Estuaries Vol. 21, No. 2, p. 328-339 June 1998 Egg Production of the Copepod Summer. 1. The Roles of Food Acartia tonsa in Florida Bay During Environment and Diet G. S. KLEPPEL ~ Department of Environmental Health Scienc~.s University of South Carolina Columbia, South Carolina 29208 GAROL A. BURKART LEE HOUCHIN Oceanographic Center Nova Southeastern University Dania, Florida 33004 CARMEI.O TOMAS Florida Marine Research Institute Department of Environmental Protection St. Petersburg, Florida 33701 ABSTRACT: The diet and egg production rate of Acartia tonsa were measured during the thermally stable period between June and October 1995 at four locations in inner and outer Florida Bay. We sought to characterize the role of A. tonsa in the bay's pelagic food web, which has been changing since 1987, when the dominant submerged vegetation began shifting from benthic seagrasses to planktonic algae. At Rankin Lake, a shallow basin on the north side of the inner bay, where extensive seagrass mortality and persistent cyanobacteria blooms have occurred, microplankton biomass was relatively high and dominated by heterotrophic protists and dinoflagellates. Nanoplankton at Rankin Lake, while numerically abundant, usually contributed only a small portion of the biomass. The ingestion rate of A. tonsa in Florida Bay varied independently of food concentration (i.e., total microplankton biomass), but rates were higher (mean - SD = 3.88 • 0.73 Itg C copepod -l d -l) on the north side of the bay than on the south side (0.78 - 0.11 Itg C copepod 1 d l ). Microzooplankton and dinoflagellates were important dietary constituents, especially in the vicinity of Rankin Lake. Egg production in this region (mean • SD = 14.2 :l: 7.7 eggs female -I d -I) was considerably higher than the baywide mean (5.8 -+ 0.81 eggs female i d 1), and principal components analysis revealed a.s.sociations between egg production and both dietary microzooplankton and dinoflagellate biomass. However, although grazing rates were relatively high in the inner bay, A. tonsa removed only 1-6% of the primary production from the water column during the summer and its egg production rates were low relative to typical rates for the species. Introduction Florida Bay is a shallow, subtropical, lagoonal es- tuary located at the southern tip of the Florida peninsula (Fig. 1). It is bordered on the east by Biscayne Bay and the upper Florida Keys. To the south are the central and lower Keys, and on the west is the Gulf of Mexico. The bay is composed of numerous small submerged basins, bounded by sand and mud banks and mangrove islands. In 1987, the extensive seagrass beds that character- ized the submerged flora of Florida Bay, particu- larly in the central and inner regions near Rankin Lake (Fig. 1), experienced massive mortality (Zie- man et al. 1989), the cause of which remains un- Corresponding Author: Tele: 803/777-4216; Fax: 803/777- 3391; E-mail: [email protected]. certain. Coincident with the loss of the seagrass community, a series of persistent cyanobacteria and ultraplanktonic diatom blooms (chlorophyll levels > 10 Izg 1-1; C. Tomas unpublished data) occurred. These blooms shifted dominance among primary producers from the benthos to the plank- ton (Boesch et al. 1993). However, it is not yet known how these changes have "affected the sec- ondary production and trophic structure of the Florida Bay ecosystem. We report here on a portion of a larger study of the factors controlling water column production in Florida Bay. We focus on the relationship between the diet and egg production of the calanoid co- pepod Acartia tonsa. Acartia tonsa occurs in the nearshore waters and estuaries of warm temperate and subtropical Cc) 1998 Estuarine Research Federation 328
Transcript
Estuaries Vol. 21, No. 2, p. 328-339 June 1998
Egg Production of the Copepod
Summer. 1. The Roles of Food
Acartia tonsa in Florida Bay During
Environment and Diet
G. S. KLEPPEL ~ Department of Environmental Health Scienc~.s University of South Carolina Columbia, South Carolina 29208
GAROL A. BURKART LEE HOUCHIN Oceanographic Center Nova Southeastern University Dania, Florida 33004
CARMEI.O TOMAS
Florida Marine Research Institute Department of Environmental Protection St. Petersburg, Florida 33701
ABSTRACT: The diet and egg product ion rate of Acart ia tonsa were measured during the thermally stable per iod between June and October 1995 at four locations in inner and outer Florida Bay. We sought to characterize the role o f A. tonsa in t h e bay's pelagic food web, which has been changing since 1987, when the dominant submerged vegetation began shifting f rom benthic seagrasses to planktonic algae. At Rankin Lake, a shallow basin on the nor th side of the inner bay, where extensive seagrass mortality and persistent cyanobacteria b looms have occurred, microplankton biomass was relatively high and dominated by heterot rophic protists and dinoflagellates. Nanoplankton at Rankin Lake, while numerically abundant , usually contr ibuted only a small por t ion o f the biomass. The ingestion rate o f A. tonsa in Florida Bay varied independent ly o f food concentrat ion (i.e., total microplankton biomass), but rates were higher (mean - SD = 3.88 • 0.73 Itg C copepod -l d - l) on the nor th side o f the bay than on the south side (0.78 - 0.11 Itg C copepod 1 d l ). Microzooplankton and dinoflagellates were impor tant dietary constituents, especially in the vicinity o f Rankin Lake. Egg product ion in this region (mean • SD = 14.2 :l: 7.7 eggs female -I d -I) was considerably higher than the baywide mean (5.8 -+ 0.81 eggs female i d 1), and principal components analysis revealed a.s.sociations between egg product ion and both dietary microzooplankton and dinoflagellate biomass. However, although grazing rates were relatively high in the inner bay, A. tonsa removed only 1-6% o f the pr imary product ion from the water column during the summer and its egg product ion rates were low relative to typical rates for the species.
Introduct ion
Florida Bay is a shallow, subtropical, lagoonal es- tuary located at the southern tip of the Florida peninsula (Fig. 1). It is bordered on the east by Biscayne Bay and the upper Florida Keys. To the south are the central and lower Keys, and on the west is the Gulf of Mexico. The bay is composed of numerous small submerged basins, bounded by sand and mud banks and mangrove islands. In 1987, the extensive seagrass beds that character- ized the submerged flora of Florida Bay, particu- larly in the central and inner regions near Rankin Lake (Fig. 1), experienced massive mortality (Zie- man et al. 1989), the cause of which remains un-
certain. Coincident with the loss of the seagrass community, a series of persistent cyanobacteria and ultraplanktonic diatom blooms (chlorophyll levels > 10 Izg 1-1; C. Tomas unpubl ished data) occurred. These blooms shifted dominance among primary producers from the benthos to the plank- ton (Boesch et al. 1993). However, it is not yet known how these changes have "affected the sec- ondary product ion and trophic structure of the Florida Bay ecosystem.
We report here on a port ion of a larger study of the factors controlling water column product ion in Florida Bay. We focus on the relationship between the diet and egg product ion of the calanoid co- pepod Acartia tonsa.
