Hylaeaicum (Ule ex Mez, 1934: 40 ) Leme, Forzza, Zizka & Aguirre-Santoro

Leme, Elton M. C., Zizka, Georg, Paule, Juraj, Santoro, Julián Aguirre-, Heller, Sascha, Ramírez-Morillo, Ivón M., Halbritter, Heidemarie, Mariath, Jorge E. A., De, Jordano D. T. & Forzza, Rafaela C., 2021, Re-evaluation of the Amazonian Hylaeaicum (Bromeliaceae: Bromelioideae) based on neglected morphological traits and molecular evidence, Phytotaxa 499 (1), pp. 1-60 : 45-48

Hylaeaicum (Ule ex Mez, 1934: 40) Leme, Forzza, Zizka & Aguirre-Santoro , gen. et stat. nov.

Basionym:— Aregelia subg. Hylaeaicum Ule ex Mez , in Engler Pflanzenr. IV. 32: 40, 52. 1934. Lectotype ( Smith & Downs 1979: 1533):–– Nidularium eleutheropetalum Ule.

≡ Canistrum sect. Hylaeaicum Ule , Verh. Bot. Ver. Prov. Brandenburg 48: 133. 1907; nom. nud.

≡ Nidularium subg. Hylaeaicum Ule ex Mez , in Engler Pflanzenr. IV. 32: 52. 1934.

≡ Neoregelia sect. Amazonicae L.B. Sm. , Phytologia 15: 191. 1967.

≡ Neoregelia subg. Hylaeaicum (Ule ex Mez) L.B. Sm. & R.W. Read , Phytologia 33: 441. 1976.

Description:— Plants epiphytic, homogamous, stemless, but offset distinctly stoloniferous; stolons slender to stout, 10–40 × 0.3–2 cm, covered by distinct cataphylls; cataphylls triangular, acuminate, usually stramineous, entire to spinulose, often persistent, or sometimes decaying with age, densely arranged and distichous or subdensely arranged, and somewhat polystichous. Leaves coriaceous or thick-coriaceous, forming water impounding rosettes; sheaths distinct, contrasting in shape with the blades; blades lanceolate to sublinear, the upper ones around the inflorescence often turning reddish, bright red, pink or purplish, to form a colorful ring, or sometimes concolorous, slightly if at all narrowed at the base, margins spinose to spinulose. Peduncle distinct, shorter to equalling the length of the fertile part of the inflorescence. Inflorescence compound or sometimes simple, densely corymbose, capitate, sunken in the leaf rosette slightly above accumulated water-level, to partially surpassing leaf sheaths especially at the end of flowering, distally flattened or slightly rounded; primary bracts resembling the upper peduncle bracts; primary fascicles to 12 in number, subsessile to bearing a distinct but short and complanate stipe, more or less flabellate to elongate-pulvinate, sometimes immature and inconspicuous at the beginning of anthesis and with delayed development, sometimes bearing 1–2 secondary fascicles; floral bracts oblong or lanceolate, membranaceous, hyaline toward the base, green near the apex, slightly exceeding the ovary to nearly equaling the sepals. Flowers diurnal, usually scentless, pedicellate; pedicel inconspicuous, merging with the slender ovary and not contrasting in shape with it; sepals slightly to distinctly asymmetric, glabrous to lepidote, apex acute, acuminate to mucronulate, connate at the base to 1/2 of their length, all sometimes carinate, entire, keels decurrent on the ovary; petals narrowly sublinear-spathulate, sublinear-lanceolate to narrowly lanceolate, acute to acuminate, (5-) 6–10 times longer than wide, free, white, the distal 1/3 to 1/4 of its length suberect or spreading-recurved at anthesis, becoming flaccidescent with involute margins to sometimes spiralled afterwards, appendaged or unappendaged but bearing well-developed lateral callosities sometimes with inconspicuous, shortly caudate, distal prolongation equalling the base of the free portion of the filament, or bifid at the distal end, to exceeding the anthers; appendages oblong or narrowly spathulate, highly adnate to the petals, the short free lobes equalling the free portion of the antepetalous filaments, apex sparsely and shortly digitate to densely and slenderly long digitate to fimbriate; stamens usually equalling the middle of the petals, deeply included and not visible to partially visible at anthesis; filaments equal in length, slightly to distinctly complanate and sometimes dilated toward distal end, the antepetalous ones highly adnate to the petals for 1/2 to 4/5 of their length, the antesepalous ones free; anthers oblong, obtuse at the base, apex apiculate to acuminate or rarely obtusely bilobed, dorsifixed slightly below to slightly above the middle, the distal portion above the connection point of the filament sometimes sterile, resembling a flattened lobe or appendix; pollen biporate, ellipsoidal, (40-) 50–65 µm, perforate to broadly reticulate, reticulum coarse proximally with thick muri and broad lumina, pores small, smooth or rarely with inconspicuous and sparse exine elements; ovary narrowly clavate to oblong, trigonous to slightly complanate, sometimes alate-carinate as a continuation of the sepal keels, glabrous, 3–6 times longer than wide; epigynous tube inconspicuous; ovules few in number, ovoid, long caudate; placentation apical; stigma conduplicate-spiral, slenderly subcylindrical to subcapitate, or simple-dilated, broadly infundibuliform, with tendency to conduplicate, white, about equalling the anthers, lobes erect to spreading, margins crenulate to lacerate, inconspicuously to distinctly and densely papillate. Fruits baccate, slightly enlarged from the ovary, narrowly clavate to narrowly ellipsoidal, sometimes slightly complanate, 14–37 × 3–6 mm (not including the sepals), white or bluish, with the persistent attached sepals blue, dark blue, greenishblue or bluish-purple, fruits and flowers often coexisting; seeds narrowly fusiform, slenderly bicaudate when mature and fresh, 4–28 in number per fruit, 3.5–6 × 1–1.8 mm not including the appendages; appendages 3–40 mm long, membranaceous, translucent, the one of the micropylar end longer to shorter than the chalazal one.

