Journal of Systematics and Evolution
47 (5): 477–496 (2009)
doi: 10.1111/j.1759-6831.2009.00046.x
Review of plant biogeographic studies in Brazil
1
1
2
Pedro FIASCHI∗
2
José R. PIRANI∗∗
(Department of Biology, Virginia Commonwealth University, Richmond, VA 23284-2012, USA)
(Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, 05508-900, São Paulo, SP, Brazil)
Abstract Molecular phylogenetic studies have become a major area of interest in plant systematics, and their
impacts on historical biogeographic hypotheses are not to be disregarded. In Brazil, most historical biogeographic
studies have relied on animal phylogenies, whereas plant biogeographic studies have largely lacked a phylogenetic
component, having a limited utility for historical biogeography. That country, however, is of great importance for most
biogeographic studies of lowland tropical South America, and it includes areas from a number of biogeographic
regions of the continent. Important biogeographic reports have been published as part of phylogenetic studies,
taxonomic monographs, and regional accounts for small areas or phytogeographic domains, but the available
information is subsequently scattered and sometimes hard to find. In this paper we review some relevant angiosperm
biogeographic studies in Brazil. Initially we briefly discuss the importance of other continents as source areas for the
South American flora. Then we present a subdivision of Brazil into phytogeographic domains, and we cite studies
that have explored the detection of biogeographic units (areas of endemism) and how they are historically related
among those domains. Examples of plant taxa that could be used to test some biogeographic hypotheses are provided
throughout, as well as taxa that exemplify several patterns of endemism and disjunction in the Brazilian angiosperm
flora.
Key words angiosperms, biogeography, Brazil, disjunction, distribution patterns, endemism.
Brazil is the fifth largest country in the world, with
more than 8.5 million km2 , and one of the most diverse
in vascular plant species, with an estimated 55,000–
60,000 species (Prance, 1994; Giulietti et al., 2005).
The territory occupied by Brazil encompasses most of
the world’s remaining areas of tropical rainforests (primarily in the Amazon), as well as considerable areas
of tropical savannas (the central Brazilian Cerrado) and
seasonally dry tropical forests (SDTFs; mostly in the
Caatinga). The country is also one of the few that includes two hotspots for the conservation of biodiversity
sensu Myers et al. (2000), the Atlantic Forest and the
Cerrado.
Despite its unquestionable importance for the study
of South American biogeography in general, there is a
serious lack of biogeographic synthesis about Brazilian
plants. Most studies so far have emphasized the detection of patterns of geographic distribution by mapping
occurrence data, relegating the explanations on how
these patterns were achieved to a somewhat speculative
level. Because the vast majority of the available studies lack a phylogenetic perspective (e.g., Prance, 1979,
1988; Giulietti & Pirani, 1988; Acevedo-Rodrı́guez,
1990; Alves et al., 2003; Gonçalves, 2004; Cavalcanti,
2007; Fiaschi & Pirani, 2008), the information generated has been regarded as having little relevance for
historical biogeography, as the detection of areas of geographic distribution correspond only to the very first
step of any historical biogeographic analysis (Crisci
et al., 2003; Santos & Amorim, 2007).
In this paper we aim to provide an overview of
the main plant biogeographic studies in Brazil. First,
we present some general information on the origin of
tropical South American flora, based mostly on recent
paleogeographic and phylogenetic studies. Second, we
briefly describe the main Brazilian phytogeographic
domains and discuss the relevant biogeographic studies from publications on several groups of organisms
(mostly animals) in order to provide a framework for
comparison with the few available plant studies. Finally, we also provide examples of angiosperm genera
that could be used to test some biogeographic hypotheses in Brazil, and of plant distribution and disjunction
patterns in and among the Brazilian phytogeographic
domains.
1
Received: 1 March 2009 Accepted: 8 June 2009
∗
Author for correspondence. E-mail: <[email protected]>;
Tel.: 1-804- 8280773; Fax: 1-804-8281562.
∗∗
E-mail: <[email protected]>.
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2009 Institute of Botany, Chinese Academy of Sciences
Origin of tropical South American flora
The break-up of West Gondwana and the separation of South America from Africa ca. 100 mya resulted
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in a long period of isolation for South America, until the
closure of the Isthmus of Panama ca. 3 mya (Burnham
& Graham, 1999; McLoughlin, 2001). This long period
of isolation as an island continent (approximately 97
my) led some authors to suggest that the South American flora has developed in situ, with little contribution
of immigrant taxa (Raven & Axelrod, 1974; Gentry,
1982; Burnham & Graham, 1999). However, the idea of
a “splendid isolation” leading to a unique South American biota does not seem to fit the many well-known
examples of disjunct taxa shared with Africa, Oceania,
Asia and North America. Thus, in addition to vicariance
explanations derived from the split of formerly united
continents, some of these general patterns of disjunction must invoke hypothesized land connections through
presently submerged areas (Morley, 2003) and climatically unfavorable areas (Sanmartı́n & Ronquist, 2004),
or episodic events of long-distance dispersal (Givnish &
Renner, 2004; Pennington & Dick, 2004), as molecular
dating of plant phylogenies have shown that the arrival
of several lineages in South America are posterior to its
separation from Africa (e.g., Sytsma et al., 2004; Trénel
et al., 2007), or prior to the closure of the Panama Isthmus (e.g., Erkens et al., 2007; Cuenca et al., 2008). In
the following paragraphs we present a brief overview of
past connections and dispersal routes that may have accounted for the presence of some angiosperm lineages
in tropical South America, especially in Brazil.
The evident floristic connection between the
African and South American floras (Raven & Axelrod,
1974; Gentry, 1982, 1993) can hardly be explained by
the break-up of West Gondwana alone, because the initial separation of these two continents took place much
earlier than the appearance of many of their plant lineages (Givnish & Renner, 2004; Renner, 2004; Sytsma
et al., 2004). After the initial development of the South
Atlantic Ocean ca. 135 mya (McLoughlin, 2001), northern South America and Africa remained connected until 110–95 mya (Sanmartı́n & Ronquist, 2004), and
some island chains may have permitted dispersal routes
for floristic exchanges between the two continents during the Late Cretaceous/Early Tertiary boundary (∼65
mya) (Hallam, 1994; Morley, 2003; Pennington & Dick,
2004). Recent phylogenetic and paleontological evidence suggests these routes may have been effective
for Arecaceae (Trénel et al., 2007) and Proteaceae
(Morley, 2003; Barker et al., 2007). Long-distance dispersals also seem to have contributed significantly to
floristic connections between Africa and South America (Renner, 2004). Phylogenetic studies of Neotropical plant taxa with just a few recent colonizers in
Africa, such as Bromeliaceae, Cactaceae, Humiriaceae,
Loasaceae, Mayacaceae, Rapateaceae, and Vochysi-
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aceae are supportive of this view (Givnish et al., 2000;
Renner, 2004; Sytsma et al., 2004).
The suggestion that most of lowland tropical South
American flora was derived from a West Gondwanan
stock (Raven & Axelrod, 1974; Gentry, 1982) does
not seem to be supported by phylogenetic evidence
(Pennington & Dick, 2004). Instead, some important
lowland Amazonian angiosperm families, such as Annonaceae, Burseraceae, Lauraceae, Melastomataceae,
Meliaceae and Moraceae seem to have had most of their
Neotropical species derived from northern hemisphere
ancestors through Laurasian migrations (Chanderbali
et al., 2001; Renner et al., 2001; Pennington & Dick,
2004; Richardson et al., 2004; Weeks et al., 2005;
Zerega et al., 2005; Muellner et al., 2006). This
Laurasian route is supported by the widespread presence
of tropical forests in the northern hemisphere during
the Paleocene and Eocene (“boreotropical forests;” see
Wolfe, 1975; Tiffney, 1985a, b), and the possible floristic
exchange between North American and South American landmasses throughout parts of the Tertiary before
the closure of the Isthmus of Panama (Iturralde-Vinent
& MacPhee, 1999; Morley, 2003). Among the possible
island chains that may have permitted such exchange
are the Middle to Late Eocene Proto-Greater Antilles
(Morley, 2003), the Eocene-Oligocene GAARlandia (Fritsch, 2001; Morley, 2003), and the Late
Miocene/Pliocene formation of the Isthmus of Panama,
which provided a land corridor for the significant
faunal exchange known as the “Great American Interchange” (Burnham & Graham, 1999; IturraldeVinent & MacPhee, 1999). Following the predictions of
Lavin and Luckow (1993), additional evidence for the
boreotropical origin of tropical South American taxa has
been obtained for Magnoliaceae (Azuma et al., 2001),
Malpighiaceae (Davis et al., 2002), Sapotaceae (Smedmark & Anderberg, 2007) and Styracaceae (Fritsch,
2001). Other angiosperm families listed by Gentry
(1982) as having a Gondwanan origin, such as Anacardiaceae, Araliaceae, Gesneriaceae, Illiciaceae and
Menispermaceae may prove to constitute additional examples of groups that arrived in South America by this
Laurasian route.
