Phytogeographical Patterns of Dry Forests Sensu Stricto in Northern Minas Gerais State, Brazil Phytogeographical Patterns of Dry Forests Sensu Stricto in Northern Minas Gerais State, Brazil

The Deciduous Complex that occurs in northern Minas Gerais State, Brazil, raises questions about the fl oristic affi nities of these formations in relation to neighboring phytogeographical domains. Little is known about the identity of the seasonal forest formations that comprise this complex, or about its relationships to abiotic components, such as soils, topography and climate. This study aimed to recognize the patterns of fl oristic similarity of all studied fragments of dry forest of northern Minas Gerais with soil and climate attributes, based on the available database. Cluster analysis indicated the existence of two fl oristic groups that had clear associations with either the Koppen's BSh (semi-arid) or Aw (seasonal tropical) climates. Likewise, the subdivisions of these groups showed clear associations with the dominant soil classes in the region. The Red-Yellow Latosol is the dominant soil classes in the BSh climatic domain, seconded by alluvial areas associated with Fluvic Neosols. The Aw domain comprised a much varied set of soils: Nitosols, Argisols, Cambisols and Litholic Neosols, most derived from the Bambuí limestone/slate formation. The ecotonal nature of northern Minas Gerais State provides a complex interaction between the fl ora of neighboring phytogeographical domains. This, allied to pedogeomorphological factors, allowed a better understanding of the effects of late Quaternary climate changes for the Deciduous Complex evolution. We conclude that the Latosols under present-day semi-arid climates (BSh) are relicts of former wetter climates, during which humid forest (semideciduous) expansion took place. Later, these semideciduous forests were subjected to a much drier climate, when selection for deciduousness led to the present-days Deciduous Complex scenario.


INTRODUCTION
The seasonally dry tropical forests, or seasonal deciduous forests, were classifi ed by Veloso et al. (1991) as a vegetation type infl uenced by a markedly seasonal climate, with a rainy summer followed by a long dry period; there, most plants are totally deciduous in the dry season.Although the defi nition of dry forest by some authors includes shrub formations (bushland, scrub, and thicket), Caatinga savannas, and the semideciduous forests of the 623-634 DANIEL M. ARRUDA, WALNIR G. FERREIRA-JÚNIOR, REINALDO DUQUE-BRASIL and CARLOS E.R. SCHAEFER Atlantic domain (e.g.Pennington et al. 2006), in the present work we chose to restrict this designation only to deciduous forest formations (deciduousness above 50%, sensu Veloso et al. 1991), which will be referred to in the text as dry forests sensu stricto (DF).Similar exclusion criteria were adopted by Gentry (1995) to analyze Neotropical DF.
In Brazil, DF are located within the Pleistocene Arch (Prado and Gibbs 1993) -an extensive range of natural forest areas extending from the northeastern Brazil (in the Caatinga domain) to the Brazilian southwest, and the dry lowlands of Bolivia and Paraguai (" Chaco").The fl oristic relationships of different DF with these two neighboring domains were described by Oliveira-Filho et al. (2006) and Queiroz (2006).
When compared to moist or wet forests, DF have lower richness and primary productivity, which are directly related to reduced rainfall (Gentry 1995) and the seasonal nature of the environment (Murphy and Lugo 1986).Thus, the seasonality of the DF constraints and determines the biological activity, growth, reproduction, and species distribution (Murphy and Lugo 1986).Their seasonal nature is also an important factor in defi ning the macrogradient from humid-ombrophilous forests to seasonaldeciduous forests (Oliveira-Filho and Fontes 2000).
On a global scale, Murphy and Lugo (1986) suggested that DF would occur in areas with precipitation rates of 600-1,800 mm/year distributed along 4-9 months, with average annual temperatures ranging from 19 to 27°C.On a regional scale of the present study, DF occur where annual precipitation ranges between 700-1,200 mm, concentrated in 5-6 months, with temperatures varying between 14-19°C in the Espinhaço Mountain Range and between 26-31°C in the depression of the São Francisco and Verde Grande River valleys in northern Minas Gerais State (Antunes 1994).This state region is marked by a transition from a tropical rainy climate (covering most of the area) to a semi-arid zone to the north (Antunes 1994).Hence it represents a broad ecotonal zone.
Consistent with the transitional climate, the northern region of Minas Gerais is marked by the transition between three large phytogeographical domains: Caatinga (to the north); Cerrado (to the west); and Atlantic Forest (to the east).Due to the contact between these domains, this region is classifi ed as a "tension zone" (Ab'Sáber 2003) or "ecotone", with mixed plant formations that are diffi cult to characterize and have complex fl oristic compositions distributed among various phytophysiognomies that change according to local topography and local edaphic conditions (Brandão 2000).
The identity of the DF formations and their associations with abiotic components (climate, topography and lithology) remain practically unknown and have not yet been investigated in any integrated or systematic manner.In light of this situation, and recognizing the complex distribution of DF in northern the Minas Gerais State, the present work examined the patterns of fl oristic similarity between several DF fragments and their association with edaphic and climatic factors.

