Elsevier

Pedobiologia

Volume 67, March 2018, Pages 45-56
Pedobiologia

Desoria trispinata (MacGillivray, 1896), a promising model Collembola species to study biological invasions in soil communities

https://doi.org/10.1016/j.pedobi.2017.11.003Get rights and content

Highlights

  • The species is easy to culture on standard gypsum-charcoal mixture.

  • D.trispinata reared by us was identified by using barcode data and morphological characters.

  • The species reproduces very fast, is very competitive and invasive.

  • Resistance to adverse conditions and toxicity contribute to its success.

  • Specimens from Germany, Russia and the UK shared a homogeneous mt COI pattern.

Abstract

The species Desoria trispinata (MacGillivray, 1896) is globally distributed but probably not native to Europe. Reports on its occurrence have increased substantially over the last years, proving that it is extremely successful, often dominating in number not only Collembola but the entire macroscopic soil fauna under favourable conditions. Still, D. trispinata has seldom been studied, and its systematic position is poorly understood. We compiled available literature on the ecology of this species, rendering information with respect to its success. In addition, during the past years we established a controlled laboratory culture and recorded life history data. Finally, we ran a molecular genetic analysis. COI sequence divergence between specimens of D. trispinata was low among specimens from Germany, UK and Russia (up to 0.1%) clearly separating these specimens from other species of the genus Desoria. However, distance to specimens of D. trispinata from Japan was high (up to 15.3%).

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.

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