Patchy Zooplankton Grazing and High Energy Conversion Efficiency: Ecological Implications of Sandeel Behavior and Strategy

Vol. 487: 123–133, 2013 MARINE ECOLOGY PROGRESS SERIES Published July 30 doi: 10.3354/meps10390 Mar Ecol Prog Ser

Patchy zooplankton grazing and high energy conversion efficiency: ecological implications of sandeel behavior and strategy

Mikael van Deurs*, Asbjørn Christensen, Anna Rindorf

DTU Aqua National Institute of Aquatic Resources, Technical University of Denmark (DTU), Jægersborg Alle 1, Charlottenlund Castle, 2920 Charlottenlund, Denmark

ABSTRACT: Sandeels display strong site fidelity and spend most of their life buried in the seabed. This strategy carries important ecological implications. Sandeels save energy when they are not foraging, but in return are unable to move substantially and may therefore be sensitive to local depletion of prey. We studied zooplankton consumption and energy conversion efficiency of the lesser sandeel Ammodytes marinus in the central North Sea, using stomach data, length and weight-at-age data, bioenergetics, and hydrodynamic modeling. The results suggested the following. (1) Lesser sandeels in the Dogger area depend largely on relatively large copepods in early spring. (2) The lesser sandeel is an efficient converter, making secondary production into fish tissue available for higher trophic levels. Hence, changes in species composition towards a more herring-dominated system, as seen in recent times, may lead to a decrease in system transfer efficiency. (3) Sandeels leave footprints in the standing copepod biomass as far as 100 km from the edge of their habitat, but smaller and more isolated sandeel habitat patches have a much lower impact than larger patches, suggesting that smaller habitats can sustain higher sandeel densities and growth rates per area than larger habitats. We conclude that sandeel behavior and strategy have ecosystem implications.

KEY WORDS: Sand lance · Food web · Trophic transfer efficiency · Bioenergetics · Growth · Food consumption · North Sea · Dogger

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INTRODUCTION plankton and thereby converting secondary production into fish tissue, which is in turn available to mar- In marine ecosystems, the main flow of energy ine predators higher in the food web. If the energy from secondary producers to larger fish, birds, and conversion efficiency of the forage fish community is mammals is often channeled through just a few key high, more of the energy ingested in the form of sec- species of small schooling fish, the so-called forage ondary producers becomes available for production fishes (Cury et al. 2000). Forage fish is a functional at higher trophic levels, and less will be lost through group characterized by fast somatic growth, early respiration. Energy conversion efficiency is therefore maturation, planktivory, and schooling behavior, and an important ecological aspect of the food web, and represents a major energy resource to a wide variety has been proposed as a major determinant of food- of predators (Alder et al. 2008). In the central North chain length (the energy-flow hypothesis) and preda- Sea, the most important forage fishes are the lesser tor production (e.g. Yodzis 1984, Rand & Stewart sandeel Ammodytes marinus (hereafter ‘sandeel’) 1998, Trussell et al. 2006). and 2 clupeids, herring Clupea harengus and sprat Although sandeels share the general characteristics Sprattus sprattus. These species act as major food- of a forage fish, they possess several unique traits. web energy conveyers, grazing vigorously on zoo- Sandeels spend a large part of their juvenile and adult

*Email: [email protected] © Inter-Research 2013 · www.int-res.com 124 Mar Ecol Prog Ser 487: 123–133, 2013

