High fish biomass – pre-1990's Nutrient cycle (balancing, regional scale, well-established): The upwelling in the Northern Benguela current provides the region with cold, nutrient rich water that encourages the growth of plankton (i.e. zoo – and phytoplankton). The increase of plankton reduces the nutrient concentrations in the water column. This feedback mechanism keeps the concentrations of plankton and nutrients at moderate levels. (Bydén et al., 2003; Bakun et al., 2010)
Seals and birds (balancing, regional scale, well-established): Top predators such as seals and birds prey on pelagic fish. When fish stocks are high the predators have plentiful food resources and their populations grow. Likewise, when fish stocks are low, predators have access to fewer food resources leading to a population decline. (Boyer and Hampton, 2001) However, when there is a large population of predators, there is increased predation of pelagic fish and therefore fish biomass decreases.
Plankton and fish biomass (balancing, regional scale, well-established): Pelagic fish feed on plankton biomass. Therefore when fish biomass is low, plankton biomass increases.However when plankton biomass is high, there is more food resources available for fish. In this regime, there is a natural fluctuation between plankton and fish biomass, keeping the system in balance (Cury and Shannon, 2004).
Fish catch and fish biomass (balancing, regional scale, well-established): High fish biomass allows high fish catch. However, when fish catch increases, fish biomass will decrease (Pascoe and Gréboval, 2003).
Fishing technology development and fish catch (balancing, regional scale, speculative): As new fishing technology develops (e.g. more efficient fishing gear), fish catch will increase. Once fish catch has increased to a substantial level, it is likely that there will be less need for new fishing technology (FAO, 1996). This loop is context and management dependent.
Fishing effort, fishing technology development and fish catch (balancing, regional scale, well-established): As international demand for fish increases, the fishing effort (e.g. time spent fishing) increases and with that a technology development is needed. With an increase in both fishing effort and technology the fish biomass decreases. (Pascoe and Gréboval, 2003) However, given the dynamics of stocks, it is likely that at a certain point effort will no longer increase catch (see regime two).
Low fish biomass – from the 1990s This regime contains the same feedbacks as in the previous regime, although their dynamics have changed in intensity and frequency. The new feedback loops are described below:
Jellyfish and plankton (balancing, regional scale, well-established): Jellyfish feed on plankton. The increasing abundance of jellyfish reduces the plankton biomass, which in turn decreases the jellyfish abundance (through predator-prey dynamics) (Richardson et al., 2009). This feedback loop is, in turn, affected by the nutrient-plankton loop, which favors jellyfish domination.
Jellyfish, fish larvae and fish biomass (reinforcing, regional scale, speculative): Jellyfish prey on fish larvae and eggs decreasing fish recruitment which in turn lead to more jellyfish in the system to prey on fish thereby creating a reinforcing loop (Cury and Shannon, 2004; Bakun et al., 2010).
Jellyfish, plankton and fish biomass (reinforcing, regional scale, well-established): Jellyfish and pelagic fish have a competitive relationship by both feeding on plankton. With the increasing abundance of jellyfish feeding on plankton, the biomass of plankton decreases. The decrease of plankton leads to less food for the fish stocks, which thereby decreases fish populations through starvation. On the other hand, decreasing fish biomass, especially a decrease of sardine stocks, leads to a jellyfish increase (Bakun et al., 2010).
Plankton, hypoxic conditions and fish biomass (reinforcing, regional scale, well-established): Plankton (both phyto – and zooplankton) consumes oxygen. An increase of plankton creates hypoxic conditions if not preyed upon which in turn creates a hostile environment for fish larvae negatively impacting fish recruitment. This loop is reinforced given the fact that reduced fish biomass leads to an increase of plankton, which results in more severe hypoxic conditions (Bakun et al., 2010).
The hypoxic events of 1993 and 1994 (regional, well-established) were caused by a southward influx of low-oxygen water from the Angolan current (Boyer et al., 2001). These are seasonal events, not uncommon to the system when upwelling is less intense. However, this occurrence covered a larger area than usual and was longer in duration (Boyer et al., 2001). Oxygen depleted water created unfavorable conditions for most fish species, seriously diminishing their spawning and recruitment capacity as well as causing shift in population distribution and increased rate of mortality (Cury & Shannon, 2004; Boyer and Hampton, 2001; Boyer et al., 2001). With less fish in the system, it is likely that the phytoplankton biomass increased, worsening hypoxic conditions, and allowing space for jellyfish to increase in abundance.
