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Investigations on Eurythoe complanata’s potential as a bioremediator specie for off-shore aquaculture
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Mallory Manon Bovey 2017
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Abstract | |
Annelids compose 40-60% of the marine benthic macro fauna, and are key actors in nutrients recycling within the ocean sediment. Through their bioturbating activity, they absorb and disperse organic matter. As such they could be considered as a bioremediator species buffering the accumulation of fish wastes released below and around aquaculture off-shore cages. This study investigated wether Eurythoe complanata showed behavioral reaction when benthic sediment they inhabit is loaded with commercial fish feed. Mobility and burrowing activity within sediment experimentally enriched in Tilapia feed at various concentrations. Total distance covered and time spend exploring were significantly lower when high quantities of fish feed were present in sediment; E. complanata did not make any attempt at burrowing in enriched sediment. Behaviors such as sediment-exploration and burrowing are intimately linked to bioturbation; these results thus suggest low potential for using E. complanata as a bioremediator against off-shore fish farming pollution. They also highlight the necessity to investigate further ways of buffering aquaculture’s environmental impacts.
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Introduction | |
Ecological importance of annelids
Annelids constitute a major part of the marine benthic community, in terms of numbers of individuals and number of species (Hutchings et al.,1993). By burrowing and feeding within the sea bed, they enhance the sedimentary processes; bioturbation, biodegradation, biosuspension and resuspension of organic matter (OM) indeed participate in the recycling and redistribution of nutrients (Hutchings, 1998, Gibson et al., 2001). Such processes modify the geochemical conditions of the sea floor (Lopez & Levinton, 1987), accelerating mineralization, while enhancing aeration (Kristensen, 1988). Sediment-dwelling annelids thus allow other animals and microbes to thrive. Annelids show diverse feeding strategies, with a great variation between species. Mud-swallowing, carnivory and herbivory are common (Fauchald & Jumars, 1979), while suspension and deposit-feeding are the most frequently observed (Snelgrove et al., 1997). Deposit-feeding annelids absorb organic matter trapped in sediment, digest it and displace it; they play a key role within the marine food chain by redistributing nutrients (nitrate and phosphate), notably by increasing the sediment-surface interface (Kristensen, 1984). The exchange of mineralized nutrients and organic matter is sped up. The bioturbation activity of annelids has been studied closely, because they dissipate excess (organic as well as non-organic) material fallen onto the sea bed, they could potentially function as bioremediators; studies has shown that genus such as Capitella, inhabitants of organic-rich sediments, as their presence is linked to that of microbes, are involved in the decomposition of oil pollutant in marine sediment (Holmer et al., 1997; Cuny et al., 2007). Hansen & Blackburn (1992) found that Nephtys sp. enhances sulphur reduction rate, by displacing organic matter deeper into the soil. Similarly, Grossi et. al. (2002), showed that the bioturbation and biodegradation activity of benthic organisms significantly impacted the fate of petroleum hydrocarbons in marine sediment after a simulated oil spill. The beneficial role of annelids on polluted sediment has been assessed many times.
Coping with increased organic matter
As they develop, human activities increase their pressure on the environment. Organic enrichement of marine waters is often linked to strong disturbances in ecosystems through the process of eutrophication (Smith & Schinder 2009). Sediment-dwelling species could help buffer negative impacts as they naturally enhance nutrient recycling. But if accumulation of organic matter on the sediment is important, the recycling activity of bioturbator species might be outreached, putting the surrounding ecosystem at risk. The extend to which annelids and the benthic communities react to increased loading of nutrients has been studied. The work of Diaz & Roesnberg (1975) and Hyland et al. (2005), among many others, revealed that an overabundance in OM can reduce species richness, abundance and biomass. Overloads of OM indeed lead to reduction of oxygen and accumulation of toxic by-product of nutrients fermentation. However, Venturini et al. (2011), found that annelids assemblages are not impacted as much by the quantity of nutrients fallen on the sea floor, as by its quality. Similarly, George (1964) highlighted a fundamental aspect of bioturbators’ biology: they don’t process organic matter homogeneously, but selectively in regard to their metabolism and the bioavailability of nutriments. This suggests that the bioremediating effect of annelids (through sediment reworking) could vary with the sediment’s composition. We need to question further what are the type of marine pollution they could help to buffer.
