Bacterial biomass and production estimates range from a conservative 2-7% and 3-5% of that of phytoplankton to 8-27% and 26-44% respectively in the least conservative case.
Substantial advances have been made with respect to the dynamics of phytoplankton-blooms and plankton-ecology in general in the southern Benguela by drogue studies (following patches of freshly upwelled water as it ages) and anchor station experiments. (The latter were also done in the northern Benguela.) During the past decade a good understanding of community structure and variability has been gained in the southern Benguela which has showed systematic trends in dominant patterns of diatoms, dinoflagellates and microflagellates in relation to upwelling, pulsing, turbulence and stratification. The importance of phytoplankton seed populations in determining the composition and time required for bloom development has been established and insights have been gained into maintenance and life-survival strategies. In this respect, diatoms tend to form spores which sink rapidly, and this enables them to remain in the nearshore and nutrient-rich environments closer to upwelling centres (Pitcher 1990). Studies on rate dynamics have enabled the quantification of the phytoplankton loss process to be made. The knowledge gained in the south, if applied in the north, should facilitate a quantum jump in the understanding of the dynamics of the Benguela – at least in respect of plankton processes.
Red tides and harmful algal blooms.
Outbreaks of red tide occur both in the northern and southern Benguela. They tend to be observed most frequently close inshore, where their visual and at times harmful effects are most apparent. Red tides are most frequent during quiescent conditions which follow upwelling, or during periods of light onshore winds and downwelling which commonly occur in the southern Benguela during times of Pacific El Niño events. The red tide causing organisms in the Benguela are generally dinoflagellates and sometimes ciliates, and contrary to popular belief, most of the red tide species are non-toxic (Horstman 1981).
That red tides occur regularly in the Benguela is not unexpected. Diatoms, which dominate the phytoplankton in the Benguela, have high nutrient requirements and are adapted to turbulent conditions. The diatom blooms which are associated with upwelling events quickly strip the nutrients from the upwelled water, and as the water column stabilises and stratifies, this provides a suitable environment for dinoflagellates, which being tolerant of low nutrient conditions, and favouring stable high light conditions, can then outcompete the diatoms and “bloom”. The dynamics of red tide blooms in the Benguela have been studied in some detail, in particular in the south, during the past two decades by Dr G. Pitcher and his coworkers. In a recent article Pitcher and Boyd (1998) have described from an examination of the distribution of dinoflagellates across the continental shelf and of currents the physical mechanisms responsible for red tide outbreaks, and for the maintenance of motile populations within the system.
The most common red tide organism in the southern Benguela is Noctiluca scintilans, a non-toxic dinoflagellate. It also occurs off Namibia. This organism has been associated with fish mortalities, however, not through any toxin, but by depleting the dissolved oxygen in the water during major blooms, and also evidently by clogging the gills of fish. Noctiluca blooms have a characteristic bright orange colour – almost luminous (see Fig. 12). The most common red tide species off Namibia appears to be Heterocapsa triquentra, and like species of Gymnodinium, Gongaulex and Scrippsiella, ithas been linked to mortalities in fish. Most reported mortalities of marine life in the Benguela which have been associated with harmful algal blooms (HABs), in particular mortalities of sand mussels and benthos have been due to a few species of Gongaulex and to Mesodinium rubrum. The latter species is also known to occur off Angola. Red tide outbreaks off Angola were first reported in the scientific literature of the 1940s. A major bloom of Prorocentrum balticum occurred between Namibe and Luanda in August-September 1951, and was associated with high fish mortality (Silva, 1953) – see also a comprehensive account of red water on the coast by Paredes (1962). Pitcher (1999) recently reviewed the pertinent information on HABs in the Benguela system. His report is an excellent overview of the subject and introduction to the published literature.
