Couplings of Watersheds and Coastal Waters: Sources and Consequences of Nutrient Enrichment in Waquoit Bay, Massachusetts

Estuaries Vol. 15, No. 4, p. 443-457 December 1992

IVAN VALIELA CHARLENE D'AVANZO KENNETH FOREMAN MICHELE BABIONE MICHAEL LAMONTAGNE Department of Natural Sciences DOUGLAS ]-IERSH Hampshire College JOSEPH COSTA 5 Amherst, Massachusetts 01003 Boston Universit'r Marine Program Marine Biological Laboratory CHI-Ho SHAM 4 Woods Hole, Massachuseits 02543 JOHN BRAWLEY Department of Geography PAULETTE PECKOL Boston University BARBARA DEMEO-ANDRESON Boston, Massachusetts 02215 Department of Biological Sciences Smith College KATE LAJTHA Northampton, Massachusetts 01063 Biology Department Boston University Boston, Massachusetts 02215

ABSTRACT: Human activities on coastal watersheds provide the major sources of nutrients entering shallow coastal ecosystems. Nutrient loadings from watersheds are the most widespread factor that alters structure and function of receiving aquatic ecosystems. To investigate this coupling of land to marine systems, we are studying a series of subwatersheds of Waquoit Bay that differ in degree of urbanization and hence ;ire exposed to widely different nutrient loading rates. The subwatersheds differ in the number of septic tanks and the relative acreage of forests. In the area of our study, groundwater is the major mechanism that transports nutrients to coastal waters. Although there is some attenuation of nutrient concentrations within the aquifer or at the sediment-water interface, in urbanized areas there are significant increases in the nutrient content of groundwater arriving at the shore's edge. The groundwater seeps or flows through the sediment-water boundary, and sufficient groundwater-borne nutrients (nitrogen in particular) traverse the sediment-water boundary to cause significant changes in the aquatic ecosystem. These loading-dependent alterations include increased nutrients in water, greater primary production by phytoplankton, and increased macroalgal biomass and growth (mediated by a suite of physiological responses to abundance of nutrients). The increased macroalgai biomass dominates the bay ecosystem through second- or third-order effects such as alterations of nutrient status of water columns and increasing frequency of anoxic events. The increases in seaweeds have decreased the areas covered by eelgrass habitats. The change in habitat type, plus the increased frequency of anoxic events, change the composition of the benthic fauna. The data make evident the importance of bottom-up control in shallow coastal food webs. The coupling of land to sea by groundwater-borne nutrient transport is mediated by a complex series of steps; the cascade of processes make it unlikely to find a one- to-one relation between land use and conditions in the aquatic ecosystem. Study of the process and synthesis by appropriate models may provide a way to deal with the complexities of the coupling.

Introduction ' We dedicate this paper to our friend and colleague, the late William E. Odum of the University of Virginia. Coastal and estuarine waters are the most nu- Work reported here is part of the Waquoit Bay Land Margin trient-enriched ecosystems on earth (Nixon et al. Ecosystems Research project, funded by the National Science 1986; Kelly and Levin 1986). Nutrient loading has Foumlation, the United States Environmental Protection Agen- cy, and the National Oceanic and Atmospheric Administration. led to increased abundance of" nuisance algae, re- "File work was carried out in the Waquoit Bay National Estu- duced oxygen content of water, decimated shell arine Research Reserve, and we thank its executive director, Christine Gauh, tbr her cooperation. s Present address: Executiw~ Office of Environmental Affairs, " Present address: The Cadmus Group, 135 Beaver Street, Coastal Zone Management, Marion, Massachusetts 02738. Waltham, Massachusetts 02154.

1992 Estuarine Research Federation 443 0160-8347/92/040443-15501.50/0 444 I. Valieta et al.

rate of nitrogen loading will affect coastal macroalgae, phytoplankton, or fish. We need experiments to quantify the effects of nutrient loading and identify causal mechanisms. The experiments should be done at sufficiently- large space and time scales to accommodate the regional nature of the land-sea coupling and the long-term features of the processes involved. Fur- ther, because waterflow, sediment characteristics, and bathymetry modify the effects of nutrient loading, design and execution of the experiments re- quires collaboration among diverse disciplines such as geology, hydrology, and hydrography, as well as the more usual suite of biological and chemical measurements. The density of human populations within the coastal zones of the world is increasing. Nixon (1988) compiled data that showed that populations near 14 coastal bays in the United States had increased between 1860 and 1980. The increases ranged from 3-fold to 25-fold. Moreover, population densities in coastal areas have been increasing at rates faster than those of the general pop- Fig. 1. Growth in housing units in Massachusetts counties, ulation. One recent survey, for instance, showed 1980-1990 in relation to distance from the sea. Housing data that the population of coastal counties in the Unit- from U.S. Census. "Distance" is calculated as the average km ed States was growing at a rate 3 times that of the from the center of the county to the shoreline. total United States population (Culliton et al. 1989). The characteristic increases in human popula- and finfish, and many other changes in structure tions can also be seen on Cape Cod, Massachusetts. and function of aquatic communities. The increas- The rate of growth in housing units in Barnstable ing delivery of nutrients to coastal waters is caused County, for example, was 35.3% between 1980 and largely by the many kinds of human activities on 1990 (United States Census data). Barnstable, which coastal watersheds. Urbanization increases release covers all of Cape Cod, is the fastest growing of all of wastewater, which in turn increases delivery of the mainland Massachusetts counties. The rate of nutrients to groundwater, streams, and coastal wa- increase in housing units during 1980-1990 in ters. Deforestation attendant to urbanization re- Massachusetts was about 10% for inland rural duces interception and storage of precipitation- counties (lower right of Fig. 1) and for coastal coun- borne nutrients, and may favor nitrification; both ties in and around Boston (lower left Fig. 1). The these effects increase loading rates to coastal wa- latter are either fully developed or economically ters. Agricultural land uses involve fertilizer and incapable of supporting further urbanization. In presence of livestock. Significant amounts of nu- contrast, relatively rural coastal areas (Nantucket, trients from fertilizer and manure leach into wa- Martha's Vineyard, and Cape Cod) show increases terways, groundwater, and coastal bays. of 30 to 45% in housing units (top left of Fig. 1). Some nutrient inputs to coastal waters may orig- The high rate of urbanization on Cape Cod (and inate from human activities far from shore. Nitric similar coastal areas elsewhere) must result in more acid in acid rain, for instance, may contribute sub- nutrient delivery to groundwater, streams, and stantially to nitrogen budgets of estuaries in the coastal waters. Northeast United States (Culliton et al. 1989). In Information on mechanisms involved in the cou- most cases, however, nutrient sources within wa- pling of watersheds and receiving waters is of basic tersheds are larger than contributions from remote and applied interest. In terms of basic principles, sources (Valiela and Costa 1988). we need to know how processes within forests, Nutrient enrichment is the most pervasive agent aquifers, and the sediment-water interfaces, as well for change in coastal waters, yet we lack knowledge as hydrodynamic flow and mixing, affect cycling, of basic relationships between nutrient supply rates sources, and fates of biogeochemically important and many key ecological processes involved in substances. We also need to know more about basic function of ecosystems (Nixon et al. 1986). We controls of primary and secondary producers on cannot, for example, reliably quantify how a given coastal bays. From an applied perspective, we need Couplings of Watersheds and Coastal Waters 445

