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A new Nidularium species from the Atlantic Forest of Sao Paulo State, Brazil, and issues against nominal extinction.

Introduction

The Brazilian Atlantic Forest today is one of the most endangered ecosystems in the world (Ranta et al., 1998), and the high number of species endemic to the remaining forest fragments suggests that many species have already become extinct before discovery (Morellato & Haddad, 2000; Morawetz & Raedig, 2007).

An average of 15 new bromeliad species from Brazil were described yearly between 1998-2002 (Leme, 2003), most apparently endemic and found in the remaining Atlantic Forest fragments. In the states of Pernambuco and Alagoas, Northeastern Brazil, where the Atlantic Forest is most depleted, and remaining fragments represent only 4.89% of the original forest area (Silva & Casteleti, 2005), 22 new endemic bromeliad taxa have been described in the past 10 years. This represents 23.65% of all known regional species (Leme & Siqueira-Filho, 2007). In contrast, Morawetz & Raedig (2007) estimate a loss of 100 narrowly endemic angiosperm species per year, facing the high rate of deforestation in the Neotropics. These examples highlight our rudimentary knowledge of Atlantic Forest biodiversity and underscore the importance of taxonomy as a basic tool for conservation and for assessing biodiversity patterns (Mayo et al., 2000). Thus, one goal of the modern taxonomists, documentation of species diversity, is trapped in a race against time ordained by habitat destruction and requires activism in "conservation-taxonomy".

Nominal extinction

In the past few years, there have been numerous taxonomic studies of the Bromeliaceae. A growing number of scientists in Brazil and overseas are working to unravel the diversity of the family and more precisely define conceptual taxon limits and phylogeny. As with most revisionary studies, a need will arise for nomenclatural changes including new names, new combinations, revalidations, synonyms, etc., that are promptly dealt with so as to reflect the different taxonomic hypotheses that are proposed.

When new taxonomic hypotheses lead to misguided nomenclatural changes, especially when names of taxa are invalidated, species may become nominally extinct. Nominal species extinction, in contrast to bona fide extinction, is abstract and hypothetical, involving the designation of incorrect synonyms at the specific or infraspecific level (Leme, 2003). For example, in a new taxonomic treatment, two or more species are reduced to heterotypic synonyms of one taxon. Due to an error, the newly synonymized taxa no longer exist for all practical purposes.

Overall, the hypotheses and understanding that we have concerning a given phenomenon do not alter the phenomenon itself. Using the same line of reasoning, the incorrect grouping of one or more taxa under a single epithet does not make these taxa disappear as biological entities. However, due to nominal extinction, taxa may become really extinct if they are no longer the focus of conservation and political decisions and actions. In other words, erroneous nominal extinction may enhance the likelihood of bona fide extinction, and in the case of the Bromeliaceae in the Brazilian Atlantic Forest, it may lead to the loss of associated flora and fauna, magnifying biodiversity loss.

Nominal extinction in "Flora de Sao Paulo" treatment

In this day and age, we cannot improve taxonomic studies of the Bromeliaceae if we do not make an effort to do field research and adopt a new philosophy of collecting botanical samples. As recommended by Brown et al. (1993), bromeliad taxonomists should concentrate on the reassessment and correlation of taxonomic traits, identifying new or under-utilized characters that provide new data and contribute to constructing a more natural system. However, as highlighted by Brown et al. (2008) some of the taxonomic concepts adopted by the recently published taxonomical treatment of Bromeliaceae in the "Flora Fanerogamica do Estado de Sao Paulo" (Wanderley & Martins, 2007) are contrary to the mainstream views of the Bromeliaceae research community, since it neither provided new data, nor a data based justification, to explain the maintenance of older arguably artificial generic concepts for the family, over more recent revisionary changes that are based on focused, systematic monographic study.

