MATERIALS AND METHODS

Morphological data was initially measured solely on the type material. In search for additional and potentially overlooked material, the following Peruvian and other herbaria were consulted: CPUN, CUZ, F, HAO, HOXA, MO, PRG, USM, QCA(^{Thiers, 2021}). This search yielded no unambiguous additional collections of the new species. The type locality was visited repeatedly and photographs and additional data were taken in situ to record intraspecific morphological variation, however no additional herbarium material was collected. Vegetative organs (leaves, petiole, floral peduncle, tubers and traps) and reproductive organs (flowers and fruits) were collected and preserved in liquid (70% ethyl alcohol or AFA), the liquid material was later dried and added to the paratype specimen. Micromorphology was studied using a stereoscope (Motic SMZ-140) and stereomicroscope (Olympus CX22). The morphological description and its terminology follow ^{Taylor (1989}). For the distribution map of the species of sect. Orchidioides native to Peru, the following online databases were consulted and data was completed with authors’ personal field observations: gbif.org, tropicos.org, inaturalist.org, atrium.andesamazon.org, collections- botany.fieldmuseum.org.

TAXONOMIC TREATMENT

Utricularia amotape-huancabambensis sp. nov.

T. Henning, E. Rodr. & J.P. Allen. TYPE: Perú, Amazonas, Bongará, pajonales de arena blanca, hierba unifolia con bulbos transparentes y rizomas entre los musgos, con flores color blanco con dos líneas amarillas en el centro, 2200 m s.m., 6-III- 2020, J. P. Allen & L. Rimarachín C. 1 (holotype HUT-60473). Figs. 2 A-D, F; 3 A-B, G-M and 4.

Diagnosis

Utricularia amotape-huancabambensis belongs to Utricularia section Orchidioides and is closely related to U. unifolia. It differs from it by having a more robust habit, a broadly ovate to rounded leaf lamina, longer petioles and inflorescences, much larger flowers with a white or slightly lavender corolla and an upper lip slightly longer and wider than the calyx. The spur is terminally curved downwards.

Fig. 2 Utricularia amotape-huancabambensis. A, leaf with petiole. B, leaf lamina. C, flower width. D, flower length. E, leaves of U. amotape-huancabambensis (i), a potential hybrid (ii) and U. unifolia (iii) from the same locality. F, comparison of adult plants of the two species. G-I, flower of U. unifolia, with the typical narrower, violet corolla and the single-bend spur. All photographs by J. P. Allen. Color version at http://www.ojs.darwin.edu.ar/index.php/darwiniana/article/view/955/1230 