Off-shore aquaculture and the release of fish food in the marine environment
One of the cause of marine sediment enrichment in OM is the recent boom of off-shore aquaculture. Today, aquaculture is the fastest growing animal food producing sector (FAO 2016). To keep up with the present demand, production is increasing rapidly, as is the release of fish waste. High amounts of feaces and uneaten food are released in the near-cages environment, and accumulate on the seafloor. This concerning phenomenon has been widely investigated (McGhie et al., 2000; Cromey et al., 2002; Sarà et al., 2004). Limiting the accumulation of organic matter in the environment thanks to bioremediator species is the aim of Integrative Multi-Trophic Aquaculture (IMTA; see Hughes et al., 2016; Neori et al., 2007): a fish farming design that propose to re-use organic wastes from cages to feed and grow other species.
Sea urchins are already used in some IMTA to absorb organic wastes fallen on the sea floor (Cook & Kelly 2007, Zamora et al. 2016). Not only are they beneficial in maintaining the benthic compartement healthy through sediment reworking; they have a high economic value. While this isn’t the case for annelids, their active use as bioremediators could be facilitated by their abundance and their presence in almost every benthic marine and estuarine sediment (Fauchald, 1977). Annelids, because they are strong bioturbators, could indeed be investigated as complementary bioremediators in off-shore fish farms. But first, we need to question wether they would thrive within sediment containing high quantity of fish feed as nutrient source.
I propose to investigate wether annelids’ behavior is modified when put in fish-feed riched sediment.. The following behaviors were monitored, as proxy for global health state: 1. Mobility: total distance traveled in a certain amount time, as well as time spent exploring sediment. 2. Burrowing activity: the number of attempts at burrowing in a certain amount of time. These behaviors are indeed essential to the bioturbation of sediment, and as such, critical to the annelids’ role as bioremediator. I aim to observe wether the presence of fish feed in the sediment will alter the annelids’ behaviors that are associated with their ecological function within the seafloor.
I used Eurythoe complanata (Pallas, 1766) as my model organism. Because it was easily accessible and possesses typical characteristics of sediment-dwelling annelids, it is a satisfactory model to study behavioral reactions to sediment enrichment. E. complanata belongs in the Polycheates class, order Amphinomida and family Amphimomidae (Beesley et al., 2000). It is most commonly known as Fireworm; it is indeed most often red, with ubiquitous bristles protruding from each parapodia; its appartenance to the polychaetes class is obvious from its body segmentation. Each segment carrying paired parapodia and setae that are used for locomotion, typically by peristaltism (Pardo & Amaral, 2005). E. complanata is found in tropical intertidal waters, subtropical waters, and have also been recorded in abyssal zones and polar regions (Kudenov 1993). Its habitat range is in fact very wide, and such a breadth in distribution has been correlated to its typical, simplistic morphology (Klautau et. al, 1999). This makes E. complanata a good model to study the extent to which annelids could integrate IMTA as bioremediators; as it could be implemented in farm in all climat. The absence of jaws, teeth and papillae, along with a highly develop sensory system suggest that Amphinomids will feed on decomposing organic material. The species is omnivorous and scavenger (Blake et al. 1995). As showed by Pardo & Amaral (2005), E.complanata react very quickly to food smell. They observed almost immediate feeding response fish was introduced in the worms’ container. I expect strong, swift reactions from E.complanata specimens when put in proximity to fish feed, with increased general response with increased food concentration.
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Materials and Methods |
Animal collection | |
E.complanata specimens were collected from aquariums of the University of Queensland facilities. I chose worms of roughly similar size; the selection was done were worms were moving, body extended. Sizes selected vary between 5.0 and 8.0 mm. While the experiment was running, worms that were not tested were kept in a 12x12x6cm plastic container filled with sand and water from the aquarium. They spent for approximately 30 minutes in the plastic container before the experiment began. The sand used throughout the experiment comes from the same aquarium. All observations were done at room temperature (20-23°C).
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Small video clip showing specimens of Eurythoe complanata exploring sediment from their UQ aquarium. Filmed on the 25th of May 2017.
