Environmental Biology of Fishes 42: 37-50,1995.

© 1995 Kluwer Academic Publishers. Printed in the Netherlands.

Trophic relationships and seasonal utilization of salt-marsh creeks by zooplanktivorous fishes

Dennis M. Allen', William S. Johnson 2 & Virginia Ogburn-Matthews' Baruch Marine Field Laboratory, University of South Carolina, P.O. Box 1630, Georgetown, SC 29442, U.S.A.

2 Biological Sciences, Goucher College, Towson, MD 21204, U.S.A.

Received 18.2.1993 Accepted 8.2.1994

• Key words: Resource partitioning, Estuarine fishes, Predation, Prey selection, Zooplankton, Menidia meni- dia, Membras martinica, Anchoa mitchilli, Anchoa hepsetus

Synopsis

In a high salinity estuary at North Inlet, South Carolina, co-occurrence and possible competition among adults of four dominant zooplanktivorous fishes were minimized by seasonal adjustments in lateral and vertical distributions as well as in dietary preferences. In winter, Atlantic silversides, Menidia menidia, occupied the entire water column while other planktivores were rare or absent from the estuary, and they consumed large prey such as mysid shrimps and fish larvae. An immigration of bay anchovies, Anchoa mitchilli, in the spring resulted in a redistribution of species with Atlantic silversides shifting to the surface waters and bay anchovies dominating the lower half of the water column. Both fishes consumed mostly copepods in the spring, but each favored a different species. There was little similarity in the large prey items consumed by the two fishes. Striped anchovies, Anchoa hepsetus, arrived in mid-summer and were most abundant at the surface while bay anchovies continued to dominate the bottom waters. Atlantic silversides were rare in all summer collections. The diets of the two anchovies were similar, but vertical separation during the period of maximum zooplank-ton abundance probably minimized competition. Rough silversides, Membras martinica, which were obligate surface dwellers, shared the upper water column with striped anchovies, but the two species had very different diets during their period of co-occurrence. Although seasonal changes in fish diets reflected shifts in zoo-plankton composition and all fishes consumed a variety of prey types, preferences for some prey taxa and total avoidance of others were indicated. Electivity indices indicated an especially strong selection for fiddler crab megalopae by all fishes in the summer and fall. All fishes, except rough silversides, which fed almost exclusive-ly on copepods and crab zoeae, consumed large prey items when they were available. Fine scale partitioning of the food resources was apparent in the selection of different copepod and insect species by the fishes. Spatial and temporal separation in the distribution and/or dietary preferences of the zooplanktivores fishes probably reduces the potential for resource competition. Given the high abundances and selectivity of the planktivores, significant impacts on some zooplankton populations probably result.

Introduction

Relationships among species of fishes comprising feeding guilds have been examined in many marine habitats such as coral reefs (Emery 1973, Gladfelter

& Johnson 1983), temperate reefs (Ellison et al. 1979, Milton 1983), the coastal ocean (Modde & Ross 1983, Kislalioglu & Gibson 1977, Ross 1977), and the deep sea (Sedberry & Musick 1978, Merrett & Roe 1974). In a review of resource partitioning in

38

fish assemblages from these and other aquatic hab-itats, Ross (1986) determined that a high level of separation among coexisting species occurred along at least one of three resource dimensions (habitat, food, and time). Comparatively little in-formation is available on how co-occurring estua-rine fishes utilize common resources, and we are not aware of any studies that focus on interactions among zooplanktivorous fishes in temperate estu-aries.

Four species of zooplanktivorous fishes are among the most abundant fishes in estuaries from New York to Florida. The Atlantic silverside, Meni-dia menidia, and the rough silverside, Membras martinica, are atherinids which spawn and spend most of their lives in tidal systems. The life history (Middaugh et al. 1984, Cadigan & Fell 1985), distri-bution (Conover & Ross 1982), and diet (Bengston 1984, Morgan 1990) of the Atlantic silverside are well known, but similar information is not available for the rough silverside. The bay anchovy, Anchoa mitchilli, has a wider geographic and salinity range than the striped anchovy, Anchoa hepsetus, but both are abundant in the lower ends of major estu-aries on the East coast. Because bay anchovies are among the most abundant fishes in Atlantic and Gulf coast estuaries, their life history (Vouglitois et al. 1987), distribution (Livingston 1976, Reis & Dean 1981, Sheridan 1992), and diet (Carr & Adams 1973, Sheridan 1978, Din & Gunter 1986, DeLancey 1989, Johnson et al. 1990) are probably better known than those of most other estuarine fishes.

