OCEAN SCIENCE

scientific report JANUARY 2013 The State of the Science: Forage Fish in the California Current . Executive Summary

In the California Current (CC), a diverse Ecosystem-based fisheries management group of forage fishes play an important (EBFM), which focuses on the role of fish- and often underappreciated role in the eries in the context of an overall ecosystem “middle” of the food web. These spe- rather than on single species, has been cies, such as Pacific sardine and north- proposed as a way to, among other things, ern anchovy, eat plankton and support emphasize the role of forage fish in the predators such as whales, sea lions, seabirds, ecosystem and consider catch on a second- sharks, salmon, and tuna. The availabil- ary basis. Some federal and state agencies ity—abundance, size, timing, and location are starting to implement EBFM, although —of forage fish has been shown to affect movements are slow. Complementary predators with declines in productivity approaches include precautionary manage- and survival when availability decreases. ment, fisheries closures, and forage reserves Meanwhile, fisheries targeting forage fishes for predators, which may be tailored to may indirectly or directly compete with predator needs in terms of prey diversity, predator needs. Although some forage fish abundance, distribution, size, seasonality, are consumed by humans, many are used and/or interannual variability. for nonfood products such as animal feed, pet food, and fishing bait. There is economic and ecosystem research that indicates leaving more forage fish in the Forage fish populations are influenced by environment to support predator fisheries environmental variation, natural processes, may be more valuable than removing them and human activities such as fishing, coastal in forage fisheries. In upwelling systems like development, and pollution. They are also the CC, forage fish may be more valuable subject to natural population cycles. These as prey than as catch. factors are not always well-understood and are difficult to incorporate into most man- Several large-scale studies have also agement approaches. recently suggested thresholds of forage fish biomass that should remain in the ocean Many forage fisheries are not managed, for predators. Under the increasing array and of those that are, management rarely of threats to forage fish, efforts should be considers such factors as predator needs made to control those factors that we can, and environmental fluctuations. Traditional such as fishing, to enable the maximum fisheries management based on maximum resilience possible to factors that we cannot sustainable yield, or the largest catch that easily control, such as climate change. This can be taken from a species’ stock over an approach is important for the health of indefinite period, is not appropriate for prey forage fish stocks themselves as well as the populations like forage fish because it does predators that rely on those fish. not account for the larger role they play in ecosystems.

2 PEW OCEAN SCIENCE: SCIENTIFIC REPORT Introduction

The California Current, which runs from factors dictating forage availability, many ecosystem functioning (Trites et al. 1997, Baja California in Mexico to Canada’s types of forage fishes are necessary to Coll et al. 2008). Many forage fisheries are British Columbia, may be the world’s most sustain important predators such as salmon not managed, and of those that are, the storied sliver of ocean. In the early 1940s, and seabirds that rely on them (Thayer and larger forage community, predator needs, sardine boats out of Monterey, California Sydeman 2009, Daly et al). or environmental fluctuations are rarely hauled in 700,000 tons a year and provided taken into account. This is despite concerns the backdrop for John Steinbeck’s nostalgic Fisheries targeting forage fish may compete researchers have raised about the effects Cannery Row. The Pacific sardine fishery with predators, either directly for the same of fishing on seabirds (Jahncke et al. 2004, subsequently suffered a spectacular crash fish or indirectly by altering food webs and Fredericksen et al. 2008, Pichegru by the late 1940s.

Globally, forage fishes are some of the most abundant and well-known in the world, including species like sardine and anchovy, but also many other important, though less well-known, species. Forage fishes play an important role in marine food webs, occupy- ing the “middle” of the food web (Figure 1); they largely eat plankton, and are in turn eaten by larger predators. Forage species can also include invertebrates such as squid and krill and juveniles of some predatory fish such as rockfish. Although there are various ways to define forage species, for this document, we consider small open- ocean schooling fish that remain at the same level in the food web for their entire life cycle, and due to their size and abun- dance are important as forage during their adult life-phase.

Forage fishes often undergo population cycles, the most famous of which is the decadal-scale fluctuations, or ‘boom- bust’ cycling, of sardine and anchovy (Schwartzlose et al. 1999, Chavez et al. 2003). For this reason, as well as other

Figure 1. Forage fish play an important role in marine food webs, occupying the “middle” of the food web. They largely eat plankton and in turn support a diverse group of predators, including commercially important species like salmon and tuna.

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 3 et al. 2010), pinnipeds (DeMaster et al. 2001, Matthiopoulos et al. 2008), and cetaceans (Constable et al. 2000, Bearzi et al. 2008). Recent studies have suggested forage thresholds needed to sustain preda- tors that would necessitate reductions in current levels of fi shing (Smith et al. 2011, Cury et al. 2011, Pikitch et al. 2012).

the role of forAge fish in the cAliforniA cUrrent

The California Current (Figure 2) is characterized by a narrow continental shelf with a steep slope, along which the main current fl ows and across which winds cause coastal upwelling (Figure 3), particu- larly important near capes and headlands (Chavez et al. 2002, Checkley and Barth 2009). Interannually, the timing of upwelling is variable but generally strongest during the spring and summer, leading to nutrient enrichment and cool temperatures in the ocean’s surface layer as water rises from the depths (Chavez et al. 2002, Bograd et al. 2009). High nutrient levels fuel plank- ton photosynthesis and growth, providing the base for the food web. The eff ect of upwelling is altered during El Niño Southern Oscillation (ENSO) events when the ocean surface mixed layer deepens, leading to warm, nutrient-poor surface waters and an infl ux of subtropical or tropical species (Chavez et al. 2002). There are also longer- term ocean fl uctuations driving marine pro- ductivity, represented by the warm or cool phases of the Pacifi c Decadal Oscillation (PDO) (Mantua and Hare 2002, Checkley and Barth 2009).

