Eithea lagopaivae Campos-Rocha & Dutilh, 2017

Campos-Rocha, Antonio, Meerow, Alan William, Lopes, Edimar Faria Menezes, Semir, Joao, Mayer, Juliana Lischka Sampaio & Dutilh, Julie Henriette Antoinette, 2017, Eithea lagopaivae, a new critically endangered species in the previously monotypic genus Eithea Ravenna (Amaryllidaceae), PhytoKeys 85, pp. 45-58 : 47-53

Eithea lagopaivae Campos-Rocha & Dutilh sp. nov. Figures 1 , 2

Diagnosis.

Eithea lagopaivae differs from E. blumenavia (Figure 3 ) by its smaller size, one flowered inflorescence (vs. 2-6, very rarely 1), a fully hollow scape (vs. solid in the lower fifth), terminated by spathe bracts fused for more than the lower fifth of their length (vs. free or fused up to the lower fifth), absence of bracteoles (vs. presence), white or only very lightly striated flowers (vs. strongly striated) and lateral and lower petals of similar width (vs. lateral petals up to twice the width of the lower).

Type.

BRAZIL. São Paulo: Piracicaba , sub-bosque de uma plantação comercial de Eucalyptus abandonada, 07 Dec 2016, A. Campos-Rocha 1654 (holotype: UEC!; isotypes: NA!, RB!) .

Description.

Geophytic herb 12-25 cm tall. Bulb subterranean, globose to ovoid or obovoid, tunicate, whitish or with a thin grey-brownish outer tunic, 1.3-3.5 cm long and 1.2-3 cm diameter; neck formed by sheathing leaf bases up to 4.5 cm long and 3-8 mm diameter (occasionally very short to absent). Leaves 1-3(-4), suberect, dark green adaxially, pale green abaxially, frequently pseudopetiolate; pseudopetiole flattened adaxially, rounded abaxially, greenish, with reddish pigmentation near the base or throughout its length, up to 9.5 cm long, 2-5.5 mm wide; lamina linear, narrowly elliptic or oblanceolate to slightly falcate, apex acute, frequently asymmetric, base attenuate, margin flat, venation transverse reticulate (with short transverse veins between the longitudinal ones), midrib inconspicuous adaxially, prominent abaxially, 8-20.8 × 1.1-2.6 cm. Inflorescence one flowered; scape erect, cylindrical, slightly laterally compressed, hollow and fragile, greenish, sometimes with reddish pigmentation near the base, 7.8-30 cm long and 2.4-6 mm diameter, elongating and becoming decumbent with fructification; spathe bracts 2, tubular, fused in the basal 0.4-2.4 cm, apex acute, whitish, generally light rose colored at the tip before opening, turning papery, 1.7-3.8 cm long. Pedicels greenish, (0.3-)1.3-5.5 cm long, often elongating with fructification to 6.5 cm long. Perigone campanulate to infundibular, white (in bud white with a rose colored tip), usually with faint thin magenta striations on the sepals and petals, especially on the upper sepal, with greenish pigmentation near the base, mostly close to the midrib, 3-5.8 cm long; hypanthium greenish, 2-4.5 mm long, paraperigone of fimbriae 0.5-2 mm long at the throat. Sepals much wider than the petals, oblanceolate to obovate, the upper one wider and longer, apex acute, apicule subapical; upper 2.7-5.6 × 1-2.4 cm, apicule 0.8-2 mm long; lateral 2.5-5.4 × 0.6-2 cm, apicule 0.6-1.4 mm long. Petals oblanceolate, apicule inconspicuous or absent; lateral 2.5-5.5 × 0.6-1.4 cm; lower slightly narrower, 2.5-5.5 × 0.4-1.2 cm. Filaments 6, in four different lengths, inserted at the mouth of the hypanthium tube, shorter than limb segments, declinate-ascending, free portion white; upper episepal 1.1-2.5 cm long; lateral episepal 1-2.2 cm long; lateral epipetal 1.7-4 cm long; lower epipetal 1.6-3.8 cm long. Anthers oblong to oblong-reniform, dorsifixed, versatile, dehiscing longitudinally, 2.5-5 mm long before anthesis; pollen pale yellow. Ovary trilocular, obtuse trigonal, obovoid, greenish, 3.5-9 mm long and 3-8 mm diameter; 8 -14 ovules per locule; ovules 0.6-1 mm long. Style declinate-ascending, white, occasionally with greenish pigmentation near the base, 2.6-5 cm long; stigma trifid, white, lobes already expanded when the flower opens, occasionally of different lengths, 1.5-4.5 mm long. Fruit capsule loculicidal, globose to globose-compressed trilobed, greenish when ripe, occasionally with reddish pigmentation, cream colored inner side, 1-2.5 cm long and 1.2-2.6 cm diameter. Seeds irregular, angular, with grey brownish to black testa containing phytomelanin, 3.5-6 mm long and 3-5.5 mm diameter, with wrinkled elaiosome up to 4.5 mm long.

