Corticolous Microlichens in Northeastern Brazil: Habitat
Differentiation Between Coastal Mata Atlântica, Caatinga and
Brejos de Altitude
Author(s): Marcela E. S. Cáceres, Robert Lücking, Gerhard Rambold
Source: The Bryologist, 111(1):98-117. 2008.
Published By: The American Bryological and Lichenological Society, Inc.
DOI: http://dx.doi.org/10.1639/0007-2745(2008)111[98:CMINBH]2.0.CO;2
URL: http://www.bioone.org/doi/
full/10.1639/0007-2745%282008%29111%5B98%3ACMINBH%5D2.0.CO
%3B2
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critical research.
Corticolous microlichens in northeastern Brazil: habitat
differentiation between coastal Mata Atlântica, Caatinga and
Brejos de Altitude
MARCELA E. S. CÁCERES
Universität Bayreuth, Lehrstuhl für Pflanzensystematik NWI, Abteilung Mykologie und Lichenologie, Universitätsstraße 30, 95440, Bayreuth, Germany.
Current address: Departamento de Micologia, Centro de Ciências Biológicas,
Universidade Federal de Pernambuco, 50670-420 Recife, PE, Brazil
e-mail: marcela.caceres@uni-bayreuth.de
ROBERT LÜCKING
Department of Botany, The Field Museum, 1400 South Lake Shore Drive,
Chicago, IL 60605-2496, U.S.A.
e-mail: rlucking@fieldmuseum.org
GERHARD RAMBOLD
Corresponding author: Universität Bayreuth, Lehrstuhl für Pflanzensystematik
NWI, Abt. Mykologie und Lichenologie, Universitätsstraße 30, 95440, Bayreuth,
Germany
e-mail: gerhard.rambold@uni-bayreuth.de
ABSTRACT. Based on a study of 22 sites in northeastern Brazil, including the three main
vegetation types, coastal Mata Atlântica (Zona da Mata), Caatinga and Brejos de Altitude
(rain forest enclaves in Caatinga areas), we studied the distribution and habitat preferences
of 456 crustose and microfoliose lichen species. Alpha-diversity ranged between three and
99 species per site, with Zona da Mata and Brejos de Altitude showing higher numbers
than Caatinga sites. Beta-diversity (dissimilarity) was highest between Zona da Mata sites
and, as a whole, the Zona da Mata showed the highest gamma-diversity, with a total of 334
species. Site ordination by non-metric multidimensional scaling (NMS), as well as cluster
analysis, both using Sørensen’s coefficient of dissimilarity, show that Zona da Mata and
Caatinga sites have distinctive lichen species compositions, with the isolated Brejos de
Altitude being more similar to coastal Zona da Mata than to Caatinga sites. Exposed Zona
da Mata sites have certain species in common with Caatinga sites but overall cluster with
the Zona da Mata sites. The transitional Agreste vegetation (one study site) also appears
transitional between Zona da Mata and Caatinga in its lichen species composition.
Indicator species analysis for each vegetation type was performed by applying a MonteCarlo test. Other than ten ubiquitous taxa (found in all three vegetation types), 59 taxa
were shared between Zona da Mata and Brejos de Altitude, 20 between Zona da Mata and
Caatinga, and none between Brejos de Altitude and Caatinga. Dissimilarity values of Zona
The Bryologist 111(1), pp. 98–117
Copyright E2008 by The American Bryological and Lichenological Society, Inc.
0007-2745/08/$2.15/0
Cáceres et al.: Microlichens in NE Brazil
99
da Mata versus Brejos de Altitude sites were high (0.77 or 23% shared species on average),
as were those of Zona da Mata versus Caatinga sites (average of 0.92 or 8% shared species).
Zona da Mata lichens had a higher proportion of Arthoniomycetidae (Arthoniales:
Arthoniaceae, Roccellaceae) and Chaetothyriomycetidae (Pyrenulales: Pyrenulaceae), as
well as Porinaceae and Thelotremataceae; frequently trentepohlioid photobionts,
predominantly transversely septate and/or narrow ascospores, and lack of lichen
substances. Brejos de Altitude lichens showed a higher proportion of Dothideomycetiae
(Trypetheliaceae) and Ostropomycetidae (Ostropales: Gomphillaceae and Graphidaceae),
as well as Pilocarpaceae; ascospores were predominantly thick-walled or muriform and
hyaline. Caatinga sites were dominated by Lecanoromycetidae (Lecanorales: Lecanoraceae;
Teloschistales: Physciaceae) and Pertusariales (Pertusariaceae); taxa were chiefly associated
with chlorococcoid photobionts, ascospores were megalosporous, non-septate and/or
brown, and showed a predominance of certain cortical substances (atranorin,
lichexanthone other xanthones, pulvinic acid derivates), as well as norstictic acid as
medullary substance.
KEYWORDS. Atlantic rain forest, Brazil, crustose and microfoliose lichens, Alagoas, Paraı́ba,
Pernambuco, Rio Grande do Norte, Sergipe.
¤
The Atlantic rain forest (Mata Atlântica) is one of the
three major rain forest blocks in the Neotropics
(Galindo-Leal & Câmara 2003; Morellato & Haddad
2000; Myers et al. 2000; Tabarelli et al. 2005;
Whitmore 1990) and it is among the 25 world
biodiversity hotspots (Costa et al. 2000; Myers et al.
2000). More than 95% of the original vegetation
cover of the Mata Atlântica in northeastern Brazil has
been eliminated or is strongly affected by human
activities, mainly agriculture (sugar cane
plantations), logging and the extension of urban
areas like Recife and Salvador (Myers et al. 2000;
Paciencia & Prado 2005; Silva Filho et al. 1998;
Tabarelli et al. 2005; Whitmore 1990). One of the
consequences of the extensive land use change since
the beginning of the Portuguese colonization in
Brazil five centuries ago is the increasing drought,
which subsequently affects the already reduced and
over-stressed rain forests remnants (Cáceres et al.
2000; Galindo-Leal & Câmara 2003; Paciencia &
Prado 2005; Silva Filho et al. 1998; Tabanez & Viana
2000).
