A New Species of Parodia (Cactaceae, Notocacteae) from Rio Grande do Sul, Brazil Marlon C. Machado and Reto Nyffeler Institut fu¨r Systematische Botanik, Universita¨t Zu¨rich, Zollikerstrasse 107, CH-8008 Zu¨rich, Switzerland.
[email protected] Urs Eggli Sukkulenten-Sammlung Zu¨rich, Mythenquai 88, CH-8002 Zu¨rich, Switzerland.
[email protected] Joa˜o F. Larocca e Silva Universidade do Vale do Rio dos Sinos (Unisinos), Av. Unisinos 950, Bairro Cristo Rei, 93022-000, Sa˜o Leopoldo, Rio Grande do Sul, Brazil.
[email protected]
ABSTRACT . A new species, Parodia gaucha M. Machado & Larocca (Cactaceae, Notocacteae), from Encruzilhada do Sul, Rio Grande do Sul, Brazil, is described and illustrated. The new species is morphologically very similar to P. muricata (Otto ex Pfeiffer) Hofacker but can be distinguished from the latter by the presence of a conical projection below each areole, the higher number of shallower and narrower ribs, more closely spaced areoles, higher number of spines, different color of the spines, and seeds with minutely striate testa-cell surfaces. RESUMO . Descreve-se e ilustra-se uma nova espe´cie, Parodia gaucha M. Machado & Larocca (Cactaceae, Notocacteae), proveniente de Encruzilhada do Sul, Rio Grande do Sul, Brasil. A nova espe´cie e´ morfologicamente muito similar a P. muricata (Otto ex Pfeiffer) Hofacker, mas pode ser distinguida desta u´ltima pela presenc¸a de uma projec¸a˜o coˆnica abaixo de cada are´ola, por apresentar um nu´mero mais elevado de costelas que sa˜o menos profundas e de menor largura, menor espac¸amento entre are´olas, maior nu´mero de espinhos, por possuir espinhos de diferente colorac¸a˜o e sementes cujas ce´lulas da testa possuem uma superfı´cie finamente estriada. Key words: Brazil, Cactaceae, campos, IUCN Red List, Notocacteae, pampas, Parodia, Rio Grande do Sul. Parodia Spegazzini, as circumscribed by the Cactaceae Working Party of the International Organization for Succulent Plant Study (Hunt & Taylor, 1986, 1990), comprises about 60 to 70 species of mostly globular or occasionally subcolumnar cacti (Barthlott & Hunt, 1993; Hunt, 1999, 2006; Ander-
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son, 2001) distributed through the eastern part of central South America. The species occur in two centers of diversity (Buxbaum, 1964, 1966–1967, 1967a, b, 1975; Endler & Buxbaum, 1974): (1) the lowland pampas regions of southern Brazil (particularly in the state of Rio Grande do Sul), Uruguay, eastern Paraguay, and northeastern Argentina; and (2) on the eastern slopes of the Andes in northwestern Argentina and eastern Bolivia. Many species have limited distribution ranges and are often threatened by grazing, agriculture, and habitat modification. The stems of Parodia generally have tuberculate ribs, but a few taxa, e.g., P. haselbergii (Ru¨mpler) F. H. Brandt and P. microsperma (F. A. C. Weber) Spegazzini, differ in having distinct tubercles arranged in helical lines. The flowers of most Parodia species are large and funnel- or occasionally bellshaped, brightly colored, and pollinated by solitary bees (Schlindwein, 1995). The flowers arise near the stem apex, and the outside of the floral tube and the pericarpel is covered with bristles and hairs. The genus is characterized by having seeds with a straight or occasionally very slightly curved embryo and a large hilum-micropylar region (Barthlott & Voit, 1979; Barthlott & Hunt, 2000). Many of the seeds possess a prominent, either pad-, dome-, or balloon-shaped strophiole associated with the hilum-micropylar region. A number of well-circumscribed subgroups can be recognized in Parodia, some of which were recognized as distinct genera in the past. One such subgroup is the group of species related to P. ottonis (Lehmann) N. P. Taylor. This group consists of species placed in the formerly separate genus Notocactus (K. Schumann) Fricˇ (now subsumed under Parodia) and comprises
