The effect of feeding behavior of the gastropods Batillaria zonalis and Cerithideopsilla cingulata on their ambient environment
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- Kamimura, S. & Tsuchiya, M. Marine Biology (2004) 144: 705. doi:10.1007/s00227-003-1238-x
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Feeding behaviors of the gastropods Batillaria zonalis, a suspension and deposit feeder, and Cerithideopsilla cingulata, an obligate deposit feeder, were studied to examine their effect on dynamics of suspended materials, total nitrogen (TN) and total organic carbon (TOC) in sediments. Suspension feeding in B. zonalis was observed in detail visually, as it had been previously unreported. An experimental system where B. zonalis and C. cingulata were cultured for 10 weeks, using previously frozen microalgae Nannochloropsis oculata as food, was then constructed. During feeding observations, the suspension-feeding B. zonalis formed a mucus “food cord” to entangle particulate materials, which were subsequently ingested. The feeding mode of B. zonalis is hence categorized as ctenidial filter feeding. For the culture experiments, decreases in suspended materials were seen only in the B. zonalis cultures, while the control (no gastropods) and C. cingulata cultures remained nearly unchanged. Sediment TN and TOC showed no significant differences between B. zonalis (with mean TN at 0.0345% and mean TOC at 0.261%) and control cultures (with TN at 0.0389% and TOC at 0.331%), but the sediments in C. cingulata cultures had lower levels (with TN at 0.0204% and TOC at 0.156%). The C/N ratios were similar for both B. zonalis (7.55) and C. cingulata (7.68) cultures, and both were lower than the control cultures (8.55). The filtration rate for B. zonalis was lower than that previously observed in bivalves inhabiting the same intertidal flat (e.g. Cyclina sinensis, Grafrarium tumidum and Barbatia virescens). However, Batillaria zonalis occurs at higher abundances than these bivalves. Therefore, it is expected that this species has a large affect upon the transport of suspended materials to the sediments. The addition of TN and TOC to sediments in B. zonalis cultures was probably caused by biodeposition, but deposit feeding by B. zonalis may have restrained the accumulation of those components. The impact of deposit feeding in Cerithideopsilla cingulata cultures was most probably stronger than sedimentation and biodeposition, because of the lower sediment TN and TOC. Bioturbation by both B. zonalis and C. cingulata yields the same effect on sediment quality, as indicated by the low C/N in the culture sediment of both treatments, despite difference in feeding modes. This paper demonstrates, for the first time, the importance of gastropods in bioturbation and removal of suspended materials in subtropical tidal flat habitats.
Many materials in the intertidal-flat ecosystem are supplied from the adjacent terrestrial and marine habitats (Knox 1986; Raffaelli and Hawkins 1996; Levinton 2001). Invertebrate feeding patterns in intertidal flats play an important role in the transportation and degradation of organic materials (Knox 1986; Raffaelli and Hawkins 1996; Lenihan and Micheli 2001). To understand the process of energy flux in the intertidal flat, it is therefore important to understand the feeding mechanisms of dominant species and their roles in nutrient transport via ingestion and fecal discharge.
The gastropods Batillaria zonalis (Family Batillariidae) and Cerithidea (Cerithideopsilla) cingulata (Family Potamididae) are dominant species in the Tomigusuku tidal flat located in the southern part of Okinawa Island, Japan (Kamimura 2000). These species probably have an important role in the energy flux of their habitat. In a study of their fatty acids, their food sources were reported to be macroalgae, bacteria and diatoms (Meziane and Tsuchiya 2000). Feeding selectivity was compared in a study of the congeneric species, B. attramentaria and C. california occurring in salt marshes located in central California (Whitlatch and Obrebski 1980). Here, B. attramentaria generally ingested larger diatoms than did C. california. Thus, there are some qualitative studies about food sources for Batillaria and Cerithidea, but no studies that quantitatively assess their roles in energy flux. B. multiformis (Morton and Morton 1983), B. cumingi (Koike et al. 1989) and B. flectosiphonata (Ozawa 1996) are reported to be deposit feeders and grazers of benthic diatoms. There are indications, however, that B. zonalis can do both suspension and deposit feeding (Kamimura 2000), but it has yet to be demonstrated in detail.
