Zamia orinoquiensis Calonje, Betancur & A. Lindstr. 2022, sp. nov.

Zamia orinoquiensis Calonje, Betancur & A.Lindstr. sp. nov. (Figs 3–5) Diagnosis: — Zamia orinoquiensis is distinguished from Z. muricata by its leaves bearing leaflets that are coriaceous (vs. papyraceous) in texture, eophylls with 2 (vs. 4) leaflets, pollen strobili that are brown to reddish brown (vs. cream to tan) with microsporophylls bearing more numerous (22–32 vs. 8–18) microsporangia, and ovulate strobili that are dark brown vs. dark olive green at maturity. Type: — COLOMBIA. Cundinamarca: Medina, 500–525 m, 1 Feb 2020, Jonatan Castro, Cristina López, Michael Calonje, Cristian Castro & Fredy Parra 1554 (holotype: HUA!, isotypes COAH!, COL!, FMB!, HUA!, JAUM!, LLANOS!) Additional specimens examined (paratypes): — COLOMBIA. Casanare: Aguazul, 12 Feb 2012, C . Ruiz et al. 325 (CUVC!); Tauramena, F. J . Mijares 2257 (HORI!); Villanueva, 300 m, 12 Feb 1939. O . Haught 2601 (COL!, US!); Cultivated in Casanare, Harry Vaughan s.n. (FTG!). Cundinamarca: Medina, 520 m, 2 Feb 2020, J . Castro et al. 1555 (COAH!, HUA!, JAUM!); 413–514 m, 25 Oct 2017, M. F . González et al. 4380 (COL!); 500–525 m, 1 Feb 2020, C . López et al. 98 (COAH!, HUA!). Paratebueno, 4 Feb 2020, 500 m, J . Castro et al. 1580 (COL!, HUA!). Meta: La Macarena, 29 Apr 2002, M . Gaitán et al. 83 (COAH!); 450 m, 6 Feb 1950, W. R . Phillipson 2368 (BM!); 296 m, 25 Jun 2004, J. G . Ramírez-Arango et al. 7701 (COAH!, COL!); 300 m, 6 Jul 2004, J. G . Ramírez-Arango et al. 8514 (COAH!); 402 m, 13 Jul 2004, J. G . Ramírez-Arango et al. 8536 (COAH!). Mesetas, 360–490 m, 25 Feb 1988, R . Callejas & O. Marulanda 5911 (HUA!, MO!); La Uribe, 350–400 m, Jul 1998, P . Stevenson 2122 (ANDES!). San Juan de Arama, 445 m, 9 Aug 2004. L . Carvajal et al. 334 (UDBC!); San Martín, 21 Oct 1945, P. H . Allen 3355 (MO!, US!); 29 May 2011, G . Téllez & F. Ciri 1650- A & 1650- B (JAUM!). Description: — Stem hypogeous, tuberous, typically solitary or rarely branching, globose to cylindrical, to 35 cm long and 12 cm diameter. Cataphylls papyraceous, narrowly triangular, beige to grey tomentose, with a pair of stipules near the apex, 1.0– 2.5 cm wide at base, 4.5–9.0 cm long. Leaves 1–3 (4) per stem apex, erect to spreading, 66–160 cm long. Petiole 53–102 cm long, with slight groove on adaxial side and abruptly swollen base to 3 cm wide, dark olive green, sparsely to moderately armed with prickles 1–5 mm long or occasionally unarmed. Rachis 13–58 cm long, typically unarmed or with few scattered prickles in proximal fourth, ending in a short 0.1–1.5 cm brown tomentose terminal tip. Leaflets 6–22, coriaceous, suboppositely to subalternately arranged, articulate insertion on rachis 1–6 mm wide, spaced 4–8 cm apart at leaf center. Median leaflets lanceolate to obovate, abruptly acuminate distally, straight to slightly falcate, with 20 to 45 spreading teeth 0.2–2.0 mm long restricted to distal one half to one quarter of leaflets, new leaflets emerging light reddish brown covered with white and orange tomentum at emergence, becoming green and glabrous at maturity. Basal leaflets 18.5–36.0 cm × 3.9–9.7 cm, median leaflets 18.0–35.0 cm × 3.8–11.0 cm, apical leaflets 17.0–29.0 cm × 3.7–9.5 cm. Eophylls with unarmed petioles 10–20 cm long, rachis 1 mm long, carrying two lanceolate leaflets 4.4–6.5 × 1.8–4.0 cm. Pollen strobili 1–3 per stem apex, brown to reddish brown tomentose, cylindrical, 7.2–12.0 × 1.6–2.2 cm at pollen shedding, peduncle brown to reddish brown tomentose, 8.0–17.0 × 0.6–1.3 cm, strobilar axis and inner surfaces of microsporophylls glabrous. Microsporophylls spirally arranged in 14–19 orthostichies of 15–24 fertile sporophylls each, 6.5–9.4 × 5.6–6.9 mm, pedicel distinct, 1.8–2.0 mm long, sterile shield encompassing 1/4 to 1/3 of sporophyll length. Margins of fertile area of microsporophylls with distinct narrow wings that are falcate and angled towards proximal end. Microsporangia spherical to slightly ovate 0.9–1.0 × 0.65–0.8 