I wrote this term paper for my Chemical Oceanography course, and I hope it contains some useful material.
Please cite any reference to it as:
Vaz, AC (University of Hawaii at Manoa). Fisheries and nutrient cycling. 1drop [blog on the internet]. [Honolulu (HI)] : [publisher unknow]. 2008 May – [cited “when you cited”]. Available from: https://1drop.wordpress.com/fisheries-and-nutrient-cycling-what-is-the-link/
(See here more about citing blogs here: http://www.ncbi.nlm.nih.gov/books/NBK7266/#A61030)
Nutrient cycling is essential to the maintenance of any ecosystem. It can be defined as the chemical alteration of nutrients and/or the flux of nutrients between different compartments, such as organisms, habitats or even ecosystems (Vanni, 2002). Even while allochthonous inputs (from outside the system) are important for many ecosystems, today it is known that animals play a central role in nutrient cycling (Hasset et al, 1997, Schindler et al, 2001, Frost et al, 2002,Vanni, 2002, Moe et al, 2005, Vanni et al, 2006). In many ecosystems, the biota can store most of the nutrients available, limiting the productivity and predator-prey dynamics that controls the cycling and distribution of nutrients (DeAngelis, 1992).
Overexploitation of fisheries resources around the world has been driving a reduction in fish stock’s abundance and changes in species composition by reducing diversity. Recent evidence shows that intensive fishing has been removing larger, commercially valuable fish and leaving the smaller fish with less associated commercial value (Pauly et al, 1998). The outcome of this scenario is the loss of a balance between predators and prey, and represents the ultimate consequence of changing trophic webs (Pauly et al, 1998, Myers and Worm, 2003). The perturbation that propagates down the food web is known as trophic cascade, which is related to changes in the primary producers and herbivores biomass, and to modifications of species composition at both trophic levels (Vanni, 2002, IMBER, 2005). It can also have an effect at the level of basic biogeochemical cycles of nutrients, causing changes in the new production values, on the rate of conversion of inorganic to organic compounds and to the extent and severity of nutrient limitation (Vanni, 2002, IMBER, 2005).
Further, fish removed from the system play an important role in liking the aquatic and terrestrial system (Maranger et al, 2008). Fish accumulate basic nutrients as biomass, which are then moved from the ocean to the land, and it is important to notice that exports from one ecosystem generally means imports to another (Vitousek et al, 1997). Considering the increase in nutrient input in the coastal environment by anthropogenic effects, this removal will play an important role on the nutrients budget. In some areas of the globe, it represents the most important anthropogenic mediated N flux on the continental shelf (Maranger et al, 2008).
At the same time, fishing activities present direct impacts on the environment that can lead to changes in the biogeochemistry of certain areas. Bottom trawling is the fishing gear that causes the biggest consequences for the chemical characteristics of the environment, disturbing the sediment, increasing the nutrient flux from the bottom at an initial moment and killing the benthic biota responsible for nutrient conversion (Duplisea et al, 2001).
Given the fundamental role that nutrient cycling has on ecosystem maintenance, the importance of fish physiological and ecological characteristics on the nutrient availability and recycling, and direct impacts of harvesting for the ecosystem, it is imperative to understand the links between fish harvesting and geochemical cycles. It is also essential to consider this information in the creation of fisheries management plans and policies.
The main objective of this paper is to recognize the link between fisheries and nutrient cycling through a review of available literature. Most of the research conducted on this topic is based in freshwater systems, given the facility to study those environments, and they can provide an approximation of what could be observed in marine environments. Primarily, nitrogen and phosphorus cycles are going to be discussed, as most studies focused on those nutrients are likely to be limited to primary producers in lakes. Further, the importance of fisheries as a Nitrogen removal mechanism will be demonstrated in a comparative analysis of the Insular Pacific-Hawaiian Large Marine Ecosystem, which includes the Hawaiian Islands.
Organisms influence nutrient cycling in many ways, so it is important to distinguish between direct and indirect effects (Schindler and Eby, 1997, Vanni, 2002). Direct effects are the ones that are related to nutrient transformations by an organism, such as consumption and excretion of nutrients or their use for metabolic purposes. Indirect effects occur with environmental fluxes and are modified by the interaction of the organism with the environment and/or other organisms.
