secondary production of macrobenthic invertebrates from delaware bay and coastal waters

I Int.Revueges.Hydrobio1. I 77 I 1992 I 2 I 187-201 1

DON MAURER~. STAVROS Horn* and WAYNE LEATHEM]

1 Biology Department California State University, Long Beach, CA 90840, USA 2 Molecular Ecology Institute California State University Long Beach, Ca 90840, USA

3Estuarine and Coastal Research, Inc. College of Marine Studies University of Delaware, Lewes, DE 19958, USA

Secondary Production of Macrobenthic Invertebrates from Delaware Bay and Coastal Waters

key words: secondary production, macrobenthic invertebrates, Delaware Bay waters

Abstract

Secondary production of benthic invertebrates was estimated for Delaware Bay and coastal Dela- ware. Production and turnover ratios were highest in Delaware Bay (P = 46,572 mg AFDW m-* yr-1, P : B = 6,O) and progressively lower at two coastal stations (P = 7,501 to 30,124mg AFDW m-2 yr-1, P : B = 2.3 to 5.3, and P = 4,485 to 4,492mg AFDW m-* yr-1, P: B = 2.3 to 4.8). Produc- tion was inversely related to sediment particle size. Production in Delaware Bay was relatively evenly distributed between deposit feeding polychaetes and suspension feeding molluscs with a definite shift in production dominance to suspension feeding molluscs at the coastal stations. Moreover, crustaceans and echinoderms played a larger role in production at the coastal stations than in Delaware Bay. Concerns about the health of soft-bottom communities i_n Delaware Bay expressed earlier were not supported here. Finally, it was concluded that P and P : B from the Dela- ware Bay area were very similar to those obtained from other areas in the North Atlantic which agrees with estimates for other estuaries in the northern hemisphere.

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188 (a) Sampling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188 (b) Laboratory processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188 (c) Environmental setting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190 (a) Annual trends in biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190 (b) Annual secondary production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192

4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194 (a) Seasonal variability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194 (b) Annual variability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 (c) The influence of sediment on production . . . . . . . . . . . . . . . . . . . . . . . 196 (d) Comparison of P and P : B with values from other areas . . . . . . . . . . . . . . . 197

5. S u m m a r y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 6. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197 7. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198

1. Introduction

Marine benthic invertebrate standing crop increases from the tropics to higher latitudes (THORSON, 1957; ZENKEVITCH, 1963; SANDERS and HESSLER, 1969; ROWE, 1983). In the northern hemisphere, benthic standing crop increases uniformly between the equator and

188 D. MAURER et al.

high latitudes (NEYMAN, 1965). According to NEYMAN (1965) this gradient in biomass is related to general latitudinal zoning in surface productivity of ocean waters. The relationship between surface productivity and benthic standing crop is not as one sided as earlier conceived. There is evidence to show that the benthos affects production in the water column not only by supplying nutrients directly, but also by enhancing rates of pelagic recycling (DOERING, 1989). Estimates of secondary production of benthos also appear to reflect the same latitudinal trend as standing crop. PETERSEN and Cmns (1 980) suggest that this relationship is based more on a relatively greater proportion of energy flow channeled from plankton to benthos in higher latitudes compared to the tropics than any absolute values of plankton production throughout the same latitudes.

For the northern hemisphere, WOLF (1977, 1983) concluded that secondary production of estuarine benthic invertebrates is high compared to other ecosystems. In contrast, prior studies in Delaware Bay showed a relatively low density and diversity of organisms (MAURER et al., 1978). Several hypotheses (predation, sediment transport, few attached algae, pollution) were invoked to explain the low density and diversity, particularly in the lower Bay. To more completely understand the Delaware Bay benthos, emphasis was shifted from describing community structure (species composition, density, diversity) to estimating community function (MAURER et al., 1979 a, b).

This paper descibes a study of secondary production of benthic invertebrates from Delaware Bay and nearby coastal waters. The study followed the design of studies per- formed earlier on both coasts of the United States (SANDERS, 1956; CAREY, 1962; NICHOLS, 1975, 1977; NICHOLS and THOMPSON, 1982) and in European waters (BUCHA- NAN and WARWICK, 1974; WARWICK et al., 1978; WARWICK, 1984; EVANS, 1983; GLEMA- REC and MENESGUEN, 1980; JOSEFSON, 1987).

2. Materials and Methods

a. Sampling

Station 29 (21 m depth) occurs in lower Delaware Bay and stations 31 (20m depth) and 32 (15 m depth) occur off the southern coast of Delaware (Fig.1). The coastal sites were included in the National Marine Fisheries Service Northeast Monitoring Program (NMFS/NEMP), in which benthic community structure was assessed biannually, throughout the middle and northern Atlantic coastal regions. Benthic samples were collected six times at stations 29, 31, and 32 during 1980 and six times at stations 3 1 and 32 in 198 1.

Production analyses were based on three replicate samples per station per sampling period with a Smith-McIntyre grab (0.1 m-2) except for July 1980 and December 1980 ( n = 5). Sampling and measurement of environmental variables were described in HOW and LEATHEM (1984). Samples were fixed with 10 % buffered formalin, stained with rose bengal, sieved through a 0.5 mm mesh, and stored in 70 % alcohol.

b. Laboratory processing

In the laboratory samples were sorted to major taxa, and measurements of wet weight and num- ber of individuals were recorded. Six species of bivalves and nine species of polychaetes were chosen as select species destined for direct measurement of secondary production (CRISP, 1971). For select species the following parameters were examined: total wet weight biomass, total density, and individual size. Size frequency distributions of each species were based on size measurements of a maximum of 100 randomly chosen individuals per replicate using indices of valve length for bivalves (valve width for Mytilus) and width of first chaetigerous segment for polychaetes.

Differentiation of size classes followed computer adapted methods of HARDING (1949) and CAS- SIE (1954) developed by S. HOW.

