Volume 54, Issue 3 pp. 273-287

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What, where, and how: a spatiotemporally explicit analysis of the drivers of habitat loss within the range of maned three-toed sloths (Bradypus torquatus and Bradypus crinitus)

Paloma M. Santos,

Corresponding Author

Paloma M. Santos

[email protected]

orcid.org/0000-0002-6932-1406

Instituto Nacional da Mata Atlântica (INMA), Santa Teresa, Espirito Santo, 29650-000 Brazil

Instituto de Pesquisa e Conservação de Tamanduás no Brasil, Ilhéus, Bahia, 45655-718 Brazil

Correspondence

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Juliano A. Bogoni,

Juliano A. Bogoni

[email protected]

orcid.org/0000-0002-8541-0556

Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, Mato Grosso do Sul, 79070-900 Brazil

Laboratório de Ecologia, Manejo e Conservação de Fauna Silvestre (LEMaC), Departamento de Ciências Florestais, Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ), Universidade de São Paulo (USP), Piracicaba, São Paulo, 13418-900 Brazil

Laboratório de Mastozoologia, Centro de Pesquisade Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso (UNEMAT), Cáceres, 78200-000 Mato Grosso, Brazil

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Adriano G. Chiarello,

Adriano G. Chiarello

[email protected]

orcid.org/0000-0003-1914-5480

Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo (USP), Ribeirão Preto, São Paulo, 14040-901 Brazil

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Paloma M. Santos,

Corresponding Author

Paloma M. Santos

[email protected]

orcid.org/0000-0002-6932-1406

Instituto Nacional da Mata Atlântica (INMA), Santa Teresa, Espirito Santo, 29650-000 Brazil

Instituto de Pesquisa e Conservação de Tamanduás no Brasil, Ilhéus, Bahia, 45655-718 Brazil

Correspondence

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Juliano A. Bogoni,

Juliano A. Bogoni

[email protected]

orcid.org/0000-0002-8541-0556

Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, Mato Grosso do Sul, 79070-900 Brazil

Laboratório de Mastozoologia, Centro de Pesquisade Limnologia, Biodiversidade e Etnobiologia do Pantanal, Universidade do Estado de Mato Grosso (UNEMAT), Cáceres, 78200-000 Mato Grosso, Brazil

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Adriano G. Chiarello,

Adriano G. Chiarello

[email protected]

orcid.org/0000-0003-1914-5480

Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo (USP), Ribeirão Preto, São Paulo, 14040-901 Brazil

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First published: 21 January 2024

https://doi.org/10.1111/mam.12342

Editor: DR

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Abstract

The first step towards understanding the conservation situation and informing conservation decision-making is to identify the habitat loss drivers. However, for nearly all tropical biota, there is a glaring lack of information on the spatiotemporal patterns of anthropogenic drivers.
Our objective was to analyse the spatial and temporal distribution of the main anthropogenic drivers of habitat loss for Bradypus torquatus and Bradypus crinitus, two endangered and endemic species to the Brazilian Atlantic Forest.
We used land-use information associated with seven major IUCN-based threats to sloths, covering a three-generation time window (1988–2020), to quantify the current area occupied, temporal changes, heterogeneity, and intensity of drivers across species distributions.
We found that cattle farming and ranching dominate the range of both species (from 49% to 56%) and cover an area larger than the remaining native forest. Other drivers also represent important spatial and temporal features of land conversion across species distributions.
Driven mainly by livestock expansion, both sloth species have experienced a significant loss of forest cover (Bradypus torquatus – 659098.70 ha; Bradypus crinitus – 139013.20 ha) in the Brazilian Atlantic forest. Overall, Bradypus torquatus showed a higher rate of deforestation than forest regeneration, whereas forest gains outweighed habitat loss for Bradypus crinitus.
Our results show that a substantial area of native forest – essential for strictly arboreal species – is being continuously replaced by cattle ranching and agricultural activities, which may lead to population isolation and decline, threatening the long-term population viability.

Resumo

Identificar os vetores de ameaça às espécies é uma importante etapa para compreender o status de conservação e estabelecer ações de conservação. No entanto, para a grande maioria da biota tropical, há uma evidente falta de informação sobre os padrões espaço-temporais dos vetores antrópicos.
Nosso objetivo foi analisar a distribuição espacial e temporal dos principais vetores de ameaças antrópicas a Bradypus torquatus e Bradypus crinitus, duas espécies de preguiças endêmicas da Mata Atlântica brasileira e ameaçadas de extinção.
Usamos informações de uso e cobertura da terra associadas a sete grandes ameaças às preguiças baseadas na lista da IUCN, abrangendo uma janela de tempo de três gerações (1988 a 2020), para quantificar a área atual ocupada, mudanças temporais, heterogeneidade e intensidade dos vetores ao longo da distribuição das espécies.
A pecuária domina as áreas de ocorrência das duas espécies (de 49% para 56%), cobrindo uma área maior que a mata nativa remanescente. Outros vetores também representam características importantes no espaço e no tempo em termos de conversão de terras sobre distribuição de espécies.
Impulsionadas principalmente pela expansão da pecuária, ambas as espécies de preguiças sofreram uma perda significativa de cobertura florestal (Bradypus torquatus – 659.098,70 ha; Bradypus crinitus – 139.013,20 ha). No geral, Bradypus torquatus exibiu uma maior taxa de desmatamento em comparação com a regeneração florestal, enquanto Bradypus crinitus, o ganho de floresta superou a perda.
Nossos resultados destacam que uma área substancial de floresta nativa – essencialmente importante para espécies estritamente arbóreas – é persistentemente substituída por atividades de pecuária e agricultura, o que pode levar ao isolamento e declínio populacional, comprometendo a viabilidade populacional de preguiças a longo prazo.

