Lippia horridula (Epling) Salimena et al. (2012: 52)

Cardoso, Pedro Henrique, Santos-Silva, Fernanda, Neto, Luiz Menini, Saraiva, Raysa Valéria Carvalho & Salimena, Fátima Regina Gonçalves, 2020, Heterophylly and post-fire flowering of Lippia horridula (Verbenaceae): a “ phoenix ” of Brazilian Cerrado, Phytotaxa 441 (1), pp. 95-102 : 96-99

Lippia horridula (Epling) Salimena et al. (2012: 52) .

Basionym: Eriope horridula Epling (1936: 191) .

Type: — BRAZIL. Goyaz: Prope Porto Real, 4 December 1828, W. J. Burchell 8426-5 (holotype K!).

Epitype: — BRAZIL, Goiás, Alto Paraíso de Goiás, 30 January 2012, J. F. B. Pastore & H. Moreira CTBS 4067 ( CEN!) (here designated).

Vegetative stage: subshrubs 20–30 cm tall, xylopodium well developed, branches woody, tetragonal, sparsely hirsute to glabrescent, nodes 1.3–2 cm long; leaves opposite, patent, petiole 1–2 mm long, blades 2–5 × 0.4–1 cm, coriaceous, narrow-elliptical, apex acute, margin coarse-serrate, ciliate, base attenuate, densely hirsute on both faces when young, with glandular-sessile trichomes, sparsely strigose at maturity, trichomes only along the veins. Reproductive stage: subshrubs 4–5 cm tall, xylopodium well developed, branches slender, tetragonal, with abundant glandular-pedicellate trichomes, nodes inconspicuous; leaves opposite, patent, petiole 0.3–0.4 mm long; blades 0.5–1.5 × 0.2–0.4 cm, membranaceous, elliptical to narrow-elliptical, apex acute, margin coarse-serrate, base attenuate, hirsute on both faces, abundant glandular-sessile and pedicellate trichomes. Inflorescence 9–12.8 × 7.1–8 mm, capituliform, peduncle 1.2– 1.6 cm long, hirsute, glandular-sessile trichomes; bracts 4.8–5.2 mm long, green, reddish in apical portion, lanceolate, alternate, 3-veined, externally hirsute, ciliate, glandular-sessile and pedicellate trichomes; calyx 1.7–3 mm long, tubular, 2-lobed, villous-canescent, with glandular trichomes; corolla tube 6–6.5 mm long; lobes unequal, pink, throat white or yellow, externally pubescent; stamens inserted in the middle of the corolla tube, ovary glabrous. Fruit unknown.

Epitypification:— In the protologue of Eriope horridula, Epling (1936) indicated as holotype a collection by Burchell 8426-5 which presents sterile material, without fertile parts, no fertile original material has been found ( Harley 1973). As defined by article 9.9 of the Code ( ICN, Turland et al. 2018), an epitype can be selected to provide unequivocal interpretation when the type or all original material associated is clearly ambiguous. Therefore, in order to ensure precise application of this name, we selected the material J. F. B. Pastore & H. Moreira 4067 (herbarium CEN) as an epitype for E. horridula . This choice was based on the presence of both vegetative and flowering stages in this recent collection ( Figure 1 ).

Fire adaptations— Lippia horridula is found in reproductive stage exclusively in recent burned fields. Flowering post-fire is a well-known adaptation of Cerrado plants, including species of Lantana and Lippia ( Coutinho 1976, 1977). Fire acts as a trigger to flowering and ensures a successful reproduction in communities ( Coutinho 1977, Keeley et al. 2011, Pilon et al. 2018). Besides this adaptation, we verified for the first time in Verbenaceae that L. horridula presents a pronounced heterophylly linked with the fire regime of the Cerrado. Font Quer (2001) defines heterophylly as the presence of leaf polymorphism within the same plant, frequently related with seasonality. Presence of heterophylly, as defined above, is also recorded in species with development of ‘summer and winter’ leaves from seasonally adapted habitats as: in drought tolerant plants ( Westman 1981), in riparian habitats ( Webb 1984) and in Mediterranean-type climates with fire-prone habitats ( Ehmig et al. 2019).

