Estuaries
Vol. 21, No. 2, p. 347-360
June 1998
Relative Importance of Grazing and Nutrient Controls of Macroalgal Biomass in Three Temperate Shallow Estuaries JENNIFER HAUXWELL ]
JAMES McCI.EI.LAND P~:a'~:RJ. BFHR IVAN VALIEI A
Boston University Marine Program Marine Biological Laboratory Woods Hole, Massachusetts 02543 ABSTRACT: Macroalgal biomass and competitive interactions among primary producers in coastal ecosystems may be conU'olled by bottom-up processes such as nutrient supply and top-down processes such as grazing, as well as other environmental factors. To determine the relative importance of bottom-up and top-down processes under different nutrient loading conditions, we estimated potential amphipod and isopod grazer impact on a dominant macroalgal species in three estuaries in Waquoit Bay, Cape Cod, Massachusetts, that are subject to different nitrogen loading rates. We calculated growth increases and grazing losses in each estuary based on monthly benthic survey data of macrophyte biomass and herbivore abundance, field grazing rates of amphipods (Microdeutopus gryllotalpa and Cymadusa compta) and an isopod (Idotea baltica) on the preferred and most abundant macroalga (Cladophora vagabunda) and laboratory grazing rates for the remaining species, and in situ macroalgal growth rates. As nitrogen loading rates increased, macroalgal biomass increased (3x), eelgrass (Zostera marina) was lost, and herbivore abundance decreased (aAx). Grazing rates increased with relative size of grazer (I. baltica > C. compta > M. gry//otodpa) and, for two of the three species investigated, were faster on algae from the high-nitrogen estuary in comparison to the low-nitrogen estuary, paralleling the increased macroalgal tissue percent nitrogen with nitrogen load. Macroalgal growth rates increased (2• with increasing nitrogen loading rate. The comparison between estimated growth increases versus losses of C. vagabunda biomass to grazing suggested first, that grazers could lower macroalgal biomass in midsummer, but only in estuaries subject to lower niUrogen loads. Second, the impact of grazing decreased as nitrogen loading rate increased as a result of the increased macroalgal growth rates and biomass, plus the diminished abundance of grazers. This study suggests the relative impact of top-down and bottom-up controls on primary producers varies depending on rate of nitrogen loading, and specifically, that the impact of herbivory on macroalgal biomass decreases with increasing nitrogen load to estuaries.
Introduction Macroalgal biomass in coastal ecosystems may be controlled by bottom-up processes such as nutrient supply (Sand-Jensen and Borum 1991; Duarte 1995; Taylor et al. 1995; Valiela et al. 1997b) and top-down processes such as grazing (Leighton 1966; Lawrence 1975; Lubchenco 1978; Zimmerman et al. 1979; Steneck 1988; Bell 1991; Duffy and Hay 1991; Tegner and Dayton 1991; Geertz-Hansen et al. 1993), as well as other environmental factors. Coincident with worldwide increases in anthropogenic nitrogen loading to the coastal zone (Nixon 1995) has been the increasing appearance of macroalgal blooms accompanied by a decrease in macrophyte diversity (see examples in Valiela et al. 1997b). These dense canopies of macroalgae are composed of fast-growing, typically nutrientlimited taxa that in the presence of high nutrients are simply able to outcompete other producers,
such as seagrasses, that may be light-limited or unable to take advantage of increased water column nutrients (Duarte 1995; Valiela et al. 1997b). Nutrient limitation, particularly nitrogen, has been documented for several estuarine macroalgal species such as Ulva lactuca and Enteromorpha plumosa (Harlin and Thorne-Miller 1981) and Cladophora vagabunda and Gracilaria tikvahiae (Peckol et al.
1994). Grazers can also directly and indirectly affect macroalgae; the first-order effect of grazing, to decrease biomass of a preferred macroalgal species, ultimately alters competitive interactions within the community of producers (as does nutrient enrichment). Grazers can control biomass and diversity of macroalgal assemblages in a variety of marine habitats, including the rocky intertidal (Lubchenco 1978), kelp forests (Leighton 1966; Lawrence 1975; Tegner and Dayton 1991), coral reefs (Brawley and Adey 1981; Steneck 1988), and estuaries (Zimmerman et al. 1979; Geertz-Hansen et al. 1993), although relatively fewer grazing studies
1 Corresponding author; Tele: 508/289-7647; Fax: 508/5487295; e-mail:
[email protected]. 9 1998 Estuarine Research Federation
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have been conducted in temperate estuaries. Specifically, amphipod and isopod grazers can consume significant amounts of macroalgae under field conditions, although the extent to which they control macroalgal standing stocks has not been settled (Hay et al. 1987; Bell 1991; Duffy and Hay 1991). These crustacean grazers may actually enhance seagrass productivity in estuaries by consuming epiphytic macroalgae and microalgae (Zimmerman et al. 1979; Caine 1980; Howard 1982; Orth and van Monffrans 1984; Howard and Short 1986; Borum 1987; Neckles et al. 1993; Williams and Ruckelshaus 1993; Neckles et al. 1994; review byJernakoff et al. 1996). Several key studies have suggested that both bottom-up and top-down processes affect producer biomass and community structure (Hall et al. 1970; Young and Young 1978; Carpenter et al. 1985; Foreman 1985; McQueen et al. 1986; Duggins et al. 1989; Hunter and Price 1992; Kuparinen and Bjornsen 1992; Menge 1992; Geertz-Hansen et al. 1993; Williams and Ruckelshaus 1993; Foreman et al. 1995). The relative importance of the two types of controls, however, is not well documented or understood, particularly in estuarine ecosystems. Because nitrogen supply to estuarine ecosystems varies depending on land use patterns within adjoining watersheds (Valiela et al. 1992; Valiela et al. 1997a), as well as o t h e r factors, comparisons among different estuaries provide the opportunity to study not only the relative importance of grazing and nitrogen supply in controlling macroalgal biomass under pristine conditions, but also whether the importance of top-down and bottom-up controls changes in relation to nitrogen loading. Within estuarine ecosystems, very few studies have actually examined the impact of herbivory on a specific population of macrophytes under a gradient of productivity or nutrient load. Geertz-Hansen et al. (1993) provide some evidence that grazing pressure by invertebrates, mainly isopods of the genus Idotea, differed between two sites in a Danish estuary subjected to different nutrient loading rates. While grazing seemed to control biomass stocks at a site with a relatively low nutrient supply, reduced grazing pressure allowed accumulation of the macroalgae Ulva lactuca at the more eutrophic site. The reduction in grazing pressure at this site was attributed to presumed lower densities of grazers rather than faster growth, but it is difficult to predict patterns emerging along a gradient of nutrient loading from their studies. No study has been conducted that examines the main parameters affecting grazing pressure under a range of nutrient loading regimes in estuaries. We measured nitrogen loading rates from watersheds to estuaries, macroalgal biomass, macroalgal
