Edited by: Heliana Teixeira, University of Aveiro, Portugal
Reviewed by: Elizabeth A. Fulton, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australia; Jean-Claude Dauvin, Université de Caen Normandie, France
This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science
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The aim of this brief research report was to define the consequential shifts in biomass and trophic structure of an ecosystem surrounding an offshore monoculture fish farm in Israel. It attempts to clarify the impact of the industry expansion and input of artificial fish pellets on functional group biomasses. We account for the direct addition of artificial food pellets, the metabolic wastes from the caged fish in a mass-balance food web model (Ecopath), as well as the temporal expansion of the farm’s production capacity to 21,000 t over a 30-year period (Ecosim). In the static mass-balance model of the food web, the addition of the fish cages at its current production size of 1000 t does not adversely affect the system, and trophic energy transfer is still dependent on primary production versus the detrital pathway. The model suggests a semi-stable ecosystem with low trophic interactions. With time, the increase in fish farming at the site is characterized by an increase of all functional group biomasses at the site over the 30-year period. The accumulation in detritus most notably correlates to greater biomass for all benthic functional niches and their secondary consumers. It is, therefore, apt to develop an indicator species list to indicate negative site disturbance. In summary, the sediment column condition will be the main indicator for ecosystem stability, as well as the increase in apex predators that are attracted to the site from the accumulation of discards at the cage bottom.
Aquaculture is a growing industry throughout many areas of the world (
The eastern Mediterranean Sea is a region afflicted by increasing sea temperature and the greatest influx of invasive marine species in the world, termed Lessepsian migrants (
Ecopath with Ecosim is a common tool for analyzing trophic flows within a given ecosystem (
This study focuses on the present-day trophic flow and community structure of an ecosystem surrounding an offshore fish farm. It is the first attempt to model the impacts from fish culture in an ultra-oligotrophic marine setting using EwE, inclusive of the microbial loop and interactions, and models the impact from increasing production 21-fold (i.e., loading of artificial pellets). The impacts to the organisms, which directly consume dissolved and particulate effluent, are specifically emphasized (i.e., primary producers, benthos and pelagic nekton). We addressed identifying in trophic structure, defined which impacts were greatest to the marine system, and how these sit within a management context for Israel, considering results from previous local studies. The trophic interrelationships and energy shifts caused by expanding the fish farm and inputting more nutrients were clarified, in order to visualize their impact on the system’s TL in terms of biomass.
The energy fluxes and trophic structure were modeled as a “snapshot” using EwE software, a static mass-balance model for a chosen period. The algorithm assumes that the ecosystem is balanced (i.e., production is equal to consumption;
where for an
The model is composed of 34 functional groups (FGs; guild of organisms occupying a functional niche) and includes 2 primary producers, 10 groups of invertebrates, squids, and plankton consumers, 15 groups of fishes (teleostei and demersal elasmobranchii), 1 group of reared fish (
Detailed FG names and all data sources may be found in the
As the artificial food pellets do not consume living biomass (
The model was balanced primarily following
The trophic flow diagram and a series of flow indices were estimated to determine the adequacy of the model’s inputs, and trophic representation of the marine ecosystem. The connectance schematic is a classic snapshot of the TL and their flows respective to each other. Flows, ecological indicators and calculated statistical estimates were considered to determine the impact of artificial food pellets and analyzed in comparison to other regional Ecopath models concerning aquaculture in the Mediterranean (assuming similar hydrographic conditions, functional niche species, and marine ecosystem characteristics;
Ecosim is a series of differential equations that estimate shifts in functional group biomass over time (
The flow diagram was typical of a 5-tier trophic outline, with primary producers and detritus groups populating TL 1, being succeeded by Demersal and Benthopelagic FGs (TL 2), and with mesopelagic and pelagic apex consumers (TLs 3–5;
Flow diagram of 34 functional group biomasses and fisheries fleets (GiliOcean, Commercial Trawler).