In addition, the treatment of Bromeliaceae in the "Flora de Sao Paulo" provides some typical examples of bromeliad taxa that were made nominally extinct. One example involves N. krisgreeniae Leme, in the chapter on Nidularium (Moreira et al., 2007), where taxonomic information available in the literature was neglected and, more importantly, where the taxonomic decisions provided were not based on new, tangibly produced data. Here the authors designated N. krisgreeniae as a new synonym of N. amazonicum (Baker) Linden & E. Morren ex Lindm. based solely on the argument that the first lies within the range of morphological variation of the latter. They also considered N. amazonicum var. paulistanum Wand. & B. A. Moreira to be a "new synonym" of the typical N. amazonicum, despite the fact that this variety had previously been considered a synonym of N. krisgreeniae by Luther (2001) and Leme (2002).

The multiple features that justify the segregation of N. krisgreeniae from N. amazonicum are explicitly provided and illustrated by Leme (2000). Both species, each with distinct geographical range, can be easily differentiated even when sterile by comparing rosette conformation, leaf texture and venation. Other sources of data (e. g., pollen and stigma microstructure, cladistic analysis of morphological data) that distinguish these species from each other are also provided by Halbritter & Till (1998), Gortan & Till (1998) and Brown & Leme (2000). Thus, N. krisgreeniae was made nominally extinguished by Moreira et al. (2007). Concerning N. amazonicum var. paulistanum, the long explanation justifying its inclusion in the synonymy of N. krisgreeniae can be accessed in Leme (2002).

Synonymizing of taxa should not be based only on vague arguments like "there is insufficient material available to confirm the trait attributed to the species" or "species X lies within the range of morphological variation of species Y". We must remember that the inability to perceive certain differences and phenomena is sometimes typical of the observer and occasionally stems from an ideological source. But based on the precautionary principle, if there are no new data and uncertainty still reigns, we must abstain from making changes that can lead to a negative result (i.e., nominal extinction) and indisputable consequences in the real world.

New Nidularium species

Moreira et al. (2007) missed the opportunity to contribute to our understanding of Nidularium biodiversity in the Flora de Sao Paulo treatment by not providing any new collection of these species for Sao Paulo state, and this is exemplified by the following new species, which was recently collected in the region of Tapirai and also belongs to the complex of species of N. amazonicum and N. krisgreeniae.

Nidularium rolfianum Leme, sp. nov. Type: Sao Paulo, Tapirai, between Piedade and Tapirai, road to Cachoeira do Cha, ca. 400 m elev., 7 Jul. 2004, E. Leme 6405 & R. Zorning, fl. cult. Febr. 2008. Holotype: HB. Isotypes: RB, SEL.

[FIGURE 1 OMITTED]
   Species nova a N. krisgreeniae Leme, cui proxima,
   laminis foliorum angustioribus, basin versus
   distincte angustatis, transversin perinconspicue
   nervatis, marginibus basin versus sparse spinulosis,
   inflorescentia bipinnata vel interdum inconspicue
   tripinnata, prope apicem substellata, fasciculis
   primariis basalibus floribus minus numerosis et
   sepalis longioribus differt.


