Vermetidae (Rafinesque, 1815), or worm-snails, are a poorly studied family of marine gastropods despite being common inhabitants of coral reefs and rocky shores (Kloppel et al. 2013). Among this family, the key defining characteristic is the irregularly coiled calcareous shell often embedded in or cemented to the substrate (Spotomo et al. 2012). There are multiple genera within the Vermetidae family, with a total of at least 160 extant species (Golding et al. 2014). Of the genera, Dendropoma (Mörch, 1861) is one of the more recognised groups with almost 40 species characterised by having a well-developed operculum. Dendropoma can be found in intertidal and shallow subtidal zones in both tropical and warm temperate areas (Keen 1961). A species of Dendropoma that can be found in Australian waters is Dendropoma platypus (Mörch, 1861).  

Three Dendropoma platypus specimens were identified on a piece of coral rubble obtained from the University of Queensland aquarium system. Specimen 1 was kept alive to examine the live characteristics and behaviour. Specimen 2 was used to examine the teleoconch (shell) and operculum. Specimen 3 was removed from the teleoconch, preserved in ethanol and dissected to examine the internal anatomy. These specimens were identified using mainly the characteristics of the operculum, the origin of coral rubble and some morphological features. 

Teleoconch

The teleoconch, or adult shell, is often embedded into or cemented on the substrate with the surface being encrusted by algae and other encrusting fauna. As such, most vermetid identifications do not rely on the characteristics of the teleoconch and require different descriptions of the soft body, larvae development or habitat to be used as well (Hadfield et al. 1972). The teleoconch of specimen 1 was embedded in the coral rubble and was heavily encrusted with only a section of the teleoconch visible on the surface of the substrate (figure 1). The teleoconch of specimen 2 was also embedded within the coral rubble and was removed from the substrate to reveal the shell characteristics. 

The teleoconch of specimen 2 was semi-opaque with brown markings on the dorsal surface (both interiorly and exteriorly (figure 2). It had approximately four whorls, the largest being 12mm in diameter and the smallest being less than 5mm. The aperture was approximately 5mm in diameter (figure 3; please note that during the process of removing the shell, the original aperture was broken).


Operculum

Dendropoma platypus are a species of Dendropoma with an operculum that has a concave shape and a small interior central mammilla (Golding et al. 2014; figure 4). The operculum of specimens 2 and 3 were circular in shape and had the concave characteristic as well a central mammilla on the interior of the operculum (figure 5, top row). The operculum of specimen 2 was not heavily encrusted, whereas specimen 3’s was heavily encrusted (figure 5, bottom row). While not pictured here, the operculum of specimen 1 was also heavily encrusted. The operculum itself, was semi-transparent and was light brown to golden in colour. Where the operculum was attached to D. platypus (the mammilla), the colour progressed from a light brown to a dark red. The operculum for both specimens were approximately 5mm in diameter, which corresponds with the aperture diameter. In addition, when attached to the vermetid, the operculum was larger than the foot of the animal. 


External Morphology of Soft Body

The only component of the soft body that was visible while the vermetid was alive and active was the head/foot region. Dendropoma platypus can be distinguished by having a dark coloured (black) head/foot with small white and yellow specks (Hadfield et al. 1972). All three specimens of D. platypus had a black head/foot region with small white spots (figure 1 shows the head/foot of specimen 1). When alive, the cephalic tentacles were extended, however when observing the preserved specimen, the tentacles had shortened drastically and were knob like on the sides of the head. 

Diet

Similar to other Dendropoma species, D. platypus are suspension feeders and feed on any particles, detritus and small planktonic organisms that are found in their immediate surroundings (Hadfield et al. 1972; Kloppel et al. 2013). By using a combination of mucus nets and their gill (ctenidial) cilia, Dendropoma are able to capture and filter their food. Dendropoma platypus specimen 1 was observed producing this mucus net on multiple occasions. Particles of algae and sediment were seen attached to the strands (figure 6 and figure 7). Dendropoma species retrieve the contents of the mucus net by using their radula (Hopper 1981). 


Mucus net

Past studies have suggested that Dendropoma mucus nets appear to have a detrimental effect on the immediate surroundings (Kloppel et al. 2013; Shima et al. 2013). The mucus is comprised of mucopolysaccharides and glycosylated proteins (Kloppel et al. 2013). Many have suggested that there is an underlying mechanism or component associated with the extruded mucus nets that affect corals negatively. Coles and Strathmann (1973) proposed that there are bioactive secondary metabolites in extruded mucus and this have been followed up by studies which have showed that there are bioactive substances in certain Dendropoma species and their mucus (Kloppel et al. 2013). While not much is known about the mucus nets of Dendropoma platypus, it would be interesting to conduct a study to determine if this species had bioactive metabolites present. This type of research has important implications for the pharmaceutical industry as marine invertebrates are known to be some of the most effective sources of bioactive secondary metabolites (Kloppel et al. 2013).


