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Feeding response of Trichomya hirsuta in different algal concentrations: A possible solution to eutrophication


Yat Long Angus Li 2016

Abstract

Eutrophication is a serious threat in Queensland waters as it caused many ecological issues. The report proposed a common bivalve species, hairy mussel (Trichomya hirsute), as bioremediation animal to reduce algae concentration in the water. It was an ex situ experiment aimed to investigate the mathematical relationship of mussels and algae in the water, the change of filtration rate at different algal concentrations, determining the optimal algal filtration rate and to examine the ability of hairy mussels as a bioremediator. Different algal concentrations of sea water were added with fix amount of mussels. The change of algal concentration in time was monitored by spectrophotometer. Results showed that algae in the water were filtered by the mussels in a linear fashion and the filtration rate increase with increasing initial algal concentration. Optimal foraging theory can explain the change of filtration rate of mussels with algae concentration. It is also believed that low filtration rate at low algae concentration was to maximising food absorption in the digestive system of mussels. However, the optimal filtration rate was not found. The potential of hairy mussel as a bioremediation species is confidently acknowledged. 

Introduction

Sea water quality in Queensland is deteriorating due to severe pollution in coastal areas. Agriculture, sewage discharge, sediment dumping and other anthropogenic activities have caused excess nutrients (such as dissolved nitrogen, phosphorous and sulphur), to enter the marine environment, resulting in eutrophication of Queensland coastal waters (Waterhouse et al., 2013). Eutrophication is a complicated environmental issue occurring in many countries around the world, including the Great Barrier Reef (Galimany et al., 2015, Waterhouse et al., 2013). Eutrophication degrades marine ecosystems by increasing the phytoplankton reproduction rate and biomass (Møhlenberg et al., 2007). This occurs because, dissolved inorganic nitrogen and phosphorus are instantaneously and entirely bioavailable for algal growth (Waterhouse et al., 2013).This is especially harmful to marine habitats, as excess planktonic activity can reduce light penetration and reduce the oxygen level in the water, leading to reduction of photosynthetic rate in seagrasses and corals and suffocation of marine macrofuana (Møhlenberg et al., 2007; Lindahl et al., 2005). Algae concentration in the GBR region increased during runoff events, in which nutrients from catchment areas were flushed down to the sea through rivers and estuaries. This increased water turbidity and was stressful for seagrass meadows and coral reefs. It is also believed that algal blooms caused by excess nutrients are the major trigger for coral-eating crown-of-thorns starfish (COTS) outbreak in the Great Barrier Reef (GBR) (Brodie et al., 2005). This is because high concentration of algae provided sufficient food source for planktotrophic COTS larvae which enhanced their survival rates (Brodie et al., 2005).

Phytoplankton is a group of single-celled algae, with diatoms and dinoflagellates being  most common in marine environment. They are called the “grasses of the sea” because they are at the very bottom of the marine food web and they are autotrophic. These algae contain at least one form of chlorophyll pigment and thus are able to utilise energy from sunlight to convert CO2 into sugar and protein molecules. Phytoplankton also require the presence of nitrogen and phosphorous in order to reproduce and grow (Suthers et al., 2009). Phytoplankton are grazed by zooplankton, krill and other filter-feeding organisms such as sponges, errant polychaetes and bivalves (Ruppert et al., 2004).

Bivalvia is a class within phylum Mollusca, consisting of approximately 8000 species, 6700 being  marine species, such as mussels, oysters, scallops and crockles. Most  bivalves are suspension feeders, whereas others are deposit feeders and carnivores. Marine mussels are filter-feeding bivalves under the family Mytilidae, which have a diet comprised mostly of suspended plankton (Ruppert et al., 2004). The filtering ability of mussels has been recognised as a sustainable solution to bioextract nutrients in over-enriched areas and improve water quality (Galimany et al., 2015). It can also be farmed through aquaculture and provide food for human needs, which recycle nutrients from sea to land (Lindahl et al., 2005). This is also because they can tolerate wide range of abiotic factors, such as temperature, oxygen level and salinity (Lopez et al., 2014).  Although they are filter-feeders, the bivlaves do not consume all the particles trapped by the lammellibrach gills. This is dependent on the characteristics of the particles, such as size, shape, membrane structure and biochemical composition (Galimany et al., 2015). Both organic and inorganic unwanted but retained particles are excreted as pseudofaeces (Effler et al., 1996). However, the molluscs may also metabolise and accumulate pollutants from the environment in their body (Ruiz et al., 2013). Therefore, they have also been used as a spatial environmental tool for detecting accumulated pollutants within the mussels (Lopez et al., 2014).

