Download The genetic diversity of Myrciaria floribunda

Journal of Tropical Ecology (2007) 23:361–367. Copyright © 2007 Cambridge University Press
doi:10.1017/S0266467407004099 Printed in the United Kingdom
The genetic diversity of Myrciaria floribunda (Myrtaceae) in Atlantic Forest
fragments of different sizes
Edivani Villaron Franceschinelli∗1 , Giuliana Mara Patrı́cio Vasconcelos†, Elena Charlotte Landau‡,
Kátia Yukari Ono§ and Flávio Antonio Maes Santos#
∗
Departamento de Biologia Geral ICB1, Universidade Federal de Goiás, Campus Samambaia, Goiânia, GO 74.001-970, Brazil
† BR 010, KM 15, Parada e Hotel Cricabom, Dom Eliseu – PA 68.633-000, Brazil
‡ Departamento de Botânica ICB, Universidade Federal de Minas Gerais, Belo Horizonte, MG 3127010, Brazil
§ Instituto Sócio-Ambiental, São Paulo SP 01238-001, Brazil
# Departamento de Botânica, IB, Universidade Estadual de Campinas, SP 13.083-970, Brazil
(Accepted 2 March 2007)
Abstract: The genetic diversity of Myrciaria floribunda, a common Atlantic Forest tree, was investigated in six
populations located in two small fragments (10 and 18 ha), two medium-sized fragments (36 and 44 ha) and one
large fragment (3003 ha). Two populations occur in the large fragment. It is expected that smaller fragments should
have lower genetic diversity and higher inbreeding. Distances between fragments varied from 0.66 to 10 km. On
average 32 young trees smaller than 20 cm basal girth were sampled in each population. Allozyme electrophoresis
was carried out, and six loci were scored. The effective number of alleles was lower for populations of the two small
fragments (1.46 and 1.51) and higher for populations of the large (1.62 and 1.71) and medium ones (1.69 and 1.84).
Small fragments showed lower values of expected and observed heterozygosities than large and medium fragments.
Most of the genetic variability occurs within populations, and there was a moderate genetic variation among them
(θ̂ p = 0.097). Our findings show a tendency of lower genetic diversity within small and isolated fragments and higher
genetic differentiation among them. But, few correlations between genetic diversity indices and fragment features (size
and isolation) were significant.
Key Words: Brazil, habitat loss, small spatial scale, tropical tree
INTRODUCTION
Forest fragmentation may cause loss of genetic diversity
within populations and disruption of gene flow among
populations or subpopulations, leading to depletion of
genes that may have adaptive importance (Barrett & Kohn
1991). Habitat fragmentation may decrease reproductive
fitness, disease resistance and population adaptation to
new environments increasing susceptibility to extinction
(Heywood & Stuart 1994, Lienert et al. 2002). Studies
showing the effect of habitat loss and isolation on the
genetic diversity and gene flow of native species are recent
(Bacles et al. 2006, Culley & Grubb 2003, Foré & Guttman
1999, Gonzalez-Astorga & Nunez-Farfan 2001, Hall
et al. 1996, Lienert et al. 2002, Prober & Brown 1994,
Tomimatsu & Ohara 2003). Some of those studies have
1
Corresponding author. Email: [email protected]
been done with native tropical trees (Aldrich & Hamrick
1998, Colevatti et al. 2001, Dayanandan et al. 1999, Dick
2001, Gillies et al. 1999, Hall et al. 1996, Schneider et al.
2003, White et al. 1999). Although many tropical tree
populations occur at very low densities and may become
isolated after fragmentation, little or no genetic diversity
difference has been found between populations of large
and small fragments (Lowe et al. 2005). The loss of genetic
diversity in tree species is not easily detectable, because
they may have originated from mating that occurred
before habitat isolation. However, information on the
genetic status of native trees that occur in fragmented
habitat is important for conducting conservation and
reforestation programmes.
In Brazil, the Atlantic forest has lost 93% of its
primary cover. Its remnants are composed of many small
fragments (1–10 ha), several medium-size (more than
30 ha) and a few continuous areas of forest (Tabarelli et al.
