2.5 Statistical procedures
Biomass of individuals was calculated based on the DGL using the
equation: Biomass = 0.173 DGLcm2.295 (Amorim et al.,
2005). We tested the normality of the data using the Shapiro Wilk test
and homogeneity using the Bartlett’s test (Crawley, 2013). Plot values
for richness, abundance, height, diameter, biomass and each physical and
chemical soil property were averaged for each area. The areas were
compared using Student’s T-tests and Pearson’s chi-squared test for
parametric data and non-parametric data, respectively.
We performed Pearson’s correlation analyses to elucidate the
relationships between vegetation and soil properties. Simple linear
regressions were performed between the variables with the highest
correlation, establishing the model which best described the results.
The adult and regenerative strata were also correlated, as the adult
vegetation acts as a vegetation cover and influences the regenerating
stratum. We subsequently generated graphs only for the significantly
correlated variables, using the plot function of the R statistical
software program (R Core Team, 2018). Only the soil properties in the
surface horizons were used in correlation analyses for the regenerating
stratum. As a result, all horizons below the surface horizon were
disregarded in the following analyses.
We performed a non-metric multidimensional scaling (NMDS) ranking to
observe possible ordering in the species composition of regenerating
stratum between the different areas using the metaMDS function of the
vegan software package. In addition, the similarity between environments
was analyzed using the ANOSIM test (Oksanen et al., 2018). All analyzes
were performed using the R Studio 3.5.0. statistical software program (R
Core Team, 2018).
Results
A total of 3,436 individuals were sampled, 2,519 of them in the adult
stratum, distributed in 41 species and 17 families (Appendix 1), which
represent the vegetation cover of our study. A total of 917 individuals
were sampled in the regenerating stratum, with 29 species identified
distributed in 15 families. The species Aspidosperma pyrifoliumMart (Apocynaceae) was the most frequent. The most frequent family was
Euphorbiaceae (six species). Area I presented 526 individuals from the
regenerating stratum, which were distributed in 11 species and six
families. Area II presented 391 individuals, 27 species and 15 families.
Two species were exclusive to Area I, while 18 species and nine families
were exclusive to Area II.
The species were ecologically classified based on their distribution
among the areas, with four categories being established: Aridity
indicators, being dominant or exclusive species from the driest area
(Area I); Sensitive species, being those found only in the most humid
environments (Area II); Tolerant species, mainly distributed in the most
humid environments, however, some individuals were also found in the
drier area, confirming that the species tolerates such conditions; and
finally, Common species, being those that are uniformly distributed
between both areas (Appendix 1).
The NMDS ranking showed a low-stress value (stress = 0.06), and the
similarity analysis showed significant differences between the areas
regarding the composition and abundance of species present in the
regenerating stratum (ANOSIM, r = 0.20; P=0.03) (Figure 2).
Note : Here figure 2 will be inserted
The mean comparison tests between Area I and II showed significant
differences in the seedling diameter and diversity. Area I presented the
largest average diameter of seedlings , and Area II had the highest
average diversity of orders 1 (RegD1) and 2 (RegD2). The Herbivory
Pressure Index in the plots ranged from 0.08 to 13.37, however there was
no significant difference between the areas (Table 1).
Note : Here Table 1 will be inserted
Cambisol was the dominant soil group identified in the study area with
six soil profiles. We also found three Luvisols, one Gleysol, one
Planosol, and one Regosol. All soil properties have high standard
deviation values in Area I and Area II, indicating high soil variability
(Table 2). All A horizons were classified as ochric horizons. They
varied between 2 and 10 cm in thickness. The A horizon in Area I and
Area II is dominantly sandy clay loam and has base saturation above
80%. The Ca2+, Mg2+,
K+ and Na+, and P contents were not
significantly different between Areas I and II. Only the average C and N
levels showed significant differences, with a higher average in Area II
(Table 2).
Note : Here Table 2 will be inserted
The herbivory pressure index showed a weakly positive relationship with
the diameter at ground level of saplings (DGL) (Figure 3b) and a
negative relationship with the diversity of order 0 of the regenerating
stratum (RegD0) (Figure 3c). RegD0 is also showed a positive
relationship with biomass (Figure 3d), diversity (D0) (Figure 3e) and
abundance of the adult stratum (Figure 3f). The DGL of the regenerating
stratum showed a negative relationship with the abundance (Figure 3a)
and biomass of the adult stratum. The abundance of seedlings also showed
a negative relationship with the height of the adult stratum.
The diversity (RegD0) and biomass of the regenerating stratum also
showed positive relationships with soil carbon and nitrogen levels
(Figure 3g and Figure 3h). Despite showing relatively weak
relationships, these linear regressions are all significant (Figure 3).
