Phylogeny, morphology, and biogeography of Chuquiraga, an Andean-Patagonian genus of Asteraceae-Barnadesioideae.
Elevated regions of the Andes and associated mountain ranges along western South America support a unique and highly diverse flora with several endemic or nearly endemic genera. The origin of this flora is complex. It has been suggested that during the Tertiary a continual sifting of taxa from lower to higher elevations occurred all along the emergent cordillera, and that throughout this period there were also migrations of austral taxa from southern South America to the north, and of northern taxa to the south (Baumann, 1988; Simpson & Todzia, 1990; Hooghiemstra & Cleef, 1995). The evolutionary history of selected genera with centers of diversity in different regions of the Andes can contribute to the understanding of the complex characteristics of the assemblage of the Andean flora.
The genus Chuquiraga Juss. is one of the largest genera of Barnadesioideae, a basal lineage of Asteraceae that is endemic to South America (Bremer & Jansen, 1992; DeVore & Stuessy, 1995; Stuessy et al., 1996; Urtubey & Stuessy, 2001). Chuquiraga consists of 23 species of evergreen shrubs distributed principally along the Andes, from more than 4000 m in Colombia to sea level in central Chile and southern Argentina (Ezcurra, 1985; Harling, 1991; Sagastegui A. & Sanchez V., 1991; Ferreyra, 1995; Granda P., 1997). Although the genus is generally considered xeromorphic, its geographical distribution is greater than the arid diagonal distribution of deserts and semideserts in South America (Fig. IB), characterized by mean annual rainfall of less than 500 mm (Espenshade, 1978), and its area generally matches temperate regions of this continent with a mean annual temperature of less than 15[degrees]C (Hoffmann, 1975) (Fig. 1A).
Chuquiraga shows variation in size and color of heads and flowers, from large and reddish orange to small and yellow, and pollination by hummingbirds or insects has been reported for various species (Carpenter, 1976; Ezcurra, 1985; Ezeurra & Crisci, 1987; Fjeldas & Krabbe, 1990). The genus is also remarkable because of the wide diversity of its leaf morphology compared with that of other large genera of the subfamily, such as Dasyphyllum and Barnadesia. It has often been suggested that differences in leaf types within the genus are related to adaptations to different habitats (Espinosa, 1933; Bocher, 1979; Ezcurra, 1985; Ezcurra et al., 1997).
The four primary morphoanatomical leaf types of the genus are: flat and hipostomatous; flat and amphistomatous; boat shaped, inverse dorsiventral, and epistomatous; and acicular-involute and subcentric, with stomata confined to the bottom of a hairy, narrow groove in the adaxial side (i.e., "inverted ericoid," as defined by Bocher ) (Fig. 2; see also Ezcurra, 1985). The latter two leaf types are also characterized by a continuous plate of subepidermal schlerenchyma in the abaxial side of the blade, a rare anatomical feature in dicotyledons (Bocher, 1979). Species with those leaf types are especially important elements in the most extreme deserts and semideserts of southern South America, from the dry puna of southern Bolivia and northern Chile and Argentina to the temperate semidesert of Patagonia (Fig. 1B).
The objective of this study is to provide a hypothesis of phylogenetic relationships among species of Chuquiraga in order to test a previous classification (Ezcurra, 1985). The resulting cladogram is also used to interpret morphological, ecological, and biogeographical patterns of the species in a historical context, and to discuss how certain biotic and abiotic environmental characteristics may have affected the evolution of the genus by exerting selective pressure.
III. Materials and Methods
A. CHOICE OF TAXA
All 23 known species of Chuquiraga were included in the analysis. Chuquiraga rotundifolia was treated as a species; C. spinosa subsp. huamanpinta and C. spinosa subsp. australis were treated as subspecies of C. rotundifolia. Dasyphyllum diacanthoides and Schlechtendalia luzulaefolia were considered as outgroups; Doniophyton weddellii and Duseniella patagonica were treated with Chuquiraga species as part of the ingroup (Stuessy et al., 1996).
