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¨tZu¨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. son, 2001) distributed through the eastern part of Machado & Larocca (Cactaceae, Notocacteae), from central South America. The species occur in two Encruzilhada do Sul, Rio Grande do Sul, Brazil, is centers of diversity (Buxbaum, 1964, 1966–1967, described and illustrated. The new species is 1967a, b, 1975; Endler & Buxbaum, 1974): (1) the morphologically very similar to P. muricata (Otto ex lowland pampas regions of southern Brazil (particu- Pfeiffer) Hofacker but can be distinguished from the larly in the state of Rio Grande do Sul), Uruguay, latter by the presence of a conical projection below eastern Paraguay, and northeastern Argentina; and (2) each areole, the higher number of shallower and on the eastern slopes of the Andes in northwestern narrower ribs, more closely spaced areoles, higher Argentina and eastern Bolivia. Many species have number of spines, different color of the spines, and limited distribution ranges and are often threatened by seeds with minutely striate testa-cell surfaces. grazing, agriculture, and habitat modification. The stems of Parodia generally have tuberculate RESUMO . Descreve-se e ilustra-se uma nova espe´cie, ribs, but a few taxa, e.g., P. haselbergii (Ru¨mpler) F. Parodia gaucha M. Machado & Larocca (Cactaceae, H. Brandt and P. microsperma (F. A. C. Weber) Notocacteae), proveniente de Encruzilhada do Sul, Spegazzini, differ in having distinct tubercles ar- Rio Grande do Sul, Brasil. A nova espe´cie e´ ranged in helical lines. The flowers of most Parodia morfologicamente muito similar a P. muricata (Otto species are large and funnel- or occasionally bell- ex Pfeiffer) Hofacker, mas pode ser distinguida desta shaped, brightly colored, and pollinated by solitary u´ltima pela presenc¸a de uma projec¸a˜ocoˆnica abaixo bees (Schlindwein, 1995). The flowers arise near the de cada are´ola, por apresentar um nu´mero mais stem apex, and the outside of the floral tube and the elevado de costelas que sa˜o menos profundas e de menor largura, menor espac¸amento entre are´olas, pericarpel is covered with bristles and hairs. The maior nu´mero de espinhos, por possuir espinhos de genus is characterized by having seeds with a straight diferente colorac¸a˜o e sementes cujas ce´lulas da testa or occasionally very slightly curved embryo and a possuem uma superfı´cie finamente estriada. large hilum-micropylar region (Barthlott & Voit, 1979; Barthlott & Hunt, 2000). Many of the seeds possess a Key words: Brazil, Cactaceae, campos, IUCN Red prominent, either pad-, dome-, or balloon-shaped List, Notocacteae, pampas, Parodia, Rio Grande do strophiole associated with the hilum-micropylar Sul. region. A number of well-circumscribed subgroups can be Parodia Spegazzini, as circumscribed by the recognized in Parodia, some of which were recognized Cactaceae Working Party of the International Orga- as distinct genera in the past. One such subgroup is nization for Succulent Plant Study (Hunt & Taylor, the group of species related to P. ottonis (Lehmann) N. 1986, 1990), comprises about 60 to 70 species of P. Taylor. This group consists of species placed in the mostly globular or occasionally subcolumnar cacti formerly separate genus Notocactus (K. Schumann) (Barthlott & Hunt, 1993; Hunt, 1999, 2006; Ander- Fricˇ (now subsumed under Parodia) and comprises

NOVON 18: 214–219. PUBLISHED ON 22 MAY 2008. doi: 10.3417/2007088 Volume 18, Number 2 Machado et al. 215 2008 Parodia gaucha (Cactaceae) from Brazil