As discussed above, evidence for vicariant patterns
between tropical African/South American elements are
restricted to a few lineages whose estimated time of
split agrees with the separation of these continents,
such as calamoid palms (Pennington & Dick, 2004).
Additional examples of disjunction patterns invoking
Gondwanan vicariance seem to apply to subtropical and
montane taxa shared between southern South America
and areas belonging to the Southern Temperate Gondwana Province, such as Australia, New Zealand and
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FIASCHI & PIRANI: Plant biogeography in Brazil
New Caledonia (Sanmartı́n & Ronquist, 2004). Land
connections through west Antarctic terrains permitted
some floristic exchange between Australia and South
America until the late Eocene (∼35 mya) or even the
early Oligocene (30–28 mya), when South America finally separated from Antarctica (McLoughlin, 2001;
Sanmartı́n & Ronquist, 2004). The prevailing impact
of this connection was to provide a stock of subtropical
elements to South America, for example, Araucaria (authors of generic names used in this study can be found in
Mabberley (2008)), Griselinia, Gunnera, Nothofagus,
Podocarpus, Cunoniaceae, some Proteaceae, and Winteraceae. However, it also made it possible for some taxa
to diversify along tropical mountain ranges, such as the
Andes and the eastern Brazilian Serra do Mar and Serra
da Mantiquera [e.g., Arecaceae-Ceroxyloideae (Trénel
et al., 2007), Alstroemeria (Hofreiter, 2007), Escallonia, Weinmannia]. The view that floristic connections
among areas in higher southern latitudes are due to
the break-up of Gondwana has also been challenged,
and it seems that long-distance dispersals were important in shaping current plant distributions in this region
(Sanmartı́n & Ronquist, 2004; Trénel et al., 2007).
Upon arrival in South America by any of the abovementioned routes (old vicariant events or more recent
dispersals, whether long-distance or by land bridges),
diversification of tropical plant lineages seem to have
been strongly influenced by the following three main
factors (Burnham & Graham, 1999): (i) the uplift of the
Andes and associated changes in drainage patterns during the Miocene, resulting in the separation of cis- and
trans-Andean biotas (Chanderbali et al., 2001; Trénel
et al., 2007; Pennington & Dick, in press) and the creation of suitable montane habitats (Ritz et al., 2007;
Smith et al., 2008); (ii) the closure of the Isthmus of
Panama (3.5–3 mya), which resulted in considerable
floristic exchanges between northern and southern landmasses, and accounted especially for the present composition of upland forests; and (iii) Quaternary climatic
fluctuations, which might have been important in the
recent diversification of large lowland tropical genera,
such as Inga (Richardson et al., 2001) and Guatteria
(Erkens et al., 2007). Other factors that may have driven
speciation in South American rainforest taxa include
ecological shifts associated with soil heterogeneity (Fine
et al., 2005), altitudinal range (Givnish et al., 2000),
and invasions of novel geographic areas and biomes
(Pennington et al., 2004; Gonçalves et al., 2007; SaslisLagoudakis et al., 2008). A good overview on the diversification of tropical South American rainforest plants,
focusing on Amazonian taxa, is presented by Pennington and Dick (in press). Additional examples of plant
diversification in Brazil are presented in the sections
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2009 Institute of Botany, Chinese Academy of Sciences
479
dedicated to the main phytogeographic domains of the
country.
2 Overview of main Brazilian phytogeographic domains
Because many Brazilian plant groups have a distribution mostly restricted to one of the main phytogeographic domains represented in the country (e.g.,
Perret et al., 2006) and several studies address domainbased, rather than taxon-based biogeographic hypotheses (e.g., Oliveira-Filho & Fontes, 2000; Queiroz, 2006;
Ratter et al., 2006; Santos et al., 2007), we first present
general information on the biogeographic divisions of
Brazil and then provide separate discussions for each of
these domains, including the relevant taxon-based studies. Geographic distribution patterns of Brazilian plants
are also illustrated, aiming to account for observed patterns of disjunction.
The first attempt to classify Brazilian vegetation was made by Martius (1824), who divided the
country into five floristic domains, each named after a Greek nymph. His system included the Amazon
(Nayades), the cerrados of central Brazil (Oreades),
the Atlantic rainforests (Dryades), the Araucaria forests
and southern grasslands (Napeias), and the northeastern Caatinga (Hamadryades). Several authors have suggested changes to this system, but the basic features remain unaltered (Sampaio, 1940; Fernandes & Bezerra,
1990; Veloso et al., 1991). Regions and provinces recognized in all biogeographic systems of South America do not show any sharp difference from this general
framework of domains (e.g., Cabrera & Willink, 1973;
Morrone, 2001).
The most widely accepted classification system
for Brazilian vegetation is that of Veloso et al. (1991),
who separated the country into four biomes (see comment on biomes below): the Amazon Forest, the Atlantic Forest, the Savanna ( = Cerrado), and the Steppe
( = Caatinga + Campos sulinos). Joly et al. (1999)
provide a good introduction to the phytogeographic divisions of Brazil, and Daly and Mitchell (2000) give
a South American overview. We divided the country into five main phytogeographic domains: Amazon,
Cerrado, Atlantic Forest (including the Araucaria
forests), Caatinga, and Campos sulinos (Fig. 1). Here,
instead of adopting a single Steppe biome for the
northeastern Caatinga and the southern Campos sulinos
(Veloso et al., 1991), we kept them separate due to their
strong floristic and climatic differences. It is worth mentioning that the use of “biome” as a synonym of “phytogeographic domain” in Brazilian phytogeographic
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Fig. 1.
Map of Brazil, showing the phytogeographic domains discussed in the text. The inset box shows the position of Brazil in South America.
published works is incorrect (Coutinho, 2006). “Biome”
refers to an area with physiognomic homogeneity regardless of the floristic composition, and the term “phytogeographic domain” implies physiognomic heterogeneity and takes the floristic composition as a very
important component.
2.1 Amazon
The Amazon forests extend over an area of approximately 6 million km2 in northern South America (Daly
& Mitchell, 2000), and account for most of the world’s
remaining rainforests. The limits of these forests have
been variously defined (Daly & Prance, 1989), but they
are somewhat congruent with the Amazon basin. The
basin, however, extends north and eastward beyond the
forested area, and the forests become replaced by savannas in most of eastern Bolivia and central-northern
Brazil (Goulding et al., 2003). Amazon rainforests are
among the most diverse in the world (Gentry, 1988a;
Valencia et al., 1994). Recent estimates of Amazonian
plant diversity range from 25,000 angiosperm species
in the entire basin (Goulding et al., 2003) to 30,000 in
the Brazilian part alone (Gentry, 1982), but these may
represent a crude underestimation of the total diversity
(Hopkins, 2007). Based on data compiled from monographs, Gentry (1982) estimated 76% of the Amazonian
flora as endemic at the species level.
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The geological history of the Amazon basin is
marked by a major shift in drainage orientation, caused
by the uplift of the Andean mountain range (Hoorn,
1993). Before the Andean uplift, most of the Amazon
basin drained westward to the Pacific and was covered
by westward deposition of low-fertility sediments from
the pre-Cambrian Brazilian and Guiana Shields (Hoorn,
1993). With the subsequent uplift of the northern Andes, starting approximately 15 mya, the direction of
sediment deposition shifted eastward, and most of the
ancient sands were covered by deep clay sediments coming from the Andes (Burnham & Graham, 1999). During
the Late Miocene (8–10 mya), the Pebasian Sea transgression created a marine seaway uniting the Caribbean
to the South Atlantic and resulted in a dramatic landscape change leading to the current configuration of
the Amazon basin (Räsänen et al., 1995; Webb, 1995).
