Regeneration of Sterculia apetala and its role as nesting site for the

MSc-thesis
Regeneration of Sterculia apetala and its role
as nesting site for the Hyacinth Macaw in the
Pantanal, Brazil
Iris van der Meer
September 2013
AV2013-21
Regeneration of Sterculia apetala and its role
as nesting site for the Hyacinth Macaw in the
Pantanal, Brazil
Iris Pauline van der Meer
September 2013
FEM 80436
Supervisor:
Dr. L. Poorter
Forest Ecology and Forest Management Group
The MSc report may not be copied in whole or in parts without the written
permission of the author and the chair group.
TABLE OF CONTENTS
Acknowledgements......................................................................................................................... 1
Summary ......................................................................................................................................... 2
1) Introduction and problem statement ..................................................................................... 3
2) Theoretical framework ............................................................................................................ 4
2.1 Pantanal ................................................................................................................................ 4
2.2 Hyacinth Macaw ................................................................................................................... 5
2.3 Sterculia apetala ................................................................................................................... 6
2.4 The palms Schelea phalerata and Acrocomia aculeata ........................................................ 7
2.5 Factors affecting regeneration and tree growth .................................................................. 7
3) Research Objectives ................................................................................................................ 8
3.1 Objective ............................................................................................................................... 8
3.2 Research Questions .............................................................................................................. 8
3.3 Hypotheses ........................................................................................................................... 8
4) Methodology ........................................................................................................................... 9
4.1 Study Site .............................................................................................................................. 9
4.2 Experimental design............................................................................................................ 10
4.3 Field measurements............................................................................................................ 10
4.4 Statistical analysis ............................................................................................................... 11
5) Results.................................................................................................................................... 13
5.1 Population structure and density of Sterculia .................................................................... 13
5.2 Influence of vegetation type, grazing and disturbance on regeneration of Sterculia ........ 14
5.3 Influence of environmental variables on Sterculia ............................................................. 14
5.4 Presence of nesting sites in Sterculia ................................................................................. 16
5.5 Population structure and density of Schelea phalerata and Acrocomia aculeata ............. 17
6) Discussion .............................................................................................................................. 19
6.1 Population structure and density of Sterculia .................................................................... 19
6.2 Influence of vegetation type, grazing and disturbance on regeneration of Sterculia ........ 21
6.3 Influence of environmental variables on Sterculia ............................................................. 22
6.4 Presence of nesting sites in Sterculia ................................................................................. 23
6.5 Population structure and density of Schelea phalerata and Acrocomia aculeata ............. 24
6.6 Strengths and limitations of this study ............................................................................... 25
6.7 Recommendations for further research ............................................................................. 26
6.8 Recommendations for management .................................................................................. 26
Conclusion ..................................................................................................................................... 28
References .................................................................................................................................... 29
Acknowledgements
This research was financially supported by ‘Stichting Het Kronendak’ and the ‘Alberta Mennega
Stichting’. My data collection could not have been collected and analysed without the advice
and support of Lourens Poorter and Lucas Leuzinger. Also many thanks to the staff of the
Fazenda Barranco Alto for their hospitality and great help with the use of horses and locating
vegetation types.
1
Summary
The large wetland of the Pantanal used to be seen as a pristine area but is becoming more and
more modified. Deforestation and land use intensification degrade vegetation areas and induce
habitat loss. Due to this habitat loss species populations are declining. The Hyacinth Macaw
(Anodorhynchus hyacinthinus) is an endangered, red list species in Brazil, and is one of the
potentially threatened species in the Pantanal. The Hyacinth Macaw is very specific in its
nesting sites and food requirements. For their reproduction, the birds depend on cavities in old
individuals of manduvi (Sterculia apetala) and for their diet on sufficient numbers of nuts of the
palm trees acurí (Schelea phalerata) and bocaiúva (Acrocomia aculeata). To survive in the longterm, the birds depend on the regeneration and existence of their main tree resources.
This MSc thesis focuses on the availability of nesting sites for the Hyacinth Macaw and the
regeneration of its host tree, Sterculia apetala, in the southern Pantanal, Brazil. It also evaluates
the population structure of the two palm species that provide the main food sources. The
population density, population structure and regeneration of Sterculia apetala, Schelea
phalerata and Acrocomia aculeata were investigated in five common vegetation types in the
Pantanal (grass, cerrado, cerradão, forest, cleared field). In total 90 plots of 40 x 40 m were
randomly located along transects. The existence of cavities in Sterculia trunks has been
explored and stem height and diameter were measured. Biotic pressure (grazing intensity) and
human pressure (distance to disturbed areas) were measured, as well as environmental factors
like bare ground cover, grass height and soil characteristics.
Sterculia apetala does not occur in grass and cerrado areas. In the other three vegetation
types where it is present, it has a similar population structure. The overall population structure
shows that there are many saplings, but that the distribution of adult tree sizes is irregular.
Grazing intensity and location disturbance did not affect the abundance of Sterculia. The
minimum tree size, for which a cavity was found, was 13.5 m stem height and a 66 cm stem
diameter, which is larger than the 50 cm stem diameter found by Santos Jr. et al. (2006). An
average of 0.42 potential nest cavities per ha was found in the vegetation types included in this
study indicates that potential nesting sites are abundant. The palm trees occurred in all
vegetation types with a minimum density of 2.23 trees/ha for Schelea phalerata and 0.83
trees/ha for Acrocomia aculeata. In vegetation types where Sterculia grows, the palm trees are
also abundant. Therefore food offer and availability of potential nest sites does not seem to be
the limiting factor for the population of Hyacinth Macaws in this part of the Pantanal.
There are three alternative explanations for the irregular population structure of Sterculia.
First, this irregularity could be explained by discontinuous recruitment because of the lightdemanding nature of the species, which requires gaps to establish. Or second, there might
actually be continuous recruitment with some peaks after establishment opportunities due to
large disturbances or more successful years, which causes irregularity. Or third, there is a large
bottleneck in the first regeneration phase but once a tree reaches a diameter of 10 cm, chances
of survival are high and trees will only die of senesce. Hence, it is recommended to set up a
monitoring plan to evaluate tree establishment, growth and survival for several years, and to
evaluate trends in regeneration.
2
1) Introduction and problem statement
The growing world population and the rising consumption lead to many environmental threats
worldwide. It creates conditions that cause global climate change, overexploitation, habitat
degradation and loss, habitat fragmentation, species extinction, pollution and spread of
invasive species (Groom et al. 2006). A big ecosystem environmentally affected is the large
wetland of the Pantanal. Ranching and farming intensification has become a major cause for
deforestation in and around the floodplain (Seidl et al. 2001, Lourival et al. 2009). The removal
of forests for farm expansion eradicates natural communities and there is increasing evidence
that the area is threatened by activities of mining, illegal hunting and fishing, and indiscriminate
use of fire. This has resulted in ecosystem disruption (Gottgens et al. 2001, Groom et al. 2006).
The internal threats to the Pantanal with the intensification of land-use systems and
overexploitation of species are exacerbated by the threats of siltation, pollution and water
diversion (Mittermeier et al. 1990, Lourival et al. 2009).
Due to habitat loss and degradation in the Pantanal species populations are declining.
The Hyacinth Macaw (Anodorhynchus hyacinthinus) is one of the threatened species. Of the
6,500 Hyacinth macaws left in the wild 5,000 live in in the Pantanal and are still commonly seen
there, but are rarely spotted in other areas. The Hyacinth Macaw is mainly threatened by
habitat destruction, poaching and the collection of feathers (Collar & Juniper 1992). Although
legislation has reduced the illegal trade, the birds are still threatened due to loss of their
habitat. Nest-trees are cleared because high ground is needed for wet-season pasture and to
protect cattle from vampire bats, which host in the cavities of the macaw’s nesting tree. The
endogamy of the Hyacinth Macaw, restricted geographic distribution, low reproductive rate,
large body size (Guedes 2004) together with the scarcity of their nesting sites make this bird
very vulnerable to extinction (Pizo et al. 2008).
To survive in the long-term, the birds depend on the regeneration and existence of their
main tree resources. Hyacinth Macaws in the Pantanal use cavities in the Sterculia apetala, also
known as manduvi, in 94% of the cases as nesting site (Santos Jr. et al. 2006). They
predominantly feed on nuts from the Palm trees acurí (Schelea phalerata) and bocaiúva
(Acrocomia aculeata) (Santos Jr. et al. 2006), which are common trees in all vegetation types of
the Pantanal (Faria et al. 2008). In some areas in the Pantanal there is lack of regeneration with
the Sterculia apetala which is not only a problem for the Hyacinth Macaw but for many other
species depending on the manduvi tree and its fruits (Santos Jr. et al. 2006).
This study focuses on the availability and regeneration of the Sterculia in the southern
Pantanal, and also looks at the population structure of the palm trees Schelea phalerata and
Acrocomia aculeata. The population structure and regeneration of the trees have been
measured in five different vegetation types (grass, cerrado, cerradão, forest and cleared field).
The influences of grazing intensity and location disturbance have been researched, as well as
environmental factors such as light in the canopy, bare ground cover, grass height and soil type
and color.
3
2) Theoretical framework
2.1 Pantanal
The large wetland of the Pantanal covers parts of Brazil, Bolivia and Paraguay. It has a size of
160,000 km2 and hosts an enormous biodiversity (Junk & Nunes de Cunha 2004). It is a
floodplain mosaic of seasonally inundated grasslands, river corridors, gallery forests, lakes, and
dry forests (Prance & Schaller 1992; Gottgens et al. 2001). The vegetation is therefore very
heterogeneous and the area has extraordinary concentrations of wildlife with at least 650
species of birds, 260 species of fish, 124 mammal species, 50 species of reptiles and over 2000
identified plant species (Seidl et al. 2000, Harris et al. 2005).
Vegetation
The vegetation in the Pantanal is
largely made up from elements from
the three biomes surrounding the
Pantanal region (Fig.1). In the east the
Pantanal is bordered by the cerrado of
Central Brazil, fringed to the northwest
by semi-deciduous forest related to the
Amazonian forest, and in the southwest it is
bordered by the dry chaco-like forest of
Bolivia (Prance & Schaller 1992). The
Pantanal floodplain consists of a mosaic of
rivers, oxbows, draining channels, wet
grasslands and permanent and temporary
water bodies (Santos Jr. et al. 2007). The
vegetation looks like a matrix as the flooded
areas are interspersed with cordilleras (Ratter
Figure 1. Location of the Pantanal in South
et al. 1988 in Santos et al. 2007), areas on
America (Source: http://www.davidmixner.com/
sandy elevation 1 to 2 meters higher than the 2013/07/travel-brazils-other-amazon-thesurrounding landscape. The cordillera habitat is a pantanal.html).
mixture of savannah and forest formations
(cerrado, cerradão, and semi-deciduous forest) (Keuroghlian et al. 2009).
