A tribute to resistance: Eugenia quilombola (Myrtaceae), a new species with multilocular anthers from the Atlantic Forest of northeastern Brazil Author Amorim, Bruno S. 0000-0002-8109-9254 Programa de Pós-Graduação em Biotecnologia e Recursos Naturais da Amazônia (PPGMBT), Universidade do Estado do Amazonas, 69065 - 001, Manaus, Amazonas, Brazil & Museu da Amazônia, MUSA, 69099 - 415, Manaus, Amazonas, Brazil & brunosarim @ yahoo. com. br; https: // orcid. org / 0000 - 0002 - 8109 - 9254 brunosarim@yahoo.com.br Author Souza, Maria Anália Duarte De Universidade Federal do Amazonas, Departamento de Biologia (DB), 69067 - 005, Manaus, Amazonas, Brazil & analiaduarte @ ufam. edu. br; analiaduarte@ufam.edu.br Author Albuquerque, Patrícia Melchionna 0000-0001-8614-7676 Programa de Pós-Graduação em Biotecnologia e Recursos Naturais da Amazônia (PPGMBT), Universidade do Estado do Amazonas, 69065 - 001, Manaus, Amazonas, Brazil & palbuquerque @ uea. edu. br; https: // orcid. org / 0000 - 0001 - 8614 - 7676 palbuquerque@uea.edu.br Author Negrão, Raquel 0000-0002-4758-8038 Royal Botanic Gardens, Kew, Richmond, Surrey TW 9 3 AE, U. K & r. negrao @ kew. org; https: // orcid. org / 0000 - 0002 - 4758 - 8038 r.negrao@kew.org Author Giaretta, Augusto 0000-0002-8263-9806 Universidade Federal da Grande Dourados, Faculdade de Ciências Biológicas e Ambientais, Unidade II, 79804 - 970, Caixa Postal 364, Brazil & augustogiaretta @ gmail. com; https: // orcid. org / 0000 - 0002 - 8263 - 9806 augustogiaretta@gmail.com text Phytotaxa 2022 2022-04-08 543 1 31 40 http://dx.doi.org/10.11646/phytotaxa.543.1.3 journal article 54982 10.11646/phytotaxa.543.1.3 083d7adc-6d57-4916-a0e9-126d5261399d 1179-3163 6424314 Eugenia quilombola B.S.Amorim, M.A.D.Souza & Giaretta sp. nov. ( Figures 1 , 2 , 3 and 4 ). Type :— BRAZIL . Pernambuco : Mun. Lagoa dos Gatos , RPPN Pedra D’Anta , mata do Peru , 08º41’29”S , 35º51’35”W , 550–600 m elev., 23 November 2011 , fl., B . S . Amorim, D . Araújo , J . Viana & M . A . Chagas 1295 ( holotype : UFP !, isotypes: JPB !, NY !) . Eugenia quilombola is morphologically similar to E. umbrosa but differs by the multilocular anthers ( vs. rimose anthers), completely fused calyx with a visible seam between the lobes in the bud ( vs. free lobes or partially fused up to the lower third) and verrucose fruits ( vs. smooth). Treelet up to 7 m tall; bark grayish and longitudinally striate; young twigs terete, glabrous. Young leaves with whitish trichomes up to 0.1 mm , appressed, scattered, glabrescent. Leaf arrangement decussate, leaf blades obovate to oblong, 10.5–30 × 5.5–10 cm , chartaceous, pulverulent and puberulent with scattered appressed trichomes on both surfaces, apex acute, base cuneate; midrib flat to raised, pulverulent adaxially, raised and pulverulent with scattered trichomes abaxially; venation brochidodromous, secondary veins 10–15 pairs, marginal vein 3–4 mm from the margin, margin slightly revolute; petioles 0.8–1.1 cm long, terete, puberulent, glabrescent. Inflorescences fasciculiform or racemiform, sometimes the main axis recovers the vegetative growth in a auxotelic arrangement, axillary, rachis 3–29 mm long, bearing 2–3 pairs of flowers; bracts 1–5 × 1–1.5 mm , linear to lanceolate, puberulent, glabrescent; pedicels 8–13 × 1.5 mm , glabrous; bracteoles lanceolate to ovate, 1–2 × 1–1.5 mm , pubescent; hypanthium smooth, puberulent. Flower buds 10–12 × 6–8 mm , obpyriform, glandular dots inconspicuous, calyx lobes 4, completely fused before anthesis with a visible seam between the lobes, tearing regularly at anthesis in two unequal pairs in size, the external ones 7–8 × 5–6 mm , wide-elliptic, the internal ones 8–9 × 6–7 mm , wide-elliptic, apex rounded, and leaving an apiculum