Edinburgh Napier University

  Anthropogenic sound has profoundly changed the acoustic environment of aquatic habitats, with growing evidence that even a short exposure to man-made sound sources can negatively affect marine organisms. Marine invertebrates have received little attention regarding their responses to anthropogenic sound, despite their pivotal role in marine ecosystems, and preliminary evidence of their sensitivity. In this thesis, I critically review the methods used in studies investigating the effects of anthropogenic noise on marine invertebrates. I identify methodological trends that have developed along the timeline of this topic, and use this information to suggest three research strategies to further the development of research in this field. From this review, current knowledge gaps are identified, and two main routes to address them are taken in this thesis.
Firstly, to address the shortage of particle motion data in anthropogenic sound literature, two new low-cost and easily accessible particle motion sensors were developed and tested, one of them at 0.1% of the cost of currently commercially available models. These sensors will allow the measurement and reproduction of the sound fields experienced by marine invertebrates in bioacoustic research, even when research budgets are tight. Particle motion is the main sound component detected by invertebrates, yet neglected in many aquatic bioacoustical studies.
Secondly, to expand on the comparably small quantity of research investigating the effects of anthropogenic sound on marine invertebrates, a series of controlled laboratory experiments were conducted. Two commercially and ecologically important model species were chosen, the blue mussel Mytilus edulis, representing sessile benthic invertebrates, and the European lobster Homarus gammarus, representing mobile benthic invertebrates.
Experiments on M. edulis were conducted taking a mechanistic, integrative approach to investigate the effects of sound on multiple levels of biological organisation, including biochemistry, physiology, and behaviour. The ultimate aim was to understand the underlying drivers behind, and interactions between, responses. Comet assay analysis of haemocytes and gill cells demonstrated a significant six-fold higher single strand breakage in the DNA of cells of mussels exposed to ship-noise playback, compared to those kept under ambient conditions. Superoxide dismutase analysis did not identify an excess of superoxide ions, and glutathione, and glutathione peroxidase assays showed no increase in either glutathione or glutathione peroxidase. TBAR assays however revealed 68% more thiobarbituric acid reactive substances, indicating lipid peroxidation in the gill epithelia of noise exposed specimens. Algal clearance rates and oxygen-consumption rates of noise-exposed mussels were significantly lower (84% reduction and 12% reduction respectively), than those of control animals, while valve gape was significantly (60%) wider. This seemingly converse reaction indicates a shock response in mussels with the onset of noise exposure. Finally, at the genetic level, heat shock protein 70 expression was investigated, but no change was identified during noise exposure.
Investigation into the noise induced behavioural responses of H. gammarus suggests seasonal differences in behaviour, using movement as a metric, in response to anthropogenic noise playbacks. During both summer and winter exposures, lobsters spent most time away from the highest noise area (98% of the observed time in summer and 78% in winter). The observed seasonal differences in the time spent in the highest noise area (2% in summer and 22% in winter) could be linked to the lobsters’ requirement for shelter during winter. This requirement seems to have had a stronger influence over the animals’ behaviour than any desire to avoid high noise levels.
The information generated in this thesis can be used by researchers working in the field of marine sound to develop well rounded studies exploring the effects of sound on not only marine invertebrates but other faunal groups as well. The construction details provided to produce low cost particle motion sensors, will allow bioacoustic researchers to easily include particle motion measurements in all future studies investigating the effects of sound on fish and invertebrates. The results of the conducted mussel and lobster experiments evidence how multiple aspects of invertebrate biology can be affected by noise. The observed impacts on both sessile and mobile life forms highlight that the effects of noise cannot be fully understood before a wide range of species with different biological and ecological traits have been studied. The integrative approach to noise research used here can serve as a model for other species, and the results pooled to inform governments and industry of the effects of anthropogenic noise in the marine environment.