Celtis atlantica (Cannabaceae): A new endangered tree species from southwest of Brazil

Abstract

During the Neotropical review of Celtis, a new species (Celtis atlantica) endemic and endangered to southeastern Brazil was discovered. A morphological description, a distribution map, conservation status, taxonomic notes, illustrations, and an identification key of the Celtis from the Southern Cone and Brazil are provided.

Keywords:
Atlantic rainforest; Brachyteles hypoxanthus; Cannabaceae; Celtis; Cerrado; endocarp; Mertensia; Neotropics; taxonomy; and Urticalean

Introduction

Celtis L. is a monophyletic genus belonging to Cannabaceae. The genus has 64 species distributed in worldwide (Fu et al. 2022). In Brazil, Celtis is represented by 13 species, distributed in all phytogeographical regions of the country (Zamengo et al. 2023 a ). Celtis can be recognized mostly by: shrubs to trees, monoecious, armed or unarmed; leaves estipulate, alternate, trinervate, domatia present or not; inflorescences solitary or in pairs, unisexual flowers; dialysepal calyx, sepals 5, corolla absent; stamens 5 and opposite to the sepals; ovary bicarpellate, uniovulate, stigma entire or bifurcate; fruits small drupes with petrous endocarp (Berg & Dahlberg 2001; Chamorro et al. 2021; Leme et al. 2020; 2021; Zamengo et al. 2020; 2021).

Since the beginning of the 21st century, the number of Neotropical species of Celtis has been questioned (Berg & Dahlberg 2001; Torres & Luca 2005; Henrickson 2010; Pederneiras et al. 2011; Oakley & Prado 2013; Ayala 2015; Asmus et al. 2018; Chamorro et al. 2021; Chamorro 2022; Zamengo et al. 2020; 2023a; b). From this scenario, Zamengo (in prep) proposed to revise the Neotropical names of Celtis.

Among the names that are being revised, Celtis orthacanthos Planchon (described for the state of Bahia), Celtis utilis (Cisneiros) Caminhoá (≡Mertensia utilis Cisneiros) and Ziziphus allemaovii Glaziou (both described for the state of Rio de Janeiro) stand out. Regarding protologues and types, Planchon (1848) cites the Salzmann s.n. collection from the Hookerianum herbarium (currently in K, under barcode numbers 000512940!, and 000964265!); Cisneiros (1846) provides a description (Fig. 1 A ) and an illustration of the species (Fig. 1 B ) without designating any material (type or not) or herbarium of deposit; Caminhoá (1881) mentions the phytotherapeutic uses of C. utilis (Fig. 1 C ), without designating any material (type or not) or herbarium of deposit; and Glaziou (1905) provides a diagnosis (“Grand arbre”) for Z. allemaovii (Fig. 1 D ) and mentions that the specimen Glaziou 18991a collected is deposited in herbaria B, K, and P (only P's specimen was located by the curators).

Figure 1.
Protologues of Mertensia utilis Cisneiros, Celtis utilis (Cisneiros) Caminhoá, and Ziziphus allemaovii Glaziou. A. Protologue of Mertensia utilis. B. Illustration of Mertensia utilis. C. Protologue of Celtis utilis. D. Protologue of Ziziphus allemaovii.

Of these four names, only C. orthacanthos is considered a legitimate name, as it is in accordance with the ICBN rules (Turland et al. 2018). With regard to M. utilis Cisneiros, Zamengo et al. (2023 b ) classified it as nomen nudum, which is incorrect, as this “name” was never, in fact, published (Art. 12.1., Turland et al. 2018). Cisneiros restricted the name to the National Library of Rio de Janeiro, without wide distribution and, does not meet the of Article 29.1. (Turland et al. 2018). This type of “name” is known as a designation, as it does not have nomenclatural status (Art. 6.3., Turland et al. 2018). Furthermore, C. utilis must be considered a nomen nudum since Caminhoá (1881) did not include a description, diagnosis or any material reference, which does not satisfy Articles 38.1. and 38.3. (Turland et al. 2018). Finally, Z. allemaovii is considered a name not validly published, since the article of Glaziou (1905) is considered suppressed (“opera utique opressa”, Art. 34.1., Turland et al. 2018) (Mansano & Pederneiras 2016).

In the latest review of Celtis subg. Mertensia Planch., Berg and Dahlberg (2001) grouped C. utilis (≡M. utilis) and Z. allemaovii in the section "Nomina nuda and/or nomina in schedula" and considered these names to be synonyms of C. orthacanthos. After noting that M. utilis cannot be recognized as a name, that C. utilis is a nomen nudum and that Glaziou's species (Glaziou 18991a) is a species of Celtis and not of Ziziphus Miller, we propose Celtis atlantica sp nov. as a new species belonging to Celtis subg. Mertensia.

