Regime shifts in upwelling ecosystems: observed changes and possible mechanisms in the northern and southern Benguela

A regime shift is considered to be a sudden shift in structure and functioning of a marine ecosystem, affecting several living components and resulting in an alternate state. According to this definition, regime shifts differ from species replacement or alternation of species at similar trophic levels, whereby the ecosystem is not necessarily significantly altered in terms of its structure and function; only its species composition changes. This paper provides an overview of regime shifts, species replacements and alternations that have been observed in the northern and southern Benguela ecosystems over the past few decades. Bottom-up control, initiating and sustaining regime shifts or species replacements via environmental forcing, is documented for both the southern and the northern Benguela ecosystems. Fishing (a case of top-down control) appears to have played an important role in regime shift processes in the Namibian ecosystem. Very low biomass levels of exploited fish stocks associated with less efficient energy transfer in the northern Benguela are indicative of a regime shift. Very high biomass levels have been reached in the southern Benguela in the 2000s. However the alternation between sardine and anchovy that has been observed in the southern Benguela over the last two decades appears not to have had major effects on the overall functioning of the ecosystem. The consequences of regime shifts for exploitation are highlighted, suggesting that fisheries managers should move towards a more effective ecosystem approach to fisheries.     

Comparing trophic flows in the southern Benguela to those in other upwelling ecosystems

A balanced trophic flow model of the southern Benguela ecosystem is presented, averaging the period 1980–1989 and emphasizing upper trophic levels. The model is based largely on studies conducted within the framework of the Benguela Ecology Programme and updates the results of an expert workshop held in Cape Town in September 1989. Small pelagic fish other than anchovy Engraulis capensis and sardine Sardinops sagax, mainly round herring Etrumeus whiteheadi and mesopelagic fish, were important components of the food web in the southern Benguela. Severe balancing difficulties were encountered with respect to the semi-pelagic resources (hake Merluccius spp.) and demersal top predators (sharks), indicating the need for further research on the interaction of these groups with their ecosystem. The model is compared to other existing trophic flow models of ecosystems in major upwelling areas, i.e. the northern Humboldt Current (4–14°S), the California Current (28–42°N) and the southern Canary Current (l2–25°N), and to two independently constructed models of the northern Benguela ecosystem. These models are compared using network analysis routines of the ECOPATH software, focusing on the interactions between the five dominant fish species (anchovy, sardine, horse mackerel Trachurus trachurus capensis, chub mackerel Scomber japonicus and hake) that support important fisheries in all systems. The upwelling systems rank by size rather than species dominance. The ratio of catches and primary production differs between systems, partly because of differences in fishing regimes. Predation on the five dominant fish groups by other fish in the system was the most important cause of fish mortality in all models. Fishery catches are generally a larger cause of mortality for these groups than predation by mammals. The ecological cost of fishing appears to be comparatively low in the southern Benguela, because catches are low compared with the primary production, but also because the fishery is relatively low in the foodweb. However, in view of the very tight foodweb demonstrated in the model. it is likely that an increase in fishing pressure would cause severe trade-offs with respect to other components of the southern Benguela ecosystem.     

Mesozooplankton dynamics in the Benguela ecosystem,with emphasis on the herbivorous copepods

Recent research developments on the ecology, dynamics and trophic position of copepods in the Benguela ecosystem are synthesized. Attention is focused on herbivorous species of the southern Benguela and how they cope with the physical and biological variability characteristic of this upwelling region. Copepods constitute on average approximately half of the total zooplankton carbon and. are most abundant during the upwelling season. They are able to maintain large population densities within local coastal upwelling areas by combining ontogenetically based vertical migration behaviour with features of the current system. Some species have developed finely tuned strategies to overcome periods of starvation between upwelling bouts by storing lipid reserves or by entering temporary developmental arrest. In situ measurements of production rates of local species are among the highest recorded for copepods. Despite an apparent excess of food, copepods exert only limited impact on the phytoplankton, removing on average <25 per cent of that available daily. Indirect estimates of carbon flux indicate that 11–25 per cent of copepod daily ration is used for egestion of faecal pellets. Copepods are the preferred prey of a wide variety of invertebrate and vertebrate predators. Large copepods in particular are important in the diet of commercially exploited pelagic fish. Localized areas of low abundance of copepods have been found in association with high densities of anchovy during peak spawning and recruitment periods. Copepods may therefore constitute a central limiting factor for pelagic fish production in the southern Benguela.     

