A new disjunct Dendrothrix (Euphorbiaceae, tribe Hippomaneae): a Guiana Shield element in sub-Andean cordilleras of Ecuador and Peru

Abstract Dendrothrix condorensis K.Wurdack, sp. nov. from the sub-Andean cordilleras of Ecuador and Peru is described and illustrated. The new species is geographically widely separated from its likely closest relative, D. yutajensis, which is endemic to the Guiana Shield region of southern Venezuela and adjacent Brazil, and notably differs in leaf morphology. Vegetative (i.e., epidermal micropapillae, trichomes) and reproductive (i.e., cymule glands, flowers, pollen) micromorphological features were examined with SEM. Rare tristaminate flowers were documented among the typical bistaminate ones. Seeds and diagnostic features among the four species of Dendrothrix are compared.


Introduction
One of the most challenging groups of Euphorbiaceae with regard to identification and classification is the hippomanoid clade of subfamily Euphorbioideae. The clade presently includes 32-40 genera and 300 species grouped in three tribes (Hippomaneae, Hureae, and Pachystromateae;Esser 2001Esser , 2012 or a single large one (Hippomaneae s.l., Webster 2014). Their taxonomy still needs considerable revision, especially at the generic level, in light of molecular phylogenetic results that reveal multiple non-monophyletic groups (Wurdack et al. 2005;Wurdack, unpublished). Dendrothrix Esser is one of the many small genera of hippomanoids (19 of the 40 genera contain three or fewer species) that have been relatively recently recognized, and one whose systematics had been confused with other taxa in the clade including Sapium Jacq. and Senefelderopsis Steyerm. (Esser 1993(Esser , 1995. The shared similarities with Sapium include their bistaminate flowers with a partly fused calyx, and with Senefelderopsis their shared inflorescence structure and Guiana Shield distribution. Dendrothrix contains four species of trees and shrubs with white latex, tiny apetalous flowers, and an unusual distribution in northern South America that includes tepuis in the Guiana Shield region and two disjunct outliers (Fig. 1). The genus is distinguished within the hippomanoids by a combination of relatively rare character states including compound thyrse inflorescences, dendritic trichomes, large disc-or cup-shaped bract glands, staminate flowers with two connate stamens, and small, dry fruits. Since Esser's original studies (1993Esser's original studies ( , 1995 little new information has been published about Dendrothrix except for wood anatomy (Mennega 2005). The relationships of Dendrothrix were thought to lie with Senefelderopsis, and although the former is a distinctive group, Webster (2014) suggested that it might be reduced to a section of Senefelderopsis. Recent work on its molecular phylogenetic placement (Wurdack, unpublished) has shown that they are not sister groups and should not be merged. Moreover, a close relationship with Mabea Aubl., which had been suggested based on the shared multicellular dendritic trichomes from which Dendrothrix gets its generic name (Esser 1993), was also not supported.
Dendrothrix yutajensis (Jabl.) Esser was reported for the flora of Ecuador (Neill and Ulloa Ulloa 2011), which represented a considerable range extension. After further study of Dendrothrix collections from sub-Andean cordilleras of southern Ecuador and adjacent Peru, I have concluded that they are morphologically distinctive enough to deserve recognition as the new species described herein. These mountains along the wet northeastern flank of the Andes, also referred to as "Andean tepuis," are rich in endemic taxa, especially in the Cordillera del Cóndor (Neill 2005). Floristic inventory work begun there in the 1990s has yielded numerous new taxa in diverse families. For the Cordillera del Cóndor in particular, its location, climate, and unusual geology of mid-Cretaceous Hollin Formation sandstone in tepui-like mesas support biogeographic affinities with the Guiana Shield biota to the east on pre-Cambrian sandstones, e.g., Phainantha Gleason, Melastomataceae (Ulloa Ulloa and Neill 2006); Stenopadus S. F. Blake, Asteraceae (Pruski 1998). The new Dendrothrix adds the first member of Euphorbiaceae to the growing list of floristic disjunctions between the Andean tepuis and their counterparts in the Guiana Shield. The Euphorbiaceae diversity for the Cordillera del Cóndor region otherwise mostly appears typical of that seen in other montane Andean floras and is not especially rich, with less than 20 taxa. However, among those taxa are the unusual endemic Croton condorensis Riina & Cerón (Riina et al. 2014), and the more widely distributed new genus Incadendron (Wurdack and Farfan-Rios 2017).
Etymology. The specific epithet refers to the Cordillera del Cóndor, where the type was collected. The mountain range name in turn comes from "condor" based on "kuntur" (Quechua) and refers to the Andean condor (Vultur gryphus L.), an important part of the ecology and culture of the Andes.
