Distribution, conservation status and proposed measures for preservation of Radiodiscus microgastropods in Chile

Chilean Radiodiscus species

We follow the currently accepted literature in assigning eight Chilean species to the genus Radiodiscus (Stuardo & Vega, 1985; Valdovinos, 1999; Aldea, Novoa & Rosenfeld, 2019). Three of those species are endemic to Chile, namely Radiodiscus coarctatus Hylton Scott, 1979, Radiodiscus quillajicola Vargas-Almonacid, 2000 and Radiodiscus villarricensis Miquel & Barker, 2009, while the remaining five species occur in Chile and Argentina: Radiodiscus australis Hylton Scott, 1970, Radiodiscus coppingeri (Smith, 1881), Radiodiscus flammulatus Hylton Scott, 1975, Radiodiscus magellanicus (Smith, 1881) and Radiodiscus riochicoensis Crawford, 1939.

Information on the distribution and biology of these species was likewise obtained from the literature, through different sources including original descriptions, subsequent taxonomic contributions, distribution records and species checklists (Smith, 1881; Pilsbry, 1911; Crawford, 1939; Hylton Scott, 1957; Hylton Scott, 1963; Hylton Scott, 1970; Hylton Scott, 1975; Hylton Scott, 1979; Stuardo & Vega, 1985; Fonseca & Thomé, 1993; Fonseca & Thomé, 1994; Valdovinos, 1999; Vargas-Almonacid, 2000; Sielfeld, 2001; Miquel & Bellosi, 2007; Tablado & Mantinian, 2004; Miquel & Bellosi, 2007; Miquel & Barker, 2009; Miquel & Aguirre, 2011; Aldea, Novoa & Rosenfeld, 2019; Salvador et al., 2021). In addition, we also include GBIF records provided by prominent malacologists or curators of mollusks collections (Darrigran & Damborenea, 2017; Tablado & Rodríguez, 2021; Goud, van der Bijl & Creuwels, 2022), as well as Hylton Scott (1970) and Hylton Scott (1979) (see Table S1 for links to these sources).

Six further species of micromollusks originally described by Philippi (1855) under the genus Helix Linnaeus, 1758 are considered of uncertain affinities (Stuardo & Vega, 1985) but have been recently listed as species of Radiodiscus in platforms such as GBIF (2021) and MolluscaBase (2021) without any explanation for the decision. Therefore, those six “Helix” species were not included in the present study.

Conservation status

Historical localities recovered from the literature for each species of Radiodiscus are available in Table S1. Those localities lacking geographic coordinates were georeferenced via the radio-point method. This procedure consists in establishing a central point within the area reported in the respective publication and to define a circumference around it that includes the most probable collection site and its associated uncertainty (Wieczorek, Guo & Hijmans, 2004; Escobar et al., 2016). Geographic coordinates and radius of uncertainty were obtained using the software Google Earth (v.7.3.3.7786; Google Inc., Mountain View, CA, USA).

The IUCN categorizes species according to five criteria: Criterion A refers to population size reduction, Criterion B to geographic range, Criterion C to small population size and decline, Criterion D to very small or restricted population, and Criterion E to quantitative analysis of the probability of extinction. We assessed the conservation status of the Chilean Radiodiscus species using Criterion B because no information is available for the application of criteria A, C, and E in this group. Criterion B considers geographic range of species, involving subcriterion B1, based on the extent of occurrence (EOO), and subcriterion B2, based on the area of occupancy (AOO). Basically, the EOO is the area covered by the polygon formed by a union line that encloses all occurrences of a species while the AOO is the sum of the estimated areas around each occurrence. In the latter case, a 2 km² grid cell was used (Bland et al., 2016; IUCN, 2019). To calculate the parameters EOO and AOO and to automatically obtain a preliminary conservation category, the geographic coordinates of each species were introduced into the GeoCAT program (Bachman et al., 2011). We also apply sub-criterion D2 (Criterion D), for species with few locations (≤ 5), an AOO ¡ 20 km² and at least one plausible threat. If a species meets these conditions it must be listed as Vulnerable: D2. The conservation categories that can be obtained using this tool are Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN) and Critically Endangered (CR).