Secondary Production of Macrobenthic Invertebrates

D E L A W A R E B A Y

3 a05 0' - CAPE HENLOPEN

R E H O B O T H I 3 1'

A T L A N T I C O C E A N

38O40' -

0-

KILOMETER8

32 75poo' 38'30'-

189

Figure 1. Map of station locations in Delaware Bay and coastal waters from which benthic secondary production was assessed.

Regression curves were prepared for conversion of individual size indices (mm) to ash-free dry weight (AFDW expressed in mg) of preserved animals. For AFDW determinations, samples were decalcified using dilute HCL, oven dried for 24 hours at 90°C. and ignited in a muffle furnace for 2 hours at 45OOC. Regression lines of AFDW compared to individual size were summarized in HOWE and LEATHEM (1984). Total production per size class was calculated following CRISP (1971) for populations with recruitment and distinguishable age classes. Total production (P = mg AFDW/mz/yr), mean biomass (B = mg AFDW/m2) and annual production: biomass ratio (P : B ) were calculated for each species based on individual size classes. Cumulative annual totals were calculated as summations of individual size classes. These methods were described in detail elsewhere (HOW and LEATHEM, 1984). Those taxa not included among select species were termed residual species and production estimates were obtained by indirect measurements. Even though biomass and production estimates were restricted to the greater than 0.5 mm size fraction, archiannelids and oligochaetes in this size fraction provided considerable 13 Int. Revue ges. Hydrobiol. 'I? (1992) 2


biomass for certain sampling periods and for the present study, this group was categorized as meiofauna.

Estimates of production of residual species, required conversion of wet weight to ash-free dry weight (AFDW). These conversions were based on results for the select species per station collected for both years from _which an overall mean conversio-n valve (0.10) was assumed.

Turnover ratios (P : B ) and mean AFDW biomass (B ) values were used to estimate production ( P ) of residual species and other taxa. Turnover ratios were based on results for comparable fauna examined in other studies. Amphipod fauna were predominately of the families Haustoriidae and Aoridae and a P : B = 8.0 was used for isopod and amphipod crustaceans (ALBRIGHT and ARM- STRONG, 1982). A P : B = 2.0 was uzed for decapod crustaceans (RICHARDS and RILEY, 1967, BUCHANAN and WARWICK, 1974), P : B = 0.5 for echinoids (BUCHANAN and WARWICK, 1974) and P : B = 8.0 for microfauna (MCINTYRE, 1964, CEDERWALL, 1977).

Production estimates based on formalin preserved fauna were converted to estimates for unpre- served tissue using a correction factor of 1.15 (HOWMILLER, 1972, MILLS, et al., 1982). Values of non-preserved tissue production were converted to carbon production using a conversion factor of 0.45 (NICHOLS, 1975).

c. Environmental setting

KNEBEL (1989) provides a detailed account of modern sedimentary environments in Delaware Bay. Sediment at station 29 consists of a fine, well sorted sand (X 0 = 2.89) containing 14.8 % silt- clay, station 31 consists of a fine to medium sand (X 0 = 1.28) with a typical range of 15-28 % silt- clay, and station 32 consists of a medium, well-sorted sand (X 0 = 1.67) containing 0.6 % silt-clay. The range of bottom water temperature, salinity and dissolved oxygen for all stations was encom- passed by 3.5 to 21.9OC. 29.5 to 33.0760 and 2.01 to 6.72 (ml/l). Station 31 was the most heteroge- neous in terms of bottom topography and sediment type (mean 0, % silt-clay, % organic content).

3. Results

a. Annual trends in biomass

Mean benthic wet weight biomass (g m-2) and respective percent per sampling period were summarized (Table 1). Biomass was higher in 1980 than in 1981 and peak biomass was recorded at station 29. During 1980 at station 29 biomass ranged from 6.3 to 269.7 g m-2 with the maximum in June. The biomass maxima for each major taxa, including meiofauna, was consistently observed during the June period in 1980. Mean annual total biomass was 74.9 g m-2 with molluscs and polychaetes accounting for 93.5 % of the total (Table 1). Molluscs accounted for 81 % of the total biomass in August though the lowest total biomass was observed during this month.

During 1980 at station 3 1 biomass ranged from 7.7 to 116 g m-2 with the maximum in June and a secondary peak in September (Table 1). Molluscs and polychaetes mainly contributed to the June peak whereas the September peak was primarily influenced by molluscs. Biomass of microfauna peaked in July. In 1981, biomass ranged from 10.6 to 27.5 g m-2 with the maximum in September. Biomass values in 198 1 were generally lower and less varible compared to 1980 values. The September peak was primarily attributable to molluscs, polychaetes and echinoderm (Table 1).

During 1980 at station 32 mean biomass ranged from 4.8 to 59.0 g m-2 with the peak in July. In July, the sand dollar Echinarachnius parma (LAMARCK) accounted for 89.5 % of the total biomass. Regardless, mean annual total biomass at station 32 was considerably lower than at station 29 or 31. In 1981, mean biomass ranged from 3.8 to 15.2gm-2 with maxima in July and September. Between July and September there was a marked increase

Secondary Production of Macrobenthic Invertebrates 191

Table 1. Monthly and annual mean biomass (g wet weight m-2) of benthic invertebrates from the Delaware Bay area. (Figures in parentheses represent percent biomass relative

to each monthly total of entire fauna.)

