Wednesday 6 January 2021

Ichnological evidence for limb-autotomy in Triassic Holocrinids.

Many Animals, including Echinoderms, are able to autotomize parts of their body usually as a defense strategy against predators. It has been argued that shed appendages, which sometimes display vigorous post-autotomy movements, reduce the animal’s mortality in two major ways: (1) they enable the animal to break away from predators that have grasped it, and (2) divert the attention of the predators away from the vulnerable body parts. Crinoids, commonly referred to as Sea Lilies, are a group of Echinoderms that is subject to a high predation pressure, have remarkable ability to autotomize and regenerate their appendages. It has been shown that arm autotomy in these echinoderms is achieved through the nervously mediated (L-Glutamate invoked) destabilisation of collagenous ligamentary fibres at specialized autotomy planes, namely (crypto)syzygial articulations. 

Although considerable effort has been devoted to study autotomy in Crinoids, little attention has been paid to post-autotomy thrashing behaviour. A 2010 study by Iain Wilkie, Alice Barbaglio, William Maclaren, and Maria Candia Carnevali, on living stalkless Comatulids (Feather Stars) only briefly reported that: 'after autotomy induced in both intact Animals and isolated arms, the detached distal portion of the arm showed rhythmical cycles of flexion and extension in the oro–aboral plane'.

In a paper published in the journal Scientific Reports on 15 September 2020, Przemysław Gorzelak of the Institute of Paleobiology of the Polish Academy of Sciences, Mariusz Salamon and Krzysztof Brom of the Faculty of Natural Sciences at the University of Silesia in Katowice, Tatsuo Oji of the University Museum at Nagoya University, Kazumasa Oguri of the Japan Agency for Marine-Earth Science and Technology, Dorota Kołbuk, also of the Institute of Paleobiology of the Polish Academy of Sciences, Marek Dec of the Polish Geological Institute, Tomasz Brachaniec, also of the Faculty of Natural Sciences at the University of Silesia in Katowice, and Thomas Saucède of Biogéosciences at the Université Bourgogne Franche-Comté, further examine thrashing behaviour in extant Sea Lilies, and explore its ichnological potential by conducting neoichnological aquarium experiments using the Stalked Crinoid Metacrinus rotundus, and then analyzed samples with articulated arm fragments of the oldest (Early Triassic) stem-group Isocrinids (Holocrinids) in order to identify evidence of this behaviour in the fossil record.

Specimens of living Stalked Crinoids of Metacrinus rotundus were dredged from a depth of about 140 m in Suruga Bay (near the town of Numazu in Shizuoka Prefecture, Japan) using a 90-cm wide naturalist dredge with a net. Then, the living specimens were transferred to an experimental seawater tank in the Nagoya University Museum. The aquarium was maintained at a constant seawater temperature (roughly 16°C) in darkness and under circulation provided by a water pump. After few weeks of acclimatising the Crinoids, a box (approximately 40 × 30 cm) floored with fine-grained sand was placed, which was smoothed before an autotomised arm was introduced. Neoichnological experiments were repeated several times using different arms from different individuals.

For comparison purposes, a series of aquarium experiments was made on production of transport-induced sole markings left on the sediment surface (fine-grained sand) by isolated dead arms being dragged (with the pinnules facing upstream or downstream) by a current (0.35 cm per second) adjusted by a water pump that was placed at the bottom of the aquarium. At the lower or higher velocity, the arms (which were placed at a distance of about 25 cm from the pump) were not moving or were lifted above the sediment surface, respectively, leaving no traces. These experiments were conducted at the Laboratory of Experimental Taphonomy at the Faculty of Natural Sciences of the University of Silesia in Katowice, Sosnowiec, Poland. Gypsum casts from both experiments are deposited at the Institute of Paleobiology of the Polish Academy of Sciences (ZPALV.42ICH).

A Lower Triassic (lowest Spathian) slab of thin-bedded silty limestone of the Thaynes Group (west of Paris, Idaho, USA) preserving five isolated fragments of arms belonging to one of the oldest (if not the oldest) post-Palaeozoic holocrinid taxon (Holocrinus sp.) deposited in the collection of the Université de Bourgogne, Géologie Dijon, France (UBGD 30564) was investigated. These arm fragments are of different lengths and lack distal arm tips and some distal pinnules.

Following autotomy of the arm, within a few seconds, its activity increased, i.e. it started to thrash mostly in the oral–aboral plane. Both frequency and style of flexions (sluggish writhing and violent flicks) and the duration of movement varied (several hours to up to about 7 days). However, only in the first hours after autotomy, detached arms showed the highest activity. The frequency and amplitude of motions decreased with time; i.e. after several hours autotomised arms remained in place; their activity could still be recorded but they did not produce any traces. In the first hours after autotomy, each autotomized arm produced two major types of traces on the sediment surface, which can be closely associated with each other.

