Nepenthes zakriana (J.H.Adam & Wilcock) J.H.Adam & Hafiza

Robinson, Alastair S., Golos, Michal R., Barer, Marc, Sano, Yosuke, Forgie, Jennifer J., Garrido, Diego, Gorman, Chandler N., Luick, Adi O., Mcintosh, Nick W. R., Mcpherson, Stewart R., Palena, Gregory J., Pančo, Ivan, Quinn, Brian D. & Shea, Jeff, 2019, Revisions in Nepenthes following explorations of the Kemul Massif and the surrounding region in north-central Kalimantan, Borneo, Phytotaxa 392 (2), pp. 97-126 : 114-119

3. Nepenthes zakriana (J.H.Adam & Wilcock) J.H.Adam & Hafiza (2006: 434, figs. 3−4) descr. emend. A.S.Rob. &

Golos ≡ Nepenthes curtisii subsp. zakriana J.H. Adam & Wilcock (1998: 151 , fig. XXIIa–b) ( Figs. 9−10 )

Type: —Borneo, Sabah, Mt. Kinabalu, Mamut, 1100 m, 21 January 1988, Adam, Adam & Aliosman 2431 (holotype UKMB, iso- ABD).

− “ Nepenthes stenoperculum ” ined . [annotated on the specimen (Clemens & Clemens) 30980/31092, deposited at BO].

− Nepenthes fusca auct . non Danser Kurata (1976: 48), partim [pl. 13]; [ Phillipps & Lamb (1988: 24), partim [3 figs.]; Phillipps & Lamb (1996: 87), partim [fig. 48]; Jebb & Cheek (1997: 41), partim; Clarke (1997: 87), partim [fig. 57]; Cheek & Jebb (2001: 64), partim; Phillipps et al. (2008: 121), partim [figs. 149–150, 152–153]; McPherson (2009: 346), partim [figs. 183–185]].

− Nepenthes maxima auct . non Reinw. ex Nees [ Kondo & Kondo (1983: 110), partim [1 fig.]; Kondo & Kondo (2006: 121), partim [1 fig.]].

Description 2: —Epiphytic or terrestrial climbing or scrambling shrub, to 3 m tall. Stems of rosettes terete, 0.4–0.6 cm in diameter, internodes 0.5–1.5 cm long; vining stems ca. 0.5 cm in diameter, internodes 6–15 cm long. Leaves of rosettes coriaceous, petiolate, elliptic to obovate, 10–12 cm long, 2.5–4.5 cm wide, apex acute to obtuse, base gradually attenuate into petiole, petiole 1.5–4 cm long, base amplexicaul and sheathing stem by 1/2 to 4/5 its circumference, not decurrent to slightly decurrent for less than 8 mm. Longitudinal veins 2–3 on either side of midrib in outer third of lamina, running parallel to the laminar margin, originating at base of leaf, inconspicuous. Pinnate veins numerous, irregularly reticulate, indistinct. Tendrils ±2 times the length of the lamina, generally 15–20 cm long. Leaves of climbing stems scattered, coriaceous, petiolate, lamina narrowly elliptic to elliptic, rarely obovate, 9–16 cm long, 3.5–5 cm wide, apex acute, base gradually attenuate, petiole 3.5–6 cm long, base amplexicaul, sheathing stem by 1/2 to 4/5 its circumference, not decurrent to slightly decurrent for less than 8 mm. Tendrils ±1.5–2 times the length of the lamina, generally 12–20 cm long, often curling twice. Lower pitchers cylindric to sub-ellipsoid throughout or narrowly 2 The emended description is based on measurements made of herbarium specimens and in situ material, and is provided in order to supplement the incomplete description presented in Adam & Hamid (2006).

