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New target fisheries lead to spatially variable food web effects in an ecosystem model of the California Current
Ecological Modelling 289 (2014) 96–105
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New target fisheries lead to spatially variable food web effects in an ecosystem model of the California Current K.N. Marshall ∗ , I.C. Kaplan, P.S. Levin Conservation Biology Division, Northwest Fishery Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Blvd E, Seattle, WA 98112, United States
a r t i c l e
i n f o
Article history: Received 18 March 2014 Received in revised form 2 July 2014 Accepted 3 July 2014 Keywords: Fishing California Current Ecosystem model Spatial Regional effects Indirect effects
a b s t r a c t Growing human populations put increasing demands on marine ecosystems. Studies have demonstrated the importance of large biomass forage groups in model food webs, but small biomass contributors are often overlooked. Here, we predict the ecosystem effects of three potential future fisheries targeting functional groups that make up only a small proportion of total ecosystem biomass using the California Current Atlantis Model: deep demersal fish such as grenadier (Albatrossia pectoralis and Coryphaenoides acrolepis), nearshore fish such as white croaker (Genyonemus lineatus), and shortbelly rockfish (Sebastes jordani). Using a spatially explicit ecosystem model, we explored individual fishing scenarios for these groups that resulted in abundance levels of 75, 40, 25, and 0 percent of the status quo fishing scenario and a combined fishing scenario simultaneously targeting all three groups. We evaluated the effects on coast-wide biomass and describe variation in affected groups by region. Results indicate that developing fisheries on the proposed targets would have small coast-wide effects on other species. However, effects varied significantly within the ecosystem, with higher impacts concentrated in the central California region of the model. Effects of fishing all three groups simultaneously were additive in some cases coastwide, but were not additive at the regional scale. This work provides a framework for evaluating effects of new fisheries and suggests that regional effects should be evaluated within a larger management context. © 2014 Published by Elsevier B.V.
1. Introduction Anthropogenic stressors on ecosystems have never been greater. Demands for food and freshwater have led to increased fishing (Anticamara et al., 2011), changes in land use patterns (Allan, 2004), and greater regulation of flows in rivers (Caissie, 2006). As pressure to extract resources builds, managers are increasingly confronting trade-offs between the direct value of the extracted resource and the indirect value of the resource left in the ecosystem (Rodriguez et al., 2006; Lester et al., 2010). Understanding these trade-offs requires approaches that can predict the indirect effects of targeted resource extraction on the rest of the ecosystem. In marine ecosystems, demands for fish and fishmeal have led to fishing activities targeting more species than in previous decades (Alder et al., 2008; Branch et al., 2010; Anderson et al., 2011). Often, new target species have low trophic levels, are important
∗ Corresponding author. Tel.: +1 206 861 7601. E-mail address: [email protected] (K.N. Marshall). http://dx.doi.org/10.1016/j.ecolmodel.2014.07.003 0304-3800/© 2014 Published by Elsevier B.V.
prey species for higher trophic level species that are of commercial importance and/or conservation concern. Therefore, a trade-off exists between the value of harvesting these forage species and the value of leaving them as prey for other species in the ecosystem. On the US West Coast, fishing limits have been put into place to protect high biomass, low trophic level species such as krill and anchovy (Pacific Fishery Management Council, 1978, 2008). These rules seek to protect from ecosystem overfishing and maintain the prey base for species that are the targets of existing fisheries. Recently, the effect of adding new fisheries for low trophic level species that constitute large proportions of the biomass of marine ecosystems has been the target of much research (Cury et al., 2011; Smith et al., 2011; Kaplan et al., 2013a,b). These efforts often focus on species or groups with high biomass, while low biomass species or groups are more easily overlooked. Fishing on low biomass groups may indeed have few impacts on food webs if those species are functionally redundant to high-biomass prey groups (Walker, 1992). However, removals of low biomass groups may have disproportionately large impacts, depending on their role in the ecosystem and spatial distribution and overlap of predators and prey. For example, central place foragers, like many seabirds,
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depend on locally abundant seasonal prey resources (Ainley et al., 2009; Pichegru et al., 2010; Cury et al., 2011). Fluctuations in these resources over small spatial and temporal scales could have severe impacts on populations that rely on them, even if a prey contributes low proportions to the overall seabird diet over the course of a year when compared to other potential prey species (Hipfner, 2009). In this study, we investigated the effects of targeted fisheries on relatively low biomass functional groups in a large marine ecosystem. Similar to previous modeling studies, we report biomass responses of species in the food web. However this work is novel in that we also explore regional variation in biomass impacts, as well as ecosystem-wide effects. We investigated target species that were broadly and narrowly distributed across the ecosystem to explore the effects of spatial variation in the food web on the impacts of fishery development. The California Current Large Marine Ecosystem (CCLME) and its associated fisheries provide an excellent example system to investigate how future fishery development could affect existing fishery yields and food web biomass distribution. The largest fleet in the ecosystem, the US west coast groundfish fishery, uses midwater and bottom gear to target 90 species of flatfish, rockfish, and roundfish. Four of these stocks are currently overfished and subject to rebuilding plans. Coastal pelagic fisheries target sardine, mackerel, anchovy and squid. To protect the pelagic prey base, krill fishing is completely banned, and sardine catch limits are set to maintain a minimum of 150,000 mt (Pacific Fishery Management Council, 2006). Here, we explore the potential effects of fishery development targeting new species with lower biomass than species previously investigated by others (Smith et al., 2011; Kaplan et al., 2013a,b). We created ecological forecasts under new fishing scenarios using an Atlantis ecosystem model for the California Current (Horne et al., 2010; Kaplan et al., 2012). Using these forecasts we explored the impacts of new fishery development on the coast-wide and regional distribution of other functional groups in the model. We describe how variation in the distributions of target and non-target species affects impacts of fisheries in a spatially heterogeneous ecosystem. 2. Methods 2.1. Model framework Atlantis is a three dimensional, spatially explicit ecosystem model, comprised of three sub-models (Fig. 1, Fulton et al., 2004). The oceanographic sub-model simulates physical transport using output from a Regional Ocean Modeling System to track temperature, salinity, and circulation. The ecological sub-model captures
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nitrogen and silicon dynamics through trophic interactions among cells, representing functional groups from bacteria and plankton to fish and marine mammals. The human impacts sub-model overlays both the ecological and oceanographic sub-models, and includes fisheries, nutrient inputs, and management control rules. This framework allows for hypothesis testing of how perturbations in the food web can propagate all the way to the management arena. The Atlantis modeling framework has been applied to ecosystems around the world; Fulton et al. (2011) summarized assumptions and options within the Atlantis code base, and detailed lessons learned from 13 recent modeling efforts around the globe. An Atlantis model was developed for the CCLME (California Current Atlantis Model – CCAM) to address federal and state level management needs (Horne et al., 2010; Kaplan et al., 2012). The modeled area extends from Cape Flattery in the north to Point Conception in the south and from shoreline to the 2400 m isobaths (Fig. 2). There are 12 latitudinal regions, broken up longitudinally by 3–7 depth zones. Each of these two dimensional areas is further divided into up to seven depth bins, capturing the sediment layer to the surface layer through the water column. The central California region of the model has higher 2-d spatial resolution in depth zones than the northern and southern regions. CCAM oceanography is based on projections of physical oceanography from a Regional Ocean Modeling System, for the period from 1958 to 2004 (Hermann et al., 2009). The ecological sub-model for CCAM compartmentalizes biomass among 62 functional groups, from phytoplankton to marine mammals. Twenty-seven groups are dedicated to capturing the diversity of fish species in the ecosystem. These groups best represent commercially harvested fish stocks, and groundfish in particular. Species are grouped based on similar life history characteristics and diets. Vertebrate functional groups are represented using 10 ageclasses, while invertebrate groups are simple biomass pools. Key features of the ecological model include type 2 functional responses for all consumers, Beverton–Holt recruitment for fish species, and 3 options for vertebrate movement (migration into and out of the model, seasonal movement within model bounds, and diel vertical migrations). This model has been calibrated to match historical patterns of abundance observed in the field or estimated from stock assessments, and to recreate levels of species productivity that are consistent with literature and stock assessment estimates. The model has been used in multiple applications in the California Current, described in Table 1. Additional details of model parameterization and calibration can be found in technical documentation and these applications (e.g. Horne et al., 2010; Kaplan et al., 2012). We used a “status quo” fishing scenario against which to compare all new fishing activities in the model. The status quo represented current fishing in the CCLME from about 2005 to 2008, and was the same as in Kaplan et al. (2012). Spatial closures represented current area-based management, and fishing mortalities were specified by targeted group and fleet and calibrated to reproduce catches from stock assessments, where applicable (Horne et al., 2010).
Table 1 Applications of the Atlantis modeling framework to the California Current Large Marine Ecosystem.
Fig. 1. A conceptual diagram of the Atlantis modeling framework.
Application
Citations
Food web impacts of forage fish fisheries Evaluating fishery management strategies (spatial management, harvest rates, quota systems) Evaluating risks of climate change, ocean acidification, and cumulative impacts of fishing
Kaplan et al. (2013a), Smith et al. (2011) Kaplan et al. (2012),Kaplan et al. (2014), Kaplan and Leonard (2012) Kaplan et al. (2010), Kaplan et al. (2013b)
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Fig. 2. Status quo distribution of new potential target groups (deep demersal fish, nearshore miscellaneous demersal fish, and shortbelly rockfish). Top panels illustrate distribution in the full model domain (A, B, C). Latitudinal regions are labeled to correspond roughly with historic International North Pacific Fisheries Commission management areas. Bottom panels show target group distribution within Central California region (D, E, F). Deep demersal fish densities were highest in slope cells (A, D), nearshore miscellaneous fish were limited to coastal areas (B, E), and shortbelly rockfish were concentrated in Central California (C, F). Legend below each panel indicates densities in kg/m2 .
2.2. Approach We explored the impacts of new fishing activities targeting three functional groups for which harvest is currently very limited. For each new target group, we created a new fleet in the model and determined the appropriate area closures based on the likely gear type required to target that group. We ran fishing scenarios for each fishery addition alone and all three fisheries together, following methods by Smith et al. (2011) and Kaplan et al. (2013a,b). For each fishery, we incrementally increased the annual fishing mortality from zero until the target group was completely depleted. Each model run was 50 years, allowing functional groups to reach quasi-equilibrium; the model does not assume true equilibrium dynamics and is driven by oceanographic forcing as well as species interactions. We then used these fishing mortalities and resulting catches to determine the maximum sustainable yield (MSY) for each group, as well as the fishing mortality required to obtain 4 levels of abundance relative to the status quo fishing scenario: 0 percent, 25 percent, 40 percent, and 75 percent of status quo biomass. For the combined fishery scenario, we used fishing mortalities determined from each single fishery scenario and fished all three target groups simultaneously.
