2007 SOUTHEASTERN NATURALIST 6(2):351–358 Deposit Feeding During Tidal Emersion by the Suspension-feeding Polychaete, Mesochaetopterus taylori Thomas O. Busby1 and Craig J. Plante2,* Abstract - Observations on tidal flats in North Inlet, SC suggested facultative suspension- and deposit-feeding in the chaetopterid polychaete, Mesochaetopterus taylori. Fecal coils consisted of two disparate sections, the first composed of small, brown fecal pellets wrapped together by mucus into long strands, which abruptly transitioned into a second gray, ropy section. We also made direct observations of exposed palps and probing of the sediment surface intermittently following tidal emersion. Granulometric analyses of gray and brown fecal material, surficial sediments, subsurface sediments, and materials in suspenson above the worm at high tide, corroborate our field observations that M. taylori is a facultative feeder, switching from suspension- to deposit-feeding with tidal emersion. Typically, this shift in feeding mode is not thought to effect a fundamental change in diet, i.e., the same materials are ingested, suspended or deposited depending on hydrodynamic regime. In contrast, M. taylori ingests finer particulates during tidal immersion, with concomitant differences in granulometric characteristics. The distinct provenance and composition of the dietary components of M. taylori likely supplies a relatively broad range of essential nutrients. The geophysical effects of M. taylori feeding are likely profound, in that it both translocates subsurface sediment to the surface during deposit feeding and deposits fine, suspended materials following filter-feeding. Introduction Many of the most important feeding guilds of aquatic animals are uncommon to terrestrial habitats, and are therefore unfamiliar to many casual observers. These include deposit- and suspension-feeders, those animals that feed on particulates deposited on the bed or suspended in water, respectively. Facultative suspension-feeding refers to an ability to switch between these two modes, often associated with changes in water flow velocity (Taghon et al. 1980). A clear-cut distinction between these two feeding modes is probably unrealistic, however, because suspended and settled particulates comprising these diets often are qualitatively similar (Snelgrove and Butman 1994, Taghon et al. 1980). The ability to shift feeding modes may be an adaptation to their variable environment (Miller and Sternberg 1988, Taghon et al. 1980), as it could be advantageous for an animal to adjust its feeding behavior to utilize food in suspension or deposited on the bottom, depending on the dominant source of food at a particular time. Switching feeding behavior may also reduce intraspecific competition in dense assemblages (Levin 1981). 1Biology Department, College of Charleston, Charleston, SC 29401. 2Grice Marine Laboratory, 205 Fort Johnson, Charleston, SC 29412. *Corresponding author - plantec@cofc.edu. 352 Southeastern Naturalist Vol. 6, No. 2 Numerous benthic organisms, including representatives of the spionid, nereid, sabellid, and oweniid polychaetes, tellinid bivalves, and amphipod crustaceans, are known to be capable of both suspension- and depositfeeding (Taghon et al. 1980). Chaetopterid polychaetes are generally suspension-feeders, employing a mucous net apparatus to filter organic particles from seawater pumped into their straight, vertically oriented tubes (Fauchald and Jumars 1979, Sendall et al. 1995). Fecal matter is carried anteriorly along a mid-dorsal ciliated groove. The principal function of chaetopterid palps is thought to be for the ejection of fecal pellets and debris (Barnes 1965). In nearshore South Carolina habitats, common chaetopterids include Chaetopterus variopedatus (Renier), Spiochaetopterus oculatus (Webster), and Mesochaetopterus taylori (Potts), with only S. oculatus known to employ both deposit- and suspension-feeding (Fauchald and Jumars 1979, Turner and Miller 1991). The present study reports on the feeding behavior of the chaetopterid, Mesochaetopterus taylori. This polychaete can reach high densities (up to 70 m-2) in intertidal areas (Sendall et al. 1995), but is patchy in distribution along the southeast US coast (Fox and Ruppert 1985). Like other chaetopterids, this species resides beneath the sediment surface and so is rarely seen; evidence of its presence is