There are many forage fi shes in the CC, including the northern anchovy (Engraulis mordax; see anchovy case study), Pacifi c sardine (Sardinops sagax; see sardine case study), Pacifi c herring (Clupea pallasii; see

figure 2. The California Current (CC) spans temperate waters from Baja California to British Columbia.

4 PEW OCEAN SCIENCE: SCIENTIFIC REPORT herring case study), Pacifi c saury (Cololabis much is still unknown about mechanisms Prey availability refers to not only forage saira), lanternfi sh (Myctophidae), Pacifi c driving population dynamics and the extent abundance, but also size classes, timing, sandlance (Ammodytes hexapterus), and to which predators depend on them. In part and geographic considerations that may smelt (Osmeridae; see smelt case study), this is due to sampling diffi culties and the determine predators’ ability to fi nd and along with many other less-well-known considerable seasonal and year-to-year consume prey. Salmon, for example, rely on species. These forage fi shes support a variability of these species. diff erent forage fi shes—including anchovy, diverse predator assemblage of whales and sardine, herring, sandlance, and smelt—at dolphins, seals and sea lions, seabirds and Availability of forage fi shes has been diff erent times of the year and at various sea turtles, sharks and rays, and large fi shes shown to directly aff ect marine predators. stages of their life cycle (Daly et al. 2009, such as salmon and tuna. Some forage For instance, prey availability infl uences dis- Merkel 1957). Salmon have prey size limita- fi shes occur throughout the CC, while tribution, diet, foraging behavior, off spring tions as small smolts entering the ocean, others are more important in the north growth, breeding success, adult body condi- yet this may be one of the most important (e.g., sandlance in Washington) or south tion and survival, and population change in periods determining young salmons’ survival (e.g., grunion in Southern California). Some seabirds (Anderson et al. 1982, Rindorf et al. (Koslow et al. 2002, Logerwell et al. 2003, other ecosystems, such as the Humboldt 2000, Jahncke et al. 2004, Davis et al. 2005, MacFarlane 2010). Seasonal availability of Current off Peru, are dominated by a few or Crawford et al. 2006, Crawford et al. 2007, forage may also be key for other predators even just one forage fi sh species and have a Piatt et al. 2007, Thayer and Sydeman 2007, (Willson and Womble 2006); herring has mid-food web bottleneck, or “wasp-waist,” Frederiksen et al. 2008, Field et al. 2010, been found to occur in 90 percent of Steller structure (see Cury et al. 2000). The degree Pichegru et al. 2010) and marine mammals sea lions’ diet at certain locations during of forage diversity in the CC arguably (Kieckhefer 1992, Aguilar 2000, Jaquet et the herring spawning period (Womble and precludes such a structure, although sardine al. 2003, Soto et al. 2004, Soto et al. 2006, Sigler 2006). Migration of surf scoters par- and anchovy are dominant species. Womble et al. 2005, Womble and Sigler allels the northward progression of herring 2006, Hlista et al. 2009, Sigler et al. 2009, spawning events along the West Coast Although little is known about many of the Winter et al. 2009, Patrician and Kenney (Lok et al. 2012). forage fi shes in the CC, some species such 2010, Miller et al. 2011). For salmon, prey as sardine and anchovy support commer- availability infl uences growth and survival Predator-prey mismatch, when the timing or cially important fi sheries and are managed (Brodeur 1991, Daly et al. 2009, Weitkamp spatial distribution of forage availability dif- and studied extensively. There is consider- and Sturdevant 2008). Tuna distributions fers from that of predator needs, is becom- ably less data on noncommercial species vary widely and track forage fi sh (Laurs et al. ing common with climate change (Bertram such as sandlance, smelt, and lanternfi sh. 1984, Polovina 1996, Kitagawa et al. 2007). et al. 2001, Edwards and Richardson 2004, Even for the more well-understood species, Durant et al. 2007, Sydeman and Bograd

figure 3. Upwelling occurs when wind drives cooler, dense, and nutrient-rich water towards winds the ocean surface, replacing the warmer surface water. Coastal upwelling in the CC is variable but generally strongest during the spring and summer, often leading to nutri- ent enrichment and cool temperatures in the ocean’s surface layer. High nutrient levels can fuel plankton growth.

