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Summary | |
Nerita albicilla is a marine gastropod that occurs across temperature, tropical and subtropical regions, and occupies the intertidal shores of the North-east Australian coast. It is recognised for the black and white blotched colouration of its shell and thick, granular operculum. This species has been observed exhibiting seasonal migratory behaviour (local scale) which has not previously been recorded for this genus and contradicts the size-dependent biogeography observed across most species of Nerita. The recent discovery of trace element and toxin accumulation in the ostracum shells of N. albicilla poses potential concern to the reproductive health and survival of individuals however, is useful as a biological indicator to the health of coastal waterways (El-sorogy et al. 2013).
The classification for this species is as follows:
Kingdom: Animalia
Phylum: Mollusca
Class: Gastropoda
Subclass: Neritimorpha
Order: Cycloneritida/Neritopsina, Cox and Knight 1960
Superfamily: Neritoidea, Rafinesque 1815
Family: Neritidae, Rafinesque 1815
Genus: Nerita
Species: Nerita albicilla, Linnaeus 1758
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Physical Description |
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Operculum | |
Whilst most Neritidae have a thick calcareous operculum, Vermeij and Hoeft (2018) suggest that tropical gastropods will have a thicker operculum than temperate, most likely as a result of increased temperature and risk of desiccation. The operculum on N. albicilla is defined as granular, avoid of any submarginal band with a spirally granulated inner lip (Sasaki 2000, see fig. 6). The operculum is attached via a distinct apophysis (hinge) in which is pivots around the columellar deck as the foot is extended (Sasaki 2000). Studies have found variation in operculum thickness between turbinid position along the intertidal gradient, however no such phenomena was observed inter or intra-specifically within Neritidae (Vermeij and Hoeft 2018).
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| Figure 6 |
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Ecology |
Habitat | |
N. albicilla are not a species or genera that favour being constantly submerged, as observed when all specimens climbed up the walls and escaped from their holding tank. Instead they prefer the intertidal rocky shore with high levels of rugosity for shelter and rock pools (Bovbjerg 2006). A study by Underwood (2006) relates the density and activity of neritids to the rugosity of the substrate and found that areas with higher density of pits and crevices saw an increase in neritid density. Whilst other genera are able to avoid the desiccation and UV radiation risks of extending their soft tissues (to feed) during the day by utilising rock pools and wet substrate to cool (Underwood 1997), Nerita have a different approach. They rely on their successful ability to aerially respire and maintain constant respiration rate with increased temperatures, rather than extended periods of evaporative cooling (Lewis 1971). It is this enhanced metabolism and thick operculum of N. albicilla that allows them to avoid desiccation risks and adopt a nocturnal lifestyle, in which they rest under rocks and crevices during the day, and migrate to mid-ebb tide at night to feed (Ruwa and Jaccarini 1988).
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Predator relationships | |
Predators of N. albicilla are typically similar to those of the genera and include other gastropods, crabs and fish (Rohrkasse and Atema 2002; Reynolds and Reynolds 1977). Shigemiya (2002) details the predatory behaviour of pebble crab, Eriphia smithii on N. albicilla on a rocky intertidal shore in Japan. The crab uses its large claw of molar teeth to first nip the outer lip of the shell aperture, and then proceed to break the shell piece by piece (termed “peeling”) from the lip of the shell. Occasionally crabs exhibited a simple squeeze and crush method however a clear preference for peeling was observed (n=123/143 eaten). This peeling behaviour may be indicative of a predator-prey arms race, in which N. albicilla adapts by increasing lip thickness and ostracum density, whilst crabs look to new and specialised methods of defeating such defences (Reynolds and Reynolds 1997).
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Life History and Behaviour |
Shell density dependent behaviour | |
Tokeshi et al. (1999) suggests that shell weight increases proportionally to body mass in gastropods and found N. albicilla to have the highest shell weight to body mass of all molluscs tested (76.4%). The paper identified a positive linear relationship between shell mass and the mechanical strength of the shell, hence heavier shells may aid in protection against predators such as muricid gastropods (Lam 2002) and crabs (Shigemiya 2002). The disadvantages of bearing such a heavy shell are demonstrated in a study by Lam (2002), in which N. albicilla individuals placed in a beaker of sea water and presented with related predators, did not move out of the water. It is suggested that this behaviour is justified due to their defences such as their thick, calcareous operculum, wide outer lip and thick shell outweighing the costs of unnecessary energy expenditure associated with moving up the beaker (Lam 2002). However, this behaviour can be attributed to individual plasticity, which is highlighted by Chapperon and Seuront (2010) by the high intra-specific variation in behavioural movement observed in multiple Nerita sp.