formed by the fusion of the external lobes, brownish pubescent indumentum outside, puberulent inside; petals 4, 5–10 × 5–6 mm , oblong or wide-obovate, glabrous; stamens ca. 8 mm long, anthers 1.5–3 mm long, multilocular; staminal ring 5 mm in diameter, rounded, glabrous; style 10–12 mm long, glabrous, stigma punctiform, ovary 2-locular, ovules not seen. Fruits ca. 3.3 × 2.2 cm , ellipsoid, verrucose, glabrous; seed one, ca. 13 × 18 mm , ellipsoid, maculate, glabrous, embryo with cotyledons completely fused and indistinguishable. FIGURE 1. Eugenia quilombola . Isotype: B.S. Amorim et al. 1295 . Image courtesy of the C. V. Starr Virtual Herbarium of The New York Botanical Garden (http://sweetgum.nybg.org/science/vh/) Affinities :— Eugenia quilombola resembles E. umbrosa by the petioles ca. 1 cm long and blade shape obovate to oblong with up to 30 cm long, secondary veins with ca. 15 pairs and marginal vein ca. 4 mm from the margin. They also share the fasciculiform inflorescence, flower with calyx lobes in two unequal pairs and ellipsoid fruits. It differs, however, by the morphological characters provided in the diagnosis. Furthermore, Eugenia quilombola , with a narrow distribution in the north portion of the Atlantic Forest in the states of Alagoas , Paraíba and Pernambuco is geographically apart from E. umbrosa , distributed along the lowland and montane forests of the states of São Paulo , Rio de Janeiro , Espírito Santo and Bahia . FIGURE 2. Eugenia quilombola . A. Detail of the bark. B. Leaf. C. Inflorescence with flower buds and an arrow showing the seam between the external (S1) and internal (S2) calyx lobes. D. Detail of flowers. E. Young fruits and an arrowhead showing a scar left by the fusion of the external calyx lobes along its boundary on the dorsal face of the internal calyx lobe. F. Mature fruit and remnant of the calyx lobes with an arrowhead indicating the scar (see the lighter apex) left by the fusion of the external calyx lobes along its boundary on the dorsal face of the internal calyx lobe (A, B, F from the B.S. Amorim et al.424 ; C–D from the holotype; E from B.S. Amorim et al. 1398 ). The pattern of calyx lobes fusion in the bud of Eugenia quilombola is formed by the fusion of the external calyx lobes along its boundary on the dorsal face of the internal lobes. This pattern of fusion leaves a scar on the dorsal lower third of the internal lobe that can be seen in the remnants of the calyx lobes (see arrowheads in Figure 2E–F ). The upper two thirds of the internal lobes are free, enclosed into the bud and cannot be seen before anthesis. Additionally, the upper portion of the external lobes is fused at each other forming a small apiculum. Recognizing external lobes in the bud is tricky in E. quilombola but the combination of the position of bracteoles and decussate arrangement supports the assignment of the apparently smaller lobe as the innermost (note that only two thirds can be seen in the flower bud, and they are apparently smaller than the external ones, but its total length is higher than the external lobes when is expanded after the anthesis. See Figures 2C, E–F ). A similar pattern of calyx fusion was described in E. atlantica Valdemarin & Sobral (in Valdemarin et al. 2019: 100 ) but it differs by the external lobes partially or completely fused while in E. quilomba they are completely fused. FIGURE 3. A–B. Details of Eugenia quilombola multilocular anthers. C. Electromicroscopy of multilocular anther in Eugenia sp. (A–B from the holotype: B.S. Amorim et al. 1295 ; C from Giaretta et al. in review.). Scale bars: A–B) 3 mm; C) 0.05 mm. FIGURE 4. Distribution map of Eugenia quilombola (red dots) in northern Atlantic Forest. Apart from these calyx features, the