Chapter 4 Bivalve fi lter feeding: variability and limits of the aquaculture biofi lter

Peter J. Cranford , J. Evan Ward , and Sandra E. Shumway

Introduction acquisition, which is regulated by feeding activity (Hawkins et al. 1999 ). Predictions of A fundamental knowledge of bivalve feeding bivalve growth and the maximum aquaculture behavior is a minimum requirement for under- yield that can be produced within an area (pro- standing how aquaculture interacts with the duction carrying capacity) often involve eco- surrounding ecosystem. The potential environ- physiological modeling, which includes mental effects and ecological services of bivalve equations describing how feeding processes culture (Chapters 1 and 9 in this book) are (particle capture, selection, and ingestion) are related, in large part, to how the cultured pop- related to population dynamics and environ- ulation interacts with the ecosystem by means mental changes. Uncertainty or inaccuracy in of suspension feeding. A close interplay feeding parameter estimates strongly infl uence between water fi ltration activity, primary pro- model predictions of bivalve growth and car- duction, seston availability, and hydrodynam- rying capacity (Dowd 1997 ). ics defi nes the magnitude of many of the Suspension feeding always results in some ecological services provided by bivalves, as local food depletion. The ecological costs of well as the sustainable level of aquaculture for seston depletion by bivalve aquaculture are a given area. Shellfi sh growth is limited pri- of concern only when the depletion zone is marily by a species ’ capacity for nutrient persistent and of an ecologically signifi cant

Shellfi sh Aquaculture and the Environment, First Edition. Edited by Sandra E. Shumway. © 2011 John Wiley & Sons, Inc. Published 2011 by John Wiley & Sons, Inc.

81 82 Shellfi sh Aquaculture and the Environment magnitude and spatial scale. Accurate informa- ence of predictive relationships for the clear- tion on how fast resident bivalve stocks can ance rate of key aquaculture species that can fi lter a body of water is required to assess the be used to help understand both positive and ecological carrying capacity of a region, which negative interactions between bivalve aquacul- is the level of aquaculture that can be supported ture activities and the environment. Our goal in the growing environment without leading to was to synthesize knowledge on specifi c aspects signifi cant changes to ecological processes, of bivalve feeding behavior relevant to the species, populations, or communities (Gibbs aquaculture issues outlined above. Several pre- 2007 ). Beyond the need to understand the viously published reviews have addressed potential direct effects of biofi ltration, indirect divergent hypotheses on physiological regula- effects on ecosystem processes and structure tion of feeding activities and autonomous may result from the by- products of suspension behavior (Jø rgenson 1996 ; Bayne 1998 ; feeding, including ammonia excretion and the Riisg å rd 2001b ). Such considerations are not egestion of particulate organic materials (feces the focus of this review, but it is not possible and pseudofeces) on marine particle transport, to address our task without contributing to energy fl ow, and nutrient cycling. this long - standing theoretical debate. Bivalve feeding activity has been studied across a wide range of laboratory and natural conditions and there is a vast literature, par- Constraints on m aximum ticularly on clearance rate, which is the volume f eeding a ctivity of water cleared of particles of a certain size in a period of time. Despite this large research Suspension - feeding lamellibranchiate bivalves effort, there remains uncertainty in the mea- rely on ciliated structures to capture and trans- surement of clearance rate, which affects our port suspended particulate matter for selection confi dence in predictions of individual to and ingestion. The particle capture organ is the community - level feeding rates (Doering and ctenidium (Ward et al. 1998 ), which also Oviatt 1986 ; Cranford and Hill 1999 ; Riisg å rd serves as the respiratory organ (gill). The asyn- 2001a, 2001b, 2004 Cranford 2001 ; Widdows chronous beating of lateral cilia on gill fi la- 2001 ; Bayne 2004 ; Petersen et al. 2004 ). A ments serves as a pump that creates a water fundamental understanding of the feeding current which fl ows into the inhalant siphon behavior of individual bivalves provides the or aperture, through the spaces between the foundation for estimating population clear- gill fi laments (or ostia) and then out of the ance rate, which is critical to understanding exhalent siphon or aperture. Particles sus- the ecological role of bivalves and environ- pended in the feeding current are captured on mental interactions with shellfi sh culture, the gill. An in - depth review of food capture, including the capacity of dense bivalve assem- transport, and processing mechanisms in blages to control the phytoplankton at the bivalve molluscs is provided by Ward and coastal ecosystem scale (Chapter 5 in this Shumway (2004) . book). Feeding rate measurements must refl ect The ciliary activity of the gill delivers a fl ow the actual responses of specifi c species and cul- that can be measured as a pumping ( = ventila- tured populations to the multiple physical, tion) rate ( P ; L h − 1 ) by various means such as chemical, and biological factors that can infl u- the constant - level apparatus developed by ence feeding behavior in the natural environ- Galtsoff (1926) , the delivery of exhaled seawa- ment. In this review, we summarize the ter into a constant fl ow of fresh water available literature pertaining to feeding (Davenport and Woolmington 1982 ), the laser behavior with a focus on ascertaining the pres- apparatus developed by Famme et al. (1986) , Bivalve fi lter feeding 83 the use of micro- fl ow meters (Meyhö fer 1985 ; clearance rate and fi ltration rate interchange- Jones et al. 1992 ), and by the application of ably, but the latter term is more often used to particle image velocimetry (Frank et al. 2008 ). defi ne the mass of particles cleared per unit Pumping rate scales with the size of the gill, time (e.g., mg h − 1 ). Clearance and pumping which is somewhat proportional to the square rates are equal if all particles in the inhalant of shell length ( L 2 ). Tissue dry weight (W ) is current are removed from suspension. Small proportional to L 3 so pumping rate can, at particles (< 2 - μ m diameter) in natural waters least in theory, be expected to scale with W2/3 are not effectively retained by most species, ( = W 0.67 ). This translates into a large increase but these particles can account for a high pro- in pumping rate for a small increase in body portion of the total suspended particulate size ( L or W ). These relationships are described matter. Clearance rate, therefore, is measured by the allometric equations for a particle size range that is retained by the species with 100% effi ciency ( > 4 - to 7 - μ m PaW==bband PaL , (4.1) diameter, depending on the presence of eu- or pro -laterofrontal cilia, respectively; reviewed where a and b are fi tted parameters. The allo- by Riisgå rd 2001a ). While pumping rate can metric exponent (b ) describes how fast the rate be measured directly by a number of methods, increases relative to body size. Jones et al. clearance rate is most often determined using (1992) reported that maximum pumping rate indirect methods that involve measuring for Mytilus edulis scaled with L 2.1 (Fig. 4.1 ) changes in particle abundance or concentra- and W 0.70 , and showed that that these allome- tion due to suspension- feeding activity of the tric coeffi cients were not signifi cantly different bivalves. from the predicted values. Under laboratory conditions, optimal food Clearance rate (C ; L h − 1 ) is the more gener- concentrations have been identifi ed that stimu- ally used measure of water processing than late the full exploitation of water pumping and pumping rate, although the two measures are particle clearance capacity in many species of closely related. Some studies use the terms bivalves (e.g., 1000– 6000 Rhodomonas sp. cells mL − 1 for Mytilus edulis ; Kittner and Riisg å rd 2005 ). Riisgå rd et al. (2003) reported 3.5 2.09 that under these conditions, the valves of Pmax = 0.0002 (L ) 2.19 Cardium edule, Mytilus edulis, and Mya are-

) 3.0 Pmean = 0.0004 (L ) –1 naria are fully open within an hour after a 2.5 starvation period of at least 24 h, and maximum 2.0 clearance rate (C max ) is thereafter maintained.

1.5 The results of Cmax measurements on 13 bivalve species of different sizes from eight studies 1.0 have been summarized by Riisg å rd (2001a, Pumping Rate (L h 0.5 2001b) . Reanalysis of the parameters of the 0.0 allometric relationships reported in these eight 10 20 30 40 50 60 70 80 studies provide the following average ( ± stan- Length (mm) dard deviation [SD ]) relationships for dry Figure 4.1 Allometric relationship between pumping rate tissue weight (W ) and shell length (L ): ( P ) of the mussel Mytilus edulis and shell length (L ). Multiple individual measurements for each mussel are shown, −±10=± ..72009 ᭛ CWmax ()..Lh 654 241 (4.2) including the maximum (P max ; ). Regression lines and equations are shown for average P (P mean ; broken line) and −±11=±..60045 Pmax (solid line) values. (Redrawn from Jones et al. 1992 .) CLmax ().Lh 0 0036 0 . 10 (4.3) 84 Shellfi sh Aquaculture and the Environment

As noted above, clearance rate is theoretically the external pressure fi eld caused by fl ow expected to scale with body geometry ( L2 and velocity (Wildish and Kristmanson 1997 ). W 0.67 ), and the above equations generally Back - pressure on the ciliary pump results confi rm the assumed constraints of body size in reduced pumping effi ciency and valve on maximum feeding activity. The exponent closure (J ø rgenson 1990 ; Wildish and Saulnier ( b ) in Equation 4.3 is lower than expected 1993 ). Similar effects of fl ow velocity have owing largely to the results of Meyh ö fer been observed for infaunal bivalves (Cole (1985) , which were conducted over a narrow et al. 1992 ), and appear to result from the size range. The median b -value of L 1.81 may reduced ability of the bivalve to draw water therefore be a more accurate estimate. into the mantle cavity when there is a high Fluid dynamic forces can control the ability cross - fl ow. of shellfi sh to clear food particles. Uncertainty Temperature and salinity also serve as con- in the literature regarding the effect of current straints on the maximum feeding rate of speed on bivalve feeding (positive vs. negative suspension - feeders. Temperature effects are relationship) appears to stem from experimen- related to a combination of mechanical (fl uid tal conditions (Ackerman 1999 ). Turbulent dynamic) and physiological effects. At a scale conditions tend to result in a negative relation- of individual cilia, viscous forces dominate ship between feeding activity and current cilia and water motion. Water viscosity is speed, whereas the opposite is generally inversely related to temperature, and the observed under laminar fl ow conditions. In higher viscosity at lower temperatures has general, there appears to be a unimodal func- been shown to account for a large fraction tional response to fl ow: Moderate current of the effect of temperature on water pump- speed and laminar fl ow conditions promote ing by ciliary fi lter - feeders, including bivalves particle clearance rate, whereas high speeds (J ø rgenson et al. 1990 ; Podolsky 1994 ). and turbulent conditions inhibit clearance Viscosity affects the resistance of water fl ow (reviewed by Ackerman 1999 ). The range of within the shellfi sh pump, and the viscosity/ velocities permitting maximal feeding and temperature relationship therefore limits their shellfi sh growth depends on the species. For maximum clearance rate (Kittner and Riisgå rd example, maximum clearance rate of Mytilus 2005 and references cited therein). Salinity edulis was reported at ∼ 25 cm s − 1 (Wildish fl uctuations also can severely disrupt normal and Miyares 1990 ) and 80 cm s − 1 (Widdows et feeding physiology (e.g., Navarro and Gonzá lez al. 2002 ), whereas Mytilus trossulus and 1998 ; Gardner and Thompson 2001 ). Some Mytilus californianus exhibited peak rates at species within the same taxon exhibit increased ∼ 18 and 12 cm s − 1 , respectively (Ackerman and tolerance to low - salinity environments, result- Nishizaki 2004 ). The scallop Placopecten ing in differentiation of some species distribu- magellanicus exhibited fl ow inhibition at tions (Seed 1992 ). 20 – 25 cm s − 1 (Wildish et al. 1987 ; Pilditch The maximum capacity for food intake is and Grant 1999 ), while the cockle Cerasto- ultimately limited by the morphological con- derma edule showed no inhibitory effects at straint of a limited gut volume and the time 35 cm s − 1 (Widdows and Navarro 2007 ). The required to digest food. Both factors impose a reduction in feeding rate with increasing major bottleneck on food uptake that morpho- fl ow velocity appears to be a response of epi- logical and physiological adaptations (e.g., faunal bivalves to a fl ow - induced pressure dif- active regulation of feeding rates) may help to ferential between the pressure fi eld in the mitigate (Hawkins and Bayne 1992 ; Bayne mantle cavity, created by the ciliary pump, and 1998 ). Bivalve fi lter feeding 85

Shellfi sh f eeding in n ature potential reasons for this variability in the following section. Shellfi sh are opportunistic feeders that exploit the diverse nature of suspended particulate matter (the seston). The types of food utilized Temporal v ariability in by shellfi sh include phytoplankton, ciliates, c learance r ate fl agellates, zooplankton, and detritus, which occur within a spatially and temporally diverse Water pumping and clearance rate may be mixture that includes inorganic materials (e.g., actively controlled by changing the activity of Trottet et al. 2008 ). Studies of the natural food the lateral cilia of the gill that create the water available to suspension - feeding bivalves in fl ow, and by controlling various musculature coastal waters reveal marked short - term to that affects shell gape (valve opening), exhalent seasonal variations in the concentration, com- siphon area (Jø rgenson et al. 1988 ; Newell et position, and nutritional value of the seston al. 2001 ), and interfi lamentary distance of the (e.g., Fegley et al. 1992 ; Cranford et al. 1998, gill (J ø rgensen 1990 ; Medler and Silverman 2005 ; Cranford and Hill 1999 ). Long - term 2001 ; Gainey et al. 2003 ). These mechanisms changes in seston abundance and composi- appear to be uncoupled (Newell et al. 2001 ; tion in temperate waters arise primarily from Maire et al. 2007 ), possibly responding to dif- the seasonal cycle of primary production. ferent stimuli and/or providing different Variability on a scale of days to weeks can degrees of control over water fl ow and food result from algal blooms, horizontal phyto- acquisition. The capacity of shellfi sh to actively plankton patchiness, storm- induced resuspen- control clearance rate is a key factor in deter- sion of bottom deposits, or the spring/neap mining food acquisition, and individual shell- tidal cycle. In many coastal systems, fi ne - scale fi sh appear to vary feeding activity continuously. fl uctuations in the seston are superimposed on Direct continuous measurements of water these longer - term trends and result largely pumping rate in Mytilus edulis by Davenport from tide- induced resuspension and deposition and Woolmington (1982) showed that under of bottom deposits and associated organic and optimal laboratory conditions (constant algal inorganic constituents. The increase in the cell diet) mussels demonstrate relatively low proportion of inorganic particles in the water temporal variability in pumping rate, but with column during resuspension events has a irregular and sometimes large interruptions “ dilution ” effect on food quality, which is gen- (Fig 4.2 A). Variable diets (periodic starvation), erally defi ned in terms of the organic and/or however, induced large fl uctuations in pumping elemental content of seston. The challenge to rate. The large degree of variability in individ- shellfi sh ecophysiologists has been to charac- ual pumping rates is also shown in Figure 4.1 B, terize feeding responses over this wide range which includes data on the full range of mea- of feeding conditions, as well as to other surements from mussels of different size, potential mediating factors. The intent of such including the maximum rate discussed above studies is to provide accurate predictive rela- (Jones et al. 1992 ). Studies utilizing natural tionships between changes in food quantity seston as the food source typically show large and quality and feeding activity. In this section, short - term variations in clearance rate over we will characterize the range of temporal and time periods ranging from minutes to hours, spatial variability in clearance rate responses including periodic cessation of all feeding measured across a wide range of natural and activity (Fig. 4.2 B and Fig. 4.2 C). Strohmeier experimental conditions prior to discussing et al. (2009) showed that large variations in 86 Shellfi sh Aquaculture and the Environment

(A) ) (C) ) 60

60 –1 –1 50 40 40 30

20 20 10

0 Pumping Rate (mL min 0 02468 Clearance Rate (L ind. h 0 6 12 18 24 30 36 42 48 52 Time (h) Time (h) )

–1 (D) (B) 100

mg 0.6

–1 80 Feeding Chamber 0.4 60

40 0.2 20 In situ Benthic 0 0 0 20 40 60 80 100 120 140 160 180 200 0 6 12 18 24 30 Siphon Diameter (% maximum) Clearance Rate (L min Time (min) Time (h)

Figure 4.2 Examples of short - term variations in shellfi sh feeding activity. (A) Continuous direct measurements of pumping rate of one Mytilus edulis during constant supply of an algal cell diet (5 × 103 cells mL − 1 ) (Davenport and Woolmington 1982 ). (B) M. edulis clearance rate of natural seston ( • , 5.5 mg L − 1 ; ᮀ , 2.5 mg L − 1 ) in fl ow - through feeding chambers (redrawn from Fré chette and Bourget 1987 ) . (C) Changes in clearance rate of 12 individual queen scallops ( Pecten maximus; the symbols identify each scallop) feeding on natural seston in fl ow - through feeding chambers (redrawn from Strohmeier et al. 2009 ). (D) Percent maximum exhalent siphon area of M. edulis measured in situ ( • ) and in feeding chambers (᭿ ) (Newell et al. 2005 ).

short - term clearance rate responses of individ- and this relationship can differ between indi- ual Mytilus edulis and Pecten maximus occur viduals and within an individual over different under relatively constant environmental con- periods of time. MacDonald et al. (2009) ditions and that this variation was not synchro- reported that exhalent siphon area explained nized with other individuals (Fig. 4.2 C). a maximum of 53% of clearance rate varia- Observations of shell gape and exhalent tions in Mytilus edulis and that the correlation siphon area have been used to study feeding appeared to differ with mussel size. Valve gape behavior under both controlled laboratory and exhalent siphon area do infl uence water conditions (Newell et al. 1998 ; Riisg å rd et al. fi ltration to varying degrees, but these mea- 2003 ; Frank et al. 2007 ; Maire et al. 2007 ) surements should not be interpreted as being and naturally variable environmental condi- synonymous with clearance rate. The true tions (Newell et al. 1998, 2005 ; Dolmer 2000 ; value of these measurements is in their Saurel et al. 2007 ). Frank et al. (2007) showed utility to provide semicontinuous measure- that valve gape accounts for an average of only ments that can reveal general trends in feeding 25% (range of 2 – 82%) of the variation in behavior (Frank et al. 2007 ; MacDonald et al. clearance rate in oysters (Frank et al. 2007 ), 2009 ). Bivalve fi lter feeding 87

Newell et al. (2001) demonstrated that Average s tandardized c learance r ates exhalent siphon area is more closely related to clearance rate than valve gape (see also Maire Rate s tandardization and a llometries et al. 2007 ), and in situ video observations in For comparative purposes, water processing a benthic mussel population in Maine, USA, rates of bivalves have generally been standard- showed large short- term variations in mussel ized to a 1- g (dry tissue weight) individual feeding activity and feeding rates that were using the following formula: typically less than 50% of the maximum (Fig. 4.2 D). Analysis of underwater photos of a = b mussel population in Limfjorden, Denmark, YYWse(),1/ e (4.4) over a 4 - day period showed that between 17% and 69% of the mussels were inactive (closed; where Y s and Ye are the corrected and experi-