INTRODUCTION

Human pressure exerts critical negative effects on biodiversity, compromising long-term biota conservation worldwide (Di Minin et al. 2019). The expansion of agricultural frontiers and the increase in urban areas play a fundamental role in the reduction of natural areas, leading to the loss of more than 100 million hectares of natural habitat throughout the globe from 1980 to 2000 (IPBES 2019). This habitat loss is particularly exacerbated across the world tropics, given that both humid and dry tropics amounted to c. 475000 km² of forest cover loss (c. 50%) in only half a decade (2000–2005; Hansen et al. 2010). Consequently, habitat loss and degradation are the main causes of species decline (Bellard et al. 2022, Bogoni et al. 2022): approximately 28386 species are threatened with extinction due to habitat loss, representing 19% of all assessed species (IUCN 2023). Habitat reduction directly affects the availability of resources and ideal conditions (e.g. environmental, and climatic) necessary for the survival of different species (Rosenzweig 1991). As populations become increasingly isolated, the maintenance of important ecological processes such as dispersal, migration, and pollination are compromised and costly to restore in terms of financial and human resources (Tambosi et al. 2014).

To assess the state of global biodiversity among various threats, the International Union for Conservation of Nature (IUCN) classifies species into several categories of endangerment (IUCN 2012). The rigorous and well-established methodology adopted in the assessment cycles is widely used in extinction risk assessments in several countries (ICMBio 2013). Understanding the effects of the multifaceted drivers of habitat loss (e.g. residential or agriculture expansion) on the persistence or decline of species populations is paramount for this classification scheme. Yet, there is a glaring lack of information about the chronic persistence, location, and other important aspects of these drivers (Harfoot et al. 2021), compromising the understanding of different spatiotemporal processes that act upon the global biota, especially across vulnerable biomes such as the Atlantic Forest of South America.

The Atlantic Forest is one of the most altered natural areas in Brazil. After centuries of intensive exploitation, less than 30% of the original forest cover remains (Rezende et al. 2018, Vancine et al. 2023), consisting of forest fragments of various shapes and sizes arranged in a heterogeneous human-dominated environment (Ribeiro et al. 2009, Vancine et al. 2023). The Atlantic Forest Law (Federal Law 11.428/06; Brasil 2006) guarantees the protection of the Atlantic forest remnants. However, since 2018, this biome has been subjected to intensified deforestation, with an alarming increase of 66% in the loss of natural areas in the recent period of 2020–2021 compared with the 2010s (Fundação SOS Mata Atlântica 2022). This recent increase in deforestation has been observed in 14 of the 17 Brazilian states overlapping this biodiversity hotspot (Fundação SOS Mata Atlântica 2022), mostly due to the expansion of agricultural frontiers into natural areas (MapBiomas Project 2023), fuelled by the Bolsonaro (former president of Brazil) administration paradigm (Escobar 2021, Bastos Lima & Da Costa 2022).

Because of the diversity of phytophysiognomies and social structures embodied in the Atlantic Forest biome (Olson et al. 2001), drivers of habitat loss are unevenly distributed. In general, however, there is a considerable gap in the spatial knowledge of these drivers, which is quite diffuse, imprecise, and generalised (Harfoot et al. 2021, Bellard et al. 2022). Anthropogenic drivers may affect more than 20000 species within the biome, of which c. 40% are endemic (CEPF 2001), including the endangered maned three-toed sloths (Bradypus spp.). Once considered a single species – Bradypus torquatus – a recent integrative taxonomic review (Miranda et al. 2023) revealed that maned sloths constitute two distinct species, the northern maned sloth (Bradypus torquatus Illiger, 1811) and southern maned sloth (Bradypus crinitus Gray, 1850). Bradypus torquatus occurs in Bahia and Sergipe, whereas Bradypus crinitus is restricted to Espírito Santo and Rio de Janeiro coastal states (Miranda et al. 2023). When still considered a unique taxon, the maned sloth was listed as vulnerable (Chiarello et al. 2022, MMA 2022). However, with the recognition of two distinct species, their respective ranges have been reduced and both species might have to be listed in a more threatened category.

