Synonomised Taxa: Turbo nivosa (Reeve, 1848)

• Phylum: Mollusca
• Class: Gastropoda
• Order: Archaeogastropoda
• Clade: Vetigastropoda
• Superfamily: Trochoidea
• Family: Turbinidae
• Subfamily: Turbininae
• Genus: Turbo
• Subgenus: Marmarostoma
• Species: T. tuberculosus

APPEARANCE

The shell of Turbo tuberculosus varies among 17-40 mm. It presents a imperforate and ventricose shell which has subovate-turreted shape. The five whorls are convex and longitudinally slightly striated. Its colour pattern is brown or dark yellow presenting green and black parts. The rounded aperture is white. Something really characteristic of its shell is that a few whorls are covered with rough prickles (Quoy and Gaimard, 1834).

SIZE

Turbo tuberculosus (Family Turbinidae) belongs to the genus Turbo where shells are between 20 and 200 mm diameter in size are found (Alf and Kreipl, 2015). This specie is a medium-sized sea snail whose shell length varies among 17 and 40 mm, being between the smaller species of this genus.

Three individuals of Turbo tuberculosus were collected from the aquarium holding facility at the School of Biological Sciences (The University of Queensland,Australia). The length of the central axis and the diameter of the operculum were measured in the three specimens.

• Specimen 1: length central axis = 23 mm / operculum diameter = 13 mm
• Specimen 2: length central axis = 22 mm / operculum diameter = 14 mm
• Specimen 3: length central axis = 22 mm / operculum diameter = 14 mm

The average length of their central axis was 23 mm while the average diameter of the operculum was 13.6 mm.

The weight of the three individuals was also measured using a laboratory weighing scale.

• Specimen 1: weight = 4.13 g
• Specimen 2: weight = 4.18 g
• Specimen 3: weight = 3.99 g

 The average weight was 4.1 g

IDENTIFICATION

TOXICITY

A number of toxic animals have been reported to occur in coral reef areas. Some of these animals are known or suspected to obtain their toxins from the organisms that are part of their diets. Seafood products are important either in a nutritional and economical point of view. However, human intoxication as a consequence from the ingestion of shellfish occurs worldwide. Several studies have reported diseases produced by these organisms, and some of them are related to species from the genus Turbo.

In Japan, the gastropod Turbo argyrostoma is eaten after removal of the viscera, which causes intoxication. Yasumoto and coworkers studied the toxic components of Turbo marmorata (1974). The ocurrence of several toxins found in the turban shell of this specie inspired the investigation of these toxins in other species associated with coral reefs (Cimino and Gavagnin, 2006).

In Marcus Island (Japan), a research was  carried out to confirm if the toxins contained in the shell of Turbo argyrostoma could cause occasional poisoning resembling ciguatera, which is a foodborne illness caused by eating certain reef fish whose flesh is contaminated with a toxin made by dinoflagellates that live intropical and subtropical water. Ciguatoxin, scaritoxin and maitotoxin were found as the toxins present in the turban shell supporting clinical symptoms related to ciguatera in humans. As was indicated in previous investigations, individuals of this species are grazers on the coral bed so they collect avariety of toxins produced by benthic organisms, especially in this area, endemic to ciguatera, associated to Marcus Island (Yasumoto and Kanno, 1976).

Toxic compounds were found, in a study also carried out in 1976 (Okinawa, Japan), from another specie of this genus, Turbo marmorata, together with Turbo argyrostoma and other two species of gastropods. Distribution of the toxins in the different parts of the body was assessed and high toxicity was found in Turbo marmorata, especially in those visceral parts that are removed before the individuals are eaten. A prohibition to prevent outbeaks of poisoning was establish in Okinawa as a consequence of this results. Feeding habits (grazer) were the main reason of the presence of specific toxins and toxicity may be variable depending on the location and time of catch (Kanno et al. 1976).

