By Konstantine J. Rountos
Department of Biology, St. Joseph’s College, 155 Roe Blvd., Patchogue, NY 11772. E-mail: [email protected]
Forage species are often defined in scientific and popular literature using terms such as “small,” “schooling,” “short- lived,” pelagic fish found at intermediate trophic levels of marine food chains. However, not all stakeholders use the same combination of terms, and their definitions include an array of fish and invertebrates that range in size, life span, and habitat preferences. Because forage species are ecologically important (e.g., Pikitch et al. 2012), often economically important (e.g., Pikitch et al. 2014), and increasingly promoted for direct human nutrition (e.g., Tacon and Metian 2013), it is both surprising and a concern that there is such an array of definitions being used. This diversity may cause undue confusion that will further complicate the sustainable management of these species.
The International Symposium on the Role of Forage Fishes in Marine Ecosystems held in Alaska determined that “forage fish is a concept that many people have come to understand because of the context it is used in, but for which we lack a concrete definition. The term embodies a peculiar combination of ambiguity and precision” (Springer and Speckman 1997:773). Nearly 20 years later, we still lack a common operational definition used among scientists, industry, policy makers, and the public. Finding a better definition is important, because there is not only a global interest in understanding the trade-offs and approaches needed to sustainably manage these species (e.g., Peck et al. 2014; Essington et al. 2015; Rountos et al. 2015), but also a need for identifying them for ecolabel certifications (e.g., Agnew et al. 2014). It is time that we created a consistent definition of forage species: what they are—and are not—to prevent a future dilemma.
This micro-analysis aimed to examine and analyze how different stakeholders have defined forage species in the past, in order to help identify and define those species in the future. Two approaches were used to compile and evaluate the various definitions of forage species being used. First, a literature search was conducted to explore the diversity of forage terminology and scientific criteria. Next, a search of the attributes (i.e., maximum total length, life expectancy, trophic level, habitat) of those species included in the literature search was carried out using FishBase (Froese and Pauly 2015) and other sources. The diversity of definitions in the results suggests that a standardized definition of forage species should (1) be more specific in life history attributes and (2) focus more on whether or not a species is providing a critical role as prey in marine ecosystems. The latter may be accomplished by establishing criteria based on dietary contributions of the forage species or using other trophodynamic indicators.
THE NAME GAME
There are many terms currently used to identify forage species, including “forage fish,” “forage species,” “small pelagics,” and “lower-trophic-level species.” Scientists who use these terms often include a variety of fish and invertebrates (e.g., euphausiids, cephalopods, shrimp); thus, the term forage fish should immediately be phased out. The term that is most appropriate from a technical standpoint is forage species, because it is not exclusive to finfish, size, habitat, or trophic level.
TO INCLUDE OR NOT TO INCLUDE, THAT IS THE QUESTION
Scientists do not always agree on whether to include juvenile fish, myctophids, euphausiids (i.e., krill), cephalopods, or shrimp in their definitions of forage species. Most considerations have included krill, but there is not a clear consensus on other invertebrates such as cephalopods or shrimp. Some studies and management documents argue that cephalopods should not be included, because they can be quite piscivorous, whereas other studies show that certain species of cephalopods provide an important dietary component to upper-trophic-level predators (e.g., Szoboszlai et al. 2015) and thus should be categorized as forage species. Ultimately, this may depend on the species of cephalopod, because they represent a range of trophic levels (Coll et al. 2013). Inclusion of juvenile fish is also debatable, because they do not fulfill a role as prey throughout their entire life history. Juvenile Alaska Pollock Theragra chalcogramma, rockfish Sebastes spp., and salmon Oncorhynchus spp. are signature examples of fish that are important forage when juveniles but do not fit this criterion as adults. Myctophids, and possibly other small midwater fishes, are another group that are rarely included in forage species definitions, even though they are ecologically important as prey (e.g., Catul et al. 2011).
IS IT A “SMALL PELAGIC” WORLD AFTER ALL?
Categorization of species as forage has often depended on physical, ecological, and behavioral attributes. In particular, forage species are often considered small (<30 cm maximum standard length), relatively short-lived (1–3 years), pelagic fish that occupy intermediate trophic levels. However, there is ambiguity when the actual attributes of these species are cross- referenced using FishBase or other sources.
