Research Article |
Corresponding author: Tilo Henning ( tilo.henning@ark-biodiversity.com ) Academic editor: Yasen Mutafchiev
© 2019 Tilo Henning, Rafael Acuña Castillo, Eric Frank Rodríguez Rodríguez, Luis Felipe García Llatas, Maximilian Weigend.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Henning T, Acuña Castillo R, Rodríguez Rodríguez EF, García Llatas LF, Weigend M (2019) A new striking and critically endangered species of Nasa (Loasaceae, Cornales) from North Peru. PhytoKeys 121: 13-28. https://doi.org/10.3897/phytokeys.121.33927
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Nasa angeldiazioides sp. nov. is described and illustrated. The species is restricted to two forest remnants on the western slope of the northern Peruvian Andes (Dept. Lambayeque) where it is found in the undergrowth of primary forest. The new taxon shows a unique leaf morphology in the family Loasaceae. Molecular and morphological data show that the new species belongs to the Nasa triphylla group. Since the relic forests of the north-western Andes are increasingly threatened by the effects of climate change, i.e. droughts and wildfires, the new species already faces imminent extinction.
Se describe e ilustra la especie inédita Nasa angeldiazioides sp. nov. Esta especie está restringida a dos remanentes de bosque de la vertiente occidental de los Andes del norte del Perú (Depto. Lambayeque), donde se la encuentra en el sotobosque de bosques primarios. Nasa angeldiazioides muestra una morfología foliar única en la familia Loasaceae. Tanto la evidencia morfológica como la molecular muestran que esta nueva especie pertenece al grupo de Nasa triphylla. Dado que los bosques relictos de los Andes noroccidentales del Perú se encuentran cada vez más amenazados por los efectos del cambio climático, como lo son las sequías e incendios forestales más frecuentes, esta nueva especie podría estar enfrentando una extinción inminente.
Loasaceae, Peru, Laquipampa, Nasa, Lambayeque, Amotape-Huancabamba-Zone, narrow-endemic, Chiñama, Angeldiazia, new species
Loasaceae Juss. and its largest genus Nasa Weigend (97 spp.) constitute a prime example for the challenges botany faces today when trying to assess Andean phytodiversity. Nasa has been recognised as the most speciose genus in the family since its segregation from Loasa Adans. (
The latest taxonomic additions to Loasaceae in general and Nasa in particular, have consequently either been discovered in remote areas that were botanically sampled only recently, often following new road cuttings (e.g. Nasa tulipadiaboli T.Henning & Weigend, three subspecies of Nasa rugosa Killip,
The surprising discovery of a conspicuous macrophyte in this area, reveals that there is significant undersampling, even in readily accessible, recognised biodiversity-rich areas of northern Peru. The lack of knowledge of biodiversity may have dire consequences for its survival as recent incidents tragically demonstrate. Contrary to our expectations, governmental monitoring and protection – given the relative proximity to major cities – could not prevent a series of wildfires in several protected areas in northern Peru, as a result of poor agricultural burning practices during a drought in 2016 (
Although detailed information on the extent of the damage varies, it is clear that even areas within official conservation programmes remain virtually unprotected when it comes to drought-promoted and human-induced wildfires.
The habitat, to which the new species is endemic, lies well in the Amotape-Huancabamba Zone (AHZ) in southern Ecuador and large parts of northern Peru (for details see:
The traditional subdivision of Nasa into four Series (Alatae, Carunculatae, Grandiflorae and Saccatae –
The Refugio de Vida Silvestre Laquipampa was established in 2006 and spans an area of 8330 hectares on the western slope of the Cordillera Occidental between 500 and 2500 m a.s.l. It is located in the Department Lambayeque, Province Ferreñafe close to the border with Department Cajamarca. The reserve is mainly covered by seasonally dry tropical forest, with increasingly humid conditions towards the mountain ridges (
The material studied was obtained from the collection locality and is preserved in HUT (Thiers 2018). Stereomicroscopes and light microscopes were used for its study.
Total DNA was extracted from silica gel or herbarium preserved material of 68 species and subspecies of Cornales, using the CTAB method (
Phylogenetic reconstructions were carried out, employing Maximum Likelihood (ML) in RAxML v. 8.1.X (
Peru: Dept. Lambayeque, Provincia Ferreñafe, Distrito Incahuasi, “Refugio de Vida Silvestre Laquipampa”, ruta Piedra Parada, April 2015, L. F. García Llatas 333 (Holotype: HUT, Isotypes: HUT)
Nasa angeldiazioides is similar to N. bicornuta, N. pteridophylla and N. urens but differs in having strongly amplexicaul leaves, sessile to amplexicaul prophylls on the pedicels and flowers with white petals and dark red nectar scales. The unique interrupted bipinnatisect leaves with rounded leaflet apices distinguish N. angeldiazioides from all other taxa of Nasa and Loasaceae as a whole.
