Zamia multidentata Calonje, Segalla & R.S.Pimenta, 2023

Segalla, Rosane, Pimenta, Ricardo Soares & Calonje, Michael, 2023, Zamia multidentata (Cycadales, Zamiaceae), a new arborescent species of Zamia from Acre, Brazil, Phytotaxa 598 (1), pp. 21-31 : 22-28

Zamia multidentata Calonje, Segalla & R.S.Pimenta sp. nov. ( Figs. 1–3 )

Diagnosis: —The combination of slender (to 6.2 cm) caulescent stems, strongly serrulate elliptic leaflets with long acuminate tips and a pronounced adaxially raised longitudinal crease, as well as seed strobili with long peduncles (15 cm +) and flat megasporophylls distinguish the new species Zamia multidentata from all other known species in the genus.

Type: — BRAZIL. Acre: Mâncio Lima : 220m, 26 Sep 2020, R. Segalla & L.V. Lima SDMR 01 (holotype RB!, isotypes UFMT!, INPA!, UFACPZ!) .

Description: — Stem epigeous, cylindrical, typically solitary, 16–45 × 4.0– 6.2 cm. Cataphylls caducous, triangular to narrowly triangular, 3.7–7.02 cm long and 1.8–2.5 cm wide at base, abaxial surface densely covered with light yellow orange (RHS 158D) felted indumentum. Ptyxis slightly reflexed. Leaves 8–14 per crown, held relatively upright, slightly spreading, 114–152 cm long and 35.1–44.9 cm wide. Petiole 35–83 cm long and 10.7–21.7 mm thick, with abruptly swollen base to 35.79 mm wide, moderately to strongly armed with prickles 1.7–5.0 mm long., petiole and rachis densely covered with grey (RHS N189D) pubescent indumentum on new leaves, gradually shedding it to reveal medium yellow green (RHS 159D) to dark brown (RHS N200A) epidermis on older leaves. Rachis 43.0– 78.5 cm long, lightly armed with prickles mostly in the proximal fourth, with occasional solitary prickles occurring beyond. Leaflets 10–26, papyraceous to chartaceous, oppositely to sub-oppositely arranged, articulate insertion on rachis 2.9– 4.4 mm wide, spaced to 2.0 to 5.5 cm apart at leaf center, ovate to elliptic with long acuminate apex, distinctly raised longitudinal crease, margins strongly serrulate beyond proximal fourth with 30–49 teeth, median section traversed by 36–47 parallel veins, light green (RHS 138D) on new leaf flushes, at maturity turning medium brown green (RHS 136C) to light green (RHS 145B) adaxially, light green abaxially (RHS 135D), basal leaflets 10.0–21.0 cm × 3.0–7.0 cm, median leaflets 18.2–21.7 cm × 4.3–9.3 cm, apical leaflets 13.5–20.0 cm × 5.0– 8.3 cm. Eophylls 13–17 cm long, petiole 12–16 cm long, rachis 0.6–1.0 cm long bearing 4 leaflets. Eophyll leaflets oval to ovate with long acuminate apices, margins strongly serrulate in the distal half, the basal leaflets 7.2–8.0 × 3.5–3.6 cm, the apical leaflets 7.0–7.8 × 2.6–2.7 cm. Pollen strobili 1–5 per stem apex, fertile portion conical-cylindrical, at pollen shedding stage 8.2–8.3 × 1.4–1.5 cm, covered with medium brown (RHS 173C) to grey brown (RHS N199C) felted indumentum, strobilus apex acute 3.0–6.0 mm long and 4.7–5.3 mm wide at base, peduncle 8.8–9.1 × 0.7–0.8 cm, densely covered with light yellow (RHS 163D) tomentose indumentum, strobilar axis glabrous. Microsporophylls spirally arranged in 7–8 orthostichies of 14–16 fertile sporophylls each, median sporophylls 4.9–5.2 × 5.0– 5.2 mm. Microsporophyll shield a distinctly extruded hexagonal prism covered with dark yellow orange (RHS 173C) to grey brown (RHS N199C) felted indumentum, 2.1–2.5 mm tall and encompassing 2/5 to 1/2 of sporophyll length, 3.6–4.6 × 2.2–2.5 mm at the base, the distal face distinctly indented and slightly reduced to approximately ¾ the size of the base. Fertile portion of microsporophyll with adaxial surface glabrous, abaxial side lightly covered with grey-brown (RHS 199B) pubescent indumentum and patches of strong orange red (RHS 169A) pubescent indumentum restricted to the areas immediately surrounding individual microsporangia. Microsporangia present only on the abaxial side of the microsporophyll, slightly ovate, 1.1–1.2 × 0.9–1.0 mm, typically aggregated into a single group of 13–17 sporangia, but occasionally separated into two distinct marginal groups of 6–8 sporangia each. Ovulate strobili one per stem apex, fertile portion cylindrical, at maturity 16.2–18.0 × 4.7–5.6 cm, with acute apex 12–13 mm long and 84–99 mm wide at base, covered with dark brown purple (RHS N186C) felted indumentum on newly emerging strobili turning orange brown (RHS 172C) to medium brown (RHS 172A) at maturity; peduncle 15–19 × 1.2–1.4 cm, covered with purple grey (RHS 201C) indumentum when newly emerging, at maturity indumentum persisting in medium yellow brown (RHS 164B) patches or shedding to reveal grey brown glabrous epidermis (RHS 199A). Megasporophylls spirally arranged in 6–9 orthostichies of 6–10 sporophylls each, 20 × 10 mm, megasporophyll shield not extruded but relatively flat, 1.8–3.0 mm thick, 20–21 mm wide, and 14–17 mm tall, the distal facet shallowly indented, narrow and elongated and encompassing approximately 1/13th to 1/16 th of the area of the base. Seeds ovoid-pyramidal, sarcotesta medium red (RHS 44A) to orange red (RHS 32A) at maturity, 17.4–18.6 × 9.0–11.0 mm, sclerotesta ovoid, glabrous, light yellowbrown (RHS 161C), 13.0–16.4 × 8.6–9.8 mm.

