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Hornborg, S., Främberg, A. (2019) Carp (Cyprinidae) Fisheries in Swedish Lakes: A Combined Environmental Assessment Approach to Evaluate Data-limited Freshwater Fish Resources as Food Environmental Management, 65(2): 232-242 https://doi.org/10.1007/s00267-019-01241-z

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Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:ri:diva-42504 Environmental Management (2020) 65:232–242 https://doi.org/10.1007/s00267-019-01241-z

Carp (Cyprinidae) Fisheries in Swedish Lakes: A Combined Environmental Assessment Approach to Evaluate Data-limited Freshwater Fish Resources as Food

1 2 Sara Hornborg ● Anton Främberg

Received: 1 July 2019 / Accepted: 4 December 2019 / Published online: 19 December 2019 © The Author(s) 2020

Abstract The role of aquatic resources to food security is both promising and constrained since the global seafood consumption is increasing while marine fisheries approach the limit of what it can produce. In Sweden, the seafood consumption per capita is higher than the European and world average but the current dietary advice is to increase consumption. Freshwater fisheries have in general been paid less attention in food security discussions. Carp fishes (Cyprinidae) in Sweden have lost their historical value and are currently, both understudied and underutilized. Here we use a combined environmental assessment approach to examine the environmental sustainability of current and potential cyprinid fisheries. We found that current 1234567890();,: 1234567890();,: commercial fisheries for Swedish cyprinids in lakes have an average carbon footprint of 0.77 kg CO2e per kg of edible product, substantially smaller than most of the popular marine and terrestrial protein sources consumed in Sweden today. This could be even lower if cyprinid resources were better utilized than currently. The cyprinids however exhibited different vulnerability to fishing pressure and are today associated with data deficiencies. Hence, it is currently uncertain how much food for human consumption they can contribute to. Improved consumer interest and management attention is needed, but to the Swedish diet, cyprinids offer a promising opportunity for future more sustainable and nutritious food systems.

Keywords Environmental assessment ● Life cycle assessment ● Productivity susceptibility analysis ● Freshwater fisheries ● Cyprinidae ● Food security

