Linking growth to environmental histories in central Baltic young-of-the-year sprat, Sprattus sprattus: an approach based on otolith microstructure analysis and hydrodynamic modelling

Otolith microstructure analysis and hydrodynamic modelling were combined to study growth patterns in young‐of‐the‐year (YoY) sprat, Sprattus sprattus, which were sampled in October 2002 in the central Baltic Sea. The observed ‘window of survival’, approximated by the distribution of back‐calculated days of first feeding (DFF), was narrow compared to the extended spawning season of sprat in the Baltic Sea (mean± SD = 22 June ± 14.1 days) and indicated that only individuals born in summer survived until October 2002. Within the group of survivors, individuals born later in the season exhibited faster larval, but more rapidly decreasing juvenile growth rates than earlier born conspecifics. Back‐calculated larval growth rates of survivors (0.48–0.69 mm day^?1) were notably higher than those previously reported for average larval sprat populations, suggesting that the YoY population was predominantly comprised of individuals which grew faster during the larval stage. Daily mean temperatures, experienced across the entire YoY population, were derived from Lagrangian particle simulations and correlated with (1) detrended otolith growth and (2) back‐calculated, daily somatic growth rates of survivors. The results showed that abrupt changes in ambient temperature can be detected in the seasonal pattern of otolith growth, and that higher temperatures led to significantly faster growth throughout the entire age range of YoY sprat.     

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

To investigate the impact of changing environmental conditions in the North Sea on the distribution and survival of early life stages of a marine fish species, we employed a suite of coupled model components: (i) an Eulerian coupled hydrodynamic/ecosystem (Nutrients, Phyto‐, Zooplankton, Detritus) model to provide both 3‐D fields of hydrographical properties, and spatially and temporally variable prey fields; (ii) a Lagrangian transport model to simulate temporal changes in cohort distribution; and (iii) an individual‐based model (IBM) to depict foraging, growth and survival of fish early life stages. In this application, the IBM was parameterized for sprat (Sprattus sprattus L.) and included non‐feeding (egg and yolk‐sac larval) stages as well as foraging and growth subroutines for feeding (post‐yolk sac) larvae. Sensitivity analyses indicated that the angle of visual acuity, assimilation efficiency and the maximum food consumption rate were the most critical intrinsic model parameters. As an example, we applied this model system for 1990 in the North Sea. Results included not only information concerning the interplay of temperature and prey availability on larval fish survival and growth but also information on mechanisms underlying larval fish aggregation within frontal zones. The good agreement between modelled and in situ estimates of sprat distribution and growth rates in the German Bight suggested that interconnecting these different models provided an expedient tool to scrutinize basic processes in fish population dynamics.     

The growth of larval cod and haddock in the Irish Sea: a model with temperature,prey size and turbulence forcing

We applied a physiological individual‐based model for the foraging and growth of cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) larvae, using observed temperature and prey fields data from the Irish Sea, collected during the 2006 spawning season. We used the model to estimate larval growth and survival and explore the different productivities of the cod and haddock stocks encountered in the Irish Sea. The larvae of both species showed similar responses to changes in environmental conditions (temperature, wind, prey availability, daylight hours) and better survival was predicted in the western Irish Sea, covering the spawning ground for haddock and about half of that for cod. Larval growth was predicted to be mostly prey‐limited, but exploration of stock recruitment data suggests that other factors are important to ensure successful recruitment. We suggest that the presence of a cyclonic gyre in the western Irish Sea, influencing the retention and/or dispersal of larvae from their spawning grounds, and the increasing abundance of clupeids adding predatory pressure on the eggs and larvae; both may play a key role. These two processes deserve more attention if we want to understand the mechanisms behind the recruitment of cod and haddock in the Irish Sea. For the ecosystem‐based management approach, there is a need to achieve a greater understanding of the interactions between species on the scale a fish stock is managed, and to work toward integrated fisheries management in particular when considering the effects of advection from spawning grounds and prey–predator reversal on the recovery of depleted stocks.     

The importance of individual behaviour for successful settlement of juvenile plaice (Pleuronectes platessa L.): a modelling and field study in the eastern Irish Sea

To study the transport of plaice (Pleuronectes platessa L.) eggs and larvae in the eastern Irish Sea, we constructed a 3D‐baroclinic physical model and coupled it to a particle‐tracking scheme that allowed aspects of larval behaviour to be simulated. Starting positions for eggs were based upon data from a series of ichthyoplankton surveys and final positions were compared with results of settled plaice distributions from two beam trawl surveys conducted on beaches around the eastern Irish Sea. If simulated larval behaviour was limited to passive drift or horizontal swimming, the particles diffused away from the spawning areas but failed to reach nursery grounds in significant numbers (85–90% remaining offshore). In contrast, switching on circatidal vertical swimming significantly increased the numbers of larvae reaching the coast (only 23–30% remained offshore). Particles tended to accumulate in bays and estuaries and this pattern compared well with the distribution of settled plaice from the field surveys. Studies in the southern North Sea (where spawning and nursery grounds are widely separated) have also demonstrated the importance of selective tidal stream transport for successful recruitment of settling plaice to nursery grounds. Although our understanding of the ontogeny of this behaviour is still poor, the model results presented suggest that this aspect of behaviour is a key factor influencing plaice settlement success.     

Seasonal changes in otolith increment width trajectories and the effect of temperature on the daily growth rate of young sardines

We studied the otolith microstructure and growth of sardine, Sardina pilchardus, in the North Aegean Sea (eastern Mediterranean Sea), using samples of larvae and juveniles that had hatched in winter (November–January) and winter–spring (February–May), respectively. The juveniles had developed during an extended period coinciding with marked pelagic ecosystem changes (from winter, mixed conditions to summer, stratified waters). To examine the relationship between environmental changes and the observed variability in their otolith increment–width trajectories (width‐at‐age), we summarized the shape of trajectories with a four‐parameter set estimated from a growth model fit to each width trajectory. The individual parameter sets were then related to the potential oceanographic conditions that fish experienced during their development, derived from a hydrodynamic–biogeochemical model (POM‐ERSEM), implemented in the sampling area. Substantial seasonal effects were demonstrated on the otolith microstructure (platykurtic versus leptokurtic trajectories in winter‐mixed versus summer‐stratified conditions), which were related to the progressive sea surface warming. In a subsequent step, in order to study the effect of oceanographic conditions on larval and juvenile daily growth rates, a GAM (Generalized Additive Model) analysis of otolith increment widths was carried out, using model‐derived oceanographic parameters and taking into account the ‘inherent otolith growth’, expressed by the explanatory variables ‘previous increment width’ and ‘Age’. Results showed a strong and positive, linear effect of temperature on the growth rate of winter‐caught larvae, whereas in juveniles, which had developed within a wide range of temperatures, an optimum temperature for growth was observed at around 24°C.     

Environmental variability and growth histories of larval Japanese sardine (Sardinops melanostictus) and Japanese anchovy (Engraulis japonicus) near the frontal area of the Kuroshio

Environmental variability and growth‐rate histories from hatching to capture were investigated for larval Japanese sardine (Sardinops melanostictus) and Japanese anchovy (Engraulis japonicus). Larvae collected around the front of the Kuroshio Current were examined using otolith microstructure analysis, and their movement was estimated from numerical particle‐tracking experiments. Sardine larvae collected inshore of the Kuroshio front originated from a coastal area near the sampling site, while those collected in the offshore area originated from an area 500–800 km west‐southwest of the sampling site. Anchovy larvae collected both inshore and offshore had been transported from widely distributed spawning areas located west of the sampling area. At the age of 13–14 days for sardine and 19–20 days for anchovy, the offshore group exhibited significantly higher mean growth rates than did the inshore group. Although the offshore area was generally warmer than the inshore area, temporal variations in growth rate are not attributable solely to fluctuations in environmental temperature. While previous studies have examined the relationship between larval growth rates and environment based solely on data at capture, the methods used in the present study, combining otolith analysis and numerical particle‐tracking experiments, utilize data up until hatching. Although the relationship between growth rate and environment was not fully confirmed, this approach will greatly advance our understanding of fish population dynamics.     