 
Traces produced by autotomised arms of Metacrinus rotundus. (a)–(c) Straight deep grooves arranged in radiating group; (d)–(f) a few sets of straight parallel grooves and furrows inclined at different angles to each other; (g)–(i) two large arched grooves; (j)–(l) small short parallel furrows. (a), (d), (g), (j) Photographs of sediment surface; (b), (e), (h), (k) photographs of gypsum casts; (c), (f), (i), (l) false-colour depth maps of gypsum casts. (m) colour scale of elevation. Large and small arrows indicate deep grooves left by the arm and shallow furrows made by pulling the pinnules along the substrate, respectively. Scale bars are 1 cm. Gorzelak et al. (2020).

The first type comprises straight to slightly arched grooves, 1.5–3 cm long (mean: 2.1 cm), 0.2–0.6 cm wide (mean: 0.3 cm) and about 0.1 cm deep, usually arranged in radiating groups; the grooves may be inclined at different angles to each other (the angles between adjacent grooves ranging from 9° to 28°) and are separated from each other by a distance of 0.9–2.8 cm (measured in the widest distance between two ends of neighbouring grooves). The length-to-width ratio of these grooves ranges from 3.8 to 10.9 (mean: 6.8). These traces were left by a rotating and more or less rhythmic movement of the flicking arm that placed the most pressure on the substrate with its median-distal arm part.

The second type comprises sets of thin and parallel (locally curving) furrows, 0.3–1.7 cm long (mean: 1.1 cm), 0.04–0.17 cm wide (mean: 0.1 cm),  and about 0.03 cm deep; these sets may be inclined at different angles to each other, locally forming a herringbone pattern. The length-to-width ratio of these furrows ranges from 4.1 to 33.6 (mean: 11.4). These traces were made by pulling the pinnules along the substrate.

Current-produced sole markings, resulting from the more or less continuous contact of the arm with the sediment surface, display a very different morphology. These grooves are continuous, long (4–6 cm), generally linear, deep (~ 0.2 to 0.4 cm) and run parallel to the flow direction.

 
Current-induced sole markings (arrows) left on the sediment surface. (a) Photograph of sediment surface; (b) photograph of gypsum cast. Gorzelak et al. (2020).

Close examination of Lower Triassic slabs from the Thaynes Group (Spathian, west of the city of Paris, Idaho, USA) revealed similar traces associated with isolated articulated fragment of arm of Holocrinus sp. Given their size, morphology and close association with the Crinoid arm, it appears that these traces could have been produced by thrashing movements of shed arm. However, the scarcity and imperfect state of preservation make the erection of the new ichnospecies impossible.

 
Possible trace fossils associated with articulated piece of arm of Holocrinus sp. (UBGD 30564; Thaynes Group, Lower Triassic; collection of Université de Bourgogne, Géologie Dijon, France). (a) Slab preserving articulated fragment of arm and associated traces (arrows); a photograph taken using a camera fixed to a tripod. (b) Slab preserving articulated fragment of arm and arched grooves (curved red arrows) arranged in radiating group and a few sets of indistinct straight parallel furrows (straight small red arrows with a question mark) and analogical traces (in dotted circle) produced by autotomised arms of Recent isocrinid; a photograph taken using a camera attached to an optical microscope. (c) False-colour depth map of a slab; (d) false-colour depth map of a slab acquired from photographs taken from binocular microscope (elevation has been increased (× 2) to enhance depth contrast); (e) colour scale of elevation. Scale bars are 1 mm; scale bar in dotted circle is 1 cm. Gorzelak et al. (2020).

One arm fragment is associated with slightly arched grooves, about 1.9 to 3.2 mm long (mean: 2.3), 0.5 to 0.8 mm wide (mean: 0.55), arranged in a radiating group (the angles between adjacent grooves range from 12° to 24°). These grooves are separated from each other by a distance of 1.9–2.6 mm (measured in the widest distance between two ends of neighbouring grooves). Dimensionally, the mean length-to-width ratio of these grooves (4.3) falls well within the range of this ratio for the grooves produced by the median-distal arm part during our neoichnological experiments. These grooves are associated with a few sets of indistinct thin and parallel (locally slightly curving) furrows, 1.8–3.2 mm long (mean: 2.4), 0.07–0.13 mm wide (mean: 0.1) of uncertain origin. Notably, however, the mean length-to-width ratio of these furrows (25.5) falls within the range of this ratio reported in Gorzelak et al.'s neoichnological experiments.

As no ethological term exists for the trace fossils produced by post-autotomy thrashing movements of shed appendages Gorzelak et al. propose a new ethological category, autotomichnia (from the Greek auto- 'self-' and tome 'severing', αὐτοτομία). Although thrashing behaviour occurs in a wide range of Vertebrate and Invertebrate taxa, autotomichnia are probably rare in the fossil record, and its identification is difficult if the traces are not found in association with the 'producer'. Such cases, however, are not likely to be common given that shed appendages displaying movements attract attention of the predators which attempt to consume them. The only ichnospecies ascribed to activity of Crinoids described so far is Krinodromos bentou. This ichnotaxon, however, in contrast to the presently described traces, refers to unusual locomotion trail, and shows different morphology in the form of two bordering grooves combined with pushed sediment piles, and a central flat area or a narrow winding furrow. Possible explanation for the fossil traces reported herein is that they simply represent sole markings produced by a dead arm moved along by a current. However, these Triassic traces bear no morphological resemblance to the experimentally induced abiotic sedimentary structures.