Acartia tonsa occurs in the nearshore waters and estuaries of warm temperate and subtropical
Fig. 1. Florida Bay, showing locations of stations sampled during this study. Off-set map shows the location of Florida Bay within the state of Florida.
regions throughout the world; it is abundant in Florida Bay (P. Ortner, personal communication). Although aspects of the distribution and ecology o f A. tonsa in Florida waters have been considered extensively (Woodmansee 1958; Reeve 1964; Reeve and Walter 1977; Roman et al. 1983; Marcus 1985; Carter 1995), we are aware of no published, quan- titative information for this species in Florida Bay.
The physiological ecology of A. tonsa is charac- terized by high P /B turnover rates and low energy storage capacity (Dagg 1977; Miller et al. 1977). Hence, variability in the food environment tends to be reflected by relatively rapid changes in pro- duction (Tester and Turner 1990). The study de- scribed here was designed to take advantage of these attributes in order to identify more clearly the consequences of changes in the bay's trophic structure to secondary production. Given the sig- nificance of copepods in the diets of fishes (e.g., Hunter 1981; Turner 1984) and the potential im- pact that changing trophic structure in Florida Bay may be having on copepod production, it is rea- sonable to expect that significant changes will oc-
cur in the composition and productivity of local fish assemblages and, ultimately, regional fisheries. It is important, therefore, that the trophic dynamic roles of the dominant copepods in Florida Bay, such as A. tonsa, be documented and understood.
Materials and Methods
SAMPI .ING
The feeding and egg production rates ofA. tonsa were measured on June 12-13,July 24-25, Septem- ber 18-19, and October 10-11, 1995, at stations reflective of a range of micro-environments in the bay (Fig. 1). In July and September, experiments were conducted with samples collected from the four stations shown in the figure. In June, the sam- ple from Sandy Bank was accidentally destroyed, and in October, no adult female A. tonsa were found in samples from Rankin Lake. Thus, exper- iments were performed with samples from three, rather than four, stations in June. In October, graz- ing experiments were performed with copepodite stage 5 A. tonsa; egg production was not measured.
330 G.S. Kleppel et al.
On the first day of each study period, two small (7 m) boats were deployed f rom the Keys Marine Labora tory of the Florida Institute of Oceanogra- phy, at Long Key. One boat sampled at Sprigger and Sandy Banks, while the o ther collected sam- ples at Rankin Lake and off Captain Key. At each station, tempera ture , conductivity, and dissolved oxygen were measured (with a Hydrolab environ- mental moni tor ing system) and 20 1 of water were collected in acid-washed, polyethylene carboys for use in experiments .
The zooplankton was sampled by towing a 202- tzm mesh Nitex net (0.5 m mou th diameter) , equ ipped with a solid cod end, th rough the water for 3-5 min. The shallow depths (ca. 1-2 m) at these stations requi red that tows be conf ined to the surface. The zooplankton was t ransferred to cool- ers containing water f rom the sampling site. A "blue ice" pack was at tached to the inside cover of each cooler, and an "Oxy-tab," oxygen-gener- ating canister, was placed in the water. The lowered wate r t e m p e r a t u r e a n d i n c r e a s e d o x y g e n a t i o n were in tended to reduce stress dur ing transit (2-4 h) to the Florida Depa r tmen t of Environmenta l Protect ion Laboratory, in Marathon, where the ex- per iments were pe r fo rmed . Copepods were active and appeared healthy when they were p repared for study.
MEASUREMENT O1" FEEDING AND DIET
Ingestion rates and diets were measured by pre- viously descr ibed methods or slight modifications t he reo f (Kleppel 1992; Carter 1995; Kleppel et al. 1996a). First, a set of 250-ml "init ial" samples f rom each station was passed th rough a 100-1~m Nitex mesh screen to remove large particulates. The sam- ple was then fixed with acid Lugol 's iodine. Next, five adult female Acartia tonsa f rom each station were sorted into each of three 1-1 polycarbonate containers filled with similarly screened water f rom that station (exper imenta l samples). Finally, an identical set of samples was p repa red without co- pepods (controls). Macronutr ients f rom the f-me- dium formula t ion of Guillard and Ryther (1962) were added to the exper imenta l and control sam- ples (final e n r i chmen t = f /16) to obviate certain "bo t t l e" artifacts associated with food limitation (Roman and Rublee 1980; Saiz et al. 1996). Both sets of samples were placed in a flow-through in- cubator on the laboratory dock, through which wa- ter f rom within 2 m of the surface was p u m p e d to maintain t empera tu re to within 0.5~ of ambient . The incubator was covered with a double layer of fiberglass screen to reduce light pene t ra t ion to ca. 5% of incident intensity. This creates a relatively natural pho toper iod , which may provide impor tan t feeding cues (Head et al. 1985; Stearns 1986; Klep-
pel et al. 1988), and simultaneously reduces ex- posure to potentially damaging light intensities (Krinsky 1971). Particles were kept in suspension by the flow of water th rough the incubator. Graz- ing rates in similarly agitated samples were not d i f fe rent f rom those in samples rota ted on a plankton wheel (unpubl ished data). Because the water col- umn was shallow, well mixed, and hence isother- mal, the probabili ty was low that the t empera tu re aliasing described by Saiz et al. (1996) occur red dur ing the experiments .
Following a 24-h incubat ion period, a 250-ml subsample was withdrawn f rom each exper imenta l and control sample and fixed with acid Lugol 's io- dine for later microscopic analysis. In September, copepods in one replicate f rom Rankin Lake and one replicate f rom Sandy Bank died dur ing the incubation. These replicates were discarded.
Cells were coun ted (min imum of 200 cells per sample) and their dimensions were measured un- der an inverted microscope. Cell dimensions were used to estimate the cell volumes of microplankton taxa by analogy to s tandard polyhedra (Kleppel 1992). Diatoms were t reated as right circular cyl- inders, dinoflagellates and ciliates were oblate spheroids (or spheres in some cases), and cells ---5 I.tm in d iameter were cons idered 5-i.tm spheres (see below). Cellular carbon con ten t was estimated with the cell volume-to-carbon conversion equa- tions of S t ra thmann (1967) for diatoms, dinoflag- ellates and nanoplankton; of Putt and Stoecker (1989) for ciliates; and of Bartram (1980) for o ther microzooplankton. For brevity, cells -<5 txm in di- amete r are re fer red to as nanop lank ton (Beers et al. 1980; Kleppel 1992; Kleppel et al. 1996a). It is recognized, however, that by definit ion, the hanD- plankton encompasses the size range f rom 2 I~m to 20 Izm (Sieburth et al. 1978). The carbon biD- mass of diatoms, dinoflagellates, nanoplankton , microzooplankton (e.g., ciliates, he te ro t roph ic di- noflagellates, and a few metazoan taxa), and mi- croflagellates (ca. 8 • 4 ixm cells that we believe to be choanoflagellates; see Tomas 1993) was de- t e rmined by multiplying cell abundances by the cellular carbon con ten t of each species and sum- ming within taxonomic groups (Kleppel 1992; Kleppel et al. 1996a).