the species included in Notocactus ser. Fricianae yellowish wool when young, later glabrescent; spines Havlı´cˇek (nom. inval., ICBN Art. 36.1 [McNeill et al., spreading, acicular, straight, almost bristly, 0.5–0.8 3 2006]) and Notocactus ser. Paucispini (Fricˇ & 0.01–0.03 cm; central spines 6, golden yellow to Kreuzinger) Havlı´cˇek: P. carambeiensis (Buining & reddish orange, hardly distinguished from the radials; Brederoo) Hofacker, P. linkii (Lehmann) R. Kiesling, radial spines 18 to 26, pale yellow; flowering areoles P. muricata (Otto ex Pfeiffer) Hofacker, P. ottonis, P. producing longer and curved spines to 1.5 cm. Flower oxycostata (Buining & Brederoo) Hofacker, P. stock- buds with a dense cover of pale brownish hairs; ingeri (Prestle´) Hofacker & P. J. Braun, and P. flowers subapical, diurnal, opening for one to several tenuicylindrica (F. Ritter) D. R. Hunt. This group of days about 5 hours after sunrise and closing 4 hours species currently lacks a formal infraspecific taxon later, shortly funnelform, to 4 3 5 cm; floral tube to name under Parodia, and thus is referred here with ca. 1 cm, internal walls colored purplish red on the the informal name P. ottonis group. Plants of the P. lower 1/3, yellow above; external walls yellowish ottonis group share the morphological synapomorphy green, with triangular bract scales subtending areoles of producing offsets on short stolons, which often that bear pale brownish to cream-yellow hairs and initially develop underground. Recent molecular long yellowish bristles to 2 cm; perianth multiseriate, systematic studies (Nyffeler, 1999; Machado et al., perianth segments pale yellow, lanceolate; stamens in prep.) have confirmed the monophyly of the P. numerous (hundreds), spreading, arranged along the ottonis group. inner walls of the floral tube, sensitive and closing In 2005 and 2006 the first author traveled around the style when touched, lowermost stamens extensively in the state of Rio Grande do Sul, Brazil, with filaments purplish red on the lower 1/3 to lower sampling populations of the Parodia ottonis group in 1/2, yellow above; filaments to 0.7 cm; style yellow, order to infer species limits in this group and ca. 1.6 3 0.2 cm; stigma lobes exserted, 10 to 12, investigate infra- and interspecific relationships by dark red. Fruit 1.0–1.4 3 0.8–1.0 cm, greenish studying morphological and molecular variation yellow, pericarpel with areoles bearing long yellowish patterns for species delimitation analyses. During brown hairs and a few curly bristles, dehiscing by one the course of one of the field excursions, a population or more longitudinal slits, pulp white; dry perianth of a distinctive taxon belonging to the P. ottonis group remnants either persistent on the fruit or falling off; was found that represents a morphologically distinct seeds 1.0–1.2 3 0.8–0.9 mm, helmet-shaped, dark entity; it is described here as a new species. 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 Parodia gaucha M. Machado & Larocca, sp. nov. against the testa, without bulging; testa cells convex, TYPE: Brazil. Rio Grande do Sul: Mun. mostly pentagonal or hexagonal, ca. 50–100 3 30– Encruzilhada do Sul, 90 m, 27 Oct. 2006, M. 80 mm, elongated along the seed axis; cell boundaries Machado 865 (holotype, ZSS; isotypes, HASU, straight, sunken; cell surface with a minutely striate HUEFS, MO). Figures 1, 2. cuticular folding pattern. Haec species Parodiae muricatae (Otto ex Pfeiffer) Distribution and habitat. Parodia gaucha is at Hofacker affinis, sed projecturis infra quamque areolam conicis, costis numerosioribus angustioribus minus profun- present known solely from its type locality in the dis, areolis densius dispositis, spinis numerosioribus color- municipality of Encruzilhada do Sul, Brazil, where it ibus diversis, cellulis testae seminis tenuiter striatis differt. grows among rock outcrops in open grassland areas on hillsides and hilltops. The area consists of more or Plant body clavate to short-cylindric, 9–12 3 5– less rounded hills rising to ca. 300 m in altitude. The 8 cm, producing offsets from areoles located at the vegetation in the region is a composite of shrubby lower portion of the body; offsets first subterranean, savanna-like vegetation on the lower parts of the hills, produced on short stolons ca. 0.1 cm diam. and to gallery forests in the valleys, and the grassland 2 cm long; epidermis bright green; cortical tissues not vegetation known as campos or pampas on the upper mucilaginous, yellowish green in the upper portion of parts of the hills. In habitat P. gaucha grows in the body but becoming orange toward the base; ribs 18 sympatry with other species of Cactaceae: P. ottonis, to 22, straight, well-defined but slightly tuberculate, Frailea pygmaea (Spegazzini) Britton & Rose, Cereus with shallow sinuses between successive tubercles, hildmannianus K. Schumann, Opuntia Miller sp., 0.2–0.4 cm tall 3 0.6–1.0 cm thick, edges serrate due Rhipsalis Gartner spp., and Lepismium Pfeiffer spp. to a conical projection (triangular in lateral view) below each areole; areoles located at the sinuses IUCN Red List category. The population of between consecutive tubercles, rounded, 0.2–0.25 cm Parodia gaucha is small, consisting of a few dozen diam., densely set, 0.3–0.4 cm apart, with pale individuals, the majority of which were located on a 216 Novon

