The genus Aristolochia L. comprises around 560 species from six continents and is especially diverse in the tropics and subtropics (González, 2012). Frequent discoveries in recent years suggest that the number is underestimated especially in the Neotropics (Freitas et al., 2013, 2017a, 2017b, 2019, 2020a, 2020b; Fernández et al., 2019; Jiménez et al., 2021a; Jiménez et al., 2021b; Frank et al., 2022; Jiménez et al., 2023). Aristolochia trilabiata Glaziou is a tropical liana from Brazil, Perú, Panama and French Guiana (Glaziou, 1905; Feuillet & Poncy, 1998; González & Pabón-Mora, 2018; Fernandes et al., 2021)(Fig. 1). It belongs to the subgenus Aristolochia section Gymnolobus Duchartre, subsection Hexandrae (Duch.) O.C. Schmidt, series Hexandrae F. González subseries Hexandrae (Duch.) F. González, which is mainly characterized by pauciflorous distal inflorescences (González, 1991, 1997; González & Pabón-Mora, 2018). Within this series, it belongs to an informal group of species referred to as ‘Exstipulosae’, characterized by the lack of pseudostipules in the leaf axils (González, 1991; González & Pabón-Mora, 2018). Diagnostic characters of infrageneric groupings within Aristolochia include leaf anatomy, inflorescence, gynostemium, and capsule and seed morphology, which have been comprehensively reviewed by González (1991). At the species level, however, many of these characteristics are less indicative, and as infrageneric groups include dozens to a hundred species that are often vegetatively similar, essentially characters of anthetic and late pre-anthetic flowers remain significantly informative. Such features include perianth shape, surface texture and indumentum, size ratios and relative position of utricle, limb and tube, and rarely also coloration (González & Stevenson, 2000a, 2000b; Blanco, 2002; Freitas et al., 2013, 2017a, 2017b, 2019, 2020a, 2020b; González & Pabón-Mora, 2017; Fernández et al., 2019; Jiménez et al., 2021a; Jiménez et al., 2021b; Frank et al., 2022; Jiménez et al., 2023). The general perianth structure of Aristolochia encompasses a proximal utricle that connects to the distal limb via a hollow structure referred to as the tube (González & Stevenson, 2000a). The limb structure of A. trilabiata is particularly characteristic, as it is formed by an upper limb zone and a lower limb zone (Fig. 1B). Such bipartite limbs are also common in other related, informal groups and species, such as species of Aristolochia series Thyrsicae F. González (e.g. Aristolochia hoehneana O.C. Schmidt), Aristolochia subseries Anthocaulicae F. González (e.g. Aristolochia cornuta Masters) and Aristolochia subseries Hexandrae (Duch.) F. González (e.g. Aristolochia birostris Duchartre, Aristolochia labiata Willdenow) (González, 1998; González & Pabón-Mora, 2017). While conducting large-scale geometric morphometry studies on Aristolochia complexes from the Neotropics and Paleotropics, specimens from French Guiana and Amazonas, Brazil, stood out from any previously described species by both vegetative and reproductive characteristics. These specimens are easily recognizable by several distinct perianth characters. The presence of a well defined, broad medial zone, the smaller size and fewer veins running through the upper limb lateral zones, short papillae covering the margins of all limb structures, and a significantly shorter tube are additional traits not found in the perianth of A. trilabiata as originally described (Glaziou, 1905; Miles Moss, 1915; Hoehne, 1927). Additionally, the leaves of these unusual specimens are elongate-cordiform, occasionally slightly hastate. Thus, it is proposed to treat these populations as a distinct species, which is corroborated by their allopatric distribution (French Guiana, Brazil: Amazonas), photographic illustration of relevant characters, and geometric morphometry. A detailed morphological comparison, remarks on closely related taxa, illustration of diagnostic characters, and a preliminary assessment of extinction risk are provided (Fig. 2, Tab. 1).

