Influences of predatory polychaetes and epibenthic predators on the structure of a soft-bottom community in a maine estuary

J. Exp. Mar. Biol. Ecol., 1984, Vol. 81, pp. 115-145 Elsevier

115

JEM 324

INFLUENCES OF PREDATORY POLYCHAETES AND EPIBENTHIC PREDATOR

ON THE STRU~URE

OF A SO~-~~OM

CO~UN~

IN A MAINE ESTUARY

WILLIAM

G. AMBROSE, JR.’

University of North Carolina, Cuwimhm in Marine Sciences, Chapel Hill, NC 27514, U.S.A

Institute of Marine Sciences, Morehead City, NC 28557, U.S.A.

Abstract: Field manipulations were used to determine the importance of two predatory polychaetes, Nere2s virens Sars and GZyceradibrunchiata Ehlers, and epibenthic predators in structuring an intertidal soft-bottom community in Maine. Epibenthic predators were excluded from portions of the soft bottom using cages which also enclosed elevated densities of the predatory polychaetes. The experiments ran 10 wk and 20 wk beginning in June 1979. Exclusion of epibenthic predators had no effect on infaunal densities after 10 wk but produced ;2:IJ-fold increase in total density after 20 wk. Since gulls (Lams spp.) avoided all cages, including those not designed to exclude epibenthic predators, the effect of gull predation on infaunal abundances was not tested using exclusion cages. Crabs, Carcinus maenas (Linnaeus) and Cancer irrorutus Say were observed in cages not designed to exclude predators. Densities of Nephtys in&a Malmgren, Poiydora ZigniWebster, Streblospio benedicti Webster, Scoloplos robustus Verrill, phyllodocids, and bivalves were highest in cages containing elevated Glycera dibranchiata density and lowest in cages containing elevated NereL virens density. N. virens was the only taxon whose abundance was reduced in the presenci of Glycera dibranchiata which may account for high infaunal densities in the G. dibranchiata treatment. Laboratory experiments demonstrated that G. dibranchiata are capable of preying on Nereis v&ens. Additional field experiments revealed that the presence of N. virens reduced the abundance of some taxa within the tirst 10 days of colon~ation. N. &ens may have reduced infaunal densities by predation andjor disturbance at the sediment surface. These results suggest that complex interactions within the infauna are important in structuring marine soft-bottom communities. Key words: benthic; community; infaunal predation; polychaeta; Maine

Knowledge of the processes st~ct~ng co~unities has been largely acquired by manipulating the distributions and abundances of species in the field (Connell, 1975). These manipulative experiments have been particularly successful in marine rocky intetiidal communities, where they have demonstrated the importance of competition, predation and physical disturbance in determining species distribution and abundance patterns (see review by Menge & Sutherland, 1976). In the rocky intertidal, both biological (Connell, 1961a, b, 1970; Paine, 1966) and physical (Dayton, 1971) disturb’ Present address: Universitetet i Oslo, Institutt for ~a~nbiolo~ Oslo 3, Norway. 0022-0981/84/$03.00 0 1484 Elsevier Science Publishers B.V.

og Limnologi, Postboks 1064, Blindem,

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WILLIAM

G. AMBROSE,

JR.

ance can prevent dominant competitors from monopoliz~g the potenti~ly limiting resource, space, and excluding other species from the community. The role that disturbance plays in promoting the coexistence of competing species is not confined to rocky intertidal communities but has also been demonstrated in a variety of other systems (Harper, 1969; Dodson, 1970; Sprules, 1972; Connell, 1978). When predation, a major type of biological disturbance, is eliminated from marine soft-bottom communities, however, the predicted exclusion of inferior competitors does not occur (see review by Peterson, 1979). Competitive exclusion may fail to occur foilow~g the exclusion of large epibenthic predators either because inte~erence and exploitation competition are ineffective or because densities are still maintained below the carrying capacity of the environment by adult-larvae interactions (Peterson, 1979). These experiments in soft-bottom communities have excluded large epibenthic predators, such as fishes, shrimps, crabs, and birds, but have failed to remove predators which live within the sediment. A review of caging literature shows that suspected predators among the infauna become proportionally more abundant following the exclusion of large epiben~ic predators (Ambrose, 1984a). Predation from predatory infauna (largely polychaete and nemertean worms) may help explain the failure of a competitive dominant to become established in soft substrata in the absence of epibenthic predators. Previous studies demonstrated that predatory infauna can influence infaunal densities (Reise, 1979; Wiltse, 1980; Commito, 1982; Oliver etal., 1982; Kent & Day, 1983). In these studies, however, the infaunal community was often disturbed (Reise, 1979) or destroyed (Commito, 1982; Oliver et al., 1982) making it difficult to assess the influence of predatory infauna in stN~t~ng natural communities. Predatory infauna may play the role of intermediate predator in soft-bottom communities serving as both prey for epibenthic gredators and predator of infauna (Ambrose, 1984a). In this study, field manipulations were used to test the hypotheses that the predatory polychaetes Nereis virens Sars and Glycera dibranchiata Ehlers are preferred prey for epibenthic predators and that predation by these polychaetes is important in determining the abundances of other infaunal species.

METHODS

The site studied was a mudflat 10 miles upstream from the mouth of the Sheepscot River at the town of Wiscasset, Maine (Fig. 1). The average tidal range in this area is 3 m and the experiments were located at 0.3 m above mean low water. The sediments are fine grained and poorly sorted with 90% by weight falling in the silt-clay category as determined by pipette analysis (Folk, 1980) of four 5.7 cm’ x 5 cm deep cores taken on 25 August 1979. During the June to October experimental period, water temperature ranged from 12-19 “C (determined from approximately weekly measurements of river surface water at low tide during 1979). During the same period, river salinity at the experimental site typically ranges from 26-29x, (Creaser unpubl. data, Maine Department of Marine Resources).

PREDATION BY POLYCHAETES AND EPIBENTHIC PREDATORS

117

GYpera ~~ranch~~a (hereafter Glycera) and Nereis vitem (hereafter Nereti) were used as the predatory polychaetes in the experiments. Nere~~ is usuahy considered an omnivore based on the recovery of algal fragments, bivalves and amphipod parts from

Fig. 1. Location of site studied in relation to the coast of Maine and the Sheepscot River and map of experimental site.

guts (Creaser unpubl. data; Fauchald & Jumars, 1979). Gt’ycera may be capable of deposit-feeding (Klawe & Dickie, 1957; Adams & Angelovic, 1970; Fauchald & Jumars, 1979), but guts have been found to contain polychaete, amphipod and isopod parts (Creaser, pers. comm.). CAGING EXPERIMENT

The importance of Nereif and G&era in influ~cing ~faun~ abund~ces and as prey for epibenthic predators was tested by simultaneously varying the densities of Nereis and Glyceru and controlling the presence and absence of epibenthic predators. This experiment involved excluding epibenthic predators from portions of the soft-bottom community and enclosing and maintaining high densities of the predatory polychaetes within the community. Enclosures were constructed by removing the bottoms from

118

WILLIAM

G. AMBROSE,

JR.

