Cololejeunea satioi T.T.G.Takash., Ilk.

Takashima, Tássia Toyoi Gomes, Pócs, Tamás & Ilkiu-Borges, Anna Luiza, 2024, Two remarkable liverworts from human-modified landscape in Eastern Amazonia: Cololejeunea minuscula Pócs and C. satioi sp. nov., Phytotaxa 671 (2), pp. 183-190 : 185-189

2. Cololejeunea satioi T.T.G.Takash., Ilk. -Borg. & Pócs, sp. nov. ( Figs. 2–3 )

Plants autoicous, densely pinnate, with numerous short, fertile branches, including fertile gynoecial innovations. Leaf lobes bordered by 1 row of finger-like cells at apex and 1–4 rows of subquadrate hyaline cells along the dorsal margin, the border continuous to sometimes interrupted between the apex and the dorsal base, where it is constantly developed. Leaf cell walls with distinct trigones, usually with 1–2 intermediate thickenings, cuticle faintly to distinctly punctate. Lobules small, 1/5–1/6 of leaf length.

Type:— BRAZIL. Pará: Irituia, São José do Açaiteua, in the understory of a selective logging forest used by Quilombolas community, on living leaves, 01°40’11.0” S, 47°21’48” W, 27 m, 12 January 2021, T. T. G. Takashima & S. Takashima 1376 (holotype MG, isotype NICH).

Autoicous. Plants 1–1.2 mm wide, yellowish-green, prostrate, strongly adhered to the substrate, growing in sparse mats on living leaves. Branches Lejeunea - type with conspicuous collars, Radula - type on the innovations, densely pinnate with numerous short, fertile, male or female branches. Stems thin, ca. 50 µm in diameter, made up of 5 epidermal cells surrounding 1 medullary cell, all cells thin-walled and uniform in size. Leaves widely spreading, subimbricate to imbricate, ovate, 270–540 µm long, 450–750 µm wide, plane, insertion line short, 4 cells long, dorsal base covering the stem, dorsal margin arched, ventral margin straight to shallowly curved, apex rounded to somewhat obtuse; apical and dorsal margin with a conspicuous border of hyaline cells, apical border formed by 1–2(–3) cell rows, the outer cells rectangular and finger-like, the inner cells quadrate to rectangular; dorsal border formed by 1–4 rows of quadrate to rectangular cells, continuous to sometimes interrupted between the apex and the dorsal base, being constantly present near the base; (non-hyaline) leaf cells near the apex isodiametric to rectangular, 10–20 × 8–20 µm, median cells isodiametric to elongate, 18–30 × 10–20 µm, basal cells elongate, 27–60 × 10–20 µm, cell walls thin at leaf base to the middle, becoming somewhat evenly thickened toward the margins, (0–)1–2 intermediate thickenings, trigones distinct, cuticle faintly to distinctly punctate; oil bodies not seen (degraded). Lobules inflated, triangular-ovate to ovate, small, 1/6–1/5(–1/4) the lobe length, 110–180 µm long, 60–90 µm wide, when well-developed made up of conspicuously elongated cells, attached to the stem by 3 cells, keel straight to slightly curved, free margin curved, shallowly incurved, first tooth erect, (1–)2 cells long, blunt, second tooth 1-celled, blunt, sometimes inconspicuous, separated from the first one by a gap of 1–2 cells, hyaline papilla ental to the base of second tooth. Androecia on short lateral branches, emerging obliquely from the stem, with 2–3 pairs of bracts, 230–310 µm wide, bracts hypostatic, imbricate. Gynoecia on short lateral branches, with one innovation, sometimes fertile, bracts similar in size, ovate, 400–700 µm long, 200–400 µm wide, bracteole lanceolate, 1/4–1/3 the bract length. Perianths obcordate, 400–500 µm long, 300–400 µm wide, with 2 lateral flattened lateral keels and one elevated ventral keel, ventral keel usually folded over the perianth surface, keels smooth, beak inconspicuous, of one row of cells. Vegetative reproduction not observed.

Etymology:— The new species is dedicated to Satio Takashima (in memoriam), collector of the species and father of the first author.

Distribution and habit:— This new species is known only from the type locality in the state of Pará, Eastern Amazonia ( Fig. 4 ). The municipality of Irituia is one of the oldest agricultural frontiers in the Eastern Amazonia, resulting in a landscape highly influenced by human activities and natural habitat loss ( Almeida et al. 2016). The collection site is a forest under selective logging for household uses of landowners. Compared to the natural forest, this forest featured small to medium-sized clearings with abundance of lianas. Cololejeunea satioi was colonizing living leaves of understory treelets together with C. cardiocarpa ( Montagne 1842:476) A. Evans (1902: 172) , a widely distributed neotropical species capable of inhabiting dry environments ( Schuster 1980, Gradstein et al. 2001).