Introduction nutrition security (Godfray et al. 2010; Tacon and Metian 2013). However, current supply has high demand and is The need to shift towards more sustainable food systems extensively traded, affecting e.g. affordability (FAO 2018). advocate for new and innovative approaches (Gordon et al. Growth of aquaculture has been vital, considering that 2017). Examples include improving resource use efficiency marine capture fisheries has not increased since the 1980s; and finding solutions to the current distance between con- on the other hand, further increase in production may lead sumers and producers from globalized markets. Aquatic to competition of feed resources (Troell et al. 2014). Even resources could play an important role to future food and so, seafood consumption is often recommended to increase due to important nutritional characteristics—but it is unclear how this could be done sustainably (Thurstan and Roberts 2014). Supplementary information The online version of this article (https:// Freshwater fisheries production is one component of doi.org/10.1007/s00267-019-01241-z) contains supplementary material, which is available to authorized users. aquatic resources that has traditionally been paid less attention to in terms of contribution to food security * Sara Hornborg (McIntyre et al. 2016; Deines et al. 2017; Lynch et al. 2017) [email protected] and could potentially add to resource availability. In parti- 1 RISE- Research Institutes of Sweden, PO Box 5401, 402 29 cular in industrialized countries, that often import the Gothenburg, Sweden majority of seafood consumed from countries with under- 2 Department of Biological and Environmental Sciences, University nourishment (Smith et al. 2010), freshwater resources are of Gothenburg, Gothenburg, Sweden not given adequate consideration as a food resource in terms Environmental Management (2020) 65:232–242 233 of management systems needed (Arlinghaus et al. 2002; fisheries (Bonow et al. 2013). They are still an important Dudgeon et al. 2006). There is thus little information resource in many other countries, including neighboring available to quantitatively determine sustainable exploita- countries. Today, they are in Sweden mainly being fished tion levels (Lorenzen et al. 2016), and risk-based assess- for other reasons than for human consumption, such as bait ments such as productivity susceptibility analysis have fish and reduction fisheries in lakes to remove nutrients as a almost exclusively been applied in a marine context (Hor- remedy against eutrophication (Bonow et al. 2013; Hansson dyk and Carruthers 2018). Small-scale fisheries with pas- et al. 1998). This implies that there is very limited data sive gears, such as those often used in freshwaters, are also available to inform on stock status and sensitivity to fishing understudied in terms of energy use per kilo landing, while pressure (Östman et al. 2016). the data available exhibit large variability (Parker and To fully identify the net effect of different options for Tyedmers 2015). Fuel use during fishing is the key driver future sustainable diets, or ‘rewiring the food system’ (sensu behind the carbon footprint of products from capture fish- Gordon et al. 2017), an integration of environmental eries (Ziegler et al. 2016; Avadí and Fréon 2013). There- assessments is needed that is capable of including both fore, including freshwater products in assessments of potential local ecological risks and offstage effects (Pascual healthy and sustainable diets is overall compromised (e.g., et al. 2017). As an example, while carbon footprints (esti- Hallström et al. 2019; Tilman and Clark 2014). mates of greenhouse gas emissions through life cycle Sweden represents an interesting case study related to assessment (LCA)) are commonly used as proxies for sus- addressing the role of freshwater fisheries in future food tainability (e.g. Tilman and Clark 2014), other tools are systems. Swedish consumption of seafood is higher than the needed to address local ecological risks of fishing (Ziegler global and European average (Borthwick et al. 2019), but et al. 2016), such as ecological risk assessments (Hobday below the dietary advice of two to three portions per week et al. 2011). The two tools may be seen as complementary recommended by the National Food Agency (NFA) in to each other in assessing pressures from capture fisheries. Sweden (NFA Sweden 2019). To reach the recommended This has been demonstrated for the Australian fisheries for level (2.5 portions a week), an increase of 3.75 kg per Patagonian toothfish Dissostichus eleginoides, where local person and year is required (assuming a portion size of ecological risks were assessed as low whereas the carbon 125 g). However, around 78% of products consumed in footprint was comparatively high (Hornborg et al. 2018); Sweden today is imported, most from marine fisheries and more case studies may be useful to map potential conflicts aquaculture from around the globe, even if the Swedish between different aspects of sustainability and contribute to government has a food strategy to increase level of self- discussions on sustainable diets. sufficiency (Borthwick et al. 2019; GoV 2016). Swedish The objective of this study is to evaluate Swedish fish- aquaculture production is marginal and has today chal- eries of cyprinids as a food resource compared to other lenges with strict environmental legislation and high pro- more popular food items consumed in Sweden today. This duction costs, with only a few commercial actors. However, is done by assessing the carbon footprint combined with the over 40,000 km2 is covered by freshwater (SCB 2019a) potential risks posed for the different carp species based on while freshwater fisheries represented only 0.7% of Swe- vulnerability to fishing pressure, i.e., a combined approach den’s reported commercial landings in 2018 (SwAM to environmental assessment. The overall aim is to form a 2018, 2019a). What role could increased utilization of basis for discussing the potential of cyprinids in sustainable freshwater fisheries in Sweden play for improved food and food systems. nutrition security? Current freshwater landings in Sweden mainly comprise of a few popular freshwater fishes, such as salmonids Materials and Methods (Salmonidae), pikeperch Sander lucioperca, perch Perca fluviatilis and pike Esox lucius, which are fully utilized or Life Cycle Assessment even in need of recovery according to the yearly account of status of Swedish fisheries resources (SwAM 2019b). The carbon footprint was quantified through a LCA However, there are also populations of virtually unutilized approach, a tool commonly used to quantify the environ- carp