Ingestion rates were c o m p u t e d with the equa- tions of Frost (1972). We did not modify the pro- tocol as suggested by Marin et al. (1986) because these modifications require shor ten ing the incu- bat ion period. Marin et al. (1986) po in ted out that as the per iod of incubat ion lengthens, the e r ror in t roduced by the necessary assumption in their protocol that food concent ra t ion remains con- stant, increases. With 24-h incubations, the e r ro r is on the o rde r of 25%. Twenty-four h o u r incuba-
tions are crucial to our protocol because the feed- ing activity of A. tonsa varies on a d i e l cycle, in a manner that is not predictable (Kleppel et al. 1985; Kleppel et al. 1988).
MEASUREMENT OF EGG PRODUCTION
Egg product ion rates were measured by pipet- ting five ovigerous adult A. tonsa from each station, in to each of th ree 1-1 con ta ine r s filled with screened water from the collection site. Following 24 h of incubation, the samples were concentrated, fixed with Lugol 's iodine, and allowed to settle for 24 h. All of the eggs in each sample were counted at 100• magnification (Kleppel 1992). We have previously measured negligible rates of cannibal- ism by A. tonsa on its eggs (Kleppel 1992).
STATISTICAl. AND NUMERICAl. ANAI.YSES
Data were analyzed by both bivariate and multi- variate techniques. Least squares regressions were used to identify relationships between food envi- ronment , feeding, and egg production. Multivar- iate relationships were identified by principal com- ponents analysis (PCA), a form of factor analysis that compresses a multivariate dataset into a new set of variables or components that are associated with one another such daat the proport ion of the total variance explained by successive components is maximized (Estrada and Blasco 1979). Function- ally, PCA permits one to identify associations be- tween groups of variables within a large, complex dataset (Kachigan 1991). The approach is concep- tually pleasing because it recognizes the multivar- iate nature of ecological systems and can reveal patterns between groups of variables within data- sets that might be difficult to discern with regres- sion analysis. A limitation of PCA is that it does not provide an equation or other mechanism to pre- dict the dependency of one variable upon another. As such, PCA might be considered as a first step in the analysis of a potentially complex system. P ( ~ was per fo rmed here with the Statistica soft- ware package, on unrotated, log-transformed en- vironmental and diet-composition data. Zeros were deleted from the analysis, per the recommenda- tions of Allen and Koonce (1973) and Estrada and Blasco (1979).
Results and Discussion TEMPERATURE AND E(;G PRODUCTION
Temperature and food environment, (Durbin et al. 1983, 1992; Hunt ley and Lopez 1992; Kleppel 1992; Kleppel et al. 1996b) are among the princi- pal determinants of feeding and egg product ion rates of copepods. In our efforts to describe the feeding dynamics of A. tonsa and to unders tand its significance to secondary product ion in Florida
35
Acartia tonsa Production in Florida Bay 331
3O
25
Q. E 20 b-
15 i 1 i Jur~ Jut Aug Sep Oct Nov Dec Jan Feb Mar Apt May Jun
1995 1996
[ .~Rankin ~Capta in -~Spdgger + S a n d y ]
Fig. 2. Water temperatures at each of four stations in Florida Bay measured once each month from June t995 to June 1996.
Bay, we sought to minimize the influence of tem- perature in the data. This was accomplished by fo- cusing on a period of time when temperature was relatively constant. A plot of monthly sea surface temperatures at each of the four locations in Flor- ida Bay between June 1995 and June 1996 (Fig. 2) shows that, in general, temperatures varied little between stations. There is, however, p ronounced seasonality in the data, commencing with a sharp decline between October and November. We com- pared the mean temperature at each station with the cumulative mean, over an increasing period of months from June, until we found the point at which the difference between the monthly mean and the cumulative mean was significant (Student 's t-test). That point occurred in November (t = 3.47; p < 0.05). Thus, on the study dates, differences between mean temperatures were not statistically significant.
To determine whether or not the egg produc- tion rate varied systematically with temperature during the summer, egg product ion rates (number of eggs female-1 d- J) were converted to estimates of carbon biomass product ion (~tg C female -1 d 1) by multiplying by 0.031 ~g C egg --~ (Kleppel 1992) and then regressed against temperature. A plot of the daily egg C-production rate versus temperature (Fig. 3) has a slope that does not differ statistically from zero (r = -0.48; p > 0.05).
Next, the egg product ion rates of A. tonsa in Florida Bay during the summer were compared to the potential rates expected if temperature alone governed egg p roduc t ion . Tempera tu re -depen- dent, potential egg product ion was estimated (sol- id line in the figure) with the equation given by Kleppel et al. (1996b)
g = 0.064e ~176 (1)
where g = the growth rate which, in this case, is
332 G . s . Kleppel et al.
2!_
"lO O
CL 8 0
g
o n
Fig. 3.
LI.I
~ J
�9 ~
l : i ' " 0 _ _ J , ; T 29 29.5 30 30.5 31 31.5 32
Temperature (C)
Scatterplot of t empera tu re (T, in uni ts o f ~ versus egg produc t ion (g, in units of I~g C copepod 1 d l) at the sta- t ions in Florida Bay sampled between J u n e and Oc tober 1995. The solid line is the es t imated t e m p e r a t u r e - d e p e n d e n t egg pro- duc t ion c o m p u t e d ti 'om the equa t ion g = 0.064e ~176 (see text).
taken to be the egg produc t ion rate (p,g C d- t ) , and T = t empera tu re (~ Observed egg produc- tion rates were well below the tempera ture-depen- den t potential.
FOOl) E:',~RONM~:gT, FEEDING AND EG(; PRODUCTION
Microplankton biomass was elevated at Rankin Lake relative to that at Sprigger Bank, Sandy Bank, and Captain Key (Fig. 4a-d) . Usually, the largest cont r ibut ion to the microplankton biomass was f rom microzooplankton , particularly ciliates and he te ro t roph ic dinollagellates (e.g., Protoperidinium spp.).