continental shelf

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 5 2009, Watanuki et al. 2009, Dorman et al. Although some forage fish are consumed There are economic and ecosystem argu- 2011). Temporal examples include variation by humans, many are used for nonfood ments that favor leaving more forage fish in herring spawning initiation of more than products such as animal feed, pet food, in the environment to support predator fish- three months, leaving predators such as aquaculture, and bait for fishing. More eries versus removing them in forage fisher- Steller sea lions with fewer or lower-quality than 36 percent of the global fish catch ies. Sardines, for example, are valuable as prey options during the lean winter months is destined for nonfood uses (Tacon and food for commercially important predators or during spring, when preparing for breed- Metian 2009), and demand is increasing in the CC, particularly salmon. The eco- ing (Willson and Womble 2006). Localized (Naylor et al. 2000). The exact propor- system value of forage fish would increase depletion of forage fishes due to fishing is tions of forage fish usage in the CC are not with consideration of predator species also a concern (Tasker et al. 2000). Spatially, well-documented. such as seabirds and marine mammals that breeding seabirds, seals, and sea lions return are not exploited but have extraordinary to offspring at land-based colonies and thus Historically, most fish that could be caught aesthetic and ecotourism value (Hanneson have limited foraging ranges, during which were used as human food sources globally; et al. 2009, Hannesson and Herrick 2010). time localized prey depletions could be del- the reduction of fish to fishmeal and oil for Therefore, in upwelling systems such as the eterious (Croll and Tershy 1998, Wanless et indirect use is a relatively recent develop- CC, forage fish are generally more valuable al. 1998, Daunt et al. 2008, Wolf and Mangel ment. The fish oil industry began in the as support to other valuable fisheries than as 2008, Plagányi and Butterworth 2012). 19th century when seasonally abundant catch themselves (Pikitch et al. 2012). More research is needed in this area. catches of herring and sardines could not be absorbed by local markets in Europe Forage species richness is key in local and North America (Watson et al. 2006). Challenges for forage fish in marine communities. A diverse forage The oil was used for lubricating machinery, the California Current assemblage can provide the redundancy leather tanning, soap production, and other needed for prey-switching opportunities, nonfood products, and the byproducts of Environmental variability especially given variability in abundance, fish oil production were used as fertilizer. The CC has historically had large natural size, distribution, or time as discussed The production of fishmeal for animal feed fluctuations in oceanographic factors and above. Despite this, the specific forage began in the early 20th century, including related forage fish abundance (Baumgartner needs of top predators have not been from sardines in California (Watson et al. et al. 1992, Chavez et al. 2003). The bio- adequately addressed in management. 2006). logical mechanisms causing these popula- The diets of some dependent predators tion cycles are still unclear but probably have not been sufficiently studied, particu- Pacific sardine (see sardine case study) is are related to current flows, upwelling, larly if such studies are logistically challeng- currently one of the most lucrative fisheries and associated sea surface temperature ing, as is often the case for cetaceans (e.g., in California. It is also caught off the coasts (MacCall 2009). The cyclical pattern of Stroud et al. 1981). Nevertheless, there is of Oregon and Washington in significant abrupt changes in forage fish populations an abundance of predator-diet data avail- amounts (California Department of Fish suggests that the driver is a combination able for the CC (e.g., Sydeman et al. 2001, and Game [CDFG] 2012, Hill et al. 2010b). of several physical and ecological factors Dufault et al. 2009, Orr et al. 2011). However, sardine abundance may be (MacCall 2009). For example, anchovies declining (Wespestad and Maguire 2012, and sardines have long been considered Zwolinski and Demer 2012). The status of to ecologically replace each other as the Forage fisheries in the anchovy (see anchovy case study) popula- environment fluctuates. However, recent California Current tions is largely unknown, although limited research suggests that the ecological data suggest that populations of these mechanisms behind out-of-phase fluctua- The schooling behavior of forage fish fish are depressed (Brodeur et al. 2006, tions may be much more complex than a allows them to be easily caught, translat- Bjorkstedt et al. 2011, Fissel et al. 2011). simple replacement (Barange et al. 2009). ing into relatively low operating costs for fisheries and thus relatively cheap fish and Herring (see herring case study) also sup- Climate change fish products for consumers. Forage fish are port very high-value fisheries in the CC, Climate change is distinct from envi- caught within the exclusive economic zones much of it for roe destined for the Japanese ronmental variability in that it refers to (EEZ) of Canada, Mexico, and the United market. Herring populations, however, are changes in the mean and/or variability States, as well as in international waters out- also at a low level, probably due to a combi- of ecosystem properties (such as tem- side these EEZs. Forage fish are generally nation of human and environmental factors peratures and sea levels) that persist for targeted with “round-haul” gear including (Landis et al. 2004, CDFG 2012, Wespestad an extended period, typically decades or purse seines, drum seines, and lampara nets and Maguire 2012). longer (Intergovernmental Panel on Climate (Figure 4). These species are also taken Change [IPCC] 2007). Effects can be incidentally with trawls, gillnets, trammel seen on physical ocean processes and nets, trolls, pots, hook-and-line, and jigs. habitats, as well as on species interactions, including cycles of forage fish dynamics and predator responses.

6 PEW OCEAN SCIENCE: SCIENTIFIC REPORT Species interactions Incidence of nonnative species is increas- ing and can also have a powerful effect on coastal food webs and fundamentally alter fish distributions. For example, an introduced clam (Corbula amurensis) in the San Francisco Bay eliminated summer-long phytoplankton blooms starting in 1987, causing a shift in anchovy distribution out of the estuary that was a direct response to reduced food availability (Kimmerer 2006). A more pervasive example in the CC is the jumbo squid (Dosidicus gigas) from tropical waters, which has been observed in substan- tial numbers in the subtropical CC since the 1998 ENSO warm-water event (Pearcy 2002, Brodeur et al. 2006, Field et al. 2007). It is a voracious predator of many forage fishes such as anchovies and sardines (Field et al. 2007).

