Effects of low oxygen waters on Chesapeake Bay zooplankton
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1 Limnol. Oceanogr., 38(8), 1993, , by the American Society of Limnology and Oceanography, Inc. Effects of low oxygen waters on Chesapeake Bay zooplankton Michael R. Roman and Anne L. Gauzens Horn Point Environmental Laboratory, University of Maryland System, Cambridge W. Kirk Rhinehart Department of Oceanography and Coastal Science, Louisiana State University, Baton Rouge Jacques R. White Horn Point Environmental Laboratory Abstract The bottom waters of the mesohaline portion of Chesapeake Bay become depleted in oxygen in summer. We found that copepods and nauplii were in low abundance or absent from bottom waters when oxygen concentrations were < 1 mg 0, litcr- I. In contrast, when oxygen concentrations were higher in bottom waters in spring or summer due to episodic mixing events, the highest copepod abundances were often found in bottom waters. Laboratory experiments confirmed that oxygen concentrations < 1 mg 0, liter- 1 resulted in reduced survival of the copepods Acartia tonsa and Oithona colcarva and inhibited the hatching of A. tonsa eggs. The decrease in Chesapeake Bay copepods in May-June parallels the decline of oxygen in bottom waters. Our field and laboratory data suggest that this dcclinc in copepods could result from reduced recruitment as a consequence of egg mortality in the low-oxygen bottom waters. In summer this source of mortality would be reduced because warmer water temperatures would allow the eggs to hatch in the upper water column above the low-oxygen bottom waters. The bottom waters of estuaries and continental shelves may become anoxic (no detectable 0,) or hypoxic (here defined as ~2 mg O2 liter- ) during part of the year (e.g. May 1973; Falkowski et al. 1980; Leming and Stuntz 1984; Officer et al. 1984). In Chesapeake Bay, hypoxia and anoxia generally occur in the mesohaline portion (5-l 8%0) in summer. Enhanced freshwater flow in spring increases the density stratification and isolates bottom waters from oxygen inputs. As a result, the degradation of organic matter depletes dissolved oxygen in the bottom waters (Kemp et al. 1992). Interannual variations in the severity and duration of oxygen depletion occur as a result of changes in freshwater and organic inputs (Malone et al. 1988; Kemp et al. 1992). There is evidence to suggest that because of greater nutrient inputs and organic production, depletion of oxygen in Chesapeake Bay waters has in- Acknowledgments This work was completed as part of a larger study examining the effects of anoxia on living resources in Chcsapeake Bay. We thank T. Malone for supplying the oxygen data. Shipboard and laboratory assistance was supplied by R. Allen, K. Ashton, J. Jensen, C. Murray, and K. Parker. This research was supported by NOAA/Sea Grant. CEES contribution creased in both extent and duration (Officer et al. 1984; Cooper and Brush 1991). Eutrophication of estuaries and continental shelf waters may be increasing throughout the world (Walsh et al ; Nixon et al. 1986). As a result, oxygen depletion in coastal waters may increase in the future. The effect of low-oxygen waters on zooplankton has been studied primarily in oceanic waters. Oxygen minimum zones are found throughout the world ocean (Kamykowski and Zentra 1990). Zooplankton abundances are frequently reduced in these oxygen minimum layers (Sewell and Fage 1948; Vinogradov and Voronina 196 1; Longhurst 1967). Oxygen minimum zones appear to be inhabited by particular zooplankton species (Judkins 1980) as well as diapause stages of zooplankton (Alldredge et al. 1984) that can tolerate low oxygen. Despite the prevalence of low-oxygen waters in continental shelf and estuarine waters, few studies have examined the effect of anoxia and hypoxia on zooplankton distributions in those waters. Olson (1987), in a 5-yr study on zooplankton abundance in Chesapeake Bay, found that zooplankton abundances were often positively correlated with dissolved oxygen concentrations.