Note : Here figure 3 will be inserted
Discussion
Our results indicate significant differences in the floristic
composition of regenerating stratum, diversity, DGL, and C and N levels
in the soil between different vegetation cover areas. Species more
resistant to water and anthropic stress and common in degraded areas,
such as A. pyrifolium, C. pyramidales, and T. palmadora(Meiado, 2012; Souza et al., 2015a, 2015b), are dominant in Area I. On
the other hand, Area II presents more than twice the number of species
in the first area, and also shows 18 exclusive species. The Hill numbers
D1 and D2 also showed higher mean richness in the area of denser
vegetable coverage (Area II), indicating a higher number of common and
dominant species in it, and consequently a more uniform distribution in
the abundances of each species.
The abundance of species and individuals of Euphorbiaceae family can be
attributed to their adaptive capacity, palatability, and potential for
use by humans (Ribeiro et al., 2015, Rito et al., 2017). The dominance
of A. pyrifolium , especially in Area I, is attributed to its high
resistance to drought and because it is unpalatable to some herbivores,
mainly goats and sheep. Such properties are conferred by its
epicuticular wax, which in addition to ensuring greater efficiency in
the use of water, has a composition rich in toxic compounds, thus
presenting a competitive advantage over species more sensitive to
semi-arid climates (Medeiros et al., 2017). Moreover, the anthropic
pressure on this species is low since its wood has little utility value.T. palmadora , the second most abundant species in our study, is
morphophysiologically adapted and resistant to water stress, unpalatable
to animals due to its large amount of spines, and has a high
reproductive rate. It can spread asexually through its branches and
fruits even under limiting conditions (Meiado, 2012). C.
pyramidale , the third most abundant specie in the study, is resistant
to water deficits, high salt concentrations, and high temperatures,
being widely found in degraded areas (Matias et al., 2018). Finally,
species of genus Jatropha also have low wood density, making it
of little use for human use. It is considered unpalatable to animals,
and it has a high water reserve capacity, guaranteeing its survival and
reproductive success (Ribeiro et al., 2015; Silva et al., 2004).
The absence of statistical differences in the content of exchangeable
bases and texture between soils of Areas I and II can be attributed to:
a) affinity of the soils with the parent material, and; b) relative
homogeneity of sampled lithologies. The semi-arid climate in Northeast
Brazil favors low chemical weathering of minerals and incipient
pedogenesis (Araújo et al., 2017). These soils consequently express
characteristics associated with their parent material, especially
Cambisols and Neossols (FAO, 2015). Since gneiss is the main lithology
of Cariri Paraibano (Lages et al., 2018), it is expected that the soils
have similar characteristics. On the other hand, the statistical
difference in the C and N levels between Areas I and II indicate
environments with different inputs of plant residues to the soil and/or
different preservation levels.
The environmental conditions provided by the greater abundance, biomass
and diversity of adults observed in Area II favor the establishment of a
more diverse regenerating stratum by: a) guaranteeing a larger seed bank
in the community (Chazdon, 2014); b) attracting dispersing and
pollinating agents (Guevara et al., 1986); c) facilitating seedling
germination and establishment; and d) and providing greater protection
to seedlings. Adult stratum areas with higher biomass protect the
regenerating stratum against predation and trampling by herbivores
(Derroire et al., 2016b; Marinho et al., 2016). Large herbivores prefer
to forage in more open environments due to greater accessibility and to
the palatability of the established herbaceous layer (Skarpe et al.,
2007). Herbivore pressure negatively influenced species diversity, which
was lower in more open areas (Area I). We suggest that the pressure of
herbivores in Area I is favored by the ease of access and greater
abundance of herbaceous plants present in the area, where their pressure
can reduce species diversity.
In addition, microclimate conditions are milder under higher vegetation
levels. The shade provided in environments with a higher number of trees
reduces the transpiration rates of seedlings by decreasing their
exposure to high light and temperature levels, as well as retaining
greater moisture in the soil and providing a higher amount of organic
waste to the soil (Derroire et al., 2016a; Lebrija-Trejos et al., 2011).
The positive correlations between the diversity of regenerative stratum
(RegD0) with C and N levels in the soil indicate the importance of soil
organic matter content in the ecological succession of areas. The supply
of plant residues and their incorporation into the soil ensures nutrient
cycling (Menezes et al., 2012; Sousa et al., 2012). As semi-arid soils
are mostly eutrophic, the availability of nutrients derived from mineral
weathering, such as Ca, Mg, and K, is not limiting for plant growth. On
the other hand, C and N are primary macronutrients derived from the
decomposition of soil organic matter (Six et al., 2004), therefore they
are highly associated with soil organic matter content and quality
(Ostrowska and Porębska, 2015). In addition, higher soil organic matter
levels favor aggregate formation, reducing soil density and increasing
porosity and water infiltration (Ferreira et al., 2018; Silva e
Mendonça, 2007).