Station 29

Month Polychaeta Mollusca Crustacea Echinodermata Meiofauna Total

1980 3 6 7 8 9

12

1980%

5.4 (33.5) 106.1 (39.3)

0.2 (3.2) 4.0 (45.8)

-

-

10.2 (63.4) 146.1 (54.2)

5.1 (81.0) 3.0 (41.1)

-

-

0 2.2 (0.8)

0.4 (6.3) 0.1 (1.4)

-

-

16.1 269.7

6.3 7.3

-

-

5.0(3.1) 0 15.3 (5.7) 0

0.6 (9.5) 0 0.2 (2.7) 0

4.2f7.4 0

- -

- - -

28.9 f 51.5 41.1 f70.1 0.9f 1.1 74.9 f 130.0

Station 31 I980

3 6 7 8 9

12

1980X

14.0 (37.7) 43.1 (37.1)

8.4 (34.6) 4.4 (26.7) 4.0 (4.3) 3.7 (48.1)

0.7 (1.8) 0.2 (0.3) 1.8 (7.4) 0.3 (1.8) 0.4 (0.4) 0.5 (6.4)

37.1 116.0 24.3 16.5 92.8 7.7

18.5 (50.0) 69.2 (59.8) 11.4 (46.9) 11.2 (67.9) 87.6 (94.4) 2.2 (28.6)

33.4 f 35.8

3.9 (10.5) 0 3.4 (2.9) 0 2.3 (9.5) 0.4 (1.6) 0.6 (3.6) 0 0.8 (0.9) 0 1.3(16.9) 0

2.05 f 1.38 0.07 + 0.15 12.9f 15.3 0.65 f 0.59 49.1 f 44.5

1981 4 6 7 9

10 11

1981 X

9.4 (68.5) 5.7 (53.8) 4.0 ( 16.6) 8.1 (29.6) 4.4 (32.8) 3.5 (18.8)

1.8 (13.1) 3.4 (32.1)

14.0 (58.1) 12.9 (46.9) 7.3 (54.6)

11.3 (60.8)

0.04 (0.3) 0.7 (6.6) 3.0 (12.4) 1.2 ( 4.4) 1.6 (11.9) 3.2 (17.2)

13.7 10.6 24.1 27.5 13.4 18.6

2.5(18.1) 0 0.8 (7.5) 0 3.1 (12.9) 0 1.4 (5.2) 3.8 (13.9) 0.1 (0.7) 0 0.6 (3.2) 0

1.4+ 1.2 0.6f 1.6

Station 32

5.9 + 2.4 8.5 f 1.5 1.6+ 1.3 18.0f 6.7

I980 3 6 7 8 9

12

1980 2

3.1 (64.6) 6.7 (53.8) 1.1 (1.9) 2.7 (19.1) 2.5 (19.7) 6.7 (47.2)

1.4 (29.2) 3.1 (24.4) 2.6 (4.4) 8.2 (58.2) 7.4 (58.3) 2.2 (15.5)

0.1 (2.1) 0.2 (1.6) 0.2 (0.3) 2.6 (18.4) 1.4 (11.0) 2.9 (20.3)

4.8 12.7 59.0

0.2 (4.7) 0 0.7 (5.5) 2.0 (15.7) 2.3 (3.9) 52.8 (89.5) 0.6 (4.3) 0 1.4(11.0) 0 0.7 (5.0) 1.7 (12.0)

1.0f0.8 9.4221.3

14.1 12.7 14.2

3.8 f 2.3 4.2 f 2.9 1.2+ 1.3 19.6+ 19.6

I981 4 6 7 9

10 11

1981 X 13.

1.5 (19.5) 3.0 (37.5) 4.2 (27.6)

10.1 (66.4) 4.4 (58.7) 0.7 (18.4)

3.8 (49.3) 1.4 (17.5) 4.6 (30.3) 1.5 (9.9) 0.6 (8.0) 0.1 (2.6)

1.3 (16.8) 0.9 (1 1.2) 3.9 (25.7) 1.3 (8.6) 1.5 (20.0) 2.5 (65.8)

7.7 8.0

15.2 15.2 7.5 3.8

1.1 (14.3) 0.01 (0.1) 2.7 (33.8) 0 1.9 (12.5) 0.6 (3.9) 1.7 (11.2) 0.6 (3.9) l.O(l3.3) 0 0.5 (13.2) 0

1.5f0.8 0.2f0.3 4.0f 3.3 2.0f 1.8 1.9f 1.1 9.6 f 4.6


in % polychaete biomass and a marked decline in % molluscan biomass. Peak percent of crustacean biomass and meiofaunal biomass also occurred at station 32. The former was in June and the latter was in July (Table 1).

b. Annual secondary production

For all stations through both years, the highest production was estimated at station 29 (P = 4637 1.8 mg AFDW m-2 y r l ) in 1980 (Table 2) representing estimated carbon production of 24,101 mg Cmm-2 y r l . This production at station 29 was 1.5 times greater than P at station 31 and 10 times greater than P at station 32. During 1981, production was greater at station 31 (P = 7,501.1 mg AFDW m-2 y r l ) than at station 32 P = 4,491.8 mg AFDW m-2 yr l ) , representing estimated carbon production of 3, 881.8mg C m-2 y r l and 2.424.5mg C m-2 yr1, respectively. Between 1980 and 1981, P declined (4 x) at station 3 1 while P remained at a similar level at station 32 for the same period (Table 2). For 1980 turnover ratios at stations 29, 3 1, and 32 were P : B = 6.0, 5.3 and 2.3, respectively, and for 198 1 P : B = 4.3 at station 3 1 and P : B = 4.8 at station 32.

During 1980 at station 29 three select pelecypod species Ensis directus CONRAD, Mytilus edulis LINNE and Tellina agilis STIMPSON accounted for 39.7 % of the recorded production, and one select polychaete species, Asabellides oculutu (WEBSTER), accounted for 48.6 %. Residual production estimates were comprised predominantly of molluscs and crustaceans (6.9 % and 2.2 % of total, respectively).

At station 31, A. oculata and M . edulis accounted for 67.4 % of the total 1980 production estimate. The remaining significant production consisted of other select species

Table 2. Total secondary production (mg AFDW m-2 yr-1) of benthic fauna. (P =Total Annual Production; B = Mean Annual Biomass; P : B =Turnover Ratio)

Station 29

1980 P

Direct Measurement

Polychaeta Mollusca

Direct Subtotal

Residual Measurement

Polychaeta Mollusca Crustacea Echinodermata Meiofauna

Residual Subtotal

Total AFDW

(Corrected Total)

(Total Carbon)

22,824.7 18.544.9

41.369.6

474.8 3,230.0 1,025.2

0 472.2

5,202.2

46,571.8

B P:B

1,929.9 11.8 4.390.9 4.2

6,320.8 6.5

197.8 2.4 765.4 4.2 415.5 2.5

7.0

1,466.2 3.6

7,767.0 6.0

0

(53,577.6)

(42,100.9)


Table 2. (continued) Station 31

I980 P

- 1981 - B P : B P B P : B

Direct Measurement

Pol ychaeta Mollusca

Direct Subtotal


Polychaeta Mollusca

Echinodermata Meiofauna

Crustacea

Residual Subtotal

Total AFDW

(Corrected Total) .