Dauer et al. (1981) proposed the term “interface feeder” for species that utilize particles from the sediment surface, in suspension and resuspended sediment. For example, the polychaetes Boccardia pugettensis, Pseudopolydora kempi japonica (Taghon and Greene 1992), Nereis diversicolor (Nielsen et al. 1995), Spiochaetopterus oculatus and Spio setosa (Bock and Miller 1997) are reported as “interface feeders”. The bivalve, Macoma balthica, also seems to feed on suspended and sediment-surface particles (Brafield and Newell 1961; Olafsson 1986) like the polychaetes. Batillaria zonalis is also expected to be an “interface feeder”.
The functional difference between suspension feeders and deposit feeders indicates that they should have different roles in energy flux (Tsuchiya and Kurihara 1980; Christensen et al. 2000). Obligate suspension feeders take particles from the water column and eject their feces and/or pseudofeces onto the sediments (for mussel see Bjork et al. 2000; for oyster see Hayakawa et al. 2001; and for clam see Jie et al. 2001). It has been reported that deposit feeders eat bacteria and organic contents in decaying cordgrass [Littoraria irrorata (Newell and Barlocher 1993)], decrease chlorophyll a [Yoldia limatula (Ingalls et al. 2000)] and decrease organic matter [Nereis virens (Kristensen and Blackburn 1987); Nucula proxima (Cheng and Lopez 1991)] in the sediment. For interface feeders like B. zonalis, it is important to determine whether they show biodeposition like Nereis diversicolor (Christensen et al. 2000), or have a role that is particularly different from suspension and deposit feeders.
The purpose of this study is to describe the mechanism of suspension feeding of B. zonalis and to estimate the effect of B. zonalis as an interface feeder in comparison to C. cingulata, an obligate deposit feeder in the same habitat. The suspension feeding mechanism in B. zonalis was observed in detail and compared with other suspension feeders. To quantify the effect, changes in concentrations of suspended materials, total nitrogen (TN), total organic carbon (TOC) and the C/N ratio in sediments were measured.
Materials and methods
Collection of gastropods
Observation on the suspension feeding of B. zonalis
The suspension-feeding mechanism of B. zonalis in a petri dish (with seawater) was observed under a stereomicroscope (Olympus SZ1145TR) and recorded using an attached camera (Olympus PM-C35DX). Also, the feeding behaviors of B. zonalis placed in a 500-ml beaker were recorded with a video camera (Sony DCR-VX1000) and single lens reflex camera (Minolta AB800). During these observations, B. zonalis was provided with previously frozen planktonic algae (Nannochloropsis oculata) at 1×106 cells/ml).
Estimation of remaining suspended materials and filtration rate
Snail biomass and estimation of biodeposition
The experiment was run for 10 weeks. Then, B. zonalis and C. cingulata were transferred to filtered seawater more than 24 h to collect their feces, and the wet weights of snail were recorded after this incubation. Feces in filtered seawater were filtered onto pre-combusted and pre-weighed Whatman GF/C filters. The feces on the filters were dried (80°C for 48 h) and weighed, then exposed to fumes of 1 N HCl for 24 h to remove inorganic carbon. Surface sediments from test chambers were collected using slide glass in place of a spatula. Sediment samples were dried (80°C for 48 h) and treated with 2 N or 6 N HCl. After this treatment, the samples were rinsed twice with deionized distilled water and dried again. TN and TOC in the feces and surface sediments samples were measured using a Sumigraph NC-80 NC analyzer (Sumitomo Chemical Company) connected to a GC-8A gas chromatograph and Chromatopac C-R6A recorder (Shimadzu). The C/N ratio was calculated using TN and TOC.