The Benguela Niño event of 1995 (regional, well established) is a poleward movement of warm, tropical, nutrient-poor waters (Boyer et al., 2001). These events are thought to be linked to large-scale wind pattern changes and are similar to those of the Pacific El Niño (Boyer et al., 2001; Cury and Shannon, 2004). Like hypoxic events, these interdecadal climate patterns are natural system processes. However, this one was particularly intense, with the water temperature in some areas water reaching eight degrees warmer than average (Boyer et al., 2001). This stressed the system in a similar way as the hypoxic events, by decreasing recruitment capacity, causing shifts in distribution and ultimately leading to large population declines. In late 1995, anchovies virtually disappeared from the system, sardines were heavily affected, and hake and horse mackerel stocks fell by about half (Boyer et al., 2001). This decline in pelagic fish had a cascading effect in the food web with top predators such as birds and seals declining dramatically in number due to starvation (Cury and Shannon, 2004). Moreover, with less fish in the system, particularly sardines, a niche was created for gelatinous plankton to increase in abundance (Cury and Shannon, 2004; Richardson et al., 2009).
Changes in upwelling (Regional, proposed) The upwelling in the Northern Benguela current provides the region with cold, nutrient rich water that encourages the growth of plankton (i.e. zoo – and phytoplankton). (Bydén et al., 2003; Bakun et al., 2010). Changes in upwelling patterns contribute to conditions more favorable for jellyfish growth, especially in the absence of small pelagic fish (Brotz, 2012).
The main external direct driver (regional, well established) that caused the shift was overfishing. This top down constant pressure targeted in particular sardines, the most socio-ecologically important species in this system (Cury and Shannon, 2004). As sardines decreased in number, they were no longer able to maintain the wasp-waist structure and dynamics of the foodweb. Before the shift, sardines controlled both the numbers of top predators as their prey, and the numbers of plankton as their predator and maintained a competition relationship with other small pelagics and gelatinous plankton (Cury and Shannon, 2004). The sardine-targeted fishery thereby eroded resilience of the system by removing a species of particular functional importance, leading to altered system structure and changes in the trophic web (Cury and Shannon, 2004). Moreover, it appears that the over-harvesting of a dominant small filter feeder, such as sardines, is often followed by a jellyfish explosion, in particular in situations where there is no other fish of similar function that can act as a replacement (Richardson et al., 2009). This is likely to have been the case in the Northern Benguela, which, unlike the neighboring Southern Benguela, did not respond to the decline in sardine biomass by an increase in anchovy biomass (de Young et al., 2004).
The main external indirect drivers that contribute to the shift include:
The international market (global, speculative) drives the activity of (over) fishing in a number of ways. For example global trade constantly drives the demand for low cost protein.
World population growth (global, speculative) and its increased demand for food may drive fishing indirectly via market mechanisms. Fish being a high source of protein is often sought after and is of high value.
Human induced climate change (global, speculative) may have acted as a driver in this shift although this remains elusive. It is uncertain whether the increased sea surface temperature of the 1990's was due to anthropogenic climate forcing or not and whether the particular magnitude of the shock events was in anyway related to climate change. See below for more detail on SST.
A slow internal system change that may have contributed to the regime shift is the rise in sea surface temperature (regional - global, speculative). There has been a general warming of SST in the Northern Benguela (Bakun et al., 2009; Cury and Shannon, 2004) although it remains uncertain whether this general rise contributed to the shift or whether it was the shorter periodic events (Benguela Niño). Warmer water temperatures are likely to be contributing to keeping the system in the new state, as jellyfish thrive in warmer conditions compared with most other fish.
Sardine abundance threshold. One of the key thresholds identified was probably crossed with the collapse in sardine biomass. Sardine populations reached a number so low they could no longer reproduce. With no other species with a similar functional role responding rapidly enough to act as an adequate replacement, repercussions echoed through the food chain.
