Updated list of Collembola species currently recorded from South Africa

Abstract Understanding the abundance and richness of species is one of the most fundamental steps in effecting their conservation. Despite global recognition of the significance of the below-ground component of diversity for ecosystem functioning, the soil remains a poorly studied terrestrial ecosystem. In South Africa, knowledge is increasing for a variety of soil faunal groups, but many still remain poorly understood. We have started to address this gap in the knowledge of South African soil biodiversity by focusing on the Collembola in an integrated project that encompasses systematics, barcoding and ecological assessments. Here we provide an updated list of the Collembola species from South Africa. A total of 124 species from 61 genera and 17 families has been recorded, of which 75 are considered endemic, 24 widespread, and 25 introduced. This total number of species excludes the 36 species we consider to be dubious. From the published data, Collembola species richness is high compared to other African countries, but low compared to European countries. This is largely a consequence of poor sampling in the African region, as our discovery of many new species in South Africa demonstrates. Our analyses also show that much ongoing work will be required before a reasonably comprehensive and spatially explicit picture of South Africa’s springtail fauna can be provided, which may well exceed 1000 species. Such work will be necessary to help South Africa meet its commitments to biodiversity conservation, especially in the context of the 2020 Aichi targets of the Convention on Biological Diversity.


Introduction
The documentation of biodiversity is an essential first step for its conservation. A major barrier to so doing for invertebrates is a lack of taxonomic information on various groups. This taxonomic impediment and its implications for biodiversity studies have been widely discussed (Godfray 2002, Samper 2004. Despite these challenges, taxonomic knowledge continues to increase globally (Nilsson-Örtman and Nilsson 2010, Joppa et al. 2011, Platnick 2014, van Noort 2014. Nonetheless, given rapid environmental change and its effects on biodiversity (Butchart et al. 2010), it is unclear what the rate of extinction is for many groups (Pimm et al. 2010, Costello et al. 2013, complicating conservation efforts and assessments of their efficacy, thus underscoring the urgency to further document global biodiversity (Dirzo andRaven 2003, Bacher 2012).
This situation is as true for southern Africa as it is elsewhere. Knowledge of the South African fauna is increasing rapidly, especially in the case of a wide range of invertebrate groups (Foord et al. 2002, Robertson 2000, Parr et al. 2003, Haddad and Dippenaar-Schoeman 2006, Hlavac 2007, Rousse and van Noort 2013. Nonetheless, many groups still remain relatively poorly studied, especially soil-dwelling taxa, which are essential for both above-and below-ground ecosystem functioning (Wardle et al. 2004, Hugo-Coetzee and Avenant 2011, Janion et al. 2011a). At the same time, considerable impacts on biodiversity continue to be documented as a consequence of habitat modification for agriculture and urban development, biological invasions, pollution, and climate change (Erasmus et al. 2002, Rouget et al. 2003, Biggs et al. 2008, Chown 2010, Pryke and Samways 2010, Huntley and Barnard 2012, Liu et al. 2012. In consequence, much need exists for documenting and understanding biodiversity and the processes underlying its variation across a wide range of groups, and especially the soil fauna.
Collembola are amongst the most widespread and abundant soil arthropods (Petersen andLuxton 1982, Hopkin 1997). Despite their obvious significance in soil systems, their utility as bioindicators (Lawrence 1953, Hopkin 1997, van Straalen 1998, their significance in the alien species faunas of many areas (Roques et al. 2009, Terauds et al. 2011, and the current growth in both morphological (Deharveng 2004) and molecular (Hogg andHebert 2004, Rougerie et al. 2009) means to assess their diversity, they remain poorly known in South Africa. Indeed, by comparison with other regions of the world (Deharveng 2004), and other invertebrate taxa in the country (Scholtz and Chown 1995, Robertson 2000, Foord et al. 2011, Dippenaar-Schoeman 2014, knowledge of the group can be considered scanty. The first attempt to collate all taxonomic information on the Collembola of South Africa was undertaken by Paclt (1959), listing ca. 65 species. Subsequently, an unpublished list entitled "Aquatic Collembola of South Africa" was made available online (P. Greenslade, no date), while Thibaud (2013) listed most publications until 2013. To date there are 38 publications on Collembola recorded or described from South Africa, the earliest by Börner (1908). Most notably, comprehensive descriptions were made by Yosii (1959), Paclt (1959Paclt ( , 1964Paclt ( , 1965Paclt ( , 1967, Coates (1968aCoates ( , 1968bCoates ( , 1969, Weiner and Najt (1991, 1998, and later Barra (1994, 1995, Barra and Weiner 2009). However, little other work has been done and the current list of species for the country is clearly an underestimate, with an incomplete understanding of which species might be introduced and thus might have substantial impacts, despite the fact that such impacts have been suggested for the country (Annecke andMoran 1982, Liu et al. 2012).
To address this substantial gap in the knowledge of soil biodiversity, a collaborative project was established in 2008 (Janion et al. 2011a, Bengtsson et al. 2011. Besides large-scale sampling and systematic assessments, which have resulted in new discoveries and species descriptions (Janion et al. 2011b, Potapov et al. 2011, 2013, a major component of the project has comprised the compilation of all currently available information on Collembola recorded from South Africa. Here we present this compilation as an updated checklist. It will provide a starting point for understanding the diversity of this group, as has been done for other geopolitical regions (e.g. Culik and Zeppelini 2003, and will assist South Africa to meet its obligations under the Convention on Biological Diversity (see for example Aichi Target 9 on identifying invasive alien species, and Aichi Target 17 on a national biodiversity strategy, http://www.cbd.int/sp/targets).

