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Trophic flows in the southern Benguela during the 1980s and 1990s
Journal of Marine Systems 39 (2003) 83 – 116 www.elsevier.com/locate/jmarsys
Trophic flows in the southern Benguela during the 1980s and 1990s Lynne J. Shannon a,b,*, Coleen L. Moloney a,b, Astrid Jarre c, John G. Field b a Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa Department of Zoology, University of Cape Town, Private Bag, Rondebosch 7701, South Africa c Danish Institute for Fisheries Research, and Greenland Institute for National Resources, P.O. Box 570, DK-3900 Nuuk, Greenland b
Received 23 January 2002; accepted 23 September 2002
Abstract Mass-balanced models of trophic flows in the southern Benguela ecosystem suggest a 10% increase in zooplankton biomass between the 1980s and the 1990s, in agreement with observed trends of increased zooplankton abundance off South Africa over the last few decades. Minimum hake biomass in balanced trophic models is substantially larger than survey and other model estimates, suggesting undersampling of hakes in surveys and underestimation of juvenile hake mortality. Model biomass and mean annual production of five important small pelagic fish groups were larger in the 1990s, and total catches were smaller than in the 1980s. Estimates of biomass per trophic level, transfer efficiencies, mixed trophic impacts and many other ecosystem attributes suggest that trophic functioning of the southern Benguela ecosystem was similar in the 1980s and 1990s. Because catches were lower and model zooplankton and small pelagic fish biomasses were larger in the 1990s, the ecosystem was less tightly constrained by predators (including fishers) and food availability than in the 1980s. Fishing took place at low trophic levels compared to other systems. Despite smaller total catches in the 1990s, fishing was ecologically more expensive (from higher trophic levels) during the 1990s than in the 1980s because snoek and hake catches were large. There was greater shared niche overlap of small pelagic fish predators in the 1990s than in the 1980s. Mean transfer efficiency was 12%. Transfer of biomass at trophic levels III – V appears to be more efficient in the southern Benguela than in other upwelling ecosystems. Primary production required to sustain catches in the southern Benguela ecosystem is 4% of total primary production, i.e. more similar to estimates for open ocean and coastal regions than for other upwelling or shelf systems averaging more than double this value. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Ecosystem models; Southern Benguela; Upwelling system; Ecopath
1. Introduction One of the traditional approaches to studying ecosystems has been to concentrate on functional
* Corresponding author. Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa. Tel.: +27-21402-3171; fax: +27-21-421-7406. E-mail address: [email protected] (L.J. Shannon).
aspects, such as energy or material flows and nutrient cycling, as opposed to interactions among populations or individuals of different species (O’Neill et al., 1986). This approach, of necessity, usually involves aggregating species into functional groups, sometimes separating different life history stages of the same species. The basis of the approach is the trophic level concept (Lindeman, 1942), and although the approach has been refined and adapted over time, it still fundamentally concerns who eats whom in a food
0924-7963/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. doi:10.1016/S0924-7963(02)00250-6
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and South Africa) southwards along the west coast and eastwards to 28jE (East London) (Fig. 1). The area covers 220 000 km2 and incorporates the west coast, the Agulhas Bank and the south coast (Fig. 1). The marine environment in the area is dominated by seasonal, pulsed, wind-driven coastal upwelling (Shannon, 1985). The resultant nutrient-enriched shelf waters have large biological productivity, and support the most important commercial fisheries of South Africa, including those for pelagic species (primarily sardine Sardinops sagax and anchovy Engraulis capensis) and hakes (Merluccius capensis and M. paradoxus). It is well known that the southern Benguela ecosystem varies at a number of scales, and that decadal changes, which manifest as changes in the relative abundance of sardine and anchovy populations, are an important feature of its dynamics (Schwartzlose et al., 1999). Off South Africa, large catches of sardine were made in the 1950s and 1960s, before the fishery collapsed. Fishing effort was switched to anchovy, which became the mainstay of the purse-seine fishery off South Africa. However, by the 1990s, abundance of anchovy was fluctuating and declining, whereas sardine biomass was increasing (Fig. 2). Both species have attained large stock sizes in the 2000s (unpublished data, Marine and Coastal Management).
Fig. 1. The Benguela upwelling ecosystem, (1) Northern Benguela Upwelling System, (2) Southern Benguela Upwelling System.
web. A large amount of information is often required to formulate the trophic interactions in a food web, and the development of trophic models is complicated by the fact that these interactions change over time and space. This variability has been taken into account in trophic models of the southern Benguela ecosystem, where a long-term ecosystem study (Moloney et al., in preparation) has provided sufficient information to develop and refine models that apply to different periods. The southern Benguela ecosystem is here assumed to cover the shelf region to approximately 500 m depth, extending from 29jS (in the vicinity of the Orange River mouth, the boundary between Namibia
Fig. 2. Estimates of spawner biomass of anchovy and sardine off South Africa (Hampton, 1992, 1996; Barange et al., 1999; Schwartzlose et al., 1999).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
To date, a number of studies have summarized the flows of carbon through the southern Benguela ecosystem, focusing attention on various aspects, namely the pelagic component (Shannon and Field, 1985; Bergh et al., 1985; Moloney and Field, 1985), the planktonic foodweb (Moloney, 1992) and comparison of ecosystem properties with other similar ecosystems (Baird et al., 1991). These above models produced average descriptions of the relevant food webs, but some are incomplete (because of limited data at the time of their development), and none could be used to assess decadal variability. In 1989, a coordinated effort was made to refine available estimates of carbon standing stocks and flows in the southern Benguela food web. At a local workshop of experts on the different species groups, both published and unpublished data were brought together to construct simple input – output carbon budgets for the southern Benguela. These data, together with those that have since become available, were used to construct the first Ecopath model of the southern Benguela ecosystem for the 1980s period (Jarre-Teichmann et al., 1998). Ecopath (Christensen and Pauly, 1992) is a software tool that facilitates the construction of mass-balance, trophic models of aquatic ecosystems, and allows analysis of different aspects of the resulting food web network. Species or groups of species are modelled as individual boxes for which input data is required, including estimates of biomass, production, consumption, diet data and harvests. For each box, production balances consumption, respiration and unassimilated food, so that input balances output for a steady-state over a given period. Interactions between boxes are described by sets of simultaneous linear equations. Subsequently, the 1980s model of Jarre-Teichmann et al. (1998) was modified by incorporating updated data and by separating some model components to avoid problems arising from intra-group cannibalism and major within-group differences in feeding modes. In addition, a second model was constructed of trophic flows through the southern Benguela ecosystem for the 1990s period (Shannon, 2001). The 1980s and the 1990s are known to have differed in terms of the relative abundance of the main pelagic species. What is not known is whether the observed changes in abundance of pelagic fish (Barange et al., 1999) can be linked to more subtle
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structural and functional changes in the rest of the food web. In this paper, we aim to present outputs of the two mass-balance models that describe the food webs and fishing pressures in the southern Benguela ecosystem during the decades of the 1980s and 1990s. We use these models to identify data gaps and imbalances that result from inconsistencies between various stock assessments. We compare these model results where possible, recognizing that there are uncertainties about data from which model inputs are estimated. We use the models to assess how observed differences or similarities in abundance, catches and dietary composition could affect overall trophic functioning, focusing on the pelagic part of the southern Benguela ecosystem. This work also serves as a basis for future comparisons of the results of possible consequences of fisheries management scenarios derived from static networks of trophic flows to dynamic simulations of fishing impacts (e.g. Shannon and Moloney, in preparation).
2. Methods 2.1. Model construction and balancing Mass-balanced models of the trophic flows through the southern Benguela ecosystem for the 1980s and 1990– 1997 have been constructed using the Ecopath software (Christensen and Pauly, 1992), version 3.1 (final version, February 1998). Primary production required to sustain the fishery was calculated using an alpha version of Ecopath with Ecosim version 4 (1999 – 2000). Detailed descriptions of the models and their data sources are given by Jarre-Teichmann et al. (1998) and Shannon (2001) but data sources and parameter estimates are summarised in Appendix A and the final balanced versions of the models are presented in Tables 1 and 2. The final models have 31 groups, which include all the major components of the pelagic ecosystem. The initial models, constructed from input data collated from published and unpublished sources, were unbalanced; the estimated production of many of the model groups was insufficient to support the estimated consumption by other groups and, in some cases, the catches. Because estimates of diet composition were uncertain, especially those for
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Table 1 Trophic levels, biomass (t km 2), catches (t km 2 year 1) and ecotrophic efficiencies (EEs, expressed as percentages of production either passed up the food web or exported) of all boxes in balanced southern Benguela ecosystem models during two decades Group
Phytoplankton Microzooplankton Mesozooplankton Macrozooplankton Gelatinous zooplankton Anchovy Sardine Redeye Other small pelagic fish Chub mackerel Juvenile horse mackerel Adult horse mackerel Mesopelagic fish Snoek Other large pelagic fish Cephalopods Small M. capensis Large M. capensis Small M. paradoxus Large M. paradoxus Pelagic-feeding demersal fish Benthic-feeding demersal fish Pelagic-feeding chondrichthyans Benthic-feeding chondrichthyans Apex predatory chondrichthyans Seals Cetaceans Seabirds Benthic producers Meiobenthos Macrobenthos
1980s
1990s
Trophic level
Biomass
Catch
EE
Trophic level
Biomass
Catch
EE
1.0 2.3 2.6 2.7 3.3 3.5 3.0 3.6 3.7 3.8 3.6 3.7 3.6 4.5 4.5 3.8 4.0 4.7 3.9 4.5 4.0 3.4 4.9 3.7 5.2 4.7 4.6 4.5 1.0 2.0 2.2
76.938 7.473 8.031 13.301 4.545 5.216 0.586 5.555 0.364 0.284 0.2 1.618 8.642 0.240 0.131 1.364 0.592 0.823 1.698 0.684 3.445 3.511 0.582 0.873 0.045 0.133 0.074 0.015 6.339 11.812 56.109
0.000 0.000 0.000 0.000 0.000 1.572 0.180 0.180 0.001 0.032 0.022 0.144 0.031 0.051 0.027 0.027 0.024 0.230 0.116 0.265 0.022 0.093 0.002 0.012 0.000 0.005 0.000 0.000 0.000 0.000 0.000
0.583 0.950 0.950 0.950 0.155 0.997 0.994 0.961 0.907 0.768 0.936 0.806 0.990 0.997 0.916 0.892 0.999 0.984 0.999 0.974 0.990 0.990 0.993 0.725 0.000 0.454 0.760 0.962 0.500 0.950 0.950
1.0 2.3 2.6 2.7 3.3 3.5 3.0 3.6 3.7 3.9 3.6 3.7 3.6 4.5 4.5 3.8 3.9 4.6 3.9 4.5 4.0 3.4 4.9 3.7 5.2 4.7 4.5 4.4 1.0 2.0 2.2
76.938 8.195 8.737 14.562 5.000 3.573 2.091 6.226 0.364 0.455 0.484 1.937 10.242 0.337 0.131 1.364 0.638 1.127 1.878 1.067 3.693 3.719 0.582 0.873 0.045 0.133 0.082 0.012 6.548 12.201 57.957
0.000 0.000 0.000 0.000 0.000 0.812 0.340 0.234 0.001 0.033 0.033 0.107 0.003 0.084 0.026 0.028 0.013 0.256 0.034 0.352 0.058 0.053 0.002 0.012 0.000 0.003 0.000 0.000 0.000 0.000 0.000
0.636 0.950 0.950 0.950 0.152 0.990 0.990 0.990 0.934 0.663 0.663 0.818 0.990 0.990 0.900 0.953 0.999 0.831 0.999 0.791 0.990 0.990 0.993 0.731 0.000 0.427 0.686 0.962 0.500 0.950 0.950
Italicized and bold parameters indicate the biomass required to sustain other components of the system, and were estimated using assumed EEs.
the 1990s, the models were mostly balanced by adjusting the diets of some groups (Table 2). 2.2. Diets There are some fundamental problems with the estimation of dietary compositions in many cases. Often, dietary data are only available for part of the periods or area modelled, biasing the mean dietary estimates. Taxonomic resolution is low in some stomach analyses. These are among the reasons for estimated predation on some components exceeding their pro-
duction. Therefore, it was necessary to alter the contributions of some prey in the diets of certain predators. In particular, the relative dietary contributions of small pelagic fish during the two decades required altering to balance the models. Anchovy in the diet of chub mackerel in the 1990s was reduced from 3% to 2%, and 1% sardine was considered to have been consumed. Consumption of sardine by large pelagic fish during the 1980s was reduced from 15% to 10% and the remaining 5% added to redeye. Redeye contribution to diet of large pelagics was assumed the same in the 1990s, and anchovy was reduced from 25% to 20% so
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
that sardine contributed 15%. The proportion of anchovy in the diet of seals was reduced from 25% to 20%, and the remainder added to the redeye contribution. Insufficient snoek production required that snoek contributed not more than 0.5% of seal diet, and 0.5% was added to other large pelagics and to other demersal fish. 2.3. Zooplankton For the 1990s model, the biomasses of micro-, meso- and macro-zooplankton were estimated as minimums required for the amount of production needed to sustain other groups in the system. This was necessary because there was uncertainty about how to convert abundance (numbers) to biomass (tonnage) for the various zooplankton components of the whole southern Benguela sub-system, and different carbon: wet weight conversion factors had been used in the past (e.g. by Jarre-Teichmann et al., 1998; Verheye et al., 1992). 2.4. Cephalopods Initially, model Cephalopod production was far too small to support consumption of cephalopods by other groups within the Benguela ecosystem. In the balanced version of the models used here, biomass, production/biomass (P/B) and production/consumption (P/Q) ratios were all increased from initial estimates (Table A.5). Cephalopods have been highlighted as a group urgently requiring further research to improve biological parameter estimates used in models such as those described here. 2.5. Ecosystem structures The trophic level concept was initially introduced by Lindeman (1942). Components of food webs can be aggregated into discrete trophic levels (Ulanowicz and Kay, 1991), giving an indication of the average number of steps in food webs and their efficiencies of transferring material and energy. Transfer efficiency (TE) is the fraction of total throughput at a discrete trophic level (TL), either exported or transferred to another TL (through consumption). Aggregation of flows and biomasses into discrete TLs are estimated and the TEs of biomass between TLs are
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computed. Ecopath also computes non-integer TLs (Pauly et al., 2000a). By definition, primary producers and detritus are assigned to TL 1. Consumers are assigned to a TL 1 greater than the average TL of their prey, weighted by the proportion of the prey in the consumer’s diet. Mean path length (Finn, 1976) is estimated from models of each decade, and corresponds to the mean number of trophic links in each trophic pathway. 2.6. Ecosystem flows Estimated total flows modelled include total consumption, total catches, total production and total system throughput (defined as the sum of total export, total respiration and total flows to detritus), the latter representing the overall size of a system in terms of flow. Ascendancy measures a system’s average mutual information and is scaled by system throughput (Ulanowicz, 1986; Ulanowicz and Norden, 1990). It is the product of total system throughput and the diversity of flows in a system, and is a measure representing size of flows as well as the organization of flows in a system (Field et al., 1989a,b). Ascendancy A is calculated as: A¼T
n X n X ðfij =T Þlogðfij T =Ti Tj Þ
ð1Þ
i¼1 j¼1
where T is throughput, f is flow and i and j are compartments or boxes in the ecosystem (Kay et al., 1989). Development capacity C is a measure of the potential of an ecosystem to develop, and is defined by Kay et al. (1989) as: C ¼ T
n X ðTi =T ÞlogðTi =T Þ
ð2Þ
i¼1
Relative ascendancy is defined as A/C, and relative system overhead is defined as (C A)/C (Kay et al., 1989). Fishing and predation mortalities are compared between species and decades. Catches are compared by converting flows in each path (towards the catch of a particular group) to primary production equiv-
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Table 2 Balanced diet composition of groups in the southern Benguela ecosystem during the 1980s and 1990s L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116 Shaded cells indicate dietary contributions altered in the balancing of the model. Where diet differs between decades, the contribution to diet during the 1990s is tabulated below the 1980s contribution. < indicates a dietary proportion of less than 0.5%.
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alents using the product of catch, production/consumption and the proportion of each group in the path in the diets of the other groups (Christensen et al., 2000):
PPR ¼
X Yi
Qpredator j predator;prey P P i predator EEpredator paths DCpredator;prey V
ð3Þ
where Y is catch of a given group i, P is production, Q consumption, EE the ecotrophic efficiency and DC is the diet composition for each predator/prey pair in each path (with cycles removed from the diet compositions).
3. Results 3.1. Biomass and production of fish During the 1980s, anchovy was the dominant small pelagic fish in the southern Benguela ecosystem (Fig. 2). By the 1990s, the size of the anchovy population had decreased and populations of sardine, redeye, horse mackerel and both species of hake had increased in size (Fig. 3 and Table 1). Summed biomasses of small pelagic fish (anchovy, sardine, redeye, juvenile horse mackerel and other small pelagic fish) increased from 2.62 million tons in the 1980s to 2.80 million tons in the 1990s, i.e. by 7%. Mean annual production by these five small pelagic groups was estimated to be 3.1 million tons in the 1980s and 3.3 million tons in the 1990s, half accounted for by anchovy and sardine.
