Introduction
Terrestrial isopods (Oniscidea) are the only crustacean lineage completely adapted to the terrestrial way of life (Hornung 2011; Richardson and Araujo 2015; Taiti 2018). The group occurs in almost all kinds of terrestrial habitats, including caves (Schmalfuss 2003; Taiti 2004). Oniscidea comprises about 4,000 species distributed in more than 500 genera and 38 families (Javidkar et al. 2015, 2017; Sfenthourakis and Taiti 2015; Dimitriou et al. 2019; Campos-Filho and Taiti 2021; WoRMS 2021).
Terrestrial isopods are one of the most representative taxa in the Brazilian subterranean environments, probably due to the special environmental conditions, such as high humidity, substrate heterogeneity, and absence of specialized predators (Fernandes et al. 2016, 2019). To date, about 210 species are known from Brazil, 70 of which, belonging to the families Styloniscidae, Philosciidae, Scleropactidae, Dubioniscidae, Platyarthridae, Porcellionidae, Armadillidae, Pudeoniscidae, and Armadillidiidae, are recorded from Brazilian caves. Thirty-two taxa are considered to be troglobites (obligatory and restricted to caves), several are troglophiles (facultative cave species), and some species are possibly trogloxenes (Souza et al. 2011; Campos-Filho et al. 2014, 2015a, 2015b, 2016, 2017a, 2017b, 2018, 2019, 2020; Bastos-Pereira et al. 2017; Fernandes et al. 2018, 2019; Cardoso et al. 2020a, 2020b, 2021). The species placed into the last two categories are difficult to assign into a correct subterranean category due to the scarcity of distribution data outside caves.
Among the troglobitic representatives of the Brazilian Oniscidea, 12 species have an amphibious way of life, all in the Styloniscidae: Chaimowiczia uai Cardoso, Bastos-Pereira, Souza & Ferreira, 2021, C. tatus Cardoso, Bastos-Pereira, Souza & Ferreira, 2021, Iuiuniscus iuiuensis Souza, Ferreira & Senna, 2015, Spelunconiscus castroi Campos-Filho, Araujo & Taiti, 2014, Xangoniscus aganju Campos-Filho, Araujo & Taiti, 2014, X. ceci Cardoso, Bastos-Pereira, Souza & Ferreira, 2020, X. dagua Cardoso, Bastos-Pereira, Souza & Ferreira, 2020, X. ibiracatuensis Cardoso, Bastos-Pereira, Souza & Ferreira, 2020, X. itacarambiensis Bastos-Pereira, Souza & Ferreira, 2017, X. lundi Cardoso, Bastos-Pereira, Souza & Ferreira, 2020, X. odara Campos-Filho, Bichuette & Taiti, 2016, and X. santinhoi Cardoso, Bastos-Pereira, Souza & Ferreira, 2020.
The present work describes two new species of Xangoniscus from the Serra do Ramalho karst area, state of Bahia, both occurring in special microhabitats, namely the upper aquifers fed by infiltration of water in the limestone rock. Moreover, aspects of their ecology and natural history, as well as conservation remarks about this particular and unique fauna and the region of Serra do Ramalho are given.
Materials and methods
Collections and taxonomy
Specimens of Xangoniscus were collected by hand with the aid of tweezers and brushes. Specimens were stored in 70% and 100% ethanol. Descriptions are based on morphological characters with the use of micropreparations in Hoyer’s medium (Anderson 1954). For each new species, the diagnosis, type material, description, etymology, and remarks are given. The habitus images were taken with the stereomicroscope model Motic SMZ-168 and the Celestron Microcapture Pro. The photographs were prepared with Adobe Photoshop CC Lite (v. 14.2.1). The appendages were illustrated with the aid of a camera lucida mounted on a CH2 Olympus microscope. The final illustrations were prepared using the software GIMP (v. 2.8) according to the method proposed by Montesanto (2015, 2016).
Maps were produced highlighting the caves where both Xangoniscus species occur, as well the hydrological attributes and pressures of economic activities in the region, representing impacts to the cave fauna. The distribution map was constructed with QGIS software (v. 3.18.1) and was edited in PowerPoint Microsoft 365 (v. 2108).