TABI,E 1. Nitrogen loading rates (based on [NO~-] of groundwater entering the seepage face and recharge values), average depths, open water area, average temperatures in July 1997 (J. Tober unpublished data), and fresh water residence times in three estuaries of Waquoit Bay (Waquoit Bay Land Margin Ecosystems Research project unpublished data). l'~tuary
Nitrogen loading rate (kg N ha -~ y-l) Depth (m) Open water area (ha) Temperature (~ Residence time (d)
624 1.1 13 24 - 1.1
520 0.5 19 22 0.3
64 ().9 13 23 2.2
growth rates and nitrogen content, herbivore abundances, and grazing rates in estuaries as components that affect grazing pressure in natural systems. Basically, we expected that in response to increased nutrients, macrophyte production would increase (Lapointe and Duke 1984; Peckol et al. 1994) as well as tissue %N (Lapointe and Duke 1984; Yates and Peckol 1993; Galen et al. 1996). Herbivores are nitrogen limited (Mattson 1980; Vince et al. 1981; Galen et al. 1996), and may have responded in a number of ways to increased quality of food, including functional and numerical responses, unless the resulting differences in habitat structure changed physical factors (oxygen depletion) or predator relationships. T H E WAQUOIT BAY SUBWATERSIIEDS AND ESTUARIES
To determine the relative importance of topdown and bottom-up processes under different nutrient loading conditions, we investigated amphipod and isopod grazer impact on a dominant macroalgal species in three estuaries (similar in depth, open water area, temperature, and short residence times) subject to relatively high (Childs River), intermediate (Quashnet River), or low (Sage Lot Pond) nitrogen loading rates (Table 1) in Waquoit Bay, Cape Cod, Massachusetts (Waquoit Bay Land Margin Ecosystems Research project unpublished data; Valiela et al. 1992; Valiela et al. 1997a). Since the 1930s, the subwatersheds of Waquoit Bay have undergone different degrees of urbanization and consequently provide receiving estuaries with different loads of anthropogenic nitrogen (i.e., wastewater and fertilizer) (Valiela et al. 1992) (Table 1, total --10• difference in nitrogen loading rate among estuaries). Increases in nitrogen loading from the relatively developed subwatersheds have significantly altered the receiving estuarine ecosystems, beginning with changes in the primary producers. Waquoit Bay and its estuaries were historically dominated by eelgrass (Zostera marina), but analysis of aerial photographs taken be-
Grazing and Nutrient Controls of Macroalgae
tween 1987 and 1992 revealed a rapid temporal decline in eelgrass in estuaries adjoining relatively urbanized subwatersheds (Short and Burdick 1996). This loss is also apparent in studies using a "space-for-time substitution" (Pickett 1989): macrophyte biomass surveys in five estuaries of Waquoit Bay subject to different nitrogen loading rates showed that macroalgal biomass (mainly C/adophora vagabunda and Gracilaria tikvahiae) increased linearly with nitrogen load to estuaries, while eelgrass decreased exponentially (Lyons et al. 1995). The resulting change in habitat, from seagrass to macroalgae, has altered the abundance and composition of benthic fauna (Valiela et al. 1992), including the conceivable loss of commercially important juvenile fish and shellfish that use eelgrass beds as nurseries (Eckman 1987; Bricelj et al. 1991; Valiela et al. 1992). Bottom-up control of macroalgae is clearly established in Waquoit Bay (Valiela et al. 1992; Peckol et al. 1994; Hersh 1995), but there is circumstantial evidence that grazers (amphipods and isopods that may reach densities greater than 4,000 individuals m -z) may also play a substantial role in control of macroalgae. Seaweed productivity in Waquoit Bay estuaries generally increases in the s u m m e r months. In 1991 field measurements, macroalgal growth rates (at the very least in the low-nitrogen estuary) doubled between March and September (Peckol et al. 1994). In the absence of grazing, therefore, we would expect that macroalgal biomass would increase throughout the summer, or eventually peak at the point at which seaweed selfshading occurred (Dodds and Gudder 1992; Hersh 1995). Biomass surveys, however, indicated no net seasonal increases in the summers of 1991 or 1992 (Hersh 1995), and recent survey data suggest midsummer decreases in macroalgal biomass in the summers of 1994 and 1995 (J. McClelland unpublished data). RFSEARCH APPROACH
In this paper we test the hypotheses that herbivory accounts for a significant amount of the "missing" midsummer seaweed biomass in Waquoit Bay estuaries, and that the impact of grazing on macroalgal biomass differs in estuaries exposed to different nitrogen loading rates. To assess the importance of grazing, we made model estimates of grazer impact on macroalgal biomass in the high-, mid-, and low-nitrogen estuaries (Table 1) by comparing consumption of macroalgae by extant grazers versus growth of extant macroalgae during two summers. The most straightforward approach to assess the importance of grazing would be to conduct a field experiment in which we compare macroalgal bio-
;349
mass differences between plots in each estuary that either included or excluded grazers. The mesh size required to exclude amphipods, however, would be so small as to significantly shade macrophytes and slow water circulation, conditions that would unquestionably add artifacts to the results. We chose an alternative approach in which we used field and laboratory data to model grazer impact. A similar manipulation was used by Nicotri (1977), who multiplied grazing rates by grazer densities to estimate the overall impact of herbivores on cultured seaweed populations, and by Nienhuis and Groenendijk (1986), who multiplied grazing rates of isopods and consumption estimates of birds by field densities to determine the percentage of annual seagrass production consumed in a marine lagoon. To obtain the data necessary for the model calculation, we first collected benthic survey data to quantify biomass of macrophytes and abundance of grazers and determine species composition of producers and grazers in the three estuaries. Second, we measured field grazing rates in each estuary by three abundant species on the preferred and most abundant macroalgal species, and also assessed nutritional differences in this alga from nitrogen-enriched versus pristine estuaries. We then used these data in addition to macroalgal growth rates (Peckol et al. 1994) to calculate grazing losses and growth increases of macroalgal biomass in each estuary and compared our estimates of macroalgal net production to independent estimates. Lastly, we compared the importance of grazing and nitrogen load among the three estuaries as controls of benthic primary production and diversity. Materials and M e t h o d s f o r M o d e l Parameters SAMPI.ING MACROPItYFE BIOMASS AND GRAZER ABUNDANCE