The presence of rainforests in the basin largely colonizes relatively recent Andean sediments. Earlier sandy
sediments from the Guiana Shield cover approximately
3% of the Amazon (ter Steege et al., 2000) and are
found in patches mostly in the upper Rio Negro of
northwestern Brazil (Anderson, 1981; Prance, 1996),
neighboring areas in Venezuela and Colombia (Daly &
Mitchell, 2000), and the Iquitos region of northeastern Peru (Alonso & Whitney, 2003). These areas of
white-sand soils do not support tall rainforests but rather
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FIASCHI & PIRANI: Plant biogeography in Brazil
several physiognomies varying from open scrublands to
low forests, depending on the proximity of the water table (Anderson, 1981; Huber, 1995; Prance, 1996; Daly
& Mitchell, 2000).
The Amazon phytogeographic domain is broadly
defined here to include the Guianan lowlands (Gentry,
1982; Granville, 1988) and the Guiana Shield (Huber,
1995) (i.e., the Amazonian subregion of Morrone,
2006), in spite of strong evidence to the contrary (Mori,
1991; Berry et al., 1995; Kelloff & Funk, 2004; Berry
& Riina, 2005). Thus, in addition to the large extension of lowland rainforests and white-sand forests, several other physiognomies are found in scattered patches
across this domain. The most prominent of these patches
are the Amazonian savannas (Prance, 1996; Daly &
Mitchell, 2000), which are floristically linked to the Cerrado (see section 2.2), and the tepuis, which are remnant sandstone plateaus of the Guiana Shield (Huber,
1995; Prance, 1996; Daly & Mitchell, 2000; Berry &
Riina, 2005). Most tepuis are restricted to Venezuela,
but some extend to northern Brazil, eastern Colombia
and the Guianas (Daly & Mitchell, 2000; Berry & Riina,
2005). The tepui vegetation is very diverse physiognomically (Huber, 1995; Daly & Mitchell, 2000), and 42% of
the flora from areas above 1500 m (the Pantepui region)
has been estimated as endemic (Berry & Riina, 2005).
Of major importance to Brazilian biogeography are
floristic connections between the Guiana Shield with
white-sand Amazonian habitats and/or eastern Brazil,
as exemplified by Bonnetia (Bonnetiaceae), Caraipa
(Clusiaceae), Potalia (Gentianaceae), Humiria (Humiriaceae), Chamaecrista and Eperua (Leguminosae),
Marcetia and Microlicia (Melastomataceae), Biophytum (Oxalidaceae), Rapateaceae, Pagamea and Sipanea
(Rubiaceae), Barbacenia and Vellozia (Velloziaceae),
and Xyridaceae. Among the few phylogenetic studies
focused on white-sand plant lineages, Struwe et al.
(1998) suggested a general pattern where endemic
white-sand taxa represent older lineages from which
more recent lineages have been derived. Although this
hypothesis has not been sufficiently tested with phylogenetic data, Frasier et al. (2008) provided additional
support for the older ancestry of endemic white-sand
taxa. Other studies, however, point to more complex
scenarios, involving several shifts to white-sand areas
from ancestors growing in more fertile clay or terrace
soils (Fine et al., 2005), back and forth movements between lowland forests and tepui summits (Steyermark,
1986; Givnish et al., 2000), and shifts to habitats with
different light conditions, flooding regimes and altitude
(Vicentini, 2007).
Based on the detection of areas of bird endemism
in the Amazon, Haffer (1969) proposed a model to ex
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2009 Institute of Botany, Chinese Academy of Sciences
481
plain the diversification of the Amazonian biota in terms
of allopatric speciation driven by forest fragmentation
during glacial events in the Quaternary. This Pleistocene
refuge model predicted that areas with a greater number
of endemic species were likely to have acted as refuges
for rainforest taxa during the expansion of savannas in
glacial times. These isolated patches of rainforest in a
landscape of savannas and dry forests would have provided the reproductive isolation required for allopatric
speciation. The same (or slightly modified) areas of endemism reported for birds were believed to have also
accounted for the diversification of frogs, lizards, butterflies and several groups of plants (Vanzolini, 1970;
Brown, 1982; Prance, 1982). However, the initial excitement to detect such refuges for several groups of organisms was accompanied by many attempts to test the
model, most of which have largely refuted the assumptions based on collection bias (Nelson et al., 1990), hypothesized paleoecological conditions (Colinvaux et al.,
2000, 2001; Bush & Oliveira, 2006), and molecular systematic data (e.g., Moritz et al., 2000; Patton & Silva,
2005). Several additional models have been proposed to
explain Amazonian biodiversity, but none have achieved
the same credibility (for a review of these models see
Haffer, 1997, 2008; Marroig & Cerqueira, 1997). Current views on Amazonian diversification suggest that it
is unlikely for the pattern to be adequately explained by
the model of vicariance alone (Bush, 1994), requiring
a mixture of pre-Pleistocene speciation events (Patton
& Silva, 2005) and recent radiations (Richardson et al.,
2001; Erkens et al., 2007). Geological processes and
marine transgressions throughout the Amazon basin
have been invoked as potential causes for currently observed vicariance patterns (Räsänen et al., 1995; Patton & Silva, 2005; Rossetti et al., 2005), whereas recent diversification of some plant groups appear to have
been promoted by ecological shifts related to habitat
(Prance, 1982, 1994; Gentry 1988b, 1989; Tuomisto
et al., 1995; Fine et al., 2005), pollinator specialization
(Gentry, 1982; Kay et al., 2005), and fluctuating temperatures and precipitation (Graham, 1997).
In order to investigate diversification of the Amazonian biota, attempts to detect areas of endemism have
been made for several groups of organisms (Haffer,
1969; Vanzolini, 1970; Prance, 1982; Brown, 1982;
Cracraft, 1985; Cracraft & Prum, 1988), although most
studies have relied solely on the detection of such areas and the possible causes for their existence. The
following areas of endemism have been consistently
identified in the Amazon: Guiana (northern Brazil,
Guyana, Surinam and French Guiana); Imeri (southern Venezuela and neighboring areas in Brazil and
Colombia); Napo (Upper Negro-Uaupés rivers in Brazil,
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and Colombian, Ecuadorian and northern Peruvian
Amazon); Inambari (southwestern Brazilian Amazon,
eastern Peru and northwestern Bolivia); Rondônia
(Madeira-Tapajós interfluvial areas, into northern
Bolivia); Pará (southern Pará and northern Mato Grosso
states in Brazil); and Belém (northeastern Brazilian
Amazon). Most information on the historical relationships among Amazonian areas of endemism based on
phylogenetic data comes from studies of birds (Cracraft,
1985; Cracraft & Prum, 1988; Marks et al., 2002; Eberhard & Bermingham, 2005; Ribas et al., 2005), butterflies (Hall & Harvey, 2002) and dipterans (Nihei &
Carvalho, 2007 and references therein) and, to our understanding, the issue of how such areas are related to
each other based on plant phylogenies has never been
addressed.
There is evidence disputing the recognition of
the Amazon as a biogeographic unit (Garzón-Orduña
& Miranda-Esquivel, 2007; Nihei & Carvalho, 2007).
Some studies suggest a composite nature where southeastern Amazonian taxa are historically linked to
eastern Brazilian taxa, and northwestern Amazonian
taxa are more proximally related to Central American, Caribbean and Chocoan ones (Amorim & Pires,
1996; Amorim, 2001; Ribas & Miyaki, 2004; Nihei &
Carvalho, 2007). Other studies are supportive of the
Amazon as a single historical unit, that is, with southeastern and northwestern areas sister to each other (Silva
& Oren, 1996; Bates et al., 1998; Eberhard & Bermingham, 2005). As far as we are concerned, the historical
separation of the Amazon in these two blocks (southeastern and northwestern) has never been tested with
plant phylogenetic studies, but seems to agree, at least
spatially, with the extension of a middle Miocene marine transgression that separated the Guiana and Brazilian shields (Räsänen et al., 1995; Webb, 1995; Nores,
1999). The hypothesis that the biota of the southeastern
portion of the Amazon region is more closely related
to that of the central Brazilian forests than to the northwestern Amazonian ones has already been suggested by
floristic analyses (e.g., Oliveira-Filho & Ratter, 1995;
Ivanauskas et al., 2008), and remains to be tested with
plant phylogenetic studies.
Regardless of the methodology used, raw distributions or taxon phylogenies, relationships among
Amazonian areas of endemism seem to show some degree of congruence (Ron, 2000; Hall & Harvey, 2002).