2 1604 Roman et al. As part of a broader study on the factors regulating anoxia in Chesapeake Bay, we examined zooplankton distribution, grazing (White and Roman 19923), and egg production (White and Roman 1992a). Presented here are data on the distribution of zooplankton in the mesohaline portion of the bay in relation to oxygen concentration. We use these data in conjunction with laboratory results on the effect of oxygen concentration on egg hatching and copepod survival to infer the impact of low-oxygen water on zooplankton dynamics in Chesapeake Bay. Methods Oxygen, temperature, salinity, chlorophyll, and zooplankton were measured at five stations on a transect across the mesohaline portion of Chesapeake Bay ( N, O W; Sta. 5-Sta. 1) in 1986 and Bottom depths at each station were: Sta. 1, 5 m; Sta. 2, 10 m; Sta. 3, 12 m; Sta. 4, 18 m; Sta. 5, 5 m. Water samples were collected with a submersible well pump (20-40 liters min-l) with a 2.5-cm-diameter hose. Temperature, salinity, dissolved oxygen, and in vivo chlorophyll fluorescence were measured at l-m intervals with a Sea-Bird model 3-O 1 /S temperature sensor, Sea-Bird model 4-O l/o conductivity sensor, YSI model 57 dissolved oxygen meter, and Turner Designs Fluorometer (Malone et al. 1988). Zooplankton were collected by the same submersible well pump and hose system. The pump was lowered to 1 m above the bottom and raised at a rate of 1 m min- I. Water was pumped through 64-pm-mesh nets in containers on deck from integrated depths below, through, and above the pycnocline at the deep stations in 1987 but only from the surfacepycnocline and from below the pycnocline in The shallow stations along the eastern and western flanks of the bay were usually well mixed, so the entire water column was integrated in the pump collections. We sampled zooplankton on the transect stations between 0900 and 1500 hours. We also conducted a diel study at the midchannel station (No. 4): water and plankton were sampled every 4 h for 30 h. Zooplankton samples were preserved in 5% Formalin, counted, and measured in the laboratory with a microscope, digitizing pad, and computer image analysis system. Pump avoidance by adult and late stage co- pepodites was estimated by comparing the catch of a 0.5-m-diameter, 200~pm-mesh net with simultaneous pump-collected samples in surface waters. No significant differences were found in the abundance of adult and CV Acartia tonsa collected with the two types of gear (paired-sample t-test, P < 0.05, n = 8). We directly assessed the effect of low-oxygen waters on copepods by conducting laboratory experiments to measure the survival of cope- pods and their eggs in low-oxygen waters. The copepods A. tonsa and Oithona colcarva, dominant in Chesapeake Bay, were isolated from net tows in summer and kept at 20 C in 2Oo/oo filtered water with the alga Thalassiosira weiss- jlogii. Water with different oxygen concentrations was prepared by bubbling filtered 20%0 seawater with N2 and siphoning the seawater into 300-ml (copepods) or 60-ml (eggs) glassstoppered, opaque bottles. Adult A. tonsa or 0. colcarva were isolated from cultures, rinsed in filtered seawater, and placed into the incubation bottles (10 copepods per bottle, three to five bottles per treatment). Eggs of A. tonsa were collected by isolating females, incubating the animals in normoxic 2O C, 20%~ filtered water containing T. weissflogii, and collecting the eggs produced over 12 h. The eggs were rinsed with filtered seawater and placed into the incubation bottles (10 eggs per bottle, five bottles per treatment). The bottles were submerged in a water bath (20 C) to reduce the possibility of oxygen input to the seawater. We checked initial oxygen concentrations (YSI model 57 or Orbisphere oxygen meter) as well as final concentrations in each bottle. If oxygen concentrations increased during the incubation, the sample was discarded. At the end of the experiment, the contents of the bottles were sieved through 20-pm mesh, the eggs, nauplii, and copepods rinsed onto a Petri dish, and the samples counted. Copepod survivorship experiments were conducted by comparing the proportion of copepods surviving to 24 h at various oxygen concentrations. The number of nauplii that hatched at different oxygen concentrations was compared over 30-h incubations. Normoxic controls were conducted for both eggs and copepods. We also tested the ability of copepod eggs to hatch after exposure to low oxygen. A. tonsa eggs (10 eggs per bottle, five bottles per treatment) were incubated in 1 mg liter- 02, 20% seawater at 20 C under constant darkness