Fig. 2. Inputs and fates of nitrogen (mol N x 108 yr ') entering the watershed and traveling toward Buttermilk Bay (from Valiela and Costa 1988).

to evaluate the consequences of a given house den- adjoining receiving waters. Then we describe an sity--or other land use--on water quality in the interdisciplinary study on Waquoit Bay, where we receiving bay, and determine how far back from have been conducting a regional-scale experiment shore do we need to extend management practices in nutrient loading that permits examination of if we intend to protect coastal environmental qual- how loading rates from watersheds take place, and ity. quantifies the effects of loading on components of We have addressed these kinds of basic and ap- the coastal aquatic ecosystem. plied questions in case studies of shallow coastal bays and their watersheds by evaluating contri- Watersheds as Nutrient Sources butions of different sources of nutrients, and as- The major sources of nitrogen to coastal water- sessing the consequences of increased nutrient sheds in our area are precipitation, fertilizers, and loading to shallow bays along the coast of Massa- domestic wastewater. In earlier studies in Butter- chusetts. We chose to study small, shallow water milk Bay, a small, shallow bay on Cape Cod, Mas- bodies because these are the coastal ecosystems that sachusetts, we found that precipitation brought al- are affected first. Shallow nearshore waters can be most 1.2 x 10 s moles of nitrogen per year to the thought of as bellweathers of future trends in eu- surface of the watershed (Fig. 2). This value was trophication, and moreover, are easier to study obtained by multiplying the annually-averaged vol- because of their smaller size. Results from studies ume of precipitation by the average concentration in shallow ecosystems could then be used to de- of dissolved inorganic nitrogen (NH4 + + NOs- + velop and test hypotheses relevant to larger, hard- NO2-) (Valiela et al. 1978; Valiela and Costa 1988; er-to-study systems. Valiela et al. 1990). Fertilizer added 8.1 x 105 In this paper we first review some of our earlier moles of N yr -I to the watershed surface, an esti- work on how human activities on coastal water- mate obtained using information on agricultural sheds lead to increased nutrients in groundwater use of fertilizers and area of cropland around the and how this in turn increases nutrient loading to bay. 446 I. Valiela et al.

Nitrogen delivered to the watershed surface can the vicinity of septic tanks. Activity of denitrifying be taken up by vegetation, be denitrified in the bacteria in aquifers may be limited at greater dis- soil, or percolate through soil. Some of the N add- tances from septic tanks because of low concentra- ed in fertilizer was harvested as crops, so our cal- tions of DOM. This is a supposition that needs culation of fertilizer input is somewhat of an over- confirmation by further studies. estimate. Incorporation of N into aggrading forests We do not know the extent of nutrient attenu- is quantitatively important in our study area (Fig. ation by denitrification during transport of nitro- 2), because forests of Cape Cod have been growing gen in groundwater. However, a rough estimate since the mid-1800s, when most of Cape Cod was of potential nitrogen reductions in the aquifer can pastureland. The rates of accumulation of nitrogen be made by comparing the inputs from septic tanks in the pine-oak forest that cover Cape Cod are with the amounts of groundwater-borne nitrogen about 5-10 kg N ha -~ yr -I (unpublished data, J. near Buttermilk Bay (Fig. 2). Concentration of ni- Melillo and colleagues). This range of nitrogen ac- trogen in groundwater adjacent to Buttermilk Bay cretion could account for more than half to all of were measured by sampling and analyzing ground- the nitrogen delivered to the watershed surface water obtained from shallow well points (Valiela (Fig. 2). and Costa 1988). We also had estimates of ground- Losses of nitrogen from the watershed surface water flow into the bay. From these data we cal- caused by denitrification in soils are likely to be culated that 1.1 x 106 moles N yr-' were carried relatively low. Rates of denitrification (Groffman into Buttermilk Bay by groundwater. This value is and Tiedje 1989) in sandy soils similar to those of somewhat smaller than the 1.5 x 106 moles N yr -I our study area would remove only 10 to 20% of delivered by septic tanks (Fig. 2). This 27% differ- the nitrogen reaching the watershed surface (Va- ence may be caused by adsorption and denitrifi- liela and Costa 1988). The 10% estimate seems cation. On the other hand, because our calcula- most likely for soils in our study area (Peter Groff- tions are based on rough approximations, we cannot man, personal communication). be sure that the difference is significant. More ac- The rough estimates we calculated for Fig. 2 curate measurements need to be done, but to be suggest that, at least in our study area, most of the conservative we assume for the moment that all of nitrogen delivered by precipitation is intercepted the nitrogen that enters the aquifer from septic at the watershed surface. Percolation of nutrients tanks eventually makes its way to the shore of re- through to the subsoil and water table should be ceiving waters. a small fraction of the inputs. We conclude, first, that in watersheds with ac- Domestic wastewater from septic tanks provides creting forests, nitrogen inputs to groundwater are more nitrogen than precipitation or use of fertil- largely uncoupled from precipitation-borne inputs izers (Fig. 2). Moreover, septic tanks release nitro- to the watershed. Second, concentrations of nu- gen deep in the subsoil, below the root systems of trients in groundwater seem more closely related nearby trees. We calculated that about 1.5 x 106 to the density of septic tanks in the watershed. moles N yr -~ leave septic tanks in the watershed of Evidence for the second conclusion is provided by Buttermilk Bay, move toward the water table, and Persky (1986), who carried out a survey of solute then are entrained down-gradient in groundwater. concentrations in groundwater below areas of Cape This estimate was made using results from engi- Cod with different building densities. This study neering studies on septic tank performance, and found that median nitrate concentrations in- data on house occupancy patterns in our area (Va- creased as building density increased (Fig. 3), a liela and Costa 1988). result that implies that nutrient enrichment of The nitrogen (mainly ammonium) released by groundwater--and hence of receiving coastal wa- septic tanks is largely nitrified as it moves toward ters-will increase along with urbanization. Of the water table. It is highly likely that the remain- course, urbanization results in felling of forests, so ing ammonium is adsorbed to surfaces of particles that, in addition to direct input of nutrients via along the way (Caezan et al. 1987; Kipp 1987). It septic tanks, urbanization may also increase load- is also possible that some of the nitrate will be ing to groundwater by removing forests that in- denitrified while passing through the aquifer (Smith tercept precipitation-borne nutrients. and Duff 1988). Denitrification is indeed likely to take place near septic systems, where there may be A Regional Experiment in Nutrient both NO3- and sufficient amounts of low molecular Loading: The Waquoit Bay LMER Project dissolved organic matter (DOM). Such DOM is The Waquoit Bay Land-Margin Ecosystems Re- needed as an energy source by denitrifier organ- search project (WBLMER) is a regional-scale ex- isms. The engineering estimates of loading from periment in nutrient loading in which we can ex- septic tanks do include losses by denitrification in amine how major components of coastal landscapes Couplings of Watersheds and Coastal Waters 447