Dolmer 2000 ). The highest percentage of mental physiological rates, respectively, W e is closed mussels corresponded with a period of the weight of the experimental animal, and b low food availability ( < 0.5 μ g chlorophyll a is the allometric exponent. Determining the [ Chl ] L − 1 ), but a signifi cant fraction of the pop- appropriate exponent to use is a critical deci- ulation was inactive even when suffi cient food sion as the accuracy of the standardized value was present. This study estimated that the degrades exponentially as the b - value is pro- gaping mussels were feeding at rates averaging gressively over- or underestimated. Selection of 55% (range: 27– 98%) of their maximum a b - value from the literature and comparisons capacity. Saurel et al. (2007) used a similar between reported values requires some precau- approach to observe mussel feeding behavior tions (see below). Utilizing body mass to stan- in the Menai Strait, UK, and showed that indi- dardize clearance rate is merely a practical viduals continuously varied feeding activity proxy for describing the effect of gill size between zero and maximum over a 48- h (surface area). A complication is that seasonal period, with an average feeding rate of between changes in body mass are unrelated to gill size 39% and 46% of maximum capacity. (fl uctuations in internal nutrient stores and Field studies of temporal variations in clear- reproductive tissues fl uctuates) and this intro- ance rate show a high degree of feeding vari- duces standardization errors that can compli- ability over tidal to seasonal time scales (Fig. cate clearance rate comparisons both within 4.3 ), with the transition between low, and between studies. Shellfi sh condition index, medium, and maximum clearance rates some- which refl ects seasonal cycles in nutritional times occurring over very short periods (e.g., and reproductive states, should be considered Bayne and Widdows 1978 ; Thompson 1984 ; when comparing weight - standardized feeding Deslous -Paoli et al. 1987 ; Fr é chette and rates. The true relationship between water Bourget 1987 ; Cranford and Hargrave 1994 ; processing rate and gill size may be more accu- Smaal and Vonck 1997 ; Smaal et al. 1997 ; rately related to shell length than to body Newell et al. 1998 , Cranford et al. 1998 ; weight (e.g., Filgueira et al. 2008 ). However, Cranford and Hill 1999 ; James et al. 2001 ; mean annual length/weight relationships can Wong and Cheung 2001b ; MacDonald and vary greatly between geographic locations Ward 2009 ; Strohmeier et al. 2009 ). These and, under this scenario, gill size may be more studies, as well as the preponderance of accurately indicated, for comparative pur- research on bivalve feeding physiology, point poses, by animal weight than by shell length. to the high fl exibility inherent within bivalve The majority of results presented on the species to alter feeding behavior over different maximum clearance capacity of different shell- temporal scales. fi sh species (above) come from populations in 88 Shellfi sh Aquaculture and the Environment

6 (A) Mytilus edulis

4

2

0 AMJJASOND 6

) Placopecten magellanicus

–1 (B) h –1 4

2 Clearance Rate (L g 0 AMJJASOND 14 (C) Crassostrea gigas 12 Cerastoderma edule 10 8 6 4 2 0 MA MJJASONDJF

Figure 4.3 Seasonal variation in standardized clearance rate of (A) the blue mussel Mytilus edulis, (B) the sea scallop ( Placopecten magellanicus ), and (C) the cockle Cerastoderma edule and oyster Crassostrea gigas . Solid lines in panels A and B are calculated from data reported in Cranford and Hill (1999 ). Discrete measurements are from Smaal et al. ( 1997; ᭿ ) and Smaal and Vonck ( 1997 ; • ) for M. edulis , MacDonald and Thompson ( 1986 ; ᭜ ) for P. magellanicus , and Deslous - Paoli et al. (1987) for C. edule and C. gigas .

Denmark, which may help to explain the rela- other researchers can more effectively make tively low variability in allometric parameters comparisons between studies. given in Equations 4.2 and 4.3 . We recom- The allometric relationship between clear- mend that the selection of a standardization ance rate and body size of 21 species is sum- method be based on the specifi c goals of the marized in Table 4.1 . This summary only study (e.g., understanding spatial vs. temporal includes studies not previously reviewed by variation), and that both the experimental Winter (1978) and Riisgå rd (2001a, 2001b) . animal weight and length be reported so that The values of the allometric exponent for dry Table 4.1 Clearance and pumping rate (C and P ; L h − 1 ) as a function of the size of different shellfi sh species according to the allometric equation Y = aXb , where Y is C or P , and X is dry tissue weight ( W ; g) or shell length ( L ; mm).

Species and reference Size T ( ° C) n Weight relationship Length relationship

Argopecten purpuratus Navarro and 0.1 – 5.7 g 12 15 C = 2.45 W 0.80 Gonz á lez (1998) Aulacomya ater Stuart (1982) 0.005 – 2.1 g 12.5 86 C = 1.48 W 0.59 Van Erkon 10 – 60 mm 15 — C = 0.89 W 0.81 C = 8.4 × 10 − 5 L 2.29 Schurink and Griffi ths (1992) Cerastoderma edule Smaal et al. — 9.5 – 15 53 C = 2.59 ± 0.12 W 0.51 ± 0.02 (1986) * Smaal et al. 0.03 – 1.4 g 1.4 – 18.5 134 C = 1.44 W 0.69 (1997) * Urrutia et al. — — — C = aW 0.57 (1996) Newell and 10 – 40 cm — 68 C = 0.60 W 0.51 Bayne (1980) * Chlamys islandica Vahl (1980) 0.01 – 7.0 g 3.4 21 C = 3.9 W 0.60 Choromytilus meridionalis Griffi ths (1980) 0.02 – 3.2 g 12, 18 64 C = 5.37 W 0.60 C = 0.0064 L1.58 Van Erkon 10 – 60 mm 15 — C = 3.49 W 1.00 C = 2.0 × 10 − 5 L 2.93 Schurink and Griffi ths (1992) Crassostrea gigas Bougrier et al. 0.1 – 3.0 g 5 – 25 316 C = 3.92 ± 0.84 W0.50 ± 0.17 (1995) * Ren et al. (2000) 0.02 – 0.4 g 10 – 13 38 C = aL0.57 C = 0.016 L1.46 Gerdes (1983) 0.05 – 0.81 g 20 10 C = 2.28 L0.73 Mercenaria mercenaria Doering and 32 – 107 mm 13 – 21 41 C = 0.0307 L0.97 Oviatt 1986 ) Mytilus edulis Jones et al. 0.01 – 2.1 g 10 – 12 24 P = 3.16 W 0.72 P = 0.0037 L2.09 (1992) ; maximum Jones et al. 0.01 – 2.1 g 10 – 12 24 P = 1.78 W 0.70 P = 0.0024 L2.19 (1992) ; mean Smaal et al. 0.02 – 3.90 g 0.4 – 19 139 C = 1.66 ± 0.55 W 0.57 ± 0.17 (1997) *

89 Table 4.1 (Continued)

Species and reference Size T ( ° C) n Weight relationship Length relationship

Hawkins et al. 45 – 57 mm — — C = aW0.45 (1985) Thompson 0.07 – 4.20 g 0 – 15 128 C = 1.73 ± 0.19 W0.41 ± 0.08 (1984) * Smaal et al. 0.01 – 1.17g 9 – 15 20 C = 1.65 ± 0.79 W0.61 ± 0.20 (1986) * Widdows (1978) 0.01 – 2.4 g 15 50 C = 2.65 W0.38 Bayne and Widdows (1978) Lyner * 0.15 – 2.9 g 7 – 21 122 C = 1.98 ± 0.49 W0.45 ± 0.24 Cattewater * 0.13 – 2.8 g 10 – 17 105 C = 1.57 ± 0.36 W0.47 ± 0.11 Mytilus edulis platensis Dellatorre et al. (2007) Wild mussels 30 – 85 mm 20 49 C = 3.89 W0.56 C = 0.0040 L1.72 Cultured 16 – 73 mm 20 52 C = 5.74 W0.58 C = 0.0022 L1.97 mussels Mytilus chilensis Navarro and 0.02 – 3 g 12 34 C = 1.13 W0.60 Winter (1982) Mytilus galloprovincialis Filgueira et al. 27 – 85 mm — 59 C = 5.80 W 0.60 C = 0.0035 L1.72 (2008) ; experiment 1 Filgueira et al. 24 – 86 mm — 93 C = 5.02 W 0.50 C = 0.0039 L1.72 (2008) ; experiment 2 Van Erkon 10 – 60 mm 15 — C = 4.08 W1.06 C = 1.7 × 10 − 5 L 3.02 Schurink and Griffi ths (1992) Ostrea edulis Haure et al. 0.1 – 2.7 g 10 – 30 149 C = 1.38 ± 1.15 W0.83 ± 0.07 (1998) * Rodhouse (1978) 0.1 – 2 g — — C = aW0.48 Ostrea chilensis Winter et al. 0.05 – 2.3 g 12 16 C = 1.32 W0.63 (1984) Winter et al. 0.05 – 2.3 g 12 12 C = 0.62 W0.60 (1984) Perna canaliculus James et al. 20 – 100 mm 11 – 17 53 C = 2.29 ± 1.05 W0.75 ± 0.31 C = 0.001 ± 0.016 L1.99 ± 0.64 (2001) *

90 Bivalve fi lter feeding 91

Table 4.1 (Continued)

Species and reference Size T ( ° C) n Weight relationship Length relationship

Perna viridis Wong and 25 – 85 mm 18 – 30 512 C = 0.81 ± 0.56 W0.61 ± 0.29 Cheung (2001b) * Perna perna Berry and 10 – 120 mm 20 97 C = 8.85 W0.66 C = 0.0027 L1.86 Schleyer (1983) Van Erkon 10 – 60 mm 15 — C = 2.55 W0.88 C = 6.5 × 10 − 5 L 2.54 Schurink and Griffi ths (1992) Pinctada margaritifera Pouvreau et al. 0.2 – 7.5 g 28 43 C = 25.88 W0.57 (1999) Yukihira et al. 0.05 – 20 g 25 52 C = 12.34 W0.60 (1998) Pinctada maxima Yukihira et al. 0.05 – 20 g 25 54 C = 10.73 W0.62 (1998) Placopecten magellanicus MacDonald and 5 – 40 g 5.5 – 12 61 C = 0.942 W0.67 Thompson (1986) ; 10 m MacDonald and 5 – 20 g 1 – 11 56 C = 0.828 W0.69 Thompson (1986) ; 31 m Saccostrea commercialis Kesarcodi - 0.005 – 3 g 22 – 25 120 C = 1.89 W0.32 Watson et al. (2001) Venerupis corrugatus Stenton - Dozey 0.03 – 0.87 g 13 – 18 54 C = 1.90 − 3.62 W0.61 and Brown (1994)

Results are from studies not included in the previous reviews identifi ed in the text. * = mean ± SD of signifi cant regressions; a = intercept not reported.

body weight averaged 0.62 ± 0.05 ( ± 2 stan- 0.94. When these outlier data are excluded, dard error [ SE ], n = 43). This b - value may be the mean b - value falls to 0.58 ± 0.04 (n = 39), somewhat overestimated owing to the anoma- which is equal to the average reported by lously high values reported by Van Erkon Winter (1978) for 12 species of bivalves Schurink and Griffi ths (1992), which averaged (0.58 ± 0.07, n = 25). Combining these data 92 Shellfi sh Aquaculture and the Environment sets gives an overall average b - value of clearance rate are addressed separately. The 0.58 ± 0.04. This exponent is less than the food concentration limits were set to permit theoretical value of 0.67 that assumes propor- comparisons within a relatively narrow, but tionality with gill surface area (see above) and commonly studied range of food concentra- is considerably less than the value of 0.72 tions. Although shellfi sh feeding is responsive reported for bivalves feeding at maximum to low levels of many common anthropogenic capacity (Eq. 4.2 ). Although fewer studies contaminants and to toxic phytoplankton, have reported relationships between clearance these topics are outside the context of this rate and shell length, the allometries summa- review and such studies were not included in rized in Table 4.1 indicate a mean b - value of the meta - analysis, with the exception of utiliz- 2.04 ± 0.54 ( n = 14). This average is also ing data designated as representing reference weighted toward the high values reported by (control) conditions. The studies reported rep- Van Erkon Schurink and Griffi ths (1992) , and resent an extensive, but not an exhaustive, a more generally applicable b -value is search of the literature. Studies were randomly 1.78 ± 0.34 (n = 10). Although there is con- selected and the results are believed to be rep- siderable variability between studies, there resentative of the full range of published clear- appears to be a tendency for b -values to be less ance rate values. Clearance rates reported in than the theoretical proportionality between graphical form were digitized using Didger 4 gill area and shell length ( L2 ). software (Golden Software, Golden, CO). The literature on mussel feeding behavior is particularly extensive and frequency distribu- Meta- analysis of c learance r ate tions of published average clearance rates for r esponses for d ifferent s pecies g roups different mussel species of standard dry body A meta- analysis was conducted on average weight (1 g) and shell length (60 mm) are pre- clearance rate measurements extracted from sented in Figure 4.4 and summary statistics are 61, 30, 25, and 17 published studies on mytilid, given in Table 4.4 . Results have generally been pectinid, oyster, and cockle species, respec- presented for mussels of standard weight tively. This was conducted to investigate ( n = 401), but 72 average values were also central tendencies in values reported over a reported for mussels of standard length (Fig. range of experimental conditions and to 4.4 B). Reported clearance rates averaged provide a foundation for discussing method- 2.98 L g − 1 h − 1 and 3.23 L h − 1 or a 60- mm mussel, ological viewpoints and the multiple factors but ranged widely with a maximum value of potentially controlling the feeding responses of 17.5 L g − 1 h − 1 (not shown) reported for Mytilus shellfi sh. Average rates reported using a wide galloprovincialis by Maire et al. (2007) . The range of direct and indirect clearance rate weight standardized distribution is skewed methodologies are incorporated in this analy- toward lower values, and the median of sis, including laboratory, fi eld, and in situ 2.32 L g − 1 h − 1 is substantially lower than the studies with algal cell, seston, and/or mixed predicted mean of 6.54 L g − 1 h − 1 calculated diets. The size of the literature dictated setting using Equation 4.2 for animals feeding at some limitations, and the studies identifi ed in maximum rates under optimal conditions. In Table 4.2 (mussels) and Table 4.3 (scallops, fact, 95% of the reported mean values are oysters, and cockles) include only work with below this predicted rate. Standardization by diet concentrations between 0 and 10 mg L − 1 , length gave a broad distribution of data (Fig. salinity greater than 20% ppt, and fl ow condi- 4.4 B) and the predicted maximum clearance tions less than 15 cm s − 1 . Potential food con- rate of 5.95 L h − 1 for a 60 - mm mussel (Eq. 4.3 centration, salinity, and water fl ow effects on using b = 1.81) is still higher than the mean of Table 4.2 Studies included in the meta- analysis of average clearance rate estimates for mytilid species subdivided by methodologies employed.

Closed system Flow - through chamber ( a clearance, b chemostat, Biodeposition (a chamber Consumption (a tunnel, (a Eq. 4.5 or b Eq. 4.6 in text) c static, or d fl ume) or b in situ ) b chamber, or c suction)

Aulacomya ater Bayne et al. (1984)a, A Stuart (1982)c, A Choromytilus merdionalis Bayne et al. (1984)a, A Griffi ths (1980)c, A Mytilus chilensis Navarro et al. (2003)a, A Velasco and Navarro (2003) a, A, S Mytilus edulis Okumus and Stirling Kittner and Riisgå rd Newell et al. (2005) a, S Prins et al. 1994 a, S (1994) a, S (2005)a, A Smaal and Vonck (1997)a, S Newell et al. (1989)c, S Petersen et al. (2004) a, S Prins et al. (1996)a, S Fr é chette et al. (1991)a, S Riisg å rd (1991)a, A Hawkins et al. (1996)a, S Bayne et al. (1989)b, A Prins et al. (1996)a, S Riisg å rd et al. (2003)a, A Cranford and Hill Smaal et al. (1986)a, S (1999) b, S Newell et al. (2005)a, S Riisg å rd and Hawkins et al. (1997)a, A Zurburg et al. (1994)a, S M ø hlenberg (1979)b, A Widdows et al. (1979)a, S Widdows et al. Dellatorre et al. (2007)a, M ø hlenberg and (2002)d, A S Riisg å rd (1979) c, A Petersen et al. (2004)a, b, S Petersen et al. (2004)c, Ki ø rboe et al. (1980)c, A S Smaal et al. (1997)b, S Riisg å rd et al. 2003 ) a, A Thompson (1984)a, S Lucas et al. (1987)c, S Bayne et al. (1987)a, S Ki ø rboe et al. (1981)b, A Bayne et al. (1985)a, b, A Clausen and Riisgå rd (1996) a, A Widdows (1978)a, A Bayne et al. (1985)c, A Widdows and Johnson (1988)a, A Smaal and Twisk (1997)a, A Widdows et al. (1984)a, S Newell et al. (1998)b, S Vismann (1990)b, S MacDonald and Ward (2009)a, S Bayne and Widdows (1978)a, S

93 94 Shellfi sh Aquaculture and the Environment

Table 4.2 (Continued)

Closed system Flow - through chamber ( a clearance, b chemostat, Biodeposition (a chamber Consumption (a tunnel, ( a Eq. 4.5 or b Eq. 4.6 in text) c static, or d fl ume) or b in situ ) b chamber, or c suction)

Mytilus galloprovincialis Filgueira et al. (2006)a, A, S Maire et al. (2007)a, A Iglesias et al. 1996 ) a, S Filgueira et al. (2008)a, A Navarro et al. (1996)a, Navarro et al. (1991)a, S A Labarta et al. (1997)a, A P é rez Camacho et al. (2000)a, S Navarro et al. (1991)a, S P é rez Camacho et al. (2000)b, A Mytilus trossulus Ackerman and Nishizaki (2004)c, S Mytilus californianus Ackerman and Nishizaki (2004)c, S Perna canaliculus James et al. (2001)a, S Zeldis et al. (2004)c, S Hawkins et al. (1999)a, S Perna perna Bayne et al. (1984)a, A Resgalla et al. (2007)c, A Berry and Schleyer (1983)c, A Perna viridis Wong and Cheung (1999)a, A Wong and Cheung (2001a)a, S Wong and Cheung (2001b)a, S

Note that some studies used several methods and/or species. Superscripts indicate the method and use of algae cell (A) and/or seston diets (S).