We describe the impacts of the new fisheries on quasiequilibrium yields and biomasses of the other functional groups in the model. We averaged the last five years of quarterly model output to represent an equilibrium catch or biomass for each functional group, with two exceptions. For groups that migrate outside the model boundaries during each year (Pacific hake, small planktivorous fish, albacore, migratory seabirds, salmon, piscivorous seabirds, pinnipeds, baleen whales, toothed whales, and small cetaceans), we averaged over the peak biomass in each of the last 5 years. The second exception was for groups with high growth rates and quick turnover that lead to population trajectories with high variance through time. For these groups (all plankton, zooplankton, and bacteria) we averaged over the last 20 years of model output. We excluded from our analysis groups that were poorly modeled in the status-quo fishing scenario, defined as biomass dropping below 10 percent of initial biomass in a 50 year run (bivalves, large crabs, benthic grazers, macroalgae, benthic infauna, salmon, small sharks, and jumbo squid). We describe impacts at two spatial scales. Coast-wide impacts were summarized qualitatively, characterizing all changes in the ecosystem as positive, negative, or neutral, with a conservative five percent change threshold. This low threshold eliminates some
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Table 2 Summary of fishing scenarios and target groups. Biomass and yield indicated are for status quo (SQ) model run. M indicates annual natural mortality rate. Maximum sustained yield (MSY) was determined using all fishing scenarios for each target group, and FMSY indicates the fishing mortality rate at MSY. Annual fishing mortality required to obtain 75, 40, 25, and 0 percent of status quo abundance is indicated by F75, F40, F25, and F0, respectively. Target group
SQ biomass (mt)
SQ yield (mt)
M
MSY (mt)
FMSY
F75
F40
F25
F0
Deep demersal fish Misc. nearshore demersal fish Shortbelly rockfish (Sebastes jordani)
183,562 20,920 16,434
2117 206 0.1
0.1 0.62 0.35
2055 9905 6687
0.03 0.12 0.2
0.01 0.04 0.05
0.03 0.1 0.1
0.04 00.12 0.2
0.1 0.24 1
level of noisiness and rounding errors associated with aggregating output, but likely captures all possible coast-wide impacts of fishing the new target groups. We used this five percent threshold because each simulated fishery targeted a small portion of the entire biomass captured in the model. Therefore, we did not expect to see large magnitude changes at the coast-wide scale as a result of our new fisheries. To characterize variability in the effects of new fishing activities along the coast, we represented each latitudinal zone in the model as a separate region. Regions roughly correspond with those historically identified by the International Pacific Fisheries Commission (INPFC) and the Pacific Fishery Management Council (http://www.pcouncil.org/wp-content/uploads/georock.pdf). Within each region, we summarized changes to functional group biomass over 2-dimensional model cells (summed over depth bins). Here, we used a threshold of 20 percent change in catch or biomass, as in Kaplan et al. (2013a,b). Within a latitudinal zone, a group was determined “impacted” if it met the 20 percent threshold in at least one cell within that latitudinal section.
2.3. New target groups In the following sections, we briefly describe the three functional groups for which we created new fisheries in the model. We describe the distribution of each group in the model, describe any current fishing activities, and outline the gear that would likely be used to target the group. We also identify the potential for a harvest market to develop.
2.3.1. Deep demersal fish The deep demersal fish group in CCAM is distributed along the continental slope (500–1200 m, Fig. 2A), and consists mostly of giant grenadier (Albatrossia pectoralis) and Pacific grenadier (Coryphaenoides acrolepis). Other species in this functional group include Pacific lamprey, eelpouts, cusk eels, and poachers (Horne et al., 2010). The west coast groundfish fleet has incidental catches of both grenadier species. Bellman et al. (2008) estimated one to two percent of the annual catch at depths greater than 250 m consists of giant and Pacific grenadier, totaling 600 mt per year. These species are rarely landed because of limited market demand (Matsui et al., 1990). A pot fishery for hagfish is also included in CCAM with harvest of 1250 mt per year (Table 2). Grenadier (family Macrouridae) catches around the world have risen since the mid 1990s. Targeted fisheries currently harvest about 45,000 mt of grenadier from the world’s oceans each year (FAO Fisheries and Aquaculture Department, 2011). In the North Pacific, Japanese harvested grenadier during the 1980s. They were processed into surimi, before the walleye Pollock fishery became a more marketable source (Matsui et al., 1990). Due to historical use and increasing demand for fish and fish products, we thought it would be useful to explore the potential impacts of landing this species complex on the US west coast. Natural mortality for the deep demersal fish group is low (0.1, Table 2), which suggests a priori that MSY will also be relatively low (Gulland, 1971). We created a target fishery on this group that
represents a fishery for grenadier using the same gear and area restrictions as the existing bottom trawl fleet (Kaplan et al., 2012). 2.3.2. Miscellaneous nearshore fish The nearshore miscellaneous fish group is a catchall group dominated by white croaker (Genyonemus lineatus), but also includes shallow sculpins and midshipman. This group is distributed across the nearshore model domain, with higher densities in central California than other regions (Fig. 2B). Life history parameters for this group are based on white croaker (Horne et al., 2010). We created a fishery on this group primarily to represent a fishery targeting white croaker. Croaker is a popular recreational target in California, but only small amounts are currently landed in commercial fisheries annually (3 mt in 2011) using round haul net, gill net, and hook and line gear (Pacific Fisheries Information Network (PacFIN), 2011). Atlantic croaker (Micropogonia undulatus) is a closely related species on the east coast of the US, with similar size, life history, and habitat and food preferences (White and Chittenden, 1977; Morse, 1980). Atlantic croaker is the target of a valuable 10,000 mt fishery (FAO Fisheries and Aquaculture Department, 2011). While the distribution of the miscellaneous nearshore fish group spans the latitudinal extent of the model domain, in reality, white croaker likely composes greater proportions of the group’s biomass from San Francisco bay south to Point Conception (Love et al., 1984). An existing modeled recreational fishery accounts for 247 mt of biomass removed from this group each year. The natural mortality rate for the group is 0.62, suggesting it would tolerate a moderate harvest rate (Table 1). We created a target fishery for croaker using the same area closures as the existing nearshore non-fixed gear sector (Kaplan et al., 2012). 2.3.3. Shortbelly rockfish Shortbelly rockfish is the most abundant of the rockfish species, and comprise their own functional group in CCAM. The most current stock assessment estimated the shortbelly stock to be 64,000 mt in 2005 (Field et al., 2007). While we initialized shortbelly biomass at that level, the quasi-equilibrium biomass in our status-quo scenario is roughly 25 percent of that value (Table 1). Considerable biomass uncertainty results from a lack of fishery dependent data and poor catchability of shortbelly in the fisheries independent trawl survey (Field et al., 2007). Shortbelly rockfish density is highest in central California (Fig. 2C). A few fleets unintentionally catch shortbelly, but these removals are limited to less than 1 mt per year (Bellman et al., 2008). A relatively high natural mortality rate in CCAM (0.35) suggests that this group should be able to sustain a moderate level of fishing mortality (Table 1). We modeled the shortbelly fishery as a mid-water trawl fishery, subjected to the same area closures as the existing groundfish trawl fleet (Kaplan et al., 2012). Fishery interest in shortbelly rockfish has historically been quite low, at least in part because shortbelly are small (maximum size less than 30 cm) (Lenarz, 1980, Field et al., 2007). Lenarz (Lenarz, 1980) identified a potential pet food or surimi market for shortbelly, however he also pointed out these were not economically viable as of 1980. Currently, an annual catch target of 50 mt is in
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place for shortbelly. The groundfish catch regulations indicate this limit is higher than recent catches of shortbelly, but the target is set conservatively because shortbelly is an important forage species for seabirds and marine mammals in the California Current ecosystem (Thayer and Sydeman, 2007; Sweeney and Harvey, 2011).
3. Results We found both general and fishery- and region-specific effects of developing fisheries for three low biomass, low trophic level groups. In this section, we first briefly describe the impacts of the three new fisheries on the species they targeted. Next, we describe patterns of ecosystem response at the coast-wide scale across all fisheries. Last, we describe regional variation in impacts across and within the fisheries.
3.1. Impacts on target species Simulations suggested that deep demersal fish could sustain a maximum harvest of 2055 mt per year, which required annual fishing mortality of 0.03. This level of fishing reduced the biomass of this group to 66,747 mt (about 40 percent of the status quo biomass, Appendix 1). The current estimate for grenadier bycatch is 600 mt (Bellman et al., 2008), resulting in capacity for a fishery using the same gear as the current trawl fishery of about 2600 mt sustained yield. A fishery on the nearshore demersal fish group attained a MSY of 2000 mt with an annual fishing mortality of 0.1 (Appendix 1, Table 1). This level of fishing reduced the biomass of the functional group to 40 percent of the status quo equilibrium biomass of 20,000 mt.
Table 3 Functional groups impacted at the coast-wide scale for each new fishery and all new fisheries together. Numbers show the trophic distance (number of links) to connect the target group with the affected group. X indicates effect in the combined fishery. Normal font indicates positive effect, bold font indicates negative effect, and dashes indicate no effect.
Octopus Mackerel Sea Otter Pink Shrimp Small Zooplankton Euphausiids
Deep demersal fish
Nearshore demersal fish
Shortbelly rockfish
All
– 2 2 1 – –
2 1 – 1 – –
– – – 2 2 –
– – – X – X
Shortbelly rockfish MSY was about 675 mt, and occurred under a fishing mortality of 0.2 per year. This coincided with a reduction in shortbelly biomass to 20 percent of the status quo. Because shortbelly grow quickly and reach maturity early, increasing fishing mortality to 1 was required to completely deplete shortbelly (Appendix 1).
3.2. Coast-wide impacts on non-target species Our coast-wide qualitative analysis revealed six functional groups that could be affected by one or more of the new fishing activities (Table 2). Only one of these groups was impacted by all three individual fisheries. Most of the observed impacts (5 of 6) were increases in biomass rather than declines. Fishing any of the new targets resulted in increased pink shrimp biomass. Indirect effects on functional groups that were neither a predator nor prey of the target group were at least as common as direct effects (Table 3).
