Reprint of: The ecophysiology of Sprattus sprattus in the Baltic and North Seas

Progress in Oceanography 107 (2012) 31–46

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Reprint of: The ecophysiology of Sprattus sprattus in the Baltic and North Seas q Myron A. Peck a,⇑, Hannes Baumann a,1, Matthias Bernreuther a,2, Catriona Clemmesen b, Jens-Peter Herrmann a, Holger Haslob b, Bastian Huwer c, Philipp Kanstinger a, Fritz W. Köster c, Christoph Petereit b, Axel Temming a, Rudi Voss b,3 a b c

Center for Earth System Research and Sustainability, Institute for Hydrobiology and Fisheries Science, University of Hamburg, Olbersweg 24, 22767 Hamburg, Germany IFM-GEOMAR, Leibniz-Institute for Marine Research at the University of Kiel, Düsternbrooker Weg 20, 24105 Kiel, Germany DTU Aqua, National Institute of Aquatic Resources, Technical University of Denmark, Charlottenlund Slot, Jægersborg Allé 1, 2920 Charlottenlund, Denmark

a r t i c l e

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Article history: Available online 2 November 2012

a b s t r a c t The European sprat (Sprattus sprattus) was a main target species of the German GLOBEC program that investigated the trophodynamic structure and function of the Baltic and North Seas under the influence of physical forcing. This review summarizes literature on the ecophysiology of sprat with an emphasis on describing how environmental factors influence the life-history strategy of this small pelagic fish. Ontogenetic changes in feeding and growth, and the impacts of abiotic and biotic factors on vital rates are discussed with particular emphasis on the role of temperature as a constraint to life-history scheduling of this species in the Baltic Sea. A combination of field and laboratory data suggests that optimal thermal windows for growth and survival change during early life and are wider for eggs (5–17 °C) than in young (8- to 12-mm) early feeding larvae (5–12 °C). As larvae become able to successfully capture larger prey, thermal windows expand to include warmer waters. For example, 12- to 16-mm larvae can grow well at 16 °C and larger, transitional-larvae and early juveniles display the highest rates of feeding and growth at 18–22 °C. Gaps in knowledge are identified including the need for additional laboratory studies on the physiology and behavior of larvae (studies that will be particularly critical for biophysical modeling activities) and research addressing the role of overwinter survival as a factor shaping phenology and setting limits on the productivity of this species in areas located at the northern limits of its latitudinal range (such as the Baltic Sea). Based on stage- and temperature-specific mortality and growth potential of early life stages, our analysis suggests that young-of-the year sprat would benefit from inhabiting warmer, near-shore environments rather than the deeper-water spawning grounds such as the Bornholm Basin (central Baltic Sea). Utilization of warmer, nearshore waters (or a general increase in Baltic Sea temperatures) is expected to accelerate growth rates but also enhance the possibility for density-dependent regulation of recruitment (e.g., top-down control of zooplankton resources) acting during the late-larval and juvenile stages, particularly when sprat stocks are at high levels. Ó 2012 Elsevier Ltd. All rights reserved.

1. Sprat and the German GLOBEC program DOI of original article: http://dx.doi.org/10.1016/j.pocean.2012.04.013 q

This article is a reprint of a previously published article. The article is reprinted here for the reader’s convenience and for the continuity of the special issue. For citation purposes, please use the original publication details: Progress in Oceanography 103 (2012) 42–57. ⁄⁄ DOI of original item: http://dx.doi.org/10.1016/ j.jat.2012.03.009 ⇑ Corresponding author. E-mail address: [email protected] (M.A. Peck). 1 Present address: School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USA. 2 Present address: Johann Heinrich von Thünen Institute, Federal Research Institute of Rural Areas, Forestry and Fisheries (vTI) – Institute for Sea Fisheries, Palmaille 9, 22767 Hamburg, Germany. 3 Present address: Sustainable Fishery, Department of Economics, University of Kiel, Wilhelm-Seelig Platz 1, 24118 Kiel, Germany. 0079-6611/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pocean.2012.10.009

The European sprat (Sprattus sprattus) was a main target species of the German GLOBEC program that investigated the trophodynamic structure and function of the Baltic and North Seas. Sprat was chosen as a research focus for three primary reasons. First, in some ecosystems sprat plays a prominent trophodynamic role by exerting both top-down control on zooplankton and being an abundant prey resource for piscivores (wasp-waist species, e.g. Cury et al., 2000). Second, decadal trends in the abundance of the Baltic sprat stock were part of a profound regime shift from an Atlantic cod (Gadus morhua) to a clupeid-dominated system that impacted almost all trophic levels (Alheit et al., 2005; Möllmann et al., 2009) and appeared to be tightly coupled to physical (climate) forcing. Third, the species is abundant within both the

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Baltic and North Seas. Examining sprat in both systems provided the opportunity to compare and contrast its role in different food webs and to determine if its life history strategy was flexible, allowing it to succeed in the vastly different conditions of physical forcing in the Baltic and North Sea ecosystems. Sprat is a small-bodied, pelagic schooling, zooplanktivorous clupeid that is distributed over a broad geographical range. In European waters it occurs from the Black and Mediterranean Seas in the south to the European Atlantic shelf, including the North and Baltic Seas (Muus and Nielsen, 1999). It tolerates a wide range of salinities and is abundant in estuarine habitats. It is considered an r-selected species (MacArthur and Wilson, 1967) because of its short lifespan, early reproduction, and low biomass. It rarely reaches an age >5 years (Bailey, 1980) or a length >16 cm (Whitehead, 1985). It is a multiple batch spawner, producing up to 10 egg batches throughout the spawning season in some areas (George and Alheit, 1987). Spawning occurs in both coastal and offshore waters (Whitehead, 1985) and the time of peak spawning, relative fecundity, and batch fecundity vary significantly between years and regions (Alheit et al., 1987). Adults are generally mature at 2 years though some individuals may spawn at 1 years (Bailey, 1980). Genetic differences exist among sprat populations in European waters (Debes et al., 2008; Limborg et al., 2009) and sub-species have been recognized. Previous studies on sprat identified temperature as a key factor affecting the population dynamics of this species at different latitudes. This is noted in both the scheduling of life-history events and inter-annual changes in the productivity of different sprat stocks. For example, in the North Sea, peak spawning occurs in the spring and early summer (Wahl and Alheit, 1988) while in southern European waters (e.g., Adriatic Sea), sprat general spawns during the winter months (October–April) with peak spawning in November/December at water temperatures between 9 and 14 °C (Dulcˆic´, 1998). MacKenzie and Köster (2004) examined recruitment strength at different water temperatures for the Baltic Sea and Black Sea stocks of sprat. Their inter-stock comparison suggested that recruitment was highest at intermediate water temperatures experienced during spawning (5.0 and 9.0 °C) but tended to be lower at colder (<3 °C) and warmer (P11 °C) waters (Fig. 1). Changes in a fitness trait (e.g., growth rate or fecundity) with an environmental factor often indicate changes in thermal optima among either (i) populations of a species inhabiting different latitudes, and/or (ii) life stages within a species. Both types of changes

Fig. 1. Water temperature at the time of spawning in relation to sprat (Spratus sprattus) recruitment in the Baltic Sea (squares, r2 adj = 0.28, p = 0.003) and Black Sea (circles, r2 adj = 0.35, p = 0.0002). A direct comparison of these two populations suggests a temperature ‘‘optimum’’ for recruitment at spawning temperatures between 5 and 9 °C. These data were digitized from MacKenzie and Köster (2004, their Fig. 2, p. 789). Black Sea data were compiled and analyzed by Daskalov (1999).

contribute to the scheduling of life-history events and define limits to the characteristics of suitable habitats. These are discussed for sprat in subsequent sections. This review summarizes available literature regarding the ecophysiology of sprat with an emphasis on progress made in the German GLOBEC program to understand how environmental factors influence the life-history strategy and vital rates of this species in the North and Baltic Seas. It compliments co-submissions on process-oriented and modeling studies conducted on this species (Hinrichsen et al., submitted for publication; Voss et al., submitted for publication) and on sprat prey-field dynamics (Schulz et al., submitted for publication). This review discusses available ecophysiological data, distinguishing among studies conducted on the earliest life stages (eggs, yolk sac and first-feeding larvae) and exogenously feeding life-stages (larvae, transitional larvae, juveniles and adults). The impacts of abiotic factors (particularly temperature) on rates of feeding, growth, and reproduction are reviewed to understand the physiological constraints that help shape the life-history strategy of this species in different regions. The focus is on physiological and life history attributes relevant for the ongoing development of biophysical, individual-based models of early life stages (e.g., Peck and Hufnagl, 2012) and models that attempt to close the life cycle (Rose et al., 2010). This review identifies gaps in knowledge to recommend areas requiring future research.

2. Endogenous and mixed-feeding period 2.1. Eggs and yolk sac larvae Sprat spawns pelagic eggs that are buoyant at different water depths in different systems due to salinity effects on ambient density. In marine waters such as the North and Mediterranean Seas, eggs remain in surface layers but in the Baltic, eggs sink below the low salinity (5–7 psu) surface waters through the thermocline to the halocline (6–15 psu) located at intermediate water depths of 30–60 m (Wieland and Zuzarte, 1991). Research on sprat eggs has focused on the impacts of water temperature and, to a lesser extent, salinity on development rate and survival. Oxygen also plays an important role for egg survival in the Baltic Sea but effects have not been examined in the laboratory. A number of studies have examined the survival and developmental rate of sprat eggs incubated at temperatures between 1 and 20 °C (Thompson et al., 1981; Nissling, 2004; Kanstinger, 2007; Petereit et al., 2008). Thompson et al. (1981) incubated sprat eggs between 4.5 and 20.0 °C and reported similar levels of survival between 4.5 and 18.0 °C but indicated that, due to relatively early developmental stage-at-hatch, larvae at >17 °C would likely not survive in the wild (Fig. 2a). Working with Baltic sprat eggs, Nissling (2004) reported relatively high (66–69%) viable hatch at temperatures between 5 and 13 °C but low percentage hatch at <3 °C (0.2–26%) (Fig. 2a). In these studies, standard length (SL)-at-hatch was 3.3–3.5 mm and relatively similar at all temperatures <17 °C as was the SL at yolk sac absorption (4.9–5.6-mm SL) (Alshut, 1988b; Kanstinger, 2007; Petereit et al., 2008). Several additional experiments have been conducted within the framework of GLOBEC Germany by Petereit (2008) on egg survival and developmental rate of eggs and yolk sac larvae that tend to confirm the results of previous studies. Petereit et al. (2008) incubated eggs at 1.8–16 °C and found the highest survival (percentage hatch) at 8 and 10 °C but, in contrast to other studies, no eggs survived when incubated at temperatures >14.7 °C. Similar incubation experiments performed on sprat eggs collected from the Adriatic Sea indicated high survival (83–100%) at 11 different temperatures between 5 and 19 °C (Petereit, 2008) which agrees with the results of previous

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effect of temperature on the window was due to starvation mortality occurring more rapidly at 3 °C (20 d) compared to 6 °C (23 d). At 14 °C mortality due to starvation occurred within 4 d (Petereit et al., 2008). Different populations of sprat may differ in the temperature-specific duration of this window. For example, the duration of this window is slightly longer at the same, intermediate temperatures in Baltic compared to Adriatic sprat (Petereit, 2008). The results of these various studies on eggs and yolk sac larvae suggest that temperatures between 7 and 13 °C support higher survival of endogenously feeding stages. Temperatures between 5–7 °C and 13–17 °C are sub-optimal and those in the ranges of 1–3 °C and 17–20 °C result in high mortality. Temperatures when spawning occurs have likely been set by these thermal boundaries. At constant temperatures between 5 and 13 °C, the combined data in four studies on eggs and yolk sac larvae (Thompson et al., 1981; Nissling, 2004; Kanstinger, 2007; Petereit et al., 2008) indicated that the duration of the endogenous feeding period is 135 ± 3 degree-days (°C d) after which the larva is 5.5 mm SL and must initiate feeding.