3 Low oxygen efects on zooplankton 1605 for varying periods of time (6, 12, 18, 24, 48, 72 h). At the end of the incubation, the caps were taken off the bottles and the water was gently bubbled for 4 min to increase oxygen concentrations to normoxic conditions. The number of nauplii that hatched 30 h after reoxygenation was then compared to the original exposure time in low-oxygen water. Results and discussion Oxygen and zooplankton distributions - Representative examples from May and August illustrate the relationship between the cross-bay distribution of oxygen and copepods (Figs. l-3). During May, the amount of oxygen in the bottom waters decreases as a result of increased stratification and enhanced decomposition of organic matter (Malone et al. 1988; Kemp et al. 1992). Note that bottom-water oxygen decreased between our 1 May and 11 May 1987 transects (Fig. 1). On both May dates, copepod abundances were relatively high near the bottom at the two deep stations. During May, the vertical distribution of copepods in the mesohaline portion of the bay does not exhibit diel changes as a result of vertical migration (Roman et al. 1988). In May, chlorophyll concentrations often exceed 20 mg m-3 in bottom waters (Malone et al. 1988). These high concentrations of bottom-water chlorophyll are often associated with maximum water-column measurements of copepod abundance, egg production (White and Roman 1992a), and ingestion (White and Roman 1991). Oxygen concentrations in the bottom waters of the mesohaline portion of the bay are usually at the yearly minimum in August (Malone et al. 1988; Kemp et al. 1992). In August 1987, about half of the 18-m water column contained < 1 mg O2 liter- * (Fig. 2). Below the pycnocline, oxygen values ranged from 1.4 to 2.7% saturation. There were few if any copepods in the low-oxygen water of the deep station (Fig. 2). At the station to the west of the deep channel, there were higher oxygen concentrations in the bottom water as well as higher abundances of copepods (Fig. 2). Both annual and short-term (10 d) distributions of oxygen and copepods change in the bay. In 1986, oxygen depletion in the bottom waters was not as severe as it was in As a likely consequence, copepods were present in the bottom waters (Fig. 3). Copepods (pre- dominantly A. tonsa) in the mesohaline portion of the bay in August usually reside in the bottom waters during the day and migrate into surface waters at night (Roman et al. 1988). This behavior would serve to decrease copepod predation by the dominant visual preda- tor, the bay anchovy, Anchoa mitchilli. However, when the oxygen content of the bottom water was < 1 mg liter - on 20 August 1987, there were few or no copepods in the bottom water at the midbay deep station and no apparent diel migration (Fig. 4). On shorter time scales, variation in bottomwater oxygen in the bay can result from mixing and advection. Southerly winds induce a crossbay seiche which can result in pycnocline tilts to the west and intrusion of low-oxygen water from midbay onto the western flanks of the bay (Malone et al. 1986; Breitburg 1990). Between 17 and 27 August 1986, the mixed layer deepened from -1Omto 14matthemidbay deep station, apparently in response to strong (>15 m s-l, measured at Patuxent NAS) northerly winds (Fig. 5). This wind event resulted in increases in both the amount of oxygen and number of copepods in the bottom water (Fig. 5) as a result of mixing, advection, or both. In summary, our field data suggest that low concentrations of oxygen (< 1 mg liter - I) can result in reduced copepod abundances in the bottom waters of the bay. When oxygen values increase, copepod densities are greatest near the bottom. In August, the normal behavior for copepods is to reside near the bottom during the day and to migrate into surface waters at night. Anoxia in bottom waters disrupts this behavior. When bottom waters are anoxic, copepod abundances are highest in the pycnocline throughout the day and night. Laboratory studies on the efect of low oxygen on copepod survival - Survivorship experiments conducted in the laboratory at various oxygen concentrations corroborated field results. For both A. tonsa and 0. colcarva (Fig, 6), the number of copepods surviving to 24 h was significantly lower in water containing < 2 mg O2 liter-. Survival at the lowest concen- trations of oxygen (0.6 and 0.1 mg 0, liter-l for 0. colcarva and A. tonsa) suggests that copepods have limited ability to survive the lowoxygen conditions that persist in bottom waters of the deep channel of the bay in summer. Respiration measurements with Oithona
4 1606 Roman et al. 1 May May 1987 A Fig. 1. Cross-bay distributions of oxygen and copepod nauplii, Acartia tonsa, and Oithona colcarva in the mesohaline Chesapeake Bay for 1 and 11 May 1987.
