Desoria trispinata (MacGillivray, 1896), a promising model Collembola species to study biological invasions in soil communities
Introduction
Collembola are a diverse group of microarthropods (Maaß et al., 2015) that live in most soils and ecosystems (Rusek, 1998). They can occur in high abundances, e.g. up to ∼100,000 individuals/m2 in grasslands (Bardgett and Cook, 1998), and are an essential part of soil ecosystems, e.g. as consumers of fungi and litter (Fountain and Hopkin, 2005). Therefore, and since they are sensitive to soil characteristics and contaminants they are exposed to, Collembola are used in ecotoxicological tests and soil quality assessment (Fountain and Hopkin, 2005, Janus et al., 2015, OECD, 2015).
The role of Collembola in community ecology has frequently been studied, too. To better understand the specific impact of individual species on ecosystem processes, manifold experiments with single species (e.g. Buse et al., 2013, Lartey et al., 1994) or manipulated community composition have been performed (e.g. ÁBear et al., 2012, Cragg and Bardgett, 2001, D’Annibale et al., 2015, Eisenhauer et al., 2011). However, all those studies were restricted to a limited set of clearly defined species that can be cultivated in the laboratory. The same holds true for ecotoxicological tests. Most of them are confined to the standard organism Folsomia candida, Willem, 1902, on which the OECD (Organisation for Economic Co-operation and Development) guideline is based (Fountain and Hopkin, 2005). However, there are hints that even different laboratory strains of F. candida may differ in sensitivity (Crommentuijn et al., 1995, Diogo et al., 2007). Other species are permitted by the guideline as well if, e.g., these species are unequivocally identified and their reproductive biology is included within the test time, which means their life-history and optimal cultural conditions for growth and reproduction should be known (OECD, 2015).
Further, in recent years, community tests have received increasing attention to take into account sensitivity differences between species (e.g. Filser et al., 2014, Renaud et al., 2017, Scott-Fordsmand et al., 2008). Sometimes specimens for such tests come from various field collections (Buch et al., 2016, Chelinho et al., 2014, Van den Brink et al., 2005), complicating standardisation. The majority of species in culture are euedaphic or hemiedaphic, whereas to our knowledge only very few epigeic species are available. These are mostly Orchesella cincta (Linnaeus, 1758; Costa et al., 2012) and Hypogastrura assimilis (Krausbauer, 1898; D’Annibale et al., 2015, Scott-Fordsmand et al., 2008). D. trispinata is a cosmoplitan species that can occur in high abundances and several habitats (see Sections 3.5.1.1, 3.5.1.2). Back in 1970, Tanaka extensively studied D. trispinata, including its culture under laboratory conditions (Tanaka, 1970). However, he cultured the specimens in grassland soil, which is hard to control and difficult to standardize. The only controlled laboratory culture we are aware of had been mentioned in Toft and Wise (1999), who both have retired by now. Thus, their cultures are not available anymore.
D. trispinata is a highly important species as it occurs worldwide and at high abundances (see Sections 3.5.1.1, 3.5.1.2). However, very little recent information on the biology of this species is available in Web of Science©. To make the situation even more complicated, its identification is difficult (see Sections 3.1, 3.3). It can be confused with Isotoma viridis according to Shaw and Benefer (2015) and it shares characteristics with other Collembola, such as a tridentate mucro with the genera Parisotoma, Pseudisotoma and Isotoma (Fjellberg, 2007, Potapov, 2001). Thus far, its systematic position remains largely unexplored.
To use D. trispinata as “standard” test organism it is essential to know whether culturing of the specimens on gypsum-charcoal plates instead of soil is possible, and what are its corresponding life history data. Therefore we attempted to shed more light on the biology of this species. Specifically, we (i) compiled available literature, (ii) scrutinized discrepancies in existing identification keys, (iii) established a laboratory culture under controlled conditions including life history information and (iv) investigated mt COI barcode sequence diversity within our established culture in terms of species identification eligibility.
Our main research questions were:
- -
Does D. trispinata from different locations form a genetically homogeneous cluster that can be clearly separated from other species of the genus?
- -
Can the species be cultivated for a long period of time on a plaster of Paris/charcoal mixture?