To assess the conservation status based on NatureServe’s standards (Faber-Langendoen et al., 2012; Master et al., 2012) we used the Conservation Rank Calculator tool (NatureServe, 2021), which allows entering the data of the species to obtain a conservation category based on the range extent (equivalent to EOO), area of occupancy (AOO), numbers of occurrences, ecological viability, population trends and threats (Table 1). NatureServe also allows the researcher to specify the geographic level of the conservation assessment: Global (G), National (N), and Subnational (S) (Faber-Langendoen et al., 2012; Master et al., 2012). Under this methodology, the species may be assigned to one of the five categories: Critically Imperiled (G1/N1/S1), Imperiled (G2/N2/S2), Vulnerable (G3/N3/S3), Apparently Secure (G4/N4/S4) and Secure (G5/N5/S5). We determined ecological viability in the sense of habitat quality using satellite images on Google Earth exploring whether the occurrence records and surrounding areas of Radiodiscus species still have natural coverage thus providing a suitable environment to live (“Good” habitat in Table S1). The threats facing species were obtained merging species occurrence records with road, hydrographic and urban development vector layers available in the Library of the National Congress of Chile (https://www.bcn.cl/siit/mapas_vectoriales), which were analyzed in QGIS v.3.22.7 software (QGIS Development Team, 2021), as well as information obtained from the literature, government organizations and the media. Operationally, in the Conservation Rank Calculator we first enter the threats identified previously in each species assigning the highest level of threat in the “Threats Assessment Worksheet” to then record in the “Calculator Form Worksheet” the data available per taxon regarding EOO, AOO, occurrence records, ecological viability and threats. The present study was carried out at the national level (N), without considering population trends due to lack of information.

Mapping of occurrences over protected areas

The Chilean National System of Protected Areas (SNASPE, “Sistema Nacional de Áreas Silvestres Protegidas del Estado”) has established 118 protected areas to preserve the country’s natural heritage (Root-Bernstein et al., 2013; Subsecretaría de Turismo, 2015). These areas include National Parks, National Reserves, Biosphere Reserves, Natural Monuments, Ramsar Sites, National Protected Goods, Marine Reserves and Coastal Marine Protected Areas. The total coverage of those areas is about 20% of the national territory (Root-Bernstein et al., 2013; Subsecretaría de Turismo, 2015). To determine if any of the species occurs within any of the protected areas, we built maps in QGIS previously entering vector layers of the country’s regions and protected areas available at the Library of National Congress of Chile (https://www.bcn.cl/siit/mapas_vectoriales). At the same time, the EOO, AOO and occurrence records of the species were downloaded from GeoCAT in KML format to be used in QGIS.

Ecological niche modeling

A total of 19 bioclimatic variables (Fick & Hijmans, 2017) were downloaded from the WorldClim database version 2.0 (http://www.worldclim.org) and used in conjunction with environmental variables obtained from the same platform (solar radiation, evaporation, elevation, wind) [resolution of ∼1 km²(30 s)]. Each variable was merged with a vector geographic layer of the Chilean territory available in the Library of the National Congress of Chile (https://www.bcn.cl/siit/mapas_vectoriales) in a new raster variable (.ASCII) using ArcGIS v.10.8 software (Esri, Redlands, CA, USA). To estimate potential species distribution, we uploaded species occurrence records and the complete set of variables in the Maxent v.3.4.4 software (Phillips, Dudík & Schapire, 2004) to run four models per species computed using the logistic option. Model 1 was performed including all climatic and environmental variables and default settings. Model 2 included all variables with a setting of 25% of the occurrences for model testing. Model 3 included only the variables that most contributed to the model and that were obtained in Model 2, with default settings. Model 4 was the Model 3 but setting 25% for model testing. The performance of the model was validated with the AUC (area under the curve) based on the Receiver Operating Characteristic (ROC), which estimates values from 0.5 to 1.0, with values above 0.8 depicting a good fit of the model (Loo, Mac Nally & Lake, 2007). The importance of the variables that best explained the presence of Radiodiscus species was evaluated with the Jackknife test, which identifies the variable with highest gain regarding the other variables. The potential species distribution map resulting from the selected model was converted from ASCII to raster in ArcGIS for visualization.

Recommended conservation measures

To date, there are no studies addressing the genetic diversity of any of the species of Radiodiscus in Chile, so it is still unknown whether there is gene flow between populations of more widespread species. Even their basic biology, such as life cycle, reproduction, development, vagility and population sizes, remains to be investigated. Considering these gaps in knowledge, and according to the degree of risk reported here, our first recommendation is to carry out basic studies on the biology of these species, prioritizing the most threatened ones.