The detrital groups (Detritus, Discards, and Pellets) had much lower reported EE values (0.334, 0.102, and 0.319, respectively). The Phytoplankton, Benthic primary producers, and Bacteria had EE’s of 0.306, 0.462, and 0.075, respectively. Mid-range EE values for Sharks, Turtles, Dolphins were typical of a higher TL status. FGs “cages” had a very low EE, as they fed almost exclusively on artificial pellets or discards, respectively. Production/Consumption (P/Q;
Statistics, ecological indicators (
Parameter | Value | Units |
Functional Groups | 34 | |
Producer groups | 2 | |
Sum of all consumption | 185.991 | t km–2 yr–1 |
Sum of all respiratory flows | 96.593 | t km–2 yr–1 |
Sum of all flows into detritus | 283.550 | t km–2 yr–1 |
Total system throughput | 583.317 | t km–2 yr–1 |
Sum of all production | 296.416 | t km–2 yr–1 |
Mean trophic level of the catch | 2.022 | |
Calculated total net primary production | 240.241 | t km–2 yr–1 |
Total primary production/total respiration | 2.487 | |
Net system production | 143.614 | t km–2 yr–1 |
Total primary production/total biomass | 17.366 | |
Total biomass/total throughput | 0.024 | |
Total biomass (excluding detritus) | 13.834 | t km–2 yr–1 |
Connectance Index | 0.211 | |
System Omnivory Index | 0.236 | |
Ecopath pedigree index | 0.112 | |
Measure of fit | 0.606 | |
Shannon diversity index | 1.831 |
Transfer efficiency (TE) from producer groups to TL 4 was the highest, likely due to the direct consumption of artificial pellets by pelagic FGs located outside the cages in the upper TLs and increased abundance of prey for apex predators who aren’t detritivores. The mean TE from producers to TL 2–5 was 18.7%, and from detritus to these FG was 18.8% (overall 21.7%). This is slightly higher when compared to the mean TE of 19% in the Israeli EwE of
The ratios of total consumption and respiration to total system throughput (TST) are indicative of lower energy usage around the fish farm (
The keystone species of the ecosystem are: Sharks > Benthic invertebrates > Benthic cephalopods > Phytoplankton > Micro/Mesoplankton. These sentinel species’ biomass are crucial to ecosystem functionality. In addition, all fish FG TLs were in agreement (within 0.5 measure) of TL estimates that are reported in
Most planktonic groups negatively impacted on their conspecifics, indicating a competitive landscape. Negative impacts are also displayed for predators on their known prey groups (
Output of Mixed Trophic Impact analysis of selected functional groups (impacting vs. impacted). Positive impacts are indicated as blue, and negative impacts are indicated by red shades.
The linear increase to 21,000 t (over 50 km2 space and over 30 years) resulted in an increase in biomass of benthic invertebrates and some herbivorous/demersal fish groups; overall, the biomass of the system increases 1–10 times the baseline biomass of the system (
Relative biomass increases of all functional groups over 30-year period (from 1000 t farm production to 21,000 t).
The model addressed effects of increasing artificial fish pellet feeding into the system, over time, on the wild biomass surrounding the fish farm. The input parameters and resulting model’s fitness was acceptable according to measure of fit (0.611). However, the model did not address dispersion (i.e., spatial considerations) of the waste products from the farmed fish, nor was the model suitable to describe the biogeochemical implications of such a farm. It is a simple, initial description of the system structure currently, and over time. The model’s confidence was met through the PREBAL “rules of thumb” routine, abridging the system information efficiently and thoroughly, and describing the trophic structure and its temporal shift with increased fish production. This was the first EwE of a mariculture system in an ultraoligotrophic setting, and to include the microbial loop. This study also separated the microbial loop from the detritus/primary production pathways, as bacterial biomass is notably greater than in other marine regions and it is common to include this group where production is insufficient for consumption.