species (Cyprinidae). Latest advice recommends an mental pressures and resource use of different products increase in fishing for bream Abramis brama, the only only throughout its lifecycle (Ness et al. 2007). The goal was to carp species included in the yearly resource assessment, but assess the carbon footprint of the current and potential with caution. Several species of carp were consumed in (defined as 100% retainment of discarded cyprinids) Sweden up until the middle of the 20th century but have Swedish freshwater cyprinid fishing to enable comparison over time been more or less abandoned in the process of with (1) other fisheries, based on Parker et al. (2018); (2) industrialization, urbanization and expansion of marine other top seafood items consumed in Sweden (Borthwick 234 Environmental Management (2020) 65:232–242 et al. 2019); and (3) Swedish beef, pork, chicken and brown emissions up to landing of the fish). Fuel use per kg live beans based on RISE Climate Database (2018). The func- weight was used, thus making the carbon footprint calcu- tional unit (FU), i.e., the unit to which all of the inputs and lated corresponding to all freshwater fishes landed using the outputs are related to, was defined as 1 kg of edible carp fish evaluated fishing method. meat to be comparable with RISE (2018). The edible yield Data on the current commercial pond net fishery (the was collected from FAO (FAO 1989) which states the same fishing method contributing to 88% of cyprinid landings of yield for all cyprinids (54% of live-weight, based on that of mainly bream; SwAM 2019a) was collected through semi- common carp Cyprinus carpio). structured interviews. A first suggestion of fishers was The system boundaries, i.e., the processes included in the obtained from the Swedish Lake Fishery Association, study, covered the production and combustion of fuel for adding further fishers through “snow-balling technique” current commercial and recent reduction fisheries in where respondents were asked to suggest others to inter- Swedish lakes, up to the point of landing. Transport of the view. Two of the Swedish big lakes were included, Vänern fish to market is excluded. This may add more to emissions and Mälaren, and one smaller lake, Bolmen. In the two than what is generally seen (low contribution of the trans- larger lakes efforts were made to obtain answers from ports) because the supply chain is today not optimized due fishers distributed throughout the lakes’ areas. Two large to the small-scale nature of the current fisheries. On the lakes were excluded, namely Vättern and Hjälmaren. Vät- other hand, the fishery in at least one of the lakes (Bolmen) tern was originally considered as a potential candidate but has no addition from the supply chain since it is locally was excluded since the nutrient poor lake holds a relatively prepared and consumed. Only emissions from fuel pro- small cyprinid population, with all the commercial catches duction and combustion during fishing were considered, already being used in the lakes’ crayfish fishery (J. Fogel, while production of boats, fishing gear and packaging was County Administrative Board Stockholm, Pers. Comm.). A excluded. This was motivated from that the fuel used during total of 14 commercial fishers provided data for one year of the fishing phase generally dominates the carbon footprint fishing (2018). Furthermore, data from five reduction fish- of seafood from capture fisheries (Ziegler et al. 2016). ing occasions in two lakes was extracted from published Allocation of emissions between species in landings was reports (Sandström 2011; Annadotter et al. 2013). Addi- based on mass; alternative allocation such as economy- tional data on reduction fisheries was obtained from inter- based is difficult since the market for cyprinids to a large views with three reduction fishers from 20 fishing occasions extent is potential rather than existing. Results will also be in eight different lakes (between 2010 and 2018). The lakes less influenced by markets over time. In processing, all included were located in the southern part of Sweden, more emissions are allocated to the edible part of the fish (no specifically the regions Skåne (Finjasjön, Häckebergasjön, utilizations of by-products are known). Cleaning and fil- Oppmannsjön, Ringsjön and Sövdesjön), Småland (Södra leting of the fish were assumed to be done by hand due to Bergundasjön, Trummen and Växjösjön) and Uppland the small scale of the freshwater fisheries, and hence no (Vallentunasjön and Östhammarfjärdarna). The samples are additional resource use and emissions was assigned to seen as representative for the fishing practices since the this stage. percentage of cyprinids in landings in the commercial Emission factors from fuel combustion was collected fisheries were approximately the same in the sample and the from the Swedish fuel and biofuel institute (SPBI 2010). It whole fleet, and data on reduction fisheries covered 40% of is assumed that all motors fueled by petrol use “Engine all the recent reduction fisheries granted funds from SwAM petrol without ethanol” (emission factor 2.36 kg CO2e/L) as Local Water Management Projects (SwAM 2019c). A whereas by diesel “Diesel – Mk1” (emission factor 2.54 kg Kruskal–Wallis one-way analysis of variance (Kruskal and CO2e/L). Emissions from upstream production of the fuel Wallis 1952) was done to determine if there were any sig- came from the Ecoinvent database in the LCA software tool nificant differences between the carbon footprint of fish SimaPro. This background data accounts for emissions from from different lakes or fishing methods. production of fuel, such as oil field exploration, crude oil production, long distance transportation, oil refining and Productivity Susceptibility Analysis regional distribution. Emissions were converted from being stated per kg to liters using densities corresponding to fuels Productivity-susceptibility analysis (PSA) is a screening at SPBI (2010). analysis to assess the potential and relative vulnerability of a To compare the carbon footprints to global fisheries, the species to a fishery based on a set of attributes related to its data collected had to be treated according to the method productivity (based on life history parameters such as life used by Parker et al. (2018). Non-fuel related inputs (such span) and susceptibility to impacts from fishing activities as production of boats and gear) were added as a theoretical (based on parameters such as overlap of fishing effort and estimate based on earlier studies (25% of the total GHG- species distribution), with different approaches used today Environmental Management (2020) 65:232–242 235