3.23 L h − 1 (median = 3.18 L h − 1 ). The literature One factor contributing to the shape of clearly shows that the maximum feeding clearance rate frequency distributions is the response has only occasionally been observed variation in the allometric exponent employed in mussels and is an extreme condition within in each study, which ranged from 0.2 to 1.1. a wide and highly variable range of average Relatively few studies determined the b - value; rates. instead using a value selected from the litera- Table 4.3 Studies included in the meta- analysis of average clearance rate estimates for scallop, oyster and cockle species.

Scallop Oyster Cockle

Argopecten irradians Crassostrea gigas Cerastoderma edule Bauder et al. (2001)1 Bayne (2004)2, 4 Deslous - Paoli et al. (1987)4 Li et al. (2009) ; low density only)1 Bayne (1999)4 Foster - Smith (1975)4 Palmer (1980)4 Bougrier et al. (1995)4 Ibarrola et al. (2000)2 Argopecten purpuratus Deslous - Paoli et al. (1987) 4 Ibarrola et al. (1998)4 Navarro et al. (2000) 4 Zurburg et al. (1994)5 Iglesias et al. 1996 )2 Navarro and Gonzá lez 1998 ) 4 Dupuy et al. (2000)4 Iglesias et al. (1998)4 Argopecten ventricosus - circularis Lefebvre et al. (2000) 2 M ø hlenberg and Riisgå rd (1979)5 Sicard et al. (1999) 4 Ren et al. (2000)1 Navarro et al. (1992)4 Argopecten nucleus Haure et al. (2003) 1 Navarro and Widdows (1997)1 Velasco (2007)1 Smaal and Zurburg (1997)5 Newell and Bayne (1980)1 Chlamys nobilis Barill é et al. (2003)1 Prins and Smaal (1989)1 Li et al. (2001) 4 Gerdes (1983)4 Prins et al. (1991) 2 Chlamys opercularis Crassostrea belcheri Riisg å rd et al. (2003)3 McLusky (1973)4 Hawkins et al. (1998)1 Smaal et al. (1997)1 Chlamys farreri Crassostrea iradelei Urrutia et al. (2001) 2 Jihong et al. (2004) 4 Hawkins et al. (1998)1 Widdows and Navarro (2007)4 Zhou et al. (2006)2 Crassostrea virginica Widdows and Shick (1985)1 Chlamys hastata Palmer (1980)4 Meyh ö fer (1985)5 Pernet et al. (2008)4 Chlamys islandica Riisg å rd (1988)4 Vahl (1980)1 Ostrea edulis Nodipecten nodosus Haure et al. (1998)1 Velasco (2007)1 Newell et al. (1977)4 Placopecten magellanicus Rodhouse (1978)4 Bacon et al. (1998)1 Wilson (1983)5 Cranford and Grant (1990)4 Buxton et al. (1981)4 Cranford and Gordon (1992)1 Ostrea chilensis Cranford et al. (1998)2 Dunphy et al. (2006)4 Cranford and Hill (1999)2 Chaparro and Thompson (1998)4 Cranford et al. (2005)2 Saccostrea commercialis MacDonald and Thompson (1986)1 Bayne et al. (1999)4 MacDonald and Ward (2009)1 Kesarcodi - Watson et al. (2001)1 Ward et al. (1992)4

95 96 Shellfi sh Aquaculture and the Environment

Table 4.3 (Continued)

Scallop Oyster Cockle

MacDonald and Ward (1994)1 Pilditch and Grant (1999)4 Wildish et al. (1992)4 Pecten maximus Strohmeier et al. (2009)1 Pecten furtivus M ø hlenberg and Riisgå rd (1979)5 Pecten opercularis M ø hlenberg and Riisgå rd (1979)5 Pecten irradians Chipman and Hopkins (1954)5

Superscripts indicate the method employed (1 = fl ow - through; 2 = biodeposition; 3 = clearance; 4 = static; and 5 = other). ture. Where suffi cient data were reported on relationships and the fact that length is not a mussel weight and/or length, the standardized particularly good surrogate for weight (Hilbish results were converted back to experimental 1986 ). rates using the reported b -value and then stan- Summaries of mean standardized clearance dardized again using the average weight and rates for scallops, oysters, and cockles are pre- length allometric exponents of 0.58 and 1.8, sented in Table 4.4 along with the mussel data respectively, determined above. Studies report- that were shown in Figure 4.4 . Given the ing nonstandardized rates were also standard- bimodal distribution of these data, differences ized by this method, which increased the between species groups are examined using number of length- standardized values from 72 median values. Based on reported rates, to 361. This procedure increased the median mussels appear to feed at slightly lower rates clearance rate to 2.46 L g − 1 h − 1 (Table 4.4 ; Fig. relative to the other three groups. 4.4 C) and 3.26 L h − 1 for a 60- mm mussel Standardization using a constant b - value of (Table 4.4 ; Fig. 4.4 D). The resulting distribu- 0.58 indicated that oysters appear to have the tion for weight- normalized rates is bimodal lowest median clearance rate. In both cases, with a smaller peak at ∼ 5 L g − 1 h − 1 that is attrib- cockles exhibited the highest clearance rates. uted to the results of studies designed to stimu- A factor having a large effect on the mean rate late maximum clearance rate through the use obtained for each species group is the type of of an optimal algal - cell diet. Comparison of experimental diet provided. Studies utilizing Figure 4.4 C and Figure 4.4 D shows that the an algal cell - based diet resulted in clearance distribution of reported clearance rates of rates of mussels, scallops, and cockles that mussels of standard weight is more closely were on average 1.7 times higher than rates constrained than for animals of standard obtained utilizing a natural seston - based diet length. This suggests that some of the vari- (Table 4.4 ). The only exception was for oysters, ability between published rates results from where data for seston diets was too sparse geographic differences in mussel length– weight ( n = 10) for an objective comparison. The Bivalve fi lter feeding 97

12 60 (A) (B) n = 401 10 n = 72 50

8 40

6 30 Frequency 20 4

10 2

0 0 60 40 (C) (D)

50 n = 357 n = 361 30 40

30 20 Frequency 20 10 10

0 0 0426804 10268 10 Clearance rate (L g–1 h–1) Clearance rate (L ind. h–1)

Figure 4.4 Frequency distributions of mussel clearance rate results from the 61 publications listed in Table 4.2 . Average rates are standardized by dry weight (A and C; L g − 1 h − 1 ) and shell length (B and D; L h − 1 for 60 mm individual). Plots A and B summarize results as published and plots C and D show the distributions after restandardization using b - values of 0.58 and 1.8 for weight and length, respectively. The arrows indicate median values, and the vertical dashed lines represent the maximum rates predicted by Equations 4.2 and 4.3 for weight - and length - standardized animals, respectively.

generally higher rates obtained for the high - rate for oysters feeding on both types of diets nutritional -quality algal- cell diets was the (2.54 L g − 1 h − 1 ) is comparable with mussels, and main reason for the bimodal frequency distri- cockles and scallops appear to have a relatively bution observed for these species groups. For high rate of feeding. most aquaculture and wild population predic- The above comparisons of clearance rates tions requiring clearance rate data, the seston - across bivalve species groups are not meant to based results are a logical choice, with mussels, be conclusive given possible differences in the scallops, and cockles feeding at 2.43, 3.49, range of experimental conditions employed in and 2.81 L g − 1 h − 1 , respectively. The average the study of each group. In fact, it may be 98 Shellfi sh Aquaculture and the Environment

Table 4.4 Summary statistics on average (± 2SE) standardized (1 g dry tissue weight and 60 mm shell length or height) clearance rate values reported in papers listed in Tables 4.2 and 4.3 and after restandardization using average b - values ( n = number of mean values applicable).

Mussel Scallop Oyster Cockle

Dry tissue weight as reported (L g − 1 h − 1 ) n 401 123 123 111 Median 2.32 2.63 3.00 3.37 Mean ± 2SE 2.98 ± 0.23 3.63 ± 0.59 3.47 ± 0.49 3.53 ± 0.44 Shell length (or height) as reported (L ind. − 1 h − 1 ) n 72 — — — Median 3.18 — — — Mean ± 2SE 3.23 ± 0.34 — — — Dry tissue weight using b = 0.58 (L g − 1 h − 1 ) n 357 172 68 90 Median 2.46 3.21 2.05 3.57 Mean ± 2SE 3.24 ± 0.26 5.10 ± 0.76 2.54 ± 0.48 3.58 ± 0.38 Seston - based diet 2.43 ± 0.28 (161) 3.49 ± 0.86 (79) 4.78 ± 0.56 (10) 2.81 ± 0.66 (50) mean ± 2SE ( n ) Algae - based diet 4.18 ± 0.41 (178) 6.66 ± 1.27 (79) 2.15 ± 0.49 (58) 4.12 ± 0.54 (61) mean ± 2SE ( n ) 60 mm shell length (height) using b = 1.8 (L ind. − 1 h − 1 ) n 361 130 49 67 Median 3.26 5.18 1.09 5.30 Mean ± 2SE 3.82 ± 0.28 7.89 ± 1.37 1.39 ± 0.28 6.03 ± 0.81

expected that mussels would have a higher variations in clearance rate. The tropical oyster feeding rate than cockles based on the observa- Pinctada margaritifera consistently exhibited tion of Hawkins et al. (1990) that the gill area the highest clearance rates of any bivalve of Mytilus edulis was more than four times studied (averaged 21.3 L g − 1 h − 1 ; Pouvreau et al. greater per unit tissue mass than Cerastoderma 1999, 2000 ; Yukihira et al. 1998 ) and had edule . However, it is important to note that an intermediate gill area of 3502 mm 2 g − 1 this morphological characteristic can be popu- (Pouvreau et al. 1999 ). This was the only lation specifi c, with the gill area- to - dry tissue species omitted from the meta - analysis owing mass ratio varying considerably within a to the large outlier effect on calculations of the species. For example, Mytilus edulis from mean clearance rate response. Denmark and Spain exhibited gill area- to - dry The average clearance rates reported in weight ratios of 2458 mm 2 g − 1 (Mø hlenberg Table 4.4 for different bivalve species are and Riisg å rd 1979 ) and 4322 mm 2 g − 1 (Hawkins useful for the fi rst - order approximation of et al. 1990 ), respectively. Morphology by itself population and community clearance values. does not fully explain inter- and intraspecifi c However, because of the very wide range of Bivalve fi lter feeding 99 clearance rates and b -values reported for indi- cate that the highest precision obtainable was vidual bivalve populations, we stress the ∼ 10% (SE/mean) and that achieving this level importance of measuring actual clearance required a minimum of 12 replicate measure- rates at the study site during the time(s) of year ments. The studies listed in Table 4.2 (mytilid that is (are) pertinent to the specifi c applica- species) were examined and 30 studies pro- tion of the data. The effect of the allometric vided suffi cient data to calculate a precision of exponent employed can be seen in the differ- 15% for 254 average clearance rate estimates ence between the reported mean and the res- (average sample size was 11.6 replicates). The tandardized mean clearance rate (Fig. 4.4 and following illustrates the importance of this Table 4.4 ). In addition, a sensitivity analysis of degree of intraindividual variability for studies a scallop (Chlamys farreri) growth model attempting to detect signifi cant differences in showed that a 10% change in the weight expo- average clearance rate responses using inferen- nent caused a 13% change in tissue growth tial statistics. Power analysis was conducted predictions (Hawkins et al. 2002 ). This effect for a paired t - test and one- way analysis of is relatively small owing to the small size of variance (ANOVA ) (Power and Precision Ver. the scallops studied. The magnitude of the 2 software) based on the typical error variance growth effect will increase with the size of the observed across these clearance rate studies at animal, such that the difference in b - values n = 10. To achieve an acceptable statistical (e.g., 0.76 in Eq. 4.2 vs. 0.58 calculated from power of 80% at α = 0.05, the minimum data in Table 4.1 ) would have a substantial “ effect size” (the standardized mean difference impact on population food removal and aqua- in clearance rate between experimental treat- culture production predictions. ments) that can be detected is 50%. This is a relatively large effect size for biological mea- surements, making it diffi cult to detect differ- Precision and a ccuracy of c learance ences in average clearance rates between r ate m easurements experimental treatments. When measuring The usual consequence of a high degree of clearance rate, the following quote by intraindividual variability in feeding activity Nakagawa and Cuthill (2007) is particularly (see above) is that a large number of replicate relevant: “ . . . all biologists should be ulti- measurements are required to obtain suffi cient mately interested in biological importance, precision (i.e., the degree of agreement between which may be assessed using the magnitude of replicated measurements) to protect the analyst an effect, but not its statistical signifi cance. ” from reaching erroneous conclusions when Other relevant statistical considerations conducting statistical hypothesis tests. that require more attention include the use of Although seldom reported, zero clearance rate regression analysis in cases where both the values are often discarded prior to statistical dependent and independent variables are analysis. This is a subjective practice that will based on the same data (e.g., clearance rate vs. increase the precision of the mean response, seston organic content) and the need to use but which will cause overestimation when repeated - measures designs when clearance rate extrapolating mean individual rates to the values are not independent (MacDonald and population level. The periodic cessation of Ward 2009 ). Time series measures on the same feeding activity is a normal occurrence (Fig. individuals cannot be avoided in some cases 4.2 ) that should not be ignored. Analysis of (e.g., in situ observations of shell gape and clearance rate data collected by Strohmeier biodeposition) so the independence assump- et al. (2009) , who collected 18 replicate mea- tion needs to be tested prior to the use infer- surements to ensure maximum precision, indi- ential statistics. Strohmeier et al. (2009) 100 Shellfi sh Aquaculture and the Environment employed autocorrelation analysis to show of clearance rate measurements continually that mussel and scallop clearance rates were requires attention, including discussion of the independent when repeated measurements validity of assumptions inherent with available were taken at time intervals greater than 1 day. clearance rate methodologies, assumptions Although clearance rate measurements of regarding the true feeding rate, and the inter- individual animals dominate the literature, an calibration of clearance rate methodologies. alternative approach is to measure population A wide range of indirect clearance rate responses. Population responses tend to require methodologies exist and can be classifi ed based fewer measurements to achieve a higher level on the measurement of bivalve particle removal of precision due to the “ built - in ” averaging of (depletion) or egestion (biodeposition). Particle interindividual variations (Cranford et al. removal methodologies include open (fl ow - 1998 ; Iglesias et al. 1998 ). Individual and through chambers, in situ tunnels, and suction population measures do not necessarily provide methods) and closed (chambers, aquaria, and comparable information, and it should not be mesocosms) systems. Examples of the closed assumed that average weight - standardized method include the “ static method” and the individual estimates are equal to similarly so - called “ clearance method ” described by standardized population estimates. Interactions Riisg å rd (2001a) . Both determine clearance between individuals (e.g., disturbance, crowd- rate from the exponential decline in particle ing, fl ow alteration, refi ltration of water) may concentration as a function of time (Coughlan infl uence some population- based methodolo- 1969 ), but the latter may be differentiated by gies if they are not controlled. the use of a bivalve population, an optimal In an attempt to justify the general applica- algal cell diet, and an algal dosing pump to tion of maximum clearance rate measurements somewhat maintain the algal concentration. in nature and related theories on shellfi sh The fl ow - through chamber method has been feeding nonresponsiveness to environmental the most commonly employed method and forcing, Riisgå rd (2001a ; see also J ø rgensen clearance rate is calculated using either of the 1996 ) concluded that “ . . . confl icting data on following two equations: fi ltration [clearance] rates seem partially due =− to the incorrect use of methods, and partly to Flow-through equation:(())CUFin F out/ F in be caused by differences in experimental con- (4.5) ditions. ” Bayne (2001) has already provided =− suffi cient rationale why this conclusion is Steady-state equation:(()),CUFin F out/ F out unacceptable, but statements such as this con- (4.6) tinue to impede the objective discussion of the extrinsic factors that affect shellfi sh feeding where U is the fl ow through the chamber − 1 behavior (e.g., Cranford 2001 ; Widdows (L h ), and Fin and Fout are food particle con- 2001 ; Filgueira et al. 2006 ) and severely affect centrations in the infl ow and outfl ow of the the peer review process. There is a need for chamber, respectively. The “ fl ow - through ” accuracy in any biological measurement and equation applies to systems where all the par- this need is particularly critical when the intent ticles in the infl ow are available to the animals is to extrapolate the responses of a few animals and recirculation of fi ltered water is absent. to predict the biofi ltration capacity of extremely The “ steady - state ” equation represents an dense populations. Any signifi cant errors in alternative for systems with low fl ow and estimating the individual response will be mag- water recirculation. The importance of nifi ed immensely at the population level. ensuring that the fl ow rate is adequate to Consequently, an assessment of the accuracy meet assumptions inherent with using the Bivalve fi lter feeding 101

10 (A) (B) 17 14

8 9 ) –1 h

–1 6 32 103 Flow-through (Eq. 4.5)

4 43 30 Clearance rate (L g 33 156 72 40

2 17 Clearance Clearance Flow-through (Eq. 4.6) Biodeposition Biodeposition Static Other Static Other Flow-through (Eq. 4.5) 0 Flow-through (Eq. 4.6) Method

Figure 4.5 Average ( + standard error [SE ], with sample size shown) weight- standardized clearance rates estimated for mytilid species by the displayed methods. Data are from studies listed in Table 4.2 . Plot A summarizes reported stan- dardized rates and plot B includes restandardized rates assuming b = 0.58. Arrows on the top of each plot connect methods that provided statistically equivalent results (ANOVA, P < 0.05).