Fishing Improvements in fishing technology such as acoustics and modernized gear have increased the vulnerability of schooling forage fish (Beverton 1990). Furthermore, fishing makes fish populations more variable than would occur naturally and more susceptible to climate perturbations (Hsieh et al. 2006, Anderson et al. 2008). Susceptibility may increase because fish populations are less abundant, have trun- cated age structures (fewer older individu- als), or are depleted locally. The latter two factors are potentially just as important as abundance in maintaining long-term sustainable population levels (Berkeley et al. 2004, Anderson et al. 2008).

Sardines provide one example. At less than 5,000 tons (MacCall 1979), sardine abundance was probably lower after the 1960s population crash than at any time in the previous 2000 years, even during periods of natural low abundance, which were historically on the order of roughly Figure 4. Forage fish are generally 400,000 tons (Baumgartner et al. 1992; targeted with “round-haul” gear see sardine case study). Another example including purse seines (top), drum seines, comes from herring along the Pacific and lampara nets (bottom). coast, which are experiencing truncated age structure and localized depletions of subpopulations (Stick and Lindquist 2009, CDFG 2012; see herring case study). These changes may threaten the ability of the overall herring metapopulation to respond to harmful changes, because it has lost valu- able genetic and behavioral diversity. For

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 7 example, remaining subpopulations may be Forage fish management in well-understood (MacCall 2009). Fishing at a genetic disadvantage for certain types the California Current itself also increases populations’ susceptibil- of adaptation, may be more susceptible to ity to climate changes (Hsieh et al. 2006, disease or parasites, or may not have the Forage fishes are managed within the U.S. Anderson et al. 2008), yet management ability to shift spawning times to account EEZ, spanning the jurisdictions of federal response often lags behind these biophysi- for climate changes or spawning locations or state agencies and Native American cal changes. in response to local habitat degradation. tribes. Federally, the Coastal Pelagic Species These could compromise herring at a meta- Fishery Management Plan (CPS FMP) The “catchability” of forage fish may population level or even eventually render includes sardines and anchovies. The Pacific increase or remain constant even as a stock the metapopulation obsolete. The benefit Fishery Management Council (PFMC) declines rapidly, due to their schooling of diversity among subpopulations, which and the National Marine Fisheries Service nature and their vulnerability to modern allows some to persist in the face of change, (NMFS) have federal jurisdiction in the CC. fishing technology (Beverton 1990). Thus, is termed the “portfolio effect” (Berkeley declines in stock size may not be apparent et al. 2004, Anderson et al. 2008, Schindler Sardines are actively managed, meaning based on commonly used catch-per-unit- et al. 2010, Carlson and Satterthwaite 2011). landings and markets are substantial enough effort statistics. to warrant annual assessment of stock Coastal development status and fishery management. Anchovies Traditional fisheries management focuses Urban, industrial, agricultural, or are monitored only for potential elevation on maximum sustainable yield through time, aquaculture development may directly to active management, because they are yet this concept is not appropriate for prey degrade coastal habitat. This may have assumed to now be landed in low numbers. populations, for populations that undergo particularly negative influences on species Herring was recently added to the CPS natural cyclical fluctuations, or when that spawn in beach, intertidal, or subtidal FMP as a new designation, “ecosystem considering effects to other species in the areas (see smelt case study). Offshore component” species. While this designation ecosystem (Larkin 1977, Legovic et al. 2010, renewable energy and desalination projects initiates monitoring of herring as incidental Zwolinski and Demer 2012). High catch are also increasing rapidly off the West catch, there are still no federal restric- rates on short-lived species also mean that Coast. For example, desalination projects tions on fishing for ecosystem-component errors or uncertainty in setting catch rates may result in changes to local water flow species. Therefore, herring management can have particularly severe consequences and salinity levels, and entrainment of is left to the states of California, Oregon, (Pinsky et al. 2010). “Pretty good yield” has larvae, eggs, and plankton in pumps and and Washington. Except for species listed been recently suggested as an alternative turbines (San Francisco Bay Conservation under the Endangered Species Act (e.g., and is defined as 80 percent of maximum and Development Commission 2005). the threatened smelt species eulachon sustained yield (Hilborn 2010), although this [Thaleichthys pacificus]), most forage fishes still does not account for any interactions Pollution in the CC are not federally or even actively with other species. Oil spills, ocean dumping, industrial managed at the state level. Examples discharge, and other chemical pollution are include most smelts, sandlance, lantern- Natural mortality (e.g., predation, dis- continuing threats for fisheries (Colodey fishes, saury, and others. ease, starvation) is notoriously difficult to and Wells 1992, Sindermann 1996, Carls estimate reliably; yet inaccurate natural et al. 1999, Landis et al. 2004, Incardona Challenges of forage fish management mortality rates may result in very mislead- et al. 2012; see herring case study). Increases Traditional stock assessment techniques ing estimates of stock status provided in runoff are anticipated due to expanding are often used with the forage fish that to managers (Vetter 1998, Lee et al. human populations, coastal development, are managed in the CC; however, these 2011). Specifically, traditional assessment and agriculture. Noise pollution could also assessments do not perform well for pelagic approaches that underestimate the magni- be a problem; trauma from high-intensity, forage fish. For example, basic management tude and dynamic nature of natural mortal- low-frequency sounds has been observed information, such as reliable estimates of ity for forage fishes lead to biomass and recently in cephalopods (André et al. 2011) population size, is not available for most yield projections that are overly optimistic and in fish (McCauley et al. 2003). forage fishes, even species with active fish- (Tyrrell et al. 2011). Moreover, different eries. In addition, most fisheries manage- survey methods result in size selectivity Together, these influences may threaten the ment focuses on individual species and does of forage fish, or bias towards certain size whole forage base (all species combined) not consider multiple species simultane- classes, that is difficult to establish and can or just specific species, cause widespread or ously, which is problematic given the critical introduce additional error into stock assess- local effects. They could increase variation ecological role of forage fish as prey. ments (see Hill et al. 2010a). Finally, preda- in forage fish dynamics, by further reducing tor needs are not adequately addressed population numbers, diversity, and the abil- Furthermore, populations of short-lived in most current management scenarios ity of fish to withstand harm. forage fish can grow or decline quickly in (Pikitch et al. 2004, Tyrrell et al. 2010). response to climatic shifts, but mecha- nisms driving these dynamics are not

