An overview of the Brazilian inselberg genus Ameroglossum (Linderniaceae, Lamiales), with the description of seven new species

Field studies of the inselberg fl ora of north-eastern Brazil have resulted in the discovery of much greater morphological diversity of the genus Ameroglossum, than previously envisaged. These enigmatic plants are endemic to isolated rock outcrops, which have long been surrounded by unsuitable habitat. The morphological forms are geographically isolated and stable in cultivation when grown under similar conditions. We here provide detailed descriptions of the two previously known species and propose an additional seven new species in the genus. A taxonomic revision of the genus, including an identifi cation key is provided. We hypothesize that the evolution of this genus is driven by the diversity of their hummingbird pollinators. Due to the threatened nature of inselberg habitats and the small populations found for most taxa, the species described here are likely to be under threat and in need for formal redlisting. European Journal of Taxonomy 746: 1–25 (2021) 2


Introduction
On March 12, 1958, Dárdano de Andrade- IPA!) collected an unusual 'Scrophulariaceae' in Quipapá, Pernambuco State, Brazil. The specimen was found to be a new genus and tentatively called 'Dardanoa' by Vinicius Castro Souza on various herbarium specimens. This name was used, in advance of publication, by some regional botanists who were aware of this proposal. However, this name was never formally published. In 1998, the German botanist Stefan Vogel visited Pernambuco and together with the Brazilian botanist Ariadna Lopes collected material of the same genus at Brejo da Madre de Deus. Specimens of the collected material were described as the genus Ameroglossum Eb.Fisch., S.Vogel & A.V.Lopes (Fischer et al. 1999
Preliminary molecular and morphological studies (in preparation) suggest that Ameroglossum is related to Cubitanthus Barringer (1984) and Stemodiopsis Engler (1897), formerly placed in Gesneriaceae and Scrophulariaceae, respectively. These genera are now known to belong to Linderniaceae (Fischer et al. 2013;Christenhusz et al. 2017), and several characters appear to be shared by Ameroglossum and this clade (Almeida et al. 2019). A molecular phylogenetic study of Linderniaceae with a focus on these taxa is currently in progress by researchers from Brazil, China and the UK.
Ameroglossum is endemic to inselbergs associated with the Borborema Plateau in north-eastern Brazil, especially in the central-eastern region of the Plateau (Almeida et al. 2016(Almeida et al. , 2019. Populations are small and geographically isolated, occurring only within small vegetation 'islands' typical of rock outcrops, with flowers pollinated by hummingbirds (ornitophilia) and barochoric dispersal of seeds (Wanderley et al. 2014a). Its species have been suggested to exhibit interpopulational genetic and phenotypic variation (differences in plant architecture and leaf and flower size) due to environmental factors and geographic distances (Wanderley et al. 2014a(Wanderley et al. , 2018. Due to the interest in genetic and cytological diversity of inselberg plants, extensive field work has been carried out in north-eastern Brazil. Diversity of the genus Ameroglossum has been found to be much greater than initially thought. One species was published first as A. manoelfelixii L.P.Felix & E.M. Almeida (in Almeida et al. 2016), which differs in the winged quadrangular stems, glabrous vegetative segments, quadrangular pedicels, and the red corolla with purple trichomes in the median lobe of the lower lip. Several unusual specimens were found, including two new putatively related genera in Linderniaceae, which were described as Catimbaua L.P.Felix, Christenh. & E.M.Almeida and Isabelcristinia L.P.Felix, Christenh. & E.M. Almeida (in Almeida et al. 2019), with the latter genus having the greatest affinity to Ameroglossum in preliminary molecular studies (not presented here). In addition to these two new genera, many new populations of Ameroglossum have been discovered, which exhibit a greater morphological diversity than previously known. A number of populations represent undescribed species, which follows the trend of recent taxonomic discoveries from the inselbergs in north-eastern Brazil (e.g., Pontes 2012;Cordeiro et al. 2018;Cardoso et al. 2019aCardoso et al. , 2019bde Lima et al. 2019;Santos et al. 2019;Morales & Morais 2020;Morales & Kollmann 2020), showing that this often taxonomically neglected region of Brazil has a greater diversity than previously assumed.
The newly discovered populations of Ameroglossum show a great morphological diversity, some clearly belonging to the two published taxa, but seven populations could not be placed satisfactorily in these species. Therefore, these new species are described below, increasing to nine the number of species in Ameroglossum. An amended description of Ameroglossum and a diagnostic key to the species are provided.