To evaluate macrophyte biomass (above-ground for seagrasses) and abundance of grazer species in each estuary, we conducted monthly surveys from June to October in 1994 and from April to October in 1995. The average depth of the estuaries is similar (Table 1), but since depth varied within estuaries, the sampling design (Hersh 1995) was stratified to collect representative samples for shallow, intermediate, and deeper locations. The average depth of each estuary was equal to the average sampling depths. Benthic samples were collected from 10 sites in each estuary using a 15 cm • 15 cm Ekman grab attached to a 2-m pole. The samples were rinsed on a 1-mm mesh sieve and sorted into macrophyte and faunal taxa; macrophytes were dried at 60~ and weighed, and grazers were separated by species and counted. We uscd two-way
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analysis o f variance (ANOVA factors: estuary, time) to d e t e r m i n e differences in m a c r o p h y t e biomass and herbivore a b u n d a n c e a m o n g estuaries and assess seasonal trends. One-way analysis o f variance (ANOVA factor: time) was used in cases where species were f o u n d only in o n e estuary to assess differences in biomass over time. We r e p o r t e d p-values only when effects o f estuary or time were significant. FIELD GRAZINGRATE EXPERIMENT
Feeding rates by the a m p h i p o d s Microdeutopus gryllotalpa and Cymadusa compta and the isopod Idotea baltica on the macroalga Cladophora vagabunda were assessed in field cage e x p e r i m e n t s during July and August 1993 and S e p t e m b e r 1994. We chose to use C. vagabunda as the f o o d item for several reasons: One, it was a b u n d a n t in each estuary (Valiela et al. 1992; Peckol et al. 1994; H e r s h 1995) and was the species that in fact exhibited the largest decline in macroalgal biomass in the high-nitrogen estuary during the summers o f 1994 and 1995 (J. McClelland u n p u b l i s h e d data). Two, previous laboratory (Heckscher et al. 1996) and field choice experiments (Martinez et al. 1995) indicated that it was preferentially inhabited by M. gryUotalpa over G. tikvahiae. T h r e e , preferential c o n s u m p t i o n o f C. vagabunda over G. tikvahiae has b e e n r e c o r d e d in laboratory feeding e x p e r i m e n t s in which M. gryllotalpa were simultaneously p r e s e n t e d with both species (J. Joy u n p u b l i s h e d data). O t h e r grazers (the isop o d Erichsonella filiformis and the a m p h i p o d Lysianopsis alba) also p r e f e r r e d C. vagabunda in these experiments. Four, stable c a r b o n and nitrogen isotopic studies indicated that C. vagabunda is a principal source o f carbon and nitrogen for all grazer species that were investigated, including M. gryllotalpa, C. compta, the a m p h i p o d Gammarus mucronatus, and the isopod Erichsonella filiformis (McClelland and Valiela in press). We selected Microdeutopus gryUotalpa for this study because it was the most a b u n d a n t grazer species in all three estuaries (Martinez et al. 1995; J. Hauxwell u n p u b l i s h e d data). It is, however, a relatively small species ( < 1 0 m m in length). To consider larger grazers in o u r calculation, we measured grazing rates by Cymadusa compta and Idotea baltica, two species that were also c o m m o n l y f o u n d in Waquoit Bay d u r i n g the study period, as midsize (up to 15 mm) and large-size (up to 20 mm) grazers. Each e x p e r i m e n t a l unit consisted o f four cages m a d e o f 9 cm • 9 cm • 9 cm plastic containers with the sides and top covered by 500-p,m mesh.
This design allowed sufficient flow between the cage and a m b i e n t water. Each cage was attached to the corners o f an a l u m i n u m wire 30 cm • 30 cm frame that was s u s p e n d e d 15 cm above the algal canopy (to avoid hypoxic conditions) by a n c h o r i n g corners to a c e m e n t brick b u r i e d in the m u d and buoying with a float. T h r e e replicate frames, each with four cages, were placed 8 m apart at depths o f 1 m in salinities between 28%0 a n d 30%o in the high-, mid-, and low-nitrogen estuaries. T h e contents o f each cage consisted o f 500 m g (blotted wet weight) o f Cladophora vagabunda that were collected f r o m each estuary, sorted to remove grazers, and rinsed with filtered seawater to remove debris. O n e cage served as a grazer-free control t h a t gave e s t i m a t e s o f m a c r o a l g a l w e i g h t changes in the absence o f consumers. Fifteen Microdeutopus gryUotalpa were a d d e d to o n e experimental cage, 10 Cymadusa compta to another, and 5 Idotea baltica to the last. Densities o f grazers in cages were c o m p a r a b l e to those in previous laboratory (J. Joy u n p u b l i s h e d data) and field experiments (Brawley and Fei 1987). C. vagabunda used were indigenous to the specific estuary in which the e x p e r i m e n t was run. T h e grazers M. gryUotalpa and C. compta were indigenous to the estuary in which they were placed. Because o f insufficient n u m b e r s in the high-nitrogen a n d mid-nitrogen estuaries, all L baltica were collected f r o m the lownitrogen estuary. Each e x p e r i m e n t (seven total) ran in the field for 4 d, after which time the grazers were separated from the algae and c o u n t e d , wet weights o f C/adophora vagabunda were r e c o r d e d , and the algae were dried at 60~ To express grazing rates on a dry weight basis (for application in m o d e l calculations), initial algal wet weights were c o n v e r t e d to dry weights using a conversion factor (2.5) determ i n e d f r o m differences between final wet and dry measurements. Grazing rates per individual grazer per day were calculated by subtracting the final wet weight f r o m the initial wet weight, adding the growth o f macroalgae f r o m the control cage for that replicate, and dividing by the n u m b e r o f e x p e r i m e n t a l days as well as by the n u m b e r o f grazers in that cage. Calculated grazing rates r e p r e s e n t total loss o f prod u c e r biomass over 1 d. We used one-way analysis o f variance (ANOVA) to d e t e r m i n e significant differences a m o n g grazing rates by different grazer species and on algae f r o m different estuaries. Twoway ANOVAs (factors: estuary, time) were used to d e t e r m i n e differences in algal growth rates in control cages in different estuaries over time. Regression analysis (using l o g - t r a n s f o r m e d a v e r a g e growth rates f r o m control cages or actual grazing rates for each species in each estuary) was used to
Grazing and Nutrient Controls of Macroalgae
9
TOTAL MACROALGAE
400]
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~
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[] MidN estuary
C. vagabunda
G. tikvahiae
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351
erage, composed 40--80% of total macroalgal biomass (Fig. 1, second panel). Gracilaria tikvahiae made up 20-50% of total macroalgal biomass and did not show a seasonal pattern (Fig. 1, third panel). The only seagrass, Zosteramarina, grew during spring, peaked in early August, and decreased thereafter (time: F -- 3, df = 11, p = 0.0013). Overall, seasonal patterns and macrophyte biomass were similar between the 2 yr. The lack of a summer increase in macroalgal biomass, rather an overall decrease in the high-nitrogen estuary (Fig. 1, top), is counter to what we expected based on increased macroalgal summer growth rates (Peckol et al. 1994). What remained to be assessed was whether grazing could account for the difference between expected versus measured macroalgal biomass.