Ecosystem modelling in the southern Benguela: comparisons of Atlantis,Ecopath with Ecosim,and OSMOSE under fishing scenarios

Ecosystem-based management of marine fisheries requires the use of simulation modelling to investigate the system-level impact of candidate fisheries management strategies. However, testing of fundamental assumptions such as system structure or process formulations is rarely done. In this study, we compare the output of three different ecosystem models (Atlantis, Ecopath with Ecosim, and OSMOSE) applied to the same ecosystem (the southern Benguela), to explore which ecosystem effects of fishing are most sensitive to model uncertainty. We subjected the models to two contrasting fishing pressure scenarios, applying high fishing pressure to either small pelagic fish or to adult hake. We compared the resulting model behaviour at a system level, and also at the level of model groups. We analysed the outputs in terms of various commonly used ecosystem indicators, and found some similarities in the overall behaviour of the models, despite major differences in model formulation and assumptions. Direction of change in system-level indicators was consistent for all models under the hake pressure scenario, although discrepancies emerged under the small-pelagic-fish scenario. Studying biomass response of individual model groups was key to understanding more integrated system-level metrics. All three models are based on existing knowledge of the system, and the convergence of model results increases confidence in the robustness of the model outputs. Points of divergence in the model results suggest important areas of future study. The use of feeding guilds to provide indicators for fish species at an aggregated level was explored, and proved to be an interesting alternative to aggregation by trophic level.     

Changes in the northern Gulf of St. Lawrence ecosystem estimated by inverse modelling: Evidence of a fishery-induced regime shift?

Mass-balance models have been constructed using inverse methodology for the northern Gulf of St. Lawrence for the mid-1980s, the mid-1990s, and the early 2000s to describe ecosystem structure, trophic group interactions, and the effects of fishing and predation on the ecosystem for each time period. Our analyses indicate that the ecosystem structure shifted dramatically from one previously dominated by demersal (cod, redfish) and small-bodied forage (e.g., capelin, mackerel, herring, shrimp) species to one now dominated by small-bodied forage species. Overfishing removed a functional group in the late 1980s, large piscivorous fish (primarily cod and redfish), which has not recovered 14 years after the cessation of heavy fishing. This has left only marine mammals as top predators during the mid-1990s, and marine mammals and small Greenland halibut during the early 2000s. Predation by marine mammals on fish increased from the mid-1980s to the early 2000s while predation by large fish on fish decreased. Capelin and shrimp, the main prey in each period, showed an increase in biomass over the three periods. A switch in the main predators of capelin from cod to marine mammals occurred, while Greenland halibut progressively replaced cod as shrimp predators. Overfishing influenced community structure directly through preferential removal of larger-bodied fishes and indirectly through predation release because larger-bodied fishes exerted top-down control upon other community species or competed with other species for the same prey. Our modelling estimates showed that a change in predation structure or flows at the top of the trophic system led to changes in predation at all lower trophic levels in the northern Gulf of St. Lawrence. These changes represent a case of fishery-induced regime shift.     

Spatial and temporal characteristics of trophic structure of the southern Huanghai Sea fish communities