mm, present only on abaxial side, aggregated into two distinct marginal groups of 12–16 each or a single group of 23–36 microsporangia. Sterile shield a distinctly extruded hexagonal prism 3.1–3.8 mm tall, 5.0–5.6 × 4.1–4.3 mm at the base, the distal facet distinctly indented and reduced to approximately ¼ of the area of the base, mostly reddish-brown tomentose with a narrow cream-yellow strip at proximal section where it comes in contact with other microsporophylls. Ovulate strobili one per stem apex, cylindrical, burgundy-tomentose at emergence and receptivity, maturing to black tomentose with green undertones, 7.3–14.0 × 4.7–5.0 cm at maturity, apex pungent and 2–5 mm long, peduncle similar in color to strobilus, 6.0–18 × 0.8–1.2 cm diameter at center, strobilar axes and megasporophyll pedicels glabrous. Megasporophylls spirally arranged in 5–7 orthostichies of 4–9 sporophylls each, 19.0–21.5 × 21.2–23.0 mm, sterile shield a shallowly extruded hexagonal prism 14.0–16.0 mm tall, 21.2–23.0 wide at the base, the distal facet shallowly indented and reduced to approximately ¼ of the area of the base. Seeds ovoid to ovoid-pyramidal, sarcotesta red-orange at maturity, 15–17 × 0.8–1.0 mm, sclerotesta glabrous, brown-yellow but abruptly and distinctly darker at distal end, 11.0–15.0 × 7.0–10.0 mm. Etymology: —The specific epithet refers to the Orinoquía natural region in Colombia where this species occurs. Common name: —Known as ‘Quiripia’ in the Serranía de La Macarena mountain range (per label on specimen Gaitan et al. 83 [COAH!]). Distribution, habitat, and climate: — Zamia orinoquiensis is endemic to the Orinoquía natural region of Colombia, also known as the Eastern Plains, or ‘Llanos Orientales’. This region, best known for its extensive savannas, consists of three major landscapes: an area of high plains known as the altillanura, extensive flood plains, and the piedmont areas of the Eastern Cordillera of the Andes (Ospina, 2005). The species occurs primarily in the foothills of the piedmont of the Eastern Cordillera as well as in foothills of the isolated Serranía de La Macarena mountain range, extending slightly into the adjacent dissected or flat altillanura landscapes of both regions (Fig. 1). Zamia orinoquiensis occurs in the shaded understory of tropical wet and tropical moist forests (sensu Holdridge, 1977) at elevations ranging from 230 to 730 m in the departments of Casanare, Cundinamarca, and Meta. The annual mean temperature within its area of occupancy ranges from 24.8–26.8° C and the annual precipitation between 2200–4200 mm. The rainfall pattern is bimodal, with the highest monthly peaks in rainfall within the area of occupancy ocurring in May through June (270–580 mm) and a smaller peak in October (260–441 mm), and the driest month being January (9–95 mm). Ecology and phenology: —Individuals are distributed in patches in the forest understory, usually on moderate slopes. The three populations visited in February 2020 all occurred in small forest fragments, but all with presence of seedlings and juveniles (see Figure 6 for a stage-based distribution of individuals of the two largest populations). There are no detailed studies on the population dynamics or the vegetative/reproductive phenology of the species, and very few fertile collections exist in herbaria. We observed mature and near-receptive ovulate strobili as well as pollen strobili at or near dehiscence during our fieldwork in February 2020. Mature ovulate strobili of this species have previously been collected in August 1998 and July 2004. In Medina we observed colonies of an unidentified species of Pharaxonotha Reitter (Coleoptera: Erotylidae), a potential pollinating agent, within a dehiscent pollen strobilus. A good proportion of viable seeds was observed in ovulate strobili at the three localities visited, indicating the presence of healthy populations of pollinators at these locations. The typical herbivores associated with Zamia species, Eumaeus (Lycenidae: Lepidoptera), were not observed in the three surveyed locations in Cundinamarca but have been reported in Casanare (Díaz-Pérez & Morales-Puentes, 2018). Most seed dispersal in Zamia is by gravity, but small vertebrates could be involved in rare long-distance dispersal events. Conservation status: —The species has a relatively large geographic distribution with a large number of populations (16 known so far), compared to other endemic Zamia species in Colombia. Nevertheless, most of the populations are within highly degraded landscapes with high rates of deforestation, and no conservation actions are known for the species. The estimated extent of occurrence (EOO) is 18,148 km 2. Five of the populations (or subpopulations sensu IUCN Standards and Petitions Committee 2019) occur within national-level protected areas with large tracts of viable habitat (Tinigua, Serranía de La Macarena and Cordillera de los Picachos national parks). However, the remaining 11 populations are not within protected areas and persist in small forest fragments (less than 100 hectares) in landscapes highly modified by urbanization and agricultural activities (mostly cattle ranching). The species can be considered as severely fragmented (10 subpopulations are small and isolated) and with continuing decline in habitat quantity/quality (sensu IUCN Standards and Petitions Committee 2019). Therefore, the species should be classified as Vulnerable (VU) using criteria B1ab(iii). Colombia has a national conservation action plan for cycads (López-Gallego, 2015), and the species will be included in this conservation plan to ensure the long-term protection of some populations and their habitats. Morphological affinities: — Zamia orinoquiensis is vegetatively similar to Z. muricata in that both species have subterranean stems and leaflets that are markedly toothed in the distal half to two-thirds. However, the two species are readily distinguishable utilizing vegetative and reproductive morphological characters (Tables 2 & 3). Z. muricata is generally a more robust plant than Z. orinoquiensis, typically bearing more leaves per stem (2–9 vs 1–4), more leaflets per leaf (15–54 vs. 6–22), and ultimately attaining a larger maximum leaf length (2.5 vs 1.6 m). It also appears to branch more frequently, as several branched plants of Z. muricata were observed in the field, whereas all plants of Z. orinoquiensis observed were single-stemmed. The leaflets of Z. orinoquiensis are coriaceous and are held rigidly, whereas the leaflets of Z. muricata are papyraceous to chartaceous and slightly pendulous. The leaflet shape generally differs between the two species, albeit with some overlap. Zamia orinoquiensis leaflets are typically obovate with abruptly acuminate apices, whereas those of Z. muricata are typically lanceolate with acute to long-acuminate apices. The eophylls of Z. orinoquiensis carry two leaflets whereas those of Z. muricata carry four. In terms of reproductive morphology, the pollen strobili of both species are readily distinguishable. The pollen strobili of Z. orinoquiensis are brown to reddish-brown tomentose externally, whereas those of Z. muricata are cream to tan tomentose. The microsporophylls of Z. orinoquiensis are much larger (6.5–9.4 × 5.6–6.9 mm vs. 4.6–6.8 × 3.6–5.7 mm) and bear more numerous microsporangia (23–36 vs. 12–18) than those of Z. muricata. Finally, the ovulate strobili of Z. orinoquiensis are brown to black tomentose at maturity, and those of Z. muricata are dark olive green to olive brown and tend to be more glabrous. The habitats where the species occur also differ, with Z. orinoquiensis occurring in tropical wet and tropical moist forests (sensu Holdridge, 1977) with an annual precipitation of 2200–4200 mm, whereas Z. muricata in Venezuela occur in dry forests and tropical moist forests with 600–1600 mm of rain per year. The populations of Z. muricata in Serranía de Macuira occur in cloud forests at the summits of hills where precipitation is very low (