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the species included in Notocactus ser. Fricianae Havlı´cˇek (nom. inval., ICBN Art. 36.1 [McNeill et al., 2006]) and Notocactus ser. Paucispini (Fricˇ & Kreuzinger) Havlı´cˇek: P. carambeiensis (Buining & Brederoo) Hofacker, P. linkii (Lehmann) R. Kiesling, P. muricata (Otto ex Pfeiffer) Hofacker, P. ottonis, P. oxycostata (Buining & Brederoo) Hofacker, P. stockingeri (Prestle´) Hofacker & P. J. Braun, and P. tenuicylindrica (F. Ritter) D. R. Hunt. This group of species currently lacks a formal infraspecific taxon name under Parodia, and thus is referred here with the informal name P. ottonis group. Plants of the P. ottonis group share the morphological synapomorphy of producing offsets on short stolons, which often initially develop underground. Recent molecular systematic studies (Nyffeler, 1999; Machado et al., in prep.) have confirmed the monophyly of the P. ottonis group. In 2005 and 2006 the first author traveled extensively in the state of Rio Grande do Sul, Brazil, sampling populations of the Parodia ottonis group in order to infer species limits in this group and investigate infra- and interspecific relationships by studying morphological and molecular variation patterns for species delimitation analyses. During the course of one of the field excursions, a population of a distinctive taxon belonging to the P. ottonis group was found that represents a morphologically distinct entity; it is described here as a new species.
yellowish wool when young, later glabrescent; spines spreading, acicular, straight, almost bristly, 0.5–0.8 3 0.01–0.03 cm; central spines 6, golden yellow to reddish orange, hardly distinguished from the radials; radial spines 18 to 26, pale yellow; flowering areoles producing longer and curved spines to 1.5 cm. Flower buds with a dense cover of pale brownish hairs; flowers subapical, diurnal, opening for one to several days about 5 hours after sunrise and closing 4 hours later, shortly funnelform, to 4 3 5 cm; floral tube to ca. 1 cm, internal walls colored purplish red on the lower 1/3, yellow above; external walls yellowish green, with triangular bract scales subtending areoles that bear pale brownish to cream-yellow hairs and long yellowish bristles to 2 cm; perianth multiseriate, perianth segments pale yellow, lanceolate; stamens numerous (hundreds), spreading, arranged along the inner walls of the floral tube, sensitive and closing around the style when touched, lowermost stamens with filaments purplish red on the lower 1/3 to lower 1/2, yellow above; filaments to 0.7 cm; style yellow, ca. 1.6 3 0.2 cm; stigma lobes exserted, 10 to 12, dark red. Fruit 1.0–1.4 3 0.8–1.0 cm, greenish yellow, pericarpel with areoles bearing long yellowish brown hairs and a few curly bristles, dehiscing by one or more longitudinal slits, pulp white; dry perianth remnants either persistent on the fruit or falling off; seeds 1.0–1.2 3 0.8–0.9 mm, helmet-shaped, dark reddish brown to black, shiny; hilum-micropylar region 0.8–0.9 mm, pear-shaped, lateral to the seed axis, rim of hilum-micropylar region sharply edged against the testa, without bulging; testa cells convex, mostly pentagonal or hexagonal, ca. 50–100 3 30– 80 mm, elongated along the seed axis; cell boundaries straight, sunken; cell surface with a minutely striate cuticular folding pattern.
Parodia gaucha M. Machado & Larocca, sp. nov. TYPE: Brazil. Rio Grande do Sul: Mun. Encruzilhada do Sul, 90 m, 27 Oct. 2006, M. Machado 865 (holotype, ZSS; isotypes, HASU, HUEFS, MO). Figures 1, 2. Haec species Parodiae muricatae (Otto ex Pfeiffer) Hofacker affinis, sed projecturis infra quamque areolam conicis, costis numerosioribus angustioribus minus profundis, areolis densius dispositis, spinis numerosioribus coloribus diversis, cellulis testae seminis tenuiter striatis differt.