The spatial and temporal characteristics of trophic structure of fish communities in the southern Huanghai Sea were examined based on the data sampled from bottom trawl surveys conducted during the autumn of 2000 and the spring of 2001. Hierarchical agglomerative cluster method and bootstrap randomization were used to identify significant trophic groups for each fish assemblage in the southern Huanghai Sea. A total of six major trophic groups were identified within this system, which classified predators based upon location in the water column or prey size （ i. e. , benthic to pelagic predators or fish to small invertebrate prey predators）. The similarity level used to identify significant trophic groups in each assemblage ranged from 24% to 34%. Although planktivores were the dominant trophic group in each assemblage （60% - 79% ）, there were spatial and temporal variations in the trophic structure, which reflected the differences in the abundance and availability of dominant preys. Simplified food webs were constructed to evaluate the most important trophic relationships between the dominant prey taxa and the fishes in each assemblage within this system. Although there were some differences in the key prey species among different food webs, pelagic prey items （mainly euphausiids and copepods） represent the most important energetic link between primary producers and higher trophic level predators. The trophic level for most fishes was between 3 and d, and the weighted mean trophic level for each assemblage ranged from 3.3 to 3.4. Compared with previous study in the mid-1980s, there was an obvious downward trend in the trophic level for most fish species, which resulted mainly from the fluctuation in key prey species in the Huanghai Sea. The decrease in the importance of Japanese anchovy seems to be offset by other abundant prey species such as Euphausia pacifica and copepods （ mainly Calanus sinicus ） .     

Exploring the spatial distribution patterns of South African Cape hakes using generalised additive models

We developed delta generalised additive models (GAMs) to predict the spatial distribution of different size classes of South African hakes, Merluccius capensis and M. paradoxus, using demersal trawl survey data and geographical (latitude and longitude) and environmental features (depth, temperature, bottom dissolved oxygen and sediment type). Our approach consists of fitting, for each hake size class, two independent models, a binomial GAM and a quasi-Poisson GAM, whose predictions are then combined using the delta method. Delta GAMs were validated using an iterative cross-validation procedure, and their predictions were then employed to produce distribution maps for the southern Benguela. Delta GAM predictions confirmed existing knowledge about the spatial distribution patterns of South African hakes, and brought new insights into the factors influencing the presence/absence and abundance of these species. Our GAM approach can be used to produce distribution maps for spatially explicit ecosystem models of the southern Benguela in a rigorous and objective way. Ecosystem models are critical features of the ecosystem approach to fisheries, and distribution maps constructed using our GAM approach will enable a reliable allocation of species biomasses in spatially explicit ecosystem models, which will increase trust in the spatial overlaps and, therefore, the trophic interactions predicted by these models.     

Structure, biomass distribution and trophodynamics of the pelagic ecosystem in the Oyashio region, western subarctic Pacific

Biomass distribution and trophodynamics in the oceanic ecosystem in the Oyashio region are presented and analyzed, combining the seasonal data for plankton and micronekton collected at Site H since 1996 with data for nekton and other animals at higher trophic levels from various sources. The total biomass of biological components including bacteria, phytoplankton, microzooplankton, mesozooplankton, micronekton, fishes/squids and marine birds/mammals was 23 g C m⁻², among which the most dominant component was mesozooplankton (34% of the total), followed by phytoplankton (28%), bacteria (15%) and microzooplankton (protozoans) (14%). The remainder (9%) was largely composed of micronekton and fish/squid. Marine mammals/birds are only a small fraction (0.14%) of the total biomass. Large/medium grazing copepods (Neocalaus spp., Eucalanus bungii and Metridia spp.) accounted for 77% of the mesozooplankton biomass. Based on information about diet composition, predators were assigned broadly into mean trophic level 3–4, and carbon flow through the grazing food chain was established based on the estimated annual production/food consumption balance of each trophic level. From the food chain scheme, ecological efficiencies as high as 24% were calculated for the primary/secondary production and 21% for the secondary/tertiary production. Biomass and production of bacteria were estimated as 1/10 of the respective values for phytoplankton at Site H, but the role of the microbial food chain remains unresolved in the present analysis. As keystone species in the oceanic Oyashio region, Neocalanus spp. are suggested as a vital link between primary production and production of pelagic fishes, mammals and birds.     

The importance of cephalopods as prey for hake and other groundfish in South African waters

Literature on trophic relationships in the Benguela ecosystem has stressed the importance of cephalopods as prey of groundfish. The groundfish community of the shelf and upper slope of southern Africa is dominated by the Cape hakes, and the results presented (1984–1991) confirm that both species of hake are important predators of cephalopods, especially taking into consideration the abundance of hake in the ecosystem. However, geographic, seasonal and species variability are evident in the patterns observed. The main prey species are Sepia spp. (predominantly Sepia australis), Loligo vulgaris reynaudii, Todaropsis eblanae and Lycoteuthis ?diadema. The last-named is an important food organism for fish. Its systematic status needs revision, however. Qualitative results of studies of cephalopod predation are also provided for kingklip and monkfish.     

