Zamia brasiliensis Calonje & Segalla, 2019

Segalla, Rosane & Calonje, Michael, 2019, Zamia brasiliensis, a new species of Zamia (Zamiaceae, Cycadales) from Mato Grosso and Rondônia, Brazil, Phytotaxa 404 (1), pp. 1-11 : 4-8

Zamia brasiliensis Calonje & Segalla sp. nov. (Figs. 1–3)

Diagnosis: — Zamia brasiliensis is distinguishable from Z. boliviana in having much broader leaflets and from Z. ulei in having unarmed petioles.

Type: — BRAZIL. Mato Grosso: Itaúba : 295m, 18 Sep 2018, R . Segalla & M. C . Jesus ITA01 (holotype UFMT!, isotype INPA!) .

Additional specimens examined: — BRAZIL. Mato Grosso: Alta Floresta , J. A . Lombardi s.n. ( HRCB 64169 ); Aripuanã : R. A . Rosa 183 ( IAN 145897 !), ex Aripuanã , cultivated at INPA in Manaus, Amazonas , W . Rodrigues 9713 ( INPA 68496 !); Guarantã do Norte : M. A . Carmello & F. J . Sonara s.n. ( UFMT 3311 !); Itaúba , 380 m, 26 Jun 2015, S. A . Antoniazzi S. A . 3630 ( HERBAM 19899 ), 280 m, 21 Oct 2015, M. E . Engels 3737 ( MBM 403994 ), 279 m, 13 May 2015, M. E . Engels 3825 ( CNMT 497 , MBM 403046 , TANG 3338 ), 289 m, 26 May 2017, M. E . Engels & L. S . Silva 95295517 Copel 9 ( HERBAM 20686 ), 374 m, 26 Oct 2015, M. E . Engels & A. S . Bezerra 3724 ( MBM 403995 ), 289 m, 26 May 2017, M. E . Engels 5517 ( HCF 24572), 295m, 12 Oct 2018, R . Segalla & E. A . Soares ITA02 ( UFMT!); Novo Mundo : 30 Jul 2006, D. Sasaki et al. 167 ( HERBAM 0411 ), 21 July 2006, D. Sasaki et al. 512 ( HERBAM 0614 ) ; Rondônia: Alvorada do Oeste : 1 May 1987, C. A . Cid Ferreira et al. 9000 ( INPA 153653 !); Cacoal : 22 Jun 1984, C. A . Cid Ferreira et al. 4701 ( INPA 121074 !); 185 m, 24 November 2018. R . Segalla & S. C . Freitas ROD05 ( INPA!), ROD06 ( UFMT!), ROD08 ( IAN!), ROD09 ( JBRJ!), ROD10 ( SP!); Campo Novo de Rondônia, 245 m, 8 Sep 2017, I . Mendes-Silva et al. 249 ( RON 15629!); Pimenta Bueno : P . Lisboa et al. 2924 ( MG 95972 !); Presidente Médici : 169 m, 21 Nov 2013, A . Petini-Benelli & S. C . Freitas APB920 ( UFMT 41202 !) .

FIGURE. Geographic distribution of Zamia brasiliensis in Mato Grosso and Rondônia. Locations marked with stars indicate the populations studied in Itaúba (Mato Grosso) and Cacoal (Rondônia).