Vertical distribution of larval Atlantic menhaden (Brevoortia tyrannus) and Atlantic croaker (Micropogonias undulatus): Implications for vertical migratory behaviour and transport

Understanding the interactions among biological and physical processes is essential to determining how the environment affects transport and survival of fishes. We examined vertical distribution in larval Atlantic menhaden (Brevoortia tyrannus) and Atlantic croaker (Micropogonias undulatus) using 126 depth stratified tows in Delaware Bay, USA, during two cruises, in December 2007 and February 2008. Menhaden larvae were 16.8–24.6 and 20.5–26.2 mm standard length in December and February. Corresponding lengths for croaker were 9.3–17.9 and 8.6–19.6 mm. Using empirical observations, and statistically derived models, we explored larval concentration for both species as a function of location, depth, diel period, tidal period, size, and pairwise interactions. Menhaden concentration was best modeled as a function of station, cruise, and interactions between depth and size as well as between station and cruise. No significant differences in larval menhaden concentration were present among tidal and diel periods. Croaker concentration was best modeled as a function of size and interactions between station and diel period, depth and size, cruise and size. Despite tidal period not emerging as a significant model parameter, we observed larger croaker larvae during nighttime flood tides. Our statistical models are consistent with processes of up‐estuary transport for both species, suggesting larvae are increasingly affected by behavioral responses as larvae grow, exhibiting stronger patterns in vertical distribution. The results refine our understanding of the potential importance of size‐related differences in vertical distribution for larval transport in these species. Future research should examine the interactions among size‐specific vertical migratory capabilities, vertical distribution, transport, and retention.     

The effects of temperature on growth,development and settlement of northern rock sole larvae (Lepidopsetta polyxystra)

Northern rock sole (Lepidopsetta polyxystra) is a commercially important fish in the North Pacific and a focal species in understanding larval transport to nursery grounds in the Bering Sea. However, the temperature‐dependent vital rates and settlement dynamics for this species have not been described in detail. We reared northern rock sole larvae in the laboratory to measure growth, condition, development and settlement parameters across four temperatures (2, 4, 7 and 10°C). Both length and mass‐measured growth rates increased with temperature and were best described by non‐linear regression. Residuals of the length–mass relationships were positively related to temperature, indicating larval condition also increased with temperature. Larval development and settlement were largely size dependent, resulting in reduced larval stage duration and earlier settlement at higher temperatures owing to more rapid growth at elevated temperatures. However, larvae at colder temperatures were less developed at a given size, but more likely to settle at smaller sizes than larvae reared in warmer conditions. These temperature–response parameters can be used to refine current and future transport models for northern rock sole larvae under changing environmental conditions in the North Pacific.     

Springtime ichthyoplankton of the slope region off the north-eastern United States of America: larval assemblages, relation to hydrography and implications for larval transport

Larval transport in the slope region off north‐eastern North America influences recruitment to juvenile habitats for a variety of fishes that inhabit the continental shelf. In this study, collections of larval fishes were made during springtime over the continental slope to provide insights into larval distributions and transport. Ichthyoplankton composition and distribution mirrored the physical complexity of the region. Three larval fish assemblages were defined, each with different water mass distributions. A Gulf Stream assemblage was found predominantly in the Gulf Stream and associated with filaments of discharged Gulf Stream water in the Slope Sea. Larvae of this assemblage originated from oceanic and shelf regions south of Cape Hatteras. Several members of this assemblage utilize habitats in the Middle Atlantic Bight (MAB) as juveniles (Pomatomus saltatrix, Peprilus triacanthus) and other members of the assemblage may share this life cycle (Mugil curema, Sphyraena borealis, Urophycis regia). A Slope Sea assemblage was found in all water masses, and was composed of epi‐ and mesopelagic fish larvae, as well as larvae of benthic shelf/slope residents. Larvae of one member of this assemblage (U. tenuis) are spawned in the Slope Sea but cross the shelf‐slope front and use nearshore habitats for juvenile nurseries. A MAB shelf assemblage was found in MAB shelf water and was composed of larvae that were spawned on the shelf. Some of these species may cross into the Slope Sea before returning to MAB shelf habitats (e.g. Enchelyopus cimbrius, Glyptocephalus cynoglossus). Previous studies have examined the effect of warm‐core rings on larval distributions, but this study identifies the importance of smaller‐scale features of the MAB shelf/slope front and of filaments associated with Gulf Stream meanders. In combination with these advective processes, the dynamic nature of larval distributions in the Slope Sea appears to be influenced, to varying degrees, by both vertical and horizontal behaviour of larvae and pelagic juveniles themselves.     

