(Monimiaceae) in the Atlantic Rainforest, Brazil

A hundred years’ tale: rediscovery of Mollinedia stenophylla (Monimiaceae) in the Atlantic rainforest, Brazil

E LTON J OHN DE L ÍRIO,JOELCIO F REITAS,RAQUEL N EGRÃO G USTAVO M ARTINELLI and A RIANE L UNA P EIXOTO

Abstract The plant Mollinedia stenophylla Perkins The Protected Area of Macaé de Cima, in the Nova (Monimiaceae) is endemic to southern Brazil and, until Friburgo municipality, holds the highest number of , had not been seen for  years. We located a single Monimiaceae species in the state ( species) and in Brazil population of the species on the margin of a watercourse (Peixoto & Pereira-Moura, ; IUCN, b). Seven are in the mountainous region of Rio de Janeiro state. We de- endemic to the area and some are known only from th scribe the location of the species, comment on its morph- century collections. This area is important for conservation ology, ecology and conservation, assess its conservation because of the presence of species with restricted distribu- status, propose conservation measures, and discuss the po- tions (Diniz et al., ). tential value of local action plans for this and other narrow Mollinedia stenophylla was described by Perkins () endemic plant species. Mollinedia stenophylla has whorled based on specimens collected by Glaziou in  (Glaziou, leaves, clonal reproduction and a low height, unusual traits n. ) and  (n. ), both from Macaé de Cima. in the genus Mollinedia. Using the IUCN Red List criteria Another specimen was collected in  (Riedell & we assess the species as Critically Endangered. This example Luschnath, n. ), from the same locality, but not cited by highlights the importance of investing time in plant surveys Perkins in the protologue. Since the collection of these spe- and taxonomy, especially in megadiverse countries such as cimens no living population had been encountered, despite Brazil. extensive fieldwork in the area during – (Lima & Guedes-Bruni, ). However, in  we rediscovered a Keywords Brazil, clonal reproduction, habitat specificity, population of M. stenophylla in Macaé de Cima (Fig. )in Monimiaceae, narrow endemic, point endemic, Red List, the same area where it had last been collected  years threatened species previously. onimiaceae is a pantropical family of flowering plants There is a general concern in plant conservation regard- Mcomprising  genera and c.  species (Renner ing the best strategies to conserve narrow endemic species et al., ) occurring mainly in moist and well conserved such as M. stenophylla. Potential strategies include research forests, with many species being rare and endemic to re- on artificial propagation, ecophysiology and pollination, stricted areas (Philipson, ; Peixoto & Pereira-Moura, monitoring, threat mitigation, reintroduction and ex situ   ) and thus susceptible to threats such as deforestation conservation (Martins et al., ; Zhang et al., ;  and fires (Peixoto et al., ). The family is highly diversi- Kraaij et al., ). Here we describe the geographical distri- fied in Neotropical rain forests, including in Brazil, and par- bution of M. stenophylla, comment on its morphology, ecol- ticularly in the state of Rio de Janeiro, where five genera and ogy and conservation, and make a new Red List assessment.  species occur, mostly on mountains (BFG, ). Branches of eight plants with flowers and fruits were collected (Lírio vouchers , , , , , , , ) and deposited at RB, M, MBML, NY and P herbaria (acronyms follow Thiers, ). Extent of Occurrence ELTON JOHN DE LÍRIO (Corresponding author), GUSTAVO MARTINELLI* and ARIANE LUNA PEIXOTO Escola Nacional de Botânica Tropical, Instituto de Pesquisas (EOO) was calculated using the area of the minimum con- Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão, 2040, 22460-030, vex polygon, and Area of Occupancy (AOO) using a grid of Horto, Rio de Janeiro, Rio de Janeiro, Brazil    E-mail [email protected] km cells (IUCN, a). The living population of M. stenophylla was found in the JOELCIO FREITAS Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil surroundings of a waterfall in Macaé de Cima. The species is  RAQUEL NEGRÃO Centro Nacional de Conservação da Flora Instituto de Pesquisas dioecious (Plate ), easily recognized by its whorled leaves Jardim Botânico do Rio de Janeiro, Dipeq, Jardim Botânico, Rio de Janeiro, and low height (,  m), which are unique characteristics Brazil in the genus Mollinedia. The species has small (c. . × . *Also at: Centro Nacional de Conservação da Flora, Instituto de Pesquisas cm), blackish-purple druplets (fruits) with contrasting, Jardim Botânico do Rio de Janeiro, Dipeq, Jardim Botânico, Rio de Janeiro,  Brazil yellowish receptacles (Plate c). Received  April . Revision requested  June . We observed that M. stenophylla exhibits clonal repro- Accepted  November . First published online  June . duction, with aerial stems that fall on moist soil and produce

