Abstract
Agricultural expansion has markedly reduced forests and reconfigured
landscapes. These changes incur a well-known detrimental impact on the
biodiversity of local forest patches, but the effects on species
persistence at entire landscapes comprised of multiple patches are
debated. We investigated how regional diversity is affected by habitat
loss, fragmentation, and cattle grazing, and how species respond to
deforestation both locally and regionally. We also investigated how the
heterogeneity in species distribution (beta-diversity) buffers
landscapes against local diversity losses. The vast majority of the 251
ant species found in our study were negatively affected by both habitat
loss and cattle at local forest patches, drastically reducing diversity
at these patches compared to pristine forests. Despite local declines in
diversity, however, heavily fragmented landscapes could still retain
most species due to the high heterogeneity in species distribution. We
found that beta-diversity is the main component of regional diversity.
Results from several studies suggest that this component is maximized
when remnant primary habitats in a landscape are spread across vast
areas. Although preserving local diversity may be important for the
adequate functioning of the ecosystem locally, our results indicate that
the maintenance of many small forest patches in a landscape can buffer
regional biodiversity against local species losses. Our results suggest
that even small forest remnants in otherwise deforested landscapes can
prevent most regional-scale species extirpations, and therefore also
merit conservation efforts.
Keywords: Habitat Loss; Species Diversity; Occupancy Models; Gamma
Diversity; Species Composition; Landscape Ecology; SLOSS.
Introduction
Forests have been severely reduced worldwide as a result of agricultural
intensification (Curtis et al. 2008). This process leads to the rapid
decline in species diversity locally (Chase et al. , 2020), but
the effects of landscape change on regional biodiversity are still
unclear. Within a region, declines in diversity are consistently
associated with the reduction in overall habitat amount (Fahrig, 2003).
However, declines in forest cover are usually coupled with habitat
fragmentation (i.e. the subdivision of habitat into isolated patches),
and the impact of this break-up (fragmentation per se ) on species
diversity remains highly debated (Fletcher et al. , 2018; Fahriget al. , 2019). While local forest patches lose species as a
result of forest break-up (Fletcher Jr. et al. , 2018; Chaseet al. , 2020), landscapes comprised of groups of isolated patches
often have higher diversity than a continuous forest with the
same amount of habitat (Fahrig, 2003; Fahrig et al. , 2019).
Identifying the drivers of these contradictory results can ensure that
optimal conservation strategies are designed to maximize local and
regional diversity.
Differences between local and regional effects of habitat change are
mediated by the poorly-explored effects of fragmentation on
beta-diversity (Solar et al. 2015; Socolar et al. , 2016; Chetcutiet al. , 2021). Beta-diversity represents the change in species
composition identity among forest patches and, combined with the number
of species found in local patches, determines the overall number of
species found in a landscape or region. When local diversity is low,
diversity in the landscape might still be high if there is sufficient
heterogeneity in species distributions (Solar et al. 2015; Lasky &
Keitt, 2013; Fahrig, 2020; Chetcuti et al. , 2021). For example,
if a patch contains a single species, a landscape comprised of 10 forest
patches may still retain 10 species if each patch contains a distinct
species. It is well known that heterogeneity in species distributions
increases regional diversity (Loreau et al. , 2003; Lasky &
Keitt, 2013). Numerous studies have demonstrated that modified
landscapes can maintain a significant level of diversity in species
composition (Jakovac et al. 2022; Solar et al. 2015; Carvalho et al.
2022; Przybyszewski et al. 2022; Ramírez-Ponce et al. 2019). However,
this outcome is highly variable and contingent upon factors such as
species dispersal capacity and habitat configuration (Arnillas et al.
2017). Most of these studies have not quantified whether this
landscape-scale heterogeneity can effectively compensate for local
biodiversity losses (but see Solar et al. 2015). Research is needed to
elucidate how the configuration of forest fragments in a landscape (e.g.
several small or few large) is associated with species heterogeneity
and, consequently, how it affects regional diversity (Socolar et
al. , 2016).
Regions represented by habitat patches that are far apart, as in
fragmented landscapes, usually covers a gradient of environmental
conditions (Tuomisto et al. , 2003). This environmental variation
may allow species with distinct adaptations to survive in distinct areas
(Lasky & Keitt, 2013). However, to maintain viable populations, many
species require large areas containing sufficient resources (Pe’eret al. , 2014) and, in many cases, that are highly connected
(Baguette & Schtickzelle, 2006), both of which are reduced when small
patches are scattered across a landscape. Therefore, as fragmented
landscapes promote heterogeneity in species distributions, which
increases regional diversity, individual fragments lose species, which
potentially reduces regional diversity. Depending on the balance between
heterogeneity (beta-diversity) and local diversity (alpha-diversity),
several forest fragments can sustain more or fewer species than a single
large forest containing the same amount of habitat (Lasky & Keitt,
2013; Arnillas et al. 2017). This balance is likely to depend on the
spatial scale under consideration (broader scales = more heterogeneity)
and the size and quality of the remaining fragments (more intact =
higher local diversity). Although empirical studies have investigated
the effects of habitat loss, fragmentation, and habitat quality on local
(alpha) and beta-diversity independently, their relative contributions
to regional diversity are yet to be estimated.
