Discussion
Agricultural expansion in the humid tropics, most of which at the
expense of primary forest cover, has led to unprecedented habitat
fragmentation. Even in remaining forest fragments, the indirect effects
of overhunting (Peres 2001), wildfires (Cochrane and Laurance 2002), and
other anthropogenic disturbances often exacerbate the detrimental
impacts of forest loss and fragmentation (Laurance and Peres 2006).
Although these negative impacts on local diversity have been extensively
studied (Decaëns et al. , 2018; Franco et al. , 2019; Chaseet al. , 2020), and their general effects are corroborated here,
previous results obtained from local forest patches are insufficient to
understand patterns of biodiversity loss at entire landscapes and inform
optimal land-use strategies.
Considering the scale of local forest patches, our models predict that
the occupancy of virtually all ant species decreases when forest patches
are reduced and cattle gain access to forest fragments. Qualitatively,
these results are in line with previous studies suggesting a strong
reduction in local species diversity with the reduction in patch size
(Chase et al. , 2020), habitat amount surrounding patches (Fahrig,
2003; Fahrig et al. , 2019), and with agricultural intensification
(Laurance et al. , 2012; Decaëns et al. , 2018). However,
there are three important findings in our study that challenge the
perception of these effects on biodiversity. First, our results suggest
that the effects of habitat loss and cattle intrusion on patch-scale
diversity have been largely underestimated. This occurs because most
species are rare and difficult to detect, especially in larger patches
(Fig. 3A), so their declines are overlooked in terms of both individual
species or entire communities. In absolute numbers, diversity tends to
be underestimated in vast pristine areas of primary habitat because they
contain a large proportion of undetected species. Using the same
sampling protocol in all patches does not guarantee that species
occupancy can be directly compared. Detection errors are common in many
taxa, including vertebrates (Ruiz-Gutiérrez et al. 2010) and plants
(Chen et al. 2013), and studies investigating differences in individual
species occurrences or diversity should use methods that take
detectability and differences in sampling sufficiency into account (Chaoet al. , 2009; Chase et al. , 2020).
Second, we demonstrate that forest remnants accessed by cattle, which in
southern Amazonia typically lack barbed-wire fences that are expensive
to implement and maintain, can experience sharp declines in species
diversity (Fig. 2C). The impact of habitat change on diversity will
therefore depend not only on the amount of habitat lost but also on the
protection level of the remaining fragments (Franco et al. ,
2019). Although cattle presence was correlated with area (smaller
fragments were more frequently accessed by cattle) we found an
independent effect of cattle intrusion and this effect was stronger than
that predicted by area reduction alone. Moreover, due to the high
correlation between fragment size, cattle access, and the relative
amount of forest edges, it is plausible that diversity declines
typically attributed to a loss in patch area is at least, if not
primarily, driven by the proportional increase in cattle access or other
factors associated with forest edges (Lasmar et al. , 2021).
Finally, our results demonstrate that, in addition to the local
diversity within individual patches, differences in species identity
among patches (i.e. beta-diversity) needs to be explicitly considered to
understand the effect of habitat change on landscape diversity. Despite
the drastic erosion in local species diversity following habitat loss
and cattle disturbance as discussed above, protecting multiple patches
with distinct community composition can counteract these losses and
still ensure that most species are able to persist regionally.