Materials and methods

The specimens were analyzed in person or using high-resolution images from the herbaria BHCB, CVRD, ESA, HUENF, IAC, K, NY, P, PMSP, RB, SP, SPF, SPSF, UEC, and US (acronyms according to Thiers 2023).

To standardize the terminology referring to the habit and the types of spines we followed Chamorro et al. (2021), the stem surfaces are according to Beentje (2016), for the types of domatia we adopted O'Dowd and Wilson (1989), for the patterns of indumentum and leaf-forms we followed Radford et al. (1974) and for colors, leaf apex, leaf base, leaf margins, leaf surfaces, leaf textures, inflorescence type, stigma divisions, fruit, and pyrene shapes we adopted Beentje (2016), pyrene ornamentations are according to Chamorro et al. (2021). For the extractions and cleaning of the pyrenes, the methodologies of Zamengo et al. (2020) were adopted.

To avoid repetitions during the taxonomic description, all colors of the structures were observed in natura or in sicco, and all trichomes mentioned in the description are ivory. The abbreviations (fl.) and (fr.) were used in the "Additional specimens examined (Paratypes)" list to cite the phenological status of the analyzed specimens. Specimens that do not have this abbreviation were collected in a vegetative state. The map was made with the program QGis 3.22.1.

Results

Taxonomic treatment

Celtis atlantica Zamengosp. nov. TYPE: BRAZIL. RIO DE JANEIRO: Rio de Janeiro, Alto da Boa Vista, Estrada Dona Castorina, Trilha em direção às cachoeiras da Gruta e dos Primatas, à direita do primeiro córrego de água, 22°57'55.2"S 43°14'57.8"W, 16.V.2023, fr., H.B.Z. Souza 230 (holotype: RB herbarium number 850940, barcode number 01490789; isotypes: IAC, K, MBM, MO, NY, P, PMSP, R, SP, SPF, US). Figs. 2, 3, 4, 5, 6, 7.

Popular names: caboco, guajissara, limoeiro, limoeiro-silvestre, and juá preto.

Diagnosis: Among the Celtis species, C. atlantica is similar to Celtis tala Gillies ex Planch. because they are the only armed species to present an arboreal habit, despite this similarity, C. atlantica differs by presenting: limb 6-12.5 × 2-5 cm vs 1.7-3.5 × 0.8-1.5 cm, apex acuminate to caudate vs acute to attenuate, base attenuate to cuneate vs obtuse, domatias inconspicuous vs conspicuous; pistillate flowers with style conspicuous vs style absent, stigmatic lobes bifid vs bilobed; pyrene monoapiculate vs without apiculum, respectively.

Figure 2.
Main characteristics of Celtis atlantica Zamengo. A. Habit. B-C. Bark. D. Branch with lenticels. E. Detail of the lenticels. F. Spines. G. Limb. G1. Adaxial surface trichomes. G2. Abaxial surface trichomes. G3. Domatias. H. Cyme. I. Staminate flower. J. Pistillate flower. K. Drupe. L. Pyrenes. L1. Pyrene verrucose. L2. Pyrene verrucose evidencing the suture.

Description: Trees 6-30 m tall, scaly wood, secondary and tertiary branches fawn or vinaceous, sinuous, entire, glabrous to subglabrous; branches armed, spines 1-13 mm length, in pairs or solitary, straight, vinaceous, glabrous to subglabrous, trichomes scarce both at the base and on the entire surface of the spines. Petiole 1-5 mm length, glabrous to subglabrous, limb elliptic, 6-12.5 × 2-5 cm, membranaceous, apex acuminate or caudate, base symmetric, attenuate or cuneate, margins with teeth, crenate-serrate or serrate, teeth congested or lax emerging from the lower third to the upper third, from the middle portion to the upper third, and/or restricted to the upper third, surfaces concolorous (both emerald or olive in natura or both buff, cinnamon, coppery, olive or stramineous in sicco), adaxial surface shiny, glabrous to subglabrous, trichomes concentrated on the veins and scarce on the laminar surface, adaxial surface smooth to the touch in sicco, abaxial surface glabrous to subglabrous, trichomes concentrated on the veins and scarce on the laminar surface, abaxial surface smooth to the touch in sicco, veins salient, chestnut or stramineous contrasting in relation to the abaxial surface, domatias in pockets, inconspicuous, glabrous to subglabrous, trichomes ciliate or arranged over the entire surface of the domatia. Inflorescence in cymes dichotomous or in glomerule, peduncle 2-3 mm length, subglabrous, not bracteolate. Staminate flowers with pedicels 1-1.5 mm length, subglabrous, bracteolate, abaxial surface of the sepals glabrous to subglabrous, margins entire. Pistillate flowers with pedicels 2-3.5 mm length, subglabrous, ovary 1.5-3 × 0.75-1.5 mm, glabrous to subglabrous, trichomes scarce both at the base and on the ovary surface, ovary surface smooth to the touch in sicco, style conspicuous (0.6-1 mm length), stigmate branches supported by the style, 3-4 mm length, stigmate lobes bifid (incisions 1-1.5 mm deep). Pedicels of the drupe with 3-3.5 mm length, glabrous to subglabrous, mature drupes lemon or primrose in natura, ovate, 10-13 × 5-11 mm, epicarp glabrous to subglabrous, trichomes scarce both at the base and on the epicarp surface, epicarp surface smooth to the touch in sicco, deciduous sepals at the base, mesocarp non-viscous, membranaceous, not ornamented, pyrene ivory, ovate, 5.5-10 × 5.5-7, apiculate, monoapiculate, apiculum aciculate, 0.5-1 mm length, apex rounded, apiculum scar absent, pyrene surface verrucose, randomly distributed warts.