1998). However, few studies have been published on the
362
effect of fragmentation on genetic diversity of Brazilian
Atlantic forest trees (Auler et al. 2002, Salgueiro et al.
2004, Seoane et al. 2002). Those studies were carried out
in a large-scale area, which makes difficult comparative
analysis. According to Aguari (2001), the Atlantic Forest
was continuous in the study site until 1910, when
human activities increased in the area with logging,
corn and bean plantations. The main timber exploited
was Araucaria angustifolia. The deforestation became
more intense after 1950, due to timber exploitation
and plantation of exotic Pinus species. At this time, the
isolated deforested areas increased in size and number
and connected, resulting in the first forest fragments.
Those fragments decreased in size until 1985, when
timber exploitation and the expansion of agriculture in
the area decreased. Nowadays, several fragments are well
conserved but others undergo selective logging and cattle
grazing. The aim of this study was to assess the variation of
population genetic diversity of a tree species within large,
medium, and small fragments at a small spatial scale of
about 10 km2 . It was conducted in fragments of Atlantic
Forest that occur in high altitude (montane forest), located
in Southern Minas Gerais State.
Myrciaria floribunda (West ex Willdenow) Berg is a
common tree species of the Atlantic Forest (Sobral 1993).
It may occur in wet forest of Central and South America. It
grows slowly and may reach 20 m in height. The species
is easy to identify by its whitish bark. Myrciaria floribunda
is pollinated by bees and its seeds are dispersed mainly by
birds (pers. obs.). It is unknown how fragmentation affects
those animals and consequently M. floribunda gene flow
among forest fragments.
Six populations from five forest fragments were
analysed. Two of them are within a quite large fragment
(3003 ha), two are in small isolated fragments (10 and
18 ha), and two are in medium-sized fragments (36 and
44 ha). One of the medium fragments is connected to the
large fragment. Only leaves of younger plants (basal girth
< 20 cm) were collected to increase the chances that the
sampled plants were produced after fragmentation. We
hypothesize that populations of small isolated fragments
have lower genetic diversity than others. Small isolated
fragments are expected to have smaller population size,
low genetic variation, increased interpopulation genetic
divergence due to increased random drift, elevated
inbreeding and reduced gene flow.
METHODS
Study site
The study area is located in Serra da Mantiqueira,
southern Minas Gerais State, in the municipalities of
Camanducaia and Gonçalves, Brazil (Figure 1). The
EDIVANI VILLARON FRANCESCHINELLI ET AL.
altitude of the studied fragments is between 1500 and
1800 m and the predominant vegetation type is wet
montane forest. The matrix surrounding the studied
fragments is composed of small farms with pasture, potato
and carrot fields. There are no M. floribunda trees in the
surrounding matrix.
Five fragments were included in the study, one large
and four smaller (M1, M2, S1, and S2) (Figure 1, Table 1).
Distances between them varied from 0.66 to 10 km. Two
distinctive areas, that are 1.18 km apart (L1 and L2), were
sampled in the large fragment. L1 area seems to be well
preserved, but there is evidence of earlier selective logging.
The landowner has a few cattle feeding inside the forest
during the dry season, which may affect the understorey
plants. L2 area seems better preserved than L1 and it has
no indication of recent grazing or logging.
M1 fragment covers 44 ha and is not very far from
the largest fragment (1.48 km). It has evidence of cattle
grazing and selective logging. M2 is 36 ha and is
linked to the large studied fragment through a natural
corridor of 100 × 30 m (Figure 1). This fragment had
been disturbed with selective logging and grazing until
2000, when the new landowner protected it from further
disturbance.
The two small isolated fragments provide strong
evidence of grazing and logging. S1 is 18 ha and it is close
to a narrow expansion of the largest fragment (0.66 km).
S2 fragment is the most isolated and disturbed. It covers
20 ha, including 10 ha of primary forest, and 10 ha of an
old Pinus plantation.
Leaves of 28 to 36 plants were collected from the
interior of each fragment within an area of about 3 ha.