fl ow - through equation has long been recog- rates; however, most published studies have nized (e.g., Riisg å rd 1977 ; Bayne et al. 1985 ) reported less than 30% reduction of particles. and can be demonstrated simply by measuring Although several of the reviewed studies on no change in clearance rate with increasing mytilid species (Table 4.2 ) report levels of food fl ow rate (U ). Riisgå rd (2001a) stated, however, depletion up to 40%, it is particularly impor- that “ the prerequisites for using the method tant to note that even at 40% particle deple- have often been disregarded” resulting in tion, the potential underestimation of true underestimated rates. Filgueira et al. (2006) clearance values resulting from insuffi cient and Pascoe et al. (2009) critically examined chamber fl ow is relatively small compared two different fl ow - through feeding chamber with the large difference between the median designs and the application of Equation 4.5 and maximal clearance rates shown in Figure and concluded that the method complies 4.4 (see fi gs. 4.4 and 4.5 in Filgueira et al. with all theoretical requirements provided 2006 ). The steady - state equation (Eq. 4.6 ) was that the percentage of particles cleared from employed to estimate clearance rate in 10% of the fl ow is less than 25– 30% (achieved at the studies listed in Table 4.2 . However, U > 150 mL min − 1 ). This maximum percentage Filgueira et al. (2006) and Pascoe et al. (2009) of particles cleared will vary somewhat with showed that this equation resulted in reduced the geometry of different feeding chambers precision and overestimation of clearance rate and is not a substitute for examining the rela- and concluded that Equation 4.5 provided a tionship between clearance values and fl ow more accurate representation of true clearance 102 Shellfi sh Aquaculture and the Environment rate. Petersen et al. (2004) reported similar damentally different methodologies is not results, but nonetheless promoted the general strictly justifi ed, but such comparisons have application of the steady - state equation. been made and the results deserve some discus- Feeding rate methodologies based on a sion. A number of studies have shown that combination of shellfi sh biodeposit produc- clearance rate values obtained with the biode- tion and suspended particle measurements position and fl ow - through chamber methods have become increasingly prominent (Table provide statistically equivalent clearance rate 4.2 ) since the development of the pseudofeces/ estimates (Urrutia et al. 1996 ; Iglesias et al. feces biodeposition method (Navarro et al. 1998 ; Cranford and Hill 1999 ; Bayne 2004 ; 1991 ) and the related in situ biodeposition Newell et al. 2005 ). Comparison of rates method (Cranford and Hargrave 1994 ). Both obtained with the biodeposition and indirect methods are similar except that the former methods also gave similar results for both approach permits measurements to be made at Mytilus edulis and Mulinia edulis (Navarro higher food concentrations where pseudofeces and Velasco 2003 ). Conversely, Petersen et al. production becomes a signifi cant fraction of (2004) concluded that the biodeposition fi ltration rate. As with all other methods, there method resulted in signifi cantly lower clear- is a need to ensure that certain assumptions ance rate estimates relative to other methods are met for the proper application of these tested. This intercalibration study and the techniques. These assumptions include the results reported have been questioned based need for accurate characterization of sus- on (1) the failure to sample biodeposits quan- pended particles retained by the gill (a common titatively (Bayne 2004 ), (2) the lack of any assumption for all indirect methods) and validation that the experimental conditions quantitative biodeposit collection. Assessment actually conform with the basic requirements of these assumptions has become routine with of the deposition method (Riisg å rd 2004 ), and the application of the in situ biodeposition (3) the erroneously high rates that can be method (Cranford and Hargrave 1994 ; obtained when using Equation 4.6 in conjunc- Cranford et al. 1998 ), and a sensitivity analy- tion with the fl ow - through method (Filgueira sis has shown that potential errors in seston et al. 2006 ; Pascoe et al. 2009 ). diet characterization using standard water fi l- Average weight - standardized clearance rate tration methods could only result in underes- data summarized in Figure 4.4 (Table 4.2 ) timating feeding rates by less than 12% were further analyzed to examine possible (Cranford and Hill 1999 ). effects of different methodologies on mean A fundamental difference between biodepo- clearance rates of mytilid species. Reported sition and particle depletion methodologies for (Fig. 4.4 A) and restandardized clearance rates measuring clearance rate is that they provide (Fig. 4.4 C) were analyzed separately by means temporally integrated and near- instantaneous of one- way ANOVAs, which indicated a sig- responses, respectively. In addition, the biode- nifi cant difference in mean results obtained by position method often provides an integrated the different methods (degree of freedom response for several animals. Short- lived [ d.f. ] = 341 and 213, respectively; P < 0.001). extreme clearance rate responses (maximum Tukey post hoc comparisons of reported rates and zero) that may be of little ecological rel- showed that most methods provided similar evance can greatly infl uence the short- term results. The exception was the clearance mean response, but have little effect on inte- method, which provided an overall mean rate grated clearance rates obtained with the biode- that was signifi cantly higher by about a factor position method. As a result, the direct of two (Fig. 4.5 A). When reported results comparison of results obtained with these fun- were restandardized, the fl ow - through method Bivalve fi lter feeding 103

(Eq. 4.5 ) gave similar results as the biodeposi- measure (growth) with instantaneous physio- tion and static chamber methods (Fig. 4.5 B), logical and dietary measures. This approach, but the clearance and steady- state fl ow - through however, has been used on several occasions. method (Eq. 4.6 ) provided signifi cantly For example, Fré chette and Bacher (1998) used ( P < 0.05) higher clearance rates (Fig. 4.5 ). published data on seston clearance rates and Data from these two methods are largely tuned the parameters of the allometric relation- responsible for the second smaller peak in the ship until a growth model provided estimates frequency distribution (Fig. 4.4 C). that matched the observed growth of mussels. The majority of published comparisons of The clearance relationship that yielded accu- indirect clearance rate methodologies, as well rate growth predictions (2.12 W 0.408 ) was as the results of our meta- analysis, shows that similar to the equation taken from the litera- similar mean clearance rate results are obtained ture (Thompson 1984 ; 1.72 W0.413 ). In this case, with most methods when they are employed a relatively low clearance rate appeared to properly under the same range of experimental provide accurate predictions. Cranford and conditions. An exception is that the applica- Hill (1999) showed that the growth of Mytilus tion of Equation 4.6 with the fl ow - through edulis and Placopecten magellanicus was method can cause overestimated values, par- similar to predictions based on seasonal clear- ticularly when chamber fl ow rates are rela- ance rates measured using the in situ biodepo- tively low (Pascoe et al. 2009 ). The clearance sition method. Clausen and Riisg å rd (1996) method has only been employed under a attempted the only validation of the applica- narrow range of conditions (optimal algal cell tion of maximum clearance rates (C max ) to a rations) and the anomalously high clearance natural population of bivalves and concluded rates that have been obtained refl ect these con- that Mytilus edulis must fully exploit their ditions as opposed to any methodological clearance capacity to explain the growth error. This method is not compatible with the observed in nature. These authors, however, use of more complex diets (i.e., natural seston) assumed that phytoplankton were the sole and a direct comparison is not possible. food resource. If the other available detrital Questions regarding the accuracy of clear- and living food resources had been included ance rate measurements have generated a in these growth calculations, a lower clear- rather fruitless debate in the literature because ance rate would also calculate the observed we cannot arbitrarily assume that any rate is growth. more accurate than another. Accuracy may A somewhat more direct approach to assess- best be assessed by determining the ability of ing clearance measurement accuracy (i.e., reported clearance values to predict measured fewer assumptions) is to back - calculate indi- tissue growth or the magnitude of phytoplank- vidual clearance rates required to explain the ton depletion resulting from the feeding activ- measured population effects on particle sedi- ity of a given bivalve population. Assessing mentation or depletion in the surrounding feeding rates by examining tissue growth over water. Doering and Oviatt (1986) showed that time requires numerous assumptions regarding clearance rates of Mercenaria mercinaria mea- measurement accuracy for all the physiological sured using a natural diet and the fl ow - through components of growth as well as for any appli- method gave estimates of gross sedimentation cable energy conversion factors. Further com- that agreed well with observations of gross plicating such an approach are the possible sedimentation in a mesocosm. They noted effects of resource limitation (selection of that the use of maximum clearance rates energy, carbon or nitrogen budget approaches) (Eq. 4.2 ) would overestimate sedimentation and problems comparing a time- integrated by up to an order of magnitude. Results of a 104 Shellfi sh Aquaculture and the Environment high - resolution spatial model of seston deple- feeding behavior under more natural condi- tion in dense Mytilus edulis culture (Grant tions for several mytilid and pectinid species et al. 2008 ), which assumed an average clear- (Widdows and Bayne 1971 ; Widdows 1973, ance rate of 2.4 L g − 1 h − 1 (similar to median 1976, 1978; Widdows et al. 1979 ; Thompson values reported herein), predicted bay - scale 1984 ; Thompson and Newell 1985 ; Prins phytoplankton depletion levels that corre- et al. 1994 ; Smaal et al. 1997 ; Cranford and spond well with measurements obtained using Hill 1999 ; Cranford et al. 2005 ; Strohmeier et rapid, high - resolution phytoplankton mapping al. 2009 ). For example, a time series of in situ surveys with a towed sensor vehicle. Petersen sea scallop (Placopecten magellanicus ) clear- et al. (2008) utilized an advection depletion ance rates measured at 3° C showed that model to determine particle depletion rates for feeding activity was variable and that the a raft - culture unit containing 40 - mm shell maximum clearance rate can be achieved even length mussels. They concluded that the mea- at this low temperature (Cranford et al. 2005 ). sured depletion rates could be estimated using In situ measurements of mussel (Mytilus clearance rates between 0.6 and 0.9 L ind. − 1 h − 1 . edulis ) clearance rates at different times of the This is lower than would be predicted using year also revealed little dependence of feeding clearance rates reported in Table 4.4 , but this on temperature (Fig. 4.6 ; Ward and MacDonald, is expected given water refi ltration under such unpublished data). dense culture conditions. Assumptions regard- An important consideration when explor- ing the above back- calculation approach to ing the effect of temperature on bivalve feeding assessing clearance rate accuracy include: No is the need to distinguish between the well - refi ltration of water by bivalves located down- documented effects of temperature on the current, and no feedback effect on clearance maximum clearance rates of fully open bivalves rate from changing food concentration (deple- and the potential effects on animals that feed tion). Although both assumptions can com- at submaximal rates. Animals stimulated to promise the validity of this approach, the exhibit the maximum clearance response are general similarity of measurements and predic- essentially physiological slaves to the con- tions across these studies tends to validate the straints that limit bivalve feeding capacity high accuracy of most clearance rate method- ologies when they are conducted under eco- logically relevant conditions. 6 ) –1 5 h –1 Controls on b ivalve c learance r ate 4

3 Accurate descriptors of shellfi sh feeding behav- ior, which are needed to predict growth and 2 environmental interactions, have to incorpo- 1 rate responses to the major endogenous and Clearance rate (L g 0 exogenous factors and must refl ect the net 024 6 810121416 response to multiple, simultaneous forcing Temperature (°C) parameters. Temperature is one factor that is known to limit the maximum feeding response Figure 4.6 Average (± SD) standardized clearance rates of in shellfi sh (e.g., Kittner and Riisgå rd 2005 ; Mytilus edulis measured in the fi eld over a wide range of water temperatures using the fl ow - through chamber see above). However, temperature has not method (J.E. Ward and B.A. MacDonald, unpublished data been identifi ed as an important control on obtained in Newfoundland, Canada). Bivalve fi lter feeding 105

) 7 (body size, fl uid dynamics, and related tem- –1 (A) High seston h 6 Hawkins et al. (1999) perature effects). Although no physiological –1 mechanisms can override these fundamental 5 constraints on clearance rate, a number of 4 studies have nonetheless employed optimal 3 Perna canaliculus laboratory conditions as a basis for concluding 2 that evidence for the regulation of feeding per- 1

Clearance rate (L g 0 formance is lacking in shellfi sh (J ø rgensen 0 5 10 15 20 1996 ; Riisg å rd 2001b; Kittner and Riisgå rd 50

) (B) Low seston

2005 ). Geometric and physical factors only –1 6 40 Strohmeier et al. (1999) constrain the upper limits of fi ltration activity Mytilus edulis and do not rule out fl exibility in feeding per- 30 4 formance at reduced rates. Riisgå rd (2001b) concluded that it is important that future 20 2 research on bivalve compensatory responses to 10 Pecten maximus variations in the environment be made under Clearance rate (L h 0 0 optimal conditions that result in maximum 0.0 1.0 2.0 3.0 feeding activity. This would perpetuate an Chlorophyll a (µg L–1) expected result that could only be extrapolated to cultured or wild shellfi sh populations if Figure 4.7 Clearance rate in relation to food concentra- tion (chlorophyll a ; μ g L − 1 ) from studies on bivalve species bivalves in nature always exhibited maximal from high (A) and low (B) seston environments. The feeding rates such as those stimulated by a curves are described by regression equations given in controlled, artifi cial diet. The above discussion Table 4.4 . on feeding variability and range of mean responses clearly shows that it is unacceptable to limit observations to an artifi cial condition bination of Chl and total particulate matter that does not exist in nature. ( TPM ) concentrations. Rates peaked around Seston concentration has a strong infl uence 2 μ g Chl L − 1 and declined at lower and higher on bivalve clearance rate and explains a large concentrations (Fig. 4.7 A). James et al. (2001) fraction of the variance in clearance rate mea- showed a similar result for this species, except surements (Table 4.4 ). Although the shape of that clearance rates of a population acclimated the relationship varies within and between to low food availability peaked at a consider- species, clearance eventually declines as seston ably lower concentration ( ∼ 0.4 μ g Chl L − 1 ). concentration increases over a narrow to This unimodal response to food concentration broad range (e.g., Hawkins et al. 2001 ; James maximizes food intake during periods of low et al. 2001 ; Wong and Cheung 2001b ; Hewitt food availability (Bayne et al. 1987 ) and can and Pilditch 2004 ; Velasco and Navarro 2003 ). benefi t energy intake at higher concentrations Numerous studies have shown that clearance by preventing saturation of preingestive par- rates exhibit an initial peak at relatively low ticle sorting mechanisms on the ctenidia and concentrations, followed by a slow decline labial palps (Iglesias et al. 1992 ). (Hawkins et al. 1999 ; James et al. 2001 ; The majority of bivalve feeding measure- Hewitt and Pilditch 2004 ). The example illus- ments have been conducted in regions where trated in Figure 4.7 A from Hawkins et al. seston concentrations exceed 1 μ g Chl L − 1 for (1999) shows that variations in clearance rate most of the year, and the general consensus of Perna canaliculus exposed to a wide turbid- from these studies is that feeding ceases at ity range could largely be explained by a com- Chl concentrations between 0.5 and 1 μ g L − 1 106 Shellfi sh Aquaculture and the Environment

(Riisg å rd and Randl ø v 1981 ; Newell et al. consistent and relatively high rate, while the 2001 ; Riisgå rd et al. 2003 ). The cessation of animals on the bottom exhibited large tidal feeding at low Chl concentrations (< 0.86 μ g L − 1 ) variations in feeding activity. This may have resulted in tissue loss (Hawkins et al. 1999 ). resulted from location - specifi c differences in A study of Pecten maximus and Mytilus edulis the food supply, exposure to fl ow conditions from an area with naturally low seston levels in the chambers that were unrepresentative of (Norwegian coast), however, showed that both ambient conditions, and/or a response of the species did not cease feeding even when Chl animals to experimental manipulation. was as low as 0.01 μ g L − 1 (Strohmeier et al. In a review that highlighted the high plastic- 2009 ; Fig. 4.7 B). This indicates that some ity of bivalve physiological processes, Bayne bivalve species can functionally adapt to pro- (1998) postulated “ . . . the a priori expecta- longed exposure to low- seston conditions such tion (and the hypotheses that fl ow from it) is that their biogeographical distribution is not that fl exibility will lead to some measurable constrained simply by their ability to clear level of compensation in feeding behaviour, dilute particles from suspension. Studies on where compensation is defi ned as a change in bivalves residing in oligotrophic waters have a physiological process, in response to a change reported some of the highest feeding rates for in feeding conditions, which results in an the given species measured under natural increase in nutritional uptake over the rate dietary conditions (Essink et al. 1989 ; Hawkins that would apply if no compensatory change et al. 1998 ; Yukihira et al. 1998 ; Loret et al. occurred. ” An endogenous factor potentially 2000 ; Pouvreau et al. 1999, 2000; Maire et al. infl uencing clearance rate in nature, therefore, 2007 ; Strohmeier et al. 2009 ). This is appar- is the instinctive feeding strategy of a given ently a necessary adaptation for growth and bivalve species. There appears to exist a con- survival in low seston conditions (Pouvreau tinuum of strategies ranging from species that et al. 1999 ). primarily regulate clearance rate (e.g., Controlled laboratory experiments provide Venerupis pullastra, Mercenaria mercenaria , valuable insights into the responses of mol- Mya arenaria, and Pinctada margaritifera ; luscan shellfi sh to specifi c conditions but have Foster - Smith 1975 ; Bricelj and Malouf 1984 ; a limited capacity to duplicate the natural Bacon et al. 1998 ; Hawkins et al. 1998 ), to environment where food quantity and quality, those that mainly regulate the production of and the ambient fl ow regime, can vary dra- pseudofeces (e.g., Mytilus edulis and Cardium matically over different timescales. Although edule ; Foster - Smith 1975 ; Bayne 1993 ; observations under laboratory conditions are Navarro et al. 1994 ; Hawkins et al. 1996 ), to needed to isolate specifi c responses, the knowl- others that employ both mechanisms to varying edge required to predict temporal changes in degrees (e.g., Atrina zelandica, Cerastoderma food acquisition by bivalves must also come edule , Crassostrea gigas, Mulinia edulis , from fi eld studies where feeding behavior may Mytilus chilensis, Placopecten magellanicus , be affected by multiple variables. An example and Perna viridis ; Cranford and Gordon 1992 ; of the importance of obtaining clearance rate Navarro et al. 1992 ; Soletchnik et al. 1996 ; estimates under strictly in situ conditions is Urrutia et al. 1996 ; Barillé et al. 1997 ; Iglesias illustrated by the results shown in Figure 4.2 D. et al. 1996 ; Bacon et al. 1998 ; Hawkins et al. Simultaneous time series of the feeding activity 1998 ; Velasco and Navarro 2002 ; Hewitt and (siphon area) of mussels were markedly differ- Pilditch 2004 ). The strategy employed also ent for animals in feeding chambers compared appears to vary between geographic locations with those in a natural benthic setting (Newell for the same species (e.g., Crassostrea gigas ; et al. 2005 ). Mussels in the chambers fed at a Ren et al. 2000 ). In areas where the nutritional Bivalve fi lter feeding 107 quality of the seston is generally high, there is Deslous - Paoli et al. 1987 ; Smaal et al. 1997 ; little bioenergetic benefi t to regulating particle Cranford and Hill 1999 ; Hewitt and Pilditch selection (pseudofeces production), so the reg- 2004 ; Strohmeier et al. 2009 ). Additionally, ulation of clearance rate with changing food bivalves residing in adjacent areas with appar- abundance is the more effective strategy. ently similar conditions can show marked dif- Bivalves residing in more turbid regions with ferences in their feeding behavior (Hewitt and variable seston conditions benefi t from regu- Pilditch 2004 ). The general lack of correlation lating pseudofeces production, but those between clearance rate and ambient environ- species that are best suited to high turbidity mental conditions may stem from a number of also regulate clearance rate to maximize energy factors including intake (see Velasco and Navarro 2002 ). The so- called “ bivalve functional response ” 1. the limited ability of the statistical methods to diet variability also depends on qualitative employed to quantify complex interactions aspects of the available seston, which make it between multivariate forcing functions, diffi cult to categorize the feeding strategy of many of which may cause a nonlinear many species from the available literature response; when only a limited range of seston qualities 2. the measurement of bulk seston variables and quantities have been employed. A good that inadequately characterize food quan- indication of the important effect of diet tity and quality and the stimulatory/ quality on clearance rate can be seen in the inhibitory properties of seston components difference between average rates measured on feeding behavior; using algal cell- and seston- based diets. For 3. the inability to continuously measure many mussels, scallops, and cockles, laboratory potentially important environmental measurements using algal cell cultures resulted parameters, particularly diet quality; in average clearance rates that are 60% higher 4. the presence of time- averaged behavior in than rates obtained using seston - based diets which the bivalves do not compensate for (Table 4.4 ). Feeding behavior is highly stimu- relatively short- term environmental varia- lated by specifi c nutritive compounds present tions but remain adapted to longer - term in the diet (Navarro et al. 2000 ) owing, at least conditions; in part, to the capacity for chemoreception 5. feedback from the regulation of digestive (Ward et al. 1992 ). Statistical descriptions of processes that effect feeding behavior; and clearance rate responses to natural dietary 6. the additional infl uence of seasonally vari- conditions have been developed for several able endogenous nutrient demands on the bivalve species and are summarized in Table animal ’ s energy balance and compensatory 4.5 . These models indicate that diet quality, feeding responses. The high energy costs of which is generally expressed as seston organic gametogenesis are an obvious, albeit poorly content, is an important factor. However, understood, seasonally variable factor clearance rate tends to be better explained by potentially forcing the need for compensa- changes in quantitative rather than qualitative tory feeding adjustments (Deslous- Paoli et aspects of the diet (see also Hewitt and Pilditch al. 1987 ; Cranford and Hill 1999 ). 2004 and cited papers). Despite an abundance of knowledge on the Whereas the majority of bivalve feeding studies responses of bivalves to a range of environ- have been concerned primarily with determin- mental forcing functions, no clear relation- ing instantaneous responses to environmental ships are apparent between seasonal variations change, the role of past feeding history (e.g., in feeding activity and these variables (e.g., the persistence of feeding behavior in the face Table 4.5 Signifi cant ( P < 0.05) regressions between bivalve clearance rate ( C ) and the total particulate matter concentration (TPM) and organic content (OC; proportion) of TPM.