Oryx, 2018, 52(3), 437–441 © 2017 Fauna & Flora International doi:10.1017/S0030605316001654 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 02 Oct 2021 at 01:21:25, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605316001654 438 E. J. de Lírio et al.

FIG. 1 The single known location of Mollinedia stenophylla in Rio de Janeiro state, Brazil.

roots, resulting in new individuals (Plate f), a phenomenon Mollinedia stenophylla could be considered rare (sensu not previously reported for Neotropical Monimiaceae. Rabinowitz et al., ; Caiafa & Martins, ) because of Mature specimens were observed with stems ,  m tall its narrow geographical range, habitat specificity and low and . cm diameter, an uncommon characteristic in population size. Rare species are more susceptible to extinc- Neotropical Monimiaceae, suggesting a neotenic stage. tion than more common species, and may incorrectly be The rediscovered population had  mature individuals,  presumed extinct if they have not been observed for many  of them pistillate, and c.  seedlings, with an AOO of  km . years (Collar, ; Penedo et al., ). The restricted distribution of this species is probably a re- In a megadiverse country such as Brazil assessment of the sult of its dependency on water. Its small, coloured druplets extinction risk of species is likely to be slow as there are a are attractive to birds that are potential dispersers for large number of species to assess (only c. % of the native Mollinedia (Lírio et al., ), as for other species of flora of Brazil has so far been assessed), and improving Mollinedia (Lorence, ; Renner & Hausner, ). knowledge of taxonomy and distributions affects previous Mollinedia stenophylla was previously categorized as conservation assessments (Moraes et al., ; CNCFlora, Endangered by Peixoto () and included in the  , in press). This highlights the importance of investing Official Threatened Flora Species List of Brazil (MMA, time in visiting herbaria, and in fieldwork and taxonomy, to ), and it is currently categorized as Endangered on update Red Lists. the IUCN Red List, although this needs updating (Varty, We recommend the development of an action plan for ). CNCFlora () assessed the species as Near M. stenophylla, including in situ conservation to control Threatened based on its EOO, including presumed occur- local threats and an ex situ approach to improve cultivation rences in Espírito Santo state, and therefore it wasn’t in- methods, practical management of risks and a strategy to cluded in the  Oﬃcial Threatened Flora Species List maintain genetic diversity (Cavender et al., ). Such strat- of Brazil (MMA, ). However, ongoing revision of egies have been proposed to protect narrow endemic species Neotropical Monimiaceae by EJL and ALP indicates the (Fenu et al., ; Martinell et al., ; Cogoni et al., ;Li species is known only from Macaé de Cima. Specimens et al., ; Martins et al., ). from Espírito Santo state, previously determined as M. ste- Currently, there are six individuals of M. stenophylla in nophylla, appear to be an undescribed species. the living collection of Rio de Janeiro Botanical Garden, The single known population of M. stenophylla has few which have been cultivated in the greenhouse since individuals, and a restricted distribution at a single location January . However, seeds need to be collected for stor- that is on the access trail to a waterfall, and hence tourism age and the maintenance of genetic diversity, and studies are and housing are the main threats (Mendes, ). Macaé de needed, in natural populations and living collections, of Cima is categorized as a low protection conservation unit in phenology, pollination, dispersal, the dioecious sexual sys- which visitation and human settlement are permitted. It is tem and vegetative reproduction. therefore likely that AOO, EOO and habitat quality will de- Faced with the challenge of preparing action plans for all cline, and M. stenophylla should be recategorized as threatened plants, the National Centre for Flora Critically Endangered based on criteria (IUCN, )Bab Conservation has implemented local action plans (e.g. (ii, iii) + Cai + D. Pougy et al., a,b) for threatened, data deficient and

