Summary PhD thesis Pim Boute: Effects of electrical stimulation on marine organisms

Marine capture fisheries are important in providing food and livelihoods globally. A common fishing method is bottom trawling, which involves dragging nets over the seafloor to capture benthic invertebrates and fishes. In Northwestern Europe, beam trawls with tickler chains are used to catch the flatfish species common sole (Solea solea) in the North Sea. This technique, however, is characterised by poor selectivity, large disturbance of the benthic ecosystem, and high fuel consumption. An alternative catch method is to replace the tickler chains by electrode arrays which generate pulsed electric fields. This electrical stimulus induces involuntary muscle contractions which immobilise fishes and enables subsequent capture. Pulse trawling raised concerns about potential negative impacts on marine organisms. In this thesis, we examined effects of electrical pulse stimulation on benthic invertebrates and fishes and explored the ecological implications of electrotrawling.

In Chapter 2, we reviewed the marine electrotrawling field, described physiological responses of organisms exposed to electrical stimulation, and outlined electrical waveform characteristics. Based on published literature, we identified a lack of consistency in the description of electrical parameters in marine electrofishing laboratory and field research. Here, we offered recommendations for better communication standards in electrofishing and pulse trawling in particular. Specifically, we aimed to standardise descriptions of electrical waveform parameters, experimental designs, and environmental parameters. Our work may also promote collaboration with the freshwater electrofishing research community.

In Chapter 3, we studied effects of electrical pulse exposure on benthic invertebrates. In particular, we quantified changes in locomotion behaviour that might increase predation risk. We also scored acute behaviour during exposure and subsequent recovery period to reveal potentially different response mechanisms between species. Furthermore, we monitored survival up to 14 days after exposure. We examined these responses in six species from four phyla, namely common starfish (Asterias rubens), serpent star (Ophiura ophiura), common whelk (Buccinum undatum), sea mouse (Aphrodita aculeata), common hermit crab (Pagurus bernhardus), and flying crab (Liocarcinus holsatus). Responses during stimulation varied from no visible effect (echinoderms) to squirming (sea mouse) and retractions (whelk and crustaceans). All animals resumed normal behavioural patterns, without signs of lasting immobilisation within 30 s after stimulation. We found no change in locomotion patterns after stimulation for starfish, serpent star, whelk, and sea mouse. In contrast, flying crab and hermit crab showed significant changes in activity that were indicative of increased shelter behaviour. We found no effect of electrical exposure on survival after 14 days in all species. These findings suggest that changes in locomotion behaviour due to electrical stimulation as used in pulse trawling are unlikely to substantially compromise survival of the investigated species.

In Chapter 4, we addressed concerns that the electric fields of pulse trawls may affect fishes outside the trawl track. We measured behavioural response thresholds for electric field strengths in the laboratory and compared these thresholds to computer-simulated field strengths around electrode arrays of a commercial pulse trawl. We assessed thresholds for electroreceptive small-spotted catshark (Scyliorhinus canicula) and thornback ray (Raja clavata) as well as non-electroreceptive European seabass (Dicentrarchus labrax), turbot (Scophthalmus maximus), and common sole. Thresholds for different species varied between 6.0 and 9.8 V m^–1, with no significant difference between electroreceptive and non-electroreceptive species. These thresholds correspond to a distance of maximally 80 cm from the electrode arrays of the simulated electric fields around the fishing gear. Our findings suggest that electrical pulses as used in pulse trawling are unlikely to elicit behavioural responses outside the nets that surround the electrode arrays.