Ecological drivers of the Pantanal
The key ecological factor determining the processes and patterns in the Pantanal is the flooding
pulse, which follows an annual, mono-modal cycle with an amplitude from 2 to 5 meter and
duration of 3 to 6 months (Harris et al. 2005). Annually, the rainfall varies from 1,200 to 1,300
mm across the region with most rain falling in the rainy season, between November and March.
From May to October the land dries out and grassland with scattered pools appears. The
Pantanal is strongly affected by its hydrology and the flooding related nutrient enrichment that
affects the food web of aquatic and terrestrial communities. Consequently, the occurrence and
abundance of species in the Pantanal is related to the seasonal ecological resources. During the
4
year there is high variability in food availability, the presence of potential competitors and
predators, and the availability of reproductive niches (Alho 2008).
Threats and protection in the Pantanal
The farming and mining activities in the area mainly cause the threats to biodiversity in the
Pantanal. About 95% of Pantanal lands are privately owned and approximately 80% of these
areas are used as cattle ranches. Cattle ranching is locally perceived as the only viable activity in
the region, and land that is not producing beef is perceived as being ‘unproductive’ (Seidl et al.
2001). This local approach gives little opportunities for conservation objectives (Mittermeier et
al. 1990, Lourival et al. 2009). The internal and external threats to the ecosystem ask for a
protection status for the Pantanal. However, according to Rylands and Brandon (2005) the
Pantanal is one of the least protected ecosystems with respect to IUCN categories I to III with
less than 5% of the ecosystem conserved in nature reserves. IUCN category I represents strict
protected areas and unmodified to slightly modified areas. IUCN category II is for national parks
and sets natural areas aside to protect the ecological processes but also provide some
foundation for environmental and cultural opportunities. Category III is to protect a specific
natural monument with a high visitor value. The IUCN categories IV to VI cover protection of
semi-natural areas together with people-nature interactions and many management
interventions (IUCN 2012). The poor performance in protection of ecosystems has been
justified by a widely accepted belief that the Pantanal region is protected by factors like its
traditional farmers, flooding, and remoteness (Harris et al. 2005).
2.2 Hyacinth Macaw
The Hyacinth Macaw (Anodorhynchus hyacinthinus) is one of the 14 endangered species in the
Psittacidae family occurring in Brazil. The total current population of the Hyacinth Macaw is
estimated at 6,500 individuals (Guedes 2004, Faria et al. 2008). Since 2000, the IUCN has listed
this species as endangered because the population has undergone very rapid reductions.
Although legislation has reduced the illegal trade, it still continues at a small scale and local
hunting still occurs (BirdLife International 2012).
Hyacinth Macaws live in pairs and have low reproductive rates with on average one
chick every two years (Pinho & Nogueira 2003, Faria et al. 2008). The birds are secondary cavity
nesters and therefore need large pre-existing tree holes for nesting. In the Pantanal two tree
species, Ximbuvera (Enterolobium contortisiliquum) and Manduvi (Sterculia apetala), were
recorded with nests of Hyacinth Macaws (Pinho & Nogueria 2003) but with to majority of nests
found in the first species (Santos Jr. et al. 2006). In other areas in Brazil the birds also tend to
breed on cliffs (Collar 1997 in Faria et al. 2008). The cavities originate mostly from the use by
woodpeckers but also from the breaking-off of branches, and from other causes such as
termites, ants, fungi, or bacteria (Pinho & Nogueira 2003, Leuzinger pers. comm. 2013). In the
Pantanal competition for the holes occurs as approximately 17 bird species use these cavities
for reproduction, and mammals and honeybees also have their preference for these holes
(Snyder et al. 2000). Competition between the macaw pairs is even stronger as only Sterculia
trees older than 60 years produce cavities large enough to be used by the Hyacinth Macaw
5
(Santos et al. 2006). Of these adult trees, only 5% of the Sterculia in the south central Pantanal
contained suitable cavities for the species (Guedes 1993 in Johnson et al. 1997). Scarcity of nest
cavities is known to limit breeding densities of parrot species (Johnson et al. 1997).
According to Pinho & Nogueira (2003), the nest density varies from 0.021 – 0.045 per
100 ha in the Pantanal, which is rather low. This if often explained by the lack of potential
breeding sites (Guedes 2004, Pizo et al. 2008). However, Pinho & Nogueira (2003) recorded
unoccupied potential breeding sites which give an estimated theoretical density of 0.11 nests
/100 ha. This is equal to 34 pairs of Hyacinth Macaws in an area of 100 ha. The unoccupied
cavities might be due to the use by other species in the non-breeding season of macaws, which
can make the cavities less attractive for the Hyacinth Macaw (Pinho & Nogueira 2003).
However, as there are more cavities available than used it is questioned what limits the
occupation of breeding sites in Pantanal.
2.3 Sterculia apetala
Sterculia apetala, also known as manduvi, and often confused with the similar Sterculia striata
is a deciduous tree, of fast growth, large size and composing the emergent stratum. Its
geographic distribution covers Southern Mexico and Central America to Peru and Brazil. It is
one of the tallest trees in the Pantanal, with a height varying between 15-35 m. In the Pantanal,
Sterculia grows in natural cordillera fragments, the non-flooded savannah-like cerrado and
deciduous to semi-deciduous forest (Santos Jr. et al. 2006, Keuroghlian et al. 2009). The
cordilleras cover only 6% of the vegetation area of the Pantanal (Silva et al. 2000, in Pizo et al.
2008).
Sterculia is light demanding and need disturbance to some extent. Therefore, they
mainly become established in primary succession or secondary succession, like old fields or
small natural clearings in the forest (Johnson et al. 1997). The growth of Sterculia differs slightly
among sub-regions of the Pantanal, but the average annual radial growth rate of Sterculia trees
is 3.44 mm/year (Santos Jr. et al. 2006). The tree has soft and light wood, probably facilitating
the excavation of nest cavities (Pinho & Nogueira 2003). The minimum size for having a nest
cavity suitable for the Hyacinth Macaw found in previous studies was 50 cm DBH (diameter at
breast height, 1.30 m). All individuals larger than 100 cm had nest cavities (Santos Jr. et al.
2006). Based on the growth rate of Sterculia apetala in the Pantanal and on the recruitment
age of new trees capable of providing nest-cavities, only trees of 60 years of age and older are
suitable to house nest-cavities for the Hyacinth Macaw. In previous research, regeneration
turned out not to be constant and to be highly influenced by the grazing of cattle (Santos Jr. et
al. 2006).
Environmental effects on Sterculia apetala
During the flooding season the forest habitats experience enlarged pressure from cattle.
Cattle have been present in the Pantanal for over two centuries, and the cumulative long-term
effects of grazing and burning could be disrupting the habitat dynamics of the floodplain
(Johnson et al. 1997). Prance and Schaller (1982) said that little vegetation remains intact in the
6
Pantanal because of the effects of cattle, fire, man or a combination of these. Young Sterculia
are preferentially foraged by cattle, which may cause high seedling mortality (Janzen 1972 in
Johnson et al. 1997). Cattle in the Pantanal have a considerable effect on the forest understory
vegetation, particularly through selective grazing and trampling (Prance & Schaller 1982). High
frequency of fire may prevent trees in forested habitats from surviving to a size capable of
providing usable cavities for birds. Guedes (1993 in Johnson et al. 1997) suggests that fire
causes a high rate of nesting tree loss. All these events combined might cause a regeneration
problem for the S. apetala and therefore a limited number potential nest sites. Guedes (1995 in
Santos Jr. et al. 2006) states that 5% of manduvi trees which shelter nests used by the Hyacinth
Macaw are lost every year due to fires, deforesting or storms.
2.4 The palms Schelea phalerata and Acrocomia aculeata
Palms are abundant in the tropics and provide an essential food for wildlife and an economic
resource for people. In many parts of the tropics, palms represent a major component of the
canopy and a conspicuous element of the understory (Scariot 1998).
Schelea phalerata, also known as the acurí palm, thrives in the Pantanal. The Prance
and Schaller (1982) study of vegetation types noted acurí as one of the most prominent
structural components of the Pantanal ecosystem. The palms are the main food source for the
Hyacinth Macaw and also present in diets of other birds and mammals, such as crested
caracaras, bare-faced curassows, white-lipped peccaries, tapirs and armadillos (Holt 2001). The
acurí can grow up to 18 m in parts of Bolivia but this is not common in the Pantanal (Barthlott &
Winiger 2001). Acrocomia aculeata is also known as the bocaiúva palm and is more scattered
throughout the landscape op de Pantanal. The bocaiúva grows up to 15-20 m, with a trunk up
to 50 cm in diameter. The acurí produces fruits all year round while the bocaiúva is more
seasonal with the peaks in the wet season. Some individuals also eat the sprouts of the palms
(Alho in Fraser & Keddy 2005, Keuroghlian et al. 2009).
2.5 Factors affecting regeneration and tree growth
The Pantanals main driver for tree regeneration and growth, its seasonal inundation, can have
major effects on plant communities. It can decrease the growth rate of trees, influence the
morphology of individuals and the richness, structure, and distributions of species (Damesceno
Jr. et al. 2005). Seasonal inundation reduces oxygen availability to trees, which is for many tree
species a key factor to germinate (Joly 1991 in Wittman et al. 2008). Some tree species are
adapted to grow in flooded areas, but Sterculia apetala seems to prefer non-flooded deciduous
to semi-deciduous forest (Santos Jr. et al. 2006). The availability of oxygen can explain the
woody vegetation covering non-flooding areas, versus herbaceous vegetation with some
dominant flooding-resistant tree species on the permanently wet parts of the Pantanal (Haase
1999). The Pantanal is large sink for sediments deriving from large variety of parent materials
from the surrounding rivers. Nutrient supply is therefore high in the Pantanal and especially in
the non-flooded soils. However, as the deciduous and semi-deciduous forest fragments in the
Pantanal are present on non-flooded ground, forest productivity is limited by a shortage of
water availability for plants in the dry season (Haase 1999). Together with this, saplings need to
7
be able to handle the high frequency of fire in the Pantanal and the high intensity of grazing by
cattle (Johnson et al. 1997).