Large Demersal Sharks
Toothed whales
Deep Demersal Fish Market Squid
Octopus
Deep Vertical Migrators
Pacific Hake Pink Shrimp +0-10%
Shallow Benthic Filter Feeders
Copepods
Benthic Detritivores
Benthic Carnivores
Deep Megazoobenthos
Euphausiids
Fig. 3. Coast-wide impacts of fishing deep demersal fish on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
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Pelagic Sharks
Small Cetaceans
101
Pinnipeds
Albacore
Large Piscivorous Flatfish
Piscivorous Seabirds Skates & Rays
Large Piscivorous Fish
Sablefish
Yelloweye & Cowcod
Mackerel +0-6%
Small Flatfish
Pacific Hake
Nearshore Demersal Fish
Pink Shrimp +0-6%
Benthic Detritivores
Benthic Carnivores
Fig. 4. Coast-wide impacts of fishing the miscellaneous nearshore fish group on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
Targeted fishing on the deep demersal fish group caused increases in one prey group (Fig. 3). Pink shrimp increased up to 9 percent when their predator was harvested. The remaining 10 prey groups of deep demersals were unaffected. Indirect effects of fishing deep demersals included increases in mackerels (2–6 percent) and sea otter (2–6 percent). Hake, market squid, pink shrimp, benthic detritivores, and euphausiids are all shared prey items between mackerels and the deep demersal fish group. Sea otters share many of the same benthic invertebrate prey groups with deep demersals. Fishing the miscellaneous nearshore demersal group led to increases in one prey group and two predator groups (Fig. 4). Pink shrimp (a prey group) and mackerel (a predator group) increased up to 6 percent with fishing. The remaining 2 prey groups and 12 predator groups were unaffected. Indirect effects were seen on octopus (4–16 percent increase). Harvest of shortbelly rockfish caused no direct impacts at the coast-wide level (Fig. 5). Indirect effects were observed, however (Table 3). Small zooplankton declined 2–6 percent with fishing targeting shortbelly rockfish, and pink shrimp increased (3–9 percent). The scenario combining all three new fishing activities had some additive effects. As in the individual targeting scenarios, fishing all three groups simultaneously caused an increase in pink shrimp biomass (4–16 percent). Fishing in this scenario also increased in euphausiid biomass (0–10 percent). The euphausiid effect was effectively summed across individual fishing scenarios that each had very small (less than 5 percent) positive, effects on this prey group.
3.3. Regional effects on non-target species We observed qualitatively different impacts of the fisheries at the scale of model cells and regions. Only one of the six functional groups (small zooplankton) that were affected at the coast-wide scale were impacted regionally, given the higher 20 percent change threshold. Instead, local scale impacts were concentrated exclusively on planktonic and bacteria groups (Table 4). High variances associated with these groups led to both increases and decreases within model regions as fishing increased in the individual fishery scenarios. We saw this mixed signal for benthic Table 4 Functional groups impacted by fishing activities for each new fishery and all three fisheries together (given a threshold of 20 percent change by model cell). Signs indicate whether changes were positive or negative, ± indicates both positive and negative changes were observed within each fishing scenario, depending on the model cell. * Benthic detritivores exhibited positive and negative changes as a result of fishing, but these were variable across fishing scenarios, not across model cells within a single fishing scenario. This table excludes declines in target species as a result of fishing.
Benthic Bacteria Pelagic bacteria Small Phytoplankton Large Phytoplankton Microzooplankton Copepods Benthic detritivores*
Deep demersal fish
Nearshore demersal fish
Shortbelly rockfish
All
± ± ± – ± ± ±
± ± ± – ± ± ±
± ± ± – ± ± ±
± – – – ± ± –
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Pinnipeds Pelagic Sharks Piscivorous Seabirds
Large Piscivorous Fish
Skates and Rays
Midwater Rockfish
Small Shallow Rockfish
Mackerel Canary Rockfish
Pacific Hake
Shortbelly Rockfish Market Squid
Benthic Detritivores Copepods
Gelatinous Zooplankton Benthic Carnivores
Euphausiids
Fig. 5. Coast-wide impacts of fishing shortbelly rockfish on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
and pelagic bacteria, small phytoplankton, small zooplankton, and copepods. Large phytoplankton only showed declines. The direction of changes in benthic detritivores depended on the level of fishing and the targeted fish group. For the scenario with all three new target species fished simultaneously, we saw more negative effects. Pelagic bacteria, small phytoplankton, and benthic detritivores responded negatively to the combined fishing scenario, in contrast with the mixed effects observed for each new target group fished alone. Across the regions in the model, more functional groups were negatively than positively affected at the local scale (Fig. 6). This contrasts with the coast-wide impacts, which were mostly positive. Negative impacts were highest in the Monterey region, and in the north and central parts of this region in particular. Surprisingly, the level of fishing did not have strong effects on the number of functional groups impacted. Even relatively small increases in fishing (removing 25 percent of the target groups compared to status quo) resulted in greater than 20 percent changes in some functional groups in all model regions. The combined fishing scenario did not display additive effects on the number of functional groups affected by region. Instead, the number of functional groups positively and negatively affected in the combined scenarios qualitatively tracks the most negative and most positive effects observed in the single species scenarios. 4. Discussion Our analysis of the ecosystem effects of developing new fisheries for new low biomass target species or functional groups in the CCLME showed minimal coast-wide impacts, but dramatic regional variation in the number and magnitude of effects. Only 6
of 62 functional groups were affected at the coast-wide scale, and most of these effects were positive (ranging from −2 to 16 percent change). In contrast, at a more local scale, individual model cells and regions showed impacts of greater than 20 percent for seven plankton and bacteria groups. Impacts were variable across cells and regions, and summed to no net effect at the coast-wide scale for most of these groups. Our findings highlight two important ideas in ecosystem ecology: (1) perturbing (harvesting, removing) species contributing even small proportions of total ecosystem biomass can have effects that propagate through the ecosystem and (2) regional variation in food webs can lead to qualitative differences in ecosystem impacts of perturbations across space. 4.1. Direct and indirect effects of small food web perturbations Even small perturbations can potentially cause large and unpredictable effects on ecosystems (Scheffer et al., 2001). Increasing fishing mortality acts as a press perturbation, and even small press perturbations can lead to whole system responses and ecological surprises (Bender et al., 1984; Yodzis, 1988; Ives and Carpenter, 2007). The direction of the net effect on connected species is often counter-intuitive; in a review of empirical studies, Montoya et al. (2009) found less than half of perturbations to predators had net positive effects on prey species due to the high prevalence of indirect effects. In our study, comparing impacts across the three new fisheries at a coast-wide scale suggests some functional groups are more sensitive to perturbations than others. Pink shrimp was affected by increased harvest of any of the three new groups, while Mackerel was affected by two of the three (deep demersals, nearshore demersals, or shortbelly rockfish). Identifying groups of species that may
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A. Deep Demersals
103
B. Nearshore Demersals C. Shortbelly Rockfish
D. ALL
Vancouver Columbia Eureka
Monterey
Conception
-10
-6
-2
2 4
-10
-6
-2
2 4
-10
-6
-2
2 4
-10
-6
-2
2 4
Number of species impacted by > 20 percent Fig. 6. Impacts of new target fisheries by region. Each set of bars represents a latitudinal region in the model with fishing scenarios represented from bottom to top B75, B40, B25, and B0. Bars to the left of the zero line indicate the number of functional groups that decline by more than 20 percent within at least one model cell within the region, compared to the status quo fishing scenario. Bars to the right or the zero line indicate the number of groups that increase by more than 20 percent. From left to right, panels indicate the effects of fishing deep demersal fish (A), miscellaneous nearshore demersal fish (B), shortbelly rockfish (C), and all three fisheries combined (D).
be sensitive to even low levels of fishing activities could provide an important starting point for managers developing monitoring protocols for species sensitive to indirect effects of fishing. Studies focusing on large biomass species and associated fisheries have described larger ecosystem-wide impacts of fishing on those groups, especially low trophic level species (Smith et al., 2011; Kaplan et al., 2013a,b). Using the same model of the California Current to explore more abundant forage groups, Kaplan et al. (2013a,b) saw coastwide changes of greater than 20 percent in many functional groups, in particular predators of forage species. Depleting the forage fish group or euphausiid group resulted in greater than 20 percent changes in 20–25 percent of model groups (Kaplan et al., 2013a,b). Targeting smaller biomass forage groups (mackerel and mychtophids) resulted in changes above the 20 percent threshold for up to 10 percent of model functional groups (Kaplan et al., 2013a,b). Our results did not show such widespread or dramatic changes. One possible reason for this is simply that biomass for the groups we tested is even lower than the low biomass forage groups tested by Kaplan et al. (2013a,b). For the three new fishery targets we described, our modeling results suggest these groups may be functionally redundant with other prey species (Walker, 1992). This necessarily means that fishery removals will have fewer direct impacts on ecosystem total biomass, and thus may minimize impacts on other functional groups. 4.2. Spatial variation in food web effects Our study demonstrates that variation in food web structure and the strength of interactions across space can strongly influence the
sign and magnitude of the effects of fishing across a large marine ecosystem. Empirical studies have documented food webs that vary spatially, but most of these examples are from distinct ecosystems separated by physical barriers such as lakes or disconnected river reaches (e.g. Kitching, 1987; Warren, 1989; Closs and Lake, 1994). In contrast, our work shows how species or functional group-specific movement and overlap of distributions can create spatially varying ecological interactions within a single, connected, large marine ecosystem. We saw disproportionately large numbers of species affected in the Monterey region. Our model predictions could have implications for the food web there, particularly in the Gulf of the Farallones and Monterey Bay National Marine Sanctuaries, both of which fall in the north and central Monterey region of the model. These sanctuaries provide habitat for many seabirds, marine mammals and other species of conservation concern (Office of National Marine Sanctuaries, 2009, 2010). Even if the magnitudes of the impacts of new fishing activities are underestimated or captured imperfectly by CCAM, our work identifies regions of the coast that are more likely to be affected. This kind of knowledge may aid regional managers in making proactive decisions, for example monitoring particular functional groups for evidence of fishing impacts. Understanding how food webs vary across regions requires models that capture the spatially explicit nature of species life histories and large and small-scale movements. The scale dependence of the number and type of functional groups affected demonstrates the utility of spatially explicit ecosystem models to capture regional variation in the impacts of a perturbation, such as increased fishing activity.