Table 1 Life history attributes Productivity attribute Low productivity Medium productivity High productivity and productivity cut-offs used (high risk) (medium risk) (low risk) based on Swedish fi freshwater shes Age at maturity (years) >6 4–5<4 Maximum age (years) >21 12–20 <10 Fecundity (eggs <8000 8000–80,000 >100,000 per year) Maximum size (cm) >60 30–60 <30 Size at maturity (cm) >30 14–30 <14 Trophic level >3.7 3.2–3.7 <3.2 Reproductive strategy Live bearer, sex change Demersal egg layer Broadcast spawner

around the world (Hordyk and Carruthers 2018). The collected from the Encyclopedia of the Swedish Flora and assessment is performed by categorizing a number of Fauna (Kullander et al. 2012). When data was lacking (on attributes of the species and fishery into low/medium/high for example trophic level, maturity size) FishBase (2019) through a score from 1 to 3. The two average values for the was used. When ranges were provided, the value resulting species productivity and susceptibility to the fishery are then in the lowest productivity score (i.e., highest risk) was used combined to form an overall vulnerability V by calculating in order to be precautionary. For details on all life history the Euclidean distance from the origin of the two numbers: parameters and risk levels used see Online resource 1. The pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi total productivity score for each cyprinid was calculated as V ¼ P2 þ S2 ð1Þ the average risk value for all attributes. Susceptibility scores were based on the data collected where productivity P is the average risk score for all from fishers during the interviews (fishing depths, post productivity attributes and susceptibility S is the average of capture mortality), together with information found on the multiplicative risk scores for all susceptibility S FishBase (2019) on species depth range and fishing reg- attributes (ranging between 1.41 and 4.24, where V < 2.64 ulations by SwAM (HVMFS 2014:22) on mesh sizes (Table equals to low risk and V > 3.18 high respectively). The 2). In a few cases, data was extracted from reports published method does not provide insights on the actual status of a after finished reduction fishery efforts (Sandström 2011; species but gives an idea of how potentially vulnerable it is Annadotter et al. 2013). Further information on the fish- to fishing relative to other species based on its biological eries, such as additional methods utilized only in reduction properties, useful to determine which ones should be fisheries, was collected from interviews with fishers. Since prioritized to be investigated further. freshwater fish is restricted by geographic barriers (different The PSA method used here was based on Hobday et al. lakes) there is a high chance of occurrence of local stocks. (2007, 2011). This method utilizes a precautionary The use of a stock structure proxy (as presented by Hobday approach to data-deficiency in the scoring of attributes, et al. (2007) was thus deemed most appropriate for the where an attribute is associated to high-risk if data is lacking Availability score (set to 3, or high risk). There was no or of poor quality. Species included were all native Swedish information found on depth ranges for the cyprinids, nor cyprinid species based on the Encyclopedia of the Swedish habitat overlap of species and fisheries, thus giving the Flora and Fauna (Kullander et al. 2012), i.e., excluding five attribute Encounterability a value of 3 (high risk). Cut-off introduced species. This was motivated from that they do values for selectivity was following the approach for gillnet, not belong to the native fauna and is thus of less con- i.e., based on mesh size relative to size for maturity/total servation concern; in total 16 species were included. Three size (e.g. high risk equals to sizes >2 × mesh size). The main target species of the current commercial pound net mesh size of the pound nets is generally very small, but fisheries were also included in the analysis for comparison: passive entrapment gear is by law required to have escape pike Esox lucius, perch Perca fluviatilis and pikeperch openings with a diameter of 60 mm (HVMFS 2014:22). Sander lucioperca. The same set of productivity attributes This diameter was considered the mesh size of the com- were used as in Hobday et al. (2011; Table 1). Cut-offs for mercial pound nets. Post capture mortality cut-off attribute low-medium-high productivity was based on the distribu- was set to 3 (high risk) in the current fisheries if the species tion of all native freshwater species registered in Swedish represented a considerable part (more than 10%) of the total lakes (37 species found at the Swedish Species Initiative pound net landings (SwAM 2018). Other species were 2019, excluding sub-species), following the recommended given a score of 2 (medium risk) since they are discarded approach. The productivity attributes were primarily alive and have a high chance for survival based on fishing 236 Environmental Management (2020) 65:232–242

Table 2 Susceptibility attributes and cut-offs for low-medium-high-risk based on Hobday et al. (2011) and assumptions made in this study Attribute Options This study High susceptibility Medium Low susceptibility susceptibility

Availability Two alternatives, (1) overlap of species range with Endemic/sub-population North hemisphere Global fishery (in %) or (2) global distribution Encounterability Two alternatives, (1) habitat- or (2) depth overlap High overlap with Medium overlap Low overlap with with fishery (%) fishing gear with fishing gear fishing gear Selectivity Vary by gear type, based on size (at maturity/ Species > 2 times mesh size Species 1–2 times Species < mesh size maximum) mesh size Post-capture Vary by gear and species Retained species, or Released alive Evidence of post-capture mortality majority dead when release and survival released method. A multiplicative approach was used for calculating from the year closest to the fishing occasion was used (two the average susceptibility score following Hobday et al. cases dating back to 1997). (2011), except for the reduction fishery where the overall Current commercial use was also collected from Fish- susceptibility score for the cyprinids to was assumed to be 3 Base (2019) to map commercial interest, as well as status on (high) since the fishing aims at removing as much cyprinid the 2015 Swedish IUCN Red List assessment (Swedish biomass as possible. Species Initiative 2019) as an additional source on potential vulnerability. Evaluation of a Potential Future Carp Fishery