Sterculia apetala trees produce their first seed crops when trees are 20-30 years old or
15-25 m tall (Janzen 1971 in Dvorak et al. 1998). The seed dispersal of Sterculia in the Pantanal
is mainly facilitated by the toco toucans and chestnut-eared aracaris (Pizo et al. 2008). They
swallow whole seeds and remove them from the vicinity of fruiting plants. The toco toucan
seems to be responsible for 83.3% of the seed dispersal. By spreading out the seeds they are
avoiding the clumping of adult Sterculia trees, which could be an advantage for the Hyacinth
Macaw, as they do not tend to place their nests close to each other (Pizo et al. 2008).
3) Research Objectives
3.1 Objective
The Hyacinth Macaw is threatened with extinction, which is partly due to illegal trade but
mostly due to habitat loss. Because the Hyacinth Macaw is very specific in its food choice and
choice for reproduction sites, it is essential to conserve its habitat to maintain reproductive
capacity and population size. The main objective of this study is to evaluate the availability and
regeneration of Sterculia apetala in the southern Pantanal. Besides the potential nesting
cavities this study also looks at the population structure of the palm trees Schelea phalerata
and Acrocomia aculeata whose fruits provide the major food source for the Hyacinth Macaw.
3.2 Research Questions
The research questions are divided into three topics: population structure and regeneration,
nest availability, and food availability.
Population structure & regeneration
1) What is the overall density and population structure of Sterculia in five common vegetation
types (grass, cerrado, cerradão, forest and cleared field) in the Pantanal?
2) Is the regeneration of Sterculia affected by vegetation type, grazing and disturbance?
3) What is the influence of environmental factors (flooding, ground cover, grass height, soil
type, and soil color) on Sterculia density?
Nest availability
4) What factors determine the presence of potential nesting sites in Sterculia?
Food availability
5) What is the overall density and population structure of Schelea phalerata and Acrocomia
aculeata in the five different vegetation types (grass, cerrado, cerradão, forest and cleared
field)?
3.3 Hypotheses
Population structure
1) Sterculia apetala is a light-demanding species and will therefore have higher densities in
more open areas like cerrado and cerradão systems, and in forest edges. Although the grass
8
vegetation is very open, a low density is expected due to oxygen deprivation caused by
flooding and due to fire occurrence.
2) The regeneration (trees ≤ 5 cm stem diameter) of Sterculia apetala will be higher in semiopen areas (cerrado and cerradão) than in dense forest areas as the species is light
demanding. However, when an area is too open there might be little regeneration because
of associated flooding and fire occurrence, high competition and therefore no
establishment opportunities. Therefore disturbance is expected to create opportunities and
positively influence regeneration. Grazing will either lead to reduced regeneration because
the seedlings might be eaten by cattle, or it may lead to increased regeneration, because
grazing reduce grasses and therefore reduces competition with grasses.
3) Sterculia regeneration increases with soil fertility (because of enhanced resource
availability) and with a decrease in herbaceous cover (because of increased competition),
and decreases with flooding intensity (because of a lack of oxygen).
Nest availability
4) Nesting probability will increase with tree diameter, as cavities needs to be of sufficient size
and older trees are more likely to be damaged and therefore have a cavity. Cavities can be
in all adult manduvi trees, but a nesting site is likely to be encountered more in forest edges
because of easier access and greater vision.
Food availability
5) The palm trees Schelea phalerata and Acrocomia aculeate are less affected by different
vegetation types and management practices as they do very well in many habitats. Palms
are light demanding and will therefore occur less in areas with a high woody cover. In
contrast with Sterculia apetala these tree species will also do well in regularly flooded areas
as palms are less affected by occasional flooding. As a result of high light availability and
flooding, these species will also occur in all the grass areas. There will be higher numbers of
Schelea phalerata and Acrocomia aculeata in total than of Sterculia apetala because they
establish easily. Besides that, the palms are used as food for cattle and as a result of this the
palms will not be cut, while the Sterculia does get cut once in a while.
4) Methodology
4.1 Study Site
This study was carried out at the Fazenda Barranco Alto (www.fazendabarrancoalto.com.br) in
the Mato Grosso do Sul State that falls into the centre of the southern Pantanal (position of the
main house: 19°34’40” S 56°09’08” W). Average annual rainfall in this region is 1,192.5 mm and
the mean monthly temperature is 26°C, ranging from 19°C to 33°C (Donatti 2011). The Fazenda
covers an area of 11,000 hectares, on which Nelore cattle are bred for meat production but of
which 3,400 ha are protected areas free of cattle since 1980. The Fazenda plays a role in ecotourism and can host up to 15 guests in their local tourist lodge. The Fazenda is a relatively
average farm in the southern Pantanal with 2000 heads of cattle and is among the most pristine
areas in the Pantanal.
9
4.2 Experimental design
A pilot study was done to explore the different vegetation types and to make a selection in
which plots could be examined to investigate S. apetala, S. phalerata and A. aculeata. Five
different vegetation types (grass, cerrado, cerradão, forest and cleared field) were inventoried.
 Grass habitat varies from areas with scattered trees to open savannah without trees. Some
of the natural grassland is seasonally flooded (Keuroghlian et al. 2009).
 Cerrado is the Brazilian term for a “dry tree and shrub savannah”. It is an open grassy
landscape with a more or less dense growth of bushes and low trees (Dubs 1992).
 Cerradão is the Brazilian term for savannah woodland. This type of vegetation has a closed
canopy of trees without a distinct stratification in the tree-layer. The trees are 10-14 m tall,
often branching low in the middle third of the trunk and with a tend to have a twisted
growth. The ground cover consists of shrubs and often many terrestrial bromeliads (Dubs
1992).
 Semi-deciduous forest is forest with an irregular upper story 18-24 meter tall. The
understory is made up of mixed evergreen and deciduous trees with in the southern
Pantanal often a domination of Acurí palms (Attalea phalerata) (Dubs 1992).
 Cleared field is the area on cordilleras (areas on sandy elevation 1 to 2 meters higher than
the surrounding landscape) of which the vegetation is cleared 30 years ago, and contains
grass for the cattle to graze. By the time of clearing some adult trees were left standing and
there are tree species regenerating on these fields (Leuzinger pers. comm. 2013).
In total 90 plots of 40 x 40 m were randomly located along transects and separated by at least
75 m to prevent pseudoreplication. There are 20 plots in cerradão, forest and cleared field and
15 plots in the grass and cerrado vegetation types as the pilot study indicated that Sterculia
does not occur in these vegetation types and therefore only the environmental variables and
the palm trees were measured in all plots. Of these areas, the different intensities of grazing as
well as human disturbance have been marked in cooperation with Lucas Leuzinger, the owner
of Fazenda Barranco Alto and also biologist. Per plot environmental variables, and individuals of
Sterculia apetala, Schelea phalerata and Acrocomia aculeata were recorded and measured as
described below.
4.3 Field measurements
Per plot – measurements were carried out to compare environmental variables, grazing
intensities and human disturbances between the different vegetation types. The tree density
and characteristics are thereafter associated with the environmental variables of the plots.
- Vegetation type, GPS coordinates and elevation.
- Grazing intensity; with low = no grazing in the area, intermediate = grazing up to two
months per year, and high = 2-6 months of grazing annually.
- Human disturbance; with low = relatively undisturbed with little human influence,
intermediate = relatively close to the road or settlements, and high = located in small
woods surrounded by pastures or roads.
- Soil type; sand, dark sand, silt, or clay.
- Soil colour; on a 5 point scale from light (1) to dark (5).
10
-
Presence/absence of litter on the soil.
Bare ground cover, total vegetation cover and grass cover (all in percentage).
Grass height (in cm).
All the individuals of Sterculia apetala ≥ 0.4 m height, as from this height the seedlings
are easy to distinguish. The individuals of Schelea phalerata and Acrocomia aculeata ≥
2.0 m height were recorded and measured, as the leaves of the plants are rather large
and only from a total height of 2.0 m the trunk might start forming.
Per tree – measurements are carried out to look at the population structure of the tree species
and to compare the characteristics of the trees between different vegetation types, different
intensities of human disturbance and different grazing intensities.
- In case of S. apetala and Acrocomia aculeata diameter at breast height (DBH), 1.30 m.
- Height of the tree in m till growth point of the trunk and till the top of the tree at the
position of the highest leaf.
- Dawkins crown illumination (according to Jennings 1999) in classes:
o 1. No direct light (crown not lit directly either vertically or laterally)
o 2. Lateral light (<10% of the vertical projection of the crown exposed to vertical
light, crown lit laterally)
o 3. Some overhead light (10-90% of the vertical projection of the crown exposed
to vertical illumination)
o 4. Full overhead light (>90% of the vertical projection of the crown exposed to
vertical light, lateral light blocked within some or all of the 90# inverted cone
encompassing the crown
o 5. Crown fully exposed to vertical and lateral illumination with the 90 degrees
inverted cone encompassing the crown.
- In case of seedlings, light was measured in percentage with a spherical densiometer
(model A, originally developed by Dr. Paul E. Lemmon).
- In case of Sterculia, the presence/absence of a cavity was inventoried. If a cavity was
present, the height of the cavity was recorded as well as the tree location (forest border
(≤ 20 m inside forest, measured from outmost tree), or in the interior (≥ 20 m from
border), or in the open field). If it could be observed the expected cause of a cavity
(woodpeckers, branch breaking, ants, fire, ...) was recorded as well as the potential use
of the cavity by birds.
4.4 Statistical analysis
During the data collection in the field several individual Sterculia trees were found that
possessed multiple stems. In that case, the stem with the largest DBH was selected to be
included in the analyses comparing vegetation types. For the allometric comparison between
the tree diameter and tree height all stems were included except for the individuals with a
height < 1.50 as only individuals with woody structures are included. The relation between tree
11
diameter and tree height was tested with a power regression to check whether DBH can predict
tree size and vice versa.
No Sterculia individuals were found in grass- and cerrado vegetation. Therefore in most
analyses these vegetation types were excluded to focus on differences between the vegetation
types where the manduvi tree did occur (cerradão, forest and cleared field). This also allowed
meeting the statistical assumption of homogeneity of variances. As the data of the population
structure and density was not normally distributed and did not turn out to be normally
distributed after log-transformation, non-parametric tests were used to compare population
structure in vegetation types, grazing intensity, location disturbance and presence of cavities.
Sterculia density (#trees/ha) was log-transformed prior to analysis to reduce outliers and to
increase the homogeneity of variance. Kruskal-Wallis tests were performed to look at
differences in population structure with DBH distribution and with DBH class distribution. The
tree diameters were put into classes of 10 cm, starting at 0.1 cm and ending with a DBH group
of ≥ 100 cm. In the graphs of the population structure a distinction has been made to show the
number of seedlings (with a height < 1.5 m) in the smallest DBH group (0-10 cm) in contrast
with the larger saplings. To test for differences in total DBH distribution between vegetation
types an independent-samples Kolmogorov-Smirnov is performed.
