The pyramid periwinkle is primarily found on intertidal rocky coastlines in the high shore area, frequently above the height of the highest spring tide (supra-littoral zone, Figure 4) (Berry, 1986; Chapman and Underwood, 1994). The supra-littoral zone is typically very variable throughout space and time due to the variable tides and weather, causing these areas to be thought of as harsh and unpredictable (Chapman 2000a). N. pyramidalis may be exposed for days at a time in this habitat, however this species still relies on moisture or seawater to feed, move and reproduce (Chapman 2000a).

This supra-littoral species feeds on microalgae on rocks in these high shore areas using its radula (Figure 5). Due to the potential for desiccation, N. pyramidalis only feeds when the substrate is wet. Therefore, foraging in these high zones are not necessarily driven by tidal influences, but potentially larger scale patterns pertaining to moisture (Little, 1989). Pyramid periwinkles also display intraspecific and interspecific aggregational behaviours in response to the environment, and these have been discussed in the behavioural section. 

Figure 5: Nodilittorina pyramidalis feeding on microalgae in the supra-littoral zone. 

When I collected specimens of N. pyramidalis from the rocky shore at Moffat Beach (QLD, 4551), I noticed the species appeared to prefer particular substrate types (Figure 6). This observation was similar to Chapman and Underwood’s hypothesis (1994) which found that pyramid periwinkles tend to avoid smooth rocks and simple topographical areas contrary to Austrolittorina unifasciata. In this investigation, the individuals that were translocated to smooth or uncomplex topographical areas quickly migrated to new areas, actively avoiding simples surfaces. Complex topography was not enough to retain individuals in a particular area for an extended period of time and it is likely the food availability is also important to the distribution of the species throughout the intertidal zone (Chapman and Underwood, 1994). I also observed that N. pyramidalis tended to either be on the most exposed surface to the ocean or in crevices within the rock. Again, this observation is similar to an observation posed by Chapman and Underwood (1994). Pits and crevices however had no correlation with distribution of pyramid periwinkles in their investigation, however it is possible that although crevices themselves may not greatly influence distribution, conditions created within the crevice environments are more preferable. For instance, microalgae may have a higher abundance within crevices or temperature and moisture may be more preferable in crevice microenvironments. 

Figure 6: Nodilittorina pyramidalis aggregation inhabiting a pit in the the complex substrate in the supralittoral zone on Moffat Beach, Queensland (4551).

Hypotheses: 

I noticed that the positioning of individuals on the substrate appeared to differ depending on their distance from the low tide water mark at Moffat Beach (QLD, 4551). I hypothesized the proportion of N. pyramidalis in milder environments will increase as the distance from water increases due to increasing need to be nearer the ocean to prevent desiccation, feed and reproduce. Similarly, the proportion of pyramid periwinkles in harsh micro-environments will decrease as you move further from shore. Hence, I conducted a small experiment to determine the distribution of N. pyramidalis throughout micro-habitats on rocky shores. 

Figure 7: Nodilittorina pyramidalis inhabiting shore-ward, side and top of rock at Moffat Beach, Queensland (4551).

Methods:

I randomly selected three approximately fifty metre transects of Moffat Beach from the low tide water mark to where the rocks ended at the hill face. The closest rock to the transect which had N. pyramidalis present was selected every metre. The individuals on each rock surface were counted (as well as the total) and placed into a harsh or mild micro-environment category. Harsh micro-environments consisted of individuals that were either on the top of the substrate or on the landward facing substrate surface. Mild micro-environments consisted of individuals on either the side of the substrate or on the shore-ward facing substrate surface. The proportion of individuals in harsh or mild environments were calculated compared.

Results:

Abundance in general increases from around 40m to about 46m from the low tide mark then decreases as distance increases (Figure 8). There is also a clear increase in the proportion of individuals in milder microhabitats as the distance from the low tide mark increases (R² = 0.77, Figure 9). Similarly, the proportion of individuals in harsher microhabitats decreases as the distance increases (R² = 0.77, Figure 9).

Reproduction and Life Cycle

Nodilittorina pyramidalis is a dioecious species, which means the male and female reproductive organs occur in separate individuals (Underwood, 1974). Males have short penial filament with papillae glands, no glandular disc at the base of the penis and have a singular large malliform gland on the base (Reid and Williams, 2004). The copulatory bursa in females opens near the end of the pallial oviduct which has two loops in the egg groove (Reid and Williams, 2004). After copulation, the sperm is nourished by a nurse cell in the female and transported to the egg where it is internally fertilised (Borkowski, 1971). Nurse cells are likely to be an adaptation within the Littorinidae family for living very high in the intertidal (Reid, 1989).