Whether or not the frequency of red tides and HABs in the Benguela is increasing, is not clear. What is known is that there are interannual fluctuatations in occurrences, probably associated with changes in weather patterns. Moreover, in the late 1980s, “green tides” occurred in the area east of Cape Point, in particular in False Bay. These outbreaks caused large mortalities of sedentary organisms such as abalone and also led to respiratory problems in humans swimming in, or in close contact with, affected areas of sea water. The species responsible was Gymnodinium nagasakiensis and is though to have been imported via ballast water discharges. However, relatively little is known about the extent of exotic species introduced into the system from such discharges.
Zooplankton and secondary plankton
Zooplankton in the Benguela ecosystem is dominated by small crustaceans (tiny shrimp-like animals), the most important groups being copepods and euphausiids. Of these copepods are numerically the most abundant and diverse group. Species diversity is highest near the warm water boundaries of the ecosystem i.e. in the vicinity of the confluence between the Angola and Benguela Currents, west of the oceanic front and shelf break, and in the extreme south over the Agulhas Bank and adjacent Agulhas retroflection area. Over the shelf, within the main upwelling system copepod diversity is lower, and biomass higher, being dominated by a mixture of small (Paracalanus, Ctenocalanus, Oithona, Clausocalanus), medium (Centropages, Metridia) and large (Calanoides, Rhincalanus) copepods. Among the most common species are Centropages brachiatus, Calanoides carinatus and Metridia lucens. On the Agulhas Bank the zooplankton biomass is dominated by a single species, the large copepod Calanus agulhensis which has a centre of distribution in the central-eastern part of the Bank – over the endemic ridge of cool water. Copepods play an important role in the trophic functioning of the Benguela ecosystem. They are the principal food of anchovies and as a consequence they are the most studied zooplankton group – in the southern Benguela at least.
There are more than 40 species of euphausiids in the Benguela ecosystem. Of these Euphausia lucens is the dominant euphasiid in the southern Benguela and Nyctiphanes capensis in the north. Except in the central Benguela i.e. near Lüderitz, these two species generally do not occur together. The latter species also occurs, however, east of Cape Agulhas. Overall abundance of euphasiids appears to decrease towards the boundaries of the Benguela ecosystem. Studies on the life history of euphausiids in relation to the physical environment have led to an improved understanding of the role of euphausiids in the ecosystem and also to a better understanding of the dynamics of the various fronts and associated upwelling and sinking processes. Studies of the vertical distribution and daily movement of euphausiids in the Benguela have shown that the younger stages to occur near the surface and migrate little, while older stages occur deeper and display significant migration. Euphausiids are important prey items for anchovy and hakes, and conversely E.lucens is capable of capturing and consuming small fish larvae.
Thaliaceans (salps and doliolids – gelatinous zooplankton) are common throughout the Benguela. They are often indicators of intrusions of warm water, particularly in the southern Benguela. Analyses of gut content suggest that thaliaceans feed mainly on phytoplankton in inshore waters and on zooplankton offshore. The impact of thaliaceans on zooplankton and ichthyoplankton (fish eggs and larvae) has not been quantified, but it could be significant at times. Likewise the abundance and impact of other gelatinous zooplankton, which is periodically abundant in the Benguela, in particular off Namibia (“jelly invasions”), has not been quantified.
In the northern Benguela peak abundances of zooplankton appear to coincide with periods of maximum phytoplankton abundance viz. November – December and March – May, the former following the main upwelling season and the latter during moderate upwelling when summer stratification weakens. In both cases the spatial distribution of zooplankton differs from that of phytoplankton in that zooplankton tend to be more abundant offshore of the (coastal) phytoplankton maxima (beltlike distribution parallel with the coastline). This is probably an oversimplification. However, as there is a general lack of proper quantitative estimates of zooplankton abundance and production in the northern Benguela, coupled with the fishery-centred sampling bias.