Description: — Stem hypogeous, solitary or clustering, globose to cylindrical, 6.4–25 × 6.2–8.4 cm. Cataphylls caducous, triangular to narrowly triangular, 6.5–8.5 cm long and 1.2–1.8 cm wide at base, margins glabrous and orange, central abaxial surface densely cream-orange tomentose, gradually loosing tomentum as cataphyll dries and turns tanbrown. Leaves 1–6 per crown, spreading, 10–112 cm long, longitudinal ptyxis inflexed. Petiole 10.5–61.2 cm long and 3.8–6.0 mm thick, slightly grooved adaxially, with abruptly swollen base to 13.5 mm wide, unarmed. Rachis 0.1–54.5 cm long, unarmed. Leaflets 2–24 (10+ on adults), chartaceous to subcoriaceous, oppositely to sub-oppositely arranged, articulate insertion on rachis 5.0– 5.5 mm wide, spaced to 1.5 to 4.7 cm apart at leaf center, lanceolate to obovate with acuminate apex, margins strongly serrated in distal 1/4 to 1/3, basal leaflets 16–22 cm × 1.9–3.5 cm, middle leaflets 16.7–21 cm × 2.4–3.5 cm, apical leaflets 12.7–17.0 cm × 2.2–3.2 cm, light green on new leaf flushes, turning dull greyish green to bright green at maturity. Eophylls to 10.5 cm long, rachis 1–2 mm long, carrying two to four leaflets 4.8 × 1.7 cm. Pollen strobili 1–3 per crown, yellow-cream tomentose, conical-cylindrical, at pollen shedding 12.8 × 1.9 cm, sterile apex obtuse and tan-brown tomentose to 8 mm long, strobilar axis densely villous with white to orange trichomes, peduncles cream colored and villous with mixed yellow and orange-brown tomentum, 3.8–4.0 × 0.8 cm. Microsporophylls spirally arranged in 9–12 orthostichies of 20–30 sporophylls each, obtrullate, 5.2–6.4 × 4.0– 4.8 mm at pollen shedding, villous in proximal section and near sterile apex transition, sterile apex encompassing 30–45 % of the total microsporophyll length, cream-yellow tomentose with brown speckles on distal section, face hexagonal to oblong hexagonal, 2.7–3.2 mm tall × 3.4–3.8 mm wide with shallowly indented terminal facet, abaxial surface of microsporophyll with 19–21 microsporangia concentrated mostly along the margins but with a few on the central area, adaxial surface glabrous, without microsporangia. Ovulate strobili 8–11.5 × 3.5–4.8 cm, typically solitary but up to five per apex, erect at maturity, cylindrical with pronounced acute or obtuse sterile apex encompassing 1/5 to 1/12 of the strobilus length, beige-green when first emerging, turning to solid orange-brown at receptivity, and at maturity the margins of megasporophylls becoming a markedly lighter tan-cream. Strobilar axes and megasporophyll pedicels glabrous on mature strobili, peduncles 10–26 × 0.5–0.6 cm, maturing from tan to brown tomentose with green undertones. Megasporophylls spirally arranged in in 9–10 orthostichies of 6–13 sporophylls each, pedicel 13.5–15.0 mm long, sterile apex 2.5–5.5 mm thick with hexagonal to oblong-hexagonal distal face 13.4–16.2 mm wide and 9.3–12.0 mm tall, roundly extruded to a narrow, shallowly depressed reddish-brown terminal facet. Seeds ovoid to ovoid-pyramidal, at maturity 11.9–16.6 × 7.1–9.3 mm with paper thin orange-red sarcotesta, sclerotesta 11.3–15.3 × 6.7–8.6 mm.

FIGURE. Extents of occurrence of a) Zamia ulei , b) Z. boliviana , and c) Z. brasiliensis . Note non-overlapping geographic distributions of the three species.

Etymology: — Zamia brasiliensis is the only species of Zamia endemic to Brazil. The specific epithet refers to its distribution which is restricted to this country.

Climate: —The climate within the area of occupancy of Zamia brasiliensis is classified as equatorial savanna with dry winter (Aw) by the Koppen-Geiger classification system ( Köppen 1918, Geiger 1954, Kottek et al. 2006). It is characterized by an average temperature of 18° C or higher, the dry season occurring in the winter, and the driest month having less than 60 mm precipitation and contributing less than 4% of the total annual precipitation. The climate is considered hot and humid, with temperatures relatively constant year round. Mean annual temperature ranges from 24.7° to 25.2° C, low temperatures from 18.9° to 20.6° C and high temperatures between 30.4° and 32.2° C (Data derived from GIS analysis using bioclimactic variables from CHELSA (Karger et al. 2016). Annual rainfall ranges from 1400 to 2500 mm per year with a distinct dry season (<100 mm per month) occurring from May through September. The driest months are June through August, receiving less than 30 mm per month, while the wettest months are December through March, receiving over 300 mm.

Ecology: —Strobili emerge from September to December, the seed strobili becoming receptive and the pollen strobili becoming dehiscent from October to December. Pollinated seed strobili develop from November through August, with seed dehiscence occurring from June to September. New leaves are produced from August to November. In Itaúba, we observed colonies of an unidentified species of Pharaxonotha Reitter ( Coleoptera : Erotylidae ), a potential pollinating agent, within dehiscent pollen strobili and in the soil around the adult plants. In the Cacoal population, larvae of a butterfly species of the genus Eumaeus Hübner (1819: 17) were observed feeding on new leaves of Z. brasiliensis .

Habitat, geology and soils: — Zamia brasiliensis occurs in various habitats within the transition zone between the Brazilian Cerrado and the Amazon forest in upland areas of northern Mato Grosso and Rondônia states (Rondônia and North Mato Grosso Uplands Landscape Region, sensu Volkoff et al. (2012), including submontane dense and open ombrophilous forests, semideciduous and deciduous seasonal forests, and woodland savannas, also known as Cerradão ( IBGE 2012).

The Itaúba (Mato Grosso) population studied occurred in submontane semideciduous forest transitioning to an open ombrophilous forest at the margins of the Teles Pires River (Figs. 3a, 3b). Semideciduous forest is characterized by two well-demarcated climatic seasons, a rainy season followed by a long biologically dry period during which 20% to 50% of all trees lose their foliage ( IBGE 2012). The forest has high biomass with lianas and epiphytes common, and a 25–30 m high canopy with a few emergents. The community structure includes trees that range from 2 to 30 m in height and from 3.18 to 92 cm diameter at breast height (1.30 m). Within the semideciduous forest, the distribution pattern of Zamia brasiliensis follows the edaphic features of the habitat, with plants appearing to be more common in the drier, sandier areas. The soil is a slightly acidic sandy clay loam (Table 1) with a rocky substratum consisting of arcosean sandstones, medium to coarse grained, with lenses of argillite conglomerates, siltstones and sandstones of the Dardanelos Formation, with the main soil types in the area being Litolic Neosols and Red-Yellow Oxisols. ( SEPLAN, 2000).

