Caribbean Seagrasses As A Food Source For The Emerald Neritid Smaragdia Viridis
Caribbean Seagrasses As A Food Source For The Emerald Neritid Smaragdia Viridis
Caribbean Seagrasses As A Food Source For The Emerald Neritid Smaragdia Viridis
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Amer. Malac. Bull. 29: 63-67 (2011)
Caribbean seagrasses as a food source for the emerald neritid Smaragdia viridis
1
Department of Environmental Sciences, University of Virginia, 291 McCormick Road, Charlottesville, Virginia 22904-4123, U.S.A.
2
Marine Environmental Program, Bermuda Institute of Ocean Sciences, 17 Biological Lane, Saint George’s GE01, Bermuda
3
Departamento de Biología Animal, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos s/n, Málaga 29071, Spain
Correspondence, K. K. Holzer: [email protected]
Abstract: Seagrass canopies harbor many different mollusc species, but information about the interaction of these seagrass residents with
their host plants remains scarce. Most gastropods inhabiting seagrass meadows are believed to feed on epiphytes rather than directly on living
seagrass tissues. In laboratory experiments, we demonstrate that the gastropod Smaragdia viridis (Linnaeus, 1758) feeds preferentially on
three seagrass species that are common in the Caribbean and Bermuda, including Thalassia testudinum, Halodule wrightii, and Syringodium
filiforme. The percentage of lysed over intact seagrass cells egested was significantly higher in gastropods fed either T. testudinum or H. wrightii
(80.3 ± 4.7% and 84.6 ± 11.4%, mean ± SD) but not for S. filiforme (59.7 ± 15.9%). Diet versatility for both pioneer (H. wrightii and S.
filiforme) and climax (T. testudinum) Caribbean seagrass species allows S. viridis to adapt to small-scale disturbances that are common in these
habitats, but a diet specializing in seagrass may make this animal vulnerable to large-scale seagrass declines occurring worldwide.
Seagrass beds represent an important habitat for a large Caribbean, S. viridis has been shown to associate with Thalassia
number of mollusc species in the world’s coastal oceans testudinum (Scheltema 1971, Lewis and Hollingworth 1982,
(Hemminga and Duarte 2000). Recent data show that Thayer et al. 1984, Sterrer 1986, Brunt and Davies 1994). The
herbivory on seagrasses is more important than previously emerald neritid is also found in Halodule wrightii and
thought, yet the role of small seagrass-feeding invertebrates is Syringodium filiforme pastures (K. Holzer, pers. obs.). The
still poorly understood (Heck and Valentine 2006). Because association of S. viridis with Caribbean seagrass meadows
most seagrass-associated molluscs (i.e., gastropods) and suggests a possible trophic dependence. In a paper published
crustaceans (i.e., amphipods and isopods) feed heavily on by Thayer et al. (1984: 362), the authors recount,“S. viridis
epiphytic algae attached to seagrass leaves (Jernakoff et al. roams about the lower half of the green [Thalassia] blades
1996), small epifauna that also obtain nutrition directly from and removes a furrow about 1 mm wide and half the thickness
living seagrass may have a competitive advantage over other of the blade with its radula.” A comment on the presence
mesograzers. Predation on these small seagrass-feeding of seagrass epidermal tissues in feces of S. viridis was also
invertebrates may represent an additional pathway in the made in a paper characterizing the epifauna of Thalassia
mobilization of seagrass carbon from plant material to meadows in Barbados (Lewis and Hollingworth 1982).
animals in higher trophic levels, such as crabs and fishes However, these two studies did not deal with ingestion of
(Castriota et al. 2005). tissues of different seagrass species by S. viridis. We addressed
The emerald neritid Smaragdia viridis (Linnaeus, 1758) this issue in a laboratory experiment where we presented S.
inhabits seagrass beds of the Caribbean Sea, Mediterranean viridis with tissues of three subtropical to tropical western
Sea, and probably the western African coasts. This large Atlantic seagrass species (T. testudinum, H. wrightii, and S.
geographic range seems to be explained by the species’ filiforme). Bermuda represents the northernmost limit of
planktotrophic development with larvae remaining in the these marine angiosperms. We documented the radular
water column up to 55 days (Scheltema 1971). In the marks made on the seagrass leaves and quantified the presence
temperate meadows of the Mediterranean Sea, this small of seagrass cells in the fecal pellets produced during the
gastropod resides in Cymodocea nodosa and Zostera marina feeding trial. We also obtained the relative proportion of
meadows, where leaf epidermal tissues of these plants are its lysed to intact seagrass cells in the feces as a proxy for
main food source (Rueda and Salas 2007). In these meadows, digestibility. This study provides data refining the often-cited
densities may reach 50 individuals m-2, with maximum values paradigm that small gastropods in subtropical to tropical
in the summer due to enhanced recruitment (Rueda et al. seagrass meadows ingest seagrass only incidentally while
2009). In the subtropical to tropical meadows of the feeding primarily on algal epiphytes.