3. Exogenously feeding life-stages 3.1. Ontogenetic changes in morphology

Fig. 2. Effect of water temperature on eggs and yolk sac larvae of sprat (Spratus sprattus). Combined data from two studies measuring the percentage survival of sprat eggs incubated at different, constant temperatures (A). The function predicts little change in relative survival of eggs between 5 and 16 °C. Time required for eye pigmentation and death (after yolk sac absorption) of unfed larvae in relation to temperature (data from three separate studies) (B). The stippled area represents an estimate of the ‘‘window of opportunity’’ for successful first-feeding (between eye pigmentation and death).

studies conducted on sprat eggs from the southern North Sea and English Channel (Thompson et al., 1981). 2.2. First-feeding larvae One of the most important capabilities acquired during the early life of larvae is the successful transition to exogenous feeding. Depending upon water temperature, sprat eye pigmentation occurs between 3 and 16 d post-hatch (dph) and jaw development and mouth opening occur 48 and 72 h later (Nissling, 2004; Kanstinger, 2007). The ‘‘window of opportunity’’ for successful first-feeding can thus be defined as the duration of time between eye pigmentation/mouth opening and the exhaustion of yolk reserves or starvation mortality (Fig. 2b). A summary of measurements made in various studies on sprat yolk sac larvae suggests that the duration of time between these events can be 2–3 times longer at 8–10 °C (11 d) compared to lower and higher temperatures (e.g., 6 and 4 d at 4 and 14 °C, respectively). This non-linear

Different life-stages of fish can be identified by morphometic differences in relative body shape (Fuiman, 1983) and changes in the slope, b, of the mass and length relationship (DM = a  SLb), can denote important changes in morphology associated with life-history events (e.g., metamorphosis), changes in behavior (e.g., changes in swimming modes), and growth allocation strategies of energy acquired via feeding (Osse and van den Boogaart, 1995) relationship between dry mass (DM) and SL. Unique characteristics of developmental stages often are expressed in changes in the slope of the mass on length relationship. For example, in early life stages of fish, the slope (b) often differs (and is more variable) than that for large juveniles and adults (e.g., Pepin, 1995; Peck et al., 2005). The relationship between DM and SL for sprat has been reported in a number of studies (Shields, 1989; Coull et al., 1989; Safran, 1992; Peck et al., 2005). Peck et al. (2005) described changes in sprat morphology by employing a segmented regression having a slope of 5.0 for individuals of 5.5–44 mm SL but declining to 3.4 for larger sprat. These results agree well with (and explained the discrepancy between) slope values previously reported for 25–39 mm SL sprat (b = 5.6; Shields, 1989) and the slopes reported for larger YOY and adults (e.g. b = 2.83–3.47; Coull et al., 1989; Safran, 1992). Statistical models allowing for gradual rather than abrupt (segmented regression) changes in the slope might be biologically more relevant (Peck et al., 2005). Indeed, a re-analysis of those and additional morphometric data collected from the Baltic Sea indicated that the scaling of dry mass and length appears to change gradually (and non-linearly) with increasing body size (Fig. 3a). These changes in the slope (b-values) of the mass-length relationship coincide with important life-history events in sprat. For example, the most rapid allocation of energy to dry mass per unit length (highest b-value) occurs at body sizes between 14 to 18-mm SL (Fig. 3b). These sizes are most likely associated with the onset of schooling in this species. We infer this from indirect evidence, specifically that large numbers of 14-mm SL sprat were found within the guts of North Sea horse mackerel (Trachurus trachurus) (Matthias Bernreuther, personal observation). Within this range in standard lengths, there is a rapid expansion of the prey niche breadth (see Section 3.2) and protein-specific growth rates (see Section 3.4.1). The rapid increase in DM per unit SL during this period is likely due to rapid increases in the size (hypertrophy) and/or number (hyperplasia) of swimming muscle. It should be noted that dif-

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Fig. 3. Dry mass (DM) in relation to standard length (SL) for sprat (Spratus sprattus) larvae, juveniles, and adults, and changes in the allometric scaling of MD and SL with body size/life stage. Combined data set of MD and SL measurements made at different life stages were from Peck et al., 2004; Günther, 2008; J.-P. Herrmann, unpublished data (Panel A). Changes in the mean(±SE) slope (b) of the DM–SL relationship (DM = a  SLb) calculated for small ranges in lengths (shown as horizontal bars at each point) (Panel B). Fish length associated with schooling (i), late-larval to juvenile metamorphosis (ii) and juvenile to adult metamorphosis (iii) are als indicated.

ferences in the size and number of muscle fibers at different body sizes have not been examined in sprat and that swimming muscle development may also depend upon temperature based upon the findings for larvae of coregonid and other clupeid species (Vieira and Johnston, 1992; Hanel et al., 1996). A second change in b-values can be noted during the metamorphosis of transitional larvae into juveniles at 35–55-mm SL, after which point the adult body form is obtained. The slope was also relatively high (4.3) at body sizes of 60–80-mm SL, sizes obtained at the end of the first growing season when sprat at relatively high latitudes (Baltic Sea) begin building somatic energy reserves in preparation for overwintering (see Section 3.4.3). Finally, b-values for adults exhibit seasonal changes in relation to changes in energy partitioning and allocation to growth in either length, mass, lipid or protein (see Section 3.4.3). The allocation strategy in the Baltic Sea in response to the timing of overwintering, spawning, and intensive feeding periods is discussed more thoroughly below. In summary, based on changes in growth allocation between mass and length and inferences from field observations (predator gut contents), six life stages or life-history events can be identified that occur after the egg and yolk-sac larval phases. For Baltic Sea sprat, these include: (i) exogenously feeding but non-schooling lar-

vae from 5 to 14-mm SL, (ii) likely onset of schooling behavior from 14 to 18 mm-SL, (iii) a ‘‘transitional-larval’’ life stage from 18 to 35mm SL, (iv) a period of late-larval/juvenile metamorphosis occurring at 35–55 mm-SL, (v) a juvenile growth phase from 55 to 90 mm-SL, and (vi) adult fish that exhibit seasonal energy allocation to somatic and gonadal (reproductive) growth starting at 100 mm-SL. 3.2. Prey field, diet, and foraging Several field studies have examined the diets of larval sprat in the Baltic (Wosnitza, 1974; Grauman and Yula, 1989; Arrhenius, 1996; Voss et al., 2003; Dickmann et al., 2007) and other ecosystems (Voss et al., 2009). The percentage feeding incidence, based upon the numbers of larvae captured with food in their guts, was reported to be low in the smallest larvae but increased rapidly with increasing body size. Unfortunately, few laboratory studies have reared sprat beyond the yolk sac stage so observations under controlled conditions are rare. Kanstinger (2007) reared exogenously feeding sprat larvae at 7, 10 and 13 °C in the presence of a nanoflagellate (Rhodomonas baltica, 6–8 lm), a phagotrophic dinoflagellate (Oxyrrhis marina, 12–25 lm) and copepod nauplii (Acartia

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tonsa, 125–175 lm). Dinoflagellates were found in the guts of all larvae sampled at 8, 13, and 14 dph at 13, 10, and 7 °C, respectively, while copepod nauplii were observed in at least 25% of the guts 2– 4 d later (10, 16, and 18 dph at 13, 10, and 7 °C, respectively). These observations agree with the theoretical window of opportunity for first feeding (Fig. 3b). In situ collections often report unidentified microplankton in the guts of 5.5–10.5-mm sprat larvae (Voss et al., 2003; Dickmann et al., 2007). It is unknown whether the presence of microplankton in guts resulted from active foraging or passive ‘‘drinking’’ and whether (or how much) larvae benefit from consuming this potential food source (e.g., whether this prey is digested and assimilated). However, diet studies have revealed that the amount of microplankton in sprat guts varied seasonally in Baltic Sea (Bornholm Basin) and tended to be positively related to field estimates of survival (Voss et al., 2003; Dickmann et al., 2007). This suggests that microplankton may be necessary but not sufficient for high rates of survival of young larvae. These laboratory and field results for young sprat larvae agree with recent laboratory experiments indicating that incidental (or direct) feeding on protists can expand the window of first feeding in sprat (Kanstinger, unpublished data) and Baltic cod (G. morhua) (Overton et al., 2010). These findings for sprat agree with observations by Pepin and Dower (2007) on the trophic position of larvae of other marine fish species and diet studies of the larvae of seven species in the North Sea (de Figuiredo et al., 2007) which suggest that components of the microbial loop (algae and heterotrophic protists) can be important prey items. The increase in the variance in prey sizes consumed (increase in niche breadth) with increasing larval size is a common feature in some marine fish larvae (Pepin and Penney, 1997) and is clearly observed in the gut contents of larval sprat. As sprat larvae increase in size, prey size also increases and, based on an analysis of combined data reported in different studies on Baltic sprat (Voss et al., 2003; Dickmann et al., 2007), prey size increases most rapidly between 10 and 15 mm-SL (Fig. 4). At body sizes >15 mm-SL (including sizes of juveniles and adults not shown in Fig. 4), the maximum prey size changes relatively little (Last, 1987; Bernreuther, 2007). This initial increase in prey size (and increased variance that leads to increased prey niche breadth) with increasing sprat size appears to be an important feature involved in growth potential and patterns of growth with respect to temperature (discussed below). The GLOBEC field sampling confirmed the impor-

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tance of copepods (Acartia sp.) in the diet of sprat larvae in recent years (Voss et al., 2003; Dickmann et al., 2007). Seasonal comparison of prey fields suggested that cladocerans might be important for survival of sprat larvae in summer, when cladoceran abundance reaches its peak. Previous investigations, conducted during the early 1990s, indicated that Baltic sprat larvae performed diel vertical migrations (Voss et al., 2007). Interestingly, diel vertical migrations were not observed during the German-GLOBEC study period (2002–2005). More recent (2007) field sampling in the southeastern Baltic (55°N, 19.25°E) confirm these decadal differences, particularly for small larvae (Karaseva and Ivanovich, 2010). The lack of diel migration in recent years is hypothesized to be due to changes in the abundance of copepod species which have different depth preferences. Specifically, the abundances of Acartia and Temora species which prefer surface waters has increased whereas the abundance of Pseudocalanus which inhabits deeper depths has decreased (Voss et al., 2007; Schulz et al., submitted for publication). Biophysical modeling results of larval feeding and growth that included these decadal changes in prey fields and water temperatures suggested fitness benefits related to the change in larval foraging behavior (Hinrichsen et al., 2010a). This is an example of how larval fish behavior and life-history strategy adapt to changes in prevailing environmental conditions within an ecosystem. Regardless of the cause for the observed change in behavior, the lack of vertical migration observed during the GLOBEC field studies is not only expected to have consequences for survival but also profound influences on larval transport (Hinrichsen et al., 2005, submitted for publication). The diet of juvenile and adult sprat life stages has been well documented for a variety of ecosystems (e.g., De Silva, 1973; Arrhenius and Hansson, 1993; Last, 1987; Cardinale et al., 2002; MacKenzie and Köster, 2004). A number of studies have examined sprat diets in the Baltic Sea (Shvetsov et al., 1983; Szypula, 1985; Rudstam et al., 1992; Arrhenius, 1996; Szypula et al., 1997; Kornilovs et al., 2001; Casini et al., 2004; Möllmann et al., 2004) due to the important role of Baltic sprat and herring (Clupea harengus) in the topdown regulation of zooplankton (Möllmann and Köster, 2002; Casini et al., 2006). Studies have investigated daily feeding rhythms (Shvetsov et al., 1983) and compared diets among years and/or seasons (e.g., Szypula, 1985; Rudstam et al., 1992; Szypula et al., 1997; Kornilovs et al., 2001; Möllmann et al., 2004). The most recent study

Fig. 4. Sizes of prey items found in 1826 larval sprat (Spratus sprattus) guts in relation to larval standard length (mm). Data are for larvae collected in the Bornholm Basin, Baltic Sea and include those from Voss et al. (2003) and Dickmann et al. (2007).

