A new Pisonia (Nyctaginaceae) from Jamaica, with an updated list of species in the genus and a key to the West Indian taxa

Here we describe a new species of Pisonia (Caryophyllales: Nyctaginaceae) from Jamaica, named P. jamaicensis Proctor ex Caraballo, K.Campbell, & S.Cross, restricted to limestone hills in the central and western part of the island. The species description is complemented with an illustration, pictures, a distribution map, and notes on its biology and conservation, including an IUCN evaluation. We also present a list of the 27 currently accepted species of Pisonia with their general distributions, and a key to separate the 16 taxa reported for the West Indies.


INTRODUCTION
The genus Pisonia L. (Caryophyllales: Nyctaginaceae) is widely distributed in tropical regions around the globe, although its diversity certainly lies within the American continent (Stevens 2001 onwards). Recent studies have reexamined the circumscription of the genus and transferred a number of species to other genera within tribe Pisonieae (Rossetto et al. 2019; Chagas and Costa-Lima 2020; Rossetto and Caraballo-Ortiz 2020). As a result, the number of currently accepted species in Pisonia has been estimated to be around 25 (The Plant List 2013 onwards; Ulloa Ulloa et al. 2018 onwards).
In the West Indies, the genus is represented by approximately 15 species, most of them endemic to the region (Acevedo-Rodríguez and Strong 2012). During current studies on the diversity of Pisonia, Caraballo-Ortiz found collections from Jamaica that did not match any of the previously published congeners. After morphological comparisons with all known species for the West Indies, we concluded that this taxon represents an undescribed species. This finding concords with the view of George R. Proctor, who labeled a series of specimens from the Institute of Jamaica Herbarium as "Pisonia jamaicensis Proctor" during the early 2000's, although he did not provide a description and effectuate its publication. In this work, we decided to adopt Proctor's proposed name and formally describe the species as P. jamaicensis Proctor ex Caraballo, K.Campbell, & S.Cross.
Pisonia jamaicensis is a tree restricted to wooded summits and upper cliffs of limestone hills in central and western Jamaica. We complement the species' description with an illustration, pictures, a distribution map, and notes on its biology. We also discuss how to separate this species from the other congener in Jamaica, and present a preliminary conservation assessment following the IUCN criteria. A table summarizing the currently accepted Pisonia worldwide with their general distributions is also included, along with a dichotomous key to separate the taxa reported for the West Indies.

MATERIALS AND METHODS
We studied all the collections identified as Guapira Aubl., Pisonia, and Neea Ruiz & Pav. from Jamaica deposited in 18 herbaria (CAYM, F, FLAS, FTG, HACC, IJ, JBSD, K, MAPR, MO, NY, P, SJ, UC, UPR, UPRRP, US, and UCWI). Measurements presented in the description were taken from dried plants using physical or virtual specimens (including types, accessible through the JSTOR Global Plants website [https://plants.jstor. org/]), while notes on colors of fresh structures for the new species were taken from plants in the field.
The estimated area of occupancy (AOO) and extent of occurrence (EOO) were calculated using GeoCat (Bachman et al. 2011) by plotting estimated points of all known localities based on herbarium specimens and field explorations. The AOO and EOO were complemented with information on number of known populations, demographic profile and trends, and known threats to conduct an IUCN evaluation based on criteria B and D. The categories and criteria obtained were verified with the Species Information Services (SIS) tool from IUCN (2020) using the same input information as in GeoCat. The SIS tool generated a draft assessment for P. jamaicensis which will be submitted to IUCN and updated as more information on the species became available in the future.
To prepare the updated list of Pisonia, first we retrieved all currently accepted species from the Vascular Plants of the Americas website (Ulloa Ulloa et al. 2018 onwards). Then, we compiled all Pisonia species included in recent regional floras across the American continent and evaluated any discrepancies. For Pisonia species from the West Indies, we conducted a deeper study by examining types and protologues of all published taxa reported for the region. We found that most species presented in Ulloa Ulloa et al. (2018 onwards) matched with the ones we found as accepted in regional studies.
Recently, many species of Pisonia from the Indian and Pacific Oceans were transferred to Ceodes J.R.Forst. & G.Forst. and Rockia Heimerl (Rossetto and Caraballo-Ortiz 2020), and species from Brazil were transferred to Guapira (Chagas and Costa-Lima 2020), and therefore, were excluded from this assessment. Our final list contained 27 species of Pisonia (including the one described in this study), of which 16 taxa -representing 15 species and one subspecies -are present in the West Indies (Table 1)

