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JENNIFER L RUESINK 1,*, G. CURTIS ROEGNER %~, P~RETF R. DUMBAULDS,.JAN A NEWTON 4,~, and DAVID A ARMSTRONG 2. Department of Biology ...

Estuaries

Vol. 26, No. 4B, p. 1079-1093

August 2003

Contributions of Coastal and Watershed Energy Sources to Secondary Production in a Northeastern Pacific Estuary JENNIFER L RUESINK1,*, G. CURTIS ROEGNER%~, P~RETF R. DUMBAULDS,.JAN A NEWTON4,~, and DAVID A ARMSTRONG2

Department of Biology, University of Washington, Box 351800, ,Seattle, Washington, 98195 t800 ,School of Aquatic and Fishery Sciences, University of Washington, Box 355020, ,Seattle, Washington, 98195-5020 s Washington Department ofFish and Wildlife, Willapa Bay Field ,Station, P. O. Box 190, Ocean Park, Washington 98640 4 Washington State Department of Ecology, P. O. Box 47710, Olympia, Washington 98504-7710 ,School of Oceanography, University of Washington, Box 357940, ,Seattle, Washington 98195 7940 We e x a m i n e d the relationship between variation in origin of organic matter and benthic secondary production in a shallow, maerotidal estuary on the United States Pacific Northwest coast, Willapa Bay, Washington. Spatial variation in energy sources a n d benthic productivity were investigated at both local (vertical height and cross-bank coinp o n e n t s ) and regional (sites within the bay) scales. We determined the stable carbon isotope ratios of oysters (Crassostrea gigas) to evaluate marine versus terrestrial energy sources, c o m p a r e d growth rates of oysters, and made time series measurelnents of physical variables at estuarine channel and intertidal stations. T h e stable carbon isotope ratios of oysters ranged f r o m -22%o in inner p o r t i o n s of the estuary to -18%0 near the m o u t h a n d oysters grown on the substrate surface were enriched in ~1~C relative to those grown in the water column. T h e s e p a t t e r n s are consistent with terrigenous inputs away f r o m the estuary m o u t h and benthic mieroalgae in the diets of on-bottom oysters. T h e highest oyster growth was f o u n d at an inner estuary site where riverine inputs are relatively high and coincided with high a m m o n i u m in the water colulnn. However, f o r nlost sites in Willapa Bay~ oyster growth actually declined away f r o m the estuary Uloutb. Reducing the tinle available f o r feeding by transplanting oysters higher in the intertidal zone h a d significant negative effects on growth (e.g., a reduction of 27-35% over 0.5 Ul), Despite the fact that oysters grown on-bottoul had access to different resources than those in the water colunln, their growth was slower at any given tidal elevation, which nlay be due to on-bottoln competition with other s u s p e n s i o n feeders, b o u n d a r y layer effects, or interference f r o m turbidity. In a practical sense~ oyster growers have been adjusting to allochthonous energetic s u p p o r t of f o o d w e b s in Willapa Bay f o r m o r e than a century~ because they have traditionally m o v e d oysters f r o m s o u t h e r n parts of the b a y w h e r e recruitment is relatively high to beds where market-size oysters can be grown closer to the mouth. This study provides mechanistic s u p p o r t f o r these practices a n d suggests that climatic events on a variety of temporal scales (Pacific Deeadal Oseillatiom upwelling events) could have economic consequences f o r aquaculture. ABSTRACT:

Introduction

1996). Sedentary suspension feeders rely on advection to supply their food resources, and there are three potential origins of this material: ocean-derived p h y t o p l a n k t o n transported into the estuary by tidal action, material of primarily terrestrial origin that enters the estuary in freshwater, and aut o c h t h o n o u s p r o d u c t i o n of microalgae and macrophyte detritus. These three origins of primary p r o d u c t i o n can lead to quite different predictions about the spatial d i s t r i b u t i o n of b e n t h i c s e c o n d a r y p r o d u c t i o n t h r o u g h o u t an estuary. While variations in river flow and entrained organic materials are known to affect patterns of benthic p r o d u c t i o n (Sklar and Browder 1998; Jassby et al. 2002), interannual differences in oceanic productivity, shaped by E1 Nifio-Southern Oscillation, decadal oscillations,

Estuaries have long b e e n viewed as ecosystems of strong physical gradients where water p r o p e r t y gradients establish biotic c o m m u n i t y composition (Bulger et al. 1998). A m o r e m o d e r n view recognizes the effects of biotic interactions c o m b i n e d with highly localized circulation on ecosystem structure and function (Ruckelshaus et al. 1993). Spatial variation in the quantity and quality of available organic material in the water c o l u m n is well known to affect benthic secondary p r o d u c t i o n , particularly of suspension feeders ( L e n i h a n et al. * Corresponding author; tele: 206/543-7095; e-mail: [email protected] u.washin gton .edu. + C u r r e n t address: NOAA Fisheries, Point Adams Biological Field Station, Box 155, H a m m o n d , O r e g o n 97013. 9 2003 Estuarine Research Federation

