Rediscovery of Passiflora danielii Killip , 1960 ( subgenus Passiflora ) : a threatened narrow endemic species of Colombia

Passiflora danielii, an endemic species to Colombia, which is threatened, was rediscovered in the Department of Antioquia, where it has not been reported since 1938. The species was only known from the type locality (Municipality of Cocorná). Now, four new locations are added near it. The current study further presents a revised morphological description of P. danielii based on fresh material, along with an updated distribution map. Finally, following the IUCN Red List Criteria, P. danielii was classified as Critically Endangered (CR) species.

The Passifloraceae comprise 17 genera and approximately 650 species, distributed throughout the tropics from the coastal zones up to 4,200 m in the Andes (Ulmer and MacDougal 2004).Passiflora, with about 576 species, is numerically and economically the most important genus of the family with alimentary, ornamental and pharmaceutical interest (Yockteng et al. 2012).In the most extensive monograph of the genus, Passiflora The American Species of Passifloraceae, Killip (1938) classified 355 species into 22 subgenera, based on floral morphology.More recently, Feuillet and MacDougal (2003) proposed a new infrageneric classification, recognizing only four subgenera: Astrophea (D.C.) Mast., Decaloba (D.C.) Rchb, Deidamioides (Harms) Killip and Passiflora, and downgrading most of Killip's divisions to lower levels.Krosnick et al. (2009) recognized subgenus Tetrapathea (DC.) Green from Oceania, raising the number of subgenera to five.
Passionflowers are generally perennial lianas or herbaceous vines climbing by tendrils, although some are trees, shrubs, or even annuals.Additional, typical vegetative traits include alternate leaves, axillary stipules, and petiolar and/or laminar nectary glands.The subgenus Passiflora includes ca.252 species and exhibits several unique floral features, such as an androgynophore, a complex corona constituted of one or several concentric rows of filaments, and a limen-operculum system limiting access to the nectary chamber, with impressive interspecific variation in size, shape and colors (Killip 1938).Their wide morphological variation appears to result from the diversity of their habitats as well as their coevolutionary relationships with many organisms, including protective ants, herbivores such as Heliconius spp.(Lepidoptera: Nymphalidae), pollinators, and the plant communities providing them physical support and access to sunlight (Yockteng et al. 2012).
Colombia is divided into 32 "departments", administrative units equivalent to provinces or states, and six main biogeographic regions: Amazonian, Andean, Caribbean, Orinoquian, Pacific and Insular.The Andean region presents a highly varied topography (100-5,400 m above sea level) with three main mountain ranges.The uplift of the Andes created new habitats and increased local isolation, favoring high speciation rates in many taxa (Gentry 1986).As a result of this habitat diversification, the Colombian flora comprises one of the world's most diverse groups of vascular plants, with 51,220 documented species (Myers et al. 2000;Kreft and Jetz 2007).However, Colombia has undergone recent transformation of large portions of its natural ecosystems, in particular in the Andean region due to development of agriculture and extensive livestock production, mining, hydroelectric generation, and illicit crops.Destruction of natural habitats has drastically affected many species distributions, often reducing their historical ranges to a set of small, fragmented populations (Brooks et al. 2002).Such habitat alteration is predicted to lead to substantial extinctions in the near future.Pereira, La Suiza, 2,350 m, 27 January 1993, William Vargas 815 (FAUC).When we determined all specimens, we found that only Brother Daniel´s specimen (US and MEDEL) belongs to Passiflora danielii, while the last six are misclassified and correspond to Passiflora oerstedii Mast., subgenus Passiflora (Supersection Stipulata, Sec tion Granadillastrum) according to the classification by Feuillet and MacDougal (2003).