Diagnosis
Pisonia jamaicensis is distinguished from its only other known congener in Jamaica, P. aculeata, by a combination of the following characteristics: tree with unarmed branches (vs. scandent shrubs or treelets with  branches armed with spines), leaves ovate and shiny when fresh (vs. leaves elliptic and dull when fresh), and anthocarps narrowly elliptic or oblong, slightly curved when unripe, with viscid glands restricted to the distal 1/3 portion (vs. anthocarps clavate or obovate, straight, with viscid glands along their whole length). Pisonia jamaicensis is endemic to Jamaica whereas P. aculeata has a pantropical distribution.

Etymology
We named the species after the island of Jamaica, where the species is endemic.

Phenology
Pisonia jamaicensis has been recorded flowering from March to April and fruiting from April to July. Trees shed leaves before flowering, and produce new leaves during or just after the flowering stage. Apparently, adult trees do not shed their leaves if they are not reproductive on a given year. The vast majority of Pisonia species seems to follow the same synchronized phenological pattern to shed leaves between February and March and produce a mast flowering during March and April. This behaviour might help facilitate cross pollination events in this mainly dioecious genus.
Some reproductive individuals of P. jamaicensis were observed bearing a few inflorescences of the opposite sex (i.e., subandroecious or subgynoecious). This situation can be interpreted as an uncommon adaptation in Pisonia to ensure fruit set in small populations or when first colonizing an island, and has been previously reported in three other species from the Caribbean (Proctor 2012;Caraballo-Ortiz and Trejo-Torres 2017).

Distribution
Pisonia jamaicensis is restricted to karstic limestone hills in central and western Jamaica (Figure 3) at elevations between 350-700 m. The 22 known collections for the species span the parishes of Hanover, Manchester, St. Catherine, St. James and Trelawny (Figure 3). The estimated AOO and EOO for its current distribution were 48 km 2 and 1,934 km 2 , respectively. Although not reported yet from the parishes of Clarendon, St. Ann, St. Elizabeth, and Westmoreland, it is probable that P. jamaicensis is also present there.

Ecology
Pisonia jamaicensis is apparently restricted to woodlands on exposed or semi-exposed hilltops and hillsides in dog-toothed moist limestone with loose rocks. We currently lack information on many ecological aspects for the species including suitable habitat and substrate, floral visitors, seed dispersers, and germination rates.

Demography and conservation notes
Detailed demographic profiles for P. jamaicensis have not been developed yet. However, preliminary field observations suggest that the estimated total number of individuals is greater than 250, distributed across five to seven subpopulations (Figure 3) Pisonia jamaicensis does not seem to be directly threatened by targeted harvesting or collection, and we are not aware of any commercial or traditional use for the species. Given its restricted distribution to tops and upper slopes of limestone hills, the species can be threatened by local farming and associated activities such as slash and burn, development, mining (especially for bauxite), and the impact of climate change such as intense droughts, fi res, and hurricanes.
Most (82%) of the known specimens for the species were collected over 20 years ago and we currently have little knowledge about their current status. Th is is especially relevant for half of the localities, which were found more than 40 years ago. It is likely that some of the sites where P. jamaicensis was reported have been altered, especially the ones outside protected areas. Fortunately, approximately 70% of the known localities are within areas with some level of legal protection such as the Cockpit County and Dolphin Head forest reserves. In addition, the rugged terrain where the species grows might offer certain degree of protection from forest clearing for agricultural purposes.
The relatively widespread distribution of P. jamaicensis across the rugged terrain from central and western Jamaica, the low levels of direct threats, and the estimated AOO and EOO estimated indicate that the species should be classifi ed as Vulnerable, under the specific IUCN criteria B2ab(i,iii,iv);D1 (IUCN 2020). However, some subpopulations in unprotected lands might be at high risk of disappearing. We thus recom-mend conducting surveys to assess the current status of all known populations to refi ne this fi rst evaluation and focus conservation eff orts where most needed.