For environmental assessment of a potential increased uti- Results lization of cyprinids within the current fishery operations in terms of carbon footprint, ecological risks and available All cyprinids are categorized as least concern (LC) on the volumes it was assumed that: Swedish IUCN Red List except for two which are red-listed (near threatened, NT): asp Aspius aspius and vimba bream (1) landing the today discarded cyprinids would not Vimba vimba (Table 3). The global commercial use of the require more fishing trips or more fuel per trip; cyprinid species varies considerably, with bream Abramis (2) there are no re-catches of the released cyprinids; and brama and crucian carp Carassius carassius being highly (3) all are of sizes of commercial interest. commercial, while belica Leucaspius delineatus, common dace Leuciscus leuciscus and gudgeon Gobio gobio being The risk score for post capture mortality was adjusted to of no commercial interest today (FishBase 2019). 3 (high risk) for all cyprinid species in the PSA, and the Cyprinid landing ratio relative to other species was found current fuel use was attributed to higher landing volumes to vary considerably between the different lakes, from 0.8% than current (100% retainment of today discarded cyprinids) in Mälaren to 57.5% in Bolmen (Table 4), but also between for the carbon footprint assessment. fishers within the lakes. The annual total landings of all fish To scale up to estimate the potential biomass of cyprinids and total fuel consumption does however not vary as much available to future fisheries from all lakes, cyprinid catches between lakes. This results in a relatively homogenous was collected from the Swedish lake monitoring database average fuel consumption per kg fish landed, between 0.06 (NORS 2019) and converted to g of cyprinids per m2 of net. and 0.18 liter of fuel per kg live weight (Table 4). Based on The largest nets, Bss (‘översiktsnät typ Stora Sjöarna’), current discard rates, cyprinid landings have the potential to were excluded from the estimate, since these were only used increase substantially, which in turn would lead to improved in lake Vänern and are disproportionally ineffective in fuel efficiency per kilo landed. catching cyprinids compared to smaller nets. The abun- The reduction fisheries all target primarily cyprinids dance from the geographically closest monitoring fishery (Table 5). Small perch were occasionally included in the site was assumed to be the same as on the stated fishing landings from pound nets and seines, making up the missing location. Abundance data from 2015 to 2017 was used for few percent. The seine and pound net reduction fisheries the commercial fisheries, whereas for the reduction fish- were all conducted with petrol driven engines, but the eries, data from the year before the reduction fishing took trawlers utilized diesel. The carbon footprint of the current place was used if available. When not available, the data commercial fishery in Swedish lakes up to the point of Environmental Management (2020) 65:232–242 237

Table 3 Native cyprinids in Common name Species Maximum size IUCN status Commercial use Sweden, IUCN Red List status and commercial utilization Asp Aspius aspius 120 cm NT Yes globally Belica Leucaspius delineatus 12 cm LC No Bleak Alburnus alburnus 16 cm LC Minor Bream Abramis brama 80 cm LC Highly Chub Squalius cephalus 45 cm LC Minor Common dace Leuciscus leuciscus 35 cm LC No Crucian carp Carassius carassius 64 cm LC Highly Eurasian minnow Phoxinus phoxinus 12 cm LC Minor Gudeon Gobio gobio 13 cm LC No Ide Leuciscus idus 24 cm LC Yes Roach Rutilus rutilus 50 cm LC Yes Rudd Scardinius erythrophtalmus 35 cm LC Minor Tench Tinca tinca 60 cm LC Yes Vimba bream Vimba vimba 50 cm NT Minor White bream Blicca bjoerkna 45 cm LC Minor Zope Ballerus ballerus 45 cm LC Minor

Table 4 Inventory results from the commercial fishery with standard deviation, separated by lake Lake % Cyprinids in Total landing per Cyprinid landing per Potential cyprinid landing Fuel use per Fuel efficiency (liter/ landings fisher (tonnes) fisher (tonnes) per fisher (tonnes) fisher (m3) live-weight)

Vänern 19.0 18.2 ± 12.6 3.5 ± 6.0 18.8 ± 14.6 2.2 ± 1.2 0.13 ± 0.07 Mälaren 0.8 20.7 ± 6.7 0.2 ± 0.4 8.0 ± 6.2 3.5 ± 1. 4 0.18 ± 0.06 Bolmen 57.5 40 23 32 2.2 0.06 Average 14.1 21.2 ± 10.2 3.0 ± 6.9 13.5 ± 11.9 3.0 ± 1. 4 0.15 ± 0.07

Table 5 Inventory results from Gear % Cyprinids in Total landing Cyprinid landing Fuel use per Fuel efficiency the reduction fisheries with landings per lake (tonnes) per lake (tonnes) lake (m3) (liter/live-weight) standard deviations, divided into groups based on gear type Pound nets 98% 16.3 ± 15.6 15.9 ± 15.4 0.22 ± 0.14 0.02 ± 0.01 Seine 99% 23.7 ± 19.1 23.4 ± 19.2 0.10 ± 0.06 0.005 ± 0.004 Trawl 100% 65.5 ± 22.3 65.5 ± 22.3 7.58 ± 3.01 0.12 ± 0.05 Average 99% 28.8 ± 25.9 28.5 ± 25.9 1.65 ± 3.27 0.04 ± 0.05