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4.3. Limitations There are several important caveats to our modeling approach. First, we used a very low threshold to detect coast-wide change in a more qualitative way than previous similar studies (Smith et al., 2011; Kaplan et al., 2013a,b). Therefore, the functional groups identified as “affected” may be overly conservative; this list can and should be subsequently revisited with additional data or analyses if any of the fisheries we explored actually developed on the US west coast. Second, seasonal movement constraints likely lead to under representing the effects of local depletion in the model. Vertebrate biomass is redistributed across the model domain quarterly, which could smooth over the effects of local depletion over longer time scales and might explain the paucity of effects we saw on upper trophic level groups. Third, nearly all functional groups that responded to reductions in target species biomass at the regional scale were highly productive and highly variable within a year or across years. These traits cause quick responses to changes in the ecosystem, but also lead to dynamics that are difficult to describe with quarterly model output. Overall, our work represents a first step toward understanding how fishing new target species that represent niche market low biomass groups could impact the CCLME using a spatially explicit ecosystem model. A next step would be a comparative analysis using the findings in Kaplan et al. (2013a,b) to motivate a spatially explicit comparative analysis of fishing large and small biomass forage groups. 4.4. Conclusions Adopting ecosystem based management approaches will necessarily result in identifying trade-offs between consumptive and non-consumptive uses in large marine ecosystems. Here we demonstrated the effects of three potential fisheries that our ecosystem models suggest will have relatively small impacts on the food web at the coast-wide scale. Instead, trade-offs may occur across space, with potentially cascading effects on planktonic and benthic invertebrate groups. Our results do not provide definitive predictions on the impacts of new fisheries, but identify regions and groups that could be targeted for monitoring potential impacts if these fisheries were to develop. More importantly, this work provides a necessary framework for evaluating the indirect effects of fishing at both the coast-wide and local scale in a heterogeneous large marine food web. Acknowledgements K. Marshall was supported by a postdoctoral fellowship from the National Research Council (NRC) at NOAA Fisheries. We thank four anonymous reviewers for feedback that improved this manuscript. The views expressed in this paper are those of the authors and do not reflect those of NOAA NMFS. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolmodel. 2014.07.003. References Ainley, D.G., Dugger, K.D., Ford, R.G., Pierce, S.D., Reese, D.C., Brodeur, R.D., Tynan, C.T., Barth, J.A., 2009. Association of predators and prey at frontal features in the California Current: competition, facilitation, and co-occurrence. Mar. Ecol.Prog. Ser. 389, 271–294. Alder, J., Campbell, B., Karpouzi, V., Kaschner, K., Pauly, D., 2008. Forage fish: from ecosystems to markets. Annu. Rev. Environ. Resour. 33, 153–166.
Allan, J.D., 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu. Rev. Ecol. Evol. Syst. 35, 257–284. Anderson, S.C., Flemming, J.M., Watson, R., Lotze, H.K., 2011. Rapid global expansion of invertebrate fisheries: trends drivers, and ecosystem effects. Plos One 6, http://dx.doi.org/10.1371/journal.pone.0014735. Anticamara, J., Watson, R., Gelchu, A., Pauly, D., 2011. Global fishing effort (1950–2010): trends, gaps, and implications. Fish. Res. 107, 131–136. Bellman, M., Heery, E., Hastie, J., 2008. Estimated discard and total catch of selected groundfish species in the 2007 U.S. West Coast Fisheries. West Coast Groundfish Observer Program Management Report, Seattle, Washington. Bender, E.A., Case, T.J., Gilpin, M.E., 1984. Perturbation experiments in community ecology – theory and practice. Ecology 65, 1–13. Branch, T.A., Watson, R., Fulton, E.A., Jennings, S., McGilliard, C.R., Pablico, G.T., Ricard, D., Tracey, S.R., 2010. The trophic fingerprint of marine fisheries. Nature 468, 431–435. Caissie, D., 2006. The thermal regime of rivers: a review. Freshw. Biol. 51, 1389–1406. Closs, G.P., Lake, P.S., 1994. Spatial and temporal variation in the structure of an intermittent-stream food-web. Ecol. Monogr. 64, 1–21. Cury, P.M., Boyd, I.L., Bonhommeau, S., Anker-Nilssen, T., Crawford, R.J.M., Furness, R.W., Mills, J.A., Murphy, E.J., Osterblom, H., Paleczny, M., Piatt, J.F., Roux, J.P., Shannon, L., Sydeman, W.J., 2011. Global seabird response to forage fish depletion-one-third for the birds. Science 334, 1703–1706. FAO Fisheries and Aquaculture Department, 2011. FishStatJ: Universal software for fishery statistical time series. Field, J., Dick, E., MacCall.F A., 2007. Stock assessment model for the shortbelly rockfish. Sebastes jordani, in the California Current. NOAA NMFS SWFSC Technical Memorandum 45. Fulton, E.A., Parslow, J.S., Smith, A.D.M., Johnson, C.R., 2004. Biogeochemical marine ecosystem models II: the effect of physiological detail on model performance. Ecol. Model. 173, 371–406. Fulton, E.A., Link, J.S., Kaplan, I.C., Savina-Rolland, M., Johnson, P., Ainsworth, C., Horne, P., Gorton, R., Gamble, R.J., Smith, A.D.M., Smith, D.C., 2011. Lessons in modelling and management of marine ecosystems: the Atlantis experience. Fish Fish. 12, 171–188. Gulland, J.A., 1971. The Fish Resources of the Ocean. Fishing News Books, West Byfleet, England. Hermann, A.J., Curchitser, E.N., Haidvogel, D.B., Dobbins, E.L., 2009. A comparison of remote vs. local influence of El Nino on the coastal circulation of the northeast Pacific. Deep Sea Res. II – Top. Stud. Oceanogr. 56, 2427–2443. Hipfner, J.M., 2009. Euphausiids in the diet of a North Pacific seabird: annual and seasonal variation and the role of ocean climate. Mar. Ecol.- Prog. Ser. 390, 277–289. Horne, P.J., Kaplan, I.C., Marshall, K.N., Levin, P.S., Harvey, C.J., Hermann, A.J., Fulton, E.A., 2010. Design and parameterization of a spatially explicit ecosystem model of the central California Current. NOAA NMFS NWFSC Technical Memorandum 104. Ives, A.R., Carpenter, S.R., 2007. Stability and diversity of ecosystems. Science 317, 58–62. Kaplan, I.C., Leonard, J., 2012. From krill to convenience stores: forecasting the economic and ecological effects of fisheries management on the US West Coast. Mar. Policy 36, 947–954. Kaplan, I.C., Burden, M., Levin, P.S., Fulton, E.A., 2010. Fishing catch shares in the face of global change: a framework for integrating cumulative impacts and single species management. Can. J. Fish. Aquat. Sci. 67, 1968–1982. Kaplan, I.C., Horne, P.J., Levin, P.S., 2012. Screening California Current Fishery Management Scenarios using the Atlantis End-to-End Ecosystem Model. Prog. Oceanogr. 102, 5–18. Kaplan, I.C., Brown, C.J., Fulton, E.A., Gray, I.A., Field, J.C., Smith, A.D.M., 2013a. Impacts of depleting forage species in the California Current. Environ. Conserv. 4, 380–393. Kaplan, I.C., Gray, I.A., Levin, P.S., 2013b. Cumulative impacts of fisheries in the California Current. Fish Fish. 14, 515–527. Kaplan, I.C., Holland, D.S., Fulton, E.A., 2014. Finding the accelerator and brake in an individual quota fishery: linking ecology, economics, and fleet dynamics of US West Coast trawl fisheries. ICES J. Mar. Sci. 71, 308–319. Kitching, R.L., 1987. Spatial and temporal variation in food webs in water-filled treeholes. Oikos 48, 280–288. Lenarz, W.H., 1980. Shortbelly rockfish Sebastes jordani – a large unfished resource in waters off California. Mar. Fish. Rev. 42, 34–40. Lester, S.E., McLeod, K.L., Tallis, H., Ruckelshaus, M., Halpern, B.S., Levin, P.S., Chavez, F.P., Pomeroy, C., McCay, B.J., Costello, C., 2010. Science in support of ecosystembased management for the US West Coast and beyond. Biol. Conserv. 143, 576–587. Love, M.S., McGowen, G.E., Westphal, W., Lavenberg, R.J., Martin, L., 1984. Aspects of the life-history and fishery of the white croaker, Genyonemus lineatus (Sciaenidae), off California. Fish. Bull. 82, 179–198. Matsui, T., Kato, S., Smith, S.E., 1990. Biology and potential use of Pacific grenadier Coyphaenoides acrolepis, off California. Mar. Fish. Rev. 52, 1–17. Montoya, J.M., Woodward, G., Emmerson, M.C., Sole, R.V., 2009. Press perturbations and indirect effects in real food webs. Ecology 90, 2426–2433. Morse, W.W., 1980. Maturity, spawning, and fecundity of Atlantic croaker, Micropogonias undulatus, occurring North of Cape-Hatteras, North-Carolina. Fish. Bull. 78, 190–195. Office of National Marine Sanctuaries, 2009. Monterey Bay National Marine Sanctuary Condition Report 2009. NOAA U.S. Department of Commerce, Office of National Marine Sanctuaries, Silver Spring, MD, p. 58.
K.N. Marshall et al. / Ecological Modelling 289 (2014) 96–105 Office of National Marine Sanctuaries, 2010. Gulf of the Farallones National Marine Sanctuary Condition Report 2010. NOAA U.S. Department of Commerce, Office of National Marine Sanctuaries, Silver Spring, MD, p. 58. Pacific Fisheries Information Network (PacFIN), 2011. Report # 307. Pacific States Marine Fisheries Commission, Portland, Oregon. Pacific Fishery Management Council, 1978. Fishery Managment Plan for Northern Anchovy. Pacific Fishery Management Council, 2006. Fishery Management Plan for Coastal Pelagic Species. Pacific Fishery Management Council, 2008. Management of krill as an essential component of the California Current ecosystem. Amendment 12 to the Coastal Pelagic Fishery Managment Plan. Pichegru, L., Gremillet, D., Crawford, R.J.M., Ryan, P.G., 2010. Marine no-take zone rapidly benefits endangered penguin. Biol. Lett. 6, 498–501. Rodriguez, J.P., Beard, T.D., Bennett, E.M., Cumming, G.S., Cork, S.J., Agard, J., Dobson, A.P., Peterson, G.D., 2006. Trade-offs across space, time, and ecosystem services. Ecol. Soc. 11, 28. Scheffer, M., Carpenter, S., Foley, J.A., Folke, C., Walker, B., 2001. Catastrophic shifts in ecosystems. Nature 413, 591–596.
105
Smith, A.D.M., Brown, C.J., Bulman, C.M., Fulton, E.A., Johnson, P., Kaplan, I.C., Lozano-Montes, H., Mackinson, S., Marzloff, M., Shannon, L.J., 2011. Impacts of fishing low-trophic level species on marine ecosystems. Science 333, 1147–1150. Sweeney, J.M., Harvey, J.T., 2011. Diet estimation in California sea lions, Zalophus californianus. Mar. Mamm. Sci. 27, E279–E301. Thayer, J.A., Sydeman, W.J., 2007. Spatio-temporal variability in prey harvest and reproductive ecology of a piscivorous seabird, Cerorhinca monocerata, in an upwelling system. Mar. Ecol. Prog. Ser. 329, 253–265. Walker, B.H., 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6, 18–23. Warren, P.H., 1989. Spatial and temporal variation in the structure of a fresh-water food web. Oikos 55, 299–311. White, M.L., Chittenden, M.E., 1977. Age-determination, reproduction, and population-dynamics of Atlantic croaker, Micropogonias undulatus. Fish. Bull. 75, 109–123. Yodzis, P., 1988. The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69, 508–515.