(watersheds, sediment-water interface, coastal bay) are coupled by nutrient transport and transformations. These studies involve understanding nutrient dynamics in the terrestrial components (watershed vegetation, soils, and aquifers), and transport and transformations of nutrients at and through the second component, the sediment-water interface. Lastly, we follow the dynamics of nutrients, and the first-, second-, and third-order effects of the different nutrient loading rates on the receiving aquatic ecosystem. The basis of the nutrient-loading experiment is that the degree of urbanization in different subwatersheds differs markedly. We delineated subwatersheds of Waquoit Bay on the basis of water table elevations (Fig. 4). Thus we can show that the watershed of Childs River, for example, is more densely urbanized than other subwatersheds such as Quashnet River and Sage Lot Pond (Fig. 5). We intend to show that differences in the land-use mo- Fig. 3. Nitrateconcentrations in groundwater below areas saic among subwatersheds result in differences in of Cape Cod having different densities of buildings. Data from Persky (1986). the rate of nutrient loading to groundwater, and hence to receiving coastal waters. The choice of subwatersheds therefore provides a regional-scale almost completely account for entry and exit of experiment in nutrient loading. flesh water, and can therefore carry out the cal- A second purpose in choosing subwatersheds that culations needed for nutrient loading estimates. are at different stages in the process of change from We estimated nutrient loadings to groundwater forest to urban is to use them as a space-for-time in the three selected subwatersheds, using land-use substitution (Pickett 1988), and thereby obtain a data and procedures by Frimpter et al. (1988) and depiction of the effects that result as nutrient load- other (Table 2). In these calculations only nitrogen ing increases over time. Development of the pres- provided by precipitation and septic tanks is con- ent differences in land use can be reconstructed sidered. For each subwatershed, surface N inputs from analysis of aerial photographs taken at inter- were divided into those intercepted by forests and vals from 1938 to the present. We will ultimately those passing into the subsoil. These calculations provide a detailed account of different types of land were made based on estimates of forest area. Pre- use in each subwatershed, but the history of ur- cipitation N entering the subsoil was added to sep- banization is captured by a simple count of build- tic system inputs to calculate loading to the water ings within each subwatershed over the course of table. time (Fig. 5). The estimated nitrogen loading rates to the dif- Quantification of nutrient loading to receiving ferent subwatersheds span a range of up to 2 orders waters begins with an assessment of freshwater flow. of magnitude. The range of nitrogen loading rates Fresh water flows into Waquoit Bay via ground- that affect subestuaries of Waquoit Bay span much water seepage and spring-fed streams. The flow of of the range of loading rates seen in other estuaries groundwater via seepage into the three selected (cf., the span across the x-axis in Fig. 7). subestuaries of Waquoit Bay was estimated by means To see if differences in house density, and hence of hydrological stream-tube calculations (Freeze in presumed N loading, actually translated into dif- and Cherry 1979). Flow through spring-fed streams ferences in nutrients concentrations in ground- was done using stream-gauge data (Table 1). The water near the shoreline, we used well points to sum of these two sources of the fresh water is re- obtain samples of groundwater at or above the high markably similar to estimates of annual flows of tide mark. Samples were obtained from well points groundwater calculated using values for annual placed at 1-m intervals on transects visited at dif- precipitation, evapo-transpirational losses, and re- ferent times of the year, and on one occasion at charge to groundwater (Table 1). The close agree- intervals of 20 m to 50 m around the periphery of ment of these two independent estimates suggests the subestuaries receiving water from each sub- seepage and streams account for all flow. It seems watershed. Concentrations of dissolved inorganic unlikely that freshwater flows beneath Waquoit Bay nitrogen (DIN) in groundwater from Childs River to the sea. Thus, we have a system where we can were an order-of-magnitude greater than those 448 I. Valiela et al.