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indicated that the copepods Temora longicornis, Pseudocalanus acuspes, and Acartia spp. along with the cladocerans Evadne nordmanni, Bosmina longispina maritima, and Podon spp were the most common prey in the guts of large juvenile and adult sprat (Bernreuther, 2007). In one study examining diel feeding patterns, sprat strongly selected T. longicornis during the day and mainly Podon spp. at night (Bernreuther, 2007). The reason for the diel shift in prey selection was unknown. Adult copepods and older copepodites (C4–5) were usually selected and younger (smaller) developmental stages avoided. However, at certain times of the day, smaller stages were positively selected. For example, Temora copepodites (c1–3) were positively selected between 19:30 and 01:30 (near and after sunset). During many German GLOBEC cruises in the Baltic Sea, copepod nauplii were often abundant in zooplankton samples but rarely encountered in stomachs of large juvenile and adult sprat (Bernreuther, 2007). Large juveniles and adults of many clupeid species including European sardine (Sardina pilchardus), European anchovy (Engraulis encrasicolus), Atlantic herring, and Atlantic menhaden (Brevoortia tyrannus) employ either filter or particulate feeding depending upon the size and concentration of prey items (Durbin and Durbin, 1975; Garrido et al., 2007). However, sprat is an obligate particulate feeder and its growth performance in nature might be strongly influenced by variability in the abundance of larger (optimal) sizes of prey (discussed below). The relatively fixed rate of prey ‘‘snatching’’ (rapid opening and closing of the mouth while swimming through a patch of zooplankton) by juvenile and adult sprat has implications for the outcome of intraspecific and inter-specific competition for food. Intra-specific competitive behavior (increased swimming speeds) was observed when sprat schools were provided limited prey resources (M.A. Peck, unpublished data) and evidence from field surveys of age0 juveniles (Baumann et al., 2007) and adults (J.-P. Herrmann, unpublished data) indicated that both life-stages may suffer from food limitation in the Baltic Sea. It is speculated that the negative impacts of prey limitation would be most severe for the largest adults that have similar maximum rates of prey snatching (J.P. Herrmann, personal observation), and maximum prey sizes, but have higher (absolute) daily energy requirements compared to smaller adults.

The importance of feeding mode to sprat may be most evident when inter-specific competition occurs with other small pelagic fishes and (potentially) invertebrate competitors such as the ctenophore Mnemiopsis leidyi which has become established in the Baltic Sea (Haslob et al., 2007). European anchovy, sardine, herring now co-occur with sprat in the North Sea. Gut content analyses of larvae of sprat and sardine that co-occurred in the German Bight indicated a high degree of diet overlap but spatial differences in the distribution of the two species minimized any potential competition for prey (Voss et al., 2009). However, competition of juvenile and adult stages may be more intense due to their increase feeding abilities. In these life stages, the ability to switch between filter- and particulate feeding modes and to utilize a wider range in prey sizes/types (e.g., see Raab et al., 2011) would appear to provide sardine, anchovy, and Atlantic herring a competitive advantage over sprat if these species experience poor feeding conditions, e.g. low zooplankton concentrations and/or prey fields characterized by relatively small zooplanktors). Furthermore, environmental ‘‘loopholes’’ in predation (Bakun and Broad, 2003) may become available to species that can utilize less productive environments that support small populations (low concentrations) of relatively large zooplankton. Such environmental loopholes would likely be unavailable to sprat due to its inflexible feeding mode. 3.3. Rates of food consumption and temperature 3.3.1. Larval feeding When fish encounter high prey concentrations, daily rates of feeding are, to a large extent, determined by the rate of gut evacuation, gut volume, and availability of sufficient light for visual foraging. Gut evacuation rates can be qualitatively assessed for larval sprat based upon the progressive decrease with time in gut contents of larvae sampled at the end of the day and at night. This ‘‘diel method’’ was applied to larval sprat sampled during three cruises between late May and July 2003 in the Bornholm Basin, Baltic Sea (Dickmann et al., 2007). Sprat gut content data were pooled by 10-min time bins and feeding incidence (FI, number of fish with prey/total number of fish analyzed) and estimates of the mean dry mass of food in each gut (lg, converted from counts and prey length measurements) were examined in relation to the time of

Fig. 5. Mean dry mass of gut contents (GC, lg) and feeding incidence (FI, %) in relation to time of the day for 13- to 16-mm standard length sprat (Sprattus sprattus) larvae captured during three cruises between late May and July 2003 in the Bornholm Basin, Baltic Sea. Groups of larvae were pooled across cruises within 10-mm bins to generate this figure (the number of larvae in each size bin is indicated at the top of the figure). FI = number of fish with prey (total number of fish analyzed)1. GC was calculated from prey lengths based upon prey species- and length-specific dry mass conversion factors. The times of sunrise (SR), sunset (SS) and civil twilight (CT) are indicated below the abscissa. The mean(±SE) slopes of the decrease in FI and GC (GC normalized to highest value) in relation to time were described by a slopes of 0.27(0.01) and 0.46(0.08), respectively (n = 4, p < 0.01). Details regarding larval sprat sampling were provided by Dickmann et al. (2007).

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T15 C MAX ¼ 1:315  DM0:83  2:872½ 10 

where T = water temperature (applied between 10 and 20 °C) and DM = larval dry mass (lg). At temperatures of 12 and 15 °C, CMAX of a 200-lg DM sprat larva is predicted to be between 39% and 53% larval DM d1. The aforementioned in situ estimates of gut contents and (non-feeding) evacuation rates correspond to feeding rates of 20% larval DM d1 during a 15-h photoperiod. In young larvae, evacuation rates often increase 2-fold during feeding suggesting that modeled and in situ estimates of larval sprat food consumption rate agree (40–45% DM d1). Comparisons of rates of feeding by larvae of different marine fish species are difficult because these rates are difficult to estimate and estimates vary widely among species (Houde and Schekter, 1983; Peck and Daewel, 2007). Houde and Zastrow (1993) reported a general, inter-specific relationship describing the effect of temperature (T) on the rate of food consumption (C, d1) by larvae (C = 0.0299T + 0.0389, see their Table 7) yielding food consumption rates between 40% and 49% DM d1 for larvae at 12 and 15 °C.

Fig. 6. Transitional larval and early juvenile sprat (Sprattus sprattus) growth rate versus food consumption rate in the laboratory at 14, 18 and 22 °C. Fish were fed brine shrimp (Artemia sp.) nauplii for 10–12 d at each temperature. Regressions are shown for growth rate (GR, % fish dry mass d1) versus food consumption (C, % fish dry mass d1). Values for maintenance food consumption rates (CMAIN, C where GR = 0) are also provided. See Peck et al. (2004) for details.

capture. Diel differences in feeding by sprat (n = 124, 13–16-mm SL) were evident (Fig. 5). The number of larvae with food in the guts was lower at dawn and dusk and no larvae had a gut with food in the early morning and late in the day. The increase in both FI and gut content was variable during daylight hours. The former displayed two (crepuscular) peaks whereas the latter generally reached maximum values in the late afternoon in agreement with the findings of Voss et al. (2003). At the end of the day, gut content declined at a rate of 0.46(0.08) (mean (±SE)) h1, an estimate suggesting that 13–16-mm SL sprat can empty their guts within about 1.75–3.5 h (evacuation rates on the order of 40–50% h1) during non-feeding periods with maximum mean dry mass of gut contents of 2.5% of larval dry mass (5 lg in a 200 lg DM larva, Fig. 5). These values agree with those measured in the larvae of a variety of different marine fish species (Peck and Daewel, 2007) and are particularly close to values obtained for herring larvae (e.g., Pedersen, 1984; Pepin and Penney, 2000). It should be noted that gut evacuation rates depend upon water temperature. Care must be taken when interpreting these field data since the larvae of sprat are susceptible to damage when captured using standard sampling procedures (e.g., see Dänhardt and Temming, 2008) which might bias estimates if the degree of damage (or the occurrence of stress-related gut evacuation) was related to tow duration or environmental conditions. Estimates of feeding rates by sprat larvae are also available from mechanistic individual-based models (IBM’s) that include foraging and growth subroutines (Peck and Daewel, 2007; Daewel et al., 2008; Kühn et al., 2008). These IBM-based estimates of food consumption rate are derived from a balanced bioenergetics budget (including metabolic costs, assimilation efficiency of food, and other parameters) and otolith-based temperature-specific somatic growth rates of sprat larvae (discussed below). To balance observed growth rates, the maximum food consumption rate (CMAX, lg prey d1) needed to change with body size and temperature according to:

