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Density-dependent consumer effects on resource quality in carbonate sediments.

ABSTRACT. -- Density-dependent mound-building activity by a burrowing shrimp (Callianassa branneri) results in a positive feedback on resource quality in Bermudian sediments. The intense mound-building activity of these shrimp can change their habitat drastically by reducing the areal extent of seagrass beds and increasing the grain size of sediments. These changes allow for replacement of refractory low quality food resources (seagrass detritus) with a high quality food resource (diatoms). Higher concentrations of the diatom pigment marker, fucoxanthin, were found in the high Callianassa densities, indicating higher standing stocks of diatoms. The extent to which diatom "gardening" can occur is largely dependent upon callianassid density (estimated from mound number), and thus mound-building activity, in an area. Density-dependent positive feedbacks between consumers and their resources also may act to stabilize populations over time, within a particular range of densities above which negative effects take over. Key words: high performance liquid chromatography (HPLC); Callianassa; benthic diatoms; resource supply; positive feedback.

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The concept of density-dependent population regulation has persisted as one of the major topics of debate in ecology for more than three decades (see reviews by Hassell, 1986, and Wolda, 1989). Much of the debate that exists in the literature today involves semantic disagreements; however, there appears to be a general consensus that both density-dependent and density-independent processes are important in regulating populations (Hassell, 1986). A broad spectrum of density-dependent feedback processes, such as competition for food, can act on population regulation. For example, it is generally thought that the amount of resource supply to an individual consumer within a population decreases as population density increases (May, 1981; Pianka, 1988). However, more recent studies have demonstrated density-dependent positive feedbacks (in asocial animals), which show an increase in resource supply to the individual consumer at higher population densities (see review in Bianchi et al., 1989). The mechanisms for such feedbacks are varied and can occur in quite divergent systems (Bianchi and Jones, 1991). For example, some mechanisms may involve direct effects on the productivity of the resource or indirect effects that could alter abiotic processes, which then result in an increase in resource supply.

In soft-bottom marine communities, bioturbation (biotic disturbance) resulting from the activities of macrobenthos (animals retained on a 500-[micro]m sieve) can drastically alter the physical and chemical properties of sediments (Rhoads, 1974; Schink and Guinasso, 1977; Aller, 1978; Rice, 1986; Rice et al., 1986). Moreover, the feeding activities of macrobenthic deposit feeders (animals that feed by ingesting sediment) can alter the abundance, metabolic activity and composition of the microbial community (Hargrave, 1970; Morrison and White, 1980; Bianchi and Levinton, 1981), which in turn can be linked (through nutrient cycling, for example) with density-dependent consumer effects on resource quality and supply.

To fully understand the trophic dynamics of macrobenthic food webs, it is necessary to be able to accurately identify resources. Plant pigments can be used to describe the distribution and composition of organic matter sources in sediments (Daley and Brown, 1973; Watts et al., 1977; Repeta 1989; Bianchi and Findlay, 1990). The degradation products of certain pigments have been used as indicators of feeding activity in trophic studies (Shuman and Lorenzen, 1975; Welschmeyer and Lorenzen, 1985; Hawkins et al., 1986; Bianchi et al., 1988).

In this paper, plant pigments are used as tracers of organic matter to investigate how density-dependent bioturbation by burrowing shrimp (Callianassa sp.) can alter resource quality. Although many studies have documented the importance of bioturbation by Callianassa sp. in sediment transport (Shinn, 1968; Clifton and Hunter, 1973; Aller and Dodge, 1974; Pemberton et al., 1976, Hines and Lyons, 1982; Waslenchuk et al., 1983, Tudhope and Scoffin, 1984; Swinbanks and Luternauer, 1987), little is known about the feeding ecology of these animals. Burrowing shrimp (Callianassa sp.) are among the most prolific bioturbating invertebrates in the marine environment; it has been estimated that these shrimp can process up to 2.59 kilograms per square meter per day (Suchanek, 1983). These animals provide an excellent opportunity to investigate the relationship between density-dependent feedback mechanisms and resource supply.

