Reassessment of Varroniabellonis - a threatened, endemic plant from Puerto Rico

Abstract Background Varroniabellonis (Urb.) Britton is a lianescent or recumbent shrub that is endemic to Puerto Rico where it is restricted to specific geology types with a limited extent on the western half of the Island. The species occurs on serpentinite geology covered by serpentine-derived soils in the west-central mountains and on limestone geology in the the northern karst region. The species area of occupancy is estimated to range between 108 km2 and 268 km2 and its extent of occurrence to be between 644 km2 and 852 km2. The number of locations are estimated to be four. There are 418 known mature individuals in the wild (Hamilton 2020a). The species was previously assessed as Critically Endangered (Linsky and Sustache 2014), based on available information. However, an international team have been collaborating to conserve the species and, based on new information derived from this work, the species is reassessed as Endangered (EN), based on Criteria B1ab(i,ii,iii,iv,v)+2ab(i,ii,iii,iv,v), according to the IUCN Red List Categories and Criteria (version 3.1) and guidelines (IUCN Standards and Petitions Committee 2019). New information Areas of suitable habitat across the native range of the threatened plant, V.bellonis, were surveyed by a team of experts between 2016 and 2019 to determine the species habitat preferences, identify threats to the species survival and provide an up-to-date meta-population status. The new information enabled members of the international team to reassess the species status and will enable sound and scientifically-based recovery actions to be recommended that can secure Varroniabellonis populations for the future. Parallel efforts are ongoing to explore the species population genetics and reproductive biology.


Introduction
In this paper, we present a species conservation profile for a species endemic to the Commonwealth of Puerto Rico.

Map of records (image):
Map of records (Google Earth):

Taxonomic notes
This species was originally described as Cordia bellonis by Urban in Symbolae Antillanae, 1: 393. 1899. It was later transferrred to Varronia by Britton and Wilson (1925). Varronia bellonis is endemic to the Island of Puerto Rico, where three additional regional endemic species occur, V. lima Desv., V. rupicola (Urb.) Britton and V. wagnerorum (R.A. Howard) Borhidi. The boundaries between these taxa are currently clear and there are no known taxonomic issues for these species. However, further research into the biogeography and phylogenetics of this group is ongoing.

Region for assessment:
-Global

Geographic range
Biogeographic realm:

Basis (narrative)
This species is endemic to Puerto Rico (Acevedo-Rodriguez and Strong 2012) and has a restricted range. Extant individuals were found in and around the boundaries of the Maricao, Susúa and Río Abajo State Forests, the three historical areas of distribution, as well as individuals in previously unrecorded locations in the Municipalities of Arecibo, San German, Sabana Grande, Utuado and Lares.

Range description
Varronia bellonis was originally described from 1884 collections by Paul Sintenis, number 310, from Indiera Fría Ward and number 310b from Monte Alegrillo, in the Municipality of Maricao (Urban 1899). Over the next century, the species was sporadically collected near the type localities and in the adjacent Municipality of San Germán. Knowledge of its range expanded in the 1990s when the species was collected by G. Observation and collection event records made between 2016 and 2019 were considered to calculate minimum values of extent of occurrence (EOO) and area of occupancy (AOO), while maximum values of EOO and AOO were calculated considering all available records and the entire area of suitable habitat covering known geology types that support the species (Maldonado 2019). The EOO was estimated to range between 644 km and 852 km . The AOO was estimated to range between 108 km and 268 km . Both calculations for EOO and AOO trigger evaluation under the IUCN Red List criterion B, threatened category of Endangered (IUCN Standards and Petitions Committee 2019) and are based on a 2 x 2 km cell size and calculated with GeoCAT (Bachman et al. 2011). The number of locations was calculated to be four, considering threats posed, which can vary depending on whether individuals are found within or outside protected areas. Suppl. material 1 A specimen of Varronia bellonis, collected by N.L. Britton (number 4287) in 1915 held at UPR (barcode UPR05414), was erroneously associated with Monte Cerrote near the Municipality of Adjuntas, outside the species recorded geology types, due to the wrong preprinted label with location information being used for the specimen. The first duplicate, held at New York Botanical Garden (barcode NY00967240), resolved the issue by clarifying the collection location as Maricao, within the species known historic range and suitable habitat.

Ecology and traits (narrative)
Varronia bellonis is a lianescent or recumbent shrub with scandent branches which allow it to clamber into surrounding trees, over surrounding vegetation and across exposed slopes (Fig. 2). In open areas exposed to intense sunlight, the species may remain as a compact, multi-stemmed shrub. Mature individuals have been recorded as clumps over one metre and clambering over fourteen metres in forested areas with dense canopy cover (Hamilton 2017b). The white flowers (Fig. 3) are visited by several insect species, but which species are effective pollinators remains unknown. The fruit is a drupe that turns red when ripe (Fig. 4) and usually develops between November and February. Several bird species have been recorded visiting the plant during the fruiting season and ongoing camera-trapping has shown clear evidence for bird dispersal (Hamilton 2019a). The generation length of this plant is estimated to be 3-5 years; however, research is underway to confirm the species generation length and understand its reproductive biology through field observations and greenhouse studies (Hamilton 2020a, Hamilton et al. 2020).

Justification for conservation actions
There is 186 km of extant preferred land cover types that support the species within three protected areas (Maldonado 2019). On the limestone geology in the western part of the northern karst region, the species is extant in the Río Abajo State Forest. In the serpentinite geology covered by serpentine soils in the west-central mountains, the species is found in Maricao and Susúa State Forests (Hamilton 2019a, Hamilton 2020a, Hamilton 2020b). This species is listed as 'Endangered' under the United States Endangered Species Act as Cordia bellonis (U.S. Fish and Wildlife Service 1997) and a recovery plan was approved in 1999 (U.S. Fish Wildlife Service 1999). Hundreds of individuals in the footprint of the Puerto Rico Highway 10 development were transplanted to the Cambalache State Forest nursery and cuttings were taken for asexual propagation. The fate of most of this material is unclear; however, work by Sánchez-Cuervo et al. (2014) suggested material re-introduced at Río Abajo did not survive. A single tagged individual in Río Abajo State Forest, located during recent surveys, is apparently the sole survivor of a transplanting activity from material grown at the Cambalache State Forest nursery (Hamilton 2016). Many individuals have been recorded outside of the existing protected area network requiring close collaboration with land owners to develop management plans and enable ex-situ collections of this species to be secured. Collaboration amongst international partners (the Royal Botanic Gardens, Kew; the University of Puerto Rico, Mayagüez Campus; The Puerto Rico Department of Natural and Environmental Resources; and the US Fish and Wildlife Service) has secured ex-situ collections of this species at the University of Puerto Rico, Mayagüez Campus nursery and seed bank (Hamilton 2019b, Hamitlon 2019, Hamilton 2020a. The partners monitor individuals (Fig. 5) across the species known range and collect seeds (Fig. 6) when available for recovery purposes. Further development of ex-situ collections, including germination and cultivation trials for living plants, is underway to aid the species recovery (Hamilton 2019b, Hamilton 2020a, Hamilton et al. 2020. Ongoing work on the species population genetics, germination requirements and reproductive biology will guide future recovery actions, including augmenting existing populations and further re-introduction efforts.