Most studies that categorize forage species as small pelagics (<30 cm) actually include species with maximum lengths ≥30 cm (e.g., Atlantic Menhaden Brevoortia tyrannus , etc.), according to FishBase. The median maximum length of forage species amongst the studies in the literature search is 28 cm, ranging from 2.5 to 76 cm. Therefore, more appropriate definitions should state that these species are small (<30 cm) to intermediate (≥30 but <90 cm) sized. Size-based classifications become more complicated if juvenile life stages of fish are included, because these species (e.g., rockfishes, mackerels, etc.) can have maximum lengths exceeding 90 cm. Because only 4% (i.e., 425 out of 9,992) of small (<30 cm) marine fish species in FishBase are from forage families (i.e., Atherinopsidae, Hemiramphidae, Dussumieriidae, Pristigasteridae, Osmeridae, Clupeidae, Alestidae, Ammodytidae, Argentinidae, Centriscidae, Atherinidae, Stromateidae, and Engraulidae), using size in a definition may not be an ideal way to define forage species.
Similar discrepancies are found in regards to longevity. Forage species are not as short-lived as many definitions have asserted, and this misconception is largely based on notable examples of short-lived forage species like the Peruvian Anchoveta Engraulis ringens (maximum age = 3). The median maximum age of forage species amongst the studies in this literature search was 10 years, ranging from 2 to 25. This point is further emphasized when juvenile fish are added as forage species, with many living a median maximum age of 18 years.
Pelagic is frequently used in definitions of forage species, but there are examples where this attribute is not appropriate. Sandeels (family Ammodytidae), for instance, are not pelagic, yet they are a major forage species (Holland et al. 2005). Similarly, benthic invertebrates (e.g., polychaetes, amphipods, mysids, etc.) also serve as important forage in some ecosystems (Ihde et al. 2015). For fish, a search of forage families in FishBase revealed that nearly 81% (i.e., 457 out of 566) of forage species are pelagic, whereas 19% (i.e., 109 out of 566) are either reef-associated (11%) or demersal (8%). Although fish species are mostly pelagic, it is not an appropriate characteristic for defining all forage species.
Forage species are often defined as occupying intermediate trophic levels, but some studies refer to them as lower-trophic- level species (e.g., Smith et al. 2011). Trophic levels of forage species included in this literature search ranged from 2.1 to 4.5, with a median trophic level of 3.2, which identifies as “intermediate.” The median trophic level increased to 3.6 when juvenile fish are included. These values would decrease if benthic invertebrates were included.
FINDING COMMON GROUND FOR AN OPERATIONAL DEFINITION
The goal of this literature search is not to single out or criticize the definitions used in specific studies but rather to emphasize the need to create a consistent operational definition for these species. Although the focus has been on the inconsistencies in species type, size, age, habitat, and trophic level, it is important to note that when defining forage species, every study indicated the ecological importance of these species to upper-trophic-level predators. Therefore, a common standard should focus more on the trophic role of a species and whether it is a critical prey resource throughout its life history. This could be done by implementing a dietary component into the definition of forage species or by using indicators such as the “SURF” index (Plagányi and Essington 2014). Diet studies and syntheses of diet data for upper-trophic-level predators can provide guidance to scientists, managers, and policy makers on which species are likely to be forage species. It is imperative that we are aware, critical, and consistent in how we define forage species in our future work, because definitions are paramount for communication, legislation, and effective ecosystem-based management (Link and Browman 2014).
The editors and Ed Houde are thanked for their thoughtful review and comments on an earlier draft of this article. Thanks are also offered to those who visited and interacted with my poster on this topic at the 2015 AFS Annual Meeting in Portland, Oregon. Rachel Silver and Alexandra DiGiacomo are especially thanked for their assistance with the FishBase searches.
Agnew, D. J., N. L. Gutiérrez, A. Stern-Pirlot, and D. D. Hoggarth. 2014. The MSC experience: developing an operational certification standard and a market incentive to improve fishery sustainability. ICES Journal of Marine Science 71(2):216–225.
Catul, V., M. Gauns, and P. K. Karuppasamy. 2011. A review on mes- opelagic fishes belonging to family Myctophidae. Reviews in Fish Biology and Fisheries 21(3):339–354.