Toxic compounds in gastropods have been studied mainly in Asia due to the importance of this organisms in the food industry. Nevertheless, the number of investigations has increased over thelast 15-20 years and it seems that the study of natural resources may lead to the further discovery of novel bioactive compounds. A better understanding to clarify the structure activity and function of these compounds is needed for developing more ambitious projects and contribute a deeper understanding of their roles in nature. I suggest that a good beginning would be to focus studies on benthic organisms of the coral reefs where there is also a high density of toxic species of gastropods, especially in those areas where not many studies have been done before. In this way, it is likely to find a variety of toxins not encountered previously.

HUMAN USES

NUTRITIONAL VALUE

DIET

Species from genus Turbo are grazers which consumes algae on the rock surface or the coral bed. The rasped and scraped offrocks and coral surfaces using their radula that is a specialized feeding organ within the mouth (Grange, 1976).

Due to their feeding system, some species that graze on coral beds might collect a variety of toxins produced by benthic organisms (Yasumoto and Kanno, 1976). This indicates that feeding habits can be the main reason of finding toxic species within this genus. However, this kind of information is mostly found in studies performed in Asia, where the use of this species as food resource is more common.

An experiment was performed by Foster (1999) to determine the effect of diet on growth rate and reproductive fitness of the South African gastropod Turbo sarmaticus. It was observed that coralline algae had a low nutritional value to this species. Moreover, dramatic changes were caused, in the previous year, in intertidal community which produce a domination by coralline algae in the habitat of this specie. For this reasons, it was decided to evaluate the dietary value of macroalgal species commonly consumed by T. sarmaticus.

The results showed that the best growth rate and reproductive fitness were reached when this species was feed on monospecific diet or mixed diet. On the other hand, specimen fed a diet with coralline algae decreased their growth rate and reproductive success (Foster et al. 1999). Therefore, this study showed the importance of assessing both growth rate and reproductive outpu twhen the effects of diet on biology of herbivores is examined.

REPRODUCTION

It was not possible to find information or studies specifically related to Turbo tuberculosus reproduction. However, a study carried out by Joll (1980), with two different species, endemic of Australia, from the genus Turbo (familyTurbinidae), found out that those species were gonochoristic and both of them spawned their eggs to the plankton. The gonochorists produce both sperm and eggs and have a single functional reproductive system (male or female). It was also discovered that was not a resting phase in the reproductive cycle so the gametogenesis was continuous over the year. Besides, family Turbinidae belongs to a taxonomic subclass of sea snails called Prosobranchia and 97 % of its species are gonochoristic (Chase, 2002). Therefore, taking all this background into consideration, it seems that Turbotuberculosus is gonochoristic.

In prosobranchs which belongs to clade Vetigastropoda, like family Turbinidae, the tubules of the male gonad join a duct located in the right kidney and the sperm is released to the sea water through this duct. In the case of females, they have a similar system where eggs are released one by one in a gelatinous covering.  The synchronization between releasing of male and female gametes, and gamete fusion is controlled by pheromones (Chase,2002).

LOCOMOTION

A large muscular foot is used by Turbo tuberculosus for locomotion along its habitat. The foot composes, together with the head, the part of the body that can be extended out of the shell and this usually happens when the snail is crawling around. The foot can be retractable into the shell by the aid of a muscle called rectractor muscle (Stachowitsch, 1992). Ciliary locomotion is used by nearly all “prosobranchs“(species belonging to taxonomic subclass Prosobranchia). The locomotion occurs by crawling thanks to the cilia that are present along the foot surface (Chase, 2002). In this way, the movement produce by the muscular foot is propelled by both cilia and waves of muscular contractions on the sole of the foot (Colin and Arneson, 1995).

CENTRAL NERVOUS SYSTEM AND SENSORY ORGANS

The central nervous system of gastropods is formed by pairs of buccal ganglia, cerebral ganglia, pleural ganglia and pedal ganglia, together with a visceral ganglia which can be found single or paired. These ganglia differ in appearance in different taxa and also additional ganglia might appear in some specific species. They are connected to each otherby commissural nerves, except for the pleurals and intestinals. However, the pleural ganglia are linked to the intestinal ganglia forming the visceral loop. Long connective nerves are also present, in the central nervous system of gastropods, linking certain ganglia (Chase, 2002).

