Introduction is characterized by high productivity and supports

Introduction  The Benguela Upwelling System is located off the southwestern coast of Africa, from the southern Angola (between 14 ºS and 16ºS) in the North, to Cape Agulhas (37? S) in the South (Figura) (Shannon et al., 1987; Shannon and Nelson, 1996; Shannon et al., 2004), across the coast of Angola, Namibia and western coast of South Africa (Blanke et al., 2005; Shilington et al., 2006).

Three currents influence it: south Atlantic Current, the Agulha Current and Antarctic Circumpolar Current (Berger et al., 1998; Shannon and O´Toole, 2003). Among the Eastern Boundary Upwelling Systems, the BUS has a unique characteristic, being limited in both north and south by two warm currents, Angola Current and Agulhas Current respectively (Shannon and Nelson, 1996; Shillington et al., 200; Shannon et al., 2010). The permanent upwelling cell at Lüderitz (27.

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5°S) divides the system in to north and south sub-systems (C.D. van der Lingen et al., 2006; Shannon et al.

, 2004; Tim et al., 2015). Each of this subsystems, has its own environmental characteristics, which lead to difference in abundance, distribution and biological characteristics of the marine living resources. Similar to other Eastern Boundaries Upwelling Systems (EBUSs), the Benguela Upwelling System (BUS) is characterized by high productivity and supports   large population of small pelagic fish that are, of great economic and social importance to the region. Beside the socio-economic importance, these species (anchovy Engraulis encrasicolus, redeye round herring Etrumeus whiteheadi, sardine Sardinops sagax, sardinellas Sardinella aurita and S. maderensis), play a crucial roll in intermediate level of the marine food web (Shannon et al., 2004), and are highly vulnerable to environmental variability (Bakun et al.

, 2015). Nevertheless, the management of these species throughout the region is difficult, due to the variability in their abundance and changes in distribution patterns, as a consequence of environmental variability (Cury and Shannon 2004; Lamont et al., 2017), which may affect their recruitment.Andrew Bakun (1990, 2004, 2015) proposed that increasing greenhouse gas concentrations would enhance upwelling in the EBUSs through intensification of upwelling-favorable wind. In the last decade, the trends of wind, seems to support Bakun hypothesis, as upwelling–favorable winds have intensified in the California, Benguela and Humbolt systems, and weakened in the Iberian system (Sydeman, 2015; García-Reyes et al., 2015).  In agreement, Narayan (2010) supports Bakun´s hypothesis, that coastal upwelling will increase as a result of global warming. In contrast, Tim et al.

, (2015) suggests a decrease of coastal upwelling in the northern Benguela and an increase in southern Benguela. Lamont et al., (2017) found similar result, with a significant decrease in upwelling in the northern BUS and a significant increase in the Agulha Bank. These trends can impact both, negative and positively the recruitment of SPF in these regions (Roy et al., 1992), as they are highly vulnerable to environmental variability, especially in their early life stage (Cury and Roy, 1989; Shannon et al., 1996), although, the impact on the pelagic fish are more expected to happen if coupled with overfishing (Bakun at al., 2015). However, the correlation of upwelling intensity and small pelagic fish (SPF) recruitment success can be positive if the relationship is dome-shaped, as suggested by “Open environmental Window hypothesis” (recruitment success is maximized at intermediate level of upwelling intensity, while at low upwelling intensity, nutrients can be limiting to productivity and at strong upwelling, biota can be advected offshore) (Cury and Roy, 1989).

In the northern Benguela, the environment has been recognized as an important driving force for regime shifts (Cury and Shannon, 2004). Boyer, (2001) stated that adverse environmental conditions were responsible for the recruitment fluctuation of the northern Benguela sardine stock observed during 1990s, but the decline that haven’t recovered yet, was a result of overexplotation. During 1993 and 1995, two environmental events (hypoxia and Benguela Niño) caused changes in distribution and abundance of sardine and anchovy in the northern BUS, with major impact on their recruitment and as a consequence, decline in catch rates was observed (Boyer et al., 2001).

The Benguela Niño, which occurs in decadal-scale, a strong and persistent intrusions of warm saline surface waters on to the northern Benguela, have been the cause of mortalities of sardine and horse mackerel off the coast of Angola and Namibia (Gammelsrod et al., 1998). At other hand, this event affected the distribution of S. aurita (Binet et al., 2001) and S. sagax (Gammelsrod et al.

