Globally invariant metabolism but density-diversity mismatch in springtails.

Soil life supports the functioning and biodiversity of terrestrial ecosystems. Springtails (Collembola) are among the most abundant soil arthropods regulating soil fertility and flow of energy through above- and belowground food webs. However, the global distribution of springtail diversity and density, and how these relate to energy fluxes remains unknown. Here, using a global dataset representing 2470 sites, we estimate the total soil springtail biomass at 27.5 megatons carbon, which is threefold higher than wild terrestrial vertebrates, and record peak densities up to 2 million individuals per square meter in the tundra. Despite a 20-fold biomass difference between the tundra and the tropics, springtail energy use (community metabolism) remains similar across the latitudinal gradient, owing to the changes in temperature with latitude. Neither springtail density nor community metabolism is predicted by local species richness, which is high in the tropics, but comparably high in some temperate forests and even tundra. Changes in springtail activity may emerge from latitudinal gradients in temperature, predation and resource limitation in soil communities. Contrasting relationships of biomass, diversity and activity of springtail communities with temperature suggest that climate warming will alter fundamental soil biodiversity metrics in different directions, potentially restructuring terrestrial food webs and affecting soil functioning.

Indigenous and introduced Collembola differ in desiccation resistance but not its plasticity in response to temperature.

Biological invasions have significant ecological and economic impacts. Much attention is therefore focussed on predicting establishment and invasion success. Trait-based approaches are showing much promise, but are mostly restricted to investigations of plants. Although the application of these approaches to animals is growing rapidly, it is rare for arthropods and restricted mostly to investigations of thermal tolerance. Here we study the extent to which desiccation tolerance and its phenotypic plasticity differ between introduced (nine species) and indigenous (seven species) Collembola, specifically testing predictions of the 'ideal weed' and 'phenotypic plasticity' hypotheses of invasion biology. We do so on the F2 generation of adults in a full factorial design across two temperatures, to elicit desiccation responses, for the phenotypic plasticity trials. We also determine whether basal desiccation resistance responds to thermal laboratory natural selection. We first show experimentally that acclimation to different temperatures elicits changes to cuticular structure and function that are typically associated with water balance, justifying our experimental approach. Our main findings reveal that basal desiccation resistance differs, on average, between the indigenous and introduced species, but that this difference is weaker at higher temperatures, and is driven by particular taxa, as revealed by phylogenetic generalised least squares approaches. By contrast, the extent or form of phenotypic plasticity does not differ between the two groups, with a 'hotter is better' response being most common. Beneficial acclimation is characteristic of only a single species. Laboratory natural selection had little influence on desiccation resistance over 8-12 generations, suggesting that environmental filtering rather than adaptation to new environments may be an important factor influencing Collembola invasions.

Now you see me, now you don't: verifying the absence of alien invasive yellow crazy ant Anoplolepis gracilipes in South Africa.

Anoplolepis gracilipes is an invasive species that is a major threat to native ecosystems worldwide. It has been listed as one of the top 100 worst invasive species in the world and is well known for its negative impact on native arthropods and some vertebrates. This study aimed to confirm the presence or absence of A. gracilipes in some major South African harbours. We did so by surveying four harbours in the Western Cape and KwaZulu-Natal provinces, using pitfall trapping, yellow pan traps, and baiting. In addition, ant collections from Iziko Museums of South Africa (Cape Town, South Africa), University of KwaZulu-Natal (Pietermaritzburg campus, South Africa), Iimbovane Outreach Project (Stellenbosch University, South Africa), and AfriBugs CC (Pretoria, South Africa) were examined for specimens of A. gracilipes. The invasive species A. gracilipes was not detected from any of the sampled harbours during this study, nor in the main ant collections in South Africa. The only, and potentially erroneous published record of A. gracilipes in South Africa, is from Durban harbour and subsequent possibly erroneous citizen science observations are from other coastal sites such as Gansbaai, Knysna, Table Bay, and Kalk Bay. This is a positive outcome for conservation authorities as this species is highly invasive and, if introduced, will likely outcompete native fauna and result in ecosystem collapse. Although A. gracilipes was not detected in the samples from this study, early detection and eradication of this species should be prioritised. This can be achieved through existing pest monitoring programs at harbours, and continued border biosecurity measures.

New and little-known Isotominae (Collembola, Isotomidae) from South Africa.