The choice of outgroups was based on the suggestion that Dasyphyllumn and the monotypic Schlechtendalia appear to be basal in the evolution of Barnadesioideae (DeVore & Stuessy 1995; Stuessy et al., 1996). The basal position of Schlechtendalia was recently confirmed in a morphological cladistic analysis of the Barnadesioideae conducted at the specific level that includes nearly 60% of the species of the group (Urtubey & Stuessy, 2001).
Arnaldoa has been described as intermediate between Dasyphyllum and Chuquiraga (Cabrera, 1977), closely related to Chuquiraga (Ezcurra, 1985), and perhaps also basal in the phylogeny of the group (Stuessy et al., 1996). It was not considered an outgroup in this work because of the suggestion that it may have originated via intergeneric hybridization between Chuquiraga and Barnadesia in the Northern Andes in relatively recent times (Stuessy et al., 1996).
On the other hand, within Dasyphyllum, subgen: Archidasyphyllum with two species from south-central Chile, has generally been considered as more primitive than subgen. Dasyphyllum, with 34 species from tropical South America (Cabrera, 1959; Stuessy et al., 1996; but see Urtubey & Stuessy, 2001). Dasyphyllum diacanthoides, the southernmost and least xeromorphic species of nearly monotypic Archidasyphyllum, is probably a relict, like several other species of monotypic or nearly monotypic genera of the temperate forests of southern South America (Arroyo et al., 1996; Stuessy et al., 1996). To reduce infrageneric variation, it was the only species of Dasyphyllum used as outgroup in this study, considering its southernmost distribution, tree life-form, and lack of leaf xeromorphy as primitive characters.
The treatment of Doniophyton and Duseniella as ingroup also follows the phylogenetic relationships within Bamadesioideae genera suggested by Stuessy et al. (1996), quite different from Bremer's earlier scheme (1994), based on a different choice of characters and outgroup. One of the two species of Doniophyton and the only species of Duseniella were used in the analyses.
B. CLADISTIC ANALYSIS
Phylogenetic reconstruction was based on 31 morphological characters (from descriptions in Ezcurra, 1985; Harling, 1991; Sagastegui A. & Sanchez V., 1991; Ferreyra, 1995; Granda P., 1997) derived from 17 vegetative and 14 reproductive attributes of the species, of which 26 are qualitative and 5 quantitative. Quantitative characters were simple gap coded (see Thiele, 1994, for coding and use of quantitative characters in cladistics) (Appendix 1, 1-31). Character polarity was assessed by outgroup comparison (e.g., Maddison et al., 1984). Discrete multistate character 12 (leaf shape in cross-section) was treated as additive, because a direct transformation series was hypothesized for it following the semophyletic evolutionary sequence suggested by Bocher (1979) from planate leaf blade, to boat shaped, to acicular by marked involution.
To select the best characters for cladistic analysis, the resulting data matrix (Appendix 2, characters 1-31, no missing data) was analyzed using the computerized parsimony program Hennig86, using the search options mh* and bb*, a heuristic method for finding minimum-length trees that retains all the shortest trees, and a strict consensus tree was obtained by applying the NELSEN command of Hennig86 (Farris, 1988). The consistency (CI) and retention indices (RI) of each of the characters on the consensus tree were estimated with the XSTEPS command. Characters with the lowest CI and RI indices (characters 1, 5, 9, 15, 16, 17, 18, 19, 24, and 31; i.e., autapomorhies and highly homoplasic characters) were eliminated, and a second matrix with a total of 21 characters was used to produce the final analyses.
Both data matrices were then analyzed using PAUP vers. 3.1.1 (Swofford, 1991), using heuristic searches with tree bisection reconnection (TBR) and MULPARS options. The bootstrap method (Felsenstein, 1985) was employed to evaluate the reliability of phylogenetic estimates. Bootstrap was conducted using PAUP with the options polytomies collapsed and MULPARS. One hundred replicates were performed using one random taxon entry sequence per replicate, and TBR branch swapping, with 10 trees saved per replicate and initial MAXTREES number set to 100. Morphological character changes were traced on the phylogeny using MacClade vers. 3.0 (Maddison & Maddison, 1992).
