Download How well will Brazil`s system of Atlantic forest reserves maintain

Biodiversity and Conservation (2005) 14:2835–2853
DOI 10.1007/s10531-004-0219-9
Ó Springer 2005
How well will Brazil’s system of Atlantic forest
reserves maintain viable bird populations?
STUART J. MARSDEN1,*, MARK WHIFFIN2, MAURO GALETTI3
and ALAN H. FIELDING4
1
Applied Ecology Group, Department of Environmental and Geographical Sciences, Manchester
Metropolitan University, Chester St. Manchester M1 5GD, UK; 253 Shipman Road, Market
Weighton, East Yorkshire YO43 3RA, UK; 3Laboratório de Biologia da Conservação, Departamento
de Ecologia, Universidade Estudual Paulista (UNESP), C.P. 199, 13506-900Rio Claro, SP - Brazil;
4
Behavioural and Environmental Biology Group, Department of Biological Sciences, Manchester
Metropolitan University, Chester Street,Manchester M1 5GD, UK; *Author for correspondence
(e-mail: [email protected]; phone: +(0)161-247-6215; fax: +(0)161-247-6318)
Received 23 September 2003; accepted in revised form 13 April 2004
Key words: Atlantic forest, Birds, Brazil, Distance sampling, Extinction, Population viability,
Protected areas
Abstract. It is crucial for biodiversity conservation that protected areas are large and effective
enough to support viable populations of their original species. We used a point count distance
sampling method to estimate population sizes of a range of bird species in three Atlantic forest
protected areas of size 5600, 22,500, and 46,050 ha. Population sizes were generally related to
reserve area, although in the mid-sized reserve, there were many rare species reflecting a high
degree of habitat heterogeneity. The proportions of forest species having estimated populations
>500 ranged from 55% of 210 species in the largest reserve to just 25% of 140 species in the
smallest reserve. All forest species in the largest reserves had expected populations >100, but in
the small reserve, 28% (38 species) had populations <100 individuals. Atlantic forest endemics
were no more or less likely to have small populations than widespread species. There are 79
reserves (>1000 ha) in the Atlantic forest lowlands. However, all but three reserves in the north
of the region (Espı́rito Santo and states north) are smaller than 10,000 ha, and we predict serious
levels of local extinction from these reserves. Habitat heterogeneity within reserves may promote
species richness within them, but it may also be important in determining species loss over time
by suppressing populations of individual species. We suggest that most reserves in the region are
so small that homogeneity in the habitat/altitude within them is beneficial for maintenance of
their (comparatively small) original species compliment. A lack of protection in the north,
continued detrimental human activity inside reserves, and our poor knowledge of how well the
reserve system protects individual taxa, are crucial considerations in biodiversity management in
the region.
Introduction
There is a consensus that protecting areas as reserves is the best way to
maintain wildlife populations in species-rich countries (Bruner et al. 2001).
Consequently there is an extensive literature on the minimum size of protected areas needed within a region to contain all its important species
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(reviewed by Rodrigues and Gaston 2001). The aim of these complimentarity-based methods is generally to select minimum-sized protected area
networks that include every endemic species within at least one area (e.g.,
Peterson et al. 2000). What has been far less extensively studied is the likely
persistence of populations within protected areas, especially if reserves are
chosen to maximise species richness, rather than large populations of individual taxa. How much of its original compliment of species a protected
area will fail to sustain long-term is a crucial question in protected area
design and maintenance. Degree of isolation (Saunders et al. 1991), suitability of the matrix for species survival and movement (e.g., Sekercioglu et
al. 2002), and habitat alteration or direct exploitation inside the reserve
(Stouffer and Bierregaard 1995) can all influence species persistence. However, the underlying factor influencing the degree to which fragments lose
species over what could be very long periods of ‘relaxation’ (Brooks et al.
1999) is size of the protected area (e.g., Gurd et al. 2001) and ultimately, the
sizes of populations that it supports (e.g., Pimm et al. 1988).
