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.