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and upwelling events, may have equal or greater impacts. Recent investigations in Willapa Bay and other Pacific Northwest estuaries have revealed a strong physical linkage to processes occurring in the coastal ocean (Hickey and ganas 2003). Coastally-derived p h y t o p l a n k t o n is routinely transported into these estuaries (Roegner and Shanks 2001; Roegner et al. 2002), where it may contribute substantially to benthic s e c o n d a r y production. We exa m i n e d spatial v a r i a t i o n m g r o w t h of a conspicuous benthic estuarine suspension f e e d e r (Pacific oyster, Crassostrea gigas T h u n b e r g ) and the environmental conditions, particularly food resources, e x p e r i e n c e d in the intertidal zone of a large coastal estuary, Willapa Bay, Washington, U.S. We r e p e a t e d studies over several years to test for consistency of spatial patterns. M u c h of the r e c e n t research on food webs in estuaries has used stable isotope analysis to determine what supports these productive systems. Consistently, seston and benthic consumers b e c o m e m o r e e n r i c h e d in gl~C along a freshwater to marine salinity gradient (Coffin and Cifuentes 1999; Fry 1999; Maksymowska et al. 9000). T h e end m e m b e r s are C3 plants at the freshwater end (8l~C < 25%0) and marine p h y t o p l a n k t o n in the ocean (~sC ranging from 22%0 to 18%o, Fry and Sherr 1984). T h e c o m m o n l y u n d e r s t o o d mechanism for e n r i c h m e n t in estuarine stable isotope ratios along salinity gradients is consistent with how m u c h terrestrial and marsh primary p r o d u c t i o n arrives from rivers. In areas of the estuary m o r e distant from rivers, the stable isotope signal from C3 plants dissipates, and the major resource for primary consumers is often a u t o c h t h o n o u s production of estuarine phytoplankton. T h e extent to which estuarine organisms directly use detritus undoubtedly varies with the system and species involved. Detritus from terrestrial and marsh plants appears relatively i m p o r t a n t for consumers in a low-salinity creek in Chesapeake Bay (Stribling and Cornwell 1997) and for fish p r o d u c t i o n in southern California wetlands (Kwak and Zedler 1997). In systems such as Apalachicola Bay, Florida, and the Gamtoos estuary, South Africa, microalgae are m u c h m o r e i m p o r t a n t than macrophytes or detritus in supporting estuarine food webs (Schlacher and Wooldridge 1996; C h a n t o n and Lewis 2002). Acceptance of the i m p o r t a n c e of terrigenous inputs has not d e p e n d e d on demonstrating that the food web is detritus-based and it is generally accepted that nutrients allowing vigorous phytoplankton growth in estuaries stem ultimately from freshwater ( C h a n t o n and Lewis 2009). T h e contrib u t i o n to e s t u a r i n e p r i m a r y p r o d u c t i o n f r o m coastal oceanic resources has generally b e e n ign o r e d or believed to be u n i m p o r t a n t .

Although estuaries show a general trend of enr i c h m e n t in 8~sC from freshwater to ocean, the specific 81sC values differ a m o n g estuaries and a m o n g species. Deposit feeders can show different stable isotope ratios than suspension feeders in the same location. Benthic-feeding species such as crab and shrimp were relatively enriched in ~l~C c o m p a r e d to oysters and anchovies that were assumed to eat p r i m a r i l y p h y t o p l a n k t o n ( C h a n t o n a n d Lewis 2002). In the Westerschelde, Belgium, Macoma 5Mthica, a facultative deposit-suspension feeder, was enriched in glsC relative to an exclusive suspension feeder ( H e r m a n et al. 2000). T h e e n r i c h e d stable carbon isotope values are likely due to diets composed of h i g h e r p r o p o r t i o n s of C4-plant detritus or benthic microalgae, both of which could be m o r e c o m m o n on- than off-bottom. H o w do these variations in resources for primary consumers relate to patterns of estuarine production? In a broad review of primary p r o d u c t i o n in estuaries, Heip et al. (1995) r e p o r t e d that estimates of p h y t o p l a n k t o n biomass generally decline from i n n e r to outer portions of estuaries. Estimates of annual p r o d u c t i o n did not match this pattern. While nutrients delivered in freshwater can stimulate p h y t o p l a n k t o n p o p u l a t i o n growth, freshwater can i n t r o d u c e osmotic stress and, at high flow, flush p h y t o p l a n k t o n out of an estuary (Muylaert et al. 2001). Rivers can also i n t r o d u c e suspended particulate matter that interferes with light required for p h y t o p l a n k t o n growth (Pennock and Sharp 1986). M a u r e r et al. (1992) suggest that P / B (production per biomass) of s e c o n d a r y consumers is higher inside Delaware Bay than at coastal stations, but this may primarily reflect the d o m i n a n c e of deposit feeders inside the bay. Although resource patterns vary consistently within estuaries, the pred o m i n a n c e of terrigenous inputs in freshwater at the head and of m a r i n e inputs at the m o u t h may not have consistent consequences for the production of benthic suspension feeders that consume pelagic resources. T h e r e are many examples in which estuarine function changes after m a n i p u l a t i o n of freshwater inputs. T h e major manipulations are diversion of freshwater and addition of a n t h r o p o g e n i c nutrients. Freshwater diversion can r e d u c e n u t r i e n t input (Smaal and Nienhuis 1992) with food web consequences that propagate to affect yields of commercial estuarine and coastal fisheries ( L o n e r a g a n and B u n n 1999). Many estuaries suffer from eutrophication due to a n t h r o p o g e n i c n u t r i e n t loading, which clearly links inputs from the watershed with changed dynamics and composition of primary p r o d u c e r s (Cloern 2001). N u t r i e n t loading appears to be particularly detrimental when residence time is relatively long and major suspension

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sized that spatial and temporal variation in delivery of these resources d e t e r m i n e s benthic s e c o n d a r y p r o d u c t i o n of suspension feeders. Estuarine gradients associated with the quality and quantity of food, r a t h e r than, for instance, t e m p e r a t u r e or salinity, would affect suspension f e e d e r growth. We tested this hypothesis by measuring the growth of Pacific oysters transplanted to multiple sites in Willapa Bay. Materials a n d M e t h o d s STUDY SITE D E S C R I P T I O N

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Fig. 1. Willapa Bay, W a s h i n g t o n , showqng study site l o c a t i o n s a n d NOAA w e a t h e r station at Toke P o i n t (circle). RP Range Point, SP = Stony Point, TP = Toke Point, ST = Stackpole, BC Bay Center, NA Nahcotta, SS Sunshine, SW Shoalwater, a n d LI = L o n g Island. D i a m o n d s i n d i c a t e water s a m p l i n g stations, c o r r e s p o n d i n g to stations 1-8 f r o m n o r t h e a s t to south.

