Renaissance of a caveat: Allee effects in marine fish

ICES Journal of Marine Science ICES Journal of Marine Science (2014), 71(8), 2152– 2157. doi:10.1093/icesjms/fst179 Contribution to the Special Issue: ‘Commemorating 100 years since Hjort’s 1914 treatise on fluctuations in the great fisheries of northern Europe’ Review Article Renaissance of a caveat: Allee effects in marine fish Jeffrey A. Hutchings 1,2* 1 Department of Biology, Dalhousie University, Halifax, NS, Canada Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo, Norway 2 *Corresponding author: tel: +1 902 494 2687; fax: +1 902 494 3736; e-mail: . Hutchings, J. A. Renaissance of a caveat: Allee effects in marine fish. – ICES Journal of Marine Science, 71: 2152 –2157. Received 17 July 2013; accepted 18 September 2013; advance access publication 14 November 2013. The population dynamics of marine fish at low abundance has long been of interest. One century ago, Johan Hjort drew attention to the importance of understanding “the laws which govern the renewal of the animal population”. Integral to the current work on the recovery of collapsed fish stocks is the association between abundance and per capita population growth rate (r), a negative correlation being representative of compensation and a positive correlation indicative of an Allee effect, also termed depensation. Allee effects are predicted to slow the rate, and increase the uncertainty, of recovery. Based on studies having sufficient data at low abundance, the magnitude of depletion experienced by some fish populations appears to have been sufficient to have generated either an Allee effect or a transition from strong to weak (or absent) compensatory dynamics. To a first approximation, empirically based Allee-effect reference points are consistent with suggested thresholds for overfishing and stock collapse. When evaluating Allee effects in marine fish, it is important not to conflate causal mechanism(s) with the pattern between r and abundance; the latter is of greater practical import. An additional caveat is that the longer a population remains at low abundance, the more likely it is that the environment around it will change in ways that are unfavourable to recovery. It might be this “temporal tyranny” of small population size that is most likely to produce an emergent Allee effect and depensatory dynamics in some collapsed marine fish populations. Keywords: depensation, population growth rate, rebuilding, recovery, reference point, threshold. A scientific legacy predicated by uncommon breadth In 1947, Johan Hjort delivered a lecture to the Danish Academy of Natural Sciences entitled “Renaissance of the Individual”. It was intended to place his fish research of the early 20th century in the context of his more recent international fisheries and whaling work. The lecture comprised his final publication (Hjort, 1948). In addition to Hjort’s personal reflections on the work for which he is best known (Hjort, 1914), the essay is of interest because of the impressive job that he does in weaving together ideas from a broad range of thinkers: Plato, Malthus, Lamarck, Darwin, Goethe. From a social-science perspective, Hjort (1948) emphasizes the importance (the “renaissance”) of the individual in the context of both human and fish populations, continuing a narrative evident in his writings in the 1930s (Hjort, 1934, 1935). Hjort was influenced by a palette of classical ideas atypical of contemporary fisheries science. These ideas contributed to a plethora of interests that sculpted a highly influential legacy to marine fisheries research. Foremost among these are his studies of environmentally driven changes in fish abundance, predicated in particular by his work on Atlantic cod (Gadus morhua) and Atlantic herring (Clupea harengus). In 1914, he posited two key ideas (Hjort, 1914, 1948). One of these was that changes in abundance can be greatly influenced by fluctuations in the marine realm (Hjort, 1914), a conclusion stemming from what he had interpreted (Hjort, 1948) to be a lack of association between catches of cod (a presumed metric of abundance) and numbers of fishers (a presumed metric of fishing pressure). A second idea that fish abundance can be significantly influenced by the strength of relatively few year classes, or cohorts, lead him to hypothesize that the primary cause of interannual changes in cohort strength was changes in the abundance of the phytoplankton and zooplankton upon which newly hatched fish larvae depend for food during their “critical period” of early life (Hjort, 1914, 1948). # 2013 International Council for the Exploration of the Sea. Published by Oxford University Press. All rights reserved. For Permissions, please email: 2153 Allee effects in marine fish The question of whether population abundance, in addition to the environment, affects per capita population growth rate (r) is of basic importance to fish population dynamics. Hjort appears to have acknowledged its relevance, noting that “it must be of the greatest importance to ascertain the nature of the laws which govern the renewal of the animal population” (Hjort, 1914). His interest in population dynamical studies matured with his experience on the International Whaling Commission (Hardy, 1950) and revealed an impressive awareness of recently published research on taxa far removed from fish and marine mammals (Richards, 1928; Klem, 1933). In 1935, for example, he used sigmoidal population growth curves of bacteria to inform changes to, and the threat of overfishing in, the Norwegian whaling industry, noting that “the future of a population may best be predicted by studying the fate of the average individual” whose “standard of life” might best be represented by the “rate of [population] growth” (Hjort, 1934, 1935). Hjort’s interest in the renewal of animal populations and of how the population growth rate is related to abundance might be said to have foreshadowed research, initiated half a century later, on factors affecting the recovery of depleted marine fish. Allee effects and depensation Few would argue against the assertion that overfishing has been a primary determinant of depletion in marine fish populations (Dulvy et al., 2003). But the question of whether low abundance per se is generally of greater influence to population growth following stock depletion than environmental variability is unresolved. One recent study, for example, concluded that although stock abundance was related to stock productivity in almost half of 230 fish populations examined, there were irregular shifts in temporal patterns of productivity that could not be explained by abundance in many stocks (Vert-pre et al., 2013). Based on Warder Allee’s classical work on how “certain aspects of survival values” can increase with density when populations are at low abundance (Allee, 1931, 1938), an Allee effect (often termed “depensation” in the fisheries literature) is “a positive relationship (...truncated)