Fig. 4. The subwatersheds in Waquoit Bay. Boundaries drawn by M. Babione and Chi-ho Sham. from Quashnet River or Sage Lot watersheds (Ta- fresh water over a year is roughly equivalent to ble 2). The differences were most marked for ni- annual recharge to the aquifer, and that no nutri- trate, so that the comparison of subwatersheds con- ent attenuation occurs during transport in the stitutes an experiment in nitrate loading. aquifer ('Fable 2). The expected concentrations of The concentrations of nitrogen measured in the dissolved inorganic nitrogen match closely the val- well-point samples can be used to check estimates ues actually found in the well-point samples (Table derived from loading calculations. We calculated 2). Even though these calculations are rough, they predicted concentrations of DIN expected to ap- do suggest that we can have some confidence about pear at the water's edge assuming that outflow of the magnitude of transport of nitrogen from wa- Couplings of Watersheds and Coastal Waters 449

TABLE 2. Nitrogen contributions (kg N yr-~) by precipitation and septic systems, and N loading to water table and hence to estuaries.

Subwatersheds Q~ashet Sage Lot Childs River ~lver Pond Precipitation Intercepted by forests 1,092 4,809 114 To soil in nonforest areas 1,209 2,634 11.5 Septic systems 13,000 11,900 320 Loading to water table 14,209 14,534 331.5 Calculated DIN conc (M)' 160 3.6 6.2 Measured DIN conc (M) in well point samples (geometric mean) 132.7 4.2 15.1 Assuming that seepage plus stream flow equals recharge.

Fig. 5. ttistorical trend in the degree of urbanization of to salinity suggests that the source of nitrate must three different subwatersheds of Waquoit Bay. Data from aerial be the freshwater end-member of the estuaries. photographs. Cf. Fig. 4 for the location of the subwatersheds. Clearly, the nitrate must come from the watershed, either from seepage along the shores of the subes- tershed through the aquifer, and to the water's tuary or from the spring-fed streams. edge. The translation between loading to a watershed and conditions in the water is articulated through Consequences of Nutrient Loading in a series of steps. The first step involves the en- Waquoit Bay trainment and possible attenuation of nitrogen in Above we reviewed evidence on delivery of" nu- flowing groundwater. The total quantity of nitro- trients, particularly of nitrate additions, from wa- gen furnished by wastewater and precipitation to tersheds to the water's edge of Waquoit Bay, and the aquifers of the Childs River and Quashnet Riv- concluded that differences in urbanization led to er subwatersheds is about the same (Table 2). How- different concentrations of nitrate in groundwater ever, the Quashnet River watershed is larger than moving from the watershed to receiving waters. the Childs River watershed (Table 2). Consequent- Below we focus on how the different rates of nitrate ly, there is more water involved in nutrient trans- loading change some key ecological components port within the aquifer of the Quashnet River wa- of the aquatic components of the three selected tershed. We calculate mean concentrations of subwatersheds of Waquoit Bay (Childs River, nitrate in groundwater about to enter Quashnet Quashnet River, and Sage Lot Pond). River by dividing the loading rate by the recharge volume, and assuming that nitrogen mixes uni- NUTRIENTS IN WATER INCREASE WITH formly within the aquifer. The calculated concen- URBANIZATION OF WATERSHEDS trations of nitrogen in groundwater about to dis- Concentrations of" nitrate in the water column charge into the Quashnet estuary are much lower of Childs River were larger than those of Quashnet than those calculated for Childs River (Table 2). River; concentrations of nitrate in Sage Lot Pond Because the assumption of mixing within the aqui- were the lowest (Fig. 6). The negative relationship fer is too simple, we are presently using ground-

TABLE 1. Annual flows of groundwater from watersheds into subestuaries (Childs River, Quashnet River, Sage Lot Pond) of Waquoit Bay. Data calculated byJ. Brawley, C.-H. Sham, and I. Valiela.

Childs River Quashnet River Sage Lot Pond Surt'ace area (ha) 687 2,657 59 Total flow of groundwater calculated from stream gauges and aquifer data Groundwater flow via stream (ms yr-0 2.01 x 106 10.91 x 106 (% of total) (56) (80.4) -- Groundwater flow via seepage (ms yr -~) 1.56 • 106 2.66 • 106 (% of total) (44) (19.6%) 3.76 x 10' Sum 3.57 • 106 1.36 • 107 3.76 • 106 Total flow of groundwater calculated from annual rain and recharge 3.1 • 106 1.2 x 107 2.67 x 10~ 450 I. Valiela et al.

Fig. 7. Distribution of number of homes (N) at different distances from the shoreline of Waquoit Bay. Data from aerial photos taken in 1938, 195.6, 1979, and 1989 are included in bars in indicate the history of urbanization in the area. Data of M. Babione and C.-H. Sham. Fig. 6. Concentration of nitrate vs. salinity in water columns of Childs River, Quashnet River, and Sage Lot Pond. Data from samples taken over the course of a year by K. Foreman. groundwater .near the shore and in regional estimates. Perhaps the nearshore concentrations are higher because of the greater density of houses water flow and transport models to incorporate a very close to the water's edge (Fig. 7). Further, a more realistic set of conditions for nutrient move- location away from shore also means longer travel ment within the aquifer. In any case, the calcula- time for nitrate in the groundwater. Average ve- tions do show that loading rates can be sharply locity of groundwater in our area is about 0.3 m modified by the volume of recharge water; there d -~, so a distance of only 300 m away from shore is no one-to-one relationship between loading from implies a year's travel time. If there is any atten- land use and nutrient concentrations discharged uation along the travel path, the importance of into coastal waters. septic tanks located farther away could be propor- The second step in the translation occurs in the tionally smaller. Thus, septic tanks near the water's shallow sediments where groundwater enters the edge are probably the most critical for nutrient estuaries. Groundwater about to enter Childs Riv- loading. This idea needs testing with actual mea- er holds about 133/~M NO3- (Table 2), but these surements of attenuation and with groundwater concentrations were not found in the receiving wa- models. ter column (Fig. 6). At most, extrapolation~ of the nitrate vs. salinity curve for Childs River in Fig. 6 PHYTOPLANKTON PRODUCTION AND yields about 60 ~M at salinity of 0~/~. This suggests BIOMASS INCREASE WITH ENRICHMENT a loss of about half the dissolved inorganic nitrogen Production by phytoplankton varied seasonally, during passage of groundwater through the thin and reached 100-200 mg C m -3 h -I in Childs River sediment-water interface. Denitrification could be during middle to late summer. These are consid- responsible for these losses (Seitziger 1988). Such losses are not seen in the Quashnet River data (Ta- ble 2 and Fig. 6). Perhaps, as argued by Seitzinger TABLE 3. Chlorophyll concentrations (mean + SE) in water and Nixon (1985) and Seitzinger (1988), rates of from stations located upstream and at the mouth of each of nitrification and denitrification increase as nitro- three subestuaries of Waquoit Bay. Each mean was calculated from eight measurements obtained at intervals over a one-year gen loading rates increase. If such were the case, period. Data of J. Costa. we might expect that denitrification rates are higher in Childs River than in Quashnet River and Sage Chlorophyll concentrations (mg m s) Lot Pond. Subestuary Upstream Sites Mouth Sites Differences in location of homes (and hence sep- Childs River 47.7 +- 21.1 25.5 + 7.6 tic tanks) may be an alternative explanation for the Quashnet River 8.6 + 2.6 5.9 + 1.7 discrepancy between measured concentrations in Sage Lot Pond -- 3.9 + 1.2 Couplings of Watersheds and Coastal Waters 451

