© 2004 International Council for the Exploration of the Sea
Balancing exploitation and conservation of the eastern Scotian Shelf ecosystem: application of a 4D ecosystem exploitation index
a Fisheries and Oceans Canada, Science Branch PO Box 1006, Dartmouth, Nova Scotia, Canada B2Y 4A2
b Food and Agriculture Organization, Sub-regional Office for the Caribbean PO Box 631-C, Bridgetown, Barbados
*Correspondence to A. Bundy: tel: +1 902 426 8353; fax: +1 902 426 1506. e-mail: bundya{at}mar.dfo-mpo.gc.ca.
Few indicators exist that measure the effects of fishing at the whole-ecosystem level. A 4D ecosystem exploitation index is proposed that integrates four measures of ecosystem status: (i) the trophic balance of exploitation, (ii) the intensity of exploitation, (iii) species richness, and (iv) disturbance of the trophic structure. The central concept is that fisheries should extract yield in proportion to the productivity at each trophic level, at sustainable exploitation rates, with minimal disturbance to the trophic structure, and with no loss in species richness. The ecosystem exploitation index is tested on simulated ecosystem data and applied to data from the eastern Scotian Shelf, Canada. The model simulations provided consistent results that should facilitate cross-system comparisons of exploitation and ecosystem status. When applied to actual observations, the results were less coherent, likely attributable to lag effects and environmental impacts. All fisheries likely alter the trophic structure of ecosystems, and the rate and trophic pattern of exploitation determines the level of change. Exploiting all trophic levels equally would always result in less change to trophic structure than top-heavy exploitation. Further testing is required to determine lag effects and sensitivity to various assumptions.
Keywords: disturbance index, ecosystem exploitation index, ecosystem indicator, species richness, trophic balance index, trophic level
Received 1 April 2004; accepted 29 November 2004.
| Introduction |
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In the light of stock collapses and overfishing both in Canada and globally, attention has turned to measuring the effects of fishing on ecosystems (Jennings and Kaiser, 1998; Hall, 1999; ICES, 2000) and ecosystem-based fisheries management (EBFM; Link, 2002; Browman and Stergiou, 2004; Hall and Mainprize, 2004; Pikitch et al., 2004; O'Boyle et al., 2005). The objectives are to set goals for managing human activities in marine ecosystems, and to develop indicators that track progress towards those goals. The concepts are not new. The United Nations Conference on Environment and Development through Chapter 17 of Agenda 21 (UN, 1994) and the Convention on Biological Diversity (CBD), and subsequently the Code of Conduct for Responsible Fisheries (FAO, 1995), recognize explicitly "long-term sustainable use of fisheries resources" as the overriding objective of conservation and management.
Nations that are signatory to the CBD, including Canada, agreed to make plans to conserve biodiversity within their national jurisdictions. The challenge facing those nations is to operationalize the intersection of these sets of exploitation and conservation objectives. Specifically, how do they achieve long-term sustainable use of marine living resources while complying with the agreements under the CBD?
In Canada, the 1997 Oceans Act requires the Department of Fisheries and Oceans to consider the effects of all human activities on the ocean ecosystem. Although this has been law for several years, the means to make this policy operational has lagged its stated aims. More recently, workshops have been held to further progress (O'Boyle, 2000; Jamieson and O'Boyle, 2001), but a set of potential indicators has not yet been fully developed or tested.
The eastern Scotian Shelf has been designated for integrated management, i.e. the coordinated management of all human activities occurring in the area. Until the early 1990s, the area supported a substantial groundfish fishery (Atlantic cod Gadus morhua, silver hake Merluccius bilinearis, haddock Melanogrammus aeglifinus, American plaice Hipploglossoides platessoides), the bulk of which was caught by large trawlers. By 1993, the groundfish resource base, and in particular cod, had collapsed and the fishery was placed under a moratorium. By 2004, cod had not recovered and the fishery had not re-opened. Fisheries for invertebrates such as shrimp, crabs, and bivalve molluscs developed throughout the 1990s as harvesters switched to other species.