Distribution and habitat: Celtis atlantica is endemic to Brazil occurring in the Cerrado and Atlantic Forest biomes (Fig. 3 A ). The type specimen was collected in Parque Nacional da Tijuca (Rio de Janeiro, Fig. 3 B ). Unlike most of Celtis Neotropical species, C. atlantica occurs within the forests (with little incidence of light), most occasionally the species is associated with humid environments (waterfalls and water streams, Fig. 3 C ). Two of the three specimens collected in the Cerrado do not have information about the phytophysiognomies in which C. atlantica was collected, only the sample Barreto et al. 393 (ESA) mentions that C. atlantica was collected in semi-deciduous mesophyll forest. For the states of Minas Gerais, Rio de Janeiro (Fig. 3 B ) and São Paulo the species was collected in areas of rainforest (at sea level), for the state of Espírito Santo, the species was collected in areas of up to 200 m altitude recognized as “Mata de Tabuleiro”.

Figure 3.
Distribution map of Celtis atlantica Zamengo and Brachyteles hypoxanthus Kuhl. A. Distribution map of Celtis atlantica Zamengo. B. Parque Nacional da Tijuca. C. Habitat of Celtis atlantica Zamengo. D. Brachyteles hypoxanthus Kuhl, photo by Henrique Junior. E. Distribution map of Brachyteles hypoxanthus, states of Espírito Santo, Minas Gerais and Rio de Janeiro.

The areas of occurrence of C. atlantica may be associated with its dispersers, since the label of specimen J. Gomes 118 (BHCB04766!) mentions Mamaliocoria dispersal by Brachyteles hypoxanthus (Kuhl, 1820, Fig. 3 D -E). This same species of monkey was observed eating the fruits of C. atlantica by Dr. Karen Strier during her doctoral project at the Caratinga Biological Station (between June 1983 and July 1984).

