Wolfe 1975). Nandi et al. reported that a broad survey of angiosperm leaves showed that salicoid teeth occur outside of Flacourtiaceae and Salicaceae only in Tetracentraceae.

Isozyme and cytological evidence show that Populus and Salix are ancient polyploids (D. E. Soltis and P. S. Soltis 1990; Wang R. and Wang J. 1991). All Salix and Populus species contain salicin (R. T. Palo 1984).

The genera often included in Salicaceae, in the narrow sense, are Chosenia, Populus, Salix (A. K. Skvortsov 1999), and, sometimes, Toisusu. Molecular studies (E. Leskinen and C. Alström-Rapaport 1999; T. Azuma et al. 2000) show that Chosenia is nested within Salix. H. Ohashi (2001) treated Toisusu as Salix subg. Pleuradinea Kimura and Chosenia as Salix subg. Chosenia (Nakai) H. Ohashi.

(Discussion copyrighted by Flora of North America; reprinted with permission.)