feeders have declined due to overexploitation or changed species interactions (Josefson and Rasmussen 2000; Jackson et al. 2001). Oysters are conspicuous estuarine suspension feeders, and their p r o d u c t i o n is economically imp o r t a n t for wild fisheries and aquaculture. Several environmental factors have b e e n suggested to affect oyster growth, including salinity, t e m p e r a t u r e , and food supply (Kobayashi et al. 1997). We focused on resource availability because of docum e n t e d fluctuations in p h y t o p l a n k t o n within the Willapa Bay estuary associated with coastal ocean events (upwelling and relaxation, Columbia River p l u m e location; R o e g n e r et al. 2002). We used three techniques ( t e m p e r a t u r e loggers, stable isotopes, fluorescence) to assess the relative a m o u n t s of o c e a n i c a n d f r e s h w a t e r r e s o u r c e s reaching sites t h r o u g h o u t the bay. We hypothe-

Willapa Bay (46~ 124~ is a b r o a d shallow estuary with two distinct arms, one oriented along a north-south axis of a b o u t 40 km and ano t h e r short eastward arm extending towards the Willapa River (Fig. 1). About 45% of the water in the bay is e x c h a n g e d between m e a n lower low water and m e a n h i g h e r high water t h r o u g h a 10 km shallow e n t r a n c e in the northwest c o r n e r (Hedgp e t h and Obrebski 1981). Freshwater i n p u t to Willapa Bay is primarily from the N o r t h and Willapa Rivers in the n o r t h , and from several smaller rivers such as the Palix in the east and Naselle in the southeast. High river flows occur primarily during winter m o n t h s of high precipitation, and little (< 7% of annual total) freshwater enters from J u n e to S e p t e m b e r (waterdata.usgs.gov/nwis). A u n i q u e feature of this bay is the periodic intrusion of freshwater t h r o u g h the m o u t h of the bay when the Columbia River p l u m e extends northward along the coast ( R o e g n e r et al. 2002). Aquaculture in Willapa Bay p r o d u c e s about 15% of oysters in the U.S., a l t h o u g h the yield from the bay has declined by m o r e than half since the mid-1940s ( H e d g p e t h and Obrebski 1981). This decline has b e e n attributed to loss of commercial oyster growth in the south part of the bay, possibly due to changes in water quality associated with u p l a n d timber extraction or cultured and naturally recruiting oysters that have e x c e e d e d the carrying capacity of the estuary ( H e d g p e t h and Obrebski 1981). T h e sites we chose within Willapa Bay to study spatial variation in energy sources and benthic productivity span the length of both arms of the estuary (Fig. 1). Sites within 10 km of the m o u t h include Stackpole, Bay Center, Stony Point, and Toke Point. Within a radius of an additional 10 km lie N a h c o t t a and Range Point. Beyond this distance along the eastern arm, oysters are not legal to harvest due to water quality concerns (high fecal coliform counts). In the s o u t h e r n part of the bay, three sites (Sunshine, Shoalwater, and Long Island) lie m o r e than 20 km from the m o u t h .

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t i m e in c o m p a r i s o n s o f o y s t e r g r o w t h a c r o s s sites. T i d a l e l e v a t i o n s w e r e c a l c u l a t e d by fitting t e m p e r a t u r e r e c o r d s ( t i m e t) at i n t e r t i d a l sites w i t h a c o m b i n a t i o n o f v e r i f i e d w a t e r t e m p e r a t u r e (Tw), a i r t e m p e r a t u r e (T~), a n d w a t e r level d a t a (W) f r o m a National Oceanic and Atmospheric Administration (NOAA) weather station at Toke Point ( w ~ w v l . p a c t i d e . n o a a . g o v / t o c . h t m ; Figs. 1 a n d 2).

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Fig. 2. (A) Sample temperature and water level records from the NOAA weather station at Toke Point. (B) Temperarares recorded at two intertidal sites in Willapa Bay,Washington. In these intertidal records, low temperatures correspond to low tides, when the loggers were exposed to air. Just prior to these low temperature periods, temperatures rose, reflecting warmer bay water passing across sites during the ebb. These records demonstrate a tidal phase delay between the mouth and head of the bay, because the air-exposed times are slightly offset. (C) Actual and best-fit estimate of temperature record from Nahcotta based on Eq. 1. In this example, L = 0.85 rn, C = 1.35~ and d 31 minutes.

ENVIRONMENTAL GRADIENTS

Temperature Loggers T e m p e r a t u r e l o g g e r s w e r e d e p l o y e d at all sites to d e t e r m i n e site-specific tidal e l e v a t i o n s a n d w a t e r temperatures. Water temperatures indicate the amount of cool o cean versus warm bay water reachi n g a site, T h i s a s s u m p t i o n is c o r r o b o r a t e d by t h e fact t h a t l o c a l w a t e r t e m p e r a t u r e s a r e l o w e s t at t h e p o i n t o f g r e a t e s t tidal i n f l u x (Fig, 2), A c t u a l t i d a l e l e v a t i o n was n e c e s s a r y to c o r r e c t for i m m e r s i o n