Distribution, habitat and ecology.

Eithea lagopaivae is known from only two small populations separated about 50 km, each composed of less than 50 individuals. The type population (Piracicaba) occurs in the understory of an abandoned Eucalyptus plan tation, next to fragments of deciduous and semideciduous forest, where the Corumbataí river meets the Piracicaba river. The second is located in a small fragment of semideciduous forest, near the junction of the basins of the Piracicaba and Tietê rivers in the municipality of Tietê (Figure 4 ). Both fragments are located on gravelly soils of litholic limestone origin ( Oliveira and Prado 1989). The region presents a well-defined seasonality, with total annual rainfall of 1230 mm and precipitation of 50 mm or less, for six months, during autumn and winter. During spring and summer, rainfall exceeds 100 mm for six months, reaching close to 250 mm in January ( EMBRAPA 2003). Ants were observed removing elaiosomes from the seeds of E. lagopaivae in their natural habitat, indicating that these animals might be dispersal agents, as is known for Griffinia .

Phenology.

Eithea lagopaivae has been collected in bloom between October and January, and occasional blooming occurs until early March. Fruits have been observed from November.

Conservation status.

With estimated AOO of 8 km2 and EOO of 13.7 km2, Eithea lagopaivae can be considered as Critically Endangered [CR, B1ab(iii) + B2ab(iii)], due to the low number of known locations (≤ 5) and decline in quality of habitat ( IUCN 2016). In the municipality of Piracicaba, at the end of the year 2016, when the species was again visited, two small scattered groups were encountered ca. 500 meters apart. The smaller of the two groups was in a trash dump on the side of the wooded area, and the second in an area of higher humidity, near a small stream. This fragment, on the edge of the urban sprawl of Piracicaba, is highly disturbed and subject to regular episodes of fire. The population of the Tietê municipality is in a slightly larger fragment of semideciduous forest with an impoverished understory, intense edge effects, with many lianas and invasive exotics. The area is located within a livestock breeding facility.

Etymology.

The epithet is a tribute to Celso do Lago Paiva, environmental analyst at ICMBio, who has collected the plant for the first time and has dedicated his life to the study and conservation of the flora of Brazil.

Additional specimens examined.

BRAZIL. São Paulo: Piracicaba , 18 Mar 1999, J. Dutilh s.n. (UEC-170468!); 17 Nov 1999, J. Dutilh s.n. (UEC-174104!); 29 Nov 1999, J. Dutilh s.n. (UEC-174105!); em cultivo no Jardim Botânico Plantarum, Nova Odessa-SP, 10 Oct 2012, A. Campos-Rocha 810 (NA!, RB!, UEC!); em cultivo em Campinas-SP, 10 Oct 2013, A. Campos-Rocha & J. Dutilh 1165 (NA!, UEC!); plantação abandonada de Eucalyptus , 09 Oct 2016, A. Campos-Rocha & R.M. Goffi 1626 (UEC!); plantação de Eucalyptus abandonada, 20 Nov 2016, A. Campos-Rocha 1647 (NA!, UEC!). Tietê, 20 Nov 2001, J. Dutilh & L.C. Bernacci s.n. (UEC-170469!); L.C. Bernacci et al. 4483, fragmento de floresta semidecídua, 03 Mar 2017 (IAC!, UEC!) .

Notes.

Eithea lagopaivae and E. blumenavia form a clade with maximal support in all phylogenetic analyses performed by García et al. (2017). Eithea lagopaivae can be distinguished from E. blumenavia by a number of characteristics (Table 1 ). It is a smaller plant (ca. 12-25 cm), usually with 2-3 leaves, rarely 4, which are deciduous before the onset of winter. Eithea blumenavia however is evergreen, with 2-8 leaves, and up to 50 cm in height, although specimens of extremely reduced size are known, also with several flowers.

Eithea lagopaivae is known from an area originally of deciduous and semideciduous forests with a well-defined dry season. In turn, E. blumenavia is found in wetlands of the Atlantic rainforest, from the south of the state of São Paulo to eastern Santa Catarina ( Dutilh 2010, Dutilh and Oliveira 2015) (Figure 4 ), especially in the coastal mountains. The region has some of the highest average annual rainfall (1650 mm) of any area of extra-Amazonian Brazil, distributed throughout the year, but more intensely during the summer, although with an average under 200 mm/month. From April to July, monthly averages are close to 100 mm ( EMBRAPA 2003).

Eithea blumenavia is considered an Endangered (EN) species ( MMA 2014).

Anatomy.

The three most obvious anatomical characteristics differentiating the two species of Eithea are: 1. Margins and cortex of the pseudopetiole (Figure 5A-B ); 2. Ornamentation and shape of the epidermal cells on the adaxial side of the leaf blades (Figure 5C-D ); 3. Presence or absence of protrusions on the upper side of the blades in the region of the midrib (Figure 5I-J ).

