Experimental taxonomy confirms the environmental stability of morphometric traits in a taxonomically challenging group of microinvertebrates

Abstract

Despite advances in molecular systematics, the taxonomy of tardigrades still depends largely on morphological and morphometric traits. The fact that the variability of any biological trait is determined by the interaction between genetics and environment prompts a very fundamental question: is it possible for tardigrades of the same genotype, but originating from various habitats that differ in environmental conditions, to have phenotypes so different that they would be erroneously classified as different species taxa by means of classical taxonomy? Here, we present the results of a broad and fully controlled laboratory experiment in which we investigated the phenotypic plasticity of a number of traits that are traditionally considered to be taxonomically important. In order to achieve this, we have cultured six tardigrade species belonging to four eutardigrade families (Milnesiidae, Hypsibiidae, Isohypsibiidae, and Macrobiotidae) under five experimental regimes, reflecting key environmental factors that are likely to vary in natural habitats (i.e. temperature and food availability). We then measured a number of key taxonomic traits and compared their dimensions between the treatments. Over two years of experimentation we have obtained more than 28 000 morphometric measurements for over 2300 individuals. Such an extensive data set allowed us to test some of the fundamental assumptions of classic tardigrade taxonomy. We found that in the five parachelan species analysed, the great majority of both absolute and relative traits differed significantly between the treatments, whereas there were no significant differences in the apochelan species. Overall, tardigrades grew largest under the low-temperature treatment, whereas the smallest specimens were observed under high-temperature and low-food regimes. However, the prevalent statistical significance resulted mainly from the considerable statistical power of our analyses, and not from effect sizes, which varied mostly between low and moderate. In other words, the differences, although consistent, were minor in terms of taxonomical significance, and probably would not be considered by classic taxonomists as sufficient to designate animals from different treatments as separate taxa.

Milnesium tardigradum Doyère, 1840: The first integrative study of interpopulation variability in a tardigrade species

“…Thus, it is not certain whether the analyzed populations comprised a single or multiple (cryptic) species, which strongly restricts taxonomic conclusions which can be drawn from such studies. More recent publications, that used genetically verified identifications to investigate phenotypic variability, utilised clonal strains (Kosztyła et al., ; Stec, Gąsiorek, et al., ). Therefore, the analyzed morphological and morphometric variation was limited to phenotypic plasticity induced by environmental factors.…”

Integrative redescription of a common Arctic water bear Pilatobius recamieri (Richters, 1911)

“…In a faunistic survey, Węglarska (1959) described a population of P. recamieri from Southern Poland, in which some specimens had a septulum, whereas others a microplacoid. However, according to current knowledge on the morphological variability in eutardigrades, traits such as microplacoids and septulae are constant within species (e.g., Pilato 1975Pilato , 1981Kosztyła et al 2016). Therefore, either Węglarska (1959) found two similar Pilatobius species in one locality (but see also below) or her observation was erroneous.…”

“…This is especially important in the face of the impact of climate change on Arctic biota and to understand the biogeographical patterns of life affected by these shifts, as some studies suggest that species alter their distributions rather than evolve in response to environmental changes influenced by global warming (Callaghan et al 2004;Hodkinson 2013). However, tardigrade taxonomy is based largely on morphological and morphometric traits (e.g., see Michalczyk and Kaczmarek 2013;Kosztyła et al 2016), and many species descriptions are incomplete and grossly outdated, with molecular data being available for only a small fraction of species (e.g., see Bertolani et al 2014). One such species with a poor diagnosis is Pilatobius recamieri (Richters, 1911), a limnoterrestrial eutardigrade described from and frequently found in the Svalbard Archipelago (Richters 1911;Zawierucha et al 2016a, b).…”

Snapshot of micro-animals and associated biotic and abiotic environmental variables on the edge of the south-west Greenland ice sheet

“…Cryoconite granules are a consortium of archaea, cyanobacteria, heterotrophic bacteria, algae and fungi (Takeuchi et al 2001a(Takeuchi et al , b, 2010Langford et al 2014). In laboratory cultures tardigrades belonging to Hypsibioidea (e.g., genus Pilatobius) feed mainly on algae (e.g., Altiero and Rebecchi 2001;Kosztyła et al 2016). Thus, those granules may be an abundant and stable source of food for invertebrates.…”

“…Among the many studies on cryoconite holes in Greenland (Cook et al 2016;Hodson et al 2010a;Stibal et al 2010) few describe cyanobacteria and algae assemblages (Uetake et al 2010(Uetake et al , 2016Kaczmarek et al 2016). The Klebsormidium genus has been often recorded in extreme Arctic habitats and has a high tolerance to gradients of light, temperature and UVR (Kitzing and Karsten 2015).…”