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Original Article Spearfishing Modulates Flight Initiation Distance of Fishes: the Effects of Protection, Individual Size, and Be ICES Journal of Marine Science (2018), 75(5), 1779–1789. doi:10.1093/icesjms/fsy059 Original Article Downloaded from https://academic.oup.com/icesjms/article-abstract/75/5/1779/5032467 by guest on 08 October 2018 Spearfishing modulates flight initiation distance of fishes: the effects of protection, individual size, and bearing a speargun Valerio Sbragaglia1,2,*,†, Lorenzo Morroni2,3† Lorenzo Bramanti4, Boris Weitzmann5, Robert Arlinghaus1,6, and Ernesto Azzurro2,7 1Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mu¨ggelseedamm 310, 12587 Berlin, Germany 2Institute for Environmental Protection and Research (ISPRA), Via del Cedro 38, 57122 Livorno, Italy 3Department of Life and Environmental Sciences, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy 4Sorbonne Universite`, CNRS, Laboratoire d’Ecoge´ochimie des Environnements Benthiques (LECOB), Observatoire Oceanologique Banyuls sur mer. 1 Avenue Pierre Fabre, 66650 Banyuls sur mer, France 5Parc Natural del Montgrı´, les Illes Medes i el Baix Ter, L’Estartit, Catalunya, Spain 6Division of Integrative Fisheries Management, Department of Crop and Animal Sciences, Faculty of Life Sciences, Humboldt-Universita¨t zu Berlin, Invalidenstrasse 42, 10115 Berlin, Germany 7Stazione Zoologica Anton Dohrn (SZN), Villa Comunale 80121 Napoli, Italy *Corresponding author: tel: þ39 0650074030; fax: þ39 0586896248; e-mail: [email protected]. †Equally contributed to this study. Sbragaglia, V., Morroni, L. Bramanti, L., Weitzmann, B., Arlinghaus, R., and Azzurro, E. Spearfishing modulates flight initiation distance of fishes: the effects of protection, individual size, and bearing a speargun. – ICES Journal of Marine Science, 75: 1779–1789. Received 24 October 2017; revised 18 April 2018; accepted 25 April 2018; advance access publication 2 June 2018. In a landscape of fear, humans are altering key behaviours of wild-living animals, including those related to foraging, reproduction, and sur- vival. When exposed to potentially lethal human actions, such as hunting or fishing, fish, and wildlife are expected to behaviourally respond by becoming shyer and learning when to be cautious. Using a rich dataset collected in temperate rocky reefs, we provide evidence of spearfishing-induced behavioural changes in five coastal fish taxa, exposed to different levels of spearfishing exploitation, by using flight initia- tion distance (FID) as a proxy of predator avoidance. We detected a significant increase of mean and size effects of FID when the observer was equipped with a speargun. Such effects were more evident outside marine protected areas where spearfishing was allowed and was com- mensurate to the historically spearfishing pressure of each investigated taxon. Our results demonstrate the ability of fish to develop fine- tuned antipredator responses and to recognize the risks posed by spearfishers as human predators. This capacity is likely acquired by learning, but harvest-induced truncation of the behavioural diversity and fisheries-induced evolution may also play a role and help to explain the in- creased timidity shown by the exploited fishes in our study. Keywords: behaviour, human predation, Mediterranean, shyness, timidity syndrome. Introduction 2009; Arlinghaus et al., 2017) and evolutionary consequences of The exploitation of wild animal populations by humans, via fish- fishing (e.g. Jørgensen et al., 2007; Laugen et al., 2014). Fish traits ing or hunting, can alter the abundance, size-structure, life-his- such as size or behaviour are typically thought to be under selec- tory, and behaviour of the targeted populations (Allendorf and tion by fishing (Law, 2007; Uusi-Heikkila¨ et al., 2008; Kuparinen Hard, 2009; Sullivan et al., 2017). Accordingly, substantial effort and Festa-Bianchet, 2017; Lennox et al., 2017), and such trait- has been devoted to understand the ecological (e.g. Worm et al., selective harvesting in combination with elevated mortality is VC International Council for the Exploration of the Sea 2018. All rights reserved. For permissions, please email: [email protected] 1780 V. Sbragaglia et al. expected to affect the size and age structure (e.g. Arlinghaus et al., traits linked to the ability of fishes to hide or escape from the 2010), life-history and behavioural traits in fish populations spearfisher may be under a strong selective pressure (Ydenberg (Jørgensen et al., 2007; Allendorf and Hard, 2009; Uusi-Heikkila¨ and Dill, 1986; Stankowich and Blumstein, 2005; Januchowski- et al., 2015; Andersen et al., 2018). Specifically, many fishing gears Hartley et al., 2011). However, fish behaviour has a large plastic selectively remove large (e.g. Law, 2007) and bold individuals