Etymology: From the Latin multi (‘many’) and dentatus (‘toothed’), referring to the numerous teeth found along the margins of the leaflets of this species.

Habitat, geology and soils: — Zamia multidentata occurs in the upper Juruá River basin ( Daly et al. 2016) within the “Southwest Amazon Moist forests Ecoregion”, a region of high endemism and species richness in vascular plants ( Olson et al. 2001). To date it has been only been observed within a vegetation type officially classified in Brazil as “Open Alluvial Ombrophilous Forest with Palms” ( IBGE 2012), where it occurs on the alluvial soils of the Moa river floodplain adjacent to the Serra do Divisor, an isolated mountain range in the southwestern Amazon characterized by fiercely dissected peaks and ridges rising out of the surrounding lowland rainforest ( Salisbury et al. 2013). The soils originated from Holocene sediments and have a high content of fine sands resulting from the erosion of Cretaceous sandstone from the Serra do Divisor ( Mendonça et al. 2020). The soils are lower in organic carbon but richer in nutrients than those from the Serra do Divisor, are high in Al 3 + and have a mixed mineralogy with 2:1 clays, hydroxyl-Al interlayered smectite, and kaolinite ( Mendonça et al., 2020).

Climate: —The region of the Serra do Divisor mountainous complex is inserted in a transitional climatic band between the Humid and the Super-humid (relative humidity index close to 100) with rainfall (2,500 to 2,750 mm per year) frequent throughout the year, since even during the driest months (June to September) the totals are usually greater than 60 mm (Associaç„o SOS Amazônia 1998). In the other months of the year, totals greater than 180 mm predominate, and over 300 mm in the months of November to April (Associaç„o SOS Amazônia 1998). The mean annual air temperature is 25.0° C, with a mean minimum daily temperature of 20.8° C in the coldest month, and a mean maximum daily temperature of 28.6° C in the warmest month.