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Ecological Modelling journal homepage: www.elsevier.com/locate/ecolmodel
New target fisheries lead to spatially variable food web effects in an ecosystem model of the California Current K.N. Marshall ∗ , I.C. Kaplan, P.S. Levin Conservation Biology Division, Northwest Fishery Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Blvd E, Seattle, WA 98112, United States
a r t i c l e
i n f o
Article history: Received 18 March 2014 Received in revised form 2 July 2014 Accepted 3 July 2014 Keywords: Fishing California Current Ecosystem model Spatial Regional effects Indirect effects
a b s t r a c t Growing human populations put increasing demands on marine ecosystems. Studies have demonstrated the importance of large biomass forage groups in model food webs, but small biomass contributors are often overlooked. Here, we predict the ecosystem effects of three potential future fisheries targeting functional groups that make up only a small proportion of total ecosystem biomass using the California Current Atlantis Model: deep demersal fish such as grenadier (Albatrossia pectoralis and Coryphaenoides acrolepis), nearshore fish such as white croaker (Genyonemus lineatus), and shortbelly rockfish (Sebastes jordani). Using a spatially explicit ecosystem model, we explored individual fishing scenarios for these groups that resulted in abundance levels of 75, 40, 25, and 0 percent of the status quo fishing scenario and a combined fishing scenario simultaneously targeting all three groups. We evaluated the effects on coast-wide biomass and describe variation in affected groups by region. Results indicate that developing fisheries on the proposed targets would have small coast-wide effects on other species. However, effects varied significantly within the ecosystem, with higher impacts concentrated in the central California region of the model. Effects of fishing all three groups simultaneously were additive in some cases coastwide, but were not additive at the regional scale. This work provides a framework for evaluating effects of new fisheries and suggests that regional effects should be evaluated within a larger management context. © 2014 Published by Elsevier B.V.
1. Introduction Anthropogenic stressors on ecosystems have never been greater. Demands for food and freshwater have led to increased fishing (Anticamara et al., 2011), changes in land use patterns (Allan, 2004), and greater regulation of flows in rivers (Caissie, 2006). As pressure to extract resources builds, managers are increasingly confronting trade-offs between the direct value of the extracted resource and the indirect value of the resource left in the ecosystem (Rodriguez et al., 2006; Lester et al., 2010). Understanding these trade-offs requires approaches that can predict the indirect effects of targeted resource extraction on the rest of the ecosystem. In marine ecosystems, demands for fish and fishmeal have led to fishing activities targeting more species than in previous decades (Alder et al., 2008; Branch et al., 2010; Anderson et al., 2011). Often, new target species have low trophic levels, are important
∗ Corresponding author. Tel.: +1 206 861 7601. E-mail address: [email protected] (K.N. Marshall). http://dx.doi.org/10.1016/j.ecolmodel.2014.07.003 0304-3800/© 2014 Published by Elsevier B.V.
prey species for higher trophic level species that are of commercial importance and/or conservation concern. Therefore, a trade-off exists between the value of harvesting these forage species and the value of leaving them as prey for other species in the ecosystem. On the US West Coast, fishing limits have been put into place to protect high biomass, low trophic level species such as krill and anchovy (Pacific Fishery Management Council, 1978, 2008). These rules seek to protect from ecosystem overfishing and maintain the prey base for species that are the targets of existing fisheries. Recently, the effect of adding new fisheries for low trophic level species that constitute large proportions of the biomass of marine ecosystems has been the target of much research (Cury et al., 2011; Smith et al., 2011; Kaplan et al., 2013a,b). These efforts often focus on species or groups with high biomass, while low biomass species or groups are more easily overlooked. Fishing on low biomass groups may indeed have few impacts on food webs if those species are functionally redundant to high-biomass prey groups (Walker, 1992). However, removals of low biomass groups may have disproportionately large impacts, depending on their role in the ecosystem and spatial distribution and overlap of predators and prey. For example, central place foragers, like many seabirds,
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depend on locally abundant seasonal prey resources (Ainley et al., 2009; Pichegru et al., 2010; Cury et al., 2011). Fluctuations in these resources over small spatial and temporal scales could have severe impacts on populations that rely on them, even if a prey contributes low proportions to the overall seabird diet over the course of a year when compared to other potential prey species (Hipfner, 2009). In this study, we investigated the effects of targeted fisheries on relatively low biomass functional groups in a large marine ecosystem. Similar to previous modeling studies, we report biomass responses of species in the food web. However this work is novel in that we also explore regional variation in biomass impacts, as well as ecosystem-wide effects. We investigated target species that were broadly and narrowly distributed across the ecosystem to explore the effects of spatial variation in the food web on the impacts of fishery development. The California Current Large Marine Ecosystem (CCLME) and its associated fisheries provide an excellent example system to investigate how future fishery development could affect existing fishery yields and food web biomass distribution. The largest fleet in the ecosystem, the US west coast groundfish fishery, uses midwater and bottom gear to target 90 species of flatfish, rockfish, and roundfish. Four of these stocks are currently overfished and subject to rebuilding plans. Coastal pelagic fisheries target sardine, mackerel, anchovy and squid. To protect the pelagic prey base, krill fishing is completely banned, and sardine catch limits are set to maintain a minimum of 150,000 mt (Pacific Fishery Management Council, 2006). Here, we explore the potential effects of fishery development targeting new species with lower biomass than species previously investigated by others (Smith et al., 2011; Kaplan et al., 2013a,b). We created ecological forecasts under new fishing scenarios using an Atlantis ecosystem model for the California Current (Horne et al., 2010; Kaplan et al., 2012). Using these forecasts we explored the impacts of new fishery development on the coast-wide and regional distribution of other functional groups in the model. We describe how variation in the distributions of target and non-target species affects impacts of fisheries in a spatially heterogeneous ecosystem. 2. Methods 2.1. Model framework Atlantis is a three dimensional, spatially explicit ecosystem model, comprised of three sub-models (Fig. 1, Fulton et al., 2004). The oceanographic sub-model simulates physical transport using output from a Regional Ocean Modeling System to track temperature, salinity, and circulation. The ecological sub-model captures
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nitrogen and silicon dynamics through trophic interactions among cells, representing functional groups from bacteria and plankton to fish and marine mammals. The human impacts sub-model overlays both the ecological and oceanographic sub-models, and includes fisheries, nutrient inputs, and management control rules. This framework allows for hypothesis testing of how perturbations in the food web can propagate all the way to the management arena. The Atlantis modeling framework has been applied to ecosystems around the world; Fulton et al. (2011) summarized assumptions and options within the Atlantis code base, and detailed lessons learned from 13 recent modeling efforts around the globe. An Atlantis model was developed for the CCLME (California Current Atlantis Model – CCAM) to address federal and state level management needs (Horne et al., 2010; Kaplan et al., 2012). The modeled area extends from Cape Flattery in the north to Point Conception in the south and from shoreline to the 2400 m isobaths (Fig. 2). There are 12 latitudinal regions, broken up longitudinally by 3–7 depth zones. Each of these two dimensional areas is further divided into up to seven depth bins, capturing the sediment layer to the surface layer through the water column. The central California region of the model has higher 2-d spatial resolution in depth zones than the northern and southern regions. CCAM oceanography is based on projections of physical oceanography from a Regional Ocean Modeling System, for the period from 1958 to 2004 (Hermann et al., 2009). The ecological sub-model for CCAM compartmentalizes biomass among 62 functional groups, from phytoplankton to marine mammals. Twenty-seven groups are dedicated to capturing the diversity of fish species in the ecosystem. These groups best represent commercially harvested fish stocks, and groundfish in particular. Species are grouped based on similar life history characteristics and diets. Vertebrate functional groups are represented using 10 ageclasses, while invertebrate groups are simple biomass pools. Key features of the ecological model include type 2 functional responses for all consumers, Beverton–Holt recruitment for fish species, and 3 options for vertebrate movement (migration into and out of the model, seasonal movement within model bounds, and diel vertical migrations). This model has been calibrated to match historical patterns of abundance observed in the field or estimated from stock assessments, and to recreate levels of species productivity that are consistent with literature and stock assessment estimates. The model has been used in multiple applications in the California Current, described in Table 1. Additional details of model parameterization and calibration can be found in technical documentation and these applications (e.g. Horne et al., 2010; Kaplan et al., 2012). We used a “status quo” fishing scenario against which to compare all new fishing activities in the model. The status quo represented current fishing in the CCLME from about 2005 to 2008, and was the same as in Kaplan et al. (2012). Spatial closures represented current area-based management, and fishing mortalities were specified by targeted group and fleet and calibrated to reproduce catches from stock assessments, where applicable (Horne et al., 2010).
Table 1 Applications of the Atlantis modeling framework to the California Current Large Marine Ecosystem.
Fig. 1. A conceptual diagram of the Atlantis modeling framework.
Application
Citations
Food web impacts of forage fish fisheries Evaluating fishery management strategies (spatial management, harvest rates, quota systems) Evaluating risks of climate change, ocean acidification, and cumulative impacts of fishing
Kaplan et al. (2013a), Smith et al. (2011) Kaplan et al. (2012),Kaplan et al. (2014), Kaplan and Leonard (2012) Kaplan et al. (2010), Kaplan et al. (2013b)
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Fig. 2. Status quo distribution of new potential target groups (deep demersal fish, nearshore miscellaneous demersal fish, and shortbelly rockfish). Top panels illustrate distribution in the full model domain (A, B, C). Latitudinal regions are labeled to correspond roughly with historic International North Pacific Fisheries Commission management areas. Bottom panels show target group distribution within Central California region (D, E, F). Deep demersal fish densities were highest in slope cells (A, D), nearshore miscellaneous fish were limited to coastal areas (B, E), and shortbelly rockfish were concentrated in Central California (C, F). Legend below each panel indicates densities in kg/m2 .
2.2. Approach We explored the impacts of new fishing activities targeting three functional groups for which harvest is currently very limited. For each new target group, we created a new fleet in the model and determined the appropriate area closures based on the likely gear type required to target that group. We ran fishing scenarios for each fishery addition alone and all three fisheries together, following methods by Smith et al. (2011) and Kaplan et al. (2013a,b). For each fishery, we incrementally increased the annual fishing mortality from zero until the target group was completely depleted. Each model run was 50 years, allowing functional groups to reach quasi-equilibrium; the model does not assume true equilibrium dynamics and is driven by oceanographic forcing as well as species interactions. We then used these fishing mortalities and resulting catches to determine the maximum sustainable yield (MSY) for each group, as well as the fishing mortality required to obtain 4 levels of abundance relative to the status quo fishing scenario: 0 percent, 25 percent, 40 percent, and 75 percent of status quo biomass. For the combined fishery scenario, we used fishing mortalities determined from each single fishery scenario and fished all three target groups simultaneously.