Plants epiphytic, propagating by short basal stolons 4-6 x 1 cm. Leaves ca. 12, green, suberect, laxly rosulate, thinly subchartaceous, forming a narrow funnelform rosette; sheaths narrowly elliptic, 8-10.5 x 3.2-4.5 cm, subdensely and inconspicuously brown-lepidote; blades sublinear-lanceolate, distinctly narrowed toward the base, canaliculate and bearing a slightly thicker median channel toward the base, 17- 32 x 2.5-3 cm, inconspicuously and sparsely white-lepidote on both sides to glabrescent, green, bearing inconspicuous, darker green, irregular transverse lines visible by transmitted light, sometimes ornamented by slightly darker green, irregular apex acuminate and finely apiculate, slightly recurved, margins laxly to subdensely spinose toward the base, spines less than 0.5 mm long, 5-11 mm apart, and densely spinulose near the apex, spines 2-5 mm apart. Scape 7-11 cm long, ca. 0.5 cm in diameter, whitish-green, equaling to slightly exceeding the leaf-sheaths, inconspicuously brown lepidote; scape bracts the basal ones subfoliaceous but shorter than the inflorescence, the upper narrowly ovate, acuminate and shortly apiculate, spinulose. Inflorescence bipinnate to inconspicuously tripinnate, obconic-rosulate, substellate at the apex, ca. 6 cm long, ca. 9 cm in diameter at the apex, exceeding the leaf-sheaths, slightly elevated and distinctly visible above the rosette; primary bracts narrowly ovate, apex narrowly acute and minutely apiculate, 8-10 x 4.5-5.5 cm, with distinction between sheaths and blades, suberect toward the base and recurved toward the apex, the visible parts orange-red, sparsely and inconspicuously white lepidote on both sides, margins densely spinulose toward the apex, spines ca. 0.5 mm long; fascicles ca. 8, subflabellate, complanate, shortly stipitate, the basal ones 30-35 x 15-20 mm (excluding the petals), 2 to 4-flowered in total, sometimes bearing a 2-flowered, single secondary fascicle; floral bracts ovate-lanceolate, apex acute and minutely apiculate, entire to inconspicuously spinulose at the apex, 24-28 x 13- 19 mm, slightly shorter to nearly equaling the sepals, carinate, membranaceous, greenish-hyaline, subdensely and inconspicuously pale-castaneous lepidote, trichomes fimbriate. Flowers 40-49 mm long, odorless, subsessile, pedicels inconspicuous, 1-2 mm long; sepals 24-26 x 8 mm, connate for ca. 4 mm, lobes narrowly elliptic to obovate- lanceolate, obtusely carinate, apex acute and apiculate, glabrous, whitish-green; petals 36- 38 mm long, connate at the base for 7-10 mm, lobes sublinear, erect, 29-39 x 6 mm, green toward the apex except for the white apical margins, bearing 2 long fimbriate appendages at the tube apex, as well as 2 conspicuous longitudinal callosities slightly shorter than the filaments, apex obtuse-cucculate, corolla tubular; filaments the antepetalous ones adnate to the petals for 20-27 mm, the antesepalous ones adnate to the petals tube and free above it; anthers ca. 7 mm long, sublinear, base acute and apex acute and apiculate, dorsifixed at the middle, the antesepalous ones slightly exceeding the antepetalous ones; pollen biporate, broadly oblong-elliptic, pores large, exine reticulate, lumina polygonal, muri narrowed; stigma conduplicate-spiral, ellipsoid, white, lobes with densely crenulate-papillose margins; ovary clavate, trigonous, white, glabrous, ca. 10 mm long, 4-5 mm in diameter; placentation apical; ovules obtuse; epigynous tube crateriform, ca. 1 mm long. Fruits unknown.

Etymology

The name chosen for this new species honors one of its collectors, Rolf Zorning, from Campinas, Sao Paulo, Brazil, a pioneer in the large scale industrial production of ornamental bromeliads, and so one responsible for the popularization of these plants in the country.

[FIGURE 2 OMITTED]

Discussion

Nidularium rolfianum is closely related to N. krisgreeniae Leme, but it differs from it by the narrower leaf blades (2.5-3 cm vs. 3.5-5 cm wide), giving to it a slimmer general appearance. Also, this new species can be distinguished by its leaf blades distinctly narrowed toward the base (vs. inconspicuously if at all narrowly toward the base), bearing very inconspicuous darker green cross-veins by transmitted light (vs. bearing conspicuous and easily visible darker green, irregular cross-veins), basal margins sparsely spinulose (spines 5-11 mm apart vs. 3-5 mm apart), inflorescence bipinnate to sometimes inconspicuously tripinnate (vs. distinctly tripinnate) and substellate at the apex (vs. rosulate-capitate), basal fascicles with 2 to 4 flowers (vs. ca. 5-flowered) and by the longer sepals (24-26 mm vs. 18-22 mm long).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

In "subcomplex amazonicum" of the "white complex" of species proposed by Leme (2000), N. rolfianum holds an intermediate morphological position between its close relatives N. krisgreeniae and N. minutum Mez. It shares with N. minutum the general slimmer appearance, the narrower leaf blades which are canaliculate and distinctly narrowed toward the base, and the usually bipinnate and apically substellate inflorescence.