To analyse the nesting potentials of the trees, only trees with a DBH ≥ 50.0 cm were
considered, as this is the minimum diameter to have a cavity suitable for Hyacinth Macaw
nesting (Santos Jr. et al. 2006). A binary logistic regression relating the probability of occurrence
of cavities of the hyacinth macaw in trunks of Sterculia apetala, as a function of diameter at
breast height (DBH), has been performed with the stepwise method starting with trees with a
DBH ≥ 10.0 cm. This has also been performed for the probability to be reproductive as a
function of the DBH with the trees ≥ 1.5 m in height. Next to all the tests for the Sterculia the
palm trees Schelea phalerata and Acrocomia aculeata were also analysed for their population
structure and density. As DBH is less important in palm trees, the trunk height (without the
palm leaves) has been used for analyses. Both palm species are not normally distributed.
Therefore log-transformation has been performed to make outliers smaller and non-parametric
tests were used. Homogeneity of sample is smaller than homogeneity of the statistical model,
which gives reason to assume the statistics will be right. Therefore, the non-parametric KruskalWallis test has been performed to compare the palm distributions in different vegetation types.
The relationships between the environmental variables, the vegetation types and the
density of Sterculia as well as the densities of Schelea phalerata and Acrocomia aculeata were
described with the use of a Principal Component Analysis (PCA) in Canoco 5.0. All the other
statistical analyses were performed using SPSS 21. The separate influence of the environmental
variables was tested with a Spearson Rank correlation and Kruskal-Wallis tests.
12
S. apetala trees (N/ha)
5) Results
Sterculia density(N/ha)
30
25
20
15
10
5
0
5.1 Population structure and density of
Sterculia
In total 172 Sterculia trees, with 189
stems were measured in the 90 plots. 53
Sterculia trees were seedlings with a
height < 1.50 m. Sterculia does not occur
in the vegetation types of grass and
Grass Cerrado Cerradão Forest Cleared
cerrado (Fig. 2). Sterculia density
(tree/ha) does not differ significantly Figure 2. Total average tree density of Sterculia in the five
vegetation types with mean and S.D. indicated.
between the vegetation types where the
species occurs (cerradão, forest, cleared field), (χ2 = 5.064, df = 2, p = 0.080).
4.0
a. Overall population structure
S. apetala trees (N/ha)
S. apetala trees (N/ha)
The overall population structure of Sterculia is characterized by a relatively large
number of seedlings but of which only a few individuals develop woody structure in time. The
diameter classes between 11-40 cm are similar indicating that once the woody structures have
been formed the individuals are surviving (Fig 3a-d). The population structure does not differ
significantly between the three vegetation types (cerradão, forest, cleared field), (KolmogorovSmirnov test, p =0.092 (Fig. 3a-d).
3.0
2.0
1.0
0.0
4.0
3.0
2.0
1.0
0.0
DBH classes (cm)
c. Population structure in cerradão
S. aptala trees (N/ha)
S. apetala trees (N/ha)
DBH classes (cm)
4.0
3.0
2.0
1.0
0.0
DBH classes (cm)
b. Population structure in cleared field
4.0
d. Population structure in forest
3.0
2.0
1.0
0.0
DBH classes (cm)
Figure 3a-d. Population structure of Sterculia trees for all three vegetation types combined (a), cleared field (b) cerradão (c) and
forest (d) (Kolmogorov-Smirnov test, p= 0.092). The seedlings with a height < 1.50 m are shown in a transparent color in the first
DBH class per vegetation type.
13
5.2 Influence of vegetation type, grazing and disturbance on regeneration of Sterculia
As showed in section 5.1, the total density does not differ between vegetation types. There is
neither a statistical difference among the three vegetation types when considering
regeneration density (individuals with a height < 1.50 m) only (χ2 = 4.464, df = 2, p = 0.107), or
when considering individuals ≥ 1.50 m (χ2 = 2.966, df = 2, p = 0.227). Grazing intensity by cattle
does not affect the occurrence and tree density of Sterculia in all the five vegetation types (χ2 =
1.182, df = 2, p = 0.554). Neither does proximity to human disturbance affect Sterculia density
(χ2 = 3.167, df = 2, p = 0.205).
1.0
5.3 Influence of environmental variables on Sterculia
Flooding and fire only occurs in grass and cerrado areas. As fire is infrequent and not well
documented by the Fazenda, data of these events were not available for analysis in this study.
Flooding occurs in some grass areas and there are no Sterculia trees in these environments.
Figure 6 gives a visual representation of the environmental factors, tree densities and
vegetation types with the dots presenting the vegetation types of the different plots. It shows a
continuum from open to closed vegetation with the division of five vegetation types. The left
side shows a lot of sand, high grass and grazing which keeps the grass system going. The other
side has more tree cover (manduvi, acurí and bocaiúva), more litter, darker soils and therefore
more fertile grounds and again closed vegetation with dark understories and a lot of bare
ground. The cleared field is intermediate with characteristics of grass and cerrado in the
amount of grass, but the area has also trees as it is derived from the forest and cerradão
systems on the cordillera. Visible is that the density of manduvi, the nesting tree, and the two
palm trees (acurí and bocaiúva) go together with the environmental variables.
Bocaiuva
Grass height
Acuri
Grass cover
Grazing
Location disturbance
Elevation
Dark sand
Manduvi
Soil color
Litter
Cerradao
Sand
Bare ground
Cerrado
Figure 4 . Visual representation
with Principal Component
Analysis (PCA) of all
environmental factors, tree
densities and vegetation types
with the dots presenting the
vegetation types (yellow =
grass, orange = cerrado, red =
cerradão, green = forest and
blue = cleared field).
Forest
Clay
Grass
-1.0
Axis 2 (14.1% explained variation)
Cleared field
-1.0
Axis 1 (63.3% explained variation)
1.0
14
Sterculia density (N/ha)
S. apetala trees (N/ha)
There is a positive effect of bare ground
cover (Spearman r = 0.34, p < 0.001) and a
negative effect of grass height (Spearman R
= -0.46, p < 0.001) on Sterculia density.
Litter presence (χ2 = 33.413, df = 1, p =
0.001) as well as soil color (Fig. 6) has also a
significant effect (χ2 = 40.749, df = 4, p =
0.001) on Sterculia density. Soil color is
used as an indication for soil fertility.
Darker soil indicates more organic matter
and a higher fertility. Sterculia density
increased with the darkness of the soil.
40
30
20
10
0
1
2
3
4
Figure 5. Sterculia density
in different
soil colors
Soil color
(light to dark)
(from light = 1, to dark =5).
5
Flooding and fire only occur in the lowers parts of the landscape, where grass and
cerrado occur. The Sterculia does not occur here, but reasons for this could not be quantified in
this study. However, as the trees do not occur there it seems that Sterculia prefers fertile soils,
avoids anoxic conditions and does not cope with fire.
53 Sterculia trees were seedlings with a height < 1.50 m and were therefore excluded
from the allometric comparison. A power regression indicates that there is a strong relation
between the tree diameter and tree height of Sterculia trees (r2 = 0.87, y= 1.529 * x^0.513, Fig.
6).
Hieght of tree ( m)
25
20
15
10
5
0
0
25
50
75
100
125
150
175
DBH of Sterculia(cm)
Figure 6. Power regression between the height (m) of the S. apetala and the diameter at
2
breast height (cm) with r = 0.87, N = 136, y= 1.529 * x^0.513, p < 0.001).
A logistic binary regression (Fig. 7) shows that the probability of being reproductive increased
sharply with tree diameter (cm) (p= 1/(1 + e^-(-5.645 + 0.115x)), Nagelkerke r2 = 0.75, Wald =
35.466, p < 0.001). The smallest tree that had fruits was 33.5 cm, whereas the tree has 50%
probability to be reproductive at a DBH of 49.0 cm (Fig. 7).
15
1
0.9
Reproductive probability
0.8
0.7
0.6
0.5
Measured values
0.4
Probability
0.3
0.2
0.1
0
0
50
100
150
Figure 7. Logistic binary
regression with probability
curve for being reproductive as
a function of tree diameter (cm)
with p= 1/(1 + e^-(-5.645 +
0.115x)), N = 173.
Sterculia DBH (cm)
5.4 Presence of nesting sites in Sterculia
In the 90 plots measured, seven manduvi trees were found with a pre-existing cavity in their
trunk. One was on the ground and therefore not a potential macaw’s nest. As research of
Santos Jr et al. (2006) indicated, only trees with a diameter > 50.0 cm could potentially have a
cavity suitable for a macaw pair. Six individuals out of 56 Sterculia trees (10.7%) with a DBH of ≥
50 cm in the plots had cavities with a nesting potential for the Hyacinth Macaw (range (min,
max) tree height (13.5 m, 15.9 m), DBH (66.1 cm, 93.4 cm), height of cavity (5.1 m, 7.5 m)).
Vegetation type (χ2 = 2.935, df = 2, p = 0.230), grazing (χ2 = 1.052, df = 2, p = 0.591) and
proximity to human disturbance (χ2 = 0.489, df = 2, p = 0.783) did not have a significant
influence on the presence of cavities.
Six cavities in 90 plots with a total surface of 14.4 ha gives 0.42/ha potential nest cavities
in the vegetation types included in this study, but does not take into account other land covers
like riparian vegetation, lakes and rivers in the Pantanal. Outside the plots two other cavities in
S. apetala individuals were recorded. With the six cavities from the plots and two cavities
outside the plots a binary logistic regression relating the probability of occurrence of cavities of
the hyacinth macaw in trunks of Sterculia apetala as a function of diameter at breast height
(DBH) has been performed (Fig.8) (p = 1/(1+ e^(7.079-0.067x)), Nagelkerke r2 = 0.42, Wald =
11.607, p = 0.001). Cavitation probability is higher than 50% once trees have attained 100 cm
DBH.
16
1
0.9
Cavity probability
0.8
0.7
0.6
0.5
Measured
0.4
Probility
0.3
0.2
0.1
0
0
50
100
150
Figure 8. Logistic binary regression
with probability curve for the
presence of a cavity as a function
of tree diameter (cm) with p = 1/(1
+ e^(7.079 - 0.067x)), N = 109.
Sterculia DBH (cm)
As this study did not take place during the breeding season of birds the occupation of
cavities and the nest use could not be recorded. The potential cause of a cavity in the trunk
could neither be identified.