fTa. t [C XTwt d

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T~ is t h e t e m p e r a t u r e e s t i m a t e d at e a c h site, b a s e d o n t h e e s t i m a t e d e l e v a t i o n o f t h e l o g g e r (L), a c o n s t a n t C t h a t allows t h e a v e r a g e w a t e r t e m p e r a t u r e at e a c h site to d i v e r g e f r o m m e a s u r e m e n t s at t h e w e a t h e r s t a t i o n , a n d a c o n s t a n t d i n t r o d u c i n g a delay in tidal p h a s e at e a c h site r e l a t i v e to t h e w e a t h e r station. We programmed temperature loggers (iguttons, Dallas S e m i c o n d u c t o r ) to r e c o r d a m b i e n t t e m p e r a t u r e e v e r y 20 m i n f i o m J u l y 15 to A u g u s t 4 o r J u l y 22 to A u g u s t 11, 2001, at 9 i n t e r t i d a l s a m p l i n g sites. A d d i t i o n a l l o g g e r s r e c o r d e d at 4 0 - m i n i n t e r v a l s bet w e e n A u g u s t 22 a n d O c t o b e r 14, 2001. T e m p e r a ture loggers were covered with a thin layer of mar i n e e p o x y ( S e a G o i n ' E p o x y Putty) a n d a t t a c h e d to p o s t s 1.2 m (July) o r 0.6 m ( A u g u s t ) a b o v e t h e m u d f l a t . We t r i e d to b e c o n s i s t e n t in p l a c i n g t h e p o s t s at m e a n l o w e r low w a t e r ( M L L W ) , b a s e d o n w a t e r level a n d s o m e s u r v e y i n g . Two l o g g e r s w e r e p l a c e d at e a c h site in J u l y a n d a n a d d i t i o n a l o n e o r two in A u g u s t . A t t h e N O A A w e a t h e r s t a t i o n at T o k e P o i n t , water level was r e c o r d e d e v e r y 6 m i n , a n d air a n d w a t e r t e m p e r a t u r e s w e r e r e c o r d e d e v e r y h o u r . We e s t i m a t e d a i r a n d w a t e r t e m p e r a t u r e s at 6 - m i n intervals b a s e d o n l i n e a r i n t e r p o l a t i o n s o f t h e h o u r l y r e c o r d s . T h e 6 - m i n r e c o r d s f r o m t h e w e a t h e r stat i o n clearly d o n o t m a p e x a c t l y o n t o 20 o r 4 0 - m i n r e c o r d s at e a c h site, in w h i c h case t h e f i t t i n g p r o cedure selected the prior weather station records. W e d e t e r m i n e d L, C, a n d d by m i n i m i z i n g t h e s u m o f s q u a r e d d i f f e r e n c e s b e t w e e n T~,t a n d a c t u a l t e m p e r a t u r e s (n - 1,438 o r 1,911 values; Fig. 2).

Stable Isotopes S t a b l e c a r b o n i s o t o p e r a t i o s w e r e u s e d to assess d i f f e r e n c e s in d i e t a m o n g oysters g r o w i n g t h r o u g h o u t W i l l a p a Bay a n d at d i f f e r e n t tidal e l e v a t i o n s , M a n y o f t h e r e s o u r c e s p o t e n t i a l l y u s e d by s u s p e n s i o n f e e d e r s h a v e b e e n p r e v i o u s l y a n a l y z e d for 61sC in a n d n e a r W i l l a p a Bay, a n d v a l u e s a r e - 2 8 % o f o r r i v e r i n e p a r t i c u l a t e o r g a n i c m a t t e r , - 2 0 % o f o r phytoplankton, and 15%0 for b e n t h i c m i c r o a l g a e ( L u b e t k i n 1997), O y s t e r s c a n f e e d o n p h y t o p l a n k ton, b e n t h i c m i c r o a l g a e , a n d m i c r o b e s ( L e G a l l et

Spatiotemporal Variation in Oyster Growth

al. 1997; Cognie et al. 2001) and select particles with relatively high chlorophyll c o n t e n t (Newell a n d J o r d a n 1983). A l t h o u g h eelgrass (Zostera rnar/,za) and i n t r o d u c e d cordgrass (,Spartina alterniflo ra) are c o n s p i c u o u s p r i m a r y p r o d u c e r s in Willapa Bay, studies in o t h e r locations have d e t e r m i n e d that m a c r o p h y t e s m a k e up a small p r o p o r t i o n of suspension feeder diets (McClelland a n d Valiela 1998). We m e a s u r e d 81~C of oysters t r a n s p l a n t e d to sites t h r o u g h o u t Willapa Bay in 2000 (4 sites) a n d twice in 2001 (9 sites). Tissue samples were taken f r o m a subset of early post-settlement oysters transplanted for growth m e a s u r e m e n t s (see Methods, Oyster Growth). F r o m each of five replicate poles p e r site, we analyzed one or two oysters at each h e i g h t on each pole for stable isotope ratios. Juvenile oysters were initially 8-95 m m in m a x i m u m shell dimension a n d grew by u p to 40 m m over two m o , so that m o s t of the tissue analyzed for stable isotope ratios grew after transplant. At the close of the growth studies, we i m m e d i a t e l y froze the samples. Frozen samples were later r e m o v e d f r o m the shell, a p o r t i o n containing the gut was separated f r o m the rest of each individual, and tissue was dried at 60~ for 72 h. Small a m o u n t s of n o n - g u t tissue (0.2-0.3 mg) were analyzed by gas c h r o m a t o g r a p h y - m a s s s p e c t r o p h o t o m e t r y at the E n v i r o n m e n tal Quality Analysis Laboratory, University of Regina or University of California-Davis. Data on ~ C : leC ratios are p r e s e n t e d relative to the standard P e e d e e belemnite. Substantial within-group variability has b e e n d o c u m e n t e d for stable isotope ratios of estuarine organisms (Cloern et al. 2002), which may m a k e it difficult to distinguish precise contributions of different energy sources to an org a n i s m ' s diet. O u r intent was not to d e t e r m i n e precise contributions, but r a t h e r to assess the a m o u n t of variation in energy sources used by oysters t h r o u g h o u t Willapa Bay, which d e p e n d e d only on the relative stable isotope values of oysters. We exa m i n e d the data for spatial a n d t e m p o r a l variation in 8I~C, using site, on- versus off-bottom, and season as fixed factors in analysis of variance (2000 data were e x a m i n e d separately to a c c o m m o d a t e fewer sites). We regressed average 81sC at a site against the water t e m p e r a t u r e offset f r o m the N O A A w e a t h e r station at Toke Point, which m e a sured the d e p a r t u r e f r o m m a r i n e conditions.