Traditional diversity indices have been estimated for the eastern Scotian Shelf (Bianchi et al., 2000), but they have not been effective at facilitating management of human activities. Such indicators reflect little of the underlying dynamics despite considerable changes in species composition and size structure of the ecosystem over the past 30 years (Bianchi et al., 2000; Zwanenburg, 2000).
Recent papers such as that of Pikitch et al. (2004) call for community-level standards, reference points, and control rules for EBFM, but few indicators of entire ecosystems have been developed. Other approaches include the FiB index (Pauly et al., 2000), the use of several indicators (Fréon et al., 2005), and an aggregate approach using many indicators (Pitcher and Preikshot, 2001; Link et al., 2002; DFO, 2003). We propose a different approach to measuring the effects of fishing on the ecosystem, which calls for a new way to look at how, and at what level of effort, fisheries exploit ecosystems.
The typical pattern in developing fisheries is first to exploit top predators, and hence the top of the trophic pyramid, then as catch rates and yields drop, to exploit species at lower trophic levels. Thus, the fishery moves down the foodweb, and the trophic structure of the ecosystem is simplified. However, we posit that maintaining the trophic structure of an ecosystem is an important requirement for sustainable, productive fisheries.
Any kind of fishing will perturb the ecosystem and its trophic structure, but the extent of disturbance depends on the level and pattern of exploitation. Consequently, a realistic fishing strategy is surely one that minimizes this disturbance and best maintains trophic structure by exploiting all exploitable species at all trophic levels (TL) at some reasonable and equal proportion of production (Figure 1). A yield in balance with production will take the same proportion of production at each TL, so keeping their relative proportions as they were before the fishery started. We used TL to structure the ecosystem, but the same theory would apply to a length-based approach.
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A series of test simulations indicated that the only fishing strategy resulting in lesser disturbance of the trophic structure (defined as absolute change in distribution of biomass among TLs) than equal exploitation across all TLs, was to focus exploitation on the lowest and most productive TL. However, because exploitation of higher TLs is generally more profitable from an economic perspective, this would seem an unrealistic approach to exploitation.
Based on the idea that equal exploitation across TLs is the harvest strategy of least harm, we develop a 4D Ecosystem Exploitation Index (EEI) to measure the pattern of exploitation and the ecosystem effects of fishing. EEI integrates four elements: a trophic balance index, an ecosystem exploitation index, a species richness index, and a disturbance index. These are presented in a conceptual "phase space", which locates the effects of exploitation in relation to the trophic structure and should give direction to management strategies aimed at improving ecosystem state. This phase space should be comparable across ecosystems, so permitting cross-system comparisons of exploitation and ecosystem status.
We test the EEI on an ecosystem model and apply it to data from the eastern Scotian Shelf.
| Methods |
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Trophic balance index
The trophic balance index (TBI) measures the evenness (pattern) of exploitation across TLs by comparing their exploitation rates, which are estimated as the sum of yield (Y) divided by the sum of production (P) at each TL. The evenness of exploitation is then given by the coefficient of variation of all Y/P:
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| (1) |
TBI does not differentiate between patterns related to how exploitation rate is distributed among individual TLs, nor does it capture the overall level of exploitation. Other measures, including Shannon's measure of evenness and McIntosh's index of diversity (Magurran, 1988) were explored, but because the results obtained were qualitatively the same, we use the simpler coefficient of variation.
Yield is compared with production rather than with biomass, because production reflects the yield that can sustainably be removed from the ecosystem: a low biomass does not imply a low yield, because yield depends on the productivity of a species. Production is defined here as the annual biomass of a species that is generated through growth and reproduction. Production might be modelled as surplus production.
The production term in the TBI is restricted to "potentially exploitable" species only and excludes groups such as phytoplankton or zooplankton, because otherwise exploitation could never be in balance with the ecosystem. Although the term potentially exploitable is subjective, species that are not currently exploited but may be so in the future should be included.