Additional specimens examined (Paratypes): BRAZIL. Espírito Santo: Linhares, estrada de Linhares a Regência, -39.7555 S, -78.41769 W, 15 January 2014, (fr.), D.A. Folli 7165 (CVRD!, RB!). Minas Gerais: Caratinga, Estação Biológica de Caratinga, mata do Jaó, 20 November 2012, (fr.), F.R. Couto 159 (BHCB!); idem 19°50’ S, 41°50’ W, 23 April 1994, J. Gomes 118 (BHCB!); idem 1 April 1984, (fr.), K.B. Strier 613 (BHCB!, NY!); idem 19°40’ S, 41°50’ W, 25 March 1984, (fr.), K.B. Strier 836 (NY!). Rio de Janeiro: Cachoeiras de Macacu, Estação Ecológica Estadual do Paraíso, acima da represa CEDAE, 9 June 1992, B.C. Kurtz et al. s.n. (RB barcode 00439269!). Campos dos Goytacazes, Mata do Mergulhão, 21°46’42” S, 41°15’27” W, 10 June 2003, M.T. Nascimento & G.R. Rabelo 34 (HUENF!), Maciço do Itaóca, 21°47’50” S, 41°26’53” W, 3 August 2012, T.P. Souza 1221 (HUENF!). Guapimirim, Estação Ecológica Estadual de Paraíso, parcela 2B, área 02B, 22°26’0” S, 42°50’0” W, 26 September 1991, (fl.), C.M. Vieira et al. 118 (RB!); parcela 7A, área 07A, 22°26’0” S, 42°50’0” W, 24 October 1991, (fl.), C.M. Vieira et al. 142 (RB!). Magé, Paraíso, Centro de primatologia (CPRJ), Serra dos Porcos, 12 November 1984, H.C. de Lima et al. 2399 (RB!). Rio de Janeiro, matas do Sumaré, 3 September 1927, (fl.), Pessoal do Horto Florestal s.n. (K barcode 000964290!, NY barcode 00476067!, P barcode 06781657!, RB barcode 00439263!); Tijuca, mata do pai Ricardo, perto da sede do horto florestal, 3 September 1927, (fr.), Paulim 1566 (RB!). São Francisco de Itabapoana, fazenda Santo Antônio, 21°17’49” S, 41°5’25” W, 17 June 2009, K.M.P.A. Archanjo & M.T. Nascimento 337 (HUENF!); fazenda Imburi, 21°19’32” S, 41°6’0” W, 9 August 2008, K.M.P.A. Archanjo & M.T. Nascimento 1129 (HUENF!); 21°19’32” S, 41°6’0” W, 9 August 2008, K.M.P.A. Archanjo & M.T. Nascimento 1821 (HUENF!); fazenda Palmeiras, 21°19’18” S, 41°7’11” W, 13 October 2008, K.M.P.A. Archanjo & M.T. Nascimento 2047 (HUENF!). São Pedro da Aldeia, Assentamento Ademar Moreira, -22.718569 S, -42.119600, 27 March 2021, H.B.Z. Souza & F.M. Bastos 147 (PMSP!, RB!). Serra do Gericinó, 15 June 1982, fr., A. Glaziou 18991a (P!). Volta Redonda, floresta da Cicuta vale do Paraíba do Sul, 22°33’2” S, 44°5’0” W, 26 September 2001, (fl.), G.R. de Souza et al. 60 (RB!). São Paulo: Americana, Carioba, Mata Boa Esperança, 21 May 1943, M. Kuhlmann 852 (IAC!, SP!). Amparo, Monte Alegre, mata da fazenda Santa Isabel, 28 August 1943, (fr.), M. Kuhlmann 991 (IAC!, SP!). Anhembi, mata da fazenda Barreiro Rico, 5 October 1956, (fl., fr.), M. Kuhlmann 3956 (IAC!, SP!). Campinas, mata da Fazenda Santana do Atalaia, fragmento M4, 22°48’ S, 46°53’ W, 10 June 2000, K. Santos & R. Balinello 1955 (UEC!); mata da Fazenda Santa Helena, fragmento P1, 22°54’ S, 46°54’ W, 16 June 2000, K. Santos & R. Balinello 2274 (UEC!); 27 July 2006, L.T. Vieira & L.P. Sims 335 (UEC!); mata Ribeirão Cachoeira, August 2008, L.P. Sims & J. Melis 1406 (UEC!); mata Santa Genebra, 1984-1985, J.Y. Tamashiro et al. 110, 250, 1053 (UEC!). Charqueada, Mata da Glória, 14 May 1993, K.D. Barreto et al. 393 (ESA!). Limeira, Fazenda Morro Azul, 5 October 1956, (fr.), M. Kuhlmann 2879 (SP!). São Paulo, Jardim Botânico de São Paulo, September 1942, (fl.), O. Handro s.n. (IAC herbarium number 54003!, NY barcode 00777749!, P barcode 06781154!, SP herbarium number 35604!, SPF herbarium number 148257!). Without locality, September 1942, (fl.), D.G.S. Camargo 608 (SPSF!). Unknown location: October 1822, (fl.), L. Riedel (NY barcode 02429058!, US barcode 1328438!); “prope mandioca”, October 1922, (fl.), L. Riedel (US barcode 01328438!); October 1923, (fl.), L. Riedel (NY barcode 02429055!, NY barcode 02429058!); 3 September 1927, (fl.), s.c (RB barcode 004392!, RB barcode 00439263!).

Conservation status: Celtis atlantica is known from 39 specimens and 19 localities from southeastern Brazil (Fig. 3 A ). Using GeoCAT (Bachman et al. 2011) and a 2 km² grid, it has an estimated extent of occurrence (EOO) of 209,878.228 km² and minimal area of occupancy (AOO) of 116 km².

The main biome present in this region is the Atlantic Forest which continues to be fragmented with the implementation of agricultural, farming, and cities. Due to deforestation, C. atlantica presents a fragmented distribution (Fig. 3 A ), occurring in isolated areas which are subject to different threats. For example, in remnants of Rio de Janeiro state (Parque Nacional da Tijuca) the species is threatened by the invasion of Artocarpus heterophyllus Lamarck, which was introduced in Brazil more than 200 years ago (Sartorelli et al. 2018).

Of the 39 specimens, 29 have a locality designation. Of these 29 specimens, 13 were collected in protected areas (Conservation Units) belonging to the states of Minas Gerais (Caratinga Ecological Station) and Rio de Janeiro (Floresta da Cicuta Area of Relevant Ecological Interest, Paraíso State Ecological Station, Tijuca National Park and Serra do Mendanha Municipal Natural Park).

As for the other 16 specimens, these were collected in Cerrado fragments located in the interior of the state of São Paulo, that are surrounded by agricultural, farming and/or urban areas. New expeditions are needed to learn more about the Cerrado's phytophysiognomies, as the labels of the specimens from these localities do not contain any information about the biome's phytophysiognomies. Based on this scenario, we recommend that C. atlantica be assessed as endangered (B1ab(i, ii, iii, iv)+2ab(i, ii, iii, iv)), based on the IUCN (2022).