7,3 12.2 18.428.1

25,740.3

1,509.0 778.2

1.63 1 .O 3.0

462.0

4.383.2

30,123.5

(34,642.0)

(Total Carbon) (15,588.9)

774.8 3.607.5

4,382.3

824.6 152.3 203.9

6.1 66.0

1,252.9

5,635.2

9.4 5.1

5.9

1.8 5.1 8.0 0.5 7.0

3.5

6.3

Station 32

285.6 3.389.3

3,674.9

887.7 1,235.7

810.9 32.0

859.9

3,826.2

7,501 .O

(8,626.3)

(3.88 1.8)

131.2 668.0

799.2

412.9 243.5 101.4 63.9

122.8

944.5

1,743.7

2.2 5.1

4.6

2.1 5.1 8.0 0.5 7.0

4.1

4.3

Direct Measurement

Polychaeta Mollusca

Direct Subtotal


Polychaeta Mollusca Crustacea Echinodermata Meiofauna

Residual Subtotal

Total AFDW

(Corrected Total)

(Total Carbon)

I980 P

324.9 1.157.2

1.482. I

454.5 413.6 795.6 470.0 869.6

3.003.3

4,485.1

(5,158.2)

(2,321.1)

1981 - B P : B P B P : B

108.5 3.0 155.7 96.3 1.6 305.8 3.8 567.6 95.1 6.0

414.3 3.6 723.3 191.4 3.8

247.0 1.8 388.6 239.9 1.6 106.3 3.8 816.8 136.8 6.0 99.5 8.0 1,359.6 170.4 8.0

940.1 0.5 10.4 20.8 0.5 124.2 7.0 1.193.1 170.0 7.0

1,520.1 2.0 3,768.5 737.9 5.1

1,934.4 2.3 4,491.8 929.3 4.8

(5,165.6)

(2,424.5)


(18 %), residual polychaete fauna (5.0 %), and residual crustacean fauna (5.4 9%). Crusta- cean production consisted mainly of the amphipods, Unciofa irrorata SAY and Pseudun- ciofu obliquua (SHOEMAKER). During 198 1, production was primarily attributable to two select molluscan species, E . directus and T. agilis (45.2 %) and residual molluscs (16.5 %).

At station 32 during 1980 all select molluscan species exclusive of Nucula annufaru HAMPSON contributed to production. The major select producer was Spisula solidissirna (DILLWYN) which accounted for 19.5 % with the molluscan fauna (select plus residual) accounting for 35 % of the annual rate. Spisufa solidissima and residual molluscs were again dominant producers in 198 1. Moreover for both years residual crustaceans, microfauna, and to a lesser extent, echinoderms, were included among codominants.

4. Discussion

In this study sampling frequency was six times per year. Even though this expanded the quarterly sampling scheme of many seasonal studies, occasional time lags of up to three months between samplings sometimes precluded definitive assessment of growth and mortality in single size classes. Production estimates of groups with rapid P : B such as small crustaceans and microfauna require increased sampling frequency over that used herein for accurate direct estimates.

The decalcification of molluscs using dilute HCL probably underestimates actual macrofaunal production (KUENZLER, 1961; HUGHES, 1970; THAYER et ul., 1973; HOWE et af . , 1988). In this study, production estimates were limited to that portion of the fauna retained on a 0.5 mm sieve. For practical purposes this sieye size isyery feasible. How- ever, based on the inverse relationship between individual B and P : B , elimination of the smaller size fraction (< 0.5 mm sieve) underestimates total community P and P : B (ROBERTSON, 1979; BANSE and MOSHER, 1980). The present study summarizes only the growth component of an energy budget for benthic macrofauna.

a. Seasonal variability

Benthic invertebrates at stations 29 and 3 1 were characterized by similar species com- positions during 1980 (LEATHEM and HOWE, 1982). Polychaetes and molluscs comprised most of the total biomass and secondary production (HOWE and LEATHEM, 1984; HOWE et al., 1988). Total wet weight biomass and secondary production generally increased form the early spring, reached a peak in June-July, and decreased markedly in August (Table 1). Maximum densities for the dominant polychaete, A . oculara and molluscs, T. agilis and M . edulis contributed to the June production peak at station 29. At station 31 the production maxima was observed in March (HOWE et u f . , 1988).

A secondary peak in density was recorded in September which was attributable to the recruitment of juveniles of Asabeffides ocularu at station 29 (HOWE and LEATHEM, 1984) and Nucula annulata at station 31 (HOWE, er al., 1988). The corresponding production for these species remained low, but the modest production peak at station 31 was due to high densities of adult M. edufis.

During 1981 at station 31, trends in seasonal flux of density, biomass and secondary production were different from fluxes recorded in 1980. Recruitment of juvenile size classes during the spring were recorded for the polychaetes Nephrys incisa MALMGREN and Aricidea catherinae (LAUBIER), although densities were low relative to 1980 (HOWE and LEATHEM, 1984). Total biomass and secondary production peaks for polychaetes were recorded in September (Table 1). These maxima were comprised principally of


Mediomastus ambiseta (HARTMAN). Seasonal trends in 198 1 for molluscs indicated peaks in biomass and production during July and September (Table 1). Evidence suggests that recruitment in T. agilis and M. edulis probably preceded the April sampling period (HOWE et al., 1988). A secondary recruitment period in September was recorded only for T. agilis.