Other pelagic fish threshold. It is likely a threshold was crossed with the collapse of most pelagic fish stocks in the 1990s, at the time of the regime shift. While drivers pushed the system into a new regime, it is possible that these stocks had crossed a point where they could not carry out the function role that they has assumed from the sardines.
Reducing fishing pressure (regional scale, speculative): Reducing fishing pressure could lead to the recovery of small pelagic fish stocks, both directly by increasing biomass and indirectly by reversing reinforcing feedback loops in the system. However, model simulations in the northern Benguela suggest that reducing fishing pressure alone may not lead to initial levels in small pelagic fish seen 40 years ago, indicating that there has been a dramatic alteration of the trophic foodweb (Roux and Shannon, 2004). Several studies argue that management must move from a single-species approach to a more effective ecosystem approach to fisheries (Cury and Shannon 2004; Roux and Shannon 2004) that takes into account trophic interactions as well as environmental anomalies (Roux and Shannon, 2004), fish migration and protection of spawning location. This includes setting target exploitation rates that are based on more than biomass levels, e.g. recent SST as this has indirect effects on fish spawning and fish recruitment (Jacobson and MacCall, 1995 cited by Boyer and Hampton, 2001).
Jellyfish removal (regional scale, speculative): Jellyfish currently occur in very high numbers in the northern Benguela. Purcell 1989, 1992, Purcell et al. 1994, as cited by Brierley, 2001, suggests that jellyfish now play an important role in trophic processes by sharing the niche of small pelagic fish. The area of invasive jellyfish is still a fairly unexplored one but Roux and Shannon (2004) demonstrated that simulated removal of gelatinous zooplankton had positive effects on most fish groups. Several actions have been proposed for managing the jellyfish. These actions include direct jellyfish removal through biocontrol, jellyfish destruction, or massive harvesting (Richardson, 2009). Up until today, there have been no attempts in the Benguela to harvest jellyfish for commercial purposes (Roux et al., 2013). However, jellyfish are culturally important as a gourmet food in China and harvest of jellyfish for human consumption could be an interesting alternative (Richardson, 2009). For more potential management responses to jellyfish outbreaks see Richardson, 2009). However, for these actions to be successful there need to be an abundance of fish to occupy the ecological niche that jellyfish currently dominates.
Targeting top predators (regional scale, speculative): Seals in the Benguela are estimated to consume about a million tons of fish annually. That equals the total annual fish catch of Namibia and South Africa combined (Boyer and Hampton, 2001). Increased sealing has been suggested to improve depleted fish stock recovery in the Benguela (Shaughnessy, 1985; Butterworth et al., 1988; Wickens and Shelton 1988 cited by Roux and Shannon, 2004). However, as Roux and Shannon (2004) demonstrated, this is a highly questioned leverage point since modeling of altered sealing only have moderate benefits to most fish groups seals prey on.
Environmental events as windows of opportunity (regional scale, speculative): Changes in large-scale climate patterns coupled with new research could provide unique opportunities for better management of the system. Efforts are being made in attempting to predict the occurrence of Benguela niño events with one study suggesting that these events can now be predicted within two months of occurring (Florenchie et al., 2003). Given the large impact on fisheries that such events have, their prediction could provide a window of opportunity for better management of the Namibian fishery. For example, 'emergency quotas' could be implemented during the period leading up to and during the Benguela Nino, as fish stocks are even more susceptible to die-offs and jellyfish predation during these events.
Ecosystem service impacts
Ecosystem services. The loss of fish biomass has most greatly impacted the provisioning service of fish production. With the shift from high to low biomass, the amount of fish caught steeply declined. For example, during the height of the sardine fishery, roughly 700,000 tons of sardines were caught annually and when the stock was at its lowest in1996, only 2,000 tons were reported (Boyer and Hampton, 2001). In the 1990s, horse mackerel, another commercially valuable species, declined to a third of their 1980s catch (Heymans et al., 2004). Additionally, seal populations declined by a third in the 1990s (Roux, 1998 as cited by Cury and Shannon, 2004) likely causing some economic losses in the Namibian sealing industry during that period, another provisioning service (Boyer and Hampton, 2001). Loss of fish biomass made room for increased numbers of jellyfish, leading to economic losses from jellyfish busting trawl nets, spoiling catches, and disrupting power generation systems on fishing vessels. Jellyfish have also hindered other marine economic activities by locking alluvial sediment to underwater diamond mining (Lynam et al., 2006).