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Size related physiology and behaviour | |
Tokeshi et al. (1999) also suggest that larger shells with greater mass may reduce the risk of desiccation, which may be attributed to the size dictated spatial variation behaviour observed within Neritidae. A study by Ruwa and Jaccarini (1998) highlights the difference in feeding migration between large and small neritids, in which the latter travel up from the lower littoral zone to feed and the former migrate down from the high tide zone. This behaviour may be attributed to size dependent respiration rates demonstrated by Lewis (1971) where larger neritids were shown to withstand the high temperatures associated with the upper littoral zone by maintaining a constant respiration rate. Comparatively, the small neritids exhibited a decrease in respiration rate as temperatures increased, therefore necessitating the need to remain within the lower littoral zone to perform evaporative cooling, which is otherwise not feasible with the high temperatures of the upper littoral zone (McMahon 1990). Due to their dark colouration and tropical geographical range, Nerita tissue temperature is capable of reaching temperatures higher than their surroundings. Despite these findings, a population of large and small N. albicilla were discovered in the lower littoral zone along the north-east Australian coast in which N. polita and N. plicata were observed above them along the intertidal gradient (Coleman 1976). Coleman (1976) found N. albicilla population to have a high metabolism (respiration rate approx. double that of N. polita) and a reduced emersion period (4h, N. polita= 10h). The cooler temperatures associated with the lower littoral may allow such high respiration rates to occur and if an individual is located in this zone it is restricted by the tide, hence the reduced emersion period. This behaviour may be attributed to seasonality of N. albiclla as inferred by the findings of Harper and Williams (2000), where differences between the ectotherms position along the intertidal varied with the wet and dry season in Hong Kong. During the wet season (Summer), only microalgae is available in crevices and cracks rather than in the higher usually dry littoral zone and thus staying by the water in the lower zone is beneficial to avoiding desiccation without the need to vertically migrate to the upper intertidal. The dry season however, despite no dramatic temperature shift in Hong Kong, the hiatus of rain encourages macroalgae growth on the upper intertidal rock surface and sees a migratory shift in N. albicilla to these regions (Harper and Williams 2000).
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Anatomy and Physiology |
Respiration | |
The pericardial cavity in which the heart operates is located in the anterior visceral mass of the neritid as a result of torsion (180° rotation of visceral mass and mantle cavity during development). The auricle chamber within the pericardial cavity is responsible for filtration of large molecules and cells via podocytes which is representative of ancestral prosobranch condition of Nerita (Estabrooks et al. 1999; see fig. 7). Nerita have an ancestral vestigial gill and one functioning gill, in which oxygen-rich water is passed over the tissue via ctendial cilia in the direction opposite to the flow of oxygen-poor blood in order for efficient diffusion to occur (Estabrooks et al. 1990).
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| Figure 7 |
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Renal function | |
Nerita only have one kidney unlike their primitive ancestors in which two kidneys functioned separately as osmoregulation and excretion respectively. Due to the right kidney being evolutionarily lost, the left kidney is presumed to perform the functional duties of both kidneys as inferred by Estabrooks et al. (1999). It is suggested that the presence of both basophilic cells and ascidophills cells together complete the necessary renal functions of a gastropod including osmoregulation and excretion. The kidney of a neritid also harbours mucoid cells which are responsible for protecting the uropore from desiccation during long periods of neritid emersion within the intertidal (Estabrooks et al. 1999).
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Radula morphology and function | |
The morphology of radula denticles varies between species and genera of molluscs, however capture of food remains relatively similar. The radula is attached to a cartilaginous structure called the odontophore and is extended from the mouth via buccal muscles attached to it (Fretter 1965). Once fully extended, the radula is immediately retracted and the heterodont teeth situated along the radula scrape and sweep the substrate before the mouth closes and the process repeats (Fretter 1965). The first lateral teeth and associated rachidians are mainly responsible for ripping and scraping the substrate as exhibited by their worn down cusps (see fig. 8; Fretter 1965). The marginal teeth fans are closed upon radula retraction and hence sweep any dislodged particles towards the shovel-like fourth lateral and mouth (Fretter 1965). The marginal fans show no wear and their only purpose is collecting dislodged food.
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| Figure 8 |
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Biogeographic Distribution | |
Nerita are known to occur in temperate, tropical and subtropical regions in freshwater streams and marine environments (Harper and Williams 2000). Marine neritids are most commonly found on rocky intertidal shores and this is no different with N. albicilla. Although many microhabitats influence the biogeographic location of ectotherms along the vertical intertidal gradient (see Life behaviour and history), there are also genera and species specific distribution patterns within macroenvironments. Although an exhaustive biogeographic distribution is not listed here, many studies have noted occurrences of N. albicilla in Indo-pacific including Japan, Eastern Indonesia and Hong Kong (Harper and Williams 2000; Tokeshi and Ota 1999; Lam 2002; Humahu and Uneputty 2018; Shigemiya 2002) and also across various coasts of Australia (Coleman 1976). Observations of this species have also been recorded in the Egyptian Red Sea (El-Sorogy et al. 2013).
