Endemic areas and distribution patterns of Spirostreptida
The spirostreptidan fauna of Brazil is largely unknown primarily due to the scarcity of trained taxonomists in the country, with new records often turning out to represent undescribed taxa (Hoffman et al. 1996, 2002). The areas of endemism detected in this study were recovered at different levels of geographical congruence, and as such, we delimited them on the basis of their contiguous grids and number of shared species. Six endemic areas are herein proposed for the Brazilian Spirostreptida: Northern Serra Geral (NSG), Southeastern mountain ranges (Smm), Cerrado and Atlantic Forest zone (CAF), Eastern Cerrado and Serra Espinhaço (ECS), Pantanal (Pt), and Southern Amazon and Cerrado zone (SAC) (Table 1).
Table 1
Areas of endemism of Brazilian Spirostreptida. See Fonseca (1985), Lorenzi (1992), Coutinho (2006), Colombo and Joly (2010), and Alvares et al. (2013) for details of the biomes and ecoregions.
Endemic Area | State | Biome | Ecoregion | Features |
Northern Serra Geral (NSG) | Santa Catarina, Paraná, São Paulo | Atlantic Forest | Araucaria Forest, Atlantic provinces | The Serra Geral is a mountain range located in southern Brazil, delimited by the Paraná Basin, and drained by tributaries of the Uruguay River. The region runs parallel to the Atlantic coast in its eastern portion and includes a narrow coastal plain connected to the southern Serra do Mar system. Its topography ranges from 900 to 1,200 meters a.s.l. with large canyons in the eastern portion. The annual mean temperature ranges from 10 to 22°C with temperatures reaching from 0 to 36°C in some areas), annual rainfall ranges from 1300 to 2200 mm. The area is characterized by largely subtropical vegetation. |
Southeastern mountain ranges (Smm) | Mostly São Paulo | Atlantic Forest | Araucaria Forest, Paraná Forest, Atlantic provinces | The region includes three of the main mountain ranges in southeastern Brazil, the Serra da Paranapiacaba (ca. 1,000 meters a.s.l.), Serra da Mantiqueira (ca. 2,800 meters a.s.l.), and Serra do Mar (ca. 2,200 meters a.s.l.). The region has a variety of climates with annual mean temperature ranging from 10 to 26°C and annual rainfall ranging from 1000 to 2500 mm. The vegetation is composed of tropical rainforests and patches of forests of Brazilian pine Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae) and Podocarpus lambertii Klotzsch (Podocarpaceae). |
Cerrado and Atlantic Forest zone (CAF) | Mosly Goiás, Minas Gerais, São Paulo | Cerrado, Atlantic Forest | Paraná Forest, Cerrado provinces | The zone may be viewed as an ecotone between the southeastern Cerrado and the western Atlantic Forest. The region is characterized by a variety of climates, with annual mean temperature ranging from 18 to 26°C and annual rainfall ranging from 1000 to 1900 mm. Elevation ranges from 250 to 3,000 meters a.s.l. The area is composed of a shifting mosaic of habitats, with both biomes occurring in well-drained areas primarily along the Grande, Paranaíba, and Tietê rivers, located between strips of gallery, deciduous, and semideciduous seasonal forests. |
Eastern Cerrado, Serra do Espinhaço (ECS) | Bahia, Minas Gerais | Cerrado, Caatinga, Atlantic Forest | Cerrado province | The region includes the Serra do Espinhaço mountain range (ca. 2,000 meters a.s.l.), which runs through the states of Minas Gerais and Bahia, and the mineral-rich “Iron Quadrangle” (Quadrilátero Ferrífero) area, composed of meta-sedimentary rocks. The region is primarily drained by the São Francisco and Doce rivers. The annual mean temperature ranges from 20 to 26°C and the annual rainfall ranges from 700 to 1600 mm. The vegetation of the region is typical of the Cerrado, represented by a shifting mosaic of habitats, including rupestrian grasslands, and gallery forests. |
Pantanal (Pt) | Mato Grosso, Mato Grosso do Sul | Pantanal | Rondônia province | The area corresponds to the Pantanal biome: a tropical wetland area interspersed with flooded grasslands. The annual mean temperature ranges from 22 to 26°C and the annual ranges from rainfall 1000 to 1900 mm. The region includes tropical grasslands, dry forests, and semiarid lowlands with a mosaic of rainforest and semiarid woodland plants. |
Southern Amazon and Cerrado Zone (SAC) | Mato Grosso, Amazonas (in part) | Cerrado, Amazon Forest | Cerrado, Xingu-Tapajós provinces | The zone may be viewed as an ecotone between the Cerrado and the southern Amazon. The annual mean temperature ranges from 24 to > 26°C, and the annual rainfall ranges from 1900 to 3100 mm. The elevation ranges from 200 to 800 meters a.s.l. The heterogenous vegetation is represented by a mosaic of habitats including rainforests, transitional, and semi deciduous forests. |
Figures. |
Most of these endemic areas are contained within the Atlantic Forest biome (Fig. 10a–e), which has been previously shown to be an area of endemism for many invertebrate and vertebrate species (Silva et al. 2004; Sigrist and Carvalho 2009; Bispo and Lecci 2011; Mendes and Sebastiani 2012; Trevine et al. 2014; DaSilva et al. 2017; Tonetti and Cavarzere 2017). Overall, two regions in the biome are highlighted in relation to their geological aspects and endemic species assemblages, the Atlantic coastal region and its continental islands, (e.g. Alcatrazes, Anchieta, Ilhabela, Moela, and Queimada Grande) and the mountain ranges in the eastern part of the region.
