Rjm J Crawford

J Sydeman William

D B Tom

J A Thayer

R B Sherley

J Shannon

A M Mcinnes

A B Makhado

C Hagen

R W Furness

W J Sydeman

L J Shannon

T Carpenter-Kling

C Saraux

Food limitation of seabirds in the Benguela ecosystem and management of their prey base

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Introduction 2

This paper provides a brief review of food limitation of four Endangered (EN) seabirds that breed in the Benguela ecosystem, of the viability of seabird colonies and Allee effects, of forage and consumption thresholds and of potential management interventions that may enhance food availability. The locations of some of the system's important seabird colonies are shown in Figure 1.

Status of the Benguela's seabirds

Fifteen seabird species breed in the cool Benguela ecosystem, which extends from about Benguela in Angola to Woody Cape in South Africa, being bounded in the north and southeast by the warm Angola and Agulhas Currents, respectively (Figure 1). Seven of these are endemic to the ecosystem (Hockey et al. 2005). Of the endemic species, in terms of criteria of the International Union for Conservation of Nature (IUCN) four are EN (African Penguin Spheniscus demersus, Cape Gannet Morus capensis, Cape Cormorant Phalacrocorax capensis, Bank Cormorant P. neglectus), one is Vulnerable (VU, Damara Tern Sternula balaenarum), one is Near-Threatened (NT, Crowned Cormorant Microcarbo coronatus) and Hartlaub's Gull Larus hartlaubii is Least Concern (LC, IUCN 2020). The non-endemic Leach's Storm Petrel Hydrobates leucorous (or Oceanodroma leucorhoa) is VU, whereas the other seven non-endemics are LC (IUCN 2020). Although substantial numbers of Leach's Storm Petrel migrate from the Northern Hemisphere into the Benguela system [START_REF] Pollet | Migration routes and stopover areas of Leach's Storm Petrels Oceanodroma leucorhoa[END_REF], the breeding population of this species in South Africa is Critically Endangered (CR, Taylor et al. 2015). In South Africa small, isolated populations of Great White Pelican Pelecanus onocrotalus, Caspian Tern Hydroprogne caspia and Roseate Tern Sterna dougallii are regarded as regionally VU (Taylor et al. 2015). Leach's Storm Petrel and Roseate Tern do not breed In Namibia, where the Cape Gannet is considered CR [START_REF] Kemper | Cape Gannet Morus capensis[END_REF], the Great White Pelican and Caspian Tern VU (Simmons 2015a, b) and the Damara Tern NT [START_REF] Simmons | Damara Tern Sternula balaenarum[END_REF].

Importance and evidence of food limitation

For a seabird population to be self-sustaining, mortality from its mature component must be balanced by recruitment or immigration. Recruitment is influenced by age at first breeding, breeding participation (proportion of mature birds electing to breed), breeding frequency (number of clutches produced annually), breeding success (chicks fledged per clutch) and survival from fledging to breeding.

Insufficient food resources may negatively affect these demographic parameters leading to population decreases, as is described below for the Benguela's four EN seabird species, which all feed mainly on three forage resources that are heavily exploited by fisheries when these are readily available. African Penguin, Cape Gannet and Cape Cormorant feed preferentially on sardine Sardinops sagax and anchovy Engraulis encrasicolus (Hockey et al. 2005). In South Africa, the intensively fished West Coast rock lobster Jasus lalandii is an important prey of Bank Cormorant [START_REF] Dyer | Geographical and temporal variation in the diet of Bank Cormorants Phalacrocorax neglectus in South Africa[END_REF], whereas in Namibia the lightly-exploited but nutritionally-deficient bearded goby Sufflogobius birarbatus is one of its staple foods (Ludynia et al. 2010a). After the collapse of sardine in Namibia in the 1970s, bearded goby also replaced it as the dominant prey item for African Penguins breeding in Namibia (Ludynia et al. 2010b).

African Penguin

Large decreases of African Penguins at colonies between Lüderitz in Namibia and Dassen Island off west South Africa from the 1960s to the 1980s were recorded following the collapse of sardine stocks off Namibia and South Africa. North of Lüderitz, increases at Mercury and Ichaboe islands after the 1960s probably resulted from an increased local abundance of bearded goby [START_REF] Crawford | Pelagic fish and seabird interrelationships off the coasts of South West and South Africa[END_REF][START_REF] Shelton | Distribution, population size and conservation of the Jackass penguin Spheniscus demersus[END_REF][START_REF] Crawford | Partitioning of a goby resource amongst four avian predators and evidence for altered trophic flow in the pelagic community of an intense, perennial upwelling system[END_REF], 2001a). However, this did not prevent an overall decrease of 90% in penguins breeding in Namibia between 1956 and the early 2000s (Figure 2, Crawford 2007).