The inclusion of the microbial loop into the model was essential for clarifying the primary productivity and detrital pathways. The higher bacterial biomass, EE and position in the food chain indicates that it may be compensating for the very low biomass of primary producers in the basin. The input of fish pellets, although mostly consumed by the farmed fish, provides a food source/attractant for the wild populations of apex predators. Benthic groups are also impacted by the build-up of organic matter on the seawater-sediment interface (indicated by lower EE estimates). As the Ecopath model area currently has such a low biomass, this increase in organic matter may be consumed by the greater biomass of benthos. The total primary productivity in relation to total biomass was higher, indicating that the artificial pellets are not overwhelming the system as a primary producer at current levels.
The flow diagram visually complemented other Mediterranean trophic flows (the Levantine model;
The greater ratio of TPP to TB means the pellets do not replace or assume the role than primary production in the system. Most EwE models do not clarify the detrital TL 1 input so definitively. However, it was necessary to elaborate on this input to clarify a bottom-up disturbance in the trophic structure. The biomass and flows to detritus were mostly from TL 2, and the greater exports of this TL were related to the addition of fish cages. The mean TE of the Ecopath model (21.7%) was similar to the Ecopath model in Israel (TE 19%,
Other models in the Mediterranean Sea region are within 3 km of their respective shoreline, and thus experience greater nutrient availability and productivity ranges (
The key findings from the Ecopath model are that the dominance of detritus over grazing pathways in the system, and that the detrital and lower TL have significant positive impacts on other groups in the system, suggesting “bottom-up” control of the food web.
When the increase in cage production is expressed over time, the Ecosim output suggests that the detritus groups act to attract and support greater abundance in the ecosystem around the fish farm (mostly benthic and demersal species). The highest increases in biomass were in Mullets and Goatfishes (14-fold), Polychaetes and Suprabenthos (approx. 13-fold) and other benthic and herbivorous group consumers (8–12-fold). Aligning with a Greek mesocosm focusing on the effects of nutrient waste from fish cages (
For nearly all groups, the increased input of artificial pellets and resulting input of nutrients to the ultra-oligotrophic marine system only serve to bring their biomasses to within a normal range reported by other regional EwE studies not focused on fish farming (i.e., “baseline conditions”). It is noted that the only other regional EwE model for comparison was situated in lesser exposed sites, closer to shore. The pellets’ forced increase by 21 times resulted in 64 times biomass relative to the initial 63 t km–2 put in 2017. This, in conjunction with the low EE of the Ecopath model, suggests that there will be moderate to high accumulation/surplus of pellets accumulating over time. The groups which exceed the other studies are all constrained to the benthos niche (Polychaetes, Suprabenthos, Shrimps, Crabs, and Invertebrates), as a reflection of the increased particulate detritus to the farming site. The increase of discard biomass is moderate, alongside an increase in sharks near the fish farm cages. As fish production increases, the consequential effect on biomass for all pelagic groups is smaller, while benthic groups steadily increase.
This is the first attempt to clarify impacts of mariculture in a far offshore, ultraoligotrophic setting. The model demonstrated the effects from the current production levels and projected the increases to all TL biomasses over a 30 year period as a result of increased farming. The increase of soluble nutrient loading, expressed through a forcing function, increased primary production at the site, but the detrital and artificial pellets loading suggests that the surplus of accumulation may have negative implications on biodiversity as farm activity increases.
More research on the microbial loop is needed – the EMS experiences greater secondary production from of bacteria than the western Mediterranean (
Most importantly, there was no observed crash in upper and lower TL biomasses (apex predators and primary producer groups). The primary and apex producers increase moderately, with no extreme biomass fluctuations. The latter groups’ increment indicates a need for greater R&D on automated discards and dead fish removal system at the base of the case, in order to limit apex predator attraction. This study’s temporal model could also be expanded to include realistic scenarios of SST increase, acidification, salinity, invasive species, and present fisheries (i.e., trawling).
The datasets generated for this study are available on request to the corresponding author.
LL, DT, and MG conceived of the presented idea. LL and MG developed the theory. LL performed the computations. MG verified the analytical methods. DT and OA supervised the findings of this work. All authors discussed the results and contributed to the final manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The Supplementary Material for this article can be found online at: