Interactive effects of temperature and predation on an estuarine zooplankton community

J. Exp. Mar. Biol. Ecol., 1983, Vol. 12, pp. 67-81

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Elsevier

INTERACTIVE

EFFEKTS OF TEMPERATURE ESTUARINE

ZOOPLANKTON

ROLLAND

AND PREDATION

ON AN

COMMUNITY

S. FULTON III’

Duke Universi@ Marine Laboratory, Beaufort. NC28516,

U.S.A.

Abstract: The winter planktonic copepod community of the estuaries near Beaufort N.C. underwent a consistent transition from dominance by Acartia tonsa Dana to dominance by Centropages spp., which was

associated with unpredictable decreases in water temperature and increases in abundance of predatory mysids. Cenfropuges subsequently remained dominant until spring. Experimental ma~pulations of water temperature and mysid abundance in enclosures showed that copepod species composition was determined by an interaction of direct temperature effects with predatory interactions among copepods and mysids. Low temperatures stimulated recruitment of Centropages spp. and inhibited recruitment of Acartia toma. Temperature decreases also apparently stimulated migration of mysids into the study area, While A. tonsa was dominant, selective predation by mysids reduced the relative abundance of A. toma, but after Cenfropages became dominant mysid predation had no effect on copepod species composition. Predation by Cenfropages on the nauphi of other species probably cont~buted to its persistent dominance in the estuary. Rising temperatures in the spring favored recruitment of Acartia tonsa and inhibited Centropages recruitment. Selective predation by tish entering the estuary in spring may have contributed to the decline in abundance of Centropages spp. and mysids.

Factors influencing the distribution and seasonal succession of marine zooplankton are poorly understood. Estuarine and coastal zooplankton have been classified by their depth, temperature, and salinity associations (Jeffries, 1967; Fleminger, 1975), but in many cases these are based only on observational studies of copepod ~st~bution. Recent experimental studies (Lonsdale, 1981) have shown that distribution and abundance patterns cannot be explained solely by physical tolerances. Studies of freshwater zooplankton have focused on biological processes, particularly predation, as determinants of distribution and succession (Brooks & Dodson, 1965; Dodson, 1974; Lynch, 1979; Zaret, 1980). However, zoogeographic studies indicate that predation cannot completely explain zoopl~kton associations and suggest that physical and chemical factors also play important roles (Dodson, 1979). There have been only a few studies indicating how biological and physical factors interact to determine zooplankton composition. Neill (1978) found that Duphniu pulex was excluded from a British Columbia lake by a combination of predation, low food ’ Present address: Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3407 Arendell Street, Morehead City, NC 28557, U.S.A. 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.

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ROLLAND S.FULTONIII

concentrations, and water quality. Neil1 (198 1) also showed that the effects of predators on a zooplankton community depended on water temperature. Marine zooplankton, at least those from temperate estuarine and coastal habitats, are subject to extensive temporal variation in their environment. There is an increasing awareness that the structure and diversity of many communities are strongly influenced by temporal variation or environmental disturbance which may prevent competitive or predatory exclusion (Hutchinson, 1961; Richerson et al., 1970; Wiens, 1977; Connell, 1978; Huston, 1979). The zooplankton community of the estuaries near Beaufort, N.C., undergoes consistent changes in species composition during the winter, from a community dominated by Acartiu tonsu Dana and other small copepods to one dominated by Centropuges spp. (Fulton, in press). In this paper, I report on how fluctuations in water temperature interact with predation to determine winter zooplankton community structure.

STUDYCOMMUNITY

The study area is a shallow estuarine system near Beaufort, N.C. This system has an average depth of 1 m at mid-tide with a tidal range of 0.8 m. The water column is well mixed, with no vertical stratification. Salinity and water temperature range from 24 to 36x0 and 2 to 32 “C, respectively. For a further description of the study area see Thayer (1971), Thayer et al. (1974), or Fulton (in press). The winter zooplankton is dominated by the copepods Centropuges spp. (largely C. humutus Lilljeborg, but some C. typicus Kroyer are also present). Acurtiu tonsu is dominant in spring and frequently during the fall, but declines in abundance during the winter (Fulton, in press). The mysids Neomysis americana and Mysidopsis bigelowi are abundant during the winter (Williams, 1972; Fulton, 1982a). Mysids are believed to be important predators in freshwater zooplankton communities (Morgan et al., 1978; Murtaugh, 1981; Rieman & Falter, 1981), and a similar role has been suggested for estuarine mysids (Heinle & Flemer, 1975). Laboratory predation experiments have indicated that these mysids feed preferentially on Acurtiu tonsu and may consume a substantial portion of copepod standing crop (Fulton, 1982~). METHODS

AND MATERIALS

From March 1979 to April 1981, macroinvertebrate predators and fish larvae were sampled biweekly, at night, at the surface and just above the bottom (at the surface only in 1979). Duplicate samples at each depth were taken from a central channel at the mouth of the Newport River, with a l-m diameter, 500~pm plankton net fitted with a flowmeter. The net was set from a futed platform and allowed to stream in tidal currents during the period of strongest current flow, 2-3 h after high tide. Current velocities at this location may exceed 5 m * s - ’ (Kjelson &Johnson, 1976). Copepods were sampled