quoit Bay lie within the scatter of Fig. 8, those of Quashnet and Sage Lot Pond lie below the fitted line. Perhaps nutrient uptake by macroalgae or denitrification in these estuaries are high enough to lower phytoplankton chlorophyll. We are cur- rently testing these hypotheses.

MACROALGAE INCREASE WITH ENRICHMENT Easily the most obvious response of the Waquoit Bay estuary ecosystems to nutrient loading is the proliferation of benthic macroalgae. Total macroalgal biomass, for example, increases 3- to 4-fold between Sage Lot Pond and Childs River (Table 4). The increases in macroalgal biomass in nutrient- loaded estuaries are the result of alteration to phys- Fig. 8. Potential input of nitrogen entering the ecosystem related to mean phytoplankton chlorophyll in water in subes- iological features of macroalgae. Cladophora vaga- tuaries of Waquoit Bay (open circles; Sage Lot Pond, Quashnet bunda is one of the two major species of macroalgae River, Childs River, in increasing order along the loading axis) in Waquoit Bay (Table 4). C. vagabunda from Childs and in other coastal waters [data compiled by Nixon and Pilson, River, the most nutrient loaded site (Table 4), have and modified from Valiela (1991)]. higher photosynthetic rates at any irradiance com- pared to C. vagabunda from Sage Lot Pond, the erably higher rates than the 10-50 mg C m -~ h -~ water body receiving the lowest nutrient load (Fig. measured in Sage Lot Pond during the peak of the 9, top). season. At other times of year, phytoplankton pro- C. vagabunda from Childs River also shows faster duction was very low, generally less than 1 mg C nitrogen uptake rates than C. vagabunda from Sage m -3 h -~ everywhere in Waquoit Bay. Lot Pond, regardless of the concentrations of am- Standing crops of phytoplankton, measured as monium in which they were incubated (Fig. 8, bot- chlorophyll, are higher in Childs River than that tom). The asymptotic uptake rate of Childs River in Quashnet River, and both of these estuaries in C. vagabunda was about twice that of the Sage Lot turn have more phytoplankton chlorophyll than Pond population. Sage Lot Pond (Table 3), the estuary that is ex- Differences in physiological performance such as posed to the lowest potential nutrient loading (Ta- shown in Fig. 9 result in differences in growth rate ble 2). The chlorophyll values are averages of mean, (Table 5). The Childs River C. vagabunda grow integrated water-column chlorophyll measure- faster than those in Sage Lot Pond when exposed ments taken over many sampling periods during to saturating irradiences. Within the macroalgal 1988-1989. There are strong down-estuary gra- canopy there is less light and slower growth rate. dients in chlorophyll concentrations in our subes- Since algae deep within the canopy appear to be tuaries (Table 3), but the differences between Childs healthy and active, there must be sufficient physical River, Quashnet River, and Sage Lot Pond are disturbances to turnover the canopy so that algae maintained down-estuary. are exposed to sufficient light at frequent enough The responses of average chlorophyll in the wa- intervals. ter to potential nutrient loading rate in our estu- Physiological responses to enhanced nutrient aries fall within the ranges observed in other es- supply, on aggregate, result in large accumulations tuarine environments (Fig. 8). The values for Childs of macroalgae. Although macroalgae were present River, the most nutrient-loaded estuary, lie within in the bay in the past (Curley et al. 1971), biomass the scatter around the line fitted to observations and cover were less than at present. The cover of from other estuaries. Although all data from Wa- macroalgae over the bay is now very extensive (Va-

TABLE 4. Mean (+ SD) of biomass of macrophytes in three selected subestuaries of Waquoit Bay. Data averaged from multiple samples per site collected monthly over one year. Data of D. ltersh.

Number of Biomass(g m2) Subestuary Samples Cladophoravagabunda Gracilaria tikoahiae Total MacroalgalBiomass Zostera marina Childs River 131 220 + 29.4 109 _+ 10.5 335 + 39.8 0 Quashnet River 130 85 _+ 11.1 48 _+ 5 150 +_ 14.3 0 Sage Lot Pond 78 36 _+_ 6 36 -+ 5.9 90 + 12.1 117 + 12.6 452 I. Valiela et al.

TABLE 5. Mean (_+_ SD) growth rates tbr Cladophora vagabunda from Childs River and Sage Lot Pond. Measurements were done in situ as increases in fresh weight in tethered fronds situated above the canopy and within the canopy.