We describe the impacts of the new fisheries on quasiequilibrium yields and biomasses of the other functional groups in the model. We averaged the last five years of quarterly model output to represent an equilibrium catch or biomass for each functional group, with two exceptions. For groups that migrate outside the model boundaries during each year (Pacific hake, small planktivorous fish, albacore, migratory seabirds, salmon, piscivorous seabirds, pinnipeds, baleen whales, toothed whales, and small cetaceans), we averaged over the peak biomass in each of the last 5 years. The second exception was for groups with high growth rates and quick turnover that lead to population trajectories with high variance through time. For these groups (all plankton, zooplankton, and bacteria) we averaged over the last 20 years of model output. We excluded from our analysis groups that were poorly modeled in the status-quo fishing scenario, defined as biomass dropping below 10 percent of initial biomass in a 50 year run (bivalves, large crabs, benthic grazers, macroalgae, benthic infauna, salmon, small sharks, and jumbo squid). We describe impacts at two spatial scales. Coast-wide impacts were summarized qualitatively, characterizing all changes in the ecosystem as positive, negative, or neutral, with a conservative five percent change threshold. This low threshold eliminates some
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Table 2 Summary of fishing scenarios and target groups. Biomass and yield indicated are for status quo (SQ) model run. M indicates annual natural mortality rate. Maximum sustained yield (MSY) was determined using all fishing scenarios for each target group, and FMSY indicates the fishing mortality rate at MSY. Annual fishing mortality required to obtain 75, 40, 25, and 0 percent of status quo abundance is indicated by F75, F40, F25, and F0, respectively. Target group
SQ biomass (mt)
SQ yield (mt)
M
MSY (mt)
FMSY
F75
F40
F25
F0
Deep demersal fish Misc. nearshore demersal fish Shortbelly rockfish (Sebastes jordani)
183,562 20,920 16,434
2117 206 0.1
0.1 0.62 0.35
2055 9905 6687
0.03 0.12 0.2
0.01 0.04 0.05
0.03 0.1 0.1
0.04 00.12 0.2
0.1 0.24 1
level of noisiness and rounding errors associated with aggregating output, but likely captures all possible coast-wide impacts of fishing the new target groups. We used this five percent threshold because each simulated fishery targeted a small portion of the entire biomass captured in the model. Therefore, we did not expect to see large magnitude changes at the coast-wide scale as a result of our new fisheries. To characterize variability in the effects of new fishing activities along the coast, we represented each latitudinal zone in the model as a separate region. Regions roughly correspond with those historically identified by the International Pacific Fisheries Commission (INPFC) and the Pacific Fishery Management Council (http://www.pcouncil.org/wp-content/uploads/georock.pdf). Within each region, we summarized changes to functional group biomass over 2-dimensional model cells (summed over depth bins). Here, we used a threshold of 20 percent change in catch or biomass, as in Kaplan et al. (2013a,b). Within a latitudinal zone, a group was determined “impacted” if it met the 20 percent threshold in at least one cell within that latitudinal section.
2.3. New target groups In the following sections, we briefly describe the three functional groups for which we created new fisheries in the model. We describe the distribution of each group in the model, describe any current fishing activities, and outline the gear that would likely be used to target the group. We also identify the potential for a harvest market to develop.
2.3.1. Deep demersal fish The deep demersal fish group in CCAM is distributed along the continental slope (500–1200 m, Fig. 2A), and consists mostly of giant grenadier (Albatrossia pectoralis) and Pacific grenadier (Coryphaenoides acrolepis). Other species in this functional group include Pacific lamprey, eelpouts, cusk eels, and poachers (Horne et al., 2010). The west coast groundfish fleet has incidental catches of both grenadier species. Bellman et al. (2008) estimated one to two percent of the annual catch at depths greater than 250 m consists of giant and Pacific grenadier, totaling 600 mt per year. These species are rarely landed because of limited market demand (Matsui et al., 1990). A pot fishery for hagfish is also included in CCAM with harvest of 1250 mt per year (Table 2). Grenadier (family Macrouridae) catches around the world have risen since the mid 1990s. Targeted fisheries currently harvest about 45,000 mt of grenadier from the world’s oceans each year (FAO Fisheries and Aquaculture Department, 2011). In the North Pacific, Japanese harvested grenadier during the 1980s. They were processed into surimi, before the walleye Pollock fishery became a more marketable source (Matsui et al., 1990). Due to historical use and increasing demand for fish and fish products, we thought it would be useful to explore the potential impacts of landing this species complex on the US west coast. Natural mortality for the deep demersal fish group is low (0.1, Table 2), which suggests a priori that MSY will also be relatively low (Gulland, 1971). We created a target fishery on this group that
represents a fishery for grenadier using the same gear and area restrictions as the existing bottom trawl fleet (Kaplan et al., 2012). 2.3.2. Miscellaneous nearshore fish The nearshore miscellaneous fish group is a catchall group dominated by white croaker (Genyonemus lineatus), but also includes shallow sculpins and midshipman. This group is distributed across the nearshore model domain, with higher densities in central California than other regions (Fig. 2B). Life history parameters for this group are based on white croaker (Horne et al., 2010). We created a fishery on this group primarily to represent a fishery targeting white croaker. Croaker is a popular recreational target in California, but only small amounts are currently landed in commercial fisheries annually (3 mt in 2011) using round haul net, gill net, and hook and line gear (Pacific Fisheries Information Network (PacFIN), 2011). Atlantic croaker (Micropogonia undulatus) is a closely related species on the east coast of the US, with similar size, life history, and habitat and food preferences (White and Chittenden, 1977; Morse, 1980). Atlantic croaker is the target of a valuable 10,000 mt fishery (FAO Fisheries and Aquaculture Department, 2011). While the distribution of the miscellaneous nearshore fish group spans the latitudinal extent of the model domain, in reality, white croaker likely composes greater proportions of the group’s biomass from San Francisco bay south to Point Conception (Love et al., 1984). An existing modeled recreational fishery accounts for 247 mt of biomass removed from this group each year. The natural mortality rate for the group is 0.62, suggesting it would tolerate a moderate harvest rate (Table 1). We created a target fishery for croaker using the same area closures as the existing nearshore non-fixed gear sector (Kaplan et al., 2012). 2.3.3. Shortbelly rockfish Shortbelly rockfish is the most abundant of the rockfish species, and comprise their own functional group in CCAM. The most current stock assessment estimated the shortbelly stock to be 64,000 mt in 2005 (Field et al., 2007). While we initialized shortbelly biomass at that level, the quasi-equilibrium biomass in our status-quo scenario is roughly 25 percent of that value (Table 1). Considerable biomass uncertainty results from a lack of fishery dependent data and poor catchability of shortbelly in the fisheries independent trawl survey (Field et al., 2007). Shortbelly rockfish density is highest in central California (Fig. 2C). A few fleets unintentionally catch shortbelly, but these removals are limited to less than 1 mt per year (Bellman et al., 2008). A relatively high natural mortality rate in CCAM (0.35) suggests that this group should be able to sustain a moderate level of fishing mortality (Table 1). We modeled the shortbelly fishery as a mid-water trawl fishery, subjected to the same area closures as the existing groundfish trawl fleet (Kaplan et al., 2012). Fishery interest in shortbelly rockfish has historically been quite low, at least in part because shortbelly are small (maximum size less than 30 cm) (Lenarz, 1980, Field et al., 2007). Lenarz (Lenarz, 1980) identified a potential pet food or surimi market for shortbelly, however he also pointed out these were not economically viable as of 1980. Currently, an annual catch target of 50 mt is in
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place for shortbelly. The groundfish catch regulations indicate this limit is higher than recent catches of shortbelly, but the target is set conservatively because shortbelly is an important forage species for seabirds and marine mammals in the California Current ecosystem (Thayer and Sydeman, 2007; Sweeney and Harvey, 2011).
3. Results We found both general and fishery- and region-specific effects of developing fisheries for three low biomass, low trophic level groups. In this section, we first briefly describe the impacts of the three new fisheries on the species they targeted. Next, we describe patterns of ecosystem response at the coast-wide scale across all fisheries. Last, we describe regional variation in impacts across and within the fisheries.
3.1. Impacts on target species Simulations suggested that deep demersal fish could sustain a maximum harvest of 2055 mt per year, which required annual fishing mortality of 0.03. This level of fishing reduced the biomass of this group to 66,747 mt (about 40 percent of the status quo biomass, Appendix 1). The current estimate for grenadier bycatch is 600 mt (Bellman et al., 2008), resulting in capacity for a fishery using the same gear as the current trawl fishery of about 2600 mt sustained yield. A fishery on the nearshore demersal fish group attained a MSY of 2000 mt with an annual fishing mortality of 0.1 (Appendix 1, Table 1). This level of fishing reduced the biomass of the functional group to 40 percent of the status quo equilibrium biomass of 20,000 mt.
Table 3 Functional groups impacted at the coast-wide scale for each new fishery and all new fisheries together. Numbers show the trophic distance (number of links) to connect the target group with the affected group. X indicates effect in the combined fishery. Normal font indicates positive effect, bold font indicates negative effect, and dashes indicate no effect.
Octopus Mackerel Sea Otter Pink Shrimp Small Zooplankton Euphausiids
Deep demersal fish
Nearshore demersal fish
Shortbelly rockfish
All
– 2 2 1 – –
2 1 – 1 – –
– – – 2 2 –
– – – X – X
Shortbelly rockfish MSY was about 675 mt, and occurred under a fishing mortality of 0.2 per year. This coincided with a reduction in shortbelly biomass to 20 percent of the status quo. Because shortbelly grow quickly and reach maturity early, increasing fishing mortality to 1 was required to completely deplete shortbelly (Appendix 1).
3.2. Coast-wide impacts on non-target species Our coast-wide qualitative analysis revealed six functional groups that could be affected by one or more of the new fishing activities (Table 2). Only one of these groups was impacted by all three individual fisheries. Most of the observed impacts (5 of 6) were increases in biomass rather than declines. Fishing any of the new targets resulted in increased pink shrimp biomass. Indirect effects on functional groups that were neither a predator nor prey of the target group were at least as common as direct effects (Table 3).