8 PEW OCEAN SCIENCE: SCIENTIFIC REPORT cAse stUDY: northern AnchoVY Engraulis mordax

Anchovies consist of two subspecies in 1981, Emmett et al. 1997). Other data the CC: Engraulis mordax mordax, which sources also suggest that these anchovy ranges from British Columbia to Baja populations remain low (Brodeur et al. California and was recently also found 2006, Bjorkstedt et al. 2011). in the Gulf of California; and E.mordax nanus, which is found in the bays of Despite limited information, commer- California. Usually seen in coastal waters cial catch in the CC increased in the within about 18 miles (30 kilometers) mid-2000s (PFMC 2010). Furthermore, from shore, anchovies form large, tightly catch outside of commercial fi sheries is packed schools. E. mordax mordax is poorly documented and underreported divided into northern, central, and south- (PFMC 2010). In 2005, for example, ern subpopulations. The central sub- anchovy mortality from bycatch, live bait, population was once the focus of large, recreational, incidental, and international commercial fi sheries in the U.S. and fi sheries totaled at minimum more than Mexico. Most of this subpopulation is 65 percent of commercial U.S. landings located in the Southern California Bight. (California, Oregon, and Washington Those found north of Cape Mendocino, [calculated from PFMC 2010]). California, are considered the northern stock, and the southern stock is found Anchovies are of high importance to entirely in Mexican waters. predators due their relatively small size, inshore distributions, and almost year- Anchovies have the ability to spawn round availability. More than 50 predator throughout the year. In California, peak species in the CC consume anchovies, spawning occurs from February to April including important commercial and and in Washington from mid-June to recreational species. The seasonal diet rAnge mid-August (Hunter and Macewicz 1980, of Chinook salmon, for example, can be high concentrAtion rAnge Laroche and Richardson 1980). The last as much as 90 percent anchovy in some comprehensive stock estimates for the years (Merkel 1957). central subpopulation were made in 1995, after population declines and the down- Increases in commercial and other land- turn of the fi shery (Jacobson et al. 1995). ings despite 15 years of low anchovy Recent population estimates, although productivity and high dependence of limited by available data types and survey predators could put the anchovy stock, and analysis methods (see Jacobson valuable predators, and the larger ecosys- et al. 1994, Fissel et al. 2011, Simmonds tem at risk.  2011), indicate a generally depressed anchovy population (Fissel et al. 2011). Only two scientifi c assessments have been completed for the northern stock, the second of which suggests there was a signifi cant decline by 1995 (Richardson

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 9 cAse stUDY: pAcific sArDine Sardinops sagax

When the population of Pacifi c sardines roughly 500,000 tons in 2010 (Hill et al. is large, this fi sh is abundant from the tip 2010b), with renewed fears of a popula- of Mexico’s Baja California to southeast- tion crash (Zwolinski and Demer 2012). ern Alaska and throughout the Gulf of California. There are three Pacifi c sardine The sardine fi shery has been federally subpopulations in the CC with spawn- regulated since 2000. Some manage- ing centers in the Gulf of California, ment measures are relatively progressive, Baja California inshore and southern to such as an environmental harvest-control central California off shore (Smith 2005, rule, although there are opportunities to Hill et al. 2010b). The central California further improve management (Jacobson subpopulation is most relevant to the et al. 2001, Smith et al. 2005, Emmett et CC as a whole. This population spawns al. 2005, Hill et al. 2010b, McClatchie from January to June, and larger adults et al. 2010, PFMC 2010, Zwolinski migrate in the spring to Washington and and Demer 2012). For example, within British Columbia. the U.S. EEZ, sardines are caught by commercial, live bait, and recreational Sardine populations naturally fl uctuate fi sheries in California, Oregon, and in abundance roughly every 50 years Washington. Sardines are also taken as (Baumgartner et al. 1992), driven mainly incidental catch in the Pacifi c mackerel, by large-scale climate fl uctuations squid, and anchovy fi sheries. The federal (Chavez et al. 2003, MacCall 2009), but harvest quota for sardine includes set- these natural up and downs in population asides for research, incidental catch, and are also exacerbated by fi shing pressure management uncertainty. The set-aside (MacCall 2009, Zwolinski and Demer for incidental catch (3,000 tons) does not 2012). Geologic records of fi sh scales appear to have been exceeded recently rAnge deposited in the Southern California in squid, anchovy or Pacifi c mack- high concentrAtion rAnge Bight indicate that unfi shed sardine erel fi sheries (PFMC 2010); however, populations fl uctuated naturally between there are no set-asides for live bait and a low of 400,000 tons to many millions of recreational fi sheries. California live bait fi sh populations spanning international tons (up to 16 million tons [Baumgartner fi sheries alone regularly exceeded 3,000 boundaries. Furthermore, overfi shing et al. 1992] ). In the 1930s and 1940s, tons annually in the past decade (PFMC measures specifi ed in the CPS FMP sardines were the largest single-species 2010). Thus the cumulative human were not implemented, despite the fact fi shery in the Western Hemisphere and removal of sardines from the ecosystem that this occurred during the recent were largely unregulated (Zwolinski and is not fully addressed in the commercial sardine population decline. Demer 2012). The population went from harvest quota. more than 3 million tons in the 1930s Many predators rely on sardines, includ- to less than 5,000 tons in the 1960s Beyond the U.S. EEZ, sardines are ing Chinook and coho salmon, Pacifi c (MacCall 1979). Sardine biomass did not caught in Mexican and Canadian fi sher- hake, and jack mackerel (Merkel 1957, increase again until the 1980s and 1990s, ies. International catch pushed total Emmett et al. 2005). Seabirds, seals, sea and the fi shery resumed; biomass peaked sardine harvest above the federal over- lions, whales, dolphins, and sharks also at more than 1.5 million tons in 2000 and fi shing limit in 2009 (Hill et al. 2010b), forage extensively for sardines (Baltz and has subsequently trended downward to highlighting the diffi culty of managing Morejohn 1977, Stroud et al. 1981,