Ingestion rates (Fig. 5a-d) ranged from 0.09 I~g C copepod-1 d i to 7.30 p,g C copepod -j d-~, or approximately 2% to 194% of body C d -~ (assum- ing a body carbon con ten t of 4 I~g; cf. Landry 1983). This range, while wide, is not inconsistent with observations on A. tonsa, both in the labora- tory (Kiorboe et al. 1985) and in the field (Kleppel 1992). Ingestion rates on the nor th (mainland) side of the bay were 5 times h igher than on the south side (mean + SD = 3.88 -+ 0.73 versus 0.78 - 0.11 p.g C copepod -1 d- l ) .
m
O
v
O9 00
E O
.Q t - O
t -
C~. O L)
700
600
500
400
300
200
100
0
C3Microfla
r-INanopl
rt'~Microzoo
==Dinofl
r~Diatoms
700
600
500
400
300
200
100
0 Captain Rank in Sandy Sprigger Captain Rankin Sandy Sprigger
Fig. 4. Microplankton biomass at the stations sampled in Florida Bay on (a) June 12, 1995, (b) July 24, 1995, (c) September 18, 1995, and (d) Oc tober 10, 1995. Shaded areas on bars refer to the b iomass o f various t axonomic g roups inc lud ing diatoms, dinoflag- eUates (Dinofl), mic rozoop lank ton (Microzoo), n a n o p l a n k t o n (Nanopl) , and microflagellates (Microfla). nd = no data (at Sandy in June ) .
Acartia tonsa Production in Florida Bay 3 3 3
"13 0 {3_
13.. 0 0
0 133
n- r o c0
c-
5 (a) June
4
3
2
1
I 0 ....... J Captain
DMicrofla rmNanopl ~aMicrozoo EDinof l
m Diatoms
I
~-~ nd Rankin Sandy Sprigger
(b) July
Captain Rankin Sandy Swigger
I0
8
6
4
2
0
(c) September
i j _ . _ _ Captain Rankin
10 I (d) October
1 !i ii!ii:'ii
I ~ 4
2
F 0 Sandy Sprigger Captain
I
Rankin Sandy Sprigger
Fig. 5. Composition of microplankton biomass in the diet of Acartia ton.sa at stations in Florida Bay on (a) June 12-13, 1995, (b) July 24-25, 1995, (c) September 18-19, 1995, and (d) October 10--11, 1995. Note that at Rankin Lake, ingestion rates were measured on copepodite stage 5. tlistograms represent mean ingestion rates (error bars are standard deviations) with shading reflecting the biomass of specific taxonomic: groups (see Fig. 4). nd = no data (at Sandy in June).
Egg produc t ion rates between J u n e and October (Fig. 6a-d) were generally low, ranging f rom 1.4 eggs female 1 d--i to 26.6 eggs female i d-t . None- theless, mean rates at Rankin Lake (mean _+ SD = 14.2 - 7.7 eggs female -I d l) were significantly h igher (t-test, p < 0.05) than the group mean for all o ther stations (7.1 + 1.3 eggs female ~ d- l ) . No systematic relat ionship between egg produc t ion and e i ther food availability or ingestion rate was evident in the data. Egg p roduc t ion rates varied independen t ly of total microplankton biomass in the water co lumn (r = 0.31; p > 0.05) and total microplankton biomass in the diet (r = 0.26; p > O.O5).
Principal componen t s analysis (Fig. 7), however, revealed a strong association between egg produc- tion and dietary microzooplankton biomass (load- ing = 0.78 in principal c o m p o n e n t 2). A weaker, but p rominen t , association (loading = 0.57) be- tween egg produc t ion and dietary dinoflagellate biomass was also de tec ted in principal c o m p o n e n t 2. Overall, >85% of the variability in the data was explained in the first three principal components , with most of this (72%) expla ined in componen t s 1 and 2 (Fig. 7). The relat ionship between egg pro- duct ion and microzooplank ton biomass is dem- onstrated fu r the r by the observat ion that at Rankin Lake, where A. tonsa exhibi ted h igher egg produc-
tion rates than it did at the o ther three stations, approximately 70% of the copepod ' s dietary C-in- take was cont r ibu ted by microzooplankton (Table 1).
NUISANCF BLOOMS AND PI~NKTON DYNAMICS IN FLORIDA BAY
Rankin Lake, in inner Florida Bay, was the site of large-scale seagrass mortality and extensive cy- anobacter ia blooms. It was also, interestingly, the location where egg p roduc t ion by Acar t ia tonsa was highest in our study. We believe that this enhanced egg produc t ion was driven by a microzooplankton t rophic link (i.e., nanop lank ton --~ microzooplank- ton ---) copepods) ra ther than by a direct link be- tween pr imary producers and copepods (Sherr et al. 1986; Kleppel et al. 1991, 1996a). A. tonsa feeds extensively on he te ro t roph ic protists (Stoecker and Sanders 1985; Gifford and Dagg 1988; Kleppei 1992), which may be nutr i t ious (Kleppel and Bur- kart 1995) and capable of suppor t ing significant egg produc t ion in this species (Stoecker and Egloff 1987; Stoecker and Capuzzo 1990; Kleppel et al. 1991; Kleppel 1992; but see Eder ington et al. 1995).
The algal blooms that began in 1987, in the vi- cinity of Rankin Lake, were composed o f nano- phytoplankton and ul t raphytoplankton (<2 Ixm in
Fig. 6. Mean egg produc t ion rates o f Acartia tonsa at stations in Florida Bay on (a) .June 12-13, 1995, (b) July 24-25, 1995, (c) Sep tember 18-19, 1995 and (d) October 10--11, 1995. Error bars are s tandard deviations.
diameter), a major component of which was the cyanobacterium Synechococcus sp. (Steidinger et al. 1995). It is unlikely that these blooms led directly to enhanced copepod production. Cyanobacteria
are thought to be difficult for calanoids to digest (R. Itturiaga personal communication), and when they occur singly, the small cells (e.g., <-1 txm di- ameter) are not efficiently captured by Acartia spp
Fig. 7. Load ing o f variables within factors (principal c o m p o n e n t s ) 1 and 2 f rom principal c o m p o n e n t s analysis o f env i ronmen ta l and dietary variables associated with env i ronmen ta l condi t ions in Florida Bay between .June and Oc tober 1995 and the diet and egg p roduc t ion o f Acartia tonsa dur ing that per iod o f time. Abbreviations: FLGIATES = dietary microflagellate biomass; DO = dissolved oxygen; NANOPLNKT = dietary n a n o p l a n k t o n biomas.s; DIATOMS = dietary d ia tom biomass; TEMP = surface tempera ture ; SALIN- ITY = salinity; DINOS = dietary dinoflagellate bioma.ss; M I C R O Z O O = dietary mic rozoop lank ton biomass; EGC, PROD = egg p roduc t ion rate.
TABLE 1. Proportion of microzooplankton in the diet o f Acm~ tia tonsa in Elnrida Bay. Smnmer 1995.
ProporUou
Month Captain Kankm Sat~dy Sprigger
June o. 13 0.43 ha" 0.70 .July 0.30 0.97 0.00 0.00 September 0.00 0.67 0.00 0.00 October 0.22 0.74 0.25 0.09 Mean 0.16 0.70 0.08 0.20 SD 0.11 0.19 0.12 0.29
Data not available.