In Chapter 5, we examined the hypothesised susceptibility of Gadidae for pulse-induced injuries by quantifying internal injuries in whiting (Merlangius merlangus) catches. We sampled specimens from pulse trawls with and without electrical stimulation, and conventional beam trawls with tickler chains to shed light on the injury origin. We visualised spinal injuries with X-radiography, followed by dissection to reveal internal haemorrhages. Both injury types were categorised on a severity scale and their location was quantified along the anteroposterior fish axis. Spinal injury probabilities in pulses-on and pulses-off catches were low (on average ≤3%) and we found no evidence for electrically-induced injuries. Severe spinal injury probability was slightly higher in tickler-chain catches (2.5%) than in pulses-on samples (0.8%) and this difference increased for smaller specimens. The locations of spinal injuries did not show a consistent pattern as previously shown in Atlantic cod exposed to electrical pulses in laboratory conditions. Severe haemorrhage probabilities were also low, but slightly higher in the pulses-on samples (1.8%) compared to fish caught with tickler chains (0.3%), especially for the larger specimens. The locations of severe haemorrhages in pulses-on catches, and a correlation with spinal injury occurrences, suggest that they may be (partly) related to electrical-pulse exposure. Overall, our results indicate that spinal injuries in whiting are rare and primarily due to mechanical impact. Severe haemorrhages may be partially related to electrical pulsing but incidences are low and coincide with a significantly lower chance for spinal injuries. Based on these findings, we rejected the hypothesised susceptibility of Gadidae for pulse injuries in general.

In Chapter 6, we focused on concerns about potential spinal injuries in fish species caught with electrical pulses. To quantify spinal injuries, we examined sixteen, widely different, fish species from catches of tickler-chain trawlers and electrical-pulse trawlers. Sampled species included common sole, dab (Limanda limanda), European plaice (Pleuronectes platessa), solenette (Buglossidium luteum), Atlantic cod, bib (Trisopterus luscus), whiting, grey gurnard (Eutrigla gurnardus), tub gurnard (Chelidonichthys lucerna), lesser sandeel (Ammodytes tobianus), greater sandeel (Hyperoplus lanceolatus), bullrout (Myoxocephalus scorpius), dragonet (Callionymus lyra), European seabass, lesser weever (Echiichthys vipera), and striped red mullet (Mullus surmuletus). To distinguish mechanically and electrically-induced injuries, we compared, for a subset of species, injuries in samples from pulse gears with electrical pulses either turned on or off. Severity of spinal injuries and their location along the anteroposterior fish axis were quantified from X-radiographs. Except for Atlantic cod and sandeels, spinal injury probability was low (<2.5%), irrespective of severity category and catch method. In sandeels, we found no evidence for electrically-induced injuries. In Atlantic cod, 40% had major spinal injuries in pulses-on samples versus 1% in tickler-chain samples. Both the location of injuries in the pulses-on samples and fish-length dependency of injury incidences, match findings for Atlantic cod in laboratory experiments. Overall, our results show that electrically-induced spinal injuries as present in Atlantic cod are not found in a wide range of other bycatch species of common-sole-targeting bottom trawling. Apart from Atlantic cod, pulse trawling is therefore unlikely to impose increased mortality on studied fish populations compared to the tickler-chain technique.

Finally, in Chapter 7, we placed our findings in a wider scientific context. We integrated the most important thesis outcomes with the existing knowledge regarding effects of electrical stimulation on marine animals. To assess the effect of electrical stimulation on organisms in a mechanistic framework, we defined zones based on thresholds for different responses around the electrode arrays. We found no evidence that organisms are affected by the electric field beyond the netting material around the electrode arrays. Electric field strength thresholds for behavioural responses, muscle activity, and internal injuries in fish are all restricted to the trawl path of the gear. No substantial negative side effects of electrical stimulation were found. Hereafter, we explored the biomimetic potential of electroreceptive and electrogenic fish species. In particular, we provided an outlook on the design of novel electrical detection and stimulation possibilities for fishing. We presented future research perspectives with numerical simulation and fishing gear innovation. Although Atlantic cod is sensitive to electrical-pulse-induced injuries, we suggest ways to mitigate this negative side-effect through gear modifications. In conclusion, we see potential to improve and refine pulse trawls and, therefore, think it would be worthwhile to further investigate such capture techniques.