Historically, the Atlantic coastal region has received considerable attention due to its very restricted millipede fauna (Brölemann 1909; Schubart 1945a, 1949, 1950), and more recently for the common occurrence of non-native species (Bouzan et al. 2018; Iniesta et al. 2020, 2021, 2022a). Most of the continental islands in the biome were connected to the continent by a land bridge during the recession of seawater at the time of the Last Glacial Maximum (~ 85,000–15,000 years ago), with many vertebrate and invertebrate populations remaining isolated from each other and the continent (Martin et al. 1986; Fleming et al. 1998). Schubart (1949: 239) suggested this scenario for some millipede species when comparing their wide variation in body size and patterns of coloration between continental and insular populations. The presence of continental islands, large rivers (e.g. Tietê and Paraná), and mountain ranges (e.g. Serra do Mar, Serra de Paranapiacaba, and Serra da Mantiqueira) is a significant factor affecting the distributional patterns and endemism of Spirostreptida in the Atlantic Forest, specifically following the climatic changes during the Pleistocene (see Cabanne et al. 2016). Studies have shown that some mountain ranges in the Atlantic Forest (e.g. the Smm area) correspond to routes of species diversification, leading to higher rates of endemism as compared to surrounding areas (Grazziotin et al. 2006; Bragagnolo et al. 2015; DaSilva et al. 2015; Oliveira et al. 2015; Lago-Barcia et al. 2020).
Historical processes, such as climatic events during the last ~ 2 M.Y., along with corresponding alterations of the phytophysiognomy of tropical forests due to fluctuations in wet and dry climates have been demonstrated to have influenced the spatial distributions of birds (Cabanne et al. 2016), beetles (Silva and Vaz-de-Mello 2020), and harvestmen (DaSilva et al. 2017) in the Atlantic Forest (Haffer 1969; Ledru et al. 2005; Silveira et al. 2019; Rodríguez-Zorro et al. 2022). Similarly, Walker et al. (2009) revealed that the broad distribution of some millipede species of Narceus Rafinesque, 1820 (Juliformia, Spirobolida) in the Appalachian Mountains is a result of a complex evolutionary history with multiple refugia in southeastern North America and population expansions in the north during the Pleistocene. Decker (2016) suggested that paradoxosomatid species (Polydesmida, Paradoxosomatidae) in Australia have high genetic variability as consequence of multiple Pleistocene refugia in the southeastern Australian mainland. In fact, historical climatic events in the Atlantic Forest may partially explain the pattern of distribution of Spirostreptida species, especially considering the relevance and influence of environmental conditions on the distribution of low vagility millipede taxa (David 2009; Gilgado et al. 2022).
The highest species richness is primarily found in the states of São Paulo and Rio de Janeiro (Figs. 4a, b, 5a). This is not unexpected, as most of our knowledge regarding Brazil’s millipede fauna is a result of extensive studies by the European naturalists O. Schubart and H. W. Brölemann at the beginning of the 19th century, which resulted in the description of a large number of species and distributional data from these states (Brölemann 1904, 1909; Hoffman 1980; Bouzan et al. 2018; Iniesta et al. 2021). Since these early studies, however, few others have focused on the taxonomy of Brazilian Spirostreptida (see Krabbe 1982).