Prior to fire season, during the vegetative stage, the specimens are 20–30 cm high, with woody branches, conspicuous leaf nodes, coriaceous leaves, with blades 2–5 × 0.4–1 cm. After the fire, these branches and leaves are lost and the plant grows again from the xylopodium. During this flowering stage, specimens are only 5 cm high, with slender branches and membranaceous diminute leaves 0.5–1.5 × 0.2–0.4 cm, with glandular-sessile and pedicellate trichomes ( Figures 2 and 3 ). Rarely burned remnants of the vegetative stage are present concomitantly during the flowering stage.

Morphological affinities: — Lippia horridula morphologically resembles Lantana glaziovii and Lippia grandiflora because it shares the reduced plant size, a developed xylopodium, small leaves and bright pink corolla during the reproductive stage. However, these three taxa can be distinguished by the trichome morphology, leaf shape and margins and arrangement and shape of floral bracts ( Table 1).

Distribution, habitat and phenology: —Present in Goiás, Federal District, Tocantins ( BFG 2018), and Maranhão states. A collection of Lippia horridula from the Parque Nacional da Chapada das Mesas (Maranhão) is a new record of this species for the Northeast Region of Brazil, representing the northernmost limit of its distribution ( Figure 4 ). In this Park, we found only a small population of four individuals. This species is exclusive of the cerrados and campos rupestres (Cerrado Domain), and its collections are frequent between August and January.

Conservation status: —The species present EOO of 111.810,155 km 2 and AOO of 60 km 2. Although it is found inside a protected area, there are only a few records in the herbarium collections and present fragmented distribution. It is possible that the flowering response to the anthropogenic fires is not synchronized with the pollinator activities, reducing the pollination events in this species. Thus, according to the criteria of IUCN (2012) the species is assigned as Endangered (EN) (B2abiii).

Examined specimens of Lippia horridula :— Distrito Federal: Reserva Ecológica do IBGE, 14 September 2006, fl., M. Aparecida da Silva s/n ( IBGE 63665 !) ; Samambaia, Parque Boca da Mata , 8 November 1995, fl., J. M. de Rezende 68 ( CEN!). Goiás: 30 September 1829, W. J. Burchell 7921 ( K image!) ; Alto Paraíso de Goiás, 30 January 2012, fl., J. F. B. Pastore & H. Moreira 4067 ( CEN!) ; Cavalcante , 8 November 2000, fl., B. M. T. Walter et al. 4617 ( CEN!) ; Niquelândia , 17 September 1998, fl., E. L. Jacques et al. 797 ( CEN) ; Pirenopólis, Serra do Pirineus, 19 August 1995, fl., C. H. Monteiro et al. 125 ( CESJ!). Maranhão: Carolina, Parque Nacional da Chapada das Mesas , 12 October 2017, fl., R. V. C. Saraiva 152 ( SLUI!). Tocantins: Dianópolis , 30 September 2003, fl., T. B. Cavalcanti et al. 3439 ( CEN!) ; Goiatins , 6 January 2000, fl., E. Rodrigues 744 ( PMSP) ; Paranã, 21 December 2006, fl., G. Pereira-Silva & G. A. Moreira 10986 ( CEN!) .

Conclusion: —The recognition of the morphological variations related to the habit and heterophylly in L. horridula was decisive for the elucidation and resolution of a taxonomic confusion that had been perpetuated for decades. Detailed description and designation of the epitype were crucial to identify L. horridula and distinguish it from the similar species. The present study contributed with the knowledge of the flora of Maranhão state and with the conservation of this species endemic to the Brazilian Cerrado Domain.

Figures

FIGURE 1. Herbarium specimen J.F.B. Pastore & H. Moreira 4067 (CEN!) selected as epitype for Lippia horridula with presence of both vegetative and reproductive structures.

FIGURE 2. Habit of Lippia horridula. A. Plant in flowering with tiny leaves (arrows). B. Flowering stage with presence of leaves from vegetative stage on the ground (arrows). C, D. Flowering individual after fire. E. Detail of bracts subtending the inflorescence. Photos A and C by Zenilton Gayoso; Photos B and E by Raysa Saraiva; Photo D by Suzana Martins.

FIGURE 3. Herbarium specimens. A. Holotype of Eriope horridula: Specimen W.J. Burchell 8426-5 (K!, http://specimens.kew.org/ herbarium/K000470883), with presence of vegetative parts only (arrow). B. Specimen Walter et al. 4617 (CEN!) with the presence of reproductive structures only.

FIGURE 4. Distribution map of Lippia horridula in the Brazilian Cerrado domain (the arrow indicates a new record for the state of Maranhão).