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Review
Pain in aquatic animals
Lynne U. Sneddon
Journal of Experimental Biology 2015 218: 967-976; doi: 10.1242/jeb.088823
Lynne U. Sneddon
University of Liverpool, Institute of Integrative Biology, The BioScience Building, Liverpool L69 7ZB, UK
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  • For correspondence: lsneddon@liverpool.ac.uk
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    Fig. 1.

    Anatomical, electrophysiological and behavioural evidence of pain in rainbow trout. (A) Section of the maxillary branch of the trigeminal nerve of the rainbow trout showing the presence of A-delta and C fibres that may act as nociceptors (×1000; scale bar, 2 μm). Adapted from Sneddon (2002) with kind permission from Elsevier. (B) Electrophysiological recordings from a nociceptive receptive field on the trout face showing responses of nociceptors to heat stimulation. This illustrates sensitization of a mechanothermal receptor to heat following noxious chemical stimulation. The firing response to ramp and hold heat stimulation is shown before (left) and 9 min after (right) subcutaneous injection of 1% formalin, <1 mm from the receptive field. The upper trace shows the heat stimulus, the middle panel plots the instantaneous firing frequency (IFF) as scatter graphs and the lower trace shows an extracellular single unit recording from the trigeminal ganglion. Thermal threshold remains the same but firing frequency is greatly increased following formalin injection. Adapted from Ashley et al. (2007) with kind permission from Elsevier. (C) The percentage change in activity (top) and opercular beat rate (OBR; bottom) in rainbow trout 30 min after they were injected subcutaneously with saline or a noxious substance (0.1% acetic acid), or acid combined with intramuscular injection of the opioid buprenorphine (0.1 mg kg−1; Bup.) or the non-steroidal anti-inflammatory drug (NSAID) carprofen (5 mg kg−1; Car.), or injected at the same site as the acid with the analgesic lidocaine (1 mg; Lid.). The grey line represents the impact of saline (control) treatment whereas the black line represents the impact of pain (acid injection). Adapted from Mettam et al. (2011) with kind permission from Elsevier.

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    Fig. 2.

    Impact of injury on anti-predator flight behaviour and survival in squid. (A) The predator–prey sequence of seabass feeding upon squid prey. (B) Injured squid lacking nociceptive sensitization had the lowest odds of survival at the conclusion of a 30 min trial with free interaction of squid and seabass. Squid in the injured (I) and injured treated with anaesthetic to prevent nociceptor sensitization (IA) groups had lower overall survival, showing that predators target injured animals compared with the uninjured (U) and uninjured with anaesthetic (UA) group. IA squid were most likely to be killed. The difference in survival between the U and the IA group can be considered the cost of being injured, while the difference in survival percentage between the IA and I groups (P=0.05) reveals the benefit that nociceptive sensitization provides to injured animals. Odds ratios are given in the bars: *P≤0.05, **P<0.01. (C) Flight initiation distance. Injured squid fled from predators at a greater distance and thus were more sensitive to predator threat than the other groups (**P<0.01). Adapted from Crook et al. (2014) with kind permission from Elsevier.

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    Fig. 3.

    Dynamics of NADPH-d/iNOS activity in the brain of Hemigrapsus sanguineus after nociceptive stimulation. (A) The distribution of nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d), a histochemical marker for inducible nitric oxide synthase (iNOS), in the olfactory lobe (ON), the lateral antenna 1 neuropils (LAN), antenna II neuropils (AnN) and cluster 9/11 is shown in control animals. Ten minutes after nociceptive injury, NADPH-d staining increased in the ON, LAN (arrows) and cluster 17. Thirty minutes after injury, NADPH-d activity maximally increased in the ON and LAN (arrows), and solitary NADPH-d-positive neurons appeared in clusters 9/11 and 6 (arrowheads). The bottom panel shows NADPH-d-positive neurons that appeared in cluster 6. Scale bars, 100 μm. (B) The temporal dynamics of NADPH-d activity (optical density) in leg neuromeres 1–5 of H. sanguineus induced by nociceptive stimulation. Data are shown for the side contralateral to injury and ipsilateral to injury. In the graphs, double daggers represent P<0.05 when compared with intact (and control) animals whose activity was unchanged during the observation period; asterisks indicate the difference obtained when contralateral and ipsilateral sides of the same neuromere were compared (*P<0.05, **P<0.01, ***P<0.001). Results represent the mean±s.e.m. from five different sections of five animals. Adapted from Dyuizen et al. (2012).

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Keywords

  • Animal pain
  • Crustaceans
  • Experimental ethics
  • Fish
  • Molluscs
  • Neurobiology
  • Nociceptors

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Review
Pain in aquatic animals
Lynne U. Sneddon
Journal of Experimental Biology 2015 218: 967-976; doi: 10.1242/jeb.088823
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Review
Pain in aquatic animals
Lynne U. Sneddon
Journal of Experimental Biology 2015 218: 967-976; doi: 10.1242/jeb.088823

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  • Top
  • Article
    • ABSTRACT
    • Introduction: the occurrence of nociception and pain
    • Pain in fish
    • Molluscs
    • Crustaceans
    • Implications for the use of aquatic animals
    • Conclusions
    • Acknowledgements
    • FOOTNOTES
    • References
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