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INTERACTIONS

69

at the mouths of the Newport and North Rivers. In 1978-1980 triplicate samples were taken during the day with a centrifugal pump with an intake diameter of 5 cm and a flow rate averaging 250 I * min - ‘. The intake was placed 5 cm above the bottom and the outflow strained through a 75-pm net. In 198 1 duplicate surface tows were taken at night with a 75pm, 30-cm diameter plankton net fitted with a flowmeter. Tow duration was < 10 s to prevent net clogging. If the volume filtered was < 500 1, the net was washed down and another tow taken. Samples taken at the bottom during the day or at the surface at night both adequately sample the dominant copepods of the Newport River estuary, which aggregate near the bottom during the day and disperse through the water column at night (Fulton, in press). Surface water temperatures were measured with a mercury thermometer during biweekly sampling. During the periods of enclosure experiments (see below), water temperatures were measured daily; weekly average temperatures were calculated from these daily measurements. Experimental studies of the effects of mysid predation and varying water temperatures on copepod composition were carried out in 1980 and 1981, using outdoor fiberglass enclosures of 600 to 1000 1in which manipulations were performed. I believe that relatively small enclosures can reasonably approximate natural conditions because of the shallow depth and complete mixing of local estuaries. The enclosures were initially filIed with estuarine water strained through a 75-pm mesh net to remove macrozooplankton. Zooplankton were added at natural densities from collections taken at night, when the copepods are most homogeneously distributed in the water column (F&on, in press). Surface tows were taken with a 75pm mesh, 30-cm diameter net fitted with a Rowmeter. The collection was well mixed, then split into sections with a Folsom plankton splitter, and subsamples were added to each of the enclosures. The zoopl~kton additions were strained through a l-mm mesh to remove mysids or other large predators. No such predators were observed in controls. Mysids were added from separate collections. In 1980, four subsamples were retained for analysis of initial composition; in 1981 each of the enclosures was sampled immediately after additions were made. The enclosures were mixed twice daily by bubbling from the bottom with compressed air, to keep them well mixed and oxygenated, as is the case in the estuary. Nutrients (nitrate, phosphate, and silicate in a 10 N : 1 P : 10 Si ratio) were added to keep phytoplankton biomass from falling substantially below that in the estuary. In 1980, 2 pg-at. N 9l- ’ were added every 10 days for the first 20 days. In 1981,2 pg-at. N - l- ’ were added approximately every 10 days for the length of the experiment. Phytoplankton biomass was estimated from fluorometric determinations of chlorophyll a taken at least twice weekly after mixing. Zooplankton were sampled weekly by vertical hauls with a 30-cm diameter, 75pm plankton net, after thorough mixing of the enclosures. Each sample filtered approximately 5% of the volume of the enclosures. Mysids were not sampled quantitatively with this method. At the end of the experiments, the enclosures were completely drained and the remaining mysids counted. Zooplankton samples were preserved in 5% formalin. All copepodites were identified to species and

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S. FULTON

III

grouped into two age classes, copepodite stages CI-CIII and stages CIV-CVI. Nauplii were not identified to species. The 1980 experiments were begun on 3 February and completed on 27 March. Nine enclosures were used, five of which held 600 I with a depth of 0.5 m and four held 1000 1 with a depth of 0.8 m. The large enclosures had a running sea-water bath which moderated water temperatures, while the small enclosures lacked a bath and underwent more extreme temperature fluctuations, particularly reaching lower minimum temperatures. Two large enclosures received 80 mysids * rnw3 (70 Neomysis americana and 10 Mysidopsis bigelowi, which is well within the range observed in the estuary), and two served as controls. One small enclosure initially received 80 mysids - m - 3 (70 Neomysis americana and 10 Mysidopssisbigeiowi), three received 160 mysids . m - 3 (140 Neomysis americana and 20 ~ys~ops~ bigelowi), and one served as a control. The 1981 experiments were begun on 7 February and completed on 29 March. Six 600-l enclosures were used, all of which were immersed in a inning sea-water pool at the Institute of Marine Sciences, Univ. North Carolina, in order to keep water temperatures close to ambient. Three enclosures were controls and three received 116 mysids m - ’ (100 Neomysis americana and 16 Mysidopsis bigelowi). The results of the enclosure experiments were analyzed by a split plot analysis of variance (ANOVA), alternatively termed a repeated measures design (Winer, 1971). This analysis has the property that observations within enclosures are correlated over time, which is appropriate for this type of experiment because population sizes on different sampling dates are not independent. The analysis was performed using the Statistical Analysis System (SAS, 1982). Tukey’s honestly significant difference (HSD) test was used to make specific a posteriori comparisons between treatments. The models used in the analysis of the experiments were:

where CI= fixed main effect due to mysid treatment, fi = fixed main effect due to enclosure size treatment, p = fixed main effect due to sample date, and 7~= random container effect nested within treatments. Note that in 1980 only two levels of mysid predation were used in the analysis, absence versus presence of high densities (i.e. differences in initial numbers and survival in the large and small enclosures were ignored). Also, in the small enclosures in 1980, the control and low mysid density containers were both considered as controls. Copepod abundances were log transformed before analysis because analysis of residuals indicated that this transformation made the variances most homogeneous and because copepod growth rates were expected to be appro~mately exponential in the early stages of population growth. The analyses were also performed using copepod relative abundances (species numbers expressed as a percentage of total copepod

