Progress in Oceanography 191 (2021) 102494 Contents lists available at ScienceDirect Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean Small pelagic fish in the new millennium: A bottom-up view of global research effort Myron A. Peck a,*, Jürgen Alheit b, Arnaud Bertrand c, Ignacio A. Catalan´ d, Susana Garrido e, Marta Moyano f, Ryan R. Rykaczewski g,k, Akinori Takasuka h, Carl D. van der Lingen i,j a Department of Coastal Systems (COS), Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg, Texel, The Netherlands b Leibniz Institute for Baltic Sea Research Warnemünde, Seestr. 15, 18119 Warnemünde, Germany c Institut de Recherche pour le D´eveloppement (IRD), MARBEC, Univ Montpellier, CNRS, Ifremer, IRD, Av. Jean Monnet, 34203 S`ete, France d Institut Mediterrani d’Estudis Avançats, IMEDEA (UIB-CSIC), Miquel Marqu´es 21, 07190 Esporles, Illes Balears, Spain e Portuguese Institute for Marine and Atmospheric Science (IPMA), Rua Alfredo Magalhaes~ Ramalho 6, 1449-006 Lisbon, Portugal f Centre for Coastal Research, University of Agder, Universitetsveien 25, 4630 Kristiansand, Norway g NOAA National Marine Fisheries Service, Pacific Islands Fisheries Science Center, 1845 Wasp Blvd., Honolulu, Hawaii 96818, USA h Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan i Department of Environment, Forestry and Fisheries (DEFF), Private Bag X2, Vlaeberg 8000, Cape Town, South Africa j Marine Research Institute and Department of Biological Sciences, University of Cape Town (UCT), Private Bag X3, Rondebosch 7700, Cape Town, South Africa k Department of Oceanography, University of Hawaiʻi at Manoa,¯ 1000 Pope Rd., Honolulu, Hawaiʻi 96822 USA ABSTRACT Small pelagic fish (SPF) play extremely important ecological roles in marine ecosystems, form some of the most economically valuable fisheries resources, and play a vital role in global food security. Due to their short generation times and tight coupling to lower trophic levels, populations of SPF display large boom-and-bust dynamics that are closely linked to climate variability. To reveal emerging global research trends on SPF as opposed to more recently published, ecosystem- specific reviews of SPF, we reviewed the literature published in two, 6-year periods in the new millennium (2001–2006, and 2011–2016) straddling the publica- tion of a large, global review of the dynamics of SPF in 2009. We explored intrinsic and extrinsic (bottom-up) factors influencing the dynamics of SPF such as anchovies, sardines, herrings and sprats within the sub-order Clupeidae. Published research efforts within 16 different biogeographic ocean regions were compiled (more than 900 studies) and compared to identify i) new milestones and advances in our understanding, ii) emerging research trends and iii) remaining gaps in knowledge. Studies were separated into 5 categories (field, laboratory, mesocosms, long-term statistical analyses and spatially-explicit modelling) and discussed in relation to 10 bottom-up categories including 5 abiotic factors (temperature, salinity, pH, dissolved oxygen, density), 3 physical processes (advection, turbulence, turbidity) and 2 biotic factors (prey quantity and quality). The peer-reviewed literature reflects changes in the number of studies between the two time periods including increases (Mediterranean Sea, Humboldt Current) and decreases (Australia, Benguela Current). Our review highlights i) gaps in ecological knowledge on young juveniles and, in general, on the impacts of hypoxia and heatwaves on SPF, ii) the utility of paleo studies in exploring population drivers, iii) the continued need to develop spatially-explicit, full life-cycle models, iv) the importance of exploring how density-dependent processes impact vital rates (growth, survival, reproduction), and v) the benefits of international collaboration for knowledge transfer and building unifying hypotheses on the role of bottom-up factors and processes that regulate SPF populations. 1. Introduction anchoveta (Engraulis ringens) were landed by the largest single-species fishery in the world, while another six species of SPF were within the 1.1. Importance of small pelagic fish top 25 major global fisheries (FAO, 2017). Stocks of SPF such as Peru- vian anchoveta are notorious for their rapid, large-scale changes in Catches of anchovies, sardines, herrings and other small pelagic distribution and/or productivity in response to climate-mediated clupeoid fishes are not only important for direct human consumption changes in bottom-up forcing (Lluch-Belda et al., 1992; Schwartzlose but also critical for fishmeal and fish oil used in agri- or aqua-feeds, et al., 1999; Tourre et al., 2007; Salvatteci et al., 2018). For example, the making small pelagic fish (SPF) significant for global food security large harvest of Peruvian anchoveta in 2015 was a 37% increase (FAO, 2016). In 2015, 4.3 million metric tonnes (MMT) of Peruvian compared to 2014. These fishes