Plant body clavate to short-cylindric, 9–12 3 5– 8 cm, producing offsets from areoles located at the lower portion of the body; offsets first subterranean, produced on short stolons ca. 0.1 cm diam. and to 2 cm long; epidermis bright green; cortical tissues not mucilaginous, yellowish green in the upper portion of the body but becoming orange toward the base; ribs 18 to 22, straight, well-defined but slightly tuberculate, with shallow sinuses between successive tubercles, 0.2–0.4 cm tall 3 0.6–1.0 cm thick, edges serrate due to a conical projection (triangular in lateral view) below each areole; areoles located at the sinuses between consecutive tubercles, rounded, 0.2–0.25 cm diam., densely set, 0.3–0.4 cm apart, with pale
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Distribution and habitat. Parodia gaucha is at present known solely from its type locality in the municipality of Encruzilhada do Sul, Brazil, where it grows among rock outcrops in open grassland areas on hillsides and hilltops. The area consists of more or less rounded hills rising to ca. 300 m in altitude. The vegetation in the region is a composite of shrubby savanna-like vegetation on the lower parts of the hills, gallery forests in the valleys, and the grassland vegetation known as campos or pampas on the upper parts of the hills. In habitat P. gaucha grows in sympatry with other species of Cactaceae: P. ottonis, Frailea pygmaea (Spegazzini) Britton & Rose, Cereus hildmannianus K. Schumann, Opuntia Miller sp., Rhipsalis Gartner spp., and Lepismium Pfeiffer spp. IUCN Red List category. The population of Parodia gaucha is small, consisting of a few dozen individuals, the majority of which were located on a
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Figure 1. Parodia gaucha M. Machado & Larocca. —A. Habit; notice the underground offsets produced on short stolons (the dotted line indicates the soil line). —B. View of a rib with spines removed from the areoles, showing the conical projection below each areole. —C. Longitudinal section of a flower. —D. Typical areole with six central spines and 26 radial spines; the central spines hardly differentiable from the radials. —E. Detail of the fruits. Drawn from the holotype M. Machado 865 (ZSS).
single rocky wall at the margin of a country road. An extensive search of the surrounding area revealed that suitable rock outcrops among the grassland held very few plants, the majority of which displayed signs of being trampled and grazed by cattle and sheep. Due to the apparent rarity, restricted distribution, and observed threats, it seems prudent to include P. gaucha in the Critically Endangered category of the IUCN Red List of
endangered plant species according to the following criteria (IUCN, 2001): CR A2a B1ab(iii,v) C2a(ii) D. Due to the rarity of Parodia gaucha at its single known locality, no paratypes have been collected. Etymology. The specific epithet is derived from the vernacular term ‘‘gau´cho’’ (feminine form: ‘‘gau´cha’’), which in Brazil designates the natives from the
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Figure 2. Seeds of Parodia gaucha M. Machado & Larocca. —A. Lateral view. —B. Hilum-micropylar region. —C. Testacell surfaces, displaying minutely striated cuticular folding patterns. —D. Close-up of the striations of the testa-cell surface. From the holotype M. Machado 865 (ZSS).