10 PEW OCEAN SCIENCE: SCIENTIFIC REPORT cAse stUDY: smelt Osmeridae

Velarde et al. 1994, Clapham et al. The “true” smelts (Osmeridae) are particularly important forage for preda- 1997, Emmett et al. 2005, Becker and several species of small silvery fi sh, tors in the central to northern CC. Beissinger 2006, Weise and Harvey including whitebait smelt, surf smelt, 2008). California sea lions alone, for night smelt, longfi n smelt, and eula- Commercial and recreational fi sher- example, may consume the equivalent chon. Smelt are common year-round ies occur on surf smelt populations at of roughly 10 percent of total sardine residents in many nearshore areas from many sites throughout Oregon and biomass in central California (Weise and California to Alaska; however, their full Washington (Bargmann 1998). Adequate Harvey 2008). Federal sardine manage- ranges are not well-documented. They fi shery statistics are lacking for smelts, ment for the U.S. West Coast includes are relatively small, short-lived fi sh, in spite of their ecologically data-poor a harvest cut-off of 150,000 tons, which reaching about 8 to 12 inches (20 to 30 status and local importance. Recreational theoretically includes stock for potential centimeters) in length and surviving for catch may actually exceed that of com- rebuilding at low population sizes, as well three to fi ve years. Some smelt have mercial catch in some instances, perhaps as sardines as forage for dependent pred- an entirely marine/estuarine life history because unlike most other forage fi sh ators (PFMC 2010) for each year under (surf, whitebait, night smelt), while others species, most smelt are used for human all environmental conditions. Further (such as eulachon and longfi n smelt) are consumption (Bargmann 1998).  synthesis of CC predator forage require- anadromous. Eulachon is federally listed ments is much needed to determine the as threatened under the Endangered adequacy of this threshold, given the Species Act, and there is an active peti- importance of sardines as forage. tion to list longfi n smelt.

There are very few fi sheries stock assess- Data on smelt life history and particular ments or harvest policies that incorporate stocks are largely lacking. There are any measure of environmental variability currently no population size estimates (except see Schirripa et al. 2009). The for most smelt species, including white- sardine federal harvest policy is relatively bait and surf smelt, although these are unique because a proxy for environmen- among the dominant pelagic schooling tal variability, a three-year average of fi shes caught in research surveys in the sea surface temperature at the Scripps Oregon-Washington region (Brodeur Institution of Oceanography pier in et al. 2003). Environmental infl uences La Jolla, California, is used as one have been demonstrated for whitebait parameter in the formula for establish- smelt in Oregon. For example, poor body ing the harvest quota (Hill et al. 2010b). condition is likely a result of poor ocean Although a recent study suggested conditions, such as reduced upwelling, problems with this specifi c approach that result in lower biomass and poor (McClatchie et al. 2010), environmental condition of zooplankton prey (Litz et factors are clearly important for sardine al. 2010). It is not known exactly where stocks. Thus, this general approach and when whitebait smelt spawn, but should continue to be pursued, even if the occurrence of larvae in estuaries the specifi cs need to be modifi ed. during fall suggests that they may be late summer spawners on subtidal banks (reviewed in Litz et al. 2010). Smelts are

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 11 cAse stUDY: pAcific herring Clupea pallesi