Gastropods perception of their environmen is limited because their world has no sounds, and in most cases, no sights neither. Despite they have eyes, only some species are able to recognize objects. This recognition, and the interpretation of the environmental signs, depends on a combination of chemoreception, mechanoreception and, in the case of those species that have eyes (as Turbo tuberculosus) photoreception as well.

Chemoreception has a great influence in several behaviours of gastropods, such as feeding, homing, aggregation, mating, escape and avoidance. Two types of chemoreceptors can be identified. The ones related to the identification of contacted objects (gustation) and those specialized for the perception of distant chemical resources (olfatation)(Croll, 1983). Mechanoreception is also involved in important roles like defensive behaviours, orienting the animal to wind and air currents, sensing position of mating partner, and locating food objects. Finally, photoreception is only available in those species that have a pair of eyes which are located at the bases of tentacles (mostly) or at the tips of retractable tentacles. These eyes are able to detect light and contain photoreceptors (simple distinction between light and dark).

EXTERNAL MORPHOLOGY

The shell of gastropods is a hollow cone coiled around a central axis called columnella. The aperture is a large opening at the base of the cone through which the head and the foot are extended or retracted. The outside edge is the outer lip and the edge lying against the rest of the shell is the inner lip. It is common to find in many species that the anterior margin of the shell aperture is indented to form a siphonal notch, or drawn out as a siphonal canal. However, in the case ofturban shells, a shiponal notch or canal is not present.

A whorl is each coil of the cone around the columnella. The outermost whorl at the base of the cone is the body whorl. It is the largest of the whorls and contains most of the visceral part of the body, including the head and food.  The rest of the whorls together form a spire that rises above the body whorl and includes the apex.

As we can see in the picture of Turbo Tuberculosus, a characteristic feature of its shell is that a few whorls are tuberculate or covered with rather rough prickles.

The above information was retrieved from Ruppert, E., Fox, R. and Barnes, R. (2004). Invertebrate Zoology: A Functional Evolutionary Approach. Brooks/Cole, Belmont,CA, USA.

INTERNAL MORPHOLOGY

It was not possible to check out the internal anatomy of Turbo tuberculosus. Anyway, understand the general patterns of internal anatomy in gastropods is interesting and useful to know how this animals works internally.

The shell of the first monoplacophoran did not have a room for expansion of the visceral mass to accommodate an enlarged gonad or digestive system (low profile of the shell). In the monoplacophoran that preceded the gastropods, progastropods, the shell increased and the size of the aperture decreased which provided space to expansion of soft tissues, especially visceral mass. Besides, associated with the increase in height of the shell came the flexure of the gut. This allows to moves the gut and associated viscera away from the longitudinal head-foot axis and up into the shell (Rupert et al. 2004)

Another important characteristic of their anatomy is the torsion. The torsion is the single most distinguish characteristic of the gastropods. Torsion refers to twisting of the body. The body plan of all modern gastropods includes torsion during some stage of their development.

An important consequence of torsion was the displacement of many interior organs. For instance, before this trait appeared, the two heart auricles were located posterior to the ventricle, but after torsion they lay anterior to the ventricle. Due to this, the digestive tract became U-shaped and some ganglia from the nervous system moved to new positions causing that nervous system acquires a twisted appearance (Chase, 2002). Despite of the importance of torsion, authorities still disagree about why torsion occurred.

About the body plan, molluscs have a thin layer of tissue called the mantle. The mantle covers the body organs, which are located in the visceral mass. Between the soft body and the mantle there is a space called the mantle cavity. The gills are located here. Gills are organs in which carbon dioxide from the mollusc is exchanged for oxygen in the water.

The mantle also protects the body if the mollusc does not have a shell. The shell is secreted from the mantle. The shell is made up of several layers. The inside layer is the smoothest but it is usually the thickest layer. The inside layer protects the body.