Benthic fauna at station 32 had consistently lower monthly values of secondary production, biomass and density compared to the fauna at stations 29 and 31 (Table 1). Maximum densities were recorded in March 1980 for molluscs and polychaetes (HOWE and LEATHEM, 1984; HOWE et al., 1988). A secondary recruitment period was observed in September for the polychaetes Ampharete arctica MALMGREN and Aricidea catherinae. Production maxima were observed in June for polychaete fauna and in September for molluscs.

Seasonal trends at station 32 were less variable from 1980 to 1981 than ones at stations 29 and 3 1. For dominant select polychaete species, recruitment was recorded during the winter (December, 1980) as well as the spring (April, 1981) and polychaete production peaked again in early summer. Two peaks for total molluscan production in 1981 were attributable to the spring recruitment period (April) as well as the maximum monthly production rate of Spisula solidissima (July).

b. Annual variability

Total secondary production exhibited marked annual variability at station 3 1. Total production in 198 1 represented approximately a four-fold reduction from 1980 (Table 2). Total polychaete production decreased almost eight-fold, attributable to the absence of Asabellides oculata during 198 1 (HOWE and LEATHEM, 1984).

Similarly, the absence of a single molluscan species, M . edulis, in 1981 contributed to a four-fold reduction in total annual molluscan production (Table 2; HOWE et al., 1988).

Total secondary production was very consistent between 1980 and 1981 (Table 2). Total polychaete production decreased from 779 to 544 mg AFDW m-2 y r * , again principally due to the absence of A. oculata (HOWE and LEATHEM, 1984). Total molluscan production decreased slightly in 1981. A reduction in the dominant select species, S. solidissima and T. agilis was balanced by a coincidental increase in the production of residual molluscan species (HOWE, et al., 1988). Moreover, crustaceans and meiofauna were significant producers at station 32 (Table 2).

The presence or absence of M. edulis and A. oculata strongly influenced the ratio of epifaunal : infaunal production at station 3 1. In 1980 the epifaunal component was dominant whereas in 198 1, the infaunal component dominated secondary production.

The influence of both species on the epifaunal : infaunal ratio was greatly diminished at station 32.

Population dynamics in temperate areas fluctuate seasonally with high densities and biomass normally associated with warmer temperatures. Reproductive cycles strongly influence temporal patterns of production (KECK et al., 1975). In a long term study of secondary production in the Skagerrak, JOSEFSON (1987) argued that the major cause of variability in production estimates is due to changes in sedimentation of organic matter. In Great Sound a coastal lagoon in New Jersey GRIZZLE and MORIN (1989) showed that tidal currents, seston and sediments positively influenced the growth of the hard clam Mercenaria mercenaria (LINNE).

In the present study, dominant molluscan species such as T. agilis and E. directus have different spawning maxima in Chesapeake Bay and the adjacent coastal waters. (CHAN- LEY and ANDREWS, 1976, DAUER et al., 1984). For S . solidissima, another dominant bivalve in Delaware coastal water, ROPES (1980) recorded two spawning periods which can


contribute to seasonal variability. Finally, the major molluscan producer in this study, M . edulis, is capable of considerable variability in spawning (NEWELL, et al., 1982).

Polychaetes represent the other major group of producers in this study and temporal variations in annual production and biomass are also expected. PRICE and WARWICK (1980) showed considerable annual variation in P, B and P : B for Nephtys and Ampha- rete. According to them, variability was mainly due to reproductive biology and long- evity.

Unusual temperatures or prevailing currents can effect seasonal and annual variability in recruitment and production (FRANZ 1976, BEUKEMA, 1974, 1979; EPIFANIO et al. , 1984). Severe low winter temperature in the Dutch Wadden Sea resulted in significant declines of macrobenthic biomass (BEUKEMA, 1979). Annual production of dominant infauna in Gullmar Fjord varied by a factor of 1 to 22 between 1977 and 1982 (MOLLER et al., 1985). The convergence of tidal and longshore currents may serve to trap larvae of S. solidissima off western Long Island (FRANZ, 1976). Since the relative strength of this convergence varies seasonally and annually, it effects recruitment accordingly.

There is evidence to indicate that seasonal variability in recruitment of benthos in mid- Atlantic estuaries and adjacent coastal waters may be partly due to physical processes (EPIFANIO et al., 1984). During warmer months some meroplankton may directly settle on the inner continental shelf. However, some portion of the meroplankton may be entrained from the inner shelf into the estuaries. Onshore transport of meroplankton along the thermocline has been proposed as a mechanism (EPIFANIO, et al., 1984). The duration of onshore transport contributes to variability of recruitment in these estuaries.

c . The influence of sediment on production

Total secondary production was highest at station 29, intermediate at station 3 1, and lowest at station 32 (Table 2). This pattern reflected a distance gradient from the estuary and a production-sediment association. Production was lower further from the estuary and with increasing sediment size.

WARWICK and UNCLES (1980) described a close correlation between both sediment bed rype and community type and the tidally average M2 bed stress. WARWICK (1982, 1984) examined the relationship between bed stress and the partitioning of total production among species. We postulate that bed stress at station 3 1 and 32 would be higher than the relatively protected position of station 29. Environmental conditions at station 3 1 and particularly station 32 would be very similar to those projected to support a Venus (Sp i - sula) community following WARWICK and UNCLES (1980). In fact, total production at station 32 was dominated by Spisula solidissima (HOWE, et a[., 1988). According to WAR- WICK’S (1984) scheme, production at station 31 and 32 should be due to a trophically mixed community dominated by a single species or several species of suspension feeders. Total production at station 31 and 32 was dominated by molluscan suspension feeders exclusive of T. agilis which exhibits a dual feeding mode (suspension and deposit). Again, following WARWICK (1980), production at station 29 might be expected to be dominated by deposit feeders in contrast to dominant suspension feeding types at stations 3 1 and 32. At station 29 in Delaware Bay total production was dominated by the deposit feeding polychaetes Asabellides oculatua, Mediomastus ambiseta and Amastigos cape- rutus (EWING and DAUER) and by the suspension feeding molluscs M . edulis, E. directus and dual feeding T. agilis (HOWE and LEATHEM, 1984, HOWE et al., 1988). Production of A. oculata provided almost 50 % of the total production compared to the three molluscs.

