Molecular phylogeny and trait evolution in an ancient terrestrial arthropod lineage: Systematic revision and implications for ecological divergence (Collembola, Tomocerinae).

Phylogenetic assessments of functional traits are important for mechanistically understanding the interactions between organisms and environments, but such practices are strongly limited by the availability of phylogenetic frameworks. The tomocerin springtails are an ancient, widespread and ecologically important group of terrestrial arthropods, whereas their phylogeny and trait evolution remained unaddressed. In the present study, we conducted the first comprehensive phylogenetic reconstruction of Tomocerinae, based on a multi-loci molecular dataset covering all major lineages within the subfamily, using Bayesian inference (BI), maximum-likelihood (ML) and maximum-parsimony (MP) approaches. Divergence time was estimated and ancestral character state reconstruction (ACSR) was performed to trace the evolutionary history of five ecomorphological traits correlated with sensory and locomotory functions. Our results support the monophyly of Tomocerinae, and indicate that current classification of Tomocerinae only partially reflects evolutionary relationships, notably the commonest and speciose genus Tomocerus is polyphyletic. The subfamily probably originated in Early Cretaceous and diversified in two Cretaceous and one Eocene radiation events. As indicated by the evolutionary patterns of functional traits, multiple ecological divergences took place during the diversification of Tomocerinae. The study suggests a potential underestimation of ecological divergence and functional diversity in terrestrial arthropods, calls for an update of present trait databases, and demonstrates the value of macroevolutionary knowledge for improving the trait-based ecology. In addition, Tomocerus, Tomocerina and Tritomurus are redefined, a new genus Yoshiicerusgen. n. and new subgenera Coloratomurussubgen. n., Ciliatomurussubgen. n., Striatomurussubgen. n. and Ocreatomurussubgen. n. are described in the appendix.

Molecular phylogeny reveals independent origins of body scales in Entomobryidae (Hexapoda: Collembola).

Entomobryidae is the largest family in Collembola but relationships within the family have never been subjected to rigorous phylogenetic analyses. Within the family, body scales are present in many species, and are fundamental in the classification at the subfamilial and tribal levels. A molecular phylogeny was reconstructed using the nuclear 18SrRNA and partial 28SrRNA and the mitochondrial 16SrRNA to examine the evolution of scales across Entomobryidae subfamilies. These datasets were analyzed separately and combined, with parsimony, likelihood and Bayesian algorithms. Monophyly of Orchesellinae was not recovered, and it was split into a scaled clade and an unscaled clade, contradicting to all recent taxonomic conceptions. The monophyly of Entomobryinae, Seirinae and Lepidocyrtinae is well supported however within Entomobryinae, the polyphyly of Entomobryini and Willowsiini implies that classification using the presence/absence of scales is not valid. Analyses of ancestral character state reconstruction in Entomobryidae indicate that the presence of body scales have evolved independently at least five times, with a loss of scales occurring independently at least twice. A revision of the family Entomobryidae on molecular and morphological basis is clearly needed.

New species of Sinella and Coecobrya (Collembola: Entomobryidae) from New Caledonia.

The genera Sinella and Coecobrya are reported from New Caledonia for the first time, with four new species: Sinella quadriseta sp. nov., S. claviseta sp. nov., S. copiosa sp. nov., and Coecobrya neocaledonica sp. nov. Sinella species studied here exhibit several morphological features that are not found in other non-cave species of the genus: paired teeth on inner edge of unguis closer to the base and distal unpaired tooth very tiny or absent, 2 medio-medial and 1 medio-lateral macrochaetae on Th. II, 2+2 lateral macrochaetae on Abd. III, and abundant short S-chaetae on Abd. IV. The four S-chaetae present on Abd. V are also different from the common pattern in Entomobryidae. C. neocaledonica sp. nov. does not exhibit unique features different from Coecobrya species of other areas.

First record of the genus Australonura Cassagnau 1980 (Collembola: Neanuridae) in the New World, with description of a new species from Paraguay.

The genus Australonura Cassagnau 1980 is newly recorded from South America. The Patagonian species Paleonura limnophila (Cassagnau & Rapoport, 1962) and Paleonura friasica Cassagnau & Oliveira, 1990 are redescribed from type material and recombined in Australonura. A new species, A. paraguayensis sp. nov., is described from Paraguay and assigned to Australonura for its head tubercle arrangement. It differs from other species of the genus by its adjacent but separate dorso-internal tubercles of Abd. V.

New species of Monodontocerus (Collembola: Tomoceridae) from southern China with diagnostic notes on the genus and introduction of new taxonomic characters.

Three new species of Monodontocerus are described from caves in southern China: M. absens sp. nov. is characterized by its cephalic chaetotaxy and the absence of chaetae from the tenaculum; M. mulunensis sp. nov. is characterized by a combination of characters including chaetotaxy, foot complex and furca; M. trigrandis sp. nov. is different from other species in the formula of dental spines and the reduction of the ungual teeth. A key to the species of Monodontocerus is provided. Potential diagnostic characters for this genus are proposed. Troglomorphy and interspecific variability are discussed. Pseudopores and the dorsal disto-lateral chaeta on the manubrium are introduced as new taxonomic characters for Tomocerinae. 