multilocular anther is the most striking characteristic used to recognize Eugenia quilombola ( Figure 3 ). This feature was reported in at least 24 families ( Endress & Stumpf 1990 , González & Rudall 2010 , Suaza-Gaviria et al. 2016 ) but has not been reported in Myrtaceae as far as we know. However,a similar “honey-comb” like anther has been cited in E. kerianthera M.A.D.Souza (in Souza et al. 2015: 90 ). It demands further investigation to elucidate its morphology, anatomy, and evolutionary significance in Myrtales where multilocular anthers were often recorded in neotropical Melastomataceae ( Baumgratz et al. 1996 , Michelangeli & Ulloa-Ulloa 2013 , Lima et al. 2019 ). Eugenia quilombola has an elongated style that stands the stigma over the stamens, a feature that has been associated to Eugenia sect. Umbellatae O. Berg (1855 –1856: 204; see Vasconcelos et al. 2018 ) and fasciculiform inflorescences, often observed in species of this section ( Mazine et al. 2016 ). Additionally, Eugenia umbrosa emerged within Eugenia sect. Umbellatae in previous phylogenetic reconstruction based on molecular sequence ( Mazine et al. 2018 , Giaretta et al. 2019b ), which hypothesizes the phylogenetic placement of Eugenia quilombola in this section. Geographic Distribution and Ecology :— Eugenia quilombola is found in lowland and submontane forests of the northeastern Brazilian states of Alagoas , Pernambuco and Paraíba ( Figure 4 ). Despite several places of collections, this species generally occurs in the interior of well-preserved forest fragments, except of recently fragmented areas where individuals can be found on the edge. Eugenia quilombola was observed with flowers from October to May and with fruits from December to July. Conservation status :—Although Eugenia quilombola has records to the lowland and submontane forest of Alagoas , Paraíba and Pernambuco states, we consider the population in the southern portion of Paraíba (collection Carrazzoni 244 ) as possibly extinct, considering that the species was formerly known or thought very likely to occur in the area, but it is most likely now extirpated from the area because habitat loss ( Souza et al. 2020 ) and owing a lack of records in the last 50 years (B.S. Amorim, pers. observ.). In this case, its estimated extent of occurrence (EOO) ranges between 26,791 km 2 to 20,998 km 2 , nearly falling into the thresholds of the Vulnerable category under the criterion B. Its estimated area of occupancy (AOO) ranges between 172 to 176 km 2 , and there are more than 10 known locations, although without evidence of severely fragmented populations or extreme fluctuation. The real estate speculation related to tourism, residential and urban expansion in this area is the main threat and cause of habitat loss and fragmentation to all lowland coastal forest of Northeastern Brazil , where this species is known to occur, from what a continuing decline of habitat quality is inferred. Therefore, E. quilombola is here rated as Near Threatened (NT), according to IUCN (2001) conservation criteria, as it nearly meets the criterion B1b(iii)+B2b(iii) regarding its restricted distribution and inferred continuing decline of habitat. Despite its narrow occurrence, it’s important to reinforce that this species is recorded in protected areas of Alagoas (AL) and Pernambuco (PE) states, such as REBIO (Reserva Biológica) Pedra Talhada (AL), RPPN (Reserva Particular de Proteção Natural) Frei Caneca (PE), RPPN Garabu (AL), RPPN Pedra D’Anta (PE), Serra D’Água Ecological Sanctuary (AL), Estação Ecológica Tapacurá (PE), and forest fragments of Usina São José (PE), and Usina Serra Grande (AL). It also occurs in large sustainable use areas such as APA (Área de Proteção Ambiental) do