Coll, M., J. Navarro, R. J. Olson, and V. Christensen. 2013. Assessing the trophic position and ecological role of squids in marine eco- systems by means of food-web models. Deep-Sea Research Part II-Topical Studies in Oceanography 95:21–36.
Essington, T. E., P. E. Moriarty, H. E. Froehlich, E. E. Hodgson, L. E. Koehn, K. L. Oken, M. C. Siple, and C. C. Stawitz. 2015. Fishing amplifies forage fish population collapses. Proceedings of the National Academy of Sciences 112(21):6648–6652.
Froese, R., and D. Pauly. 2015. FishBase. Available: www.fishbase.org. (July 2015).
Holland, G. J., S. P. Greenstreet, I. M. Gibb, H. M. Fraser, and M. R. Rob- ertson. 2005. Identifying sandeel Ammodytes marinus sediment habitat preferences in the marine environment. Marine Ecology Progress Series 303:269–282.
Ihde, T. F., E. D. Houde, C. F. Bonzek, and E. Franke. 2015. Assessing the Chesapeake Bay forage base: existing data and research pri- orities. STAC Publication Number 15-005, Chesapeake Bay Pro- gram, Edgewater, Maryland.
Link, J. S., and H. I. Browman. 2014. Integrating what? Levels of marine ecosystem-based assessment and management. ICES Journal of Marine Science 71(5): 1170–1173. DOI: 10.1093/icesjms/ fsu026.
Peck, M. A., S. Neuenfeldt, T. E. Essington, V. M. Trenkel, A. Takasuka, H. Gislason, M. Dickey-Collas, K. H. Andersen, L. Ravn-Jonsen, N. Vestergaard, S. F. Kvamsdal, A. Gårdmark, J. Link, and J. C. Rice. 2014. Forage fish interactions: a symposium on “creating the tools for ecosystem-based management of marine resources.” ICES Journal of Marine Science 71(1):1–4.
Pikitch, E. K., P. D. Boersma, I. L. Boyd, D. O. Conover, P. Cury, T. E. Ess- ington, S. S. Heppell, E. D. Houde, M. Mangel, D. Pauly, É. Plagányi, K. Sainsbury, and R. Steneck. 2012. Little fish, big impact: manag- ing a crucial link in ocean food webs. Lenfest Ocean Program, Washington, D.C.
Pikitch, E. K., K. J. Rountos, T. E. Essington, C. Santora, D. Pauly, R. Watson, U. Sumaila, P. D. Boersma, I. L. Boyd, D. O. Conover, P. Cury, S. S. Heppell, E. D. Houde, M. Mangel, É. Plagányi, K. Sains- bury, R. Steneck, T. M. Geers, N. Gownaris, and S. B. Munch. 2014. The global contribution of forage fish to marine fisheries and ecosystems. Fish and Fisheries 15:43–64.
Plagányi, É. E., and T. E. Essington. 2014. When the SURFs up, forage fish are key. Fisheries Research 159:68–74.
Rountos, K. J., M. G. Frisk, and E. K. Pikitch. 2015. Are we catching what they eat? Moving beyond trends in the mean trophic level of catch. Fisheries 40(8):376–385.
Smith, A. D. M., C. J. Brown, C. M. Bulman, E. A. Fulton, P. Johnson, I. C. Kaplan, H. Lozano-Montes, S. Mackinson, M. Marzloff, L. J. Shan- non, Y.-J. Shin, and J. Tam. 2011. Impacts of fishing low-trophic level species on marine ecosystems. Science 333(6046):1147– 1150.
Springer, A. M., and S. G. Speckman. 1997. A forage fish is what? Sum- mary of the symposium. Pages 773–816 in B. Baxter and C. W. Mecklenburg, editors. Forage fishes in marine ecosystems. Pro- ceedings of the international symposium on the role of forage fishes in marine ecosystems. University of Alaska, Alaska Sea Grant College Program Report Number 97-01, Fairbanks, Alaska.
Szoboszlai, A. I., J. A. Thayer, S. A. Wood, W. J. Sydeman, and L. E. Koehn. 2015. Forage species in predator diets: synthesis of data from the California Current. Ecological Informatics 29(1):45–56.
Tacon, A. G. J., and M. Metian. 2013. Fish matters: importance of aquatic foods in human nutrition and global food supply. Re- views in Fisheries Science 21(1):22–38.
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