The summary area cladogram (Guiana + (Rondônia +
(Pará + Belém))) + (Imeri + (Napo + Inambari)) presented by Hall and Harvey (2002) seems to be a good
working hypothesis, because it combines data from several unrelated groups of organisms. According to this
hypothesis two Amazonian blocks (S/SE and W/NW)
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are sister groups and, as a whole, sister to Guiana. Alternative scenarios have been proposed, especially regarding the position of Rondônia as part of the W/NW block
(Cracraft & Prum, 1988; Eberhard & Bermingham,
2005), and Guiana as part of the S/SE block (Racheli &
Racheli, 2004; Eberhard & Bermingham, 2005; GarzónOrduña & Miranda-Esquivel, 2007). Large-scale phylogenetic studies of plant taxa with widespread distribution in the Amazon basin, but with limited dispersal
ability, could be designed to test if these area relationships are supported.
2.2 Cerrado
The Cerrado domain originally covered ca. 2 million km2 of the central Brazilian Plateau, extending west
into Bolivia, south to Paraguay, and east to the Caatinga,
and with some isolated patches found scattered across
the Amazonian and Atlantic forests, and the Caatinga
(Prance, 1996; Daly & Mitchell, 2000). Most of the
cerrado vegetation is characterized by savanna physiognomies with a grass-rich ground layer growing on
nutrient-poor soils with high aluminum content (Eiten,
1972; Ratter et al., 1997, 2006). The woody flora is
mostly composed of sclerophyllous evergreen plants
adapted to periodic fires, and with well-developed root
systems reaching underground water tables. Depending
on the density of the woody component, the structure
of the vegetation can vary from open grassland to forest
with a closed canopy (Silva & Bates, 2002; Ratter et al.,
2003, 2006).
The Cerrado flora is very rich, with an estimated
vascular plant diversity ranging from 6,429 to approximately 10,500 species (Mendonça et al., 1998; Ratter
et al., 2006). Approximately 35% of the trees and 70%
of the herbaceous and shrubby plants that grow in the
Cerrado are endemic to this domain (Pennington et al.,
2006a; Ratter et al., 2006), whereas most of the nonendemic species are associated with the Atlantic Forest
domain (Méio et al., 2003; Ratter et al., 2006; but see
Gonçalves, 2004 for an Amazonian connection). Besides the high levels of diversity and endemism, the
Cerrado has sufferred a high degree of disturbance, especially due to agricultural expansion, cattle ranching,
and charcoal production (Ratter et al., 1997; Silva &
Bates, 2002). There are estimates that less than 20% of
the cerrado vegetation remains undisturbed, which has
resulted in its recommendation as a biodiversity hotspot
(Myers et al., 2000; Mittermeier et al., 2005).
Floristic comparisons among several sites in the
Cerrado domain have led to the recognition of seven
floristic provinces based on the presence/absence of
woody taxa (Ratter et al., 1996, 2003, 2006). These studies have pointed to a previously unrecognized floristic
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FIASCHI & PIRANI: Plant biogeography in Brazil
heterogeneity mostly associated with soil type and geographic location. A few taxonomic based biogeographic
studies (e.g., Simon & Proença, 2000; Fiaschi & Pirani,
2008) seem to corroborate these patterns, and phylogeographic studies of endemic Cerrado plant species are
suggestive of genetic structuring among these floristic
provinces following Quaternary climatic changes (e.g.,
Ramos et al. 2007).
The highest levels of endemism in the Cerrado domain are found along the mountains of the Espinhaço
Range (Minas Gerais and Bahia states), and the Chapada dos Veadeiros (Goiás state) (Prance, 1994; Simon
& Proença, 2000; Silva & Bates, 2002; Fiaschi & Pirani,
2008). Most of the endemic species grow in areas above
900–1000 m along these mountains, which are covered
by a low, mostly herbaceous or shrubby vegetation on
sandy or stony soils called campos rupestres (Giulietti
& Pirani, 1988; Harley, 1995; Alves et al., 2007). The
high level of endemism in the campos rupestres flora has
been recognized by several authors (Joly, 1970; Giulietti
& Pirani, 1988; Harley, 1995; Rapini et al., 2002), but
the explanations proposed for these diversity patterns
remain very speculative because most of the relevant
studies lack phylogenetic hypotheses for the endemic
taxa.
Studies exploring diversification patterns among
endemic Cerrado plants using dated molecular phylogenies are just beginning. A few studies suggest recent (3–
4.7 mya) diversification events in high-altitude clades
including Viguiera (Asteraceae), Microlicieae (Melastomataceae), and Minaria (Apocynaceae) (Schilling
et al., 2000; Fritsch et al., 2004; and Rapini et al., 2007,
respectively). Further phylogenetic studies of the endemic flora of the Cerrado could provide additional
data to evaluate whether most of the endemic flora is
the result of recent radiations, as suggested by Pennington et al. (2006b). Several angiosperm groups are
good candidates for this goal, such as: Eremanthus,
Lychnophora and Richterago (Asteraceae), Encholirium (Bromeliaceae), Kielmeyera (Clusiaceae), Eriocaulaceae, Pseudotrimezia (Iridaceae), Eriope (Lamiaceae), Chamaecrista and Mimosa (Leguminosae),
Diplusodon (Lythraceae), Byrsonima (Malpighiaceae),
Microlicia and Trembleya (Melastomataceae), Sauvagesia (Ochnaceae), Declieuxia (Rubiaceae), Barbacenia
and Vellozia (Velloziaceae).
2.3 Atlantic forest
The Atlantic forests originally occupied approximately 1.5 million square kilometers, extending from
Rio Grande do Norte to Rio Grande do Sul states along
the Brazilian coast. The width of this forest strip is
very variable, and it extends far inland in some ar
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eas of southeastern Brazil, eastern Paraguay, and Misiones Province of Argentina (Galindo-Leal & Câmara,
2003; Oliveira-Filho et al., 2006). The Atlantic coastal
forests are separated from the Amazonian forests by a
northeast–southwest diagonal swath of open or dry formations (Prado & Gibbs, 1993; Prado, 2000; Silva et al.,
2004), which are believed to act as a current barrier
to floristic exchange between these two forest blocks
(Mori et al., 1981; but see Oliveira-Filho & Ratter,
1995; Costa, 2003). Because the Atlantic forests harbor a unique biota that is very rich in endemic species,
and because of the high level of habitat destruction the
region has been suffering – only approximately 7.5% of
the original vegetation remains – it is considered one
of the world’s priorities for biodiversity conservation
(Myers et al., 2000; Mittermeier et al., 2005).
The Atlantic Forest domain is characterized mostly
by evergreen tropical forest but SDTFs (Oliveira-Filho
et al., 2006) and subtropical forests (the Paranaense
Province of Cabrera & Willink, 1973, including
Araucaria forest) are also usually considered part of
the domain (Oliveira-Filho & Fontes, 2000; the Parana
Subregion of Morrone, 2006). In addition to forest physiognomies, mangroves and shrubby restinga vegetation
are widespread in sea-level sandy areas (Scarano, 2002),
and patches of high altitude grasslands and rocky outcrops are usually found above 2000 m along the Serra
do Mar and Serra da Mantiqueira mountain ranges
(Safford, 1999, 2007). The archipelago-like open formations found along the montane areas of the Atlantic
forests harbor a highly endemic flora (over 20%) that has
strong floristic connections with other South American
montane areas such as the Andes (Safford, 2007), and
the aforementioned campos rupestres of the Espinhaço
Range (Giulietti & Pirani, 1988; Di Maio, 1996;
Safford, 1999; Calió et al., 2008). The fragmented distribution of these open areas, coupled with episodic dispersal events, appear to have favored allopatric speciation in Sinningieae (Gesnericaeae) (Perret et al., 2007),
and suggest that habitat heterogeneity may have played
an important role in the diversification of the endemic
Atlantic forest flora.
Vascular plant diversity and endemism in the
Atlantic rainforests are among the highest in the world
(Martini et al., 2007), but information on the geographic
distribution of many taxa is lacking. There are approximately 20,000 species of vascular plants in the
Atlantic forests (Myers et al., 2000), with estimated levels of endemism varying from 33% of the pteridophytes
to more than 81% of the 803 species of bromeliads
(Martinelli et al., 2008), and 41.6–44.1% of the total
number of vascular plants from two reserves at southern Bahia (Thomas et al., 1998). Among the angiosperm
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genera, 159 are endemic to the Atlantic forests and
approximately half of those are monotypic (Stehmann
et al., in press). Many others groups are represented
better there than anywhere else in the Neotropics, such
as Hornschuchia (Annonaceae), many Bromeliaceae
genera, Nematanthus and Sinningia (Gesneriaceae),
Huberia and Pleiochiton (Melastomataceae), Dorstenia (Moraceae), Calyptrogenia and Myrceugenia (Myrtaceae), Oxalis subg. Thamnoxys (Oxalidaceae), Atractantha and Merostachys (Poaceae), Coccocypselum
(Rubiaceae), Conchocarpus and Galipea (Rutaceae).