Material and methods
Field collections were undertaken on rock outcrops in the geomorphological structure of the Borborema Plateau, which covers parts of the Brazilian states of Rio Grande do Norte, Paraíba, Pernambuco and Alagoas (Fig. 1). The Borborema Plateau corresponds to a group of continuous highlands distributed along the eastern section of north-eastern Brazil, to the north of the São Francisco River, with elevations often exceeding 800 m (Corrêa et al. 2010). The predominant vegetation in that region is caatinga (thorny, dry-deciduous vegetation). A semi-arid climate that is susceptible to humid coastal winds on its eastern flank allows the development of enclaves of humid vegetation (called brejos de altitude; Andrade-Lima 1981). Morphological analyses were based on material preserved in 70% alcohol, as well as on live plants grown in the experimental garden of the Plant Cytogenetic Laboratory of the Agricultural Sciences Centre of the Federal University of Paraíba. Descriptions of the morphological characters are based on terminology proposed by Gonçalves & Lorenzi (2007) and Radford et al. (1974) for general terminology and on Payne (1978) for trichome morphology. Important herbarium collections were consulted, but not all historical material was studied, because many collections were inaccessible due to the COVID-19 pandemic. It is therefore possible that additional undescribed species are hiding among this material.
Ameroglossum is restricted to north-eastern Brazil (so far reported in the states of Alagoas, Paraíba, Pernambuco and Rio Grande do Norte). It comprises nine species and is morphologically similar to Cubitanthus, Catimbaua, Isabelcristinia and the African Stemodiopsis. A key to the species of Ameroglossum, Isabelcristinia, Catimbaua and Cubitanthus is provided below.

Note
The inflorescence was described by Fischer et al. (1999) as a frondose thyrse, which was based on the little material that was available to them at the time. However, this description of the inflorescence is incorrect. We have observed in cultivated material that when inflorescences are initiated, the plant produces inflorescence buds in the axils of leaves in the upper part of the main stems, which grow into inflorescences. These leafy stems can continue to grow for more than one flowering season. Therefore, the inflorescence is not a thyrse, but the inflorescences are axillary simple or compound dichasia.

Diagnosis
A species morphologically similar to A. manoelfelixii because it has glabrous to glabrescent, lustrous vegetative parts and inflorescences. However, A. alatum sp. nov. differs from this and other species of Ameroglossum, by having conspicuous membranous wings on the stem extending to the peduncle of the inflorescence and the pedicel (vs not or sparsely winged). Because of its green stems and leaves, A. alatum sp. nov. may also appear similar to A. bicolor sp. nov., although it differs by having its inflorescence in a simple dichasium (vs compound dichasium), winged peduncles and pedicels (vs partially winged) and the sepals not overlapping (vs sepals overlapping).

Etymology
The name is derived from the Latin adjective ʻalatusʼ, ʻwingedʼ, referring to the conspicuous wings on the branches, peduncles and pedicels.

Distribution
Currently known only from a single population on a granite outcrop near the city of Maravilha, in the Sertão Alagoano mesoregion, Alagoas State, Brazil. Elevation ca 790 m.

Ecology
As for the other taxa of Ameroglossum, A. alatum sp. nov. is restricted to granite outcrops, where it is probably pollinated by hummingbirds. Flowering and fruiting were recorded in August.

Population and threats
The population is composed of approximately 20 adult individuals, restricted to an area of approximately 3000 m² on one of the tops of this granite outcrop. The small population demonstrates elevated homozygosity, suggesting a low genetic diversity, probably caused by a founder and / or a genetic bottleneck effect (Wanderley et al. 2018).

Diagnosis
This species is distinguished by the presence of two conspicuous wings on the dorsal sepal (vs calys without wings in all other species). It also has leaves that are rough to the touch with aciculate hairs (vs glabrous or softly hairy in all other species).