2.7. Species interactions 3.2. Trophic levels and trophic aggregation Relative impacts of each group on all other groups in the system are quantified using mixed trophic impact analysis, and serve to highlight those groups playing important roles in the system, and those having only small effects on other system components. Mixed trophic impact assessment measures the relative impact of a change in the biomass of one component on other components of the ecosystem (Ulanowicz and Puccia, 1990), and is based on an input –output method for assessing direct and indirect economic interactions, initially applied to the economy of the United States of America (Leontief, 1951). The prey niche overlap index of Pianka (1973) is used to determine the degree of overlap between species utilising common prey resources. A value of 1 indicates complete overlap in shared prey resources, whereas 0 indicates that the predators do not share common prey resources. A similar predator overlap index is used to determine the degree of overlap between species being consumed by common predators, with a similar interpretation of the 0 – 1 range of values. Comparing these varied outputs of the models of the 1980s and 1990s facilitates assessment of the trophic functioning of the southern Benguela ecosystem during two decades dominated by different pelagic fish species.
In Table 1, non-integer trophic levels (TLs) of the 31 living boxes in models of the southern
Fig. 3. Average annual stock sizes (millions of tons) of important fish in the southern Benguela ecosystem during the 1980s and 1990s. Stock sizes of anchovy, sardine and horse mackerel in both decades, and of redeye in the 1980s, were estimated from data and were input to the Ecopath models. Stock sizes of mesopelagic fish, hakes and other demersal fish in both decades, and of redeye during the 1990s, were estimated minimum values (*) required to support consumption by all groups within the system, given estimates of EE which were input to the models (Table 1).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116 Table 3 Biomass (t km 2) and transfer efficiency (%) at each discrete trophic level in models of the southern Benguela ecosystem in the 1980s and 1990s Trophic level
I II III IV V VI VII VIII
Biomass
Transfer efficiency
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proportions went to predation (Fig. 4). Microzooplankton, having a high respiration rate, accounted for the large proportion of throughput going to respiration at TL II.
1980s
1990s
1980s
1990s
3.3. Consumption
83.277 83.959 32.237 16.115 4.878 0.680 0.072 0.006
83.486 88.364 35.193 17.813 5.459 0.790 0.081 0.006
6.5 24.3 22.0 11.3 12.1 9.1 8.1
6.5 24.3 22.0 11.2 11.9 9.2 8.3
Relative consumption by the various groups highlights differences between periods (Fig. 5). In the
Benguela ecosystem during the 1980s and 1990s are tabulated. Small pelagic fish occupy TLs between 3.0 and 4.0, whereas top predators such as seals, seabirds, pelagic-feeding chondrichthyans and apex chondrichthyans are at TLs larger than 4.0 (Table 1). TEs between trophic levels and biomass at each trophic level are almost identical in both decades (Table 3). Small proportions of the throughput at TL II, V, VI, VII and VIII were consumed by predators, whereas at intermediate trophic levels III and IV, larger
Fig. 4. The fate of throughput at each discrete trophic level in the model of the southern Benguela ecosystem in the 1990s, expressed as the percentage of throughput used for respiration, flow to detritus and consumption by predators.
Fig. 5. Relative consumption by fish and top predators estimated by the mass-balanced model of the southern Benguela ecosystem in the 1980s and 1990s.
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fish production. Hake were the dominant consumers of small pelagic fish production, followed by other demersal fish (Fig. 6). Adult horse mackerel, large pelagic fish (including snoek), cephalopods, marine mammals and seabirds all consumed similar proportions of small pelagic fish production (between 8% and 13%). 3.4. Summary statistics and flows Total biomass and many total flows through the southern Benguela upwelling ecosystem were larger in the 1990s model than the 1980s model (Table 4). Average annual catches of small pelagic fish were reduced by 27% and total annual catches were reduced by 18% from the 1980s to the 1990s. Lower net system production (production minus respiration) in the 1990s than in the 1980s (Table 4) is due in part to the 10% increase in biomass of microzooplankton, which have high respiration rates. The southern Benguela ecosystem was less heavily exploited in the 1990s than the 1980s (Table 4)
Table 4 Comparison of summary statistics from models of the southern Benguela ecosystem for the 1980s and 1990s, including % change from 1980s to 1990s 1980s
Fig. 6. Relative consumption of small pelagic fish production by predators, estimated by the mass-balanced model of the southern Benguela ecosystem in the 1980s and 1990s.
1980s, anchovy, redeye and mesopelagic fish consumed the greatest proportions of production. Relative consumption by anchovy decreased in the 1990s, and that by redeye, horse mackerel, mesopelagic fish and sardine increased. Consumption by marine mammals and birds was small in both decades. In models of the 1980s and 1990s, respectively, predators consumed 84% and 88% of small pelagic
1990s
% Change
Total biomass 221 231 +5 (excluding detritus) Sum of all consumption 17 230 18 831 +9 Sum of all exports 2559 1698 34 Sum of all flows to detritus 8771 8496 3 Total system throughput 37 975 39 304 +3 Sum of all production 16 233 16 638 +3 Net system production 2559 1698 34 Sum of all respiratory flows 9416 10 279 +9 Total net primary production 11 974 11 977 <1 Total catches 3.04 2.48 18 Mean trophic level of 4.74 4.80 +1 the fishery Mean path length 3.17 3.28 +3 (Finn, 1976) System overhead 104 304 108 820 +4 Relative ascendancy 21 20 <1 Flows are in t km 2 year 1, biomass and catches in t km 2, system overhead in flowbits (bits t km 2 year 1) and relative ascendancy as %.
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southern Benguela ecosystem during both decades are those of anchovy, large hakes and snoek (Fig. 7). PPR for all fisheries is 4.4% of the total primary production in the 1980s and 4.5% in the 1990s. Catches in the southern Benguela ecosystem were mainly taken from TL III and IV (Fig. 8), corresponding to large transfer efficiencies at these trophic levels (Table 3, TE is the fraction of production either exported from the system, e.g. as catches, or transferred to higher TLs by means of predation). The ratio of PPR by the fisheries to total annual harvest is 290 in the 1990s model, compared to 228 in the 1980s model. This is despite 18% smaller Fig. 7. Modelled primary production required (t km 2 year 1) to sustain catches of commercially important species in the southern Benguela ecosystem during the 1980s and 1990s. Species requiring less than 15 t km 2 year 1 during both decades are omitted.
(a)
although system throughput and biomass were larger in the 1990s model. 3.5. Primary production required to sustain catches The greatest amounts of total primary production required (PPR) to support catches in models of the
Fig. 8. Proportion of catches taken from discrete trophic levels in models of the southern Benguela ecosystem during the 1980s and 1990s.
(b)
Fig. 9. Relative mortality by predation, fishing and other causes in the southern Benguela ecosystem, (a) 1980s and (b) 1990s, calculated using Ecopath.
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Fig. 10. Mixed trophic impacts of selected groups in the southern Benguela ecosystem during the (A) 1980s and (B) 1990s (outputs of Ecopath models). The bars indicate relative net impact (scaled between 0 and 1), where positive impacts are shown above the zero line for each impacting group, and negative impacts below. Impacted groups are arranged along the horizontal axis and impacting groups down the vertical axis.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Fig. 10 (continued).
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In the southern Benguela ecosystem, anchovy, sardine, redeye, other small pelagic fish and juvenile horse mackerel showed large degrees of overlap in both the prey they consumed and in the predators
0.14 0.09 0.26 0.32 0.82 0.85 0.42 0.17 0.45 0.50 0.79 0.79 0.70 0.70 0.92 0.92 0.39
1.00 0.99 0.99 0.96 0.96 0.51 0.96
0.90
0.96
0.90
0.51
1.00 1.00 1.00 0.91 1.00 0.91 1.00 0.50 0.50 1.00 0.50 0.50
0.39
1.00 0.36 0.15 0.13 0.60 0.27 0.48 1.00
0.42
1.00 1.00 1.00 0.21 1.00 0.14 1.00 0.52 0.73 1.00 0.33 0.65
80s 90s 80s 90s 80s 90s 90s
0.66
1.00
90s 80s 90s 80s 90s 80s 90s 80s 90s 90s
80s
1.00 0.90 0.57 0.63
80s 80s
Other small pelagics Redeye
1.00 0.67 0.55 0.50
Redeye Anchovy Sardine Anchovy
Juvenile horse mackerel
Predator overlap index
3.8. Predator and prey niches
Prey overlap index
The reduction in anchovy biomass and the increase in abundance of sardine in the 1990s is reflected in their relative net impacts on predatory fish such as snoek and other large pelagic fish, seabirds, seals and cetaceans (Fig. 10). In the 1990s, redeye was abundant and had a positive modelled impact on marine mammals. In this decade, the chub mackerel stock included large fish that have a more piscivorous diet than smaller chub mackerel. A quarter of the diet of chub mackerel consisted of mesopelagic fish in the 1990s model and this is reflected in the positive impact of mesopelagic fish on chub mackerel (Fig. 10B). Fishing had larger negative impacts on sardine in the 1980s than in the 1990s, when sardine biomass was larger.
Group
3.7. Mixed trophic impacts
Table 5 Predator and prey overlap indices for the five groups of small pelagics and mesopelagic fish in the southern Benguela ecosystem
Relative mortalities attributed to fisheries, predation and other causes are shown in Fig. 9. Modeled mortality is largest in the cephalopod and small hake groups, particularly caused by heavy predation. Of the total natural predation on hakes in the southern Benguela ecosystem model for the 1980s, 32% was through cannibalism, 27% of hake production was eaten by cephalopods and 12% went to seals. In the 1990s model, cannibalism made up 40%, predation by cephalopods accounted for 24% and seals consumed 11%. Total catches of hakes amounted to 12% and 11% of hake production in the 1980s and 1990s, respectively. Fishing mortality of sardine and juvenile horse mackerel increased over the two decades, whereas anchovy fishing mortality was reduced in the 1990s.
1.00 0.59 0.99 0.92
3.6. Mortality
1.00 0.59 0.99 0.92
Other small pelagics
total annual catches during the 1990s. In the 1990s model, the proportion of the catch in discrete trophic levels IV, V and VI is slightly larger than in the 1980s (Fig. 8).
Anchovy Sardine Redeye Other small pelagics Juvenile horse mackerel Mesopelagic fish
Juvenile horse mackerel
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Sardine
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that consumed them (Table 5). These five small pelagic fish groups showed identical prey overlaps in the 1980s and 1990s because diet compositions of these groups are assumed constant between the two decades. However, there were greater overlaps in shared predators of small pelagic fish during the 1990s than the 1980s (Table 5). This may be related to the smaller total catches in the 1990s than the 1980s (Table 4) and the 13% increase in biomass of small pelagic fish predators (large pelagic fish, hakes, seabirds, seals and cetaceans) from the 1980s to the 1990s.
4. Discussion Given the variable accuracy and precision of the different data series used to estimate input parameters for the models, and the constraints of periods and areas for which data were available, there is uncertainty associated with the model outputs. For example, coefficients of variation (CV) of spawner biomass hydro-acoustic surveys from 1985 to 1997 ranged between 12% and 33% for anchovy and between 21% and 55% for sardine (Barange et al., 1999). Similarly, CVs of spring biomass estimates for horse mackerel from bottom trawling ranged between 21% and 30% and from hydroacoustic surveys, between 17% and 50% (Barange et al., 1998). Therefore, careful interpretation is required of differences in model summary statistics between the 1980s and 1990s. Shannon (2001) investigated sensitivity to parameterization of models of the southern Benguela ecosystem in the 1980s and 1990s. Overall, results of sensitivity analyses, analyses of possible combinations of parameters for which models are balanced and investigations using alternate parameter values show that the models are constrained, with little scope for allocating parameter values far from those considered to be best estimates. Model structure forces constraints on parameter values, even those that are poorly known. Therefore, there are a limited number of possible combinations of parameters describing this ecosystem, making quantifiable aspects of the model more believable (for example, larger sardine M used in the ecosystem models of this study than in stock assessment models).