1.00 0.80 not statistically significant (Kruskal–Wallis H = 3.51, p = 0.60 = fi 0.40 0.17, df 2). Emissions from reduction sheries vary sig- e/kg edible 2 0.20 nificantly depending on gears (Kruskal–Wallis H = 18.28, CO 0.00 p = 0.0001, df = 2), where trawl is similar to commercial Current Potential Pound net Seine Trawl pound net fisheries (0.71 kg CO e/kg edible), but seine and Commercial pound net Reduction fisheries 2 Fuel combustion Fuel production pound nets have considerably lower emissions (0.03 kg and 0.10 kg CO e/kg edible respectively). fi 2 Fig. 1 Average carbon footprint of commercial and reduction sheries The carbon footprint of the cyprinids is substantially (separated by gear) with contribution of fuel combustion and pro- duction to the total calculated average carbon footprint lower than that of most popular seafoods consumed in Sweden today. Cyprinids caught in the current commercial fisheries contribute to only about a third of the greenhouse landing was on average 0.77 kg CO2e/kg edible, which may gas emissions compared to popular seafood products like decrease by 32% in a future fishery by landing all cyprinids Atlantic cod Gadus morhua, Saithe Pollachius virens, and that are discarded today (Fig. 1). The carbon footprint farmed Atlantic salmon Salmo salar (Fig. 2). Herring Clu- varied between the lakes in the commercial fishery but was pea harengus products are the only ones with a smaller 238 Environmental Management (2020) 65:232–242

30 10.00 25 8.00 20 e/kg

2 6.00 15 e/kg edible 2 10 4.00 5 kg CO 2.00 kg CO 0 0.00 Cod Pork Beef Saithe Shrimp Herring Chicken Potential Commercial Brown beans Farmed salmon Agriculture Seafood Cyprinid Fig. 3 Average carbon footprint for one kg of live-weight fish, fishing including theoretical estimations for upstream production of boats, Fig. 2 Average carbon footprints for the cyprinids based on this study gear etc., for the Swedish freshwater fisheries examined in this study in relation to other more popular protein sources consumed in Sweden (labeled as Freshwater fish), relative to marine seafood categories today (based on data from RISE Climate Database 2018) presented by Parker et al. (2018) carbon footprint compared to the cyprinids from the current utilizing more of the cyprinids that are discarded today. The commercial fishery, whereas brown beans has a similar cyprinids caught in reduction fisheries with seine have an carbon footprint to current commercial cyprinid fisheries. even lower carbon footprint, lower than any other fishery In comparison to other fisheries for which there is fuel type studied Parker et al. (2018). However, since this fishery data, Swedish freshwater pound net and reduction fisheries is aiming at eradicating fish, the catch efficiency and asso- are amongst the most fuel-efficient fisheries (Fig. 3), with ciated carbon footprint may not be seen as a long-term only fisheries of small pelagic fish (<30 cm) being more sustainable food production but rather a underutilized efficient. resource; the biomass caught should be further investigated The PSA indicated different risk levels of the species, but in terms of usefulness as feed or food depending on quality none had a higher vulnerability score than current target and supply chains enabled. species (Table 6). Cyprinids had an average productivity The carbon footprint does not however, convey infor- score of 1.93 (SD 0.41) whereas the targeted freshwater mation on potential local ecological risks with the fisheries. species had an average productivity score of 2.81 (SD 0.08), Jointly considering the carbon footprint results with those of i.e. higher risks than any of the individual cyprinid species. the productivity susceptibility analysis (PSA) is important The cyprinids had an average vulnerability score of 2.95 (SD since the PSA indicated that the different cyprinid species 0.48) in the current fisheries, increasing to 3.40 (SD 0.52) in may have different vulnerability to fishing pressure. As a a potential future fishery landing all cyprinids as a result of result, even if the carbon footprint of current fisheries the increased susceptibility score (post-capture mortality). (which primarily target bream) would decrease in a fishery These estimates are however associated with a lot of where more cyprinids are utilized, potential risks increase, uncertainties. Even if most productivity attributes were advocating that expansion of fishing should be accompanied known (except for size at maturity for two cyprinid species), by suitable monitoring. PSA is designed to have a precau- several susceptibility attributes were given a high-risk based tionary approach and is only an initial screening of relative on data deficiency. Out of the 16 considered cyprinid spe- risks for species to support prioritization of further effort by cies, four species are considered having low vulnerability, management and research (Hobday et al. 2011). The eight medium and four high respectively to the current assessment was associated with uncertainties and could freshwater pound net fishery. In a future fishery with 100% potentially be improved by further method adaptation to retainment of cyprinids, the vulnerability scores increase for freshwater conditions since life history cues for extinction all species in the family. risk may not be correlated for marine and freshwater fishes (Reynolds et al. 2005; Olden et al. 2007). There is to our knowledge only one example of when PSA has been used to Discussion and Conclusion assess the vulnerability in a freshwater context (between populations of Arctic char Salvelinus alpinus in Canada; The low carbon footprint of current commercial fisheries Roux et al. 2011). Even so, none of the species was found to catching cyprinids in Swedish lakes clearly indicates that it have a potentially higher vulnerability than current target is a promising commodity in this sense compared to most of species in Swedish lake fisheries. the commonly consumed protein sources in Sweden today— The combined carbon footprint and ecological risk-based even compared to most other global fisheries. An even lower approach utilized here can illustrate potential trade-offs in carbon footprint per kilo may be achieved simply by sustainability when evaluating new seafood resources from Environmental Management (2020) 65:232–242 239