Fig. 1
figure 1

Aristolochia trilabiata. A. Leaf blade. B. Preanthetic flower with medial upper limb zone (mu), lateral upper (lu) and lower limb zones (ll), utricle (u), and tube (t). C.–D. Anthetic flower. Note the presence of papillae (p) only on the lateral upper limb zones. The medial upper limb zone (mu) is rudimentary. E. Dissected utricle (u) and gynostemium (g). F. Immature fruit. [Scale bar: A. 20 cm; B.–C. 5 cm; D. 3 cm; E.–F. 5 cm. Photos (all reproduced with permission): A. by Jared Shorma, near Manú Learning Center, Madre de Dios, Perú, unvouchered; B.–F by Richard C. Hoyer, near Canutama, Amazonas, Brazil, unvouchered.].

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Fig. 2
figure 2

Aristolochia franzii. A. Habit. B. Adaxial leaf blade. C. Abaxial leaf blade. D. Preanthetic flower with protruding medial upper limb zone (mu), lateral upper (lu) and lower limb zones (ll), utricle (u), and tube (t). The proximal end of the upper limb terminates 0.5–1 cm prior to the distal end of the lower limb (d). E.–F. Anthetic flower. Note that all margins are covered in papillae (p). G. Dissected utricle (u) and gynostemium (g). H. Fruit. [Scale bar: A. 50 cm; B.–C. 2.5 cm; D.–E. 2 cm; F.–G. 2 cm; H. 6 cm. Photos (all reproduced with permission): A.–H. by Paul Franchet, near Roura, Cayenne, French Guiana, unvouchered.].

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Table 1 Morphological comparison of Aristolochia franzii and its relative Aristolochia trilabiata, derived from field observations and cultivated specimens.
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Materials and methods

In total, 41 vouchers were investigated, eight corresponding to Aristolochia franzii and 33 to A. trilabiata (acronyms follow Thiers, 2023): BM, CAY, CLEMS, CONN, F, IAN, K, L, MG, MO, NY, P, RB, U, US, WAG. Of these, specimens with unfragmented leaves and flowers in late pre-anthesis were subjected to geometric morphometry. Landmarks for homologous structures (Fig. 3) comprise eight landmarks for each leaf and flower (tube and limb, excluding the utricle as of preservation artifacts due to its inflated nature). The morphometric analysis was employed as detailed in Freitas et al. (2020b), using TpsDig version 2.31 (Rohlf, 2017) and MorphoJ version 1.07a (Klingenberg, 2011) to perform a principal component analysis (PCA, Fig. 4). A total of 88 leaves and 41 flowers were examined, of which 37 leaves and 13 flowers were derived from A. franzii, and 51 leaves and 28 flowers of A. trilabiata.

Fig. 3
figure 3

Homologous points selected as landmarks for geometric morphometry of leaves (A.–B.) and preanthetic flowers in lateral view (C.–D.) of Aristolochia franzii (A., C.) and Aristolochia trilabiata (B., D.).

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Fig. 4
figure 4

Principal component analysis (PCA) of selected landmarks from Aristolochia franzii (red) and A. trilabiata (blue). A. Leaves. B. Flowers.

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Living specimens and ex-situ photographs from French Guiana, generously provided by Paul Franchet, and cultivated plants from Burgers’ Zoo (Arnhem, The Netherlands) were examined and compared with the herbarium vouchers. The conservation assessment for A. franzii was conducted according to IUCN criteria (IUCN, 2012, 2013, 2022). Area of Occupancy (AOO) and Extent of Occurrence (EOO) were calculated with the GeoCAT Geospatial Conservation Assessment Tool (Bachman et al., 2011).

Results

Geometric morphometry

The morphometric analysis of the flowers separated the examined vouchers entirely into two distinct entities (Fig. 4). Principal component 1 (PC1 = 47.9%) and PC2 (13.6%) cumulatively covered 61.5% of the flower variation observed. Morphometry further corroborated the distinction found in the flowers by leaf characters (PC1 = 74.7%, PC2 = 11.7%), explaining a total of 86.4% leaf variation. The latter result was surprising given that closely related Aristolochia species are usually barely distinguishable by vegetative characters, and are mostly circumscribed by floral and reproductive features. Since eight landmarks (dimensions) were used to generate a two-dimensional PCA plot covering limb and tube structure, the significance of the analysis is underlined. It thus becomes evident that geometric morphometry, as applied the first time in Aristolochia by Freitas et al. (2020b), can be confirmed to represent a reliable and potentially powerful tool to visualize and precisely distinguish closely related species and complexes in Aristolochia.