In addition to its highly endemic flora, the Atlantic forests harbor early diverging lineages of some
angiosperm groups, such as the Poaceae subfamily
Anomochlooideae (Judziewicz & Clark, 2007), Goniorrhachis and Barnebydendron, which correspond to the
first diverging branches of the Detarieae clade of Leguminosae (Bruneau et al., 2008), and the Harleyi clade of
Pagamea (Rubiaceae), which point to a possible arrival
through dispersal from African ancestors (Vicentini,
2007). Based on the presence of presumably “primitive”
species in the Atlantic forests, Gentry (1982) suggested
that it could be a “source area” of Gondwanan taxa
for other phytogeographic regions, such as the geologically recent Amazon lowlands and the Andes, although
Prance (1982) discounted the floristic contribution of
the Atlantic forests to the Amazon flora due to their
early isolation. The basal placement of Atlantic forest
taxa in several phylogenetic hypotheses of Neotropical
organisms seems to support the contribution of early diverging lineages to the Atlantic Forest biota (Cracraft &
Prum, 1988; Bates et al., 1998; Eberhard & Bermingham, 2005). In other cases, however, the presence of
some lineages in these forests seems to result from more
recent colonization from other South American source
areas (Cracraft & Prum, 1988; Costa, 2003; Vicentini,
2007). Thus, as suggested by Silva and Castelletti (2003)
and Pennington et al. (2006b), it seems more prudent to
view the Atlantic Forest biota as having contributions
from both old and recently diverged lineages.
Multiple centers of endemism based on several
groups of organisms have been proposed for the Atlantic
Forest domain (Prance, 1982; Cracraft, 1985; Soderstrom et al., 1988; Costa et al., 2000; Silva et al., 2004;
Santos et al., 2007). The number of such centers varies
depending on the organisms under consideration and
the specific questions being addressed, both of which
influence the selection of areas. Thus, although some
studies point to a northern/southern separation in just
two blocks (Cracraft, 1985; Soderstrom et al., 1988),
finer-scale studies using low-vagility organisms suggest
more numerous and smaller areas (e.g., Pinto-da-Rocha
et al., 2005). Regardless of the study group and method-
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ology used, most studies agree that there is an historical
separation between the northern and southern parts of
the domain, whose limits are more or less coincident
with the Rio Doce valley (northern Espı́rito Santo state)
(Cracraft & Prum, 1988; Amorim & Pires, 1996; Costa,
2003; Silva et al., 2004; Pinto-da-Rocha et al., 2005;
Perret et al., 2006). Several examples of plant taxa restricted to either one of these areas are known, resulting
in a strong floristic differentiation between the northern
and southern Atlantic forests (Oliveira-Filho & Fontes,
2000; Oliveira-Filho et al., 2005).
The northern Atlantic forest (NAf) ranges from
Rio Grande do Norte (ca. 5◦ S) to northern Espı́rito
Santo (ca. 19◦ S) states, and comprises mostly a
narrow strip of forest bounded to the west by the
Caatinga domain (Thomas & Barbosa, 2008), as well
as some inland areas, such as the “brejos nordestinos”
(Rodal & Sales, 2008) and the Chapada Diamantina
forests (Funch et al., 2008). Two centers of endemism
are usually recognized in the NAf: Pernambuco (ca.
8◦ S), and Bahia (“central corridor”, from approximately 13◦ to 19◦ S) (Thomas et al., 1998). The
NAf shows some floristic influence from the Amazonian forests, presumably due to historical connections
through the Cenozoic (Rizzini, 1963; Andrade-Lima,
1966; Prance, 1979; Mori et al., 1981; Costa, 2003).
Although the extension of these forest connections are
unknown, three main routes for floristic exchange between the Amazonian and Atlantic rainforests have been
proposed (Costa, 2003): a southern route through the
Paraná River basin, a northeastern route through the
Caatinga domain (Rizzini, 1963; Andrade-Lima, 1966),
and a route by way of gallery forests across the central Brazilian cerrado (Oliveira-Filho & Ratter, 1995).
The closer biogeographic relationship of the Pernambuco center plus the brejos nordestinos to the Amazon
rather than to southern Atlantic forests is supportive
of the northeastern route (Prance, 1979, 1982; Silva
et al., 2004; Santos et al., 2007). In addition, evidence
is provided by the disjunct occurrence of several genera
in the NAf and the Amazonian forests that are lacking in the southern Atlantic forests such as Lacmellea and Macoubea (Apocynaceae), Anthodiscus (Caryocaraceae), Glycydendron (Euphorbiaceae), Gustavia
and Lecythis (Lecythidaceae), Macrolobium and Parkia
(Leguminosae), Roucheria (Linaceae), Adelobotrys and
Graffenrieda (Melastomataceae), Anomospermum and
Orthomene (Menispermaceae), Naucleopsis and Pseudolmedia (Moraceae), Aptandra (Olacaceae), Atractantha and Pariana (Poaceae), and Pagamea and Remijia
(Rubiaceae).
The southern part of the domain [southern Atlantic
forests (SAf)] ranges from Espı́rito Santo (ca. 19◦ S)
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to southern Santa Catarina (ca. 29◦ S), and it includes
a large western extension of seasonally dry forests in
southeastern Brazil, eastern Paraguay, and Misiones
in Argentina (Oliveira-Filho & Fontes, 2000; OliveiraFilho et al., 2006), and the Araucaria angustifolia Forest
Province (Morrone, 2006). The seasonally dry forests of
the Paranaense and Misiones nuclei are currently considered a distinct phytogeographic unit (Prado, 2000;
Pennington et al., 2006a), whereas the subtropical Araucaria forests are sometimes considered on their own as
the Paranaense Province (Cabrera & Willink, 1973) or
the Araucaria angustifolia Forest Province (Morrone,
2006). The SAf block comprises an extensive center of
endemism that seems to coincide well with the Serra do
Mar and Serra da Mantiqueira mountain ranges (Prance,
1982; Silva et al., 2004; Pinto-da-Rocha et al., 2005).
Here we adopt the delimitation of the Serra do Mar
center of endemism as proposed by Silva et al. (2004),
which is congruent with a group of historically related
areas ranging from southern Espı́rito Santo to northern
Santa Catarina (Pinto-da-Rocha et al., 2005). Instead of
sharing a high number of taxa with Amazonia, the SAf
seems to be influenced more strongly by elements of
other regions. As an example, some Andean-centered
taxa can be found in the SAf but are usually absent
in the NAf (A. Amorim, pers. comm., 2009), such
as Oreopanax (Araliaceae), Clethra (Clethraceae),
Gaultheria (Ericaceae), Escallonia (Escalloniaceae),
Gordonia (Theaceae), Macrocarpaea (Gentianaceae),
Hypericum (Clusiaceae), Meriania (Melastomataceae),
Calyptrogenia and Myrceugenia (Myrtaceae), Fuchsia (Onagraceae), Aulonemia, Chusquea and Colanthelia (Poaceae), Euplassa (Proteaceae), Meliosma (Sabiaceae), and Valeriana (Valerianaceae). As discussed in
section 1, other floristic elements of the SAf are probably remnants of a southern Gondwanan land connection
(Sanmartı́n & Ronquist 2004), such as A. angustifolia,
Canellaceae, Weinmannia (Cunoniaceae), Crinodendron (Elaeocarpaceae, Crayn et al., 2006), Griselinia
(Griseliniaceae), Podocarpus (Podocarpaceae), some
Proteaceae (Barker et al., 2007), and Drimys (Winteraceae).
The floristic differences between the northern and
southern blocks of the Atlantic forests are supported
by the available phylogenetic data. Most biogeographic
studies point to the Atlantic Forest domain as a composite biogeographic area where the southern and northern areas are not sister groups (e.g., Cracraft & Prum,
1988; Costa, 2003; Perret et al., 2006; Nihei & Carvalho, 2007; Santos et al., 2007), however, in others the
same two blocks form a monophyletic Atlantic Forest
(e.g., Amorim & Pires, 1996; Costa et al., 2000). Although rare, the exchange of floristic elements between
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485
the NAf and SAf has been proposed by Perret et al.
(2006) and seems to account for the presence of typical
elements of the SAf in montane areas of southern Bahia
(A. Amorim, pers. comm., 2009) and the Chapada Diamantina (Funch et al., 2008).