Table 6 PSA results for the sixteen Swedish cyprinids and three target species in the current commercial fishery and a potential land-all scenario Group Species Productivity Susceptibility, Vulnerability, Risk Susceptibility, Vulnerability, Risk current current category, potential potential category, current potential

Carps Asp 2.43 2.33 3.36 High 3.00 3.86 High White bream 1.86 2.33 2.98 Med 3.00 3.53 High Eurasian minnow 1.43 1.43 2.02 Low 1.65 2.18 Low Zope 2.00 2.33 3.07 Med 3.00 3.61 High Chub 2.14 2.33 3.16 Med 3.00 3.69 High Belica 1.57 2.33 2.81 Med 3.00 3.39 High Ide 2.71 2.33 3.57 High 3.00 4.05 High Bleak 1.29 1.88 2.27 Low 2.33 2.66 Med Roach 2.00 2.33 3.07 Med 3.00 3.61 High Gudeon 1.29 1.88 2.27 Low 2.33 2.66 Med Rudd 1.71 1.88 2.54 Low 2.33 2.89 Med Vimba bream 2.14 2.33 3.16 Med 3.00 3.69 High Bream 2.29 3.00 3.77 High 3.00 3.77 High Crucian carp 2.29 2.33 3.26 High 3.00 3.77 High Common dace 1.71 2.33 2.89 Med 3.00 3.46 High Tench 2.00 2.33 3.07 Med 3.00 3.61 High Target Perch 2.71 3.00 4.05 High 3.00 4.05 High Pike 2.86 3.00 4.14 High 3.00 4.14 High Pikeperch 2.86 3.00 4.14 High 3.00 4.14 High capture fisheries (e.g., freshwater resources, bycatches), and proper measures are taken to minimize potential risks for identify different improvement potentials and associated the species with increased exploitation. From a nutritional constraints. Combining elements of the two tools, which both perspective, seafood from marine capture fisheries provides are used to support decision making in environmental man- important contributions of micronutrients as e.g. shown agement, has gained increase interest in recent years (Harder recently by Hicks et al. (2019). Freshwater fishes were et al. 2015). In a fisheries context, this is the second study excluded in the analysis due to data deficiencies, but there is utilizing the combined approach, the other being a study on a no evidence for them having in general lower nutritional vastly different fishery in the form of the Australian fisheries value. They may rather have benefits compared to marine for Patagonian toothfish Dissostichus eleginoides (Hornborg species, such as a higher ability to produce longer-chain et al. 2018). The toothfish study showed a development of the omega 3 fatty acids out of vegetable oils when farmed fishery from high to low ecological risks through management (Khalili Tilami, Sampels 2018). Comparing some of the actions taken, but the opposite for carbon footprint develop- most important nutrients between the freshwater bream ment. The latter is not considered by management authorities (based on the Swedish National Food agency (NFA)) and but of interest to industry and other societal actors. These popular marine fish species (based on Hornborg et al. 2019) results are both opposite and similar to this study. Similar in show that the cyprinid has higher concentration of vitamin the sense of being cases of exploitation of new resources, with B12, selenium, and niacin than both Atlantic cod Gadus potential ecological risks higher at start (especially the morhua and farmed Atlantic salmon Salmo salar. The reduction fisheries) but carbon footprint lower. Opposite, concentration of polyunsaturated fatty acids in bream is since the assessment indicate low carbon footprint of Swedish lower than in Atlantic salmon, but on the other hand, sub- cyprinids but higher potential ecological risks due to data stantially higher than in Atlantic cod. Therefore, increased deficiency, the latter requiring management effort. utilization of cyprinids in the Swedish seafood diet may improve nutritional security. Cyprinids as a New Resource in the Swedish Food In a recent report on nutritional and climate aspects of System Swedish seafood consumption (Hornborg et al. 2019), cyprinids were not included as they were deemed irrelevant Improved utilization of current cyprinid resources offers an due to the negligible consumption. In 2017, 52 tonnes of opportunity to improve food and nutrition security, given carp fishes were available for consumption in Swedish retail 240 Environmental Management (2020) 65:232–242

