Understanding the flow of energy from prey to predators gives insight into ecosystem production and functioning in that the energy available at the lowest trophic levels limits potential production at higher trophic levels (Paine, 1972). The energetic content of prey species themselves is also likely to vary based on seasonality, sex, ontogeny, and other factors. Together with trophic efficiency, based on energy loss as it transfers up trophic levels, these fundamental parameters mediate the proportion of that energy that ultimately supports predator populations and thus overall food web structure and productivity (Eddy et al., 2021). Despite the importance of these fundamental data, the energy content of prey species (primary and secondary consumers) remains poorly understood, particularly in marine ecosystems that are undergoing rapid environmental change. It is well established that energy density within food webs is influenced by environmental conditions. In the North Pacific, for example, the marine heatwave in 2015 and 2016 resulted in smaller krill (Robertson and Bjorkstedt, 2020), which may lead to lower energetic quality. Similarly, the 2015-2016 heatwave caused a decline in nutritional quality of Pacific sand lance (Ammodytes personatus), a forage fish species, in Prince William Sound, Alaska (Von Biela et al., 2019).

The California Current Large Marine Ecosystem (CCLME) is a highly productive ecosystem along the west coast of North America where wind-driven, coastal upwelling brings nutrient-rich deep waters to the surface. These physical forcings in the spring underlie strong primary production in the late spring and summer, which are the basis for a rich and biodiverse ecosystem (Checkley and Barth, 2009). The CCLME supports commercial fisheries and a robust ecotourism industry focused on resident and migratory predators, including fish, seabirds, and marine mammals, all of which rely on the prey from this ecosystem. Several studies have reported the energy densities of similar species in other ecosystems (Mr°rtensson et al., 1996; Davis et al., 1998; Abraham and Sydeman, 2006; Tirelli et al., 2006; Dubreuil and Petitgas, 2009; Färber-Lorda et al., 2009; Sánchez et al., 2013; Albo-Puigserver et al., 2017; Chenowith, 2018); however, there has been little published work on important prey species in the CCLME. Without these data it is challenging to develop bioenergetic models for this ecosystem (Dawson et al., 2020; Lawson et al., 2021).

Euphausiids (Euphausia pacifica and Thysanoessa spinifera; hereafter ‘krill’), northern anchovy (Engraulis mordax; hereafter ‘anchovy’), Pacific sardine (Sardinops sagax; hereafter ‘sardine’), and market squid (Doryteuthis opalescens) are fundamental prey for predators including large fish, seabirds, and marine mammals throughout the CCLME (Szoboszlai et al., 2015). In addition, krill are key prey for anchovy, sardine, and market squid. Several predators in the CCLME specialize in krill including Cassin’s auklet (Ptychoramphus aleuticus) and blue whale (Balaenoptera musculus); krill are also important prey for several species targeted by regional commercial and recreational fisheries, including Chinook salmon (Oncorhynchus tshawytscha) and anchovy (Miller et al., 2010). Forage fish, such as anchovy and sardine, are vital mid-trophic links between the base of the food web and top predators. Furthermore, the recent cultural history of some regions of the CCLME, like Monterey Bay, is inextricably linked to these forage fish and the canneries that operated in the 20^th-century to harvest them (Palumbi and Sotka, 2011). Market squid comprise Monterey Bay’s largest modern fishery by landings and are important mesopelagic prey for various predatory fish, toothed whales, and seabirds (Vojkovich, 1998; Szoboszlai et al., 2015; Wells et al., 2017; Thompson et al., 2019). Here, we measured the energetic content of krill, anchovy, sardine, and market squid from late spring through early fall in the CCLME. A better understanding of the energetics of these key prey species will provide useful data for fisheries, ecosystem ecology, and understanding responses of foodwebs in the CCLME to environmental change.