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1994
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1995
Fig. 1. Comparison of lnonthly 1994 and 1995 s u m m e r biomass (g dry weight in '2) o f total macroalgae, C l a d o p l m r a vagaand Z o s t e r a m a r i n a in the high-, mid-, bunda, Gracilaria tikvahiae, and low-nitrogen estuaries (mean _-.-SE).
determine if there was a relationship between algal growth rate and nitrogen load or grazing rate and nitrogen load. To compare relative food quality of Cladephora vagalmnda indigenous to each of the high, mid, and low N estuaries, we measured % carbon and nitrogen. C. vagabunda were collected from each estuary in September 1994, cleaned of animals and debris, and rinsed with fresh water. Algae were dried at 60~ in a drying oven for 24 h and then ground to a fine powder with a mortar and pestle. Five replicate samples from each estuary were analyzed on a model 2400 Perkin Elmer CHN Analyzer. Results and D i s c u s s i o n o f M o d e l Parameters M.ACROPH~TE BIOMASS
Macrophyte biomass varied depending on season, species of macrophyte, and estuary of origin (Fig. 1). Total macroalgal biomass (Fig. 1, top) was highest in late spring or early summer, and decreased through the warmer months (except at the mid-nitrogen estuary in 1995), mainly following the pattern of Cladophoravagabunclawhich, on av-
The biomass of most macrophyte species was strongly affected by estuary of origin (Fig. 1), which we interpret as the effect of different rates of nitrogen loading. Total macroalgal biomass, again owing largely to the response of Cladophora vagabunda (estuary: F = 16, df = 2, 11, p = 0.0001), was highest in the estuary subject to the highest nitrogen loading rate (estuary: F = 16, df = 2, 11, p = 0.0001) (on average, 3• that of the mid or low-nitrogen estuaries) (Fig. 1, top and second panels). Gracilariatikvahiaedid not respond to nitrogen loading rate (Fig. 1, third panel), but Zostera marina was eradicated in estuaries subject to increased nitrogen loads (Fig. 1, bottom panel). The differences we found in overall biomass and taxonomic composition of benthic primary producers among estuaries of Waquoit Bay with high, mid, and low nitrogen loading (Fig. 1) corroborate those found in past surveys (Valiela et al. 1992; Hersh 1995; Lyons et al. 1995) where macrobenthic production shifts from eelgrass- to macroalgaldominated with increased nitrogen loads (Valiela et al. 1997b). The concomitant loss of eelgrass meadows with eutrophication has been widely documented in estuaries in New England (Valiela et al. 1992; Short et al. 1993). Laboratory and mesocosm experiments demonstrated that the likelihood of shading via increased phytoplankton, increased macroalgal or microalgal epiphytes, and overgrowth of unattached benthic macroalgae increases with fertilization (Short and Burdick 1996; Short et al. 1995; Short et al. 1993; Harlin and Thorne-Miller 1981). The potential contribution by each of these agents of shading has been documented in the relatively high nitrogen-loaded estuaries of Waquoit Bay. Valiela et al. (1992) showed that phytoplankton abundance increased with nitrogen load in the same three estuaries of Waquoit Bay. Wright et al. (1995) measured epiphyte accumulation in estuaries of
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J. Hauxwoll et al.
TABLE 2. Species and relative summer abundances of small crustacean grazers found in the Waquoit Bay estuaries. Rare refer tu > 0--10, Common > 10-100, and Numerous > 100 average individuals m -z from benthic surveys in summers 1994 and 1995. Estuary Grazer
High
Nitrogen
Low
Nitrogen
Numerous -Common Common Rare --
Numerous -Common Common Common Rare
Numerous ' Numerous Common Common Common Common
Isopods ErichsoneUafiliformis Edotea triloba Idotea baltica
Common Rare --
Common Common --
Common Rare Rare
5000- TO'T/~,L GRAZERS . t~
HighN estuary
m
Mid N estuary Low N estuary_~
~ 3000-
lO00//
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i
i
9
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,
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I
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,
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~
Nitrogen
Amphipods Microdeutopus gryllotalpa Ampithoe longimana Cymadusa compta Lysianopsis alba Gammarus mucronatus Elasnurpus levis
Waquoit Bay still containing eelgrass meadows and suggested that the rate o f epiphyte accumulation increased with nitrogen load. T h e increase in benthic macroalgal biomass with nitrogen load is app a r e n t in Fig. 1 and has b e e n d o c u m e n t e d in several o t h e r studies (Valiela et al. 1992; H e r s h 1995; Lyons et al. 1995). Most likely, the c o m b i n e d effect o f shading by these three types o f algal p r o d u c e r s
.~
Mid
5000.
M. gryllotalpa
< 3000
1000, ! M J J AS
1994
0
AMJ
J A SmO '
1995
Fig. 2. Comparison of monthly 1994 and 1995 summer grazer abundance (no. individuals in ~-'-')in the high-, mid-, and lownitrogen estuaries. The total of all amphipod and isopod grazers (listed in Table 2) is shown in the top panel, and number of the amphipod Microdeutopus gryllotalpa is shown in the bottom panel (mean -+ SE).
is an i m p o r t a n t cause o f eelgrass decline in Waquoit Bay a n d its estuaries. HERBIVORE ABUNDANCE
Nine major taxa o f herbivorous a m p h i p o d s and isopods were f o u n d in the Waquoit Bay estuaries (Table 2). T h e c o m b i n e d a b u n d a n c e s of these grazers (Fig. 2, top) were highest in the low N estuary. O n average, there were 2 x m o r e grazers in the low-nitrogen estuary than in the mid-nitrogen estuary, and 4• m o r e than in the high-nitrogen estuary (estuary: F = 21; d f = 2, 11; p = 0.0001). Seasonal patterns were a p p a r e n t in each estuary for b o t h summers, with grazer a b u n d a n c e s peaking between early July and early August (time: F = 8; d f = 2, 11; p = 0.0001), c o i n c i d e n t with the p e r i o d when macroalgal biomass was e x p e c t e d to increase, but in fact, did n o t (Fig. 1, top). T h e r e was a significant estuary x time interaction (F = 2; df = 2, 11; p < 0.004), indicating that temporal patterns of a b u n d a n c e were offset a m o n g estuaries. Peaks in grazer a b u n d a n c e were h i g h e r in 1994 than in 1995 for low and high-nitrogen estuaries. T h e a m p h i p o d Microdeutopus gryllotalpa was o n average the most a b u n d a n t species o f grazer in each estuary (Table 2 a n d Fig. 2, bottom) a n d comprised 53-61% of the m e a n n u m b e r o f total grazers f o u n d in each estuary (Fig. 2, top). M. gryllotalpa a b u n d a n c e s showed analogous differences a m o n g estuaries (estuary: F = 12, d f = 2, 11, p = 0.0001) and seasons (time: F = 7, d f = 2, 11, p = 0.0001) as total grazer abundances. T h e only o t h e r species that was n u m e r o u s was the a m p h i p o d Ampithoe longimana, b u t its greatest a b u n d a n c e was only for o n e survey (August 1) in o n e estuary (low nitrogen) in 1994 and 1995 (Table 2 and Fig. 2, n o t e difference between top and b o t t o m panels). T h e isopod Idotea baltica was n u m e r o u s (385 -+ 75) in the low-nitrogen estuary in preliminary surveys c o n d u c t e d July 1993 (J. Hauxwell u n p u b l i s h e d
Grazing and Nutrient Controls of Macroalgae