Nidularium rolfianum, N. krisgreeniae and N. minutum are endemic species of the Atlantic Forest of Sao Paulo state. Nidularium rolfianum was found growing as an epiphyte in the forest understory in the region of Tapirai, from 400 to 800 m elevation, while the typical N. krisgreeniae lives in the region of Sete Barras and Sao Miguel Arcanjo, not far away from Tapirai.

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

[FIGURE 7 OMITTED]

The few specimens from Tapirai identified in herbaria as N. krisgreeniae may very probably represent this new taxon. Nidularium minutum occurs nearby in the region of Santo Andre, at Alto da Serra de Paranapiacaba, where it forms large populations on the forest floor at high altitudes, with N. albiflorum (L. B. Sm.) Leme and N. rubens Mez, which are also members of the "white complex". Nidularium amazonicum is the remaining member of the "subcomplex amazonicum" and it grows typically in the states of Rio Grande do Sul, Santa Catarina and Parana, with putative residual occurrence in Sao Paulo (one specimen collected about 78 years ago in Cotia river (Leme, 2000), which is supposed to belong to the micro-region of Itapecerica da Serra, however, there is a "Cotia river" in the state of Parana too). Another more recent collection (28 Aug. 1999, Leme # 4745 et al., deposited in HB) indicates the presence of this species on a hill of about 200 m elevation in the region of Cananeia, close to the border with Parana State, near the coast.

With this new species, the identification key for the "subcomplex amazonicum" in Leme (2000) must be amended as follows:

42b- Petals connate at the base for less than 1/2 of their length, bearing fimbriate appendages at the apex of the petal tube.

53a- Scape distinctly shorter than the leaf sheaths or exceeding them for ca. 2 cm; petals green or yellowish at the apex with white margins.

54a- Leaf sheaths 5-7 (-12) cm wide; leaf blades 3-6 (-9) cm wide; inflorescence distinctly tripinnate, rosulate-capitate, basal fascicles 5- to 8- (to 13-) flowered.

55a- Leaf blades acuminate-caudate; scape distinctly shorter than the leaf sheaths; inflorescence sunken in the leaf-rosette; primary bracts suberect-recurved toward the apex; flowers sessile.

43- N. amazonicum.

55b- Leaf blades acute to acuminate; scape equaling to slightly exceeding the leaf sheaths; inflorescence equaling to slightly elevated above the leaf-rosette; primary bracts recurved to revolute toward the apex; flower pedicels 2-3 mm long.

44- N. krisgreeniae.

54b- Leaf sheaths 3.2-4.5 cm wide; leaf blades 2.5-3 cm wide; inflorescence usually bipinnate to inconspicuously tripinate, substellate at the apex, basal fascicles 2- to 4-flowered.

44a- N. rolfianum

53b- Scape distinctly exceeding the leaf sheaths for 1.5-2.5 times of their length; inflorescence bipinnate, stellate at the apex; petal apex totally white.

45- N. minutum.

Conclusion

The issues of synonymy and formal extinction are indisputably complex. Clearly, there is a need for legitimate, objective, data-driven synonymy in taxonomy. However, superfluous synonym can have adverse consequences, and this type of taxonomic error in the past probably had no effect on the real world, and could await corrective measures in the subsequent taxonomic revisions. Today however, especially in highly endangered biomes like the Atlantic Forest, any one of man's activities, academic or not, that interferes negatively with conservationist activities and policies leads to real consequences that cannot be ignored. As stressed by Ibisch (2008), in a rapidly changing world with declining biodiversity it becomes ever more difficult and even questionable to study the richness of life without looking beyond the pure natural sciences. He concluded: "without being responsible by the imminent threats to biodiversity, those naturalists who close their eyes and pretend they cannot make a difference become accomplice to the destruction of nature". In synthesis, a "conservation- taxonomy" activism is more than desired. It is urgently needed.

Acknowledgements

We thank Rolf Zorning for his companionship and support during field studies in the region of Tapirai, Sao Paulo, as well as Gregory K. Brown for reviewing the manuscript and for his valuable comments and suggestions.