Wet weight of individuals and feces data were analyzed by t-test for comparison between treatments (P<0.05). The Bonferroni-Dunn procedure, a multiple comparison procedure, is attributed to Dunn (1961). The procedure was used for comparison of remaining suspended materials or sediments between control and two treatments.
Suspension feeding behavior of B. zonalis
Remaining suspended materials and filtration rate
The algal suspension in the B. zonalis treatment showed dramatic decreases, and its concentration was 37.9±11.2% (mean±SD) of the initial concentration after 3 h. In the control and C. cingulata chambers, however, there were only slight changes over 3 h, the concentration for the control treatment being 82.3±7.3% while that for the C. cingulata treatment was 91.9±15.2%. There are significant differences between treatments after 3 h (P<0.0167 by the Bonferroni-Dunn test).
Snail biomass and estimation of biodeposition
Batillaria zonalis and Cerithideopsilla cingulata. Comparison of wet weight including shell (g), before and after experiments, using a t-test (P<0.05). Data shown are means±SD (n=20) for all replicates
In this study, we show the suspension feeding process of B. zonalis. This is the first report describing the mechanism of suspension-feeding activity in Batillaria. Suspension feeding in gastropods species is relatively uncommon in comparison to bivalves, and is reported to occur in 37 species (Fenchel et al. 1975; Declerck 1995; Chaparro et al. 2002). A review of such species distinguished three feeding styles (Declerck 1995): (1) ctenidial filter feeding, where particles are filtered from the respiratory current passing through the mantle cavity; (2) mucus-net feeding, where suspended mucus nets are used to take particles from ambient currents; and (2) ciliary-tract feeding, where particles are trapped in ciliated fields on lobes of the foot. B. zonalis is categorized as a ctenidial filter feeder because its ctenidium is used for trapping particles in the respiratory current.
It is hypothesized that suspension feeding developed from gill cleaning mechanisms (Jørgensen 1966). Suspension feedings for B. zonalis and for bivalves [e.g. clams and cockles (Ruppert and Barnes 1994); mussels (Beninger and St-Jean 1997); and pearl oysters (Prouvreau et al. 2000)] are similar in that their gills (ctenidia) are important organs for catching and entangling particles within mucus. However, the feeding and disposing processes are different, as mentioned below. The mouth of a bivalve lies near the gill, and labial palps sort ingested particles, whether into the mouth or out through the out-flow siphon (Brusca and Brusca 1990; Ruppert and Barnes 1994; Morse and Zardus 1997). For disposing of particles, bivalves transport them to the out-flow siphon after sorting. On the other hand, the mouth of B. zonalis lies under part of its head and they have to turn their heads to eat the food cord, including particles. The food cord is elongated from the gills, pooled on the foot and, if uneaten, would be pseudofeces, as observed in this study. It appears that bivalves have a more functional feeding process than B. zonalis, and the feeding process of B. zonalis is secondarily derived from ctenidial cleaning. Their uptake of materials in seawater is so definite that they may be called suspension feeders. B. zonalis might also be called a “modified suspension feeder” because of the involvement of the of food cord in their feeding, in order to distinguish between this feeding process and bivalves’ methods.
