First live records of the ruby seadragon (Phyllopteryx dewysea, Syngnathidae)

The documentation of living ruby seadragons at more than 50 m depth confirms that these fish live at deeper depths than leafy and common seadragons and in a very different habitat. Leafy seadragons occur along the coast of Western and South Australia from south of Perth to east of Adelaide and are generally found in depths from 3 to 25 m near brown algae, seagrass, and sand (Kuiter 2000; Stiller et al. 2017; Connolly et al. 2002a). Leafy seadragons are known from as deep as 30 m and with a reddish coloration (Kuiter 2000). Ultrasonic tracking of leafy seadragons showed that they stay over Posidonia seagrass, macroalgae-covered reefs and sand, but seemed to avoid Amphibolis seagrass and boulders with brown algae (Connolly et al. 2002b). Common seadragons have wider geographic range, extending east to the central New South Wales coast and also around Tasmania (Wilson et al. 2016). They show a similar depth preference to leafy seadragons and are also known for living associated with rocky reefs, sand patches, kelp and seagrass (Kuiter 2000; Sanchez-Camara and Booth 2004). The video results for the ruby seadragon clearly show that these fish live in a very different habitat compared to their relatives. They also lack dermal appendages as opposed to the prominent appendages of leafy and common seadragons. In the sparse habitat they occupy, appendages would serve little purpose as camouflaging agents and could add significant costs in drag or fluid resistance, particularly in strong surge. It appears that at these low-light depths, an efficient camouflage strategy for ruby seadragons is to rely on cryptic red coloration.

Surprisingly, we also saw that the ruby seadragon has what appears to be a prehensile tail. Although neither fish was observed to use it in a direct hold, the conditions on the day were relatively calm. The fish would often be exposed to much stronger surge, and then may well use their tails to stop from being swept off the very limited reefal habitats. A prehensile tail is found across a range of Syngnathidae and appears to have evolved at least five times from an ancestral state where the tail possessed a tail fin (Neutens et al. 2014). With regards to seadragons, the phylogeny and transformation for tail shown by Neutens et al. (2014) shows the leafy and common seadragon as a clade tail lacking a tail fin and without grasping capacities. This condition was reasonably interpreted as a single loss of prehensile ability by Neutens et al. (2014) since pipehorses (Solegnathus and Syngnathoides) have prehensile tails and are the closest relatives of the seadragon clade. In these pipehorses, the ability to curl the tail appears to be facilitated by a reduction of the plates, either ventrally (Solegnathus) or entirely (Syngnathoides) (Neutens et al. 2014). The ruby seadragon holotype (Stiller et al. 2015) lacks the very tip of the tail (ca. 1 cm) and so the available microCT scan cannot detect this. Nonetheless, the plates do not appear to be reduced as in pipehorses and all rows seem to be present along the tail in the ruby seadragon.

The discovery that the ruby seadragon has a prehensile tail complicates the scenario of the evolution of prehensile tails in this group, as it is the closest relative to the common seadragon (Stiller et al. 2015), which cannot bend its tail. One parsimonious explanation is that the absence of a prehensile tail in the leafy and common seadragons has independently evolved in each species and that the prehensile tail of the ruby seadragon is a retained plesiomorphic condition. Alternatively, the prehensile tail may have been lost in an ancestor of all seadragons, and the ruby seadragon has re-acquired a prehensile tail. To help choose between these scenarios, detailed observations of leafy and common seadragon tails could be compared to the available microCT scan of the ruby seadragon (Stiller et al. 2015).