The Curious and Neglected Soft-Bodied Meiofauna: Rouphozoa (Gastrotricha and Platyhelminthes)
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Hydrobiologia (2020) 847:2613–2644 https://doi.org/10.1007/s10750-020-04287-x (0123456789().,-volV)( 0123456789().,-volV) MEIOFAUNA IN FRESHWATER ECOSYSTEMS Review Paper The curious and neglected soft-bodied meiofauna: Rouphozoa (Gastrotricha and Platyhelminthes) Maria Balsamo . Tom Artois . Julian P. S. Smith III . M. Antonio Todaro . Loretta Guidi . Brian S. Leander . Niels W. L. Van Steenkiste Received: 1 August 2019 / Revised: 25 April 2020 / Accepted: 4 May 2020 / Published online: 26 May 2020 Ó Springer Nature Switzerland AG 2020 Abstract Gastrotricha and Platyhelminthes form a meiofauna. As a result, rouphozoans are usually clade called Rouphozoa. Representatives of both taxa underestimated in conventional biodiversity surveys are main components of meiofaunal communities, but and ecological studies. Here, we give an updated their role in the trophic ecology of marine and outline of their diversity and taxonomy, with some freshwater communities is not sufficiently studied. phylogenetic considerations. We describe success- Traditional collection methods for meiofauna are fully tested techniques for their recovery and study, optimized for Ecdysozoa, and include the use of and emphasize current knowledge on the ecology, fixatives or flotation techniques that are unsuitable for distribution, and dispersal of freshwater gastrotrichs the preservation and identification of soft-bodied and microturbellarians. We also discuss the opportu- nities and pitfalls of (meta)barcoding studies as a means of overcoming the taxonomic impediment. Guest editors: Nabil Majdi, Jenny M. Schmid-Araya & Walter Traunspurger / Patterns and Processes of Meiofauna in Finally, we discuss the importance of rouphozoans in Freshwater Ecosystems. aquatic ecosystems and provide future research direc- tions to fill in crucial gaps in the biology of these Electronic supplementary material The online version of organisms needed for understanding their basic role in this article (https://doi.org/10.1007/s10750-020-04287-x) con- tains supplementary material, which is available to authorized the ecology of benthos and their place in the trophic users. M. Balsamo (&) Á L. Guidi M. A. Todaro Department of Biomolecular Sciences, University of Department of Life Sciences, University of Modena and Urbino, Urbino, Italy Reggio Emilia, Modena, Italy e-mail: [email protected] e-mail: [email protected] L. Guidi B. S. Leander Á N. W. L. Van Steenkiste e-mail: [email protected] Departments of Botany and Zoology, University of British Columbia, Vancouver, BC, Canada T. Artois e-mail: [email protected] Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium N. W. L. Van Steenkiste e-mail: [email protected] e-mail: [email protected] J. P. S. Smith III Department of Biology, Winthrop University, Rock Hill, SC, USA e-mail: [email protected] 123 2614 Hydrobiologia (2020) 847:2613–2644 networks linking micro-, meio-, and macrofauna of studied and are far better known worldwide. Fresh- freshwater ecosystems. water gastrotrichs and microturbellarians not only share a number of morphological and biological traits, Keywords Fresh waters Á Ecology Á Study methods Á but their parent phyla, Gastrotricha and Platy- Taxonomy Á Species diversity helminthes, also recently emerged in a monophyletic clade within the Spiralia called Rouphozoa (Gr. Rouphao, ingesting by sucking; Struck et al., 2014), which was endorsed by two subsequent, independent Introduction phylogenomic studies (Egger et al., 2015; Laumer et al., 2015a). However, Bleidorn (2019) recovered a Meiofauna constitutes a significant reservoir of biodi- clade comprising Nemertea and Platyhelminthes sep- versity in aquatic ecosystems that is often overlooked. arate from the clade of Gastrotricha; thus, it is clear Sediments and vegetation in freshwater habitats, that further molecular and morphological work is including freshwater ponds, lakes, and rivers, but also needed to test the monophyly of the Rouphozoa. The mosses, wet soils and semi-aquatic agricultural duo-gland adhesive system, recently studied in detail ecosystems (e.g., paddy fields), are teeming with for platyhelminthes (Wunderer et al., 2019), was hundreds of thousands, if not millions of poorly known proposed as a possible synapomorphy for both taxa or completely unrecorded species of these micro- (Giribet & Edgecombe, 2019). However, studies of the scopic animals (Giere, 2009). gastrotrich duo-gland system are much older (Tyler & Traditional morphology-based sampling techniques to Rieger, 1980; Ruppert, 1991). Consequently, detailed study biodiversity and ecology of meiofauna are usually molecular studies of the duo-gland system in Gas- addressed towards