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.