Three new species, Parisotoma ruseki sp. nov., P. yehlathi sp. nov., and Folsomotoma amyliuae sp. nov. are described from South Africa. Parisotoma ruseki sp. nov. is characterized by four posterior s-chaetae on each side of the three first abdominal segments and seven posterior chaetae on dens, Parisotoma yehlathi sp. nov. by five s-chaetae and eight chaetae on dens, respectively. All s-chaetae on the body of Folsomotoma amyliuae sp. nov. are short, unlike its congeners. The genera Folsomotoma and Halisotoma are recorded for the first time in South Africa.

A shocking-red new species of Setanodosa Salmon, 1942 (Collembola: Brachystomellidae) from South Africa.

A new species of Setanodosa, S. jacquesi sp. nov. is described from the Western Cape (South Africa). It differs from other species of the genus by its unique shocking red pigmentation, the number of vesicles in the post antennal organ, and the number of clavate tenent hairs on the tibiotarsi. A comparative table of the world Setanodosa and a key of Brachystomellidae species known from South Africa are provided. DNA barcoding results are provided for several Brachystomellidae species from South Africa, Australia and the sub-Antarctic to support our findings. It shows that a species provisionally identified as Brachystomella cf. platensis is unambiguously present in both South Africa and Australia.

Mitogenome selection in the evolution of key ecological strategies in the ancient hexapod class Collembola.

A longstanding question in evolutionary biology is how natural selection and environmental pressures shape the mitochondrial genomic architectures of organisms. Mitochondria play a pivotal role in cellular respiration and aerobic metabolism, making their genomes functionally highly constrained. Evaluating selective pressures on mitochondrial genes can provide functional and ecological insights into the evolution of organisms. Collembola (springtails) are an ancient hexapod group that includes the oldest terrestrial arthropods in the fossil record, and that are closely associated with soil environments. Of interest is the diversity of habitat stratification preferences (life forms) exhibited by different species within the group. To understand whether signals of positive selection are linked to the evolution of life forms, we analysed 32 published Collembola mitogenomes in a phylomitogenomic framework. We found no evidence that signatures of selection are correlated with the evolution of novel life forms, but rather that mutations have accumulated as a function of time. Our results highlight the importance of nuclear-mitochondrial interactions in the evolution of collembolan life forms and that mitochondrial genomic data should be interpreted with caution, as complex selection signals may complicate evolutionary inferences.

Taxonomy of the Proisotoma complex. VI. Rediscovery of the genus Bagnallella Salmon, 1951 and epitoky in Bagnallelladavidi (Barra, 2001), comb. nov. from South Africa.

The genus Bagnallella Salmon is restored and given a diagnosis. It takes an intermediate position between Proisotoma Börner and Cryptopygus Willem complexes and is characterized by the separation of the two last abdominal segments (like in Proisotoma) and 3 and 5 s-chaetae on the fourth and fifth abdominal segments (like in Cryptopygus and its allies). A list of and key to species belonging to Bagnallella is given. Bagnallellabiseta comb. nov., B.dubia comb. nov., B.sedecimoculata comb. nov., and B.tenella comb. nov. are commented and redescribed. Morphology of Bagnallelladavidi (Barra), comb. nov. is described from the specimens from South Africa. So far B.davidi appears to be a complex of forms differing in size of the furca and macrochaetae. Two types of strongly modified males were found and described. Antennae, ventral side of abdomen, posterior edge of abdominal tergites, and mandibles are affected with epitoky. The nature of the discovered strong polymorphism is unclear.

An unusually diverse genus of Collembola in the Cape Floristic Region characterised by substantial desiccation tolerance.

Trait-environment interactions have contributed to the remarkable plant radiations in the Cape Floristic Region (CFR) of southern Africa. Whether such interactions have also resulted in the diversification of the invertebrate fauna, independently of direct associations with plants is, however, not clear. One candidate where this may be the case is the unusually diverse Collembola genus Seira. Including 89 species in the CFR, many of which are localised habitat specialists, this genus includes many species inhabiting the warm, dry fynbos shrubland-a habitat atypical of usually desiccation-sensitive Collembola. Here, we investigate whether desiccation tolerance may have contributed to the considerable diversity of Seira in the CFR. First, we demonstrate, by measuring vapour pressure deficits (VPD) of the species' microhabitats (fynbos shrubland and moister Afrotemperate Forests), that the fynbos shrublands are dry environments (mean ± S.E. maximum VPD 5.2 ± 0.1 kPa) compared with the Afrotemperate Forest patches (0.3 ± 0.02 kPa) during the summer activity period of Seira. Then we show that Seira species living in these shrublands are more desiccation tolerant (mean ± S.E. survival time at 76% relative humidity: 74.3 ± 3.3 h) than their congeners in the cooler, moister Afrotemperate Forests (34.3 ± 2.8 h), and compared with Collembola species globally (3.7 ± 0.2 h). These results, and a previous demonstration of pronounced thermal tolerance in the fynbos shrubland species, suggest that the diversity of Seira in the CFR is at least partly due to pronounced desiccation and thermal tolerance, which has enabled species in the genus to exploit the hot and dry habitats of the CFR.