Several in situ and ex situ conservation measures have been proposed in conservation biology (Berkmüller & Savasdiasara, 1981; Bloxam, Tonge & Horton, 1984; Tonge & Bloxam, 1991; CBD, 1992; Pearce-Kelly et al., 1997; Balmford, Leader-Williams & Green, 1995; Mace, Pearce-Kelly & Clarke, 1998; IUCN, 2002; Hadfield, Holland & Olival, 2004; Anonymous, 2005; Kadis, Thanos & Laguna Lumbreras, 2013; Trias-Blasi, Gücel & Özden, 2017). Article 8 of the CBD (1992) proposes 13 in situ conservation measures, including the establishment of protected areas, along with its management and protection, to promote the preservation of ecosystems and natural habitats, as well as to prevent the introduction of (or facilitate control or eradication) of exotic species. In accordance with these recommendations, ideally, we propose to enlarge the area of some national parks, create reserves, micro-reserves and environmental interpretive trails to preserve species of Radiodiscus in Chile (Berkmüller & Savasdiasara, 1981; Balmford, Leader-Williams & Green, 1995; Laguna et al., 2004). Although the beneficial results of interpretive trails have been questioned (Navrátil, Knotek & Pícha, 2015), the creation of this type of infrastructure remains common in conservation biology as it focuses on the education of the public rather than in all-out preservation of the area and its biota (Berkmüller & Savasdiasara, 1981; Munro, Morrison-Saunders & Hughes, 2008). On the other hand, micro-reserves have proven effective in conservation, where small plots of land of a few hectares are established (Kadis, Thanos & Laguna Lumbreras, 2013; Trias-Blasi, Gücel & Özden, 2017). Micro-reserves are easier to create and can benefit the area and its species, although they need to be established as a network of reserves to succeed (Lumbreras, 2001). Their success for plant species (Laguna et al., 2016) might be a good sign for micromollusks with supposed reduced mobility.

Article 9 of the CBD (1992) also proposes five ex situ measures that may be implemented for species conservation. Some ex situ conservation efforts have been developed through captive breeding programs to preserve tree snails of the families Achatinellidae and Partulidae (Bloxam, Tonge & Horton, 1984; Tonge & Bloxam, 1991; Pearce-Kelly et al., 1997; Mace, Pearce-Kelly & Clarke, 1998; Hadfield, Holland & Olival, 2004), endemic to Hawaii and islands of the south-western tropical Pacific Ocean, respectively, which face extinction. However, up to our knowledge there are no reports of successful breeding of minute Charopidae snails such as Radiodiscus spp., so the feasibility of this approach is uncertain.

Some in situ and ex situ conservation measures are proposed below for Chilean Radiodiscus species. The benefits and drawbacks of each approach must be assessed and weighted against costs and immediate and potential benefits. Realistically, not all of these measures will be feasible in all concerned areas in Chile and, as such, they should be assessed on a case-by-case basis alongside policy makers.

Radiodiscus australis (Fig. 1A) presents only two occurrences in Chile, none of them within a protected area. It is exposed to a high level of nature and sports tourism, and forestry activities (exploitation of native forests for wood, firewood and paper and livestock disturbance) (Magallanes, 2012; Arredondo et al., 2019). Furthermore, the area is inhabited by beavers (Castor canadensis Kuhl, 1820), an invasive species that drastically modifies the habitat (Graells, Corcoran & Aravena, 2015), although its net impact on the terrestrial snail fauna remains unstudied. Moreover, the Brunswik Peninsula has coal reservoirs (Magallanes, 2012), the exploitation of which could become a threat to the species in the near future. Today, ex situ conservation actions such as captive breeding should be trialed as a priority to preserve the species. We also recommend the implementation of in situ conservation actions such as environmental interpretive trails and beaver eradication where R. australis populations occur. The implementation of micro-reserves would also be an appropriate conservation measure.

Radiodiscus coarctatus (Fig. 1B) faces threats associated to tsunamis, tourism, artisanal fishing and soil erosion due to heavy rainfalls and strong winds (DAPMA, 2009), although adverse weather conditions in turn reduce tourism (CONAF, 2021). Although the species was described from Caleta Nantuel, Vidal Gormaz Island, within the Kawésqar National Park (Fig. 1B), we recommend the implementation of an environmental interpretation trail and implement ex situ conservation programs as mentioned above.

Radiodiscus coppingeri (Fig. 1C) faces threats in many fronts, such as tourism, soil erosion due to rainfall (storms), activities associated to artisanal fishing (DAPMA, 2009), solid contamination caused by the influx of tourists (El Heraldo Austral, 2019), illegal logging of native forest (Magallanes, 2012; Mardones, 2020), risk of forest fires (CONAF, 2020), and change in land use due to livestock (Arredondo et al., 2019), as well as the presence of beavers in austral Patagonia (Graells, Corcoran & Aravena, 2015; GEF, 2019). In addition, several populations are close to urban areas, volcanoes, hydrocarbon mines (SONAMI, 2021) and coal reserves (Martinic, 2004; Magallanes, 2012). Even though R. coppingeri is the species with the highest number of occurrences, the conservation category resulting from this study was Endangered (EN) according to IUCN criteria (AOO) and Imperiled (N2) under NatureServe criteria (Table 2). We recommend enlarging the Bernardo O’Higgins National Park since there are five occurrences located on the eastern margin of the Serrano River. We also recommend the creation of environmental interpretive trails in different localities where this species occurs, as well as beaver eradication.