Growth Rates (Doublingsd ~) Above Canopy Within Canopy Location (High Light Intensity) (Low Light Intensity) Childs River 0.09 -+ 0.02 0.04 -+- 0.02 Sage Lot Pond 0.04 _+ 0.02 0.03 + 0.02

comparison's sake, we can see that the potential uptake over a day, by only one of the algal taxa present in Childs River, is an order of magnitude higher than the stock of DIN. The nitrogen loading rate (Table 2), when converted to appropriate units, is 2-8 • 10 l~ ~mol N d -I. Loading rate is therefore of the same magnitude as the potential uptake by C. vagabunda, which of course is only one of the macroalgal species present in Childs River. All these comparisons are rough and ignore features such as regeneration of DIN, but they do suggest the potential importance of macroalgae in nutrient dynamics in our estuaries. In fact, uptake by macroaigae, we believe, is responsible for low nutrients in the water of Waquoit Bay during warmer months (unpublished data). A second example of the importance of macroalgae is their effect on oxygen content of the water. Fig. 9. Net photosynthesis vs. light intensity (top) and ni- Photosynthesis and respiration by macroalgae de- trogen uptake rate vs. concentration in water (bottom) for Cla- termine the vertical profiles of oxygen in Waquoit dophora vagabun<~acollected in Childs River and from Sage I.ot Pond. Data of P. Peckol. Bay and its estuaries. This is unusual, since physical mixing by wind, currents, and tides commonly overwhelm biological processes and largely deter- liela et al. 1990), and in some places within Waquoit mine oxygen content in coastal waters. Evidence Bay the algal canopy may be up to 75 cm thick for the role of macroalgal control of oxygen con- (unpublished data). In addition to the enhanced tent is presented in detail elsewhere (D'Avanzo et biomass, there is a marked shift in species com- al. in preparation), but Fig. 10 is a clear example. position of the macrophyte canopy. Nutrient load- At dawn, oxygen is depleted near the bottom (Fig. ing eliminates eelgrass and fosters growth of a green 10, black circles). As the sun comes up, photosyn- (Cladophora vagabunda) and a red (Gracilaria tik- thesis by phytoplankton and macroalgae generates vahiae) algal species (Table 4). The current abun- oxygen, and the profile of oxygen concentrations dance of Gracilaria tikvahiae is of particular inter- slides to the right (Fig. 10, open circles). The dom- est, since it was not mentioned in a survey done in inant effect of macroalgal photosynthesis is evident 1967 (Curley et al. 1971). from the pattern of" the daily swing; the largest Changes in biomass and composition of vegeta- change in oxygen occurs just above the macroalgal tion such as shown in Table 4 have significant re- canopy. After dusk, respiration consumes oxygen, percussions throughout the bay ecosystem. For ex- and the daily fluctuation is completed. Of course, ample, we calculate that at measured uptake rates there are many kinds of organisms in the bay, all (from Fig. 9) and an average ambient 20 gM DIN, of which respire, but unpublished data of P. Peckol the approximately 200 g m -~ of C. vagabunda in suggest that respiration by the macroalgae may Childs River would take up about 4 • 101~-< moles account for most of the oxygen depletion that takes DIN in the Childs River estuary. There are about place during the night. 7.5 x 109 #moles DIN in the Childs River estuary, Phytoplankton of course are partially responsi- on average, at any one instant. It is difficult to ble for the excursion of oxygen concentrations seen compare standing crops to uptake rates, but for in Fig. 10. The increased oxygen within the upper Couplings of Watersheds and Coastal Waters 453

Fig. 10. Vertical profiles of oxygen in Childs River during dawn and midafternoon of a sunny day (circles), and during afternoon after three cloudy days in a row. Data from C. O'Avanzo. portion of tile water column is probably due in some measure to phytoplankton production. K. Foreman's measurements of phytoplankt0n production suggest that during most of the year phytoplankton are not as productive as macroalgae, and account for about 20% of total primary production. During a few weeks in mid to late summer phytoplankton peak, and contribute perhaps 70% of the oxygen. If there is a sequence of a few cloudy days, photosynthesis by the macroalgae may be low enough that the daytime recovery of oxygen content seen in Fig. 10 does not take place. In as little as three cloudy days, the consumption of oxygen by respiration uncompensated by photosynthesis can pro- duce hypoxic or anoxic conditions (Fig. 10, tri- angles) near the bottom, or even over the entire water column. Anoxic events have far-reaching second- and third-order effects throughout the food web of Wa- quoit Bay. During the summer of 1988, for example, we recorded a prolonged overcast period July 19-23 (Fig. 11, top graph). This occurred

Fig. 11. Time course of light, temperature, oxygen, ammonium, phosphate, and chlorophyll in water of Waquoit Bay, summer 1988. Modified from Costa et al. (in press). 454 I. Valiela et al.

Fig. 12. Changes in eelgrass distribution in Waquoit Bay, 1951-1987. Black areas are eelgrass beds with cover near 100%. The diagonal stripes in 1951 map show an area of patchy eelgrass cover. The dotted ones in 1951 map refer to parts of photograph where it was impossible to interpret the information. From Costa et al. (in press).

during a time when the water was warm (Fig. 11, and the effect of macroalgae on the vertical dis- second graph) and the water column was strongly tribution of oxygen therefore poises the bay eco- stratified. During this period, net production by system in a rather unstable state, one in which there macroalgae was nil, while macroalgal respiration is an increase in the frequency of anoxic events exceeded 80 -< mol O~d-' h-' (Peckol et al. in prep- that can severely alter the trophic web and geo- aration). The oxygen content of surface water de- chemistry of the bay. Consumers, as well as nutri- creased sharply after that cloudy period (Fig. 11, ents and producers, are affected by increased fre- second graph). The lower oxygen was accompa- quencies of anoxia. Anoxic events can result in nied by increases in ammonium and phosphate extensive kills offish and invertebrates. In Waquoit concentrations (Fig. 11, third graph), presumably Bay we have recorded kills following anoxic events caused by increased regeneration. The increase in in each of the summers during our study (1988 to nutrients was followed almost immediately by a present). Nutrient loading thus leads to a cascade bloom of phytoplankton growth, as shown by the of fairly complicated second- and third-order ef- chlorophyll data (Fig. 11, bottom graph). We have fects. unpublished data that show that phytoplankton are Loading rates are also likely to prompt third- nitrogen-limited in the more saline areas of Wa- order effects on bacteria. One of the always puz- quoit Bay. Anoxic events thus have repercussions zling features of denitrification is the paradox of throughout key components of aquatic ecosystems. how anaerobic bacteria manage to find sufficient Anoxic events may occur on occasion in unen- nitrate, a compound that is obviously in short sup- riched shallow coastal water bodies, even if mac- ply in anaerobic environments. Perhaps one reason roalgae are scarce, and these events have effects for the increases in denitrification we have already on their ecosystems also. The point here, however, mentioned is that in enriched waters there are wide is that abundant macroalgae may increase the fre- daily fluctuations in oxygen conditions, as implied quency of such events and hence increase the con- in Fig. 10. These fluctuations could allow nitrate sequent changes in nutrient availability and phy- to reach the vicinity of anoxic microzones where toplankton as well as throughout the food webs. denitrifiers can survive and somehow have access Enrichment leads to dominance of macroalgae, to the new nitrate. Couplings of Watersheds and Coastal Waters 45S