The region of northeastern Brazil includes the
states of Maranhão, Piauı́, Ceará, Rio Grande do
Norte, Paraı́ba, Pernambuco, Alagoas, Sergipe and
¤
¤
Bahia. Of these, Rio Grande do Norte, Paraı́ba,
Pernambuco, Alagoas and Sergipe form the small
northeastern coastal states focused upon in this
study. The region has three main vegetation types:
(1) coastal Atlantic rain forest (Zona da Mata), (2)
Caatinga (Sertão) and (3) isolated montane Atlantic
rain forest remnants within the Caatinga and the
transitional Agreste vegetation, the so-called Brejos
de Altitude (Andrade-Lima 1954, 1961; Galindo-Leal
& Câmara 2003; Marcelli 1998; Rizzini 1977; Silva
Filho et al. 1998; Whitmore 1990). The Mata
Atlântica covers a narrow strip along the coast,
extending from Rio Grande do Norte in northeastern
Brazil to Rio Grande do Sul in southern Brazil,
becoming broader and covering the Serra da
Mantiqueira, Serra do Mar and Serra do Espinhaço at
the latitudes of Minas Gerais and São Paulo states. In
its northeastern part, it is characterized as a perennial
forest with a pronounced dry season, while its
southern part is more humid (Galindo-Leal &
Câmara 2003; Morellato & Haddad 2000; Tabarelli et
al. 2005; Whitmore 1990). The Caatinga is a dry
thorn-bush, in some parts desert-like vegetation,
while the Brejos de Altitude are Pleistocene rain
forest remnants, isolated from the coastal vegetation
100
THE BRYOLOGIST
111(1): 2008
and located within the Caatinga (Rodal 1998), in
areas of higher altitude (500–1100 m). As much as
95% of the original cover of the Atlantic rain forest
has been deforested in northeastern Brazil, and many
tree species have locally disappeared (Cardoso Silva
& Tabarelli 2000; FIDEM 1987; Galindo-Leal &
Câmara 2003; Myers et al. 2000; Ranta et al. 1998;
Tabanez & Viana 2000; Tabarelli et al. 2005;
Whitmore 1990).
Hitherto, no comprehensive lichen inventory
has been undertaken in northeastern Brazil, although
the major vegetation types are assumed to have high
lichen diversity, possibly near 1000 species within the
study region. Barros and Xavier-Filho (1972)
published a catalogue of lichens housed in the
herbarium of the Federal University of Pernambuco
in Recife (URM), but a large part of the lichen samples
cited in this compilation are from areas outside
northeastern Brazil, including Europe, and came to
the herbarium by exchange. Batista and collaborators
made extensive collections of foliicolous lichens in
the area (Silva & Minter 1995), but most of their
identifications were subsequently found to be
incorrect (Lücking et al. 1998, 1999). The most
recent lichen inventory for this area, including
a thorough revision of collections made by Batista
and co-workers, covered foliicolous lichens only,
reporting 191 species for Pernambuco state (Cáceres
1999; Cáceres & Lücking 2000; Cáceres et al. 2000;
Lücking et al. 1999). Except for a few large-scale
monographic treatments that mention a few
collections from the area (Ahti 2000; Brako 1991;
Frisch et al. 2006; Harris 1986, 1989; Kalb et al. 2000,
2004; Kashiwadani & Kalb 1993; Sparrius 2004;
Staiger 2002; Staiger & Kalb 1995, 1999; Tehler 1993;
Tibell 1996), and collections made by the German
lichenologist Klaus Kalb mostly in Bahia state (Kalb
1981, 1982a–d, 1983, 1984, 1987, 2001, 2004; Kalb &
Elix 1995), little is known about the corticolous
lichens of northeastern Brazil, in particular the
crustose and microfoliose species.
Apart from the lack of knowledge of the lichen
biota, much less is known about the distribution and
ecology of lichens within the area. Such knowledge is
indispensable to assess, for example, the feasibility of
using lichens as bioindicators of the impact of
deforestation and land use change. Foliicolous
lichens have demonstrated potential as bioindicators
of the impact of fragmentation on biodiversity in
Atlantic rain forest remnants in Pernambuco
(Cáceres et al. 2000), and since corticolous
microlichens are not restricted to evergreen rain
forests, their potential applications as bioindicators
are more extensive. While knowledge of tropical
lichen ecology is rudimentary, a few quantitative
studies have been published, including montane rain
forests in Colombia and Ecuador and lowland rain
forest and savannas in Venezuela, Guyana and
French Guiana (Cornelissen & Ter Steege 1989;
Komposch & Hafellner 1999, 2000, 2002, 2003;
Marcelli 1992; Martins 2006; Montfoort & Ek 1990;
Nöske 2004; Nöske & Sipman 2004; Wolf 1993).
Microlichens make up a significant part of the
diversity of lowland forests, but were identified to
species level only in a few studies (Komposch &
Hafellner 1999, 2000, 2002, 2003; Marcelli 1992;
Martins 2006).
In northeastern Brazil, a recent study dealing
with the diversity of corticolous lichens in three
Atlantic rain forest remnants (Pereira et al. 2005a–c)
was the first to assess microlichen diversity in
individual forest fragments. Expanding from that
study, the present paper is the first to examine the
distribution and habitat preferences of corticolous
microlichens across the three principal vegetation
zones in northeastern Brazil, based on the
identification of 456 species (Cáceres 2007).
MATERIAL AND METHODS
For the comparative analysis of the crustose and
microfoliose corticolous lichen biota in the three
vegetation types in northeastern Brazil, 22 localities
(Fig. 1) were selected, representing the coastal Mata
Atlântica or Zona da Mata (13 sites), transitional
Agreste (1 site), Caatinga (5 sites) and Brejos de
Altitude (3 sites). A detailed description of the study
area and collecting sites is given elsewhere (Cáceres
2007; Cáceres et al. 2007a, b).
Non-quantitative opportunistic sampling was
applied to each site as suggested by Sipman (1996).