, 1998), forcing them to move southwards, to northern and central Namibia respectively. Furthermore, intensification of upwelling in central Namibia (Luderitz) result in the displacement to south Angola of up to 50% of the stock of S. sagax. Binet, (2001) described that during the Guinean Niño were observed a displacement of both S. aurita and S. maderensis stock in the northern Angola and Congo.

Off the Angolan coast, is being observed a clear migration patern in seasonal and decadal-scale in the distribution of Sardinella spp. During cold season (June-October), S.maderensis move northwards, and southwards at the beginning of the warm season (February to may) (FAO, 2000), while S. aurita population is located off Angola almost throughout the year. So far, in the Angola Subtropical System (ASS), no attempts have been made to correlate environmental fluctuations to recruitment success of the two most important small pelagic fish Sardinella aurita and S.

maderensis. Due to their ecological and economic importance for the region, understanding the influence of future climate variability on recruitment of these valuable species is a key for their future management. Thus, with this review paper we aim to understand how Sardinella recruitment may be affected by future environmental variability as a result of global climate change. Key words: Northern Benguela, Angola Subtropical System, Sardinellas, recruitment, and environmental variability.                  Ø  Major physical processes in the BUS The BUS is driven by several factors such as coastal topography and climatological winds (Shannon et al., 1985).

The region is governed by both, southerly and southeasterly winds (Hagen et al., 2001), that are influenced by the cyclones moving westward over the south Benguela and by pressure over the southern Africa (Shannon and Nelson, 1996). Compared to other EBUSs, the BUS displays some particular characteristic such as: I) Low bathymetry off southern Angola (20 km), south Luderitz (75 km) and off Cape Peninsula (40 km) (Shannon and Nelson, 1996); II) dominant equatorward wind stress inducing Ekman transport of the surface water, which is replaced by cool, nutrient rich surface central water (Shillington, 1998); III) Poleward undercurrent along the continental shelf break which induces on the shallower continental shelf in vários places; IV) Kelvin wave like disturbances traveling eastewards along the Atlantic Ocean equatorial waveguide, travel from south America to Africa, turning polewards along the Angolan coast, giving rise to Benguela Niños (Florenchia et at.

, 2004); V) Agulha ring formation after the Agulhas Current retroflection south and west of Cape Town, and the subsequent interaction of these rings with the southern Benguela upwelling frontal zone (Shillington, 1998) and; VI) The seasonal and interannual displacement of the Angola-Benguela Frontal Zone (ABFZ) and the almost decadal variability of the Benguela Niños (Veitch et al., 2006).   The Northern Benguela The Benguela upwelling system is divided in two sub-systems, the northern and southern Benguela, being separated by the strongest upwelling cell at Luderitz (26ºS) (Shannon and Nelson, 1996), that provide a barrier to north-south migration of sardine and anchovy (Cury and Shannon, 2004). The northern Benguela extends from the Angola-Benguela Front (between 14 and 16ºS) to Luderitz upwelling cell (Shannon and Nelson, 1996; Hutchings et al.

, 2009). The NB is influenced by tree oceanographic features: I) ABFZ which exhibits a latitudinal displacement southwards during the austral summer and drives the NB boundary to southwards to approximately 18ºS; II) Low oxygen waters off the continental shelf of Namibia, as a result of biological and hydrological processes, extending to depth of up to 100-150 m with the conditions persisting for approximately 90 km offshore; III) occurrence of upwelling cell on the southern extremities, which weakens during the late summer (Hutchings et al., 2009). The Luderitz (26 ºS), is the strongest upwelling cell (Shannon and Nelson, 1996), and is characterized by persistent and strong winds that persist throughout the year, elevated turbulence and high levels of offshore advection, considered to impact negatively the retention, concentration and enrichment of the first life stages of marine living resources (Beer, 2014).

In the NB, the upwelling is moderate in a narrow shelf and moderate to high eddy activity (Tim et al., 2015), and occurs farther offshore, westward up to 150-250 km (Shannon and Nelson, 1996). The upwelling shows weaker seasonal variation, and has its peak in austral autumn and spring (Veitch et al., 2010). In the northern parte of the ABFZ that extends north of Tômbwa until Namibe is considered to exhibit a perennial upwelling regime, which intensifies during the winter (Hutchings et al., 2009), while in the central region of the NB, from Tômbwa to Cunene River mouth, is associated with the ABFZ (Tim, 2014).The physical oceanography of the Angola subtropical system  The Angola Subtropical System of about 1650 km of coastline and a continental shelf of 51000 km2 with a width varying from 10 to 100 km, is characterised by two oceanographic regimes: the Angola Current with southward movement and the Benguela Current with northward migration, meeting at the Angola-Benguela Frontal Zone (ABFZ) (Shannon et al.