TABLE. Soil analysis results for submontane semideciduous forest habitat in Itaúba (Mato Grosso) and woodland savannah (cerradão) in Cacoal (Rondônia) localities of Zamia brasiliensis . Soil analysis conducted by Agroanálise Labs, Cuiabá, Mato Grosso, Brazil .

The Cacoal (Rondônia) population studied occurred in a woodland savanna (cerradão) in an area of rolling hills characterized (Figs. 3c, 3d) by a lithology of basement rocks and Paleozoic sediments (Central Rondônia hills sensu Volkoff et al., 2012). The soil is a slightly acidic sandy clay loam (Table 1) with a rocky substratum consisting of arcosean sandstones and ortho-quartzites with lenses of coal and gypsum (Pimenta Bueno formation, CPRM 1999). Plants appeared most common along the edges of the cerradão at is interface with the more open ‘campo cerrado’. Here the plants grew interspersed among grasses, shrubs and trees.

Distribution and conservation status: — Zamia brasiliensis has an extent of occurrence (EOO) of 139,453 km 2 and has been collected in at least ten different locations (Fig. 4). Although the geographic distribution range for this species is broad, the species occurs within the “Arc of Deforestation”, the Brazilian agricultural frontier in southsoutheastern Amazonia where the highest rate of deforestation in the Amazon basin occurs ( Coe et al. 2013). In the last 30 years (1987 to 2017), forest cover within the EOO has decreased by 32.45%, and only approximately 60% of the EOO remains forested. As is the case for the Amazon as a whole ( Tyukavina et al. 2017), by far the primary cause for deforestation within the EOO has been agro-industrial forest clearing for cattle pasture, with 34% of the area currently converted to pasture. The area of occupancy (AOO) for Z. brasiliensis is estimated to be 53.3 km 2. Most of the historic collections of this species occurred in areas that have been severely deforested, and only a few disjoint populations are known to persist. Only a single protected area is known to harbor this species, the Parque Estadual Cristalino, in the state of Mato Grosso ( Sasaki et al. 2010, Zappi et al. 2011). Based on the AOO smaller than 500 km 2, severe fragmentation of the remaining populations, and a projected decline in EOO, AOO, and habitat quality due to continued land transformation in the region, we recommend this species be listed as Endangered (EN) based on IUCN Red List criteria B2ab(i-v) (IUCN Standards and Petitions Subcommittee, 2017).

TABLE. Distinguishing traits of Zamia brasiliensis , Z. boliviana , and Z.ulei .

Morphological affinities: — Zamia brasiliensis shares morphological similarities with Z. ulei and Z. boliviana , three subterranean-stemmed species with adjacent but non-overlapping geographic distributions (Fig. 5). Zamia ulei is broadly distributed in the Amazon basin, Z. boliviana occurs in the Cerrado biome of Brazil and Bolivia, and Z. brasiliensis inhabits various habitats within the Cerrado-Amazon transition zone. Collections of Z. brasiliensis in herbaria have often been misidentified as Z. ulei , most likely because the leaf size and leaflet shape of Z. brasiliensis are similar to those of young plants of Z. ulei . However, adult individuals of Z. ulei produce much larger leaves and leaflets that far exceed the dimensions of those of Z. brasiliensis . Even at a young age, the species are easily diagnosable, because Z. ulei has petioles armed with robust prickles, whereas Z. brasiliensis has unarmed petioles. Unarmed petioles are very rare in mainland American Zamia , and in South America, they are only associated with Z. encephalartoides Stevenson (2001: 40) , Z. boliviana , and Z. brasiliensis . The unarmed petioles, relative geographic proximity, and broad similarities in reproductive structures suggest that Z. boliviana is the closest relative of Z. brasiliensis . However, the two species are readily distinguishable based on differences in both vegetative and reproductive morphology. Z. brasiliensis has leaflets that are considerably broader (2.4–3.5 cm) than those of Z. boliviana (0.8–2 cm). The faces of the mature megasporophylls of Z. boliviana are much wider (18.1–21.9 cm) than those of Z. brasiliensis (14.1–15.0 cm). Additionally, fewer sporophyll orthostichies are found in Z. boliviana seed strobili (6–7) than in those of Z. brasiliensis (8–14). The pollen strobili in both species is yellow-cream tomentose, but in Z. boliviana , the color is solid, whereas in Z. brasiliensis , the sterile apex is covered with orange-brown tomentum (Fig. 2c). The three species are readily distinguishable based on quantitative and qualitative characters (Table 2). A taxonomic key to aid in the identification of these species is provided below.