Catolé e Fernão Velho (AL), Dois Irmãos Zoo (PE), ESEC (Estação Ecológica) Murici Ecological Station (AL), and Recife Botanical Garden (PE). It is strongly recommended further fieldwork across its range, especially in the habitat types where the species was not collected for more than 30 years, to confirm potential local extinction and to support conservation action plans to prevent the species going to higher risk categories in a near future. Etymology :—The epithet refers to the inhabitant of quilombos (called ‘quilombolas’ in Portuguese) who are descendants of Africans in America. The quilombos are settlements founded by escaped enslaved communities in colonial Brazil , during Portuguese rule. This act of resistance kept their culture and religion alive, and they continued to exist even after the end of the slavery. Currently, there are 3,475 quilombola communities spread all over the country (FCP 2021). The distribution range of E. quilombola is known to be similar to the range of quilombola communities in northeastern Brazil , and similarly managed to resist and survive all this time living near forest fragments. This epithet also makes reference to the period Brazil is going through, in which Brazilians have to fight for survival during a criminal, careless and inefficient government, with more than half a million deaths caused by the SARS-CoV-2. Paratypes :— BRAZIL . Alagoas : Mun. Barra de Santo Antônio , Fazenda São Brás , 15 October 1998 , fl., R . P . Lyra-Lemos & M . N . Rodrigues 3949 ( JPB !, HUEFS-image!, MAC-image!); mun. Branquinha , Fazenda Riachão , 17 March 2002 , fr., R . P . Lyra-Lemos , W . W . Thomas , M . R . Barbosa & M . Rodal 6328 ( MAC !); mun. Chã Preta , Serra Lisa , 6 May 2009 , fr., Chagas-Mota & N . Ramos 3496 (MAC-image!); mun. Flexeiras , Fazenda Triunfo , 12 February 2011 , fr., R . C . Pinto , J . W . A . Silva & A . S . Costa 93 (MAC-image!); ibidem , ESEC Murici , Fazenda Ibiquara , 20 January 2011 , fl. & fr., Chagas-Mota , R . C . Pinto & J . M . Ferreira 10085 (MAC-image!); ibidem , 12 April 2011 , fr., Chagas-Mota , R . C . Pinto & J . M . Ferreira 10774 (MAC-image!); mun. Ibateguara , 11 December 2010 , fr., Chagas-Mota , J . W . A . Silva & J . M . Ferreira 9729 (MAC-image!); ibidem , Usina Serra Grande , Coimbra , 12 March 2003 , fr., M . Oliveira & A . A . Grillo 1321 ( JPB , MAC-image!); mun. Maceió , 22 December 2007 , fl., W . S . Ferreira-Júnior 86 (MAC-image!); ibidem , Fazenda Boa Vista , Usina Cachoeira , 5 April 2008 , fr., W . S . Ferreira-Júnior & J . Y . A . Galdino 108 (MACimage!); ibidem , Serrada Saudinha , 13 November 2008 , fl., Chagas-Mota, D. S . Correia & P . B . Alves 1541 (MACimage!); ibidem , Tabuleiro dos Martins , 2 January 1992 , fl., R . P . Lyra-Lemos 2570 (MAC-image!); mun. Matriz do Camaragibe , 16 May 2005 , fl., G . B . Araújo & F . Cavalcante 87 (MAC-image!); ibidem , 9 May 2009 , fl., J . W . A . Silva , E . C . O . Chagas & M . C . S . Mota 164 (MAC-image!); ibidem , Santuário Ecológico da Serra D’Água , 18 October 2003 , fr., R . P . Lyra-Lemos 8067 (MAC-image!); mun. Murici , 9 November 2005 , fl., N . T . Mendonça 246 ( MAC , image!); ibidem , ESEC Murici , Mata das Bananeiras, 2 April 2013 , fl., B . S . Amorim , J . L . Costa-Lima & E . Pessoa 1795 ( UFP !); ibidem , 1 December 2016 , fl., M . Figueira & B . Schindler 538 ( JPB ); mun. São Luiz do Quintude , Usina Santo Antônio , RPPN Garabu , 26 January 2008 , fl., R . P . Lyra-Lemos , P . B . Alves & Chagas-Mota 10860 (MAC-image!); mun. Satuba , APA Catolé e Fernão Velho , 29 October 1998 , fl., M . N . Rodrigues , R . P . Lyra-Lemos , S . Costa & S . Rocha 1324 (HUEFS-image!, MAC-image!); mun. Quebrangulo , Reserva Biológica de Pedra Talhada , Mata próxima à Pedra Talhada , 600–650 m alt., 15 May 2009 , fr., B . S . Amorim & A . Alves-Araújo 455 ( HST , UFP !); ibidem , 24 January 2012 , fr., B . S . Amorim , A . A . Araújo , C . Araújo , V . S . Sampaio & M . A . Chagas 1398 ( JPB , MO , NY !, UFP !); ibidem , 20 December 2012 , fl., B . S . Amorim , J . L . Costa-Lima , L . A . Pereira & M . A . Chagas 1713 ( JPB , NY !); ibidem , 17 October 2014 , fl., L . Nusbaumer 4182 ( JPB , MAC-image!, NY-image!, UFP !); mun. Rio Largo , Flexa , 22 October 2010 , fl., Chagas-Mota & C . Couto 9164 (MAC-image!); mun. Viçosa , Fazenda Jussara , 25 november 2010 , fr., Chagas-Mota & J . M . Ferreira 9619 (MAC-image!). Paraíba : s. loc., Km 231 estrada João Pessoa , Recife , 14 October 1974 , fl., E . Carrazzoni 244 ( IPA !) . Pernambuco : s. loc., Caxanga Wood , 1887, fl., H . N . Ridley , T . S . Lea & G . A . Ramage ( BM 001254017 !); mun. Água Preta , Fazenda Camarão , 25 October 2012 , fl., R . A . Pontes & A . Vicente 831 ( JPB , NYimage!); ibidem , 2 January 2013 , fl., fr., R . A . S . Pontes 854 ( JPB , NY-image!); mun. Igarassu , Usina São José, Mata de Macacos , 16 April 2008 , fl., J . Irapuan & J . S . Marques 12 ( IPA !); ibidem , Mata de Pezinho , 15 February 2008 , fr., A . Alves-Araújo , & J . S . Marques 875 ( UFP !); ibidem , Mata de Piedade , 31 January 2002 , fr., S . G . Freire , H . C . H . Silva & H . M . C . Fernandes 38 (BHCB-image!); ibidem , 2 March 2009 , fr., A . A . Araújo & A . Melo 1167 ( UFP !); ibidem , Mata de Vespas , 30 October 2007 , fl., J . S . Marques & N . A . Albuquerque 262 ( IPA !); ibidem , 12 March 2009 , fl. & fr., B . S . Amorim , T . A . Pontes , J . D. Garcia & J . Novaes 424 ( UFP !); ibidem , Mata de Zambana , 29 November 2008 , fr., M . A . M . Silva , P . G . A . Mendes & T . N . F . Guerra 38 ( PEUFR , UFP !); ibidem , 28 March 2003 , fl., G . L . Bezerra & A . Melquíades 177 ( PEUFR ); mun. Jaqueira, RPPN Frei Caneca , Próximo a Barragem das Moças , 11 March 2011 , fr., B . S . Amorim , A . V . Melo , E . M . Pessoa & M . A . Chagas 818 ( JPB , UFP !); ibidem , Mata do Quengo , 30 January 2013 , fl., B . S . Amorim , J . L . Costa-lima , E . M . Pessoa , D. A . Araújo , S . N . Moreira & M . A . Chagas 1757 ( JPB , UFP !); mun. Lagoa dos Gatos , RPPN Pedra D’Anta , 18 December 2010 , fl., J . L . Viana 246 ( JPB ); ibidem , 23 November 2011 , fl., B . S . Amorim, D . Araújo , J . L . Viana & M . A . Chagas 1398 ( JPB , UFP !); mun. Paudalho , Matas de Bicopeba , 14 October 1965 , fl., G . Teixeira 2891 ( PEUFR ); mun. Paulista , Loteamento Alto do Morumbi , 2 March 2002 , fr., M . F . A . Lucena , A . Araújo & J . E . Araújo 954 ( UFP !); mun. Recife , Curado , Campus do Comando Militar do Nordeste, 26 July 1999 , fr., C . Eugênio & C . Ferreira 67504 ( IPA ); ibidem , Dois Irmãos , 4 April 1966 , fr., G . Mariz s.n. ( IPA 13991); ibidem , s. loc., 25 August 1967 , fl., A . Lima 5073 ( HUFSJ , IPA !); ibidem , Engenho São João , 3 December 2007 , fl., E . P . Queiroz & W . R . L . Filho 2552 (BHCB-image!); mun. Rio Formoso , Cupe , Praia de Muro Alto , 6 February 1970 , fl., Andrade-Lima 70-5702 ( IPA !); ibidem , 6 February 1970 , fl., Andrade-Lima 70-5703 ( IPA !) ibidem , mun. São Lourenço da Mata , Estação Ecológica de Tapacurá , 10 October 2000 , fl., T . M . C . Silva & K . Almeida 26 ( IPA , JPB , PEUFR , SP-image!); ibidem , 28 May 2000 , fr., K . Ameida 47 ( PEUFR , SP-image!); ibidem , 20 October 2000 , fl., E . S . da Silva 29 ( PEUFR ); ibidem , s.d., K . Almeida 113 ( JPB , PEUFR , SP-image!); ibidem , 23 February 2022 , fr., J . R . Maciel & L . M . Nascimento 2030 ( UFP ); mun. Tamandaré , Mata de Pau Amarelo , 14 January 2000 , fl., M . F . A . Lucena 820 ( PEUFR ) .