5.5 Population structure and density of Schelea phalerata and Acrocomia aculeata
The palms acurí (Schelea phalerata) and bocaiúva (Acrocomia aculeata) provide the food source
of the Hyacinth Macaws. The palms occur in all five vegetation types, but they are not very
common in grass and cerrado systems (Fig. 9a-b). The acurí density in general is much higher
than the bocaiúva density. The acurí density differs amongst vegetation types (χ2 = 66.278, df =
4, p < 0.001) with significant pairwise differences between all vegetation types (Fig. 9a). Acurí
attains its highest density in the forest, followed by cerradão. The bocaiúva density also differs
amongst vegetation types (χ2 = 24.738, df = 4, p < 0.001), but with the bocaiúva the density is
similarly high in cerradão, forest and cleared field, and similarly low in grass and cerrado (Fig.
9b).
Acuri density )N/ha)
d
100
80
c
60
40
e
20
a
b
0
Grass
Cerrado
Cerradão
Forest
Cleared
Field
Bocaiuva density (N.ha)
a. Acuri density (N/ha)
120
20
18
16
14
12
10
8
6
4
2
0
b. Bocaiúva density (N/ha)
b
b
b
a
a
Grass
Cerrado
Cerradão
Forest
Cleared
Field
Figure 9a-b. Total average tree density (N/ha) of acurí (Schelea phalerata) and bocaiúva (Acrocomia aculeata) in the five
vegetation types with the lower size limit in acurí of 2.23 trees/ha and in bocaiúva 0.83 trees/ha. The errors bars show
standard error of the mean and the same letters indicate similarity in density.
17
10
9
8
7
6
5
4
3
2
1
0
a. Population structure acuri (N/ha)
Bocaiuva trees (N/ha)
Acuri trees (N/ha)
The overall population structure of acurí and bocaiúva are shown in Fig. 10a-b. The
population structure of acurí seems to have a partly negative exponential size distribution with
a slight dip in the height classes 0.5 – 1.5 m. The population structure of bocaiúva on the other
hand seems to have an optimal curve, with a peak in the height class of 8-10 m.
10
9
8
7
6
5
4
3
2
1
0
b. Population structure bocaiúva (N/ha)
2-4
Height classes (m)
4-6
6-8
8-10 10-12 12-14 14-16
Height classes (m)
Figure 10a-b. The total population structure of acurí (Schelea phalerata, N = 589) and bocaiuva (Acrocomia aculeata,
N = 115) in which the trunk height is put into classes with 0.5 m interval in the acurí case and 2 m with bocaiuva.
As the Hyacinth Macaws depend on the nuts of acurí and bocaiúva, the reproductivity of
these palms is analysed. A binary logistic regression relating the probability of reproductiveness
of the palm as a function of the palm trunk height (m) has been performed (Fig. 11a-b). When
acurí attains a stem height of 1.1 m it has 50% probability to be reproductive whereas for
bocaiúva this threshold lays at 4 m. The minimum trunk size for acurí to be reproductive is 0.15
m, together with the leaves the acurí palm is 2.00 m (p =1/(1 + e^(3.254 -2.901x)), Nagelkerke r2
= 0.73, Wald = 166.333, p < 0.001). For bocaiúva this is 4.50 m with a total height including leaf
top of 5.40 (p =1/(1 + e^(2.435 - 0.597x)), Nagelkerke r2 = 0.32, Wald = 16.245, p < 0.001).
Bocaiuva reproductivity
1
1
0.9
0.9
0.8
0.8
0.7
0.6
0.5
Measured
0.4
Probability
0.3
0.2
Reproduction probability
Reproduction probability
Acurí reproductivity
0.7
0.6
0.5
0.2
0.1
0
0
1.00
2.00
3.00
4.00
5.00
Probability
0.3
0.1
0.00
Measured
0.4
0.00
5.00
10.00
15.00
Acurí height (m)
Bocaiuva height (m)
Figure 11a-b. Logistic binary regression with probability curve for being reproductive as a function of tree trunk height
(m) for both acurí (Schelea phalerata, N = 589) with p =1/(1 + e^(3.254 -2.901x)) and bocaiúva (Acrocomia aculeata, N
= 115) with p =1/(1 + e^(2.435 - 0.597x)).
18
6) Discussion
The aim of this study was to to evaluate the availability and regeneration of Sterculia apetala in
the southern Pantanal. Besides the population structure of Sterculia and the potential nesting
cavities, this study looked at the population structure of the palm trees Schelea phalerata and
Acrocomia aculeata whose fruits provide the major food source of the Hyacinth Macaw.
6.1 Population structure and density of Sterculia
I hypothesized that, because of its light-demanding nature, Sterculia would have higher
densities in more open vegetation types like cerrado, cerradão and in forest edges, and a lower
density in grass vegetation because of flooding and fire. The expected high density in cerrado,
cerradão and in forest edges turned out to be untrue (Fig. 2). Although the species is light
demanding, Sterculia apetala does not occur in grass and cerrado vegetation, but they are
relatively abundant in cerradão, forest and cleared field. I further hypothesized a low density in
grass, which turned out to be the case. Grass areas are the seasonally flooded areas in the
Pantanal and the oxygen deprivation during flood together with the fire occurrence and the soil
texture are likely to limit the establishment of trees like Sterculia (Pott et al. 2011). Although
cerrado is also part of the cordilleras and does not get flooded, the fact that the tree does not
grow there might be due to the soil conditions in the savannah-like ecosystem (Kricher 2011).
For the population structure I expected more seedlings (≤ 5 cm stem diameter) in semiopen areas (cerrado and cerradão) than in dense forest areas, as the species is light demanding.
I hypothesized relatively many seedlings and a negative exponential distribution with
decreasing numbers over time or with increasing diameter. I did find a relatively high number of
seedlings and a stable number of adults in the diameter classes of 11-40 cm, which was
followed by discontinuous recruitment in the older trees (Fig. 3a-d). Santos Jr. et al. (2007)
studied the population structure of manduvi trees taller than 1.5 m in three sub-regions
(Aquidauana, Miranda and Nhecolândia) in the Pantanal. They also found many seedlings with a
diameter up to 5 cm and found low recruitment in classes of DBH larger than 5 cm. Their overall
population structure in three areas show some sort of discontinuous recruitment with a
reduction in the occurrence of individuals greater than 50 cm DBH and very few individuals with
a DBH larger than 110 cm, similar to the results in this study. However, Johnson et al. (1997)
found a negative exponential recruitment of Sterculia apetala in the Pantanal in pasture areas
where cattle has been excluded for at least 5 years. Instead of negative exponential, the
population structure in the different vegetation types in this study is irregular.
From the static picture of the population structure I tried to describe the population and
regeneration dynamics. Sterculia seems to have a relatively good reproduction (as indicated by
the many small saplings) and discontinuous recruitment (as indicated by the dips and peaks in
the population structures at 41-50 cm and 51-60 cm, Fig. 3a). Such peaks in the population
structure might be explained by the light-demanding nature of species, which regenerates
when rare, large gaps are formed (Bongers & Popma 1988). According to Bongers and Popma
(1988) three different types of population structures in forest can be distinguished; 1) good
reproduction and continuous recruitment (the negative exponential curve), which probably
19
indicates a shade-tolerant species; 2) good reproduction and discontinuous recruitment, which
probably indicates a light-demanding species that regenerates when rare, large gaps are
formed, and 3) good reproduction but bad recruitment. Due to the good reproduction but
discontinuous recruitment of Sterculia in my study, I would describe this curve as a type 2 in the
classification of Bongers & Popma (1988). The apparent peaks and dips in the Sterculia
population structure could also be explained by size-dependent growth and mortality as
described by Zuidema and Boot (2002) for the Brazilian nut (Bertholletia excelsa).
Another potential explanation is that trees are going through a bottleneck in the first life
stages and that there is low mortality in the next life stages. Zuidema and Boot (2002) found
that Bertholletia seedling dynamics were characterized by high rates of recruitment and
mortality. Sterculia is relatively abundant as seedling, but decrease rapidly after the first phase.
Mostacedo and Fredericksen (1999 in Zuidema & Boot 2002) found that high turnover rate in
seedlings and strong influence of climatic circumstances cause seedling abundance to vary
greatly in time. This implies that seedling abundance alone is an unreliable indicator for
Bertholletia regeneration potential and perhaps also for Sterculia regeneration (Mostacedo &
Fredericksen 1999 in Zuidema & Boot 2002).
Another theory is that there might actually be continuous recruitment with some peaks
after establishment opportunities due to large disturbances or more successful years. Peaks in
recruitment are driven by oscillations in the macroclimate with wet years and droughts as
historical events (Middendorp et al. 2013). Surprisingly, the population structure is similar in
three vegetation types where the amount of light available and vegetation cover differs from
one another. This suggests that the population structure is an emergent property of the typical
population dynamics of the species.
Light-demanding species tend to invest heavily in leaves and extension growth. This has
been observed in Sterculia seedlings where the leaves are 5-10 times larger than the leaves of
adult Sterculia trees. This can maximize their potential growth rate when resources are ample,
but limit their survival when resources are scarce (Wright et al. 2003). Sterculia also tends to
grow faster in cleared field compared with forested areas (Leuzinger pers. comm. 2013)
indicating the effect of more light available. Wright et al. (2003) state that light-demanding
species are relatively rare as seedlings and saplings because seedlings and saplings are
ephemeral, either dying quickly if shaded, or growing rapidly into larger size classes if light
levels remain high. In contrast, shade-tolerant species are relatively abundant as seedlings and
saplings because seedlings and saplings are persistent, with most surviving and growing slowly
in deep shade. In this study many seedlings with a height < 1.50 m were found, but relatively
few individuals of more than 1.50 in height and up to a diameter of 10 cm. Conversely, Wright
et al. (2003) also acknowledge that gap-dependent or light-demanding species can establish
and thrive in tree-fall gaps where light levels are high and root competition is reduced. This
statement seems more in line with the results from this study.
During the field measurements and observations outside the plots it seemed as if the
Sterculia trees grow in some sort of cluster. If they occur in a certain area, there are many trees
20
of approximately the same size and likely the same age. This might be partly due to specific
large gap disturbances that stimulate community wide seedling establishment (Hubbell et al.
1999). Perhaps in certain years growth peaks were present with this species, but this could not
be quantified. With the use of tree-ring analysis one could investigate the age structure of the
trees in potential clusters (Middendorp et al. 2013).