There has been much debate as to the minimum sizes of populations that
are viable in the long-term, and the factors that might affect these values
(e.g., Lynch and Lande 1998). Estimates of minimum viable populations
(MVPs) can range from tens or a few hundred individuals (Howells and
Edwards-Jones 1997; Wielgus 2002) to tens of thousands (Tscharntke 1992),
with enormous within-taxon variability (Harcourt 2002). Clearly, MVPs are
variable, dependent on many factors, not least the timescale over which
extinction risk is assessed. In this study, we acknowledge the fact that we do
not know the true values of MVPs for the study species, and use a range of
MVPs from 100 to 3000, within which the real values are generally thought
to fall (e.g., Franklin 1980; Gilpin and Soulé 1986; Lynch and Lande
1998).
The danger of significant loss of species from the entire eco-region is
particularly acute in hotspots such as the endemic-rich Atlantic forest
(Fonseca 1985; Brooks et al. 1999). Only around 7.6% of the original forest
remains (Morellato and Haddad 2000), and in some states much less (e.g.,
Brown and Brown 1992). What is left is generally small and isolated protected areas (Ranta et al. 1998; Chiarello 1999), many of which are impacted by local people (e.g., Redford 1989), and lying within a matrix
dominated by agriculture, disallowing persistence or passage by much of the
region’s wildlife (Terborgh and Weske 1969; Stouffer and Bierregaard 1995;
Marsden et al. 2000).
Here we estimate population sizes for a range of bird species in three
lowland Atlantic forest reserves of size 5600, 22,500 and 46,050 ha (Figure
1). We identify the proportions of endemics amongst those species with
small populations to see whether such taxa are in particular danger of local
extinction. Finally, we estimate likely bird population sizes in other Atlantic
Forest protected areas to examine the degree to which the current reserve
system might protect birds from extinction.
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Figure 1. Map of southeastern Brazil showing the locations of Sooretama/Linhares, Ilha do
Cardoso and Ilha Grande. States are labeled as follows: PA, Paranà; SP, São Paulo; RJ, Rio de
Janeiro; ES, Espı́rito Santo; MG, Minas Gerais; BH Bahia.
Methods
Study sites
Birds were censused in three reserves/reserve complexes (Figure 1):
1. The Sooretama/Linhares complex of east-central Espı́rito Santo state,
comprises the 24,250 ha Sooretama Biological Reserve (19 030 S 40 000 W),
which lies adjacent to the 21,800 ha Linhares Forestry Reserve, owned by
Compania Vale do Rio Doce (Wege and Long 1995; Chiarello 1999). The
complex represents a Key Area for Threatened Birds in the Neotropics (Wege
and Long 1995). Both reserves lie close to sea level. Besides a small marsh and
clearings for administration buildings, the reserves are wholly forested, being
composed mostly of ‘terra firme’ forest up to 40 m in height, with some
‘mussununga’ forest containing much smaller trees on sandier soils (Simão
et al. 1997). There is a history of logging within the reserves (according to
park guards, some illegal logging persists in Sooretama), and some areas are
secondary growth. Most of the area around the reserve is pasture, Eucalyptus
plantations, arable farmland and coffee plantation, although some small
private preserves remain. Hunting is a common practice in the area and may
affect abundance of some gamebirds (Chiarello 2000). Bird surveys were
conducted in both reserves between 11 August and 16 October 1998 (transect
positions and density estimates can be found in Marsden et al. (2001)).
2. Ilha Grande State Park (23 090 S 44 100 W) covers 5600 ha of Ilha Grande
(19,000 ha) in the Baia da Ilha Grande, 2 km from the mainland of Rio de
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Janeiro State. The dominant habitat is lowland Atlantic forest, although the
island is dominated by two peaks, the higher of which reaches 1033 m
(Alves 2001). All bird surveys were conducted between June and August
1999 within the state park itself. The island has a long history of human
occupation and original forest habitat is highly fragmented (Alves 2001).
Further details of study sites and bird density estimates can be found in
Marsden et al. (2004).
3. Ilha do Cardoso (25 040 S 47 550 W), in southernmost São Paulo state, is
wholly protected within the Ilha do Cardoso State Park covering an area of
22,500 ha. The island rises to 800 m, with major habitats comprising sandplain forest (restinga), lowland evergreen forest through to humid montane
forest. Bird surveys were done during July 1999 along the network of narrow trails cut especially for researchers, and were restricted to forest
and restinga below 200 m. Further details of study sites and bird density
estimates can be found in Marsden et al. (2004).