provided by a sandy, cylindrical tube, which projects vertically above the sediment-water interface. It is generally considered to be less common than other chaetopterids on southeastern coasts (e.g., Chaetopterus and Spiochaetopterus; Ruppert and Fox 1988). However, its tube resembles that of the common onuphid polychaete, Kinbergonuphis jenneri (Gardiner); thus, its abundance might be greatly underestimated due to this similarity. Observations on the Debidue River tidal flats in North Inlet, SC (33°21'0"N, 79°11'27"W) suggested facultative feeding in this species in that we noted that its fecal coils seemed to consist of two disparate sections. One section was brown and was composed of small, distinct fecal pellets wrapped together by mucus into long coils. These coils abruptly changed into gray, ropy coils, more reminiscent of the egesta of arenicolid polychaetes and hemichordates (Fig. 1). The spatial orientation of these coil sections suggested that the brown pellets, probably processed suspended matter, were egested first. Gray material was egested later, typically after > 60 minutes of tidal exposure, and likely represented materials that were ingested via deposit feeding just after emersion. This speculation was supported by direct observation of exposed palps, apparent probing of the sediment surface, and movement of collected sediment toward the mouth (Fig. 2) intermittently following tidal emersion. Most documented facultative feeding has been shown in flume experiments; however, in some instances, switching in feeding modes may have been artifactual due to use of unrealistic flow velocities (Barnes 1964, Turner and Miller 1991). In addition, M. taylori lives in deep burrows, and it has proven exceedingly difficult to collect intact specimens for experimentation 2007 T.O. Busby and C.J. Plante 353 (Barnes 1965, Petersen 1966). Instead, we tested for facultative feeding in M. taylori by comparing geological and biological characteristics of the two dissimilar fecal sections, in addition to those of surrounding surface sediment, subsurface sediments, and suspended particulate materials in waters overlying the worms at high tide. Methods All samples were collected during a 􀂧 4-hour period surrounding low tide while the sandflat was emersed. The first step in the sampling process was to identify and flag specimens of M. taylori that showed signs of recent feeding (i.e., tube apertures surrounded by small, packaged, brown pellets). All egesta samples and surface sediment samples were collected from one small area (􀂧 20 m non-vegetated zone between creek and Spartina alterniflora Figure 1. Fecal coils of Mesochaetopterus taylori exhibiting two distinct sections, differing in color and composition. Figure 2. Deposit feeding at sediment surface by M. taylori at low tide. 354 Southeastern Naturalist Vol. 6, No. 2 marsh, along < 100 m of shoreline) using clean spatulas and pipettes. Fecal or sediment samples were pooled to obtain individual replicates, each of at least 1 ml of material. Number of replicates ranged between 5 and 7 for the various sample types. Deeper sediment samples (􀂧 5 cm) were collected using a corer (30-ml plastic pipette with dispensing end cut off). Several liters of the nepheloid layer also were collected using a sterile 1-L filtering flask (with tubulation) with 􀂧 1 m of sterile tubing attached. The intake end of tubing was held 0.5–1 cm above the sediment surface (approximate height of M. taylori tube), with tube opening facing directly upward into the highly turbid water column. Suction was applied, and water flowed into the flask. Samples were placed on ice for transport to the laboratory where material that was suspended in water was separated using centrifugation (10 min at 4000 x g). Using copious amounts (> 3 L) of distilled water, samples were washed through a series of eight small (􀂧 50-mm diameter) sieves of mesh sizes of 1000, 500, 355, 250, 180, 125, 90, and 63 mm. Fractions collected on each sieve were then washed under pressure onto pre-dried (> 2 h at 60 ºC) and pre-weighed glass fiber filters (Millipore, Bedford, MA). Material passing through the 63-mm sieve was also collected. Filters with sample were then dried at 60 ºC (at least overnight) and re-weighed. Measures of median grain diameter were obtained from graphical analysis of cumulative frequency curves. In addition, the degree of scatter (or