(a) Bay-wide Average
Acartia tonsa Production in Florida Bay 335
(Niva l a n d N iva l 1976; P a f f e n h 6 f e r 1988) . C o n - verse ly , c y a n o b a c t e r i a a r e r e a d i l y i n g e s t e d a n d di- g e s t e d by m a l t y h e t e r o t r o p h i c p ro t i s t s ( I t u r r i a g a a n d M i t c h e l l 1986; S h e r r a n d S h e r r 1987) . W e h a v e o b s e r v e d h i g h r a t e s o f m i c r o z o o p l a n k t o n g r a z i n g a t R a n k i n L a k e ( K l e p p e l e t al. u n p u b l i s h e d d a t a ) . W e n o t e , h o w e v e r , t h a t we h a v e f o c u s e d o n t h e a d u l t s o f a s i n g l e c o p e p o d spec i e s . O t h e r de - v e l o p m e n t a l s t ages a n d s p e c i e s m a y f e e d o n s m a l l ce l l s u n a v a i l a b l e to a d u l t A . t o n s a ( P a f f e n h 6 f e r 1984)
F i g u r e 8 p r e s e n t s a se t o f c o n c e p t u a l i z a t i o n s t h a t c o m p a r e f o o d w e b s t r u c t u r e a t R a n k i n L a k e , in t h e
micro-phytop lankton mesozoop lank ton ,.~O IR--55.1o ~g C/m31d
6O, o -
14 23 mg C/m3/d ~ i i ~ zoop lank ton
7.70 mg C/ i ! 2.80 mg C/ i ~ 197.3 mg +d ' : ~
eggs ~
nano-phy top lank ton 48.5 mg C/m3
Fig. 8. (a) Conceptualizadon of the Florida Bay-wide, average planktonic food web. (b) As in (a) but at Rankin Lake, where seagrass die-of& and persistent uuisauce algal blooms have occurred. Values associated with compartments (e.g., microzooplankton) are C-biomass (units are, mg C m-~). IR = ingestion rate of Acartia to'usa was computed by muhiplying the measured, copepod-specific ingestion rate by the approximate abundance ofA. tonsa during the summer (estimated at 14.7 A. tonsa l -t fbr the inner bay, and 4.6 A. tonsa 1 ~ tot the bay-wide awwage; P. Ortncr personal communication). Percentages next to arrows rcprescnt percent of dietary C for A. tonsa feeding on a given 1hod source. The decimal ti'action associated with each arrow is either an ingestion rate for a particular kind of food or the egg production rate. The units of both rates are mg C m s d 4. The ? indicates that the amount ot" carbon transferred fi'om the nanophytoplankton to the microzooplankton is uncertain.
336 G.S. Kleppel et al.
TABLE 2. A comparison of the egg product ion rates of Acartia tonsa from estuaries and coastal waters in the United States. i 'ligher rates were achieved with phytoplankton from nutrient-enriched or otherwise optimized environments.
Temperature Range Egg Production Location (~ (eggs fenlale -I d -~) Reference
Florida Bay, Florida 28.2-32.3 5.8 -+ 0.81 This study Rankin Lake (inner Florida Bay) 28.8-32.3 14.2 -+ 7.7 Port Everglades, Florida 18.0-28.0 16.2 -+ 13.2 Carter 1995 East Lagoon, Texans 20.0-30.0 �9 56.0 +- 22.0 Ambler 1985 Skidaway River, Georgia nd ~ 25.5 Stearns et al. 1989 Newport River, North Carolina nd �9 10.0 Stearns et al. 1989 l .ong Island Sound, New York <2.0-22.0 32.9 Bellantoni and Peterson 1987 Narragansett Bay, Rhode Island <18.0-25.0 24.1 -+ 15.2 Durbin et al. 1983
85.3 -+ 8.8 Sullivan and Ritacco 1985 l,os/Mlgeles Harbor. California 14.6--21.5 19.4 -+ 11.7 Kleppel 1992
" nd = data not available.
region where the most severe blooms and seagrass mortality occurred, to the "bay-wide average," computed from the other three stations that we studied. Because we did not sample the zooplank- ton quantitatively, estimates of A. tonsa biomass from nearby locations and sampling dates close in time to the dates of our study were kindly provided by E Ortner (National Oceanic and Atmospheric Administration, Atlantic Oceanographic and Met- erological Laboratory, Miami, personal communi- cation).
While nanoplankton biomass at Rankin Lake was about the same as the bay-wide average, microphy- toplankton and microzooplankton biomasses were 3-4 fold higher at Rankin Lake than in the bay, on average. About 70% of the diet of Acartia was com- posed of microphytoplankton "bay-wide," whereas, at Rankin Lake, about 70% of the diet was com- posed of microzooplankton. The high microzoo- plankton biomass at Rankin Lake, coupled with the importance of microzooplankton in the cope- pod diet (Fig. 7 and Table 1) supports the hypoth- esis that the trophic structure of Rankin Lake de- pended more heavily on the microbial food web than on a predominantly herbivorous food web.
Tomas (1996) reported higher rates of primary production at Rankin Lake (i.e., more than 3 g C m -'2 d 1 or approximately 1,000 mg C m -~ d J) than in the outer bay (1-3 g C m -2 d-1, o r 333- 1,000 mg C m :4 d-t). Given the ingestion rates that we observed (9.5 mg C m -'~ d 1 and 55.1 mg C m -s d ~ bay-wide and at Rankin Lake, respectively), it would appear that A. tonsa could not graze more than 6% of the primary production at Rankin Lake (Fig. 8b) and ca. 1-3% of the primary production in the bay, on average (Fig. 8a).
T I l E CddJSE OF Low EGG PROI)UC.TION
A. tonsa exhibited significantly higher average rates of egg production at Rankin Lake than it did at the other stations we studied; however, rates were nonetheless low relative to those typical for
the species (Table 2). Egg production at Rankin Lake was similar to that observed by Carter (1995) at Port Everglades, an urbanized estuary on the southeast coast of I"lorida, but rates at the other stations were the lowest reported to date 1or Acartia tonsa.
Although egg production rates by Acartia tonsa in Florida Bay varied with the concentration of mi- crozooplankton in the diet (Fig. 7), we have not addressed the question of why, overall, egg pro- duction rates were low. We rejected the possibility that egg production was inhibited by high temper- atures because temperature did not vary signifi- cantly during the study and, further, temperature showed no systematic relationship with tempera- ture (Fig. 3). Principal components analysis sug- gests egg production rates were not associated with salinity or dissolved oxygen levels during the sum- mer (Fig. 7). Our results to date suggest a link to food quality, the importance of which has been well documented for Acartia tonsa (Durbin et al. 1983; Roman 1984; Ambler 1986; Stoecker and Egloff 1987; Kleppel 1992; White and Roman 1992). It is probable, however, that over the course of the year, variability in temperature, may affect egg production, as well (Ambler 1985; Kleppel 1992).