Overall, anchovy E_W was 7.85 (1.62) kJ g^-1, ahead of sardine 6.66 (1.75) kJ g^-1, squid 4.85 (0.83) kJ g^-1, and krill 4.22 (1.64) kJ g^-1 ( Figure 4 ). Anchovy has a significantly greater energy density than sardine (E_W t-value = -9.76, P< 0.001; E_D t-value = -19.78, P< 0.001) and squid (E_W t-value = - -27.18, P< 0.001; E_D t-value = -38.95, P< 0.001). Krill had the lowest energy density, less than squid, though the mean difference was< 0.5 kJ g^-1(E_W t-value = -14.76, P< 0.001; E_D t-value = -23.72, P< 0.001).

Market squid showed the lowest variation in energy density, whereas the greatest variation was found in sardine ( Figure 4 ). Sardine and anchovy reported comparable amounts of water content which tended to be lower than either krill or squid. Ash content was highest in krill and lowest in squid with sardine and anchovy ash contents being comparable. There were no significant relationships for squid energy density (E_W) in relation to size (length: t-value = -1.69, P = 0.09; weight: t-value = -0.16, P = 0.87; Figure 5 ). The same was true of sardine (length: t-value = 0.41, P = 0.73; weight: t-value = 0.53, P = 0.60; Figure 5 ). Anchovy energy density showed a positive relationship with weight (t-value 5.12, P< 0.001), but no relationship with length (t-value = 1.75, P = 0.08; Figure 5 ). Energy density in krill showed a strong positive relationship for both length and weight (krill length: t-value = 5.88, P< 0.001; weight: t-value = -4.64, P< 0.001; Figure 5 ). Sufficient samples were available to test anchovy, sardine, and squid for energetic phenology from across seasons. For all three, energy densities increased significantly from late spring (May) to summer and early fall (June – September; anchovy: F-statistic = 14.65, P< 0.001; sardine: F-statistic = 26.86, P< 0.001; squid: F-statistic = 21.06, P< 0.001 Figure 6 ).

Here, we report energy densities for four key prey groups in the CCLME collected from late spring to early fall. Overall, we find that forage fish are more energy dense than krill or squid ( Figure 4 ). While these results are generally consistent with other studies for similar species, there are some notable discrepancies ( Table 3 ). For example, our values for anchovy are higher than other values reported in the literature ( Table 3 ). The overall lack of these fundamental data for these forage species in the primary literature is striking, especially considering their abundance and importance to the well-studied CCLME.

Within species, we found notable differences across seasons for certain groups. Specifically, we observed an increase in energy densities of forage fish and squid species from late spring (May) to the summer and early fall (June-September; Figure 6 ). This trend corresponds with the phenology of the ecosystem. During the early spring, upwelling winds drive high primary productivity, which persists throughout the spring and early summer months bolstering phytoplankton blooms that support primary consumers such as larval fish and krill, which subsequently support production at higher trophic levels (Cross et al., 2005; Checkley and Barth, 2009). As krill are a primary prey for other species in this study, increases in anchovy, sardine, and market squid energy densities from the spring to fall may reflect both increasing krill abundance (Cross et al., 2005) and lipid reserves, as has been found in the Oregon and Washington populations (Fisher et al., 2020). Other work has also uncovered seasonal variability in anchovy and sardine energy densities related to ecosystem phenology (Gatti et al., 2018; Albo-Puigserver et al., 2020), though the effects ontogeny and differences in reproductive energy allocation strategies were also significant. These dynamics in the energy densities of fish, squid, and crustaceans have important ecological implications for higher trophic level predators. For example, the temporal patterns we find help explain why highly mobile predators, including seabirds, marine mammals, and predatory fish, aggregate in CCLME in the greatest numbers when their prey is abundant and most energy rich, during the summer and fall (Cross et al., 2005; Block et al., 2011), and spatial and temporal variability in their reproductive success (Warzybok et al., 2018).

