Tun formation is not a prerequisite for desiccation tolerance in the marine tidal tardigradeEchiniscoides sigismundi

Abstract

The so-called 'tun' state is best known from limno-terrestrial tardigrades and rotifers that rely on this compact body shape for anhydrobiotic survival. Little is known of tun formation in marine species and the evolutionary origin of the state is presently unknown. Here, we investigate desiccation tolerance and tun formation in the marine tidal echiniscoidean tardigrade, Echiniscoides sigismundi (M. Schultze, 1865). Groups of approximately 20 E. sigismundi sampled from Lynaes (Denmark) were dehydrated on filter paper from seawater as well as ultrapurified water and kept for 48 h at 5°C, after which they were rehydrated in seawater. The activity and behaviour of the tardigrades was examined under a light microscope, whereas scanning electron microscopy was used for high-resolution three-dimensional imaging. When dehydrated from seawater, E. sigismundi enters a tun, however, when exposed to ultrapurified water, the tardigrade swells and becomes incapable of movement, and thus incapable of tun formation. Nonetheless, E. sigismundi tolerates being dehydrated from ultrapurified water, revealing an exceptional and unparalleled resilience towards losing structural integrity. Our results confirm previous investigations, which suggest that tun formation relies on a functional musculature. They further suggest that tun formation may have evolved as a response to elevated external pressure rather than desiccation per se.

Data from new taxa inferIsoechiniscoidesgen. nov. and increase the phylogenetic and evolutionary understanding of echiniscoidid tardigrades (Echiniscoidea: Tardigrada)

“…Our preliminary investigations suggest that Isoechiniscoides has lower cryptobiotic abilities than the extremotolerant taxa in Echiniscoides . Species within the Echiniscoides sigismundi ‐complex tolerate extreme environmental stress (Hygum et al ., ). Isoechiniscoides sifae sp.…”

“…Two specimens of this species have, presently, been processed and analysed via scanning electron microscopy, conducted according to Halberg, Jørgensen & Møbjerg () and Hygum et al . (). Twenty‐six slides of material relating to Echiniscoides higginsi from the RMK collection at the Zoological Museum, University of Copenhagen, were consulted for the morphological analyses.…”

“…Cryptobiosis is well known within eutardigrades and echiniscoideans from terrestrial and limnic habitats. However, little is known of the phenomenon among marine echiniscoideans and arthrotardigrades (Jørgensen & Møbjerg, ; Hygum et al ., ). The marine tardigrade family Echiniscoididae (Echiniscoidea) was established in 1980 (Kristensen & Hallas, ), comprising the genera Anisonyches Pollock, and Echiniscoides Plate, following the idea of Pollock ().…”

“…The genus represents the most dominant tardigrades in intertidal habitats, but has also been recorded at 80 m depth (D'Addabbo Gallo et al ., ). Species within Echiniscoides are highly versatile cryptobionts as they may survive freezing, dehydration and extreme osmotic stress (Møbjerg et al ., ; Clausen et al ., ; Hygum et al ., ). Furthermore, Echiniscoides can produce cysts with several layers of cuticle (Clausen et al ., ), a feature better known from the terrestrial eutardigrades (Guidetti et al ., ).…”

Tolerance to Gamma Radiation in the Marine Heterotardigrade, Echiniscoides sigismundi

“…sigismundi is a marine species adapted to tidal habitats with recurrent exposure to dry conditions on barnacle shells, and with a recently documented ability to tolerate complete desiccation (i.e., anhydrobiosis) [21,22]. In contrast to limno-terrestrial tardigrades it can survive desiccation with or without contracting into a so-called “tun” [22]. Thus it must clearly be considered a desiccation-tolerant tardigrade.…”