The relationship between the egg production and ingestion rates (as carbon) is defined by the gross efficiency of egg production
Kt = E P / I R (2)
where EP and IR are the daily rates of egg pro- duction and ingestion, respectively, in units of Ixg C copepod -1 (Table 3). Kiorboe (1989) observed that K] varies with the C:N ratio, suggesting that K] is influenced by food quality. In the present study, Kj varied from 0.02 to 1.00, suggesting that all of the egg production observed during the study could be accounted for by the carbon in the plank- tonic diet (i.e., K t > 1.0 indicates that either some additional source of C, not accounted for in the
Acartia tonsa Production in Florida Bay 337
TABI,E 3. Gross efficiency of egg product ion (KI) of Acartia tonsa at four stations in Florida Bay between June and October 1995. Stations are CPTN = Captain Key, RNKN = Rankin Lake, SPRG = Sprigger Bank, SNDY = Sandy Bank.
Month CPTN RNKN SPRG SNDY Mean SD
.Jmle 0.28 0.96 1.00 nd ~ 0.75 0.33 July 0.33 0.23 0.36 0.05 0.24 0.12 September 0.13 0.07 0.05 0.05 0.08 0.03 October 0.02 nd 0.02 0.04 0.03 0.01 Mean 0.19 0.42 0.36 0.05 SD 0.12 0.39 0.39 0.005
n d = no data.
analysis, is required to produce the observed bio- mass of eggs or that maternal reserves are being used to produce eggs). In general, Kt was higher during the early summer than later in the season. Thus, during June, A. tonsa ingested between 9% and 23% of its body C d -L, and produced between 6% and 19% of its weight in eggs. In October, the copepod ingested 80-194% of its body weight in C d-~ but it produced only 1-5% of its body C in eggs. The range of Kt values exceeded that ob- served in the laboratory (0.094).49; Kiorboe et al. 1985; Kiorboe 1989) but was smaller than that ob- served in A. tonsa in Los Angeles Harbor (0.15- 2.10, mean = 0.80; Kleppel 1992). Within-station, between-experiment variability in K1 was greater than within-experiment, between-station variability.
Because, as suggested above, egg production was independent of temperature and food availability, the observed decrease in K~ through the summer, despite increased feeding activity, may be associat- ed with changes in food quality. However, the downward shift in K~ was not attributable to changes in plankton community structure; that is, we detected no systematic change in microplank- ton taxonomic composition over time. Nor did we observe significant temporal differences between the average proportions of microzooplankton in the diet over the summer. We did not, however,
measure nutritional parameters (e.g., proteins, lip- ids, etc.) in the seston during this study and cannot rule out the possibility that the nutritional value of the food supply changed. The nutritional compo- sition of protists is known to vary (J6nasd6ttir et al. 1995) and recent field studies and experimental manipulations have shown that variability in the fatty acid, sterol, and amino acid composition of the microplankton can affect the egg production rates of the copepods that feed on them (J6nas- d6ttir 1994; Ederington et al. 1995; Jbnasd6ttir et al. 1995; Kleppel and Burkart 1995; Kleppel et al. unpublished data).
There is also preliminary evidence that egg pro- duction by Acartia tonsa in Florida Bay may be af- fected by water quality. Recent trials of a chronic
toxicity assay using egg production by harpacticoid copepods as the test, revealed a significant sup- pression of egg production by extracts from sedi- ments obtained from the inner bay (Chandler and Green 1996; Chandler et al. unpublished data). The source of this toxicity is speculative, however, and further study is warranted.
We suggest that egg production may be simul- taneously enhanced and suppressed at Rankin Lake. While A. tonsa appears to derive significant nutrition from participation in a microbial food web, its egg production is lower than one would expect in a productive subtropical estuary. Given the intensity of human activity in the region around Florida Bay (Kleppel 1996), anthropogen- ically induced suppression of reproductive poten- tial seems reasonable. Florida Bay seems to exem- plify an ecosystem that is responding to multiple, natural and anthropogenic forcing functions. Dis- criminating the human source term for trophic stress from natural variation is not simple. Yet, ul- timately, the ability to do so seems crucial to the understanding of estuarine function in the face of increasing human modification of the ecosystem.
ACKNOWLEDGMENTS
We are gratefid to J. IIunt , director of the Depar tment of Environmental Protection ! .aboratory in Marathon, Florida, for making facilities available to us dur ing this study, and to the staff ot the Keys Marine Laboratory for their technical suppor t o f our sampling operat ions. We also thank B. Bendis for a-.sis- tance dur ing the exper iments and E Or tner of the National Oceanic and Atmospheric Administration Atlantic Oceano- graphic and Meteorological Lalx>ratory, Miami, Florida, to t data on copcpod abundances. This project was suppor ted by contract MR075 from the Florida Depar tment of Environmental Protec- tion, and by National Science Foundation grant OCE93-01534.
LITERATURE. CITED
AI I.EN, T. F. ANDJ. E KOONCE. 1973. Multivariate approaches to algal stratagems and tactics in systems analysis o f phytoplank- ton. Ecology 54:1234-1246.
AMBLER, J. w. 1985. Seasonal factors affecting egg product ion and variability of eggs of A cartia tonsa Dana from East Lagoon, Texas. Estuarine, Coastal and Shelf Science 20:743--760.
AMBLER, J. w. 1986. Effect o f food quantity and quality on egg product ion of Acartia tonsa Dana from East I,agoon, Galves- ton, Texas. Estuarine, Coastal and Shelf Science 23:18,3-196.
BARTRAM, W. 1980. Experimental deve lopment o f a model for the feeding of neritic copepods on phytoplankton. Journal of Plankton Research 3:25--51.
B~:F~gS, J. R., F. M. It . RIED, AND G. L. STEWART. 1980. Micro- plankton populat ion structure in southern California near- shore waters in late spring. Marine Biology 60:20.0,-226.
BELLA_\'IONI, D. C. AND W. T. PETER.SON. 1987. Temporal vari- ability in egg product ion rates of Acartia tonsa Dana in Long Island ~)und. Journal of Experimental Marine Biology and Ecology 107:199-208.
BoF.scri, D. F., N. E. ARMSI'RONG, C. ]7. D'ELIA, N. G..'~8_AYNARD, AND S. L. WII.I.IAMS. 1993. DeTerioration of the Florida Bay ecosystem: An evaluation of the scientific evidence. National Oceanic and Atmospheric Administration Coastal Ocean Pro- gram. Silver Springs, Maryland.
338 G.S. Kleppel et al.
C~,RIER, K. 1995. T h e egg produc t ion o f calanoid copepods in coastal waters o f Florida and its relat ion to the nutr i t ional env i ronmen t . Masters Thesis, Nova Southeas te rn University, Ft. Lauderdale , Florida.
CttANI)I.ER, (~,. T. AND A. S. GRFI'~N. 1996. A 14-day harpact icoid copepod reproduc t ion bioassay for laboratory and field con- t amina ted m u d d y sediments , p. 23-39. In G. K. Os t rander ted.) , Techn iques in Aquatic Toxicology, Lewis, Boca Raton.