C. PHLYLOGENETIC BIOGEOGRAPHY
To reconstruct the probable biogeographical history of this Andean Patagonian genus, which has centers of diversity in the high tropical Andes and in arid and semiarid regions of southern South America, presence or absence of each of its species in the Southern, Central, and Northern Andes regions was established. Limits of these Andean units follows Reig (1986), based on the Andean regions described by Simpson (1975) (Fig. 1A). Distributional information for each taxon was taken from dot maps in Ezcurra (1985) and from later literature.
Environmental factors that have been hypothesized to be important in the evolution of the genus are temperature and aridity, herbivory by mammalian grazers, and different types of pollinators (Ezcurra & Crisci, 1987; Ezcurra et al., 1997). It has been suggested that higher temperatures and increased aridity have exerted selective pressure on leaf morphology, resulting in the evolution of narrow, involute, acicular leaves from ancestors with wider leaves (Ezcurra et al., 1997). Together with increased aridity, the effect of herbivory of vertebrates that dispersed into South America at the end of the Tertiary, such as camelids, currently represented by guanaco (Lama guanicoe) and vicuna (Vicugna vicugna), has also been related to the evolution of this type of acicular, prickly leaf (Ezcurra et al., 1997). Based on observations and on differences in floral morphology, different pollinators--i.e., hummingbirds and insects--have been associated with the presence of the two types of flowers and flower heads present in the genus (Carpenter, 1976; Ezcurra & Crisci, 1987; Fjeldsa & Krabbe, 1990).
To explore the historic influence of these factors on the evolution of morphological traits in the genus, current relationships were inferred by mapping the geographical range of each Chuquiraga species and superimposing it onto the distribution of hillstar hummingbirds (Oreotrochilus spp.) (Carpenter, 1976; Fjeldsa & Krabbe, 1990) (Fig. 3A), principal bird pollinators of Chuquiraga species (Carpenter, pers. comm.; Fjeldsa, pers. comm.), onto the distribution of guanaco (Lama guanicoe) (Franklin, 1982) (Fig. 3B), reported as grazers of Chuquiraga species (Pelliza-Sbriller et al., 1995; Somlo, 1997), and onto the range of high summer temperatures (higher than 20[degrees]C mean January temperature) in South America (Hoffmann, 1975) (regions outside areas marked in black in Fig. 3C), which, in combination with aridity, produce the most extreme deserts of southern South America (Cabrera & Willink, 1980) (Fig. 1B). A presence/absence data matrix of the relationships of each taxon with these environmental factors w as constructed (Appendix 2, characters I-IV).
The ecological and biogeographical characteristics of the species inferred to be associated with these factors--i.e., pollination by hummingbirds, high summer temperature resistance, herbivory resistance, and presence in the Central and Northern Andes (Appendix 2, characters I-IV)--were superimposed onto the phylogeny and optimized using MacClade vers. 3.0 (Maddison & Maddison, 1992) to produce hypotheses of relationships between morphological changes and the selective pressure of environmental factors in a historical context (Brooks & McLennan, 1991). In order to avoid circularity in tests of evolutionary hypotheses, the phylogenetic tree should never be constructed using the ecological or biogeographical information under study (e.g., Brooks & McLennan, 1991). Therefore, the biogeographical and ecological evolutionary relations of the present analyses were analyzed using a cladogram based on overall morphological data (Appendix 1: 1-31).
A. CLADISTIC ANALYSIS
Parsimony analysis of the complete data set yielded 108 most parsimonious trees, each with 73 steps and having a consistency index (CI) of 0.44 and a retention index (RI) of 0.76 (Farris, 1989), which were summarized in a strict consensus tree (Fig. 4). Analysis of the reduced data set (without characters 1, 5, 9, 15, 16, 17, 18, 19, 24, and 31) yielded a single most parsimonious tree (L 37; CI = 0.60; RI = 0.89). The single tree showing bootstrap replication frequencies is presented in Fig. 5. Both analyses produced trees with similar topologies in which two clades, one originating in a relatively more basal position (CAL-LON, including Chuquiraga calchaquina, C. weberaueri, C. rairnondiana, C. spinosa, C. arcuata, C. rotundifolia, C. jussieui. C. oblongifolia, and C. longiflora) and the other terminal (RUS-ERI, including C. ruscifolia, C. echegarayi, C. atacamensis, C. kuschelii, C. acanthophylla, C. rosulata, C. aurea, C. ulicina, and C. erinacea), show nearly identical relationships among species. Therefo re, the single tree from the reduced database was used to analyze character change on the phylogeny and to explore ecological and biogeographical hypotheses.