- -
If so, does it exhibit similar life history data as in cultures with natural soil?
- -
Are there any recent studies that support the proposed invasiveness of D. trispinata?
Section snippets
Literature review
In April 2017 we ran a literature research using Web of Science©, ScienceDirect® and GoogleScholar© with Desoria trispinata and its synonyms (see Section 3.1) as keywords.
Species origin
The specimens were sampled from a population located in Bremen, Germany. In early April 2016 soil cores (depths: 0–4, 4–8 cm, 100 cm3) were taken within an extensive grassland (53.1301°N 008.8928°E). The dominating ground vegetation is Holcus mollis, H. lanatus and Poa pratensis interspersed with mainly Plantago lanceolata,
Morphological identification of living specimens
D. trispinata (MacGillivray, 1896) is a little-known Collembola (Shaw and Benefer, 2015) with several synonyms: Isotoma trispinata, Isotoma maritima meridionalis, Halisotoma meridionalis, Isotoma setinornata (Potapov, 2001). However, the synonym Isotoma trispinata can be mixed up with synonyms of other Desoria species (Bellinger et al., 1992–2017): Isotoma trispinata, Tuxen, 1944 which is partly synonymized to Desoria olivacea (Tullberg, 1871), partly to Desoria violacea (Tullberg, 1876). This
Conclusions
D. trispinata was originally described from Salineville, Ohio (MacGillivray, 1896) and later on intensively studied in Japan by Tanaka (1970). Today it is spread over India, Korea, Hawaii, the US, Canada, Central and South America, Europe, Russia and Turkey. The sequence of records seems to indicate that western areas of the Palaearctic are the territory of invasion of this species, which is possibly originated from either the East Palaearctic or the Nearctic.
We successfully established a
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Acknowledgements
We are indebted to Jürgen Schulz and Arne Fjellberg who confirmed the determination of Desoria trispinata (MacGillivray, 1896). We wish to extend our thanks to the two unknown reviewers for their constructive comments.
References (90)
- et al.
Functional aspects of soil animal diversity in agricultural grasslands
Appl. Soil Ecol.
(1998) - et al.
Ecotoxicity of mercury to Folsomia candida and Proisotoma minuta (Collembola: Isotomidae) in tropical soils: baseline for ecological risk assessment
Ecotoxicol. Environ. Saf.
(2016) - et al.
The Edaphobase Project of GBIF-Germany – a new online soil-zoological data warehouse
Appl. Soil Ecol.
(2014) - et al.
New trophic biomarkers for Collembola reared on algal diets
Pedobiologia (Jena)
(2013) - et al.
Community structures of Collembola in sugar maple forests: relations to humus type and seasonal trends
Pedobiologia (Jena)
(2000) - et al.
Soil microarthropod community testing: a new approach to increase the ecological relevance of effect data for pesticide risk assessment
Appl. Soil Ecol.
(2014) - et al.
How changes in soil faunal diversity and composition within a trophic group influence decomposition processes
Soil Biol. Biochem.
(2001) - et al.
Biodiversity of Collembola in tropical agricultural environments of Espı́rito Santo
Brazil. Appl. Soil Ecol.
(2002) - et al.
Influence of elevated CO2 and GM barley on a soil mesofauna community in a mesocosm test system
Soil Biol. Biochem.
(2015) - et al.
Natural occurrence of entomophthoralean fungi pathogenic to Collembolans
J. Invertebr. Pathol.
(2001)
Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity
Soil Biol. Biochem.
Experimental studies on the reactions of Collembola to copper contamination
Pedobiologia (Jena)
Collembola in ecotoxicology—Any news or just boring routine?
Appl. Soil Ecol.
Elaboration, characteristics and advantages of biochars for the management of contaminated soils with a specific overview on Miscanthus biochars
J. Environ. Manage.
Interactions of mycophagous Collembola and biological control fungi in the suppression of Rhizoctonia solani
Soil Biol. Biochem.
Functional role of microarthropods in soil aggregation
Pedobiologia (Jena)
Defensive role of cystidia against Collembola in the basidiomycetes Russula bella and Strobilurus ohshimae
Mycol. Res.
Biodiversidad de Collembola (Hexapoda: Entognatha) en México
Rev. Mex. Biodivers.