Species and source Equation Applicable range r2

Atrina zelandica Hewitt and Pilditch (2004) C (mL g − 1 h − 1 ) = 337 × e − 0.5(log(TPM - 100)/1.1) × 2 50 – 580 mg TPM L − 1 0.81 (Four determinations) − − − × − C (mL g 1 h 1 ) = 193 × e 0.5(log(TPM - 86)/0.81) 2 18 – 550 mg TPM L 1 0.88 C (mL g − 1 h − 1 ) = 428 × e − 0.5(log(TPM - 1.06)/160) × 2 70 – 600 mg TPM L − 1 0.85 C (mL g − 1 h − 1 ) = 360 × e − 0.5(log(TPM - 1.3)/93) × 2 50 – 580 mg TPM L − 1 0.65 Argopecten irradians Palmer (1980) C (L g − 1 h − 1 ) = − 0.649(TPM) + 6.364 0 – 10 mg algae L − 1 0.80 Cerastoderma edule Iglesias et al. (1996) C (L g − 1 h − 1 ) = e(0.3968 − 0.2118(TPM) × OC) 5 – 22 mg TPM L − 1 0.50 Navarro et al. (1992) C (L g − 1 h − 1 ) = e( − 0.0409 × Vol + 0.560) 3 – 30 mg TPM L − 1 0.66 Chlamys farreri Hawkins et al. (2001) C (L g − 1 h − 1 ) = [91 × (Vol + 1) 1.2 × (Chl + 1) 2.1 3.2 – 105 mg TPM L − 1 0.58 × e( − 1.7 × (Vol + 1)) + ( − 1.4 × (Chl + 1)) + (0.21 × (Vol + 1) × (Chl + 1)) ] − 1 Crassostrea gigas Ren et al. (2000) C (L h − 1 cm − 1 ) = 0.17 × (TPM/(TPM + 0.39)) ∼ 1 – 650 mg TPM L − 1 0.79 × e( − 0.00378 × TPM) Mulinia edulis Velasco and Navarro (2002) C (L g − 1 h − 1 ) = 10(2.95 − 0.59 × logTPM − 1.53 × logOC) 2 – 203 mg TPM L − 1 0.82 Velasco and Navarro (2003) C (L g − 1 h − 1 ) = 2.3841 × e( − 0.0054 × TPM) 3 – 200 mg TPM L − 1 0.85 Mytilus edulis Hawkins et al. (1996) C (L g − 1 h − 1 ) = 0.60 + 0.039(TPM) 5 – 120 mg TPM L − 1 0.54 Strohmeier et al. (2009) C (L h − 1 ) = 5.35 − 0.67(Chl) + 0.56(lnChl) 0 – 3 μ g Chl L − 1 0.34 + 0.001/(Chl) Mytilus chilensis Velasco and Navarro (2002) C (l g − 1 h − 1 ) = 10(2.94 − 0.61 × logTPM − 1.33 × logOC) 2 – 203 mg TPM L − 1 0.83 Velasco and Navarro (2003) C (L g − 1 h − 1 ) = 1.2423 × e( − 0.0064 × TPM) 3 – 200 mg TPM L − 1 0.92 Perna canaliculus Hawkins et al. (1999) C (L g − 1 h − 1 ) = 6.81 × (lnChl/1.1)2.71 2 – 3790 mg TPM L − 1 0.53 × e( − 2.71 × ((lnChl/1.11) − 1)) × e( − 0.19 × lnTPM) James et al. (2001) * C (L h − 1 ) = ( a × ( e( b × Chl) ))/(1 + (Chl/ c ) d ) 0.3 – 0.51 μ g Chl L − 1 0.83 Perna viridis Hawkins et al. (1998) C (L g − 1 h − 1 ) = 12.2 × POM − 0.90 2 – 17 mg POM L − 1 0.33 Wong and Cheung (2001b) C (L g − 1 h − 1 ) = 4.351 × TPM − 1.140 1 – 18 mg TPM L − 1 0.68 Wong and Cheung (2001b) C (L g − 1 h − 1 ) = 3.114 × TPM − 1.462 1 – 18 mg TPM L − 1 0.64 Pecten maximus Strohmeier et al. (2009) C (L h − 1 ) = 44.12 − 13.96(Chl) + 5.02(lnChl) 0 – 3 μ g Chl L − 1 0.44 + 0.018/(Chl)

Seston abundance was measured as chlorophyll a ( Chl ; μ g L − 1 ), total particulate matter ( TPM ; mg L − 1 ), particle volume ( Vol ; mm3 L − 1 ), and/or particulate organic matter (POM ; mg L − 1 ). * Equation constants not reported. 108 Bivalve fi lter feeding 109 of further change) and time- dependent physi- tion. Suspension feeding, however, might have ological acclimation processes in defi ning food indirect effects on suspended particles as well, acquisition processes has seldom been further contributing to benthic - pelagic cou- addressed (Bayne 1993 ). It has been suggested pling. Studies by Ward and coworkers demon- that at least some bivalves do not regulate food strate that bivalves and other suspension - feeders utilization over the short term, but utilize time- can produce signifi cant quantities of TEPs; averaged optimization behavior (Hawkins Mckee et al. 2005 ; Heinonen et al. 2007 ; Li et al. 1985 ). For example, if food availability et al. 2007 ). TEPs are discrete, gel - like parti- fl uctuates rapidly over short- time scales, the cles that can be found in both marine and animal may waste valuable internal resources freshwater systems (Alldredge et al. 1998 ; responding to every change. Although clearing Passow et al. 2001 ; Passow 2002 ). They are particles requires minimal energetic cost, the composed of high - molecular - weight muco- higher costs of digestion and the need to make polysaccharides that are released into the continuous digestive enzyme adjustments may water column by a variety of microorganisms make continous adaptation an overly wasteful including phytoplankton and bacteria (Decho strategy. The time- averaged optimization strat- 1990 ; Ki ø rboe and Hansen 1993 ; Passow and egy was supported by time series data on sea Alldredge 1994 ; Alldredge et al. 1998 ). The scallop feeding responses to storm - induced presence of TEPs can have a substantial impact dietary changes (Cranford et al. 1998 ). on coagulation effi ciency and fl occulation of suspended matter into marine snow (Alldredge et al. 1993 ; Passow 2002 ). TEPs can act as a glue that binds together small organic and Emerging k nowledge on e cosystem inorganic material, resulting in the formation i nteractions with the b ivalve b iofi lter of larger aggregates that sink rapidly to the benthos (Alldredge and Silver 1988 ; Alldredge Research on ecosystem- level interactions with et al. 1993 ; Ki ø rboe et al. 1994 ; Passow and the feeding activity of bivalve populations has Alldredge 1995 ). focused on the potential control of phyto- The abundance and distribution of TEPs in plankton assemblages and seston via particle the marine environment has been measured in depletion, and the consequences of excreted numerous studies (measured as gum xanthan and egested waste products to energy fl ow and [ GX ] equivalents). In general, mean TEP con- nutrient cycling. Two emerging research topics centrations are lower in open- ocean waters are briefl y summarized here that emphasize the − (e.g., 29 – 512 μ g GX L 1 , Engel 2004 ; Wurl need for consideration of additional effects of and Holmes 2008 ) and higher in coastal biofi ltration on coastal ecosystems. These − waters (e.g., 100 – 3500 μ g GX L 1 ; Passow effects further contribute to the characteriza- 2002 ; Wetz et al. 2009 ). Peak concentrations tion of some bivalve molluscs as “ ecosystem are associated with phytoplankton blooms, engineers. ” and high concentrations have been measured in near- shore waters inhabited by dense assemblages of corals, macroalgae, mangroves, Transparent exopolymer particle seagrasses, and suspension - feeders (e.g., ( TEP ) p roduction 290 – > 8000 μ g GX L − 1 , Ramaiah et al. 2001 , Fabriciusa et al. 2003 ; Mckee et al. 2005 ; The feeding processes of bivalves can directly Wurl and Holmes 2008 ; Wetz et al. 2009 ). The affect the water column through removal of concentration of TEPs at any specifi c location, suspended particulate matter, that is, biofi ltra- however, can vary widely depending on 110 Shellfi sh Aquaculture and the Environment local physical and biological conditions. One their major competitors and predators (ciliates potentially signifi cant source of TEPs in near - and fl agellates), the increased light availability shore waters is assemblages of suspension- that accompanies bivalve- mediated seston feeding bivalves. In laboratory studies, depletion, and the excretion of ammonia biomass - specifi c production rates of TEPs directly into nutrient - depleted summer surface from suspension - feeders fall within the range waters by the suspended culture. Picoplankton of 0.8– 6.7 μ g GX g − 1 h − 1 (Mckee et al. 2005 ; may become available to the bivalves, however, Heinonen et al. 2007 ; Li et al. 2007 ), but can through particle aggregation processes vary due to differences in water pumping (Cranford et al. 2005 ; Kach and Ward 2008 ), activity of the animals. Species- specifi c TEP or through linkage to higher tropic levels via production rates under natural conditions, the microzooplankton (Loret et al. 2000 ). however, may be higher. For example, in a fi eld Mesocosm studies show that mussel grazing study using benthic chambers, Mckee et al. can change phytoplankton species composi- (2005) measured a production rate for eastern tion, shifting the community to one dominated oysters of 34 μ g GX g − 1 h − 1 . Using this fi eld pro- by picoplankton (Olsson et al. 1992 ; Prins duction rate, an oyster with a dry tissue mass et al. 1997 ). Size - selective feeding by extensive of 1 g could produce about 816 μ g of TEPs in bivalve culture is thought to be an important 24 h. Although the fate and turnover time of reason why picoplankton cells constitute the TEPs is not entirely known (hours to months; most abundant component of the phytoplank- Passow 2002 ), some of this material is likely ton community in the Thau Lagoon in France transported both vertically and horizontally (Courties et al. 1994 ; Vaquer et al. 1996 ; away from shellfi sh beds. Bivalve - derived Souchu et al. 2001 ), and in Tracadie Bay, TEPs are known to enhance the aggregation of Canada (Cranford et al. 2008 ). Picoplankton suspended particulate matter (Li et al. 2007 ). species have also been shown to dominate the Therefore, such processes could increase depo- phytoplankton biomass in several embayments sition of particulate matter, and enhance supporting extensive suspended mussel culture benthic - pelagic coupling, in areas devoid of in Prince Edward Island (50 – 80% of total suspension - feeders. Chl), but not in an adjacent unfarmed bay where the microphytoplankton dominate (Cranford et al. 2008 ). That study showed a Size - dependent p article r etention close relationship between the average bay - wide picophytoplankton contribution and an Grazing of phytoplankton by dense assem- index of bay- scale seston depletion by mussel blages of bivalves not only has the potential to culture. Future research is needed to assess the change phytoplankton biomass but may also ecosystem consequences of this top - down affect community composition (Prins et al. destabilization of the food chain, including 1998 ; Nor é n et al. 1999 ). Bivalves effectively possible changes in predator– prey relation- retain particles larger than ∼ 2 – 8 μ m, depending ships and competitive interactions that could on the species, and therefore some nanoplank- result in trophic regime shifts. A shift from ton and all picoplankton (both photoautotro- microphytoplankton to picophytoplankton phic and heterotrophic) are not effectively biomass could affect particle transport dynam- captured and consumed. Picoplankton cells ics via reduced settling velocity and altered essentially exist within a size range that repre- fl occulation processes. The latter is dependent sents refugia from capture by bivalves and on the production of sticky exopolymers that where they may benefi t from bivalves depleting can be produced in large quantities by diatoms Bivalve fi lter feeding 111

(see also previous section). These potential the literature demonstrates that the opposing ecological effects of shellfi sh culture need to theory of autonomous feeding is obsolete. be better understood and considered in the Bivalve feeding behavior has important determination of carrying capacity predictions implications for aquaculture, including the and when considering implementing schemes optimization of farm location and layout, the that use bivalve farms for combating eutrophi- forecasting of bivalve growth and carrying cation (Lindahl et al. 2005 ). capacity, and the determination of potential ecological services and impacts. An abundance of information is available on the clearance Conclusions rate responses of bivalves in nature that can support these applications. Clearance rates are Forty years ago, Brian Morton wrote: “ The highly variable across short to long temporal view that bivalve molluscs are ideally adapted scales and large near - and far - fi eld differences to fulfi lling a mode of life in which the pro- in feeding behavior occur within the same cesses of feeding and digestion are continuous species. Predicting wild and farmed bivalve has long been accepted by most zoologists. An population responses to environmental vari- increasing amount of evidence, however, is ability over different scales is a major chal- being put forward to suggest that the opposite lenge. For clearance rate measurements to be is true, that is, that bivalves are discontinuous relevant to addressing aquaculture issues, they in their feeding and digestive habits” (Morton need to address scales of variation that are 1970 ). This evidence has since increased dra- relevant to the specifi c question being matically and, with few exceptions, reveals a addressed. Incorporating additional elements remarkable capacity of bivalve suspension - of environmentally induced physiological reg- feeders to fi nely adjust clearance rate as ulation into bivalve growth models is challeng- opposed to simply switching between feeding ing as it is diffi cut for the models to deal with and nonfeeding states (see Fig. 4.8 ). The above fi ne - scale temporal variations in the seston meta - analysis of the contemporary literature (Grant 1996 ). Despite this shortcoming, the demonstrates that accurate and comparable current modeling capacity appears suffi cient estimates of clearance rate can easily be for accurately replicating observed seasonal obtained using many direct and indirect meth- growth responses of bivalves (Chapter 6 in this odologies using familiar precautions. A major book), and also appears acceptable for accu- methodological pitfall stems from the applica- rately predicting effects of feeding on ambient tion of artifi cial dietary conditions that stimu- food supplies (see above). Nonetheless, site - late a predetermined (e.g., maximal) feeding and time - specifi c measurements of clearance response as a basis for developing theories on rate are encouraged whenever possible to help bivalve feeding behavior in nature. This improve or to test model applications. These approach represents an experimental bias that measurements will increase confi dence among defi es basic scientifi c principles, but has been aquaculture stakeholders on the practical and a prerequisite for all studies that continue to regulatory applications of population- level support the autonomous view of bivalve clearance calculations. They will also improve feeding. Whether or not the exhibited high ecophysiological and ecosystem model predic- fl exibility in clearance rates constitutes a tions and will increase capacity to address homeostatic strategy to maximize the individ- more specifi c questions related to fi ne - scale uals net energy balance is outside the scope of changes in feeding behavior. For example, this review. However, the preponderance of greater spatial resolution within models would 112