Taxonomic notes:— Cololejeunea satioi belongs to the subg. Pedinolejeunea due to the presence of a shiny hyaline margin in the leaf lobe ( Pócs et al. 2014). It differs from other members of the subgenera by (1) an apical border formed by 1–2(–3) cell rows, of which the outer ones are finger-like (basal cells quadrate to rectangular), and a dorsal border formed by 1–4 rows of quadrate to rectangular cells ending near the insertion line (basal border constantly present); (2) lobules small, less than 1/4 of lobe length, bearing an erect first tooth, (1–)2 cells long, blunt, and a blunt second tooth, 1-celled, sometimes inconspicuous, and the two teeth are separated by a gap of 1–2 cells; (3) leaf cell walls with conspicuous trigones and intermediate thickenings; and (4) cuticle faintly to distinctly punctate.

The new species is closely related to two widely distributed Neotropical members of subg. Pedinolejeunea , Cololejeunea subcardiocarpa and C. verwimpii . All three species have a hyaline border along the apical and dorsal leaf margin, from the apex to the base. In C. subcardiocarpa and C. verwimpii , however, the apical border is formed by a single row of finger-like cells (rarely with quadrate cells at its base), and the dorsal border also consists of a single row of rectangular cells ( Tixier 1980, Pócs et al. 2014), which is not interrupted, instead they fade away toward the dorsal base. In C. satioi , however, the hyaline margin is broader and can also be interrupted between the apex and the base, where it is always well-developed. Occasionally interruptedly hyaline margins are also observed in Cololejeunea bencei Pócs (2021: 418) , an epiphyllous species endemic to submontane wet forest of Venezuelan Guayana ( Pócs 2021). The latter species differs from C. satioi in many ways, especially by lacking finger-like apical cells and by most leaf cells with a rounded papilla on the dorsal cell surface.

Differences between Cololejeunea satioi and C. subcardiocarpa are also seen in the lobule, which is notably smaller in C. satioi (1/6–1/5 the lobe length, rarely smaller) than in C. subcardiocarpa (1/3 the lobe length, rarely larger). Cells of C. satioi have a faintly to distinctly punctate cuticle, while C. subcardiocarpa possesses a completely smooth surface. Besides, C. subcardiocarpa has thinner leaf cell walls, without intermediate thickenings and lacking trigones or having much smaller trigones ( Tixier 1980, Pócs et al. 2014).

Cololejeunea verwimpii clearly differs from C. satioi in leaf shape, being elliptic to obovate with both arched dorsal and ventral margins, and in the smooth cuticle (Pócs 2009). In C. satioi , the leaves are ovate with an arched dorsal margin and an almost straight ventral margin, and the cuticle is faintly to distinctly punctate. Additionally, the lobules of C. verwimpii are made up of isodiametric to slightly elongate cells while in C. satioi , the lobule cells are conspicuously elongate (in well-developed lobules) and rather sinuose.

The type collection of C. satioi was mixed with the common and widespread neotropical C. cardiocarpa , a further member of subg. Pedinolejeunea . Cololejeunea cardiocarpa is readily separated from the new species by the restriction of the hyaline border to the leaf apex, being absent along the dorsal leaf margin ( Schuster 1980, Pócs et al. 2014).

Key to the species of Cololejeunea subg. Pedinolejeunea in Brazil

This key is based on Pócs et al. (2014) with modifications; for illustrations see the latter publication.

1. Leaf lobe apex with finger-like or orbicular hyaline cells (many leaves must be observed) .............................................................2

1. Leaf lobe apex with quadrate, subquadrate or rectangular hyaline cells..........................................................................................10

2. Hyaline cells restricted to the leaf apex..............................................................................................................................................3

2. Hyaline cells not restricted to the leaf apex........................................................................................................................................7

3. Lobule setaceous formed by 4–6 uniseriate cells on a triangular base of 6–10 cells. Ventral merophyte 1 cell wide......................... .................................................................................................................................................................................. C. micrandroecia

3. Lobule not setaceous ..........................................................................................................................................................................4

4. Lobule small, about 1/10 of the lobe length, consisting of 8–18 cells, flat, rectangular or triangular, with unicelled tooth topped by one hyaline papilla. Perianth obovate, keeled, beak short........................................................................................... C. minutilobula

4. Lobule large, at least 1/3 of the lobe length, inflated on almost all leaves, shape various, one or two teeth at the apex. Perianth of various shapes and ornamentation......................................................................................................................................................5

5. Leaf triangular-ovate, with 1–2 finger-like or orbicular hyaline cell at the apex (many leaves must be observed since they are frequently broken). Lobules ovate to ellipsoidal, up to 1/2 the lobe length, 1-celled first tooth (blunt). Perianth wings crenate ....... ...................................................................................................................................................................................... C. panamensis