Dominant suspension feeders in Tomishiro tidal flats. The values shown are means
Filtration rate (ml g wet weight−1 h−1)
Habitat density (g wet weight/625 cm2)
In situ filtration rate (ml/625 cm2 h−1)
Obligate suspension feeders take particles from the water column and deposit their feces and/or pseudofeces onto the sediments. For example, in mussel (Bjork et al. 2000), clam (Jie et al. 2001) and oyster (Hayakawa et al. 2001), biodeposition increases organic material content in the sediment. Although the interface feeder, Nereis diversicolor, shows biodeposition in the manner of an obligate suspension feeder, it is also known that deposit feeding in this species occurs during phytoplankton-poor periods (Christensen et al. 2000). In contrast, B. zonalis treatments in this study show that the addition of TN and TOC in the sediments occurs at similar levels as in the control treatments. At the same time, however, the C/N ratios in the sediments of the B. zonalis treatment were lower than for the control treatment. These results indicate that the addition of TN and TOC in the B. zonalis sediments are quantitatively similar to controls, but different in quality. It is assumed that increases of TN and TOC in the control treatments were mostly due to physical sedimentation, and occurred when the algal-rich seawater drained through the sediment during the low tide simulation. In contrast, biodeposition in B. zonalis cultures is the most likely cause of increased TN and TOC in their sediments. This is supported by the higher removal of suspended algal material in the B. zonalis treatment, indicating their suspension-feeding activity. Furthermore, settled material on the sediments should be available for adventitious deposit feeding by B. zonalis and it is possible that this deposit feeding limited the accumulation of TN and TOC in sediments. Thus, the TN and TOC levels in sediments of the B. zonalis treatment may implicate both features of suspension and deposit feeding styles. In addition, other bioturbation factors such as foraging and mucus secretion must be considered, but it is likely that these factors are also present in the Cerithideopsilla cingulata treatment.
Deposit feeders, in general, take organic materials from sediments and eject feces onto those same sediments. It has been reported that deposit feeding decreases organic content in sediments (e.g. Kristensen and Blackburn 1987; Cheng and Lopez 1991). On the other hand, it is known also that some types of biodeposition by deposit feeders, such as fecal production and mucus secretion, positively affect microbial biomass (Newell 1965; Riemann and Schrage 1978; Tsuchiya and Kurihara 1979; Davies and Beckwith 1999). In this study, the sediments with C. cingulata show lower values of TN, TOC and C/N than those of the control treatments. The lower TN and TOC results are due to deposit feeding and the lower C/N suggests that the number of bacteria was increasing (Kautsky and Evans 1987). The contents of C. cingulata sediments are probably a result of the antagonistic effects of deposit feeding versus sedimentation and biodeposition. However, the impact of deposit feeding was most probably stronger, given the relatively lower TN and TOC content in C. cingulata sediments. The initial (time 0) culture sediments had a low organic content (Fig. 5). Therefore, materials deposited on the sediment were “fresh” and useful for deposit feeders, and might be one cause of the clear results in sediments inhabited by C. cingulata.
B. zonalis and C. cingulata are considered to show some similarities in their ecological niches, such as inhabiting the upper 5 cm of sediments and foraging on the surface (our observations). However, they differ greatly in feeding modes: B. zonalis is a suspension and deposit feeder and C. cingulata is an obligate deposit feeder. In this study, mode differences were evident, namely the lower algal-suspension content in the 3-h B. zonalis treatment, and the lower TN and TOC accumulation in C. cingulata sediments. The amount of feces can also positively affect the TN and TOC content of sediments. Dry weight, TN and TOC in feces of both species show no significant differences, but B. zonalis did not egest pseudofeces during the incubation time when there were no suspended materials (see “Materials and methods”). Non-suspension feeders, like C. cingulata, produce few pseudofeces, if any. So, B. zonalis sediments were affected by both feces and pseudofeces, while C. cingulata sediments only received fecal material. These feces and pseudofeces also may positively affect microbial biomass on each sediment. Bioturbation by both gastropods yields the same effect on quality of sediments, as indicated by sediments C/N, despite feeding mode differences.
We thank Okinawa Prefectural Land Development Public Corporation and Metocean Environment Inc for a support grant and for laboratory systems. We also would like to express our gratitude to Dr G.C. Fiedler and M. Black for helpful suggestion on English terms. Many grateful thanks are due to Dr. S. Ohgaki and an anonymous reviewer for their valued suggestions and comments.