Planktonic egg capsules are released into the ocean during spawning where they develop into long-lived planktotrophic veliger larvae which feeds on plankton (Borkowski, 1971; Underwood, 1974). The spawning season is from October to March, it is beneficial for spawning to occur during this time because phytoplankton blooms are at their largest, increasing food availability for planktotrophic larvae and improving the likelihood of survival (Underwood, 1974). Spawning in pyramid periwinkles is reliant on their height on the shore, the amount of tidal wetting and critical temperatures, resulting in spawning occurring on average every two weeks with the spring tides (Berry, 1986; Borkowski, 1971). Spawning during spring tides increases dispersal distance of the larvae and this is beneficial because it increases genetic diversity and potentially allows for new habitats to be explored (Berry, 1986). During the spawning season the reproductive organs of both males and females swell (Underwood, 1974). After March has past, the reproductive organs begin to decrease in size and eggs that were unfertilised in the females undergo cytolysis (destroying egg cells) and are reabsorbed into the body (Underwood, 1974).  

Little is known about the recruitment of juvenile N. pyramidalis back to the high shore, however since much smaller individuals are often found in crevices lower in the shore, it is hypothesised that juveniles settle and metamorphose in these rock crevices and later move higher in the intertidal (Reid and Williams, 2004).

Torsion

Throughout development, all gastropods undergo torsion (Brusca et al., 2016). Torsion typically takes place during the veliger larvae stage. Torsion is the rotation of the visceral mass of the gastropod 180 degrees, resulting in the mantle cavity and anus moving to near the head (Brusca et al., 2016). Since Nodilittorina pyramidalis is a gastropod, it too undergoes torsion, however when it occurs has not been well studied. The adaptive significance of torsion is not yet agreed upon. One theory is that the torsion allows for a better retraction of the head into the shell as protection from predators (Brusca et al., 2016), however this theory is still unsubstantiated.  A further possibility is that torsion and coiling in the shell evolved in unison to allow for better body alignment within the shell, more balance and more growth (Brusca et al., 2016).

Body Posturing

Posturing is how an individual snail positions themselves s on the substrate. Several positions have been observed in Nodilittorina pyramidalis. The positions function to minimize thermal stress and to prevent desiccation by decreasing contact with the substrate (Lim, 2008). Decreasing substrate contact minimising the amount of heat that is transferred to the animal body by conduction and prevents the escape of moisture (Lim, 2008). A species in the same family, Echinolittorina malaccana, also demonstrate these thermoregulatory behavioural responses. A study conducted on these species found that these standing positions significantly reduce the amount of heat entering to body of the individuals allowing them to remain under the critical thermal limit of the snail, even more so then being in a shaded environment (Marshall and Chua, 2012).

Three main positions have been identified in N. pyramidalis:

-        Standing: The operculum is closed, and the snail is held vertically secured by a hold fast.

Shell

Nodilittorina pyramidalis is a large periwinkle typically ranging shell sizes between a tiny eight millimetres and approximately three centimetres (Reid and Williams, 2004). The shell is covered in rows of white nodules, however these are not axially aligned (Figure 15), and which is a distinguishing feature from other similar looking species. Unlike a similar looking species Echinolittorina trochoides, there is only one row of nodules on the penultimate whorl (Figure 15) and there are two rows of nodules on the final whorl (Reid and Williams, 2004). The shape of the shell is between a tall-spired turbinate shape and more conical shell shape and shell shape has been seen to vary slightly between different beaches (Reid and Willams, 2004). The shell is also covered in fine cords around the entire surface, however these cords are not nodulose (Figure 15). The aperture of this species is also is brown with two cream bands (Reid and Williams, 2004).

 Figure 14: Nodilittorina pyramidalis shell. Scale bar (white) is 0.5cm.

Figure 15: Shell morphology of Nodilittorina pyramidalis. Blue line shows the lack of axial alignment of nodules. Scale bar (white) is 0.5cm. 