life buried in the seabed in areas with well-oxygenated bottom substrate consisting of gravel or coarse sand (Reay 1970, Jensen et al. 2011). They remain buried throughout the diel cycle in winter, except during spawning around the beginning of the year. However, in early spring, they start to emerge every day to feed, and become one of the most abundant fish species in the water column of the North Sea for the following 3 to 4 mo (Macer 1966, Winslade 1974, MacLeod et al. 2007). When burrowed, sandeels are motionless and their metabolism is reduced to a minimum (e.g. Behrens et al. 2007, van Deurs et al. 2011a). This cryp- tic energy-saving behavior potentially renders sandeels more efficient as food-web energy conveyers compared to forage fish with more active behavior. Another unique trait of sandeels is the high degree of site fidelity, resulting in a foraging behavior resem- bling that of central place foragers. Feeding takes place near their nightly burying habitat (e.g. Engelhard et al. 2008, van der Kooij et al. 2008, Jensen et al. 2011). Therefore, the movement of water and associated zoo- Fig. 1. Study area showing sandeel Ammodytes marinus habitats (Jensen et al. 2011) (white patches), locations of the plankton relative to the fixed location of the sandeels is commercial hauls providing information on growth (clusters likely to greatly influence the food available to the of grey dots), and locations of stomach sampling (black dots). sandeels and thus their impact on the local zooplank- Black surfaces are land (eastern UK) ton. In contrast, fully pelagic forage fishes such as clupeids are able to move more freely in response to food the Danish Fisherman’s Association and the Techni- density (Dragesund et al. 1997, Corten 2001) and can cal University of Denmark. Samples were taken at effectively graze continuously on the same copepod sea by the fishermen and immediately frozen. Sam- population for prolonged periods of time. ples were later transported, to gether with informa- The aim of the present study was to explore the tion on haul location and time, to the university for ecological implications of these 2 unique traits of further analysis. In the laboratory, a subsample of sandeels, with particular focus on energy conversion each sample was measured and rounded down to the efficiency and site fidelity. We studied lesser sand- nearest half centimeter group. Ten sandeels per half eels inhabiting the sand banks in the Dogger area centimeter group were randomly selected, and age located in the frontal region of the central North Sea was determined using otoliths. For further details, (Fig. 1). First, the amount of zooplankton consumed see Jensen et al. (2011). Mean length-at-age was by sandeels was estimated from stomach contents estimated by combining length distributions with and bioenergetics. Second, the energy conversion age-length keys. Age-length keys were produced efficiency from ingested zooplankton to fish tissue separately for each distinct fishing ground and week was calculated for sandeels. Third, the ecosystem using the method described by Rindorf & Lewy effects of differential energy conversion efficiencies (2001). Condition was estimated as weight (g)/total among forage fishes were analyzed. Lastly, the graz- length (cm)b, where b = 3.06 is equal to the exponent ing pressure on local zooplankton communities was of the power law function describing fish weight as a modeled by taking water movement and sandeel site function of total length when all data is used. Only fidelity into account. samples collected between 2001 and 2008 (a period of consistently high sampling intensity throughout the second quarter of the year) and from the major MATERIALS AND METHODS fishing grounds were used (Fig. 1). During the same sampling program, a total of Sampling and data 472 sandeel stomachs were analyzed. Stomachs were collected between 2006 and 2008 (in April, May, and Sandeel samples were collected during a data col- June) from all over the Dogger area. Stomachs were lection program carried out in cooperation between removed, then gently dabbed on both sides with van Deurs et al.: Ecological implications of sandeel strategy 125

tissue before being weighed (g wet weight). Approxi- spring. Based on this data, copepods were given an mately every third stomach was put aside after energy density of 3200 J g−1 wet weight for individu- weighing for further diet analysis (preserved in 98% als <1.3 mm, and 5600 J g−1 wet weight for larger alcohol). copepods. Average energy density of the diet, ed, was then determined from the proportion of large

(>1.3 mm) copepods observed in the diet, Plarge, as Amount of zooplankton consumed ed = 3200(1 − Plarge) + 5600Plarge.

Two approaches were used to estimate consumption by sandeels: stomach contents and bioenergetic Daily ration estimated from stomach data calculation. The weight of the stomach contents was used to estimate consumption for the period in which We assumed a simple Bajkov-type relationship the samples were taken. This is often seen as a more between the amount of food consumed and the accurate method than bioenergetics modeling when amount of food in the stomach (e.g. Eggers 1977), growth is food-limited (Elliott & Persson 1978). In and calculated the weight-specific daily ration RD contrast, bioenergetic modeling provides the oppor- (weight of daily food intake relative to body weight) tunity to estimate food consumption over longer as: periods in which the sampling of stomachs becomes 24φ()TW× increasingly labor-intensive. Before any estimates of R = S (1) D W* consumption were made, a diet analysis was carried out to investigate the size distribution of copepods. φ(T) is the evacuation coefficient as a function of This information was necessary to account for the temperature, and was adopted from van Deurs et

different energy densities of different-sized cope- al. (2010). WS is the net weight of the stomach (g wet pods (e.g. Corner & O’Hara 1986). weight) (total weight of the stomach minus the weight of the emptied stomach; weights of empty stomachs were estimated based on a curve fitted to Diet analysis 30 empty stomachs). W* is the mean body weight of the fish, defined as the body weight halfway through