Distribution and ecology. The new species mostly occurs at 800-1000 m in dense, low, wet forest and sclerophyllous scrub over nutrient poor, acidic, sandstone-derived soils. Such habitats resemble those in the Guiana Highlands occupied by D. yutajensis. The three well-separated localities (Cordillera del Cóndor, Cordillera Escalera, Cerro Teyu; Fig. 1) are discoveries due to recent exploration in remote sub-Andean cordilleras, and continued floristic work is likely to extend its range to similar habitats further south in Peru. Floristic affinities between the Cordillera del Cóndor and Cordillera Escalera are notable (Neill et al. 2014). Flowers and fruits were collected during September-November and flowers in March (also fruits in July fide Croat 91402, not seen). Dendrothrix yutajensis with more collections to finely document phenology, is reproductive from November to May and appears to flower and fruit continuously during this period.
Conservation status. Following the criteria and categories of IUCN (2012), D. condorensis is given a preliminary status of Vulnerable (VU) under geographic range criteria B2 area of occupancy <2000 km 2 (B2a, known to exist at no more than 10 locations; B2b, continuing decline projected). Threats to this taxon in the Cordillera del Cóndor include mining for the underlying silica sand. The Cordillera Escalera is protected as a conservation area.
Additional collections. ECUADOR. Zamora-Chinchipe: Nangaritza, Cordillera del Cóndor region, west side of upper Río Nangaritza, along road about 13 km south of Guayzimi, silica mine "La Daniela", dense wet forest on sloping Hollín sandstone plateau, being mined for silica sand for glass manufacture, 04°08 Discussion. The four species of Dendrothrix are morphologically similar, and major differences are presented in Table 1. Dendrothrix condorensis and D. yutajensis are likely closely related as they have nearly identical floral features. However, they are easily distinguished by foliar characters (i.e., size, shape, thickness, and details of leaf architecture), seed caruncle differences, and biogeography. Although leaf architecture has not been rigorously compared through clearings and anatomy, several orders of the varyingly prominulous venation are evident in unprepared specimens that allow gross comparisons such as were shown by Esser (1993) to be informative for the group. In D. condorensis, secondaries are 18-22 pairs, mostly straight with few course deflections, and distally curving upward for <1/4 of course; intersecondaries are rare, and tertiaries are percurrent (Fig. 3G). In D. yutajensis, secondaries that are fewer (usually 7-9 pairs), not straight due to a slight zigzag (fractiflexuous) appearance where tertiaries diverge, and distally curving upward for half of their course; intersecondaries and frequent, and tertiaries are reticulate (Fig. 3J). Even on unusually robust specimens of D. yutajensis (e.g., Maguire & Maguire 35103, US), the largest leaves (16.5-18 × 6.5-7.8 cm) have only up to 11 pairs of secondaries. The leaves of D. condorensis more closely resemble those of D. multiglandulosa Esser with which it shares the generally larger blades and percurrent venation. Dendrothrix multiglandulosa is only known from two collections from the Cuao-Sipapo massif in Venezuela and potential variation is poorly understood. Dendrothrix yutajensis is the most frequently collected and wide-ranging species of Dendrothrix, known from many well-separated tepuis, but intraspecific variation appears low. Dendrothrix wurdackii Esser has previously unrecognized intraspecific variation with an odd collection (i.e., BRAZIL, Pará: km 872 Cuiabá-Santarém [Highway], Distinctly connate at base (to 0.5 mm), lobes rounded to broadly acute; margin erose or irregularly minutely toothed, very sparsely ciliate Pistil Style 1.5-2 × 0.5-0.7 mm; stigma branches long (to 1.1 mm), thin, recurved/coiled Style 1.5(-2) × 0.5-0.7; stigma branches long (to ca 1 mm), thin, recurved/coiled Style 1-1.3 × 0.5-0.7 mm; stigma branches short (to 0.5 mm), spreading but not recurved Style 1-1.5 × 0.5-0.6 mm; stigma branches long (to ca 1  Serra do Cachimbo, forest beside small stream, 6 Nov 1977, G. Prance 24947, MO, NY, US), having much larger (to 18 × 8.5 cm), long acuminate, glabrous leaves with poorly developed abaxial micropapillae as compared with the four other collections of the species that closely resemble the type. This collection, which Grady Webster annotated as a new species of Senefeldera Mart., clearly has closest affinities with D. wurdackii based on similarities in leaf shape and venation, basilaminar glands, pistillate sepal shape, and biogeography. While the morphological differentiation and slight disjunction (Fig. 1) may be significant, it is not to the degree used here to justify the recognition of D. condorensis and I have refrained from further taxonomic adjustments until D. wurdackii is better understood. Leaf micromorphological features are similar among the taxa of Dendrothrix. The distinctive, loosely attached, branched trichomes (Fig. 3E, K) are structurally very similar but can differ in pigmentation (rusty brown versus whitish; see Table 1). Epidermal microrelief such as micropapillae or striations that give an often light-colored, matte sheen to abaxial leaf surfaces