Distribution and habitat:—Species of Hylaeaicum are typically epiphytes in the lowland Amazon Forest (see biogeography section above), at 50-400 m elevation, and also in some Amazonia related habitats, like the “islands” of sandy enclaves, in the midst of the ‘ocean’ of the Amazon rainforest, covered by a more open, shrubby or low-tree vegetation known as Campinas and Campinaranas, where they may grow exceptionally as a terrestrial on the sand (e.g., H. eleutheropetalum in Amazonas, Brazil). Hylaeaicum reaches the highest elevation habitats westward on the eastern slopes of the Andes in Ecuador and Peru, inhabiting epiphytically montane forests to 1200 m elevation. Similar range and habitat preference are also observed for some Amazonian Aechmea of the “Streptocalycoid complex” [i.e., Aechmea vallerandii (Carrière) Erhardt, Götz & Seybold (2008: 1825) and related species]. This geographical overlap includes Aechmea aculeatosepala , segregated from Hylaeaicum by Leme (1997), but in sister position of Hylaeaicum ( Heller 2018, this study), an endemic species to even higher elevated habitats in Peru, 1000 m elevation, and Ecuador, 1350-1600 m elevation.

The geographical Amazonian range of Hylaeaicum reveals a clearly distinct pattern when compared to all members of the “Nidularioid complex” s.str. (i.e., excluding Canistrum and related members of the “ Gravisia complex”), which are typically endemic to eastern Brazil, except for two non-Brazilian species of Neoregelia ( N. cathcarthii and N. johnsoniae , from Venezuela and Peru, respectively) which are morphologically closely related in all aspects to the typical Neoregelia (figs. 2, 3). However, these two species have never been recollected after type collection, raising doubts on the accuracy of their geographical origin.

Etymology:—The name Hylaeaicum is based in the word “Hylea” (or “Hylaea”), which is a reference to the vast South-American Amazonian pluvial forest.