The effect of a determined fish species on nutrient cycling seems then to be tied both to their physiological characteristics, such as nutrient body content, and their ecological characteristics, such as the preferred prey type (Schindler and Eby, 1997).
The preferable prey of a fish will determine the type of nutrient regeneration that it will induce. Predation on zooplankton regenerates pelagic nutrients (phosphorus and nitrogen), but primary producers cannot utilize these, while predation on benthic and terrestrial prey regenerates nutrients that can be used by primary producers (Schindler et al, 2001). The later effect can be observed as well for detritivorous fish, for which excretion increases the nutrient content, releasing sediment-bound nutrients (Vanni et al, 1997). Those nutrients originally present in the benthic zone will be a new source of N and P to the pelagic area (Schindler and Eby, 1997). Consequently, the removal or introduction of fish species with different foraging characteristics will affect the type and ratio of nutrients available in the system. The differences in nutrient availability can change primary production rates and thereby the whole local trophic web.
The greater the differences in nutrient content of the predator in relation to the prey, the stronger the effect that the consumers are going to exert on nutrient cycling (Dantas and Attayde, 2007). Omnivorous species will have a supply of food varying in nutrient content and in quantities higher than their consuming needs, therefore the imbalance between nutrient demand and supply will change the N:P ratio of their excretion. On the other hand, specialized species, such as carnivores fishes are going to face a small availability of their preferred food source, and their excretion will be at a small and constant N:P rate (Dantas and Attayde, 2007). This is within the scope of the ecological stoichiometry, the study of the balance of chemical elements and energy in ecological interactions and processes (Hasset et al, 1997, Karl et al, 2001, Frost et al, 2002, Moe et al, 2005). The term stoichiometry refers to the elemental composition of the organisms and this composition follows thermodynamics and mass balance laws, even when energy and chemical compounds are transferred between tropic levels (Frost et al, 2002, Moe et al, 2005). After Redfield et al (1963) seminal work, it became clear that the elemental composition of organism is strongly linked to nutrient cycling. Thus, the variation of elemental requirements by different organisms will create an imbalance between what is ingested and what will be utilized, resulting in excretion of all nutrients ingested in excess, consequently affecting the ratio by which organisms recycle nutrients.
The nutrients ratio accumulated in any fish species seems to be almost constant during the life cycle, therefore the excretion rates are going to have an inverse relationship with body nutrient content (Dantas and Attayde, 2007).
The amount of nutrient released by fishes can be one of the most important nutrient sources for many systems as showed in Schaus et al (1997). The authors estimated the release of ammonia nitrogen (NH3-N) and soluble reactive phosphorous (SRP) by gizzard shad in lakes and compared those values to other sources of nutrients, such as nutrient content on the lake inflow water and release of P from anoxic hypolimnetic sediments, and their results are showed in the Table 1. As can be observed, the nutrient input by fish excretion is bigger than the other sources, except when considering inorganic N content in the stream water. It means that nutrient input by this species is important to the system, and the removal of this fish can reduce the primary production that is supported by this nutrient source.
The decomposition of the organisms is another way that the nutrients accumulated in the tissues can again be made available, and this process can influence nutrient cycles. Decomposition of whales on the ocean can occur from 3 to 17 years and a variety of fauna can associate and live exclusively with the carcasses (Smith et al, 1989). Exhaustion of this nutrient source can be fatal for some locations and species. In lakes and rivers, comparable situations can be observed, with the nutrient cycling associated with carcasses decomposition appearing as a determinant factor in the ecosystem functioning because it makes available essential nutrients to oligotrophic environments (Parmenter and Lamarra, 1991). Migratory species are considered to be especially important for seasonal nutrient input of which salmon is a well-known example. These fish carcasses bring essential nutrients for the oligotrophic environments in which they are found (Finney et al, 2000), as in Karluk Lake in Kodiak Island Alaska, where the amount of nutrient brought by the carcasses represent half of the Phosphorous (P) and Nitrogen (N) annually available in the lake water (Finney, 1998).