The target species of this report is Trichomya hirsuta (hairy mussel). This bivalve is not a commonly studied species, but is very abundant in eastern and southern Australia, from Cairns to Tasmania. They mostly live in the intertidal and subtidal zone, forming clumps or attached to rocks on the sea floor (Queensland museum, 2016; NSW Department of Industry, 2016). The aim of the report is to 1. investigate the mathematical relationship of mussels filtering algal cells, 2. the change of filtration rate at different algal concentrations, 3. determining the optimal algal filtration rate of hairy mussels and 4. as a pilot study to examine the ability of hairy mussels as a bioremediator to improve Queensland water quality.

Materials and Methods

Experiment Design
The hairy mussels used in the experiment were collected in the Moreton Bay Region, Australia. The mussel clumps were cleaned to remove the mud, as well as to divide them into individual bivalves. Encrusted animals on the mussel shells were also removed to prevent biased results. The cleaned mussels were then stored at the University of Queensland’s aquarium for a week to calibrate with synthetic salt water and allowing the mussels to recover after the stressful treatment. It was also ensured that live mussels were used with empty stomachs to ensure a consistent experimental setup. Approximately 100g of mussels (7-10 individuals) were placed in 18x8x8 cm plastic containers with 500ml of filtered sea water. All mussels were submerged in the water. Different volumes of algae solution was added to each of the individual containers with sea water, creating ten arbitrary concentrations with three replicates each (n=30) (Fig. 1&2). The algae solution used in the experiment was a commercial shellfish diet, consisting  of Isochrysis,Pavlova, Tetraselmis, Chaetocerous calcitrans, Thalassiosira weissflogii and Thalassiosira pseudonana (Fig. 3) Positive and negative controls with three replicates each were also deployed in the experiment, algae-only and mussels-only.
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Figure 1
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Figure 2
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Figure 3

Water and Statistical Analysis

A spectrophotometer was used to determine the amount of algae in the water by detecting chlorophyll a absorbance. Water samples were measured at 30 minute intervals. Each of the 30 replicates was treated as an individual setup. The results of each setup was tested with linear regression. The slopes of each individual linear model were also tested with a linear regression against their initial chlorophyll a absorption.

Results

All algae concentrations decreased with the presence of mussels, while the concentration of the algae-only setup remained unchanged. By comparing the initial and ending setup, the change of water colour can be observed easily with the human eye. The lighter initial concentrations had changed from slight yellow into clear water, and stronger concentrations went from dark brown water to light orange (Fig. 2&4). Set up with initial absorbance below 0.4λ can clear the water into 0λ with three hours.

From figure 5, it can be seen that algae concentration was decreasing in a linear fashion. Linear regressions of all 30 setups showed that 28 setups can be largely explained by a linear model with R2 values higher than 80%. Figure 6 showed that the slopes of each setup had a significant negative relationship with their initial chlorophyll a concentration (r2 = 0.93, p = 2e-16). This indicates the lines of best fit of the setups were steeper, with increasing initial algae concentration. No trend or plateau can be observed in figure 2.  
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Figure 4
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Figure 5
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Figure 6

Discussion

The mussels were remediating the algae in the water

The hairy mussels directly caused the decrease in algal concentration, demonstrated by the difference between the algae-only treatment and other setups with mussels. It can also be observed that the shells of the mussels were opened and generating a water current (Fig. 7). The mussels tended to filter algae cells in a linear fashion. This suggests that the filtration of mussels is highly regulated and in proportion with time. Water condition can be classified into 3 categories; below 0.1λ  chlorophyll a absorbance as light pollution, 0.1-0.2λ as heavy pollution and over 0.2λ as unrealistic situations, solely by the transparency and colour of the experiment water. From this experiment, it can be deduced that 100g of hairy mussels should be able to purify 500ml of light and heavy polluted sea water into clear water within 2 hours.  The experiment also showed that hairy mussels responded to different initial algal concentrations by changing the filtration rate. The mussels filtered sea water more rapidly when the initial algae amount was high, illustrated by  the steepness of the linear models increasing linearly with increasing initial concentration. Due to the time constraints with a limited concentration gradient, the optimal filtering ability of hairy mussels was not determined as there was no sign of a plateau in the slopes along mussels treated with different initial concentrations. As a pilot study, the filtering ability of hairy mussel as a bioremediation species is positively recognised.