Exploitation index
The exploitation index (E) estimates the level of exploitation, integrated over all TLs, as the total yield divided by total production for all exploited species (k):
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Species richness index
A species richness index (SRI) was calculated as the number of species in any year whose numerical abundance or biomass was larger than some percentage of their value in a reference year. Ideally, pristine biomasses would be used as reference values, but these are rarely available. SRI is aimed at linking function to structure. The threshold chosen should reflect the value at which the functional role of a component ceases to be important, so effectively changing the structure of the ecosystem. The extent of structural change depends on the ecological role of the component (e.g. whether it is a key prey or predator). The IUCN Red List criteria would suggest using a 10% or 20% criterion for SRI, depending on whether or not the change is reversible. Because it remains uncertain whether changes observed in marine ecosystems are reversible (Scheffer et al., 2001), we used the 20% criterion to be more cautious.
Disturbance index
The disturbance index (DI) measures the change in trophic structure of the ecosystem and was calculated as the sum, across all TLs
2, of the absolute difference in the relative biomass (BTL/BTotal) within each TL at the beginning (ref) and end of a period (y):
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Ecosystem exploitation index
The four indices are relatively simple to measure, and as far as possible, do not require complex modelling frameworks. Three of them (TBI, E, and DI) are based on TL, and the same trophic bin size should be used for each. The EEI phase space is given by plots of DI against E and TBI, whereas points are labelled with the number of species that fall below the 20% SRI criterion. The central idea is that as TBI departs from zero, the ecosystem should be exploited more conservatively, to minimize fishing impacts. If exploitation is out of trophic balance with the ecosystem and/or exploitation is high, fishing could both deplete the resource and change ecosystem structure. If exploitation affects TL equally (is in balance with the ecosystem), exploitation may be higher, because ecosystem structure will change less. Clearly, there should be an upper limit to sustainable exploitation.
Exploration and application
The phase space of EEI was explored using an Ecopath model for the Gulf of Thailand (FAO/FISHCODE, 2001). The model consisted of 40 groups spanning four TLs (Table 1). The model was adapted to have no fishing, and no biomass accumulation terms, at the beginning of the simulation. All TLs
2 were included in the calculation of the four indices, and species were grouped into 0.5 trophic bins (totalling five bins).
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A series of 50-year simulations was conducted to compare the effects of equal and unequal exploitation. The scenarios investigated were: (i) unequal exploitation concentrated on upper TL (top heavy), (ii) unequal exploitation concentrated on lower TL (bottom heavy), and (iii) equal exploitation across all TLs (Table 2). TBI estimates for bottom-heavy scenarios were multiplied by 1 for distinction from top-heavy and equal estimates. The first year of the simulation was used as the reference year for SRI and DI.
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The method was applied to explore whether exploitation of the eastern Scotian Shelf has been in balance with the ecosystem, compared with the situation in the early 1980s. The average for 19801985 was used as a reference, because yield was high during that period and the ecosystem was considered still to have been in a fairly good state.
Landings data were taken from official statistics, and biomass estimates were derived from trawl surveys of the eastern Scotian Shelf (19702002), with some adjustment for differences in catchability among species (Harley et al., 2001; Bundy, 2004). Years prior to the reference period were included for comparative purposes. Information on P/B ratios and TLs of all species groups was taken from an Ecopath model of the area (Bundy, 2004). Some species were grouped into assemblages; of the 39 groups distinguished, 30 (spanning four TLs) were considered potentially exploitable (Table 3).
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| Results |
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Under any of the exploitation scenarios explored, the trophic structure of the Gulf of Thailand ecosystem was altered (i.e. DI always >0). DI increased with exploitation (Figure 2), but the rate of increase varied with the pattern of exploitation. TBI increased with increasing unevenness in exploitation pattern, values ranging between ±0.6 over the simulations explored (Table 2). The maximum value that TBI can reach for five TLs is 2.24, and this value is observed when exploitation is highly concentrated on one TL (not shown). E ranged between 4% and 40% of annual production (Figure 2), bottom-heavy scenarios resulting in higher E than top-heavy ones, because the index is weighted by the greater production in the lower TL. However, the impact of bottom-heavy scenarios on the ecosystem for any given E is lower than the impact of the top-heavy or equal exploitation scenarios, as measured by DI and SRI.