3.3.2. Feeding rates in transitional-larvae and young juveniles Transitional-larval and juvenile sprat were found to be relatively amenable to laboratory work since they frequently occur in dense schools in shallow coastal waters and are little affected by capture and transport to the laboratory. Direct measurements of food consumption and growth have been made for 30 to 45mm SL transitional-larval sprat in the laboratory (Peck et al., 2004). When tested at 14, 18, and 22 °C, the highest rates of food consumption were observed at 18 °C. At this temperature, food consumption rates were between 36% and 44% fish DM d1 (Fig. 6). At 22 and 14 °C, maximum feeding rates were 30% and 8% DM d1, respectively. When groups of larval sprat at 18 °C were starved for 12 d and re-fed for an additional 12 d, no increased rates of feeding were observed in terms of the absolute number of zooplankton consumed indicating that 45% DM d1 appears to be a good approximation of an upper limit (CMAX) for transitional larvae and young juveniles of this species feeding during the summer in the Baltic Sea. The CMAX by sprat (mean 50-mg DM) is essentially the same as that (50% DM d1) found for a variety of fishes at that same body size and water temperatures (e.g., Keckeis and Schiemer, 1992, see their Fig. 7). 3.3.3. Feeding rates in juvenile and adult sprat Feeding rates by large juvenile sprat (50–80-mm SL) have been estimated in laboratory experiments examining gut fullness and gut evacuation rates. Using this method, rates of feeding have exceeded 1.2% DM h1 (Bernreuther et al., 2009) or 16% DM d1 when using a 15-h feeding period. When feeding on live zooplankton (brine shrimp, Artemia sp., nauplii) in the laboratory, the mean wet weight of gut contents of large juvenile sprat could be up to 8% fish wet mass (WM) (J.P. Herrmann, personal observation). In contrast, estimates of gut content mass have not exceeded 1.7% sprat WM (Arrhenius, 1998). Typically, gut contents vary between 0.1% and 0.4% WM in Baltic Sea sprat (Bernreuther, 2007). In other systems (e.g., Scottish west coast, Black Sea), the maximum gut content weight in juvenile sprat appears to be between 0.4% and 2.8% wet body mass for this species (De Silva, 1973; Sirotenko and Sorokalit, 1979). Based upon a balanced bioenergetics budget and known growth rates calculated from changes in the energy content of age-0 juveniles captured monthly in the Bornholm Basin, estimates of maximum feeding rates were 3.26% WM d1 (12% MD d1) in June (Bernreuther, 2007). Hence, there is a large discrepancy between observed gut contents, calculated feeding rates, and estimates of energy input needed for observed growth for sprat in the Bornholm Basin. The discrepancy could be explained by seasonal shifts in sprat feeding grounds from the deeper

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Fig. 7. Sprat (Sprattus sprattus) standard length (SL, mm) in relation to otolith ring count for larvae collected in six different field studies and SL in relation to larval age (days) reported in two laboratory studies. Three separate field studies collected larvae in the North Sea and one study collected larvae from the Baltic Sea. The back-calculated lengths of sprat juveniles from the Baltic Sea are also shown for comparison. Regression equations for North and Baltic Sea larval data: circles, SL = 0.466  ORC + 5.79, r2 = 0.849; triangles, SL = 0.405  ORC + 7.79, r2 = 0.895; squares, SL = 0.444  ORC + 6.38, r2 = 0.880; diamonds = 0.4414  ORC + 6.311, r2 = 0.749). In all cases, regressions were significant (p < 0.05). Unlike field data, laboratory data include known ages of fish and include growth during and for 2 weeks after the yolk sac period at 14–15 °C.

basins to near-shore (shallower) waters. In that case, observed growth rates would be calculated for fish that returned to the Bornholm Basin after feeding in another (more productive) region that was outside of the GLOBEC sampling area. Alternatively (or, in parallel), in situ feeding rates may be underestimated if fish evacuate some of their gut content as a stress response during capture. 3.4. Growth rates and temperature A number of approaches have been used within the German GLOBEC program to measure growth or growth potential of transitional larvae, juveniles, and adult sprat in the Baltic and North Seas. For example, otolith increment widths have been measured in young-of-the-year juveniles captured in autumn surveys in the Baltic (Baumann et al., 2006a,b, 2008) and North Seas (Baumann et al., 2009). Direct measurements of growth are available from controlled laboratory studies performed on 25–45-mm SL transitional- (late-) larval sprat (Peck et al., 2004) and 55–70-mm SL juveniles (J.-P. Herrmann, unpublished data). Growth rates of larger juveniles and adults have been estimated from changes in dry mass and length of fish captured in monthly cruises in the Baltic (J.-P. Herrmann, unpublished data). These studies combined with the research discussed here on early life-stages (eggs and larvae), provide an opportunity to assess the ontogeny of temperature-dependent growth in sprat. 3.4.1. Growth rates of larvae Most studies that investigate growth rates of marine fish focus on mean growth rates of groups within cohorts, despite the fact that processes act upon the individual. An important distinction should

be made between mean growth rates (e.g., those obtained for cohorts of larvae) and growth rates of individuals (e.g., larvae within those cohorts). Naturally, the former may be biased due to the selective loss of either slow-growing individuals (e.g., due to natural mortality) or fast-growing individuals (e.g., gear avoidance by relatively large larvae) and/or due to the mixing of cohorts having different mean ages. For larval sprat, growth rates of individuals are available from measurements of otolith increment widths and RNA-DNA ratios (Lee et al., 2006; Peck et al., 2007; Huwer, 2004; Hinrichsen et al., 2010b). These growth rates often reflect a high degree of growth variability among individual sprat larvae captured at the same time from the same station (e.g. coefficient of variation of growth rates often >40%, Peck et al., 2007). With only a few exceptions (e.g., Voss et al., 2006; Hinrichsen et al., 2010b), inter-individual growth variability has been ignored in most process-oriented field studies examining sprat growth rates. Therefore, for purposes of comparison we report mean growth rates of groups in all subsequent sections. The vast majority of sprat growth data come from field studies because it has proven difficult to rear larval sprat in the laboratory (e.g., Alshut, 1988b; Shields, 1989; Kanstinger, 2007). The few estimates of growth rate for laboratory-reared larval sprat tend to be lower than those from field studies (e.g., Fig. 7) even when compared to growth rates of relatively small field-caught larvae in which issues of gear avoidance can be ignored. Mean growth rates of larval sprat have been determined from otolith and biochemical (RNA-DNA ratios) methods applied to individuals captured in the Baltic, North, Irish, and Adriatic Seas (Munk, 1993; Rè and Gonçalves, 1993; Dulcˆic´, 1998; Valenzuela and Vargas, 2002; Huwer, 2004; Holtappels, 2004; Lee et al., 2006; Voss et al., 2006; Daenhardt et al., 2007). Most estimates of growth rates

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Fig. 8. Larval sprat (Sprattus sprattus) biochemical-based protein-specific growth rate in relation to water temperature at the time and location of field collection. Rates are shown for relatively small (8- to 12-mm standard length, SL) and large (12- to 16-mm SL) larvae. Boxes display the upper and lower 25th and 75th percentiles, whiskers denote the 10th and 90th, circles represent measurements outside those ranges, and the thick line represents the mean value. Larvae were collected during five cruises in the Bornholm Basin in late March to early July 2002. Multinet gear sampled larvae in discrete depths and temperature corresponds to the depth of capture. Symbols showing measurements for 8- to 12-mm SL larvae between 10 and 16 °C were shifted slightly so that they did not overlap with those for 12- to 16-mm SL larvae.

are for larvae <20 mm SL. There are indications from these studies that growth-temperature relationships vary with larval size. For example, biochemical-based growth rates for 8–12-mm SL larvae in the Baltic Sea (Bornholm Basin, late March to early July 2002) declined at temperatures >9 °C (Fig. 8). In contrast, no decline in protein-specific growth rates (or RNA-DNA ratios) was observed for larger (12- to 16-mm SL) larvae at temperatures up to 16 °C. Although we cannot separate the impacts of temperature from prey level in field studies of larval growth, our biochemical measurements were made for sprat larvae from both size classes captured in multiple time periods which further supports our conclusion that these differences in growth potential between size classes at various temperatures reflect ontogenetic changes in foraging efficiency. It may also correspond to ontogenetic changes in metabolism which have not yet been measured. Due to increases in mouth gape and swimming ability, larger sprat larvae can consume larger prey, and this increase in the spectrum of available prey sizes would help support growth at higher temperatures. Smaller larvae would require a better ‘‘match’’ with prey (due to a smaller range in suitable prey sizes) to successfully forage and grow. Moreover, smaller fish larvae are poorer swimmers and have higher mass-specific metabolic costs at the same temperature compared to larger larvae. Variation in growth due to temperature and stage (size) observed in larval sprat may be indicative of more general, inter-specific trends since maximum prey size and mass-specific metabolic costs (e.g., routine respiration rates) generally increase and decrease, respectively, with increasing body size (Houde, 1989). A general expectation would be that larger and older larvae can exploit warmer habitats than smaller and younger larvae. Indeed, young juveniles in many species often display the widest thermal tolerances (Pörtner and Peck, 2010). Otolith-based estimates of growth of North Sea sprat (ages 1– 30 d post first-feeding) varied from 0.40 to 0.46 mm d1 (Munk, 1993; Rè and Gonçalves, 1993; Huwer, 2004) and are similar to those (0.44 mm d1) of Baltic sprat larvae (Hinrichsen et al., 2010a) (Fig. 7). Although many field studies have reported otolith-based mean growth rates for larval sprat cohorts, only Munk (1993) could detect significant differences in growth rates in relation to hydrographic features (i.e. collection station position in relation to a frontal zone in the North Sea). Only Munk (1993) employed gear that caught larger sprat larvae and the association of growth

rates with frontal locations was only expressed in large larvae (>15 mm SL). 3.4.2. Growth rates of transitional larvae and juveniles In field-caught transitional-larval and juvenile sprat, the optimal temperature for growth can be inferred from the widths of otolith increments deposited during the first month after first feeding. These otolith studies have examined temperature and growth

Fig. 9. Growth proxies (otolith increment widths, Panel A; RNA-DNA ratio, Panel B) of 30- to 50-mm SL sprat in relation to water temperature from laboratory trials. In ‘‘CMAX Trials’’, groups of sprat were maintained using ad libitum food rations for 5 d prior to measurements of growth proxies at each of the five temperatures. Mean values for 5–15 fish are shown. Two data points at 18 °C are mean values for similar-sized sprat maintained at ad libitum feeding conditions in 10-d ‘‘Growth Trials’’ (see Fig. 6) and were not used to fit the regression lines. See Peck et al. (2004) for details.