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Figure 7

Optimal foraging theory applied on mussels

Mussels are very adaptive bivalves. Galimany et al. (2015) has shown that the atlantic ribbed mussel, Geukensia demissa, can adapt its feeding response from a low plankton environment to high organic particles within 6 days. The study also suggested that the ribbed mussels had an increased filtration rate in response to the high concentration of particulate matter. Conversely, Gascoigne et al. (2007) demonstrated that there was a very strong positive correlation between the valve gape aperture of the blue mussel, Mytilus edulis, and chlorophyll a concentration in the water column. This suggests that blue mussels open wider with high food availability, and thus filtered more algae. These results corroborate with the experimental data of this study, which observed that the chlorophyll a decreased more rapidly in higher initial concentration algal treatments, relating to the optimal foraging theory.

Mussels tend to stop feeding at very low algal concentration because the energy spent for obtaining food particles exceeds the energy gained from food. Therefore, feeding in such an environment is not economically efficient (Gascoigne et al., 2007). Mussels conserve energy and wait for better conditions. This explains the lowered filtration rate of hairy mussels in the light pollution setup. This is because the environment was not rich enough for the mussels to spend more energy to obtain algae cells. On the other hand, the heavy and unrealistic setups were worth more energy input from the hairy mussels to obtain algal food. In additional, the lower filtration rate suggests that food particles were retained longer in the  digestive system of the mussels , improving the absorption efficiency to compensate for the lack of food availability in the environment (Galimany et al., 2013).

Successes of mussels improving water quality

Mussels are generally better bioremediators compared with other filter-feeding bivalves. This is because mussels are less responsive to environmental change and retain high filtering efficiency in different conditions (Macdonald and Ward, 2009).

There have been multiple incidences of zebra mussels restoring nutrient polluted natural fresh water systems in the US (Glaser et al., 2009). The study also showed that a 50% reduction of zebra mussel populations can result in a boost of algal concentration up to five-fold. This was primarily due to zebra mussels filtering plankton and extracting nutrients in the environment. As a result, zebra mussels greatly improved water clarity. Zebra mussel invasion in New York Seneca River have been observed to turn the plankton rich ecosystem into low plankton environment, greatly increasing Secchi disc transparency (Effler et al., 1996).

Møhlenberg et al. (2007) documented the change of water quality in Skive Fjord, Denmark with blue mussel populations. The study stated that large numbers of mussels can improve water transparency and reduce algae concentration in the water, thus increasing primary production of the ecosystems. The study also suggested that if the mussel population is large enough, the potential filtration volume of blue mussel may exceed the total volume of water in the system (Møhlenberg et al., 2007). Lindahl et al. (2005) stated that blue mussel farming in Gullmar Fjord in the Swedish coast has reduced 20% of nitrogen transport, also proposing to the species be used in the aquaculture industry as a cost effective method of sustainable food production.

Doubt in food safety of bioremediation mussels

Eutrophication of marine water is due to excess nutrient input from terrestrial sources, however it is very rare that nutrients are the only pollutant in such environments. Runoff, dumping and sewage discharge often bring in a variety of pollutants to the water systems, such as bacteria, heavy metals and other noxious waste. If an area requires mussels for bioremediation and nutrient extraction, then such mussels should not be participating in commercial aquaculture food production. Food safety is of major concern because the mussels are sessile filter-feeding animals and their body directly reflects the level of pollution in the environment (Brenner et al., 2014). Mussels do not significantly metabolise ingested pollutants from the water (Walker and Macaskill, 2014). Instead, they accumulate organic contaminants, heavy metals and microplastics in their digestive cells. Additionally, mussels in polluted environments also have higher chances to contract gonadal neoplastic disorders. This is because polluted water with PCBs has higher mutagenic potential in filter-feeding molluscs (Ruiz et al., 2013). Furthermore, there were exceptionally higher numbers of human pathogenic bacteria found in mussels after runoff events, such as Escherichia coli, Salmonella spp, and Giardia cysts (Tryland et al., 2014). Ingestion of mussels in polluted areas may cause long term and immediate health issues. 

Conclusion

More study should be done on the hairy mussel, Trichomya hirsute, exploring the filtering ability as bioremediation in Queensland coastal waters. Factors such as optimal filtering ability should be investigated, as well as methods to increase mussel populations and the impact of mussels in the ecosystems. This pilot study has indicated that hairy mussels can be a potential species for bioremediating Queensland waters to relieve current stresses in the GBR. However, it is not recommended to commercially farm hairy mussels in polluted sites for human consumption, as the issue of food safety remains unsolved. 

Acknowledgements
Thanks to our course coordinator, Bernard Degnan, and the tutors for providing assistance and professional advice. Also thanks to my colleagues who has helped in the experiment and the report. Last but not least, thank God for giving me inspiration and strength to complete this report. 

References

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