Biology and ecology of the emerald neritid Smaragdia viridis (Gastropoda) and its link with seagrasses in Europe
Jose L. Rueda
Departamento de Biología Animal, Universidad de Málaga, Campus de Teatinos s/n, 29071- Málaga, Spain.
Individual of Smaragdia viridis (shell height 1.7 mm) grazing on a Cymodocea nodosa leaf and leaving a characteristic radular mark.
It is widely known that seagrass beds represent a suitable habitat for a high number of species due to their complex structure (e. g. sediment and seagrass shoots) which offers a shelter from predation and a wide range of food sources, among other features (Hemminga and Duarte, 2000). Most species associated with seagrass beds, including the group of molluscs, do not graze directly on seagrass tissues and may feed on other food sources (e.g. epiphytes, periphyton, detritus) which are also highly available in this type of habitat (Thayer et al., 1984; Valentine and Duffy, 2006). In Europe, some molluscs grazing on microalgae (e.g. J. striatus, R. membranacea), which are dominant in seagrass beds, may also form stable populations in other similar habitats, such as algal beds of Caulerpa prolifera (Rueda and Salas, 2003), and therefore their dependence on seagrass beds is questionable. In fact, few molluscan species seem to feed directly on alive seagrass leaves (Carlton et al., 1991; Zimmerman et al., 2001), which also represent an important food source for different species of vertebrates and sea urchins (Hemminga and Duarte, 2000). Up to date, no detailed information is available on the importance of seagrasses as a direct food source for any molluscan species living in European coasts, which may imply a high dependence on seagrass beds and an important component in the mobilization of seagrass carbon to higher trophic levels.
The emerald neritid Smaragdia viridis (Linnaeus, 1758) is the only native marine species from the family Neritidae in European coasts. Little is known on the ecology and biology of this species, with some information indicating that it is highly associated with Zostera marina (in open marine bays from southern Spain) and Cymodocea nodosa beds, forming therein stable populations (Luque and Templado, 2004). This species also occurs in the Caribbean sea where it is mainly associated with the seagrasses Thalassia testudinum or Halodule wrightii (Holzer, comm. pers.). Other Smaragdia species are also highly associated with seagrasses such as S. bryanae with different species of the genus Halophila in Hawaiian Islands (Unabia, 1980), S. rangiana with Halophila stipulacea, Halodule uninervis and Cymodocea rotundata in the Red Sea (Zuschin and Hohenegger, 1998) or S. souverbiana with Zostera capricorni in eastern Australia (Rueda, pers. comm.). The relationship between S. viridis and the seagrasses Z. marina and C. nodosa has not been thoroughly investigated yet, so that it was interesting to study (1) the possible trophic dependence of this neritid on both seagrass species under laboratory experimental conditions and field observations and (2) some aspects of its biology such as its temporal dynamics and growth in mono-specific beds of both seagrass species.
Laboratory experiments with live S. viridis individuals of different sizes have been performed using (1) shoots of Z. marina, (2) shoots of C. nodosa and (3) leaves with similar area of both seagrasses (experiments on selection). Moreover, quantitative samples of shoots of Z. marina collected using quadrats (25 x 25 cm) in a mono-specific bed located in Cañuelo Bay (southern Spain) have been used for testing some of the results obtained in experiments with Z. marina. The ingestion rate of each individual was estimated using image analysis by measuring the area of all radular marks left on the shoot after 24 h experiments. Moreover, the location of each radular mark was annotated in order to know if there was any trend related with tissue quality. Finally, the absorption of the ingested epidermal tissues was also estimated by the percentage of broken (digested) and unbroken seagrass cells in faecal pellets collected after experimental treatments of each individual. The temporal dynamics and growth of S. viridis populations were studied by monthly quantitative samples of S. viridis collected in mono-specific seagrass beds of Z. marina (MPA Acantilados de Maro - Cerro Gordo, Málaga-Granada) and C. nodosa (MPA Cabo de Gata, Almería). The samples (2-3 monthly replicates) were collected at similar depths (10-14 m) during 1999 in C. nodosa and in during 2000-2001 in Z. marina using a small Agassiz trawl that covered a sampling area of 222 m2. These samples were collected during a project on the fauna associated with these seagrass beds in southern Spain (Alboran Sea) funded by the Spanish Government.