Taxonomic treatment

Aristolochia franzii D.Frank, sp. nov. (Figs. 2, 5).—Type: French Guiana, Cayenne: Nouragues Field Station and vicinity, junction of Crique Kwak and Crique Nouragues, 04°05'17.9"N, 52°40'46.4"W, 10 Jan 2003, S.A. Mori, T. Lobova, V. Hequet, A. Berkov, J. Feinstein, B. Keeley & A. Tejedor 25549; (holotype: NY barcode 668825 [!]; isotypes: P barcode P06793067 [!]; CAY barcode 036880 [!])

Fig. 5
figure 5

Distribution of Aristolochia franzii and Aristolochia trilabiata.

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Diagnosis.—Aristolochia franzii differs from A. trilabiata by the presence of a medial upper limb zone, the length of the tube, the length of the lateral upper limb zones, the veins stabilizing the lateral upper limb zones, the presence of short papillae on all three upper limb and the single lower limb zones, the proportions of the lower limb zone in relation to the upper limb zones, the leaf contour, and the geographical distribution.

Climbing liana, shoots glabrous, growing into the canopy up to 15 m, stems corky; twigs terete, internodes 7–15 cm long. Leaves alternate, cordiform-elongate to hastate, 9.5–21 × 6.5–10 cm, leathery, glabrous, base cordate, sinus narrow, main veins 5–7, leaf apex acuminate, sometimes slightly caudate. Petioles glabrous, 2.3–5 cm, pseudostipules absent. Solitary flowers appear from leaf axils of young, main shoots. Peduncles 3.5–5 cm, ovary 6-carpellate and 6-locular, ca. 1.5–2 cm. Gynostemium hexandrous, ca. 8–12 mm. Utricle ca. 2.5–4.5 × 1.8–3.5 cm. Tube short, ca. 0.9–1.8 cm, adaxial side partially sunken in utricle before and during anthesis, dense cover of friable trichomes inside the tube, limb divided into three upper limb zones and a single lower limb zone (Fig. 2D–E), two lateral upper limb zones ca. 2.2–3.2 cm long, stabilized by 2–4 intensely red to purple veins, margin covered in short papillae of identical color, medial upper limb zone ca. 0.8–1.2 × 0.6–1 cm, margin covered in identical papillae as mentioned above, lower limb zone ca. 1.5–2.2 cm long, distal end terminating 0.5–1 cm before proximal end of upper limb zones, inside of lower limb zone covered in friable trichomes, and margins covered in short papillae. Perianth primary color pale green to light brown outside, with veins of slightly darker color, intense green to yellow within, surface glabrous outside and inside, except for utricle (which is densely pilose within; Fig. 2G). Fruits capsular, six-chambered, cylindrically elongated, ca. 17.5–23 × 0.9–1.5 cm. Seeds ovate, approximately 3–4 × 2–3 mm, thick, non-winged, abaxial side convex, adaxial side concave with small elaiosome present.

Notes.—The most obvious difference of the new species from Aristolochia trilabiata is the presence of a medial upper limb zone in the anthetic flowers of A. franzii (0.8–1.2 cm × 0.6–1 cm, Fig. 2D) versus its absence or reduction to a short, filamentous structure in A. trilabiata (Fig. 1D), also visible in lateral view during floral development as a protrusion (Fig. 2D). The length of the tube from the utricle to the proximal end of the lower limb zone is shorter (9–18 mm) in A. franzii than in A. trilabiata (28–45 mm). Overall, the ratio of the utricle size with respect to tube and limb size is considerably larger in A. franzii. Similarly, lateral upper limb zones are shorter in A. franzii (2.2–3.2 cm) than in A. trilabiata (4.5–6 cm), and the veins stabilizing the lateral upper limb zones are notably fewer (A. franzii: 2–4, A. trilabiata: 7–13). A further diagnostic character is the presence of short papillae on all three upper limb and the single lower limb zones of A. franzii, versus their restriction to the two lateral upper limb zones in A. trilabiata (Fig. 1C–D). By viewing from the side, the proportions of the lower limb zone in relation to the upper limb zones are also distinct; in A. franzii, the proximal end of the upper limb is located 0.5–1 cm apart from the distal end of the lower limb (Fig. 2D), while in A. trilabiata the upper limb zones start where lower limb zone terminates, or rarely even overlap (Fig. 1B).