The co-occurrence of adults of these four species in South Carolina estuaries suggests that some means of partitioning habitat and trophic resources may exist. In this study, we describe both the sea-sonal patterns of abundance and distribution and the seasonal differences in the diets of adult plank-tivorous fishes within a major tidal creek. We also relate patterns of prey consumption to zooplankton availability and determine prey preferences for the planktivores. Finally, we integrate information on the distribution of the fishes with their feeding pat-terns and discuss the extent of overlap, the parti-tioning of resources, and impacts on prey popula-tions within a warm temperate estuary.

Materials and methods

Collections of fishes were made in Town Creek, a large tidal creek (100 m wide, 3 m deep) 3 km inside of North Inlet, South Carolina. The 2800 ha estuary is dominated by Spartina alterniflora marsh. Salin-ities in the major waterways remain above 30 ppt for most of the year due to strong tidal exchange with the coastal ocean and a lack of significant sources of freshwater runoff. Tidal range is about 2 m and depth in Town Creek channel is about 2.5 m at mean low tide. Current velocities up to 1.0 m sec-1 minimized salinity and temperature stratification of the turbid water column.

Collections were made every two weeks from June 1985 through February 1987 (41 dates). Trawl nets were used to collect fishes at both the surface and bottom of the water column during the last hour of the daytime ebbing tide. The surface trawl was a 12 m wide, 1 m high net which tapered from the wings to a deep funnel and cod end. The mesh in the body of the net was 7 mm and the tail bag mesh was 3 mm. A 1 m wooden stake spread the weighted lower line and the floated head rope at each end of the net. A bridled tow rope connected each end of the net to a different boat. The net was towed be-tween two boats along a 300 m path which took about 10 min to cover. Following the surface tow, an otter trawl (4.9 m wide, 1.5 m high) was deployed from a single boat and towed along a 300 m path parallel to the surface trawl path near the center of the creek. The mesh was 7 mm in the front of the net and 3 mm in the taper and tail bag of the trawl. It was not possible to use exactly the same net design to sample both levels of the water column. Varia-tions in wind speed and direction and tidal current conditions caused fluctuations in the volume of wa-ter filtered; however, we estimate that about 1.3 times more water was filtered in a typical surface tow than in the corresponding bottom tow. In order to make the catch per unit effort values of the two gear types more comparable, the catch data for the surface collections were reduced by 30%. The aver-age surface tow sampled about 3500 m 3 of water. Immediately after the tows, the catches were sorted on board. To facilitate processing of typically large catches, one of the following techniques was used. If

39

Atlantic silverside Striped anchovy

2000

1500

.1-

'8 1000

0 Z 500

450

350

250

150

50

W Sp Su F W

Rough silverside

Su F 1985

Sp Su 1986 1987

400

300

200

100

Bay anchovy

Su F W Sp Su

1985 1986 1987

No.

of fi

sh

50

40

30

20

10

striped anchovy Anchoa hepsetus

bay anchovy Anchoa mitchilli

Atlantic silverside Menidia menidia rough silverside Membras martinica

Jun—Sep Apr—Sep Nov—May May—Nov

63% 90% 68% 68%

12 975 218 267 166

363 8 6 4

299 055 949 653

30-105 30-65 35-90 30-90

1.3 •urfac• III bottom

t21 surf/to• 1111 bottom

Fig. 1. Mean catch (+ 1 S.E.) in surface (striped) and bottom (shaded) trawls for each season from summer 1985 through winter 1986-1987. Values for surface catches are adjusted (see Methods) and different vertical scales are used for each species. Abbreviations for seasons are Su for summer, F for fall, W for winter, and Sp for spring.

there appeared to be fewer than 100 individuals of a species, all individuals were counted. If more than 100 were present, a subsample of about 100 was ran-domly selected from the catch and used to estimate the total number of that species in the catch before

the rest were released. Although a few individuals of other planktivorous fishes were sometimes col-lected, only the four primary species were pro-cessed. Up to 100 individuals representing the full range of lengths were injected with preservative

Table 1. Summary of combined catch data for 81 trawl collections in Town Creek, North Inlet, SC from June 1985—February 1987. Fre-quency of occurrence is based on the number of dates out of 41 in which the species was present. Data from all surface and bottom trawl collections were pooled for this summary.

Species Standard

Maximum Frequency Mean catch Total catch length (mm)

period of abundance

1 0 0

cti 80 -

Ca

c.)

15

a) 40 - c.)