Undoubtedly, habitat loss is the main threat to these species, due to their strictly arboreal and folivorous habit (Chiarello 1998a, b, Giné et al. 2015, Mureb et al. 2023). Although maned sloths can use modified areas, such as cabrucas (cocoa agroforests) (Cassano et al. 2011, Falconi et al. 2015), human-induced land use (e.g. land conversion to pasture) negatively affects the species (Falconi et al. 2015, Santos et al. 2019). Four leading IUCN threats closely linked to habitat loss are currently recognised for maned sloths (Chiarello et al. 2022): residential and commercial expansion (Housing and urban areas), agriculture & aquaculture (Annual and perennial non-timber crops; Wood and pulp plantations; Livestock farming and ranching), biological resource use (Hunting and trapping terrestrial animals; Logging and wood harvesting), and transportation and service corridors (Roads & railroads). However, because of the structural and social complexity of the Atlantic Forest, other latent threats to species may exist to the species (e.g. aquaculture, wildfires, mining, etc.; Marques et al. 2021).

Land use drivers responsible for habitat loss can vary widely in terms of configuration and composition, resulting in different impacts on natural habitats and species. A more heterogeneous non-habitat matrix may cause less challenges to biodiversity, given that species tend to respond differently to multiple drivers of habitat changes (Benton et al. 2003, Azhar et al. 2015, Brüning et al. 2018). In addition, the persistence of a particular driver across an area also matters. Evidence so far indicates that regional extinctions may experiment a delay to take place after landscape modifications, a process known as extinction debt (Lira et al. 2019). Both the range and persistence of the drivers can have negative implications for biodiversity, challenging conservation planning. Taken together, therefore, landscapes with greater heterogeneity and lower intensity of land-use drivers responsible for habitat loss may have less detrimental effects on those with less heterogeneity and higher intensity.

Effective allocation of resources towards the conservation of endangered species is facilitated by understanding the spatial extent and temporal dynamics of these drivers. This understanding depends on identifying, locating, and spatiotemporally analysing the main drivers impacting habitats and their species (Harfoot et al. 2021). A crucial element of this effort includes understanding the status of land use, pinpointing causes of deforestation, identifying locations for forest regeneration, and tracking shifts in human-induced land use. Thus, our aim was to identify, locate, and determine the temporal dynamics of the main drivers of habitat loss to maned three-toed sloths across the Atlantic Forest. More specifically, this study addresses three key conservation dilemmas: What – What are the primary drivers of habitat loss for the two maned sloth species? What is the intensity of these drivers? Where – Where are these key drivers located? Where is habitat loss occurring? Where has each driver increased or decreased? and, How – How have threats changed over time?

METHODS

Geographical space and study species

We conducted our study within the range limits of two maned sloth species (Bradypus torquatus and Bradypus crinitus) distribution. Endemic to the Brazilian Atlantic Forest, the maned sloths inhabit almost exclusively ombrophilous forests along the coast (Fig. 1). To delimit the species range limits, we used the most recent and updated range map provided by the IUCN for Bradypus torquatus (Chiarello et al. 2022). Since the IUCN still treats Bradypus torquatus as a single species, we have divided the map by designating the region including Sergipe and Bahia as the range of Bradypus torquatus and the area including Espírito Santo and Rio de Janeiro as the range of Bradypus crinitus. This division resulted in a distribution area of 56415.95 km² for Bradypus torquatus and 28525.09 km² for the recently described Bradypus crinitus.

Details are in the caption following the image — **Fig. 1**
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Geographic space and distribution ranges of two species of maned sloths (*Bradypus torquatus*, Illiger 1811 and *Bradypus crinitus*, Gray 1850) across the Brazilian Atlantic Forest. Geographic coordinate system; Datum: WGS 84.

Driver identification and selection

We first identified the land-use classes associated with each potential driver of habitat loss (hereafter drivers; Appendix S1) beyond those already listed by the IUCN for the species (Chiarello et al. 2022), based on land-use cover and natural system modifications (e.g. wildfires) data provided by the MapBiomas project collection 6.0 (2022). The IUCN-listed threat of biological resource use was excluded because we focused on the drivers of habitat loss due to land use changes. Using Google Earth Engine (https://earthengine.google.com/), we separately extracted binary maps that provided the presence/absence of each potential driver derived from land use. For example, areas identified as soybean or rice crops were reorganised into one IUCN threat category – Annual & perennial non-timber crops (Appendix S1). We also extracted any natural area data (e.g. Forest formation and Other Natural Areas, consisting of mangroves, savannas, sandbanks, wetlands, and rocky outcrops). All classes (i.e. drivers and natural areas – Forest formation and other natural areas) were selected from a time series spanning 32 years from 1988 to 2020. This time window corresponds to three generations (~10.76 years) for both species, a parameter used in the IUCN extinction risk assessment (IUCN 2022). We took a more conservative approach by adopting the generation length determined by Pacifici et al. (2013). In that study, the mean generation length value was assigned to species that fall within the same bin of log body mass and belong to the same order (Pacifici et al. 2013).

Spatial patterns of the drivers

With the main drivers identified and extracted throughout the entire species ranges, we first calculated the current area occupied (in %) by each class overlapping the species ranges, including the area taken up by natural formation (Forest formation and other natural areas). Then, using the historical series, we estimated the relative change in class area (natural formation + drivers) using the following equation (Equation 1):

Relative change {(%)}_{i - grid} = \frac{{LY}_{i - grid} - {FY}_{i - grid}}{{FY}_{i - grid}}

((Equation 1))

where LY is the total class area in the last year (i.e. 2020) of the time series, FY is the total class area in the first year (i.e. 1988) of the time series, whereas i-grid corresponds to the particular grid being evaluated (i.e. i in N-total grids). This equation (Equation 1) was adapted from the IUCN equation used to estimate population reduction (IUCN 2022). Using this approach, it is possible to determine whether the class areas from the first year have decreased or increased compared with the current class areas.