Description

Terrestrial herb, relatively robust, perennial, up to 80 cm tall. Rhizoids absent. Stolons few, linear- filiform, loosely branched, irregularly spaced branches, up to 50 cm, 0.5-1 mm diam. Tubers ellipsoid, translucent, attached just below petioles and peduncles or attached sparsely on stolons, single or in pairs, up to 1 cm diam. Leaves 1-2 from the peduncle base, long-petiolate, petioles terete, slightly grooved at the base of the lamina, 24-40 cm, 1-1.5 mm diam., the lamina broadly ovate to rounded, glabrous, margin entire, sometimes slightly sinuous, with the base acutely cuneate to long attenuated, sometimes asymmetrical, and apex slightly acute to obtuse, mostly 5-7.5 × 4.1-6.5 cm, 0.8-1 mm thick, multi-veined, coriaceous, brittle. Traps numerous on capillary stolon branches, globose, subsessile, 0.5-1 mm diam., the mouth basal with two reflected dorsal subulate appendages. All vegetative parts, leaf veins, petiole bases and flower peduncles, tubers and traps covered with scattered globose-cylindrical glands. Inflorescence erect or spreading, 40-80 cm, solitary; peduncle terete, glabrous, 1.5-2.2 mm diam. The scales usually sparse, sessile, generally narrowly elliptical, often falcate, acute, 3-4 × 0.6-0.8 cm. Bracts similar to the scales, 3-4 cm, but often slightly wider, 0.6-1 cm wide. Bracteoles usually somewhat smaller than the bract, up to 1.5-2 cm. Flowers 1-3, the raceme lax, with the internodes 3-3.5 cm; pedicels filiform, narrow-winged, 2-2.5 cm. Calyx lobes subequal, widely ovate, with the base slightly cordate and the apex acute, greenish-purple, multi-veined, 2.3-3 × 1.6-2.1 cm. Corolla 4-6 × (4-) 5-7 (-8) cm, white or slightly lavender with two elongated yellow spots at the base of the lower lip, sparsely stipitate- glandular; upper lip ovate, with rounded apex, the basal sac with a distinctive raised marginal rim, slightly longer and wider than the calyx; lower lip limb subcircular in outline, the base with a conspicuous rounded swelling, the apex rounded or retuse, irregularly lobed; palate with a pubescent, slightly raised, marginal rim; spur subulate, white, about as long as, or longer than the lower lip, located in a long cavity, curved upwards towards the lower lip, apex acute, turned downwards. Filaments 2, curved, thickened at the apex, 4-5 mm, the anther thecae distinct. Ovary globose, 2-2.5 mm diam.; style short, thick, 1.5-2 mm; stigma lower lip quadrate, the upper lip much smaller, deltoid. Fruit not seen.

Etymology

The name refers to the Amotape-Huancabamba Zone, the area around the Huancabamba depression, a partial interruption of the Andean mountain range by the Chamaya river drainage system, which occupies large parts of northernmost Peru and the southern tip of Ecuador (Fig. 1). The mosaic landscape in this region is characterized by a remarkable diversity in different habitat types and a corresponding exceptional zoo- and phytodiversity. In particular, the high rate of narrow endemism concentrated in this relatively small area is intriguing and has led to the idea to consider this area a phytogeographical zone of its own right (such as e.g. the Capensis). “A sizable part of Andean biodiversity seems to be concentrated into this relatively small area, which makes effective protection of the diverse habitats of this zone a high priority” (^{Weigend, 2002}). The name of this new species has been chosen to reinforce this demand and encourage Peru and Ecuador to intensify the urgent conservation efforts for the remaining habitats in this otherwise highly fragmented landscape. Both climate change and urban sprawl are massive threats especially to the remaining forest patches. They are home to an unparalleled diversity of flora and fauna, the known extent of which is here complemented by this emblematic species of flowering plant. The name is intended to serve as a hortatory reminder of the unabated destruction of irreplaceable biodiversity in areas such as the Amotape-Huancabamba Zone (^{Karger et al., 2021}) that are both: heavily overexploited while still underexplored.

Affinities

The new species is closely allied to other Andean Utricularia from section Orchidioides, in particular to sympatric (syntopic) U. unifolia. Initial considerations that it might be an aberrant local form of U. unifolia were rejected due to the considerable and consistent differences in leaf and flower morphology and overall size of the plants (Figs. 2, 3). Utricularia unifolia is widespread, well documented and a “quite distinct species” (^{Taylor, 1989}: 124), although morphological variation to a lesser extent has been reported (Taylor, 1989; pers. obs.).

Fig. 3 Utricularia amotape-huancabambensis. A, flowering plant, growing fully exposed to sunlight with upwards- bended, shield-like leaf. B, ditto, flower in front-lateral view. C-F, flower of a plant growing in the shade with thinner corolla and greenish calyx. G-H, inflorescence of the typical form. I-J, leaves growing out of the moss cushions. K, tuber. L, utricle, frontal view. M, utricle, lateral view. All photographs by J. P. Allen. Color version at http://www.ojs. darwin.edu.ar/index.php/darwiniana/article/view/955/1230 

Remaining doubts were allayed after the discovery of hybrid individuals in syntopic populations of U. unifolia and U. amotape- huancabambensis. These hybrid plants represent morphological intermediate individuals and indicate a secondary contact of the two taxa. The presence of hybrids underlines the distinctiveness of the new taxon and therefore its status as a valid species, as well as its clear affinity to U. unifolia as the potential closest sister taxon.