These two clades have relatively high support bootstrap values (87% and 98%) and coincide with two infrageneric groups recognized by Ezcurra (1985); that is, Chuquiraga sect. Chuquiraga ser. Chuquiraga and Chuquiraga sect. Acanthophyllae, suggesting monophylly for both of these infrageneric taxa. The origin of the ser. Chuquiraga dade (CAL-LON) appears to be associated with changes in size of the head, anthers, and flowers (characters 21, 23, and 26), whereas the origin of the sect. Acanthophyllae dade is associated with changes in leaf morphology (characters 8, 10, and 12-15) (Fig. 5).
The other infrageneric taxon recognized (Ezcurra, 1985), Chuquiraga sect. Chuquiraga ser. Parviflora (C. parviflora, C. oppositifolia, C. morenonis, C. avellanedae, C. straminea), resulted paraphyletic in the analyses, and Duseniella and Doniophyton also appeared internested among these species. The future taxonomic disposition of all these taxa needs further investigation.
B. PHYLOGENETIC BIOGEOGRAPHY AND EFFECT OF BIOTIC AND ABIOTIC ENVIRONMENTAL FACTORS ON THE EVOLUTION OF THE GENUS
Optimization of current latitudinal distribution of the species (Appendix 1, factor I) onto the phylogeny suggests an austral origin for the group in relation to the relatively southern distribution of the outgroup and the basal species C. parviflora. The cladogram shows two major evolutionary radiations, one principally in the Central and Northern Andes and the other in the Southern Andes, Chile, and Patagonia, with only three species of the principally southern dade appearing in the Central Andes (Fig. 6A). As shown in Figure 5, the northern dade is well supported by changes in head and floret size; the southern dade is characterized by major changes in leaf morphoanatomical characteristics.
Hummingbird pollination optimized onto the phylogeny of Chuquiraga (Fig. 6B) suggests that the changes in floral size of the northern dade (characters 21, 23, and 26) evolved in the ancestor of the whole group of species, in adaptation to hummingbird pollination pressure. Long floral size appears to be a current phylogenetic constraint in the species of the northern dade (Fig. 5).
Herbivory by guanaco (Lama quanicoe) optimized onto the phylogeny of Chuquiraga (Fig. 7A) suggests that the history of herbivory in the southern dade may have exerted selective pressure and may be related to several of the leaf characteristics of the group, including morphoanatomic characters that result in harder, more schlerenchymatous, less palatable leaves (e.g., characters 10 and 13) (Fig. 5).
Resistance to high summer temperatures optimized onto the phylogeny of Chuquiraga (Fig. 7B) suggests an effect of high temperatures associated with aridity on the evolution of leaf morphology in several species of Chuquiraga of the southern dade. Leaf characteristics of Chuquiraga species that extend to areas with higher summer temperatures (C. rosulata, C. aurea, C. ulicina, C. erinacea), such as narrow acicular leaf shape and maximum leaf involution, in combination with schlerenchyma in an abaxial shield (Fig. 5), are probably related to the history of increasing aridity of the warm deserts of South America.
These last results suggest that both temperature and herbivory seem to have interacted in the history of the southern clade.
Chuquiraga has been classified as part of an Austral-Antarctic phytogeographical element in the flora of the tropical Andes, suggesting a probable southern origin of the genus (Ulloa U. & Jorgensen, 1993). The results of this study support an origin of Chuquiraga in southern South America, from which two principal lineages, one northern (Central and Northern Andean) and one southern (principally Southern Andean and Patagonian), have probably evolved. The current geographical distribution of Chuquiraga parviflora, a basal lineage in the cladogram, agrees with the idea of an origin of the genus (as Protochuquiraga) in subtropical latitudes of southern South America, probably with the onset of aridity at these latitudes (Stuessy et al., 1996), related to the stressing of climatic zonation during the Miocene (Simpson, 1975; Solbrig, 1976). But the origin of the genus could have been even more southern, for the Patagonian Andes are an older formation than Andean cordilleras to their north (Taylor, 1991) and may ha ve exerted an appreciable rain-shadow effect on the North Patagonian massif since the Miocene, as fossil evidence suggests (Pascual, 1984; Pascual & Ortiz J., 1990). Climatic deterioration after the middle Miocene, together with increased elevation of the Central Andes, may have produced an extension of the cooler climate of northern Patagonia to lower latitudes and allowed the dispersal of Chuquiraga species toward the Central Andes.