data), but it was rare or absent in samples collected during the summers of 1994 and 1995 (Table 2). The differences in overall abundances of grazers (Fig. 2) and grazer species (Table 2) among estuaries may be linked to indirect a n d / o r direct effects of nitrogen loading. As nitrogen load increases, hypoxic events b e c o m e m o r e f r e q u e n t (D'Avanzo and Kremer 1994), which may deplete abundance of grazers. In addition, although the height of macroalgal canopies increases with loading rate (Peckol and Rivers 1996), this does not necessarily mean that there is more habitat available for grazers. Only the upper 6-10 cm of macroalgal canopies (which corresponds to 260 g m -2) might be available to grazers, because the canopy is often anoxic below this depth (Waquoit Bay Land Margin Ecosystem Research project unpublished data). Differences in community structure among estuaries (eelgrass-dominated versus macroalgal-dominated) may also influence amphipod and isopod abundances due to differences in the type and abundance of available food items and the ability of grazers to avoid predation in habitats with different types and amount of vegetative cover (Young et al. 1976; Young and Young 1978; Nelson 1979a, b; Stoner 1980; Nelson 1981; Holmlund et al. 1990). FIELD GRAZING RATE EXPERIMENT
Algal Weight Changes in Cages Cladophora vagabunda weight changes (final minus initial) in the grazer-free control cages showed that the algae grew during our experiments, except at the low-nitrogen estuary in late July 1993, and in the mid and low-nitrogen estuaries in late September 1994 (Fig. 3, top panel). Differences in growth rate were apparent among estuaries (estuary: F = 87, df = 2, 6, p < 0.0001) and correspond to nitrogen load (regression analysis after log-transformation: F = 115840, p < 0.0023, r = 1.0); macroalgae from the high-nitrogen estuary grew fastest (5.4 -+ 0.4% d ~), followed by macroalgae from the mid-nitrogen estuary (2.6 +- 0.4% d 1) and lownitrogen estuary (0.1 -+ 0.7% d-l), respectively. Peckol et al. (1994) also observed differences (23• between the high and low-nitrogen estuaries in their growth experiments. Physiological differences between macroalgae indigenous to the highnitrogen estuary versus the low-nitrogen estuary, such as faster nitrogen uptake rates and higher photosynthetic rates of high-nitrogen estuary C. vagabunda (Valiela et al. 1992), translate into differences in production rates between the two estuaries. C. vagabunda growth in our cages also varied significantly with time (time: F = 13, df = 2, 6, p < 0.0001), and there was a significant estuary •
9
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Fig. 3. Cladophora vagatmnda weight change (mg dry weight d -j) ill the grazing rate experiment control cages (containing only algae) and treatment cages (containing either approximately 15 Microdeutopusgryllotalpa, 10 Cymadusa compta, or 5 Idotea baltica individuals) (mean _+ SE).
time interaction (F = 7, df = 2, 6, p < 0.0001), indicating differences in temporal patterns of growth among estuaries. Cages containing grazers had lower average macroalgal weight changes in relation to control cages containing only algae, indicating that measurable grazing occurred (Fig. 3, all panels). In late July, average weight change in Cladophoravagabunda in cages containing Microdeutopusgryllotalpawere similar to those in the control. In almost all cases, however, grazer impact on the growing parcel of macroalgae was least for the high-nitrogen estuary. This effect was mainly the result of increased algal growth, rather than consumption by grazers, as we explain below.
Grazing Rates Grazing rates (calculated from data in Fig. 3) varied depending on grazer species and nitrogen loading rate to the estuary (Fig. 4). Differences Among Grazer Species. Grazing rate increased with grazer size (Fig. 4) (F = 113, df = 1, p < 0.0001); Microdeutopusgryllotalpa, the smallest
354
J. Hauxwell el al.
9
M. gryllotalpa
9
C. compta
*
1. baltica
TABLE 3. Comparison of nutritional composition of Cladophora vagalmnda (mean _+ SE) in three estuaries of Waquoit Bay. 1989-1992 data are averages from monthly collections (adapted from Peckol et al. 1994). Estuary
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Nitrogen loading rate (kg N-ha-1 9y-l) Fig. 4. Comparison of grazing rates (mg dry weight individual -1 d 1) of Microdeutopus gryllotalpa, Cymadusa compta, and ldotea baltica on Cladophova vagabunda versus nitrogen loading rate (kg N ha -~ yr l). Points represent averages of measurements taken between July 1993 and September 1994 (+SE). Best-fit lines are shown for each species along nitrogen loading rates.
grazer, had the slowest average grazing rate while Idotea baltica, the largest, grazed fastest (Fig. 4) as indicated by comparing y-intercepts and slopes of the best-fit lines. The average grazing rate of L baltica in our experiment (7.3 mg ww individual 1 d -1) (adapted from Fig. 4) is within the range of those measured by Nicotri (1980) on several different macroalgal species (0.2-8.1 mg ww individual- 1 d 1). N Loading Rate to Estuary. The average percent nitrogen of Cladophora vagabunda was highest in the high-nitrogen estuary and lowest in the lownitrogen estuary, with a 1% absolute difference (Table 3). Peckol et al. (1994) also observed significantly higher tissue nitrogen for C. vagabunda from the high-nitrogen estuary than from the lownitrogen estuary during all seasons (Table 3). Because the percent carbon of C. vagabunda from the high-nitrogen estuary was similar to that in the lownitrogen estuary, there was a lower C:N in the highnitrogen estuary than in the low-nitrogen estuary. Increased nitrogen c o n t e n t of macroalgae is one of the features that increases quality of food for herbivores (Mattson 1980). Since macroalgal tissues in the high-nitrogen estuary are enriched in nitrogen relative to the lownitrogen estuary (Table 3), we also expected grazing rates to vary with estuary. Idotea baltica (ANOVA: F = 34, df = 1, p < 0.0001) (regression analysis: F = 170, p < 0.05, r = 0.997) and Cymadusa
11igh Nitrogen
Mid Nitrogen
Low Nitrogen
September 1994 Percent carbon Percent nitrogen C:N
27.5 +_ 1.4 3.0 -+ 0.3 11.0 +- 0.7
23.5 -+ 1.2 2.8 _+ 0.2 9.9 _+ 0.2
27.3 _+ 0.4 2.0 +_ 0.1 16.4 -+ 1.2
1989-1992 Percent nitrogen
3.9
3.1
compta (ANOVA: F = 28, df = 1, p < 0.0001) (regression analysis: F = 27, p = 0.12, r = 0.979) (2• in both cases) had significantly faster m e a n grazing rates on Cladophora vagabunda from the high-nitrogen estuary than from the low-nitrogen estuary, alt h o u g h the grazing rate of Microdeutopus gryUotalpa did n o t vary significantly a m o n g estuaries (Fig. 4). In our cages containing L baltica and C. compta, these differences in grazing rates a m o n g estuaries were overwhelmed by the even larger differences in C. vagabunda growth rate (Fig. 3, top); even though grazing rates were fastest on high N algae (Fig. 4), losses of C. vagabunda were least in the high-nitrogen estuary (Fig. 3, third and bottom panels). Nicotri (1980) also f o u n d that herbivores fed faster on preferred food items, so that feeding rate could be a proxy for preference. Similarly, in other feeding choice experiments using Fucus vesiculosis from the high versus the low-nitrogen estuaries of Waquoit Bay, the snail Littorina littorea selectively grazed algae from the high-nitrogen estuary (Yates and Peckol 1993); F. vesiculosis from the high-nitrogen estuary had consistently higher tissue nitrogen and lower polyphenolic concentration (feeding-deterrent) than the low-nitrogen estuary over a year (1990-1991).