Stomach contents were spread evenly on a Petri the growth period. RD was calculated for each fish dish with 2 to 3 mm of water. A sub-area of 4 cm2 in separately to allow us to calculate the geometric the middle of the dish was photographed using a mean and standard error for various length intervals stereo-microscope. Copepods completely dominated and for early and late spring. Note that RD is directly the diet. Other organisms, such as annelids, crusta - comparable to daily consumption as derived from cean larvae, amphipods, appendicularians, and fish bioenergetics described in the next section. Stomach eggs each constituted ~1% of the diet. Further analy- data were only available for adults. ses therefore focused on copepods. A reliable quanti- tative separation into copepod species was not possi- ble due to the advanced stage of digestion of the Bioenergetic modeling of consumption stomach contents. Instead, Image Pro Plus software was used to digitally measure the length of all intact Conventional bioenergetic calculations consider copepod prosomes, ignoring stomach contents in growth over time as a function of consumption, respi- advanced stages of digestion. Laboratory experi- ration, egestion, and excretion (e.g. Hansen et al. ments have shown that sandeels prefer fish larvae 1993). However, in the present study, the calculations over copepods (Christensen 2010). Hence, to inves - were inverted in order to find the amount of energy tigate whether a major proportion of sandeels’ diet required to obtain observed changes in growth and consists of fish larvae, we also examined the stomach condition over time. Input values to the bioenergetics contents for pieces of fish larvae. calculations were therefore observed total length (L, cm) and condition (K) on the first (t1) and last day of the year (t2) of the calculation period. Calculation Energy density of copepods of different sizes periods for adults (Age 1 and Age 2) were taken as the entire growth period (April 1 to June 30), and Corner & O’Hara (1986) reported the monthly early and late spring separately (April 1 to May 15 energy content of 4 North Sea copepod species in and May 15 to June 30), corresponding to the first 126 Mar Ecol Prog Ser 487: 123–133, 2013

and second half of the growth period (Macer 1966, Winslade 1974, MacLeod et al. 2007). For juveniles (Age 0), we assumed a summertime growth period of 100 d (not split into early and late growth/spring as for the adults). Lt1, Lt2, Kt1, and Kt2 for adults were determined by fitting a 4th-order polynomial to ob - served weekly mean length or weekly mean condition as a function of week (Figs. 2 & 3), except for early spring Age 2 fish, where we assumed Lt1(Age 2) = Lt2(Age 1). Juveniles (Age 0) were poorly represented in the samples, since they metamorphose and settle to the sand banks after the main fishing season has ended. We therefore chose to define Lt1(juveniles) and Lt2(juveniles) as the size at metamorphosis (5 cm; Wright & Bailey 1996) and Lt2(juveniles) = Lt1(Age 1), and values of K and K were assumed identical to t1(juveniles) t2(juveniles) Fig. 2. Ammodytes marinus. Length during the growth pe- those of Age 1 sandeels. riod of adult lesser sandeels (black: Age 1; grey: Age 2). Individual food consumption in terms of energy Curves were created by fitting a 4th-order polynomial to (CE, J) for a given age-class and period was calcu- data. Vertical dashed line represents the split between early lated as: and late spring (Week 18 is included in late spring) ΔΔEEM++ C = sR (2) E 07. where ΔEs and ΔER are the change in body energy (J) attributable to structural growth (length growth) and energy reserves (condition increase), respectively, taking place over the calculation period, M is metabolism (J ind.−1 h−1) (see Eq. 3), and 0.7 is the universal assimilation efficiency for fish (Ciannelli et al. 1998).