5 6 August 1987 Low oxygen efects on zooplankton August I / I 0 Fig. 2. As Fig. 1, but for 6 and 20 August 1987.
6 1608 Roman et al. 11 August August 1986 Fig. 3. As Fig. 1, but for 11 and 27 August 1986.
7 Low oxygen efsects on zooplankton 20) n Surface 1 r 0 32 Time (h) Time (h) Fig. 4. Changes over time in the vertical distribution of oxygen and copepod nauplii, Acartia tonsa, and Oithona colcarva at the midchannel station (No. 4) on August (Lampitt and Gamble 1982) suggest that this cyclopoid copepod has a low metabolism and thus requires less oxygen than Acartia. Our laboratory results suggest that Oithona might be able to survive low-oxygen conditions better than Acartia. We are not aware of similar laboratory studies on the survival of copepods at different oxygen concentrations. However, it has been demonstrated that low oxygen reduces the filtration rate of zooplankton. Kring and O Brien (1976) found that the filtration rate of the freshwater cladoceran, Daphnia pulex, decreased sharply when oxygen concentrations fell below 3 mg liter- I. This reduction in filtration activity may be a response to reduce metabolic rate in low-oxygen conditions. Eflects of low oxygen on copepod eggs-the proportion of A. tonsa eggs hatching in 30 h was affected by oxygen content of the water (Fig. 7). At oxygen concentrations ~2 mg liter-l, hatching was reduced compared to controls. No A. tonsa eggs hatched at oxygen concentrations ~0.5 mg liter-l (Fig. 7). Uye and Fleminger (1976) found that the lower limit of oxygen concentration below which no Acartia eggs developed was mg liter-l. Ambler (1985) found a similar threshold oxygen concentration (0.19 mg liter- ) below which A. tonsa eggs would not hatch. Lutz et al. (1992) reported that no A. tonsa eggs hatched at oxygen concentrations < 0.09 mg liter - 1 and that < 10% of the eggs hatched at oxygen concentrations between 0.09 and 0.13 mg liter-l. This apparent greater hatching success at lower oxygen concentrations reported by Lutz et al. as compared to our study and the studies of Uye and Fleminger and Ambler may be a result of the longer incubation time in the Lutz et al. study (5 d), differences in the measurement precision for oxygen, or different physiological states of the eggs in the various experiments. Through the advection of bottom waters, mixing events, and cross-bay seiches, it is possible that copepod eggs in low-oxygen bottom waters could be reaerated. To test the effect of low-oxygen conditions on subsequent hatch-
8 1610 Roman et al. 0 Sigma-t I I I I I I 14 IOOr A 0 mg DO. liter-l - 8 2o0 17 August &3S I 1 I I I 150 OO 21 4 I 6 8 I 10 J D-0. mg liter- Fig. 6. Survival (% of total) of Acartia tonsa and Oithona colcarva after 24 h in different oxygen concentrations. physiological differences between eggs make absolute comparisons between studies diffi cult. It appears, however, that A. tonsa eggs Zooplankton liter -I [I can survive brief periods of anoxia. Although Fig. 5. Vertical profiles of density, oxygen, and zoo- with increased time on the bottom, sedimenplankton abundance at the midchannel station (No. 4) on tation and predation by benthos may also re- 17, 20, and 27 August sult in reduced hatching and recruitment to the population. ing success in higher oxygen waters, we incu- The input of copepod eggs to low-oxygen bated A. tonsa eggs in water with 1 mg liter- l bottom waters is determined by their sinking oxygen for various periods of time and then rate and development time. Uye (1980) found reaerated the water. Our results suggest that if that eggs of Acartia clausi and Acartia steuri eggs were held in low-oxygen water for > 2 d, sank in 20 C 32%0 seawater at rates of 32 and their hatching success in fully oxygenated wa- 6 1 m d-l. At 2O C, 32Y~ seawater, eggs from ter was reduced (Fig. 7). Uye and Fleminger A. tonsa sank at - 20 m d-l (N. Marcus pers. ( 1976) also found that A. tonsa eggs could sur- comm.). The development time of copepod vive in low-oxygen waters for only 2 d. Lutz eggs is a function of temperature. If we use the et al. (1992) found evidence to suggest that regression determined by Ambler ( 1985) [where some A. tonsa eggs held in water containing D = 9.0 x 103(T + 1.0)-2.05, with D the de- < 0.17 mg oxygen liter- l for 5 d and then reaer- velopment time of A. tonsa eggs in hours, and ated could hatch, although as pointed out pre- T the temperature] we find that, during the viously, differences in egg incubation times, period when the bottom waters have low oxmeasurement techniques for oxygen, and ygen (May through September), minimum es-