By contrast, an increase between the 1950s and 1970s and a later decrease in numbers of penguins at Dyer Island, southwest South Africa, coincided with an increase and subsequent fluctuations in anchovy abundance [START_REF] Crawford | Responses of African penguins to regime changes of sardine and anchovy in the Benguela system[END_REF]. From 1989-2009 numbers of penguins breeding along west South Africa were significantly correlated with the overall biomass of sardine and anchovy in South Africa, as also was the case from 1999-2009 in Algoa Bay (Figure 2, [START_REF] Crawford | Collapse of South Africa's penguins in the early 21 st century: a consideration of food availability[END_REF]. The formation of new penguin colonies at Stony Point and Boulders on South Africa's mainland and at Robben Island, and increases at these colonies and at Dassen Island, took place during a period of recovery of South Africa's sardine in the 1980s and 1990s and an increase in the biomass of anchovy at the start of the 21 st century. This led to an overall increase in the numbers of penguins breeding in west South Africa [START_REF] Underhill | Regionally coherent trends in colonies of African penguins Spheniscus demersus in the Western Cape, South Africa, 1987-2005[END_REF].

After 2004, large decreases in numbers of penguins breeding in west South Africa were associated with a shift to the south and east of adult anchovy and sardine and a collapse of sardine [START_REF] Crawford | Collapse of South Africa's penguins in the early 21 st century: a consideration of food availability[END_REF]. Concomitant with the altered distribution of prey there were decreases in penguins at all South African colonies north of Cape Town (the northernmost colony at Lambert's Bay became extinct in 2006; [START_REF] Crawford | African Penguin (Spheniscus demersus)[END_REF]. By contrast, in the south numbers increased or stabilized at Boulders and Stony Point and penguins attempted to form a new colony at De Hoop Nature Reserve [START_REF] Underhill | Regionally coherent trends in colonies of African penguins Spheniscus demersus in the Western Cape, South Africa, 1987-2005[END_REF], Crawford et al. 2011). Although trends in numbers of African Penguins at colonies are often regionally coherent [START_REF] Underhill | Regionally coherent trends in colonies of African penguins Spheniscus demersus in the Western Cape, South Africa, 1987-2005[END_REF], at Dyer Island, also in the south, penguins decreased in the 2000s. This may have resulted from heavy exploitation of sardine in its vicinity: 70,000 tonnes of sardine were caught within 30 km of Dyer Island in 2004 [START_REF] Ludynia | Processes influencing the population dynamics and conservation of African penguins on Dyer Island, South Africa[END_REF]) and the exploitation rate of sardine west of Cape Agulhas rose to 30-44% in 200230-44% in and from 200530-44% in -200730-44% in (Coetzee et al. 2008)). When the colony size at Dyer Island was > 3,500 pairs, numbers of penguins breeding there were negatively related to sardine catches made within 20 nautical miles of the island [START_REF] Ludynia | Processes influencing the population dynamics and conservation of African penguins on Dyer Island, South Africa[END_REF], suggesting an impact of catches on local food availability. Local or regional abundances or availability of sardine and anchovy have been related to numbers of African Penguins breeding [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF], Crawford et al. 2011[START_REF] Sherley | Influence of local and regional prey availability on breeding performance of African penguins Spheniscus demersus[END_REF], to adult and immature survival [START_REF] Crawford | Collapse of South Africa's penguins in the early 21 st century: a consideration of food availability[END_REF], 2019, Sherley et al. 2014[START_REF] Robinson | Quantifying the projected impact of the South African sardine fishery on the Robben Island penguin colony[END_REF], to age at first breeding (Whittington et al. 2005), to breeding participation (Crawford et al. 1999b[START_REF] Durant | Influence of feeding conditions on breeding of African penguins -importance of adequate local food supplies[END_REF], to breeding success (Adams et al. 1992[START_REF] Crawford | Responses by four seabirds to a fluctuating availability of Cape anchovy Engraulis capensis off South Africa[END_REF], Crawford et al. 1999b, 2006a[START_REF] Cury | Global seabird response to forage fish depletion -one-third for the birds[END_REF][START_REF] Sherley | Influence of local and regional prey availability on breeding performance of African penguins Spheniscus demersus[END_REF]) and to foraging performance [START_REF] Pichegru | Marine no-take zone rapidly benefits Endangered penguin[END_REF][START_REF] Campbell | Local forage fish abundance influences foraging effort and offspring condition in an endangered marine predator[END_REF], McInnes et al. 2019). Additionally, onset of breeding was probably delayed during a period of food scarcity [START_REF] Crawford | Responses by four seabirds to a fluctuating availability of Cape anchovy Engraulis capensis off South Africa[END_REF] and the chick fledging period was negatively correlated with prey abundance [START_REF] Sherley | Influence of local and regional prey availability on breeding performance of African penguins Spheniscus demersus[END_REF]. Delayed breeding and longer fledging periods may reduce the breeding frequency and cause abandonment of unfledged chicks when parents are constrained to leave colonies for pre-moult fattening [START_REF] Crawford | Bottom-up and top-down control of the Benguela ecosystem's seabirds[END_REF].