Figure 4.8 Blue mussels, Mytilus edulis , actively fi ltering seawater. (Courtesy of Tore Strohmeier and Ø ivind Strand.) Bivalve fi lter feeding 113 permit more quantitative assessments of the feeding, selection, and absorption of the optimal farm site location/layout and multi- oyster Crassostrea gigas . Journal of Experimental farm interactions, whereas increased temporal Marine Biology and Ecology 212 : 149 – 172 . resolution will aid in predicting Barill é , L. , Haure , J. , Pales - Espinosa , E. , and seasonally variable bivalve controls on the Moran ç ais, M. 2003 . Finding new diatoms for intensive rearing of the pacifi c oyster ( Crassostrea phytoplankton. Additional work is needed gigas ): energy budget as a selective tool. across a wide range of biogeographical set- Aquaculture 217 : 501 – 514 . tings, timescales, and species to further resolve Bauder , A.G. , Cembella , A.D. , Bricelj , V.M. , and details on the interactions between bivalves Quilliam , M.A. 2001 . Uptake and fate of diar- and their environment, and the way in which rhetic shellfi sh poisoning toxins from the dino- feeding responds to quantitative and qualita- fl agellate Procentrum lima in the bay scallop tive dietary stimuli. Argopecten irradians. Marine Ecology Progress Series 213 : 39 – 52 . Bayne , B.L. 1993 . Feeding physiology of bivalves: Literature cited time - dependence and compensation for changes in food availability . In: Dame , R.F. (ed.), Bivalve Ackerman , J.D. 1999 . Effect of velocity on the fi lter Filter Feeders in Estuarine and Marine Ecosystem feeding of dreissenid mussels (Dreissena poly- Processes , NATO ASI Series, Vol. G 33. Springer - morpha and Dreissena bugensis ): implications Verlag , Berlin , pp. 1 – 24 . for trophic dynamics. Canadian Journal of Bayne , B.L. 1998 . The physiology of suspension Fisheries and Aquatic Sciences 56 : 1551 – 1561 . feeding bivalve molluscs: an introduction to the Ackerman , J.D. , and Nishizaki , M.T. 2004 . The Plymouth “ TROPHEE ” workshop. Journal of effect of velocity on the suspension feeding and Experimental Marine Biology and Ecology growth of the marine mussels Mytilus trossulus 219 : 1 – 19 . and M. californianus : implications for niche Bayne , B.L. 1999 . Physiological components of separation . Journal of Marine Systems 49 : 195 – growth differences between individual oysters 207 . ( Crassostrea gigas) and a comparison with Alldredge , A.L. , and Silver , M.W. 1988 . Saccostrea commercialis. Physiological and Characteristics, dynamics and signifi cance of Biochemical Zoology 72 : 705 – 713 . marine snow . Progress in Oceanography 20 : Bayne , B.L. 2001 . Reply to comment by H.U. 41 – 82 . Riisg å rd . Ophelia 54 : 211 . Alldredge , A.L. , Passow , U. , and Logan , B.E. 1993 . Bayne , B.L. 2004 . Comparisons of measurements The abundance and signifi cance of a class of of clearance rates in bivalve molluscs . Marine large, transparent organic particles in the ocean. Ecology Progress Series 276 : 305 – 306 . Deep - Sea Res 40 : 1131 – 1140 . Bayne , B.L. , and Widdows , J. 1978 . The physiologi- Alldredge , A.L. , Passow , U. , and Haddock , S.H.D. cal ecology of two populations of Mytilus edulis 1998. The characteristics and transparent exo- L . Oecologia 37 : 137 – 162 . polymer particle (TEP) content of marine snow Berry , P.F. , and Schleyer , M.H. 1983 . The brown formed from thecate dinofl agellates . Journal of mussel Perna perna on the Natal coast, South Plankton Research 20 : 393 – 406. Africa: utilization of available food and energy Bacon , G.S. , MacDonald , B.A. , and Ward , J.E. budget . Marine Ecology Progress Series 1998. Physiological responses of infaunal ( Mya 13 : 201 – 210 . arenaria ) and epifaunal (Placopecten magellani- Bayne , B.L. , Klumpp , D.W. , and Clarke, K.R. 1984 . cus ) bivalves to variations in the concentration Aspects of feeding, including estimates of gut and quality of suspended particles I. Feeding residence time, in three mytilid species (Bivalvia, activity and selection. Journal of Experimental Mollusca) at two contrasting sites in the Cape Marine Biology and Ecology 219 :105 – 125 . Peninsula, South Africa . Oecologia 64 : 26 – 33 . Barill é , L. , Prou , J. , Heral , M. , and Razet , D. 1997 . Bayne , B.L. , Brown , D.A. , Burns , K. , Dixon , D.R. , Effects of high natural seston concentrations on Ivanovici , A. , Livingstone , D.R. , Lowe , D.M. , 114 Shellfi sh Aquaculture and the Environment

Moore , M.N. , Stebbing , A.R.D. , and Widdows , Cole , B.E. , Thompson , J.K. , and Cloern , J.E. 1992 . J. 1985 . The Effects of Stress and Pollution on Measurement of fi ltration rates by infaunal Marine Animals. Chapter 7: Physiological bivalves in a recirculating fl ume . Marine Biology Proceedures . Praeger , New York, pp. 161 – 178 . 113 : 219 – 225 . Bayne , B.L. , Hawkins , A.J.S. , and Navarro , E. Coughlan , J. 1969 . The estimation of fi ltration rate 1987 . Feeding and digestion by the mussel from the clearance of suspensions . Marine Mytilus edulis L. (Bivalvia: Mollusca) in mix- Biology 2 : 256 – 358 . tures of silt and algal cells at low concentrations. Courties , C. , Vaquer , A. , Troussellier, M. , Lautier , Journal of Experimental Marine Biology and J. , Chr é tiennot - Dinet , M.J. , Neveux , J. , Ecology 111 :1 – 22 . Machado , C. , and Claustre , H. 1994 . Smallest Bayne , B.L. , Hawkins , A.J.S. , Navarro , E. , and eukaryotic organism. Nature 370 : 255 . Iglesias , I.P. 1989 . Effects of seston concentra- Cranford , P .J. 2001 . Evaluating the “ reliability ” of tion on feeding, digestion and growth in the fi ltration rate measurements in bivalves. Marine mussel Mytilus edulis . Marine Ecology Progress Ecology Progress Series 215 : 303 – 305 . Series 55 : 47 – 54 . Cranford , P.J. , and Grant , J. 1990 . Particle Bayne , B.L. , Svensson , S. , and Nell , J.A. 1999 . The clearance and absorption of phytoplankton physiological basis for faster growth in the and detritus by the sea scallop Placopecten Sydney rock oyster, Saccostrea commercialis . magellanicus (Gmelin) . Journal of Experimental The Biological Bulletin 197 :377 – 387 . Marine Biology and Ecology 137 : 105 – 121 . Bougrier, S. , Geairon, P. , Deslous - Paoli , J.M. , Cranford , P.J. , and Gordon , D.C. 1992 . The infl u- Bacher , C. , and Jonqui è res , G. 1995 . Allometric ence of dilute clay suspensions on sea scallop relationships and effects of temperature on clear- ( Placopecten magellanicus) feeding activity and ance and oxygen consumption rates of tissue growth . Netherlands Journal of Sea Crassostrea gigas (Thunberg) . Aquaculture Research 30 : 107 – 120 . 134 : 143 – 154. Cranford , P.J. , and Hargrave , B.T. 1994 . In situ Bricelj , V.M. , and Malouf , R.E. 1984 . Infl uence of time - series measurement of ingestion and algal and suspended sediment concentrations on absorption rates of suspension- feeding bivalves: the feeding physiology of the hard clam Placopecten magellanicus (Gmelin). Limnology Mercenaria mercenaria. Marine Biology and Oceanography 39 : 730 – 738 . 84 : 155 – 165 . Cranford , P .J. , and Hill , P.S. 1999 . Seasonal varia- Buxton , C.D. , Newell , R.C. , and Field , J.G. 1981 . tion in food utilization by the suspension- feeding Response - surface analysis of the combined bivlave molluscs Mytilus edulis and Placopecten effects of exposure and acclimation temperatures magellanicus . Marine Ecology Progress Series on fi ltration, oxygen consumption and scope for 190 : 223 – 239 . growth in the oyster Ostrea edulis . Marine Cranford , P.J. , Emerson , C.W. , Hargrave , B.T. , and Ecology Progress Series 6 : 73 – 82 . Milligan , T.G. 1998 . In situ feeding and absorp- Chaparro , O.R. , and Thompson , R.J. 1998 . tion responses of sea scallops Placopecten mag- Physiological energetics of brooding in Chilean ellanicus (Gmelin) to storm - induced changes in oyster Ostrea chilensis . Marine Ecology Progress the quantity and composition of the seston . Series 171 : 151 – 163. Journal of Experimental Marine Biology and Chipman , W .A. , and Hopkins , J.G. 1954 . Water Ecology 219 : 5 – 70 . fi ltration by the bay scallop, Pecten irradians, as Cranford , P.J. , Armsworthy , S.L. , Mikkelsen , O. , observed with the use of radioactive plankton . and Milligan , T .G. 2005 . Food acquisition Biological Bulletin, Marine Biological responses of the suspension - feeding bivalve Laboratory, Woods Hole 107 :80 – 91 . Placopecten magellanicus to the fl occulation and Clausen , I. , and Riisg å rd , H.U. 1996 . Growth, fi l- settlement of a phytoplankton bloom. Journal of tration and respiration in the blue mussel, Experimental Marine Biology and Ecology Mytilus edulis: no evidence for physiological 326 : 128 – 143 . regulation of the fi lter- pump . Marine Ecology Cranford , P.J. , Li , W. , Strand, Ø . , and Strohmeier , Progress Series 141 :34 – 45 . T. 2008 . Phytoplankton depletion by mussel Bivalve fi lter feeding 115

aquaculture: high resolution mapping, ecosys- Engel , A. 2004 . Distribution of transparent exo- tem modeling and potential indicators of eco- polymer particles (TEP) in the Northeast Atlantic logical carrying capacity . ICES CM Document Ocean and their potential signifi cance for aggre- 2008/H:12. 5 p. www.ices.dk/products/CMdocs/ gation processes . Deep - Sea Research 51 : 83– CM - 2008/H/H1208.pdf 92 . Davenport , J. , and Woolmington , A.D. 1982 . A Essink , K. , Tydeman , P. , de Koning , F. , and Kleef , new method of monitoring ventilatory activity H.L. 1989 . On the adaptation of the mussel in mussels and its use in a study of the ventila- Mytilus edulis L. to different environmental sus- tory patterns of Mytilus edulis L . Journal of pended matter concentrations . In: Klekowski , Experimental Marine Biology and Ecology R.Z. , Styczynska - Jurewicz , E. , and Falkowski , 62 : 55 – 67 . L. (eds.), Proc. 21st Eur. Mar. Biol. Symp. Decho , A.W. 1990 . Microbial exopolymer secretion Gdansk, Poland, 1988 . Ossolineum, Gdansk , in ocean environments: their role in food webs 41 – 51 . and marine processes. Oceanography Marine Fabriciusa , K.E. , Wildb , C. , Wolanskia , E. , and Biology Annual Annual Review 28 : 73 – 153 . Abelec , D. 2003 . Effects of transparent exopoly- Dellatorre , F.G. , Pascual , M.S. , and Bar ó n , P.J. mer particles and muddy terrigenous sediments 2007. Feeding physiology of the Argentine on the survival of hard coral recruits . Estuarine, mussel Mytilus edulis platensis (d ’ Orbigny, Coastal and Shelf Science 57 : 613 – 621 . 1846): does it feed faster in suspended culture Famme , P. , Riisg å rd , H.U. , and Jorgensen , C.B. systems? Aquaculture International 15 : 415 – 1986 . On direct measurements of pumping rates 424 . in the mussel Mytilus edulis . Marine Biology Deslous - Paoli , J. - M. , H é ral , M. , Goulletquer , P. , 92 : 323 – 327 . Boromthanarat , W. , Razet , D. , Garnier , J. , Prou, Fegley, S.R. , MacDonald , B.A. , and Jacobsen , T.R. J. , and Barillet , L. 1987 . Evolution saisonniere 1992 . Short - term variation in the quantity and de la fi ltration de bivalves intertidaux dans des quality of seston available to benthic suspension conditions naturelles . Oc é anis 13 ( 4 – 5 ): 575 – feeders . Estuarine, Coastal and Shelf Science 579 . 34 : 393 – 412 . Doering , P.H. , and Oviatt , C.A. 1986 . Application Filgueira , R. , Labarta , U. , and Fernandez - Reiriz , of fi ltration rate models to fi eld populations of M.J. 2006 . Flow - through chamber method for bivalves: an assessment using experimental clearance rate measurements in bivalves: design mesocosms . Marine Ecology Progress Series and validation of individual chambers and meso- 31 : 265 – 275. cosm . Limnology and Oceanography Methods Dolmer , P. 2000 . Feeding activity of mussels Mytilus 4 : 284 – 292 . edulis related to near- bed currents and phyto- Filgueira , R. , Labarta , U. , and Fern á ndez - Reir í z , plankton biomass. Journal of Sea Research M.J. 2008 . Effect of condition index on allome- 44 : 221 – 231 . tric relationships of clearance rate in Mytilus Dowd , M. 1997 . On predicting the growth of cul- galloprovincialis Lamarck, 1819. Revista de tured bivalves . Ecological Modelling 104 : 113 – Biolog í a Marina y Oceanografi a 43 ( 2 ): 391 – 131 . 398 . Dunphy , B.J. , Hall , J.A. , Jeffs , A.G. , and Wells , Foster - Smith , R.L. 1975 . The effect of concentra- R.M.G. 2006 . Selective particle feeding by the tion of suspension on the fi ltration rates and Chilean oyster, Ostrea chilensis; implications for pseudofaecal production for Mytilus edulis (L.), nursery culture and broodstock conditioning . Cerastoderma edule (L.), and Venerupis pullas- Aquaculture 261 : 594 – 602. tra (Montaga). Journal of Experimental Marine Dupuy, C. , Vaquer , A. , Lam - H ö ai , T. , Rougier , C. , Biology and Ecology 17 : 1 – 22 . Mazouni , N. , Lautier , J. , Collos , Y. , and Le Gall , Frank , D.M. , Hamilton , J.F. , Ward , J.E. , and S. 2000 . Feeding rate of the oyster Crassostrea Shumway , S. 2007 . A fi ber optic sensor for high gigas in a natural phytoplankton community of resolution measurement and continuous moni- the Mediterranean Thau Lagoon . Marine toring of valve gape in bivalve molluscs . Journal Ecology Progress Series 205 :171 – 184 . of Shellfi sh Research 26 : 575 – 580 . 116 Shellfi sh Aquaculture and the Environment

Frank , D.M. , Ward , J.E. , Shumway , S.E. , Gray , C. , Haure , J. , Penisson , C. , Bougrier , S. , and Baud , J.P. and Holohan , B.A. 2008 . Application of particle 1998 . Infl uence of temperature on clearance and image velocimetry to the study of suspension oxygen consumption rates of the fl at oyster feeding in marine invertebrates . Marine and Ostrea edulis : determination of allometric coef- Freshwater Behaviour and Physiology 41 : 1 – 18 . fi cients . Aquaculture 169 : 211 – 224 . Fr é chette , M. , and Bacher , C. 1998 . A modelling Haure , J. , Huvet , A. , Palvadeau , H. , Nourry, M. , study of optimal stocking density of mussel pop- Penisson , C. , Martin , J.L.Y. , and Boudry , P. ulations kept in experimental tanks . Journal of 2003 . Feeding and respiratory time activities in Experimental Marine Biology and Ecology the cupped oysters Crassostrea gigas , Crassostrea 219 : 241 – 255 . angulata and their hybrids. Aquaculture Fr échette , M. , and Bourget , E. 1987 . Signifi cance of 218 : 539 – 551 . small - scale spatio- temporal heterogeneity in Hawkins , A.J.S. , and Bayne , B.L. 1992 . Physiological phytoplankton abundance for energy fl ow in interrelations, and the regulation of production. Mytilus edulis . Marine Biology 94 : 231 – 240 . In: Gosling , E. (ed.), The Mussel Mytilus: Fr é chette , M. , Booth , D.A. , Myrand , B. , and B é rard , Ecology, Physiology, Genetics and Culture . H. 1991 . V ariability and transport of organic Elsevier , Amsterdam , pp. 171 – 222 . seston near a mussel aquaculture site . ICES Hawkins , A.J.S. , Salkeld , P.N. , Bayne , B.L. , Gnaiger , Marine Science Symposium 192 :24 – 32 . E. , and Lowe , D.M. 1985 . Feeding and resource Gainey , L.F. , Walton , J.C. , and Greenberg , M.J. allocation in the mussel Mytilus edulis : evidence 2003 . Branchial musculature of a venerid clam: for time - averaged optimization . Marine Ecology pharmacology, distribution, and innervation. Progress Series 20 : 273 – 287 . The Biological Bulletin 204 :81 – 95 . Hawkins , A.J.S. , Navarro , E. , and Iglesias , J.I.P . Galtsoff , P.S. 1926 . New methods to measure the 1990 . Comparative allometries of gut- passage rate of fl ow produced by the gills of oysters and time, gut content and metabolic faecal loss in other Mollusca . Science 63 : 233 – 234. Mytilus edulis and Cerastoderms edule. Marine Gardner , J.P.A. , and Thompson , R.J. 2001 . The Biology 105 : 197 – 204 . effects of coastal and estuarine conditions on the Hawkins , A.J.S. , Smith , R.F.M. , Bayne , B.L. , and physiology and survivorship of the mussel H é ral , M. 1996 . Novel observations underlying Mytilus edulis and M. trossulus and their hybrids . the fast growth of suspension - feeding shellfi sh in Journal of Experimental Marine Biology and turbid environments: Mytilus edulis . Marine Ecology 265 :119 – 140 . Ecology Progress Series 131 : 179 – 190 . Gerdes , D. 1983 . The Pacifi c oyster Crassostrea Hawkins , A.J.S. , Smith , R.F.M. , Bougrier , S. , Bayne , gigas Part I. Feeding behaviour of larvae and B.L. , and H é ral , M. 1997 . Manipulation of adults . Aquaculture 31 : 195 – 219. dietary conditions for maximal growth in Gibbs , M.T. 2007 . Sustainability performance indi- mussels, Mytilus edulis, from the Marennes- cators for suspended bivalve aquaculture activi- Ol é ron Bay, France . Aquatic Living Resources ties . Ecological Indicators 7 : 94 – 107 . 10 : 13 – 22 . Grant , J. 1996 . The relationship of bioenergetics Hawkins , A.J.S. , Smith , R.F.M. , Tan , S.H. , and and the environment to the fi eld growth of cul- Yasin , Z.B. 1998 . Suspension - feeding behaviour tured bivalves. Journal of Experimental Marine in tropical bivalve molluscs: Perna viridis, Biology and Ecology 200 : 239 – 256. Crassostrea belcheri, Crassostrea iradelei, Grant , J. , Bacher , C. , Cranford , P.J. , Guyondet, T. , Saccostrea cucculata and Pinctada margarifera . and Carreau , M. 2008 . A spatially explicit eco- Marine Ecology Progress Series 166 : 173 – system model of seston depletion in dense mussel 185 . culture . Journal of Marine Systems 73 : 155 – Hawkins , A.J.S. , James , M.R. , Hickman , R.W. , 168 . Hatton , S. , and Weatherhead , M. 1999 . Griffi ths , R.J. 1980 . Filtration, respiration and Modelling of suspension - feeding and growth in assimilation in the black mussel Choromytilus the green - lipped mussel Perna canaliculus meridionalis . Marine Ecology Progress Series exposed to natural and experimental variations 3 : 63– 70 . of seston availability in the Marlborough Sounds, Bivalve fi lter feeding 117