NOTES ON GEOGRAPHIC DISTRIBUTION
Based on the high quality photographs of live material (Figure 1) and the additional herbarium specimens incorporated in the present study (isotype and holotype), a morphological description that more accurately reflects Passiflora danielii is presented here.Of particular interest are color details not perceptible in the older herbarium specimen.The observation of fresh material has provided additional insights into P. danielii regarding fruit characters, which were not described by Killip (1960).Due to the rarity of the species, photographs of P. danielii were taken and a single herbarium specimen was collected in March 2013 from Cocorná and deposited in the herbarium of the Universidad Nacional de Colombia sede Medellín (MEDEL; J. Restrepo, W. Giraldo and J. Ocampo, No. 210), as a voucher for morphological study.
In Colombia, Passifloraceae are represented by 171 species grouped in three genera, Ancistrothyrsus (2), Dilkea (4), and Passiflora (165) with the greatest diversity in the Andean region (82%).The largest number of species is found between 1,000 and 2,000 m above sea level and the most common ones thrive in disturbed habitats, such as roadsides, cultivated land, and secondary forest (Ocampo et al. 2007).The distribution of the Passifloraceae has been drastically affected by deforestation, mainly in the Andean region.Its historical range corresponds to a region with a long history of livestock and agriculture that currently supports extensive plantations of coffee, sugar cane, rice, bananas, and potatoes.The country has 58 endemic Passifloraceae species, 95% of them exclusively Andean, implying a high extinction risk, as the Andes region is the most densely populated and disturbed of the country (Morales et al. 2007).The Department of Antioquia concentrates the highest diversity and endemism (5 spp.) of Colombian Passiflora, with 42% of the species, mainly in the Andean region (Ocampo et al. 2007).According to the categories and criteria of IUCN Red List of threatened species (IUCN 2003), Hernández and Garcia (2006) and Ocampo et al. (2007) have established that more than 110 Colombian species of Passifloraceae are threatened to some degree, with three species considered extinct.
The goal of the present study is to document the rediscovery of Passiflora danielii Killip, 1960 in the locality where it was originally described and in areas where it is likely to occur but not reported yet, and to assess its current status.
In August 1938, an enthusiast of Colombian flora, Brother Daniel F.S.C. (né Julián González Patiño), collected a plant of Passiflora in the Municipality of Cocorná, Department of Antioquia (Daniel 1968).The specimen was deposited in the U.S. National Herbarium (No. 1742750) and Killip (1960) described it as P. danielii in his Supplemental Notes on the American Species of Passi floraceae with Descriptions of New Species, belonging to the series Simplicifoliae of the subgenus Passiflora.
No other observation of the species has been reported since 1938.When we visited the recorded locality for P. danielii in the Municipality of Cocorná (Department of Antioquia), the forest had been cleared or heavily disturbed and the species was not found.However, we observed eight plants across four new localities in Cocorná.These newly collected specimens and photographs of fresh material of P. danielii allowed improving the original description of Killip (1960).The species is redescribed herein with data on morphology, ecology and geographic distribution.
Phenology: flowering in August-September to February-March; fruiting from November-December to April-May.
Distribution: rare narrow endemic to the Colombian, Department of Antioquia, Municipality of Cocorná, Eastern flank of the Central Cordillera (Figure 2).Ecology: P. danielii was observed on hillsides, along roadsides or along secondary forest margins, climbing onto shrubs or trees in thickets, at elevations ranging from 1,710 to 2,093 m above seas level.This species grows in areas with moist soil of texture sandy clay loam, annual mean temperature of 19.04°C and annual rainfall of 3,464 mm.
Conservation status: According to Myers et al. (2000) and Robbirt et al. (2006), rarity and endemism represent two factors of particular significance for decline and extinction.In this context, under the IUCN Red List guidelines (IUCN 2014) and supported with the Geospatial Conservation Assessment Tool -Geo-CAT (Bachman et al. 2011), Passiflora danielii should be classified as critically endangered (CR), based on two assessment criteria, B2a and D. Within category B, P. danielii is classified as B2a, area of occupancy estimated less than 10 km 2 : severely fragmented and known to exist at a single location.With respect to criterion D, the population size is estimated to number fewer than 50 mature individuals, with just eight plants observed in Cocorná over one year of field survey.Our results are consistent with Ocampo et al. (2007), whose list classifies P. danielii in the critically endangered (CR) category, but not with the Red List of Passifloraceae published by Hernández and Garcia (2006) where it is in the least concern (LC) category.
Strategies of conservation: Passifloraceae diversity is not well protected by the network of Colombian protected areas (Ocampo et al. 2010).The new localities where we found Passiflora danielii do not correspond with Andean protected areas and the in situ conservation of this threatened species, as well as its habitat, is urgent.Conservation or restoration efforts for P. dan ielii habitats must be integrated in the more general management at the landscape level.The latter can be ensured by coordinating existing actions for watershed protection, management of private and low-level public reserves, creation of environmental corridors, and improvement of agricultural practices that integrate the landscape.Ex situ conservation in botanical gardens and seedbanks is another strategy that must be implemented when critical habitats are destroyed.Another important aspect is the assessment of P. dan ielii as a germplasm resource for crop diversification programs, implying the need for a better understanding of the species' morphological and genetic diversity.

Figure 1 .
Figure 1.Floral and vegetative characteristics of Passiflora danielii: a flowers at anthesis, b floral bud, c longitudinal transect of the flower, d immature fruit, e mature seeds, f ovate-lanceolate bracts with glandular margin, g ovate-lanceolate leaf, h petiolar nectaries and stipules.Photographs by Jorge Restrepo and Wilmer Giraldo.