Cape Gannet

In Namibia, the Cape Gannet population decreased by 95% after the collapse of that country's sardine stock in the 1970s (Figure 2, [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF]. However, at the same time the numbers of gannets in South Africa increased. Trends in the proportions of forage fish (sardine and anchovy) and gannets found in Namibia and in South Africa were similar (Figure 3) suggesting an impact of food.

However, increases of gannets in South Africa did not offset losses in Namibia so that the overall abundance of Cape Gannets deceased (Crawford et al. 2007a).

In the 21 st century, the movement of Cape Gannets to the south and east continued with a decrease in numbers breeding off west South Africa and an increase in Algoa Bay, matching a shift in the distribution of their prey [START_REF] Crawford | A changing distribution of seabirds in South Africa -the possible impact of climate and its consequences[END_REF], Sherley et al. 2019). In the west, foraging effort of Cape Gannets increased and nest attendance decreased with reduced consumption of sardine and anchovy, and adult body condition was negatively impacted by increases in the dietary proportion of hake Merluccius sp. discarded by fisheries [START_REF] Cohen | Changes in prey availability impact foraging behaviour and fitness of Cape gannets over a decade[END_REF]. At Malgas Island, Cape Gannets had substantially reduced breeding success when they fed their chicks mainly low-quality fish discards [START_REF] Grémillet | A junk-food hypothesis for gannets feeding on fishery waste[END_REF]. Between 2011 and 2014 there was a net deficit in energy expenditure during foraging for most Cape Gannets tracked from Malgas Island [START_REF] Grémillet | Starving seabirds: unprofitable foraging and its fitness consequences in Cape gannets competing with fisheries in the Benguela upwelling ecosystem[END_REF].

Cape Cormorant

In Namibia, numbers of Cape Cormorants decreased by 62% after the collapse of sardine in the 1970s (Figure 2). It was a lesser decrease and occurred later than those of African Penguins and Cape Gannets, possibly owing to Cape Cormorants benefitting from increased breeding space at Ichaboe Island and making use of alternative prey in the form of bearded goby [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF], Crawford et al. 2007b[START_REF] Erasmus | Predatory species left stranded following the collapse of the sardine Sardinops sagax (Pappe, 1854) stock off the northern Benguela upwelling system: a review[END_REF]. Additionally artificial nesting platforms constructed in central Namibia provided breeding habitat for Cape Cormorants closer to the reduced range of the sardine [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF]. By contrast, gannets and most penguins in Namibia bred in the south and suffered food shortages as the sardine's range contracted northwards [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF]. Cape Cormorants colonised Ilha dos Tigres in southern Angola in the 2000s and > 16,000 pairs bred there in 2017 (Mendelsohn and Haraes 2018).

Unlike in Namibia, numbers of Cape Cormorants breeding in west South Africa decreased in the mid-1990s prior to recent decreases in that region of African Penguins and Cape Gannets (Crawford et al. 2007b). There were substantial mortalities of adult Cape Cormorants at several colonies in west South Africa between 1991 and 2006 caused by avian cholera Pasteurella multocida, outbreaks of which may be triggered by stressful events such as food limitation (Crawford et al. 1992a[START_REF] Ward | Coastal killers: causes of seabird mortality[END_REF][START_REF] Waller | Management of avian cholera Pasturella multocida outbreaks on Dyer Island, South Africa, 2002-2005[END_REF]. Its initial occurrence at Dassen Island may have been precipitated by a scarcity of forage fish during 1989 and 1990 (Crawford et al. 1992a). Conforming to the recent shift in the distribution of sardine and anchovy, Cape Cormorants decreased off northwest South Africa but remained stable in the south, where new colonies formed (including at Robben Island and Stony Point) and some others increased [START_REF] Crawford | Cape cormorants decrease, move east and adapt foraging strategies following eastward displacement of their main prey[END_REF]).

When food is scarce, as well as experiencing increases in adult mortality, Cape Cormorants, like some other cormorant species, often skip or abandon breeding or delay their first breeding attempt [START_REF] Berry | Physiological and behavioural ecology of the Cape cormorant Phalacrocorax capensis[END_REF], Crawford et al. 2001b, 2016[START_REF] Crawford | Responses by four seabirds to a fluctuating availability of Cape anchovy Engraulis capensis off South Africa[END_REF]. They may also suffer extensive breeding failure [START_REF] Duffy | Effects of the 1982-3 warm water event on the breeding of South African seabirds[END_REF], Crawford et al. 1992b). In November 2008, Cape Cormorants brooding small chicks expended significantly greater foraging effort at Malgas and Dassen islands than at Dyer Island farther south [START_REF] Hamann | A hard-knock life: the foraging ecology of Cape cormorants amidst shifting prey resources and industrial fishing pressure[END_REF]. During May and June 2014 Cape Cormorants north of Cape Town attempted to take bait from hand-lines used to fish for snoek Thyrsites atun, a behaviour not previously observed and that suggested poor food availability at that time [START_REF] Crawford | Cape cormorants decrease, move east and adapt foraging strategies following eastward displacement of their main prey[END_REF].