Based on hydrodynamic conditions and community types proposed by WILDISH and KRISTMANSON (1979), WARWICK and UNCLES (1980) and WARWICK (1984). the emergence of a trophically mixed local fauna dominating production under comparable condition is


consistent with their predictions. In our view, the work of WILDISH and KRISTMANSON (1979) is probably more appropriate for estuaries and enclosed bodies of water and that of WARWICK and UNCLES (1980) and WARWICK 1984) is more appropriate for open coastal and shelf waters. It is interesting to see how closely their work was presaged earlier by SANDER’S (1958) concerns over the effect of hydrodynamic processes in community structure and function.

According to EMERSON ( 1989) the influence of windforced hydrodynamics on plankton and sediment has been widely recognized even in environments with strong tidal action. EMERSON developed regression models relating macrobenthic secondary production to physical variables. Wind stress was the most significant variable accounting for observed variation in benthic secondary production (EMERSON, 1989).

d. Comparison of P and P : B with values from other areas

Production estimates obtained from Long Island Sound, Swansea Bay, and Carmarthen Bay England, and Gullmar Fjord, Sweden were lower than estimates for the Delaware Bay station (Table 3). Production levels greater than that recorded for Delaware Bay were obtained from the Ythan Estuary, England and the Grevelingen Estuary, Netherlands (Table 3). In both cases M . edulis was a dominant producer. Production of M . edulis at the Delaware Bay station (29) was significant but not as dominant as at coastal station 31 (HOWE et al., 1988). Production in estuaries is quite high compared to other marine habitats because of the relative abundance of food, food availability and a predominance of relatively opportunistic species characterized by high growth rates and a rapid turnover (WOLFF, 19-83).

The P : B for the Delaware Bay-station (6.0) exceeded those frqm Long Island s_ound ( P : B = 2.6), Carmarthen Bay ( P : B = 0.6), and Swansea Bay ( P : B = 1.0). The P : B for the coastal stations (31 and 32) ranged from 4.3 to 5.3 and from 2.3 to 4.3, respectively (Table 2). Community turnov-er ratios at station 31 were closer to the P : B of the Dela- ware Bay station than the P : B at coastal station 32.

5. Summary

Total secondary production and P : B was highest in Delaware Bay and correspond- ingly lower away from the Bay. Production estimates from Delaware Bay and the adje- cent coastal area were very comparable to those reported from other soft bottoms in the North Atlantic (Table 3). STEIMLE’S (1982) review of the literature-suports this conten- tion. Based on total community P and P : B (Table 2) and P and P : B of major taxa such as molluscs and polychaetes concerns about the health of soft-bottom benthic communities in Delaware Bay expressed earlier (MAURER et al., 1978) were not supported here. Moreover, these findings agree with the observations proposed by PETERSEN and CURTIS (1980) and WOLFF (1983) involving relatively high benthic production in higher latitudes compared to the tropics, and the potential of estuaries to support some of the highest secondary production estimates recorded in marine habitats.

6 . Acknowledgements

This research was supported by the National Marine Fisheries Services Northeast Monitoring Program (grant # NA-80-FA-C-00032). We are pleased to thank Dr. JOHN PEARCE, Mr. R. REID, Mr. F. STEIMLE, R. TERRANOVA, Ms. A. Frame and Mrs. K. SCUDLARK for their help.


Table 3. Comparison of macrobenthic community production for the Northern Atlantic Ocean (P = mg AFDW m-2 yr-1; sieve size expressed in mm)

Sediment Type

Silt

Mud

Mud

Fine sand

Fine sand & silt

Mixed silt-sand

Mixed sild-sand

Mixed mudl fine sand

Fine sand

Fine sand

Medium sand

Rock & gravel

Locality Condition Genus Produc- Sieve tion Size

Northumberland, 80m Heteromastus 1,738 0.5 England Glycera

Long Island 8-29m Nephtys 29,600 0.3 Sound, U.S.A. Pandora

Yoldia Cistenides

Long Island 9-17m Ampharere 20,025 0.3 Sound, U.S.A. Neomysis

Delaware Bay 21 m Asabellides 46,572 0.5 (Sta. 29), U.S.A. Ensis

Coastal 19m Asabellides 7,501-30,124 0.5 Delaware Mytilus (Sta. 31), U.S.A.

S wansea, 14m Abra 14,200 0.5 England

Ythan Estuary, 2.5m Mytilus 108,250 0.6 England Hydrobia

Estuary, Arenicola Netherlands Mytilus

Spiophanes

Asterias

Grevelingen 6 m Macoma 57,400 1.0

Cerastoderma Hydrobia

Carmathen Bay, 9-17m Pharus 25,800 0.5 England Spiophanes

Venus

Gullmar Fjord, 1 m fygospio 26,500 0.5 Sweden Capitella

Coastal 15m Aricidea 4.492 0.5 Delaware Ampharete (St. 32), U.S.A. Spisula

Bristol Channel, 37m Modiolus 34,100 0.5 England

Corophium

- Author

BUCHANAN & WARWICK, 1974 BUCHANAN et al., 1974

SANDERS, 1956

RICHARDS & RILEY, 1967 (including estimates from SANDERS, 1956)

Present study

Present study

WARWICK, 1984

BAIRD & MILNE, 1981

WOLFF. 1977

WARWICK et al., 1978

EVANS, 1983

Present study

WARWICK. 1984

7. References

ALBRIGHT, R., and D. ARMSTRONG, D. 1982: Corophium spp. productivity in Grays Harbor, Wash- ington, Grays Harbor and Chehalis River Improvements to Navigation Environmental Studies.- Technical Report to Washington Game Dept. and U.S Army Corps of Engineers: 1-3.