2Vut.r'ie~ts and Fluorescence We r e c o r d e d surface water p r o p e r t i e s at eight stations in d e e p channels, r u n n i n g f r o m station 1 in the n o r t h e a s t p a r t of Willapa Bay (Willapa a n d N o r t h Rivers) to station 8 in the south (Naselle River; Fig. 1). Stations 2 - 4 were closest to the m o u t h a n d oceanic influence. During s u m m e r

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( J u n e - S e p t e m b e r ) , water samples were collected five times in 1999 and four times in 2000. Samples of nutrients and f l u o r e s c e n t p i g m e n t s (chl a a n d p h a e o p i g m e n t s ) were o b t a i n e d using a rosette of Niskin bottles a r o u n d the conductivity, t e m p e r a ture, and d e p t h (CTD) logger, closed r e m o t e l y at the desired depth. Sampling p r o c e d u r e s for these p a r a m e t e r s follow Ecology protocols for the Marine Waters M o n i t o r i n g (Newton et al. 1998). Analyses for dissolved nutrients were c o n d u c t e d by University of Washington M a r i n e C h e m i s t r y Lab for nitrate, nitrite, a m m o n i u m , o r t h o p h o s p h a t e , a n d silicate. All n u t r i e n t samples were filtered t h r o u g h N a l g e n e 0.45 I~m p o r e cellulose acetate filters in the field at the time of collection a n d m a i n t a i n e d at 4~ Samples were frozen u p o n return to land (roughly 2 - 7 h after sampling). Nutrient samples were analyzed using T e c h n i c o n AutoAnalyzer II (United Nations Educational, Scientific, a n d Cultural O r g a n i z a t i o n 1994). Samples for chl a were filtered t h r o u g h Whatm a n G F / F glass fiber filters (0.70 p.m n o m i n a l p o r e size) at the end of the sampling day. T h e filters were i m m e r s e d in 90% a c e t o n e and stored frozen in glass centrifuge tubes. Frozen samples were analyzed for chl a using a T u r n e r 10 f l u o r o m e t e r a n d the standard acidification m e t h o d of L o r e n z e n (1966). At four of the stations samples were taken for p h y t o p l a n k t o n p r o d u c t i o n using 14C-carbon uptake at six depths t h r o u g h o u t the euphoric zone. In addition to these transects in d e e p c h a n n e l s in Willapa Bay, we r e c o r d e d water p r o p e r t i e s on intertidal mudflats. YSI m o d e l 6920 data sondes e q u i p p e d with f l u o r o m e t e r s were placed in PVC sleeves that were inserted vertically in the substrate. Sensors were 7-10 cm above the s e d i m e n t surface. During periods of e m e r s i o n only t e m p e r ature values were valid. T h e time series m e a s u r e m e n t s were used to c o m p a r e water p r o p e r t y values at +0.6 m M L L W at Stackpole and Nahcotta. OYSTER GROWTH We c o m p a r e d the growth of oysters on three spatial scales: Vertical position ( p e r c e n t aerial exposure), Cross-bank position (relative to the channel), and Regional position (relative to the m o u t h of Willapa Bay). Oysters were grown on PVC poles situated at known tidal elevations. T h e s e elevations c o r r e s p o n d e d to i m m e r s i o n times estimated f r o m h y p s o g r a p h i c curves. Poles were placed based on t o p o g r a p h i c s u r v e y s r e l a t i v e to n e a r b y b e n c h marks, and actual elevations were later adjusted by evaluating in situ t e m p e r a t u r e time series (as described above). T h e cross-bank distance b e t w e e n poles was standardized by e m e r s i o n a n d varied a m o n g sites due to variation in the slope of the mudflats. We used linear shell extension as the re-

1084

J.L. Ruesink et al.

T A B L E l. S t u d i e s o f o y s t e r g r o w t h in W i l l a p a Bay. T i d a l e l e v a t i o n s a c r o s s r n u d f l a t s w e r e d i f f i c u l t to a c h i e v e exactly, so we u s e d l o c a l t e m p e r a ~ , n - e r e c o r d s to d e t e r m i n e a c t u a l t i d a l e l e v a t i o n s . Dates

June 15 October 18, 1994

Initial oyster size (mm) Substrate Number of sites

90-150 Single oysters 1 (Nallcotta)

Tidal elevations vertically along poles (m) Tidal elevations across rnudflat (In)

Auguat 1 October 1S, 2000

June 20 August 18, 2001

August 20 October 1B, 2001

0.2-8.5 Ceramic tiles 9

8-8.9 Ceramic tiles 9

0.8, 1.1, 1.4, 1.7

5-25 Cultch S (a fom-th site contained poles at 0 rn MLLWonly) 0, 0.6, 1.2, 1.8

0, 0.6, 1.2, 1.8, 2.4

0, 0.6

0.8, 1.1, 1.4, 1.7

0, 0.6, 1.2, 1.8

0 (1.2 m at 2 sites)

0

sponse variable, and analysis of variance to evaluate spatial and temporal differences in growth. Experiments were carried out four times in three different years, with the details of the design varying as outlined below and summarized in Table 1. T h e first e x p e r i m e n t study took place at Nahcotta from J u n e 1 5 - O c t o b e r 18, 1994, and used yearling oysters placed in mesh bags at 0.8, 1.1, 1.4, and 1.7 m MLLW. These tidal elevations were achieved at four contours from channel to bank and also vertically t h r o u g h the water column. Each c o n t o u r and water c o l u m n position was replicated four times. Five oysters were placed in each bag and one set of oysters was planted directly on the tidal flat at each replicate to test for an enclosure effect. Linear shell growth was m e a s u r e d for each oyster. More recent studies used juvenile oysters within a few m o n t h s of settlement. T h e 2000 e x p e r i m e n t was c o n d u c t e d between August 1 - O c t o b e r 1S at four regional sites along the north-south axis of the estuary (Stackpole (ST), N a h c o t t a (NA), Shoalwater (SW), and Sunshine (SS) Sites, Fig. 1). Oysters had b e e n settled on adult oyster shell ( - 1 0 - 2 0 per cultch) the previous a u t u m n at a commercial hatchery. Oysters were grown at four intertidal elevations, 0, 0.6, 1.2, and 1.8 m MLLW, c o r r e s p o n d ing to full immersion (0% emersion), 20%, 40%, and 60% emersion, respectively. Different tidal elevations included four contours from channel to bank and vertical positions t h r o u g h the water column. Five replicate poles were placed parallel to shore along each c o n t o u r over a distance of a b o u t 50 m. Growth (nearest 0.5 mm) was d e t e r m i n e d by m e a s u r i n g the shell length of k n o w n individuals before and after the experiment. Subsamples of these oysters were analyzed for stable c a r b o n isotopes as described above. In 2001, we a d d e d sites but r e d u c e d the coverage from c h a n n e l to bank by placing most poles at 0 m MLLW. Two experiments were run. D u r i n g the J u n e 20-August 18 experiment, a fifth tidal elevation (+2.4 m, - 8 0 % emersion) was added. During the August 2 0 - O c t o b e r 14 experiment, we grew oysters at 0 (on-bottom) and 0.6 m only. For