For krill, our temporal sampling was too limited to test for differences in energy density related to season; however, changes in krill lipid reserves, likely reflecting energy density, related to phenology has been demonstrated in Oregon and Washington (Fisher et al., 2020). These dynamics many have important ecosystem implications. For example, recording krill energetic density before, during, and after blue whales arrive in Monterey Bay may shed light on how this species modulates the timing of their migration to and from the region (Abrahms et al., 2019; Oestreich et al., 2022). We demonstrated a strong positive relationship between size (both length and weight) and krill energy density ( Figure 5 ). Similar findings have been reported for Antarctic krill (Färber-Lorda et al., 2009), but not yet for krill in the eastern North Pacific. This result has important ecological implications, particularly given the emerging evidence that warm oceans, such as those in the CCLME during recent marine heatwaves, are associated with smaller sized krill for both krill species examined in our study (Robertson and Bjorkstedt, 2020; Killeen et al., 2022). The role of size, along with life stage, sex and species-specific (Färber-Lorda et al., 2009; Fisher et al., 2020), energy densities in mediating these shifts in krill structure is currently unknown and highlights the need to study the bioenergetics of krill, and other species such as forage fish and squid (Cross et al., 2005) that represent important links in marine food webs. Resolving how prey energy density varies in response to climate change and extreme climate events, such as marine heatwaves, could guide understanding and management of ecosystem health and resilience (Dawson et al., 2020). These results come at a critical time for the CCLME that is experiencing a rapid increase in cumulative anthropogenic stressors in recent decades (Calambokidis et al., 2019; Santora et al., 2020; Bograd et al., 2023).

While our study suggests that factors such as seasonality and size play an important role in explaining differences in energy densities, it is also important to consider other aspects that may influence the observed variation within and among groups. For instance, in our study we were unable to account for known sex-specific differences in energy density in krill, anchovy and sardine, which vary with ontogeny (Färber-Lorda et al., 2009; Gatti et al., 2018; Albo-Puigserver et al., 2020) nor potential differences in seasonal energy density between Euphausia pacifica and Thysanoessa spinifera (Fisher et al., 2020). Reproductive cycles may play an important role in mediating energy density in mature individuals of both fish species independent of size, particularly anchovy which are known to exhibit a capital breeding strategy (McBride et al., 2015), accumulating fat in the spring through summer which is utilized for reproduction in the winter (Hunter and Leong, 1981). In addition, the observed variation in water content within sardine, which corresponded with variation in energy density, have been demonstrated elsewhere for sardine and other fish species (Wuenschel et al., 2006; Gatti et al., 2018) highlighting the importance of accounting for ontogeny or other physiological factors. Future studies should aim to account for these potential confounding factors to gain a more complete understanding of the drivers of energy density variation in marine prey species.

Nevertheless, our study outlines foundational understanding of the ecosystem energetics of the CCLME with potential implications for predicting how the environment will affect species and trophic dynamics in the region (Wells et al., 2017; Dawson et al., 2020; Lawson et al., 2021). By shedding light on the drivers of energy density variation among marine prey species, this work may ultimately inform our understanding of higher trophic level predator ecology, such as migration timing, foraging location, and reproductive success. Overall, our findings provide valuable insights into the energy content of CCLME prey species, which could prove instrumental in forecasting how this ecosystem will respond to future environmental change.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://github.com/mssavoca/CCE_preyspp_energetics.

Ethical approval was not required for the study involving animals in accordance with the local legislation and institutional requirements because samples were collected as part of commerical fishing operations or as part of NOAA cruises under State of California – Department of Fish and Wildlife SCIENTIFIC COLLECTING PERMIT S-210680001-21162-002.

SP: Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing. MS: Conceptualization, Data curation, Formal analysis, Methodology, Project administration, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. MK: Conceptualization, Data curation, Investigation, Methodology, Project administration, Supervision, Writing – review & editing. MC: Data curation, Software, Supervision, Validation, Writing – review & editing. DM: Data curation, Investigation, Resources, Writing – review & editing. SL: Methodology, Writing – review & editing. DC: Data curation, Project administration, Writing – review & editing. JG: Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Writing – review & editing.