Etymology: The epithet "atlantica" was attributed in allusion to the main biome where the species occurs.

Phenology: The species has flowering records for the months of September and October, while the fruit was collected in January, March, April, June, August, September, October and November.

Taxonomic notes: Analyzing herbarium specimens, we observed that C. atlantica is frequently confused with C. orthacanthos (due to the misinterpretation of Berg & Dahlberg 2001) and with C. tala. To distinguish these species, we suggest that some characteristics be compared (habit, leaves (length × width, apex and base, Fig. 4 A ), pistillate flowers (ovary indumentum, style length, degree of incision of stigmatic lobes, Fig. 4 B ), mature drupe (size), pyrene (size, form, presence of apiculum, presence of apiculum scar and ornamentations, Fig. 4 C ), and areas of distributions (Fig. 4 D , Table 1).

Figure 4.
Main differences between Celtis atlantica Zamengo, Celtis orthacanthos Planch., and Celtis tala Gillies ex Planch. A. Leaves. A1. Celtis atlantica. A2. Celtis orthacanthos. A3. Celtis tala. B. Pistillate flowers. B1. Celtis atlantica. B2. Celtis orthacanthos. B3. Celtis tala. C. Pyrenes. C1. Celtis atlantica. C2. Celtis orthacanthos. C3. Celtis tala. D. Distribution map of Celtis atlantica, Celtis orthacanthos and Celtis tala.

Table 1.
Main morphological differences between C. atlantica, C. orthacanthos and C. tala.

Characteristic	C. atlantica	C. orthacanthos	C. tala
Habit	Tree not climbing	Climbing shrub	Tree not climbing
Leaf (size cm)	6-12.5 × 2-5	4-12.5 × 1.5-5.5	1.7-5 × 0.8-2.5
Leaf (apex)	Acuminate to caudate	Acuminate	Acute to attenuate
Leaf (base)	Attenuate to cuneate	Obtuse, rounded to sub-cordate	Obtuse
Perfect flower (indumentum ovary)	Glabrous to subglabrous	Subglabrous to pilose	Glabrous to subglabrous
Pistilate flower (length of style)	0.6-1 mm	0.6-1 mm	Null
Pistilate flower (stigmatic lobes)	Bifid (1-1.5 mm deep)	Bifid (3-4 mm deep)	Bilobate (0.1-0.5 mm deep)
Drupe (size mm)	10-13 × 5-6.5	11.5-13 × 9.5-10.5	4-7 × 3-5
Pyrene (size mm)	5.5-10 × 5.5-7	7-9 × 5-6	3.5-4 × 3-4
Pyrene (form)	Ovate	Ovate	Globose
Pyrene (apiculum)	Present	Present	Absent
Pyrene (apiculum scar)	Absent	Present	Absent
Pyrene (ornamentation)	Verrucose	Alveolate-crateriform	Verrucose
Distribution areas	Southeast Brazil	Southeast and Northeast Brazil	Southern Bolivia and Brazil, eastern, central and western Argentina, and throughout Uruguay

Below we provide the new identification key, contemplating the new species and all the others currently recognized (Chamorro et al. 2021; Zamengo et al. 2023 a ). We did not include Celtis iguanaea (Jacquin) Sargent since we believe that this species does not occur in these regions (see Zamengo et al. 2020; Chamorro et al. 2021). Based on the results obtained by Fu et al. (2022), we also excluded Celtis schippii Standley. For the characteristics related to fruits and endocarps, see Fig. 7.

Figure 5.
Holotype of Celtis atlantica Zamengo.

Figure 6.
Illustration of Celtis atlantica Zamengo. A. Branch. B. Leaf. C. Domatia. D. Staminate flower. E. Pistillate flower. F. Drupe. G. Pyrene. Illustrator: Klei Rodrigo Sousa.

Figure 7.
Drupes and pyrenes of Celtis species currently accepted for Brazil and the Southern Cone. A-B. Celtis atlantica. C-D. Celtis brasiliensis. E-F. Celtis chichape. G-H. Celtis clausseniana. I-J. Celtis flavovenarum. K-L. Celtis fluminensis. M-N. Celtis lancifolia. O-P. Celtis orthacanthos. Q-R. Celtis pallida var. discolor, white arrow indicating the foliated brachyblast. S-T. Celtis pallida var. pallida. U-V. Celtis serratissima. W-X. Celtis spinosa. Y-Z. Celtis spinosissima. AA-AB. Celtis tala.