Methods
All publications on Collembola species described or recorded from South Africa were collated from Salmon (1964) and Thibaud (2013). The list was checked and completed using the website "Checklist of the Collembola of the World" (Bellinger et al. 2014), the bi-annual bibliographical lists issued by the Museum National d'Histoire Naturelle (Paris, France), Zoological Record, Web of Science TM (full date range of 1900 to 2014), and genus or species revisions from taxonomic journals sourced from the references identified using the original search methods. Nomenclature follows Bellinger et al. (2014), as it may have changed for certain taxonomic groups since the original description of the species. All published papers and webpages were examined and the following information was recorded when available: collection details including date, collector, province, place, nearest town, habitat type, and collection method, type locality and accession number if given. Only species with full species names were included in the species list of Table 2, thus excluding morphospecies identified to genus or to suspected species (e.g. Seira sp. or Isotomurus cf. maculatus). However, every record from the literature is listed in the Supplementary material (Suppl. material 1). The species were assigned a South African province from the locality recorded. From these points a species richness map was produced in ArcMap V10.2 (ESRI 2014).
The species were also divided into the following categories based on their distribution: 1) endemic if they were described from South Africa and have not been recorded elsewhere, 2) introduced if there is evidence from the literature that the species was introduced from another place, 3) widespread if the species is also present outside of South Africa but its origin is unknown, thus not considered introduced, or 4) dubious, when the species name given in the literature is considered a misidentification based on current taxonomic knowledge or if subsequent taxonomic work suggested this is the case (see Suppl. material 1).
To make an estimate of expected species richness, we used data collected from extensive sampling in the Western Cape Province of South Africa, which has been the main focus of much work on the group. The dataset comprises a total of 217 samples we obtained using several sampling techniques (see below) in as many localities and different microhabitats as possible throughout the Western Cape, including Afromontane forest, different fynbos vegetation types (see Mucina and Rutherford 2006), intertidal habitats, caves, and disturbed areas such as gardens and agricultural areas. Leaf litter, moss, rotten wood and soil samples were taken at different sampling sites over the duration of the project (2008)(2009)(2010)(2011)(2012), and occasionally sieving and pitfall traps were also used. Typically, samples were extracted using a Berlese-Tullgren approach for five to seven days, or until dry (Berlese 1905, Tullgren 1918, Hopkin 1997). In addition, active searching was done in the field. Riparian soil was washed for water-dependent species, which were collected with a fine brush on the surface of water. Fine sand such as sea sand was washed in the laboratory and animals were also collected with a brush. Vegetation such as branches from bushes, fynbos shrubs, and grasses was beaten over a tray and animals were collected by means of an aspirator. All samples are stored in 96-99% ethanol at the Centre for Invasion Biology (C•I•B) Stellenbosch, or the Museum National d'Histoire Naturelle (MNHN) Paris. As identifications and species descriptions are still ongoing, we only used confirmed morphospecies for the purpose of calculating the number of species expected for the Western Cape.
Sampled-based rarefaction curves were plotted to estimate the number of species for the Western Cape, using Chao1 and Jacknife 2 in EstimateS V8.2.0 (Colwell 2009). Jacknife 2 does not require data to be normally distributed and provides conservative, but accurate estimates (Magurran 2004). Sampling is considered adequate when the rarefaction curves and the estimators converge at the highest observed values (Longino et al. 2002).