Large Demersal Sharks
Toothed whales
Deep Demersal Fish Market Squid
Octopus
Deep Vertical Migrators
Pacific Hake Pink Shrimp +0-10%
Shallow Benthic Filter Feeders
Copepods
Benthic Detritivores
Benthic Carnivores
Deep Megazoobenthos
Euphausiids
Fig. 3. Coast-wide impacts of fishing deep demersal fish on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
K.N. Marshall et al. / Ecological Modelling 289 (2014) 96–105
Pelagic Sharks
Small Cetaceans
101
Pinnipeds
Albacore
Large Piscivorous Flatfish
Piscivorous Seabirds Skates & Rays
Large Piscivorous Fish
Sablefish
Yelloweye & Cowcod
Mackerel +0-6%
Small Flatfish
Pacific Hake
Nearshore Demersal Fish
Pink Shrimp +0-6%
Benthic Detritivores
Benthic Carnivores
Fig. 4. Coast-wide impacts of fishing the miscellaneous nearshore fish group on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
Targeted fishing on the deep demersal fish group caused increases in one prey group (Fig. 3). Pink shrimp increased up to 9 percent when their predator was harvested. The remaining 10 prey groups of deep demersals were unaffected. Indirect effects of fishing deep demersals included increases in mackerels (2–6 percent) and sea otter (2–6 percent). Hake, market squid, pink shrimp, benthic detritivores, and euphausiids are all shared prey items between mackerels and the deep demersal fish group. Sea otters share many of the same benthic invertebrate prey groups with deep demersals. Fishing the miscellaneous nearshore demersal group led to increases in one prey group and two predator groups (Fig. 4). Pink shrimp (a prey group) and mackerel (a predator group) increased up to 6 percent with fishing. The remaining 2 prey groups and 12 predator groups were unaffected. Indirect effects were seen on octopus (4–16 percent increase). Harvest of shortbelly rockfish caused no direct impacts at the coast-wide level (Fig. 5). Indirect effects were observed, however (Table 3). Small zooplankton declined 2–6 percent with fishing targeting shortbelly rockfish, and pink shrimp increased (3–9 percent). The scenario combining all three new fishing activities had some additive effects. As in the individual targeting scenarios, fishing all three groups simultaneously caused an increase in pink shrimp biomass (4–16 percent). Fishing in this scenario also increased in euphausiid biomass (0–10 percent). The euphausiid effect was effectively summed across individual fishing scenarios that each had very small (less than 5 percent) positive, effects on this prey group.
3.3. Regional effects on non-target species We observed qualitatively different impacts of the fisheries at the scale of model cells and regions. Only one of the six functional groups (small zooplankton) that were affected at the coast-wide scale were impacted regionally, given the higher 20 percent change threshold. Instead, local scale impacts were concentrated exclusively on planktonic and bacteria groups (Table 4). High variances associated with these groups led to both increases and decreases within model regions as fishing increased in the individual fishery scenarios. We saw this mixed signal for benthic Table 4 Functional groups impacted by fishing activities for each new fishery and all three fisheries together (given a threshold of 20 percent change by model cell). Signs indicate whether changes were positive or negative, ± indicates both positive and negative changes were observed within each fishing scenario, depending on the model cell. * Benthic detritivores exhibited positive and negative changes as a result of fishing, but these were variable across fishing scenarios, not across model cells within a single fishing scenario. This table excludes declines in target species as a result of fishing.
Benthic Bacteria Pelagic bacteria Small Phytoplankton Large Phytoplankton Microzooplankton Copepods Benthic detritivores*
Deep demersal fish
Nearshore demersal fish
Shortbelly rockfish
All
± ± ± – ± ± ±
± ± ± – ± ± ±
± ± ± – ± ± ±
± – – – ± ± –
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Pinnipeds Pelagic Sharks Piscivorous Seabirds
Large Piscivorous Fish
Skates and Rays
Midwater Rockfish
Small Shallow Rockfish
Mackerel Canary Rockfish
Pacific Hake
Shortbelly Rockfish Market Squid
Benthic Detritivores Copepods
Gelatinous Zooplankton Benthic Carnivores
Euphausiids
Fig. 5. Coast-wide impacts of fishing shortbelly rockfish on their predators and prey. Each oval shows a prey or predator species of the target species and vertical position approximates trophic level. Impacts are given by shading: light gray indicates positive impacts, dark gray indicates negative impacts, and no shading indicates no impact.
and pelagic bacteria, small phytoplankton, small zooplankton, and copepods. Large phytoplankton only showed declines. The direction of changes in benthic detritivores depended on the level of fishing and the targeted fish group. For the scenario with all three new target species fished simultaneously, we saw more negative effects. Pelagic bacteria, small phytoplankton, and benthic detritivores responded negatively to the combined fishing scenario, in contrast with the mixed effects observed for each new target group fished alone. Across the regions in the model, more functional groups were negatively than positively affected at the local scale (Fig. 6). This contrasts with the coast-wide impacts, which were mostly positive. Negative impacts were highest in the Monterey region, and in the north and central parts of this region in particular. Surprisingly, the level of fishing did not have strong effects on the number of functional groups impacted. Even relatively small increases in fishing (removing 25 percent of the target groups compared to status quo) resulted in greater than 20 percent changes in some functional groups in all model regions. The combined fishing scenario did not display additive effects on the number of functional groups affected by region. Instead, the number of functional groups positively and negatively affected in the combined scenarios qualitatively tracks the most negative and most positive effects observed in the single species scenarios. 4. Discussion Our analysis of the ecosystem effects of developing new fisheries for new low biomass target species or functional groups in the CCLME showed minimal coast-wide impacts, but dramatic regional variation in the number and magnitude of effects. Only 6
of 62 functional groups were affected at the coast-wide scale, and most of these effects were positive (ranging from −2 to 16 percent change). In contrast, at a more local scale, individual model cells and regions showed impacts of greater than 20 percent for seven plankton and bacteria groups. Impacts were variable across cells and regions, and summed to no net effect at the coast-wide scale for most of these groups. Our findings highlight two important ideas in ecosystem ecology: (1) perturbing (harvesting, removing) species contributing even small proportions of total ecosystem biomass can have effects that propagate through the ecosystem and (2) regional variation in food webs can lead to qualitative differences in ecosystem impacts of perturbations across space. 4.1. Direct and indirect effects of small food web perturbations Even small perturbations can potentially cause large and unpredictable effects on ecosystems (Scheffer et al., 2001). Increasing fishing mortality acts as a press perturbation, and even small press perturbations can lead to whole system responses and ecological surprises (Bender et al., 1984; Yodzis, 1988; Ives and Carpenter, 2007). The direction of the net effect on connected species is often counter-intuitive; in a review of empirical studies, Montoya et al. (2009) found less than half of perturbations to predators had net positive effects on prey species due to the high prevalence of indirect effects. In our study, comparing impacts across the three new fisheries at a coast-wide scale suggests some functional groups are more sensitive to perturbations than others. Pink shrimp was affected by increased harvest of any of the three new groups, while Mackerel was affected by two of the three (deep demersals, nearshore demersals, or shortbelly rockfish). Identifying groups of species that may
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A. Deep Demersals
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B. Nearshore Demersals C. Shortbelly Rockfish
D. ALL
Vancouver Columbia Eureka
Monterey
Conception
-10
-6
-2
2 4
-10
-6
-2
2 4
-10
-6
-2
2 4
-10
-6
-2
2 4
Number of species impacted by > 20 percent Fig. 6. Impacts of new target fisheries by region. Each set of bars represents a latitudinal region in the model with fishing scenarios represented from bottom to top B75, B40, B25, and B0. Bars to the left of the zero line indicate the number of functional groups that decline by more than 20 percent within at least one model cell within the region, compared to the status quo fishing scenario. Bars to the right or the zero line indicate the number of groups that increase by more than 20 percent. From left to right, panels indicate the effects of fishing deep demersal fish (A), miscellaneous nearshore demersal fish (B), shortbelly rockfish (C), and all three fisheries combined (D).
be sensitive to even low levels of fishing activities could provide an important starting point for managers developing monitoring protocols for species sensitive to indirect effects of fishing. Studies focusing on large biomass species and associated fisheries have described larger ecosystem-wide impacts of fishing on those groups, especially low trophic level species (Smith et al., 2011; Kaplan et al., 2013a,b). Using the same model of the California Current to explore more abundant forage groups, Kaplan et al. (2013a,b) saw coastwide changes of greater than 20 percent in many functional groups, in particular predators of forage species. Depleting the forage fish group or euphausiid group resulted in greater than 20 percent changes in 20–25 percent of model groups (Kaplan et al., 2013a,b). Targeting smaller biomass forage groups (mackerel and mychtophids) resulted in changes above the 20 percent threshold for up to 10 percent of model functional groups (Kaplan et al., 2013a,b). Our results did not show such widespread or dramatic changes. One possible reason for this is simply that biomass for the groups we tested is even lower than the low biomass forage groups tested by Kaplan et al. (2013a,b). For the three new fishery targets we described, our modeling results suggest these groups may be functionally redundant with other prey species (Walker, 1992). This necessarily means that fishery removals will have fewer direct impacts on ecosystem total biomass, and thus may minimize impacts on other functional groups. 4.2. Spatial variation in food web effects Our study demonstrates that variation in food web structure and the strength of interactions across space can strongly influence the
sign and magnitude of the effects of fishing across a large marine ecosystem. Empirical studies have documented food webs that vary spatially, but most of these examples are from distinct ecosystems separated by physical barriers such as lakes or disconnected river reaches (e.g. Kitching, 1987; Warren, 1989; Closs and Lake, 1994). In contrast, our work shows how species or functional group-specific movement and overlap of distributions can create spatially varying ecological interactions within a single, connected, large marine ecosystem. We saw disproportionately large numbers of species affected in the Monterey region. Our model predictions could have implications for the food web there, particularly in the Gulf of the Farallones and Monterey Bay National Marine Sanctuaries, both of which fall in the north and central Monterey region of the model. These sanctuaries provide habitat for many seabirds, marine mammals and other species of conservation concern (Office of National Marine Sanctuaries, 2009, 2010). Even if the magnitudes of the impacts of new fishing activities are underestimated or captured imperfectly by CCAM, our work identifies regions of the coast that are more likely to be affected. This kind of knowledge may aid regional managers in making proactive decisions, for example monitoring particular functional groups for evidence of fishing impacts. Understanding how food webs vary across regions requires models that capture the spatially explicit nature of species life histories and large and small-scale movements. The scale dependence of the number and type of functional groups affected demonstrates the utility of spatially explicit ecosystem models to capture regional variation in the impacts of a perturbation, such as increased fishing activity.