these experiments, we used juvenile oysters that had been settled on the unglazed side of ceramic tiles (11 X 11 cm) a b o u t 6 wk prior to the study. T h e oysters were grown in the field until n e e d e d , and as a result the plates received some natural oyster settlement prior to being transplanted to study sites. We excluded all oysters < 3 m m initial length fi-om analysis. We used digital p h o t o g r a p h y to record the initial size (nearest 0.1 m m ) and position of each oyster ( R o e g n e r and M a n n 1995). Oysters were r e p h o t o g r a p h e d at the end of the exp e r i m e n t and individual growth rates determined. Sample size was initially five poles per site, but some losses o c c u r r e d and r e d u c e d replication at some sites. Linear growth rate of juveniles was calculated on a per cultch or per plate basis as the average c h a n g e in shell length of surviving juvenile oysters. Growth of yearling oysters was based on the average shell extension of all oysters in a bag. Because study design differed slightly a m o n g iterations, we asked several questions by selecting particular portions of the full data set. To examine oyster growth variation a m o n g sites and seasons we used early and late s u m m e r 2001 data fi-om nine sites and two elevations (0, 0.6 m MLLW or o n - b o t t o m and off-bottom, respectively) ; site, o n - v e r s u s off-bottom, and season were used as fixed factors in analysis of variance. This was our focal question because it implicitly addressed the relationship between resource patterns and benthic s e c o n d a r y productivity: Does oyster growth vary in any consistent way along a gradient of primarily oceanic to riverine influence? We then asked this question explicitly by regressing oyster growth on glsC. To examine the effect of intertidal elevation on oyster growth we used data fi-om 9 sites and 5 intertidal elevations in early 2001, corrected for tidal elevation based on estimates from t e m p e r a t u r e loggers. Site was a fixed factor and tidal elevation was a covariate in analysis of covariance. Effect of growing on- versus off-bottom when immersion time is constant was examined to see if oyster growth was altered by conditions close to a

Spatiotemporal Variation in Oyster Growth

1085

TABLE 2. Estimates of tidal elevation, tidal phase delay, and water temperature offset at nine sites in Willapa Bay. The minimization procedure did not work effectively for tidal phase delay, so best fit values were selected by hand in increments of 7.2 rain (0.005 d). Bay Center, Stony Point, Toke Point, and Range Point temperature records were from July 23 to August 12, 2001, in 20-min increments 1.2 m above the substrate, or fl'om August 22 to October 14, 2001, in 40-rain increments 0.6 m above the substrate; other sites ran from July 15 m August 4 or August 22 to October 14, 2001. n = number of temperature loggers. The substrate elevation was selected to be dose to mean lower low water (0 m). Bracketed nm:abers in the tidal phase delay colin:an are derived from NOAA predictions for nearby locations, available at htt-p://co-ops.nos.noaa.gov/tides. Substrate Elevation (SE, m MLLW)

Site (n)

Range Point (2) Toke Point (5) Stony Point (3) Bay Center (4) Stackpole (3) Nahcotta (5) Sunshine (4) Shoalwater (4) Long Island (2)

-0.37 0.84 -0.33 0.81 -0.56 0.20 -0.45 0.86 -0.51

(0.04) (O.OS) (0.05) (0.11) (0.09) (O.O8) (0.10) (0.09) (0.14)

Tidal Phase Delay (SE, Minutes) [Predicted]

9.6 0.5 0.5 20.0 10.3 28.8 31.9 41.6 39.1

m u d s u b s t r a t e , w h i c h c o u l d i n c l u d e b o u n d a r y layer effects ( l o w e r r e s o u r c e flux) a n d i n c r e a s e d turb i d i t y o r a c c e s s to b e n t h i c m i c r o a l g a l r e s o u r c e s . T h e analysis u s e d d a t a f r o m S t a c k p o l e , N a h c o t t a , a n d S u n s h i n e in 2000. W e s e l e c t e d t r e a t m e n t s t h a t w e r e g r o w i n g o n - b o t t o m a n d p a i r e d t h e m with oysters g r o w i n g o f f - b o t t o m at t h e s a m e tidal e l e v a t i o n on poles placed farther from shore. Three pairings w e r e p o s s i b l e , at + 0 . 6 (e.g., o n - b o t t o m at 0.6 m a n d 0.6 m o f f - b o t t o m at M L L W ) , 1.2, a n d 1.8 m M L L W . Site, on- v e r s u s o f f - b o t t o m , a n d tidal elev a t i o n w e r e f i x e d f a c t o r s in analysis o f v a r i a n c e . To c o m p a r e g r o w t h v e r t i c a l l y t h r o u g h t h e w a t e r c o l u m n a n d a c r o s s t h e m u d f l a t , t h e effects o f t i d a l e l e v a t i o n o n j u v e n i l e a n d y e a r l i n g oysters w e r e exa m i n e d u s i n g d a t a f r o m N a h c o t t a in 1994 (yearlings) a n d 2000 ( j u v e n i l e s ) . B e c a u s e t h e s t u d i e s w e r e p e r f o r m e d in d i f f e r e n t y e a r s f o r d i f f e r e n t d u r a t i o n s , a n d g r o w t h o f oysters slows with size (Kob a y a s h i et al. 1997), we w e r e n o t c o n c e r n e d w i t h d i f f e r e n c e s in g r o w t h overall b e t w e e n t h e two s t u d ies. W e w e r e i n t e r e s t e d in w h e t h e r j u v e n i l e s a n d y e a r l i n g s r e s p o n d e d d i f f e r e n t l y to i m m e r s i o n t i m e a n d p r o x i m i t y to t h e s u b s t r a t e . O y s t e r a g e ( - exp e r i m e n t ) a n d on- v e r s u s o f f - b o t t o m w e r e f i x e d factors, a n d tidal e l e v a t i o n was a c o v a r i a t e in a n a l ysis o f c o v a r i a n c e . Results ENVIRONMENTAL