has evolved in many genera of Euphorbiaceae, including Dendrothrix, and other hippomanoids (e.g., Gymnanthes hypoleuca Benth., Sebastiania larensis Croizat & Tamayo, Senefelderopsis croizatii Steyerm.). The microrelief likely has functional significance related to optimized stomatal conductance and reduced leaf wetting (Neinhuis and Barthlott 1997). The morphology of the leaf micropapillae in Dendrothrix is unusual and may be synapomorphic. They have positional size variation in being short to absent on major veins and grading to longer in intercostal regions (Fig. 3K). In D. condorensis, the micropapillae are finger-like, 25-30 μm tall, ornamented with ridges, and form a protective canopy that obscures the stomata (Fig. 3H-I). Epicuticular waxes are not well developed, in keeping with the non-glaucous appearance. The stomata are only abaxial, with the adaxial surface being relatively featureless (Fig. 3I). Glands are often present on leaves and/or inflorescences of Euphorbiaceae, and Dendrothrix is no exception where they occur in pairs at the base of the leaf and subtending the bracts. The nature of scattered laminar glands in Dendrothrix is partly unclear. In the case of D. wurdackii they resemble typical Euphorbiaceae laminar glands with a well defined raised border and an abaxial distribution adjacent to secondary veins towards the leaf margin. The glands on Prance 24947 contain drops of clear exudate that are still sticky after 40 years. I have not found clearly homologous structures on the other taxa of Dendrothrix. Circular to widely elliptic, small (<0.5 mm diameter), gland-like structures with smooth surfaces and without raised edges are sparsely present in D. condorensis and more abundantly so in D. multiglandulosa, where in the latter they were considered of systematic significance (Esser 1993). Although not examined anatomically, these appear to be wound response to microbial damage rather than typical glands as evidenced by their absence in the few young leaves available, erratic distribution, the presence of apparently intermediate epidermal blistering stages that are clearly necrotic, and margins that are not clean under SEM (not shown) but rather contain fragments that suggest micropapillae residue from surficial degradation.
Among reproductive characters that are variable among the species are details of the pistillate flowers including sepal and stigma morphology (see Table 1). Staminate bract glands vary in number with Dendrothrix multiglandulosa usually having 2-3 pairs (variable from 1-4, and paired or unequal in number between the bract sides), while the other species have one pair (D. yutajensis rarely has a second gland on one side, e.g., Maguire & Maguire 35103, NY). Inflorescence branching is potentially variable, with 2-3 orders for D. condorensis and D. multiglandulosa, and the other species have only two orders. It is unclear if this represents noteworthy interspecific variation or possible collector bias for smaller inflorescences that better fit herbarium sheets. Dendrothrix is characterized by staminate flowers with two connate anthers (Fig. 4D-E). Rare flowers with three anthers are present on collections of D. condorensis (i.e., Neill & Quizhpe 14939, MO) and D. yutajensis (i.e., Maguire & Maguire 35103, NY). Such flowers have more or less symmetrical androecia, connate filament columns, partial third sepals, and developed pollen, which indicates they may be functional despite being teratological in gross structure (Fig. 4F). The triandrous flowers may be of significance in reflecting the likely plesiomorphic condition for the tribe and the ease of merosity change even in groups that appear fixed. The bract glands are smooth and without pores (Fig. 4B-C). The staminate sepals bear stomata and are externally minutely papillose (Fig. 4A). The pollen of Dendrothrix ( Fig. 4G; Esser 1994) is tricolporate with a perforate exine, which closely resembles that of other Hippomaneae (see Park and Lee 2013). Seed variation occurs among the taxa of Dendrothrix (Fig. 3A-D) with a wider, more globose seed in D. multiglandulosa, and a well-developed caruncle in D. wurdackii. In D. yutajensis the caruncle is small, and there is no caruncle in D. condorensis or D. multiglandulosa. The 13 available seeds of D. condorensis from dehisced fruits (some slightly immature; note lighter brown coat in Fig. 3B relative to other samples) do not show evidence of caruncle growth (Fig. 3F), while all seeds that I examined of D. yutajensis have a small caruncle.
Dendrothrix has a noteworthy Guiana Shield disjunct distribution (Fig. 1), which now combines two patterns with its over 1000 km distant outliers including elements in both the Andean (i.e., D. condorensis) and Amazon (i.e., D. wurdackii) phytogeographic regions. Such a tripartite distribution does not appear to be shared with other Guiana Shield near-endemic plant genera, although many have disjunct species in just one of those regions (Berry and Riina 2005). Raveniopsis Gleason (Rutaceae) also has a distribution of Guiana Shield endemics and two Brazilian Amazon lowland outliers, and interestingly, one of the few localities of D. wurdackii (Calderón et al. 2682, NY) is also the type locality for one of those outliers, Raveniopsis campinicola Kallunki (Calderón et al. 2722, US).