The negative correlation between the abundance of seedlings and the
adult stratum height can be attributed to establishing a denser canopy
in forest conditions than open areas. Areas with taller trees guarantee
more favorable environmental conditions for plant growth (Lebrija-Trejos
et al., 2011), providing greater balance in the community than the
proliferation of more resistant species observed in more disturbed
environments such as Area I (Rito et al., 2017). The higher number of
exclusive species sensitive to degradation in Area II reinforces this
hypothesis (Barbosa et al., 2007, Souza et al., 2015a).
The higher mean DGL of the regenerating stratum in the area of lower
plant density (Area I) can be attributed to the decrease in competition
for light (Mclaren and Mcdonald, 2003). However, despite the greater
shading faced by seedlings in Area II, it is known that light is not one
of the most limiting resources in the Caatinga (Sampaio, 2003). Thus,
this factor alone does not fully explain our results. The DGL also
showed a positive correlation with pressure by herbivory, and we
speculate that these effects are indirect, and the greater secondary
growth in Area I is related to the plant’s physiological adaptations to
water stress to which it is subjected.
The growth of some plant species in arid and semi-arid environments is
limited to the season of water availability, passing through growth
pulses during the rainy season and dormancy during the driest months
(García-Cervigón et al., 2017). Therefore, plants respond quickly to
precipitation events because of this limitation, investing in wood and
leaf production while water is available in soil. The irregular
distribution of rainfall observed in the Brazilian semi-arid region with
sporadic precipitation events in the dry months can stimulate several
growth pulses during the year (Aragão et al., 2019). Furthermore, the
distribution of photoassimilates by the plant varies according to the
availability of resources, and root growth and secondary growth become
the priority over primary growth when under limiting conditions (Mattos,
1999). Thus, the largest mean diameter observed in Area I can be
attributed to such factors. However, complementary physiological studies
are necessary to confirm this idea since these responses vary between
different species (Aragão et al., 2019).
As expected, RegD0 was negatively related to pressure by herbivory.
Herbivores generally cause adverse effects on plant communities, causing
habitat degradation, limiting the growth of individuals, and affecting
the taxonomic composition (Sfair et al., 2018; Souza et al., 2015a). The
effects on the regenerative stratum are even more robust, since the
animals have a preference for younger individuals due to their
palatability, and they are even more susceptible to trampling mortality,
compromising the diversity, structure, and maintenance of the plant
community in the future (Marinho et al., 2016).
Our results indicate a more advanced secondary succession stage in Area
II. In addition to the low diversity, Area I has many individuals
identified as A. pyrilifolium , which suggests biotic
homogenization due to anthropic disturbance. Diversity in degraded
environments is reduced due to a decrease in species which are more
sensitive to environmental changes and an increase in the abundance of
the most resistant species (Ribeiro-Neto et al., 2016). The lower C and
N levels in the soils of Area I also seem to be directly related to the
anthropic disturbance. This scenario is the first step towards
establishing the desertification process. These results are a
consequence of the degradation regime imposed on the Caatinga since its
colonization, including agricultural activities (Travassos and Souza,
2014). Nowadays, deforestation and inappropriate land use in
agricultural areas compromise productivity, hampering natural
regeneration in these areas (Leal et al., 2005; Marinho et al., 2016;
Sousa et al., 2012; Sfair et al., 2018).
Considering the colonization and occupation processes of Cariri
Paraibano, the impacts could mainly be related to livestock activities,
especially goat farming, since it is a prevalent practice in the area,
in which animals are raised freely to feed on native vegetation (Leal et
al., 2005). This was evidenced in our study through the high biomass of
fecal pellets found. This fact is pointed out as one of the main reasons
for the vegetation cover loss in drylands and a strong driver of the
desertification process (Marinho et al., 2016).
These results highlight the importance of adjusting the grazing practice
of these areas to guarantee maintenance of plant communities and
biological diversity. One of the most efficient land management
practices is fallow, which isolates the land and allows it to recover
through its resilience, promoting recovery of soil fertility, water
storage capacity, and plant communities (Ferreira, et al., 2018). In the
case of the Brazilian semi-arid region, this practice is not yet
realistic for social and economic reasons. However, the development of
public policies to raise awareness and incentives for more sustainable
development is indicated. For example, better livestock management along
with the creation of trapped herders avoids continuous removal of native
vegetation andallows its restoration through natural regeneration (Leal
et al., 2005). Another measure of fundamental importance would be
creating Conservation Units of Integral Protection, which are still
scarce in the Caatinga (Antongiovanni et al., 2020; MMA, 2011).
Conclusions
Our results confirm the effects of vegetation cover on the natural
regeneration of plant communities in the Brazilian semi-arid region. The
higher biomass and diversity of the adult stratum added to a higher C
and N content in Area II soil led to the establishment of a higher
number of species, with even greater equity.
The results indicate overgrazing as one of the main threats and drivers
of the desertification process in the region, highlighting the
importance of implementing management techniques in the use of these
lands. Creating Conservation Units of Integral Protection and
encouraging more sustainable development through environmental education
are essential measures to be implemented.