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Set-up | |
Using six-wells Greener plates, I allocated six wells per each treatments (five types of sediment composed of sand + fish feed, in variable ratios: 0, 25, 50, 75 and 100% of fish food (FF), completed by sand), and six wells as controls (no sediment). One worm monitored in each well, as to obtain six replicates per treatment and 6 replicates for control. Fish food used was Tilapia feed pellets, obtained from A. Barnes laboratory. FF was crushed using a grinder bowl, from the original pellets to a rough powder. Sand was scooped from the worms’ container. Care was taken to select sand as fine as possible in order to match the FF powder. Excess water was removed by gravity. Measurements for the 25, 50 and 75% treatment groups’ sediment mixes were done using a 14ml Falcon tube, filled with FF dose first and complemented with the sand. Sand and FF were then mixed as homogeneously as possible on a 12x12cm plastic plate. For each treatment, a small amount of sediment (sand, 100% FF, or mix) was laid in the plates’ wells, and spread homogeneously on the well bottom. The layer was thick enough that it covered the well plastic, but as thin as possible so potential tracks from the worms would be visible. Small quantities of salt water from the worms’ container were added until the sediment was covered by 1-2mm of water, approximately.
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Mobility: Distance travelled | |
Position
of each worm from the centre of the well was estimated by superposing a
bull-eye target above each well, with concentric lines separated by 2 mm (see figure 1). First
inner circle is the one centred around the centre point of the well, and has a
4mm diameter. At the centre of the trials, worms were “centred”: put inside the
inner circle. Maximum distance from centre was 14mm (8th concentric circle).
Position was recorded based on the worm’s head position relative to the
circles. Each minute, for a total of seven minutes, a picture was taken and the
position of the worm was recorded. Head halfway through first and second line
was counted as position of 1mm, head on the second line, distance of 2mm, etc.
Timing started when the first worm was centred.
Total
distances travelled were calculated by adding the differences between the
positions recorded during the seven minutes interval.
Example:
Figure 2 shows position data for one of the worm in the control group.
Total
distance travelled was calculated as: 2+4+2+0+1+1+1 = 11.
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| Figure 1 |
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| Figure 2 |
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Mobility: Time spent exploring the sediment | |
Middle zone of wells is here defined as the space between the first inner circle (4mm ø, around well center) and the most extern concentric circle (8th from the center, ø 36mm). Worms spending time inside this zone are considered as sediment-exploring. In contrary, worms that
- stayed within the inner circle (where they were put at the start of the trials),
- stayed put against the wells’ walls,
- started climbing the wells’ walls
were considered not to show sediment-exploring behaviors.
Worms that swam directly to the edge of the wells after they’ve been centered, and never return in the middle zone, were counted as having spent 0 min in the middle zone. (most of the time, worms reaching the wells’s wall would indeed stay “floating” there in the thin layer of water suspended between the wall and the sediment).
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Burrowing | |
Burrowing behavior was monitored as a count of attempts at burrowing during seven minutes intervals. One attempt for each time a worm started to cover itself in sand (see figure 3). Sand was then gently removed to pursue the monitoring. For this set of measurements, the control was set to be the 100% sand group (only sand, no fish food). The treatment groups were as for above: 25, 50, 75 and 100% fish food.
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| Figure 3 |
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Data Analysis | |
All
analysis performed in R Studio 0.99.484. Differences between groups for
distances travelled, time spent sediment-exploring and burrowing attempts where
investigated through one-way ANOVAs (significance threshold alpha set at 0.05).
For these two first data sets, identification of significantly different groups
was done thanks to TuckeyHSD tests.
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Results |
Mobility: Distance travelled | |
The total distance travelled by worms seemed significantly impacted by the composition of the sediment (one-factor ANOVA: F5,29 = 5.56, p-value = 1.03 x 10-3). Significance differences in travelled distance were indeed found between control group and 100% sand group, and between 100% sand group and 100% fish feed group:
Worms showed a greater mobility (in term of travelling distance) when moving in sediment composed of 100% sand than when moving on the bare bottom of plastic wells (TukeyHSD test; difference in means = - 9.33mm, adjusted p-value = 3.22 x 10-4). They also covered a greater distance when moving through sediment made of 100% sand than when moving in 100% fish feed (difference = -6.60mm, adjusted p-value = 2.23 x 10-2).