plastic buckets (36 cm high by 28 cm inside diameter, 0.06 m2 top area). A 5 cm high strip’of DuPont VEXAR (6-mm mesh) was attached around each bucket’s rim using stainless steel wire threaded through holes drilled 1 cm below the rim. Strips supported VEXAR cage tops (6-mm mesh) above the sediment surface. The rim holes allowed drainage of surface water at low tide. Full tops to exclude epibenthic predators and controls for these tops, half tops, were attached to the VEXAR strip with nylon cable ties. Enclosures were imbedded at the experimental site by pushing them into the sediment until only 1 cm of the bucket remained exposed above the sediment surface. Enclosures penetrated a hard clay layer, below which worms or worm burrows were never observed. Three iron stakes marked unmanipulated plots which were controls for the buckets. Three densities of predatory polychaetes tested separately the effects of Nereis and Glyceru on the abundances of infaunal species: (1) natural density, no predatory polychaete addition, (2) 16X Glyceru (whereXis average natural density), and (3) 7X Nereis (Nereis with a first setiger width > 3 mm only). Natural Glyceru and Nereis densities and justification of experimental densities are discussed below. Three cage top treatments, full top, halftop and no top, tested the effects of epibenthic predators on the abundances of the predatory polychaetes and other infaunal species. There were 10 replicates of every possible (9 total) density and cage top treatment combination. Ten unmanipulated plots at natural density only controlled for the bucket artifacts. Buckets and unmanipulated plots were randomly situated 1 m apart in a matrix with 10 treatments or unmanipulated plots to a side (Z 12 x 12 m’). Four buckets with no tops and 7X Nereis density were haphazardly located on the perimeter of the matrix. These buckets were sampled after 1 wk of the experiment and the Nereis counted. These results provided an estimate of the number of Nereis lost from the elevated Nereis density no top treatment in the first week of the experiment. The natural density of Nereis was determined from 3 1 replicate 0.02 m2 x 30 cm deep cores taken from adjacent to the matrix between 4 June and 10 June 1979. The average density of Nereis with a first setiger width > 3 mm was 1.8 per 0.02 m2 (SE = 0.17). Only Nereis within this size class were manipulated because smaller individuals are more difficult to collect and may not be predators. An experimental density of 7X was outside the range of densities sampled by the 0.02 m2 cores (OX to 3X) but was considered necessary to allow for mortality and emigration of worms during the experiment while still ensuring a significant difference in the number of large worms between treatment and control. Data presented below show that this elevated density was quickly reduced. Each bucket was assumed to enclose initially z 1X (X = 5.4) Nereis and an additional 33 individuals (6X) were added to each 0.06-m’ bucket receiving a 7Xdensity treatment. GIyceru are present in the experimental area but none were collected in initial samples. As a result, Glyceru density was estimated from long-term data collected from replicate m2 plots located in approximately the same area as the matrix and dug for commercial sized Glyceru (> 6 g) between 1970 and 1974 (Creaser unpubl. data, Maine Department of Marine Resources). These data indicated that Glyceru density ranged from 0.5 per

PREDATION

BY POLYCHAETES

AND EPIBENTHIC

PREDATORS

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m2 to 2.0 m2 with an average over the 4 yr of 1 per m2. Based on this low density, Glyceru was assumed to be initially absent from enclosures. This proved to be a reasonably good assumption because only 2 of the 60 buckets which did not initially receive Glyceru contained one at the end of the experiment. One Glycera (> 6 g) was added to each bucket designated to receive experimental (16X) densities. Without using larger buckets 16X was the lowest experimental density that could be achieved. The experiment began on 17 June 1979 and was sampled by hand (5 replicates in each treatment) after 10 wk on 23-27 August and after 20 wk on 26-30 October. Unmanipulated plots were sampled by first inserting a bucket between the stakes and then removing all the enclosed sediment. The complete contents of all buckets were returned to the laboratory where the sediment was washed through a 0.5-mm mesh sieve. The residue retained on the sieve was stained with Rose Bengal and stored in 12% formalin until sorting. Sorting was done by eight technicians who randomly selected replicates. Sorting efliciency was greater than 95% for total infauna and is discussed elsewhere (Ambrose, 1982). A dissecting microscope was used to identify and count individuals. Before the sampling described above, one small core (5.7 cm2 x 5 cm deep) was taken from each replicate of all treatments and controls. These cores were frozen for sediment analysis. Graphic mean, inclusive standard deviation, skewness, kurtosis and per cent weight loss on ignition were determined for unmanipulated plots and cage top treatments with no predators added according to procedures outlined in Folk (1980). A subsample of each sediment core was analysed with a C-H-N elemental analyzer (Carbo Erba Elemental Analyzer Model 1106) to determine the percentage of carbon present in each sample. These sediment properties provided measurements of physical sedimentary artifacts related to cage tops and buckets. A model I analysis of variance (ANOVA) was used to test the effects of predatory polychaete density and cage top treatments and interactions among these main treatment effects on the abundance of all common taxa (density of > 3.0 individuals per 0.06 m2 replicate bucket) and the abundance of total infauna for each experimental period, 10 wk and 20 wk. All bivalve species were treated as a group in the analyses because the densities of all bivalves other than Mucoma balthica (Linnaeus) were low (< 1.0 individual per 0.06 m’). All phyllodocid polychaetes were also treated as a group because, except for Eteone Zongu(Fabricius), the densities of all species in this family were < 2.0 individuals per 0.06 m2. Three size classes of Nereis were arbitrarily defined: small (< 1.5 mm first setiger width), medium (1.5-3.0 mm), and large (> 3.0 mm) and these size classes were treated separately in the ANOVA. These size separations were made for Nereis because there was a large range in the size of Nereis and the treatments might have affected size classes differently. It was also important to determine if the manipulated Nereis, those in the large size class, were present in the Nereis addition treatment at the end of each experimental period. To test for the artifacts of the bucket, a t-test was used to compare unmanipulated plots and no cage top buckets without added predators for each experimental period. A t-test was also used to compare the number of large, manipulated Nereis recovered from buckets with 7X Nereis density

120

WILLIAM

G. AMBROSE,

JR.

sampled after only 1 wk and no top cages with 7X Nereis density sampled after 10 wk. To determine whether buckets and cage tops altered the sedimentary regime, means (based on two replicates) of the statistical parameters of grain size listed above, per cent weight loss on ignition, and per cent carbon were compared between cage top treatments (full top, half top, no top) with no predators added and unmanipulated plots. Separate model I ANOVAs were used within each experimental period for these comparisons. Prior to all ANOVAs and t-tests, the F-max test was used to test for homogeneity of variances (Sokal & Rohlf, 1969). When this test indicated that significantly different variances (P < 0.05) existed between treatments, data were transformed using a logarithmic transformation, log,& + l), and re-tested. With the exceptions of kurtosis, weight loss on ignition, and per cent carbon, this transformation was sufficient to correct all heterogeneous variances. Kurtosis data were transformed using k/l + k (where k is kurtosis), as suggested by Folk (1980$, and per cent weight loss on ignition and per cent carbon data were transformed using an arcsin transformation (Sokal & Rohlf, 1969). Unless otherwise indicated, back-transformed abundance data are presented in the figures and tables. Wherever an ANOVA indicated a significant treatment effect (P < 0.05), Duncan’s Multiple Range Test was used to compare individual treatment means. This test was not used when there was a significant interaction between main effects in the two-way ANOVAs. Under these circumstances, a one-way ANOVA and Duncan’s Multiple Range Test were used to compare treatments of one type (cage top or density) while holding the other constant (Underwood, 1981). Glyceru addition replicates which did not contain a Glycera at the end of the experiment (N = 4 for lo- and 20-wk periods combined) and replicates at natural and Nereis addition densities from which a GZycera was recovered (N = 2) were excluded from the two-way analyses. The Glycera density of these replicates was not equivalent to other replicates in the same treatment. To test the effect of excluding epibenthic predators on the survival of Glyceru, Glyceru recovery from cage top treatments was analysed using Fisher’s exact test. This test was used because the sample size was < 20 when analysing experimental periods separately. Even when data from both periods were combined, one third the expected frequencies in a 2 x 3 contingency table were < 5.0. Therefore, half top and no top replicates were combined and the data tested to determine whether Glyceru recovery was independent of epibenthic predator exclusion, the presence and absence of full cage tops (Siegel, 1956). This analysis was done separately for the lo- and 20-wk experimental periods and for both periods combined. The shell length of all bivalves was measured to test whether bivalve mortality was size dependent. Whenever the two-way ANOVA indicated that predatory polychaete density or cage top treatments had a significant effect on bivalve abundance, chi-square analysis (Siegel, 1956) was used to determine if the proportion of small (shell length 6 5 mm) and large (length > 5 mm) bivalves varied between predatory polychaete density treatments or between cage top treatments. This analysis was done

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BY POLYCHAETES

AND EPIBENTHIC

PREDATORS

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separately for lo- and 20-wk periods. A shell length of 5 mm was selected to divide size classes because Ratcliffe et al. (198 1) found that almost all Mucoma balthicu in the top 1 cm of the sediment had a shell length < 5 mm. These shallow dwelling individuals may be more susceptible to predation from epibenthic predators and predatory polychaetes than deeper dwelling individuals. Faecal material from GIyceru and Nereis used in the experiments was qualitatively examined to determine which infaunal species these predators consumed. G&era and large Nereis were removed from the samples during sieving, washed in sea water to remove sediment, separated in trays containing clean sea water and allowed 24 h to clear their guts. Faecal material was fixed with 12% formalin, stained with Rose Bengal and searched for prey parts under a dissecting microscope at 12 x magnification.