Cross section of pseudopetiole margins of E. lagopaivae are flatter, more laminar (Figure 5A , arrow) than those of E. blumenavia , which are angular (Figure 5B , arrow). The pseudopetiole is composed by chlorenchyma, aerenchyma and vascular bundles. In E. lagopaivae , 1-3 aerenchyma lacunae were found below the vascular bundles (Figure 5A ), while in E. blumenavia several lacunae above and below the bundles could be observed (Figure 5B ).

In the cross section of leaf lamina, epidermal cells were more elongated in E. lagopaivae and polyhedral in E. blumenavia (Figure 5C-D , respectively). We found periclinal thickening on the outer wall of the epidermal cells of both species as occurs in Hippeastrum puniceum (Lam.) Kuntze ( Alves-Araújo et al. 2012). Ornamentation of the external periclinal epidermal cell wall of E. blumenavia (Figure 5D , arrow) was not found in E. lagopaivae (Figure 5C ). Mesophyll of E. lagopaivae and E. blumenavia is composed of about 6-8 layers of chlorenchyma with arm-palisade cells (also called arm-cells, H-palisade or H-cells) (Figure 5E-F ), which showed their typical morphology in paradermic sections (Figure 5G-H ). Arm-cells were first described by Haberlandt (1880) as a morphological modification of palisade cells and seem to be more common in plants of forest understory, probably increasing photosynthetic capacity ( Chatelet et al. 2013). In the midrib region, the lacunae of the aerenchyma were larger and wider in E. lagopaivae than in E. blumenavia (Figure 5I-J ).

A protrusion on the abaxial leaf surface opposite the central vascular bundle was evidenced in both species (Figure 5I-J , arrows) and the parenchyma cells in this region were regular and rounded. However, adaxial surface of the leaf in E. lagopaivae was flat (Figure 5I ), while in E. blumenavia it was possible to observe two protrusions opposite to the vascular bundles adjacent to the midrib (Figure 5J , arrowheads). The alternation of aerenchyma with vascular bundles found in Eithea species was described for other species of the family ( Arroyo and Cutler 1984, Meerow 1989, Raymúndez et al. 2000, Alves-Araújo et al. 2012). In Eithea , lacunae of aerenchyma in the pseudopetiole and leaf blade may have been originated by lysis, as suggested for Griffinia , Habranthus , Hippeastrum and Nothoscordum Kunth ( Alves-Araújo et al. 2012); however leaf development studies are needed to confirm this hypotheses.

Figures

Figure 1. Eithea lagopaivae A Habit in flower B Detail of leaf venation C Spathe bracts D Flower with perigone removed, showing stamens and style E Sepals and petals F Tips of sepals and petals F 1 Upper sepal F 2 Lateral petal F 3 Lateral sepal F 4 Lower petal G Detail of fimbriae of the paraperigone H Stigma I Longitudinal section of the ovary J Cross section of the ovary K Habit in fruit L Fruit M Seed.

Figure 2. Eithea lagopaivae A Typical habitat (October 2016) B Individual plant flowering amid trash dumped at type locality C Flowering plant (Campos-Rocha 1647) D Flower buds E Flower, frontal view (Bernacci 4483) F Flower buds and flowers (Campos-Rocha 1654) G Plants in fruit H Mature capsule exposing the seeds I Seed (elaiosome indicated by the arrow).

Figure 3. Eithea blumenavia A Flowering plants in habitat B Lateral view of inflorescence C Detail of spathe bracts D Bracteoles (white arrow) E Sepals and petals (adaxial view) separated from stamens and style. B-E of Campos-Rocha 1624, UEC.

Figure 4. Distribution map showing collections of Eithea lagopaivae (red circles) and E. blumenavia (black diamonds). PR = Parana. SC = Santa Catarina. SP = Sao Paulo.

Figure 5. Comparative leaf anatomy of Eithea lagopaivae and E. blumenavia. A Cross section of the pseudopetiole of E. lagopaivae and B E. blumenavia C Cross section detail of the adaxial epidermis of E. lagopaivae and D E. blumenavia E Cross section of the leaf blade of E. lagopaivae and F E. blumenavia G Longitudinal paradermic section detail of the leaf blade, showing the arm-cells of the chlorenchyma in E. lagopaivae and H E. blumenavia (slide of stained fresh material) I Cross section of the leaf blade in the midrib region of E. lagopaivae and J E. blumenavia. * = arm-cell; ab = abaxial epidermis; ad = adaxial epidermis; ae = aerenchyma; ep = epidermis; vb = vascular bundle. Scales bars: 500 µm (A, B); 10 µm (C, D), 50 µm (E, F), 20 µm (G, H); 200 µm (I, J).