63
64 AMERICAN MALACOLOGICAL BULLETIN · ·
29 1/2 2011
MATERIALS AND METHODS feces were also tallied. The potential assimilation of the three
seagrass species was then estimated as the percentage of empty
A microcosm feeding experiment was conducted in seagrass cells compared to the total number of seagrass cells
October 2008 to establish diet preferences of the neritid (empty and intact).
gastropod Smaragdia viridis which is a common component Separate Chi-square analyses for each seagrass diet were
of the epifauna assemblage in seagrass meadows of the used to evaluate whether snails (1) prefer seagrass tissues or
Caribbean and Bermuda. In Bermuda we recorded snail epiphytes and (2) lyse seagrass cell walls to access the cellular
densities of 0-150 individuals m-2 in different seagrass areas, contents. The independent variable in both cases was cell
as well as the presence of the characteristic hemispherical (ca. type and the dependent variable was abundance of that cell
1 mm diameter) glossy-yellow spawn masses deposited on type in the fecal pellet. Expected values were based on a
epiphyte-free seagrass blades at the base of the shoot. For predicted equal number of (1) seagrass and epiphyte cells
this experiment, neritids were collected by snorkelers on and (2) empty and intact seagrass cells, for each of the three
Bermuda’s north shore from three shallow (ca. 2 m depth) seagrass diets. While statistical tests were run on cell abundance,
mixed-species beds dominated by Thalassia testudinum, and we report the percentage of the different cell types comprising
also including Halodule wrightii and Syringodium filiforme: fecal pellets to convey more clearly significant trends in
Fort Saint Catherine (32°23ƍN, 64°40ƍW), Higgs Cut (32°22ƍN, the data.
64°39ƍW), and Clearwater (32°21ƍN, 64°39ƍW). All study Smaragdia viridis makes consistent and characteristic
animals were found attached to one of the three seagrass grazing trails, independent of season. The weeklong feeding
species and were never observed on rock or algal substrates. trial was repeated in July 2009 to obtain seagrass and feces
They were acclimated to laboratory conditions for a week and samples to photograph.
supplied with abundant seagrass-epiphyte forage from their
local meadows.
The weeklong feeding trial was performed in an outdoor RESULTS
flowing seawater system exposed to ambient temperature,
light, and weather conditions at the Bermuda Institute of Smaragdia viridis left radular marks while eating the
Ocean Sciences. Individual microcosms consisted of neutrally epidermal tissues of all three seagrass species (Figs. 1A, 1D,
buoyant 120 ml transparent plastic containers that were 1G). Radular marks were made along the central part of leaves
perforated with 14 × 3-4 mm holes to permit constant water (up to 5 cm long), except for Syringodium filiforme, which
exchange. One Smaragdia viridis was placed inside each has a circular leaf cross-section. In Thalassia testudinum, the
container along with a single-species seagrass diet (N = 10). radular marks were less continuous than in both S. filiforme
Food items consisted of healthy (green) undamaged and Halodule wrightii, and sometimes epidermal tissues of
5-10 cm long segments of both new and old seagrass leaves both sides of the T. testudinum blade were ingested producing
(Thalassia testudinum, Halodule wrightii, or Syringodium transparent lines (Fig. 1A).
filiforme) and attached epiphytes. Food was collected from In all cases, fecal pellets were cylindrical (200–400 µm
Bailey’s Bay (32°20ƍN, 64°43ƍW) at ca. 2 m depth, where length) with a longitudinal green line (10–20 µm width) rich
epiphyte loads were 1.6 ± 0.5 mg DW cm-2 and epiphyte in chloroplasts. Under microscopic observation, the feces
organic content was 25 ± 2% (mean ± SD, N = 10). Fresh consisted mainly (> 95%) of tissues of the three seagrass
forage was exchanged daily for five consecutive days. On the species, which were easily distinguished by cell size and shape
sixth day, the animals were held in separate glass bowls (Fig. 1C, 1F, 1I). Ungrazed leaves of the three different
containing seawater filtered through a 45-µm membrane, seagrass species are shown for comparison (Figs. 1B, 1E, 1H).
and feces were recovered after 24 hours with a pipette. Epiphytes (macroalgae, diatoms, and foraminifers) repre-
At the end of each experiment, seagrass blades were sented < 3% of the fecal composition and were significantly
examined for radular marks created by the neritid using a lower in abundance than seagrass cells (empty and intact)
binocular microscope, and those areas on leaves containing for all seagrass treatments (Thalassia testudinum Ȥ2 = 45.9,
feeding trails were fixed in Lugol. Feces egested by Smaragdia df = 1, N = 10, P < 0.05; Halodule wrightii Ȥ2 = 15.1, df = 1,
viridis during the experiment were also collected using a N = 10, P < 0.001; Syringodium filiforme Ȥ2 = 23.0, df = 1,
pipette and fixed in Lugol for further microscopic analyses. N = 10, P < 0.001) (Fig. 2A). The abundance of empty
Empty seagrass cells (without cytoplasm and chloroplasts) seagrass cells was significantly higher than intact cells for
and intact seagrass cells (with cytoplasm and chloroplasts) Thalassia testudinum (Ȥ2 = 18.2, df = 1, N = 10, P < 0.001) and
were counted in fecal pellets collected during the experiment Halodule wrightii (Ȥ2 = 9.4, df = 1, N = 10, P < 0.01), but not
using the three seagrass species. Components of the epiphyte for Syringodium filiforme (Ȥ2 = 3.3, df = 1, N = 10, P > 0.05)
community (macroalgae, diatoms, and foraminifers) in the (Fig. 2B).
SEAGRASS GRAZING NERITID 65