ΔEs and ΔER were calculated from the change in mass of structural tissue (Δms, g) and energy reserves (ΔmR, g) over the time period: ΔEs = 4500Δms and ΔEs = 4500Δms, where the coefficients 4500 and 8600 represent energy densities (J g−1) of structural tissue and energy reserves, respectively. Energy density of structural tissue was derived from Hislop Fig. 3. Ammodytes marinus. Condition factor (weight/ et al. (1991, their Table 2) (data from March/April length3.06) during the growth period of adult lesser sandeels when reserves of lesser sandeel are at their mini- (black: Age 1; grey: Age 2). Curves were created by fit - mum), and energy density of reserves from van ting a 4th-order polynomial to data. Vertical dashed line Deurs et al. (2011a). Δm and Δm were calculated as represents the split between early and late spring (Week 18 s R is included in late spring) Δ 3.06 3.06 Δ 3.06 ms = (Kt1Lt2 ) − (Kt1Lt1 ) and mR = (Kt2Lt2 ) − 3.06 (Kt1Lt2 ). The exponent 3.06 corresponds to the b exponent mentioned in ‘Sampling and data’. The lat- bolic rate in the period t1 to t2 is simply 24SMR × ter equa tion is more accurate when Kt1 approaches (t2− t1), where t1 and t2 are given as days of the K minimum. CE(late spring) was therefore approximated from year. The metabolic cost of swimming was estimated CE(entire growth period) − CE(early spring) rather than using as the product of the hours spent swimming per day the equation. (β), an activity multiplier (α), and the duration of the Metabolism M (used in Eq. 2) was modeled as the calculation period t1 to t2: αSMRβ × (t2 − t1), where standard metabolic rate (SMR, J ind.−1 h−1) plus the α was given the default value 3.3 (from: van Deurs et metabolic cost of swimming during the daily foraging al. 2010). This activity multiplier is in agreement with period. Specific dynamic action (the metabolic cost Boisclair & Sirois (1993). The duration of the daily associated with digesting a meal) is accounted for in activity period was set to β = 10 h, in accordance the assimilation coefficient in Eq. (2). Standard meta- with laboratory experiments (van Deurs et al. 2011b). van Deurs et al.: Ecological implications of sandeel strategy 127

Together, this resulted in an estimate of M in the since some of the reserve accumulated during the calculation period t1 to t2 of:0 growth period fuels metabolism outside the growth period. To allow a comparison, we also estimated M = 24SMR[t2 – t1] + 33SMR[t2 – t1] (3) annual energy conversion efficiency for sandeels. SMR was modeled as a function of body mass and This was done by including the metabolic cost of temperature and was adopted directly from van overwintering in Eq. (6) as follows: CEannual(sandeel) = 0.8 Deurs et al. (2011a): SMR = 1.36W × (0.08T − 0.25), (ΔEs + ΔER − Cost of overwintering)/C E × 100%, where 2.66 where W is the weight of the fish (g wet weight) (here Cost of overwintering = 18.69Lt2 (J) (derived from defined as the weight halfway through the calcu- van Deurs et al. 2011a, their Table 2). lation period, back-calculated from Figs. 2 & 3 using W = K × L3.06). T is the mean sea surface temperature during the calculation period as provided by the Ecosystem effects Danish Meteorological Institute.