Transition between classes involves identifying the conversion of any given class (i.e. threats and/or natural areas) to another from the first to the last year to analyse their spatiotemporal dynamics. We aimed to determine whether the drivers had been transformed into other drivers or whether their expansion had contributed to habitat loss through forest conversion. We also wanted to determine whether forest areas had taken over areas previously occupied by these drivers, thereby contributing to habitat regeneration. We calculated the transition maps by combining the codes for the first and last years (Equation 2):

{Transition}_{i - grid} = (C_{i - th - class} {FY}_{i - grid} \times 100) + C_{i - th - class} {LY}_{i - grid}

((Equation 2))

where CFY is the class category identified in the pixel in the first year and CLY is the class category identified in the pixel in the last year. We multiplied the first part of the equation by 100 to identify the type of transition. Classes can be more readily identified by introducing a value shift of 100, which facilitates a clear distinction between transitions. For instance, a 106 code indicates that a pixel identified as a forest (pixel = 1) in 1988 was transformed into a livestock area (pixel = 6) in 2020, that is, (1forest × 100) + 6 livestock = 106. This equation was sourced from the MapBiomas project (see details in: https://brasil.mapbiomas.org/en/colecoes-mapbiomas/), which provides data on land cover changes in one pixel over consecutive years (MapBiomas Project 2023). As the specific time window used in this study (i.e. from 1988 to 2020) was not provided by the project, we calculated the aforementioned transition rates. Based on the same equation and using the annual fire data available from the MapBiomas project (2023), we also determined which classes were most likely to have fire occurrences. In doing so, we derived annual estimates of fire incidence from 1988 to 2020. As aforementioned, the i-grid corresponds to the particular grid being evaluated [i.e. i in 1 to N, where N is the total number of pixels (or cells)], and the i-th-class corresponds to any class of land use evaluated.

Heterogeneity and intensity of the drivers

We overlapped the species range limits with a 400-ha (2000 × 2000 m) cell grid, a size used by the IUCN (2022) to calculate the Area of Occupancy (AOO). In this study, we used this grid size only to locate the drivers. Then, using the binary map derived from our multiple spatial data extractions, we estimated the heterogeneity of the drivers in each gridded cell. Therefore, this parameter indicates the number of drivers in each 400-ha grid cell by simply counting all the drivers present in the cell.

The intensity of drivers is a parameter that combines both the persistence (indicated by the number of years each driver occurs in each pixel, ranging from 1 to 32) of each threat within a grid cell from 1988 to 2020 and the current area (ha) occupied by each threat. To do so, we first summed all binary rasters with the presence/absence of drivers in the time series window. We then corrected these maps by subtracting the summed raster from the current raster, once the driver was originally present but is currently absent. We calculated the current area from the last year's map (i.e. from 2020) by summing all pixels of each driver within the 400-ha grid cell. To estimate the intensity of the driver, we adopted the following equation (Equation 3):

{Intensity}_{grid} = \sum \frac{P_{i - grid} \times A_{i - grid}}{\max_{i - th - grid}}

((Equation 3))

where P (Persistence) indicates how long the driver is present on that 400-ha grid cell (time in years), A (Area) represents the amount (extent in hectares), i-grid corresponds to the particular 400-ha grid being evaluated (i.e. i in N-total grids), and i-th-grid corresponds to any grid evaluated with the largest intensity of drivers. In case it has several values ranging from 1 to 32, we used the mean of the values. The final intensity raster is the sum of persistence × area estimation of each driver (e.g. livestock persistence × area + wood and pulp plantation persistence × area, etc.). We then standardised both parameters (heterogeneity and intensity) on a scale ranging from 0 to 1 based on the largest heterogeneity and on the largest intensity, respectively, obtained for the i-th-grid, where 1 indicates the largest heterogeneity and the largest intensity of drivers. All spatial analyses were conducted using QGIS software, version 3.18.3 (QGIS 2020).

RESULTS

Seven major drivers of habitat loss and two classes of natural areas were identified for the maned three-toed sloth species (Fig. 2). However, the spatial pattern was distinct across the distribution ranges of each species. Although livestock farming and ranching dominate the range areas of the two species (Bradypus torquatus – 49%; Bradypus crinitus – 56%), covering an area even larger than that of native forest (Bradypus torquatus – 42%; Bradypus crinitus – 36%), the second and third threat classes were distinct. For Bradypus torquatus, wood and pulp plantations (4.24%), followed by residential and commercial development (1.81%), dominated the landscapes overlapping the species ranges, whereas for Bradypus crinitus, the second and third threat classes were residential and commercial development (3.87%) and annual and perennial crops (1.42%), respectively. Other threats account for less than 4.5% of the coverage of the distribution ranges of both species (Fig. 2).