The leaves of A. franzii are consistently cordiform-elongate to cordiform-hastate versus broadly cordiform in A. trilabiata (Fig. 2B–C).

Aristolochia franzii can also be geographically separated from A. trilabiata. Aristolochia franzii is distributed in French Guiana and Brazil (Guiana Shield), whereas A. trilabiata covers Brazil (Acre, Amazonas, Espírito Santo, Maranhão, Mato Grosso, Pará, Rondônia), Bolivia, Ecuador, Panama, Perú and Venezuela (González & Pabón-Mora, 2018; Freitas et al., 2020a). The observed disparities are further summarized in Table 1.

Distribution and ecology.—Aristolochia franzii is distributed in French Guiana and Brazil (Amazonas) (Fig. 5). It grows in primary and secondary tropical rainforests, often in proximity to streams, rivers, and roadsides.

Phenology.—Flowers of Aristolochia franzii have been reported from July to February, and fruits have been reported from September to March.

Etymology.—The species is named in memory of the author’s late father Franz Frank, who died early but fueled the author’s passion for natural sciences and botany.

Preliminary assessment of Extinction Threat.— Aristolochia franzii is recorded from 12 points constituting 10 locations herein. The Area of Occupancy (AOO = 40 km2) and Extent of Occurrence (EOO = 178,000 km2) suggest Aristolochia franzii can be categorized as Least Concern (LC) according to IUCN criteria (IUCN 2012, 2013, 2022). The broad distributional area covers protected habitats where the species has already been reported (Park Amazonien de Guyane, Réserve Naturelle Nationale des Nouragues). Furthermore, no threatening human interference or decline in the known populations has been recorded.

Additional specimens examined.—BRAZIL. Amazonas: Municipio de Presidente Figueiredo, Canteiro de obras da Usina Hidrelétrica de Balbina, próximo a estacao de tratamento de água, 14 Jul 1986 (fl.), C.A. Cid Ferreira 7571 (K, MG).

FRENCH GUIANA. Cayenne: Bourg de Saint-Georges de l'Oyapock, Bassin de l'Oyapock, chemin dans le bourg de Saint-Georges, 14 May 1983 (st.), M.-F. Prévost 1353 (CAY, P); Montagne de Kaw, Plaine et Montagne de Kaw, 275 m, 20 Mar 1985 (fl.), L.E. Skog et al. 5675 (CAY); Zidok ville, Abattis autour du village, 31 Oct 1974 (fr.), J.-P. Lescure 374 (P). Saint-Laurent-du-Maroni: Montagne Carbet Mitan, Région de Saül, 09 Jan 1980 (fl.), G. Cremers 6069 (CAY); Region de l'Inini, Sommet nord, 7 km à l'est de Gobaya Soula, Monts Atachi Bakka, Bassin du Maroni, 03°33'N, 53°55'W, 360 m, 28 Jan 1989 (fl., fr.), J.-J. de Granville et al. 10,947 (CAY, P, US).

NETHERLANDS. Arnhem: Burgers Zoo, Tropical Greenhouse (cultivated), 09 Jan 2013 (fl.), P.J.M. Maas et al. 10461 (WAG).

Remarks.—The new species is cultivated in several Botanic Gardens under the name of Aristolochia didyma S. Moore, a synonym of A. trilabiata (Miles Moss, 1915; Freitas et al., 2017a, 2017b; González & Pabón-Mora, 2018). Aristolochia rodriguesii Hoehne is another heterotypic synonym of A. trilabiata (Hoehne, 1927; Ahumada, 2010; Freitas et al., 2017a, González & Pabón-Mora, 2018). The synonymy of these two names under A. trilabiata is confirmed herein by the inclusion of the respective type specimens (A. didyma: Miles Moss s.n.; A. rodriguesii: E. Ule 9338) within the morphometric analysis (see specimens of A. trilabiata examined). A comparison of diagnostic characters of Aristolochia franzii and A. trilabiata is provided in Table 1.