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.

near threatened species that occur in the same area. There Fisher and two anonymous reviewers who made important are  other endemic plant species with a restricted distribu- contributions to this work. We thank Coordenação de tion in Macaé de Cima (CNCFlora, , in press). An ac- Aperfeiçoamento de Pessoal de Nível Superior, Fundação tion plan with a territorial approach provides a list of de Amparo à Pesquisa do Rio de Janeiro and Conselho indicators that facilitate recognition of the studies and ac- Nacional de Desenvolvimento Científico e Tecnológico for tions required for threat mitigation. granting their PhD fellowship to EJL and JF. 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 Author contributions Secretariat for the Environment of Rio de Janeiro (SEA-RJ) and with the collaboration of more than  taxonomists. EJL collected the species, EJL and ALP identified the species, The Red Book of Rio de Janeiro Endemic Flora is complete RN and GM made the risk assessment, JF prepared the and will be published in . The migration of these data to Plate, and EJL, JF, RN, GM and ALP wrote the article. the IUCN system and the territorial action plan for the endemic species of the state of Rio de Janeiro is ongoing. References

Acknowledgements BFG (THE BRAZIL FLORA GROUP)() Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia, , –. We thank Augusto Giaretta, Fernanda Masullo, and Pablo CAIAFA, A.N. & MARTINS, F.R. () Forms of rarity of tree species in Vianny for their assistance during fieldwork; Eline Martins the southern Brazilian Atlantic rainforest. Biodiversity and Conservation, , –. and Tainan Messina for comments on the text; Fernanda CAVENDER, N., WESTWOOD, M., BECHTOLDT, C., DONNELLY, G., Wimmer for the distribution map; Adèle Rossetti Morosini OLDFIELD, S., GARDNER, M. et al. () Strengthening the and Rafael F. Almeida for help with English; and Martin conservation value of ex situ tree collections. Oryx, , –.