In general, the drivers exhibited a relatively stable trend, either increasing or decreasing, over the three-decade time series (Appendix S1). Once we analysed the time series for the relative change from the first to the last year, we observed that almost all threats had increased during that period (Table 1). The exception was the fire & fire suppression events, which exhibited a decrease (Bradypus torquatus – 86%; Bradypus crinitus – 86%; Table 1). Annual and perennial non-timber crops showed rampant growth of 2796.35% (c. 87% year⁻¹ representing 562.53 ha year⁻¹) within the Bradypus torquatus range and 146.46% (c. 4.58% year⁻¹ representing 601 ha year⁻¹) within the Bradypus crinitus range (Table 1). Mining also showed a high relative increase for both species (Bradypus torquatus 532%, Bradypus crinitus 375.70%; Table 1). Mining and non-timber crops increased due to their spatial expansion into livestock areas (Fig. 3). Forest formation areas decreased by 11% in the Bradypus torquatus range (Table 1) but increased slightly (i.e. 1.42%) in the Bradypus crinitus range (Table 1).

Table 1. Absolute (ha) and relative (%) current area, and absolute (ha) and relative change (%) of each class from the first year (1988) to the last year (2020) of the time series. Red numbers indicate the highest values for that category

Class	Bradypus torquatus				Bradypus crinitus
Class	Current area (ha)	Current area (%)	Absolute change (ha)	Relative change (%)	Current area (ha)	Current area (%)	Absolute change (ha)	Relative change (%)
Natural formations
Forest formation	2275998.48	40.80	(−) 270417.21	(−) 10.62	856204.68	35.54	(+) 11951.62	(+) 1.42
Other natural formations	269143.52	4.82	(+) 23154.75	(+) 9.41	74242.28	3.08	(+) 8015.32	(+) 12.10
Drivers
Residential and commercial development	103257.48	1.85	(+) 43716.14	(+) 73.42	96492.09	4.00	(+) 32118.14	(+) 49.89
Annual and perennial non-timber crops	19227.60	0.34	(+) 18563.74	(+) 2796.35	33370.07	1.39	(+) 19830.38	(+) 146.46
Wood and pulp plantations	230008.11	4.12	(+) 108585.62	(+) 89.42	32099.42	1.33	(+) 10042.18	(+) 45.53
Livestock farming and ranching	2677952.94	48.00	(+) 100072.09	(+) 3.88	1315505.37	54.60	(−) 78304.86	(−) 5.62
Marine and freshwater aquaculture	2258.48	0.04	(+) 529.03	(+) 30.59	1291.41	0.05	(−) 1058.6	(−) 45.07
Mining	881.55	0.02	(+) 740.81	(+) 526.40	85.87	0.00	(+) 67.82	(+) 375.70
Fire	20.42	0.00	(−) 123.18	(−) 85.78	20.42	0.00	(−) 124.92	(−) 85.98

During this 32-year period, deforestation was almost five times larger in the range of Bradypus torquatus than in the range of Bradypus crinitus (659098.70 ha and 139013.20 ha of forest loss, respectively) (Fig. 3). The reverse process (i.e. the forest regeneration) occurred in 382750.21 ha within the Bradypus torquatus range and in 150665.62 ha within the Bradypus crinitus range. For both species, livestock was the main driver of deforestation, accounting for 91% and 93% of the forest loss for Bradypus torquatus (600143.13 ha) and Bradypus crinitus (128818.37 ha) (Fig. 3). Conversely, a significant area of former cattle ranch land is currently undergoing forest regeneration (87% and 98% of total forest regeneration in Bradypus torquatus and Bradypus crinitus ranges, respectively; Fig. 3). Wood and pulp plantations, residential & commercial development, and annual and perennial non-timber crops also contributed, although to a much smaller extent, with forest lost within both species' ranges (Bradypus torquatus: 5.83%, 0.73%, 0.66%, respectively; Bradypus crinitus: 4.78%, 1.08%, 0.80%, respectively). The expansion of these drivers was not followed by forest regeneration, which showed a negative balance, except for wood and pulp plantations in the Bradypus torquatus range (11%).

Despite the loss of forests, the emergence of new human-modified areas was mainly observed in anthropic regions, such as annual and perennial non-timber crops, mainly for Bradypus crinitus (Fig. 3). For this threat, which experienced the highest rate of change among the analysed classes at the Bradypus torquatus range, most parcels occurred over older livestock areas (75%), whereas only 22% occurred in forest formation areas (Fig. 3). In the Bradypus crinitus range, mining – which experienced the highest relative growth rate (Increase of 67.82 ha, corresponding to a relative growth of 375.70%) – mainly occupied areas formerly used for livestock (54.61 ha, 76%; Fig. 3).

Most fire events – which experienced a drop in both distributions (Table 1) – occurred over the livestock areas (Fig. 4). For Bradypus torquatus, fire in forest formations has decreased over the years, although it is the third class that is most affected by fire (Fig. 4). The number of fires in other natural areas has increased over the past three decades, being the second most affected within the Bradypus torquatus range (Fig. 4).