We investigated how both local and beta diversity contribute to regional
diversity in a highly fragmented Amazonian landscape comprised of a wide
gradient of forest remnants ranging in size from 2.4 to 14,481 ha, some
of which could be accessed by bovine cattle in adjacent pastures. By
partitioning landscape diversity into its alpha and beta components, and
comparing groups of small vs. large fragments, we show 1) how
landscape-scale diversity is distributed into its alpha/beta components,
2) how the relative contribution of these components change along a
gradient from a single small fragment to a vast tract of continuous
forest, and 3) how habitat quality (cattle presence) affects local and
regional diversity. To estimate these effects considering missing
species and sampling effects, we used occupancy models that control for
biases in species detection for both measures of species local diversity
and beta-diversity. All analyses were performed using data on
leaf-litter ants, a hymenopteran group that is particularly vulnerable
to changes in microclimatic conditions caused by cattle trampling and
edge effects. Our analyses integrated both community-level and
individual species responses. We also explored the connection between
species responses and two important traits: species body mass and
foraging strategy. These traits have often been associated with
invertebrate responses to changes in habitat (Hoffman and Andersen 2003;
Andersen 2018; Carvalho et al. 2022).Material and Methods
The study was carried out in the Alta Floresta region, state of Mato
Grosso, Brazil (09°53’S, 56°02’W, Fig. 1). This region is part of the
“deforestation arc” of southern Amazonia, a heavily fragmented region
that originally consisted of pristine, unbroken tracts of Amazonian
forest (Fearnside, 2005). Deforestation in the region occurred in the
early 1980s with the conversion of forests into farms and ranches
(Michalski et al. 2008). The landscape is comprised of a few continuous
forest areas, a few large forest remnants, and many small variable-sized
remnants typically surrounded by cattle pastures (Fig. 1). The climate
in the region is tropical humid (Aw classification in the Köppen system;
Alvares et al. , 2013) with a mean annual rainfall of 2,350 mm,
mean annual temperature of 26.5°C, and marked dry (May-September) and
wet seasons (October-June; RADAMBRASIL 1983).
Ants were systematically sampled from March to July 2008 within 24
forest patches. Two patches were represented by pristine forests that
had not been disturbed by fires and timber extraction. The 22 remaining
patches were selected to cover a gradient of patch sizes (range from 2.4
to14,480.5 ha) and presence of cattle (n=7) while spaced apart by a
minimum of 5 km. Fragments diverging in patch size were randomly
selected in the landscape to avoid spatial autocorrelation in this
predictor variable.
In each patch, ants were collected using 10 Winkler sacks placed at the
center of each fragment (total of 240 Winkler extractions). Winkler
extractors were placed 10-m apart from each other, and for each Winkler
extraction we removed 1m2 of leaf litter from the
soil. The litter was sieved and placed in bags and the soil fauna
removed from the extractor after 72 h (Bestelmeyer et al. , 2000).
In addition, we collected ants manually for 10 min (100 min per patch)
at each extraction site, immediately after removing the leaf litter from
the soil. To avoid introducing sampling biases during manual
collections, sampling was performed by the same collectors. Ants were
then separated from the overall extracted material at the Laboratório de
Biologia, UNEMAT, Alta Floresta, and identified in the Laboratório de
Ecologia de Interações Inseto-Planta, UFMT, Cuiabá, using specialized
bibliography (Fernandez, 2003; Baccaro et al. 2015). All voucher
specimens were deposited at the Zoology Museum of the University of São
Paulo (MUZUSP).
Although we followed a standardized sampling protocol across all
fragments, it is important to note that some small fragments may have
been better represented in our data due to potential differences in
species detectability among patches. To address this potential sampling
bias, we conducted tests and applied statistical corrections using
occupancy models. These models account for species detection as a
function of, for example, fragment size (see Data Analysis section
below).
In each patch, we also quantified predictor variables including forest
patch area, cattle presence, distance to the nearest fragment, and the
habitat amount throughout the surrounding landscape. Patch area was
obtained from Landsat images (1984-2008) using the Fragstats 3.0
software (McGarigal et al. , 2002). For the two continuous
forests, we assigned an area value that was one order of magnitude
larger than the size of the largest forest patch, measured on a
log10 scale. This approach is commonly employed in
studies investigating species-area relationships (e.g. Palmeirim et al.
2021; 2022). Management history and cattle intrusion were obtained from
direct observations of cattle presence within the patches, indirect
evidence (dung and tracks), and information provided by local
landowners. Bovine cattle were more frequently found in smaller
fragments (correlation coefficient: r = -0.54). Consequently, it is
likely that cattle had access to a significant portion of the fragments
wherever they were present. Distance to the nearest fragment was
calculated based on the distance between the centroids of any two
fragments and the minimum distance between fragments. Habitat amount at
the time of sampling was measured from pre-classified forest cover maps
obtained from MapBiomas (Mapbiomas, 2021) as the percentage of forest
cover within a buffer area from the centroid of each patch. We used
several radial buffer distances (100m, 200m, 500m, 1000m, and 1500m) to
calculate the habitat amount across the landscape (Fahrig et al. 2020).
Habitat amount measured at the 500-m buffer maximized the correlation
between observed species richness and habitat amount and was therefore
used in subsequent analyses. Our analysis did not reveal any significant
association between distance to the nearest fragment and species
richness, regardless of whether we used raw, semi-log, or
log-transformed variables in simple or multiple regression models
(partial). As a result, we did not include this predictor in our
occupancy models. It is worth noting that centroid distance and minimum
distance between fragments showed a high correlation (r = 0.97) and
yielded similar results, with slightly stronger but non-significant
effects observed when using centroid distance.
We associated species response to habitat change with species traits
(see below). We obtained species body mass and foraging mode at the
genus level from the Global Ants Database (Parr et al. , 2017).
Whenever possible, preference was given to traits available from the
same species found within our study area or a congener from elsewhere in
the Amazon.