At each site, lichens were collected from tree bark
along the main trail through the site. Trees were
inspected within a 20 m broad strip along both sides
of the corresponding trail, with a distance of about
Cáceres et al.: Microlichens in NE Brazil
101
Figure 1. Map of Brazil showing the five major geographic regions (A) and the location of the study area and sites (B). Three of
the 17 dots each indicate two close localities, and one indicates three localities, for a total of 22.
10–20 m between each tree. About 50–100 trees were
sampled at each site. Each lichen thallus recognized
as potentially distinct in the field and featuring
identifiable structures (ascomata, conidiomata,
soralia, isidia, etc.) was collected, amounting to a total
of 1–5(–10) thalli per tree and a total of 100–200
(–300) specimens per locality (see also Cáceres et al.
2007a, b). One site, the RPPN Fazenda São Pedro,
was sampled three times repetitively, for a separate
analysis comparing different sampling methods
(Cáceres et al. 2007b).
Methods and literature used for the
identification of the lichen material are given with
detail in Cáceres (2007). Most lichen samples were
duplicated and sets were deposited in URM, B and F.
For the statistical analysis, each species was
assigned an abundance score for each site, based on
the number of collections made: 0 5 absent, 1 5 rare
(1–3 collections), 2 5 intermediate (4–10
collections), and 3 5 abundant (.10 collections).
Alpha-diversity was calculated as the number of
species per site, while gamma-diversity was calculated
as the total number of species per vegetation type.
Beta-diversity, that is dissimilarity between sites, was
computed using the relative Sørensen coefficient of
dissimilarity (McCune & Mefford 1999; McCune et
al. 2002).
Lichen species composition at each site was used
to ordinate and classify sites by applying non-metric
multidimensional scaling (NMS) as ordination
method and cluster analysis based on the relative
Sørensen coefficient of dissimilarity as classification
method (McCune et al. 2002; McCune & Mefford
1999). Flexible beta 5 20.25 was used as the
102
THE BRYOLOGIST
111(1): 2008
clustering algorithm; this method resulted in tight
clusters similar to those obtained from Ward’s
method but contrary to the latter, flexible beta is
compatible with a distance matrix derived from
Sørensen’s coefficient of dissimilarity (McCune et al.
2002).
Indicator species analysis was performed to
detect species that can be classified as characteristic of
a given vegetation type. For that purpose, a MonteCarlo test was performed on the original frequency
(number of sites where species was present) and
abundance data (categorized number of collections
per site), that is the data were mixed randomly with
1000 repetitions, and it was tested whether the
observed data distribution deviated significantly
from the random distribution derived from the
Monte-Carlo test, i.e., whether a given species was
significantly more abundant and frequent within
a given vegetation type than expected by random
(McCune et al. 2002).
Lichen species unique to each of the three major
vegetation types (Atlantic rain forest, Brejos de
Altitude and Caatinga) were used to test whether the
observed frequency of selected character states
(systematic affinity, morphology, anatomy,
chemistry) among vegetation types differed
significantly from the expected frequency based on
the overall frequency of the character state assuming
random distribution. Observed versus expected
frequencies were compared within each vegetation
type across all states of a given character, and a ChiSquare test was used to determine statistical
significance of the observed differences. Twelve
characters were used with different sets of character
states (see Results for details).
The statistical analyses were carried out using
STATISTICATM 6.0 and PC-ORD 4.0 (McCune &
Mefford 1999).
RESULTS
Patterns of alpha-, beta- and gamma-diversity.
A total of 456 species of corticolous crustose and
microfoliose lichens were found in the three
vegetation types in northeastern Brazil. A complete
checklist and taxonomic treatment for the reported
taxa is published elsewhere (Cáceres 2007). The
number of species per site varied from three to 99
(Figs. 2, 3). The site with the highest number of
species (99) was the repetitively sampled RPPN
Fazenda São Pedro in the state of Alagoas; here, the
first trip resulted in 53 species and the two
subsequent trips produced an increase of 87%. The
highest species numbers for sites sampled one time
opportunistically were found for Brejos de Altitude,
which contributed 84 (Brejo dos Cavalos) and 73
species (Parque Municipal de Bonito), respectively.
Apart from RPPN Fazenda São Pedro, sites within
the Zona da Mata had slightly lower species numbers,
the richest being the Refúgio Ecológico Charles
Darwin (71) and the Estação Ecológica de Gurjaú
(60) in Pernambuco state. The three sites of exposed
secondary vegetation within the Zona da Mata,
RPPN Rosa do Sol, UFPE Campus, and the exposed
secondary vegetation at Gurjaú, showed little
variation in the number of species (16–19), while
only eight taxa were found at the exposed secondary
vegetation at Brejo dos Cavalos. One site, Estação
Ecológica de Tapacurá, was located in the transitional
Agreste region; it had 22 species. Within the
Caatinga, the number of species varied between 23
and 54 per site, with the largest number reported for
the most conserved Caatinga vegetation at IPA in
Caruaru. The two sites representing exposed
secondary Caatinga area, Garanhuns and the exposed
secondary vegetation at IPA, had 3–12 species.
Combining all sites within each of the three
main vegetation types, the Zona da Mata yielded
a total of 281 species, being the most diverse of the
three vegetation zones (Fig. 3). For the exposed
secondary Zona da Mata sites and the higher altitude
Zona da Mata forests, 43 and 25 taxa were found in
total, and the combined number for all Zona da Mata
sites, including exposed secondary sites, was 334. The
Brejos de Altitude localities represented the second
most diverse region of the study area, with a total of
136 species. The three sites representing Caatinga
vegetation comprised a total of 79 species, and the
two exposed secondary Caatinga sites yielded 15 taxa,
totaling 84 species for all five Caatinga sites. Because
of the different number of sample sites per
vegetation, total species numbers across vegetation
are not directly comparable; logarithmic
transformation of these numbers [S9 5 S/100 3
log(N)], where S9 5 logarithmically transformed
Cáceres et al.: Microlichens in NE Brazil
103
Figure 2. Alpha-diversity (number of species) per site. Sites arranged according to major vegetation types and subtypes
(anthropogenic variations), from high to low values for each type.