Specimens of A. trilabiata examined.—BOLIVIA. Pando: Cobija, Jan 1912 (fl.), E. Ule 9338 (MG).

BRAZIL. Acre: Mun. Sena Madureira, 4 km of right bank of Rio Iaco, 05 Oct 1980 (fl.), C.A. Cid Ferreira 2775 (MO, NY, RB, US); Rio Branco, 02 Jan 1944 (fl.), J.T. Baldwin 3156 (NY, US). Amazonas: Mun. Humaitá, basin of Madeira, near Livramento, on Rio Livramento, 12 Oct 1934 (fl.), B.A. Krukoff 6578 (K, MO, NY, US, U). Espírito Santo: Serra da Itabapoana, 22. Sep 1875 (fl.), A. Glaziou 10033 (K, P). Maranhão: Araguana, Alto Turi, terreno ao acampamento da Sudene, 06°35′23"S, 48°28′26"W, 26 Sep 1966 (fl.), W. Rodrigues 8253 (CLEMS, CONN). Mato Grosso: Novo Mundo, 11 Nov 2006 (fl.), D. Sasaki 1078 (K). Pará: Altamira, 08 Aug 1998 (fl.), S.V. da Costa Neto 277 (MG); Belém, 20 Dec 1962 (fr.), E. Oliveira 2362 (IAN); Breves, local onde foi feito um levantamento florestal, Oct-Nov 1957 (fl.), J.M. Pires et al. 6658 (IAN, RB); km 130 da rodovia Belém-Brasília, 30 May 1960 (fl.), E. Oliveira 833 (IAN); Moju, Campo Experimental da Embrapa Amazônia Oriental, rodovia PA-150, km 30; margem do ramal de exploração, lado esquerdo, a aproximadamente 50 m da PA-150, 31 Jan 2001 (fr.), G.C. Ferreira 651 (IAN); Nova Timboteua, Tauarizinho, propriedade do Sr. João Pompeu, 22 Mar 1994 (fr.), N.A. Rosa 5724 (MG); Rio Cuparí, Ingatubinha, entre São Raimundo e Flexal, capoeira, 30 Dec 1947 (fl.), G.A. Black 2159 (IAN, L); Rio Solimões, Igarapé Belém, 10 Dec 1948 (fl.), R.L. Fróes 23705 (IAN); Utinga and Souza, s.d. (fl.), A. Miles Moss s.n. (BM, US, S); Vicinity of Igarapé Kazuo, km 1221, 20 Nov 1977 (fl.), G.T. Prance 25586 (MO, NY); 1877–1878 (st.), M. le Jobert 361 (P). Rondônia: At km 16 on the road to Saldanha close to Guajara-Mirim, tree fall close to road and primary forest, 12 Dec 1977 (st.), J.H. Kirkbride Jr. 2701 (MG); Porto Velho, distrito de Jaci Paraná, beira da estrada próxima a trilha para o Rio Branco, margem da estrada, 29 Oct 2015 (fl.), H. Medeiros 1981 (RB).

ECUADOR. Esmeraldas: San Lorenzo, Parroquia Mataje, Reserva Etnica Awá, Centro Mataje, 01°08'N, 78°33'W, 200 m, 21 Sep 1992 (fl.), C. Aulestiaz et al. 605 (MO).

PANAMA. Colón: Donoso, Teck Cominco Petaquilla mining concession, slope, collected near plot C003, 08°50′22"N, 080°38′51"W, 184 m, 18 Sep 2007 (fr.), G. McPherson 19663 (MO); Donoso, Teck Cominco Petaquilla mining concession, streamside in dense forest, 08°50′20"N, 080°41′28"W, 121 m, 14 Sep 2007 (fl.), G. McPherson 19520 (MO); MPSA mining site, forested slopes in area called Botija Abajo, 08°49′43"N, 080°37′25"W, 92 m, 05 Sep 2014 (fl.), G. McPherson 21586 (MO); Rio Pintamazo, Helipad 22, lowland forest, 8°50′04''N, 80°45′38''W, 55 m, 13 Sep 2012 (fl.), H. van der Werff et al. 24467 (MO, US).