Pacifi c herring have long been exploited et al. 2012) presumably reducing already by humans and are consumed by natural depressed numbers (CDFG 2012). Other predators. Herring have been an historically large herring spawning popu- important resource for Native American lations in California, such as Tomales Bay, groups in the Pacifi c Northwest for are also signifi cantly reduced (Bartling centuries (Hourston and Haegele 1980, 2006). Gobalet and Jones 1995, Bargmann 1998). Commercial fi sheries have repeat- Some herring populations are distinct, edly sprung up and crashed along the not mixing with neighboring popula- U.S. West Coast. A small commercial tions due to geographic or behavioral sport bait fi shery in south Puget Sound diff erences such as varied spawning (Stick and Lindquist 2009) and small times. Where genetic diff erences have commercial roe, eggs on kelp, and fresh not been established, populations may herring fi sheries in San Francisco Bay demographically be characterized as a (CDFG 2012) are the only signifi cant meta-population. Understanding local fi sheries remaining. population structure, however, is essential for the preservation of spawning poten- Pacifi c herring are found throughout tial and genetic and life history diversity the coastal zone from northern Baja (Gustafson et al. 2006). California around the North Pacifi c Rim to Korea. They spawn between Pacifi c herring have been documented October and April in shallow parts of to live as long as 15 years, though few bays and inlets, preferably onto marine exceed 9 years (Ware 1985). While vegetation or subtidal rocks, but man- CC stocks included long-lived fi sh in made structures are also used. the 1970s, herring older than 4 or 5 are rAnge now rare, and the median age is 2 to 3 high concentrAtion rAnge Threats to herring in the CC include (Hershberger et al. 2005, Gustafson et al. large population declines due to climate 2006, Mitchell 2006, Stick and Lindquist and overexploitation, truncated age 2009, CDFG 2012). This change is structure, localized population deple- probably largely due to intense fi shing. tions, degraded spawning habitat, and Other factors include predation and oil and other chemical pollution increased rates of pathogenic infection (Zebdi and Collie 1995, Toresen and in older fi sh, which may contribute both Østvedt 2000, Landis et al. 2004, Stout directly and indirectly (through increased et al. 2001, Stick and Lindquist 2009, predation) to mortality (Hershberger CDFG 2012, Incardona et al. 2012, et al. 2002, Stick and Lindquist 2009). Wespestad and Maguire 2012). The Declining longevity may further harm spawning habitat of what was the largest herring populations, for example by Washington herring population, Cherry reducing the quantity and quality of Point in Puget Sound, is now centered in eggs (Hay 1985, Ware 1985), shortening an area of industrial activity and urban the spawning season and thus decreas- development (Stout et al. 2001). The ing the populations’ overall reproductive largest remaining California population, potential (Wright and Trippel 2009).  in urban San Francisco Bay, recently suff ered eff ects of an oil spill (Incardona

12 PEW OCEAN SCIENCE: SCIENTIFIC REPORT Improving forage fish management marine decadal regimes) and short-term synthesis of predator-forage requirements When assessing fish population status for (e.g., ENSO) fluctuations, as well as trend- utilizing a combination of these and other use in management decisions, the inclusion ing temperatures and increasing variability approaches will be useful. of ecological interactions is central to an associated with climate change (Field and ecosystem-based perspective. This is not Francis 2005, Curtin and Prellezo 2010, When determining catch levels for com- a new concept (e.g., May et al. 1979), yet Belgrano and Fowler 2011). Environmental mercial fisheries, insufficient attention is incorporating basic ecological processes effects, however, are also rarely incorpo- often paid to the total human removal of such as predation and competition into fish- rated into fish population assessments or forage fish from the ecosystem, both by eries stock assessments is still uncommon fisheries management decisions (except species and as a forage group. Such removal (Link 2002, Tyrrell et al. 2011). While there see Hill et al. 2010b, Schirripa et al. 2009; includes nontarget, or incidental, catch, are movements toward EBFM at the federal see sardine case study). EBFM should also bycatch, live bait fisheries, recreational fish- and state levels, they are nascent, slow, or consider risks to fish populations and the ing, and fishing outside the U.S. EEZ that implemented in a piecemeal fashion (Field ecosystem from human sources such as targets stocks spanning political boundaries and Francis 2005, Ruckelshaus et al. 2008, habitat destruction and pollution (Pikitch (Pikitch et al. 2004, Ruckelshaus et al. 2008, Halpern et al. 2010). Moreover, the degree et al. 2004, Curtin and Prellezo 2010; see PFMC 2010). Catch outside of commercial to which proposed fisheries ecosystem herring and smelt case studies). fisheries can be significant in some cases plans, one of the key approaches to imple- (Pikitch et al. 2004), although it is often menting EBFM, are enforceable is unclear. In addition to integrating predator effects poorly documented and underreported Regardless, a more ecosystem-centric man- into fish population assessments, EBFM in the CC (PFMC 2010; see sardine and agement approach by definition is holistic should take the needs of predators into anchovy case studies). Even after predator and includes multiple considerations. account in relation to degree of fishing needs have been considered, these other (Smith et al. 2011, Cury et al. 2011, Pikitch types of human removal further reduce the One important consideration in EBFM, et al. 2012). Approaches include precaution- amount of target forage fishes available for a precautionary management approach, ary management, fisheries closures, and commercial fisheries. emphasizes the role of forage fish in the forage reserves for predators, which may be ecosystem and considers catch secondarily. apportioned to predator needs in terms of Many tools to implement EBFM already This effectively shifts the “burden of proof” prey diversity, abundance, distribution, size, exist (Ruckelshaus et al. 2008, Lester et al. to show that a given fishing level is safe seasonality, and/or interannual variability 2010, Tyrrell et al. 2011, Pikitch et al. 2012). before allowing it. Such an approach is espe- due to climate or other factors. There are some data gaps, such as limited cially important in data-poor instances or in quantification of relationships between fish the face of scientific uncertainty (Pikitch Several large-scale studies have recently stocks (Hannesson and Herrick 2010), but et al. 2004, Curtin and Prellezo 2010). suggested thresholds of forage fish biomass modeling tools to address this issue exist that should remain in the ocean for preda- or are being developed (see Tyrrell et al. Time and/or spatial fisheries closures can tors. A report of the Lenfest Forage Fish 2011 and references therein). Other types protect spawning fish aggregations or Task Force (Pikitch et al. 2012) compared of data gaps or stock performance under hotspots of predators and prey, and, more one type of ecosystem model across many various conditions might be approximated generally, life history characteristics and systems globally and found that approxi- from other systems that are better studied biodiversity (Babcock et al. 2005, Field mately 80 percent of unfished forage fish (Dickey-Collas et al. 2010). A wealth of and Francis 2005, Hyrenbach et al. 2000, biomass should remain in the water to avoid predator diet data exists, although synthe- Ruckelshaus et al. 2008, Santora et al. a 50 percent reduction in any dependent sis of forage requirements would enable 2011). Limitations on fishery gear—such as predator population. A study, partially improved management of fishery resources allowable gear types, net length, and mesh funded by the Marine Stewardship Council in an ecosystem manner. size—are important in protecting habitat, (Smith et al. 2011), compared three types minimizing bycatch, and avoiding harvest- of ecosystem models across five systems. ing of fish before they reach full maturity Based on the study’s results, the authors (Belgrano and Fowler 2011). suggest leaving 75 percent of unfished forage fish biomass in the ocean to maintain The nature, strength, and changes in ecosystem function. Cury et al. (2011) used ecological processes, such as predation a different approach, numerical response and competition, influence single-species curves, in seven ecosystems to determine population dynamics as well as ecosystem the threshold of roughly 30 percent of the functioning (Field and Francis 2005, Tyrrell maximum long-term forage fish biomass et al. 2011). Environmental variation further below which seabirds experience consis- influences single-species dynamics and tently reduced and more variable productiv- interactions among species. Environmental ity. Each method has its advantages and effects include long-term (e.g., warm/cool difficulties, and additional analysis and