The total sample size was 195 plants. Data on girth at tree
base were collected for the sampled plants. Basal girth
measure was preferred to girth at breast height, since
many trees sampled were smaller than 1.30 m height.
Only young plants smaller than 20 cm bg (basal girth)
were sampled in order to focus on the generational cohort
expected to bear genetic impacts of forest fragmentation.
Plant density data were collected along one transect of
50 × 20 m in each studied area.
Allozyme analyses
The leaf material was transported in liquid nitrogen
(−196 ◦ C) from the field to the Universidade Federal
de Minas Gerais and stored at −80 ◦ C until enzyme
extraction. A small piece of each leaf was ground in
liquid nitrogen and the powdered tissue was mixed
with extraction buffer number one of Alfenas et al.
(1998) and absorbed onto filter paper wicks. Allozyme
electrophoresis was carried out on horizontal 13%
starch gel. Twenty enzyme systems were screened
with three electrophoretic buffers. Five enzyme systems
Genetic diversity in Atlantic Forest fragments
363
Figure 1. Map of the sampled fragments in the municipalities of Camanducaia and Gonçalves, Minas Gerais State, Brazil.
showed simple banding patterns and could be reliably
scored: uridine diphosphoglucose pyrophosphorylase
(UGPP, EC 2.7.7.9), isocitrate dehydrogenase (IDH, EC
1.1.1.41), glucose-6-phosphate dehydrogenase (G6PDH,
EC 1.1.1.49), triose-phosphate isomerase (TPI, EC
5.3.1.1) and aspartate aminotransferase (GOT EC
2.6.1.1). Uridine diphosphoglucose pyrophosphorylase,
IDH, and G6PDH were resolved on a morpholine citrate
buffer system at pH 6.5 (Alfenas et al. 1998). Aspartate
aminotransferase and TPI were assayed on a lithium
borate buffer at pH 8.3 (Soltis et al. 1983).
Locus banding patterns were consistent with typical
subunit structures. Different loci and alleles for a given
system were designated sequentially, with the lowest
number corresponding to the most anodally migrating
locus or allele.
Data analyses
Standard measures of allozyme diversity were calculated:
the proportion of polymorphic loci (P0.99 ), mean
number of alleles per locus (Â) and per polymorphic
Table 1. Coordinates and characteristics of the fragments where Myrciaria floribunda were sampled. Isolation degree 1 is the distance of the sampled
fragment to the largest fragment (km). Isolation degree 2 is the distance of the sampled fragment to the closest 50-ha fragment (km) and bg is tree
basal girth.
Fragments
L1
L2
M2
M1
S1
S2
Altitude (m)
Size (ha)
Isolation degree 1 (km)
Isolation degree 2 (km)
bg of sampled plants (cm)
Density (indiv. ha−1 )
1810
1720
1622
1745
1590
1610
3003
3003
36
44
18
10
0
0
0
1.48
0.66
2.39
0
0
0
0.18
0.66
1.64
15.8 ± 4.13
14.6 ± 4.63
11.2 ± 5.60
13.4 ± 3.72
6.1 ± 2.179
14.9 ± 3.57
49
33
148
150
228
178
364
EDIVANI VILLARON FRANCESCHINELLI ET AL.
Table 2. Genetic diversity parameters (mean ± SE) for the studied populations of Myrciaria floribunda.