PERÚ. Loreto: Maynas, Carretera Iquitos-Nauta, km 60, 04°10'S, 73°30'W, 150 m, 10 Apr 1988 (fl.), J.C. Ruiz M. 1179 (MO). Madre de Dios: Manú National Park, Pakitsa Station, Tachigali trail N to marker 50, 11°56'S, 71°16'W, 15 Dec 1988 (st.), R. B. Foster 12565 (F, NMNH). Pasco: Oxapampa, distrito Palcazu, Parque Nacional Yanachaga Chemillén, Estación Biológica Paujil, 10°19'S, 75°15'W, 400 m, 22 Oct 2002 (fl., fr.), A. Monteagudo et al. 4224 (NY). San Martín: Lamas, Convento, trail to Nuevo Lamas, km 68 of Tarapoto-Yurimaguas road, 06°16'S, 76°17'W, 200 m, 10 Aug 1986 (fl.), S. Knapp 7961 (MO, NY). Mariscal Caceres, Dtto, Tocache Nuevo, Camino al Pueblo de Viejo Tochache, 19 Jan 1970 (fl., fr.), J. Schunke Vigo 3742 (F, NMNH, NY, US); Mariscal Cáceres, Dtto, Tocache Nuevo, Carretera Marginal de la Selva, about km 50 N of Tocache Nuevo, between Puerto Pizana and Quebrada de Salas, 07°57'S, 76°39'W, 460–470 m, 23 Dec 1986 (st.), T.C. Plowman et al. 11645 (MO). Mariscal Cáceres, Dtto, Tocache Nuevo, Quebrada de Pucayacu, cerca a la Chacra del Sr. Pator González, 03 Sep 1980 (fl.), J. Schunke Vigo 12231 (F, MO, NMNH, NY, RB); Mariscal Cáceres, Tocache Nuevo, Quebrada de Cachiyacu, afluente de la quebrada de Huaquisha, al borde de la quebrada, 500–600 m, 11 May 1975 (fl.), J. Schunke Vigo 8468 (MO, NY).

VENEZUELA. Bolívar: Las Trincheras-Puerto Cabello, 80 m, 11 Jun 1984 (fl.), S. López-Palacios et al. 4678 (NY).

Discussion

The flowers of Aristolochia are regarded as the main source of diagnostic characters in the genus, especially among closely related species (González & Stevenson, 2000a, 2000b; Blanco, 2002; Fernández et al., 2019; Freitas et al., 2020b; Jiménez et al., 2021b; Frank et al., 2022; Jiménez et al., 2023). Here, a case is reported where two closely related species can be entirely distinguished not only by floral features but also by the leaf shape. This was possible by carefully investigating herbarium material and the application of geometric morphometry, a tool that has been shown to exhibit huge potential to unravel complex species relations in diverse genera such as Aristolochia (Freitas et al., 2020b).

By close inspection of collections from French Guiana and Brazil (Amazonas), previously lumped together with A. trilabiata, it becomes obvious that these populations represent a distinct species, described here as A. franzii.

Recognition of A. franzii requires the exclusion of specimens of A. trilabiata from the Flora of French Guiana cited by Feuillet & Poncy (1998), and the inclusion of A. franzii in the Flora do Brasil (Amazonas state) (Freitas et al., 2020a).

No specimens displaying clinal variation with respect to the diagnostic floral characters used to separate Aristolochia franzii from A. trilabiata were found by either visual inspection or geometric morphometry. It is, thus, possible to tell apart the two taxa reliably (for a detailed comparison, see Table 1). A denser sampling in Amazonas, especially the area that is attributed to the southern end of the Guiana Shield, would promote a more precise distributional assessment of the two allopatric species (Fig. 5).