EELGRASS ABUNDANCE IS REDUCED BY LOADING Eelgrass is absent from nutrient-loaded subestuaries of Waquoit Bay (Table 4). This is a second- order phenomenon rather than a direct conse- quence of nutrient additions (Costa 1988). Growth of" eelgrass is light-limited rather than nutrient- limited in Cape Cod (Dennison and Alberte 1985). Nutrient enrichment encourages growth of epiphytes on eelgrass leaves, and epiphytes intercept light (Costa 1988). The potential result is a decrease in vigor of eelgrass, with eventual reduced cover, and loss of the eelgrass habitat. There is a historical parallel to the differences in eelgrass cover we found in comparing the subwatersheds exposed to different loading rates. Eel- grass habitat in Waquoit Bay has decreased (Fig. 12), while the number of dwellings and the result- ing potential nutrient loading have increased during recent decades. The data of Fig. 12 were obtained from aerial photographs using interpretative methods developed by Costa (1988). We cannot be sure that the decrease in eelgrass was the direct result of nutrient loadings, but there is a negative correlation between nutrient loading calculated from the number of houses in the watershed and the loss of eelgrass cover in the bay (unpublished data). The disappearance of eelgrass over recent decades is documented by long-time residents, who recall that Childs River was an eelgrass-dominated estuary before the 1960s. Moreover, in the space- for-time substitution afforded by comparisons of the subestuaries (Table 4), it is clear that macroalgae replace eelgrass in the bottom of enriched estuaries.

ABUNDANCE OF ANIMALS DECREASES WITH LOADING The abundance and species richness of invertebrates found on the bottom and macroalgal canopy are lower in parts of Waquoit Bay in which more macroalgae are present (Fig. 13). These results are from replicated samples obtained using an Ekman dredge at several sites over Waquoit Bay. Fig. 13. Abundance and species richness of invertebrates from various sites in Waquoit Bay (samples of macroalgae from We can show a historical parallel to the spatial which animals were obtained were collected with an Eckman comparison of Fig. 12, using data from shellfish dredge: data from J, Buckley, A. Forrester, and R. Siwko). The catch reports. The catch of bay scallops (Argopecten sample point with lowest algal biomass and highest richness and irradians) from Waquoit Bay have decreased since abundance was taken in the part of the bay where eelgrass still the 1960s (Fig. 14). The decrease has been even exists. more marked in Eel Pond, which is on the western section of the bay and receives loadings from the has remained about the same over the last several Eel Pond and Childs River subwatersheds (Fig. 4), decades (Fig. 14), so not all benthic invertebrate the two most urbanized estuaries of Waquoit Bay. species are affected similarly. There may be some The scallop yield from the more urbanized water- differential tolerance for low oxygen between these body decreased more than that in the relatively two shellfish species. Perhaps more likely to ac- less urbanized Waquoit Bay proper (Fig. 14). count for the difference between the responses of On the other hand, the catch of quahogs (Mer- scallops and clams may be differential effects of cenaria mercenaria) in Waquoit Bay and Eel Pond eutrophication on the specific habitats used by these 456 I. Valiela et al.

Fig. 14. Reported catch of two major species of shellfish, scallops (Argopecten irradians) and quahogs (Mercenaria mercenaria), from Waquoit Bay proper and from Eel Pond. Data from Town of Falmouth Annual Reports, compiled by the Shellfish Warden. One bushel equals 35.2 1.

