Floristics and life-forms along a topographic gradient , central-western Ceará , Brazil

Universidade Federal do Ceará, Depto. Biologia, Centro de Ciências, bloco 906, Campus do Pici, 60455-760, Fortaleza, CE, Brazil. Correponding author: tchesca@ufc.br Abstract To test whether the flora is organized in discrete or continuous units along a topographic gradient, three physiognomies were assessed on different soil classes in a semi-arid region of northeastern Brazil: caatinga (xeric shrubland) at altitudes from 300 to 500 m, deciduous forest at altitudes from 500 to 700 m and carrasco (deciduous shrubland) at 700 m. In each physiognomy a species inventory was carried out, and plants were classified according to lifeand growth-forms. Species richness was higher in the deciduous forest (250) than in the carrasco (136) and caatinga (137). The caatinga shared only a few species with the carrasco (6 species) and the deciduous forest (18 species). The highest species overlap was between the deciduous forest and the carrasco (62 species). One hundred and four species occurred only in the caatinga, 161 only in the deciduous forest and 59 only in the carrasco. Woody species predominated in physiognomies on sedimentary soils with latosol and arenosol: 124 species occurred in the deciduous forest and 68 in the carrasco. In the caatinga on crystalline basement relief with predominance of planosol, herbs showed the highest species richness (69). Comparing the biological spectrum of Brazilian plant life-forms, the caatinga stood out with higher proportion of therophytes and chamaephytes. Considering the flora of the three phytophysiognomies studied here, we can affirm that the caatinga is a discrete floristic unit.


Introduction
At a global scale, the main environmental variables used to classify vegetation are climate zones.A group of similar vegetation types that occur in similar climate zones in different continents is known as a vegetation-type or biome (Whittaker 1975(Whittaker , 1978a, b;, b;Box & Fujiwara 2005).
Changes in topography or microclimate can affect the biology of the vegetation, leading to particularities that can be detected only at a local scale (Spellerberg & Sawyer 1999).Gradual changes in climate related to topography or to distance from the ocean, at a small scale, result in continuous vegetation units, which makes a classification based on floristic attributes difficult.However, when a climate variable is associated with different soil types, the regional flora may be discontinuously distributed, forming discrete communities, whose limits, along a topographic gradient, can be determined by an analysis of floristic composition and of the main growth-or life-forms of the plant species (Whittaker 1975;Box & Fujiwara 2005).
To describe community types it is necessary to characterize plant forms, since physiognomy results from the dominant forms that compose a community (Whittaker 1975).Classes or types of plant forms are called growth-forms; this classification usually does not correspond to the categories used by taxonomists to classify plants.Height, woody or herbaceous habit, stem form, leaf form and intensity of leaf deciduousness are characteristics used to define the following types of growth-forms (Whittaker 1975): trees, shrubs, lianas, epiphytes, herbs and thallophytes.
Instead of using a system of multiple characteristics such as the growth-form system proposed by Whittaker (1975), the life-form system of Raunkiaer (1934) is based on a single characteristic: the relationship between the position of the perennial tissue (meristem), which remains inactive during the winter or dry season, and the growth surface.The life-form of a species represents a set of life history characteristics selected by the environment.Raunkiaer (1934) classified plants into five life-forms: phanerophytes, chamaephytes, hemicryptophytes, cryptophytes and therophytes.
The world spectrum, or normal spectrum, was calculated by Raunkiaer (1934) based on a representative sample of all the vascular flora of the world.From that sample, the patterns recorded in different directions reflect environmental effects, especially related to climate, on plant adaptations observed in a community (Raunkiaer 1934).Hence, whereas the growth-form classification is used to characterize community structure (because some forms are dominant or more conspicuous), the lifeform spectrum describes environmental adaptations of the species that compose that community (Whittaker 1975;Raunkiaer 1934).Indirectly, this system provides information on local seasonality.According to Whittaker (1975), life-forms are not a structural attribute, but a floristic attribute: when the number of species is converted into percentage of life-forms, this percentage would represent the spectrum of life-forms in this community or geographic area.The fact that a given community is characterized by particular life-forms indicates species convergence toward certain environmental conditions; and this represents a functional attribute of the community.