GRADIENTS

T i d e s in W i l l a p a Bay a r e d e l a y e d by a b o u t 40 r a i n at t h e s o u t h e n d o f t h e e s t u a r y r e l a t i v e to t h e mouth. This result emerged from comparing the t i m e w h e n d r a m a t i c t e m p e r a t u r e shifts, i n d i c a t i n g w a t e r - t o - a i r t r a n s i t i o n s , o c c u r r e d a c r o s s sites (Fig. 2, T a b l e 2). W a t e r t e m p e r a t u r e s w e r e also w a r m e r away f r o m t h e m o u t h o f t h e bay. W a t e r t e m p e r a t u r e a n d tidal p h a s e d e l a y w e r e positively r e l a t e d

(0) [8] (2.9) [O] (1.9) (1.5) [24] (6.5) (2.4) [25] (2.4) [38] (4.6) (0.7) [38]

W~.ter Temperature Offset (SE, ~

1.28 0.26 -0.10 0.20 0.19 1.89 1.84 2.09 1.98

(0.28) (0.11) (0.26) (0.20) (0.12) (0.09) (0.22) (0.37) (0.42)

Extrapolated Maximum Tidal Elevation %r Oyster Survival (m MLLW)

1.85 1.60 1.66 1.70 2.03 2.07 2.19 2.13 --

( P e a r s o n ' s r - 0.866, n - 9, p < 0.01), b u t t h e points that deviate from the relationship should be n o t e d . R a n g e P o i n t , l o c a t e d a l o n g t h e W i l l a p a River c h a n n e l , was w a r m e r t h a n e x p e c t e d g i v e n t h e s h o r t t i m e it t o o k t h e t i d e to arrive. N a h c o t t a , o n t h e west s i d e o f t h e bay, was c o n s i d e r a b l y c o o l e r t h a n S u n s h i n e o n t h e east side, e v e n t h o u g h t h e i r tidal p h a s e d e l a y s w e r e similar. W a t e r t e m p e r a t u r e is a b e t t e r i n d i c a t o r o f coastal o c e a n i n f l u e n c e t h a n tidal p h a s e delay, b e c a u s e t e m p e r a t u r e c h a n g e s with t h e a r r i v a l o f n e w water, w h e r e a s t i d e s m a y o c c u r as l o c a l w a t e r m o v e s u p a n d d o w n . T h e best-fit t i d a l e l e v a t i o n c a l c u l a t i o n s b a s e d o n l o c a l t e m p e r a t u r e l o g g e r s i n d i c a t e d t h a t all o f t h e p o l e s w e r e p l a c e d b e l o w t h e i n t e n d e d level o f 0 m MLLD?. O y s t e r s w e r e t r a n s p l a n t e d to p a r t i c u l a r l y low e l e v a t i o n s at L o n g I s l a n d , S u n s h i n e , a n d Stackp o l e ( 0.45 to 0.56 m M L L W ; T a b l e 2). T h e s e a r e t h r e e o f t h e f o u r sites at w h i c h o y s t e r s s u r v i v e d o n p l a t e s p l a c e d 9.4 m a b o v e t h e s u b s t r a t e in e a r l y 2001; t h e f o u r t h site was S h o a l w a t e r . I n c o n c e r t with r i s i n g w a t e r t e m p e r a t u r e s , s t a b l e c a r b o n i s o t o p e r a t i o s o f oysters w e r e d e p l e t e d a l o n g a g r a d i e n t f r o m t h e m o u t h to t h e h e a d o f W i l l a p a Bay (Fig, 3). N e a r t h e o c e a n , ~1~C r a n g e d from 18%0 to 20%o in e a r l y s u m m e r 2001 a n d c e n t e r e d o n - 1 7 % o in late s u m m e r 2001. R a n g e P o i n t ( u p t h e W i l l a p a River) a n d sites at t h e s o u t h e n d o f t h e bay w e r e 3 - 5 % 0 l o w e r in glsC. I n a n a l ysis o f v a r i a n c e o f b o t h t r a n s p l a n t s in 2001, a sign i f i c a n t s e a s o n X site i n t e r a c t i o n e m e r g e d (Fs, ~s - 51,0, p < 0,001), T h e s e site-specific v a l u e s for s t a b l e c a r b o n i s o t o p e r a t i o s s u g g e s t t h a t oysters were consuming different resources across space a n d t i m e . S t a b l e c a r b o n i s o t o p e s also i n d i c a t e d t h a t oysters g r o w i n g o n - b o t t o m c o n s u m e d different resources than those growing off-bottom, with o n - b o t t o m oysters s i g n i f i c a n t l y e n r i c h e d in 81~C

'1086

J . L . Ruesink et al.

-17

A -18

4,

]~NA

-19

tx3

-20

I

-21

~SW o_

-22

SS

-23 -17

-18

BC,

I

9 On bottom O Off bottom

,

-19

~

-20

', I

sp{

NA

:z~Tp

j_

~SW

-21 RP

-22

SS o

I

]~ LI

!