MATERIALS AND METHODS
A database was produced by reviewing the scientifi c literature for fl oristic and/or phytosocio logical surveys in areas of dry forests (DF) sensu stricto in northern Minas Gerais State.This literature review included lists of arboreal species (using the inclusion criteria of plants with circumference at breast height equal to or greater than 15 cm) from scientifi c surveys undertaken in the region as well as lists produced by the Forest Inventory of Minas Gerais (Mello et al. 2008) (Table I).Surveys undertaken in gallery forests were not included to avoid undesirable overlaps with the semideciduous fl ora.
The coordinates of each locality were overlaid on a map of soil classes produced during fi eld expeditions and processed at the Geoprocessing Laboratory at the Universidade Federal de Viçosa (Fig. 1).
The Species List of Brazil's Flora (Forzza et al. 2010) database was used to standardize species PHYTOGEOGRAPHY OF TROPICAL DRY FOREST nomenclature.Floristic comparison analyses were performed at the species level; and to ensure greater reliability of the results (and lessen any errors related to possible erroneous identifi cations) the same analyses were repeated at the genus level (Rodal et al. 2008).Matrixes were constructed using data concerning the presence of 396 species and 193 genera, representing 65 botanical families in 26 areas of DF in northern Minas Gerais, to aid identifying similar fl oristic groups.The matrixes were used in TWINSPAN divisive clustering analyses (Hill et al. 1975) and agglomerating Cluster Analyses (Sneath and Sokal 1973), both employing the Jaccard similarity coeffi cient.These analyses were processed by the PC-ORD program for Windows version 5.1 (McCune and Mefford 2006).
The hierarchical groupings formed together with their preferential species, as indicated by the TWINSPAN analyses, were also analyzed in relation to the dominant soil classes and to the climate types described by Antunes (1994) for the region (the latter based on the classifi cation system of Köppen) (Fig. 2).