MATERIALS AND METHODS

Study Area and Organism

The study area was located at Coot Pond, Bermuda (Fig. 1), an intertidal flat on St. George's Island. Coot Pond is a shallow (half a meter to two meters) semi-enclosed basin with approximately 40 percent of the bottom heavily bioturbated by Callianassa sp. activity; the remainder of the bottom is covered by seagrasses (Thalassia testudinum and Syringodium filiform) and a variety of macrophytic algae (Waslenchuk et al., 1983). Black mangrove (Avicennia nigrans) is the dominant tree species that borders much of the pond's perimeter.

Burrowing shrimp of the genus Callianassa (Decapoda, Thalassinoidea), which can burrow to three meters in depth, have widespread occurrence in both temperate and tropical sediments (Pemberton et al., 1976; Suchanek, 1983). C. branneri is the mound-building deposit-feeding species (Biffar, 1971) that I will concentrate on in this study. This shrimp generally excavates a volcano-shaped mound of sediment at the top of its burrow system (60 centimeters in height by about 80 centimeters in diameter).

Field Sampling

I sampled Coot Pond sediments in the summer of 1989 along two transects in areas having distinct differences in C. branneri abundance. Because of the extreme difficulty in capturing these animals, mound density was used as an estimate of population density. The pond is composed of two distinct areas of low (transect I, 0.5 mounds per square meter) and high (transect II, five to six mounds per square meter) C. branneri densities. A transect (having three stations, A, B, C) was sampled in each of the two areas (Fig. 1). Sediment cores were collected using hand-held corers along each of the transects. Sediment cores were extruded and sectioned at one-centimeter intervals down to nine centimeters. Fresh intact fecal pellets were collected from the surface of the mounds with a spatula. Percent organic matter in sediments was calculated by measured weight loss after combustion at 550[degrees]C for 12 hours. All remaining samples were kept frozen for determination of plant pigment composition using reversed-phase high-performance liquid chromatography (HPLC).

[FIGURE 1 OMITTED]

Pigment Analysis

Plant pigment concentrations in Coot Pond sediments were used to determine dominant organic matter sources to the sediment and the general diet of C. branneri. Sediments were extracted for plant pigments using 100 percent acetone. Pigments were determined by ionpairing, reversed-phase HPLC, using the methods of Mantoura and Llewellyn (1983) as modified by Bianchi et al. (1988). Using these methods, I was able to achieve pigment resolution for all pigments of interest relating to sediment resources and Callianassa diet (Fig. 2). Information on the pigment standards, extinction coefficients, and calculations used for quantification of pigments can be found in Bianchi et al. (1988). Identification of all pigments was confirmed by comparing absorption spectra with a Waters 990 photo diode-array detector with that of published values (Davies, 1976; Braumann and Grime, 1981; Mantoura and Llewellyn, 1983; Wright and Jeffrey, 1987).

Statistical Procedures

An Fmax test was used prior to ANOVA analyses to check for homogeneity of variances. A two-way nested ANOVA was used to test the effects of Callianassa mound density (group level), station, and sediment depth (subgroups) on plant pigment concentrations. When transect differences were significant (P <0.05) by ANOVA, an a posteriori least significant difference (LSD) test was performed on station means (Sokal and Rohlf, 1981).

[FIGURE 2 OMITTED]

RESULTS

Sediment Characteristics

Sediments from transects I and II had an average organic matter content ranging from three to seven percent of dry weight (Fig. 3). Density of C. branneri significantly affected (P <0.05) percent organic matter in Coot Pond sediments (Fig. 3). Percent organic matter was significantly higher (P <0.05) at stations IIB and IIC, along the high density C. branneri transect, than at transect I stations (Fig. 3).

Plant Pigment Tracers

Concentrations of chlorophyll c, fucoxanthin, chlorophyll b, and total phaeophorbide were significantly different (P <0.05) along transects I and II in Coot Pond sediments (Figs. 4-7).