Figure 3. Variation in alpha-diversity across sites and gammadiversity (total number of species) per vegetation type. Box and
whiskers show mean, standard deviation (box) and min-max
(whisker); bold numbers indicate gamma-diversity per vegetation subtype (differentiating between closed forest and exposed
secondary vegetation), while thinner numbers indicate total
gamma-diversity for main vegetation types (specifically Zona
da Mata and Caatinga).
diversity index, S 5 original species number per
vegetation type, and N 5 number of sites per
vegetation type, results in S9 5 2.9 for Zona da Mata,
4.5 for Brejos de Altitude, and 1.2 for Caatinga,
indicating that the highest overall diversity is to be
expected in Brejos de Altitude vegetation (which is
supported by the higher average species numbers for
the two study sites).
Beta-diversity (Sørensen dissimilarity) in lichen
species composition between any two sites was
relatively high, with values ranging between 0.41 and
1.00 and a mean of 0.79 (Table 1). In other words,
any two sites shared between 0% and 59% of their
species, with a mean of 21%. When comparing Zona
da Mata sites only, the smallest dissimilarity value
between any two sites was 0.45, which means that a
maximum of 55% of the species was shared between
any two sites. The two sites representing Brejos de
Altitude had a dissimilarity of 0.56, meaning that
they shared 44% of the species. With respect to the
104
THE BRYOLOGIST
111(1): 2008
Table 1. Sørensen dissimilarity and percentage of similarity between sites (ranges and mean), arranged according to the three
main vegetation types and their anthropogenic variations.
Vegetation type
Dissimilarity (range)
Dissimilarity
(mean)
Similarity
(range)
Similarity
(mean)
Zona da Mata (0–100 m)
Zona da Mata (0–100 m exposed)
Zona da Mata (300–500 m montane)
Brejos de Altitude
Caatinga
Caatinga (exposed)
0.45–1.00
0.67–0.85
—
—
0.41–0.83
—
0.78
0.75
1.00
0.56
0.64
0.72
0–55%
15–33%
—
—
17–59%
—
22%
25%
0%
44%
36%
28%
All sites
0.41–1.00
0.79
0–59%
21%
three undisturbed Caatinga sites, the smallest
dissimilarity was 41% and the highest 83%, which
means 17–59% of the species were shared between
sites. Although mean similarity was highest between
Brejos de Altitude sites and lowest between Zona da
Mata sites, the differences were not statistically
significant (Kruskal-Wallis ANOVA).
Comparing sites across the three main
vegetation types, dissimilarity values of Zona da Mata
versus Brejos de Altitude sites were found to be
relatively high, with an average value of 0.77 or 23%
shared species (Table 2). Differences in species
composition of Zona da Mata versus Caatinga were
even more pronounced, with dissimilarity values
averaging 0.92 (8% shared species). Similarly high
dissimilarity values were found between sites
representing Brejos de Altitude and Caatinga. While
the average similarity of Zona da Mata versus Brejos
de Altitude is not different from the average between
Zona da Mata sites (22%) and the average for all sites
(21%), similarity of Zona da Mata and Brejos de
Altitude versus Caatinga sites is significantly lower
(8% vs. 22%, 44% and 36%, respectively). This
indicates that Caatinga lichen communities are more
distinct from both Zona da Mata and Brejos de
Altitude communities than Brejos de Altitude from
Zona da Mata communities.
Ordination and classification of sites. NMS
(non-metric multidimensional scaling) ordination,
based on lichen species composition at each site,
revealed a distinct pattern reflecting the three main
vegetation types and their anthropogenic disturbance
variations (Fig. 4). Sites representing closed Zona da
Mata vegetation in the upper and left portion of the
diagram are clearly differentiated against the
Caatinga sites in the lower right portion. The two
Brejos de Altitude sites are found at the upper left
extreme of this polarization axis, but fairly close to
the Zona da Mata sites. The exposed secondary sites
of the Zona da Mata (upper right portion of the
diagram) show affinities with both Zona da Mata and
Caatinga sites, but eventually cluster with Zona da
Mata sites (Fig. 5). The two montane Zona da Mata
sites at higher elevations do not cluster together and
also do not cluster with the two Brejos de Altitude
sites, suggesting distinct differences in their lichen
species composition compared to the latter. The
Agreste site (Tapacurá) falls intermediate between
the Zona da Mata and the Caatinga sites, reflecting its
transitional character. Contrary to the Zona da Mata
Table 2. Sørensen dissimilarity and percentage similarity between sites (ranges and mean), comparing sites across the three main
vegetation types.
Vegetation type
Dissimilarity
(range)
Dissimilarity
(mean)
Similarity
(range)
Similarity
(mean)
Zona da Mata vs. Brejos de Altitude
Zona da Mata vs. Caatinga
Caatinga vs. Brejos de Altitude
0.57–1.00
0.69–1.00
0.87–0.98
0.77
0.92
0.92
0–43%
0–31%
2–13%
23%
8%
8%
All sites
0.41–1.00
0.79
0–59%
21%
Cáceres et al.: Microlichens in NE Brazil
105
Figure 4. NMS ordination of the 22 sites. Arrowed lines indicate correlations of the main axes with humidity (precipitation
regime) and exposure (light level). M 5 Zona da Mata sites, S 5 montane Zona da Mata sites, B 5 Brejos de Altitude sites, A 5
Agreste site, C 5 Caatinga sites; black and gray dots indicate closed vegetation; white dots indicate exposed secondary vegetation.
sites, the exposed secondary Caatinga sites do not
cluster separately from the closed Caatinga sites, and
the exposed Brejo de Altitude site clusters together
with the Caatinga sites, far from the closed Brejos
sites, indicating that exposed vegetation near Brejos
is dominated by Caatinga lichens.
The cluster analysis of the 22 sites chiefly
supports the pattern observed in the NMS diagram,
with the formation of two major clusters (Fig. 5).