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4.1. Zooplankton The minimum required zooplankton biomass (summed micro-, meso- and macrozooplankton biomass) was estimated to be 10% larger in the 1990s than that input to the 1980s model (Table 1). This increase in zooplankton biomass is consistent with observed increases in abundance in the region of St. Helena Bay, on the west coast of South Africa (Verheye and Richardson, 1998; Verheye et al., 1998). Between 1951 and 1996, zooplankton abundance increased by at least an order of magnitude in all size classes. The biomass of copepods (including some large calanoid copepods that are macrozooplankton) increased by about 60% between the late 1980s and 1995/1996 (Verheye et al., 1998). Verheye et al. (1998) concluded that there has been a longterm change in the food environment of small pelagic fish in the southern Benguela since the 1950s. Because the model biomass of zooplankton and the stocks of small pelagic fish were larger in the 1990s than in the 1980s, there was more food available to their model predators during this decade. This, and the larger catches of small pelagic fish in the 1980s, meant that the southern Benguela model ecosystem was more tightly constrained by predators (including the fishery) and availability of food in the 1980s than in the 1990s. Tight constraints are also reflected in the larger individual ecotrophic efficiencies of most fish groups in the 1980s compared to those in the 1990s (Table 1). 4.2. Hakes Hake biomass indices from surveys (Badenhorst and Smale, 1991) are greater than biomass estimated by the production model (Leslie, 1996). Further, it is likely that hake biomass exceeds the survey indices because untrawlable ground is not covered and small, pelagic hake may be missed. Therefore, it is expected that biomass, in particular that of small hake, is larger than stock assessment production model estimates. Accordingly, because the Ecopath models showed that production of small hake was insufficient to support the consumption by large hake and other predators, the required biomass of small hake was estimated, assuming an ecotrophic efficiency (proportion of production con-
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sumed or exported from the system) of 99.9%. Models showed that minimum required biomass of hake was 34% (1980s) and 22% (1990s) more than the production model index. The additional biomass was in the small hake classes and is not necessarily inconsistent with results from production models because juvenile mortality is likely to be underestimated, therefore also underestimating biomass (R.W. Leslie, Marine and Coastal Management, pers. comm.). 4.3. Biomass and production of fish Shannon and Field (1985) estimated that a maximum biomass and annual production of 2 million tons of small pelagic fish could be supported in the southern Benguela ecosystem. Accounting for the smaller area (Orange River to Cape Agulhas) considered by Shannon and Field (1985), and their use of a lower conversion ratio from carbon to wet mass, our estimates of 3.1 and 3.3 million tons are remarkably similar to this. Moloney and Field (1985) estimated that 25% of pelagic fish production off southern Africa is exploitable by humans. This is equivalent to 775 000 t year 1 in the 1980s and 825 000 t year 1 in the 1990s. However, Moloney and Field (1985) did not recommend full exploitation of pelagic fish production because areas such as the Agulhas Bank are important for spawning pelagic fish and are likely to be important buffers against the large catches made off the west coast of South Africa. Total annual catches of the five small pelagic fish groups were larger in the 1980s (430 100 t, i.e. 14% of total small pelagic fish production) than in the 1990s (312 400 t, i.e. 9% of total small pelagic fish production). The opposite was the case for predatory snoek; annual catches rose from 11 000 to 18 000 t over the last decade (Table 1). Groups such as mesopelagic fish and redeye are not caught in large quantities in the southern Benguela ecosystem. However, these groups play a potentially large role in the trophic functioning of the southern Benguela ecosystem by providing food for other species. For example, the model estimates suggest that hake consumed 1.1 million tons of mesopelagic fish during the 1990s. This far exceeds earlier estimates by Payne et al. (1987) and Bergh et al. (1985), and is in agreement with Armstrong and Prosch’s
(1991) conclusion that annual consumption of lightfish in the southern Benguela ecosystem is considerably larger than initially thought. 4.4. Trophic levels and trophic aggregation Trophic levels of seals and cetaceans are in the upper part of the range reported by Pauly et al. (1998a) for these groups, indicating that they are feeding fairly high in the southern Benguela food web. Differences in availability of prey in the 1980s and 1990s meant that top pelagic predators were forced to consume larger quantities of prey lower in the food web during the 1990s, leading to marginally reduced trophic levels in the 1990s model for M. capensis, seabirds and cetaceans, which prey on small pelagic fish. This is explained by sardine (trophic level of 3.0) becoming more abundant and anchovy (trophic level of 3.5) decreasing from the 1980s to the 1990s. These differences are surprisingly small, being buffered by the increase in the contribution of redeye to the diets of cetaceans and seabirds in the 1990s model. Redeye occupies a higher trophic level than anchovy and sardine, at 3.6. Heavy fishing on large chub mackerel during the late 1970s and 1980s left a population in the 1980s dominated by young fish that are largely zooplanktivorous. By the 1990s, the population structure had recovered, with large chub mackerel eating mostly fish, this being indicated by their slightly higher trophic level (Table 1). Analysis of 50 models of estuarine and marine ecosystems showed that in general, the mean TE between TLs is approximately 10%, although variance is large (Christensen and Pauly, 1995). In upwelling ecosystems, TEs are generally lower than this (Jarre-Teichmann, 1992; Christensen and Pauly, 1993; Jarre-Teichmann and Pauly, 1993; Jarre-Teichmann and Christensen, 1998). This is true for flows through TL II (consumption of phytoplankton by microzooplankton) in the southern Benguela ecosystem (Table 3). Only 55% and 60% of net primary production is consumed by herbivores in the southern Benguela ecosystem during the 1980s and 1990s, respectively. Although larger than the 39% estimated previously (Baird et al., 1991), these efficiencies are still much smaller than those in the Peruvian upwelling system and may be explained by the mismatch in
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space and time between phytoplankton blooms and zooplankton production (Baird et al., 1991). Results agree with the work of Shannon and Field (1985), who estimated that 44– 73% of phytoplankton production was not consumed by zooplankton or fish. Because of the nature of the pulsed upwelling events in the southern Benguela ecosystem, the migration of pelagic fish through the system, and because some phytoplankton are of unsuitable quality or size, pelagic fish are probably only able to utilise about 12.5% of primary production in the system (Shannon and Field, 1985). Walker and Peterson (1991) estimated that copepods consume between 12% and 42% of primary production along the productive west coast of South Africa. By comparison, this study of the southern Benguela sub-system, covering a larger region and including the productive upwelling regions along the west coast as well as the less productive Agulhas Bank and south coast areas, shows that mesozooplankton consume only 4– 5% of primary production and that microzooplankton consumed 49% and 53% of total modelled primary production in the 1980s and 1990s, respectively. In their preliminary carbon budget for the southern Benguela ecosystem, Walker and Peterson (1991) estimated that 75% of phytoplankton production was lost from the euphotic zone as detritus. By comparison, models suggest that only 45% and 39% of phytoplankton production is lost in the form of detritus and sedimentation from the southern Benguela ecosystem during the 1980s and 1990s, respectively. This may suggest more efficient use of phytoplankton than previously thought. Transfer of biomass at TL III – V appears to be more efficient in the southern Benguela ecosystem than in other upwelling ecosystems (Jarre-Teichmann et al., 1998). The geometric mean TE of biomass for TL II – IV in the southern Benguela system was 15.1% in both decades. TEs at each TL are all greater than means estimated by Christensen and Pauly (1995) for upwelling ecosystems. These large values indicate a ‘‘bottleneck’’ of flows at the levels of zooplankton (TL II and III) and small pelagic fish (TL III and IV), pointing to the groups as being important in the overall trophic structure of the ecosystem. The high TEs also indicate that the southern Benguela ecosystem may be foodlimited. This is in agreement with the suggestion by Shannon and Field (1985) that at large stock sizes,
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anchovy and sardine may be food-limited in the southern Benguela ecosystem. During both the 1980s and 1990s, the geometric mean transfer efficiency for TL II – VIII (containing biomass >0.0005 t km 2) was 12.0%, close to Baird et al.’s (1991) estimate of 12.1%. Biomass was concentrated in trophic levels I and II, i.e. the producer (phytoplankton) and detritus level (TL 1) and the primary consumer (microzooplankton) level (Table 3). This is true of many ecosystems such as coral reefs (e.g. Alino et al., 1993; Opitz, 1993), coastal regions (e.g. De Paula E Silva et al., 1993; Vega-Cendejas et al., 1993), shelf ecosystems (e.g. Arrenguin-Sanchez et al., 1993) and other upwelling systems (e.g. Jarre-Teichmann and Christensen, 1998). 4.5. Consumption of small pelagic fish Modelled consumption of anchovy by hake amounted to 70% of the anchovy caught during the 1980s. This differs from Field et al.’s (unpublished) estimate that hake consumed twice the quantity of anchovy taken by the fishery during the 1980s. Estimates of diet and stock sizes of many of the model groups have been revised since Field et al.’s (unpublished) preliminary model, accounting for the differences between their results and those presented here. This points out sensitivity of results to best estimates that may not be accurate. The small proportion of small pelagic fish production consumed by seabirds (8%) in the southern Benguela ecosystem is at the top of the 5– 8% range estimated for seabirds in the North Sea (Bailey, 1986), and much less than the 20 –30% estimate of Furness (1982) and MacCall (1990) for seabirds in other upwelling systems. Of the 9% of small pelagic fish production that is consumed by marine mammals, consumption by seals accounted for twothirds of this, reconfirming Bergh et al.’s (1985) suggestion that whales and dolphins currently play a small trophic role in the southern Benguela ecosystem. 4.6. Summary statistics and flows In previous studies, five upwelling systems, including the southern Benguela during the 1980s, were ranked according to primary production, biomass,
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system throughput and catches, all measures of ecosystem size (Jarre-Teichmann and Christensen, 1998; Jarre-Teichmann et al., 1998). In terms of biomass and throughput, the southern Benguela system was most similar to the Peruvian system during the 1970s, after the collapse of the Peruvian anchovy Engraulis ringens fishery. The southern Benguela ecosystem ranked between the Peruvian and northern Benguela systems in terms of primary production (Jarre-Teichmann et al., 1998). However, the southern Benguela ecosystem was larger in biomass and catches, had a higher total system throughput and was more productive than the Californian system (Jarre-Teichmann et al., 1998). Ware (1992) estimated that the catch efficiency (catch divided by primary production) on the South African west coast was larger than that for the Californian ecosystem. This suggests that although primary production is not efficiently utilised in the southern Benguela ecosystem, the Californian ecosystem is even less efficient, probably because of its sizeable alongshore extent and the consequent large losses of primary production through offshore transport (Ware, 1992). Mean path lengths estimated in this study are longer than the path length of 2.54 in the Benguela model of Baird et al. (1991), showing that at least some summary statistics are to a certain degree dependent on model structure. In the models of the southern Benguela ecosystem, the maximum number of steps from primary producer to top predator (chain length) is 10. By comparison, a maximum chain length of eight was reported for upwelling and oceanic systems, whereas paths in models of some shelf and coastal systems were longer (Christensen and Pauly, 1993). However, none of the models they considered explicitly included several zooplankton boxes, notably microzooplankton. Maximum chain length of the southern Benguela models is large because not only do the models include the upwelling zones along the west coast, they also extend over the Agulhas Bank region. Even longer maximum chain lengths would be expected if planktonic groups were considered in more detail in models of the southern Benguela ecosystem. Considering the work of Odum (1969) on the development of ecosystems, Christensen (1995) found that system overhead, which reflects the potential of a system to increase its ascendancy to meet unexpected perturbations, is positively correlated with maturity
and is a possible measure of stability. Relative ascendancy is dimensionless, excludes the influence of system throughput on both terms, and therefore it is considered to be a suitable measure for comparing different ecosystems (Christensen, 1995; Field et al., 1989a,b). Relative ascendancy was previously estimated to be 51% in the Benguela ecosystem (Baird et al., 1991). In this study, relative ascendancy is less than half this during both decades (Table 4). This result is more in line with the findings of JarreTeichmann (1992) for the Peruvian upwelling system, where relative ascendancy varied around 30%, and relative overhead around 70%. The Peruvian system shows characteristics of a typical upwelling system (Jarre-Teichmann et al., 1998) in that it is even less stable (‘‘mature’’) than the southern Benguela system, with a lower relative overhead (70% for the Peruvian system vs. 80% for the southern Benguela system). Relative overhead values for the models of upwelling systems compared in Jarre-Teichmann (1998) ranged from 63% to 70% and support this interpretation, although it should be viewed with some caution given the differences in model structure. In a model with a very different structure, focussed on trophic interactions in the benthic community of the Antarctic eastern Weddell Sea shelf, Jarre-Teichmann et al. (1997) found a relative overhead of 77%, and suggested that this was a characteristic indicating stability of the system to external perturbations—in this particular case, scraping of the bottom by icebergs in combinations with low turnover rates (caused by low temperature). 4.7. Primary production required to sustain catches Primary production equivalents are used to compare effects of fishing at different trophic levels (Pauly and Christensen, 1995). For example, harvesting of fish at low trophic levels is ecologically less expensive than fishing at a higher trophic level, given the inefficient transfer of energy up the food web. Primary production equivalents required to sustain catches in the southern Benguela ecosystem are small proportions (4%) in comparison to the Peruvian system (13 – 15%), and less than half the 9.5% mean for the seven upwelling systems examined by Jarre-Teichmann and Christensen (1998). They are more in line with percentages required to sustain catches in open ocean
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
(small primary production and catch densities) or coastal regions (large primary production and catches) than in other upwelling systems or shelf systems (Pauly and Christensen, 1995). Jarre-Teichmann and Christensen (1998) explained the discrepancy between their mean PPR for upwelling systems with the mean of 25% estimated by Christensen and Pauly (1995); the latter authors considered the 1990s, when there were large catches (especially in the southeastern Pacific), and assumed primary production equal to that in the 1980s, whereas Jarre-Teichmann and Christensen (1998) focussed on the 1970s and early 1980s in their study, when catches were smaller. Further, Christensen and Pauly (1995) included discards in their estimates, whereas Jarre-Teichmann and Christensen (1998) used nominal catches. Discards were not included in southern Benguela models of this study. Catches in the southern Benguela ecosystem are small in comparison to other upwelling systems, and primary production is larger than that of the northern Benguela, northwest African and Californian upwelling systems (Jarre-Teichmann et al., 1998). In addition, fishing in the southern Benguela ecosystem takes place at low trophic levels, with the overall result that the percentage PPR to sustain catches is small. The mean trophic level of the fishery increased slightly from the 1980s to the 1990s (Table 4) because a larger proportion of the catch in the 1990s was of snoek and hakes, which occur at higher trophic levels than small planktivorous fish. Therefore, in the southern Benguela pelagic ecosystem, we do not appear to be ‘‘fishing down the food web’’ as has been shown for many regions (Pauly et al., 1998b, 2000a,b). The mean trophic level of the fishery in upwelling systems in 1988 –1991 is 3.8 (Pauly and Christensen, 1995). This is lower than that in the southern Benguela ecosystem (Table 4) where not only small pelagic fish but also hake and snoek are targeted. By comparison, the mean trophic level of the fishery off Peru was 3.5 in the 1960s when anchovy was targeted, and 3.7 in the 1970s when more sardine and hake were caught (Jarre-Teichmann, 1998). 4.8. Fishing mortality It has been estimated that the total finfish biomass consumed globally by finfish is three times larger than
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the global catches of finfish (Christensen, 1996). A generalisation from more than 50 models of aquatic ecosystems is that catches are much smaller than the production consumed by predators, even in heavily exploited systems (Bax, 1991; Jarre et al., 1991; Christensen and Pauly, 1995). This is in agreement with Moloney and Field’s (1985) assumption that humans are able to exploit not more than 25% of pelagic fish production off South Africa. For most species in the southern Benguela ecosystem, fishing mortality is much smaller than predation mortality (Fig. 9). Exceptions are predators such as snoek, other large pelagic fish and large M. paradoxus, for which fishing mortality is estimated to be similar or larger than predation mortality (Fig. 9). In the 1970s, fishing mortality for hake in the Peruvian, Namibian and northwest African upwelling systems was similar to natural mortality (Jarre-Teichmann and Christensen, 1998). Equal portions of the total hake production in the southern Benguela ecosystem go to the fishery and to seals, in contrast to the initial estimate of Field et al. (unpublished) that seals take only 22% of the amount of hake caught in the fishery. The mean size of hake eaten by seals is 21 cm, smaller than 25 cm, the minimum length of hake taken by the fishery (David, 1987). Taking into account seal mortality related to fishing vessels, the net benefit of the fishery to seals is that 2 –5% of the seal population is being ‘‘supported’’ by the fishing industry on a year-round basis (David, 1987). However, only 0.3% of total consumption by seals is of fish scavenged during fishing operations (Wickens et al., 1992). Most of the hake eaten by seals are consumed naturally or scavenged when discarded by trawlers. The anchovy fisheries in the southern Benguela and Peruvian ecosystems show similarities. For anchovy, the ratio of natural mortality (predation and other mortality) to fishing mortality in the southern Benguela ecosystem was 2.97 in the 1980s and 4.22 in the 1990s. These mirror the ratios of 2.38 and 4.10 for anchovy in the Peruvian system during the 1960s, when there was a large fishery for anchovy, and the 1970s, after the collapse of the anchovy fishery (JarreTeichmann and Christensen, 1998), highlighting the competition for anchovy between its natural predators and the fishery. Off Peru, specialised anchovy predators (cormorants) have decreased with increased fish-
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ing (Tovar et al., 1987). Off South Africa, low anchovy abundance negatively affected the breeding of African Penguins, Cape Cormorants and Swift Terns (Crawford and Dyer, 1995). However, this is not because fishing pressure on anchovy increased, but because anchovy abundance decreased, reflecting the extent to which some predators rely upon particular prey species. In contrast, many species are opportunistic, taking advantage of any available prey (Crawford et al., 1987). The specialists are the ones that are at risk from overfishing and natural fluctuations in prey abundance. 4.9. Functioning of the southern Benguela ecosystem in the 1980s and 1990s Some differences have been shown between the anchovy-dominated system of the 1980s and the 1990s when sardine biomass increased. For example, many flows through the southern Benguela ecosystem are larger in the 1990s model (Table 4). However, owing to the large uncertainty around model input parameters, some of these differences (such as those less than 10%) may not be representative of change from the 1980s to the 1990s. For example, production of small pelagic fish only differs by 7% between decades, which may be negligible given the coefficients of variation between 12% and 55% for anchovy and sardine biomass surveys (Barange et al., 1999). Overall differences between the trophic models are not as large as expected from the differences in biomass and catches of many species. Trophically, the southern Benguela ecosystem seems to have functioned in a similar way during both decades, as shown by the similarity in transfer efficiencies, biomass per trophic level, mixed trophic impacts and relative ascendancy. This is in line with results from comparisons of models of upwelling systems, where the systems tend to group by ‘‘sys-
tem’’ rather than by decade or dominance regime (Jarre-Teichmann and Christensen, 1998). Biomass and catches of the small pelagic fish component of the southern Benguela ecosystem differ between the two periods. However, model production by small pelagic fish is close to 3 million tons in both decades, at least partly because it has been maintained at this level through careful management of the pelagic fisheries. Further, the combined model ecotrophic efficiency of small pelagic fish (calculated as the ratio of the sum of catches and their consumption by predators to production by the group) is constant over the two decades (0.977 in 1980s and 0.976 in 1990s). In addition, the proportion of small pelagic fish production consumed by predators is similar in the two decades modelled. The apparently small differences between the generalised trophic structure of the anchovy- and sardine-dominated ecosystems suggest some degree of trophic similarity of small pelagic fish in the southern Benguela ecosystem; it is likely that in this system, small pelagic fish species are trophically interchangeable to a certain extent.
Acknowledgements We are very grateful to many scientists in the region for assistance with, provision of and discussions about data used in our models. We would like to thank Mrs Cathy Boucher for preparing Figs. 1 and 10 for use in this paper.
Appendix A Sources of data used to estimate input parameters and diets for southern Benguela Ecopath models (Tables A.1 –A.10).
Table A.1 Plankton: input data for southern Benguela Ecopath models Original value
Source
Value used
Comments
Phytoplankton B
1.2 106 t C
P/B
133.3 year 1
Brown et al., 1991 used conversion factor of 14.25 for C:wet mass Brown et al., 1991
154.4 year 1
Sedimentation
368.4 t km 2 year 1
Pitcher et al., 1991
Primary production in Brown et al. (1991) increased by 18% to account for particulate dissolved organic C (1989 workshop). Sedimentation estimated to be 3.7% of daily production (Pitcher et al., 1991).
Microzooplankton (2 – 200 lm equivalent spherical diameter; nanoflagellates, ciliates, zooplankton larvae) B 5.525 t km 2 Jarre-Teichmann et al., 1998, Estimated Using Ecopath, estimated B required in 1980s and 1990s. from Brown et al. (1991) and P/B 482 year 1 Painting et al. (1992); used conversion factor of 14.25 for C:wet mass P/Q 20% Calculated from U and respiration/Q in 25% Jarre-Teichmann et al., 1998 Painting et al., 1992 U 20% Stoecker, 1984 Mesozooplankton (200 – 2000 lm; copepods, in particular Calanoides carinatus and Calanus agulhensis) B 187 600 t C Hutchings et al., 1991 Estimated Using Ecopath, estimated B required during each decade. P/B 20 year 1 Hutchings et al., 1991 40 year 1 P/Bs estimated from Verheye et al. (1992) were larger, between 30 and 91 year 1. P/Q 30% Omori and Ikeda, 1984 U 35% Verheye et al., 1992; Probyn et al., 1990, 11 – 50% of food consumed by South African copepods is Probyn, 1992; H. Verheye, egested as faecal pellets. As in Jarre-Teichmann et al. (1998), MCM, pers. comm. U was estimated to be 35%. Macrozooplankton (2 – 20 mm; mainly euphausiids (on which most of the macrozooplankton estimates are based), but also includes groups such as amphipods and fish larvae) B 63 600 t C Hutchings et al., 1991 Estimated Using Ecopath, estimated B required during each decade. P/B 13 year 1 Hutchings et al., 1991 P/Q 41% Hutchings et al., 1991 U 35% Jarre-Teichmann et al., 1998 20% Assimilation efficiency of euphausiids is closer to 80% H. Verheye, MCM, pers. comm. Gelatinous Zooplankton (Cnidaria, Ctenphora, tunicates, chaetognaths) B 55 106 t A.J. Boyd, MCM, pers. comm. P/B P/Q U
0.584 year 1 35% 20%
Jarre-Teichmann et al., 1998 H. Verheye, MCM, pers. comm. Purcell, 1983
106 t
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Parameter
Biomass more likely in the range of 10 – 50% of combined meso- and macro-zooplankton biomass (L. Hutchings, MCM, pers. comm.). This is from gross efficiency of chaetognaths and siphonophores. This is from assimilation efficiency of siphonophores. 103
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Table A.2 Small pelagic fish: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Armstrong et al., 1991
1147 500 t 786 143 t
1984 – 1989 acoustic estimate, Barange, 1997. 1990 – 1996 acoustic estimate, Barange, 1997. Data for northern Benguela, agrees with South African estimate (J. De Oliveira, MCM, pers. comm.).