-23 -16

C -17

Sp~Tp

ST

-18

o

NA

-19 I

ii

-20

I

-21

H

r

SW SS o

-22 -23

;

oRP

LI

r 0

1

( A N O V A o n - v e r s u s o f f - b o t t o m : F~.z~s - $8.5, p < 0.001; Fig. S). A v e r a g e 8~sC v a l u e s w e r e s t r o n g l y a n d n e g a t i v e l y r e l a t e d to w a t e r t e m p e r a t u r e a c r o s s sites (Early 2001: ~l~G 19.0-1.2ST, r 2 - 0.48, n - 9; L a t e 2001: ~lSC; 16.6-2.$9T, r ~ - 0.81, n - 9). D e p l e t e d v a l u e s o f 8~sC a r e c o n s i s t e n t with h i g h e r t e r r i g e n o u s c o n t r i b u t i o n s to t h e diet, as w o u l d b e e x p e c t e d at e s t u a r i n e sites c l o s e r to r i v e r mouths and farther from the ocean. O v e r two g r o w i n g s e a s o n s ( 1 9 9 9 - 9 0 0 0 ) , a m m o n i u m o c c u r r e d at c o n s i s t e n t l y h i g h e r c o n c e n t r a t i o n s in t h e c h a n n e l w h e r e t h e N o r t h a n d W i l l a p a Rivers e n t e r e d t h e b a y ( s t a t i o n 1) t h a n at m o r e o c e a n i c o r s o u t h e r n W i l l a p a Bay s t a t i o n s (Fig. 4). Nitrate concentrations showed a different pattern o f s p a t i a l v a r i a t i o n , s l i g h t l y h i g h e r at o c e a n i c stat i o n s b u t e x t r e m e l y v a r i a b l e at s t a t i o n 1. F o r c h l o r o p h y l l , c o n c e n t r a t i o n s w e r e h i g h e s t at o c e a n i c stations, b u t s t a t i o n 1 was also c o n s i s t e n t l y h i g h e r t h a n s t a t i o n 8. C h l o r o p h y l l o c c u r r e d at h i g h e r c o n c e n t r a t i o n s in t h e a r e a o f W i l l a p a Bay w i t h h i g h river i n p u t t h a n in t h e a r e a with low r i v e r i n p u t . P : g m e a s u r e m e n t s t a k e n f o u r t i m e s in A p r i l to J u l y 1999, i n d i c a t e d h i g h p h y t o p l a n k t o n p e r c a p i t a g r o w t h at s t a t i o n 1. P:B v a l u e s r a n g e d f r o m 1 0 50% h i g h e r at s t a t i o n 1 t h a n at o c e a n i c sites, alt h o u g h t h e s e h i g h a p p a r e n t g r o w t h r a t e s m a y in fact r e f l e c t low b i o m a s s e s t i m a t e s at t h e u p r i v e r station. Intertidally, water properties varied between S t a c k p o l e a n d N a h c o t t a c o n s i s t e n t with o c e a n i c f o r c i n g f r o m t h e e s t u a r y m o u t h (Fig. 5). Sites s p e n t s i m i l a r a m o u n t s o f t i m e e x p o s e d to air at low tide ( 2 0 % ) b u t w e r e s l i g h t l y o u t o f p h a s e . T e m p e r a t u r e s w e r e slightly l o w e r a n d s a l i n i t y h i g h e r at Stackpole, consistent with gradients throughout t h e e s t u a r y (Fig. 4). Low-pass f i l t e r e d c h l o r o p h y l l s h o w e d g e n e r a l l y h i g h e r levels at S t a c k p o l e , with t h e e x c e p t i o n o f s e v e r a l l a r g e p e a k s in c h l o r o p h y l l c o n c e n t r a t i o n at N a h c o t t a (Fig. 5).

2

Water temperature offset (~ Fig. 8. Stable carbon isotope ratios in tissue of juvenile oysters grown on- and off-bottom at sites in WiUapa Bay that differ in water temperature (a measure of departure from ma~ne conditions, parameter C in Eq. 1). (A) Four sites sampled in 2000. For on-bottom oysters, each point averages g-5 values, and for off-bottom oysters, each point averages 8-16 values throughout the water column. (B) Nine sites sampled in early stmmler 2001 (June-August). (C) Nine sites sampled in late summer 2001 (August-October). Error bars show standard errors. For clarity, temperature variation at each site is not induded for off-bottom points.

OYSTER GROWTH

G r o w t h r a t e s o f j u v e n i l e Pacific o y s t e r v a r i e d spad a l l y in W i l l a p a Bay, a n d t h e r e l a t i v e p e r f o r m a n c e c h a n g e d b e t w e e n e a r l y a n d late s u m m e r 2001: t h e r e was a s t r o n g s e a s o n >4 site i n t e r a c t i o n in A N O V A (F~, 209 - 2.48, p - 0.02; Fig. 6). Survival r a t e s did not vary among locations: ANOVA on in-transf o r m e d survival r e v e a l e d n o s i g n i f i c a n t effects o f site, o n - v e r s u s o f f - b o t t o m , o r t h e i r i n t e r a c t i o n in early s u m m e r 2001. S i m i l a r c a l c u l a t i o n s in o t h e r s e a s o n s w e r e h a m p e r e d by n a t u r a l r e c r u i t m e n t . Survival o f n e w l y - s e t t l e d j u v e n i l e oysters a v e r a g e d a l m o s t 4 0 % , a n d a l m o s t all s h e l l s o r tiles c o n t a i n e d a few survivors. H i g h e s t s e c o n d a r y p r o d u c t i o n , as i n d i c a t e d by o y s t e r g r o w t h , o c c u r r e d a l o n g t h e Will a p a River a n d n e a r t h e m o u t h o f W i l l a p a Bay,

Spatiotemporal Variation in Oyster

Growth

1087

y

1999 I

9

A

2

2000 i

I

D

(

1

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