Bank Cormorant

In Namibia, Bank Cormorants decreased from 7,166 pairs in 1978-1980 to 3,735 pairs in 1995-1997; a severe reduction of bearded goby in central Namibia in 1994 was a probable cause of the decrease (Crawford et al. 1999a). In South Africa, Bank Cormorants decreased from 1,506 pairs in 1978-1980 to 846 pairs in 2010-2013 [START_REF] Crawford | A changing distribution of seabirds in South Africa -the possible impact of climate and its consequences[END_REF]. Total numbers breeding at 11 readily accessible localities between Lambert's Bay and Dyer Island fell from above 500 pairs during 1978-1987 to 350 pairs from 1995 to 2006. The most northern colony (Lambert's Bay) was extinct by 1999 and there were substantial decreases at the two largest colonies, Malgas and Dassen islands, which are north of Cape Town. There was fluctuating growth at Robben Island, near Cape Town, where birds were oiled by spills in 1994 (Apollo Sea) and 2001 (Treasure). Farther east numbers at two colonies increased. These trends are consistent with a reduced abundance of rock lobsters in the north and an expansion of this resource to the east [START_REF] Crawford | Divergent trends in bank cormorants Phalacrocorax neglectus breeding in South Africa's Western Cape consistent with a distributional shift of rock lobsters Jasus lalandii[END_REF]. As with other endangered species, fishing in the immediate vicinity of Malgas and Dassen islands may have reduced densities of lobsters below levels needed to sustain the larger colonies of Bank Cormorants. Where rock lobsters had not been severely depleted, Bank Cormorants showed a positive response to their local availability and modelling suggested that areas with no-take of lobsters at 20-30 km around Bank Cormorant colonies would benefit the conservation of this seabird [START_REF] Sherley | Defining ecologically-relevant scales for spatial protection using long-term data on an endangered seabird and local prey availability[END_REF].

Colony viability and Allee effects

Traditionally, the Benguela's four Endangered seabirds bred in large colonies and those three that feed mostly on sardine and anchovy have often foraged in large multi-species flocks (Hockey et al. 2005). However, as populations have fallen, breeding colonies have decreased in size and on occasion fragmented into smaller units (e.g. [START_REF] Cordes | Decrease of African Penguins at the Possession Island group, 1956-1995 -contrasting trends for colonial and solitary breeders[END_REF][START_REF] Crawford | Cape cormorants decrease, move east and adapt foraging strategies following eastward displacement of their main prey[END_REF], Sherley et al. 2019).

The probabilities of extinctions of different-sized colonies of African Penguins over 40 years were obtained from empirical observations on the performance of 41 discrete colonies in southern Africa from 1956-1996(Crawford et al. 2001a). Only one (< 4 %) of 28 colonies that in 1956 had ≤ 50 pairs was extant in 1996, compared to 26% of those having 251-1,000 pairs, 67% of those having 1,001-5,000 pairs and 100% of those with > 5,000 pairs (Figure 4). Whereas three of the 30 breeding colonies extant in 2004 held > 5,000 pairs and, in terms of these probabilities, had no likelihood of extinction within 40 years, by 2019 none of the 25 remaining colonies had > 5,000 pairs so that all had some chance of extinction during such a period. In 2019, fifteen colonies had < 250 pairs and hence a 96% chance of extinction by 2059 (Figure 4). In 2019, only seven colonies held > 1,000 pairs and had a 67% probability of surviving to 2059: Mercury Island in Namibia; Dassen, Robben, Dyer, St Croix and Bird (Algoa Bay) islands and Stony Point in South Africa.