129 000 t 460 000 t 1.2 year 1
1984 – 1989 acoustic estimate, Barange 1997. 1990 – 1996 acoustic estimate, Barange 1997. From P/B = Z = F + M, P/B of South African sardine estimated to be 1.2 year 1 (1980s) and 1.0 year 1 (1990s). However, to account for larger increase in B in 1990s (Barange, 1997), P/B was assumed equivalent in both decades, i.e. 1.2 year 1. Q/B lies within the range estimated from Van der Lingen’s (1998) daily rations for sardine.
P/B
1.2 year 1
Hewitson and Cruickshank, 1993
Q/B
12.3 year 1
Armstrong et al., 1991
Sardine (Sardinops sagax) B 146 000 t
Armstrong et al., 1991
P/B
1.1 year 1
Hewitson and Cruickshank, 1993, Northern Benguela
P/Q
9.7%
Armstrong et al., 1991
Redeye (Round herring; Etrumeus whiteheadi) B 1980s 1 222 000 t Roel and Armstrong, 1991 B 1990s
P/B P/Q
1.2 year 1 10%
Estimated
Minimum estimate from acoustic surveys (1986, 1987, 1989). Likely that redeye B was larger, particularly in 1990s (L. Hutchings and C. van der Lingen, MCM, pers. comm.). Therefore allowed Ecopath to estimate B required in 1990s. Assumed similar to P/Bs of anchovy and sardine. Assumed similar to other clupeoids (Jarre-Teichmann et al., 1998).
Other small pelagic fish (saury (Scomberesox saurus), flying fish (Exocoetidae), pelagic goby (Sufflogobius bibarbatus)) B 80 000 t 1989 Workshop B assumed constant in 1980s and 1990s. P/B 0.9 year 1 1989 Workshop 1.0 year 1 Assumed closer to P/B of anchovy, sardine and redeye. P/Q 10% Assumed similar to other clupeoids (Jarre-Teichmann et al., 1998).
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Cape anchovy (Engraulis capensis) B 1106 000 t
Table A.3 Horse and chub mackerel: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Large (>20 cm) horse mackerel (Trachurus trachurus capensis) B 1980s 356 000 t 1980s: B on south coast (1975 – 1983) B 1990s 426 240 t estimated from Kinloch et al.’s (1986) VPA analysis and Kerstan and Leslie’s (1994) length – mass relation. 1990s: Based on Barange et al. (1998). P/B 0.52 year 1 Jarre-Teichmann et al., 1998 Q/B 5.1 year 1 Jarre-Teichmann et al., 1998 U 30% Chub mackerel (Scomber japonicus) B 1980s 62 500 t B 1990s 100 000 t P/B 1980s 0.6 year 1 P/B 1990s
0.5 year 1
P/Q U 1980s U 1990s
10% 25% 20%
Crawford, 1989; Crawford et al., 1983; Jarre-Teichmann et al., 1998 Assuming fish were smaller in 1980s after collapse of stock P/B assumed similar to other predatory fish (snoek)
Comments
Assumed similar to P/Bs of anchovy and sardine. Assumed similar to Q/Bs of anchovy and sardine. Juveniles are zooplanktivorous.
B on west coast is five times smaller than on south coast (Barange et al., 1998).
1.0 year 1 10 year 1
0.9 year 1 0.8 year 1
Calculated from larger Q/B with P/Q at 10%. Q/B larger from daily rations in Pillar and Barange (1998). Large horse mackerel eat zooplankton and fish.
B in 1990s estimated to be that prior to heavy exploitation in the 1970s, i.e. that in Crawford, 1989. P/B = 0.89 year 1 used off North West Africa (Jarre, DFU, pers, comm. based on F = 0.49 and M = 0.4 year 1). If P/Q = 10%, Q/B likely exceeds 5 – 6 year 1 considering daily ration (Hatanaka et al., 1957, in Livingston and Goiney, 1984).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Small ( < 20 cm) horse mackerel (Trachurus trachurus capensis) B 1980s 44 000 t Estimated from unpublished data, B 1990s 106 560 t Marine and Coastal Management. P/B 1.2 year 1 Q/B 12 year 1 U 35%
Assumed Heavy exploitation left more small, zooplanktivorous fish in 1980s, whereas by 1990s fish were larger (piscivorous).
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Table A.4 Other large pelagic fish: input data for southern Benguela Ecopath models Parameter Snoek (Thyrsites B 1980s B 1990s P/B P/Q U
Original value atun) 52 700 t ? 0.5 year 1
Value used
Comments
Penney et al., 1991a
52 700 t Estimated
Similar estimate for 20% exploitation rate (L. Hutchings, MCM, pers. comm.). Larger catches in 1990s, reflect increased B? Ecopath estimated B required in 1990s. P/B = Z = F + M, where M assumed same as chub mackerel (O. Centurier-Harris, formerly MCM, unpublished data) and barracuda (Opitz, 1991), F calculated from catches. Assumption. Following Winberg, 1956, snoek assumed to be efficient predators.
10% 20%
Penney et al., 1991a Penney et al., 1991a
No indication of change in B in 1990s, B constancy assumed. Combined P/B calculated by weighting according to relative Bs. Geelbek P/B estimated from Z = F + M using Griffiths (1995) and Griffiths and Hecht (1995). Tuna P/B estimated from M using Pauly (1980) and Laurs and Wetherall (1981) and F using Penney et al., 1991a. Considered P/Q = 5% for tuna, 10% for others. Tuna P/Q corresponds to Q/B within Palomares and Pauly’s (1998) estimated range. Large pelagic fish assumed efficient predators.
20%
Table A.5 Cephalopods and mesopelagic fish: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Cephalopods B
40 000 t
1989 Workshop
300 000 t
P/B
1.5 year 1
Jarre-Teichmann et al., 1998
3.5 year 1
P/Q
10%
Jarre-Teichmann et al., 1998
35%
Maximum B index for chokka squid is 100 000 t (Lipinski, 1992). B of cephalopods assumed to be three times B of chokka alone. Larger P/B required to obtain P of 1 million t estimated by Bergh et al. (1985). Their P is an order of magnitude larger than if P/B = 1.5 year 1. At lower limit of range estimated by O’Dor et al. (1980, in Livingston and Goiney, 1984).
U
20%
Mesopelagic fish (Lanternfish lampanyctodes hectoris and lightfish maurolicus muelleri) B 1 – 2.4 106 t Armstrong and Prosch, 1991; Estimated Armstrong et al., 1991 P/B 1.2 year 1 Hewitson and Cruickshank, 1993 P/Q 10% U 35%
Ecopath used to estimate actual B required in each decade (fell within indicated range) Assumed similar to P/Q of anchovy Assumed same as U of other zooplanktivorous fish
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Other large pelagic fish B 28 775 t Group P/B 0.48 year 1 Kob 0.36 year 1 Yellowtail 0.53 year 1 Geelbek 0.88 year 1 Tuna 0.47 year 1 P/Q 5.6 year 1 U
Source
Table A.6 Hake: input data for southern Benguela Ecopath models Original value
Source
Value used
Comments
Small M. capensis B 1980s B 1990s
65 457 t 73 752 t
Estimated Estimated
Ecopath used to estimate B required in both decades
P/B
1.2 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998, similar to small pelagic fish
2.0 year 1
Bergh et al. (1985) estimated hake P/B = 4.8 year 1 given rapid turnover of small hake. P/B increased for Ecopath model.
P/Q U
15% 35%
Jarre-Teichmann et al., 1998
Large M. capensis B 1980s B 1990s
181 036 t 247 909 t
P/B
0.6 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998
0.8 year 1
P/Q U
25% 20%
Jarre-Teichmann et al., 1998
18%
Small M. paradoxus B 1980s B 1990s
226 866 t 290 249 t
P/B
1.2 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998, similar to small pelagic fish
P/Q U
15% 35%
Large M. paradoxus B 1980s 150 553 t B 1990s 234 646 t P/B P/Q
0.6 year 1 25%
U
20%
Assumed similar to other zooplanktivorous fish
P/B and P/Q adjusted so that Q/B = 4.4 year 1, estimated from daily ration of large M. capensis in Punt and Leslie, 1995 Assumed similar to other predatory fish
Estimated Estimated
Ecopath used to estimate B required in both decades
2.0 year 1
Bergh et al. (1985) estimated hake P/B = 4.8 year 1 given rapid turnover of small hake. P/B increased for Ecopath model.
Jarre-Teichmann et al., 1998
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Parameter
Assumed similar to other zooplanktivorous fish
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
0.8 year 1 17%
P/B and P/Q adjusted so that Q/B = 4.7 year 1, estimated from daily ration of large M. paradoxus in Punt and Leslie, 1995 Assumed similar to other predatory fish 107
108
Table A.7 Other demersal fish and chondrichthyans: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Pelagic-feeding chondrichthyans B 128 000 t P/B Q/B U
0.5 year 1 4.5 year 1 20%
Chondrichthyan B estimated to be 330 000 t (Jarre-Teichmann et al., 1998). Pelagic-feeders estimated to comprise 40% of B excluding apex predators. Assumed similar to other large pelagic fish. Similar to Q/B for dogfish (Livingstone and Goiney, 1984) and sandbar shark (Stillwell and Kohler, 1993). Assumed similar to other predatory fish and carnivores.
Benthic-feeding chondrichthyans B 192 000 t P/B 1.0 year 1 P/Q 10% U 20%
Estimated to comprise 60% of B excluding apex predators. Assumed similar to P/B of demersal fish. Assumption. Assumed similar to other predatory fish and carnivores.
Apex predatory chondrichthyans B 10 000 t P/B 0.5 year 1 P/Q 10% U 20%
Assumed to comprise 3% of total chondrichthyan B. From Z of great white sharks off South Africa (Cliff et al., 1996). Assumption. Assumed similar to other predatory fish and carnivores.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Pelagic- and benthic-feeding demersal fish (P/B, P/Q and U are assumed to be the same for both groups) B 230 000 t for all Japp et al., 1994, Estimated Using Ecopath, B of each group estimated each decade. demersals 1989 workshop P/B 1.0 year 1 Jarre-Teichmann P/B estimated for Q/B = 5 year 1, in middle of range estimated by Palomares and Pauly (1988) for et al., 1998 flatfish, and double that for more sedentary kingklip (MacPherson, 1983). P/Q 20% Assumed similar to large hake; within range estimated for flatfish (Livingstone and Goiney, 1984). U 20% Assumed similar to large hake.
Table A.8 Marine mammals and birds: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments Counts of pups from 1971 to mid-1990s do not show overall increase in seals off South Africa, therefore B assumed constant.
P/B Q/B
0.946 year 1 19.3 year 1
U
20%
Cetaceans B 1980s
16 200 t
B 1990s P/B Q/B
18 000 t 0.6 year 1 7.5 – 10 year 1
1989 Workshop Jarre-Teichmann et al., 1998
U
21%
Gaskin, 1982
Seabirds B 1980s B 1990s P/B Q/B U
3257 t 2616 t 0.123 year 1 118 year 1 26%
Crawford Crawford Crawford Crawford Crawford
1989 Workshop Estimated from Balmelli and Wickens’ (1994) Q estimate, Butterworth et al.’s (1988) mean weight and Wickens et al.’s (1992b) abundance estimate. Furness (1984) for carnivorous mammals.
B of Bryde’s whales estimated from Best and Rickett (1984).
B of other trophically important cetaceans probably does not exceed B of Bryde’s whales. Assuming 1% annual increase.
et et et et et
al., al., al., al., al.,
1991a 1991a 1991a 1991a 1991a
10 year 1
From daily rations of bottlenose and humpback dolphins (Smale et al., 1994) and Bryde’s whales (Best and Rickett, 1984). Within Tamura and Ohsumi’s (2000) range for cetaceans in the Southern Hemisphere.
1990s B estimated from unpublished data, MCM; Crawford et al., 1991a, 1995, 1999.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Seals (Arctocephalus pusillus pusillus) B 29 180 t 1989 Workshop
109
110
Parameter
Original value
Source
Benthic producers B ? P/B
15.0 year 1
Jarre-Teichmann et al., 1998
Meiobenthos B P/B P/Q U
? 4.0 year 1 12% 20%
Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
Macrobenthos B P/B P/Q U
? 1.2 year 1 12% 20%
Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
Value used
Comments
Estimated
Using Ecopath, required B estimated for each decade; EE assumed 50% because benthic producers often consumed as decaying matter, modeled as detritus.
Estimated
Using Ecopath, required B estimated for each decade.
10%
Assimilation efficiency of benthic consumers is high (H. Verheye MCM, pers. comm.)
Estimated
Using Ecopath, required B estimated for each decade.
10%
Assimilation efficiency of benthic consumers is high (H. Verheye MCM, pers. comm.)
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Table A.9 Benthos: input data for southern Benguela Ecopath models
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
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Table A.10 Sources of dietary data used to compile the diet matrices for southern Benguela Ecopath models during the 1980s and 1990s Group
Dietary data source
Microzooplankton Mesozooplankton Macrozooplankton Gelatinous zooplankton Anchovy Sardine Redeye Other small pelagic fish Chub mackerel
Data unavailable therefore assumed following Jarre-Teichmann et al., 1998 Hutchings et al., 1991 Hutchings et al., 1991 Gibbons et al., 1992; Purcell, 1983; H. Verheye and J.J. Heymans (pers. comm.) Armstrong et al., 1991 Armstrong et al., 1991, Van der Lingen, 1998; L. Hutchings, MCM, pers. comm. Wallace-Fincham, 1987; Armstrong et al., 1991 1989 Workshop Baird, 1978, weighted by relative proportions of small and medium-sized (1980s) and small, medium and large chub mackerel (1990s), using VPA of O. Centurier-Harris (formerly MCM, unpublished data) Andronov, 1983, 1985 Andronov, 1983, 1985; Pillar and Barange, 1998, S.C. Pillar, MCM, pers. comm. Armstrong et al., 1991 1980s: Dudley, 1987; 1990s: Griffiths, 2000 Geelbek: Griffiths and Hecht, 1995 Kob, yellowtail, tuna: Penney et al., 1991b Lipinski, 1992; Sauer and Lipinski, 1991; Augustyn et al., 1994; Santos and Haimovici, 1998; Lordan et al., 1998 Punt and Leslie, 1995; Punt et al., 1992; Pillar and Wilkinson, 1995; Pillar and Barange, 1993; Pillar and Barange, 1997; Payne et al., 1987
Juvenile horse mackerel Adult horse mackerel (>20 cm) Mesopelagic fish Snoek Other large pelagic fish Cephalopods Small M. capensis Large M. capensis Small M. paradoxus Large M. paradoxus Pelagic-feeding demersal fish Benthic-feeding demersal fish
g
Pelagic-feeding chondrichthyans Benthic-feeding chondrichthyans Apex predatory chondrichthyans Seals Cetaceans Seabirds Meiobenthos Macrobenthos
g
Meyer and Smale, 1991a Meyer and Smale, 1991b; Horwood, 1993; Ansell and Gibson, 1990; Molinero and Flos, 1992; Braber and De Groot, 1973; MacPherson, 1983; Payne and Badenhorst, 1989 Penney et al., 1991b; Compangno et al., 1989; Cliff et al., 1989; Smale, 1991; Sauer and Smale, 1991; Ebert et al., 1992 Penney et al., 1991b; Compagno et al., 1989 Cliff et al., 1989; Ebert, 1991 David, 1987; Meyer et al., 1992; Punt et al., 1995 1980s: Best, 1967, Sekiguchi et al., 1992 1990s: few changes made to 1980s diet so that model balanced 1980s: Crawford et al., 1991b; Best et al., 1997 1990s: Crawford et al., 1991b; Crawford, 1999; Crawford and Dyer, 1995 Poorly known, therefore assumed following Jarre-Teichmann et al., 1998
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Trophic flows in the southern Benguela during the 1980s and 1990s Lynne J. Shannon a,b,*, Coleen L. Moloney a,b, Astrid Jarre c, John G. Field b a Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa Department of Zoology, University of Cape Town, Private Bag, Rondebosch 7701, South Africa c Danish Institute for Fisheries Research, and Greenland Institute for National Resources, P.O. Box 570, DK-3900 Nuuk, Greenland b
Received 23 January 2002; accepted 23 September 2002
Abstract Mass-balanced models of trophic flows in the southern Benguela ecosystem suggest a 10% increase in zooplankton biomass between the 1980s and the 1990s, in agreement with observed trends of increased zooplankton abundance off South Africa over the last few decades. Minimum hake biomass in balanced trophic models is substantially larger than survey and other model estimates, suggesting undersampling of hakes in surveys and underestimation of juvenile hake mortality. Model biomass and mean annual production of five important small pelagic fish groups were larger in the 1990s, and total catches were smaller than in the 1980s. Estimates of biomass per trophic level, transfer efficiencies, mixed trophic impacts and many other ecosystem attributes suggest that trophic functioning of the southern Benguela ecosystem was similar in the 1980s and 1990s. Because catches were lower and model zooplankton and small pelagic fish biomasses were larger in the 1990s, the ecosystem was less tightly constrained by predators (including fishers) and food availability than in the 1980s. Fishing took place at low trophic levels compared to other systems. Despite smaller total catches in the 1990s, fishing was ecologically more expensive (from higher trophic levels) during the 1990s than in the 1980s because snoek and hake catches were large. There was greater shared niche overlap of small pelagic fish predators in the 1990s than in the 1980s. Mean transfer efficiency was 12%. Transfer of biomass at trophic levels III – V appears to be more efficient in the southern Benguela than in other upwelling ecosystems. Primary production required to sustain catches in the southern Benguela ecosystem is 4% of total primary production, i.e. more similar to estimates for open ocean and coastal regions than for other upwelling or shelf systems averaging more than double this value. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Ecosystem models; Southern Benguela; Upwelling system; Ecopath
1. Introduction One of the traditional approaches to studying ecosystems has been to concentrate on functional
* Corresponding author. Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa. Tel.: +27-21402-3171; fax: +27-21-421-7406. E-mail address: [email protected] (L.J. Shannon).
aspects, such as energy or material flows and nutrient cycling, as opposed to interactions among populations or individuals of different species (O’Neill et al., 1986). This approach, of necessity, usually involves aggregating species into functional groups, sometimes separating different life history stages of the same species. The basis of the approach is the trophic level concept (Lindeman, 1942), and although the approach has been refined and adapted over time, it still fundamentally concerns who eats whom in a food
0924-7963/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. doi:10.1016/S0924-7963(02)00250-6
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L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
and South Africa) southwards along the west coast and eastwards to 28jE (East London) (Fig. 1). The area covers 220 000 km2 and incorporates the west coast, the Agulhas Bank and the south coast (Fig. 1). The marine environment in the area is dominated by seasonal, pulsed, wind-driven coastal upwelling (Shannon, 1985). The resultant nutrient-enriched shelf waters have large biological productivity, and support the most important commercial fisheries of South Africa, including those for pelagic species (primarily sardine Sardinops sagax and anchovy Engraulis capensis) and hakes (Merluccius capensis and M. paradoxus). It is well known that the southern Benguela ecosystem varies at a number of scales, and that decadal changes, which manifest as changes in the relative abundance of sardine and anchovy populations, are an important feature of its dynamics (Schwartzlose et al., 1999). Off South Africa, large catches of sardine were made in the 1950s and 1960s, before the fishery collapsed. Fishing effort was switched to anchovy, which became the mainstay of the purse-seine fishery off South Africa. However, by the 1990s, abundance of anchovy was fluctuating and declining, whereas sardine biomass was increasing (Fig. 2). Both species have attained large stock sizes in the 2000s (unpublished data, Marine and Coastal Management).
Fig. 1. The Benguela upwelling ecosystem, (1) Northern Benguela Upwelling System, (2) Southern Benguela Upwelling System.
web. A large amount of information is often required to formulate the trophic interactions in a food web, and the development of trophic models is complicated by the fact that these interactions change over time and space. This variability has been taken into account in trophic models of the southern Benguela ecosystem, where a long-term ecosystem study (Moloney et al., in preparation) has provided sufficient information to develop and refine models that apply to different periods. The southern Benguela ecosystem is here assumed to cover the shelf region to approximately 500 m depth, extending from 29jS (in the vicinity of the Orange River mouth, the boundary between Namibia
Fig. 2. Estimates of spawner biomass of anchovy and sardine off South Africa (Hampton, 1992, 1996; Barange et al., 1999; Schwartzlose et al., 1999).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
To date, a number of studies have summarized the flows of carbon through the southern Benguela ecosystem, focusing attention on various aspects, namely the pelagic component (Shannon and Field, 1985; Bergh et al., 1985; Moloney and Field, 1985), the planktonic foodweb (Moloney, 1992) and comparison of ecosystem properties with other similar ecosystems (Baird et al., 1991). These above models produced average descriptions of the relevant food webs, but some are incomplete (because of limited data at the time of their development), and none could be used to assess decadal variability. In 1989, a coordinated effort was made to refine available estimates of carbon standing stocks and flows in the southern Benguela food web. At a local workshop of experts on the different species groups, both published and unpublished data were brought together to construct simple input – output carbon budgets for the southern Benguela. These data, together with those that have since become available, were used to construct the first Ecopath model of the southern Benguela ecosystem for the 1980s period (Jarre-Teichmann et al., 1998). Ecopath (Christensen and Pauly, 1992) is a software tool that facilitates the construction of mass-balance, trophic models of aquatic ecosystems, and allows analysis of different aspects of the resulting food web network. Species or groups of species are modelled as individual boxes for which input data is required, including estimates of biomass, production, consumption, diet data and harvests. For each box, production balances consumption, respiration and unassimilated food, so that input balances output for a steady-state over a given period. Interactions between boxes are described by sets of simultaneous linear equations. Subsequently, the 1980s model of Jarre-Teichmann et al. (1998) was modified by incorporating updated data and by separating some model components to avoid problems arising from intra-group cannibalism and major within-group differences in feeding modes. In addition, a second model was constructed of trophic flows through the southern Benguela ecosystem for the 1990s period (Shannon, 2001). The 1980s and the 1990s are known to have differed in terms of the relative abundance of the main pelagic species. What is not known is whether the observed changes in abundance of pelagic fish (Barange et al., 1999) can be linked to more subtle
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structural and functional changes in the rest of the food web. In this paper, we aim to present outputs of the two mass-balance models that describe the food webs and fishing pressures in the southern Benguela ecosystem during the decades of the 1980s and 1990s. We use these models to identify data gaps and imbalances that result from inconsistencies between various stock assessments. We compare these model results where possible, recognizing that there are uncertainties about data from which model inputs are estimated. We use the models to assess how observed differences or similarities in abundance, catches and dietary composition could affect overall trophic functioning, focusing on the pelagic part of the southern Benguela ecosystem. This work also serves as a basis for future comparisons of the results of possible consequences of fisheries management scenarios derived from static networks of trophic flows to dynamic simulations of fishing impacts (e.g. Shannon and Moloney, in preparation).
2. Methods 2.1. Model construction and balancing Mass-balanced models of the trophic flows through the southern Benguela ecosystem for the 1980s and 1990– 1997 have been constructed using the Ecopath software (Christensen and Pauly, 1992), version 3.1 (final version, February 1998). Primary production required to sustain the fishery was calculated using an alpha version of Ecopath with Ecosim version 4 (1999 – 2000). Detailed descriptions of the models and their data sources are given by Jarre-Teichmann et al. (1998) and Shannon (2001) but data sources and parameter estimates are summarised in Appendix A and the final balanced versions of the models are presented in Tables 1 and 2. The final models have 31 groups, which include all the major components of the pelagic ecosystem. The initial models, constructed from input data collated from published and unpublished sources, were unbalanced; the estimated production of many of the model groups was insufficient to support the estimated consumption by other groups and, in some cases, the catches. Because estimates of diet composition were uncertain, especially those for
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Table 1 Trophic levels, biomass (t km 2), catches (t km 2 year 1) and ecotrophic efficiencies (EEs, expressed as percentages of production either passed up the food web or exported) of all boxes in balanced southern Benguela ecosystem models during two decades Group
Phytoplankton Microzooplankton Mesozooplankton Macrozooplankton Gelatinous zooplankton Anchovy Sardine Redeye Other small pelagic fish Chub mackerel Juvenile horse mackerel Adult horse mackerel Mesopelagic fish Snoek Other large pelagic fish Cephalopods Small M. capensis Large M. capensis Small M. paradoxus Large M. paradoxus Pelagic-feeding demersal fish Benthic-feeding demersal fish Pelagic-feeding chondrichthyans Benthic-feeding chondrichthyans Apex predatory chondrichthyans Seals Cetaceans Seabirds Benthic producers Meiobenthos Macrobenthos
1980s
1990s
Trophic level
Biomass
Catch
EE
Trophic level
Biomass
Catch
EE
1.0 2.3 2.6 2.7 3.3 3.5 3.0 3.6 3.7 3.8 3.6 3.7 3.6 4.5 4.5 3.8 4.0 4.7 3.9 4.5 4.0 3.4 4.9 3.7 5.2 4.7 4.6 4.5 1.0 2.0 2.2
76.938 7.473 8.031 13.301 4.545 5.216 0.586 5.555 0.364 0.284 0.2 1.618 8.642 0.240 0.131 1.364 0.592 0.823 1.698 0.684 3.445 3.511 0.582 0.873 0.045 0.133 0.074 0.015 6.339 11.812 56.109
0.000 0.000 0.000 0.000 0.000 1.572 0.180 0.180 0.001 0.032 0.022 0.144 0.031 0.051 0.027 0.027 0.024 0.230 0.116 0.265 0.022 0.093 0.002 0.012 0.000 0.005 0.000 0.000 0.000 0.000 0.000
0.583 0.950 0.950 0.950 0.155 0.997 0.994 0.961 0.907 0.768 0.936 0.806 0.990 0.997 0.916 0.892 0.999 0.984 0.999 0.974 0.990 0.990 0.993 0.725 0.000 0.454 0.760 0.962 0.500 0.950 0.950
1.0 2.3 2.6 2.7 3.3 3.5 3.0 3.6 3.7 3.9 3.6 3.7 3.6 4.5 4.5 3.8 3.9 4.6 3.9 4.5 4.0 3.4 4.9 3.7 5.2 4.7 4.5 4.4 1.0 2.0 2.2
76.938 8.195 8.737 14.562 5.000 3.573 2.091 6.226 0.364 0.455 0.484 1.937 10.242 0.337 0.131 1.364 0.638 1.127 1.878 1.067 3.693 3.719 0.582 0.873 0.045 0.133 0.082 0.012 6.548 12.201 57.957
0.000 0.000 0.000 0.000 0.000 0.812 0.340 0.234 0.001 0.033 0.033 0.107 0.003 0.084 0.026 0.028 0.013 0.256 0.034 0.352 0.058 0.053 0.002 0.012 0.000 0.003 0.000 0.000 0.000 0.000 0.000
0.636 0.950 0.950 0.950 0.152 0.990 0.990 0.990 0.934 0.663 0.663 0.818 0.990 0.990 0.900 0.953 0.999 0.831 0.999 0.791 0.990 0.990 0.993 0.731 0.000 0.427 0.686 0.962 0.500 0.950 0.950
Italicized and bold parameters indicate the biomass required to sustain other components of the system, and were estimated using assumed EEs.
the 1990s, the models were mostly balanced by adjusting the diets of some groups (Table 2). 2.2. Diets There are some fundamental problems with the estimation of dietary compositions in many cases. Often, dietary data are only available for part of the periods or area modelled, biasing the mean dietary estimates. Taxonomic resolution is low in some stomach analyses. These are among the reasons for estimated predation on some components exceeding their pro-
duction. Therefore, it was necessary to alter the contributions of some prey in the diets of certain predators. In particular, the relative dietary contributions of small pelagic fish during the two decades required altering to balance the models. Anchovy in the diet of chub mackerel in the 1990s was reduced from 3% to 2%, and 1% sardine was considered to have been consumed. Consumption of sardine by large pelagic fish during the 1980s was reduced from 15% to 10% and the remaining 5% added to redeye. Redeye contribution to diet of large pelagics was assumed the same in the 1990s, and anchovy was reduced from 25% to 20% so
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
that sardine contributed 15%. The proportion of anchovy in the diet of seals was reduced from 25% to 20%, and the remainder added to the redeye contribution. Insufficient snoek production required that snoek contributed not more than 0.5% of seal diet, and 0.5% was added to other large pelagics and to other demersal fish. 2.3. Zooplankton For the 1990s model, the biomasses of micro-, meso- and macro-zooplankton were estimated as minimums required for the amount of production needed to sustain other groups in the system. This was necessary because there was uncertainty about how to convert abundance (numbers) to biomass (tonnage) for the various zooplankton components of the whole southern Benguela sub-system, and different carbon: wet weight conversion factors had been used in the past (e.g. by Jarre-Teichmann et al., 1998; Verheye et al., 1992). 2.4. Cephalopods Initially, model Cephalopod production was far too small to support consumption of cephalopods by other groups within the Benguela ecosystem. In the balanced version of the models used here, biomass, production/biomass (P/B) and production/consumption (P/Q) ratios were all increased from initial estimates (Table A.5). Cephalopods have been highlighted as a group urgently requiring further research to improve biological parameter estimates used in models such as those described here. 2.5. Ecosystem structures The trophic level concept was initially introduced by Lindeman (1942). Components of food webs can be aggregated into discrete trophic levels (Ulanowicz and Kay, 1991), giving an indication of the average number of steps in food webs and their efficiencies of transferring material and energy. Transfer efficiency (TE) is the fraction of total throughput at a discrete trophic level (TL), either exported or transferred to another TL (through consumption). Aggregation of flows and biomasses into discrete TLs are estimated and the TEs of biomass between TLs are
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computed. Ecopath also computes non-integer TLs (Pauly et al., 2000a). By definition, primary producers and detritus are assigned to TL 1. Consumers are assigned to a TL 1 greater than the average TL of their prey, weighted by the proportion of the prey in the consumer’s diet. Mean path length (Finn, 1976) is estimated from models of each decade, and corresponds to the mean number of trophic links in each trophic pathway. 2.6. Ecosystem flows Estimated total flows modelled include total consumption, total catches, total production and total system throughput (defined as the sum of total export, total respiration and total flows to detritus), the latter representing the overall size of a system in terms of flow. Ascendancy measures a system’s average mutual information and is scaled by system throughput (Ulanowicz, 1986; Ulanowicz and Norden, 1990). It is the product of total system throughput and the diversity of flows in a system, and is a measure representing size of flows as well as the organization of flows in a system (Field et al., 1989a,b). Ascendancy A is calculated as: A¼T
n X n X ðfij =T Þlogðfij T =Ti Tj Þ
ð1Þ
i¼1 j¼1
where T is throughput, f is flow and i and j are compartments or boxes in the ecosystem (Kay et al., 1989). Development capacity C is a measure of the potential of an ecosystem to develop, and is defined by Kay et al. (1989) as: C ¼ T
n X ðTi =T ÞlogðTi =T Þ
ð2Þ
i¼1
Relative ascendancy is defined as A/C, and relative system overhead is defined as (C A)/C (Kay et al., 1989). Fishing and predation mortalities are compared between species and decades. Catches are compared by converting flows in each path (towards the catch of a particular group) to primary production equiv-
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Table 2 Balanced diet composition of groups in the southern Benguela ecosystem during the 1980s and 1990s L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116 Shaded cells indicate dietary contributions altered in the balancing of the model. Where diet differs between decades, the contribution to diet during the 1990s is tabulated below the 1980s contribution. < indicates a dietary proportion of less than 0.5%.
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alents using the product of catch, production/consumption and the proportion of each group in the path in the diets of the other groups (Christensen et al., 2000):
PPR ¼
X Yi
Qpredator j predator;prey P P i predator EEpredator paths DCpredator;prey V
ð3Þ
where Y is catch of a given group i, P is production, Q consumption, EE the ecotrophic efficiency and DC is the diet composition for each predator/prey pair in each path (with cycles removed from the diet compositions).
3. Results 3.1. Biomass and production of fish During the 1980s, anchovy was the dominant small pelagic fish in the southern Benguela ecosystem (Fig. 2). By the 1990s, the size of the anchovy population had decreased and populations of sardine, redeye, horse mackerel and both species of hake had increased in size (Fig. 3 and Table 1). Summed biomasses of small pelagic fish (anchovy, sardine, redeye, juvenile horse mackerel and other small pelagic fish) increased from 2.62 million tons in the 1980s to 2.80 million tons in the 1990s, i.e. by 7%. Mean annual production by these five small pelagic groups was estimated to be 3.1 million tons in the 1980s and 3.3 million tons in the 1990s, half accounted for by anchovy and sardine.
2.7. Species interactions 3.2. Trophic levels and trophic aggregation Relative impacts of each group on all other groups in the system are quantified using mixed trophic impact analysis, and serve to highlight those groups playing important roles in the system, and those having only small effects on other system components. Mixed trophic impact assessment measures the relative impact of a change in the biomass of one component on other components of the ecosystem (Ulanowicz and Puccia, 1990), and is based on an input –output method for assessing direct and indirect economic interactions, initially applied to the economy of the United States of America (Leontief, 1951). The prey niche overlap index of Pianka (1973) is used to determine the degree of overlap between species utilising common prey resources. A value of 1 indicates complete overlap in shared prey resources, whereas 0 indicates that the predators do not share common prey resources. A similar predator overlap index is used to determine the degree of overlap between species being consumed by common predators, with a similar interpretation of the 0 – 1 range of values. Comparing these varied outputs of the models of the 1980s and 1990s facilitates assessment of the trophic functioning of the southern Benguela ecosystem during two decades dominated by different pelagic fish species.
In Table 1, non-integer trophic levels (TLs) of the 31 living boxes in models of the southern
Fig. 3. Average annual stock sizes (millions of tons) of important fish in the southern Benguela ecosystem during the 1980s and 1990s. Stock sizes of anchovy, sardine and horse mackerel in both decades, and of redeye in the 1980s, were estimated from data and were input to the Ecopath models. Stock sizes of mesopelagic fish, hakes and other demersal fish in both decades, and of redeye during the 1990s, were estimated minimum values (*) required to support consumption by all groups within the system, given estimates of EE which were input to the models (Table 1).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116 Table 3 Biomass (t km 2) and transfer efficiency (%) at each discrete trophic level in models of the southern Benguela ecosystem in the 1980s and 1990s Trophic level
I II III IV V VI VII VIII
Biomass
Transfer efficiency
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proportions went to predation (Fig. 4). Microzooplankton, having a high respiration rate, accounted for the large proportion of throughput going to respiration at TL II.
1980s
1990s
1980s
1990s
3.3. Consumption
83.277 83.959 32.237 16.115 4.878 0.680 0.072 0.006
83.486 88.364 35.193 17.813 5.459 0.790 0.081 0.006
6.5 24.3 22.0 11.3 12.1 9.1 8.1
6.5 24.3 22.0 11.2 11.9 9.2 8.3
Relative consumption by the various groups highlights differences between periods (Fig. 5). In the
Benguela ecosystem during the 1980s and 1990s are tabulated. Small pelagic fish occupy TLs between 3.0 and 4.0, whereas top predators such as seals, seabirds, pelagic-feeding chondrichthyans and apex chondrichthyans are at TLs larger than 4.0 (Table 1). TEs between trophic levels and biomass at each trophic level are almost identical in both decades (Table 3). Small proportions of the throughput at TL II, V, VI, VII and VIII were consumed by predators, whereas at intermediate trophic levels III and IV, larger
Fig. 4. The fate of throughput at each discrete trophic level in the model of the southern Benguela ecosystem in the 1990s, expressed as the percentage of throughput used for respiration, flow to detritus and consumption by predators.
Fig. 5. Relative consumption by fish and top predators estimated by the mass-balanced model of the southern Benguela ecosystem in the 1980s and 1990s.
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fish production. Hake were the dominant consumers of small pelagic fish production, followed by other demersal fish (Fig. 6). Adult horse mackerel, large pelagic fish (including snoek), cephalopods, marine mammals and seabirds all consumed similar proportions of small pelagic fish production (between 8% and 13%). 3.4. Summary statistics and flows Total biomass and many total flows through the southern Benguela upwelling ecosystem were larger in the 1990s model than the 1980s model (Table 4). Average annual catches of small pelagic fish were reduced by 27% and total annual catches were reduced by 18% from the 1980s to the 1990s. Lower net system production (production minus respiration) in the 1990s than in the 1980s (Table 4) is due in part to the 10% increase in biomass of microzooplankton, which have high respiration rates. The southern Benguela ecosystem was less heavily exploited in the 1990s than the 1980s (Table 4)
Table 4 Comparison of summary statistics from models of the southern Benguela ecosystem for the 1980s and 1990s, including % change from 1980s to 1990s 1980s
Fig. 6. Relative consumption of small pelagic fish production by predators, estimated by the mass-balanced model of the southern Benguela ecosystem in the 1980s and 1990s.
1980s, anchovy, redeye and mesopelagic fish consumed the greatest proportions of production. Relative consumption by anchovy decreased in the 1990s, and that by redeye, horse mackerel, mesopelagic fish and sardine increased. Consumption by marine mammals and birds was small in both decades. In models of the 1980s and 1990s, respectively, predators consumed 84% and 88% of small pelagic
1990s
% Change
Total biomass 221 231 +5 (excluding detritus) Sum of all consumption 17 230 18 831 +9 Sum of all exports 2559 1698 34 Sum of all flows to detritus 8771 8496 3 Total system throughput 37 975 39 304 +3 Sum of all production 16 233 16 638 +3 Net system production 2559 1698 34 Sum of all respiratory flows 9416 10 279 +9 Total net primary production 11 974 11 977 <1 Total catches 3.04 2.48 18 Mean trophic level of 4.74 4.80 +1 the fishery Mean path length 3.17 3.28 +3 (Finn, 1976) System overhead 104 304 108 820 +4 Relative ascendancy 21 20 <1 Flows are in t km 2 year 1, biomass and catches in t km 2, system overhead in flowbits (bits t km 2 year 1) and relative ascendancy as %.
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southern Benguela ecosystem during both decades are those of anchovy, large hakes and snoek (Fig. 7). PPR for all fisheries is 4.4% of the total primary production in the 1980s and 4.5% in the 1990s. Catches in the southern Benguela ecosystem were mainly taken from TL III and IV (Fig. 8), corresponding to large transfer efficiencies at these trophic levels (Table 3, TE is the fraction of production either exported from the system, e.g. as catches, or transferred to higher TLs by means of predation). The ratio of PPR by the fisheries to total annual harvest is 290 in the 1990s model, compared to 228 in the 1980s model. This is despite 18% smaller Fig. 7. Modelled primary production required (t km 2 year 1) to sustain catches of commercially important species in the southern Benguela ecosystem during the 1980s and 1990s. Species requiring less than 15 t km 2 year 1 during both decades are omitted.
(a)
although system throughput and biomass were larger in the 1990s model. 3.5. Primary production required to sustain catches The greatest amounts of total primary production required (PPR) to support catches in models of the
Fig. 8. Proportion of catches taken from discrete trophic levels in models of the southern Benguela ecosystem during the 1980s and 1990s.
(b)
Fig. 9. Relative mortality by predation, fishing and other causes in the southern Benguela ecosystem, (a) 1980s and (b) 1990s, calculated using Ecopath.
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Fig. 10. Mixed trophic impacts of selected groups in the southern Benguela ecosystem during the (A) 1980s and (B) 1990s (outputs of Ecopath models). The bars indicate relative net impact (scaled between 0 and 1), where positive impacts are shown above the zero line for each impacting group, and negative impacts below. Impacted groups are arranged along the horizontal axis and impacting groups down the vertical axis.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Fig. 10 (continued).
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In the southern Benguela ecosystem, anchovy, sardine, redeye, other small pelagic fish and juvenile horse mackerel showed large degrees of overlap in both the prey they consumed and in the predators
0.14 0.09 0.26 0.32 0.82 0.85 0.42 0.17 0.45 0.50 0.79 0.79 0.70 0.70 0.92 0.92 0.39
1.00 0.99 0.99 0.96 0.96 0.51 0.96
0.90
0.96
0.90
0.51
1.00 1.00 1.00 0.91 1.00 0.91 1.00 0.50 0.50 1.00 0.50 0.50
0.39
1.00 0.36 0.15 0.13 0.60 0.27 0.48 1.00
0.42
1.00 1.00 1.00 0.21 1.00 0.14 1.00 0.52 0.73 1.00 0.33 0.65
80s 90s 80s 90s 80s 90s 90s
0.66
1.00
90s 80s 90s 80s 90s 80s 90s 80s 90s 90s
80s
1.00 0.90 0.57 0.63
80s 80s
Other small pelagics Redeye
1.00 0.67 0.55 0.50
Redeye Anchovy Sardine Anchovy
Juvenile horse mackerel
Predator overlap index
3.8. Predator and prey niches
Prey overlap index
The reduction in anchovy biomass and the increase in abundance of sardine in the 1990s is reflected in their relative net impacts on predatory fish such as snoek and other large pelagic fish, seabirds, seals and cetaceans (Fig. 10). In the 1990s, redeye was abundant and had a positive modelled impact on marine mammals. In this decade, the chub mackerel stock included large fish that have a more piscivorous diet than smaller chub mackerel. A quarter of the diet of chub mackerel consisted of mesopelagic fish in the 1990s model and this is reflected in the positive impact of mesopelagic fish on chub mackerel (Fig. 10B). Fishing had larger negative impacts on sardine in the 1980s than in the 1990s, when sardine biomass was larger.
Group
3.7. Mixed trophic impacts
Table 5 Predator and prey overlap indices for the five groups of small pelagics and mesopelagic fish in the southern Benguela ecosystem
Relative mortalities attributed to fisheries, predation and other causes are shown in Fig. 9. Modeled mortality is largest in the cephalopod and small hake groups, particularly caused by heavy predation. Of the total natural predation on hakes in the southern Benguela ecosystem model for the 1980s, 32% was through cannibalism, 27% of hake production was eaten by cephalopods and 12% went to seals. In the 1990s model, cannibalism made up 40%, predation by cephalopods accounted for 24% and seals consumed 11%. Total catches of hakes amounted to 12% and 11% of hake production in the 1980s and 1990s, respectively. Fishing mortality of sardine and juvenile horse mackerel increased over the two decades, whereas anchovy fishing mortality was reduced in the 1990s.
1.00 0.59 0.99 0.92
3.6. Mortality
1.00 0.59 0.99 0.92
Other small pelagics
total annual catches during the 1990s. In the 1990s model, the proportion of the catch in discrete trophic levels IV, V and VI is slightly larger than in the 1980s (Fig. 8).
Anchovy Sardine Redeye Other small pelagics Juvenile horse mackerel Mesopelagic fish
Juvenile horse mackerel
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Sardine
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that consumed them (Table 5). These five small pelagic fish groups showed identical prey overlaps in the 1980s and 1990s because diet compositions of these groups are assumed constant between the two decades. However, there were greater overlaps in shared predators of small pelagic fish during the 1990s than the 1980s (Table 5). This may be related to the smaller total catches in the 1990s than the 1980s (Table 4) and the 13% increase in biomass of small pelagic fish predators (large pelagic fish, hakes, seabirds, seals and cetaceans) from the 1980s to the 1990s.
4. Discussion Given the variable accuracy and precision of the different data series used to estimate input parameters for the models, and the constraints of periods and areas for which data were available, there is uncertainty associated with the model outputs. For example, coefficients of variation (CV) of spawner biomass hydro-acoustic surveys from 1985 to 1997 ranged between 12% and 33% for anchovy and between 21% and 55% for sardine (Barange et al., 1999). Similarly, CVs of spring biomass estimates for horse mackerel from bottom trawling ranged between 21% and 30% and from hydroacoustic surveys, between 17% and 50% (Barange et al., 1998). Therefore, careful interpretation is required of differences in model summary statistics between the 1980s and 1990s. Shannon (2001) investigated sensitivity to parameterization of models of the southern Benguela ecosystem in the 1980s and 1990s. Overall, results of sensitivity analyses, analyses of possible combinations of parameters for which models are balanced and investigations using alternate parameter values show that the models are constrained, with little scope for allocating parameter values far from those considered to be best estimates. Model structure forces constraints on parameter values, even those that are poorly known. Therefore, there are a limited number of possible combinations of parameters describing this ecosystem, making quantifiable aspects of the model more believable (for example, larger sardine M used in the ecosystem models of this study than in stock assessment models).
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4.1. Zooplankton The minimum required zooplankton biomass (summed micro-, meso- and macrozooplankton biomass) was estimated to be 10% larger in the 1990s than that input to the 1980s model (Table 1). This increase in zooplankton biomass is consistent with observed increases in abundance in the region of St. Helena Bay, on the west coast of South Africa (Verheye and Richardson, 1998; Verheye et al., 1998). Between 1951 and 1996, zooplankton abundance increased by at least an order of magnitude in all size classes. The biomass of copepods (including some large calanoid copepods that are macrozooplankton) increased by about 60% between the late 1980s and 1995/1996 (Verheye et al., 1998). Verheye et al. (1998) concluded that there has been a longterm change in the food environment of small pelagic fish in the southern Benguela since the 1950s. Because the model biomass of zooplankton and the stocks of small pelagic fish were larger in the 1990s than in the 1980s, there was more food available to their model predators during this decade. This, and the larger catches of small pelagic fish in the 1980s, meant that the southern Benguela model ecosystem was more tightly constrained by predators (including the fishery) and availability of food in the 1980s than in the 1990s. Tight constraints are also reflected in the larger individual ecotrophic efficiencies of most fish groups in the 1980s compared to those in the 1990s (Table 1). 4.2. Hakes Hake biomass indices from surveys (Badenhorst and Smale, 1991) are greater than biomass estimated by the production model (Leslie, 1996). Further, it is likely that hake biomass exceeds the survey indices because untrawlable ground is not covered and small, pelagic hake may be missed. Therefore, it is expected that biomass, in particular that of small hake, is larger than stock assessment production model estimates. Accordingly, because the Ecopath models showed that production of small hake was insufficient to support the consumption by large hake and other predators, the required biomass of small hake was estimated, assuming an ecotrophic efficiency (proportion of production con-
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sumed or exported from the system) of 99.9%. Models showed that minimum required biomass of hake was 34% (1980s) and 22% (1990s) more than the production model index. The additional biomass was in the small hake classes and is not necessarily inconsistent with results from production models because juvenile mortality is likely to be underestimated, therefore also underestimating biomass (R.W. Leslie, Marine and Coastal Management, pers. comm.). 4.3. Biomass and production of fish Shannon and Field (1985) estimated that a maximum biomass and annual production of 2 million tons of small pelagic fish could be supported in the southern Benguela ecosystem. Accounting for the smaller area (Orange River to Cape Agulhas) considered by Shannon and Field (1985), and their use of a lower conversion ratio from carbon to wet mass, our estimates of 3.1 and 3.3 million tons are remarkably similar to this. Moloney and Field (1985) estimated that 25% of pelagic fish production off southern Africa is exploitable by humans. This is equivalent to 775 000 t year 1 in the 1980s and 825 000 t year 1 in the 1990s. However, Moloney and Field (1985) did not recommend full exploitation of pelagic fish production because areas such as the Agulhas Bank are important for spawning pelagic fish and are likely to be important buffers against the large catches made off the west coast of South Africa. Total annual catches of the five small pelagic fish groups were larger in the 1980s (430 100 t, i.e. 14% of total small pelagic fish production) than in the 1990s (312 400 t, i.e. 9% of total small pelagic fish production). The opposite was the case for predatory snoek; annual catches rose from 11 000 to 18 000 t over the last decade (Table 1). Groups such as mesopelagic fish and redeye are not caught in large quantities in the southern Benguela ecosystem. However, these groups play a potentially large role in the trophic functioning of the southern Benguela ecosystem by providing food for other species. For example, the model estimates suggest that hake consumed 1.1 million tons of mesopelagic fish during the 1990s. This far exceeds earlier estimates by Payne et al. (1987) and Bergh et al. (1985), and is in agreement with Armstrong and Prosch’s
(1991) conclusion that annual consumption of lightfish in the southern Benguela ecosystem is considerably larger than initially thought. 4.4. Trophic levels and trophic aggregation Trophic levels of seals and cetaceans are in the upper part of the range reported by Pauly et al. (1998a) for these groups, indicating that they are feeding fairly high in the southern Benguela food web. Differences in availability of prey in the 1980s and 1990s meant that top pelagic predators were forced to consume larger quantities of prey lower in the food web during the 1990s, leading to marginally reduced trophic levels in the 1990s model for M. capensis, seabirds and cetaceans, which prey on small pelagic fish. This is explained by sardine (trophic level of 3.0) becoming more abundant and anchovy (trophic level of 3.5) decreasing from the 1980s to the 1990s. These differences are surprisingly small, being buffered by the increase in the contribution of redeye to the diets of cetaceans and seabirds in the 1990s model. Redeye occupies a higher trophic level than anchovy and sardine, at 3.6. Heavy fishing on large chub mackerel during the late 1970s and 1980s left a population in the 1980s dominated by young fish that are largely zooplanktivorous. By the 1990s, the population structure had recovered, with large chub mackerel eating mostly fish, this being indicated by their slightly higher trophic level (Table 1). Analysis of 50 models of estuarine and marine ecosystems showed that in general, the mean TE between TLs is approximately 10%, although variance is large (Christensen and Pauly, 1995). In upwelling ecosystems, TEs are generally lower than this (Jarre-Teichmann, 1992; Christensen and Pauly, 1993; Jarre-Teichmann and Pauly, 1993; Jarre-Teichmann and Christensen, 1998). This is true for flows through TL II (consumption of phytoplankton by microzooplankton) in the southern Benguela ecosystem (Table 3). Only 55% and 60% of net primary production is consumed by herbivores in the southern Benguela ecosystem during the 1980s and 1990s, respectively. Although larger than the 39% estimated previously (Baird et al., 1991), these efficiencies are still much smaller than those in the Peruvian upwelling system and may be explained by the mismatch in