ellipsoid in lower half and cylindric above, often narrowing slightly towards mouth, 12–16(–23) cm tall, 3–5 cm wide, with fringed wings 2–3 mm wide, fringe elements to 7 mm long, 3–6 mm apart; peristome oblique, typically wider towards raised neck, neck often recurved forwards over mouth, 3–5 mm wide at front of pitcher, sub-cylindric, slightly flattened, increasingly so towards neck and broadening to 6–8 mm wide, ribs ca. 0.3–0.4 mm apart, teeth minute, ≤ 0.4 mm long. Lid ovate to sub-triangular, 3–5 cm long, 1–1.8 cm wide, margins sinuate, occasionally revolute, abaxial midline rib pronounced, with semi-circular basal keel to 3.5 mm tall, distal part sometimes with apical protuberance 2–3 mm long, bearing ocellate-crateriform glands 0.5–0.8 mm in diameter, abaxial surface of lid with small, scattered, pitted glands ca. 0.2 mm in diameter.Spur simple, 5–8 mm long. Upper pitchers generally infundibular with a prominent ventral gibbosity below peristome, rarely narrowly infundibular throughout, 10–16(–19) cm tall, 4–6 cm wide, wings reduced to prominent ridges, peristome sub-cylindric, somewhat flattened, 2–6 mm wide at front and ca. 1/3 wider at rear, ±horizontal at front, rising sharply towards rear into neck, neck often recurved over mouth. Lid narrowly triangular-ovate, appearing ligulate due to revolute margins, 1.5–3.8(–5) cm long, generally>4.5 times longer than wide, typically 0.5–1 cm wide, abaxial midline rib with pronounced semi-circular basal keel, apex with or without glandular apical protuberance up to 3 mm long bearing ocellate-crateriform glands, same glands sometimes present along abaxial midline rib, small nectar glands present across abaxial surface. Spur simple, filiform, 4–12 mm long. Male inflorescence to ca. 20 cm long, 30–80 flowers, peduncle 3–8 cm long, rachis 9–15 cm long, partial peduncles 2-flowered, pedicels ca. 0.8 mm long, tepals elliptic, 3–4 mm long, 2.5–3 mm wide, apex acute, staminal column 3–4 mm long, anther head 1.5 mm in diameter. Female inflorescence to ca. 28 cm long, 30–50 flowers, peduncle 5–12 cm long, rachis 4–13(–20) cm long, partial peduncles 2-flowered, pedicels 0.8–1.2 cm long, tepals elliptic in shape, 3.5–5 mm long, 2.5–3 mm wide, apex acute, fruit 2.5–3 cm long, seeds filiform, 1.2–1.8 cm long, pale brown. Indumentum variable, consisting of short, simple, rufous to white hairs present on stems, pitchers, leaf margins, abaxial leaf surfaces, abaxial midribs, and on developing foliage, becoming caducous in some plants such that older stems and leaves may appear sub-glabrous, generally denser and more persistent on inflorescences. Colour of stems and leaves green, new foliage sometimes suffused with red, pitcher colouration highly variable, lower pitchers green, grey-green or yellow-green, usually mottled red, purple or black, peristome green, yellow to almost black, typically striated with bands of red or purple, but often of uniform colour, upper pitchers equally variable, externally solid yellow-green or with red to purplish-brown blotches, peristome often striated yellow and red, occasionally wholly yellow or red.

Phenology: —Herbarium specimens of Nepenthes zakriana in flower exist for almost every month of the year, suggesting that flowering may occur at any point in time for a given individual.

Distribution and ecology: — Nepenthes zakriana has been recorded with certainty only from Sabah, and chiefly the Crocker Range ( Fig. 4 ), with Mt. Kinabalu and surrounding areas being its locus classicus. A single, pitcherless specimen from Sarawak’s Gunung Mulu National Park ( (Jermy) 13253) is labelled as N. fusca and resembles N. zakriana (lacking the decurrent leaf bases of N. dactylifera ), but its laminae are broadly elliptic with obtuse apices and abruptly attenuated bases, atypical for the species; more complete material would be needed to confirm the identity of this taxon.

Nepenthes zakriana is generally found at elevations of 1200–2500 m, but occasionally down to 800 m. This species appears to be predominantly epiphytic, but is often observed growing terrestrially above 1300 m, being ruderal at sites like road cuttings and on serpentine rubble, but also occurring on natural humus and moss banks.