Constant and fluctuating temperature acclimations have similar effects on phenotypic plasticity in springtails.

Much interest exists in the extent to which constant versus fluctuating temperatures affect thermal performance traits and their phenotypic plasticity. Theory suggests that effects should vary with temperature, being especially pronounced at more extreme low (because of thermal respite) and high (because of Jensen's inequality) temperatures. Here we tested this idea by examining the effects of constant temperatures (10 to 30 °C in 5 °C increments) and fluctuating temperatures (means equal to the constant temperatures, but with fluctuations of ±5 °C) temperatures on the adult (F2) phenotypic plasticity of three thermal performance traits - critical thermal minimum (CTmin), critical thermal maximum (CTmax), and upper lethal temperature (ULT50) in ten species of springtails (Collembola) from three families (Isotomidae 7 spp.; Entomobryidae 2 spp.; Onychiuridae 1 sp.). The lowest mean CTmin value recorded here was -3.56 ± 1.0 °C for Paristoma notabilis and the highest mean CTmax was 43.1 ± 0.8 °C for Hemisotoma thermophila. The Acclimation Response Ratio for CTmin was on average 0.12 °C/°C (range: 0.04 to 0.21 °C/°C), but was much lower for CTmax (mean: 0.017 °C/°C, range: -0.015 to 0.047 °C/°C) and lower also for ULT50 (mean: 0.05 °C/°C, range: -0.007 to 0.14 °C/°C). Fluctuating versus constant temperatures typically had little effect on adult phenotypic plasticity, with effect sizes either no different from zero, or inconsistent in the direction of difference. Previous work assessing adult phenotypic plasticity of these thermal performance traits across a range of constant temperatures can thus be applied to a broader range of circumstances in springtails.

Taxonomy of the Cryptopygus complex. III. The revision of South African species of Cryptopygus and Isotominella (Collembola, Isotomidae).

Species of the genera of the Cryptopygus complex in South Africa are morphologically revised. Five new species of the genus Cryptopygus Willem, 1902 s. s. and one new species of the genus Isotominella Delamare Deboutteville, 1948 are described. Cryptopygus abulbus sp. nov. and C. bulbus sp. nov. have only one chaeta on the anterior side of dens and no chaetae on the anterior side of manubrium, the latter species being characterized by the presence of a bulb at apex of antennae; C. inflatus sp. nov. shows a rare combination of eight ocelli on each side of the head with a tridentate mucro; C. longisensillus sp. nov. has five long s-chaetae on the fifth abdominal segment; C. postantennalis sp. nov. is unique by having a very long and slender postantennal organ with strong inner denticles; Isotominella laterochaeta sp. nov. is the second member of the genus and differs from the type species by many more anterior chaetae on the manubrium and the presence of chaetae on ventral side of metathorax. The genera are discussed and a key to all species of the Cryptopygus complex recorded in South Africa is given. The focus is on the Western Cape Province where the complex is the most diverse and sampling more complete than in other provinces of South Africa.

Basal tolerance but not plasticity gives invasive springtails the advantage in an assemblage setting.

As global climates change, alien species are anticipated to have a growing advantage relative to their indigenous counterparts, mediated through consistent trait differences between the groups. These insights have largely been developed based on interspecific comparisons using multiple species examined from different locations. Whether such consistent physiological trait differences are present within assemblages is not well understood, especially for animals. Yet, it is at the assemblage level that interactions play out. Here, we examine whether physiological trait differences observed at the interspecific level are also applicable to assemblages. We focus on the Collembola, an important component of the soil fauna characterized by invasions globally, and five traits related to fitness: critical thermal maximum, minimum and range, desiccation resistance and egg development rate. We test the predictions that the alien component of a local assemblage has greater basal physiological tolerances or higher rates, and more pronounced phenotypic plasticity than the indigenous component. Basal critical thermal maximum, thermal tolerance range, desiccation resistance, optimum temperature for egg development, the rate of development at that optimum and the upper temperature limiting egg hatching success are all significantly higher, on average, for the alien than the indigenous components of the assemblage. Outcomes for critical thermal minimum are variable. No significant differences in phenotypic plasticity exist between the alien and indigenous components of the assemblage. These results are consistent with previous interspecific studies investigating basal thermal tolerance limits and development rates and their phenotypic plasticity, in arthropods, but are inconsistent with results from previous work on desiccation resistance. Thus, for the Collembola, the anticipated advantage of alien over indigenous species under warming and drying is likely to be manifest in local assemblages, globally.