The first cluster unites all Zona da Mata sites, as well
as Brejos de Altitude and Agreste sites, while the
second cluster is comprised of the Caatinga and the
exposed Brejos site. One exception is the Caatinga
site Itabi, which in the ordination diagram (Fig. 4) is
the Caatinga site closest to the Zona da Mata sites
and in the cluster analysis clusters with the latter; this
site is situated very close to Zona da Mata vegetation
and therefore its lichen species composition appears
to include a portion of Zona da Mata lichens. Within
the large Zona da Mata cluster, there are two
subgroups: one includes the two Brejos de Altitude
sites and the high diversity Zona da Mata sites
(Charles Darwin, Gurjaú, RPPN São Pedro and Serra
Itabaiana), while the second includes the three
106
THE BRYOLOGIST
111(1): 2008
Figure 5. Cluster analysis of the 22 sites. M 5 Zona da Mata sites, S 5 montane Zona da Mata sites, B 5 Brejos de Altitude sites,
A 5 Agreste site, C 5 Caatinga sites; black and gray dots indicate closed vegetation; white dots indicate exposed
secondary vegetation.
Cáceres et al.: Microlichens in NE Brazil
Figure 6. Number of lichen species unique for, and shared
between, each of the three main vegetation types. Numbers in
boldface in white circles indicate number of shared species
between vegetation types, and numbers in parentheses below
indicate total number of species for combined vegetation types.
exposed secondary sites, the Agreste and the Caatinga
site, and all low diversity Zona da Mata sites. This
suggests that low diversity, transitional and exposed
sites all share a number of possibly common,
widespread species with broader ecological amplitude
(otherwise they would not cluster together), while
the high diversity sites share more ecologically
restricted and rare taxa. Still, the structure of the
cluster diagram shows overall high dissimilarity
between individual sites, even within smaller clusters.
Vegetation types and their indicator species.
Among the 456 corticolous crustose and microfoliose
lichen species found in the present study, only ten
were shared among all three main vegetation types:
Dyplolabia afzelii, Lecanora helva, Malcolmiella
fuscella, M. gyalectoides, M. leptoloma, M. vinosa,
Phaeographis brasiliensis, Trypethelium ochroleucum,
T. subeluteriae and T. tropicum. Fifty-nine taxa were
shared between Zona da Mata and Brejos de Altitude,
20 between Zona da Mata and Caatinga and none
between Brejos de Altitude and Caatinga, supporting
the affinity of Brejos de Altitude with Zona da Mata
rather than Caatinga in terms of lichen species
composition. A total of 366 species were unique to
one zone, either Zona da Mata (245), Brejos de
Altitude (67) or Caatinga (54) (Fig. 6). Genera
containing more than one species and unique to the
Zona da Mata or particularly well-represented there
are Arthonia, Arthothelium, Bactrospora, Bapalmuia,
Bacidiopsora, Bathelium, Carbacanthographis,
107
Coccocarpia, Cresponea, Crocynia, Cryptothecia,
Enterographa, Fellhanera, Herpothallon, Letrouitia,
Myriotrema, Opegrapha and Sarcographa. Unique to
Brejos de Altitude or particularly well represented
there are Astrothelium, Calopadia, Echinoplaca,
Eugeniella, Hemithecium, Lopezaria, Sagenidium,
Trichothelium and Vainionora. Genera restricted to
Caatinga or most commonly found there include
Baculifera, Chrysothrix, Cratiria, Dirinaria, Hafellia,
Lecanographa, Lecanora, Maronina, Ochrolechia,
Pertusaria, Physcia, Pyxine, Rinodina and
Stigmatochroma.
Although 245 lichen species are unique to the
Zona da Mata, none is significantly indicative for this
type of vegetation (Table 3). This is due to the fact
that the Zona da Mata sites included in the study
(13) outnumbered the Brejos de Altitude (3) and
Caatinga sites (5), so the deviations observed from
expected indicator values (IV) are too small to
produce significant p-levels. For example, a species
present at all 13 Zona da Mata sites but absent from
Brejos de Altitude and Caatinga would have an
expected frequency within the Zona da Mata of 132/
22 5 7.7 if randomly distributed, and the observed
frequency of 13 would be within the 95% confidence
interval of that value. On the other hand, a species
present at all five Caatinga sites would only have an
expected random Caatinga frequency of 52/22 5
1.14; in that case, the observed frequency lies outside
the 95% confidence interval and the difference
becomes significant at the 5% level. Accordingly, the
Brejos de Altitude sites have 24 statistically significant
indicator species and the Caatinga sites have eight
(Table 3).
The aspect of characteristic Zona da Mata,
Brejos de Altitude and Caatinga lichen species is very
different from each other (Figs. 7–9). Among the
lichen species unique to the Zona da Mata, there is
a higher proportion of subclasses Arthoniomycetidae
(Arthoniales: Arthoniaceae, Roccellaceae) and
Chaetothyriomycetidae (Pyrenulales: Pyrenulaceae),
as well as the families Porinaceae and
Thelotremataceae (Table 4). Because of the
aforementioned explanation, this difference is not
significant (Chi-Square test). Brejos de Altitude have
a significantly higher proportion of
Dothideomycetiae (Trypetheliaceae) and
108
THE BRYOLOGIST
111(1): 2008
Table 3. Indicator lichen species analysis for the three main vegetation types in northeastern Brazil. Columns 2–4 give the combined
abundance/frequency score for each species within each vegetation type; IV indicates observed and expected indicator values
(combined abundance/frequency scores) for the vegetation type in which the species is relatively most common. IV values for Zona da
Mata are not statistically significant because of the high proportion of study sites belonging to this vegetation type (see text).