Distinctive characters:—When compared to Neoregelia s.str., in which Hylaeaicum was historically included as a subgenus, it differs by the (a) densely corymbose inflorescence (vs. usually umbellate or rarely corymbose), usually surpassing leaf sheaths and partially to distinctly situated above the accumulated water-level in the central tank [vs. positioned below the accumulated water-level (petals excluded) or slightly emerging from it ( fig. 9 G to M)]; (b) inflorescence often with coexisting flower and ripe fruits due to the late development of dormant flower buds (vs. not coexisting or exceptionally coexisting in one species with many-flowered inflorescence, but not due to the late development of dormant flower buds); (c) flowers obscurely pedicellate with the inconspicuous pedicel merging with the slender ovary and not contrasting in shape with it [vs. distinctly pedicellate with pedicel sharply contrasting in shape with the ovary (fig. 11 L to S)]; (d) petals appendaged or unappendaged (vs. always unappendaged); (e) ovules slenderly long caudate at the chalazal end (vs. exappendiculate or rarely inconspicuously and obtusely caudate); (f) stigma conduplicate-spiral or simple-dilated with tendency to conduplicate (vs. always conduplicate-spiral); (g) fruits white, bluish to dark blue with bluish to dark blue attached sepals [vs. white, dark red or rarely yellow with green or red attached sepals (fig. 20 G to J)]; and (h) seeds slenderly long bicaudate [vs. exappendiculate (fig. 23 A, B, C)].

Hylaeaicum has a closer affinity with Aechmea aculeatosepala , a morphologically unique species (fig. 10 A, B), which is confirmed by its strongly supported sister position to the Hylaeaicum clade in the phylogenetic analysis (fig. 1). However, Hylaeaicum differs from it by its (a) usually compound or pseudosimple, sometimes simple inflorescence (vs. simple); (b) flowers obscurely pedicellate with the inconspicuous pedicel merging with the slender ovary and not contrasting in shape with it [vs. shortly but distinctly pedicellate with pedicel sharply contrasting in shape with the ovary (fig. 12 Y)]; (c) sepals entire [vs. densely spinose (fig. 12 Y)] and always erect [vs. with suberect to nearly spreading apical portion (fig. 12 Y)]; (d) petals acute to acuminate [vs. obtuse-cucullate (figs. 10 B; 13 H)], appendaged or unappendaged [vs. unappendaged (fig. 13 H)]; ovary narrowly clavate to oblong [vs. broadly ellipsoid or obovoid (fig. 12, Y, Z)], glabrous (vs. coarsely castaneous lepidote); and (f) pollen ellipsoidal, biporate [vs. subglobose, prevailing triporate (70%), with some variation from 2 to 4 appertures (fig. 18 L)].

There is no available data on fruits and seeds of the Ecuadorian-Peruvian A. aculeatosepala . However, its ovary presents apical placentation (but not clustered apically) and ovules with a long caudate chalazal appendage (fig. 12 Z, a), suggesting the probability of the retention of this long appendage at the chalazal end of the seeds, while the development of an appendage at the micropylar end by the elongation of the funiculus can not be discarded, although the shorter and broader ovary, with a distinct shape (i.e., broadly ellipsoid or obovoid), is similar to other species with monocaudate seeds (e.g., A. mertensii ).

It is not clear wether there are any other known species close enough to A. aculeatosepala to be considered a morphological relative, or if is the only representative of an unique evolutionary lineage which in a future reorganization of the core Bromelioideae will likely become a monotypic genus. The unusual apical curvature of its spinose sepals (with suberect to nearly spreading apical portion), forming a campanulate calyx, recall the calyx of the mysterious A. campanulata Smith (1957: 316) from Pakaraima mountains in Guyana, a small-sized species which also shares long and slender stolons, white petals with longitudinal callosities, globose pollen, and caudate ovules. The calyx of Aechmea hoppii ( Harms, 1935: 526) Smith (1953: 213) ‒ a large-sized species from Ecuador and Colombia ‒ composed of spinose sepals (fig. 12 e), is also morphologically similar to A. aculeatosepala , but petals have well-developed basal appendages, pollen are psillate, and ovules are obtuse, without any appendage (fig. 12 d). Another species with an unusual campanulate calyx is Ronnbergia campanulata Gilmartin & H. Luther ( Luther 1990: 206) endemic to a high elevated area in Ecuador, but the genus is characterized by chalazal ovule appendage absent or rudimentary (Aguirre- Santoro 2017).