Results
According to the literature, a total of 160 species from 61 genera and 17 families have been recorded from South Africa (Table 1), with a relatively steady increase in descriptions since the first records in the early 1900s (Fig. 1). Of the recorded species, 36 are considered dubious, most of them misidentified records from Paclt (1959Paclt ( , 1967. Of the other species, 75 are endemic, 25 are thought to be alien species introduced to the country by human activity, and 24 have a widespread distribution, at least so far as current sampling indicates ( Table 2). The majority of species have been recorded from the Western Cape (67 species), Kwazulu-Natal (46 species) and the Eastern Cape (20 species) (Fig. 2). Records from the other provinces are sparse (1-10 species), with the North West Province and Limpopo having the lowest recorded richness (three and one species, respectively). Although many authors did not indicate the habitat type where collections took place (Supplementary Material Suppl. material 1), the majority mentioned were from sites that are within the forest biome (see Mucina and Rutherford 2006 for full details of South Africa's biomes and vegetation types). However, other vegetation types mentioned include those of the grassland biome and disturbed areas such as gardens, orchards and plantations. The sample-based species rarefaction curve for the Western Cape did not reach an asymptote (Fig. 3). The two richness estimators (Jacknife2: 348 species, Chao1 with 95% Confidence Intervals: 323, lower CI: 270,upper CI: 416) suggest that at least 6-7 times more than the number of species currently recorded from the literature will be found in the province, given the steep slope of the non-asymptotic curve. Table 2. Collembola species recorded from South Africa, with "Current species name" as confirmed name (Bellinger et al. 2014), and "Name published in source" as name used in the original source when different from current species name. Abbreviations   Womersley, 1928in Womersley 1934 Hypogastrura (Hypogastrura) purpurescens (Lubbock, 1868) in Paclt 1959Paclt , 1967 The species can be considered as introduced from Northern hemisphere, as has recently been confirmed for Australia

D Soil and vegetation
The numerous records of this species by Paclt are all dubious, and concern various endemic species of the genus. S. squamoornata is today considered to be limited to the Palaearctic region. Coates, 1968Coates 1968, 1970 WC E
A revision of these tropical Sphaeridia is clearly needed.

KZN D
The South African records of this sub-Antarctic species need confirmation.
Widely distributed in the southern hemisphere and in tropical Asia.  (Börner, 1907) Africa and Argentina.
This species is only known from Japan.
Other species exist in Madagascar, Sumatra, Thailand and Congo. The South African species is probably new (Betsch 1980).

Sminthurus viridis
(Linnaeus, 1758) Lawrence 1953, Paclt 1959 WC I On vegetation Mainly holarctic species, thought to have been introduced from Europe (via Australia) as eggs in soil through the importation of clover seed (Wallace 1968, Wallace andWalters 1974).