6.2 Influence of vegetation type, grazing and disturbance on regeneration of Sterculia
For the impact of vegetation type on regeneration of the trees (≤ 5 cm stem diameter) I
hypothesized that, because of its light-demanding nature, Sterculia would have higher
regeneration in more open vegetation types like cerrado, cerradão and in forest edges, and a
lower density in grass vegetation because of flooding, fire and high competition which would
reduce the establishment opportunities. As discussed in the population structure, there is no
Sterculia regeneration in grass en cerrado, which is likely due to the oxygen deprivation during
floods together with the fire occurrence and the soil texture (Pott et al. 2011). By looking at the
vegetation types where Sterculia does occur, there were no differences in densities between
cerradão, forest and cleared field. They all grow on the cordilleras, the higher grounds of the
Pantanal, which are likely to have similar features in soil conditions and water availability. The
difference between cerradão and forest is small as they are both classified as dry forests on
ancient levees of cordilleras (Pott et al. 2011). The clearing of forest did not seem to have an
effect on the Sterculia and with that on the nesting opportunities of the Hyacinth Macaw.
However, this might be very site specific, as the Fazenda Barranco Alto kept some adult trees
when they deforested the area 30 years ago. With adult trees there are potential seed sources
nearby, and this has resulted in sufficient natural regeneration. Although cleared field might
not have had a negative effect on this tree and bird at the Fazenda, it is plausible that the
clearing of forest will have effects on biodiversity, microclimate, animal behavior and soil
conditions in the long term as it does in other areas of Brazil (Laurance et al. 2000). Especially as
there are fewer trees on the cleared field and therefore less litter fall, which will result in less
soil organic matter. Consequently, there will be fewer nutrients available for the plants as the
soil becomes less fertile and this might result in a lower success rate in trees in future.
Grazing was expected to either negatively influence regeneration as cattle would eat the
seedlings, or grazing would have a positive influence as it could give less competition of
seedlings with grasses. However, both did not turn out to be true as there were no differences
in regeneration density and tree density between areas with different grazing intensities. Yet,
the amount of bare ground cover and the grass height did have an influence on the Sterculia
density, which indirectly might be caused by cattle grazing. In other studies the discontinuous
recruitment has been explained by the time spend grazing in the Sterculia areas (Johnson et al.
1997). Grazing especially damages the seedlings. Although in this study cattle has not been
observed in the forest and cerradão, they might spend more time there in winter to find shelter
(Desbiez et al. 2009). At Fazenda Barranco Alto the effect of grazing on seedlings has not been
found. Seedlings also survive in the cleared field where there is a lot of grass cover and where
cattle graze. Johnson and colleagues (1997) found a clear negative exponential distribution in
height classes of Sterculia in areas where cattle have been excluded for more than 5 years. This
21
may mean that exclusion of cattle enhances the tree regeneration and gives many seedlings,
while only a few will actually succeed into adults. However, in areas where cattle is present for
6 months or more per year, the population structure was found to be more irregular (Johnson
et al 1997). They indicated gaps in the population structure with no individuals of 1-5 m in
height and very few manduvi trees larger than 12 m (Johnson et al. 1997). In this study a similar
irregular distribution has been observed in general, but without an effect of grazing. However,
as the study of Johnson et al. (1997) measured trees in the field where cattle has only be
excluded for 5 years it is questioned whether this could be used as an explanation for the total
Sterculia population structure.
Disturbance was expected to create opportunities and positively influence regeneration,
but this has not been recorded in this study. The scope of disturbance in this particular area is
unknown, but does not have an effect on the survival and development of Sterculia. It might
have effects on the behavior of birds, but this has not been investigated. In the study of Pinho
and Nogueira (2003), it turned out that Hyacinth Macaws do not avoid areas with human
disturbance when choosing their nesting sites. Due to the fact that the variables of grazing and
human disturbance were categorical there was limited resolution with these factors.
6.3 Influence of environmental variables on Sterculia
I hypothesized that Sterculia regeneration would increase with soil fertility (because of
enhanced resource availability), would decrease with herbaceous cover (because of increased
competition), and would also decrease with flooding intensity (because of a lack of oxygen). Soil
color has been used as an indicator for soil fertility, where darker soils are more fertile. Darkcoloured soils have more soil organic matter and therefore a larger reservoir of carbon,
nutrients and energy (Jenkinson 1988, in Craswell & Lefroy 2001), which is in line with the
hypothesis. The presence of litter on the ground as well as soil color (Fig. 5) has showed to have
a positive influence on the presence of Sterculia in an area. This could be explained by the
amount of nutrients in the soil where there is sufficient litter fall during the year and therefore
turnover of litter to soil organic matter. Decomposition of organic matter enhances soil fertility
and will therefore enhance tree regeneration and growth (Kricher 2011).
As expected, bare ground cover has a positive impact on the Sterculia density where less
herbaceous cover will decrease competition between Sterculia seedlings and other plants.
However, even with low herbaceous cover the amount of light available can be limiting as the
canopy might be closed due to adult trees. This asymmetric competition indicates that
seedlings and saplings are much more impacted by adult trees than adult trees are by seedlings
and saplings (Harms et al. 2004).
Grass cover and height turned out to have a negative influence on Sterculia density.
Grass cover and tall grass together with the soil type (sand) seems to keep the grass system
going and limits the growth of Sterculia. This is likely linked with the occurrence of flooding and
fire in the lower parts of the Pantanal, although this could not be quantified in this study. The
Sterculia does not grow in areas where there is high grass density, and this could, amongst
22
other reasons, be due to flooding, fire, poor soil and grass competition. The vegetation types, as
described in section 6.2, do not show significant difference indicating that the soil conditions
are relatively similar on the cordilleras (the higher ground). Colinas et al. (1994) showed that
increased seedling growth has been associated with increased nutrient mineralization where
soil animals stimulated microbial turnover in soils. This could mean that soil fertility and
rhizosphere presence are the main factors for successful regeneration of Sterculia.
At the start in this study tree diameter was chosen to do most analyses with as the size
and circumference of the trunk seemed to be more representative for suitable cavities for
nesting. The power regression (Fig. 6) indicates that there is a strong relation between the tree
diameter and tree height of Sterculia trees. Therefore it is eligible to either use the height or
the diameter of Sterculia when referring to potential nesting sites in these trees. Pizo et al.
(2008) and Johnson et al. (1997) used tree height in their analysis while Santos Jr. et al. (2006,
2007) used DBH measurements for potential nesting trees.
Once Sterculia trees have a diameter of 50.0 cm the chance to be reproductive is 50%.
According to Santos Jr. et al. (2007) trees with a DBH of 50.0 cm are approximately 60 years.
Therefore it takes quite some time before the tree starts to fruit. The size however might
fluctuate between areas as in cleared field area younger trees are already much bigger than
trees of the same age in forested areas, probably due to the light availability (Leuzinger pers.
comm. 2013).
6.4 Presence of nesting sites in Sterculia
The hypothesis of increased probability on a nesting cavity when trees are bigger turned out to
be right, which is not very surprising. The chance of a cavity and therefore a potential nesting
sites increases with larger tree diameter. I found in Fazenda Barranco Alto a 10.7% presence of
cavities in adult Sterculia trees (DBH ≥ 50.0 cm), which is twice the percentage (5%) compared
to a study in the south central of the Pantanal (Guedes 1993 in Johnson et al. 1997). The
minimum tree height of 13.5 m and DBH of 66.1 cm is higher than the 50.0 cm diameter found
by Santos Jr et al. (2006). In their research all the trees with a DBH > 100.0 cm had a nest cavity,
while in this study only two out of five trees with DBH > 100.0 cm had a potential nesting cavity.
The 0.42 nest cavities per ha in this study are much higher than the estimated
theoretical density of 0.0011 nest cavities/ha in the study by Pinho and Nogueira (2003). The
observed density in that study varied from 0.0002 – 0.0005 per ha in the Pantanal, but some
potential nest sites were not occupied. The theoretical density of potential cavities in this study
is much higher but this can be partly explained by the fact that this study only focused on five
vegetation types and did not include the area covered by lakes, rivers, riparian vegetation and
other vegetation types. However, as unoccupied cavities were recorded it is questioned what
really limits the Hyacinth Macaw. There are two factors involved. The first is the availability of
vegetation in which the Sterculia occurs and with that the possibility for suitable nesting sites.
The second is the occupation of nesting sites in an area, which is directly influenced by behavior
of the Hyacinth Macaw. Unoccupied nesting sites might be caused by the preference of the
23
Hyacinth Macaw to reproduce in rather open forests and borders of forest patches (Pinho &
Nogueira 2003). Pinho and Nogueira (2003) explained this by a greater area of vision and easier
access in forest borders for Hyacinth Macaws. Preference could also be influenced by food
availability as the fruit production of palms may be lower when the palm is shaded (Salis et al.
1996 in Pinho and Nogueira 2003). As this study did not take place during the breeding season,
the nest use could not be investigated. It is therefore logical that vegetation type, grazing and
proximity to human disturbance did not have an influence on the presence of cavities as this is
a natural process and all trees have a similar chance of a natural cavity. However, the use of
these cavities can be affected by the factors of vegetation type, grazing and disturbance. Pinho
and Nogueira (2003) found that cattle presence and human disturbance had no correlation with
nesting success.
Hyacinth Macaws tend to have nest site fidelity in the Pantanal and the same pair could
be using the same tree cavity for breeding in consecutive years (Guedes & Harper 1995 in Faria
et al. 2008). Species that are not primary excavators, like the Hyacinth Macaw, are more often
short of nesting sites (Newton 1994, in Johnson et al. 1997). However, in this study as well as in
the research of Pinho and Nogueira (2003) in the northern Pantanal the availability of potential
nest sites does not seem to be the limiting factor for the population of Hyacinth Macaws.
In the past, Hyacinth Macaws at the Fazenda Barranco Alto have been observed using a
total of four trees to make their nests in pre-existing cavities in the tree trunk: Tarumã (Vytex
cymosa), Ximbuva (Enterolobium contortisiliquum), Angico Branco (Albizia nipioides) and the
Manduvi (Sterculia apetala) (Leuzinger pers. comm. 2013). Currently there does not seem to be
a problem with the Sterculia in this part of the Pantanal, but if the tree becomes scarcer, it
might turn out that the birds will adapt and use cavities in other trees more frequently.
Moreover, results in other parts of the Pantanal have been and can be completely different and
generalizations should not be made after the results of this study.
6.5 Population structure and density of Schelea phalerata and Acrocomia aculeata
For the population structure of the palm trees acurí (Schelea phalerata) and bocaiúva
(Acrocomia aculeata) I expected little influence of vegetation type and management practices
as they do very well in several habitats. However due to their light demanding nature I
hypothesized that they would occur less in areas with a high woody cover and that they would
also manage to survive in areas with occasional flooding. A higher total number of Schelea
phalerata and Acrocomia aculeata than of Sterculia was expected because of two reasons. First
they establish easily, and second the farmers would not cut them as the palms are used as food
for cattle.