TEMPERATURE-PREDATION

INTERACTIONS

71

abundance in each sample) because changes in relative abundance more clearly show selective effects of experimental treatments on species composition than do changes in numbers. Copepod relative abundances were arcsine transformed before analysis to stabilize the variances (Winer, 1971). Because of doubts about the validity of the assumption of homogeneity of the variance-covariance matrices, conservative degrees of freedom discussed in Winer (197 1) were used in the analysis. Because of the conservative nature of the split plot ANOVA (Winer, 1971), and because of the low replication in 1980 (two replicates for three of the four treatment combinations), 0.1 > P > 0.05 was considered marginally significant (significance at this level occurred only for certain treatment by sample date interactions and never for the main treatment effects or interactions between treatments of major interest). For the better replicated 198 1 experiment, P < 0.05 was a criterion for statistical significance. RESULTS

In the estuary, abrupt decreases in water temperature were associated with increases in mysid abundance and changes in copepod species composition. Other potential predators (ctenophores, chaetognaths, fish larvae) were not abundant at this time. Minimal water temperatures in early February 1979 (Fig. 1C) were associated with a decline in the relative abundance of Acartia tonsa and a rise to dominance by Centropuges spp. (Fig. 1A). Quantitative mysid samples were not taken until early March, at which time abundances were very high (Fig. lB), but frequent qualitative samples taken before this indicated that numbers increased in early February. A sharp decrease in water temperature in early March 1980 (Fig. 1F) was associated with an increase in mysid abundance (Fig. lE), a decrease in relative abundance ofkartia ronsa and a rise to dominance by Centropages spp. (Fig. 1D). In 198 1, minimal water temperatures in early January (Fig. 11)were associated with a rise to dominance by Cennopuges (Fig. 1G) and increases in mysid abundance (Fig. lH), although mysids were not as abundant as in previous years. In all three years Centropuges spp. remained dominant until late March, when they rapidly disappeared as water temperatures approached 20 “C, and Acartiu tonsa again became dominant (Fig. 1). In the 1980 enclosure experiments, the small enclosures experienced wider temperature fluctuations, reaching consistently lower temperatures (Fig. 2A,D). The break in the temperature lines in early March was a period following a blizzard during which the enclosures were snow and ice covered. Mysid survival was better in the large enclosures, in which mean density increased to 162. m - 3 by the end of the experiment. In the small enclosures, final mysid densities were 23 - m- 3 in the low density enclosure and 35 . m - 3 in the high density enclosures. Although the final mysid densities were only l/3 lower in the low density experiment, the difference may have been greater for much of the experiment. Quantitative information on mysid abundance could not be obtained during the course of the experiment. Because of the poor survival of mysids in the small low density enclosure, and the small differences between this enclosure and the control

00 10 1

-0 ,’ -4

P

I

15 10 5 k 1979

1980 DATE

Fig. 1. A,D,G, relative abundances (% k SE) ofAcartiu tonsa (0) and Centropuges spp. (0) in North and Newport River estuaries: 1978-1979 (A); 1979-1980 (D); 1980-1981 (G). B,E,H, mysid abundance (no.. m -3 + SE) in Newport River estuary: 1978-1979 (B); 1979-1980 (E); 1980-1981 (H); 0, surface; 0, bottom. C,F,I, surface water temperature (“C): 1978-1979 (C); 1979-1980 (F); 1980-1981 (I).

Feb.

Mar. 1980

Feb.

Mar. 1980

Feb.

Mar. 1981

Fig. 2. A,D,G, water temperature (mean of two daily readings) during enclosure experiments: A, small enclosures 1980 experiment; D, large enclosures 1980 experiment; G, 1981 experiment. B,E,H, chlorophyll a (mean mg. mm3): standard errors overlap completely and are omitted to improve clarity; 0, control enclosures; 0, mysid enclosures; B, small enclosures 1980; E, large enclosures 1980; H, 1981 experiment. C,F,I, total copepodite abundance during enclosure experiments (log transformed no.. me3 f 2 SE): 0, controls; 0, mysid enclosures; C, small enclosures 1980 experiment; F, large enclosures 1980 experiment; I, 1981 experiment.

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INTERACTIONS

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(note the small standard errors of the controls in Fig. 2C), I considered these two enclosures as controls in the analysis. Chlorophyll 4 did not differ significantly between the controls and mysid enclosures (1$(,,q = 0.02, P > 0.9, Fig. 2B,E). However, copepod abundances were significantly lower in the mysid enclosures (Fc1,5j = 18.7, P < 0.01, Fig. 2C,F). There was a marginally significant interaction of enclosure size and sample date on abundance of A. tonsa (F,, ,5j = 4.9, P < 0.1). Tukey’s HSD tests were applied separately on each date, comparing overall mean abundance in the large enclosures with that in the small enclosures. These showed that abundances of A. tonsa were significantly higher in the large enclosures on three of the last four sampling dates (P < 0.01, Fig. 3A,B). There was a significant effect of mysid predation on abundance of A. tonsa (41s~ = 22.1, P < O.Ol), as well as a marginally significant interaction between predation and sampling date (F, ,5j = 4.2, P < 0.1). Tukey’s HSD tests were applied on each date, comparing overall mean abundance in controls with that in the mysid treatments. These showed that the abundances of A. tofu were si~~c~~y lower (P < 0.05) in mysid treatments between 12 February and 20 March, but ab~d~ces recovered at the end of the experiment so that there was no si~~c~t difference on the last sample date (Fig. 3A,B). There was a highly significant effect of enclosure size on Centropages spp. abundance Vi ,5) = 28.3, P < O.Ol), as well as a signiticant interaction between enclosure size and 4 A

E’

Feb.