Like most Nepenthes , N. zakriana hybridises readily with its congeners. The literature records putative natural hybrids between N. zakriana (under the name N. fusca ) and the following species: N. burbidgeae Hook. f ex Burbidge (1882: 56) on Mt. Kinabalu and adjacent areas such as Mamut copper mine (AR, MG pers. observ., Lowrie 1983); N. lowii on Mt. Alab ( Phillipps et al. 2008; originally identified as N. lowii × N. pilosa Danser (1928: 355) by Clarke 1997) and Mt. Trus Madi ( Fretwell 2013); N. reinwardtiana near Mt. Kinabalu (S. Hirosi pers. comm., McPherson 2009; N. naquiyuddinii Adam & Hamid (2006: 431) may represent this cross, per Phillipps et al. 2008); N. stenophylla Masters (1890: 240) on Mt. Trus Madi ( Phillipps et al. 2008) and Mamut copper mine (AR pers. observ., Thong 2006); N. tentaculata on Mt. Alab ( Phillipps et al. 2008); and N. rajah Hooker (1859: 421) in the Mt. Kinabalu area ( Clarke 1997).

Conservation status: — Nepenthes zakriana occurs widely across the western highlands of Sabah and is found in a number of protected areas including the Crocker Range NP and Kinabalu NP. It qualifies as Least Concern when evaluated against the IUCN 3.1 criteria ( IUCN 2012).

Notes: —The name Nepenthes zakriana is applied to this taxon as it was validly published by Adam & Hamid (2006) to describe type material collected from a well-characterised and representative population of N. fusca sensu Kurata (1976) from Mamut copper mine (Mt. Kinabalu). However, the protuberant apical lid appendage cited by Adam & Hamid (2006) as a key characteristic of N. zakriana cannot be regarded as a reliable diagnostic feature of this species. Different plants within a single population may or may not produce apical appendages, while different pitchers on a single plant can be equally variable—an inconsistency that can be verified at the type locality (AR, MG pers. observ.), as well as on trails around the Kinabalu Park Headquarters, Mt. Alab and Mt. Trus Madi (AR pers. observ.). However, other features (listed in Table 2) including leaf base decurrency, lid morphology, pitcher shape and indumentum make it possible to distinguish readily between this taxon and the closely related N. dactylifera .