Many previous studies on land cover change, which are largely influenced
by the metapopulation (Hanski & Ovaskainen, 2000) and island
biogeography paradigms (MacArthur & Wilson, 1967), have investigated
species responses to habitat loss (“island area”) and isolation
(habitat subdivision) using local habitat patches as units of analysis
(Fletcher et al. , 2018; Chase et al. , 2020). These studies
usually suggest that conservation must be focused on large and highly
connected forest areas because, in a pairwise comparison where the same
amount of habitat is selected in both large and small patches, large
patches protect a disproportionately larger number of species (Diamond,
1975; Chase et al. , 2020). We agree that this should remain an
important conservation strategy if either only a single forest fragment
is available to be preserved or the entire landscape is compositionally
homogeneous. However, these studies often ignore the high heterogeneity
in species identity observed in fragmented landscapes (beta-diversity:
Lasky & Keitt, 2013; Fahrig, 2020, Jakovac et al. , 2022;
Carvalho et al. , 2022; Przybyszewski et al. , 2022;
Ramírez-Ponce et al. , 2019), which we found to be the main
contributor to regional diversity (Fig. 5D; see also results from Solar
et al. 2015). We found that the increase in landscape diversity compared
to what is found in local patches does not result only from the fact
that larger landscapes host more habitat area, but because small
fragments add species heterogeneity. Our results indicate that this
heterogeneity can be maximized when the landscape is comprised of many
forest patches spread across the wider landscape, which explains why
fragmented landscapes — which are typically dominated by many small
fragments (Taubert et al. 2018) — often contain more species than a
single tract of continuous forest containing the same amount of habitat
(Fahrig, 2003, 2020). Several previous studies have found high species
turnover in fragmented landscapes (Jakovac et al. , 2022; Solaret al. , 2015; Carvalho et al. , 2022; Przybyszewskiet al. , 2022; Ramírez-Ponce et al. , 2019).Here, we further
provide evidence to support that this turnover is sufficiently high to
counterbalance the majority of local species losses resulting from
habitat loss and the presence of cattle.
Although beta-diversity is the leading component of regional diversity
in fragmented landscapes and maximizes regional diversity, it is
important to note that (1) landscape-scale habitats loss is still a
major cause of species declines, and (2) we do not infer a causal
relationship between habitat fragmentation and beta-diversity. When
habitat amount increases across the landscape, additional species are
preserved (Fig. 5A). If this increase is achieved by adding several
small patches, large numbers of species can be retained because each new
habitat adds distinct sets of species to the regional species pool
(increase in beta-diversity; Fig. 5C). Therefore, habitat amount
increases both alpha and beta-diversities. In spite of the species
surplus added by beta-diversity when several small fragments are
maintained (higher than expected by the Species-Area relationship; R
> 1), the break-up of habitat is unlikely to be the main
cause of this beta-diversity. When the landscape is comprised of several
forest patches, these patches tend to be far apart thereby experiencing
divergent environmental conditions, which naturally increases
beta-diversity (Tuomisto et al. , 2003). The natural balance
between colonization and extinction, which is influenced by local
habitat conditions, is the underlying factor behind the observed species
turnover in fragmented landscapes (Lu et al. , 2019). In this
study, we lack temporal data required to directly estimate how
colonization and extinction events are specifically altered within local
fragments (MacKenzie et al. , 2003). Nonetheless, it is likely
that local extinction rates increased with habitat loss, consequently
leading to a reduction in species occupancy (Fahrig et al. ,
2022). Although fragmentation itself is likely to influence these
processes and beta-diversity (Fahrig et al. , 2022), it is highly
probable that areas containing multiple small fragments were already
characterized by some degree of beta-diversity prior to habitat loss and
fragmentation, so beta-diversity can be pervasive even if
colonization-extinction rates do not change.
Contrary to expectations, we did not observe the negative association
between beta-diversity and geographic or environmental distances.