Diversity indices
Sample size
Expected heterozygosity ( Ĥe )
Observed heterozygosity ( Ĥo ) (all loci)
Number of alleles per locus (Â)
Number of alleles / polymorphic loci (Âp )
Effective number of alleles (Ae )
Percentage of polymorphic loci ( P̂ ) (0.99)
F Wright
S1
S2
M1
M2
L1
L2
33.0 ± 2.0
0.28 ± 0.075
0.30 ± 0.082
2.00 ± 0.3
2.33
1.46
83.33
−0.09NS
31.5 ± 0.8
0.30 ± 0.084
0.27 ± 0.07
2.00 ± 0.3
2.33
1.51
83.33
0.09NS
34.5 ± 0.9
0.38 ± 0.078
0.37 ± 0.077
2.00 ± 0.3
2.33
1.69
83.33
0.03NS
30.3 ± 1.1
0.42 ± 0.086
0.34 ± 0.075
2.00 ± 0.3
2.33
1.84
83.33
0.18NS
27.2 ± 0.5
0.35 ± 0.080
0.36 ± 0.092
2.00 ± 0.3
2.33
1.62
83.33
−0.02NS
28.5 ± 0.3
0.38 ± 0.079
0.33 ± 0.068
2.00 ± 0.3
2.33
1.71
83.33
0.13NS
locus ( Â p ), effective number of alleles (Ae = 1/ pi2 ),
observed heterozygosity
( Ĥo ), the expected heterozygosity
( Ĥe = 1− pi2 ), and Wright’s fixation index F (F =
1− Ĥo / Ĥe ). Test for significant deviations from Hardy–
Weinberg expectations was verified through chi-square
test within populations. All those parameters were
calculated using BIOSYS-2 (original version of Swofford
& Selander 1981; modified by Black 1997 – BIOSYS-2: a
computer program for the analysis of allelic variation in
population genetics and biochemical systematics, release
1.7. Illinois History Survey: 1989, Illinois). Spearman
rank order correlations was used to test if parameters
of genetic variability ( Ĥe , Ĥo and Ae ) varies according to
size and isolation degree of fragments.
Wright’s (1943) F-statistics ( fˆ, θ̂ p and F̂ ) were
used to measure hierarchical population structure and
were calculated by the methods of Weir & Cockerham
(1984). Jack-knifing and bootstrapping were used
for combining information over alleles and loci, for
estimating sample variances and confidence intervals.
FSTAT program version 2.9.3.2 (software developed
by J. Goudet 2002 – Available from http://www2.
unil.ch/popgen/softwares/fstat.htm) was used for these
analyses.
populations within the medium fragment (0.38 and 0.42,
respectively, for M1 and M2). Populations within the large
fragment had high heterozygosity values too (0.35 and
0.38, respectively, for L1 and L2). But, t-test showed
neither Ĥe nor Ĥo values were significantly different
among the studied fragments (α = 0.05). M2 and L2
showed higher fixation indices values (Table 2), but they
were not significant (Fisher’s exact test).
The correlation analyses revealed that Ĥe , Ĥo and
Ae tend to be higher in the largest fragment. Those
indices are also higher in fragments closer and connected
to the largest fragment of the area. The correlation
between the effective number of alleles and fragment
size was significant, as well as the inverse correlation
between Ĥo and distance from the largest fragment (Table
3). The inverse correlation between Ĥe and distance
from the largest fragment was high (r = 0.80) but not
significant (P = 0.055). The correlations between Ĥe and
area, Ĥo and area, and Ĥo and distance from the closest
neighbouring fragment ≥ 50 ha were also high but not
significant.
F-statistics indicate moderate genetic divergence
among the six populations analysed (Table 4). Yet, value
of θ̂ p for the smallest and isolated fragments is higher
than for populations of the large and connected fragment
(Table 5).
RESULTS
Six loci and twelve alleles were analysed. Significant
deviations from Hardy–Weinberg expectations were
detected only for the L2 population in the GOT locus. No
other loci showed significant deviation from the genotypic
proportion expected by the Hardy–Weinberg equilibrium.
The percentage of polymorphic loci and average
number of alleles per locus were similar for all populations
(Table 2). The effective number of alleles (Ae ) was lower for
populations of the smallest fragments (1.46 and 1.51) and
higher for populations in the largest (1.62 and 1.71). The
medium fragment M1 had also high Ae value (1.69). But,
the medium fragment M2 (connected) had the highest Ae
value (1.84). The average effective number of alleles for
the six populations was 1.64.
The expected heterozygosity was also low for the two
smallest fragments (0.28 and 0.30) and highest for
Table 3. Correlation analyses (Spearman Rank Order Correlations)
between genetic indices of diversity and characteristics of the studied
fragments. Ĥe is expected heterozygosity, Ĥo is observed heterozygosity,
Ae is effective number of alleles, area is the size of the fragment in hectares,
DLF is distance from the larger fragment, DF 50 ha is distance from the
closest neighbouring fragment ≥50 ha.