COGONI, D., FENU, G., CONCAS,E.&BACCHETTA,G.() The MORAES, M.A., BORGES, R.A.X., MARTINS, E.M., FERNANDES, R.A., eﬀectiveness of plant conservation measures: the Dianthus MESSINA,T.&MARTINELLI,G.() Categorizing threatened morisianus reintroduction. Oryx, , –. species: an analysis of the Red List of the flora of Brazil. Oryx, , COLLAR, N.J. () Extinction by assumption; or, the Romeo Error on –. Cebu. Oryx, , –. PEIXOTO, A.L. () Mollinedia stenophylla.InCenturia Plantarum CNCFLORA (CENTRO NACIONAL DE CONSERVAÇÃO DA FLORA) Brasiliensium Exstintionis Minitata (eds L.E. Mello-Filho, G. () Mollinedia stenophylla Perkins. Http://cncflora.jbrj.gov.br/ V. Sommer & A.L. Peixoto), p. . Sociedade Botânica do Brasil, portal/pt-br/profile/Mollinedia%stenophylla [accessed  July Rio de Janeiro, Brazil. ]. PEIXOTO, A.L. & PEREIRA-MOURA, M.V.L. () Monimiaceae. In CNCFLORA () Livro vermelho das plantas endêmicas do Rio de Reserva Ecológica de Macaé de Cima, Nova Friburgo, RJ. Aspectos Janeiro. Andrea Jakobson Estúdio, Instituto de Pesquisas Jardim Florísticos das Espécies Vasculares (eds M.P.M. Lima & Botânico do Rio de Janeiro, Rio de Janeiro, Brazil (in press). R. Guedes-Bruni), pp. –. IBGE/JBRJ, Rio de Janeiro, Brazil. DINIZ, M.F., GONÇALVES,T.V.&BRITO,D.() Last of the green: PEIXOTO, A.L. & PEREIRA-MOURA, M.V.L. () A new genus of identifying priority sites to prevent plant extinctions in Brazil. Oryx, Monimiaceae from the Atlantic Coastal Forest in South-Eastern , –. Brazil. Kew Bulletin, , –. FENU, G., MATTANA,E.&BACCHETTA,G.() Distribution, status PEIXOTO, A.L., LÍRIO,E.J.,MAURENZA,D.,REIS-JÚNIOR,J.S., and conservation of a Critically Endangered, extremely narrow SANTOS-FILHO, L.A.F., ABREU,M.B.etal.() Monimiaceae. In endemic: Lamyropsis microcephala (Asteraceae) in Sardinia. Oryx, Livro Vermelho da Flora do Brasil (eds G. Martinelli & M.A. Moraes), , –. pp. –. Andrea Jakobsson Estúdio, Rio de Janeiro, Brazil. IUCN () IUCN Red List Categories and Criteria: Version .. nd PENEDO, T.S.A., MORAES, M.A., BORGES, R.A.X., MAURENZA,D.& edition. IUCN, Gland, Switzerland, and Cambridge, UK. Http:// MARTINELLI,G.() Considerations on extinct species of www.iucnredlist.org/technical-documents/categories-and-criteria Brazilian flora. Rodriguésia, , –. [accessed  January ]. PERKINS,J.() Monographie der Gattung Mollinedia. Botanische IUCN (a) Guidelines for using the IUCN Red List Categories and Jahrbücher für Systematik, Pflanzengeschichte und Criteria. Version . Prepared by the Standards and Petitions Pflanzengeographie, , –. Subcommittee. Http://www.iucnredlist.org/documents/ PHILIPSON, W.R. () Monimiaceae. In The Families and Genera of RedListGuidelines.pdf [accessed  April ]. Vascular Plants. Volume . Flowering Plants. Dicotyledons: IUCN (b) The IUCN Red List of Threatened Species. Version Magnoliid, Hamamelid and Caryophyllid Families (eds K. Kubitzki, -. Http://www.iucnredlist.org [accessed  February ]. J.G. Rohwer & V. Bittrich), pp. –. Springer Verlag, Berlin, KRAAIJ, T., BAARD, J.A. & CRAIN, B.J. () Conservation status and Germany. management insights from tracking a cryptic and Critically POUGY, N., MARTINS, E., VERDI, M., MAURENZA, D., LOYOLA,R.& Endangered species of Orchidaceae. Oryx, http://dx.doi.org/./ MARTINELLI,G.(a) Plano de Ação Nacional para a conservação S. da flora ameaçada de extinção da região de Grão Mogol-Francisco LI, B., ZHANG,Z.&ZHANG,D.() Conservation status of the Sá. CNCFlora, Laboratório de Biogeografia da Conservação, Jardim unique population of Wenchengia alternifolia, an enigmatic plant Botânico do Rio de Janeiro. Andrea Jakobsson Estúdio, Rio de endemic to Hainan Island, China. Oryx, , –. Janeiro, Brazil. LIMA, H.C. & GUEDES-BRUNI, R.R. () Serra de Macaé de Cima: POUGY, N., VERDI, M., MARTINS, E., LOYOLA,R.