Additional specimens examined:— SABAH: Beaman 8178 (K!, L!; photo), Penampang District, Crocker Range, Km 50.7 on Kota Kinabalu–Tambunan Road , 5°50’N 116°19’E, 1600 m, 2 January 1984 [K, L —climbing stem with upper pitcher] ; Beaman 8910 (K! [2 sheets]), Penampang District, Crocker Range , Km 51.8 on Kota Kinabalu– Tambunan Road , 5°50’N 116°20’E, 1500–1600 m, 16 March 1984 [separate leaves and pitchers; pitcherless climbing stem] ; Beaman 9957 (K!, L!; photo), Ranau District, Mamut Copper Mine , 6°02’N 116°39’E, 1600–1700 m, 30 May 1984 [K—climbing stem with upper pitchers, separate lower pitcher; L —leaf with lower pitcher, separate lower pitchers]; (Clemens & Clemens) 30980/31092 ( BO!), single sheet combining two labels: (30980) Upper Kinabalu, Penibukan, near Table rock, left trail, north ridge, 5000 ft [= 1524 m], 16 January 1933; (31092) Mt. Kinabalu, Penibukan, ridge above Kina Taki river , 4000 ft [= 1219 m], 16 January 1933 [climbing stem with upper pitchers, infructescence; “ N. stenoperculum MSC ”—annotation by M.S. Clemens]; (Clemens & Clemens) 31570 ( BO!), two conflicting labels: (1) Mt. Kinabalu, Penibukan , 4000–5000 ft [= 1219–1524 m], 7 February 1933; (2) Mt. Kinabalu, Keebambang river , 4000 ft [= 1219 m], 3 August 1933 [climbing stem with upper pitchers, male inflorescence]; (Clemens & Clemens) 34454 (BO! [2 sheets]), Mt. Kinabalu, Colombon basin, below Keebambang lobang, 3500 ft [= 1067 m], 14 August 1933 [climbing stems with upper pitchers]; (Clemens & Clemens) 50961 (K!), Upper Kinabalu , 7000–8000 ft [= 2134–2438 m], 7 December 1933 [climbing stem with upper pitchers] ; Collenette 815[a] (K!), Royal Society Route [up Mt. Kinabalu], near platform 2 hrs above Base , 5275 ft [= 1608 m], 16 August 1961 [separate leaf and lower pitcher elements] ; Collenette 815[b] (K!), Mt. Kinabalu , eastern shoulder, 4000–5000 ft [= 1219–1524 m], 16 August 1961 [short stem with lower pitchers] ; Collenette 816[a] (K!), Royal Society Route [up Mt. Kinabalu], near platform 2 hrs above Base , 5275 ft [= 1608 m], 16 August 1961 [leaf with upper pitcher] ; Collenette 816[b] (K!), Mt. Kinabalu , eastern shoulder, 4000–5000 ft [= 1219–1524 m], 16 August 1961 [climbing stem with upper pitchers] ; Comber 4031 (K!), Sapong , 3000 ft [= 914 m], no date [climbing stem with upper pitchers, male inflorescences] ; de Vogel 8078 ( L!), West Coast Residency, road Kimanis–Keningau, Crocker Range , on the watershed, 5°28’N 116°03’E, 1500 m, 6 October 1986 [stem with intermediate pitchers] ; Hobbs 17 (K!), Trus Madi , SE ridge, 4500 ft [= 1372 m], 22 August 1977 [pitcherless climbing stem and leaf with lower pitcher] ; Hobbs 18 (K!), Trus Madi , SE ridge, 4500 ft [= 1372 m], 22 August 1977 [short stem with lower pitchers] ; Hobbs 72 (K!), Ranau, Mt. Kinabalu , 5500 ft [= 1676 m], 26 September 1977 [climbing stem with intermediate pitcher, separate lower pitcher] ; Hobbs 73 (K!), Ranau, Mt. Kinabalu , 6500 ft [= 1981 m], 26 September 1977 [short stem with lower pitchers] ; Rickards 101 (K!), Mt. Kinabalu , 5400 ft [= 1646 m], 19 June 1976 [short stem with lower pitchers] ; Rickards 156 (K!), Mt. Kinabalu , 5500 ft [= 1676 m], 20 June 1976 [short stem with lower pitchers] ; RSNB 4377 (Chew & Corner) (K!), Bembangan River , 5000 ft [= 1524 m], 19 February 1964 [climbing stem with upper pitchers, male inflorescence] ; RSNB 4415 (Chew & Corner) (K!), Bembangan River , 5000 ft [= 1524 m], 20 February 1964 [stems with lower pitchers] ; SAN 60818 (Amin et al.) (K!), Tambunan District, Gu. Alab Range , 600 ft [= 183 m] [sic —clearly an error; the elevation of Mt. Alab is ca. 6200 ft (1900 m)], 21 July 1984 [climbing stem with upper pitcher, female inflorescence] ; SAN 82759 (Lantoh) (K!, KEP, L, SAR), Ranau District, Kinabalu Sabah National Park , 6000 ft [= 1829 m], 26 January 1976 [K—climbing stem with upper pitchers, male inflorescences] ; SAN 91184 (Aban & Dewol) (K!, KEP, L, SAR, SING), Beluran District, Bukit Liminintong , 2800 ft [= 853 m], 9 April 1980 [K—short stem with lower pitchers] ; SAN 91185 (Aban & Dewol) (BO, K!, KEP, L, SAR, SING), Beluran District, Bukit Liminintong , 2800 ft [= 853 m], 9 April 1980 [K—climbing stem with upper pitcher, infructescence] ; SAN 121014 (Amin et al.) (K!, L!), Ranau District, Bambangan , no elevation data, 10 September 1987 [K, L —climbing stem with intermediate pitcher] ; SAN 127727 (Fidilis) (K!, L!), Penampang District, Togudon / Tungol Km 48 Jalan Tambunan / Penampang , 1400 m, 14 August 1989 [K—two climbing stems: one with upper pitcher, one pitcherless with male inflorescence; L —pitcherless climbing stem with infructescence] ; SAN 147507 (Suzana) (K!, L!), Ranau, Mamut Copper Mine , 6°20’N 116°40’E, 1200 m, 29 November 2005 [K—climbing stem with upper pitcher, female inflorescence; L —pitcherless climbing stem with female inflorescence] ; Schwallier 60 ( L!), Crocker Range, down main road [from] Alab Station , 5°49’4.09”N 116°20’23.16”E, 1836 m, 24 September 2012 [climbing stem with upper pitcher, male inflorescence] ; Schwallier 61 ( L!), Crocker Range, down main road [from] Alab Station , 5°48’51.2”N 116°20’23.58”E, 1778 m, 24 September 2012 [climbing stem with upper pitcher, female inflorescence (unopened flowers)] ; Schwallier 62 ( L!), Crocker Range, down main road [from] Alab Station , 5°48’52.38”N 116°20’23.82”E, 1764 m, 24 September 2012 [short stem with lower pitcher] ; Schwallier 63 ( L!), Crocker Range, down main road [from] Alab Station , 5°48’52.38”N 116°20’23.82”E, 1764 m, 24 September 2012 [climbing stem with upper pitcher, inflorescence (unopened flowers)]. SARAWAK: (Jermy) 13253 (K!), Gunung Mulu National Park , around Camp 3 [of Royal Geographical Society’s Expedition to Gunong Mulu 1977–78], 1150– 1250 m, 5 October 1976 [pitcherless climbing stem—in the absence of pitchers, the specimen is of limited value] .