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prior to and during the phase of transition between larval and latelarval stages. The influence of temperature (T) on mean larval sprat growth rate (GL, mm d1) during the first 30 d post-feeding estimated from otolith-based growth rates from 0-group juveniles (Bornholm Basin, 2002 and 2003) and mean temperatures from a hydrodynamic model (Baumann et al., 2008) is described well by:

GL ¼ 0:23  T  0:005  T 2  1:69 ðr 2 ¼ 0:90;

n ¼ 22;

p

< 0:001Þ: Growth rates were estimated to be 0.5 and 0.9 mm d1 for fish in June and July at temperatures of 13–20.5 °C. The relationship implies Q10 values of 3.8 and 1.6 for changes in growth rates between temperatures of 13–17 °C and 17–21 °C, respectively, and (by extrapolation) a temperature optimum at 22 °C. Also using otoliths, Günther (2008) reported an exponential increase in growth rates of transitional-larval and young juvenile sprat captured at water temperatures between 10 and 22 °C in nearshore areas of the western Baltic Sea. Again, estimates of temperature-dependent growth in wild fish are confounded because feeding history is unknown. When transitional-larval and early juvenile sprat were provided ad libitum rations of live zooplankton (Artemia nauplii) in shortterm (4–5 d) laboratory feeding trials at 7, 11, 15, 18, and 22 °C, otolith increment widths and nucleic acids (RNA-DNA ratios) tended to reach their highest values between 18 and 22 °C (Fig. 9A and B) (Peck et al., 2004). These increases were most rapid between 10 and 15 °C and suggest that growth rates may not increase at temperatures >22 °C. This pattern of growth stabilization (or decline) at temperatures >22 °C agrees with the otolith growth histories of late stage-larvae and early transitional larvae. The estimates from biochemical and otolith methods from short-term feeding trials also agree well with the results of longer-term (12–14 d) feedinggrowth trials. During those trials, maximum specific growth rates of transitional larvae were 2.5%, 11.5% and 7.5% DM d1 at 15, 18 and 22 °C (see Fig. 6). In somewhat larger juveniles, the physiological underpinning of the growth-temperature relationship has been examined by measuring rates of energy loss and energy gain at different temperatures. A strong dependence of feeding rates on temperature was apparent from gastric evacuation experiments performed on groups of juvenile (mean 63-mm TL, 283-mg DM) sprat fed Artemia sp. nauplii (Bernreuther et al., 2009). The rate of decrease in gut contents changed with temperature in a non-linear manner. With increasing temperature, the rate increased exponentially between 10 and 15 °C, increased more slowly starting at approximately 16 °C, and reached a maximum at 20 °C (Fig. 10A). The temperature-dependent change in gut evacuation rates of 55-mm SL juveniles agrees well with the temperature-dependent changes in ingestion rates determined for smaller sprat transitional larvae (relatively low CMAX at 14 and 22 °C compared to 18 °C, described previously). Rates of energy loss, measured via rates of O2 consumption by Meskendahl et al. (2010), appear to increase exponentially with increasing water temperature between 4 and 21 °C (Fig. 10B). Thus, the scope for growth (Brett, 1979) would appear to be relatively low at temperatures <10 °C and >22 °C, and maximal between 18 °C and 20 °C in young juvenile sprat. 3.4.3. Spawning and growth of adults Similar to many other clupeiform species, sprat is an indeterminate batch spawner that releases eggs over a prolonged period. Intra- and interannual variability is expected in spawning season length, batch fecundity, and batch frequency in all regions (Heidrich, 1925; Alheit, 1988; Alshut, 1988a). Based upon the timing of spawning at different latitudes, spawning occurs between 6 and 15 °C. In northern European waters (North and Baltic Seas), peak spawning

Fig. 10. Rates of gut evacuation (A) and standard respiration (B) in relation to temperature for juvenile (55–70 mm standard length) sprat in the laboratory. Data in Panel A and B were from Bernreuther et al. (2009) and Meskendahl et al. (2010), respectively.

occurs between May and August (Petrova, 1960; Wahl and Alheit, 1988) when water temperatures are commonly between 8 and 15 °C. In southern European waters (Adriatic Sea), sprat general spawns during the cooler time of the year (October–April) with peak spawning in winter (November to December) at water temperatures between 9 and 14 °C (Dulcˆic´, 1998). In all regions, however, the onset and duration of spawning may vary due to temperature and feeding conditions. Recent observations in the Baltic detected spawning females as early as January (Haslob, 2011) and a second spawning peak observed in autumn 2003 was related to exceptional warm water masses during summer in the Bornholm Basin (Kraus et al., 2004). The batch fecundity (BF) of Baltic sprat was estimated via the hydrated oocyte method by Haslob et al. (2011). Those results indicated BF differed significantly among years and areas. For sprat in the Bornholm Basin, BF increased linearly with increasing TL according to: BF = 413  TL  3510 (r2 = 0.43, n = 774, p < 0.05). Mean(±SE) size-specific BF varied from 86.0(±6.5) to 149(±4.5) eggs (g ovary-free WM)1 for female sprat in the Bornholm Basin (Haslob et al., 2011) which is lower than sprat BF for the southern North Sea (413) and the Kiel Bight (232) (Alheit, 1988). Differences in BF are likely driven by differences in environmental conditions (e.g., Petrova, 1960). In the case of Bornholm sprat, Haslob (2011) reported that absolute BF was positively related with water temperature (T, °C) during the pre-spawning period and fish size (TL, cm) according to:

0  0:5@

ln

1:46ð0:55Þ

BF ¼ 359:5ð23:5Þ  TL  e 2

ðr ¼ 0:70;

n ¼ 179;

12

T 6:97ð2:50Þ

A  2753:2ð243:5Þ

p < 0:05Þ

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Fig. 11. Phenology of growth of sprat (Sprattus sprattus) in the Bornholm Basin (Baltic Sea). Measurements include dry mass (A) total protein content (Panel B) and total lipid content (C) for each of seven sprat year classes (1997–2003). Basin-wide mean values are shown for each cohort on each date. Three periods within each year are recognized (different shades of gray): spawning phase, summer somatic growth phase, and an over-wintering phase. During the summer, growth is initially allocated to increase protein content (and length, not shown) and, subsequently, to a rapid increase in lipid to prepare individuals for over-wintering and gonadal maturation.

where mean(±SE) parameter estimates are provided. During peak spawning, egg batches appeared to be released approximately every 4 d (Haslob, 2011, spawning frequency estimated by macroscopic inspection of hydrated ovaries). These estimates agree well with previous studies (Alekseev and Alekseeva, 2005; Kraus and Köster, 2004). In terms of seasonal growth patterns, the physiological studies conducted on juveniles agree well with growth rates determined from repeated sampling of juvenile and adult sprat in the Bornholm Basin of the Baltic Sea between February 2002 and May 2004 (J.-P. Herrmann, unpublished data). Measurements of SL, DM, proximate composition (amounts of protein, lipid and energy), and counts of otolith annuli revealed a more complete picture of the seasonal growth and energy allocation strategy of sprat in the Bornholm Basin (Fig. 11A). For the different cohorts assessed (age classes), the seasonal allocation of energy to somatic and gonadal growth depends, to a large extent, upon the timing of spawning, the timing and availability of prey resources and physiological limitations imposed by seasonal changes in water temperature. The seasonal changes in SL and DM (Fig. 11A) depict the life-history strategy and growth dynamics of sprat in the Baltic, near the northern extreme of sprat’s geographical distribution. First, immature stages of two cohorts (2002 and 2003) are first captured in summer or autumn which decrease in body size during their first autumn and winter from 1.75 to 1.0 g DM. Inter-annual differences in the growth of immature fish are also apparent. The 2001 year class had small body sizes when first sampled (at age 1) in April 2002. That 2001 year class likely matured at 2-year-olds. In spawning fish, the lowest DM was reached by approximately June of each year (2002, 2003 and 2004) which marks the end of the main reproductive season. This is followed by a rapid but ephemeral increase in DM by all year classes except the oldest (e.g., 6 year-old fish in 2003) which are lost from samples at that time. The rapid increase in DM during the late spring and early

summer is due mostly to increases in somatic protein content (Fig. 11B). This rapid increase in protein ended in mid to late summer but DM continued to increase due to rapid deposition of lipid reserves later in summer (Fig. 11C). These lipid reserves are critical since, to a large extent, they fulfil the energy requirements of this species during the overwinter period (when prey are scarce at this latitude) and also fuel maturation and the onset of spawning activity. The utilization of energy reserves is depicted by the decrease in DM observed throughout the overwintering and spawning periods. Feeding by sprat in the spring may help to extend the spawning period by replenishing depleted energy reserves but this has not been directly examined. Examples of this type of detailed seasonal growth data are available for a variety of marine fish species (e.g., Dygert, 1990; Smith and Paul, 1990; Jorgensen et al., 1997) but are uncommon for clupeids. Unfortunately, no comparable data exist on the seasonal growth dynamics of sprat at lower latitudes where annual growth patterns would likely be different due to differences in the phenology of prey resources and severity of the overwintering period (see Conover, 1992). A recommendation stemming from the results of field studies conducted in the German-GLOBEC program would be to compare seasonal growth dynamics of sprat in the Baltic to those of conspecifics at lower latitudes. This would provide a more complete understanding of how abiotic and biotic factors interact to control ‘‘life-history scheduling’’ in this species. 4. Temperature-dependent life-history strategy in the Baltic Sea This summary of knowledge on life stage- and temperaturespecific growth patterns enables a more thorough understanding of the constraints placed on ‘‘life-cycle scheduling’’ of sprat, especially in the Baltic Sea. Based on laboratory and field studies, there appears to be ontogenetic changes in the range of temperatures that support growth with transitional-larval and early juvenile

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Fig. 12. Temperature-specific growth potential and life history scheduling of sprat (Sprattus sprattus) in the Baltic Sea. Relative impact of different water temperatures on the vital rates (rates of survival, feeding, and growth) of various life stages (Panel A). This conceptual diagram is based upon multiple field and laboratory studies discussed elsewhere in the text. The phenology and scheduling of various life history events for sprat in the Bornholm Basin (Panel B) was based upon mean, depth-specific water temperatures for 2002 and 2003 (shown at the bottom). The first appearance of eggs, larvae, transitional larvae and juveniles is constrained by the availability of tolerable (warm) surface water temperatures (and the development rate of earlier life stages). The time period of final appearance of these life stages is constrained by temperaturedependent growth potential and size thresholds observed prior to overwintering that are potentially required for overwinter survival. Note, surface water temperatures are too warm for eggs and young larvae during the summer but cooler, optimal temperatures occur at depth. The phenology of spawning and protein and lipid growth (gray bars) are based upon from field measurements (see Fig. 11).

stages able to exploit warmer temperatures than eggs, larvae or adults (Fig. 12a). Theory suggests that young juveniles may be able to exploit (grow well in) a larger range in temperatures compared to either earlier (eggs/larvae) or later (mature adult) life stages (Pörtner and Farrell, 2008; Rijnsdorp et al., 2009; Pörtner and Peck, 2010) and our summary for sprat supports this theory. In other temperate marine fish species such as Atlantic cod (G. morhua) and sole (Solea solea), ontogenetic expansion and contraction of tolerable thermal environments have been reported for juveniles and spawning adult phases, respectively, and stem from increases and decreases in aerobic performance capacity (Pörtner and Peck, 2010). There are three, main temperature-dependent constraints that impact the scheduling of life-history events for Baltic sprat: survival of eggs, success of YOY overwintering and energy partitioning and gonadal maturation of adults (Fig. 12b). Successful spawning (spawning that produces viable offspring) would not occur until waters are P5 °C due to low survival of eggs incubated at colder temperatures. Interestingly, temperatures <5 °C are actively

avoided by large juvenile and adult sprat (Stepputtis, 2006). Temperatures supporting successful development of early life stages of sprat occur (at depth) for much of the year (April–November) but the end of the spawning season is constrained by the time required by offspring to reach (juvenile) body sizes that can successfully overwinter. Young-of-the-year overwintering mortality, a common growth constraint in populations of freshwater and marine fish inhabiting temperate latitudes (Schultz et al., 1998; Gotceitas et al., 1999; Höök et al., 2007), has not been examined in sprat but size requirements for successful overwintering can be inferred from in situ observations. Specifically, sprat consistently obtained a mean size of P75 mm SL at the end of the first growing season during time periods when Baltic sprat year class recruitment indices where quite high (ICES, 2009). The mean SL of YOY sprat captured in November in 2002, 2003, 2005, and 2006 was 79.3, 78.5, 81.7 and 73.7 mm, respectively (J.-P. Herrmann, unpublished data). Otolith-based growth histories of survivors (age-0 juveniles) caught in November 2002 (data from H. Baumann) indicated that about 100 d (mean ± range of 98 ± 7 d) were needed for growth

