DISCUSSION Neoregelia pernambucana is one of the most interesting taxa discovered to date because of its unique combination of morphological features. The foliage of sterile plants is easily confused with Wittrockia cyathiformis or W. gigantea because
the leaves are broad with dark spots and well-developed spines (2-5 mm long). The orange fruits are very similar to those of these two species. This fruit color has not been reported before in other Neoregelia species.
An analysis of the remaining traits of N. pernambucana suggests a closer association with the genus Neoregelia. The leaf anatomy of this species is very similar to that of N. johannis and it also approaches N. kautskyi and N. johnsoniae in some features (Sajo, pers. comm.).The internal organization of N. pernambucana leaves is identical to that of these other species of Neoregelia subgen. Neoregelia. These species have a water-storage hypodermis on the adaxial leaf surface which is absent in W. cyathiformis and W. gigantea. The fibers surrounding the vascular bundles contain cellulose (they are lignified in the aforementioned species of Wittrockia) and the chlorophyll-containing parenchyma is more or less radially arranged around the vascular bundles, a trait that is not seen in the
two Wittrockia species (Sajo; pers. comm.; Sajo et al., 1998)
The subspreading leaf arrangement of N. pernambucana at anthesis, forming a broad crateriform rosette, is similar to the strategy adopted by several species of the type subgenus of Neoregelia (e.g., N. johannis and N. concentrica). Due to a considerable capacity to accumulate water, N. pernambucana is often used as a birdbath (e. g., by Tangara fatuosa and T. cyanocephala).The simple inflorescence, wide at the apex and many-flowered, shows the same affinity pattern as mentioned above. However, the shape and size of the sepals (48-52 x 7-8 mm), the very long petals (55-62 mm long), anthers dorsifixed near the base and the absence or near absence of an epigynous tube suggest that this species is more in line with the concept of Neoregelia subgen. Longipetalopsis.
Of the known species of Longipetalopsis, N. menescalii is most closely related to N. pernambucana. But the latter is easily distinguished from N. menescalii by its longer, distinctly dark-green-spotted leaves and broadly capitate inflorescence, 11-12 cm in diameter at the apex. It also has attenuate-acuminate sepals, shorter connate at the base, and green petals at the center of the inflorescence which are acuminate and short connate at the base. The odorless flowers of N. pernambucana have erect corollas, or nearly so, at anthesis and these are long-tubular as in N. longipedicellata. This trait is rare in Neoregelia but it is part of pollination strategy in Wittrockia and Nidularium (see chapter 5 and the following section).
The affinity between N. menescalii and N. pernambucana does not necessarily imply a direct mutual derivation of these taxa. Evidence points to the former existence (or perhaps even a residual presence today) of nidularioid species in Brazil's northeastern Atlantic forest, north of Bahia, that, if known to science, would portray a clearer
phylogenetic lineage uniting these taxa. Since most of the Atlantic forest has been eliminated from this region, however, and its physiognomy and flora have been drastically changed over centuries (Coimbra Filho & Camara, 1996), countless species have most surely become extinct such as those of the understory that are dependent on forest microclimate.The majority of the nidularioid complex species fall in this category.
Observations recorded during field work in Paraiba in 1998 serve as an example. Due to favorable soil conditions and humidity on the coast near Joao Pessoa, Santa Rita (Mata dos Guaribas), and also farther inland at Serra do Caja, the forests that we visited are equivalent to the Atlantic forest in physiognomy and have a good number of epiphytes. However, it is clear that the bromeliad epiphytes most common today in these forests (e.g., Aechmea lingulata, Hohenbergia sp., Tillandsia polystachia, T. recurvata and T. juncea) are but a poor sample of what once was. These are sun-loving species and can even live in caatinga vegetation. The bromelioids (i. e., Aechmea lingulata and Hohenbergia sp.) can easily become established on the ground or on rocks, while the tillandsioids (i.e., Tillandsia spp.) typically have plumed seeds that can be dispersed over great distances by the wind. Only these species managed to survive (the bromelioids) or to recolonize (the tillandsioids) these forests after each cycle of deforestation and subsequent natural regeneration.
Once the forest had been cut down, only sun-loving bromeliads or those that also grow on the ground or on rocks would have been able to survive in these exposed habitats, returning to the forest once it had regenerated. Sun-loving, wind-dispersed species would also be capable of returning to these habitats, arriving from remnant patches farther away. On the other hand, the bromeliad species typical of the Atlantic forest understory, as a rule, are delicate, often small, plants unable to survive extreme environmental change (i.e., full sunlight, low humidity etc.) and would swiftly disappear.