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4.3. Limitations There are several important caveats to our modeling approach. First, we used a very low threshold to detect coast-wide change in a more qualitative way than previous similar studies (Smith et al., 2011; Kaplan et al., 2013a,b). Therefore, the functional groups identified as “affected” may be overly conservative; this list can and should be subsequently revisited with additional data or analyses if any of the fisheries we explored actually developed on the US west coast. Second, seasonal movement constraints likely lead to under representing the effects of local depletion in the model. Vertebrate biomass is redistributed across the model domain quarterly, which could smooth over the effects of local depletion over longer time scales and might explain the paucity of effects we saw on upper trophic level groups. Third, nearly all functional groups that responded to reductions in target species biomass at the regional scale were highly productive and highly variable within a year or across years. These traits cause quick responses to changes in the ecosystem, but also lead to dynamics that are difficult to describe with quarterly model output. Overall, our work represents a first step toward understanding how fishing new target species that represent niche market low biomass groups could impact the CCLME using a spatially explicit ecosystem model. A next step would be a comparative analysis using the findings in Kaplan et al. (2013a,b) to motivate a spatially explicit comparative analysis of fishing large and small biomass forage groups. 4.4. Conclusions Adopting ecosystem based management approaches will necessarily result in identifying trade-offs between consumptive and non-consumptive uses in large marine ecosystems. Here we demonstrated the effects of three potential fisheries that our ecosystem models suggest will have relatively small impacts on the food web at the coast-wide scale. Instead, trade-offs may occur across space, with potentially cascading effects on planktonic and benthic invertebrate groups. Our results do not provide definitive predictions on the impacts of new fisheries, but identify regions and groups that could be targeted for monitoring potential impacts if these fisheries were to develop. More importantly, this work provides a necessary framework for evaluating the indirect effects of fishing at both the coast-wide and local scale in a heterogeneous large marine food web. Acknowledgements K. Marshall was supported by a postdoctoral fellowship from the National Research Council (NRC) at NOAA Fisheries. We thank four anonymous reviewers for feedback that improved this manuscript. The views expressed in this paper are those of the authors and do not reflect those of NOAA NMFS. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolmodel. 2014.07.003. References Ainley, D.G., Dugger, K.D., Ford, R.G., Pierce, S.D., Reese, D.C., Brodeur, R.D., Tynan, C.T., Barth, J.A., 2009. Association of predators and prey at frontal features in the California Current: competition, facilitation, and co-occurrence. Mar. Ecol.Prog. Ser. 389, 271–294. Alder, J., Campbell, B., Karpouzi, V., Kaschner, K., Pauly, D., 2008. Forage fish: from ecosystems to markets. Annu. Rev. Environ. Resour. 33, 153–166.
Allan, J.D., 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu. Rev. Ecol. Evol. Syst. 35, 257–284. Anderson, S.C., Flemming, J.M., Watson, R., Lotze, H.K., 2011. Rapid global expansion of invertebrate fisheries: trends drivers, and ecosystem effects. Plos One 6, http://dx.doi.org/10.1371/journal.pone.0014735. Anticamara, J., Watson, R., Gelchu, A., Pauly, D., 2011. Global fishing effort (1950–2010): trends, gaps, and implications. Fish. Res. 107, 131–136. Bellman, M., Heery, E., Hastie, J., 2008. Estimated discard and total catch of selected groundfish species in the 2007 U.S. West Coast Fisheries. West Coast Groundfish Observer Program Management Report, Seattle, Washington. Bender, E.A., Case, T.J., Gilpin, M.E., 1984. Perturbation experiments in community ecology – theory and practice. Ecology 65, 1–13. Branch, T.A., Watson, R., Fulton, E.A., Jennings, S., McGilliard, C.R., Pablico, G.T., Ricard, D., Tracey, S.R., 2010. The trophic fingerprint of marine fisheries. Nature 468, 431–435. Caissie, D., 2006. The thermal regime of rivers: a review. Freshw. Biol. 51, 1389–1406. Closs, G.P., Lake, P.S., 1994. Spatial and temporal variation in the structure of an intermittent-stream food-web. Ecol. Monogr. 64, 1–21. Cury, P.M., Boyd, I.L., Bonhommeau, S., Anker-Nilssen, T., Crawford, R.J.M., Furness, R.W., Mills, J.A., Murphy, E.J., Osterblom, H., Paleczny, M., Piatt, J.F., Roux, J.P., Shannon, L., Sydeman, W.J., 2011. Global seabird response to forage fish depletion-one-third for the birds. Science 334, 1703–1706. FAO Fisheries and Aquaculture Department, 2011. FishStatJ: Universal software for fishery statistical time series. Field, J., Dick, E., MacCall.F A., 2007. Stock assessment model for the shortbelly rockfish. Sebastes jordani, in the California Current. NOAA NMFS SWFSC Technical Memorandum 45. Fulton, E.A., Parslow, J.S., Smith, A.D.M., Johnson, C.R., 2004. Biogeochemical marine ecosystem models II: the effect of physiological detail on model performance. Ecol. Model. 173, 371–406. Fulton, E.A., Link, J.S., Kaplan, I.C., Savina-Rolland, M., Johnson, P., Ainsworth, C., Horne, P., Gorton, R., Gamble, R.J., Smith, A.D.M., Smith, D.C., 2011. Lessons in modelling and management of marine ecosystems: the Atlantis experience. Fish Fish. 12, 171–188. Gulland, J.A., 1971. The Fish Resources of the Ocean. Fishing News Books, West Byfleet, England. Hermann, A.J., Curchitser, E.N., Haidvogel, D.B., Dobbins, E.L., 2009. A comparison of remote vs. local influence of El Nino on the coastal circulation of the northeast Pacific. Deep Sea Res. II – Top. Stud. Oceanogr. 56, 2427–2443. Hipfner, J.M., 2009. Euphausiids in the diet of a North Pacific seabird: annual and seasonal variation and the role of ocean climate. Mar. Ecol.- Prog. Ser. 390, 277–289. Horne, P.J., Kaplan, I.C., Marshall, K.N., Levin, P.S., Harvey, C.J., Hermann, A.J., Fulton, E.A., 2010. Design and parameterization of a spatially explicit ecosystem model of the central California Current. NOAA NMFS NWFSC Technical Memorandum 104. Ives, A.R., Carpenter, S.R., 2007. Stability and diversity of ecosystems. Science 317, 58–62. Kaplan, I.C., Leonard, J., 2012. From krill to convenience stores: forecasting the economic and ecological effects of fisheries management on the US West Coast. Mar. Policy 36, 947–954. Kaplan, I.C., Burden, M., Levin, P.S., Fulton, E.A., 2010. Fishing catch shares in the face of global change: a framework for integrating cumulative impacts and single species management. Can. J. Fish. Aquat. Sci. 67, 1968–1982. Kaplan, I.C., Horne, P.J., Levin, P.S., 2012. Screening California Current Fishery Management Scenarios using the Atlantis End-to-End Ecosystem Model. Prog. Oceanogr. 102, 5–18. Kaplan, I.C., Brown, C.J., Fulton, E.A., Gray, I.A., Field, J.C., Smith, A.D.M., 2013a. Impacts of depleting forage species in the California Current. Environ. Conserv. 4, 380–393. Kaplan, I.C., Gray, I.A., Levin, P.S., 2013b. Cumulative impacts of fisheries in the California Current. Fish Fish. 14, 515–527. Kaplan, I.C., Holland, D.S., Fulton, E.A., 2014. Finding the accelerator and brake in an individual quota fishery: linking ecology, economics, and fleet dynamics of US West Coast trawl fisheries. ICES J. Mar. Sci. 71, 308–319. Kitching, R.L., 1987. Spatial and temporal variation in food webs in water-filled treeholes. Oikos 48, 280–288. Lenarz, W.H., 1980. Shortbelly rockfish Sebastes jordani – a large unfished resource in waters off California. Mar. Fish. Rev. 42, 34–40. Lester, S.E., McLeod, K.L., Tallis, H., Ruckelshaus, M., Halpern, B.S., Levin, P.S., Chavez, F.P., Pomeroy, C., McCay, B.J., Costello, C., 2010. Science in support of ecosystembased management for the US West Coast and beyond. Biol. Conserv. 143, 576–587. Love, M.S., McGowen, G.E., Westphal, W., Lavenberg, R.J., Martin, L., 1984. Aspects of the life-history and fishery of the white croaker, Genyonemus lineatus (Sciaenidae), off California. Fish. Bull. 82, 179–198. Matsui, T., Kato, S., Smith, S.E., 1990. Biology and potential use of Pacific grenadier Coyphaenoides acrolepis, off California. Mar. Fish. Rev. 52, 1–17. Montoya, J.M., Woodward, G., Emmerson, M.C., Sole, R.V., 2009. Press perturbations and indirect effects in real food webs. Ecology 90, 2426–2433. Morse, W.W., 1980. Maturity, spawning, and fecundity of Atlantic croaker, Micropogonias undulatus, occurring North of Cape-Hatteras, North-Carolina. Fish. Bull. 78, 190–195. Office of National Marine Sanctuaries, 2009. Monterey Bay National Marine Sanctuary Condition Report 2009. NOAA U.S. Department of Commerce, Office of National Marine Sanctuaries, Silver Spring, MD, p. 58.
K.N. Marshall et al. / Ecological Modelling 289 (2014) 96–105 Office of National Marine Sanctuaries, 2010. Gulf of the Farallones National Marine Sanctuary Condition Report 2010. NOAA U.S. Department of Commerce, Office of National Marine Sanctuaries, Silver Spring, MD, p. 58. Pacific Fisheries Information Network (PacFIN), 2011. Report # 307. Pacific States Marine Fisheries Commission, Portland, Oregon. Pacific Fishery Management Council, 1978. Fishery Managment Plan for Northern Anchovy. Pacific Fishery Management Council, 2006. Fishery Management Plan for Coastal Pelagic Species. Pacific Fishery Management Council, 2008. Management of krill as an essential component of the California Current ecosystem. Amendment 12 to the Coastal Pelagic Fishery Managment Plan. Pichegru, L., Gremillet, D., Crawford, R.J.M., Ryan, P.G., 2010. Marine no-take zone rapidly benefits endangered penguin. Biol. Lett. 6, 498–501. Rodriguez, J.P., Beard, T.D., Bennett, E.M., Cumming, G.S., Cork, S.J., Agard, J., Dobson, A.P., Peterson, G.D., 2006. Trade-offs across space, time, and ecosystem services. Ecol. Soc. 11, 28. Scheffer, M., Carpenter, S., Foley, J.A., Folke, C., Walker, B., 2001. Catastrophic shifts in ecosystems. Nature 413, 591–596.
105
Smith, A.D.M., Brown, C.J., Bulman, C.M., Fulton, E.A., Johnson, P., Kaplan, I.C., Lozano-Montes, H., Mackinson, S., Marzloff, M., Shannon, L.J., 2011. Impacts of fishing low-trophic level species on marine ecosystems. Science 333, 1147–1150. Sweeney, J.M., Harvey, J.T., 2011. Diet estimation in California sea lions, Zalophus californianus. Mar. Mamm. Sci. 27, E279–E301. Thayer, J.A., Sydeman, W.J., 2007. Spatio-temporal variability in prey harvest and reproductive ecology of a piscivorous seabird, Cerorhinca monocerata, in an upwelling system. Mar. Ecol. Prog. Ser. 329, 253–265. Walker, B.H., 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6, 18–23. Warren, P.H., 1989. Spatial and temporal variation in the structure of a fresh-water food web. Oikos 55, 299–311. White, M.L., Chittenden, M.E., 1977. Age-determination, reproduction, and population-dynamics of Atlantic croaker, Micropogonias undulatus. Fish. Bull. 75, 109–123. Yodzis, P., 1988. The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69, 508–515.