quartile deviation) and data asymmetry around the median (i.e., skewness) were obtained according to Buchanan and Kain (1971). Percent silt/clay was calculated as the percent of total mass comprised of material passing through the smallest (63-mm) sieve. One-way ANOVA was used to compare granulometric attributes among sample types. When significant (􀁟 = 0.05) global differences were noted, pairwise comparisons were conducted using Fisher’s LSD correction. Results Grain-size analysis revealed significant global differences in median grain diameter (Md􀁱; F4,24 = 231.26, P < 0.001), quartile deviation (QD􀁱; F4,24 = 4.32, P < 0.009), and skewness (Skq􀁱; F4,24 = 6.90, P < 0.001). Median grain size in all sample types was significantly larger than in the nepheloid layer (P < 0.001 for all such comparisons, Fisher’s LSD; Table 1). Otherwise, only the surface and subsurface sediments differed, with deeper sediments significantly coarser (P = 0.022), whereas all other pairwise grain-size comparisons were not significant, P > 0.107). Surface sediment and brown fecal casts were more poorly sorted (i.e., larger spread between 25 and 75% points on the cumulative frequency curve, QD􀁱) than the other three sample types (Table 1; P values ranged between 0.002 and 0.089 for all pairwise comparisons), and did not differ from one another in this regard (P = 0.606). The nepheloid layer showed the lowest QD􀁱 (Table 1), but was not significantly different than either subsurface sediment (P = 0.405) or the 2007 T.O. Busby and C.J. Plante 355 gray fecal casts (P = 0.292). The nepheloid samples also deviated from all other sample types in that the only negative Skq􀁱 values were from these samples. Subsurface sediments and gray fecal casts again resembled one another in this aspect (P = 0.859), and differed from surface sediment and brown fecal casts (P < 0.041 for all four cross-comparisons), whereas surface sediment and brown casts were not significantly different (P = 0.823). The % silt/clay fraction (< 63 mm grain size) differed globally (F4,24 = 147.69, P < 0.001) and among various sample types (Table 1). While gray fecal coils differed from both brown fecal material (P = 0.028) and surface sediments (P = 0.010), % silt/clay was not significantly different than the deeper sediment samples (P = 0.663). Brown feces differed in this regard from subsurface sediments (P = 0.008), but were not significantly different than surface sediments (P = 0.725). Again, the nepheloid layer differed from all other sample types, with a much higher fraction of fine grains (P < 0.001 for all pairwise comparisons; Table 1). Discussion In sum, the material ingested during suspension-feeding most closely matched the brown, fine materials collected as surface deposit at low tide. This material shared some qualities with the nepheloid layer, but it appears that the finest fraction of this seston is not deposited during the tidal ebb, so is not sampled as surface deposit at low tide. After emersion, M. taylori deposit feeds on coarser material. Observation of feeding activity suggests that these deposits lie just below this surficial fluff layer. However, we cannot rule out the possibility that M. taylori also feeds from the opposite end of its tube during this interval, on much deeper sediments. Analogous comparisons of chlorophyll concentrations, and bacterial community structure (C.J. Plante and T.O. Busby, unpubl. data) similarly matches brown fecal coils with seston, and subsurface sediments to that ingested at low tide. Table 1. Mean (± SD) of granulometric properties of various sample types (FC = fecal casts). Md􀁱, QD􀁱, and Skq􀁱 refer to median grain size, quartile deviation, and skewness, respectively. Sample type Md􀁱 QD􀁱 Skq􀁱 % silt/clay Brown FC 2.91 (0.13) 0.43 (0.23) 0.13 (0.12) 15.6 (11.0) (133 􀂗m)A Gray FC 2.88 (0.01) 0.25 (0.03) 0.03 (0.02) 4.8 (1.2) (136 􀂗m) Surface sediments 2.95 (0.19) 0.39 (0.20) 0.12 (0.10) 17.2 (10.1) (129 􀂗m) Subsurface sediments 2.80 (0.05) 0.23 (0.02) 0.02 (0.01) 2.8 (1.4) (144 􀂗m) Nepheloid layer 4.31 (0.02) 0.16 (0.04) -0.05 (0.03) 86.3 (6.8) (50 􀂗m) AMedian grain sizes were converted from 􀁱 units to diameter (in 􀂗m) using the equation: d = antilog10(-0.30103􀁱). 