Radiodiscus flammulatus (Fig. 1D) is threatened by tourism and recreational activity, such as camping, that causes solid contamination (El Heraldo Austral, 2019; Robles, 2021). On the other hand, the Laguna del Laja National Park borders on infrastructure associated with the El Toro hydroelectric plant, causing droughts in the area (Arnaboldi, 2016; Díaz, Jaque & Ojeda, 2018). Because R. flammulatus is Endangered (EN) or Imperiled (N2) according to our assessment, we suggest enlarging the Alerce Andino National Park since there is one occurrence approximately 0.1 km outside the park towards the V-657 highway. Similarly, we also suggest enlarging the Bernardo O’Higgins National Park (as for R. coppingeri above) because there is another occurrence located approximately 1.6 km from the park towards Lake Brush. We also recommend the creation of environmental interpretive trails since some of the threats mentioned above affect even the interior of protected areas.

Radiodiscus magellanicus (Fig. 1E) faces various threats such as monoculture forestry and exploitation of native trees (Magallanes, 2012), livestock activities for consumption and export (Arredondo et al., 2019), heavy rainfall (storms), high tourist activity and presence of the invasive beaver (Graells, Corcoran & Aravena, 2015; GEF, 2019). In addition, several populations of the species are located near volcanoes, highways/roads, urban areas and hydrocarbon mines. We recommend the creation of environmental interpretive trails in addition to enlarging the Bernardo O’Higgins National Park (as for R. coppingeri and R. flammulatus above), since there is one occurrence approximately 1 km from the park towards Lake Brush. We also recommend beaver eradication.

Radiodiscus quillajicola (Fig. 1F) inhabits a single locality near a busy highway with potential for landslides (Cooperativa, 2016; Arenas, 2017). In addition, this locality is not a protected area and is close to the Laguna del Maule volcanic complex, which currently has a yellow alert level (SERNAGEOMIN, 2021). Thus, the severity of the threats to this species is high. The trialing and implementation of ex situ conservation actions such as captive breeding should be considered a priority to preserve the species. We also recommend the creation of a micro-reserve to protect both the species and its habitat, in addition to implementing an environmental interpretation trail and surveying the neighboring area for eventual occurrences of the species.

Radiodiscus riochicoensis (Fig. 1G) faces serious threats such as the presence of the invasive beaver (Graells, Corcoran & Aravena, 2015; GEF, 2019), forestry activities for the exploitation of native forests (Magallanes, 2012), livestock activity focused on export (Arredondo et al., 2019), activities associated with artisanal fishing (DAPMA, 2009), pollution (El Heraldo Austral, 2019), risk of forest fires (Vidal et al., 2015), heavy rainfall (storms), and a high degree of tourism and recreational activities. In addition, some populations are located close to volcanoes, highways, urban areas, coal reservoirs (Magallanes, 2012) and hydrocarbon mines (SONAMI, 2021). We recommend the creation of environmental interpretive trails and micro-reserves for the protection of the species, as well as beaver eradication.

The three localities where R. villarricensis inhabits (Fig. 1H) face a large amount of tourism and recreational activities (Subsecretaría de Turismo, 2017; Morales Flores, 2019) and the risk of forest fires (Villavicencio, 2015; Morales Flores, 2019; Enríquez, 2021). In addition, two of the three occurrences are close to urban areas and one to volcanoes. We recommend the trialing and implementation of ex situ conservation programs, the creation of environmental interpretive trails, and the creation of a micro-reserve in Fundo El Manzano, Bío-Bío Region. The feasibility of creating a national reserve in Cerro Caracol, Concepción city, should also be taken into consideration.

Identifying threatened species is one of the main tasks of conservation biology, following with an assessment of the threats and the development of strategies to remediate the situation (Purvis et al., 2000; Barbini et al., 2020). In the present study, we proposed in situ and ex situ conservation measures to preserve eight species of Radiodiscus in Chile, most of which are highly threatened. However, although these types of actions are not exempt from difficulties, such as the cost of the land, its management, territorial custody, associated facilities, staff and the type of feed and appropriate abiotic environmental conditions in the case of artificial rearing systems (Hadfield, Holland & Olival, 2004; O’Rorke et al., 2016; Kadis, Thanos & Laguna Lumbreras, 2013; Laguna et al., 2004; Carranza et al., 2020), they have been rather promising and therefore applicable to preserve species, including small snails.