Environmental factors influencing larval sprat Sprattus sprattus feeding during spawning time in the Baltic Sea

The management of Baltic sprat is challenged by highly variable recruitment success and hence large stock fluctuations. Recent studies have identified the larval and early juvenile life stages to be critical for the survival rate of a sprat year class. Although prey abundance was found to be linked to larval survival success, an analysis identifying the functional relationship and relative importance of other environmental factors is still missing. Sprat larval feeding was investigated in 2002 during three cruises, covering the main spawning time in the Bornholm Basin, Baltic Sea. The aim of the study was to identify the key environmental factors determining the feeding success of larval sprat taking their potential interactions explicitly into account. An extension of generalized additive models (GAMs) was adopted that allows the inclusion of interaction terms in a non‐parametric regression model. The final model of sprat larval feeding success explained ～80% of the variance in the data and was based on the following environmental factors: bottom depth, cubed wind speed as proxy for small‐scale turbulence rates, degree of cloudiness as proxy for light conditions and prey density in combination with a feeding period–cloudiness interaction term. Our study demonstrates that the feeding success of sprat larvae in the Baltic Sea is controlled by a number of simultaneously acting key environmental factors.     

Influence of larval transport and temperature on recruitment dynamics of North Sea cod (Gadus morhua) across spatial scales of observation

The survival of fish eggs and larvae, and therefore recruitment success, can be critically affected by transport in ocean currents. Combining a model of early‐life stage dispersal with statistical stock–recruitment models, we investigated the role of larval transport for recruitment variability across spatial scales for the population complex of North Sea cod (Gadus morhua). By using a coupled physical–biological model, we estimated the egg and larval transport over a 44‐year period. The oceanographic component of the model, capable of capturing the interannual variability of temperature and ocean current patterns, was coupled to the biological component, an individual‐based model (IBM) that simulated the cod eggs and larvae development and mortality. This study proposes a novel method to account for larval transport and success in stock–recruitment models: weighting the spawning stock biomass by retention rate and, in the case of multiple populations, their connectivity. Our method provides an estimate of the stock biomass contributing to recruitment and the effect of larval transport on recruitment variability. Our results indicate an effect, albeit small, in some populations at the local level. Including transport anomaly as an environmental covariate in traditional stock–recruitment models in turn captures recruitment variability at larger scales. Our study aims to quantify the role of larval transport for recruitment across spatial scales, and disentangle the roles of temperature and larval transport on effective connectivity between populations, thus informing about the potential impacts of climate change on the cod population structure in the North Sea.     

Spatial and temporal patterns of walleye pollock (Theragra chalcogramma) spawning in the eastern Bering Sea inferred from egg and larval distributions

Walleye pollock Theragra chalcogramma (pollock hereafter) is a key ecological and economic species in the eastern Bering Sea, yet detailed synthesis of the spatial and temporal patterns of pollock ichthyoplankton in this important region is lacking. This knowledge gap is particularly severe considering that egg and larval distribution are essential to reconstructing spawning locations and early life stages drift pathways. We used 19 yr of ichthyoplankton collections to determine the spatial and temporal patterns of egg and larval distribution. Generalized additive models (GAMs) identified two primary temporal pulses of pollock eggs, the first occurring from 20 February to 31 March and the second from 20 April to 20 May; larvae showed similar, but slightly lagged, pulses. Based on generalized cross‐validation and information theory, a GAM model that allowed for different seasonal patterns in egg density within three unique areas outperformed a GAM that assumed a single fixed seasonal pattern across the entire eastern Bering Sea. This ‘area‐dependent’ GAM predicted the highest densities of eggs (i.e., potential spawning locations) in three major areas of the eastern Bering Sea: near Bogoslof Island (February–April), north of Unimak Island and the Alaska Peninsula (March–April), and around the Pribilof Islands (April–August). Unique temporal patterns of egg density were observed for each area, suggesting that pollock spawning may be more spatially and temporally complex than previously assumed. Moreover, this work provides a valuable baseline of pollock spawning to which future changes, such as those resulting from climate variability, may be compared.     

