AQUACULTURE ENVIRONMENT INTERACTIONSAquacult Environ Interact

Vol. 7: 2947, 2015doi: 10.3354/aei00131

Published online June 8

INTRODUCTION

Both seagrasses and reef-forming bivalves serve avariety of important ecological functions in estuaries,including: enhancing biodiversity and providingstructured nursery habitat and refuge from predatorsfor fish and invertebrates (e.g. seagrasses: Bostrom etal. 2006, Gillanders 2007, Heck et al. 2008; bivalves:Coen et al. 1999, Gutierrez et al. 2003, Grabowski etal. 2008), water column filtration and water propertyenhancement (particularly bivalves as phytoplank-ton grazers; Prins et al. 1998, Newell 2004, Ferreira etal. 2011), sediment accretion and erosion controlthrough current modification (seagrasses: Peralta et

al. 2008, Koch et al. 2009; oysters: Smith et al. 2009,Scyphers et al. 2011), carbon sequestration (sea-grasses: Mateo et al. 2007, Fourqurean et al. 2012),and finally, as foraging areas for waterfowl andshorebirds (both seagrasses and bivalves; Caldow etal. 2007, Rivers & Short 2007, Anderson & Lovvorn2012). Reef-forming bivalves and seagrasses are alsodeclining worldwide due to numerous anthropogenicdisturbances, including eutrophication, wetland fill-ing and diking, fishing, and dredging (Orth et al.2006, Waycott et al. 2009, Beck et al. 2011, ZuErmgassen et al. 2012). These declines have led toefforts to protect and restore seagrass and bivalvepopulations, as well as an increased focus on identi-

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*Corresponding author: brett.dumbauld@ars.usda.gov

Effect of oyster aquaculture on seagrass Zostera marina at the estuarine landscape

scale in Willapa Bay, Washington (USA)

Brett R. Dumbauld*, Lee M. McCoy

Agricultural Research Service, US Department of Agriculture, Hatfield Marine Science Center, Newport, OR 97365, USA

ABSTRACT: Both seagrasses and bivalve shellfish provide valuable ecosystem services in estuar-ies worldwide. Seagrasses are protected by no-net-loss provisions in US federal and state regula-tions, resulting in precautionary management that avoids any direct impacts from developmentactivity, including shellfish aquaculture. Recent research suggests that oyster aquaculture hasdirect impacts on native seagrass (eelgrass Zostera marina) at small spatial and short temporalscales in US west coast estuaries. We quantified impacts of oyster aquaculture on Z. marina at theestuarine landscape scale in Willapa Bay, Washington. A model of Z. marina cover outside ofaquaculture was created using distance to estuary mouth, distance to nearest channel, salinity,elevation, and cumulative wave stress as factors, and was then used to predict Z. marina distribu-tion within oyster aquaculture beds and compared to an inverse distance interpolation of pointsoutside of aquaculture. The amount of Z. marina cover observed within oyster aquaculture bedswas less than predicted, but represented

Aquacult Environ Interact 7: 2947, 2015

fying and mitigating the factors that are negativelyimpacting each of them (Brumbaugh & Coen 2009,Schulte et al. 2009, Orth et al. 2010a, Thom et al. 2012).

Bivalve shellfish aquaculture acts as an anthro-pogenic disturbance to seagrass, but can also posi-tively interact with seagrass and may restore some ofthe services lost where native bivalve populationshave declined (reviewed by Dumbauld et al. 2009,Forrest et al. 2009, Coen et al. 2011, McKindsey et al.2011). The interactions between bivalve shellfishaquaculture and seagrasses have been widely stud-ied at the experimental scale, particularly those be -tween Pacific oysters Crassostrea gigas, cultured inmany estuaries worldwide, and eelgrass Zosteramarina, a common temperate species of seagrass.Shellfish influence seagrass via 3 primary mecha-nisms: physical structure of shells/reefs, nutrientaddition to sediments and water column via excre-tion, and increased water clarity via filtration. Oys-ters are expected to compete for space with seagrass,especially when they are cultured directly on thesediment surface. Research on oyster aquaculture inWillapa Bay, Washington on the US west coast sug-gests that this interaction is nonlinear and thresholdsoccur above which shoot density of Z. marina de -clines markedly (Wagner et al. 2012). Oysters grownon structures can have additional physical effects, in -cluding shading and sediment erosion around thestructure. These factors caused 75% reduction in eel-grass cover relative to controls for oyster stake cul-ture and up to 100% loss of eelgrass under oysterracks (Everett et al. 1995), yet oysters grown on long-lines with more open space caused little reductionin eelgrass density and cover (Wisehart et al. 2007,Tallis et al. 2009). Further study suggested that eel-grass metrics scaled with spacing between these oys-ter lines and that both shading and dessication fromstranding over the lines contributed to the effect(Rumrill & Poulton 2004). Experimental evaluationsof the effects of shading due to oyster culture in sus-pended bags and hanging culture of floating oysterbags showed reduced eelgrass structure, morpho-metrics and photosynthesis observed at 26% reduc-tion in subsurface irradiance, but design of the struc-tures was clearly important, as the floating bags onlyreduced eelgrass directly below the structures (Bul-mer et al. 2012, Skinner et al. 2014). Bivalves havealso been shown to enhance seagrass growth by sup-plying nutrients via biodeposits and by improvingwater clarity via filtration, especially where nutrientsin sediment limit seagrass growth and in eutrophicwaters where phytoplankton blooms cause shadingeffects (Peterson & Heck 2001, Booth & Heck 2009,