O. 20

S 0 N .1 F F W Sp Su

1986

4

4 SON DJE

F W 1987 1985

0

Su

60

A

A

*al

O

sai a

100

80

60"

40

20"

0

40

Surface

J J A s 0 N 11LE ILELI J J A S 0 N D J F

Su F W S p S u F W

1985 1986 1987

Bottom

0 Rough slvs. ❑ Atlantic slvs. ❑ Striped anch. • Bay anch.

Fig. 2. Percentage of the total catch for each of the four planktivorous fishes collected in surface and bottom trawls each month. Propor-tions are based on averages for all dates during that calender month. Abbreviations for seasons are as in Fig. 1. Abbreviations for months within seasons are in consecutive order starting with June.

and placed in a 41 container of 10% seawater for-malM for transport to the laboratory.

In the laboratory, we analyzed the stomach con-tents of adult (50-90 mm) fishes representing all four species. Diets were determined for at least one date each season, usually a date when all or most species were present. Usually 10 to 20 individuals of each species were analyzed, but, in two cases, only 4 or 5 individuals were available. Species-area curves

using cumulative number of prey species and plots of running averages of percentages of major diet categories consumed indicated that sample sizes were sufficient to both qualitatively and quantita-tively characterize the diets of all four species. To determine the diets, the stomach (anterior to the in-testine) of each individual fish was removed and the contents were identified to the lowest possible tax-on and enumerated. The volume of each food cate-

100 -

8 0 -

6 0 -

4 0 -

2 0 -

Winter

41

0

Spring 1 0 0

8 0 -

6 0 -

4 0

20

111111111111111

Summer 100"

80 -

60 -

40 -

20 -

Fall 1 0 0

80

6 0 -

4 0 -

2 0 -

Striped

Bay

Atlantic

Rough

anch. anch. slvs. slvs.

others

El fish larvae El insects

❑ shrimp larvae

mysids

0 crab megalopae ED crab zoeae

▪

copepods

Fig. 3. Percentage of the total volume of stomach contents accounted for by each of the major prey taxa for each fish species and season. Proportions are based on averages for all individual fishes analyzed in 1986. Open cells indicate that the fish species was not present in sufficient numbers to conduct the analysis. Copepods and crab zoeae are referred to as small prey, and mysids, fish larvae, crab megalo-pae, insects, and shrimp larvae are referred to as large prey. Abbreviations for fishes are striped anch, for striped anchovy, Bay anch, for bay anchovy, Atlantic slvs. for Atlantic silverside, and Rough slvs. for rough silverside.

42

gory and the proportion of the total volume it com-prised were recorded. Stomachs which contained fewer than 10 items, had contents too digested to be identified or had less than 30% fullness by volume were excluded from all analyses. A total of 138 indi-viduals were used to compare diets among species. Prey items were referred to as small (< 1 mm in length: copepods, crab zoeae, and barnacle cyprids) or large (> 1 mm in length: crab megalopae, shrimp larvae, mysids, fish larvae) zooplankton.

Stomach contents were compared to the zoo-plankton prey present at the time of collection. Zooplankton densities were determined immedi-ately before the fish collections on each date by de-ploying a pair of 153 micron mesh opening-closing nets and making a series of sequential replicate tows with a 365 micron epibenthic sled at the same location that the fishes were collected. Zooplank-

ton samples were preserved with 10% buffered for-malin. In the laboratory, zooplankters were identi-fied to the lowest possible taxon and enumerated. Density estimates of each zooplankton taxon were based on collections from only one of the two net types.

An index of feeding electivity, L (Gabriel 1979) was used to provide a measure of relative selectiv-ity. L is the natural log of the odds ratio (Fleiss 1973; also identical to the 'forage ratio' of Jacobs 1974) calculated as ln(Pi -0 2/P2Q1) where P, is the percent in the diet, Q, is the percent of all other prey eaten (or 100-P,), P2 is the percent of the taxon in the plankton, 02 is the percent of all other potential prey (100-0 1). An L of zero indicates no selection. Values greater than zero indicate positive selection and those less than zero suggest negative selection. This index was used because it allows the compari-

Table 2. Approximate size and densities of dominant zooplankton in the water column at the time fishes were collected in 1986. Abbrevia-tions following the taxon indicate whether the prey type is referred to as small (sm) or large (1g). Densities of small zooplankton were based on collections with the 153 micron nets and densities of large taxa were based on collections with the 365 micron nets. The first four taxa are dominant copepod species. Mean number ± 1 SE per cubic meter is shown for each of the seven sampling dates from which fishes were analyzed for stomach contents. The first winter date is 6 Feb and the second is 21 Feb. Spring values are from 21 May. The first summer date is 4 Jun and the second is 18 Aug. The fall data are from 31 Oct and 2 Dec, respectively.