Fragmented seabird populations may suffer from Allee effects, i.e. reduced fitness at low population size increasing their likelihood of extinction [START_REF] Ryan | African penguins Spheniscus demersus, bait balls and the Allee effect[END_REF]. African Penguins that feed in groups have a higher catch of prey per unit effort than solitary birds [START_REF] Mcinnes | Group foraging increases foraging efficiency in a piscivorous diver, the African penguin[END_REF]), but colonies may become too small for sufficient foraging groups to form [START_REF] Ryan | African penguins Spheniscus demersus, bait balls and the Allee effect[END_REF]. For example, in 2012 more penguins were documented foraging in a single flock of at least 158 birds [START_REF] Ryan | African penguins Spheniscus demersus, bait balls and the Allee effect[END_REF]) than were breeding in 2019 at 10 of the 25 presumed extant African Penguin colonies. For plunge-diving Cape Gannets, highlysynchronised prey pursuits, which are likely contingent on their ability to locate an adequate number of conspecifics at sea, benefitted from improved foraging efficiency when feeding on sardine schools [START_REF] Thiebault | How to capture fish in a school? Effect of successive predator attacks on seabird feeding success[END_REF]. A lower number of individuals could also decrease the role of colonies as information centres, or the possibility to use conspecifics as cues to locate prey (e.g. [START_REF] Thiebault | How to capture fish in a school? Effect of successive predator attacks on seabird feeding success[END_REF]. Again smaller colonies have a larger proportion of birds nesting at colony edges, where eggs and chicks are at a greater risk to predation (e.g. [START_REF] Cordes | Decrease of African Penguins at the Possession Island group, 1956-1995 -contrasting trends for colonial and solitary breeders[END_REF], and sex-biased mortality (e.g. Pichegru and Parsons 2014) may decrease productivity of monogamous breeders at small colonies. The higher risks of extinction for small colonies make it imperative to maintain colony sizes above thresholds at which Allee effects are manifest. Furthermore, small numbers of seabirds that have a late age at maturity may take substantial periods to recover, even with fishery closures (e.g. [START_REF] Robinson | Quantifying the projected impact of the South African sardine fishery on the Robben Island penguin colony[END_REF].

In 2010, Mercury Island held 72% of the global population of Bank Cormorants [START_REF] Roux | Birds to watch in Namibia: red, rare and endemic species[END_REF] and 73% of Namibia's African Penguins [START_REF] Crawford | African Penguin (Spheniscus demersus)[END_REF]. In 2018, c. 70% of the overall Cape Gannet population was at Bird Island, Algoa Bay at the eastern boundary of the Benguela ecosystem [START_REF] Sherley | The status and conservation of Cape Gannets Morus capensis[END_REF]). In the 2010s, 54% of South Africa's Cape Cormorants bred at Dyer Island [START_REF] Crawford | Cape cormorants decrease, move east and adapt foraging strategies following eastward displacement of their main prey[END_REF]. Such congregations of large proportions of a species at a single locality may offset Allee effects but render the species highly susceptible to local catastrophic events such as oil spills (e.g. [START_REF] Crawford | Initial impact of the Treasure oil spill on seabirds off western South Africa[END_REF], disease outbreaks (e.g. Waller and Underhill 2007), severe weather events (e.g. [START_REF] Randall | Rain-related breeding failures in Jackass Penguins[END_REF]) and reduced availability of resources.

Forage thresholds

Forage abundance thresholds

In a meta-analysis of long-term studies in seven marine ecosystems from around the globe, [START_REF] Cury | Global seabird response to forage fish depletion -one-third for the birds[END_REF] demonstrated key thresholds in prey (fish and krill) abundance, below which seabirds 10 dependent on that food type suffered reduced and more variable breeding success. The threshold was equal to the long-term average biomass of prey and equivalent to one-third of the maximum observed prey biomass. Similar relationships were established at the species level, namely for 13 of the 14 seabirds studied, including African Penguin and Cape Gannet from the Benguela ecosystem. The socalled "1/3 for the birds" rule provides a benchmark for management of forage fish fisheries at a level that would sustain seabird productivity over the long-term [START_REF] Cury | Global seabird response to forage fish depletion -one-third for the birds[END_REF].

In a related study, [START_REF] Robinson | Quantifying the projected impact of the South African sardine fishery on the Robben Island penguin colony[END_REF] showed that annual mortality of adult African Penguins at Robben Island increased markedly when the biomass of sardine aged 1 y or older off west South Africa fell below 25% of its maximum value. The lower forage threshold observed for adult mortality (25%) than for breeding success (33%) confirmed the theoretical prediction of [START_REF] Cairns | Seabirds as indicators of marine food supplies[END_REF] that decreases in forage abundance would influence seabird breeding success ahead of survival. When data for African Penguins at Dassen and Robben islands were grouped, a generalised additive model (GAM) showed that adult survival decreased when standardised (i.e. centred and scaled) sardine abundance off west South Africa fell below a threshold of zero (Figure 5).