356 Southeastern Naturalist Vol. 6, No. 2 Sedimentological analyses corroborate our field observations that M. taylori is a facultative feeder, switching from suspension- to deposit-feeding with tidal emersion. This capacity to both suspension- and deposit-feed is not novel, having previously been noted in at least one species, Spiochaetopterus oculatus, of the same polychaete family (Chaetopteridae), and is even more familiar among spionid polychaetes, tellinid bivalves, and varied crustaceans. However, unlike these other invertebrates that primarily deposit-feed, but may switch to suspension-feeding at high flow velocity, M. taylori is typically classified as a suspension-feeder. This switching behavior is also unusual in that the switch is not due to change in water velocity, but rather to fluctuations in tidal height (i.e., emersion). In addition, switching in most facultative feeders is not thought to represent a fundamental switch in diet, i.e., the same materials are thought to be ingested, simply suspended or deposited depending on flow (e.g., Taghon 1980). With M. taylori, on the other hand, finer particulates are ingested during tidal immersion, with concomitant differences in granulometric characteristics. Large-scale spatial distributions of benthic fauna have largely been explained by the notion that the suspension-feeding guild dominates where water velocity is relatively high and the flux of suspended matter is adequate, whereas deposit-feeders should be more abundant where flow is reduced and organic particulates are deposited on the sea bed. Facultative feeders defy this simple scheme and illustrate that flow is variable to greater or lesser degrees, so the dominant mode of feeding in a given habitat can vary temporally. Earlier work has demonstrated facultative deposit-feeding, which has lead to predictions that “switching” between feeding modes should occur in dynamically variable benthic habitats (Taghon 1980, Turner and Miller 1991), for instance, when flow is oscillatory or when the average rate of flow varies significantly through time. During periods of reduced flow, deposit-feeding is predicted. Mesochaetopterus taylori provides an extreme example of this situation, as there is obviously no flow of seawater to carry suspended matter to them at low tide. The ability to continue deposit-feeding after emersion is an adaptation to intertidal life and potentially provides a competitive advantage to M. taylori in this habitat, as most supension feeders cease feeding during aerial exposure (Newell 1972). Perhaps even more important, the disparate dietary components (with respect to both provenance and composition) of M. taylori should supply a relatively broad range of essential nutrients and remedy the nutritional deficiencies of specific detrital components (Phillips 1984). Deposit feeding has been shown to alter sedimentary microbial communities, both through translocation of sediments (Plante and Wilde 2004) and digestive removal (Dobbs and Guckert 1988, Plante and Wilde 2004). It has not yet been established if the quantitative or qualitative effects of various deposit-feeding species are unique or are generally similar (Plante and Shriver 1998, Plante and Wilde 2004). The compositional effects on the microbiota of bulk sediment of M. taylori are likely unique and particularly 2007 T.O. Busby and C.J. Plante 357 great, in that it both translocates subsurface sediment to the surface during deposit feeding and deposits fine, suspended materials following filter feeding. Geophysical effects may even be more significant, for similar reasons. On one hand, the worm brings subsurface sediments to the surface, defecating this material in coils that project into the benthic boundary layer, enhancing their resuspension when the tide returns. On the other hand, fine, suspended particles are removed from the nepheloid layer and packaged into mucus-bound pellets, and deposited in relatively large coils. Acknowledgments Field assistance was provided by Jeremiah Easley and Jason Curry. Primary funding was provided through the National Science Foundation grant DEB 0108615. Additional support was provided to T.O. Busby by the College of Charleston Biology Department’s fund for undergraduate research. Literature Cited Barnes, R.D. 1964. Tube-building and feeding in the chaetopterid polychaete, Spiochaetopterus oculatus. Biological Bulletin 127:397–412. Barnes, R.D. 1965. Tube-building and feeding in the chaetopterid polychaetes. Biological Bulletin 129:217–233. 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