Putative deciduous (^{Taylor, 1989}) Utricularia endresii, that occurs from Central America to Ecuador, also has large, lavender to whitish flowers and has been reported to ascend into similar altitudes at its southern distribution limit in Ecuador. However, it is characterized by a dense glandular corolla, a leaf morphology and texture similar to that of U. unifolia (narrowly oblong and thin, membranous when dried; Taylor, 1989) and is supposed to be adapted to (seasonally) drier habitats where it loses its foliage to survive the dry season in dormancy. It cannot be confused with the new species and any other Andean Utricularia. Also, U. amotape-huancabambensis shows some similarity to U. praetermissa from Central America. Both species share the basic flower morphology with double-curved spurs and a usually white corolla. Furthermore, the leaves of both species show a prominent venation and are relatively thick compared with those of other members of the section Orchidioides sensu Taylor (1989). These characters are shared with U. unifolia, indicating a possible closer relationship of the three taxa. Utricularia amotape-huancabambensis, however, is generally much taller than U. praetermissa and detailed flower and leaf morphology differ as does their distribution.

The other two members of section Orchidioides present in Peru, U. jamesoniana and U. asplundii, show more affinities to each other (e.g. tri-partite lower corolla lip; ^{Taylor 1989}) than to U. unifolia and the new species, and may be considered more distantly related. The sheer size of U. amotape- huancabambensis (leaves > 40cm) and especially the length of the inflorescence (>80cm) with the huge, almost white flowers that can potentially reach a diameter up to 8 cm, make this species readily apparent and unmistakable from any other species of sect. Orchidioides and in fact any other species of Utricularia. Similar plant sizes are only reached in the U. nelumbifolia - U. reniformis A. St.-Hil. - U. cornigera complex (= sect. Iperua sensu Taylor), but the leaf morphology and distribution (lowlands of eastern Brazil) of these taxa differ greatly.

Distribution

The new species inhabits the páramo of the sandstone rock plateaus (white sands) of the sub- Andean mountain range of low elevations defined as the continuation of the southern branches of the Cordillera del Condor, located in central-northern Peruvian Andes (Fig. 1). The whole area lies well inside the so-called Amotape-Huancabamba Zone (^{Weigend, 2002}, 2004), a biodiversity hotspot that spans from the pacific coast to the slopes of the eastern Andes of southern Ecuador and large parts of northern Peru. This area is particularly rich in phytodiversity and has been retrieved as one of the centers of diversity for many plant groups (Weigend et al., 2005a; ^{Struwe et al., 2009}; Muttke et al., 2014; ^{Böhnert & Weigend, 2017}; ^{Deanna et al., 2018}; ^{Escobar et al., 2018}). Moreover, this area is characterized by an exceptionally high percentage of (narrow) endemisms, even for plant groups that are not exclusively Andean or particularly rich in endemic taxa. This has only recently been shown for the Lentibulariaceae with the description of Pinguicula rosmarieae^{Casper, Bussmann & T. Henning (Casper et al., 2020}). This species is narrowly endemic to the very moist eastern Andes in the department San Martín in north Peru, whereas most other species of this genus are rather widespread. The same seems true for the new Utricularia species described here. Whilst all closely allied taxa show a considerable distributional range, U. amotape-huancabambensis is so far known only from two nearby populations. Although it cannot be ruled out that the true range of the species is much larger than initially assumed, it seems unlikely that such a striking species had been overlooked in a much wider area. Another similarity to the situation observed in Pinguicula L. in the Amotape-Huancabamba Zone is the fact that the narrowly endemic taxon occurs sympatric with a widespread related species and both are separated by contrasting habitat requirements only.