Head-foot

The head and sides of the foot of the pyramid perwinkle are grey to black in colour (Reid and Williams, 2004). The head has two cephalic tentacles with simple eyes at the base of the tentacles (Figure 16). The cephalic tentacles have two wide black stripes on the sides of the tentacles, but have a pale tip (Reid and Williams, 2004).  The foot is muscular and contains mucus producing cells (pedal gland) which secrete mucus and both are used for movement and adhesion to the substrate (Davies and Hawkins, 1998). In littorinids, the foot is divided into three main sections: the propodium, the mesopodium and the metapodium (Reid, 1989). The propodium and mesopodium are near the head region on the foot and are separated by a deep transverse groove (Reid, 1989). The metapodium is at the posterior end of the body and bears the operculum. The foot in most littorinids has a longitudinal division which allows for locomotion using two series of waves (ditaxic locomotion) (Reid, 1989). This form of movement allows for better turning and adhesion to the substrate and is hence thought be evolutionarily beneficial for highshore species such as N. pyramidalis (Reid, 1989).

Figure 16: Nodilittorina pyramidalis feeding on microalgae. Head, foot and cephalic tentacle indicated with red lines and labels.  

Operculum

The operculum is the structure which closes and seals the aperture (Reid, 1989). In high shore littorinids, it is common for the operculum to be thick with more spiral to decrease water loss. In Nodilittorina pyramidalis, the operculum is brown and spiralled however is not as thick as other littorinids (Reid, 1989). However, the circular shape helps to decrease water loss.

Mantle

The mantle in all gastropods is very important since it is the outer layer of the body and secretes the gastropod shell. It is a sheet like organ that envelops the molluscan body (Brusca, et al., 2016). This organ creates the mantle cavity which houses the ctenidium, osphariadia, nephridiopores, gonopores and anus (Brusca, et al., 2016).

Mouth and Radula

The pyramid periwinkle is an herbivorous gastropod, feeding on microalgae in the high intertidal zone, and as such have a specialised mouth and radula (Reid, 1989). The mouth is a structure on the head between the cephalic tentacles that faces downwards towards the substrate. The radula protrudes through the mouth and collects microalgae from the substrate and brings it back into the mouth.

The radula in littorinids tends to be long because it can become degraded relatively quickly from feeding on microalgae on hard substrates and therefore also has many tooth rows (Reid, 1989). There are four main types of tooth on the littorinid radula: rachidian, lateral tooth, inner marginal tooth and the outer marginal tooth. In rock dwelling species such as the pyramid periwinkle, there are typically three or less cusps on the rachidian, lateral tooth and inner marginal tooth, which is a potentially a function of feeding on hard substrates (Reid, 1989). The rachidian in N. pyramidalis has only one major elongated cusp (Reid and Williams, 2004). The lateral and inner marginal tooth have to main cusps and are large and blunter at the tip (Reid and Williams, 2004) In Nodilittorina, the outer marginal tooth has a distinct shape, where there is a narrow neck before broadening into a cusp bearing head with six or seven elongated and pointed cusps (Reid, 1989; Reid and Williams, 2004).

Figure 17: Nodilittorina pyramidalis without shell and radulua out. Radula is the rope like structure. Scale line (Black) is 0.5cm.

Figure 18: Longitudinal section of Nodilittorina pyramidalis buccal cavity, showing the Radula. 

Circulatory and Respiratory

In most molluscs, the main body cavity is a hemocoel where tissues are bathed in hemolymph (blood) (Brusca et al. 2016). The hemolymph has many different cell types and its main functions is to transport oxygen and nutrients around the body. The heart in littorinids is in the pericardinal chamber and has only one atria and one ventricle (Mill, 1972). Oxygenated hemolymph is transported from the branchial vessel near the ctenidium into the atrium which then pump the hemolymph into the ventricle (Brusca, et al, 2016). The ventricle then pumps the oxygenated hemolymph through the main artery into the sinus and haemocoel area, bathing the tissues in hemolymph. The de-oxygenated blood is then funnelled back to the branchial vessels to become oxygenated again (Brusca, et al., 2016).

Littorinids have lost the right ctenidium and the left ctenidium is attached directly to the mantle (Mill, 1972). The gill filaments extend into the mantle cavity (known as the monopectinate condition). As water enters the mantle cavity from the left, cilia on the ctenidia move water over the ctenidia (Brusca, et al. 2016). The hemolymph flows in the vessels in the opposite direction (Brusca, et al., 2016). This allows for counter-current exchange of oxygen, which is very effective as maximal oxygen can always be diffusing across into the haemolymph. The water depleted in oxygen then exits on the right side of the head near the opening of the anus and nephridiopore (Brusca, et al., 2016).

Figure 19: Longitudinal Section of Nodilittorina pyramidalis ctendium. Image showing the gill filaments extending into the mantle cavity. 
 