Springtail phylogeography highlights biosecurity risks of repeated invasions and intraregional transfers among remote islands.

Human-mediated transport of species outside their natural range is a rapidly growing threat to biodiversity, particularly for island ecosystems that have evolved in isolation. The genetic structure underpinning island populations will largely determine their response to increased transport and thus help to inform biosecurity management. However, this information is severely lacking for some groups, such as the soil fauna. We therefore analysed the phylogeographic structure of an indigenous and an invasive springtail species (Collembola: Poduromorpha), each distributed across multiple remote sub-Antarctic islands, where human activity is currently intensifying. For both species, we generated a genome-wide SNP data set and additionally analysed all available COI barcodes. Genetic differentiation in the indigenous springtail Tullbergia bisetosa is substantial among (and, to a lesser degree, within) islands, reflecting low dispersal and historic population fragmentation, while COI patterns reveal ancestral signatures of postglacial recolonization. This pronounced geographic structure demonstrates the key role of allopatric divergence in shaping the region's diversity and highlights the vulnerability of indigenous populations to genetic homogenization via human transport. For the invasive species Hypogastrura viatica, nuclear genetic structure is much less apparent, particularly for islands linked by regular shipping, while diverged COI haplotypes indicate multiple independent introductions to each island. Thus, human transport has likely facilitated this species' persistence since its initial colonization, through the ongoing introduction and inter-island spread of genetic variation. These findings highlight the different evolutionary consequences of human transport for indigenous and invasive soil species. Crucially, both outcomes demonstrate the need for improved intraregional biosecurity among remote island systems, where the policy focus to date has been on external introductions.

Comparing thermal performance curves across traits: how consistent are they?

Thermal performance curves (TPCs) are intended to approximate the relationship between temperature and fitness, and are commonly integrated into species distributional models for understanding climate change responses. However, TPCs may vary across traits because selection and environmental sensitivity (plasticity) differ across traits or because the timing and duration of the temperature exposure, here termed time scale, may alter trait variation. Yet, the extent to which TPCs vary temporally and across traits is rarely considered in assessments of climate change responses. Using a common garden approach, we estimated TPCs for standard metabolic rate (SMR), and activity in Drosophila melanogaster at three test temperatures (16, 25 and 30°C), using flies from each of six developmental temperatures (16, 18, 20, 25, 28 and 30°C). We examined the effects of time scale of temperature exposure (minutes/hours versus days/weeks) in altering TPC shape and position, and commonly used descriptors of the TPC: thermal optimum (Topt), thermal limits (Tmin and Tmax) and thermal breadth (Tbr). In addition, we collated previously published estimates of TPCs for fecundity and egg-to-adult viability in D. melanogaster We found that the descriptors of the TPCs varied across traits (egg-to-adult viability, SMR, activity and fecundity), but variation in TPCs within these traits was small across studies when measured at the same time scales. The time scale at which traits were measured contributed to greater variation in TPCs than the observed variance across traits, although the relative importance of time scale differed depending on the trait (activity versus fecundity). Variation in the TPC across traits and time scales suggests that TPCs using single traits may not be an accurate predictor of fitness and thermal adaptation across environments.

Basal resistance enhances warming tolerance of alien over indigenous species across latitude.

Soil systems are being increasingly exposed to the interactive effects of biological invasions and climate change, with rising temperatures expected to benefit alien over indigenous species. We assessed this expectation for an important soil-dwelling group, the springtails, by determining whether alien species show broader thermal tolerance limits and greater tolerance to climate warming than their indigenous counterparts. We found that, from the tropics to the sub-Antarctic, alien species have the broadest thermal tolerances and greatest tolerance to environmental warming. Both groups of species show little phenotypic plasticity or potential for evolutionary change in tolerance to high temperature. These trait differences between alien and indigenous species suggest that biological invasions will exacerbate the impacts of climate change on soil systems, with profound implications for terrestrial ecosystem functioning.

Taxonomy of the Cryptopygus complex. II. Affinity of austral Cryptopygus s.s. and Folsomia, with the description of two new Folsomia species (Collembola, Isotomidae).