The material is deposited in the scientific collection of cave fauna of the Laboratório de Estudos Subterrâneos (LES), Universidade Federal de São Carlos, São Carlos, Brazil (Curator: Maria E. Bichuette).
Ecological and behavioral study
Both populations were studied in one field trip in October 2020, during the dry-wet season transition. Specimens were sampled ad libitum (sensu Altmann 1974; Martin and Bateson 2007). In addition, direct observations of other ecological and behavior data were recorded including reproductive aspects, movement, and microhabitat preferences as well as course estimations of abundance and population density. Microhabitat data included cave zone, type of substrate, depth, water current, and physicochemical variables – pH and temperature.
To assess population parameters (density and size of the population), the individuals were counted along microhabitat inside caves, and measurements (such as length, width, and total area) of the occurrence sites were taken. The population parameters were calculated by dividing the number of individuals observed by area of the occurrence site. Photographs and short videos were taken to document the behavior of both species and the influence of the microhabitat on their distribution in the caves (see Supplementary Online Material).
Discussion
Both species described herein show the classical signs of troglomorphism (eyes absent and body depigmented), as observed for the other eight valid species of Xangoniscus, i.e., X. aganju, X. ceci, X. dagua, X. ibiracatuensis, X. itacarambiensis, X. lundi, X. odara and X. santinhoi. This could be a pattern for the entire genus, since all species described until now show these same characteristics. Morphological variability in these two characters was not observed for any species of Xangoniscus. To date, no Xangoniscus species has been recorded outside caves, in the epigean environment, which may denote an ancient isolation of this group.
Morphologically, X. lapaensis sp. nov. and X. aganju (including specimens from Gruna Chico Pernambuco and Domingão caves, see Campos-Filho et al. 2019) exhibit some level of similarities in the pereopods 5 and 6 of males, e.g., merus and carpus with fringed scales and dense field of thin setae on external margin and carpus distally depressed (see figures of X. aganju in Campos-Filho et al. 2014). The complex shape of the distal portion of the male pleopod 2 endopod is quite similar among specimens of X. aganju from Gruna do Mandiaçu cave (type locality) and Gruna Chico Pernambuco cave and X. lapaensis sp nov. (see figure 13C in Campos-Filho et al. 2014, and figure 7B in Campos-Filho et al. 2019), and specimens of X. aganju from Domingão cave and X. loboi sp. nov. shares the presence of two transverse processes (see figure 7C in Campos-Filho et al. 2019). Taking into account the geographic distribution of these species (see Fig. 1) and these morphological characteristics, it is likely that these species represent a species complex. Future phylogenetic analyses potentially will elucidate the hypotheses proposed herein.
The Serra do Ramalho region has been locally exploited historically by agriculture activities and charcoal production on a small scale. At a broader scale, mining projects and large agriculture production along the boundaries of the region pose future threats (Gallão & Bichuette, 2018) (Fig. 1C, D). To date, no effective law guarantees protection of the caves in the region. However, both Gruna Boca da Lapa and Gruna da Pingueira II caves are type-localities of endemic and probably rare troglobites, classifying these caves as maximum relevance sensu Brazilian legislation (BRASIL 2008). However, this action likely will not be sufficient, because protection is restricted to a small portion of an extensive massif. The creation of a conservation unit for the entire karst area would probably be the most effective action to ensure the preservation of the biological and speleological heritage of the Serra do Ramalho karst region.
A preliminary evaluation of the conservation status of these species was conducted following the IUCN (International Union of Conservation of Nature) classification. Despite their high population density and abundance, Xangoniscus lapaensis sp. nov. and Xangoniscus loboi sp. nov. were classified as Critically Endangered (CR) according to the criteria B2ab(iii). Both species are endemic, restricted to their type-locality and found in a specific microhabitat (travertine pools and streams formed by infiltration water). The surrounding areas of the cavities are impacted by deforestation for pastures and the native vegetation is present only at their entrances (Fig. 3A, B). Furthermore, the Gruna Boca da Lapa cave is threatened by uncontrolled tourism. These threats, combined with the impacts mentioned above for the Serra do Ramalho region, justify the conservation status proposed in this evaluation.