In contrast, in the southern Benguela there are relatively good estimates of zooplankton distribution, abundance and production. Zooplankton standing stock estimates in the upwelling area off the Cape Peninsula display distinct seasonality, associated with the upwelling cycle, with a winter minimum and a summer maximum. Superimposed on the seasonal cycle is substantial shorter period variability (determined by upwelling pulsing, the dynamics of the phytoplankton blooms and the life histories of the various zooplankton groups). The series of drogue studies in the 1980s which followed an upwelling pulse and tracked the processes as the freshly upwelled water parcels aged, have contributed substantially to the understanding of plankton dynamics. In the southern Benguela the best estimates of zooplankton production suggests that it is of the order of 80gC/m2/y.
Hutchings et al. (1995) have reviewed inter alia zooplankton grazing in upwelling systems and highlighted a number of generally applicable principles which follow: Although copepods and euphausiids have rapid responses to increased food in terms of egg production, their response in terms of growth of juvenile stages to adulthood are much slower. Behavioural adaptations promote maintenance in the upwelling circulation. Juvenile stages remain near the surface; older stages migrate more extensively and are advected back into inshore water again, allowing grazers to prolong contact with phytoplankton blooms. Wind reversals/calms which allow phytoplankton to return shorewards or be entrained in eddies as they develop may increase the phasing effiencing between phytoplankton and zooplankton. Because of their limited mobility power, zooplankters need to adapt behavioural responses to maximise contact with food items and also minimise predation mortality. The recirculation of zooplankton may be favoured by undercurrents, eddy structures – such as exist near upwelling centres – and inshore counter currents. Like upwelling systems in general, in the Benguela zooplankton biomass maxima tend to exist downstream from upwelling centres and it is these areas which are preferred habitats of developing juveniles of fish species such as anchovy and sardine. Examples of these areas are St Helena Bay, Orange River bight, near Walvis Bay and off northern Namibia.
During the past decade Cape Town-based planktologists have focussed much of their attention on copepod and euphausiid ecology, reinforcing field studies with experiments using animals reared in the laboratory. This has led to a greatly improved understanding of feeding requirements, growth rates and how zooplankton adapt to environmental variability in the southern Benguela. Combined field-laboratory experiments have shown that anchovy are size-selective feeders (“biters”) rather than filter feeders and derive most of their energy requirements from large copepods and euphausiids. Conversely sardine (pilchard) feed predominantly by filtering – even filtering relatively large zooplankton such as euphausiids. Only when the density of large food organisms is very low does biting become more important for sardine than filtering (Van der Lingen 1994). Whereas the energy costs of filter feeding for anchovy are high (higher swimming speeds result in high respiration), for sardine the opposite applies i.e. the costs for filter feeding remain much lower than for anchovy even at high swimming speeds, while more energy has to be expended to orientate on prey in a biting mode (Van der Lingen 1995). This food partitioning is illustrated diagrammatically in Fig. 13. The consequence of the different feeding behaviour between anchovy and sardine is that sardine do better when small food particles dominate as in stratified waters, whereas anchovy should do better when the sea is dominated by larger particles, such as during turbulent upwelling conditions and might explain why sardine and anchovy appear to undergo alternative phases of dominance in upwelling regions over periods of 30-60 years (Hutchings and Field 1997). It might also explain some of the observed differences between the southern (rapidly pulsed) and northern (more uniform) parts of the Benguela ecosystem.
The past decade has also witnessed close collaboration between biological oceanographers, physical oceanographers and fishery scientists fostered through joint participation in hydroacoustic fish survey cruises, and this enabled the application of oceanographic knowledge about mechanisms of upwelling and plankton dynamics to be applied directly to solving fishery problems. Apart from obvious increased relevance of research, it also resulted in a greatly improved fundamental understanding of biological oceanographic processes and the role of these as a determinant of fish recruitment. Suites of papers which have appeared in the South African Journal of Marine Science Volumes 5, 12 and 19 and other mainstream international journals document these developments, while progress in various aspects of biological oceanography in the Benguela ecosystem have been very adequately reviewed in a recent article by Hutchings and Field (1997).