DAGG, M. R. 1977. Some eft~:cts of patchy food env i ronmen t s on copepods . Limnology and Oceanography 22:99-107.
DURBIN, E. G., A. G. DURBIN, AND R. G. CAMPBH L. 1992. Body size and egg p roduc t ion in the mar ine copepod , Acartia hud- sonica, dur ing a winter-spring d ia tom b loom in N a r r a g a n ~ t t Bay. Limnology and Oc~eanography 37:342-360.
DURBtN, E. G., A. G. DURBtN, T. J. SMAYDA, AND P. G. VERITY. 1983. Food l imitation o f p roduc t ion by adul t Acartia tonsa in Narraganse t t Bay, R hode Island. Limnology and Oceanography 28:1199-1213.
EDI.~RINC, t'ON, M. C., G. B. MCMANt'S, AND H. R. IIARW:Y. 1995. Tropttic t ransfer of fatty acids. Limnology and Oceanography 40: 860-867.
ESTRADA, M. AND D. BLASCO. 1979. Two phases of the phyto- p lankton c o m m u n i t y in thc Baja upwelling. Limnology and Oceanography 24:1065-1080.
FRO,KI', B. W. 1972. EffecLs of the size and concen t ra t ion o f food particles on the feeding behavior o f the mar ine p lanktonic copepod Calanus pacificus. I.imnology and Oceanography 17:805- 825.
(;IFFORn, D.J . AND M. J. I)A(;t;. 1988. Feed ing o f the es tuar ine copepod Acartia tonsa Dana: Carnivory vs. herbivory in n a t m a l microp lankton assemblages. Bulletin of Marine Science 43:458- 468.
GUII.I~.RD, R. R. L. ANt)J. H. RYI'IIER. 1962. Studies o f mar ine p lanktonic diatoms. I. Cyclotella nana l lus ted t and Detomda confervacea (Cleve) Gran. Canadian JouD,al of Microbiology 8: 229-239.
IiEAD, E.J. II., L. R. HARRIS, AND C. ABOU DEBS. 1985. Eit~ct of daylength and food concen t ra t ion on in situ d iurna l feeding rhy thms in Arctic copepods . Marine Ecology Progress Series 24: 281-288.
IIuNrv:R, J. R. 1981. Feeding ecology and p reda t ion o f mar ine fish larvae, p. 33-80. In R. Lasker (cd.), Marine Fish Larvae, Mnrphology, Ecology and Relat ion to Fisheries. University o f Washington, Seattle, Waslt ington.
Ilt.NILEY, M. E. AND M. D. (;. LOPEZ. 1992. Tempera tu re -depen- den t p roduc t ion of mar ine copepods: A global synthesis. A nwrican Naturalist 140:210-242.
I'tqIRtAC, A, R. AND P,. C,. MrtCIIELL. 1986. Chroococcoid cyano- bacteria: A significant c o m p o n e n t in the food web dynamics o f the open sea. Marine Ecology Progre.gs Ser/es 28:291-297.
JONASDOrIIR, S. H. 1994. Effects of tood quality on the repro- dnctive success o f Acartia tonsa and Acartia hudsonica: l~abo- , 'atory observat ions. Marine Biology 121:67-81.
JtSNASDO'I'rIR, S. 11., D. FIEI.I)S, AND S. PANTOJA. 1995. C o p e p o d egg produc t ion in L ong Is land Sound, USA, as a funct ion o f the chemical composi t ion of the seston. Marine Ecology 15"ogress Ser/es 119:87-98.
KAtzlHGAN, S. K. 1991. Multivariate Statistical Analysis. A Con- cel>tual In t roduct ion . 2nd Edition, Radius, New York.
IQORBOF,, T. 1989. Pbytoplankton growth rate and n i t rogen con- tent: Implicat ions tor feed ing and fecundi ty ill a herbivorous copepod. Marine Ecology Progress Series 55:229-234.
KIORBOE, T., E MOtlI.ENBFR(;, AND K. HAMBt'RGER. 1985. Bioen- ergetics o f the p lanktonic copepod Acartia tonsa: Relation be- tween ti-eding, egg produc t ion and respiration, and compo- sition of dynamic action. Marine Ecology th'ogress X,'6~ 26:85- 97.
KIEPPEI,, (.;. S. 1992. Env i ronmenta l regulat ion o f feeding and
egg produc t ion by Acartia tonsa off s o n t h e r n California. Ma- rine B/o/ogy 112:57-65.
KLEPPFI., G. S. 1996. The state o f Florida's estuaries. Part 1. A synopsis of Florida's es tuar ine resources with r e c o m m e n d a - t ions for their conservat ion mad m a n a g e m e n t . TP-85, Florida Sea Grant Program, Gainesville, Florida.
KLEPPEL, G. S. AND C. A. BURKART. 1995. Egg produc t ion and the nutr i t ional e n v i r o n m e n t o f Acartia tonsa: The role o f food quality in copepod nutr i t ion, lCFSJournal of Marine Scienc~ 52: 297-304.
KI.EPPEI., G. S., C. A. BURKART, K. CARTER, AND C. TOMAS. 1996a. Diets o f calanoid copepods on the west Florida cont inen ta l shelf: Relat ionships between food concent ra t ion , food com- posit ion and fi:eding activity. Marine Biology 127:209-217.
KI,EPPEL. G. S., C. S. DAVIS, AND K. (~.RTER. 1996b. Tem p era tu r e and copepod growth in the sea: A c o l n m e n t on the temper- a t u r e -dependen t mode l o f Hunt ley and I.opez. American Nat- uralist 148:397-406.
KLEPPEL, G. S., D. V. HOI.I.IDAY, AN'I) R. E. PIEPER. 1991. Trophic interact ions between copepods and microplankton: A ques- tion about the role of diatoms. I.imnology and Oceanography 36: 172-178.
KI.EPPEI., G. S., R. E. PIEPFR, A.ND G. TRAGER. 1988. Variability ill the gatt con ten t s o f individual Acartia tonsa ti 'om waters off sou the rn California. Marine Biology 97:185-190.
KL~:PPEI., G. S., L. WILLBANKS, AND R. E. PIEPER. 1985. Diel vari- a t ion in body caro tenoid con ten t and feed ing activity in zoo- p lankton assemblages. Journal of Plankton Research 7:567-580.
KRINSKY, N. I. 1971. Funct ion, p. 669-716. In O. lsler ted.) , Ca- rotenoids. Burkhauser , Basel.
I_~NDRu M. R. 1983. The deve lopmen t of mar ine calanoid co- pepods with c o m m e n t on tile i sochronal rule. Limnology and Oceanography 24:614-624.
MARt:US, N. H. 1985. E n d o g e n o u s conu'ol o f spawning in a ma- rine copepod. Journal of Experimental Marine Biology and Ecology 91:263-269.
