ICES CM 2015/ H:12 CO2-induced ocean acidification increases risk of predation in a coastal temperate fish larvae Ana M Faria (1), Ana F Lopes (1), Ana P Oliveira (2), Phil Munday (3), Emanuel J Gonçalves (1) (1) MARE – Marine and Environmental Science Centre, ISPA−IU, Rua Jardim do Tabaco, 1149-041 Lisboa, Portugal; (2) IPMA – Instituto Português do Mar e da Atmosfera, Algés, Portugal; (3) School of Marine and Tropical Biology, James Cook University, Australia. Presenter contact details: [email protected], phone +351 218 811 700 Summary The larval period of most marine organisms is highly vulnerable to predation. The ability to recognize and avoid predators during this life stage should increase both the immediate and future prospects of survival. A growing number of studies suggest that behaviour of early life stages of fishes may be highly affected by ocean acidification. Fish reared under high CO2 levels fail to recognize predator cues and adopt bolder and riskier behaviours, therefore increasing vulnerability to predators. Here we tested if larvae of a temperate fish species, Atherina presbyter, have the capacity to recognize the olfactory cues produced by predators, and whether this ability is disrupted by exposure to high levels of CO2 (pH ~7.8 and 7.6). Additionally, we’ve investigated the preference for a light-dark environment (scototaxis), which can represent “anxiety” or “fear”-like behavior. Results suggest that larvae exposed to increasing CO2 conditions might be in a greater risk of predation compared to larvae reared in control conditions. Introduction The ability to recognize a potential predator is an important component of antipredator behavior because a failure increases the probability that the predator captures or injures the prey (Lima and Dill 1990). Although a suite of sensory mechanisms is available for predator detection, olfaction plays a significant role in the initial detection of predators (Chivers et al. 2001). Recent research has demonstrated that the ability of larval fish to detect predator odours and conspecific alarm cues is hindered by ocean acidification (Dixson et al. 2010). Impairment of behaviour by elevated CO2 levels could have far-reaching implications for survival and ultimately sustainability of adult populations. Here we tested the hypothesis that exposure to high levels of CO2 increases risk of predation of sand smelt Atherina presbyter larvae by disrupting the ability to recognize olfactory cues produced by predators, and becoming more anxious and active. Materials and methods Wild-caught sand-smelt larvae were randomly assigned to one of three pCO2 treatments - control (~600 µatm), medium (~950 µatm) and high (~1500 µatm) - and reared for 20 days. The response of larvae to olfactory cues of a predator, Diplodus sargus, was tested in a two-channel flume chamber (adapted from Gerlach et al. 2007), where larvae were given the choice of two streams of water containing different olfactory cues. Experimental scototaxic (light/dark preference) testing was performed as described by Hamilton et al. (2013). Proportion of time spent in the black and white compartments (%) and number of times the individuals entered each compartment was recorded. Results and Discussion Results show that larvae reared in the high pCO2 treatment spent, on average, 76% of time in the predator cue, which was significantly higher when compared to larvae from control (51 %) and mid (65 %) pCO2 treatments (Fig 1A). This disruption of olfactory behavior has also reported for other tropical fish larvae (Dixson et al. 2010), and may be attributed to an alteration of neuro-sensory functioning following exposure to elevated CO2 (Nilsson et al. 2012). We also show that control larvae have a significant preference for the light compartment of the experimental arena (Fig 1B), which might be related to the fact that larva are transparent and in a light environment they would be less visible to the predators. However, larvae from mid and high CO2 treatments show no preference for any of the compartments in the chamber. Despite the tendency for control larvae to spend more time in light area and be more active (Fig 1C) than larvae from mid and high treatments, it wasn’t statistically significant and we cannot conclude that high CO2 levels result in increased anxiety, but we can conclude that the lack of preference for the light comparment make these larvae more easily detected by a predator. These results contrasts with the results obtained by Hamilton et al. (2013), who reported that control rockfish had no preference for any of the compartments, but fish exposed to high CO2 levels had a strong preference for the dark zone. Overall, our results suggest that impairment of critical behaviours for predator detection and avoidance might make these larvae more vulnerable to the risk of predation in a high CO2 world. Figure 1. Average time (s) spent in the predator cue (A); average time (s) spent in the light compartment (B); average entries in light and dark compartments (C), by larvae reared in control, mid and high pCO2 conditions. Mean ± SE References Chivers, D.P., Mirza, R.S., Bryer, P.J., and Kiesecker, J.M. 2001. Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Canadian Journal of Zoology, 79:867–873 Dixson, D.L., Munday, P.L., and Jones, G.P. 2010. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters, 13: 68-75 Gerlach, G., Atema, J., Kingsford, M.J., Black, K., and Miller-Sims, V. 2007. Smelling home can prevent dispersal of reef fish larvae. Proceedings National Academy of Sciences of the United States of America (104): 858–863 Hamilton, T.J., Holcombe, A., and Tresguerres, M. 2013. CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning. Proceedings of the Royal Society B-Biological Sciences, 281(1775): 20132509 Lima, S.L., and Dill, L.M. 1990. Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology, 68: 619-640 Nilsson, G.E., Dixson, D.L., Domenici, P., McCormick, M.I., Sorensen, C., Watson, S.-A., and Munday, P. 2012. Near-future CO2 levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change, 2: 201-204.
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