Etymology
The epithet derives from the Latin ʻasperʼ, ʻroughʼ, and ʻfoliumʼ, ʻleafʼ, reflecting the rough texture the leaves of this species.

Distribution
Ameroglossum asperifolium sp. nov. is known only from a small population growing on a granite outcrop where it covers an area of approximately 0.5 ha in the Leste Alagoano mesoregion, Alagoas State, Brazil. Elevation ca 510 m.

Ecology
Flowering and fruiting was observed in June and October. The rocky outcrop where the species was collected is located at the edge of a secondary road near the Usina Serra Grande sugarcane plantation, Alagoas State, and was probably originally surrounded by Atlantic Forest vegetation.

Population and threats
There is only a single known isolated population of this species, occupying an area of less than 10 km 2 . In addition to the degradation of the surrounding habitat due to agricultural expansion, we observed invasion of the outcrop by Furcraea foetida (L.) Haw. (Asparagaceae), resulting in competition for space and consequent reduction of the population of this newly described taxon.

Diagnosis
This species is morphologically similar to A. alatum sp. nov. in having lustrous branches and leaves, winged pedicels, and white trichomes on the lower lip of the corolla tube. It differs in having green or slightly purplish vegetative portions (vs completely green), wings not evident (vs strongly winged), inflorescence usually a compound dichasium (vs simple dichasium) and the dorsal sepal partially covering the lateral sepals (vs the sepals not overlapping).

Etymology
The specific epithet is the Latin adjective ʻbicolorʼ, ʻtwo-coloredʼ, referring to the vegetative variation observed in its populations. Among the four populations described here, it was possible to encounter green or purplish, almost wine-coloured, plants in the same population, a characteristic only observed in this species. Fig. 4. a-

Distribution
Three populations of Ameroglossum bicolor sp. nov. are known from granite outcrops in the municipalities of Agrestina, Bonito and Caruaru in the Agreste mesoregion of Pernambuco State, Brazil. It grows at elevations between 425 and 700 m.

Ecology
Ameroglossum bicolor sp. nov. has been collected in flower from May to October, with high inter- and intrapopulational synchrony (Wanderley et al. 2014a).

Diagnosis
This species is similar to A. manoelfelixii in having lustrous, purple-tinged vegetative parts and scarlet flowers, but it differs in having inflorescences in simple dichasia (vs compound dichasia), peduncle winged (vs peduncle not winged) and white trichomes on the lower lip of the corolla (vs trichomes violet). It differs from the other species of Ameroglossum by the deep vinaceous colour of its vegetative parts.

Etymology
The specific epithet is dedicated to the Fulni-ô Amerindians whose territories are located in the Serra do Comunaty where the type material was collected. Members of the Fulni-ô ethnic group have conserved many of their traditional cultural values, being one of the few indigenous groups in north-eastern Brazil that have conserved their original language, Yaathe or Ia-tê, from the Macro-Jê linguistic branch.

Distribution
Only two populations of A. fulniorum sp. nov. are known growing near Águas Belas, Serra do Comunaty, in the Agreste mesoregion of Pernambuco State, Brazil. Elevation ca 900 m.

Ecology
Like other species of Ameroglossum, the occurrence of A. fulniorum sp. nov. is restricted to granite outcrops. Flowering and fruiting in August.

Population and threats
Only two populations of A. fulniorum sp. nov. are currently known, which together comprise approximately 40 widely spaced adult individuals. Due to the isolation of those populations and their restricted distributions, together with environmental pressure from trampling by domestic animals and the occasional passage of wildfires, this species is highly threatened.

Diagnosis
This species is morphologically similar to A. manoelfelixii in having young leaves with revolute margins, vegetative structures lustrous and violet trichomes on the lower lip of the corolla tube. It differs from that species in its green vegetative portions (vs tinged purple), leaf blade elliptic to ovate (vs elliptic to narrowly elliptic, sometimes trullate) and flowers orangish (vs scarlet).