BAIRD, D., and H. MILNE, 1981: Energy flow in the Ythan Estuary, Aberdeenshire, Scotland.-Est. Coast., Shelf Sci. 13: 455-472


BANSE, K., and S . MOSHER, 1980: Adult body mass and annual production/biomass relationships of field populations.-Ecol. Monogr. 50: 355-379.

BEUKEMA, J. J., 1974: Seasonal changes in the biomass of the macrobenthos of a tidal flat in the Dutch Wadden Sea.-Netherlands J. of Sea Res. 8: 94-107.

BEUKEMA, J. J., 1979: Biomass and specis richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea: Effects of a severe winter.-Netherlands J. of Sea Res. 13:

BUCHANAN, J. B., P. F. KINGSTON and M. SHEADER, 1974: Long-term population trends of the benthic macrofauna in the offshore mud of the Northumberland c0ast.J. Mar. Biol. Ass. U.K.,

BUCHANAN, J. B., and R. M. WARWICK, 1974: An estimate of benthic macrofaunal production in the offshore mud of the Northumberland c0ast.J. Mar. Biol. Ass. U.K., 54: 197-222.

CAREY, A. G., 1962: an ecological study of two benthic animal populations in Long Island Sound.-Ph. D. dissertation, Yale University, New Haven, CT. p. 1-6 1.

CASSIE, R. M., 1964: Some uses of probability paper in the analyses size frequency distributions.- Aust. J. Mar. Freshw. Res. 5: 513-522.

CEDERWELL, H., 1977: Annual macrofauna production of a soft bottom in the Northern Baltic Proper. In: B. F. KEEGAN, P. 0. CEIDIGH, and P. J. S . BOADEN (eds.), Biology of Benthic Organ- isms. Oxford: Pergamon Press, p. 155-164.

CHANLEY, P., and J. D. ANDREWS, 1971: Aids for identification of bivalve larvae of Virginia.- Malacologia 11: 45-1 19.

CRIPS, D. J. , 1971: Energy flow measurements. I n : N. A. HOLME, and A. D. MCINTYRE (eds.), Methods for the study of Marine Benthos, IBP Handbook 16. Cambridge University Press, Cam- bridge, U.K., p. 197-280.

DAUER, D. M., T. L. STOKES, H. R. BARKER, R. M. EWING and J. W. SOURBEER, 1984: Macrobenthic communities of the lower Chesapeake Bay. IV. Bay-wide transects and the inner Continental Shelf.-Int. Revue ges. Hydrobiol. 69: 1-22.

DOERING, P. H., 1989: On the contribution of the benthos to pelagic production.-J. Mar. Res. 47:

EMERSON, C. W., 1989: Wind stress limitation of benthic secondary production in shallow, soft- sediment communities.-Mar. Ecol. Prog. Ser. 52: 65-77.

EPIFANIO, C. E., C. C. VALENTI and A. E. PEMBROKE, 1984: Dispersal and recruitment of blue crab larvae in Delaware Bay, U.S.A.-Est. Coast. Shelf Sci. 18: 1-12.

EVANS, S., 1983: Production, predation, and food niche segregation in a marine shallow soft-bottom community.-Mar. Ecol. Progr. Ser. 10: 147-157.

FRANZ, D. R., 1976: Distribution and abundance of inshore populations of the surf clam Spisula sblidissirna.-Limnol. Oceanogr. Spec. Sym. 2: 404413.

GLEMAREC, M., and A. MENESGUEN, 1980: Functioning of a muddy sand ecosystem: Seasonal fluctuations of different trophic levels and difficulties in estimating production of the dominant macrofauna species. In: K. R. TENORE and B. C. COULL (eds.), Marine Benthic Dynamics, Belle W. Baruch Library in Marine Science No. 11. University of South Carolina Press, p. 49-68.

GRIZZLE, R. E., and P. J. MORIN, 1989: Effect of tidal currents, seston, and bottom sediments on growth of Mercenuriu mercenaria: Results of a field experiment.-Mar. Biol. 102: 85-93.

HARDING, J. P., 1949: The use of probability paper for the graphical analysis of polymodal frequency distributions.-J. Mar. Biol. Assoc. U.K. 28: 141-153.

HOWE, S., and M. LEATHEM, 1984: Secondary production of benthic macrofauna at three stations of Delaware bay and coastal Delaware.-NOAA Tech. Mem. NMFS-F/NEC 32: 1-62.

HOW, S., M. LEATHEM and D. MAURER 1988: Secondary production of benthic molluscs from the Delaware Bay and coastal area.-Est. Coast. Shelf Sci. 26: 81-94.

HOWMILLER, R., 1972: Effects of preservatives on weights of some common macrobenthic invertebrates.-Trans. Amer. Fish. SOC. 101: 764-753.

HUGHES, R. N., 1970: An energy budget for a tidal flat population of Scrobiculariu planu (DA COSTA).-J. Anim. Ecol. 39: 357-381.

JOSEFSON, A. B., 1987: Large-scale patterns of dynamics in subtidal macrobenthic assemblages in the Skagerrak: Effects of a production related factor?-Mar. Ecol. h o g . Ser. 38: 13-23.

KECK, R. T., D. MAURER and H. LIND, 1975: A comparative study of the hard clam gonad develop- mental cycle.-Biol. Bull. 148: 243-258.

203-223.

54: 785-795.

371-383.


KNEBEL, H. J., 1989: Modem sedimentary environments in a large tidal estuary, Delaware Bay.- Marc. Geol. 86: 119-136.

KUENZLER, E. J., 1961: Structure and energy flow of a mussel population in a Georgia salt marsh.-Limnol. and Oceanogr. 6: 191-204.

LEATHEM, W., and S. HOW, 1982: Monitoring of benthic communities at two NEMP stations of coastal Delaware.-Final Report submitted to NOAA/NMFS for Northeast Monitoring Program,

MCINTYRE, A. D., 1964: Meiobenthos of sub-littoral muds.-J. Mar. Biol. Assoc., U.K., 44: 665-674.

MAURER, D., L. WATLING, P. KINNER, W. LEATHEM and C. WETHE, 1978: Benthic invertebrate assemblages of Delaware Bay.-Mar. Biol. 45: 65-78.