RESULTS
Divisive clustering analyses at the species level fi rst showed a division into two large dry forest (DF) groups (eigenvalue 0.49) (Fig. 3).These two groups have most areas distributed in different climatic domains.Likewise, the subgroups formed had strong associations with the predominant soil classes in their respective areas.
Some species were shared between different areas, although specifi c sets of species proposed by the TWINSPAN analysis were observed to be associated with certain environments (Table II).In addition, some species stood out due to their frequent occurrence in these groups, and even though they might occasionally occur in another group, they were strong indicators of the associations in question.Similarly, commonly occurring species with no preference for either groups were considered typical DF species.Already, exclusive species of specifi c groups are indicated in bold type in Table II.
The fi rst main group was formed by the localities in the seasonal tropical climate domain (Aw), where covered large areas on many different soil classes; the second main group was formed by localities strongly associated with the semi-arid climate domain (BSh), developed on Red-Yellow Latosols (according to the Brazilian System of Soil Classifi cation) or Fluvic Neosols (Alluvial soils).
The Aw group was divided into fi ve subgroups.The fi rst subgroup (corresponding to cluster 1) was found in areas of Haplic Nitosols and Latosols (Montes Claros [II] and Januária [I] respectively) and differed considerably from all of the others (eigenvalue 0.44).The second subgroup (corresponding to cluster 2) represented by areas located in the southernmost region (including Montes Claros [I] and Juramento) on Haplic Nitosols and Argisols (Podzolic soil) respectively.This latter group has a great fl oristic affi nity with the third subgroup (corresponding to clusters 3 and 4) representing areas of dry forest located in the northernmost part of the state (in the municipalities of Juvenília [I, II, III, IV and V] and Montalvânia) on varying soil classes,    The BSh group was divided into two subgroups.The fi rst, represented by clusters 7, 8, 9 and 10, was mainly formed by areas of Red-Yellow Latosols (including Matias Cardoso [I, II, III, IV], Pai Pedro and Januária [II]); however, areas of Haplic Cambisols (Jaíba [III] and Manga [IV]) were also included, although all in soil associations with latosols.The second subgroup comprised forests growing on Fluvic Neosols (Manga [II and III] and Jaíba [I]) and corresponded to cluster 11 in Figure 3.This group comprise very heterogeneous soil associations, including Fluvic Neosols, Planosols, Cambisols and Latosol, all associated with fl oodplain landscapes (várzeas seasonally fl ooded forests) and terraces along the São Francisco and Verde Grande rivers.
Similarity analysis at the genus level (Fig. 4) confi rmed the two large groups identifi ed at the species level analysis, demonstrating the reliability of these groups, even though slightly different methods were used.This analysis had a high cophenetic correlation index (0.91), indicating low distortions between the real data and the dendrogram.