Fig. 4 Utricularia amotape-huancabambensis. A, habit. B, leaves. C, inflorescence. D, flower, frontal view. E, flower, lateral view. F, calyx. G, stamen and pistil. H, utricle. Drawing prepared by Olivia Mendoza. 

In Pinguicula, the newly described P. rosmarieae is only found in open, permanently wet situations, whereas sympatric P. calyptrata Kunth is often found in the undergrowth in shrubby grasslands without constant water flow (^{Casper et al., 2020}). In Utricularia, a similar situation can be observed, with U. amotape-huancabambensis preferring drier sites than sympatric U. unifolia.

Habitat

Utricularia amotape-huancabambensis has been found in two habitat types, both dominated by the characteristic short-growth sclerophyllous vegetation typical for páramo habitats. At the type locality, the species inhabits a specific micro habitat niche hidden within the generally drier area. This landscape is mostly dominated by small shrubs and grasses with full sun exposure from late morning to late afternoon. Utricularia amotape- huancabambensis is extremely common here whereas U. unifolia is absent and this could be due to the extreme abundance of Sphagnum at this site. The second locality consists of a rock wall seepage surrounded by dense humid cloud forest. The site receives full sun exposure from midday to mid/ late afternoon. The majority of the rock wall face is covered by a constant seepage of water, however, the extremities of this site are drier due to the lack of water seepage. Utricularia unifolia dominates this locality within the seepage areas, whereas U. amotape-huancabambensis is almost absent in the seepage areas and prefers the slightly drier sites of the extremities of this microhabitat. Sphagnum (L.) is present in this site, but with low population density and U. amotape-huancabambensis seems to almost exclusivelyprefertheseareaswhereSphagnumoccurs (Fig. 3 I, J), whereas U. unifolia tends to prefer situations where Sphagnum is not present. The lack of Sphagnum cushions could explain the rarity of U. amotape-huancabambensis here. At this site, we have identified a natural hybrid between U. unifolia and the new species.

Ecology

Utricularia amotape-huancabambensis sends out very long running stolons through the Sphagnum cushions and the deteriorating vegetation on the soil surface. Rarely, it was found growing on bare rock, where the stolons had penetrated cracks in the rock surface, but these plants showed very stunted growth. Utricularia amotape-huancabambensis usually grows beneath the cover of surrounding vegetation, sending out new growing points as stolons up to 50 cm long and petioles up to 40 cm long to reach sunlight; both likely adaptations to thrive in dense, fast growing vegetation such as Sphagnum cushions. Another interesting observation in this context is that the petioles often grow in a horizontal direction away from the hillside and then gradually curve back upwards before forming a round, slightly folded leaf, giving the appearance of an almost upside down growth habit (Fig. 3 A, I- J). This growth habit is very unusual and has not been reported for U. unifolia or other taxa of section Orchidioides.

Phenology

Similar to the related Andean species, the plants likely flower throughout most of the year. However, the sites have been visited only in March and December, during the rainy season and flowering plants could be observed at both occasions. It is most likely that they at least flower throughout all months of the rainy season (November to April) and possibly to some extent into the dry season. Fruiting individuals were scarce, indicating some seasonality with a possible flowering break during the dry season.

Associated flora

The new species was seen in association with herbaceous and shrubby vegetation: Dillandia subumbellata V.A. Funk & H. Rob. (Asteraceae), Baccharis reticulata (Ruiz & Pav.) Pers. (Asteraceae), Clethra sp. (Clethraceae), Weinmannia sp. (Cunoniaceae), Ericaceae, Symbolanthus sp. (Gentianaceae), Miconia sp. (Melastomataceae), Escobedia grandiflora (L. f.) Kuntze (Orobanchaceae), Elleanthus sp., Sobralia sp. (Orchidaceae), Asplundia sp. (Cyclanthaceae), Paepalanthus planifolius (Bong.) Körn. (Eriocaulaceae), Lycopodiella cernua (L.) Pic. Serm. (Lycopodiaceae), Sticherus cf. bifidus (Willd.) Ching (Gleicheniaceae), Polypodium sp. (Polypodiaceae), Frullania sp. (Frullaniaceae) and Sphagnum sp. (Sphagnaceae). Besides U. unifolia, another species of Utricularia is present in the habitat with two different forms.