Annual herb 30–50 (–110) cm tall. Stem subterete to weakly grooved, 3–9 mm thick at base, pale green with dispersed darker green streaks and dots and whitish protuberances; set with scattered yellowish setae 1–1.5 mm long and covered with medifixed t-shaped hairs, 0.1–0.3 mm. Adventitious roots present in the L-shaped stem base. Leaves alternate, petiolate below (petiole to 10–15 mm), amplexicaul above sometimes with decurrent base, sessile in between; glabrescent; lamina oblong to widely rhomboidal in outline, (80-) 150–280 (-310) mm long and (25-) 60–220 (-280) mm wide (the petiolate leaves smaller than the sessile ones), pinnate at the base and apex, bipinnatisect in the central part, dissected nearly to midvein, central pinnae subpinnatisect, lobules narrowly-oblong; apex acuminate; abaxial surface covered with short, prostrate, yellowish glochidiate hairs, 0.05–0.1 mm and scabrid hairs 0.2–0.3(-0.5) mm along the veins; adaxial surface covered with few scabrid hairs 0.2–0.3 mm long (never on the veins), venation pinnate. Inflorescences of 2–5 terminal or axillary monochasial branches each 10–20 cm long, with (3-) 5–10 (-15) pendent flowers per branch. Flowers borne opposite to an amplexicaul upper leaf, bracts sometimes recaulescent, simple, ovate, margin dentate, sessile, (10-) 15–30 (-33) long and (6-) 10–17 (-25) mm wide, pedicel often provided with a single, ovate, sessile to amplexicaul prophyll, (15-) 20–25 mm long and 12–15 mm wide. Flowers pentamerous, pedicels 30–50 mm, green at the upper half, basally brownish, appearing dessicated, calyx covered densely with scabrid hairs (0.5–0.7 mm) and sparse glochidiate hairs (0.1–0.2 mm), tube conical, 4 × 3 mm, calyx lobes ovate acuminate, 7 × 4 mm, densely covered with scabrid hairs on back. Petals spreading to slightly reflexed, white, deeply cymbiform, cucullate, 15–23 mm long, 5 mm wide and 9–10 mm deep, base green, unguiculate and abruptly widened into two small triangular teeth 2 mm from base, these bent towards the centre of the petal, almost touching each other and leaving only a narrow gap for the stamens, adaxial surface set with scattered scabrid (0.2–0.3 mm) and uniseriate short glandular (3–7 cells) (0.3–0.7 mm) hairs; abaxial surface set with scattered glochidiate (0.1–0.2 mm) and uniseriate short glandular (3–7 cells) (0.3–0.7 mm) hairs. Nectar scales dark red at the base (sacs), white towards the neck and wings, with triangular back, much narrowed above, 7–8 × 4 mm, base incurved, back with two conspicuous, globose nectar sacs about 2 mm in diameter, scale back with 4–5 transversal calli, neck thickened and slightly recurved, laterally protracted into two small erect wings 1 mm long and 0.5 mm wide. Staminodia 9–10 mm long, base slightly dilate, filiform above, papillose, yellowish. Stamens in epipetalous fascicles of 12–15 each, filaments 8–10 mm, white, anthers 0.3 mm long and wide, yellow. Ovary inferior, with three parietal placentae and numerous ovules. Fruit a capsule, horizontal to semi-erect due to the sigmoid pedicel that elongates postflorally, capsule narrowly clavate, slightly curved, purplish, opening with 3 apical valves.
Nasa angeldiazioides adds even more morphological diversity to highly diverse Nasa. In previous taxonomic works (
Nasa angeldiazioides shares the presence of amplexicaul bracts, with several species of the Nasa stuebeliana group (e.g. N. formosissima Fig.
Morphology of Nasa angeldiazioides (A–E, L, M) and similar taxa (F–K). A Flower, frontal view B Flower, lateral view C Capsule, lateral view, note the thin, curved pedicel D General habit of several flowering plants in their natural habitat, Bosque de Chiñama E Mature basal leaf F Mature leaf of Nasa urens G Young plant of N. pteridophylla H Flower of Nasa formosissima, lateral view I Amplexicaul bract of N. formosissima J, K Leaves of Angeldiazia weigendii, abaxial surface, note the overall shape and the ampexicaul leafbase visible in the background L Bract, prophyll and capsules of Nasa angeldiazioides M Lowermost bract of N. angeldiazioides, outlined from a specimen photograph. (Credits: photographs A, B, D B. Esquerre-Ibañez J, K Mario Zapata).