Zona da Mata
Brejos
Caatinga
Obs. IV
Exp. IV
p-level
Zona da Mata
Malcolmiella psychotrioides
Pyrenula mamillana
Malcolmiella badimioides
Letrouitia domingensis
Graphis glaucescens
Letrouitia vulpina
Pyrenula nitidula
Cryptothecia striata
Malcolmiella granifera
Coenogonium subdentatum
Arthonia bessalis
Phaeographis crispata
53
40
53
40
33
33
33
27
27
27
27
27
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
53.3
40.0
53.3
40.0
33.3
33.3
33.3
26.7
26.7
26.7
26.7
26.7
30.7
27.2
31.0
28.1
26.6
26.9
27.1
23.8
24.7
25.3
25.1
25.2
0.100
0.103
0.107
0.127
0.250
0.292
0.299
0.417
0.445
0.489
0.492
0.500
Brejos de Altitude
Chapsa platycarpella
Herpothallon rubrocinctum
Byssoloma chlorinum
Byssoloma leucoblepharum
Byssoloma aff. meadii
Calopadia pruinosa
Diorygma reniforme
Echinoplaca leucotrichoides
Malcolmiella hypomela
Phaeographis kalbii
Trichothelium horridulum
Coenogonium geralense
Chapsa dilatata
Malcolmiella gyalectoides
Malcolmiella leptoloma
Porina nucula
Malcolmiella atlantica
Coenogonium strigosum
Dyplolabia afzelii
Phaeographis haematites
Trypethelium tropicum
Laurera megasperma
Malcolmiella fuscella
Coenogonium pyrophthalmum
5
0
0
0
0
0
0
0
0
0
0
0
11
4
2
3
2
6
8
10
1
0
0
0
84
95
100
100
96
100
100
100
100
100
100
94
73
78
82
85
86
76
71
71
70
47
48
47
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
1
0
8
0
0
0
84.3
94.9
100
100
95.7
100
100
100
100
100
100
93.7
73.2
77.6
82.2
84.9
85.7
76.3
70.6
71.4
69.8
46.9
47.9
46.9
28.9
21.4
18.3
18.6
21.1
18.6
18.6
18.6
18.5
18.3
18.2
21.4
29.2
28.9
27.9
26.3
24
28.4
30.6
28.4
28.5
17.8
17.4
18.1
0.003
0.004
0.005
0.005
0.005
0.005
0.005
0.005
0.005
0.005
0.005
0.007
0.008
0.010
0.010
0.010
0.011
0.019
0.023
0.027
0.036
0.049
0.049
0.050
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
83
67
50
50
67
50
43
42
83.3
66.7
50
50
66.7
50
43.1
41.7
27.6
24.8
22.4
21.8
25.1
22.1
24.5
25.1
0.006
0.022
0.024
0.024
0.026
0.026
0.051
0.060
Caatinga
Pyrrhospora haematites
Baculifera pseudomicromera
Pertusaria flavens
Maronina multifera
Haematomma persoonii
Lecanora hypocrocina
Dirinaria leopoldii
Pertusaria quassiae
Cáceres et al.: Microlichens in NE Brazil
109
Figure 7. Selected lichen species characteristic of the coastal Mata Atlântica (Zona da Mata) vegetation in northeastern Brazil: A.
Arhonia bessalis. B. Coenogonium subdentatum. C. Cryptothecia striata. D. Graphis glaucescens. E. Letrouitia domingensis. F.
Malcolmiella badimioides. G. Phaeographis crispata. H. Pyrenula nitidula.
110
THE BRYOLOGIST
111(1): 2008
Figure 8. Selected lichen species characteristic of the Brejos de Altitude vegetation in northeatsern Brazil: A. Chapsa platycarpella.
B. Diorygma reniforme. C. Dyplolabia afzelii. D. Laurera megasperma. E. Lopezaria versicolor. F. Phaeographis kalbii. G. Sagenidiopsis
undulata. H. Trichothelium horridulum.
Cáceres et al.: Microlichens in NE Brazil
111
Figure 9. Selected lichen species characteristic of the Caatinga vegetation in northeastern Brazil: A. Baculifera pseudomicromera. B.
Cratiria lauricassiae. C. Dirinaria leopoldii. D. Haematomma persoonii. E. Maronina multifera. F. Ochrolechia africana. G. Pertusaria
quassiae. H. Pyrrhospora haematites.
112
THE BRYOLOGIST
111(1): 2008
Table 4. Differences in the relative proportion of lichen species belonging to different higher taxa and showing different
morphological, anatomical, and chemical features, between the three main vegetation types (Chi-Square test). Predominant taxa
and features are indicated in boldface. TTT 5 highly significant (p , 0.001), T 5 significant (p , 0.05), (T) 5 tendential (p ,
0.1), and (–) 5 not significant.
Subclass
Order/Suborder
Family
Thallus type
Photobiont
Ascomatal type
Vegetative dispersal
Ascospore type
Ascospore septa
Ascospore shape
Ascospore color
Chemistry
Zona da Mata
p-level
Brejos de Altitude
p-level
Caatinga
p-level
Arthoniomycetidae
Chaetothyriomycetiae
Arthoniales
Ostropales
Pyrenulales
Arthoniaceae
Porinaceae
Pyrenulaceae
Roccellaceae
Thelotremataceae
squamulose
trentepohlioid
perithecia
(–)
Dothideomycetidae
Ostropomycetidae
Ostropales
T
Lecanoromycetidae
T
T
TTT
(–)
Gomphillaceae
Graphidaceae
Pilocarpaceae
Trypetheliaceae
T
Lecanorales
Pertusariales
Teloschistales
Lecanoraceae
Pertusariaceae
Physciaceae
(–)
T
(–)
byssoid
[none]
lirellae
(–)
(–)
(–)
(T)
TTT
(–)
isidia
[none]
transverse
narrow
[none]
nil
psoromic acid
(–)
(–)
(–)
(–)
(–)
(–)
[none]
thick-walled
muriform
broad
hyaline
nil
(–)
(–)
T
(–)
(–)
(–)
microfoliose
chlorococcoid
apothecia
stromata
soredia
megalosporous
nonseptate
broad
brown
atranorin
lichexanthone
norstictic acid
pulvinic acids
xanthones
(–)
Ostropomycetidae (Ostropales: Gomphillaceae and
Graphidaceae), as well as Pilocarpaceae (p , 0.05),
while Lecanoromycetidae (Lecanorales:
Lecanoraceae; Teloschistales: Physciaceae) and
Pertusariales (Pertusariaceae) are the predominant
subclasses, orders and families found in Caatinga (p
, 0.001).