Hummingbird pollination appears to have arisen in the base of the northern lineage. A relatively recent radiation of this clade seems to have produced the several large-headed, very closely related species of Chuquiraga. currently found in the Central and Northern Andes, which contradicts the idea that bird pollination could be generally ancestral in the Asteraceae (Funk et al., 1995). The origin of this northern group may be associated with the presence of Andean hillstar hummingbirds, their current principal pollinators (Carpenter, 1976, pers. comm.; Fjeldsa & Krabbe, 1990; Fjeldsa, pers. comm.), which are now typically found in very high parts of the tropical Andes. The origin of these birds was probably related to the appearance of high Andean open supraforest environments in the Northern Andes and the northern Central Andes during the second half of the Tertiary, from the Miocene onward (Simpson, 1986; Hooghiemstra & Cleef, 1995), when major Northern Andean orogenesis took place (Hooghiemstra & Cleef, 19 95) and high-elevation Trochiline hummingbird clades arose (Bleiweiss et al., 1994).
The final radiation of the northern Chuquiraga clade was probably related to the more recent Pliocene-Pleistocene climatic variations that appear to have so affected diversity in the Central and Northern Andes (Simpson, 1975, 1986). Several very closely related taxa of Chuquiraga in this area, in some cases treated as subspecies and in others as species (e.g., Ezcurra  and Granda P. , versus Ferreyra ), coincide with a similar pattern of closely related species or subspecies in Oreotrochilus hummingbirds (Carpenter, 1976; Fjeldsa & Krabbe, 1990). This suggests the importance of the relatively recent effect of the highly dynamic history of late Pliocene and Quaternary climatic changes on Andean montane ecosystems (Gentry, 1982; Hooghiemstra & Cleef, 1995), resulting in numerous relatively recent speciation events within genera (e.g., Simpson, 1986; Stuessy et al., 1996). The importance of the Andean uplift in relation to the evolutionary explosion of several hummingbird-pollinated shrubby or epiphytic taxa centered in the Northern Andean region has been emphasized by Gentry (1982).
Adaptation to aridity appears to have been the principal selective force that produced the diversification of leaf morphology and the radiation of the southern lineage of Chuquiraga.' Unequivocal xeromorphic leaf characters, such as leaf-area reduction, involute leaf margins, and stomata in pits, characteristic of many species of the southern clade, probably evolved in the Southern Hemisphere since the late Miocene (Hill, 1998), when the climate became cooler and drier from its peak of wet-warm in the middle Eocene (Raven & Axelrod, 1974; Solbrig, 1976). However, taxa adapted to aridity may also have originated in preexisting xeric habitats of South America, such as in rocky or skeletal soils, products of previous tectonic or volcanic activity.
The final uplift of the Andes was a more recent event, probably occurring mostly at the end of the Pliocene (Simpson, 1975; Taylor, 1991). At this time the deserts and semideserts of South America--i.e., currently corresponding to the Altoandina (High Andean), Puna, Patagonica, Desierto, Chilena, Prepuna, and Monte biogeographical provinces (Cabrera & Willink, 1980)--probably started to develop (Solbrig, 1976), as the rain-shadow effect of the Andes increased to a maximum and the cold Humboldt current acquired its present characteristics. This produced the hyperarid climates that rapidly reached their greatest extent and development during the Pleistocene and the Holocene (e.g., Simpson, 1975; Villagran et al., 1983; Simpson & Neff, 1985; Simpson & Todzia, 1990; Hinojosa & Villagran, 1997). It is the hyperaridization of Pliocene-Pleistocene times that appears to have been the selective force resulting in the adaptation of present-day taxa to the most extremely arid conditions of the warm deserts of South Amer ica, such as the Argentine Monte and the Pacific Desert. It is interesting to note that, based on molecular analyses of other groups of organisms, taxa of the high Andes and Patagonia have also been suggested as prime candidates for the impact of Pleistocene effects on biodiversification (Chesser, 2000).