In the marine environment, the ecological and behavioral characteristics presented by many migrating fish species has relevance for many ecosystems. It is known that many marine species engage in transoceanic migrations, so this mass movement of fish carry bounded in their biomass a mass of nutrients that can be released at different areas from where they were assimilated (Roxane Maranger, personal communication). Migration can represent an important process for the nutrient cycles at small scales as well, providing nutrient for oligotrophic environments such as coral reefs (Meyer and Schultz, 1985) and to export nutrients from rich estuarine systems to the coastal environment (Deegan, 1993).
3. Effects of fishing on nutrient cycling
3.1 Direct impacts
One direct effect of fishing on the nutrient availability in a system, and consequently in the nutrient cycle will be the perturbation of the sediments accompanying the use of bottom trawling fishing gear. It represents a major disturbance of the physical environment and alters many ecological parameters such as diversity, species and size composition, and production of benthic communities. It also alters geochemical parameters such as fluxes and carbon mineralization rates (Duplisea et al, 2001, Lykousis and Collins, 2005).
Processes occurring in the sediment are important to make nutrients available to the water column. It is on the sediments that dead organic matter will deposit, decay, and contribute to the nutrient re-mineralization processes. Then upward transport driven mainly by molecular diffusion and biological irrigation will spread these nutrients to utilization in diverse processes. In an undisturbed situation, approximately one third of the nutrients used by primary producers in the continental shelf will come from the sediment (Pilskaln et al, 1998).
Pilskaln et al (1998) described three major impacts that trawling can have on the sediment and subsequent biogeochemical implications. The first is the burial of fresh organic matter into the subsurface, altering the anaerobic and aerobic community distribution and mixing sediments. The aerobic populations exposed to aerobic conditions would change to anaerobic conditions on the subsurface, while the initial anaerobic sediment will be exposed to sediment-water conditions. The magnitude of the impacts will depend on the characteristics of the sedimentary reduction-oxidation zones, such as depth and thickness of the trawling properties and the depth that it mixes into the sediment. During experimental conditions, it was registered that the bacterial biomass and activity in the water column was enhanced after sediment resuspension, what can impacts the particulate organic matter (POM) diagenesis (Lykousis and Collins, 2005).
The second effect mentioned is the liberation of the nutrients retained in the sediment pore water. As the trawling will disturb the sediment and release all of these nutrients at once, it will cause a punctual input, but with a magnitude that is much bigger than the input under normal conditions. It can change the primary producer community’s regime and have consequences on the organic carbon fluxes. Duplisea et al (2001) estimated the magnitude of this pulse of nutrient release due to bottom trawling for the North Sea and found that this input can be 20 times greater than undisturbed conditions for nitrate, 45 times greater for ammonium and 26 times greater for silicates.
The third is the dramatical effects that bottom trawling can cause in megafaunal, macrobentic and macrofauna assemblages (Pusceddu et al., 2005). The faunal distribution is patchy and the distribution of metazoan and prokaryotic communities follows a complicated scheme that is linked to nutrient regeneration. Bottom trawling changes the spatial distribution of the organisms that will then change the nutrient recycling rates of the sediment. As an example, fluxes of NO3- are directly related to burrow wall thickness (burrow abundance divided by burrow radius), so the number and size of burrows can affect nitrification and denitrification processes (Pilskaln et al, 1998).
One major impact on the nitrogen input to the water column occurs when trawling disturbs the denitrifying bacteria found at deeper anaerobic layers and then mixes on the aerobic surface. The release of metabolic products initially unavailable to the biota results in available regenerated ammonium and nitrate. In the Gulf of Maine it is estimated that the annual release of ammonium caused by sediment disturbance from bottom trawling gear is about 306 x 106 uMN (Christensen, 1989). The concentration of ammonium in the water column during a summer where the bottom was not disturbed by trawling is 1 uM in the upper level and of 0.1 uM in deep waters. Consequently, the release of nutrients caused by bottom trawling disturbances is significant for the annual nitrogen budget of the system and also can provide the required nutrients to increase the nitrite production in the water column. The sediment disturbed is also a great source of silicates for the biota, making available silicate that was buried on the sediment to biological utilization.