The predominant thallus type is squamulose for
Zona da Mata, byssoid for Brejos de Altitude and
microfoliose for Caatinga, but the observed
differences are significant for the Caatinga only
(Table 4). Lichens in the Zona da Mata frequently
have trentepohlioid photobionts (p , 0.05), while
those in Caatinga vegetation are associated with
chlorococcoid photobionts (p , 0.001). Vegetative
dispersal by isidia is more common within the Zona
da Mata, while Caatinga lichens more frequently
disperse by soredia, but the difference is not
significant. The predominant ascomatal types are
perithecia for Zona da Mata, lirellae for Brejos de
TTT
(T)
T
T
(–)
T
TTT
Altitude and apothecia and stromata for Caatinga,
but the differences are not significant. Ascospores are
predominantly transversely septate and/or narrow in
lichens of the Zona da Mata (not significant), thickwalled or muriform (p , 0.05) and hyaline in those
of Brejos de Altitude, while megalosporous (largespored) non-septate and/or brown (all p , 0.05) in
Caatinga species. Both Zona da Mata and Brejos de
Altitude lichens have no predominant secondary
substances, except for psoromic acid in the first, but
Caatinga lichens show a highly significant
predominance of atranorin, lichexanthone and other
xanthones, as well as pulvinic acid derivatives, as
cortical substances, and norstictic acid as a medullary
substance.
DISCUSSION
Few studies are available in which lichen species
diversity, specifically microlichens, has been assessed
for tropical vegetation. Also, the available studies all
Cáceres et al.: Microlichens in NE Brazil
used somewhat different sampling techniques,
included different forest strata and identified the
lichens to various taxonomic levels depending on
growth form. While several studies included canopy
lichens collected with tree-climbing techniques, often
only macrolichens were identified to species level.
Comparisons of the numbers found in this study
with other tropical sites are therefore difficult,
especially as a separate analysis of our data (Cáceres
et al. 2007b) showed that opportunistic, repetitive
and quantitative sampling can yield different species
numbers, with opportunistic sampling
underestimating lichen diversity by as much as 50%.
Defining ‘‘site’’ as a single, continuous study
area of about 1–5 ha in size, montane rain forests in
Costa Rica, Colombia and Ecuador had 32–51
macrolichens and an undetermined number of
microlichen species per site (Holz & Gradstein 2005;
Nöske 2004; Nöske & Sipman 2004; Wolf 1993); in
these cases, microlichens were left mostly
undetermined or determined to genus level only.
Montane forests are quite different from the
relatively dry and hot northeastern Atlantic rain
forest and Caatinga and generally have higher lichen
biomass but fewer species, especially microlichens,
than lowland forests. Lowland sites were investigated
in Venezuela by Komposch and Hafellner (1999,
2000, 2002, 2003), in Guyana by Cornelissen and Ter
Steege (1989), in French Guiana by Montfoort and
Ek (1990), and in Brazil by Aptroot (2002), Marcelli
(1992) and Martins (2006). These workers reported
mostly macrolichens and left most of the
microlichens unidentified, except for Aptroot (2002),
Komposch and Hafellner (1999, 2000, 2002, 2003),
Marcelli (1992) and Martins (2006), who counted
161–268 species at a single site, including all lichen
groups and forest strata. The latter numbers are
consistent with the study by Aptroot (1997, 2001)
who identified 173 lichen species on a single tree in
Papua New Guinea, and recent inventories in Costa
Rica, with about 300 corticolous lichen species each
found at a lowland and a lower montane rain forest
site (Lizano et al., in prep.; Moncada et al., in prep.).
Based on these figures and the discussed
uncertainties, the number of species per site observed
in this study (as many as 84 for opportunistic and 99
for repetitive sampling) appear moderate, especially
113
compared to the figures by Aptroot (1997, 2001,
2002), Komposch and Hafellner (1999, 2000, 2002,
2003) and Martins (2006), who studied comparable
vegetation types. On the other hand, the figures are
similar to those reported by Pereira et al. (2005a–c)
for three Atlantic rain forest remnants (including one
site also studied here: Gurjaú), with 37, 45 and 53
species, respectively; these authors used the same
opportunistic sampling technique. Assuming that
opportunisting sampling underestimates lichen
diversity by as much as 50% (mostly because
inconspicuous, cryptic and frequently sterile taxa are
not sampled; Cáceres et al. 2007b), and assuming that
sampling of the forest understory only recovers a part
of the diversity (25–75% depending on forest
structure), the actual species numbers are probably
2–3 times as high as observed, which would result in
estimated numbers, for the richest sites, of 180–250
species, within the same range as those reported by
the aforementioned papers. Indeed, in a separate
study using a quantitative approach sampling 47
trees in the understory at one site, a total of 150
species was found (Cáceres et al. 2007b), while
opportunistic one-time sampling of that site yielded
53 species and repetitive sampling 99 species.
Another explanation for the moderate species
numbers is the potential effect of forest
fragmentation, as observed in other organisms such
as pteridophytes, trees and birds (Machado &
Fonseca 2000; Paciencia & Prado 2005; Tabanez &
Viana 2000). In studies in Amazonia, it has been
shown that rain forest fragmentation specifically kills
mature and large trees (Laurance et al. 2000), and
since certain microlichen groups, such as
Thelotremataceae (Rivas Plata et al. 2007), are
dependent on such trees, fragmentation will
eventually eliminate such lichen species. The
stochastic component of such processes would result
in higher dissimilarity between fragments, which is
supported by the high beta-diversity values between
sites observed in our study. High beta-diversity was
more pronounced between Zona da Mata sites,
compared to Caatinga and Brejos de Altitude sites,
which agrees with the notion that anthropogenic
fragmentation is more pronounced in the Zona da
Mata, which naturally constitutes a continuous rain
forest area (Machado & Fonseca 2000; Silva et al.
114
THE BRYOLOGIST
111(1): 2008
1998), whereas Brejos de Altitude sites have been
naturally isolated during geological times; the latter
are considered ‘‘Pleistocene refugia,’’ where species
richness and composition were not significantly
disturbed by the unfavorable climate conditions
affecting their surrounding areas (Rodal 1998;
Whitmore 1990). Caatinga lichens are more adapted
to exposed conditions, for example, by frequently
producing secondary cortical substances as
demonstrated here, and hence less affected by
anthropogenic disturbances than closed rain forest
lichens. It can therefore be concluded that specifically
in the Zona da Mata, forest fragmentation
stochastically reduces lichen diversity within
individual fragments, depending on the impact level,
and at the same time increases beta-diversity between
fragments. This underlines the need for protection of
many different forest fragments in order to conserve
high biodiversity (Machado & Fonseca 2000;
Paciencia & Prado 2005; Tabanez & Viana 2000).