Bird surveys
In 1998, a period of 7 weeks was spent practising bird identification and distance estimation prior to the census in Sooretama/Linhares. This followed an
extensive period of practice in bird identification from literature and especially
from bird recordings. In the 1999 surveys of Ilha Grande and Ilha do Cardoso,
data were collected by the same team, and a period of 3 weeks was spent
re-training in bird identification and distance estimation prior to the survey.
All bird surveying was done by a pair of observers, with MW always the
principal recorder. A variable circular plot method (e.g., Reynolds et al. 1980;
Marsden et al. 2001) was used to produce density estimates (individuals per
km2 ) for birds in the two reserves. Unidentified birds (usually ones which were
heard only) were noted. The distance sampling method used allows for
unidentified bird contacts, so long as all birds encountered very close to the
recorder, are identified (Marsden 1998).
In each reserve, transects were set up along existing paths of width <3 m.
Census stations were marked out along these transects at intervals of 200 paces
(around 200 m). Ideally, each census station should have been positioned
randomly, but this was not possible for the given the timescale of the fieldwork.
Bird censuses were carried out between 07:00 and 11:30 and only in the absence
of rain or heavy mist. This census period was seen as appropriate, because
during a pilot study, bird activity tended to be high during the whole morning
with a noticeable fall off in activity after 11:30 which lasted much of the
afternoon. Birds were counted at each census station for a period of 10 min.
The count period commenced immediately on arrival at the station. Recording
effort was concentrated within 30 m of the plot’s central point, although for
some species such as parrots, birds seen, or more usually heard, at distances up
to 50 m away, were also recorded. The distance from the recorder to each bird
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encountered was estimated to the nearest metre. The number of individuals in
each encounter was recorded, if ascertainable. When approaching a census
station, if any birds were disturbed (flushed) from the plot, these were recorded
as being present during the census period.
Species such as parrots, toucans, pigeons if encountered in flight at census
stations were noted, but records were omitted from the density calculations
because aerial birds violate an assumption of the census method used (Marsden
1999). For contacts where birds were heard only, the mean group size for visual
contacts with that species was substituted for the missing group size values.
Data analysis
Density and population estimation
Data from VCPM were analysed using the DISTANCE 3.5 program (http://
www.ruwpa.st-and.ac.uk/distance). We produced density estimates only for
species which were recorded ten or more times. In many species, we pooled bird
records across sites to allow more robust modelling of detection functions (e.g.,
Marsden et al. 2001). Bird groups were entered as clusters and in ungrouped
format. All key functions and associated series expansions were considered,
and choice of model for detection function governed by Akaike’s information
criterion as detailed in Buckland et al. (2001). Data in some instances were
right-hand truncated to remove outliers, but because search effort was usually
restricted to within 30 m of the recorder, truncation was sometimes unnecessary and at most 10% of the furthest records were excluded. Actual values for
truncation and subsequent grouping of records into distance bands was done
following visual inspection of detection histograms and checking of density
estimate precision under different analysis conditions.
Density estimates were used in conjunction with data on reserve sizes to
calculate, where possible, total population estimates for each species in each
reserve (total population = population density area). Standard errors for
population estimates were based on those computed for density estimates by
DISTANCE. They may be underestimated, although the standard error that
the program attaches to density estimates does have a variance component
calculated to account for survey effort replicate design (Buckland et al. 2001).
Population sizes across the three reserves
Many species were recorded at census stations, but on too few occasions to
produce a density estimate. However, it is still important to estimate their likely
population size within the reserves as these rarely recorded species are those
most likely to have small populations. We examined the relationship between
the number of records accumulated and the density estimate derived for species
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which were recorded more often. To do this, we used regression analysis with
each species’ density estimate as the dependent variable and the number of
records accumulated for the species as the independent variable. We then used
the regression equation to predict the population density for species for which
we had at least one bird record, but for which we could not calculate a density
estimate. We considered a number of possible regression curve shapes and
retained the equation that explained the largest proportion of variability.