Range in length (mm)

Winter Spring Summer Fall

0.48-0.53 50 ± 27 1952 ± 105 4284 ± 15 1679 ± 30 103 ± 18 3507 ± 39 2082 ± 30

0.46-0.64 19 ± 19 75 ± 23 376±8 554 ± 160 0 101 ± 7 374 ± 15

0.76-1.60 0 20 ± 20 107 ± 40 23 ± 12 9±8 12 ± 12 0

0.83-0.99 1489 ± 179 1285 ± 184 714 ± 5 481 ± 45

864 ± 86 2293 ± 442 299 ± 40

0.63-0.99 0 842 ± 109 417 ± 18 28 ± 5

0 2351 ± 195 0 1.28-3.36 0 3.7 ± 0.2 132 ± 28 < 1 ± < 1

0 2 ± 0.7 0 1.33-9.17 0 5.4 ± 1.5 14.4 ± 1.6 1.1 ± 0.4

0.1 ± 0.1 4.4 ± 0.8 0.1 ± 0.1

2.33-15.50 43 ± 17 11 ±5 20 ± 3 < 1 ± < 1 1 ± < 1 <1 ±<1 < 1± < 1

3.67-5.42 <1±<1 12 + 4 45 ± 2 1 ± < 1 < 1 ±<1 9±2 <1±<1

3.25-7.58 1 ± < 1 17 ±4 87 ± 17 12 ± 2

< 1 ± < 1 6±2 6 ± 1

4.00-20.0 1 ± < 1 22 ± 2 33±4 < 1 ± < 1

< 1 ± < 1 3 ± < 1 <1±<1

Taxon

Parvocalanus crassirostris (sm)

Euterpina acutifrons (sm)

Pseudodiaptomus coronatus (sm)

Acartia tonsa (sm)

crab zoeae (sm)

crab megalopae (lg)

shrimp larvae (lg)

mysids (Ig)

hydromedusae (1g)

chaetognaths (1g)

fish larvae (lg)

43

sons over wide ranges of prey abundance (Jumars et al. 1982). Electivity values were calculated with stomach content data from fishes collected within 40 min following plankton collection on each date. In both the diet and distribution analyses, seasons were defined as follows: winter (Dec 21 — Mar 20), spring (Mar 21— Jun 20), summer (Jun 21 — Sep 20), and fall (Sep 21 — Dec 20).

Results

Distribution and abundance

Striped anchovies, Anchoa hepsetus, bay anchovies, Anchoa mitchilli, Atlantic silversides, Menidia me-nidia, or rough silversides, Membras martinica, were the dominant adult 30 mm) zooplanktivo-rous fishes in all collections. More than 383 000 indi-viduals were collected in the 81 trawls taken during the 20 month period. The abundance of each spe-

cies varied considerably among seasons (Fig. 1). Striped anchovies were, overall, the most abundant (Table 1), even though one very large collection (about 350 000 individuals) in July 1986 accounted for 95% of the total catch of that species. Bay an-chovies were the most frequently collected. Periods of occurrence varied among species, and some were absent or rare for one or two seasons each year (Fig. 1), but at least one of the four species was present on each of the 41 biweekly collection dates. The largest collections of striped anchovies, bay anchovies, and rough silversides occurred from spring to fall, whereas Atlantic silversides reached peak abun-dances in winter. Seasonal changes in the vertical distributions of the planktivorous fishes were also observed within the shallow tidal creek (Figs 1, 2). Generally, more species and greater numbers of in-dividuals were taken in surface collections. In sum-mer, striped anchovies dominated collections at the surface (Fig. 2), but they were relatively uncommon at the bottom where the largest summer collections

Table 3. Summary of seasonal changes in diet showing the mean number of prey items of each major taxon that occurred in the stomachs of fishes collected at the same time. Total items indicates the mean total number of all prey consumed by a single fish during that season. Other prey include amphipods, mollusks, ostracods, and polychaete larvae. The number of fish stomachs analyzed, the mean percent fullness of the stomachs, and the mean standard length of the fishes are shown. Abbreviations for fish species are as follows: Bay = Anchoa mitchilli, Atl. = Menidia menidia, Rough = Membras martinica, Str. = Anchoa hepsetus. The first four prey taxa are copepods. A indicates that adults were counted. A + C indicates both adults and copepodids were counted.