Stations IIB and IIC, along the high density C. branneri transect, had significantly (P <0.05) higher concentrations of chlorophyll c, in the top 1.5 centimeters, than all stations along transect I (Fig. 4). Similarly, concentrations of the carotenoid, fucoxanthin, were also significantly higher (P < 0.05), in the top 1.5 centimeters, at the high density C. branneri stations than at the low density stations (Fig. 5). Chlorophyll b concentrations at stations IB and IC were significantly higher (P < 0.05), in the top 1.5 centimeters, than at all transect II stations (Fig. 6). Total phaeophorbide concentrations were significantly higher (P < 0.05), in the top 1.5 centimeters, at stations IIB and IIC than at all the transect I stations (Fig. 7).

[FIGURE 3 OMITTED]

DISCUSSION

High levels of mound-building activity (bioturbation) by C. branneri can drastically alter the composition of potential food resources. Along transect II, where C. branneri densities are high (about five to six mounds per square meter), the abundance of living seagrasses and macroalgae adjacent to mounds is low. It has been suggested that the activity of mound building by Callianassa either physically smothers the plants or reduces the available light for photosynthesis in higher plants, because of sediment resuspension (Suchanek, 1983). Suchanek (1983) demonstrated these amensalistic effects on plants by experimental field manipulation of seagrass nodes in areas of high and low Callianassa densities. Unlike seagrasses, benthic diatoms are capable of maintaining a high enough turnover rate to keep up with the mound-building activity of Callianassa. However, in another similar study it was found that the burrowing activity of C. kraussi dramatically changed the depth distribution of diatoms but did not produce a density-dependent increase (Branch and Pringle, 1987). These differences may be attributed to variability in the motility of benthic diatom species found at these study sites. Benthic diatoms are generally tolerant of low light regimes and, if motile, can migrate vertically in the sediment thus avoiding burial (Admiraal, 1977; Admiraal and Peletier, 1980). Chlorophyll c and the carotenoid, fucoxanthin, are markers for the presence of diatoms (Wright and Jeffrey, 1987); I found higher concentrations in the area of intense mound-building activity (Figs. 4 and 5). It appears that in areas of high Callianassa activity, a "garden" of benthic diatoms is maintained at the sediment surface in the absence of higher plants (seagrasses). The lower chlorophyll b concentrations in these sediments indicate something close to a monoculture of diatoms (Fig. 6), because diatoms do not contain chlorophyll b.

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

Phaeophorbide, a degradation product of chlorophyll, is considered to be a good indicator of metazoan grazing activity (Shuman and Lorenzen, 1975; Carpenter and Bergquist, 1985; Welschmeyer and Lorenzen, 1985; Bianchi et al., 1988). Higher total phaeophorbide concentrations at the high density C. branneri stations indicate more grazing activity (Fig. 7). Fucoxanthinol, which is a degradation product of fucoxanthin, provides evidence of grazing on diatoms. Fresh fecal pellets collected from C. branneri surface mounds in the high-density region (II) had dominant fucoxanthinol peaks, indicating the importance of diatoms (which are the primary sources of fucoxanthin) as a food resource (Fig. 2). Zeaxanthin also appears as a dominant peak in C. branneri fecal pellet pigments, indicating the presence of blue-green algae, as a potential food resource (Fig. 2). These results support the idea that organic matter on the slopes of Callianassa mounds, in this case diatom mats, can be recycled down into burrows and utilized as a food resource (Suchanek, 1983).

[FIGURE 6 OMITTED]

High population densities of C. branneri have a positive density-dependent feedback on the quality of their food resources. Because of the negative relationship between seagrasses and mound-building activity by Callianassa, high population densities of these animals are able to "garden" a higher-quality resource (diatoms) than at lower densities. Benthic diatoms are believed to be one of the highest quality food resources available for deposit-feeding macrobenthos (Fenchel and Kofoed, 1976; Jensen and Siegismund, 1980; Levinton and Bianchi, 1981; Bianchi and Levinton, 1984; Bianchi and Rice, 1988). At the lower-density C. branneri stations, most of the available food resource is in the form of seagrass detritus, which is more refractory (higher lignin content) and generally lower in food quality for most deposit-feeders (Levinton et al., 1984; Lopez and Levinton, 1987).