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from 12.0 mm to 75 mm SL in that year. Given average water temperatures in the Bornholm Basin and based upon estimates of the development and growth rates of earlier life stages (see earlier sections on eggs and yolk sac larvae), sprat would require 120– 140 d after fertilization to obtain this pre-winter size. Pre-recruits would not be able to reach this pre-winter size if spawning took place after mid-July (see Fig. 12). The lack of eggs in surveys conducted in mid-July supports this sprat life-history constraint in the Bornholm Basin of the Baltic Sea (R. Voss, personal observation). A combined analysis of otolith-based growth trajectories and hydrodynamic modeling (providing likely temperatures experienced) predicted that young-of-the year sprat always benefited from relatively warm temperatures in the Bornholm Basin (Baumann et al., 2008). However, optimal temperatures predicted for growth in transitional-larval and juvenile sprat (20–22 °C) occur for only a short time period (e.g., 2 weeks in late July, 2003, see Fig. 12b) within the Bornholm Basin, one of the main spawning grounds. From a physiological perspective, shallow inshore waters that warm more than offshore areas would be more optimal areas for rapid growth of transitional larvae and young juvenile sprat, provided that these areas have ample prey fields to support growth, which may not always be the case (see Baumann et al., 2007). Finally, a certain amount of time is required for post-spawning adults to forage and partition energy to somatic growth. Work is in progress to develop energy partitioning rules (e.g., what food energy is allocated to gonadal versus somatic growth) to model life-history growth strategies (K. Andersen, DTU Aqua, personal communication). Differences exist between life-history attributes of North Sea and Baltic Sea sprat that do not appear to be driven by physiological differences between these populations. In fact, most facets of the physiology appear similar between the Baltic and North Sea populations (development rates of endogenously feeding life stages, growth rates of young larvae, etc.). Although a recent analysis utilizing nine microsatellite markers uncovered genetic differences between these populations (Limborg et al., 2009), we postulate that differences in life-history scheduling only reflect differences in seasonality in water temperature and prey production. In the North Sea, the sprat spawning season extends later in the summer (sometimes through August) and, at the end of their first growing season, sprat are 10–12 mm (20%) smaller than their Baltic conspecifics. We speculate that the severity of overwintering conditions is an important factor regulating life-history scheduling in northern populations of sprat. A larger pre-winter size may be required in the Baltic Sea compared to the North Sea due to the harsher environment experienced during the winter (and perhaps due to the lower salinities) in the former system. However, overwintering zooplankton populations, potential feeding and sizespecific survival have not been assessed in either the North Sea or Baltic Sea. This lack of knowledge on overwintering dynamics appears to exist for most small pelagic fishes that now exist in the North and Baltic Seas (e.g., sprat, herring, European anchovy, European sardine). Ecophysiological constaints such as factors affecting overwintering survival are clearly a relevant topics to address in future research programs that attempt to go beyond merely correlating changes in abundance and distribution to climate indices (e.g., Alheit et al., 2012) but also attempt to reveal the mechanisms causing these fluctuations (e.g., Hufnagl and Peck, 2011; Petitgas et al., 2012) in order to gain a cause-and-effect understanding that will aid in projections of future conditions.

gained during the German GLOBEC program. Considerable information now exists on the ecophysiology of most life stages of this species. The review was restricted to aspects of feeding and growth physiology and did not encompass a variety of topics (e.g., migration behavior, stock structure, population demographics, mortality rates, and recruitment patterns). Field and laboratory research allowed, among other things, the development of physiologicallybased growth models including mechanistic individual-based models (IBMs) of larval foraging and growth (e.g., Peck and Daewel, 2007). These IBM’s, when coupled to 3-D hydrodynamic models, are tools that are normally developed and applied towards the end of large-scale fisheries oceanographic research programs (like GLOBEC-Germany) as a way of synthesizing and testing process knowledge. Larval sprat IBMs utilized in German GLOBEC have examined the impacts of prey field variability on survival and growth in the North Sea (Daewel et al., 2008; Kühn et al., 2008) and Baltic Sea (Hinrichsen et al., 2010a, submitted for publication). Knowledge on stage-specific growth physiology is a prerequisite for building robust process models that attempt to explain (in a mechanistic fashion) environmental constraints on the vital rates and recruitment of marine fish populations and projecting climate impacts (Pörtner and Farrell, 2008; Rijnsdorp et al., 2009; Pörtner and Peck, 2010). Based on our review, a number of gaps in knowledge were identified including processes related to (1) first-feeding prey and feeding success (potential role of the microbial loop), (2) ontogenetic development during the larval period (physiological changes permitting larvae to inhabit and grow well in higher temperatures), and (3) late-stage juveniles (high rate of feeding and the role of overwinter mortality as a constraint to life-history scheduling in northern areas). Such topics would be germane for future investigations on sprat and many other temperate marine fish species. Based on sequential correlations of the abundance of different life stages with recruitment, the transitional-larval/early juvenile phase was recognized as a critical period in Baltic sprat (Köster et al., 2003; Baumann et al., 2006a; Voss et al., submitted for publication) but the mechanisms were not identified. In terms of growth physiology of sprat in the Baltic Sea, it appears that cohorts produced relatively late in the spawning season can contribute the bulk of survivors in some years (Voss et al., submitted for publication) and access of YOY juveniles to relatively warm, productive waters would be required to enhance growth and survival. On the other hand, at high stock sizes (when juveniles are very abundant), this life-history strategy might increase the potential for top-down control of zooplankton. This density-dependent mechanism would reduce survival and recruitment both indirectly (by reducing growth rates making individuals more vulnerable to predation) and directly (via starvation prior to or during the overwinter period).

5. Conclusions: From physiology to process knowledge

References

This study summarized existing knowledge on the ecology and growth physiology of sprat and highlighted recent knowledge

Alekseev, F.E., Alekseeva, E.I., 2005. Batch fecundity and daily egg production of the Baltic sprat Sprattus sprattus balticus (Clupeidae) from the southeastern part of the Baltic Sea. Journal of Ichthyology 45, 93–102.

Acknowledgements The authors would like to thank all of the participants of the German GLOBEC program including the many laboratory assistants and members of research vessel crews that helped collect the data that were presented within this manuscript. GLOBEC Germany was funded by the German Federal Ministry for Education and Research (FKZ 03F0320E). Partial funding for this research was also received from the ‘‘FACTS’’ (Forage Fish Interactions, EU FP7, 244966) research program.

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M.A. Peck et al. / Progress in Oceanography 107 (2012) 31–46

Alheit, J., 1988. Reproductive biology of sprat (Sprattus sprattus): factors determining annual egg production. Conseil International pour le Exploration de la Mer 44, 162–168. Alheit, J., Wahl, E., Cibangir, B., 1987. Distribution, abundance, development rates, production and mortality of sprat eggs. International Council for the Exploration of the Seas. ICES CM/H:45. Alheit, J., Möllmann, C., Dutz, J., Kornilovs, G., Loewe, P., Mohrholz, V., Wasmund, N., 2005. Synchronous ecological regime shifts in the central Baltic and the North Sea in the late 1980s. ICES Journal of Marine Science 62 (7), 1205–1215. Alheit, J., Pohlmann, T., Casini, M., Greve, W., Hinrichs, R., Mathis, M., O’Driscoll, K., Vorberg, R., Wagner, C., 2012. Climate variability drives anchovies and sardines into the North and Baltic Seas. Progress in Oceanography 96, 128–139. Alshut, S., 1988a. Seasonal variations in length frequency and birthdate distribution of juvenile sprat (Sprattus sprattus). International Council for the Exploration of the Sea. ICES CM 1988/H:44. Alshut, S., 1988b. Daily growth increments on otoliths of laboratory reared sprat, Sprattus sprattus L., larvae. Meeresforschung 32, 23–29. Arrhenius, F., 1996. Diet composition and food selectivity of 0-group herring (Clupea harengus L.) and sprat (Sprattus sprattus L.) in the northern Baltic Sea. ICES Journal of Marine Science 53, 701–712. Arrhenius, F., 1998. Food intake and seasonal changes in energy content of young Baltic Sea sprat (Sprattus sprattus L.). ICES Journal of Marine Science 55, 319– 324. Arrhenius, F., Hansson, S., 1993. Food consumption of larval, young and adult herring and sprat in the Baltic Sea. Marine Ecology Progress Series 96, 125–137. Bailey, R.S., 1980. Problems in the management of short-lived pelagic fish as exemplified by North Sea sprat. Rapports et Proces-Verbaux des Reunions, Conseil International pour L’Exploration de la Mer 177, 477–488. Bakun, A., Broad, K., 2003. Environmental ‘loopholes’ and fish population dynamics: comparative pattern recognition with focus on El Niño effects in the Pacific. Fisheries Oceanography 12, 458–473. Baumann, H., Hinrichsen, H.-H., Voss, R., Stepputtis, D., Grygiel, W., Clausen, L.W., Temming, A., 2006a. Linking growth- to environmental histories in central Baltic young-of-the-year sprat, Sprattus sprattus: an approach based on otolith microstructure analysis and hydrodynamic modeling. Fisheries Oceanography 15, 465–476. Baumann, H., Gröhsler, T., Kornilovs, G., Makarchouk, A., Feldman, V., Temming, A., 2006b. Temperature-induced regional and temporal growth differences in Baltic young-of-the-year sprat, Sprattus sprattus. Marine Ecology Progress Series 317, 225–236. Baumann, H., Peck, M.A., Götze, E., Temming, A., 2007. Starving early juvenile sprat, Sprattus sprattus L., in Western Baltic coastal waters: evidence from combined field and laboratory observations in August/September 2003. Journal of Fish Biology 70, 853–866. Baumann, H., Voss, R., Hinrichsen, H.-H., Mohrholz, V., Schmidt, J.O., Temming, A., 2008. Investigating the selective survival of summer- over spring-sprat, Sprattus sprattus, in the Baltic Sea. Fisheries Research 91, 1–14. Baumann, H., Voss, R., Malzahn, A., Temming, A., 2009. The German Bight (North Sea) is a nursery area for both locally and externally produced sprat juveniles. Journal of Sea Research 61, 234–243. Bernreuther, M., 2007. Investigations on the feeding ecology of Baltic Sea herring (Clupea harengus L.) and sprat (Sprattus sprattus L.). PhD Thesis. Institute for Hydrobiology and Fisheries Science, University of Hamburg, Hamburg, Germany, 184pp. Bernreuther, M., Temming, A., Herrmann, J.-P., 2009. Gastric evacuation in sprat (Sprattus sprattus L.). Journal of Fish Biology 75, 1529–1541. Brett, J.R., 1979. Environmental factors and growth. In: Hoar, W.S., Randall, D.J., Brett, J.R. (Eds.), Fish Physiology, vol. VIII. Academic Press, London, pp. 599– 667. Cardinale, M., Casini, M., Arrhenius, F., 2002. The influence of biotic and abiotic factors on the growth of sprat (Sprattus sprattus) in the Baltic Sea. Aquatic Living Resources 15, 273–281. Casini, M., Cardinale, M., Arrhenius, F., 2004. Feeding preferences of herring (Clupea harengus) and sprat (Sprattus sprattus) in the southern Baltic Sea. ICES Journal of Marine Science 61, 1267–1277. Casini, M., Cardinale, M., Hjelm, J., 2006. Inter-annual variation in herring, Clupea harengus, and sprat, Sprattus sprattus, condition in the central Baltic Sea: what gives the tune? Oikos 112, 638–650. Conover, D.O., 1992. Seasonality and the scheduling of life history at different latitudes. Journal of Fish Biology 41 (Suppl. sB), 161–178. Coull, K.A., Jermyn, A.S., Newton, A.W., Henderson, G.I., Hall, W.B., 1989. Length/ weight relationships for 88 species of fish encountered in the North Atlantic. Scottish Fisheries Research Reports 43, 1–80. Cury, P., Bakun, A., Crawford, R.J., Jarre, A., Quinones, R.A., Shannon, L.J., Verheye, H.M., 2000. Small pelagics in upwelling systems: patterns of interaction and structural changes in ‘‘wasp-waist’’ ecosystems. ICES Journal of Marine Science 57, 603–618. Daenhardt, A., Peck, M.A., Clemmesen, C., Temming, A., 2007. Depth-dependent nutritional condition of sprat larvae in the central Bornholm Basin. Baltic Sea Marine Ecology Progress Series 341, 217–228. Daewel, U., Peck, M.A., Kühn, W., St. John, M.A., Alekseeva, I., Schrum, C., 2008. Coupling ecosystem and individual-based models to simulate the influence of environmental variability on potential growth and survival of larval sprat (Sprattus sprattus L.) in the North Sea. Fisheries Oceanography 17, 333–351. Dänhardt, A., Temming, A., 2008. Effects of haul duration on the physical condition of sprat larvae. Aquatic Biology 1, 135–139.