Burkholder & Shumway 2011). Though nutrientsin sediment porewater were enhanced by the pres-ence of oysters in Willapa Bay (Wagner et al. 2012)and oysters measurably cleared the water (Wheat &Ruesink 2013), only eelgrass shoot size was affectedby oysters at the local scale (Wagner et al. 2012), sug-gesting that seagrass response differs depending onestuarine conditions.

Seagrasses have been shown to be sensitive to awide variety of pulse disturbances with parallels tomechanical implements used to harvest shellfish (e.g.boat propellors, anchors, and moorage chains: Daweset al. 1997, Thom et al. 1998; dredge and fill operationsand simple trampling: Erftemeijer & Lewis 2006). Shell -fish harvest practices have been less studied, but me-chanical harvest implements directly removed plantsand generally caused more disturbance than hand har -vest or off-bottom longline oyster culture techniquesin Willapa Bay (Wisehart et al. 2007, Tallis et al. 2009).

Most of the experimental studies outlined abovedescribe effects of oyster aquaculture on seagrass atsmall spatial and short temporal scales. There hasbeen an extensive amount of effort devoted to usingremote sensing to understand seagrass dynamicsat larger estuarine landscape scales, particularly inestuaries where other anthropogenic disturbancessuch as eutrophication are more likely to affect change(Kendrick et al. 2000, Dekker et al. 2007, Orth et al.2010b, Lyons et al. 2013), but only recently haveinvestigators addressed impacts of shellfish aquacul-ture on seagrass at this scale (Ward et al. 2003, Car-swell et al. 2006, Barille et al. 2010, Martin et al. 2010,Bulmer et al. 2012). Willapa Bay provides a uniqueopportunity to examine this interaction at the estuar-ine landscape scale because shellfish aquaculturewithin eelgrass was not restricted prior to 2007 whena new permit (US Nationwide Permit 48) was issuedby the US Army Corps of Engineers (US ACOE) withprotection for native eelgrass Z. marina. This permitdid not influence the placement or activities on privately owned or leased aquaculture beds, but ifthese activities occurred in eelgrass, pre-construc-tion notification was required and any expansion ofaqua culture must leave buffers for eelgrass. Initial landscape-scale estimates from Willapa Bay clearlyde picted reductions of eelgrass cover on individualbeds, but suggested that when averaged over spaceat similar tidal elevations, the proportion of area witheelgrass present inside and outside of oyster culturegrounds was similar (Dumbauld et al. 2009). Here wefurther that effort for this estuary by first constructinga model to predict seagrass distribution outside ofaquaculture using several factors that we suspected

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Dumbauld & McCoy: Landscape effects of aquaculture on seagrass

could influence the distribution of Z. marina and forwhich we had spatial data to create layers, includingdistance to estuary mouth, distance to nearest chan-nel, salinity, elevation, and cumulative wave stress.We then use these factors to predict Z. marina distri-bution for each aquaculture bed and compare themodel-predicted, interpolated, and actual quantitiesof Z. marina. Our study had several related objec-tives: (1) quantify the distribution of Z. marina andoyster aquaculture in this estuary, (2) quantify theoverall impact of oyster aquaculture on Z. marina,(3) determine the relative impact of different oysteraqua culture harvest methods and bed types, and (4)determine whether any impacts of oyster aquacul-ture on Z. marina were chronic or transitory by ana -lyzing data from 3 separate years.

MATERIALS AND METHODS

Study site

Willapa Bay, Washington (46 N, 124 W; Fig. 1) is amacrotidal estuary on the US Pacific coast, with alarge tidal exchange and a well-mixed water columnheavily influenced by tidal exchange near the estu-ary mouth, especially during summer months (Banaset al. 2007). It is the third larg