Literature cited

Brown, G. K. and E. M. C. Leme (2000). Cladistic Analysis in the Nidularioid Complex. Nidularium -Bromeliads of the Atlantic Forest. Rio de Janeiro, Sextante: 240-247.

Brown, G. K., H. Luther, et al. (1993). "Comments on the responsibility of taxonomists." J. Bromeliad Soc. 43(4): 154-156.

Brown, G. K., W. H. Till, et al. (2008). "A review: Bromeliaceae--Flora Fanerogamica do Estado de Sao Paulo." J. Bromeliad Soc. 58(4): 159-162.

Gortan, G. and W. H. Till (1998). Stigma morphology of Nidularium and related genera. Canistropsis, Bromeliads of the Atlantic Forest. E. M. C. Leme. Rio de Janeiro, Salamandra: 124-131.

Halbritter, H. and W. H. Till (1998). Morfologia Polinica do Complexo Nidularioide. Canistropsis--Bromeliads of the Atlantic Forest. E. M. C. Leme. Rio de Janeiro, Salamandra: 114-121.

Ibisch, P. L. (2008). "Messages from a Worst-Case Scenario: Mata Atlantica in Northeastern Brasil." CONSERV BIOL 22(4): 1078-1079.

Leme, E. M. C. (2000). Nidularium: Bromeliads of The Atlantic Forest. Rio de Janeiro, Sextante Artes.

Leme, E. M. C. (2002). "Two Nidularium Species from Sao Paulo State, Brazil: Synonyms and Further Comments." J. Bromeliad Soc. 52(5): 195-201.

-- (2003). "Nominal Extinction and the Taxonomist's Responsibility: the Example of Bromeliaceae in Brazil." TAXON 52: 299-302.

Leme, E. M. C. and J. A. Siqueira-Filho (2007). Taxonomic Considerations Correlated with Bromeliaceae of Pernambuco and Alagora. Fragments of the Atlantic Forest of Northeast Brazil, Biodiversity, Conservation and the Bromeliads. J. A. Siqueira-Filho and E. M. C. Leme. Rio de Janeiro, Andrea Jakobsson Estudio: 383-407.

Luther, H. (2001). "De Rebus Bromeliacearum III." Selbyana 22(1): 34-67.

Mayo, S. J., E. G. Goncalves, et al. (2000). Refuges, Fragmentation and Biodiversity Conservation: The Case of the Araceae. Topicos Atuais em Botanica, Palestras Convidadas do 51[degrees] Congresso Nacional de Botanica, Embrapa, Brasilia.

Morawetz, W. and C. Raedig (2007). "Angiosperm biodiversity, endemism and Conservation in the Neotropics." TAXON 56(4): 1245-1254.

Moreira, B. A., M. G. L. Wanderley, et al. (2007). "Nidularium " Bromeliaceae 5 95-109 Fundacao de Amparo Pesquisa do Estado de Sao Paulo, Sao Paulo.

Morellato, L. P. C. and C. F. B. Haddad (2000). "Introduction: The Brazilian Atlantic Forest." BIOTROPICA 32(4B): 786-792.

Ranta, P., T. Blom, et al. (1998). "The Fragmented Atlantic Rain Forest of Brazil: Size, Shape and Distribution of Forest Fragments." BIODIVERS CONSERV 7(385-403).

Silva, J. M. C. and C. H. M. Casteleti (2005). Estado da biodiversidade da Mata Atlantica brasileira. Mata Atlantica, biodiversidade, ameacas e perspectivas. C. Galindo-Leal and I. G. Camara. Belo Horizonte, Fundacao SOS Mata Atlantica, Conservacao Internacional & Centro de Ciencias Aplicadas Biodiversidade: 43-59.

Wanderley, M. G. L. and S. E. Martins (2007). "Bromeliaceae." Bromeliaceae 5: 39-43, Fundacao de Amparo Pesquisa do Estado de Sao Paulo, Sao Paulo.

Elton M. C. Leme. Illustrations by the Author.
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Title Annotation:Scientific
Author:Leme, Elton M.C.
Publication:Journal of the Bromeliad Society
Article Type:Report
Geographic Code:3BRAZ
Date:Nov 1, 2009
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