We then plotted a cumulative population size curve (most to least abundant in
rank order) for all species for which we had a predicted population size. In order
to predict population sizes for species that were unrecorded in our survey, but
listed as present within the reserve, we fitted an asymptotic curve (cumulative
population size ¼ b1 x=ðx þ b2 Þ using species rank as the independent variable. The coefficients (b1 and b2 ) were estimated iteratively using Solver from
Excel (Office 2000). Population sizes for unrecorded species were estimated by
extrapolating beyond the last recorded species. Although it is always dangerous to
extrapolate beyond the limits of the independent variable, it is unlikely that
unrecorded species have anything other than tiny populations and the errors are
likely to be small relative to the MVPs used in subsequent analyses.
To ascertain whether species endemic to the Atlantic forest were more or less
likely to have small populations than widespread species, we used chi-squared
tests, with Yates’ correction, to examine the proportions of endemic versus nonendemic species that were actually recorded in the reserves. Because there is no
definitive list of bird species recorded on Ilha Grande (see Table 1), we did not
undertake an analysis for that reserve. Each species known from the reserves was
coded according to whether it is endemic to the Atlantic forest or not according to
the list in Brooks et al. (1999). To test whether Atlantic forest endemics predominated amongst species likely to have low population sizes, we grouped all
bird species known from a reserve into the following: endemic and recorded at
points, endemic and not recorded at points, non-endemic and recorded at points,
and non-endemic and unrecorded. In effect, a species from Sooretama/Linhares
that was actually recorded at one census station or more has an estimated population equal to or greater that 715 individuals, while a species with at least one
record from Cardoso should have a population in excess of 473 individuals.
Therefore, we tested for differences in proportions of endemic and non-endemic
species having populations greater than 714 in Sooretama and 473 on Cardoso.
Consideration of other Atlantic forest reserves
Available data on the sizes of protected areas within the lowland Atlantic
forest were collated from Fernandes (1997). Only protected areas greater than
1000 ha, and having most of their land area within the Atlantic forest lowlands
[Endemic Bird Area 075 as defined by Stattersfield et al. (1998)], were included.
Highland protected areas were included only if they contain substantial areas
of forest below 500 m a.s.l. Protected areas were split by region: the north
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Table 1. Summary statistics for the three reserves, their avifaunas and the surveys.
Area (ha)
Total avifauna spp.
No. surveyable forest spp.d
No. endemic forest spp.d
No. points/counts
Point counts per ha
No. surveyable species recorded at points (%)
No. species for which population estimation possible
Sooretama/
Linhares
Ilha do
Cardoso
Ilha Grande
46,050
>286a
221a
48
273 (546)
1:84
112 (51%)
40
22,500
418b
226
73
105 (210)
1:107
71 (31%)
27
5600
200c
140c
76 (152)
1:37
62 (44%)
23
a
Data from Parker and Goerck (1997).
Data from Martuscelli unpubl. data.
c
Figures are estimates as no complete list of birds recorded is available.
d
Excluding waterbirds, waders, rails, birds of prey, kingfishers, swifts, hirundines, owls, nightjars,
potoos, mockingbirds, house sparrow and grassland birds such as Anthus, Volatina, Sicalis and
Emberizoides. Also excluded on Cardoso are species occupying only the higher altitudes (>500 m)
of the island.
b
which includes the states of Alagoas, Sergipe, Bahia, and Espı́rito Santo, and
the south including the states of Rio de Janeiro, Săo Paulo, Paraná, Santa
Catarina, and Rio Grande do Sul.
Data on the proportion of bird species in surveyed reserves with population
estimates less than given thresholds are used to estimate similar proportions in
other protected forest areas. A species can be considered in serious danger of
extinction if its population size falls below its MVP. As few data are available
on MVPs, the numbers and percentages of species under threat were estimated
for each reserve over a range of realistic MVPs.
Results
In total, 546 counts were made at 273 points at Sooretama/Linhares (Table 1).
This figure equates to 1 point count per 84 ha. There were 210 counts at 105
points in Ilha do Cardoso State Park (1 per 107 ha) and 152 counts at 76 points
in Ilha Grande State Park (1 per 37 ha). There were sufficient bird records to
produce density estimates, and hence population estimates, for 40 species from
Sooretama/Linhares, 27 species from Cardoso and 23 species from Ilha Grande
(Table 1).