Driver heterogeneity and intensity

There is great heterogeneity of drivers in the southern range of Bradypus torquatus. For Bradypus crinitus, there is clearly greater heterogeneity in the northern range (Espírito Santo; ES) than in the southern range (Rio de Janeiro; RJ) (Fig. 5). Driver intensity, on the other hand, is concentrated in the extreme north, south, and western ranges of Bradypus torquatus. For Bradypus crinitus, the intensity was concentrated in the southern, northern, and eastern limits of the northern portion (ES) and in the southern and northeastern regions of the southern portion (RJ) (Fig. 5). By analysing heterogeneity and intensity together, we found that the central-western region of the distribution of Bradypus torquatus is more negative for the species, since it presents low heterogeneity and high intensity, as well as Bradypus crinitus distribution in the southern region of Espírito Santo and Rio de Janeiro. On the other hand, points in the southern distribution of Bradypus torquatus can be considered more positive areas, as well as the northwestern region of the distribution of Bradypus crinitus in Espírito Santo (Fig. 5).

For both sloths, residential and commercial development are mainly concentrated in large urban areas, whereas annual and perennial non-timber crops and wood and pulp plantations are mainly concentrated in southern Bahia (Bradypus torquatus) and Espirito Santo State (Bradypus crinitus) (Appendix S1). Moreover, livestock and ranching are widely distributed across their ranges, similar to fire occurrence, but less intense (Appendix S1). Aquaculture (Bradypus torquatus – South Sergipe, Bradypus crinitus – South Rio de Janeiro; Appendix S1) and mining (Bradypus torquatus – West Bahia, Bradypus crinitus – South Rio de Janeiro; Appendix S1) are sparsely concentrated. Finally, it is evident that areas undergoing significant relative change (Annual and perennial non-timber crops and Mining; Table 1) have lower intensity due to their expansion over the time window analysed (Appendix S1). Conversely, livestock farming and ranching and residential and commercial development are well-established land uses in the biome, and their occupied areas are mostly of high intensity. (See the Appendix S1 for a full overview of driver heterogeneity and intensity separately).

DISCUSSION

Our overview of spatially explicit threats (>30 years) impacting two endangered species of Neotropical sloths indicates that livestock is the primary driver of habitat loss for both species. Annual and perennial non-timber crops, residential and commercial development, and wood and pulp plantations are also important drivers of habitat loss but reach much lower extension than cattle ranching. The spatiotemporal distribution of these threats was mainly confined to the margins of both species' distributions, neighbouring important forest remnants for species survival in the medium- to long-term (Moreira et al. 2014). A number of other important threats to the group, such as selective logging, vehicle injuries, electrocution, and dog attacks (PM Santos unpublished data), were not considered in this study, mainly due to the difficulty of collecting this information. Similarly, although agroforestry systems (mainly composed of cocoa plantations shaded by native trees) also play an important role for Bradypus torquatus to thrive in southern Bahia (Cassano et al. 2011, Falconi et al. 2015), this use was not studied due to the lack of temporal data. Furthermore, in the maps provided by the MapBiomas project (2023), most cocoa plantations shaded by native trees are classified as forest formations. Nevertheless, to the best of our knowledge, this is the first study to simultaneously analyse the broad spatial and temporal patterns of anthropogenic land use drivers of habitat loss for these two maned sloth species.

Current composition patterns

This study highlights the overwhelming preponderance of livestock areas in both sloth ranges. This element may have a pervasive influence on sloth ecology and behaviour (Garcés-Restrepo et al. 2018), given their strictly arboreal habits (Sunquist & Montgomery 1973, Chiarello 1998b, Neam & Lacher 2015). Livestock production does not provide any resources or conditions suitable for this forest-dependent group (Falconi et al. 2015). Crossing larger livestock or anthropic areas can result in exposure to opportunistic predation (Vaughan et al. 2007) and energy expenditure that is higher than the corresponding resource gains (Goffart 1971). Evidence suggests that in human-dominated environments, the maned three-toed sloth has a high occupancy probability when forest cover exceeds 35% (Santos et al. 2019). In landscapes with less than 20% forest cover, consisting of pasture and exposed soil, the probability of species' occupancy probability is significantly reduced, often reaching zero (Santos et al. 2019).

Forests in human-altered landscapes are prone to negative interactions with non-habitat areas, altering the climatic conditions and structure of the forest (Santos et al. 2008, Tabarelli et al. 2008, Rocha-Santos et al. 2016). Seed germination from shade-tolerant trees may be hindered (Rocha-Santos et al. 2016), and although individual maned sloths may use some shade-intolerant tree species, their suite of trees used as a food sources or for other daily activities is locally concentrated in a few species from different ecological groups (Chiarello 1998a, Giné et al. 2022, Mureb et al. 2023). Furthermore, forests near pastures face challenges such as cattle intrusion, leading to soil compaction and reduced plant seedling survival (Ali et al. 2020, Searle & Meyer 2020, Mochi et al. 2022).