Perhaps the most significant finding during recent years is that of Verhehe et al (1998) who observed that crustacean zooplankton abundance, expressed in terms of number of animals, increased by two orders of magnitude in the southern Benguela between 1951 and 1996,suggesting that a major change in the ecosystem has occurred. (This is discussed in Section 5.)
Readers interested in the zooplankton of the Benguela ecosystem within the context of the physics and chemistry and general biology of the South Atlantic Ocean are referred to a recent review article by Boltovskoy et al (1999).
Foodweb and carbon budget
As Hutchings and Field (1997) have pointed out, grazing by copepods and euphausiids and the sedimentation of organic material within the Benguela cannot account for the decline in phytoplankton blooms after upwelled water has stabilised, so considerable recycling of organic material must take place in the water column in the southern part of the ecosystem. This has been confirmed by the application of stable isotope techniques (N15 uptake methodology) by Probyn (1992), Waldron et al (1998) and others that the f-ratio (a relative index of new production) in the Benguela is relatively low (0.2 – 0.3) - only about one half or one third of the value in the Humboldt and California Current systems (Refer also back to Fig. 10). Thus, despite the high rate of new nitrogen input to the shelf waters via upwelling, much of the shelf water is dominated by the microbial foodweb fuelled by recycled nutrients (Hutchings et al 1995). Following the argument further, as it is new production which determines the productivity at higher tropic levels (fish), and as the food chain in the Benguela has been found to be much more complex (and less efficient) than the classical 20% applicable in a simple short-food chain (phytoplankton zooplankton fish), this to some extent explains why the Benguela yields considerably less fish than 100 million tons which simplistic estimates might indicate. Perhaps the most realistic model of the trophic functioning of the Benguela was that developed by Moloney (1992), by incorporating the microbial foodweb. Her model is illustrated diagrammatically in Fig. 14. The fundamental concepts embodied in this simple sketch have major implications for understanding the functioning of upwelling systems and their evident resilience! The understanding of the complexities of the foodweb and underlying processes is an imperative for the management and sustainable utilisation of the living marine resources of the Benguela ecosystem.
In a comprehensive examination of the mechanisms which drive the carbon flux in the Benguela, Monteiro (1996) concluded that upwelling source water moves on to the shelf at three principle sites which are determined by topography (the most important of these being at 27S near Lüderitz, the others being at 18S at Cape Frio and at 32S), and that it is modified on the shelf, becoming enriched in nitrogen and carbon before eventually outcropping at the main upwelling centres (of which there are six). Monterio (1996) hypothesised that the three source sites act as “gates” or barriers to the southward movement of water on the shelf. He developed a model which suggested that the water which upwells at sites north of Lüderitz resulted in outgassing of carbon dioxide, while at Lüderitz and further south, the “carbon pump” and biological activity result in that part of the system being a carbon dioxide sink. Based on certain assumptions about dissolved organic carbon, Monterio calculated that the Benguela system as a whole was a small carbon dioxide sink of 0.34 – 1.5 million tons C/y. The better quantification of upwelling systems such as the Benguela as sources or sinks of carbon dioxide has important implications for the global carbon budget. The Achilles heel remains inadequate knowledge about fluxes of dissolved organic carbon.
A complex array of processes affect the Benguela over a broad spectrum of space and time scales, ranging from the molecular level and fractions of a second to those which span several thousands of kilometers (basin-wide and global) and take place over several months, years, decades or even longer.
There are a number of physical factors which are important determinants of the structure and functioning of the ecosystem, and of these the wind – and in particular the periodicity in the longshore upwelling producing wind – is of over-riding importance. The wind field and wind frequency significantly influence coastal trapped shelf waters (these are internal waves in the sea, referred to earlier), upwelling, formation of fronts, production of filaments, surface and near-surface currents and the depth of the thermocline inter alia, and a host of dependant chemical and biological processes. The large-scale wind field is also an important determinant of basin-wide circulation, and consequently changes in winds even thousands of kilometers away can impact on the movement of water at the boundaries of the Benguela and within the system.