MAURER, D., L. WATLING, W. LEATHEM and P. KINNER, 1979a: Seasonal changes in feeding types of estuarine benthic invertebrates from Delaware Bay.-J. Exp. Mar. Biol. Ecol. 36: 125-155.

MAURER, D., W. LEATHEM, P. KINNER and I. TINSMAN, 1979b: Seasonal fluctuations in coastal benthic invertebrate assemblages-Est. Coast. Shelf Sci. 8: 181-193.

MILLS, E., K. PIITMAN and B. MUNROE, 1982: Effect of preservation on the weight of marine benthic invertebrates.-Can. J. Aquat. Sci. 39: 22 1-224.

MOLLER, P., L. PIHL and R. ROSENBERG, 1985: Benthic faunal energy flow and biological interac- tion in some shallow marine soft bottom habitats.-Mar. Ecol. Prog. Ser. 27: 100-121.

NEWELL, R. I. E., T. J. HILBISH, R. K. KOEHN and C. J. NEWELL, 1982: Temporal variation in the reproductive cycle of Mytilus edulis L. (Bivalvia, Mytilidae) from localities on the east coast of the United States.-Biol. Bull. 162: 299-310.

NEYMANN, A. A., 1965: Some data on the quantitative distribution of benthos on the Australian coastal shelf.-Oceanology 5: 108-1 12.

NICHOLS, F. H., 1975: Dynamics and energetics of three deposit-feeding benthic invertebrate populations in Puget Sound, Washington.-Ecol. nonogr. 45: 57-82.

NICHOLS, F. H., 1977: Infaunal biomass and production on a mudflat, San Francisco Bay, Califor- nia. In: B. C. COULL (ed.), Ecology of Marine Benthos, Belle W. Baruch Library in Marine Science No. 6. University of South Carolina Press, p. 339-357.

NICHOLS, F. H., and J. K. THOMPSON, 1982: Seasonal growth in the bivalve Mucoma balthica near the southern limit of its range.-Estuaries 5: 110-120.

PETERSEN, G. H., and M. A. CURTIS, 1980: Differences in energy flow components of subarctic, temperate, and tropical marine shelf ecosystems.-Dana 1: 53-64.

PRICE, R., and R. M. WARWICK, 1980: Temporal variations in annual production and biomass in estuarine populations of two polychaetes, Nephrys hombergii and Ampharefe ucurifrons.-J. Mar. Biol. Ass., U.K. 60: 481-487.

RICHARDS, S. W., and G. A. RILEY, 1967: The benthic epifauna of Long Island Sound.-Bull. Bing. Oceanogr. Coll. 19: 89-127.

ROBERTSON, A. I., 1979: The relationship between annual production : biomass ratios and lifespans for marine macrobenthos.-Oecologia 38: 193-202.

ROPES, J. W., 1980: Biological and fisheries data on the Atlantic surf clam, Spisula solidissima (DILLwYN).-NMFS, Sandy Hook Laboratory. Tech. Serv. Rep. 24: 1-88.

ROWE, G. T., 1983: Deep-sea biology. The Sea, Vol. 8 . John Wiley and Sons. p. 1-560. SANDERS, H. L., 1956: Oceanography of Long Island Sound, 1952-1954, X. The biology of marine

SANDERS, H. L., 1958: Benthic studies in Buzzards Bay. 1. Animal-sediment relationships.-Limnol.

SANDERS, H. L., and R. HESSLER, 1969: Ecology of the deepsea benthos.-Sci. 163: 1419-1424. STEIMLE, F. W., 1985: Biomass and estimated productivity of the benthic macrofauna in the New

THAYER, G. W., M. E., SCHAAF, J. W. ANGELOVIC and M. W. LACROIX, 1973: Caloric measurements

THORSON, G., 1957: Bottom communities.- Geol. SOC. Amer. Mem. 67(I): 461-534. WARWICK, R. M., 1982: The partitioning of secondary production among species in benthic com-

WARWICK, R. M., 1984: The benthic ecology of the Bristol Channel.- Mar. Poll. Bull. 15: 70-76. WARWICK, R. M., C. L. GEORGE and J. R. DAVIES, J. R., 1978: Annual production of macrofauna in

p. 1-20.

bottom communities.-Bull. Bing. Oceanogr. Coll. 15: 345-414.

Oceanogr. 3: 245-258.

York Bight: A stressed coastal area.-Est. Coast. Shelf. Sci. 21: 539-554.

of some estuarine organisms.-Fish. Bull. 71: 289-294.

munities.-Netherlands J. Sea Res. 16: 1-16.

a Venus community.-Est. Coast. Shelf Sci. 7: 215-241.

Secondary Production of Macrobenthic Invertebrates 20 1

WARWICK, R. M.. and R. J. UNCLES, 1980: Distribution of benthic macrofauna associations in the Bristol Channel in relation to tidal stress.-Mar. Ecol. h o g . Ser. 3: 97-103.

WILDISH, D. J., and D. D. KRISTMANSON, 1979: Tidal energy and sublittoral macrobenthic animals in estuaries.-J. Fish. Res. Bd. Can. 36: 1197-1206.

WOLFF, W. J., 1977: A benthic food budget for the Grevelingen Estuary, the Netherlands, and a consideration of mechanics causing high benthic secondary production in estuaries. In: B. C. COULL (ed.), Ecology of Marine Benthos. Belle Baruch Matine Library in Marine Science No. 6. University of South Carolina Press, Columbia, S.C., p. 267-280.

WOLFF, W. J.. 1983: Estuarine benthos. In: B. H. KETCHUM (ed.), Estuaries and Enclosed Seas. Elsevier Scientific Publishing Co., Amsterdam, p. 151-192.

ZENKEVITCH, L., 1963: Biology of the Seas of the U.S.S.R. George Allen and Unwin LTD, London, 1-958.

secondary production of macrobenthic invertebrates from delaware bay and coastal waters

Documents