Folsomia minoraesp. n. and Folsomia australicasp. n. are described from New Zealand and Australia, respectively. Their possible affinity to two different groups of Cryptopygussensu stricto is discussed. Attention is paid to the variability of sensillary patterns of the genital segment in Cryptopygus: mainly, all s-chaetae are subequal, but in more advanced forms the dorsal triplet, lateral duplet or either of them become macrochaeta-like in length. Cryptopygus ulrikeae (= Folsomia ulrikeae Najt & Thibaud, 1987), comb. n. is given a new generic position.

Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being.

Distributions of Earth's species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation's Sustainable Development Goals.

Interactions between rates of temperature change and acclimation affect latitudinal patterns of warming tolerance.

Critical thermal limits form an increasing component of the estimation of impacts of global change on ectotherms. Whether any consistent patterns exist in the interactive effects of rates of temperature change (or experimental ramping rates) and acclimation on critical thermal limits and warming tolerance (one way of assessing sensitivity to climate change) is, however, far from clear. Here, we examine the interacting effects of ramping rate and acclimation on the critical thermal maxima (CTmax) and minima (CTmin) and warming tolerance of six species of springtails from sub-tropical, temperate and polar regions. We also provide microhabitat temperatures from 26 sites spanning 5 years in order to benchmark environmentally relevant rates of temperature change. Ramping rate has larger effects than acclimation on CTmax, but the converse is true for CTmin. Responses to rate and acclimation effects are more consistent among species for CTmax than for CTmin. In the latter case, interactions among ramping rate and acclimation are typical of polar species, less marked for temperate ones, and reduced in species from the sub-tropics. Ramping rate and acclimation have substantial effects on estimates of warming tolerance, with the former being more marked. At the fastest ramping rates (>1.0°C/min), tropical species have estimated warming tolerances similar to their temperate counterparts, whereas at slow ramping rates (<0.4°C/min) the warming tolerance is much reduced in tropical species. Rates of temperate change in microhabitats relevant to the springtails are typically <0.05°C/min, with rare maxima of 0.3-0.5°C/min depending on the site. These findings emphasize the need to consider the environmental setting and experimental conditions when assessing species' vulnerability to climate change using a warming tolerance approach.

Indirect effects of habitat disturbance on invasion: nutritious litter from a grazing resistant plant favors alien over native Collembola.

Biological invasions are major threats to biodiversity, with impacts that may be compounded by other forms of environmental change. Observations of high density of the invasive springtail (Collembola), Hypogastrura manubrialis in heavily grazed renosterveld vegetation in the Western Cape, South Africa, raised the question of whether the invasion was favored by changes in plant litter quality associated with habitat disturbance in this vegetation type. To examine the likely mechanisms underlying the high abundance of H. manubrialis, cages with three types of naturally occurring litter with different nutrient content were placed out in the area and collected after different periods of time. Hypogastrura manubrialis was mainly found in the nutrient-rich litter of the yellowbush (Galenia africana), which responds positively to disturbance in the form of overgrazing. This suggests that invasion may have been facilitated by a positive interaction with this grazing resistant plant. By contrast, indigenous Collembola were least abundant in yellowbush litter. Negative correlations between high abundance of H. manubrialis and the abundance and diversity of other species suggest that competitive interactions might underlie low abundance of these other species at the patch level. Group behavior enables H. manubrialis to utilize efficiently this ephemeral, high quality resource, and might improve its competitive ability. The results suggest that interactions among environmental change drivers may lead to unforeseen invasion effects. H. manubrialis is not likely to be very successful in un-grazed renosterveld, but in combination with grazing, favoring the nutrient-rich yellowbush, it may become highly invasive. Field manipulations are required to fully verify these conclusions.

Growth and reproduction of laboratory-reared neanurid Collembola using a novel slime mould diet.

Although significant progress has been made using insect taxa as model organisms, non-tracheated terrestrial arthropods, such as Collembola, are underrepresented as model species. This underrepresentation reflects the difficulty in maintaining populations of specialist Collembola species in the laboratory. Until now, no species from the family Neanuridae have been successfully reared. Here we use controlled growth experiments to provide explicit evidence that the species Neanura muscorum can be raised under laboratory conditions when its diet is supplemented with slime mould. Significant gains in growth were observed in Collembola given slime mould rather than a standard diet of algae-covered bark. These benefits are further highlighted by the reproductive success of the experimental group and persistence of laboratory breeding stocks of this species and others in the family. The necessity for slime mould in the diet is attributed to the 'suctorial' mouthpart morphology characteristic of the Neanuridae. Maintaining laboratory populations of neanurid Collembola species will facilitate their use as model organisms, paving the way for studies that will broaden the current understanding of the environmental physiology of arthropods.

Updated list of Collembola species currently recorded from South Africa.

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.