It is noteworthy that off west South Africa, Cape Gannets were better able to buffer effects of reduced prey abundance than African Penguins [START_REF] Distiller | Factors affecting adult survival and inter-colony movement at the three South African colonies of Cape Gannet[END_REF], Sherley et al. 2014[START_REF] Robinson | Quantifying the projected impact of the South African sardine fishery on the Robben Island penguin colony[END_REF]. After an eastward displacement of the main forage resources and the collapse of sardine [START_REF] Coetzee | Has the fishery contributed to a major shift in the distribution of South African sardine?[END_REF], adult gannets, due to their movement capabilities, were able to feed on alternative food, such as saury Scomberesox saury and hake offal [START_REF] Grémillet | A junk-food hypothesis for gannets feeding on fishery waste[END_REF], 2019, Crawford et al. 2014, 2019). Consequently, their survival was unrelated to standardised estimates of the overall abundance of sardine and anchovy (Figure 5). [START_REF] Saraux | Seabird-induced natural mortality of forage fish varies with fish abundance: evidence from 5 ecosystems[END_REF] investigated thresholds for the consumption of forage fish stocks by seabirds in five marine ecosystems: off Norway, South Africa, Peru, in the Baltic Sea (Sweden) and at Shetland (Scotland). In each of these systems, the predation pressure, estimated as the proportion of a forage fish stock consumed by seabirds, was generally small (median = 1% of biomass) but increased sharply when prey biomass decreased below a threshold of 15 to 18% of its maximum recorded value. A threshold of 18% was considered a limit not to be reached in order to avoid a sharp rise in the natural mortality rate of forage fish resources, and below which extra cautious management of fisheries would be required [START_REF] Saraux | Seabird-induced natural mortality of forage fish varies with fish abundance: evidence from 5 ecosystems[END_REF]. Similarly, [START_REF] Essington | Fishing amplifies forage fish population collapses[END_REF] advised that a risk-based management scheme that reduces fishing when populations become scarce would protect both forage fish and their predators from collapse, with little effect on long-term average catches.

Forage consumption thresholds

Other Forage Considerations

Forage quality

Condition of prey may influence its ability to sustain predator populations in addition to its abundance (e.g. [START_REF] Grémillet | A junk-food hypothesis for gannets feeding on fishery waste[END_REF]. For example, poor food quality likely caused unprecedented breeding failures at many seabird colonies on the east coast of Great Britain in 2004 [START_REF] Wanless | Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea[END_REF], decreased mass at fledging of Common Guillemots (Murres) Uria aalge in the Baltic Sea and brought about breeding failures and mass mortality of this species in the Northeast Pacific in 2015-2016 [START_REF] Osterblom | Fish, seabirds and trophic cascades in the Baltic Sea[END_REF][START_REF] Piatt | Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016[END_REF]. In South Africa, the condition of sardine deteriorated in the 2000s [START_REF] Ndjaula | Establishing a baseline for evaluating changes in body condition and population dynamics of sardine (Sardinops sagax) in the southern Benguela ecosystem[END_REF], possibly contributing to some of the seabird population decreases. As also mentioned above, reliance on fish offal as a food source reduced Cape Gannet chick survival [START_REF] Grémillet | A junk-food hypothesis for gannets feeding on fishery waste[END_REF].

Fisheries mortality

In addition to contributing to collapses of forage resources (e.g. [START_REF] Essington | Fishing amplifies forage fish population collapses[END_REF], fishing may cause localised depletion of prey; as such, the fisheries mortality rate (F) can be employed as another management threshold. For example, the performance of three species of Pygoscelis penguins breeding near the Antarctic Peninsula was reduced when local harvest rates of Antarctic krill Euphausia superba were ≥ 10% of the estimated biomass [START_REF] Watters | Long-term observations from Antarctica demonstrate that mismatched scales of fisheries management and predator-prey interaction lead to erroneous conclusions about precaution[END_REF]. By comparison, the exploitation rate of South Africa's sardine west of Cape Agulhas increased substantially after 1999 and reached 44% in 2006 [START_REF] Coetzee | Has the fishery contributed to a major shift in the distribution of South African sardine?[END_REF]. Spatially explicit thresholds in fishing mortality need to be carefully defined to assist in management of fish stocks so as to support viable seabird populations in the Benguela system.

Forage availability

It is not only the absolute abundance of prey but also its availability that impacts energy acquisition, demography and population trends of seabirds. For example, [START_REF] Crawford | Food habits of an endangered seabird indicate recent poor availability of abundant forage resources[END_REF] used long-term information on the diet of Cape Gannets off west South Africa to derive an index of the availability of anchovy and sardine per unit biomass to seabirds in that region, terming it a Forage Availability Index (FAI). The study demonstrated a substantial decrease in the availability of anchovy and sardine to seabirds in the 2000s compared to the 1990s. Breeding numbers of Cape Gannets and Cape Cormorants and survival of adult African Penguins at both Dassen and Robben islands were significantly related to the FAI. For gannets, the numbers breeding increased when the FAI, which increases as anchovy and sardine contribute more to the diet, was > c. -1 and for cormorants when it was > c. 1. The higher threshold for Cape Cormorants than Cape Gannets at which numbers breeding were predicted to increase probably resulted from the fact that, unlike Cape Gannets but similarly to African Penguins, Cape Cormorants are mostly unable to access alternative food such as saury and hake offal (Crawford et al. 2019). Notably, frequent aggregations of anchovy close to the seabed were thought to have reduced safe ecological limits (https://www.cbd.int/convention/text/default.shtml). In South Africa, the Marine Living Resources Act of 1988 attempts to provide legislative support for the EAF but is in urgent need of updating and further amendment better to achieve this [START_REF] Cochrane | An evaluation of the Marine Living Resources Act and supporting legal instruments as a framework for implementation of an ecosystem approach to fisheries in South Africa[END_REF].