Population sizes in the reserves
In all three reserves, the best fit for population estimates of species against
number of records accumulated was a power curve where lnðyÞ ¼ lnðb0 Þþ
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b1 lnðtÞ. Regression equations for all three reserves were highly significant
(Fmin ¼ 15:4, df ¼ 38, p < 0:001).
Figure 2 shows predicted populations of all bird species actually recorded in
the reserves based on the regression equations of population estimate against
the number of records accumulated for each species. Species are ranked by
decreasing predicted population size. The fit of the cumulative population size
curve to the data was good for all three sites (Figure 3) allowing estimates of
population size for all species in each reserve (Figure 4). The bird species list for
Cardoso, the mid-sized reserve, is actually larger than that for the largest
reserve, Sooretama. In turn, the nth commonest species in Cardoso is far less
numerous than the corresponding species in Sooretama (Figure 4). Figure 5
shows the actual numbers of species, and the percentages of the species in the
avifauna of each reserve that have estimated populations lower than a series of
realistic MVPs. Numbers of ‘threatened’ species are highly dependent on MVP
size, and are especially sensitive to changes at low values of MVP. Importantly,
at an MVP of 100 individuals, Cardoso has relatively few species under threat,
because while it has many rare species, they still have populations greater than
100. If, however, the MVP rises to just 200, then it has a relatively large
proportion of species under threat (because many species have populations
estimated between 100 and 200). This, we believe, is a product of the reserve’s
habitat heterogeneity, and the scale at which it manifests itself in terms of bird
populations.
There was no difference in the proportions of endemics and non-endemics
with ‘small’ populations in either Sooretama/Linhares (v21 ¼ 0:03, p ¼ 0:88) or
Cardoso (v21 ¼ 1:96, p ¼ 0:16). If anything, in the latter reserve, there was a
greater proportion of endemics with large populations than expected.
Estimates of population size across the protected area network
Figure 6 shows the proportions of the avifauna which may be at risk under a
range of MVP scenarios (100–3000) for reserves of different size. MVP has a
very clear influence on our ideas as to the percentage of bird species safe in
reserves. Reserves around 200,000 ha and over appear to be large enough to
protect full, or almost full avifaunas, even at medium-to-high MVP values.
Conversely, reserves between 1000 and 10,000 ha are expected to lose very high
proportions of species: even with an MVP of 150, a reserve of 10,000 ha has
around 45%, and a reserve of 1000, almost 50 % of its species having populations below the MVP level.
Figure 7 shows the size of each protected area (>1000 ha) in the north and
south of the Atlantic forest region. Large reserves are rare: only eight reserves
in the south, and not one reserve in the north of the region is larger than
50,000 ha (Sooretama/Linhares is the largest reserve in the north). Twenty-six
of 63 (41%) reserves in the south, but only three of 16 (19%) in the north, are
larger than 10,000 ha.
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Figure 2. Ranked population sizes in the three reserves.
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Figure 3. Population accumulation curves showing power regression population estimates
(symbols) and fitted curves extrapolated to last known species using an asymptotic function. Order
from highest to lowest: Sooretama/Linhares, Ilha do Cardoso and Ilha Grande.
Figure 4. Estimated population sizes from the fitted asymptotic function curve. Order from
highest to lowest: Sooretama/Linhares, Ilha do Cardoso and Ilha Grande.
Discussion
How reliable are the population figures?
Our dataset from Sooretama/Linhares is one of the largest for birds using point
counts in the neotropics, and yet only around half of Sooretama/Linhares’s
forest species were recorded during more than 500 point counts, and density
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Figure 5. The numbers of species (a) and the percentages of species (b) in the three protected areas
(of size 5600, 22,500 and 46,050 ha) with populations greater than a series of MVPs.
estimation was possible in only 10–15% of species. One problem is that, even if
most birds are detected within a radius of 20 m at each census point, then the
area of census at Sooretama was only around 0.7 km2 . With such a small area
of census then there is a high likelihood of missing rare species from the census.
Most bird species are undoubtedly rare, in Sooretama as in tropical forests
generally (e.g., Thiollay 1994), so even with large datasets, indications of
abundance for rare species will be either highly imprecise, or lacking altogether.