Nervous and Sensory

General

The most common nervous system in the family Littorinidae is one with an epiathroid structure (Reid, 1989). In epiathroid neural structures, the cerebral and pleural ganglia are adjacent (Reid, 1989). Peripheral nerves stem from the cerebral ganglia to other sense organs and the buccal ganglia which control buccal musculature, the radula and the oesophagus, which further innervates other organs in the mantle cavity (Brusca, et al., 2016). Visceral cords stem from the pleural ganglia which continue to the posterior of the animal. From these visceral cords, peripheral nerves stem to the mantle and visceral mass (Brusca, et al., 2016). However, due to torsion, the gastropod nervous system is twisted into a figure eight and the posterior nerves are now localised near the head and have been shortened (Brusca, et al., 2016). Nerves are also present in the foot, allowing for locomotory movement (Brusca, et al., 2016). Some important sense organs include the eye, the cephalic tentacles and osphradia.

The Eye

The eye is a prominent and obvious sensory structure of Nodilittorina pyramidalis due to its dark pigmentation. The eye is located at the base of the cephalic tentacle and is visible through the transparent skin overlaying it (Newell, 1963). The eye in littorinids receives light from both in front and above it based on its structure (Newell, 1963). The main components of the littorinid eye include the lens, cornea (and associated muscle), pigment layer and the optic nerves (Newell, 1963; Brusca, et al., 2016). In Newell’s 1963 investigation of the eye of Littorina littorea eye, he found that the eye should produce sharp images of distant object in the air and underwater that view would only be slightly distorted. This would be useful in littorinid species, particularly the pyramid periwinkle since it spends most of its time above the water.

Figure 20: Longitudinal section of Nodilittorina pyramidalis eye. Image shows the Cornea, Epidermis layer, Lens and pigment layer. 

The Cephalic Tentacle

The cephalic tentacles are tentacles that are localised on the head. Species in the family Littorinidae only have one pair of cephalic tentacles and no other tentacles (Ng, et al., 2013). The cephalic tentacles are long, mobile and are not covered in cilia (Reid, 1989). In Ng, et al.’s investigation (2013), the cephalic tentacles of littorinids were seen to frequently contact the substrate during trail following, likely with tactile and chemosensors. Therefore, it has been hypothesised the tentacles are an important component of sensory trail following and may be particularly important in forming aggregations which prevent aggregations (Ng, et al., 2013).

Figure 21: Nodilittorina pyramidalis head and cephalic tentacles with the eyes at the base. Notice black bands on the side of the tentacles. Scale bar (Black) is 0.5cm. 

Osphradia

Osphradia are chemoreceptors located near the ctenidium which sometimes assist with ventilation (Brusca, et al., 2016). In Littorinidae, the osphraidum occurs on the ctenidia and has many nerves and is highly ciliated outside the sensory zone (Haszprunar, 1985). In high-shore species such as the pyramid periwinkle, the ctenidium are reduced but the osphradia is still well developed (Haszprunar, 1985). More about the osphradia is yet to be understood particularly because it varies greatly within taxonomic groups (Brusca, et al., 2016).

Digestive System

All gastropods have complete guts and digestion takes place extracellularly including in Nodilittorina pyramidalis. Microalgae is scraped up into the mouth by the radula which is stored in the buccal cavity. There are several glands secreting into this buccal region to ensure a smooth functioning radula as well several glands secreting enzymes (Brusca, et al., 2016). Food passes down through the oesophagus into the gizzard which is a highly muscular stomach and grinds tough vegetable matter. The enzymes secreted in the foregut, stomach and in the digestive gland cells accomplish extracellular digestion (Brusca, et al., 2016). Intracellular digestion occurs after the food matter has passed through the stomach into the digestive gland cells and in the walls of the intestine (Brusca, et al., 2016). Waste passes through the intestine and expelled through the anus near the head of the animal.

Figure 22: Digestive sac (Stomach) of Nodilittorina pyramidalis. Image showing digestive muscle and internal digestive cavity.

Excretory System

In littorinids, the heart is where primary urine is produced, and this is transported from the pericardinal sac to the nephridium (Emson, et al., 2002). The nephridium is large in littorinids and is the site of selection reabsorption of organic solutes (Emson, et al., 2002; Brusca, et al., 2016). The fluid then passes out through the nephridiopores, typically near the anus (Emson, et al., 2002; Brusca, et al., 2016). The structure of excretory system is quite variable within Littorinidae, however highshore species typically have adaptations to decrease the production of primary urine, most likely to survive the harsh environment (Emson, et al., 2002).