Daskalov, G., 1999. Relating fish recruitment to stock biomass and physical environment in the Black Sea using generalized additive models. Fisheries Research 41, 1–23. de Figuiredo, G.M., Nash, R.D.M., Montagnes, D.J.S., 2007. Do protozoa contribute significantly to the diet of larval fish in the Irish Sea? Journal of the Marine Biological Association of the UK 87, 843–850. De Silva, S.S., 1973. Food and feeding habits of the herring Clupea harengus and the sprat C. sprattus in inshore waters of the west coast of Scotland. Marine Biology 20, 282–290. Debes, P.V., Zachos, F.E., Hanel, R., 2008. Mitochond rial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic. Molecular Ecology 17, 3873–3888. Dickmann, M., Möllmann, C., Voss, R., 2007. Feeding ecology of Central Baltic sprat Sprattus sprattus larvae in relation to zooplankton dynamics: implications for survival. Marine Ecology Progress Series 342, 277–289. Dulcˆic´, J., 1998. Larval growth of sprat, Sprattus sprattus phalericus, larvae in the northern Adriatic. Fisheries Research 36, 117–126. Durbin, E., Durbin, A., 1975. Grazing rates of the Atlantic menhaden Brevoortia tyrannus as a function of particle size and concentration. Marine Biology 33, 265–277. Dygert, P., 1990. Seasonal changes in energy content and proximate composition associated with somaticgrowth and reproduction in a representative age–class of female English sole. Transactions of the American Fisheries Society 119, 791– 801. Fuiman, L.A., 1983. Growth gradients in fish larvae. Journal of Fish Biol. 23, 117–123. Garrido, S., Marçalo, A., Zwolinski, J., van der Lingen, C.D., 2007. Laboratory investigations on the effect of prey size and concentration on the feeding behaviour of Sardina pilchardus. Marine Ecology Progress Series 330, 189– 199. George, M.R., Alheit, J., 1987. Ovarian maturation cycle of sprat, Sprattus sprattus. International Council for the Exploration of the Sea. ICES CM/H 47. Gotceitas, V., Methven, D.A., Sandy Fraser, S., Brown, J.A., 1999. Effects of body size and food ration on over-winter survival and growth of age-0 Atlantic cod, Gadus morhua. Environmental Biology of Fishes 54, 413–420. Grauman, G.B., Yula, E., 1989. The importance of abiotic and biotic factors in early ontogenesis of cod and sprat. Rapports et procès-verbaux des réunions, Conseil permanent international pour l’exploration de la mer 190, 207–210. Günther, C., 2008. Untersuchungen zum Sommerwachstum juveniler Sprotten (Sprattus sprattus) in der westlichen Ostsee. University of Hamburg, Diplomarbeit, 89 pp. Hanel, R., Karjalainen, J., Wieser, W., 1996. Growth of swimming muscles and its metabolic cost in larvae of whitefish at different temperatures. Journal of Fish Biology 48, 937–951. Haslob, H., 2011. Reproductive ecology of Baltic sprat and its application in stock assessment. Dissertation. University of Kiel, Kiel, Germany, 133 pp. Haslob, H., Clemmesen, C., Schaber, M., Hinrichsen, H.-H., Schmidt, J.O., Voss, R., Kraus, G., Köster, F.W., 2007. Invading Mnemiopsis leidyi as a potential threat to Baltic fish. Marine Ecology Progress Series 349, 303–306. Haslob, H., Tomkiewicz, J., Hinrichsen, H.H., Kraus, G., 2011. Spatial and interannual variability in Baltic sprat batch fecundity. Fisheries Research 110 (2), 289–297. Heidrich, H., 1925. Über die Fortpflanzung von Clupea sprattus in der Kieler Bucht. Wissenschaftliche Meeresuntersuchungen 20, 1–47. Hinrichsen, H.-H., Kraus, G., Voss, R., Stepputtis, D., Baumann, H., 2005. The general distribution pattern and mixing probability of Baltic sprat juvenile populations. Journal of Marine Systems 58, 52–66. Hinrichsen, H.-H., Peck, M.A., Schmidt, J., Huwever, B., Voss, R., 2010a. Decadal changes in the diel vertical migration behaviour of Baltic sprat larvae: causes and consequences. Limnology and Oceanography 55 (4), 1484–1498. Hinrichsen, H.H., Voss, R., Huwer, B., Clemmesen, C., 2010b. Variability of larval Baltic sprat (Sprattus sprattus L.) otolith growth: a modeling approach combining spatially and temporally resolved biotic and abiotic environmental key variables. Fisheries Oceanography 19, 463–479. Hinrichsen, H.-H., Kühn, W., Peck, M.A., Voss, R., submitted for publication. The impact of physical and biological factors on the drift and spatial distribution of larval sprat: a comparison of the Baltic and North Seas. Progress in Oceanography. Holtappels, M., 2004. The nutritional condition of sprat and sardine larvae in the frontal systems of the German Bight. M.Sc. Thesis. University of Rostock, Institute for Baltic Sea Research, Warnemünde, Germany, 87 pp. Höök, T.O., Rutherford, E.S., Mason, D.M., Carter, G.S., 2007. Hatch dates, growth, survival, and overwinter mortality of age-0 alewives in Lake Michigan: implications for habitat-specific recruitment success. Transactions of the American Fisheries Society 136, 1298–1312. Houde, E.D., 1989. Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. US Fishery Bulletin 87, 471– 495. Houde, E.D., Schekter, R.C., 1983. Oxygen uptake and comparative energetics among eggs and larvae of three subtropical marine fishes. Marine Biology 72, 283–293. Houde, E.D., Zastrow, C.E., 1993. Ecosystem- and taxon-specific dynamic and energetic properties of larval fish assemblages. Bulletin of Marine Science 53 (2), 290–335. Hufnagl, M., Peck, M.A., 2011. Physiological-based modelling of larval Atlantic herring (Clupea harengus) foraging and growth: insights on climate-driven life history scheduling. ICES Journal of Marine Science 68 (6), 1170–1188.

M.A. Peck et al. / Progress in Oceanography 107 (2012) 31–46 Huwer, B., 2004. Larval growth of Sardina pilchardus and Sprattus sprattus in relation to frontal systems in the German Bight. Diploma Thesis. Institut für Meereskunde, Christian-Albrechts-Universität zu Kiel, 108 p. ICES, 2009. Report of the Baltic Fisheries Assessment Working Group (WGBFAS), 22–28 April 2009. ICES Headquarters, Copenhagen. ICES CM 2009/ACOM:07, 626 pp. Jorgensen, E.H., Johansen, S.J.S., Jobling, M., 1997. Seasonal patterns of growth, lipid deposition, and lipid depletion in anadromous Arctic charr. Journal of Fish Biology 51, 312–326. Kanstinger, P., 2007. Growth and condition of larval sprat (Sprattus sprattus): a combined laboratory and field investigation. University of Hamburg, Diplomarbeit, 86 pp. Karaseva, E.M., Ivanovich, V.M., 2010. Vertical distribution of eggs and larvae of the Baltic Sprat Sprattus sprattus balticus (Clupeidae) in relation to seasonal and diurnal variation. Journal of Ichthyology 50, 259–269. Keckeis, H., Schiemer, F., 1992. Food consumption and growth of larvae and juveniles of three cyprinid species at different food levels. Environmental Biology of Fishes 33, 33–45. Kornilovs, G., Sidrevics, L., Dippner, J.W., 2001. Fish and zooplankton interaction in the Central Baltic Sea. ICES Journal of Marine Science 58, 579–588. Köster, F.W., Hinrichsen, H.-H., Schnack, D., St. John, M.A., MacKenzie, B.R., Tomkiewicz, J., Möllmann, C., Kraus, G., Plikshs, M., Makarchouk, A., Eero, A., 2003. Recruitment of Baltic cod and sprat stocks: identification of critical life stages and incorporation of environmental variability into stock-recruitment relationships. Scientia Marina 67 (Suppl. 1), 129–154. Kraus, G., Köster, F.W., 2004. Estimating Baltic sprat (Sprattus sprattus balticus S.) population size from egg production. Fisheries Research 69, 313–329. Kraus, G., Mohrholz, V., Voss, R., Dickmann, M., Hinrichsen, H.H., Hermann, J.P., 2004. Consequences of summer inflow events on the reproduction cycle of Baltic sprat. International Council for the Exploration of the Sea. ICES CM/L:19. Kühn, W., Peck, M.A., Hinrichsen, H.-H., Daewel, U., Moll, A., Pohlmann, T., Stegert, C., Tamm, S., 2008. Defining habitats suitable for larval fish in the German Bight (southern North Sea): an IBM approach using spatially- and temporallyresolved, size-structured prey fields. Journal of Marine Systems 74, 329– 342. Last, J.M., 1987. The food of immature sprat (Sprattus sprattus (L.)) and herring (Clupea harengus L.) in coastal waters of the North Sea. Journal du Conseil International pour l´Exploration de la mer 44, 73–79. Lee, O., Danilowicz, B.S., Dickey-Collas, M., 2006. Temporal and spatial variability in growth and condition of dab (Limanda limanda) and sprat (Sprattus sprattus) larvae in the Irish Sea. Fisheries Oceanography 15, 490–507. Limborg, M.T., Pedersen, J.S., Hemmer-Hansen, J., Tomkiewicz, J., Bekkevold, D., 2009. Genetic population structure of European sprat Sprattus sprattus: differentiation across a steep environmental gradient in a small pelagic fish. Marine Ecology Progress Series 379, 213–224. MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton Univ. Press, Princeton, NJ. MacKenzie, B.R., Köster, F.W., 2004. Fish production and climate: sprat in the Baltic Sea. Ecology 85, 784–794. Meskendahl, L., Herrmann, J.P., Temming, A., 2010. Effects of temperature and body mass on metabolic rates of sprat, Sprattus sprattus L. Marine Biology 157, 1917– 1927. Möllmann, C., Köster, F.W., 2002. Population dynamics of calanoid copepods and the implications of their predation by clupeid fish in the Central Baltic Sea. Journal of Plankton Research 24, 959–977. Möllmann, C., Kornilovs, G., Fetter, M., Köster, F.W., 2004. Feeding ecology of central Baltic Sea herring and sprat. Journal of Fish Biology 65, 1563–1581. Möllmann, C., Diekmann, R., Müller-Karulis, B., Kornilovs, G., Plikshs, M., Axe, P., 2009. Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Global Change Biology 15, 1377–1393. Munk, P., 1993. Differential growth of larval sprat Sprattus sprattus across a tidal front in the eastern North Sea. Marine Ecology Progress Series 99, 17–27. Muus, B.J., Nielsen, J.G., 1999. Seafish. Blackwell Science, Oxford, UK, pp. 1–340. Nissling, A., 2004. Effects of temperature on egg and larval survival of cod (Gadus morhua) and sprat (Sprattus sprattus) in the Baltic Sea – implications for stock development. Hydrobiologia 514, 115–123. Osse, J.W.M., van den Boogaart, J.G.M., 1995. Fish larvae, development, allometric growth and the aquatic environment. ICES Marine Science Symposium 201, 21– 34. Overton, J.L., Meyer, S., Støttrup, J.G., Peck, M.A., 2010. The role of heterotrophic protists in first feeding by cod (Gadus morhua L.) larvae. Marine Ecology Progress Series 410, 197–204. Peck, M.A., Daewel, U., 2007. Physiologically-based limits to larval fish food consumption and growth: implications for individual-based models. Marine Ecology Progress Series 347, 171–183. Peck, M.A., Hufnagl, M., 2012. Can IBMs explain why most larvae die in the sea? Model scenarios and sensitivity analyses reveal research needs. Journal of Marine Systems 93, 77–93. Peck, M.A., Clemmesen, C., Baumann, H., Herrmann, J.-P., Stäcker, S., Temming, A., 2004. The growth-feeding relationship in post-larval sprat (Sprattus sprattus): comparison of somatic, nucleic acid- and otolith-based growth rates. International Council for the Exploration of the Sea. ICES CM 2004/L:25. Peck, M.A., Clemmesen, C., Herrmann, J.-P., 2005. Ontogenic changes in the allometric scaling of the mass and length relationship in Sprattus sprattus. Journal of Fish Biology 66, 882–887.