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space and time between phytoplankton blooms and zooplankton production (Baird et al., 1991). Results agree with the work of Shannon and Field (1985), who estimated that 44– 73% of phytoplankton production was not consumed by zooplankton or fish. Because of the nature of the pulsed upwelling events in the southern Benguela ecosystem, the migration of pelagic fish through the system, and because some phytoplankton are of unsuitable quality or size, pelagic fish are probably only able to utilise about 12.5% of primary production in the system (Shannon and Field, 1985). Walker and Peterson (1991) estimated that copepods consume between 12% and 42% of primary production along the productive west coast of South Africa. By comparison, this study of the southern Benguela sub-system, covering a larger region and including the productive upwelling regions along the west coast as well as the less productive Agulhas Bank and south coast areas, shows that mesozooplankton consume only 4– 5% of primary production and that microzooplankton consumed 49% and 53% of total modelled primary production in the 1980s and 1990s, respectively. In their preliminary carbon budget for the southern Benguela ecosystem, Walker and Peterson (1991) estimated that 75% of phytoplankton production was lost from the euphotic zone as detritus. By comparison, models suggest that only 45% and 39% of phytoplankton production is lost in the form of detritus and sedimentation from the southern Benguela ecosystem during the 1980s and 1990s, respectively. This may suggest more efficient use of phytoplankton than previously thought. Transfer of biomass at TL III – V appears to be more efficient in the southern Benguela ecosystem than in other upwelling ecosystems (Jarre-Teichmann et al., 1998). The geometric mean TE of biomass for TL II – IV in the southern Benguela system was 15.1% in both decades. TEs at each TL are all greater than means estimated by Christensen and Pauly (1995) for upwelling ecosystems. These large values indicate a ‘‘bottleneck’’ of flows at the levels of zooplankton (TL II and III) and small pelagic fish (TL III and IV), pointing to the groups as being important in the overall trophic structure of the ecosystem. The high TEs also indicate that the southern Benguela ecosystem may be foodlimited. This is in agreement with the suggestion by Shannon and Field (1985) that at large stock sizes,
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anchovy and sardine may be food-limited in the southern Benguela ecosystem. During both the 1980s and 1990s, the geometric mean transfer efficiency for TL II – VIII (containing biomass >0.0005 t km 2) was 12.0%, close to Baird et al.’s (1991) estimate of 12.1%. Biomass was concentrated in trophic levels I and II, i.e. the producer (phytoplankton) and detritus level (TL 1) and the primary consumer (microzooplankton) level (Table 3). This is true of many ecosystems such as coral reefs (e.g. Alino et al., 1993; Opitz, 1993), coastal regions (e.g. De Paula E Silva et al., 1993; Vega-Cendejas et al., 1993), shelf ecosystems (e.g. Arrenguin-Sanchez et al., 1993) and other upwelling systems (e.g. Jarre-Teichmann and Christensen, 1998). 4.5. Consumption of small pelagic fish Modelled consumption of anchovy by hake amounted to 70% of the anchovy caught during the 1980s. This differs from Field et al.’s (unpublished) estimate that hake consumed twice the quantity of anchovy taken by the fishery during the 1980s. Estimates of diet and stock sizes of many of the model groups have been revised since Field et al.’s (unpublished) preliminary model, accounting for the differences between their results and those presented here. This points out sensitivity of results to best estimates that may not be accurate. The small proportion of small pelagic fish production consumed by seabirds (8%) in the southern Benguela ecosystem is at the top of the 5– 8% range estimated for seabirds in the North Sea (Bailey, 1986), and much less than the 20 –30% estimate of Furness (1982) and MacCall (1990) for seabirds in other upwelling systems. Of the 9% of small pelagic fish production that is consumed by marine mammals, consumption by seals accounted for twothirds of this, reconfirming Bergh et al.’s (1985) suggestion that whales and dolphins currently play a small trophic role in the southern Benguela ecosystem. 4.6. Summary statistics and flows In previous studies, five upwelling systems, including the southern Benguela during the 1980s, were ranked according to primary production, biomass,
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system throughput and catches, all measures of ecosystem size (Jarre-Teichmann and Christensen, 1998; Jarre-Teichmann et al., 1998). In terms of biomass and throughput, the southern Benguela system was most similar to the Peruvian system during the 1970s, after the collapse of the Peruvian anchovy Engraulis ringens fishery. The southern Benguela ecosystem ranked between the Peruvian and northern Benguela systems in terms of primary production (Jarre-Teichmann et al., 1998). However, the southern Benguela ecosystem was larger in biomass and catches, had a higher total system throughput and was more productive than the Californian system (Jarre-Teichmann et al., 1998). Ware (1992) estimated that the catch efficiency (catch divided by primary production) on the South African west coast was larger than that for the Californian ecosystem. This suggests that although primary production is not efficiently utilised in the southern Benguela ecosystem, the Californian ecosystem is even less efficient, probably because of its sizeable alongshore extent and the consequent large losses of primary production through offshore transport (Ware, 1992). Mean path lengths estimated in this study are longer than the path length of 2.54 in the Benguela model of Baird et al. (1991), showing that at least some summary statistics are to a certain degree dependent on model structure. In the models of the southern Benguela ecosystem, the maximum number of steps from primary producer to top predator (chain length) is 10. By comparison, a maximum chain length of eight was reported for upwelling and oceanic systems, whereas paths in models of some shelf and coastal systems were longer (Christensen and Pauly, 1993). However, none of the models they considered explicitly included several zooplankton boxes, notably microzooplankton. Maximum chain length of the southern Benguela models is large because not only do the models include the upwelling zones along the west coast, they also extend over the Agulhas Bank region. Even longer maximum chain lengths would be expected if planktonic groups were considered in more detail in models of the southern Benguela ecosystem. Considering the work of Odum (1969) on the development of ecosystems, Christensen (1995) found that system overhead, which reflects the potential of a system to increase its ascendancy to meet unexpected perturbations, is positively correlated with maturity
and is a possible measure of stability. Relative ascendancy is dimensionless, excludes the influence of system throughput on both terms, and therefore it is considered to be a suitable measure for comparing different ecosystems (Christensen, 1995; Field et al., 1989a,b). Relative ascendancy was previously estimated to be 51% in the Benguela ecosystem (Baird et al., 1991). In this study, relative ascendancy is less than half this during both decades (Table 4). This result is more in line with the findings of JarreTeichmann (1992) for the Peruvian upwelling system, where relative ascendancy varied around 30%, and relative overhead around 70%. The Peruvian system shows characteristics of a typical upwelling system (Jarre-Teichmann et al., 1998) in that it is even less stable (‘‘mature’’) than the southern Benguela system, with a lower relative overhead (70% for the Peruvian system vs. 80% for the southern Benguela system). Relative overhead values for the models of upwelling systems compared in Jarre-Teichmann (1998) ranged from 63% to 70% and support this interpretation, although it should be viewed with some caution given the differences in model structure. In a model with a very different structure, focussed on trophic interactions in the benthic community of the Antarctic eastern Weddell Sea shelf, Jarre-Teichmann et al. (1997) found a relative overhead of 77%, and suggested that this was a characteristic indicating stability of the system to external perturbations—in this particular case, scraping of the bottom by icebergs in combinations with low turnover rates (caused by low temperature). 4.7. Primary production required to sustain catches Primary production equivalents are used to compare effects of fishing at different trophic levels (Pauly and Christensen, 1995). For example, harvesting of fish at low trophic levels is ecologically less expensive than fishing at a higher trophic level, given the inefficient transfer of energy up the food web. Primary production equivalents required to sustain catches in the southern Benguela ecosystem are small proportions (4%) in comparison to the Peruvian system (13 – 15%), and less than half the 9.5% mean for the seven upwelling systems examined by Jarre-Teichmann and Christensen (1998). They are more in line with percentages required to sustain catches in open ocean
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
(small primary production and catch densities) or coastal regions (large primary production and catches) than in other upwelling systems or shelf systems (Pauly and Christensen, 1995). Jarre-Teichmann and Christensen (1998) explained the discrepancy between their mean PPR for upwelling systems with the mean of 25% estimated by Christensen and Pauly (1995); the latter authors considered the 1990s, when there were large catches (especially in the southeastern Pacific), and assumed primary production equal to that in the 1980s, whereas Jarre-Teichmann and Christensen (1998) focussed on the 1970s and early 1980s in their study, when catches were smaller. Further, Christensen and Pauly (1995) included discards in their estimates, whereas Jarre-Teichmann and Christensen (1998) used nominal catches. Discards were not included in southern Benguela models of this study. Catches in the southern Benguela ecosystem are small in comparison to other upwelling systems, and primary production is larger than that of the northern Benguela, northwest African and Californian upwelling systems (Jarre-Teichmann et al., 1998). In addition, fishing in the southern Benguela ecosystem takes place at low trophic levels, with the overall result that the percentage PPR to sustain catches is small. The mean trophic level of the fishery increased slightly from the 1980s to the 1990s (Table 4) because a larger proportion of the catch in the 1990s was of snoek and hakes, which occur at higher trophic levels than small planktivorous fish. Therefore, in the southern Benguela pelagic ecosystem, we do not appear to be ‘‘fishing down the food web’’ as has been shown for many regions (Pauly et al., 1998b, 2000a,b). The mean trophic level of the fishery in upwelling systems in 1988 –1991 is 3.8 (Pauly and Christensen, 1995). This is lower than that in the southern Benguela ecosystem (Table 4) where not only small pelagic fish but also hake and snoek are targeted. By comparison, the mean trophic level of the fishery off Peru was 3.5 in the 1960s when anchovy was targeted, and 3.7 in the 1970s when more sardine and hake were caught (Jarre-Teichmann, 1998). 4.8. Fishing mortality It has been estimated that the total finfish biomass consumed globally by finfish is three times larger than
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the global catches of finfish (Christensen, 1996). A generalisation from more than 50 models of aquatic ecosystems is that catches are much smaller than the production consumed by predators, even in heavily exploited systems (Bax, 1991; Jarre et al., 1991; Christensen and Pauly, 1995). This is in agreement with Moloney and Field’s (1985) assumption that humans are able to exploit not more than 25% of pelagic fish production off South Africa. For most species in the southern Benguela ecosystem, fishing mortality is much smaller than predation mortality (Fig. 9). Exceptions are predators such as snoek, other large pelagic fish and large M. paradoxus, for which fishing mortality is estimated to be similar or larger than predation mortality (Fig. 9). In the 1970s, fishing mortality for hake in the Peruvian, Namibian and northwest African upwelling systems was similar to natural mortality (Jarre-Teichmann and Christensen, 1998). Equal portions of the total hake production in the southern Benguela ecosystem go to the fishery and to seals, in contrast to the initial estimate of Field et al. (unpublished) that seals take only 22% of the amount of hake caught in the fishery. The mean size of hake eaten by seals is 21 cm, smaller than 25 cm, the minimum length of hake taken by the fishery (David, 1987). Taking into account seal mortality related to fishing vessels, the net benefit of the fishery to seals is that 2 –5% of the seal population is being ‘‘supported’’ by the fishing industry on a year-round basis (David, 1987). However, only 0.3% of total consumption by seals is of fish scavenged during fishing operations (Wickens et al., 1992). Most of the hake eaten by seals are consumed naturally or scavenged when discarded by trawlers. The anchovy fisheries in the southern Benguela and Peruvian ecosystems show similarities. For anchovy, the ratio of natural mortality (predation and other mortality) to fishing mortality in the southern Benguela ecosystem was 2.97 in the 1980s and 4.22 in the 1990s. These mirror the ratios of 2.38 and 4.10 for anchovy in the Peruvian system during the 1960s, when there was a large fishery for anchovy, and the 1970s, after the collapse of the anchovy fishery (JarreTeichmann and Christensen, 1998), highlighting the competition for anchovy between its natural predators and the fishery. Off Peru, specialised anchovy predators (cormorants) have decreased with increased fish-
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ing (Tovar et al., 1987). Off South Africa, low anchovy abundance negatively affected the breeding of African Penguins, Cape Cormorants and Swift Terns (Crawford and Dyer, 1995). However, this is not because fishing pressure on anchovy increased, but because anchovy abundance decreased, reflecting the extent to which some predators rely upon particular prey species. In contrast, many species are opportunistic, taking advantage of any available prey (Crawford et al., 1987). The specialists are the ones that are at risk from overfishing and natural fluctuations in prey abundance. 4.9. Functioning of the southern Benguela ecosystem in the 1980s and 1990s Some differences have been shown between the anchovy-dominated system of the 1980s and the 1990s when sardine biomass increased. For example, many flows through the southern Benguela ecosystem are larger in the 1990s model (Table 4). However, owing to the large uncertainty around model input parameters, some of these differences (such as those less than 10%) may not be representative of change from the 1980s to the 1990s. For example, production of small pelagic fish only differs by 7% between decades, which may be negligible given the coefficients of variation between 12% and 55% for anchovy and sardine biomass surveys (Barange et al., 1999). Overall differences between the trophic models are not as large as expected from the differences in biomass and catches of many species. Trophically, the southern Benguela ecosystem seems to have functioned in a similar way during both decades, as shown by the similarity in transfer efficiencies, biomass per trophic level, mixed trophic impacts and relative ascendancy. This is in line with results from comparisons of models of upwelling systems, where the systems tend to group by ‘‘sys-
tem’’ rather than by decade or dominance regime (Jarre-Teichmann and Christensen, 1998). Biomass and catches of the small pelagic fish component of the southern Benguela ecosystem differ between the two periods. However, model production by small pelagic fish is close to 3 million tons in both decades, at least partly because it has been maintained at this level through careful management of the pelagic fisheries. Further, the combined model ecotrophic efficiency of small pelagic fish (calculated as the ratio of the sum of catches and their consumption by predators to production by the group) is constant over the two decades (0.977 in 1980s and 0.976 in 1990s). In addition, the proportion of small pelagic fish production consumed by predators is similar in the two decades modelled. The apparently small differences between the generalised trophic structure of the anchovy- and sardine-dominated ecosystems suggest some degree of trophic similarity of small pelagic fish in the southern Benguela ecosystem; it is likely that in this system, small pelagic fish species are trophically interchangeable to a certain extent.
Acknowledgements We are very grateful to many scientists in the region for assistance with, provision of and discussions about data used in our models. We would like to thank Mrs Cathy Boucher for preparing Figs. 1 and 10 for use in this paper.
Appendix A Sources of data used to estimate input parameters and diets for southern Benguela Ecopath models (Tables A.1 –A.10).
Table A.1 Plankton: input data for southern Benguela Ecopath models Original value
Source
Value used
Comments
Phytoplankton B
1.2 106 t C
P/B
133.3 year 1
Brown et al., 1991 used conversion factor of 14.25 for C:wet mass Brown et al., 1991
154.4 year 1
Sedimentation
368.4 t km 2 year 1
Pitcher et al., 1991
Primary production in Brown et al. (1991) increased by 18% to account for particulate dissolved organic C (1989 workshop). Sedimentation estimated to be 3.7% of daily production (Pitcher et al., 1991).
Microzooplankton (2 – 200 lm equivalent spherical diameter; nanoflagellates, ciliates, zooplankton larvae) B 5.525 t km 2 Jarre-Teichmann et al., 1998, Estimated Using Ecopath, estimated B required in 1980s and 1990s. from Brown et al. (1991) and P/B 482 year 1 Painting et al. (1992); used conversion factor of 14.25 for C:wet mass P/Q 20% Calculated from U and respiration/Q in 25% Jarre-Teichmann et al., 1998 Painting et al., 1992 U 20% Stoecker, 1984 Mesozooplankton (200 – 2000 lm; copepods, in particular Calanoides carinatus and Calanus agulhensis) B 187 600 t C Hutchings et al., 1991 Estimated Using Ecopath, estimated B required during each decade. P/B 20 year 1 Hutchings et al., 1991 40 year 1 P/Bs estimated from Verheye et al. (1992) were larger, between 30 and 91 year 1. P/Q 30% Omori and Ikeda, 1984 U 35% Verheye et al., 1992; Probyn et al., 1990, 11 – 50% of food consumed by South African copepods is Probyn, 1992; H. Verheye, egested as faecal pellets. As in Jarre-Teichmann et al. (1998), MCM, pers. comm. U was estimated to be 35%. Macrozooplankton (2 – 20 mm; mainly euphausiids (on which most of the macrozooplankton estimates are based), but also includes groups such as amphipods and fish larvae) B 63 600 t C Hutchings et al., 1991 Estimated Using Ecopath, estimated B required during each decade. P/B 13 year 1 Hutchings et al., 1991 P/Q 41% Hutchings et al., 1991 U 35% Jarre-Teichmann et al., 1998 20% Assimilation efficiency of euphausiids is closer to 80% H. Verheye, MCM, pers. comm. Gelatinous Zooplankton (Cnidaria, Ctenphora, tunicates, chaetognaths) B 55 106 t A.J. Boyd, MCM, pers. comm. P/B P/Q U
0.584 year 1 35% 20%
Jarre-Teichmann et al., 1998 H. Verheye, MCM, pers. comm. Purcell, 1983
106 t
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Parameter
Biomass more likely in the range of 10 – 50% of combined meso- and macro-zooplankton biomass (L. Hutchings, MCM, pers. comm.). This is from gross efficiency of chaetognaths and siphonophores. This is from assimilation efficiency of siphonophores. 103
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Table A.2 Small pelagic fish: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Armstrong et al., 1991
1147 500 t 786 143 t
1984 – 1989 acoustic estimate, Barange, 1997. 1990 – 1996 acoustic estimate, Barange, 1997. Data for northern Benguela, agrees with South African estimate (J. De Oliveira, MCM, pers. comm.).