COLONIZATION

EXPERIMENT

Predatory polychaetes could affect the abundance of infaunal species by preying on adults, juveniles and/or newly settled larvae, and/or by affecting larval site selection. To test the effect of the presence of Nereis and its activity on the settlement and juvenile survival of infaunal species, colonization of sediment both with and without Nereis was followed. Azoic sediment (containing no infaunal organisms) was produced by filling plastic buckets (36 cm deep by 28 cm inside diameter, 0.06-m’ top area) with sediment from the intertidal and air drying it from 13 May to 13 June 1980. This procedure was assumed to be effective because when the contents of two haphazardly chosen buckets were sieved through a 0.5-mm mesh sieve and the residue sorted for animals none were collected. Drainage holes were drilled around bucket rims at the level of the dried sediment. Buckets were returned to the intertidal on 13 June 1980 and dug into the sediment until the sediment inside and outside the bucket was at the same height (this left z 1 cm of the rim exposed above the surrounding sediment surface). On the following low tide, but before the receding water uncovered the buckets, the water content of the sediment was increased by stirring the sediment in each bucket by hand. On 15 June 1980,20 replicates of both control and Nereis addition treatment buckets were established. Control buckets contained only azoic sediment. Nereis addition buckets contained azoic sediment with a 9X density of Nereis added (50 individuals > 3 mm first setiger width). Five replicates of the control and the Nereis treatment were sampled after the experiment had been in place 10,20,40, and 60 days. At each sampling, six cores (5.7 cm* x 5 cm deep) were removed from each replicate bucket, fmed with 12% formalin and then washed through a 0.25-mm mesh sieve. Sediment remaining in the bucket was washed through a 0.5-mm mesh sieve to recover the rest of the Nereis. All residues were stored in 12% formalin and stained with Rose Bengal until sorting. All residue from the cores was sorted under a dissecting microscope at 12 x magnitication. The residue from the buckets was searched for Nereis only.

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WILLIAM

G. AMBROSE,

JR.

Separate r-tests were used for each colonization period to compare the abundances of taxa between the control and the Nereis addition treatment. The analyses were limited to taxa which had an average density of at least 1.0 per core for treatment or control during any colonization period. The mean abundance of each taxon per core in each replicate was used in the tests. The abundance of small, medium, and large sized Nereis from the control and the Nereis treatment was also compared. EPIBENTHIC

PREDATION

Observations made in May 1979 suggested that predation by gulls (primarily the herring gull Larus argentatus Pontoppidan but also the ring-billed gull L. delawarensis Ord and the greater black-backed gull L. marinus (Linnaeus) may be an important source of mortality for Nereis and perhaps Glycera. To determine if the cages affected gull activity, the density of gulls observed in the experimental matrix and in two adjacent areas marked by stakes was compared. The adjacent areas were at the same tidal height as the matrix and had dimensions identical to the matrix (12 m x 12 m). The number of gulls feeding within the matrix and within the two adjacent areas were counted at 30-min intervals for 3.5 h during 3 low tides on 25, 27, and 28 September, 1979. The total number of bird counts in each area for each tide were determined and the mean number of counts per area per tide compared using ANOVA and Duncan’s Multiple Range Test. Because the caging experiment was designed in part to test the impact of epibenthic predators on the abundances of Nereis, Glycera, and other infaunal species, attempts were made to determine if other potential predators besides birds were feeding within the matrix. The experimental site was observed by SCUBA diving during two daytime high tides on 18 July and 20 August, 1979. Because visibility was
STUDY

OF GLYCERA PREDATION

ON NEREIS

To determine if Glycera were capable of preying on Nereis, the two species were confined together in aquaria (20 cm deep x 15 cm inside diameter) in the laboratory. The aquaria were filled to within 3 cm of the rim with sediment that had been previously collected from the area studied and frozen for 3 wk at 0 “C to kill ah existing infauna. Each aquarium was covered with a screen (l-mm mesh) to prevent worms from escaping. Water flowed into each aquarium separately and overflowed around the rim. Four replicates of each of the following treatments were established: (1) 10 Nereis and 1 G&era, and (2) 10 Nereis and 2 Glycera. Four control aquaria each contained 10 Nereis. All Nereis used in this experiment had a first setiger width > 3 mm and all Glycera were heavier than 6 g. After 4 wk the number of Nereis and Glycera recovered from each aquarium were counted. Differences in the abundance of Nereis recovered per replicate were compared using a model I ANOVA and treatment means compared using Duncan’s Multiple Range Test.

PREDATION BY POLYCHAETES AND EPIBENTHIC PREDATORS DISTRIBUTION

123

OF TAXA WITHIN THE SEDIMENT

To determine at what depths within the sediment org~isms lived, cores were sectioned by depth and each section analysed separately. On 11 September 1981, three 0.02 m2 x 30 cm deep cores were taken adjacent to the area where the matrix was located in 1979 and 1980. Cores were divided into four sections: O-4,4-10, lo-20 and 20-30 cm and the contents of each section sieved through a OS-mm mesh. Abundances for each section were summed across all three cores and the percentage of a taxon’s abundance in each section dete~ned.

RESULTS CAGING EXPERIMENT

As will be shown below, elevated densities of both Glycera and Nereis were rn~t~~ for the lo- and 20-wk periods. The caging experiment, therefore, tested for the effects of both predatory polychaete addition and epi~n~~ predator exclusion on infaunal densities. The taxa which enter into the statistical analyses are listed in Table I, as also are feeding type and depth distribution of these taxa. TABLE I

Feeding type and depth dist~bution of common taxa: all taxa except bivalves {%com bu~~hicaand other bivalves) were treated separately in the statistical analyses; bivalves were treated as a group; depth distributions are percentages of total number of individuals (N) from three 0.02-m’ cores taken at the experimental site in September 1981; (A), Annelida; (C), Crustacea; (M), Mollusca; C, carnivore; DF, deposit-feeder; FF, filter-feeder; 0, omnivore; see Barnes, 1974; Fenchel etal., 1975; de Wilde, 1975; Fauchald & Jumars, 1979; a, Efeone longa, Phyllodoce arenae Webster, and P. maculata (Linnaeus); b, Ensis directus Conrad, Gemma gemma Totten, and Lyonsia hyalina Conrad. Depth distribution (%). cm Taxa (A) (A) (A) (A) (A) (A) (A) (A) (A) (C) (C)

Glycera dibranchiata Nephtys in&a Nereir virens Notomastus latericew Phyllodocidae” Poiydora ligni Scoioplos robustus ~~eb~ospjo benedicti

Ohgochaetes Corophium volutator

Copepods (C) Cumaceans (M) Macoma balthica (M) Other bivalvesb

Feeding type

o-4

10-20

-

C

C,DF C DF C DF DF DF DF DF DF FF,DF FF,DF FF

4-10

100

0

86

6 45 0 0 27 0 38 0 0 0 16

1

10;

100 65 100 38 100 100 100 0

0 7 45 0 0 7 0 24 0 0 0 84

20-30

N

-

0

0 2 3 0 0 0 0 0 0 0 0 0

54 59 29 4 9 26 158 381 320 4 7 19 0

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WILLIAM G. AMBROSE, JR.