Predators

Dendropoma platypus does not have any known predators, however within the genus that it belongs to, there are a number of predators that are associated with other Dendropoma species. For example, a species of guard crab, Trapezid serenei, has been shown to consume the mucus nets that are produced by Dendropoma (Kloppel et al. 2013). While this is not directly harming/preying upon the Dendropoma species, removing the mucus nets essentially removes the vermetid’s ability to capture food. A more direct form of predation involves another gastropod consuming a Dendropoma species. Muricid gastropods have been observed feeding on Dendropoma maximum individuals and then depositing their eggs into the empty Dendropoma shells (Brown et al. 2014). 


Interactions with other marine invertebrates

While examining the different specimens on the coral rubble, it was observed that small and slender polychaetes were found amongst crevices on the surface created by the teleoconch of Dendropoma platypus. This suggests that in their natural habitat, D. platypus can provide microhabitats or protective shelter for much smaller marine invertebrates. While D. platypus has not been known to be a part of reef building, other Dendropoma species have been considered important ecosystem engineers as they form structures which facilitate local diversity of various marine animals such as fish, polychaetes and other molluscs (Golding et al. 2014). 

Dendropoma platypus is non-gregarious, and does not form large species specific colonies like many other Dendropoma species. However, D. platypus have occasionally been found attached to or amongst an aggregate of other Dendropoma species such as Dendropoma gregarium (Golding et al. 2014). 

Brooding and larvae

Dendropoma platypus populations are able to reproduce year round, with different individuals reproducing at different times of the year (Hopper 1981). They are able to produce a few, non-overlapping broods per year. The brood size is often larger than some other Dendropoma species’ brood sizes and females will mature at a larger size than some other species as well (Hopper 1981). D. platypus females can brood at least five capsules in the mantle cavity at any given time (Hadfield et al. 1972). 

The capsules are round in shape with two membrane layers and a gelatinous matrix. The capsules are approximately 3mm in diameter and can contain as many as 70 embryos during the hatching stage (Hadfield et al. 1972). This is made possible as during embryonic development, the capsule becomes flexible and expands as yolk is consumed and the gelatinous matrix reduces in size, creating more room for embryos.

Dendropoma produce both planktonic veliger larvae and crawling larvae. However, D. platypus have only been observed (in laboratory conditions) to produce crawling larvae (Hadfield et al. 1972). There are reports however, of veliger larvae being captured by plankton tows but this is not confirmed (Golding et al. 2014).

Upon hatching, larvae can be as small as 0.68mm x 0.53mm in size with a small unpigmented protoconch (larval shell) with approximately 1 ½ whorls (Golding et al. 2014). Dendropoma platypus is the only ‘concave operculate’ species of Dendropoma to have a protoconch with tall axial ribs that are spaced widely apart (Hadfield et al. 1972). This a key characteristic as other ‘convex operculate’ species of Dendropoma have axial ribs that are short and are spaced close to one another (figure 8). The larval operculum has an orange centre and the larval foot is often identified by its yellow pigment (Hadfield et al. 1972). 

Mini Project: Dissection

To further understand and gather a clearer image of what the internal components of Dendropoma platypus looked like, a dissection was carried out. 

Upon removal of the Dendropoma platypus specimen from the teleoconch, it was discovered that the mantle region was swollen (figure 10). It was suggested that it could have been caused by parasites, however when the specimen was dissected, there were no visible signs of parasitism. It is not known why the specimen had a swollen mantle region. 

The specimen used was stored in ethanol for up to a week before the dissection occurred. During this time, it had lost a little colour around the head/foot region and the body had turned slightly green. The specimen measured approximately 25mm in length from anterior to posterior. The specimen was clearly divided into three regions - head/foot, mantle and a visceral mass. 


Head/Foot region

The operculum was removed, however it would have been attached in the groove/dimple of the vermetid (GrO in figure 10). The foot of D. platypus is much fleshier than the rest of the head/foot region. While not examined in this specimen, the radula of D. platypus has a length of up to 3mm, with 53 rows of teeth. Outer marginal teeth are present and two cusps are present on the inner side (Golding et al. 2014). The head/foot region comprised of 1/10 of the specimen. 


Mantle region

Dissection of the D. platypus specimen was carried out on the ventral surface. An incision was made along the mantle region and the tissue was pulled back revealing various organs and other tissues underneath. The mantle region (including the swollen area) took up 5/10 of the specimen. 

The first noticeable organ was the single gill (ctenidia) located in the left portion of the mantle cavity (Gi in figure 11 and figure 13). There were approximately 16 leaflets per mm, and each leaflet was approximately 1mm in length. An osphradium was located along the gill (Os in figure 11). To the right of the mantle cavity was the rectum, which extended along the length of mantle cavity (Re in figure 11 and figure 12). Toward the posterior end of the mantle cavity, connected to the rectum were the intestines (In in figure 11 and figure 12). Beside the rectum were organs that were presumably components of the male reproductive system - the accessory gland and the vas deferens (AcG and VaD in figure 11 and figure 12). As a result, it was determined that this specimen was of a male Dendropoma platypus. From this dissection, it was clear that many of the vital components of Dendropoma platypus were located in the mantle region. 