ecdysozoan taxa such as nematodes trotricha and research to identify other possible and copepods, and have so far failed to account for the synapomorphies within Rouphozoa are sorely needed. sometimes equally abundant and diverse soft-bodied Because of their abundance, small body size and gastrotrichs and meiofaunal flatworms or so-called ‘‘mi- selective micro- and meiophagous feeding behavior, croturbellarians’’(Martens & Schockaert, 1986; Nesteruk, gastrotrichs and microturbellarians most likely play a 2006;Schockaertetal.,2008;Giere,2009). Perhaps more critical role in freshwater trophic networks and ecosys- so than other meiofaunal groups, gastrotrichs and micro- tem dynamics (Palmer et al., 1997; Balsamo & Todaro, turbellarians also exemplify the taxonomic impediment, 2002; Majdi et al., 2019). However, their diversity and including a lack of knowledge on their biodiversity and ecological roles in aquatic ecosystems are still insuffi- organismal biology, a lack of experts and a lack of ciently known. For freshwater gastrotrichs, the results of taxonomic infrastructure. As such, they have lagged the few targeted studies on functional ecology appear behind in species discovery and identification, uncovering controversial (Strayer, 1985; Hummon, 1987; Nesteruk, (cryptic) speciation, biodiversity surveys, population 1996a, 2007b; Schmid-Araya, 1997), and for freshwater genetics, and phylogeography. Traditional morphology- microturbellarians no such studies exist to date. based identification methods are often time-, effort-, and In this study, we aim to give an overview of the resource-intensive, depend on a handful of taxonomic current state of knowledge on the diversity, distribution, experts, and cannot uncover cryptic diversity. As shown and ecology of freshwater rouphozoans. This includes by a few comprehensive studies of single taxa, the current an updated census of species in the various biogeo- number of described species of these two groups in fresh graphical regions, a summary on the importance of waters is significantly lower than the estimated species environmental parameters on biotic interactions and diversity (e.g., Catenulida: Larsson et al., 2008; Micros- habitat preferences, spatial and temporal distribution, tomum: Atherton & Jondelius, 2018, 2019; Gastrotricha: dispersal and trophic ecology of these two groups. We Balsamo et al., 2008). also provide recommendations to overcome method- In this contribution, we will focus on the micro- and ological problems and challenges in qualitative and meiofaunal freshwater representatives of these taxa quantitative collection and identification of these and largely omit the numerous members of the animals, and discuss future research avenues to fill in macrofaunal flatworm group Tricladida, which, crucial gaps in our knowledge on these important because of their large size, have been rather well freshwater animals. 123 Hydrobiologia (2020) 847:2613–2644 2615 Methodologies for sampling and study all the habitats of a single biotope (Heitkamp, 1988). The main criteria for qualitative/quantitative sampling It is clear that in studies of freshwater meiofauna, of microturbellarians and gastrotrichs are summarized Rouphozoa are frequently not considered (Fig. 1). As in Table 1. already noted by some authors (e.g., Traunspurger & Individuals of both groups are more successfully Majdi, 2017), we hypothesize that this is because studied alive in fresh samples than in preserved extraction methods used for these soft-bodied organ- samples, since their body frailty and strong contrac- isms are very different from those used for ecdysozoan tility often cause diagnostic morphological characters taxa. This is further supported by historical studies that to be distorted after fixation (Balsamo & Todaro, recovered large numbers of rouphozoan taxa using 2002, Balsamo et al., 2014). In the laboratory, extraction methods compatible with their preservation collected fresh samples are moved into bowls (e.g., Strayer, 1985; Robertson et al., 2000). Finally, equipped with an aeration system and a lighting neon metabarcoding studies in a marine context routinely tube if also vegetation is present. The bowls are filled recover rouphozoans thought previously to be rare with additional filtered water from the sampling site based solely on morphotaxonomic studies (e.g., (or spring water if necessary) and kept at room Rzeznik-Orignac et al., 2017; Leasi et al., 2018). temperature. Accordingly, we provide up-to-date methods below A comparative summary of methods for extraction for the collection, preservation, and study of roupho- and study of freshwater microturbellarians and gas- zoans (Tables 1, 2). trotrichs is reported in Table 2. Extraction of animals from fresh samples implies direct observation of small Sampling and extraction