Total distances travelled were similar among the various ratio of fish feed-to-sand (i.e. between the 100, 75, 50 and 25%FF groups.).
Results can be visualized in figure 4.
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| Figure 4 |
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Mobility: Time spent exploring | |
Statistical analysis revealed that the composition of the sediment significantly impacted the time that worms spent exploring it (one-factor ANOVA: F5,30 = 16,58, p-value = 7.46 x 10-8).
On average, worms spent more time exploring sediment when it was only sand than when it has a high concentration of fish feed (TukeyHSD test; difference in means = -4.67 min in the 100%FF group, p-value = 1.04 x 10-3, / - 5.83 min in FF50% group, p-value = 4.47 x 10-5 / - 5.67 min in FF75% group, p-value = 7.03 x 10-5). No significant difference between time spent exploring in sand and the mix with lowest feed fish concentration (25%).
Significant differences where also found between the control and the groups subjected to a blend of fish feed + sand. The worms spent more time moving around the middle zone of the wells when they were empty (control), with no sediment, than when they were layered with the blends of fish feed and sand, regardless of the FF:sand ratio.
The strongest difference was between the control group and the 75% FF group: worms spent more time on average (+6.67 min; TukeyHSD test: p-value = 4,7 x 10-6 ) in the middle zone when wells were empty than when they contained sediment composed of 75% fish feed.
The smallest significant difference was between 25% FF and control groups: on average worms in control group spent more time (+4.83 min, p-value = 6.70 x 10-4).
Time spent exploring the middle zone was not significantly different between the control and 100% sand groups.
No significant difference were found between the FF + sand mixes groups, i.e. between the 25, 50 and 75%FF groups.
Results can be visualized in figure 5.
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| Figure 5 |
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Burrowing | |
The only attempts at burrowing were recorded for worms of the control group (100%sand). In this group, worms would cover themselves in sand and disappear very quickly (in a few seconds). When dug out, most of them (five out of the five that actually burrowed) crawled along a small distance before they started to burrow again. One-factor ANOVA: F4,25 = 15.97, p-value = 1.30 x 10-6).
Results are presented in figure 6.
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| Figure 6 |
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Discussion |
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The idea to monitored specifically the time spent within the sediment, “exploring” it, came while doing the first set of measurements on the distances covered by Eurythoe complanata. Indeed, it appeared early on that focusing only on the total distances would not reflect the worms’ affinity for a sediment type over any others; this is because greater distances are covered by worms crawling directly from the centre to the edges of the wells. This behavior was observed consistently for the treatment groups where the fish feed concentration was the highest: mean distance travelled = 14 mm for the 100, 75, 50 and 25%FF groups. In almost every of these groups, all replicates did a single “crossing” from the centre to the edges during the first minutes and would not move back to the middle zone. Instead, worms would remain there, still, floating in the build-up of water between the sediment and the plastic walls (see figure 7). Some worms would even start climbing up the walls. In such case a big distance was recorded (14mm, the distance from the first inner circle to the most extern). However, it cannot be fairly associated with any kind of sediment-processing behavior, or any sign of the worm feeding, scavenging, burrowing, reworking (bioturbating) the sediment.
Worms did however seem to cover significantly greater distances (within the seven minutes intervals) when moving through sediment devoid of fish feed (+ 6.60mm when sediment was only sand, see figure 1). Then their mobility could more fairly be associated with their functional role of bioturbation, as they spent time actively exploring the sand, moving back and forth between the inner and outer parts of the wells. The significant difference suggests that E. complata would be more willing to inhabit and function normally in sand without fish feed.
Even though greater distances (in FF groups) could not fairly be associated with a preference for a type of sediment, because they actually lead to the worms “escaping” the sediment, I decided to keep, and present, these results; it was quite interesting to see the promptness with which the worms reacted to the presence of fish feed. The general behaviors observed were extremely different between worms evolving in their “natural” 100% sand environment, compared with a fish feed-richsediment.