Nepenthes stenophylla :— SABAH: SAN 83146 (Cockburn) (K!, L), Lamag District , Inarat, S. ridge of Gunung Lotung, 3000 ft [= 914 m], 15 May 1976 [K—high epiphyte; climbing stem with upper pitcher, lid absent] ; SAN 83251 (Cockburn) (K!, L), Lamag District , Inarat, S. slopes of Gunong Lotong [Maliau Basin], 4300 ft [= 1311 m], 16 May 1976 [K—climbing stem with upper pitcher, infructescence] ; SAN 151747 (Pereira) ( L!), Ranau, west of Bkt. Hampuan FR [Forest Reserve], 6°01’26”N 116°39’41”, 1489 m, 12 May 2010 [climbing stem with upper pitcher, infructescence] .

Notes on specimens examined: — SAN 83251 (Cockburn) was labelled as Nepenthes cf. stenophylla but subsequently identified as N. fusca by Smythies (20/12/1977) and Jebb (9/11/1993) on the sheet. However, the lid, though partially folded, appears complanate and is noted to be as large as the pitcher opening, which is atypical of N. fusca s.lat. —based on extensive exploration of the Maliau Basin, AR, SM and BQ determine that this material represents the diminutive heath-forest form of N. stenophylla found throughout the Maliau Basin above elevations of ca. 1000 m. SAN 83146 (Cockburn) is conspecific with this taxon. SAN 151747 (Pereira), identified as N. fusca by Madani (7/2010), likewise represents N. stenophylla (det. AR & MG), which is widespread at the stated locality.

The isotype of Nepenthes zakriana at the University of Aberdeen Herbarium ( ABD) could not be located despite an extensive search of the collections ; staff indicate that there are no records that it was ever deposited.

Figures

FIGURE 4. Distribution of Nepenthes dactylifera, N. fusca and N. zakriana in Borneo based on accessions held at BO, K, L and SAR herbaria, supplemented by field observations. Drawn by A.S. Robinson.

FIGURE 9. Nepenthes zakriana (J.H.Adam & Wilcock) J.H.Adam & Hafiza. A—climbing stem. B—lower pitcher. C—abaxial surface of lid of lower pitcher. D—upper pitchers, top right Mamut copper mine, bottom left, Mt. Trus Madi. E—abaxial surface of lid of upper pitcher. F—cross section of peristome. G—inflorescence. H—dehiscing seed capsules. Scale bars: A, B, D, G, H = 1 cm, C, E, F = 5 mm. Based on Beaman 9957 and Hobbs 17, and supplemented with photographs and measurements made of in situ material. Illustrated by M. Barer.

FIGURE 10. Pitchers of Nepenthes zakriana. A—lower pitcher (Mamut copper mine). B—lower pitcher (Mt. Trus Madi). C—upper pitcher (Mt. Trus Madi). D—upper pitcher (Mt.Alab). E—climbing stem with pitchers, showing non-decurrent leaf bases (Mamut copper mine). Photographs A–E by A.S. Robinson.