Global fine-resolution data on springtail abundance and community structure.

Springtails (Collembola) inhabit soils from the Arctic to the Antarctic and comprise an estimated ~32% of all terrestrial arthropods on Earth. Here, we present a global, spatially-explicit database on springtail communities that includes 249,912 occurrences from 44,999 samples and 2,990 sites. These data are mainly raw sample-level records at the species level collected predominantly from private archives of the authors that were quality-controlled and taxonomically-standardised. Despite covering all continents, most of the sample-level data come from the European continent (82.5% of all samples) and represent four habitats: woodlands (57.4%), grasslands (14.0%), agrosystems (13.7%) and scrublands (9.0%). We included sampling by soil layers, and across seasons and years, representing temporal and spatial within-site variation in springtail communities. We also provided data use and sharing guidelines and R code to facilitate the use of the database by other researchers. This data paper describes a static version of the database at the publication date, but the database will be further expanded to include underrepresented regions and linked with trait data.

The genus Cyphoderopsis Carpenter (Collembola: Paronellidae) in Thailand and a faunal transition at the Isthmus of Kra in Troglopedetinae.

The genus Cyphoderopsis Carpenter is recorded for the first time from continental Southeast Asia, with four new species described from Peninsular Thailand. New characters of taxonomic importance are introduced. The new species herein described are distinguished from other species of the genus by the following combination of characters: dens with two rows of spines, absence of eyes and pigment, and claw with inner teeth. They differ among them in the number of inner teeth on claw, morphology of tenent hairs (pointed versus clavate), number of dental spines and number of central macrochaetae on Th.II (3+3 versus 4+4). The genus Cyphoderopsis in Thailand is shown to be restricted to the South of the Isthmus of Kra, while the closely related genus, Troglopedetes Absolon, replaces it further north, providing new evidence that the Isthmus of Kra is an important biogeographical boundary in Southeast Asia. A checklist and a key to world species of the genus are given.

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.

Systematics of Lepidocyrtinusboneti Denis, 1948 (Collembola, Seirinae) reveals a new position for the species within Seirinae.

Seiraboneti Denis, 1948, comb. nov. is examined and redescribed based on syntypes and by a newly discovered Chinese population. Lectotype and paralectotypes were designated, and the type locality of the species has been fixed to Câuda, near Nhatrang, Vietnam. The species was first described in the genus Lepidocyrtinus, but based on morphological and molecular evidence it is here transferred to Seira. For the phylogenetic placement of Seiraboneticomb. nov., its mitogenome was included in a dataset comprising 19 species of Seirinae. Maximum Likelihood and Bayesian inferences clustered the species next to Seirasanloemensis Godeiro & Cipola, 2020 from Cambodia, forming a distinct Seira clade from the Old World, confirming the hypothesis of the existence of a different basal lineage of Seirinae in Southern Asia.

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.

Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenomic rearrangements.

Here we study the evolution of nucleotide composition in third codon-positions of CO1 sequences of Chelicerata, using a phylogenetic framework, based on 180 taxa and three markers (CO1, 18S, and 28S rRNA; 5,218 nt). The analyses of nucleotide composition were also extended to all CO1 sequences of Chelicerata found in GenBank (1,701 taxa). The results show that most species of Chelicerata have a positive strand bias in CO1, i.e., in favor of C nucleotides, including all Amblypygi, Palpigradi, Ricinulei, Solifugae, Uropygi, and Xiphosura. However, several taxa show a negative strand bias, i.e., in favor of G nucleotides: all Scorpiones, Opisthothelae spiders and several taxa within Acari, Opiliones, Pseudoscorpiones, and Pycnogonida. Several reversals of strand-specific bias can be attributed to either a rearrangement of the control region or an inversion of a fragment containing the CO1 gene. Key taxa for which sequencing of complete mitochondrial genomes will be necessary to determine the origin and nature of mtDNA rearrangements involved in the reversals are identified. Acari, Opiliones, Pseudoscorpiones, and Pycnogonida were found to show a strong variability in nucleotide composition. In addition, both mitochondrial and nuclear genomes have been affected by higher substitution rates in Acari and Pseudoscorpiones. The results therefore indicate that these two orders are more liable to fix mutations of all types, including base substitutions, indels, and genomic rearrangements.

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.

Response of arboreal Collembola communities to the conversion of lowland rainforest into rubber and oil palm plantations.