9 Low oxygen eflects on zooplankton 1611 timates (based on eggs spawned in surface waters) of egg development times would range from 2 1 to 10 h (at 18 and 27 C, respectively). As the eggs sink through the water, water temperatures decrease and egg hatching time would increase. Thus, it is likely that A. tonsa eggs would sink to low-oxygen bottom waters, especially at the early stages of anoxia when water temperatures are lower. The distribution and abundance of copepod eggs and nauplii reflect the interacting effects of hatching time, anoxia, and predation. In May, the distribution of copepod eggs and nauplii was displaced (Fig. 8). Nauplii abundance was highest in surface waters, whereas abundance in eggs peaked in the thermocline or the bottom water. Our laboratory data suggest that the low concentrations of oxygen on 21 May 1987 (1 mg liter- 1 = 10% saturation) would have inhibited the hatching of copepod eggs. In August, maximum abundances of eggs and nauplii occurred at the same time (Fig. 8), and we did find copepod eggs in the bottom water (0.1 mg 0, liter-l = 1% saturation). Our laboratory data, as well as that of Uye and Fleminger (1976) and Ambler (1985), indicate that the eggs found in the August bottom water would not hatch. Differences in temperature and egg-hatching time may be partially responsible for the vertical distribution patterns of eggs and nauplii as well as for differential mortality of copepod eggs in May-June vs. August. In May, water temperatures would likely result in egg development times long enough (>24 h) that the eggs would sink to, the low-oxygen bottom waters. When the oxygen content ofbottom water falls below 1 mg liter- I, hatching would be reduced. In August, warmer water temperatures would accelerate egg hatching (< 10 h) so that most of the eggs would hatch before they sank to the anoxic bottom waters. The abundance maxima of copepod eggs and nauplii cooccur in August but not in May (Fig. 8). In the mesohaline Chesapeake Bay, the annual minimum of copepod abundance occurs in May-June (Olson 1987). Copepod abundance usually declines over the month of May (Olson 1987; Fig. 9). This decline is enigmatic because phytoplankton biomass is usually near its annual maximum in May (Malone et al. 1988). Both food quantity and food quality in May-June are sufficient to support maximum loor A. 0 D-0. (mg liter-l) B. 1 mg liter- D.O., I 12 I 24 I I 48 I I 72 Time (h) Fig, 7. Hatching (O/of total) of Acartia tonsa eggs (A) after 30 h at different oxygen concentrations and (B) after different exposure times to 1 mg oxygen liter- I and then 30 h at 8 mg oxygen liter-l, means plotted with standard deviations. copepod production (White and Roman 1992a). Since copepods do not appear to be food limited during this period, it is possible that predation may reduce copepod abundances. Inverse correlations between the abundance of the ctenophore, Mnemiopsis Zeidyi, and copepods in the bay have led some investigators to conclude that predation controls the standing stock of copepods (Lonsdale 198 1; Brownlee and Jacobs 1987; Olson 1987). However when grazing rates were combined with estimates of ctenophore abundance, Purcell et al. (1994) found that gelatinous zooplankton predators could not cause the observed decrease in copepod standing stock. Another possible cause for reduced copepod abundances in May-June is low oxygen in bottom waters. The decline in bottom-water oxygen parallels the decrease in copepods at our midbay station (Fig. 9). Although it is tenuous
10 1612 Roman et al. 11 May 1987 od.o. mg lid Eggs liter May 1987 D-0. mg lid Eggs liter -I 25 c E 8 o Nauplii liter-l25 o Acartia lid 5 ONauplii liter 4 25 o Acartia liter 5 0 I I I I I, 6 August August 1987 D.O. mg liter-l liter Eggs 25 0 I / -2o- g 25 Temp., OC 28 I I I Llll, I 2025 Temp., OC 28 Nauplii liter 4 Acartia liter s Fig. 8. Vertical profiles of oxygen, temperature, copepod eggs, nauplii, and Acartia tonsa at the midchannel station (No. 4) on 11 and 21 May and 6 and 20 August 1987.