Mar. 1980

’

Feb.

’

’

Mar. 1980

’

Feb.

Mar. 1981

Fig. 3. Copepod abundances (log transformed no.. IX- 3 f 2 SE) in enclosure experiments: 0, controls; 0, mysid enclosures. A-C, Acartia tonsa: A, small enclosures 1980 experiment; B, large enclosures 1980 experiment; C, 1981 experiment. D-F, Cenwopages spp.: D, small enclosures 1980 experiment; E, large enclosures 1980 experiment; F, 1981 experiment.

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III

sample date (FC1,5j= 7.8, P < 0.05). Tukey’s HSD tests, comparing overall mean abundance in the large enclosures with that in the small enclosures on each sample date, showed that Centropuges was significantly more abundant in the small enclosures on the last five sample dates (P < 0.05 on 26 February, P < 0.01 on the last four dates, Fig. 3D,E). Mysid predation had a significant effect on abundance of Centropuges spp. (E;w = 7.3, P c 0.05, Fig. 3D,E). Although mysid predation appeared to have a greater effect in the small enclosures (Fig. 3D) than in the large (Fig. 3E), there was no significant interaction between treatments. Enclosure size had strong effects on copepod species composition. There were highly significant effects of enclosure size on relative abundances of both Acartiu tonsa (F&, = 78.6, P < 0.001) and Centropuges spp. (FC,,51= 81.2, P < O.OOl), as well as significant enclosure size by sample date interactions (Acurtiu tonsu, Fc,,5j = 14.1, P < 0.05; Centropuges, Fc,,5j = 23.4, P < 0.01). Tukey’s HSD tests, comparing overall mean relative abundance in the large enclosures with that in the small enclosures on each sampling date, showed that these differences occurred by the 6 March sampling date; the relative abundance of A. tonsu was significantly higher (P < 0.01) in the large enclosures than in the small enclosures on all succeeding sampling dates (Fig. 4A,B), while the relative abundance of Centropuges was significantly higher (P < 0.01) in the small enclosures (Fig. 4D,E). There was a significant interaction of mysid predation and enclosure size treatments for the relative abundances of both Acurtiu tonsu (Fc,,5j = 16.1, P = 0.01) and Centropuges w. (F( I .5j = 7.4, P < 0.05). To examine the nature of these interactions, Tukey’s

20

5 12 I9 26 6 13 20 26 Feb. hkw. I980

5 12 I9 26 6 13 20 26 Feb. Mar. 1980

7 ;z,”

I

8

15 22 29 hh.

1981

Fig. 4. Copepod relative abundances in enclosure experiments: mean back transformed relative abundance + 2 SE; crosshatched, copepodite stages CI-CIII; open bars, copepodite stages CIV-CVI; for each sample date, the first column is the controls and the second column is the mysid enclosures. A-C, Acartia tonsa: A, small enclosures 1980 experiment; B, large enclosures 1980 experiment; C, 1981 experiment. D-F, Centropagesspp.: D, small enclosures 1980 experiment; E, large enclosures 1980 experiment; F, 1981 experiment.

TEMPERATURE-PREDATION

INTERACTIONS

15

HSD tests were carried out separately in the large and small enclosures, comparing mean relative abundances in the controls and mysid treatments on each sampling date. In the large enclosures, Tukey’s HSD tests showed that the relative abundance of Acartiu ton~a was significantly reduced (P < 0.05) by mysid predation on the last five sampling dates (Fig. 4B), while the relative abundance of Centropuges was significantly higher (P < 0.01) in the mysid treatment on the last two sampling dates (Fig. 4E). However, in the small enclosures, there were no significant differences until the last two sampling dates, when the relative abundance ofAcurtiu tonsu became significantly higher (P < 0.01) in the mysid treatment (Fig. 4A), while the relative abundance of Centropuges was significantly lower (P < 0.05) in the mysid treatment (Fig. 4D). These differences in the small enclosures were due to strong recruitment of juvenile Acurtiu tonsu that occurred only in the mysid treatment (Fig. 4A). Water temperatures were not as low during the 1981 experiments as in the previous year (Fig. 2G). Mysid recruitment was much better than in the previous year. Mean final mysid density was 1442 * m - 3 and final numbers ofthe more predaceous adults (Fulton, 1982~) were 153. rne3. Chlorophyll u did not differ significantly between treatments (Lq = 4.55, P = 0.1, Fig. 2H), but copepod numbers were significantly reduced in the mysid enclosures (Fc,,4j = 24.4, P < 0.01, Fig. 21). Centropuges spp. dominated the copepod community at the beginning and remained heavily dominant throughout the experiment, reaching higher densities than in 1980 (Figs. 3F,4F). Numbers of Centropages were significantly lower in the mysid enclosures (Fc1,4j= 46.0, P < 0.01, Fig. 3F). Abundances of Acurtiu tonsu were not significantly a.tTected by mysid predation (Fig. 3C). As in the small enclosures in the previous year, there were no effects of mysid predation on species composition (Fig. 4C,F). Unlike the previous year, A. tonsu did not recruit into the enclosures near the end of the experiment (Fig. 4C). DISCUSSION