One tool available to manage fisheries so as to avoid harmful impacts on associated or dependent species (ADS) is marine spatial planning, for example the implementation of fishing closures around important seabird colonies (e.g. [START_REF] Ludynia | The Namibian Islands' Marine Protected Area: using seabird tracking data to define boundaries and assess their adequacy[END_REF][START_REF] Sherley | Bottom-up effects of a no-take zone on endangered penguin demographics[END_REF], 2018). In northeast Scotland, Black-legged Kittiwakes Rissa tridactyla benefitted from closure of fishing for sandeels Ammodytes marinus, an important prey for kittiwakes, around breeding colonies [START_REF] Daunt | The impact of the sandeel fishery closure on seabird food consumption, distribution, and productivity in the northwestern North Sea[END_REF][START_REF] Furness | Sandeel stocks and seabirds in the North Sea[END_REF]).

In the Californian upwelling ecosystem off west North America, a precautionary ecosystem approach that avoids localised depletion of forage resources (including anchovy and sardine) near predator concentrations is deemed necessary. In 1983, nearshore (within 3 to 6 km of the coast) fishing for anchovy was prohibited, the main objectives being to protect pre-recruit anchovy, live bait and recreational fisheries, and predator forage (Pacific Fisheries Management Council 1983, Thayer andSydeman 2020). At the time, the anchovy-dependent Brown Pelican Pelecanus occidentalis was listed as Federally Endangered in USA [START_REF] Anderson | Brown Pelicans: influence of food supply on reproduction[END_REF]). In the Humboldt upwelling ecosystem off west South America, fishing for Peruvian anchoveta close to a Peruvian Booby colony increased the birds' foraging effort. The more the fishery reduced the quantity of anchoveta in the area, the farther the breeding boobies needed to forage from the colony to find food [START_REF] Bertrand | Local depletion by a fishery can affect seabird foraging[END_REF]). In the Benguela system, in which similarly to the California and Humboldt systems sardine and anchovy are key forage resources, short-term fishery closures around African Penguin colonies, even though not matched to the late age at recruitment and high mate and site fidelity of the penguins [START_REF] Crawford | African Penguin (Spheniscus demersus)[END_REF], have increased breeding productivity and deceased parental foraging costs [START_REF] Pichegru | Marine no-take zone rapidly benefits Endangered penguin[END_REF][START_REF] Sherley | Bottom-up effects of a no-take zone on endangered penguin demographics[END_REF], 2018, Sydeman et al. 2021). and implementation of ecosystem thresholds, below which fishing would be prohibited. Ecosystem thresholds have already been widely applied to minimise by-catch mortality of ADS in fisheries (e.g. [START_REF] Rollinson | Patterns and trends in seabird bycatch in the pelagic longline fishery off South Africa[END_REF][START_REF] Rocha | Reduction in seabird mortality in Namibian fisheries following the introduction of bycatch regulation[END_REF] and are increasingly proposed as means to ensure sufficient quantities of prey for predators, such as seabirds (e.g. [START_REF] Cury | Global seabird response to forage fish depletion -one-third for the birds[END_REF][START_REF] Smith | Impacts of fishing low-trophic level species on marine ecosystems[END_REF][START_REF] Sydeman | Best practices for assessing forage fish fisheries -seabird resource competition[END_REF][START_REF] Hill | Reference points for predators will progress ecosystem-based management of fisheries[END_REF]). In the Californian upwelling ecosystem a harvest rule disallows fishing of sardine when its biomass is below 150,000 metric tonnes (Pacific Fisheries Management Council 2003, Thayer andSydeman 2020).

A third mechanism to achieve adequate food for seabirds is to offset mismatches in the distributions of the breeding localities and the prey of seabirds through establishment of colonies nearer to the food supply. Guano platforms in Namibia served this purpose for Cape Cormorants [START_REF] Crawford | Food, fishing and seabirds in the Benguela upwelling system[END_REF]) and an attempt to establish a new African Penguin colony in South Africa closer to the present distributions of sardine and anchovy has been initiated (BirdLife South Africa 2016).