Etymology
The specific name is in honour of Prof. Genaro Viana Dornelas, a senior professor at the Universidade Federal da Paraíba, who has a vast knowledge of the flora of Paraíba State.  Almeida & J.M.P. Cordeiro 17,486;EAN[25,542]

Distribution
This taxon has a more northerly distribution than the other species of Ameroglossum and occurs the lowest for this genus. It occurs on rock outcrops in the Agreste Paraibano mesoregion, in Paraíba State (two populations), and in the Agreste Potiguar mesoregion in Rio Grande do Norte State (four populations), Brazil. Elevation between 70 and 300 m.

Ecology
Ameroglossum genaroanum sp. nov. occurs on rock outcrops. Flowering and fruiting between April and June.

Population and threats
Ameroglossum genaroanum sp. nov. is represented only by small isolated populations with up to 60 individuals distributed in small geographical areas susceptible to various anthropic impacts.  Almeida 14,339;EAN[19,860]!.

Distribution
Only two populations of Ameroglossum intermedium sp. nov. are currently known, both in the municipality of Quebrangulo, Agreste mesoregion of Alagoas State. Elevation ca 500 m.

Ecology
This species occurs exclusively on granite outcrops. Flowering and fruiting recorded in August and like all other Ameroglossum species it is pollinated by hummingbirds. The surrounding vegetation was probably originally composed of deciduous forest, but this has now been replaced by natural pasture.

Population and threats
Only two rock outcrops separated by pasture in a single municipality in Alagoas State are known to harbour this species. Approximately 200 adult individuals can be found in the first population, whereas the other comprises approximately 30 individuals. The main threat to these populations are farming and grazing of the site by stray animals.

Taxonomic notes
Among the species of Ameroglossum with quadrangular stems, A. intermedium sp. nov. stands out by having reproductive and vegetative structures covered in trichomes, a characteristic otherwise typically observed in A. pernambucense. However, A. intermedium sp. nov. differs by having leaves that are principally opposite and decussate, inflorescences of compound dichasia and the revolute lower lip.

Distribution
Ameroglossum manoelfelixii occurs exclusively on granite outcrops in Paraíba State, restricted to the Agreste da Borborema, Curimataú and Brejo microregions. Elevation between 500 and 700 m.

Ecology
This species is pollinated by hummingbirds . It has been collected with flowers and fruits between March and August.

Population and threats
This species has a fragmented distribution and its populations are under intense anthropogenic pressure. Many rock outcrops where the species occurs have been quarried for cobblestones, and many populations are on farms where the vegetation is trampled and grazed by livestock. Fires are also often set to these vegetation islands for no clear purpose. Eb.Fisch., S.Vogel & A.Lopes Fig. 2H Feddes Repertorium 110: 529-534 (Fischer et al. 1999

Ecology
Plants are saxicolous on tall granite rocks. Flowering from March to October, with flowering peak in July, and pollinated by hummingbirds (Wanderley et al. 2014a.

Population and threats
The populations known typically comprise approximately 50 mature plants. Other populations have been observed on rock outcrops nearby. The fragmented subpopulations are often subjected to trampling by cattle and long periods of drought.

Taxonomic notes
Ameroglossum pernambucense is the type species and differs from the other species proposed here principally in having verticillate, villose leaves (vs opposite leaves); apart from A. xukuruorum sp. nov., which has verticillate, glabrous leaves and the slighty apically trilobed lower lip of the corolla (vs lower lip entire to slightly crenate).

Etymology
The specific epithet is dedicated to the Amerindian Xukuru people, because the type material was collected with their assistance on tribal lands in the Serra do Ororubá Range.

Distribution
Ameroglossum xukuruorum sp. nov. has only been collected above 1000 m a.s.l., which corresponds to the highest areas of the Borborema Plateau in the states of Paraíba (São João do Tigre in the Cariri Ocidental microregion) and Pernambuco (Pesqueira in the Vale do Ipojuca microregion). Elevation between (800-)1000 and 1200 m.

Ecology
Ameroglossum xukuruorum sp. nov. appears to prefer higher elevation habitats. It was encountered flowering and fruiting between April and August and is pollinated by hummingbirds (pers. obs.).