2.4
Caatinga
The Caatinga domain of northeastern Brazil is the
largest continuous area of SDTFs of South America,
originally covering an area of approximately 850,000
km2 (Queiroz, 2006). The vegetation varies from an
open thorny scrub to low dry forests; it is conditioned
by a prevailing semiarid climate, with high evapotranspiration potential (1500–2000 mm/year) and low precipitation (300–1000 mm/year) concentrated during a
short period of 3–5 months (Sampaio, 1995; Queiroz,
2006). Floristic diversity in the Caatinga is relatively
low (Sampaio, 1995), especially when compared to that
of the Atlantic rainforests and the Cerrado (e.g., Castro
et al., 1999; Myers et al., 2000); however, 46% endemic
species have been reported for the tree flora (Pennington
et al., 2006a), and 52.5% for the family Leguminosae
(144 of 274 species endemic to this domain, Queiroz,
2006). Likewise, Giulietti et al. (2002) have listed 18
angiosperm genera and 318 species as endemic to the
Caatinga.
The floristic composition of the Caatinga shows
strong links with other nuclei of South American
SDTFs, such as Misiones, Piedmont, the Caribbean
coast of Colombia and Venezuela, and the dry interAndean valleys, but not to the mostly subtropical South
American dry forests of the Chaco domain (Prado &
Gibbs, 1993; Prado, 2000; Pennington et al., 2000,
2006a). The recent recognition that SDTFs represent an
archipelago-like biogeographic unit (Prado, 2000) has
stimulated interest in the historical processes that may
have shaped current distributions of SDTF-centered
taxa (Pennington et al., 2000, 2004; Lavin, 2006; Ritz
et al., 2007), not to mention their importance as repository areas for the conservation of the highly threatened
Neotropical dry forest flora (Gentry, 1995).
Few studies have specifically focused on the
Caatinga (Pennington et al., 2006a). In a first attempt
to examine the historical biogeography of the Caatinga,
Queiroz (2006) used distribution data of Leguminosae
species, which account for approximately one-third of
the total number of plant species found in the biome
(Giulietti et al., 2002). By plotting the known geographic distributions of 274 species in the area occupied by the biome, he found that despite sharing
an overall physiognomic similarity, the flora of the
Caatinga could be divided into two distinct floristic
blocks. One of these blocks is associated with soils
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derived from the crystalline basement and accounts for
most of the floristic link of the Caatinga with the remaining areas of SDTFs (Prado, 2000). Genera characteristic of these areas include Amburana, Apuleia and
Pterogyne (Leguminosae), as well as Balfourodendron
(Rutaceae), Quiabentia (Cactaceae), Astronium (Anacardiaceae), and Patagonula (Boraginaceae) (Queiroz,
2006). The second group corresponds to plants growing on sandy sedimentary areas scattered across the domain, and these accounts for most of the endemic taxa
of Leguminosae found in the Caatinga.
The historical development of this scenario was
proposed as the result of a widespread process of
pediplanation during the early Quaternary that uncovered the Precambrian crystalline bedrock in the region.
According to this hypothesis, the earlier continuous
sedimentary surfaces became dissected, leading to allopatric differentiation of their taxa. The exposed areas derived from the crystalline bedrock were occupied by elements typical of the SDTF flora (Queiroz,
2006), which were postulated as having evolved during
the Miocene–Pliocene (Pennington et al., 2004; SaslisLagoudakis et al., 2008) and may have migrated later to
the Caatinga. Phylogenetic analyses of taxa with multiple species centered in the Caatinga would be critical
to test this scenario. Some good candidates for this purpose are groups within Croton and Jatropha (Euphorbiaceae), several Leguminosae genera such as Vachellia (Acacia s.l.), Aeschynomene, Bauhinia, Calliandra,
Centrosema, Chamaecrista, Lonchocarpus, Macroptilium, Mimosa, Senna, Stylosanthes, and Zornia, as well
as genera with several species endemic to the Caatinga,
such as Melocactus and Pilosocereus (Cactaceae), Apodanthera (Cucurbitaceae), Hyptis (Lamiaceae) and Piriqueta Aubl. (Turneraceae) (Giulietti et al., 2002).
2.5 Campos sulinos (southern grasslands)
Extensive areas of southern Brazil are covered by
open grassy formations generally called campos, which
have been used as natural pastures (see Overbeck et al.,
2007 for an overview on South Brazilian campos). In
Brazil alone it is possible to distinguish between the
campos do Planalto Meridional, which have a patchy
occurrence within the Atlantic Forest domain and range
from Paraná to northern Rio Grande do Sul states (Araucaria angustifolia Forest Province of Morrone, 2006),
to the continuous pampas or campos da Campanha
Gaúcha, which covers the largest part of Rio Grande do
Sul and neighboring areas of Uruguay and Argentina
(Pampa Province of Morrone, 2006). The patchy distribution of the campos do planalto is a consequence of its
dynamics with the Araucaria Forest, which tends to advance over the campos – young Araucaria plants cannot
2009
grow in shade – with forest expansion being controlled
by fire and other human activities (Klein, 1960; Behling
et al., 2004; Overbeck et al., 2007).
Within the pampas, some authors further separate
the southern Brazilian and Uruguayan grasslands (north
of Rio da Prata) from the Argentinian pampas based
on floristic differences (e.g., Soriano et al., 1992). The
word “pampa” itself has a Quechua origin meaning “flat
region.” In this sense, it includes all low, flat areas of
the Rio da Prata basin northward to the Serra Geral. In
this section we use the term pampas in this broad definition, which agrees with Morrone’s Pampa Province
(Morrone, 2006).
Floristic and physiognomic differences between
the campos do planalto and the pampas are evident.
Among the grasses, the relative importance of megathermic groups, such as Andropogoneae, Chlorideae, Eragrosteae and Paniceae in the campos do planalto is
much higher than in the pampas, which in turn have a
higher contribution of microthermic elements, including Agrostis, Aristida, Briza, Bromus, Calamagrostis,
Danthonia, Piptochaetium, and Stipa (Burkart, 1975;
Longhi-Wagner & Zanin, 1998; Boechat & LonghiWagner, 2000; Overbeck et al., 2007). In fact, the grass
flora of the pampas consists of a mixture of both megathermic and microthermic grasses, which have distinct
phenological phases (Burkart, 1975). Also noteworthy
is the common presence of palms (mostly small species
of Butia) in the campos do planalto, and its rarity or
absence in the pampas.
Plant diversity in the Campos sulinos has
been estimated as between 3,000 and 4,000 species
(Overbeck et al., 2007), and some studies point to
these grasslands as among the most species-rich in the
world (Overbeck et al., 2006). The flora is dominated by
species of sedges and grasses, but also includes shrubs
and subshrubs of several families, such as Apiaceae
(mostly Eryngium), Asteraceae (several species of Baccharis), Leguminosae, Myrtaceae, Malvaceae, Oxalidaceae and Rubiaceae (Joly, 1970; Soriano et al., 1992;
Overbeck et al., 2007). The flora of the Campos sulinos in general has links to other open formations of
South America. Several elements from the herbaceous
flora of the Cerrado domain have their southern limits
in the Campos sulinos (e.g., Boechat & Longhi-Wagner,
2000), where many elements of temperate/subtropical
floras are fairly common. At the same time, some of
these southern elements have their northernmost occurrence in this same region (e.g., Longhi-Wagner & Zanin,
1998). The apparent transitional nature of the Campos
sulinos flora is even more evident in the state of Rio
Grande do Sul, where the campos de planalto are replaced by the pampas at about 30◦ S (Smith, 1962;
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Burkart, 1975; Waechter, 2002; Ritter & Waechter,
2004; Overbeck et al., 2007).
Many examples of Andean-derived taxa are known
from southern Brazil (Rambo, 1956; Smith 1962). A
good example of connection with the Andean flora is
provided by the presence of Gunnera manicata (Gunneraceae) in the wet hills and swamps of the high eastern
planaltine areas of Santa Catarina and Rio Grande do
Sul states. Dispersals of Andean genera both through
Argentina to southern Brazil (Klein, 1960; Leite, 2002)
and from the Paraná basin grasslands to the Andes (Katinas & Crisci, 2008) have been reported. The resulting
disjunct pattern (see section 3.2.2.) is supported not
only by similar mild climatic conditions, but also by former Quaternary connections that could have taken place
during interglacial wetter periods (Ortiz-Jaureguizar &
Cladera, 2006).