3.2 Shifts in fish community composition
McIntyre et al. (2007) used field data in probabilist numerical simulations to evaluate the nutrient recycling changes when a species of the system went extinct. The nutrient recycling of N and P was calculated for a river (69 species) and a lake (36 species) through measurements of population densities and analysis of individual excretion composition.
The effects upon nutrient recycling were related to the capacity of the surviving fish species to moderate the effects of the extinction and on the sequence in which species went extinct. Nutrient recycling rates increased or decreased depending on the trophic level of the species that compensate the extinction. When species of the same trophic level as the extinct species increased, the mean N and P recycled decreased. Conversely, when species with high recycling rates compensated the loss, the N and P recycling rates increased. When a trophic level was totally extinct, larger losses on nutrient recycling rates were observed and the ecosystem productivity will be serious compromised, especially because the primary production would decrease.
Large impacts on nutrient recycling rates were generated by the simulation where the fishing pressure caused the extinction Strong harvesting lead to the biggest decline observed on nutrient recycling and also reduced the aggregate N:P ratio of the recycled nutrients.
Another study removed a detritivorous fish species from a river system, subsequently observing that the flux of particulate organic matter on the bottom of the river increased and POC biomass increasing 450% (Taylor et al, 2006). The residence time of POC increased after the removal and the gross primary production doubled. This contradicts the conclusions of McIntyre et al (2006) and Schaus et al (1997) mentioned before, but the authors justified that in this case, instead of using organic carbon released by the fish, the primary production consumes OC produced upstream on the river where the detritivorous fish was still present or in the terrestrial environment (Taylor et al, 2006). Another alternative is that the primary production in the absence of this fish species will be the large component of the organic matter pool, sustaining a higher biomass of decomposing microbes. The microbial community would then make the organic matter from phytoplankton decaying available again to phytoplankton production.
To the contrary, when a new species is introduced in an environment, the nutrient recycling rates tend to increase, as would be expected (Schindler et al, 2001). The new production of nutrients that are readily available for primary producers use can lead to an increase in algal production and changes on the geochemistry of the sediments. An algal bloom will sequester P from the water column, that will change the equilibrium between the sediment and the water, and more P will then be released from the sediment (Brooks and Edgington, 1994). At the end of the bloom, all this organic matter will be deposited on the lake bottom, and the sediment will be enriched with nutrients, raising the microbial activity. Besides, the phytoplankton will consume silica, and during large algal blooms or in eutrophicated systems silica will not be deposited on the sediments nor transported to the ocean (Humborg et al, 2000).
However, it is not clear how these results could be applied for the oceanic ecosystem. Comparison of time series of nutrient concentration, phytoplankton, zooplankton and fish biomass in marine pelagic ecosystems showed that a higher availability of nitrogen can imply higher primary production, but does not represent an increase in fish biomass concentration (Micheli, 1999). These results are based on mesocosm experiments, and can only be extrapolated to the ecosystem level with caution, however the indication is that conclusions obtained for freshwater and marine systems contrast and must be carefully interpreted. But even in spite of these differences, the freshwater systems results represent an abundant source of information that should not be neglected. Nutrient cycling in both aquatic environments relies on microbial activity to decompose organic nutrients into mineral forms that are available for primary producers that require similar nutrients in both systems. There are no evidences of biogeochemical processes limiting N or P availability to phytoplankton occurring in just one of these environments (Hecky and Kilham, 1988). Primary production presents seasonal variability in both ecosystems due to hydrodynamic conditions, such as turbulence and stratification (Brooke and Edgington, 1994, Hecky and Kilham, 1998, Dore et al, 2002). No major differences in nitrogen fixation by benthic bacteria was found between freshwater and marine ecosystems (Howarth et al, 1988). Also, the principal source of nitrate for denitrification in both aquatic systems was reported to be the nitrification in the sediments and the range of denitrification rates for freshwater and coastal marine ecosystems is similar (Seitzinger, 1988).
3.3 Removal of nutrients
One important and usually neglected effect of fishing is the removal of nutrients in the marine ecosystem, because the fish itself represents a stock of nutrients for the environment, as discussed previously in this work.