While this is a major problem for conservation biologists conducting autecological studies of such taxa, we were interested in the species abundance curve
for the whole community, where estimates of the actual populations of individual taxa were less important.
The principal recorder conducted every point in the survey and was well
trained in bird identification and distance estimation. However, while the
common birds were no doubt identified well by sight and sound, some of the
rarer species (of more than 200 species) are more problematic. The problem is
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Figure 6. The percentages of species within the avifaunas of reserves with expected populations
lower than a series of MVPs against reserve area.
Figure 7. Ranked size distribution of protected areas >1000 ha in the northern and southern
Atlantic forest regions. Data from Fernandes (1997).
not so much with individuals seen close to the recorder, but largely with birds
heard but not observed. Distance sampling, in theory at least, allows for
undetected or unidentified encounters so long as all birds at, and very close to
the recorder, are detected (e.g., Buckland et al. 2001). More problematic is that
if in one species, most birds are identified within say 20 m, and in another,
within just 5–10 m, then the ratio of encounter rates to resultant density estimates will be different in the two (the first species will have a higher encounter
rate for a given density estimate). This is a potential problem when detection
functions are combined across habitats or species, when data are pooled across
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periods when recorders are becoming better at detecting and identifying birds,
or as in this study, where a relationship between encounter rate and density
estimates is being identified (Marsden 1998). No study has as yet addressed this
problem so in this study we can only caution that population estimates for
some of the rarer species, themselves predicted from the relationship between
encounter rate and population density in the commoner species, may be
underestimated due to identification problems.
Two issues concerning placement of sampling points warrant discussion.
First, multiplying density estimates by the amount of available habitat is a
reasonable method to estimate total populations so long as the sample taken is
representative of the area as a whole. Bird surveys in Sooretama/Linhares
covered the reserves quite well as many paths cross the reserves (Marsden et al.
2001), although the sample was not placed randomly. In the other areas, bird
surveying was more restricted, and this may have caused more serious problems of bias. For example, on Cardoso, we could survey birds only at lower
altitudes, but we know that several mid-altitude species are recorded from the
island’s peak, where no surveying was done. The same island is also rather
different to Sooretama/Linhares in that it contains rather distinct forest types
(e.g., restinga) and holds several altitudinal migrants (e.g., Galetti 2001, pers.
obs.).
The second issue is that bird censusing was usually done from existing paths
and this may, to some extent, have biased our estimates of abundance for some
bird species. For example, any edge habitat bordering paths open to increased
sunlight may be preferentially chosen by hummingbirds, tanagers and other
bird species while at the same time may be avoided by other shade-loving,
forest interior species. While we do not pretend to know the full effect of such
bias on population estimates for individual species, we suggest that the effect is
manageable when we identify the trends in abundance across the whole bird
community.
Inaccuracy in density estimates for individual species may not be such a
problem, unless there is systematic underestimation or overestimation across
the whole assemblage due to problems with the census method. There have
been no rigorous tests of the accuracy of VCPM (where actual density is
known) in the census of tropical birds, and data from temperate habitats are
few and the results usually ambiguous (Buckland et al. 2001). The most valid
tests of point count density estimation against known bird densities remain the
two studies by DeSante (1981, 1986). DeSantes (1981) found, for eight bird
species in a scrub habitat, that point count density estimates were underestimated by an average of 18% (2–70% in individual species). In a later study
of subalpine forest birds, estimates were far less precise, and could be
overestimates as well as underestimates (DeSante 1986).
Although falling short of actual tests, various studies have attempted to
identify factors influencing point count census accuracy, particularly with a view
to tailoring field methods and analysis procedures to avoid violations of key
method assumptions (e.g., Marsden 1998; Marsden 1999; Tobias and Seddon
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2002). Taken together, we suggest that our estimates, or rather the species
abundance curve derived from these estimates, may have possible errors of up to
33%. If this was the case, then our calculations of the proportions of species at
risk in reserves under the various MVP scenarios would reflect these errors.
Implications for species extinction/conservation
The main problem with the approach taken in this study is that we do not
know the MVP of any of the species. However, there seems little doubt that
populations of many species in most reserves are small – over 70% of bird
species in reserves less than 10,000 ha in area are expected to have populations
less than 500 individuals. Using a species-area related approach, Brooks et al.