Key to the species of Celtis from Brazil and Southern Cone

1. Trees ............................................................................................................................. 2

2. Limb 6-12.5 × 2-5 cm, apex acuminate to caudate, base attenuate to cuneate, domatias inconspicuous; style conspicuous, stigmatic lobes bifid; pyrene monoapiculate .......................................................................................................................... C. atlantica

2’. Limb 1.7-3.5 × 0.8-1.5 cm, apex acute to attenuated, base obtuse, domatias conspicuous; style absent, stigmatic lobes bilobed; pyrene without apiculum ......... C. tala

1. Shrubs ........................................................................................................................... 3

3. Foliated brachyblasts present; pyrenes cream .............................................................. 4

4. Limb discolorous, abaxial surface pubescent to velutinous ........ C. pallida var. discolor

4’. Limb concolorous, abaxial surface glabrous to pilose ................. C. pallida var. pallida

3’. Foliate brachyblasts absent; pyrenes ivory .................................................................. 5

5. Adaxial lamina surface scabrous in sicco ..................................................................... 6

6. Abaxial lamina surface scabrous in sicco ............................................. C. flavovenarum

6’. Abaxial lamina surface lanate in sicco ........................................................................ 7

7. Branches, spines, flowers and drupes with trichomes chestnut in sicco .... C. fluminensis

7’. Branches, spines, flowers and drupes with trichomes ivory or lemon in sicco ........... 8

8. Mature drupe orange in natura, pyrene surface alveolate to smooth ....... C. serratissima

8’. Mature drupes lemon, primrose or saffron in natura, pyrenes surfaces alveolate-crateriform, alveolate-crateriform-verrucose or verrucose ............................................... 9

9. Drupe surface lanate in sicco; pyrene bi-apiculate, apicular scar present, pyrene surface verrucose ........................................................................................................ C. lancifolia

9’. Drupe surface scabrous or smooth in sicco; pyrene mono-apiculate, apicular scar absent, pyrene surface alveolate crateriform or alveolate-crateriform-verrucose ........... 10

10. Adaxial lamina surface subglabrous; ovary 2-3 × 2-3 mm; mature drupe primrose in natura, 10.3-10.6 × 8.5-9.3 mm, epicarp glabrous to subglabrous, mesocarp viscous, pyrene 6.5-7 × 5.5-5.7 mm, pyrene surface alveolate-crateriform-verrucose ...................................................................................................................... C. brasiliensis

10’. Adaxial lamina surface pilose to pubescent; ovary 1-2 × 0.5-1 mm; mature drupe lemon and/or saffron in natura, 6.5-8.5 × 3-6.5 mm, epicarp pilose to pubescent, mesocarp not viscous, pyrene 4.5-5 × 3.5-4.5 mm, pyrene surface alveolate-crateriform ................................................................................................................... C. clausseniana

5’. Adaxial lamina surface smooth ................................................................................. 11

11. Style inconspicuous; pyrene without apiculum .......................................... C. chichape

11’. Style conspicuous; pyrene apiculate ........................................................................ 12

12. Mature drupe orange .................................................................................... C. spinosa

12’. Mature drupes primrose ........................................................................................... 13

13. Branches secondary and tertiary not sulcate; adaxial surface shiny; peduncle 5-11 mm length, arranged flowers in dichotomous cymes; mesocarp not ornamented, pyrene surface alveolate-crateriform .................................................................... C. orthacanthos

13’. Branches secondary and tertiary sulcate; adaxial surface opaque; peduncle 1-1.5 mm length, arranged flowers in glomerular cymes; mesocarp ornamented, pyrene surface verrucose ................................................................................................... C. spinosissima

Discussion

Celtis atlantica is a new species described for the Celtis subg. Mertensia (Planchon 1848). In Brazil, among the species with spines, C. atlantica and C. tala are unique to present an arboreal habit. Despite this similarity, the species have distinct distributions, C. atlantica is restricted to southeastern Brazil and C. tala is restricted to southern South America (Fig. 4 D ).

For Glaziou (1905) the specimen Glaziou 18991a (here identified as C. atlantica) should be recognized as a species of the genus Ziziphus. This proposal should be ignored, as this specimen has the same morphological characteristics as the specimens identified here as C. atlantica. In addition to the morphological characteristics, the results of Zamengo et al. (2020) also refute Glaziou's (1905) proposal. In this phylogeny, Zamengo et al. (2020) compared a specimen (M. Kuhlmann 3956) which has the same characteristics as the Glaziou 18991a specimen with 18 other specimens of Celtis, and they all proved to be monophyletic.

Based on the results of Zamengo et al. (2020) associated to the morphological, nomenclatural and taxonomic results here presented, we conclude that C. atlantica and C. orthacanthos (sense Planchon 1848) are distinct species. Finally, we would like to point out that Berg and Dahlberg's (2001) characterization of C. orthacanthos is mistaken, as all the specimens (^{Appendix 1}) used to characterize this species refer to C. atlantica.