The shift to low biomass also had an impact on recreational fishing and tourism. The recreational fishing sector in Namibia had grown rapidly after independence, attracting visitors from Namibia and South Africa, and generated considerable employment and revenue in coastal towns. However since the shift, the number of fish caught has declined significantly (Kirchner 1998 as cited in Boyer and Hampton, 2001). There has been a loss of the regulating service of water purification via the disruption of underlying ecosystem processes. Loss of fish biomass has led to an influx in phytoplankton, contributing to low oxygen hypoxic conditions (Cury and Shannon, 2004).
Human wellbeing impacts. The two centuries prior to Namibian independence in 1990 were characterized by international overexploitation of the marine resources in the Northern Benguela (Sowman and Cardoso, 2010) thus prior to 1990, those benefiting most were foreign fishers and consumers. Still, after independence it is said that only "a privileged minority" benefits from the Namibian fisheries, as 90% of marine catch is exported and many local fishers often hold contracts with foreign groups (Sowman and Cardoso, 2010). Most of the marine catch from Namibian fisheries is for export, thus with the shift in the 1990s, the loss of services was felt most by members of the industrial fishing industry, such as fishers and owners of and employees in processing plants. Additionally, foreign consumers of fish are affected by loss of food supply; however, this loss is masked by the global market (Berkes et al., 2006).
Fishing is the third-largest sector in the Namibian economy, and is the second fastest growing industry in Namibia (Boyer and Hampton, 2001). Since independence, there has been a push to promote the "Namibianization" of the fishing industry (both fishing and onshore processing) to create local employment and to promote the consumption of fish by Namibians. As there is a growing concern about local food security in Namibia, securing local food resources is becoming increasingly important (Sowman and Cardoso, 2010).With uncertainty surrounding the stock recovery, and consequential impacts on other resource-dependent industries such as sealing, the well-being of Namibians is likely to be more affected by the continuous low biomass state.
Despite the fact there is no formal artisanal fishing sector in Namibia, there are some fishing activities carried out by poor coastal fishers that would be classified as artisanal fishing in other countries (Sowman and Cardoso, 2010). These small-scale fishers are directly impacted by loss in fish biomass, which decreases well-being by reducing local food supply. Last, recreational fishers are negatively impacted by the loss of fish biomass, especially with the increasing importance of the recreational fishing sector (see above).
Uncertainties and unresolved issues
There are great uncertainties surrounding the Northern Benguela system, in regards to what drove the regime shift, and if it can be brought back to it's prior state of high fish biomass.
Initial uncertainty revolves around the tipping points of the system. Overfishing and environmental perturbations clearly drove the regime into the new state, however there is much debate as to which driver played a greater role. We have argued that it was overfishing that undermined ecological resilience, making the system more vulnerable to environmental anomalies that occurred in the 1990s.
There is also uncertainty about the role of climate change in shifting the regime, as well as maintaining the regime in its current low biomass state. Additionally, the role of climate change in increasing the intensity of environmental anomalies of the 1990s is unknown.
Marine upwelling ecosystems dominated by gelatinous plankton is a fairly new, but common problem at a global scale (Richardson et al., 2009). However, there has been little research on its long-term impacts on socio-ecological systems. Most jellyfish outbreaks are unreported and under-monitored and it appears there is a need for more research on the ecological role of jellyfish and their life cycles (Richardson et al., 2009).
Lastly, the system seems to be characterized by hysteresis, indicating that a shift back to a sardine dominated state might be impossible. It is argued that current TAC (Total Available Catch) values may not reflect the actual sustainable levels required to maintain the health of the ecosystem. This is a common problem in marine systems, as understanding their dynamics is extremely difficult. More knowledge about the underlying ecosystem processes and functions in marine systems would help resolve these uncertainties.