Ecology: —The species was rare in the surveyed area, with scattered individuals occurring in the forest understory, usually on flat to gentle slopes.Accordingly, very few seedlings or juvenile plants were observed. As this species to our knowledge has not been studied or collected before, little is known its population dynamics, reproductive phenology, or the plant-animal interactions affecting it. Although most South American species of Zamia are pollinated by beetles in the genus Pharaxonotha Reitter ( Coleoptera : Erotylidae ) ( Segalla et al. 2021, Tang et al. 2018), the pollination agents for this species remain unknown. Similarly, the seed dispersal agents are not known, and no evidence of herbivory by caterpillars of the genus Eumaeus ( Segalla & Morellato 2019) was observed in habitat. Strobili emerge from April to June, with the reproductive period when the seed strobili become receptive and the pollen strobili become dehiscent occurring from May through June. Pollinated ovulate strobili mature for approximately one year after pollination, with seed dehiscence occurring from May to July the year following cone emergence. New leaves are produced from October through December.

Distribution and conservation status: —The Sierra do Divisor’s ridge divides Brazil’s Jurua river basin from Peru’s Ucayali basin and serves as the international boundary between the two countries ( Salisbury et al., 2013). On the Brazilian side of the boundary lies the Serra do Divisor National Park, and on the Peruvian side its transboundary sister reserve, the Sierra del Divisor National Park. The adjacent transnational parks are part one of the largest contiguous blocks of protected areas in the Amazon, but despite their protected status, the region is threatened by anthropogenic activities including agriculture, hunting and subsistence fishing, tourism, and plant extraction for timber, charcoal, firewood, and horticulture (Associaç„o SOS Amazônia 1998; Daly et al. 2016; Esteves & Luz 2019). The location surveyed in this study, selected as the type locality, is protected within the Serra do Divisor National Park (SDNP), whereas the other known locality occurs outside of the park boundaries in an area that has been actively deforested in the last 40 years and where habitat transformation and deforestation continue unabated. The two known locations of Zamia multidentata are approximately 30 km away from each other within the Moa river floodplain at an elevational range of 200– 220 m. The species was infrequent within the SDNP location visited, and local field guides reported being aware of past extraction of wild plants in the region for horticultural purposes. Although no Peruvian collections are currently known, the species occurs approximately 20 km from the Peruvian border, so its distribution range may possibly extend into this country as well. Based on the two known locations for this species, the continuing decline in habitat quantity/quality in at least one of these locations, the reported threat to the species from commercial extraction for horticulture, and the small Extent of Occurrence (25 sq. km) and Area of Occupancy (8 sq. km), we recommend a listing of this species by the IUCN as Endangered based on criteria B1ab(i,ii,iii,iv,v)+2ab(i,ii,iii,iv,v); C2(i) (sensu IUCN Standards and Petitions Committee 2022).

Morphological affinities: — Zamia multidentata shares some morphological similarities with the Amazonian species Z. urep and Z. hymenophyllidia , including elliptic leaflets with long acuminate tips as well as ovulate strobili with long peduncles. Z. multidentata most closely resembles Z. hymenophyllidia , with which it shares the presence of a pronounced adaxially raised longitudinal crease on the leaflets, and slender (less than 7 cm wide) caulescent stems. Whether these morphological affinities correspond to a close phylogenetic relationship is currently unknown. While all species of Zamia from the Amazon basin phylogenetically evaluated to date appear to belong to the same clade, the fine-scale relationships between the constituent species in this clade remain unresolved and their resolution will require the use of new high-throughput sequencing technologies ( Calonje et al., 2019). Nevertheless, as within the Amazon basin these three species are the most likely to be confused morphologically, we hereafter discuss the morphological differences and similarities between them in order to aid in their identification.

The three species can be readily distinguished by their leaflet morphology alone ( Fig. 4 ), as they vary in their dentation, number and prominence of leaflet veins, and the presence or absence of an adaxially raised longitudinal crease ( Table 1 ). Zamia multidentata leaflets have a larger number of veins and teeth than the other two species. The presence of an adaxially raised longitudinal crease is present in both Z. multidentata and Z. hymenophyllidia , but absent in Z. urep which has relatively flat leaflets. The veins are extremely prominent on the adaxial leaflet surface of Z. urep , less so in Z. hymenophyllidia (though highly prominent in dried specimens), and not prominent in Z. multidentata . The color of newly emerging and expanding leaflets is green in both Z. multidentata and Z. hymenophyllidia , and medium yellow brown (RHS 163A) in Z. urep .