Acknowledgments

The authors HBZ, LCP, and ALG thank the Jardim Botânico do Rio de Janeiro, Instituto de Pesquisas Ambientais, and Universidade Estadual do Centro-Oeste, Brazil. The authors thank the reviewers and the editor in charge, whose contributions substantially improved this work. HBZ thanks CAPES (88887.721972/2022-00) for the Grant awarded. HBZ thanks all the curators of the herbaria visited physically and virtually. HBZ is grateful for the nomenclatural clarifications provided by Dr. Jefferson Prado (IBt). HBZ also thanks his colleagues Diego Ferreira da Silva for your help in the field collection. HBZ thanks Dr. Karen Strier for the information related to the monkeys of Caratinga (Minas Gerais, Brazil). HBZ thanks the staff of the National Library of Rio de Janeiro for their help in locating the articles by Caminhoá and Cisneiros. The author FMB thanks the Instituto Estadual do Ambiente (Inea/RJ) for the institutional support. The author LCP thanks Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, E-26/202.277/2019, E-26/202.278/2019).

References

• Asmus J, Chamorro D, Mogni VY, Oakley LJ, Prado DE. 2018. Identidad Taxonómica de Los “Talas”: Analisis morfológico de Celtis tala y Celtis pallida (Celtidaceae). Boletin de la Sociedad Argentina de Botanica 53: 653-664. doi: 10.31055/1851.2372.v53.n4.22117
  » https://doi.org/10.31055/1851.2372.v53.n4.22117
• Ayala MM. 2015. Cannabaceae. In: Flora del Valle de Tehuacán-Cuicatlán. México, Instituto de Biología, Universidade Nacional Autónoma de México, UNAM, Fasc. 129. p. 1-21.
• Bachman S, Moat J, Hill AW, de la Torre J, Scott B. 2011. Supporting Red List threat assessments with GeoCAT: Geospatial conservation assessment tool. ZooKeys 150: 117-126.
• Beentje H. 2016. The Kew Plant Glossary an illustrated dictionary of plant terms. 2nd. edn. Richmond, Royal Botanical Garden, Kew.
• Berg CC, Dahlberg SV. 2001. A revision of Celtis subg. Mertensia (Ulmaceae). Brittonia 53: 66-81. doi: 10.1007/BF02805398
  » https://doi.org/10.1007/BF02805398
• Caminhoá JM. 1881. Botânica geral e médica. Vol. V, fascículos XI e XII. Rio de Janeiro, Typographia Nacional.
• Chamorro DC, Zamengo HB, Mogni VY et al 2021. Morfología comparada de diez taxones del género Celtis (Cannabaceae) del Cono Sur Sudamericano. Darwiniana 9: 217-244. doi: 10.14522/darwiniana.2021.91.936
  » https://doi.org/10.14522/darwiniana.2021.91.936
• Chamorro DC. 2022. Estudio filogenético y biogeográfico del género Celtis (Cannabaceae) para el cono sur Sudamericano. PhD Thesis, Universidad Nacional de Rosario, Rosario.
• Cisneiros FFA. 1846. Estudos botânicos 1834-1866 , Vol. VI. p. 20-23.
• Fu XG, Liu SY, Velzen R et al 2022. Phylogenomic analysis of the hemp family (Cannabaceae) reveals deep cyto-nuclear discordance and provides new insights into generic relationships. Journal of Systematics and Evolution 61: 806-826. doi: 10.1111/jse.12920
  » https://doi.org/10.1111/jse.12920
• Glaziou AFM. 1905. Mémoires 3 Plantae Brasiliae centralis a Glaziou lectae. Bulletin de la Société Botanique de France 52: 1-662.
• Henrickson J. 2010. Comments on a revision of Celtis subgenus Mertensia (Celtidaceae) and the recognition of Celtis pallida Journal of the Botanical Institute of Texas 4: 287-293.
• IUCN. 2022. IUCN Red List Categories and Criteria. The IUCN Red List of Threatened Species. Version 2022-2. https://www.iucnredlist.org/. 25 Sep. 2023.
  » https://www.iucnredlist.org/.
• Leme FM, Schönenberger J, Staedler YM, Teixeira SP. 2020. Comparative floral development reveals novel aspects of structure and diversity of flowers in Cannabaceae. Botanical Journal of the Linnean Society 193: 64-83. doi: 10.1093/botlinnean/boaa004
  » https://doi.org/10.1093/botlinnean/boaa004
• Leme FM, Schönenberger J, Staedler YM, Teixeira SP. 2021. Floral morphogenesis of Celtis species: implications for breeding system and reduced floral structure. American Journal of Botany 108: 1595-1611. doi: 10.1002/ajb2.1724