In the present study, we assessed life-forms, growth-forms and floristic composition of three neighboring physiognomies that occur under different climates, soils and topographies.These community attributes were determined for an area located in the semi-arid region of northeastern Brazil, which comprises two geomorphological units: sedimentary basin and crystalline basement.
Based on these data, we tested the following predictions: i) the floras of the two geomorphological units are different, and constitute two discrete units; ii) the life-form spectrum varies according to altitude and soil type, probably as a consequence of differences in water availability, resulting mainly in the occurrence of phanerophytes in the sedimentary basin and of therophytes in the crystalline basement.
The study area is located in two geomorphological units: i) the crystalline basement complex, with flat to slightly undulating relief and Floristics and life-forms along a topographic gradient low altitude (c.400 m) and ii) the Meio Norte sedimentary basin, on its eastern margin, which forms an asymmetric cuesta, known as Ibiapaba Plateau (altitudes between 500 and 700 m).
The caatinga occurs in the crystalline basement complex, where the dominant classes of soils are: Solodic Planosol, Solodized Solonetz (natric Planosols) and Lithic soils (Lithic Neosols) at altitudes that vary from 300 to 500 m.
In the Meio Norte sedimentary basin, on Ibiapaba Plateau, the Latosol occurs on the eastern hogback and quartz sand (quartzarenic neosols) on the top and backside (Brasil 1972).The deciduous forest occurs on the eastern hogback of the plateau, on Latosol, at altitudes between 500 and 700 m.The carrasco is present on the backside of the plateau, on quartz sand, at altitudes of ca.700 m.We emphasize that the Ibiapaba Plateau is a 'cuesta', with higher asymmetry in its southern part, our study area, where there is no top, but an inverted V-shaped topography where the leeward on the backside exhibits a smooth declivity.
Climate data were not available, because there are no meteorological or pluviometric stations located on the cuesta, top and immediate backside sites on the southern part of the Ibiapaba Plateau, our study area.

Floristic inventory
The flora of Serra das Almas Natural Reserve was extensively sampled from 1999 to 2004, in several projects: reserve management plan; longterm ecological research programs -Site Caatinga/ CNPq/PELD; Instituto do Milênio do Semiárido-IMSEAR; Biodiversity inventories -Caatinga (PROBIO-MMA) and Edital Universal do CNPq / 476285/2003-8.In these studies, branches of angiosperms (five duplicates) in reproductive phase (flower buds, flowers and/or fruits) were collected on trails and inside the best-conserved fragments of each physiognomy.Vouchers were deposited in the Prisco Bezerra Herbarium (EAC), of Universidade Federal do Ceará.Botanical identification was carried out using analytical keys (Freire 1983;Barroso et al. 1978Barroso et al. , 1984Barroso et al. , 1986) ) and by comparison with the material present in the EAC Herbarium or, when necessary, by consulting specialists.The classification used was APG III (2009).Species names were updated considering the synonymy of Missouri Botanical Garden (Tropicos.org2009); names and/or abbreviations of species authors were written in accordance with Brummitt & Powell (1992).

Growth-and life-forms
Each species was classified into growth-forms following Whittaker (1975).
The classification of each species in life-forms was done based on the protection level of growing tips and on the reduction of the aerial part during the unfavorable season, following Raunkiaer (1934, see also Cain 1950;Mueller-Dombois & Ellenberg 1974): therophytes (Th), cryptophytes (Cr), hemicryptophytes (H), chamaephytes (Ch) and phanerophytes (Ph).Woody lianas and cacti were considered as phanerophytes and non-woody lianas were classified according to the level of reduction of their aerial part during the dry season (according to Raunkiaer 1934).

Data analysis
Floristic data were organized as a list with families, species, vernacular names, life and growthforms, physiognomy and collectors.We calculated species and family richness for the whole dataset and by physiognomy.To compare the richest families between physiognomies, we used histograms with the ten richest families in descending order.