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Equal exploitation (TBI = 0) always resulted in a lower DI than top-heavy scenarios for a given E, whereas for TBI = 0, species start falling below the critical SRI threshold at higher E (>0.28 y1) than for top-heavy scenarios (
0.13 y1). Although these simulations are not exhaustive, they do indicate that top-heavy exploitation leads to greater disturbance of the ecosystem than equal exploitation. As TBI and E increase, disturbance increases, and species reach critical SRI levels more frequently. Moving to the eastern Scotian Shelf, TBI fluctuated annually over the first 20 years, with perhaps a minor decrease during the 1970s (Figure 3a). After 1990, it declined sharply to a lower value in 1996 and remained around 0.6 thereafter. Apparently, the fishery has never been exploited equally across all TLs. E was high during the 1970s, when large foreign fishing fleets exploited the area (Figure 3b), but with the declaration of Canada's EEZ, E dropped to an average of 0.2 y1 from 1977 to 1992. Once the cod fishery collapsed in 1993, E stayed extremely low (around 0.05 y1), the low value reflecting the high production and low exploitation of the mid-TL range, which encompasses forage species such as herring. SRI stayed relatively constant until the early 1990s (Figure 3c). Deviations throughout the time-series are due to poorly sampled species such as sandlance (Ammodytes dubius) and mackerel (Scomber scombrus), whereas the increase in 1985 was caused by an influx of capelin (Mallotus villosus) to the Scotian Shelf (Frank et al., 1996). There was no real decrease in SRI until the early 1990s, when cod and (in some years) skate biomass fell below their critical values (10 years). DI was always subject to relatively large annual variation, but it initially decreased until the early 1980s, and then gradually increased until recently (Figure 3d).
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When these four indices are plotted into a 4D phase space (FIgure 4), there is no clear response of increasing DI with increasing TBI and E, as seen for the Gulf of Thailand model. Rather, in contrast to the reference period (19801985), most years have high values of DI, regardless of TBI or E. Since the early 1990s, the ecosystem has shown most change in terms of SRI.
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| Discussion |
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The 4D ecosystem exploitation index (EEI) is based on measures related to both sustainability and biodiversity, encompassing concepts such as ecosystem structure, function, and species richness. In principle, it should allow comparison across systems, and ultimately may permit determination of sustainable levels and patterns of exploitation. We hypothesize that a fishery that exploits the marine ecosystem at a moderate level, in proportion to the production of each exploitable species within all trophic levels, would be sustainable without substantially changing relative trophic structure and without loss of biodiversity. The simulations indicate that exploitation always, and regardless of its trophic pattern, disturbs the ecosystem, but that the extent of disturbance depends both on its rate and on its distribution across trophic levels. Equal exploitation always results in lesser disturbance than top-heavy exploitation. Although concentrating on lower trophic levels should reduce disturbance compared with equal exploitation, this may not be economically viable as a strategy.
Although the phase space of EEI may be a useful tool for assessing exploitation status and developing sustainable management plans with regard to both ecosystem structure and biodiversity, further testing is required to determine whether a generic phase space can be described. A surface fitted to the simulated indices would be asymmetrical, increasing steeply as TBI becomes more positive (top-heavy exploitation) and more gradually as TBI becomes more negative (bottom-heavy exploitation), with an upward curving trough where TBI = 0. Establishing such ecosystem reference levels is a key challenge for EBFM (Hall and Mainprize, 2004). With more comprehensive modelling and further exploration of other models and ecosystems, it may be possible to develop reference exploitation patterns for sustainable and non-sustainable zones, and to elucidate patterns of ecosystem response.
