Monimiaceae is a pantropical family of flowering plants comprising 28 genera and c. 200 species (Renner et al., Reference Renner, Strijk, Strasberg and Thébaud2010) occurring mainly in moist and well conserved forests, with many species being rare and endemic to restricted areas (Philipson, Reference Philipson, Kubitzki, Rohwer and Bittrich1993; Peixoto & Pereira-Moura, Reference Peixoto and Pereira-Moura2008) and thus susceptible to threats such as deforestation and fires (Peixoto et al., Reference Peixoto, Lírio, Maurenza, Reis-Júnior, Santos-Filho, Abreu, Martinelli and Moraes2013). The family is highly diversified in Neotropical rain forests, including in Brazil, and particularly in the state of Rio de Janeiro, where five genera and 33 species occur, mostly on mountains (BFG, 2015).
The Protected Area of Macaé de Cima, in the Nova Friburgo municipality, holds the highest number of Monimiaceae species in the state (16 species) and in Brazil (Peixoto & Pereira-Moura, Reference Peixoto, Pereira-Moura, Lima and Guedes-Bruni1996; IUCN, 2016b). Seven are endemic to the area and some are known only from 19th century collections. This area is important for conservation because of the presence of species with restricted distributions (Diniz et al., Reference Diniz, Gonçalves and Brito2017).
Mollinedia stenophylla was described by Perkins (Reference Perkins1900) based on specimens collected by Glaziou in 1888 (Glaziou, n. 17768) and 1893 (n. 20220), both from Macaé de Cima. Another specimen was collected in 1832 (Riedell & Luschnath, n. 315), from the same locality, but not cited by Perkins in the protologue. Since the collection of these specimens no living population had been encountered, despite extensive fieldwork in the area during 1989–1993 (Lima & Guedes-Bruni, Reference Lima and Guedes-Bruni1997). However, in 2015 we rediscovered a population of M. stenophylla in Macaé de Cima (Fig. 1) in the same area where it had last been collected 122 years previously.
Fig. 1 The single known location of Mollinedia stenophylla in Rio de Janeiro state, Brazil.
There is a general concern in plant conservation regarding the best strategies to conserve narrow endemic species such as M. stenophylla. Potential strategies include research on artificial propagation, ecophysiology and pollination, monitoring, threat mitigation, reintroduction and ex situ conservation (Martins et al., Reference Martins, Fernandes, Maurenza, Pougy, Loyola and Martinelli2014; Zhang et al., Reference Zhang, Luo and Chen2014; Kraaij et al., Reference Kraaij, Baard and Crain2016). Here we describe the geographical distribution of M. stenophylla, comment on its morphology, ecology and conservation, and make a new Red List assessment.
Branches of eight plants with flowers and fruits were collected (Lírio vouchers 1219, 1220, 1224, 1253, 1255, 1256, 1257, 1258) and deposited at RB, M, MBML, NY and P herbaria (acronyms follow Thiers, Reference Thiers2016). Extent of Occurrence (EOO) was calculated using the area of the minimum convex polygon, and Area of Occupancy (AOO) using a grid of 4 km2 cells (IUCN, 2016a).
The living population of M. stenophylla was found in the surroundings of a waterfall in Macaé de Cima. The species is dioecious (Plate 1), easily recognized by its whorled leaves and low height (< 1 m), which are unique characteristics in the genus Mollinedia. The species has small (c. 0.8 × 0.6 cm), blackish-purple druplets (fruits) with contrasting, yellowish receptacles (Plate 1c).
Plate 1 The (a) branch and whorled leaves, (b) pistillate flowers, (c) fruit receptacle and druplets, (d) empty receptacle, (e) staminate flowers, (f) clonal reproduction (details in g,h), and (i) habitat of M. stenophylla.
We observed that M. stenophylla exhibits clonal reproduction, with aerial stems that fall on moist soil and produce roots, resulting in new individuals (Plate 1f), a phenomenon not previously reported for Neotropical Monimiaceae. Mature specimens were observed with stems < 1 m tall and 1.5 cm diameter, an uncommon characteristic in Neotropical Monimiaceae, suggesting a neotenic stage. The rediscovered population had 49 mature individuals, 13 of them pistillate, and c. 30 seedlings, with an AOO of 4 km2.
The restricted distribution of this species is probably a result of its dependency on water. Its small, coloured druplets are attractive to birds that are potential dispersers for Mollinedia (Lírio et al., Reference Lírio, Peixoto and Siqueira2015), as for other species of Mollinedia (Lorence, Reference Lorence1985; Renner & Hausner, Reference Renner, Hausner, Harling and Andersson1997).
Mollinedia stenophylla was previously categorized as Endangered by Peixoto (Reference Peixoto, Mello-Filho, Sommer and Peixoto1992) and included in the 2008 Official Threatened Flora Species List of Brazil (MMA, 2008), and it is currently categorized as Endangered on the IUCN Red List, although this needs updating (Varty, Reference Varty1998). CNCFlora (2012) assessed the species as Near Threatened based on its EOO, including presumed occurrences in Espírito Santo state, and therefore it wasn't included in the 2014 Official Threatened Flora Species List of Brazil (MMA, 2014). However, ongoing revision of Neotropical Monimiaceae by EJL and ALP indicates the species is known only from Macaé de Cima. Specimens from Espírito Santo state, previously determined as M. stenophylla, appear to be an undescribed species.