Organic wastes as soil amendments −Effects assessment towards soil invertebrates
J. Hazard. Mater.
The toxicity of copper contaminated soil using a gnotobiotic Soil Multi-species Test System (SMS)
Environ. Int.
Atmospheric CO2 enrichment induces life strategy- and species-specific responses of Collembolans in the rhizosphere of sugar beet and winter wheat
Soil Biol. Biochem.
Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing Collembola
Glob. Chang. Biol.
Spatial and temporal variation in the abundance and taxonomic composition of estuarine and terrestrial macrofauna associated with mangrove logs
J. Mar. Biol. Assoc. United Kingdom
Taxonomic Studies on Selected Species of Collembola from North-East India
Checklist of springtails (Collembola) from the Republic of Moldova
Trav. du Muséum Natl. d’Histoire Nat. Grigore Antipa
“COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies
J. Crustac. Biol.
Bioecology of edaphic Collembola and Acarina
Annu. Rev. Entomol.
Insects of Hawaii. Collembola., Museum
Influence of adaptive evolution of cadmium tolerance on neutral and functional genetic variation in Orchesella cincta
Ecotoxicology
Comparative ecotoxicity of cadmium, chlorpyrifos and triphenyltin hydroxide for four clones of the parthenogenetic collembolan Folsomia candida in an artificial soil
Funct. Ecol.
Techniques for clearing and mounting Collembola from old ethanol collections
Soil Org.
Tolerance of Genetically Characterized Folsomia candida Strains to Phenmedipham Exposure. A comparison between reproduction and avoidance tests
J. Soils Sediments
Impact of Mustards (Brassicaseae) Grown as Cover Crops on Non-target Arthropod Communities. Thesis
Ecological Studies of Soil Arthropods in Forest and Jhum Systems of Laitkor, Meghalaya. Thesis
Methoden Der Bodenbiologie
MUSCLE: Multiple sequence alignment with high accuracy and high throughput
Nucleic Acids Res.
The Collembola of Fennoscandia and Denmark, part II: Entomobryomorpha and Symphypleona
Fauna Entomologica Scandinavica
DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates
Mol. Mar. Biol. Biotechnol.
Folsomia candida (Collembola): a “standard” soil arthropod
Annu. Rev. Entomol.
Invertebrates associated with a horizontal-flow, subsurface constructed wetland in a northern climate
Environ. Entomol.
Soil Acarina and Collembola in forest and cultivated land of Khasi hill
Meghalaya. Rec. Zool. Surv. India
High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida)
J. Evol. Biol.
Cited by (3)
Half a century of thermal tolerance studies in springtails (Collembola): A review of metrics, spatial and temporal trends
2022, Current Research in Insect ScienceCitation Excerpt :These wingless and ametabolous animals help soil particle aggregation (Maaß et al., 2015), modifying organic matter that directly influences soil nutrient flux (Lussenhop and BassiriRad, 2005; Kaneda and Kaneko, 2008). For this reason, an increasing number of publications have used them as sentinels of anthropogenic-driven changes in ecosystems or as bioindicators of ecological stress (Convey et al., 2003; Cassagne et al., 2006; Greenslade, 2007; Zeppelini et al., 2009; Roithmeier et al., 2018). Both global warming and land use changes can have a significant impact on the processes of decomposition of organic matter (Jucevica and Melecis, 2006; Yin et al., 2019), which reinforces the importance of deepening the biology and ecophysiology of Collembola as a key group to understand the effects of global change on soil functioning.
DNA barcoding for revealing a possible new species of Anurophorus (Collembola: Isotomidae) associated with Korean fir (Abies koreana Wilson)
2020, Journal of Asia-Pacific BiodiversityCitation Excerpt :Second, the mean genetic distance between Anurophorus sp. and A. laricis was 14.5%, and this value from this study fell within the range to clarify species in case of Collembola (Stevens et al 2006; Porco et al 2014; Matsumoto et al 2019). This result could give us a strong suggestion that COI sequencing is useful for the discrimination of Anurophorus sp. from congeneric species (Barjadze et al 2016; Roithmeir et al 2018; Chang and Park 2020). Further sampling and investigations are needed for DNA barcoding of this genus.