Similarly, results related to burrowing behavior have to be considered together with results obtained from measuring the time spent exploring the middle zone; indeed, the shorter exploration time of worms in group FF100% is partly explained by the fact that none of them tried to burrow. In contrary, worms from group 100% sand stopped crawling regularly to burrow themselves. This could clearly be associated with their longer exploration time (+5.83 min spent exploring when sediment was only composed of sand compared to it was made of 75% fish feed). The fact that no worm in the treatment groups started burrowing suggest that E. complata would not show normal behaviors in sediment enriched with fish feed. Burrowing is crucial to annelids’ bioturbation activity (Hutchings, 1998), as it moves nutrients and organic matter vertically within the sea floor; annelids that don’t burrow within polluted sediment wouldn’t be efficient as bioremediators.
For the three set of behavior measurements, no significant differences were observed for the different levels of fish feed concentration. This suggest that E. complata react more strongly and promptly to the presence of fish feed than to its quantity. When they studied the mobility and foraging behaviors in E. complata, Pardo & Amaral (2005) also noted that the worms reacted extremely quickly to food smell and showed immediate feeding response. They linked it to their highly developed chemosensory system (worms from the amphinomidae family lack jaws, teeth and papillae; they instead rely on their senses to find decaying food). Such swift reactions were expected; the absence of differential response to various levels of FF could be associated with the very strong smell sense; E. complata detect and react to fish food as strongly when in low concentration as in higher concentration. In our experiment however, if strong reactions where obvious, no sign of feeding on the fish food has been observed.
If annelids within benthic communities were found to react strongly to small quantities of fish food, and were repelled from it instead of being attracted to feed on it, it would discard the possibility of using them as bioremediator in highly polluted sediment.
Set-up limitations
There is a lot to be said on the (absence of) accuracy with which the present set-up mimics the field conditions. I would emphasis especially on the difficulty to obtain a blend of crushed fish feed and sand. My first intention was to use a fine sieve to select together particles from similar size range. That would have reduced the effect of particle size on the worms’ behavior. Surface deposit-feeders (such as E. complata) are indeed known to be highly size-selective in their interaction with sediment/food particles; they collect and sort them by size (Fauchald & Jumars, 1979) before ingesting them. When monitoring variation in behavior between sediment types, significant differences could be wrongly associated with the nature of the particles, when they are in fact linked to their size. Unfortunately, I could not access to such sieves. The blend was hence quite rough, and heterogenic in particle size. A major issue was also the fact that fish feed tends to float on top of the sand rather than to mix with it. This could have bias observations by shielding the sand from the worms, that were quite “coated” in fish feed, and prevented from burrowing in it. Fish feed particles would show different characteristic in the field; they would notably be smaller. Thus, observations made within experimental conditions may differ greatly from what could be seen in the field. The fact that fish feed was so difficult to mix with sand can also highlight the question of how waste from fish cages will be able to be “absorbed” in the environment. If wastes do not mix in sand, but rather accumulate on the sea bed, it wouldn’t even be accessible to the endobenthic micro and macro fauna. This would obviously prevent any of these organisms to act (or to be used) as bioremediators.
My study used mobility as a proxy for general health state of the annelids; further skills and advanced material could be used to monitor behaviors more precisely. For exemple, measurements of feeding rate, burrowing patterns, digestion, excretion and reworking rates could help understand wether annelids maintain their ecological function as bioturbators in enriched sediment.
Besides its limitations, I believe that this study is a good starting point in assessing the tolerance of benthic annelids to fish waste pollution. Indeed, if fundamental behaviors such as mobility (which cover foraging, sheltering, mate seeking, predation, migration, etc.) are negatively impacted, it could be expected that their beneficial roles would be greatly impaired below fish cages. Current assessments of the ecological impacts of aquaculture should include further studies on the relationship between sediment loading and bioturbator species.
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Acknowledgements | |
I would like to thank Bernie & Sandie Degnan for their inspirational lectures, guidance, and precious help for the realization of this project. Many thanks to the lab assistants that were always so helpful and patient. The whole course and this project taught me tons and tons about the fascinating life of marine inverts, and were thoroughly enjoyed!
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References | |
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