Although these forests are quite suited to supporting delicate understory bromeliads, what we see today are empty niches. The forests resemble "houses without inhabitants" or "the living dead" (Janzen,1988). It is for this reason that today we feel a deep sense of frustration when faced with the impossible task of tracing a clearer phylogeneric lineage for new species such as N. pernambucana that are still being discovered.
DISTRIBUTION & HABITAT
The known geographic range of the subgenus Longipetalopsis was restricted to South-eastern Brazil (ES, MG, RJ and SP) plus Bahia in the Northeast. The discovery of this new species has pushed the limit farther north, leaving a gap in the states of Sergipe and Alagoas.
Neoregelia pernambucana was found in a rare patch of well-preserved Atlantic forest in the state of Pernambuco, in an area belonging to the Usina Frei Caneca. According to the
owner, Gustavo J. P. S. Barros, this sugar mill was founded in 1887 by the Barao de Lucena, and is one of the oldest in Pernambuco. This region of rolling hills and sharp relief, well suited to the sugarcane monoculture that has dominated the landscape for most of its history is reported to be a center of endemism of Atlantic forest species (Brown, 1979; Prance, 1979,1982). Forest cover in southern Pernambuco has been
drastically reduced, mainly due to this type of agriculture, and today only 7% remains in forest patches with over 100 hectares (Ranta et al., 1998)
Serra do Urubu (8°42'37"S; 35°50'01”W), a spur of the Borborema Plateau, is contained within the borders of the Usina Frei Caneca property in the municipalities of Jaqueira
and Lagoa dos Gatos. It is one of the last remaining plant and animal refugia in Pernambuco. It lies in the Zona da Mata (forest zone) of southern Pernambuco, near the border with Alagoas, about 160 km from Recife. Sugarcane and banana fields cover the lowlands (some 500 m above sea level) on Usina Frei Caneca (Usina Colonia) property; there are six dams and two hydroelectric plants that supply electricity for the mill. The only densely forested areas left are on the hilltops at 600-750 m above sea level. Clouds
often cover these higher elevations during the day, even in the dry season, and the dense fog creates an ideal microclimate for the survival of the more delicate and demanding bromeliad species. These conditions are typical of montane Atlantic forest (Veloso et al., 1991).
Neoregelia pernambucana was discovered at higher elevations in the Mata da Serra do Quengo, as one part of the Serra do Urubu is called. It grows in tufts on the uppermost branches of 30-40-meter-tall trees that make up the forest canopy. It is difficult to identify this new bromeliad from a distance because the clumps look very much like those of the sympatric species Portea leptantha and Hohenbergia ramageana. These plants are probably found only in the canopy because they have been removed from other
forest layers. Neoregelia pernambucana is a very attractive species, mainly due to the intense red color of its leaves, and this probably brought it to the eye of illicit plant collectors that still roam the forests in this area. Plants in the lower strata of the forest would be more accessible and would have been quickly eliminated by these collectors.
Furthermore, N. pernambucana grows readily when transplanted to the shade of the understory. In contrast, some local species of Vriesea from the canopy cannot withstand the increased accumulation of organic matter at lower levels (J. Siqueira, pers. obs.).
N. pernambucana flowers from December to January and produces fruit in August. Two to five flowers open daily on the many-flowered inflorescence, which has an average of 48 ± 12.12 (N=4) flowers. The long flowering period (over 30 days with only a few flowers opening each day suggests a uniform access strategy (Gentry, 1974).This flowering strategy was reported in Canistrum aurantiacun (Siqueira, 1998), another
nidularioid species from Pernambuco.
Anthesis begins around 4:20 a.m., when it is still dark, and this must be when the hawkmoths visit the flowers. The long-tubular corolla is made up of erect, or nearly so, petals, each with a lilac or white apex. The corollas rise above the large volume of water accumulated in the central tank of the plant. The flowers are accessible to hummingbirds until 5 p.m. when the petals begin to twist downward in a movement typical of Neoregelia (Leme, 1998).
Although hummingbirds have not been seen visiting N. pernambucana, the flower morphology of this species (tubular corolla up to 62 mm long) plus volume [76.63 ± 18.05 µl (N=6)] and concentration [32.51 ± 1.31% (N=6)] of nectar suggest that these visits do take place. Pollination is probably carried out by long-billed hummingbirds, such as Phaethorninae, who have a high energy demand. These birds have an enhanced field of vision and may be attracted to this bromeliad's bright-red dark-spotted leaves.