component and can thus also rapidly change through learning to (e.g. Klefoth et al., 2017), thereby favouring fast life-histories avoid an approaching spearfisher (Kelley and Magurran, 2003; (Heino et al., 2013; Laugen et al., 2014) and often more cautious Tran et al., 2016). As a consequence, levels of timidity can sub- behavioural types (Arlinghaus et al., 2017; Diaz Pauli and Sih, stantially increase via increased spearfishing pressure within few 2017; Andersen et al., 2018). Harvest-induced changes can be days after opening a fishing zone (Goetze et al., 2017). caused both by plastic and evolutionary responses (Kelley and The rapid increase of spearfishing in the last 60 years in the Magurran, 2003; Laugen et al., 2014; Arlinghaus et al., 2017; Mediterranean area (Coll et al., 2004) represents a new pressure Downloaded from https://academic.oup.com/icesjms/article-abstract/75/5/1779/5032467 by guest on 08 October 2018 Andersen et al., 2018). for fish populations and an opportunity to understand how fish The potential for fisheries to alter the behavioural composition cope with the sudden arrival of a new human predator. Fishes in fish populations has not been fully explored (Uusi-Heikkila¨ can became aware of the presence of predators by olfactory et al., 2008; Heino et al., 2015; Arlinghaus et al., 2017; Tillotson (Chivers and Smith, 1998), tactile or auditory stimuli (Kelley and and Quinn, 2018) despite the publication of the first observations Magurran, 2003), but in clear water conditions typical for many and hypotheses in the mid-1950s (Miller, 1957). Recent develop- areas of the Mediterranean rocky reefs, visual cues are likely the ments in fish personality research (e.g. Mittelbach et al., 2014) primary source of information that allows fishes to recognize have generated a theoretical basis to derive hypotheses about the predators from long distances (Aksnes and Giske, 1993). Fishes proximate and ultimate mechanisms of fisheries-induced behav- quickly learn how to reduce predation risk and as a consequence ioural modification (Andersen et al., 2018). Animal personality modulate the fundamental growth-mortality trade-off (Werner traits can correlate forming behavioural syndromes defined as and Hall, 1974; Ydenberg and Dill, 1986; Stamps, 2007). In par- correlated behavioural trait complexes that vary consistently ticular, the escape behaviour will be fine-tuned according to the among individuals across ecological contexts and time (Sih et al., presence of local food availability and individual internal states. 2004). On the basis of the behavioural syndrome concept, a wide- For example the approach of a predator may be more closely tol- spread harvesting-induced “timidity syndrome” has been hypoth- erated by a hungry fish in a food-deprived environment than by a esized (Arlinghaus et al., 2016; 2017). The timidity syndrome hy- satiated counterpart (see the economic hypothesis in Ydenberg pothesis suggests that exploitation by passive fishing gears and Dill, 1986). Learning can be both an individual or social pro- selectively removes bold, aggressive, explorative or active individ- cess, contributing to the large plasticity in behavioural repertoire uals, rendering the exploited population more “timid” compared that is typical of many fish species (Kieffer and Colgan, 1992; with unexploited populations of the same species (Arlinghaus Mangel and Stamps, 2001; Odling-Smee and Braithwaite, 2003). et al., 2017). The term “timidity” summaries expected changes in Learning ability is also correlated with personality traits, for ex- any or a combination of personality traits (e.g., activity, bold- ample in guppies (Poecilia reticulata) bolder individuals learn ness), rendering the surviving fishes collectively more cautious more quickly than shy individuals (Trompf and Brown, 2014). against passive fishing gears (Arlinghaus et al., 2016, 2017). It is Notwithstanding that different personalities can emerge from an open question whether this increased timidity towards fishing clonal fishes reared in identical environmental conditions (e.g. gears also translates to increased timidity against natural preda- Bierbach et al., 2017), consistent differences in behavioural traits tors, in turn forming a syndrome that may have a range of eco- have been found to carry a large genetic (i.e. heritable) compo- logical, social and economic consequences, most notably by nent (Dochtermann et al., 2014). Thus, spearfishing-induced se- altering the catchability or natural mortality rates of exploited lection on behaviour could also induce evolutionary change populations (Arlinghaus et al., 2016, 2017). towards increased shyness by removing bold, risk-taking fishes Spearfishing (defined as fishing with a speargun while freediv- (Andersen et al., 2018). ing) is a globally popular
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