Results after 10 weeks

There were no significant cage top x predatory polychaete treatment interaction effects so main effects could be evaluated separately (Table II). The statistical analysis detected an effect of cage top treatments on the abundance of phyllodocids, copepods, and cumaceans (Table II). Phyllodocids were significantly (P < 0.05) more abundant and cumaceans and copepods less abundant in full top than in no top treatments (Fig. 2). TABLE II

Significance levels from two-way ANOVAs analysing the effect ofcage top and predatory polychaete density treatments on the abundances of all common taxa (and total infauna) after 10 and 20 wk: values for large Nereis do not strictly reflect a treatment effect because this size class was added to the Nereti addition treatment; *P < 0.05; **P < 0.01; *** P < 0.001; ns = not significant (P > 0.05). 10

Taxa Nephtys incisa Small Nereis

Medium Nereb Large Nereis Notomastus latericeus Polydora ligni Scoloplos robustus Streblospio benedicti

Phyllodocidae Oligochaetes Corophium volutator

Copepods Cumaceans Bivalves Total infauna

Cage top ns ns ns ns ns ns ns ns ** ns ns ** *** ns ns

weeks

Predatory polychaete density *** ns *** *** ns *** * *** *** ns * ** ns *** ***

20 weeks

Cage X density

Cage top

ns ns ns ns ns ns ns ns ns ns ns ns ns ns ns

*** ns ns ** ns * ns ** ns *** ns *** ** ns ***

Predatory polychaete density

Cage X density

*** *** *** ***

ns ns ns **

ns *** ** *** ** ns ns **

ns ns ns ns ns ns ns **

ns *** ***

ns ns ns

No association between the presence or absence of a full cage top and Glycera recovery was detected (Fisher’s exact test, P = 0.66). Only one Glycera addition treatment replicate was lacking a Glycera at the end of the experimental period. The addition of predatory polychaetes significantly affected the abundances of Nephtys incisa Malmgren, medium Nereis, Polydora ligni Webster, Scoloplos robustus Verrill, Streblospio benedicti Webster, Corophium volutator (Pallas), copepods, phyllodocids, bivalves, and total infauna (Table II). Large Nereis were also significantly affected but this significance test is confounded because large Nereis were added to the Nereis addition treatment. A comparison of treatment means between Nereis addition and no predator addition treatments shows that the abundances of Corophium volutator, Streblospio benedicti, Polydora ligni, and Nephtys incisa were significantly (P < 0.05)

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lower in the presence of increased Nere& density (Fig. 3). Only copepods and large Nereis were more abundant in the Nereis addition treatment than in the no predator addition treatment. The G&era addition treatment contained significantly (P < 0.05) greater abundances of Streblospio benedicti, Polydora ligni, Nephtys incisa, Scoloplos 10 Weeks FT- Full Top Cage HT- Half Top Cage NT-No Top Cage

FT HTNT Phyllodocids

FTt?T;T Cumaceans

FT HTI

5

Copepods

Pig. 2. Effect of cage top treatments on the abundance of taxa with a significant cage top effect in the two-way ANOVA, 10 wk after the start of the caging experiment: mean number ( + 1 SE) of individuals per 0.06-m* bucket (iV = 13) are presented; Duncan’s Multiple Range Test was used to determine significant differences between means; means with common underline are not significantly different (P > 0.05).

robin,

phyl~odocids, bivalves, and total ~nfauna compared with the no predator addition treatment (Fig. 3). Abundances of copepods and medium and large sized Nereis were significantly less abundant in the Glycera addition treatment than in the no predator addition treatment. The significantly greater number of large sized Nereis in the Nereis addition treatment as compared to the no predator addition treatment (Fig. 3) indicates that an elevated density of Nereis was maintained for 10 wk. This elevated density, however, was not the initial 7X Nereis density. The Nereis addition treatm~t contained a mean of 23.2 (SE = 0.96) large Nereis, 61% of the estimated 38 worms originahy present in the treatment. This reduction of the experimental density apparently occurred rapidly. The t-test comparing Nereis abundance between no top buckets sampled after 1 wk which contained an average 21.0 (SE = 2.3) large Nereis and the no top Nereis treatment sampled after 10 wk which contained an average 22.8 (SE = 2.2) large Nereis was

WILLIAM G. AMBROSE, JR.

126

not significant (t = 1.06, d.f. = 7, P > 0.05). By the end of 10 wk the Nereis addition treatment contained * 3.5 times as many large Nereis as the no predator addition treatment (Fig. 3). IO Weeks NP- No predator addition G- Glycera addition N- Eaddition

I

30

20 “E

t5 6

IO-

&i CL i

GNPN .GNPN medium 7 . lacge

25 -E

PhyHo~ids

m

2

G _NP N

GNPN --

GNPN

GNPh

Bivalves C.volutator Copepods 3ooor

150 L

GNP N S.benedicti _-

bp GNP N Eu

G NP N S.robustvs

G NP N N. incise

GNP N Tgfal

Fig. 3. Effect of predatory polychaete addition on the abundances of taxa with a significant predatory polychaete effect in the two-way ANOVA 10 wk after start of the caging experiment: mean number ( + 1 SE) of individuals per 0.06m2 bucket for Giyceru (N = lo), Nereis (N = 14) and no predator addition (N = 15) treatments are presented; Duncan’s Multiple Range Test was used to determine significant differences between means; means with common underline are not si~ific~tly different (P > 0.05).

The chi-square analysis comparing the proportions of small and large bivalves from predatory polychaete addition treatments was significant (x2 = 10.18, d.f. = 2, P -c 0.005). The Nereis addition treatment contained proportionally fewer small bivalves compared with the no predator addition and Glyceru addition treatments.

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121

Results after 20 weeks

The cage x predatory polychaete treatment interaction was significant for large Nereis and copepods (Table II) but main effects can be evaluated for other taxa. Cage top treatments significaritly affected the abundances of Nephtys in&a, Polydora ligni, Streblospio benedicti, oligochaetes, cumaceans, and total infauna (Table II). Nephtys incisa, Streblospio benedicti, oligochaetes, and total infauna were more abundant in the full top treatment than no top or half top treatments while the reverse was true for cumace~s (Fig. 4). PoZydoraligni abundance was not si~~c~dy different between full top and no top treatments but the full top treatment had si~i~c~~y (P < 0.05) more P. ligni than the half top treatment.

20

“E g

Weeks

FT- Full Top Cage HT-Half Top Cage NT- Flit Top Cage

1000

6

& a

FT HT NT N. in=

ii5

2 2

FT HT NT

Oligstes

FT HT NT

Total

300

:T HT NT

s benedicti

FTHTNf --

Pm

Cuma~eans

Fig. 4. Effect of cage top treatment on the abundances of taxa with a significant cage top effect in the two-way ANOVA, 20 wk after the start of the caging experiment: mean number ( + 1 SE) per 0.06m2 bucket for full top cage (N = 12), half top cage (N = 11) and no top cage (N = 12) are presented; Duncan’s Multiple Range Test was used to determine significant differences between means; means with common underline are not significantly different (P > 0.05).

WILLIAM G. AMBROSE, JR.

128

As during the lo-wk period, Fisher’s exact test indicated that the presence or absence of a full cage top did not affect Glyceru recovery (P = 0.26). Only three Glyceru treatments were lacking a Glyceru at the end of the experimental period. Fisher’s test is still not significant when the data on Glyceru recovery from 10 and 20 wk are combined (P = 0.34). Addition of predatory polychaetes significantly affected the abundances of all taxa except Notomustus luterikeus Sars, oligochaetes, Corophium volututor and cumaceans (Table II). In the presence of experimental Nereis density the abundances of bivalves, Streblospio benedicti, Polydoru ligni, Nephtys incisu, and total infauna were significantly (P < 0.05) lower than at natural density in the no predator addition treatment (Fig. 5). Abundances of small and medium sized Nereis were lower in the presence of Glyceru than at natural density (Fig. 5). With the exception of Scoloplos robustus, abundances of all other taxa affected by the addition of predatory polychaetes were greater in Glyceru’s presence than at natural density. A significant cage top x predator treatment interaction for large Nereis and copepods NP-No Predator addition G-Glycera addition N-Nereis addition

20 Weeks

30 1 20

IO

1

I& A

G NP N small 1

G --NP N medium I

Nereis

k G NP N Sbenedicti --

G NP N

Ill G NP N

Phyllodocids Bivalves

looo~h

kh

GNPN

JNJNP

-F!t&i

--S.robustus

G NP N N. incisa --

G NP N Total

Fig. 5. Effect of predatory polychaete addition on the abundances of taxa with a significant predatory polychaete effect in the two-way ANOVA, 20 wk after start of the caging experiment: mean number ( + 1 SE) of individuals per 0.06-m* bucket for GZycera (N = 12) Nereis (N = 10) and no predator addition (N = 13) treatments are presented; Duncan’s Multiple Range Test was used to determine significant differences between means; means with common underline are not significantly different (P > 0.05).