The field data and enclosure experiments show that the abrupt transitions from an A. tonsu to a Centropages spp. dominated assemblage in the Newport and North River estuaries, shown schematically in Fig. 5, were due to an interaction of physical and biological factors. I interpret the significant effect of enclosure size on copepod species composition in the 1980 experiment as being due to differences in water temperature. The divergence between the large and small enclosures occurred on 6 March, the fast sampling date following the sharp decrease in water temperatures (Fig. 2A,D). During this period, the abundance and relative abundance of Acurtiu tonsu sharply declined in the small enclosures, which experienced lower water temperatures (Figs. 3A,4A), while Centropages spp. heavily recruited and became dominant (Fig. 4D). This was the same time that Centropuges became dominant in the estuary (Fig. 1D). However, in the warmer large enclosures, Centropuges did not heavily recruit and Acartiu tonsu maintained its dominance (Fig. 4B,E). These effects are consistent with available information on

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ROLLAND S. FULTON III

reproduction and distribution of these species. Reproduction of A. tonsa ceases below water temperatures of =lO”C (Heinle, 1966; Zillioux & Gonzalez, 1972; Lee & McAlice, 1979). While less is known of the breeding biology of Centropages hamatus, it has been characterized as a winter species (Fish, 1925; Wilson, 1932). Water temperature also influences the transition to a Centropuges spp. dominated community through its effects on mysid abundance and the significant interaction between temperature and mysid predation. Low water temperatures are associated with high numbers of mysids (Fig. 5). The abrupt increases in mysid abundance during

High

LOW

WATER TEMPERATURE

Fig. 5. Schematic representation of predator importance and copepod relative abundances as a function of water temperature.

periods of sharp decreases in water temperature (Fig. 1) were largely due to migration. Neomysis americana has been found year-round in the low salinity upper reaches of the estuary but appeared in the lower estuary only in mid-winter (Fig. 1; Williams, 1972). N. americana was actively reproducing during the winter, but growth rates are higher at warmer temperatures (Pezzack & Corey, 1979). A4ysidopsi.sbigelowi apparently does not reproduce below 11 “C (Hopkins, 1965) and populations were dominated almost entirely by adults. In the enclosure experiments, mysid recruitment was higher in 1981, when water temperatures were warmer. Low mortality from fish predation probably also contributes to the high winter mysid abundance. Mysids are common prey of a number of fish (Mauchline, 1980), but fish abundance is very low in the estuaries in mid-winter (Tagatz & Dudley, 1961; Adams, 1976). So although mysid production is not especially high in mid-winter, migration to the lower estuaries during periods of low water temperature and low mortality result in sharp peaks in mysid abundance.

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IDEATIONS

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The significant interaction between enclosure size and mysid predation treatments on copepod species composition (Fig. 4) indicates that the effects of mysid predation on community structure depended on the composition of the copepod community. In all cases mysid predation significantly reduced copepod densities (Figs. 2,3). In the large enclosures in 1980, Acartiu tonsa, the preferred prey of the mysids (Fulton, 1982c), dominated and mysid predation significantly reduced the relative abundance ofA. tonsa and increased the relative abundance of Centr0page.r spp. (Fig. 4). The relative abundances of several other minor species, notably ~up~irel~usp., also increased in the large mysid enclosures, resulting in an increase in species diversity (Fulton, 1982a). However, in the small enclosures in 1980, and also in 1981, the nonpreferred Centropages (F&on, 1982~) dominated and there was no effect of mysids on species composition. Therefore, mysid predation probably influences copepod species composition only during the transition from an Acurtiu tonsu to a Centropages dominated community. After Centropages becomes dominant, mysid predation should nonselectively reduce copepod numbers. The increased diversity due to mysid predation when Acartia tonsa was dominant agrees with the results of other studies of the effects of selective predation on the dominant prey species (Paine, 1971; Lubchenco, 1978). However, the lack of an effect of mysid predation on species composition when Centropuges dominated conflicts with earlier studies that found predation enhanced dominance and reduced diversity when nonpreferred prey were competitively dominant (Lubchenco, 1978). There are three possible reasons for the absence of an effect of mysid predation on species composition when Centropuges was dominant. First, prey preferences may have changed, so the mysids preyed more heavily on Centropuges as it increased in abundance. There is some evidence for frequency dependent predation in the freshwater mysid, ~ysis relicta {Cooper & Goldman, 1980; Folt etul., 1982). Secondly, while adult Cen~ropages are nonpreferred prey, this may not be the case for juveniles, which are similar in size to Acartiu tonsu. The Ceniropages populations in the large enclosures were dominated by adults, but reproduction was better in the small enclosures and they were dominated by juveniles (Fig. 4). Van Valen (1974) concluded that nonselective predation would have no effect on prey species composition. However, if prey growth rates differ then unselective predation may favor species with the highest growth rates (May, 1977). Finally, greater predation by Centropuges on the nauplii of Acurtia tonsu in the controls may have compensated for the absence of mortality of A. tonsa from mysid predation (see below). Even at the very high numbers attained in the 1981 experiments, mysids did not eliminate any copepod species. These densities clearly could not be supported by a diet of copepods alone. Gut contents of mysids collected at the end of the experiment indicated that most were feeding on detritus; copepod remains were found only in adult mysids. The amount of overlap in vertical distribution of copepods and mysids may have been less in the enclosures than in the estuary. Both copepods and mysids aggregate close to the bottom in the estuary during the day (Herman, 1963; F&ton,