Floristic overlap between physiognomies was analyzed by calculating the frequency of species and families in overlapping classes: occurrence in all physiognomies, in pairs of physiognomies (caatinga/carrasco, caatinga/deciduous forest, carrasco/deciduous forest), and restricted to each physiognomy (caatinga, carrasco or deciduous forest).Results are presented in histograms.To test for differences in the composition of life-forms among physiognomies, we calculated the life-form spectrum, which is the proportion of species of each life-form.We determined which lifeform characterized each physiognomy by comparing our results with the normal spectrum proposed by Raunkiaer (1934).This spectrum represents the world flora and was used here as null hypothesis.At first, we tested for differences between the obtained and the normal spectrum using a χ 2 test (Vieira 2004).When differences were significant, we calculated the relative contribution of each life-form's deviation to the computed χ 2 statistic.The life-form with higher contribution in each test was considered as characteristic of the physiognomy where it occurs.
To test for similarities with other Brazilian vegetation types (in terms of life-forms), we compiled studies with spectra determined for Brazilian physiognomies (Tab.1).We kept the names used by each author for the vegetation types of each study.To facilitate comparison, we used only the five main life-form classes of Raunkiaer (1934).Hence, epiphytes and woody lianas were included in the class phanerophytes, saprophytes in cryptophytes, and aerophytes in chamaephytes.We compared the life-form spectra found in Serra das Almas Natural Reserve with those from other studies with a detrended correspondence analysis -DCA (Jongman et al. 1995;Batalha & Martins 2002); results were expressed in ordination diagrams with scores of each study and of each life-form.

Results
We recorded 419 species/morphospecies from 72 families (Annex 1).Families (55) and species richness (250) were higher in the deciduous forest.Richness values of the carrasco (46 and 136) and caatinga (44 and 137) were similar to each other and lower than in the deciduous forest.
Fabaceae (86 species), Euphorbiaceae (38 species) and Convolvulaceae (22 species) were the richest plant families in Serra das Almas Natural Reserve.The richest families were different among physiognomies (Fig. 2).The exception was the family Fabaceae, which had the highest number of species in all three physiognomies (Fig. 2).However, the representativeness of subfamilies varied, with higher richness of Papilionoidae in the deciduous forest (25 species) and of Caesalpinioidae in the caatinga (12 species) and carrasco (15 species).
Family overlap was about one third among all physiognomies (Fig. 3).However, the carrasco and the deciduous forest shared the highest number of families, and had the highest (carrasco) and lowest (deciduous forest) number of exclusive families (Fig. 3).Species overlap was low, as only nine out of 419 species occurred in all physiognomies (Fig. 3).The carrasco and the deciduous forest had higher floristic affinity with each other, since they shared more species (15%) and both had low overlap with the caatinga (1.3 % overlap with carrasco and 4.2% with deciduous forest -Fig.3).Note: caatinga = xeric shrubland; carrasco = deciduous shrubland; cerrado sensu stricto = savanna; cerrado fechado = dense savanna; cerrado aberto = open savanna; campo cerrado = grassland with scatered shrubs; campo sujo = grassland with scatered shrubs; campo limpo = grassland; cerradão = tall woodland savanna; restinga = sandy coastal plains.
In the physiognomies on sedimentary relief, woody species (shrubs and trees) predominated, totaling 124 in the deciduous forest and 68 in the carrasco.In the caatinga, on the crystalline basement, the highest species richness (69) was represented by herbs.
In the comparisons of life-form spectra among physiognomies of Serra das Almas Natural Reserve with other Brazilian vegetation types, the two first axes of the DCA corresponded to over 60% of the total inertia: 49.68% on the first axis and 13.30 % on the second.In the ordination diagram three groups of life-form spectra stood out: i) spectra with scores next to the ones of phanerophytes, ii) of cryptophytes and iii) of chamaephytes and therophytes (Fig. 5).The life-form spectra of the carrasco and the deciduous forest in Serra das Almas Natural Reserve nearly overlapped in the ordination space, in group 2, which also comprises the restinga and cerrado spectra (Fig. 5).In this group, carrasco and deciduous forest exhibited scores close to those of restinga and different from those of cerrado, apparently because of the lower proportion of cryptophytes (Fig. 5).The caatinga composed a well-defined group, which comprised spectra of other caatinga studies, including vegetation on inselbergs.This group is associated with higher proportion of chamaephytes and therophytes (Fig. 5).