3
Patterns of distribution of Brazilian flora
As previously discussed, many angiosperm genera present in Brazil are also found on other continents. The most common patterns of intercontinental disjunctions include: (i) Africa, for example,
Duguetia (Annonaceae), Pitcairnia (Bromeliaceae),
Rhipsalis baccifera (Cactaceae), Chrysobalanus icaco
(Chrysobalanaceae), Conceveiba and Pogonophora
(Euphorbiaceae), Symphonia globulifera (Clusiaceae),
Sacoglottis (Humiriaceae), Dalbergia ecastophyllum
(Leguminosae), Aptandra and Ptychopetalum (Olacaceae), and Paullinia pinnata (Sapindaceae) (Thorne,
1973; Prance, 1979; Renner, 2004); (ii) other southern lands derived from Gondwana breakup (Sanmartı́n
& Ronquist, 2004); and (iii) tropical and subtropical
Asia, e.g., Anaxagorea (Annonaceae), Dendropanax
(Araliaceae), Hedyosmum (Chloranthaceae), Rourea
(Connaraceae), Caryodaphnopsis (Lauraceae), Schoepfia (Olacaceae), and Gordonia (Theaceae) (Good, 1974).
The geographic distribution patterns of Brazilian
plant species are in general agreement with the main
geomorphological domains and their vegetation types.
Most species are either endemic to one domain or found
in a regional subdivision or small portion of each domain; several species, however, are widespread in the
Neotropics or disjunct between two of these domains.
In addition to the genera previously mentioned as candidates for biogeographic studies of the Brazilian flora
using a phylogenetic approach, we provide here examples of species and genera that illustrate geographic distributions endemic to one domain and disjunct between
domains. We have tried to represent all life habits among
these examples, but it is worth mentioning that we have
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487
a relative paucity of data on the geographic distribution
of vines when compared to that of the other life habits.
There are few recent monographs on important Neotropical vine groups, such as Bignoniaceae, Celastraceae
(subfam. Hippocrateoideae), Cucurbitaceae, Menispermaceae, Sapindaceae and Vitaceae.
3.1
Endemic to one domain
Each of the above-mentioned Brazilian phytogeographic domains has its own set of endemic genera and
species. Some genera and species have a geographic distribution somewhat similar to that of the domain where
they occur, and can serve as an indicator of domain
limits. Because the number of species endemic to each
domain is very extensive, we mention just a few as
examples.
3.1.1 Amazon We estimate that the number of angiosperm genera endemic to the Amazon may be approximately 300–350, in addition to the 80 endemic
genera of the Guiana Shield flora (Berry & Riina,
2005). It is difficult to estimate how many of the
Amazonian genera are restricted to Brazil, because
many of them are found in poorly explored areas close
to the Venezuelan, Colombian and Peruvian borders
(e.g., Yanomamua, Grant et al., 2006). In addition,
many new genera have been recently described for the
Amazonian flora but are not yet recorded in Brazil
(Zuloaga & Judziewicz, 1993; Londoño et al., 1995;
Woodward et al., 2007; Fernández-Alonso & Arbeláez,
2008). Examples of Amazonian endemic genera are:
Polygonanthus (Anisophylleaceae), Leopoldinia (Arecaceae), Hevea (Euphorbiaceae), Goupia (Goupiaceae), Asteranthos and Bertholletia (Lecythidaceae),
Dinizia and Eperua (Leguminosae), Huberodendron
(Malvaceae), Brachynema and Curupira (Olacaceae),
Parachimarrhis (Rubiaceae), Adiscanthus (Rutaceae),
Duckeodendron (Solanaceae), Phenakospermum (Strelitziaceae), and Thurnia (Thurniaceae). Endemic
species are numerous, many of which extend their
ranges beyond Brazilian frontiers; selected examples are Mauritia carana (Arecaceae), Protium
calendulinum (Burseraceae), Caryocar microcarpum
(Caryocaraceae), Hirtella physophora (Chrysobalanaceae), Parkia decussata (Leguminosae), and
Zanthoxylum djalma-batistae (Rutaceae).
3.1.2 Cerrado We estimate that ca. 60 angiosperm
genera are endemic to the Cerrado domain, including
Klotzschia (Apiaceae), Diplusodon (Lythraceae), and
Salvertia (Vochysiaceae). As already mentioned, 35% of
the tree species and 70% of the herbaceous and shrubby
plants found in the Cerrado are believed to be endemic.
These include Schefflera macrocarpa (Araliaceae), Butia archeri and Syagrus petraea (Arecaceae), Tabebuia
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ochracea (Bignoniaceae), Caryocar brasiliense
(Caryocaraceae), Kielmeyera coriacea (Clusiaceae),
Connarus suberosus (Connaraceae), Andira cujabensis,
Dimorphandra mollis and Hymenaea stigonocarpa
(Leguminosae), Oxalis hirsutissima (Oxalidaceae),
Esenbeckia oligantha (Rutaceae), Styrax martii (Styracaceae), Piriqueta tamberlikii (Turneraceae), Stachytarpheta gesnerioides (Verbenaceae), and Qualea
grandiflora and Q. parviflora (Vochysiaceae).
3.1.3 Atlantic Forest
Stehmann et al., (2009)
reported 159 angiosperm genera and 3,364 species as
endemic to the Atlantic Forest. Most of the endemic
species are not found across the entire range of the
domain, and the ones listed below are illustrative
of many distinct distribution patterns: Carpotroche
brasiliensis (Achariaceae), Hippeastrum reticulatum
(Amaryllidaceae), Schefflera angustissima (Araliaceae), Allagoptera arenaria (Arecaceae), Tabebuia
elliptica (Bignoniaceae), Maytenus aquifolium (Celastraceae), Stephanopodium blanchetianum (Dichapetalaceae), Sloanea obtusifolia (Elaeocarpaceae),
Nematanthus lanceolatus (Gesneriaceae), Cariniana
legalis (Lecythidaceae), Poecilanthe falcata (Leguminosae), Leandra melastomoides (Melastomataceae),
Trichilia pseudostipularis (Meliaceae), Mollinedia engleriana (Monimiaceae), Ficus organensis
(Moraceae), Virola gardneri (Myristicaceae), Hindsia
glabra (Rubiaceae), Conchocarpus insignis (Rutaceae),
Chrysophyllum inornatum (Sapotaceae), and Vochysia
schwackeana (Vochysiaceae).
3.1.4 Caatinga A comprehensive list of endemic
angiosperm genera from the Caatinga can be found
in Giulietti et al. (2002). The following are examples of endemic genera and species are illustrative. Genera: Apterokarpos (Anacardiaceae); Alvimiantha (Rhamnaceae); Anamaria (Scrophulariaceae);
Barnebya and Mcvaughia (Malpighiaceae); Facheiroa
(Cactaceae); Fraunhofera (Celastraceae); Blanchetiodendron (Leguminosae); and Rayleya (Malvaceae).
Species: Cyrtocarpa caatingae and Spondias tuberosa
(Anacardiaceae), Annona vepretorum (Annonaceae),
Aspidosperma pyrifolium (Apocynaceae), Copernicia
prunifera (Arecaceae), Tabebuia spongiosa (Bignoniaceae), Patagonula bahiensis (Boraginaceae), Encholirium spectabile (Bromeliaceae), Arrojadoa rhodantha
and Discocactus bahiensis (Cactaceae), Colicodendron
yco (Capparaceae), Mimosa paraibana and Hymenaea
eriogyne (Leguminosae), Ceiba glaziovii (Malvaceae),
Ruprechtia glauca (Polygonaceae), Pilocarpus sulcatus
(Rutaceae), and Averrhoidium gardnerianum (Sapindaceae).
3.1.5 Campos sulinos To our knowledge, Onira
(Iridaceae) is the only angiosperm genus restricted to
2009
the Brazilian sector of the Campos sulinos. According to Katinas et al. (2008), many genera of Asteraceae found in the campos are shared with neighboring areas in Argentina, Paraguay, and Uruguay, such as
Criscia, Holocheilus, Ianthopappus, and Pamphalea.
Lists of common species from the Brazilian campos
de planalto and pampas were provided by Overbeck
et al. (2007), including 10 endemic to the former and
nine to the pampas. A few selected examples include E.
megapotamicum and E. urbanianum (Apiaceae), Mangonia tweedieana (Araceae), Butia yatay (Arecaceae),
Mikania oreophila, Panphalea araucariophila, and Trichocline humilis (Asteraceae), Kelissa brasiliensis (Iridaceae), Aristida teretifolia, Eragrostis acutiglumis, and
Stipa charruana (Poaceae), Mimosa cruenta (Leguminosae), and Oxalis eriocarpa (Oxalidaceae).