, 1985). The Angola Current forms the eastern section of a large Cyclonic Gyre in the Gulf of Guinea, and is influenced by input from Equatorial Current and the south Equatorial Current at approximately at 5ºS (Peterson and Sherman, 1991). It is a fast, narrow with a stable flow that reaches 250-300m depths and covers both the regions and the continental slop (Vas-Velho 2011). Generally, the Angola Current has a temperature and salinity greater than 24º and 36.4 psu respectively, of which water becomes colder and saline as it moves southwards (Lass at al. 2000).

The Angola Dome, a cyclonic eddy doming of a thermocline, centered near 10ºS and 9ºE, is another important feature of the Angola Subtropical System that happens only in the summer and which extension and width depends on the intensity and horizontal share of the southeasterly trade winds (Signarini et al., 1999). Ø  Small pelagic fish assemblages and distributionenAs in other parte of the BUS, in the Angola Subtropical System, environmental forces is believed to affect the distribution and abundance of marine living resources (Vaz-Velho, 2011), being evident in the pelagic species, resulting in seasonal, interannual and decadal-scale variability of their distribution, abundance and biological characteristics. Off Angolan coast, there has been a substantial change in the distribution of horse mackerel and sardinella species.

The distribution and availability to fisheries, of Sardinella spp. important to purse-seine catch, is influenced by either warm water intrusion, as well by the Congo River plume.  Sardinella aurita and S. maderensis are widely distributed in the Atlantic Ocean and Mediterranean Sea, displaying strong migratory patterns throughout their areas of occurrence. Their migratory pattern is mostly associated with areas of strong upwelling. Off the Angolan coast, these species are one of the most important commercial pelagic species and account for approximately 60% the landed fish resources. The area between Pointe Noire and the Congo River is thought to be the spawning areas for both species, with peak spawning in March-Abril. They make seasonal longshore migration, with an equatorward shift during the first part of the year, with the adults returning later in the year.

There are evidences that in the mid- 1960s occurred southward shift of both species, which was followed by an equatorward displacement during the early 1980s, coinciding with changes in the distribution of sardine off Namibia.     Ø  Biomass and Recruitment Most of the major fisheries resources of the BUS are shared between the bordering countries or migrate across national jurisdictional zones, including sardine, anchovy, horse mackerel and Sardinella spp. According to Shannon et la., (2006), the considerable climatic and environmental variability is the primary driving force of biomass change in the BUS, influencing some of the major stock fluctuations.  The biomass of small pelagic fish off Angola is estimated by annual hydroacustic surveys that have been conducted by the Norwegian research vessel “Dr Fridtjof Nansen” since 1985.

Up to date, the Biomass of Sardinella spp is considered to be at stable level, with an annual TAC of 150 000 tones. Ø  Fisheries and variability in abundance The fishing sector is important for both Namibia and Angola economy, contributing with 6.4 % and 3 to 5% respectively of their GDP (Vaz-Velho, 2011). Significant reduction in the most important resources of the NB occurred over the past decades.

Concerning to SPF, in the early 1960s, sardine was the most abundant SPF off Namibia. During 1967-1969, the catches were high, resulting in a decrease of sardine biomass, as a consequence, in 1970s, sardine was no longer the most abundant specie off Namibia, being replaced by cape horse mackerel (T. capensis). Sardine biomass increased again between 1986 and 1991.

According to Boyer, (2001), during 1993 and 1995, the two environmental anomalies (hypoxia and Benguela Niño) were pointed to cause changes in distribution of sardine, resulting in poor recruitment and catch rates, affecting as well, the distribution and abundance of other species such as anchovy, horse mackerel and sardinella spp.  Fisheries in Angola increased rapidly since the end of civil war in 2002. Round sardinella (S. aurita), flat sardinella (S.maderensis), Cunene horse mackerel (T.

trecae), cape horse mackerel (T. capensis), and South African sardine (S. sagax) are the main commercial species caught off Angolan coast, and they account for about 80% of the total fish catches (Vaz-Velho, 2011). Most Sardinella spp. occur and are caught to the north of the ABFZ, but most of the catch data for this resources are not reliable.

They are mostly caught by industrial fishery, but some times are caught by artesanal fishery.  


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