DISCUSSION
The fact that some areas did not correlate with expected climatic domains (e.g.Januária II, Jaiba III and Pai Pedro in the BSh domain, and Manga I and Jaiba II in the Aw domain) can be  related to an edaphic similarity between areas under contrasting climates, or to the ecotonal nature of these domains, otherwise artifi cially expressed by rainfall lines.Hence, abrupt limits between domains area not realistic.Besides, it is possible that the BSh domain extend further into the northern Minas Gerais, covering a much larger area of the sertaneja depression, as suggested by recent climatic data of rainfall and air temperature data (INMET 2011).
The 396 species considered in the present analysis indicated that the northern region of Minas Gerais State is an important ecotone possessing various vegetation forms.A large proportion of the species considered to be typical of dry forest (DF) also occur in other Brazilian phytogeographical domains, such as Caatinga (e.g.Commiphora leptophloeos, Piptadenia viridifl ora, Cereus jamacaru and Spondias tuberosa) and Cerrado (e.g.Platypodium elegans, Sterculia striata, Machaerium acutifolium and Peltophorum dubium).They can also occur in the humid Atlantic forests (e.g.Tabebuia roseo-alba, Enterolobium contortisiliquum, Machaerium villosum and Eugenia fl orida) (Oliveira-Filho 2006, Forzza et al. 2010).
The presence of typical Caatinga species has led to the inclusion of DF within this domain.Consistently, Andrade-Lima (1981) described the forests associated with the calcareous soils as a southeastern transitional zone with the Caatinga biome, due to high deciduity and the presence of "bottle-shaped trees" such as Cavanillesia umbellata e Ceiba spp., besides many cacti species.Also, Ratter et al. (1978), in a study of Forests growing on mesotrophic soils, have considered the dry forests of Januária as a Forested Caatinga, since it presents species not found in other mesotrophic forests of Central Brazil.In this context, according with Andrade-Lima's Caatinga classifi cation schemes, the DF of the present study corresponds to a vegetation-type 1, called "Tall Caatinga Forest".
In addition to their ample distribution in Brazil, most of the species mentioned in the present work also follow the distributions proposed by Some of the species considered typical of DF (e.g.Anadenanthera colubrina, Enterolobium contortisiliquum, Myracrodruon urundeuva, Combretum leprosum and Sterculia striata) or indicators of their groups (e.g.Tabebuia impetiginosa and Maclura tinctoria for the groups BSh and Aw respectively) were also indicated by Prado and Gibbs (1993) and Oliveira-Filho and Ratter (1995) as indicators of mesotrophic soils.As these species occur widely in the northern part of the state, it indicates that DF frequently grow on soils with moderate to high fertility.Similarly, Ratter et al. (1978) reported typical calcicolous species in Central Brazil, correlating the deciduousness with soil moisture regime.Queiroz (2006), in a study of the fl oristic similarity of the Leguminosae of the Caatinga, indicated that DF could be found both on shallow soils over crystalline basement rocks or on very deep soils in the inland depression zone (e.g.Acacia langsdorffi i, Amburana cearensis, Albizia polycephala, Bauhinia cheilantha, Senna spectabilis, Plathymenia reticulata, among others).The species cited by this author are similar to the species composing the BSh group, with very close relationships to the subgroup of DF growing on Red-Yellow Latosols (which includes the central depression zone).Queiroz (2006) also noted that the tallest forests are associated with richer soils derived from limestone formations, with common occurrences of the species Apuleia leiocarpa, Goniorrhachis marginata, Copaifera langsdorffi i, Enterolobium contortisiliquum, Pterogyne nitens, and Plathymenia reticulata, among others.In the present study, some of these species demonstrated a random patterns of occurrence, while others were restricted to the large Aw group associated with shallow limestone soils associated with the Bambuí Group.
The Aw group, more specifi cally the subgroup of the DF growing on Haplic Nitosols and Argisols, was separated from the other groups by a marked infl uence of typical Cerrado fl ora (e.g.Leptolobium dasycarpum, Curatella americana, Cybistax antisyphilitica, Eriotheca pubescens, Eugenia dysenterica, Dilodendron bipinnatum, Machaerium opacum, and Qualea grandifl ora, among others).This fact demonstrates that the southern portion of the region comprises localities where the Cerrado domain greatly infl uences the DF fl oristic composition, explained by environmental similarities (both climatic and edaphic) between the two areas.
According to Oliveira-Filho et al. (2006), DF is part of the Atlantic complex forest gradient that begins with the ombrophilous formations of the coastal lowlands and becomes progressively seasonal towards the west, comprising semideciduous seasonal forests that transition to completely deciduous forests in the continental interior.This gradient is driven by the reducing water availability, increasingly seasonality.According to Andrade-Lima (1981), this continental gradient ends in the northeastern Brazil with scrubby, torny Caatinga formations.
In a continental scale perspective, high similarities between areas so widely separated, with endemisms and strong dissimilarity with neighbouring formations, all points to a new phytogeographic unit (Prado 2000).In the same scale, Oliveira-Filho et al. (2006) suggests observed that the main infl uence for the grouping with fl oristic similarity in DF is the geographic DANIEL M. ARRUDA, WALNIR G. FERREIRA-JÚNIOR, REINALDO DUQUE-BRASIL and CARLOS E.R. SCHAEFER proximity; but when focusing on a given subregion, the predominant infl uence is then shifted to soil climate.A review of the fl ora of the Caatinga published by Sampaio (1995) described a very similar pattern for that vegetation type, noting that fl oristic similarities tend to be greater on different substrates in the same locality, then on similar substrates from distant localities.Consistently with our study, however, climate determines the grouping on a regional scale, but edaphic factors have a strong role at local scale, allowing to establish subgroups with separate fl oristic affi nities.
The Aw group is formed by forest fragments associated with the tropical rainy climatic domain and comprises environments with higher annual rainfall and smaller seasonal and temperature fl uctuations, contrasting with the group formed of fragments associated with the semi-arid climatic domain (group BSh).These Aw group fragments occur on shallower and often richer soils associated with strong environmental heterogeneity; topography is slightly more varied with a wide spectrum of landscapes of limestone's and siltstone/slate's outcrops that give way to a wide diversity of soils.The Cerrado domain fl ourishes under this same climatic regime, but mostly on deeper and poorer soils.
The BSh group comprises localities with greater average annual temperatures and with highly seasonal rainfall, below 750 mm/year (Antunes 1994).These forest fragments are present in the eastern part of the São Francisco River basin but do not cover extensive areas.They are associated with Alluvial (Fluvic Neosols), Planosols and Cambisols, which are eutrophic due the deposition of sediments from the São Francisco and Verde Grande Rivers.In strong pedological contrast, dry forest fragments cover extensive areas in the central depression and occupy old, deep, and well drained Red-Yellow Latosols.Virtually all Latosols are closely associated with the micro topography "Murundus", large termite mounds reaching up to 3 meters in height, and regularly distributed across the landscape.
The predominance and extensive occurrence of Red-Yellow Latosol with "Murundus" mounds in the northern part of Minas Gerais State indicates a previous wet phase of the Late Quaternary.At that time, the lowlands, valleys and depressions of the Verde Grande and São Francisco Rivers had climates that were much wetter than today, and probably occupied by extensive semideciduous forest formations.This period resulted in strong leaching and the development of deep Latosols.Virtually all Latosols associated with "Murundus" (now largely inactive) are also relics of this past humid phase.
It was not possible to evaluate the infl uence of historical uses of the DF fragments on their observed patterns of fl oristic similarity because very few sources in the database presented any such information.Hence, it is possible that some of the observed patterns of fl oristic similarity result from successional stages, of these DF.
It is important to state that most DF in this region has long been converted into agriculture or pasture, and only scattered fragments of secondary forests remain, most associated with limestone outcrops.The original tall forest, 25-30 m up to high, as described by former studies (Ratter et al. 1978, Andrade-Lima 1981and Kuhlmann et al. 1994), are seldom found (e.g.some fragments of Juvenília (Santos et al. 2007), Capitão Enéas (Arruda et al. 2011) and Januária (D.M. Arruda, unpublished data).