Figure 1.
The cumulative number of Collembola species described from South Africa. The three major increases in described species are indicated by the author names (Womersley, Coates and Barra).

Discussion
The number of Collembola species recorded for South Africa is low compared to wellstudied regions such as Europe (Deharveng 2007), but is the highest of all African countries south of Sahara (Thibaud 2013). Low sampling intensity in Africa seems to be the main reason for this pattern. Based on new records and species discovered during recent systematic sampling in the Western Cape Province alone (Janion et al. 2011a, b, Potapov et al. 2011, Liu et al. 2012, Janion et al. 2013, it is clear that many species remain to be recorded and described for this province. Given low richness documented elsewhere in South Africa the same situation is likely to be the case both there and in other African countries. The spatial distribution of species richness records also suggests that incomplete sampling coverage lies at the heart of the current diversity patterns. Most records to date have come from those provinces where taxonomists were either based or hosted such as in Cape Town of the Western Cape Province (Womersley 1934, Paclt 1959, Yosii 1959, and in Pretoria of the Gauteng Province (Coates 1969), reflecting a recurrent bias in geographic patterns of diversity of poorly known groups (Deharveng et al. 2000). Although Collembola do generally prefer moist environments (Hopkin 1997), which may mean lower diversity in arid provinces such as the Northern Cape and North-West Provinces (see Mucina and Rutherford 2006), low species richness in provinces such as Limpopo and Kwazulu-Natal is at odds with most other groups in the country (see e.g. Davis 1997 for dung beetles, Erasmus et al. 2000for antlions, Foord et al. 2002for spiders, Evans et al. 2006 for amphibians and birds, Schoeman and Foord 2012 for ants). The only exception to the poor knowledge of the fauna is for the sub-Antarctic Prince Edward Island group (consisting of Marion Island and the smaller Prince Edward Island), which is geopolitically a part of South Africa, and for which the fauna has been thoroughly investigated (Table 3, Gabriel et al. 2001, Hugo et al. 2006, Chown and Froneman 2008. Such a general situation of poor knowledge is typical for the Collembola in many parts of the world (e.g. Cicconardi et al. 2013), and will hamper efforts both to conserve this diversity (Cardoso et al. 2011) and to understand which components of it are non-indigenous and may be having impacts on the indigenous fauna (see discussion in Roques et al. 2009).
With the caveat in mind of undersampling, both in many parts of Africa and country-wide, it is worth considering what the current information on species in the country suggests. It appears that endemicity is likely to be high (currently 65%). This value is similar to that found for other invertebrate groups and plants in South Africa, with an extraordinary high number of endemic species found in the south-western Cape (see Colville et al. 2002, Goldblatt and Manning 2002, Herbert and Kilburn 2004, Rebelo et al. 2006, Pryke and Samways 2010. Endemicity is expected to increase with local sampling, but will likely decline if sampling is undertaken in neighbouring countries where information on the group is similarly low (e.g. Namibia, see Thibaud and Massoud 1988). Currently, sampling in the southern part of Africa mostly concerns sites within South Africa, generating a rapid increase in species richness and endemicity, as many additional endemic species have been obtained from samples as little as a few kilometres from already well sampled areas (Janion-Scheepers, Bedos and Deharveng unpublished results).
Currently, six genera are thought to be endemic to South Africa: Najtafrica Barra, 2002 (one species, Pseudachorutinae), Probrachystomellides Weiner & Najt, 1991 (one species, Brachystomellidae), Capbrya Barra, 1999 (two species, Entomobryidae), Lepidokrugeria Coates, 1969 (one species, Lepidocyrtinae), Neophorella Womersley, 1934 (one species, Tomoceridae) and Tritosminthurus Snider, 1988 (one species, Bourletiellidae). Neophorella dubia was described from a single specimen by Womersley (1934) and is the only endemic species of the family Tomoceridae to occur in South Africa.  