45

Peck, M.A., Kühn, W., Clemmesen, C., Hinrichsen, H.-H., Holtappels, M., Huwer, B., Pohlmann, T., 2007. Variability in growth rates of larval fish at frontal stations in the southern North Sea: is the ‘‘mean’’ all that matters? GLOBEC International Newsletter 14 (1), 70–71. Pedersen, B.H., 1984. The intestinal evacuation rates of larval herring (Clupea harengus L.) predating on wild plankton. Dana 3, 21–30. Pepin, P., 1995. An analysis of the length-weight relationship of larval fish: limitations of the general allometric model. US Fisheries Bulletin 93, 419–426. Pepin, P., Dower, J.F., 2007. Variability in the trophic position of larval fish in a coastal pelagic ecosystem based on stable isotope analysis. Journal of Plankton Research 29 (8), 727–737. Pepin, P., Penney, R.W., 1997. Patterns of prey size and taxonomic composition in larval fish: are there general size-dependent models? Journal of Fish Biology 51, 84–100. Pepin, P., Penney, R.W., 2000. Feeding by a larval fish community: impact on zooplankton. Marine Ecology Progress Series 204, 199–212. Petereit, C., 2008. Influence of temperature and salinity on sprat (Sprattus sprattus) eggs and yolk sac larvae from contrasting environments. PhD Dissertation. University of Kiel, Kiel, Germany, 113 pp. Petereit, C., Haslob, H., Kraus, G., Clemmesen, C., 2008. The influence of temperature on the development of Baltic Sea sprat (Sprattus sprattus) eggs and yolk sac larvae. Marine Biology 154, 295–306. Petitgas, P., Alheit, J., Peck, M.A., Raab, K., Irigoien, X., Huret, M., van der Kooij, J., Pohlmann, T., Wagner, C., Zarraonaindia, I., Dickey-Collas, M., 2012. Anchovy expansion in the North Sea. Marine Ecology Progress Series 444, 1–13. Petrova, E.G., 1960. On the fecundity and maturation of Baltic sprat. Trudy Vsesojuznyj naucno issledovatelskij. Institut Morskogo Rybnogo Xozjajstva i Okeanografii 42, 99–108 (in Russian). Pörtner, H.O., Farrell, A.P., 2008. Physiology and climate change. Science 322, 690– 692. Pörtner, H.O., Peck, M.A., 2010. Climate change impacts on fish and fisheries: towards a cause and effect understanding. Journal of Fish Biology 77, 1745– 1779. Raab, K., Nagelkerke, L.A.J., Boerée, C., Rijnsdorp, A.D., Temming, A., Dickey-Collas, M., 2011. Anchovy Engraulis encrasicolus diet in the North and Baltic Seas. Journal of Sea Research 65, 131–140. Rè, P., Gonçalves, E., 1993. Growth of sprat Sprattus sprattus larvae in the German Bight (North Sea) as inferred by otolith microstructure. Marine Ecology Progress Series 96, 139–145. Rijnsdorp, A., Peck, M.A., Engelhard, G.H., Möllmann, C., Pinnegar, J.K., 2009. Resolving the effect of climate change on fish populations. ICES Journal of Marine Science 66, 1570–1583. Rose, K.A., 24 co-authors, 2010. End-to-end models for the analysis of marine ecosystems: challenges, issues, and next steps. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 2, 115–130. Rudstam, L.G., Hansson, S., Johansson, S., Larsson, U., 1992. Dynamics of planktivory in a coastal area of the northern Baltic Sea. Marine Ecology Progress Series 80, 159–173. Safran, P., 1992. Theoretical analysis of the weight-length relationship in fish juveniles. Marine Biology 112, 545–551. Schultz, E.T., Conover, D.O., Ehtisham, E., 1998. The dead of winter: size dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae: Menidia menidia) from different latitudes. Canadian Journal of Fisheries and Aquatic Science 55, 1149–1157. Schulz, J., Barz, K., Peck, M.A., Schmidt, J.O., Hansen, F., Peters, J., Renz, J., Dickmann, M., Mohrholz, V., Dutz, J., Hirche, H.-H., submitted for publication. Spatial and temporal habitat partitioning by zooplankton in the Bornholm Sea (central Baltic Sea). Progress in Oceanography. Shields, R.J., 1989. Studies of growth and nutritional status in 0-group sprat, Sprattus sprattus (Clupeidae), using otolith microstructure and lipid analytical techniques. PhD Thesis. University of Wales, Bangor. Shvetsov, F.G., Starodub, M.L., Sidrevits, L.L., 1983. The daily feeding rhythm of the Baltic sprat, Sprattus sprattus balticus (Clupeidae). Journal of Ichthyology 23 (2), 99–105. Sirotenko, M.D., Sorokalit, L.K., 1979. Seasonal changes in the food of the Mediterranean sprat, Sprattus sprattus phalericus. Journal of Ichthyology 19 (5), 37–51. Smith, R.L., Paul, A.J., 1990. Seasonal changes in energy and energy cost of spawning in Gulf of Alaska Pacific cod. Journal of Fish Biology 36, 307–316. Stepputtis, D., 2006. Distribution patterns of Baltic sprat (Sprattus sprattus L.) – causes and consequences. PhD Thesis. Leibniz Institute for Marine Research, Kiel, 198 pp. Szypula, J., 1985. Comparative studies on herring and sprat feeding in the southern Baltic within 1978–1982. Acta Ichthyologica et Piscatoria 15 (2), 75–89. Szypula, J., Grygiel, W., Wyszynski, M., 1997. Feeding of Baltic herring and sprat in the period 1986–1996 in relation to their state and biomass. Bulletin of the Sea Fisheries Institute 3 (142), 73–83. Thompson, B.M., Milligan, S.P., Nichols, J.H., 1981. The development rates of Sprat (Sprattus sprattus L.) eggs over a range of temperatures. International Council for the Exploration of the Sea. ICES CM 1981/H:15. Valenzuela, G.S., Vargas, C.A., 2002. Comparative growth rate of Sprattus sprattus in relation to physical and oceanographic features in the North Sea. Archive of Fisheries and Marine Research 49 (3), 213–230. Vieira, V.L.A., Johnston, I.A., 1992. Influence of temperature on muscle-fibre development in larvae of the herring Clupea harengus. Marine Biology 112, 333–341.

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M.A. Peck et al. / Progress in Oceanography 107 (2012) 31–46

Voss, R., Köster, F.W., Dickmann, M., 2003. Comparing the feeding habits of cooccurring sprat (Sprattus sprattus) and cod (Gadus morhua) larvae in the Bornholm Basin, Baltic Sea. Fisheries Research 63, 97–111. Voss, R., Clemmesen, C., Baumann, H., Hinrichsen, H.-H., 2006. Baltic sprat larvae: coupling food availability, larval condition and survival. Marine Ecology Progress Series 308, 243–254. Voss, R., Schmidt, J.O., Schnack, D., 2007. Vertical distribution of Baltic sprat larvae: changes in patterns of diel migration? ICES Journal of Marine Science 64 (5), 956–962. Voss, R., Dickmann, M., Schmidt, J.O., 2009. Feeding ecology of sprat (Sprattus sprattus L.) and sardine (Sardina pilchardus W.) larvae in the German Bight, North Sea. Oceanologia 51, 117–138. Voss, R., Peck, M.A., Hinrichsen, H.-H., Clemmesen, C., Baumann, H., Stepputtis, D., Bernreuther, M., Schmidt, J.O., Temming, A., Köster, F.W., submitted for

publication. Recruitment processes in Baltic sprat – a re-evaluation of GLOBEC-Germany hypotheses. Progress in Oceanography. Wahl, E., Alheit, J., 1988. Changes in the distribution and abundance of sprat eggs during spawning season. International Council for the Exploration of the Sea. ICES CM 1988/H:45. Whitehead, P.J.P., 1985. Clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolfherrings. Part 1 Chirocentridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis 125 (7), 1–303. Wieland, K., Zuzarte, F, 1991. Vertical distribution of cod and sprat eggs and larvae in the Bornholm Basin (Baltic Sea) in 1987–1990. International Council for the Exploration of the Sea. ICES CM 1991/J:37. Wosnitza, C., 1974. Die Nahrung von Fischbrut in der westlichen Ostsee. Berichte der Deutschen Wissenschaftlichen Kommission für Meeresforschung 24, 79–92.