Parameters
r
P
Ĥe and area
Ĥe and DLF
Ĥe and DF 50 ha
0.75
−0.801
−0.678
0.086
0.055
0.139
Ĥo and area
Ĥo and DLF
Ĥo and DF 50 ha
0.783
−0.880
−0.759
0.066
0.021
0.080
Ae and area
Ae and DLF
Ae and DF 50 ha
0.928
−0.577
−0.698
0.008
0.231
0.123
Genetic diversity in Atlantic Forest fragments
365
Table 4. Estimates of Wright’s F statistics (f̂, F̂ and θ p ) described for each
polymorphic locus and for overall populations of Myrciaria floribunda.
f̂ = mean fixation index of individuals relative to their population;
θ p = population coancestrality coefficient; F̂ = mean overall inbreeding
coefficient of an individual.
Loci
fˆ
F̂
θ̂ p
UGPP-1
IDH-1
G6PDH-1
GOT-2
GOT-3
Mean
SE
P
0.052
0.186
0.108
−0.017
−0.017
0.189
0.296
0.194
0.050
0.024
0.143
0.139
0.101
0.066
0.040
0.062
0.040
ns
0.153
0.053
ns
0.097
0.021
ns
Table 5. Estimates (mean ± SE) of Wright’s F statistics (f̂, F̂ and θ p )
described for the three isolated and the connected fragment populations.
F statistics
fˆ
F̂
θ̂ p
Populations isolated
Populations connected
0.020 ± 0.058ns
0.137 ± 0.096ns
0.117 ± 0.050ns
0.111 ± 0.031ns
0.158 ± 0.047ns
0.053 ± 0.023ns
Plant density of M. floribunda varied from 49 to 228
plants ha−1 . It was negatively related to the fragment size
(r2 = 0.84, y = −0.045x + 178, P = 0.0102). Among the
sampled plants, fragment S1 showed the smallest average
basal girth (6.11 ± 2.17 cm). Fragments L1, S2 and L2
showed the highest average basal girth (Table 1).
DISCUSSION
Myrciaria floribunda showed high number of alleles per
locus (2.00), expected heterozygosity (0.28–0.42) and
percentage of polymorphic loci (83.33) compared to the
values found for others tropical species. According to
Hamrick & Godt (1989), the mean number of alleles per
locus and values of expected heterozygosity found for
tropical species was 1.45 and 0.109, respectively. The
genetic diversity found for M. floribunda is similar to other
long-lived, non-endemic tropical Brazilian species (Auler
et al. 2002, Conte et al. 2003, Margis et al. 2001, Salgueiro
et al. 2004, Seoane et al. 2002).
Genetic diversity indices did not differ significantly
among the studied fragments. But Ĥe , Ĥo and Ae tended
to be lower in smaller and isolated fragments (Table 2).
The correlation rates between those indices and fragment
size and isolation were high, but only significant in some
cases (Table 3). The lack of significant correlations showed
above may be explained by the recent forest fragmentation
events in the study area. Probably, not enough time
has passed for the genetic drift to decrease the genetic
diversity of M. floribunda in the small fragments. Some
genetic diversity of fragments S1 and S2 may have been
lost at the time of fragmentation due mainly to genetic
bottlenecks. A single data source on M. floribunda growth
rate available in the literature (Laurance et al. 2004)
showed a median diameter growth rate of 0.39 mm y−1 .
Considering this growth rate and that studied fragments
are about 50 y old, a M. floribunda sapling would have
girth at breast height of 9.26 cm and basal girth of
11 cm after 50 y. This means that part of our sample
may be older than the forest fragmentation in the area.
Nevertheless, all plants sampled within S1 were very small
trees, smaller than 11 cm bg. Fragments M1 and M2
also had most of their sampled trees smaller than 11 cm
bg and these fragments showed high genetic diversity.
Inbreeding could have already been detected in these
fragments. However, fixation index did not differ among
them, besides it was negative and not significant in S1.