Prey taxon

Parvocalanus

crassirostris (A) Euterpina acutifrons (A) Pseudodiaptomus

coronatus (A + C) Acartia tonsa (A) crab zoeae crab megalopae shrimp larvae mysids fish larvae insects others mean total prey no. of fishes mean percent full mean fish length (mm)

Winter Spring Summer Fall

Bay Atl. Bay Atl. Rough Str. Bay Atl. Rough Str. Bay Atl. Rough

0 0 1 0 0 0 0 0 1 6 35 51 82 0 0 31 1 27 1 1 0 0 1 75 24 17

0 4 1 48 18 1 1 0 1 0 0 292 20 11 16 54 24 63 8 16 0 192 43 74 0 33 0 0 30 0 90 9 17 0 332 0 0 0 0 0 0 0 0 0 11 20 8 20 1 1 0 0 0 1 0 4 0 5 5 9 0 0 0 0 0 2 2 0 0 0 0 0 0 0 0 0 0 0 0 2 0 1 0 1 0 6 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 45 44 1 4 10 7 2 2 2 1 2 5 3 1 3

14 29 127 85 200 38 62 25 548 56 188 413 199 10 12 10 10 5 20 20 4 10 7 10 10 10 63 75 40 63 33 61 64 78 66 41 67 76 69 65 87 57 89 91 65 50 88 64 82 55 78 89

44

of bay anchovies were made (Fig. 1). Bay anchovies were widely distributed in the water column in spring and early summer until striped anchovies and rough silversides dominated the surface from mid-summer through fall (Fig. 2). Atlantic silver-sides were most abundant at the surface, but they occupied the entire water column in winter when other species were not common. Rough silversides were restricted to surface waters all year.

Diets

Based on the size of the prey consumed by the four fishes, the two silversides represented opposite ends of the feeding spectrum (Fig. 3, Table 2). Rough silversides had the narrowest feeding pat-tern, preying almost exclusively on copepods and crab zoeae less than about 1 mm in length. Unlike

the other three fishes, rough silversides almost nev-er consumed larger zooplankton such as decapod larvae and fish larvae. In contrast, Atlantic silver-sides fed predominantly on larger prey, making greater use of shrimp and fish larvae than of cope-pods and crab zoeae. The more similar diets of bay anchovies and striped anchovies were intermediate in that these fishes consumed prey which ranged from 0.5 to 15.0 mm in length when both small and large prey were available.

Seasonal changes in the diets of the four fishes (Fig. 3) generally reflected temporal shifts in the composition of the zooplankton prey (Table 2). In winter, both resident fishes (Atlantic silversides and bay anchovies) concentrated on larger prey items. Although both ate copepods, Acartia tonsa, mysid shrimps, Neomysis americana, were major prey items (Table 3, Fig. 3). A major difference in the diets of the two winter fishes was the consump-

Table 4. Electivity indices for planktivorous fishes collected on 7 dates in 1986. Numerical values indicate strength and sign of the index. A value was calculated whenever a prey category was present in both the stomachs of the fishes and the collections of zooplankton taken at the same time and place. Other symbols are as follows: - means prey item was in the nets but not eaten; 0 means prey item was neither present in the nets nor in the stomachs; + means the prey was eaten but not collected in the nets. Blank cells indicate no fishes of that species were available for diet analyses. For each prey taxon, values on the first row are for the first collection date that season; values on the second row are for the second date. Fish species abbreviations are same as in Table 3.

Spring Summer Fall

Atl. Bay Atl. Rough Str. Bay Atl. Rough Str. Bay Atl. Rough

- 5.0 - 1.6 -1.0 - 7.9 - 2.5 - 0.5

3.0 -0.2 2.2 -2.3 -2.7 - -2.2 1.6

0 0.8 - 0.6 - 0.1

0 - 1.4 5.7 3.2 - 0.7 3.5 1.1 - - 1.6

0.7 0.6 0.1 0.2 1.5 1.7 - 3.4 1.7

- 1.1 - 0.8 - 0.5 0.6 1.0

0 0.3 1.3 0.8 0.3 - 0 0.9 1.5 1.6 0 0

0 - - 3.1 3.8 3.5 6.1 4.5

0 7.9 7.0 5.3 0 0

0 3.9 - 5.2 4.3 4.7 0 0

7.7 2.6 2.2 - 0 0

2.8 - - - - - 0 0

3.4 0 0 0 1.0 - 2.2 - 4.4 0 0

8.7 2.5

Prey taxon Winter

Bay

Parvocalanus

crassirostris (A)

Euterpina acutifrons (A) -

Pseudodiaptomus

coronatus (A + C)

0

Acartia tonsa (A)

0.7

crab zoeae 0

crab megalopae 0

shrimp larvae 0

mysids 2.3

fish larvae -

Summer

30 -

45

Winter

No.

ea

ten

2 0 -

1 0 -

0

1 2 0 —

C

tv 80

0 Z 40

tel ce

200

1 0 0

400

C

cC a) 300 -

200 -

1 0 0

-

Spring

Fall

• A • Striped anch. Bay anch. Atlantic slvs. Rough slvs.

g Euterpina 0 Parvocalanus UPseudodiaptomus Acartia

Fig. 4. Average numbers of each copepod species consumed by the zooplanktivorous fish species during each season in 1986. Note that different vertical scales are used for each season. Abbreviations for fishes are the same as in Fig. 3.