The fisheries catch will represent a flux of nutrients from the marine environment to terrestrial environment (Maranger et al, 2008). Maranger et al (2008) compared the rates in which nitrogen has been introduced and removed from the marine ecosystem through anthropogenic process. Considering the input of N to coastal areas via fertilizer run-off and the removal through the fisheries, the authors observed that the fisheries represent a significant removal of the anthropogenic introduced N. The ratio of N removal by fisheries and N input by fertilizer can vary from 0.04 in the Gulf of Mexico to 25.2 for the Canary Current (Figure 1). In a long-term analysis, the ratio of N removed through fisheries to N introduced by fertilizing use has been declining, since even if both series showed the tendency to increase with time, the use of fertilizer and subsequent delivery to coastal ocean increased at higher rates.
Figure 1. N input to coasts as fertilizer run-off versus N removed in commercial fisheries. a, Total amount of N in fertilizer run-off (Tg N yr-1 =1012 g N yr-1 )vdelivered to the global ocean (left axis, blue line) and N returned as fish biomass (left axis, red line) per year over time. The orange line (right axis) is the proportion of fish N removed relative to fertilizer N exported (ratio fish N:fertilizer N) reported as a percentage. b, The ratio of fish N removed to fertilizer N entering 58 different large marine ecosystems (LMEs) for the year 1995 (from Maranger et al, 2008).
Different parts of the globe presented different ratios of output/input, because of regional processes. Rivers of tropical and subtropical zone are the major exporters of N (TN = PN + DIN + DON), P (TP = PP+DIP+DOP) and organic C (TOC), however, the ratio of TN:TP varies widely and there is no longitudnal correlation (Seitzinger and Mayorga, 2008). The rate of nitrogen exported in rivers is highly correlated with the human-derived nitrogen used (Howart et al, 1996). Also, the contribution of groundwater to the nutrient budget of coastal water needs to be considered. The nutrient content of the groundwater and its export to the marine environment depends on the soil type and land use. In soils with high carbonate content, P can be removed from the water (Lapointe et al, 1990). A higher groundwater flux into the marine environments occurs in regions where the coastal sediments are coarse and unconsolidated (Valiela et al, 1990). Intensive agriculture increases nitrate concentrations on the aquifers (Howart et al, 1996) and the use of septic tanks will increase P and N in the groundwater (Lapointe et al, 1990).
It is important to remember the concept of the fish migration. Harvesting of migratory species before completion of a migratory cycle can prevent a region of receiving nutrients that are important for the local dynamics. At the same time, a great share of the fish harvested is not consumed locally. In 2004 the exportation of fish production was about 38% of all captures (FAO, 2006), which results in a transfer of nutrients from one global zone to the other, via a process that is totally disconnected from the normal nutrient cycling and ecosystem functioning. It can bring a greater nutrient input for rivers, lakes and coastal zones of countries that are the biggest importer of the production, such as Japan that alone imports more than 20% of the global fish traded (FAO, 2006).
3.3.1 Anthropogenic input of N and removal through fisheries in the Hawaiian Large Marine Ecosystem
The oceanic area around the Hawaiian Islands comprises one Large Marine Ecosystem (LME), named Insular Pacific-Hawaiian, that is going to be used as the basic unit for a comparative analysis of N input on the system by anthropogenic processes and removal through fisheries. It has an area of 979225 Km2, and approximately 1,285,498 habitants (U.S. Census Bureau, 2006).
Figure 2 shows a comparison between N input from fertilizer use and removal by fisheries on the Insular Pacific-Hawaiian LME. Data of fertilizer use on the islands were obtained from the Hawaii Agricultural Statistics Service (2003). It was assumed that 12% of N content on fertilizer applied on the islands would run-off to the ocean (Maranger et al, 2008). It does not include the nutrient input from groundwater flux, which can be important for the costal waters in the Hawaiian Islands. Garrison et al. (2003) studying a bay on west Oahu (Kahana Bay) estimated that groundwater fluxes into the bay of total dissolved phosphorus and nitrogen were 500 and 200% higher than fluxes via surface runoff. Since incorporation from fertilizer nutrients into the groundwater and from there to the ocean is complex and there is a lack of information available on the islands, it will not be considered in the present comparison. Fisheries data was obtained from Sea Around Us (2008) and the fish Nitrogen content was estimated as 2.6% N per unit wet-weight fish (Ramseyer, 2002).