Börner, 1902Deharveng (1981 S ENTOMOBRYOMORPHA Isotomidae Cryptopygus antarcticus travei Deharveng, 1981Deharveng (1981 E Cryptopygus dubius Deharveng, 1981 Deharveng ( Salmon, 1964in Deharveng (1981 Katianna sp. Chown and Froneman (2008) E Paclt (1959) mentioned that besides the single holotype specimen, this species was not found again and he synonymised it with the Paronellidae Dicranocentruga nigromaculata (Schött, 1903). Ireson and Greenslade (1990) re-examined the type specimen and re-assigned the species to Tomoceridae, stressing however its similarity with Isotomidae (Skaife 1954). In spite of intensive sampling in its type locality of Table Mountain (Janion-Scheepers, Bedos and Deharveng unpublished results), the species was not retrieved in any of our samples, and is considered here as a species inquirenda. The current information also suggests that approximately 20% of the Collembola species found in South Africa may have been introduced by humans to the region and should therefore be considered alien (see Pyšek et al. 2004 for terminology). Understanding what the proportion of introduced species in the fauna actually is will depend on additional comprehensive sampling, and on further consideration of species currently though to be alien. Thus, several species resembling well-known European taxa had previously been mistakenly assigned to these taxa. For example, Seira squamoornata, which was originally described from the Ukraine, was thought to be a common polymorphic species in South Africa after Paclt (1959). However, Yosii (1959) did not even include this species in his list, while Coates (1968b) found that specimens labelled as one species (S. squamoornata) by Paclt (1959), could actually be identified as several endemic species described by Yosii (1959) or Coates (1968b), and concluded that this European species does not occur in South Africa. Indeed, to date 25 indigenous species of Seira have been described from South Africa (Yosii 1959, Coates 1968b, and the richness of the genus is likely much larger. Nonetheless, that several alien species are present, especially of European origin, is not surprising given the close historical links between South Africa and Europe (Giliomee and Mbenga 2007). Most of the invasive species were collected in disturbed environments, in gardens or close to human settlements (Supplementary Material Suppl. material 1) bearing out findings for a range of other groups that disturbance may favour alien species establishment (Chytrý et al. 2005, MacDougall and Turkington 2005, Richardson and Pyšek 2006. Perhaps the best known of the alien species is Sminthurus viridis, also known as the Lucerne flea (Wallace 1964, Wallace andWalters 1974), which received considerable attention in South Africa during the late 1960s due to its pest status. It is thought to have arrived from Australia as eggs in soil through the importation of clover seed (Walters 1968, Wallace andWalters 1974). It was first collected in 1951 near Somerset West and by 1959 over 50 000 hectares of Lucerne were infested (Wallace and Walters 1974). The problem now appears largely to have been resolved, although the species is still listed as a pest of Lucerne (Annecke and Moran 1982).
In conclusion, based on published knowledge only, the Collembola species richness of South Africa is high compared with other African countries (Thibaud 2013), but low compared with non-African countries (Deharveng 2007) and with the richness of other invertebrate groups in the South African region (Scholtz and Chown 1995). This is likely due to undersampling, as recent discoveries (e.g. Janion et al. 2011b, Potapov et al. 2011, 2013 have indicated. Owing to a recent, large and comprehensive ecological and systematic study, accompanied by DNA Barcoding (Porco et al. 2012) largely focused on the country's Western Cape Province (Bengtsson et al. 2010, Janion et al. 2011a, Liu et al. 2012), a substantial increase in the number of species is expected. With 67 species recognised for the Western Cape from the recorded literature, the richness estimates indicating at least 6-7 times that number being present, and based on experience in other undersampled countries such as Thailand (Bedos 1994), we expect that species richness for the country will exceed 1000. Improvement of systematic knowledge through studies such as these, and improvements in ecological understanding of the impacts of both landscape change and invasive species on the springtail fauna (e.g. Gabriel et al. 2001, Liu et al. 2012, will help South Africa meet its commitments to biodiversity conservation especially as set out in the 2020 Aichi Biodiversity Targets.