(Borthwick et al. 2019), or 10 grams per person and year i.e., not an assessment on absolute risk. The arguable most (based on the Swedish population in 2019; SCB 2019b). A important question at this point is however how to re-gain future fishery when all cyprinids are retained in the com- consumer interest in Sweden. This has been lost during the mercial fishery and extrapolated to all active fishers in the past decades with globalized markets (Bonow et al. 2013). lakes included in the study could tentatively provide almost Only three of the sixteen cyprinid species assessed here 228 tonnes edible product. This would still only represent have no commercial interest in a global perspective, but all less than 1% of the increase in fish consumption recom- have today low consumer interest in Sweden. Some species mended by the Swedish NFA. If the average current discard that should be fully avoided include red-listed species (asp level of cyprinids (22%) was extrapolated to all freshwater and zope), and belica, the latter on which fishery is also pound net fishers, including other Swedish lakes, the total forbidden in Sweden (FIFS 2004:37). Examination of landing could be 350 tonnes edible product. This may cause potential occurrence of hazardous substances (such as heavy competition between bait and food, especially in lake Vät- metals or toxins) in cyprinids caught in different lakes are tern, but available volumes could also increase further by also needed. This is especially true for the cyprinids caught including catches from coastal fisheries in the Baltic Sea in reduction fisheries, since lakes with a high inflow of (were abundance of, e.g., roach is increasing; Ådjers et al. nutrients also often can potentially have a high inflow of 2006), which were not considered here. Further investiga- other substances as well. tions on potential biomass available and associated risks Lastly, seafood is today a highly traded, global com- with exploitation are however required since species com- modity (FAO 2018), with pitfalls and promises. The position varies between lakes (Lehtonen et al. 2008), which knowledgebase concerning freshwater resources and their should also include coastal fisheries. vulnerability to effects from climate change differ between The potential maximum volume available to human countries (Deines et al. 2017; Lynch et al. 2017), calling for consumption from the reduction fisheries is more difficult to increased attention by managers. This may improve by estimate since there is no information on how many lakes increased consumer interest. A shift back towards that would benefit from reduction fisheries. It would also improved utilization of local freshwater resources in a require more research related to product quality and suitable country such as Sweden would be an opportunity for supply chains to ensure high-quality products. If not suited improving the current food system (sensu Gordon et al. for human consumption, they should be suitable for other 2017). This is perhaps especially needed for fish and purposes like animal feed, resources much sought after shellfish since consumers are today distant from the local today (Troell et al. 2014). The estimate for potential ecosystem where it is produced and thus fail to see eco- cyprinid volume available to fishing have in general no system effects from demand (Crona et al. 2016). Building information on size- and species-composition, and small resilience in food systems in light of climate change is also individuals may not be of commercial interest. The smallest urgent, since food production shocks are increasing (Cot- cyprinids are on the other hand not caught in today’s trell et al. 2019). Nordic countries have in a European commercial pound net fisheries, due to the 60 mm escape perspective a more vulnerable seafood production sector openings, but are likely caught in reduction fisheries. With today than in the past since they are much reliant on these aspects providing uncertainties to the estimates, and temperature-sensitive species—whereas species such as by (i) assuming that all Swedish lakes with poor or unsa- common carp is more tolerant to higher temperatures tisfying ecological status would benefit from reduction compared to e.g. salmonids (Blanchet et al. 2019), the top fishing of cyprinids, and (ii) the catch per hectare in the consumed seafood product in Sweden today (Borthwick reduction fisheries included in this study can be extra- et al. 2019). Freshwater cyprinids offer an opportunity to polated to all lakes of respective ecological status, a total Swedish consumers, at this point calling for improved catch of 3050 tonnes (edible yield) could be possible. This management focus and supply chains. would represent around 8% of the increase in fish con- sumption recommended by the Swedish NFA. This is Acknowledgements The authors want to thank the fishers who pro- however not a stable yearly catch, as reduction fisheries are vided the data and Jonatan Fogel who assisted in interviewing fishers meant to reduce the cyprinid densities considerably, but in lake Mälaren. SH want to acknowledge funding from the Swedish some improved utilization than current (at best used for Research Council Formas in the form of two grants, SEAWIN (2016- 00227) and mobility grant (2016-00455). Open access funding pro- biogas today) should be possible; higher value is also of vided by RISE Research Institutes of Sweden. interest to fishers. If fishing effort on cyprinids were to increase, monitoring Compliance with Ethical Standards of stock status development is needed where the contribu- tion of this study has only been to identify the potential and Conflict of Interest The authors declare that they have no conflict of relative risks between different species to fishing pressure, interest. Environmental Management (2020) 65:232–242 241

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