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in press); however, in the enclosures the copepods aggregated at the upper sunlit edges while mysids remained in the shaded portion at the bottom during the day. Nevertheless, the mysids appear not to have the capability of eliminating preferred prey species as is suspected for freshwater mysids (Morgan etal., 1978; Murtaugh, 1981; Rieman & Falter, 1981). Several factors probably contribute to the lesser effect of these estuarine mysids. Copepods are less susceptible to mysid predation than cladocerans, the group most heavily affected by mysid predation in lakes (Cooper & Goldman, 1980; Murtaugh, 1981). Alternate food sources, including suspended detritus and large diatoms, are available in the estuary. Also producti~ty of prey species is high when temperatures are suitable, and mysids are abundant for only a short period. Once Centropages spp. became established in the estuary, their predation on copepod nauplii (PatfenhOfer & Knowles, 1980) probably limited recruitment of other species. In 1980, the inhibition of recruitment of Acartia tonsa in the small control enclosures (Fig. 4A) was probably due to predation from Centropages. Centropuges stages CIV-CVI were much more abundant in the controls (on 20 March 15 200 . m - 3 in the controls as compared to 2300 - m - 3 in the mysid enclosures). Nauplii densities on this date were close to 20 * I- r. At that density, Paffenhbfer & Knowles (1980) report that adult females of Centropugesfircatw ate 2-5 nauplii * day- ‘. The water temperature in the enclosure experiment was lower than that used by Paffenhofer & Knowles, and not all the Centropuges CIV-CVI were adult females. Assuming as a minimal estimate, a daily predation rate of one nauplius * Centropuges CIV-CVI - ‘, then on 20 March Centropages could consume an estimated 76% of the nauplii standing crop * day- ’ in the controls, but only 11y0 in the mysid enclosures. Thus, by reducing Cen~opages abundance, mysids could have the somewhat paradoxical effect of enhancing recruitment of their preferred prey species. Centropages spp. were never as numerous in the estuary as in the experiments. The highest observed density of copepodite stages CIV-CVI in the estuary was 2920 * m - 3 on 15 February 1981. Nauplii densities on this date were 20.7 *l- I. Assuming again a daily predation rate of one nauplius . Centropages CIV-CVI - ‘, an estimated 15% of the naupliar strung crop could be consumed daily by Centropages on this date. Once Centropages had become established in the estuary, their predation on the nauplii of other species could contribute to their persistent dominance, particularly while low water temperatures inhibit copepod recruitment. The spring transition back to an Acartia tonsa dominated community (Figs. 1, 5), also appears to be due to an interaction of physical and biological factors. The rapid decline of Centropages spp. may be partly due to inhibition of reproduction at warmer temperatures. The thermal tolerance limits of Centropages ha~at~ are not known, but juveniles were still being produced at the end of the 1980 experiments at water temperat~es of up to 15 oC (Fig. 4). Raymont & Miller (1962) found that C. hamatus failed to recruit in enclosures at temperatures of near 20 “C. Another factor probably contributing to the decline of Centropages is predation by postlarval fish, which enter the estuary in large numbers as water temperature begins to rise in mid-March (Thayer et al., 1974; Fulton,

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1982b). The most abundant fish, Leiostomus xanthunts, prefers the larger, more heavily pigmented Centropages over Acartiu tonsa (Kjelson et al., 1975; Fulton, 1982b). Fish predation may also contribute to the spring decrease in mysid numbers (Figs. 1,5). Heavy recruitment of A. tmsa at the warmer higher temperatures in spring (Heinle, 1966; Zillioux & Gonzalez, 1972; Lee & M&lice, 1979), combined with reduced mortality from Centropages spp. predation, results in its rise to dominance. Mysids appear to be ineffective in inhibiting spring recruitment of Acartiu tonsu (Fig. 3A,B). Two features of mysid predation would tend to minimize their effects on the rapid spring increase ofA. tonsu. Mysids rarely feed on copepod nauplii (Cooper & Goldman, 1980; Siegfried & Kopache, 1980; Murtaugh, 1981), and so would have little effect on the recruitment of juveniles. Also the Type II functional response of these mysids (Fulton, 1982~) results in a lower predation intensity at high prey densities; so by rapidly recruiting A. tonsa may escape predatory control (Holling, 1965). Low water temperatures and predation by mysids and probably by Centropuges spp. had significant effects on copepod community structure, and their combined effects might be expected to eventually eliminate Acartiu tonsu. However, perturbations in the physical environment prevented its exclusion even in the relatively small, closed system of the enclosures. The estuary is both an open system and is large enough to contain considerable spatial heterogeneity. These factors would greatly prolong the time required for exclusion of prey species or inferior competitors (Caswell, 1978; Crowley, 1981). It is likely that equilibrium is never reached in the estuary, due to frequent perturbations in physical factors and associated changes in predator abundance and copepod reproductive rates. This may be.generally true in planktonic communities, which, with the possible exception of central oceanic gyres (Hayward & McGowan, 1979; McGowan & Walker, 1979), are characterized by considerable spatial and temporal heterogeneity. Co~unity structure in planktonic communities may best be explained by nonequilib~~, disturbance models (Hutchinson, 1961; Caswell, 1978; Connell, 1978; Huston, 1979). ACKNOWLEDGEMENTS

This research was completed in partial fulfillment of the requirements for the Ph.D. degree from Duke University. I thank R. Barber, W. Kirby-Smith, D. Livingstone, J. Lundberg, K. Russell, F. Schwartz, R. Searles, J. Sutherland, P. Thomson, and H. Wilbur. During the study period I was supported by a National Science Foundation graduate fellowship and a Duke University Marine Laboratory teaching assistantship. Research support was provided by a Sigma Xi Research Support Grant and Duke University. Victoria University of Wellington provided computer time and support during manuscript preparation.