The terminal position of the most xeromorphic acicular-leaved clade in the cladogram (formed by C. rosulata, C. aurea, C. erinacea, and C. ulicina, which currently inhabit the most arid regions of these deserts) suggests the relatively recent effect of aridity, in combination with the higher temperatures of lowland areas. Very narrow, rolled epistomatous leaves are disadvantageous except with sustained water stress, to minimize water loss and leaf overheating (Parkhurst & Loucks, 1972; Redmann, 1985). This type of adaptation is adequate in a group that appears to have had its origin in relatively cooler, semiarid, elevated or semielevated areas of southern South America and that later adapted to the extremely arid conditions of warmer, lower elevations (Ezcurra et al., 1997). The effect of high summer temperatures on the evolution of the annual genera Doniophyton and Duseniella appears to be related to the possibility of the species completing their life cycles in only one season, which generally does not occ ur in species found at high elevations in the winter snow-capped Southern Andes (Ferreyra et al., 1998).
Increased aridity at the end of the Tertiary and during the Quaternary seems to have coincided with the appearance and diversification of camelids in South America. This group of mammalian herbivores entered South America through North America from the end of the Pliocene to the beginning of Pleistocene (e.g., Webb, 1978) after the formation of the Isthmus of Panama (Parrish, 1987). The current geographical range of guanaco (Franklin, 1982; Wheeler, 1995) roughly matches the distribution of the southern Chuquiraga clade. In addition, Chuquiraga species have been reported to be a constant and abundant portion of the current diet of guanaco in Patagonia (Pelliza-Sbriller et. al., 1995; Somlo, 1997). These herbivores are thought to have exerted a selective pressure on the evolution of the leaf morphology of several southern species of Chuquiraga (Ezcurra et al., 1997). Guanacos, currently the largest native mammalian herbivores in the area of this genus, were very abundant until relatively recent times, and thei r selective pressure appears to have affected other spiny shrubs of Patagonia as well (Lauenroth, 1998).
Mechanical defenses, such as axillary spines and prickly leaf points, possibly originated early in the evolution of Barnadesioideae. This subfamily, with many spiny representatives, appears to rely more on physical defense mechanisms than on the chemical ones found in the rest of the Asteraceae (Robinson, 1987; Bohm & Stuessy, 1995). Experimental evidence suggests that spinescence deters feeding by vertebrates and that it could increase under selective pressure exerted by browsing animals (Obeso, 1997). These mechanical defenses probably evolved as protection against the rich fauna of large mammalian herbivores and ground ratite birds that were present in southern South America during the Tertiary, especially in the early Miocene (Webb, 1978; Bucher, 1987; Pascual & Ortiz J., 1990; Feduccia, 1996). Most of this megafauna became extinct at the end of the Tertiary, but in some cases it was replaced by other groups of herbivores, such as the camelids, that came from North America These, as "legions of the North, " dispersed into South America across the Central American land bridge during the beginning of the Quaternary (Pascual et al., 1985; Webb, 1985). Prickly blade points probably exapted to the extremely hard and prickly acicular leaves typical of the southern terminal clade in relation to browsing and grazing by these newcomers, which appeared in combination with increased aridity.
Extensive grazing and semiarid climates appeared simultaneously in the history of several plant groups. For example, it has also been suggested that an interplay between the effect of climate and herbivores was significant in the evolution of grasses (Stebbins, 1981; Coughenour, 1985). The simultaneous origin makes it difficult to ascertain the original adaptive value of traits that enhance survival under both aridity and grazing (Coughenour, 1985; Lauenroth, 1998). This appears to be the case in the southern Chuquiraga dade, which is most diversified in the deserts and semideserts of arid South America.
The present morphological approach to reconstructing the phylogeny of an Andean genus suggests a southern origin, as well as relatively recent adaptive radiations in the high tropical Andes and in the deserts of South America. Other Asteraceae genera currently found in the tropical Andes, such as Espeletia, also appear to have radiated recently, but they probably originated in lower latitudes (Cuatrecasas, 1986). This supports the idea that the combination of the unique history of each evolutionary group has resulted in the complex composition of the rich Andean flora.