BACKGROUND: In the last decades, Southeast Asia has experienced massive conversion of rainforest into rubber and oil palm monoculture plantations. The effects of this land-use change on canopy arthropods are still largely unknown. Arboreal Collembola are among the most abundant canopy arthropods in tropical forests, potentially forming a major component of the canopy food web by contributing to the decomposition of arboreal litter and being an important prey for canopy arthropod predators. We investigated abundance, richness, and community composition of, as well as the influence of a series of environmental factors on, canopy Collembola communities in four land-use systems in Jambi Province, Sumatra, Indonesia: (1) lowland rainforest, (2) jungle rubber (rubber agroforest), and monoculture plantations of (3) rubber and (4) oil palm. RESULTS: Using canopy fogging in 32 research plots in both the dry and rainy seasons in 2013, we collected 77,104 specimens belonging to 68 (morpho) species. Generally, Collembola communities were dominated by few species including two species of the genus Salina (Paronellidae; 34% of total individuals) and two species of Lepidocyrtinae (Entomobryidae; 20%). The abundance of Collembola in lowland rainforest (53.4 ± 30.7 ind. m-2) was more than five times higher than in rubber plantations, and more than ten times higher than in oil palm plantations; abundances in jungle rubber were intermediate. Collembola species richness was highest in rainforest (18.06 ± 3.60 species) and jungle rubber (16.88 ± 2.33 species), more than twice that in rubber or oil palm. Collembola community composition was similar in rainforest and jungle rubber, but different from monoculture plantations which had similar Collembola community composition to each other. The environmental factors governing community composition differed between the land-use systems and varied between seasons. CONCLUSIONS: Overall, this is the first in-depth report on the structure of arboreal Collembola communities in lowland rainforest and agricultural replacement systems in Southeast Asia. The results highlight the potentially major consequences of land-use change for the functioning of arboreal arthropod food webs.

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.

Towards evidence-based conservation of subterranean ecosystems.

Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-analytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.

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.

Conversion of rainforest into oil palm and rubber plantations affects the functional composition of litter and soil Collembola.

Rainforest conversion and expansion of plantations in tropical regions are associated with changes in animal communities and biodiversity decline. In soil, Collembola are one of the most numerous invertebrate groups that affect the functioning of microbial communities and support arthropod predators. Despite that, information on the impact of changes in land use in the tropics on species and trait composition of Collembola communities is very limited. We investigated the response of Collembola to the conversion of rainforest into rubber agroforestry ("jungle rubber"), rubber, and oil palm plantations in Jambi Province (Sumatra, Indonesia), a region which experienced one of the strongest recent deforestation globally. Collembola were sampled in 2013 and 2016 from the litter and soil layer using heat extraction, and environmental factors were measured (litter C/N ratio, pH, water content, composition of microbial community and predator abundance). In the litter layer, density and species richness in plantation systems were 25%-38% and 30%-40% lower, respectively, than in rainforest. However, in the soil layer, density, species richness, and trait diversity of Collembola were only slightly affected by land-use change, contrasting the response of many other animal groups. Species and trait composition of Collembola communities in litter and soil differed between each of the land-use systems. Water content and pH were identified as main factors related to the differences in species and trait composition in both litter and soil, followed by the density of micro- and macropredators. Dominant species of Collembola in rainforest and jungle rubber were characterized by small body size, absence of furca, and absence of intense pigmentation, while in plantations, larger species with long furca and diffuse or patterned pigmentation were more abundant. Overall, land-use change negatively affected Collembola communities in the litter layer, but its impact was lower in the soil layer. Several pantropical genera of Collembola (i.e., Isotomiella, Pseudosinella, and Folsomides) dominated across land-use systems, reflecting their high environmental adaptability and/or efficient dispersal, calling for studies on their ecology and genetic diversity. The decline in species richness and density of litter-dwelling Collembola with the conversion of rainforest into plantation systems calls for management practices mitigating negative effects of the deterioration of the litter layer in rubber plantations, but even more in oil palm plantations.

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.

The multiformity of antennal chaetae in Troglopedetes Joseph, 1872 (Collembola, Paronellidae, Troglopedetinae), with descriptions of two new species from Thailand.

Two new species of the genus Troglopedetes Joseph, 1872 (T. meridionalis sp. nov. and T. kae sp. nov.) are described from caves of the Thai peninsula. This is the first report of the genus south of the Kra Isthmus. The two new species have two rows of dental spines shared by all Thai Troglopedetes. They differ from other members of the genus mainly in the arrangement of dorsal chaetotaxy on head. The antennal chaetotaxy of the two species is analysed in detail in the second part of the paper. All types of antennal chaetae of both new species and their distribution patterns are described for each antennal segment: scales, ordinary chaetae, S-chaetae and subapical organite of Ant. IV. Twenty different types of chaetae are recognised and all except one are present in both species. The total numbers of ordinary chaetae and S-chaetae and their patterns of distribution on antenna are very similar between the two species (483 vs. 518 ordinary chaetae; 207 vs. 208 S-chaetae). Each type of chaetae has its own distribution pattern, markedly contrasted between dorsal and ventral side of antennae, and between antennal segments. This diversity of morphologies and distribution patterns and their similarity between the two species, as well as differences with other species of the same family, suggest that antennal chaetotaxy could provide powerful new characters for the taxonomy of Troglopedetes and related genera.