Weight-specific daily consumption (Cw, in propor- To explore the potential ecosystem effects of the tion of body weight) was estimated as: contribution of sandeels to the forage fish community, we calculated the combined annual energy con- CWB /* CW = (4) version efficiency of the North Sea forage fish com- (–)tt21 munity (sandeels and clupeids) for each year from where CB is the total biomass consumed per individ- 1974 to 2010 as: ual during the calculation period (g ind.−1) calculated BB(sandeel)××CE (sandeel) (clupeiid)× CE (clupeid) as: CB = CE/ed, where ed corresponds to the energy CE = (foragefish) B content of the diet (from ‘Energy density of copepods (foragefish) (7) of different sizes’).W* is the mean body weight of the fish defined as the body weight halfway through the where CE is conversion efficiency and B is the stock growth period. biomass in a given year (B(clupeid) includes both her- Population-level consumption rate per surface area ring and sprat). Stock biomasses of all species were −1 −2 (CP, g wet weight d m ) was estimated as: derived from the multispecies model (SMS) of the North Sea (Lewy & Vinther 2004, ICES 2011b). CNttB ××(–)21 CP = (5) CE(foragefish) was calculated using either annual values or 15× 109 growth period-specific CE values. CEgrowthperiod(sandeel) where CB corresponds to the definition given under and CEannual(sandeel) are calculated above ‘Conversion Eq. (4). N is the average stock number for the period efficiency of sandeels’ (we used the average across 2001 to 2008 and for the sandeel stock assessment age-classes). The growth period-specific value for Area 1 (corresponding to the Dogger area) in ICES clupeids was derived from values for Atlantic (2011a), and 15 × 109 is roughly the combined surface herring Clupea harengus given in Varpe et al. area (m−2) of sandeel habitats in the Dogger area (2005) and De Silva & Balbontin (1974), resulting in

(Jensen et al. 2011). CEgrowthperiod(clupeids) = 15%. Annual values were not available for Atlantic herring, sprat, or any closely related species. We therefore chose 10% for the Conversion efficiency of sandeels purpose of these calculations, assuming herring spent accumulated reserves during overwintering The energy conversion efficiency during the growth and spawning migration. period CEgrowthperiod (% of ingested energy that is con- verted to fish tissue via structural growth or reserve accumulation) was calculated as: Grazing pressure on local zooplankton communities

ΔΔEE+ CE = sR× 100 (6) Grazing pressure and local gradients in copepod growthperiod C E concentrations resulting from patchy distribution of where ΔEs, ΔER, and CE are taken from Eq. (2). In the sandeels were investigated using a simple logistic literature, energy conversion efficiency is either grazing/production model coupled to a 3-dimensional given specifically for the growth period or the entire operational ocean circulation model, the Danish year. For zooplanktivorous fishes in seasonal envi- Meteorological Institute hydrodynamical operational ronments, the annual value is expected to be lower, model, BSHCmod. De tails of performance and model 128 Mar Ecol Prog Ser 487: 123–133, 2013

results verification of this model are reported in grazing ratio averaged over the entire simulation

