Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences

Abstract

Comparative efforts to understand the body plan evolution of stalked jellyfishes are scarce. Most characters, and particularly internal anatomy, have neither been explored for the class Staurozoa, nor broadly applied in its taxonomy and classification. Recently, a molecular phylogenetic hypothesis was derived for Staurozoa, allowing for the first broad histological comparative study of staurozoan taxa. This study uses comparative histology to describe the body plans of nine staurozoan species, inferring functional and evolutionary aspects of internal morphology based on the current phylogeny of Staurozoa. We document rarely-studied structures, such as ostia between radial pockets, intertentacular lobules, gametoducts, pad-like adhesive structures, and white spots of nematocysts (the last four newly proposed putative synapomorphies for Staurozoa). Two different regions of nematogenesis are documented. This work falsifies the view that the peduncle region of stauromedusae only retains polypoid characters; metamorphosis from stauropolyp to stauromedusa occurs both at the apical region (calyx) and basal region (peduncle). Intertentacular lobules, observed previously in only a small number of species, are shown to be widespread. Similarly, gametoducts were documented in all analyzed genera, both in males and females, thereby elucidating gamete release. Finally, ostia connecting adjacent gastric radial pockets appear to be universal for Staurozoa. Detailed histological studies of medusozoan polyps and medusae are necessary to further understand the relationships between staurozoan features and those of other medusozoan cnidarians.

Morphological and molecular diagnostic species characters of Staurozoa (Cnidaria) collected on the coast of Helgoland (German Bight, North Sea)

“…Nevertheless, morphological species identification is still mainly based on these variable macromorphological features, e.g., the shape and dimensions of body parts, numbers of tentacles and gonad vesicles, and patterns of white nematocyst spots (e.g., Miranda et al 2009Miranda et al , 2017Kahn et al 2010). Investigations on internal structures of the arms confirm that this feature, established by Hirano (1997), is important for the species differentiation in the genus Haliclystus Clark, 1863(Miranda et al 2016aHolst and Laakmann 2019). Recent histological studies reveal that internal morphological structures have a high scientific value for systematic and evolutionary studies on staurozoans (Miranda et al 2013(Miranda et al , 2016a but the applicability of this technique is limited to single selected specimens because of the invasive and time-consuming nature of histological sectioning.…”

“…Investigations on internal structures of the arms confirm that this feature, established by Hirano (1997), is important for the species differentiation in the genus Haliclystus Clark, 1863(Miranda et al 2016aHolst and Laakmann 2019). Recent histological studies reveal that internal morphological structures have a high scientific value for systematic and evolutionary studies on staurozoans (Miranda et al 2013(Miranda et al , 2016a but the applicability of this technique is limited to single selected specimens because of the invasive and time-consuming nature of histological sectioning. The taxonomic value of cnidome analyses is considered to be low for staurozoans because the same two nematocyst types were described for several staurozoan species (Fautin 2009).…”

“…(e.g., Clark 1863 as Craterolophus tethys; Mayer 1910 as C. tethys; Kramp 1961). Gonads of stauromedusae are generally organized in vesicles as evaginations of gastrodermis, but in some species, the gonadal content is restricted to a simple layer between gastrodermis and epidermis, without the organization of vesicles (Miranda et al 2016a).…”

Stalked jellyfishes (Cnidaria: Staurozoa) of South Africa, with the description of Calvadosia lewisi sp. nov.

“…Staurozoan species have a unique life cycle consisting of a non-ciliated planula larva that settles on the substratum and develops into a stauropolyp, which subsequently undergoes apical metamorphosis into a stauromedusa, without strobilation or budding (Wietrzykowski 1912;Kikinger & Salvini-Plawen 1995;Miranda et al 2010). Stauromedusae thus possess characters found both in polyp and medusa stages of other medusozoans (Collins et al 2006;Miranda et al 2013Miranda et al , 2016a.…”

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“…These animals have unique life history attributes, including non-ciliated, creeping, larval planulae that develop into polyps, which later undergo metamorphosis (unique from strobilation or budding) into adult stauromedusae (Kikinger and Vonsalviniplawen 1995;Miranda, et al 2013;Wietrzykowski 1912). In addition, the adult staurozoan body plan includes features common to both the polyp and medusa stages of other cnidarians, thus adding to their phylogenetic significance (Collins 2002(Collins , 2010Miranda, et al 2016a;Miranda, et al 2013;Miranda, et al 2016b). The phylogenetic position of staurozoans relative to other medusozoan lineages remains controversial and recent hypotheses (Kayal, et al 2013;Simion, et al 2017;Zapata, et al 2015) present different implications for the evolution of medusozoan body plans ( Figure 1F).…”