Change rate and transition dynamics

In general, most drivers showed a relatively discrete increase in the relative rate of change. We highlighted annual and perennial non-timber crops, which increased by 2796% (18563.74 ha in absolute terms) over the last 32 years within the Bradypus torquatus range and was the land cover with the second highest rate of change within the Bradypus crinitus range (146.46%, 19830.38 ha in absolute terms). Notwithstanding the relatively low change rate presented by the other drivers, together all the analysed drivers are still responsible for the loss of more than 700000 ha of forest areas, mainly driven by the expansion of livestock areas.

To meet the high food demand, Brazil has produced more than one billion tonnes of agricultural products (AGROSTAT 2023). Cropland expanded 14 Mha in the Atlantic forest between 2010 and 2015 (Soterroni et al. 2018), reflecting the pattern of agribusiness expansion associated with high rates of deforestation in the tropics (Soterroni et al. 2018, Di Minin et al. 2019, MPES 2022). Similarly, the expansion of timber and pulp plantations is directly linked to the growing global demand for these commodities (FAO 2022), with Brazil being one of the main suppliers (Nobre 2020, IBÁ 2022). In the last 35 years, forestry has expanded by more than four million hectares in the Atlantic Forest, covering 3.8% of its original area (MapBiomas Project 2023). This increase in demand has led to the conversion of natural areas into forestry, especially in southern Bahia and Espírito Santo (MapBiomas Project 2023, https://brasil.mapbiomas.org/en/destaques/), regions with the highest concentration of this commodity in the study.

Besides the agricultural and forestry sectors, residential and commercial development accounted for the third highest amount of deforestation in both species ranges. Expansion of land speculation is one of the main drivers of habitat loss in the mountainous region of Espírito Santo (MPES 2022), an important stronghold for Bradypus crinitus (Santos et al. 2016, 2019), mainly through illegal land subdivision (MPES 2022). Similarly, construction companies have been targeting the north coast of Bahia to build luxury condominiums, many of which have been constructed without any environmental licence, leading to the introduction of exotic species and the invasion of protected areas (MPBA 2010, 2015, Prefeitura Municipal de Mata de São João 2021). Consequently, both the traditional human population and the local species have become marginalised (Brito 2018).

In addition to being the most common and long-standing driver in the range of both species, livestock is also a high-intensity driver. High intensity can lead to a range of impacts on biodiversity (Ewers & Didham 2006, Swift & Hannon 2010). Furthermore, our results suggest that higher intensity regions are less heterogeneous, which is more detrimental to biodiversity because they are less permeable and have more contrasting land-use matrices. For example, Bradypus crinitus individuals have been observed using coffee plantations in advanced growth stages and timber and pulp plantations as movement corridors between fragments (Santos et al. 2016). However, cattle-dominated areas that have been established and maintained for years have a negative impact on the species' occurrence (Santos et al. 2019).

Apart from the main drivers mentioned, there has been a notable increase in mining activities and, to a lesser extent, aquaculture. While aquaculture is predominantly associated with aquatic environments (Franco et al. 2018), inland aquaculture occasionally requires the creation of terrestrial ponds (Boyd & Gross 2000), resulting in habitat loss, as evidenced during a field visit to a significant forested area at the northern limit of the Bradypus torquatus distribution. Despite the expansion of these activities, the total area occupied in both ranges remains relatively small (<1%). Therefore, a slightly larger increase in occupied area may not necessarily indicate a significant impact.

Fire regimes have decreased and are concentrated in anthropic regions, mainly in livestock areas. However, the natural areas within the native range of Bradypus torquatus have experienced an increase in area affected by fire. Historically, fire has been used primarily to expand and maintain livestock and deforested areas (Cochrane et al. 1999, Cochrane 2003, Barona et al. 2010), resulting in unintentional fires spreading across forest formations (Gascon et al. 2000). Therefore, this traditional practice of setting fires in pastures may be responsible for the increase in fires in other natural areas. Alternatively, the deforestation of nearly 700000 hectares of forest can have a significant impact on the climate by reducing precipitation (Smith et al. 2023) and consequently prolonging drought (Pivello et al. 2021). Drier areas are likely to experience more wildfires (Pivello et al. 2021), with varying impacts on supply conditions and resources (Silva et al. 2020).

Livestock areas within the range of Bradypus torquatus exceed those of 30 years ago, mainly by encroaching on natural areas, leading to an alarming increase in deforestation in the region. Conversely, within the range of Bradypus crinitus, there has been a noticeable shift from pasture to agriculture, indicating an intensification in agricultural production without additional deforestation. This is evidenced by the fact that pastureland has visibly shrunk over the last 30 years to make way for forest regrowth, which has also occurred significantly over timber and pulp plantation areas. The Southeast Atlantic Forest region consists mainly of consolidated agricultural areas (limited land availability and high prices; Barretto et al. 2013). Thus, to ensure agricultural productivity, it is necessary to optimise land use in terms of spatial compartmentalisation and reduction of cultivated areas, thereby reducing habitat loss (Sparovek et al. 2010). Meanwhile, the northeastern Atlantic Forest contains many agricultural frontier areas where there are abundant and inexpensive lands (Barretto et al. 2013). The increase in livestock areas in the Bradypus torquatus range and the decrease in the Bradypus crinitus range may reflect the ‘migration’ of livestock production from the agriculturally consolidated areas (southeast) to the agricultural frontier areas (northeast).

Finally, the increase and establishment of land-use drivers of habitat loss can also lead to several other conflicts related to the presence or proximity of humans and their infrastructure, where arboreal animals, including sloths, can be persecuted by domestic dogs (Vaughan et al. 2007) or fall victim to roadkill (Ferreguetti et al. 2014), electrocution (Pedrosa et al. 2021), and illegal animal trade (Carder et al. 2018).

Conservation perspectives

According to our findings, some of the human-dominated land expansion has occurred primarily on vacant anthropogenic land, mainly within the range of Bradypus crinitus. Thus, despite the alarming situation we have uncovered, our analyses also suggest that a more sustainable economy is achievable. Studies show that it is possible to increase the productivity of current agricultural landscapes, such as cattle, timber production, and other crops, without further converting natural habitats (Strassburg et al. 2014, Soterroni et al. 2018, de Mello et al. 2021). Greater commitment from stakeholders in these sectors is therefore needed to ensure that this happens. For example, while plantation forest companies are increasingly seeking green seals to demonstrate their commitment to greener and more sustainable management practices (Nobre 2020, IBÁ 2022), a significant part of the expansion of managed forests still occurred in areas of forest formation (Bradypus torquatus – 22%; Bradypus crinitus – 32%).

The recent increase in the deforestation rate of the Atlantic Forest is a side effect of weakness or noncompliance with the Atlantic Forest Law, which regulates land use and protects its forests (Brasil 2006). According to this law, areas of secondary native vegetation can be suppressed if they are in the public interest or for social purposes and must necessarily be compensated. Therefore, it is necessary to determine whether such deforestation is within the law in order to avoid future deforestation. In addition, it is imperative to preserve the existing vegetation by evaluating and implementing new protected areas. Although the Atlantic Forest biome has the potential for natural regeneration in abandoned agricultural areas, which supports forest recovery (Crouzeilles et al. 2019, 2020), newly established forests differ from established old-growth or late secondary forests, which are critical for species such as maned sloths (Falconi et al. 2015, Santos et al. 2022). Disturbed Atlantic Forest areas can take decades or centuries to fully recover (Liebsch et al. 2008, Poorter et al. 2016). Therefore, although the regeneration trend is positive, especially for Bradypus crinitus, it cannot fully replace the previous forest types.

In other areas, compliance with environmental legislation is required, along with forest regeneration of legally protected areas defined by the Native Vegetation Protection Law (Brasil 2012), the Legal Reserves (LR, native vegetation in private agricultural lands required by law), and the Areas of Permanent Preservation (APP, native vegetation in sensitive areas, such as hilltops and riparian vegetation). Overall, these areas are in deficit throughout the Atlantic Forest (Metzger et al. 2019, de Mello et al. 2021), and their restoration, preservation, and compensation are essential to achieve key conservation goals and ensure the long-term maintenance of biodiversity. For example, the use of agricultural sustainability certificates (e.g. Rainforest Alliance; Rainforest Alliance 2023) can incentivise landowners to better comply with environmental regulation (d'Albertas et al. 2023). The future will require better planning of urban and economic land use, not only to reduce habitat loss and conserve natural resources but also to allow for important forest regeneration processes to ensure the long-term viability of wild populations.

ACKNOWLEDGEMENTS

We sincerely thank the two anonymous reviewers for their important contributions to our manuscript. We thank the Instituto Nacional da Mata Atlântica for their invaluable support in the planning and development of this manuscript. In addition, we extend our sincere thanks to the dedicated team of the MapBiomas project for their exceptional efforts in collecting, analysing, and sharing comprehensive data on land-use dynamics in Brazil and beyond. AGC thanks the Brazilian Science Council for a research fellowship (CNPq 308660/2021-8). We dedicate this article to Gustavo A.B. da Fonseca, whose lifelong commitment to biodiversity conservation is a great inspiration to the new generation of conservationists.

FUNDING

This study was supported by the Programa de Capacitação Institucional from Instituto Nacional da Mata Atlântica (PCI/INMA), which also provided fellowships via National Council for Scientific and Technological Development – CNPq to PMS (317795/2021-0. 300893/2022-1, 300499/2023-0, and 301376/2023-9). JAB is supported by Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq) postdoctoral fellowship (grant 150261/2023-3). AGC has a research fellowship from CNPs (grant 308660/2021-8).

Open Research

DATA AVAILABILITY STATEMENT

The range maps and the land-use land cover maps are freely available at https://www.iucnredlist.org/resources/spatialdata-download and https://mapbiomas.org/download, respectively. Details of the R script operationalisation and database can be requested from the corresponding author (P.M. Santos; [email protected]). See also github (https://github.com/pmqsantos/Maned_sloths_threats.git) for the R code and interactive Sankey chart. See Appendix S1 for further details.

Supporting Information

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Volume54, Issue3

July 2024

Pages 273-287

What, where, and how: a spatiotemporally explicit analysis of the drivers of habitat loss within the range of maned three-toed sloths (Bradypus torquatus and Bradypus crinitus)

Abstract

Resumo

INTRODUCTION