Investigations into the diet and feeding ecology of the bearded goby Sufflogobius bibarbatus off Namibia

The bearded goby Sufflogobius bibarbatus has come to replace sardine Sardinops sagax in the diets of many top predators within the marine environment off Namibia, and it is playing a key role within the region's foodweb. Previously published information on the diet of the bearded goby has been derived from small samples and has been contradictory. We investigated the gut contents of over 3 500 specimens of S. bibarbatus from two separate studies. The results indicate that the species has a fairly generalised diet, feeding mostly on benthic and pelagic animals (phytoplankton was rare), in a way that reflects ontogeny, habitat and likely prey availability. Smaller, more pelagic individuals included a substantial number of pelagic organisms in their diet and the proportion of benthic organisms increased with the size of the goby. Given the importance of this species in recycling benthic carbon through the foodweb of the northern Benguela ecosystem, there is a need to describe and quantify the benthic food environment.     

Application of the sequential t-test algorithm for analysing regime shifts to the southern Benguela ecosystem

Long-term ecosystem changes, such as regime shifts, have occurred in several marine ecosystems world-wide. Multivariate statistical methods have been used to detect such changes. A new method known as the sequential t-test algorithm for analysing regime shifts (STARS) is applied to a set of biological state variables as well as environmental and anthropogenic forcing variables in the southern Benguela. The method is able to correct for auto-correlation within time-series by a process known as prewhitening. All variables were tested with and without prewhitening. Shifts that were detected with both methods were termed robust. The STARS method detected shifts in relatively short time-series and identified when these shifts occurred without a priori hypotheses. Shifts were generally well detected at the end of time-series, but further development of the method is needed to enhance its performance for auto-correlated time-series. Since 1950, two major long-term ecosystem changes were identified for the southern Benguela. The first change occurred during the 1960s, caused predominantly by heavy fishing pressure but with some environmental forcing. The second change occurred in the early 2000s, caused mainly by environmental forcing. To strengthen these findings, further analyses should be carried out using different methods.     

Trophic modeling of the Northern Humboldt Current Ecosystem, Part I: Comparing trophic linkages under La Niña and El Niño conditions

The El Niño of 1997–98 was one of the strongest warming events of the past century; among many other effects, it impacted phytoplankton along the Peruvian coast by changing species composition and reducing biomass. While responses of the main fish resources to this natural perturbation are relatively well known, understanding the ecosystem response as a whole requires an ecotrophic multispecies approach. In this work, we construct trophic models of the Northern Humboldt Current Ecosystem (NHCE) and compare the La Niña (LN) years in 1995–96 with the El Niño (EN) years in 1997–98. The model area extends from 4°S–16°S and to 60 nm from the coast. The model consists of 32 functional groups of organisms and differs from previous trophic models of the Peruvian system through: (i) division of plankton into size classes to account for EN-associated changes and feeding preferences of small pelagic fish, (ii) increased division of demersal groups and separation of life history stages of hake, (iii) inclusion of mesopelagic fish, and (iv) incorporation of the jumbo squid (Dosidicus gigas), which became abundant following EN. Results show that EN reduced the size and organization of energy flows of the NHCE, but the overall functioning (proportion of energy flows used for respiration, consumption by predators, detritus and export) of the ecosystem was maintained. The reduction of diatom biomass during EN forced omnivorous planktivorous fish to switch to a more zooplankton-dominated diet, raising their trophic level. Consequently, in the EN model the trophic level increased for several predatory groups (mackerel, other large pelagics, sea birds, pinnipeds) and for fishery catch. A high modeled biomass of macrozooplankton was needed to balance the consumption by planktivores, especially during EN condition when observed diatoms biomass diminished dramatically. Despite overall lower planktivorous fish catches, the higher primary production required-to-catch ratio implied a stronger ecological impact of the fishery and stresses the need for precautionary management of fisheries during and after EN. During EN energetic indicators such as the lower primary production/total biomass ratio suggest a more energetically efficient ecosystem, while reduced network indicators such as the cycling index and relative ascendency indicate of a less organized state of the ecosystem. Compared to previous trophic models of the NHCE we observed: (i) a shrinking of ecosystem size in term of energy flows, (ii) slight changes in overall functioning (proportion of energy flows used for respiration, consumption by predators and detritus), and (iii) the use of alternate pathways leading to a higher ecological impact of the fishery for planktivorous fish.     