Larsen et al. (2007) and She et al. (2007a,b). area: ρ2 = Sandeel grazing/Total grazing (averaged The grazing/production model was formulated as over the simulation). Lastly, the spatial heterogeneity a differential equation: scale in copepod concen trations, resulting from patchy distribution of grazing sandeels, was investi- Δc ⎛ c ⎞ = λμμc 1− − ()sandeel + 0 c (8) gated by depicting the average copepod concentra- t ⎝ c0 ⎠ Δ tion (averaged over the entire simulation period) for where Δc/Δt is the change in copepod concentration each grid cell in a color gradient map. c for a given time interval t, c0 is the copepod carrying capacity (given as a concentration) of the system in the absence of grazing, λ is 1/(produc tion time RESULTS scale), μsandeel is grazing pressure exerted by sand - eels, and μ0 is a background grazing level provided Zooplankton consumption by other grazers in the region. The first term on the right-hand side of the equation can be interpreted as During early spring, larger copepods dominated the copepod production p, and provides a production the stomach contents of adult sandeels. Cope pods time scale (1/λ) and a copepod concentration (c) that with prosome lengths around 2.25 mm were the most equals carrying capacity of the system (c0) in the important. Juvenile sandeels were not available for absence of grazing. The second term on the right- stomach sampling. In late spring, smaller copepods hand side of the equation is the grazing term. The dominated in terms of numbers, but biomass-wise, equation was parameterized by assuming (1) a cope- relatively large copepods (>1.5 mm) were still the pod vertical distribution (δ ) of 0 to 8 m from the sur- more important food source (Fig. 4). face; (2) production maximum = 0.5c0; (3) a regional There was a large degree of similarity between characteristic copepod production pδ = 1.5 g wet daily consumption (CW; bioenergetic approach) and −2 −1 weight m d and copepod concentration cδ = 15 g daily ration (RD; stomach data) (Fig. 5). Both methods wet weight m−2 (Nielsen & Munk 1998; see also Berg - resulted in lower estimates of consumption in late green et al. 1988); (4) total grazing (sandeels plus spring compared to early spring. Parameter values other) equals total copepod production; and (5) graz- used in the bioenergetics calculations are summa- ing rate of sandeels (μsandeelδc) equals the sum of rized in Table 1. At the individual level, juvenile CP(Age 1) plus CP(Age 2) from Eqn. (5). sandeels (summer) had higher weight-specific con- The differential equation was solved using Euler- sumption compared to adults (spring), but lower ian forward simulations performed by solving mass absolute consumption due to their lower weight. For balance equations for each grid cell (6 × 6 nautical adults, consumption rates were highest during early miles) on a computational grid. Mass fluxes over grid spring (Table 2). cells were derived from spatially and temporally varying water currents provided by the circulation model. The Eulerian simulation period was April Conversion efficiency 2007 to June 2007 (corresponding to the growth period for adult sandeels). The computational grid The consumed secondary production was con- was restricted to the Dogger area (53.5 to 56°N and verted to sandeel biomass with an energy conversion 1 to 5°E), and Dirichlet boundary conditions were efficiency of 32 to 56% within the growth period. applied. Information about the geographical distri- Energy conversion efficiency was lowest for Age 2 in bution of sandeel habitat (Christensen et al. 2009, late spring, and in general, highest during early Jensen et al. 2011) was used to constrain grazing to spring. Annual energy conversion efficiencies were defined grid cells within the computational grid. As a considerably lower (Table 2). simplification, spatio-temporal variation in sandeel The sensitivity of the model to the activity multi- consumption rate and copepod production rate were plier (α), daily activity period (β), timing of the neglected. growth period (t2 − t1), and temperature (T) was Grazing pressure was quantified as (1) the average low. Estimated consumption and energy conversion fraction of the copepod biomass grazed by sandeels efficiency varied no more than 5% in response to inside sandeel habitats relative to the total grazing of decreasing or increasing these parameter values by copepods inside sandeel habitats: ρ1 = μsandeel/(μsandeel 15%, except for T, which varied between 5 and 8% + μ0) (averaged over the simulation), and (2) the bulk depending on the age of the fish (8% for Age 2). van Deurs et al.: Ecological implications of sandeel strategy 129

Ecosystem effects

The results suggest that the proportion of sandeels in the forage fish community has ecosystem implications, although the extent depends on whether calculations are based on growth period efficiency or annual efficiency. The combined forage fish energy conversion efficiency (of the growth period) varied markedly be tween 1974 and 2010, and decreased by 35% in the period 2003 to 2005 (a period of low sandeel stock biomass) compared to the average level from 1974 to 2000. This was ap- proximately halved (17%) when annual efficiencies were used (Fig. 6).

Grazing pressure on local zooplankton communities

Fig. 4. Ammodytes marinus. Size composition of copepods in the diet of lesser sandeels in (A,B) early spring and (C,D) late spring. Relative diet size The grazing pressure exerted by distributions are ex-pressed in (A,C) numbers and (B,D) biomass sandeels relative to total copepod grazing was estimated to be ρ1 = 0.697 (SD = 0.032) inside sandeel habitats, and ρ2 = 0.367 (SD = 0.031) for the study area as a whole (including the spaces between sandeel habitats). Assuming that sandeels are evenly distributed within sandeel habitats, copepod concentrations drifting over sandeel habitats with a large surface area or dense habitat clusters were effectively diluted (by grazing), and distinct local gradients in copepod concentrations appeared with a heterogeneity length scale of ~100 km (Fig. 7).