Dichotomous key to separate species of Pisonia from the West Indies
The following dichotomous artificial key contain the 16 taxa of Pisonia that, based on our assessment, are currently accepted for the West Indies. Most members in this genus have short flowering and fruiting periods, and therefore, many collections in herbaria are sterile. In consequence, the characters used to build this key are mostly vegetative, complemented with geographic locations and reproductive features. Certain taxa appear more than once to cover variations in their morphology. Some entries have been modified from Trejo-Torres (2005) and Caraballo-Ortiz and Trejo-Torres (2017).
The key to separate the nine genera within Pisonieae presented in Rossetto and Caraballo-Ortiz (2020) should help users verify that their specimens are actually Pisonia and not Guapira or Neea, which are the only other genera from this tribe present in the West Indies.

DISCUSSION
The addition of P. jamaicensis increases to 27 the number accepted species of Pisonia and brings in a second species -the first endemic -of this genus to the flora of Jamaica. The rest of the Greater Antilles and Grand Cayman also have endemic Pisonia, making the West Indies a hotspot for the genus. In fact, more than half (16 taxa; 59%) of its diversity is found in the Caribbean, of which 88% are restricted to the region and 69% are single-island endemics (Table 1). Cuba is the most diverse island with seven taxa (six species and one subspecies), of which 71% are endemics. The second most diverse island is Puerto Rico holding six species with half of them endemics, followed by Hispaniola with three species and 33% endemism. All other islands or archipelagos (i.e., Bahamas, Cayman Islands, Jamaica and the Lesser Antilles) have two species of Pisonia, with the only endemics in Grand Cayman and Jamaica.
The records of P. subcordata from Jamaica reported by Adams (1972) and Acevedo-Rodríguez and Strong (2012) Proctor (1982). However, some specimens originally labeled as P. subcordata were, in fact, the species here described. When sterile, G. rotundata can be separated from P. jamaicensis based on mature leaves, which are elliptic or obovate, stiffly leathery, and dry yellowish brown with secondary veins brown, thin and inconspicuous. These characters contrast with the leaves of P. jamaicensis, which are ovate (rarely broadly elliptic or rounded), chartaceous or soft leathery, and dry brown with secondary veins black, corky and conspicuous.
After clarifying that P. subcordata is not present in Jamaica, this island now contains two species of Pisonia: P. aculeata and the newly described P. jamaicensis. The former can be separated from the latter by having a scandent habit with twigs bearing spines, and broadly elliptic fruits with viscid glands distributed along the whole length (vs. tree habit with unarmed twigs, and narrowly elliptic fruits with viscid glands restricted to the upper third portion in P. jamaicensis). Regarding the distribution of P. subcordata, this species is now restricted to coastal habitats in northern and eastern Puerto Rico, Virgin Islands and the Lesser Antilles, extending to Martinique (Acevedo-Rodríguez and Strong 2012; Caraballo-Ortiz and Trejo-Torres 2017).
Our estimate of 27 accepted species in Pisonia is still in need of more investigation as some taxa are poorly known and it is difficult to assess their validity. For example, P. proctorii, a spineless liana from Belize, could be a variation of P. aculeata. Moreover, P. indecora Heimerl might represent a species of Guapira, possibly G. boliviana (Britton ex Rusby) Lundell (E.F.S. Rossetto, pers. comm.). Therefore, further work on Pisonia is needed to help refine its taxonomy and reach a more precise estimation of accepted species.
Although no comprehensive phylogenetic or biogeographic study of Pisonia have been published to date, a recent study of tribe Pisonieae by Rossetto et al. (2019) found an intriguing relationship between P. grandis and the taxa from the West Indies. However, P. grandis -renowned as the Birdcatcher tree -has a native range covering myriads of islands across the Indian and Pacific Oceans but does not reach the American continent. Further systematic studies on the genus might shed light on this finding and help reconstruct the evolutionary relationship among species to resolve taxonomic uncertainties, especially within the P. aculeata complex, whose members have a shrubby-scandent habit and are often armed with stout spines.

AUTHOR CONTRIBUTIONS
MACO prepared a first draft of the manuscript, revised herbaria, prepared the species description, compiled the list of accepted Pisonia, and built the dichotomous key. KCSEC and SJC collected the species, revised herbaria, prepared the distribution map, and performed the IUCN evaluation. All authors contributed to the manuscript and approved the final version.