129 000 t 460 000 t 1.2 year 1
1984 – 1989 acoustic estimate, Barange 1997. 1990 – 1996 acoustic estimate, Barange 1997. From P/B = Z = F + M, P/B of South African sardine estimated to be 1.2 year 1 (1980s) and 1.0 year 1 (1990s). However, to account for larger increase in B in 1990s (Barange, 1997), P/B was assumed equivalent in both decades, i.e. 1.2 year 1. Q/B lies within the range estimated from Van der Lingen’s (1998) daily rations for sardine.
P/B
1.2 year 1
Hewitson and Cruickshank, 1993
Q/B
12.3 year 1
Armstrong et al., 1991
Sardine (Sardinops sagax) B 146 000 t
Armstrong et al., 1991
P/B
1.1 year 1
Hewitson and Cruickshank, 1993, Northern Benguela
P/Q
9.7%
Armstrong et al., 1991
Redeye (Round herring; Etrumeus whiteheadi) B 1980s 1 222 000 t Roel and Armstrong, 1991 B 1990s
P/B P/Q
1.2 year 1 10%
Estimated
Minimum estimate from acoustic surveys (1986, 1987, 1989). Likely that redeye B was larger, particularly in 1990s (L. Hutchings and C. van der Lingen, MCM, pers. comm.). Therefore allowed Ecopath to estimate B required in 1990s. Assumed similar to P/Bs of anchovy and sardine. Assumed similar to other clupeoids (Jarre-Teichmann et al., 1998).
Other small pelagic fish (saury (Scomberesox saurus), flying fish (Exocoetidae), pelagic goby (Sufflogobius bibarbatus)) B 80 000 t 1989 Workshop B assumed constant in 1980s and 1990s. P/B 0.9 year 1 1989 Workshop 1.0 year 1 Assumed closer to P/B of anchovy, sardine and redeye. P/Q 10% Assumed similar to other clupeoids (Jarre-Teichmann et al., 1998).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Cape anchovy (Engraulis capensis) B 1106 000 t
Table A.3 Horse and chub mackerel: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Large (>20 cm) horse mackerel (Trachurus trachurus capensis) B 1980s 356 000 t 1980s: B on south coast (1975 – 1983) B 1990s 426 240 t estimated from Kinloch et al.’s (1986) VPA analysis and Kerstan and Leslie’s (1994) length – mass relation. 1990s: Based on Barange et al. (1998). P/B 0.52 year 1 Jarre-Teichmann et al., 1998 Q/B 5.1 year 1 Jarre-Teichmann et al., 1998 U 30% Chub mackerel (Scomber japonicus) B 1980s 62 500 t B 1990s 100 000 t P/B 1980s 0.6 year 1 P/B 1990s
0.5 year 1
P/Q U 1980s U 1990s
10% 25% 20%
Crawford, 1989; Crawford et al., 1983; Jarre-Teichmann et al., 1998 Assuming fish were smaller in 1980s after collapse of stock P/B assumed similar to other predatory fish (snoek)
Comments
Assumed similar to P/Bs of anchovy and sardine. Assumed similar to Q/Bs of anchovy and sardine. Juveniles are zooplanktivorous.
B on west coast is five times smaller than on south coast (Barange et al., 1998).
1.0 year 1 10 year 1
0.9 year 1 0.8 year 1
Calculated from larger Q/B with P/Q at 10%. Q/B larger from daily rations in Pillar and Barange (1998). Large horse mackerel eat zooplankton and fish.
B in 1990s estimated to be that prior to heavy exploitation in the 1970s, i.e. that in Crawford, 1989. P/B = 0.89 year 1 used off North West Africa (Jarre, DFU, pers, comm. based on F = 0.49 and M = 0.4 year 1). If P/Q = 10%, Q/B likely exceeds 5 – 6 year 1 considering daily ration (Hatanaka et al., 1957, in Livingston and Goiney, 1984).
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Small ( < 20 cm) horse mackerel (Trachurus trachurus capensis) B 1980s 44 000 t Estimated from unpublished data, B 1990s 106 560 t Marine and Coastal Management. P/B 1.2 year 1 Q/B 12 year 1 U 35%
Assumed Heavy exploitation left more small, zooplanktivorous fish in 1980s, whereas by 1990s fish were larger (piscivorous).
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Table A.4 Other large pelagic fish: input data for southern Benguela Ecopath models Parameter Snoek (Thyrsites B 1980s B 1990s P/B P/Q U
Original value atun) 52 700 t ? 0.5 year 1
Value used
Comments
Penney et al., 1991a
52 700 t Estimated
Similar estimate for 20% exploitation rate (L. Hutchings, MCM, pers. comm.). Larger catches in 1990s, reflect increased B? Ecopath estimated B required in 1990s. P/B = Z = F + M, where M assumed same as chub mackerel (O. Centurier-Harris, formerly MCM, unpublished data) and barracuda (Opitz, 1991), F calculated from catches. Assumption. Following Winberg, 1956, snoek assumed to be efficient predators.
10% 20%
Penney et al., 1991a Penney et al., 1991a
No indication of change in B in 1990s, B constancy assumed. Combined P/B calculated by weighting according to relative Bs. Geelbek P/B estimated from Z = F + M using Griffiths (1995) and Griffiths and Hecht (1995). Tuna P/B estimated from M using Pauly (1980) and Laurs and Wetherall (1981) and F using Penney et al., 1991a. Considered P/Q = 5% for tuna, 10% for others. Tuna P/Q corresponds to Q/B within Palomares and Pauly’s (1998) estimated range. Large pelagic fish assumed efficient predators.
20%
Table A.5 Cephalopods and mesopelagic fish: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Cephalopods B
40 000 t
1989 Workshop
300 000 t
P/B
1.5 year 1
Jarre-Teichmann et al., 1998
3.5 year 1
P/Q
10%
Jarre-Teichmann et al., 1998
35%
Maximum B index for chokka squid is 100 000 t (Lipinski, 1992). B of cephalopods assumed to be three times B of chokka alone. Larger P/B required to obtain P of 1 million t estimated by Bergh et al. (1985). Their P is an order of magnitude larger than if P/B = 1.5 year 1. At lower limit of range estimated by O’Dor et al. (1980, in Livingston and Goiney, 1984).
U
20%
Mesopelagic fish (Lanternfish lampanyctodes hectoris and lightfish maurolicus muelleri) B 1 – 2.4 106 t Armstrong and Prosch, 1991; Estimated Armstrong et al., 1991 P/B 1.2 year 1 Hewitson and Cruickshank, 1993 P/Q 10% U 35%
Ecopath used to estimate actual B required in each decade (fell within indicated range) Assumed similar to P/Q of anchovy Assumed same as U of other zooplanktivorous fish
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Other large pelagic fish B 28 775 t Group P/B 0.48 year 1 Kob 0.36 year 1 Yellowtail 0.53 year 1 Geelbek 0.88 year 1 Tuna 0.47 year 1 P/Q 5.6 year 1 U
Source
Table A.6 Hake: input data for southern Benguela Ecopath models Original value
Source
Value used
Comments
Small M. capensis B 1980s B 1990s
65 457 t 73 752 t
Estimated Estimated
Ecopath used to estimate B required in both decades
P/B
1.2 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998, similar to small pelagic fish
2.0 year 1
Bergh et al. (1985) estimated hake P/B = 4.8 year 1 given rapid turnover of small hake. P/B increased for Ecopath model.
P/Q U
15% 35%
Jarre-Teichmann et al., 1998
Large M. capensis B 1980s B 1990s
181 036 t 247 909 t
P/B
0.6 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998
0.8 year 1
P/Q U
25% 20%
Jarre-Teichmann et al., 1998
18%
Small M. paradoxus B 1980s B 1990s
226 866 t 290 249 t
P/B
1.2 year 1
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998, similar to small pelagic fish
P/Q U
15% 35%
Large M. paradoxus B 1980s 150 553 t B 1990s 234 646 t P/B P/Q
0.6 year 1 25%
U
20%
Assumed similar to other zooplanktivorous fish
P/B and P/Q adjusted so that Q/B = 4.4 year 1, estimated from daily ration of large M. capensis in Punt and Leslie, 1995 Assumed similar to other predatory fish
Estimated Estimated
Ecopath used to estimate B required in both decades
2.0 year 1
Bergh et al. (1985) estimated hake P/B = 4.8 year 1 given rapid turnover of small hake. P/B increased for Ecopath model.
Jarre-Teichmann et al., 1998
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Parameter
Assumed similar to other zooplanktivorous fish
Estimated from unpublished data and model outputs, Marine and Coastal Management Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
0.8 year 1 17%
P/B and P/Q adjusted so that Q/B = 4.7 year 1, estimated from daily ration of large M. paradoxus in Punt and Leslie, 1995 Assumed similar to other predatory fish 107
108
Table A.7 Other demersal fish and chondrichthyans: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments
Pelagic-feeding chondrichthyans B 128 000 t P/B Q/B U
0.5 year 1 4.5 year 1 20%
Chondrichthyan B estimated to be 330 000 t (Jarre-Teichmann et al., 1998). Pelagic-feeders estimated to comprise 40% of B excluding apex predators. Assumed similar to other large pelagic fish. Similar to Q/B for dogfish (Livingstone and Goiney, 1984) and sandbar shark (Stillwell and Kohler, 1993). Assumed similar to other predatory fish and carnivores.
Benthic-feeding chondrichthyans B 192 000 t P/B 1.0 year 1 P/Q 10% U 20%
Estimated to comprise 60% of B excluding apex predators. Assumed similar to P/B of demersal fish. Assumption. Assumed similar to other predatory fish and carnivores.
Apex predatory chondrichthyans B 10 000 t P/B 0.5 year 1 P/Q 10% U 20%
Assumed to comprise 3% of total chondrichthyan B. From Z of great white sharks off South Africa (Cliff et al., 1996). Assumption. Assumed similar to other predatory fish and carnivores.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Pelagic- and benthic-feeding demersal fish (P/B, P/Q and U are assumed to be the same for both groups) B 230 000 t for all Japp et al., 1994, Estimated Using Ecopath, B of each group estimated each decade. demersals 1989 workshop P/B 1.0 year 1 Jarre-Teichmann P/B estimated for Q/B = 5 year 1, in middle of range estimated by Palomares and Pauly (1988) for et al., 1998 flatfish, and double that for more sedentary kingklip (MacPherson, 1983). P/Q 20% Assumed similar to large hake; within range estimated for flatfish (Livingstone and Goiney, 1984). U 20% Assumed similar to large hake.
Table A.8 Marine mammals and birds: input data for southern Benguela Ecopath models Parameter
Original value
Source
Value used
Comments Counts of pups from 1971 to mid-1990s do not show overall increase in seals off South Africa, therefore B assumed constant.
P/B Q/B
0.946 year 1 19.3 year 1
U
20%
Cetaceans B 1980s
16 200 t
B 1990s P/B Q/B
18 000 t 0.6 year 1 7.5 – 10 year 1
1989 Workshop Jarre-Teichmann et al., 1998
U
21%
Gaskin, 1982
Seabirds B 1980s B 1990s P/B Q/B U
3257 t 2616 t 0.123 year 1 118 year 1 26%
Crawford Crawford Crawford Crawford Crawford
1989 Workshop Estimated from Balmelli and Wickens’ (1994) Q estimate, Butterworth et al.’s (1988) mean weight and Wickens et al.’s (1992b) abundance estimate. Furness (1984) for carnivorous mammals.
B of Bryde’s whales estimated from Best and Rickett (1984).
B of other trophically important cetaceans probably does not exceed B of Bryde’s whales. Assuming 1% annual increase.
et et et et et
al., al., al., al., al.,
1991a 1991a 1991a 1991a 1991a
10 year 1
From daily rations of bottlenose and humpback dolphins (Smale et al., 1994) and Bryde’s whales (Best and Rickett, 1984). Within Tamura and Ohsumi’s (2000) range for cetaceans in the Southern Hemisphere.
1990s B estimated from unpublished data, MCM; Crawford et al., 1991a, 1995, 1999.
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Seals (Arctocephalus pusillus pusillus) B 29 180 t 1989 Workshop
109
110
Parameter
Original value
Source
Benthic producers B ? P/B
15.0 year 1
Jarre-Teichmann et al., 1998
Meiobenthos B P/B P/Q U
? 4.0 year 1 12% 20%
Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
Macrobenthos B P/B P/Q U
? 1.2 year 1 12% 20%
Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998 Jarre-Teichmann et al., 1998
Value used
Comments
Estimated
Using Ecopath, required B estimated for each decade; EE assumed 50% because benthic producers often consumed as decaying matter, modeled as detritus.
Estimated
Using Ecopath, required B estimated for each decade.
10%
Assimilation efficiency of benthic consumers is high (H. Verheye MCM, pers. comm.)
Estimated
Using Ecopath, required B estimated for each decade.
10%
Assimilation efficiency of benthic consumers is high (H. Verheye MCM, pers. comm.)
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
Table A.9 Benthos: input data for southern Benguela Ecopath models
L.J. Shannon et al. / Journal of Marine Systems 39 (2003) 83–116
111
Table A.10 Sources of dietary data used to compile the diet matrices for southern Benguela Ecopath models during the 1980s and 1990s Group
Dietary data source
Microzooplankton Mesozooplankton Macrozooplankton Gelatinous zooplankton Anchovy Sardine Redeye Other small pelagic fish Chub mackerel
Data unavailable therefore assumed following Jarre-Teichmann et al., 1998 Hutchings et al., 1991 Hutchings et al., 1991 Gibbons et al., 1992; Purcell, 1983; H. Verheye and J.J. Heymans (pers. comm.) Armstrong et al., 1991 Armstrong et al., 1991, Van der Lingen, 1998; L. Hutchings, MCM, pers. comm. Wallace-Fincham, 1987; Armstrong et al., 1991 1989 Workshop Baird, 1978, weighted by relative proportions of small and medium-sized (1980s) and small, medium and large chub mackerel (1990s), using VPA of O. Centurier-Harris (formerly MCM, unpublished data) Andronov, 1983, 1985 Andronov, 1983, 1985; Pillar and Barange, 1998, S.C. Pillar, MCM, pers. comm. Armstrong et al., 1991 1980s: Dudley, 1987; 1990s: Griffiths, 2000 Geelbek: Griffiths and Hecht, 1995 Kob, yellowtail, tuna: Penney et al., 1991b Lipinski, 1992; Sauer and Lipinski, 1991; Augustyn et al., 1994; Santos and Haimovici, 1998; Lordan et al., 1998 Punt and Leslie, 1995; Punt et al., 1992; Pillar and Wilkinson, 1995; Pillar and Barange, 1993; Pillar and Barange, 1997; Payne et al., 1987
Juvenile horse mackerel Adult horse mackerel (>20 cm) Mesopelagic fish Snoek Other large pelagic fish Cephalopods Small M. capensis Large M. capensis Small M. paradoxus Large M. paradoxus Pelagic-feeding demersal fish Benthic-feeding demersal fish
g
Pelagic-feeding chondrichthyans Benthic-feeding chondrichthyans Apex predatory chondrichthyans Seals Cetaceans Seabirds Meiobenthos Macrobenthos
g
Meyer and Smale, 1991a Meyer and Smale, 1991b; Horwood, 1993; Ansell and Gibson, 1990; Molinero and Flos, 1992; Braber and De Groot, 1973; MacPherson, 1983; Payne and Badenhorst, 1989 Penney et al., 1991b; Compangno et al., 1989; Cliff et al., 1989; Smale, 1991; Sauer and Smale, 1991; Ebert et al., 1992 Penney et al., 1991b; Compagno et al., 1989 Cliff et al., 1989; Ebert, 1991 David, 1987; Meyer et al., 1992; Punt et al., 1995 1980s: Best, 1967, Sekiguchi et al., 1992 1990s: few changes made to 1980s diet so that model balanced 1980s: Crawford et al., 1991b; Best et al., 1997 1990s: Crawford et al., 1991b; Crawford, 1999; Crawford and Dyer, 1995 Poorly known, therefore assumed following Jarre-Teichmann et al., 1998
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