THE STATE OF THE SCIENCE: FORAGE FISH IN THE CALIFORNIA CURRENT 13 Summary

In the CC, sardines are the most heav- ily fished forage fish. Sardines are also relatively well-studied and progressively managed, yet there is still much unknown about their populations, and management could be improved, especially in regard to cumulative human removal from the eco- system, effects of fishing on age structure, West Coast-wide overfishing, the environ- mental harvest control rule, and quantitative predator needs. Even less is known and little management exists of other forage fishes, despite variable levels of fishing pressure and high importance to predators.

Recent scientific syntheses, although using different methodologies, reach similar con- clusions: forage fish management worldwide is important but insufficient (Smith et al. 2011, Cury et al. 2012, Pikitch et al. 2012). Under the increasing array of threats to forage fish, efforts should be made to control the factors we can, such as fishing, to enable the maximum resilience possible to factors that we can’t easily control, such as climate change. This approach is impor- tant for the health of forage fish stocks themselves as well as fostering continued species diversity and ecosystem functioning in the CC. Public and economic ramifica- tions of sustainable forage fish management are substantial, both for predators with no market value (such as seabirds, marine mammals, and threatened and endangered species) and those with considerable market value (such as commercial fisheries for salmon, tuna, and rockfish).

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The Pew Environment Group is the Scientific Contributors conservation arm of The Pew Charitable Trusts, a non-governmental organization Julie Thayer, Ph.D. William Sydeman, Ph.D. headquartered in the United States that Dr. Thayer has worked in the California Dr. Sydeman’s career spans nearly three applies a rigorous, analytical approach to Current marine ecosystem for the past 18 decades of ecological research. Starting improving public policy, informing the years. She did undergraduate work in marine as an intern marine ornithologist working public, and stimulating civic life. biology at the University of California, on the Farallon Islands in 1981, he spent Santa Cruz, and Long Marine Lab, and 15 years as the director of marine ecology 901 E Street NW, 10th Floor obtained a doctorate in marine ecology at PRBO Conservation Science before Washington, DC 20004 from the University of California, Davis. establishing the Farallon Institute Phone: 202.552.2000 Dr. Thayer has conducted research on a (faralloninstitute.org). Dr. Sydeman Email: [email protected] variety of top marine predators and their obtained his doctorate in ecology from Printed on 100% recycled paper. prey in relation to ocean climate. Recently the University of California, Davis. He has she organized a group of researchers from conducted a number of plankton-to-pred- www.PewEnvironment.org around the North Pacific Rim (Canada, ator studies in the California Current large Japan, United States) for a comparative marine ecosystem and has written about study of forage fish eaten by a seabird, seabirds, marine mammals, and various rhinoceros auklet, focusing on spatiotem- fish species. He serves on many scientific Cover photo: Two fishermen transfer poral synchronicity in connection with local panels, notably as the chair of the Advisory anchovies, Engraulis mordax, from a to basin-scale marine variability (Thayer et Panel for Marine Birds and Mammals for the commercial fishing boat hold to a live bait al. 2008). She has also led a collaborative North Pacific Marine Science Organization storage pen, San Francisco Bay, California. fisheries research project in which scientific and Scientific Advisory Committee for Abner Kingman/Getty data on the diet of salmon are collected implementation of the California’s Marine Illustrations: Steve Ravenscraft in partnership with local recreational and Life Protection Act. Dr. Sydeman has Maps: Adapted from maps by commercial fishers, synthesizing historical presented to state and federal policymakers GreenInfo Network data to help understand the recent salmon on the effects of climate change on marine Design: Imaginary Office population crash. ecosystems and how to best design and use the nation’s new ocean observing systems.

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