___PPY

No predator addition G&era addition Nerreisaddition

No top Half top Full top Half top

No top 1.3 0.0 62.6

0.0

0.0

!&L._-_ 0.0 112.9

9.2 7.3

No predator addition

0.0 0.0

Gfyceru addition

0.0 0.0 125.7

Fuh top

Nere& addition ___I_112.9 62.6 125.7

Copepods

** ns ns

Significance level

*** *** ***

Significance level

4.4 0.0 15.5

No top

0.0 1.0 0.0

G&era addition

5.0 1.0 147 -L_.

Half top

6.4 5.0 6.8

No predator addition --

Nereis

6.8 0.0 23.0

Full top

15.5 14.7 23.0

Nereis addition

*

llS

ns

Significance level

*** *** *c*

1__--Significance level

Mean number ofcopepods and large Nereis per 0.06 m2 bucket from predatory polychaete addition treatments (no predator addition, G&era addition, hkreis addition) at each cage top treatment (no top, half top, full top) and means from cage top treatments at each predatory polychaete density after 20 wk of the caging experiment: a one-way ANOVA was used to test for the effects of predatory polychaete treatments within each cage top treatment or for the effects of cage top treatments within each density; significance level of ANOVAs are indicated; when an ANOVA was significant (P c 0.05) Duncan’s Multiple Range Test was used to compare treatment means; means with common underline are not si~~~cantly different (P > 0.05); * P cz 0.05; ** P < 0.01; *** P < 0.001; us, not sign&cant (P > 0.05).

TABLE iI1

130

WILLIAM

G. AMBROSE,

JR.

prevents a separate evaluation of either main effect. There is a significant interaction for these groups because there was only a significant effect of cage top trea~ents at one predatory polychaete density. The one-way ANOVAs indicate that copepods were significantly less abundant in the full top treatment compared with no top and half top treatments but only at no predator addition density (Table III). Nereis was only significantly affected by the cage top treatments in the Nereis addition treatment (Table III). Full top cages contained a signi&antly greater abundance of large Nereis than half top or no top treatments. Copepods were always significantly more abundant in the presence of Nereis (Table III). Elevated densities of Nereis were rn~nt~~ for 20 wk because large Nereis were always significantly more abundant in the Nereis addition treatment compared with the no predator addition treatment regardless of the cage top treatment (Table III). Large Nereis were almost absent from the Glyceru addition treatment (Table III). The chi-square analysis comparing the proportions of small and large bivalves from predatory polychaete addition treatments was not significant (2” = 2.32, d.f. = 2, P > 0.05). Treatment effects on shallow- and deep-dwelling taxa

After analysing the. effects of epibenthic predators and predatory infauna on the abundances of individual taxa, the taxa were separated into shallow- and deep-dwelling groups and the two-way ANOVA repeated for both lo- and 20-wk experimental periods. A taxon was ~bi~~y defmed as deep-dwe~mg if greater than one third of its indi~du~s were found below a sediment depth of 4 cm (Table I). By this definition, Notomastus Iatericeus, ScoIoplos robustus, oligochaetes, and bivalves were considered deep-dwelling and Nephtys incisa, phyllodocids, Polydora ligni, Streblospio benedicti, Corophium volutator, copepods and cumaceans were shallow-dwelling. Nereis was excluded from the analysis. For the lo-wk experimental period neither shallow- nor deep-dwelling taxa were affected by the exclusion of epibenthic predators (Table IV). Both groups were most abundant in the presence of G&era and least abund~t in the presence of Nereis. For the 20-wk period both shallow- and deep~welling taxa were affected by the exclusion of epibenthic predators but only shallow-dwellers were significantly affected by the addition of predatory polychaetes (Table IV). The full top treatment had a greater abundance of both groups than no top or half top treatments. The abundance of shallow-dwelling taxa was greatest in the Glycera addition treatments and lowest in the Nereis addition treatments.

PREDATION BY POLYCHAETES AND EPIBENTHIC PREDATORS TABLE

131

IV

Mean number of shallow- and deep-dwelling taxa per 0.06-m’ bucket from cage top and predatory polychaete density treatments after 10 and 20 wk of the caging experiment: two-way ANOVAs were used to test for cage top and density treatment effects within each experimental period; significance Ievels of these ANOVAs are indicated; cage top X density treatment interaction was not significant (P > 0.05) for shallowor deep-dwelling taxa for either experimental period; when an ANOVA was significant (P < 0.05) Duncan’s Multiple Range Test was used to compare means; means with a common underline are not significantly different (P > 0.05); * P < 0.05; *** P < 0.01; ns, not significant (P > 0.05). 10 weeks

Shallow Deep

Half top

Full top

1417.5 444.8

1290.7 448.6

1347.4 472.3

ns ns

Nereis addition

Significance level

G&era addition Shallow Deep

Si~i~cance level

No top

1917.5 535.4

No predator addition

-

1326.7 460.8

974.9 392.0

*** 1

20 weeks No top

Half top

Full top

Significance level

Shallow Deep

680.6 328.1

709.3 323.9 __-.-

1390.2 891.7

*** ***

Nereis addition 503.2

Significance level

Shallow

G&era addition 1423.7

Deep

634.1

No predator addition 869.9 473.3

443.9

*** ns

Bucket and cage top artifacts

Infaunal abundances in the presence of buckets with no cage top and no predatory polychaetes added and from unm~ip~ated plots were not consistently different for either lo- or 20-wk periods (Table V). For 10 wk the r-tests indicated that large A&is and Corophium volutatorwere significantly (P < 0.05) more abundant in the presence of buckets than in unmanipulated plots while the reverse was true for Scoloplos robustus (Table V). For 20 wk Streblospio benedicti was significantly (P < 0.05) more abundant in buckets than in unmanipulated plots (Table V). The sed~ent~ analyses provide a second method of assessing bucket and cage top artifacts. No ANOVA was significant so the results of these analyses indicate that neither buckets nor cage tops significantly altered the measured parameters for either experimental period (Table VI). Although no attempt was made to quantify their behavior, crabs, Cancer irroratw Say and Carcinus maenas (Linnaeus), were observed inside replicates of no top and half top

V

-

Streblospio benedicti Oligochaetes Corophium volutator Copepods Cumaceans Bivalves Total infauna

Polydora ligni Scoloplos robustus

Phyllodocids

Notomastus latericeus

Small Nereis Medium Nereis Large Nereis

Nephtys in&a

1118.2 14.8 12.3 9.4 24.8 4.2 46.8 72.0 146.6 389.4 44.4 39.6 31.8 15.6 2022.2

(64.0) (2.6) (2.2) (0.9) (3.7) (0.7) (3.8) (12.4) (30.8) (74.8) (25.2) (15.4) (5.9) (1.1) (187.9)

No cage top no predator addition

10 weeks

959.5 14.0 10.6 3.3 21.5 3.0 38.0 125.5 163.5 455.3 7.3 21.8 27.0 18.8 1856.5

(126.4) (2.8) (1.9) (1.3) (1.6) (0.6) (4.5) (18.6) (27.4) (68.7) (2.3) (9.7) (10.8) (2.4) (200.7)

Unmanipulated plot ns ns ns * ns ns ns * ns ns * ns ns ns ns

Significance level 520.8 12.4 12.8 6.4 15.4 5.0 24.4 137.6 176.6 169.0 9.2 13.2 17.2 14.4 1234.0 (31.4) (2.1) (1.7) (1.4) (2.4) (1.8) (2.4) (18.6) (33.5) (72.9) (1.3) (5.4) (5.9) (1.8) (225.4)

No cage top no predator addition

20 weeks

497.0 12.8 11.4 3.2 21.6 2.8 45.0 145.8 88.6 159.4 9.4 9.2 31.4 16.0 1018.6

(65.6) (2.1) (0.8) (0.5) (1.6) (1.1) (7.9) (5.5) (14.5) (41.5) (1.3) (4.6) (6.9) (2.6) (118.4)

Unmanipulated plot

ns ns ns ns ns ns

ns ns ns ns ns ns ns ns *

Significance level

Comparisons of infaunal abundances between no top cage treatment with no predators added and unmanipulated plots after 10 and 20 wk for a11taxa tested in ANOVAs: mean number of individuals (and 1 SE of the mean) per 0.06 m* bucket for no top cages (N = 5) and unmanipulated plots (N = 4) and significance levels of f-tests comparing these means are presented for each taxon and total infauna; data are untransformed; * P < 0.05; ns, not significant (P > 0.05).

