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The crustacean chemosensory system: Consequences of climate and environmental change

Final Report Summary - CRUCSCHANGE (The crustacean chemosensory system: Consequences of climate and environmental change)

The overall objective of the research project has been to provide improved understanding of the combined impacts of climate change and pollutants on marine organisms, focusing on the chemosensory system of ecologically and economically important crustaceans.
Specific research objectives were to:
- Study impacts of multiple stressors from climate change and pollutants on chemically mediated behaviour.
- Identify impacts of multiple stressors on odour detection.
- Investigate the plasticity of the chemosensory system and its ability to adapt to environmental change, using Idotea baltica populations locally adapted to fully marine or brackish waters in reciprocal transplant experiments.

Mainly, the combined impacts of ocean acidification (OA) and metal pollution have been investigated, which is of extra concern since decreasing pH affects bioavailability and thus the toxicity of metals in seawater. This research project has primarily investigated effects on odour detection and downstream behaviour, such as food search. However, also other kinds of effects on behaviour and ecophysiology (e.g. general activity level, avoidance behaviour, metabolism, cardiac performance and metal uptake) have been studied, as well as effects on the immune-defence. By using a combination of behavioural investigations and physiological techniques, this project has identified effects from present and future environmental stressors on different organization level in these important crustaceans.

Main results
Within this research project, the combined effects of longer-term exposure to OA and more short-term, additional stressors from hypoxia or manganese (Mn) were investigated on the Norway lobster, Nephrops norvegicus. To get a comprehensive picture, effects on different organization level were studied, i.e. everything from behavioural and physiological effects to effects on lobster immune response to bacterial infection. Moreover, different life stages, i.e. eggs, juveniles and adult males and females, were included. So far, this has resulted in one publication (Hernroth et al., 2015) showing clear effects on bacteriostatic response in lobsters exposed to these stressors. Specifically:
- Lobsters exposed to hypoxia had a lower ability to reduce the number of bacteria after infection, while in lobsters exposed to OA or Mn, there was no reduction at all or even increased number of bacteria.
- In lobsters exposed to Mn or to OA combined with either hypoxia or Mn, the number of hemocytes (blood cells involved in their immune defence) was reduced by ~35%.
- While reduction of bacteria in lobsters was clearly affected by these stressors, the growth, survival and hemolytic properties of the bacteria stayed unaffected. Thus, it was concluded that this predicted stress scenario is beneficial for the pathogen in its host interaction.
The open circulatory system of marine invertebrates results in a continual risk of infection and thus reduced immunocompetence may have profound effect on survival. As OA proceeds, it may force the health of the Norway lobster to a tipping point if exposed to more short-term stressors such as the periodical events of hypoxia and Mn. This could impact lobster condition and biomass and may as well increase the risk for bacterial transmission to consumers.

Besides effects on lobster immune-defence, rather severe behavioural and physiological effects were found. Lobsters from the hypoxic treatment showed decreased reaction to food, while lobsters exposed to hypoxia in combination with OA had a completely abolished ability to locate food by use of odour cues. Furthermore, it was found that N. norvegicus has the ability to sense, and actively avoid, acified seawater, but that this avoidance ceased in OA-treatments combined with either hypoxia or Mn. Physiological parameters like respiration were mainly affected by hypoxia, which drastically reduced respiration rate in all life stages (by 40-80%) and also caused an increase in embryo heart rate. Respiration was also affected by OA and Mn, but in a life-stage dependent manner. Mn alone reduced respiration (by 30%) in females, but not significantly so in males or embryos. Synergistic effects of OA were found, but the outcome differed between life-stages. For embryos, OA caused a decrease in respiration both in combination with hypoxia or with Mn. In contrast, an increase in respiration was found for the adults, when exposed to the combination of OA and Mn. Altogether, the results from this experiment show that OA and the spread of hypoxia could have severe impacts on the ecologically and economically important N. norvegicus in the future. However, the effects were complex and vary greatly depending on life stage and organization level. So far, the behavioural and physiological parts of the experiment have resulted in a BSc Thesis (Mattsson, 2014) and a manuscript included in a PhD Thesis (Styf et al. 2014). Both manuscripts are currently being reformatted for publication in scientific journals. The experiment was also highlighted in national radio and newspapers and results have been presented at three international conferences and several seminars.

In addition to the different experiments on N. norvegicus, several experiments on the isopod Idotea spp. have been conducted in the project. Firstly, the plasticity of the chemosensory system and its ability to adapt to environmental changes (OA, change in salinity) were investigated, using three Idotea baltica populations locally adapted to fully marine or brackish waters in reciprocal transplant experiments. Preference of olfactory cues from food (Fucus vesiculosus) was investigated using a two-choice bioassay, to look for differences in chemosensory ability and stress tolerance between populations. However, no clear effect could be detected, partly due to low survival rate/few replicates. Trans-generational effect of heat chock treatment of gravid I. baltica was tested in another experiment, which unfortunately had to be terminated prematurely due to low number of progeny. Thirdly, the ability of Idotea granulosa to detect predator chemical cues and their influence on habitat and food choice was investigated. Despite very promising results from a pilot study, also this experiment was terminated early, due to problems with the set up (non-responding controls). Finally, the combined effect of OA and copper on I. baltica was investigated, looking at behavioural as well as physiological responses such as odour detection, general activity level, respiration and metal accumulation. Here, clear effects were found for both OA and copper on isopod swimming activity, while isopods from the OA treatment had a reduced respiration. This final experiment is currently being written up as a MSc Thesis report and will thereafter be reformatted for scientific publication.

Significance and socio-economic impact
OA is a gradually increasing, ongoing process with great concern to marine biota. Yet the knowledge of how OA will affect marine organisms is still limited, and we know particularly little about the combined effects of OA and other stressors, such as periodic events of hypoxia and pollution. Results from this research project provide new knowledge on the impacts we can expect at near future OA conditions, which will help identify risks and improve the understanding of the research field. The results may thus form a basis when authorities and policy makers develop assessment criteria to for environmental health and for new directives and legislation. The project has demonstrated severe impacts at different organisation levels of ecologically and economically important crustaceans. Not least, the results highlight that the combined effects of OA and other stressors are very complex, and susceptibility vary greatly between organization levels as well as between different life stages. Nevertheless, in several cases it was the combination of stressors that caused the most sever effects, implying future studies on interactions with pollutants and natural variables to better predict the influence of OA on marine organisms.

Crustaceans are often keystone species in coastal ecosystems, e.g. as important bioturbators and important prey for fish. Chemosensory disrupting effects of OA, or other sublethal effects with consequences on feeding/growth, reproduction, or animals’ ability to function in an ecological context, are of great ecological relevance, relating directly to individual fitness, with possible consequences to populations and marine ecosystems. Several crustaceans also form the basis of valuable fisheries, e.g. one of the model species of this project, N. norvegicus, which is one of the commercially most important fishery species in Europe, providing ca. € 200 million each year. Future deteriorating conditions for this and other valuable fishery species could have significant economic consequences to the fisheries sector.