Distribution and drift pathways of Greenland halibut (Reinhardtius hippoglossoides) during early life stages in the eastern Bering Sea and Aleutian Islands

We describe the spatial distribution and dispersal pathways of Greenland halibut (Reinhardtius hippoglossoides) early life stages based on historical field data from the eastern Bering Sea and adjacent water along the eastern Aleutian Islands. Our results indicate that Greenland halibut from preflexion larvae to newly settled juveniles have a long pelagic duration and are subject to extended drift pathways. Hatching may occur in deep water, below 530 m, and larvae rise in the water column as they grow. Flexion/postflexion larvae are mostly found around the Pribilof Islands over the middle shelf (50–100‐m isobaths) in July, and settling occurs during late summer on the middle shelf near St. Matthew Island. However, given that age‐1 individuals were primarily found on the outer shelf, it appears that Greenland halibut actively move to deeper water with age (or size). The mechanisms of slope–shelf connectivity in preflexion larvae may be related to the Bering Slope Current in the vicinity of both Bering and Pribilof Canyons. This study shows that Greenland halibut early life stages have extensive horizontal ontogenetic migrations in the Bering Sea, and utilize a range of geographic areas over the basin and slope along the Aleutian Islands and in the eastern Bering Sea. Based on these results, it is hypothesized that settlement success and recruitment of Greenland halibut may be influenced by variability in currents and flows of the Bering Sea slope and shelf during their transport.     

Effect of tank proportions on survival of seven-band grouper Epinephelus septemfasciatus (Thunberg) and devil stinger Inimicus japonicus (Cuvier) larvae

We examined the effects of rearing‐tank proportions on early survival, surface death and growth of the seven‐band grouper Epinephelus septemfasciatus (Thunberg) and the devil stinger Inimicus japonicus (Cuvier). Fertilized eggs were introduced into three differently shaped 100 L rearing tanks. The three tanks had different water surface areas, and included a shallow tank (S; 71 × 26 cm in diameter and depth, respectively), an intermediate tank (I; 57 × 39 cm) and a deep tank (D; 44 × 70 cm). Both species showed their highest survival rate and the lowest numbers of surface death in the D tank (P<0.05). There were no significant differences between fish reared in the three tank shapes in notochord length, total length, growth rate and dry weight. Rearing‐tank shape affected larval movement in the water column, with the duration of larval movement under the water surface being the shortest in the D tank. These results suggest that using a rearing tank of a suitable shape could significantly reduce the surface death of marine fish larvae.     

Variability of larval Baltic sprat (Sprattus sprattus L.) otolith growth: a modeling approach combining spatially and temporally resolved biotic and abiotic environmental key variables

Plankton sampling was conducted in the Baltic to obtain sprat larvae. Their individual drift patterns were back‐calculated using a hydrodynamic model. The modelled positions along the individual drift trajectories were subsequently used to provide insight into the environmental conditions experienced by the larvae. Autocorrelation analysis revealed that successive otolith increment widths of individual larvae were not independent. Otolith increment width was then modelled using two different generalized additive model (GAM) analyses (with and without autocorrelation), using environmental variables determined for each modelled individual larval position as explanatory variables. The results indicate that otolith growth was not only influenced by the density of potential prey but was controlled by a number of simultaneously acting environmental factors. The final model, not considering autocorrelation, explained more than 80% of the variance of otolith growth, with larval age as a factor variable showing the strongest significant impact on otolith growth. Otolith growth was further explained by statistically significant ambient environmental factors such as temperature, bottom depth, prey density and turbulence. The GAM analysis, taking autocorrelation into account, explained almost 98% of the variability, with the previous otolith increment showing the strongest significant effect. Larval age as well as ambient temperature and prey abundance also had a significant effect. An alternative approach applied individual‐based model (IBM) simulations on larval drift, feeding, growth and survival starting as exogenously feeding larvae at the back‐calculated positions. The IBM results revealed optimal growth conditions for more than 97% of the larvae, with a tendency for our IBM to slightly overestimate larval growth.     