are also emblematic of the relatively * Corresponding author. E-mail address: [email protected] (M.A. Peck). https://doi.org/10.1016/j.pocean.2020.102494 Received 19 July 2020; Received in revised form 22 November 2020; Accepted 7 December 2020 Available online 16 December 2020 0079-6611/© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). M.A. Peck et al. Progress in Oceanography 191 (2021) 102494 rapid (regime) shifts (dramatic and abrupt changes in the abundance ancillary manner, or iv) focused on predators of SPF (seabirds, marine and relative dominance of SPF that are persistent in time) documented mammals and fish). The majority of excluded studies was within the in many marine ecosystems worldwide (e.g., Alheit and Niquen, 2004; latter category. At this point, the list contained 374 papers published Alheit et al., 2005; Watanabe, 2009). The high inter-annual variability from 2001 to 2006 and 376 papers published from 2011 to 2016. Some of SPF biomass, their sensitivity to climate variability, and the occur- papers were not found by our search string and, based on our collective rence of productivity regimes that are difficult to predict in terms of knowledge and expertise in specific regions, a further 195 studies were onset and duration all pose challenges to the sustainable management added. The final list contained 945 studies (434 in 2001–2006 and 511 and efforts to prevent overfishing of SPF populations. These fish also in 2011–2016). We recognize that there is insightful research that has or play a pivotal role in marine food webs by acting as conduits of energy is being conducted that may not be included here, and we do not intend from lower to upper trophic levels (Pikitch et al., 2012). Thus, from both to be insular in our assessment. Rather the approach taken is an analysis an ecological and a societal point of view, it is essential that we gain a of trends in the mass literature, not an analysis of the most important (or full understanding of the factors and processes that drive changes in the most all inclusive) research on planktivorous fishes. Although it is likely productivity of populations and management units (stocks) of these that some studies were missed during the two, 6-yr time periods, in our fishes. This knowledge can buttress science-based advice to fisheries opinion, the 945 papers compiled here have captured trends during the management (e.g., Kaplan et al., 2016) as well as the robustness of new millennium in basic (fundamental) as well as emerging research longer-term projections of future impacts of climate change (MacKenzie themes on SPF among 16 regions (large marine ecosystems) around the et al., 2012; Peck et al., 2013). world. We also reviewed the types of studies including specific methods / 1.2. Scope of this review themes (Section 2) and compared research conducted on SPF in different regions (see Section 3). For these and other sections, we integrated the The present study reviewed research conducted on SPF using a semi- findings of studies published before, between and after the two 6-yr time structured review of literature published during 2001–2006 and periods that were used to compare trends. For example, many studies 2011–2016. We compared the two time periods to reveal emerging were published from 2012 to 2015 and more than 150 references in this research trends globally and to complement recently published, 4-yr period were used in this review. The 2017 symposium on SPF ecosystem-specific reviews of SPF (e.g.,Takasuka, 2018). The first time produced 38 publications in two special volumes (Alheit and Peck, 2019; period was chosen to capture research finalized at the start of the new Alheit et al., 2019b) and some of those and other recent studies are also millennium (e.g., published in 2001) that appeared in the peer-reviewed included here. literature prior to a key, global review of the dynamics of SPF prepared in 2008 (Checkley et al., 2009) that arose from the GLOBEC Small Pe- 1.3. Categories of studies lagics and Climate Change (SPACC) collaborative research programme, and two special issues on upwelling systems (Bertrand et al., 2008b; During the period between 2001 and 2006, field studies, statistical Freon´ et al., 2009). The second period represented the same number of analyses/reviews, spatially-explicit modelling, laboratory experiments, years after the SPACC book but just prior to a large, international and mesocosm research accounted for 70, 20, 10, 9 and 0.5%, respec- symposium on SPF that was convened in March 2017 (Alheit and Peck, tively, of the studies published on SPF (some studies were in multiple 2019; Alheit et al., 2019b). categories) (Fig. 1A). Between 2011 and 2016, these same five cate- The emphasis of this review was on how bottom-up processes and gories accounted for 67, 20, 12, 10 and 1%, respectively, of the pub- abiotic environmental factors regulate SPF populations or stocks.