two stocks of shellfish: clams use the very shallow duction in eelgrass habitat brought about by eu- sandy littoral strips, and scallops depend on eel- trophication would make it difficult for the current grass beds in deeper areas. Eutrophication has, for population or for new recruits to find sufficiently some reason, not greatly altered the vegetation large areas of suitable habitat. In addition, the in- cover of littoral sands in Waquoit Bay. The strip creased frequency of anoxia must deplete scallop of littoral sands is still largely devoid of vegetation. populations. In contrast, the favored habitat of scallops has been much reduced by nutrient enrichment (Fig. 12). General Conclusions Macrolgal canopies are rather inhospitable hab- Nutrient loading has had pervasive repercus- itats for scallops--scallops that move into macroal- sions throughout the food web of the Waquoit Bay gal beds sink into the thick canopy of loose fronds. ecosystem. The first-, second-, and third-order ef- Suspension feeding within the canopy must be im- fects associated with different degrees of nutrient paired, and water within the canopy often becomes loading result in very different configurations of anoxic on a daily basis. Scallops that wander into the food web, differences in nutrient and carbon the macroalgal beds certainly are unlikely to thrive cycling, elemental budgets, and input-output bud- there. gets. Although we have enough knowledge to show It may be argued that the decrease in scallop that the differences exist, we need further study to catch reported in Fig. 14 is a regional recruitment establish cause and effect mechanisms and to quan- phenomenon, perhaps unrelated to local eutro- tify actual trends created by increased nutrient phication. This may be so, but even if there were loading. a sudden increase in larval recruitment of scallops The suite of effects that seem related to nutrient into Waquoit Bay, we suspect that the great re- enrichment in Waquoit Bay strongly imply the im- Couplings of Watersheds and Coastal Waters 457 portance of "bottom-up" controls in this aquatic period in the depth distribution of photosynthetic response ecosystem. We have as yet not explored the im- of Zostera marina (eelgrass). Marine Ecology Progress Series 25: 51-61. portance of "top-down" controls. FREEZE, R. A. ANDJ. A. CHERRY. 1979. Groundwater. Prentice- Our data so far suggest that land-use mosaics on llall. Englewood Cliffs, New Jersey. 604 p. coastal watersheds, even though separated by con- FRIMPTER, M. H.,j.j. DONOHOE, AND M. V. RAPACZ. 1988. A siderable distances from receiving waters, are mass balance nitrate model for predicting the effects of land use on groundwater quality in municipal wellhead protection strongly coupled to adjoining aquatic ecosystems, areas. Cape Cod Aquifer Management Project. United States and this coupling has fundamental consequences Geological Survey, Marlboro, Massachusetts. 54 p. for the structure and function of the receiving wa- GROFFMAN, P. M. AND J. M. TIEDJE. 1989. Denitrification in ter ecosystem. Human activities on the watersheds North Temperate forest soils: Spatial and temporal patterns work to increase "natural" nutrient sources and and the landscape level and seasonal sinks. Soil Biology Bio- chemistry 21:613-620. transport, and are ultimately responsible for in- KELLY, J. R. ANn S. A. LEVIN. 1986. A comparison of aquatic creases in nutrient delivery to coastal waters. and terrestrial nutrient cycling and production processes in Ideally, we would like to have a suitable index natural ecosystems, with reference to ecological concepts of of land use, for example, "number of houses" or relevance to some waste disposal issues, p. 165-203. In G. Kullenberg (ed.), The Role of the Oceans as a Waste Disposal "area of accreting forests," or some combination Option. NATO Advanced Research Workshop Series. D. of these variables. We could then search for a cor- Reidel Publishing Company, Dordrecht. respondence of the index to water quality in the KIPP, K. !.. 1987. Preliminary one-dimensional simulation of receiving water body. As is obvious from the dis- ammonium and nitrate in the Cape Cod sewage plume, p. cussion above, one-to-one translations of land use B43-B44. In Toxic Waste and Groundwater Contamination Program, 3rd Technical Meeting. United States Geological to nutrient loading, and to consequences for water Survey, Boston, Massachusetts. quality and resources are unlikely. The many linked NIXON, S. W., C. A. OVIATT, J. FRVrHSEN, AND B. SULLIVAN. mechanisms, and their first-, second-, and third- 1986. Nutrients and the productivity ofestuarine and coastal order effects, make the finding of such correspon- marine ecosystems. Journal of the Limnological Society of South Africa 12:43-71. dences a challenging task. Many ostensibly "obvi- NIXON, S. W. 1988. Physical energy inputs and the comparative ous" relationships fail to materialize. There is no ecology of lake and marine ecosystems. Limnology and Ocean- doubt that the translation exists. Comprehensive, ography 33(pt.2): 1005-1025. interdisciplinary study and modelling of the inter- PERSKV, J. H. 1986. The relation of ground-water quality to actions, and of the responses of processes involved, housing density, Cape Cod, Massachusetts. U.S.G.S. Water- Resources Investigations Report 86-4093, Boston, Massachu- promise timely answers to the central question of setts. 29 p. how land use on watersheds is coupled to conse- PICKE'r~', S. T. A. 1988. Space for time substitution as an al- quences in the receiving aquatic ecosystem. ternative to long-term studies, p. 110-135. In G. E. Likens (ed.), Long-Term Studies in Ecology. Springer-Verlag, New York. LITERATURE CITED SEITZINGER, S. P. 1988. Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. CAEZAN, M. C., E. M. "I'HURMAN, AND R. L. SMI'I'tt. 1987. The Limnology and Oceanography 33:702-724. role of cation exchange in the transport of ammonium and SEITZINGER, S. P. ANn S. W. NIXON. 1985. Eutrophication and nitrate in a sewage--contaminated aquifer, p. B53-B58. In rate of denitrification and N20 production in coastal marine Toxic Waste and Groundwater Contamination Program, 3rd sediments. Limnology and Oceanography 30:1332-1339. "Technical Meeting. United States Geological Survey, Boston, SMITH, R. L. ANnJ. H. DUTY. 1988. Denitrification in a sand Massachusetts. and gravel aquifer. Applied EnvironmentalMicrobiology 54:1071- COSTA, J. E. 1988. Distribution, production, and historical 1078. changes in abundance of eelgrass (Zostera marina) in south- VALIV.LA, I. 1991. Ecology of water columns, p. 29-56. In R. eastern Massachusetts. Ph.D. Thesis. Boston University, 352 p. S. K. Barnes and K. H. Mann (eds.), Fundamentals of Aquatic COSTA, J. E., B. L. IIowzs, A. E. GmLIN, AND I. VALIELA. In Ecology. Blackwell, Oxford. press. Monitoring nitrogen and indicators of nitrogen to sup- VALIELA, I. AND J. COSTA. 1988. Eutrophication of Buttermilk port management action in Buzzards Bay. In D. II. McKenzie, Bay, a Cape Cod coastal embayment: Concentrations of nu- D. E. Hylact, and V.J. McDonald (eds.), Ecological Indicators. trients and watershed nutrient budgets. Environmental Man- Volume 1. Elsevier Press, London. agement 12:539-551. CULLITON, T. J., C. M. BLACKWELL, D. G. REMER, T. R. VALIELA, 1., J. TEAL, S. VOLKMANN, D. SHAFER, AND E. CAR- GoonSPEEI), AND M. A. WARREN. 1989. Selected character- PENTER. 1978. Nutrient and particulate fluxes in a salt marsh istics in coastal states, 1=980-2000. NOAA's Coastal Trends ecosystem: Tidal exchanges and inputs by precipitation and Series: Report 1. National Oceanic and Atmospheric Admin- groundwater. Limnology and Oceanography 23:798-812. istration, Strategic Assessment Branch, Rockville, Maryland. VALIELA, I.,J. COSTA, K. FOREMAN,J. M. TEAL, B. HOWES, AND 15p. D. AUBREY. 1990. Transport of groundwater-borne nutri- CURLEY,J. R., R. P. LAWTON, J. M. HIGK~'I', AND J. D. FISKE. ents from watersheds and their effects on coastal waters. Bin- 1971. A study of the marine resources of the Waquoit Bay- geochemistry 10:177-197. Eel Pond Estuary. Department of Marine Fisheries, Sandwich Massachusetts. 40 p. Receivedfor consideration, September 1, 1990 DENNISON, W. C. AND R. S. ALBERTE. 1985. Role of daily light Acceptedfor publication, March 13, 1992