MARLY, V., M. E. ttt;NILVV, AND B. W. FRO,',-r. 1986. Measm' ing fi~eding rates of pelagic herbivores: Analysis o f exper imenta l des ign and methods . Marine Biology 93:49-58.
MILLr.R, C. B., J. K. JOHNSON, AND D. R. IIEINLE. 1977. Growth rules in the mar ine copepod genus Acartia. l,imnology and Oceanography 22:326--334.
NIVAL, P. ANt) NIVAI.. 1976. Particle re tent ion efficiencies o f the herbivorous copepod Acartia clausi (adult and copepodi te stages): Effects on grazing. Limnology and Oceanography 21:24- 38.
PAFFENHOFER, G.-A. 1984. Food ingest ion by the mar ine plank- tonic copepod l'aracaklnus in relation to a b u n d a n c e and size dis t r ibut ion o f food. Marine Biology 80:323-333.
PAFFENHGFER. G.-A. 1988. Feed ing rates and behaviors o f zoo- p lankton. Bulleti~ of Marine Science 43:430-445.
P t r r , M. AND D. K. STOECKFR. 1989. An exper imenta l ly deter- m ined carryon:volume ratio for mar ine "o l igot r ichous" till- ares f rom estuar ine and coastal waters. Limnology and Ocean- ography 34:1097-1103.
REEVE, M. R. 1964. Studies on the seasonal variation of the zoo- p lankton on a mar ine subtropical in-shore env i ronmen t . Bul- letin of Marine Science 14:103-122.
RFEW:, M. R. AND M. A. WALTER. 1977. Observa t ions on the exis tance o f lower th reshold and u p p e r critical food concen- trations for the copepod Acartia toT~ga Dana. Journal of Experi- nwntal Marine Biology and Ecology 29:211-221.
ROMAN, M. R. 1984. Utilization of detr i tus by Acartia tonsa. Lim- nology and Oceanography 29:949-959.
ROMAN, M. R., M. R. REEVE, ANDJ. L. FROG(;ERT. 1983. Carbon produc t ion and expor t f rom Biscayne Bay, Florida I. Tempo- ral pa t te rns in pr imary product ion , seston and zooplankton. Estuarine, Coastal and Shelf Sciences 17:4.r~59.
ROMAN, M. R. AND E RUBIIE. 1980. C o n t a i n m e n t effects in co-
pepod grazing experiments: A plea to end the black box ap- proach, l.imnology and Oceanography 25:982-990.
SA[z, E., A. (~I.BFI', 1. TREPAT, X. IRIGOIEN, AND M. AI.CARAZ. 1996. Food availability as a potential source of bias in the egg product ion me thod for copepods. Journal of Plankton Research 19:1-14.
SIIERR, F.. B. AND B. E SIIERR. 1987. High rates of consumpt ion of bacteria by pelagic ciliates. Nature, London 325:710-711.
SHERR, E. B., B. E SHERR, AND G.-A. PAFFENHfIFER. 1986. Pha- gotrophic protozoa as food for metazoans: A missing link in pelagic food webs. Marine Microbial t'bod Webs 1:60-80.
SIEBt'RTII, J. McN., V. SMETACEK, ANDJ. I.ENZ. 1978. Pelagic eco- system structure: Hetero t rophic compar tments and their re- lationship to plankton size fractions. Limnology and Oceanog- raphy 23:1256-1263.
STEAIL'qS, D. E. 1986. Copepod grazing behavior in simulated natural light and its relation to nocturnal feeding. Manne Ecol- ogy Progress S~ries 30:65-76.
STEARN'S, D. E., P. A. TF '̂-',TER, AND R. L. WAI.KER. 1989. Diel changes in the egg product ion rate of Acartia tonsa (Cope- poda, Calanoida) and related environmental factors in two estuaries. Marine Ecology l~'ogress Series 52:7-16.
STEIDINGER, K., W. RICHARDSON, E. "I'RUBY, R. BRAY, N. DIERSING, AND D. EAKEN. 1995. Microalgae of Florida Bay, p. 152-154. Florida Bay Science ( 'onference: A Report by Principal Inves- tigators. October 17-18, University of Florida, Sea Grant Pro- gram, Gainesville, Florida.
STOFCKER, D. K. &\'D J. M. CAPt:ZZO. 1990. Predation on proto- zoa: Its importance to zooplankton.Journal of Plankton Research 12:891-908.
STOECKF.R, I). K. AND D. A. EGLOFI-'. 1987. Predat ion by Acartia tonsa Dana on planktonic ciliates and rotifers. Journal of Ex- perinu,ntal Marine Biology and Ecology 110:53-68.
STOE(:KER, D. K. AND N. K. SANDERS. 1985. Differential grazing
Acartia tonsa Production in Florida Bay 339
by Acartia tonsa on a dinoflagellate and a tintinnid. Journal of Plankton Research 7:85-100.
STV, n l'rtMnr,'y, R. R. 1967. Estimating the organic carbon content of phytoplankton from cell w)lnme or plasma v()lume. Lim- nology and Oceanography 12:411-418.
SUI.LWAN, B. K. AND P.J. RITA(:(:O. 1985. The response of dom- inant copepod species to food limitation in a coastal mar ine ecosystem. Archiv fuer Hydrobiologte Beih. Ergebnisse der l.imnol- og/e 21:407-418.
TESTER, E A. AND J. T. TL'r~NF:R. 1990. How long does it take copepods to make eggs? Journal of Fxperimental Marine Biology and Ecology 141:169-182.
TOMAS, C. R. (i.D.,). 1993. Mm'ine Phytoplankton. A Guide to the Naked Flagellates and Coccoli thophorids. Academic, San Diego, California.
TOMAS, C. R. 1996. The role of nutr ients in initiating and sup- port ing Florida Bay microalgal blooms and primary produc- tion, p. 89-9. 1996 Florida Bay ~: ience Conference, Decem- ber 10-12, Key l.argo, Uifiversity of Florida, Sea Grant Pro- gram, Gainesville, Florida.
TUP,.','ER, J. T. 1984. Feeding ecology of some zooplankters that are prey items of larval fish. National Oceanic and Atmo- spheric Administration Technical Report NMFS 7:1-28.
WHI I E, J. R. A.','D M. R. ROMAN. 1992. Seasonal study of grazing by metazoan zooplankton in the mesohal ine Chesapeake bay. Marine Ecology t:u Series 86:251-261.
WOOI)MANSEE, R. A. 1958. The seasonal distribution of the zoo- plankton off Chicken Key in Bi~:ayne Bay, Florida. Ecology 39: 247-262.
ZIEMAN, J. C., J. w. FOt;RQURE.AN, A.\D R. L. IVFRSON. 1989. Dis- tribution, a lmndance and productivity of seagrasses and mi- croalgae in Florida Bay. Bulletin of Marine Science 44:292-311.
Submitted for consideration, January 3, 1997 Accepted for publication, September 2, 1997