CONCLUSIONS
The different climatic conditions (semi-arid and semi-humid) found in northern Minas Gerais favored the establishment of two distinct groups of dry forests sensu stricto (DF) that could be further subdivided in relation to their different soil classes.
The peculiarities and relations of DF, at a regional scale, besides its fl oristic traits, long term evolution under contrasting climates, presence PHYTOGEOGRAPHY OF TROPICAL DRY FOREST of endemics and dissimilarities with other neighbouring domains, all corroborate its identity as a separate phytogeographic unit.
The Latosols (deep-weathered soils) of the semiarid domain indicate a more humid paleoclimate during their formation, with corresponding semideciduous vegetation formations.Later, when semiarid climates established in the São Francisco/Verde Grande River Depression, these forest formations became progressively more deciduous, leading to the present-day distribution pattern.

ACKNOWLEDGMENTS
The authors thank Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Secretaria de Estado de Ciência, Tecnologia e Ensino Superior (SECTES-MG) for fi nancing the project and for granting the scholarship for the fi rst author.The authors also thank constructive comments of the two anonymous referees.

Figure 2 -
Figure 2 -Approximate spatial distribution of climatic types identifi ed for the northern region of Minas Gerais, according to the Köppen climate classifi cation (redrawn from Antunes 1994).

Figure 3 -
Figure 3 -Dendrogram of the relationships between 26 areas of dry forest sensu stricto (DF) in northern Minas Gerais as produced by the divisive clustering analyses of 396 species.The numbers in parentheses correspond to the clusters cited in the text.

Figure 4 -
Figure 4 -Dendrogram of similarities between 26 areas of dry forest sensu stricto (DF) in northern Minas Gerais State, as formed by the agglomerative grouping analysis of 193 genera.The areas are identifi ed by the codes listed in the Figure 1.BSh and Aw correspond to semi-arid and seasonal tropical climate domain, respectively.