It has been argued that ichnology can provide valuable insights on the evolutionary origins of behaviors and on many of their functional and adaptive aspects. Gorzelak et al.'s experiments showed that autotomised arms of Stalked Crinoids (isocrinids) display vigorous movements similar to that observed in shed arms of Brittlestars. They produce distinct traces on the sediment surface, which may have some potential to be preserved as trace fossils. This finding opened new perspectives for tracing the origin of thrashing behaviour in crinoids. Indeed, Gorzelak et al.'s examination of fossil material from the Thaynes Group suggests that similar traces are associated with isolated articulated fragment of arm of the oldest (approximately 250.6 million years old) stem-group Isocrinids (Holocrinus). The fact that this arm fragment lacks distal arm tip and some distal pinnules is suggestive that it was autotomised due to predatory attack prior to rapid burial rather than another type of disturbance (e.g. storm). It must be emphasised that although abiotic factors (such as high current velocities induced by storms or other environmental trauma) may lead to arm loss, most autotomy in natural settings results from biotic interactions. This is consistent with recent data which showed that the thruster-produced extreme flow or suction force did not lead to arm loss or any other type of injury in deep-water, Stalked Crinoid Democrinus sp.

Trace fossils described by Gorzelak et al. suggest that the origin of thrashing behaviour in Crinoids could be traced back to at least the Early Triassic. The question of whether this behaviour could have appeared in the Palaeozoic Crinoids (independently in several clades or in one lineage and was then inherited by the post-Palaeozoic descendants) is presently unclear. However, it should be emphasised that, in contrast to the highly flexible muscular arms of recent and post-Palaeozoic Crinoids in which syzygial or cryptosyzygial ligamentary articulations specifically designed for autotomy are localised, many Palaeozoic Crinoids possessed primitive arms with limited flexibility. Although regeneration is frequently documented in Palaeozoic Crinoids, most of them, if not all, have not yet developed autotomy planes. This suggests that they lacked autotomy abilities, or at least that they were less specialised in that regard.

The end-Permian mass extinction profoundly influenced the evolutionary history of Crinoids, not only through the demise of major Palaeozoic crinoid groups but also through changes in their functional morphology. Notably, post-Palaeozoic crinoids are considered to have descended from only a single survivor (i.e. a Cladid ancestor, Ampelocrinids). In the Middle Triassic, however, they rebounded and underwent a major radiation resulting in the appearance of several motile taxa showing many anti-predatory morphological and behavioral innovations to increased predation pressure during the Mesozoic Marine Revolution. Holocrinids are among the first Crinoids to appear in the aftermath of the end-Permian Mass Extinction. These Crinoids display many adaptations to benthic and nektonic predators. For instance, they developed specialised rupture points at the distal nodal facets in their stalk, allowing them to free themselves of the sea bottom, crawl with the aid of highly flexible muscular arms and re-attach. Furthermore, they elaborated localised autotomy planes (cryptosyzygies) in the arms, which in Recent Isocrinid descendants greatly reduce mortality and arm damage. Gorzelak et al. suggest that Holocrinids might have also displayed post-autotomy arm thrashing. Interestingly, in some Lizards, it has been observed that their wildly thrashing autotomised tails (in contrast to taxa having a much lower rate of tail thrashing) consistently distract attention of predator away from the escaping Lizard and increase predator-handling time, providing additional opportunity to escape. Intriguingly, however, in some Lacertid Lizards, duration of thrashing between different species, shows little variation, either because it is less costly, or because the underlying physiological pathways are evolutionary conservative. Notwithstanding, the high numbers of shed Lizard tails are commonly found in predator stomachs. All these indicate that caudal autotomy and thrashing behaviour in these Vertebrates is an effective antipredatory strategy. Accordingly, Iain Wilkie argued that thrashing behaviour in Ophiuroids is also likely to be an effective decoy against Fish predators. Consequently, Gorzelak et al. hypothesise that this behaviour in crinoids also probably acts as a defense strategy to distract predator attention, and/or to increase predator handling time, providing additional getaway chances to Crinoids. A moving autotomized arm might itself be sufficient attraction as a food source. Accordingly, acquisition of thrashing behaviour in the Early Triassic Crinoids may underscore the magnitude of the anti-predatory traits that occurred during the Mesozoic Marine Revolution, which had already started soon after the end-Permian extinction. The thrashing behaviour along with the specific arm construction consisting of two types of articulations (muscular ones playing a great role in locomotion and postural changes by maximising arm flexibility, and strictly ligamentary (crypto-)syzygial ones, specifically designed for autotomy) have been maintained in Isocrinid/Comatulid descendants up to the present.

Given the scarcity and imperfect state of preservation of the trace fossils described herein, further ichnological findings are needed to fully test the above hypotheses. Results of neoichnological experiment presented herein highlight the preservation potential of thrashing behaviour of Crinoid arms, thus rock slabs preserving detached Crinoid arms are worthy of in-depth investigation.

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