46

tion of 10 to 14 mm spot larvae, Leiostomus xanthu-rus, and pinfish, Lagodon rhomboides, by Atlantic silversides but not by bay anchovies. In spring, co-pepods became more important in the diets of At-lantic silversides and bay anchovies. Crab zoeae (primarily Uca spp.) became abundant in spring (Table 2), but they were not consumed by Atlantic silversides which continued to eat larger prey such as shrimp and fish larvae (Fig. 3).

The diets of the four members of the zooplank-tivorous fish feeding guild were most different in summer (Table 3, Fig. 3) when prey abundance and variety reached maximum levels (Table 2). In sum-mer, rough silversides continued to consume cope-pods and crab zoeae while Atlantic silversides re-stricted their diet to larger taxa, principally shrimp and fish larvae, and crab megalopae. Striped ancho-vies and bay anchovies had more varied diets with both small and large prey items being consumed in summer. Major shifts in the diets of all four fishes were observed in fall when larger invertebrate lar-vae became less available. Both anchovies showed a strong reliance on copepods while both silversides supplemented copepod diets with insects. The sil-verside species consumed different species of leaf-hopper: rough silversides ate Prokelisia marginata, and Atlantic silversides ate Delphacodes detecta.

Electivity values indicated that all four fishes had a preference for larger prey in seasons when they were available. Some of the highest electivity values were for fish and shrimp (Penaeus aztecus) larvae in winter and for shrimp (Palaemonetes spp. and Al-pheus spp.) larvae and crab megalopae (Uca spp.) in summer (Table 4). Electivity values for large prey were consistently high in winter. Negative values were not observed for large prey, but hydromedu-sae and chaetognaths, which were present all year and often at relatively high densities (Table 2), were never identified from the stomach of any fish. Elec-tivity values for small prey were generally lower, and they varied considerably among prey and pred-ator species. Values for the abundant copepod, Par-vocalanus crassirostris, were consistently negative, and, often, when it was abundant, it was not con-sumed at all. For Acartia tonsa, which was con-sumed by almost all fishes in all seasons, values were usually near neutral. Other copepod values

were more variable. Crab zoeae were consistently consumed in a slightly higher proportion to their availability.

All four fishes consumed adult copepods, but each fish showed a distinct preference. Four species accounted for over 99% of the copepods available in the water column, but only rough silversides con-sumed all four (Fig. 4). Acartia tonsa was eaten by all fishes most of the year, but it was virtually the only copepod consumed by striped anchovies. Only bay anchovies favored the smaller harpacticoid, Euterpina acutifrons, whereas only Atlantic silver-sides ate the relatively large Pseudodiaptomus cor-onatus in notable numbers (Table 3, Fig. 4). Parvo-calanus crassirostris was common throughout the year (Table 2), but it was only consumed when it was the dominant copepod. Even when eaten, Parvoca-lanus crassirostris was not a major dietary item and negative electivity values were typical (Table 4).

Discussion

Seasonal changes in the abundance of adult plank-tivorous fishes within the tidal creek and their dis-tribution within the water column resulted in rela-tively little spatial overlap among species. The change from a period of minimum co-occurrence in winter, when Atlantic silversides almost totally dominated, to a period of maximum occurrence in spring and summer when bay anchovies, striped an-chovies, and rough silversides repopulated the tidal creeks was characterized by a spatial redistribution of all species. The tendency for rough silversides and striped anchovies to occupy the surface level and bay anchovies to occur near the bottom sug-gested that a partitioning of the water column oc-curred when all species were concentrated in the creek channel during low tide. Vertical segregation of other species of planktivorous fishes has been de-scribed for a tropical shallow water assemblage (Parrish 1989), but our data appear to be the first to demonstrate the vertical segregation of these wide-ly distributed estuarine planktivores. Evidence for minimal spatial overlap was also found in the shore zone adjacent to the trawl path. Analyses of data from a four-year seine survey showed that schools