&MARTINELLI,G. Diversidade Florística e Conservação em Mata Atlântica. Instituto de (b) Plano de ação nacional para a conservação da flora Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brazil. ameaçada de extinção da Serra do Espinhaço Meridional. CNCFlora, LÍRIO, E.J., PEIXOTO, A.L. & SIQUEIRA, M.F. () Taxonomy, Laboratório de Biogeografia da Conservação, Jardim Botânico do conservation, geographic and potential distribution of Macrotorus Rio de Janeiro. Andrea Jakobsson Estúdio, Rio de Janeiro, Brazil. Perkins (Mollinedioideae, Monimiaceae), and a key to the RABINOWITZ, D., CAIRNS,S.&DILLON,T.() Seven forms of rarity Neotropical genera of Monimiaceae. Phytotaxa, , –. and their frequency in the flora of the British Isles. In Conservation LORENCE, D.H. () A monograph of the Monimiaceae (Laurales) in Biology: the Science of Scarcity and Diversity (ed. M.E. Soulé), pp. the Malagasy region (Southwest Indian Ocean). Annals of the –. Sinauer Associates, Sunderland, USA. Missouri Botanical Garden, , –. RENNER, S.S. & HAUSNER,G.() Siparunaceae, Monimiaceae. In MARTINELL, M.C., PUJOL, J.L., BLANCHÉ, C., MOLERO,J.&SÀEZ,L. Flora of Ecuador no.  (eds G. Harling & L. Andersson), pp. –. () Conservation assessment of Aquilegia paui (Ranunculaceae): Department of Systematic Botany, University of Gothenburg, a case study of an extremely narrow endemic. Oryx, , –. Gothenburg, Sweden. MARTINS, E.M., FERNANDES, F., MAURENZA, D., POUGY, N., LOYOLA, RENNER, S.S., STRIJK, J.S., STRASBERG,D.&THÉBAUD,C.() R. & MARTINELLI,G.() Plano de Ação Nacional para a Biogeography of the Monimiaceae (Laurales): a role for East Conservação do Faveiro-de-wilson (Dimorphandra wilsonii Rizzini). Gondwana and long distance dispersal, but not West Gondwana. Andrea Jakobsson Estúdio: Instituto de Pesquisa Jardim Botânico Journal of Biogeography, , –. do Rio de Janeiro, Rio de Janeiro, Brazil. THIERS,B.() Index Herbariorum: a global directory of public MENDES, S.P. () Implantação da APA Macaé de Cima (RJ): um herbaria and associated staff. New York Botanical Garden’s Virtual confronto entre a função social da priopriedade e o direito ao meio Herbarium. Http://sweetgum.nybg.org/science/ih/ [accessed  July ambiente ecologicamente preservado. V Encontro Nacional da ]. ANPPAS, Florianópolis, Santa Catarina, Brazil. VARTY,N.() Mollinedia stenophylla. The IUCN Red List of MMA (MINISTÉRIO DO MEIO AMBIENTE)() Espécies da flora Threatened Species : e.TA. Http://dx.doi.org/. brasileira ameaçadas de extinção. Instrução normativa n. ,de de /IUCN.UK..RLTS.TA.en [accessed  setembro de . January ]. MMA (MINISTÉRIO DO MEIO AMBIENTE)() Lista Nacional ZHANG, Q., LUO,X.&CHEN,Z.() Conservation and Oficial de Espécies da Flora Ameaçadas de Extinção. Portaria MMA reintroduction of Firmiana danxiaensis, a rare tree species endemic no. , Brasília, Brazil. to southern China. Oryx, , .

Biographical sketches sessments at CNCFlora, which supports the Brazilian Flora Red List Programme. G USTAVO M ARTINELLI is interested in mountain bio- E LTON J OHN DE L ÍRIO’ S research interests encompass systematics diversity, currently coordinates CNCFlora, and is the Brazilian focal and conservation of phanerogams. J OELCIO F REITAS is interested point for the Global Strategy for Plant Conservation. A RIANE L UNA in systematics and conservation of early diverging angiosperms. P EIXOTO specializes in systematic and conservation studies of R AQUEL N EGRÃO works as a data analyst for flora risk extinction as- phanerogams and in the history of botany.