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 endangered plant species according to the following extensive search of the surrounding area revealed that criteria (IUCN, 2001): CR A2a B1ab(iii,v) C2a(ii) D. suitable rock outcrops among the grassland held very Due to the rarity of Parodia gaucha at its single few plants, the majority of which displayed signs of being known locality, no paratypes have been collected. trampled and grazed by cattle and sheep. Due to the apparent rarity, restricted distribution, and observed Etymology. The specific epithet is derived from threats, it seems prudent to include P. gaucha in the the vernacular term ‘‘gau´cho’’ (feminine form: ‘‘gau´- Critically Endangered category of the IUCN Red List of cha’’), which in Brazil designates the natives from the Volume 18, Number 2 Machado et al. 217 2008 Parodia gaucha (Cactaceae) from Brazil

Figure 2. Seeds of Parodia gaucha M. Machado & Larocca. —A. Lateral view. —B. Hilum-micropylar region. —C. Testa- cell 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 lower number of ribs and spines, and it has seeds with ICBN Art. 23.2 (McNeill et al., 2006). with a smooth testa-cell surface (Table 1). Parodia tenuicylindrica differs from all other species of the P. Systematic relationships. Parodia gaucha belongs ottonis group by producing hooked central spines; it to the P. ottonis group by virtue of producing offsets differs from P. gaucha due to its smaller size, absence on short stolons and having fruits with a thick and of a conical projection below each areole, the lower fleshy pericarpel that dehisces by longitudinal slits. It number of ribs and spines, and different color of the is morphologically similar to the other many-ribbed spines (Table 1). species of this group, P. muricata, P. stockingeri, and Parodia gaucha is geographically well separated P. tenuicylindrica. The species that most closely from the other similar species of the P. ottonis group. resembles P. gaucha is P. muricata, but the latter can Parodia muricata occurs in southwestern Rio Grande be distinguished from the former by the following suite do Sul, Brazil, where it is known from a number of of characters: absence of a conical projection below localities around the municipality of Jaguari. The each areole; lower number of ribs (only to 18), which nearest populations of P. muricata are separated from are wider and higher than the ribs of P. gaucha; P. gaucha by over 250 km. Parodia stockingeri also areoles that are less closely spaced; smaller number of occurs in southwestern Rio Grande do Sul, Brazil, spines (only to 18 including central and radial spines); where it is known from a handful of localities spines of different color; and seeds with smooth testa- southeast of the village of Unistalda, municipality of cell surfaces (Table 1). Parodia stockingeri shares Santiago. It is separated from P. gaucha by over with P. gaucha the presence of a conical projection 320 km. Parodia tenuicylindrica occurs in southwest- below each areole, but it is a smaller plant with a ern Rio Grande do Sul, Brazil, and northwestern 218 Novon

Table 1. Comparison of morphological characters of species of the Parodia ottonis group.

P. gaucha P. muricata P. stockingeri P. tenuicylindrica Body diameter (cm) to 8 to 10 to 4 to 4 Shape of body clavate to globose to clavate to clavate to cylindric short-cylindric short-cylindric cylindric No. of ribs 18 to 22 16 to 18 12 to 15 13 to 21 Height of rib (mm) 2–4 6–8 3–5 2–4 Width of rib (mm) 6–10 10–14 4–8 4–6 Distance between areoles (mm) 3–4 6–10 3–4 1.5–3 No. of central spines 6 3 or 4 4 2 to 4 Color of central spines yellow to orange-red reddish brown yellow to reddish brown to black orange-red No. of radial spines 18 to 26 10 to 14 10 to 16 10 to 16 Color of radial spines yellow glassy white cream-yellow to cream-yellow to yellow yellow Testa-cell surface of seeds minutely striated smooth smooth minutely striated