(1999) reasoned that while there have been no documented extinctions amongst
Atlantic forest birds, around 40% of endemic taxa may succumb to extinction
in the coming years due to past habitat loss. While there are problems with the
approach taken by Brooks et al. (Kinzig and Harte 2000), which may overestimate the magnitude of the extinction ‘debt’ owed, our study identifies a
mechanism by which a significant number of local extinctions are expected,
primarily as a result of habitat loss/fragmentation. The degree to which these
predicted local extinctions meld to produce global extinctions will depend on
precise patterns of distribution amongst Atlantic forest endemics and the degree of protection offered to them within the current reserve network. We know
far too little about the above to predict future extinction patterns in the
Atlantic forest accurately, and work on these issues across the region as a
whole is a real priority (see later).
The species on the brink of extinction or at least those with very small and
isolated populations are, in some cases, well known. Cracids such as Red-billed
Curassow Crax blumenbachii, known only from Sooretama and a few other
patches, and Jacutinga Pipile jacutinga (Galetti et al. 1997) are prime candidates for global extinction in the medium term. Even more serious is the plight
of several critically endangered species, including Alagoas Foliage-gleaner
Phylidor novaesi, and Alagoas Antwren Myrmotherula snowi, occurring only in
tiny patches in the north (Stattersfield et al. 1998). The message from our study
is that there are many other taxa heading for local extinction in small reserves
across the region. For some endemic species, this will spell global extinction. In
others, local losses may fall short of becoming global extinctions, but we believe that many will end up being restricted to just one or two protected areas.
Such species may include almost all the Alagoas endemics, several ‘Espı́rito
Santoan/Bahian’ species such as Red-browed Amazon Amazona rhodocorytha
and Banded Cotinga Cotinga maculata, which may, in time, contract to the
Sooretama/Linhares reserve, and other, currently ‘widespread’ species,
including several southern coastal birds.
The minimum area requirement to avoid extinction of populations is clearly
influenced by population density, and there is greatest concern for the viability,
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within reserves, of populations of the higher vertebrates such as birds and large
mammals (Schonewald-Cox 1983; Belovsky 1987). Minimum-sized areas to
avoid extinction of mammal species from North American reserves was calculated to be upwards of 2700 km2 (Gurd et al. 2001) and up to 18,000 km2 for
grizzly bears Ursus arctos (Wielgus 2002). No study to date has examined
population sizes for tropical forest bird communities across whole reserves,
although areas of 5000–25,000 ha may be needed to hold viable populations of
the temperate gamebird Tetrao urogallus (Marshall and Edwards-Jones 1998;
Grimm and Storch 2000). Our study suggests that while the region’s largest
reserves should retain their full species compliments, reserves smaller than
10,000 ha are in serious danger of losing considerable components of their
avifaunas in the long term.
Just as some species may need greater areas than others, some reserves may
tend to have a higher proportion of very rare species than we might expect for
their size. In this study, Cardoso has very high bird species richness, but many
species are extremely uncommon or localised on the island. In fact, a high
proportion of species are known from just one or a tiny number of records
(e.g., Harpia harpyja, Triclaria malachitacea, Platyrinchus leucoryphus). Despite its relatively large size, we suggest that populations of many birds are
extremely small, as some are associated with upland areas (e.g., Touit melanonota), or restricted to certain habitats such as restinga scrub (e.g., Phylloscartes kronei) or bamboo (Sporophila frontalis) (Sick 1993). In this way,
reserves with particularly large faunal lists for their size (after controlling for
how well the area has been studied), may not support large populations of
individual species, as high species richness may be a reflection of habitat
diversity, while population sizes of species may more reflect the quantity of
preferred habitat.