Methods for Predicting Grazer Impact and Verifying Macroalgal Production Estimates PREDICTING GRAZER IMPACT ON SUMMER MACRO~LGAL BIOMASS
To estimate the effect grazers may have on macroalgal biomass over the s u m m e r m o n t h s a n d compare the relative impact of grazers a m o n g the different estuaries, we m o d e l e d the a m o u n t of C/adophora vagabunda that grew a n d the a m o u n t that was grazed (all in g m -2 d -1) in each estuary. We calculated growth increases by multiplying macroalgal growth rates (in g C. vagabunda grown per g C. vagabunda d J) by macroalgal biomass (in g C. vagabunda m -2) in each estuary. Grazing losses were calculated by multiplying grazing rates (in g C. vagabunda consumed individual -x d 1) by grazer
:355
Grazing and Nutrient Controls of Macroalgae
abundances (in individual m-2) in each estuary. Growth and grazing rates were applied to 1994 and 1995 survey data (Figs. 1 and 2) to estimate growth increases and grazing losses that occurred during each month of those summers. The following sections explain in more detail how these values were calculated.
DUE TO GROWTH 12~
To model macroalgal growth in the field, we adapted data obtained in field experiments by Peckol et al. (1994) in which fronds of Cladophora vagabunda were tethered above and within the macroalgal canopy in both the high and low-nitrogen estuaries of Waquoit Bay. Fronds above and within the canopy are exposed to different light regimes and grow at different rates representative of macroalgae on the top layer of a canopy versus macroalgae within the canopy itself. Since depth of canopy varied among estuaries and months, we had to consider how differences in canopy depth affected growth rates. Algal biomass beneath a threshold canopy depth is not photosynthetically active due to self-shading. We therefore calculated average canopy depth in each estuary for each month of the summer by using a regression between C. vagabunda biomass and canopy thickness reported by Peckol and Rivers (1996). By assuming that biomass of algae is distributed evenly with canopy depth, we calculated the biomass of algae 0-1 cm and 1-3 cm deep into the canopy. Below 3 cm, the photosynthetic rate of algae is 0 (Peckol and Rivers 1996), so these fronds are not growing. Canopy depths greater than 1 cm existed only in the high nitrogen estuary and were present June through August in 1994 and April through August in 1995. Summer measurements (see Peckol et al. 1994) were averaged to obtain above-canopy and within-canopy growth rates in high (above mat: 8.3 -+ 1.2% d-i; within mat: 5.0 -+ 0.6% d -l) and low N (above mat: 3.8 -+ 0.7% d l; within mat: 2.7 +0.3% d 1) estuaries. The biomass of algae 0-1 cm deep was multiplied by above-canopy growth rates and 1-3 cm deep by within-canopy growth rates. The growth data of Peckol et al. (1994) were reported only for the high- and low-nitrogen estuaries. To estimate Cladophora vagabunda growth rates in the mid-nitrogen estuary, we examined the relationship between average growth rates in the control cages of our field grazing rate experiment and nitrogen loading rate and found it to be exponential (regression analysis after log-transformation: F = 115840, p < 0.0023, r = 1.0). We therefore calculated mid nitrogen above-canopy (6.6 % d 1) and within-canopy (4.8% d l ) growth rates by using an exponential interpolation of
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Fig. 5. Estimated change in Cladophora vagabunda biomass (g dry weight m -2 d l) due to growth o f extant algae (top) and to grazing by all extant grazers (middle) and extant populations of Microdeutopus gryllotalpa (bottom panel) during s u m m e r s 1994 and 1995 in high, mid, and low-nitrogen estuaries (-+propagated SE).
above-canopy or within-canopy rates across nitrogen loading rates (Peckol et al. 1994).
Grazing Loss We estimated the amount of Cladophora vagabunda c o n s u m e d (in the absence of macroalgal growth) by Microdeutopus gryllotalpa alone, and also by all grazer species combined (Fig. 5, bottom and middle). To estimate grazer impact by the populations of M. gryllotalpa (Fig. 5, bottom), we multiplied M. gryllotalpa grazing rates by M. gryllotalpa monthly mean abundances (Fig. 2) in each estuary. To estimate the impact of the total amphipod and isopod grazing community on C. vagabunda biomass in each estuary, we multiplied the monthly abundance of each grazer species by its grazing rate (Fig. 5, middle). For M. gryllotalpa, Cymadusa compta, and Idotea baltica, we used the grazing rates measured in our field experiment. We only measured grazing rates of three species in our field experiment but have previously measured grazing rates of additional grazer species on Cladophora vagabunda from the high-nitrogen and
356
J. Hauxwell et al.
"FABLE 4. Grazing rates (mg dry weight individual-l d -l) of three amphipod and two isopod species on Cladophoravagabunda from the high and low-nitrogen estuaries measured in laboratory experiments (mean -+ SE).
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0.5 0.6 0.8 3.9 1.6
-+ 0.2 -+ 0.1 -+ 0.1 -+ 0.4 -+ 1.0
0.5 0.5 0.3 3.0 0.3
-+ 0.2 -+ 0.3 -+ 0.1 -+ 0.6 -+ 0.7
l o w - n i t r o g e n e s t u a r i e s in l a b o r a t o r y e x p e r i m e n t s ( T a b l e 4). G r a z i n g r a t e s by Microdeutopus gryllotalpa a n d Idotea baltica w e r e s i m i l a r b e t w e e n f i e l d a n d l a b o r a t o r y e x p e r i m e n t s (Fig. 4 a n d T a b l e 4). W e t h e r e f o r e a p p l i e d g r a z i n g r a t e s o f Gammarus mucronatus, Lysianopsis alba, a n d Erichsonella filiformis o b t a i n e d in l a b o r a t o r y e x p e r i m e n t s to o u r m o d e l . Since mid-nitrogen estuary grazing rates generally were between those of high-nitrogen and low-nitrog e n e s t u a r i e s (Fig. 4), w e i n t e r p o l a t e d t h e h i g h n i t r o g e n a n d l o w - n i t r o g e n r a t e s ( T a b l e 4) to estim a t e m i d - n i t r o g e n rates. Ampithoe longimana a n d Elasmopus levis a r e a p p r o x i m a t e l y t h e s a m e size as C. compta, so we u s e d C. compta g r a z i n g r a t e s f r o m our field experiment for these species.