47

of Atlantic silversides did not co-occur with schools of bay anchovies (Ogburn-Matthews & Allen 1993). Spatial overlap between these co-occurring fishes may be further reduced during high tide when intertidal habitats become available. With flooding tides, Atlantic silversides migrate into vegetated in-tertidal areas (Middaugh 1981, Hettler 1989, Kneib 1991), whereas bay anchovies are more likely to re-main in intertidal creeks (Reis & Dean 1981), pools (Crabtree & Dean 1982), and at the edge of the marsh (Rakocinski et al. 1992). Although bay an-chovies have been collected from stands of emer-gent vegetation, striped anchovies and rough silver-sides, which were present in open waters adjacent to a North Carolina marsh collection side, were nev-er taken in marsh flumes (Hettler 1989). No direct measurements of fish movement into intertidal habitats were made in the present study, but high tide trawl collections yielded very few planktivores in the major tidal creeks.

In addition to the spatial and temporal partition-ing of the habitat, potential competition is further reduced by the dietary preferences of these co-oc-curring planktivores. Within most seasons, there was broad overlap in the prey taxa consumed; how-ever, both the relative numbers and volumes of a single taxon in the diet were usually distinctive for each species of fish. Although seasonal differences in prey consumed generally reflected changes in zooplankton community composition, shifts in diets of some fishes could not be explained by changes in prey availability. In some cases, a prey item not consumed in one season was eaten in large numbers in another season. The result of these ap-parent adjustments in primary prey consumed was relatively little dietary overlap within seasons. Gladfelter & Johnson (1983) also reported a similar combination of habitat partitioning and site specific dietary specialization resulting in minimal overlap in tropical squirrelfishes in the same location. Beng-ston (1984) concluded that temporal changes in the partitioning of habitat and food resources account-ed for the co-occurrence of two silverside species in Rhode Island waters.

Simultaneous measurements of prey bases and diets of multiple species within a feeding guild are uncommon (Lazarro 1987). Here, all species

showed marked selection for particular prey types within a diverse prey field, and these preferences changed seasonally. Bay anchovies can be highly se-lective oppportunistic feeders (Johnson et al. 1990), and our data suggest that the same applies to all planktivores in this study. Since the number of spe-cific prey items consumed by any fish during any season was rarely in proportion to the abundance of that prey, predation was probably neither a function of simple straining of the water nor of indiscrimi-nate prey seizure. The most striking example of se-lectivity was the within season differences in cope-pod species consumed. Although other studies have identified copepods as major dietary items for adult bay anchovies (Sheridan 1978, Carr & Adams 1973, Din & Gunter 1986, Johnson et al. 1990), striped an-chovies (Carr & Adams 1973, Modde & Ross 1983, DeLancey 1989), and Atlantic silversides (Cadigan & Fell 1985, Fulton 1985, Warkentine & Rachlin 1989), selection for copepods at the species level has been examined only in the bay anchovy (Johnson et al. 1990). The mechanism for selection of specific prey in zooplanktivores has been widely reported in studies in freshwater fishes and fish larvae (see re-views by O'Brien 1979, Lazarro 1987), but informa-tion is lacking for estuarine species in turbid condi-tions. Whether these preferences for individual co-pepod species are due to feeding behavior of the fish or result from morphological or behavioral characteristics of the prey, the result is a finely parti-tioned utilization of the prey resources.

Regardless of the extent to which the diets of the four species overlap, it is difficult to argue that the supply of food is a limiting factor for these fishes in estuarine systems. Both during periods of maxi-mum predator pressure (summer) and minimum prey abundance (winter), densities of zooplankton (especially copepods which were constituents of all four fishes' diets) exceeded 1500 individuals per cu-bic meter. Coupled with the ability of all four spe-cies to use a wide variety of prey, sufficient supplies of suitable prey were probably available all year. Although there would appear to be enough prey to feed all of the fishes present at any moment, plank-tivorous fishes probably have significant impacts on zooplankton abundance and distribution. Fulton (1984) concluded from enclosure experiments that

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predation by anchovies and silversides prevented Acartia tonsa from dominating the estuarine cope-pod assemblage during summer and fall. Kimmerer & McKinnon (1989) determined that selective pre-dation by planktivorous fishes explained the spatial distribution of copepods in an Australian bay.