5. Leaf long-ovate, with a group of finger-like to orbicular hyaline cells at the apex. Lobule ovate to lanceolate, 1/3‒1/2 of the lobe length, with elongate, 2-celled first tooth. Perianth wings entire.......................................................................................................6

6. Leaves ovate, ventral and dorsal margins curved. Lobule broad ovate, 20–50 cells wide. Lobule cells isodiametric. First lobule tooth straight. Male bracts ovate with truncate apex................................................................................................... C. cardiocarpa

6. Leaves triangular-ovate, ventral margin straight, dorsal margin curved. Lobule narrow ovate, 12–14 cells wide. Lobule cells elongate (2–5 times longer than wide). First lobule tooth falcate, turned downwards. Male bracts lanceolate with acute apex ........ ........................................................................................................................................................................................... C. schusteri

7. Hyaline cells form a continuous margin extending to the dorsal border............................................................................................8

7. Hyaline cells interrupted between the apex and the dorsal base ............................................................................................ C. satioi

8. Hyaline finger-like cells gradually change into a row of rectangular ones towards the dorsal lobe..................................................9

8. Hyaline finger-like cells abruptly change into 1‒3(‒4) row of rectangular ones towards the dorsal lobe............................. C. satioi

9. Lobules relatively large, 1/3‒1/2 of the lobe length, inflated, never reduced. Cuticle smooth.............................. C. subcardiocarpa

9. Lobules small, less than 1/4 of the lobe length, inflated or flat, sometimes reduced and triangular. Cuticle smooth to finely striate. .............................................................................................................................................................................. C. verwimpii

10. Lobules small, less than 1/3 of lobe length ......................................................................................................................................11

10. Lobules large, more than 1/3 of lobe length.....................................................................................................................................13

11. Lobule ovate (triangular if reduced). Cuticle conspicuously reticulate (hence lobe cells opaque)............................ C. surinamensis

11. Lobule triangular-lanceolate or trapezoid to triangular. Cuticle smooth or finely punctate.............................................................12

12. Lobules triangular-lanceolate (2× wider than the keel), with 1–2 teeth on the lateral margin. Cuticle finely punctate ...................... .......................................................................................................................................................................................... C. lanciloba

12. Lobule trapezoid or triangular, with 1–2 blunt or obsolete teeth. Cuticle smooth ....................................................... C. subscariosa

13. Hyaline cells concentrate at the leaf apex, forming an abruptly broadening, protruding, multiseriate group ................... C. nigerica

13. Hyaline cells forming a continuous margin extending to the dorsal leaf margin.............................................................................14

14. Lobule mostly wider than long, ligulate or trapezoid (very variable in shape), flat, usually with an obsolete tooth on its lateral margin............................................................................................................................................................................. C. planissima

14. Lobule never wider than long, ovate to long-ovate, inflate, with 1 or 2 distinct teeth on the distal margin....................................15

15. First lobule tooth 2 or 3-celled; second lobule tooth triangular, formed by 2‒4 cells at base tapered by a 1‒2 celled tip .................. ..................................................................................................................................................................................... C. bischleriana

15. First lobule tooth 1 or 2-celled; second lobule tooth triangular, formed by 1 acute cell or obsolete ...............................................16

16. Median lobule cells elongate, 3–4 times longer than wide. First lobule tooth often falcate and bent downwards.......... C. cremersii

16. Median lobule cells quadrate to rectangular, maximally 2 times longer than wide. First lobule tooth straight...............................17

17. Dorsal leaf base auriculate, projecting beyond the stem. Hyaline border extending from the mid-ventral margin to the dorsal leaf base (almost to the insertion). First lobule tooth 2-celled ................................................................................................. C. vitaliana

17. Dorsal leaf base rounded, covering the stem, but not projecting beyond. Hyaline border extending from the apex to the dorsal margin. First lobule tooth 1–2-celled ........................................................................................................................ C. submarginata

Figures

FIGURE 2. Cololejeunea satioi. A. Habit with gynoecia (with perianth and innovation) and androecia. B. Cladographs of fertile plant (circle = gynoecia, dots = androecia). C. Leaves in dorsal and ventral view. D. Lobules. E. Cross section of a stem. F. Leaf in ventral view. G. Leaf insertion (A = 500 µm; C, F = 100 µm; D–E, G = 50 µm; All from the holotype).

FIGURE 3. Cololejeunea satioi. A, B. Leaf cells. C. Hyaline cells from apex. D. Hyaline cells from leaf base. E. Leaf in ventral view (A, B = 25 µm; C, D = 25 µm; E = 100 µm; All from the holotype).

FIGURE 4. Localization of type species of Cololejeunea satioi, in the municipality of Irituia, state of Pará, in the understory of a selective cutting forest used by a traditional community.