Comparison with Independent Production Estimates Ecosystem gross and net production estimates h a v e b e e n m a d e f o r t h e e s t u a r i e s o f W a q u o i t Bay f r o m m e a s u r e m e n t s o f d i e l c h a n g e s in f r e e waterd i s s o l v e d o x y g e n m o n t h l y o v e r s u m m e r 1991 ( D ' A v a n z o e t al. 1996). P h y t o p l a n k t o n g r o s s p r o duction measurements (using light/dark bottles and oxygen measurements) were made at the same t i m e ( J u l y to O c t o b e r ) (K. F o r e m a n u n p u b l i s h e d d a t a ) . T h e d i f f e r e n c e b e t w e e n t h e s e two e s t i m a t e s is itself a n e s t i m a t e o f m a c r o p h y t e g r o s s p r o d u c t i o n (K. F o r e m a n u n p u b l i s h e d d a t a ) . T h e s e m e a s u r e m e n t s c a n b e u s e d to o b t a i n a n i n d e p e n d e n t e s t i m a t e o f a v e r a g e n e t p r o d u c t i o n b y Cladophora vagabunda b e t w e e n J u l y a n d O c t o b e r 1991 in e a c h e s t u a r y ( T a b l e 5). T o o b t a i n t h e s e e s t i m a t e s , we
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1995 Fig. 6. Estimated net change in Cladophoravagabunda biomass (g dry weight m -2 d l) due to growth of extant algae and grazing by all extant grazers (top) and grazing by extant pop_ ulations of MicrodeutopusgryUotalpa (bottom) during summers 1994 and 1995 in high-, mid-, and low-nitrogen estuaries ( -+propagated SE).
a p p l i e d t h e g e n e r a l p h o t o s y n t h e t i c e q u a t i o n to c o n v e r t g r a m s o x y g e n to g r a m s b i o m a s s a n d a c o n v e r s i o n f a c t o r f o r m a c r o a l g a e ( 5 0 % ) a n d seagrasses ( 4 3 % ) f r o m g r o s s to n e t p r o d u c t i o n ( D u a r t e a n d C e b r i ~ n 1996) to t h e p e r c e n t a g e o f t o t a l m a c r o p h y t e b i o m a s s m a d e u p o f C. vagabunda f r o m o u r s u r v e y d a t a (Fig. 1). We then averaged our estimates of net product i o n ( w h i c h d o n o t i n c l u d e a d j u s t m e n t s f o r storage, decomposition, or export) between July and O c t o b e r in 1994 a n d 1995 (Fig. 6, t o p ) to c o m p a r e
TABLE 5. Mean net prodnction by Cladxrphoravagabundabetween July and October ba.~d on independent oxygen measnrements in 1991 (D'Avanzo et al. 1996; K. Foreman unpublished data) and our estimates. Our estimates (Fig. 6, top) were based on growth rate measurements (Peckol et al. 1994), biomass in 1994 and 1995, and grazing rate measurements. Mean percentage of net production accounted fbr by herbivory (Fig. 5, middle) is given for both estimates (oxygen data and this study) assuming no net change in biomass (+-SE of means between years 1994 and 1995 for our estimates).
Estuary High nitrogen Mid nitrogen Low nitrogen
NetProductionby('.vagabunda (gdwproducedm-2d-I) ICstimates based on oxygendata Thispaper 2.4 1.0 0.2
5.8 -+ 0.0 1.3 -+ 0.1 -0.1 +- 0.1
%NetProductionbyC. vagabunda AccountedforbyHerbivory F~stoxygen imatebased sdataon Thispaper 12 40 447
4 -+ 1 27 + 1 129 _+ 24
Grazing and Nutrient Controls of Macroalgae
with the oxygen-based estimates (Table 5). We also averaged summer estimates of grazing between July and October 1994 and 1995 (Fig. 5, middle) to determine the percentage of net production by Cladophora vagabunda which is accounted for by grazing (assuming no net change in biomass) (Table 5).
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Results and Discussion of Grazer Impact Estimates PREDICTED NET CHANGE IN
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CLADOPHORA VAGABUNDABIOMASS
The calculated increase of Cladophora vagabunda biomass (due to growth alone) (Fig. 5, top panel) was highest in the high-nitrogen estuary. These differences were due to higher growth rates (Peckol et al. 1994) and higher initial biomass (Fig. 1) in the high-nitrogen estuary. Possible losses of Cladophora vagabunda biomass due to grazing were lowest in the high-nitrogen estuary (Fig. 5, middle and bottom) because of low abundances of grazers (Fig. 2). Biomass losses peaked in the low-nitrogen estuary between June and August 1994 at the time when grazers were most abundant (Fig. 2). The calculated loss ofmacroalgal biomass to the entire grazing community was slightly larger than estimated losses due to Microdeutopus gryllotalpa, the species that makes up, on average, over 50% of the total grazing community (Fig. 2 and Table 2). The calculation of growth and consumption makes it possible to evaluate whether biomass of Cladophora vagabunda will increase or decrease seasonally in the estuaries subject to different nitrogen loading rates. Consumption of C. vagabunda by grazers is likely to have exceeded rates of macroalgal growth during mid-summer periods in the low- and mid-nitrogen estuaries (Fig. 6), resulting in net loss of biomass during part of each summer. At peak grazer densities in the low-nitrogen estuary (early August 1994), grazers could have consumed algae almost 5 • faster than the algae grew. In the mid-nitrogen estuary in early June 1995, grazers could have consumed algae at almost 4• the rate the algae grew (Fig. 6), largely because of the low C. vagabunda biomass at that time (Fig. 1). In the high-nitrogen estuary, at their peak in abundance (July 1994), grazers could have consumed algae only at one-tenth the rate the algae grew (Fig. 6). Grazers, therefore, are unlikely to account for the seasonal midsummer loss of macroalgae in the estuary subject to high nitrogen loads (Fig. 1) but can account for the lack of a peak in macroalgal biomass during summer (as predicted by estimates based on increased summer growth rates) in the mid- and low-nitrogen estuaries. To highlight the interaction between grazing
0q"
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~
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Growth rate (g. m-2- d-l) Fig. 7. Modeled grazing rates of Cladophora vagabunda by total grazers (g dry weight m -2 d 1) versus growth rates of C. vagabunda (g dry weight m 2 d 1) in the three estuaries of Waquoit Bay from data in Fig. 5 (middle and top). Nitrogen loading rates are shown next to the corresponding data. A dashed 1:1 line is also shown.