TABLE

133

PREDATION BY POLYCHAETES AND EPIBENTHIC PREDATORS

treatments during both SCUBA dives. Flatfish were observed inside the matrix but were not observed inside buckets of any type. Observations made during day (N = 10) and TABLEVI Statistical parameters ofgrain size, per cent weight loss on ignition (LOI) and per cent carbon for sediment samples taken from each type of cage top treatment and from unmanipulated plots after 10 and 20 wk: mean values (and 1 SE of the mean) based on two replicates are shown; one-way ANOVAs within time periods showed no significant difference in grain size, LO1 or carbon between treatments (and unm~ipulated plots). Parameter

Full top

Half top

No top

Unmanipulated

10 weeks Graphic mean Inclusive standard deviation Skewness Kurtosis LGI (%) Carbon ( % )

6.55 1.79 + 0.06 0.48 5.05 3.48

(0.28) (0.11) (0.02) (0.03) (0.06) (0.20)

6.50 2.01 - 0.01 0.50 4.76 3.62

(0.07) (0.05) (0.05) (0.00) (0.12) (0.07)

6.41 2.07 + 0.10 0.5 1 5.22 3.48

(0.09) (0.02) (0.07) (0.00) (0.11) (0.20)

6.50 1.95 - 0.01 0.49 4.99 3.49

(0.33) (0.13) (0.01) (0.00) (0.17) (0.06)

20 weeks Graphic mean Inclusive standard deviation Skewness Kurtosis LGI (%) Carbon (%)

6.51 1.80 + 0.02 0.53 5.39 3.57

(0.02) (0.06) (0.01) (0.03) (0.11) (0.07)

6.65 2.04 0.00 0.47 5.19 3.59

(0.15) (0.07) (0.00) (0.02) (0.09) (0.02)

6.34 2.02 + 0.03 0.49 5.31 3.57

(0.18) (0.12) (0.00) (0.00) (0.09) (0.07)

6.45 1.96 - 0.01 0.49 5.08 3.50

(0.02) (0.13) (0.02) (0.00) (0.20) (0.03)

night (N = 4) low tides never revealed any epibenthic predators inside cage treatments nor were any epibenthic predators recovered from cages during sampling. Predatory polychaete faecal pellet analyses

Because Glycera apparently does not have a functions anus (Klawe & Dickie, 1957) and regurgitates ingested material after digestion and when disturbed, material collected from the trays containing G&era represented both recently ingested prey and hard parts of digested prey. Material collected from Nereis passed through the entire gut and contained primarily hard parts of digested prey although soft parts of Nephtyx in&a and oligochaetes were recovered (Table VII). A majority (62%) of the Glycera guts were empty and Glyceru pellets had fewer taxa than Nereis.

134

WILLIAM G. AMBROSE, JR. TABLEVII

Presence and absence data for prey and prey parts recovered from pler& (N = 390) and Glyceru (N = 26) faecal material. Food item

Nereis

Giycera

Annelida Nephtys in&a Nereis v&ens

Qaws and soft parts) Spionid tube Oligochaetes Mollusca Myu arenaria Macoma balthica

Shell fragments

+ + i+ + f

+”

I

Crustacea

COLONIZATION

Coroph~~m volutator

c

Copepods Cumaceans

+

“k

+

EXPERIMENT

Fig. 6 shows the mean number ( + SE) of the most common taxa {densities > 1.0 in~vidu~ per core) per core for each replicate which settled into the control and the Nereis addition treatment during each colonization period. AU these taxa were significantly less abundant in the Nereis addition treatment than in the control during at least one period. All the annelids sampled by the cores were assumed to be recently settled juveniles because of their small size. At the time of fast appearance, individual Nephrys incisa and Streblospio benedicti had an average first setiger width of < 0.10 mm, Polydoru Iigni a width of 0.16 mm and Scoioplos robustus a width of c 0.20 mm. All individuals had < 20 setigers. Adult, repr~u~tively mature Corop~i~~ vo~#tuto~as well as juveniles were sampled. The density of Nereis in the control increased during the experiment (Fig. 7). As the size class data indicate, not all of these i~i~~ts were settling larvae. There were, however, always significantly more large Nereis in the addition treatment than in the control (Fig. 7). These large Nereis appear to have inhibited the settlement and immigration of small and medium sized Nereis since significantly fewer individuals of these size classes were recovered from the Nereis addition treatment when compared with the control at 40 and 60 days. As in the caging experiment, the experimental Mere& density was quickly reduced. only 64% of the Nereis added to the iVerek addition treatment remained after 10 days. This density, * 4X to 5X, remained relatively constant during the remainder of the experiment.

PREDATION BY POLYCHAETES AND EPIBENTHIC PREDATORS

T

60 Days

N.incisa S.benedicti l?li& --_-_

135

Cmlutator S.robustus Oliqochoetes _-----

Fig. 6. Effect of Nereis on the settlement and survival of Nephtys incisa, Streblospio benedicti, Polydora ligni, Corophium volutator, Scoloplos robustus, and oligochaetes: mean numbers ( + 1 SE) of individuals per core (N = 6), per replicate (N = 5) for the control and Nereis addition treatment after 10,20,40, and 60 days of colonization are presented; significance level of each t-test comparing abundances between control and Nereis addition treatment is indicated by asterisks; * P < 0.05; ** P < 0.01; *** P < 0.001; no asterisk P > 0.05.