Population and threats
Ameroglossum xukuruorum sp. nov. is restricted to the municipalities of Jataúba, Pesqueira and São João do Tigre and has been collected in the Xukuru Indigenous Reserve on a rock outcrop covering approximately 50 ha, with a population of more than 100 individual adult plants. Additionally, the Serra do Ororubá Range, where the reserve is located, has a series of granite outcrops that are difficult to access, and it is possible that other populations of A. xukuruorum sp. nov. (or other species of Ameroglossum) are yet to be discovered there. The two known locations in Paraíba State have a total of ca 100 adult individuals. The isolated populations are exposed to burning and trampling by livestock.

Discussion
Ameroglossum (Linderniaceae, Lamiales) now comprises nine species. This is likely not to be the final total because we predict that there may be additional undescribed species among herbarium specimens or in regions that have not yet been investigated. Our survey of inselbergs in the region was extensive but by no means exhaustive, and it is thus possible that additional diversity is present.
This level of hidden diversity is not unique to Ameroglossum, because a similar unexpected diversity has been found in a number of plant and animal groups in north-eastern Brazil (e.g., Plowman 1986; Gonçalves-Oliveira et al. 2017;Mângia et al. 2018;Chagas & da Costa-Lima 2020;Pinagé et al. 2020, etc.).
The drivers of this unexpectedly high diversity on these relatively dry granitic outcrops may be due to the isolation of these sites. These rock formations are ecologically islands, usually called inselbergs (Porembski & Barthlott 2000), and this has often resulted in allopatric speciation and has been found in many groups of animals and plants typically found there, including Ameroglossum (Wanderley et al. 2018).
Pollinators also seem to be the drivers of the diversity of this genus (Wanderley et al. 2014a;Almeida et al. 2019). Further studies on pollinators of these new species of Ameroglossum, and of the related genus Isabelcristinia, are needed to elucidate this phenomenon. Speciation by hummingbird pollination has been shown to occur in several plant groups (e.g., Zung et al. 2015;Kessler et al. 2020;Kriebel et al. 2020). Because of the differences in corolla colour and lip-shape between these species, it is likely that this diversity is linked to specific hummingbird pollinators, but extensive field observations will be needed to better understand this relationship. Wanderley et al. (2020) studied pollination success of A. manoelfelixii and A. pernambucense in isolated populations and showed that both species selfpollinate. However, pollination by hummingbirds increased fecundity. Nevertheless, the limited crosspollination success (ca 3%) suggested that Ameroglossum has a low capacity to counteract genetic erosion . This contrasts with the bromeliad Encholirium spectabile Mart. ex Schult. & Schult.f., which is dominant in similar habitats where Ameroglossum is found and shows a unique genetic composition on each inselberg, although populations are still genetically linked (Gonçalves-Oliveira et al. 2017). This is due to differences in pollinators; Encholirium Mart. is pollinated by bats, resulting in the inselbergs being less isolated simply because bats have a larger range than hummingbirds  and are thus more likely to visit more than one inselberg.
Meanwhile, inselberg habitats are greatly threatened by cattle ranching, mining, invasive species and fire, and many species dependent on these vegetation islands are under great pressure (Porembski 2007;Wanderley et al. 2014b). Now that we know that Ameroglossum is not a single widespread species, but consists of a complex of at least nine species with limited distributions, it is adamant that in situ programmes are developed, protecting as many populations as possible. Currently, only 1.5% of the genetic diversity of the region lies within protected areas (Fonseca et al. 2019), and therefore, to maintain evolutionary potential in the region, areas with higher genetic diversity need to be included in future conservation planning, not only to safeguard the new species described here, but also to preserve these unique inselberg communities.
Ex situ conservation through horticulture is also an option because the species are easily cultivated, stems root readily in water (pers. obs.) and plants make attractive horticultural subjects, suitable for dry tropical and subtropical regions. As with other endangered plant species (e.g., Wollemia nobilis W.G.Jones, K.D.Hill & J.M.Allen: Trueman et al. 2007), profits from the sale of plants propagated horticulturally may help fund the protection of inselberg habitats to the benefit of these species.