and nitrogen loading, we plotted modeled grazing rate by all grazers (g m -2 d -1) v e r s u s growth rate of Cladophora vagabunda (g m -2 d -1) in each estuary for all our data (Fig. 7). Nitrogen loading rate to each of the three estuaries is shown as the numbers next to each dataset. If loss of macroalgal biomass due to consumption equaled gain of biomass due to growth of the macroalgae, then biomass of algae would remain constant, and points would fall on the 1:1 line. Under low rates of nitrogen loading (64 kg N ha -1 yr-1), points scatter around the 1:1 line and extend to the upper left. This suggests that for the most part, grazing and growth are of similar magnitude, but that at times with maximum grazer abundance, their consumption is large enough to reduce macroalgal biomass. Thus, und e r low nitrogen loads, during the s u m m e r months, the biomass of C. vagabunda sometimes increases and sometimes decreases because of the shifting balance between growth and consumption. With increased nitrogen loading rate (520 kg N ha 1 yr 1), the scatter of points shifts such that the majority fall to the right of the 1:1 line. This shift indicates that macroalgal growth begins to exceed consumption, and becomes relatively more important in controlling macroalgal biomass. As nitrogen loading rate increases beyond 624 kg N ha -1 9 yr -1, the scatter of points lies far to the lower right, indicating that growth rates of the nitrogen-limited alga have increased and abundance of grazers have decreased to such a magnitude that macroalgae clearly escape control by grazers.
358
J. Hauxwell et al.
COMPARISON W I T I I INDEPENDENT PRODUCTION ESTIMATES
Our estimates of net production for summers 1994 and 1995 are within the same order of magnitude and relatively similar to those based on independent oxygen measurements in 1991 (Table 5). Both estimates yield the same general pattern: net production by Cladophora vagabunda increases with nitrogen load. The two estimates of the percent production accounted for by herbivory are, therefore, also similar (Table 5). These calculations suggest that the fate of autotrophic carbon differs in estuaries of different nitrogen loads. As the importance of herbivory in accounting for net production decreases as nitrogen load increases (two orders of magnitude in this study), other processes (storage, decomposition, or export) must increase in relative importance, especially considering the summer decline in biomass at the highnitrogen estuary, which is unaccounted for by herbivory (Fig. 1). Conclusion
The comparison between estimated growth increases and grazing losses of Cladophora vagabunda biomass (Figs. 6 and 7) suggests, first, that there is a potentially significant mid-summer impact of grazers on seaweeds in estuaries subject to lower nitrogen loads. Second, as nitrogen load increased, the increased macroalgal growth rates and biomass and diminished abundance of grazers resulted in relatively negligible top-down control of macroalgae biomass. This study therefore suggests the relative importance of top-down and bottom-up controls on primary producers varies depending on rate of nitrogen loading, and specifically, that the impact of herbivory on macroalgal biomass decreases with increasing nitrogen load to estuaries. Our results parallel those obtained in fresh water. McQueen et al. (1986) concluded, after reviewing several studies, that the interaction between top-down and bottom-up controls changes with the trophic status of lake ecosystems. In eutrophic systems, where primary productivity was relatively high, there was relatively higher biomass at each trophic level and the impact of top-down control (by herbivores on primary production) was weaker than in oligotrophic systems. We observed similar changes in the interaction between top-down and bottom-up effects, although our high nutrientloaded estuary contained lower herbivore abundance than the more pristine estuary. Similar changes in the importance of top-down control were also found fbr salt marsh grazers (hares, rabbits, and geese) along productivity gradients, although the mechanism causing differences in graz-
ing pressure had to do with decreased grazing efficiency in dense stands of salt marsh vegetation (van de Koppel et al. 1996). In temperate estuaries, grazers may govern not only the abundance of macroalgae but may also influence competitive interactions among different species of primary producers. As demonstrated in several relatively pristine estuaries (review by Jernakoff et al. 1996), amphipod and isopod grazers can maintain eelgrass beds by consuming fouling macroalgal and microalgal epiphytes. Presumably, significant grazer consumption of free-living benthic macroalgae (as predicted at our low- and midnitrogen estuaries) is also beneficial to eelgrass growth since accumulated mats can subsequently shade out eelgrass seedlings and shoots (Cowper 1978; Short et al. 1993). In fact, early August, the time when grazer impact is greatest in the low-nitrogen estuary (Fig. 6, middle and bottom), is also the peak biomass period for Zostera marina (Fig. 1, bottom). Significant consumption of benthic or epiphytic macroalgae at this time may actually facilitate eelgrass growth in this estuary. In Waquoit Bay estuaries subject to higher nitrogen loading rates and where grazer impact is lessened, eelgrass beds are likely harmed by epiphyte shading a n d / or are competitively e x c l u d e d by macroalgal growth (Borum 1985; Williams and Ruckelshaus 1993; Neckles et al. 1994), and macroalgal accumulations can result in canopies >75 cm thick (Hersh 1995). A(;m\'owI ~EDGMENTS This research was supported by a grant from National Oceanic and Atmospheric Administration, Coastal Ocean Program, a grant from the Land Margin Ecosystems Research initiative of the National Science Foundation, Waquoit Bay Fellowships awarded to J. McClelland and J. Hauxwell, a fellowship from NOAA (Sanctuaries and Reserves Division, ()ffice of Ocean and Coastal Resource Management, National Ocean Service) awarded to J. Hauxwell, and NSF REU internship site grants. We thank A. Downing for providing assistance in the field grazing experiment and macroalgal nutrient analyses, L. Soucy and J. Nixon for assistance in collecting benthic survey data, J. Joy for conducting the laboratory grazing rate experiment, J. Tober for providing temperature data, and K. Foreman for providing ind e p e n d e n t estimates of macrophyte production. Just Cebrifin and anonymous reviewers provided valuable comments and suggestions for improving the manuscript. We would also like to thank the Waquoit Bay National Estuarine Research Reserve for the use of their facilities. LITERATURE CITED BELL, S. S. 1991. Amphipods as insect equivalent.s? An alternative view. Ecology 72:350-354. BORUM,J. 1985. I)evelopment of epipbytic communities on eelgrass (Zostera marina) along a nutrient gradient in a Danish estuary. Marine Biology 87:211-218. BORUM,J. 1987. Dynamics of epiphyton on eelgrass (Zostera marina L.) leaves: Relative roles of algal growth, herbivory and substratum turnover. Limnology and Oceanography 32:986-992.
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Received for consideration, February 18, 1997 Acceptedfor publication, October21, 1997 UNPUBI JSHEI) MATERIALS FOREMAN, KEN. The Ecosystems Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543. HAUXWELL,.]FNNIWR. Boston University Marine Program, Marine Biological Laboratory, Woods I tole, Massachusetts 02543. JoY, JFNNIFER. Woods Hole Oceanographic Institution, Mailstop #32, Woods ttole, Massachusetts 02543. McCI.FI.I.AND,.IAMES.Boston University Marine Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02543. TOBER,JOANNA.Boston University Marine Program, Marine Biological Laboratory, Woods t / t i e , Massachusetts 02543. WAQUOIT BAY LAND MARGIN ECOSYSTEM RESFARCIIPROJFCT, % Ivan Valiela, Boston University Marine Program, Marine Biological l.aboratory, Woods Hole, Massachusetts 02543.