The preference for large crustacean and fish lar-vae demonstrated by adult bay anchovies, striped anchovies, and Atlantic silversides suggest that pre-dation by these fishes may be an important factor in the recruitment success of some estuarine macro-fauna. In this study, the highest electivity values were for fiddler crab (Uca spp.) megalopae. They were selected for even when their densities were low. Given the intensity of the selection and the high abundances of planktivorous fishes during the entire recruitment period, predation may have a significant impact on fiddler crab recruitment. Fid-dler crabs are among the most dominant salt marsh invertebrates, and they constitute major sources of food for some fishes, terrapins, birds, and mam-mals. Adult fiddler crabs produce large pulses of zoeae which are rapidly transported to the coastal ocean where larval development is completed; megalopae re-enter the estuary and recruit to adult habitats (Christy 1989). Predation on crab zoeae probably has much less of an impact on fiddler crab populations than does fish predation on the much less abundant megalopae. Morgan (1990) examined predation by anchovies and silversides on Uca spp. zoeae and concluded that the magnitude and timing of release of larvae and the dispersal patterns of the zoeae probably minimized the risk of planktivory on these species. Electivity values for shrimp larvae (especially for Penaeus spp., Palaemonetes spp., and Alpheus spp.) were high during summer, and the recruitment success of these populations may be in-fluenced by planktivore predation. We also suspect that fish preference for the mysid shrimp, Neomysis americana, may contribute to the low densities of these winter dominants after the planktivorous fishes repopulate the tidal creeks in the spring.

The occurrence of fish larvae in the diets of striped anchovies and Atlantic silversides also sug-gests a potential for influencing recruitment success for certain fish populations. Predation on fish lar-vae has been reported for several common coastal

marine fishes (Johannes 1978, Pepin et al. 1987), but the magnitude of the impacts remain unknown. Al-though the occurrence of some anchovy larvae among the gut contents of large striped anchovies was evidence of cannibalism, the low incidence of such predation suggests that a significant impact on anchovy populations is unlikely. However, Atlantic silverside consumption of late larval stages of spot and pinfish recruiting to estuarine habitats from ocean spawning areas may be an important and pre-viously unreported source of mortality for these dominant estuarine fishes. This observation is espe-cially noteworthy since the predation occurs during the coldest months when large predators are thought to be uncommon and the survival rates of recruiting fish larvae are expected to be high.

The importance of silversides and anchovies as forage for larger coastal fishes including bluefish, striped bass, mackerels (Merriman 1941, Bayliff 1950, Bigelow & Schroeder 1953, Schaefer 1971), and birds (Safina & Burger 1985, Takita et al. 1984) has been recognized in estuarine and coastal ocean systems over a wide geographic range. Conover & Ross (1982) discussed the potential importance of Atlantic silversides as exporters of estuarine pro-duction to the ocean during winter seaward migra-tions. The emigration of large numbers of bay an-chovies, striped anchovies, and rough silversides from the North Inlet Estuary each fall undoubtedly represents a major transfer of energy to the rela-tively low production areas outside of the inlet. We agree with other investigators that, since a signif-icant portion of the emigrating planktivorous fish populations does not survive to return to estuaries the following spring, the net balance of biomass and energy transfer strongly favors export to the coastal ocean.

In addition to confirming the important trophic role these fishes play as major consumers of zoo-plankton, we documented a new and direct trophic link between Spartina alterniflora and migratory fishes. Leafhoppers, which are among the few salt marsh herbivores, were consumed by rough and At-lantic silversides. Insects, including leafhoppers, have been reported in the diets of fishes associated with salt marshes (Pfeiffer & Wiegert 1981, La Salle et al. 1991), but the direct consumption of terres-

49

•

•

trial-based foods by predators more characteristic of open waters represents a more rapid and wide-spread transfer of energy to the estuary. In general, the Spartina-leafhopper-fish pathway offers more rapid turnover and greater efficiency in the transfer of energy than the Spartina (via microbial and me-chanical decay)-zooplankton-fish pathway. The sig-nificance of these linkages on the ecosystem level may not be substantial, but they illustrate that es-tuarine food webs are even more complex than they have been described previously.

Acknowledgements

We thank the many staff members and students of the Baruch Institute who assisted in the collection and processing of the field measurements and sam-ples. Special thanks go to D.L. Barker, C. Chapal, P. Kenny, and S. Service for their help with the collec-tions and with data management and to J. Schmidt for analyzing the fish stomach contents. K. Caul-field and S. Hutchinson assisted in the preparation of the manuscript. This study was supported by the National Science Foundation grant BSR-8514326 to the Belle W. Baruch Institute of the University of South Carolina for the Long-term Ecological re-search (LTER) Program. This paper constitutes Contribution Number 1005 from the Belle W Ba-ruch Institute for Marine Biology and Coastal Re-search of the University of South Carolina.

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