The habitat heterogeneity of reserves may be crucial in determining rates of
local extinction across the Atlantic forest reserve network. For a given size,
we might expect homogeneous reserves to preserve a greater proportion of
their current avifaunas than will heterogeneous ones. We suggest that many
of the Atlantic forest reserves are so small, in terms of the populations of
rarer species that they can support, that homogeneity of habitat, with its
accompanying low total species list, is a desirable thing for long-term conservation of their present avifaunas. Perhaps heterogeneity is only desirable in
the very largest reserves. We did not actually measure habitat heterogeneity
across the reserves, and neither do we pretend that such measures, if we had
them, would be valid for all species at all scales (e.g. Ricklefs and Lovette
1999; Tews et al. 2004). However, altitudinal range within the reserves is a
useful correlate of habitat heterogeneity and species richness, and we can say
with certainty that the altitudinal range represented within the Cardoso
protected area was much greater than that in either Sooretama or Ilha
Grande. It may be important, and somewhat fortuitous, that Sooretama and
Monte Pascoal, the biggest reserves in the north, are comparatively homogeneous (they are low-lying so have little altitudinal zonation and lack really
2850
distinct habitat zonation). In contrast, the large reserves in the Serro do Mar
of the south have broad altitudinal ranges with marked altitudinal zonation
of endemic birds (Goerck 1999).
An important consideration is whether species survive in reasonable
numbers in the habitats and areas surrounding protected areas or not (e.g.,
Marsden et al. 2001; Sekercioglu et al. 2002). For species intolerant of the
matrix, maintenance of populations inside reserves or in undesignated forest
patches on private land is the only conservation option available. A few
highly mobile species, such as some parrots, may be able to move between
some Atlantic forest protected areas, especially those around the Serro do
Mar or where the matrix retains some forest blocks. This is important as it
may allow linkage in the form of metapopulation structure (Gilpin and
Hanski 1991), which may assist in both genetic mixing and in the rescue of
extinct subpopulations. Realistically, however, the great majority of protected
areas in the Atlantic forest, and especially those in the north of the region,
must be seen by conservationists as isolates, as far as almost every taxon is
concerned.
In terms of minimising extinction risk in the future, the biggest reserves (and
those with large areas of a given habitat) are the only areas which are likely to
maintain their species richness over time. We believe that smaller reserves will
likely go through extended periods of faunal relaxation at the end of which the
smallest are predicted to be highly impoverished. Protection of the stronghold
reserves such as Serra do Mar, Iguaçu, Sooretama/Linhares and Monte Pascoal is critical if species richness, especially amongst endemics, is to be maintained in the long term. Protection will be particularly important in the north
of the region where there has been so little provision of large reserves (e.g.,
Silva and Tabarelli 2000). The situation is nowhere worse than in the Atlantic
slope of Alagoas and Pernambuco which has several endemics not found in the
south of the region, and where remains just 878 km2 of forest in patches
averaging just 1.5 km2 (Stattersfield et al. 1998).
The next step is to compare the provision of protection for individual endemic species across the whole network of reserves, to find out (1) whether all
endemic species do occur in reasonable numbers within at least one stronghold
protected area, (2) to identify gaps in protected area provision for individual
taxa or clusters of taxa that could be remediated by additional protected area
provision, and (3) to examine the role for extending habitat management efforts to areas adjacent to protected areas to boost populations of key species
they contain. To make this step, many more data on population sizes are
needed from across important sites in the region, along with an analysis of the
spatial arrangement of protected areas, and the suitability of the matrix to
properly assess how isolated bird populations are in individual reserves. The
issues raised in this study are, of course, not specific to the Atlantic forest, and
assessments of the viability of wildlife populations in reserve systems from
other regions is needed if we are to know how well systems will conserve their
full compliment of species long-term.
2851
Acknowledgements
For various help in the field, we thank Lisa Sadgrove, Paulo Guimarães Jr and
Eliana Cazetta. Permission to conduct research in Sooretama and Linhares
reserves, logistical help and accommodation was kindly provided by Sr Gilberto Gerhardt of IBAMA- Espı́rito Santo, and Sr Renato de Jesus, of
Linhares CVRD. Our project in Sooretama and Linhares was funded by
Blackpool Zoo. Fieldwork on Ilha do Cardoso and Ilha Grande was funded by
Royal Geographical Society, Gilchrist Educational Trust, Percy Sladen
Memorial Fund, and the Department of Biological Sciences, Manchester
Metropolitan University. For permission to conduct research on Cardoso,
logistical help and accommodation, we thank Marcos Campolim. Mauro
Galetti receives a CNPq fellowship (Proc. 300025/97-1). Martin Jones kindly
improved the manuscript.
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