Effect of different enrichment products rich in docosahexaenoic acid on growth and survival of meagre,Argyrosomus regius (Asso, 1801)

Live prey used in aquaculture to feed marine larval fish – rotifer and Artemia nauplii – lack the necessary levels of n‐3 polyunsaturated fatty acids (n‐3 PUFA) which are considered essential for the development of fish larvae. Due to the high voracity, visual feeding in conditions of relatively high luminosity, and cannibalism observed in meagre larvae, a study of its nutritional requirements is needed. In this study, the effect of different enrichment products with different docosahexaenoic acid (DHA) concentrations used to enrich rotifers and Artemia metanauplii have been tested on growth, survival, and lipid composition of the larvae of meagre. The larvae fed live prey enriched with Algamac 3050 (AG) showed a significantly higher growth than the rest of the groups at the end of the larval rearing, while the larvae fed preys enriched with Multigain (MG) had a higher survival rate. DHA levels in larvae fed prey enriched with MG were significantly higher than in those fed AG‐enriched prey. High levels of DHA in Artemia metanauplii must be used to achieve optimal growth and survival of meagre larvae.     

Putting the pieces together: Recent growth,nutritional condition,and mortality of Engraulis anchoita larvae in the Southwest Atlantic

Dynamics of clupeiform fish populations such as anchovy are frequently impacted by environmental variations which can affect the success of the species recruitment. Herein, we have analyzed recent otolith growth rate, RNA/DNA nutritional condition index (sRD), and mortality rate of argentine anchovy larvae Engraulis anchoita from three different nursery areas in the Southwest Atlantic. We have evaluated the relationship between the environmental variables (abundance of copepod nauplii, temperature, chlorophyll‐a concentration, and abundance of E. anchoita larvae) and larval endogenous variables (size, weight, age, and otolith radius) to sRD and recent growth rate. Fast larval growth rates were observed toward the northern sector of the studied area, characterized by higher temperature. High values of sRD were associated with higher nauplii abundance in the proximity of coastal fronts. The larvae with the lowest growths and lowest minimum values of nutritional condition coincided with the area where there was less abundance of nauplii and higher larval mortality. Larval size and nauplii abundance were positive explanatory factors for both recent growth rate and sRD index. Temperature had a positive effect on recent growth rate and a negative effect on sRD index. This condition index was poorly explained in terms of model fit in comparison with the growth model. The results herein provided could be significant to better understand the recruitment of the species, as to determining favorable areas for the growth and survival of anchovy larvae.     

An example of meso‐scale hydrographic features in the central Baltic Sea and their influence on the distribution and vertical migration of sprat,Sprattus sprattus balticus (Schn.)

A wind‐driven meso‐scale pattern of temperature, salinity and oxygen was found along a transect in the northern Bornholm Basin (southern Baltic Sea). Strong winds caused currents along this transect, which shifted cold intermediate water (minimum: 3.6°C) towards the south. The transect was surveyed with a towed CTD‐system and hydroacoustics in parallel to investigate the distribution of sprat, Sprattus sprattus balticus (Schn.) in relation to the observed meso‐scale pattern. In those parts of the transect where the cold intermediate water was observed, sprat were restricted to water layers below the halocline. In other parts of the transect, sprat moved into higher water layers and occupied a wider depth range. The important factor was temperature, which set an upper limit to the vertical sprat distribution. The development of hydrography, as measured in the field, was evaluated with a hydrodynamic model.     

Importance of the Shatsky Rise Area in the Kuroshio Extension as an offshore nursery ground for Japanese anchovy (Engraulis japonicus) and sardine (Sardinops melanostictus)

Recent findings suggest that recruitment of Japanese anchovy (Engraulis japonicus) and sardine (Sardinops melanostictus) depends on survival during not only the first feeding larval stage in the Japanese coastal waters and the Kuroshio front but also during the post‐larval and juvenile stages in the Kuroshio Extension. Spatial distributions of juvenile anchovy and sardine around the Shatsky Rise area in the Kuroshio Extension region and the Kuroshio–Oyashio transition region are described, based on a field survey in the late spring using a newly developed mid‐water trawl for sampling juveniles. All stages of anchovy from post‐larvae to juveniles were obtained in the northern Shatsky Rise area. The Kuroshio Extension bifurcates west of the Shatsky Rise area and eddies are generated, leading to higher chlorophyll concentrations than in the surrounding regions in April and May. When Japanese anchovy and sardine spawn near the Kuroshio front or the coastal waters south‐east of Japan, their larvae are transported by the Kuroshio Extension and are retained in the Shatsky Rise area, which forms an important offshore nursery ground, especially during periods of high stock abundance.