Hylaeaicum shares with Canistrum aurantiacum , the type species of the genus, and C. alagoanum , the same fruit color and shape, as well as the unique bicaudate appendaged seeds, but distinctly shorter appendaged in the latter. Canistrum aurantiacum and C. alagoanum constitute, along with other members of the “ Gravisia clade” and the “ Portea complex”, a clade (i.e., clade M, fig. 1) sister to Hylaeaicum , A. aculeatosepala , and Amazonian Araeococcus clade (i.e., clade N), despite weakly supported. Members of the Gravisia clade, including Canistrum and “ Portea complex”, are characterized, among other characteristics, by the globose and polyporate pollen (fig. 19 C, L), greatly contrasting with the ellipsoidal and biporate pollen of Hylaeaicum (fig. 18 A to K), while A. aculatosepala has prevailingly three apertures [varying in small percentage from 2 to 4 apertures (fig. 18 L)], and Araeococcus has sulcate pollen. Hylaeaicum can be clearly distinguished from C. aurantiacum and C. alagoanum by the (a) inflorescence sunk in leaf rosette but partially situated above the accumulated water-level in the central tank [vs. distinctly elevated above leaf rosette by means of a well-developed peduncle (fig. 10 E)]; (b) peduncle, primary and floral bracts not showy (vs. bright red; upper peduncle bracts and primary bracts involucral); (c) flowers obscurely pedicellate (vs. sessile); (d) petals white [vs. yellow-orange (fig. 10 E)]; (e) petals appendages highly adnate to the petals, the short free blades equaling the basal free portion of the antepetalous filaments, apex sparsely and shortly digitate to densely and slenderly long-digitate-fimbriate, or unappendaged [vs. appendages obtuse, positioned at the basal portion of the petals, many times shorter than the filaments (fig. 13 K)]; (f) pollen ellipsoidal, biporate [vs. globose, polyporate (fig. 19 C)]; (g) clustered apical placentation (vs. median to nearly apical axillary placentation); (h) ovules long caudate at the chalazal end (vs. apiculate to shortly caudate); (i) stigma white [vs. yellowish-orange (fig. 15 N)]; and (j) seeds long bicaudate, with appendages distinctly longer than the seed itself [vs. shorter bicaudate with at least the appendages at the micropylar end shorter than the seed itself (fig. 23 H)].

Species:— Hylaeaicum is composed of 12 species and two varieties.

Figures

FIGURE 9. Inflorescences of Neoregelia. A–F, H, K, M. Neoregelia subg. Neoregelia. G, I–J. Neoregelia subg. Longipetalopsis. L. Neoregelia subg. Protoregelia. A. N. ampullacea from Rio de Janeiro state, Brazil (Leme 9299). B. N. compacta from Rio de Janeiro state, Brazil (Leme 5744). C. N. cathcartii from type locality, Venezuela (Leme 2545). D–E. N. johannis from Rio de Janeiro state, Brazil (Leme 5976). D. Top view with the exceptional concomitant presence of outer ripe fruits and a flower at the inner part of the inflorescence, indicated by arrows. E. Lateral view of fruits after removing floral bracts. F. N. lactea from Rio de Janeiro state, Brazil (Leme 1371). G. N. rubrovittata from Rio de Janeiro state, Brazil (Leme 1865). H. N. pontualii from Rio de Janeiro state, Brazil (Leme 5520). I. N. pernambucana from Pernambuco, Brazil (Leme 4407). J. N. viridovinosa from Minas Gerais, Brazil (Leme 8165). K. N. carolinae from Rio de Janeiro state, Brazil (Leme 9332). L. N. longisepala from Bahia, Brazil (Leme 3049). M. N. concentrica from Rio de Janeiro state, Brazil (Leme 221).