Apart from winds, seasonal change in insolation (solar heating) is important, influencing the temperature of the surface layer, its thickness and thermocline formation, while variations in light intensity likewise are important in terms of photosynthesis and primary production. What should be recognised is that over one third of the Benguela upwelling area and all of Angola’s coastal oceanic waters lie within the tropics, and consequently receive high levels of thermal radiation and light. Tides and tidal currents are important in the near-shore environments, especially in semi-enclosed bays, although in comparison with coastal areas in those parts of the world which experience large tidal ranges, their effects within the Benguela are relatively minor. (The tidal range in the Benguela is typically 1-2m.) There are a number of similarities between the variability in the Benguela and other upwelling systems, but there are also some important differences. What distinguishes the system from other eastern boundary regions is the existence and variations in the northern and southern boundaries viz. the Angola- Benguela front and the Agulhas retroflection area. In addition, the variability in the southern Benguela caused by the free passage of westerly winds and low pressure systems south of the sub-continent make this area quite unique.
However, like in other upwelling systems which are pulsed, the biota in the Benguela ecosystem are generally well adapted to the inherent variability in physical forcing on seasonal and shorter time scales. The biota are, however, less well adapted to sustained major events or changes which occur less frequently i.e. every several years or even over decades. Accordingly, we provide only abridged comments on aspects of small-scale and seasonal variability, and focus most of the discussion on the “catastrophic” occurences which have system-wide impacts. We also highlight some long-term and decadal changes which have been observed in the system.
Small-scale variability Processes which occur on time scales of hours to several days and space scales of meters to tens of kilometers are characteristic of upwelling events. These “event scale” processes attracted considerable research attention in the 1970s and 1980s in the southern Benguela, and much of this work has been reviewed by Shannon (1985), Chapman and Shannon (1985) and Shannon and Pillar (1986). The application of remote sensing using aircraft and satellites during wind events in combination with in situ measurements using ships, provided knowledge about the initiation of upwelling, the growth and decay of upwelling plumes off the Cape Peninsula and Cape Columbine following the onset, intensification and subsequent reversal of the upwelling causing winds. Measurements in situ over hours and days provided a good understanding of biochemical processes and plankton dynamics. For example, by following patches of water and frequent sampling of these during upwelling events, the supply and depletion of nutrients, effects of light and light limitation, development of plankton “blooms”, species successions, decay processes etc were observed and quantified (e.g. Barlow 1982, Brown and Hutchings 1985). Although most of this research was conducted in the southern Benguela, scientists from the former German Democratic Republic undertook off central Namibia in 1976 one of the most intensive studies of the system over a period of a few weeks, using a combination of repeated surveys along a line of stations and quasi-continuous sampling at a fixed station. (e.g. Postel 1982). Their work showed vividly how the chemistry and biology of the water column changes in response to changes in its physical structure. A somewhat similar experiment was conducted in St Helena Bay a decade later and the findings were published in a special issue of Progress in Oceanography (Volume 28).
There is so much information contained in the hundreds of scientific publications which resulted from the era of event-type process studies in the southern Benguela, that it is just not possible to condense it adequately and explain it simply. What is apparent, however, is that there exists as superb body of information on the dynamics of upwelling and its consequences in the southern Benguela. Volumes 5 and 12 of the South African Journal of Marine Science published in 1987 and 1992 respectively contain many of the relevant papers. The small and mesoscale processes in the northern Benguela and in Angolan waters have, however, with few exceptions, received less attention. As the systems there function differently from that in the south, simple extrapolation of results and application of some of the concepts developed in the south to the Namibian and Angolan systems may be inappropriate and misleading.