Most molluscs have a well-developed head with mouth and sensory organs. The foot is muscular (located in the underside of the mollusc) and is used mainly for locomotion, but also for capturing prey for food and attachment to the substratum.

Radula is a feature that is seen only in molluscs. It is an anatomical structure, located in the mouth, used for feeding (not found in Bivalvia). Its structure ranges from simple tongue like ones to scrape algae off rocks to complex harpoon-like ones seen in the cone snails.

The coelom is haemocoel-quite reduced (haemocoel for internal transport) and found near and around the heart and as cavities around the excretory (nephridium) and reproductive organs (gonads).

The gut involves a complete digestive tract with mouth and anus. The gut is regionalised with digestive ceca and the radula is located in the anterior buccal cavity.

The above information (only information about the body plan) was retrieved from Ruppert, E., Fox, R. and Barnes, R. (2004). Invertebrate Zoology: A Functional Evolutionary Approach. Brooks/Cole, Belmont,CA, USA.

FOSSIL HISTORY

The phylum Mollusca originated in the late Precambrian period or early Cambrian period about 600 million years ago. Within this phylum, gastropods originated in the early Cambrian period about 550 million years ago (Chase, 2002).

Currently, the Indo-West Pacific region (IWP) contains one of the highest levels of biodiversity of shallow water marine invertebrates. The origin of the biodiversity in this region was due to a combination of several processes as a consequence of tectonic events. Within this processes, vicariance and temperature changes were the most importantones (Williams, 2007).

The highest diversity of family Turbinidae is found in the Indo-West Pacific region. Turban shells are well represented in the fossil record, specially those species from genus Turbo. However, there is still a lack of documentation so taxonomic assignment is not completely reliable.

Recent studies have suggested that the present IWP species from genus Turbo are the result of a radiation in situ. This is based on the fact that the closure of the Tethys sea took place when a land barrier, that was separating the proto-Mediterranean sea from the IWP, closed about 19 million years ago. Within genus Turbo, well-preserved fossils exist for the subgenus Marmarastoma. Current distribution and ocurrence of this subgenus is limited to the IWP. It is specially well represented in the central IWP centre of diversity where coral diversification was more successful. The emergence of Marmarastomais associated to a significant increase in diversification rate that took place 24 million years ago. This time corresponds to the time where the collision of Australia and New Guinea with South-East Asia happened, about 25million years ago. This event probably led to the creation of new shallow-water habitats in the central IWP. At the same time, in the last 20-25 million years,there has been a period of reef building coral diversification. Therefore, taking all this factors into consideration, it is assumed that the subgenus Marmarastoma diversified within the Indo-West Pacific region after the appearance of novel shallow-water habitats and the increased of coral reefs (William, 2007).

PHYLOGENETICS

A phylogenetic analysis was carried out by Williams (2007) in order to assess the evolutionary history of gastropods from family Turbinidae in the Indo-West Pacific region (IWP).  Analyses indicated that all species from genus Turbo form a single clade approximately 68 million years in age. The results showed the Indo-West biogeographical region is acting as a cradle of diversity (with new species originating in situ) and a museum of diversity (with maintained lineages).

Bayesian and parsimony analyses were also carried out in that study. Thanks to these analyses, five clades were recovered for subfamily Turbininae. Furthermore, the temperate regime (tropical or temperate) of each species was mapped using parsimony. Based on this, it was suggested that, in at least four of the clades, temperate habitat is anancestral character.  Bayesian reconstruction of ancestral states also backed up this result.

The molecular phylogeny of this study was used in another one, performed by Vermeij and Williams (2007), to compare opercular characteristics of Turbininae. This comparison showed that operculum in shallow-water clades (where genu Turbo is included) is thicker. This result suggested that a thicker operculum is a selective advantage in shallow-water, tropical environments where crushing predators like crabs are most diverse (Williams and Ozawa, 2006; Vermeij and Williams, 2007; Williams 2008).