Other neotropical studies (Apsit et al. 2001, Dick 2001,
White et al. 2002) suggest that pollen flow increases under
fragmentation, but it depends on the pollinator behaviour
after fragmentation. Gene flow among fragments may
be preventing such inbreeding effects. According to Mills
& Allendorf (1996) and Wang (2004), the migration of
1–10 individuals per generation among fragments may
avoid inbreeding. Myrciaria floribunda is pollinated by
bees and has its seeds dispersed mainly by birds (pers.
obs.). It is not known how fragmentation has affected
those animals in the studied area. But, apparently some
birds that disperse M. floribunda seeds seem to be able
to leave the forest and fly in open areas. Bacles et al.
(2006) showed that seed dispersal is up to six times more
effective than pollen dispersal at maintaining genetic
connectivity among remnants of Fraxinus excelsior, a
wind-pollinated and -dispersed temperate tree. We believe
gene flow after fragmentation may have increased in
the studied sites only in the last 20 y, when Atlantic
Forest remnants in the area started being better protected,
and as a result, some fragments have increased in size
(Aguari 2001).
Myrciaria floribunda plant density was negatively
related to the fragment size. This may influence the
relative low genetic diversity in the large fragment,
particularly compared to the medium-sized fragments.
The highest values of expected heterozygosity and
effective number of alleles were found in the fragment M2.
This fragment showed high plant density and is connected
to the largest studied fragment, which may increase the
access of pollinators and seed dispersers among them. No
conclusive explanation was found to explain the lowest
plant density in populations of the largest fragment, since
M. floribunda seems to be a late-successional species and
not expected to do better in disturbed habitat. Aldrich &
Hamrick (1998) have found higher abundance and
density of Symphonia globulifera seedlings in remnant
fragments than in continuous forest, although this is a
late-successional species as well.
366
F-statistics showed results similar to those of other
tropical tree species (Auler et al. 2002, Eguiarte et al.
1992, Margis et al. 2001, Salgueiro et al. 2004, Seoane
et al. 2002). Most of the genetic variability is within
populations, but some genetic variation among them
(θ̂ p = 0.097) was found. According to Hartl (1988),
θ̂ p values of 0.05–0.15 indicate moderate genetic
differentiation. However, Wang (2004) presumes that
populations are expected to retain genetic connectivity
when θ̂ p is smaller than 0.20. In this case, θ̂ p values
found for M. floribunda populations may still partly reflect
pre-fragmentation landscape conditions. Nevertheless,
the genetic variation among populations within the
large fragment was lower (θ̂ p = 0.053) than among
populations of the small fragments (θ̂ p = 0.117), which
indicates that fragmentation may already be increasing
differentiation among populations in the studied area. A
considerable rate of inbreeding was found at the species
level ( F̂ = 0.153). Even populations within the large
fragment ( F̂ = 0.158) showed substantial inbreeding.
This may be due to habitat loss in the small fragments
and genetic differentiation among them, and to the low
plant density in the largest fragment.
The lack of significant differences in genetic diversity
among fragments may also be due to low allele diversity
of allozyme markers, which may not provide enough
statistical power to test the proposed hypotheses. A
new study that includes M. floribunda and other species,
higher number of fragments, and DNA markers has been
developed in the same area in order to check the present
data.
ACKNOWLEDGEMENTS
This work was supported by a grant from
PROBIO/MMA (Projeto de Conservação e Utilização
Sustentável da Diversidade Biológica Brasileira/
Ministério do Meio Ambiente) to the first author. We are
indebted to Roselaini M. do Carmo, Antonio Pereira da
Silva, and Virginia Tenório for their assistance in the
lab and in the field. We are grateful to Altair Rezende de
Souza, Sebastião Loreano, Zé Maria Pinheiro de Souza,
Carlos Alberto Pompeu, Antonio Bueno de Souza e José
Leite de Mello for allowing us to work in their properties.
Thanks are due to Alexandre Siqueira Guedes Coelho for
his help in statistical analyses. The comments of Claudia
Jacobi and anonymous revisers greatly improved this
final version.
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