The palm trees do occur in all vegetation types measured in this study. Acurí is,
compared with bocaiúva, much more common in this part of the Pantanal. The lower size limit
in density of acurí is 2.23 trees/ha and in bocaiúva 0.83 trees/ha, but the density fluctuates
between vegetation types (Fig.9a-b). The palm trees have the highest densities in forest and
cerradão. This may be due to the perching of birds in trees of these vegetation types and
24
therefore increasing site-specific seed dispersal. The site-specific seed dispersal could be
enhanced by trees and shrubs, facilitating seedling development by providing improved growth
conditions, including for example, lower irradiance and reduced rates of evapotranspiration
(Gómez-Aparicio et al. 2005).
During this study it showed that acurí occurs everywhere and in all sizes while there
were very few small bocaiúva observed. The population structure of acurí seems to have a
partly negative exponential size distribution with a slight dip in the height classes 0.5 – 1.5 m.
The acurí has good reproduction but not such recruitment and would be a curve type 2 in the
classification of Bongers and Popma (1988). The population structure of bocaiúva on the other
hand seems to have an optimal curve, with a peak in the height classes of 8-10 m. The bellshaped size distribution of bocaiúva indicates that there is lack of natural regeneration and
establishment with a high proportion of individuals in the population being intermediate in size
based on height and DBH (Puechagut et al. 2013).
As macaws and other birds are dependent on the nuts of the palm trees, their
reproductivity is essential. When acurí attains a stem height of 1.1 m it has 50% probability to
be reproductive whereas for bocaiúva this threshold lays at 4 m. Salis et al. (1996 in Pinho &
Nogueira 2003) found that the fruit production of palm species is lower when palms are
shaded. It seems that where Sterculia is abundant, the palm trees are also abundant indicating
that there are perfect living conditions for the Hyacinth Macaw. This is in line with the study of
to Pinho and Nogueira (2003) in the northern Pantanal where food offer and availability of
potential nest sites does not seem to be the limiting factor for the population of Hyacinth
Macaws. However, caution should be taken for future use of palm trees. The uprooting of A.
phalerata observed in other studies could affect the recruitment of the palm as well as
potential trampling by cattle (Desbiez et al. 2001). Delobel et al. (1995) showed that palms in
the Peruvian amazon were susceptible to infestations by bruchid beetles. Up to 97% of the
acurí fruits were infested with corresponding infestation rates of seeds reaching up to 84%
(Delobel et al. 1995).
6.6 Strengths and limitations of this study
This thesis studied differences in population structure of Sterculia in five different vegetation
types and not just the general composition in the southern Pantanal. By including the cleared
field, I was also able to study the influence of clearing for farm expansion. Another strength of
this study next to the use of different habitats is that I looked explicitly at the relation of
environmental variables with the tree density. In this research 90 plots of 40 x 40 m were used,
but 30 plots of these were in a vegetation type where the Sterculia does not occur. Because the
Sterculia seems to grow in clusters, it would be recommended to establish more plots in further
research. Another limitation of this study is that the research was static and the purpose of the
measures was to find an explanation of the population and regeneration dynamics. Due to
financial constraints soil nutrients could not be quantified which would have been useful in this
research context.
25
6.7 Recommendations for further research
This study showed that the light demanding Sterculia appears to have a relatively good
reproduction and discontinuous recruitment. There might actually be continuous recruitment
with some peaks after establishment opportunities due to large disturbances or more
successful years. Or there is a large bottleneck in the first regeneration phase but once a tree
reaches a diameter of 10 cm, chances of survival are high and trees will only die of senesce. To
investigate whether the trees really only establish themselves when gaps are accidentally
formed or whether it is caused by historical events, the population should be monitored over
several years, or pulses in establishment can be inferred using tree-ring analysis. Middelkoop et
al. (2013) advise to use the combined application of tree-ring analysis with spatial statistics to
reconstruct disturbance histories. Growth rates are important because they determine how
much time it takes for a tree to grow to a size where it can have cavities. Santos Jr. et al. (2006)
found annual radial growth rates of Sterculia in sub-regions of Miranda, Aquidauana and
Nhecolândia in Mato Grosso do Sul varying between 2.97 and 3.81 mm/year. As growth rates
vary a lot locally and potentially vary between vegetation types with different light
availabilities, it is suggested to measure growth rates again in the southern Pantanal, either by
direct monitoring, or by measuring tree rings.
It seems that the soil conditions determine whether Sterculia occurs in specific
vegetation types, but in order to verify this more measures, such as nutrient and moisture
content, and soil samples should be taken than just the vegetation cover, soil type and soil
color. This thesis studied the presence and absence of cavities, which could function as a
potential nest for the Hyacinth Macaw. However, to determine whether these nests are
actually used by the Hyacinth Macaw, research should take place during the breeding season
(July-November) and the behavior of the birds should be monitored. The short and long term
effects of flooding and fire on soil fertility and vegetation cover should be investigated to
examine the ecological consequences for Sterculia and the palm trees.
6.8 Recommendations for management
To stimulate conservation and to protect areas in the Pantanal, the development of habitat
management strategies for cattle ranching in the Pantanal wetland are necessary to achieve
long term conservation for the Hyacinth Macaw as well as the other threatened and more
common species. As Sterculia only grows in cordillera fragments (higher grounds) and this
vegetation just covers 6% of the vegetation area of the Pantanal (Silva et al. 2000 in Pizo et al.
2008), precaution is needed in the management of these areas.
It is suggested to set up a monitoring plan at Fazendas where cattle ranching,
ecotourism and conservation are combined. By monitoring the vegetation and wildlife one has
a management policy that is goal orientated and adaptive in approach. The principles of
Strategic Adaptive Management (SAM), as regularly used in Southern Africa, looks at an
adaptive planning process and would be a useful tool in the Pantanal (Vos et al. 2000). Forming
an important component of SAM, thresholds of potential concern (TPCs) provide measureable
endpoints or define acceptable limits of change in ecosystem or biodiversity composition,
26
structure and function. Minimum tree density, population size and structure could be set as
potential threshold of potential concern once they have been identified. The monitoring of
TPCs represents goals/outcomes towards which the success of ecosystem management can be
measured (Foxcroft 2009, Gaylard & Ferreira 2011). If this would be implemented in the
Pantanal, conservation management would be allowed to modify practices through adaptive
management which can be a helpful approach when knowledge is limiting (Boshoff et al. 2001).
Food sources are abundant where Sterculia is also abundant and the food sources even
occur in areas where there is no Sterculia. In areas where natural nesting availability is absent,
tree establishment and growth should be stimulated. Saplings could be planted on the
cordilleras where no flooding occurs and where the soil has sufficient nutrients and plenty bare
ground to reduce competition. Using reported annual radial growth rates up to 3.81 mm/year
(Santos Jr. et al. 2006) the trees could have attained a stem diameter of > 66 cm (which is the
start of potential nest cavities), after 85 years and by this time 75% of the trees is reproductive.
However, as tree growth seems to differ a lot locally it is suggested to measure growth rate in
this area and in different vegetation types. Once there are sufficient reproductive trees in an
area, natural regeneration should occur and planting is no longer required as long as the
management team protects old trees instead of cutting them. Although natural regeneration
and the use of cavities in tree trunks are preferred, a possible alternative is to place artificial
nest boxes similar to, or together with, the Arara Azul project in the Pantanal (Guedes 1999).
The addition of artificial nest boxes has also proved to increase the number of breeding adults
of different psittacine species, such as the Green-rumped Parrotlet (Forpus passerinus) in
Venezuela (Beissinger & Bucher 1992, Newton 1994 in Vaughan et al. 2003).
27
Conclusion
The objective of this study was to evaluate the availability and regeneration of Sterculia apetala
in the southern Pantanal and also looked at the occurrence of nesting cavities and the
population structure of the palm trees Schelea phalerata and Acrocomia aculeata of which the
majority of the Hyacinth Macaw’s diet consists.
The food offer and availability of potential nest sites does not seem to be the limiting
factor for the population of Hyacinth Macaws in this part of the Pantanal. There are relatively
many nesting sites, the palm trees are abundant, and produce fruits at relatively small size. The
future for nesting availability is uncertain due to the irregular population structure of Sterculia
trees. There are three alternative explanations for this irregular population structure. First, this
irregularity could be explained by discontinuous recruitment because of the light-demanding
nature of the species, which requires gaps to establish. Or second, there might actually be
continuous recruitment with some peaks after establishment opportunities due to large
disturbances or more successful years that causes irregularity. Or third, there is a large
bottleneck in the first regeneration phase but once a tree reaches a diameter of 10 cm, chances
of survival are high and trees will only die of senesce.
To enhance the use of nesting sites in Sterculia in the long term the cordilleras (higher
grounds) will need protection from mining, clearing and cattle grazing. To ensure regeneration
of Sterculia, it is recommended to set up a monitoring plan for several years to evaluate tree
establishment, growth and survival and to evaluate trends in regeneration. In this case it is
possible to intervene or stimulate recruitment when it turns out to be necessary.
28
References




















Alho, C. J. R. 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to
environmental degradation. Brazilian Journal of Biology 68 (4), 957-966.
Barot, S., Gignoux, J. & Menaut, J. C. 1999. Seed shadows, survival and recruitment: how simple
mechanisms lead to dynamics of population recruitment curves. Oikos 86, 320-330.
Barthlott, W. & Winiger, M. 2001. Biodiversity: A Challenge for Development Research and Policy.
Second edition. Springer-Verslag Berlin Heidelberg New York.
BirdLife International. 2012. Species factsheet: Anodorhynchus hyacinthinus. Downloaded from
[http://www.birdlife.org] on 15/12/2012.
Bongers, F. & Popma, J. 1988. Trees and gaps in Mexican tropical rain forest: species differentiation
in relation to gap associated environmental heterogeneity. PhD thesis, Utrecht University, Utrecht.
Boshoff, A. F., Kerley, G. I. H. & Cowling, R. M. 2001. A pragmatic approach to estimating the
distribution and spatial requirements of the medium-large-sized mammals of the Cape Floristic
Region, South Africa. Diversity and Distributions 7 (1), 29-43.
Colinas, C., Perry, D., Molina, R. & Amaranthus, M. 1994. Survival and growth of
Pseudotsugamenziesii seedlings inoculated with biocide-treated soils at planting in a degraded
clearcut. Canadian Journal of Forest Research 24(8): 1741-1749.