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ROLLAND S. FULTON III REFERENCES

ADAMS, S. M., 1976. The ecology of eelgrass, Zosteru marina (L.) fish communities. I. Structural analysis. J. Exp. Mar. Biol. Ecol., Vol. 22, pp. 269-291. BROOKS,J. L. L S. I. DODSON, 1965. Predation, body size, and composition of plankton. Science, Vol. 150, pp. 28-36. CASWELL, H., 1978. Predator-mediated coexistence: a nonequilibrium model. Am. Nut., Vol. 112, pp. 127-154. CONNELL,J.H., 1978. Diversity in tropical rain forests and coral reefs. Science, Vol. 199, pp. 1302-1310. COOPER,S. D. & C. R. GOLDMAN,1980. Opossum shrimp (Mysis relicta) predation on zooplankton. Can. J. Fish. Aquat. Sci., Vol. 37, pp. 909-919. CROWLEY, P.H., 1981. Dispersal and stability of predator-prey interactions. Am. Nat., Vol. 118, pp. 673-701. DODSON, S. I., 1974. Zooplankton competition and predation: an experimental test of the size efficiency hypothesis. Ecology, Vol. 55, pp. 605-613. DODSON, S.I.,1979. Body size patterns in arctic and temperate zooplankton. Limnol. Oceanogr., Vol. 24, pp. 940-949. FISH, C.J., 1925. Seasonal distribution of the plankton of the Woods Hole region. Bull. U.S. Bur. Fish., Vol. 41, pp. 91-179. FLEMINGER,A., 1975. Geographical distribution and morphological divergence in American coastal-zone planktonic copepods of the genus Labidocera. In, Estuarirze research. Vol. 1. Chemistry, biology, and the es&urine system, edited by L. E. Cronin, Academic Press, New York, pp. 392-419. FOLT, C. L., J. T. RYBOCK& C. R. GOLDMAN,1982. The effect of prey composition and abundance on the predation rate and selectivity of Mysir relicta. Hydrobiologia, Vol. 93, pp. 133-143. FULTON,R. S. III, 1982a. Preliminary results of an experimental study of the effects of mysid predation on estuarine zooplankton community structure. Hydrobiologiu, Vol. 93, pp. 79-84. FULTON, R. S. III, 1982b. Predation and the organization of an estuarine copepod community. Ph.D. dissertation, Duke University, Durham, N.C., 421 pp. FULTON,R.S. III, 1982~. Predatory feeding of two marine mysids. Mar. Biol., Vol. 72, pp. 183-191. FULTON, R. S. HI, in press. Distribution and community structure of estuarine copepods. Estuaries. HAYWARD,T.J. & J. A.MCGOWAN, 1979. Pattern and structure in an oceanic zooplankton community. Am. Zool., Vol. 19, pp. 1045-1055. HEINLE, D.R., 1966. Production of a calanoid copepod, Acartiu tonsa in the Patuxent River estuary. Chesapeake Sci., Vol. 7, pp. 59-74. HEINLE, D.R. & D.A. FLEMER, 1975. Carbon requirements of a population of the estuarine copepod Ewytemora afinis. Mar. Biol., Vol. 31, pp. 235-247. HERMAN, S.S., 1963. Vertical migration of the opossum shrimp, Neomysis americana Smith. Limnol. Oceanogr., Vol. 8, pp. 228-238. HOLLING, C. S., 1965. The functional response of predators to prey density and its role in mimicry and population regulation. Mem. Ent. Sot. Can., Vol. 45, pp. 3-60. HOPKINS, T.L., 1965. Mysid shrimp abundance in surface waters of Indian River Inlet, Delaware. Chesapeake Sci., Vol. 6, pp. 86-91. HUSTON, M., 1979. A general hypothesis of species diversity. Am. Nut., Vol. 113, pp. 81-101. HUTCHINSON,G.E., 1961. The paradox of the plankton. Am. Nat., Vol. 95, pp. 137-146. JEFFRIES, H. P., 1967. Saturation of estuarine zooplankton by congeneric associates. In, Estuaries, edited by G.H. Lauff, Am. Association for Advancement of Science Publ. No. 83, Washington, D.C., pp. 500-508. KJELSON, M. A. & G. N. JOHNSON,1976. Further observations of the feeding ecology of postlarval pin&h, Lagodon rhomboides, and spot, Leiostomus xanthurus. Fish. Bull. NOAA, Vol. 74, pp. 423-432. KJELSON, M. A., D. S. PETERS, G. W. THAYER& G. N. JOHNSON, 1975. The general feeding ecology of postlarval fishes in the Newport River estuary. Fish. Bull. NOAA, Vol. 73, pp. 137-144. LEE, W.Y. & B. J. MCALICE, 1979. Seasonal succession and breeding cycles of three species of Acartia (Copepoda: Calanoida) in a Maine estuary. Estuaries, Vol. 2, pp. 228-235. LONSDALE,D.J., 1981. Regulatory role of physical factors and predation for two Chesapeake Bay copepod species. Mar. Ecol. Prog. Ser., Vol. 5, pp. 341-351.