3.2 Disjunct
Several patterns of disjunction have been described
for the Brazilian flora (e.g., Prance, 1979, 1988; Giulietti & Pirani, 1988; Mori, 1988; Pirani, 1990; Granville,
1992; Prado & Gibbs, 1993). In many cases they appear
to be the result of dispersal events rather than a consequence of the fragmentation of a wider ancestral distribution, as the distinct areas of occurrence have asymmetric species diversity (Lavin et al., 2000; Givnish
et al., 2000); in others cases the disjunct distribution
may be adequately explained by vicariance. For example, studies of paleoclimate and paleovegetation in
northeastern Brazil point to the previous existence of
extensive moist forests in the area presently occupied
by the dry Caatinga domain. The current presence of
scattered islands of montane forests (“brejos”) in this
domain is believed to represent relicts of these once
more widespread moist forests in the region (AndradeLima, 1982; Oliveira et al., 1999).
Besides the fact that disjunct geographic distributions provide cases well suited for historical biogeographic studies, the geographic separation of biological
entities is also suggestive of an interruption – or at least
reduction – of genetic flow, thus promoting opportunities for allopatric speciation. The examples provided
below are well-known cases of disjunct distribution patterns that are unlikely to be due to sampling artifacts.
As most of the disjunct taxa listed below are species or
small genera, we suggest that both species-level (phylogeographic) and phylogenetic studies of higher taxa
must be carried out. By adopting a multi-level approach
we believe that a better understanding of the intricate
interactions among geographic isolation, genetic differentiation, and eventually speciation can be achieved.
3.2.1 Amazon–Atlantic Forest As mentioned in
section 2.3, several studies point to former connections
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2009 Institute of Botany, Chinese Academy of Sciences
FIASCHI & PIRANI: Plant biogeography in Brazil
between the Amazonian and the Atlantic forests (e.g.,
Andrade-Lima, 1966; Prance, 1979; Mori et al., 1981;
Oliveira & Daly, 1999; Santos et al., 2007). Many examples of disjunct taxa found in these two forest blocks
are known, such as Philodendron ornatum (Araceae),
Anthodiscus amazonicus (Caryocaraceae), Parinari
excelsa (Chrysobalanaceae), Glycydendron (Euphorbiaceae), Couratari macrosperma and Eschweilera
ovata (Lecythidaceae), Sextonia (Lauraceae), Byrsonima laevigata (Malpighiaceae), Adelobotrys (Melastomataceae), Trichilia lepidota (Meliaceae), Elvasia
(Ochnaceae), Peperomia rhombea (Piperaceae), and
Pouteria venosa (Sapotaceae).
3.2.2 Southern Brazil–Andes The occurrence in
southern Brazil of a few species belonging to genera
best represented in the Andes (or even in the Holarctic
region, like Berberis L.) has been pointed out by several authors (e.g., Rambo, 1956; Smith, 1962; Clark,
1995; Waechter, 2002; Berry et al., 2004). In a floristic survey of the Aparados da Serra, in the northeastern part of Rio Grande do Sul state, Rambo (1956)
listed 742 seed plant species, and ascribed an “Andean origin” to 197 (26%) of them. In most cases
of this distribution pattern, the Brazilian extension is
restricted to subtropical or tropical high-altitude areas. Selected examples (some mentioned in section
2.3) include: Araucaria (Araucariaceae, with only two
species in South America, Araucaria araucana in Chile
and Araucaria angustifolia in Brazil); Holocheilus,
Mutisia and Perezia (Asteraceae), Berberis (Berberidaceae), Hedyosmum (Chloranthaceae), Clethra scabra
(Clethraceae), Hypericum (Clusiaceae), Crinodendron
(Elaeocarpaceae), Acca and Myrceugenia (Myrtaceae),
Fuchsia (Onagraceae), Chusquea (Poaceae), Quillaja (Quillajaceae), Acaena (Rosaceae), and Viviania
(Vivianiaceae).
3.2.3 Campos rupestres–Restinga
The term
restinga refers to low scrubs and forests on sandy areas of recent origin along the Brazilian coast (Daly &
Mitchell, 2000; Thomas & Barbosa 2008). Some studies have suggested a floristic connection between these
lowland restinga areas and the campos rupestres vegetation of the Espinhaço Range usually found above
1000 m (Giulietti & Pirani, 1988; Harley, 1988), as
reported for species of Lagenocarpus (Cyperaceae),
Leiothrix (Eriocaulaceae), Eriope (Lamiaceae), Mimosa
(Leguminosae), Marcetia (Melastomataceae), Phyllanthus (Phyllanthaceae), Eragrostis (Poaceae), and Vellozia (Velloziaceae). Among 56 plant taxa presumably
representative of this pattern, Alves et al. (2007) have
confirmed only nine (16%) as truly disjunct. Most of
the remaining species have also been found in lowland
Cerrado and Atlantic rainforests.
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2009 Institute of Botany, Chinese Academy of Sciences
489
3.2.4 Eastern Brazil–Guiana Shield This pattern
was mentioned by several authors (Steyermark, 1982;
Giulietti & Pirani, 1988; Berry & Riina, 2005). It is representative of groups with high diversity in the Guiana
Shield, and just one species in the Espinhaço Range,
such as the Schefflera group “Crepinella” (Araliaceae),
Bonnetia (Bonnetiaceae), and Cottendorfia (Bromeliaceae), or groups with highest diversity in the Espinhaço
Range and just a few species in the Guiana Shield,
such as Leiothrix (Eriocaulaceae), Chamaecrista (Leguminosae), Marcetia and Microlicia (Melastomataceae),
Declieuxia (Rubiaceae) and Vellozia (Velloziaceae). The
occurrence of asymmetric diversity in both directions is
suggestive that these patterns were achieved by recent
dispersal events, either westward (e.g., Chamaecrista,
Declieuxia, Leiothrix), or eastward (e.g., Bonnetia, Cottendorfia, Schefflera group Crepinella).
3.2.5 Disjunct among SDTFs This pattern is characteristic of species associated with two or more of the
SDTFs nuclei (Pennington et al., 2000, 2006a; Prado,
2000; Queiroz, 2006), among which the Caatinga,
Paranaense, Misiones and Piedmont account for most
of the species found in Brazil. It fits the Pleistocenic arc pattern proposed and richly illustrated by
Prado and Gibbs (1993). A few selected examples include Schinopsis brasiliensis (Anacardiaceae), Carica
quercifolia (Caricaceae), Amburana cearensis, Geoffroea spinosa and Poeppigia procera (Leguminosae),
Ruprechtia laxiflora (Polygonaceae), and Galipea ciliata (Rutaceae).
3.2.6 Disjunct among rock outcrops in Atlantic
Forest and/or Cerrado mountains Several genera
and species are shared among the “islands” of montane open formations found across the Atlantic Forest and Cerrado domains (Giulietti & Pirani, 1988;
Di Maio, 1996; Safford, 1999; Safford & Martinelli,
2000; Calió et al., 2008). Some examples of plant
taxa either restricted to areas within one of these
domains or disjunct between the two domains include: Wunderlichia (Asteraceae), Prepusa and Senaea
(Gentianaceae), Pseudotrimezia (Iridaceae), Crotalaria
claussenii (Leguminosae), Luxemburgia (Ochnaceae),
Aulonemia effusa, Chusquea pinifolia and Glaziophyton
mirabile (Poaceae), Bradea and Hindsia (Rubiaceae),
Physocalyx (Scrophulariaceae), Vellozia (Velloziaceae),
Stachytarpheta glabra (Verbenaceae), and Xyris (Xyridaceae).
Acknowledgements We wish to thank Jun WEN for
inviting us to contribute to this volume. We also thank
Douglas C. DALY, Robyn J. BURNHAM, and Hong
QIAN for their reviews. Luciano P. QUEIROZ and
Toby PENNINGTON provided valuable comments and
490
Journal of Systematics and Evolution
Vol. 47
No. 5
critical references. Juliana OTTRA helped digitalizing
the map. PF greatfully acknowledges Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico
(CNPq; Grant No. 200682/2006-7) and the Integrative
Life Sciences PhD Program from Virginia Commonwealth University for financial support. JRP is grateful
to CNPq for financial support.
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2009 Institute of Botany, Chinese Academy of Sciences