S. viridis is a seagrass feeder and ingests epidermal cells of Z. marina and C. nodosa leaves, leaving characteristics radular marks in both seagrasses. Faeces egested by this gastropod are mainly composed (> 99 %) of digested seagrass tissues. More detailed information with pictures of radular marks and faeces of this gastropod has been published in Rueda & Salas (2007). In relation with the selection of tissues within shoots, this neritid feeds mainly on young tissues of Z. marina such as those located in the central or first pair of adjacent leaves and close to the junction of the sheath with the leaves. The same trend was observed in the shoots used in the experiments and in those collected quantitatively in the Z. marina bed. In C. nodosa, a similar trend of feeding has been observed with most radular marks located in the central leaf and in areas close to the junction of the leaves with the sheath. In seagrasses, young tissues are located in these areas within the shoots and the content of non easily digestible compounds such as cellulose and lignin is lower in these areas in comparison with older tissues located in the apical parts of the leaves (with high amount of epiphytes) or the outer leaves.
The ingestion rate of S. viridis individuals is size-dependent and is significantly higher in C. nodosa than in Z. marina, grazing up to 5 % of the leaf area of one shoot per day. In a Z. marina bed, the grazing impact is around 2.5 % of the Leaf Area Index of this seagrass bed so it seems that the direct impact is low compared to other seagrass feeding gastropods (e.g. Tectura depicta) (Zimmerman et al., 2001). Nevertheless, the secondary effects on the plant are unknown. Contrary to the ingestion rate, the absorption of cells is larger in Z. marina than in C. nodosa, probably due to thicker cell walls and higher content of cellulose in the latter which may difficult the digestion of epidermal cells. A preferential selection of S. viridis for Z. marina has been found in those experiments of selection when both seagrasses were available.
This gastropod occurs along the entire year in the both seagrass beds, displaying similar densities with less than 1 individual per m2 with maximum abundances in spring and summer months when seagrass leaf biomass reaches maximum values. The recruitment occurs during summer months in Zostera marina and also in autumn ones in C. nodosa. In the studied populations, a lower growth rate has been obtained for that associated with C. nodosa when compared to that of Z. marina. This is probably the result of the lower absorption of C. nodosa tissues compared to those of Z. marina as observed during the experiments, however detailed aspects of the nutritional quality of both seagrasses are still unknown.
Molluscs known to feed basically on fresh tissues of seagrasses are very scarce world-wide and they always represent a very low percentage of the species associated with seagrass beds. The gastropod S. viridis represents one of these species and probably the first known prosobranch within this trophic category for the European malacofauna.
This study has been funded by a research grant of The Malacological Society of London under the project "Biology and ecology of Smaragdia viridis (Linnaeus, 1758) and its link with seagrasses".
|Carlton, J. T., Vermeij, G. J., Lindberg, D. R., Carlton, D. A. & Dudley, E. C. 1991. The first historical|
|extinction of a marine invertebrate in an ocean basin: The demise of the eelgrass limpet Lottia alveus. Biological Bulletin, 180: 72-80.|
|Hemminga, M. A. & Duarte, C. M. 2000. Seagrass Ecology. Cambridge University Press, Cambridge.|
|Luque, A. A. & Templado, J. 2004. Praderas y bosques marinos de Andalucía. Junta de Andalucía,|
|Rueda, J. L. & Salas, C. 2003. Seasonal variation of a molluscan assemblage living in a Caulerpa|
|prolifera meadow within the inner Bay of Cádiz (SW Spain). Estuarine Coastal and Shelf Science, 57: 909-918.|
|Rueda, J. L. & Salas, C. 2007. Trophic dependence of the emerald neritid Smaragdia viridis|
|(Linnaeus, 1758) on two seagrasses from the European coasts. Journal of Molluscan Studies,73: 211-214.|
|Thayer, G. W., Bjorndal, K. A., Ogden, J. C., Williams, S. L. & Zieman, J. C. 1984. Role of large|
|herbivores in seagrass communities. Estuaries, 7: 351-376.|
|Unabia, C. 1980. Smaragdia, a seagrass animal. Pacific Science, 34: 340.|
|Valentine, J. F. & Duffy, J. E. 2006. The central role of grazing in seagrass ecology. In: Seagrasses:|
|Biology, Ecology and Conservation (Eds: A. W. D. Larkum, R. J. Orth & C. M. Duarte), Springer, Dordrecht, pp. 463 - 501.|
|Zimmerman, R. C., Steller, D. L., Kohrs, D. G. & Alberte, R. S. 2001. Top-down impact through a|
|bottom-up mechanism. In situ effects of limpet grazing on growth, light requirements and survival of the eelgrass Zostera marina. Marine Ecology Progress Series, 218: 127-140.|
|Zuschin, M. & Hohenegger, J. 1998. Subtropical coral-reef associated sedimentary facies|
|characterized by molluscs (northern Bay of Safaga, Red Sea, Egypt). Facies, 38: 229-254.|