秋季黄海中南部鱼类群落对饵料生物的摄食量

研究鱼类与饵料生物之间食物定量关系进而为多鱼种资源评估提供依据,2000~2002年秋季(10~11月)在黄海中南部海域进行了定点底拖网调查,应用Eggers模型,计算了带鱼(Trichiurus lepturus)、小黄鱼(Pseudosciaena polyactis)、黄(Lophius litulon)、细纹狮子鱼(Liparis tanakae)等23种鱼类在秋季对饵料生物的摄食量。结果表明:黄海中南部23种鱼类在秋季对饵料生物的总摄食量约为309万t,其中,鱼(Engraulis japonicus)的摄食量最高(在250万t以上),占总摄食量的80.9%。中上层和底层鱼类对饵料生物的摄食量分别为262万t和47万t左右,占总摄食量的84.7%和15.3%,鱼和细纹狮子鱼分别是中上层和底层鱼类中最主要的捕食者。磷虾类是中上层鱼类最主要的食物来源,其次是桡足类、端足类和毛颚类;虾类和鱼类是底层鱼类最主要的食物来源,其次是磷虾类。太平洋磷虾(Euphausia pacifica)、中华哲水蚤(Calanus sinicus)、细长脚虫戎(Themisto gracilipes)、脊腹褐虾(Crangon affinis)和鱼同时是黄海中南部被摄食量最高的5种饵料生物,它们被摄食的生物量之和约为233万t,占总摄食量的75.5%。     

Seabirds as consumers in the southern Benguela region

Estimates of consumption of fish by breeding seabirds in the southern Benguela region converge on 50–60 × 10³ tons of food per year. Total annual avian consumption of food is approximately 15,5 × 10⁴ tons, 74 per cent being taken by species which feed on pelagic prey and most of the rest by species which frequently feed on offal at demersal trawlers. Avian consumption is similar in magnitude to that of Cape fur seals and to the catch of the commercial fishery in the southern Benguela region, but far less than consumption by snoek, squid, and, probably, sharks and jellyfish.     

Top predators in the Benguela ecosystem — implications of their trophic position

Many top predators in the Benguela ecosystem feed on prey species targeted by commercial fisheries. Their roles as indicators of the state of exploited prey resources, as competitors with commercial fisheries for resources, and as susceptible to impact from commercial fishing on those resources are briefly considered. Trends in the occurrence of anchovy Engraulis capensis and pilchard Sardinops ocellatus in the diet of Cape gannets Morus capensis off South Africa's west coast are related significantly to survey estimates of the abundance of these fish species, and they provide useful confirmation of those estimates. In the 1980s, anchovy decreased in the diet of Cape gannets, but pilchard increased. In both the northern and southern portions of the Benguela system, groundfish were thought to eat most (66–73%) of the total quantity of cephalopods and vertebrates consumed by predators and man in the 1980s. South African fur seals Arctocephalus pusillus pusillus, predatory pelagic fish and man removed roughly equal amounts, with squids, seabirds and cetaceans having a smaller impact. In the 1980s, man and seals removed about two million tons live mass more than in 1930. Indices of the rate of natural mortality of anchovy and pilchard attributable to Cape gannets are not related to biomass of the prey species. That for anchovy was high in 1989 when a poor anchovy year-class was formed. Decreased abundance of anchovy led to poor breeding by Cape cormorants Phalacrocorax capensis in 1989 and 1990. A model linking the Cape cormorant population with anchovy is used to explore the impact of possible exploitation strategies for anchovy on Cape cormorants.     