New Zealand . Marine Ecology Progress Series Iglesias , J.I.P. , Urrutia , M.B. , Navarro , E. , Alvarez - 191 : 217 – 232 . Jorna , P. , Larretxea , X. , Bougrier , S. , and H é ral , Hawkins , A.J.S. , Fang , J.G. , Pascoe , P .L. , Zhang, M. 1996 . Variability of feeding processes in the J.H. , Zhang , X.L. , and Zhu , M.Y. 2001 . cockle Cerastoderma edule (L.) in response to Modelling short- term responsive adjustments in changes in seston concentration and composi- particle clearance rate among bivalve sispension- tion . Journal of Experimental Marine Biology feeders: separate unimodal effects of seston and Ecology 197 : 121 – 143 . volume and composition in the scallop Chlamys Iglesias , J. , Urrutia , M. , Navarro , E. , and farreri . Journal of Experimental Marine Biology Ibarrola , I. 1998 . Measuring feeding and absorp- and Ecology 262 : 61 – 73 . tion in suspension- feeding bivalves: an appraisal Hawkins , A.J.S. , Duarte , P. , Fang , J.G. , Pascoe , P.L. , of the biodeposition method . Journal of Zhang , J.H. , Zhang , X.L. , and Zhu , M.Y. 2002 . Experimental Marine Biology and Ecology A functional model of responsive suspension- 219 : 71 – 86 . feeding and growth in bivalve shellfi sh, confi g- James , M.R. , Weatherhead , M.A. , and Ross , A.H. ured and validated for the scallop Chlamys 2001 . Size - specifi c clearance, excretion, and res- farreri during culture in China. Journal of piration rates, and phytoplankton selectivity for Experimental Marine Biology and Ecology the mussel Perna canaliculus at low levels of 281 : 13 – 40 . natural food. New Zealand Journal of Marine Heinonen , K.B. , Ward , J.E. , and Holohan , B.A. and Freshwater Research 35 : 73 – 86 . 2007. Production of transparent exopolymer Jihong , Z. , Fang , J.G. , Hawkins , A.J.S. , and Pascoe , particles (TEP) by benthic suspension feeders in P.L. 2004 . The effect of temperature on clear- coastal systems . Journal of Experimental Marine ance rate and oxygen consumption of scallops, Biology and Ecology 341 : 184 – 195. Chlamys ferreri . Journal of Shellfi sh Research Hewitt , J.E. , and Pilditch , C.A. 2004 . Environmental 23 : 715 – 721 . history and physiological state infl uence feeding Jones , H.D. , Richards , O.G. , and Southern , T.A. responses of Atrina zelandica to suspended sedi- 1992 . Gill dimensions, water pumping rate and ment concentrations. Journal of Experimental body size in the mussel Mytilus edulis. Journal Marine Biology and Ecology 306 :95 – 112 . of Experimental Marine Biology and Ecology Hilbish , T.J. 1986 . Growth trajectories of shell and 155 : 213 – 237 . soft tissue in bivalves: seasonal variation in J ø rgenson , C.B. 1990 . Bivalve Filter Feeding: Mytilus edulis L. Journal of Experimental Hydrodynamics, Bioenergetics, Physiology and Marine Biology and Ecology 96 : 103 – 113 . Ecology . Olsen and Olsen, Fredensborg, Ibarrola , I., Navarro , E. , and Iglesias , J.I.P. 1998 . Denmark . Short - term adaptation of digestive processes in J ø rgenson , C.B. 1996 . Bivalve fi lter feeding revis- the cockle Cerastoderma edule exposed to dif- ited . Marine Ecology Progress Series 142 : 287 – ferent food quantity and quality. Journal of 302 . Comparative Physiology B 168 : 32 – 40 . J ø rgenson , C.B. , Larsen , P.S. , M ø hlenberg , M. , and Ibarrola , I. , Navarro , E. , and Urrutia , M.B. 2000 . Riisg å rd , H.U. 1988 . The bivalve pump: proper- Acute and acclimated digestive responses of the ties and modelling . Marine Ecology Progress cockle Cerastoderma edule (L.) to changes in Series 45 : 205 – 216 . food quality and quantity . Journal of J ø rgenson , C.B. , Larsen , P.S. , and Riisg å rd , H.U. Experimental Marine Biology and Ecology 1990 . Effects of temperature on the mussel 252 : 181 – 198. pump . Marine Ecology Progress Series 64 : 89 – Iglesias , J.I.P. , Navarro , E. , Alvarez , P.J. , and 97 . Armentia , Y. 1992 . Feeding, particle selection Kach , D.J. , and Ward , J.E. 2008 . The role of marine and absorption in cockles Cerastoderma edule aggragates in the ingestion of picoplankton- size (L) exposed to variable conditions of food particles by suspension - feeding molluscs. Marine concentration and quality . Journal of Biology 153 : 797 – 805 . Experimental Marine Biology and Ecology Kesarcodi - Watson , A. , Lucas , J.S. , and Klumpp , 162 : 177 – 198. D.W. 2001 . Comparative feeding and physiolog- 118 Shellfi sh Aquaculture and the Environment

ical energetics of diploid and triploid Sydney setting: application of a fl ow - cytometric tech- rock oysters, Saccostrea commercialis I. Effects nique . Aquaculture 296 : 237 – 245 . of oyster size . Aquaculture 203 :177 – 193 . Lindahl , O. , Hart , R. , Hernroth , B. , Kollberg , S. , Ki ø rboe , T. , and Hansen , J.L.S. 1993 . Phytoplankton Loo , L. - O. , Olrog , L. , Rehnstam - Holm , A. - S. , aggregate formation: observations of patterns Svensson , J. , Svensson , S. , and Syversen , U. and mechanisms of cell sticking and the signifi - 2005 . Improving marine water quality by mussel cance of exopolymer material . Journal of farming — a profi table solution for Swedish Plankton Research 15 : 993 – 1018 . society . Ambio 34 : 131 – 138 . Ki ϕ rboe , T. , M ϕ hlenberg , F. , and N ϕ hr , O. 1980 . Loret , P. , Gall , S.L. , Dupuy , C. , Blanchot , J. , Feeding, particle selection and carbon absorp- Pastoureaud , A. , Delesalle , B. , Caisey , X. , and tion in Mytilus edulis in different mixtures of Jonqui è res , G. 2000 . Heterotrophic protists as a algae and resuspended bottom material. Ophelia trophic link between picocyanobacteria and the 19 : 193 – 205. pearl oyster Pincada margaritifera in the Takapoto Ki ϕ rboe , T. , M ϕ hlenberg , F. , and N ϕ hr , O. 1981. lagoon (Tuamotu Archipelago, French Polynesia). Effect of suspended bottom material on growth Aquatic Microbial Ecology 22 : 215 – 226 . and energetics in Mytilus edulis. Marine Biology Lucas , M.I. , Newell , R.C. , Shumway , S.E. , Seiderer , 61 : 283 – 288 . L.J. , and Bally , R. 1987 . Particle clearance and Ki ø rboe , T. , Lundsgaard , C. , Olesen , M. , and yield in relation to bacterioplankton and sus- Hansen , J.L.S. 1994 . Aggregation and sedimen- pended particulate availability in estuarine and tation processes during a spring phytoplankton open coast populations of the mussel Mytilus bloom: a fi eld experiment to test coagulation edulis . Marine Ecology Progress Series 36 : theory . Journal of Marine Research 52 : 297 – 215 – 224 . 323 . MacDonald , B.A. , and Thompson , R.J. 1986 . Kittner , C. , and Riisgå rd , H.U. 2005 . Effect of tem- Infl uence of temperature and food availability perature on fi ltration rate in the mussel Mytilus on the ecological energetics of the giant scallop edulis : no evidence for temperature compensa- Placopecten magellanicus. III. Physiological tion . Marine Ecology Progress Series 305 : 147 – ecology, the gametogenic cycle and scope for 152 . growth . Marine Biology 93 : 37 – 48 . Labarta , U. , Fern á ndez - Reir í z , M.J. , and Babarro , MacDonald , B.A. , and Ward , J.E. 1994 . Variation J.M.F. 1997 . Differences in physiological ener- in food quality and particle selectivity in the sea getics between intertidal and raft cultivated scallop Placopecten magellanicus (Mollusca: mussels Mytilus galloprovincialis. Marine Bivalvia) . Marine Ecology Progress Series Ecology Progress Series 152 :167 – 173 . 108 : 251 – 264 . Lefebvre , S. , Barill é , L. , and Clerc , M. 2000 . Pacifi c MacDonald , B.A. , and Ward , J.E. 2009 . Feeding oyster ( Crassostrea gigas ) feeding responses activity of scallops and mussels measured simul- to a fi sh - farm effl uent . Aquaculture 187 : 185 – taneously in the fi eld: repeated measures sam- 198 . pling and implications for modelling . Journal of Li , S. - C. , Wang, W.- X. , and Hsieh , D.P.H. 2001 . Experimental Marine Biology and Ecology Feeding and absorption of the toxic dinofl agel- 371 : 42 – 50 . late Alexandrium tamarense by two marine MacDonald , B.A. , Robinson , S.M.C. , and bivalves from the south China Sea . Marine Barrington , K.A. 2009 . Evaluating the use of Biology 139 :617 – 624 . exhalent siphon area in estimationg feeding Li , B.L. , Ward , J.E. , and Holohan , B.A. 2007 . Effect activity of blue mussels, Mytilus edulis. Journal of transparent exopolymer particles (TEP) from of Shellfi sh Research 28 : 289 – 297 . suspension feeders on particle aggregation. Maire , O. , Amouroux , J. - M. , Duch ê ne , J. - C. , and Marine Ecology Progress Series 357 :67 – 77 . Gr é mare , A. 2007 . Relationship between fi ltra- Li , Y. , Veilleux , D.J. , and Wikfors , G.H. 2009 . tion activity and food availability in the Particle removal by Northern bay scallops Mediterranean mussel Mytilus galloprovincialis . Argopecten irradians irradians in a semi- natural Marine Biology 152 : 1293 – 1307 . Bivalve fi lter feeding 119

Mckee, M.P . , Ward , J.E. , MacDonald , B.A. , and Navarro , E. , Iglesias , J.I.P. , and Ortega , M.M. Holohan , B.A. 2005 . Production of transparent 1992 . Natural sediment as a food source for exopolymer particles (TEP) by the eastern oyster, the cockle Cerastoderma edule (L.): effect of Crassostrea virginica. Marine Ecology Progress variable particle concentration on feeding, diges- Series 288 : 141 – 149. tion and the scope for growth . Journal of McLusky , D.S. 1973 . The effect of temperature on Experimental Marine Biology and Ecology the oxygen consumption and fi ltration rate of 156 : 69 – 87 . Chlamys (Aequipecten ) opercularis (L.) Navarro , E. , Iglesias , J.I.P. , Ortega , M.M. , and (Bivalvia) . Ophelia 10 : 141 – 154. Larretxea, X. 1994 . The basis for a functional Medler , S. , and Silverman , H. 2001 . Muscular alter- response to variable food quantity and quality ation of gill geometry in vitro : implications for in cockles Cerastoderma edule (Bivalvia bivalve pumping processes . The Biological Cardiidae) . Physiological Zoology 67 : 468 – Bulletin 200 : 77 – 86 . 496 . Meyh ö fer , E. 1985 . Comparative pumping rates in Navarro , E. , Iglesias , J.I.P. , Perez Camacho, A. , and suspension - feeding bivalves. Marine Biology Labarta , U. 1996 . The effect of diets of phyto- 85 : 137 – 142 . plankton and suspended bottom material on M ø hlenberg , F. , and Riisgå rd , H.U. 1979 . Filtration feeding and absorption of raft mussels ( Mytilus rate, using a new indirect technique, in thirteen galloprovincialis Lmk). Journal of Experimental species of suspension - feeding bivalves. Marine Marine Biology and Ecology 198 : 175 – 189 . Biology 54 : 143 – 147. Navarro , J.M. , and Gonzá lez , C.M. 1998 . Morton , B. 1970 . The tidal rhythm and rhythm of Physiological responses of the Chilean scallop feeding and digestion in Cardium edule. Journal Argopecten purpuratus to decreasing salinities . of the Marine Biological Association of the Aquaculture 167 : 315 – 327 . United Kingdom 50 : 499 – 512. Navarro , J.M. , Leiva , G.E. , Martinez , G. , and Nakagawa , S. , and Cuthill , I.C. 2007 . Effect size, Aguilera , C. 2000 . Interactive effects of diet and confi dence interval and statistical signifi cance: a temperature on the scope for growth of the practical guide for biologists . Biology Reviews scallop Argopecten purpuratus during reproduc- of the Cambridge Philosophical Society 82 : tive conditioning . Journal of Experimental 591 – 605 . Marine Biology and Ecology 247 : 67 – 83 . Navarro , J.M. , and Widdows, J. 1997 . Feeding Navarro , E. , Labarta , U. , Fern á ndez - Reir í z , M.J. , physiology of Cerastoderma edule in response to and Velasco , A. 2003 . Feeding behaviour and a wide range of seston concentrations. Marine differential absorption of biochemical compo- Ecology Progress Series 152 :175 – 186 . nents by the infaunal bivalve Mulinia edulis and Navarro , J.M. , and Winter , J.E. 1982 . Ingestion the epibenthic Mytilus chilensis in response to rate, assimilation effi ciency and energy balance changes in food regimes. Journal of Experimental in Mytilus chilensis in relation to body size and Marine Biology and Ecology 287 : 13 – 35 . different algal concentrations . Marine Biology Newell , R.I.E. , and Bayne , B.L. 1980 . Seasonal 67 : 255 – 266 . changes in the physiology, reproductive condi- Navarro , J.M. , and Velasco , L.A. 2003 . Comparison tion and carbohydrate content of the cockle of two methods for measuring fi ltration rate in Cardium ( = Cerastoderma ) edule (Bivalvia: fi lter feeding bivalves. Journal of the Marine Cardiidae) . Marine Biology 56 : 11 – 19 . Biological Association of the United Kingdom Newell , R.C. , Johnson , L.G. , and Kofoed , L.H. 83 : 553 – 558. 1977 . Adjustment of the components of energy Navarro , E. , Iglesias , J.I.P. , Perez Camacho, A. , balance in response to temperature change in Labarta , U. , and Beiras , R. 1991 . The physiolog- Ostrea edulis. Oecologia (Berl.) 30 : 97 – 110 . ical energetics of mussels (Mytilus galloprovin- Newell , C.R. , Shumway , S.E. , Cucci , T.L. , and cialis Lmk) from different cultivation rafts in the Selvin , R. 1989 . The effect of natural seston Ria de Arosa (Galicia, N.W. Spain). Aquaculture particle size and type on feeding rates, feeding 94 : 197 – 212 . selectivity and food resource availability for the 120 Shellfi sh Aquaculture and the Environment

mussel Mytilus edulis Linnaeus, 1758 at bottom exopolymer particles (TEP) in the ocean. Marine cuture sites in Maine . Journal of Shellfi sh Ecology Progress Series 113 : 185 – 198 . Research 8 ( 1 ): 187 – 196 . Passow , U. , and Alldredge , A.L. 1995 . Aggregation Newell , C.R. , Campbell , D.E. , and Gallagher , S.M. of a diatom bloom in a mesocosm: the role of 1998 . Development of the mussel aquaculture transparent exopolymer particles (TEP). Deep - lease site model MUSMOD © : a fi eld program to Sea Research. Part II, Topical Studies in calibrate model formulations . Journal of Oceanography 42 : 99– 109 . Experimental Marine Biology and Ecology Passow , U. , Shipe , R.F. , Murray , A. , Pak , D.K. , and 219 : 143 – 169. Brzezinski , M.A. 2001 . Origin of transparent Newell , C.R. , Pilskaln , C.H. , Robinson, S.M. , and exopolymer particles (TEP) and their role in the MacDonald , B.A. 2005 . The contribution of sedimentation of particulate matter . Continental marine snow to the particle food supply of the Shelf Research 21 : 327 – 346 . benthic suspension feeder, Mytilus edulis . Journal P é rez Camacho, A. , Labarta , U. , and Navarro , E. of Experimental Marine Biology and Ecology 2000 . Energy balance of mussels Mytilus gallo- 321 : 109 – 124. provincialis : the effect of length and age. Marine Newell , C.R. , Wildish , D.J. , and MacDonald , B.A. Ecology Progress Series 199 : 149 – 158 . 2001 . The effects of velocity and seston concen- Pernet , F. , Tremblay , R. , Redjah , I. , S é vigny , J. - M. , tration on the exhalent siphon area, valve gape and Gionet , C. 2008 . Physiological and bio- and fi ltration rate of the mussel Mytilus edulis . chemical traits correlate with differences in Journal of Experimental Marine Biology and growth rate and temperature adaptation among Ecology 262 :91 – 111 . groups of the eastern oyster Crassostrea virgin- Nor é n, F. , Haamer , J. , and Lindahl, O. 1999 . ica . Journal of Experimental Biology 211 : Changes in the plankton community passing a 969 – 977 . Mytilus edulis bed. Mar. Ecol. Prog. Ser. Petersen , J.K. , Bougrier , S. , Small , A.C. , Garen , P. , 191 : 187 – 194 . Robert , S. , Larsen , J.E.N. , and Brummelhuis , E. Okumus , I. , and Stirling , H.P. 1994 . Physiological 2004 . Intercalibration of mussel Mytilus edulis energetics of cultivated mussel ( Mytilus edulis ) clearance rate measurements . Marine Ecology populations in two Scottish west coast sea lochs. Progress Series 267 : 197 – 194 . Marine Biology 119 : 125 – 131. Petersen , J.K. , Nielsen , T.G. , van Duren , L. , and Olsson , P. , Graneli , E. , Carlsson , P. , and Abreu, P. Maar , M. 2008 . Depletion of plankton in a raft 1992 . Structuring of a postspring phytoplankton culture of Mytilus galloprovincialis in R í a de community by manipulation of trophic interac- Vigo, NW Spain. I. Phytoplankton . Aquatic tions . Journal of Experimental Marine Biology Biology 4 : 113– 125 . and Ecology 158 : 249 – 266. Pilditch , C.A. , and Grant , J. 1999 . Effect of varia- Palmer , R.E. 1980 . Behaviour and rhythmic aspects tions in fl ow velocity and phytoplankton concen- of fi ltration in the bay scallop, Argopecten irra- tration on sea scallop (Placopecten magellanicus ) dians concentricus (Say) and the oyster, grazing rates. Journal of Experimental Marine Crassostrea virginica (Gmelin). Journal of Biology and Ecology 240 : 111 – 136 . Experimental Marine Biology and Ecology Podolsky , R.D. 1994 . Temperature and water vis- 45 : 273 – 295 . cosity: physiological versus mechanical effects Pascoe , P.L. , Parry , H.E. , and Hawkins , A.J.S. 2009 . on suspension feeding . Science 265 : 100 – Observations on the measurement and interpre- 103 . tation of clearance rate variations in suspension- Pouvreau , S. , Jonqui è res , G. , and Buestel , D. 1999 . feeding bivalve shellfi sh . Aquatic Biology Filtration by the pearl oyster, Pinctada mar- 6 : 181 – 190 . garitifera , under conditions of low seston load Passow, U. 2002 . Transparent Exopolymer Particles, and small particle size in a tropical lagoon TEP, in aquatic environments. Progress in habitat . Aquaculture 176 : 295 – 314 . Oceanography 55 : 287 – 333 . Pouvreau , S. , Bodoy , A. , and Buestel , D. 2000 . In Passow , U. , and Alldredge , A.L. 1994 . Distribution, situ suspension feeding behaviour of the pearl size and bacterial colonization of transparent oyster, Pinctada margaritifera : combined effects Bivalve fi lter feeding 121