Our study confirms findings of other studies in
both temperate and tropical regions that different
vegetation types support different lichen
communities (Burgaz et al. 1994; Johnson 1981;
Komposch & Hafellner 2003; Wolf 1993). In our
case, strong differences were found between Zona da
Mata and Caatinga sites, not only at different
taxonomic levels but also regarding certain
morphological, anatomical and chemical characters
and character states. Because such characters often
correlate with certain taxonomic levels, their
evaluation as potential adaptations is limited. On the
other side, the presence of predominant characters
and character states in a speciose clade restricted to
a certain vegetation type suggests that such characters
can be considered preadaptations. In the present
study, we found a distinct shift from
Arthoniomycetidae, Chaetothyriomycetidae,
Dothideomycetidae and Ostropales, with
predominantly trentepohlian photobiont,
squamulose-byssoid, often isidiate thalli lacking
secondary substances, perithecia or perithecioid
ascomata, and septate, hyaline ascospores,
dominating Zona da Mata communities, towards
Lecanoromycetidae (in particular Lecanoraceae and
Physciaceae) and Pertusariales, with chlorococcoid
photobionts, often sorediate thalli producing a wide
array of cortical substances (atranorin, lichexanthone
and other xanthones, pulvinic acid derivatives),
apothecia, and often non-septate and/or dark brown
ascospores, characterizing Caatinga communities.
Most of the latter characters, in particular cortical
substances and pigmented ascospores, are of
advantage in an environment characterized by high
solar insolation and extended drought. Therefore,
certain similarity exists between Zona da Mata
lichens from exposed secondary or canopy
microhabitats and Caatinga communities, although
overall they cluster with closed Zona da Mata
communities. An interesting case is the abundant
and widespread Pyrrhospora russula sensu lato, which
was found at exposed Brejos de Altitude sites and on
fallen canopy branches, as well as abundantly in the
Caatinga. Recent revision (Kalb, pers. comm. 2006)
divides the taxon into two species, P. haematites with
norstictic acid and P. russula with fumarprotocetraric
acid (Cáceres 2007). While P. haematites included all
Caatinga and exposed Brejos collections (which are
dominated by Caatinga lichens), P. russula was only
found on a fallen canopy branch in a Brejos de
Altitude site, underlining the difference between the
two vegetation types. The fact that Brejos de Altitude
sites are much more similar to Zona da Mata sites,
although they are located within Caatinga vegetation,
supports their interpretation as isolated Pleistocene
remnants of the Atlantic rain forest (Rodal 1998;
Whitmore 1990).
Only ten (2%) of the reported 456 taxa are
shared between all three vegetation types, which
means that each vegetation type contributes
substantially to the overall lichen diversity of
northeastern Brazil. The relatively low number of
species shared between Zona da Mata and Brejos de
Altitude sites suggests that, apart from the
interpretation of the latter as Pleistocene refugia,
major climatic differences exist between the two
types, Brejos de Altitude being more similar to
montane rain forests in their precipitation regime
(Rodal 1998). This is true even if the overall altitude
of the studied Brejos does not exceed 800 m, because
of the so-called Massenerhebungseffekt (‘‘mass
elevation effect’’), that compresses altitudinal
zonation of vegetation belts in low mountains close
to coastal areas (Grubb 1971). Although none of the
Cáceres et al.: Microlichens in NE Brazil
taxa reported for the Zona da Mata is significantly
indicative for that vegetation, because of the high
number of sites compared to other vegetation types,
many are representative for this biome. Most
Arthonia, Coenogonium, Malcolmiella and Porina
species are restricted to the Zona da Mata, and other
exclusive genera and species include Letroutia
domingensis, L. vulpina, Phaeographis crispatula,
Pyrenula mamillana and P. nitidula, among others.
Brejos de Altitude sites are characterized by a high
number of indicative species, including Lecanactis
epileuca, Sagenidiopsis undulata and Lopezaria
versicolor, the latter being a typical montane taxon.
Baculifera spp., Cratiria spp., Dirinaria spp.,
Haematomma persoonii, Lecanora spp., Maronina
multifera, Pertusaria spp. and Pyrrhospora haematites,
are significant indicator species for Caatinga sites.
Although indicative for these vegetation types, most
of these species are widespread in the tropics and
found in similar habitats, such as the Amazon
lowland rain forest (Zona da Mata lichens), the lower
Andes (many Brejos de Altitude lichens) and dry
forests and savannas in Central and South America
and the Cerrado in central Brazil (most Caatinga
lichens). Among the 456 species found in the study
area, only 18 (4%) are new and potentially endemic,
almost all found in Zona da Mata and Brejos de
Altitude sites (Cáceres 2007). Thus, while each site
and vegetation type substantially contributes to the
overall lichen diversity in the study area, the
taxonomic contribution of that area to neotropical
lichen diversity is relatively low.
ACKNOWLEDGMENTS
The work was supported by a Ph.D. grant to the first author
from the Deutscher Akademischer Austauschdienst (DAAD).
The first author thanks Leonor Costa Maia and her staff at the
Departamento de Micologia, Centro de Ciências Biológicas,
Universidade Federal de Pernambuco, for logistic and organizational support in order to access the localities sampled.
Franciso Quintella and his wife, owners of the RPPN Fazenda
São Pedro, are warmly acknowledged for their help during the
repeated visits to the site. Tatiana Gibertoni provided welcome
company and transportation during visits to several localities.
Drs. André Aptroot, Klaus Kalb and Harrie Sipman assisted in
the identification or confirmation of certain lichen groups. Dr.
Luciana Zedda is thanked for revising the manuscript and
giving some useful suggestions concerning the statistical
analyses.
115
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