136

WILLIAM G. AMBROSE, JR. m

Control

0

Nereis addition

IO Days

~~~ a L

Nereis

Nereis

sqall

me$um Nereis

lar;ge

sqall

medium m

large

Fig. 7. Nereis recovery for the colonization experiment: mean number (+ 1 SE) of Nereis per replicate (N = S) in three size classes; small (< 1.5 mm first setiger width), medium (1.5-3.0 mm), and large (> 3.0 mm), recovered from the control and Nerds addition treatment after 10, 20, 40, and 60 days of colonization; significance level of each r-test comparing Nereis abundance between control and Nereis addition treatment is indicated by asterisks; * P < 0.05; ** P < 0.01; *** P c 0.001; no asterisk P > 0.05.

EPIBENTHIC

PREDATION

Crabs, Cancer irroratus and Car&us mamas, and flatfish were observed within the matrix, and crabs within no top and half top cage treatments. Gulls were the most conspicuous avian predators on the flat, although black-bellied plovers, Pluvialis squatarola (Linnaeus), lesser yellowlegs, Tringa flavipes Gemlin, and semipalmated sandpipers, Calidris p&la Linnaeus, were also observed during the fall mi~ation (late August and early September) in both 1979 and 1980. The ANOVA comparing bird counts between the portion of the study area containing cages and areas containing no cages was significant (P < 0.01). Duncan’s Multiple Range Test revealed no significant difference between the mean number of birds counted in the two areas adjacent to the matrix (means of 11.7 and 8.7 gulls), but these means were significantly different (P < 0.05) from the mean of 1.3 gulls observed within the matrix. The other birds were never observed within the matrix.

PREDATION LABORATORY

STUDY

BY POLYCHAETES

OF GLYCERA

AND EPIBENTHIC

PREDATION

PREDATORS

137

ON NEZtEZS

ANOVA comparing the number of Nereis recovered after 4 wk from the control and Glyceru treatments was significant (P < 0.01). In the absence of Gfycera a mean of 9.67 Nereis was recovered while in the 1-Glyceru and 2-Glyceru treatments means of 3.33 and 1.00 Nereis, respectively, were recovered. Duncan’s Multiple Range Test indicated no significant difference in Nereis recovery between the Glyceru treatments but these treatments were significantly different (P c 0.05) from the control. The

DISCUSSION

The major results can be summarized as follows: (1) infaunal densities increased following the exclusion of large epibenthic predators but not until after 20 wk of exclusion, and (2) infaunal densities were highest in the presence of Glycera and lowest in the presence of Nereis. These results will first be interpreted and then the importance of predatory infauna in structuring soft-bottom communities assessed.

CAGE

ARTIFACTS

Cage artifacts can seriously interfere with the interpretation of caging results in soft-sediment systems (Virnstein, 1978; Peterson, 1979; Dayton & Oliver, 1980; Hulberg & Oliver, 1980). Only the densities of a few taxa were significantly different between unmanipulated plots and cages with no predators added (Table V). The numerical response of these taxa to the presence of the bucket does not interfere with an interpretation of the results because all treatments required the use of buckets. The purpose of this comparison was to determine ifbuckets distorted the natural community to the point where conclusions reached using bottomless buckets could not be extended to the natural community. Distortion of abundances to this extreme does not appear to have occurred. Significant differences in infaunal abundances between half top and no top cage treatments would suggest that the physical structure of cage tops affected infaunal abundances or that epibenthic predators did not react the same to both treatments. Of the taxa significantly affected by cage top treatments, only the abundance of copepods varied significantly between no top and half top treatments (Fig. 2). This artifact prevents an assessment of the effect of excluding epibenthic predators on copepod abundance. For the IO-wk period the result of excluding epibenthic predators on phyllodocid abundance is hard to interpret because full top and halftop treatments were not significantly difTerent (Fig. 2). Cages have not always been completely effective in excluding epibenthic predators in previous exclusion experiments in soft-sediment systems (Young et al., 1976; Virnstein, 1978; Peterson, 1979; Kneib & Stiven, 1982). The successful exclusion of epi-

138

WILLIAM G. AMBROSE, JR.

benthic predators from full top cages in this study may have been due to the intertidal position of cages and lack of tide-pool refuges for crabs and fish. Cage walls extending deep into the sediment probably prevented crabs from digging into cages. EPIBENTHIC

PREDATION

Exclusion of epibenthic predators in other unvegetated areas has generally resulted in significant increases in infaunal abundances within two months (Vimstein, 1977; Holland et al., 1980; Woodin, 1981). Despite the presence of fishes and crabs in the experimental area, only phyllodocids were significantly more abundant in full top than in no top treatments after 10 wk (Table II, Fig. 2) and as discussed above this result is difficult to interpret. Substantially higher (increases between 80% and 380%) infaunal densities were recorded in full top cages than in no top cages after 20 wk (Table II, Fig. 4). This result is most likely due to the exclusion of epibenthic predators. Predators were observed in the matrix and within no top and half top treatments. Furthermore, cage artifacts do not interfere with the interpretation of density differences between full top and no top treatments. Since no cages were estabhshed for just the last 10 wk it is impossible to determine whether this effect is due to increased predation during the last 10 wk of the experiment or a cumulative effect of predation over 20 wk. The average density of infauna in unmanipulated plots was equal to = 31000 individuals per m2 in August 1979 at the end of 10 wk of the caging experiment (N = 4) and 17ooO per m* in October at the end of 20 wk (N = 5). These densities are considerably higher than densities from other unvegetated intertidal areas in the eastern United States south of Cape Cod (Dexter, 1969; Commito, 1976; Dorges, 1977 ; Simon & Dauer, 1977; Woodin, 1978; Hunt, 1981). Woodin (1976) has suggested that higher infaunal densities north of Cape Cod relative to the remainder of the eastern United States may be due to the absence of the blue crab, Callinectes sapidus, a predaceous portunid crab, which digs pits 3-12 cm deep (Orth, 1977; Woodin, 1978) and may be responsible for substantial mortality by disturbance as well as by predation. The absence of this predator and other disturbers such as the horseshoe crab, Lim~~~~po~yphernus (Linnaeus), present in New England but not observed in the area studied may help to account for the relative lack of importance of epibenthic predator/disturbers in determining infaunal densities in this area. Gulls were less abundant in the experimental matrix compared with the surrounding flat so the experiment did not adequately test the hypothesis. that Nereis and Glycera are preferred prey for epibenthic predators or the impact of gull predation on the densities of other infauna. Survival of large Nereis held at high experimental densities for 20 wk was better in ftdl top than in no top treatments (Table III). This increased survival may have been due to the exclusion of gulls (those that did enter the matrix), fishes, and/or crabs. There are at least two other explanations for this result: (1) cage tops may have inhibited Nereti emigration, and/or (2) higher infaunal densities in full top cages may have been able to support higher densities of Nereis. Large Nereis were observed to crawl

PREDATION

BY POLYCHAETES

AND EPIBENTHIC

PREDATORS

139

in the field, and swim in the laboratory, through the 6-mm mesh used as cage tops. Furthermore, there was no evidence of cage tops restricting emigration during the fast IO-wk period, when the largest escape reaction might be expected (Table II). Infaunal densities were higher in full top cages than half top and no top cages by 20 wk (Fig. 4) and this difference was largely due to increases in taxa which were found in Nereis faecal material (Table VII) and whose abundances Nereis affected (Fig. 5). More data on epibenthic predator activity inside the matrix would be needed to confirm that the increased survival of large Nereis in the absence of epibenthic predators was the result of excluding these predators. Gull predation was not measured using exclusion cages but observational data collected from the experimental site at the same time as the experiments were conducted indicate that gulls preyed heavily on Nereis (Ambrose, 1982). In other areas, gulls take a variety of infauna including nereids (Spaans, 1971). Analyses of gull faecal material indicate that in the experimental area predation on infauna is limited to Nereis (Ambrose, 1982). Measurements ofjaws collected from faecal material indicate that gulls preyed primarily on large Nerefi (first setiger width > 3.0 mm) (Ambrose;1982). Nereis are particularly susceptible to predation by gulls because individuals extend up to two-thirds of their body outside their burrow to graze the surface and capture prey (Pettibone, 1963; pers. obs). Gbceru are probably not preyed upon by gulls because glycerids come to the surface only briefly to capture prey (Ockelmann & Vahl, 1970). EFFECTS OF NEREIS

AND GLYCERA

The hypothesis that Nereis and Glycera predation is important in determining infaunal abundances was supported by the experiments, but the interactions were complex. Presence of Nerejs caused a substantial reduction in the abundance of several taxa (Figs. 3,5). When Glyceru was present the abundances of these taxa increased relative to no predator addition treatments. Glyceru addition reduced the abundance of Nereis and essentially produced a OX Nereis treatment (Figs. 3, 5, Table III). Assuming that G&era activity did not enhance settlement, then higher densities in the Glycera treatment can be attributed to decreased Nereis abundance in the presence of Glyceru. This seems reasonable because Glyceru appear to have little effect upon sedimentary properties. Glyceru maintain a semi-permanent burrow so do not disturb the sediment with continual burrowing activity, do not deposit large quantities of faecaJ material on the sediment surface, and are not active on the sediment surface (pers. obs.). Consequently, their presence is unlikely to affect larval site selection. While G&era are obviously capable of reducing the abundance of Nereis, there are at least two possible mechanisms for this interaction. Glyceru predation can substantially reduce Nereis abundance, as shown by the laboratory experiments, and Glyceru prey on Nereis in the field (Table VII). The observed low Nereis density in the Glyceru field treatments, however, may also have been due to emigration of Nereis by swimming (Dean, 1978) or crawling. Emigration of several infaunal species has been found to be greater in the presence than in the absence of predators (Ambrose, 1984b).