The single known population of M. stenophylla has few individuals, and a restricted distribution at a single location that is on the access trail to a waterfall, and hence tourism and housing are the main threats (Mendes, Reference Mendes2010). Macaé de Cima is categorized as a low protection conservation unit in which visitation and human settlement are permitted. It is therefore likely that AOO, EOO and habitat quality will decline, and M. stenophylla should be recategorized as Critically Endangered based on criteria (IUCN, 2012) B2ab (ii, iii) + C2ai + D.
Mollinedia stenophylla could be considered rare (sensu Rabinowitz et al., Reference Rabinowitz, Cairns, Dillon and Soulé1986; Caiafa & Martins, Reference Caiafa and Martins2010) because of its narrow geographical range, habitat specificity and low population size. Rare species are more susceptible to extinction than more common species, and may incorrectly be presumed extinct if they have not been observed for many years (Collar, Reference Collar1998; Penedo et al., Reference Penedo, Moraes, Borges, Maurenza and Martinelli2015).
In a megadiverse country such as Brazil assessment of the extinction risk of species is likely to be slow as there are a large number of species to assess (only c. 17% of the native flora of Brazil has so far been assessed), and improving knowledge of taxonomy and distributions affects previous conservation assessments (Moraes et al., Reference Moraes, Borges, Martins, Fernandes, Messina and Martinelli2014; CNCFlora, 2017, in press). This highlights the importance of investing time in visiting herbaria, and in fieldwork and taxonomy, to update Red Lists.
We recommend the development of an action plan for M. stenophylla, including in situ conservation to control local threats and an ex situ approach to improve cultivation methods, practical management of risks and a strategy to maintain genetic diversity (Cavender et al., Reference Cavender, Westwood, Bechtoldt, Donnelly, Oldfield and Gardner2015). Such strategies have been proposed to protect narrow endemic species (Fenu et al., Reference Fenu, Mattana and Bacchetta2011; Martinell et al., Reference Martinell, Pujol, Blanché, Molero and Sàez2011; Cogoni et al., Reference Cogoni, Fenu, Concas and Bacchetta2013; Li et al., Reference Li, Zhang and Zhang2014; Martins et al., Reference Martins, Fernandes, Maurenza, Pougy, Loyola and Martinelli2014).
Currently, there are six individuals of M. stenophylla in the living collection of Rio de Janeiro Botanical Garden, which have been cultivated in the greenhouse since January 2015. However, seeds need to be collected for storage and the maintenance of genetic diversity, and studies are needed, in natural populations and living collections, of phenology, pollination, dispersal, the dioecious sexual system and vegetative reproduction.
Faced with the challenge of preparing action plans for all threatened plants, the National Centre for Flora Conservation has implemented local action plans (e.g. Pougy et al., Reference Pougy, Martins, Verdi, Maurenza, Loyola and Martinelli2015a,Reference Pougy, Verdi, Martins, Loyola and Martinellib) for threatened, data deficient and near threatened species that occur in the same area. There are 41 other endemic plant species with a restricted distribution in Macaé de Cima (CNCFlora, 2017, in press). An action plan with a territorial approach provides a list of indicators that facilitate recognition of the studies and actions required for threat mitigation.
The extinction risk assessment of the endemic species of Rio de Janeiro state was carried out by CNCFlora, the National Red List Authority, in partnership with the State Secretariat for the Environment of Rio de Janeiro (SEA-RJ) and with the collaboration of more than 100 taxonomists. The Red Book of Rio de Janeiro Endemic Flora is complete and will be published in 2017. The migration of these data to the IUCN system and the territorial action plan for the endemic species of the state of Rio de Janeiro is ongoing.
Acknowledgements
We thank Augusto Giaretta, Fernanda Masullo, and Pablo Vianny for their assistance during fieldwork; Eline Martins and Tainan Messina for comments on the text; Fernanda Wimmer for the distribution map; Adèle Rossetti Morosini and Rafael F. Almeida for help with English; and Martin Fisher and two anonymous reviewers who made important contributions to this work. We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Fundação de Amparo à Pesquisa do Rio de Janeiro and Conselho Nacional de Desenvolvimento Científico e Tecnológico for granting their PhD fellowship to EJL and JF.
Author contributions
EJL collected the species, EJL and ALP identified the species, RN and GM made the risk assessment, JF prepared the Plate, and EJL, JF, RN, GM and ALP wrote the article.
Biographical sketches
Elton John de Lírio's research interests encompass systematics and conservation of phanerogams. Joelcio Freitas is interested in systematics and conservation of early diverging angiosperms. Raquel Negrão works as a data analyst for flora risk extinction assessments at CNCFlora, which supports the Brazilian Flora Red List Programme. Gustavo Martinelli is interested in mountain biodiversity, currently coordinates CNCFlora, and is the Brazilian focal point for the Global Strategy for Plant Conservation. Ariane Luna Peixoto specializes in systematic and conservation studies of phanerogams and in the history of botany.