Visceral mass

This section of the specimen was very loosely coiled when removed from the teleoconch. After a week in ethanol, it had straightened out a little bit (figure 11). Within this region, the colouration of the body varied from black blotches to pale brown (before storage). This region was also relatively transparent, as many different tissues and vesicles were seen through the epithelium. The testes were located in the very posterior end of the specimen (Te in figure 11 and figure 12).

Dendropoma platypus can be found in intertidal areas that are subjected to strong tidal activity and in areas with depths of 10m or more (Hadfield et al. 1972). In addition to this, they are also often found in shallow coral reefs where encrusting coralline algae is present and tidal changes are frequent. Among literature pertaining to Dendropoma platypus, specimens were found in Brazil, Hawaii, Heron Island (Australia) and in French Polynesia (Hadfield et al. 1972; Hopper 1981; Golding et al. 2014). This species as well as other Dendropoma species are commonly found in tropical and warm temperature regions of the world. 

Evolution

While there is little information about Dendropoma species specifically in regards to evolution, there are some resources available on the evolution and fossil record of Vermetidae. Vermetidae have a fossil record that extends back to the Late Cretaceous, more than 65 million years ago (Rawlings et al. 2010). The vermetids are a part of the caenogastropods, which began to radiate at approximately the same time, in the early Cenozoic Era. The caenogastropods are a taxonomic clade which comprises predominantly of marine gastropods with a small number of terrestrial and aquatic gastropods. Mitochondrial genomic analysis suggests that the Vermetidae exhibit a number of derived changes in gene sequence/coding that can also be found in other members of the Caenogastropoda (Rawlings et al. 2010). In addition, multiple changes associated with genomic order have occurred within Vermetidae, and based on molecular dating, this occurred within the past 38 million years (Rawlings et al. 2001).


Systematics

Through molecular phylogenetic analysis, it was determined that the species within the genus Dendropoma forms a well-supported monophyletic clade (Golding et al. 2014). In the past, this genus has been known as Siphonium Mörch, 1859 (and as such, Dendropoma platypus was known as Siphonium platypus). However, this genus was synonymised by Keen in 1961, who reclassified it as Dendropoma Mörch, 1961. The type species designated by Keen for this genus is Dendropoma lituella Mörch, 1961. 

Knowledge of systematics among other aspects associated with the family Vermetidae are becoming more important to various fields of research such as paleoclimatology. Various vermetid genera are important for understanding past sea temperatures, sea levels and productivity and as such, can be useful tools for predicting future climatic changes (Golding et al. 2014). 

The current status of Dendropoma platypus is unknown, however, many vermetid species can be considered threatened by the changing conditions of the ocean.  

With ocean acidification, many calcifying marine animals are unable to create shells, and this can often lead to the inability to settle and eventually lead to mortality. Experiments performed on other Dendropoma species found that sites with increased acidification yielded significantly lower numbers of settled recruits (Milazzo et al. 2014). By extrapolating from this study and considering that it is a shelled gastropod, it can be assumed that Dendropoma platypus has the potential to be affected by ocean acidification. 

Brown AL, Zill J, Frazer TK, Osenberg CW (2014) Death and life: muricid snails consume the vermetid gastropod, Dendropoma maximum, and use empty shells for reproduction. Coral Reefs 33 [doi: 10.1007/s00338-014-1141-6].

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Golding RE, Bieler R, Rawlings TA, Collins TM (2014) Deconstructing Dendropoma: a systematic revision of a world-wide worm-snail group, with descriptions of new genera. Malacologia 57: 1-97.

Hadfield MG, Kay EA, Gillette MU, Lloyd MC (1972) The Vermetidae (Mollusca: Gastropoda) of the Hawaiian Islands. Mar Biol 12: 81-98.

Hopper CN (1981) The ecology and reproductive biology of some Hawaiian vermetid gastropods. Ph.D. thesis, University of Hawaii, p 39.

Keen AM (1961) A proposed reclassification of the gastropod family Vermetidae. Bull Br Mus (Natural History), Zoology 7: 181-213.

Kloppel A, Brummer F, Schwabe D, Morlock G (2013) Detection of bioactive compounds in the mucus nets of Dendropoma maxima, Sowerby 1825 (Prosobranch Gastropod Vermetidae, Mollusca). J Mar Biol 2013 [doi: 10.1155/2013/283506].

Milazzo M, Rodolfo-Metalpa R, Chan VBS, Fine M, Alessi C, Thiyagarajan V, Hall-Spencer JM, Chemello R (2014) Ocean acidification impairs vermetid reed recruitment. Scientific Reports 4 [doi: 10.1038/srep04189].

Rawlings TA, Collins TM, Bieler R (2001) A major mitochondrial gene rearrangement among closely related species. Mol Biol Evol 18: 1604-1609.

Shima JS, Phillips NE, Osenberg CW (2013) Consistent deleterious effects of vermetid gastropods on coral performance. J Exp Mar Bio Ecol 439: 1-6.

Spotomo P, Tamega FTS, Bemvenuti CE (2012) An overview of the recent vermetids (Gastropoda: Vermetidae) from Brazil. Strombus 19: 1-8. 



All photos were taken by Berilin Duong (unless stated otherwise).