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Evolution and Systematics | |
Protobranchs are modified from primitive forms descended from aspidobranch ancestors (Fretter 1995). Neritacea is a group of rhipidoglossate (radula-bearing) prosobranchs, which is separated into two families: Neritidae and Helicinidae. The latter is a pulmonate snail that has lost all ctendium tissue and is terrestrial. The new subclass, Neritacea, originated from the divergence of snails in Archaeogastropoda via the following characteristics (see fig. 7): the loss of the right ctenidium, which resulted from the development of an enlarged genital duct; enlargement of the left kidney due to the subsequent loss of (most) the right kidney; the incorporation of right kidney duct into the genital tract; and finally, internal fertilisation as a consequence of cephalic penis and glandular genital duct development (Fretter 1995).
In regards to N. albicilla, Neritospina is a clade that originated in the Ordovician and is now considered as Neritimorpha in which recent members have shared derived traits including odontophoral cartilages and muscles, anterior digestive tract and nervous systems (Sasaki 2000). The clade gave rise to wide adaptive radiation of lineages in varying habitats across the globe (Sasaki 2000).
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Conservation and Threats | |
This species of Nerita is not listed on the IUCN red list, however anthropogenic associated risks have been reported in recent literature. N. albicilla is one of the few species that has been recorded to accumulate various chemicals and toxins into its prismatic calcium carbonate shell (Sasaki 2000; El-Sorogy et al. 2013). Elements such as copper and zinc have been observed amongst the accumulated and it is unclear yet as to what, if any, implications this has on neritid growth, survival and reproduction (El-Sorogy et al. 2013). Global warming is an increasing threat on the survival of any population, particularly intertidal gastropods, however due to the phenological plasticity and adaptive behavioural patterns of the population, urgent action has no need for concern for near future.
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References | |
Bovbjerg, R. (1984). Habitat Selection in Two Intertidal Snails, Genus Nerita. Bulletin of Marine Science 34, 185-196
Chapperon, C., and Seuront, L. (2010). Variability in the motion behaviour of intertidal gastropods: ecological and evolutionary perspectives. Journal of the Marine Biological Association of the United Kingdom 91, 237-244.
Coleman, N. (1976). Aerial respiration of nerites from the North-East Coast of Australia. Australian Journal of Marine and Freshwater Research 27¸ 455-466.
El- Sorogy, A., El Kammer, A., Ziko, A., Aly, M., Nour, H. (2013). Gastropod shells as pollution indicators, Red Sea coast, Egypt. Journal of African Earth Sciences 87, 83-99.
Estabrooks, W. A., Kay, E. A., and McCarthy, S. A. (1999). Structure of the excretory system of Hawaiian nerites (Gastropoda: Neritoidea). The Malacological Society of London 65, 61-72.
Fretter, V. (1965). Functional studies of the anatomy of some neritid prosobranchs. Zoology 147, 46-74.
Harper, K., and Williams, G. (2000). Variation in abundance and distribution of the chiton
Acanthopleura japonica and associated molluscs on a seasonal, tropical, rocky shore. Zoology 253¸ 293-300.
Humahu, S., and Uneputty, P. (2018). Morphometric variation of ten species of Nerita (Molluscs: Gastropods) in rocky intertidal zone of Oma Village, Central Moluccas, Eastern Indonesia. International journal of Fisheries and Aquatic Studies 6, 276-280.
Lam, K. (2002). Escape responses of intertidal gastropods on a subtropical rocky shore in Hong Kong. The Malacological Society of London 68, 297-306.
Lewis, J. (1971). Comparative respiration of some tropical intertidal gastropods. Journal of Experimental Marine Biology and Ecology 6, 101-108
McMachon, R. F. (1990). Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193, 241-260.
Reynolds, W., Reynolds, J., (1977). Zoogeography and the predator-prey `arms race :' A comparison of eriphia and nerita species from three faunal regions. Hydrobiologia 56, 63-67
Rohrkasse, S., Atema, J., (2002). Tracking behavior of busyconinae whelks. The Biological Bulletin 203, 235-238
Ruwa, R., and Jaccarini, V. (1988) Nocturnal feeding migrations of Nerita plicata, N. undata and N. textilis (Prosobranchia: Neritacea) on the rocky shores at Mkomani, Mombasa, Kenya. Marine biology. Berlin, Heidelberg 99, 229-234.
Sasaki, T. (2000). Macro- and microstructure of shell and operculum in two recent gastropod species, Nerita (Theliostyla) albicilla and Cinnalepeta pulchella (Neritopsina: Neritoidea). Paleontological Research 5, 21-31.
Shigemiya, Y. (2002). Does the handedness of the pebble crab Eriphia smithii influence its attack success on two dextral snail species? Zoology 260¸259-265.
Tokeshi, M., Ota, N., and Kawai, T. (1999). A comparative study of the morphometry in shell-bearing molluscs. Zoology 251, 31-38.
Underwood, A.J. (1977). Movements of intertidal gastropods. Journal of Experimental Marine Biology and Ecology 26, 191-201.
Underwood, A.J. (2006). Landing on one¹s foot: small-scale topographic features of habitat and the dispersion of juvenile intertidal gastropods. Marine Ecology Progress Series 268, 173-182.
Vermaij, G., and Hoeft, E. (2018). Geography, shell form and opercular thickness of living marine neritid gastropods. Journal of Molluscan Studies 84, 498-500.
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