Plastid molecular data, clearly show that this new species belongs to the Nasa triphylla group and is closely related to Nasa pteridophylla and N. humboldtiana (Fig.
Maximum likelihood tree based on a plastid combined dataset (matK, rps16, trnL-trnF, trnS-trnG). ML bootstrap support values are indicated above branches and Bayesian posterior probabilities are indicated below; only values above 50 and 0.5, respectively are shown. Nasa angeldiazioides is marked by a grey rectangle.
The epithet refers to a recently described monotypic genus of Asteraceae from the same area, Angeldiazia weigendii M.O.Dillon & Zapata (
The species was first reported by Santos Llatas Quiroz in May 2007 in the Bosque de Chiñama. Luis Felipe García Llatas collected the species in the Laquipampa Wildlife Refuge in March 2013 in sterile condition (specimen not deposited in a herbarium) and then in April 2015 with flowers and fruits (type collection deposited in HUT). An additional sighting from the Bosque de Chiñama by Boris Esquerre-Ibañez reported full flowering plants in June 2014 (B. Esquerre-Ibañez photographic evidence, no specimen).
The life-cycle of this taxon is strongly linked to the precipitation seasonality and its corresponding inter-annual variation. Annual plant development is mostly affected by the amount of precipitation during the growing season in February and March. Flowering time coincides with other annual taxa of the group in that area, which is typically starting with the end of the rainy- and beginning of the dry season. The length of the flowering period in turn is proportional to the intensity of summer rains during the dry season and can last between some weeks to up to three months depending on overall humidity. Accordingly, fruiting plants can be found from May onwards.
So far, this species is known only from Laquipampa and the neighbouring Bosque de Chiñama (Fig.
The associated arboreal and shrubby species that allow the development of shady, humid microclimates and soils rich in decaying plant matter are the "Pasallo" (Eriotheca ruizii (K. Schum.) A. Robyns, Malvaceae) that, at the time of the collections, show fresh foliage and provide shade to many herbaceous species around, as well as Clusia sp. (Clusiaceae), Bauhinia weberbaueri Harms (Fabaceae), Tecoma sp. (Bignoniaceae) and “San Pedro” (Trichocereus pachanoi Britton & Rose, Cactaceae). The accompanying ombrophile herbaceous taxa include Cranichis sp. (Orchidaceae), Callisia monandra (Sw.) Schult. & Schult. f. (Commelinaceae), Dioscorea sp. (Dioscoreaceae), Commelina sp. (Commelinaceae) and Oxalis sp. (Oxalidaceae).
No pollinator observations are available for this species, but based on flower morphology, it likely falls into the group of taxa predominantly pollinated by rather specialised short-tongued bees (
Nasa angeldiazioides has only been reported from two relic forests in close proximity whose areas occupy less than 200 km2. Given the relatively easy accessibility and the comparatively good knowledge of the floristic inventory of the region in general, it is rather unlikely that vast populations have been overlooked in adjacent areas. Furthermore, this taxon is found as part of the undergrowth flora of otherwise intact primary forests. Unlike closely related taxa that are frequently found in open, disturbed situations, such as roadsides or field margins (N. pteridophylla, N. bicornuta) or in the undergrowth of secondary vegetation and for example, coffee plantations (N. humboldtiana subspp.), N. angeldiazioides seems dependent on native vegetation and is incapable of thriving in habitats that are subject to change caused by human activities. Due to its very restricted known range, small populations (L. García Llatas, B. Esquerre-Ibañez, pers. obs.) and the serious environmental threats (wildfires, deforestation, agriculture) that the whole north-western slope of the Western Cordillera of Peru faces, we consider this species as Critically Endangered (CR B1a,biv), according to the IUCN threatened species assessment guidelines (
Although reported twice from the Bosque de Chiñama, the taxon has so far only been collected in Laquipampa. Only the type collection from 2015 is deposited in the Herbario de la Universidad Nacional de Trujillo (Herbarium Truxillense, HUT).
Thanks are due to Boris Esquerre-Ibañez (Chiclayo) for sharing information and photos of the new species from the Bosque de Chiñama and Michael O. Dillon and Mario Zapata for providing photos of the leaves of Angeldiazia weigendii. Esteban Jiménez (USJ) and Barry Hammel (MO) provided access to valuable material or accompanied us in the field. We acknowledge support by the German Research Foundation and the Open Access Publication Fund of the Freie Universität Berlin.
List of taxa sampled for the molecular analyses with their respective voucher specimen (herbarium acronyms in parentheses), geographic origins and GenBank accession numbers
Data type: molecular data