Three hummingbird species, Phaethornis ruber, P. pretrei and Glaucis hirsuta, were observed visiting other Bromeliaceae in the area. It is important to note that the large amount of nectar secreted by N. pernambucana could be related to the length of the corolla. This taxon has the longest petal tube and the highest volume of nectar per flower of the 33 species that make up the local bromeliad community.
Neoregelia pernambucana has orange fruits, each with a persistent calyx up to 52 mm long.The long calyx facilitates dispersor activity. The fruit is immersed in the water
accumulated in the central tank of the plant but the long calyx rises above water level. Birds such as the Thraupinae remove the fruit by tugging on the calyx. Tangara
cyanocephala and T. fastuosa were seen feeding on the fruits of N. pernambucana. The latter species is endemic and threatened with extinction (Sick, 1997). Pipra rubrocapilla
(Pipridae) disperses Canistrum aurantiacum fruit (Siqueira, 1998) and may also disperse N. pernambucana seeds.
Very little information is available on the number of seeds produced by bromeliad species. In the wild, each N. pernambucana fruit produces 716.57 ± 49.25 seeds
N=7). This number is high when compared to C. aurantiacum which produces 28 ± 13.10 seeds (N=140; Siquiera, 1998).
THE CHALLENGE OF CONSERVATION BIOLOGY
Species richness in the Atlantic forest of Brazil is very high, but this biome has also suffered from a long history of deforestation and manmade habitat fragmentation brought
about by agricultural practices in the 16th century (Tabarelli et al., 1999). In spite of the destruction of natural areas, the number of bromeliad species recorded in Pernambuco has increased considerably, especially in the last few years. Marcgrave (1643) mentioned only five taxa and that number rose to 43 in A. Lima's survey, published in 1966. In a more recent study, 72 species were identified for the state (J. Siqueira, unpub. data), the discovery of N. pernambucana being one of the results of this work.
The Serra do Urubu site has played an important role in more recent surveys because a significant percentage of the Atlantic forest species are found here. A total of 33 bromeliad species belonging to 17 genera have been recorded for this area (Siqueira, 1998), as well as other non-bromeliad taxa which serve as bio-indicators of healthy ecosystems. Some of these are endemic to the area. There are 22 anuran species (A. Carnaval, pers. comm.), 110 bird species (A. Roda, pers. comm.) and 35 mammal species (Siqueira, pers. obs.). Other records are especialiy meaningful such as that of Bothriophis bilineata (Viperidae), seen foraging in bromeliads inside the forest; this snake was last reported in Pernambuco 59 years ago.
The future of forests like those found on the Serra do Urubu will depend on an increased understanding of the mechanisms of plant-animal interactions that are unique to this delicate species-rich ecosystem (Mori, 1994). Habitat fragmentation is a permanent reality today and is also the main cause of biodiversity loss. Species such as N. pernambucana that have strict niche requirements (e.g., humidity light and the epiphytic habit and specific pollinators and dispersors suffer acutely from this fragmentation (Murcia,1995; Renner, 1998) and are extremely vulnerable to manmade disturbance.This species has an estimated population of under 100 plants and is therefore classified as rare. However, other natural populations of this species may be discovered in similar
mountainous areas in the state of Alagoas.
Although scienrtists agree as to the effects of habitat fragmentation on pollination, it is hard to quantify these effects given the complexity of the variables under consideration (Renner, 1998). An example that illustrates the impact of fragmentation on bird-pollinated species of Bromeliaceae is the role of co-pollinator played by Coereba
flaveola. This bird is an opportunist and may fill in for legitimate pollinators, when these are absent, or in disturbed areas (Sazima & Sazima, 1999).
Attempts to understand pollination and reproduction in N. pernambucana are essential if we are to succeed in saving this species from impending extinction. However, broader
measures must be taken to guarantee the survival of these populations at the Serra do Urubu site where we find the most important Atlantic forest fragments (areas over 500
hectares) in the Zona da Mata of southern Pernambuco. Among the proposals set forth by Mori (1989) is the need to preserve forests in regions of high endemism in Pernambuco
as well as the need to study plant-animal interactions, especially of economically important species.
The Serra do Urubu was recently classified as a priority conservation area during a meeting in Atibaia, Sao Paulo, that was held to determine which areas of Atlantic forest
should be preserved (M. Tabarelli, pers. comm.). This is a step in the right direction to preserve local biodiversity. In addition to this measure, forest corridors connecting Atlantic forest fragments must be established and private reserves created. Equally important is the development of research and nature education projects that involve local
communities. Fortunately the Usina Frei Caneca has adopted some of these measures in an effort to guarantee the preservation of Pernambuco's last remnants of Atlantic forest. —SeeLeme 2000a