of body size and weather - related seston compo- American bivalves . Marine Ecology Progress sition . Aquaculture 181 : 91 – 113 . Series 45 : 217 – 223 . Prins , T .C. , and Smaal , A.C. 1989 . Carbon and Riisg å rd , H.U. 1991 . Filtration rate and growth in nitrogen budgets of the mussel Mytilus edulis L. the blue mussel, Mytilus edulis Linnaeus, 1758: and the cockle Cerastoderma edule (L.) in rela- dependence on algal concentration. Journal of tion to food quality. Scientia Marina 53 : 477 – Shellfi sh Research 10 : 29 – 35 . 482 . Riisg å rd , H.U. 2001a . On measurement of fi ltration Prins , T.C. , Smaal , A.C. , and Power , A.J. 1991 . rates in bivalves— the stony road to reliable data: Selective ingestion of phytoplankton by the review and interpretation . Marine Ecology bivalves Mytilus edulis L. and Cerastoderma Progress Series 211 : 275 – 291 . edule (L.) . Hydrobiological Bulletin 25 : 93 – Riisg å rd , H.U. 2001b . Physiological regulation 100 . versus autonomous fi ltration in fi lter - feeding Prins , T.C. , Dankers , N. , and Smaal , A.C. 1994 . bivalves: starting points for progress. Ophelia Seasonal variation in the fi ltration rates of a 54 : 193 – 209 . semi - natural mussel bed in relation to seston Riisg å rd , H.U. 2004 . Intercalibration of methods composition . Journal of Experimental Marine for measurement of bivalve fi ltration rates — a Biology and Ecology 176 :69 – 86 . turning point. Marine Ecology Progress Series Prins , T.C. , Escaravage , V. , Smaal , A.C. , and Peeters , 276 : 307 – 308 . J.C.H. 1995 . Nutrient cycling and phytoplank- Riisg å rd , H.U. , and M ø hlenberg , F. 1979 . An ton dynamics in relation to mussel grazing in a improved automatic recording apparatus for mesocosm experiment. Ophelia 41 : 289 – 315 . determining the fi ltration rate of Mytilus edulis Prins , T.C. , Smaal , A. , and Dame , R. 1997 . A as a function of size and algal concentration . review of the feedbacks between grazing and Marine Biology 52 : 61 – 67 . ecosystem processes. Aquatic Ecology 31 : Riisg å rd , H.U. , and Randl ø v , A. 1981 . Energy 349 – 359 . budgets, growth and fi ltration rates in Mytilus Prins , T.C. , Smaal , A.C. , Pouwer , A.J. , and Dankers , edulis at different algal concentration. Marine N. 1996 . Filtration and resuspension of particu- Biology 61 : 227 – 234 . late matter and phytoplankton on an intertidal Riisg å rd , H.U. , Kittner , C. , and Seerup , D.F. 2003 . mussel bed in the Oosterschelde estuary (SW Regulation of the opening state and fi ltration Netherlands) . Marine Ecology Progress Series rate in fi lter - feeding bivlaves ( Cardium edule, 142 : 121 – 134. Mytilus edulis, Mya arenaria ) in response Ramaiah , N. , Yoshikawa , T. , and Furuya , K. 2001 . to low algal concentration. Journal of Experi- Temporal variations in transparent exopolymer mental Marine Biology and Ecology particles (TEP) associated with a diatom spring 284 : 105 – 127 . bloom in a subarctic ria in Japan. Marine Rodhouse , P.G. 1978 . Energy transformations by Ecology Progress Series 212 :79 – 88 . the oyster Ostrea edulis L. in a temperate estuary . Ren , J.S. , Ross, A.H. , and Schiel , D.R. 2000 . Journal of Experimental Marine Biology and Functional descriptions of feeding and energetics Ecology 34 : 1 – 22 . of the Pacifi c oyster Crassostrea gigas in New Saurel , C. , Gascoigne , J.C. , Palmer , M.R. , and Zealand . Marine Ecology Progress Series 208 : Kaiser , M.J. 2007 . In situ mussel feeding behav- 119 – 130 . iour in relation to multiple environmental Resgalla , C. , Brasil , E.S. , Laitano , K.S. , and Reis factors: regulation through food concentra- Filho , R.W. 2007 . Physioecology of the mussel tion and tidal conditions. Limnology and Perna perna (Mytilidae) in Southern Brasil. Oceanography 52( 5 ): 1919 – 1929 . Aquaculture 207 : 464 – 474. Seed , R. 1992 . Systematics, evolution and distribu- Riisg å rd , H.U. 1977 . On measurements of the fi l- tion of mussels belonging to the genus Mytilus: tration rates of suspension feeding bivalves in a an overview . American Malacological Bulletin fl ow system . Ophelia 16 : 167 – 173. 9 : 123 – 137 . Riisg å rd , H.U. 1988 . Effi ciency of particle retention Sicard , M.T. , Maeda - Martinez , A.N. , Ormart , P. , and fi ltration rate in 6 species of Northeast Reynoso - Granados, T. , and Carvalho , L. 1999 . 122 Shellfi sh Aquaculture and the Environment

Optimum temperature for growth in the Catarina Aulacomya ater (Molina) fed on a diet of kelp scallop ( Argopecten ventricosus - circularis , detritus of different ages. Marine Biology Letters Sowerby II, 1842). Journal of Shellfi sh Research 3 : 289 – 306 . 18 : 385 – 199. Thompson , R.J. 1984 . The reproductive cycle and Smaal , A.C. , and Twisk , F. 1997 . Filtration and physiological ecology of the mussel Mytilus absorption of Phaeocystis cf. globosa by the edulis in a subarctic, non - estuarine environment . mussel Mytilus edulis L. Journal of Experimental Marine Biology 79 : 277 – 288 . Marine Biology and Ecology 209 :33 – 46 . Thompson , R.J. , and Newell , R.I.E. 1985 . Smaal, A.C. , and Vonck , A.P.M.A. 1997 . Seasonal Physiological responses to temperature in two variation in C, N and P budgets and tissue latitudinally separated populations of the mussel, composition of the mussel Mytilus edulis . Marine Mytilus edulis . In: Gibbs , P.E. (ed.), Proceedings Ecology Progress Series 153 :167 – 179 . of the 19th European Marine Biology Symposium . Smaal , A.C. , and Zurburg , W. 1997 . The uptake Cambridge University Press, Cambridge , pp. and release of suspended and dissolved material 481 – 495 . by oysters and mussels in Marennes- Ol é ron Bay. Trottet , A. , Roy , S. , Tamigneaux , E. , Lovejoy , C. , Aquatic Living Resources 10 : 23 – 30 . and Tremblay , R. 2008 . Impact of suspended Smaal, A.C. , Vonck , A.P.M.A. , and Bakker , M. mussels (Mytilus edulis L.) on plankton com- 1997 . Seasonal variation in physiological ener- munities in a Magdalen Islands lagoon (Qué bec, getics of Mytilus edulis and Cerastoderma edule Canada): a mesocosm approach. Journal of of different size classes. Journal of the Marine Experimental Marine Biology and Ecology Biological Association of the United Kingdom 365 : 103 – 115 . 77 : 817 – 838. Urrutia , M.B. , Iglesias , J.I.P. , Navarro , E. , and Prou, Smaal , A.C. , Verhagen , J.H.G. , Coosen , J. , and J. 1996 . Feeding and absorption in Cerastoderma Haas , H.A. 1986 . Interaction between seston edule under environmental conditions in the Bay quantity and quality and benthic suspension of Marennes - Oleron (Western France). Journal feeders in the Oosterschelde, The Netherlands. of the Marine Biological Association of the Ophelia 26 : 385 – 399. United Kingdom 76 : 431 – 450 . Soletchnik , P. , Goulletquer , P. , H é ral , M. , Razet , D. , Urrutia , M.B. , Navarro , E. , Iglesias , J.I.P. , and and Geairon, P. 1996 . Evaluation di bilan é ner- Iglesias , J.I.P. 2001 . Preingestive selection pro- g é tique de l’ hu î tre creuse, Crassostrea gigas, en cesses in the cockle Cerastoderma edule: mucas baie de Marennes - Ol é ron (France). Aquatic production related to rejection of pseudofaeces . Living Resources 9 : 65 – 73 . Marine Ecology Progress Series 209 : 177 – Souchu , P. , Vaquer , A. , Collos , Y. , Landrein , S. , 187 . Deslous - Paoli , J. - M. , and Bibent , B. 2001 . Vahl , O. 1980 . Seasonal variations in seston and the Infl uence of shellfi sh farming activities on the growth rate of the Iceland Scallop, Chlamys biogeochemical composition of the water column islandica (O.F. Mü ller) from Balsfjord, 70° N . in Thau Lagoon . Marine Ecology Progress Series Journal of Experimental Marine Biology and 218 : 141 – 152 . Ecology 48 : 195 – 204 . Stenton - Dozey , J.M.E. , and Brown , A.C. 1994 . Van Erkon Schurink , C. , and Griffi ths , C.L. 1992 . Short - term changes in the energy balance of Physiological energetics of four South African Venerupis corrugatus (Bivalvia) in relation to mussel species in relation to body size, ration tidal availability of natural suspended particles. and temperature . Comparative Biochemistry Marine Ecology Progress Series 103 :57 – 64 . and Physiology 101A : 779 – 789 . Strohmeier , T. , Strand , Ø . , and Cranford , P. 2009 . Vaquer, A. , Troussellier , M. , Courtues , C. , and Clearance rates of the great scallop (Pecten Bibent , B. 1996 . tandind stock and dynamics of maximus ) and blue mussel (Mytilus edulis) at picophytoplankton in the Thau Lagoon (north- low seston concentrations . Marine Biology west Mediterranean coast) . Limnology and 156 : 1781 – 1795 . Oceanography 41 : 1821 – 1828 . Stuart , V. 1982 . Absorbed ration, respiratory cost Velasco , L.A. 2007 . Energetic physiology of the and resultant scope for growth in the mussel Caribbean scallops Argopecten nucleus and Bivalve fi lter feeding 123

Nodipecten nodosus fed with different microal- Widdows , J. 2001 . Bivalve clearance rates: inaccu- gal diets. Aquaculture 270 : 299 – 311. rate measurements or inaccurate reviews and Velasco , L.A. , and Navarro , J.M. 2002 . Feeding misrepresentation? Marine Ecology Progress physiology of infaunal (Mulinia edulis) and epi- Series 221 : 303 – 305 . faunal (Mytilus chilensis) bivalves under a wide Widdows , J. , and Bayne , B.L. 1971 . Temperature range of concentrations and qualities of seston. acclimation of Mytilus edulis with reference to Marine Ecology Progress Series 240 : 143 – its energy budget. Journal of the Marine 155 . Biological Association of the United Kingdom Velasco , L.A. , and Navarro , J.M. 2003 . Feeding 51 : 827 – 843 . physiology of two bivalves under laboratory and Widdows , J. , and Johnson , D. 1988 . Physiological fi eld conditions in response to variable food con- energetics of Mytilus edulis : scope for growth . centrations . Marine Ecology Progress Series Marine Ecology Progress Series 46 : 113 – 121 . 291 : 115 – 124. Widdows , J. , and Navarro , J.M. 2007 . Infl uence of Vismann , B. 1990 . Field measurements of fi ltration current speed on clearance rate, algal cell deple- and respiration rates in Mytilus edulis L. An tion in the water column and resuspension of assessment of methods . Sarsia 75 : 213 – 216 . biodeposits of cockles ( Cerastoderma edule ) . Ward, J.E. , and Shumway , S.E. 2004 . Separating Journal of Experimental Marine Biology and the grain from the chaff: particle selection in Ecology 343 : 44 – 51 . suspension - and deposit- feeding bivalves . Journal Widdows , J. , and Shick, J.M. 1985 . Physiological of Experimental Marine Biology and Ecology responses of Mytilus edulis and Cardium edule to 300 : 83 – 130 . aerial exposure . Marine Biology 85 : 217 – 232 . Ward , J.E. , Cassell , H.K. , and MacDonald , B.A. Widdows , J. , Fieth , P. , and Worrall , C.M. 1979 . 1992. Chemoreception in the sea scallop Relationships between seston, available food Placopecten magellanicus (Gmelin). I. and feeding activity in the common mussel Stimulatory effects of phytoplankton metabo- Mytilus edulis. Marine Biology 50 : 195 – 207 . lites on clearance and ingestion rates . Journal of Widdows , J. , Donkin , P. , Salkeld , P.N. , Cleary , J.J. , Experimental Marine Biology and Ecology Lowe , D.M. , Evans , S.V. , and Thomson , P.E. 163 : 235 – 250. 1984 . Relative importance of environmental Ward , J.E. , Sanford , L.P. , Newell , R.I.E. , and factors in determining physiological differences MacDonald , B.A. 1998 . A new explanation of between two populations of mussels (Mytilus particle capture in suspension - feeding bivalve edulis ) . Marine Ecology Progress Series molluscs . Limnology and Oceanography 17 : 33 – 47 . 43 : 741 – 752. Widdows , J. , Lucas , J.S. , Brinsley , M.D. , Salkeld , Wetz , M.S. , Robbins , M.C. , and Paerl , H.W. 2009 . P.N. , and Staff , F.J. 2002 . Investigation of the Transparent exopolymer particles (TEP) in a effects of current velocity on mussel feeding and river - dominated estuary: spatial - temporal distri- mussel bed stability using an annular fl ume . butions and an assessment of controls upon Helgoland Marine Research 56 : 3 – 12 . TEP formation. Estuaries and Coasts 32 : 447 – Wildish , D.J. , and Kristmanson , D.D. 1997 . Benthic 455 . Suspension Feeders and Flow. Cambridge Widdows , J. 1973 . The effects of temperature on the University Press, Cambridge . metabolism and activity of Mytilus edulis L. Wildish , D.J. , and Miyares , M.P. 1990 . Filtration Netherlands Journal of Sea Research 7 : 387 – 398 . rate of blue mussels as a function of fl ow velocity: Widdows , J. 1976 . Physiological adaptation of preliminary experiments . Journal of Experimental Mytilus edulis to cyclic temperatures. Journal of Marine Biology and Ecology 142 : 213 – 219 . Comparative Physiology 105 ( 2 ): 115 – 128 . Wildish , D.J. , and Saulnier , A.M. 1993 . Widdows , J. 1978 . Combined effects of body size, Hydrodynamic control of fi ltration in Placopecten food concentration and season on the physiol- magellanicus . Journal of Experimental Marine ogy of Mytilus edulis. Journal of the Marine Biology and Ecology 174 : 65 – 82 . Biological Association of the United Kingdom Wildish , D.J. , Kristmanson , D.D. , Hoar , R.L. , 58 : 109 – 124 . DeCoste , A.M. , McCormick , S.D. , and White, 124 Shellfi sh Aquaculture and the Environment

A.W. 1987 . Giant scallop feeding and growth Wong , W.H. , and Cheung , S.G. 2001b . Feeding responses to fl ow . Journal of Experimental rates and scope for growth of green mussel, Marine Biology and Ecology 113 :207 – 220 . Perna viridis (L.) and their relationship with Wildish , D.J. , Kristmanson , D.D. , and Saulnier , food availability in Kat O, Hong Kong . A.M. 1992 . Interactive effect of velocity and Aquaculture 193 : 123 – 137 . seston concentration on giant scallop feeding Wurl , O. , and Holmes , M. 2008 . The gelatinous inhibition . J. Exp. Mar. Biol. Ecol. 155 : nature of the sea - surface microlayer. Marine 161 – 168 . Chemistry 110 : 89 – 97 . Wilson , J.H. 1983 . Retention effi ciency and Yukihira, H. , Klumpp , D.W. , and Lucas , J.S. 1998 . pumping rate of Ostrea edulis in suspensions of Effects of body size on suspension feeding and Isochrysis galbana . Marine Ecology Progress energy budgets of the pearl oysters Pinctada Series 12 : 51 – 58 . margaritifera and P. maxima. Marine Ecology Winter , J.E. 1978 . A review of knowledge of sus- Progress Series 170 : 119 – 130 . pension - feeding in lamellibranchiate bivalves, Zeldis , J. , Robinson , K. , Ross , A. , and Hayden , B. with special reference to artifi cial aquaculture 2004 . First observations of predation by New systems . Aquaculture 13 : 1 – 33 . Zealand Greenshell mussels (Perna canaliculus ) Winter , J.E. , Acevedo , M.A. , and Navarro , J.M. on zooplankton. Journal of Experimental Marine 1984 . Quempill é n estuary, an experimental Biology and Ecology 311 : 287 – 299 . oyster cultivation station in southern Chile. Zhou , Y. , Yang , H. , Zhang , T. , Liu , S. , Zhang, S. , Energy balance in Ostrea chilensis. Marine Liu , Q. , Xiang , J. , and Zhang, F. 2006 . Infl uence Ecology Progress Series 20 : 151 – 164. of fi ltering and biodeposition by the cultured Wong, W.H. , and Cheung , S.G. 1999 . Feeding scallop Chlamys farreri on benthic - pelagic cou- behaviour of the green mussel, Perna viridis (L.): pling in a eutrophic bay in China . Marine responses to variation in seston quantity and Ecology Progress Series 317 : 127 – 141 . quality. Journal of Experimental Marine Biology Zurburg , W. , Smaal , A. , H é ral , M. , and Dankers , and Ecology 236 :191 – 207 . N. 1994 . Seston dynamics and bivalve feeding Wong, W.H. , and Cheung , S.G. 2001a . Feeding in the Bay of Marennes - Ol é ron (France). rhythms of the green- lipped mussel, Perna viridis Netherlands Journal of Aquatic Ecology (Linnaeus, 1758) (Bivalvia: Mytilidae) during 28 ( 3 – 4 ): 459 – 466 . spring and neap tidal cycles. Journal of Experimental Marine Biology and Ecology 257 : 13 – 36 .