Figure 2. N input on the Insular Pacific-Hawaiian LME by fertilizer use and N removal by fisheries. The ratio represents the proportion of N removed as fish biomass by N input in fertilizer(fish N : fertilizer N), in percentage. Values of nitrogen are expressed in TonN/Year.
Figure 3 shows the net N input from human waste, fertilizer use and atmospheric deposition, N removal through fisheries and the % ratio between the two. Net atmospheric deposition of nitrogen in the the North Pacific Ocean is estimated as approximately 22 mol N day-1 (Deutsch et al, 2001), that will result in a deposition of 1.1008 x 105 TonN year-1 for the whole LME area. The average introduction of nitrogen by human waste was assumed to be 1.8 KgN year-1 person-1 (Caraco and Cole, 1999). Considering the population of the Hawaiian Islands, it will be equal to 2.3135x 103 TonN year-1. It can be observed that in this scenario, the N removal by the fisheries is insignificant compare to the N net input on the system.
Figure 3. Net N input on the Insular Pacific-Hawaiian LME by fertilizer use, human waste and atmospheric deposition and N removal by fisheries. The ratio represents the proportion of N removed as fish biomass by N input in fertilizer, human waste and atmospheric deposition (fish N : net input N), in percentage. Values of nitrogen are expressed in TonN/Year.
However, local catches on the islands that do not need to be reported can change these numbers. It is estimated that the catch is in fact 200 fold higher then that reported to the FAO (Daniel Pauly, UBC Fisheries, personal communication). The inclusion of non-reported estimates for fish harvest increases N-export by 2 orders of magnitude (Figure 4). It can be observed that the fisheries alone can represent a significant output of introduced nutrients on marine environments.
Figure 4. Net N input on the Insular Pacific-Hawaiian LME by fertilizer use, human waste and atmospheric deposition and removal by fisheries with corrected catches values. The ratio represents the proportion of N removed as fish biomass by N input in fertilizer, human waste and atmospheric deposition (fish N : net input N), in percentage. Values of nitrogen are expressed in TonN/Year.
It is undeniable that commercial fishing around the globe has been causing profound changes to marine ecosystems, altering species composition, biomass values and food web interactions (Pauly et al, 1998, Myers and Worm, 2003). However, the effect of those changes on the geochemical cycles and chemical species availability is still largely unknown and often ignored. Limited research investigated these interactions at an ecosystem level in the oceans. An ongoing research project titled “Integrated Marine Biogeochemistry and Ecosystem Research” (IMBER, 2005) considers understanding the role that fisheries play on food webs and biogeochemical cycles, but it has not presented any published data thus far.It is clear that bottom trawling can directly impact the biogeochemistry of areas where this fishing gear is intensively used. It will impact the nutrient cycles, especially N cycles, since nitrification/denitrification processes are affected by the bottom physical disturbance and a large amount of N products are going to be released in the water column and are going to be readily available to the biota.
Studies conducted in lakes showed that nutrient cycles suffer large variations when species are introduced or removed from the environment. To which extent those results can be applied to marine environments is still unclear, but they suggest that the alteration of the trophic webs and of the bottom up/top down controlling mechanisms would ultimately cause changes on the biogeochemical processes.
Fisheries also represent a direct removal of nutrients associated with the fish biomass. The decline of fisheries globally would represent more nutrients being concentrated in the marine environment, which in the long term can become a major issue, since the increasing of anthropogenic nitrogen deposition is linked to higher ocean acidification (Doney et al, 2007).
For the Insular Pacific-Hawaiian LME, it was showed that the fisheries represent a significant output of introduced nutrients on this marine environment. Future studies should investigate the processes described in this work through data acquisition on the marine environment and modeling studies. It would allow the incorporation of the links between fisheries and nutrient cycling in forecast models, and this information would be available to use for fisheries managers and policy makers.
I would like to thank Roxane Maranger for her comments, data and bibliography provided. Lance Kobashigawa for the statistics of fertilizer use in Hawaii and Glen K. Fukumoto for his comments on the fertilizer statistics. Finally, thanks to Brian Glazer and an anonymous reviewer for helpful comments on this manuscript and Paul Christensen for the invaluable English reviews.
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