The endemic pattern of Spirostreptida in the Cerrado (areas CAF, ECS, and SAC) may be best explained by the physiognomically heterogeneous vegetation of the biome (Lorenzi 1992) (Fig. 10f). Overall, these areas present a composition typical of a semi-humid tropical climate (Alvares et al. 2013) with a shifting mosaic of relatively well-drained gallery forest habitats along streams (e.g. São Francisco and Paraná rivers). Due to the low vagility of millipedes, it is plausible that many species have very limited distributions in specific areas across the biome (e.g. eastern portion of the Cerrado in CAF, or western portion of the Cerrado in SAC) resulting in a distinctive faunal composition. The expansions and contractions of woodlands under cool and moist conditions in the Cerrado during the Last Glacial Maximum may have been influential in the diversification of species (Oliveira et al. 2020), although this has not been well documented for millipedes.
Most studies in the Pantanal have revealed high species richness influenced by a local mosaic of forests and savannas in extensive floodplains (Marques et al. 2016; Martins et al. 2021). The composition of millipedes shows high dissimilarity and high turnover of species as compared to other Brazilian terrestrial biomes (Fig. 6). The spatial distribution of Spirostreptida is largely concentrated in the northern part of the region and in the Cáceres and Poconé subregions (Fig. 4a, b) where extensive faunal surveys have been conducted during the last two decades (Golovatch et al. 2005; Battirola 2009, 2017; Santos-Silva 2019; Iniesta et al. 2022b). Most Spirostreptidae found in the Pantanal migrate along the surface following the flood line during high water periods (Battirola 2017). The same activity has been observed in some Central Amazonian millipede species (Adis 1981, 1992) in areas close to the Araguaia and Amazon rivers (Schubart 1947a). Most populations found in these areas are composed of large-bodied individuals with relatively high mobility (Santos-Silva, 2019) as compared to species from other endemic areas (e.g. Smm).
Most species recovered in the SAC endemic area are concentrated in the southern Amazon and in the northern Cerrado, a transitional zone partly composed of open ombrophylous forest with spaced vegetation and characterized by long periods of drought. The low species richness of the Amazon forest, as compared to the transitional area to the Cerrado, is likely a result of the limited number of taxonomic studies on the millipede fauna of the region (Brölemann 1904; Hoffman et al. 1996, 2002).
In general, little is known regarding the ecological drivers affecting the distributional patterns of Spirostreptida at small and medium scales. Nonetheless, average temperature and humidity have been recognized as important bioclimatic variables in determining the occurrence of millipede species around the world (David 2015; Gilgado et al. 2022; Iniesta et al. 2022a). Some spirostreptidans have a low ecological demand regarding their occurrence and abundance in old growth forests or in poly/monocultures of Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae), Eucalyptus L'Hér. (Myrtacea), Coffea L. (Rubiacea), Zea mays L., Citrus reticulata Blanco (Rutaceae), Nicotiana L. (Solanaceae), and beans (Fabacea) depending only on relative humidity and availability of organic resources (Schubart 1942, 1945b, 1949, 1955). In addition, some synanthropic species found in close proximity to residential areas are known for their occasional population outbreaks (Schubart 1944, 1945b, 1947b, 1958).
Conservation status of Spirostreptida
Most Brazilian Spirostreptida occur in areas that have not been designated as conservation units or do not have conservation policies in place. To date, five spirostreptidan species are classified as either endangered or critically endangered according to the most recent list of threatened species provided by Brazilian authorities (Fig. 9). All of these taxa occur in subterranean environments and represent troglomorphic species with specialized morphological traits, such as Pseudonannolene ambuatinga Iniesta & Ferreira, 2013, P. lundi Iniesta & Ferreira, 2015d spelaea Iniesta & Ferreira, 2013 (Pseudonannolenidae) (see Sket 2008).
In Brazil, since the publication of the Federal Decree n°6640/2008 and the Normative Instruction MMA 02/2017, subterranean environments are protected by law according to geological and biological attributes (e.g. presence of troglomorphic species), so that only caves of maximum relevance are fully protected (Brasil 2008, 2017). As a result, most of the Brazilian cave fauna has been extensively studied in the last two decades, resulting in the description of species, habitats, and biological attributes. With the exception of P. lundi, which occurs in a single, relatively well-preserved, rarely visited cave, the remaining species occur in areas which are at least partially impacted by anthropogenic activities. The caves where P. ambuatinga occurs are the focus of an intense investment in mining operations of carbonate rock to produce cement, lime, and soil correctives, directly affecting the subterranean environment and cave communities (Iniesta and Ferreira 2013a). Other impacts observed in the surrounding areas include deforestation, agropastoral practices, and construction in close proximity to drainages and/or cave entrances (Cavalcanti et al. 2012). Pseudonannolene spelaea is regarded as an Amazon Rainforest relict, occurring only in caves of the Serra do Carajás located in the region of the Floresta Nacional de Carajás (FLONA-Carajás), an Amazonian landscape composed of large plateaus of ferruginous outcrops (Iniesta and Ferreira 2013b). This region has experienced intensive exploration of its vast iron ore deposits, which has influenced the local economy and increased environmental pressures (Palheta et al. 2017). Other endemic invertebrates, such as beetles, crickets, flies, centipedes, spiders, and terrestrial isopods, are also found in these ferruginous outcrops, reinforcing the urgency of additional studies to understand the impacts of mining operations on species distribution and conservation (Iniesta et al. 2012; Brescovit et al. 2018; Campos-Filho et al. 2020; Chagas-Jr and Bichuette 2018; Bouzan et al. 2019; Asenjo et al. 2019; Junta et al. 2020; Teodoro et al. 2021). Although no apparent morphological features indicate the restriction of P. imbirensis to caves, all known specimens have been collected from caves or cave entrances (Fontanetti 1996; Gallo and Bichuette 2017; Bichuette et al. 2019). Populations of P. imbirensis from the Angélica, São Bernardo II, and São Vicente II caves have been considered as troglobitic, while those from the Terra Ronca II cave have been considered as troglophilic by Gallo and Bichuette (2017). Among the five IUCN threatened spirostreptidan species, P. tocaiensis is a typical troglophilic species known only from its type locality, Toca cave (Itirapina, São Paulo state), which has a fairly well-preserved surrounding area (Fontanetti 1996; Freitas et al. 2004). Importantly, the most recent presidential decree (decree n°10.935, January 12, 2022) is currently allowing the destruction of even the most conservation relevant caves in Brazil, and represents a serious threat to all Brazilian subterranean biodiversity (see Ferreira et al. 2022).
Although the southeastern region has the highest spirostreptidan species richness in Brazil (Figs. 4a, 5a), it also has the highest concentration of threatened species (Fig. 7b). The distribution of species in the Atlantic Forest has been severely altered by accelerated deforestation and subsequent fragmentation effects, medium to large-scale farming activities (e.g coffee, orange, and sugar cane), and by indiscriminate urban expansion and industrialization since the beginning of the 20th Century (see Fonseca 1985; Lembi et al. 2020). Only approximately 10% of the original area of the Atlantic Forest (once covering 16% of Brazil) remains, represented by small forest patches and regenerating areas (Colombo and Joly 2010; Joly et al. 2014; Rezende et al. 2018). A similar situation can be seen in the Pantanal and the Cerrado, in which a number of endemic areas were recovered during this work. Studies have shown that there is a high potential for loss of biodiversity in these regions through deforestation due to extensive cattle farming, agricultural activities, wildfire, hunting, and unregulated tourism (Ratter et al. 1997; Durigan et al. 2007; Alho et al. 2019; Berlinck et al. 2022).
This is the first study focused on exploring the distribution of Spirostreptida in the Neotropics based on analytical methods, with six areas of endemism proposed for the 133 Brazilian Spirostreptida species. Most endemic areas fall within the Atlantic Forest biome, an extremely biodiverse Neotropical area harboring an abundance of invertebrate and vertebrate taxa. Although the southeastern region of Brazil (including the Cerrado and Atlantic Forest endemic areas) has the highest recorded Spirostreptida species richness, it also has the highest concentration of threatened species. In recent times, anthropogenic activities, such as farming practices and urban expansion, leading to an accelerated deforestation and habitat fragmentation, have greatly affected the flora and fauna of the region. The majority of Brazilian Spirostreptida, likely also true for other groups with low vagility, are either endangered or critically endangered, with the highest concentration of endangered species occurring in the Atlantic Forest. Our study demonstrates that species assemblages of Spirostreptida are largely restricted to small and medium scale areas (e.g. islands, mountain ranges, and caves) susceptible to human impacts. Moreover, these areas are severely threatened by the lack of comprehensive conservation strategies, especially those containing caves, which are continually threatened by mining and development operations. Increased taxonomic efforts coupled with in-depth exploration of biogeographic patterns may reveal detailed local patterns, such as in the Amazon and the Caatinga, which are largely unknown regarding Spirostreptida and Diplopoda as a whole.