DISCUSSION

In the present study, we estimated the food consumption and energy conversion efficiency for lesser sandeels inhabiting the Dogger area in the North Sea. Based on this information, we demonstrated the ecological implications of (1) fluctuating proportions Fig. 5. Ammodytes marinus. Comparison of weight-specific of sandeels in the forage fish community, and (2) daily consumption (in proportions of body weight) estimated sandeel habitat patchiness. from stomach contents (R ) and bioenergetic calculations D Daily ration estimated from stomach data agreed (CW). Black symbols: geometric mean of RD (±SE) for each of 4 length groups and early spring (d) and late spring (m) sep- well with daily consumption estimated from bioener- s arately. Open symbols: CW in early spring ( ) and late spring getics, although during late spring, the stomach data n ( ). CW for Age 1 and Age 2 adults during early spring corre- gave values that were generally lower than values de- sponded to length groups 11−12 and 13−14 cm, and was rived from bioenergetics. The difference was particu- therefore placed accordingly on the graph. Likewise, Age 1 and Age 2 corresponded to length groups 12−13 and 14−15 cm larly pronounced in late spring, indicating that the during late spring fish length at the end of this period was under- 130 Mar Ecol Prog Ser 487: 123–133, 2013

Table 1. Ammodytes marinus. Parameter values used in the bioenergetic calcula- calculations provided estimates 2 to tions. Condition factor and length of fish at the beginning and end of the calcula- 4 times higher than methods based tion period (Kt1, Kt2, Lt1, and Lt2), the first and last day-of-the-year of the calculation period (t1 and t2), mean water temperature (T), and energy density of prey on stomach contents (Arrhenius & (ed). Values used when calculating the entire growth period, and values used Hansson 1994, Maes et al. 2005). when modeling the first half (early spring) and second half (late spring) sepa- The weight-specific consumption rately, are presented of 1.6 to 2.7% of body weight for adults was considerably lower than Input Age 0 Age 1 Age 2 reported for other forage fishes (i.e. parameter Entire Entire Early Late Entire Early Late clupeids). Biomass and production

Kt1 0.0021 0.0021 0.0021 0.00275 0.00195 0.00195 0.0027 estimates for pelagic planktivorous K t2 0.0029 0.0029 0.00275 0.0029 0.00285 0.0027 0.00285 fishes in the North Sea have sug- L 5 10.8 10.8 12.1 13.2 13.2 14.2 t1 gested a daily weight-specific con- Lt2 10.8 13.2 12.1 13.2 14.6 14.2 14.6 t1 150 80 80 123 80 80 123 sumption of 4% (Greenstreet et al. t2 250 165 123 165 165 123 165 1997). Average daily weight-specific T 14 10 8 12 10 8 12 consumption for adult Norwegian e 5150 5350 5550 5150 5350 5550 5150 d spring spawning herring during its growth period is roughly 7% (de- Table 2. Ammodytes marinus. Food consumption derived from the bioenergetic rived from values in Varpe et al. calculations. Total amount of energy consumed per individual during the calcula- 2005). Likewise, Age 0 herring tion period (CE), daily consumption relative to body mass (CW), population-level and sprat consume between 3.6 and consumption rate per surface area (C ), and energy conversion efficiency during P 11% of their body weight per day the growth period (CEgrowthperiod) and for the entire year (CEannual). (De Silva & Balbontin 1974, Arrhe- Measures of Early spring Late spring Summer nius 1998, Maes et al. 2005), a range consumption Age 1 Age 2 Age 1 Age 2 Age 0 (juvenile) which contains the value estimated here for juvenile sandeel (6.1%). C (J) 31080 49287 33119 33220 44964 E Relatively lower consumption rates, CW (in proportion of 0.027 0.024 0.022 0.016 0.061 body weight) in particular for adults, may relate to −2 −1 CP (g wet weight m d ) 0.89 0.23 1.02 0.17 1.31 the foraging strategy of sandeels, CEgrowthperiod (%) 56 54 40 32 47 which resembles that of a central CE (%) 22 18 16 11 25 annual place forager. Compared to migra- tory fish such as herring that can move to areas of high food concentration (Dragesund et al. 1997, Corten 2001), sandeels have a rather limited foraging range, as they are obliged to stay near suitable burying habitat. Both stomach data and bioenergetics showed that food consumption decreased from early to late spring, indicating that food limitation was more important in late spring/early summer, when copepods were smaller. In line with the present findings, Macer (1966) found the diet of lesser sandeels on Dogger Bank to Fig. 6. Inter-annual variation in (A) forage fish biomass in consist predominantly of copepods. Genus and spe- the North Sea separated into clupeids (black shading) and cies were not identified in the present study, yet the Ammodytes marinus (grey shading), and (B) energy conver- size distributions show a clear change in diet compo- sion efficiency (CE) calculated for the forage fish community sition from early to late spring. In early spring, cope- as a whole using either CEgrowthperiod (black line) or CEannual (grey line) pods smaller than 1 mm were absent, and size distribution peaked around 2 mm, suggesting a major estimated. This could be caused by size-selective bur- contribution from late Calanus stages. Calanus is the ial, where longer sandeels with a high condition factor only genus common to the North Sea that reaches an tended to enter the sediment earlier than smaller average length >1.5 mm (Pitois et al. 2009), and C. sandeels (Pedersen et al. 1999). However, the overes- finmarchicus tend to reach a maximum in abundance timation is considerably less than experienced in pre- earlier in the season than other common North Sea vious studies of forage fish, where the bioenergetic species (Fransz et al. 1991). van Deurs et al.: Ecological implications of sandeel strategy 131