Discussion
In general, in the semi-arid region of northeastern Brazil, areas with higher annual average rainfall associated with higher altitudes exhibit higher species richness (Lima et al. 2009;Araújo et al. 2007;Ferraz et al. 1998;Gomes 1980).This pattern was also observed in the physiognomies of deciduous forest and carrasco, both located at higher altitudes than the caatinga in Serra das Almas Natural Reserve.Besides, deciduous vegetation on sedimentary areas, even with rainfall indexes similar to the caatinga area of the crystalline basement, have been pointed out in general as having higher species richness (Silva et al. 2003), though there are some exceptions (Rodal et al. 1998;Pereira et al. 2002).These exceptions show that being sedimentary alone does not result in higher species richness; other  Floristics and life-forms along a topographic gradient factors must also be considered, such as the position of the hogback, level of desiccation of the relief and physiochemical composition of the soil.The deciduous forest of Serra das Almas Natural Reserve is located on the windward side, between 500 m and 700 m, whereas the carrasco, though located at a higher altitude about 700 m, is located on the leeward side and on sandier soils, which results in a physiognomy of lower height, smaller and slender plants and lower richness than in the deciduous forest.
Concerning the herbaceous component of the Brazilian semi-arid flora, studies carried out in the inter-plateau depression of the crystalline complex indicate that the highest richness of the caatinga sensu stricto is in the herbaceous component (Sampaio 1995;Rodal et al. 2005;Costa et al. 2007;Mamede & Araújo 2008).Comparatively, studies carried out in sedimentary formations recorded low richness of herbaceous flora (Rodal et al. 1999;Figueirêdo et al. 2000).
In Serra das Almas Natural Reserve, the floristic richness of woody species increased at high altitudes in areas of deciduous forest and carrasco, whereas the richness of herbaceous species decreased.The increase in richness of trees and shrubs with altitude seems to be a general pattern for vegetation of arid and semi-arid regions.In the Brazilian semi-arid region, the increase in richness of herbaceous growth-forms and decrease in woody growth-forms is related to the increase in aridity (lower rainfall and higher temperature).In previous studies, the replacement of non-woody life-forms by woody life-forms and the increase in richness along humidity gradients have been observed in arid areas (Pavón et al. 2000), tropical savannas (Williams et al. 1996), forests and temperate grasslands (Kovács-Lang et al. 2000).
Considering woody and herbaceous flora together, the deciduous forest on the sedimentary basin exhibited higher richness than the caatinga located on the crystalline basement.Potentially, there must be higher humidity in the air and soil resulting from the elevation; there must be also soils with permanent water availability in deep layers (latosols and quartz sands), which possibly contribute to the higher floristic richness observed.
Comparing the carrasco and the deciduous forest located in the same sedimentary basin, the latter exhibited higher richness.In this case, humidity seems to be an important factor: the deciduous forest is located on the cuesta and the carrasco on the immediate backside.On the backside the air is probably drier and wind speed is higher, which causes more desiccation.Besides, soil seems to play a role too, since carrasco soils are sandier (Araújo & Martins 1999;Araújo et al. 1999).
Despite the high species richness found in the region of Ibiapaba Plateau, it is important to highlight the contribution of the non-woody component (herbs, subshrubs and herbaceous lianas) to the total species richness of each physiognomy.In the caatinga, on the crystalline basement, non-woody plants were responsible for most of the floristic richness, that is expected in arid and semi-arid climates, due to the predominance of therophytes in these environments.On the contrary, in the carrasco and in the deciduous forest, woody plants were responsible for the highest richness, since in more humid climates phanerophytes predominate.
Higher water availability favors the establishment of life-forms that do not need large reductions of the aerial shoot system during the unfavorable season (phanerophytes), which is a necessary strategy for the survival of most species in arid and semi-arid regions (see Raunkiaer 1934;van Rooyen et al. 1990;Kovács-Lang et al. 2000).In the case of Serra das Almas Natural Reserve, which is inserted in a semi-arid climatic domain, the increase in altitude may potentially favor high water availability on the windward side.Besides, soil must be taken into account, since there are two different geological units: lowlands of the crystalline basement and the Meio Norte sedimentary basin.