TEMPERATURE-PREDATION

INTERACTIONS

81

LUBCHENCO,J., 1978. Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am. Nut., Vol. 112, pp. 23-39. LYNCH,M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnol. Oceanagr., Vol. 24, pp. 253-272. MAUCHLINE,J., 1980. The biology of mysids. A&. Mar. Biol., Vol. 18, pp. 3-369. MAY, R.M., 1977. Predators that switch. Nature (London), Vol. 269, pp. 103-104. MCGOWAN,J. A. & P. A. WALKER,1979. Structure in the copepod community of the North Pacific central gyre. Ecol. Monogr., Vol. 49, pp. 195-226. MORGAN, M.D., S.T. THRELK~LD& C.R. GOLDMAN, 1978. Impact of the introduction of kokanee (Oncorhynchus nerka) and opossum shrimp (Mysis relicta) on a subalpine lake. J. Fish. Res. Bd. Can., Vol. 35, pp. 1572-1579. MURTAUGH,P. A., 1981. Selective predation by Neomysis mercedis in Lake Washington. Limnol. Oceanogr., Vol. 26, pp. 445-453. NULL, W. E., 1978. Experimental studies on factors limiting colonization by Daphniapulex Leydig of coastal montane lakes in British Columbia. Can. J. Zooi., Vol. 56, pp. 2498-250’7. NEILL,W.E., 1981. Impact of Chaoborus predation upon the structure and dynamics of a crustacean zooplankton community. Oecologiu (Berlin), Vol. 48, pp. 164-177. PAFFENH~FER,G.-A. & S. C. KNOWLES,1980. Omnivorousness in marine planktonic copep0ds.J. Plankton Res., Vol. 2, pp. 355-365. PAINE, R. T., 1971. A short-term experimental investigation ofresource partitioning in a New Zealand rocky intertidal habitat. Ecology, Vol. 52, pp. 1096-l 106. PEZZACK, D.S. & S. COREY, 1979. The life history and distribution of Neomysis americana (Smith) (Crustacea, Mysidacea) in Passamaquoddy Bay. Can. J. Zool., Vol. 57, pp. 785-793. RAYMONT,J. E. G. & R. S. MILLER,1962. Production of marine zooplankton with fertilization in an enclosed body of sea water. Int. Rev. Gesamten Hydrobiol. Vol. 47, pp. 169-209. RICHERSON. P., R. ARMSTRONG& C.R. GOLDMAN, 1970. Contemporaneous disequilibrium, a new hypothesis toexplain the“paradox ofthe plankton”. Proc. Nat. Acad. Sci. U.S.A., Vol. 67, pp. 1710-1714. RIEMAN,B. E. & C. M. FALTER,1981. Effects of the establishment ofMy& relicta on the macrozooplankton of a large lake. Trans. Am. Fish. Sot., Vol. 110, pp. 613-620. SAS INSTITUTE,INC., 1982. SAS user’sguide:statistics, 1982 edition. SAS Institute, Inc., Cary, NC, 584 pp. SIEGFRIED,CA. & M. E. KOPACHE,1980. Feeding ofNeomysis mercedis (Holmes). Biol. Bull. (Woods Hole, Mas,s.), Vol. 159, pp. 193-205. TAGATZ,M. E. & D. L. DUDLEY, 1961. Seasonal occurrence of marine fishes in four shore habitats near Beaufort, North Carolina, 1956-60. U.S. Fish ~iidl. Serv., Spec. Sci. Rep. Fish., No. 390, 19 pp. THAYER,G. W., 1971. Phytoplankton production and the dist~bution of nutrients in a shallow ~stratified estuarine system near Beaufort, N.C. Chesapeake Sei., Vol. 12, pp. 240-253. THAYER,G. W., D.E. Hess, M. A. KJELSON,W.F. HETTLER,JR. & M. W. LACROIX,1974. Biomass of zooplankton in the Newport River estuary and the influence of postlarval fishes. Chesapeake Sci., Vol. 15, pp. 9- 16. VAN VALEN, L., 1974. Predation and species diversity. J. Theoret. B&Z., Vol. 44, pp. 19-21. WIENS, J. A., 1977. On competition and variable environments. Am. Sci., Vol. 65, pp. 590-597. WILLIAMS,A. B., 1972. A ten-year study of meroplankton in North Carolina estuaries: mysid shrimps. Chesapeake Sci., Vol. 13, pp. 254-262. WILSON,C. B., 1932. The copepod crustaceans of Chesapeake Bay. Proc. U.S. Nat. A&s., Vol. 80, pp. l-54. WINER, B. J., 1971. Statisticalprinciples in experimentaldesign. 2nd edition. McGraw-Hill, New York, 907 pp. ZARET, T.M., 1980. Predation andfreshwater communities. Yale University Press, New Haven, 187 pp. ZILLIOUX,E. J. & J.G. GONZALEZ,1972. Egg dormancy in a neritic calanoid copepod and its implications to overwintering in boreal waters. In, F$th European Marine Siologv Symposium, edited by B. Battaglia, Piccin Editore, Padua, pp. 217-230.