Fig. 7. Ammodytes marinus. Simulation of grazing impact from patchily distributed sandeels in the Dogger area: (left) spatial heterogeneity in grazing impact depicted as copepod concentration relative to carrying capacity (c/c0) (averaged over the simulation period April 1 to July 1); (upper right) 2-dimensional cross-sections corresponding to lines A and B in the left-hand (color) graph; (lower right) grazing impact in a given grid cell as a function of relative sandeel habitat coverage within a radius of 45 km. Sandeel habitat is represented by 10 × 10 km square cells

During the growth period, lesser sandeels con- mented, although the general consensus is that the verted consumed secondary production to sandeel individual sandeel only leaves the sediment for a tissue with an energy conversion efficiency of ~50%, brief period to spawn, and that spawning migration resulting in an annual average of 20%. This finding behavior is absent. Hence, the energetic cost associ- is consistent with what has been found for other spe- ated with spawning activity is most likely small, and cies of sandeel: 38% for Ammodytes personatus in the sensitivity analysis showed that results changed growth experiments (Sun et al. 2010), and an annual only by 5% when daily activity in the model was efficiency of 20% for A. dubius based on comparable raised by 15%. bioenergetics calculations (Gilman 1994). These val- The high energy conversion efficiency of sandeels ues imply that sandeel is more energy-efficient than, was also evident at the system level, suggesting that for example, clupeids, where 17% has been reported the relative proportion of sandeels in the forage fish during the growth period for Norwegian spring- community has important implications for the eco - spawning herring using comparable methodology system. For example, during the period of reduced (Varpe et al. 2005), and 5 to 12% for North Sea her- sandeel biomass in 2003 to 2005, our calculations ring in growth experiments (De Silva & Balbontin indicated a reduction in the forage fish conversion 1974). The present study’s estimates of energy con- efficiency of 15 to 35% compared to the average version efficiency derived from bioenergetics can be level up until 2000. This result implies that the pro- considered accurate, or in the worst case, a slight duction available for higher trophic levels (i.e. birds underestimation, as stomach data resulted in lower and Atlantic cod) is reduced when clupeids dominate consumption rates than those found using bioener - the forage fish community, provided total forage fish getics. It should, however, be noted that the ex - consumption is bottom-up-controlled, as suggested cess metabolic cost of spawning activity was not by Frederiksen et al. (2006). accounted for when converting from growth period Population-level consumption rates of 1.2 g wet efficiency to annual efficiency. The behavior of lesser weight d−1 m−2 is close to the daily copepod pro- sandeels during spawning has never been docu- duction rate reported for the Dogger area in May 132 Mar Ecol Prog Ser 487: 123–133, 2013

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Editorial responsibility: Konstantinos Stergiou, Submitted: December 26, 2012; Accepted: April 29, 2013 Thessaloniki, Greece Proofs received from author(s): July 8, 2013