Herbaceous or sub-woody plants (herbs, subshrubs and herbaceous lianas) are the life-forms that exhibit the highest reduction of the aerial shoot system during the dry season (therophytes, cryptophytes, and hemicryptophytes; Raunkiaer 1934).The biological spectrum of the caatinga studied was characterized mainly by therophytes, a life-form characteristic of arid and semi-arid regions (Raunkiaer 1934;van Rooyen et al. 1990;Kovács-Lang et al. 2000).Indeed, among the three physiognomies studied, the caatinga occurs on shallow soils in the lowlands of the crystalline basement, where temperature is potentially higher and rainfall is potentially lower than in mountainrange areas, resulting in lower water availability.The physiognomies on the Ibiapaba plateau (carrasco and deciduous forest) must occur under lower water restrictions, since higher altitude contributes to the potential occurrence of higher rainfall and lower temperature, which favor phanerophytes, a life-form characteristic of sites with lower water restriction.
In addition to numeric differences in species richness, remarkable differences between the floristic complexes of each physiognomy were observed in the present study.The two main complexes (caatinga and carrasco + deciduous forest) are consistent with the soil types that occur in the area, resulting from the type of source rock.Although species overlap between deciduous forest and carrasco may be considered low (15%), differences are even larger when compared with caatinga, whose overlap is only 4%.Carrasco and deciduous forest are floristically more similar because both have a set of species that prefer sandy soil with low pH, whereas caatinga differs from that floristic group by the presence of species typical of soils originated from the crystalline basement of the inter-plateau depression.The crystalline and sedimentary floras of northeastern Brazil also differ at a broader scale, as it was observed in analyses of data matrices created from local inventories, carried out in several areas of the Brazilian semi-arid region (Araújo et al. 1998a, b;Lemos & Rodal 2002;Alcoforado-Filho et al. 2003;Araújo et al. 2005;Lima et al. 2009).
As Andrade- Lima (1981) emphasized, in the Brazilian semi-arid region, when the predominant variation is in climate, as observed in the two physiognomies studied in the Ibiapaba Plateau (the deciduous forest occurs on the windward side whereas the carrasco occurs on the leeward side), these do not form discrete units.They form a continuum represented by species overlap and by the same biological spectrum, as emphasized by Austin (2005).
When analyzing physiognomies on different geomorphological units, apart from the climate, the soil component may determine discrete units; communities that, according to Whittaker (1975), can be delimited by floristic composition and lifeforms, such is the case of the difference found between the caatinga and the complex deciduous forest + carrasco.
In the comparative analysis with the biological spectra from other Brazilian seasonal vegetation types, the discrimination of the caatinga by higher proportion of therophytes and chamaephytes shows that this vegetation is composed of species whose life-forms represent better the semi-arid climatic pattern, since the predominance of these life-forms is characteristic of vegetations of arid and semi-arid environments (Raunkiaer 1934;Cain 1950).The biological spectrum is similar to the spectrum of arid and semiarid climate zones of the world.
In summary, the two geomorphological units present in the study area have two distinct floristic complexes, characterized by the predominance of therophytes on the crystalline basement and of phanerophytes on the sedimentary basin.These results show that when implementing reserves in Brazilian semi-arid areas, abiotic local factors, such as soils and relief, must be taken into account, because these factors seem to reflect regional floristic variation.The environmental heterogeneity may result not only in high species diversity, but also in high functional diversity in the Brazilian semi-arid domain, which, in the present study, may be observed in differences in life-form spectra among the three physiognomies analyzed.Annex 1 -List of families and species found, with respective growth-forms and life-forms, in three phytophysiognomies, caatinga (CA), carrasco (CR) and deciduous forest (DF), of the Natural Reserve Serra das Almas, Ceará State, deposited in the EAC Herbarium of the Universidade Federal do Ceará.x = presence of species in the phytophysionogmy.Growth-form (FC) = tree (tre), shrub (shr), sub-shrub (sub), liana (lia), herb (her).Life-form (FV) = phanerophyte (Ph), chamaephyte (Ch), hemicryptophyte (H), therophyte (Th), cryptophyte (Cr).

Floristics
and life-forms along a topographic gradient