11 Low oxygen e#ec Its on zooplankton Fig. 9. Changes in water-column copepod abundance and bottom-water oxygen at the midchannel station (No. 4) in May-June to infer a cause-and-effect relationship, it is possible that low-oxygen bottom waters inhibited the hatching of copepod eggs, thus reducing copepod recruitment. The water-column temperatures in May-June would result in longer egg development times, which would allow the eggs to sink into the low-oxygen bottom waters. Our laboratory data suggest that oxygen levels ~2 mg liter- inhibit the hatching of A. tonsa eggs. In combination with grazing by gelatinous zooplankton, invertebrate predators, and fish, anoxic bottom waters likely contribute to the observed reduction in copepod abundance in May-June. In August, warmer water temperatures result in reduced egg development times (< 10 h). Although the depth and level of oxygen depletion in midlate summer is greater than in May-June, the effect on copepod recruitment is likely reduced because the eggs hatch in the upper water column. In Chesapeake Bay, anoxia results from degradation of organic matter in bottom waters. In spring, stratification of the water column combined with high organic flux to the bottom initiates oxygen depletion. In many temperate bays and estuaries the abundance of copepods is near the annual maximum in May-June, presumably the result of high food concentrations (e.g. Conover 1956; Roman 1980; Durbin and Durbin 198 1). However, in Chesapeake Bay, the standing stock of copepods is usually at the yearly minimum during May- June when phytoplankton stocks are maximal. The development of low-oxygen waters may reduce zooplankton recruitment and thus uncouple the production of phytoplankton and copepods. One result of this uncoupling would be a reduction in copepod grazing pressure, thus increasing the amount of phytoplankton that sinks to the bottom where this organic matter would contribute to oxygen depletion. References ALLDREDGE, A. L., AND OTHERS Direct sampling and in situ observation of a persistent copepod aggregation in the mesopclagic zone of the Santa Barbara Basin. Mar. Biol. 80: AMBLER, J. W Seasonal factors affecting egg production and viability of eggs of Acartia tonsa Dana from East Lagoon, Galveston, Texas. Estuarine Coastal Shelf Sci. 20: BREITBURG, D. L Near-shore hypoxia in the Chesapeake Bay: Patterns and relationships among physical factors. Estuarine Coastal Shelf Sci. 30: BROWNLEE, D. C., AND F. JACOBS Mesozooplankton and microzooplankton in the Chesapeake Bay, p In S. K. Majumdar et al. [eds.], Contaminant problems and management of living Chcsapcake Bay resources. Penn. Acad. Sci. CONOVER, R. J Oceanography of Long Island Sound, Biology of Acartia claw and A. tonsa. Bull. Bingham Oceanogr. Collect. 15: COOPER, S. R., AND G. S. BRUSH Long-term history of Chesapeake Bay anoxia. Science 254: DURBIN, A. G., AND E. G. DURBIN Standing stocks and estimated production rates ofphytoplankton and zooplankton in Narragansett Bay, R.I. Limnol. Oceanogr. 