The typical form of Utricularia subulata L. could be detected at the base of the hillside (where U. amotape-huancabambensis is not present) in a permanently waterlogged site and its cleistogamous dwarf form (^{Taylor, 1989}) was found growing in and amongst U. amotape-huancabambensis high up on the steep hillside.

Hybridization

As mentioned above, hybrid individuals were found in one of the two known populations of U. amotape-huancabambensis. At this locality, U. unifolia grows syntopic and it is not surprising that crosses between the two closely related species occur. There are a number of successful hybridizations reported from cultivated species of Utricularia in general and sect. Orchidioides in particular (^{Studnička, 2005}, 2006). Natural hybrids, however, have so far not been reported for members of the section and generally seem rather rare in the whole genus (^{Taylor, 1989}). However, hybridization is common in other Andean plant groups and likely plays an important role in speciation processes, especially in younger lineages (^{Ackermann et al., 2008}). The assumption that the recently described U. cornigera is in fact a natural hybrid between U. nelumbifolia and U. reniformis (^{Fleischmann, 2012}) was later refuted with interbreeding experiments (Studnička, 2013, 2015), which were subsequently supported by molecular data (^{Rodrigues et al., 2017}). The situation observed at the sympatric populations of U. amotape-huancabambensis and U. unifolia, however, also seems more complex than initially thought. At first glance, the striking new species clearly can be differentiated from U. unifolia and the more or less intermediate hybrid individuals (Fig. 2 C-F, 3 E), based on morphological divergence and spatial separation. Upon closer inspection, especially after subsequent comparisons from observations of the putative “typical” plants of U. unifolia in the wild and in herbarium collections, it becomes apparent that this widespread and locally common species not only looks different from the plants categorized as hybrids, but that the majority of U. unifolia at this site differ to some extent and do not fit the morphological spectrum of U. unifolia as currently circumscribed. Whilst the superficial flower and leaf morphology clearly is that of U. unifolia, a large percentage of plants found at the site are more robust, with many plants being generally larger than in any other U. unifolia population seen so far, both in situ and in herbarium collections. Since the divergence observed is a continuum with a fluent transition to the more obvious hybrid individuals, one could speculate that after a hybridization event upon a secondary contact, the hybrid offspring seems to have a competitive advantage and is slowly displacing most of the typical U. unifolia. Both observations, a more robust habit and an increased competitiveness could be explained with the heterosis effect (^{Grant, 1975}). However, it seems quite clear that the continuum in morphological similarity is skewed towards U. unifolia and so seems the repression process. The hybrid individuals can easily be distinguished from U. amotape-huancabambensis, whilst the variability in the other direction is more even, and only a low percentage of “pure” U. unifolia could be found at this spot. A closer examination applying molecular techniques of population genetics is strongly encouraged. The recently recognized collection from Ecuador (see Additional specimens examined) further underscores the need for strengthening the scientific exploration efforts in this part of the Amotape-Huancabamba Zone to better understand the actual distribution of the new species and the species boundaries to its closest relatives U. unifolia and U. endresii whose populations apparently overlap in that area.

Preliminary conservation status

The two known populations of the new species are small and scattered throughout its distributional range. The type locality has a size of approximately 50 × 50 m and the second known population inhabits an area of ca. 100 × 200 m. The number of plants is difficult to assess due to the topology of the sites, but it is estimated to be a few hundred individuals. Anthropogenic pressure on the remaining vulnerable Andean habitats is constantly growing: agriculture, mining activities, and urban sprawl (^{Weigend et al., 2005}b, 2006; ^{Henning et al., 2019}). Moreover, the impact of climate change shows increasing negative effects in that region. Changingtemperatureand precipitations regimes have led to severe wildfires that destroyed numerous forest remnants (^{Mutke et al., 2017}).