140

WILLIAM

G. AMBROSE,

Nereis may have reduced infaunal abundances

JR.

by predation, disturbance and/or influencing larval site selection. Remains of a number of taxa were recovered from Nereis faecal material (Table VII). Nereis, however, disturb the surface by extending large portions of their body onto the surface during feeding and by depositing faecal material there. These activities could result in the burial of larvae, juveniles and adults, interfere with tube construction and provide clues for settling larvae. The disproportionate reduction in the abundance of small bivalves during the first 10 wk of the caging experiment could have been the result of direct predation, but smaller individuals might also have been adversely affected by Nereis surface activity. In the colonization experiment, Nereis presence reduced the abundance of several species during settlement or early development (Fig. 6). These results do not aid in determining the developmental stage (larval, juvenile or adult) most vulnerable to Nereis but do indicate that many of the interactions between Nereis and their “prey” may be in the form of adult-larval or adult-juvenile interactions. All infaunal species, regardless of where they live in the sediment column, must pass through the surface layer during settlement and are therefore exposed to Nereis activity. Permanent residents of the surface layer, however, are more likely to be affected by Nereis than deep-dwelling taxa which may only maintain intermittent contact with the surface following settlement. As a group, deep-dwelling taxa were less affected by Nereis than shallow-dwelling taxa during the caging experiment (Table IV). The results of the colonization experiment and the caging experiment may appear inconsistent. Nereis decreased the abundances of the same taxa in both experiments, but towards the end of the colonization experiment spionids, Streblospio benedicti and Polydoru ligni, and Nephtys incisa were equally abundant in the control and the Nereis addition treatment (Fig. 6). Two possible and reasonable explanations are: (1) Corophium volututorpresence in the control decreased the abundance of spionids and Nephtys incisa, and/or (2) increased Nereis in the control (Fig. 7) decreased the abundance of these species. Commit0 (1982) found a negative correlation between Corophium volututor density and total infaunal density. In the present experiments, as C. volutator became more abundant in the control compared with the Nereis addition treatment, the difference in the abundances of spionids and Nephtys incisu between the control and the Nereis addition treatment began to disappear (Fig. 7). After 60 days the density of Corophium volututorwas 15 per 5.7 cm2 so the amphipods may have out-competed other surfacedwellers for space. Evidence of such competition in dense infaunal assemblages has been found in other systems (Woodin, 1974; see review by Woodin & Jackson, 1979; but see Hulberg & Oliver, 1980). Alternatively, C. volututor may have depressed the abundances of these species by predation and disturbance. Amphipods have been found to reduce infaunal densities by burial and ingestion of larvae and juveniles (Segerstrale, 1962, 1965, 1973; Oliver et al., 1982). The effect of C. volututor on the abundances of other infauna could not be observed in the caging experiments because this amphipod occurred at very low density in 1979.

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Nereis immigrated and settled into buckets during the colonization experiment (Fig. 7). Although most of these Nereis were small and medium sized, they could have affected the abundances of colonizers. It is unlikely, however, that they had as large an effect on abundances as the large Nereis in the Nereis addition treatment. In the caging experiment an unnaturally high experimental density of Nereb was created. This elevated density, however, was quickly reduced by emigration and/or mortality. Experimental density declined to an average of 4Xin no top cages within 1 wk and to an average of 3.5X in all Nereis additions by 10 wk. These densities are much closer to the highest density, 3X, recorded in the initial 0.02-m’ cores and made the experiments a more realistic test of Nereis’s ability to influence infaunal abundances than if the initial density had persisted. Furthermore, although confounded by Glycera’s presence, the Glyceru addition treatment acted as a Nereis removal treatment and provided a (confounded) means of evaluating the effects of Nereis removal on infaunal abundances. SOFT-BOTTOM

COMMUNITY

STRUCTURE

The results of the present study indicate that predatory infauna need to be considered when attempting to predict the outcome of interactions in soft-bottom communities. Simple characterizations of soft-bottom communities which portray fishes, crabs, and birds as predators and infaunal species as prey are probably an accurate prediction of interactions between epibenthic predators and infaunal species only where epibenthic predators are simultaneously major disturbers. Effects of epibenthic predators/disturbers on infaunal densities are likely to overwhelm interactions among the infauna. In areas where these epibenthic predators are largely absent, such as under exclusion cages, in New England waters north of Cape Cod and in the Pacific Northwest (Woodin, 1974, 1976) or where these predators are ineffective, such as in grass beds (Orth, 1977; Reise, 1978; Peterson, 1979, 1982), then more complex interactions may be important in structuring soft-bottom communities. The Glycera-Nereis-other infauna interactions are similar to the sea otter-urchin-kelp interactions of nearshore hard-bottom communities in the northwestern Pacific (Estes et al., 1978). Additional support for such complexity in soft-bottom communities is provided by Kneib & Stiven (1982) who present evidence for interactions between fish-small epibenthic predators-infauna in North Carolina salt marshes. Many of the interactions which are important in structuring soft bottom communities, such as adult-larvae interactions, sediment-mediated interactions and predation by epibenthic predators/disturbers, appear to take place on the sediment surface (Rhoads &Young, 1970; Woodin, 1976; Myers, 1977; Virnstein, 1979; Brenchley, 1981; Wilson, 198 1). Therefore, any attempt to include predatory infauna into a model of soft-bottom community structure should take into account their contact with the sediment surface. In addition to preying directly on infauna, those predatory infauna which are active on or near the sediment surface may disturb the sediment and affect infaunal densities by

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burying infauna and affecting larval site selection. Polychaetes are not the only group of predatory infauna cont~~g species which are active on the sediment surface. Some nemerteans (Roe, 1976), gastropods (Wiltse, 1980), and amphipods (Oliver et al., 1982) are also potential predators/disturbers because of their surface activity. The individual effects of surface-active predators will depend on their prey and the frequency and magnitude of their effect on the sediment (Wilson, 1981). Surface-active predators will also be more susceptible than subsurface predators to predation by fishes, crabs, and birds because they are often visible to these epibenthic predators. Gull and shorebird predation on large surface-active predatory infauna (largely polychaetes and nemerteans) has been well documented (Spaans, 1971; Woodin, 1974; Goss-Custard, 1977; Goss-Custard et al., 1977; Bryant, 1979; Hicklin & Smith, 1979; Kent & Day, 1983). These infauna are also well represented in fish guts (Wells & Steele, 1973; Arntz, 1979; Hacunda, 1981; Kent & Day, 1983). G&era, Nerds, Polinices and several species of phoxocephalid amphipods are the only predatory infauna which have been manipulated (Reise, 1979; Wiltse, 1980; Com~to, 1982; Oliver er ai., 1982; Kent & Day, 1983) so it is difficult to assess the general importance of predatory infauna in reducing competition and preventing competitive exclusion from occurring between other infaunal species. The ability of predatory infauna to increase infaunal densities by preying upon intermediate predators/disturbers may even intensify competition between members of the infaunal community. Predatory infauna have been shown, however, to reduce substantially infaunal densities (present study; Reise, 1979; Wiltse, 1980; Commito, 1982). The failure to account for the activity, predation and disturbance, of predators among the infauna in previous predator exclusion experiments could help account for the failure of a competitive dominant to become established following the removal of epibenthic predators. Criteria in addition to predatory behavior, however, may be necessary to predict the effects of predatory infauna on soft-bottom community structure.

I would like to thank my committee members particularly C. H. Peterson as well as other colleagues for discussion and critical review of this manuscript. D. Reinhold did the carbon analysis of the sediments. I thank the personnel at the Maine Department of Marine Resources, Boothbay Harbor, especially T. Creaser, for making laboratory space and equipment available. The University of North Carolina Institute of Marine Sciences provided laboratory and office space. This work was supported by a doctoral dissertation research grant from the Biological Oce~o~aphy Division of NSF (OCE 79-19916), an R. J. Reynolds Research Fellowship, a University of North Carolina Smith Fund grant, the University of North Carolina at Chapel Hill Curriculum in Marine Sciences, NSF grants OCE 77-07939 and OCE 79-09323 from the biological Oceanography Program to C. H. Peterson, and funds from my father, W. G. Ambrose.

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