Zamia multidentata and Z. hymenophyllidia have caulescent trunks whereas Z. urep is acaulescent. In addition to differences in vegetative characters, Z. multidentata has microsporophylls typically bearing more microsporangia (12–17) than either Z. hymenophyllidia (10–12) or Z. urep (9–10) ( Table 1 ). Finally, although the three species are endemic to the Amazon basin, their geographic ranges do not overlap and are separated by hundreds of kilometers from each other ( Fig. 5 ).

Most Amazonian Zamia species have subterranean stems, and prior to this description, the massive species Z. poeppigiana , with its stems reaching 3 m tall and 30 cm in diameter ( Calonje et al., 2011), was considered the only truly arborescent species. Our field surveys documented that an arborescent habit is also widespread in Zamia multidentata , albeit it produces much shorter and more slender stems reaching up to 45 cm tall and 6.2 cm in diameter. Furthermore, we report that Zamia hymenophyllidia , previously considered a subterranean-stemmed species ( Stevenson, 2001), is an arborescent species producing similarly slender stems to Z. multidentata . Although most plants observed in our survey for this species in Leticia (Amazonas, Colombia) were acaulescent, we did observe a small number of plants in habitat with short slender stems up to 12 cm tall and 4 cm wide, and specimens report stems for this species up to 40 cm tall ( Barona 5044 [COAH!]) and 7 cm in diameter (Bernal et al. 2545 [COL!]). The slender (7 cm or less) caulescent stems produced by Z. multidentata and Z. hymenophyllidia are unusual in the genus, as most arborescent species have considerably thicker stems typically exceeding 8 cm at maturity. The extremely slender stems of these two species are perhaps only comparable to those of younger plants of Z. obliqua Braun (1875: 376) which at maturity can have stems from 6.5 to 15 cm in diameter.

Figures

FIGURE 1. Vegetative characteristics of Zamia multidentata. A. Median leaflet attached to rachis, B. Top view of eophyll, C. Habit of adult individual with ovulate strobilus. D. Newly emerging leaf showing slightly reflexed ptyxis and indumentum covering rachis, E. Middle section of petiole showing some patches of indumentum and prickles, F. Leaf. All photographs used for the preparation of the illustration were taken at the type locality.

FIGURE 2. Reproductive characteristics of Zamia multidentata. A. Near mature ovulate strobilus, B. Mature ovulate strobilus with ripe seeds, C. Immature ovulate strobilus. D. Megasporophyll shield, E. Megasporophyll with two mature seeds with sarcotesta intact, F. Seed sclerotesta, G. Pollen strobilus at pollen dehiscence stage, H. Microsporophyll abaxial view, I. Microsporophyll adaxial view, J. Pollen strobilus cross section showing microsporophyll arrangement, abaxial side, K. Close up of distal half of pollen strobilus.All photographs used for the preparation of the illustration were taken at the type locality.

FIGURE 3. Zamia multidentata in habitat. A. Adult plant in habitat with post-receptive ovulate strobilus, B. Abaxial side of leaf, with Márcio Sombra, C.Adult plant with Rosane Segalla for scale, D.Adult plant growing near river.The nutrient poor sandy soils of the region evident on the opposing riverbank. All photographs taken at type locality.

FIGURE 4. Comparison of microsporophylls and leaflets of Zamia multidentata, Z. hymenophyllidia, and Z. urep. A. Microsporophyll of Z. multidentata, abaxial side, B. Median leaflet of Z. multidentata, adaxial side, C. Microsporophyll of Z. hymenophyllidia, Nong Nooch Tropical Botanical Garden (NNTBG) accession 16022A, originally collected from Loreto, Perú. D. Median leaflet of Z. hymenophyllidia, adaxial side, photographed in Leticia, Amazonas, Colombia, E. Microsporophyll of Z. urep, abaxial side, F. Median leaflet of Z. urep, adaxial side. Photographs of Z. multidentata from material collected at type locality, photographs of Z. urep from NNTBG accession 15233A.

FIGURE 5. Disjunct geographic distribution of Zamia multidentata (triangles), Z. hymenophyllidia (circles), and Z. urep (crosses).