23: FALKOWSKI, P. G., T. S. HOPKINS, AND J. J. WALSH An analysis of factors affecting oxygen depletion in the New York Bight. J. Mar. Res. 38: JUDKINS, D. C Vertical distribution of zooplankton in relation to the oxygen minimum off Peru. Dcep- Sea Res. 27: KAMYKOWSKI, D., AND S. ZENTRA Hypoxia in the world ocean as recorded in the historical data set. Deep-Sea Res. 37: 186 l-l 874. KEMP, W. M., P. A. SAMPOU, J. GARBER, J. TUTTLE, AND W. R. BOYNTON Seasonal depletion of oxygen from bottom waters of Chesapeake Bay: Roles of benthic and planktonic respiration and physical exchange processes. Mar. Ecol. Prog. Ser. 85: KRING, R. L., AND W. J. O BRIEN Effect of varying oxygen concentrations on the filtering rate of Daphnia pulex. Ecology 57: LAMPITT, R. S., AND J. C. GAMBLE Diet and respiration of the small planktonic marine copepod, Oithona nana. Mar. Biol. 66: 185-l 90. LEMING, T. D., AND W. E. STUNTZ Zones ofcoastal hypoxia revealed by satellite scanning have implications for strategic fishcries. Nature 310: 136-l 38. LONGHURST, A. R Vertical distribution of zooplankton in relation to the eastern Pacific oxygen minimum. Deep-Sea Rcs. 14: LONSDALE, D. J Regulatory role of physical factors and predation for two Chesapeake Bay copepod species. Mar. Ecol. Prog. Ser. 5: LUTZ, R. V., N. H. MARCUS, AND J. P. CHANTON Effects of low oxygen concentrations on the hatching and viability of eggs of marine Calanoid copepods. Mar. Biol. 114: MALONE, T. C., L. H. CROCKER, S. E. PIKE, AND B. WENDLER Influences of river flow on the dy-
12 1614 Roman et al. namics of phytoplankton production in a partially stratified estuary. Mar. Ecol. Prog. Ser. 48: AND OTHERS Lateral variations in the production and fate of phytoplankton in a partially stratified estuary. Mar. Ecol. Prog. Ser. 32: MAY, E. B Extensive oxygen deplction in Mobile Bay, Alabama. Limnol. Oceanogr. 18: NIXON, S. W., C. A. OVIATT, J. FRITHSEN, AND B. SULLI- VAN Nutrients and the productivity of estuaries and coastal marine ecosystems. J. Limnol. Sot. 1 S. Afr. 12: OFFICER, C. B., AND OTHERS Chesapeake Bay anoxia: Origin, development and significance. Science 23: OLSON, M. M Zooplankton, p In Ecological studies in the middle reach of Chesapeake Bay. Coastal Estuarine Stud. V. 23. Springer. PURCELL, J. E., J. R. WHITE, AND M. R. ROMAN Predatiot by gelatinous zooplankton and resource limitation as potential controls of Acarlia tonsa copepod populations in Chesapeake Bay. Limnol. Oceanogr. 39: In press. ROMAN, M. R Tidal resuspension in Buzzards Bay, Massachusetts. 3. Seasonal cycles of nitrogen and carbon: Nitrogen ratios in the seston and zooplankton. Estuarine Coastal Mar. Sci. 11: , K. A. ASHTON, AND A. L. GAUZENS Day/ night differences in the grazing impact of marine copepods. Hydrobiologia : 2 l-30. SEWELL, R. B., AND L. FACE Minimum oxygen layer in the ocean. Nature 162: VINOGRADOV, M. E., AND N. A. VORONINA The influence of oxygen deficit upon the plankton distribution in the Arabian Sea. Okeanologiya 2: UYE, S Development of neritic copepods Acartia clausi and A. steuri. 1. Some environmental factors affecting egg development and the nature of resting eggs. Bull. Plankton Sot. Jpn. 27: l-9. -, AND A. FLEMINGER Effects of various environmental factors on egg development of several species of Acartia in southern California. Mar. Biol. 38: WALSH, J. J., G. T. Rowe, R. L. IVERSON, AND C. P. McRou Biological export of shelf carbon is a sink of the global COz cycle. Nature 291: WHITE, J. R., AND M. R. ROMAN Measurement of zooplankton grazing using particles labcllcd in light and dark with [methyl- H] methylamine hydrochloride, Mar. Ecol. Prog. Ser. 71: , AND a. Egg production by the calanoid copepod Acartia tonsa in the mcsohaline Chesapcake Bay: The importance of food resources and temperature. Mar. Ecol. Prog. Ser. 86: , AND b. Seasonal study of grazing by metazoan zooplankton in the mesohaline Chesapeake Bay. Mar. Ecol. Prog. Ser. 86: 25 l Submitted: 29 December 1992 Accepted: 7 June 1993 Revised: 15 July 1993
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