Collar, N. J. & Juniper, A. T. 1992. Dimensions and causes of the parrot conservation crisis. Chapter 1
(p. 1 – 24) in Beissinger, S. R. & Snyder, F. R. (eds). New parrots in crisis: solutions from conservation
biology. Smithsonian Institution Press, Washington D.C.
CITES. 2012. The CITES appendices. Downloaded from [http://www.cites.org/eng/app/index.php] on
15/01/2013.
Craswell, E. T. & Lefroy, R. D. B. 2001. The role and function of organic matter in tropical soils.
Nutrient Cycling in Agroecosystems 61, 7-18.
Damesceno Jr., G.A., Semir, J., Santos, F. A. M. & Freitas, H. 2005. Structure, distribution of species
and inundation in a riparian forest of Rio Paraguai, Pantanal, Brazil. Flora 200, 119-135.
Delobel, A., Couturier, G., Kahn, F. & Nilsson, J. A. 1995. Trophic relationships between palms and
bruchids (Coleoptera: Bruchidae: Pachymerini) in Peruvian Amazania. Amazonia 13, 209-219.
Desbiez, A. L. J., Santos, S. A. & Keuroghlian, A. 2001. Predation of young palms (Atalea phalerata)
by feral pigs in the Brazilian Pantanal. Suiform Soundings 9(1), 35-40.
Desbiez, A. L. J., Bodmer, R. E. & Santos, S. A. 2009. Wildlife habitat selection and sustainable
resources management in a Neotropical wetland. International Journal of Biodiversity and
Conservation 1 (1), 11-20.
Donatti, C. I. 2011. Ecological studies on seed dispersal networks insights from a diverse tropical
ecosystem. PhD dissertation at Stanford University, California.
Dubs, B. 1992. Birds of Southwestern Brazil. Schellenberg Druck AG, Switzerland.
Dvorak, W. S., Urueňa, Morena, L. A. & Goforth, J. 1998. Provenance and family variation in Sterculia
apetala in Colombia. Forest Ecology and Management 111, 127-135.
Faria, P. J., Guedes, N. M. R., Yamashita, C., Martuscelli, P. & Miyaki, C. Y. 2008. Genetic variation
and population structure of the endangered Hyacinth Macaw (Anodorhynchus hyacinthinus):
implications for conservation. Biodiversity Conservation 17: 765-779.
Foxcroft, L. C. 2009. Developing threshold of potential concern for invasive alien species:
Hypotheses and concepts. Koedoe 50 (1), Art. #157.
Fraser L. H. & Keddy, P. A. 2005. The World’s Largest Wetlands: Ecology and Conservation.
Cambridge University Press, New York.
29


















Gaylard, A. & Ferreira, S. 2011. Advances and Challenges in the Implementation of Strategic
Adaptive Management beyond the Kruger National Park – Making Linkages between Science and
Biodiversity Management. Koedoe 53 (2), Art. #1005.
Gómez-Aparicio, L., Gómez, J. M., Zamora, R., & Boettinger, J. L. 2005. Canopy vs. soil effects of
shrubs facilitating tree seedlings in Mediterranean montane ecosystems. Journal of Vegetation
Science 16, 191-198.
Gottgens, J. IF., Perry, J. E., Fortney, R. H., Meyer, J. E., Benedict, M. & Rood, B. E. 2001. The
Paraguay-Paraná Hidrovía: Protecting the Pantanal with Lessons from the Past. BioScience 51 (4),
301 -308.
Groom, M. J., Meffe, G. K. & Carroll, C. R. 2006. Principles of Conservation Biology. Third Edition.
Massachusetts: Sinauer associates.
Guedes, N. M. R. 1999. Installing and monitoring artificial nests by the Hyacinth Macaw in the
Pantanal, Brazil. In: Neotropical Ornithological Congress 6, Book of Abstracts, 155-156. Monterrey y
Saltillo, México.
Guedes, N. M. R. 2004. Management and conservation of the large macaws in the wild. Ornitologia
Neotropical 15, 279-283.
Haase, R. 1999. Litterfall and nutrient return in seasonally flooded and non-flooded forest of the
Pantanal, Mato Grosso, Brazil. Forest Ecology and Management 17, 129 -147.
Harms, K. E., Powers, J. S. & Montgomery, R. A. 2004. Variation in Small Sapling Density, Understory
Cover, and Resource Availability in Four Neotropical Forests. Biotropica 36(1): 40-51.
Harris, M. B., Tomas, W., Mourao, G., da Silva, C. J., Guimaraes, E., Sonoda, F. & Fachim, E. 2005.
Safeguarding the Pantanal Wetlands: Threats and Conservation Initiatives. Conservation Biology 19
(3), 714-720.
Holt van, T. 2001. The influences of the Scheelea Phalerata palm and landscape patterns on the
terrestrial mammalian and avian communities of forest islans in the Brazilian Pantanal. MSc-thesis,
University of Florida.
Hubbell, S. P., Foster, R. B., O’Brien, S. T. O., Harms, K. E., Condit, R., Wechsler, B, Wright, S. J. & Loo
de Lao, S. 1999. Light-Gap Disturbances, Recruitment Limitation, and Tree Diversity in a Neotropical
Forest. Science 283, 554-557.
International Union for Conservation of Nature (IUCN). 2012. Categories. Downloaded from
[http://www.iucn.org/about/work/programmes/gpap_home/gpap_quality/gpap_pacategories/] on
15/01/1013.
Johnson, M. A., Tomas, W. M. & Guedes, N. M. R. 1997. On the Hyacinth macaw’s nesting tree:
density of young manduvis around adult trees under three different management conditions in the
Pantanal wetland, Brazil. Ararajuba 5(2), 185-188.
Junk, W. J. & Nunes da Cunha, C. 2005. Pantanal: a large South American wetland at a crossroads.
Ecological Engineering 24, 391-401.
Keuroghlian, A., Eaton, D. P. & Desbiez, A. 2009. Habitat use by Peccaries and Feral Pigs of the
Southern Pantanal, Mato Grosso do Sul, Brazil. Suiform Soundings 8 (2), 9-17.
Kricher, J. 2011. Tropical Ecology. Princeton University Press, New Jersey.
Laurance, W. F., Vasconcelos, H. L. & Lovejoy, T. E. 2000. Forest loss and fragmentation in the
Amazon: implications for wildlife conservation. Oryx 34 (1), 39-45.
Lourival, R., McCallum, H., Grigg, G., Arcangelo, C., Machado, R. & Possingham, H. 2009. A
systematic evaluation of the conservation plans for the Pantanal wetland in Brazil. Wetlands 29 (4),
1189-1201.
30


















Middendorp, R. S., Vlam, M., Rebel, K. T., Baker, P. J., Bunyavejchewin, S.& Zuidema, P. A. 2013.
Disturbance History of a Seasonal Tropical Forest in Western Thailand: A Spatial Dendroecological
Analysis. Biotropica 0, 1-9.
Mittermeier, R. A., de Gusma1o Câmara, I., Pádua, M. T. J. & Blanck, J. 1990. Conservation in the
Pantanal of Brazil. Oryx 24(2), 103-112.
Pinho, J.B. & Nogueira, F. M. B. 2003. Hyacinth Macaw (Anodorhynchus hyacinthinus) reproduction
in the northern Pantanal, Mato Grosso, Brazil. Ornitologia Neotropical 1, 29-38.
Pizo, M. A., Donatti, C.I., Guedes, N. M. R. & Galetti, M. 2008. Conservation puzzle: Endangered
hyacinth macaw depends on its nest predator for reproduction. Biological Conservation 141, 792796.
Pott, A., Oliveira, A. K. M, Damasco Jr., G.A. & Silva, J. S. V. 2011. Plant diversity of the Pantanal
wetland. Brazilian Journal of Biology 71 (1), 265-273.
Prance, G. T. & Schaller, G. B. 1982. Preliminary Study of Some Vegetation Types of the Pantanal,
Mato Grosso, Brazil. Brittonia 34 (2), 228-251.
Puechagut, P. B., Politi, N., Bellis, L. M. & Rivera, L. O. 2013. A disappearing osasis in te semi-arid
Chaco: Deficient palm regeneration and establishment. Journal for Nature Conservation 21, 31-36.
Rylands, A. B. & Brandon, K. 2005. Brazilian Protected Areas. Conservation International 19 (3), 612618.
Santos Jr., A., Hiromi Ishii, I., Guedes, N. M. R., & Almeida de, F. L. R. 2006. Appraisal of the age of
trees used as nests by the Hyacinth Macaw in the Pantanal, Mato Grosso. Natureza & Conservaḉão
4 (2), 180-188.
Santos Jr., A. Tomas, W. M., Ishii, I. H. & Hay, J. D. 2007. Occurrence of Hyacinth Macaw nesting sites
in Sterculia apetala in the Pantanal Wetland, Brazil. Gaia Scientia 1(2), 127-130.
Scariot, A. 1998. Dispersal and Predation in Aconomia aculeata. Principes 42 (1), 5-8.
Seidl, A. F., Vila de Silva dos Santos, J. & Moraes, A. S. 2001. Cattle ranching and deforestation in the
Brazilian Pantanal. Ecologica Economics 36, 413-425.
Snyder, N., McGowan, P., Gilardi, O. & Grajal, A. (Eds.). 2000. Parrots: Status Survey and
Conservation Plan 2000-2004. IUCN, Gland, Switzerland.
Vaughan, C. Nemeth, N. & Marineores, L. 2003. Ecology and management of natural and artifical
scarlet macaw (ara macao) nest cavities in Costa Rica. Ornitologia neotropical 14, 381-396.
Vos, P., Meelis, E. & ter Keurs, W. J. 2000. A framework for the design of ecological monitoring
programs as a tool for environmental and nature management. Environmental Monitoring and
Assessment 61, 317-344.
Wittman, F., Zorzi, B. T., Tizianel, F. A. T., Urquiza, M. V. S., Faria, R. R., Sousa, N. M, Modena, E.,
Gamarra, R. M. & Rosa, A. L. M. 2008. Folia Geobotanica 43 (4), 397- 411.
Wright, S. J., Muller-Landau, H. C., Condit, R. & Hubbell, S. P. 2003. Gap-dependent recruitment,
realized vital rates, and size distributions of tropical trees Ecology 84 (12), 3174-3185.
Zuidema, P.A. & Boot, R. G. A. 2002. Demography of the Brazil nut tree (Bertholletia excelsa) in the
Bolivian Amazon: impact of seed extraction on recruitment and population dynamics. Journal of
Tropical Ecology 18, 1-31.
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