Recommendations from the 2020 AEWA Benguela Current Forage Fish Workshop

In November 2020, a Benguela Current Forage Fish (BCFF) Workshop, organized by the African-Eurasian Migratory Waterbird Agreement (AEWA), in collaboration with the Benguela Current Convention (BCC) and BirdLife South Africa, recommended actions to be undertaken as a matter of urgency under the auspices of BCC, AEWA and the AEWA Benguela Coastal Seabird International Working Group, as well as by the national governments of Angola, Namibia and South Africa. These included:

 developing tools to increase the availability of sufficient forage [fish] for threatened endemic Benguela seabird species, such as setting ecosystem thresholds (i.e. sizes of forage resource populations below which a range of precautionary measures relating to fishing would be implemented at various spatial scales) and closing key foraging areas to fishing, adjacent to major seabird colonies;  ensuring the existence or creation of suitable seabird breeding habitat within the contracted or altered distributions of forage fish species to partially alleviate the impact of an altered distribution of prey on affected seabird species;

 and facilitating and prioritising the recovery of seabird colonies to sufficient sizes to minimise known and potential Allee effects, thus reducing the probability of colony extinctions (AEWA 2020).

Conclusion

In conclusion, it is apparent that food limitation has been a major driver of adverse trends in the population sizes and conservation status of four Benguela seabirds that compete with fisheries for food. Hence it will be important to manage the impact of fisheries on the availability of prey to these seabirds, including through the use of measures that were successfully applied elsewhere or that have empirical support for use in the Benguela ecosystem.

Acknowledgements

We are grateful to F Dakwa for drawing Figure 1, to W Froneman and a second reviewer for constructive comments on a draft manuscript, and to all persons and organisations who contributed to collecting and analysing data used in this paper. The paper is an output of the BCC's marine top predator working group (BECUMATOP). Estimates of survival were from [START_REF] Sherley | Age-specific survival and movement among major African penguin Spheniscus demersus colonies[END_REF] for African Penguins and [START_REF] Distiller | Factors affecting adult survival and inter-colony movement at the three South African colonies of Cape Gannet[END_REF] for Cape Gannets. Estimates of prey abundance were updated from [START_REF] Cury | Global seabird response to forage fish depletion -one-third for the birds[END_REF]. The prediction (and 95% confidence interval) of the GAM is indicated with the black curve (and grey polygon) for African

Penguins. The vertical dashed line represents the threshold below which adult survival decreased markedly with decreasing sardine abundance. For Cape Gannets, no significant relationship was found between adult survival and prey (sum of anchovy and sardine) abundance.

Figure 1 .Figure 2 .

 12 Figure 1. A map of the Benguela Current ecosystem showing locations of some of the region's important

Figure 3 .

 3 Figure 3. Trends in the proportions of the Benguela ecosystem's sardine and anchovy and Cape Gannets

Figure 4 .Figure 5 .

 45 Figure 4. Top: numbers of African Penguin colonies of different sizes in 2004 (left) and 2019 (right).

Whittington, P[A], Klages N[TW], Crawford R[JM], Wolfaardt A[C], Kemper J. 2005. Age at first breeding of the African Penguin. Ostrich 76: 14-20.

Sardine & anchovyAfrican Penguin

Sardine & anchovyCape gannet

allowable catch (TAC) of anchovy in recent years (DAFF 2016).

The importance of prey depth was highlighted in a modelling study from the Humboldt upwelling system off western South America, where it primarily determined foraging success of Peruvian Boobies Sula variegata and Guanay Cormorants P. bougainvilliorum, which feed mainly on Peruvian anchoveta Engraulis ringens [START_REF] Boyd | Effects of variation in the abundance and distribution of prey on the foraging success of central place foragers[END_REF]. Peruvian Boobies and Guanay Cormorants are the ecological equivalents in that system of Cape Gannets and Cape Cormorants in the Benguela system (Crawford et al. 2006b).

African Penguins and other diving piscivores may herd prey shoals upwards, thereby facilitating their availability to surface-feeding predators (e.g. McInnes and Pistorius 2019). Hence their loss will influence ecosystem functioning.

Possible interventions to enhance food availability

Various international agreements require participating parties to implement an ecosystem-based approach to fisheries management (or ecosystem approach to fisheries, EAF). For example, the Code of Conduct for Responsible Fisheries of the United Nations' Food and Agriculture Organisation, adopted in 1995, stated that Management measures should not only ensure the conservation of target species but also of species belonging to the same ecosystem or associated with or dependent upon the target species (http://www.fao.org/3/v9878e/v9878e00.htm). The sixth Aichi Target of the Convention on Biological Diversity's Strategic Plan for Biodiversity 2011-2020 reads: By 2020 all fish and invertebrate stocks and aquatic plants are managed and harvested sustainably, legally and applying ecosystem based approaches, so that overfishing is avoided, recovery plans and measures are in place for all depleted species, fisheries have no significant adverse impacts on threatened species and vulnerable ecosystems and the impacts of fisheries on stocks, species and ecosystems are within