The fact that this striking species has not been collected earlier suggests that it is indeed restricted to a number of small, scattered (relic) populations. Hence the species is even more threatened by any potential impact of human interference. Moreover, since its ecological niche seems to be very narrow, in particular in terms of moisture requirements, the negative effects of climate change might be the most immediate threat to the populations as already reported for many other carnivorous plants associated with moist habitats (^{Cross et al., 2020}). Due to the very few collections made so far in this generally under-collected area, one might consider a categorization of this taxon as Data Deficient (DD) according to the IUCN guidelines (2019). However, in the light of the aforementioned observations and assessments, U. amotape- huancabambensis is a very rare, narrowly endemic species occupying a highly specific ecological niche within a region severely threatened by climate change. The province of Bongará and surrounding areas have been comparatively well sampled which is substantiated by the fact that related species of Utricularia have been collected here repeatedly. It is very unlikely that vast populations of U. amotape-huancabambensis have been overlooked, otherwise this striking taxon would have been described earlier or would at least be documented in the local herbaria.

Utricularia amotape-huancabambensis might already be at the brink of extinction and is therefore considered Critically Endangered (CR) based on the criteria A3, B1 and B2. To prevent at least additional pressure by poaching of this potentially highly sought after carnivorous plant for the illegal international trade (^{Cross et al., 2020}), we keep the exact locality information confidential in this paper.

Additional specimens examined

Paratype: PERU. Amazonas. Bongará, pajonales de arena blanca, hierba unifolia con bulbos transparentes y rizomas entre los musgos, con flores color blanco con dos líneas amarillas en el centro, 2200 m s.m., 06-III-2020, J. P. Allen 3 (HUT-60722).

Utricularia cf. amotape-huancabambensis: ECUADOR. Zamora Chinchipe. 2000-2440 m s.m., 26-VI-2014, Pérez et al. 7423 (QCA-235884!). The leaves and flowers of this specimen show a similar morphology, in particular to the plants we consider to be hybrids with U. unifolia, i.e. intermediate in size (inflorescences 40-45 cm), ovate leaves and pale- lavender to violet corolla.

PERU. Amazonas. Condorcanqui, Cordillera del Condor, 2160 m s.m., 31-VII-1994, Beltran 1519 (F- 2177976!, USM!). The collection at F shows a single inflorescence with only the calyx lobes left and without any other organs. It is added here due to the suspicious size of the flower stalk and the suitable collection area.

Key to the Andean and selected similar taxa of Utricularia sect. Orchidioides (modified from ^{Taylor 1989})

1. Corolla lower lip deeply 3-lobed 2

2. Corolla lower lip entire or obscurely lobed 3

2(1). Corolla lower lip very much shorter than the spurU. jamesoniana

3. Corolla lower lip as long as or longer than the spurU. asplundii

3(1). Corolla upper lip broader than long, 2-3 times as wide as the calyx 4

4. Corolla upper lip longer than broad, narrower than, or only slightly wider than the calyx 5

4(3). Corolla densely covered with gland-tipped hairsU. endresii

5. Corolla glabrous or with very few gland-tipped hairsU. alpina

5(3). Corolla upper lip shorter and narrower than the calyx, apex of spur curved upwardsU. unifolia

6. Corolla upper lip wider and longer than the calyx, apex of spur curved downwards 6

6(5). Scales and bracts less than 8 mm, leaves narrowly elliptic with petiole less than 20 cm long. Central America .....

................................................................................................................................................................. U. praetermissa

7. Scales and bracts 3-4 cm long; leaves broadly ovate to rounded, with petiole more than 20 cm long. North Peru ....

.......................................................................................................................................... U. amotape-huancabambensis