Downscaling biogeochemistry in the Benguela eastern boundary current

Dynamical downscaling is developed to better predict the regional impact of global changes in the framework of scenarios. As an intermediary step towards this objective we used the Regional Ocean Modeling System (ROMS) to downscale a low resolution coupled atmosphere–ocean global circulation model (AOGCM; IPSL-CM4) for simulating the recent-past dynamics and biogeochemistry of the Benguela eastern boundary current. Both physical and biogeochemical improvements are discussed over the present climate scenario (1980–1999) under the light of downscaling.Despite biases introduced through boundary conditions (atmospheric and oceanic), the physical and biogeochemical processes in the Benguela Upwelling System (BUS) have been improved by the ROMS model, relative to the IPSL-CM4 simulation. Nevertheless, using coarse-resolution AOGCM daily atmospheric forcing interpolated on ROMS grids resulted in a shifted SST seasonality in the southern BUS, a deterioration of the northern Benguela region and a very shallow mixed layer depth over the whole regional domain. We then investigated the effect of wind downscaling on ROMS solution. Together with a finer resolution of dynamical processes and of bathymetric features (continental shelf and Walvis Ridge), wind downscaling allowed correction of the seasonality, the mixed layer depth, and provided a better circulation over the domain and substantial modifications of subsurface biogeochemical properties. It has also changed the structure of the lower trophic levels by shifting large offshore areas from autotrophic to heterotrophic regimes with potential important consequences on ecosystem functioning. The regional downscaling also improved the phytoplankton distribution and the southward extension of low oxygen waters in the Northern Benguela. It allowed simulating low oxygen events in the northern BUS and highlighted a potential upscaling effect related to the nitrogen irrigation from the productive BUS towards the tropical/subtropical South Atlantic basin. This study shows that forcing a downscaled ocean model with higher resolution winds than those issued from an AOGCM, results in improved representation of physical and biogeochemical processes.     

Spatial characterisation of the Benguela ecosystem for ecosystem-based management

The three countries of the Benguela Current Large Marine Ecosystem (BCLME), namely Angola, Namibia and South Africa, have committed to implementing ecosystem-based management (EBM) including an ecosystem approach to fisheries (EAF) in the region, to put in practice the principles of sustainable development in ocean-related matters. There is also recognition of the need for marine spatial planning (MSP) as a process for informing EBM with regard to the allocation and siting of ocean uses so that ecosystem health is ensured and trade-offs between ecosystem services are appropriately dealt with. Marine spatial planning is both an integrated and an area-based process, and this paper produces a spatial characterisation of the BCLME for achieving a common basis for MSP in the region, focusing on the oceanography, biology and fisheries. Recognising spatial variation in physical driving forces, primary and secondary production, trophic structures and species richness, four different subsystems are characterised: (1) north of the Angola–Benguela Front, (2) from the Angola–Benguela Front to Lüderitz, (3) from Lüderitz to Cape Agulhas, and (4) from Cape Agulhas to Port Alfred on the south-east coast of South Africa. Research and monitoring requirements of relevance for MSP and EBM in the region are identified, focusing on understanding variability and change, including with regard to the boundary areas identified for the system. To this end, 14 cross-shelf monitoring transects are proposed (including seven that are already being monitored) to estimate fluxes of biota, energy and materials within and between the subsystems. The usefulness of models for understanding ecosystem variability and changes is recognised and the need for fine-scale resolution of both sampling and modelling for adequate MSP as input to EBM for the often-conflicting interests of conserving biodiversity, and managing fisheries, recreation, offshore oil and gas exploration and exploitation, offshore mining and shipping routes, is emphasised.     

Biophysical models of larval dispersal in the Benguela Current ecosystem

We synthesise and update results from the suite of biophysical, larval-dispersal models developed in the Benguela Current ecosystem. Biophysical models of larval dispersal use outputs of physical hydrodynamic models as inputs to individual-based models in which biological processes acting during the larval life are included. In the Benguela, such models were first applied to simulate the dispersal of anchovy Engraulis encrasicolus and sardine Sardinops sagax ichthyoplankton, and more recently of the early life stages of chokka-squid Loligo reynaudii and Cape hakes Merluccius spp. We identify how the models have helped advance understanding of key processes for these species. We then discuss which aspects of the early life of marine species in the Benguela Current ecosystem are still not well understood and could benefit from new modelling studies.