state of Rio Grande do Sul; this epithet is in accordance with ICBN Art. 23.2 (McNeill et al., 2006). Systematic relationships. Parodia gaucha belongs to the P. ottonis group by virtue of producing offsets on short stolons and having fruits with a thick and fleshy pericarpel that dehisces by longitudinal slits. It is morphologically similar to the other many-ribbed species of this group, P. muricata, P. stockingeri, and P. tenuicylindrica. The species that most closely resembles P. gaucha is P. muricata, but the latter can be distinguished from the former by the following suite of characters: absence of a conical projection below each areole; lower number of ribs (only to 18), which are wider and higher than the ribs of P. gaucha; areoles that are less closely spaced; smaller number of spines (only to 18 including central and radial spines); spines of different color; and seeds with smooth testacell surfaces (Table 1). Parodia stockingeri shares with P. gaucha the presence of a conical projection below each areole, but it is a smaller plant with a
lower number of ribs and spines, and it has seeds with a smooth testa-cell surface (Table 1). Parodia tenuicylindrica differs from all other species of the P. ottonis group by producing hooked central spines; it differs from P. gaucha due to its smaller size, absence of a conical projection below each areole, the lower number of ribs and spines, and different color of the spines (Table 1). Parodia gaucha is geographically well separated from the other similar species of the P. ottonis group. Parodia muricata occurs in southwestern Rio Grande do Sul, Brazil, where it is known from a number of localities around the municipality of Jaguari. The nearest populations of P. muricata are separated from P. gaucha by over 250 km. Parodia stockingeri also occurs in southwestern Rio Grande do Sul, Brazil, where it is known from a handful of localities southeast of the village of Unistalda, municipality of Santiago. It is separated from P. gaucha by over 320 km. Parodia tenuicylindrica occurs in southwestern Rio Grande do Sul, Brazil, and northwestern
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Table 1. Comparison of morphological characters of species of the Parodia ottonis group. P. gaucha Body diameter (cm) Shape of body
P. muricata
to 8 clavate to short-cylindric No. of ribs 18 to 22 Height of rib (mm) 2–4 Width of rib (mm) 6–10 Distance between areoles (mm) 3–4 No. of central spines 6 Color of central spines yellow to orange-red
to 10 globose to short-cylindric 16 to 18 6–8 10–14 6–10 3 or 4 reddish brown
No. of radial spines Color of radial spines
18 to 26 yellow
10 to 14 glassy white
Testa-cell surface of seeds
minutely striated
smooth
Uruguay. The distribution of this species in Brazil is restricted to the area around and between the municipalities of Santana do Livramento and Quaraı´ in Rio Grande do Sul, with the northern limit south of the municipality of Alegrete; in Uruguay, the species is distributed in the area around and between the municipalities of Rivera and Artigas, with the southern limit north of the municipality of Tacuarembo´. The nearest populations of P. tenuicylindrica are separated from P. gaucha by over 260 km. Superficially, Parodia gaucha is reminiscent of yellow-spined forms of P. scopa (Sprengel) N. P. Taylor, but the latter is clearly distinguishable from P. gaucha because it has a higher number of ribs (24 to 40) and radial spines (36 to 40 or more), flowers with stamens lacking a reddish color at the base of the filaments, smaller fruits with a thin pericarpel that becomes papery and disintegrates after drying, and seeds with testa-cell surfaces displaying larger striate cuticular folding patterns (Glaetzle & Prestle´, 1986). Moreover, offsets of P. scopa are not produced on short stolons nor developed underground, characteristics that are synapomorphic for the P. ottonis group. Furthermore, P. scopa belongs to a clade distinct from that of the P. ottonis group (Nyffeler, 1999; Machado et al., in prep.). Acknowledgments. The authors would like to thank Cassio van den Berg, Universidade Estadual de Feira de Santana, for revising and correcting the Latin diagnosis of Parodia gaucha; Luciano Paganucci de Queiroz, Universidade Estadual de Feira de Santana, for his assistance during fieldwork of MCM in Rio Grande do Sul; Carla de Lima for skillfully preparing the botanical illustration of P. gaucha; and Julien Bachelier, University of Zu¨rich, for support in preparing SEM pictures of the P. gaucha seeds. This study was supported by grant 3100A0-103583 from the Swiss National Science Foundation to RN and UE.
P. stockingeri to 4 clavate to cylindric 12 to 15 3–5 4–8 3–4 4 yellow to orange-red 10 to 16 cream-yellow to yellow smooth
P. tenuicylindrica to 4 clavate to cylindric 13 to 21 2–4 4–6 1.5–3 2 to 4 reddish brown to black 10 to 16 cream-yellow to yellow minutely striated
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