Uruguay. The distribution of this species in Brazil is Literature Cited restricted to the area around and between the Anderson, E. F. 2001. The Cactus Family. Timber Press, municipalities of Santana do Livramento and Quaraı´ Portland. in Rio Grande do Sul, with the northern limit south of Barthlott, W. & G. Voit. 1979. Mikromorphologie der the municipality of Alegrete; in Uruguay, the species Samenschalen und Taxonomie der Cactaceae: ein raster- elektronenmikroskopischer U¨ berblick. Pl. Syst. Evol. 132: is distributed in the area around and between the 205–229. municipalities of Rivera and Artigas, with the ——— & D. R. Hunt. 1993. Cactaceae. Pp. 161–197 in K. southern limit north of the municipality of Tacuar- Kubitzki (editor), The Families and Genera of Vascular embo´. The nearest populations of P. tenuicylindrica Plants, Vol. 2. Springer-Verlag, Berlin. are separated from P. gaucha by over 260 km. ——— & ———. 2000. Seed-diversity in the Cactaceae subfamily Cactoideae. Succ. Pl. Res. 5: 1–176. Superficially, Parodia gaucha is reminiscent of Buxbaum, F. 1964. Bericht ueber den Stand der Untersu- yellow-spined forms of P. scopa (Sprengel) N. P. Taylor, chungen zur Phylogenie der Tribus Notocacteae. IOS Bull. but the latter is clearly distinguishable from P. gaucha 2: 46–62. because it has a higher number of ribs (24 to 40) and ———. 1966–1967. Gattung Parodia. In H. Krainz (editor), radial spines (36 to 40 or more), flowers with stamens Die Kakteen. Lieferung 1. XI. 1966 und 1. I. 1967. Frankh’sche Verlagsbuchhandlung, Stuttgart. lacking a reddish color at the base of the filaments, ———. 1967a. Der gegenwaertige Stand der stammes- smaller fruits with a thin pericarpel that becomes geschichtlichen Erforschung der Kakteen. Kakteen Sukk. papery and disintegrates after drying, and seeds with 18: 3–9, 22–27. testa-cell surfaces displaying larger striate cuticular ———. 1967b. Gattung Notocactus. In H. Krainz (editor), ´ Die Kakteen. Lieferung 35, CVIc. Frankh’sche Verlags- folding patterns (Glaetzle & Prestle, 1986). Moreover, buchhandlung, Stuttgart. offsets of P. scopa are not produced on short stolons nor ———. 1975. Provisorische Neugliederung der Tribus developed underground, characteristics that are syna- Notocacteae. In H. Krainz (editor), Die Kakteen. pomorphic for the P. ottonis group. Furthermore, P. Lieferung 60, CVI. Frankh’sche Verlagsbuchhandlung, scopa belongs to a clade distinct from that of the P. Stuttgart. Endler, J. & F. Buxbaum. 1974. Die Pflanzenfamilie der ottonis group (Nyffeler, 1999; Machado et al., in prep.). Kakteen. Ein systematischer Wegweiser fuer Liebhaber und Zu¨chter, 3rd ed. Albrecht Philler Verlag, Minden, Acknowledgments. The authors would like to Germany. thank Cassio van den Berg, Universidade Estadual Glaetzle, W. & K. H. Prestle´. 1986. Seed-morphology of the de Feira de Santana, for revising and correcting the genus Notocactus. Bradleya 4: 79–96. Latin diagnosis of Parodia gaucha; Luciano Paga- Hunt, D. R. 1999. CITES Cactaceae Checklist, 2nd ed. Royal Botanic Gardens, Kew. nucci de Queiroz, Universidade Estadual de Feira de ———. 2006. The New Cactus Lexicon. DH Books, Santana, for his assistance during fieldwork of MCM Milborne Port, United Kingdom. in Rio Grande do Sul; Carla de Lima for skillfully ——— & N. P. Taylor (editors). 1986. The genera of the preparing the botanical illustration of P. gaucha; and Cactaceae: Towards a new consensus. Bradleya 4: 65–78. Julien Bachelier, University of Zu¨rich, for support in ——— & ——— (editors). 1990. The genera of Cactaceae: Progress towards consensus. Bradleya 8: 85–107. preparing SEM pictures of the P. gaucha seeds. This IUCN. 2001. IUCN Red List Categories and Criteria Version study was supported by grant 3100A0-103583 from 3.1. Prepared by the IUCN Species Survival Comission. the Swiss National Science Foundation to RN and UE. IUCN, Gland, Switzerland. Volume 18, Number 2 Machado et al. 219 2008 Parodia gaucha (Cactaceae) from Brazil

McNeil,J.,F.R.Barrie,H.M.Burdet,V.Demoulin, Nyffeler, R. 1999. Notocactus versus Parodia—The search D.L.Hawksworth,K.Marhold,D.H.Nicolson,J. for a generic classification of the subtribe Notocactinae. Prado, P. C. Silva, J. E. Skog, J. H. Wiersema & Cactaceae Cons. Initiat. 7: 6–8. N. J. Turland (editors). 2006. International Code of Schlindwein, C. 1995. Specialized solitary bees as effective Botanical Nomenclature (Vienna Code). Regnum Veg. pollinators of South Brazilian species of Notocactus and 146. Gymnocalycium (Cactaceae). Bradleya 13: 25–34.