[FIGURE 7 OMITTED]

This density-dependent positive feedback, between C. branneri and diatoms, also may result in a greater supply of resources per individual. The major changes associated with callianassid mound-building activity that allow for greater production of diatom resources are losses of seagrass beds and an increase in sediment grain size. In a recent study, it was demonstrated that increased grain size can allow for greater diffusion of nutrients from depth to diatoms at the sediment surface, resulting in increased production (Bianchi, 1988; Bianchi and Rice, 1988). Furthermore, this increase in diatom production, which was linked to a density-dependent positive feedback, resulted in an increase in the amount of resource (diatoms) per individual consumer (polychaetes) (Bianchi and Rice, 1988). Similarly, although not measured in this study, the amount of diatom supply to an individual callianassid is likely to be higher in the high-density areas where the "garden" of diatoms is more developed. It also has been shown that the flux of phosphorus from depth up through the sediment-water interface was enhanced in the presence of Callianassa mound-building activity in Coot Pond sediments (Waslenchuk et al., 1983). These nutrients are likely to be important to algae at the sediment surface; recent evidence suggests that plants in marine carbonate sediments are phosphorus limited (Carpenter and Capone, 1981; Powell et al., 1989; Short et al., 1990). Certainly, as predicted in the feedback model of Bianchi et al. (1989), populations are constrained to upper limits by intraspecific competition. Factors that control these limits will be affected by the feedback mechanism involved and the intrinsic constraints of the system (Bianchi and Jones, 1991).

Positive feedbacks may affect the stability of populations over time. C. branneri densities at the high-density stations reported here are not different from the densities reported by Waslenchuk et al. (1983) at the same site. Results of other studies also have revealed year-to-year stability among populations of deposit-feeding macrobenthos where similar density-dependent feedbacks were operating (Rice, 1986; Bianchi and Rice, 1988). Co-existing macrofauna also may benefit from feedback systems; higher densities of other deposit-feeding taxa (for example, polychaetes) were found in sediments with high C. branneri densities than in the low-density seagrass area of Coot Pond (F. C. Dobbs, personal communication). It generally is thought that Callianassa species have a negative influence on other faunal groups (Suchanek, 1983; Riddle et al., 1990). Recent work also shows that the size-class of animals co-existing within regions of intense callianassid activity (predominantly polychaetes) appear to be dominated by smaller animals--animals passing through a two-millimeter sieve but retained on a half-millimeter sieve) (Riddle et al., 1990). Many of these animals are quite resilient to change, and thus can live within and between the mounds of Callianassa, allowing them to reap the benefits of a high quality food resource (diatom "garden"). Unlike larger macrofauna, such as Limulus sp. (horseshoe crab), the activity of smaller animals may be less likely to disrupt the coupling mechanism of the feedback in such heavily bioturbated systems.

ACKNOWLEDGMENTS

I would like to thank Bertrand Boeken, Stuart Findlay, Clive Jones, and Richard Ostfeld for critical comments, and JoAnn Bianchi for her invaluable assistance in the laboratory. This work was supported by a Grant-in-Aid from the Bermuda Biological Station and the Mary Flagler Cary Charitable Trust. This article is a contribution to the program of the Insitute of Ecosystem Studies.

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THOMAS S. BIANCHI

Institute of Ecosystem Studies, The New York Botanical Garden, Millbrook, New York 12545

Present address: Department of Biology, Lamar University, Beaumont, Texas 77710.
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Author:Bianchi, Thomas S.
Publication:The Texas Journal of Science
Date:Aug 1, 1991
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