The ultimate test of a phylogeny is the congruence or lack thereof between cladograms constructed from independent data sets, or the robustness of a cladogram with the addition of new data (Ruse, 1979; Eggleton & Vane-Wright, 1994). It would therefore be desirable, at this point, to reconstruct the phylogeny of Chuquiraga with molecular data, in order to test the phylogenetic and biogeographical hypotheses obtained from the results presented here.
VIII. Appendix 1: Morphological Characters and Character States Used in Cladistic Analysis of Chuquiraga and Related Genera (1-31), and Biogeographical and Ecological Characteristics of the Species (I-IV)
1. Habit: 0, ligneous; 1, herbaceous.
2. Pubescence on young stems: 0, present; 1, absent.
3. Leaf base: 0, shortly petiolate or subsessile; 1, sessile or vaginate.
4. Leaf position: 0, alternate; 1, opposite.
5. Leaves in rosettes: 0, absent; 1, present.
6. Leaf pubescence: 0, glabrous on both sides; 1, not glabrous on both sides.
7. Leaf pubescence: 0, not on abaxial side only; 1, on abaxial side only.
8. Leaf pubescence: 0, not on adaxial side only; I, on adaxial side only.
9. Maximum leaf length: 0, less than 3.5 cm; 1, more than 4 cm.
10. Involute leaf margin 0, absent, 1, present.
11. Axillary spines: 0, present; 1, always absent.
12. Leaf shape in cross-section: planate; 1, boat shaped; 2, acicular by marked involution.
13. Subepidermic schlerenchyma; 0, in longitudinal bands; 1, in a continuous abaxial plate.
14. Stomatal position on leaf surface: 0, hypo- or amphistomatous; 1, epistomatous.
15. Mesophyll: 0, dorsiventral or isolateral; 1, inverted dorsiventral or subcentric.
16. Involucre shape: 0, not turbinate; I, turbinate.
17. Position of external phyllaries: 0, erect; 1, radiating.
18. Position of internal phyllaries: 0, erect; 1, radiating.
19. Pubescence of phyllaries: 0, pubescent; 1, glabrous.
20. Maximum number of flowers per head: 0, up to 35; 1, 36 and more.
21. Floret size: 0, less than 15 mm; 1, more than 18 mm.
22. Corolla segments: 0, unequal; 1, equal.
23. Anther length: 0, less than 12 mm; I, more than 15 mm.
24. Brachyblasts with different leaves: 0, absent; 1, present.
25. Leaf shape: 0, not lineal; 1, lineal (ratio maximum length;width equal to or more than 10).
26. Maximum head length: 0, less than 30 mm; 1, equal to or more than 35-mm.
27. Head type: 0, homogamous; 1, heterogamous.
28. Head color: 0, greenish white to pure yellow; 1, yellow-orange to reddish orange.
29. Anther base: 0, obtuse; 1, sagittate.
30. Pollen shape: 0, with concave intercolpal regions; 1, without concave intercolpal regions.
31. Pappus type: 0, more or less plumose; 1, scaly.
I. Andean hillstar hummingbirds (Oreotrochilus spp.) on range of species: 0, absent; 1, present.
II. Mean January temperatures of more than 20[degrees]C on range of species: 0, absent; 1, present.
III. Guanaco (Lama guanicoe) on range of species: 0, absent; 1, present.
IV. Midlatitude of range of species: 0, Southern Andes and/or Patagonia; 1, Central and Northern Andes.