In examining the behaviour of four indices for the eastern Scotian Shelf data, the results do not seem to support the results of the simulations. Although TBI decreased during the 1990s and E was relatively low, DI was high and SRI decreased. The explanation for this discrepancy may lie in the historical development of the fishery. Until the mid-1990s, exploitation was top heavy, focusing on TLs 3.54.5 (Figure 5), and especially 3.53.9, which includes the gadoids. Exploitation of the lowest TL increased in the 1980s, rapidly increased during the 1990s, and now exceeds exploitation on any of the others, an example of fishing down the foodweb (Bundy, 2004). Currently, after a stock collapse and other severe stock declines, the exploitation pattern is more equal, but DI is high and the biomass of several species has decreased below the threshold. The difference between the observed and simulated EEI surfaces may be largely due to lag effects of high top-heavy exploitation rates persisting from earlier years. Therefore, although TBI has decreased, there has been no concurrent decrease in DI.
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Our current estimates of eastern Scotian Shelf E are weighted downwards by the high production of lower TLs. However, this masks greater exploitation rates on the targeted groups (Figure 5). An integrated ecosystem exploitation rate necessarily averages across trophic levels (or species) and alternative indices might include differential weighting across TLs.
Several aspects of the EEI requiring further investigation have been identified: lag effects (see above), sensitivity to criteria for potentially exploitable species, choice of trophic bin size, and production estimates. The definition of potentially exploitable species affects both the TBI (Figure 6) and E. Initial studies indicate little sensitivity to trophic bin size used, whereas TBI appears to be sensitive to production estimates when these are varied randomly by ±50% of the estimated value, although clear trends can be identified.
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Species interactions and environmental effects also influence the EEI. There is much debate about the relative strength of species interactions and their impact on ecosystem structure and function (e.g. top-down vs. bottom-up control; Hunter and Price, 1992; Matson and Hunter, 1992). Because natural mortalities and types of control within ecosystems are not well known, a conservative approach to managing human activities would be to keep the exploitation rate of trophic production constant at a low value, as proposed here. This is akin to a constant harvest rate (Walters and Parma, 1996). However, we need particularly to determine the strength of linkages between target species of the fisheries, key species groups, and overall ecosystem productivity. Strong linkages between species may exacerbate exploitation impacts, whereas effects of environmental dynamics may be less predictable, although environmental variation can alter the productivity of species and the impact on the EEI phase space needs to be explored.
Both DI and SRI require reference points, which relates to the question of how the characteristics of the "desirable ecosystem" can be defined. Although projects are underway to explore how earlier ecosystems may have looked (Jackson et al., 2001; Pitcher, 2001), this question has no general answer. For the eastern Scotian Shelf, we used the period 19801985 as a reference, but the ultimate choice will clearly affect management plans. Even if our understanding of regime shifts and their causes remains rudimentary, a discussion of appropriate reference points should be guided by the possibility that ecosystem changes may not be reversible (Scheffer et al., 2001), and that the "desirable" configuration might not be recovered. Moreover, lucrative fisheries currently exist on the Scotian Shelf for crab, shrimp, and lobster, while the major groundfish stocks are at all-time lows. Deciding whether the crustacean-rich state is "worse" than the original gadoid-rich state involves a value judgement that cannot be resolved by science. Exploitation rate, as measured here, is currently relatively low on most TLs and more evenly distributed than in the past. In the absence of clear management direction for restoration, it might be advisable to keep the situation as it is and try to minimize further disturbance. Nevertheless, simulation studies might be used to explore remedial exploitation strategies.
EBFM is believed to require the development of a range of indicators. The 4D EEI has been developed to measure whole-ecosystem effects of fishing. Developing this type of indicator is challenging and necessarily involves considerable data reduction and aggregation. However, we contend that studies such as the present one must be done to gain a wider understanding of the ecosystem effects of fishing. Moreover, we kept EEI as simple as possible, in keeping with recent indications (Fulton et al., 2005) that simple indices perform better than complex ones.
| Acknowledgements |
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We thank Bob Mohn, Bob O'Boyle, and two anonymous referees for providing detailed and insightful comments, which led to a much improved manuscript. We also thank the editor for his patience during the revision process.
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