  » https://doi.org/10.1002/ajb2.1724
• Mansano VF, Pederneiras LC. 2016. Proposal to add Glaziou’s “Plantae Brasiliae centralis a Glaziou lectae” to the list of suppressed works in Appendix VI. Taxon 65: 1181-1182. DOI: 10.12705/655.28
  » https://doi.org/10.12705/655.28
• O’Dowd DJ, Wilson MF. 1989. Leaf domatia and mites on Australasian plants: ecological and evolutionary implications. Biological Journal of the Linnean Society 37: 191-236. doi: 10.1111/j.1095-8312.1989.tb01901.x
  » https://doi.org/10.1111/j.1095-8312.1989.tb01901.x
• Oakley LJ, Prado DE. 2013. Consideraciones sobre la identidad y delimitación de Celtis chichape (Wedd.) Miq. (Celtidaceae). Rojasiana 12: 117-124.
• Pederneiras LC, Costa AF, Araújo DSD, Carauta JPP. 2011. Ulmaceae, Cannabaceae e Urticaceae das restingas do estado do Rio de Janeiro. Rodriguésia 62: 299-313. doi: 10.1590/2175-7860201162207
  » https://doi.org/10.1590/2175-7860201162207
• Planchon JE. 1848. Sur les Ulmacées (Ulmacées et Celtidées de quelques auteurs) considerées comme tribu de la famille des Urticées. In: Brongniart MMAD, Decaise J (eds.). Annales des Sciences Naturelles. Paris, Victor Mason. p. 244-341.
• QGIS Development Team. 2022. QGIS Geographic Information System. http://qgis.osgeo.org. 10 Jun. 2022.
  » http://qgis.osgeo.org.
• Radford AE, Dickison WC, Massey JR, Bell CR. 1974. Vascular plant systematics. New York, Harper & Row Publishers.
• Sartorelli PAR, Benedito ALD, Campos Filho EM, Sampaio AB, Gouvêa APML. 2018. Guia de plantas não desejáveis na restauração florestal. São Paulo, Agroicone.
• Thiers B. 2023. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ih/. 1 Aug. 2023.
  » http://sweetgum.nybg.org/ih/.
• Torres RB, Luca AQ. 2005. Ulmaceae. In: Wanderley MGL, Shepherd G, Giulietti AM, Melhem TS (eds.). Flora Fanerogâmica do Estado de São Paulo. São Paulo, RiMa. p. 361-370.
• Turland NJ, Wiersema JH, Barrie FR et al 2018. International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Shenzhen, Glashütten, Koeltz Botanical Books.
• Zamengo HB, Gaglioti AL, Chamorro D et al 2020. Nomenclatural novelties in Celtis (Cannabaceae) and a preliminary phylogeny of the genus with emphasis on the South American species. Brazilian Journal of Botany 43: 947-960. doi: 10.1007/s40415-020-00656-x
  » https://doi.org/10.1007/s40415-020-00656-x
• Zamengo HB, Gaglioti AL, Romaniuc S. 2021. Celtis L. (Cannabaceae) do Brasil. História, diversidade morfológica e uma sinopse taxonômica de Celtis do Brasil. London, Novas Edições Acadêmicas.
• Zamengo HB, Machado AFP, Silva MFO. 2023a. Celtis Flora e Funga do Brasil, Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB608655/. 1 August 2023
  » https://floradobrasil.jbrj.gov.br/FB608655/.
• Zamengo HB, Chamorro D, Gaglioti AL, Oakley L, Pederneiras LC. 2023b. Nomenclatural notes on Brazilian Celtis (Cannabaceae). Phytotaxa 579: 209-218. doi: 10.11646/phytotaxa.579.3.6.
  » https://doi.org/10.11646/phytotaxa.579.3.6.
• Zamengo HB. in prep Taxonomia e filogenia de Celtis L. (Cannabaceae) com foco nas linhagens neotropicais. PhD Thesis, Escola Nacional de Botânica Tropical, Rio de Janeiro.

Appendix

Appendix 1. Materials of Celtis atlantica Zamengo erroneously cited as Celtis orthacanthos Planchon by Berg & Dahlberg (2001). Minas Gerais: Caratinga, Estação Biológica de Caratinga, 1 April 1984, (fr.), K.B. Strier 613 (BHCB, NY); idem 19°40’ S, 41°50’ W, 25 March 1984, (fr.), K.B. Strier 836 (NY!). Rio de Janeiro: Rio de Janeiro, matas do Sumaré, 3 September 1927, (fl.), Pessoal do Horto Florestal s.n. (K barcode 000964290!, NY barcode 00476067!, P barcode 06781657!, RB barcode 00439263!). Serra do Gericinó, 15 June 1982, fr., A. Glaziou 18991a (P!). Unknown locality: “prope mandioca” October 1923, (fl.), L. Riedel (NY barcode 02429055!, NY barcode 02429058!).

Publication Dates

• Publication in this collection
  26 Feb 2024
• Date of issue
  2024

History

• Received
  03 July 2023
• Accepted
  02 Nov 2023