IX. Appendix 2 Data Matrix The morphological characters and biotic and abiotic factors related to ecoological and biogeographical characteristics of the taxa are numbered in accordance to Appendix 1. Taxon names corresponding to acronyms are: DACA, Dasyphyllum diacanthoides (Less.) Cabrera; SLUZ, Schlechtendalia luzulaefolia Less.; CAL, Chuquiraga calchaquina Cabrera; WEB, C. weberaueri Tovar; RAI, C. reimondiana Granda; SPI, C. spinosa Less.; ROT, C. rotundifolia Wedd. (incl. C. spinosa Less. subsp. huamanpinta C. Ezcurra and subsp. australis C. Ezcurra as subspecies of C. rotundifolia); JUS, C. jussieui J. F. Gmel.; ARC, C. arcuata Harling; OBL, C. oblongifolia Sagast. & Sanchez Vega; LON, C. longiflora (Griseb.) Hieron.; OPP, C. oppsitifolia D. Don; PAR, C. parviflora (Griseb.) Hieron.; MOR, C. morenonis (O. Kunteze) C. Ezcurra; AVE, C. avellanedae Lorentz; STR, C. straminea Sandwith; RUS, C. ruscifolia D. Don; ECH, C. echegarayi Hieron.; ATA, C. atacamensis Kuntze; KUS, C. kuschelii Acevedo; ACA, C. acanthophylla Wedd.; ROS, C. rosulata Gaspar; AUR, C. aurea Skottsb.; ULI, C. ulicina (Hook. & Arn.) Hook. & Arn.; ERI, C. erinacea D. Don; DWED, Doniophyton weddellii Katinas & Stuessy; DPAT, Duseniella patagonica (O. Hoffman) K. Schum. 1 11111 11112 22222 22223 3 12345 67890 12345 67890 12345 67890 1 I II III IV DACA 00000 00000 00000 00000 00000 00000 0 0 0 0 0 SLUZ 10111 10010 10000 00000 00000 00000 1 0 1 0 0 CAL 00010 11010 00000 11010 10100 10111 0 1 0 0 0 WEB 00010 11000 10000 00011 10100 10111 0 1 0 0 1 RAI 00010 11000 00000 00011 10100 10111 0 1 0 0 1 SPI 00010 11000 00000 00000 10100 10111 0 1 0 0 1 ROT 00010 01000 00000 00000 10100 10111 0 1 0 0 1 JUS 00000 00000 00000 10001 10100 10111 0 1 0 0 1 ARC 00000 11000 00000 10000 10100 10111 0 1 0 0 1 OBL 00000 00000 10000 00001 10100 10111 0 1 0 0 1 LON 00010 00000 00000 00010 10100 10111 0 1 0 0 1 OPP 00010 10000 00000 10000 01000 00111 0 0 0 1 0 PAR 00010 00000 00000 10010 00000 00011 0 0 0 0 0 MOR 00000 10000 00000 10000 01000 00011 0 0 0 1 0 STR 00000 10000 00000 00010 01010 00111 0 0 0 1 0 AVE 00000 10000 00000 00110 01000 00011 0 0 0 1 0 RUS 01100 10101 11111 00010 01000 00011 0 0 0 1 0 ECH 01100 10101 11111 01000 01000 00011 0 0 0 1 0 ATA 00100 10101 11111 11010 00000 00011 0 0 0 1 1 KUS 00100 10101 11111 10110 00000 00011 0 0 0 1 1 ACA 00100 10101 11111 10010 00000 00011 0 0 0 0 1 ROS 00101 10101 12111 10000 01011 00011 0 0 1 1 0 AUR 00100 10101 12111 00010 01001 00011 0 0 1 1 0 ULI 00100 10101 12111 11100 00001 00011 0 0 1 1 0 ERI 00100 10101 12111 00110 01001 00011 0 0 1 1 0 DWED 10000 10010 00000 01000 01001 01011 0 0 1 1 0 DPAT 10100 10010 10000 00010 01001 01011 0 0 1 1 0
Thanks are given to Beryl Simpson, Tod Stuessy, and an anonymous reviewer for constructive comments on the manuscript, to Adriana Ruggiero for help with the data analysis and for inspiring discussion, and to Victoria Amos and Florencia Funes for assistance with the illustrations. Support for this work was provided by the Universidad Nacional del Comahue (PI B068) and the Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET), Argentina (PIP 4120/96). The invitation of Carmen Ulloa Ulloa and Blanca Leon, organizers of the symposium on the biogeography and evolution of Andean plants at the XVI International Botanical Congress at Saint Louis, and the financial assistance of the congress that enabled me to present this work, are gratefully acknowledged. This article is dedicated to the memory of Angel L. Cabrera, who introduced me to the beauty and appeal of Andean plants.
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