However, we believe that this could be attributed to several factors,
including the specific history of habitat change, the distribution of
habitat types, and other unmeasured variables within our sampling
region. Our study region is a complex edaphic mosaic situated near the
transition zone between the Cerrado and Amazonia biomes, and it is
possible that even distant patches shared similar natural vegetation
types (see similar results in Cáceres et al. 2014). Additionally,
some patches in the core area of the region (Fig. 1) may have shared a
similarly older history of land use that we were unable to assess in
this study. These factors may have influenced observed patterns of
beta-diversity and the lack of a clear association with geographic and
environmental distances.Unmeasured environmental variables may differ
between the sampled fragments, so that any increase in the overall
number of fragments (regardless of size and fragmentation status) also
increases the chance of accommodating distinct species. At broader
geographic scales (e.g. the Amazon basin), beta-diversity almost always
increases with either geographic or environmental distance (Tuomistoet al. , 2003), and setting-aside environmentally heterogeneous
landscapes is likely to be an important conservation strategy (Lasky &
Keitt, 2013; Socolar et al. , 2016; Fahrig, 2020). If landscape
scale beta-diversity results mostly from the natural distribution of
species along environmental gradients, then heterogeneous landscapes
must be prioritized for conservation. For instance, Tuomisto et
al. (2003) showed that soil nutrient levels in the Amazon play a
crucial role in driving natural changes in floristic composition. This
has also been observed in various plant and animal taxa at broad
geographic scales (Dambros et al., 2020). Collectively, these studies
suggest that variation in soil nutrients have a significant influence on
the composition of plant and animal communities in Amazonia and
potentially other regions.
Identifying the drivers of beta-diversity is important to understand how
landscape diversity changes under several scenarios. Habitat
subdivision, croplands, roads, railroads, and urban areas may create
additional environmental heterogeneity that disrupts species movements.
Therefore, these landscape elements have the potential to alter regional
diversity through their simultaneous effects both on alpha- and
beta-diversity. It is well known that habitat area and connectivity
increases local diversity (Lasky & Keitt, 2013), but factors that
homogenize the environment (McKinney, 2006; Gámez-Virués et al. ,
2015) or amplify the movement of species (Lasky & Keitt, 2013; Chaseet al. ) could potentially counteract these increases by reducing
beta-diversity. This study lacked the necessary data to unravel the
complex ecological processes that contribute to the high observed
heterogeneity in species composition. Consequently, we were unable to
fully explain why such landscapes can harbor more species compared to a
single large fragment of the same size (SS > SL; Fahriget al. , 2022). Understanding the dynamic processes of
differential colonization and extinction in continuous versus fragmented
landscapes, as well as the roles of habitat history, species
adaptations, and dispersal, would likely require surveying multiple
landscapes, including data on species movement and extinction risks
(Fahrig et al. , 2022). Nonetheless, our study demonstrates that
in a fragmented landscape, the high heterogeneity in species composition
plays a critical role in maintaining regional diversity, even in the
face of species loss within local remnants. This highlights the
importance of considering landscape-scale processes and heterogeneity in
understanding biodiversity persistence in fragmented landscapes. The
advantages of a conservation strategy at landscape to regional scales
need to be evaluated taking into account the effects of multiple factors
on both alpha- and beta-diversity and the relative importance of these
components to regional diversity.
In several of the world’s terrestrial biomes, especially tropical
forests, anthropogenic grazelands reduce natural ecosystems in any
landscape while allowing cattle to move into, overgraze and trample
habitat remnants, all of which can reduce local species diversity.
Nevertheless, in many areas where a mosaic of forest, croplands, and
rangelands persist, multiple natural fragments are typically spared
across the landscape (Hendershot et al. , 2020). Our results
suggest that a considerable amount of the total biodiversity is likely
to have been preserved in those fragments because they greatly differ in
species composition (Fig. 5C). In this study, ~88% of
all species found across the entire landscape could be found in only 14
fragments ranging from 2.4 to 87 ha, most of which were penetrated by
cattle. Although some species may be extirpated due to deforestation and
patchy species distributions may impair the proper functioning of the
ecosystem or services provided by biodiversity, the remaining small
forest remnants could still act as an insurance policy that ensured some
of the native biodiversity and ecosystem functions can be restored at
sites where they had been lost. Some studies suggest that natural
habitats should be embedded within agropastoral landscapes to maximize
biodiversity conservation (Kremen & Merenlender, 2018; Hendershotet al. , 2020). Our results demonstrate that this may be possible
for most of the arthropod fauna if a minimum amount of habitat and
heterogeneity in species distributions are preserved.